Advances in Parasitology Volume 10

Advances in PARASITOLOGY

V O L U M E 10

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Advances in

PARASITOLOGY Edited by

BEN DAWES Professor Emeritus, University of London

V O L U M E 10

1972

ACADEMIC PRESS London and New York

ACADEMIC PRESS INC. (LONDON) LTD. 24/28 Oval Road, London NWl United States Edition published by ACADEMIC PRESS INC. 111 Fifth Avenue New York, New York 10003

Copyright @ 1972 by ACADEMIC PRESS INC. (LONDON) LTD.

AII Rights Reserved No part of this book may be reproduced in any form by photostat, microfilm, or any other means, without written permission from the publishers Library of Congress Catalog Card Number: 62-22124 ISBN: 0-12-03 1710-9

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CONTRIBUTORS TO VOLUME 10 JOHNR. BAKER,Molten0 Institute, University of Cambridge, England (p. 1) GORDON F. BENNETT,Department of Biology, Memorial University of Newfoundland, St. John’s, Newfoundland, Canada (p. 1)

GLENW. CLARK, Department of Biological Sciences, Central Washington State College, Ellensburg, Washington, U.S.A. (p. 1)

ALEXANDER FLETCHER, Department of Tropical Medicine, Liverpool School of Tropical Medicine, Liverpool, England (pp. 31 and 49) DONALDHEYNEMAN, Hooper Foundation, University of California, San Francisco, California 94122, U.S.A. (p. 191)

LAIRD,Department of Biology, Memorial University of Newfoundland, St. John’s, Newfoundland, Canada (p. 1)

MARSHALL

*DONALD L. LEE,Houghton Poultry Research Station, Houghton, Huntingdon, England (p. 347)

HOK-KAN LIM, Hooper Foundation, University of California, San Francisco, California 94122, U.S.A. (p. 191) Department of Tropical Medicine, Liverpool School of Tropical Medicine, Liverpool, England (pp. 3 1 and 49)

BRIAN MAEGRAITH,

ZBIGNIEW PAWLOWSKI, Clinic of Parasitic Diseases, Przybyszewskiego 49, Poznan, Poland (p. 269) C. PEARSON, Department of Parasitology, University of Queensland, St. Lucia, Brisbane 4067, Queensland, Australia (p. 153)

JOHN

tKLAus ROHDE,Department of Parasitology, University of Queensland, St. Lucia, Brisbane 4067, Australia (p. 78)

MYRONG. Scnurrz, Center for Disease Control, U S . Department of Health, Education and Welfare, Atlanta, Georgia, U.S.A. (p. 269)

* Author in the section “Short Review” Present address: Department of Pure and Applied Zoology, University of Leeds, Leeds, England. t Present address: Department of Zoology, University of Khartoum, Sudan.

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PREFACE At the end of a decade and with ten volumes of Advances in Parasitology published I may be permitted to make an appraisal of a series of books which, because of a regular annual addition, has been regarded wrongly in some biological bibliographies as a scientific journal. Now that Volume 10 has appeared, 68 contributors have produced 57 original reviews and (since 1968) 15 short updated reviews, a vast summation of modern biological information and ideas in the field of parasitology. Thirty-one contributors lived in Great Britain, nine in Australia, ten in the U.S.A., six in Canada, three in Brazil, two each in Czechoslovakia, Poland, South Africa and Japan, and one in Israel. At my request, these writers found the time to record their thoughts and research experiences in well documented reviews. This may have cost innumerable man-hours, as have my editorial duties, but the benefit gained by stimulating teachers and researchers to greater effort in parasitology could hardly be reckoned in such units. Sixteen reviews deal with Protozoa, 13 with Trematoda, five with Cestoda and Acanthocephala, 12 with Nematoda, five with “helminths” and six with various parasitological topics. In the entire sequence of reviews, those on the Protozoa are concerned with avian and mammalian malaria, Chagas’ disease, coccidiosis, entamoebiasis, leishmaniasis, toxoplasmosis and trypanosomiasis. Trematode reviews are linked similarly with clonorchiasis, fascioliasis, paragonimiasis, paraimphistomiasis and schistosomiasis, cestode reviews with cysticercosis, echinococcosis and taeniasis, nematode reviews with ancylostomiasis, dracontiasis, filariasis, onchocercosis, parasitic bronchitis and trichiniasis. In vitro and in vivo culture of Protozoa come into the picture, and also similar methods of handling schistosomes and other trematodes and cestodes. There are reviews about snail vectors of trematodes and their control, about small but significant groups such as Aspidogastrea and Acanthocephala, about the evolution of parasites and their hosts, and about dynamic parasitic equilibrium in nematodes. There are reviews on larval Monogenea, on the life history sequence of digenetic trematodes and on intra-molluscan and intertrematode antagonism. There are reviews on parasitism and symbiosis in Turbellaria, on tissue reactions in the hosts of nematodes and on anthelmintic treatment and its results. Electronmicroscopy often comes into the picture and biochemistry plays some part in reviews. Much groundwork has been covered but it must be extended and many lacunae remain to be filled in. However, it is my hope to achieve much of this during another decade, if health permits. In the present volume, John R. Baker, Gordon F. Bennett, Glen Clark and Marshall Laird deal with what were once considered to be protozoan parasites of doubtful status and are here termed avian blood coccidians. They make a bold attempt to unravel tangled taxonomic confusion regarding two distinct groups of blood-dwelling stages of coccidia: (1) small non-pigmented nucleophilic parasites of mononuclear cells in the viscera and peripheral circulation; and (2) typical adeleine haemogregarines such as parasitize the vii

...

Vlll

PREFACE

blood cells of vertebrates during the course of the life cycle. Publications on avian blood coccidians of both groups of parasites are listed chronologically in Table I and a check-list of avian hosts of both groups of parasites is given in Table 11.These parasites are considered in separate sections as atoxoplasms and adeleine haemogregarines. It is unnecessary here to follow the detailed discussions of this team of professional protozoologists, who also give in Table I11 a classified host-list indicating atoxoplasm materials in thin Giemsastained blood films which are available for study in the WHO International Reference Centre for Avian Malaria Parasites at the Memorial University of Newfoundland. That there has been much confusion about the taxonomic status of these enigmatical blood parasites of birds is evident to the reader and the summarized information presented provides, in the words of the authors, “a fascinating basis for speculation”, and also “suggests hypotheses meriting early testing” by controlled experimentation to determine the true nature of atoxoplasms, and whether or not all atoxoplasms belong to the genus Zsospora and belong to one or more than one widespread species. Another point of wonderment is whether or not the few records of adeleine haemogregarines from birds represent simply accidental infection with parasites of reptiles which share the avian host environment. Alexander Fletcher and Brian Maegraith have not attempted to write a comprehensive review of literature on the metabolism of the malaria parasite but instead discuss some considerations and some current resarch trends which seem to advance our knowledge of fundamental biochemical processes which occur in parasites and are involved in the host-parasite relationship. After making some general considerations about the hazards presented by most types of cell preparation, they focus attention on the pentose phosphate pathway (PPP), for which the malaria parasite could have an absolute requirement, because it is probably the principal pathway for the production of pentose sugars necessary for nucleic acid synthesis. There is now evidence that most of the malaria parasites studied up to the present are dependent on the glucose-6-phosphate dehydrogenase (G-CPD), the initial enzyme of the PPP, the parasites being unlikely to thrive in enzyme-deficient cells and thus unable to produce an overwhelming infection. Further metabolism remains enigmatical, but current trends in research with mammalian species are discussed. Other topics considered are carbon dioxide fixation by malaria parasites, aerobic mechanisms, and the metabolism of chloroquine-resistant malaria parasites. These writers then turn to consider the metabolism of the host during infection, namely biological changes in erythrocytes, the effects of acute infection on host-tissue metabolism and host lipid metabolism. Such studies are enabling some advances to be made in our understanding of the pathological process involved in malaria. In another review Brian Maegraith and Alexander Fletcher concern themselves with the pathogenesis of malaria and they commence by indicating that the hypothesis of the physiopathological pattern of malaria is essentially inflammatory and non-specific in nature has long been upheld and is substantially correct. Research has been applied mainly on the effects of malaria infection on vascular membranes and vasomotor mechanisms of the host

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ix

and on the links between the parasite in its erythrocytic environment and the host. Two features are examined: the pathophysiology of malaria as an “inflammation”, and the possible initiating and maintaining factors involved. Attention is drawn to local and general responses in malaria which are similar to those which occur in inflammation and are demonstrable in bacterial infections and in malaria, babesiasis and other protozoan infections. Changes in endothelial permeability in malaria are next considered at some length, followed by statements on vasomotor changes in malaria in the hepatic, renal and intestinal circulations, which have been specially studied at the Liverpool School of Tropical Medicine. The kinin complex and other pharmacologically active agents are discussed fully, and it is shown that the kinin complex plays a significant part in disturbances that develop in permeable membranes, and is concerned with physiological change and resultant ultimate structural patterns. Another topic discussed is intravascular coagulation in malaria, the importance of which remains to be resolved in future research, one interesting region of which is the possible relationship between the peptide-peptidase which has been demonstrated in the kinin complex and the peptidase reactions involved in coagulation. Other topics discussed are anoxic anoxia (asphyxia), cytotoxic factors, and particularly mitochondria1 respiration inhibitors, and the physiological chain reaction which is set up and then leads to local or general disturbances that may be reversible but in time may become irreversible, leading to tissue death and the appearance of characteristic patterns of pathology. It is deemed helpful in visualizing the effects of a developing plasmodia1 infection to have this simple concept of initiating factors setting off a chain reaction of interlinked and interacting pathophysiological processes which may eventually involve changes in the local and general circulation of the blood, membrane permeability, hormone balance, and perhaps other as yet undisclosed effects. Klaus Rohde has not spared himself in writing the long review on the Aspidogastrea, especially Multicotyle purvisi Dawes, 1941. His researches on this trematode have occupied him throughout the last decade and it is noteworthy that we now know more about M . purvisi than we do about any other single aspidogastrid species. None of this research was completed when in 1961 I visited Kuala Lumpur as Examiner to the University of Malaya, and the review is of special interest to me because I described and proposed the erection of the new species and genus more than 30 years ago (Parasitology 33 (1 949, 300-3 15) from two well-preserved specimens collected on 25 July, 1932 from the river turtle Siebenrockiella crassicollis at Alor Star (north of Penang) by Mr G. B. Purvis, F.R.C.V.S., who was then serving as District Government Veterinary Surgeon in Malaya. I hasten to add that Klaus Rohde has given the name of this trematode fully not out of deference to any wish of mine but solely because of what I will call his teutonic insistence on precise delineation, and I am delighted to mention this record on the account of Mr G . B. Purvis. The review is divided into an introduction and eight other parts, which are subdivided. The introduction draws attention to the fact that the Aspidogastrea is the smallest of the three groups of Trematoda but of great interest because it shows a combination of the characters of Monogenea

X

PREFACE

and Digenea and contains forms ill-adapted to a parasitic mode of life and likely therefore to throw some light on the origin of parasitism in the flatworms. One section deals with general characters and leads on to another section giving a very detailed account of adult structure under the headings of tegument, digestive tract, protonephridial, genital and nervous systems, receptors and details of the characteristic ventral adhesive disc occupying most of the ventral part of the body. Rohde prefers to call the outermost layer of the body the “tegument”, which other writers designate by other names; the essential point is that it is not a hard resistant cuticle as once supposed but a cytoplasmic layer of much greater complexity, as revealed by electron-microscopy. It contains mitochondria and ovoid bodies, in some areas vacuoles and lamellated bodies, and the surface membrane forms elevations between which there is a mucoid layer of variable thickness. In some areas rib-like elevations of the surface support a thick mucoid layer consisting of a reticulum of fibres with electron dense bodies of various sizes. This “tegument” is syncytial, and apparently it is not formed by fusion of epithelial cells in M . purvisi but originates in its definitive form. Other organs of the adult-digestive tract, protonephridial, genital and nervous systemshave their structures elucidated with the help of the electron-microscope, and the details of the nervous system are revealed in their exquisite complexity. The sensory receptors are more complex and varied than has generally been supposed, and much more numerous. The structure of the free-living larva is described in the same thorough manner, in terms relating to general structure, tegument and ciliated tufts, glands and caudal appendage, digestive protonephridial and nervous systems, and sense receptors. As far as possible the details are integrated with what is known about other aspidogastrid larvae. Development is then considered in terms of the egg, cleavage and larval development, hatching, development of the parasitic stage and relative (allometric) growth. The portrayal of changing relative size in various organs during growth approaches and surpasses what I first attempted more than 30 years ago for Styphlodora elegans Dawes, 1941 (Parasitology, 33 (1941), 445-458) and more recently for Fasciola hepatica (J. Helminthology 36 (1962), 11-38). The biology of aspidogastrids is closely considered in respect of life span, behaviour and infectivity of free larvae, route of invasion in the mollusc, localization and sexual maturation in the intermediate host, infectivity in the vertebrate host and growth, localization in this host and specificity of infection, with some information on the survival of adult forms outside this host. Rohde then discussed the phylogenetic position of the Aspidogastrea, which have some archaic features. Reasons are given for placing aspidogastrids in a separate group, and for believing that they are closely related to the Digenea. An attempt is made to derive the digenetic life cycle from that of the aspidogastrid and to discuss some unresolved problems. It is likely that many parasitologists will agree that Rohde’s review greatly enhances our knowledge of trematode structure development and biology. John C . Pearson has chosen to write on a phylogeny of life cycle patterns of digenetic trematodes, a theme that has long invited speculation. After an Introduction giving details of earlier ideas and some recent views, this writer

PREFACE

xi

details what he considers to be the “singular features” of digenetic life cycles, adding what he believes any scheme of phylogeny should take into consideration, namely, alternation of generations, alternation of molluscan and piscine hosts, the existence of a tailed larva (the cercariae) and methods of transfer that include penetration of the free-swimming miracidium into some snail, the escape from the snail in many instances, and the ingestion of a cercarial or metacercarial stage by a definitive host, except in schistosomes. He is generous in his comments about these minimal considerations before passing on to his detailed scheme. After considering the adoption of parasitism and a one-host cycle, he goes on to deal in turn with the origin of an alternation of generations, the addition of a vertebrate host and a redial generation in the parasite, the addition of a metacercarial stage, the acquisition of a second intermediate host and the three-host cycle and its modifications. He then notes phylogenetic implications and summarizes his findings. In order to explain the “ubiquity” of the cercaria he postulates that the present first intermediate host was the original host of the proto-digenean and that escape from this host is primitive. To explain the occurrence in many life cycles of a free-swimming miracidium he further postulates that the proto-digenean was an ectoparasite of the molluscan host. Assuming that it became a visceral parasite that escaped from the host as an adult in order to lay its eggs, he indicates that the known life cycles of contemporary Digenea may be interpreted in an order of acquisition of hosts as follows: vertebrate definitive (two-host cycle) and invertebrate second intermediate (three-host cycle). More than this it is not necessary to state here, except that the three-host cycle is the commoner and has arisen several times over from two-host cycles, and has been secondarily reduced in some groups of the Digenea through loss of the definitive host or of the second intermediate host, or possibly the loss of both hosts. There are no simple cycles amongst the Digenea and speculation is hypothetical but this thoughtful effort by John Pearson will help us to classify the multifarious life cycles and also point the way to further study in other and future researches. The review by Hok-Kan Lim and Donald Heyneman is concerned with intramolluscan inter-trematode antagonism. It has been known for some years that echinostome larvae within a snail host may inhibit and disrupt or prevent the development of other trematode larvae but only recently was this phenomenon demonstrated in laboratory experiments carried out in San Francisco and Kuala Lumpur, Malaya, basically to study single or double trematode infections within a molluscan host. After an Introduction, Lim and Heyneman give much information about the maintenance of certain snails and trematodes, mainly the snail Biomphalaria glabrata and the trematodes Paryphostomum segregatum (an echinostome) maintained as adults in a Brazilian black vulture (uruba) and Schistosoma mansoni, maintained as adults in the golden hamster. The term direct antagonism was used to denote predatory or physical activities by rediae on other trematode larvae within the snail. By study and analysis it was hoped to recognize, evaluate and “quantitate” the conditions that predispose one trematode to dominate another trematode within the same snail. Various trematode interaction

xii

PREFACE

patterns are noted-rediae dominating sporocysts, predatory activity of rediae which feed upon sporocysts but may devour other larvae, e.g. mother rediae devouring daughter rediae or young cercariae. Redial morphology is considered carefully, the efficiency of predation and a triggering mechanism as well. Non-predatory effects are considered for both rediae and sporocysts as inhibitory or degenerative changes and possible mechanisms such as snail immunity, direct toxicity, and competition for nutrients or oxygen. An important section of the review is concerned with the parameters of intramolluscan inter-trematode antagonism. In the quest for a suitable antagonist against Schistosoma mansoni six species of echinostomes were tested in the laboratory, and Paryphostomum segregatum was the most effective. Consequently, much research was carried out on antagonism using the snail Biomphalaria glabrata, the trematode Schistosoma mansoni (target) and the echinostome Paryphostomum segregatum (predator). This model gave examples of miracidial penetration in either trematode species superimposed on the other species, the establishment of infection in B. glabrata, delayed redial migration, delayed germinal development within the redia, the attraction of predaceous rediae to sporocysts, the speed at which larval domination is completed and the unusual appearance of what appear to be third-generation sporocysts of S. mansoni. The phenomenon of trematode antagonism is then discussed in a separate section, in its relation to biological control. Trematode diseases such as fascioliasis and schistosomiasis have called forth the use of parasites, pathogens and predators of snails-protozoa, nematodes, leeches, fishes, ducks and geese-and reference is made to the discoveries with the molluscicide larvae of sciomyzid flies by C. 0. Berg (Advances in Parasitology 2 (1965), 259). Intramolluscan and inter-trematode antagonism is a new approach to biological control, and it is claimed that encouraging results so far obtained justify field trials against human schistosomes in endemic areas. Echinostomes are at present favoured for control of such trematode disease but other rediae-producing species must be isolated and tested, although trematode biocontrol may be applicable only in local or regional approaches. Success of control by trematode antagonism depends on strong infectivity of the antagonist in the snail that harbours the target species, and this entails heavy infection by a single miracidium in all ages of host snail in the full range of natural habitats, followed by rapid growth and development despite preceding trematode infection. It may therefore be that a single trematode species cannot be so adaptive and powerful an antagonist as to serve in biological control in other than endemic areas where it is already adapted to local snails. A plea is made therefore to develop trematode biocontrol locally. The snail is the limiting environment, imposing real barriers to a newly-introduced trematode species. Once inside the snail and successfully multiplying it is not unlikely that the antagonist would dispatch the prey trematode. Much that cannot be mentioned here is discussed in this review and in a summary the point is made that this formof biocontrol “offers limited but possibly important usefulness, especially if teamed with other control methods, such as molluscicide, sanitary and therapeutic”. In the review by Zbigniew Pawlowski and Myron G. Schultz we are

PREFACE

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XI11

reminded that cestodes have been known since ancient times and also told that in recent years several reviews dealing with cestode diseases have appeared. Nevertheless, there have not been any recent reviews which deal in a comprehensive manner with infection by Taeniu suginuta. Therefore, these writers have tried to summarize all significant matters concerning this cestode and its cysticercus, i.e. nomenclature, host-relationships, structure and biology, clinical and therapeutic features, epidemiology and epizootology, and the prevention of infection. After a brief Introduction, they consider some taxonomic problems in one section and the hosts of T. saginata in another. Man appears to be the sole definitive host of the adult of this cestode species, but because larval cestodes are much less specific than corresponding adults, the list of intermediate hosts is long and constantly extending. Man may serve as intermediate host, 12 instances having been described, one in Chile concerned 59 patients, another in Rhodesia 62 patients. In India 450 instances of cysticercosis concerned soldiers, but T. saginata was not reported. A section of this review deals with structure and biology of the adult worm, egg, onchosphere and cysticercus in turn. One interesting point about the living adult tapeworm is that it is by no means passive but often moves against the peristaltic movements in the host’s intestines. The usual site seems to be the jejunum, but radiologists have found the worm in the terminal ileum, which is said to be the part best shown by radiological examination. The entire scolex and strobila has been recorded in several unusual locations such as the appendix and the gall bladder. The idea that the worm occurs singly has been refuted, although multiple infections occur in less than 1 % of cases, except in Mexico (nearly 573, but much greater infections have been observed in the southern republics of U.S.S.R. Many other interesting points arise in this part of the review. The number of eggs in one proglottis of T. saginata has been put at about 80,000, the daily output 720,000. Elsewhere the clinical aspects of taeniasis are dealt with in terms of symptomatology, clinical pathology, diagnosis and treatment, which cannot be considered here, except to say that there is much to interest clinicians. The matter of treatment by chemotherapy has been dealt with in two reviews during the 1960s, both from the Wellcome Research Laboratories, and they are detailed here. Yomesan is the drug of choice for T. saginata infection in Man at present and some suggestions are made for treatment with this and other drugs. A sixth section deals with epidemiology and concerns transmission between animals and man, a seventh with losses due to taeniasis and cysticercosis. These sections are very informative. It is stated that taeniasis and cysticercosis (T. saginata) are cosmopolitan in distribution and have become more prevalent in recent years. During the past 25 years the world population has increased by about 50% and that of cattle by about loo%, so that it is safe to assume that infections greatly exceed the 39 million estimated by Norman Stoll in 1947. Losses are difficult to estimate, because infection is rarely fatal, but some figures are available for European, African and American areas. Meat inspection is dealt with as a means of prevention, likewise serological diagnosis and the immunization of cattle. Sanitation is a matter discussed, its improvement, expensive but connected with higher standards of living.

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The solitary updated review by Donald L. Lee lays emphasis on new work rather than on research that does not break new ground, and much more space is now devoted to the outer coverings of larval helminths and the development of this covering in adults. The following groups and species are considered : Turbellaria (Kronborgia amphipodicola) ; Monogenea (various species); Digenea (Fasciola hepatica and various other species); Cestodaria (Gyrocotyle urna) ; Cestoda (various species) ; Nematoda (various species); Acanthocephala (Polymorphus minutus). A summary is provided. At the end of one decade and the beginning of another I am happy once more to express my gratitude to friends and colleagues who have worked hard and long at compiling these reviews and who have helped to produce what I referred to above as a vast summation of modern biological information and ideas in the field of parasitology. I am equally pleased to thank the staff of Academic Press who have ironed out innumerable difficulties and smoothly brought out the tenth volume in this series, and to hope that our cooperation can continue far into a second decade, to say the least. “Rodenhurst” 22 Meadow Close* Reedley Drive REEDLEY, Nr Burnley Lancs BBlO 2QU England

* Note modified address.

BENDAWES Professor Emeritus: University of London January 1972

CONTENTS ............................................................

v vii

CONTRIE~UTORS TO VOLUME 10 PREFACE.......................................................................................

.

. . .

Avian Blood Coccidians .

.

JOHN R BAKER. GORDON F BENNETT. GLEN W CLARK AND MARSHALL LAIRD

I Introduction ........................................................................... I1 Atoxoplasms ........................................................................... 111 Adeleine Haemogregarines .........................................................

1 3 14 16 17 17

IV. Conclusions ........................................................................... Acknowledgements .................................................................. References ..............................................................................

The Metabolism of the Malaria Parasite and its Host ALEXANDER FLETCHER A N D BRIAN MAEGRAITH

I. The Metabolism of the Malaria Parasite ....................................... I1. The Metabolism of the Host During Infection .............................. References ..............................................................................

31 41

44

The Pathogenesis of Mammalian Malaria

. .

BRIAN MAEGRAITH AND ALEXANDER FLETCHER

I Introduction ........................................................................... 11 Local and General Responses in Malaria Similar to those which Occur in Inflammation .................................................................. 111. Changes in Endothelial Permeability in Malaria .............................. IV. Vasomotor Changes in Malaria ................................................ V. The Kinin Complex and Other Pharmacologically Active Agents ...... VI. Intravascular Coagulation in Malaria .......................................... VII Anoxic Anoxia ........................................................................ VIII. Cytotoxic Factors: Mitochondria1 Respiration Inhibitors .................. IX. The Chain Reaction ............................................................... References ..............................................................................

49 51 51

58 60 67 68 70 71 72

.

The Aspidogastrea, Especially Multicotyle purvisi Dawes, 1941 KLAUS ROHDE

I. Introduction ........................................................................... 11. General Characteristics ............................................................ I11. Structure of the Adult ............................................................... IV Structure of the Free Larva ...................................................... V. Development ........................................................................... VI . Biology ................................................................................. VII Phylogenetic Position of Aspidogastrea ....................................... VIII Derivation of Digenean Life Cycles from Aspidogastrean Cycle............ IX. Some Unresolved Problems ...................................................... References ..............................................................................

.

. .

xv

78 78 79 107 120 134 140 143 144 145

xvi

CONTENTS

A Phylogeny of Life-cycle Patterns of the Digenea . .

J C PEARSON

I . Introduction ........................................................................... I1. Adoption of Parasitism: One-host cycle .......................................

111. Origin of Alternation of Generations

..........................................

IV . Addition of Vertebrate ............................................................... V . Addition of Metacercarial Stage ................................................ VI . Acquisition of Second Intermediate Host: The Three-host Life.cyc1e ... VII . Three-host Life-cycle ............................................................... VIII . Modification of the Three-host Life.cyc1e ....................................... IX . Phylogenetic Implications ......................................................... X . Summary .............................................................................. References ..............................................................................

153 156 158 160 165 167 170 173 178 179 181

Intramolluscan Inter-trematode Antagonism: a Review of Factors Influencing the Host-Parasite System and its Possible Role in Biological Control HOK-KAN LIM AND DONALD HEYNEMAN

I . Introduction

........................................................................... ............................................................ 111. Trematode Interaction Patterns ................................................... IV. Parameters of Intramolluscan Inter-trematode Antagonism ............... V . Trematode Antagonism in Biological Control ................................. VI. Summary .............................................................................. References .............................................................................. I1. Materials and Methods

192 193 199 225 244 251 253

Taeniasis and Cysticercosis (Tueniu suginata) .

ZBIGNIEW PAWLOWSKI AND MYRON G SCHULTZ

I . Introduction ........................................................................... I1. Nomenclature ........................................................................ 111. Hosts of Taenia saginutu ............................................................ IV. Structure and Biology of Taenia saginatu ....................................... V. Clinical Aspects of Taeniasis ( T. suginata) .................................... VI . Epidemiology and Epizootiology ................................................ VII . Prevention ..............................................................................

269 270 271 275 282 295 304

C 0N T E N T S

xvii

SHORT REVIEW Supplementary Contribution of Previous Volume

The Structure of the Helminth Cuticle D . L . LEE

I . Introduction ........................................................................... 11. Turbellaria .............................................................................. 111. Monogenea ........................................................................... IV. Digenea ................................................................................. V . Cestodaria .............................................................................. VI . Cestoda ................................................................................. VII . Nematoda .............................................................................. VIII . Acanthocephala ........................................................................ IX . General Summary ..................................................................... References.............. .................................... .........

347 348 348 352 357 357 360 369 370 312

AUTHOR INDEX ................................................................................. SUBJECT INDEX.................................................................................

381 401

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Avian Blood Coccidians* JOHN R. BAKER?, GORDON F. BENNETT!:, GLEN W. CLARK5 A N D MARSHALL LAIRD!:

I. Introduction. ................. 11. Atoxoplasms ...................................................... I l l . Adeleine Haernogregarines ........................................................... IV. Conclusions .................. Acknowledgements ....................... References ............... .........................................

1.

14 11

INTRODUCTION

The “Pseudovermiculi sanguinis” that Danilewsky (1 889) found in the blood of certain birds (particularly magpies and owls) were said by him to resemble drepanidia and haemogregarines on the one hand, and coccidians from the kidneys of frogs on the other. He thus regarded them as gregarines, probably Coccidia. Labbe afterwards variously ascribed them (in part) to Drepanidium and Lankesterella, his (1 899) work on the Sporozoa listing Lankesterella ( = Drepanidium) avium (LabbC, 1894) from Danilewsky’s hosts and other birds too. Labbe had demonstrated his familiarity with Proteosoma (=Plasmodium) and Halteridium (= Huemoproteus)from avian hosts at this time, and moreover was well aware of the appearance of a diversity of haemogregarines of reptiles and amphibians in both living and fixed material. We wonder, therefore, whether amidst all the taxonomic confusion relating to avian blood parasitology in the last decade of the nineteenth century adeleine haemogregarines had not in fact already been recognized in birds at this time. Nevertheless, the earliest recognizable account of a blood coccidian from birds appeared-conveniently enough for the tidy-minded bibliographer-in the first year of this century (Laveran, 1900). The parasite of Padda oryzivora (the Java sparrow) described therein, was duly designated Haemogregarina paddae by Aragilo (1911). It was soon afterwards transferred to the genus Toxoplasma by Marullaz (1913), there to remain until Zasukhin et a/. (1956)

* Studies in Biology from Memorial University of Newfoundland No. 295. Contribution from the World Health Organization’s International Reference Centre for Avian Malaria Parasites No. 2. Molteno Institute, University of Cambridge, England. $ Department of Biology, Memorial University of Newfoundland, St. John’s, Newfoundland, Canada. 9: Department of Biological Sciences, Central Washington State College, Ellensburg, Washington, United States of America. 1

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J . R . B A K E R , G. F. B E N N E T T , G . W . C L A R K A N D M . L A I R D

recognized it as referable to the recently established Atoxoplasma. Just three years later, Lainson (1959) claimed that the organism was really a member of the genus Lankesterella, while Laird (1959) argued that Atoxoplasma paddae (Aragilo) is the valid type species of Atoxoplasma-Garnham (1950) having so designated a synonym of this species, A. avium (Marullaz, 1913). Box (1970) has now suggested that the same or a closely related parasite of Serinus canaria and Passer domesticus is in fact a species of Isospora. This sequence of events eloquently summarizes the taxonomic confusion which has reigned over these organisms since their first discovery. Although they have been relegated to that repository for insufficiently known forms, “Protista Incertae Sedis” from time to time, they are nowadays rather generally held to be bloodinhabiting stages of coccidia, referable to two distinct groups. Members of the first group resemble the organism described by Laveran (1900) and are seen in the peripheral circulation and (more often) the viscera, as small, unpigmented nucleophilic parasites, usually of mononuclear cells. Where one organism is present it generally lies in the cytoplasm of the host cell, which stains much more brightly with Giemsa than its own. It then appears as a conspicuously pale haemogregarine with a large and rather diffuse nucleus and a decidedly faint outline, and is often pressed into a depression of the host cell nucleus. Where (as is commonly the case) two organisms are present, they are round, oval or pyriform. They stain as do the larger single forms, and quite deeply indent the host cell nucleus, chromatin matter of which often appears to be pinched up between them. We are inclined to question the apparent homogeneity of this first group. Nevertheless, in order to defer commitment to the use of any particular generic name, all such intraleucocytic blood coccidians considered in this literature review will be referred to as “atoxoplasms”. The second group are typical adeleine haemogregarines (i.e. members of the sub-order Adeleina, order Eucoccida, sub-class Coccidia, class Telosporea, sub-phylum Sporozoa, which inhabit the blood cells of vertebrates at some stage of their life cycle). There has, however, been much dispute about their generic position. They occur in erythrocytes of the circulating blood, and their intense red-and-blue staining reaction with Giemsa is characteristically haemogregarine. Table I lists chronologically publications dealing with avian blood coccidians of both groups. The relevant literature will be reviewed separately for each. Papers where it is either impossible to tell whether the author was or was not dealing with Toxoplasma, or where there is a probability of confusion with haemoproteids, babesioids, etc. (e.g. de Mello’s 1937 record of an intraleucocytic organism from an Indian Buzzard-eagle) are left out of this Table; so are various purely secondary authorities such as Bhatia (1938). These omissions notwithstanding, it is still impossible to be quite certain to which of the two groups some reports refer, and the author’s views have not always been followed. Table II lists the recorded hosts of both groups. Other check-lists of avian haemogregarines (amongst other parasites) have been published by Wenyon (1926), Lucena (1941 ; Neotropical Region), Herman (1944; North America), Levine and Kantor (1959; Columbiformes) and Bray (1964; West Africa). The last-mentioned author was the only one of these to

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attempt a critical reassessment of authors’ identifications of the parasites. In the year when Bray’s paper appeared, Berson (1964) published a review of the protozoa parasitizing avian blood cells. The latter review mentions only a few of the records of blood coccidians from birds. Also, it retains Atoxoplasma as well as Lankesterella with A . argyae Garnham and L. argyae (Garnham) both listed under the appropriate headings. 11. ATOXOPLASMS As already mentioned, the first report of members of this group was made by Laveran (1900). He saw them in mononuclear cells in spleen and bonemarrow smears of Padda oryzivora also infected with “Haemamoeba danilewskyi”. The latter designation might refer to a true Plasmodium, but data from the World Health Organization’s International Reference Centre for Avian Malaria Parasites (Memorial University of Newfoundland) indicate that haemoproteids are much more characteristic of this host. Laveran thought that the small non-pigmented organisms might be stages in the life-cycle of “ H . danilewskyi”, but did not exclude the possibility that they were “parasites nouveaux”. Novy and MacNeal (1904, 1905) described similar organisms from Passer domesticus as Haemoproteus rouxi (“rouxii” in the second paper). Adie (1907, 1908) observed parasites in mononuclear cells of P . domesticus in India (recommending-1908-their study to fellow expatriate Englishmen in India as one of “a few things to amuse oneself with in the long days of the hot weather. . .”). He sent specimens to Laveran, who recognized their similarity to the parasite of P . oryzivora but thought they probably represented a different species. Adie (1908) was perhaps the first author to remark on the characteristic nucleophily of the atoxoplasms, which frequently lie apparently pressed into a notch in the host cell’s nucleus. (See Plate I, Figs 1 and 2. The white arrow in Fig. 1 points towards the inner margin of this notch, the black arrow to the rather brightly staining parasite nucleus.) Noller (1920) thought that some of the stages of this parasite might have been close to Toxoplasma, and some of his stages illustrating “Schizogonie” in the spleen might indeed have been. However, the birds were obviously infected with Plasmodium, either alone or together with Huemoproteus, since erythrocytic schizonts were described. It is thus possible that some at least of the atoxoplasm-like forms were exo-erythrocytic schizonts of Plasmodium. Araggo (191 1) named the organisms described by Laveran (1900) and Adie (1908) Haemogregarina paddae and H . adiei respectively. He also described what he thought were seven other species of Haemogregarina from mononuclear cells of as many species of birds in Brazil. Hoare (1924) transferred five of these species to the genus Hepatozoon (see p. 14 below), regarding the other two as avian toxoplasmas (i.e. atoxoplasms). The latter two (which to modern eyes may well be conspecific) had already been named Haemogregarina sporophilae and H. sicalidis by AragFto (191 I), who discussed them in Sporophila albogularis and Sicalisflaveola respectively. Marullaz (1913) afterwards studied (in Padda oryzivora and other passerines) the organism first reported by Laveran (1900). Marullaz tried, but failed, to

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FIGS1, 2. “Lunkesterellu garnhumi” from fledgling Passer domesticus (spleen impression smear) (J. R. Baker, England, 15 June 1960). Note marked indentation of host-cell nucleus, and deeply staining atoxoplasm nucleus. FIGS3-6. “Atoxoplasma corcothraustis” from Coccothruustes corcothraustes (lung impression smear) (A. Corradetti, Italy, ref. Corradetti and Scanga, 1963). Note faintly staining periphery of parasite and of the associated shrinkage zone outline. FIGS7, 8. “Lankesterella corvi” from Corvus fvugilegus (thin blood smear) (J. R. Baker, England, 30 June 1960). Note clearly marked periphery of intraerythrocytic sporozoites. FIGS9-16. Adeleid haemogregarine (of lizard origin?) (thin blood smear of Loomelaniu meluniu) ( G . W. Clark, San Benito Island, N. Mexico, 10 May 1967). Note pyknotic appearance of parasites as, e.g., in Figs 13 and 14, also typically reptilian-type “tailed” haemogregarine (Fig. 16). See pp. 15-16. All figures x 825 approx.

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infect mice with the parasite (which he named Toxoplasnza avium); he concluded, on morphological grounds, that it belonged to the genus Toxoplasma, described only a few years previously by Nicolle and Manceaux (1908, 1909). As pointed out by Noller (1920), this specific name is a junior synonym of AragBo’s (191 1) Haemogregarina paddae. Attempts to transmit it to other birds were inconclusive. The following year, Laveran and Marullaz (1914) described another species-T. liothricis [sic]-from Leiothrix lutea. They mentioned that the parasite was often pressed into the host cell’s nucleus. This feature seems to be almost diagnostic of the atoxoplasms (Figs 1 and 2), as does the remarkably indistinct periphery of the parasites themselves and the only faintly staining boundary of the host-cell cytoplasm with the parasites-or with a slight empty space perhaps indicating shrinkage of the latter during the preparation of the Giemsa-stained slides (Figs 3-6): it should be added that the periphery of intraerythrocytic atoxoplasms-Baker et al’s (1959) “sporozoites of Lankesterella corvi”-is usually well demarcated (Figs 7 and 8). Mine (1914) described a so-called Leucocytozoon of Passer montanus in Japan. Certain stages of his parasite (in particular, schizonts from the spleen) could well have been atoxoplasms (as suggested by Noller, 1920). Plimmer (1 9 15, 1916) recorded “Toxoplasma” from a Ducula (= Carpophaga) concinna* (fruit pigeon) dying in the London Zoological Gardens. Carini (1909) had shown that “pigeons” (presumably Columba livia) were susceptible to Toxoplasma gondii (“T. cuniculi”) and (Carini, 1911) had recorded a spontaneous infection in the same species of bird. The parasites of the latter pigeon were named T. columbue by Yakimoff and Kohl-Yakimoff (1912). Noller (1920) suggested that the organisms reported by de Mello (1913) and de Mello et a]. (1917) from Indian pigeons-again presumably C. livia-belonged to this species. Unfortunately, de Mello’s organism is impossible to categorize. It could just as well have been an atoxoplasm or even an adeleine haemogregarine (see p. 14 below). Plimmer (I 9 1 5) also recorded “To.uoplasms” from Saxicola (=Pratincola) caprata in India; this may have been in fact an atoxoplasm. Under the heading “Toxoplasmes (ou HCmogregarines?)”, Carini and Maciel (19 16) referred to finding parasites resembling those described by AragBo (191 I ) and others in various unspecified birds in Brazil. For these, they adopted Marullaz’s (1913) name Toxoplasma avium. I t is likely that some at least of their organisms were atoxoplasms. Fantham (1919, 1924) described what was probably an atoxoplasm from the mononuclear cells of Amadina erythrocephala in South Africa. Naming it Leucocytogregarina amadinae, Fantham ( 1924) remarked that the genus in question “has by some been termed Hepatozoon”. Noller (1920) discussed the “Vogeltoxoplasmen” at some length, citing unpublished work by Mayer, continued by himself, in which these parasites were studied in naturally infected siskins, Carduelis (= Chryson7itris) spinus, obtained from a Hamburg dealer. Stages in the intestinal wall of infected birds were identified as schizonts (or sporonts) and gametocytes of the eimeriine *When the host name used by the original author differs from that accepted by Peters (193 I et seq.) the former is shown in parentheses thus.

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type. The macrogametocytes were said to be significantly smaller than those of Zsospora though the schizonts were similar in size. The lymph spaces of the intestinal wall were filled with “toxoplasms” which were thought to be the progeny of the neighbouring schizonts. Other, larger “merozoites” (10-12 pm long) were also seen. Attempts to transmit the parasite failed, which would have been an unlikely result had the organism been Toxoplasma gondii. Noller concluded that while atoxoplasms bear a close morphological resemblance to both Toxoplasma and intraleucocytic haemogregarines, they differ considerably from the former in their pathogenicity and transmissibility. A further account of what was thought to be the parasite found by Mayer in siskins was given by Walzberg (1923), who concentrated upon the pathology of birds which appeared to be dying from the infection. Although the parasites themselves were not described in detail by Walzberg, his illustrations show organisms more resembling T. gondii than atoxoplasms. Perhaps Mayer and Walzberg were not in fact dealing with the same organism. Thus Walzberg’s birds might conceivably have acquired accidental laboratory infections with T. gondii. In a footnote added to the proof of Walzberg’s paper (1923; p. 32), Noller referred to work by Nitsche, and stressed the importance of differentiating the gut stages of atoxoplasms from those of Zsospora lacazei (see also Noller and Nitsche, 1923). Various other authors reported small intraleucocytic parasites of birds under the general designation Toxoplasma. Some of these reports were accompanied by little or no descriptive or illustrative material. Thus it is not always possible to decide whether the organisms concerned were atoxoplasms, adeleine haemogregarines or even, perhaps, sometimes Toxoplasma gondii itself. Nevertheless, the first of these identifications often seems the most probable. These reports include references 9, 10, 13, 16, 20, 22, 25, 30, 31, 33, 34, 36, 37, 38,40,41, 43,46, 54, 55, 57, 61, 62 and 64 in Table 1. They are not further referred to in this review apart from the inclusion of relevant host records in Table IT. Table I1 also includes numerous records concerning material that has been deposited in the World Health Organization’s International Reference Centre for Avian Malaria Parasites, which is in the Department of Biology, Memorial University of Newfoundland (Bennett and Laird, 1971) (this material is listed in more detail in Table 111). References by Neiva and Penna (1 91 6) and Primio (1925) to “Haemogregarina” of birds, which may refer to atoxoplasms, are discussed on pp. 14 and 15. Correa (1928) recorded as “Haemogregarina” parasites from three species of birds in Brazil : “H.” pessoai nsp. from Poospiza thoracica, “H.” paulasousai” nsp. from Stephanophorus diadematus (= S. leancocephalus) and “H.” sp. indet. from Molothrus b. bonariensis. These forms are perhaps more likely to be atoxoplasms than adeleine haemogregarines. Noller (1 93 l), briefly reviewing the

* Also spelt “puulusouzui” in the original paper. Since the dedication was to Professor de Paulo Souza, and the “z” was used after the first usage, the first spelling is probably a lupsus culumi. However, since the “s” spelling was used by Lucena (1941), the “first reviser” in the terms of article 32b of the International Code of Zoological Nomenclature (ed. 2, 1964; International Trust of Zoological Nomenclature, London), this must presumably stand as the “correct original spelling”.

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atoxoplasms of cagebirds, thought that transmission occurred most probably through the mite Dermanyssus uvium. AragiXo (1933) repeated his assertion that parasites of this type were all members of the genus Haemogregarina (see pp. 3 and 14), and criticized their identification as Toxoplusma. He gave the name H. serini to the species found by himself and other workers in Serinus canaria. Wolfson (1 937, 1938) recorded “Toxoplasma” or “Toxoplasma-like bodies” from S. canaria and P. domesticus. She later (1940) concluded that the organisms identified in her first paper (Wolfson, 1937) were in fact exo-erythrocytic schizonts of Plasmodium. In her second paper (Wolfson, 1938), though, she described parasites resembling atoxoplasms from birds in which malaria was not demonstrable. Kikuth and Mudrow (1938) described “Einschlusse” (inclusions) in mononuclear cells of S. canaria used in the experimental study of avian malarias. One of these inclusions illustrated by Kikuth and Mudrow (1938, Plate 1, Fig. 6 ) looks like an atoxoplasm, and was so identified by Wolfson (1940). Manwell (1939) discussed at length the confusion between “avian Toxoplasma” and exo-erythrocytic schizonts of Plasmodium in birds. He concluded that the two forms were distinct, those which were not Plasmodium being “most probably Toxoplasma”. However, he also pointed out that “there is no doubt that the Toxoplasma commonly found in birds and that isolated from mammals (. . .) are different species, and it is indeed possible that they should be placed in different genera. . . . Morphologically the bird and mammalian types are quite distinct. . . and they affect the host cell rather differently. . . .” Manwell (1 939) drew attention to the characteristic “notching” of the host cell’s nucleus by “avian Toxoplusma”, a feature which, as already mentioned, is almost diagnostic of the atoxoplasms. He also remarked that he had seen the “Einschlusse” (Kikuth and Mudrow, 1938; see above) in “numerous wild birds”, implying that they were unrelated to either Plusmodium or “avian Toxoplasma”. Six years later he (Manwell et al., 1945) suggested that they “might be due to light infections with coccidia”. Hewitt (1940) described, under the wisely non-committal term “unclassified intra-leucocytic parasites”, what were certainly atoxoplasms from two birds (Curpodacus mexicanus frontalis and Molothrus sp.) in Mexico. He was unable to transmit the parasites to S . canaria by blood inoculation. Hewitt ( 1940) concluded that the organism “resembles Hepatozoon in many respects although no sporogonic stages have ever been described”. In the same year, Wolfson (1940) discussed in detail the identity of “organisms described as avian Toxoplusma”. In what was perhaps the greatest understatement of that year, she wrote that “there exists a certain amount of confusion in the literature.. . .” Wolfson’s excellent account (1940) reviewed the literature up to that time. She pointed out that there were three main periods in the recorded history of the “avian Toxoplasmas” ; ( I ) pre-1909, when they were generally confused with the haemoproteids; (2) 1909-1937, when they were usually regarded as species of Toxoplusma (sensu stricto); and (3) the “recent” period during which this identification began to be doubted and in which some confusion arose between the organisms in question and the newly discovered exoerythrocytic stages of avian malaria parasites (cf. Manwell, 1939).

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Wolfson concluded that, in the past, at least three types of parasite had been included in the “avian Toxoplasmas”: ( I ) exo-erythrocytic stages of Plustnodium; (2) a “distinct parasite which resembles certain stages of leucocytic haemogregarines” ; and (3) organisms “perhaps identical with the mammalian Toxoplasma” ; all three types were illustrated by line drawings. Type 2, which corresponded with what are here referred to as atoxoplasms, had been seen by Wolfson in “over 25% of laboratory canaries” (S. canaria). Type 3, she studied in slides provided by Rosenbusch (cf. Rosenbusch, 1932). Wolfson concluded that Rosenbusch’s organism was probably true Toxoplasma. A study of his paper’s illustrations (1932) suggests that he may have been observing mixed infections including atoxoplasms as well (for this reason the paper has been included in the list in Table I). Wolfson further pointed out that the “type 2” organism differed from true Toxoplasma in that it “cannot bc transmitted to mammals nor even to birds of the same or different species” and also the two parasites in canaries “can be distinguished morphologically”. Finally, Wolfson considered the life-cycle of her “type 2” parasite. She observed stages in the intestinal epithelium of canaries which resembled merozoites and schizonts of “Coccidium” (presumably Isospora) in birds with and without patent infections with “type 2” and attempted to establish a ielationship between these two organisms. “Some evidence” for such a relationship was obtained by the apparent infection of two birds with “type 2” after introducing into their crops epithelial scrapings from a bird showing intestinal forms. However, she rightly pointed out that more work was needed before any such relationship, or the reality of this transmission, could be accepted. The first report of atoxoplasms in erythrocytes was published by Manwell (1941), who recorded seeing “avian Toxoplasma” in many red blood cells, as well as mononuclear cells, of an infected Passer domesticus. Plasmodium was excluded, for the parasites were unpigmented and sub-inoculation of blood did not produce infection in the recipient. This appears to be the only record of atoxoplasms of the sparrow inhabiting any circulating cells other than those of the lymphoid-macrophage series. Indeed there were, as far as we know, only two other records of intraerythrocytic atoxoplasms, one from Corvus frugilegus in England (Baker et al., 1959) and one from Climacterus picumnus in Australia (Mackerras and Mackerras, 1960). To these, we now add two (of 55) examples of the white-breasted swiftlet Collocalia esculenta, from Malaysia (Table 111). Thin blood films from both birds showed occasional small intraerythrocytic Lankesterella-like haemogregarines as well as the more typical pale-staining intraleucocytic stages of atoxoplasms. Also, only one of the fcw descriptions of avian adeleine haemogregarines refers to intraerythrocytic parasites (Franchini, 1923, 1924; see p. 14 below). Coulston (1942), in a paper unfortunately published only as an abstract, resurrected Noller’s (1920) and Wolfson’s (1 940) idea of a possible relationship between atoxoplasms and intestinal coccidia of the Isospora type. Coulston thought that the “so-called Toxoplasrna of English sparrows” ( P . domesticus) was “probably the result of a coccidial infection of the intestine having no apparent relationship with classical Toxoplasma”. He suggested that merozoites were carried in circulating lymphocytes, monocytes and macrophages

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from the intestine (where they were present in large numbers) to the spleen, liver, lungs, brain and kidneys. Unfortunately it is not clear what, if any, precautions Coulston took to avoid possible confusion due to mixed infections in his birds. This proposed identification of atoxoplasms with intestinal coccidia was also adopted by Manwell et al. (1945), who wrote that “avian Toxoplasma . . . is probably of coccidian nature”. Later, however, Manwell (1957) had changed his mind sufficiently to write that Coulston’s suggestion was “indeed possible, b u t . . . unlikely”, and he rightly drew attention to the possibility of confusing two distinct parasites in birds infected with both. Wood and Herman (1943) recorded “Hepatozoon” and “intraleucocytic parasites” from monocytes, lymphocytes and (in one bird) thrombocytes of nine species of birds in south-western United States of America (specific names of the hosts are included in the check-list, Table 11). The two types o f parasite were differentiated mainly on the grounds of shape and rather minor morphological features (nuclear shape, presence or absence of cytoplasmic granules and vacuoles), though there were also distinct size differences. Some of the so-called Hepatozoon spp., as well as the intraleucocytic parasites, resembled atoxoplasms. However, the “Hepatozoon” from Parus (= Baeolophus) inornatus transpositus was appreciably larger than atoxoplasms usually are. This parasite alone of those described by Wood and Herman we provisionally query as a true adeleine haemogregarine, with the reservation that it also may in fact be only a larger form or stage of an atoxoplasm. Garnham (1950) sought to clarify the rather confused situation by separating the small intraleucocytic parasites into a new genus, Atoxoplasma. The species A . avium (Marullaz, 1913) was designated as the type species but, as pointed out by Laird (1959), this name is a synonym of A . paddae (AragBo, 19 1 I ) and hence (under Article 67(e) of the International Code of Zoological Nomenclature, ed. 2: London, 1964) the latter must be the type species. In establishing this genus, Garnham (1950) summarized the previous work on the group and concluded that, “although the systematic position of these organisms remains unknown, for the sake of convenience it is desirable to given them a new generic name.. . .” The parasites were recorded from Lanius collaris and Turdoides (= Argya) rubiginosa in Kenya, and the species from the latter bird was named Atoxoplasnm argyae. Reichenow (1953), while accepting Garnham’s (1950) name Atoxoplasma, classified these organisms “probably” (“vermutlich”) with Schellackia and Lankesterella-i.e. in the subfamily Cryptosporidiinae of the family Eimeriidae. This suggestion was later apparently substantiated by Lainson (1 959see below). Rousselot (1953) described, under the name “Hepatozoon sperniesti n. sp.”, a parasite in the mononuclear cells of Lonchura (= Spermestes) c. cucullarus and Passer griseus in West Africa. He believed that he had succeeded in transmitting the parasite by inoculation of blood or liver homogenate to other L. c. cucullatus and P. griseus. The possibility of a pre-existent infection in the recipient birds was not adequately excluded, though Rousselot’s ( 1 953) description and illustrations indicate that these parasites were probably atoxoplasms. His remark that the organisms were sometimes “inclus dans le

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noyau” of the host cell is particularly suggestive in this context. Bray (1964) transferred this species to Lankesterella. Rousselot (1953) also reported “Toxoplasma passeris” from Passer griseus and Bray (1964) suggested that this, too, may have been an atoxoplasm. Zasukhin et al. (1956) reviewed the status of the small avian intraleucocytic parasites, concluding that they fell into two groups-Toxoplasma (sensu stricto), recorded from “pigeons, hens, capercaillie, blackcocks and some other birds”* and Garnham’s (1950) Atoxoplasma, recorded mainly from Passeriformes. They described and illustrated schizogony of “Atoxoplasma”, and recorded its presence in five species of birds in the U.S.S.R., including the ubiquitous Passer domesticus (see check-list, Table 11). Zasukhin et al. (1957) published a further description of the schizogony of “Atoxoplasma danilewskii” in Carduelis (= Spinus) spinus and recorded their failure to transmit the organism experimentally. They regarded the genus as probably belonging to the Sporozoa, but thought that further study of its systematic position was necessary. Manwell (1957) wrote that “Atoxoplasma is perhaps actually the most common blood parasite of the English sparrow” (P. domesticus), having observed it in at least 20% of the young birds he had examined in the U.S.A. He inoculated brain homogenates from over 250 P. domesticus to mice, but failed to isolate a single strain of Toxoplasma gondii-a most valuable piece of negative evidence. However, Manwell’s experimental inoculation of forty P. domesticus showed that this bird is susceptible to T. gondii, none of the inoculated animals recovering from the infection. This paper also briefly recorded the isolation of true Toxoplasma from a “crow”. Manwell (1957) now thought it “unlikely” that “Atoxoplasma” was a stage in the life-cycle of a coccidian intestinal parasite, as suggested by Coulston (1942) (but cf. Manwell et al., (1945), p. 9 herein). Mohammed (1958) recorded atoxoplasms (under the term “intra-leucocytic parasites”) from 13 of 176P. domesticus niloticus from Egypt, reserving judgement as to their correct generic name. Lainson (1958a) recorded atoxoplasms from P. domesticus in England and differentiated the parasites from Toxoplasma. Later in the same year he (Lainson, 1958b) described schizonts of this parasite within lymphoid-macrophage cells of the spleen, liver and bone-marrow of naturally infected fledgling P. domesticus. All the birds examined (adult and fledgling) were found to be infected, some of the fledglings “very heavily”. The infection appeared to be pathogenic, killing many of the fledglings under the presumed additional stress of captivity. Lainson (1958a) suspected transmission by Dermanyssus gallinae (red mite), but was unable to prove this because of the impossibility of obtaining experimental birds known to be uninfected. In the following year, Lainson (1959) described this organism’s full life-cycle including schizogony (as reported earlier), gametogony and sporogony. He claimed that the latter two processes occurred within lymphoid-macrophage cells of the liver, kidney and lung. Gametogony was said to be “of the typical Eimeria type”, the oocyst developing after fertilization of the macrogametocyte having a prominent cyst wall, and the zygote within the oocyst dividing repeatedly to produce

* Quoted from the English summary.

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many small sporozoites without the intervention of any sporoblastic or sporocystic stages. It was indicated that these sporozoites then enter lymphocytes or monocytes of the circulating blood. All these stages were fully and convincingly described, and illustrated by means of line drawings and photomicrographs. On the basis of these studies, Lainson (1959) agreed with Reichenow (1953) that atoxoplasms belong to the family Eimeriidae, sub-family Cryptosporidiinae. Within this sub-family there were only two genera into which atoxoplasms could be placed, as they possessed asporous, polyzoic oocystsLankesterella and Eleutheroschizon. The latter was parasitic in annelids, while the former haemogregarine genus was best known from amphibia (but had also been reported from Passer domesticus italiae by Raffaele, 1938). Lainson (1959) could “find no reason why they [atoxoplasms and Lankesterella] should be separated as two distinct genera”. He therefore proposed that the name Atoxoplasma Garnham, 1950, be regarded as a synonym of Lankesterella Labbt, 1899. Lainson (1959) provisionally regarded the forms from P. d. domesticus and Serinus canaria as distinct species, naming them L. garnhami (Figs 1 and 2) and L . serini respectively. He retained Raffaele’s (1938) specific name L. passeris for the form from P. domesticus italiae, but stated that the previously described species “may well be all included under the single specific name of L. paddae in the future”. Unfortunately, although quoting LabbC (1 899), Lainson (1 959) overlooked this author’s designation of Lankesterella avium. Laird (1959) also missed this point which clearly gives priority to Lankesterella (= Drepanidium) avium (Labbe, 1894) over names later proposed by AragBo (191 1) and Marullaz (1913). Lainson (1960) later reduced L. serini to a junior synonym of L. garnhami, the transmission of which he demonstrated, using Dermanyssus gallinae (a mite which he had earlier-1958b-suspected of being a vector) to infect Serinus canaria from unparasitized stock, after acquiring the organism from other canaries and house sparrows. No development of L. garnhami occurred in Dermanyssus, infection taking place when mites containing sporozoites were ingested by the recipient birds. Writing before the publication of Lainson’s later work, Laird (1959) had stressed the affinities between atoxoplasms and haemogregarines, emending the definition of the genus Atoxoplasma Garnham, 1950, to take into account its pathogenicity, demonstrated by Lainson (1958b), and the probability that it would prove to be less host-specific than had been thought when the natural means of transmission was discovered. Laird (1959) regarded all the species of atoxoplasm then described, on morphological grounds, as inseparable from Laveran’s (1900) original material. As already indicated he pointed out that the correct name for this organism was A . paddue (AragBo, 1911), not, as stated by Garnham (1950), A. avium (Marullaz, 1913). In so doing, though, he failed to notice LabbC’s (1894) description of Drepanidium avium, later emended to Lankesterella avium by LabbC (1899) himself. Laird (I 959) also recorded atoxoplasms from several species and sub-species of birds in New Zealand and tropical South Pacific islands (see Table 11). Two other species of Lankesterella, with life cycles resembling that des-

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I . R. BAKER, G . F . BENNETT, G . W . CLARK A N D M . LAIRD

cribed by Lainson (1959; 1960) for L. garnhami, were now described. The hosts were Corvusf.jrugilegus in England (Baker et a/., 1959) (Figs 7 and 8) and Acridotheres tristis melanosternus in Ceylon (Dissanaike et a/., 1965; Dissanaike, 1967). The parasites were named L. corvi and L. lainsoni respectively. Mackerras and Mackerras (1960) described L. picumni from Climacteris picumnus and recorded L. paddae-following Laird’s (1950) usage-from Passer domesticus and Zosterops lateralis, in Australia. They pointed out, however, that L. picumni (which inhabits erythrocytes and, both in this respect and morphologically, resembles L. corvi Baker et al., 1959) differs considerably in appearance from the “atoxoplasms” and that “it may well be that two different genera occur in birds”. Levine (1961) reduced L. garnhami Lainson. 1959, to a junior synonym of L. adiei (AragBo, 191 I)* since the hosts of both were merely different subspecies of P. domesticus. Lainson (1959) had in fact thought it “especially likely” that these species would be found to be conspecific. Corradetti and Scanga ( I 963) described a parasite of the atoxoplasm type from mononuclear cells of Coccothrausks coccothraustes in Italy (Figs 3-6), suggesting that only parasites of this type which inhabit erythrocytes should be placed in Lankesterella LabbC, 1899. They regarded the difference in host-cells of even a single stage in the life cycle as having generic value. However, it must be pointed out that this contention had been expressly denied by Lainson (I 959) on the grounds that (a) some species of Heputozoon and Schelluckia inhabit erythrocytes while others live in white cells and (b) sporozoites of Lankesterella corvi (see p. 12 above) were seen by Baker et a/. (1959) in erythrocytes (Figs 7 and 8), thrombocytes, lymphocytes, monocytes and polymorphonuclear leucocytes. Bray ( I 964) recorded “Lankesterella sp.” from Ploceus ( = Plesiositagra) cucullutus in Liberia. In the same paper, he transferred the species Hepatozoon spermesti Rousselot, 1950, to Lankesterella (see pp. 9-10). It now seemed that the problem of the “intra-leucocytic parasites” or atoxoplasms of birds was largely solved-they were in fact eimeriine haemogregarines of the genus Lankesterella (though Mackerras and Mackerras, 1960, sounded a warning that more than one genus might be involved), Box (1966) then began studying these parasites (which she referred to as Lankesterella) in Passer domesticus in Texas, U.S.A. She later dropped a bombshell into the midst of this relatively quiescent situation by reviving the suggestion made by Manwell et a/. (1945) and, earlier, by Coulston (1942), Wolfson (1940) and Noller (1920), that the atoxoplasms are in fact stages in the life cycle of an intestinal coccidian. Initially, Box (1967) found that the feeding of Isospora oocysts to P. domesticus resulted in increased parasitaemia and mortality due to atoxoplasms. Exposure to, or administration of, mites (Ornithonyssus bursa) did not have this effect. Neither did administration of tissue homogenates containing atoxoplasms. Although she explained these observations “as a suppression of premunition to the former infection [atoxoplasmosis] by the coccidial infection”, Box did permit herself the speculation that “the identity of Lankesterella and Isospora would fit my observations with [one] exception. . . .”

* Levine (1961) gave incorrectly the date of publication of L. rrdieias

1933.

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Taking scrupulous care to avoid previous infections of experimental birds (Serinuscanaria)with lsosporu or atoxoplasms, or infestations of Ornithonyssus, Box (1970) was later able to show that feeding such birds on oocysts resembling those of I . lacazei gave rise to tissue infections with organisms morphologically indistinguishable from atoxoplasms. Similarly, she showed that transfer of liver from birds infected with atoxoplasms (but not uninfected liver), produced infections of I . lacazei in the recipients. Much of the life-cycle was elucidated and is described in her paper (Box, 1970). After infection with oocysts, parasites are first seen in the core of the duodenal villi; they then apparently spread posteriorly along the small intestine, enter the blood stream in monocytes and parasitize other viscera such as the liver, spleen and lungs. It is impossible at present to reconcile with any certainty the conflicting results obtained by Lainson (1959, 1960) and by Box (1970). The work of both authors was careful and convincing, and Lainson’s observations were at least partially confirmed by Dissanaike (1967). Further study is clearly necessary, using atoxoplasms of as many different host species as possible and under the most rigorous conditions to exclude previous infection (a very difficult thing to do, as both Lainson and Box record). The use of tissue cultures might be worth investigating. Meanwhile, there seem to be two possible explanationseither that the two studies were made on parasites which, though morphologically identical at certain stages of their life-cycle, are in fact distinct at the familial level or (perhaps and) that one, or both, investigators was (or were) using birds with mixed infections in spite of the care taken to avoid this. While the first explanation seems less probable, it is considered likely, as predicted by Mackerras and Mackerras (1960), that more than one genus has been included under the name Lankesterella in recent years (see Khan and Desser, 1971). There are considerable morphological differences between the atoxoplasms seen in avian monocytes and the classical Lankesterella minima, which inhabits erythrocytes of frogs (see Wenyon, 1926). There have been three earlier reports of avian atoxoplasms from erythrocytes (Manwell, 1941 ; Baker et af., 1959; Mackerras and Mackerras, 1960). These are now supplemented by a further record from Malaysia (p. 8). Perhaps, as suggested by Corradetti and Scanga ( I 963), only these forms are truly members of the genus Lankesterella, the other “intraleucocytic parasites” requiring to be placed in a separate genus. Nevertheless, we agree with Lainson (1959) that the type of host cell inhabited by the sporozoites is not, of itself, a sufficient criterion for generic distinction (as proposed by Corradetti and Scanga, 1963). Were this generic separation valid, it would be conceivable that Lainson’s birds were chronically infected with the “true” Lankesterella as well as with atoxoplasms; although the fact that he never saw parasites in their erythrocytes would then be difficult to explain (Manwell, 1941, had found atoxoplasms in both leucocytes and erythrocytes of P. domesticus). Alternatively, it is also possible that, in spite of all her care, the birds used by Box were harbouring chronic, sub-patent infections of lsospora (their parents were known to be infected with this parasite).

14

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F.

B E N N E T TG, . w .

CLARK AND M. LAIRD

The recent demonstration that Toxoplasma (sensu stricto) of mammals is itself an isosporan coccidian (or even a species of Zsospora; see Overdulve, 1970) undergoing metastatic schizogony throughout the viscera of a wide range of warm-blooded hosts but, apparently, able to complete its typical isosporan sexual development only in the cat (Hutchison et ul., 1970; Frenkel et al., 1970; Sheffield and Melton, 1970), has, as noted by Box (1970), made especially relevant the latter’s findings and tends to support her suggestion that the “life-cycles of some parasites classified as Isospora may be quite different from that of the typical coccidian” (Box, 1970). Atoxoplasms have been studied by electron microscopy (Lainson, 1961 ; Garnham et al., 1962; Ludvik, 1963; Biittner, 1968; Khan andDesser, 1971). The ultrastructure revealed is markedly similar to that of Toxoplasma (e.g. SCnaud, 1967) and the other einieriid coccidia such as Eimeria spp. (e.g. Snigirevskaya, 1969; Strout and Scholtyseck, 1970) and Isospora (Schmidt et al., 1967). 111. ADELE~NE HAEMOGRECARINFS

Eleven years after Laveran’s (1900) clear description of undoubted atoxoplasms, Aragilo (I 9 11) described seven species of what he regarded as Haeniogregarina from mononuclear blood cells of seven species of South American birds. He also named the parasites described by Laveran (1900) and Adie ( I 907, 1908) Haemogregarina paddae and H. adiei respectively. Hoare ( I 924) believed that, of Aragiio’s seven species, five-H. atticorae from Notiochelidon ( = Attica [sic])gyanoleucus, H. rhamphoceli from Ramphocoelus bresilius, H. poroariae [sic] from Paroaria?dominica (= P . lavata [sic]),H. tanagrae from Thraupis ( = Tanagra) palmarium and H. brachyspizae from Zonotrichia (= Brachyspiza) capensis-were true adeleine haemogregarines of the genus Hepatozoon, probably representing only a single species, while the other two ( H . sporophilae and H. sicalidis) were not; the latter two almost certainly being atoxoplasms (see p. 3 above). Reports of adeleine haemogregarines from birds are rather rare. Todd and Wolbach (19 12) described an organism almost certainly belonging to this group from the mononuclear cells and, rarely, eosinophils and neutrophils, of a Necrosyrtes (= Neophron) monachus (vulture) in Gambia. They named the parasite Leucocytogregarina neophrontis. Their species has since been transferred to the genus Hepatozoon by Bray (1964). The parasite reported by de Mello (1915) and de Mello et al. (1917) from a pigeon (presumably Columba livia) in India, and named Haemogregarina francae by de Mello (1915), and that reported as a “leucocytogregarina” of Belonopterus chilensis lampronotus ( = B . cayennensis) by Neiva and Penna (1916), may belong in this group; they are impossible to categorize (see pp. 5 and 6.) Franchini (1923 and 1924) recorded (with no detailed description) haemogregarines within the erythrocytes and free in the plasma of Anas (= Querqueduula) crecca and A . (= Q.) circia in Italy. Hoare (1924) described a parasite from mononuclear leucocytes of an unidentified Indian eagle, and named it Hepatozoon adiei. A review by

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Mohammed and Mansour (1960) makes brief reference to this species. Primio (1 925) described three species of “Haemogregarina” from birds in Brazil“H.” aragaoi from Paroaria c. capitata, “H.” pintoi from Cathartes aura ruficollis and Coragyps atratus foetens, and “H.” travassosi from Taraba m. major. We have not been able to refer to Primio’s publication and it is therefore not possible to criticize his taxonomic ascriptions of the parasites. However, as their hosts are vultures (family Carthartidae, order Falconiformes), a group from which other undoubted adeleine haemogregarines have been reported, it is very probable that “H.” pinioi belongs to this group-perhaps to the genus Hepatozoon. Lucena (1938) briefly recorded “Haemogregarina” from four passerine birds in Brazil (Certhiaxis cinnamomea russeola, Passerina (= Cyanocompsa) c. cyanea, Saltator similis and Tachyphonus coronatus). In the absence of any description of the parasites or their host-cells, though, it is impossible to be certain of the group to which these organisms belonged. Huff (1939), also, recorded briefly, without description, a “haemogregarine?” in unspecified host cells of one Zenaidura macroura carolinensis out of nearly 200 examined during a ten-year period. Wood and Herman (1943) recorded “Hepatozoon” from six species of birds in the south-western United States of America. As discussed above (p. 9) most of these records are thought to refer to atoxoplasms. However, that from Parus (=Baeolophus) inornatus transpositus is provisionally regarded as referring to a true adeleine haemogregarine. Bray (1954) recorded Hepatozoon from a Pandion haliaetus of unspecified provenance. Other reports of “haemogregarines”, “Hepatozoon”, etc. from avian hosts are considered probably to have referred to atoxoplasms and have been reviewed in the previous section. In fact, Bray (1964) regarded only three species of adeleine haemogregarines from birds as “relatively authenticated”. These are H. monachus (Todd and Wolbach, 1912), H. adiei Hoare 1924, and his own record from P. haliaetus (Bray, 1954). Bray (1964) pointed out that these three “authenticated” records are all from large birds of prey. He continued, “it is at least possible that these birds when consuming their prey also swallow the mites, ticks, leeches, etc., which are the vectors of the haemogregarines and thus become accidentally infected by their prey’s haemogregarines”. It is also possible that Franchini’s (1923, 1924) ducks (Anas spp.) (see p. 14 above) had fed upon leeches serving as vectors of some species of adeleine haemogregarine of amphibia or fishes. These possibilities were strengthened by a very interesting discovery on the part of Clark and Swinehart (1969), who reported “Hepatozoon” from one of 15 frigate birds (Fregafa magniJicens) and one of five black storm-petrels (Loomelania melania) from offshore islands of northern Mexico. Neither host was previously known to harbour haematozoa, which are remarkably uncommon in marine birds as a whole (except for certain gulls locally parasitized by Plasmodium spp., e.g. in Australia and the U S A . and penguins, in the northern part of their range and when maintained in zoos in the presence of infected vectors). Further examination of the slide from L. melania showed the abundant presence of adeleine haemogregarines in erythrocytes only (Figs 916). The large parasites occupied the greater part of the free space on one side of the erythrocyte’s nucleus, which was crammed against the opposite cell 3

16

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G . W. CLARK AND

M. L A I R D

membrane. These organisms immediately brought to mind similar adeleine haemogregarines of reptiles. In some instances, especially where the host red blood corpuscle was partly disintegrated, the haemogregarine could clearly be seen to have a sharply reflected “tail” (Fig. 16). This was the more thoughtprovoking in that the particular island from which the parasitized petrel was collected (San Benito) abounded with terrestrial lizards. Add to this the fact that like other storm-petrels L. melaniu nest in burrows and crevices where encounters with terrestrial lizards (and their ectoparasites) are likely to occur with some frequency, and the possibility must be entertained that the bird in question was harbouring not a true avian haemogregarine but a species properly referable to a lizard host or hosts and accidentally acquired in this instance by, e.g. the ingestion of infective acarines, if not the bite of a mosquito or sandfly (see note on p. 22). Such an explanation is further supported by the fact that every one of the many intraerythrocytic haemogregarines examined was margined by a rim staining red with Giemsa; exhibited poorly defined chromatin/cytoplasm separation; and had irregular reddish masses distributed about (especially at the periphery of its body). These indications of unsuccessful capsule formation(?) and advancing pyknosis would be in accord with the presence of a haematozoon in an altogether foreign host to which it was failing to adjust. It is also worth mentioning in this context that Ayala (1970) has recently demonstrated that Hepatozoon-like parasites discovered as oocysts in the haemocoele of Californian sandflies, Phlebotomus vexator occidentalis, are capable of infecting hosts as diverse as garter snakes and western fence lizards when inoculated as sporocysts. At all events, there are various known field situations where the hypothesis of accidental infection of birds by reptilian adeleine haemogregarines could be tested. One that comes to mind besides the Baja Californian Islands is Stephens Island in Cook Strait, one of a number of New Zealand’s offshore islands where the only surviving rhynchocephalian, the tuatara (Sphenodon punctatus), is still not uncommon. This reptile very often shares burrows with the petrels and shearwaters which occupy the island in great numbers-and its extremely large erythrocytes are parasitized by an adeleine haemogregarine (Laird, 1950b).

IV. CONCLUSIONS It is evident that much confusion persists as to the proper taxonomic status of avian blood coccidians. The existing information, summarized herein, certainly provides a fascinating basis for speculation. It also suggests hypotheses meriting early testing by carefully controlled laboratory and field experimentation, to settle such questions as : Are all atoxoplasms really referable to Zsospora? If they are, do they really belong to more than a single widespread species? If there are indeed two different groups currently lumped together as atoxoplasms, are these two groups monospecific or not? Last but not least, are the relatively few probable records of adeleine haemo-

AVIAN BLOOD COCCIDIANS

17

gregarines from birds simply due to accidental infection with parasites of reptiles sharing the avian hosts’ habitats? ACKNOWLEDGEMENTS

We are very grateful to the Librarians and staffs of the London School of Hygiene and Tropical Medicine (University of London) and the Scientific Periodicals Library, Cambridge, for their cooperation and to Mr. C. W. Benson of the Department of Zoology, University of Cambridge, for invaluable assistance generously given, in checking the names of birds. Mr. Roy Ficken, Biology Department Photographer, Memorial University of Newfoundland, prepared the plate of photomicrographs (Plate I, Figs 9-16 of which were made available by one of us; G.W.C.), and our thanks are due to him for this. The work was in part supported by a grant to two of the authors (G.F.B. and M.L.) from the National Research Council of Canada, and the services of the World Health Organization’s International Reference Centre for Avian Malaria Parasites proved very helpful. REFERENCES Adie, J. R. (1907). A plea for scraps. Indian med. Gar. 42, 250-256. Adie, J. R. (1908). Note on a parasite in the sparrow. Indian med. Gat. 43, 176-180. Anschutz, G. (1909). Ueber den Entwicklungsgang des “Haemoproteus orizivorae” nov. spec. Zentbl. Bakt. ParasitKde (Abt. I, Orig.) 51, 654-659. Araggo, H. de B. (1911). ObservaG6es sobre algumas haemogregarinas das aves. Mems Inst. Oswaldo Cruz 3, 54-64. Aragiio, H. de B. (1918). Classifica~iiodos hemosporidios. Mems Inst. Butantan 1, 167-185. Aragiio, H. de B. (1933). Considbrations sur les himogregarines des oiseaux. C. r. SPanc. Sac. Biol. 113,214-215. Ayala, S. C. (1970). Hemogregarine from sandfly infecting both lizards and snakes. J. Parasit. 56, 387-388. Baker, J. R., Lainson, R. and Killick-Kendrick, R. (1959). Lankesterella corvi n. sp., a blood parasite of the English rook, Coruusf: frugilegus L. J. Protozool. 6, 233-238. Bennett, G. F. and Laird, M. (1971). Reference centre for avian malaria parasites. WHO Chronicle 25, 17-1 9. Berson, J. P. (1964). Les protozoaires parasites des hematies et du systbme histiocytaire des oiseaux: essai de nomenclature. Rev. Elev. Med. vet. Pays trop. 17, 43-96. Bhatia, B. L. (1938). Protozoa : Sporozoa. In “The Fauna of British India”. Taylor and Francis Ltd., London. Box, Edith D. (1966). Blood and tissue protozoa of the English sparrow (Passer domesticus domesticus) in Galveston, Texas. J. Protozool. 13,204-208. Box, Edith D. (1967). Influence of Isospora infections on patency of avian Lankesterella (Atoxtplasmu,Garnham, 1950). J. Parusit. 53, 1140-1 147. Box, Edith D. (1970). Atoxoplusma associated with an isosporan oocyst in canaries. J. Protozool. 17, 391-396. Bray, R. S. (1954). A Hepatozoon sp. of the osprey. Trans. R. SOC.trop. Med. Hyg. 48, 1.

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Bray, R. S. (1964). A check-list of the parasitic protozoa of West Africa with some notes on their classification Bull. Inst. fr. Afr. noire 26 (series A), 238-315. Biittner, D. W. (1968). Das cytostom von Lankesterella garnhami. Z . Zellforsch. mikrosk. Anat. 88, 126-137. Carini, A. (1909). Reproduction expkrimentale de la toxoplasmose du lapin. BUN. SOC.Path. exot. 2,465-469 and 524-525. Carini, A. (1911) Infection spontanke du pigeon et du chien due au “Toxoplasrna cuniculi”. Bull. SOC.Path. exot. 4, 518-519. Carini, A. and Maciel, J. (1916). Quelques hernoparasites du Brdsil. Bull. SOC.Path. exot. 9,247-265. Clark, G. W. and Swinehart, B. (1969). Avian haematozoa from the offshore islands of northern Mexico. Bull. Wildlife Disease Assoc. 5 , 11 1-1 12. Clark, G. W., Lee, M. A. and Lieb, D. E. (1968). Avian haematozoa of central Washington. Bull. Wildlqe Disease Assoc. 4, 15. Corradetti, A. and Scanga, M. (1963). Atoxoplasma coccothraustis n. sp., parassita del frosone (Coccothraustes coccothraustes). Parassitologia 5, 61-72. Correa, C . (1928). ContribuiCBo ao estudo das hemogregarinas do Brasil. Reuta Biol. Hyg. 1 (3), 75-81. Cory, C. B. and Hellmayr, C. E. (1927). “Catalogue of Birds of the Americas and the Adjacent Islands in Field Museum of Natural History” (Ed. W. H. Osgood), Vol. 5. Field Museum of Natural History, Chicago. Coulston, F. (1942). The coccidial nature of “avian Toxoplasma”. J . Parasit. 28, Suppl. 16 (Abstract only). Danilewsky, B. (1889). “La Parasitologie compark du Sang. I. Nouvelles recherches sur les parasites du sang des oiseaux.” D a d , Kharkov. Dissanaike, A. S. (1967). Lankesterella lainsoni sp. nov. from the Ceylon Mynah bird Acridotheres tristis melanosternus. Ceylon J. Sci. biol. Sci. 6, 225-229. Dissanaike, A. S., Nelson, P., Fernando, M. A. and Niles, W. J. (1965). Studies on haemosporidia of Ceylon birds with special reference to plasmodia. Ceylon vet. J. 13, 65-75. Fantham, H. B. (1919). Some parasitic protozoa found in South Africa-11. S. Afr. J. Sci. 16, 185-191. Fantham, H. B. (1924). Some parasitic protozoa found in South Africa-VII. S. Afr. J. Sci. 21,4344l4. Franchini, G. (1923). Hkmatozoaires de quelques oiseaux d’Italie. Bull. SOC.Path. exot. 16,118-125. Franchini, G . (1924). Observations sur les hematozoaires des oiseaux d‘Italie. Annls Inst. Pasteur, Paris 38,470-51 5. Frenkel, J. IS.,Dubey, J. P. and Miller, N. L. (1970). Toxoplasma gondii in cats: fecal stages identified as coccidian oocysts. Science, N. Y. 167, 893-896. Garnham, P. C. C. (1950). Blood parasites of East African vertebrates, with a brief description of exo-erythrocytic schizogony in Plasmodium pitrnani. Parasitology 40,328-337. Garnham, P. C. C., Baker, J. R. and Bird, R. G. (1962). The fine structure of Lankesterella garnhami. J. Protozool. 9, 107-1 14. Hamerton, A. E. (1936). Report on the deaths occurring in the Society‘s gardens during the year 1935. Proc. zool. SOC.Lond. 659-686. Hart, J. W. (1949). Observations on blood parasites of birds in South Carolina. J. Parasit. 35, 79-82. Hegner, R. and Wolfson, Fruma (1938). Toxoplasrna-like parasites in canaries infected with Plasmodium. Am. J. Hyg. 27,212-220.

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Herman, C. M. (1937). Toxoplasma in North American birds and attempted transmission to canaries and chickens. Am. J. Hyg. 25, 303-312. Herman, C. M. (1938). The relative incidence of blood protozoa in some birds from Cape Cod. Trans. Am. microsc. SOC.57,132-141. Herman, C. M. (1944). The blood protozoa of North American birds. Bird-Banding 15,89-112. Hewitt, R. (1940). Studies on blood protozoa obtained from Mexican wild birds. J . Parasit. 26, 287-295. Hoare, C. A. (1924). Hepatozoon adiei, n. sp. A blood parasite of an Indian eagle. Trans. R. SOC.trop. Med. Hyg. 18, 63-66. Huff, C. G. (1939). A survey of the blood parasites of birds caught for banding purposes. J. Am. vet. med. Ass. 94, 615-620. Hutchison, W. M., Dunachie, J. R., Siim, J. C. and Work, K. (1970). Coccidian-like nature of Toxoplasma gondii. Br. med. J. i, 142-144. Khan, R. A. and Desser, S. S. (1971). Avian Lankesterella infections in Algonquin Park, Ontario. Can. J. Zool. 49, 1105-1110. Kikuth, W. and Mudrow, Lily (1938). Die endothelialen Stadien der Malariaparasiten in experiment und theorie. Zentbl. Bakt. ParasitKde (Abt. I, Orig.) 142, 113132. Labbb, A. (1894). Recherches zoologiques et biologiques sur les parasites endoglobulaires du sang des vert6brCs. Arch. 2001.expkr., Ser. 3,2, 55-258 (158-160). LabbC, A. (1899). Sporozoa. In “Das Tierreich”. Friedlander, Berlin. Lainson, E. (1958a). Atoxoplasma Garnham, 1950, in an English sparrow (Passer domesticus domesticus Linn.). Trans. R. SOC.trop. Med. Hyg. 52, 15-16. Lainson, R. (1958b). Some observations on the life-cycle of Atoxoplasma, with particular reference to the parasite’s schizogony and its transmission by the mite Dermanyssus gallinae. Nature, Lond. 182, 1250-1251. Lainson, R. (1959). Atoxoplasma Garnham, 1950, as a synonym for Lankesterella LabbC, 1899. Its life cycle in the English sparrow (Passer domesticus domesticus, Linn.). J. Protozool. 6, 360-371. Lainson, R. (1960). The transmission of Lankesterella (= Atoxoplasma) in birds by the mite Dermanyssus gallinae. J. Protozool. 7, 321-322. Lainson, R. (1961). [Discussion to paper by Goldman, M. Classification of Toxoplasma, pp. 700-720.1 Surv. Ophthal. 6, 71 3-71 6. Laird, M. (1950a). Some blood parasites of New Zealand birds. Victoria University College, N.Z., Publs Zool. no. 5, 1-20. Laird, M. (1950b). Haemogregarina tuatarae sp. n., from the New Zealand rhynchocephalian Sphenodon punctatus (Gray). Proc. zool. SOC.Lond. 120, 529-533. Laird, M. (1959). Atoxoplasma paddae (AragBo) from several South Pacific silvereyes (Zosteropidae) and a New Zealand rail. J. Parasit. 45,47-52. Laird, M. (1962). Malayan protozoa 5. Two avian malaria parasites. J. Protozool. 9, 21-26. Laird, M. and Laird, Elizabeth (1959). In “The Natural History of Rennell Island, British Solomon Islands”, 2,213-234. Roy. Danish Museum, Copenhagen. Laveran, A. (1900). Au sujet de I’hCmatozoaire endoglobulaire de Padda oryziuora. C. r. SLanc. SOC.Biol. 52, 19-20. Laveran, A. and Marullaz, M. (1914). Sur deux htmamibes et un toxoplasme du Liothrix luteus. Bull. SOC.Path. exot. 7 , 21-25. Lawrence, J. (1946). Some observations on the plasmodia and other blood parasites of sparrows. Proc. Linn. SOC.N.S. W. 71, 1-5. 38

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J . R . BAKER, G . F . B E N N E T T , G . W . C L A R K A N D M . L A I R D

Levine, N. D. (1961). “Protozoan Parasites of Domestic Animals and Man.” Burgess Publishing Company, Minneapolis. Levine, N. D. and Kantor, S. (1959). Check-list of blood parasites of birds of the order Columbiformes. Wildl. Dis. no. 1, 1-38 [Microcard]. Lucena, D. (1938). Haemoparasitas de algumas aves de SBo Paulo. Revta Biol. Hyg. 9, 158-161. Lucena, D. T. (1941). Lista dos protozokrios hemoparasitas de aves da regiao neotr6pica. Anais SOC.Biol. Pernamb. 2 (2), 3-61. Ludvik, J. (1963). Electron microscopic studies of some parasitic protozoa. Int. Congr. Protozool. 1, 387-392. Mackerras, M. Josephine and Mackerras, I. M. (1960).The haematozoa of Australian birds. Aust. J. Zool. 8, 226260. Manwell, R. D. (1939). Toxoplasma or exoerythrocytic schizogony in malaria? Riv. Malar. 18,7688. Manwell, R. D. (1941). Avian toxoplasmosis with invasion of the erythrocytes. J. Parasit. 27, 245-250. Manwell, R. D. (1957). Blood parasitism in the English sparrow, with certain biological implications. J. Parasit. 43,428-433. Manwell, R. D. and Herman, C. M. (1935). Blood parasites of birds of the Syracuse (N.Y.) region. J. Parasit. 21,415-416. Manwell, R. D., Coulston, F., Binckley, Ellen C. and Jones, Virginia P. (1945). Mammalian and avian Toxoplasma. J. infect. Dis. 76, 1-14. Marullaz, M. (1913). Au sujet d’un toxoplasme des oiseaux. Bull. SOC.path. exot. 6, 323-326. de Mello, F. (1915). Preliminary note on a new haemogregarine found in the pigeon’s blood. Indian J. med. Res. 3,93-94. de Mello, F. (1937). Further contributions to the study of the blood parasites of the Indian birds, together with a list of the hemoparasites hitherto recorded. J. roy. Asiat. SOC.Bengal, Science, 1936 2,95-122. de Mello, F., de Sa, B., Bras, de Sousa Loreto, Dias, A. and Moroha, R. (1917). Hematozoaires et pseudo-hematozoaires de 1’Inde portugaise. Annais scient. Fac, Med. Porto 3,5-24. Mine, N. (1914). Beitrage zur kenntnis der Blutparasiten der Vogel in Japan. Arch. Protistenk. 34, 198-21 1. Mohammed, A. H. H. (1958). “Systematic and Experimental Studies on Protozoal Blood Parasites of Egyptian Birds”, Vol. 1. University Press, Cairo. Mohammed, A. H. H. and Mansour, N. S. (1960). The haemogregarine complex. Bull. Fac. Sci. Cairo Univ. no. 35, 39-51 (dated 1959). Neiva, A. and Penna, B. (1916). Viajem cientifica pel0 Norte da Bahia, sudoeste de Pernambuco, Sul do Piauhi e de norte a sul de Goiaz. Mems. Inst. Oswaldo Cruz 8 (3), 74-224. Nicolle, C. and Manceaux, L. (1908). Sur une infection A corps de Leishman (ou organismes voisins) du gondi. C . r. hebd. Se‘anc. Acad. Sci. 147,763-766. Nicolle, C. and Manceaux, L. (1909). Sur un protozoaire nouveau du gondi. C. r. hebd. Skanc. Acad. Sci. 148,369-372. Noller, W. (1920). In “Handbuch der pathogenen Protozoen” (Eds S. von Prowazek and W. Noller), Vol. 2, pp. 907-918. J. A. Barth, Leipzig. Noller, W. (1931). In “Tierheilkunde und Tierzucht” (Eds V. Stang and D. Wirth), vol. 9, pp. 424-440. Urban and Schwarzenberg, Berlin and Vienna. Noller, W.and Nitsche, 0. (1923). Ueber einige verbreitete Erkraukungen unserer einheimischen Sperlingsvogel. Berl. tierartzl. Wschr. 39,443-447 and 455-458.

A V I A N BLOOD C O C C I D I A N S

21

Now, F. G. and MacNeal, W. J. (1904). On the trypanosomes of birds. J . infect. Dis. 2, 256-308. Novy, F. G. and MacNeal, W. J. (1905). Trypanosomes and bird malaria. Am. Med. 8, 932-934. Overdulve, J. P. (1970). The identity of Toxoplasma Nicolle and Manceaux, 1909 with Zsosporu Schneider, 1881 (I). Proc. K . ned. Adad. wet., C 73,129-151. Pessha, S. B. and Conga, Clovis (1929). Nota sobre toxoplasmas dos passaros. Anaispaul. Med. Cirurg. 20, 103-106. Peters, J. L. (1931 et seq.). “Check-list of Birds of the World” (continued by various authors and editors). Harvard University Press (continued by Museum of Comparative Zoology), Cambridge, Mass. Plimmer, H. G. (1915). Report on the deaths which occurred in the zoological gardens during 1914, together with a list of the blood parasites found during the year. Proc. zool. SOC. Lond. 123-130. Plinimer, H. G. (1916). Notes on the genus Toxoplasma, with a description of three new species. Proc. R. SOC.,B 89,291-296. Primio, R. di (1 925). “Contribuiqiio para o Estudo das Hemogregarinas Brasilieras”. Typ. Lenzinger, Rio de Janeiro. [Not seen; cited by Lucena (1914).] Raffaele, G. (1932). Sulle cosidette toxoplasmosi dei passeri. Riu. Malar. 11, 825838. Raffaele, G. (1938). Evoluzione di Plasmodium, Toxoplasma ed altri microrganismi negli organi interni dei vertebrati. Riu. Malur. 17, 85-100. Reichenow, E. (1953). “Lehrbuch der Protozoenkunde”, Vol. 2, pp. 820-966. Gustav Fischer, Jena. Rosenbusch, F. (1932). Toxoplasmosis avium en 10s canarios. Reun. SOC.argent. Patol. reg. N. (7), 904-906. Rousselot, R. (1953). “Notes de Parasitologie Tropicale”, Vol. 1, pp. 62-64. Vigot, Paris. Schmidt, K., Johnston, M. R. L. and Stebhens, W. E. (1967). Fine structure of the schizont and merozoite of Zsospora sp. (Sporozoa : Eimeriidae) parasitic in Cehyra uariegata (Dumeril and Bibron, 1836) (Reptilia: Gekkonidae). J. Protorool. 14,602-608. SBnaud, J. (1967). Contribution A 1’6tude des sarcosporidies et des toxoplasmes (Toxoplasmea). Protistologica 3, 167-232. Sheffield, H. G. and Melton, Marjorie L. (1970). Toxoplasma gondii: the oocyst, sporozoite, and infection of cultured cells. Science, N. Y. 167, 892-893. Snigirevskaya, E. S. (1969). Electron microscopic study of the schizogony process in Eimeria intestinalis. Acta Protozool. 7, 57-70. [Russian with English summary.] Stauber, Mabel F. and Stauber, L. A. (1942). Bird malaria in southern New Jersey. Proc. New Jers. Mosq. Exterm. Ass. 29,4546. Strout, R. G . and Scholtyseck, E. (1970). The ultrastructure of first generation development of Eimeria tenella (Railliet and Lucet, 1891) Fantham, 1909 in cell cultures. 2.ParasitKde 35, 87-96. Taddia, L. (1938). Plasmodidi e corpi Toxoplusma-simili nei passeri del Veneto. Riu. Malar. 17,239-241. Todd, J. L. and Wolbach, S. B. (1912). Parasitic protozoa from the Gambia. J. med. Res. 26, 195-218. Uegaki, J. (1930). Untersuchungen iiber die Blutprotozoen von Vogeln der Siidsee. Arch. Protistenk. 72,7490. Walzberg, U . (1923). Zur pathologischen Histologie der naturlichen Toxoplasmose des Zeisigs. Z . Infektkrankh. parasit. Krankh. Hyg. Haustiere 25, 19-33.

22

J . R . BAKER, G . F . B E N N E T T , G . W . C L A R K A N D M . L A I R D

Wenyon, C. M. (1926). “Protozoology”, Vol. 2. Ballikre, Tindall and Cox, London. [Reprinted 1965 by Ballikre, Tindall and Cassell, London.] Wetmore, Psyche W. (1941). Blood parasites of birds of the District of Columbia and Patuxent Research Refuge vicinity. J. Parasit. 27, 379-393. Wohnus, J. F. and Ryerson, D. L. (1941). Hematozoa from California birds. J. Parasit. 27, 540-541. Wolfson, Fruma (1937). Experimental transmission of Toxoplasma in canaries. J. Parasit. 23, 553. Wolfson, Fruma (1938). Two types of Toxoplasma-like bodies in canaries. J. Parasit. 24, Suppl. 22 [Abstract only]. Wolfson, Fruma (1940). Organisms described as avian Toxoplasma. Am. J. Hyg. 32, C 88-99. Wood, S. F. and Herman, C. M. (1943). The occurrence of blood parasites in birds from southwestern United States. J. Parasit. 29, 187-196. Wood, Fae D. and Wood, S. F. (1937). Occurrence of haematozoa in some Californian birds and mammals. J. Parasit. 23, 197-201. Yakimoff, W. L. and Kohl-Yakimoff, N. (1912). Toxoplasma canis (Mello). Arch. Protistenk. 27, 195-206. Zasukhin, D. N., Vasina, S. G . and Levitanskaya, P. B. (1956). [Atoxoplasma and Toxoplasma of birds]. Zool. Zh. 35, 1799-1808. [English summary in Zool. Zh. 35 (12), Summaries, 6.1 Zasukhin, D. N., Vasina, S. G . and Levitanskaya, P. B. (1957). [On the problem of the atoxoplasmas of birds.] Trudj Leningr. Obshch. Estest. 73,117-120. [German summary on p. 120.1 Papers not included in Tables I and 11: Bax, Edith D. (1971). Lankesterella (Atoxoplasma). In “Infectious and Parasitic Diseases of Wild Birds” (Eds. J. W. Davis, R. C. Anderson, L. Karstad and D. 0. Trainer), pp. 309-312. Iowa State University Press, Ames, Iowa. Oda, S. M., Chao, J. and Ball, G. H. (1971). Additional instances of transfer of reptile haemogragarines to foreign hosts. J. Parisit, 53, 1377-1378. Poelma, F. G., Zwart, P. and Strick, W. J. (1970). [Lankesterella infections in birds in the Netherlands.] Tijdschr. Diergeneesk. 95, 1163-1 169. [In Dutch; English version (1971) in Nerh. J. vet. Sci. 4, 43-50.]

ADDENDUM.

NOTE ADDED IN PROOF. Oda et al. (1971; see addendum above) have recently reported the experimental transfer of a Hepatozoon from a snake to a lizard, and state that “There is now a considerable body of evidence that at least some haemogregarines of reptiles can be transferred experimentally to foreign hosts”.

23

AVIAN BLOOD COCCIDIANS

TABLEI Chronological list of publications on avian haemogregarines (including atoxoplasms)*

1 2 3 4

Laveran, 1900 Novy and MacNeal, 1904 Novy and MacNeal, 1905 Adie, 1907 5 Adie, 1908 6 Anschiitz, 1909 7 AragBo, 1911 8 Todd and Wolbach, 1912 9 Marullaz, 1913 10 Laveran and Marullaz, 1914 11 Mine, 1914 12 de Mello, 1915 13 Plimrner, 19151 14 Carini and Maciel, 1916 15 Neiva and Penna, 1916 16 Plimmer, 19161 17 de Mello et al., 1917 18 AragBo, 1918 19 Fantham, 1919 20 Noller, 1920 21 Franchini, 1923 22 Noller and Nitsche, 1923 23 Walzberg, 19232 24 Fantham, 1924 25 Franchini, 1924 26 Hoare, 1924 27 Primio, 1925 28 Wenyon, 1926 29 CorrEa, 1928 30 Pessoa and CorrEa, 1929 31 Uegaki, 1930 32 Noller, 1931 33 Raffaele, 1932 34 Rosenbusch, 1932 35 AragBo, 1933 36 Manwell and Herman, 1935 37 Hamerton, 1936 38 Herman, 1937 39 Wolfson, 19373 40 Wood and Wood, 1937 41 Hegner and Wolfson, 1938 42 Kikuth and Mudrow, 1938 43 Herman, 1938 ~

44 Lucena, 1938 45 46 47 48 49 50 51 52 53 54

Raffaele, 1938 Taddia, 1938 Wolfson, 1938 Huff, 1939 Manwell, 1939 Hewitt, 1940 Wolfson, 1940 Lucena, 1941 Manwell, 1941 Wetmore, 1941 55 Wohnus and Ryerson, 1941 56 Coulston, 1942 57 Stauber and Stauber, 1942 58 Wood and Herman, 1943 59 Herman, 1944 60 Manwell et al., 1945 61 Lawrence, 1946 62 Hart, 1949 63 Garnham, 1950 64 Laird, 1950 65 Reichenow, 1953 66 Rousselot, 1953 67 Bray, 1954 68 Zasukhin et al., 1956 69 Manwell, 1957 70 Zasukhin et al., 1957 71 Lainson, 1958a 72 Lainson, 1958b 73 Mohammed, 1958 74 Baker et al., 1959 75 Lainson, 1959 76 Laird, 1959 77 Laird and Laird, 1959 78 Levhe and Kantor, 1959 79 Lainson, 1960 80 Mackerras and Mackerras, 1960 81 Mohammed and Mansour, 1960 82 Lainson, 1961 83 Levine, 1961 84 Garnham et al., 1962 85 Corradetti and Scanga, 1963 86 Ludvik, 1963

~

~~

~

* Authors publishing in the same year are listed alphabetically. Possibly refers to Toxoplasma sensu siricto. Mostly refers to Toxoplasma but record from Chrysomiiris spinus on p. 20 may refer to atoxoplasms. 3 Said by Wolfson (1940) to be a misidentification of exoerythrocytic forms of PIasmodium. 1 2

24

J . R. BAKER, G . F. BENNETT, G . W. CLARK A N D M . LAIRD

TABLEI (continued) 87 Bray, 1964 88 Dissanaike et al., 1965 89 Box, 1966 90 BOX,1967 91 Dissanaike, 1967 92 Biittner, 1968

93 94 95 96 97

Clark et al., 1968 Clark and Swinehart, 1969 Ayala, 1970 Box, 1970 Khan and Desser, 1971

TABLEI1 Check list of avian hosts of haemogregarines (including atoxoplasms)* Acanthis cannabina cannabina (L.)[Cannabinalinota] Acridotheres tristis tristis (L.) Acridotheres tristis melanosternus Legge Agelaius phoeniceus (L.) Amadina erythrocephalassp. Ammodramus sandwichensis savanna (Wilson) [Passerculus sandwichensis savanna] Anas crecca ssp. [Querquedulacrecca] Anas querquedula L. [Q. circial Aramides cajanea cajanea (P. L. s. Miiller) Belonopterus chilensis lampronotus (Wagler) [B. cayennensis] Carduelis chloris ssp. [Chlorischloris] Ibid. [Ligurinuschloris] Carduelis cucullata Swainson ( ?) [Coryphospinguscucullatus] Carduelis spinus (L.) [Chrysomitrisspinus] Ibid. [Spinusspinus] Carpodacus mexicanus ssp. Carpodacus mexicanusfrontalis (Say) Cathartes aura ruficollis Spix Certhiaxis cinnamomea russeola (Vieillot) Chamaeafasciata ssp. Chamaea fasciata henshawi Ridgway Climacterispicumnus ssp. Coccothraustes coccothraustes coccothraustes (L.) Collocalia esculenta (L.) Columba livia ssp. ["pigeon"] Columba rufina sylvestris Vieillot Columbigallinatabacoti talpacoti (Temminck) Copsychus saularis ssp. Coragyps atratusfoetens (Lichenstein) Corvusfrugilegusfrugilegus L. Cyanocitta cristata ssp. Dendroica coronata auduboni (Townsend) Ibid. [D. auduboni] Ducula concinna ssp. [Carpophaga concinna] Dumetella carolinensis (L.) Emberiza citrinella ssp. Erythruraprasina ssp.

22,23 WHO/IRC 88,91 89 19,24 43 21 H 25 H 44 15 68 22,23 44 201 68,70 WHO/IRC 40, 50, 58 27 H 44H WHO/IRC 55,58 80 85, WHO/IRC WHO/IRC 12, 17, 20, 28 44 44 WHO/IRC 27 H 74 2 WHO/IRC 58 13,16 38,43, 54, 57 68 31

25

A V I A N BLOOD C O C C I D I A N S

TABLE I1 (continued) Euphagus carolinus nigraus Burleigh and Peters Euplectus orix franciscanus (Isert) [Pyromelanafranciscana] Fregata magnificens Fringilla coelebs coelebs L. (?) [Serinus balearicus] Fringilla coelebs ssp. Gallirallus australis australis (Sparrman) [G.a. scotti] Gallusgallus ssp. (var. domesticus) Garrulax erythrocephalus ssp. Hesperosiphonia v. vespertina (Cooper) Hirundo rustica erythrogaster Boddaert Icterus galbula ssp. Lagonosticta senegala ssp. Lagopus Iagopus ssp. Lanius collaris ssp. Leiothrix lutea ssp. Lonchura cucullatus cucullatus (Swainson) [Spermestes c. cucullatus] Lonchura maja (L.) [Munia maja] Lonchura malacca atricapillu (Vieillot) [M.atricapilla] Lonchura m. malacca (L.) [M. malacca] Lonchura malabarica ssp. [Aidemosyne malabarica] Lonchura punctulata topela (Swinhoe) [M. topela] Macronus ptilosus ssp. Mimus polyglottus leucopterus (Vigors) Molothrus ater ater (Boddaert) Molothrus ater obscurus (Gmelin) Molothrus bonariensis ssp. Molothrus bonariensis bonariensis (Gmelin) Molothrus sp. Muscicapa narcissina ssp. Necrosyrtes monachus ssp. [Neophronmonachus] Notiochelidon cyanoleuca ssp. [Attica cyanoleucus] Oceanodroma meania (Bonaparte) [Loomelania melania] Pachycephala cinarea ssp. Padda oryzivora (L.) Ibid. [“Spermestes oryzivora oder Orizornis oryzivora”] Ibid. [“Oryzornisoryzivora (Padda oryzivora)”] Ibid. [Reisvogel] Pandion haliaetus ssp. Paroaria capitata capitata (d‘orbigny and Lafresnaye) P. ? dominicana (L.) [P. lavata] Parus inornatus ssp. Parus inornatus transpositus (Grinnell) [Baeolophusinornatus transpositus] Passer domesticus indicus Jardine & Selby [Sparrow] Passer d. italiae (Vieillot) [P. italiae] Ibid. [Sparrow] Ibid. [P. italicus] Passer d. niloticus Nicolle & Bonhote

WHO/IRC 9 94 H 37 9 76 44 WHO/IRC 97 93 2, 43 9 WHO/IRC 63 10

66 31 31 31 31 31 WHO/IRC 58 43, WHO/IRC 58 29 H 44 50 WHO/IRC 82 H 7H 94 H, WHO/IRC WHO/IRC 1,9 6 31 65 67 H 27 7H WHO/IRC 58 H 4, 5 25 33,46 45 73

26

J . R . BAKER, G . F. B E N N E T T , G.

W. C L A R K A N D M. L A I R D

TABLE I1 (continued) Passer domesticus ssp. [“Sparrow”] Ibid.

Passer griseus ssp. Passer montanus ssp. Passer flaveolus ssp. Passerina cyanea (L.)[Cyanocompsacyanea cyaneal Petrochelidonpyrrhonota ssp. Pheucticus melanocephalus ssp. I bid. [Hedymeles rnelanocephalus] P. ludovicianus (L.) Pipilo erythrophthalmus erythropthalmus (L.) Pitta brachyura ssp. Ploceus cucullatus ssp. [Plesiositagracucullatus] Ploceusphilippinusphilippinus (L.)[P. bayal Pycnonotus goiavier ssp. Pycnonotus jocosus ssp. Pycnonotus xanthopygos (Ehrenberg) Poospiza thoracica (Nordman) Quelea erythrops (Hartlaub) Quiscalus mexicanus ssp. Quiscalusquiscula quiscula (L.) Ramphocoelus bresilius ssp. Rhipidurajavanica ssp. Saltator similis ssp. Saxicola caprata ssp. Serinus canaria (L.)

Sicalis flaveola ssp. Spizella passerina ssp. Ibid. [Chipping sparrow] Sporophila albogularis (Spix) Sporophila caerulescens ssp. Stachyris leucotis ssp. Stachyris nigricollis (Temminck) Stephanophorus diadematus (Temminck) [S. leancocephalus] Sturnella magna ssp. Sturnus vulgaris ssp. Tachyphonus coronatus (Vieillot) Ibid. [Techyphoceuscoronatus] Taraba major major (Vieillot) Thraupispalmarum palmarum (Wied.) [Tanagra palmarum]

3,85 22, 232, 36,38, 43,47,49, 53, 54,56, 58, 61, 62, 68, 69,71, 72, 75, 79, 80, 82, 833, 84, 89, 90,92,96 66 11,25 WHO/IRC 44 H WHO/IRC WHO/IRC 58 97 38,43 WHO/IRC 87 31 WHO/IRC WHO/IRC WHO/IRC 29 H 9 89 54 7H WHO/IRC 44H 16 34, 35, 36, 38, 3g4,41,42,47 51, 68,72, 75, 79,90,96, WHO/IRC 7 38,43 69 7

44 WHO/IRC WHO/IRC 29 H 89 38,43 44H 30 27 7H

27

AVIAN BLOOD COCCIDIANS

TABLE I1 (continued) ~

Thraupis sayaca sayaca (L.) [Tanagra sayaca] Toxostoma redivivum redivivum (Gambel) Trichostoma abbotti ssp. Trichostoma bicolor (Lesson) Trichostoma restratum ssp. Turdoides rubiginosa ssp. [Argya rubiginosa] Tyrannus tyrannus (L.)5 Uraeginthusbengalus bengalus (L.) [Estrildaphoenicotis] Volatiniajacarina ssp. Woodfordia superciliosa North Zenaidura macroura carolinensis(L.) Zonotrichia capensis matutina (Lichenstein) [Brachyspizacapensis matutinal Zonotrichia capensis ssp. [Brachyspiza capensis] Zonotrichia georgiana ssp. [Melospizageorgiana] Zonotrichia melodia melodia (Wilson) [Melospiza melodia melodia] Zonotrichia melodia ssp. [songsparrow] Zosterops flavifrons flavifrons (Gmelin) Zosteropsf. majuscula Murphy & Mathews Zosterops lateralis ssp. Zosterops 1. griseonota Gray Zosterops rennelliana Murphy “Indian eagle”

30 58, WHO/IRC WHO/IRC WHO/IRC WHO/IRC

63 38,43 9 44 76,17 48 H 44 7H 38,43 38,43 69 76 76 64,80 76 76,77 26 H

* (i) Host names have been checked with Peters (1931 et seq.) and, where this differs significantly, the nomenclature used by the author of the paper cited is given in square brackets. Where a subspecific determination is neither given nor self-evident from the context, “ssp.” (indicating “subspecies unknown”) follows the specific name without indication of authorship. (ii) Numbers refer to Table I, and “WHO/IRC” to material deposited in the World Health Organization’s International Reference Centre for Avian Malaria Parasites separately listed in more detail in Table 111. (iii) Records marked “H” refer, or are believed to refer, to adeleine haemogregarines. All others (and the great majority) refer to atoxoplasms, or organisms believed to be atoxoplasms. 1 Citing personal communication by Mayer. a Footnote by W. Noller on p. 32. 3 Citing unpublished work by D. D. Myers. 4 Probably misidentification of Plasmodium-see ref. 51. 5 Name checked in Cory and Hellmayr (1927).

TABLE I11

h, 00

Atoxoplasmmaterial(thin Giemsa-stained bloodfilms)availablefor study in the collections of the WorldHealth Organization’s International Reference Centrefor Avian Malaria Parasites (Department of Biology, Memorial Universityof Newfoundland,St. John’s, Newfoundland, Canada)

Systematic position APODIDAE Collocalia esculenta (L.) CHAMAEIDAE Ckamaeafasciata ssp. EMBERIZIDAE Pkeucticus melanocephalus spp. FRINGILLIDAE Carpodacus mexicanus ssp. Coccotkraustescoccotkraustes coccotkraustes (L.) Serinus canaria (L.) ICTElUDAE Euphagus carolinus nigraus Burleigh and Peters Molotkrus ater ater (Boddaert)

MIMIDAE Toxostoma redivioum rediviuum (Gambel)

Common name

WHO/IRC accession number

Country where collected

Date of collection

LI

? m

>

No. sampled for WHO/IRC up to July 1971

No. infected

55

2 1

2 2

*z

White-breasted Swiftlet

2680 2679)

Malaysia

-14161

Pallid Wren-Tit

1036

U.S.A.

15/8/37

1

Black-headed Grosbeak

379

U.S.A.

22/8/37

48

House Finch

1446 1382} 276

,lb n ? m

rn

U.S.A.

17/6/36

Hawfinch

1506 16922

Italy

26/11/61

1

Canary

16920

Madagascar

1/4/66

1

1

Rusty Blackbird

16660

Canada

14/7/70

10

1

1168

U.S.A.

21/5/37

55

1

U

3 r

Cowbird

2 0

U

California Thrasher

880

U.S.A.

6/8/37

14

1

MUSCICAPIDAE Muscicapa narcissina ssp. Pachycephala cinerea ssp. Rhipidurajavanica ssp.

Narcissus Flycatcher Mangrove Whistler Pied Fantail

4701 4846 4468

Malaysia Malaysia Malaysia

4471 PARIDAE Parus inornatus ssp. PARULIDAE Dendroica coronata auduboni (Townsend) PIl7-IDA.E Pitta brachyura ssp.

San Diego Titmouse Audubon’s Warbler Blue-winged Pitta

2017161 5/8/62 15/6/61 31/5/61

U.S.A.

1 1

6

4

2

U.S.A. 957

13 54

20112/37

47

3332 3333} Malaysia

(8i)

20

3334 Pitta megarhyncha ssp.

PLOCELDAE Passer fIaveolusssp. PYCNONOTIDAE Pycnonotus goiavier ssp. Pycnonotusjocosus ssp. Pycnonotus xanthopygos (Ehrenberg) STURNLDAE Acridotheres tristis tristis (L.)

TETRAONIDAE Lagopus lagopus ssp.

Greater Bluewinged pitta

Malaysia

15/6/60

0

3

Pegu Sparrow

12615

Thailand

27/7/67

122

Yellow-vented Bulbul Red-whiskered Bulbul Black-capped Bulbul

7875 12376

Malaysia Thailand

25/4/65 15/1/68

561 22

1 1

19449

Tanzania

21/11/70

30

1

Indian Mynah

16915 16916)

Madagascar

3

2

188

1

Willow Ptarmigan

8932

Canada

0

a

N \D

Systematic position TIMALIIDAE Minla strigula malayana (Hartert) Macronusptilosus ssp. Stachyris leucotis ssp. Stachyris nigricollis (Temminck) Trichostoma abbotti ssp. Trichostoma bicolor (Lesson) Trichostoma rostratum ssp.

TABLE I11 (continued) WHO/IRC Country accession where Common name number collected

w

0

Date of collection

No. sampled for WHO/IRC up to July 1971

No. infected

p m

Chestnut-tailed Siva

4313

Malaysia

2013162

Fluffy-backed Tit Babbler White-eared Tree Babbler Black-necked Tree Babbler Abbott’s Jungle Babbler Ferruginous Jungle Babbler Blyth’s Jungle Babbler

3866

Malaysia

3015162

32

3987

Malaysia

9/5/63

3

3732

Malaysia

2911163

19

3708

Malaysia

24/8/62

24

Malaysia

3577

34

16/2/61 Malaysia

1 119

3589 TURDIDAE Copsychussaularis ssp. Garrulax erythrocephalus ssp.

Magpie Robin Red-headed Laughing Thrush

5271 4087

Malaysia Malaysia

* Listed as “Lunkesteria” (in double infection with Plasmodium rouxi) by Laird (1962).

7/5/61 -/-/61

107 17

3

r >

The Metabolism of the Malaria Parasite and its Host ALEXANDER FLETCHER AND BRIANMAEGRAITH Department of Tropical Medicine, Liverpool School of Tropical Medicine, Liverpool, England I. The Metabolism of the Malaria Parasite ................................................... A. Introduction ................................................................................. B. General Considerations .................................................................. C. Pentose Phosphate Pathway Activity in Malaria-infected Erythrocytes ...... D. Further Metabolism of Glucose ......................................................... E. Carbon Dioxide Fixation by Malaria Parasites .................................... F. Aerobic Mechanisms in Mammalian Malaria Parasites ........................... G. The Metabolism of Chloroquine-resistant Malaria Parasites.. ................... H. Concluding Remarks ..................................................................... 11. The Metabolism of the Host During Infection ............................................. A. Biochemical Changes in Erythrocytes ................................................ B. Effects of Acute Infection on Host-tissue Metabolism ........................... C. Host Lipid Metabolism .................................................................. D. Concluding Comments ..................................................................

I. THE METABOLISM OF A.

THE

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MALARIA PARASITE

INTRODUCTION

This review is not intended as a comprehensive account of recent literature in this field. Instead, we shall discuss certain considerations which are necessary in metabolic investigations of Plasmodia and some current research trends which we think are advancing our understanding of the fundamental biochemical processes present in parasites and involved in the host-parasite relationship. The mode of action of drugs and mechanisms of drug resistance will be mentioned only when necessary, in order to present a logical account of the selected subject matter; these topics have recently been well reviewed by Peters (1970). B.

GENERAL CONSIDERATIONS

Metabolic studies of malaria parasites are usually performed either on infected blood, parasitized erythrocytes or on parasites freed from their host erythrocytes. When infected blood is examined biochemically, the tacit assumption is often made that any changes in the biochemical parameters being studied 31

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are due directly to the activities within parasitized erythrocytes. The contribution of the non-infected cells in the infected blood is generally assumed to alter very little from its pre-infection state. Some workers do make reservations regarding this assumption but others do not mentioned this point at all. It is becoming increasingly obvious that biochemical changes occur in uninfected cells as well as in their parasitized counterparts. This will be referred to in a later section. It must be borne in mind that such biochemical changes may not be in the same direction. As a result the apparent changes in parasitized cells may either be minimized or magnified, depending on the stage of parasite development and other related factors. Many workers have attempted to overcome such problems by attempting to isolate suspensions of parasitized erythrocytes. This is relatively easy when there is a synchronous development of asexual parasites, as shown by the pioneering work of Christophers and Fulton (1938), working with P.knowlesi. Other workers have extended their method of differential centrifugation by the use of gradients, sometimes employing polymers; an example of this approach is the albumin flotation method used by Fulton and Spooner (1956) to concentrate P. berghei-infected rat reticulocytes. Such methods employing large molecules or sucrose gradients (Williamson and Cover, 1966), while being suitable for the isolation of parasitized erythrocytes with the aim of isolating certain parasite fractions, may not necessarily be suitable for studying metabolic processes in the host-erythrocyte complex because of associated osmotic effects. The introduction of zonal centrifugation for the separation of marginally different populations of cells or cell organelles offered a new approach to the isolation of parasitized erythrocytes. Sucrose gradients have commonly been used for this procedure but because of possible osmotic effects, large molecules, such as synthetic polysaccharides, have to be considered. Using this technique and the synthetic polymer Ficoll (Pharmacia, A.G., Uppsala, Sweden) Ali and Fletcher (1971b) have recently described promising results for the concentration of P.knowlesi-infectedmonkey erythrocytes. Preliminary results with P.berghei-infected mouse erythrocytes are also promising. Leucocyte and platelet contamination in separated cell suspensions, a problem which should always be considered and the steps taken to eliminate them described, can be reduced to a minimum. There are several examples in the literature where this factor does not appear to have been satisfactorily controlled. This may distort the findings considerably. We consider that it is generally necessary to think of parasite metabolism as being so integrated with that of the host erythrocyte that the system must be studied as a metabolic complex; however, there are occasions when it is useful to study the parasite in isolation. Methods of isolation have mainly employed the use of haemolytic anti-serum and complement or surface-active agents such as saponin. Recent electron microscopic studies (Cook et al., 1969; Killby and Silverman, 1969) have revealed the possible hazards of these methods of isolation. Host-cell contamination of parasites is a frequent occurrence and can be a potential source of error when differences between parasite and host-cell biochemical and physio-chemical characteristics are being determined. The effects of these liberating agents may be far reaching

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and may even produce changes in those biochemical features of the host cell mentioned above, with the result that grossly misleading information may be obtained. Rupture of, or damage to the liberated parasites may make such preparations of questionablevalue in metabolic studies. It is therefore important that such possible consequences are considered when this kind of approach is necessitated. Thus it is clear that work with most types of cell preparation present their particular hazards. These should, however, not deter workers from choosing the preparation which they consider is the best means of giving them the information they require, but it must be emphasized that adequate steps should be taken to overcome the problems outlined. It is equally important to convince others that such steps have been taken.

C.

PENTOSE PHOSPHATE PATHWAY ACTIVITY IN MALARIA-INFECTED ERYTHROCYTES

Considerable attention has been focused on this metabolic pathway since it was suggested, by analogy with the sickle-cell gene, that genetically determined deficiency of human erythrocytic glucose-6-phosphate-dehydrogenase (G-6-PD), the initial enzyme of the pathway, could afford some degree of protection against infection with P. falciparum (Motulsky, 1960; Allison and Clyde, 1961). Results of field and hospital studies to investigate this hypothesis have been conflicting (see Gilles et al., 1967). Metabolic studies to investigate whether malaria parasites utilize this pathway appear to have also produced conflicting results. On theoretical grounds, it seemed probable that the malaria parasite could have an absolute requirement for the pentose phosphate pathway (PPP), even if considered only from the point of view that it is probably the principal, if not the only, pathway for the production of the pentose sugars necessary for nucleic acid synthesis. Bowman et al. (1961) used specifically labelled 1%-glucose to determine the extent of the participation of the PPP in the breakdown of glucose by P. berghei-infected mouse erythrocytes and by freed parasites. They came to the conclusion that this represented only a minor route of glucose utilization. Fletcher and Maegraith (1962) found that levels of G-6-PD and 6-phosphogluconate-dehydrogenase (6-PGD) in erythrocytes from monkeys infected with P. knowlesi rose with increasing parasitaemia, presumably reflecting increased PPP activity. Increases in the dehydrogenases were mainly restricted to the parasitized erythrocytes. They could find no dehydrogenase activity in parasites liberated by a variety of methods, suggesting that the parasite is dependent on the PPP of the host erythrocyte. A similar conclusion could be drawn from the radioactive studies of P. berghei by Bryant et al. (1964). Herman et al. (1966) used specifically labelled glucose in their studies on P. gallinaceum-infected chicken erythrocytes and found that PPP activity increased on erythrocyte infection. At the same time no activity could be detected in liberated parasites. Langer and his colleagues (1967) also studied the dehydrogenases of the

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PPP, and three pentose cycle enzymes, in P. berghei infections in mice; on the basis of electrophoretic and kinetic observations they suggested that P. berghei itself has an active pentose phosphate pathway. Their electrophoretic evidence is debatable because although they were able to show bands of G-6-PD activity with different mobilities from uninfected erythrocytes and from extracts of liberated P. berghei, it is significant that they were able to show only one band with infected erythrocytes with a mobility similar to that obtained from normal erythrocytes. Attempts in this laboratory to reproduce these electrophoretic findings in P. berghei and also P . knowlesi infections have so far been unsuccessful, only one zone of G-6-PD activity being demonstrable in each case. It could be argued that all the biochemical approaches mentioned above are open to some criticism,because, just as it is possible to get host-cell contamination of parasite preparations, it could be claimed that soluble enzymes (as G-6-PD is reputed to be) may be leached out of parasite preparations by washing procedures. In an effort to overcome some of these difficulties Theakston and Fletcher (1971a, b) adopted a different approach. They used a cytochemical procedure at the electron microscope level to determine the localization of G-6-PD activity in infected erythrocytes ( P . gallinaceum, P. berghei, P. knowlesi and P.fakiparum in Aotus). Activity was demonstrable only in the host erythrocyte, none being present in any parasite except in food vacuoles with recognizable host-cell contents. Here again, it could be suggested that diffusion of enzymes out of the parasite may have taken place or that the reaction components did not gain access into the parasite. It seems reasonable to suggestthat the incubation procedure necessary for demonstration of enzyme activity would maintain a metabolically viable system in almost a native state. Moreover, some demonstrable enzyme activity within food vacuoles indicates that parasite membranes were not impermeable to reaction components. Further indirect support for the above observations that malaria parasites are completely dependent on the G-6-PDYand possibly the 6-PGD, of the host erythrocyte is provided by the recent work of Luzzatto et al. (1969). They used a cytochemical method at the light microscope level to demonstrate that G-6PD-deficient human erythrocytes were rarely infected with P. falciparum while erythrocytes with a normal enzyme content in the same individual (female heterozygotes) were found to be frequently infected. This indicates clearly the dependence of the parasite on the G-6-PD of the host erythrocyte. The studies of Pollack et al. (1966) who investigated the effects of chemical agents which simulated the metabolic limitations of G-6-PD-deficient red cells in P . berghei malaria have some relevance in this respect. It would seem therefore that whereas field and hospital studies are always likely to be open to criticism, if only on statistical grounds, there is now a substantial amount of evidence to indicate that most, if not all, of the malaria parasites studied to date are dependent on the G-6-PD, and probably the PPP, of the host erythrocyte; parasites are unlikely to thrive in enzyme-deficient cells, at least not to the extent where they are able to produce an overwhelming infection.

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D. FURTHER METABOLISM OF GLUCOSE

Although the central role of glycolysis in the breakdown of glucose by plasmodia has been firmly established for many years, the nature of further metabolism beyond this metabolic sequence remains enigmatic, particularly in the case of the mammalian species of malaria parasites studied. Early work established that there was malonate inhibition of the aerobic oxidation of various substrates by avian species, indicating the presence of an active Krebs cycle, whereas no inhibition by malonate of glucose oxidation by P.knowlesi was observed (see Moulder, 1948). The following discussion therefore refers mainly to current trends of work with mammalian species. Recent work indicates that in P. knowlesi no homolactate breakdown of glucose occurs (Scheibel and Miller, 1969; Ali and Fletcher, 1971a). The preliminary report of the latter workers states that for each micromole of glucose utilized, one micromole of lactate accumulates and one microatom of oxygen is consumed. Pentose phosphate pathway activity could account for no more than 20 % of this oxygen uptake. This suggests that glycolytic intermediates are being diverted, perhaps to oxidative steps, or that there is further metabolism of pyruvate. Cenedella et al. (1969), working with P. berghei in rats, found that a significant amount of tritium from 6-labelled glucose was incorporated into parasite phospholipids exclusively via a-glycerol phosphate, no tritium label being found in the total fatty acids of the parasite. This suggests that triose phosphates are being utilized either via dihydroxy-acetone phosphate and glycerol-phosphate dehydrogenase activity, or via glyceraldehyde phosphate, and the action of glyceraldehyde kinase, glycerol dehydrogenase and glycerol kinase. Both sequences involve reductive steps using reduced nicotinamide-adenine-dinucleotide(NADH or NADPH), so that there is no possibility of oxidative mechanisms being involved. However, any surplus of glycerol phosphate formed by the second sequence, or otherwise, could be oxidized aerobically by glycerol-phosphate dehydrogenase to dihydroxyacetone-phosphate which could with glyceraldehyde-3-phosphate, then complete an aerobic glycerol cycle. Alternatively, a situation somewhat similar to that observed in some trypanosomes (Grant el al., 1961), may be present in malaria parasites. It is interesting to note that early work on the carbohydrate metabolism of several parasites showed that glycerol as substrate alone would maintain, and in the case of P. knowlesi apparently enhance, their oxygen uptake (see McKee, 1951). It cannot be ruled out that glyceraldehyde-3-phosphate dehydrogenase can also operate aerobically in parasites. Another explanation for the heterolactate degradation of glucose could be that 2,3-diphosphoglycerate, which is present in red cells in relatively high concentrations and is intimately concerned with haemoglobin in oxygen transport (Benesch and Benesch, 1969), accumulates in infected erythrocytes. No evidence for this was found in P.berghei-infected mouse erythrocytes (Ali, Fletcher and Maegraith, 1971). Usually, decreases in the amounts of this phosphate ester occurred during infection. Firm information on the further metabolism of pyruvate by mammalian

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parasites is still lacking, although more recent work is shedding new light on the possibilities. As already stated, the work of Cenedella et al. (1969) with P. berghei showed that there was no significant labelling of fatty acids from tritiated glucose, indicating that if acetyl-CoA is formed from pyruvate little, if any, is diverted towards de novo synthesis of fatty acids. Various workers have shown that there is little radioactive COZproduction by malaria parasites from 6-14C-glucoseindicating that there is insignificant Krebs cycle activity either in free parasites or infected erythrocytes. P.berghei and P. knowlesi particularly have been examined in this respect (Bowman et al., 1961; Scheibel and Miller, 1969; Ali and Fletcher, 1971a). It should however always be borne in mind that the possibility of dilution of radioactive intermediates between glucose and any oxidation in the Krebs cycle means that the yield of any radioactive COz from 6-14C-glucose is always likely to be relatively low compared with the evolution of labelled COz from l-14C-glucose in the pentose phosphate pathway. In this case only two or three enzymatic steps take place prior to the oxidative decarboxylation of 6-14C-giucose. Scheibel and Miller (1969) also used 3,4-14C-glucose in their studies on liberated P. knowlesi and showed some evolution of radioactive COz which indicates decarboxylation of pyruvate to a Cz-compound. This suggests the presence of pyruvic dehydrogenase activity, and the subsequent formation of acetyl-CoA. These workers did not consider that the addition of CoA increased the yield of l4COZin the above system although their figures could be interpreted as indicating the reverse. Much of the earlier work, particularly on mammalian parasites (see Moulder, 1948) showed that lactate as substrate maintained oxygen uptake at a level similar to that with glucose. The recent work by Ali and Fletcher (1971a) indicates that lactate and pyruvate will stimulate the endogenous respiration of P. knowlesi-infected erythrocytes, the respiration in the presence of lactate exceeding that of glucose. They also reported that malonate does not inhibit glucose-, lactate- or pyruvate-stimulated respiration. In these circumstances it is not easy to explain this respiration, if it is accepted that there is insignificant Krebs cycle activity, unless it is envisaged that there is a very active pyruvic dehydrogenase operating aerobically. There seems to be little possibility of oxidation of any lipid substances formed from acetyl-CoA and apart from a reversal of glycolysis leading to oxidation of glycerol phosphate, as outlined earlier, explanation of this stimulation of respiration by lactate is difficult. The only other possibility is that pyruvate undergoes transamination with glutamate to alanine and that alanine then undergoes oxidative deamination back to pyruvate, in a reaction analogous to that catalysed by glutamate dehydrogenase. Obviously, this would produce no net removal of pyruvate and is therefore unlikely to be a mechanism of any significance. The above account shows that, in the absence of a Krebs cycle, which is discussed in a later section, the respiration of mammalian malaria parasites is still inexplicable, although the possibility of an active and aerobic pyruvic dehydrogenase is currently under investigation in our laboratory. In this context it is worthwhile bearing in mind the work of Trager (1954, 1966) and Bennett and Trager (1967) on P. lophurae which indicated the dependence of

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this parasite, at least, on supplies of co-enzyme A, necessary for the above enzyme reaction, from the host erythrocyte. It is feasible that in mammalian parasites generally, supplies are limited and impose some restrictions on this reaction and any other which are co-enzyme A-dependent. E.

CARBON DIOXIDE FIXATION BY MALARIA PARASITES

The mechanism of C02 fixation by Cs-compoundsin certain micro-organisms and mammalian tissues is well established (see Wood and Utter, 1965). It is only relatively recently that this mechanism has been demonstrated in plasmodia, first in P. lophurae-infected duck erythrocytes (Ting and Sherman, 1966) and then in P.knowlesi-infected monkey red cells by Sherman and Ting (1968). Siu (1967) showed that C02 fixation occurred in liberated P. berghei and also demonstrated the presence of two of the enzymes involved, phosphoenolpyruvic carboxylase and carboxykinase in cell-free preparations. He showed that both enzymes could be inhibited by chloroquine and quinine. C02 fixation by liberated P. berghei and infected rat erythrocytes was also demonstrated by Nagarajan (1968a). The products of C02 fixation were shown in each case to be C4-dicarboxylic acids which are normally associated with the Krebs cycle. The studies of Ting and Sherman (1966) and Sherman and Ting (1968) on the kinetics of radioactive labelling of C4-compounds in P. lophurae- and P. berghei-infected erythrocytes respectively following incubation with 14C-bicarbonateindicated that oxaloacetic and a-ketoglutaric acids were the initial products of this reaction, with the amino acids, aspartate and glutamate appearing as stable secondary products. Their work also indicated that radioactivity appeared rapidly in other dicarboxylic and also tricarboxylic acids normally present in the Krebs cycle. The rapid labelling of these acids suggested to these workers that C02 fixation by the parasites was serving an anaplerotic function. Kornberg (1966) described anaplerotic sequences (from the Greek for “filling up”) as “routes ancilliary to the (central) cycles which must operate to maintain the levels of intermediates in these cycles”. This is necessary so that, when intermediates are tapped off from the central cycles to be built into anabolic products, the cycles will not be interrupted. The importance of this mechanism is not easily understood, particularly in mammalian parasites in which the majority of workers think that a functional Krebs cycle is unlikely to be present. In this respect it is interesting to note that the labelled amino acids, the major products of COz fixation in P.lophuraeinfected erythrocytes, were not incorporated into parasite protein. It is also worthwhile to note in all the studies mentioned above that the incorporation of radioactive C02 into either free parasites or infected erythrocytes amounted to about 1% of the added radioactive bicarbonate. In these studies it is relatively easy to explain the rapid labelling of aspartic acid by transamination of oxaloacetate, an initial product of C02 fixation. The rapid labelling also of a-ketoglutarate and glutamic acid is more difficult to explain. Either oxaloacetate is rapidly converted via citrate and iso-citrate to a-ketoglutarate in a conventional Krebs-cycle manner with subsequent

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transamination to glutamic acid or an as yet unknown COz-fixing mechanism gives rise to x-ketoglutarate directly. The first alternative would of course require the participation of acetyl co-enzyme A and citrate synthase. It is worthwhile noting that, in the studies using P. lophurae- and P. knowlesiinfected erythrocytes, significant amounts of labelled citrate and iso-citrate were reported to be found.

F. AEROBIC MECHANISMS I N MAMMALIAN MALARIA PARASITES

Many electron microscopic studies of the asexual stages of malaria parasites have shown that whereas the avian species studied all possess typical protozoan mitochondria with tubular cristae, the mammalian species do not appear to possess recognizable mitochondria, although trophozoites of P.falciparum in Aotus monkeys have structures which resemble mitochondria (Smith et al., 1969). Smith and Theakston (1970) in a short study of P. malariae-infected blood from two patients, observed structures which appeared to be typical protozoan mitochondria. Apart from these two exceptions, the ultrastructural studies agree with the biochemical evidence so far available on these species. For instance, the classical studies of Speck et al. (1946) showed quite clearly that P. gallinaceum fulfilled all the biochemical criteria necessary to show that it possesses a Krebs cycle. On the other hand, the work of Bowman et al. (1961) on P. berghei and more recently that of Scheibel and Miller (1969) and Ali and Fletcher (1971a) with P.knowlesi shows that these mammalian parasites do not possess a Krebs cycle as judged by the standard criteria. It is interesting to note that Ladda (1969) and Howells (1970) reported the presence of mitochondria in trophozoites of certain strains of P. berghei, which they considered to contain villus-like cristae. However, the latter worker found that these cristate mitochondria were rare and stated that such parasites usually possessed acristate mitochondria, unlike the erythrOcytic sexual and sporogonic stages of P.berghei in which typical protozoan-type mitochondria could be recognized. It may seem a little premature at this stage to consider that organelles without recognizable morphological features can be described as mitochondria, although the general hypothesis proposed by Howells (1970) of mitochondria1 metamorphosis during the life cycle of P. berghei is attractive. In this respect it is worthwhile to note that the electron cytochemical study of Theakston et al. (1969) showed that cytochrome oxidase activity in trophozoites of P.berghei were more frequently associated with the concentric-membraned organelle than with other membranes of the plasma, nuclear or food vacuole membranes or the “acristate structures”. Similar studies of NADH- and NADPH-dehydrogenases in the erythrocytic stages of P. berghei also showed that this “oxidative enzyme complex” was again mainly associated with the concentric membraned organelle. In neither case was enzyme activity particularly concentrated in the relatively structureless organelles termed “acristate mitochondria”. Moreover, Howells and his colleagues (1970) could not detect succinate dehydrogenase activity in normal drug-sensitive P. berghei trophozoites in contrast to chloroquine-resistant

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strains. These biochemical considerations,therefore, are another factor making it difficult to describe these organelles as mitochondria at this stage. Biochemical studies by Nagarajan (1968b) on blood from P . bergheiinfected rats, however, demonstrated progressive stimulation of oxygen uptake by free parasites by increasing concentrations of succinate and also inhibition of this stimulated uptake by malonate. This is in contrast to the findings of other workers already mentioned. The host cells in this infection were reticulocytes which can often present problems particularly with regard to contamination of free parasite preparations. It is interesting to note that this worker, like Howells et al. (1970) working with P. berghei-infected mouse erythrocytes, was unable to demonstrate succinate dehydrogenase activity in cell-free extracts of free parasites. The only demonstrable enzymes normally associated with the Krebs cycle were malate dehydrogenase and fumarase, two cycleenzymeswhich are found in mature human erythrocytes(see Prankerd, 1961). The presence of malate dehydrogenase has previously been demonstrated in extracts of P. berghei by Sherman (1966), who also reported that the electrophoreticand kinetic characteristics of the parasite and host-erythrocyte enzyme were different. It is still not possible, therefore, on the evidence available to date to get a clear picture of aerobic mechanisms in mammalian species. What is clear, however, is that if COZkation by these species takes place at a significantlevel it must be accepted at present that the Krebs-cycle sequence from oxalacetate to a-ketoglutarate through citrate does function, since a reversal of the steps of the conventional Krebs cycle sequence from malate to a-ketoglutarate via succinate is extremely unlikely, certainly on thermodynamic grounds. Moreover, co-enzyme A participates in one of the intermediate steps of the reverse sequence and may be limited in supply even for the metabolism of pyruvate, as mentioned in an earlier section. If the enzyme sequences normally associated with the Krebs cycle are restricted to a shuttle operating at the most to between malate and a-ketoglutarate, it is difficult to envisage a significant role for the cytochrome oxidase activity (Theakston et al., 1969; Scheibel and Miller, 1969) and NADH- and NADPH-dehydrogenases (Theakston et al., 1970), and co-enzyme Q (ubiquinone) system (Skelton et al., 1969) already demonstrated in mammalian parasites. The possibility remains that these are associated with aerobic mechanisms operating in the glycolytic sequence, further metabolism of pyruvate or side reactions of glycolysis, as discussed earlier. G . THE METABOLISM OF CHLOROQUINE-RESISTANT MALARIA PARASITES

To date, only a limited number of reports on the aerobic and carbohydrate metabolism of drug-resistant parasites have appeared. These have all been carried out on chloroquine-resistant strains of P. berghei in the mouse. Cho and Aviado (1968) used an oxygen-electrode system to compare the oxygen uptake of control mouse erythrocytes with those parasitized with drugsensitive P. berghei and a chloroquine-resistant strain. Comparison of the oxygen uptakes by the sensitive and resistant strains is difficult because of

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differences in the respective erythrocyte infection rates. A lack of data on reticulocyte levels in the two infections also makes the results difficult, if not impossible, to interpret. The latter is an important consideration since it is well established that a preference for immature red cells is a feature of chloroquine-resistant strains of P . berghei (see Peters, 1970). Preliminary investigations in our laboratory have attempted to take this factor into consideration. Table I compares the figures for the oxygen consumption of erythrocytes infected with a drug-sensitive and a drug-resistant strain of P . berghei with those for mouse blood in which an approximately equivalent level of reticulocytes to that occurring in the resistant strain had been induced by bleeding. TABLEI The oxygen consumption of mouse erythrocytes infected with chloroquine-sensitiveand chloroquine-resistantP. berghei, and with elevated reticulocyte levels (Boonyun and Fletcher, unpublished observations)

Cell suspension N strain P. berghei,

drug-semitive RC strain P. berghei, chloroquineresistant Reticulocyte-rich mouse blood

Erythrocyte infection rate (%) 72 60 66 67 0 0

Reticulocyte level (%)

Oxygen consumption (patoms/lOecells/h)

100.

+

++

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rediae seek out the sporocysts, following them even into the tentacles. In 27 tentacles of 60 doubly-infected snails 33 mother sporocysts were seen after 6 days and rediae were already found in 12 tentacles (compared with a single redia found in 1 tentacle among the singly-infected echinostome controls). 7. Speed of completion of larval dominance Manifestation of dominance is expressed by disappearance or significant decrease in larval stages of the subordinate species, with particular emphasis on cessation or prevention of cercarial shed. The speed of such end-stages is doubtless influenced by the time interval between the paired infections and number of miracidia in each experimental combination. The studies conducted in our laboratories in Kuala Lumpur and San Francisco demonstrate the broad spectrum of intensity and strength of the interaction. A remarkable example of highly effective predation is the case of E. audyi studied in Malaysia by Lie (personal communication). He obtained cessation of Fasciola gigantica cercarial shed in laboratory tests in as short a period as 12-13 days, and of Trichobilharzia brevis in only 18-26 days. On the other hand, it takes over 60 days for E. malayanum to cause S. spindale to stop shedding cercariae. By this criterion E. malayanum is a weak antagonist, although the final measure of strength is the total interaction of the various parameters of the interaction plus the effect it has on the host snail. In the S. mansonifP. segregatum model studied in B. glabrata, 10 doublyinfected and 10 singly-infected snails with S. mansoni controls were maintained in small aquaria within the same larger tank, using a common circulation as previously described. Snails were examined over 90 days for shedding of schistosome cercariae, beginning 3 days after exposure to P. segregatum. Table XIV indicates the diminution of schistosome cercariae shed by the doubly-infected snails. After about 6 weeks of interaction, the average schistosome cercarial shed per snail fell below 100. Subsequently, only a few cercariae were shed. Cercarial output from the S. mansoni controls remained at a high level and undiminished throughout the study. 8. Third-generation sporocysts of S . mansoni In histological sections of double infections with P. segregatum and S. mansoni, we frequently have seen unusual structures within the schistosome daughter sporocysts that resembled young daughter sporocysts (Figs 24, 25,26,27). Lie (1969a, c) described these bodies as third-generation schistosome sporocysts. They appear to have developed from germinal cells in an injured or modified daughter sporocyst. When many third-generation sporocysts were found inside an injured second-generation larva, the germinal cells along the wall were observed to have been sharply decreased in number. This unusual sporocyst generation has only rarely been observed in singly-infected S. mansoni snails (Lie, 1969c). Apparently certain sporocysts, whether from injury or other trauma, or normal variability, are able to cease producing cercariae and to produce instead additional, albeit modified daughter sporocysts. Whether this is simply an injury reaction or an adaptive change to replace lost sporocysts from redial attacks, we have no way to determine. Dinnik

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and Dinnik (1964) demonstrated with Fasciola giguntica that the usual succession of redia followed by cercaria production can be manipulated to produce only redial stages when the temperature is lowered, and can produce mixed generations at an intermediate temperature range. E. barbosai rediae infected with microsporidia appear to develop additional redial stages, in addition to the cercarial one (Lie, 1969b). Gordon et a/. (1934) in their early description of the intramolluscan stages of S. mansoni and S. haematobium observed that the first stage of development is a local multiplication of sporocysts near the site ofpenetration by the miracidium, followed by migration of motile sporocysts, which they called “Type I sporocysts”. After these sporocysts arrived at the liver they became motionless and developed into “Type I1 sporocysts”, which are found only in the liver. Type 11 sporocysts were said to vary greatly in size, owing to the fact that some were recently formed by multiple splitting off from others. Further change later took place in the liver and then “Type TI1 sporocysts” developed, which eventually gave rise to cercariae. Maldonado and Acosta-Matienzo (1947) considered Type 111 sporocysts to be the bodies that broke away from Type 11 sporocysts. Pan (1965), assuming Type 1 sporocysts to be mother sporocyst stages, rejected the thesis of Gordon et al., because mother sporocysts ordinarily do not migrate. Gordon’s views of sporocyst formation by multiple splitting involving 3 generations, were not accepted by subsequent workers, such as Faust and Hoffman (1934), Maldonado and Acosta-Matienzo (1947), Olivier and Mao (1949), Pan (1965). Yet, the possibility of a third sporocyst generation in the schistosome life-cycle remains an interesting challenge as to whether it is a rare, an abnormal, or an injury response. Recent work with sporocyst transplantation, pioneered by Chernin (1 966) and repeated by DiConza and Hansen (1972) may add to a better understanding of the normal range of sporocyst development. The latter workers have demonstrated, by inoculation of individual daughter sporocysts into digestive gland tissue of E. glabrata, that these implanted sporocysts produce additional sporocysts, which produce normal cercariae. DiConza and Basch are currently investigating the nature of this multiplication by in vitro studies (personal communication). Hansen (personal communication) has been able to show the presence of daughter sporocysts within daughter sporocysts in vivo in the liver of E. glabrata kept at 28”C,over a period of more than 2 months after inoculation. Presence of young daughter sporocysts freely active in the liver in these older infections strengthens the view that sporocyst multiplication of S. mansoni is not so rigidly restricted to 2 generations as has formerly been believed. B.

HISTOLOGICAL OBSERVATIONS

1. P. segregatum superimposed on S . mansoni Snails harbouring 30-day S. mansoni, then re-exposed to 20 P. segregaturn miracidia, were prepared for histological study. Forty-six snails with double infections were fixed 1, 3, 6, 9, 1 1 , 13, 16, 18, 20, 25, 27, 34, 38,41,46, 53, 60 and 90 days after exposure to P. segregatum. Forty-five snails with a single P. segregatum infection, 3 1 single-infection S. mansoni snails, and 36 uninfected

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snails served as controls, being fixed along with each pair of experimental snails. The P . segregatum miracidia penetrated and developed in schistosomeinfected snails in their usual locations. Though their sporocysts were smaller during the first week of infection than in controls (Figs 28-31), no host cellular response was seen against them. Initial appearance of mother rediae in the snail tissues was delayed about a week, as was migration of daughter rediae to the ovotestis area (Figs 32-36). Daughter rediae within rediae, along with germballs and cercariae, could still be seen after 26 days (Fig. 37). In doubly-infected snails, rediae were concentrated in the hepatopancreas where the S. mansonidaughter sporocysts were located, rather than in the usual site in the ovotestis, as in the control infections. Rediae reached the liver as quickly as the 18th day in double infections. Considerable damage to the organ was done by the time a number of rediae had crowded into it (Figs 38,39,40). The ovotestis region was very lightly parasitized until about the seventh week, owing to the diversion of echinostome rediae from their normal site in the ovotestis, presumably until the food source in the liver was exhausted. After rediae had been among the schistosome daughter sporocysts for several weeks, the latter began to show injury owing to the combination of redial attack and a strong host tissue reaction (Lim, 1970a; Figs 41,42, 43,44). S. mansoni daughter sporocysts usually retained the integrity of their body wall, a remarkably resistant structure, though an occasional redia broke through and entered the sporocyst body. Striking concentrations of amoebocytes around the injured daughter schistosome larvae appeared to press in on the weak spots of the unbroken but doubtless injured sporocyst body wall (Figs 45, 46). The larvae appeared edematous, with depositions of host fibrous tissue visible on them. Encapsulated schistosome sporocysts occasionally showed lysis of their germinal contents, though direct infiltration of encapsulated sporocysts by host amoebocytes seldom was seen (Figs 7,s). Occasionally a schistosome daughter sporocyst escaped severe injury and retained well-developed cercariae (Fig. 47). As noted previously, this explains the irregular shedding of small numbers of schistosome cercariae from a few doubly-infected snails often after very long periods. By the time most schistosome larvae had been encapsulated by the host tissue response, the echinostome rediae migrated to their normal ovotestis location. The host gonads were gradually consumed by these echinostome larvae, as occurs in single-speciesP . segregatum infections (Figs 48,49). 2. S . mansoni superimposed on P. segregatum B. glabrata, about 5 mm diameter, were exposed to 10 P . segregatum miracidia. After 39 days, 50 of these snails shedding P . segregatum cercariae were exposed to 50 S. mansoni miracidia. Controls were previously noninfected snails of the same age, also exposed to 50 S. mansoni miracidia. P . segregatum single-infection and non-infected controls were also established.

FIGS28-34. (28), Single infection with 2-day P. segvegutum sporocyst in B. glubrutu foot. Arrow indicates an eye-spot, 300 x ; (29), Double infection in B. glubrufu: 2-day P. segrezut ~ sporocyst m in snail previously infected with 32-day S. munsoni infection (not visible), foot. Arrow indicates eye-spot, 175 x ; (30), Single infection with 5-day P.segregurum sporocyst in B. glubrufu foot. Arrow indicates wall of sporocyst, note well-developed redia, 280 x ; (31), Double infection in B. glubruru: 5-day P. segregufum sporocyst in snail with 35-day S. munsoni infection, note repressed development compared with (30), foot, 250 x ; (32) and (33), Double infection in B. glubrutu: S. munsoni (day 50) and P.segregufirm (day 20). Crosssections of liver area, 80 x (32) and foot-head, ovotestis-liver areas, 70 x (33). Note absence of rediae in ovotestis region, but presence in anterior region (arrows); (34), Double infection in B. glubratu: S. munsoni (day 64) and P. segregutum (day 34). Observe absence of rediae in the ovotestis, the usual site in single infections at this age (Figs 35,36).

FIGS35-42. (35) and (36), Single infection of P. segregafum in B.glubrufu:arrival of redia in ovotestis (day 9), 7 5 x (35); and complete destruction of this organ in a well-developed infection (day 77), 17.5 x (36); (37)-(42), Double infections in B. glubruta. Daughter rediae inside a first-generation redia (S. mansoni, day 56, and P. segregufum, day 26), 300 x (37); Damage to liver area and encapsulated daughter sporocysts (arrows), (S. mansoni, day 90, and P . segregatum, day a), 17.5 x (38); Damage to liver area, showing redia attacking sporocyst (arrow), (S. mansoni, day 83, and P. segregatum, day 531, 30 x (39); Enlargement of portion of Fig. 39, t o show one redia in vicinity of sporocysts, 70 x (40); Encapsulated S. mansoni daughter sporocysts (S. munsoni, day 120, and P . segregufum, day YO), 70 x (41) and (42).

FIGS43-49. Double infections in B. glabraia. (43), S. mansoni (day 71) and P . segregairrrn (day 41), predatory activity of redia inside daughter sporocyst, liver, 7 0 x ; (44), S. mansoni (day 120) and P . segregatum (day 90), redia inside schistosome sporocyst, enclosed by host reaction, liver, 300x ; (45) and (46), S. mansoni (day 120) and P . segreguium (day 90), host tissue reactions (arrows) to injured schistosome sporocysts, liver, 188 x ; (47), S. mansoi (day 120) and P . segregaium (day 90), showinguninjured S. mansoni sporocyst, note absence of host tissue response, liver, 70 x ; (48), S. mansoni (day 90) and P . segregatum (day 60), rediae filling in ovotestis, 10 x ; (49), S. mansoni (day 120) and P. segregatum (day 90), showing delayed migration of rediae into usual site (ovotestis), after mass destruction of sporocysts in liver area, 5 x

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FIGS50-55. Double infections in B. glabrata. (501, P. segregarum (day 40) and S. mansoni (day I), schistosome mother sporocyst in tentacle (arrow) shortly after penetration, 188 x ; (51), P . segregatirm (day 45)and S. mansoni (day 6 ) , uninjured schistosome mother sporocyst in tentacle, 75 x ; (52) and (53), P. segregatum (day 60) and S. mansoni (day 21), massive proliferation of rediae and single still surviving sporocyst (arrow), liver, 17.5 x (52); enlarged portion near arrow of Fig. 52, showing strong host tissue response around daughter sporocyst, 175 x (53); (54), P . segregarum (day 196) and S. mansoni (day 157), encapsulated schistosome sporocyst, liver, 75 x ; ( 5 9 , P . segregatum (day 204) and S. mansoni (day 165), encapsulated schistosome sporocyst, liver, 280 x .

Samples of experimental and control snails were fixed from the first day after the schistosome challenge exposure, and at various intervals thereafter for 165 days. Schistosome mother sporocysts began to develop in a normal fashion at the miracidial site of entry (Fig. 50) until the P. segregurum rediae appeared and began to consume them. This happened as quickly as 3 days after the S. munsoni exposure. Three or four small rediae usually attacked a single developing mother sporocyst, which rapidly degenerated (Figs 17, 18). Occasionally, a

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schistosome mother sporocyst survived and went on to produce daughter sporocysts (Fig. 5 1). One or more daughter sporocysts might subsequently reach the normal site in the hepatopancreas and develop cercariae (Figs 52,53), but usually most daughter sporocysts were sufficiently damaged by rediae (though seldom killed) to stimulate a strong encapsulation response by the host (Figs 54, 55). This aspect proved to be of particular interest. It was one not fully appreciated until we had undertaken a histological study of the interaction process. That is, the contribution of the host’s cellular response, leading to suppression of the subordinate parasite, S. mansoni. Though the predatory rediae seldom succeeded in destroying the schistosome daughter sporocysts, they frequently damaged them, or released stimulating material, resulting in the host’s encapsulation response. In single S. mansoni infection, daughter sporocysts generally develop and grow in the liver with no apparent host cellular recognition or reaction. After cercarial shed begins, as Pan (1965) has observed, some cellular response is manifested, especially against cercariae trapped in host tissues. He suggested that the generalized tissue response is incited primarily by the cercariae and that precercarial stages “sensitize” the snail tissue, causing it to respond promptly and intensively to the stimulus provided by cercariae after they have escaped from the daughter sporocysts. Contents of sporocysts that leak out during cercarial breakthrough may have elicited this generalized tissue response. In the case of S. mansoni daughter sporocysts attacked by P. segregatum rediae, the host tissue response is indeed severe. Frequent redial sucking on the daughter sporocyst body wall may have caused leakage of the larval contents, which may have served to stimulate the host’s amoebocytes and result in the fibrotic response. The possibility of the intact parasite surface serving as a camouflage against detection either by absorption or by incorporation of host material into the larval body wall to deceive the host’s defense mechanism was considered b$Heyneman et al. (1971a). Salt (1960,1968) demonstrated the role of the parasite surface among insect parasitoids as a defensive mechanism against host hemocytes. In our system, redial attacks on the schistosome wall may have broken this mimicry. Experiments are under way in our laboratory to explore this possibility further.

v.

TREMATODE ANTAGONISM IN BIOLOGICAL CONTROL

The relatively new field of biological control has been developed to achieve a highly specific form of control of agricultural insect, weed, or any other undesirable pest organism by use of natural predators or pathogens (see general reviews in Sweetman, 1958;DeBach, 1964). Discussion of the principles of competitive displacement and coexistence can be found in DeBach and Sundby (1963), and DeBach (1966), one of the founders of this field. Results have at times achieved spectacular success, as in the control of citrus scale by parasitic wasps in California, or of the feral European rabbit in Australia with myxomatosis. Most applications of biological control of fluke diseases, such as schistosomiasis and fascioliasis, have, prior to the development of trematode inter-

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action as a possible approach, focused on the snail intermediate host. Michelson (1957) has summarized these efforts to develop effective parasites, pathogens, and predators of snails, which vary from haplosporidia (Barrow, 1965), to amoebae (Richards, 1968), Tetrahymena ciliates (Michelson, 1971), through the full range of nematodes (Mengert, 1953; Chernin et a]., 1960; Chernin, 1962), leeches (McAnnally and Moore, 1966), fish (Davidie and Metge, 1965; Mvogo and Bard, 1964) to ducks and geese. Johnson (1968) has assembled a valuable compendium of references to the pathology of invertebrates, a major portion of which is devoted to pathogenic agents and pathology of molluscs. Stephenson and Knutson (1966) have reviewed the associates of slugs, a good example of the number and variety of potential mollusc biological control agents. Berg (1964) reviewed data on parasitoids of snails, with particular reference to his remarkable discoveries with the molluscicidal larvae of sciomyzid flies. Important biological background studies are included in Foote (1 959) ; Neff (1966); Neff and Berg (1 966); Knutson and Berg ( I 967); Bratt et al. (1969). Population dynamics were studied in the laboratory by Geckler (197 1). Competition between Marisa cornuarietis and B. glabrata has been studied and field experiments attempted in Puerto Rico with varying success by Ferguson et al. (1958); Oliver-Gonzalez and Ferguson (1959); Demian and Lutfy (1966); Ferguson and Butler (1966); Butler et a/. (1969); Ruiz-Tiben e f a/, (1969); Jobin and Berrios-Duran (1970); Jobin et a/. (1970). Another approach to biological control of trematode diseases would be by controlling the free-swimming larval stages. Reports have appeared on predatory activity or toxic effects against trematode miracidia and cercariae by rhabdocoele turbellaria (Holliman and Mecham, 1971); hydrozoans (Mattes, 1949); oligochaete annelids (Backlund, 1949; Ruiz, 1951 ; Khalil, 1961 ; Wajdi, 1964; Boray, 1964); mosquito larvae and planarian exudates (Chernin and Perlstein, 1971); Cyclops, Daphnia, and Cypridopsis crustacea (Courmes et al., 1964); guppy, Lebistes reticulatus (Oliver-Gonzalez, 1946; Pellegrino el a]., 1966; Knight et al., 1970), and aquatic plants (Gibson and Warren, 1970). Biological misdirection and other forms of interference with miracidial hostfinding capacity were tested experimentally by Chernin (1968) and by Chernin and Perlstein ( I 969). Hyperparasitism of the intramolluscan trematode stages by microsporidia, summarized in Dollfus’ monographic review (1946), has been described by Martin (1936), Dissanaike (I 957a, b), Schaller (1 959, 1960), Cort et al. ( I 960a, b), Canning and Basch (1968), Lie and Basch (1970). These sporozoan parasites show a distinct specificity for the trematode and not the mollusc host tissue, although degrees of specificity to the trematode larvae vary widely. The Nosenza species described by Cort et al. (1960a) infects strigeoid parasites, whereas Perezia helnzinthorurn Canning and Basch, 1956 can infect all of the trematode larvae to which we have exposed it in many snail hosts, both aquatic and terrestrial (and a variety of other aquatic organisms as well, such as oligochaetes and mosquito larvae-Lie, personal communication). However, the role of microsporidial hyperparasitism in biological control is probably not one that can be employed as an independent tool. I t often, however, may become

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an important adjunct to other control measures. In the Malaysian field trials, Perezia appeared abundantly in the larvae of most trematodes once high infection levels of the controlling echinostome agent had been reached. This proved to be one of the major factors in the total infection complex in these field tests (Lie et al., 1970, 1971), and similarly in other regions may be an important and unanticipated parameter or limiting factor in future biocontrol effectiveness of trematode antagonism. Other protozoan or microbial infections, such as parasitic or facultative amoebae, may also add an unexpected factor in the intramolluscan biome, as we have discovered, on occasion, to our dismay. The unusual type of specificity in which only parasite and not snail tissue is involved appears confined to the microsporidia. The trematode antagonists-the chief focus of our attention for the past six years-select trematodes as food or affect them by other means, but also consume mollusc tissues and severely debilitate the snail hosts. Intramolluscan inter-trematode antagonism as a new approach to biological control (Wright, 1968; Berrie, 1970) began with the laboratory studies already reviewed. It was followed by the small-plot field efforts in Malaysia to control S. spindale with E. malayanum in Indoplanorbis exustus, also discussed in this review and by Heyneman and Umathevy (1968), Lie (l969a, b, 1971), Lie e t a / . (1970, 1971). These studies are continuing with the E. audyi-T. brevis system in L. rubiginosa snails and E. audyi-Fasciola gigantica in the same hosts by Lie and co-workers. A very rapid and complete degree of control has been achieved with E. audyi, particularly against T. brevis (Owyang and Lie, personal communication). Comparable studies with local strains of dominant echinostomes are being carried out in Thailand by Lie and colleagues. The encouraging results achieved to date would appear to justify field trials against human schistosomes in various endemic areas, where the problems faced and lessons learned undoubtedly will differ very greatly. At the present time, echinostomes are favored for control of schistosomiasis or fascioliasis, but a variety of other redia-producing predatory forms must be isolated and tested for use in other areas if trematode biocontrol is to be broadly applied. This, in fact, is a problem that probably will keep this a local, or at least a regional approach. In biological control of insects, local strains of controlling agents generally are of little value, and extensive search must be made for imported biocontrol agents. With trematodes, the opposite condition appears to be true. A key factor in success of control by trematode antagonism is strong infectivity of the competing antagonist in the snail harbouring the target species. This entails (1) a high rate of infection by a single miracidium, in (2) all ages of host snail, in (3) its full range of natural habitats, followed by (4) rapid growth and development in spite of a preceding trematode infection. Though a sufficiently strong or infective species may overcome local strain differences among various snail populations, such differences (of both snails and parasites) may greatly alter the characteristics of host-parasite adaptation from region to region. It is therefore unlikely that we can expect to find a single trematode species so broadly adaptive and so powerful an antagonist that it could serve as a biocontrol agent in areas other than those in which it is endemic and already adapted to the local snail or strains. Perhaps a few

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powerful or active predators (such as P. segregatum and E. audyi) will prove to be exceptions to this generalization. But we feel that the main effort to develop trematode biocontrol should be made locally, by study of the regional trematode fauna in the infected area in order to discover endemic rediaproducing candidate agents that are not infective to (or pathogenic in) man or his domestic animals. The selected agents should then be tested against the target trematode in the local snail strain, followed by larger-scale field pond experiments, as test results and local conditions permit. This raises an obvious objection : if local host-adapted antagonists are most effective, why hasn’t control already occurred naturally? It reminds one of the equally challenging query made to the stockbroker: “If you’re so smart, why ain’t you rich?” Perhaps the answer, too, is analogous: egg, concentration of host and available capital. It is necessary to seed selected disease transmission hostspots with large numbers of eggs of the antagonist in order to raise the infection level to one far higher than ordinarily would occur in nature. The inevitable adaptive interplay of numerous ecological factors would be expected to keep natural infection levels low. Unless a high proportion of host snails become infected, control by trematode interaction cannot occur. Only under artificially crowded, man-created conditions can one ordinarily expect to find snailinfection levels much above 25 %. The more usual condition is an infection rate ranging from less than 1 % to about 5 % of the snail population. Since a relatively small number of snails infected with a disease-producing trematode usually can still sustain transmission, we must artificially maintain a very high infection level to control the target trematode in the entire snail population. There are therefore two important distinctions between biological control by introduced insect parasites (or parasitoids) and trematode antagonism. Both characteristics are possible disadvantages to trematode biocontrol. For the latter to occur, we must (1) use a predator already adapted (or preadapted) to the host snail, and we must (2) artificially raise and sustain a high snail infection rate with the dominant parasite. Insect biocontrol depends upon introduction of an agent against which the local target species is not adapted, so that little resistance is offered to an epidemic spread of the controlling agent. The external environment, presumably, offers few obstacles to the agent’s spread. The important limiting factors are those that affect host numbers, concentration, and natural resistance to infection or predation. Trematode biocontrol, on the other hand, depends upon an agent that is adapted to the local host, the snail. Lack of such adaptation may mean failure to respond to host signals or enzymes, lack of tissue compatibility, or imbalance of any of the little-understood characteristics that determine specificity of infection. The controlling agent must clear the snail hurdle before it can even approach its target. The snail is therefore the limiting environment, which imposes very real barriers to a newly introduced trematode species. Once inside the snail and successfully multiplying, there is little reason to believe that the antagonist would not dispatch the prey trematode, providing it is a strongly predaceous, rapidly-growingform. The other obvious obstacle to a self-sustainingcycleis the necessity for a vertebrate final host. Although specificity for the final host is seldom as extreme as for the intermediate host, the extra steps of a transport 12

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host or some means to carry the metacercaria to the final host, and the various limitations associated with the final host make it highly unlikely that a selfsustaining life cycle can be counted on to achieve control of the disease agent. For the echinostomes we have tested, snails and other aquatic organisms are readily available and easily infected transport hosts. In most of these species, water birds and rodents serve as final hosts, easily maintained and reinfected. The key for field use is a sufficient concentration of infective eggs to sustain the high snail infection levels required for biocontrol. The life cycle may well be self-maintaining without such an effort, but then usually at a low or sporadic level, unsuitable for biocontrol. The cycle must be maintained artificially, then, in order to keep up the required snail infection level. In a life cycle that requires a rare final host or a host difficult to sustain, practical field use of such a trematode is not possible. P . segregatum, a powerful, effective control agent, is an example. Its only known vertebrate hosts are vultures and other raptorial birds-not especially suitable for mass-rearing of eggs, though vultures are easily cage-adapted and relatively long-lived for experimental purposes. This requirement imposes other pre-conditions for a trematode antagonist suitable for biocontrol: (1) an appropriate number of the required vertebrate final host, (2) readily procured and inexpensively maintained, and (3) easily infected and reinfected, to allow (4) a high continuous production of hardy eggs that ( 5 ) can be frequently harvested and stored without hatching under laboratory or controlled conditions (Lie and Owyang in preparation). The comparison between insect and trematode models of biocontrol would be more apt (and accurate) if it compared hyperparasitoid-parasitoid-host insect with trematode antagonism. In this more biologically complex mode1 of insect biocontrol, the hyperparasite depends for survival upon suitability of its parasitoid host, much as the trematode antagonist depends upon suitability of its snail host. An important difference, of course, is that the hyperparasite, to the degree it reduces the predator population or efficiency, is a negative value to the control system. Development of theoretic models and comparisons between these systems is currently under way in our laboratory by A. Kuris (unpublished observations). The trematode model has still other biological levels of complexity : microsporidial infection of both the predatory and target trematode; reduced life span of snails that serve as hosts of the dual infections; and the castration of host snails by echinostome rediae and cercariae in the snail ovotestis. Differential mortality and cessation of egg production by infected snails has been a significant factor in all of the biocontrol field tests we have so far undertaken. Equally important has been the presence (or absence) of a high infection rate with Perezia helminthorum. Lie et al. (1970) found that microsporidia appeared spontaneously once the echinostome infection reached a high level, but that apparently the echinostomes were more affected than were the schistosomes. As a result, a number of examples were found of snails simultaneously shedding both species of cercariae, a three-way interaction in which the microsporidia tipped the scales in favor of the schistosomes. Eventually, however, a combination of snail death and successful echinostome antagonism eliminated the schistosomes. In a subsequent field trial in the same pond, a microsporidial

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epidemic did not occur, or at least was delayed until schistosome control by the echinostome predators was nearly complete. Echinostome superinfection developed normally, r ' dual cercarial shed occurred, and control of the subordinate parasite was readily achieved (Lie et al., 1971). These interacting factors in trematode biocontrol-echinostome infection level, microsporidial epidemic, and snail death-are intimately related. Both the microsporidial epidemic and snail castration and death reached significant levels only after the echinostome level was artificially raised to a very high level, perhaps 70 % or more of the snail population. The combination may serve the same ends-control of the disease agent, whether by death of the host or the target trematode. But the complexities they pose and possible perturbations of the interaction cannot be predicted, as in the preceding example, and each infection system selected must be evaluated for its specific area. To do so will require careful laboratory study of the underlying parameters of hostparasite relationship surveyed in the present review. Perhaps the most unusual example of biological layering of complexity is one just now being studied in Malaya (Owyang and Lie, personal communication). They have developed a three-way trematode infection model consisting of Hypoderaeum dingeri, a relatively ineffectual echinostome antagonist, Trichobilharzia brevis, a bird schistosom'e,and E. audyi, a powerful echinostome antagonist. T. brevis sporocysts, interacting with H . dingeri rediae, most remarkably, can destroy the echinostome or reduce its rediae to granule-filled sacs, acting entirely by indirect antagonism (Owyang and Lie, 1971). This is the first example reported of domination of sporocysts over rediae (indirect over direct antagonism). These workers readily reinfected a group of snails, already shedding H. dingeri cercariae, with T. brevis. The schistosome was somewhat delayed in its early development, but succeeded in producing normal cercariae, while the echinostome rediae soon ceased shedding cercariae. The rediae lost their germinal contents or developed a third redial generation in place of cercariae, much as we described for S. mansoni in the presence o f P .segregatum. Eventually, schistosome domination was complete. The reverse sequence, T. brevis followed by H . dingeri, was an even more pronounced sporocyst domination. The echinostome miracidia penetrated freely and reached the site of mother sporocyst development in the snail heart, but no further development took place (Owyang and Lie, personal communication). However, when snails were exposed first to H . dingeri, and, after an appropriate period, to T. brevis and then to the highly predatory E. audyi, a remarkable interaction took place. H . dingeri, itself repressed by T. brevis, nonetheless exerted an inhibitory effect on development of the E. audyi, which thereby was blocked from destroying the schistosome. A three-way interaction interfered with the expected two-way interactions that would have occurred in the absence of the third species. An uneasy balance was produced, with the target schistosome being protected by a preceding infection with a subordinate species, which added enough inhibitory or indirect influence to block the direct antagonism of the predator, Addition of a microsporidial infection to this conglomerate of parasites would add a further complexity we hestitate to contemplate!

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These interaction possibilities are suggestive of problems that may well appear in field applications of biological control by trematode antagonism. Successful use of the technique in one area therefore cannot assure us that application elsewhere will be equally successful, however similar the conditions may appear to be. Obviously, one success does not preclude a wider ranging success, but the method is sufficiently sensitive to local ecological conditions to suggest that a prior survey and testing of local trematode strains should precede initial field trials. Nonetheless, it is our view that such efforts should be made in endemic areas and that even the most modest chance for success must not be ignored, in view of the growing urgency of schistosomiasis spread. If the antagonist life cycle can be sustained easily and inexpensively and eggs produced in large numbers, local application of biocontrol may be quite feasible in selected areas of high transmission. Procedures not yet developed may make the process far more efficient and easily sustained at the local level. At present we seed with eggs that have been isolated from laboratory host faeces and then incubated under carefully managed conditions. It would be far simpler and less costly to use raw animal faeces or perhaps a filtered faecal product kept for a week and then applied within a day or two of normal hatching. Simple floating trays or screens of faecal matter might prevent eggs from sinking into the mud or being washed from areas where snail infection is desired. Relatively small numbers of laboratory-infected animals currently provide great numbers of eggs. Some 20 or 30 pigeons for E. audyi and 30 rats for E. malayanurn support the studies now under way in Malaysia (Lie, personal communication). Larger-scale technology can easily be developed once the basic usefulness of the approach is established for a given area. The potential advantages of biocontrol are sufficiently promising to justify the initial effort to consider and evaluate it where conditions appear to make a trial feasible. The initial steps required to locate a trematode antagonist, isolate and test it in the laboratory, and select the appropriate strain or species among eligible candidates (outlined in Fig. 56) will have to be done at a major laboratory with appropriate facilities and, most important, experienced personnel. Such laboratories do exist or could be activated in most university medical centres in endemic areas. An important factor simplifying setting up these studies is the possibility of using local snail and trematode strains, without costly search in other areas, as has traditionally been done with insect parasitoids. Furthermore, the sensitive problem of importing “foreign” parasites is avoided, though of course the responsibility is nonetheless important to select an appropriate antagonist species, one non-pathogenic to domestic animals or man. Once the process of selecting the parasite predator has been completed, maintenance of the cycle, standardization of procedures, and longterm application of eggs should be feasible and quite inexpensive, even in regions distant from the developmental laboratory. If trematode antagonism could be teamed with other means of control, chemical, biological, clinical, and sanitary, the chance for long-term success would be greatly enhanced (as proposed in a Societyfor Invertebrate Pathology symposium, Levine, 1970a, with special reference to the review of integrated control of snails-Levine, 1970b). It might prove especially useful to tie

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COLLECT FIELD SNAILS (schistosonie intermediate hosts), select out: Snails + for echinostome metacercariae

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‘ I Collect eggs; establish snail colony

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FIG.56. Suggested sequence in search for local schistosome antagonists in known snail hosts.

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molluscicide application, with its high kill ratio but brief duration, to biocontrol of the few remaining snails and of the newly hatched snails, highly vulnerable to infection, that escape chemical death. Rapid recolonization of chemically decimated snail colonies, soon reinfected by continued recontamination of the water with egg-laden human faeces, is the often-repeated fate of molluscicide campaigns without concomitant sanitary control and clinical treatment. In such areas of continuous high-level transmission, biocontrol may help bridge the time interval between control of cercarial shed by infected snails and of egg-shedding by man (especially infected children). Sustained, frequently repeated seeding with eggs of an effective trematode antagonist in limited areas of high transmission danger might eliminate schistosomes from the few remaining infected snails (and in all probability eliminate the snails as well). More important, the eggs could infect newly hatched and newly arrived snails at a high enough level to provide a buffer zone of pre-infected snail hosts, intractable to infection with schistosomes or other target trematodes.

VI. SUMMARY The study of intramolluscan single and double trematode infections has proved to be a useful approach to a better understanding of this ancient hostparasite relationship. Modification and disruption of snail infection with trematodes is reviewed in terms of our laboratory studies, particularly those of Dr Lie Kian Joe, to whom this review is dedicated. The parameters and characteristics of various infection combinations are described. Possible application of this knowledge to trematode biological control by introduction of rival parasites into snail populations infected with a disease agent remains a major source of interest in this work. Biologically, however, the inter-trematode reactions and the responses of the snail host offer remarkable opportunities to examine and isolate various aspects of this host-parasite relationship. The basic system used as a reference model is the interaction between Schistosoma mansoni (NIH strain) and the echinostome Paryphostomum segregatum in Biomphalaria glabrata (NIH albino strain). The single species infection patterns differ widely between the pure sporocyst type, exemplified by S. mansoni, and the redial type, typified by P. segregatum. Characteristics of each are reviewed. Their interaction is then reviewed, based on original data and comparison with other studies. Redial predation (“direct antagonism”) is discussed in terms of relative activity, efficiency, and predatory response to triggering stimuli in the snail. Sporocyst influence (a purely “indirect antagonism”, whereas rediae can show both) is viewed as a repressive influence on rate of development and time of migration of rival stages, and a cause of cytolysis of germinal material within these stages. This indirect effect may be a direct toxic or competitive inhibition or be acting as a stimulus to a tissue response by the snail. Possible mechanisms of indirect antagonism are reviewed, with a fuller consideration of snail immunity as induced by these infections and measured experimentally. Quantitation of these interactions is not yet possible, but the parameters or

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characteristics of single-species infection are described and related to one another in a preliminary fashion as an “adaptation index” (AI), which includes such parameters as infection rate, period for 50 % snail death, and period to cercarial shed. A species with a higher A1 is presumed to possess greater dominance in an interaction with a species having a lower index in a specific host snail. Other factors that influence predatory capacity must eventually be incorporated in any measure of potential value of a trematode for use as a controlling agent. These include: (1) localization in the snail, (2) vigor and speed of onset of predatory response, (3) pharyngeal size and gut length of predatory redia, (4) number of rediae produced, (5) toughness of body wall of the prey species, (6) relative adaptation or degree of success of each species in the snail host species (or geographical race). Initial data and background are reviewed for determination of an “interaction index” using the P. segregatum-S. nzansoni model in B. glabrata. Successive steps in the interaction are described, both for superinfection of the echinostome on the schistosome and the reverse sequence, as suggested by experimental data. Modification of infection rate and developmental period and of the redial migratory pattern are useful indicators of the intertrematode influence. Schistosome daughter sporocysts under attack will produce third-generation sporocysts instead of cercariae, a particularly interesting indication of an indirect effect by rediae. Intertrematode injury will initiate a tissue response by the host snail that is often well marked and suggestive of a well organized defensive response by the host. Questions of the capacity of host snails to demonstrate an immune response are reviewed in some detail. These findings are then evaluated for possible application in the biological control of human schistosomiasis and other trematode diseases of man and domestic animals. Preliminary field trials, already completed and still underway in Malaysia by Lie and colleagues, are reviewed. Results are promising, but important limitations and uncertainties of the approach are evident. Basic differences, advantages and disadvantages are explored between trematodetrematode-snail interaction and the insect prey-parasitoid approach to biological control. We conclude that the trematode method is locally applicable, using indigenous strains supplied and sustained at a high level by continual reseeding with eggs of the controlling trematode (or processed faeces from the appropriate final hosts). Effective biocontrol as a self-sustaining life-cycle appears highly improbable, as is the expectation that this method can be adopted on a wide scale with the same controlling agent. Yet, for intensive use in restricted areas of high infection transmission, the approach may well prove to be valuable and research should be initiated to develop improved methods and isolate additional species in endemic areas that might be useful as antagonists. Biocontrol, in our view, offers limited but possibly important usefulness, especially if teamed with other control methods, such as molluscicide, sanitary, and therapeutic. REFERENCES

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Ruiz-Tiben, E., Palmer, J. R. and Ferguson, F. F. (1969). Biological control of Biornphalariaglabrata by Marisa cornuarietis in irrigation ponds in Puerto Rico. Bull. Wid Hlth Org. 41, 329-333. Saint-Guillain, M. (1968). Etude histologique des premiers stades evolutifs de Fasciola hepatica L. Acta Zool. Path. Antwerp 46, 77-131. Salt, G. (1960). Surface of a parasite and the haemocytic reaction of its host. Nature, Lond. 188, 162-163. Salt, G. (1961). Competition among insect parasitoids. I n “Symposia of the Society for Experimental Biology”, No. 15, pp. 66-1 19. Cambridge University Press. Salt, G. (1963). The defense reactions of insects to metazoan parasites. Parasitology 53,527-642. Salt, G . (1967). Cellular defense mechanisms in insects. Fed. Proc. 26, 1671-1674. Salt, G. (1968). The resistance of insect parasitoids to the defense reactions of their hosts. Biol. Rev. 43, 200-232. Salt, G. (1970). “The Cellular Defense Reactions of Insects.” Cambridge University Press. Saoud, M. F. A. (1965). Susceptibilities of various animal intermediate hosts of Schistosoma mansoni to different strains of the parasite. J . Helminth. 39,363-376. Saoud, M. F. A. (1966). Susceptibility of some planorbid snails to infection with Schistosoma rodhaini from Kenya. J. Helminth. 40, 379-384. Sasanov, A. M. (1957). Epizootiology and control of fascioliasis in ruminants. Veterinariya 34, 28-30. Schaller, G. (1959). Microsporidienfall and Degenerationserscheinungen der Trematodenlarven im Zwischenwirt (Tropidiscus planorbis). Z . wiss. Zool. 162,144-190. Schaller, G. (1960). Hyperparasitismus bei Trematoden-eine zusatzliche Bekampfungsmoglichkeit ? Urania 19, 35-38. Schwabe, C. W. and Kilejian, A. (1968). Chemical aspects of the ecology of platyhelminthes. I n “Chemical Zoology” (Eds M. Florkin and B. Scheer), Vol. 2, pp. 467-549. Academic Press, New York and London. Simmonds, F. J. (1953). Parasites of the frit-fly Oscinella frit L. in Eastern North Africa. Bull. ent. Res. 43, 504-542. Southgate, V. R. (1970). Observations on the epidermis of the miracidium and on the formation of the tegument of the sporocyst of Fasciola hepatica. Parasitology 61,177-190. Standen, 0.D. (1952). Experimental infection of Australorbis glabratus with Schistosoma mansoni. I. Individual and mass infection of snails and the relationship of infection to temperature and season. Ann. trop. Med. Parasit. 46,48-53. Stauber, L. A. (1961). Immunity in invertebrates, with special reference to the oyster. Proc. nut. Shellfish Ass. 50, 7-20. Stephens, J. M. (1963). Immunity in insects. I n “Insect Pathology. An Advanced Treatise” (Ed. E. A. Steinhaus), Vol. 1 , pp. 273-297. Academic Press, New York and London. Stephenson, J. W. and Knutson, L. V. (1966). A rksumb of recent studies of invertebrates associated with slugs. J. econ. Ent. 59,356-360. Stirewalt, M. A. (1954). Effect of snail maintenance temperatures on development of Schistosoma mansoni. Expl Parasit. 3, 504-51 6. Stunkard, H. W. (1946). Possible snail hosts of human schistosomiasis in the United States. J. Parasit. 32,539-552. Stunkard, H. W. (1960). Further studies on the trematode genus Himasthla with descriptions of H . mcintoshin. sp., and stages in the life-history of H . cornpacta n. sp. Biol. Bull. 119, 529-549.

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Stunkard, H. W. (1966). The morphology and life history of the digenetic trematode, Himasthla littorinae sp. n. (Echinostomatidae). J. Parasit. 52, 367-372. Sudds, R. H., Jr. (1960). Observations of schistosome miracidial behaviour in the presence of normal and abnormal snail hosts and subsequent tissue studies of these hosts. J. Elisha Mitchell Sci. SOC.76, 121-133. Swales, W. E. (1935). The life-cycle of Fascioloides magna (Barri, 1875) the large liver-fluke of ruminants in Canada. Can. J. Res. 12, 177-215. Sweetman, H. L. (1958). “The Principles of Biological Control.” W. C. Brown Co., Iowa. Taylor, A. E. R. and Baker, J. R. (1968). “The Cultivation of Parasites in vitro.” Blackwell, Oxford and Edinburgh. Timberlake, P. H. (1910). Observations on the early stages of two aphidiine parasites of aphids. Psyche 17, 125-130. Tripp, M. R. (1963). Cellular responses of mollusks. Ann. N.Y. Acad. Sci. 113, 467-474. Tripp, M. R. (1969). Mechanisms and general principles of invertebrate immunity. In “Immunity to Parasitic Animals” (Eds G. J. Jackson and I. Singer), Vol. 1, pp. 111-128. Appleton, New York. Tripp, M. R. (1970). Defense mechanisms of mollusks. RES-J. reticuloendoth. SOC. 7, 173-182. Tripp, M. R. (1971). Immunity in invertebrates. In “Aspects of the Biology of Symbiosis” (Ed. T. C. Cheng), pp. 275-281. University Park Press, Baltimore. Ubelaker, J. E., Cooper, B. and Allison, V. F. (1970a). The fine structure of the cysticercoid of Hymenolepis diminuta. I. The outer wail of the capsule. 2. ParasitKde 34,258-270. Ubelaker, J. E., Cooper, B. and Allison, V. F. (1970b). Possible defense mechanisms of Hymenolepis diminuta cysticercoids to hemocytes of the beetle Tribolium confusum. J. Invert. Path. 16, 310-312. Ubelaker, J. E. and Olsen, 0. W. (1970). Influence of temperature on survival rate and infectivity of miracidia of two species of Phyllodistomum (Trematoda) to pelecypods. J. Invert. Path. 16, 363-366. Ullyett, G. C. (1943). Some aspects of parasitism in field populations of Plutella maculipennis Curt. J. ent. SOC.S . Afr. 6, 65-80. Van derPlank, J. E. (1968). “DiseaseResistance inPlants.” Academicpress, New York. Van Steenburgh, W. E. and Boyce, H. R. (1937). The simultaneous propagation of Macrocentrus ancyfivorus Roh. and Ascogaster carpocapsae Vier. on the peach moth (Luspeyresia molestu Busck), a study in multiple parasitism. Rep. ent. SOC.Ont. 68,2426. Vernberg, W. B. and Vernberg, F. J. (1968). Interrelationships between parasites and their hosts. IV. Cytochrome c oxidase thermal-acclimation patterns in a larval trematode and its host. ExplParasit. 23,347-354. Vernberg, W. B., Vernberg, F. J. and Beckerdite, F. W., Jr. (1969). Larval trematodes: double infections in common mud-flat snail. Science 164, 1287-1288. Von Brand, T. (1966). “Biochemistry of Parasites.” Academic Press, New York and London. Wajdi, N. (1964). The predation of Schistosoma mansoni by the oligochaete annelid Chaetogaster. J. Helminth. 38, 391-392. Wajdi, N. (1966a). Penetration by the miracidia of S. mansoni into the snail host. J. Helminth. 40, 235-244. Wajdi, N. (1 966b). Immunity to Schistosoma haematobium in Bulinus truncatus. Trans, R. SOC.trop. Med. Hyg. 60,774-776.

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Waksman, S. A. (1945). “Microbial Antagonism and Antibiotic Substances.” Commonwealth Fund, New York. Warren, K. S. (1967). Studies on the treatment of molluscan schistosomiasismansoni with antibiotics, non-antibiotic metabolic inhibitors, molluscicides and antischistosomal agents. Trans. R. SOC.trop. Med. Hyg. 61, 368-372. Warren, K. S. and Weisberger, A. S. (1966). Suppression of schistosomiasis in snails by chloramphenicol. Nature, Lond. 209,422423. Webbe, G. and James, C. (1971). The importation and maintenance of schistosomes of human veterinary importance. In “Isolation and Maintenance of Parasites in vitro” (Eds A. E. R. Taylor and R. Muller), Symposia of the British Society for Parasitology, Vol. 9, pp. 77-107. Blackwell, Oxford and Edinburgh. Wesenberg-Lund, C. (1934). Contributions to the development of the trematoda digenea. Part 11. The biology of the fresh water cercariae in Danish fresh waters. D. Kgl. Dansk. Vidensk. Selsk. Skr. Nature Math. Afd. Raekke 9,1-223. Wilson, R. A. (1971). Gland cells and secretions in the miracidium of Fasciola hepatica. Parasitology 63, 225-231. Wilson, R. A., Pullin, R. and Denison, J. (1971). An investigation of the mechanism of infection by digenetic trematodes: the penetration of the miracidium of Fasciola hepatica into its snail host Lymnaea truncatula.Parasitology 63,491-506. Winfield, G . F. (1932). On the immunity of snails infested with the sporocysts of the strigeid, CotylurusfIabelliformis, to the penetration of its cercariae. J. Parasif. 19,130-133. Wood, R. K. S. (1967). “Physiological Plant Pathology.” Blackwell, Oxford and Edinburgh. Wright, C. A. (1966a). Relationships between schistosomes and their molluscan hosts in Africa. J. Helminth. 40,403412. Wright, C. A. (1966b). The pathogenesis of helminths in the mollusca. Helmintli. Abstr. 35, 207-224. Wright, C. A. (1968). Some views on biological control of trematode diseases. Trans. R. SOC.trop. Med. Hyg. 62,320-324. Yarwood, C. E. (1967). Response to parasites. In “Annual Review of Plant Physiology” (Eds L. Machlis, W. R. Briggs and R. B. Park), Vol. 18, pp. 419-438. Annual Reviews, Palo Alto. Zischke, J. A. (1966). Studies on the early development of the digenetic trematode Echinostoma revolufum (Froelich). Ph.D. thesis, Tulane University, New Orleans.

Taeniasis and Cysticercosis (Tueniu suginutu) ZBIGNIEW PAWLOWSKI

Clinic of Parasitic Diseases. Przybyszewskiego 49. Poznah. Poland AND

.

MYRON G SCHULTZ

Center for Disease Control. U S. Department of Health. Education and Welfare. Atlanta. Georgia. U.S.A. I . Introduction .................................................................................... I1. Nomenclature .......................................... ......................................

.

111 Hosts of Tueniu suginutu ........................... ...................................... IV . Structure and Biology of Tueniu suginutu ................................................ A Adult ....................................................................................... B. Egg ..................... ................................................................. C. Onchosphere .............................................................................. D Cysticercus ................................. ................................. V . Clinical Aspects of Taeniasis (T suginutu) ................................. A Symptomatology ........................................................................ B. Clinical Pathology ..................................................................... C. Diagnosis ................................................................................. D . Treatment ................................................................................. VI . Epidemiology and Epizootiology ......................................................... A . Transmission Between Man and Animals .......................................... B Epidemiological and Epizootiological Data ....................................... C. Losses Due to Taeniasis and Cysticercosis ....................................... VII . Prevention ....................................................................................... A . Meat Inspection .............................. ..................................... B Serological Diagnosis and Immunization of Cattle .............................. C Sanitation ................................................................................. References .................................................................................

.

. .

.

.

. .

269 270 271 274 274 278 279 280 282 282 285 287 289 295 295 299 303 304 304 306 306 310

“NO animal has been responsible for more hypotheses, discussions and errors than the tapeworm.” C . Davaine, 1860

I. INTRODUCTION Tapeworms have been known since prehistoric times-it is difficult indeed for the host to ignore the discharge of proglottides or fail to wonder about their origin. Tapeworms are referred to in the Papyrus Ebers. in Indian literature. in Chinese literature. and by Graeco.Roman. Byzantine and Arabian authors (Hoeppli. 1958). Many theories were held about the nature of tapeworms . 269

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They were viewed as products of spontaneous generation, as transformed strips of intestinal mucosa, or as a union of separate animals in a chain invested by a membrane formed in the intestine. The term cucurbitini was applied to proglottides not only because they look like seeds of the pumpkin (Cucurbita sp.) but also because pumpkin seeds were one of the earliest, effective treatments for tapeworm infection. Taenia saginata was recognized as a distinct species by Goeze in 1782. The relationship between the adult parasite and bladder worms of cattle was established by Leuckart in 1861 who fed gravid proglottides to a calf and obtained the larval stage. Eight years later Oliver reversed the procedure and infected man with cysticerci of cattle. In the century that has since passed a great deal of knowledge has been developed about this parasite, although work on the adult stage has been impeded by the inability to infect experimental animals. Taeniasis of man and cysticercosis of cattle have also been recognized as important public health and economic problems. In recent years several reviews have appeared dealing with selected aspects of cestodiasis but none has reviewed Taenia saginata infection in a comprehensive manner. Our aim in preparing this review is to summarize advances in all aspects of T. saginata taeniasis and cysticercosisnomenclature, host relationships, structure and biology, clinical and therapeutic features, epidemiology and epizootiology, and prevention, in the hope that our work will stimulate further inquiry and lead to better control of this zoonotic disease.

11. NOMENCLATURE At the outset we must indicate that there is considerable confusion about the nomenclature and the taxonomy of the parasite that is the subject of this monograph. At present, some unarmed tapeworms occurring in man are poorly understood (Huang, 1967) or doubtfully named. Indeed, in the last few years two different opinions have been expressed concerning the generic name of the unarmed tapeworm of man acquired from the consumption of beef. Both Taenia saginata and Taeniarhynchus saginatus are generic and specific names used for this parasite. The choice of name depends on whether unarmed human tapeworms belong to a genus separate from other tapeworms. The two opposite opinions on this point are best expressed by Abuladze and Verster. Abuladze 1964 (Principles of Cestodology, Vol. 4, Taeniata, p. 163) said “Perrier (1 897) and a number of other workers regarded Taeniarhynchus as a sub-genus of Taenia, and Holl (1919) used it as a synonym of Taenia, we cannot agree with these opinions because the presence or absence of hooks in teniid should be respected as a generic criterion. We and most present day working helminthologists regard Taeniarhynchus as a separate genus.” Abuladze’s opinion is in agreement with that of Wardle and McLeod (1952) who used the generic name Taeniarhynchus proposed by Weinland in 1859. Wardle and McLeod’s textbook probably popularized the generic name Taeniarhynchus, especiallyin Europe. On the other hand, Verster (1969) in a paper titled “A taxonomic revision of the geuns Taenia (Linnaeus, 1758)” disagreed with the use of the generic name

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Tueniarhynchus and says “The genera Tueniurhynchus Weinland (I 858) and Monordotaenia Little (I 967) (synonym : Fossor Honess 1937) are differentiated from Taenia oiily on the absence of rostellar hooks in the former and on a single row in the latter. A single character may justify the creation of a new species but it cannot be the sole criterion for the erection of a new genus. If the practice of basing a genus on a single character were to be consistently followed, it would necessitate the erection of four more genera to accommodate the eight species in which the genital ducts pass the longitudinal excretory vessels ventrally to cross into the cortex. This is, however, clearly unwarranted and the continued use of Tueniurhynchus and Monordotaeniu as well as Multiceps, Hydutigeru, and Tetrutirotaenia at the generic level would only lead to further confusion.” Venter’s opinion agrees with the earlier opinion of Joyeux and Baer (1929). Abuladze and Verster also disagree on the number of species of unarmed tapeworms of man. Abuladze (1964) distinguished T. africuna (Linstow, 1900), T. confusa (Ward, 1896) and T, hominis (Linstow, 1902) from Taeniarhynchw suginutus. However, Verster (1969) stated that these species are no longer valid and considers them all synonyms of Taeniu suginutu. The final verdict remains for the taxonomists to decide. In the meantime we have chosen, without prejudice, to use the generic name Taeniu suginatu for the common, unarmed tapeworm of man, and for human infection we use the term taeniasis (T. saginutu). We do have strong convictions about the term ‘‘Cysticercus bovis”. It is illogical to give a separate generic and specific names to the larval stage of a parasite that already has a distinctive name, therefore, the term “Cysticercus bovis”, although it enjoys common usage, should be cast into oblivion. For the term “Cysticercus bovis” we use “Taeniu saginata cysticercus” and for infection with “Cysticercus bovis” we use “Taenia saginata cysticercosis”. 111. HOSTSOF TAENIA SAGINATA

Man is the only definitive host of Taenia suginuta. Laboratory animals, including monkeys (Calrenburg, 1932, cit. Nelson et ul., 1965)failed to develop adult Taenia suginatu infections when fed with the intermediary stage. A very extensive search for adult Taenia saginata in Kenya carried out by Nelson et ul. (1965) in 271 wild primates revealed tapeworms of at least six different species, but none was Tueniu saginutu. Southwell (1921) described tapeworm proglottides (from a goat in Accra) which closely resembled Tuenia saginuta segments, however, no scolex was found and this observation is inconclusive. Cestode larvae are less host specific than adult cestodes, therefore, the list of intermediary hosts of Taeniu suginatu is considerable and expands as each year goes by. The main intermediary hosts for Taenia saginafu are domestic Bovidue. These include Bos tuurus, Bos bufellus, Bos indicus and Bos grunniens (see Abuladze, 1964). In recent years the reindeer (Rungifer turundus) has been added to the list of intermediary hosts. According to Abuladze (1964) raw reindeer meat was first implicated in 1956 as the source of T. suginuta infection in the Jamalsko-Nienecki region of the U.S.S.R. In 1960, Safronov

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found cysticerci in ten reindeer carcasses in the Oleniekski region of the U.S.S.R. and suggested that they might be cysticerci of T. suginutu because there are many individuals with tapeworm infection in the region (59 of 200 school children examined) and cattle are not bred in this area. In 1961 Krotov confirmed this observation in reindeer breeders at a state farm in the U.S.S.R. There are virtually no data about wild intermediary hosts of T. suginutu in the Americas. The one exception is a report in 1906 of infection in the llama and pronghorn antelope. However, in Africa unhooked cysticerci are sporadically found in wild animals: wildebeeste (Gorgon tuurinus) (Nelson et ul., 1965), bush-buck (Tregefuphus scriptus) (Tremlett, personal communication to Nelson et ul., 1965)and the tame oribi (Ourebiu ourebi) (see LeRoux, 1957). According to Nelson et ul. (1965) there are only a few records of T. suginutu cysticerci from African animals in zoological gardens ; they include giraffes (Railliet 1885, Schwartz 1928, Buckley 1947) and lemur (Hamerton 1934). In addition Maczulski (1941) (according to Abuladze, 1964) found cysticerci, probably of T. suginutu, in Guzeffugutturosuand Taylor (1958) found cysticerci of Tueniu suginuru in the liver of an onyx-antelope kept in a zoo. To the contrary Graber (1959) found cysticerci of Tueniu suginutu in cattle, camels, sheep, Dorcas gazelle (Guzeffudorcu), red fronted gazelle (Guzeffurusifrons) and other unspecified antelopes in the Chad Republic. This finding should be confirmed and further work is necessary to understand the role of wild animals in the potential spread of T. suginutu in Africa. There is one striking report concerning wild animals as intermediary hosts of T. suginutu in Asia. Among aborigines in Wulai District of Taiwan, Huang (1967) found 28 tapeworms with scoleces which he identified as T. saginutu. He successfully infected newborn calves with eggs of these tapeworms and produced cysticerci which differed in some respects from normal cysticerci of T. suginutu. Because there are no cattle in this area he suggested that wild goats might be a natural intermediary host of T. suginutu in this region. Boev (1960) pointed out that only experimental cross infections could prove a particular wild animal as the intermediary host of T. suginutu. For example, he corrected the improper finding of T. suginutu cysticercosis in roe-deer. Sometimes cross infection experiments raise further questions. Price (1961), for example, infected himself with some cysticerci from the liver of a giraffe and found that the adult worms differed from normal T. suginutu. He proposed the name of Tueniu suginutu var. giruffae. It has been suggested that this may be an example of morphologic variation caused by the transmission of a parasite to an abnormal host. There will probably never be a final list of all the intermediary hosts of T. suginutu. The most controversial question about these hosts is the role of man himself. Two different opinions have been expressed in recent years concerning cysticercosis of man. Nelson et ul. (1965) said that some cysts reported in man may be cysts of Tueniu saginutu or small hydatids. On the other hand, Verster (1967) commented on the discrepancy between the incidence of human cysticercosis and the incidence of adult Tueniu solium infection. She said that Tueniu solium infection may be not as rare as is generally assumed. As far as we are able to determine, 12 cases of Tueniu suginutu cysticercosis

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of man have been described in the literature. The older reports include: Arndt (1867, according to Meggitt, 1924), Nabias and Dubreuilh (1889, according to Meggitt, 1924), Heller (according to Abuladze, 1964), Fontan (1919), Watkins and Pitchford (1924, according to Brumpt, 1936), and Castellano et al. (1928). The more recent reports include: Naumov (1929), de Rivas (1937), Tanasescu and Repciuc (1939), Asenjo and Bustamente (1950), Niiio (1950), Bacigalupo and Bacigalupo (1956) and Goldsmid (1966). Naumov in 1929 reported the first case of human T. suginuta cysticercosis in the U.S.S.R. (Abuladze, 1964): the patient was a 40-year-old man who at autopsy had nine cysticerci discovered in his heart and one in the meninges and an adult T. saginata in the intestine. The cysticerci were hookless and were diagnosed by Naumov as cysticerci of T. saginata. A case in Pennsylvania was reported by de Rivas in 1937. Autopsy examination revealed numerous cysticerci distributed throughout all the muscles and the author’s description and drawing depict cysticerci with scoleces each with four suckers but without hooks. Tanasescu and Repciuc (1939) reported a 59-yearold Romanian woman with a tumor in the mammary region. Their paper presents seven photographs of cross sections through the unarmed scolex. They believed it was a cysticercus of T. saginata because it had “five suckers instead of four characteristic of Taenia solium larvae”. Since the photographs show rugae in the wall surface the diagnosis is probable. The patient also had tumors in other areas of the body. This case and a very similar case of Fontan’s (1919) probably came to the attention of the authors because of the suspicion of carcinoma in the mammary region. Asenjo and Bustamente (1950) in discussing 59 patients with cysticercosis in the Santiago de Chile Neurological Clinic mentioned that all but one were due to cysticerci of T. solium and stated that the other was due to cysticerci of Taeniasaginutu. No other details were given. Nifio (1950a, b) reported a case of C. bovis in a lymph node of the meso-appendix. Goldsmid (1966) in discussing human cysticercosis in Rhodesia mentioned that of 62 cases at Harari Central Hospital in Salisbury between 1955-1965 one was diagnosed as T. saginata cysticercosis but no proof was found in the records indicating the absence of hooks. In the report by Dixon and Lipscomb (1961) of 450 cases of cysticercosis in soldiers from India no mention is made of T. saginata cysticercosis. There is no doubt that hookless scoleces in cysticerci have been found in the human body. Also, there are instances where adult Taenia saginata infection occurs contemporaneously with human cysticercosis (Fontan, 1919; Naumov, 1929). It would be interesting to know, however, how many cases of cysticercosis due to T. solium in man or swine have cysticerci with unarmed scoleces, as well as what percentage of scoleces in each case are unarmed. From the theoretical point of view a parasite may find itself in an unexpected host or unusual tissue in very special circumstances, i.e. malignancy. These special conditions can occur in man but in the cases previously described none were noted. Cysticercosis of man due to T. saginata is still an open question. Its resolution is dependent on careful morphological examination of cysticerci removed from human patients.

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Iv.

STRUCTURE AND

BIOLOGYOF Taenia saginata

A. ADULT

Work on the morphology of adult T. saginata has attracted little interest during the past 20 years. However, there are two recent, important papers dealing with morphological aspects of T. saginata (Verster 1967,1969) and one observation by Rivero (1952) that described a new sphincter in the cirrus pouch of the adult T. saginata. Morphological studies of T. saginata have two important aspects; they often demonstrate abnormalities of structure and they reveal taxonomic variants of T. saginata which may be of epidemiological importance. Elsdon-Dew and Proctor (1965) and Verster (1967) claimed that the apparent scarcity of T. solium, at least in Africa, may be due to a misdiagnosis of the proglottides of T. suginata. For this and other reasons, it is worthwhile to present the important diagnostic features of T. saginata which will serve to differentiate it from T. solium. We have chosen four of the many works on this subject that cite the important diagnostic features of T. saginata. They are listed in Table I. Table I shows how different four authors’ criteria can be when considering the diagnosis of T. saginuta. Verster (1967) carefully points out those features that are unquestionably diagnostic of T. saginata. They are: (1) the presence or absence of an armed rostellum, (2) the number of ovarian lobes, and (3) the presence or absence of a vaginal sphincter. She completely discards the diagnostic value of the number of lateral uterine branches in the gravid proglottis. These differentiating features are important in doubtful cases. However, in most cases where the lateral uterine branches number more than 20-25 there is no need to complicate the routine diagnostic procedures by making permanent slides to look for the vaginal sphincter. Morphological abnormalities of T. saginata that have been observed for the past two centuries are presented in Clapham’s paper (1939). In a more recent summary of abnormal morphology of T. saginata, Burrows and Klink (1955) discussed abnormalities of the entire strobila (tri-radiation, tetra-radiation, penta-radiation, pigmentation and bifurcation) ; abnormalities of one or more proglottides (bifurcation, fenestration, fusion, variation in segmentation, supernumerary or intercalary segments); and variations in reproductive organs. Other more recent papers on morphological abnormalities of T. saginata are Pezenburg and Oleck (1955). Thlice and PBrei Moreira (1955), Starkoff (1956), Voge! (1961), Larrougy and Sardou (1963), Merdivenci (1964) and Kuimicki (1970). Owing to the introduction of new techniques, i.e. histochemistry and electron microscopy, knowledge of cestode structure and physiology has grown very rapidly and has been summarized in recent reviews by Read and Simmons (1963), von Brand (1 966) and Smyth (1 969). However, the physiology of adult T. saginata has not been as well investigated as other more readily available cestodes. For example, the ultrastructure of the tegument of nine different species of Cyclophyllidea has been examined but not that of T. saginata (see Srnyth 1969).

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TABLEI Specific morphological features of Taenia saginata that di.#er jkom Taenia solium

du Noyer and Baer Brumpt (1 928) (1949) ~

~

Entire body Length

Verster (1 967)

~~

4-8 ni

412 m

Maximal breadth 12-14 m m Approx. 2000 No. of proglot tides Scolex Diameter Shape Diameter of suckers Hooks Rostellum

Abuladze (1964)

1 ‘5-2 nim 1 ‘9-2 mni Quadrangular 0.7-0.8 mm Absent A bsen t Absent

Mature proglottides Musculature Calcareous bodies 300-400 Testes

Up to 10 m, exceptionally more 12-14 mni

-

1 5-2 inn1

Absenl

Well developed Very numerous 800-1 200 not confluent posterior to vitellarium

Terminal vesical Present Cirrus pouch

Absent

Ovary Vaginal sphincter Present Present Course of vagina Straight Irregular Genital atrium Alternate

2 lobes Present

Gravid proglottides Breadth to length 1 : 3 4 ratio No. of uterus 18-25 branch Way of leaving host

Absent Absent

15-30 18-32 Dichotomic Single and spontaneously

Does not extend to excretory vessels 2 lobes Present

Spontaneously

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According to Lunisden et al. (1970) the tapeworm body surface can no longer be considered “an inert cuticle”. It has a major role in integrating the parasite’s physiological activities with the immediate environment. Very little is known about the chemical constitution of the tegument of T. saginata, but it is known to show alkaline phosphatase activity (Chowdhury, 1955). According to Arme and Read (1970) the tegument of T, saginata, like that of other tapeworms, is probably a digestive-absorptive structure showing some morphological and functional similarities to the luminal mucosal structures of vertebrates. Apart from the works of Logachev (1953a, b) and Chowdhury et al. (1956a) little attention has been paid to the mesenchymal cells of T. saginata. These studies may provide some interesting information about the differentiation of cells in the hind part of the “neck” region of T. saginata which would help to explain details in the growth of the parasite (Logachev, 1953b). Much information has arisen about the calcareous corpuscles in T. saginata due to the work of Chowdhury et al. (1956d, 1962) and von Brand (1960, 1965, 1967) but their function still remains a mystery. Possibly they act to buffer anaerobically produced acids (von Brand et al., 1960)or as a reservoir of phosphates (Brand, 1966). Very little is known about the uptake of tagged substances into the body of T. saginata. In comparison to Diphyllobothrium latum, T. saginata absorbs only a small amount of vitamin B-12 (Nyberg, 1958) and it does not absorb CoB0(Scudamose et al., 1961). The presence of cholinesterase and acetylcholine-like substances (Artemov and Lure, 1941; Schardein and Waitz, 1955; Pylko, 1956) suggests that they may be transmitter substances in the nervous system of the tapeworm. The presence of glucose-6-phosphate and glucose-6phosphate dehydrogenase suggests that in carbohydrate metabolism a pentose phosphate pathway is active besides the pathway of Embden-Meyerhof (Ley and Vercruysse, 1955). The finding of purinolytic enzymes is difficult to interpret (Read and Simmons, 1963): a search for some antigenic substances is another source of information about proteins (Machnicka-Roguska, 1965) and mucopolysaccharides which appear to be concentrated in the scolex and first part of the strobila of T. saginata (see Marzullo et al., 1957). The biochemical analysis of lipids resulted in the finding of saturated and unsaturated fatty acids (cmelik and Bartl, 1956), some lipid-like lecithins, inositol phosphatides (von Brand, 1966) and cholesterol and other sterol-like material (C‘melik and Bartl, 1956). Due to the fine studies of PrBv6t et al. (1952) the normal site of attachment of T. saginata was found to be 40-50 cm below the duodenojejunal flexure. Only three of 53 patients with T. saginata infection had the scolex situated further down in the jejunum. Their observations indicate that the tapeworm is by no means passive or resting, but is itself often moving against intestinaI peristaltic motion in the host. Most radiologists find the tapeworm body in the ileum, some even located it in the terminal ileum. However, PrCv6t et al. (1952) pointed out that only the hind part of the tapeworm body may reach the ileum and this is the part most easily shown by radiological examination. The observations of PrBvBt et al. have been confirmed by Hornbostel and Dorken (1952).

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The entire body of T. saginata, including the scolex, has been found in several unusual locations such as the appendix, gall-bladder, and adenoid tissue of the nasopharynx (Shakhsuvarli et a/., 1964). In the latter case a 14-year-old girl more or less regularly discharged T. saginata proglottides from her nose. This condition started several days after a bout of vomiting and a feeling of some foreign body in her nasopharynx; it lasted, with some remittent periods, for more than one year. Part of the tapeworm body was found in material taken out by adenectomy and gravid proglottides were found in the posterior part of the nasopharynx. Prior to surgery she expelled 14 proglottides during a 4-day period, providing an example of a most unusual adaptation of the adult tapeworm to a luminal region other than the intestinal tract. The idea that T.saginataoccurs only in single infections is no longer upheld. This topic was discussed by Andrews and Ogilvie (1944), Vogelsang and Fernandez (1943, Mazzotti et al. (1947), Vieira (1954), Pawlowski and Rydzewski (1958), Altmann and Bubis (I959), Donckaster and Donoso (1960), Lee e t a / . (1966), and Strikovsky (1970). Donckaster and Donoso (1960) summarized five authors’ observations of 2020 Taenia sp. infections and found that the percentage of multiple infections is below 1 %: P e r u 4 . 2 9 % (Castillo, 1958), United Kingdom--O.46% (Jopling and Woodruff, 1959), Poland-456 % (Pawlowski and Rydzewski, 1958), C h i l e 4 . 8 5 % (Donckaster and Donoso, 1960). However, in Mexico the percentage of multiple infections was 4.9 % (Mazzotti et al., 1947) and it is very high in some endemic foci in the southern republics of the U.S.S.R., e.g. in Azerbaidjan multiple infection reached 40 % and in Armenia 67 % with an extraordinary maximum of I50 tapeworms in one person (Podyapolskaya and Kapustin, 1958). Evidently, the “crowding effect” operates in multiple T. saginata infections. For instance, in one patient with 16 tapeworms the lengths of the strobila was 50-80 cm (Altmann and Bubis, 1959). At present, the factors that account for single infections with T. saginata are not known and general belief is that superinfection does not occur. However, Hornbostel (1959) described a case in which three adults of T. saginata developed after the sequential ingestion of three cysticerci, the second administered 1 week after the first and the third 2 months after the first. The coexistence of T. saginata with other intestinal parasites is a most interesting biological phenomena. T. saginata can coexist with T. solium (Vogelsang and Fernandez, 1945; Mazzotti et al., 1947; Donckaster and Donoso, 1960; Strikovsky, 1970) or Diphyllobothrium latum (O’Connor, 1944). T, saginata infection is often found in association with Giardia intestinalis infection (Junod, 1967; Batko and Kacka, 1969). The specific reasons why tapeworms can withstand digestion during their life in the small intestine is not understood but we know that the ability to withstand digestion is a general attribute of all living membranes. The time of development from the ingestion of a cysticercus to a fully grown tapeworm has been established by Penfold et al. (1937a) as 100 days, and by Sztrom (1938) as 91 days; however, in recent years with the use of modern taeniacides the regeneration time appears to be up to 4 months (Frolova

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1970). Proglottides are expelled irregularly. As many as 34 proglottides may be expelled in 1 day but the mean daily output was found to be 6.6 by Belyaev and Monisov (1967) and nine by Penfold and Penfold (1936b). In a patient with artificial anus as many as 40 proglottides were discharged daily (BonillaNaar, 1946). Most proglottides are passive; but they become motile most commonly between the hours of 1-8 p.m. The length of life of an adult T, saginata appears to be limited only by that of the host. Spontaneous cure may occur but this is exceptional. B.

EGG

During the last 10 years the eggs of T. saginata have attracted much more interest than any other stage of the parasite. The development of taeniidae eggs has been summarized by Rybicka (1966). An interesting phenomenon pointed out by Kamalova (1953), and Silverman (1954b) is the uneven maturation of ova within proglottides. According to Silverman (1954b) the gravid proglottides of T. saginata and T. pisifbrmis contain 50 % mature ova, 40 immature ova, and 10 % infertile ova. The mature ova are present only in the terminal 30-50 proglottides. Immature ova are present in distal as well as proximal gravid proglottides. Some immature ova can mature outside the host within 2 weeks, whereas others have failed to mature after 2 months. There are a considerable number of recent publications concerning the membranes of T. saginata ova (Silverman, 1954a; Chowdhury et al., 1955a, c; 1956b, c; Lee et al., 1959; Morseth, 1965; Slais, 1970a). According to Slais (1970a) each egg consists of an outer shell, chorionic membrane, thick and striated embryophore, basement embryophore membrane, and two oncospherol membranes. There are two anatomical features of T. saginata eggs that are of epidemiological interest. The remnants of yolk masses, which rest on the outer membrane clot the embryophores together and enable them to remain attached to the host skin for some time. Also, the complicated membrane structure of T. saginata embryophores may in some way explain their resistance to chemical and physical factors. Some authors (Noyer and Baer, 1928; Kamalova, 1953; Verster, 1967) believe that there are morphological differences between T. saginata and T. solium embryophores; the former are said to be more ovoid, the latter more spherical. In fact, the difference is about 1-2 pm, and can hardly be regarded as an essential one. Other authors (Maplestone, 1937; Miretski, 1948) believe that the embryophores of T. solium and T. saginata cannot be distinguished by shape or measurement. An interesting way of differentiating T. saginata and T. solium embryophores is by staining with Ziehl-Nelsen stain (Brygoo er al., 1959; Capron and Rose, 1962). The stain is positive in T. saginata embryophores and negative in those of T. solium: this selective staining phenomenon depends on acid-alcohol resistance of egg membranes as suggested by Dubos (1947). The number of eggs in a single proglottis was determined by Penfold (1937a), as about 80 OOO, and the mean daily output of eggs as approximately 720 000. The number of eggs in an active proglottis varies a great deal according to

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the patency of the uterine branches and the activity of the proglottis. Most eggs leave the proglottis through an opening called the proctostoma, which is developed by damage of the thysanus, a bundle of parallel uterine branches, with club-shaped endings that touch the anterior margin of the proglottis (Mazzotti, 1944b; Rijpstra et al., 1961). Rijpstra et al. (1961) observed that of 16 proglottides discharged in the feces only two were “fully” gravid (77 700 and 82 430 eggs); in five, the number was 1000-6000, and in nine, the number was only 20G800. According to the very precise studies of these authors there is an active egg laying mechanism effected by pressure exerted by large masses of ova in the uterus and later by muscular activity of the motile proglottides. They observed a single proglottis lay 15 490 eggs within a few minutes, then 48 070 eggs were deposited in a track 6.5 mm long during creeping, and 18 870 eggs were left in the dried proglottis. The number of eggs remaining in a proglottis is usually less than 500 (Rijpstra et al., 1961). The eggs can be released only after maceration of the proglottis (Gonnert et al., 1968). C.

ONCHOSPHERE

This stage of T. saginata has not often been invesligated. Some information about the morphology and development of the onchospheral stage was summarized by Voge (1967). Hatching involves two processes : digestion of the embryophore and activation of the hexacanth embryo. A 13h action by gastric juice, then a 45 min action by intestinal juice seems to be necessary to digest the embryophore (Silverman, 1954a). Peptic and then tryptic digestion in uitro will also cause a rapid disintegration of the embryophore. Hyaluronidase, peptic digestion alone, chymotrypsin, carboxypeptidase B, and tryptic digestion alone, have little effect on distintegration of the embryophore (Silverman, 1954a; Gonnert et al., 1967; Gonnert and Thomas, 1969). A stimulus to activate the onchosphere must penetrate through lipoid and scleroprotein membranes after the embryophore has disintegrated. Since 1922 (Isobe according to Silverman, 1954a) it has been known that bile is necessary to activate the tapeworm embryo but it is not yet known how bile works and how important bile is in creating selective host specificity (Smyth, 1969). Voge (1967) stated that the physiological factors that affect host specificity or susceptibility are very complex and not yet fully understood. The free, activated onchosphere penetrates the intestinal mucosa by means of hooks and penetration glands. Hooks appear to be used for the initial attachment to the mucosa. The secretion of penetration glands in some tapeworms other than T. saginata has been observed by Reid (1948). Silverman and Maneely (1955) found secreting glands in the onchospheral state of T. saginata which play some part in penetration by cytolysis of the mucosal cells. The cytolytic effect of the onchospheral stage of some Taenidae has been shown in the rabbit’s intestines by Heath (see Smyth, 1969). Smyth pointed out, that the secretion of onchospheral penetration glands may produce an immunological effect. Very little is known about the migration of the onchospheral stage of T. suginata to the final location in the intermediary host’s tissues. Intravenous 13

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administration of onchospheres to 6-day-old calves failed to produce cysticercosis. Onchospheres given subcutaneously or intramuscularly do not migrate but develop in the site of inoculation (Froyd and Round, 1960; Wikerhauser et al., 1970). D. CYSTICERCUS

There are two reviews that summarize recent knowledge on the postembryonic development of cestodes and the morphology of the cysticercus stage of T. saginata and T. solium (Voge, 1967; Slais, 1970a). In addition, there are a number of original papers on the morphology of the cysticercus (Holz and Petzenburg, 1957; Voge, 1963; Siddiqui, 1963; $lais 1966a, 1966b, 1970a, b). The structure of cysticerci appears to be more complicated than originally believed. According to Voge (1963) the external tissue of the T. saginata cysticercus consists of hairlike processes, a peripheral collagenous-fibrous layer, below which are a group of ovoid cells, muscle bundles, a duct system, flame cells, and fine fibres. The internal tissue fold consists of tegument, a peripheral fibrous layer, two muscle layers, peripheral cells, calcareous corpuscles, flame cells, a duct system embedded in a loose fibrous net, and a central band of muscles. Slais (1970a) pointed out that the histological structure of the bladder portion of the T. saginata cysticercus differs from that of the scolex portion. It is too early to say how far a knowledge of structure may influence knowledge of the functions of the cysticercus. Slais suggested a morphological analogy between the bladder wall of the cysticercus and the trophoblast of mammalian embryos. There are different opinions about the possibility of differentiating between the wall structure of T. solium and T. saginatu cysticerci. Voge (1963) said “in spite of minor apparent differences the structure of the two species is very similar and their specific differentiation cannot be guaranteed when the scolex is not available”. On the other hand, Slais (1970a) stated that “even if scoleces are not present, a differential diagnosis of C . cellulosae, C. bovis and Coenurus cerebralis can be made on the grounds of a detailed analysis of the histological structure of the bladder wall of the cysticercus”. We are reproducing Slais’s valuable table on the diagnostic characters of some cestode larvae which occur in man (Table 11). The development of T. saginata cysticerci has been studied by McIntosh and Miller (1960) in 34 infected steers. The first cysticerci visible by naked eye were found on day 11 and the size was about 0.13 x 0.1 mm, the surrounding connective tissue 3 x 2 mm. Three weeks after infection a cavity and immature scolex were found and at 5-6 weeks the scolex with suckers was fully developed. At 10 weeks an invaginated neck is visible. Cysticerci that are 10-12 weeks old are believed to be the youngest stage capable of infecting the definitive host. Throughout the experimental period of 55 weeks no absorption of dead cysts was observed. The detailed histological studies of Silverman and Hulland (1961) showed that the growth rate and development of T. saginuta cysticerci is variable and depends on the host response and the tissue invaded. Varying results by different authors working on the development, viability, and longevity of T. suginata is therefore understandable.

28 1

T A E N I A S I S A N D CYSTICERCOSIS

TABLEI1 Diagnostic characters of some cestode larvae which may be found in man (after slais (1970a)) Coenurus cellulosae -

C. bovis

C. cerebralis

______.____~_

One

Scolex :

____

~.

~~

One

...

+

Hooks :

____ 0

Several

Many

-~

+

+

Bladder : _

_

Echinococcus granulosus

.

. _

~

-

.

~~

~

Cuticle

Surface

Cuticle -

~~~

Ranging from 3-6 pm below 1 pm to 2.5 pm

Subcuticular

+

groups of muscles

~ _ ~ _ _ _ _ _ _

-

Cuticle

_ _ _ _ ~

Superficial hairlike cuticular extensions

~~

Stratified hyaloidine membrane -

1-2 pm

0

0

0

0

Make-up of wall

Wartlike processes

Rugae

Smooth and Smooth also rugose

Base of superficial protuberances

27-38 pm

50-70 pm

28-46 pm

0

Height of superficial protuberances

15-27 pm

23-27 pm

15-22 pm

0

A point of particular epidemiological interest is the question of the longevity of T. saginata cysticerci, which may not be uniform even in the same animal and depends on the tissue invaded (Van den Heever, 1967; Soulsby, 1963). In the liver, lung and heart some cysticerci degenerate as early as 20 days after infection (Soulsby, 1963). It is not unusual to find living and dead cysticerci in the same host (Penfold et al., 1937b; Friedrich, 1961; Dewhirst et al., 1963). Calves may differ from cattle in the maximal survival time of cysticerci (Koudela, 1967b). In Froyd’s experiment (1964b) cysticerci survived 21-30 months. Dewhirst et al. (1963) infected 4-6 month old steers with one million eggs and viable cysticerci were found on day 639. According to Urquhart and Brocklesby (1965) cysticerci survive for 21 months in lightly infected animals. Van den Heever and Tustin (1967) found viable cysticerci in an Afrikander crossbred cow 3 years after an experimental infection. In an experiment done by Leikina et al. (1964) in 14 young calves, all cysticerci were degenerated

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within 11 months. In Penfold’s classic experiment (1937b) carried out in 30 oxen, no cysticerci survived 9 months. Peel (1953) and Leikina et aZ. (1964) suggest that the variable longevity of cysticerci may be referable to different strains of T. saginata in Africa and elsewhere in the world. Discussing this point, Smyth (1969) stated that the differences might be attributable to various strains of cattle rather than to differences of tapeworms. It is an oversimplification to expect that this complex phenomenon is dependent only on differing parasite or host strains. Unlike the adult worm, which is weakly immunogenic, the larval stage of T. saginata produces an active immunological response when it invades the intermediary host, as Weinmann (1966, 1970) has shown. According to Froyd and Round’s (1960) suggestions and Gemmell’s (1967) observations of tapeworm occurring in sheep there are at least two immune responses against larval taeniid tapeworms in the intermediary host. One, which is probably species specific, occurs in the small intestine and is directed against penetrating oncospheres. The other interferes with growing larval forms in the muscle. It is responsible for strong, life-long resistance of cattle to reinfection, approaching a level of absolute immunity. Also, the life span of primary cysticerci can be shortened by secondary exposure (Leikina et al.,1964). It is generally assumed that T. saginata cysticercosis does not alter the state of health of the intermediary host. The only exceptions are Dewhirst et aZ.’s observation (1960) of a small decline in the haemoglobin level of infected animals, the finding of Evranova and Mosina (1966) that glycogen synthesis in the liver and skeletal muscles of infected calves is depressed, and Taylor’s report (1958) of a death of an onyx-antelope because of pericarditis and coronary vessel embolization secondary to intensive cysticercosis. The physiological factors that stimulate evagination of the cysticercus once it is ingested by the definitive host were investigated by Hornbostel (1959). The most important factors are the action of gastric and intestinal juice and the speed of intestinal passage. The stimulation of cysticercus evagination by surface-active agents was observed by Campbell and Richardson (1960) and by Campbell (1963). V. CLINICAL ASPECTS OF TAENIASIS (T. saginata) In a paper titled “Troublesome Tapeworms” in Lancet (i, 1953) Asher, who worked at the Central Middlesex Hospital in London, wrote, “Tapeworms in this country are often considered as a joke, and regarded as more suitable for examination questions than for consideration of their clinical importance”. Even in the United Kingdom, with its high standards of meat inspection, Taeniasaginatainfection can no longer be considered risible for it is encountered by clinicians there as well as in most other parts of the world. A.

SYMPTOMATOLOGY

Taenia saginata like all other human helminths may provoke symptoms or may cause an unrecognized infection. However, an asymptomatic T. suginata infection may, within a short time, change into a life-threatening

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condition when a proglottis is vomited and aspirated or when a proglottis enters the appendix. Short of these dramatic events, the difference between a symptomatic and an asymptomatic T.saginata infection can be very obscure. There are no pathognomonic signs and even the most experienced clinician cannot say for sure that a particular sign or symptom is due to a tapeworm infection. The literature on the symptomatology of T. saginata infection is widely scattered ;we have summarized eight of the more important reports. The most frequent symptom of T. suginata infection is the discharge of proglottides (98.3 %). This is a distinctive symptom that can hardly go unnoticed by the patient, although it is well tolerated by some individuals, For a period of 5-10 min the patient feels a sensation in the rectum and then the passing of the proglottis through the anus associated with a crawling sensation in the perianal area (Belyaev and Monisov, 1967). In addition to the passage of proglottides approximately three of every four patients infected with T. saginata experience one or more other symptoms. From eight studies including observations of 31 10 patients the symptoms are arranged in decreasing order of frequency (Penfold et al., 1937a; Swartzwelder, 1939; Mazzotti et al., 1947; Dzicciolowski and Kuimicki, 1953; d’Alessandro Bacigalupo, 1956a; Hornbostel, 1959; Beier, 1963; Pawlowski and Chwirot, 1970). Symptom Abdominal pain Nausea Weakness Loss of weight Increased appetite Headache Constipation Dizziness Diarrhea Pruritis ani Excitation

Per cent 35.6 34.4 24.8 21 .o 17.0 15.5 9.4 8.2 5.9 4.5 3.4

The above mentioned symptoms may vary widely in character. Abdominal pains are usually vaguely localized in the midline of the epigastrium or umbilical region. They vary in intensity from dull, aching, gnawing, burning to intensive colic-like sharp pain. This pain is probably due to a distension or spasm of the intestinal wall in reaction to the movement of the tapeworm. This is true visceral pain. A characteristic feature of this abdominal pain is its prompt relief by taking some food. The same feature applies to the symptom of nausea. Both abdominal pain and nausea are usually more intensive in the morning. Nausea is the third most common symptom of T.saginata infection. Nausea might be explained as the result of extension or spasm of the duodenum or jejunum as is also true of abdominal pain. An alternate explanation is that it is

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caused by gastric hyposecretion, a phenomenon that commonly occurs in Taenia saginata infection. A common symptom of T. saginata infection is alteration of appetite (Beier, 1963; Pawlowski and Chwirot, 1970; Hennemann and D’Heureuse, 1958). Some patients have an increase of appetite, others have a decreased appetite, and still others have an alternating increase and decrease in their appetite. The hunger frequently associated with tapeworm infection is difficult to explain. It might be due to hypoglycemia. Hornbostel(l959) noted a low blood glucose value of 64 mg % during an “attack” of hunger in a patient with T. suginata infection. On the other hand, Abuladze (1964) said that hunger “attacks” might be the result of irritation of the ileocaecal valve by tapeworm proglottides. A characteristic feature of increased appetite associated with T. saginata infection is its satisfaction by an inordinately small amount of food. This increased appetite rarely results in weight gain, a phenomenon that has been observed in only 2 % of 2200 patients by Pawlowski and Chwirot (1970). Decreased appetite is as frequently observed as increased appetite (12 and 13% respectively; Pawlowski and Chwirot, 1970). It seems to be more strongly influenced by the psyche of patients than by any other factor. Loss of weight was observed in 15% of 2200 patients (Pawlowski and Chwirot in press). Weight loss correlates well with the symptom of decreased appetite, but weight loss can also occur in individuals with no change in appetite or even in those patients who report that they eat more. The tendency to lose weight as a result of tapeworm infection is not a dependable phenomenon and is surely a poor rationale for allowing tapeworm infections to survive in obese patients in order to correct their body weight. Vomiting is an infrequent symptom of T. saginata infection. It occurs most commonly in children and in emotionally labile individuals. At times proglottides are vomited. Penfold (1937a) reported two such cases, one in an individual undergoing anaesthesia and another in a patient with pneumonia. Alterations in bowel movements due to T. suginata infection are usually temporary in nature. Some individuals experience both constipation and diarrhea, whereas others experience one or the other of these symptoms, which may be due to irritation of the intestinal wall by the parasite. Some cases of severe diarrhea due to T. saginata infection have been reported (Loeper, 1931 ; Hurst and Robb-Smith, 1942; Kaufman, 1961). The mechanism of this diarrhea is obscure; it may occur with or without an associated eosinophilic response. Although the most common symptom of T. suginata infection is the passage of tapeworm proglottides only a minority of patients developed pruritis ani. Some authors believe that pruritis ani has an allergic background (Burckhardt, 1945). Mazzotti et al. (1947) and d’Alessandro Bacigalupo (1956a) found that pruritis ani was a common symptom, but many of their patients were infected with other parasites at the time of examination. Urticaria is seldom reported in patients with T. saginata infection (da Franqa, 1952; Wigand and Warnecke, 1953; d’Alessandro Bacigalupo, 1956a; Link and Cassorla, 1964). Other skin disorders such as prurigo

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nodularis and allergic skin pruritis are even less commonly reported than urticaria (Rollier, 1956; da FranCa, 1958). There are a few reports of syncope associated with T. saginata infection, usually in young patients. Although the mechanism is obscure two possible explanations are vaso-vagal disorders or hypoglycemia. Another uncommon symptom is the sensation of a lump in the throat (globus hystericus). This phenomenon is ill-understood (Lockhart, 1961). Tt was reported by Pawlowski and Chwirot (1970) in 3% of 2200 patients, most commonly in middle-aged women. In addition to specific characteristics of T. saginata infection in individual patients there are group characteristics that are dependent on age, sex, and co-existing conditions. Infected children more frequently manifest change of appetite, abdominal pain, epileptic-like seizures and syncopal episodes (Shah and Joshi, 1965; Karnaukhov, 1967). In 30 children who were 5-14 years of age Kluska et al. (1969) reported that the mean gain in weight within 8 weeks after successful treatment of T. saginata infection was 1-2kg. Signs of infection in infants (Perez, 1955; Mossmer, 1955; Link and Cassorla, 1964) are usually quite pronounced and consist of vomiting, diarrhea, fever, weight loss, and irritability. Elderly patients usually manifest fewer symptoms than young or middle-aged patients except for hypersalivation. There is a slightly higher frequency of symptoms in women than in men (79.3% vs. 74.9%)). Change in appetite, loss of weight, nausea, vomiting, constipation, and headache are more pronouned in women. Two symptoms, globus hystericus and urticaria, do not occur in men. Pawlowski and Chwirot (1 970), found a slight correlation between asymptomatic infections and duration of infection. 21 % of patients discharging proglottides for no more than 2 weeks were asymptomatic whereas 31 % of patients discharging proglottides for more than 3 years were asymptomatic. The symptomatology of T. saginata infection depends not only on the host but also on certain parasite factors. In unusual cases of multiple infection or bizarre location, the parasite can cause various acute conditions or complications. These complications are as follows: intestinal obstruction (Christopherson and Izzedin, 1918, according to Brumpt, 1949; Ferracani, 1941); perforation (one case reported by Stieda, 1900, and by Nauwerck, 1900, Kaan, 1941); perineal abscess (Gombarros, 1943); hepatic abscess (Negre, 1957); cholecystitis (Arnell, 1949; Talice and Ptrei-Moreira, 1954; Ardao et al., 1956; Logan, 1960; Adamiya and Gogotishvili, 1968); and appendicitis (Letulle and Lagane, 1908; Boveri, 1939; Richard, 1943; Niiio, 1944; Clark, 1946: Deschiens and Bablet, 1948; Upton, 1950; Berry and Burrows, 1955). These complications, of course, have their own unique symptomatology. B.

CLINICAL PATHOLOGY

Rees’ review (1967) gives an admittedly general account of the pathogensis of adult cestodes in man and animals. The paper by Hornbostel (1959) is more medically oriented, however, but the portion dealing with pathogensis is limited. The pathogenesis of T. suginuta infection will be reviewed here in terms of its traumatic, irritative, toxic, allergic, local and systemic actions.

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Whenever the parasite changes its natural environment it may cause traumatic or irritative action in its new location. For example, during vomiting T. saginata proglottides may be aspirated and cause obstruction of the respiratory tract (Shahin, 1932; Bruning, 1933; Verdiev, 1958); the worm may enter the middle ear through the eustachian tube (Shahin, 1932); it may localize and grow in the adenoid tissue of the nasopharynx (Shakhsuvarli et al., 1964) and it has been found in the uterine cavity (Schacher and Hajj, 1970). Cases have been reported of the migration of T.saginata proglottides into the common bile duct (Logan, 1960; Benedict, 1926). A perforation of the intestinal tract by T. saginata was reported 72 years ago (Stieda, 1900; and Nauwerck, 1900). A more common complication is appendicitis. Until 1950 there were 55 reported cases of appendicitis caused by Taenia sp. (Upton, 1950). Berry and Burrows (1955) cited cases of appendicitis caused by various cestodes; amongst them were 42 cases of T. saginata, ten of T. solium, 25 of Taenia sp., one of Hymenolepsis nana, and five of Echinococcus granulosis. As many as four proglottides have been found in the appendix but usually only one or two are present and sometimes only abundant eggs are found. In three cases the scolex was recovered. The tapeworm may elicit a wide range of reactions in the appendix from very slight inflammatory reaction to a chronic, subacute, or acute appendicitis of catarrhal, phlegmatic, or follicular type (Berry and Burrows, 1955). The traumatic and irritative action of T. saginata on the intestinal wall is ill-understood. One report describes a piece of intestinal mucosa in the tapeworm sucker (see Hornbostel, 1959); however, Hornbostel (1959) has not confirmed this in the examination of 16 scoleces. Intestinal mucosa taken by biopsy in patients with T. saginata infection show slight subacute inflammatory reaction in many cases (Gasparov et al., 1962; Kubicki and Karlinska, 1967). The symptomatology of T. saginata infection such as abdominal pain and nausea suggest that there is an irritative action of the tapeworm which may result in a distension or spasm of the intestine. A study of intestinal absorption in T. saginata infection by El-Mawla et al. (1966) in 20 Egyptians failed to demonstrate any abnormalities in d-xylose absorption or fecal fat excretion but Ciauri and Mastrandrea (1960) observed lower fat absorption in patients with T. saginata infection. The suggestion of Hennemann and d’Heureuse (1958) that hypochromic anemia due to diminished iron absorption occurs in children with T. saginata infection has not been proved. Separate cases of agranulocytosis (Thiodet et al., 1953) and hyperchromic anemia (Tronchetti and Cartei, 1948) have been reported. Moderate eosinophilia has been reported in from 5 % (d’Alessandro Bacigalupo, 1956a) to 46% (Adonajto and Bonczak, 1961) of patients. A higher level of eosinophilia, 20-30 %, is observed sporadically. Lapierre (1953) reported an unusual case of increasing eosinophilia with a maximum of 53 ”/, 14-2 months before discharge of T. saginata proglottides and 36 76 at the time of the appearance of proglottides. Talyzin (1949) in a self-experimentproduced eosinophilia up to 16.5 % by injections of extracts of T. saginata. The evidence for an allergic action of the parasite includes not only the finding of eosinophilia but also the symptoms of urticaria, pruritis and asthma (Burckhardt, 1945; Blamoutier, 1952; da Franca, 1952; 1958; Rollier, 1956).

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There is little evidence that tapeworms induce a bacterial infection in their intestinal environment; however, when proglottides migrate to unusual locations, i.e. appendix, biliary ducts, they may carry intestinal bacteria with them. On the other hand, it is known that cestodes possess some bactericidal properties (Rees, 1967). There is an interesting association between T. saginata infection and lowered gastric secretion (Hornbostel, 1959; Todorov, 1966; Chodera et al., 1967). C.

DIAGNOSIS

Since there is no characteristic clinical picture of T. saginata infection the diagnosis must be based on laboratory findings. Fecal tests, anal swabs, serological and skin tests determine whether a tapeworm infection exists; however, the exact species diagnosis of T. saginata infection is made by the finding and examination of the scolex or those proglottides that show typical species characteristics. Questioning of the patient about discharge of proglottides is an important part of the diagnosis (Podyapolskaya, 1942; Artikov and Safarov, 1964). The value of the medical history is dependent on the degree of cooperation between the physician and the patient. Monisov (1966) showed how frequently a false answer would be obtained by failure to ask detailed questions. The demonstration of T. saginata proglottides and brief questioning of a group of 842 people elicited 54 positive replies including 26 (48.2 %) false positive answers which were not confirmed by laboratory examination. People who gave a false positive answer had either a T. saginata infection in the past or an infection with Ascaris or Enterobius or other inappropriate reasons. In another group of 920 people more detailed questions about the number, size, color, activity of actually discharged proglottides, together with their demonstration, gave much better results. Fifty patients answered affirmatively and only three (6 %) proved to be false positive replies. In another group of 986 people to whom Ascaris and Enterobius adult €orms were demonstrated, in addition to the detailed questioning, 116 gave positive replies and four (3.9%) proved to be false positive. The inadequacy of fecal examination for detecting T. saginata infection has been known for many years (Kouri and Basnuevo, 1933; Mazzotti, 1944a, b). Nevertheless, in the past decade some authors have pointed out that thick fecal smears are valuable. Rijpstra et al. (1961) arranged the following coprological methods in decreasing order of efficiency: thick smear according to Hein; concentration technique according to Teleman ; thin fecal smears repeated six times; and flotation according to Faust-Bijlmer. Miiller (1968) stated that the efficacy of the Hein thick smear technique for a single examination was 77 %, for two examinatioiis 91 %, and for three examinations 97 %, in 35 cases. He indicated that the Fiilleborn flotation technique was 20% effective, the direct thin smear 57 %, the Teleman concentration method 66 %, and simple sedimentation 71 % effective, Scraping of the anal region as an effective means of diagnosing T. saginata infection was reported as early as 1927 by Oleinikov and 1929 by Bogojavlenski and Lewitski. Anal swabs have become more and more popular as a means of

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detecting T. saginata infections (Bacigalupo, 1940). Podyapolskaya ( I 942) reported that scrapings of the wall of the lower part of the rectum gave 76 % positive results whereas the Fulleborn technique gave only 57 % positive results. Mazzotti (1944a, b) found the Graham method superior to fecal examination (85 % versus 73 %). The usefulness of anal swabs has been confirmed by many authors; Pipkin and Rizk (1948), Garaguso (1954), Doby et al. (1957), Hsieh (1960), Roman (1961), Petru and VojtEchovskB (1963a). Roman (1961) preferred the Graham Scotch tape method over the Schiiffner-Swellengrebel (1943) pestle method which was advocated by Petru and VojtEchovskB (1963a). Eggs found on perianal skin are more likely to be T. saginata. T. saginata eggs may be distinguished from T. solium eggs by special stains (Capron and Rose, 1962). The differential species diagnosis of mature proglottides requires the use of fixation and staining methods. Gravid proglottides are usually prepared by simply pressing them between two glass slides and examining the number of lateral uterine branches in strong transmitted light. This method has been accepted everywhere for many years. In those cases where the diagnosis is uncertain or where there are unusual features of the tapeworm body, it would be desirable to send a portion of the tapeworm pressed between two glass slides and fixed in 10% formalin to a helminthologist. Staining of the specimen and examination according to Verster's criteria should differentiate T. saginata from T. solium in these doubtful cases. Examination of the scolex is a classic means of differentiating T. saginata from T. solium. There is, however, a case report (Hussey 1963) in which the scolex was unhooked and the proglottides resembled T. solium having only 4-12 paired uterine branches. Serological tests are more useful for the detection of human cysticercosis than for adult tapeworm infection. Although the precipitin reaction with T. saginata antigen has long been used (Langer, 1905), the complement fixation test since 1909 (Weinberg, 1908) and the skin hypersensitivity test since 1927 (Ramsdell, 1928), their value in the diagnosis of intestinal infection has been in doubt (Deschiens and Renaudet, 1941; Podyapolskaya and Kamalova, 1942; Gaehtgens, 1943). Nevertheless, in the past decade considerable progress has been made in the serological diagnosis of T. saginata infection (Dobrowolska, 1950; Roguska and Zwierz, l964,1966a, b; Machnicka-Roguska, 1965; Sokolovskaya, 1968, 1969; Zapart et al., 1969). Machnicka-Roguska and Zwierz (1964, 1966a, b), using the hemagglutination test of Middlebrook-Dubos, obtained 60 % positive results in 125 patients infected with T. saginata. Best results were obtained with a purified polysaccharide fraction of the antigen. 15% of sera still gave a positive reaction 5-19 months after successful treatment. Sokolovskaya (1968) used a latex agglutination test with an homogenate of T. saginata body as an antigen. She obtained 96.3 % positive results with sera of 285 T.saginata patients, but she also obtained 15.6"/o positive results with sera from 96 patients who formerly had T. saginata infection 2 months to 2 years in the past and 3.6% positive results with sera of 55 individuals who had no prior exposure and were free from infection. The latex agglutination test with a protein fraction homogenate from the body of T. saginata gave even better results. In patients

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infected with T. saginata 99.2% were positive, but positive results were obtained in patients who formerly had T. saginata infection (20.8%) and in uninfected persons (10.9 %). Zapart (1968) using a complement fixation test with an antigen fractionated according to Melcher’s method found 73.7 % of patients positive and when he used a ring precipitation test found 82.5 % of patients positive. Three months after successful treatment 12.5% reactions were found using the CFT and 10% using the ring precipitation test. The efficacy of intradermal tests using similar antigens was much lower (Zapart et al., 1969). Attempts to develop more specific serological tests have been made by fractionating antigens (MachnickaRoguska, 1965), by preparing antigens from different parts of the tapeworm’s body (Mukhin, 1969), by using a cysticercus antigen (Cramer and Dewhirst, 1965) by finding a special substance (C-type) in antigens (Biguet et al., 1965), and by purification of antigens by physico-chemical methods (T. solium) Morris et al., 1968). In sporadic cases where T. saginata infection is suspected but the patient is not passing proglottides, a radiological examination of the intestinal tract may be helpful. In distinction to Ascaris lumbricoides which gives a sharply outlined radiolucent shadow and linear traces of barium in the worm’s intestine, the tapeworm body, despite its great length, usually remains concealed from the radiologist. The front part of the body is so extremely narrow as to preclude its demonstration by radiological technique (Monroe and Norton, 1962). The broader hind parts of the tapeworm body give a ribbon-like radiolucent defect but in most cases this is visible only in the ileum (Hamilton, 1946; PrCv6t et al., 1952; Benassi, 1954; Monroe and Norton, 1962; Fetterman, 1965). D. TREATMENT

In the past decade, two valuable reviews of the chemotherapy of cestode infections have appeared ;both are from the Wellcome Research Laboratories. The review by Standen (1963) deals mainly with experimental chemotherapy, and Keeling’s review (1968) deals with advances in chemotherapy in the intervening 5 years. With these valuable reviews of the chemotherapy of cestode infections as a background we have concentrated our attention on the clinical aspects of the therapy of T. saginata infections. Despite the advances that have been madeit is still true that precise knowledge of the mode of action of even well-known taeniacides is scanty (Hatton, 1970). Experimental chemotherapy has been based exclusively on cestodes other than T. saginata (Steward, 1955; Pawlowski, 1964b; Mattila and Takki, 1966; Cavier and Notteghem, 1968; Saz and Lescure, 1968; Scheibel et al., 1968; Saz, 1970) and does not satisfactorily explain the mode of action of the common taeniacides. Some observations have been made of the T. saginata body expelled after treatment (Mustakallio and Saikkonen, 1954; Makhmudova, 1958; Izmailova-Guseinova, 1959; Rusak, 1964; Gonnert, 1968) but they do not provide conclusive information. Individual clinical reports concerning efficacy and safety of taeniacides are also inadequate in most cases. This is true because methods are not uniform, the number of patients observed is usually inadequate and follow-up examination is frequently

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deficient. Despite these shortcomings, there is a wealth of publications about drugs for the treatment of tapeworm infection and cumulatively they provide much useful information on which to base the choice of drug. The choice of drug depends on two paramount factors-efficacy and safety. The common taeniacides are at least 80 % effective (Dufek and Kalivoda, 1969; Petrosyan et al., 1969; Pawlowski, 1970a); therefore, any new compound must be at least this effectivein order to replace the ones that are in current use. Because taeniasis (T. saginata) is not a life-threatening infection, taeniacides that are toxic should not be used. I t is generally true that the newer taeniacides are less toxic than the older taeniacides and this is the main reason that they have won a place in the therapeutic armamentarium. Keeling (1968) suggested that the following drugs be used for T. saginata infection in man: niclosamide, dichlorphen, aspidium oleoresin, and mepacrine hydrochloride. There is no doubt in our minds that niclosamide is now the drug of choice, but in the place of dichlorophen and aspidium oleoresin we would substitute tin compounds. Other taeniacides that will be discussed briefly are paromomycin, bithionol, pumpkin seed extract, and hypertonic magnesium sulfate solution. Niclosamide (Yomesan) [N-/2’-chloro-4’-nitrophenyl/-5-chlorosalicylamide] is undoubtedly the drug of choice for T. saginata infection of man at the present time. During the past 3 years the following authors reported on their experience with Yomesan: Gherman (1968) 93.6% cure rate; Ahkami and Hadjian (1969) 95.5% cure rate; Khalil (1969) 84.6% cure rate; Pawlowski (1970a) 90% cure rate; Perera et al. (1970) 97.0% cure rate. The efficacy of Yomesan based on 3 3 publications from 1960 to 1966 which included 766 cases of T. saginarainfection was 88.5 % (Schultz, 1968). There are some reports which give a much lower efficacy of niclosamide: Donckaster et al. (1961) 53 % cure rate; Nitzulescu et al, (1962) 58%; Karnaukhov and Stromskaya (1966) 7% cure rate; Krotov et al. (1968) 74% cure rate. Pawlowski (1970a) stated that there were some batches of drug (Yomesan produced in 1962) or products (Vermitin produced in 1964) that had much lower efficacy. This is also true of Phenasal produced in 1962 to 1963 (Karnaukhov and Stromskaya, 1966). It seems that the particle size of these compounds was outside the range of 2-6 pm which is necessary for the drug to be active (Krotov et al., 1968). The following are some suggestions for treating patients with T. saginata infections with Yomesan. No pretreatment is necessary except for those patients with constipation who should receive a purge or enema one day before treatment. The drug is taken on an empty stomach or just after a light meal. The tablets should be crushed or chewed and followed by a small amount of water. It is best to keep the patient on a light diet during the day of treatment. As a rule, it is not necessary to use any purgative drug, but it might be helpful for a patient when he does not tolerate the treatment well. A saline purge would help to eliminate the worm more easily, avoid some adverse reactions and perhaps relieve the anxiety in waiting for the worm to be passed. The dosage of Yomesan has remained the same for the past 10 years. For adults it is four tablets which are each 0.5 g, thus the total dose is 2 g. Although reported side effects of niclosamide are mostly minor ones, syncope has been

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29 1

reported (Beier, 1963, 1966; Pawlowski and Chwirot, 1970). There are no strict contraindications to this drug. Although Yomesan is widely used throughout the world, knowledge of its mode of action is quite limited. Mattila and Takki (1966) did pointout that niclosamide uncouples the oxidative phosphorylation in rat liver mitochondria as do other salicylate compounds. Scheibel et al. (1968) indicated that niclosamide inhibits the phosphorylation mechanism of mitochondria. This may account for the anthelmintic action of niclosamide. Gonnert (1968) summarized knowledge of Yomesan’s mode of action as follows: “The drug inhibits the uptake of oxygen and glucose. The decomposition of glycogen is increased, whereas the activity of the lactodehydrogenase is inhibited. Taeniacidal activity is concentrated upon the upper part of the strobila, whereas the microscopic and histological investigation of gravid segments T. saginata and T. solium proves that no significant differences exist in the state of maceration between proglottides of untreated and Yomesan treated cases.” According to Gonnert (1 968) “the investigations with radioactive labeled and unlabeled compound prove that 25-30 % of orally administered compound are excreted with the urine (the greater part being metabolites) and the remainder is excreted with the feces. No accumulation of compound or its metabolites take place in the whole body or in single organs. The compound is rapidly and quantitatively excreted.” These undoubtedly are the reasons for the good tolerance and safety of niclosamide. Standen (1963) briefly mentioned inorganic tin compounds and Keeling (1968) did not, although he devoted a chapter to organic tin compounds, which are promising veterinary taeniacides, especially for poultry. Tin as a taeniacide was used by Paracelsus (Cavier, 1953) and was still in usein Europe in the early nineteenth century (Hirte, 1951, 1957); however, it fell into disuse, possibly due to toxic reactions from lead, antimony, and arsenic contamination (Deschiens et al., 19.56). The efficacy of metallic tin for taeniasis was rediscovered in 1943by Poey-Noquez (Cavier, 1953)and confirmed by some French authors in the 1940s (LeGac, 1947) and Basnuevo (1947, 1948). In the early 1950s some German investigators introduced tin compounds into broader medical use (Hirte, 1951; Kuhls, 1953). The efficacy of tin compounds varies according to the particular drug used. Taenifuge is 72% effective and Stannotaen 98% (Chodera et al., 1970). Storage of the drug for longer than 2-3 years will result in a loss of efficacy (Pawlowski, 1959,1970a). The efficacy of various tin compounds based on the treatment of 868 outpatients with T. saginata infection was 88.8 % (Dufek and Kalivoda, 1969; Pawlowski, 1970). The drug is taken two or three times a day for a period of 5 days irrespective of the fact that the strobila may be evacuated early in the treatment course. At the third day and at the end of treatment, a saline purgative is advocated. The exact dosage depends on the particular product used sincethe ingredients in each product differ. For example, one tablet of Cestodin contains 580mgmetallic tin, 150 mg tin oxide, and 32.5 mg tin chloride (Hirte, 1957). The total number of tablets vary from Cestodin-15, Stannotaen-10, Taenifuge-90. The drug should be well pulverized since it probably acts by covering the cuticle with a

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thin layer of active tin particles and renders the strobila susceptible to digestion (Harant et al., 1957). The partially digested distal part of the strobila is usually expelled on the second or third day of treatment. Sometimes no part of the strobila is visible. Pure metallic tin and tin oxide particles seem to be virtually non-toxic but the irritative action of tin chloride is probably responsible for the side effects observed in patients treated with tin compounds (Dadlez et al., 1954). The percentage of side effects noted by several authors was 36.6% (Dufek and Kalivoda, 1969), 46.6 % in outpatients (Pawlowski and Chwirot, 1970) and 5-37 % in inpatients depending on which drug was used (Chodera et al., 1970). The side effects are mostly gastrointestinal disorders and rarely fever and syncope (Pawlowski and Chwirot, 1970). Malformation of a newborn child (agenesis of the right hand with aplasia of the radius and ulna) was reported by Notter et al. (1963) after treatment of a 28-year-old woman in the tenth week of pregnancy with stannous oxide. The contraindications for this group of drugs are pregnancy, gastrointestinal disorders that produce increased drug absorption and severe liver and renal disease (Bojanowicz and Pietrowa, 1968). Despite the risk of intolerance and overdosage Acridine derivatives are still in common use. At the present time they should be reserved for refractory cases of T. saginata infection (Keeling, 1968). Acridine derivatives other than quinacrine (Mepacrine, Atabrine), i.e. Acrichin (Krotov and Rusak, 1964) and Acranil (Beier, 1963; Pawlowski, 1970a), are now in use. The usual dose of one of these drugs for an adult is 0-6-0.8 g. The most effective way of giving the treatment is by intraduodenal tube followed by a saline purgative 1 h later. Treatment by mouth and treatment of infected children have become less popular because of vomiting, with consequent loss of a portion of the dose. Although the acridine derivatives have been used since 1939 (Neghme, 1951) their mode of action is as yet not understood (Standen, 1963). According to Mattila and Takki (1966) Atabrine uncouples the oxidative phosphorylation of Taenia taeniaformis but this fact does not fully explain its anthelmintic activity. Beier (1965a) observed that these drugs intensify both the motility of the tapeworm and the peristaltic movements of the host intestine resulting in the expulsion of the parasite. It is highly probable that the anthelmintic action is based on interference with the sucking action of the tapeworm. The affinity of the acridine derivatives for the suckers of the tapeworm has been confirmed by fluorescent microscope observations (Mustakallio and Saikkonen, 1954; Saikkonen and Mustakallio, 1963). It is possible that these relax as a result of some shrinking of mucous membranes producing a partial vacuum between the scolex and the intestinal wall (Lepes, 1956, cit. Beier, 1965a). Following the observations of Wagner in Ethiopia in 1960, Ulivelli (1968) presented a more detailed study on the eficacy of paromomycin for T. saginata infection. He treated 208 cases of T. saginata infection, 32 cases of T. solium infection, and eight cases of Hymenolepis nana infection with an overall efficacy of 98-100%. Doses of 20-30 mg/kg/day divided into four parts for four consecutive days were given. No preliminary preparation or subsequent treatment was necessary. The treatment was well tolerated even in children.

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Gastrointestinal side effects occurred infrequently. The early observations of Ulivelli have been confirmed by Salem and Al-Allaf (1967), Garin et al. (1970) and Botero (1970). In a group of patients with amebiasis treated by Salem and Al-Allaf (1967) 47 patients also had T. saginata infection. All patients were cured with a daily dose of 50 mg/kg of paromomycin administered for 5 days. The strobila was evacuated on the second or third day of treatment. Reexamination of patients was done between the fourth and eighth month. Eight of the 47 patients complained of abdominal discomfort or diarrhea during treatment. Botero (1970) used two dose schedules of paromomycin: 40 mg/kg/day for 5 days in 15 patients and a single dose of 75 mg/kg (max. 4 g) in another 15 patients. One treatment failure occurred in each group. Side effects were less common when a single dose was given. Garin et al. (1970) tested four oligosaccharide antibiotics in patients infected with T. saginata. Paromomycin was the most effective and cured all of 20 patients. The mode of action of paromomycin is unknown. Cavier and Notteghem (1968) were unable to correlate their clinical results with the results of their experiments in animals. Garin et a/. (1970) suggested that the action against T. saginata may be similar to the drug’s action against bacteria, i.e. by changing ultrastructure of the basic membrane. In tapeworms this would make the parasite susceptible to the host’s digestive mechanisms. These reports make paromomycin a promising alternative treatment for T. saginata infection. Dichlorophen, 5 :5’-dichloro-2:2’-dehydroxydiphenylmethane,has been the subject of some favorable early reports (Lassance et al., 1957; Adams and Seaton, 1959; Schneider, 1959; Shafei, 1959; Seaton, 1960; Guilhon and Graber, 1960) but this has not been verified in practice (Turner, 1963; Alterio, 1968; Dufek and Kalivoda, 1969; Pawlowski, 1970a; Chodera er al., 1970). For some time this drug has been used in the U.S.S.R. for mass treatment but more recently intolerance to standard doses (6-9 g in adults) have relegated dichlorophen to use only as an alternative drug (Krotov et al., 1968). Following the suggestion of Krotov et al. (1968) dichlorophen has been used in a very low dose (1.0 g) together with niclosamide (2.0 g) under the name of Dichlosal. In the U.S.S.R. Dichlosal is believed to be the most effective drug for the mass treatment of T. saginata infection. Cure rates of 100 % have been reported by Suvorov (1966), 98-100% by Monisov and Niezbekov (1966) and 97.2% by Petrosyan et al. (1969). The report of Doroshchak and Kite1 (1968) concerning very serious side effects in two hospitalized patients raises doubt whether the mixture of these drugs is safe. Bithionol (2,2’-thiobis 9/4,6-dichlorophenol) for the treatment of taeniasis was introduced by Yokogawa et al. (1962), Miyakoda et al. (1963) and Nagahana et al. (1966). Kaliszewicz et al. (1967) on the basis of treating four patients stated that bithionol is a promising drug. Dufek and Kalivoda (1969) administered bithionol to 20 patients and cured 18 of them. They advocated 40-55 mg/kg usually in two doses separated by a 1 h interval and followed in 2 h by a saline purgative. The maximum total dose used was 3.4 g. Gastroenteric side effects were more frequent than those that occur with tin compounds or niclosamide. At the present time these limited observations are insufficient

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to warrant the introduction of bithionol for broader use as an alternative drug for the treatment of T. saginata infection. The discovery of pumpkin seeds as a taeniacide has been reviewed by Rybaltovsky (1966). The bulk of pumpkin seeds limits their use; however, refined extracts of pumpkin seeds have overcome this problem. Junod (1964) showed that a concentrated extract of pumpkin seeds is an effective taeniacide. Twenty-two of 26 patients were cured when the drug was given orally and 100% of 54 patients were cured when the drug was given by gastric or duodenal intubation. Bailinger and Sequin (1966) found two extracts from the seed coat of Cucurbitapepo active against T.saginata. There is much more to be done in the evaluation of the active substances of pumpkin seeds to determine their safety and eficacy. Extracts of male fern or related synthetic chemicals are still in use for the treatment of T. saginata infections (Kovalev, 1960; Dodion, 1962; Shah and Joshi, 1965; Ditzel and Schwartz, 1967; Alterio, 1968; Petrosyan et al., 1969), but the high toxicity of these drugs should exclude them from further use. Reports from Europe have cited unexpected fatalities from the use of these regimens. For example, Hanel (1950) summarized the experience with 22 000 treatments for tapeworm infection with extract of male fern in Germany. Permanent blindness occurred in four patients and at least 20patients were temporarily blinded. From other statistics cited by Hiinel (1950) among 121 reported cases of intoxication from extract of male fern, 47 resulted in permanent blindness and 17 were fatal. Since male fern and related compounds are relatively effectual taeniacides, work is still going on to develop further knowledge of their chemistry and toxicology (Oelkers and Ohnesorge, 1954; Heikinheimo, 1963; Nosslin, 1963; Hargreaves, 1966; Takki, 1967; Takki et al., 1968). As early as 1932 de Rivas suggested the use of hypertonic solutions given by duodenal tube for the treatment of tapeworm infection. In more recent years some authors rekindled this idea and used hypertonic solutions of magnesium sulfate as a taenifuge (Furst, 1951; Rosen and Kiefer, 1958; Donckaster et al., 1960). Fatal reactions from intraduodenal doses in excess of 60 g due to magnesium intoxication have been reported from Germany (Rosler, 1952) consequently this treatment is no longer advisable. It is evident that considerable progress has been made in the treatment of T. saginata infection. This point is illustrated by data from Poland during the past 15 years (Kalawski and Pawlowski, 1970) which show that the average TABLE I11 Treatment of 1750patients with T.saginata infection Poznah, Poland, 1953-1968* Years

Mean treatments required for cure

1953-56 1957-60 1961-65 1966-68

1.9 1.4 1.4 1.1

Drugs used

Pumpkin seeds, mepacrine, male fern

Tin compounds, pumpkin seeds, mepacrine Tin compounds, niclosamide Niclosamide, tin compounds

* Kalawski and Pawlowski (1970).

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number of treatments required for each patient dropped from 1.9 to 1.1 (Table 111). There is still need for further progress as there is no taeniacide that may be given without medical supervision or for mass chemotherapy. VI. EPIDEMIOLOGY AND EPIZOOTIOLOGY A.

TRANSMISSION BETWEEN MAN AND ANIMALS

T. saginata infection is a true zoonosis according to Sprent (1969b) who states that it is an “anthropozoonotic helminthiasis” in which “man is the usual or essential definitive host and disseminator of infection; vertebrate animals act as intermediate hosts”. This is in agreement with Garnham’s 1958 definition of “euzoonoses” in which man is an essential link in the life-history of the parasite. The fact that man is the only definitive host of T. saginata simplifies the epidemiology of this infection. On the other hand, the varied relationships between man, his animals and his environment makes for complex factors affecting the transmission of this parasite. In the most general terms transmission from man to animals may be either direct or indirect. Direct transmission is uncommon. It can occur when hands contaminated with T. saginata eggs feed and handle calves (Urquhart, 1961;Goulart et al., 1966). Much more common is the indirect method of transmission. This can occur through contamination of cattle feed, soil, sewage, spread by birds or flies, etc. In general, when there is close contact between an infected human and susceptible animals heavy infections result, whereas, when eggs are widely distributed in the environment most infections are light. A variety of ecologic factors influence the viability of eggs during indirect transmission. Knowledge of these factors is rather limited but some general statements can be made. Taeniid eggs will withstand the action of unfavorable external factors quite well. According to Laws (1967) and Mackie and Parnell (1967) taeniid eggs survive the action of most chemical disinfectants. They also resist a variety of physical factors. Laws (1968) did a variety of in vitro experiments with Echinococcus granulosus, Taenia pisiforrnis, T. ovis and T. hydatigena eggs. He concluded that desiccation is the dominant factor affecting the survival of taeniid eggs under natural conditions. At a temperature of 38°C desiccation is accelerated and leads to a rapid breakdown of the eggs. He demonstrated that desiccated eggs carry an electrostatic charge which may in part account for their adhesive properties. Under natural conditions it is generally accepted that moisture is the most important factor controlling the survival of T. saginata eggs (Penfold et al., 1937b; Jepsen and Roth, 1952; Silverman, 1956b; Suvorov, 1965). Silverman (1956b) pointed out that eggs do not survive longer than 14 days in the absence of surface moisture. Lucker and Douvres (1960), stated that small numbers of eggs survived in hay stored for 22 days but none survived in hay stored for 10 weeks. At a temperature of 4-5”C, T. suginata eggs can survive for at least 168 days (Froyd, 1962). Silverman (1956b) pointed out that some could be “activated” after 335 days. He stated that eggs could be activated when kept in saline at

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room temperature for 60 days and are inactivated by at least 10 min exposure at 59”C, but not by 4 h exposure at 45°C. According to Suvorov (1965) the optimum temperature for survival of T.saginata eggs is -4°C at which temperature they survive for 62-64 days. When the temperature is decreased to - 30°C the survival time is decreased to 16-19 days. These data confirm the observations of Lucker (1960) that at -4.5”C T. saginata eggs survived in significant numbers for 12 days but few kept at this temperature for 76 days were able to infect cattle. Jepsen and Roth (1952) found that T. suginata eggs survived at least 16 days when stored at 18°C in a dish filled with liquid manure. The survival time in liquid manure in an underground cistern was up to 71 days. In Denmark during the months of June-July 1947 the eggs survived for 58 days in grass and for 159 days during the months of February-July 1948. According to Penfold et al. (1937b) T. saginata eggs survive in Australia long enough to permit a protracted contamination of fields, water and crops. According to Duthy and van Someren (1948) the eggs can survive for about 1 year in the highlands of Kenya. A considerable number of experiments on the survival of T. suginata eggs in natural field conditions were performed by various authors in the U.S.S.R. They are summarized by Suvorov (1965). These studies, which were done in continental climates, show that under conditions where there are great differences between summer and winter temperatures, T. saginuta eggs will withstand cold winter conditions much better than they will withstand hot summer conditions. This is probably due to the desiccation that occurs during the summertime. It is important to note that under most conditions eggs survive better when they are free than when they are within proglottides (Suvorov, 1965). Sewage is important means of spreading T. saginata infection between human populations and cattle (Profi, 1934; Sinnecker, 1955; Liebmann, 1963). The increase of urban populations with consequent increased usage of water and overloading of sewage works lead to the breakdown of formerly reliable sewage treatment systems and the spread of T. saginata infection (Silverman and Griffiths, 1955b). Furthermore, the increased use of detergents interferes with the sedimentation, putrefaction and oxidation processes and enables a greater portion of parasite eggs to survive these processes (Silverman and Griffiths, 1955b). The passage of T. suginata ova through a variety of sewage installations has been observed by Vasilkova (1944); Newton et al. (1949); Jepsen and Roth (1952); Wang and Dunlop (1954); Silverman (1955b); Silverman and Griffiths (1955b); Kabler (1959); Menschel (1964); and Amirov and Salamov (1967). Greenberg and Dean (1958) summarized the situation by stating that “conventional sewage treatment is inadequate to completely eliminate Tuenia sp. eggs”. They state that treatment to eliminate T. suginata eggs adequately from sewage effluent can only be done by very slow sand filtration as described by Newton et ul. (1949) or by microstraining as described by Silverman and Griffiths (1955b). Sewage sludge has to be heattreated or left to dry for at least a year in order to be safe. Silverman and Guiver (1960) suggested that storage for 20 days at 35°C or retention for 1-5 days under mesophilic anaerobic conditions suffices to inactivate T.

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saginata eggs. Liebman (1963) stated that in order to assure the destruction of Taenia sp. eggs the time of digestion of the sludge in unheated septic tanks must be at least 3 months whereas in heated septic tanks it must be at least 2 months. When sewage is improperly treated, the final effluent is an important source of infection. This has been noted in a variety of circumstances. For example, in the United Kingdom in 1955 Silverman stated that 50% of cattle drank sewage-polluted water; in the United States in 1956 Miller commented that changing farming and irrigation practices increased the likelihood that livestock would be exposed to contaminated sewage. Epizootics of T. saginata infection attributed to sewage have also been noted by Schultz etal. (1969) in the U.S.A., and Sinnecker (1955) and Denecke (1966) in Germany. Even when sewage is channeled to the sea or rivers the natural purification process is slow. This phenomenon was noted by Vasilkova (1944) in the Moskva river in 1940 to 1941 where there were 4500 helminth eggs per m3 of sewage and 3 % of these eggs were Taenia sp. eggs. 2-5 km below the main sewage outlet there were 263 eggs per m3 of river water and 32 km below there were still 91 helminths eggs per m3. Also Amirov and Salamov (1967) found Taenia and Ascaris eggs in sea water and on the sea shore near Baku (Azerbaijan, U.S.S.R.) where the sewage outlet was 250 m out into the sea. These facts have led to the opinion that sewage effluent should be very carefully used in agriculture if indeed it should be used at all (Miller, 1956; Greenberg and Dean, 1958). Liebman (1963) even suggested an inverse correlation between the degree of sewage purification and the spread of cysticercosis in some areas in middle Europe. Gotzsche (1951), seeking an explanation for the uniform dissemination of T. saginata infection in Denmark, suggested that T. saginata eggs were transmitted by gulls and possibly other birds fed on proglottides. He failed to find viable Taenia eggs in herring-gull’s feces but he was able to infect some calves by feeding them the droppings of gulls. Gulls were also implicated by Silverman and Griffith (1955), Guildal (1956), Crewe (1967) and Crewe and Crewe (1969). Silverman and Griffiths (1955b) were also able to pass Taenia eggs through the intestinal tract of young chickens (before they developed a crop). They failed to demonstrate transmission through pigeons. Guildal (1956) found Taenia sp. eggs in the intestinal tract of six of 96 blackheaded gulls (Larus ridibundus), one of 34 common gulls (L. canus) none of 15 herring-gulls (L. argentatus) or lesser blackheaded gull (L.fuscus). In one Larus ridibundus he found as many as 28 000 eggs in the intestinal tract. The transmission of helminth eggs by flies was discussed early in the twentieth century by Nicolle (191 1) and Shircore (1916). In Mombasa, where 29%of natives had Taenia sp. eggs in their feces, Shircore (1916) observed that eight of 270 houseflies (species not described) had helminth eggs in their intestinal tracts. In Uzbek, U.S.S.R., Sycevskaja and Petrova (1958) observed that flies transmitted Taenia saginata eggs. Round (1961) examined filth flies, Chrysomyia albicans, Ch. chloropyga and Sarcophaga sp. in Kenya. He stated that T. saginata eggs can be passed by these flies for periods up to 11 days after ingestion. However, the majority are passed within 3 days and during

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that time the eggs are viable, He concluded that filth flies in Kenya may play an important role in the transmission of Taenia sp. eggs. Nadzhafov (1967) found that seven out of eight species of flies experimentally infected with T. saginata had ova in their feces and regurgitations. The greatest number of eggs were found in Lucilia sericata and L. caesar. According to Nadzhafov (1967) in Azerbaijan, U.S.S.R., an area endemic for T. saginata infection, 4.8% of 4372 flies belonging to 20 species had Taenia sp. eggs on their external surfaces or in their intestinal tracts. The highest infection rates (8.8 %) were observed in Sarcophagidae. The degree of contamination of flies depended substantially on the extent of fecal contamination of the soil in four village territories that were investigated. On the basis of these experiments and observations Nadzhafov (1967) stated that synanthropic flies definitely play a role in the dissemination of T. saginata infection. Other species of insects, e.g. Periplaneta americana (Macfie, 1922) and BIatta germanica (Round, 1961) are also able to disseminate T. saginata eggs but their role in natural conditions seems to be of little importance because they do not feed on feces. The role of other coprophagic invertebrates as disseminators of T. saginata eggs has not been investigated yet despite some suggestions that they may be effective in spreading the infection. The finding of mature cysticerci in calves a few weeks old would indicate that transmission by the intrauterine route is possible (Kolbe, 1937; Canhan, 1946; McManus, 1960; Urquhart, 1961,1966). This phenomenon seems to be rather frequent in endemic areas. For example, McManus (1960) stated that 3.07% of 14855 calves in Kenya in 1957 to 1958 were condemned for T. saginata cysticercosis. The majority of calves (80%) were 2-21 days old. The author was able to find mature T. saginata cysticerci in 28 calves that were 2-10 days old. Prenatal transmission of T. saginata infection is of epidemiological importance because thorough sanitation may not suffice to eradicate the disease when this alternate means of transmission occurs. Also Soulsby’s experiments (1963) show that very young animals are immunologically unresponsive to T. saginata cysticercosisinfection. Thus, prenatal infection may confer little immunity to exogenous infection. At the present time it is too early to evaluate the importance of intrauterine transmission in maintaining the disease in enzootic areas. Infection of man occurs by the simple act of eating raw or partially cooked infected beef. However, the factors that favor the eating of raw meat are very complex. They are discussed in their ecological, economic and ethnological contexts. Ecological factors are more important in the transmission of T. saginata from man to animals than they are in the transmission from animals to man. Since the cysticercus has no contact with the external environment, ecological factors act only on the host. Man is the only known definitive host of T. saginata; the only geographical limitation of this infection is the regions of the world inhabited by man. Ecological factors do have an important role in determining the cattle breeding areas of the world. Also, wild animal reservoirs of this infection have been found in Taiwan (Huang, 1967), and the northern zones of the U.S.S.R. ;their role in Africa is not clear (Nelson et al,, 1965).

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From the economic standpoint, world beef production has doubled in the 20 years following World War 11.In many areas there is greater contact between cattle and man both as a breeder as well as a consumer. In the Poznan region of Poland a direct correlation has been found between increased beef consumption and incidence of T. saginata infection in the urban population (Pawlowski, 1970b; Kalawski and Pawlowski, 1970). Unfortunately similar data are not available from other countries. Animal-to-man transmission of T. saginata infection occurs both in developed and developing countries but the socioeconomic reasons for this are ironically opposite-infection is prevalent in developed countries because they are rich, and in developing countries because they are poor ! Transmission between animal and man also depends on ethnological factors, i.e. human habits, behavior, religion and beliefs. They influence the type of food man consumes and the manner of its preparation. Some practices are based on hundreds of years of tradition. Some are conducive to the transmission of T. saginata and it is doubtful that they can be changed rapidly. In the Transcaucasus and Buriat regions of the U.S.S.R. slices of meat cooked on spits such as “shashlik” or semi-raw meat used as stuffing for regional dishes are responsible for transmitting T. suginata (Abasov, 1957; Kovalev, 1965; Abdullaev, 1968). In Egypt, Turkey and Middle East countries, a beef dish known as “basterma” or kebab-like dishes are suspected (Nagaty, 1946). In East and Central Africa pieces of beef briefly roasted in an open fire are an important source of infection (Carmichael, 1952). In Thailand a raw beef dish, “larb” is responsible for group infections (Chularerk et al., 1967). In areas such as Lebanon taeniasis is caused by adulteration of raw mutton dishes with beef which is cheaper (Schwabe, 1963). The reasons why raw mutton meat, steak tartar, and a variety of semi-raw beef products are so popular in western European countries is not well understood (Pawlowski, 1970b) but they are responsible for the increase of T. saginata infections in this region. The chance of being infected by tasting meat during cooking is probably exaggerated because the amount of meat taken in this manner is very small compared to the meat taken as a dish. It is worthwhile to point out Hornbostel’s suggestion (1954) that T. saginata cysticerci easily attach themselves to the hands and can be readily transmitted to the mouth; it is doubtful that this fact has epidemiologic importance. Studies of the social and ethnological aspects of taeniasis are only beginning; they should be included in future epidemiological investigation. Studies in the Poznah region of Poland have shown that they are very important in evaluating the epidemiological situation in this area (Kalawski and Pawlowski, 1970; Pawlowski, 1970b). B.

EPIDEMIOLOGICAL AND EPIZOOTIOLOGICAL DATA

Epidemiological data on the prevalence of human taeniasis (T. saginatu) are grossly defective. Frequently the data that do exist are inadequate because laboratory procedures are not standardized, or only some part of a population is examined, e.g. children, hospital patients, or else the number of people examined is too small to give an objective picture of the true prevalence.

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Moreover, much of the data is dispersed in time, covering the last 20 years. The exceptions are some mass surveys in the U.S.S.R. and Poland. Knowledge of the incidence of taeniasis is also scanty. Compulsory notification of new cases is the exception rather than the rule for most countries in the world. Even if notification were introduced in some countries it would not cover all the diagnosed or treated cases. Therefore, it is possible only to point out some figures from the world literature which may not be representative of the particular region or country and to provide bibliographies on the world-wide distribution of T. saginata cysticercosisand taeniasis. Data on T. saginata cysticercosis originate from meat inspection reports. Meat inspection is carried out in many parts of the world but not in a uniform comparable way, Therefore, the data can be discussed only in a general manner. Data in FAO/WHO/OIE Animal Year Book (1970) shows where cysticercosis is found frequently, rarely, not at all, or where no data exists. The most recent papers that deal with the incidence of T.saginata cysticercosis are Merle (1958), Urquhart (1961), and Froyd (1965b). The following discussion deals with the incidence and prevalence of T. saginata taeniasis and cysticercosis in various parts of the world. The most detailed data come from theU.S.S.R. and they were summarized by Prokopenko (1968). Based on stool examination of 14.2 million people in 1950, the mean prevalence of human T. saginata infection was 0.6 %. The respective data for the years 1960 and 1966 are 46.4 and 65.8 million examined and prevalences of 0.3 % and 0.075 %. The sharp decrease in prevalence was due to extensive mass examination followed by mass treatment. For example, in 1960more than 97 000 cases were treated and in 1966 more than 120 000 cases were treated. The prevalence was not equal in the different republics of the U.S.S.R. The endemic foci are in Caucasian area (southern Dagestan, western Azerbaijan, northern Armenian, eastern Georgian) and in the south-central Asian republics (Uzbek, Kirghiz and Kazak). The highest prevalences were in Dagestan20.4% (Kovalev, 1960), in Azerbaijan-45-2% (Abasov, 1957) and 29.1 % (Nadzhafov, 1966), in Armenia-7.7 % (Avakyan, 1961) and 20 % (Martikyan, 1963), in Uzbek-43.5 % (Magdiev, 1966, 1968), in Kazak-7.9 % (Ghenis, 1968). The incidence of cysticercosis for the whole of the U.S.S.R. was about 1 % in the 1960s. In some areas of Armenia it was as high as 20.7 % (Avakyan, 1961). In contrast to data on human infection the animal data are very scanty. In Poland the prevalence of taeniasis in 1954 to 1956 was 259/100 000 based on stool examination of more than 100 000 adults (Zembrzuski, 1965). The incidence in 1965 was six per 100 000 and in 1967 it was nine per 100 000 (Adonajlo et al., 1969). The corresponding figures for T. saginata cysticercosis were 0.56% and 0.58% in the years 1965 and 1967 (Adonajlo et al., 1969). In the city of Poznan the prevalence in 1967 was 40.1 per 100 000 for men and 63.3 per 100 000 for women (Kalawski and Pawlowski, 1970). In Czechoslovakia in 1964 the incidence of T.saginata cysticercosis was 1.385% in the Czech region and 0.312% in Slovakia (Koudela, 1965b). The incidence of cysticercosis of cattle in Hungary was 0.213% (Takics et al., 1967) and in Bulgaria it was 0.07416% in the years 1937 to 1942

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30 1

(Pavlov, 1944) and 0.62% in 1960 to 1964 (Petkov and Jodorov, 1970). In East Germany T. saginata cysticercosis was found in 1946 in 0.49% of cattle, in 1952 in 2.2% (Kupey, 1954), in 1963 in 2.01 %, and in 1964 in 2.63 % of examined cattle (Hiepe et al., 1967). Cysticercosis was as high as 7.0% in 1962 at Halle (Ockert, 1965) and 7.32% in 1966 at Frankfurt (Oder) (Mielke, 1969). According to Raschke (1957) the percentage of cysticercosis found in Germany was 0.32% in 1904, 0.37% in 1910, 0.16% in 1920, 0.33% in 1930, and 0.30 % in 1940. In West Germany it was 0.38 % in 1951 and 2.06 % in 1964. The incidence of human 7'.saginata infection is calculated at 0.024 in Frankfurt (Oder) (Mielke, 1969). In Yugoslavia, in the areas of Bosnia, Kosmet, Sandzak, and Montenegro more than 15% of the inhabitants were carriers of T. saginata and more than 30% of cattle were infected with cysticercosis (Lepes, 1954). In other parts of Yugoslavia the incidence of cysticercosis was 10% or more, e.g. 24.64% in Pljevla (Nenadic, 1958), and approximately 10% in Bosnia and Hercegovina (Grujic, 1960). In the United Kingdom T. saginata was seldom found in man and cattle before World War 11. However, after the war many authors observed a sharp increase in the incidence of T. saginata cysticercosis (LeRoux, 1949; Marsden, 1950; Priestly, 1950; Griffiths, 1950; Seiler and Norval, 1950). Silverman in 1955a reported an incidence between 0.21 % and 0.58 % from 200 slaughterhouses but he suggested that the real percentage is between 0.81 % and 3.47 %. Logan (1967) gave the official percentages of 2.3% and 2.8% for Ireland in 1961 and 1963, but pointed out that the percentage may differ in various abattoirs from 0.1 % to 10%. In Holland, Belgium, Sweden, Denmark, the incidence of T. saginata cysticercosis is about 1 % (Tarnaala, 1941 ; Grigoire et al., 1956; van Keulen, 1959; van Gils, 1963; Honer, 1963; Enequist, 1965; de Vries, 1968). These data indicate that in many parts of Europe the prevalence of human T. saginata infection does not exceed 0.5 % except for some endemic foci in U.S.S.R. and Yugoslavia. This is far below the prevalence noted before the introduction of meat inspection in Europe when, for example, 5 % of the population was infected in Germany in 1855 (cited by Beier, 1963). Also, the prevalence of T. saginata cysticercosis is below 1 %, but in some areas it may exceed 5 % (Blackpool, 1948; Belfast, 1948; Genoa, 1953; Pljevla, 1958; Frankfurt (Oder), 1962; Halle, 1962; Berlin, 1965). Despite improvements brought about by meat inspection T. saginata taeniasis and cysticercosis appears to be increasing in Europe as shown by an analysis of 85 publications in the post-World War 11 period (Pawlowski, 1971). The following figures from European slaughterhouses illustrate this point: Prague 0.34 % (1945) to 1.6% (1955) and 3.1 % (1964); Berlin approx. 1 % (1945-1959) to 5.5 % (1965); and Poznan 0.5 % (1955) to 2-3% (1962). Cysticercosis and taeniasis have decreased, however, in the U.S.S.R. and Bulgaria (Petkov and Todorov, 1970) where mass control measures have been introduced. In the United States comprehensive data on T. saginata cysticercosis and taeniasis has only recently become available (Schultz et al., 1970). Prior to

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1959, only sporadic reports of cysticercosis of cattle were available; in 1912 the incidence was 0*14%,in 1930 it was 0*37%,and in 1942 it was 0.6%. Since 1959 annual data from the U.S. Department of Agriculture has shown that 0.04-0.08 % of cattle slaughtered in federally inspected abattoirs have cysticercosis. The rate for cattle slaughtered in California is 20 times greater than for cattle slaughtered in the remainder of the United States. A review of 1.8 million stool examinations from 43 states has shown that 23/100 OOO are positive for Taenia sp.; since other evidence indicates that T. solium is rare in the United States, virtually all of these identifications are believed to be T. saginata. Thus, transmission of T. saginata, albeit at a low level, occurs even in a highly developed country-the United States. In the latter part of the nineteenth century T. saginata infections were common in Abyssinia, Sudan, Algeria and Senegal (Hoeppli, 1969). Now, with more intensive grazing of cattle in the African continent the incidence is quite high in comparison to other parts of the world. Prevalances of human taeniasis above 10% have been reported from Kenya (Froyd, 1965a; McKinnon, 1957), the Congo (van Grunderbeeck and Penson, 1954), and South Africa (Elsdon-Dew, 1964). No infections, however, have been found in Congo pygmies (Price et al., 1963) and there is a low prevalence in children living in forest regions of Cameroun (Doby et al., 1957) and in coastal tribes in Kenya (Froyd, 1965a). An incidence of T. saginata cysticercosis greater than 10 % has been reported from Sudan (Eisa et al., 1962), Eritrea (Coceani, 1949), Kenya (Ginsberg, 1954, 1955; Ginsberg et al., 1956; Froyd, 1960, 1965a), Rhodesia (Rhodesia report, 1969), Uganda (Mitchell, 1967), Urundi (Marsboom et al., 1960; Biche and Thienpont, 1959), Chad (Graber and Thome, 1966), Congo (Versyck and Jacob, 1958; Urquhart, 1961) and Portuguese Guinea (de Oliveira Lecuona, 1956). Urquhart (1961) added to this list Bechuanaland, Cameroun, Ethiopia, French Guinea, Madagascar, Nigeria, Oubangui, Sierra Leone and Tanganyika, and Froyd (1965b) added Libya. An incidence of cysticercosis less than 10% has been reported from Egypt (Abdou, 1959; El-Afifi et al., 1961), and the Republic of South Africa (Canhan, 1946; Verster 1966; van den Heever, 1969). The conclusion is inescapable that cattle breeding Africa is full of T. saginata. There is very limited and outdated information on taeniasis and cysticercosis in the world’s two largest populations-China (Wu, 1939) and India (Mukerji and Bhaduri, 1944). Froyd (1965a) stated that the incidence of T. saginata cysticercosis in India was 1.4% and reports by Peatt (1950) and Shah and Joshi, (1965) show that T. saginata taeniasis and cysticercosis are common in some parts of the country. India is better known as the source of T. solium cysticercosis (Dixon and Lipscomb, 1961). In Asia the endemic foci of T. saginata are in the Near Eastern countries (Bottom, 1945; Thornton, 1957; Interdept. Committee, Lebanon, 1962; Froyd, 1965a; Witenberg, 1968). There are also foci in Thailand (Interdept. Committee, Thailand, 1962; Chularerk et al., 1967); Burma (Tu and Hkun-Saw-Lwin, 1968); Taiwan (Hsieh, 1960; Huang, 1967); Mongolia (Froyd, 1965b); South Korea (Lee et al., 1966; Seo et al., 1969); and Japan (Morishita et al., 1964).

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There is little information available from Australia except for Penfold’s (1936a) remark that T. saginata is very common in people of Syrian origin. According to Fewster (1967) cysticercosis was suspected in 0.21 % of one million slaughtered cattle and proved in 57% of suspected cases. Shortridge (1966) reported T. suginata infection in cattle in New Zealand. Most of the information on T. suginata taeniasis and cysticercosis in South America comes from Brazil. Pessoa (1967) stated that the prevalence of T. saginutu in Sao Paolo is 1-1.5 %. Elsewhere in Brazil, DeFreitas (1964) cited a prevalence of 1.6 %, Paoliello (1965) 2.0 % and Dias (1967) 0.37 % of children. Cysticercosis has been reported in approximately 1 % of Brazilian cattle (Ribeiro, 1949; Pardi et al., 1952; Costa and Brant, 1964; Brant et al., 1965). suginatu) in other Central and South American The prevalence of taeniasis (7‘. countries are: Cuba-0.16 % (Alvaro-Diaz, 1967), Panama Canal Zone0.16 % (Cosgrove, 1960), Guatemala-1.72 % (Acha and Aguilar, 1964), Ecuador--O.7% (Lopez, 1969), Chile-1.6 % (Delard et al., 1958) and Argentina-062 % (Niiio, 1964). Since these data are so fragmentary it is difficult to compare them with Stoll’s assessment in 1947 that 39 million of the world‘s population was infected with T. saginata. One can, however, state that T. suginata taeniasis and cysticercosisare cosmopolitan in distribution ;that they have become more prevalent in many areas of the world where comparative data exist; that since 1947 the world’s population has increased by approximately 50 % and the cattle population has increased by about 100%, so that it seems safe to conclude that more people are infected with T. suginatu now than the 39 million estimated by Stoll in 1947. C.

LOSSES DUE TO TAENIASIS AND CYSTICERCOSIS

T. suginatu infection causes two types of losses-the intangible losses due to the medical complications caused by the adult tapeworm and the tangible economic losses to agricultural societiesdue to cysticercosis. The medical costs of T. saginatu taeniasis are difficult to establish. The infection is rarely fatal unless the tapeworm body is in an unusual location. Symptomatology is quite varied and probably causes some lowering of productivity in infected populations. There is no information concerning the debilitating effects of taeniasis in a population living on a protein-deficient diet, but it is probably not a serious problem becauseinfected peopleare usually meat eaters. In Poland more than 20% of patients with T. saginata were treated in hospitals (Adonajlo and Gancarz, 1967) and the proportion seems to be the same in other countries. The cost of treating patients has been estimated to be between 1/20 (Mielke, 1969) and 1/13 (Logan, 1967) of the annual loss due to cysticercosis. There is considerable information about the financial losses due to T. saginata cysticercosis. In West Germany it has been said to be as high as 5 million DM (Friedrich, 1961); in East Germany 121 000 DM (Mielke, 1969); in Yugoslavia 6 million dinars (Winterhalter, 1965) and 87 million old dinars (Diinleski et al., 1963); in Belgium 25 million Belgian francs (Granville et al.,

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1958); in the United Kingdom 2100 000-500 000 (Silverman and Griffiths, 1955a); in Ireland €100000 (Logan, 1967), in Kenya €500000 (Mann, personal communication, 1971); and in the United States about $500 000 is lost each year by the condemnation and freezing of infected carcasses. These figures are impressive but they cannot be generalized to other regions. A better way is to estimate the average loss per animal and multiply it by the number infected for each particular region. According to Logan (1967) the mean loss for an infected animal is €10 (approximately $25). Silverman and Griffiths (1955a) counted the decreased value of meat, loss on weight (about 279, cost of additional handling, refrigeration and transport and an estimated mean loss as 230 ($75). According to Costa and Brant (1964) an infected animal is worth about one-third less than an uninfected animal. In the U.S. the cost of freezing infected carcasses is approximately $75 (condemned carcasses, of which there are few, represent a loss of approximately $300). Thus, a reasonable estimate of the losses due to cysticercosis is $25 per animal in developing countries and $75 per animal in industrialized countries. Apart from the direct losses there are other important consequences of cysticercosis. This is especially true in East Africa where the development of a profitable beef industry is inhibited by the high prevalence of cysticercosis. VII. PREVENTION A. MEAT INSPECTION

The history of meat inspection has recently been described by Dolman (1957) and Schwabe (1969). Meat inspection for cysticercosis has been in existence for 70 years and it is the foremost public health measure for the prevention of T. saginata transmission. However, meat inspection alone, particularly as it is now practised, cannot be expected to eradicate T. saginata infection (Thieulin et al., 1963). At the present time the important issues in the inspection of beef carcasses for cysticercosisare the question of the localization of cysticerci, the thoroughness of the inspection, and the use of new diagnostic techniques. Knowledge of the localization of cysticerci in beef carcasses is essential for proper meat inspection. There have been numerous papers dealing with this subject; nevertheless, there are still many opinions about “predilection sites” and the subject is controversial. Some authors report that the heart is the organ most frequently involved (LiGvre, 1933; Penfold et al., 1938; Silverman, 1956a; Varges, 1957; Marsboom et al., 1960; El-Afifi et al., 1963; Plaschke and Kramm, 1966; Dewhirst et al., 1967; Fewster, 1967); other authors believe that the examination of masseters, introduced by Hertwig in 1889 (cit. Desprts and Ruosch, 1961), is the most effective means of detection (Lazzaro, 1961; Koudela, 1967a), and still others believe the shoulder muscle incision, advocated by Viljoen in 1937 is most effective (El-Afifi et al., 1963; Cironeau and Popovici, 1968). There is probably no “predilection site” which would be acceptable for all cattle. There may be differences due to geographic area, breed of cattle, age, and activity of muscle groups (Kearney, 1970). For example, cysticerci tend to settle in the deeper muscles of the body,

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which have a higher level of metabolic activity and a dense branching distribution of blood vessels. The choice of muscles examined by meat inspectors should be based on studies done within each country or region. Another aspect of meat inspection is its efficacy. This is discussed by Marsboom et al. (1960), El-Afifi et al. (1963), Urquhart (1966), Koudela (1967a), Takics et al. (1967) and Dewhirst et al. (1967). They found that examination of the masseters, heart, tongue and shoulder muscles was important but routine and found 27.7%-68*9% of all inspection of these organs is insufficient for detecting light infections. According to Ginzel(l961) routine meat inspection can be improved by 2 %; Varges (1957) said from 1.5% to 14-2%, Kleibel (1961) from 2 to 8.6%, Desprts and Ruosch (1961) from 1.05 % to 5.3 %, Takbcs et al. (1967) from 0.2 to 0.7%. The improvement was brought about by better lighting, better timing of processing, and better training and rewarding of inspectorspsychological factors that are as important as physical factors. Luminescence under ultraviolet light of cysticerci was first described by Derrier (1927) (cit. after Marazza and Persiani, 1960) and first put to practical use by Koller (1943) (cit. Gibson, 1969). The efficacy of meat inspection with ultraviolet light was studied by Brandes (1958), Lerche and Elmossalami (1958), Marazza and Persiani (1960, 1961a, 1961b), van Gils (1963), Pirkl (1964), Franssen (1 964), and Koudela (1966a). These authors agree that ultraviolet light increases the probability of finding cysticerci but they disagree about the practical value of this technique. There are two aspects of treatment of infected meat: first to decide to what degree the meat is infected, and second, to determine the disposition of the meat. The regulations dealing with “measIy” beef are usually old ones (Antipin et al., 1956; Liegeois, 1956; Schmid, 1957; Ahrens and Aedtner, 1964; Gibson, 1969). The exceptions are the regulations in Australia (Fewster, 1967) and recent changes in United States regulations. The old regulations adhere to two archaic concepts. The first is the belief that cysticerci exist singly in carcasses and the other is the belief that there is a uniform life span of cysticerci. There is much information which shows that living cysticerci coexist with dead ones in the same carcass. Furthermore, removal of a single visible cysticercus on the assumption that the carcass then becomes safe for consumption is unjustified, even in light infections, because many more cysticerci are undoubtedly present in the carcass. Discarding all infected carcasses is not feasible economically, unless they are heavily infected. The carcasses are usually frozen or boiled. Gamma radiation as proposed by Pawel and Janikk (1963a, b) has not been put to practical use. Boiling meat to a temperature above 56”C, the thermal death point of T. saginata cysticerci (Allen, 1949, is effective provided the heat penetrates to the center of the meat. Freezing of meat at - 10°C (1 5°F) for 10 days effectively kills cysticerci (Landi and Monzini, 1954; Malheiro et al., 1966; Hajduk et al., 1969). Shorter time periods would reduce the expense of freezing carcasses, but studies dealing with various time and temperature requirements to kill cysticerci are generally out of date (Zunker, 1935; Keller, 1937, 1938a; Terhorst, 1938).

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B. SEROLOGICAL DIAGNOSIS AND IMMUNIZATION OF CATTLE

Ante-mortem diagnosis of cysticercosis of cattle has been attempted by skin serological and biochemical examination (Dewhirst et al., 1960; Dewhirst and Cramer, 1965). Skin tests performed in the caudal fold of cattle by Bugyaki (1961) gave 83.1 % positive reaction in infected animals but false positive reactions were frequent. In the detailed studies of Froyd (1963) various antigens were not specific enough. Similar results were obtained by Kosminkov (1965) and Leikina et al. (1966). Serological tests such as the hemagglutination and latex agglutination tests (Leikina et al., 1964, 1966; Kosminkov and Filipov, 1967; Sokolovskaya, 1968; Alferova, 1969) as more specific. According to Sokolovskaya (1968) the latex agglutination test with antigen from lyophylized cysticerci is 98.7 % sensitive and 99.7 % specific. According to Alferova (1969) the indirect hemagglutination test using Boyden’s technique and Kent’s antigen successfully diagnosed cysticercosis in 18 calves. No cross reaction with Echinococcus or Fasciola was observed. Two peaks of antibody response were observed, one was between 18-24 days and due to migration and development of larvae, and the other was observed between 81-101 days and probably due to destruction and release of somatic antigen. Soulsby found a substantial level of non-specific globulins in the serum of infected cattle and Mosina (1965) noted an increase of gamma globulin by paper electrophoresis on the 25th day of infection. This area deserves further work, Penfold and Penfold (1937) described complete immunity to reinfection of oxen that were infected with T. saginata cysticerci. The existence of immunity has been proved both experimentally (Urquhart, 1961) and in practice (Peel, 1953; Froyd, 1960; Graber and Thome, 1966). This immunity seems to be lifelong (Urquhart, 1961) except for light infection of calves (Soulsby, 1963). This lifelong immune response has led to attempts to immunize cattle as originally suggested by Penfold and Penfold (1937), as a means of controlling cysticercosis. Immunization can be carried out in three ways: per os infection with irradiated eggs (Urquhart et al., 1963; Urquhart, 1966), intramuscular infection with onchospheres (Wikerhauser et al., 1970), or by induction of heterologous immunity with T. hydatigena (Wikerhauser et al., 1970) but all of these methods are still experimental. Froyd’s (1964a) attempt to induce passive immunity in calves was unsuccessful. Further studies on passive and active immunization is warranted. C.

SANITATION

Schoop’s statement (1962) that no proper control methods for T. saginata taeniasis and cysticercosis have been found is too pessimistic. The control measures used in the U.S.S.R. have significantly reduced, but not eradicated, human taeniasis (Prokopenko, 1968; Sergiev, 1966; Magdiev, 1968; Abasov, 1968) and the changing sanitary and economic conditions in modern Israel have virtually eliminated T.saginata from that country (Witenberg, 1968). Various authors have expressed different views on the best ways to control

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this zoonosis. Some have put the major emphasis on man as the carrier of the adult parasite whereas others have emphasized animals as the disseminator of infection to man. This is really a moot point since successful control depends on a variety of measures that are aimed at all parts of the life cycle of the parasite. The need for close cooperation between medical and veterinary services has been pointed out by Ginsberg (1954), Kupey (1954), Magdiev (1968) and Popov et al. (1970). The control measures proposed by various authors fall into the following categories ; mass diagnosis and treatment, sanitation and sanitary education, ante-mortem testing and post-mortem inspection of cattle, and immunization (the latter two subjects have been discussed in the previous section). Mass diagnosis of populations in endemic areas and compulsory treatment of all patients infected with T. saginata has been carried out in U.S.S.R. and Bulgaria (Kovalev, 1960; Nadzhafov, 1966; Magdiev, 1968; Popov et al., 1970; Todorov, 1970). In Poland there is also compulsory treatment of all diagnosed cases and compulsory mass-treatment has been carried out in Kenya (Ginsberg, 1954) and the Congo (Versyck and Jacob, 1958). Compulsory diagnosis and treatment of cattle farm workers has been advocated by Sussman and Prchal (1950), Miller (1956), McIntosh and Miller (1960), Mattes (1962), Ahrens and Aedtner (1964) and Schultz et al. (1970). Although notification of Taenia cases is not a new idea (Krueger, 1934) it is rather the exception than the rule even in countries with high levels of preventive medical services. Long-term reduction in transmission depends on improved sanitation and sanitary education. The need for sanitation in rural endemic areas has been pointed out by Kovalev (1960), Enequist (1965), Logan (1967) Abasov (1968), Magdiev (1968), Schwabe, (1969) and Popov et al. (1970). The need for proper treatment and disposal of sewage has been stressed by Silverman (1955b), Mattes (1962), Miller (1956), Logan (1967) and Friedrich (1961) and proper sanitation in campgrounds and recreation areas has been discussed by Kleibel (1961) and Mattes (1962). Improvement of sanitation is expensive and inevitably connected with a generally higher standard of living. Without social acceptance of control measures through programs of education they will be less effective; the importance of sanitary education has been pointed out by Sussman and Prchal (1950), Gregoire et al. (1956), Kovalev (1960) and Hermus (1961). At the 19th WorId Veterinary Congress in Mexico during 1971, the veterinary profession virtually declared war on cysticercosis and taeniasis caused by Taenia solium and T. suginata (communication of Dr I. Mann). In our opinion, any success gained in that war will depend on the promotion of adequate research, better cooperation between workers in the veterinary and medical professions in both the field and the laboratory, and the acceptance and understanding of control measures by authorities deciding matters of economic importance and meat-eating peoples.

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TABLE IV World-wide distribution of taeniasis and cysticercosis (T.saginata) : References

General Stoll (1947); Greenberg and Dean (1958); Merle (1958); Urquhart (1961); Froyd (1965b); FAO/WHO/OIE Animal Health Yearbook (1970). Europe Bachlechner (1941); Ginzel (1961); Kleibel(l961) Gregoire et al. (1956); Granville et al. (1958) Pavlov (1944); Ghenov (1964); Avlavidov and Kovchazov (1965); Denev (1965) ; Petkov and Todorov (1970) CZECHOSLOVAKIA Hovorka (1963); Petrh and Vojtechovskti (1963b); Petrd and Gregor (1963); Koudela (1965b, 1966b) DENMARK Emsbo (1938); Jepsen and Roth (1950); Thorp (1950); Gotzsche (1951); Jepsen and Roth (1952) FINLAND Tarnaala (1941); Huhtala (1950) FRANCE Reuter (1944); Fonteneau (1950) GERMANY EAST Kupey (1954); Sinnecker (1955); Hermus (1961); Schulze (1964); Grumbach (1965); Ockert (1965); Plaschke and Kramm (1966); Hiepe et al. (1967); Hajduk et al. (1969); Mielke (1969) GERMANY WEST Bishop (1952); Summa and Steppe (1956); Raschke (1957); Lerche and Elmossalami (1958); Friedrich (1961); Beier (1963); Schlachter (1963); Ahrens and Aedtner (1964); Beier (1965b) HOLLAND Hofstra (1954); van Keulen (1959); Honer (1963); Van Gils (1963); D e Vries (1968) HUNGARY Taktics et al. (1967) IRELAND Logan (1967) ITALY Pellegrino (1954); Pellegrini (1958); Schmid (1958); Masellis (1960); Ricci (1961); Marrenghi (1962); Gallo and Anello (1967); Pennisi et al. (1967); D e Carneri et a/. (1968); Corso et al. (1969) POLAND Trawinski (1957); Pawlowski and Rydzewski (1958); Pawtowski (1959); Adonajlo and Boliczak (1961); Lutyhski and Wasowa (1963); Pawtowski (1964a); Zembrzuski (1965); Adonajto and Gancarz (1967); Piqtkowska (1967); Adonajlo et al. (1969); Kalawski and Pawlowski (1970) RUMANIA Ureche (1965); Cironeau and Popovici (1968) SOVIET WONAbasov (1957); Mamedov (!958); Kovalev (1960); Avakyan (1961); Mukvoz (1961); Topuriya and Matikashvili (1961); Merkushev et al. (1962); Martikyan (1963); Pugachevskaya (1965); Ma diev (1966); Nadzhafov (1966); Prokopenko(l966); Sergiev et af. (1966); Shekhovtsov 8967); Ghenis (1968); Magdiev (1968); Prokopenko (1968) SPAIN Orduna (1957) SWEDEN Enequist (1965) SWITZERLAND Despres and Ruosch (1961); Despres (1962); Boch (1965) UNITED KINGDOM LeRoux 1949); Griffiths (1950); Hardwick (1990); Marsden (1950); McCleery and Blamire l1950); Priestly (1950); Seiler and Norval (1950); Silverman AUSTRIA BELGIUM BULGARIA

(1955a)

Lepes (1954); Simitch and Nevenitch (1955); Winterhalter and Stuparid (1957); NenadiC (1957,1958); ZelejkoviC and BokoviC (1959); Grujic 1960); NeCev and ACkov (1960); NenadiC (1960); Vujic et al. (1961); AlagiC eta/. (1965; DZinleski et al. (1963); Mijatovif (1964); Winterhalter (1965)

YUGOSLAVIA

Africa

ALGERIA Pampiglione et al. (1965) EGYPT Nor El Din and Baz (1949); Abdou ETHIOPIA Diesfeld (1965) CAMEROON Doby et al. (1957)

(1959); El Afifi et al. (1961)

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309

TABLEIV World-wide riistributio~iof cysticercosis (T. saginata) : References

Graber and Thome (1966); Graber and Tab0 (1968); Shabelnik and Chechugo (1970) CONGO van Grunderbeeck and Penson (1954); Versyck and Jacob (1958); Urquhart (1961); Price et a/. (1963); Roberts (1970) KENYA Daubney and Carman (1928); Mann and Mann (1947); Ginsberg (1954, 1955); Ginsberg eta/.(1956a, b); McKinnon (1957); Froyd (1960); Ginsberg(l960); McManus (1960); Froyd (1965a, 1966) MALAWI Fitzsimmons (1966) NIGERIA Okpala (1961); Hinz (1966) PORTUGUESE GUINEA de Oliveira Lecuona (1956) RHODESIA Goldsmid (1968); Rhodesia report (1969); Thornton and Goldsmid (1969) SOUTH AFRICA Canhan (1946); Elsdon-Dew (1964); Verster (1966); van den Heever (1969) SUDAN Sankale et al. (1958); Eisa et al. (1962); El Afifi et a/. (1963) UGANDA Mitchell (1967) URUNDI Biche and Thienpont (1959); Marsboom et nl. (1960) CHAD

ARGENTINA NiAo (1964) BRAZIL Ribeiro de Assis

Americas

(1949); Pardi et al. (1952); Costa and Brant (1964); De Freitas (1964); Brant et a/. (1965); Paoliello (1965); DaSilva et a/. (1966); Alonso (1967); Dias (1967); Pessoa (1967); Roiter (1968); Lima et a/. (1970) CHILE Delard et a/. (1958) CUBA Alvaro-Diaz Artidle (1967) ECUADOR Lope2 o l ? i Z (1969) GUATEMALA Acha and Aguilar (1964); Zapatel et al. (1965) PANAMA CANAL ZONE Cosgrove (1960) UNITED STATES Marx (1942); Sussman and Prchal (1950): Miller (1956); Schultz et al. (1970) VENEZUELA del Corral and Vogelsang (1943)

Asia BURMA Tu and Hkun-Saw-Lwin (1968) CAMBODIA Brumpt and Kong-Kim-Chuon (1965) CHINA Wu (1939); Chin (1959) I ~ I A Mukerji and Bhaduri (1944); Peatt (1950); Shah and Joshi (1965) IRAN Endrejat (1938); Sabbaghian and Arfaa (1970) IRAQ Thornton (1957) ISRAEL Witenberg (1968) JAPAN Masdaki (1960); Morishita et a/. (1964) KOREA Lee et a/. (1966); Seo et a/. (1969) LEBANON Interdept. Committee (1962) MONGOLIA Froyd (1965b) PAKISTAN Yaqub (1953); Muazzam and Ali (1961); Haleem el al. (1965) PHILIPPINES Refuerzo and Albis (1949) SIKKIM Mitra (1970) SYRIA Bottom (1945) TAIWAN Hsieh (1960); Bergner (1964); Huang (1967); Wen (1969) THAILAND Interdept. Committee (1962); Chularerk et a/. (1967); Papasarathorn

(1967) YEMEN Felsani (1959)

Australia AUSTRALIA Fewster (1 967) NEW ZEALAND Shortridge (1966)

et a/.

310

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REFERENCES Abasov, K. D. (1957). [Effect of the way of keeping cattle on the spreading of taeniarhynchosis.] Medskaya Parazit. (Moskva) 26, 137-140. Abasov, K. D. (1965). [Epidemiological factors in the formation of foci of taeniasis in the Azerbaidzhan SSR and the eradication of this disease.] Medskaya Parazit. (Moskva) 34,439-444. Abasov, K. D. (1968). The landscape epidemiology and accesses to eradication of taeniarhynchosis in Azerbaidjan SSR. Znt. Congr. Trop. Med. Malar. (8th), Teheran 1968,1120-1121. Abbate, E. A. and Del Gesso, L. (1945). Seudo intoxicacih tuberculosa por teniasis. Prensa mid. argent. 32, 813-815. Abdou, A. E. H. (1959). Cysticercosis-a public health problem in Egypt. J. Egypt. Publ. Hlth ASS.34, 205-215. Abdou, A. H., El Sherif, A. F. and Tadros, G. (1961). Internal parasites of swine in Egypt. J. Arab vet. med. Ass. 21, 57-83. Abdullaev, A. M. (1968). [Survival of cysticercus of beef tapeworm in veal dishes prepared in the Buryal ASSR.] Medskaya Parazit. (Moskva) 37, 108-109. Abuladze, K. I. (1964). [Principles of cestology, Vol. IV, Taeniata.] Zzd. Nauka, Moscow. Acha, P. N. and Aguiiar, F. J. (1964). Studies on cysticercosis in Central America and Panama. Am. J. trop. Med. Hyg. 13,48-53. Adamiya, G. and Gogotishvili, T. G. (1968). [Acute cholecystitis and bilious peritonitis caused by Taenia saginata.] Sov. Med. 31, 126-127. Adams, A. R. D. and Seaton, D. R. (1959). Treatment of Taenia saginata infection with Dichlorophen. (Demonstration.) Trans. R. SOC.trop. Med. Hyg. 53,5. Adonajlo, A. and Bodczak, J. (1961). Zakaienia tasiemcami w Swietle materiahjw z poradni schorzed jelitowych Warszawa-Praga P6lnoc. Przegl. epidem. Warsaw 15,425-427. Adonajio, A. and Gancarz, Z. (1967). Analiza epidemiologiczna tasiemczyc w Polsce. Przegl. epidem. 1,27-32. Adonajio, A., Boliczak, J., Gancarz, Z., Jarzqbski, Z. and Kondracka, H. (1969). [The epidemiologic and epizootiologic situation of taeniasis and cysticercosis in Poland in the years 1965-1967.1 Epidemiol. Rev. 23,232-234. Ahkami, S . and Hadjian, A. (1969). [The appearance of the scolex of Taenia saginata in the stool after the eradication of the parasite by niclosamide.] Z. Tropenrned. Parasit. 20, 341-345. Ahrens, G. and Aedtner, K. (1964). Ein Beitrag zum Rinderfinnenproblem. M i . VetMed. 19, 525-528. AlagiC, D., GavranoviC, I. and BeganoviC, H. A. (1962). Razmatranja o ikriEavosti mesa goveda zaklanih na sarajevskoj klaonici. Veteriizaria. Saraj, 11,219-224. d’Alessandro Bacigalupo, A. (1956a). Clinica de la teniasis humana por Taetiin saginata. Prensa mdd. argent. 43,1520-1 527. d’alessandro Bacigalupo, A. (1956b). Tratemiento de la teniasis humana por Taenia saginata. Prensa mid. argent. 43,1600-1 608. d’Alessandro Bacigalupo, A. (1956~).El estan6 en el tratamiento de la teniasis humana por Taenia saginata. Prensa mid. argent. 43,2546-2552. Alferova, M. V. (1969). [Dynamics of the indirect hemagglutination test in cysticercosis of cattle.] Medskayu Parazit. (Moskva) 38, 162-166. Allen, R. W. (1945). The thermal death point of Cysticercus bovis. J. Parasit. 31, Suppl. p. 21.

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Allen, R. W. (1947). The thermal death point of cysticerci of Tuenia saginata. J. Parasit. 33, 331-338. Alonso, M. T. (1967). [Incidence of intestinal protozoal and helminth infections in children in “Triangulo Mineiro”.] Hospital, Rio de Janeiro 72,935-940. Alterio, D. L. (1968). Tratamento das teniases humans por T. solium e T.saginutu com extrato etBreo de feto machointroduzido atravBs da entubaciio duodenal, Revta Hosp. Clin. Fac. Mid. Univ. S. Paul0 23, 150-152. Altmann, G. and Bubis, J. J. (1959). A case of multiple infection with Tueniasaginata. Israel med. J. 18, 35. Alvaro-Diaz Artilde, J. (1967). [Present position of intestinal parasitism in Havana province, Cuba.] Revta Cub. Med. trop. 19, 105-126. Amirov, R. 0. and Salamov, D. A. (1967). [Sanitary and helminthological evaluation of the use of sewage water for field irrigation in the climate of the Apsheronsk Penninsula.] Gig. Sanit. 32, 104-105. Andrews, G . W. S . and Ogilvie, A. C. (1944). Multiple infestation with Taeniu saginata. Br. med. J. i, 772. Anon. (1957). Bovine cysticercosis. Vet. Rec. 69, 66. Antipin, D. N., Ershov, V. S . , Zolotarev, N. A. and Salyaeva, V. A. (1956). [Parasitology and parasitic diseases of livestock.] State Publ. House for Agricultural Literature. Moscow. Ardao, H., Praderi, L. A., Talice, R. V. and PCrei-Moreira, L. (1956). Colecistitis parasitaria. Un caso de localizacibn de Taenia saginatu en la vesicula biliar. Archos urug. Med. Cirug. 49, 90-99. Arme, C. and Read, C. P. (1970).A surface enzyme in Hymenolepisdiminuta (Cestoda). J. Parasit. 56, 514-516. Arnell, 0. (1949). Biliary tract disease caused by Tuenia saginata. Acfa chir. scund. 99,280-284. Artemov, N. M. and Lure, R. N. (1941). On the content of acetylcholine and cholinesterase in the tissues of tapeworms. Bull. Acad. sci USSR (SBr. Biol.) 2,278-282. Artikov, M. B. and Safarov, G. I. (1964).[Eradication of a focus of taeniasis among the population of a collective farm in the Bukhara region.] Medskayu Parazit. (Moskva), 33,458-461. Asenjo, A. and Bustamente, E. (1950). Die neurochirurgische Behandlung der Cysticercose. Dt. med. Wschr. 75, 1180-1 183. Asher, R. (1953). Troublesome tapeworms. Lancet i, 1019-1021. Atias, A. (1962). Eosinofilia y enfermedades parasitarias. Boln chil. Parasir. 17, 103-106. Atienza Fernandez, M., Gomez Garcia, V. and Gonzales Castro, J. (1969). Empleo de particules inertes para el diagnbstico de la cysticercosis bovina. I. Prueba de la bentonita. Revta ib&. Parasit. 29, 35-43. Avakyan, D. M. (1961). [Taeniasis in the Kafansk area.] Medskuya Parazit. (Moskva) 30, 148-150. Avlavidov, T. and Kovchazov, G. (1965). [An attempt to eradicate taeniasis in the Varna area of Bulgaria.] Medskaya Parazit. (Moskva) 34, 572-575. Bachlechner, K. (1941). Beitrag zur Rinderfinnenbekampfung in der Ostmark. Wien. tierarztl. Mschr. 28, 1-7. Bacigalupo, J. (1940). MCtodo prhctico para el diagnbstico de la teniasis por Taenia saginata. Semana mid, Ano 47,184-1 85. Bacigalupo, J. and d‘Alessandro Bacigalupo, A. (1956). La Taenia suginuta puede producir Cysticercus bovis en el hombre? Prensa mid. argent. 43,1052-1054. Bailinger, J. and Seguin, F. (1966). [Anthelmintic activity of a preparation from squash seeds.] Bull. Soc. Pharm., Bordeaux 105,189-200. 14

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Vogel, H. (1961). Uber eine unsegmentierte, eingeschlechtliche Taenia saginata. J . Helminth., R. T. Leiper. Suppl., pp. 191-198. Vogelsang, E. G. and Fernandez, A. J. (1945). Caso de poliparasitismo simulthneo por T. saginata y T. solium, Trabajos del Centro de Investigaciones Cientifcas, Caracas, No. 3, pp. 1 1 1-1 15. von Bfand, T. (1966). “Biochemistry of Parasites.” Academic Press, New York and London. vonBrand,T., Mercado,T.I.,Nylen, M. U. andScott,D. B.(1960). Observationson function, composition and structure of cestode calcareous corpuscles. Expl Parasit. 9,205-214. von Brand, T., Scott, D. B., Nylen, M. U. and Pugh, M. H. (1965). Variations in the mineralogical composition of cestode calcareous corpuscles. Expl Parasit. 16, 382-391. von Brand, T., Nylen, M. U., Martin, G. N. and Churchwell, F. K. (1967). Composition and crystallization patterns of calcareous corpuscles of cestodes grown in different classes of hosts. J. Parasit. 53,683-687. von Harnack, G. A. (1959). Bandwurmbehandlung im Kindesalter mit Cestodin. Dt. med. Wschr. 84, 865-866. Vujic, B., Nikolic, P. and Anic, N. (1961). Neka pitanja epizootiologije Taenia saginata i Cysticercus inermis u jednom delu Sandfaka. Vet. Glasn. Belgrade 15,65-69. Wang, W. L. and Dunlop, S. G. (1954). Animal parasites in sewage and irrigation water. Sewage Works J. 26, 1020-1032. Wardle, R. A. and McLeod, J. A. (1952). “The Zoology of Tapeworms.” The University of Minnesota Press, Minneapolis, Minnesota. Webbe, G. (1967). The hatching and activation of taeniid ova in relation to the development of cysticercosis in man. Z . Tropenmed. Parasit. 18, 354-369. Wegmann, T. (1965). Diagnostik, Klinik und Therapie von Echinococcus and Taeniases. Schweizer Arch. Tierheilk. 107, 244-265. Weinberg, M. (1908). Valeur comparee de deux prockdbs de laboratoire (dkviation du complement et prkcipito-diagnostic) au vue du diagnostic de l’bchinococcose. C . r . Seanc. SOC. Biol. 66,133-135. Weinland, F. (1859). Observations on a new genus of Taenioides. Proc. Boston SOC. Natur. History, Vol. 6. Weinmann, C. J. (1966). Immunity mechanisms in cestode infections. In “Biology of Parasites” (Ed. E. J. L. Soulsby). Academic Press. Weinmann, C. J. (1970). Cestodes and acanthocephala. In “Immunity to Parasitic Animals,” Vol. 2 (Ed. G. J. Jackson, R. Herman and Ira Singer). AppletonCentury-Crofts, New York. Wen, Y. F. (1969). [A survey on helminthic infections among aborigines in Chien-Shih district of Hsin-Chu County, Taiwan.] J. Formosan Med. Ass. 68,445-452. Wigand, R. and Warnecke, W. (1953). Uber Bandwurmkuren (Taenia saginata). Dt. med. Wschr. 78, 1493-1494. Wikerhauser, T., Zukovic, M. and Diakula, N. (1970). Vaccination against bovine cysticercosis.J. Parasit. 56, 369. Winterhalter, M. (1965). IkriCavost goveda u toviligtima stoke. Vet. Glasn. Belgrade 19, 779-783. Winterhalter, M. and Stuparic, D. (1957). IkriCavost goveda. Vet. GIasn. Belgrade 11,458-465. Witenberg, G . G. (1968). Helminth fauna in man and domestic animals in Israel. Israel J. Med. Sci. 4, 1069-1073.

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Wojciechowska, L. and Wachowska, M. (1964). [Specific antibodies in sera of patients infected with Taenia saginata.] Medycyna dosw. Mikrobiol. 16, 343-346. Wolff, F., Schanabel, R. and Moldenschardt, H. (1959). [A fatal case of mepacrine poisoning during the treatment of tapeworm infection by the intraduodenal route. Z . arztl. Fortbill. 53, 683-687. Wu, L. S. (1939). Taenia infection. Report based on stool examinations of 56,286 patients in the Peiping Union Medical College. Chin. med. J . 55, 561-565. Yaqub, M. (1953). Cysticercirs bovis in a bullock. (Abstract.) Proc. Pakist. Sci. Conf, 5th 1953, Medicine a. Veterinary Science Section, p. 13. Yokogawa, M., Yoshimura, H., Okura, T. and Saito, M. (1962). [Treatment of Taeniu saginata with bithionol.] Jap. J. Parasit. 11, 3 9 4 4 . Lapart, W. ( 1 968). Zastosowanie antygenu frakcjonowanego w serologicznej diagnostyce tasiemczyc u ludzi. Wiad. Parazyt. 14, 203-209. Zapart, W., Adonajlo, A. and Gancarz, Z. (1969). Proby srodskorne z alergenami frakcjonowanymi w diagnostyce tasiemczyc u ludzi. W a d . Parazyt. 15,77-81. Zapatel, J., Ubieto, A. and Martinez, M. (1965). Cysticerci in processed meat in Guatemala. Am. J. trop. Med. Hyg. 14, 1 13-1 16. ZelejkoviC, S. and Bokovic, T. (1 959). Istraiivanje bobicavosti kod goveda i teladi zaklanih u banjaluEkoj klaonici 1957 godine. Vet. Glusn. Belgrade 13, 308-310. Zembrzuski, K . (1965). Materialy do epidemiologii tasiemczyc. Wiad. Parazyt. 11, 161-164. Zunker, M. (1935).DieAbtotung der Rinnderfinen durchKuhl-und Gefrier-verfahren. Z . Fleisch-u. Milchhyg. 45, I 2 1 -I 26. Zwierz, C. (1 963). Skojarzone leczenie inwazji Taenia saginata. Bull. Inst. Mar. Med. Gdat'isic, 14, 289-29 1 . Zwierz, C. (1964). Modyfikacjaleczenia inwazji Taetiiasaginuta preparatem Yomesan. [A modified treatment of Taenia saginata invasion with Yomesan.] (Abstract.) Wial. Parazyt. 10,454-455. ADDITIONAL REFERENCES ADDED IN PROOF

Brandes, H. (1958). Untersuchungen zur Feststellung der Finnigkeit beim Rind unter besonderer Beriicksichtigung der Untersuchung mit filtrierten U.V.Strahlen. Archiv Lebensmittelhjg. 9, 241-243. Graber, M. (1959). La cysticercose bovine. Son importance dans les zones sahaliennes d'elevage de la Republique du Tchad. Revue Elev. MPd, vkt Pays trop. 12, 121-143. Naumov, N. A. (1929). A case of cysticercosis of heart and meninges. Perm. Med. Zh. 7, 1-2.

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SHORT REVIEW Supplementing Contribution of Previous Volume

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The Structure of the Helminth Cuticle D. L. LEE*

Houghton Poultry Research Station, Houghton, Huntingdon, England

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............ I. Introduction ....................... ..... ...... 11. Turbellaria .................................................................................... A. Structure ............................................. ............................. B. Function ....... .................................................... 111. Monogenea ............................................... .................................... .................. A. Structure .................................. B. Function ................................................................................. .......... IV. Digenea ............................................ ............. A. Structure ................................................................................. B. Function ................................................................................. ................. V.

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I. INTRODUCTION This short review supplements the earlier one (Lee, 1966b) and should be read in conjunction with it. Because of the limit on size of these up-dated reviews emphasis will be placed on completely new work and less attention will be paid to work which consolidates, or is very similar to, previously described work. When the earlier review was published little attention had been paid to the outer coverings of larval helminths. This has now changed and much of the work described in this review is on larval forms and on the development of the outer covering of the adult.

* Present address: Dept. of Pure and Applied Zoology, University of Leeds. 347

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11. TURBELLARIA

A.

STRUCTURE

Kronborgia amphipodicola is an endoparasitic turbellarian which lives in the body cavity of certain amphipods. It is dioecious and both sexes lack mouth, pharynx, intestine and excretory system. The female has a single-layered epidermis” which rests on a thin basal lamina. Sub-epidermal gland cells are numerous. The epidermis is covered with numerous cilia and long microvilli. The cilia are arranged in longitudinal rows and have a cross-striated rootlet running from the basal body of the cilium into the epidermis. The microvilli have globular expanded tips and narrow bases but show no internal differentiation. A glycocalyx covers the epidermis. Rhabdite-like structures occur close to the outer surface of the epidermis. Nuclei lie close to the base of the epidermis; Golgi bodies, poorly developed endoplasmic reticulum, ribosomes, large lipid droplets, mitochondria and an irregular network of microtubules are also present (Bresciani and Karie, 1970). An interesting aspect of this epidermis is the apparent breakdown of the lateral membranes of the epidermal cells. Lateral membranes are seldom continuous; in most places only the basal part of the lateral cell membrane remains. The outer regions of some epidermal cells are connected by desmosomes but these disappear during development. The sub-epidermal gland cells have long slender processes which pass through the epidermis to the surface. Desmosomes connect the process to the epidermis at the surface. After the female has left the host and has completed spawning the epidermis changes in character, apparently as a result of histolysis (Bresciana and K&e, 1970). B.

FUNCTION

K . amphipodicola possesses no alimentary tract and grows considerably in 10 months and it must therefore absorb nutriment from the host through the epidermis. The epidermis of free-living turbellaria possesses short microvilli but that of K . amphipodicola possesses numerous long microvilli; it would appear that these enlarged microvilli are an adaptation to parasitism as they increase the absorptive area of the parasite. The sub-epidermal glands are believed to function during escape of the parasite from the host and also during construction of the cocoon. 111. MONOCENEA A.

STRUCTURE

When the earlier review was written there were no papers published on the ultrastructure of the outer covering of the Monogenea. Brief descriptions of the adult epidermis of Lepfocotyle minor, Rajonchocotyle emarginata,

* The term “epidermis” is used throughout this review to denote what in trematodes and cestodes was once commonly known as the “cuticle” and, by some writers more recently, the “tegument” or “integument” (see Rohde’s review in this volume-Ed.).

FIG.1. Electronmicrograph of T.S. body wallof the unusual juvenilemonogenean Anzphibclella flavolimwtu, from the blood system of an electric ray (Torpedo nobiliuna). The outer epidermis is a cytoplasmic syncytium bearing small microvilli and it contains dense granules and mitochondria. The nucleated epidermal “cell” body which connects with this layer lies beneath the basement lamina and muscle layers and secretes dense granules into the superficial epidermis. bl, basement lamina; dg, dense granules; ep, epidermis; epc, epidermal “cell” body; mu, muscle; mv, microvilli; nu, nucleus. (From Lyons (1971). Parasitology 62. By kind permission of the author and Cambridge University Press.)

FIG.2A. Electronmicrograph of the syncytial epidermis of Acunthocotyle eleguns from the dorsal surface of Raiu cluvafu.The epidermis bears microvilli on the dorsal surface of the worm and contains two kinds of granular inclusions as well as mitochondria. FIG.2B. Electronmicrograph of L.S. body wall of Acunthocotyle eleguns showing a large epidermal “cell” body in the parenchyma which contains many Golgi bodies secreting the epidermal granules. Several processes are given off from this “cell” and penetrate the muscle layers and basement lamina to connect with the superficial cytoplasmic, syncytial epidermis. bl, basement lamina; ep, epidermis; epc, epidermal “cell” body; g, Golgi bodies; mu, muscles; mv, microvilli ; nu, nucleus; pr, processes of epidermal “cell”. (By kind permission of Dr. K. M. Lyons.)

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Gastrocotyle trachuri and Dictyocotyle coeliaca have been given by Lyons (1968). More recently, fuller descriptions of the epidermis of adult Entobdella soleae, Acanthocotyle elegans and Gyrodactylus sp. and of the unborn juvenile of Gyrodactylus sp. have been given (Lyons, 1970a, b). The outer covering of all of these species is a cytoplasmic epidermis which is syncytial(Figs 1and2),exceptinthe head region of E.soleae. Nuclei do not occur in this syncytial epidermis but, in E. soleae and A . elegans, they are situated in nucleated extensions of the epidermis that lie in the parenchyma beneath the outer muscle layers (Fig. 2B) (Lyons, 1970a).Nuclei are apparently absent from the epidermis of adult Gyrodactylus and no sunken nucleated regions were found (Lyons, 1970b). The dorsal surface of E. soleae and A . elegans, including the dorsal surface of the haptor, bears long microvilli but the ventral surface, including the ventral surface of the haptor, is smooth. The epidermis which covers the adhesive head glands is densely covered with microvilli. An amorphous surface coat, probably glycocalyx, covers all of the epidermis. In the epidermis of E. soleae small mitochondria with few cristae lie near the base, and electron-dense inclusions are scattered in the cytoplasm. The epidermis is attached to the basement lamina by half-desmosomes. The cytoplasm of the nucleated cell-like structures contains more ribosomes than the outer epidermis, Golgi complexes, granular endoplasmic reticulum and mitochondria. The epidermis of A . elegans (Fig. 2) is similar to that of E. soleae but it contains two types of secretory inclusion and also has two types of nucleated cell-like structure sunk in the parenchyma. The epidermis of Leptocotyle minor, Rajonchocotyle emarginata and Gastrocotyle trachuri is rather similar to that of E. soleae and A . elegans. The epidermis of the endoparasitic monogeneans, Dictyocoryle coeliaca and juvenile Amphibdellaflauolineata, is not obviously modified as an adaptation to endoparasitism (Lyons, 1968). Diclidophora merlangi has an epidermis which is more like that of adult Digenea than of the other Monogenea which have been described. The syncytial epidermis is connected by cytoplasmic processes to nucleated celllike structures in the parenchyma; a few finger-likeprotrusions extend from the surface and bristle-like structures occur on the epidermis of the buccal region (Morris and Halton, 1971). The epidermis of Gyrodactylus sp. has short microvilli scattered over the surface and contains small mitochondria, lamellate inclusions, Golgi complexes and membrane-bound vesicles with fibrous contents, some of which open to the exterior. The epidermis which covers the ventral adhesive head glands bears many long microvilli and contains denser vesicular inclusions. The epidermis which covers the posterior haptor is similar to, but thinner than, the epidermis of the main body region (Lyons, 1970b). The late-stage juvenile of Gyrodactylus sp., which lies within the parent, has no microvilli, or other epidermal processes. Unlike the epidermis of the adult, that of the juvenile worm is packed with ribosomes. Nuclei are present in the epidermis of the juvenile but these apparently disappear in the adult worm (Lyons, 1970b).

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A study of the early embryos of E. soleae dissected from the egg suggests that the original ciliated cells are replaced by other ciliated cells which arise in the parenchyma (Lyons, 1968), as described by Skaer (1965) for the embryos of the free-living turbellarian Polycelis tenuis. The unciliated adult epidermis, which initially has superficial nuclei, appears under these ciliated cells. Later, the epidermal cell bodies differentiate but remain sunk in the parenchyma. In the hatched oncomiracidium the ciliated cells overlie the thin adult epidermis which, although at first discontinuous, may eventually cause shedding of the superficial ciliated epidermal cells by spreading beneath them (Lyons, 1968). B.

FUNCTION

Lyons (1970a) has suggested that the function of the microvilli on the epidermis of the Monogenea may be to support a layer of mucus or, alternatively, to increase the surface area and thus facilitate respiratory exchanges. The role of the mucus layer may be to protect the epidermis from abrasion and to discourage the growth of bacteria and other micro-organisms on the body surface. Neither ferritin nor thorium dioxide were taken up by E. soleae, A . elegans or Gyrodactylus sp. Non-specific esterases, acid and alkaline phosphatases were not detected in the epidermis of these three worms (Lyons, 1970a, b). Lyons (1970a) suggested that the surface coat of mucoprotein may bind ions such as Ca2’,prior to uptake by the worm. The microvilli which cover the epidermis of the adhesive head glands of E. soleae and A . elegans may assist in spreading the adhesive secretion of the head glands over the skin of the host into a thin “tacky” film and may also help to mix the products of different gland cells (Lyons, 1970a). Morris and Halton (1971) found that inclusion bodies in the epidermis of D.merlangi are continually secreted on to the surface of the worm and could have a protective function. They also found evidence that the epidermis may be involved in absorption of nutrients, especially through the opisthaptor. The bristle like protuberances on the epidermis of the buccal region suggest an abrasive or adhesive function; it is possible that they are responsible for rupturing blood vessels of the host tissues as the parasite is sanguinivorous. Lyons (1970a) has proposed an interesting hypothesis about the origin of the cuticle in some other invertebrates. Microvilli are characteristic of the epidermal and epithelial layers of both invertebrates and vertebrates and Lyons suggests that the extra cellular covering layers, such as earthworm cuticle, pogonophoran cuticle (see Gupta and Little, 1970) and even insect cuticle, could have arisen from ancestors which had a body surface similar to that of the monogeneans described above if the mucoprotein which lies over and between the microvilli were to become stabilized and perhaps collagenous (or chitinous). 1V. DICENEA A.

STRUCTURE

1. Miracidia Wilson (1969) and Southgate (1970) described the ultrastructure of the outer covering of the miracidium of Fasciola hepatica, and Southgate (1970) has

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described the changes which occur during development of the sporocyst from the miracidium. The epidermis of the miracidium of F. hepatica is made up of 21 ciliated cells which are arranged in five tiers (Dawes, 1960). These are separated from each other by a syncytial non-ciliated ridge of material formed by an extension of the sub-epidermal layer to the surface. The ciliated cells are attached to the ridges by prominent desmosomes. The cilia and their tapering rootlets have been described by Wilson (1969). The nucleus of the ciliated cells lies near the posterior border of the cell. In the miracidium of Schistosoma mansoni the nuclei of the ciliated epidermal cells lies in extensions of the cell below the muscles of the body wall (Brooker, in Southgate, 1970). Numerous cytoplasmic projections are present between the cilia of the epidermal cells in F. hepatica and large numbers of mitochondria, membrane-bound vesicles and large amounts of glycogen are present in the cells. The surface of the miracidium is coated with a thin layer of acid mucopolysaccharide (Wilson, 1969). The intercellular ridges contain mitochondria, elongate membrane-bound vesicles and granules. Nucleated cells, which lie below the muscle layers of the body wall, are in cytoplasmic continuity with the syncytial ridges and form the sub-epidermal layer (Southgate, 1970). As the ridges are syncytial and are in continuity with the sub-epidermal cells then the whole complex forms a syncytium. The apical papilla has no ciliated epidermal cells; the surface is covered with a thin corrugated layer of cytoplasm and is connected by cytoplasmic processes to the apical gland (Wilson, 1969).

2. Sporocysts Dawes (1960) has shown that when the miracidium of F. hepatica penetrates the snail the ciliated epidermal cells are shed. This has been confirmed by Wilson (1969) and Southgate (1970). According to Wajdi (1966), the miracidia of S. mansoni does not shed these cells during penetration of the snail. Southgate (1970) described the changes which occur in the outer layer of the trematode during penetration of the snail and during consequent development of the sporocyst stage. During penetration large vacuoles appear beneath the ciliated cells and these are eventually cast. The intercellular ridges then flow over the exposed muscles of the body wall to form a thin cytoplasmic covering. The membranous vesicles of the ridges apparently contribute their membrane to this rapidly forming layer and material from the sub-epidermal cells also contributes to the formation of the layer. It is complete within 2-3 h after penetration. This syncytial layer then increases in depth and develops the characteristic structure of the outer covering of the sporocyst. No cytoplasmic connections between the epidermis of the sporocyst and sub-epidermal cells were detected but these may be broken and reformed depending upon the requirements of the epidermis. Thin folds extend from the surface of the epidermis; it contains mitochondria, small amounts of glycogen, and a few Golgi complexes but no nuclei (Southgate, 1970). The sporocysts of other trematodes which have been investigated are rather similar to that of F. hepatica in that they have an outer syncytial epidermis,

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covered with cytoplasmic folds or microvilli, which is usually in cytoplasmic continuity with nucleated cell-like bodies in the parenchyma. Examples are Posthodiplostonium cuticola and an unidentified strigeid (Ginetsinskaya et al., 1966), and the sporocysts of Cercaria pectinata (Matricon-Gondran, 1969), Cercaria buchanani and an unidentified strigeid (Bils and Martin, 1966). According to Matricon-Gondran (1969) the sub-epidermal cell-like structures originate in the parenchyma and later make contact with the outer epidermis: also, the epidermis of the redia and cercaria is apparently derived from the primary syncytial epidermis of the embryo. According to James et al. (1966) the outer covering of the daughter sporocysts of Cercaria bucephalopsis hairnaena consists of a syncytial cytoplasmic layer in which nuclei are present and are not in sunken portions in the parenchyma. 3. Rediae The outer covering of rediae appears to be similar in the few species which have been studied. There is a cytoplasmic syncytial epidermis which has no cytoplasmic connection with cells in the parenchyma. The outer surface is thrown into folds or microvilli; mitochondria are present in the epidermis but nuclei have not been detected. Rees (1966, 1971a) described the redia of Parorchis acanthus; Bils and Martin (1966) described that of Acanrhoparyphium spinulosum; Ginetsinskya et al. (1966) that of Petasiger neocommense, Krupa et al. (1967, 1968) that of Cryptocotyle lingua and Dixon (1970) that of Cloacitrema narrapeenensis.

4.Cercariae An understanding of the early development of cercariae is essential if one is to determine the origin of the outer layer of cercariae, metacercariae and adults but surprisingly little attention has been paid to this aspect of the life cycle. Bils and Martin (1966) described the development of the cercarial epidermis in Acanthoparyphium spinulosum. In rediae, the germ cell is enveloped by one or more supporting cells; later, cell membranes of this supporting layer disappear so that the germ cell is surrounded by a syncytial layer. The germ cell then divides to form the germinal ball. Once this germinal ball is a multicellular mass, the enveloping syncytial layer, which originated from the redia, is shed. Prior to this, peripherally located cells of the germinal ball form a syncytial outer layer which is the epidermis of the cercaria. The cell bodies of the epidermis remain within the parenchyma but retain cytoplasmic connection with the epidermis. Dixon and Mercer (1967), however, stated that the outermost layer of the cercariae of F. hepatica within the redia is a cellular embryonic epithelium, which accumulates mucopolysaccharide, mucoprotein and tanned protein granules from secretory cells within the parenchyma. This embryonic epithelium apparently forms the outer covering of the cercariae and is shed when the cyst of the metacercaria is formed. Hockley (1970a) stated that the cercariae of Schistosoma mansoniare covered at an early stage of development with an epithelium of flattened, nucleated cells.

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The outer covering of the cercaria appears beneath this epithelium as a similar thin, cytoplasmic, nucleated, syncytial layer. The epithelium is lost before much differentiation of the embryo has occurred and at about the same time the nuclei of the cercarial epidermis degenerate and disappear. The surface coat on the cercaria is produced by the epidermis once the primitive epithelium is lost. The sub-epidermal cells are only temporarily connected to the epidermis. According to Rifkin (1970), however, the development of the cercaria ensues as germinal cells enter the lumen of the sporocyst, divide, and produce a germ ball. After the cercarial cells begin to differentiate, a number of elongate daughter sporocyst cells, which line the lumen of the sporocyst, surround the cercarial germ ball. These cells form the cytoplasmic syncytium which will become the epidermis of the cercaria. Development of the epidermis of the cercaria of Cloacitrema riarrabeenensis is similar to that described by Hockley (1970a) for S. mansoni (see Dixon, 1970). The epidermis of emerged cercariae is fundamentally the same in all species which have been examined. There is a syncytial cytoplasmic epidermis, containing mitochondria but no nuclei, which is in cytoplasmic continuity with nucleated cell-like structures in the parenchyma, i.e. a typical sunken epidermis except that it is syncytial. Microvilli are rarely present on the surface. The structure of the epidermis varies in different regions of the body (Hockley, 1968; Rees, 1967, 1971a, b). The epidermis of the main body of the cercaria contains a variety of secretory granules, some of which appear to produce mucopolysaccharides, as in Acanthatriunz oregonense (see Belton and Harris, 1967). An outer mucus-like covering on the cercaria of Schistosoma mansoni has been described by several authors (see Kemp, 1970). Descriptions of the epidermis of the cercaria and schistosomula of S. mansoni have been given by Smith et al. (1969), by Bruce et al. (1970) and by Morris and Halton (1971) (cercaria only). The epidermis of the schistosomula is similar to that of the cercaria but has fewer mitochondria. Inatomi et a/. (1970) gave brief descriptions of the epidermis of Metagonimus takahoshii, S. japonicum and S. spindale.

5. Adults Several papers on the ultrastructure of the outer covering of a variety of adult digeneans have appeared since the last review but it is impossible to describe them in detail in the space allotted. The epidermis of S. niansoni was studied by Morris and Threadgold (1968), Smith et al. (1969) and Silk et al. (1969, 1970) and they extend the brief description given by Lee (1966b). Very few mitochondria are present in the epidermis and the structures originally described as large vacuoles are probably channels which extend down into, but not through, the epidermis. Hockley (1970b) has shown that the outer membrane of the epidermis of S. mansoni usually consists of four dense layers separated by three less dense layers and that some of these layers are lost by delamination. Dense elliptical bodies and spherical membranous bodies, both of which are formed in the sub-epidermal cells, pass into the epidermis where the elliptical bodies probably contribute to the ground substance of the epidermis while the spherical membranous

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bodies may contribute to the outer membrane. It is suggested that this outer membrane is continuously delaminated and is reformed by the membranous bodies. The epidermis of S. japonicum appears to be similar to that of S. mansoni (Inatomi et al., 1969, 1970). Burton (1966) found that the epidermis of Gorgoderina sp. was similar to that of Haplometra but it lacked spines. The following digeneans have been shown to possess the basic epidermal structure, with minor modifications: Dicrocoelium dendriticum (see Reznik, 1966); Ornithobilharzia turkestanicum (see Logachev, 1964); Clonorchis sinensis (see lnatomi et al., 1968a, 1970); Haplometra cylindracea (see Threadgold, 1968); Posthodiplostomum minimum (see Bogitsh and Aldridge, 1967) ;Megalodiscus temperatus(see Bogitsh, 1968);F. hepatica(see Threadgold, 1967); Metagonimus yokogawai takashii (see Inatomi et al., 1968b, 1970); Opisthorchis viiierrini and Paragonimus ohirrai (see Inatomi et al., 1970). Erasmus, in an excellent series of papers (Erasmus, 1967, 1968, 1969a, b, c, 1970a, b, c) has studied the structure of the adhesive organ and the outer covering of strigeid trematodes (see also Ohman, 1965, 1966). The outer layer of these trematodes is essentially the same as those of other digeneans but the adhesive organ is modified as a secretory and absorptive epithelium. Erasmus has also studied the surface of the lappets of these strigeids. It is apparent from the work done by Erasmus and others that there is surface differentiation in some trematodes. This is especially so in the case of S. mansoni (Smith et al., 1969). B.

FUNCTION

The ciliated epidermal cells of the miracidia are undoubtedly locomotory in function and are used to bring the niiracidium into contact with the next host. They may also assist in initial penetration of the mollusc. The outer coverings of the sporocyst and redia are apparently adapted to an absorptive function because their extensively folded epidermis will greatly increase the surface area of the parasite. Presumably it is involved in the uptake of nutrients from the molluscan host (see Dixon, 1970). The epidermis of the cercaria probably performs different functions at different stages in the life of this particular form. Within the redia it will probably be used in the uptake of nutrients through the body surface (Rees, 1971a). It may also play a part in avoiding the defence reactions of the host. Outside the mollusc it may serve in osmoregulation and ionic regulation. In a secondary intermediate host it may assist in the evasion of the host’s defence reactions or in the uptake of nutrients. The epidermis of cercariae is very important in the formation of the metacercarial cyst as the various granules which go to form the various layers of the cyst wall pass into and then out of the epidermis. According to Dixon and Mercer (1967) the granules which form the outer cyst wall are shed together with the outer layer of the cercaria of F. hepatica. Other granules then pass through the new epidermis to form the remaining layers of the cyst. The new epidermis is formed from the cells containing the keratin-type granules which migrate from deep within the cercaria to the external surface. Southgate (in press) has studied the changes which occur in the epidermis of the cercaria

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of Notocotylus attenuatus during the formation of the metacercarial cyst. The original epidermis is retained in an altered form, after the various components which form the cyst wall have been extruded, and becomes the epidermis of the metacercaria and of the adult worm. The epidermis of adult digeneans is still thought to play a part in the uptake of nutrients but this may vary from species to species. In S. mansoni horseradish peroxidase was taken up only by the dorsal epidermis of the male (Smith et a/., 1969). The outer surface of S. mansoni also plays an important part in “disguising” the parasite in the host (Smithers and Terry, 1969; Smithers et al., 1969; Clegg et al., 1971). In strigeids the adhesive organ apparently plays a part in bringing about histolysis of host tissue and in the subsequent uptake of nutrients (see papers by Erasmus).

V. CESTODARIA A.

STRUCTURE

The Cestodaria have, until recently, been classified as a separate group of cestodes. Recently it has been suggested that either they are monogeneans or that they occupy a phylogenetic position between the monogeneans and the cestodes (see Llewellyn, 1965). Lyons (1969) has studied the fine structure of the outer covering of Gyrocotyle urna, which resembles that of the cestodes more than that of the monogeneans. The cytoplasmic epidermis has numerous microvilli and is in cytoplasmic continuity with nucleated cell bodies situated in the parenchyma. The microvilli lack the dense tip which is so characteristic of the microvilli of adult cestodes, but terminate in a fine spike composed of an extension of the apposed apical plasma membranes. The epidermis contains rod-shaped bodies and they are apparently released at the surface to form the mucoprotein substance which overlies the surface. B.

FUNCTION

Of the various functions which the epidermis performs one of the most important will be the uptake of nutrients.

VI. CESTODA A.

STRUCTURE

I . Laroal cestodes The outer surface layer of oncospheres of Taenia taeniaeformis and of Hymenolepis citelli is a thin dense cytoplasmic layer which has long thin cytoplasmic evaginations on its surface but no nuclei or connections with nucleated cell-like bodies deeper in the body wall (Nieland, 1968; Collin, 1969). Nieland (1968) has described the formation of the various outer layers of the developing onchosphere of T. taeniaeformis. The cyst wall of Multiceps serialis invaginates to form the protoscoleces and

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is covered with a cytoplasmic layer, which is very similar in structure to that described for adult cestodes except that the outer border of microvilli lack the dense tip found on microvilli of adult cestodes (Race et al., 1965), The epidermis contains mitochondria and connections join it to cells in the parenchyma. In Echinococcusgranulosus the germinal “membrane” is continuous with the wall of the brood capsule and with the outer covering of the protoscolex (Morseth, 1967). Finger-like processes extend from this membrane into the cyst wall. The rest of the “membrane” is somewhat similar to the epidermis of the protoscolex but it contains nuclei within it. The wall of the brood capsule is a vacuolated layer which has nuclei within it at irregular intervals. The epidermis of the protoscolex is similar in structure to that of adult cestodes. The outer walls of the suckers are formed by the epidermis and have spined microvilli like the rest of the epidermis. After 42 days in culture the sunken cells of the epidermis were multinucleate and it has been suggested that this, togethei with an increase in number of mitochondria and of Golgi complexes, may be related to the rapid growth necessary for segmentation which occurs about this time (Morseth, 1967). The protoscolex of E. multilocularis has an epidermis similar to that of E. granulosus (Sakamoto and Sugimura, 1969). Development of larval E. multilocularis, including formation of the outer layers, has been well described by Sakamoto and Sugimura (1970). The bladder wall of Cysticercus jasciolaris consists of an outer epidermis and an inner parenchyma (Nieland and Weinbach, 1968); the epidermis is similar in structure to that of adult cestodes. That of C. longicollis is also like the epidermis of adult cestodes but the tips of the microvilli are not dense. The epidermis of the scolex is continuous with that of the bladder wall (Baron, 1968). The wall of C. bovis seems to be similar ($lais, 1970). During budding and scolex differentiation of the bladder wall of Taenia crassiceps the sub-epidermal cells dominate budding and it is suggested that they are multipotential cells, capable of migration and derived from undifferentiated parenchyma cells (Bilqees, 1970). The outer surface of the 3-day precysticercoid of Hymenolepis citelli in the beetle is a thin epidermis which is covered with long, thin microvilli. After 5 days in the beetle the epidermis bears shorter and fewer microvilli and host cells attached to these microvilli are frequently cytolysed (Collin, 1970). The epidermis of the cysticercoid of Raillietina cesticillus is covered with short microvilli (Baron, 1971). The surface layer of Tylocephalum sp. from the oyster is a non-nucleate syncytium connected by occasional cytoplasmic bridges to internal cell bodies. Long coiled microvilli are present on the surface (Rifkin etal., 1970). The epidermis of the procercoid and plerocercoid stages of Diphyllobothrium Zatum is similar to that of the adult worm except that lamellated bodies occur in the larval stages but not in the adult, and they have fewer microvilli. The larval epidermis also contains fewer mitochondria (BrAten, 1968a, b) Similar results were obtained by Timofiev and Kuperman (1968) for the procercoid and plerocercoid of Triaenophorus nodulosus. Charles and Orr (1968) studied the epidermis of the plerocercoid of Schistocephalus solidus and of Ligula intestinalis and found that they have the basic structure as found

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in adult cestodes. The microvilli have long tapering electron-dense spines but there are differences in the nature of the microvilli of the two species. Morris and Finnegan (1969) found that in the differentiating plerocercoid of S . solidus portions of the epidermis retain an apparently primitive or undifferentiated morphology during growth. The epidermis of the velum remains thin and similar to the epidermis of small worms but the superficial epidermis increases greatly in depth, develops basally situated mitochondria and elaborates numerous microvilli and other protrusions. Pore canals were found. 2. Adult cestodes Work published since 1965 on the structure of the outer covering of adult cestodes has confirmed the basic plan of the cestode epidermis. Lumsden (1966) carried out a thorough study of the outer covering of Hymenolepis diminuta, Lacistorhynchus tenuis and Calliobothrium verticillatum and clarified many points. The epidermis consists of an anucleate cytoplasmic layer covered with microvilli with dense spine-like tips and is in cytoplasmic continuity with nucleated cells in the parenchyma. These cells appear to synthesize proteins which are then transported to the outer epidermis. Morseth (1966) showed that the epidermis of Echinococcus granulosus, Taenia hydatigena and T. pisformis is similar to that of other adult cestodes but he found structures resembling pore canals in the epidermis. The epidermis of Diphylbothrium latum is similar to that of other cestodes. The microvilli on the plerocercoid increase in length, are slimmer and are more numerous in the adult and there is also an increase in the number of mitochondria present from the plerocercoid stage to the adult (Briten, 1968b). The basic plan of the epidermis has been demonstrated in T. multiceps (see Race et al., 1966); Triaenophorus nodulosus (see Timofiev and Kuperman, 1968); Caryoplzyllaeus laticeps, C. fennica and Anomotaenia constricta (see Biguin, 1966); Ligula intestinalis and Schistocephalus solidus (see Charles and Orr, 1968); Diphylidium caninum and Taenia saginata (see Inatomi et al., 1970). According to Howells and Erasmus (1969) the interproglottidal glands of Moniezia expansa consist of clusters of cells surrounding crypt-like invaginations of the epidermis. Three main types of epidermis were found covering the apex of the scolex, the suckers and the rest of the surface of the scolex; on the scolex it resembles normal cestode epidermis; on the apex of the scolex it resembles that on the posterior face of the mature proglottides, and on the acetabula it is thinner and the microvilli are short. B.

FUNCTION

The function of the bladder wall of larval cestodes is probably partly protective against the defence reactions of the host, partly nutritive and, in cases such as E. granulosus, partly to retain the numerous scoleces in one area of the host. Slais (1966) made an interesting comparison between the trophoblast of the mammalian embryo and the bladder of the cestode cysticercus. The epidermis of procercoids and plerocercoids probably plays an important

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role in the nutrition of these larval stages as well as serving as a protective and packing layer. There has been a lot of work published on the distribution of enzymes and on the uptake of nutrients by adult cestodes since the earlier review appeared, and all confirm the important role of the epidermis in the uptake of nutrients. Lumsden et al. (1970b) have shown that adult Hymenolepis diminuta do not take up thorium dioxide, carbon particles, ferritin or the 14C-labelled protein fraction from Chlorella vulgaris and claim that transmembranosis of colloids by tapeworms does not occur. The glycocalyx on the surface of tapeworms is capable of adsorbing cations at neutral pH (Lumsden et al., 1970a) and it also plays an important part in contact digestion (Taylor and Thomas, 1968).

V11. NEMATODA A.

STRUCTURE

Since the earlier review appeared a number of papers which describe the structure of the cuticle of a number of larval nematodes have been published and the subject has been reviewed by Bird and Bird (1969). Wisse and Daems (1968) published an excellent paper on the second stage larvae of Heterodera rostochiensis. Four different layers were distinguished in the cuticle: (1) a dark layer 250 A thick; (2) a fibrillar layer 0.25 pm thick; (3) an electron transparent layer about 0.15 pm thick, which is thought to be fluid filled and which is crossed by small columns of material; (4) a striated layer, 0.25 pm thick, which has characteristic striations with a periodicity of 200 A. This fourth layer is lined on its inner side by a thin dark layer. The striations are perpendicular to the surface of the cuticle. The lateral alae consist of three ridges of cuticle in which the layers remain the same except that the striated layer becomes fibrous, thicker and two-layered. This basic plan of the cuticle has been found, with modifications (usually one or more fibrous layers beneath the striated layer and a membrane or membrane-like structure on the surface of the cuticle) in a number of larval nematodes and also in a few adults. Examples are : the third-stage larva of Nippostrongylus brasiliensis (see Lee, 1966a; Janiuar, 1966; Inatomi et al., 1970); the third-stage larva of Necator americanus, Ancylostoma duodenale, A . caninum, Trichostrongylus orientalis, Strongyloides stercoralis, S. fulleborni and S. ratti (see Inatomi et al., 1963), S. myoptonii (see Colley, 1970) and Haemonchusplacei(see Smith, 1970); the fourth-stage larva and adults of Panagrellus silusiue (see Samoiloff and Pasternak, 1968, 1969; Yuen, 1968); third-stage larva of Neoaplectana glaseri (see Jackson and Bradbury, 1970); the second-, third- and fourthstage larvae and adults of Hemicycliophora arenaria (these nematodes are unusual in that they also possess a multi-layered sheath), adults and fourthstage larva of Hirschmaniella gracilis and H. belli and all stages of Aphelenchus avenue (see Johnson et al., 1970a, b); developmental stages of Heterodera schachtii (see Gunther and Kampfe, 1967); the second-stage larva of Meloidogyne javanica (see Bird, 1968) and of M . haplu (see Ibrahim and Hollis, 1967); adults of Ditylenchus dipsaci (see Yuen, 1967); adults of Tylenchorhynchus

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martini (slight differences between swarming and non-swarming individuals) (see Ibrahim, 1967) ; adults of Capillaria hepatica and Trichuris myocastoris (see Wright, 1968) and T. suis (see Bogoyavlenski, 1965; Jenkins, 1969); adults of Rhabditispellio (no striated layer mentioned) (see Beams and Sekhon, 1967); and the microfilaria of Dirojlaria immitis (see Kozek, 1970b). The cuticle of the second-stage larvae of Ascaris lumbricoides has been briefly described by Thust (1966) and that of the third-stage larva of A . mum illustrated, but not described, by Morseth and Soulsby (1969). In these there does not appear to be a striated layer. The cuticle has an outer membrane, a thin dense outer cortex, a thicker less dense layer and then what appears to be a fibrillar layer. A rib-like structure is present in the lateral alae (based on the plates in Morseth and Soulsby, 1969). Bogoyavlenski has studied the structure of the cuticle of a number of different nematode groups. In the Spirurata he studied Crassicauda crassicauda, Ascarops strongylina, Habronema muscae and Echinuria uncinata. The following features were typical of these species : (1) a single cortical layer; (2) two homogeneous layers between the fibrous layers (in all except E. uncinata);(3) one or two well-developed basal layers (Bogoyavlenski, 1961). The cuticle of Dictyocaulus iiuiparous, Metastrongylus elongatus, M . salmi and M . pudentotectus are similar to one another, but differ considerably from that of intestinal strongylids and ascarids. The cuticle is very thin and consists of a cortex, a homogeneous layer, a fibre layer and a basal layer (Bogoyavlenski, 1963). The cuticles of Oesophagostomum columbianum and of Delafondia vulgaris, which are intestinal species, have eight layers (Bogoyavlenski, 1964a). The cuticle of Syngamus skrjabinomorpha has five layers (Bogoyavlenski (1964b) ; that of Amidostomum anseris, Epomidiostomum orispinum and Ostertagia ostertagi have six, six and four layers respectively. Differences in the cuticles of 0. ostertagi and Mecistocirrus digitatus are related to the fact that one lives in the mucosa, and the other in the lumen of the abomasum (Bogoyavlenski, 1964~). The cuticles of two metastrongyloid nematodes, Crenosoma vulpis and Perostrongylus pridhani, consists of a cortex, a matrix and a basal layer. The so-called teguminal sheath of these nematodes is not a true sheath but corresponds to the cortical layer of the cuticle. The very wide matrix layer, which separates the cortex from the basal layer, is thought to contain a fluid (Stockdale et al., 1970). The cuticle of the third-stage larvae of Contracaecirm multipapillaturn is rather similar to that of adult Ascaris lumbricoides but has one, not three, fibre layers. There is no striated layer present (Larsh et al., 1968). Bruce (1970) has described the formation of the first cuticle and the cuticles of the pre-infective and infective larvae and of the adult of Trichinella spiralis. The embryo in utero is covered by a thin sheet of mucus-like material and by the egg-shell. The early post-embryonic larvae is covered by this mucoid-looking material. Internal to this is a thin dense layer (precursor of the outer membrane) and a fine homogeneous layer attached to the hypodermis by half-desmosomes at crests in the hypodermis. The cuticle of the late-stage larva in utero has an outer membrane, a cortex and an inner fibrillar layer. The pre-infective larva,

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11-12 days after parturition, in the muscles of the host has a cuticle consisting of an outer membrane, a cortical layer, a medial layer and a fibril layer. That of the infective larva has an outer membrane, an outer and inner cortex, a thin dense medial layer and two fibril layers (see also Despommier et al., 1967). In the cuticle of the adult worm the medial layer is striated and the orientation of the fibrils in the two fibril layers is more clearly shown. The cuticle of the microfilaria of Litomosoides carinii has an outer and an inner membrane separated by a thin amorphous layer (Schardein et al., 1968). The cuticle of the fourth-stage larva of Nematospiroidesdubius is divided into six layers. The outer membrane is covered by fine filamentous material to which Thorotrast adheres. There is an outer and inner cortex, a matrix and two fibre layers. Dense bars are embedded in the matrix layer and extend into the longitudinal ridges of the cuticle. The outer membrane and the outer cortex of the adult cuticle are similar to those of the fourth-stage cuticle, but the rest of the cuticle is not clearly layered. Bars, which support the longitudinal ridges, are present (Bonner et al., 1970). The cuticle of the fourth-stage larva of Nippostrongylus brasilirnsis is similar to that of the adult (Lee, 1970b). Tsubota (1966) and Inatonii et al. (1970) have shown that the cuticle of Enterobius vermicularis is very similar in structure to that of Aspiculuris tetrupteru (Anya, 1966). The cuticle of Syphacia obveluta consists of cortical, matrix and basal layers in the larva, young female and mature male (Dick, 1970). There is a striated zone in the cortex; tubules were observed in all regions of the cuticle, except the cortex. The gravid female has a thicker cuticle and the matrix layer contains a lot of striated material. Regional differentiation of the cuticle gives rise to alae, annulae and striae. The cuticle of the cephalic regions of Trichodorus christiei consists of an outer and an inner cuticle with a space between. The outer cuticle is covered by a membrane and has an outer fibrous layer followed by an inner electron dense homogeneous layer. The inner cuticle consists of a homogeneous material (Hirumi et al., 1968). The cuticle of Xiphinema index has been re-described by Roggen et al. (1967). There is an outer membrane, a structureless layer, a layer consisting of regularly spaced longitudinal ribbons, three fibre layers, a layer of variable thickness consisting of a number of sub-layers, and a basal layer. The cuticle of Longidorus macrosoma has a similar structure (Aboul-Eid, 1969). Wright and Hope (1968) have shown that the punctations and pore complexes in the cuticle of Acanthonchus duplicatus are due to the presence of dense material within the middle layer of the cuticle in the form of rods and collar-like rings. The cuticle is three-layered. The pore passes through the cuticle into the hypodermis. They concluded that these pore complexes are not campaniform sense receptors. Lee (1970a) described the cuticle of adult female Mermis nigrescens. There is an epicuticle of muco-protein-like material on the surface membrane. The cortex is penetrated by canals which extend from the surface to the matrix of the layer beneath the cortex (Fig. 3). Two layers of giant fibres, which spiral

FIG.3A. Electron micrograph of L.S. outer layers of the cuticle of Mermis nigrescens to show the canals in the cortex and the outer layer of giant fibres. x 29 O00. FIG.3B. Electron micrograph of H. (horizontal) S . cortex of the cuticle of Mermis nigrescens to show the canals cut in cross section. x 36 000. c, canal; cl, cortical layer; gf, giant fibre.

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around the nematode, lie beneath the cortex (Fig. 3A) and beneath these is a thick layer containing a network of fibres and a basal layer. The canals in this cuticle are much smaller than the pore canal complex described by Wright and Hope (1968) for Acanthonchus. Riding (1970) has made the startling discovery that adult females of Bradynema sp., which live in the haemocoel of the mushroom fly Megaselia halterata, lack a cuticle. The hypodermis has a microvillous surface and that is the outer covering of the nematode. Deladenus siricidicola also has scattered clusters of microvilli on its surface. Green (1967), de Grisse and Lagasse (1969) and Ogden (1971) have used the scanning electron microscope to study the cuticular structure of nematodes. This technique is very useful in the study of surface configuration but does not reveal internal structure.

Moulting A number of important papers describing moulting and cuticle formation have appeared since the earlier review (1966) and that of Bird and Bird (I 969) were published. Roggen et al. (1967) briefly described moulting in Xiphinema index. Cyclical fluctuations of leucine aminopeptidase occur in the hypodermis and it is thought that this enzyme could be involved in the breakdown of the old cuticle and the synthesis of the new cuticle. Samoiloff and Pasternak (1969) described the formation of the new cuticle at each of the postpartum moults of Panagrellus silusiae; it is similar for each moult. At the beginning of the moult a fibrous material accumulates adjacent to the hypodermis. Eventually a new cuticle forms beneath thepre-existing one; this new cuticle lacks organization during the early stage of the moult. Shedding of the old cuticle varies at different moults. In the second and third moults and in the moult to the adult female, the cuticle is discarded gradually. At the moult to form the adult male the old cuticle splits and is shed in one piece. Resorption of the old cuticle does not occur. Johnson et al. (1970b) studied cuticle formation and moulting in Hemicyliophora arenaria, Aphelenchus avenue and Hirschrnanniella gracilis. In all parasitic stages of H . arenaria the moult commenced with the separation of the cuticle from the hypodermis. The new sheath and cuticle were then formed by the hypodermis. Most of the old cuticIe is apparently absorbed before ecdysis. Fourth larval stage males undergo a final moult-a double moult during which a sixth cuticle is formed. The sheath is produced at each moult and must be regarded as an integral part of the whole cuticle and not as a residual cuticle. Moulting in A. avenue and H. gracilis was less complex. After cuticle separation the hypodermis gave rise to a new three-layered membrane, the future cortex, the matrix and striated layers. The old cuticle broke down as moulting neared completion. Observations on the last moult of the developing female of Syphacia obvelata indicate that during formation of the new cuticle striated regions are laid down between projections of the hypodermis in close association with the cell surface (Dick, 1970). It is suggested that striated material is deposited at

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the cuticle-hypodermis interface and moves through spaces within the basal layer to the matrix layer where it is deposited. Thust ( I 966) stated that in the second moult of Ascaris lumbricoides, which occurs within the egg, the cortex separates from the middle layer and a new membrane forms on the outside of the middle layers. Subsequently the new cortex develops between the new membrane and the middle layer; all that remains of the moulted cuticle is the external cortical layer (Crandall and Arean, 1967). During cuticle formation in Nematospiroides dubius the outer hypodermal membrane becomes the outer membrane of the new cuticle. The cortex and matrix layers of the adult cuticle form by differentiation of hypodermis cytoplasm underneath the cuticle/hypodermis membrane. The fibre layers form under the matrix layer by secretion from within the hypodermis (Bonner et al., 1970). In the final moult of Nipposrrongylus brasiliensis the old cuticle separates from the hypodermal membrane and the new cuticle is secreted between the outer hypodermal membrane and a new hypodermal membrane which forms beneath it. The first layers to be formed under the outer membrane of the new cuticle are the two fibre layers (Fig. 4). Formation of the outer cortex and of the struts is associated with an increase in rough endoplasmic reticulum in the hypodermis. The struts separate out from the fibrillar and granular components of the outer cuticle (Fig. 5). Formation and secretion of* the cuticular substances by the hypodermis is similar to secretion of collagen by fibroblasts. There is no resorption of the old cuticle (Figs 4, 5) (Lee, 1970b). In Trichinellu spiralis the moulting infective larva in the intestine of the host forms a new cuticle beneath the old cuticle and this old cuticle is shed at an early stage in development of the new cuticle. The cast cuticle consists of the outer membrane, the medial layer and parts of the fibril layers; the rest of the old cuticle is apparently digested, possibly by digestive enzymes in the host’s intestine. A cast cuticle has not been observed around the encapsulated larva in the muscles of the host although a moult probably occurs there 12 days after parturition (Bruce, 1970). Kozek (1970a), however, states that all four moults occur in the intestine of the host. During formation of new cuticle the material of the cuticle is secreted into trough regions of the outer hypodermal membrane under the previously formed outer membrane of the cuticle (Bruce, 1970). According to Kan and Davey (1 968) the adult cuticle of Phocanema decipens is deposited at the edge of the hypodermis as three discrete layers of protein. The cortex is keratinized at the periphery as soon as it appears and later differentiates into two layers. The middle layer differentiates into three bands, apparently by the secretion of more material from the hypodermis. The larval cuticle becomes loosened from the developing adult cuticle as soon as the second primary layer is formed, but ecdysis does not occur in culture until the new cuticle is fully differentiated. Ecdysis is also described by Davey and Kan (1968). According to Kampfe (1966) the last moult of various cyst-forming

FIG.4. Electron micrograph of L.S. body wall of a moulting fourth-stage larva of Nippostrongylus brasiliensis (middle stages of moulting). x 26 000. h, hypodermis; mu, muscle; ncu, new cuticle; ocu, old cuticle.

FIG.5. Electron micrograph of L.S. body wall of a moulting fourth-stage larva of Nippostrongylris brusiliensis (late stages of moulting). x 20 OOO. h, hypodermis; ncu, new cuticle; ocu. old cuticle.

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nematodes may be a partial one in that some layers of the cuticle are retained while a new basal layer is formed. It would appear that moulting differs in different types of nematode and sometimes in different stages of the life cycle. Some species break down and resorb much of the old cuticle whereas others discard it almost intact. This may be related to the environment of the nematode. For example, it is to the advantage of a moulting larva inside an egg to reduce the thickness of the old cuticle, as it has to live within this cast cuticle in the confines of the egg until it is released from the egg. A thin flexible cuticular remnant allows greater growth and freedom of movement than a thicker intact cast cuticle. The larva also depends upon stored foods in the egg for its development and will therefore have a greater need for the amino acids and carbohydrates of the broken down cuticle than will nematodes which are able to feed freely on exogenous nutrients. Similarly, nematodes which are fixed in one place in the tissues of the host animal or plant, e.g. Meloidogyne and infective larvae of Trichinella spiralis, will obtain an advantage if they greatly reduce the thickness of the old cuticle; the cuticle will be more pliable and, being thinner, will be easier to break by their restricted body movements. Actively moving nematodes will be able to free themselves of thicker cuticles more easily and, especially i n nematodes parasitic in the alimentary tract of animals, the old thick cuticle will also protect the nematode while the new cuticle is thickening and becoming resistant. B.

FUNCTION

There is little to add to the comments given in the earlier review on the function of the cuticle of nematodes. The lack of a cuticle and the presence of microvilli on the body wall of some insect parasitic nematodes is obviously related to the uptake of nutrients through the body wall of these nematodes (Riding, 1970). The function of the pores in the cuticle of Acanrhoncus (Wright and Hope, 1968) and of the small canals in the cuticle of Mermis (Lee, 1970a) is obscure; it may be that in Mermis they secrete the epicuticle. It has been suggested by Wright (1968) that the striated layer, which occurs in the cuticle of many nematodes, provides the tensile strength given by fibre layers in the cuticle of other species of nematode. Lee (1969) has suggested that in those nematodes which have broad, blunt lateral alae, such as the third-stage larvae of Nippostrongylus brasiliensis, the shape of the alae is such that they give the larva a stable base during movement, as nematodes lie on their sides and move by means of dorso-ventral undulations. The alae, especially the longer, sharper type, will also act as a fin during swimming. The fluid-filled layer in the lateral alae of the third-stage larva of N . brasiliensis may reduce the effect of shearing forces set up in this part of the cuticle when the larva moves in thin films of moisture by increasing the elasticity of that part of the cuticlewhichlies between the substratum and the contracting muscles of the nematode. Lee (1969) has also suggested that the fluid-filled layer of the cuticle of adult N . brusiliensis may play an important role in locomotion.

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VIII. ACANTHOCEPHALA A.

LARVAL FORMS

Butterworth (1969) has described the development of the body wall of Polymorphus minutus in its intermediate host. The cortex of the early acanthella is a syncytium which contains giant nuclei, mitochondria, Golgi bodies, endoplasmic reticulum and a few lipid droplets. The cuticle, which is similar to that of the adult, is penetrated by pores which open into vesicles in a vesicular region below the cuticle. The pores in the cuticle increase in number as the animal grows. A pore canal layer develops beneath the pores in the cuticle towards the end of development of the late acanthella stage. The outer cortex of the cystacanth has a cuticle and pore canals similar to that of the adult. The body wall of the acanthor of Moniliformis dubius is composed of several components. The outer three-layered membrane is associated externally with an amorphous material. Two felt-like layers, separated by a cytoplasmic area, lie beneath the surface membrane. The surface membrane is unfolded to form intra-hypodermal crypts; these crypts are lined by a membrane which is extensively evaginated to form microvilli within the crypt. The crypts and labyrinths associated with them open at the surface by means of pores (Wright and Lumsden, 1970). B.

ADULT Acanthocephala

Hammond (1967) described the fine structure of the trunk and praesoma wall of Acanthocephalus ranae. It is similar in many ways to that of other adult acanthocephala described in the earlier review. The wall of both the trunk and of the praesoma are similar. There is an external membrane, a cuticle, a striped layer, a canal layer, central layers containing the so-called lacunar system (see Butterworth, 1969) and a folded basement membrane. The wall of the praesoma is much thinner than that of the trunk. Hammond (1968) also used the scanning electron microscope to study the body surface of A . ranae, Echinorhynchus truttae and Pomphorhynchus laevis. Pores were clearly seen on the trunk surface of A. ranae but were not seen in the other two species, possibly because they were masked with mucus. Most of the pores on the proboscides were associated with discrete masses of material which was apparently exuded from the pores. Wright and Lumsden (1969) redescribed the body wall of Moniliformis dubius and also the epicuticle (1968). The epicuticle is a filamentous coat external to the superficial membrane of the body wall and intimately associated with the structure. It is similar cytochemically and morphologically to a glycocalyx and, as such, is an integral part of the surface of the parasite. C.

FUNCTION

The epicuticle probably serves as a protective layer and possibly for the adsorption of enzymes for contact digestion. The pore-canal complex is probably a stable, structural specialization for increasing the free surface of the

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parasite and for chemical exchange with the environment (Wright and Lumsden, 1969). Rothman (1967) has localized alkaline and acid phosphatases on the membranes lining the canals of Moniliformis dubius and these may be involved in the uptake of materials by the worm.

IX. GENERAL SUMMARY In the earlier review I indicated that work on the ultrastructure of the Monogenea, the Temnocephalida, the larval stages of Platyhelminthes and freeliving nematodes would help to fill many gaps in our knowledge of the structure and origins of the outer covering of helminths. In this up-dated review much of the space has been devoted to work carried out on the Monogenea, the larval stages of Platyhelminthes, the larval stages of nematodes and moulting in nematodes, but work is still needed on the Temnocephalida, on more freeliving nematodes, on more Monogenea and Turbellaria and on the embryology and development of the outer covering of all of the Platyhelminthes. The description of the outer covering of an endoparasitic turbellarian has been of particular interest because although the epidermis is ciliated it is also covered with many long microvilli and the epidermis appears to become syncytial by the breakdown of the lateral membranes of the epidermal cells. On present evidence it would appear that the outer covering of the Monogenea may vary in structure. The epidermis of some monogeneans is apparently very similar to that of the Digenea in that it is a syncytial epidermis with cytoplasmic connections to nucleated cell-like bodies sunk in the parenchyma, whereas in others, notably Gyrodactylus, nuclei and sunken nucleated celllike bodies are not associated with the epidermis. In the one species which has been studied the original ciliated cells of the early embryo are replaced by other ciliated cells which arise in the parenchyma, as in the embryo of free-living turbellaria. The unciliated adult epidermis initially has superficial nuclei and appears under these ciliated cells. In the Digenea the change from miracidium to sporocyst also involves shedding of the ciliated epidermal cells and the formation of a syncytial epidermis from cells which lie below the muscles. The epidermis of the sporocyst is covered with cytoplasmic folds or microvilli and is usually in cytoplasmic continuity with nucleated cell-like bodies in the parenchyma, although in one example nuclei are present in the epidermis. The epidermis of the redia is similar in the few species which have been studied. The syncytial epidermis appears to have no cytoplasmic connection with cells in the parenchyma; nuclei have not been detected but mitochondria are present. The outer surface is thrown into folds or microvilli. There is still confusion about the origin of the outer layer of the cercaria. Some authors claim that the outer layer of the cercariae developing inside the redia is formed by cells of the redia and that once the germinal ball is a multicellular mass then this layer is shed. The layer which is to be the epidermis of the cercaria is formed from peripherally located cells of the germinal ball. Other authors state that the outermost layer of the cercaria within the redia

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is an embryonic epithelium, that this forms the epidermis of the cercaria and that it is shed when the cyst of the metacercaria is formed. Other authors claim that during cyst formation the epidermis is altered but not shed and that it becomes the epidermis of the metacercaria and then the adult. Whatever its origin, the epidermis of emerged cercariae is very similar in all species which have been examined. There is a syncytial epidermis, containing mitochondria but no nuclei, which is in cytoplasmic continuity with nucleated cell-like bodies in the parenchyma. There are variations in structure of the epidermis in different regions of the body, especially on the tail. Recent work on the epidermis of adult digeneans has been briefly summarized as it has confirmed descriptions of the epidermis of other species described in the earlier review. One important point which is emerging from this work is the fact that surface specializations of the epidermis do occur in different regions of the adult worm, especially in the strigeids. Recently it has been suggested that the Cestodaria are either monogeneans or that they occupy a phylogenetic position between the monogeneans and the cestodes. Ultrastructural work on one species has shown that the epidermis resembles that of cestodes more than that of monogeneans but this could be adaptation to the environment and does not invalidate the theory. The cytoplasmic epidermis bears numerous microvilli on its surface and is in cytoplasmic continuity with nucleated cell-like bodies in the parenchyma. The microvilli lack the dense spine-like tip which is so characteristic of the microvilli of adult cestodes. The development of the epidermis of adult cestodes still needs much work to clarify the situation, especially from the embryological point of view. The epidermis of adult cestodes has been confirmed as an outer cytoplasmic syncytial epidermis which is covered with microvilli bearing electron-dense spine-like tips, and in cytoplasmic continuity with nucleated cell-like bodies in the parenchyma. A characteristic feature of most of the parasitic Platyhelminthes, including many of the larval stages, is the presence of a syncytial epidermis which is in cytoplasmic continuity with nucleated cell-like bodies in the parenchyma, There is accumulating evidence that these sunken cells are not permanently in contact with the epidermis but that they migrate from within the parenchyma to make contact with the epidermis and then perhaps lose contact once their function at the epidermis is complete. The numbers associated with the epidermis could be related to the activity or degree of growth of the epidermis. If this is so then it could help to explain why these cells have not been found, or are only rarely found, associated with the epidermis of some species or stages in the life cycle. The cuticle of many different stages and species of nematode have now been examined with the electron microscope and a certain type of cuticle structure appears to be common to most larval nematodes and also to some adults. There is an outer layer which is similar to, and may be, a thick unit membrane; a cortical layer which is usually sub-divided; a striated layer; and a thin fibrillar (as distinct from a fibre) layer. The cuticle of adult nematodes appears to vary considerably from species

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to species and can usually be related to the nature of the environment. The most extreme cases are in some insect-parasitic nematodes where the cuticle is almost completely absent and the hypodermis has developed microvilli. Several examples of moulting in nematodes have been described and it would appear that moulting differs in different types of nematode and sometimes in different stages of the life cycle. Some species resorb much of the old cuticle whereas others discard it almost intact. It has been suggested that this may be related to the environment of the nematode. The body wall of some larval stages of two acanthocephalans has been described by means of electron microscopy and shown to be rather similar to that of the adult. More work has also been done on the body wall of adult acanthocephalans and has extended previous descriptions.

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Hammond, R. A. (1968). Observations on the body surface of someacanthocephalans. Nature, Lond. 218, 872-873. Hirumi, H., Chen, T. A., Lee, K. J. and Maramorosche, K. (1968). Ultrastructure of the feeding apparatus of the nematode Trichodorus christiei. J. ultrastr. Res. 24,434-453. Hockley, D. J. (1968). Scanning electron microscopy of Schistosoma mansoni cercariae. J. Parasit. 54, 1241-1243. Hockley, D. J. (1970a). The development of the tegument of Schistosoma mansoni. In Proc 2nd Int. Cong. Parasit. J. Parasit. 56, Section 2, 150-1 51. Hockley, D. J. (1970b). Ultrastructure of the outer membrane of Schistosoma mansoni. In Proc 2nd Int. Cong. Parasit. J. Parasit. 56, Section 2, 151. Howells, R. E. and Erasmus, D. A. (1969). Histochemical observations on the tegumentary epithelium and interproglottidal glands of Moniezia expansa. Parasitology 59,505-51 8. Ibrahim, I. K. A. (1967). Morphological differences between the cuticle of swarming and nonswarming Tylenchorhynchus martini. Proc. helminth. SOC. Wash. 34, 18-20. Ibrahim, I. K. A. and Hollis, J. P. (1967). Cuticle ultrastructure of the Meloidogyne hapla larva. Proc. helminth. SOC.Wash. 34, 137-1 39. Inatomi, S., Sakamoto, D. Itano, K. and Tanaka, H. (1963). [Studies on the submicroscopic structure of body surface of larval nematodes.] Jap. J. Parasit. 12, 16-39. Sakamoto, D., Itano, K., Suguri, S. and Ito, Y.(1968a). [The Inatomi, S.,Tongu, Y., ultrastructure of helminths. I. The body wall of Clonorchis sinensis (Cobbold, 1875) Looss, 1907.1Jap. J. Parasit. 17, 395-401. Inatomi, S., Tongu, Y.,Sakamoto, D., Suguri, S. and Itano, K. (1968b). [The ultrastructure of helminths. 2. The body wall of Metagonimus yokagawi takahashii Suzuki, 1930.1Jap. J. Parasit. 17,455-460. Inatomi, S . Tongu, Y.,Sakamoto, D., Suguri, S. and Itano, K. (1969). [The ultrastructure of helminths. 3. The body wall of Schistosoma japonicum.] Jap. J. Parasit. 18, 174-181. Inatomi, S., Sakumoto, D., Tongu, Y.,Suguri, S. and Itano, K. (1970). “Electron Micrograph of Helminth.” The 20th ann. Publ., Dept. of Parasitology, Okayama University Medical School, Okayana, Japan. Jackson, G. J. and Bradbury, P. C. (1970). Cuticular fine structure and molting of Neoaplectana glmeri (Nematoda), after prolonged contact with rat peritoneal exudate. J. Parasit. 56, 108-1 15. James, B. L., Bowers, E. A. and Richards, J. G. (1966). The ultrastructure of the daughter sporocyst of Cercaria bucephalopsis haimaena Lacaze-Duthiers, 1854 (Digenea: Bucephalidae) from the edible cockle, Cardum edule L. Parasitology 56,752-762. Jamuar, M. P. (1966). Electron microscope studies on the body wall of the nematode Nippostrongylusbrasiliensis.J. Parasit. 52,209-232. Jenkins, T. (1969). Electron microscope observation of the body wall of Trichuris suis, Schrank, 1788 (Nematoda: Trichuroidea). 1. The cuticle and bacillary band. Z. ParasitenKde 32, 374-387. Johnson, P. W., Van Gundy, S. D. and Thomson, W. W. (1970a). Cuticle ultrastructure of Hemicycliophora arenaria, Aphelenchus avenue, Hirschmaniella gracilis and Hirschmaniella belli. J. Nematol. 2, 42-58. Johnson, P. W., Van Gundy, S. D. andThomson, W. W. (1970b). Cuticle formation in Hemicycliophora arenaria, Aphelenchus avenue and Hirschmaniella gracilis. J. Nematol. 2, 59-79. 16

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Riding, I. L. (1970). Microvilli on the outside of a nematode. Nature, Lond. 226, 179-180. Rifkin, E. (1970).An ultrastructural study of the interaction between the sporocysts and the developing cercariae of Schistosoma mansoni. In Proc. 2nd Int. Cong. Parasit. J. Parasit. 56,Section 2,284. Rifkin, E., Cheng, T. C. and Hohl, H. R. (1970).The fine structure of the tegument of Tylocephalum metacestodes: with emphasis on a new type of microvilli. J. Morph. 130,ll-24. Roggen, D. R., Raski, D. J. and Jones, N. 0. (1967). Further electron microscopic observations of Xiphinema index. Nematologica 13,1-16. Rothman, A. H. (1967). Ultrastructural enzyme localization in the surface of Moniliformis dubius (Acanthocephala). Expl Parasit. 21,42-46. Sakamoto, T. and Sugimura, M. (1969). [Studies on echinococcosis. XXI. Electron microscopical observations on general structure of larval tissue of multilocular echinococcus.] Jap. J. Vet. Res. 17,67-80. Sakamoto, T. and Sugimura, M. (1970). [Studies on echinococcosis. XXIII. Electron microscopical observations on histogenesis of larval Echinococcus multilocularis.] Jap. J. vet. Res. 18,131-144. Samoiloff, M. R. and Pasternak, J. (1968). Nematode morphogenesis: fine structure of the cuticle of each stage of the nematode, Panagrellus silusiae (de Man 1913) Goodey 1945.Can. J. Zool. 46,1019-1022. Samoiloff, M. R. and Pasternak, J. (1969).Nematode morphogenesis: fine structure of the molting cycles in Panagrellus silusiae (de Man 1913)Goodey 1945. Can. J. ZOO^. 47,639-643. Schardein, J. L., Lucas, J. A. and Dickerson, C. W.(1968).Ultrastructural changes in Litomosoides carinii microfilariae in gerbils treated with diethylcarbamazine. J. Parasit. 54, 351-358. Silk, M. H., Spence, I. M. and Buch, B. (1970).Observations of Schistosoma mansoni blood flukes in the scanning electron microscope. S. Afr. J. med. Sci. 35, 23-29. Silk, M. H., Spence, I. M. and Gear, J. H. S. (1969). Ultrastructural studies of the blood fluke-Schistosoma mansoni. I. The integument. S. Afr. J. med. Sci. 34, 1-10. Skaer, R. J. (1965).The origin and continuous replacement of epidermal cells in the planarian Polycelis tenuis (Iijima). J. Embryol. exp. Morph. 13, 129-1 39. Slais, J. (1966).The importance of the bladder for the development of the cysticercus. Parasitology 56,707-713. Slais, J. (1970).The electron-microscopical characteristics of various components of the bladder wall of the cysticercus. In Proc. 2nd Int. Cong. Parasit. J. Parasit. 56,Section 2, 320-321. Smith, K. (1970).Electron-microscopical observations on the body wall of the third stage larva of Haemonchusplacei. Parasitology 60,411-416. Smith, J. H.,Reynolds, E. S. and von Lichtenberg, F. (1969). The integument of Schistosoma mansoni. Am. J. trop. Med. Hyg. 18,28-49. Smithers, S . R. and Terry, R. J. (1969).Immunity in schistosomiasis.Ann. N. Y. Acad. Sci. 160,826-840. Smithers, S . R., Terry, R. J. and Hockley, D. J. (1969). Host antigens in schistosomiasis. Proc. R. SOC.B 171,483-494. Southgate, V. R. (1970). Observations on the epidermis of the miracidium and on the formation of the tegument of the sporocyst of Fasciola hepatica. Parasitology 61,177-190.

THE S T R U C T U R E O F THE HELMINTH CUTICLE

379

Southgate, V. R. (1971). Observations on the fine structure of the cercaria of Notocotyliis attentiatus and formation of the cyst wall of the metacercaria. 2. Zellforsch. 120, 420449 Stockdale, P. H. G., Fernando, M. A. and Gilroy, J. (1970). Ultrastructural study of the teguminal sheaths of two metastrongyloid nematodes. Can. J. Zool. 48, 423425. Taylor, E. W. and Thomas, J. N. (1968). Membrane (contact) digestion in the three species of tapeworm Hymenolepis diminuta, Hymenolepis microstoma and Moniezia expansa. Parasitology 58, 535-546. Threadgold, L. T. (1967). Electron-microscope studies of Fasciola hepatica. 111. Further observations on the tegument and associated structures. Parasitology 57,633-637. Threadgold, L. T . (1968). The tegument and associated structures of Haplometra cylindracea. Parasitology 58, 1-7. Thust, R. (1966). Elektronenmikroskopische Untersuchungen uber den Bau des larvalen Integumentes und zur Hautungsmorphologie von Ascaris lumbricoides. Zool. Anz. 177,411-417. Timofiev, V. A. and Kuperman, B. I. (1967). [Ultrastructure of the outside layers of Triaenophorus nodulosus coracidia.] Parazitolgiya 1, 124-1 30. Timofiev, V. A. and Kuperman, B. I. (1968). [Ultrastructure of the cuticle and subcuticular layer in the procercoid, plerocercoid and adult of Triaenophorus nodulosus.]Parazitologiya 2,42-49. Tsubota, T. (1966). [Ultrastructure of Enterobius vermicularis. I. Cuticle.] Jap. J. Parasit. 15,58-63. Wajdi, N. (1966). Penetration by the miracidia of 5’.mansoni into the snail host. J. Helminth. 40,235-244. Wilson, R. A. (1969). Fine structure of the tegument of the miracidium of Fasciola hepatica L. J. Parasit. 55,1241 34. Wisse, E. and Daems, W. T. (1968). Electron microscopic observations on secondstage larvae of the potato root eelworm Heterodera rostochiensis. J. ultrastr. Res. 24, 210-231. Wright, K. A. (1968). The fine structure of the cuticle and interchordal hypodermis of the parasitic nematodes, Capillaria hepatica and Trichuris myocastoris. Can. J. 2001.46, 173-179. Wright, K. A. and Hope, W. D. (1968). Elaborations of the cuticle of Acanthonchus duplicatus Wieser, 1959 (Nematoda : Cyatholaimidae) as revealed by light and electron microscopy. Can.J. Zool. 46, 1005-101 1. Wright, R. D. and Lumsden, R. D. (1968). Ultrastructure and histochemical properties oftheacanthocephalanepicutic1e.J. Parasit. 54,1111-1 123. Wright, R. D. and Lumsden, R. D. (1969). Ultrastructure of the tegumentary porecanal system of the acanthocephalan Moniliformis dubius.J. Parasit. 55,993-1003. Wright, R. D. and Lumsden, R. D. (1970). The acanthor tegument of Moniliformis dubius. J. Parasit. 56, 727-735. Yuen, P. H. (1967). Electron microscopical studies on Ditylenchirs dipsaci (Kuhn). I. Stomata1 region. Can. J . Zool.45,1019-1033. Yuen, P. H. (1968). Electron microscopical studies on the anterior end ofPanagrelhs silusiae (Rhabditidae). Nematologica 14, 554-564.

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Author Index Numbers in italics refer to pages in the References at the end of each article

A Abasov, K. D., 299, 300, 306, 307, 308, 310 Abbate, E. A., 310 Abdallah, A,, 286, 317 Abdel-Malek, E. T., 168, 181, 219, 253, 254 Abdou, A. E. H., 302, 308,310 Abdullaev, A. M., 299, 310 Aboul-Eid, H . Z., 362, 372 Abramova, I . G., 306,307,308,333,337 Abuladze, K. I., 270, 271, 272, 273, 275, 284,310 Abunagimov, Kh. Z., 327 Acha, P. N., 303, 309,310 ACkov, M., 308, 330 Acosta-Matienzi, J., 201, 219, 220, 221, 238,262 Adamiya, G., 285,310 Adams, A. R. D., 293,310 Adams, J. E., 168,181,186 Adie, J. R., 3, 14, 17, 25 Adonajlo, A., 286, 288, 289, 300, 303, 308,310, 343 Aedtner, K., 305, 307, 308, 310 Agapova, A. I., 139, I45 Agarwal, S. M., 164, I81 Aguilar, F . J., 303, 309,310 Ahkami, S . , 290, 310 Ahrens, G., 305, 307, 308, 310 Aikawa, M., 32, 45 Akram, M., 309,321 &am, S., 309,321 AlagiC, D., 308, 310 Al-Allaf, G., 293, 335 Albis, F. S., 309, 334 Aldridge, F. P., 356, 372 d’Alessandro Bacigalupo, A., 273, 283, 284, 286,310,311 Alferova, M . V., 306,310 Ali, M.T., 309, 329 Ali, S. N., 32, 35, 36, 38, 44, 45 381

AIieva, S. I., 277, 286, 337 Allan, N., 33, 46 Allen, P. J., 213, 254 Allen, R. W., 305, 310, 311 Allison, A. C., 33, 45 Allison, L. N., 169, 172, 181 Allison, V . F., 203, 267 Alonso, M. T., 309, 311 Alterio, D. L., 293, 294, 311 Altmann, G., 277,311 Alvaro-Diaz Artilde, J., 303, 309, 311 Alworth, W . L.. 360. 376 Ameel, D. J., i63, 164, 165, 181, 183, 245,257 Amirov, R. O., 296,297,311 Anderson, F . M., 164, 177, 181 Anderson, G. A,, 162,181 Anderson, M. G., 164, 177, 181 Andrews, G. W. S., 277, 311 Andrews, W . H . H., 59, 69, 72, 74 Anello, G., 308, 319 Angel, L. M., 160, 168, 171, 181, 184, 185 Angus, M. G. N., 42,43,44,45 Anic, N., 308, 342 Anon, 311 Anschiitz, G., 17, 25 Anteson, R. K., 209, 210, 254 Antipin, D. N., 305, 311 Antoniewicz, K., 287, 314 Anya, A. O., 362,372 Araggo, H. deB., 1,3,5,7,9, 11, 12, 14, 17, 25, 26, 27 Araujo, T. L., 139, I45 Ardao, H., 285,311 Arean, V . M., 365, 373 Arfaa, F., 309,335 Anne, C., 276,311, 360,376 Armed Forces Institute of Pathology, 199,254 Amell, O., 285, 311 Artemov, N.M., 276, 311 Artikov, M. B., 287,311

382

AUTHOR INDEX

Ascenti, E., 308, 333 Asenjo, A., 273,311 Asher, R., 282, 311 Astakhova, 0. O., 306,325 Atias, A., 290, 311, 317 Atienza Fernandez, M., 311 Aubert, H., 136, 137, 140, 145 Audy, J. R., 192,205,214, 225, 262 Augustine, D. L., 245,256 Avakyan, D. M., 300,308,311 Avetisyan, S. F., 290, 293, 294,333 Aviado, D. M.,39, 45 Avlavidov, T., 308, 311 Ayala, S. C., 16, 17 B Babeau, P.,286,340 Bablet, J., 285, 316 Bachlechner, K., 308,311 Bacigalupo, J., 273, 288, 311 Backlund, H. O., 245,254 Baer, J., 155,156, 158,162,167,172,181 Baer, J. G., 78, 141, 145, 169, 185, 271, 275, 278, 322,331 Baer, K. E.V., 135, 136, 137, 140, 145 Bailinger, J., 294, 311 Bairamalibekova, R. T., 277, 286, 337 Baker, J. R., 5, 8, 12, 13, 14, 17, 18, 24, 26, 214,267 Bal, A. K., 354, 376 Bang, F. B., 207, 213, 254 Barbosa, F. S., 211, 219, 223, 254 Bard, J., 245, 263 Bareto, A. C., 219,223, 254 Barker, F. C., 139,145 Baron, P. J., 358, 372 Barrow, J. H. Jr., 245,254 Bartl, Z., 276,314 Basch, P. F., 192, 193, 194, 195, 198, 201,202, 203, 204, 205, 206, 207, 210, 211, 214, 225,226,227,234, 245,254, 255, 260,261, 262 Basnuevo, J. G., 287, 291,312,324 Bass, A. C., 42, 47 Batko, B., 277,312 Batsakis, J. G., 320 Baugh, S. C., 202,260 Bayer, F. A. H., 202,254 Baylis, H. A., 153, 157, 158, 181 Baz, I, I., 308, 331 Beamer, P. R., 320 Beams, H. W., 361,372

Bearup, A. J., 168,181 Beaver, P. C., 168, 169,181, 202,254 Beck, A. J., 192, 205,214, 225,262 Becker, C . D., 136, 144,148 Beckerdite, F. W. Jr., 203, 215, 267 BeganoviC, H. A., 308,310 Begiun, F., 359,372 Beier, A., 283, 284, 291, 292, 301, 308, 312 Bekhli, A. F., 290, 293, 324 Belopol'skaya, M. M.,172, 174, 181 Belton, C. M., 355, 372 Belyaev, A. E., 278, 283,312 Benassi, E., 289, 312 Benedict, E. G., 286, 312 Benesch, R., 35,45 Benesch, R. E., 35, 45 Benetazzo, B., 312 Btnex, J., 208, 245, 254, 257 Bennett, G. F., 6, 17 Bennett, H. J., 296, 330 Bennett, M. J., 164, 181 Bennett, T. P., 36,45 Berg, C. O., 245, 255, 260, 263 Bergner, J. F., 309, 312 Berrie, A. D., 246, 255 Bemos-Durran, L. A., 245, 260 Berry, L. R., 285,286,312 Berson, J. P., 3, 17 Bertrand, D., 291, 316 Bhabani, A. R., 61, 62, 63, 74 Bhaduri, N. V., 276,278, 302,314, 329 Bhatia, B. L., 2, 17 Biagi, F. F., 308, 315 Biche, Y., 302, 309, 312 Biguet, J., 289, 312 Billings, F. T., 66, 72 Bilqees, F. M., 358, 372 Bils, R. F., 162, 181, 354,372 Binckley, Ellen C., 7, 9, 10, 12, 20 Bioy, E., 326 Bird, A. F., 360, 364, 372 Bird, J., 360, 364, 372 Bird, R. G., 14, 18, 26 Bishop, H. W.,308,3I2 Bisset, K. A,, 208, 255 Black, D. A. K., 312 Blamoutier, P., 286, 312 Blamire, R. V., 308, 328 Blanchard, R., 312 Bloch, E. H., 68, 73

383

A U T H O R INDEX

Boch, J., 308, 312 Boev, S. N., 272,312 Bogitsh, B. J., 356, 372 Bogojavlenski, N. A., 287, 312 Bogoyavlenski, Y.K., 361, 373 Bojanowicz, K., 292, 312 BokoviC, T., 308, 343 Bonczak, J., 286, 300, 308, 310 Bonilla-Naar, A., 278, 312 Bonner, T. P., 362, 365, 373 Boray, J. C., 192, 193, 203, 220, 221, 245,255 Boreham, P. F. L., 62, 72 Botero, D. R., 293, 313 Bottom, F., 302, 309, 313 Boudenes, G., 292,331 Boveri, J. L., 285, 313 Bowers, E. A., 153, 154, 155, 156, 158, 159, 160, 162, 163, 173, 184, 354, 375 Bowman, I. B. R., 33, 36, 38,45 Box, Edith D., 2, 12, 13, 14, 17, 24, 26 Boyce, H. R., 205, 267 Brackett, S., 172, 176, 183, 192, 203, 210,256, 257 Bradbury, P. C., 360, 375 Brandes, 305, 343 Bras, de Sousa Loreto, 5, 14, 20, 24 Brant, P. C., 303, 304, 309, 3B, 315 Brlten, T., 358, 359, 373 Bratt, A. D., 245, 255 Braun, M., 78, 145 Bray, R. S., 2, 10, 12, 14, 15, 17, 18, 25, 26 Bresciani, J., 348, 373 Brewer, G. J., 42, 45 Brinkmann, A. Jr., 81, 107, 123, 131, 139, 145 Brocklesby, D. W., 281, 340 Brodsky, M., 302, 304, 305, 309, 327 Brooks, C. P., 223, 255 Brooks, W. M., 207,255 Brown, P. W., 327 Bruce, J. I., 193, 217, 255, 355, 373 Bruce, R. G., 361, 365, 373 Brumpt, E., 273, 275, 285, 313 Brumpt, V., 309,313 Briining, H., 286, 313 Bruzzoni, N. R., 335 Bryant, C., 33, 45 Brygoo, E. R., 278,313 Bubis, J. J., 277, 311 Buch, B., 355,378

Buchwalder, R., 301, 308, 321 Bueding, E., 289,291,336 Bugyaki, L., 306,313 Burch, J. B., 219, 255 Burckhardt, W., 284, 286, 313 Burmeister, H., 141, 145 Bums, Wrn. C., 176,181 Burrows, R. B., 274, 285, 286, 312, 313 Burt, D. R. R., 106, 128,145 Burton, P. R., 356, 373 Bustamente, E., 273, 311 Butler, J. M., 245, 255, 258 Butterworth, P. E., 369, 373 Buttner, A,, 168, 172, 174, 176, 182, 202,255 Buttner, D. W., 14, 18, 26 Bychowsky, B., 93, 127, 128, 136, 139, 145 Bychowsky, I., 93, 127, 128, 136, 139, 145 Byram 111, J., 326 Byrd, E. E., 162, 176,182 C Cable, R. M., 139, 150, 157, 158, 160, 161, 162, 163, 164, 165, 169, 172, 178, 182 Cameron, J., 302, 309, 319 Cameron, T. W. M., 155, 158, 167, 182 Campana-Rouget, Y.,162,182 Campbell, W. C., 282,313 Canhan, A. S., 298, 302, 309,313 Canning, E. U., 225, 245, 255 Cannon, P. R., 49, 72 Caponnetto, S., 308, 315 Capron, A., 278, 288, 289, 312, 313 Carini, A., 5, 18 Carman, J. A., 309, 315 Carmichael, J., 299, 313 Carney, D. M., 219, 263 Cartei, S., 286, 340 Cassorla, E., 284, 285, 326 Castel, P., 292, 321 Castellano, T., 273, 313 Castillo, Lindley E., 277, 313 Catala, L., 315 Cavier, R., 289, 291, 293, 313 Cenadella, R. J., 35, 36, 45 Chabaud, A. G., 162, 170,182 Chadwick, J. S., 213, 255 Chain, E., 49, 73

384

A U T H O R INDEX

Chandler, A. C., 313 Chapman, K . H., 313 Charles, G. H., 358, 359, 373 Chauhan, B. S., 139, 141, 145 Chechugo, I. S., 309,337 Chen, T . A., 362, 375 Cheng, T. C., 177, 182, 203, 207, 208, 213, 214, 223, 231, 255, 256, 358, 378 Chernin, E., 213, 238, 245, 256 Chi, L. W., 219, 256 Chin, T. H., 309, 314 Ching, H. L., 169, 182 Chiriboga, J., 245, 260 Cho, W. C., 39,45 Chodera, L., 287, 291, 292, 293, 314 Chongsuphajaisiddhi, T., 44, 47, 58, 59, 73, 75 Chowaniec, W., 21 1, 256 Chowdhury, A. B., 276, 278, 314 Christensen, A. M . , 158, 183 Christophers, S. R., 32, 45 Chu, K. Y., 219,256 Chubrik, G. K., 166, 183 Chularek, P., 299, 302, 309, 314 Chularerk, U., 299, 302, 309, 314 Churchwell, F. K., 276, 342 Chwirot, E., 283, 284, 285, 287, 291, 292, 293,314,332 Ciauri, G., 286, 314 Cigala, O., 328 Ciordia, H., 164, 183 Cironeau, I., 304, 308, 314 Clapham, P. A., 274,314 Clarenburg, A., 314 Clark, G. W., 15, 18, 25 Clark, H . C., 285, 314 Clegg, J. A., 357, 373 Clyde, D. F., 33, 45 Cmelik, S., 276, 314 Coan, C. C., 42,45 Coceani, C., 302, 314 Coelho, M. D. V., 21 9, 220, 256 Coelho, M. V., 211, 254 Colley, F. C., 360, 373 Collin, W. K., 203, 256, 357, 358, 373 Combnescu, N., 290, 331 Conrad, M. E., 67, 68, 73 Conroy, D. A., 315 Cook, R.T . , 32, 45 Cooper, B., 203, 267 Cooper, E. L., 207, 208, 259 Corradetti, A., 4, 12, 13, 18, 24, 26

del Corral, P., 309, 315 Correa, L. R., 218, 264 Correa, C., 6, 18, 25, 26 Corrba, Clovis, 21, 26, 27 Corso, P., 308, 315 Cort, W. W., 163, 164, 165, 172, 176, 183, 192, 203, 210, 245, 256, 257, 264 Cory, C. B., 18, 27 Cosgrove, G. E., 303, 309, 315 da Costa, A. S., 303, 304, 309, 313, 315 Coulson, F., 7, 8, 9, 10, 12, 18, 20, 26 Courmes, E., 245, 257 Cousi, D., 315 Cousineau, G. H., 354, 376 Cover, B., 32, 48 Cram, E. B., 218, 219. 257, 259 Cramer, J. D., 281, 289, 304, 305, 306, 315.316 Crandall, C. A., 365, 373 Crandall, R. B., 164, 165, 182,183 Crane, R. K., 315 Crewe, S. M., 297, 315 Crewe, W., 297, 315 Cridland, C. C., 219, 257 Crosby, W. H., 34,47 Cruickshank, I. A. M., 213, 257 Cunningham, J. T., 126, 137, 141, 145

D Dadlez, J., 292, 315 Daems, W. T., 360, 379 Damme, E., 329 Danilewsky, B., 1, 18 Dasgupta, B., 276, 278, 314 Da Silva, A. L., 309, 315 Da Silva, W . R. K., 295, 320 Daubney, R., 309,315 Davaine, C., 315 Davey, K . G., 365, 373, 376 Davey, T . H., 219,238, 259 Davidie, J. A., 245, 257 Davis, A. K., 42, 47 Dawes, B., 78, 139, 141, 145, 153, 183, 201, 220, 221, 257, 353, 374 Dayal, J., 139, 146 Dean, B. H., 296, 297, 308,320 DeBach, P., 200, 214, 244, 257, 258 De Beer, G . Sir, 172, 183 Deberdt, A,, 301, 307, 308, 320 Deberdt, P., 303, 308, 320 Deblock, S., 288, 302, 308, 316 Debrot, S.,315

385

AUTHOR I N D E X

De Carneri, I., 308, 315 Deegan, T., 44,46, 69, 72, 73, 74 De Freitas, 0 . T., 303, 309, 315 Delard, G., 303, 309, 315 Del Gesso, L., 310 Delon, J., 315 De Maria, M., 245, 264 Demian, E. S . , 245, 257 De Morales, D. S., 295, 320 De Moura, M. F., 245, 264 Denecke, K., 297, 315 Denev, D., 308, 315 Denison, J., 268 Dennis, L. H., 67, 68, 73 De Resende, P. R., 309, 315 De Rivas, D., 273, 294, 315 Derrier, E., 305, 315 Deschiens, R., 285, 288, 291, 316 Deschiens, R. E. A., 245, 257 Despeignes, J., 293, 319 Despommier, D. D., 362, 374 Desprks, P., 304, 305, 308, 316 Desser, S. S . , 13, 14, 19, 25, 26 Desowitz, R. S . , 50, 65, 73, 74 Devakul, K., 66, 67, 69, 73, 74 De hies, J., 301, 308, 316 Dewhirst, L. W., 281,282, 289, 304, 305, 306, 315,316 Dewitt, W. B., 219, 258 D’heureuse, R., 284, 286, 321 Dias, A., 5 , 14, 20, 24 Dias, J. C. P., 303, 309, 316 Diaz, L. M. T., 168, 186 Dick, T. A., 362, 364, 374 Dickermann, E. E., 121, 137, 138, 139, 141, 146, 164, 183 Dickerson, C. W., 362, 378 Di Conza, J. J., 238, 258 Diesfeld, H. J., 308, 316 Diesing, K. M., 136, 139, 146 Dike, S. C., 276, 326 Dinnik, J. A., 163, 164, 183, 201, 238, 258 Dinnik, N. N., 163, 164, 183, 201, 238, 258 Dissanaike, A. S., 12, 13, 18, 24, 245, 258,316 Ditzel, J., 294, 316 Dixon, H. B. F., 273, 302, 316 Dixon, K. E., 171, 183, 354, 355, 356, 3 74 Dobrovolny, C. G., 174, 177, 183

Dobrovolski, A. A., 354, 374 Dobrowolska, H., 288, 316 Doby, J. M., 288, 302, 308, 316 Doby-Dubois, M., 288, 302, 308, 316 Dodion, L., 294, 316 Dollfus, R. Ph., 78, 91, 103, 107, 110, 122, 123, 129, 136, 139, 141, 146, 158, 163, 166, 176, 183, 245, 258 Dolman, C. E., 304, 316 Donckaster, R., 277, 290, 294, 317 Donges, J., 163, 166, 172, 183, 213, 258 Donoso, F., 277, 290, 317 Dorken, H., 276, 289, 321, 334 Doroshchak, 0 . F., 293,317 Doutt, R. L., 200, 258 Douvres, F. W., 295, 326 Duarte, G. G., 303, 309, 331 Dubey, J. P., 14, 18 Dubois, G., 163, 172, 183, 184 Dubos, R. J., 278, 317 Dubreuilh, W., 273, 329 Dufek, M., 290, 291, 292, 293, 317 Dujardin, F., 136, 140, 146 Dunachie, J. R., 14, 19 Dunlop, S. G., 296, 342 Dunn, M. J., 41, 42, 45 Durie, P. H., 163, 164, 184 Dusanic, D. G., 208, 258 Duthie, E. S., 49, 73 Duthy, B. L., 296, 317 Diakulla, N., 280, 306, 342 Dzhabriev, N. I., 327 Dzieciolowski, Z . , 283, 317 Diinleski, B., 303, 308, 317

E Eckmann, F., 139,146 Edington, G. H., 67, 73 Edney, J. M., 163, 184 Eichelberger, J. N., 67, 68, 73 Eisa, A. M., 302, 309, 317 El-AM, A., 302, 304, 305, 308,309,317 El-Cindy, M. El. S., 204, 211, 258 Eliot, T. S . , 52, 68, 73 El-Mawla, N. G., 286, 317 Elmossalami, E. S., 302. 304, 305, 308, 309,317,325 Elsdon-Dew, D., 334 Elsdon-Dew, R., 274,289,302, 309,317, 329,334 El Sherif, A. F., 310 Emsbo, P., 308, 317

386

AUTHOR INDEX

Endrejat, E., 309,317 Enequist, N., 301, 307, 308, 317 Enigk, K., 317 Erasmus, D. A., 356, 359, 374, 375 Ernster, L., 43, 48 Ershov, V. S., 305, 311 Esch, G. W., 358, 359, 377 Etges, F. J., 202, 258, 362, 365, 373 Evans, E. A. Jr., 38,48 Evranova, V. G., 282,317 Ewers, W. H., 204, 258 Eymmer, H. J., 305, 308, 321

F Fahmy, M. A. M., 302, 308,317 Faiguenbaum, J., 290, 317, 330 Fantham, H. B., 5,18, 24 Fao, Who, Oie, 300,318 Faraco, B. F. C., 295, 320 Farchmin, G., 301, 308, 321 Faulk, W. P., 208, 209, 222, 226, 258, 259 Fauran, P., 245, 257 Faust, E. C., 82, 110, 113, 121, 136, 139, 141, 146, 158,184, 201, 220, 221,238, 258 Fehkr, J., 300, 305, 308, 339 Felsani, F., 309, 317 Feng, S. Y.,208, 258 Ferguson, F. F., 245,255, 258,259,260, 263,264, 265,266 Fernandez, A. F., 277, 342 Fernando, M. A., 12,18,24, 361, 379 Ferracani, R. S., 285, 317 Fetterman, L. E., 289, 318 Fewster, G. E., 303, 304, 305, 309, 318 Fielding, C. M., 42, 46 Figgat, W. B., 296, 330 Files, V. S., 218, 219, 257, 259 Filipov, V. V., 306, 323 Filipovic, B., 286, 319 Findlay, G. M., 50, 73 Finnegan, C. V., 359, 377 Fischer, C., 318 Fishthal, J. H., 170, 184 Fisher, R. C., 200, 214, 259 Fitzgerald, F., 202, 204, 206, 227, 262 Fitzsimmons, W. M., 309, 318 Fletcher, K. A,, 32, 33, 34, 35, 36, 38, 39, 42, 43, 44,45, 46, 47, 48 Florey, H. W., 68, 73 Flosi, A. Z., 66, 73

Foes, 0. M., 309,326 Folkers, K., 39, 47 Fontan, C., 273, 318 Fonteneau, M., 308, 318 Foote, B. A., 245,255, 259 Fourrier, A,, 286, 340 da Franca, 0. H., 284,285, 286, 318 Franchini, G., 8, 14, 15, 18, 24, 25, 28 Franssen, J. G., 305, 318 Fredrickson, D. S., 43,46 Frenkel, J. K., 14, 18 Friedrich, J., 281, 303, 307, 308, 318 Friendlander, Y., 33, 46 Frolova, A. A., 277, 318 Froltsova, A. E., 331 Froyd, G., 280,281,282, 295, 300, 302, 306, 308, 309,318 Fudenberg, H. H., 226, 259 Fuentes, P. B., 318 Fuhrmann, O., 141, I46 Fullard, J., 38, 39, 41, 46, 48 Fulton, J. D., 32, 45, 46 Furst, O., 294, 319 G Gaehtgens, W., 288, 319 Gailiunas, P., 319 Galil, N., 286, 317 Gallo, C., 308, 319 Gancarz, Z., 288, 289, 300, 303, 308, 310,343 Gangolli, D. A,, 319 Garaguso, P., 288, 319 Garin, J. P., 293, 319 Garnham, P. C. C., 2, 9, 10, 11, 14, 18, 25, 26, 27, 295, 319 Gasparov, A., 286, 319 GavranoviC, I., 308, 310 Gazzola, E., 308, 315 Gear, J. H. S., 355, 378 Gebauer, O., 319 Geckler, R. P., 245, 259 Geiger, S., 211, 218, 260 Geiman, W. M., 39,47 Gelber, A,, 290, 331 Gemmell, M. A., 282, 319 Gentner, H. W., 136, 146 George, J. N., 34,47 Gerwel, Cz., 292, 315 Ghenis, D. E., 300, 308, 319 Ghenov, G. M., 308,319 Gherman, I., 290, 319

AUTHOR

Gibson, M., 245, 259 Gibson, T. E., 305, 319 Gilles, H. M., 33, 46, 66, 67, 73, 74 Gilroy, J., 361, 379 Ginetzinskaya, T. A., 142,146, 153, 154, 155, 156, 157, 158, 167, 170, 184, 354, 374 Ginsberg, A., 302, 307, 309, 319 Ginzel, E., 305, 308, 319 Giroud, P., 322 Gladkikh, V. F., 320 Goddard, W. B., 302, 309, 319 Godoy, M., 294, 31 7 Gogotishvili, T. G., 285, 310 Golden, A., 42, 47 Goldsmid, J. M., 273, 309, 320, 340 Gombarros Alvarez, E., 285, 320 Gomez, Garcia, V., 311 Gonnert, R., 279, 289, 291, 320 Gonzales Castro, J., 311 Gonzalez, G., 326 Goodchild, C. G., 172, 184 Goodwin, L. G., 62, 66, 73 Gordon, R. M., 219, 238, 259 Gordon, R. S., 43,46 Gotzsche, N. O., 297, 308, 320 Goulart, E. G., 295, 320 Gould, S . E., 320 Gouveia, A. L., 303, 309, 313 Graack, B., 179, 187 Grabda-Kazubska, B., 177, 184 Graber, M., 272, 293, 302,306,309,320, 343 Graham, C. F., 320 Grailet, L., 293, 325 Grant, P. R., 33, 35, 36, 38, 45, 46 Granville, A., 301, 303, 307, 308, 320 Gras, G., 292, 321 Green, C. D., 364, 374 Greenberg, A. E., 296, 297, 308,320 Grkgoire, C., 301, 303, 307, 308, 320 Gregor, O., 308,333 Grieve, J. M., 302, 309, 319 Griffiths, R. B., 296, 297, 301, 304, 308, 320,337 Grimaldi, E., 325 Grisse, A., de, 364, 374 Grott, J. W., 293, 322 Grujic, I., 301, 308, 320 Grumbach, R., 308, 320 Guarniera, D., 308, 333 Guildal, J. A., 297, 320

INDEX

387

Guilhon, J., 293, 320 Guiver, K., 296, 337 Guilisano, G., 308, 315 Gunther, B., 360, 374 Gunther, H., 320 Gupta, B. L., 352, 374 H Hadjian, A., 290, 310 Hajduk, F., 305, 308,321 Hajj, S. N., 286, 336 Haleem, M. A,, 309,321 Halterman, L. G., 297, 336 Halton, D. W., 170, 184, 351, 352, 355, 377 Hamerton, A. E., 18, 25 Hamilton, J. B., 289, 321 Hammond, R. A,, 369, 374, 375 Hanel, L., 294, 321 HanSen, E. L., 238, 258 Harant, H., 292, 321 Hardwick, E. F., 308, 321 Hargreaves, T., 294, 321 Harinasuta, T., 67, 69, 73 Harris, P. J., 355, 372 Hart, J. W., 18, 26 Hatton, C. J., 289, 321 Heath, D. D., 279, 338 Hegner, R., 18, 26 Heikinheimo, E., 294, 321 Hein, B., 324 Helander, E. V., 321 Hellmayr, C. E., 18, 27 Hendrickse, R. G., 33, 46 Hendrix, S . S., 83, 90, 136, 137, I46 Hennemann, H. H., 284,286,321 Hennessy, E., 334 Herman; C. M., 2, 9, 15, 19, 20, 22, 24, 25, 26, 27 Herman, R., 33,46 Herman, Y. F., 33, 46 Hermos, J. A., 301, 307, 309, 336 Hermus, G., 307, 308, 321 Hewitt, R., 7, 19, 24, 25 Heyneman, D., 153, 155, 156, 157, 158, 159, 163, 166, 167, 168, 173, 184, 192, 194, 195, 198, 201, 202, 203, 204, 205, 206, 207, 208, 209, 213, 214, 221, 222, 225,226,227,231, 234,236,244,246, 254, 258, 259, 260,261, 262 Hickman, V. V., 176, 184 Hiepe, T., 301, 308,321

388

AUTHOR INDEX

Hildemann, W. H., 207, 208, 259 Hinerman, D. L., 320 Hinz, E., 309, 321 Hirte, W. E., 291, 321 Hirumi, H., 362, 375 Hkun-Saw-Lwin, 302, 309, 340 Hoare, C. A., 3, 14, 15, 19, 27 Hockley, D. J., 354, 355, 357, 375, 378 Hoeppli, R., 269, 302, 321 Hoffman, J. F., 42, 46 Hoffman, M. A,, 193, 194, 201, 202, 227, 261 Hoffman, W. A., 201, 220, 238, 258 Hofstra, K., 308, 321 Hohl, H. R., 358, 378 Holliman, R. B., 178, 184, 245, 259 Hollis, J. P., 360, 375 Holz, J., 280, 321 Homewood, C. A., 38, 39, 40, 46 Honer, M. R., 301, 308,321 Hope, W. D., 362, 364, 368,379 Hopkins, S. H., 136, 137, 139, 146, ISI Hornbostel, H., 276, 277, 282, 283, 284, 285, 286, 287, 289, 299,321, 324 Hornell, J., 128, 137, 150 Hovorka, J., 308,321 Howells, R. E., 38, 39, 40, 41, 46, 48, 359, 275 Hsieh, H. C., 288, 302, 309, 322 Hsu, H. F., 219, 260 Hsu, S. Y., 219, 260 Huang, S. W., 270, 272, 298, 302, 309, 322 Huff, C. G., 15, 19, 27, 208, 260 Huhtala, A., 308, 322 Huizinga, H. W., 361, 376 Hulland, T. J., 280, 337 Humes, A. G., 164, 181 Humphreys, R. M., 219, 260 Hurst, A., 284, 322 Hussey, K. L., 155, 184, 245, 257, 288, 322 Hutchison, W. M., 14, 19 Hyman, L. H., 141, 146, 155, 156, 166, 184 I

Ibrahim, I. K. A., 360, 361, 375 Ilin, M. M., 308, 328 Tnatomi, S.,355, 356, 359, 360, 362, 375 Index Catalogue, 136, 146 Inmin, M. M., 67, 68, 73

Interdepartmental Committee on Nutrition, 302, 309, 322 Irvine. C., 322 Isseroff, H., 164, 182 Itakura, T., 293, 329 .-. Itano, K., 355, 356, 359, 360, 362, 375 Ito, Y., 356. 375 IAailova-Guseinova, R. A., 289, 322 J Jackson, G. J., 360, 375 Jacob, H., 302, 307, 309, 341 Jadin, J., 322 Jagerskiold, L. A., 128, 139, 147 James, B. L., 153, 154, 155, 156, 158, 159, 160, 162, 163, 165, 173, 174, 184, 354, 375 James, C., 193, 268 Jamieson, B. G. M., 157, 162, 176, 184 Jamuar, M. P., 360, 375 JaniEek, J., 305, 332 Janicki, C., 155, 184 Jaroonvesema, N., 67, 73 Jarpa, A., 290, 317 Jarrell, J. J., 35, 36, 45 Jarrett, W. F. H., 306, 340, 341 Jarzebski, Z., 300, 308, 310 Jenkins, T., 361, 375 Jeong, K. H., 208, 244, 259 Jepsen, A., 295,296, 308, 322 Jeyarasasingam, U., 195, 198, 201, 202, 207, 231, 236, 259, 260 Jobin, W. R., 245, 260 Johnson, P. T., 245, 260 Johnson, P. W., 360, 364, 375 Johnston, M. R. L., 14, 21 Johnston, T. H., 168, 171, 184, 185 Jones, A. W., 278,322,325 Jones, M. F., 218, 219, 257 Jones, N. O., 362, 364, 378 Jones, Virginia, P., 7, 9, 10, 12, 20 Jopling, W. H., 277, 322 Joshi, V. G., 285, 294, 302, 309, 337 Joyeux, Ch., 78, 141, 145, 155, 156, 158, 162, 167, 169, 172, 181, 185, 271, 322 Junod, C., 277, 294, 322 K Kaan, J. D., 285, 322 Kabler, P., 296, 322 Kacka, I., 277, 312

A U T H O R INDEX

Kagan, I. G., 176, 185, 211, 218, 260, 339 Kajima, M., 362, 374 Kalawski, K., 294, 299, 300, 308, 322 Kalb, J. C., 293, 319 Kaliszewicz, S., 293, 322 Kalivoda, R., 290, 291, 292, 293, 317 Kamalova, A. G., 278, 288, 322, 333 Kaminski, A., 292, 315 Kamo, H., 293,329 Kampfe, 365, 376 Kampfe, L., 360, 374 Kan, S. P., 365, 373, 376 Kanakakorn, K., 69, 73 KanneworfT, B., 158, 183 Kantor, S., 2, 20 Kapustin, V. T., 277, 333 Karle, E., 213, 258 Karlinska, A., 286, 324 Karnaukhov, V. K., 285, 290, 323 Katz, N., 193, 264 Kaufman, R. S., 284, 323 Kawanishi, K., 323 Kearney, A., 304, 323 Kebbouche, L., 308, 331 Keeling, J. E., 289, 290, 291, 292, 323 Keller, H., 305, 323 Kelly, H. M., 136, 137, 139, 144, 147 Kemp, W. M., 355,376 Kendall, S. B., 220, 223, 260 Kent, N., 323 Kermack, W. O., 33, 36, 38, 45 Kerr, K. B., 323 Khalil, H. M., 290, 323 Khalil, L. F., 220, 245, 260 Khan, R. A., 13, 14, 19, 25, 26 Kiefer, E. D., 294, 335 Kikuth, W., 7, 19, 26 Kilejian, A., 223, 266 Killby, V. A. A., 32, 46 Killick-Kendrick, R., 5, 8, 12, 13, 17, 24 Kim, C. H., 277, 302, 309, 325 King, A. C., 323 Kinoti, G., 217, 219, 221, 260 Kitel, V. S., 293, 317 Kleibel, A., 305, 307, 308, 323 Klink, G. E., 274,313 Klusaka, J., 285,323 Knight, W. B., 245, 260 Knisely, M. H., 52, 68, 73 Knorr, R., 323 Knotz, I., 323

389

Knutson, L. V., 245, 255, 260, 266 Kofoid, C. A., 136, 139, 147 Kohl-Yakimoff, N., 5, 22 K0oe, M., 348, 373 Kolbe, F., 298, 323 Komiya, Y., 172,185, 302, 309, 329 Kondo, K., 293, 330 Kondracka, H., 300, 308, 310 Kong-Kim-Chuon, 309,313 Kornberg, H. L., 37, 46 Koskowski, W., 323 Kosminkov, N. E., 306,323 Kostenko, D., 285, 323 Kotova, 0. M., 308, 328 Koudela, K., 281, 300, 304, 305, 308, 323, 324 Kouri, P., 287, 324 Kovalev, N. E., 294, 299, 300, 307, 308, 324 Kovchazov, G., 308, 311 Kozek, W. J., 361, 365, 376 Kramm, D., 304, 308,333 Kreier, J. P., 42, 47 Krotov, A. I., 272, 290, 292, 293, 324 Krueger, 307, 324 Krull, W. H., 169, 176, 185 Krupa, P. L., 354, 376 Kubicki, S., 286, 324 Kuhls, R., 291, 324 Kumzicki, R., 283,317 Kuntz, R. E., 155,185, 219,260 Kuperman, B. I., 358, 359,379 Kupey, P., 301, 307, 308, 324 Kuimicki, R., 274, 324 Kwo, E. H., 194, 225, 227, 246, 248, 249, 260, 262, 264 L Labbk, A., 1, 11, 12, 19 Ladda, R. L., 38, 46 Lagane, D. M. M., 285,325 Lagasse, A., 364, 374 Lainson, E., 10, 19, 26 Lainson,R.,2, 5,8,9, 10, 11, 12, 13, 14, 17, 19, 24, 25 Laird, Elizabeth, 19, 27 Laird, M., 2, 6, 9, 11, 12, 16, 17, 19, 25, 27, 30 Lal, M. B., 202, 260 Lamina, J., 324 Lamy, L., 208, 254 Landi, A., 305, 325

390

AUTHOR INDEX

Landis, E. M., 69, 73 Lang, B. Z., 177,185 Langer, B. W. Jr., 33, 46 Langer, J., 288, 325 Lapierre, J., 286, 325 Larrougy, G., 274,325 Larsh, J. E., 358, 359, 361, 376, 377 LaRue, G. R., 163, 165, 169, 173, 176, 185 Lassance, M., 293, 325 Laveran, A., 1, 2, 3, 5 , 11, 14, 19, 23, 25 Lawrence, J., 19, 26 Laws, G. F., 295,325 Lazzaro, D. A., 304,325 Lebedeva, M. N., 320 Lebour, M. V., 163,185 Lee, D. L., 347, 355, 360, 362, 365, 368, 376 Lee, H. G., 213, 262 Lee, H. H. K., 278,325 Lee, K. J., 362, 375 Lee, K. T., 277, 302, 309, 325 Lee, M. A., 18, 25 Lee, M. Y.,277, 302, 309, 325 Le Gac, P., 291, 325 Leidholdt, H. G., 329 Leidy, J., 136, 147 Leigh, W. H., 177,185 Leikina, E. S., 281, 282, 306, 325 Leinati, L., 325 Leithead, C. S., 66, 74 Lengy, J., 201, 217, 219, 220, 221, 261 Lennon, E. A,, 308,333 Lepes, T., 301, 308, 325 Lerche, M., 305, 308, 325 Le Row, P. L., 272, 301, 308, 325 Lescure, 0. L., 289, 336 Letulle, M., 285, 325 Leuckart, K. G. F. R., 153, 155, 156, 159,185 Leuckart, R., 141, 147 Le Viguelloux, J., 309, 335 Levine, N. D., 2, 12, 20, 26, 250, 261 Levitanskaya, P. B., 1, 10, 22, 24, 26 Lewert, R. M., 208, 258 Lewitzki, R. G., 287,312 Ley, J., de, 276, 325 Le Zotte, L. A,, 161, 163, 174, 185 Liard, F., 245,260 Lichtenberg, F., von, 355, 356, 357, 378 Lie, K. J., 168, 185, 192, 193, 194, 195, 198, 199, 201, 202, 203, 204, 205, 206,

207, 214, 215, 220, 221, 222, 223, 225, 226, 227, 231, 234, 237, 238, 245, 246, 248, 249, 254, 260, 261, 262, 264 Lieb, D. E., 18, 25 Liebman, H., 296, 297, 325 Liegeois, F., 305, 325 Lidvre, H., 304, 326 Lim, H. K., 195,198,201,202,207,208, 209, 213, 215, 219, 222, 223, 231, 236, 244,258,259, 260,262 Lim, H. W., 142,147 Lima, D. F., 309,326 Lindner, R., 33, 46 Lindsay, G. K., 219, 255 Link, A,, 284, 285,326 Linstow, O., 136, 147 Linton, E., 137, 139, 141, 147 Lipscomb, F. M., 273, 302, 316 Little, C., 352, 374 Little, W., 32, 45 Llewellyn, J., 155,158, 170,186,357,376 Lloyd, E. L., 326 Lo, C. T., 219, 262 Lockhart, H. B., 285, 326 Loeper, M., 284,326 Logachev, E. D., 276,326, 356,376 Logan, C. J. H., 285,286,326 Logan, J. S., 301, 303, 304, 307, 308,326 Loos-Frank, B., 176,186 Looss, A., 103, 107, 139, 147, 170, 186 Lopez Ortiz, R., 303, 309, 326 Lopukhina, N. G., 307,333 Lucas, J. A., 362,378 Lucena, D., 15, 20, 24, 25, 26, 27 Lucena, D. T., 2, 6,20 Lucian, O., 290, 331 Lucker, J. T., 295, 296,326,341 Ludvik, J., 14, 20 Lumme, R., 326 Lumsden, R. D., 276,326,359,360,369, 370, 376, 379 Lunan, K. D., 39,47 Luque, F., 273, 313 Lure, R. N., 276,311 Lutfy, R. G., 245, 257 Lutyfiski, R., 308, 326 Luzzato, L., 34, 46 Lyons,K. M., 349,351,352,357,376,377 M McAnnally, R. D., 245, 262 MacCallum, G. A., 139,147

A U T H O R INDEX

MacCallum, W. G., 139, 147 McCarty, J. E., 355, 373 McCleery, E. F., 308, 328 McClelland, W. F. J., 211, 263 Macfie, J. W. S., 298, 327 Macdonald, J. D., 137, 147 Macheoboeuf, M., 323 Machnicka-Roguska, B., 276, 288, 289, 326,327 Maciel, G. A., 305, 327 Maciel, J., 5, 18 McIntosh, A., 280, 307, 328 McIntyre, W. I. M., 306, 341 McKee, R. W., 35,47 Mackerras, I. M., 8,12, 13,20,24,26,27 Mackerras, M. Josephine, 8, 12, 13, 20, 24, 26, 27 Mackie, A., 295, 327 McKinnon, J. A,, 302, 309,327,328 McLeod, J. A., 270,342 McManus, D., 298, 309,328 McMullen, D. B., 176,186, 192,203,257 MacNeal, W. J., 3, 21, 24, 25, 26 McQuay, R. M. Jr., 218, 219, 263 Maegraith, B. G., 33, 39, 42, 43, 44, 45, 46,47,48,50,51, 52,56,58, 59,60,61, 62, 63, 65, 66, 67, 68, 69, 70, 72, 72, 73, 74, 75 Magath, T. B., 327 Magdiev, R. R., 300, 306, 307, 308, 327 Mahfouz, M., 323 Makhmudova, S. A., 289, 327 Maldonado, J. F., 201, 219, 220, 221, 238,262 Malheiro, D. M., 305, 327 Malko, A. T., 335 Mamedov, A. A., 308,327 Manceaux, L., 5, 20 Maneely, R. B., 279,338 Mann, E., 309,327 Mann, G. V., 302, 309,334 Mann, I., 309, 327 Mansour, N., 198, 201, 231, 260 Mansour, N. S., 15, 20 Manter, H. W., 107, 108, 121, 122, 128, 134, 139,147, 176, 178, 186 Manwell, R. D., 7, 8, 9, 10, 12, 13, 20, 26, 27 Mao, C. P., 238, 264 Maples, W. P., 162, 182 Maplestone, P. A., 278, 327 Maramorosche, K., 362, 375

39 I

Marazza, V., 305, 325, 327 Markaryants, L. A., 327 Markkanen, T., 327 Marrenghi, O., 308, 327 Marsboom, R., 302, 304, 305, 309, 327 Marsden, K. H., 301, 308, 328 Martikyan, E. S., 300, 308, 328 Martin, G. A., 297, 336 Martin, G. N., 276, 342 Martin, G. W., 177, 186 Martin, J. H., 358, 359, 361, 376, 377 Martin, W. E., 162, 168, 169, 174, 178, 181, 186, 192, 203, 215, 245, 262, 354, 372 Martinez, M., 309, 343 Marullaz, M., 1, 2, 3, 5,9, 11, 19,20, 25, 26, 27 Marx, G. W., 309, 328 Marzano, F., 309, 315 Marzullo, F., 276, 328 Masdaki, S., 309, 328 Masellis, G. de, 308, 328 Mashanski, U. F., 354, 374 Maskrey, P., 43, 47, 48 Massoud, J., 213, 219, 256, 262 Mastrandrea, G., 286, 314, 328 Mathias, P., 168, 186 Matikashvili, T. S., 308, 340 Matricon-Gondran, M., 354, 377 Matsubayashi, H., 302, 309, 329 Matsuno, K., 293, 330 Matta, A., 213, 262 Mattes, D., 220, 221, 245, 262 Matsubayashi, H., 329 Mattes, D., 307, 328 Mattila, M., 289, 291, 292, 328 Mazzotti, L., 277, 279, 283, 284, 287, 288,328 Mecham, J., 245,259 Meggitt, F. J., 273, 328 Mehra, H. R., 165,186 Meister, G., 279, 320 Meleney, H. E., 201, 219, 221, 258, 263 de Mello, F., 2, 5, 14, 20, 24 Melton, Marjorie L., 14, 21 Menefee, M. G., 362, 365, 373 Mengert, H., 245, 263 Menschel, E., 296, 328 Mercado, T. I,, 44,47, 276, 342 Mercer, E. H., 171, 183, 354, 356, 374 Merdivenchi, A., 214, 328 Merkushev, A. V., 308,328

392

AUTHOR INDEX

Merle, A., 300, 308, 328 Memll, J. M., 302, 309, 334 Metge, R., 245, 257 Metlitskii, L. V., 213, 263 Michelson, E. H., 128, 136, 140, 147, 208,220, 245, 256,263 Mielke, D., 301, 303, 308, 328 Migasena, P., 59, 60, 65, 74 Mijatovic, I., 308, 328 Mikhailyan, E. A., 290, 293, 294, 333 Milhade, J., 309, 335 Miller, D., 280, 297, 307, 309, 328, 329 Miller, J., 35, 36, 38, 39, 47 Miller, N. L., 14, 18 Mills, R. R., 326 Milward de Andrade, R. W., 219, 263 Mine, N., 5, 20, 26 Miretski, 0. Y., 278, 329 Mitchell, J. R., 302, 309, 329 Mitra, S.K., 309, 329 Miyakoda, J., 293, 329 Mohammed, A. H . H., 10, 15,20, 25 Moldenschardt, H., 343 Mollaret, C., 329 Molnir, L., 300, 305, 308, 339 Monisov, A. A., 278, 283, 287, 293, 312, 329 Monroe, L. S.,289, 329 Monticelli, F. S., 93, 123, 136, 139, 141, 147, 148 Monzini, A., 305, 325 Moore, D. V., 219, 245, 263 Moore, G. A., 38, 39, 48 Moos, W., 285,323 Moose, J. W., 218, 219, 263 Morales, I., 294, 317 Moreno, A. G., 305,327 Morishita, K., 302, 309, 329 Moriya, K., 82, 137, 148 Moriyama, S.,329 Moroha, R., 5, 14, 20, 24 Morris, G. P., 351, 352, 355, 359, 377 Morris, N., 289, 329 Morseth, D. J., 278, 329, 358, 359, 361, 377 Mosina, S. K., 282, 306, 317, 329 Moskvin, S. N., 281, 282, 306, 325, 338 Mossmer, A., 285,329 Motulsky, A. G., 33, 47 Moulder, J. W., 35, 36, 38, 47, 48 Muazzam, M. G., 309, 329 Mudrow, Lily, 7 , 19, 26

Mukerji, A. K., 302, 309, 329 Mukhin, V. N., 289, 329 Mukhtari, L., 308, 331 Mukvoz, L. G., 308,329 Miiller, K . H., 287, 305, 308, 329 Miiller, K. O., 213, 263 Miiller, R., 321 Mulligan, W., 306, 340, 341 Mustafa, A. A., 302, 309, 317 Mustakillio, K. K., 326, 335 Mustakallio, K . M., 289, 292, 329 Mvogo, L., 245, 263 N Nabias, B. de, 273, 329 Nadzhafov, I. G., 298, 300, 307, 308,330 Nagahana, M., 293, 330 Nagarajan, K., 37, 39, 47 Nagaty, H. F., 299, 330 Nahhas, F. M., 162, 178, 182 Najarian, H. H., 83, 103, 121, 136, 137, 140,148, 168,186 Naquira, F., 330 Nasir, P., 168, 186, 204, 263 Naumov, 273, 343 ' Naumova, R. P., 330 Nauwerck, C., 285, 286, 330 NeEev, T., 303, 308, 317, 330 Neff, S. E., 245, 263 Neghme, A., 292, 330 Nkgre, A., 285,330 Negrete, M. J., 318 Negus, M. R. S., 203, 264 Neiva, A., 6, 14, 20, 24 Nelson, G. S.,271, 272, 298, 330 Nelson, P., 12, 18, 24 NenadiC, M. B., 301, 308, 330 Nevenitch, V., 308, 338 Newton, W. L., 193, 218, 219, 222,264, 296, 330 Nickerson, W. S., 81, 83,90, 93,99, 102, 103, 107, 111, 113, 126, 137, 139, 148 Nicolle, C., 5, 20 Nieland, M. L., 357, 358, 377 Niezbekov, K., 293, 329 Nikolic, P., 308, 342 Nikulshina, 0. A., 308, 328 Niles, W. J., 12, 18, 24 Niiio, F . L., 273,285, 303, 309, 330 Nitsche, O., 6, 20, 24, 26

AUTHOR INDEX

Nitzulescu, V., 290, 331 Noda, K., 163, I86 Nolf, L. O., 210, 256, 264 Noller, W., 3, 5, 6, 8, 12, 20, 24, 26, 27 Nor El Din, G., 308, 331 Norton, R. A., 289, 329 Norval, J., 301, 308, 337 Nosslin, B., 294, 331 Notteghem, M. J., 289, 293, 313 Notter, A., 292, 331 Novy, F. G., 3, 21, 24, 25, 26 Nowak, S., 285, 323 du Noyer, M. R., 275, 278, 331 Nyberg, W., 276, 331 Nylen, M. U., 276, 342 0

Oaks, J. A., 276, 326, 360,376 Ockert, G., 301, 308, 331 O’Connor, N., 277, 331 Odening, K., 163, 166, 168, 177, 178, 186,187 Odhner, T., 90, 121, 139, 141, 148 Oelkers, H. A., 294, 331 Ogden, C. G., 364, 377 Ogilvie, A. C., 277, 311 Ogston, D., 33, 36, 38, 45 ohman, C., 356, 377 Ohnesorge, G., 294, 331 Okpala, L., 309, 331 Okura, T., 293, 343 Oleck, H. G., 274,333 Oleinikov, S. V., 287, 331 Olivier, L., 171, 172, 183, 187, 210, 238, 256, 264 Oliveira Lecuona, M., de, 302, 309, 331 Olivier-Gonzalez, J., 245, 255, 259, 264 Olsen, 0. W., 219, 267 Olsson, P., 139, 148 Onabanjo, A. O., 61, 62, 63, 65, 66, 68, 74, 75 Orduna Prieto, C., 308, 331 Orecchia, P., 308, 331 Orgaz, J., 273, 313 Orr, T. S. C., 358, 359, 373 Orzet-Fichtel, A., 331 Osborn, H. L., 83, 90, 93, 99, 103, 113, 121, 136, 137, 138, 140, 141, I48 Osche, G., 141, 148 Osmanov, S. O., 139, 148 Ostertag, V., 332 Overdulve, J. P., 14, 21

393

Overman, R. R., 41, 42, 47 Owen, Ch. A. Jr., 276, 336 Ow-Yang, C. K., 194, 204, 220, 221, 225, 227, 246, 248, 249, 260, 261, 262, 264 Ozeretskovskaya, N. N., 331 Ozeretskovskaya, 0. L., 213, 263 P Paggi, L., 308, 331 Palmer, J. R., 245, 259, 260, 266 Palombi, A., 177, 187 Pampiglione, S., 308, 331 Pan, C. T., 199, 202, 211, 215, 223, 238, 244,264 Panetta, J. C., 305, 327 Pantaleon, J., 304, 340 Paoliello, J. C., 303, 309, 331 Papasarathorn, T., 299, 302, 309, 314, 331 Paperna, I., 203, 264 Paraense, W. L., 218, 264 Pardi, M. C., 303, 309, 331 Park, C. T., 277, 302, 309, 325 Parnell, I. W., 295, 327 Parsons, S., 139, 145 van Parys, O., 302, 304, 305, 309, 327 Pasternak, J., 360, 364, 378 Pauley, G. B., 136, 144, 148 Pavanand, K., 65, 73 Pavlov, P., 307, 308, 332 Pavlovskii, E. N., 139, 148 Pawel, O., 305, 332 Pawlowski, Z., 291, 292, 293, 314 Pawlowski, 2. S., 277, 283, 284, 285, 289, 290, 291, 292, 293, 294, 299, 300, 301, 308, 322, 332 Pearson, J. C., 160, 161, 164, 166, 170, 177, 178, 187 Peaston, H., 219, 238, 259 Peatt, E. S. W., 302, 309, 332 Peel, C., 282, 306, 332 Peeters, E., 293, 325 Pellegrini, D., 308, 332 Pellegrino, A., 308, 332 Pellegrino, J., 193, 245, 264 Pemberton, C. E., 205, 264 Penfold, H. B., 277, 278, 281, 282, 283, 284, 295, 296, 303, 304, 306, 332 Penfold, W. J., 277, 278, 281, 283, 295, 296, 303, 304, 306, 332 Penna, B., 6, 14, 20, 24

394

AUTHOR INDEX

Pennisi, L., 308, 333 Penson, D., 302, 309,341 Perera, D. R., 290, 333 Pkref-Moreira, L., 274, 285, 311, 339 Perez Moreno, B., 285, 333 Perlstein, J. M., 245, 256 Persiani, G., 305, 325, 327 PessBa, S. B., 21, 26, 27, 303, 309, 333 Pester, F. R. N., 271, 272, 298, 330 Peters, J. L., 5 , 21, 27 Peters, W., 31, 38, 39, 40, 41, 46, 47;48 Petkov, A., 301, 308, 333 Petrosyan, N. A., 290, 293, 294, 333 Petrova, T. A., 297, 339 Petru, M., 288, 308, 333 Pezenburg, E., 274, 280, 321,333 Pezzlo, F., 355, 373 Pham-Ngoc-Thach, 333 Phillips, M., 277, 281, 283, 295, 296, 304,332 Phisphumividhi, P., 33, 46 Piqtkowska, W., 308, 333 Pietrowa, R., 292, 312 Pigulevskii, S. V., 155, 157, 187 Pipkin, A. C., 288, 333 Pirkl, J., 305, 333 Pistor, W. J., 281, 282, 306, 316 Pittaluga, J. Z., 333 Planeta-Malecka, I., 285, 323 Plaschke, W., 304, 308, 333 Plimmer, H. G., 5, 21, 24, 26 Podyalpolskaya, V. P., 277, 287, 288, 333 Poinar, G. O., 208, 264 Pokier, J., 139, 148 Pokier, M., 333 Poletaeva, 0. G., 281, 282, 306, 325 Pollack, S., 34, 47 Popov, N. P., 139,148 Popov, V. F., 307,333 Popovici, V., 304, 308, 314 Porter, A., 265 Poll, M. C., 334 Pouplard, L., 301, 307, 308, 320 Powell, E. C., 176, 188 Powell, N. T., 213, 214, 265 Powell, S. J., 334 Praderi, L. A., 285,311 Prankerd, T. A. J., 39, 47 Pratt, H. S., 141, 149 Pratt, I., 162, 176, 181 Prchal, C. J., 307, 309, 339

Prkvot, G., 168, 186 Prkvbt, R., 276, 289, 334 Price, C. E., 141, 149 Price, D., 208, 209, 222, 258 Price, D. L., 302, 309, 334 Price, E. W., 272, 334 Price, H. F., 170,187 Priestly, H., 301, 308, 334 Primio, R. di, 6, 15, 21, 24, 25, 26 Proctor, E. M., 274, 317, 329 Proctor, R. M., 289,334 Profk, 296,334 Prokopenko, L. I., 290, 293, 300, 306, 307, 308, 324, 333,334 Przyjalkowski, Z., 334 Pugachevskaya, E. F., 308, 334 Pugh, M. H., 276,342 Pujatti, D., 334 Pullin, R., 268 Purnell, R. E., 211, 219, 265 Pylko, 0. O., 276, 334 Pytel, A. Y., 334 R Rabin, H., 208, 265 Race, G. J., 358, 359, 361, 376, 377 Radke, M. G., 193, 217, 255,265 Raffaele, G., 11, 21, 25 Rai, S. L., 82, 107, 108, 113, 120, 121, 122, 127, 135, 136, 137, 139, 140, 141, 149, 162, 187 Ramsdell, S. G., 288, 334 Randriamalala, J. Ch., 278, 313 Rankin, J. S., 177, 187 Rankin, J. S. Jr., 160, 187 Rao, M. P. C., 221, 265 Rasameeprabha, K., 299, 302, 309, 314 Raschke, H., 301, 308, 334 Raski D. J., 362, 364, 378 Rausch, R., 174, 187 Rausch, R. L., 139, 149 Rawat, P., 139, 149 Ray, A. P., 44,47, 59, 70, 75 Ray, H. N., 276, 278,314 Read, C. P., 274,276,311, 334 Reddy, S., 33, 34, 46 Reed, R. E., 282, 306,316 Rees, G., 285, 287, 334, 354, 355, 356, 377 Refuerzo, P. G., 309, 334 Reichenow, E., 9, 11, 21, 25 Reid, H. A., 67, 73

395

AUTHOR INDEX

Reid, W. M., 279, 334 Reinecke, R. K., 341 Reisinger, F., 179, 187 Renaudet, R., 288, 316 Renesch, B., 142, 149 Repciuc, E., 273, 339 Reuter, F., 308, 334 Reynolds, E. S., 355, 356, 357, 378 Reznik, G. K., 356, 377 Ribeiro, P. de Assis, 303, 309, 334 Ricci, M., 308, 334 Rich, A. B., 297, 336 Richard, A., 285, 334 Richards, C. S., 218, 219, 245, 265 Richards, J. G., 354, 375 Richards, W. H. G., 62, 66, 73, 75 Richardson, T., 282, 313 Rickman, R., 271, 272, 298,330 Riding, I. L., 364, 368, 378 Riflcin, E., 208, 256, 355, 358, 378 Riggin, G. T., 169,187 Rijpstra, A. C., 279, 287, 335 Riley, M. V., 44, 46, 70, 75 Ritchie, L. S., 245, 260, 265 Rivero, E., 274, 335 Rivoalen, A., 309, 335 Rizk, E., 288, 333 Robbins, C. L., 199, 265 Robb-Smith, A. H. T., 284, 322 Roberts, C. J., 309, 335 Robert, J., 292, 331 Robson, E. M., 265 Robtser, A. N., 335 Rocha, U. F., 303, 309,331 Rock, R. C., 32, 45 Rodrigues Solis, L., 335 Rodriguez, L., 277, 283, 284, 328 Rodriguez Gonzalez, M., 334 Roels, 0. A., 302, 309, 334 Rogers, W. P., 214, 265 Roggen, D. R., 362, 364, 378 Rohde, K., 79, 80, 81, 82, 83, 84, 85, 90, 91, 93, 94, 95,96, 97, 98, 99, 100, 102, 103, 104, 105, 106, 108, 109, 110, 111, 112, 113, 114, 117, 118, 120, 121, 124, 125, 126, 130, 131, 132, 133, 134, 135, 138, 139, 140, 141, 142, 143, 149,150 Rohringer, R., 213, 265 Roiter, M., 309, 335 Rollier, R., 285, 286, 315, 335 Roman, E., 288, 335 Romand, A., 291,316

Romanenko, N. A., 335 RosB, F., 278, 288, 289, 312, 313 Rosen, S. W., 294, 335 Rosenbusch, F., 8, 21, 26 Rosler, 0 . A., 294, 335 Rosset, R., 304, 340 Rossi, A. A., 335 Roth, H., 295, 296, 308, 322 Rothman, A. H., 370, 378 Rothschild, M., 172, 179, 187, 215, 265 Round, M. C., 280, 282, 297, 298, 318, 335 Rousselot, R., 9, 10, 12, 21, 25, 26 Ruiz, J. M., 220, 245, 265 Ruiz-Tiben, E., 245, 266 Rumbold, D. W., 139, 150 Ruosch, W., 304, 305, 308, 316 Rusak, L. V., 289, 292, 324,335 Rybaltovsky, 0. V., 294, 335 Rybicka, K., 278, 335 Rydzewski, A., 277, 308, 332 Ryerson, D. L., 22, 24 Ryley, J. F., 35, 46

S de Sa, B., 5 , 14, 20, 24 Saalbreiter, R., 305, 308, 321 Sabbaghian, H., 219, 256, 309, 335 Sachs, R., 335 Safarov, G. I., 287, 311 Saikkonen, J., 289, 292, 329, 335 Saint-Guillain, M., 220, 266 Saito, M., 293, 343 Sakamoto, D., 355, 356, 359, 360, 362, 375 Sakamoto, T., 358, 378 Salamov, D. A., 296, 297, 311 Salem, H. H., 293,335 Salemme, M. A., 312 Salt, G., 200, 208, 213, 214, 244, 266 Salyaeva, V. A,, 305,311 Samborski, D. J., 213, 265 Samoiloff, M. R., 360, 364, 378 Sandars, D. F., 335 Sankale, M., 309, 335 Saoud, M. F. A., 219,266 Sardou, R., 274, 325 Sargent, J. R., 35, 46 Sarkisyan, V. A., 290, 293, 294, 333 Sasanov, A. M., 220,266 Saugrain, J.. 336 Savchenko, L. P., 336

396

AUTHOR INDEX

Saxe, L. H., 35, 36,45 Saz, H. J., 289, 291, 336 Scanga, M., 4, 12, 13, 18, 24, 26 Scarza, J. V., 168, 186 Schacher, J. F., 286,336 Schaller, G., 245, 266 Schanabel, R., 343 Schardein, J. L., 276, 336, 362, 378 Scheibel, L. W., 35, 36, 38, 39, 47, 289, 291, 336 Schell, S. C., 157, 162, 181, 187 Schlachter, H., 308, 336 Schmid, G., 305,336 Schmid, M., 308, 336 Schmidt, K., 14, 21 Schneider, H. H., 336 Schneider, I. S., 305, 327 Schneider, J., 293, 336 Schnell, J. V., 39, 47 Schoen, R., 336 Scholtyseck, E., 14, 21 Schoon, J. G., 336 Schoop, G., 306,336 Schuffner, W., 288,336 Schultz, M. G., 290, 297, 301, 307, 309, 333, 336 Schulze, U., 308, 336 Schumbert, R., 336 Schwabe, C. W., 223,266,299,304,307, 336 Schwartz, M., 294, 316 Scott, D. B., 276, 342 Scudamose, H. H., 276, 336 Seaton, D. R., 293, 310, 336 Seed, T. M., 42, 47 SBnaud, J., 14, 21 Seguin, F., 294,311 Seiler, H. E., 301, 308, 337 Sekhon, S. S., 361, 372 Sellers, T. F., 339 Seo, B. S., 302, 309, 337 Sergiev, P. G., 306, 308, 337 Sewell, R. B. S., 156, 159, 164, 177, 188 Shabelnik, V. I., 309, 337 Shafei, A. Z., 293, 337 Shah, P. M., 285,294, 302, 309,337 Shahin, H., 286 337 Shakhsuvarli, M,. A., 277, 286, 337 Sharma, G. K., 59, 70, 75 Sharp, N. C. C., 306, 341 Sheffield, H. G., 14, 21 Shekhovtsov, V. S., 308, 337

Sheldon, J. J., 304, 305, 316 Sherman, I. W., 37, 39, 47, 48 Sherwood Jones, E., 69, 72, 74 Shipley, A. E., 128, 137, 150 Shircore, T. O., 297, 337 Short, R. B., 83, 90, 136, 137, 146, 176, 188

Shortridge, E. H., 303, 309, 337 Shulman, E. S., 306, 307, 308, 333, 337 Sibileva, L. M., 331 Siddiqi, A. H., 139, 150 Siddiqui, E. H., 280, 337 Siddiqui, W. A., 39, 47 sijakov, I., 303, 308, 317 Siim, J. C., 14, 19 Silk, M. H., 355, 378 Sillman, E. I., 162, 170, 188 Silverman, P. H., 32, 46, 278, 279, 280, 295, 296, 297, 301, 304, 307, 308, 337, 338 Simer, P. H., 139, 150 Simitch, T., 308, 338 Simmonds, F. J., 205, 266 Simmons, J. E. Jr., 274, 276, 334 Simonescu, O., 290, 331 Simonffy, Z., 300, 305, 308,339 Simpson, E. R., 168, 185 Singh, R. N., 172, 188 Sinha, B. B., 139, 150 Sinitsin, D., 155, 156, 157, 158, 169, 188 Sinitzin, D. F., 136, 150 Sinnecker, H., 296, 297, 308, 338 Siu, P. M. L., 37, 47 Skaer, R. J., 352, 378 Skelton, F. S., 39, 47 Skirrow, M. B., 44,47, 58, 59, 75 Skrjabin, K. I., 78, 141, 150 Skvortsov, A. A., 338 slais, J., 278,280,281,338, 358, 359, 378 Smircic, P., 286, 319 Smit, A. M., 279,287,335 Smith, D. H., 38, 48 Smith, J. H., 355, 356, 357, 378 Smith, K., 360, 378 Smith, K. J. H., 33, 45 Smithers, S. R., 357, 373, 378 Smyth, J. D., 158, 170, 172, 188, 274, 279, 282, 338 Snigirevskaya, E. S., 14, 21 Snyder, R. W., 203, 256 Sogandares-Bernal, F., 139, 150, 172, 188

397

A U T H O R INDEX

Sokolovskaya, 0. M., 281,282,288,306, 325,338 Solarino, A., 308, 315 Soliman, K . N., 302, 309, 317 Someren, V. D., van, 296, 317 Sommer, S. C., 164, 165, 189 Sonsino, P., 136, 150 Soulie, P., 326 Soulsby, E. J . L., 281, 298, 306, 319, 338, 361, 377 Southgate, V. R., 221, 266, 352, 353, 356, 378, 379 Southwell, T., 271, 338 Speck, J . F., 38, 48 Spector, W. G., 65, 75 Spence, I. M., 355, 378 Spooner, D. F., 32, 46 Sprengers, R., 301, 307, 308, 320 Sprent, J . F . A., 295, 338 Sprinz, H., 32, 45 Squadrini, F., 276, 328 Ssinitzin, D. Th. von, 177, I88 Stafford, J., 83, 90, 91, 93, 103, 108, 136, 137, 144, 150 Standen, 0. D., 219,266, 289, 291, 292, 338 Starkoff, O., 274,338 Stauber, L. A., 21, 24, 208, 266 Stauber, Mabel F., 21, 24 Stebhens, W . E., 14, 21 Steele, J . H., 301, 307, 309, 336 Steenstrup, J . J . Sm., 153, 188 Steigler, 301, 308 Steinberg, D., 128, 136, 137, 138, I50 Stephens, J. M., 208, 266 Stephenson, J . W., 245,266 Steppe, W., 308, 339 Steward, J . S., 289, 339 Stieda, A., 285, 286, 339 Stirewalt, M . A., 170, 188, 219, 266 Stockdale, P. H . G., 361, 379 Stoll, N. R., 303, 308, 339 Stossich, M., 139, I50 Stoye, M., 317 Stratman-Thomas, W . K., 52, 73 Strikovsky, T. L., 277, 339 Stromberg, P. C., 136, 150 Stromskaya, T. F., 290, 323 Strout, R. G., 14, 21 Strufe, R., 279, 320 Stunkard, H. W., 93, 103, 136, 139, 141, 151, 155, 156, 157, 158, 159, 164, 167,

176, 178,188, 202, 219, 266, 267 Stuparic, D., 308, 342 Sudds, R. H . Jr., 222, 230, 267 Sugimura, M . , 358, 378 Suguri, S., 355, 356, 359, 360, 362, 375 Summa, H., 308, 339 Sundby, R. A., 200, 214,244, 257 Sunkes, E. J., 339 Sussman, O., 307, 309, 339 Suvorov, V. Y., 293, 295, 296, 339 Swales, W. E., 223, 267 Swartzwelder, J . C., 283, 339 Sweetman, H. L., 244, 267 Swellengrebel, N. H., 279, 287, 288, 335,336, 339 Swierstra, D., 339 Swiezawska, E., 293, 322,324 Swinehart, B., 15,18, 25 Sycevskaja, V. L., 297,339 Syogaki, K., 82,151 Szelenyi, L., 300, 305, 308, 339 Szidat, L., 162, 168, 170, 188 Sztrom, Z. K., 277, 339 Szyfres, B., 339 T Tabo, R., 309,320 Taddia, L., 21, 25 Tadros, G., 310 Takacs, J., 300, 305, 308, 339 Takki, S., 289, 291, 292, 294, 328, 339 Talavera, J., 339 Talice, R. V., 274, 285, 311, 339 Talyzin, F . F., 286, 339 Tanaka, H., 360, 375 Tanasescu, I., 273, 339 Tandon, R. S., 137, 140, 151 Tang,C.C., 121, 139, 141, 146, 158, 184 Taparelli, F., 276, 328 Tarnaala, K., 308, 339 Tarpila, S., 294, 339 Taylor, A. E. R., 214, 267 Taylor, D. C., 272, 282, 339 Taylor, E. W., 360, 379 Telkka, A., 326 Tella, A., 61, 62, 63, 74, 75 Terhorst, H., 305, 340 Thakur, A. S., 208, 256 Ter-Karapetiants, N. N., 340 Terry, R. J., 357, 373, 378 Theakston, R. D. G., 34, 38, 39, 43,48

398

A U T H O R INDEX

Thienpont, D., 302, 309, 312 Thieulin, G., 304, 340 Thillet, C. J., 219, 263 Thiodet, J., 286, 340 Thomas, H., 279,320 Thomas, J. D., 176,188 Thomas, J. N., 360, 379 Thome, M., 302, 306, 309,320 Thompson, Jr., J. H., 276, 336 Thomson, W. W., 360, 364, 375 Thornton, H., 302, 309, 340 Thorp, W. T. S., 308, 340 Threadgold, L. T., 355, 356, 360, 376, 377,379 Thurnham, D. I., 43,48 Thust, R., 361, 365, 379 Timberlake, P. EI., 214, 267 Timofiev, V. A., 358, 359, 379 Timon-David, J., 164, 166, 169, 177, 185,188,189 Ting, I. P., 37, 47, 48 Todd, J. L., 14, 15, 21 Todorov, R., 287,301,307,308,333,340 Tongu, Y., 355, 356, 359, 360, 362, 375 Topuriya, I. I., 308, 340 Totterman, G., 326, 340 Trager, W., 36, 45, 48 Tran van Ky, P., 289,312 Trautman, R. J., 282, 306, 316 Trawinski, A., 308, 340 Trevino, A., 277, 283, 284, 328 Tripp, M. R., 207, 208,267 Tronchetti, F., 286, 340 Tsubota, T., 362, 379 Tu, M., 302, 309,340 Turner, P. P., 293, 340 Tustin, R. C., 281, 341

U.S. Department of Agriculture, 78,151 Utter, M. F., 37, 48

V Valtonen, E. J., 294, 339 Valverde, A., 341 Van Beneden, P. J., 180, 189 Van Cleave, H.-J., 136, 138, 140, 151 Van den Heever, L. W., 281, 302, 309, 341 Van der Plank, J. E., 213, 267 Van Der Woude, A., 163, 164, 165,183, 189 Van Gils, J. H. J., 301, 305, 308, 341 Van Grunderbeeck, R., 302, 309, 341 Van Gundy, S. D., 360, 364, 375 Van Keulen, A., 301, 308, 341 Van Steenburgh, W. E., 205, 267 Varges, W., 304, 305,341 Vasilkova, Z. G., 296, 297, 341 Vasina, S. G., 1, 10, 22, 24, 26 Vegors, H. H., 341 Vercruysse, R., 276, 325 Verdiev, G. Y., 286, 341 Vernberg, F. J., 203, 215, 267 Vernberg, W. B., 203, 215, 267 Verster, A., 270, 271, 272, 274, 275, 278, 302, 309, 341 Versyck, M., 302, 307, 309, 341 Vieira, C. B., 277, 341 Viles, J. M., 326 Viljoen, N. F., 304,341 Villalobos, P. R., 318 Villanyi, J., 301, 307, 308, 320 Vincent, G., 293, 319 Voeltzkow, A., 90, 93, 103, 107, 108, 120, 121, 122, 127, 128, 134, 135, 136, 137, 139, 140, 151 U Voge, M., 203, 259, 279, 280, 341 Ubelaker, J. E., 203, 219, 267 Vogel, H., 274, 341 Ubieto, A., 309, 343 Vogelsang, E. G., 277, 309,314, 342 Vojtgchovskk, M., 288, 308, 333 Uegaki, J., 21, 24, 25, 26 Ulivelli, A., 292, 340 Voller, A., 33, 45 Ullyett, G. C., 205, 267 von Brand, T., 44, 47, 214, 267, 274, Ulmer, M. J., 164, 165, 169, 171, 189 276, 342 Umathevy, T., 168, 185, 192, 194, 195, Von Harnack, G. A., 342 201, 204, 225, 231, 246, 259, 261, 262 Vujic, B., 308, 342 Upton, A. C., 285,286,340 W Ureche, L., 308, 340 Urquhart, G. M., 281, 295, 298, 300, Wachowska, M., 342 Wagner, E. D., 219, 256 302, 305, 306, 308, 309,340, 341 Usanga, E. A., 34,46 Waitz, J. A,, 276, 336

A U T H O R INDEX

Wajdi, N., 211, 220, 245, 267, 353, 379 Waksman, S. A,, 200, 213, 214, 268 Walde, A. W., 323 Walzberg, U., 6, 21, 24, 26 Wang, W. L., 296, 342 Ward, H. B., 139, 151 Ward, R. A., 33, 46 Wardle, R. A., 270,342 Warhurst, D. C., 38, 39, 40, 46 Warnecke, W., 284, 342 Warren, K. S., 21 1, 213, 245, 259, 268 Wasowa, D., 308, 326 Watkins, S., 213, 262 Webbe, G., 193,213, 262,268,279,320, 342 Wegmann, T., 342 Weinbach, E. C., 358, 377 Weinberg, M., 288, 342 Weinland, F., 270, 342 Weinmann, C. J., 282, 342 Weisberger, A. S., 213, 268 Wen, Y. F., 309, 342 Wenyon, C. E. M., 59, 72, 74 Wenyon, C. M., 2, 13, 22, 24 Wesenberg-Lund, C., 201, 202, 204, 268 Western, K. A., 290, 333 Wetmore, Psyche W., 22, 24, 26 Wharton, G. W., 137, 139,151 Wigand, R., 284, 342 Wikerhauser, T., 280, 306, 342 Willard, H. F., 205, 264 Williams, C. O., 107, 108, 128, 129, 136, 137, 138, 140, 141,151 Williams, I. C., 265 Williams, J. E., 218, 219, 263 Williamson, J., 32, 48 Wilmot, A. J., 334 Wilson, R. A., 220, 268, 352, 353, 379 Winfield, G. F., 209, 268 Wisse, E., 360, 379 Witenberg, G. G., 302, 306, 309, 342 Winterhalter, M., 303, 308, 342 Wohnus, J. F., 22, 24 Wojciechowska, L., 342 Wojtak, S., 331 Wolbach, S. B., 14, 15, 21 Wolbert, B., 213, 258 Wold, N., 219, 256

399

Wolff, F., 343 Wolfson, Fruma, 7, 8, 12, 18, 22, 23, 26 Wood, Fae D., 22, 24 Wood, H. G., 37, 48 Wood, R. K. S., 213, 268 Wood, S. F., 9, 15, 22, 24, 25, 26, 27 Woodruff, A. W., 277,322 Wootton,D. M., 107,108,113,126,135, 137,151, 156, 176, 189 Work, K., 14, 19 Wostmann, B. S., 362, 374 Wright, C. A., 156, 178, 179, 189, 214, 215,246,268 Wright, K. A., 361, 362, 364, 368, 379 Wright, R. D., 369, 370, 379 Wu, L. S., 302, 309, 343 Wyant, K. D., 278, 322,325 Y Yajima, Y., 355, 373 Yakimoff, W. L., 5, 22 Yamaguti, S., 78, 127, 139, 141, 151, 176,189 Yaqub, M., 309,343 Yarwood, C. E., 213, 268 Yates, D. B., 66, 75 Yokogawa, M., 293,343 Yoshida, Y., 293, 330 Yoshimura, H., 293, 343 Youssef, L. B., 304, 305, 309, 317 Yuen, P. H., 360, 379 Z Zacharias, O., 83, 113, 151 Zapart, W., 288, 289,343 Zapatel, J., 309, 343 Zasukhin, D. N., 1, 10, 22, 24, 26 ZelejkoviC, S., 308, 343 Zembruski, K., 300, 308, 343 Zetterstrom, R., 43, 48 Zimmer, E., 317 Zingano, A. G., 309,326 Zischke, J. A., 201, 268 Zolotarev, N. A., 305, 311 hkovic, M., 280, 306, 342 Zunker, M., 305, 343 Zwierz, C., 326, 327, 343

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Subject Index Acanthatrium, 172 oregonense, cuticle structure, 355 Acanthocephala, cuticle structure and function, 369-370 Acanthocephalus ranae, cuticle structure, 367 Acanthocotyle elegans cuticle function, 352 structure, 350, 351 Acanthoncus duplicatus cuticle function, 368 structure, 362 Acanthoparyphium spinulosum, I 68 cuticle structure, 354 Acridines in taeniasis therapy, 292 Adeleine haemogregarines, 2-3, 14-1 6 Allocreadium alloneotenicum, life cycle 176 Alaria, life cycle, 177-8 Amidostomum anseris, cuticIe structure, 361 Amphibdella flavolineata, cuticle str ucture, 349, 351 Ancylostoma caninum, cuticle structure, 360 duodenale, cuticle structure, 360 Anomotaenia constricta, cuticle structure, 359 Aphelenchus avenae cuticle structure, 360 moulting, 364 Ascaris lumbricoides cuticle structure, 361 diagnosis, 289 moulting, 365 Ascarops strongylina, cuticle structure, 361 Aspiculuris tetrptera, cuticle structure, 362 Aspidocotyle miitabile, 78 Aspidocotylus cochleariformis, 78 401

Aspidocaster . protonephridial system, 83 antipai, localization in mollusc, I36 conchicola adult genital system, 90, 91, 93 marginal bodies, 103 protonephridial system, 82 biology infectivity of larvae, 136 infectivity to vertebrate host. 138 invasion into mollusc, 135 life span, 134 localization in mollusc, 135 in vertebrate host, 139 sexual maturation in mollusc, 137, 138 survival of adult outside host, 140 development egg, cleavage and larval development, 120 hatching, 121, 122 parasitic stage, 126-1 3 1 larvae, free infectivity, 135 life span, 134 structure general morphology, 107, 108 protonephridial system, 1 13 tegument and ciliary tufts, I10 indica adult, protonephridial system, 82 biology localization in mollusc, 136 sexual maturation in mollusc, 137 survival of adult outside host, 140 development egg, cleavage and larval development, 120 hatching, 121, 122 parasitic stage, 127 larvae, free

402

S U B J E C T INDEX

Aspidogaster indica (contd.)

general morphology, 107, 108 protonephridial system, 113 limacoides

genital system, 93 localization in vertebrate host, 139 parasitic stage, 127, 128 Aspidogastrea adult digestive tract, 81-82 genital system, 90-93 marginal bodies, 103-107 nervous system, 82-90 protonephridial system, 82-90 sense receptors, 99-103 tegument, 79-81 ventral disc, 103 biology infectivity to vertebrate host, 138139 invasion into mollusc, 135 larvae, free infectivity, 135 life span and behaviour, 134-135 localization in mollusc, 135-137 in vertebrate host, 139 sexual maturation in mollusc, 137138 survival of adult outside host, 140 development allometric growth, 131-134 egg, cleavage and larval development, 120-121 hatching, 121-123 parasitic stage, 124-131 larvae, free infectivity, 135 life span and behaviour, 134-5 structure digestive tract, 111-1 12 general morphology, 107-108 glands and caudal appendage, 111 nervous system, 114-1 18 protonephridial system, 112-1 14 sense receptors, 118-120 tegument and ciliary tufts, 108111 life cycle and digenean cycles, 143144 phylogenetic position, 140-143

Asymphylodora amnicolae, life cycle, 176

Atabrine in taeniasis therapy, 292 A toxoplasma argyae, 9 avium, 2, 9, 11 coccothraustus, 4 danilewskii, 10 paddae, 2, 9, 11

Atoxoplasms, 2,3-14 Austrobilharzia terrigalensis, intraniolluscan interaction with Stictodora,

204 Azygia, 170

B Babesiu canis, effect of nor-adrenaline

in shock caused by, 66 Biological control using inter-trematode antagonism 244-251 Biomphalaria glabrata

inter-trematode interactiois in, 194-195,225-238 maintenance, 193-197 straminea, inter-trematode interaction in, 194 Bithionol in taeniasis therapy, 293 Bivesicula, 170 cercariae, 161 Bradynema, lack of cuticle, 364 Burnellus, 169 trichofurcatus, 171 life cycle, 169 Calliobothrium

C verticillatum,

cuticle

structure, 359 Capillaria hepatica, cuticle structure, 361 Carbon dioxide fixation by Plasmod i m , 37-38 Caryophyllaeus fennica, cuticle structure, 359 laticeps, cuticle structure, 359 Catatropis verrucosa, 166 Cephalogonimus, life cycle, 177 Cercaria bucephalopsis haimaena, cuticle struc-

ture, 354 buchanani, cuticle structure, 354 doricha, intramolluscan development,

203 gorgonocephala, 169

pectinata, cuticle structure, 354

403

SUBJECT INDEX

Cestoda, cuticle structure and function, 357-360 Cestodaria, cuticle structure and function, 357 Cestodin in taeniasis therapy, 291 Chloroquine resistance in Plasmodium, 39-41 Clinostomum, 174 giganticum. 164 marginatum, 164 Cloacitrema narrapeenensis, cuticle structure, 354,355 Clonorchis sinensis, cuticle structure, 356 Coccidia, avian, 1-17 adeleine haemogregarines, 14-1 6 atoxoplasms, 3-14 Coenurus cerebralis, differential diagnosis, 280, 281 Coitocaecum anaspidis, life cycle, 176 Contracaecum multipapillaturn, cuticle structure, 361 Control, biological, using inter-trematode antagonism 244-251 Cotylaspis egg, cleavage and larval development, 120 protonephridial system, 83 cokeri, marginal bodies, 103 insignis adult genital system, 90 sense receptors, 99 biology localization in mollusc, 136-137 sexual maturation in mollusc, 137,138 survival of adult outside host, 140 hatching, 121 larvae, free, structure, 113 protonephridial system, 113 reelfootensis, 136, 137 Cotylogaster michaelis adult genital system, 93 nervous system, 93 hatching, 123 occidentalis adult genital system, 90, 93 marginal bodies, 103

biology, infectivity to vertebrate host, 138 localization in mollusc, 137 sexual maturation in mollusc, 137 development hatching, 121 parasitic stage, 126 larvae, free general morphology, 107, 108 protonephridial system, 1 1 3 tegument and ciliary tufts, 1 1 1 Cotylogasteroides occidentalis see Cotylogaster Cotylurus flabelliformis, snail immunity to, 209, 210 lutzi intramolluscan interactions with Paryphostomum segregaturn, 21 1 Schistosoma mansoni, 195, 206207,234 Crassicauda crassicauda, cuticle structure, 361 Crenosema vulpis, cuticle structure, 361 Cryptocotyle lingua, cuticle structure, 354 Cucurbita pep0 seeds in taeniasis therapy, 294 Cysticercosis epidemiology, 299-303 medical and economic losses, 303-304 prevention, 304-307 transmission, 295-299 Cysticercus bovis cuticle structure, 358 differential diagnosis, 280, 281 cellulosae, differential diagnosis, 280, 281 fasciolaris, cuticle structure, 358 longicollis, cuticle structure, 358

D Dasymetra conferta, 162 Delandenus siricidicola, cuticle structure,

364 Delafondia vulgaris, cuticle structure, 361 Derogenes varicus, life cycle, 176

404

S U B J E C T INDEX

Diachasma tryoni, interaction with Opius humilis, 205 Dichlorophen in taeniasis therapy, 293 Dichlosal in taeniasis therapy, 293 Diclidophora merlangi, cuticle structure and function, 351, 352 Dicrocoelium dendriticum, cuticle structure, 356 Dictyocaulus viviparirs, cuticle structure, 361 Dictyocotyle coeliaca, cuticle structure, 351 Digenea cuticle structure and function, 352356 generations alternation, 158-160 suppression and replacement, 164 evolution, 163-1 64 life cycles one host, 156-158 two host, 160-161 three host, 167-177 four host, 177-178 metacercarial stage, 165-1 67 phylogenetic implications, 178-1 79 redial generation, 162-163 Diphylidium caninum, cuticle structure, 359 Diphyllobothrium laturn, 276, 211 cuticle structure, 358, 359 Diplostomum JIexicaudum life cycle, 176 snail immunity to, 210 Dirofilaria immitis, cuticle structure, 361 Ditylenchus dispnci, cuticle structure, 360 Drepanidium, 1 avium, I , 1 1

E Echinochasmus, life cycle, 168 Echinococcus granulosus appendicitis caused by, 286 cuticle function, 359 structure, 358,359 differential diagnosis, 281

egg survival, 295 multilocularis, cuticle structure, 358 Echinoparyphium life cycle, 168 dunni, intramolluscan interaction with xiphidiocercaria, 194 Echinorhynchus truttae, cuticle structure, 369 Echinostoma, 174 life cycle, 168 auclyi biological control of trematodes with, 246 intramolluscan interaction with other trematodes, 194, 225, 237, 249 harbosai adaptation index, 224, 225 infection rate, 220 intramolluscan interaction with Paryphostomum segregatum, I 94 Schistosoma mansoni, 195 maintenance, 198 redial population size, 223, 238 snail immunity to, 21 1 liei infection rate, 216, 220 intramolluscan interaction with Paryphostomum segregatum, 195 Schistosoma mansoni, 195, 20 I , 202, 207, 226, 236 maintenance, 198 redial population size, 223 Iindoense adaptation index, 224, 225 antigen-binding substance in infected Biomphalaria glabrata, 208 infection rate, 218, 220 intramolluscan interaction with Paryphostomum segrega tum, I 95, 204-205 maintenance, 198 miracidia penetration, 222 redial population size, 223 snail immunity to, 21 I malayanum biological control of Schistosoma mansoni with, 246 infection rate, 218 intramolluscan interaction with Schistosoma spindale, 194, 225, 237

S U B J E C T INDEX

Echinostoma malayanum (contd.) miracidia penetration, 220, 221, 222 nudicaudatum, rediae cannibalism, 204 paraensi adaptation index, 224, 225 infection rate, 220 intramolluscan interaction with Paryphostomum segregatui, 195, 205 maintenance, 198 redial population size, 223 snail immunity to, 21 1 Echinuria uncinata, cuticle structure, 361 Eimeria, 14 Eleutheroschizon, I I Enterobius vermicularis, cuticle structure, 362 Etitobdella solne, cuticle structure and function, 351,352 Epomidiosfomum orispinum, cuticle structure, 361 Eiiparyphium, life cycle, 168

F Fasciola intramolluscan development, 201 gigantica biological control by Echinostoma audyi, 246 intramolluscan interaction with E. audyi, 194, 237 miracidia penetration, 220, 221 redial stage limitation, 238 hepatica cuticle, function, 356 structure, 352-354, 356 miracidia penetration, 220, 221, 222 Fascioloides magna, 223 Fern extracts in taeniasis therapy, 294 G Gastrocotyle trachuri, cuticle structure, 351 Glucose nietabolism in Plasmodium, 35-1 Glucose-6-phosphate-dehydrogenase in malaria infected erythrocytes, 33-34

405

Glypthelmins life cycle, 177 pennsylvanicus, intramolluscan development, 203 Gorgoderina,cuticle structure, 356 Gymnophallus choledochus, life cycle, 176 Gyrocotyle urna, cuticle structure, 357 Gyrodactylus, cuticle structure and function, 351, 352 H Habronema muscae, cuticle structure, 361 Haemamoeba danilewkyi, 3 Haemogregarina adiei, 3, 14 aragaoi, 15 atticorae, 14 brachyspizae, 14 francae, 14 monachus, 15 paddae, I , 3, 5, 14 paulasousai, 6 pessoai, 6 pintoi, 15

poroiae, 14 rhamphoceli, 14 serini, 7 sicalidis, 3, 14 sporohilae, 3, 14 tanagrae, 14 travassosi, 15 Haemogregarines, adeleine, 2-3, 14-16 Haemonchus placei, cuticle structure, 360 Haemoproteits rouxi, 3 Haplometra cylindracea,cuticle structure, 356 Helminths, cuticle structure and fiinction Acant hocephala, 369-3 70 Cestoda, 357-360 Cestodaria, 357 Digenea, 352-6 Monogenea, 348-352 Nematoda, 360-369 Turbellaria, 348 Hemicycliophora aretiaria cuticle structure, 360 moulting, 364 Hepatozoon, 9, 15-1 6 ndiei, 14, 15

406

S U B J E C T INDEX

Hepatozoon (contd .) nephrontis, 14 spermesti, 9, 12 Heronimus chelydrae, 164-1 65 mollis, 165 Heterodera rostochiensis, cuticle structure, 360 schachtii, cuticle structure, 360 Himasthla life cycle, 167, 168 quissetensis, 215 Hirshmaniella belli, cuticle structure, 360 gracilis cuticle structure, 360 moulting, 364 Histamine in protozoal infections, 66 Horogenes chrysosticto, oxygen cornpetition with Nerneritis canescens, 214 Hydatigera, 271 Hymenolepis citelli, cuticle structure, 357, 358 diminuta cuticle function, 360 structure, 359 intramolluscan development, 203 nana appendicitis caused by, 286 infection, parornomycin therapy, 292 Hypoderaeum dingeri intramolluscan interaction with Trichobilharziabrevis, 204 T.brevis-Echinostoma audyi, 249 I

Indoplanorbis exustus, inter-trematode interaction in, 194 Isospora, 2, 12-14 lacazei, 6, 13 Zsthmiophora melis, snail immunity to, 213 K Kallikrein in malaria, 63-65 Kinin response to malaria, 60-67 Kronbergia amphipodicola, cuticle structure and function, 348

L Lacistorhynchus tenuis, cuticle structure, 359 Lankesterella, 1, 2, 7, 10, 11, 12-13 adiei, 12 avium, 1, 11 corvi, 4, 5, 12 garnhami, 4,11,12 lainsoni, 12 minima, 13 paddae, 11, 12 passeris, 11 picumni, 12 serini, 11 Lepocreadium setijieroides,215 Leptocotyle minor, cuticle structure, 348, 351 Leucocytogregarina amadinae, 5 neophrontis, 14 Ligula intestinalis, cuticle structure, 358, 359 Lissemysia ovata localization in mollusc, 137 sexual maturation in mollusc, 137 survival of adult outside host, 140 Litomosoides carinii, cuticle structure, 362 Lobatostoma localization in mollusc, 137 ringens, localization in vertebrate, 139 Longidirus macrosoma, cuticle structure, 362 Lophotaspis corbiculae, protonephridial system, 82-83 macdonaldi, localization in mollusc, 137 margaritgerae, localization in mollusc, 137 orientalis, hatching, 121 vallei adult marginal bodies biology localization in mollusc, 137 movement, 134 sexual maturation in mollusc, 137 hatching, 121, 122 larvae, free general morphology, 107,108 life span, 134

SUBJECT INDEX

Lymnaea rubiginosa, inter-trematode interactions in, 194

407

pudentotectus, cuticle structure, 361 salmi, cuticle structure, 361 Mitochondria] respiration inhibition in malaria, 70-72 M Molluscs, biological control, 245 Macraspis Monieza expansa, cuticle structure, cristatn, localization in vertebrate, 139 359 elegans Moniliformis dubius, cuticle structure adult and function, 369, 370 digestive tract, 81 Monogenea, cuticle structure and funcgenital system, 90 tion, 348-352 marginal bodies, 106 Monordotaenia, nomenclature, 27 1 development Multiceps, 271 hatching, 123 serialis, cuticle structure, 357-358 parasitic stage, 128 larvae, free, general morphology, Multicalyx cristata see Macraspis Multicalyx cristatus, hatching, 121 107 localization in vertebrate, 139 Multicotyle purvisi Malaria (see also Plasmodium) adult mammalian, pathogenesis digestive tract, 81-82 anoxic anoxia, 68-70 genital system, 90-93 chain reaction, 71-72 marginal bodies, 103-106 cytotoxic factors, 70 nervous system, 93-99 endothelial permeability changes, protonephridial system, 83-90 51-58 sense receptors, 100-102 inflammation-like responses, 51 tegument, 79-81 intravascular coagulation, 67-68 ventral disc, 103 kinins, 60-67 biology mitochondria1 respiration inhibiinfectivity to vertebrate host, 138tors, 70-72 139 vasomotor changes, 58-60 larvae, free, hepatic, 59 infectivity, 135 intestinal, 59-60 life span and behaviour, 134renal, 59 135 Marisa cornuarietis-Biomphalaria glasexual maturation in mollusc, 137 brata competition in biological control survival of adult outside host, 140 Mecistocirrus digitatus, cuticle strucdevelopment ture, 361 allometric growth, 131-134 Megalodiscus temeperatus, cuticle strucegg, cleavage and larval developture, 356 ment, 120-121 Meloidogyne hatching, 121-122 haplu, cuticle structure, 360 parasitic stage, 124-126, 130 javonica, cuticle structure, 360 larvae, free Mermis nigrescens, cuticle structure and infectivity, 135 function, 3624, 368 life span and behaviour, 134-135 Metagonimoides oregonensis, life cycle, structure 176 digestive tract, 111-1 12 Metagonimus general morphology, 108 takahoshi, cuticle structure, 355 glands and caudal appendage, yakagawi, cuticle structure, 356 111 Metastrongylus nervous system, 114-1 18 elongatus, cuticle structure, 361 protonephridial system, 113-1 14

408

S U B J E C T INDEX

Parahemiurus bennettae, life cycle, 176 Multicotyle purvisi (contd.) Paralepoderma brumpti, life cycle, 176 sense receptors, 118-119 tegument and ciliary tufts, 108- Parapronocephalum symmetricum, 1 66 111 Paromomycin in taeniasis therapy, 292-293 Parorchis acanthus, cuticle structure, 354 N Parvatrema homoeotecnum, 162 Necator americanus, cuticle structure, life cycle, 165,173-174 360 Paryphostomum Nematoda, cuticle structure and funclife cycle, 168 tion, 36&369 segregatum Nematospiroides dubius adaptation index, 224,225 cuticle structure, 362 infection rate, 216,219,220 moulting, 365 intraniolluscan interaction with Nemeritis canescens, oxygen competition Cotylurus lutzi, 21 1 with Horogenes chrysostictos, 214 Echinostoma barbosai, 194 Neoaplectana glaseri, cuticle structure, E. liei, 195 360 E. lindoense, 195,204-205 Niclosamide in taeniasis therapy, 290E. paraensi, 195,205 291 Ribeiroia marini, 194,195 Nippostrongylus brasiliensis Schistosoma mansoni, 195, 200, cuticle 202, 206, 207, 208-209, 210, function, 368 214-215,225-244 structure, 360,362 maintenance, 197-198 moulting, 365-367 rediae Nosema, in biological control of treformation, 203,205 matodes, 245 population, 223 Notocotyloides petasatum, 1 66 snail immunity to, 21 1 Notocotylus attenuatus, cuticle structure, sporocysts, 199 357 Paucivitellosus, cercariae, 164 0 fragilis, 166 cercariae, 161 Oesophagostomum columbianum, cuticle Pentose phosphate pathway in malaria structure, 361 infected erythrocytes, 33-34 Opisthioglyphe, life cycle, 177 Perezia helminthorum, in biological Opisthorchis viyerrini, cuticle structure, control of trematodes, 245-6,248 356 Perostrongylus pridhani, cuticle strucOpius humilis, interaction with Diachasture, 361 ma tryoni, 205 Petasiger, Ornithobilharzia turkestanicum, cuticle life cycle, 168 structure, 356 neocommense, cuticle structure, 354 Ostertagia ostertagi, cuticle structure, Phenasal in taeniasis therapy, 290 361 Phenoxybenzamine, effect on vasomotor changes in malaria, 59-60 Philophthalmus, 162 P Phocanema decipens, moulting, 365 Panagrellus silusiae 6-phosphogluconate-dehydrogenase in cuticle structure, 360 malaria infected erythrocytes, 33-34 moulting, 364 Phyllodistomum Paragonimirs ohirri, cuticle structure, simile, life cycle, 176 356 solidum, 172

SUBJECT INDEX

Phytoalexins, 213 Plagioporus lepomis, 177 Piagiorchis life cycle, 176 snail irmnunity to, 210 Plasmodium, 7-8 (See also Malaria) metabolism, 3 1 4 1 aerobic mechanisms, 38-39 carbon dioxide fixation, 37-38 chloroquine resistance, 3 9 4 I glucose, 35-37 pentose phosphate pathway in infected erythrocytes, 33-34 metabolism of host, 41-44 berghei effect on permeability of brain endothelial membrane, 56 erythrocyte coalescence by, 53 intravascular coagulation in infection, 67-68 kallikrein in infection, 65 metabolism, 32 aerobic mechanisms, 38-39 carbon dioxide fixation, 37 chloroquine resistance, 3 9 4 1 glucose, 35, 36 pentose phosphate pathway, 3334 metabolism of host erythrocytes, 41, 42 tissue, 43 mitochondria, 38 mitochondria1 respiration inhibition by, 70 roatneyi host erythrocyte metabolism, 41,42 kinins in infection, 65 falciparum anoxic anoxia, 69 52-53 intravascular coagulation, 67, 68 metabolism, pentose phosphate pathway, 33, 34 metabolism of host erythrocytes, 41 mitochondria, 38 sulphamethoxine effect on cerebral circulation in infection, 56 vasomotor changes in infection, 58 gallinaceum metabolism aerobic mechanisms, 38

409

pentose phosphate pathway, 33, 34 metabolism of host erythrocytes, 42 knowlesi anoxic anoxia in infection, 69 effect of nor-adrenaline on shock caused by, 66-67 effect on permeability of brain endothelial membranes, 54-55 erythrocyte coalescence by, 53 histamine in infection, 63-65 kallikrein in infection, 63-5 kinins in infection, 61-67 metabolism, 32 aerobic mechanisms, 38 carbon dioxide fixation, 37, 38 glucose, 35, 36 pentose phosphate pathway, 33, 34 metabolism of host, erythrocytes, 41, 42 lipids, 44 tissue, 43 mi tochondrial respiration in hi bition by, 70 vasomotor changes in infection hepatic, 59 intestinal 59-60 renal, 59 Iophurae carbon dioxide fixation, 37, 38 glucose metabolism, 36-37 malariae, mitochondria, 38 vinckei, metabolism of host erythrocytes, 42 Pleurogenes medians, life cycle, 176 Polycelis tenuis, 352 Polymorphus minutus, cuticle structure, 369 Pomphorhynchus laevus, cuticle structure, 369 Posthodiplostomum cuticola, cuticle structure, 354 minimum, cuticle structure, 356 Proctoeces maculutus, 168 Prosthogonimus~ 72 Proterometra dickermani, 164, 1 77 Pseudovermiculi sanguinis, 1 Psilotrema spiculigerum, life cycle, 168 Pumpkin seeds in taeniasis therapy, 293-294

410

SUBJECT INDEX

R Raillietina cesticullus, cuticle structure, 358 Rajonchocontyle ernarginata, cuticle structure, 348, 351 Ratzia j o y e d , life cycle, 176 Renicola thaidus, life cycle, 178-179 Rhabditis pellio, cuticle structure, 361 Ribeiroia marini, interaction with Paryphostomum segregatum, 194, 195 Schistosoma mansoni, 194, 195 ondatrae, life cycle, 168 S

Saccacocoeliodes,cercariae, 164 Schistocephalus solidus, cuticle structure, 358-3 59 Schistosoma bovis infection rate, 217 intramolluscan development, 20 1 miracidia penetration, 220, 221 haematobium infection rate, 219-220 intramolluscan interaction, 203 stages, 238 japonicurn cuticle structure, 355, 356 intramolluscan development, 201 miracidia penetration, 221 mansoni adaptation index, 224, 225 biological control with Echinostoma malayanum, 246 cuticle function, 357 structure, 353, 354356, 358 infection rate, 217-218, 219 intramolluscan development, 201,202 interaction with Cotylurus lutzi, 195, 206-207, 234 Echinostoma barbosai, 195, 226 E. liei, 195, 201, 202, 207, 226, 236 E. Indoense, 226 E. piaraense, 226

Paryphostomurn segregaturn, 195, 200, 202, 206, 207, 208, 210,214215,225-244 Ribeiroia marini, 194, 195, 226 maintenance, 197 miracidia immobilization in Planorbis corneus, 208 penetration, 220, 221, 222-223 snail immunity to, 21 1 toxicity, 213 mattheei infection rate, 217 miracidia penetration, 21 1 spindale cuticle structure, 355 intramolluscan interaction with Echinostoma malayanum, 194, 225, 237 miracidia penetration, 222 Sigrnapera cincta, life cycle, 176 Sphaeridiotrernaglobulus, life cycle, 168 Stannotaen in taeniasis therapy, 291 Stellantchasmus falcatus, 163 Stephanoprora, life cycle, 168 Sterrhurus musculosus,host range, 176 Stichocotyle nephropis adult digestive tract, 81 genital system, 90 sense receptors, 99, 103 biology localization in mollusc, 137 in vertebrate, 139 survival of adult outside host, 140 development hatching, 121 parasitic stage, 126 Stichorchis, 164 Stictodora, intramolluscan interaction with Austrobilharzia terrigalensis, 204 Strigea, life cycle, 177 Strongy loides fulleborni, cuticle structure, 360 rnyoptorni, cuticle structure, 360 ratti, cuticle structure, 360 stercoralis, cuticle structure, 360 Syngarnus skrjabinomorpha, cuticle structure, 361

SUBJECT INDEX

Syphacia obvelata, cuticle structure, 362 moulting, 364-365

T Taenia africana, 271 confusa, 271 crassiceps, cuticle structure, 358 hydatigena cuticle structure, 359 egg survival, 295 immunization against, 306 hominis, 271 multiceps, cuticle structure, 359 ovis, egg survival, 295 pisiformis cuticle structure, 350 egg survival, 295 proglottides, 278 saginata egg survival, 295-299 hosts, 271-273 nomenclature, 270-27 1 structure and biology adult, 274-278 cuticle, 359 cysticercus, 280-282 eggs, 278-279 oncosphere, 279-280 solium, 272-275 appendicitis caused by, 286 cysticercus, 280 diagnosis, 288 embryophores, 278 taeniaeformis, cuticle structure, 357 Taeniarhynchussaginatus, nomenclature, 270-271 Taeniasis clinical aspects diagnosis, 287-289 pathology, 285-287 symptornatology, 282-285 treatment, 289-294 acridines, 292 bithionol, 293 dichlorphen, 293 fern extracts, 294 paromomycin, 292-293 pumpkin seeds, 293-294 tin compounds, 291-292

41 1

Yomesan, 290-291 epidemiology and epizootiology epidemiology, 299-303, 308-309 medical and economic losses, 303304 transmission between man and animals, 295-299 prevention meat inspection, 304305 sanitation, 306-307 serological diagnosis and imrnunization of cattle, 305-306 Taenifuge, 291 Tetratirotaenia, 271 Tin compounds in taeniasis therapy, 291-292 Toxoplasma, 3-10, 14 avium, 5 columbae, 5 cuniculi, 5 gondii, 5, 6, 10 liothricis, 5 passeris, 10 Trematodes, intramolluscan interaction interaction factors, 199-225 materials and methods, 193-199 parameters of antagonism, 225-244 use in biological control, 244-251 Triaenophorus nodulosus, cuticle structure, 358, 359 Trichinellaspiralis cuticle structure, 361-362 moulting, 365, 368 Trichobilharzia brevis biological control by Echinostoma audyi, 246 intramolluscan interaction with E. audyi, 194, 225, 237 E. audyi-Hypoderaeum dingeri, 249 H. dingeri, 204 Trichodorus christiei, cuticle structure, 362 Trichostrongylusorientalis, cuticle structure, 360 Trichuris myocastoris, cuticle structure, 361 suis, cuticle structure, 361 Trypanosomabrucei histamine in infection, 66 kinins in infection, 62

412

SUBJECT INDEX

Turbellaria, cuticle structure and function, 348 Tylenchorhynchus martini, cuticle structure, 360-361 Tylacephalum,cuticle structure, 358

v Vermitin in taeniasis therapy, 290

X Xiphinema index

cuticle structure, 362 moulting, 364 Y Yomesan in taeniasis therapy, 290-291

z Zonocotyfe bicaecata, 78