Kluwer Academic / Plenum Publishers New York, Boston, Dordrecht, London, Moscow
The author has made every effort to ensure the accuracy of the information herein. However, appropriate information sources should be consulted, especially for new or unfamiliar procedures. It is the responsibility of every practitioner to evaluate the appropriateness of a particular opinion in in the context of actual clinical situations and with due considerations to new developments. The author, editors, and the publisher cannot be held responsible for any typographical or other errors found in this book.
ISBN: 0-306-48675-X eISBN: 0-306-48676-8 C 2005 by Kluwer Academic/Plenum Publishers, New York
233 Spring Street, New York, New York 10013 C 1998, 2000 by ICMSF Copyright (Formerly published by Chapman & Hall, ISBN 0-7514-0430-6)
http://www.wkap.nl 10 9 8 7 6 5 4 3 2 1 A C.I.P. record for this book is available from the Library of Congress. All rights reserved No part of this work may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher, with the exception of any material supplied specifically for the purpose of being entered and executed on a computer system, for exclusive use by the purchaser of the work. Permissions for books published in Europe:
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[email protected] Printed in the United States of America
Contents
Preface 1
xiii
Meat and meat products
1
I
1 2 2
Introduction A Definitions B Important properties C Methods of processing and preservation D Types of meat products II Initial microflora A Ruminants B Pigs III Primary processing A Ruminants B Pigs C Spoilage D Pathogens E Control E Control (farm) F Control (transport and holding at abattoirs) G Control (slaughter and dressing of cattle and sheep) H Control (slaughter and dressing of pigs) I Control (chilling (cattle, sheep, and pigs)) J Control (storage and transport) IV Carcass cutting and packaging A Effects of processing on microorganisms B Spoilage C Pathogens D Control (meat stored in air, vacuum-packed or stored in modified atmospheres) V Frozen meat A Effects of processing on microorganisms B Spoilage C Pathogens D Control (frozen meats) VI Raw comminuted meats A Effects of processing on microorganisms B Spoilage C Pathogens D Control (raw comminuted meats) VII Raw cured shelf-stable meats A Effects of processing on microorganisms
3 4 4 4 10 15 15 23 31 32 38 38 40 41 42 43 45 46 46 48 50 51 52 52 52 53 53 54 54 55 55 58 59 59
B Spoilage C Pathogens D Control (raw, cured, shelf-stable meats) Control (Chinese sausages) D Control (dry salami, e.g., Hungarian) D Control (fermented, high acid sausages) VIII Dried meats A Effects of processing on microorganisms B Spoilage C Pathogens D Control (dried meats) IX Cooked perishable uncured meats A Effects of processing on microorganisms B Spoilage C Pathogens D Control (cooked perishable uncured meats) X Fully retorted shelf-stable uncured meats A Effects of processing on microorganisms B Spoilage C Pathogens D Control ( fully retorted shelf-stable uncured meats) XI Cooked perishable cured meats A Effects of processing on microorganisms B Spoilage C Pathogens D Control (cooked, perishable cured meats) XII Shelf-stable cooked cured meats A Effects of processing on microorganisms B Spoilage C Pathogens D Control (shelf-stable cooked cured meats) XIII Snails A Definition B Production and processing C Pathogens D Control (snails) XIV Froglegs A Definition B Production and processing C Pathogens D Control (froglegs) References
62 62 64 65 66 67 68 68 69 69 69 71 71 72 73 74 75 75 76 76 76 78 78 79 80 82 83 83 83 83 84 84 84 85 85 85 86 86 86 87 87 88
vi
2
CONTENTS
Poultry products I
Introduction A Definitions B Important properties C Method of processing D Types of poultry products II Initial microflora (effect of farm practices) III Primary processing (whole birds and parts) A Effects of processing on microorganisms B Spoilage C Pathogens D Control (primary processing, whole birds and parts) IV Frozen poultry products A Effects of processing on microorganisms B Spoilage C Pathogens D Control (frozen poultry product) V Perishable, cooked poultry products A Effects of processing on microorganisms B Spoilage C Pathogens D Control (perishable, cooked poultry products) VI Fully retorted (“botulinumcooked”) poultry products A Control (fully retorted shelf-stable poultry products) VII Dried poultry products A Effects of processing on microorganisms B Spoilage C Pathogens D Control (dried poultry products) References
3
Fish and fish products I II III
IV
Introduction A Definitions B Important properties Initial microflora A Saprophytic microorganisms B Pathogens and toxicants Primary processing A Finfish of marine and freshwater origin Control (finfish of marine and freshwater origin) B Crustacea Control (crustacea) C Mollusca Control (mollusca) Aquaculture A Initial microflora B Spoilage
107
C Pathogens D Control (aquaculture) V Frozen raw seafood A Freezing process B Saprophytes and spoilage C Pathogens D Control (frozen raw seafood) VI Minced fish and surimi products VII Cooked crustaceae (frozen or chilled) A Cooking, picking, and packaging B Saprophytes and spoilage C Pathogens D Control (cooked crustaceae, frozen or chilled) VIII Lightly preserved fish products A Introduction B Saprophytes and spoilage C Pathogens D Control (lightly preserved fish products) IX Semi-preserved fish products A Introduction B Saprophytes and spoilage C Pathogens D Control (semi-preserved fish products) X Fermented fish products A Control (fermented fish products) XI Fully dried or salted products A Control (fully dried or salted products) XII Pasteurized products A Introduction B Saprophytes and spoilage C Pathogens D Control (pasteurized fish products) XIII Canned seafood A Processing B Control (canned seafood) References
107 108 108 108 108 110 111 111 123 127 145 146 146 146 147 147 148 148 149 150 152 154 154 155 156 156 156 156 157
174 174 174 175 177 177 180 190
4
Feeds and pet foods I II
III
190 195 197 200 202 206 208 208 208
IV
Introduction Roughages A Effects of processing on microorganisms B Spoilage C Pathogens D Control (roughages) Animal by-products A Effects of processing on microorganisms B Spoilage C Pathogens D Control (animal by-products) Fish meal A Effects of processing on microorganisms B Spoilage C Pathogens D Control (fish meal)
209 210 211 211 212 212 213 214 215 215 215 217 220 221 221 222 223 225 227 227 227 228 228 229 230 231 232 232 232 233 233 234 235 235 235 236
250 250 251 252 252 253 254 256 257 258 258 261 263 264 265 265 265
vii
CONTENTS
V
Compounded feeds A Effects of processing on microorganisms B Spoilage C Pathogens D Control (compounded feeds) VI Pet foods A Effects of processing on microorganisms B Spoilage C Pathogens D Control (pet foods) References
5
Vegetables and vegetable products I
Introduction A Definitions and important properties II Initial microflora (including field practices and harvest) A Saprophytic microorganisms B Pathogens C Good agricultural practices III Raw and minimally processed vegetables A Effects of transportation, processing, and storage on microorganisms B Saprophytes and spoilage C Pathogens D Control (raw and minimally processed vegetables) IV Cooked vegetables A Effects of processing on microorganisms B Saprophytes and spoilage C Pathogens D Control (cooked vegetables) V Frozen vegetables A Effects of processing on microorganisms B Saprophytes and spoilage C Pathogens D Control (frozen vegetables) VI Canned vegetables A Effects of processing on microorganisms B Saprophytes and spoilage C Pathogens D Control (canned vegetables) VII Dried vegetables A Effects of processing on microorganisms B Saprophytes and spoilage C Pathogens D Control (dried vegetables) VIII Fermented and acidified vegetables A Effects of processing on microorganisms B Saprophytes and spoilage C Pathogens
266
D Control (fermented and acidified vegetables) IX Sprouts A Effects of harvesting, transportation, processing, and storage B Saprophytes and spoilage C Pathogens D Control (sprouts) X Mushrooms A Effects of harvesting, transportation, processing, and storage on microorganisms B Saprophytes and spoilage C Pathogens D Control (mushrooms) XI Cassava A Effects of harvesting, transportation, processing, and storage on microorganisms B Control (cassava) References
266 267 268 268 270 271 271 271 272 272
277 277 277 278 279 279 280
6
Fruits and fruit products I
281 281 283 284 289 294 294 294 294 295 295 295 296 296 297 297 297 298 299 299 301 301 301 302 302 303 303 305 305
Introduction A Definitions B Important properties C Methods of processing D Types of final products II Initial microflora (fresh fruits) III Primary processing A Effects of processing on microorganisms B Spoilage C Pathogens D Control (fresh fruits) IV Pre-cut (minimally processed) fruit A Effects of processing on microorganisms B Spoilage C Pathogens D Control (pre-cut (minimally processed) fruit) V Frozen fruits A Effects of processing on microorganisms B Spoilage C Pathogens D Control (frozen fruits) VI Canned fruits A Effects of processing on microorganisms B Spoilage C Pathogens D Control (canned fruits) VII Dried fruits A Effects of processing on microorganisms B Spoilage C Pathogens D Control (dried fruits)
306 307 307 307 308 309 311 311 312 312 313 314 314 315 315
326 326 326 326 326 327 328 328 328 329 334 336 338 338 339 339 340 341 341 341 342 342 342 342 343 343 344 345 345 346 346 347
viii
CONTENTS
VIII Fermented and acidified fruits A Effects of processing on microorganisms B Spoilage C Pathogens D Control (fermented and acidified fruits) IX Tomato products A Effects of processing on microorganisms B Spoilage C Pathogens D Control (tomato products) References
7
Spices, dry soups, and oriental flavorings Spices, herbs, and dry vegetable seasonings A Definitions B Important properties C Methods of processing and preservation D Types of final products E Initial microflora F Primary processing G Processing H Control (spices, herbs, and dry vegetable seasonings) II Dry soup and gravy mixes A Definitions B Initial microflora C Primary processing D Control (dry soup and gravy mixes) III Soy sauces A Definition B Important properties C Methods of processing and preservation D Types of final products E Initial microflora F Primary processing G Control IV Fish and shrimp sauces and pastes A Definitions B Important properties C Methods of processing and preservation D Types of final products E Initial microflora F Primary processing G Control References
II
Initial microflora A Fungi B Bacteria III Primary processing A Effects of processing on microorganisms B Spoilage C Pathogens and toxins D Control (cereals) IV Flours, starches, and meals A Effects of processing on microorganisms B Saprophytes and spoilage C Pathogens and toxins D Control (flours, starches and meals) V Dough A Effect of processing on microorganism B Spoilage C Pathogens and toxins D Control (dough) VI Breads A Effects of processing on microorganisms B Spoilage C Pathogens and toxins D Control (breads) VII Pasta and noodles A Effects of processing on microorganisms B Spoilage C Pathogens and toxins D Control (pasta and noodles) VIII Breakfast cereals and snack foods A Effects of processing on microorganisms B Spoilage C Pathogens and toxins D Control (breakfast cereals, snack foods) IX Pastries and filled products A Effects of processing on microorganisms B Spoilage C Pathogens D Control (pastries and filled products) References
348 348 349 350 350 351 351 351 352 352 353
360
I
8
Cereals and cereal products I
Introduction A Definitions B Important properties C Methods of processing D Types of final products
360 360 360 362 362 363 365 368 371 372 372 372 373 374 374 374 374 375 377 378 378 380 382 382 382 382 383 383 384 385 385
9
Nuts, oilseeds, and dried legumes I
392 392 392 393 393 394
II
Introduction A Definitions B Important properties C Methods of processing D Types of final products Initial microflora A Nuts B Oilseeds C Legumes D Coffee
394 394 398 399 399 401 403 408 409 409 411 411 412 413 413 414 414 415 415 415 417 419 419 421 421 421 422 423 423 423 424 424 424 425 425 425 426 426 429
440 440 440 440 441 442 443 443 443 443 443
ix
CONTENTS
III
Primary processing A Effects of processing on microorganisms B Spoilage C Pathogens D Control (primary processing of tree nuts, peanuts, coconut, dried legumes, and coffee) IV Tree nut, peanut, and coconut processing A Effects of processing on microorganisms B Spoilage C Pathogens D Control (tree nut, peanut and coconut processing) V Oilseed products A Effects of processing on microorganisms B Spoilage C Pathogens D Control (oilseed products) VI Legume products A Effects of processing on microorganisms B Spoilage C Pathogens D Control (legume products) VII Coffee products References
10
Cocoa, chocolate, and confectionery I
Introduction A Definitions B Important properties II Initial microflora III Primary processing A Effects of processing on microorganisms B Methods of processing IV Processed products A Effects of processing on microorganisms B Spoilage C Pathogens D Control (cocoa, chocolate and confectionery) References
III
Mayonnaise-based salads A Definitions B Important properties C Methods of processing and preservation D Microbial spoilage and pathogens E Control (mayonnaise-based salads) IV Margarine A Definitions B Important properties C Methods of processing and preservation D Microbial spoilage and pathogens E Control (margarine) V Reduced-fat spread A Definitions B Important properties C Methods of processing and preservation D Microbial spoilage and pathogens E Control (reduced-fat spread) VI Butter A Definitions B Important properties C Methods of processing and preservation D Microbial spoilage and pathogens E Control (butter) VII Water-continuous spreads VIII Miscellaneous products References
444 444 448 449 455 458 458 458 458 459 460 460 460 460 460 460 460 461 461 461 461 461
467 467 467 467 468 468 468 470 470
12
Sugar, syrups, and honey I II
III
470 471 472 474 476 IV
11
Oil- and fat-based foods I II
General introduction Mayonnaise and dressings A Definitions B Important properties C Methods of processing and preservation D Microbial spoilage and pathogens E Control (mayonnaise and dressings)
480 480 481 481 482 V 483 485 491
Introduction Cane sugar A Initial microflora B Effects of processing on microorganisms C Spoilage D Pathogens E Control (cane sugar) Beet sugar A Initial microflora B Effects of storage and processing on microorganisms C Spoilage D Pathogens E Control (beet sugar) F Microorganisms in refined sugar capable of spoiling other food Palm sugar A Initial microflora B Effects of processing on microorganisms C Spoilage D Pathogens E Control (palm sugar) Syrups A Initial microflora B Effect of processing on microorganisms C Spoilage
493 493 493 493 494 495 496 496 497 497 500 502 504 504 505 505 506 507 508 508 509 509 510 513 515 516 516
522 522 522 522 523 525 526 527 528 528 528 530 531 531 532 533 533 533 533 533 534 534 534 535 535
x
CONTENTS
D Pathogens E Control (syrups) VI Honey A Initial microflora B Effect of processing on microorganisms C Spoilage D Pathogens E Control (honey) References
13
Soft drinks, fruit juices, concentrates, and fruit preserves I
Introduction A Foods covered B Important properties C Initial microflora II Potential food safety hazards A Mycotoxins B Bacterial pathogens C Viruses D Parasites III Spoilage A Preservative resistant yeasts B Filamentous fungi (molds) C Bacteria IV Processing A Heat processing B Chilled storage C Preservatives D Stabilization of concentrated fruit products E Stabilization of fruit preserves F Combination of pasteurization and preservatives G Alternative non-thermal methods Control (soft drinks, carbonated and non-carbonated) Control (fruit juice and related products) H Tea-based beverages References
14
Water I
II
III
Introduction A Important properties B Methods of processing and preservation C Types of final products Drinking water A Definitions B Initial microflora C Primary processing of raw water D Pathogens E Spoilage F Control (drinking water) Process or product water A Definition B Initial microflora
536 536 537 538
C Primary processes of processing or product water D Control (process or product water) IV Bottled water A Definitions B Initial microflora C Primary processing C Effects of processing on microorganisms C Pathogens D Spoilage E Control (natural mineral water) References
538 539 539 539 540
544
15
544 544 545 548 548 549 549 550 551 551 551 554 554 556 557 559 559
I
Introduction A Definitions B Important properties C Types of products II Initial microflora A Transovarian transmission B Contamination in the cloacae C Contamination in the production environment III Shell eggs A Effect of initial processing B Spoilage C Pathogens D Control (shell eggs) IV Liquid eggs A Effects of processing on microorganisms B Spoilage C Pathogens D Control (liquid eggs) V Dried eggs A Effects of processing on microorganisms B Spoilage C Pathogens D Control (dried eggs) VI Further processed egg products References
562 563 563 564 565 565 568 568
574
Eggs and egg products
16
Milk and dairy products I
574 574 574 574 574 574 575 576 580 580 581 583 583 584
II
Introduction A Definitions B Importance of microorganisms and other important properties C Methods of processing and preservation D Types of final products Raw milk—initial microflora A Interior of the udder B Udder and teat surfaces C Milk handling equipment D Environment E Persons handling milk F Antimicrobial factors naturally present in milk G Inhibitory substances and veterinary drug residues
584 585 587 587 587 587 588 590 590 590 592
597 597 597 597 601 602 602 606 607 608 608 612 614 616 617 617 625 625 627 629 629 631 631 632 632 633
643 643 643 644 645 645 645 646 647 647 648 648 648 649
xi
CONTENTS
III
Raw milk for direct consumption A Effects of handling of raw milk on microorganisms B Spoilage C Pathogens D Control (raw milk for direct consumption) IV Processed fluid milk A Introduction B Initial processing steps C Basic procedures to reduce the initial microflora D Cleaning and disinfection E Effects of processing on microorganisms F Spoilage G Pathogens H Control (processed fluid milk) I Shelf-stable milk Control (shelf-stable milk) V Cream A Effect of processing on microorganisms B Spoilage C Pathogens D Control VI Concentrated milks A Effects of processing on microorganisms B Spoilage C Pathogens D Control (concentrated milks) VII Dried dairy products A Effects of processing on microorganisms B Spoilage C Pathogens D Control (dried dairy products) VIII Ice cream and frozen dairy desserts A Effects of processing on microorganisms B Spoilage C Pathogens D Control (ice cream and frozen dairy desserts) IX Fermented milks A Effect of processing on microorganisms B Spoilage C Pathogens D Control (fermented milks) X Cheese A Effects of processing on microorganisms B Spoilage C Pathogens D Control (fresh and ripened cheese) Control (processed cheese) References
650 650 651 651 654 657 657 657 657 659 659 659 660 662 664 666 668 668 668 668 668 669 669 670 670 671 672 672 673 673 674 676 677 677 678
17
Fermented beverages
716
Introduction A Definitions B Important properties C Methods of processing D Types of final products II Initial microflora A Grains B Grapes III Primary processing A Effects of processing on microorganisms B Spoilage C Pathogens D Control (fermented beverages) References
716 716 716 716 718 718 718 718 719
I
Appendix I Objectives and accomplishments of the ICMSF History and purpose Functions and membership Recent projects Past and future
Appendix II ICMSF participants Officers Past members of the ICMSF Members of the Latin American Subcommission Former members of the Latin American Subcommission Members of the South-East Asian Subcommission
719 719 721 722 723
725 725 725 726 727
729 729 730 731 732 732
678 680 680 683 683 684 685 686 689 690 693 696 698
Appendix III Publications of the ICMSF Books WHO publications Other ICMSF technical papers Translations About the ICMSF
Index
733 733 734 734 734
737
Preface
The second edition of Microbiology of Foods 6: Microbial Ecology of Food Commodities was written by the ICMSF, comprising 16 scientists from 11 countries, plus consultants and other contributors to chapters. The intention of the second edition was to bring the first edition (published in 1996) up to date, taking into account developments in food processing and packaging, new products, and recognition of new pathogens and their control acquired since the first edition. The overall structure of the chapters has been retained, viz each covers (i) the important properties of the food commodity that affect its microbial content and ecology, (ii) the initial microflora at slaughter or harvest, (iii) the effects of harvesting, transportation, processing, and storage on the microbial content, and (iv) an assessment of the hazards and risks of the food commodities and (v) the processes applied to control the microbial load. In 1980s, control of food safety was largely by inspection and compliance with hygiene regulations, together with end-product testing. Microorganisms in Foods 2: Sampling for Microbiological Analysis: Principles and Specific Applications (2nd ed. 1986) put such testing on a sounder statistical basis through sampling plans, which remain useful when there is no information on the conditions under which a food has been produced or processed, e.g. at port-of-entry. At an early stage, the Commission recognized that no sampling plan can ensure the absence of a pathogen in food. Testing foods at ports of entry, or elsewhere in the food chain, cannot guarantee food safety. This led the Commission to explore the potential value of HACCP for enhancing food safety, particularly in developing countries. Microorganisms in Foods 4: Application of the Hazard Analysis Critical Control Point (HACCP) System to Ensure Microbiological Safety and Quality (1988) illustrated the procedures used to identify the microbiological hazards in a practice or a process, to identify the critical control points at which those hazards could be controlled, and to establish systems by which the effectiveness of control could be monitored. Recommendations are given for the application of HACCP from production/harvest to consumption, together with examples of how HACCP can be applied at each step in the food chain. Effective implementation of HACCP requires knowledge of the hazardous microorganisms and their response to conditions in foods (e.g. pH, aw , temperature, preservatives). The Commission concluded that such information was not collected together in a form that could be assessed easily by food industry personnel in quality assurance, technical support, research and development, and by those in food inspection at local, state, regional or national levels. Microorganisms in Foods 5: Characteristics of Microbial Pathogens (1996) is a thorough, but concise, review of the literature on growth, survival, and death responses of foodborne pathogens. It is intended as a quick reference manual to assist making judgements on the growth, survival, or death of pathogens in support of HACCP plans and to improve food safety. The second edition of Microorganisms in Foods 6: Microbial Ecology of Food Commodities (2004) is intended for those primarily in applied aspects of food microbiology. For 17 commodity areas, it describes the initial microbial flora and the prevalence of pathogens, the microbiological consequences of processing, typical spoilage patterns, episodes implicating those commodities with foodborne illness, and measures to control pathogens and limit spoilage. Those control measures are presented in a standardized format, and a comprehensive index has been added.
xiv
PREFACE
The second edition of Microorganisms in Foods 6: Microbial Ecology of Food Commodities has been written following Microorganisms in Foods 7: Microbiological Testing in Food Safety Management (2002). The latter illustrates how systems such as HACCP and GHP provide greater assurance of safety than microbiological testing, but also identifies circumstances where microbiological testing still plays a useful role in systems to manage food safety. It continues to address the Commission’s objectives to: (a) assemble, correlate, and evaluate evidence about the microbiological safety and quality of foods; (b) consider whether microbiological criteria would improve and assure the microbiological safety of particular foods; (c) propose, where appropriate, such criteria; (d) recommend methods of sampling and examination; (e) give guidance on appraising and controlling the microbiological safety of foods. It introduces the reader to a structured approach for managing food safety, including sampling and microbiological testing. The text outlines how to meet specific food safety goals for a food or process using Good Hygienic Practice (GHP) and the HACCP system. Control measures as used in GHP and HACCP are structured into three categories: those that influence the initial level of the hazard, those that cause reduction, and those that may prevent increase, i.e. during processing and storage. In Microorganisms in Foods 6, a control section following each commodity group uses this structured approach. Microorganisms in Foods 5, 7, and the second edition of Microorganisms in Foods 6 (2005) are intended for anyone using microbiological testing and/or engaged in setting Microbiological Criteria, whether for the purpose of Governmental Food Inspection and Control or in Industry. The contents are essential reading for food processors, food microbiologists, food technologists, veterinarians, public health workers and regulatory officials. For students in Food Science and Technology, they offer a wealth of information on Food Microbiology and Food Safety Management, with many references for further study.
xv
PREFACE
Editorial committee T. A. Roberts (Joint Chairman) J.-L. Cordier L. Gram R. B. Tompkin
J. I. Pitt (Joint Chairman) L. G. M. Gorris K. M. J. Swanson
ICMSF Members during preparation of the second edition of Microbiology of Foods 6: Microbial Ecology of Food Commodities Chairman Secretary Treasurer Members
Consultants
M. B. Cole M. van Schothorst (retired 2003) L. Gram (from 2003) J. M. Farber R. L. Buchanan S. Dahms B. D. G. M. Franco J.-L. Jouve A. M. Lammerding J. I. Pitt (to 2002) K. M. J. Swanson R. B. Tompkin (to 2002) J. Braeunig (2000) L. G. M. Gorris (2000) H. Kruse (2000) J. I. Pitt (2003) T. A. Roberts (2001–03) K. M. J. Swanson (2000) M. Zwietering (2003)
J.-L. Cordier R. S. Flowers L. G. M. Gorris F. Kasuga Z. Merican M. Potter P. Teufel M. Germini (2003) F. Kasuga (2002–03) X. Lui (2003) M. Potter (2002–03) R. Stephan (2003) R. B. Tompkin (2003)
xvi
PREFACE
Contributors and reviewers Chapter
2
Poultry
Contributors J. Greig (Can) T. Nesbakken (Norway) R. Stephan (Switz) F. Kasuga (Japan)
3 4
Fish Feeds
F. Kasuga (Japan) —
5 6 7 8
Vegetables Fruit Spices Cereals
M. L. Tortorello (USA) — —
9 10 11
Nuts Cocoa Oils & fats
— — —
1
Meat
12 Sugar 13 Soft drinks 14 15
Water Eggs
16
Milk
17
Fermented beverages
18
Index
L. Eyde (Aus) C. Stewart (Aus) K. Deibel (USA) — R. Buchner (USA) J. Braunig (Ger) P. Hall (USA) A. Lillie (Den) P. Sigsgaard (Den) J. Eyles (Aus)
Reviewers — J. E. L. Corry (UK) T. Humphrey (UK) Q. L. Yeoh (Malaysia) B. Veldman (Neth) F. Driehuis (Neth) C. Jakobsen (Den) M. Kundura (USA) — — T. Smith (USA) S. Hood (USA) — — R. van Santen (Neth) G. Naaktgeboren (Neth)
— — J. E. L. Corry (UK) T. Humphrey (UK)
— —
1 Meat and meat products
I Introduction Red meat is derived from a number of animal species (e.g. cattle, sheep, goat, camel, deer, buffalo, horse, and pig). Total world production of red meats and quantities in international trade can be obtained from http://apps.fao.org/page/collections?subset=agriculture, a part of http://www.fao.org. Red meat has the potential to carry pathogenic organisms to consumers. In the past, the main public health problem was caused by the classical zoonoses, i.e. diseases or pathogens that can be transmitted from animals to human beings, such as bovine tuberculosis, and also produce pathological changes in animals. However, the measures introduced by classical meat inspection (inspection, palpation, and incision) have proved highly effective against them. Thus, tuberculosis shows very typical changes of the lymph nodes (granulomatous lymphadenitis); they can be reliably detected by incision of the nodes during meat inspection. However, today, the main problem is latent zoonoses. These pathogens occur as a reservoir in healthy animals, where they produce no pathological conditions or changes. However, they can contaminate the food chain in meat production, for instance during slaughtering. The slogan “healthy animals, healthy food” is not true from this point of view. Strict maintenance of good practices of slaughter hygiene in meat production is of central importance, because microbiological hazards are not eliminated in the slaughtering process. Bacteria able to cause food-borne disease, and which can constitute a hazard in at least some meat products, include Salmonella spp., thermophilic Campylobacter spp., enterohemorrhagic Escherichia coli (e.g. serogroup O157; EHEC), some serovars of Yersinia enterocolitica, Listeria monocytogenes, Clostridium perfringens, Staphylococcus aureus, Cl. botulinum, and Bacillus cereus. Meats are also subject to microbial spoilage by a range of microorganisms including Pseudomonas spp., Shewanella, Enterobacteriaceae, Brochothrix thermosphacta, lactic acid bacteria (LAB), psychrotrophic clostridia, yeasts, and molds. In recent years, bovine spongiform encephalopathy (BSE) (“mad cow disease”) has attracted public health attention. The first cases of BSE were reported in Great Britain in November 1986. It appears probable that the disease can be transmitted to humans by food. The prions that cause the disease are very resistant to chemical and physical influences, i.e. to heat, UV, and ionizing radiations and disinfectants. Prions are sensitive to certain alkaline substances and moist heat under high pressure. An effective disinfectant measure is steam sterilization at 133◦ C and 3 bar pressure for 20 min. On the basis of current knowledge, the cause of the BSE epidemic was animal feed (meat- and bone-meal and the like) containing brain, eyes or spinal cord of infected animals, and other tissues that had been inadequately heated during the production process. To protect human health, the use of certain bovine organs (so-called specified risk materials: brain, eyes, spinal cord, spleen, thymus (sweetbread), bovine intestines of cattle >6 months old, visible lymph and nerve tissue, as well as lymph nodes) is prohibited for manufacturing foodstuffs, gelatine, tallow, drugs or cosmetics. More information and actual data can be obtained from the following web-sites: http://www.oie.int/eng/en index.htm; http://www.who.int/mediacentre/factsheets/fs113/en/; http://www.defra.gov.uk/animalh/bse/index.html; http://www.aphis.usda.gov/oa/bse/; http://www.tseandfoodsafety.org/; http://www.unizh.ch/pathol/neuropathologie/. This chapter, however, mainly describes the microorganisms that contaminate red meats and meat products, and factors and operations that increase or decrease the numbers or spread of microorganisms
2
MICROORGANISMS IN FOODS 6
during processing, storage, and distribution. It also contains sections on the microbiology of froglegs and snails as foods. A Definitions Red meat is primarily the voluntary striated skeletal muscular tissue of “red” meat animals. The muscle is made up of contractile myofibrillar proteins, soluble sarcoplasmic proteins (e.g. glycolytic enzymes and myoglobin) and low molecular weight soluble organic and inorganic compounds. Connective tissue is in intimate association with muscle cells and can constitute up to 30% of total muscle protein. Fat cells occur subcutaneously and both within and surrounding the muscle. Within a muscle, fat cells are located in the perimysial space. Up to one-third of the weight of some muscles may be fat. Muscle tissues also contain 0.5–1% phospholipid. Meat as legally defined commonly includes various organs (“variety meats” or “offals”). The organs and other parts of the carcass that are regarded as edible vary between countries. The heart has some similarities to skeletal muscle and is composed of striated involuntary muscle, connective tissue, and some lipid. The liver contains uniform liver cells with a network of blood vessels and epithelial-lined sinusoids. In the kidney, there is a meshwork of connective tissue that supports renal tubules, small veins, and arteries. B Important properties Meat has a high water and protein content, is low in carbohydrates and contains a number of low molecular weight soluble constituents (Table 1.1). The vitamin content (µg/g) of muscle is approximately: thiamine, 1; riboflavin, 2; niacin, 45; folic acid, 0.3; pantothenic acid, 10; B6 , 3; B12 , 0.02 and biotin, 0.04 (Schweigert, 1987). The concentrations of vitamins vary with species, age, and muscle. Pork muscle has 5–10 times more thiamine than is found in beef or sheep muscle. Vitamins tend to be higher in organs (e.g. liver and kidney) than in muscle. Meat is a nutritious substrate with an aw (0.99) suitable for the growth of most microorganisms. Growth is primarily at the expense of low molecular weight materials (carbohydrates, lactate, and amino acids). Microbial proteolysis of structural proteins occurs at a very late stage of spoilage (Dainty et al., 1975).
Table 1.1 Approximate composition of adult mammalian muscle after rigor mortis Component Water Protein Lipid Glycogena Glucosea,b and glycolytic intermediatesa Lactic acida Inosine monophosphateb Creatineb Amino acidsb Dipeptides (carnosine and anserine)b pHa Lawrie (1985). a Varies between muscles and animals. b Varies with time after rigor mortis.
% Wet weight 75 19 2.5 0.1 0.2 0.9 0.3 0.6 0.35 0.35 (5.5)
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During death of the animal when the oxygen supply to the muscle is cut off, anaerobic glycolysis of stored glycogen to lactic acid lowers the pH. Post-mortem glycolysis continues as long as glycogen is available or until a pH is reached which inhibits the glycolytic enzymes. In typical muscles this pH is 5.4–5.5. In some muscles (e.g. beef sternocephalicus muscle), glycolysis ceases at a pH near 6 even though considerable glycogen remains. The ultimate pH varies between muscles of the same animal and between animals, and is determined by the glycogen content of the muscle and the accessibility of glycogen to glycolysis. The pH of post-rigor muscle can vary from 5.4–5.5 (lactate content close to 1%) to 7.0 (very little lactate present). The lactate content of muscle is inversely proportional to its pH. On the surfaces of beef and sheep carcasses, the availability of oxygen permits aerobic metabolism to continue, and much of the exposed surface tissue has a pH >6 (Carse and Locker, 1974), which facilitates microbial growth. In the live animal, the glycogen concentration of muscle averages 1%, but varies considerably. Glycogen in pig muscle is readily depleted by starvation and moderate exercise, whereas glycogen in the muscles of cattle is more resistant to starvation and exercise. In both species, pre-slaughter stress (e.g. excitement and cold) depletes muscle glycogen. Glycogen is more concentrated in liver (2–10%) than in muscle, and its content is also affected by pre-slaughter conditions. A low concentration of glycogen in muscles results in a high ultimate pH, which gives rise to “dark-cutting” beef or dark, firm and dry meat (DFD). The amount of glucose in post-rigor muscle varies with pH (Newton and Gill, 1978) being virtually absent in muscle of pH > 6.4. In normal-pH (5.5–5.8) muscle, glucose is present at about 100–400 µg/g (Gill, 1976). Liver has a high glucose content (3–6 mg/g), which appears to be independent of pH (Gill, 1988). By the time the ultimate pH is reached, adenosine triphosphate has largely broken down to inosine monophosphate (IMP). During the storage of meat, IMP and inosine continue to degrade to hypoxanthine, ribose, and ribose phosphate. Ribose, inosine, and IMP can be used as energy sources by a number of fermentative Gram-negative bacteria, and ribose by Broch. thermosphacta, and a number of lactic acid bacteria. Fatty tissue contains less water than muscle, has a pH near neutrality with little lactate, and contains low molecular weight components (glucose and amino acids) from serum (Gill, 1986). Consequently, microbial growth on fat is slower than on the surface of muscle. C Methods of processing and preservation Animals are raised on farms where some are grazed and some are raised under intensive or almost industrial conditions. The microflora in the intestinal tract or on the external surfaces of the animals may vary with the systems of animal production (e.g. more fecal material on the hides of feed-lot cattle). Animals may be slaughtered when young (e.g. calves at 3–4 weeks of age), or when 1 or 2, or several, years old (e.g. cattle and sheep). At the abattoir, the skin of cattle and sheep is removed, the skin of pigs is usually scalded (although it is removed in some plants), then the intestinal tract and viscera are removed. The carcass may then be washed, where regulations permit it, or not, and then chilled. Spoilage organisms grow rapidly on meat, which is a highly perishable commodity. Thus, trade in meat, even at the local level, depends on some degree of preservation that controls the spoilage flora. The most important means of preservation are chilling or freezing, cooking (includes canning), curing, drying, and packaging. Packaging affords extension of shelf-life. Several procedures to reduce microbial growth are often combined. Chilled temperature storage enables fresh meat to be held for only a limited time before spoilage ensues. However, by vacuum-packaging chilled meat in films of low permeability to gases, or by packaging in modified atmospheres, storage-life may be extended for up to at least 12 weeks.
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D Types of meat products Red meats are traded as chilled or frozen carcasses, large primal pieces or retail size portions, chilled or frozen offals, chilled vacuum-packed meat, dried meats, fermented meat, raw or cooked cured products, cooked uncured meat and cooked canned products.
II Initial microflora A Ruminants At birth, the digestive tract of a ruminant is physiologically that of a monogastric. The rumino-reticulum complex develops quickly between 2 and 6 weeks of age when the animals are fed roughage. Initially, large numbers of E. coli, Cl. perfringens and streptococci are in the gut and are shed in feces (107 – 108 cfu Cl. perfringens/g, 109 cfu E. coli/g). After about 2 weeks, Cl. perfringens declines to about 104 cfu/g and E. coli to ca. 106 cfu/g at about 3 months of age. When comparing fecal excretion of coliforms, the mean count for eight calves between 3 and 8 weeks of age was log10 7.2 cfu/g and for adult cows was log10 4.9 cfu/g (Howe et al., 1976). Invasive serotypes of salmonellae, such as Salmonella Typhimurium and S. Enteritidis, are more difficult to control in the live animal than serovars occasionally found in feed. In the first few days of life, young ruminants are more susceptible to salmonellae. Calves dosed with S.Typhimurium prior to 3 days of age were more easily infected, and excreted salmonellae for longer periods and in greater numbers, than calves inoculated at 18 days (Robinson and Loken, 1968). At slaughter, salmonellae were also detected more frequently in mesenteric and cecal lymph nodes from the younger animals. Young calves that are surplus to dairy farm requirements may be sold through markets and dealers to rearing farms. In England, salmonellae have been found in 3.7% of environmental samples taken at calf markets and in 20.6% of swab samples from vehicles used to transport calves (Wray et al., 1991). Salmonellae have also been detected on the walls (7.6% of swabs) and floors (5.3% of swabs) at dealers’ premises (Wray et al., 1990). The mixing of young susceptible calves and their subsequent transport to rearing farms disseminates salmonellae. On arrival at rearing farms, the prevalence of salmonellae in calf feces is relatively low but can increase rapidly. When fecal samples were taken from 437 calves within 2 days of arrival at a rearing farm, salmonellae were detected in 5.3% (Hinton et al., 1983). After about 2 weeks on the farm, salmonellae were found in 42.2% of 491 animals sampled. The shedding rate of salmonellae peaked at 2–3 weeks and then declined; this is possibly associated with the development of a more adult-type intestinal flora. The high concentration of volatile fatty acids and the pH of the fluid in the developed rumen of the well-fed animal provide some protection to infection with salmonellae and verotoxin-producing E. coli (often of the serogroup O157; VTEC) (Chambers and Lysons, 1979; Mattila et al., 1988). Viable cells of these organisms disappear from rumen fluid at a rate faster than expected from wash-out. Starved or intermittently fed ruminants are more susceptible to infection as salmonellae and VTEC O157 can then grow in the rumen. This probably influences the percentage of infected animals on farms during periods of low feed intake (e.g. drought, mustering, shearing or dipping and high stocking densities). On farms, the prevalence of salmonellae in the intestinal tract varies (Edel and Kampelmacher, 1971). Outbreaks of clinical bovine salmonellosis tend to show seasonal patterns. In the UK, most incidents of bovine salmonellosis occur in summer–autumn and peak near the end of the grazing season (Williams, 1975). Peaks of clinical salmonellosis in sheep in New Zealand during summer–autumn have been associated with movement and congregation of sheep for shearing and dipping. In a study of the prevalence of salmonellae in cow–calf operations (Dargatz et al., 2000), of 5 049 fecal samples collected from 187 beef cow–calf operations, salmonellae were recovered from 1 or more
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fecal samples collected on 11.2% (21 of 187) of the operations. Overall 78 salmonellae representing 22 serotypes were isolated from 1.4% (70 of 5 049) of samples, and multiple serotypes from eight samples from a single operation. The five most common serotypes were S. Oranienburg (21.8% of isolates) and S. Cerro (21.8%), followed by S. Anatum (10.3%), S. Bredeney (9.0%) and S. Mbandaka (5.1%). Although it is broadly accepted that human salmonellosis is derived from foods, especially meat and poultry, firm proof is elusive. Sarwari et al. (2001) concluded from US data for 1990–1996, that there was a significant mismatch between the distribution of Salmonella species isolated from animals at the time of slaughter and that of isolates found in humans. This questions the validity of assumptions that raw animal products are the primary source for human salmonellosis, or whether there are methodological reasons for the difference. The increased susceptibility to infection resulting from changes in the rumen can also affect the prevalence of salmonellae in cattle and sheep during transport from farm to slaughter, or in long transport from farm to farm when feeding patterns and type of feed are changed. Frost et al. (1988) reported a high prevalence of salmonellae in the mesenteric lymph nodes and rumen fluid of adult cattle during the first 18 days of entering a feed-lot from a market. After 80 days in the feed-lot, there was little evidence of salmonellae infection. Some of the deaths of sheep during sea-shipment from Australia to Singapore and the Middle East have been due to salmonellosis, which was associated with empty gastrointestinal tracts, loss of appetite and poor adjustment from grazing green pastures to dry feed. Although healthy cattle may excrete thermophilic campylobacters in their feces, numbers are generally low (NACMCF, 1995). While thermophilic campylobacters are frequently found in the lower intestinal tract of ruminants (prevalence range 0–54%), it is usually present in numbers 50% of the spoilage flora with Ps. fragi (clusters 1 and 2), Ps. lundensis and Ps. fluorescens being the most important species. Broch. thermosphacta and psychrotrophic Enterobacteriaceae usually form only a small proportion of the spoilage flora but appear to be more prevalent on the fat surfaces of sheep and pork. Storage at 5◦ C rather than at 0–1◦ C tends to favor their growth (Dainty and Mackey, 1992). At high ambient storage temperatures (25–30◦ C), Enterobacteriaceae and Acinetobacter spp. dominate the spoilage flora (Gill and Newton, 1980; Rao and Sreenivasamurthy, 1985). When storage has caused the surfaces to remain dry, colonies of micrococci, yeasts, and molds may appear. Growth is uneven over the carcass mostly owing to variations in surface aw . Limited information on the bacterial flora of horses and goats has been reported (Cantoni, 1977; Sinha and Mandar, 1977). D Pathogens Salmonella. The prevalence of salmonellae on beef, sheep, and pig carcasses varies widely. Sometimes salmonellae are rarely found (Biemuller et al., 1973). Sometimes they can be found on close to half of the carcasses (Oosterom and Notermans, 1983), and at other times on all carcasses from a herd (Grau and Smith, 1974). In a large survey in the United States, salmonellae were found on 1% of excised 25 g samples of brisket from 3 075 chilled carcasses of steers, heifers, bulls, and cows and on 5% of samples from 397 calves (Hogue et al., 1993). A more recent US survey (Tables 1.15 and 1.16), also detected salmonellae on 1% of samples excised from chilled steer and heifer carcasses (USDA, 1994). In Canada, salmonellae were detected on 11.2% of 596 pork carcasses, on 4.1% of 267 veal and on 1.7% of 666 beef carcasses when neck muscle samples, excised from carcasses before chilling, were examined (Lammerding et al., 1988). Contamination rates for animals in Eygptian abattoirs were: buffalos 1–2% (Lotfi and Kamel, 1964; El Moula, 1978); camels up to 44% (El Moula, 1978); sheep 3–4% (Lotfi and Kamel, 1964); a wide range of serotypes were found. The extent of carcass contamination is strongly influenced by the prevalence and concentration of salmonellae in the intestinal tract and, for sheep and cattle, by the contamination of the fleece and hide. It is also influenced by the care taken in slaughter and dressing. The salmonellae status of animals at slaughter is determined by contamination acquired at the farm and by holding conditions before slaughter. Salmonellae can be found in the internal tissues of liver and spleen from apparently normal animals (Tables 1.6 and 1.7). Normally, only small numbers of salmonellae are on carcass or offal meats. However, inadequate chilling, storage or transport, at temperatures above about 7◦ C, can permit growth. Outbreaks of salmonellosis can follow from inadequate cooking, mishandling, and recontamination. Raw meats can act as a source of cross-contamination of cooked meats, or other foods, in the kitchen or in meat processing plants. Escherichia coli O157:H7. Generally a small percentage of cattle carry EHEC O157:H7 in the intestinal tract at slaughter (Table 1.4), but occasionally the percentage is high. Care taken during evisceration and hide removal can limit, but not entirely prevent, contamination of the carcass. Growth of the organism can occur if chilling, storage or transport conditions of the carcass are inadequate (temperature above about 7◦ C). Inadequately cooked ground beef, contaminated with E. coli O157:H7, has caused a number of outbreaks of bloody diarrhea (HC) and hemolytic uraemic syndrome (Doyle, 1991; Griffin
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and Tauxe, 1991). Cooking hamburgers to an internal temperature of 68◦ C has been recommended (Meng et al., 1994). Undercooking of ground beef or hamburger patties is a common cause of outbreaks attributed to E. coli O157:H7. A large outbreak in the United States (1993) affected 732 people, undercooked hamburgers were the cause. Ground beef has also been identified as carrying E. coli O157, published prevalences varying from 0 (Willshaw et al., 1993; Lindqvist et al., 1998; Tarr et al., 1999) to 0.7 (Doyle and Schoeni, 1987), 1.3% (Kim and Doyle, 1992) and 2.4% (Sekla et al., 1990). Quantitative analysis of some of the positive lots conducted by FSIS and CDC resulted in MPN values in the range of 1–4 cfu/g, with a single high value of 15 cfu/g (FSIS, 1993). In an Argentine study 11 E. coli O157:H7 isolates were detected in 6 (4%) out of 160 ground beef samples produced directly by retailers from different combinations of cuts and trimming of boneless beef (Chinen et al., 2001). In the same study, 4 (8%) out of 83 fresh sausages were positive for E. coli O157:H7. In a Swiss study, a total of 400 minced meat samples from 240 small butcheries were collected and analyzed for the presence of STEC and L. monocytogenes (Fantelli and Stephan, 2001). The samples comprised 211 samples of minced beef and 189 samples of minced pork. STEC was isolated from 7/400 (1.75%) samples. In particular, 5/211 (2.3%) minced beef samples and 2/189 (1%) minced pork samples were contaminated. Serotyping of the seven strains yielded five different serotypes, but none of the strains was O157:H7. Two STEC strains harbored stx1 and stx2 and five strains harbored stx2c genes. Furthermore, four strains harbored one or more additional virulence factors. However, none of the strains was positive for eae. L. monocytogenes was isolated from 43/400 (10.75%) samples. Nineteen of the 43 strains belonged to serotype 1/2a, two to serotype 1/2b, 12 to serotype 1/2c, and 10 to 4b. Forty-two strains harbored the Lhly and 43 strains the plcA genes. Macrorestriction analysis of the L. monocytogenes strains using SmaI yielded 12 different PFGE-patterns. The predominating pattern G was associated to the serotype 1/2c. Ground beef patties inoculated with ca. 106 E. coli O157:H7 and frozen at −20◦ C for 24 h and then thawed at 4◦ C for 12 h, at 23◦ C for 3 h, or using microwave heating for 120 s at 700 W, showed variable destruction depending upon the strain, the recovery method and the thawing regimen (Sage and Ingham, 1998). Podolak et al. (1995) reported fumaric acid (1% and 1.5%) to be more effective than 1% lactic or acetic acid in reducing populations of E. coli O157:H7 in vacuum-packaged ground beef patties. According to guidelines of the UK Advisory Committee on the Microbiological Safety of Food (1995), however, target/temperature of 70◦ C for 2 min is recommended to ensure safety of minced meat products. Campylobacter jejuni. After slaughter, thermophilic campylobacters have been found from 19% to 70% of sheep carcasses, from 2% to 32% of adult cattle carcasses and from 20% to 97% of calf carcasses. Thermophilic campylobacters (mostly C. coli) have been found on 20–60% of pork carcasses. In a Canadian survey (Lammerding et al., 1988), campylobacters were found on 12% of pork, 15% of beef, and 35% of beef neck samples taken from carcasses before chilling. Fecal samples from 94 dairy cows and 42 calves in three different herds were examined by a variety of techniques for campylobacters (Atabay and Corry, 1998). Seventy-nine percent of cattle in herd A carried campylobacters, 40% in herd B and 37.5% in herd C. Most animals carried only one species of Campylobacter: C. hyointestinalis was isolated most frequently (32% animals positive) with C. fetus subsp. fetus detected in 11% of animals and C. jejuni subsp. jejuni 7%. In addition, a novel biotype of C. sputorum was isolated from 60% of 47 cows tested in herd A. During carcass chilling, there is a significant reduction in the prevalence and number of viable campylobacters, and, even on originally relatively heavily contaminated carcasses, numbers are usually
