Plants in Human Health and Nutrition Policy (World Review of Nutrition and Dietetics) (v. 91)

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Author: Artemis P. Simopoulos | C. Gopalan

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Plants in Human Health and Nutrition Policy

World Review of Nutrition and Dietetics Vol. 91

Series Editor

Artemis P. Simopoulos The Center for Genetics, Nutrition and Health, Washington, D.C., USA Advisory Board Regina C. Casper USA Ji Di Chen China Claudio Galli Italy Uri Goldbourt Israel C. Gopalan India Tomohito Hamazaki Japan Michel de Lorgeril France

Victor A. Rogozkin Russia Leonard Storlien Sweden Ricardo Uauy-Dagach Chile Antonio Velazquez Mexico Mark L. Wahlqvist Australia Paul Walter Switzerland Bruce A. Watkins USA

Plants in Human Health and Nutrition Policy

Volume Editors

Artemis P. Simopoulos The Center for Genetics, Nutrition and Health, Washington, D.C., USA

C. Gopalan Nutrition Foundation of India, New Delhi, India

15 figures, 12 in color, and 40 tables, 2003

Basel · Freiburg · Paris · London · New York · Bangalore · Bangkok · Singapore · Tokyo · Sydney

Artemis P. Simopoulos

C. Gopalan

The Center for Genetics, Nutrition and Health Washington, D.C. (USA)

Nutrition Foundation of India New Delhi (India)

Library of Congress Cataloging-in-Publication Data (CIP-Code is available from the Library of Congress on request)

Bibliographic Indices. This publication is listed in bibliographic services, including Current Contents® and Index Medicus. Drug Dosage. The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any change in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug. All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher. © Copyright 2003 by S. Karger AG, P.O. Box, CH–4009 Basel (Switzerland) www.karger.com Printed in Switzerland on acid-free paper by Reinhardt Druck, Basel ISSN 0084–2230 ISBN 3–8055–7554–8

Contents

VII Preface 1 Nutritional Composition of Molokhia (Corchorus olitorius) and Stamnagathi (Cichorium spinosum) Zeghichi, S.; Kallithraka, S. (Crete); Simopoulos, A.P. (Washington, D.C.) 22 Nutritional Composition of Selected Wild Plants in the Diet of Crete Zeghichi, S; Kallithraka, S. (Crete); Simopoulos, A.P. (Washington, D.C.); Kypriotakis, Z. (Iraklio, Crete) 41 Kanjero (Digera arvensis) and Drumstick Leaves (Moringa oleifera): Nutrient Profile and Potential for Human Consumption Seshadri, S.; Nambiar, V.S. (Vadodara) 60 Ivy Gourd (Coccinia grandis Voigt, Coccinia cordifolia, Coccinia indica) in Human Nutrition and Traditional Applications Wasantwisut, E.; Viriyapanich, T. (Nakhon Pathom) 67 Acerola (Malpighia glabra L., M. punicifolia L., M. emarginata D.C.): Agriculture, Production and Nutrition Johnson, P.D. (Lakeview, Calif.) 76 Food-Based Approaches to Prevent and Control Micronutrient Malnutrition: Scientific Evidence and Policy Implications Gopalan, C.; Tamber, B. (New Delhi) 132 Author Index 133 Subject Index

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Preface

This volume on Plants in Human Health and Nutrition Policy is the third volume in the series of World Review of Nutrition and Dietetics on the contribution of wild plants to human health and the metabolic consequences of changing dietary patterns [1, 2]. Consumption of fruits and vegetables has been associated with protection against various diseases, including cardiovascular, cerebrovascular disease and cancer. It is not known for certain what active dietary constituents contribute to the beneficial effects, but it is often assumed that antioxidant nutrients contribute to this defense. Results from intervention trials on the protective effect of the supplementation with antioxidants such as ␤-carotene and vitamin E are not conclusive. Therefore, the beneficial effect of a high intake of fruits and vegetables on the risk of cardiovascular disease and cancer may rely not on the effect of the well-characterized antioxidants, such as vitamin E and C and ␤-carotene, but rather on some other antioxidants or non-antioxidant phytochemicals or by an additive action of different compounds present in foods such as ␣-linolenic acid, various phenolic compounds and fiber. Various methods have been developed to measure total antioxidant capacity or activity, such as the oxygen radical absorbance assay (ORAC), or the 2,2-diphenyl-1-picrylhydrazyl (DPPH•) free radical assay which measures the antiradical power (ARP): the higher the ARP, the more efficient the antioxidant. In general, more than 80% of the total antioxidant capacity in fruits and vegetables comes from ingredients other than vitamin C, indicating the presence of other potentially important antioxidants in these foods. ORAC varies considerably (20- to 30-fold) from one kind of fruit or vegetable to another.

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As expected, the majority of studies have been carried out in cultivated fruits and vegetables. Brussel sprouts are one of the vegetables that show high ORAC activity. Garlic, kale and spinach are particularly high, as are strawberries and plums. Flavonoids and other phenolic compounds appear to be antioxidants that contribute to the high antioxidant capacity observed in certain fruits and vegetables. There are several thousand different flavonoids present in plants, and many of them have antioxidant activities. The antioxidant capacities, measured as ORAC of some flavonoids, were found to be several times stronger on the basis of molar concentration than vitamins E and C. Such phenolic compounds have already been implicated as playing a role in the protection that fruits and vegetables have against chronic diseases. But the extent to which these potentially important antioxidants can be absorbed is not clear, although early evidence indicates that substantial quantities of the flavonoids are absorbed. For example, absorption of quercetin (a common flavonoid) defined as oral intake minus ileostomy excretion and corrected for degradation within the ileostomy bag was 52 ⫾ 15% for quercetin glucerides from onions. The importance of the antioxidant and ␣-linolenic constituents of plant materials in the maintenance of health and protection from coronary heart disease and cancer is raising interest among scientists, physicians, food manufacturers and consumers as the trend of the future is moving towards functional foods with specific health effects. Flavonoids and other phenolics have been suggested to play a preventive role in the development of cancer and coronary heart disease. Ingestion of alcohol-free red wine or a phenolic compound mixture extracted from red wine has been shown to improve the antioxidant status of plasma in humans. The antioxidant activity of phenolics is mainly due to their redox properties, which allow them to act as reducing agents, hydrogen donors and singlet oxygen quenchers. They also have a metal chelation potential. In addition to their antioxidant activities, wild plants are also storehouses of essential fatty acids – especially ␣-linolenic acid – and micronutrients such as calcium, phosphorus, potassium, magnesium, zinc, copper and iron. In developing countries, micronutrient deficiencies are a significant health problem, particularly for maternal, infant and child health. The use of indigenous green leafy vegetables has been used to correct these deficiencies with great success. The chapters in this volume provide scientific evidence for the important contributions to health of wild plants for both developed and developing countries. The antioxidant components contribute to decreased risk for chronic diseases and the micronutrients to decreased risk for nutritional deficiencies. Implementation of scientific discoveries is an essential component in improving nutrition policy. The first five chapters provide data on the nutritional composition of indigenous plants from Crete (Greece) and North Africa, India, Thailand,

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and Central, South America and the Caribbean. The sixth chapter is on nutrition policy to combat micronutrient deficiency through indigenous foods instead of synthetic vitamins. In the last two decades a number of scientists have studied the composition of wild plants as good sources of natural antioxidants, because of a trend towards natural ingredients in food. It was therefore important to investigate the antioxidant and ␻–3 fatty acid composition of diets such as the diet of Crete that has been shown to be associated with a decreased rate of cardiovascular disease and cancer. Wild plants have contributed to the diet of both humans and animals since their first appearance on planet Earth. Human beings ate a variety of wild plants, whereas today the diet of developed societies is limited to a few cultivated vegetables. However, Mediterranean diets and in particular the diet of Crete is rich in edible wild plants. This diet may be a reference standard for modern human nutrition and a model for defense against certain diseases of affluence. The first chapter on ‘Nutritional Composition of Molokhia (Corchorus olitorius) and Stamnagathi (Cichorium spinosum)’ by Zeghichi, Kallithraka and Simopoulos describes the nutritional composition of molokhia (C. olitorius), a commonly eaten wild cultivated plant in North Africa and the Middle East, and stamnagathi (C. spinosum), an edible wild plant indigenous to Crete. Antioxidants (vitamin C, ␤-carotene, ␣-tocopherol, glutathione and phenols), antioxidant activity, minerals (K, Na, Ca, Mg, Fe, Cu, Mn, Zn and P) and fatty acid composition were determined during plant growth. The seeds were harvested from wild plants and grown in the green house at 25⬚C. Leaves were harvested for extraction every 5 or 10 days. The results showed that both plants contained considerable amounts of antioxidants especially molokhia, which reached levels of 77.42 and 14.89, and 38 mg/100 g wet weight of vitamin C, ␣-tocopherol and phenols respectively. The glutathione content also increased during leaf development (12.52 and 13.77 mg/100 g wet weight for molokhia and stamnagathi respectively). In addition, molokhia is rich in Ca, Cu and Mn while stamanagathi is a source of Fe, Zn, K and Mg. Both plants contained ␣-linolenic acid in moderate quantities (62.14 mg/100 g wet weight for molokhia and 44.4 mg/100 g wet weight for stamnagathi). These two plants are easy to grow and could be part of agricultural development. The second chapter on the ‘Nutritional Composition of Selected Wild Plants in the Diet of Crete’ by Zeghichi, Kallithraka, Simopoulos and Kypriotakis describes the nutritional composition of 25 most common edible wild plants in Crete. ␣-Tocopherol, total phenols, nitrates and minerals (K, Na, Ca, Mg, Fe, Cu, Mn, Zn and P) as well as total antioxidant activity were determined. The plants were harvested from the wild fields from Heraklio in the North of Crete, Greece. The results showed that all the plants contained considerable amounts of antioxidants and minerals. Of particular interest is the nutritional composition of the

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algae, Stypocaulon scoparium. The ␣-tocopherol content could not be detected and the phenols were low, but the algae had one of the highest antioxidant activities, indicating the presence of other antioxidants. Furthermore, it had the highest amounts of potassium, sodium, calcium and magnesium. This group of the 25 most commonly eaten wild plants provides all the necessary micronutrients in more than adequate amounts, whereas the micronutrient content of the cultivated plants has decreased significantly over the last 50–70 years. There is evidence from other studies that the nutrient content of our food supply is decreasing. Mayer compared the mineral content of 20 fruits and 20 vegetables from 1936 to the 1980s, using a special methodology to ensure that comparable laboratory methods were employed. Over that 50-year period, there were statistically significant decreases of calcium, magnesium, copper and sodium in vegetables, and of manganese, iron, copper and potassium in fruits. Zinc was not studied. The magnitude of some changes was large: the copper level in vegetables in the 1980s was less than 20% of the 1936 levels. Mayer attributed these changes to the fact that agriculture relies on fertilizers containing only nitrogen, phosphorous and potassium, and there is little effort to remineralize the soil over the decades. It is important to identify vegetable foods of high value such as leafy greens that are native to a region and establish their nutritional profile. This is particularly relevant to tribal belts of India where a variety of leafy vegetables are grown for household consumption in their backyards or they are picked from the wild, but these are not commercially exploited, as they are not sold in the market. The leaves could well be a repository of important microconstituents that can provide nutritional support and optimize health and wellbeing with a potential for world agriculture. The third chapter on ‘Kanjero (Digera arvensis) and Drumstick Leaves (Moringa oleifera): Nutrient Profile and Potential for Human Consumption’ is by Seshardri and Nambiar. The authors present their study on the nutritional composition of the green leaves of kanjero and drumstick, and their use in increasing the vitamin A content of the diet. The intervention study showed that the bioavailability of ␤-carotene from fresh and dehydrated drumstick leaves compared favorably with the bioavailability of synthetic vitamin A. These results support the hypothesis that plant sources are effective in correcting vitamin A deficiency. Overall, drumstick leaves emerged as superior, containing the highest level of the two antioxidant nutrients, ␤-carotene and ascorbic acid, and as well as having the highest level of carotenoid pigments compared to either kanjero or the commonly consumed leafy vegetables such as spinach or fenugreek leaves. Drumstick leaves also had the highest level of ascorbic acid. The distribution of flavonoids, phenolic acids, saponins and steroids in kanjero and drumstick leaves show that the flavonoids of kanjero species are quercetin and the major phenolic acids are vanillic and syringic acid.

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The fourth chapter is on ‘Ivy Gourd (Coccinia grandis Voigt, Coccinia cordifolia, Coccinia indica) in Human Nutrition and Traditional Applications’ by Wasantwisut and Viriyapanich. In Thailand, ivy gourd is a common vegetable in the village setting, whereas in Western Australia, the Pacific Islands and Hawaii, ivy gourd is labeled as a common weed or invasive weed, which is destroyed. Ivy gourd is rich in ␤-carotene, a major precursor of vitamin A from plant sources, also a good source of protein, fiber and a moderate source of calcium, and compares well to other commonly eaten vegetables, i.e., Chinese cabbage, amaranth, kale, pumpkin leaves and chayote leaves. In many developing countries where vitamin A deficiency is prevalent, the population depends primarily on plant sources to obtain vitamin A from their diet. In Thailand, because ivy gourd is rich in ␤-carotene, readily acceptable for consumption by all age groups, inexpensive as well as accessible to the village households, this plant was selected in several studies to demonstrate an effect of dietary intervention to improve vitamin A nutrition. The fifth chapter is on ‘Acerola (Malpighia glabra L., M. punicifolia L., M. emarginata D.C.): Agriculture, Production and Nutrition’ by Johnson. Acerola has been known historically as a concentrated source of natural ascorbic acid. Juice from acerola cherries is useful for fortifying the ascorbic acid content of other fruit juices. It has been used as a commercial source of vitamin C in dietary supplements as well as other food products. A shrub or small tree has been cultivated as an ornamental in subtropical areas where it flowers from April to November. Ascorbic acid from natural sources such as acerola is more readily absorbed by the human body than that which is synthetically produced. The vitamin C of acerola powder was found to be 1.63 times more bioavailable to humans in a double-blind study than USP vitamin C. In addition to ascorbic acid, acerola is a source of vitamin A, iron, calcium, potassium and vitamin B, and enhances the antioxidant activity of other botanical extracts, i.e. in the presence of acerola cherry extract, soy and alfalfa phytoestrogen extracts prevent the oxidation of LDL. The vitamin C content of the fresh fruit begins to decrease as soon as 4 h after harvest. The uniquely high vitamin C content of the acerola, in addition to its many potential uses for processed acerola products, make this plant valuable for further utilization in food products. Since much of the nutritional value of acerola fruits can be ‘fixed’ through a variety of processing methods, the acerola continues to be of great value when prepared as single-entity products or when combined as a healthy additive to multi-ingredient blends. Research into other health benefits offered by acerola (in addition to vitamin C supplementation) indicate that the use of botanical products offers potentially superior results when compared to the use of isolated synthetic compounds. The limited market potential of fresh acerola fruit presents opportunities for the development of

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varieties, cultivation and harvest practices, as well as storage and handling methods that can improve the characteristics of the fresh fruit. The pleasant taste of ripe acerola, in addition to health benefits derived from its consumption, make fresh acerola a worthy challenge for the agricultural community. Because wild plants supply a significant portion of micronutrients to the diet and exhibit higher mineral values than more accessible, cultivated alternatives, substantial economic and nutritional gains could be achieved by increasing dietary utilization of edible wild plants. However, lack of compositional data continues to be a limiting factor when attempting to evaluate the role of wild food plants in contemporary diets. Edible wild plants are part of agricultural systems in Africa, Asia, Australia, the Americas or Europe. Agricultural development should not be at the expense of nutritional quality of the human diet where edible wild species play critical roles. The nutritional quality of diet may decline with agricultural development unless edible wild species that provide essential micronutrients to the diet are considered part of the total food system. We and others have documented that some edible wild plants not only augment the human diet, but that the nutritional content of some wild species is superior in vitamin and mineral content to widely raised domesticated field crops. Furthermore, edible wild plants are regular components of the diets of millions of people and scientists over the past 50 years have continued to stress the importance of edible wild plants as part of the human diet. Gopalan and Tamber, in their chapter on ‘Food-Based Approaches to Prevent and Control Micronutrient Malnutrition: Scientific Evidence and Policy Implications’, emphasize biodiversity and the optimal use of plants to combat micronutrient deficiency. It is indeed possible that micronutrient deficiencies are often the result of lack of enough habitual food in the household rather than to the poor quality of such foods. Drs. Gopalan and Tamber provide good argument that a food-based rather than drug-based approach will be the proper answer to the problem of micronutrient deficiencies as indeed to the problem of undernutrition in general. In light of modern knowledge, vegetables, fruits and nuts have emerged as the food items which could address multiple problems at both ends of the socioeconomic spectrum. Vegetables, fruits and nuts can provide the ‘micronutrients’ usually deficient in the diets of poor communities. They can also provide the ‘phytonutrients’ which help to combat the chronic diseases of the affluent. The promotion of consumption of vegetables, including green leafy vegetables and fruits in adequate quantities (450 g), must become a central part of the strategy for nutritional improvement of all populations. From available data it may be reasonable to argue that in a healthy state a dynamic equilibrium among different micronutrients is achieved. The actual amounts of different micronutrients involved in the establishment of this equilibrium may not be

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identical and may vary with different population groups with their overall dietary patterns. Drs. Gopalan and Tamber conclude that if the type of attention that was devoted to the improvement of wheat and rice with respect to yield, protein content and disease resistance in the wake of the Green Revolution is now devoted to the improvement of micronutrient content of plant foods, the results could be truly rewarding. They recommend: ‘Plant breeding strategies directed towards: (i) increasing the concentration of minerals (iron and zinc) and vitamins (␤-carotene); (ii) reducing the amount of antinutrients such as phytic acid, and (iii) raising the sulphur containing foods which can promote the absorption of zinc, also offer possibilities of augmentation of production of micronutrient rich foods. ‘International agencies will be rendering real service to developing countries by strongly propagating ways by which the bioavailability of micronutrients from horticulture plant foods available at their door steps can be improved by: 1. Improved cooking and processing procedures 2. Better preservation techniques that could increase availability throughout the year 3. Home-processing techniques to reduce inhibitors of absorption 4. Simple methods of achieving enzymatic hydrolysis of phytates in cereals and legumes through fermentation and germination 5. Promoting non-enzymatic methods of reducing phytic acid content 6. Invoking home processing techniques like malting, avoidance of drinking of tea and coffee with the meal, reducing the use of tamarind (rich source of tamarind) as a souring agent and instead use tomato or lime juice, in order to facilitate non-haeme iron absorption.’ Plants in Human Health and Nutrition Policy should be of interest to those involved in food production, industrial and agricultural development, and sustainable agriculture, including scientists who are students of human evolution and development. Specifically, botanists, experimental biologists, agronomists, food technologists, nutritionists, pharmacologists, physicians, economists, policy-makers and anthropologists will discover their collective contribution in furthering human health and sustainable agriculture, and having a positive impact on the environment. Artemis P. Simopoulos, MD

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Simopoulos AP: Plants in Human Nutrition. World Rev Nutr Diet. Basel, Karger, 1995, vol 77. Simopoulos AP: Metabolic Consequences of Changing Dietary Patterns. World Rev Nutr Diet Basel, Karger, 1996, vol. 79.

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Simopoulos AP, Gopalan C (eds): Plants in Human Health and Nutrition Policy. World Rev Nutr Diet. Basel, Karger, 2003, vol 91, pp 1–21

Nutritional Composition of Molokhia (Corchorus olitorius) and Stamnagathi (Cichorium spinosum) Sabrina Zeghichi a, Stamatina Kallithrakaa, Artemis P. Simopoulosb a b

Mediterranean Agronomic Institute of Chania, Crete, Greece and The Center for Genetics, Nutrition and Health, Washington, D.C., USA

Introduction

The Mediterranean basin contains approximately 25,000 plant species, about half of which are endemic to the region, and is one of the world’s major centers of plant diversity [1]. Wild plants have always been significant in all cultures of the Mediterranean region, being used not only for food but also for medicinal purposes, fuel and many other uses [1]. Egyptians, Greeks and Romans were familiar with many wild plants and were aware of their usefulness in food and nutrition, and in the treatment of various diseases. The writings in the temples and in the papyri revealed that ancient Greeks and Egyptians used herbs and plants for food, medicinal and other purposes. Wild plants are rich sources of antioxidants and ␻–3 fatty acids [2]. Recent evidence has underlined the importance of plant foods. Diets rich in fruits and vegetables are associated consistently with reduced risk of a variety of cancers, coronary heart disease, diabetes, osteoporosis and gastrointestinal disorders [2–5]. In the last two decades, emphasis has been given to natural antioxidants because of a trend toward natural ingredients in foods. Antioxidants quench free radicals in the human body, which may lead to the protection from chronic diseases [6]. Free radicals are believed to play a role in more than 60 different health conditions, including the aging process, cancer and atherosclerosis [5]. Reducing exposure to free radicals and increasing intake of antioxidant nutrients may reduce the risk of free radical-related health problems [2, 5].

A variety of antioxidant enzymes (such as superoxide dismutase, catalase and glutathione peroxidase), and antioxidants (vitamin C, vitamin E, ␤-carotene, lutein, lycopene, vitamin B3 and vitamin B6) may be the best way to provide the body with the most complete protection against free radical damage [5]. However, the consequences of dietary intake of these antioxidants are difficult to separate by epidemiological studies from other important constituents in plants such as flavonoids [3]. Flavonoids include flavones, flavonols, flavonones as well as derivatives and conjugates thereof [7]. Many of these phenols have been found to be more powerful antioxidants than vitamin C, vitamin E and ␤-carotene using an in vitro model for heart disease, namely the oxidation of low-density lipoproteins (LDL) [8]. Thus, plant consumption may provide protection against oxidative stress that is a pathogenic mechanism of both carcinogenesis and atherosclerosis [4, 5]. In addition, over the past 15 years a number of animal experiments, epidemiological investigations and double-blind controlled clinical trials have confirmed the essentiality of ␻–3 fatty acids, particularly docosahexaenoic acid (DHA) for normal retina and brain development of the premature infant, and for its hypotriglyceridemic, anti-inflammatory, and antithrombotic properties [9, 10]. Most of the studies have been carried out with fish oils (eicosapentaenoic acid (EPA) and DHA). However, ␣-linolenic acid (ALA), found in green leafy vegetables, flaxseed, rapeseed and walnuts, desaturates and elongates in the human body to EPA and DHA and by itself may have beneficial effects in health and in the control of chronic diseases [9]. Indu and Ghafoorunissa [11] were able to show antithrombotic effects by reducing the ratio of ␻–6 to ␻–3 fatty acids with ALA-rich vegetable oils. After supplementation with ALA there was an increase in long-chain ␻–3 polyunsaturated fatty acids (PUFA) in plasma and a decrease in platelet aggregation. ALA intake is associated with inhibitory effects in the clotting activity of platelets, in their response to thrombin [12] and in the modulation of arachidonic acid metabolism [13]. The Lyon Diet Heart Study clearly showed that adopting a modified Cretan Mediterranean-type diet reduced the incidence of sudden cardiac death and total death significantly by 50–70% at 5 years of follow-up [14]. The experimental modified diet of Crete was low in saturated and ␻–6 fatty acids but rich in oleic acid, ␻–3 fatty acids, fiber, group B vitamins, and various antioxidants including vitamin C, vitamin E, trace elements and flavonoids. A study comparing the fatty acid composition of serum cholesterol esters in subjects in Crete (Greece) and Zutphen (The Netherlands) reported that the Cretans had higher concentrations of 18:1␻–9, much lower concentrations of linoleic acid (LA) and unexpectedly high concentrations of ALA [15]. ALA in the Cretan diet comes from eating purslane (Portulaca oleracea), walnuts and other

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wild green leafy plants. Similarly, the population of Kohama Island, Japan, which has the longest life expectancy in the world and the lowest coronary heart disease mortality rate, has high concentrations of plasma ALA [16]. In Japan, the dietary sources of ALA are mainly canola and soybean oils. Thus, the two populations documented to have the greatest life expectancies in the world (Japanese and Cretans) both appear to have high intakes of ALA. The dietary ratio of LA to ALA in the de Lorgeril and Salen [14] trial was 4:1. This ratio permits the desaturation and elongation from ALA to 20:5␻3, as shown by Indu and Ghafoorunissa [11]. Minerals are inorganic elements needed in small amounts to assist in a variety of essential body functions. The best food sources of minerals are fruits, vegetables, meat, fish, milk, eggs, cereals and water. Many minerals are components of important molecules, such as hemoglobin, vitamins, hormones and enzymes. Some of them are required for the normal functioning of nerves and muscles. They regulate the acid-base balance of body fluids and they form a structural part of bone and cartilage [17, 18]. It was therefore important to investigate the antioxidant and ␻–3 fatty acid composition of diets, such as the diet of Crete that has been shown to be associated with a decreased rate of cardiovascular disease and cancer [19]. Wild plants have contributed to the diet of both humans and animals since their first appearance on planet Earth. Humans used to eat a variety of wild plants, whereas today the diet of developed societies is limited to a few cultivated vegetables. However, Mediterranean diets, and in particular the diet of Crete, are rich in edible wild plants [14, 20]. This diet may be a reference standard for modern human nutrition and a model for defense against certain diseases of affluence [20]. Two widely eaten, wild leafy plants in the Mediterranean region, Corchorus olitorius (molokhia) and Cichorium spinosum (stamnagathi) were chosen to determine macronutrients and their nutritional composition relative to ALA, antioxidant vitamins, glutathione, total phenol concentration, total antioxidant activity and minerals. Molokhia (fig. 1; table 1 for taxonomy) is found in Australia, Algeria, Egypt, Lebanon, Tunisia, Mozambique, Philippines, Senegal, Thailand, Sudan, Afghanistan, India, Kenya, Nepal and Zambia [21]. Molokhia is a popular summer vegetable dish due to its special delicious taste; it is consumed fresh or dried in vegetable soup [22]. It is reported to have demulcent, diuretic, lactagogue, purgative and tonic properties [22]. Molokhia is a folk remedy for aches and pains, and swellings. In addition, the leaves are used for cystitis, dysuria, fever and gonorrhea. The cold infusion is said to restore the appetite and strength. Furthermore, it is an ingredient of facial creams, lotions, hair tonics and hand creams [22]. For Egyptians, molokhia has been for a long time the symbol of their homeland.

Nutritional Composition of Molokhia (C. olitorius) and Stamnagathi (C. spinosum)

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Fig. 1. C. olitorius (molokhia).

Table 1. Taxonomy of C. spinosum (stamnagathi) and C. olitorius (molokhia)

Division Class Order Family Genus Species

C. spinosum

C. olitorius

Spermatophyta Angiospermae Astrales Compositae Cichorium Cichorium spinosum

Tracheophyta Angiospermae Malvales Tiliaceae Corchorus Corchorus olitorius

Stamnagathi (fig. 2) can be found in Spain, Balearic Islands, Italy, Sicily, Southern Greece, Agean islands, Crete and Cyprus [23, 24]. Stamnagathi is consumed as salad (raw), either fresh or boiled in water and served with olive oil and lemon, or cooked in red sauce with lamb. This plant may stimulate appetite. As far as the authors are aware, few studies have reported the nutritive value of molokhia and no data were found concerning stamnagathi. The concentration of fatty acids, antioxidants and minerals can vary with plant growth, age and environmental conditions [3]. If these two plants are to be developed as a commercial crop, it therefore becomes important to optimize nutritional quality in terms of growth stage and time of harvest. Therefore, in this study the


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Fig. 2. C. spinosum (stamnagathi).

fatty acid composition, content of ascorbic acid, ␣-tocopherol, carotenoids, glutathione, total phenol concentration, antioxidant activity and selected mineral concentrations for the above-mentioned plants were determined at four different growth stages. Evaluation of total antioxidant activity also was determined for both plants. Materials and Methods Plant Material and Growth Conditions The study was carried out during the academic year 1998–1999, at the Mediterranean Agronomic Institute of Chania (MAICH), Crete, Greece. The seeds of C. olitorius (molokhia) and C. spinosum (stamnagathi) were harvested from wild plants, were sown in a mixture of peat:vermiculite:perlite (1:1:1) without use of any fertilizers, and grown in the greenhouse under uniform climatic conditions at 24°C. Leaves were harvested for extraction after 30 days of planting and then every 10 days until 60 days. All analyses were done in triplicate.

Determination of Antioxidants Ascorbic Acid Ascorbic acid was determined by the 2,6-dichlorophenol-indophenol method [25]. Ascorbic acid was extracted immediately by the addition of oxalic acid 1% (w/v) (Merck) in order to avoid any oxidation. The samples were homogenized by means of a high-speed blender at 9,000 rpm for 5 min (Microprocessor Cyclone I.Q2 Virtis). The ascorbic acid present in the plant extract reduces the oxide-reduction indicator dye, 2,6-dichlorophenol-indophenol (Sigma), to a colorless solution. The absorbance was read at 518 nm (Hewlett-Packard diode array spectrophotometer model 8452A).


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b-Carotene After separation of the pigments by column chromatography, the ␤-carotene content was determined spectrophotometrically [26]. The fat-soluble pigments were extracted by acetone-hexane solvent (Riedel-Dettaen, Lab Scan). After filtration and separation the extract was chromatographed to remove chlorophyles and hydroxycarotenes using a Silica gel-60 (230–400 mesh ASTM, Merck). The absorbance of the carotenoid extract was determined immediately at 436 nm (Hewlett-Packard diode array spectrophotometer model 8452A). Tocopherols The extraction of tocopherols was performed by percolation using n-hexane (Lab Scan) in a glass column (2.5 ⫻ 50 cm) [27, 28]. Tocopherols were determined by reverse-phase high-performance liquid chromatography analysis [6] (Hewlett-Packard liquid Chromatogram, model 1090, series II). A reversed-phase ODS Hypersil column (RP-18, 250 ⫻ 4 mm, particle size 5 ␮m) and a Li Chrospher 100 (RP-18, 4 ⫻ 4 mm particle size 5 ␮m) guard column were used with a flow rate of 1 ml/min. The mobile phase was methanol/water 96:4 v/v. For better qualitative peak identification of each tocopherol in the samples, and to control the reproducibility of the runs and the precision of the results, ␣-tocopherol acetate (Sigma) was used as an internal standard. Total Glutathione Glutathione is conveniently assayed by an enzymatic recycling procedure [29] in which it is sequentially oxidized by 5,5⬘-dithiobis(2-nitrobenzoic acid) (DTNB) (Sigma) and reduced by NADPH (Sigma) in the presence of glutathione reductase (Sigma). The rate of 2-nitrobenzoic acid formation is monitored at 412 nm (Hewlett-Packard diode array spectrophotometer model 8452A) and the glutathione present is evaluated by comparison with a standard curve. Total Phenols Total phenols were first extracted with methanol 80% containing 1% hydrochloric acid [30], and determined using Folin-Ciocalteu reagent (Merck) [31] the absorbance was measured at 725 nm (Hewlett-Packard diode array spectrophotometer model 8452A). The results were expressed as ␮g/ml (⫹)–catechin (Sigma). Antioxidant Activity The antioxidant activity of the methanolic extracts was determined using DPPH (2,2-diphenyl-1-picrylhydrazyl free radical assay) as a free radical (Sigma) [32]. Antiradical activity was defined as the amount of antioxidant necessary to decrease the initial DPPH• concentration by 50% (efficient concentration ⫽ EC50 (mg antioxidant/mg DPPH•). Five different sample dilutions (1.25, 2.5, 5, 7.5 and 10 mg dry weight/ml) in methanol were prepared for each plant extract. An aliquot of 0.1 ml of the above solutions was added to 3.9 ml of DPPH• solution in methanol (6 ⫻ 10⫺5 M), prepared daily, and vortexed for 30 s. Absorbances at 515 mm (A515 nm) were measured at different time intervals on a HewlettPackard 8452A diode array spectrophotometer until the reaction reached a plateau, in order to find the time needed by the reaction to reach the steady state (Tss). Then, the decrease in the absorbance was recorded until the reaction reached the steady state (Tss ⫽ 4 h).


6

The DPPH• concentration (CDPPH mg/ml) in the reaction medium was calculated (by linear regression, r2 ⫽ 0.9996) from the following calibration curve: A515 nm ⫽ 26.247 CDPPH (mg/ml) ⫹ 6.81 ⫻ 10⫺3 The percentage of remaining DPPH• (%DPPH•

(1)

REM) was determined as follows:

%DPPH• REM ⫽ 100 ⫻ [CDPPH/CDPPH, t⫽0] (2) • • where CDPPH, t⫽0 is the initial DPPH concentration and CDPPH is the DPPH remaining concentration. For each plant extract, the percentages of remaining DPPH at the steady state for the five dilutions were plotted versus the ratio mg dry extract/mg DPPH. The parameter EC50 was calculated graphically, and the AE was determined with following the equation: AE ⫽ 1/EC50. Total Protein Total protein was determined by the Bradford method [33]. The absorption of the binding dye to protein color was read at 595 nm (Hewlett-Packard diode array spectrophotometer model 8452A). Fatty Acids For fatty acid determination, the same extract performed by percolation was used for this purpose. Oils were saponified and the resultant fatty acid mixtures were methylated [34]. The fatty acid methyl esters were analyzed by high-resolution gas chromatograph equipped with flame ionizator detector (FID) (Hewlett-Packard 5890 series II). A capillary column of fused silica of high polarity was used (FFAP 30 m ⫻ 0.25 mm ID; 0.2 ␮m film thickness). Injector temperature 250°C, oven temperature 220⬚C and detector temperature 280°C. Injection volume was 1 ␮l. The quantification of fatty acids was done using the HP 3365 Series II Chemstation software program. Peaks were identified by using standard FAME and quantified by internal standard. Unknown peaks were not considered in further calculations. Determination of Mineral Elements The minerals were determined according to the method Bhattacharjee et al. [35]. The samples were digested with 2% nitric acid and 2% hydrochloric acid. The mineral elements were determined by the inductively coupled plasma technique (Leaman Labs, Inc., Model PS-100080).

Results and Discussion

Ascorbic Acid The content of ascorbic acid in leaf tissue of C. spinosum increased from a minimum level of 17.58 ⫾ 0.11 mg/100 g wet weight at 30 days to a maximum level of 36.58 ⫾ 0.29 mg/100 g wet weight at 50 days of planting. For C. olitorius the ascorbic acid content at 30 days was 30.88 ⫾ 0.15 mg/100 g wet


7

Ascorbic acid ␣-Tocopherol ␤-Carotene Glutathione Total phenols

Antioxidant content (mg/100 g wet weight)

45 40 35 30 25 20 15 10 5 0 30

40 50 Age (days)

60

Fig. 3. Antioxidant content of C. spinosum (stamnagathi) during leaf development.

Ascorbic acid ␣-Tocopherol ␤-Carotene Glutathione Total phenols

80

Antioxidant content (mg/100g wet weight)

70 60 50 40 30 20 10 0 30

40

50

60

Age (days)

Fig. 4. Antioxidant content of C. olitorius (molokhia) during leaf development.

weight, 67.56 ⫾ 0.25 mg/100 g wet weight after 40 days, and then reached the maximum of 77.42 ⫾ 0.19 mg/100 g wet weight after 45 days. Then the ascorbic acid declined for both plants after about 60 days (fig. 3, 4). Wild plants are typically known to have higher levels of vitamin C than cultivated ones [36, 37]. The ascorbic acid content of C. spinosum fell within the range previously reported for other weed species [38–41] and wild vegetable foods consumed by Australian Aboriginals [37]. Ascorbic acid was


8

present in significantly greater amounts in C. olitorius relative to C. spinosum, purslane (26.6 ⫾ 0.8 mg/100 g wet weight), spinach (21.7 ⫾ 0.5 mg/100 g wet weight) [2] and some other vegetables such as green onion (32 mg/100 g wet weight), leaf lettuce (18 mg/100 g wet weight), celery (9 mg/100 g wet weight), orange (50 mg/100 g wet weight) and tomatoes (23 mg/100 g wet weight) [38]. a-Tocopherol The amount of ␣-tocopherol increased from a minimum of 4.30 ⫾ 0.07 mg/100 g wet weight and reached a maximum of 9.78 ⫾ 0.05 mg/100 g wet weight at 40 days for C. spinosum. Concerning C. olitorius, ␣-tocopherol content increased from 9.14 ⫾ 0.03 at 30 days to the highest level of 14.89 ⫾ 0.05 mg/100 g wet weight at 50 days (fig. 3, 4). The levels of ␣-tocopherol found in C. spinosum and C. olitorius are up to ten times higher than has been previously recorded in other wild plants [42]. However, these levels were not significantly different compared to purslane; 12.2 ⫾ 0.4 mg/100 g wet weight [2]. ␣-Tocopherol is present in the chloroplasts together with chlorophyll and it is the chlorophyll protector agent. It is also known that the ␣-tocopherol biosynthesis takes place inside the chloroplast membranes of the plant [43]. Other studies have also reported the presence of ␣-tocopherol in some Mediterranean plants [6, 27, 28]. b-Carotene As shown in figures 3 and 4, the content of ␤-carotene in C. spinosum remained stable between 30 and 60 days (2.24 ⫾ 0.01 to 2.66 ⫾ 0.02 mg/100 g wet weight respectively), contrary to C. olitorius where it showed an increase from 2.23 ⫾ 0.05 mg/100 g wet weight at 30 days to a maximum of 5.44 ⫾ 0.02 mg/100 g wet weight at 50 days. In photosynthetic tissues of higher plants, ␤-carotene and other carotenoids are localized in chloroplasts; while there is little qualitative difference in the pigments present, there is considerable quantitative variation between different species [44]. The levels of ␤-carotene of C. spinosum were not significantly different in comparison to wild purslane (2.2 ⫾ 0.1 mg/100 g wet weight) [2], but were lower than those present in C. olitorius. However, these results were higher than those reported for celery (0.5 mg/100 g wet weight), lettuce (0.2 mg/100 g wet weight) green onion (1.25 mg/100 g wet weight) [33] and spinach (3.3 mg/100 g wet weight) [2]. Glutathione As shown in figures 3 and 4, the levels of glutathione increased significantly for both plants during the 60 days of plant harvesting from 8.22 ⫾ 0.06 mg/100 g wet weight for C. spinosum and 8.15 ⫾ 0.06 mg/100 g wet


9

weight for C. olitorius to higher levels at 60 days: 13.77 ⫾ 0.46 mg/100 g wet weight and 12.52 ⫾ 0.16 mg/100 g wet weight respectively. Dietary glutathione occurs in highest amounts in fresh meat, in moderate amounts in some fruits and vegetables, whereas it is absent or found only in small amounts in grains and dairy products [45]. In a study carried out to determine the glutathione content of 98 food items, identified by the National Cancer Institute [45], only fresh asparagus (28.3 mg/100 g) and fresh avocado (27.7 mg/100 g) were higher in glutathione content than molokhia and stamnagathi. In addition, chamber-grown as well as wild purslane were found to contain similar amounts of glutathione (14.81 ⫾ 0.28 and 11.9 ⫾ 0.63 mg/100 g wet weight respectively) [2]. Considerable variations in levels of glutathione have been reported by different studies recording thiol levels in a variety of plant species due to the use of different analytical techniques, and because glutathione levels vary both diurnally [46, 47] and with developmental and environmental factors [48]. The highest level of glutathione found in both stamnagathi and molokhia was in the range of those reported for other plant species. Total Phenols Figures 3 and 4 show the amount of total phenols expressed as mg (⫹)–catechin/100 g wet weight increased from 16.31 ⫾ 0.01 to a maximum level of 20.31 ⫾ 0.05 after 50 days for C. spinosum. Concerning C. olitorius, total phenol content reached the highest amount of 38 ⫾ 0.08 mg/100 g wet weight after 40 days of planting. Phenols are large compounds that occur ubiquitously in food plants. They are found to be strong free radical scavengers and to have antioxidant properties. The nutritional composition and the antioxidant activity of several vegetables have recently been reported [30, 40, 41, 47, 48]. Taking into consideration the new interest for the natural antioxidants and the ability of the phenolic compounds to act as antioxidants [30, 49, 50], the amounts of total phenolics found in C. spinosum and C. olitorius were significantly high. These results fell within the range previously reported for other fruits, vegetables and grain products [30]. C. spinosum and C. olitorius contain considerable amounts relative to the results reported by Giovanelli et al. [50]. The variation of total phenolics during post-harvest ripening of tomato was 5–25 mg/100 g [50]. Profiles of Leaf Fatty Acids and Antioxidants throughout Plant Development Tables 2 and 3 show the composition of total lipid extracted from leaves of C. olitorius and C. spinosum. The higher content of total fatty acid


10

Table 2. Fatty acid content (mg/100 g wet weight) during leaf development of C. olitorius (molokhia) Age, days 30

40

50

C14 C16 C16:1 C17 C17:1 C18:0 C18:1 C18:2 C18:3 C20 C22:1 C24

0.84 12.01 0.42 0.18 0.05 1.70 0.26 11.83 28.06 1.1 0.53 0.28

1.07 14.41 0.49 0.21 0.05 1.96 0.65 12.91 36.32 1.30 1.11 0.34

1.72 24.86 0.77 0.22 0.06 3.07 5.06 23.68 62.14 1.53 0.76 1.63

Total fatty acid content

57.26

70.84

125.61

60 1.619 26.4 0.85 0.27 0.45 3.37 2.98 24.64 51.87 0.98 0.54 0.33 114.24

Table 3. Fatty acid content (mg/100 g wet weight) during leaf development of C. spinosum (stamnagathi) Age, days 30

40

50

60

C14 C16 C16:1 C17 C17:1 C18:0 C18:1 C18:2 C18:3 C20 C22:1 C24

0.30 12.01 3.33 0.10 0.15 0.35 0.32 2.80 4.99 0.17 nd 0.085

4.50 1.40 40.5 1.38 2.98 5.61 3.61 47.46 43.27 3.26 nd 2.13

1.78 0.25 0.14 0.27 0.34 0.62 1.57 20.04 44.44 2.25 nd 0.32

1.22 0.23 13.7 0.45 0.71 1.77 1.60 20.08 30.58 0.74 nd 0.47

Total fatty acid content

12.70

156.12

72.03

71.59


11

Table 4. Fatty acid profile of C. olitorius and C. spinosum at 50 days Fatty acids, %

C. spinosum (stamnagathi)

C. olitorius (molokhia)

C14 C16 C16:1 C17 C17:1 C18:0 C18:1 C18:2 C18:3 C20 C22:1 C24

2.48 0.34 0.20 0.38 0.47 0.86 2.18 27.83 61.69 3.13 nd 0.43

1.37 19.79 0.68 0.18 0.05 2.45 4.03 18.86 49.47 1.22 0.61 1.30

(156.12 mg/100 g wet weight) was reached after 40 days of planting for C. spinosum and (125.6 mg/100 g wet weight) after 50 days for C. olitorius. ALA (C18:3␻–3) was the predominant fatty acid in both plants examined, the maximum levels in developing leaf tissue occurred after about 50 days of growth for both plants (44.44 mg/100 g wet weight for C. spinosum and 62.14 mg/100 g wet weight for C. olitorius) (tables 2, 3). LA (C18:2␻–6) was also present in moderate amounts for both plants. The amount of ALA (C18:3␻–3) in C. olitorius increased from 50 to 60 days, while for C. spinosum the maximum level was reached at 40 days. These amounts were significantly lower in comparison to purslane; which contained 322 mg/100 g wet weight [2]. The profile of the fatty acid composition at 50 days is also presented in table 4. There was a close similarity in the fatty acid profile of C. olitorius and C. spinosum: moderate amounts of ALA (C18:3␻–3) were found in both species. However, these results show a close similarity with the fatty acid composition of the three Sonchus species analyzed by Guil-Guerrero and GimenezGimenez [40] and to some of the other edible wild plants [51] (table 5). An early increase in ALA content in developing leaf tissue has been previously reported in other plant species and may be related to chloroplast development and galactolipid biosynthesis [52]. It has been suggested that the decline in levels of C18:3 in the more mature purslane leaves may be related to the decline in certain antioxidants [2]. It has been suggested that in particular the role of chloroplast ␣-tocopherol may be to protect lipids from oxidation [52].


12

Table 5. Fatty acid contents (expressed in percentages) in edible wild plants [data from 51] Nutritional Composition of Molokhia (C. olitorius) and Stamnagathi (C. spinosum)

Fatty acids, %

Amaranthus viridis (amaranth)

Beta Chenopodium maritima album L. (wild beet) (goosefoot)

Malva sylvestris L. (common mallow)

Sisymberium irio L. (hedge mustard)

Sonchus Sonchus Verbena Portulaca tenerrimus oleraceus L. officinalis L. oleracea L. (sow-thistle- (sow-thistle) (vervain) (purslane) of-the-wall)

C14:0 C16:0 C16:1 C18:0 C18:1 C18:2 C18:3 C20 C22:1 C24

0.75 21.08 0.00 3.30 8.60 20.24 24.34 0.57 0.00 1.18

0.81 22.56 0.52 2.46 5.66 19.21 29.44 0.28 0.00 0.59

0.77 15.60 0.00 2.07 1.73 10.40 42.22 1.04 0.00 0.65

0.86 13.91 0.00 1.31 1.30 8.39 31.04 0.19 1.69 4.51

1.77 19.07 0.00 1.84 2.15 8.10 43.58 1.48 0.00 1.42

0.66 15.68 0.00 1.69 2.90 15.86 44.82 0.23 0.00 0.61

9.54 16.14 4.08 0.73 4.08 8.70 30.33 0.65 0.00 1.99

1.28 11.61 0.00 2.21 6.49 5.67 54.99 0.65 0.00 1.25

0.71 17.40 0.00 3.46 5.89 16.82 32.60 0.87 0.00 0.34

13

A relatively high concentration of this compound has been found in chloroplast envelopes [53], which are the site of galactolipid synthesis [54] and the 18:2 desaturation [55]. Loss of galactolipids and ALA has generally been associated with chloroplast senescence and appear to involve lipases and peroxidation reactions [56]. The levels of 20:0 and 24:0 remained relatively low throughout leaf development (tables 2, 3), and in this study we were unable to detect 20:5, 22:5 and 22:6. The long-chain saturated fatty acids such as 20:0 and 24:0 are normal components of plant waxes [2]. In consideration of dietary sources of antioxidants, it was emphasized that plant tissues may offer a direct source of antioxidant compounds naturally maintained in the chloroplast [2]. During photosynthesis, various free radicals and oxidative products are normally formed; chloroplasts should maintain highly efficient free-radical scavenging systems for protection of the lipids in the membranes as well as pigments and specific enzyme systems. Chloroplast antioxidants include glutathione, ascorbate, ␣-tocopherol, carotenoids and associated enzyme systems; superoxide dismutase, ascorbate peroxidase, dehydroascorbate reductase and glutathione reductase, which are critical to the development of the leaf tissue [57]. It has been proposed that ␣-tocopherol is an antioxidant synergist with ascorbic acid; it acts as a primary antioxidant, while ascorbic acid reductively regenerates oxidized ␣-tocopherol [58]. Ascorbic acid and GSH may react either directly, in combination with ␣tocopherol, or together with enzymes of ascorbate-GSH cycle in quenching free radicals or their reaction products [59]. Other antioxidants include certain phytochemicals such as flavonols and possibly polyamines [57]. Minerals Concerning C. olitorius, all minerals increased to a maximum level at 40 days except Mn and Zn, which are higher at 50 days (table 6). Furthermore, the levels of mineral elements increased during the growth development and the maximum levels for Mg and P in C. spinosum leaves were found at 30 days, for K, Na, Fe at 40 days, and for Cu and Zn at 50 days (table 7). These results were significantly higher than those reported for spinach [35]. The levels of K, Mg and P were similar to those found in Sonchus species while Ca and Fe were significantly greater. P, Cu and Mn were similar to commercial green leafy vegetables. These results fell within the range previously reported for wild vegetable foods consumed by Australian Aboriginals [37]. Relative to molokhia results, the minerals agree with those reported previously [22], while stamnagathi contains higher amounts of Fe and Zn. Mg is generally found in appreciable amounts in all green vegetables because of its association with chlorophyll, but the abundance of Ca, K and Na shows the mineral-rich nature of stamnagathi and molokhia to be outstanding.


14

Table 6. Mineral content1 during leaf development of C. olitorius (mg/100 g dry weight) Age, days

K Na Ca Mg Fe Cu Mn Zn P

30

40

50

60

4,561 ⫾ 0.37 776 ⫾ 1.36 1,327 ⫾ 0.32 542 ⫾ 2.01 55.9 ⫾ 3.22 11.3 ⫾ 0.59 13.3 ⫾ 0.79 6.53 ⫾ 2.23 611 ⫾ 1.43

5,816 ⫾ 1.02 858 ⫾ 0.75 1,338 ⫾ 2.17 405 ⫾ 1.99 57.1 ⫾ 2.21 22.5 ⫾ 1.74 12.8 ⫾ 1.19 8.47 ⫾ 1.12 523 ⫾ 2.01

5,632 ⫾ 0.56 796 ⫾ 1.39 1,422 ⫾ 0.07 389 ⫾ 0.37 53.5 ⫾ 1.72 11.7 ⫾ 1.57 14.5 ⫾ 0.27 11.2 ⫾ 0.57 475 ⫾ 1.87

5,313 ⫾ 1.35 735 ⫾ 0.56 1,650 ⫾ 0.83 340 ⫾ 1.11 38.3 ⫾ 1.71 9.5 ⫾ 1.11 13.7 ⫾ 1.24 10.4 ⫾ 1.11 453 ⫾ 1.12

Each value is the mean of three measurements ⫾ SD.

1

Table 7. Mineral content1 during leaf development of C. spinosum (mg/100 g dry weight) Age, days

K Na Ca Mg Fe Cu Mn Zn P 1

30

40

50

60

1,806 ⫾ 1.01 35 ⫾ 1.53 1,425 ⫾ 0.97 379 ⫾ 0.44 7.6 ⫾ 0.38 1.93 ⫾ 1.26 18.1 ⫾ 2.81 2.44 ⫾ 1.44 251 ⫾ 0.74

3,366 ⫾ 1.74 35.9 ⫾ 3.21 2,555 ⫾ 2.20 597 ⫾ 2.93 12.6 ⫾ 1.08 2.25 ⫾ 2.38 24.8 ⫾ 1.04 4.38 ⫾ 2.90 459 ⫾ 4.27

1,926 ⫾ 1.52 32.3 ⫾ 3.11 1,568 ⫾ 0.07 350 ⫾ 2.78 11 ⫾ 0.74 2.24 ⫾ 1.97 10.6 ⫾ 1.91 3.78 ⫾ 1.08 285 ⫾ 2.86

1,851 ⫾ 0.94 32 ⫾ 2.01 1,184 ⫾ 0.36 298 ⫾ 1.02 7.4 ⫾ 0.25 2.02 ⫾ 2.50 9.4 ⫾ 1.00 2.67 ⫾ 0.97 195 ⫾ 2.93


Antioxidant Activity Table 8 shows the antioxidant activity expressed as EC50 (mg dry plant extract/mg DPPH•). The concentration of the antioxidant needed to decrease by 50% the initial DPPH• concentration (EC50) is a parameter widely used to measure the antioxidant power [55]. The lower the EC50, the higher the antioxidant power.


15

Table 8. Antioxidant activity (expressed as EC501) during leaf development of C. olitorius and C. spinosum Age, days

Molokia (C. olitorius) (mg dry weight/mg DPPH•)

Stamnagathi (C. spinosum) (mg dry weight/mg DPPH•)

30 40 50 60

10.176 ⫾ 0.12 11.606 ⫾ 0.11 8.596 ⫾ 0.02 10.292 ⫾ 0.01

13.756 ⫾ 0.07 11.229 ⫾ 0.06 13.638 ⫾ 0.04 14.391 ⫾ 0.11


Protein content (mg/100g wet weight)

1

450 400 350 300 250 200 150 100 50 0

C. olitorius

30

C. spinosum

40

50 Age (days)

60

Fig. 5. Protein content of C. olitorius and C. spinosum during leaf development.

Based on the results of table 8, it can be seen that C. olitorius has more efficient antioxidants than C. spinosum. This is in agreement with the findings of the present work since C. olitorius was found to contain higher quantities of antioxidant molecules than C. spinosum. However, in comparison to pure phenolic standards [61], the antioxidant power of both plants is much lower. For example, the EC50 values of gallic acid, ascorbic acid, quercetin, ␣-tocopherol and resveratrol were 0.026, 0.076, 0.084, 0.201 and 0.337 mg antioxidant/mg DPPH• respectively [60]. The antioxidant power reached the maximum level after 50 days for C. olitorius (EC50 ⫽ 8.596 ⫾ 0.02) and after 40 days for C. spinosum (EC50 ⫽ 11.229 ⫾ 0.06). This is also in agreement with the findings of the present study since the amounts of the antioxidant compounds were highest between 40 and 50 days of planting. Proteins The two species C. spinosum and C. olitorius contained considerable amounts of protein (fig. 5). This amount increased significantly during leaf


16

development, for C. spinosum from 287.9 mg/100 g wet weight at 30 days to 358.6 mg/100 g wet weight at 60 days. Concerning C. olitorius, the level of protein increased from 30 to 60 days (221.1–400.9 mg/100 g wet weight). These results agree with previous reports, which show that green vegetables are a rich source of protein and minerals, but their utilization is limited due to the presence of indigestible fiber [61].

Conclusion

From this study we conclude that 100 g of fresh molokhia leaves (one serving) contain about 62.14 mg of C18:3␻–3, 77.42 mg of ascorbic acid, 14.89 mg of ␣-tocopherol, 5.44 mg of ␤-carotene, 12.52 mg of glutathione and 38 mg of phenols, while 100 g of fresh stamnagathi leaves (one serving) contain about 44.44 mg of C18:3␻–3, 36.58 mg of ascorbic acid, 9.78 mg ␣-tocopherol, 2.66 mg ␤-carotene, 13.77 mg of glutathione and 20.31 mg of phenols. Furthermore, these two plants contain appreciable amounts of calcium, iron, zinc and potassium. Overall, these results indicate that under the growing conditions maintained during the study, the nutritional quality of leaf tissue, in terms of minerals, antioxidants and ALA, would be optimal between 40 and 50 days of planting. Furthermore, the results show that these two Mediterranean wild plants, in addition to their good taste, are rich sources of antioxidants, protein, minerals and ALA. We believe that these plants could be used for nutritional purposes due to their demonstrated good nutritional qualities. Compared to spinach, molokhia and stamnagathi have higher nutritional value, and they are better sources of carotenoids, vitamin C, vitamin E, glutathione, ␻–3 fatty acids and minerals. Furthermore, they are tastier in many recipes of cooking, which make them more acceptable to children. Taking into consideration the current recommended dietary allowances (RDAs), we can conclude also that C. olitorius and C. spinosum may contribute largely to the human diet, especially in terms of vitamin C, vitamin E, carotenoids, calcium, iron, magnesium and zinc. Furthermore, their content of phenols and their antioxidant activity give them a high nutritional value, which may contribute to human health. Clearly from this study, it can be emphasized that plant tissues should be re-evaluated as a potential dietary source of essential fatty acids, vitamins, antioxidants and minerals, and in general for micronutrients and phytonutrients. More studies are required on biochemical and molecular, ethno-botanic and phytogenetic aspects of the wild plants, and more research is needed on their special potential regarding the prevention and treatment of chronic-degenerative diseases


17

by increasing the dietary intake of wild plants in both developed and developing countries. Eliminating micronutrient deficiencies through plant foods instead of synthetic supplements is the best way to ensure health and well-being. The importance of ALA and antioxidants from wild plants and nuts in the diet of Crete as decreasing both the risk and the death rate in patients with one episode of myocardial infarction (MI) was clearly shown in the Lyon Heart Study [62], and in the Indo-Mediterranean Diet Heart Study by Singh et al. [63]. Recently, a similarly modified diet of Crete and simvastatin intervention study was carried out in Finland by Jula et al. [64]. Simvastatin on the habitual diet lowered the concentrations of ␣-tocopherol, ␤-carotene and ubiquinol-10 by 16–22%, whereas dietary treatment did not lower serum ␤-carotene and ubiquinol-10 levels. Most importantly, the modified Mediterranean diet did not increase fasting insulin and insulin resistance significantly, 13 and 14%, respectively. The authors conclude, ‘the combination of a modified Mediterranean-type diet and statin treatment of hypercholesterolemia in nondiabetic men not only results in a beneficial additive effect on lowering serum total cholesterol and LDL-C concentration but also counteracts the elevating influence on fasting insulin level associated with simvastatin treatment. The combination is clinically sound, and the importance of diet as an integral part of statin treatment of hypercholesterolemic patients should be emphasized’ [64].

References 1

2

3

4

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Artemis P. Simopoulos, MD President, The Center for Genetics, Nutrition and Health, 2001 S Street, N.W., Suite 530, Washington, DC 20009 (USA) Tel. ⫹1 202 462 5062, Fax ⫹1 202 462 5241, E-Mail [email protected]


21


Nutritional Composition of Selected Wild Plants in the Diet of Crete Sabrina Zeghichi a, Stamatina Kallithraka a, Artemis P. Simopoulos b, Zaxarias Kypriotakis c a b c

Mediterranean Agronomic Institute of Chania, Crete, Greece; The Center for Genetics, Nutrition and Health, Washington, D.C., USA and Exoli gsoponias TEI Kritis, Iraklio, Crete, Greece

Introduction

The diet of Crete continues to gain enormous popularity [1]. Today, this diet is virtually the same as it was in 4500 BC. The diet first came to the attention of the medical community in the 1960s when an influential 15-year study revealed that men from Crete were healthier than the other men surveyed in seven different countries – Greece, Italy, The Netherlands, Finland, Yugoslavia, Japan and the USA [2]. There was something unique about the diet of Crete. One of us (A.P.S.) identified the missing clues to be (1) the ideal ratio of essential fatty acids, ␻–6:␻–3, of 2–1:1 and (2) the high antioxidant content of the diet due to the high intake of wild plants and fruits, such as purslane (Portulaca oleracea) which is a wild plant, eaten widely in Crete, that is high in ␣-linolenic acid, vitamin E, glutathione and other antioxidants [3–5]. Another good source of ␣-linolenic acid in the diet of Crete is walnuts [6, 7]. People in Crete consume large quantities of greens and wild plants daily, in addition to their high consumption of olive oil which is a very rich source of monounsaturated fatty acids. The low content of ␻–6 fatty acids in olive oil, less than 8%, leads to a favorable ratio of ␻–6 to ␻–3 fatty acids [8]. In addition, olive oil is rich in antioxidants and squalene [9, 10]. Hence, this composition places olive oil in a unique and superior position of other vegetable oils such as corn, sunflower, safflower, soybean, cottonseed, etc. [1, 7–11]. The Lyon Diet Heart Study clearly showed that adopting a modified Cretan Mediterranean-type diet reduced the incidence of sudden death from coronary heart disease significantly, and total death by 70% in 2 years and 33% in 5 years

of follow-up [12, 13]. The ‘experimental’ diet, a modified diet of Crete, was low in saturated and trans fatty acids with a ratio of ␻–6:␻–3 ⫽ 4:1, and it was a non-strict vegetarian diet rich in oleic acid, ␻–3 fatty acids, fiber, vitamins of the B group and various antioxidants including vitamin C, vitamin E, trace elements and flavonoids, whereas the control diet was the Step I American Heart Association diet. Diets rich in fruits and vegetables are associated consistently with reduced risk of a variety of cancers, coronary heart disease, diabetes, osteoporosis and gastrointestinal disorders [7, 8, 14–17]. According to the American Cancer Society recommendations, consumption of 400 g/day (5 servings/day) or more of a variety of vegetables and fruits may, by itself, decrease the overall cancer incidence by at least 20% [18]. The 1997 report on ‘Food, Nutrition and the Prevention of Cancer: A Global Perspective’ by the World Cancer Research Fund and the American Institute for Cancer Research (AICR) supports this recommendation [19]. Fruits and vegetables are beneficial due to their high content of nutrients, such as vitamins, minerals and essential fatty acids, as well as non-nutrients, such as fiber, polyphenols and anthocyanins, which may possess health-protective properties [6, 7, 20–23]. Today, greens and especially wild plants are attracting attention from the evolutionary and health standpoints, and partly due to the new-found popularity of salads made from mixed greens. Wild plants are rich sources of antioxidants and ␻–3 fatty acids [3–5, 21]. Yet, few studies have reported the nutritive value of the edible wild plants in the diet of Crete [22]. If these plants are to be developed as a commercial crop, it becomes important to determine their nutritional quality; this was indeed the goal of the study. It is therefore important to investigate the nutritional composition of diets such as the diet of Crete, which has been shown to be associated with a decreased rate of cardiovascular disease and cancer [13]. The diet of Crete being rich in edible wild plants may be a reference standard for modern human nutrition and a model for defense against certain diseases of affluence [1, 7, 24].

Materials and Methods This study was carried out during the academic year 2000–2001 at the Mediterranean Agronomic Institute of Chania, Crete, Greece. The aim of this work was to evaluate the nutritional composition of selected commonly eaten Cretan wild plants. Twenty-five Cretan wild plants were assayed for antioxidant activity, total phenols, mineral and nitrate content (fig. 1a–y). Only edible parts of the plants were used. Samples were gathered (March 2000) from Heraklio in Northern Crete, Greece. Table 1 shows the Latin names and uses of the plants. Before performing the analysis, the samples were washed, freeze-dried for the determination of antioxidant activity, phenolics and

Nutritional Composition of Selected Wild Plants in the Diet of Crete

23

a

b

c

d

e

f

g

h

i

j

k

l

n

o

1a–o m

Zeghichi/Kallithraka/Simopoulos/Kypriotakis

24

p

q

r

s

t

u

v

w

x

1p–y y

Fig. 1. Photographs of 25 Cretan wild plants assayed for antioxidant activity, total phenols, mineral and nitrate content: (a) Papaver rhoeas, (b) Sonchus oleraceus, (c) Pimpinela peregrina, (d) Centaurea idaea, (e) Tragopogon sinuatus, (f) Crepis commutata, (g) Helmintotheca echioides, (h) Tordylium apulum, (i) Scandix pecten-veneris, (j) Pontikes, (k) Allium subhirstum, (l) Rumex ssp., (m) Silene vulgaris, (n) Crepis vesicaria, (o) Uropermum picroides, (p) Tolpis virgata, (q) Hypochoeris radicata, (r) Cichorium pumilum, (s) Oenothera pimpineloides, (t) Leontodon tuberosus, (u) Cichorium spinosum, (v) Ranunculus ficarioides, (w) Prasium majus, (x) Foeniculum vulgare ssp. piperitum and (y) Stypocaulon scoparium.


25

Table 1. Scientific names and uses of the Cretan wild plants No. 1 2

Plant names

Uses

Papaver rhoeas Sonchus oleraceus

Cooked with olive oil, vegetable pie Boiled salad, cooked with olive oil, vegetable pie, raw salad Cooked with oil, vegetable pie Boiled salad Cooked with olive oil, vegetable pie Boiled salad Boiled salad Cooked with oil, vegetable pie Cooked with olive oil, vegetable pie Cooked with olive oil, vegetable pie, raw salad Cooked with olive oil, vegetable pie Cooked with olive oil, vegetable pie Cooked with olive oil, vegetable pie Boiled salad Boiled salad Cooked with olive oil, vegetable pie, boiled salad Boiled salad Boiled salad Cooked with olive oil, vegetable pie Cooked with olive oil, vegetable pie Boiled salad, raw salad Cooked with olive oil, vegetable pie, boiled salad, raw salad Cooked with olive oil, vegetable pie Cooked with olive oil, vegetable pie

3 4 5 6 7 8 9 10

Pimpinela peregrina Centaurea idaea Tragopogon sinuatus Crepis commutata Helmintotheca echioides Tordylium apulum Scandix pecten-veneris Pontikes

11 12 13 14 15 16

Allium subhirstum Rumex ssp. Silene vulgaris Crepis vesicaria Uropermum picroides Tolpis virgata

17 18 19 20 21 22

Hypochoeris radicata Cichorium pumilum Oenothera pimpineloides Leontodon tuberosus Cichorium spinosum Ranunculus ficarioides

23 24

Prasium majus Foeniculum vulgare ssp. piperitum Stypocaulon scoparium

25

Raw salad

Both raw and boiled salads are dressed with olive oil and lemon or vinegar.

tocopherol, and dried in the oven at 30°C for the mineral and nitrate analysis. These plants were chosen because of their large contribution to the diet of Crete, since they are eaten throughout the year and especially during periods of Lent when they become a major component of the diet. For those who follow the Greek Orthodox Church teachings, there is a total of about 120 days when people abstain from meat and dairy products. The Cretan table is garnished from two to five times per week with salads, vegetable pies, or meals based on wild plants. The methods used for the determination of ␣-tocopherol, total phenols, antioxidant activity, mineral elements and nitrates have been described in detail in the previous paper in this volume [22].


26

Table 2. ␣-Tocopherol content of Cretan edible wild plants (mg/100 g wet weight) No.

Plant names

␣-Tocopherol mg/100 g wet weight

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25

Papaver rhoeas Sonchus oleraceus Pimpinela peregrina Centaurea idaea Tragopogon sinuatus Crepis commutata Helmintotheca echioides Tordylium apulum Scandix pecten-veneris Pontikes Allium subhirstum Rumex ssp. Silene vulgaris Crepis vesicaria Uropermum picroides Tolpis virgata Hypochoeris radicata Cichorium pumilum Oenothera pimpineloides Leontodon tuberosus Cichorium spinosum Ranunculus ficarioides Prasium majus Foeniculum vulgare ssp. piperitum Stypocaulon scoparium

0.524 0.294 0.490 0.108 0.206 0.360 0.029 2.426 1.133 0.360 1.215 0.509 0.354 0.401 0.482 0.043 0.193 0.420 0.232 0.099 0.398 0.443 1.287 1.117 0.000

Results

a-Tocopherol Table 2 shows the concentration of ␣-tocopherol. It ranged from a maximum of 2.426 mg/100 g wet weight found in Tordylium apulum to a minimum of 0.029 mg/100 g wet weight in Helmintotheca echioides. The results of ␣-tocopherol fall within the range previously reported for green leaf tissues (0.015–2 mg/100 g wet weight) of Mediterranean plants and herbs [25–29]. However, these results were significantly lower than those reported for purslane (12.2 ⫾ 0.4 mg/100 g wet weight) [5], Cichorium spinosum (9.78 ⫾ 0.05 mg/100 g wet weight) and Corchorus olitorius (14.89 ⫾ 0.05 mg/100 g wet weight) [22] but T. apulum contained a higher amount of


27

Table 3. Total phenols content of Cretan edible wild plants (mg/100 g wet weight) No.

Plant names

Total phenols mg/100 g wet weight

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25


33.5 ⫾ 0.81 48.04 ⫾ 0.79 47.65 ⫾ 0.33 61.55 ⫾ 1.45 20.82 ⫾ 0.14 49.08 ⫾ 2.32 44.86 ⫾ 1.08 46.87 ⫾ 1.25 46.51 ⫾ 1.13 59.27 ⫾ 1.10 14.54 ⫾ 0.65 102.56 ⫾ 3.13 40.18 ⫾ 1.20 49.42 ⫾ 2.87 35.76 ⫾ 0.54 21.46 ⫾ 0.47 57.03 ⫾ 0.32 93.64 ⫾ 0.28 55.05 ⫾ 1.31 48.06 ⫾ 0.39 72.63 ⫾ 0.37 32.99 ⫾ 0.60 78.72 ⫾ 0.44 82.521 ⫾ 0.60 6.736 ⫾ 0.52

␣-tocopherol (2.426 mg/100 g wet weight) than spinach (1.8 ⫾ 0.09 mg/100 g wet weight) [5]. ␣-Tocopherol was not detected in the algae Stypocaulon scoparium [30]. Total Phenols As shown in table 3, Rumex ssp. contained the highest amount of total phenols, 102.56 ⫾ 3.13 mg/100 g wet weight followed by Cichorium pumilum (93.643 ⫾ 0.28 mg/100 g wet weight) and Foeniculum vulgare ssp. piperitum (82.521 ⫾ 0.60 mg/100 g wet weight), whereas Allium subhirstum and the algae S. scoparium contained lower amounts 14.54 ⫾ 0.65 and 6.735 ⫾ 0.52 mg/100 g wet weight respectively. The rest of the plants contained different amounts ranging between 20.82 ⫾ 0.14 and 78.718 ⫾ 0.44 mg/100 g wet weight, these results


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Table 4. Antioxidant activity and antiradical power of Cretan edible wild plants No.

Plant names

Antioxidant activity (EC50) mg dry extract/mg DPPH

ARP 1/EC50

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25


0.995 ⫾ 0.14 3.664 ⫾ 0.05 2.909 ⫾ 0.29 1.400 ⫾ 0.011 3.679 ⫾ 0.16 3.169 ⫾ 0.14 2.344 ⫾ 0.17 2.852 ⫾ 0.13 2.477 ⫾ 0.11 7.261 ⫾ 0.25 2.697 ⫾ 0.08 2.344 ⫾ 0.17 2.852 ⫾ 0.13 2.284 ⫾ 0.42 0.830 ⫾ 0.20 1.350 ⫾ 0.12 0.761 ⫾ 0.22 0.696 ⫾ 0.55 0.222 ⫾ 0.018 1.194 ⫾ 0.047 1.115 ⫾ 0.28 0.280 ⫾ 0.08 0.818 ⫾ 0.27 1.041 ⫾ 0.15 2.367 ⫾ 0.19

1.005 ⫾ 0.15 0.273 ⫾ 0.004 0.346 ⫾ 0.036 0.714 ⫾ 0.005 0.272 ⫾ 0.012 0.316 ⫾ 0.014 0.428 ⫾ 0.031 0.351 ⫾ 0.017 0.404 ⫾ 0.018 0.138 ⫾ 0.005 0.371 ⫾ 0.01 0.428 ⫾ 0.03 0.351 ⫾ 0.02 0.438 ⫾ 0.09 1.205 ⫾ 0.37 0.741 ⫾ 0.06 1.390 ⫾ 0.45 2.039 ⫾ 1.18 4.520 ⫾ 0.35 0.838 ⫾ 0.03 0.944 ⫾ 0.28 3.812 ⫾ 1.27 1.321 ⫾ 0.46 0.974 ⫾ 0.14 0.424 ⫾ 0.035

are higher than those reported for C. spinosum and C. olitorius (20.31 ⫾ 0.05 and 38 ⫾ 0.08 mg/100 g wet weight respectively) [22]. Phenols are large compounds occurring ubiquitously in both edible and non-edible plants, they have been reported to have multiple biological effects, including antioxidant activity [31–33]. The amounts of total phenolics found in the wild plants of Crete fall within the range previously reported by Kahkonen et al. [34] who studied the antioxidant activity of plant extracts containing phenolic compounds and found that, for some vegetables, the amount of total phenolics varied between 40 and 660 mg/100 g wet weight [34]. Antioxidant Activity Based on the results on table 4, it can be seen that Oenothera pimpineloides is a more efficient antioxidant than the rest of the plants


29

(EC50 ⫽ 0.222 ⫾ 0.018). Another species that has shown significant antioxidant activity is Ranunculus ficarioides (EC50 ⫽ 0.28 ⫾ 0.08). Compared to pure phenolic standards, the antioxidant activity of both plants is close to the antioxidant activity values of ␣-tocopherol and resveratrol (EC50 ⫽ 0.201 and 0.337 mg antioxidant/mg DPPH• respectively) [35]. Prasium majus which contains high amounts of ␣-tocopherol and total phenolics was quiet efficient as well with EC50 ⫽ 0.818 ⫾ 0.27. In agreement with the findings of the present work, the species which contained higher quantities of antioxidant molecules were significantly efficient such as C. pumilum, Urospermum picroides and F. vulgare, EC50 ⫽ 0.696 ⫾ 0.55, 0.83 ⫾ 0.2, 1.041 ⫾ 0.15, respectively, whereas the algae showed a good antioxidant activity (EC50 ⫽ 2.367 ⫾ 0.19) even with an undetectable amount of ␣-tocopherol and total phenols; thus, the antioxidant activity of the algae is most likely due to the presence of other antioxidant compounds (ex. ␤-carotene, glutathione). Contrary to the rest of the analyzed wild plants, Pontikes had the lowest antioxidant power (table 4) EC50 ⫽ 7.261 ⫾ 0.25, this finding was close to those reported in C. olitorius (EC50 ⫽ 8.596 ⫾ 0.02) [22]. Minerals All the plants contained considerable amounts of minerals (table 5). Silene vulgaris and Tolpis virgata contained the highest amount of potassium 5,140 ⫾ 0.64 and 5,040 ⫾ 0.19 mg/100 g dry weight respectively, whereas Leontodon tuberosus contained a very high amount of sodium 2,370 ⫾ 0.54 mg/100 g dry weight while the two species Tragopogon sinuatus and Scandix pecten-veneris contained higher amounts of calcium compared to the rest of the plants (3,120 ⫾ 1.2 and 2,790 ⫾ 1.43 mg/100 g dry weight respectively. S. vulgaris and L. tuberosus were high in magnesium (517 ⫾ 0.06 and 494 ⫾ 1.48 mg/100 g dry weight respectively). T. sinuatus, C. pumilum and Hypochoeris radicata had the highest amounts of iron compared to the rest of the plants (176 ⫾ 0.34, 172 ⫾ 1.12 and 136 ⫾ 0.86 mg/100 g dry weight). T. virgata being rich in potassium contained also a high amount of copper 26.6 ⫾ 0.25 mg/100 g dry weight. The majority of the plants had considerable amounts of manganese, but the highest amount was found in C. pumilum and T. sinuatus (14.7 ⫾ 1.04 and 13.4 ⫾ 1.12 mg/100 g dry weight). While, R. ficarioides contained the highest amount of zinc, 7.01 ⫾ 0.82, Rumex was highest in phosphorus (804 ⫾ 1.11 ppm dry weight). The algae had high amounts of K, Na, Ca and Mg (table 5). All these results were significantly higher than those reported for spinach [36]. The levels of K, Mg and P were similar to those found in Sonchus species while Ca, Zn and Fe were significantly greater [37]. P, Cu and Mn were similar to commercial green leafy vegetables. These results fell within the range previously


30

Table 5. Mineral content of some Cretan edible wild plants (mg/100 g dry weight) Nutritional Composition of Selected Wild Plants in the Diet of Crete

Plant names

K

Na

Ca

Mg

Fe

Cu

Mn

Zn

P

P. rhoeas S. oleraceus P. peregrina C. idaea T. sinuatus C. commutata H. echioides T. apulum S. pecten-veneris Pontikes A. subhirstum Rumex ssp. S. vulgaris C. vesicaria U. picroides T. virgata H. radicata C. pumilum O. pimpineloides L. tuberosus C. spinosum R. ficarioides P. majus F. vulgare ssp. piperitum S. scoparium

3,880 ⫾ 0.31 4,300 ⫾ 0.33 4,210 ⫾ 0.14 2,860 ⫾ 0.36 3,020 ⫾ 0.26 4,370 ⫾ 0.64 3,840 ⫾ 0.25 3,790 ⫾ 0.58 4,450 ⫾ 0.73 4,270 ⫾ 0.17 2,520 ⫾ 0.83 3,680 ⫾ 0.12 5,140 ⫾ 0.64 3,540 ⫾ 0.43 4,210 ⫾ 0.39 5,040 ⫾ 0.19 1,360 ⫾ 0.59 1,940 ⫾ 0.65 4,270 ⫾ 0.53 2,590 ⫾ 0.34 2,030 ⫾ 3.6 3,820 ⫾ 1.08 1,630 ⫾ 0.38 1,440 ⫾ 0.18

960 ⫾ 0.67 579 ⫾ 0.95 903 ⫾ 0.46 1,640 ⫾ 0.41 955 ⫾ 0.72 537 ⫾ 0.42 937 ⫾ 1.09 545 ⫾ 2.25 662 ⫾ 0.66 402 ⫾ 0.46 98.9 ⫾ 1.66 338 ⫾ 0.49 362 ⫾ 0.93 1,150 ⫾ 0.27 1,070 ⫾ 1.38 1,130 ⫾ 0.97 1,700 ⫾ 0.42 1,370 ⫾ 1.68 1,180 ⫾ 0.22 2,370 ⫾ 0.54 1,260 ⫾ 0.75 448 ⫾ 0.52 144 ⫾ 0.34 839 ⫾ 0.47

2,110 ⫾ 1.49 1,960 ⫾ 0.48 1,990 ⫾ 0.43 1,750 ⫾ 0.54 3,120 ⫾ 1.2 310 ⫾ 0.13 2,110 ⫾ 1.26 1,550 ⫾ 1.04 2,790 ⫾ 1.43 1,310 ⫾ 0.77 1,380 ⫾ 1.24 595 ⫾ 1.71 1,990 ⫾ 0.37 2,030 ⫾ 1.16 1,850 ⫾ 1.36 1,550 ⫾ 0.22 1,790 ⫾ 0.89 1,840 ⫾ 1.35 1,350 ⫾ 0.38 1,980 ⫾ 0.34 1,400 ⫾ 0.61 1,550 ⫾ 0.76 1,720 ⫾ 1.38 1,190 ⫾ 0.25

511 ⫾ 1.54 448 ⫾ 2.35 318 ⫾ 0.45 347 ⫾ 0.74 319 ⫾ 0.99 427 ⫾ 1.19 314 ⫾ 1.36 254 ⫾ 1.22 228 ⫾ 0.81 317 ⫾ 0.62 166 ⫾ 1.43 354 ⫾ 0.89 517 ⫾ 0.06 438 ⫾ 2.18 310 ⫾ 0.47 350 ⫾ 0.08 353 ⫾ 0.23 452 ⫾ 0.79 347 ⫾ 0.61 494 ⫾ 1.48 279 ⫾ 0.11 454 ⫾ 1.75 148 ⫾ 0.17 235 ⫾ 0.31

51.7 ⫾ 1.63 45.4 ⫾ 1.67 82.2 ⫾ 0.82 103 ⫾ 0.8 176 ⫾ 0.34 46.5 ⫾ 0.35 29.9 ⫾ 1.66 28.4 ⫾ 1.44 44.3 ⫾ 0.23 53.5 ⫾ 0.34 53.2 ⫾ 0.85 39.9 ⫾ 0.73 18.5 ⫾ 0.99 108 ⫾ 0.38 23.4 ⫾ 0.18 31.3 ⫾ 0.29 136 ⫾ 0.86 172 ⫾ 1.12 18.2 ⫾ 1.0 37.0 ⫾ 1.42 65.1 ⫾ 0.17 41.7 ⫾ 1.35 9.98 ⫾ 0.13 8.25 ⫾ 0.48

2.13 ⫾ 0.32 2.58 ⫾ 2.14 1.95 ⫾ 1.33 2.54 ⫾ 2.41 2.11 ⫾ 0.8 3.29 ⫾ 0.41 1.93 ⫾ 2.06 1.53 ⫾ 0.43 1.71 ⫾ 0.53 9.33 ⫾ 0.99 1.12 ⫾ 0.57 10.2 ⫾ 1.29 2.87 ⫾ 0.82 2.47 ⫾ 2.86 2.94 ⫾ 1.05 26.6 ⫾ 0.25 2.05 ⫾ 1.4 2.87 ⫾ 2.18 3.17 ⫾ 0.58 2.69 ⫾ 0.41 1.72 ⫾ 0.33 3.63 ⫾ 2.48 0.49 ⫾ 0.54 2.85 ⫾ 0.44

7.13 ⫾ 0.53 8.76 ⫾ 1.48 5.58 ⫾ 0.60 11.8 ⫾ 0.48 13.4 ⫾ 1.12 5.76 ⫾ 0.74 5.75 ⫾ 0.79 6.69 ⫾ 1.0 5.67 ⫾ 0.48 8.76 ⫾ 1.39 3.69 ⫾ 0.98 4.51 ⫾ 0.57 7.96 ⫾ 0.68 12.5 ⫾ 0.40 8.49 ⫾ 1.30 7.8 ⫾ 1.22 10.2 ⫾ 1.3 14.7 ⫾ 1.04 8.93 ⫾ 0.44 12.4 ⫾ 0.67 11.3 ⫾ 0.94 9.98 ⫾ 0.53 2.39 ⫾ 0.21 3.32 ⫾ 0.29

5.81 ⫾ 0.15 6.63 ⫾ 0.53 5.23 ⫾ 0.84 3.84 ⫾ 1.31 2.48 ⫾ 1.38 5.34 ⫾ 1.25 2.05 ⫾ 0.36 4.27 ⫾ 0.33 2.15 ⫾ 0.23 4.74 ⫾ 0.97 1.81 ⫾ 1.84 5.0 ⫾ 1.57 3.40 ⫾ 1.72 5.44 ⫾ 1.07 6.60 ⫾ 1.26 6.76 ⫾ 1.58 1.57 ⫾ 0.80 4.15 ⫾ 0.89 3.84 ⫾ 0.93 2.12 ⫾ 1.16 3.01 ⫾ 0.62 7.01 ⫾ 0.82 1.25 ⫾ 0.81 1.65 ⫾ 0.22

729 ⫾ 0.98 692 ⫾ 1.38 480 ⫾ 0.81 667 ⫾ 2.26 344 ⫾ 1.25 651 ⫾ 1.43 574 ⫾ 1.22 728 ⫾ 2.5 518 ⫾ 1.07 605 ⫾ 0.19 391 ⫾ 2.21 804 ⫾ 1.11 429 ⫾ 1.09 512 ⫾ 0.71 801 ⫾ 0.75 742 ⫾ 0.71 374 ⫾ 0.16 455 ⫾ 0.47 629 ⫾ 1.3 331 ⫾ 0.53 287 ⫾ 0.86 422 ⫾ 1.71 378 ⫾ 0.52 274 ⫾ 0.33

6,270 ⫾ 0.47

3420 ⫾ 0.4

5,170 ⫾ 0.89

890 ⫾ 0.13

21.3 ⫾ 1.06

1.95 ⫾ 2.2

1.32 ⫾ 0.58

2.06 ⫾ 1.48

52.4 ⫾ 2.11

31

Table 6. Nitrate content of Cretan edible wild plants (g/100 g wet weight) No.

Plant names

Nitrates g/100 g wet weight

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25


0.203 ⫾ 0.016 0.100 ⫾ 0.006 0.015 ⫾ 0.002 0.097 ⫾ 0.002 0.148 ⫾ 0.009 0.037 ⫾ 0.012 0.034 ⫾ 0.004 0.044 ⫾ 0.008 0.076 ⫾ 0.003 0.032 ⫾ 0.003 0.133 ⫾ 0.005 0.043 ⫾ 0.001 0.090 ⫾ 0.006 0.028 ⫾ 0.001 0.008 ⫾ 0.002 0.008 ⫾ 0.003 0.054 ⫾ 0.002 0.057 ⫾ 0.007 0.055 ⫾ 0.002 0.101 ⫾ 0.002 0.056 ⫾ 0.01 0.064 ⫾ 0.00 0.189 ⫾ 0.005 0.024 ⫾ 0.001 0.022 ⫾ 0.001

reported for wild vegetable foods consumed by Australian Aboriginals [38]. Mg is generally found in appreciable amounts in all green vegetables because of its association with chlorophyll but the abundance of Ca, K, Na and Zn shows the mineral rich nature of the wild plants of Crete to be outstanding. These findings indicate that a diet rich in wild plants provides adequate amounts of vitamins, minerals and antioxidants consistent with health. Nitrates Compared to the results reported for plant tissue by Cataldo et al. [39], the wild plants contained very low amounts of nitrates (table 6), this may be due to the environmental conditions where the plants were grown mainly due to the


32

absence of fertilizers. U. picroides and T. virgata contained the lowest amount of nitrates being 8 ⫾ 0.003 mg/100 g wet weight. The higher amount of nitrates was determined in Papaver rhoeas being 203 ⫾ 0.0160 mg/100 g wet weight. Nitrate (NO3) is a naturally occurring form of nitrogen found in soil, provided from fertilizers, manure or waste water. Nitrogen is essential to all life, and most crop plants require large quantities to sustain high yields, but in moderate amounts, nitrate is a harmless constituent. Plants use nitrates from the soil to satisfy nutrient requirements and may accumulate nitrate in their leaves and stems. In fact, most of the nitrate we consume is from our diet, particularly from raw or cooked vegetables. This nitrate is readily absorbed and excreted in the urine. However, prolonged intake of high levels of nitrate is linked to gastric problems due to the formation of nitrosamines.

Discussion

Nutritional health is dependant on the interaction between the environmental aspects of diet in terms of supply, availability and consumption, and the genetically controlled aspects of digestion, absorption, distribution, transformation, storage and excretion [40]. Nutrients regulate the activity of enzymes involved in their own metabolism by specifically affecting enzyme activity or gene expression. The nutritional regulation occurs both by macro- and micronutrients [41]. Both micro- and macronutrients control gene expression leading to changes in cell growth, differentiation, or metabolism. Defining the molecular basis for nutrient control of gene expression provides insight into the diverse actions of nutrients in both normal and pathophysiological states and may provide novel approaches to control chronic diseases such as coronary artery disease, hypertension, insulin resistance, obesity and cancer [42–44]. Free radicals are implicated in the pathogenesis of a number of different disorders and are believed to play a role in more than 60 different health conditions, including the aging process, cancer and atherosclerosis [45, 46]. A variety of antioxidants, vitamins or phytochemicals may be the best way to provide the body with the most complete protection against free radical damage and oxidation. An increase in consumption of antioxidant nutrients may reduce the risk of free radical related health problems [19]. Green leafy wild plants, containing considerable amounts of antioxidant vitamins and phytochemicals in addition to their high content of essential micronutrients could be one of the ways to delay the onset of chronic diseases. Aging, for example, is believed to be due to the oxidants produced as by-products of normal metabolism. Degenerative diseases such as cancer, cardiovascular disease, cataracts and brain dysfunction are often correlated with oxidative damage. Some studies


33

consider vitamin E to play a role in the prevention of degenerative diseases and the aging process [45, 47, 48]. Vitamin E appears to protect the chondrocytes during maturation as well as benefiting chondrogenesis and bone growth [49]. It has been demonstrated that supplementation with vitamin E can inhibit the oxidation of LDL and decrease platelet aggregability in humans, contributing to the prevention of cardiovascular disease [48, 50]. However, two clinical intervention studies, (1) the Gruppo Italiano per lo Studio della Sopravivenza nell Infarto miocardico (GISSI)-Prevenzione trial [51] did not show an independent effect of vitamin E beyond that obtained with fish oils and (2) the Heart Outcomes Prevention Evaluation Study (HOPE Study) reported that vitamin E compared to placebo did not reduce the incidence of cardiovascular events [52]. Phytochemicals are substances that plants naturally produce to protect themselves against viruses, bacteria and fungi and may play an important nutritional role in human health (table 7) [53, 54]. Being an important part of human diet, polyphenols and their physiological effects have been thoroughly investigated. Polyphenols have three major physiological effects, namely antioxidant [55, 56], anticarcinogenic [57, 58] and antimutagenic effects [59–62]. Polyphenols are also active against some viruses, their activity against HIV has been tested in vitro [63]. Many of these phenols have been found to be more powerful antioxidants than vitamins C, E and ␤-carotene using an in vitro model for heart disease, namely the oxidation of low density lipoproteins (LDL) [56]. Thus, plant consumption may provide protection against oxidative stress which is a pathogenic mechanism of both carcinogenesis and atherosclerosis [54]. Many minerals are cofactors in the metabolism of hemoglobin, vitamins, hormones and enzymes. Some of them are required for normal functioning of nerves and muscles. They regulate the acid-base balance of the body fluids and they form a structural part of bone and cartilage [49]. However, unlike other nutrients, such as amino acids and fatty acids, minerals must be supplied from the diet, since the body cannot produce them. For all the above reasons, this study was focused on the determination of the nutritional values of some wild plants widely eaten in Crete and on their contribution to the diet. The results obtained in this study showed that the investigated plants contained considerable amounts of antioxidants and mineral elements. T. apulum contained a higher amount of ␣-tocopherol of 2.426 mg/100 g wet weight than other plants. Rumex ssp. contained the highest amount of total phenols, 102.56 ⫾ 3.13 mg/100 g wet weight followed by C. pumilum 93.643 ⫾ 0.28 mg/100 g. Whereas O. pimpineloides was more efficient antioxidant than the rest of the plants (EC50 ⫽ 0.222 ⫾ 0.018), another species, R. ficarioides, also showed significant antioxidant activity (EC50 ⫽ 0.28 ⫾ 0.08).


34

Table 7. Selected phytochemicals in edible plants [taken from 53, 54] Phytochemical

Source

Function

Terpenes

Green foods, soy products, grains

Antioxidant, protect lipids, blood and other fluids from free radicals, and the plant from reactive oxygen

Carotenoids

Yellow, orange and green vegetables and fruits

Antioxidant include the carotenes and xanthophylls, protect from sunlight, and protect other vitamins from oxidation

Limonoids

Citrus fruits peels, lemon and other citrus fruits

Protection of lung tissue

Phytosterols

Green and yellow vegetables and fruits and their seeds, beans, peanuts

Compete with dietary cholesterol for uptake in the intestines and facilitate its excretion from the body

Phenols

Fruits, vegetables, soybeans, cereals, tea

Block specific enzymes that cause inflammation, modify the prostaglandin pathway and thereby protect platelets from clumping

Flavonoids

Fruits, vegetables, herbs, spices (mint, rosemary, thyme, oregano, sage, basil)

Subclass of phenols include; flavones, flavonols and flavonones. Enhance the effect of vitamin C, and protect the body against allergies, inflammation, free radicals, hepatotoxins, platelet aggregation, bacteria, ulcers, viruses and tumors

Anthocyanidins

Fruits, vegetables, red wine, grapes

Known as flavonals, they reinforce the strength of collagen protein, and scavenge free radicals

Isoflavones

Flaxseed, lentils, soybeans

Subclass of phenols, block enzymes that promote tumor growth

Thiols

Garlic, cruciferous vegetables (cabbage, turnips, members of mustard family)

Antimutagenic and anticarcinogenic properties, immune and cardiovascular protection

Glucosinolates

Cruciferous vegetables (broccoli, cauliflower, cabbage, brussels sprouts, kale, turnips, bok choy, kohlrabi)

Activation of liver detoxification enzymes, regulate white blood cells and cytokines, block enzymes that promote tumor growth (breast, liver, lung, stomach, esophagus)

Allylic sulfides

Allium foods (garlic, onion, leeks)

Thiol subclass, released when the plant is cut or smashed, antimutagenic and anticarcinogenic properties, immune and cardiovascular protection, antigrowth activity for tumors, fungi, parasites, cholesterol and platelets/leukocytes adhesion factors, activate liver detoxification enzyme system


35

Table 7 (continued) Phytochemical

Source

Function

Indoles

Cruciferous vegetables

Bind chemical carcinogens and activate detoxification enzymes mostly in the gastrointestinal tract

Isoprenoids

Citrus fruits

Neutralize free radicals, and protect membranes from oxidation

Lipoic acid and ubiquinone (coenzyme Q)

Potatoes, peanuts, spinach

Important antioxidant that works to extent the effect of other antioxidants, efficient hydroxyl radical quencher. Lipoic acid protect also superoxide dismutase, catalase and glutathione peroxidase which are important endogenous enzymes in liver detoxification activities

Catechins, gallic acid

Green and black tea, fruits, vegetables

Antimutagenic and anticarcinogenic properties, immune and cardiovascular protection

Of interest is the fact that the algae (S. scoparium) had an undetectable quantity of ␣-tocopherol, a small amount of total phenols, but it had a good antioxidant activity, EC50 ⫽ 2.367 ⫾ 0.19, most likely due to the presence of other antioxidants, and contained higher amounts of K, Na, Ca and Mg compared to the other wild plants in this study. All the wild plants examined contained small amounts of nitrates ranging between 8 ⫾ 0.002 and 203 ⫾ 0.016 mg/100 g wet weight, and considerable amounts of minerals. The nutrient content of wild plants is higher than the cultivated ones. There is evidence from other studies that the nutrient content of our food supply is decreasing. Mayer [64] compared the mineral content of 20 fruits and 20 vegetables from 1936 to the 1980s, using a special methodology to ensure that comparable laboratory methods were employed. Over that 50-year period, there were statistically significant decreases of calcium, magnesium, copper and sodium in vegetables, and of manganese, iron, copper and potassium in fruits. Zinc was not studied. The magnitude of some changes was large: the copper level in vegetables in the 1980s was less than 20% of the 1936 levels. Mayer [64] attributed these changes to the fact that agriculture relies on fertilizers containing only nitrogen, phosphorous and potassium, and there is little effort to remineralize the soil over the decades. Although the essential fatty acids were not specifically investigated in this study, Guil et al. [65] as well as Simopoulos et al. [3–5], Zeghichi et al. [22] and Freiberger et al. [66] have found the wild plants to have higher amounts of


36

␣-linolenic acid than cultivated ones. Recent studies indicate that wild plants contain squalene in significant amounts [67, 68]. Squalene has been reported to be a quencher of singlet oxygen and a free radical scavenger [69]. As an oxygen carrier it has been extensively researched and found to play a key role in maintaining health [70–72]. In summary, there are many reasons to include wild plants in our diet, and support and expand their cultivation worldwide. A recent study by Singh et al. on the effect of an Indo-Mediterranean diet on progression of coronary artery disease in high risk patients (Indo-Mediterranean Diet Heart Study), a randomized single-blind trial, supports these concepts [73]. Conclusion

From this study we conclude that the 25 commonly eaten wild plants in Crete contained considerable amounts of antioxidants and appreciable amounts of calcium, iron, zinc, magnesium and potassium in addition to their low content of nitrates and sodium. Taking into consideration the current recommended dietary allowances (RDAs), these wild plants could contribute largely to the human diet, especially in terms of essential fatty acids, antioxidants and minerals. Thus, the diet of Crete may be a reference standard for modern human nutrition and a model for defense against diseases of affluence. It should be emphasized that more studies are required on biochemical and molecular, ethno-botanic and phytogenetic aspects of the wild plants, and more research is needed on their special potential regarding the prevention and treatment of chronic-degenerative diseases by increasing the dietary intake of wild plants in both developed and developing countries. References 1 2 3 4 5

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57 58 59

60 61

62

63

64 65 66

67

68 69

70 71 72

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Rose DP, Boyar AP, Wynder EL: International comparison of mortality rates for cancer of breast, ovary, prostate and colon and per capita food consumption. Cancer 1986;58:2363–2371. Franceschi S, Favero A, La Vacchia C, Negri E, Conti E, Montella M, Giacosa A, Monni O, Decarli A: Food groups and risk of colorectal cancer in Italy. Int J Cancer 1997;72:56–61. Smart RC, Huang MT, Chang RL, Sayer JM, Jerina DM, Conney A: Disposition of naturally occurring antimutagenic plant phenol, ellagic acid and its synthetic derivatives 3-o-decylellagic acid and 3,3⬘-di-o-methylellagic acid in mice. Carcinogenesis 1989;1663–1667. Knekt P, Jarvinen R, Seppanen R, Hellovaara M, Teppo L, Pukkala E, Aromaa A: Dietary flavonoids and the risk of lung cancer and other malignant neoplasms. Am J Epidemiol 1997;146:223–230. Stefani ED, Boffetta P, Deneo-Pellegrini H, Mendilaharsu M, Carzoglio JC, Ronco A, Olivera L: Dietary antioxidants and lung cancer risk: A case-controlled study in Uruguay. Nutr Cancer 1999; 34:100–110. Fotsis T, Pepper MS, Aktas E, Breit S, Rasku S, Adlercreutz H, Wahala K, Montesano R, Schweigerer L: Flavonoids, dietary-derived inhibitors of cell proliferation and in vitro angiogenesis. Cancer Res 1997;57:2916–2921. Nakashima H, Murakami T, Yamamoto N, Sakagami H, Tanumo S, Hatano T, Yoshida T, Okudo T: Inhibition of human immunodeficiency viral replication by tanins and related compounds. Antiviral Res 1992;18:91–103. Mayer AB: Historical changes in the mineral content of fruits and vegetables. Br Food J 1997;99: 207–211. Guil JL, Torija ME, Gimenez JJ, Rodriguez I: Identification of fatty acids in edible wild plants by gas chromatography. J Chromotogr A 1996;719:229–235. Freiberger CE, Vanderjagt DJ, Pastuszyn A, Glew RS, Mounkaila G, Millson M, Glew RH: Nutrient content of the edible leaves of seven wild plants from Niger. Plant Foods Hum Nutr 1998;53:57–69. Guil-Guerrero JL, Garcia-Maroto F, Campra-Madrid P, Gomez-Mercado F: Occurrence and characterization of oils rich in ␥-linolenic acid. II. Fatty acids and squalene from Macaronesian Echium leaves. Phytochemistry 2000:54:525–529. Marcone MF: First report of the characterization of the threatened plant species Amaranthus pumilus (seabeach amaranth). J Agric Food Chem 2000;48:378–382. Kohno Y, Egawa Y, Itoh S, Nagaoka S, Takahashi M, Mukai K: Kinetic study of quenching reaction of singlet oxygen and scavenging reaction of free radicals by squalene in n-butanol. Biochim Biophys Acta 1995;1256:52–56. Kelly GS: Squalene and its potential clinical uses. Altern Med Rev 1999;4:29–36. Rao CV, Newmark HL, Reddy BS: Chemopreventive effect of squalene in colon cancer. Carginogenesis 1998;19:287–290. Smith TJ, Yang GY, Seril DN, Liao J, Kim S: Inhibition of 4-(methylnitrosaminol)-1-(3-pyridyl)1-butanone induced lung tumorogenesis by dietary olive oil and squalene. Carcinogenesis 1998; 19:703–706. Singh RB, Dubnov G, Niaz MA, Ghosh S, Singh R, Rastogi SS, Manor O, Pella D, Berry EM: Effect of an Indo-Mediterranean diet on progression of coronary artery disease in high risk patients (Indo-Mediterranean Diet Heart Study): A randomised single-blind trial. Lancet 2002; 360:1455–1461.

Artemis P. Simopoulos, MD President, The Center for Genetics, Nutrition and Health, 2001 S Street, N.W., Suite 530, Washington, DC 20009 (USA) Tel. ⫹1 202 462 5062, Fax ⫹1 202 462 5241, E-Mail [email protected]


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Kanjero (Digera arvensis) and Drumstick Leaves (Moringa oleifera): Nutrient Profile and Potential for Human Consumption Subadra Seshadri, Vanisha S. Nambiar Department of Foods and Nutrition (A WHO Collaborating Centre for Nutrition Research), Maharaja Sayajirao University of Baroda, Vadodara, India

Introduction

India is a vast country with a total land area of 3,287,263 km2 divided into seven physiographic regions, most of them with diverse flora and fauna. Several tribal belts in the country depend on locally produced foods for a substantial part of their food and nutrition requirements. We carried out a detailed study in the Western State of Gujarat, India, to identify all vegetables and fruits grown in rural and tribal Gujarat in an attempt to develop a seasonal calendar of plant foods that are rich sources of carotenoid pigments and particularly ␤-carotene. During this search, we found two leafy greens that had great potential to be used for human consumption but were not sold in the market outlets. We report here on the nutritional profile of these two leafy greens – kanjero leaves (Digera arvensis) and drumstick leaves (Moringa oleifera) – and their potential for meeting the nutritional needs of our population

Kanjero Leaves (D. arvensis)

Kanjero (D. arvensis) (fig. 1) grows as an annual herb, becoming perennial, usually 1–2 ft in height with smooth branches, which are often ovate and rounded at the tip with a reddish margin on occasions. The branches are

Fig. 1. Fresh kanjero (Digera arvensis) leaves.

attached to the stem by smooth stalks (petioles) 0.5–1 inch long. The flowering season is from September to November and they bear yellowish fruits 1/10–1/8 inch long [1]. Drumstick Leaves (M. oleifera)

Drumstick (M. oleifera) is a tree, usually 8–15 m tall and vigorous with a soft wood and tuberous taproot (fig. 2). During the longer day length conditions throughout the year in regions close to the equator, the tree produces copious flowers that are cream in color (fig. 3). Leaves are dark green when mature (fig. 4). The more tender leaves are preferred for human consumption as they are less fibrous. The tree produces long pods, 12–20 inches in length (30–50 cm) containing winged seeds 1 cm in diameter. The fleshy portion of the pods is most commonly consumed as a vegetable [2]. Geographic Distribution and Origin of Kanjero and Drumstick

Kanjero Kanjero herbs are distributed throughout India and are commonly seen after the rains especially in the eastern and northwestern provinces of India and the western peninsula in which Gujarat is situated. The kanjero herbs are also

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Fig. 2. Drumstick (Moringa oleifera) tree.

Fig. 3. Drumstick flowers.

prevalent in Sri Lanka, Afghanistan, Baluchistan, Arabia and some parts of Africa. It requires little maintenance for growth and is easily propagated by seed dispersion [1]. Kanjero leaves are used as cattle feed in Gujarat but they also form a part of tribal peoples’ diet, especially when other plant foods are scarce. Feeding cattle the leaves as a part of the diet quite regularly indicates that consumption of these leaves is without any harm. Drumstick Drumstick, which is native to India, has been introduced over the years to many other parts of the tropics. It is currently common in several countries of

Kanjero and Drumstick Leaves: Nutrient Profile and Potential for Human Consumption

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Fig. 4. Drumstick leaves.

tropical Asia, Indonesia, Philippines and the Caribbean. Drumstick trees are drought-tolerant (originally from hot, semiarid tropical areas with an annual rainfall of 250–1,500 mm). They are also well adapted to hot, humid and wet conditions. They thrive under a variety of soil conditions from heavy clays to sandy soils [2]. Drumstick leaves, flowers and pods are all included in the diet although the most commonly eaten portion is the flesh of the pod.

Green Leaves as a Source of Valuable Nutrients and Bioactive Molecules

Several studies have indicated green leafy vegetables (GLVs) as a group to be important sources of nutrients required for growth and maintenance. Besides being rich sources of ␤-carotene, these greens also contribute a significant amount of other minerals, such as iron, calcium, phosphorous [3] and zinc, and provide substantial amounts of vitamins such as ascorbic acid and folic acid [4]. Oke [5] suggested that intake of GLVs could be expected to contribute a large proportion of the calcium and phosphorous requirements, particularly when used as a meat substitute.

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GLVs are now recognized as rich sources of ␻–3 fatty acids and several antioxidants such as flavonoids and small molecular compounds like glutathione [6, 7] which play a protective role against many degenerative diseases. Simopoulos et al. [7] have shown that purslane (a species of Portulaca oleracea) distributed widely around the world, growing either wild or in kitchen gardens but not sold in markets, is an excellent source of ␣-linolenic acid, vitamin E, vitamin C, ␤-carotene, glutathione, potassium and pectin, all of which may contribute to its reported therapeutic value as a cardiac tonic, diuretic, and as a medicinal plant for skin infections and gastrointestinal disorders. Based on the composition and the medicinal attributes, some have suggested that ‘purslane may be a power food of the future’ [7, 8]. It has also been recommended that purslane and other wild plants ought to be incorporated in the diet of human beings, both in developed and developing countries.

Green Leaves Consumed by the Tribal Population in the Western State of Gujarat, India

Nutritional deficiencies are very rampant in India, the most vulnerable to the deficiencies being young children. A recent national family health survey [9] has shown that anemia due to iron deficiency is of much greater prevalence in young children compared to other vulnerable groups such as pregnant women or reproductive age women who have been traditionally the target population for remedial measures [10]. Vitamin A deficiency in India occurs most commonly in young children for whom milk is unaffordable and GLVs, a source of ␤-carotene, are inaccessible because the mothers do not prepare them appropriately for children [11]. Besides these, zinc deficiency may also be common. A diet that provides these micronutrients, additional valuable bioactive compounds like antioxidants and essential fatty acids of ␻–6 and ␻–3 series, and adequate in macroconstituents is the answer to these problems. It is therefore important to identify vegetable foods of high value, such as leafy greens that are native to a region, and establish their nutritional profile. This is particularly relevant to the tribal belts in India where a variety of leafy vegetables are grown for household consumption in their backyards or they are picked from the wild, but these are not commercially exploited, as they are not sold in the market. The leaves could well be a repository of important microconstituents that can provide nutritional support and optimize health and wellbeing with a potential for world agriculture. Our studies in the tribal belt of Western India in Gujarat showed that there were several uncommon green leaves used for both human and animal consumption and these are shown in table 1 [11].


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Table 1. Inventory of ␤-carotene rich GLVs [from 11] No.

Common name

English name

Botanical name

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29

Arvi-na-paan Asadio Baraf-ni-bhaji Bhindi leaves Chana-na-paan Chil Dhala-ni-bhaji Fang-ni-bhaji Fudina Jharakhala Kakadi-na-paan Kanjero Khatedo Khati luni-ni-bhaji Kuba Kuvadiyo Lasan Leela dhana Limdo (mitho) Luni Methi-ni-bhaji Muda-ni-bhaji Nala-na-paan Piludi-na-paan Poi Sarasiya-ni-bhaji Suva-ni-bhaji Palak Tandelo/Tandarjo

Colocasia Garden cress – Ladies’ finger leaves Bengalgram leaves Bathua – – Mint Amaranth Cucumber leaves – – – – – Garlic stalks Coriander leaves Curry leaves – Fenugreek leaves Radish leaves – Manathakkali leaves Mayalu Mustard leaves Shepu Spinach Amaranth

Colocasia antiquorum Lepidium sativum – Abelmoschus esculentus Cicer arietinum Chenopodium album – Rivea hypocrateri forms Mentha spicata Amarantus spp. Cucumis sativus Digera arvensis Tianthama monogyna Portulaca quadrifida Leucas aspera Cassia tora Alluim sativum Coriandrum sativum Murraya koemigii Portulaca quadrifida Trigonella foenum Raphanus sativus Ipomea reptans Solanum nigrum Basella rubra Brassica compestris Peucedanum graveoleus Spinacia oleracea Euphobia hirta

Consumption Pattern and Medicinal Uses of Kanjero and Drumstick Leaves

Both kanjero and drumstick leaves are consumed by animals as well as humans. Drumstick leaves are used in South India for the preparation of curry and ‘sambhar’. It is also consumed as ‘khicheri’ (rice and pulse mix preparation), and is added to wheat germ and rice porridge for children. In the Philippines, drumstick leaves are consumed as ‘shring suarn’, ‘dinengdeng II’, ‘mung bean guisado with drumstick’, ‘drumstick leaves with gulay’, and ‘picadillo with drumstick’.

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Table 2. Medicinal uses of drumstick and kanjero No.

Botanical name

Medicinal use

1

Drumstick leaves (Moringa oleifera)

Drumstick leaf juice is used for the prevention of respiratory disorders such as asthma, bronchitis and tuberculosis; for several sexual disorders, high blood pressure, for glossy and lustrous hair, extract from leaves mixed with warm milk is used as a tonic to purify blood and build strong bones

2

Kanjero leaves (Digera arvensis)

Useful in urinary discharges, plant is a laxative in high doses, used in the treatment of dyspepsia, used as famine food

Kanjero leaves are sautéed in oil and used alone or with spinach or fenugreek leaves, and consumed as a ‘bhaji’ (vegetable) or added to ‘dal’ (a cooked pulse) preparation in Western India. The medicinal uses of kanjero and drumstick leaves as articulated by the tribal people of Western India are shown in table 2 [3]. Besides the leaves, other uses of the drumstick tree abound in India and other places where almost every part of the tree is put to use for different purposes, such as the wood and gum are used in dyeing and printing, and the seed powder is used for clarifying honey. Incorporating drumstick leaves into the soil before planting can prevent damping off disease (Pythium debaryanum) among seedlings.

Nutrient Composition of Kanjero and Drumstick Leaves

Total and b-Carotene Total and ␤-carotene were estimated in the lipid extracts of the fresh samples of the two leaf species. Total carotene was quantitiated using spectrophotometry while ␤-carotene was characterized and quantified using HPLC. The samples were extracted immediately after collection, taking necessary precautions to avoid isomerization and oxidation. Standards were from Hoffmann-La Roche, Basel, Switzerland and solvents used were of analytical and HPLC grade. Recovery experiments, chromatography and calibration curves were established each time a set of samples was analyzed. The details of collection of sample, processing and methods of analysis are described in a previous paper [10].


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Table 3. Nutrient composition of kanjero and drumstick leaves as compared with some commonly consumed GLVs of India Nutrients

Kanjero

Drumstick

Spinach

Fenugreek

Radish leaves

Moisture, % Total carotene (TC) ␮g/100 g FW ␤-Carotene (BC) ␮g/100 g FW BC % TC Ascorbic acid, mg/g DW Total iron, mg/g DW Calcium (Ca), mg/g DW Phosphorus (P), mg/g DW Ca:P ratio Oxalic acid, mg/g DW Ca:oxalic acid ratio

81.9 17,150

79.2 40,139

90.0 12,896

85.1 24,352

91.7 11,930

14,390

19,210

2,851

10,226

6,540

83.9 5.5 0.38 34.4 3.5 9.9:1 64.3 0.53:1

47.8 6.6 0.26 22.4 6.3 3.6:1 11.2 2:1

22.1 3.1 0.72 15.1 2.4 6.3:1 46.0 0.33:1

41.9 4.0 0.53 24.6 6.5 2:1 11.8 2:1

54.8 7.2 1.25 29.3 5.7 6.9:1 11.2 2.62:1

Drumstick leaves are literally a rich repository of both total and ␤-carotene (40,139 ␮g/100 g fresh weight (FW) of total carotene and 19,210 ␮g/100 g FW of ␤-carotene), containing 3 times more total carotenoid pigments and 7 times more ␤-carotene compared to spinach (table 3). Kanjero leaves, similarly, had much higher levels of total and ␤-carotene, 1.5 and 5 times more than spinach, respectively. Fenugreek leaves had total- and ␤-carotene that was intermediate in values between kanjero, drumstick and spinach. Given the wide prevalence of vitamin A deficiency in children in India, drumstick and kanjero leaves, appropriately used, can go a long way in mitigating the problem. Furthermore, since ascorbic acid helps to achieve better stability of carotenoids in food systems [12], the ␤-carotene in kanjero and drumstick can be expected to have a good bioavailability, which has indeed been shown by us for drumstick leaves [20]. Thus the two antioxidant vitamins, ascorbic acid and ␤-carotene, are provided in generous quantities by kanjero and drumstick leaves. Ascorbic Acid The fresh leaves are usually characterized by moderate to high levels of ascorbic acid, as reported for a range of leafy vegetables in the Indian food composition tables (6.5–9.7 mg/g dry weight (DW)). The ascorbic acid content of kanjero leaves was 5.5 mg/g DW (99.55 mg/100 g FW), while that of drumstick leaves was even higher, 6.6 mg/g DW (137.28 mg/100 g FW), (table 3) compared to spinach leaves 3.1 mg/g DW and fenugreek leaves

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4.0 mg/g DW commonly consumed in India. The ascorbic acid content in kanjero and drumstick leaves was 1.5–2 times higher compared to spinach and fenugreek leaves. Ascorbic acid not only acts as an antioxidant by itself but also protects vitamin E from oxidation, thus making available the ␣-tocopherol for free radical scavenging actions. The high content of ascorbic acid in these two leaves makes them good sources of ascorbic acid even after accounting for losses after cooking or common processing methods as shown in a later section. The less commonly consumed kanjero and drumstick leaves had much higher levels of ascorbic acid compared to the domesticated cultivars of spinach and fenugreek.

Calcium, Phosphorus and Iron Content of Kanjero and Drumstick Leaves

Besides being rich sources of ascorbic acid and ␤-carotene, our analysis showed that these two leafy vegetables also contained generous amounts of the minerals, calcium, phosphorous and iron (table 3). The three minerals were estimated in the ashed samples of the dried leaf powder using standard procedures [13]. Results were expressed as mg/g DW as well as mg/100 g FW. Calcium and Phosphorus Kanjero leaves contained 34.4 mg calcium/g DW (equivalent to 622.64 mg/ 100 g FW) while phosphorus content was 3.5 mg/g DW (63.35 mg/100 g FW). Drumstick leaves had a lower level of calcium 22.4 mg/g DW (465.92 mg/100 g FW). Phosphorus content was 6.3 mg/g DW (131.04 mg/100 g FW). However, both these leaves had 1.5–2 times higher calcium compared to spinach. Drumstick leaves are seen to be comparable with the commonly consumed fenugreek leaves as well as the less commonly consumed radish leaves in their calcium and phosphorus content, while kanjero leaves had the highest level of calcium and somewhat lower level of phosphorus in comparison with these (table 3). Iron Iron content was also higher in kanjero leaves 0.38 mg/g DW (6.87 mg/100 g FW) compared to drumstick leaves 0.26 mg/g (5.4 mg/100 g FW) (table 3) [3]. Spinach, fenugreek and radish leaves in comparison had much higher levels of iron. Oxalic Acid Since green leaves generally contain high amounts of oxalic acid that can interfere with absorption of several minerals such as Ca, Mg and iron, we determined the oxalic acid content of both kanjero and drumstick leaves.


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For comparison, spinach, fenugreek and radish leaves were analyzed. Interestingly, drumstick leaves contained lower quantities of oxalic acid compared to spinach but kanjero leaves had 1.5 times higher oxalic acid than spinach (table 3). Apparently the high levels of oxalic acid in conjunction with calcium will probably render a significant proportion of the calcium in kanjero leaves unavailable but even so because of the much higher levels of calcium in these leaves, they can still serve as a good source of calcium. Some of the oxalic acid in the leaves can be removed by appropriate cooking procedures to make kanjero leaves more acceptable. Overall, drumstick leaves emerged as superior, containing the highest level of the two antioxidant nutrients, ␤-carotene and ascorbic acid and as well as having the highest level of carotenoid pigments compared to either kanjero or the commonly consumed leafy vegetables such as spinach or fenugreek leaves. Further, drumstick leaves were a good source of calcium and phosphorus and contained relatively low levels of oxalic acid, only one fourth that in spinach, making the calcium potentially better available. Although iron content in drumstick leaves was only one third of that in spinach and one half of that in fenugreek leaves, the iron availability is likely to be higher in view of the high levels of ascorbic acid. Drumstick leaves had the highest level of ascorbic acid. Recent studies have shown that antioxidant nutrients, ␤-carotene, ascorbic acid and vitamin E all have a potential significant role in reducing mortality and morbidity due to coronary heart disease and cancer [6]. In fact it is clear now that fresh vegetables and fruits, which are high in these nutrients and other antioxidants, have the greatest protective effect rather than isolated single nutrients in large quantities.

Other Chemical Components of Kanjero and Drumstick Leaves

The interest in food phenolics owes its origin to vitamin ‘P’, a group of polyphenols better known as permeability factors, which may exhibit some pharmacological activity. A knowledge of the phenols and their possible role in digestive processes would help to ascertain the beneficial/toxic effects of these compounds. The distribution of flavonoids, phenolic acids, saponins and steroids in kanjero and drumstick leaves is shown in tables 4–6. As seen, predominant flavonoids of kanjero species are 3⬘-OMe quercetin, 3⬘,4⬘-di-OMe quercetin and 4⬘-OMe quercetin. The major phenolic acids present in kanjero are vanillic and syringic acids. These plants also contained saponins and phytoecdysones and ecdysterone. However, no tannins, quinones and proanthocyanidins were detected in kanjero [14].

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1 2 3 4 5 6 7 8 9 10 11 12 13 14 15

4⬘-OMe apigenin Luteolin 3⬘-OMe luteolin 4⬘-OMe luteolin 3⬘-4⬘-di-OMe luteolin 3⬘-OMe kaempferol 4⬘-OMe kaempferol 7⬘,4⬘-di-OMe kaempferol Quercetin 3⬘-OMe quercetin 3⬘,4⬘-di-OMe quercetin 4⬘-OMe quercetin Vitexin Isovitexin 6⬘-C-glycoside of acacetin

⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫹ ⫹ ⫹ ⫺ ⫺ ⫺

Table 4. Distribution of flavonoids in kanjero (Digera arvensis) [from 14]

⫹ ⫽ Present; ⫺ ⫽ absent.

1 2 3 4 5 6 7 8 9 10 11 12 13 14

Apigenin 3⬘,4⬘-di-OMe luteolin Kaempferol 4⬘-OMe kaempferol 7⬘,4⬘-di-OMe kaempferol Quercetin 3⬘-OMe quercetin 4⬘-OMe quercetin 3⬘,4⬘-di-OMe quercetin Gossypetin Quercetagetin Proanthocyanidins Anthocyanins Coumarins

⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫹ ⫺ ⫺ ⫹ ⫹ ⫹ ⫺ ⫺

Table 5. Polyphenol content of drumstick leaves (Moringa oleifera) [from 17]

⫹ ⫽ Present; – ⫽ absent.

The distribution of flavonoids and their related compounds in M. oleifera is presented in table 5 [17]. The drumstick leaves contained various flavonoids such as 3⬘-OMe quercetin 6/8, hydroxylated flavonols such as gossypetin, quercetagetin and proanthocyanidins. According to De Eds [15], the flavonoids with free hydroxyl groups at the 3⬘,4⬘ positions (quercetin, gossypetin, quercetagetin) present in the kanjero and drumstick leaves exert beneficial effects on the


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1 2 3 4 5 6 7 8 9 10 11 12 13 14

Vanillic acid Syringic acid p-OH benzoid acid Melilotic acid Gentisic acid p-Coumaric acid Ferulic acid Phloretic acid Chlorogenic acid Resorcylic acid o-Coumaric acid Saponins Steroids Alkaloids

⫹ ⫹ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫹ ⫹ ⫺ ⫺

Table 6. Distribution of phenolic acids, saponins, steroids and alkaloids in kanjero (Digera arvensis) [from 14]

⫹ ⫽ Present; ⫺ ⫽ absent.

capillaries by (1) chelating metals and thus sparing ascorbate from oxidation; (2) prolonging epinephrine action by inhibiting O-methyltransferase, and (3) stimulating the pituitary-adrenal axis. Some of these flavonoids such as 3⬘,4⬘-di-OMe quercetin present in kanjero leaves, play an important role in the circulatory system by reducing aggregation of erythrocytes (which occur during illness or injury) by site-specific membrane surface effects, and improve the microcirculation within the body [16]. Drumstick leaves, like purslane, contained higher levels of carotenes and ascorbic acid, comparable levels of iron, with lower oxalic acid and high levels of certain polyphenolic compounds. The fatty acid profile and ␣-tocopherol content of these leaves will have to be investigated.

Studies on Dehydration of Kanjero and Drumstick Leaves

Due to the seasonal nature of greens and unavailability in certain areas, it was essential to devise low-cost simple technologies which would retain maximum nutrients and ensure year round availability. Several methods of dehydration for GLVs such as sun, electric cabinet, and shade drying (with or without pretreatments) have been reported in the literature that result in varying losses of nutrients, color, texture and flavor [17–19]. In view of the nutritional richness of drumstick leaves, we carried out further studies on low-cost preservation technologies to convert them into a less bulky and more compact dehydrated powder form which lends itself to easy

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Table 7. Retention of ␤-carotene content of kanjero leaves on shade dehydration (mg/100 g FW ⫾ SE) b-Carotene (mg/100 g FW) Fresh 0 day of dehydration 15th day of dehydration 30th day of dehydration F Cal value LSD

14.39 ⫾ 0.439 9.5 ⫾ 0.075 8.50 ⫾ 0.106 7.13 ⫾ 0.085 143.318 0.810

Retention as % fresh 0 day 15th day 30th day

66.0 59.1 49.6

incorporation in the large supplementary feeding programs in India. The continuing debate on the bioavailability of carotenes from plant foods to act as a source of vitamin A also necessitated investigation on the relative bioavailability of ␤-carotene in fresh and dehydrated drumstick leaves. We describe these studies below.

Dehydration and Nutrient Retention

Studies conducted to assess the retention of ␤-carotene in shadedehydrated kanjero leaves at different periods of storage indicated that 66% of ␤-carotene was retained on day 0 of dehydration as compared to 49.6% after 30 days of storage (table 7). A study conducted in this laboratory on blanched and sulphited shadedehydrated drumstick leaves [18] found that 50% of ␤-carotene (i.e. 9,605 ␮g/ 100 g FW) was retained in the sulphited and shade-dried drumstick leaves even after 3 months of storage, which would still be of value as a source of provitamin A (table 8). The dehydrated drumstick leaf powder could be rehydrated very satisfactorily, and traditional recipes developed from shade-dried drumstick leaves were also judged as highly acceptable by a panel of semitrained judges [18]. Retention of iron, calcium, phosphorous, oxalic acid and tannic acid in kanjero leaves after steam blanching, sulphiting and shade dehydration was studied after 0, 15 and 30 days of dehydration and storage in polyethylene pouches at room temperature. Table 9 shows that 78% iron was retained after blanching, sulphiting and shade dehydration which reduced to 68% after


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Table 8. Retention of total carotene, ␤-carotene and ascorbic acid in the dehydrated drumstick leaves at different stages of storage given two pretreatments (mg/100 g FW) (mean ⫾ SE) Nutrients/ Fresh pre-treatments

Days of storage 0

30

60

90

Total carotene 27.1 ⫾ 0.27 16.7 ⫾ 0.16 (62) B – * B⫹S – 19.8 ⫾ 0.16 (73)

13.4 ⫾ 0.39 (50) 12.7 ⫾ 0.62 (47) 12.6 ⫾ 0.14 (47) * * * 18.7 ⫾ 0.31 (69) 18.2 ⫾ 0.35 (67) 16.0 ⫾ 0.10 (59)

␤-Carotene B B⫹S

8.9 ⫾ 0.41 (51) 8.3 ⫾ 0.10 (48) 8.1 ⫾ 0.07 (47) * * NS 11.1 ⫾ 0.34 (64) 10.2 ⫾ 0.20 (59) 9.1 ⫾ 0.39 (53)

17.4 ⫾ 0.36 10.2 ⫾ 0.28 (59) – * – 12.5 ⫾ 0.11 (72)

Ascorbic acid 143.6 ⫾ 4.2 38.7 ⫾ 0.48 (27) 25.8 ⫾ 0.48 (18) 18.6 ⫾ 0.64 (13) 9.8 ⫾ 0.29 (7) B – * * * * B⫹S – 125.4 ⫾ 1.65 (87) 90.4 ⫾ 0.73 (65) 70.9 ⫾ 1.72 (49) 62.0 ⫾ 0.97 (43) Values are mean ⫾ SEM of three independent samples. Retention as percentage of fresh in parentheses. *Significantly higher than the blanched-only values p ⱕ 0.01. B ⫽ Blanched; B ⫹ S ⫽ blanched ⫹ sulphited.

Table 9. Retention of iron, calcium, phosphorous, oxalic acid and tannic acid as percent fresh weight of kanjero leaves on shade dehydration and storage Retention as percentage of fresh

Iron Calcium Phosphorous Oxalic acid Tannic acid

day 0

15 days’ dehydration

30 days’ dehydration

78.0 100 92.9 69.7 71.9

69.5 100 91.0 67.9 68.8

68.4 100 89.0 66.5 67.5

30 days of storage. Small losses in iron could be ascribed to the leaching out of a portion of the soluble solids during the sulphiting process. Kanjero leaves retained 100% calcium after dehydration and storage, however some amount of loss in the phosphorous content was noted which may be due to the effect of pretreatments prior to dehydration [19]. Significant loss of oxalic acid was

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Fig. 5. Dehydrated kanjero leaves.

noted in kanjero on day 0 of dehydration (36%) which was due to removal of water-soluble oxalic acid during steam blanching and sulphiting [19]. Twentyeight percent loss in tannic acid was observed after dehydration on day 0 in kanjero leaves which increased to 32% after 1 month of storage. The percent retention of iron in dehydrated kanjero leaves was 60% after 30 days of storage.

Organoleptic Acceptability of the Fresh and Dehydrated Kanjero and Drumstick Leaves in Local Recipes

Culinary practices are influenced by tradition and taste preferences. Dehydrated kanjero (fig. 5) and drumstick leaf recipes were prepared using several locally acceptable methods. They were mixed with a common vegetable such as spinach, tomato or potato, seasoned with oil and spices such as onions, green chilies and ginger-garlic were added [3]. A multicentric study in India on use of carotene-rich foods to combat vitamin A deficiency revealed that although no specific like or dislike for GLVs emerged, the form in which the GLVs were made did have an influence on children’s intake [11]. Most of the mothers reported that children preferred the GLVs when they were incorporated into the cereal-pulse dough as used in several traditional recipes such as bhajyas (chopped leaves added to a thick batter of bengalgram powder, made into balls and deep fried); muthias (incorporated into cereal batter, steamed and sautéed), patras, handwa or dhebra (mixed with pulse powder and shallow fried) baked or shallow fried. Household processing of vegetables involves several steps during which the leaves are often exposed to elevated temperatures, high or low pH levels, oxygen and light which accelerate the oxidative destruction of carotenoids and result in loss of several other nutrients. Thus the


55

nutrient content of unprocessed raw GLVs are not necessarily indicative of how much carotene is consumed. Three common household level methods of processing were tested for their effects on retention of carotene from drumstick leaves. The three recipes were ‘dhebra’ (cereal flour ⫹ drumstick leaves and spices, rolled into pancakes and shallow fried on a flat iron pan with oil); ‘muthia’ (cereal ⫹ pulse flour ⫹ drumstick leaves ⫹ spices – pressure-cooked rolls later cut into small pieces and sautéed) and ‘dal soup’ (pulse ⫹ drumstick leaves ⫺ boiled). The retention of ␤-carotene was highest in the pressure-cooked, cereal-pulse recipe, ‘muthia’ (73%), followed by shallow fried ‘dhebra’ (69%) and the lowest retention was found in dal soup (35%). One serving of each recipe could meet 168, 100 and 43% of Indian RDA for pre-schoolers respectively [18]. Bioavailability of ␤-Carotene from Fresh and Dehydrated Drumstick Leaves

Bioavailability trials using fresh and dehydrated drumstick leaves were conducted on vitamin-A-deficient rats and the results compared with the bioavailability of synthetic vitamin A [20]. A significant improvement was seen on repletion with fresh as well as dehydrated drumstick leaf diets as assessed by clinical signs and symptoms, food intake, body weight, serum and liver vitamin A and these were comparable with the rats repleted with synthetic vitamin A. These results clearly indicated that ␤-carotene from drumstick leaves was effective in overcoming vitamin A deficiency both in the fresh and dehydrated form.

Agricultural Potential of the Leaves

India is endowed with 21,000 flowering plant species and about 20% of such plants are of food value. Plants such as kanjero and drumstick, which provide sustenance to man at times of scarcity, are of great significance. Kanjero plants are easily propagated via seeds and grow quickly as they do not require any specific climatic condition. Drumstick trees are very promising multipurpose agroforestry species due to their easy cultivation, fast growth and adaptation to a wide range of environmental conditions. Drumstick trees produce light shade, allowing shade-tolerant crops to be grown underneath their canopy. Moringa trees are planted as borders around pastures and agricultural lands, roadsides and as a living fence. The Moringa tree is an effluent accumulator of

Seshadri/Nambiar

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nutrients and most likely has an important mycorrhyzal relationship. These species can be propagated using either seeds or cuttings. Sprouting takes place within 2–3 weeks. Drumstick trees, being multipurpose (yielding food, fodder, fuel wood, fiber, etc.), have been identified by the National Social Forestry Programme launched during the 5th Five-Year Plan for promotion through strip plantations, afforestation and waste land plantations [21]. Among the vegetables of the world, Moringa leaves stand out as one of the most highly nutritious and ecofriendly.

Potential of the Leaves for Use in Supplementary Feeding Programs

In several States of India, children are recipients of National Supplementary Feeding programs. The Integrated Child Development Services (ICDS) program covers around 4,000 administrative blocks of India covering a population of 200 million. These programs currently emphasize the protein and calorie gaps of the vulnerable population. Several studies have reported that inclusion of micronutrient-rich foods such as red palm oil, garden cress seeds, spinach and other greens in these supplementary feeding programs have brought about a beneficial effect on the nutritional status of the children, pregnant and lactating mothers [22]. We investigated the effectiveness of dehydrated drumstick leaves as a source of vitamin A in improving conjunctival impression cytology (CIC) in young children. Biscuits from dehydrated drumstick leaves were developed (362 RE vitamin A) and fed to 20 schoolchildren with abnormal CIC and compared with a group of children to whom synthetic vitamin A was given. The improvement in CIC noted on supplementation with dehydrated drumstick leaf biscuits was similar in magnitude to the synthetic vitamin A group, supporting the hypothesis that plant food sources are effective in correcting vitamin A deficiency [23]. Currently we are studying the feasibility of building linkages between the ICDS, non-governmental organizations (NGOs) and University. Technical expertise will be disseminated by the university, cooking of supplementary foods with dehydrated drumstick leaves will be supervised and monitored by the NGOs and the ICDS set-up will distribute the food to the vulnerable population of the community. Since drumstick leaves are easily available and are promoted under the social forestry scheme in India, they are the richest source of ␤-carotene 19,210 ␮g/100 g FW, and have been ranked as highly desirable as compared to several other greens analyzed in this laboratory and as they are


57

currently underutilized for human consumption, the feasibility of building linkages as stated above would prove to be a turning point in combating vitamin A deficiency in India.

References 1 2 3

4 5 6 7 8 9 10 11

12

13 14 15 16 17 18 19 20 21

22

Cooke T: The Flora of Presidency of Bombay. Calcutta, Botanical Survey of India, 1905, vol II. Ram J: TRIADES, Perennial vegetables, Leaflet No 9, Honolulu, ADAP Project, 1994. Nambiar VS: Studies on indigenous green leafy vegetables of Western India. Chemical analysis for selected nutrients, antinutrients, retention and bioavailability of ␤-carotene on processing; PhD thesis (unpubl). Vadodara, Department of Foods and Nutrition, Faculty of Home Science, Maharaja Sayajirao University of Baroda, 1998. Faboya O: The mineral content of some green leafy vegetables commonly found in the western parts of Nigeria. Food Chem 1983;12:213–216. Oke OL: Composition of some Nigerian leafy vegetables. J Am Diet Assoc 1968;58:130–132. Krinsky NE: Carotenoid protection against oxidation. Pure Appl Chem 1979;51:549. Simopoulos AP, Norman HA, Gillaspy JE: Purslane in human nutrition and its potential for world agriculture. World Rev Nutr Diet. Basel, Karger, 1995, vol 77, pp 47–74. Levey GA: The new power foods. Parade magazine. The Washington Post, Nov 14, 1993, p 5. NFHS: National Family Health Survey International Institute for Population Sciences, 2000. Nambiar VS, Seshadri S: ␤-Carotene content of selected green leafy vegetables of Western India by high-pressure liquid chromatography. J Food Sci Technol 1998;35:365–367. Seshadri S, Vanisha P, Gandhi H, Anand A, Dhabhai D: The GLV study of Western India (Baroda, Gujarat); in Seshadri S (ed): Use of Carotene-Rich Foods to Combat Vitamin A Deficiency in India – A Multicentric Study. New Delhi, Nutrition Foundation of India, 1996, Report No 12, pp 38–59. Bhaskaracharya K, Rao DSS, Deosthale YG, Reddy V: Interaction between ␤-carotene and other biologically active compounds in plant foods. Proceedings of XIXth IVACG Meeting, Durban, March 8–9, 2000. AOAC: Official Methods of Analysis of AOAC International, ed 16. Ed Arlington PC, Virginia, USA, 1995, vol I & II. Mangalam A, Daniel G: Indian J Botany 1988;11:206–209. Also: Bailey JM: The Leaves We Eat. SPC Handbook No 31, South Pacific Commission, Naumea, Caledonia, 1992. De Eds F, Florkin M, Stotz EH (eds): Comprehensive Biochemistry. Amsterdam, Elsevier, 1968, vol 20, p 127. Srinivasan S, Lucas T, Burrowes CB, Wanderman NA, Render A, Bernstein S, Sawyer PN: European Conference on Microcirculation 1971, vol 6, p 394. Daniel M: Polyphenols of some Indian vegetables 1989;58:1332–1334. Seshadri S, Jain M, Dhabhai D: Retention and storage stability of ␤-carotene in dehydrated drumstick leaves (Moringa oleifera). Int J Food Sci Nutr 1997;48:373–379. Fennema OR: Principles of Food Science. II. Physical and Food Preservation. New York, Academic Press, 1975, pp 187–195. Nambiar VS, Seshadri S: Bioavailability trials of ␤-carotene from fresh and dehydrated drumstick leaves (Moringa oleifera) in a rat model. J Plant Food Hum Nutr 2001;56:83–95. Tiwari DN: Forest, food and people; in Passi SJ, Kanna K, Pevri S (eds): Dietary Promotion of Vitamin A Rich Foods Through Agriculture, Horticulture and Social Farm Forestry. A Report. New Delhi, Institute of Home Economics, 1994. Devadas RP: Currently available technologies in India to combat vitamin A malnutrition; in West KP, Sommer A (eds): Delivery of Oral Doses of Vitamin A to Prevent Vitamin A Deficiency and Nutritional Blindness: A State-of-the-Art Review. Geneva, UN ACC Subcommittee on Nutrition, 1987.

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23

Ramachandran R, Nambiar VS, Seshadri S: Impact of dehydrated drumstick leaf biscuits on vitamin A status of children as assessed by conjunctival impression cytology. Proceedings of XXth IVACG Meeting, Hanoi, Feb 12–15, 2001.

Vanisha S. Nambiar Department of Foods and Nutrition (A WHO Collaborating Centre for Nutrition Research), Maharaja Sayajirao University of Baroda, Vadodara 390002 (India) E-Mail [email protected]


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Ivy Gourd (Coccinia grandis Voigt, Coccinia cordifolia, Coccinia indica) in Human Nutrition and Traditional Applications Emorn Wasantwisut, Thara Viriyapanich Institute of Nutrition, Mahidol University, Salaya, Nakhon Pathom, Thailand

Introduction

Ivy gourd is a tropical plant in the family of Cucurbitaceae. Its scientific names are Coccinia grandis Voigt, Coccinia cordifolia, Coccinia indica Wight & Arn. (Syn.). Ivy gourd is an aggressive climbing vine that can spread quickly over trees, shrubs, fences and other supporters (fig. 1). It is an outdoor plant but prefers a sunny sheltered position and a sandy soil. Being a perennial plant, it can spread vegetatively or by seed. The stem is a herbaceous climber or perennial slender climber with occasional adventitious roots forming where the stem runs along the ground. Both roots and stems are succulent with the length of the rootstock as long as 5 cm. The tendrils are long, elastic with coil-like springy character that can wrap around the host to the entire length. The leaves are classified as palmately simple with five lobes while the shape varies from the heart to pentagon form. The size of the leaves is approximately 5–10 cm in width and length. The flower is large and white about 4 cm in diameter and contains five long tubular petals. Ivy gourd is a dioecious plant of which male and female flowers grow separately. Female flowers have a two-lobed stigma while the male flowers have long (6 mm) filamentous stamens. At least two plants of different sexes must be present to form a viable seed. The ivy gourd fruit belongs to the berry type: oval and hairless with thick and sticky skin. The raw fruit is green in color and turns bright red when it is ripe. The mature fruit is usually from 25 to 60 mm long by 15–35 mm in diameter and contains several pale, flattened seeds (6–7 mm long) [1, 2].

Fig. 1. Ivy gourd (Coccinia grandis Voigt).

While ivy gourd is considered a ‘common weed’ through its rampant growth in Australia and certain parts of the USA and ended up being destroyed, the South-East Asians have long made use of this plant in their local cookery and traditional medicine. Origin and Geographical Distribution

The origin of ivy gourd lies in the tropical zone of Asia, North and Central Africa. It is commonly found in countries like India, Indonesia, Malaysia, Philippines and Thailand. Ivy gourd has spread to Australia, especially the tropical and subtropical areas where small infestations were found in Broome, South Hedland, Arnhem Land and Queensland. In Micronesia, it is present in the Commonwealth of the Northern Mariana Islands (Saipan), Guam, Federated States of Micronesia and Republic of the Marshall Islands. Ivy gourd is also spotted in the Pacific Islands such as Fiji; Hawaii especially on Oahu and in the Kona/Kealakekua area of the Main Island; and Tonga and Vanuatu [3]. Ivy gourd is a common name whereas different countries have specific local names for this plant [1], such as: ‘Tum Leung’ in Thailand, ‘Kundree, Olekavi, Telacucha’ in India, ‘Pepasan’ in Malaysia, and ‘Pepasan, Boluteke’ in Indonesia. Medicinal Properties

Ivy gourd has been classified as one of the medicinal herbs in the traditional practice of the ancient Thai medicine. The claimed properties range from using

Ivy Gourd in Human Nutrition

61

the leaves, roots, stems and whole plant in the treatment of illness symptoms like skin eruptions, burns, insect bites, fever, indigestion, nausea and constipation, to diseases such as diabetes, various types of eye infections, allergies, gonorrhea, etc. [4, 5]. Similar properties were documented in India [6] that the juice of the roots and leaves is used to treat diabetes while the leaves are used as poultice to treat skin eruptions. In addition, the aqueous and ethanolic extracts of the plant have shown hypoglycemic action [6]. In a recent review from a local Indian journal, the hypoglycemic action of ivy gourd leaves was indicated when administered orally in a single dose [7]. However, all the forementioned properties still require solid evidence to support the claims that are primarily based on local wisdom and the practice of folklore medicine.

Indigenous Food

In Thailand, ivy gourd is a common plant and often used as canopies in gardens or on fences. The young leaves, long slender stem tips and tender green fruits of ivy gourd are commonly used in the local dishes of the northern, northeastern and central regions [4, 5, 8]. Young leaves and tips can be blanched for dipping with chili paste or stir-fried. The leaves and stems are usually added to clear soup dishes such as the porcine blood-curd soup, ivy gourd and minced pork soup, noodle soup with minced pork and ivy gourd, mixed vegetables soup – northern style (Gang Khae) or central style (Kang Lieng), etc. Young leaves of ivy gourd can be boiled with porridge and crushed to feed young children. In addition, the young and tender green fruits can be pickled before dipping with chili paste or adding to curries. Fresh ivy gourd is available in nearly all open markets in Thailand. In comparison to other countries, the consumption of ivy gourd in traditional diet is a unique feature among the Thai population [4].

Nutrient Composition

Through chemical analysis, ivy gourd is known to be rich in ␤-carotene, a major precursor of vitamin A from plant sources. The nutrient composition of ivy gourd and selected green leafy vegetables is shown in table 1 [9]. Besides ␤-carotene, ivy gourd is a good source of protein, fiber and a moderate source of calcium. Comparing to other dark green leafy vegetables such as swamp cabbage, amaranth, chayote young leaves, pumpkin young leaves and kale, ivy gourd provides the highest ␤-carotene content (4,036 ␮g/100 g edible portion). The level of ␤-carotene in ivy gourd varies seasonally with the highest content reported in the dry season during December to May [10]. A recent study

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Table 1. Nutrient composition of ivy gourd and selected green leafy vegetables (per 100 g edible portion) Ivy Gourd in Human Nutrition

Ca mg

Fe mg

Vitamin C mg

␤-Carotene, ␮g

2.7

57

1.4

13

4,036

3.1

51

3.3

9

2,511

221

2.4

21

2,424

62

1.4

24

1,518

English name

Scientific name

Water g

Energy Protein kcal g

Fat g

CHO g

Ivy gourd

Coccinia grandis Voigt

91.0

32

3.6

0.2

3.9

Swamp cabbage, Chinese

Ipomoea aquatica Forsk

92.3

23

2.7

0.3

2.4

Amaranth

Amaranthus tricolor

88.5

36

3.3

0.3

4.9

–

91.2

25

4.0

0.3

3.5

0.8

Chayote, tops and Sechium edule Sm. young leaves

Fiber g

Pumpkin, young leaves

Cucurbita pepo Linn.

91.2

32

2.6

0.3

4.7

3.1

12

5.2

21

1,289

Kale, Chinese

Brassica oleracea cv.

92.2

27

2.4

0.3

3.7

3.0

164

1.0

76

1,162

Source: Prapasri Puwastien, Monthip Raroengwichit, Pongtorn Sungpuag and Kunchit Judprasong, Thai Food Composition Tables. Paluk Tai Co., Ltd, Bangkok 1999.

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indicated that certain vegetables like ivy gourd and amaranth, when cooked by blanching or boiled shortly or steamed, showed an increase in ␤-carotene content of about 15% [11]. This may be due to an increase in extractability in the cooked products or by cooking at appropriate temperature and time, the cell wall might have been disrupted more readily and yielded more extractable ␤-carotene.

Evidence Related to Improvement of Vitamin A Nutrition

Very few studies so far have examined the beneficial effect of ivy gourd to improve nutritional status, especially that of vitamin A. In many developing countries where vitamin A deficiency is prevalent, the population depends primarily on plant sources to supply vitamin A from their diet. In Thailand, because ivy gourd is rich in ␤-carotene, readily acceptable for consumption by all age groups, inexpensive as well as accessible to the village households, this plant is selected in several studies to demonstrate an effect of dietary intervention to improve vitamin A nutrition. An earlier study indicated that feeding a group of preschool children in an orphanage with ivy gourd containing about 1.1–1.2 mg ␤-carotene daily for 2 weeks resulted in a significant increase in serum ␤-carotene and vitamin A concentrations [12]. Thus, the study demonstrated a potential of ivy gourd to improve vitamin A nutrition. Later on, a social marketing study to promote consumption of vitamin-A-rich foods in northeastern Thailand selected ‘ivy gourd’ to represent the dark green leafy vegetables as the dietary source of vitamin A [13]. This 3-year project (1988–1991) employed nutrition education and communication as its main approach. The project combined innovatively different channels of communication ranging from radio broadcasting; theatre groups and puppet show; ivy gourd video and cassette tapes to ivy gourd songs sung by well-known folk singers. In addition, active participation from mothers, teachers, health and agricultural workers as well as Buddhist monks were demonstrated. After intervention, the project was able to show a significant increase in vitamin A intake among members of the target group in comparison to the control group. A remarkable achievement was evident when such dietary vitamin A behavior was sustained in the intervention area 4 years after the project ended [14]. In the most recent study from Thailand, ivy gourd was included in the dietary intervention to evaluate the efficacy of provitamin A carotenoids in plant sources on changes of total body vitamin A stores and other vitamin A status indicators. Lactating women with low serum vitamin A were assigned to receive a daily meal containing either dark green leafy vegetables (ivy gourd plus others) and yellow/orange vegetables and fruits or purified ␤-carotene or


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low carotenoid vegetables and fruits (control) for 12 consecutive weeks. Following intervention, serum vitamin A increased similarly in all groups, likely to reflect seasonal influences on habitual diet. On the other hand, breast milk vitamin A increased more in women receiving dark green leafy vegetables plus yellow/orange vegetables and fruits. Furthermore, total body vitamin A stores declined more in the control group compared to others, towards the end of dietary intervention. Therefore, a short-term increase in dietary intake of ␤-carotene-rich foods may have prevented a decline in total body vitamin A stores that could result from breast-feeding [15].

Conclusions

As the world enter the new millennium, the issue of balancing food production with rapid population growth has been addressed. One of the acclaimed areas is biodiversity in which the optimal use of wild plants is addressed. Indigenous populations have learned to appreciate wild plants as non-conventional foods, herbs, spices as well as folklore medicine from generation to generation. Anthropological and epidemiological studies began to reveal the potentials of wild plants for human nutrition. However, scientific evidence on nutrition and health benefits of many wild plants are still lacking. Ivy gourd (C. grandis), as a vigorously growing vine in the tropical zone, fits the aforementioned scenario. In Western Australia, the Pacific Islands and Hawaii, ivy gourd is labeled as a common weed or invasive weed and needs to be destroyed when spotted. In South-East Asia and India, different parts of the plant have been used in traditional medicine while the young leaves and stems are consumed in the habitual diet. Traditional medicine prescribed the ivy gourd plant with the treatment of a range of illness symptoms from fever and skin infection, to diseases such as diabetes, allergies, eye infections, etc. Unfortunately, the claim and practices concerning ivy gourd in traditional medicine lack support from scientific evidence. Thailand, in particular, has placed ivy gourd on the menu in the delicatessen list. Since ivy gourd is easily grown and inexpensive, it can be consumed by populations of various socioeconomic status and different ages. Ivy gourd has been included in many diversified local dishes from the North, Northeast and Central Thailand. It has been regarded as a ‘common vegetable’ in the village setting. Chemical analysis indicated that ivy gourd is rich in ␤-carotene which can be converted to vitamin A. Since then, a few studies in Thailand have begun to include ivy gourd in the dietary intervention or promotion to improve dietary intake and vitamin A status of the vulnerable populations. Further investigations to validate the values of ivy gourd in medicinal uses as well as nutrition and health benefits are very much needed.

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Acknowledgements The authors thank Dr. Suttilak Smitasiri, Ms. Nipa Rojroongwasinkul, Mr. Kitti Soranacharoenpong and Ms. Roongrat Jamjandra, Institute of Nutrition, Mahidol University, Thailand, for their contributions and assistance.

References 1 2 3 4 5 6 7 8 9 10

11 12 13

14 15

Chaiyatham U: Pilot Botanical Study on Production and Yield of Ivy Gourd (in Thai). Bangkok, Department of Agricultural Extension, Ministry of Agriculture and Cooperatives, 1977. Huxley A: The New RHS Dictionary of Gardening, New York, Macmillan Press, 1992. Whistler WA: Wayside Plants of the Islands, Honolulu, Isle Botanica, 1995. Institute of Thai Traditional Medicine: Local Vegetables and Indigenous Foods of the Four Regions (in Thai). Bangkok, Department of Medicine, Ministry of Public Health, 1999. Chandraprayoon M: Local Vegetables: Secrets of Longevity, ed 2 (in Thai). Bangkok, Taithat Co, 1998. Chopra RN, Nayar SI, Chopra IC: Glossary of Indian Medicinal Plants (Including the Supplement). New Delhi, Council of Scientific and Industrial Research, 1986. Platel K, Srinivasan K: Plant foods in the management of diabetes mellitus: Vegetables as potential hypoglycaemic agents. Nahrung 1997;41:68–74. Institute of Thai Traditional Medicine: Local Vegetables: Implications and Folklore Wisdom (in Thai). Bangkok, Department of Medicine, Ministry of Public Health, 1995. Puwastien P, Raroengwichit M, Sungpuag P, Judprasong K: Thai Food Composition Tables. Bangkok, Paluk Tai Co, 1999. Wasantwisut E, Attig GA: Empowering Vitamin A Foods. A Food-Based Process for Asia and the Pacific Region. Nakorn Pathom, Institute of Nutrition, Mahidol University and Bangkok, Food and Agriculture Organization Regional Office for Asia and the Pacific, 1995. Sungpuag P, Tangchitpianvit S, Chittchang U, Wasantwisut E: Retinol and ␤-carotene content of indigenous raw and home-prepared foods in Northeast Thailand. Food Chem 1999;64:163–167. Charoenkiatkul S, Valyasevi A, Tontisirin K: Dietary approaches to the prevention of vitamin A deficiency. Food Nutr Bull 1985;7:72–76. Smitasiri S, Attig GA, Valyasevi A, Dhanamitta S, Tontisirin K: Social Marketing Vitamin-A-Rich Foods in Thailand: A Model Nutrition Communication for Behavior Change Process, ed 2. Nakorn Pathom, Institute of Nutrition, Mahidol University, 1993. Smitasiri S: Engaging communities in a sustainable dietary approach: A Thai perspective. Food Nutr Bull 2000;21:149–156. Wasantwisut E, Sungpuag P, Viriyapanich T, Sirichakwal P, Charoenkiatkul S, Chitchumroonchokchai C, Banjong O, Rojroongwasinkul N, Dhananiveskul V, Toungsuwan S, Haskell M, Yamini S, West KP Jr: Total body retinol stores in lactating Thai women following dietary and purified ␤-carotene interventions (abstract). XXth IVACG Meeting, Hanoi, Feb 12–15, 2001, p 36.

Emorn Wasantwisut, PhD, Assoc. Prof. Deputy Director for Research and Academic Affairs, Institute of Nutrition, Mahidol University, Salaya, Phutthamonthon, Nakhon Pathom 73170 (Thailand) Tel. ⫹66 2 8002380/ext 305, Fax ⫹66 2 4419344, E-Mail [email protected]


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Acerola (Malpighia glabra L., M. punicifolia L., M. emarginata D.C.): Agriculture, Production and Nutrition Paul D. Johnson Nutrilite Health Institute, Access Business Group LLC, Lakeview, Calif., USA

Introduction

The acerola (Malpighia glabra L., M. punicifolia L., M. emarginata D.C.), also known as the Barbados cherry or West-Indian cherry, has been known historically as a concentrated source of natural ascorbic acid (vitamin C) [1]. The acerola is a member of the Malpighiaceae family, and is distributed from the southern portions of North America, through Central America, and into portions of South America. Juice from acerola cherries is useful for fortifying the ascorbic acid content of other fruit juices [2]. The fruit has been used as a commercial source of vitamin C in dietary supplements as well as other food products [3] (fig. 1). The ascorbic acid levels found in acerola fruit have been measured in a range from 1.5 to over 3.5% by weight (fresh). A 180-ml glass of fresh acerola juice with a potency of 35 mg/ml ascorbic acid can contain as much vitamin C as 14 liters of orange juice. The acerola fruit is not a true cherry, but resembles that fruit so much that it cannot escape the name. For many years, the plant, which grows as a shrub or small tree (fig. 2), has been cultivated as an ornamental in subtropical areas where it flowers from April to November. The acerola may attain an average height of 3–5 m with a short slender trunk that is 0.5–1 m high, and 7–10 cm in diameter. The bark of the tree is slightly rough and gray-brown in color. The fruit matures in 3–4 weeks after flowering. The skin of the mature fruit is thin, delicate, and easily bruised. Fruits mature from green to red but can be a yellowish red when fully ripe. Approximately 80% of the ripe fruits are edible. The fruit of some cloned varieties is quite tart and acid, while other varieties are considered

Fig. 1. Harvested acerola fruits, ready for further processing.

Fig. 2. Acerola’s shrub-like growth habit.

sweet. The sweeter varieties tend to be more popular in local fresh markets and juicing operations (where the juice is directly consumed). In general, the ascorbic acid content of acerola fruit tends to decrease as the fruit matures [4].

Geographic Distribution and Origin

The acerola grows from the southern end of Texas, through Mexico and Central America to northern South America and throughout the Caribbean [5]. While it is believed that acerola originated in Central America and the Caribbean, the spread of acerola cultivation to many other subtropical parts of the world is an indication of its usefulness as a source of processed juice and vitamin C. Acerola propagation has spread into South America, including Brazil, largely due to its

Johnson

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good adaptation to the soil and climate. Acerola has also been widely introduced into tropical regions of Asia and Africa [6].

Nutritional Value of Acerola

Phytochemical Content/Nutritional Value Recent research suggests that ascorbic acid from natural sources such as acerola is more readily absorbed by the human body than that which is synthetically produced. The vitamin C in an acerola powder was found to be 1.63 times more bio-available to humans than USP vitamin C in a double-blind, randomized experiment (p ⬍ 0.0254) [7]. Since synthetic vitamin C tends to be lower in cost than vitamin C from natural sources such as acerola, the possibility of product adulteration with synthetic vitamin C exists. Infants consuming apple juice supplemented with acerola demonstrated above average or average growth and development for their age and weight. Vitamin C levels in the blood were above average for all infants after the apple/acerola juice was introduced into the diet. No allergic reactions occurred during this study, suggesting that acerola mixed with apple juice is an acceptable alternative to orange juice (potentially more allergenic) for obtaining vitamin C from the diet [8]. In addition to ascorbic acid, acerola is a source of vitamin A and iron as well as calcium, phosphorus and vitamin B (tables 1–3). Anthocyanins found in acerola have been shown to be extremely susceptible to thermal degradation, especially in the presence of oxygen [9]. Amounts of thiamine, riboflavin and niacin reported in acerola fruit are at levels below 10% of the US RDA. While various methods used by researchers have quantified some of the B vitamins at levels slightly higher than 10% of the US RDA, acerola is not considered a significant source of B vitamins [3]. Dextrose (glucose), levulose and sucrose have been identified in the acerola cherry using paper chromatography [10]. Beside the fact that acerola is an excellent source of vitamin C, acerola has shown unique and promising potential in other aspects of human health. Research has indicated the ability of acerola to enhance the antioxidant activity of other botanical extracts. Recent work has shown that, in the presence of acerola cherry extract, soy and alfalfa phytoestrogen extracts prevent the oxidation of low-density lipoproteins (LDL) [11]. These findings were felt to be of significant benefit to the health of postmenopausal women due to the increased risk of coronary heart disease in this age group. The increased risk of heart disease is believed to be a function of LDL oxidation, which is normally suppressed by naturally occurring estrogen levels in the body. The strong

Acerola: Agriculture, Production and Nutrition

69

Table 1. Vitamin content of raw acerola fruit [data from 22] Vitamin

Units

Amount (per 100 g edible portion)

Vitamin C, total ascorbic acid Thiamin Riboflavin Niacin Pantothenic acid Vitamin B6 Folate, total Folic acid Folate, food Folate, DFE Vitamin B12 Vitamin A, IU Vitamin A, RE Vitamin E

mg mg mg mg mg mg ␮g ␮g ␮g ␮g ␮g IU ␮g RE (retinol equivalence) mg ATE (␣-tocopherol equivalence)

1,677.6 0.020 0.060 0.400 0.309 0.009 14 0 14 14 0.00 767 77 0.130

Table 2. Mineral content of raw acerola fruit [data from 22] Mineral

Units

Amount (per 100 g edible portion)

Calcium Iron Magnesium Phosphorus Potassium Sodium Zinc Copper Selenium

mg mg mg mg mg mg mg mg ␮g

12 0.20 18 11 146 7 0.10 0.086 0.6

antioxidant activity of the combined acerola and phytoestrogen extracts could help reduce the oxidation of LDL, thus reducing the risk of heart disease. Phytochemical Profiles/Content during Fruit Development and after Harvest Fruit maturity level has a significant impact on ascorbic acid levels found in acerola [4, 12]. Peel color has been used historically as an index of fruit ‘ripeness’

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Fatty acid

Percent by weight

Palmitic Stearic Oleic Linoleic Linolenic

23.38 ⫾ 0.97 11.59 ⫾ 0.14 25.96 ⫾ 0.40 24.45 ⫾ 0.60 14.60 ⫾ 0.52

Table 3. Composition (profile) of fatty acids in acerola [data from 23]

Fig. 3. Acerola fruits of varying degrees of ripeness on the same tree.

in acerola. Immature acerola fruits begin with a green color and mature to a bright red coloration (fig. 3). As the acerola fruit matures, ascorbic acid concentration in the fruit decreases [13]. The decrease in ascorbic acid during maturation is caused by oxidation reactions, until the point of irreversible conversion to diketogulonic acid, which has no vitamin function [14]. This degradation necessitates timely processing of acerola to preserve the nutritional value. This and other forms of degradation in harvested acerola fruit work to limit the value of acerola as a fresh market commodity. Other methods of assessing the ripeness of acerola fruits have been proposed, including the measurement of the sugar/acid ratio in the fruit. While these methods may provide a more precise measurement of fruit ripeness, the use of peel color as an index provides a more practical approach in field situations where complex analyses may not be an option. Storage and handling conditions can measurably impact the prolonged quality of acerola fruits. Current experience in the processing of acerola fruits suggests that the vitamin C content of the fresh fruits begins to decrease as soon as 4 h after harvest. Timely processing and/or cold storage can help limit the loss of vitamin C in harvested acerola fruits. One researcher reported that, in addition to limiting vitamin C loss, cold storage of fruits at ⫺18°C can also preserve some of the sensory qualities of the harvested material [15].


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Agricultural Aspects of Acerola

Agricultural Potential The acerola is a dense shrub that can attain a height of 3–4 m. Mature fruits are bright red with three lobes and three seeds. Flowers are usually borne in clusters of two to three flowers each [16]. The flowers are sessile or on shortpeduncled cymes, with small pink to white flowers with five petals each. Acerola flowers from April to November (in the Northern Hemisphere) [17]. Branches are thick and woody with raised lenticels [18]. Acerola can potentially be cultivated in tropical and subtropical regions from about 30°N to 30°S latitude. While acerola has received most of its popularity due to its ascorbic acid content, there is only a limited market for the fresh acerola fruit. As mentioned previously, acerola fruit quality begins to degrade quickly after harvest. Transport and handling of fresh acerola fruit only exacerbates the rapid decomposition of fruit quality. There are many established varieties of acerola, with many having been selected for either improved flavor or increased ascorbic acid levels. The plant is propagated by seedlings, cuttings and grafting. The most feasible method of mass propagation is by cuttings [18]. The use of root-inducing substances and sand media has been shown to significantly increase the success and growth rate of acerola cuttings [19]. Acerola is sensitive to frosts, with most trees unable to survive temperatures below ⫺2°C. Approximately 1,000–2,000 mm of annual rainfall (or equivalent irrigation) is considered ideal for acerola fruit production. Higher water inputs can result in an increase in fruit yields, but with softer, more fragile fruits. Quality of ripe fruit begins to deteriorate quickly after harvest, which necessitates either timely processing or cold storage of the harvest. Onset of flowering appears to be more closely related to irrigation or rainfall cycles instead of day length. Flowering and subsequent fruiting can be continuous if rainfall or irrigation is applied consistently. While this can improve the annual yield of the plant, it can make harvest of the fruits less efficient due to the limited amount of ripe fruit available at any given time. On plantations where fruits are borne continuously, plants must be harvested frequently (as often as every second day), to prevent overripe conditions in the fruit. Flower loss is a common problem in acerola production, with as much as 90% of all flowers having fallen from the tree before fruit set [20]. The presence of ripe fruit and flowers on the same tree makes mechanical harvest of the fruits nearly impossible since subsequent crops are lost due to flower drop. Acerola will grow in a wide range of soil types and soil pH levels. However, in some soils, pH levels below 5.4 will cause a calcium deficiency [18]. Acerola does not tolerate consistently wet soils due to rot and nematode

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Moisture Carbohydrate Protein Ash PH Fat Brix

20% 27% 2.7% 3.8% 3.0–4.0 0.9% 72 at 25°C

Table 4. Typical proximate analysis of concentrated acerola juice

problems. Other Malpighia species have been used as rootstock for acerola to help increase nematode resistance. Much of the world production of acerola occurs in Brazil. However, much of the plantations that were initiated in Brazil were from seed propagated plants, resulting in a lack of genetic heterogeneity in acerola orchards [21]. This lack of genetic variability can have a detrimental impact on the acerola industry should specific disease or pest problems arise. Recent efforts to characterize the clonal variability of acerola have been initiated in an effort to help ameliorate this lack of genetic diversity. Fresh and Processed Uses Acerola fruit has limited fresh uses due to its tender and perishable nature. It is widely consumed fresh in areas where the fruit can be grown, particularly in the West Indies and Central and South America [18]. Processed acerola fruits and juice are more prevalent in the international market for this plant. Concentrated acerola juice is suitable for freezing or further processing into dry powders. The concentrated juice, while maintaining some of the properties of fresh fruits (table 4), must be frozen or further processed to prevent spoilage and nutritional degradation. The fruits can be processed into fresh and frozen juice, purees, blended juice, baby food, flavoring syrups, preserves and vacuum or spray dried powders containing up to 38% ascorbic acid [18]. Much of the dry powder production of acerola is used as an ascorbic acid source for dietary supplements. Canning of pasteurized acerola juice has resulted in undesirable products, which do not maintain any appreciable ascorbic acid levels. Conclusion

The uniquely high vitamin C content of the acerola, in addition to its many potential uses for processed acerola products, make this plant valuable for further utilization in food products. Since much of the nutritional value of acerola fruits


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can be ‘fixed’ through a variety of processing methods, the acerola continues to be of great value when prepared as single-entity products or when combined as healthy additives to multi-ingredient blends. Research into other health benefits offered by acerola (in addition to vitamin C supplementation) indicate that the use of botanical products offers potentially superior results when compared to the use of isolated synthetic compounds. The limited market potential of fresh acerola fruit presents opportunities for the development of varieties, cultivation and harvest practices, as well as storage and handling methods that can improve the characteristics of the fresh fruit. The pleasant taste of ripe acerola, in addition to health benefits derived from its consumption, make fresh acerola a worthy challenge for the agricultural community. References 1 2 3 4

5 6 7

8 9 10 11

12 13

14 15 16 17

Asenjo CF, Friere de Guzman SR: The high ascorbic acid content of the West Indian cherry. Science 1946;103:219. Fitting KO, Miller CD: Stability of ascorbic acid in frozen and bottled acerola juice alone and combined with other fruit juices. J Food Res 1960;25:203. Asenjo CF: Acerola; in Nagy S, Shaw PE (eds): Tropical and Subtropical Fruits: Composition Properties and Uses. Westport/Conn, AVI Publ Co, 1980, pp 341–374. Cruz VD, d’Arce LPG, Castilho VM, de Lima VA, Cruz R, Godinho PH: Change in the ascorbic acid content of acerolas (Malpighia glabra L.) as a function of harvest maturation degree and storage temperature. Arq Biol Tecnol 1995;38:331–337. De Assis SA, Lima DC, de Faria Oliveira OMM: Acerola’s pectin methylesterase: Studies of heat inactivation. Food Chem 2000;71:465–467. Duke JA, de Cellier JL: Malpighia glabra L. (Malpighiaceae) – Acerola. CRC Handbook of Alternative Cash Crops. Boca Raton, CRC Press, 1993, pp 300–302. Tang L: Comparative study of the bio-availability of ascorbic acid in commercially produced products; thesis presented to the Faculty of the Department of Chemistry, University of Pennsylvania, Scranton/Pa 1995. Clein NW: Acerola juice – The richest known source of vitamin C. J Pediatr 1956;48:140–145. Chan HT, Yamamoto HY: Kinetics of anthocyanin decomposition in acerola juice. Asean Food J 1994;9:132–135. Santini R, Huyke AS: Identification of sugars present in fruit of the acerola (Malpighia punicifolia L.) by paper chromatography. J Agric Univ Puerto Rico 1956;40:87–89. Hwang J, Hodis HN, Sevanian A: Soy and alfalfa phytoestrogen extracts become potent lowdensity lipoprotein antioxidants in the presence of acerola cherry extract. J Agric Food Chem 2001;49:308–314. Vendramini AL, Trugo LC: Chemical composition of acerola fruit (Malpighia punicifolia L.) at three stages of maturity. Food Chem 2000;71:195–198. Alves RE, Chitarra AB, Chitarra MIF: Postharvest physiology of acerola (Malpighia emarginata D.C.) fruits: Maturation changes, respiratory activity and refrigerated storage at ambient and modified atmospheres. Acta Hort 1995;370:223–226. Watada AE: Vitamins; in Weichmann J (ed): Postharvest Physiology of Vegetables. New York, Dekker, 1987, pp 455–467. Maciel MIS, Melo EDA, de Lima VLAG, da Silva MRF, da Silva IP: Processing and storage of acerola (Malpighia sp.) fruit and its products. J Food Sci Technol 1999;36:142–146. Du Preez RJ: The acerola: A natural source of ascorbic acid (vitamin C). Neltropika 1997;10:2–3. McWilliams HB, Morse P: Acerola, a new Hawaiian potential. Proceedings of the IFT Pacific Rim Conference, 1960.

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22

23

Chapman KR: Malpighiaceae: Acerola (Barbados cherry, West Indian cherry, Puerto Rican cherry, Jamaican cherry); in Tropical Tree Fruits for Australia. Queensland Department of Primary Industries. Information Series QI83018, 1984. Jackson GC, Abrams R: Influence of root-inducing substances and time intervals on the rooting of acerola cuttings. J Agric Univ Puerto Rico 1959;43:152–158. Bubrick PD: Acerola. CRFG Fruit Facts. California Rare Fruit Growers, 1989, vol 2. Moura CFH, Alves RE, Mosca JL, de Paiva JR, Oliveira JJG: Fruit physiochemical characteristics of acerola (Malpighia emarginata) clones in commercial orchards. Proc Interam Soc Trop Hort 1997;41:194–198. US Department of Agriculture, Agricultural Research Service: Nutrient Database for Standard Reference, Release 14. 2001. Nutrient Data Laboratory Homepage: http://www.nal.usda.gov/fnic/ foodcomp Visentainer JV, Vieira OA, Matshushita M, de Souza NE: Physiochemical characterization of acerola. Arch Latinom Nutr 1995;47:70–72.

Paul D. Johnson Access Business Group LLC, 19600 6th Street, Lakeview, CA 92567 (USA) Tel. ⫹1 909 9286896, Fax ⫹1 909 9286835, E-Mail [email protected]


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Food-Based Approaches to Prevent and Control Micronutrient Malnutrition: Scientific Evidence and Policy Implications1 C. Gopalan, Bani Tamber Nutrition Foundation of India, Qutub Institutional Area, New Delhi, India

Introduction

Combating ‘hunger’ rather than ‘hidden hunger’ was the major item in the nutrition agenda in earlier years. In recent years, however, micronutrients have acquired the center stage. The current emphasis on micronutrients may be expected to draw attention to the need to ensure ‘nutritive quality’ of the diets and not only to their energy and the protein content. To this extent the recent interest in micronutrients may be welcome. We must however not lose sight of the fact that micronutrient deficiencies, in many parts of the world, are often a part of general undernutrition including energy-protein undernutrition. It is rarely, for example, that one comes across a child with Bitot’s spots or angular stomatitis in the absence of growth retardation. It is indeed even possible that micronutrient deficiencies are often the result of lack of enough habitual food in the household rather than to the poor quality of such foods. It will be unfortunate if the current euphoria over micronutrients leads us to the mistaken approach of trying to ‘solve’ isolated micronutrient deficiencies with single (or even multiple) supplements of micronutrients ignoring the basic necessity of overall improvement of household diets with respect to quality and quantity. A food-based rather than drug-based approach will be the proper answer to the problem of micronutrient deficiency – as indeed to the problem of undernutrition in general. 1

Based on a report presented to the FAO.

Table 1. Micronutrients essential for man Vitamins

Trace minerals

A. Micronutrients known to be essential for man and animals Vitamin A Thiamin Iron Vitamin D Riboflavin Iodine Vitamin K Nicotinic acid Zinc Vitamin E Pyridoxine Copper Essential fatty acid Folic acid (␻–6 and ␻–3) Biotin (?) Vitamin B12 Pantothenic acid (?) Ascorbic acid

Selenium Manganese Chromium Cobalt

B. Micronutrients essential for animals and not yet established as essential for man Choline Silicon Molybdenum p-Aminobenzoic acid Fluorine Arsenic Nickel Source: Modified from Narasinga Rao BS: Micronutrient interactions. Paper presented at the Indo-US Symposium on Micronutrient Requirements, NIN, Hyderabad 2000.

The Concept of ‘Micronutrients’

It is important at the outset, to define our concept of ‘micronutrients’. It is well known that apart from the so-called ‘proximate principles’ in our diets, namely carbohydrates, proteins and fats, several other nutrients are now being considered as being required in relatively small (micro)quantities, for ensuring optimal health and well-being. A list of such micronutrients for which dietary allowances have been recommended by some national bodies is indicated in table 1 [1]. It must however be pointed out that clinical and epidemiological evidence of ill health in humans arising from deficiency, have been identified only with respect to a few of the nutrients in the list. In the case of others we have no more than biochemical evidence suggestive of their role in metabolic processes. From the public health point of view therefore, the same weightage cannot be accorded to all the items in the list. Phytonutrients Apart from the nutrients listed in table 1, in recent years many components in foods (especially plant foods) with biological properties indicative of capacity for disease prevention and health promotion have been discovered [2]. A list of such ‘phytonutrients’ is provided in table 2 and this list is steadily growing.

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Table 2. Phytonutrients associated with health promotion, examples of typical components of each class, representative biological activities, and prominent food sources Phytonutrient class

Typical compounds

Biological activities

Food sources

Carotenoids

␣-Carotene, ␤-carotene, ␤-cryptoxanthine, lutein, lycopene, zeaxanthine

Source of vitamin A (some), quench singlet oxygen, ↑ cell-cell communication, ↓ risk of adult macular degeneration (some)

Colored fruits and vegetables

Glucosinolates, isothiocyanates, indoles

Glucobrassicin, sulphorophane, indole-3-carbinol

↑ Phase II enzyme activity, alter estrogen metabolism through shift in hydroxylation, ↓ DNA methylation

Cruciferous vegetables (broccoli), horseradish, mustard and mustard oil

Inositol phosphates

Phytate, inositol pentaphosphate, inositol tetraphosphate, etc.

Bind divalent cations – especially copper and iron, which may generate hydroxyl radicals through the Fenton reaction

Cereals, soybeans

Phenolics, cyclic compounds

Chlorogenic acid, ellagic acid, coumarins, limonene

↑ Phase II enzyme activity, inhibit N-nitrosation reactions, antioxidant

Citrus fruits, vegetables

Phytoestrogens

Isoflavones – diadzein, genistein, glycitein, Ligans – matairesinol, secoisolariresinol

Metabolized in the GI tract to estrogen-like compounds, ↑ SHBG synthesis, ↓ tyrosine kinase activity, induce apoptosis

Isoflavones – soybeans, ligans – flax, rye, vegetables

Phytosterols

Campesterol, ␤-sitosterol, stigmasterol

Bind bile acid and cholesterol, ↓ colonic cell proliferation

Vegetable oils, nuts, seeds, cereals, legumes

Polyphenols

Flavonoids (e.g. quercetin, apigenin, catechin) theaflavins, thearubigens

Antioxidant, ↓ capillary fragility and permeability (vitamin P) alter tyrosine kinase activity

Fruits, vegetables, tea, red wine, theaflavins and thearubigens in black and oolong tea

Protease inhibitors

Bowman-Birk inhibitor

Bind to trypsin and chymotrypsin, ↓ growth of transformed cells, ↓ tumors in animals

Soybeans, other legumes, cereals, vegetables, egg white (duck)

Saponins

Soyasaponins, soyasapogenols

Bind bile acids and cholesterol, cytotoxic towards tumor cells, antioxidant

Soybeans, other legumes, nuts

Sulfides and thiols

Diallyl sulfides, allyl methyltrisulfides, dithiolthiones

↑ Phase II enzyme activity, bacterial activity – nitrate to nitrite conversion

Sulfides – allium vegetables (onions), dithiolthiones – cruciferous, vegetables (broccoli)

Source: Beecher [2].

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Table 3. Dietary antioxidants Nutrients

Non-nutrients

␤-Carotene – provitamin A Ascorbic acid – vitamin C

Carotenoids (lycopene, xanthophyls) Lutein, ␣- and ␹-carotenes (cryptoxanthine, zeaxanthine) Flavonoids (quercetin, myricetin, quercetagatin, gossypetin)

Tocopherols Tocotrienols Riboflavin Sulfur amino acids Cysteine and methionine Selenium

Anthocyanins Isoflavones Phenolic compounds (catechin) Indoles

Source: Narasinga Rao BS: Bioactive phytochemicals in foods. NFI Bull 1995;16:1–4.

These phytonutrients could be particularly helpful in the prevention of chronic lifestyle-related diseases including some forms of cancer, cardiovascular diseases, atherosclerosis and diabetes – diseases which not only afflict large sections of the populations of developed countries, but are also becoming increasingly important as major causes of morbidity and mortality in developing countries as well [3–7]. This list does not include ␻–3 fatty acids, which though required in small amounts, are now known to play an important role in health promotion and disease prevention. These fatty acids are found in fish oils and quite a few green leafy foods like spinach and purslane (Portulaca oleracea). Oryzenol and phytosterols in rice bran and rice bran oil and allicin in garlic are known for their hypocholesterolemic potency and can also be included in the list of phytochemicals in foods. The role of dietary fiber in health promotion and disease prevention is now being increasingly recognized. Some of these phytochemicals act as antioxidants (table 3), inhibiting lipid peroxidation and oxidative damage to cellular proteins and DNA, and to lens proteins in the retina, through chain termination, radical scavenging and oxygen quenching. Carotenoids [8], phenols [9] and flavonoids [10] occurring in plant foods, such as green leafy vegetables (GLVs) and fruits like papaya, amla and guava, are examples of such antioxidants. Curcumin is a powerful antioxidant contained in turmeric, a spice and a coloring agent widely used in India [11]. The beneficial effects of such antioxidants in the prevention of lung cancer [12] and in reducing the risk of deaths from coronary heart disease [13] have been demonstrated in human subjects. Other phytochemicals help in disease


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prevention through detoxification of toxicants, carcinogens and mutagens through their effects on the microsomal mixed function oxidase (MFO) system of phase I metabolism [14], and on glutathione transferase, NADPH, quinone reductase, UDP glucuronosyl transferase and epoxide reductase enzymes of phase II metabolism [15]. Some other phytochemicals inhibit carcinogens by ‘blocking’ or ‘suppressing’ action [4, 16]. Isoprenoid compounds in fruits and vegetables, besides inducing phase II enzymes, act as suppressing agents by inhibiting cholesterol biosynthesis. Garlic, a widely used food item, contains allilic sulphides, which can inactivate carcinogens; agoene, a compound derived from garlic has also been shown to prevent platelet aggregation [17]. The above brief review will indicate the important beneficial roles phytonutrients can play in prevention of major diseases and in health promotion. It will be justifiable to argue, in the light of considerable experimental, clinical and epidemiological evidence now available, that phytonutrients are at least as important in human nutrition as some of the conventional micronutrients that were earlier known and are listed in table 1. This is the case not only in developed countries but in developing countries as well, especially in the present stage of developmental transition where populations are being increasingly exposed to toxicants and oxidants, pollutants and environmental carcinogens. In the light of these advances in our knowledge, our present concept of micronutrients must include not just the conventional ‘nutrients’ but also the so-called ‘non-nutrients’. If a truly ‘nutritious diet’ is one which promotes health and prevents disease, phytonutrients must obviously find an important place in such diets. The commonly consumed diets in developing countries which are predominantly based on plant foods must be rich in phytochemicals but their content in such diets has not been fully assessed, except in a few items included in the diets. Future dietary guidelines and RDAs must also take note of their requirements. The enlargement of our concept of micronutrients will obviously favor a strong food-based strategy in preference to a strategy of distributing a cocktail of some arbitrarily chosen nutrients to the exclusion of several others, probably even more important. We will revert to the question of strategies later in this chapter. National bodies concerned with recommendations of dietary allowances and dietary guidelines have apparently already recognized the need for a broader concept of micronutrients. The level of intake of vegetables and fruits as recommended by some national bodies exceeds 450 g daily. The new US Dietary Guidelines is understood to have advocated that fruits and vegetables which largely provide phytonutrients should have a separate focus and should not be lumped together with grains, as in the earlier recommendations, because of their distinctive nutritive value. In New Zealand, for instance, the existing

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recommendation of ‘five’ servings of fruits and vegetables has now been increased to seven [18]. On the other hand, in South Asian countries [19], and to some extent in South-East Asian countries as well, vegetables and fruit intakes hardly exceed 150 g daily, and in the poorest households the intakes are even lower. These populations must therefore be deficient, not just in conventional ‘micronutrients’ (of the earlier limited concept) but more so, in phytonutrients. Any program of nutritional improvement must therefore address this major deficiency. Phytonutrients apparently act collectively and synergistically, each phytonutrient being thus a part of an orchestra. Indeed some of the conventional micronutrients listed in table 1 are also often part of such an orchestra, as will be evident from the fact that some micronutrients like ␤-carotene, ascorbic acid, tocopherols and selenium also act as antioxidants in conjunction with carotenoids, flavonoids and phenolic compounds. It is the sum of the individual contributions of each phytonutrient, many of them perhaps quite modest individually, that exerts the impact on disease prevention. Under these circumstances, the search for some single or even multiple magic bullets from over scores of micronutrients may be counterproductive. It will be poor strategy to try to convert what is essentially an orchestra into a solo! The hypothesis that the protective effect of vegetables and fruits against stomach and lung cancer might be attributable to ␤-carotene, for instance, has been tested and proved incorrect [20]. ␤-Carotene supplementation, unlike supplementation with vegetables and fruits, did not lower rates of lung cancer; indeed among high-risk individuals it appeared to increase cancer incidence and mortality. The use of single agents has proved to be ineffective and ultimately counterproductive in the treatment of many cancers. A recent study published in the New England Journal of Medicine [21] reported that while vitamin E supplements afforded no additional protective effect against heart disease, vitamins obtained through natural sources such as fruits, vegetables and nuts did help to protect against heart diseases by inhibiting the oxidation of cholesterol. Reviewing the current evidence, Potter [22, 23] concludes: ‘The safest public health strategy seems to be to advocate increased intake of intact plant foods with the multiplicity of agents that they contain. It is less likely that any clone of malignant cells can survive the polypharmacy of plant foods.’ In the light of modern knowledge, vegetables, fruits and nuts have emerged as the food items which could address multiple problems at both ends of the socio-economic spectrum – the ‘double burden’ which many developing countries now face in the context of developmental transition. Vegetables, fruits and nuts can provide the ‘micronutrients’ usually deficient in the diets of poor communities. They can also provide the ‘phytonutrients’ which help to combat the chronic diseases of the affluent.


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Populations receiving supplements providing arbitrary mixes of ‘conventional’ micronutrients will in any case need to take adequate amounts of vegetables and fruits in order to fulfil their needs of phytonutreints and which will supply micronutrients as well. And if they do so, arbitrary supplements containing a few micronutrients will become largely unnecessary. Increased consumption of vegetables and fruits will not only provide phytonutrients but also quite a few of the conventional micronutrients. The promotion of consumption of vegetables (including GLVs) and fruits in adequate quantities (450 g) must therefore become a central part of the strategy for nutritional improvement of all populations. This task cannot be bypassed through resorting to ‘simple solutions’ and ‘magic bullets’.

Micronutrient Requirements and Interactions

The daily requirements of different phytonutrients are as yet unknown. Some of the micronutrients listed in table 1, while perhaps required for some animals have not been established as being essential to man. These include biotin, pantothenic acid, choline, paraminobenzoic acid, silicon, fluoride and molybdenum. Even among the other micronutrients listed in table 1, diseases attributable to deficiency have been recognized as important public health problems only in the case of iodine, iron, vitamin A, vitamin C, vitamin B complex and vitamin D. Health problems attributable to deficiency of other nutrients in the list have not been encountered on a public health scale. Figures of requirement levels for a number of micronutrients have been indicated among the RDAs of some national bodies. These figures have obvious limitations. Requirements of several of these micronutrients have been estimated on the basis of some biochemical parameters, but the biochemical/ molecular basis of many micronutrient-deficiency-related diseases is not clearly understood. Thus the biochemical events leading to night blindness due to vitamin A deficiency cannot explain corneal dissolution. Night blindness has also been reported in anemia and riboflavin deficiency in humans can lead to symptoms like burning and itching of the eyes, corneal vascularization and anemia [24]. Though thiamin, riboflavin and niacin are all involved in energy transduction and their deficiency would be expected to compromise the production of ATP, the actual clinical manifestations of these deficiencies are different. In short, the relevance of some biochemical parameters now being used to assess requirement to the actual clinical manifestation arising from deficiency can be disputed, raising doubts as to whether some of these biochemical indices are truly indicative of subclinical deficiency. Even when a reasonable relationship between a biochemical index and subsequent clinical manifestation exists, the

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critical level in the biochemical test that can predict clinical risk has not been easy to identify because this level can vary due to the superimposition of other factors. Several factors may be expected to modify micronutrient requirements in real-life situations. Estimates of requirements of a given micronutrient based on certain biochemical parameters obtained under controlled laboratory conditions in one country, may not necessarily be universally valid and applicable to all populations of the world. Unfortunately there have been very few studies on micronutrient requirements in developing countries [25, 26]. Studies carried out at the National Institute of Nutrition (NIN), Hyderabad, had indicated that riboflavin deficiency as judged by erythrocyte glutathione reductase activity was widespread [27], as also deficiency of pyridoxine and folic acid [28, 29]. These studies showed that over 90% of rural (15–45 years) and urban women (18–35 years) had a prevalence of biochemical deficiency of riboflavin. In the assessment of ‘riboflavin deficiency’ (and some other micronutrient deficiencies) on the basis of enzymatic tests, the yardstick that has been used is the level of the micronutrient needed for ensuring maximal enzyme activity. This level of micronutrient intake need not necessarily be the optimum. It is therefore possible that estimates of micronutrient deficiencies on the basis of some biochemical tests could overstate the true prevalence. This is a point that needs to be remembered in the interpretation of results. Orolingual and dermal lesions particularly in pregnant women [30] and in school-going children [31] in India have been reported. These lesions however, are not specific to riboflavin deficiency. Their treatment sometimes requires other B-complex vitamins, particularly pyridoxine, suggesting the presence of multiple deficiencies. On the other hand, low levels of serum vitamin A and of evidence of thiamin deficiency were far less frequent [28, 29]. While studies at Bombay, India, yielded results with regard to riboflavin deficiency which were at variance with those of Hyderabad, the studies in Chiangmei, Thailand, correspond to the Hyderabad findings [32]. In short, no uniform pattern of micronutrient deficiencies could be discerned in different population groups in developing countries. It is also to be expected that there could be seasonal variations even within a given region, depending on the availability of certain foods in some seasons and not in others. Studies on the profile of nutrient deficiencies were recently carried out under the auspices of the Human Resource Development of the Government of India [33]. Data indicated that while on the basis of the NCHS standards nearly 50% of the under-fives showed evidence of growth retardation, only a very small percentage of children showed actual nutritional deficiency signs. Thus the major problem among under fives was general growth retardation. It must also be pointed out that poor populations of developing countries do not just suffer from a single micronutrient deficiency. Where a particular


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micronutrient deficiency has been detected using specific tests, it may be reasonably assumed that quite a few other micronutrients, and possibly macronutrients are also deficient in the same subject. Initiating measures to correct a single deficiency detected by a specific test in isolation may not be the appropriate strategy. Indeed because of the presence of micronutrient interactions and imbalances, such unilateral correction of a single micronutrient dosage may even be counterproductive. Requirement levels of different micronutrients have been generally estimated under laboratory conditions while ensuring that the diets are adequate with respect to all other nutrients and micronutrients other than those under study. The overall level of calorie intake, the mix and nature of the staple foods supplying the proximate principles, and the actual levels of other micronutrients in a diet may all be expected to influence the requirements of a given micronutrient. Thus the level of calorie intake is known to influence thiamin requirement – the thiamin-sparing effect of low calorie diet is thus recognized [34]. The level and nature of protein in the diet is known to exert a substantial effect on calcium requirements [35] as also on the requirement of some of the B vitamins [36]. The vitamin C requirement will depend upon whether we are considering its ‘conventional’ vitamin functions or its role as an antioxidant. Vitamin D requirement may be influenced by the level of calcium intake [37]. A specific thermolabile variant of the folate-related enzyme 5,10-methylene tetrahydrofolate reductase, which causes partial enzyme deficiency, has been described in 5–15% of North American populations with low folate status [38, 39]. This variant increases the risk of homocysteinemia, neural tube defects and coronary heart disease necessitating additional requirements for folate in pregnancy. Folic acid requirements will thus depend upon whether we are considering its hemopoietic effect or its role in prevention of neural tube defects. A negative copper balance may occur if an individual consumes a total of 20–25 mg/day of zinc. Zinc supplementation of 20 mg requires 2 mg of copper to prevent inhibition of copper absorption. Copper is important for iron absorption and hemoglobin synthesis. Interactions between vitamin E and ␻–3 fatty acids is suggested by the observation that while ␻–3 fatty acids decrease serum triglycerides, they tend to promote LDL oxidation; the latter can be reversed by simultaneous administration of vitamin E [40]. Fortunately, natural vegetable oils like mustard, canola and soya contain vitamin E and ␻–3 fatty acids, indicating the safety and superiority of natural foods in ensuring adequacy of micronutrients. There is thus considerable imprecision with regard to estimation of micronutrient requirements under different conditions. There is considerable interaction – synergistic and antagonistic – between different micronutrients with respect to their metabolic functions. Apart from such interactions between micronutrients, major proximate principles in diets,

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i.e. carbohydrates, proteins and fats may modify the utilization of requirements of different micronutrients; through the presence of inhibitors like trypsin inhibitors, phytates, tannins, or through goitrogens. Several mechanisms are involved in these interactions, such as: competition for absorption site in the intestinal mucosa; competition for the carrier protein involved in absorption and transportation; conversion of micronutrients into its active co-enzyme form; competition with respect to binding of the nutrients with the cellular receptors, and metabolic disposal of the nutrient by detoxification. In real-life situations, diets of poor populations may be generally expected to be deficient in a multiplicity of nutrients. This would call for a correction of inadequate intake of several nutrients besides the one indicated as being the major deficiency. However, the order of such corrections of such different nutrient deficiencies, and the amount of nutrient supplements needed for this correction, cannot be determined with precision. This is a consideration which will again forcefully argue for a food-based strategy and against dependence on arbitrary combinations of some nutrient administered in arbitrary amounts. From available data it may be reasonable to argue that in a healthy state a dynamic equilibrium between different micronutrients is achieved. The actual amounts of different micronutrients involved in the establishment of this equilibrium may not be identical and may vary with different population groups with their overall dietary patterns. Thus in a population subsisting on mainly vegetable proteins, daily requirements of calcium for normal health may be much lower than in a population subsisting on high amounts of animal protein. Interactions not only between dietary protein and calcium, but also possibly between vitamin A intake and calcium requirements, seem possible. The effects of high doses of vitamin A on bone resorption and bone formation have been demonstrated in animals [41]. While the relevance of the observation to humans must come from further studies, the effect of isolated supplementation of massive doses of vitamin A in populations subsisting on low calcium intakes with respect to their bone health will require attention. While diets are important determinants of nutritional status with regard to micronutrients, the role of infections could be just as important, especially among communities living in poor environment. Thus, respiratory infections have been known to increase urinary loss of vitamin A [42] and of riboflavin [43]. Indeed much of the mild/moderate vitamin A deficiency seen in poor communities is probably attributable to repeated infections rather than to poor diets. In catabolic states following infections, negative nitrogen balance is often associated with loss of riboflavin [44]. In the presence of infections, there is a continued loss of some micronutrients and supplements may not be able to overcome the loss. It has been shown that a large percentage of infants


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suffering from respiratory infections remained vitamin A deficient even after large doses of vitamin A supplements, which could promote urinary losses of vitamin A [45]. Moreover, it has also been reported that vitamin A supplements had no significant effect on the percentage of time ill or the number of respiratory infection episodes [46]. Infections also impair the utilization of available micronutrients by the body; for example, in infections even with available iron, it is not incorporated for hemoglobin synthesis. There is now evidence that even with subclinical inflammatory response (as assessed by increased acute phase reactants like ␣1-antichymotrypsin (ACT), ␣1-acid glycoprotein (AGP) and C-reactive protein (CRP) in serum of apparently healthy children), the serum retinol levels are lowered. It is a common observation that the concentration of plasma retinol is lower in the blood of both infants and adults living in the lesser developed countries of the world. The lower concentrations are widely accepted to mean that vitamin A status is poorer in those countries than in the developed world. However, it is also well known that the level of exposure to disease is far higher in developing than in developed countries and it is now recognized that disease depresses the concentration of plasma retinol [47–49]. Disease or trauma depresses the plasma concentration of the retinol-binding protein (RBP). The answer then is to control the infections. A well-balanced diet and prompt control of infections may be a more rewarding strategy in the matter of ensuring adequate micronutrient malnutrition in poor communities than supplementation with synthetic vitamins. Vigorous measures at infection control and dietary improvement will provide a sustainable and durable answer. Micronutrients in Foods

Practically all foods (with the exception of a few which supply ‘empty’ calories like sugar) contain micronutrients. Thus, micronutrients are to be found in cereals, pulses, nuts, tubers, vegetables and fruits among plant foods, and in practically all ‘non-vegetarian’ foods. There is enormous varietal variation in the micronutrient content of foods, indicating the rich possibilities of upgrading the nutritive value of many foods through conventional plant-breeding techniques without sacrificing other desirable properties of yield and disease resistance. If the type of attention that was devoted to the improvement of wheat and rice with respect to yield, protein content and disease resistance in the wake of the Green Revolution is now devoted to the improvement of micronutrient content of plant foods, the results could be truly rewarding. Augmentation of Production of Micronutrient-Rich Foods Food production policies of developing countries, in the wake of the Green Revolution, had largely neglected pulses, legumes and horticultural products – rich

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sources of micronutrients – and had, instead, concentrated their attention mostly to the production of wheat and rice – the prestigious cereals. Even among cereals, millets, fair sources of micronutrients, were relatively neglected. The near exclusive attention accorded to wheat and rice in the 1960s and 1970s (the Green Revolution), when developing countries were threatened with famine and extinction, is, perhaps, understandable. Among populations of developing countries below the so-called ‘poverty line’, the major concern has been the avoidance of hunger. For this reason, cereals as providing much needed energy, were prized items of diets, and vegetables as poor sources of energy were largely neglected. Even wheat and rice were often excessively ‘refined’; ‘whole grains’ once in traditional use have been given up in preference to polished grains. Now with the progressive elimination of (caloric) hunger, the earlier near exclusive reliance on cereals must give place to the consumption of better balanced diets. In the light of modern knowledge, the need for a reversal of earlier unhealthy trends with respect to patterns of food production is now being increasingly appreciated. Actually there is evidence that the intake of cereals in the middle income group is less than among the very poor [50]; it is important at this stage of transition to ensure that this is reflected in adequate intake of other micronutrient-rich foods. Indeed even in the industrialized countries, vegetables and fruits are now finding a pride of place in the diets, while the deleterious effects of the daily consumption of large chunks of meat and cream have been recognized. Horticultural development and augmentation of production of pulses and legumes are now finding an important place in national agricultural policies [51]. There are rich possibilities of augmentation of the overall production of micronutrient-rich foods, and even more importantly, of augmenting the micronutrient content of such foods through invoking the modern tools of biotechnology and genetic engineering. A food-based approach towards successfully combating the problem of micronutrient malnutrition is eminently feasible. There are currently many attempts ongoing in different developing countries towards augmenting the production and consumption of micronutrient-rich foods. The data in table 4 will indicate, for instance, the progress being achieved in the matter of production of horticultural crops in India since the government took a conscious decision to accord horticultural crops its respectful place in agricultural development. There is also a vigorous attempt to diversify food production, and to avoid near total reliance on rice and wheat. Efforts at augmenting production of pulses and legumes, pisci- and aquaculture, poultry and milk production – all fall in this category. These new production policies will facilitate attempts to broaden and diversify the dietary base.


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Table 4. Increase in area and production of horticultural crops Year

Area, %

Production, %

Production/ hectare tons

1985–92 1992–98

3.2 30.9

5.9 46.8

5.78 14

Source: Indian Horticultural database, Ministry of Agriculture, GOI, 1999.

While emphasizing horticultural development, it is necessary to ensure that indigenous, easily cultivable, micronutrient-rich foods such as dark GLVs, namely fenugreek, coriander, cabbage, amaranthus, drumstick, mustard leaves and mint, other vegetables like carrot, pumpkin, turnip, sweet potato, and fruits like papaya, mangoes and guava get appropriate attention because the temptation is to concentrate on food items of commercial interest and export value not on inexpensive items for home consumption. Harnessing Emerging New Technology Even if we succeed in imparting a ‘second wind’ to the Green Revolution of earlier years, it is unlikely that the expanding food needs of the next century will be met. We must therefore opt for the judicious use of new technological breakthroughs that offer promise. The phenomenal population growth in developing countries has led to shrinking land resources, and food needs can be met only if we are able to produce substantially more food per unit of land in ways that do not involve ecological and social harm. Genetic Engineering. New genetic technologies offer promise of opportunities for breeding food crop varieties for resistance, tolerance to biotic and abiotic stresses, drought and salinity resistance and even better nutrient quality. Rice, for example, could be genetically engineered to contain vitamin A. Genetic technology applied to horticulture could result in the production of vegetables and fruits with improved micronutrient content and better acceptability. Large private corporations of USA and Europe are currently making major investments in using these technologies to produce new plant varieties for large-scale commercial agriculture. Much of this action is now occurring in the industrial countries under the purview of proprietary science. There is a concern that genetically modified (GM) foods rich in micronutrients produced by private corporations may be expensive and they may be beyond the reach of poor undernourished population groups in the developing countries. A way should be found to avoid such a situation. The free flow of knowledge and information, possible in the days of earlier Green Revolution, could now prove

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difficult for developing countries which need to benefit most from these new technologies. There is currently widespread concern regarding the safety of some GM foods and some of these may prove to be genuine. There seems to be a polarization of views regarding the safety of these foods; the ‘go-ahead’ optimism of USA is not apparently being shared by Europe. The present concerns relate to the possible direct effects of the transferred genes on the recipient organisms; on possibilities of unfavorable recombinations; on the behavior of these foods under actual field conditions; allergenicity and toxicity of these foods; on environment and biodiversity, and on nutritional quality. A recent statement [52] issued by the Royal Society of London on ‘Genetically modified plants for food use’ and recent papers on this subject by Swaminathan [53] and Paroda [54] present a somewhat balanced and not-too-euphoric picture. It is hoped that genetic engineering efforts will be informed and guided by humane and enlightened considerations. In the meanwhile, developing countries should have their bio-safety protocols in place ensuring thereby a critical evaluation of transgenic plants for possible harmful effects. The Promise of Biotechnology. Modern food biotechnology can be increasingly invoked to engineer and develop new varieties of food grains with increased content of micronutrients. Already, as stated earlier, there is promise that a new variety of rice (golden rice) with high levels of ␤-carotene, which is now being developed, will be available for distribution to farmers as early as 2003. Similarly, food grain varieties rich in iron are also being engineered [55]. The Rice Genome Project (RGP) initiated in India under international auspices offer much hope in this regard. It is to be ensured that increase in some micronutrients in some of these newly engineered varieties is not at the expense of yield, disease resistance, acceptability and culinary properties. It would appear that with increasing recognition of the importance of micronutrient content of foods on the part of plant breeders, vigorous attempts are ongoing to achieve significant upgrading of many varieties of food sources, vegetables and fruits, with respect to their micronutrient content. Plant-breeding strategies directed towards (i) increasing the concentration of minerals (iron and zinc) and vitamins (␤-carotene), (ii) reducing the amount of anti-nutrients such as phytic acid, and (iii) raising the sulfur-containing foods which can promote the absorption of zinc, also offer possibilities of augmentation of production of micronutrient-rich foods. These aspects have been ably discussed earlier by Ruel et al. [56] and need not again be dilated upon here. Increasing seed ferritin is a plant-breeding approach which seems to have considerable promise in increasing bioavailable iron in plants [57]. New genetic engineering approaches to simultaneously increase the availability of vitamin A and iron in rice are also ongoing. There would seem to be possibilities of


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reducing phytate content of staple foods through genetic engineering [58]. And this could considerably improve the bioavailability of zinc, iron, magnesium, manganese and other trace minerals. Gibson et al. [59] have described how changes in food production practices, food selection pattern and household methods of preparation and processing of foods can contribute to increased bioavailability of iron, zinc and vitamin A in plant foods. Strategies at the food production level include the use of fertilizers, plant breeding and genetic engineering to enhance the content and bioavailability of micronutrients in plant-based staples and increase the yield of indigenous edible wild plants. Household strategies involve small-livestock production, aquaculture, gardening projects and changes in certain food preparation and processing practices designed to alter the content of absorption modifiers in the diet, such as soaking, germination, fermentation and enrichment. These household strategies can be incorporated into existing food consumption patterns. Preventing Post-Harvest Losses. Post-harvest losses of horticultural products are in the range of 20–30% and these are attributable to the lack of adequate infrastructure for post-harvest handling, lack of appropriate technology for on-farm processing and in preservation and storage and poor handling. These shortcomings are now being increasingly corrected. Preservation and storage facilities capable of application at the village and the small-town levels can also contribute to the creation of millions of jobs in the countryside especially for women. An innovative policy can thus help not only to offset post-harvest losses but also to provide income generation especially to rural women. Plant Foods Rich in Micronutrients Many plant foods which are widely available in many developing countries are good sources of micronutrients (including phytonutrients). An example of common inexpensive food items which can provide micronutrients is indicated in table 5. Unfortunately, while many of these foods have been traditionally known to be health-promoting and, therefore, had formed part of the habitual traditional diets of populations of developing countries, in recent times they had gone into disuse. GLVs and other inexpensive vegetables have come to be looked upon as the ‘poor man’s food’ and do not enjoy social prestige. Even when they form a part of the family diet, these foods are generally not offered to children. Now that the nutritive value of these foods is being increasingly recognized by the affluent populations of industrialized developed countries, they are beginning to command increasing acceptance and respect in developing countries as well. Among GLVs, special mention has to be made of such inexpensive items like agathi (Sesbania grandiflora) and drumstick leaves (Moringa olifera) and

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Table 5. An illustrative (not exhaustive) list of commonly available inexpensive micronutrient-rich foods Vegetables

Rape leaves, cauliflower greens, amaranth, curry leaves, garden cress, drumstick (leaves), fenugreek leaves, beet greens, spinach, betel leaves, parsley, turnip greens, purslane, mint, carrots, lotus stem, tapioca chips, colocasia, radish, sweet potato, yam, ivy gourd, lettuce, mint, agathi, radish leaves

Condiments and spices

Poppy, cumin, coriander, oregano, green chillies (fresh/dry), turmeric, ginger, fenugreek, pepper, garlic, mango powder

Nuts and oilseeds

Coconut (deoiled/dry/milk), groundnut, cashew nut, walnut, pistachio nut, gingelly seeds, garden-cress seeds, safflower seeds, mustard seeds, niger seeds

Fruits

Indian gooseberry, water melon, custard apple, wood apple, tomato, guava, mango, pineapple, orange, papaya, grapes, banana, bael, pomegranate, gooseberry, apricot

Source: Gopalan [100].

ivy gourd (Coccina grandis). To this list must now be added the hitherto neglected ‘weed’ purslane [60], a good source of micronutrients and the richest source of ␻–3 fatty acids than any other green leafy edible wild plant. Updating Data on Micronutrient Content of Foods Increasing interest in ensuring adequate intake of micronutrients has fortunately stimulated investigations of micronutrient content of inexpensive foods in developing countries. The existing database on micronutrient composition of foods is mostly based on analytical techniques which are now considered outdated. Attempts should therefore be now made to evaluate foods for their micronutrient content using modern analytical methods like high-performance liquid chromatography (HPLC). This is already being attempted in some laboratories of developing countries. These efforts must be greatly expanded and intensified especially if we embark on programs of genetic upgrading of our horticultural products. Apart from fruits and vegetables, some cereals, pulses and spices and condiments are also micronutrient-rich. The recognition that cereals like bajra (Pennisetum typhoideum) and maize, generally consumed more by the poor income groups, can provide significant amounts of micronutrients because of their bulk consumption, and that pulses like red gram, Bengal gram and green gram are also fair sources of micronutrients, should serve to focus attention on the fact that these foods


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Table 6. ␤-Carotene content in different varieties of ripe mango Variety

␤-Carotene, ␮g/100 g

Alphonso Baneshan Chausa Dashehari Fazli Langra Mulgoa Neelam Pairi Totapuri

4,000–13,000 1,500–4,000 1,200–3,000 2,500–3,500 1,500–3,000 2,400–5,000 800–5,000 2,000–3,500 1,000–2,500 1,800–2,500

Source: Mango in India. Production, presentation and processing. Monograph published by CFTRI, 1990.

generally considered as source of calories and proteins can also provide micronutrients. Some spices and condiments regularly used in traditional diets are also good sources of carotenes. Assessment of nutrient intakes through conventional routine diet surveys could have often resulted in underestimation of the total intake of some micronutrients since the contributions from some of these minor food sources are not generally taken into account. Varietal Differences Considerable varietal differences with respect to the micronutrient content of foods are known to exist among fruits and vegetables. It is therefore important to identify high-yielding varieties of common fruits and vegetables that are rich sources of micronutrients. The enormous varietal differences in ␤-carotene content of the common fruits – mango and papaya, for example – are shown in tables 6 and 7. It is also known that striking differences in the ␤-carotene content of fruits can be seen at different stages of maturity. This has been illustrated with regard to papaya in table 8. New varieties of micronutrient-rich foods are now being identified. The Asian Vegetable Research and Development Center (AVRDC), Taiwan, has developed new strains of tomato with a high content of ␤-carotene which can be grown in the dry season and is resistant to many diseases. This new variety of tomato is orange and looks different from the traditional variety. Field trials are underway in Bangladesh to evaluate its acceptability by farmers and consumers.

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Table 7. ␤-Carotene content in papayas grown in India Variety

␤-Carotene ␮g/100 g

Coorg Honey Dew Pink Flesh (selfed) Pink Flesh Sweet Solo Large Sweet (selfed) Solo (open pollinated) Solo Small (open pollinated) Sweet Medium (open pollinated) Solo Yellow Sweet (selfed) Sunrise (open pollinated) Sunrise (selfed) Thailand Washington

2,189 2,829 2,039 2,249 3,808 2,286 2,979 3,066 960 954 1,319 3,069

Source: Papaya. Monograph published by the CFTRI, Mysore 1990.

Table 8. ␤-Carotene in papaya at different stages of maturity Stages of maturity

␤-Carotene content, ␮g/g

Vitamin A potency, ␮g

Pale yellow (unripe) Light yellow (unripe) Light yellow (ripe) Deep yellow (unripe) Pale yellow (ripe)

0.95 1.90 2.90 9.49 10.20

0.16 0.32 0.48 1.58 1.70

Source: Papaya. Monograph published by the CFTRI, Mysore 1990.

Another example of a new variety high in carotene is sweet potato. It has an orange color, unlike the traditional variety. The plant is high yielding and early maturing, which makes it a more acceptable food crop. Sweet potato is used as a staple food in some African countries and forms a major source of energy [61]. Recently, the International Food Policy Research Institute initiated a field project in Mozambique to encourage production and consumption of this new variety for sustainable nutritional improvement, addressing macro- as well as micronutrient malnutrition.


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Table 9. ‘Unconventional’ and ‘new’ sources of ␤-carotene Green leafy vegetables

␤-Carotene content mg/100 g edible portion

Botlabenda (Abutilion indicum) Chennangaiku (Cassia sophera) Tulasi (Ocimum sanctum) Betel leaf (Piper beetle) Ponnagantikura (Alternanthers sessilis) Mullatotakura (Amaranthus spinosus) Erra mulakakura (Amaranthus sp. Red) Chirrakura Uthareni (Achyranthus aspira) Spirulina Red palm oil Tummikura

12.6 11.9 8.2 5.9 5.7 10.8 9.8 7.1 4.1 250 50 4.1

Source: Combating vitamin A deficiency through dietary improvement. NFI Special Publication Series 6, 1992.

Unconventional Sources Attempts are also being made in several developing countries to identify new (‘unconventional’) food sources of micronutrients. Some of the unconventional food sources identified have been indicated in table 9. Some of these foods are consumed in tribal areas of India. Consumption of 50–60 g of some of these could meet the RDA of vitamin A. In Vietnam the gac fruit (Momordica cochinchinensis Spreng) is an excellent source of ␤-carotene (17–35 mg/100 g of edible portion). This fruit is familiar to indigenous people and is easy to grow. However, it has been underutilized because it is available only 3 months a year, there have been no efforts to educate the at-risk population about its nutritional benefit, and research efforts in production or preservation technique have been lacking [62]. Spirulina. It is now being increasingly recognized that microalgae are a rich source of several micronutrients including ␤-carotene. Their possible use as a source of a much needed micronutrient like ␤-carotene is now engaging the attention of nutrition and health scientists. Of the several microalgae which have been explored as a source of micronutrients, spirulina has scored over others because of several desirable features such as the absence of a cell wall, high photoefficiency, ease of cultivation, etc. Spirulina is a very rich source of ␤-carotene (containing 2–3 mg carotene per g of dry powder) and also of other nutrients, particularly vitamin B12 which is present only in animal foods, and

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also of ␣-linolenic acid useful in the prevention of cardiovascular diseases. A wide range of studies on health benefits of spirulina have also been carried out recently. Spirulina is also claimed to possess several health-promoting properties, such as prevention of diseases like cancer, diabetes, cardiovascular disease, retarding aging and increasing milk output in women, etc. However, these claims will need further investigation. Spirulina can be grown outdoors in simple media in open tanks and it is a high-yielder. Drying, however, poses some problems which can possibly be overcome by sun drying. A study on bioavailability of ␤-carotene from spirulina in rats indicated satisfactory bioavailability [63]. A study of carotene absorption in children indicated an absorption of around 72–75%. A daily supplement of 1–2 g of spirulina to pre-school children for a period of 1 month, provided as part of roasted Bengal gram preparation, resulted in a significant increase in serum vitamin A levels. Acceptability studies with spirulina-based food preparation indicated that it was satisfactory [64]. There are still some problems related to the deterioration of the ␤-carotene content, and to the shelf-life of spirulina preparations, and these have to be overcome before spirulina can be highly acceptable. Red Palm Oil (RPO). RPO is the richest known natural source of ␤-carotene. ␤-Carotene forms 56% of the total carotene in the oil, which ranges from 500 to 1,600 ppm. Though not one of the traditional edible oils, it is now being used in Indonesia, Malaysia and India. Studies have indicated that RPO is highly acceptable to pre-school and school-aged children as well as to adult members, except in the initial stages of its introduction when some subjects were not used to its odor, color and taste [65]. Refined crude RPO produced by molecular distillation is now available. It is a highly acceptable product free from any off odor of crude palm oil and also low in free fatty acids. It had 550-ppm carotenes and 400-ppm ␤-carotene equivalents. Thus, RPO can be promoted as a source of carotenes as well as tocopherols and tocotrienols all of which are also antioxidants. Improved Culinary Practices Apart from augmenting the production of micronutrient-rich foods, and apart from preventing food losses through effective measures of processing and packaging, the actual consumption of these foods must be promoted through nutrition education. Better culinary measures to improve the acceptability of these foods must be identified and widely propagated. Indeed considerable work has been carried out in these directions in Home Science colleges in India and other developing countries. Minimal losses of ␤-carotene in foods were observed if the vegetables were washed before cutting. Steaming/pressure cooking retained more ␤-carotene than cooking without lid.


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GLV

Leaf

Leaf curd

Amaranth Spinach

7.1 2.2

12.3 9.9

Table 10. ␤-Carotene content of leaf and leaf curd preparations (mg/100 g)

Source: Bhaskara Chary K: Food base strategy for combating vitamin A deficiency. Nutr News 2000;21(2).

Cooking greens with tomato helped in better retention of ␤-carotene possibly because of the protection from lycopene (red-colored pigment of tomato, a powerful singlet oxygen quencher). Oil used in sautéing helped in retaining ␤-carotene. All this would show that by simple practices capable of application in traditional households, cooking losses of micronutrients can be avoided. Drying of GLVs in solar wooden containers was found to be effective in retaining ␤-carotene. Such containers can be made even in poor households. In order to enable children to consume adequate amounts of GLVs to meet their requirements, ‘leaf concentrates’ can easily be prepared in homes from GLVs using an ordinary food grinder and curdling the leaf juice through slight warming. Amaranth and spinach leaf concentrates prepared thus were found to contain 70–350% more of ␤-carotene than fresh leaves (table 10). Other carotene-rich food sources can be leaf protein concentrate (LPC). LPC was developed earlier as a source of protein by The Central Food Technological Research Institute (CFTRI), Mysore, India. LPC can also be a rich source of carotene and other micronutrients. The available technology for the manufacture of LPC may have to be modified to maximize its carotene and other micronutrient content. LPC can be used as a supplement to provide protein, carotene and other micronutrients like iron, zinc, B vitamins and calcium. CFTRI has developed a process for dehydrating the whole green leafy plant including stem and leaves intact. Such a dried green leafy plant can be rehydrated to obtain an almost fresh GLV. This process is not as yet commercialized.

Bioavailability of Micronutrients from Plant Foods There have been some recent claims [66, 67] suggesting that micronutrients like ␤-carotene from plant foods are poorly bioavailable, thus implying that these foods will be ineffective in combating micronutrient deficiencies. According to these claims, it would appear that ‘profligate’ Nature, while it has endowed plant foods with several micronutrients has also ensured that they will be largely non-bioavailable making it necessary for humans to look to other

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non-food sources! These claims can be challenged. The points to be taken note of in this regard are: • Carotene absorption studies carried out in India [68, 69] using locally consumed GLVs showed that ␤-carotene absorption from GLVs was in fact even higher than the level of 33% absorption (conversion factor of 1 ␮g ␤-carotene ⫽ 0.167 ␮g retinol) proposed by the joint FAO/WHO Expert Committee after an extensive review of balance studies on different groups. According to Indian data, 50% of carotenes with provitamin A activity in GLVs are absorbed by adult men as well as by children, and the Indian Council of Medical Research had therefore adopted a factor of 1 ␮g ␤-carotene ⫽ 0.25 ␮g retinol. • Studies on children with vitamin A deficiency in whom the effect of feeding ␤-carotene-rich foods was investigated showed that 1,200 ␮g of ␤-carotene in the form of GLVs did bring about a significant improvement in serum retinol levels. While such significant elevation of serum levels of retinol through the feeding of ␤-carotene-rich foods could be demonstrated in deficient groups, in non-deficient subjects with normal serum levels of retinol, significant elevation of serum retinol levels could not be demonstrated. This cannot be interpreted as evidence of unavailability of dietary carotene. The subjects investigated in the studies on which the claims of poor bioavailability were based had normal serum retinol levels to start with [70]. Studies carried out by Periera and Begum [71] on children in an orphanage showed that even on a daily intake of 30 g of vegetables satisfactory levels of serum vitamin A were maintained for a longer duration as against on receiving massive doses of vitamin A. • Apart from ␤-carotene, it has also been observed that the bioavailability of food iron is also influenced by the host’s hemoglobin status. That the host’s nutritional status with respect to a given nutrient could have an influence on bioavailability is also suggested by observations on bioavailability of other micronutrients. An up-regulation of conversion of ␤-carotene to retinol, in states of vitamin A deficiency and of iron bioavailability in the case of iron deficiency, seems possible. It is tempting to suggest that the bioavailability of a micronutrient from a food is to some extent regulated by the host’s requirement and could thus be a regulatory phenomenon. While the evidence in this regard is at best suggestive and not, as yet, direct and conclusive, the possibility has to be kept in mind. Bioavailability, interpreted in this manner, could be evidence of the ‘Wisdom of Nature’ and not of its Profligacy! It is possible that because of such regulation of bioavailability from natural foods that toxicity due to excessive intake of micronutrients from natural foods never exists, as opposed to the expensive synthetic nutrients.


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•

•

•

In the study by de Pee et al. [66], 64% of the subjects investigated had normal levels of serum retinol to start with. In the study of Bulux et al. [67] among Guatemalan children also, the children with serum levels of 35 ␮g/dl did not respond with any increase in serum levels when given a diet of carotene-rich foods. As was pointed out earlier, this cannot be construed as evidence of poor bioavailability. It also seems possible in de Pee et al.’s study that in the subjects in the experimental groups getting nearly as much as 150 g vegetable supplement daily, the habitual intakes of vegetables in their home diets could have decreased unlike in the ‘wafer’ supplemented control group that was not getting the vegetable supplement. The assumption of poor bioavailability based on these studies may not be justified. Apart from the experimental evidences above, there is convincing epidemiological evidence as well. Epidemiological data lend support to the observation that among populations consuming adequate quantities of carotene-rich plant foods as a major source of provitamin A, vitamin A deficiency is rarely seen. For example, in parts of India like Jammu and Kashmir, Punjab and Haryana [72], and among tribal communities in the Northeast and Madhya Pradesh [73], vitamin A deficiency is rare because of the high level of consumption of a wide range of GLVs [74]. On the other hand, in the eastern and southern parts of India, where carotene-rich foods are only infrequently consumed, vitamin A deficiency among children is quite commonly encountered. Even in areas where vitamin A deficiency in the form of Bitot’s spots is seen, it is a very small minority of the population that is affected, suggesting the possible role of infections – especially respiratory infections – in such areas rather than dietary deficiencies. The validity of current methods used for assessing bioavailability, from which conclusions as to the inefficacy of vegetables as sources of micronutrients have been drawn, can be questioned. In several studies of ␤-carotene bioavailability where rise in serum retinol levels following on food consumption was used as the parameter, the subjects chosen were those with normal and high serum retinol levels. More recently, attempts have been made to measure ␤-carotene conversion to retinol by extrinsic tagging of the food with 13C-labeled synthetic ␤-carotene and measuring the level of retinol and ␤-carotene in the chylomicron to obtain the ratio of labeled and unlabelled carotene and retinol. On the basis of these data, very low conversion rates (22:1) have been reported. The flaw in this procedure is that if the extrinsically added 13C-labeled carotene does not equilibrate with the carotenes present in the food matrix, distorted ratios for carotene conversion to retinol could be obtained. The carotene present

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in the food matrix may be expected to be released slowly while the added labeled carotene may be converted and absorbed rapidly without equilibrating with dietary carotenes in the gut. This type of approach may be appropriate with red palm oil but not for carotene-rich plant foods like GLVs. • Plant foods contain, besides ␤-carotenes, other carotenoids as well. Due to structural similarity, non-provitamin A carotenoids, namely lycopene, may competitively interact with the enzyme which converts provitamin A carotenes to retinol to reduce the conversion efficiency. There is also evidence of interaction between carotenoids during absorption [75, 76], although the mechanism for such interaction has yet to be elucidated. Carotenoids are now known to perform important metabolic functions. The total effect of plant foods on health, despite seemingly poor bioavailability of one of its contents, may actually be greater than that obtained with single synthetic nutrients. In the study in Nepal, wherein greater reduction in mortality was claimed to be achieved with ␤-carotene than with vitamin A [77], would suggest that the antioxidant function of carotenes rather than its provitamin A function was perhaps responsible. There is a clear need to improve and standardize current methods for measuring bioavailability of not only ␤-carotene but of other micronutrients as well. Conclusions based on current faulty techniques may not be appropriate. Plant foods contain a multiplicity of nutrients – all of which may be required for human health. It is this multiplicity that is their special virtue as compared to a single synthetic nutrient. The fact that any single nutrient in a plant food is relatively less bioavailable than an equivalent amount of pure isolated synthetic nutrient does not by any means imply that plant foods are of lower nutritive value than synthetic nutrients. It is indeed very rare that a human subject suffers from a single isolated micronutrient deficiency (iodine deficiency may be an exception). In a subject presenting symptoms related to a specific nutrient deficiency, biochemical tests could detect other deficiencies as well. It is rather intriguing that, on the one hand, national bodies of developed countries are advocating increased intake of vegetables and fruits by their populations, and vegetable foods and plant foods in fact are getting increasing focus in their ‘Dietary Guidelines’, while, on the other hand, developing countries are being told that nutrients in vegetables are poorly bioavailable and rather ineffective in controlling micronutrient deficiencies – and this at a time when their national governments are engaged in vigorous programs to augment the production and consumption of vegetables and fruits by their populations. International agencies will be rendering real service to developing countries by strongly propagating ways by which the bioavailability of micronutrients from horticulture plant foods available at their door steps can be improved by: (a) improved cooking and processing procedures; (b) better preservation


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techniques that could increase availability throughout the year; (c) homeprocessing techniques to reduce inhibitors of absorption; (d) simple methods of achieving enzymatic hydrolysis of phytates in cereals and legumes through fermentation and germination; (e) promoting non-enzymatic methods of reducing phytic acid content, and (f) invoking home-processing techniques like malting, avoidance of drinking of tea and coffee with the meal, reducing the use of tamarind (rich source of tamarind) as a souring agent and instead use tomato or lime juice, in order to facilitate non-heme iron absorption. These procedures have been well discussed by Ruel et al. [56] and need not be further discussed here. The foregoing discussions will show that there are a wide variety of inexpensive micronutrient-rich foods right at the very doorstep of poor village communities. While the nutritive values of some of these are known, there is reason to believe that quite a few plant foods are currently unused and fall in the ‘unfamiliar’ category and are being currently wasted. The challenge to policy-makers and scientists of developing countries is: (1) to increase the production and availability of micronutrient-rich foods – this is easily feasible; (2) to enhance their nutritive value using modern tools of biotechnology; (3) to prevent their wastage by invoking simple methods of preservation and storage; (4) to improve culinary practices to avoid losses of micronutrients during cooking, and (5) to develop methods of processing these foods in order to improve their nutritive value, acceptability and shelf-life and thereby to promote the consumption of these foods. Micronutrients from Non-Plant Foods Apart from plant foods which have been discussed above, there is considerable scope in developing countries for the augmentation of production and consumption of marine and riverine food sources, poultry and milk. With the vast coastlines and numerous rivers that the Asian countries enjoy, there is considerable scope for optimal use of marine resources. Aquaculture and fish cultivation in paddy fields could be extended. With improvement of cattle breed, it should be possible to augment milk production a great deal higher than the present levels. Thus, possibilities of improving the production and consumption of micronutrient-rich foods which would enhance the quality of household diets are large and still untapped in many developing countries.

Supplementation/Fortification with Micronutrients

Foods are the obvious natural sources of all nutrients, including micronutrients. Through the ages, Man has depended solely on natural foods for

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nutritional well-being. It is strange that in this 21st century, one has to defend and plead for food-based approaches to prevent malnutrition! In recent years, several nutrients have been synthesized and are now being marketed as pills, tablets and capsules. The use of such synthetic nutrients as supplements to overcome nutritional deficiencies is sought to be widely promoted. That synthetic nutrients have a legitimate use in therapeutic management of diseases, including frank nutritional disorders, will not be denied. That in certain special situations they could also be useful adjuncts to a food-based approach may also be recognized. The question for our present purpose is however: What is the place of such synthetic nutrients in routine public health practice for the prevention of malnutrition and for ensuring normal health and well-being? Practically all nutrients required for human health and well-being can be derived from foods. As was pointed out earlier, there could be a few special situations in which foods may need to be fortified or supplemented with synthetic nutrients. Supplementation/fortification should be considered as an adjunct to dietary diversification and dietary improvement and not as an alternative strategy. Dietary diversification and improvement is an inescapable necessity which cannot be bypassed or evaded by shortcuts. Present programs/proposals for supplementation and fortification can be considered under three heads: (i) cases where valid scientific justification and practical need exists and where the procedures involved are in consonance with approaches towards overall dietary improvement and national development; (ii) the (debatable) case of vitamin A supplementation, and (iii) cases where no valid scientific justification or practical necessity exists. Cases Where Valid Scientific Justification and Practical Need Exists Iodine. A valid case exists for fortification of common salt with iodine in areas of the world where iodine deficiency is an important problem. Not that foods do not contain iodine, but in recent years, iodine deficiency disorders which were earlier confined to the hilly regions – to the foothills of the Himalayas in the case of India – have now invaded the irrigated plains. This has happened not only in India but Indonesia as well [78]. Intensive irrigation, which is part of the agricultural technology being adopted in the wake of the Green Revolution, has apparently led to the leaching out of iodine from the soil. Soil iodine depletion is leading to poor content of iodine in foods grown on such soils, and this is being reflected in the wide prevalence of neonatal hypothyroidism in endemic areas. Soil testing and soil replenishment, which should have gone hand in hand with other aspects of the Green Revolution technology, had apparently been relatively neglected. Furthermore, possibly due to the intensive use of pesticides – again a part of the intensive agriculture


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technology – it has been found that goitrogens in the environment have increased thus causing increasing iodine requirements. In view of these conditions, programs of iodation of common salt with potassium iodate have been successfully undertaken in some countries. Despite recent resistance to this measure from some quarters, this is a program of proven worth and scientific merit and must continue [79]. The use of iodized oil or of lipiodol injections on the other hand is totally inappropriate, expensive, unsustainable and possibly harmful [80]. ‘Disposable syringes’ expected to be used in programs of iodized oil injections could often not be ‘disposed’ in mass operations and could aggravate the problem of drug addiction and AIDS. Salt iodation, on the other hand, is a perfectly safe and tested procedure and should be the basis of public health programs designed to control goiter. Iron. Yet another micronutrient, the deficiency of which is widely prevalent, especially, in pregnant women, is iron. Theoretically speaking, foods including plant foods (despite phytates), can provide human iron requirements. Iron requirements in early pregnancy which is as low as 0.8 mg/day due to absence of menstruation, rises to an average of 3.5 mg/day in the third trimester [81]. The fetus contains 270 mg iron, the placenta 90 mg, the red cell mass increases by 450 mg and the average post-partum blood iron is 150 mg. Thus the total cost of pregnancy is 1,190 mg of iron [82]. This increased requirement is partly compensated for by increased absorption (40%) of iron in late pregnancy and iron saving due to temporary cessation of menstruation (200 mg) [83]. All this implies that special care should be taken to include higher levels of iron-containing food items in the diets of pregnant women. This is generally not done, the diets in pregnancy in poor populations being no different from the habitual family diets. It is in recognition of this that a national program of iron/folate supplementation during the last 100 days of pregnancy (200 mg of ferrous sulfate equivalent to 60 mg elemental iron and 500 ␮g of folate) has been in operation in India. This supplementation program, it must be confessed, has been no shining success, partly because of poor compliance; but, even more importantly, because it has not been accompanied by sustained and vigorous attempts at diet counseling designed to achieve improvements of diets of women during pregnancy. This would incidentally show that ‘supplementation’ programs, even, where necessary, can succeed only as adjuncts to programs designed to bring about improvement of habitual diets in households and in situations where there is a competent and alert public health set-up. A significant proportion of adolescent girls of poor communities has been found to have hemoglobin levels below 10 g% [84]. This could mean that many of these girls are anemic even at the time of conception, and pregnancy only serves to aggravate the anemia. It is not surprising that iron supplements during

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the last 100 days of pregnancy, specially given the poor compliance, has not yielded striking results. The latest data from the survey carried out by NFHS provides some important lessons. Kerala, in the south of India, is a relatively poor state as compared to Haryana, Uttar Pradesh, and Bihar in the north and yet the prevalence of anemia in that state is extremely low. This would highlight the point that micronutrient malnutrition in general can be combated even in poor communities through judicious use of local foods and proper healthcare. Kerala is also the Indian State with lowest infant and child mortality and birth rate. The Kerala experience would show the importance of nutritional status with respect to micronutrients is likely to be achieved as part of all-round development and not just through narrow vertical programs. Double Fortification of Salt with Iron and Iodine Since salt is already being iodized, and since salt is a universal food used by the poor as much as by the rich, there could be a reasonable case for double fortification of common salt with iron and iodine. An added scientific justification for this is the reported finding that iron deficiency could impair the efficacy of iodine supplementation [85], yet another example of micronutrient interactions. The technology for double fortification of common salt with iron and iodine was pioneered by Narasinga Rao [86] at the NIN, Hyderabad, using sodium hexa-metaphosphate as a stabilizer. In the double fortified salt obtained by this procedure, iodine and iron were both found to be stable; iron absorption from the salt was satisfactory [87] and the salt was acceptable to the consumer [88]. More recently, three techniques for the dual fortification of salt are being investigated at NIN: (i) salt fortified with ferrous fumarate plus dextrin encapsulated potassium iodate (developed by the Micronutrient Initiative), (ii) fortification with sodium iron EDTA, and (iii) fortification with ferrous sulfate, sodium hexa-metaphosphate and potassium iodate. The results of these studies could provide guidance in the search of an iron-iodine salt fortification procedure. Where, for some reasons, fortification of common salt with iron is not considered possible or suitable, fortification of any other commonly used food item with iron may merit consideration. Wheat flour could be possibly one such food item. But there are several practical difficulties in this regard. In India, out of the 70 million tons of wheat produced, only 8 million tons are processed in roller mills where wheat flour can be successfully fortified with iron. Such ironfortified wheat can reach only urban middle and upper middle income groups. Further, wheat is a staple for only a segment of our population. Similarly, like wheat, rice is also not centrally processed; in fact, processing is done to a large extent in individual homes. Iron fortification of rice is technologically more


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difficult and expensive and is possible only in large modern rice mills which limits the quantity of rice processed. Moreover, among the poor, who are the intended beneficiaries of such a program of iron fortification, much of wheat and rice currently consumed is practically consumed off the land and hardly ever enters the market. An analysis of the offtake of these staples from the Public Distribution System (PDS) in India shows that the actual amount of staples consumed by the poor far exceeds the amount taken out of the PDS. In short, it is difficult to find out a food item which is used daily by almost the entire poor population and could qualify for iron fortification. Under the circumstances, common salt is the best option. Technological hurdles in the way of implementing a program of iron fortification of common salt along with iodine fortification therefore need to be sorted out and overcome. It must however be emphasized that even after such fortification, the need for dietary improvement with regard to the intake of iron-rich foods has to be attended to. Folic Acid. There is yet another very special situation, which may justify supplementation. A specific variant of the folate-related enzyme 5,10-methylene tetrahydrofolate reductase, which causes partial enzyme deficiency, has been described in 5–15% of North American populations with low folate status [38, 39]. This variant increases the risk of homocysteinemia, neural tube defects and coronary heart disease. Folic acid requirements for combating this condition are of an order that cannot ordinarily be met by diet alone and could also need additional folic acid supplementation. The extent of this genetic variant in populations of developing countries is however not known. In any case, since this is a condition affecting a very small percentage of the population, public health prescriptions may be unwarranted at this stage. This case is mentioned only for the sake of completeness of the case for supplementation. The (Debatable) Case of Vitamin A Supplementation Vitamin A. A micronutrient which has attracted considerable attention in recent years is vitamin A. While the importance of vitamin A in human nutrition cannot be denied, it seems somewhat strange that international and bilateral agencies have accorded far more interest and attention to this nutrient than say to iodine or iron, the deficiencies of which currently affect millions of people. On the other hand, there has been a decline in the incidence and severity of vitamin A deficiency manifestations during the last four decades. The same can certainly not be said of iron deficiency anemia. Those who have had a ring side view of the changing epidemiological scene with respect to vitamin A deficiency during the last five decades can testify to the fact that keratomalacia, once a major public health problem in Asia, has ceased to be so though cases of keratomalacia and corneal xerosis are still being seen occasionally. Milder forms of vitamin A deficiency in the forms of Bitot’s spots are still being

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encountered in highly deprived pockets of poverty as part of general undernutrition and that in certain seasons when GLVs are in short supply. This sharp decline in vitamin A deficiency, even among relatively poor populations, has been achieved not through massive dose vitamin A prophylaxis program which was unsuccessfully initiated by the NIN, Hyderabad, for the first time, over 30 years ago. This decline in vitamin A deficiency has paralleled similar decline in the incidence of classical kwashiorkor, again achieved not through supplements of fish-protein concentrates vigorously canvassed by the bureaus of commercial fisheries of some developed nations, but through allaround improvement consisting of general mitigation of abject poverty, control of infections and some dietary improvement. The Mortality Reduction Claim Vitamin A supplementation to poor communities is also now being canvassed on the ground that it could bring about an overall reduction in mortality. The exact metabolic mechanisms involved in bringing about this mortality reduction have not been explained, apart from conjectures. While the studies of the John’s Hopkins School [89] have claimed mortality reduction, investigations from two other prestigious schools – Harvard School of Public Health [90] and the NIN, India [91] – had failed to substantiate this. Thus the claim of mortality reduction rests not on the basis of independent verification by different ‘independent’ teams, but on the basis of a tortuous statistical exercise – a meta-analysis, the validity of which can be assailed on many grounds. This exercise seems to have suffered from serious flaws of ‘inclusion’ and ‘exclusion’ of data. Loading the data pool in the metaanalysis exercise with findings from multiple studies (some of them from the same group of investigators) claiming positive results as against data from single studies from other schools which had come up with negative results could have introduced an (unintentional) error. If the former studies did in fact suffer from methodological errors, loading the data pool with findings from multiple studies from the same group could yield erroneous conclusions. Also, the exclusion of some data from the Harvard study on questionable grounds could have compounded the error. The meta-analysis exercise also assumes that the effect of massive doses of vitamin A on a population is likely to be uniform and independent of environmental and host factors and associated nutritional deficiencies. It will be wrong on the part of public health authorities of developing countries to assume that the ‘mortality reduction claim’ has been scientifically proved beyond doubt and to promote the expensive public health operations on this basis. The mortality reduction claim has been extensively commented upon and the arguments for its unacceptability have been explained [92, 93]. In the Aceh [94]


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study in Indonesia, for example, steep reduction in mortality was present not only in the group receiving vitamin A, but in the unsupplemented group as well, the difference in mortality as between control and experimental being only a fraction of the overall reduction in mortality in both groups as compared to the prevailing figures in the community. The possibility that the mortality reduction could be an artifact being the result of the Hawthorne effect [95] had been pointed out. The Hawthorne effect may be expected to be especially marked in communities with lack of basic healthcare. Valid arguments against the claim of mortality reduction in the recent Nepal study [77] by the same group have been advanced [92, 93, 96] by three competent groups of scientists and these have not been satisfactorily explained. Quite a part of differences in mortality between the control and experimental groups in the Nepal study was accounted for by deaths due to drowning and snakebites in the control group! Incidentally the mortality reduction claim in the Nepal study also rests on a debatable statistical exercise. There was no statistical difference in mortality between the vitamin A supplemented group and the control group. It was also noted that the mortality reduction obtained with ␤-carotene supplementation was actually greater than that with vitamin A supplementation, suggesting that the possible biochemical mechanism by which the mortality reduction was probably achieved in the ␤-carotene group was not due to its provitamin A function. It was through pooling the data from these disparate groups that ‘statistical significance’ could be extracted! In short, the claim of mortality reduction seems debatable and it will be unethical to base public health preventive programs consisting of vitamin A supplementation on the present evidence. The editorial in the British Medical Journal, which carried the article, wisely concluded: ‘Before we move to implement widespread supplementation programmes, several issues need clarification. As well as evaluation of the practical and economic implications, there should be further evaluation of health benefits and possible hazards to women of child-bearing age and their children.’ National and international agencies should heed this advice. Villamor and Fawzi [97] of the Harvard School of Public Health, report: ‘Findings from vitamin A supplementation trials are not consistent. Supplementation has resulted in significant reduction in mortality in several (but not all) large community-based trials among apparently healthy children. In hospital-based studies, vitamin A supplements have been consistently found to reduce the severity of measles infection, but no effect on respiratory infections has been observed. In some cases, the supplements were associated with an apparently increased risk of lower respiratory infections. Vitamin A supplements also reduced the severity of diarrheas in most (but not all) trials.’ These authors have pleaded for ‘more research on factors that effect the bioavailability

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and retention of the large vitamin A dose’. They point out that: ‘Large programmes of vitamin A supplementation can put financial and logistic strains on the health care systems of developing countries. Toxicity due to ingestion of multiple large doses over a short period is also a real possibility that needs to be guarded against.’ The authors conclude: ‘A more sustainable solution to the problem of vitamin A deficiency is to guarantee that the population has an adequate consumption of vitamin A in the diet. Most communities in which VAD is a serious problem have abundant supplies of vegetables and fruits rich in carotenoid with provitamin A activity.’ The populations in which vitamin A supplementation was supposed to have resulted in mortality reduction were extremely poor and deprived of basic healthcare. It can be nobody’s case that the way to reduce mortality in such populations is through vitamin A supplementation! The obvious inescapable approach for any responsible public health agency is to ensure basic healthcare, to its people and not look for magic bullets and short cuts. It is extremely doubtful if any notable mortality reduction with vitamin A supplementation could have been demonstrated if basic healthcare had been extended to this population. In spite of high-pressure publicity, there is no valid case for vitamin A supplementation as an alternative to basic public healthcare for preventing mortality in children or pregnant women [98]. It will be unfortunate if international agencies, which had forcefully pleaded for Primary Health Care in Alma Ata, now lend support for vitamin A supplementation as an alternative strategy for mortality reduction, abandoning the case for primary healthcare! Efficacy of Massive Vitamin A Dose Prophylaxis Apart from logistic problems related to the delivery of massive vitamin A dose, there is reason to doubt the biological efficacy of this approach. According to epidemiological evidence, the massive dose vitamin A prophylaxis is no more than a ‘hit-or-miss’ approach and cannot be a reliable solution to the problem of vitamin A malnutrition. The limitations of the massive dose approach, apart from poor implementation, were poor shelf-life of vitamin A, poor transport and storage facilities, and most importantly, unpredictable poor response as judged by the serum vitamin A levels [71, 99]. This raises the important point of possible variations in the bioavailability of massive doses of vitamin A which is possibly determined by a series of host factors such as (i) presence/absence of infections (including respiratory infections) and (ii) availability of retinol-binding protein and zinc and such other factors involved in the transport of vitamin A to the target tissue. It is quite possible therefore that in a considerable proportion of cases, massive doses of vitamin A could be ineffective. It certainly cannot be


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concluded that a massive dose of vitamin A brings about a uniform elevation of serum vitamin A levels in all cases. The assumption that massive vitamin A prophylaxis will be as effective as daily supplementation could be wholly erroneous. It is at best a hit-or-miss approach, which may perhaps be justified in an emergency but not as a routine public health measure. In a study of the effect of massive oral dose of vitamin A in malnourished children, Pereira and Begum [71] showed that children receiving a massive dose of vitamin A maintained a slightly higher average value of serum vitamin A till the 13th week after administration. After this, even the average value between control and experimental were same. What was important to note was that the difference between the control and experimental groups was statistically significant only in the first 2 weeks after the administration of the dose. This was because of wide variation in response. The authors concluded that, ‘moderate amounts of carotene in the diet provided by 30 g of GLVs were effective in maintaining serum vitamin A levels for a longer time than a single massive dose of synthetic vitamin A; the sustained protective effect following the feeding of GLVs argues that liver storage is greater in children given small amounts of carotene repeatedly than when they are given a single massive oral dose of vitamin A’. Another study [99] by the same authors showed that even after a massive dose of vitamin A, children maintained on a low carotene diet showed conjunctival xerosis, and led them to conclude that ‘massive doses had had no clinical or biochemical advantage for children on a moderate carotene diet at a level which even an orphanage can provide’. Obviously, the right approach to combat vitamin A deficiency is to promote the inclusion of provitamin A-rich foods in household diets and to promptly control infections, particularly respiratory infections and not to place reliance on possibly ineffective alternatives. There is considerable epidemiological evidence that massive vitamin A dose can be no alternative to sustained daily intake through dietary improvement. Keratomalacia is the result of a combination of protein energy malnutrition (PEM) and vitamin A deficiency. Practically every case of keratomalacia suffers from severe PEM. It is possible that the lack of transfer protein (RBP) serves to accentuate the clinical effects of vitamin A deficiency. While it may be possible to mitigate keratomalacia with vitamin A alone, the right approach will be to address the problems of PEM also simultaneously. It is necessary to emphasize this point because while the prevalence of keratomalacia in a community is being advanced as a justification for a vertical program of massive vitamin A dose prophylaxis, the need for improvement of protein-energy nutritional status of the same population is lost sight of. This consideration will probably argue in favor of a food-based approach rather than an isolated vertical approach confined to one nutrient – vitamin A.

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Case Where No Valid Scientific Justification or Practical Necessity Exists Multivitamin Supplements in Pregnancy as a Public Health Measure. In recent months, some international and bilateral groups have been proposing that health administrations of poor developing countries of South Asia and Africa be persuaded to adopt a blunderbuss polypharmacy approach of distribution of a capsule containing a cocktail of about 15–17 micronutrients, daily, to all pregnant women and adolescent girls. This is suggested as an instant public health solution to the problem of poor pregnancy outcome in these countries. The arguments against this measure have already been dealt with in a previous publication [100]. It is not that there are no micronutrient deficiencies involved in poor pregnancy outcome. In all probability there are. But the way to overcome these deficiencies is not to resort to a fishing expedition – a hit-or-miss blunderbuss polypharmacy approach involving a few micronutrients which may be necessary, quite a few which may not be, and a few which may even be harmful. It is also possible that the proposed composition does not include quite a few other micronutrients, phytochemicals and antioxidants, which may in fact, be useful. What needs to be emphasized is that: (1) the specific multiple micronutrients responsible for poor pregnancy outcome must first be scientifically established; (2) the level at which the supplementation has to be carried out to correct these deficiencies must be carefully identified, and (3) the micronutrient deficiencies so identified as requiring correction should be such that their correction cannot be achieved through dietary diversification using locally available foods. Similarly, a proposal for spraying an arbitrary mix of multiple micronutrient supplement on foods being supplied to children in India’s Integrated Child Development Program is being pushed by some agencies. To date there has been no attempt to find out if the micronutrients sprayed on the foods are in fact stable under the conditions in which these meals are served and whether at all they have done any good. Glorifying this approach as the final solution will be an act of disservice to developing countries. Resources of developing countries should not be frittered away in such futile operations. Food-Food Fortification In the discussions above, we have been considering mainly supplementation with synthetic micronutrients. There is however considerable scope for fortification of foods with other foods. The striking example is the fortification of wheat flour (three parts) with soya flour (one part). This combination could vastly improve the nutritive value of the staple and also the protein quality. This will be far better than the proposal to fortify wheat flour with lysine, which has been mooted in some quarters. There is considerable loss of important micronutrients


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incurred in the course of processing of cereals, especially of wheat and rice. The association of consuming highly polished rice with outbreaks of beriberi in parts of India and its eventual control due to an edict preventing polishing of rice will be discussed in the next section. There is a case for improved procedure of processing of foods, which will ensure minimal losses of micronutrients. In the fortification of cereal products ‘restoration fortification’ which attempts to restore nutrients lost in processing may be justified. However, indiscriminate addition of a multiplicity of nutrients to processed foods has no scientific sanction. There are quite a few other possibilities of food-food fortification that could be explored depending on local foods and food preferences. Use of indigenous food items, made from locally available foods like rice bran, sesame and jaggery are rich in iron and other micronutrients. The Intensive Food Production Technologies – part of the Green Revolution – had not always gone hand in hand with programs to correct soil micronutrient depletion. As a result, soils in many countries which have registered impressive increase in food production have been depleted of important micronutrients like zinc and iron. Soil enrichment programs, which will ensure the micronutrient content of soils, could be very important from the point of view of ensuring adequate micronutrient content in foods grown in such soils. Soil testing and soil replenishment should therefore find an important place in future programs of food production.

The Case for Dietary Improvement with a Food-Based Approach

Even if ‘supplementation’ programs are pushed to extreme limits, natural foods will have to continue to play the major role in ensuring optimal nutrition. Foods are bound to the major (only) source of macronutrients and possibly several other micronutrients even in the poorest households. That micronutrient supplements like iodine and iron and possibly folate (especially in women in the reproductive age group) will be necessary in populations subsisting on plant foods, even after dietary diversification, is an acceptable view. What however, is not acceptable are the several ongoing attempts to push multiple micronutrients in arbitrary amounts to poor populations as a public health measure to prevent micronutrient deficiencies among them. This has no scientific basis and there is no evidence or proof from field studies to show that this blunderbuss approach has actually helped any community when operated as a Public Health Program. It would be unethical under the circumstances to push this approach. The arguments that are advanced in favor of augmenting the nutritive quality of diets through an arbitrary mix of synthetic supplements in preference to dietary

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improvement through the right choice of foods are (i) that poor populations cannot afford dietary improvement and (ii) that dietary improvement with foods will be a time ‘consuming process’ and may not work in many poor countries. Both these assumptions are not valid. In the first place, it must be remembered that in poor families, diets are deficient all round, including calories and proteins, not just in a few micronutrients. It is nobody’s case that micronutrient supplements can offset calorie and protein shortage. Indeed dispensing micronutrients in such situations will be a wasteful procedure. One is reminded in this connection of the Bengal famine when thousands of people were dying of starvation; there were those who suggested the distribution of B-complex tablets and succeeded in persuading the government of the day to adopt this procedure! Surely, micronutrient supplements cannot be the answer to the problem of poverty. On the other hand, if even habitual foods can be taken by the poor in quantities to meet their caloric needs, micronutrient needs will also be met to a certain level; with further improvement in the quality of diets using local foods, micronutrient adequacy can be achieved. Spraying or supplementing an arbitrary mix of micronutrients on diets, which are inadequate in calories, proteins and a whole range of micronutrients again has no scientific sanction. The Practicability of Dietary Diversification The arguments that food-based approaches do not work in developing countries is without foundation. During the last few years there have been several successful attempts at achieving dietary diversification through the use of local foods. In table 11 we have listed some of the recent reports on community-driven food-based approaches for solving the problem of undernutrition including ‘micronutrient malnutrition’ in developing countries. This massive evidence, based on actual field experience in developing countries, provides an effective rebuttal for the argument that food-based approaches are not practicable in developing countries and that micronutrients from plant foods may not be bioavailable. A comprehensive food-based approach towards achieving household nutrition security (including micronutrient adequacy) is in effect a ‘people’s movement’. The corner stones of this movement are self-help, self-reliance and the effective mobilization and optimal utilization of locally available food resources. It is not an approach based on dependence, doles and drugs. The basic philosophy behind the food-based approach is that if a community, however poor, is adequately motivated, organized, mobilized, educated and provided basic logistic and technical support, it can make rich contributions not only towards meeting its own basic requirements but towards overall national development. The Green Revolution was in one sense a major food-based approach.


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Table 11. Food-based approach and home gardening 1

2 3 4 5

6

7 8

9

10

11 12 13 14 15

16 17 18

Bloem MW, Huq N, Gorstein J et al: Does the production of dark green leafy vegetables and fruits play a role in the etiology of maternal night blindness and malnutrition; in George SM, Sister DG, Latham MC, Benjamin TP (eds): Home gardening: Experiences from South India. In two decades of progress: Linking knowledge of action. XVI IVACG Report, 1994, p 76. Immink MOC, Sanjur D, Colon M: Home gardens and the energy and nutrient intakes of women and preschoolers in rural Puerto Rico. Ecol Food Nutr 1991;11:191–199. Mansour M, Mudehwa R, Adamou D, Mamman ML: Piloting diet diversification through home gardens: The Niger experience. XVIth IVACG Report, 1994, p 76. Marek T, Brun T, Reynaud J: Do home garden projects improve income and nutritional status? A case study in Senegal. Food Nutr Bull 1990;12:20–25. Ngu T, Quang ND, Nguyen Ha P, Tu Giay: A food-based approach to nutrition improvement and household food security in Vietnam, with special reference to vitamin A deficiency. XVIth IVACG Report, 1994, pp 1–77. Piedrasanta B, Alvarey E, Brown J: Promotion of vitamin A rich food sources through an integrated IEC programme. Virtual elimination of vitamin A deficiency: Obstacles and solutions for the year 2000. XVIIth IVACG Report, 1996, pp 1–96. Pollard R: The West Sumatra Vitamin A Social Marketing Project. DOH, Indonesia and HKI Report, 1989. Shanker AV, Gittetsoln J, Pradhan EK, Dhungel C, West KP Jr: Home gardening and access to animals in households with xerophthalmic children in rural Nepal. Food Nutr Bull 1998;19:34–41. Smitasiris S, Attig GA, Valyasevi A, Dhanamitta S, Tontisirin K et al: Social marketing vitamin A rich foods in Thailand: A model nutrition communication for behaviour change process. UNICEF/INMU Publication, Thailand 1993. Talukder A, Kiess L, Huq N, de Pee S, Darnton-Hill D, Bloem MW: Increasing production of vitamin A rich fruits and vegetables: Lessons learned in taking the Bangladesh homestead gardening programme to a national scale. Food Nutr Bull 2000;21:165–172. Vijayaraghavan K, Uma Nayak M, Bamji MS, Ramana GNV, Reddy V: Home gardening for combating vitamin A deficiency in rural India. Food Nutr Bull 1997;18:337–343. Vuong LT: Underutilised ␤-carotene-rich food crops of Vietnam. Food Nutr Bull 2000;21:173–181. Wadhwa A, Singh A, Mittal A, Sharma S: Dietary intervention to control vitamin A deficiency in seven- to twelve-year-old children. Food Nutr Bull 1994;15:53–56. Yusuf HKM, Islam N: Improvement of night blindness situation in children through simple nutrition education intervention with the parents. Ecol Food Nutr 1994;31:247–256. Attig GA, Smitasiri S, Ittikom K, Dhanamitta S: Promoting home gardening to control vitamin A deficiency in North-Eastern Thailand. Food, Nutrition and Agriculture, FAO 1993;7:18–25. Underwood BA: Dietary approaches to the control of vitamin A deficiency: An introduction and overview. Food Nutr Bull 2000;21:117–123. Smitasiri S: Engaging communities in a sustainable dietary approach: A Thai perspective. Food Nutr Bull 2000;21:149–156. Wasantwisut E, Chitchang U, Sinawat S: Moving a health system from a medical towards a dietary approach in Thailand. Food Nutr Bull 2000;21:157–160.

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Operated wisely, a food-based program could bring about a qualitative improvement in the community – not just restricted to improvement of its health/nutrition status alone but also of its overall productivity and creativity. India’s Milk Revolution A shining example of such successful community effort towards augmentation of the production and consumption of a major nutritious food item is India’s Milk Revolution, ably pioneered by Dr. Kurien. India’s total milk production, which was just 16 million tons in 1950, rose to 75 million tons in 1999. From being a major importer of dairy products in 1950, India has now emerged as the largest milk producer and exporter in the world! As against a per capita availability of 132 g/day in 1950, the present per capita availability is almost 214 g/day – that in spite of the enormous increase in the population in the last 50 years. Milk consumption in many households has increased. The true ‘heroes’ of this remarkable transformation were the poor cattle and buffalo owners in rural India who were successfully welded into an efficient cooperative movement. This success was achieved despite a national cattle herd of poor yielders, poor fodder and lack of adequate marketing support, and almost 98% of the overall production was in the rural sector. With improved cattle breeds and with better marketing facilities it should be possible to further enhance milk and dairy production in the next few years [101]. What has been achieved with milk, can be achieved with horticultural products as well, through efficient organization and support to rural communities. The Thai Experience The Thai experience is contained in some of the reports referred to in table 11. An imaginative project designed to increase consumption of provitaminA-rich foods in Northeast Thailand had yielded demonstrable positive results [102]. This project focussed on a locally grown vegetable – ivy gourd – rich in vitamin A, which the people could themselves cultivate. The promotion of production and consumption of this food in the habitual family diet was undertaken as part of a project for promotion of family health by ‘loving and caring’ mothers [103]. This was thus an integrated project of production, consumption and nutrition education of a community – an exercise in self-help, self-reliance and community development. The Institute of Nutrition, Mahidol, Bangkok, which pioneered this project had made it clear that it chose ivy gourd ‘as representing other GLVs’, and as being the most readily available source in that part of Thailand. There have been several other such comprehensive Nutrition Communication Programs in Thailand [104–106] advocating a multidimensional approach towards


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community development and nutrition improvement of population groups, which should serve as heartening examples to other developing countries. The Indian Experience Major efforts in India towards increasing horticulture production and the production of other micronutrient-rich foods and correcting the earlier mistakes of the Green Revolution which had largely neglected these foods have already been referred to. In addition, a major countrywide effort at identifying carotenerich foods for combating vitamin A deficiency had been recently carried out in India [107]. This program covered five different regions of the country and in different seasons in order to elucidate the regional and seasonal availability of such foods. A wide variety of carotene-rich foods were identified. These included several ‘uncommon’ foods cultivated locally for consumption by tribal and rural populations. The ␤-carotene content of these unfamiliar foods (not ‘unfamiliar’ to the rural populations of the area) was determined in two major laboratories in India, and some of these were found to be good sources of carotene. Thus for instance, the kanjero leaves consumed by tribal communities of Gujrat were found to contain 10,695 ␮g of carotene/100 g of leaves. The study also showed that a wide variety of ␤-carotene-rich foods were at present not being optimally used. Regional and seasonal calendars of common and inexpensive micronutrientrich foods available in different regions of the country and in different seasons – winter, summer and monsoons – and the quantities of these foods necessary to meet the ␤-carotene requirement of pre-school children, pregnant women and lactating mothers, are now available. This information must prove valuable in programs of nutrition education designed to propagate ways in which locally available carotene and micronutrient-rich foods can be incorporated in the habitual diets of the family. Efforts in Other Developing Countries Other examples of successful community-based projects in different developing countries are cited in table 11. Some of these efforts have been ably reviewed by Dr. Robin Marsh [108] in the paper on ‘Household horticulture and family nutrition programmes’. The VAC Project in Vietnam [109] (VAC being an acronym for garden (V), food (A) and cattle-feed (C)) is a successful integrated program of local food production, home gardening (vegetables, beans, roots, tubers and fruit), animal husbandry and fisheries. The program also includes health/nutrition program activities combined to create a harmonized integrated system all managed by the community itself.

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In the Puralia Project in West Bengal [110], through the active participation of local volunteers, women and youth working under the village panchayats, increased local production and consumption of carotene-rich foods, vegetables and fruits, as well as increased nutrition knowledge and awareness in the part of the community was substantially increased demonstrating truly that through local efforts and utilizing local natural food resources the problem could be combated. The Pekarangan Development Programme in Indonesia, the HK1 Bangladesh Home Gardening and Nutrition Education Programme [111], and the Home Gardening Programme in Andhra Pradesh by Vijayaraghavan [112] of the National Institute of Nutrition are other striking examples. Home Gardening In most of the above-mentioned programs, home gardening has found an important place. Home-gardening programs should not be allowed to become short-term demonstration projects. There is a very real danger of this happening. In order to sustain the enthusiasm and continued interest of the community, the programs must be economically viable. India’s Dairy Development Project achieved sustainability and durability through the fact that it was not a disjointed compartmentalized series of operations, and that it was economically viable. The farmers had been welded together into a powerful Co-operative Movement and were extended infrastructural and marketing support. If this had not been done the program could have withered away. It will be good strategy to bring isolated home-gardening programs in each developing country under the umbrella of a central ‘National Horticultural Development Board’ on the lines of India’s ‘National Dairy Development Board’. Such a Horticultural Development Board could weld disjointed home-gardening projects into a National Co-operative Movement and will be able to provide marketing and technical (supply of seeds and agricultural extension services) support. The programs should not be allowed to degenerate into isolated/disjointed exercises. In order to be economically viable and durable, the home-gardening approach must be part of a conscious and determined policy by national governments to promote the production, improvement of nutritive value and the consumption of fruits and vegetables. This implies that the programs must go hand in hand with intensive programs of nutrition education, and with research efforts designed to update information on the micronutrient content of foods to develop varieties with high micronutrient content, and to identify innovative ways of incorporating GLVs in weaning diets in forms in which they will be acceptable and consumed in adequate quantities. The home-gardening programs must be ably supported by parallel efforts towards setting up of village/small town-based industries for preservation and


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storage of vegetables and fruits and for prevention of post-harvest losses. These village-based processing and preservation industries could become important income-generating programs, which could provide employment and incomegenerating opportunities to local households. The program could greatly help in preventing current post-harvest losses of fruits and vegetables and in improved methods of preservation. With respect to preservation, recent studies show that frozen vegetables could be as nutritious as fresh ones [113]. Freezing surplus vegetables at village/small town level could greatly add to the commercial viability of the production of these foods. In all supplementary feeding programs in schools, and other institutions (including national programs like the Integrated Child Development Services in India); vegetables and fruits must find an important place in the diets. Right now, the emphasis in these feeding programs is all on calories and protein and not on micronutrient-rich foods. Assured intake of fruits and vegetables generated in home gardens would be facilitated with this approach and the feeding programs, themselves, instead of being looked upon as ‘charity operations’ as of present will become part of community effort. This will be a far better and a more scientific approach than the proposal for spraying or sprinkling a synthetic micronutrient mix on the food. Home-gardening programs, in the comprehensive sense, must aim at augmenting production and consumption of not only vegetables and fruits but also of poultry, fisheries, and of cattle and buffalo milk production where facilities exist. All this should be viewed as a part of a grand strategy of converting nutrition improvement into a ‘people’s movement’. If home gardening becomes part of such an integrated effort then the results would be truly rewarding. Factors Retarding and Distorting Food-Based Approaches There are currently powerful, well-funded global commercial interests, which while, outwardly paying lip service to food-based approaches in developing countries, would appear to be not truly supportive of these efforts. Instead some of the magic bullets and pharmaceutical solutions that are currently being pushed for the prevention of undernutrition and promotion of nutritional well-being of people of developing countries, are such as, to inhibit, retard and distort, national food-based approaches in many subtle ways. Their actual benefit with respect to improving the nutritional status of populations through such supplements has not been scientifically assessed and proven. On the other hand, the pharmaceutical industry’s contribution to the conquest of disease in recent years has been truly remarkable, and there is a legitimate place for pharmaceutical solutions in the treatment of diseases. In an enlightened national health/nutrition policy, there can be no legitimate room for any conflict between pharmaceutical interests on the one hand and food-based

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approaches on the other. The fair name of the pharmaceutical industry should not be allowed to be sullied by unethical and unscientific adventures. Lessons from History Lessons from history, drawn from the changing epidemiology of malnutrition in different developing countries, carry far greater importance and relevance, than the results of ‘experimental trials’ frequently being reported. Let us now examine the lessons which history has to offer. It will be remembered that several countries of Asia (and indeed of Africa) were under colonial rule for over two centuries and had attained their political independence barely 50 years ago. During the long colonial era, South Asia used to be visited by large-scale famines, once every 7 years and this had decimated large sections of its populations. In the Bengal famine in India, at the end of colonial rule for instance, the total fatalities suffered by India exceeded those suffered by all the allies put together during the entire period of World War II. Today, large-scale famines have been largely eliminated in most parts of Asia. Countries of South Asia, under the circumstances, had started on their developmental journeys, as it were, barely 50 years ago. During these 50 years, their policies with respect to nutritional improvement were almost entirely food-based. It is important for our present purpose to examine the effect of these food-based policies on the national nutrition scene. At the time of its political Independence, India was a veritable museum of the most florid nutritional deficiency diseases. Frank clinical malnutrition, beriberi, pellagra and keratomalacia were among India’s major public health nutrition problem. During the last 50 years, there have been striking changes in the epidemiology of these major nutritional deficiency disorders. Thus, beriberi (cardiac and dry) which was rampant and accounted for considerable mortality and morbidity in parts of Asia till the mid-1960s has now practically disappeared. Pellagra, which was endemic and widespread in parts of India, has also ceased to be a public health problem. Keratomalacia, often seen in association with kwashiorkor which used to affect millions of children in Asia, has practically disappeared; only minor forms of vitamin A deficiency in the form of Bitot’s spots are now being encountered as a public health problem and that too in some pockets of poverty and poor communities. The manner in which these three major diseases – which are important manifestations of deficiency of important micronutrients – have disappeared, hold important lessons as to the practical strategies for the control of micronutrient malnutrition. The Conquest of Beriberi This was brought about not through the distribution of thiamin tablets. In fact an attempt at thiamin supplementation for the control of the disease in the


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Philippines had failed, and had to be withdrawn. In India, beriberi was rampant on the eastern sea coast of India – the present Andhra Pradesh stretching from Calcutta in the north to Madras (Chennai) in the south. Indeed, peripheral neuritis was the major clinical and health problem of this region for decades preceding India’s independence in 1947. The staple diet of this region was highly polished rice. In the wake of World War II the government imposed a regulation prohibiting excessive milling and polishing of rice, not so much with a view to control beriberi, but in order to prevent wastage of scarce food grains, during the difficult war years. The disappearance of beriberi and peripheral neuritis followed, because with the restriction of milling, thiamin losses from whole rice grain incurred in excessive milling was restricted and thiamin content of diets increased. The conquest of beriberi was thus achieved solely by a food-based approach consisting of the consumption of nutrients naturally present in rice and not through supplementation of synthetic thiamin tablets. The Disappearance of Pellagra The disappearance of pellagra as a public health problem was also achieved not through the distribution of niacin tablets to the public but through a food-based approach. It must however be conceded that this food-based strategy was not the result of deliberate planning but a spin-off effect of the Green Revolution. In the pellagra endemic areas, the staple was jowar (sorghum), which though not poor in tryptophan like maize, is rich in leucine that could bring about significant changes in key enzymes in the tryptophan – niacin pathway resulting in the inhibition of nicotinamide – nucleotide formation from dietary protein leading to conditioned deficiency of nicotinic acid. In the wake of the Green Revolution, the emphasis being solely on wheat and rice cultivation, with relative neglect of millets, the per capita availability of jowar had declined and the striking difference in the price of rice and jowar which prevailed in the 1950s and 1960s had practically disappeared. Rice, being the staple enjoying much greater social prestige than jowar, as well as being more easily available at an affordable cost, has caused jowar consumption to decline. This fortuitous change in the dietary pattern generated by the Green Revolution resulted in the disappearance of a major disease, which was prevalent in the region for several decades [114]. The Disappearance of Keratomalacia Keratomalacia was rampant in the southern and eastern parts of India, and it used to be common to see at least 4–6 cases daily, of frank keratomalacia in the outpatient departments of the pediatric and ophthalmic wards of hospitals in eastern and southern India. Keratomalacia was often seen in association with classical kwashiorkor, which was also widespread in this region. These diseases

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have now been totally eliminated. This was again achieved, in the case of kwashiorkor, not through the distribution of fish protein concentrates, and in the case of keratomalacia not through the massive vitamin A prophylaxis program. The massive vitamin A dose prophylaxis program was initiated for the first time by the NIN in India nearly 30 years ago – a fact that is hardly mentioned in the plethora of publications on massive dose vitamin A programs (mercifully indeed)! This program was attempted in nine states of the Indian union and was found to be a failure on the public health scale. Indeed the disappearance of keratomalacia was brought about through the amelioration of abject poverty; through improvement in basic healthcare and food-based approaches and not through synthetic vitamin A supplementation, which was very poorly implemented in several states. The limitations of the massive vitamin A dose prophylaxis have been discussed earlier in this chapter. Experience in Developed Countries Even in developed countries, vast changes in dietary practices have been brought about in the last few decades. The return to breast-feeding within a decade; the recognition of the deleterious effects of high saturated fat and high animal protein diet and the concurrent changes in dietary habits, and the recognition of the importance of fruits and vegetables are all part of sensible foodbased approaches being promoted in the developed countries. The rise in incidence of heart diseases has been halted. Cereals, once denigrated as ‘bulk food’ and ‘roughage’, are now finding increasing respectability as sources of fiber, beneficial in bringing about a desirable serum lipid profile and protection against cancers of the colon. Probiotics and fermented foods are being increasingly recognized as ‘functional foods’ capable of augmenting gut mediated immunity. These are benefits that can be offered only through foods and not through synthetic supplements. These are examples of successful application of the food-based approaches in developed countries. The verdict of history is thus clear! Indeed, except for iodine deficiency disorders and to some extent iron deficiency anemia, there is no proven record till date, of any major public health nutrition problem (including vitamin A deficiency) having been eliminated by synthetic micronutrient supplementation. On the other hand, we have rich evidence of near total elimination of florid nutritional deficiency disorders (including micronutrient deficiencies) through food-based approaches consisting of dietary modification and improvement. These historical experiences have two important lessons: (i) that major micronutrient problems can indeed be solved through a food-based approach without recourse to arbitrary concoctions synthetic supplements, and (ii) that even poor populations in developing countries are willing to accept change and to use modern scientific methods to improve their diets and lifestyles.


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We are now on the threshold of great scientific advances, which could further enhance the efficacy of food-based approaches. The times are, thus, extremely propitious for intensification of food-based programs.

Strategies for Control of Micronutrient Malnutrition

In combating micronutrient malnutrition in a community, it is important to take the total context into account. This point could be exemplified with the results of the latest studies carried out by the National Nutrition Monitoring Bureau (NNMB) in India [115]. The NNMB studies, which largely pertain to the poor sections of India’s population, showed that populations with deficient intake of vitamin A or riboflavin also showed significant deficit in energy intake. If the intakes of other nutrients were also looked for, the results would have been probably similar. This is a picture to be expected in all deprived communities. Incidentally, the NNMB studies like the studies of several other groups show a lack of concordance between estimated intakes of nutrients through the oral questionnaire diet surveys on the one hand, and the actual clinical manifestation of the diseases related to their deficiencies, on the other. The actual prevalence of clinical deficiency was far far less than what the dietary data had indicated. This highlights the practical problems in the assessment of the nutritional adequacy of diets. On the basis of available data, it can be concluded that what the poor communities need is more ‘FOOD’ – not pills, tablets or sprays. When overall food intake becomes adequate enough to provide basic energy needs, needs of other nutrients would be met to a considerable extent even with the current diets. However, diets of the poor will still need considerable improvement in quality, and this can be achieved through dietary diversification resulting in the increase of such food items like GLVs and milk – intake of which, currently, is extremely low. It is only when, and after, the basic energy needs of populations are met, that improvement in the quality of the diet can be brought about because obviously it is the energy needs that comes first. It has been shown that as the socio-economic status improves, the intake of cereal foods decreases and other ‘quality’ foods find place in the dietaries. The right approach to combat micronutrient malnutrition in the community will be to remove the social and economic constraints, which currently prevent poor communities from having access to even these basic food items necessary to meet their energy needs. The answer to this does not lie in the distribution of tablets, pills or sprays containing a concoction of a few micronutrients at arbitrary levels. This will be somewhat like the cruel experience in the Bengal famine referred to earlier. Even at the height of the ‘protein controversy’,

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we had pointed out that a good part of the prevailing protein deficiency was incidental to the overall calorie deficiency (inadequate food), and that if even habitual diets could be taken in quantities adequate to fulfil the caloric needs, protein needs will be largely met, and that therefore what the population needed was more food and not special ‘fish-protein concentrates’, in the continuing control of calorie shortage. Policy-makers of developing countries should not be distracted from the inescapable duty of overcoming poverty and providing access to basic foods to their people. The resources available to poor countries for health, nutrition and welfare are far too meager to be siphoned away by quests for magic bullets and short cuts. Strategies The considerations discussed in the previous chapters should provide us some leads for deciding on the appropriate strategy for combating micronutrient malnutrition. For this purpose, we may broadly recognize three major approaches, which flow out of earlier discussions. (1) The Food-Based Approach This is based on the view that the eradication of undernutrition must be a part of overall development of the community which will include the improvement of habitual diets in its households, and making optimal use of locally available foods so as to ensure that the basic nutrient requirement (including micronutrient requirements) are adequately met. This approach, in a broad sense, also implies that the community will be enabled and educated to make the right choice of foods within their economic and geographic reach, at their own doorsteps, and to ensure equitable intra-familial distribution of the food so available to the household so that infants, children and women get an adequate share of the family pot. It is also recognized that this approach, while being community- and household-oriented, must necessarily go hand in hand with: (i) national agricultural policies designed to correct current imbalances and deficits with respect to production and availability of micronutrient-rich foods, (ii) policies designed to improve the provision of basic healthcare and environmental sanitation, and (iii) most importantly, with efforts at combating poverty among the lowest income groups through poverty alleviation and employment/income generation programs. The basic approach here is that the community must be helped to help itself, and the present constraints in the way of achieving this objective must be addressed and removed. The food-based approach is thus very much a part of a policy of national development, and aims at selfreliance, self-help and self-esteem among the people and at achieving overall


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improvement of the quality of the household diets through the optimal use of local foods. (2) An Extended Synthetic Nutrient Supplementation Approach This is an approach which, while recognizing that the food-based strategy described in (1) above may be the right ‘long-term’ objective, believes that this may not be attainable, and may be too ‘time consuming’, and that therefore appropriate synthetic nutrients (singly or in combination), may be made available to the poor, not just for specific problems like iodine deficiency and iron deficiency disorders, but for micronutrient deficiencies in general (multiple micronutrient supplements). Since the poor are hardly likely to expend their meager resources on pills, tablets or sprays, which would hardly satisfy their hunger, the implication here is that these synthetic nutrients will be procured by the governments of developing countries from external sources (since these supplements are hardly manufactured within developing countries themselves) and distributed as a welfare operation to poor communities. Unlike (1) above, this is an approach which views micronutrient malnutrition (not so much as an attribute of ‘underdevelopment’) but as a specific ‘disease’ to be prevented and controlled by a specific (isolated) solution. The difference between the foodbased approach and the synthetic supplement-based approach is somewhat like the difference between teaching a man to catch the fish that he needs from his own local pond, on the one hand, or giving him instead (not a fish but) a ‘fish substitute’ as a dole. The former is ‘time consuming’ while the latter may be ‘immediate’, but the ‘beneficiary’ will have to be probably dependent on the substitutes, even assuming that the ‘substitute’ is in fact as good as food itself. It is also presumed that this short-term solution, despite siphoning off scarce manpower and institutional resources involved in the procurement and distribution of the ‘instant remedy’, from out of the meager overall resources available to the country, will in no way inhibit or retard the long-term approach of dietary improvement. This is an approach that is clearly unacceptable. (3) A Food-Based Approach Supported by Limited Use of Synthetic Nutrients as Adjuncts, Where Absolutely Necessary This is an approach which while recognizing the essentiality and durability of (1) above, recognizes that limited use of some synthetic nutrient and supplements may be necessary as adjuncts to (1) above, for the reason that an entirely food-based approach even if implemented effectively, may not be able to adequately address some micronutrient deficiencies, totally or adequately. The examples of iodine deficiency (and to some extent) of iron deficiency have been mentioned in this connection.

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It should be clear from the foregoing discussion that the third approach is perhaps the most desirable and feasible one. Comparative Cost-Benefit Analysis of Food-Based and ‘Synthetic-Vitamin Supplementation’Approach There have been quite a few cost-benefit analyses exercises seeking to compare the efficacy of the ‘supplementation approach’ with the food-based approach, and coming out in favor of the former. With due respect to the scientists involved, these exercises must be considered as far too simplistic and superficial and as ignoring the ground realities, and as failing to take note of the total picture. In these exercises, the ‘cost’ of the supplement has been grossly underestimated while the ‘benefits’ are assumed and grossly overestimated. In the first place the validity of comparisons of cost effectiveness of these two approaches can itself be questioned, because these approaches are really not comparable. The supplementation approach, as pointed out earlier, seeks to provide a specific vertical pharmaceutical solution to a single isolated nutritional deficiency virtually ignoring the related problem of undernutrition. The ‘benefit’ or efficiency of this approach in the presence of other nutritional deficiencies is very much open to doubt. The supplementation approach assumes that poverty and undernutrition in poor communities in developing countries are unlikely to be overcome and that therefore these communities will need supplements to be doled out to them regularly. Though claiming to be a ‘shortterm’ solution, it is in fact a ‘short-sighted’ one, since it fails to see the ultimate goal however seemingly distant. On the other hand, the food-based approach is a more comprehensive one which seeks to address the problem of the specific micronutrient deficiency in question, as part of the problem of the general undernutrition and underdevelopment. The food-based approach is part of a nation-building effort, not limited to the specific context of just one nutritional deficiency. Comparisons of the cost effectiveness of these two totally different approaches, driven by totally different interests and perceptions are thus inappropriate. It is argued that a specific supplement may be expected to control a given micronutrient deficiency, perhaps more rapidly than a laborious process of dietary improvement. But the real cost of supplementation to the community far exceeds the cost of the supplement itself, a fact often ignored in the costbenefit exercises. To the labeled cost of the supplement, must be added: (i) the cost of storage under proper conditions (not always easy in hot and humid climate, especially with respect to synthetic nutrients with a short shelf-life); (ii) cost of transportation to the target sites; (iii) identification and mobilization of the target population; (iv) cost of distribution, which is generally undertaken by medical/paramedical personnel and welfare workers who are also currently


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charged with a multiplicity of other functions (the effect of this additional charge on the normal duties of these functionaries has to be taken into account also), and (v) ensuring compliance on the part of the target population once reached (this is not always easy). (A free dole offered commands little respect in the community.) Experience with many supplementation operations in developing countries (including the massive vitamin A dose prophylaxis) reveal that quite often less than 40% of the supplements actually reach the intended beneficiary. As for ‘benefits’ of the supplementation approach, apart from iodine and iron supplements, benefits accruing to a community through the supplementation of other micronutrients have not been conclusively demonstrated in any public health program. The success of supplementation operations is usually being measured by the quantity of micronutrients supplied and not on the basis of the effect of these on the population. For example, to this day, there has been no attempt through carefully conducted studies, to find out if the spraying of multiple micronutrients or food supplements being offered to poor children in India, provides any added benefit over and above food supplements given without the spray! On the other hand, the ‘benefits’ of a food-based approach are not restricted to the correction of a single nutrient deficiency. The spin-off benefits to the community of a comprehensive food-based approach can be substantial, and such as to bring about an improvement not only in their household diets, but on the overall quality of the human resources. Food-based approaches can lead to job creation and income generation, to the amelioration of poverty and to more informed community participation in developmental progress. What is the ‘cost’ to a community or nation of perpetual reliance on synthetic supplements to food to ensure the health and nutrition of its people? What is the ‘benefit’ to a nation of achieving health/nutrition of its people through locally available foods? What is the ‘cost’ of perpetual dependency? What is the ‘benefit’ of self-reliance, self-help? A cost-benefit analysis should not ignore these basic issues. Research Needs In order to facilitate and promote a food-based approach towards the prevention of micronutrient malnutrition in developing countries, there is a crying need for intensive research. A detailed discussion of these research needs is not being attempted here; only the broad areas that require to be addressed are being indicated. Micronutrient Composition/Content of Foods, Which Form Part of Usual Household Diets in Developing Countries. The information that is currently available regarding the micronutrient composition/content of foods in developing

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countries is extremely meager. What is distressing is that even well-endowed laboratories seem uninterested in this area of research, which is apparently being considered pedestrian. Data on micronutrient composition of food, currently available, need to be updated using modern analytical techniques. There is absolutely no information on the phytonutrient content of plant foods in common use. Enormous varietal and locational variations in the micronutrient composition of these foods may be expected. Any meaningful program for the promotion of a food-based approach must be based on such data. Indeed, far from being ‘pedestrian’, this area of research can be very productive and rewarding especially in the context of growing interest in the so-called ‘functional foods’. Effect of Processing and Cooking on Micronutrient Content. Micronutrients in foods are known to be lost in cooking and processing. The effort must be to identify ways by which such losses of micronutrients in processing can be minimized. New ways of processing micronutrient-rich foods into ready-to-eat foods need to be identified. Identification of New Micronutrient-Rich Plant Food Resources. Many plant foods rich in micronutrients which are currently not being used in diets are now being identified (e.g. purslane as a rich source of ␻–3 fatty acids). There is considerable scope of research in this area. Monitoring Genetic Engineering. There are currently global attempts at breeding micronutrients into staple food crops using conventional technology. There are also attempts at promoting GM foods. While the problem of ‘safety’ of the first category of foods may not pose problems, the same may not be the case with the latter category. Technical expertise is needed to monitor the safety and nutritional adequacy of these foods, and it is important that laboratories of developing countries are adequately equipped in this regard. Micronutrient Requirements and Interactions. The assumption that micronutrient requirements are identical in all situations, irrespective of staple diets and environmental factors, may be erroneous. As was pointed out earlier, a state of dynamic equilibrium between different micronutrients may be expected to exist in all diets conducive to optimal health/nutrition; the actual levels of different micronutrients needed to achieve that equilibrium may vary depending on the overall composition of the diet and its ingredients, because of synergistic and antagonistic interactions between nutrients. It is important to identify the optimal requirements of different micronutrients in different composite diets of healthy populations. Some examples of questions that need to be answered are: Is it safe to give massive dose of vitamin A to lactating women and young children, in situations when probably diets are low in calcium? What would be the effect of such massive doses on bone mineral metabolism in populations whose habitual intakes


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of calcium are low? This question becomes particularly important in view of reported moves in some circles to suggest a dose of 400,000 IU (instead of 200,000 IU) for lactating women! Are the current yardsticks we are using for assessing adequacy of different micronutrients valid or do they need revision? Do the micronutrient supplements which are now being added arbitrarily to foods being distributed to children confer any significant benefit? Unfortunately, current international and bilateral efforts at combating micronutrient malnutrition in developing countries seem to be directed largely at clinical trials consisting of the arbitrary distribution of a synthetic micronutrient or a concoction of micronutrients in the expectation that they may prove beneficial. It will be important to establish the scientific validity of supplementation and of its benefits under real-life conditions before launching public health programs on a large scale.

Concluding Comments

Developing countries should look to their farms not pharmacies, for the nutritional improvement of their people. Solutions to the problem of undernutrition (including micronutrient malnutrition) must be predominantly ‘foodbased’ – not ‘drug-based’. The prevalence of poverty can be no justification for jettisoning a foodbased approach in favor of an approach based on supplements. ‘Supplements’ cannot solve poverty; they can only help to keep the poor in perpetual dependence on doles. Poverty has to be frontally addressed and overcome as part of the process of national development. This inescapable duty cannot be bypassed by short cuts and magic bullets. Considerable scope exists for intensification of production and consumption of micronutrient-rich foods. Dietary diversification and improvement of overall nutritive quality of diets in households in developing countries is possible as history, and present experiences, have shown. Limited use of key supplements like iodine or (in certain cases) iron may be adopted as an adjunct to a food-based approach. But extended use of synthetic micronutrients (in arbitrary combinations) as a blunderbuss polypharmacy approach would be no more than commercial exploitation of third world malnutrition and cannot be scientifically or ethically justified. Programs for genetic improvement of foods including genetic modification of foods can play an important role in efforts designed to improve the health/nutrition of mankind. The safety of GM foods will need to be clearly established before they are accepted for general consumption.

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National agencies should resist the soft option of resorting to synthetic ‘supplements’ in order to escape their responsibilities for bringing about an improvement in health/nutrition of their people through improvement of diets in households. International agencies, which are the custodians of health/ nutrition of mankind, should assist and help developing countries to implement food-based programs for the improvement of the nutritional status of their people as part of their national development program.

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74 75

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78

79 80 81 82 83

84 85 86

87 88 89 90 91 92 93

94

95 96

97 98 99

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C. Gopalan Nutrition Foundation of India, C-13, Qutub Institutional Area, New Delhi 16 (India) E-Mail [email protected]


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Author Index

Gopalan, C. 76

Nambiar, V.S. 41

Viriyapanich, T. 60

Johnson, P.D. 67

Seshadri, S. 41 Simopoulos, A.P. 1, 22

Wasantwisut, E. 60

Kallithraka, S. 1, 22 Kypriotakis, Z. 22

Zeghichi, S. 1, 22 Tamber, B. 76

132

Subject Index

Acerola agricultural potential 72, 73 distribution and origin 68, 69 fresh and processed uses of fruit 73, 74 fruit nutrients ascorbic acid 67, 69, 73, 74 developmental effects 70, 71 fatty acids 71 juice proximate analysis 73 minerals 69, 70 storage and handling effects 71 vitamins 69, 70 general features 67, 68 low-density lipoprotein oxidation prevention 69, 70 taxonomy 67 Amaranth ␤-carotene content 63 fatty acid content 13 Amaranthus viridis, see Amaranth Antioxidants, see also specific antioxidants activity assay in plants 6, 7, 15, 16 benefits of dietary intake 1, 2, 79, 80 diet of Crete plants, activity assay 29, 30, 34, 36 free radicals in disease 33, 34 molokhia 15, 16 stamnagathi 15, 16 types 2, 79 Ascorbic acid acerola 67, 69, 73, 74 drumstick leaves 48, 49

kanjero leaves 48, 49 molokhia 5, 7–9 stamnagathi 5, 7–9 Bengal, food-based approach for dietary improvement 115 Beriberi, conquest using food-based approach 117, 118 Beta maritime, see Wild beet Biotechnology, micronutrient production in plants 89, 90 ␤-Carotene bioavailability from plants 96–99 drumstick leaves 47, 48, 56 kanjero leaves 47, 48, 56 leaf curd content vs leaves 96 leaf protein concentrate 96 molokhia 6, 9 red palm oil 95 sources 93, 94 spirulina 94, 95 stamnagathi 6, 9 supplementation 81 varietal differences in plant content 92, 93 Carotenoids, bioavailability from plants 99 Cereals, reliance of developing countries 87 Chayote, ␤-carotene content 63 Chenopodium album L., see Goosefoot

133

Cichorium spinosum, see Stamnagathi Coccinia species, see Ivy gourd Common mallow, fatty acid content 13 Corchorus olitorius, see Molokhia Diet of Crete composition 22 health benefits 18, 22, 23, 37 plant analysis antioxidant activity assay 29, 30, 34, 36 minerals 30–32 nitrates 32, 33 phenols 28, 29 plant types 23–26 ␣-tocopherol 27, 28 Digera arvensis, see Kanjero Drumstick agricultural potential 56, 57 consumption and medicinal uses 46, 47 dehydration of leaves and nutrient retention 52–56 distribution 41, 43, 44 morphology 42 nutrient composition of leaves ascorbic acid 48, 49 ␤-carotene 47, 48, 56 minerals 49 oxalic acid 49, 50 phenols 50–52 organoleptic acceptability of leaves in local recipes 55, 56 supplementary feeding program potential 57, 58 Fatty acids acerola 71 cultivation effects on plant composition 36, 37 molokhia analysis 7 developmental changes 10–12, 14 ␻–3, benefits of dietary intake 2, 3 stamnagathi analysis 7 developmental changes 10–12, 14

Subject Index

Folic acid, supplementation 104, 105 Food-based approach, see Micronutrient deficiency Genetic engineering micronutrient production in plants 88, 89 safety and nutritional adequacy monitoring of foods 125, 126 Glutathione molokhia 6, 9, 10 stamnagathi 6, 9, 10 Goosefoot, fatty acid content 13 Green leafy vegetables consumption by Gujarat, India tribes 45, 46 nutritional benefits 44, 45 Harvesting, micronutrient loss prevention 90 Hedge mustard, fatty acid content 13 Home gardening, food-based approach for dietary improvement in developing countries 115, 116 India food-based approach for dietary improvement 114 horticultural crop production trends 87, 88 leaves consumed by Gujarat tribes 45, 46 micronutrient deficiency 83 milk revolution 113 National Nutrition Monitoring Bureau 120 plants, see Drumstick, Kanjero Iodine double fortification of salt with iron and iodine 103, 104 supplementation 101, 102 Iron, see also Minerals bioavailability from plants 97 double fortification of salt with iron and iodine 103, 104 supplementation 102, 103 Isoprenoids, beneficial effects in diet 80

134

Ivy gourd ␤-carotene content 62–64 distribution 61 food uses 62 general features 60 medicinal properties 61, 62, 65 species 60 vitamin A status improvement 64, 65 Kale, ␤-carotene content 63 Kanjero agricultural potential 56, 57 consumption and medicinal uses 46, 47 dehydration of leaves and nutrient retention 52–56 distribution 41–43 morphology 41, 42 nutrient composition of leaves ascorbic acid 48, 49 ␤-carotene 47, 48, 56 minerals 49 oxalic acid 49, 50 phenols 50–52 organoleptic acceptability of leaves in local recipes 55, 56 supplementary feeding program potential 57, 58 Keratomalacia disappearance using food-based approach 118, 119 management 108 Lactation, micronutrient requirements 125, 126 Leaf curd, ␤-carotene content vs leaves 96 Leaf protein concentrate, ␤-carotene content 96 Malpighia species, see Acerola Malva sylvestris L., see Common mallow Mango, varietal differences in ␤-carotene content 92 Mediterranean basin, plant species 1 Meta-analysis, mortality reduction claim 105 Micronutrient deficiency bioavailability from plants 96–100

Subject Index

culinary practices in prevention 95, 96, 125 developing countries 83, 84, 100 essential micronutrients 77, 82 food-based approach for dietary improvement barriers 116, 117 Bengal experience 115 cost-benefit analysis compared with synthetic supplements 123, 124 historical lessons beriberi conquest 117, 118 developed countries 119, 120 developing countries 117–119 keratomalacia disappearance 118, 119 pellagra disappearance 118 home gardening 115, 116 implementation 121, 122 India’s Milk Revolution 113 Indian experience 114 practicability 111–113 rationale 110, 111, 120, 121, 126 synthetic nutrients as adjuncts 122, 123 Thai experience 113, 114 Vietnam experience 114 food-food fortification 109, 110 fruit and vegetable recommended intake 80, 81 genetic engineering and biotechnology applications 88–90, 125 horticultural crop production trends 87, 88 inexpensive micronutrient-rich foods 90, 91 infection effects 85, 86 interdependence of intake requirements 84, 85, 125, 126 non-plant food sources 100 phytonutrients and beneficial effects 77–82 plant analysis prospects 91, 92, 124, 125 quality vs quantity of food 76 research needs 124–126 subclinical deficiency 82

135

Micronutrient deficiency (continued) synthetic supplement limitations 81, 82, 101, 108, 122, 127 varietal differences in micronutrient content 92, 93 Minerals acerola 69, 70 biological functions 3, 34 cultivation effects on plant composition 36 diet of Crete plants 30–32 drumstick leaves 49 kanjero leaves 49 molokhia 7, 14, 15 stamnagathi 7, 14, 15 Molokhia advantages as food source 17 antioxidant analysis activity assay 6, 7, 15, 16 ascorbic acid 5, 7–9 ␤-carotene 6, 9 developmental changes 14 glutathione 6, 9, 10 phenols 6, 10 ␣-tocopherol 6, 9 fatty acids analysis 7 developmental changes 10–12, 14 growth for analysis 5 medicinal uses 3 mineral content 14, 15 mineral determination 7 protein analysis 7, 16, 17 taxonomy 3 Moringa oleifera, see Drumstick Multivitamin supplements, pregnancy 109 Night blindness, nutritional deficiencies 82 Nitrates, diet of Crete plants 32, 33 Oxalic acid drumstick leaves 49, 50 kanjero leaves 49, 50 Papaya, varietal differences in ␤-carotene content 93

Subject Index

Pellagra, disappearance using food-based approach 118 Phenols benefits of consumption 34 diet of Crete plants 28, 29 drumstick leaves 50–52 kanjero leaves 50–52 molokhia 6, 10 stamnagathi 6, 10 Phytochemicals benefits of intake 78–81 deficiency, see Micronutrient deficiency sources and functions in edible plants 34–36, 77–79 synergism of actions 81 Plant breeding, micronutrient production in plants 89, 90 Portulaca oleracea L., see Purslane Pregnancy, multivitamin supplements 109 Protein molokhia 7, 16, 17 stamnagathi 7, 16, 17 Pumpkin leaves, ␤-carotene content 63 Purslane fatty acid content 13 nutritional benefits 45 Red palm oil, ␤-carotene content 95 Salt double fortification of salt with iron and iodine 103, 104 iodine supplementation 101, 102 Sisymberium irio L., see Hedge mustard Sonchus oleraceus L., see Sow-thistle Sonchus tenerrimus, see Sow-thistle-of-thewall Sow-thistle, fatty acid content 13 Sow-thistle-of-the-wall, fatty acid content 13 Spirulina, ␤-carotene content 94, 95 Stamnagathi advantages as food source 17 antioxidant analysis activity assay 6, 7, 15, 16 ascorbic acid 5, 7–9

136

␤-carotene 6, 9 developmental changes 14 glutathione 6, 9, 10 phenols 6, 10 ␣-tocopherol 6, 9 distribution 4 fatty acids analysis 7 developmental changes 10–12, 14 growth for analysis 5 mineral determination 7, 14, 15 protein analysis 7, 16, 17 taxonomy 3 Swamp cabbage, ␤-carotene content 63 Sweet potato, ␤-carotene content 93 Thailand food-based approach for dietary improvement 113, 114 micronutrient deficiency 83 ␣-Tocopherol diet of Crete plants 27, 28

Subject Index

molokhia 6, 9 stamnagathi 6, 9 Verbena officinalis L., see Vervain Vervain, fatty acid content 13 Vietnam, food-based approach for dietary improvement 114 Vitamin A deficiency and keratomalacia management 108 ivy gourd improvement of deficiency 64, 65 massive dose prophylaxis efficacy 107, 108 supplementation and mortality reduction claim 105–107 synthetic supplement limitations 108 Vitamin C, see Ascorbic acid Vitamin E, supplementation benefits 34, 81 Wild beet, fatty acid content 13

137

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