JournalsNutritional importance of animal source foods

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Animal Source Foods to Improve Micronutrient Nutrition and Human Function in Developing Countries Nutritional Importance of Animal Source Foods1 Suzanne P Murphy*2 and Lindsay H Alleny *Cancer Research Center of Hawaii, University of Hawaii, Honolulu, HI 96813 and yDepartment of Nutrition, University of California, Davis, CA 95616 KEY WORDS:  animal source foods  schoolers  dietary quality  micronutrients Through choice or necessity, many people consume diets that contain few or no animal source foods (ASF)3 Both macronutrients and micronutrients may be present in suboptimal levels in primarily vegetarian diets (1–3); however, these diets are considered by many to be a healthy alternative to a more omnivorous diet that is high in saturated fat and cholesterol and low in fiber (4,5) Both lacto-ovo vegetarian and nonvegetarian diets can be nutritionally adequate, but considerable care must be taken with true vegan diets, which include no ASF This article will discuss the advantages of combining plant-based diets with ASF Findings from the Nutrition Collaborative Research Support Program The Nutrition Collaborative Research Support Program (NCRSP), conducted in the 1980s, identified a variety of micronutrients that were low in the diets of children in marginally malnourished regions of Kenya, Mexico and Egypt (6) In both Kenya and Mexico, the diets contained few animal products Although protein intake appeared to be adequate for almost all children, even after adjustment for protein quality, the intake of several micronutrients was clearly low Table shows the estimated prevalence of inadequate intake by young children for six nutrients of particular concern: iron, zinc, vitamin B-12, riboflavin, calcium and vitamin A Negative health outcomes are known to occur if intake of these nutrients is below requirements These problems include anemia, diminished work capacity, night blindness and poor growth, as a result of moderate inadequacies More severe problems can result from long-term low intake of these nutrients: rickets, impaired cognitive performance, blindness, neuromuscular deficits, psychiatric disorders and death Findings from the NCRSP also indicated that intake of ASF was associated with a higher quality diet (6) For example, animal source energy intake and animal source protein intake both were correlated positively with intakes of vitamin A, riboflavin and vitamin B-12 in all three countries, whereas animal source protein was a strong predictor of calcium intake Presented at the conference ‘‘Animal Source Foods and Nutrition in Developing Countries’’ held in Washington, D.C June 24–26, 2002 The conference was organized by the International Nutrition Program, UC Davis and was sponsored by Global Livestock-CRSP, UC Davis through USAID grant number PCE-G-00-98-00036-00 The supplement publication was supported by Food and Agriculture Organization, Land O’Lakes Inc., Heifer International, Pond Dynamics and Aquaculture-CRSP The proceedings of this conference are published as a supplement to The Journal of Nutrition Guest editors for this supplement publication were Montague Demment and Lindsay Allen To whom correspondence should be addressed E-mail: suzanne@crch hawaii.edu Abbreviations used: ASF, animal source foods; FGP, Food Guide Pyramid; HEI, Healthy Eating Index; NCRSP, Nutrition Collaborative Research Support Program 0022-3166/03 $3.00 Ó 2003 American Society for Nutritional Sciences 3932S Downloaded from jn.nutrition.org by on September 16, 2008 ABSTRACT Animal source foods can provide a variety of micronutrients that are difficult to obtain in adequate quantities from plant source foods alone In the 1980s, the Nutrition Collaborative Research Support Program identified six micronutrients that were particularly low in the primarily vegetarian diets of schoolchildren in rural Egypt, Kenya and Mexico: vitamin A, vitamin B-12, riboflavin, calcium, iron and zinc Negative health outcomes associated with inadequate intake of these nutrients include anemia, poor growth, rickets, impaired cognitive performance, blindness, neuromuscular deficits and eventually, death Animal source foods are particularly rich sources of all six of these nutrients, and relatively small amounts of these foods, added to a vegetarian diet, can substantially increase nutrient adequacy Snacks designed for Kenyan schoolchildren provided more nutrients when animal and plant foods were combined A snack that provided only 20% of a child’s energy requirement could provide 38% of the calcium, 83% of the vitamin B-12 and 82% of the riboflavin requirements if milk was included A similar snack that included ground beef rather than milk provided 86% of the zinc and 106% of the vitamin B-12 requirements, as well as 26% of the iron requirement Food guides usually recommend several daily servings from animal source food groups (dairy products and meat or meat alternatives) An index that estimates nutrient adequacy based on adherence to such food guide recommendations may provide a useful method of quickly evaluating dietary quality in both developing and developed countries J Nutr 133: 3932S–3935S, 2003 NUTRITIONAL IMPORTANCE OF ANIMAL SOURCE FOODS TABLE Prevalence (%) of inadequate intake by school-age children, NCRSP, 1984–19861 Nutrient Egypt Kenya Mexico Protein Vitamin A2 Vitamin B-12 Riboflavin Calcium Iron2 Zinc2 0.0 9.2 23.6 16.3 69.3 70.4 3.5 0.0 0.6 86.9 1.6 91.2 31.4 29.5 0.0 24.4 38.3 83.4 0.0 87.3 9.2 See reference 29 Using basal requirement estimates Nutrients in plant and animal source foods The nutrient levels in several plant and animal source foods are compared in Table Whether considered per unit of weight or per unit of energy, ASF tend to be richer sources of the six nutrients of concern Not only are these foods high in many micronutrients, but the nutrients often are more available Table shows that both iron and zinc are more bioavailable in animal foods In addition, the bioavailability of carotenoids as vitamin A precursors is now believed to be lower than indicated in traditional food composition tables (7) Thus, for diets that depend on plant sources of vitamin A, more fruits and vegetables are needed to meet requirements than was thought previously In the case of vitamin B-12, all requirements must be met from ASF, as there is virtually no vitamin B-12 in plant source foods Thus, ASF can fill multiple micronutrient gaps at a lower volume of intake than can plant source foods Just 100 g of cooked beef provides an entire day’s recommended intake of protein, vitamin B-12 and zinc and contributes substantially to meeting the riboflavin and iron recommendations Likewise, 100 g of milk also can provide substantial amounts of calcium, vitamin B-12, vitamin A and riboflavin Thus, small amounts of ASF added to a vegetarian diet can compensate for many of the vitamin and mineral inadequacies Furthermore, ASF provide multiple micronutrients simultaneously, which may be important in diets that are marginally lacking in more than one nutrient For example, vitamin A and riboflavin are needed for iron mobilization and hemoglobin synthesis, and iron supplements may not reduce the prevalence of anemia if intakes of these other nutrients are low (8) Thus, foods such as liver that contain substantial levels of both iron and preformed vitamin A may be more effective than single-nutrient supplements in alleviating poor micronutrient status ASF also tend to be sources of macronutrients that may not be desirable in the diet, such as saturated fat and cholesterol, although lean alternatives contain less of these macronutrients (Table 2) ASF also may be undesirably high in total fat, energy and protein For children in developing countries, a concentrated source of these macronutrients often is desirable, although for children (and adults) in more affluent countries, excessive consumption of energy-dense foods may lead to overconsumption of energy Although meat intake has been associated with an increased risk of colon cancer in several studies, processed meats appear to be stronger predictors than unprocessed meats (9) Particularly in developing countries, the contribution of meat to improved nutrient intake more than offsets this uncertain association with colon cancer (10,11) Studies of the effects of vegetarian diets on nutrient intake and status Dagnelie and colleagues have shown that Dutch infants consuming macrobiotic (strictly vegan) diets had poorer nutritional status and were more likely to have rickets and deficiencies of vitamin B-12 and iron (12,13) In Nepal, xeropthalmia in young children was less likely to occur if they had relatively high meat or fish intake when they were 13 to 24 TABLE Composition of selected foods (per 100 g) compared with requirements for a school-age child1 Nutrient Maize, cooked Kidney beans, cooked Kale, cooked Carrots, raw Milk, whole, unfortified Beef, medium fat, cooked Recommended intake2 Energy (kcal ) (kJ ) Protein (g) Vitamin A (mg RAE)3 Vitamin B-12 (mg) Riboflavin (mg) Calcium (mg) Available iron (mg) Available zinc (mg) Fat (g) Saturated fat (g) Cholesterol (mg) 119 497 2.7 0 0.07 0.12 0.12 1.2 0.2 127 531 8.7 0 0.06 28 0.15 0.11 0.5 0.1 32 134 1.9 370 0.07 72 0.14 0.02 0.4 0.1 45 188 1.1 971 0.06 31 0.06 0.14 0.2 0.0 51 213 3.3 55 0.39 0.16 119 0.01 0.18 3.9 2.4 14 269 1124 24.9 1.87 0.15 0.32 2.05 18 8.4 75 1600 6688 17.3 400 1.2 0.6 800 1.86 1.44 N/A N/A N/A Nutrient composition data from reference 30 Daily recommended intake for a 7-y-old child weighing 20 kg See references (7,31–35) Retinol equivalents were converted to retinol activity equivalents (RAE) in foods by reducing the vitamin A activity of provitamin A carotenoids by 50% (as recommended in reference 7) Downloaded from jn.nutrition.org by on September 16, 2008 in both Egypt and Kenya, but not in Mexico, where substantial calcium is supplied by tortillas prepared with lime In Kenya, it was possible to examine intakes of 49 toddlers who had at least d of intake recorded on days when no ASF were consumed and another d when some ASF were consumed On days when animal products were consumed (irrespective of the amount), intakes of riboflavin, vitamin B-12, calcium, phosphorus, fat and protein were significantly higher (6) 3933S SUPPLEMENT 3934S mo of age (14) U.S men consuming vegan diets had lower serum ferritin concentrations, and 10 of 25 vegans in the study had marginal deficits of vitamin B-12 (15) However, the vegan diets also tended to be lower in fat and higher in fiber, vitamin C, folate, magnesium, copper and manganese Recently, Hunt (16) summarized studies of the iron and zinc status of vegetarians and expressed concern about mineral status for those consuming plant-based diets The panel setting the new Dietary Reference Intakes for iron assumed 10% iron absorption for vegetarian diets versus 18% absorption for a mixed diet and thus suggested that the Recommended Dietary Allowance for iron should be 80% higher for vegetarians (7) It is commonly assumed that vitamin B-12 deficiency is unlikely if small amounts of ASF are consumed However, this is clearly not the case, as it is becoming clear that the prevalence of vitamin B-12 deficiency is very high in many poorer regions of the world, including Kenya (17), India (18), Guatemala (19) and Mexico (20) A number of studies now show the vitamin B-12 status of lacto-ovo vegetarians in industrialized countries to be considerably worse than that of omnivores (21, 22), presumably because of the lower amount of vitamin B-12 in milk than in meat Concern also has been expressed about the difficulty that children have in obtaining adequate energy and nutrient intake from bulky plant-based diets Recent recommendations from the World Health Organization on complementary feeding demonstrate that only ASF have the potential to provide enough calcium, iron and zinc for infants (23) than the vegetarian snack When averaged across the eight nutrients in Table 3, the milk and beef snacks provided more than twice as great a proportion of the recommendations Although a combination of both milk and meat plus githeri was not tested, it is clear from the data in Table that the overall proportion of the recommended intake provided would have increased even more Diets based on starchy staples other than maize (i.e., rice) would be improved equally by the addition of small amounts of ASF It also is interesting to note in Table that the snacks provided to the school-age children supplied only 20% of the children’s energy requirement, yet the milk and beef snacks supplied a substantially higher proportion of the recommendation for other nutrients compared to the vegetarian snack Using the information in Table 2, it is possible to design a diet that supplies the recommended intake of all eight nutrients using 400–500 mL of milk (to obtain sufficient calcium) and 300 g of cooked beef (to provide zinc and approximately half of the iron recommendation) The remaining at-risk nutrients would be obtained if a vegetarian dish similar to githeri were used to supply the remaining energy requirement The Food Guide Pyramid (FGP) for the U.S was developed to provide guidance to Americans on food choices that would provide a nutritionally adequate diet (24,25) It includes recommended amounts of meat or meat substitutes, and dairy products Development of a vegetarian alternative to the FGP has proved to be difficult, because few plant source foods can provide meaningful levels of nutrients such as calcium Furthermore, in a vegan diet with no animal products, a supplemental source of vitamin B-12 must be provided Although a vegetarian equivalent to the FGP has recently been proposed (26), it relies on fortified foods to obtain adequate intakes of vitamin D, vitamin B-12 and calcium Food guides for other countries usually include recommendations for both dairy and meat intakes (27) Thus, the FGP recommendation to consume 2–3 servings of dairy products (where cup of milk is a serving) and 5–7 ounces of lean meat or meat substitutes (where one-half cup of cooked dried beans, egg or one-third cup of nuts counts as ounce of meat) appears to be applicable to developing countries as well Designing an intervention to provide ASF We utilized information on the nutrient content of foods to design a snack to feed to school-age children in rural Kenya It was hypothesized that children who received a combination of githeri (a local stew of maize, beans and vegetables) and either milk or beef would consume a more nutritionally adequate diet overall than children who received the same amount of energy from githeri alone and thus would perform better on a variety of health and performance measures Table shows the composition of the three snacks expressed as a percentage of a schooler’s recommended intake As expected, the two snacks containing ASF supplied a higher proportion of most nutrients TABLE Percentage of a school-age child’s recommended nutrient intake supplied by three snacks Nutrient Recommended intake1 Githeri2 only (%) Githeri plus milk (%) Githeri plus beef (%) Energy Protein Vitamin A3 Vitamin B-12 Riboflavin Calcium Available iron4 Available zinc4 Average 1600 kcal 6688 kJ 17.3 g 400 RAE 1.2 mg 0.6 mg 800 mg 1.86 mg 1.44 mg N/A 20 62 53 25 11 12 23 20 73 70 83 82 38 12 48 20 124 17 106 27 26 86 51 Daily recommended intake for a 7-y-old child weighing 20 kg (7, 31–35) Githeri is a stew of maize and beans (in a ratio of 3:2 dry weight) plus small amounts of oil, onion, kale and salt Children in the ‘‘githeri only’’ group received 230 g of githeri; children in the ‘‘githeri plus milk’’ group received 100 g of githeri plus 250 mL of milk; children in the ‘‘githeri plus beef’’ group received 225 g of githeri containing 68 g of cooked minced beef Recipes reflect those in use in 1999 Retinol activity equivalents (RAE) for the snacks were converted from retinol equivalents as recommended in reference Iron and zinc availability were calculated assuming that the snack foods were not combined with any other foods Downloaded from jn.nutrition.org by on September 16, 2008 Food guides NUTRITIONAL IMPORTANCE OF ANIMAL SOURCE FOODS Although the sources and amounts of these animal products may vary across cultures, the advice to include them in a healthy diet should be universally applicable Dietary quality LITERATURE CITED Murphy, S P & Allen, L H (1997) A greater intake of animal products could improve the micronutrient status and development of children in East Africa In: Small Ruminant CRSP East Africa Livestock Assessment Workshop Proceedings pp 188–196, University of California, Davis, CA Neumann, C G., Sigman, M., Murphy, S P & Allen, L H (1997) The role of animal-source foods in improving diet quality and growth and development in young children In: Small Ruminant CRSP Latin America Regional Livestock Assessment Workshop Proceedings pp 191–204, University of California, Davis, CA Neumann, C., Harris, D M & Rogers, L M (2002) Contribution of animal source foods in improving diet quality and function in children in the developing world Nutr Res 22: 193–220 Dwyer, J T (1994) Vegetarian eating patterns: science, values, and food choices—where we go from here? Am J Clin Nutr 59: 1255S–1262S Dwyer, J (1999) Convergence of plant-rich and plant-only diets Am J Clin Nutr 70: 620S–622S Calloway, D H., Murphy, S., Balderston, J., Receveur, O., Lein, D & Hudes, M (1992) Village Nutrition in Egypt, Kenya and Mexico: Looking Across the CRSP Projects University of California, Berkeley, CA Institute of Medicine (2001) Dietary Reference Intakes for Vitamin A, Vitamin K, Arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum, Nickel, Silicon, Vanadium and Zinc National Academy Press, Washington, DC Allen, L H (2002) Iron supplements: scientific issues concerning efficacy and implications for research and programs J Nutr 132: 813S–819S Truswell, A S (2002) Meat consumption and cancer of the large bowel Eur J Clin Nutr 56: S19–S24 10 Hill, M (2002) Meat, cancer and dietary advice to the public Eur J Clin Nutr 56: S36–S41 11 Biesalski, H K (2002) Meat and cancer: meat as a component of a healthy diet Eur J Clin Nutr 56: S2–S11 12 Dagnelie, P C., Vergote, F J., Van Staveren, W A., van den Berg, H., Dingjan, P G & Hautvast, J G (1990) High prevalence of rickets in infants on macrobiotic diets Am J Clin Nutr 51: 202–208 13 Dagnelie, P C., Van Staveren, W A., Vergote, F J., Dingjan, P G., van den Berg, H & Hautvast, J G (1989) Increased risk of vitamin B-12 and iron deficiency in infants on macrobiotic diets Am J Clin Nutr 50: 818–824 14 Gittelsohn, J., Shankar, A V., West, K P., Ram, R., Dhungel, C & Dahal, B (1997) Infant feeding practices reflect antecedent risk of xerophthalmia in Nepali children Eur J Clin Nutr 51: 484–490 15 Haddad, E H., Berk, L S., Kettering, J D., Hubbard, R W & Peters, W R (1999) Dietary intake and biochemical, hematologic, and immune status of vegans compared with nonvegetarians Am J Clin Nutr 70: 586S–593S 16 Hunt, J R (2002) Moving toward a plant-based diet: are iron and zinc at risk? Nutr Rev 60: 127–134 17 Siekmann, J H., Allen, L H., Bwibo, N O., Demment, M W., Murphy, S P & Neumann, C G (2003) Kenyan school children have multiple micronutrient deficiencies, but increased plasma vitamin B-12 is the only detectable micronutrient response to meat or milk supplementation J Nutr 133: 3972S– 3980S 18 Refsum, H., Yajnik, C S., Gadkari, M., Schneede, J., Vollset, S E., Orning, L., Guttormsen, A B., Joglekar, A., Sayyad, M., Ulvik, A & Ueland, P M (2001) Hyperhomocysteinemia and elevated methylmalonic acid indicate a high prevalence of cobalamin deficiency in Asian Indians Am J Clin Nutr 74: 233–241 19 Casterline, J E., Allen, L H & Ruel, M T (1997) Vitamin B-12 deficiency is very prevalent in lactating Guatemalan women and their infants at three months postpartum J Nutr 127: 1966–1972 20 Allen, L H., Rosado, J L., Casterline, J E., Martinez, H., Lopez, P., Mun˜oz, E & Black, A K (1995) Vitamin B-12 deficiency and malabsorption are highly prevalent in rural Mexican communities Am J Clin Nutr 62: 1013–1019 21 Herrmann, W., Schorr, H., Purschwitz, K., Rassoul, F & Richter, V (2001) Total homocysteine, vitamin B-12, and total antioxidant status in vegetarians Clin Chem 47: 1094–1101 22 Krajcovicova-Kudlackova, M., Blazicek, P., Kopcova, J., Bederova, A & Babinska, K (2000) Homocysteine levels in vegetarians versus omnivores Ann Nutr Metab 44: 135–138 23 Brown, K., Dewey, K & Allen, L (1998) Complementary feeding of young children in developing countries: a review of current scientific knowledge WHO/NUT/98.1 WHO: Geneva, Switzerland 24 U.S Department of Agriculture Human Nutrition Information Service (1992) The Food Guide Pyramid Home and Garden Bulletin 252, U.S Government Printing Office, Washington, DC 25 U.S Department of Agriculture Human Nutrition Information Service (1993) USDA’s Food Guide Background and development Miscellaneous Publication No 1514, U.S Government Printing Office, Washington, DC 26 Venti, C A & Johnston, C S (2002) Modified Food Guide Pyramid for lactovegetarians and vegans J Nutr 132: 1050–1054 27 Painter, J., Rah, J.-H & Lee, Y.-K (2002) Comparison of international food guide pictorial representations J Am Diet Assoc 102: 483–489 28 Kennedy, E T., Ohls, F., Carlson, S & Fleming, K (1995) The Healthy Eating Index: design and applications J Am Diet Assoc 95: 1103–1108 29 Murphy, S P., Calloway, D H & Beaton, G H (1995) Schoolchildren have similar predicted prevalences of inadequate intakes as toddlers in village populations in Egypt, Kenya, and Mexico Eur J Clin Nutr 49: 647–657 30 Calloway, D H., Murphy, S P., Bunch, S & Woerner, J (1994) WorldFood Dietary Assessment System User’s Guides The University of California, Berkeley, CA 31 Torun, B., Davies, P.S.W., Livingstone, M.B.E., Paolisso, M., Sackett, R & Spurr, G B (1996) Energy requirements and dietary energy recommendations for children and adolescents to 18 years old Eur J Clin Nutr 50: S37– S81 32 Dewey, K G., Beaton, G., Fjeld, C., Lonnerdal, B & Reeds, P (1996) Protein requirements of infants and children Eur J Clin Nutr 50: S119–S150 33 Institute of Medicine (1997) Dietary Reference Intakes for Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride National Academy Press, Washington, DC 34 Institute of Medicine (1998) Dietary Reference Intakes for Thiamin, Riboflavin, Niacin, Vitamin B6, Folate, Vitamin B-12, Pantothenic Acid, Biotin, and Choline National Academy Press, Washington, DC 35 Institute of Medicine (2000) Dietary Reference Intakes for Vitamin C, Vitamin E, Selenium, and Carotenoids National Academy Press, Washington, DC Downloaded from jn.nutrition.org by on September 16, 2008 Dietary quality can be evaluated in a variety of ways One of the easiest ways is to determine a mean proportion of nutrient recommendations that is supplied by the diet (as was done for the snacks for the Kenya study and shown in Table 3) This approach also could be used to evaluate the impact of including various amounts of ASF on overall nutrient adequacy, using a more extensive list of nutrients However, a food-based dietary quality measure also has been utilized in scoring schemes such as the Healthy Eating Index (HEI) (28) This approach to determining dietary quality compares intakes of the five major food groups (grains, vegetables, fruit, dairy and meats) to those recommended by the FGP and assigns a score (e.g., zero for no intake of a food group and 10 for at least the recommended intake) The average score across the five groups then can be used to determine the overall dietary quality In addition, the HEI scores intakes of total fat, saturated fat and cholesterol to provide measures of overconsumption Such an evaluation scheme eliminates the need to utilize extensive food composition tables when determining overall dietary quality Thus, an index like the HEI could provide a useful method of quickly evaluating dietary quality in both developing and developed countries A diet with a high dietary quality score needs to include either dairy or meat products (or meat substitutes), but still be moderate in fat 3935S ... and animal source foods The nutrient levels in several plant and animal source foods are compared in Table Whether considered per unit of weight or per unit of energy, ASF tend to be richer sources... the snack foods were not combined with any other foods Downloaded from jn.nutrition.org by on September 16, 2008 Food guides NUTRITIONAL IMPORTANCE OF ANIMAL SOURCE FOODS Although the sources and... plant source foods Thus, ASF can fill multiple micronutrient gaps at a lower volume of intake than can plant source foods Just 100 g of cooked beef provides an entire day’s recommended intake of
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