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
ABSTRACT Animal source foods can provide a variety of micronutrients that are difcult to obtain in adequate quantities from plant source foods alone. In the 1980s, the Nutrition Collaborative Research Support Program identied six micronutrients that were particularly low in the primarily vegetarian diets of schoolchildren in rural Egypt, Kenya and Mexico: vitamin A, vitamin B-12, riboavin, calcium, iron and zinc. Negative health outcomes associated with inadequate intake of these nutrients include anemia, poor growth, rickets, impaired cognitive performance, blindness, neuromuscular decits 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 childs energy requirement could provide 38% of the calcium, 83% of the vitamin B-12 and 82% of the riboavin 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: 3932S3935S, 2003. KEY WORDS:  animal source foods  schoolers  dietary quality  micronutrients

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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 (13); 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 ber (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, identied 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 1 shows the estimated prevalence of inadequate intake by young children for six nutrients of particular concern: iron, zinc, vitamin B-12, riboavin, 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 decits, 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, riboavin and vitamin B-12 in all three countries, whereas animal source protein was a strong predictor of calcium intake

1 Presented at the conference Animal Source Foods and Nutrition in Developing Countries held in Washington, D.C. June 2426, 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 OLakes 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. 2 To whom correspondence should be addressed. E-mail: suzanne@crch. hawaii.edu. 3 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 2003 American Society for Nutritional Sciences.

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TABLE 1
Prevalence (%) of inadequate intake by school-age children, NCRSP, 198419861
Nutrient Protein Vitamin A2 Vitamin B-12 Riboavin Calcium Iron2 Zinc2
1 2

Egypt 0.0 9.2 23.6 16.3 69.3 70.4 3.5

Kenya 0.0 0.6 86.9 1.6 91.2 31.4 29.5

Mexico 0.0 24.4 38.3 83.4 0.0 87.3 9.2

See reference 29. Using basal requirement estimates.

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 6 d of intake recorded on days when no ASF were consumed and another 6 d when some ASF were consumed. On days when animal products were consumed (irrespective of the amount), intakes of riboavin, vitamin B-12, calcium, phosphorus, fat and protein were signicantly higher (6). Nutrients in plant and animal source foods The nutrient levels in several plant and animal source foods are compared in Table 2. 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 2 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 ll multiple micronutrient gaps at a lower volume of intake than can plant source foods. Just 100 g of cooked beef provides an entire days recommended intake of protein, vitamin B-12 and zinc and contributes substantially to meeting the riboavin and iron recommendations. Likewise, 100 g of milk also can provide substantial amounts of calcium, vitamin B-12, vitamin A and riboavin. 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 riboavin 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 afuent 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 deciencies 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 sh intake when they were 13 to 24

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TABLE 2
Composition of selected foods (per 100 g) compared with requirements for a school-age child1
Maize, cooked 119 497 2.7 0 0 0.07 2 0.12 0.12 1.2 0.2 0 Kidney beans, cooked 127 531 8.7 0 0 0.06 28 0.15 0.11 0.5 0.1 0 Kale, cooked 32 134 1.9 370 0 0.07 72 0.14 0.02 0.4 0.1 0 Carrots, raw 45 188 1.1 971 0 0.06 31 0.06 0.14 0.2 0.0 0 Milk, whole, unfortied 51 213 3.3 55 0.39 0.16 119 0.01 0.18 3.9 2.4 14 Beef, medium fat, cooked 269 1124 24.9 0 1.87 0.15 4 0.32 2.05 18 8.4 75 Recommended intake2 1600 6688 17.3 400 1.2 0.6 800 1.86 1.44 N/A N/A N/A

Nutrient Energy (kcal ) (kJ ) Protein (g) Vitamin A (mg RAE)3 Vitamin B-12 (mg) Riboavin (mg) Calcium (mg) Available iron (mg) Available zinc (mg) Fat (g) Saturated fat (g) Cholesterol (mg)
1 2 3

Nutrient composition data from reference 30. Daily recommended intake for a 7-y-old child weighing 20 kg. See references (7,3135). 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).

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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 decits of vitamin B-12 (15). However, the vegan diets also tended to be lower in fat and higher in ber, 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 deciency 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 deciency 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 difculty 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). 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 3 shows the composition of the three snacks expressed as a percentage of a schoolers recommended intake. As expected, the two snacks containing ASF supplied a higher proportion of most nutrients

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 3 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 3 that the snacks provided to the school-age children supplied only 20% of the childrens 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 400500 mL of milk (to obtain sufcient 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.
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Food guides 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 difcult, 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 fortied 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 23 servings of dairy products (where 1 cup of milk is a serving) and 57 ounces of lean meat or meat substitutes (where one-half cup of cooked dried beans, 1 egg or one-third cup of nuts counts as 1 ounce of meat) appears to be applicable to developing countries as well.

TABLE 3
Percentage of a school-age childs recommended nutrient intake supplied by three snacks
Nutrient Energy Protein Vitamin A3 Vitamin B-12 Riboavin Calcium Available iron4 Available zinc4 Average
1 2

Recommended intake1 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

Githeri2 only (%) 20 62 53 0 25 4 11 12 23

Githeri plus milk (%) 20 73 70 83 82 38 5 12 48

Githeri plus beef (%) 20 124 17 106 27 2 26 86 51

Daily recommended intake for a 7-y-old child weighing 20 kg (7, 3135). 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 reect those in use in 1999. 3 Retinol activity equivalents (RAE) for the snacks were converted from retinol equivalents as recommended in reference 7. 4 Iron and zinc availability were calculated assuming that the snack foods were not combined with any other foods.

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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 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 ve 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 ve 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. LITERATURE CITED
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