JournalsNutritional importance of animal source foods

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 1
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

1
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.
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 Ó 2003 American Society for Nutritional Sciences.

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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 1

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

1
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 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 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 2
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
0.07
2

0.12
0.12
1.2
0.2
0

127
531
8.7
0
0
0.06
28
0.15
0.11
0.5
0.1
0

32
134
1.9
370
0
0.07
72
0.14
0.02
0.4
0.1

0

45
188
1.1
971
0
0.06
31
0.06
0.14
0.2
0.0
0

51
213
3.3
55
0.39
0.16
119
0.01
0.18
3.9
2.4
14

269
1124

24.9
0
1.87
0.15
4
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

1
2
3

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).

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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 riboflavin, vitamin B-12, calcium, phosphorus, fat and protein were significantly higher (6).

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SUPPLEMENT

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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 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 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
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 1 cup of milk is a serving) and 5–7 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.

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 schooler’s recommended intake. As expected, the two snacks
containing ASF supplied a higher proportion of most nutrients

TABLE 3
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
0
25
4
11
12
23

20
73
70
83

82
38
5
12
48

20
124
17
106
27
2
26
86
51

1
2

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.
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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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
1. 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.
2. 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.
3. 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.
4. Dwyer, J. T. (1994) Vegetarian eating patterns: science, values, and
food choices—where do we go from here? Am. J. Clin. Nutr. 59: 1255S–1262S.
5. Dwyer, J. (1999) Convergence of plant-rich and plant-only diets. Am.
J. Clin. Nutr. 70: 620S–622S.
6. 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.
7. 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.
8. Allen, L. H. (2002) Iron supplements: scientific issues concerning
efficacy and implications for research and programs. J. Nutr. 132: 813S–819S.
9. 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 1 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.

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