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Micronutrient deficiencies

Several lines of evidence suggest that micronutrient (mineral and/or vitamin) deficiencies may explain at least some of the early growth failure. As summarized in Table 3, there was a high predicted prevalence of inadequate vitamin and mineral intakes in all three CRSP countries (Callowly et al. 1992, Murphy et al. 1992). The estimates of mineral adequacy were based on algorithms that took into consideration the high intake of phytate (especially in Mexico) and the low consumption of animal products and ascorbic acid. The Guatemalan diet is also high in fiber and phytate and low in ascorbic acid and animal products.

TABLE 3 Predicted prevalence of children with inadequate nutrient intakes¹

¹ From analyses by Calloway et al. (1992) and Murphy et al. (1992). Intakes of niacin, folate, vitamin B-6 and copper were adequate in all three locations. For vitamin A, iron, zinc and copper comparisons are against FAO/WHO basal requirements, i.e., that needed to prevent clinically detectable signs of functional impairment. The prevalence of low intakes would have been substantially higher if based on normative requirements.

There was a very high prevalence of anemia and iron deficiency (low ferritin) in all three CRSP studies. For Egypt, Mexico and Kenya, respectively, low hemoglobin was present in 73, 62 and 74%, and iron deficiency (low ferritin) was present in 38,45 and 40% of preschoolers (Murphy et al. l 992). There is a strong possibility that the Guatemalan children were also iron deficient based on the similarity of their diet to that of the Mexican children, the poor absorption of iron from maize (Martinez-Torres et al.1987) and the high prevalence of iron-deficiency anemia in Central America (DeMaeyer and Adiels-Tegman 1985). Habicht et al. (1973) reported that anemia was not found in 1971 in unsupplemented 2-y olds; however, information about iron deficiency without anemia was not provided. Finally, iron supplements have improved the cognitive (mental) performance of rural Guatemalan children in other studies (Lozoff et al. 1985).

Preschoolers' growth in Mexico and Kenya was related positively to the amount of animal products consumed in their usual diet (Allen et al. l992b, Neumann et al. 1992); animal products supply more nutrients, such as available iron and zinc, and vitamin A and are markers for a diet that is generally of higher quality and lower in fiber and phytate (Allen et al. 1992a). Animal product consumption, as well as other indicators of a better quality diet, also predicted a number of cognitive and behavioral outcomes in children in all three countries.

Micronutrient content of the INCAP supplements

The comparative data presented in Figure 1 also illustrates the important point that even the Guatemalan children supplemented with Atole did not attain the average size of those in any of the CRSP countries and that the supplement failed to prevent all but a very small amount of their growth faltering. Because even the smaller degree of growth stunting of CRSP children was associated with functional deficits, it is reasonable to assume that even those Guatemalan individuals who benefited from the Atole supplement still suffered from a substantial amount of functional impairment.

INCAP's Atole supplement was designed to provide additional energy and protein. It consisted of (g/180 mL) Incaparina,, a vegetable protein mixture (13.5), dry skim milk (21.6) and sugar (9.0) (Martoreal et al. 1995a). The Fresco, which contained only sugar, provided only one third as much energy and no protein. The Atole contained calcium and phosphorus whereas the Fresco did not. Because the Atole ingredients also contained micronutrients, the concentrations of several vitamins and minerals were matched in the two supplements with the aim of preventing differences in these from confounding the interpretation of the results. However, between birth and 2 y of age, the children unexpectedly drank about four times as much Atole as Fresco and twice as much between birth and 3 y (Schroeder et al. 1992). This means, as presented for the 0-2-y age period in Table 4, that there was a difference in the actual micronutrient intake between the two groups. Estimated intakes of four micronutrients (zinc, vitamin B-6, folacin and vitamin B-12) not originally considered in the formulation have been calculated here from the dry skim milk in the Atole. Data are not available for the micronutrient composition of the incaparina. The 1989 RDA values are used (NRC, 1989).

TABLE 4 Nutrients in INCAP supplemento consumed by children 1-2 y

¹ Calculated contribution from the skim milk in Atole.

The difference between the micronutrients consumed in the two supplements raises two concerns. First, it is impossible to be certain that the greater benefits of the Atole supplement on postpartum growth and development are attributable to its energy content alone. [We note that this was not true for the relationship between energy supplementation of the pregnant woman and birth weight, where this association remained significant when the amount of supplement was controlled for (Habicht et al. l995).] Second, the supplements failed to improve the intake of some micronutrients substantially. Notably, neither supplement contributed much zinc, which may be growth limiting in this population, or ascorbic acid, which might have improved iron absorption and subsequently growth, or vitamin B-6, which might have improved infant cognitive development. Although this is speculation, there is no doubt that even the Atole did not supply enough of some nutrient(s) to prevent growth stunting during the first 2 y after birth.

The nutritional implications of early growth stunting

Figure 2 compares children's average length growth rates between 18 and 30 mo of age for the three CRSP projects, the INCAP study (Martorell and Klein 1980) and the National Center for Health Statistics (NCHS) reference population (Hamilll et al. 1979). The rate of increase in the four poorer countries was less than that of the reference children so that some growth failure was still occurring during this period. However, given that the Guatemalan children were so much shorter than CRSP children at 30-36 mo (Fig. 1), it is remarkable that even the Guatemalans supplemented with Fresco were growing at least as fast as children in Egypt and Kenya, and those supplemented with Atole grew as rapidly as children in all three CRSP locations. The pattern for weight was similar, the Atole-supplemented Guatemalans growing faster than the Mexicans or Kenyans during this period (Fig. 3). This means that the greater degree of growth failure of the Guatemalan children occurred before the age of 18 mo (see Martorell et al. 1995b). Infants in all four countries were breast-fed, the majority receiving almost all of

FIGURE 2 Rate of length growth of NCHS reference, Nutrition CRSP and Guatemalan children. E = Egypt; M = Mexico; K = Kenya; GS = Guatemalans supplemented with Atole; GNS = Guatemalans supplemented with Fresco. Values are for the 18-30-mo age period for all groups. their nutrients from breast milk through at least the first 8 mo of life. Guatemalan infants consumed an average of ~10% of their energy requirements from Atole between 3 and 12 mo of age (Schroeder et al. 1995), most of this presumably toward the end of the first year. Some children still received small amounts of breast milk beyond 18 mot Considering that the most rapid growth failure occurred within a few months of birth in all the population samples, the conclusion must be that either maternal milk or weaning foods failed to supply the nutrients needed by the children.

FIGURE 3 Rate of weight growth of NCHS reference, Nutrition CRSP and Guatemalan children. E = Egypt; M = Mexico; K = Kenya; GS = Guatemalans supplemented with Atole; GNS = Guatemalans supplemented with Fresco. Values are for the 18-30-mo age period for all groups.

The CRSP found some evidence that the poor micronutrient status of the mothers had an adverse effect on breast milk composition. The concentrations of water soluble vitamins in breast milk are especially responsive to maternal dietary intake. In Egypt, breast milk concentrations of vitamin B-6 were only about one half those in milk of nonsupplemented American women and predicted the behavior of the infants at 6 mo of age (McCullough et al. 1990). The milk content of this vitamin was not analyzed in Kenya or Mexico. The only other vitamin measured in breast milk was vitamin B-12 in Kenya and Mexico. The content was deficient in the milk of all the Kenyan mothers (Neumann et al. 1992) and in 62% of the milk samples in Mexico (Black et al. 1994). More data are needed concerning whether the micronutrient content of maternal milk is adequate to support infant growth and development in regions where dietary quality is poor.

The INCAP and Nutrition CRSP studies show that growth failure occurs very early in life in marginally malnourished populations. They leave little doubt that early malnutrition usually causes permanent growth stunting and associated functional deficits. However, we still do not know why it occurs or which nutrients are growth limiting. In Kenya and Guatemala, where there was a shortage of food, inadequate energy intake probably explains some, but not all, of the growth failure. However, the energy provided by the INCAP Atole supplement was not very effective at preventing growth stunting and children given this supplement were still smaller than the average CRSP child at ~30 mo of age.

It is highly probable that, as in the Nutrition CRSP, micronutrient deficiencies played a role in the failure of Guatemalan children to grow adequately. In preschoolers and schoolers this can be attributed in part to their low intake of animal products and the poor bioavailability of minerals from dietary constituents. But the growth failure occurs during the first few months after birth when breast milk provides all or by far the majority of infant's nourishment. It is also evident from these comparisons that the greater severity of growth stunting in the Guatemalan children can be attributed to their nutritional status before the age of 18 mo; between 18 and 30 mo they grew as well or faster than the CRSP children.

For many compelling reasons nutritionists support breast milk as the sole food for infants during the first 4-6 mo of life. Certainly, however, breast milk was not adequate to support optimal growth of either the CRSP or the INCAP infants. Although the introduction of supplementary foods and infant morbidity (especially subclinical) cannot be ruled out definitively as causes of the inadequate growth, in none of the four locations have these explained more than a small proportion of the growth faltering. Further attention should be paid to the possibility that maternal micronutrient deficiencies result in infants having stores at birth and/or intakes from breast milk that are inadequate to support optimal growth and development in such environments. Efforts should now be focused on understanding when to intervene, how to intervene and what nutrients to provide to prevent early growth stunting and its associated persistent functional deficits.

ACKNOWLEDGMENTS

The author is indebted to her coprincipal investigators in the Mexico Nutrition CRSP, Gretel H. Pelto of the University of Connecticut and Adolfo Chavez who headed the research team at the Instituto Nacional de la Nutrición in Mexico City. Thanks are also due to the principal investigators of the Egypt and Kenya projects, the team at Berkeley and the INCAP investigators, who produced the data discussed here and made helpful comments on this paper.

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