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5. Continued residence in the same environment with improvements in nutrition

If nutritional deficits and disease burden are the primary causes of stunting in early childhood, as stated earlier, improvements in nutrition to avert or reverse stunting should be most efficacious at the ages when these conditions are most extreme. Using data from a longitudinal nutritional supplementation trial conducted in Guatemala, an analysis of the age differences in the impact of supplementation on length gain strongly supports this hypothesis.

In the original study nearly 2400 children between birth and 7 years of age (and their mothers) received either a high energy, high protein supplement (Atole) or low energy, no protein supplement (Fresco) between 1969 and 1977 (Martorell, Habicht & Klein, 1982). For this analysis, annual growth, supplement, illness, and home diet data were summarized for the first seven years of life 3. A series of multiple linear regression models were then used to examine the impact of supplement intake on length change while controlling for body size, percent of time with diarrhea, home diet, socioeconomic status, and gender (Schroeder et al., in press).

3 For the first year, data for ages 3-12 months were used because very little supplement was consumed before the third month of life. This information was converted to yearly figures for comparability with the other intervals.

During the first year of life, each 100 kcal/day of supplement was associated with approximately 9 mm in additional length gain (Fig. 9). The impact of this amount of supplement decreased to 5 mm and 4 mm in years two and three, respectively; nutritional supplementation had no significant impact on linear growth after age three.

Also presented in Fig. 9 are the percent of days per year with diarrhea and the RDAs, each of which declines over the first seven years of life. The deficit in energy intakes relative to the RDAs rather than the RDAs themselves would be preferable here; unfortunately, the data were not collected in such a way that these values could be calculated. However, it is likely that, because the RDAs are highest in the first three years of life and children's diets in this population are frequently insufficient in energy, the relative magnitude of energy deficits mirrored recommended allowances. In other words, the ages of highest nutritional needs, relative to weight, were also those of greatest deficit.

Fig. 9. Recommended energy intakes, percent of year spent with diarrhea, velocity deficit* and adjusted slopes of supplement (100 kcal/day) by age interval (Schroeder et al., in press).

* Compared to WHO/NCHS reference data.

Finally, the velocity deficit (cm/year) of the children who received the low energy supplement compared to the US reference (Baumgartner, Roche & Himes, 1986) is also presented in Fig. 9. As mentioned earlier, this pattern of velocity deficit is determined by the deficits in energy and high rates of illness as well as the expected rates of growth (not shown).

In summary, this analysis suggests that improvements in nutrition will have a maximal effect when growth deficits, as well as growth velocities, are highest.

These findings are consistent with other studies that have examined the impact of supplement by age. In India, 1-2-year-old children, who were fed approximately 170 kcal/day of supplement in the form of a sweet cake, grew 2.8 cm more over 14 months than unsupplemented children of the same age (Gopalan et al., 1973). This difference decreased to 1.7 cm in 2-3 and 3-4 year olds and only 1.1 cm in 4-5 year olds. It is likely that an effect was seen in the 4-5 year olds in India, because this population was more severely malnourished than the Guatemalan population described above, where no effect was found at these older ages.

The hypothesis that dietary and illness patterns determine whether nutritional improvements can avert or reverse stunting is corroborated by work from Colombia. Comparing supplemented and unsupplemented children, Lutter et al. (1990) found that responsiveness of length to supplementary feed was greatest during the weaning period (3-6 months of age) and during the peak prevalence of diarrhea (9-11 months of age).

6. Relocation from the environment that gave rise to stunting

The third group of studies to be considered involve an abrupt improvement in living conditions through migration or adoption.

6.1. Children who migrated to developed countries

Changes from 1986 to 1989 in the prevalence of low length- or height-for-age, defined as values below the 5th centile of the WHO/NCHS curves, were investigated using data collected by the Pediatric Nutrition Surveillance System of the Centers for Disease Control from 28,725 Southeast Asian refugees and 2,173,644 poor children under 5 years of age who enrolled in public health clinics of 12 US states (Yip, Scanlon & Trowbridge, 1992). There was a progressive and significant decline in the prevalence of low length-for-age in Southeast Asian but not in poor US children. In Asian children 1 to 23 months of age, the prevalence declined from 24.8% in 1982 to 13.5% in 1989, a relative reduction of more than 46%. A similar relative decline (50%) was observed in low height-for-age in older children (24 to 60 months). Standardized height-for-age Z scores were then used to determine whether the reductions were related to a sub-population of short children or to general improvement of the entire height distribution; the distribution of height Z scores for three periods over ten years had similar variance and shape, implying the latter. Each successive cohort became taller, suggesting that the steady improvement in the quality of life of the Southeast Asian population was the most likely explanatory factor.

Schumacher, Pawson & Kretchmer (1987) assessed the impact of migration and change in nutrition on the growth of 835 children 6 to 12 years of age of Hispanic, Chinese, Southeast Asian, and Filipino descent enrolled in three 'newcomer schools' in the San Francisco Bay area between December 1982 and June 1985. All birth cohorts were short upon arrival; most ethnic groups were between the 5th and 25th centile of WHO/NCHS reference values. The authors note that most cohorts exhibited a median growth velocity that was similar to or exceeded the US median. However, a sense of the magnitude of this accelerated growth is not given, limiting the potential value of the study.

6.2. Children adopted into developed countries

Winick, Meyer & Harris (1975) and Lien, Meyer & Winick (1977) examined whether adoption of previously malnourished Korean children into US families results in improved development. These studies are summarized in Table 3. Subjects were classified according to height on admission to the Holt Adoption Service using Korean growth standards (Hong, 1970). The first study included initial measurements prior to 2 years of age (early adoption) and follow-up at 6 to 8 years; the second study used measurements from 2 to 5 years of age (late adoption) compared to measurements when the children were 7 to 9 years old. The ranking of the groups remained at follow-up. However, mean centiles for height-for-age (Table 3) were greater for all groups at follow-up, suggesting catch-up growth relative to their status before adoption and to the Korean reference data. Groups who were younger at adoption improved the most (i.e., study I vs study II). The authors note that all three groups were below the 50th centile of the Harvard curves. This suggests incomplete catch-up growth. 4

4 The Korean reference used does not represent growth potential as indicated by the fact that the adopted sample is significantly taller than the Korean reference median. It is not certain, however, that the WHO/NCHS reference data is appropriate for East Asian children (Martorell, 1985). Unfortunately, comparison of the results of this study to the WHO/NCHS data is not possible because the data on actual height-for-age are not given in the published documents.

In two separate studies, one longitudinal and the other retrospective, Proos and colleagues examined the growth of Indian children from underprivileged circumstances who were adopted by Swedish families.

The longitudinal study by Proos et al. (1992), which followed 46 boys and 68 girls for 2 years after arrival, illustrates the remarkable potential for catch-up growth if children are moved from a deprived to an adequate environment at a very young age. Children were 3 to 72-months of age at arrival in Sweden (median = 9.3 months); with 62% younger than 12 months and more than 90% less than 36 months of age. The prevalence of stunting (< -2 SD below the WHO/NCHS median) decreased from 54% to 5% after 2 years of follow-up. The mean length-for-age Z scores were -2.2 upon adoption but declined to -0.7 SD 18 months after adoption. In those classified as stunted at adoption, the mean Z score declined from -3.2 SD to -1.0 SD and in those who were not stunted on adoption, the decline was from -1.1 SD to -0.21 SD after 2 years.

Table 3. Mean height centile at follow-up of Korean children adopted by US families

Group at admission*

Study I (Winick et al., 1975)

Study II (Lien et al., 1977)




















* Definition: I (<3rd centile); II (3-24 centile); and III (25 centile) of Korean growth standards for height and weight (Hong, 1970).

The retrospective study examined 107 Indian girls from the Adoption Centre, Stockholm (Proos, Hofvander & Tuvemo, 1991). The mean age of adoption was 3.7 years (range: 1 month to 11 years). Sixty-two percent of the girls were classified as stunted (below -2 SD) at arrival, with a mean height-for-age of -2.2 SD. After 2 years, the mean height Z score increased to -0.8 SD and only 20% of the girls were stunted. Oddly, mean final height, defined as the height attained 3 years after menarche, was 154 cm, only slightly greater than the height of the general Indian population. The mean adult Z score decreased to -1.4 SD, with 31% of the sample classified as stunted according to WHO/NCHS reference values 5. The mean age at onset of menarche was 11.6 years, which is 2 to 3 years earlier than found in rural Indian populations and lower in fact than observed in Swedish girls 6. Analysis indicated that later adoption was associated with faster catch-up growth and that faster catch-up growth in turn, predicted earlier menarche. The explanation for understanding why final stature was less than expected may lie in the timing of menarche. It is possible that catch-up growth in older pre-pubescent girls may trigger endocrinological responses which would lead to an earlier onset of menarche. By accelerating maturation, the duration of growth would be shortened, and in this way some of the growth that had earlier been compensated through catch-up would be lost again.

5 The WHO/NCHS reference curves used (Hamill et al., 1979) do not contain values for adults. Proos et al. (1991) appear to have used NCHS original data to estimate Z scores for final height.

6 Eveleth & Tanner (1990) give values of 13.0 for Swedish girls.

7. Discussion and conclusions

Linear growth retardation, or stunting, occurs primarily in the first 2 to 3 years of life and is a reflection of the interactive effects of poor energy and nutrient intakes and infection. In this review data were examined to investigate how much, if any, catch-up growth occurs during later childhood and adolescence in various settings in developing countries.

Some of the findings presented may be questioned because of the use of external reference data, commonly from the United States. If ethnic differences among populations are important determinants of adolescent growth patterns (e.g., variations in age at take off, peak height velocity and duration of growth), then our ability to detect catch-up growth will be obfuscated by the use of an inappropriate reference population. These concerns do not apply to the analyses of Guatemalan and Indian data which relate stunting in early childhood to growth from 5 years of age till adulthood (i.e., these analyses do not depend on an external reference). The Korean study (Lien, Meyer & Winick, 1977; Winick, Meyer & Harris, 1975) also is less problematic since it used a Korean standard. Most analyses presented, however, relied on US reference data to make inferences about catch-up growth from cross-sectional data. For many of the populations studied the issue of ethnic differences in adolescent growth with respect to the US reference population remains unresolved. With regard to the American slaves, there should be less concern about appropriateness of the reference population, since US Blacks and whites have similar growth patterns during adolescence and nearly identical mean adult heights (Frisancho, 1990).

One conclusion of this review is that prolongation of the growth period can make up for some of the earlier growth retardation. How much catch-up growth is achieved depends on the degree to which biological maturation is delayed. In settings where maturation is grossly retarded, the potential for catch-up in growth will be marked. However, in developing countries today maturation is measurably delayed but not dramatically retarded. Median ages at menarche, for example, are almost always less than 15 years and sometimes not very different from what is observed in well-nourished populations (Eveleth & Tanner, 1990). Along with less maturational retardation, there is also less stunting compared to a few decades ago (Eveleth & Tanner, 1990). These two conditions mean that, while there is less growth failure to make up, there is less opportunity to do so through the simple mechanism of a prolonged growth period.

A second mechanism through which catch-up growth can be achieved is through accelerated growth rates. This is clearly evident in the studies of children adopted by Swedish families. The change in the prevalence of stunting and in the average Z scores two years after adoption were of such magnitude that growth rates must have greatly exceeded normality. Is this an unusual occurrence? Are children prior to adoption endocrinologically compromised, perhaps through psycho-social mechanisms, and hence likely to show catch-up growth once adopted? There are no clear answers to these questions.

A strong conclusion is that in most populations in developing countries, exemplified in this review by samples from rural Kenya, Malawi, India and Guatemala, the marked degree of retardation incurred in early childhood generally remains into adulthood. In other words, catch-up growth during later childhood and adolescence seems to be minimal in populations which continue to reside in the same environment which gave rise to stunting in early childhood. On the other hand, stunting can be reduced in early childhood if the environment is improved. This is demonstrated by the beneficial impact of food supplementation on the growth of Guatemalan children less than 3 years of age. The adoption studies of Korean children by US families and of Indian children by Swedish families show that adoption within the first few years of life leads to substantial catch-up in growth (though initial inter-group differences may remain) and increased height at follow-up. Unfortunately, these studies have not provided us with good information about growth during adolescence nor do they always report adult stature. Lack of this information does not allow us to make more definitive statements about the degree of catch-up growth which can be achieved through adoption.

Stunting in school age children and in adolescents may be less reversible. Earlier it was noted that, if subjects remain in their places of origin with conditions unchanged, little or no catch-up in growth usually occurs. The Guatemalan study shows that a food supplement that is highly effective in improving growth during the period of growth failure does not improve growth in children from 3 to 7 years of age, when growth is normal. Confirmation of this differential effect of supplementation by age in other developing country settings is desirable. Also needed are studies that examine the effects on growth of nutrition and health interventions aimed at adolescents in developing countries; currently, there is no information of this type. There are also the intriguing findings from Sweden that suggest that although older children grow faster after adoption, the response hastens maturation, shortens the growth period, and in effect limits the possibility of catch-up growth. Confirmation of these findings is desirable as well.

Finally, what is the effect of catch-up growth in school age or adolescence on the functional correlates of stunting? While this is not a question addressed in this review, we would like to caution that remedial actions later in life may not redress all of the problems for which stunting is a marker. The effects on the functional correlates of stunting may vary greatly, some aspects improving along with stature and others not, perhaps as a function of whether they are direct or indirect consequences of growth retardation. Possible examples of direct and hence alterable correlates of growth are increased lean body mass and decreased obstetric risk in women due to small maternal size. On the other hand, effects of early childhood malnutrition on learning and behavior may not be redressed fully by the conditions which can produce catch-up growth. If these views hold, addressing the problems of malnutrition and infection of early childhood is the preferred strategy in a resource poor environment because it would prevent stunting as well as its functional correlates. Intervening later, on the other hand, may have only a limited effect.

Acknowledgments - This work was supported by grant #IC-75/03 from the International Center for Research on Women and by the Cornell International Institute for Food, Agriculture and Development.


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