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A major consideration in any discussion of the results presented above is the choice of reference population. The ideal population to use would be one with similar growth potential as the Guatemalan population but living in an environment that does not constrain growth. Whether the Mexican-American population is the appropriate choice is not entirely clear. Just as Guatemalans, Mexican-Americans are of Spanish-Indian ancestry, though differences may exist in the proportions of admixture. Mexican-Americans are one of the tallest Hispanic populations reported in the literature (Martorell et al.1989) and are as tall as well-to-do populations from Guatemala (Johnston et al. 1973, Johnston et al. 1976) and Mexico City (Ramos-Galván 1975). Before adolescence, Mexican-Americans are as tall as the general USA population suggesting unconstrained growth but important differences are observed during adolescence (Figure 2). One explanation might be that differences are due to genetic factors that lead to a faster growth tempo in Mexican-Americans and, hence, to a shorter duration of the adolescent growth phase. On the other hand, sexual maturation data for Mexican-Americans from HHANES do not suggest precociousness relative to patterns observed in European longitudinal studies (Villareal et al. 1989). But, data of this type are notoriously difficult to collect reliably and cross-study comparisons may be flawed. Also, the lack of USA reference data for sexual maturation is a serious limitation.
Two of the sets of reference data (i.e., NCHS/WHO, Frisancho) used in this report are derived from crosssectional data and are subject to biases introduced by cohort effects. Periodic surveys reveal that average heights in the general US population have not changed for some time and hence these biases are unlikely to be important in the US data of Frisancho (1990). In the case of Mexican-Americans, marked changes in stature have occurred over time (Martorell et al. 1989). It is not clear whether future national surveys will reveal differences with respect to HHANES data, now 8-10 y old. Cohort effects could invalidate conclusions about growth during adolescence that are derived from cross-sectional studies, as in this case. Suppose that Mexican American adolescents examined in HHANES grew poorly in early childhood because of poor diets and infection. Also, suppose that conditions changed such that young Mexican-American children measured in HHANES were not constrained in their growth. If these conditions apply, the patterns of adolescent growth that are inferred from the HHANES cross-sectional data would be erroneous. Adolescents would be short, not because of poor growth during adolescence, but because of early childhood retardation and estimates of age at peak height velocity would be biased downward. The same concern applies to the studies of well-to-do populations in Guatemala (Johnston et al. 1973, Johnston et al. 1976) and Mexico City (Ramos-Galvan 1975), particularly in view of the fact that the data were collected at least two decades ago. Cohort-like effects also may be produced by migration patterns. The Mexican American data set includes an unknown proportion of Mexican-born children. If immigration rates were greater for adolescents than, for young children, the pattern shown in Figure 4 also could be produced under certain conditions (e.g., if adolescents born in Mexico were subjected to greater nutritional stress and growth retardation than native born adolescents). However, we have no evidence for differential immigration by age.
At this time, it is not clear which of the two reference populations is most appropriate for assessment of the growth of rural Guatemalans. For assessment of growth during childhood, either reference may be used because patterns exhibited by Mexican-Americans are nearly identical to those of the general US population. Guatemalan children are born retarded in length and begin experiencing additional retardation shortly after birth. Both feeding practices as well as increased frequency of illness are the likely proximate determinants for this further decline. Though breastfeeding is nearly universal in this population, exclusive breastfeeding, clearly shown to reduce the risk of infectious illness (Brown et al. 1989), is rarely practiced. In addition, during the second half of infancy, complementary foods are generally inadequate in both quantity and quality to meet requirements.
The infant-feeding practices of the populations upon which the references are based should also be considered. Even under industrialized country conditions, growth patterns differ between breast-fed and bottle-fed infants with bottle-fed infants showing generally greater growth, more so in weight than in length, compared to exclusively breastfed infants (Waterlow 1988). Notably, the Fels children were primarily bottle fed with 85% completely weaned by 3 mo of age (Roche et al 1989).
In the adolescent period, it is less clear whether Guatemalan growth patterns should be compared with the Mexican-American or USA general reference. If the USA data are used as the reference population, one would conclude that absolute linear growth during adolescence is as expected. If Mexican-American data are more appropriate as a reference population, one would be further impressed by the extent to which some of the losses in early childhood are made up during adolescence, perhaps through delayed maturation and longer growth periods (see Martorell et al. 1994 for a discussion of this mechanism). Whether nutrition interventions aimed at adolescents might be helpful in promoting even greater compensatory growth is not clear because these efforts also may accelerate maturation with the unwanted result of reducing growth potential (Proos et al 1991).
Regardless of the choice of reference population, it is clear that growth is markedly retarded in rural Guatemalans only in early childhood. Adolescence is certainly not a period in life when growth is constrained to a significant degree. In poor Guatemalans, therefore, stature in older children and adults indicates the degree to which growth was constrained in early childhood. Referring to height for age as an indicator of "chronic malnutrition" has brought about much confusion because it may be taken to mean that the process is still continuing. Rather, as noted by Beaton et al. (1990), length for age in the first 2-3 y of life can be said to mark the state of "failing to grow" in early childhood, particularly if repeated measures are taken, whereas in older subjects, height for age marks the state of having "failed to grow". Height for age data at school entry, for example, would be a useful but lagged indicator of nutritional status, in that it reflects conditions at about 4 or more y previously (i.e., when the children were <3 y old).
The patterns of linear growth observed in Guatemala may differ from those common to other areas of the developing world. Skeletal age assessments, made relative to British reference data, indicate a delay of ~ 1.2 y in boys 11-14 y but none in girls of the same age (Pickett et al. 1995). This may explain the pattern shown in Figure 4; differences in girls with respect to the reference do not vary much with age. In boys however, differences increase temporarily at ages 12-14 y, which suggests earlier ages at peak height velocity in the reference population than in the study sample. Growth in height appears to continue to 19-20 y of age in males (analysis not shown) but little growth takes place in females after 15 y of age.
Menarche occurs at 13.7 y in the study sample, a year or so delayed when compared with US values (Khan et al. 1995). Thus, there is an apparent contradiction between the skeletal age (no delay) and menarche (1-y delay) results in girls but it is important to point out that both assessments of maturation indicate that delays are not severe. In other areas of the world, maturation may be more delayed and a prolonged period of linear growth, for example, might allow for substantial recuperation of the height retardation incurred in early childhood (Martorell et al. 1994).
relative ignorance of growth during adolescence in developing
countries reflects the long-standing focus of attention on young
children, who are at greatest risk of malnutrition. Although the
priority remains unchanged, particularly for public health
measures, greater attention needs to be given to research on
adolescence, if only to understand the full impact of
malnutrition in early childhood.
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