- Top of page
- DISCUSSION AND CONCLUSION
- LITERATURE CITED
Stunting, or linear growth retardation, has been documented in up to half of all children in rural indigenous populations of South America. Stunting is well understood as a signal of adverse conditions during growth, and has been associated with developmentally induced modifications to body composition, including body fat and muscularity, that stem from early growth restriction. This article examines the relation between short stature and three anthropometric indicators of body composition during childhood and adolescence among a rural, indigenous population of forager-horticulturalists. Anthropometric data were collected annually from 483 Tsimane' youth, ages 2–10 years, in 13 communities in the Beni region of Bolivia for 6 consecutive years (2002–2007). Baseline height-for-age was used to indicate stunting (HAZ < −2.0) and compared with z-scores of body mass index (BMI), sum of two skinfolds, and arm muscle area. Multilevel regression models indicate baseline stunting is associated with lower BMI z-scores (B = −0.386; P < 0.001), body fatness (ZSkinfold, B = −0.164; P < 0.001), and arm muscularity (AMAZ, B = −0.580; P < 0.001) in youth across a period of 6 years. When split by sex, there was a stronger relation between baseline stunting and lower skinfold body fat scores among girls (B = −0.244; P < 0.001) than boys (B = −0.080; P = 0.087). In contrast, baseline stunting was associated with lower arm muscularity in both girls (B = −0.498; P < 0.001) and boys (B = −0.646; P < 0.001). The relation between linear growth restriction and indicators of body composition persist into adolescence, providing additional insight into the influence of adverse conditions during growth. Am J Phys Anthropol 153:92–102, 2014. © 2013 Wiley Periodicals, Inc.
Stunting, or linear growth retardation (< −2.0 SD in height-for-age Z-score), is common in many rural indigenous populations of South America, and most recent estimates suggest that about 165 million children under the age of five worldwide were growth stunted (de Onis et al., 2012; Black et al., 2013). The bulk of research on growth patterns in biological anthropology (Kuzawa, 1998; Bogin, 1999; Walker et al., 2006; Bogin et al., 2007) draws on evolutionary life history, which explicitly grapples with how trade-offs between overlapping domains of growth, reproduction, and maintenance serve to enhance survival and reproduction in heterogeneous environments. In terms of understanding human phenotypic variation, these developmental trade-offs connect early growth deficits to long-term consequences including shorter stature (Stein et al., 2010; Sterling et al., 2012) and increased risk of developing metabolic diseases including cardiovascular disease and type 2 diabetes (Barker et al., 2002). While there is considerable evidence linking growth restriction in utero to adult outcomes, research on the associations between postnatal stunting and later-life body composition has produced more variable results. Body fat reserves play important roles in survival and reproduction and developmental oscillations in body composition throughout childhood and adolescence may have evolutionary consequences (Zafon, 2007; Adair, 2008; Wells, 2010). Therefore, research examining how growth restriction or stunting in childhood is related to body composition may deserve additional attention.
Over the past several decades, research has shown links between early growth stunting and later body composition but the direction of the association likely varies with local context. Among some urbanizing populations, childhood stunting exists alongside rapidly rising rates of obesity. This dual nutritional burden is hypothesized to stem from developmental adaptations in which metabolic adjustments early in life result in increased risk of metabolic disease, including obesity, later in life (Frisancho, 2003; Leonard et al., 2009; Wilson et al., 2012). Several large studies have identified the co-occurrence of both stunting and overweight or obesity in children (Popkin et al., 1996; Fernald and Neufeld, 2007) and evidence for metabolic trade-offs associated with linear growth stunting is mounting (Hoffmann et al., 2000a,b). For example, in large surveys from Russia, Brazil, China, and the Republic of South Africa, Popkin et al. (1996) found that stunted children had a 1.7–7.8 times increased risk of being overweight than their non-stunted peers, depending on country and household income. Research among Mayans in urban Mexico has also demonstrated associations between child stature, lean body mass, and total energy expenditure (Wilson et al., 2012) and that the effects of shortness and stunting may persist across generations (Varela-Silva et al., 2009; Azcorra et al., 2013).
Several longitudinal or cohort studies have failed to find clear associations between stunting and weight or body fat during childhood or adolescence. For example, in their longitudinal research among South African urban children, Cameron et al. (2005) found children who were stunted at 2 years of age were shorter and lighter than their non-stunted peers at 9 years of age, but they did not identify associations between stunting and later BMI, body composition, or fat patterning. Research from Guatemala (Li et al., 2003) and Jamaica (Walker et al., 2002, 2007) has also suggested early growth restriction is associated with less body fat and muscularity over time. The results in this literature indicate that the consequences of linear growth restriction are complex and likely depend on local environment, diet, and developmental timing. Therefore, as several researchers have noted (Baker et al., 2009; Varela-Silva et al., 2012), longitudinal research in rural areas of low-income countries is needed to better understand the full range of consequences of growth trade-offs.
The goal of this article is to examine the short-run biological consequences of linear growth stunting throughout childhood and adolescence in a foraging-horticultural group with high rates of stunting and infection but limited evidence for overnutrition. We explore the consequences of growth stunting on both muscularity and body fatness using anthropometric data collected from Tsimane' youth from 2002 to 2007. Prior work among Bolivia's Tsimane' has documented both frequent stunting (Foster et al., 2005) and evidence for catch-up growth during childhood associated with household composition and income (Godoy et al., 2010a). Additionally, previous research suggests immune activation is related to linear growth retardation and reduced body fat reserves (McDade et al., 2008). Given these associations, we first predict that tracking childhood growth will identify associations between growth stunting and body composition across a 6-year period. Second, we predict that sex will modify the relations between growth stunting, muscularity, and body fat based on literature suggesting that boys may be more sensitive to the nutritional environment than girls (Stinson, 1985; Kuzawa, 2007). Third, we predict that the association between stunting and body composition will vary with age and, more specifically, become stronger at later ages as growth becomes canalized (Bogin, 1999). Finally, we predict that the association between stunting and body fatness will remain after controlling for maternal, household, and community effects.
DISCUSSION AND CONCLUSION
- Top of page
- DISCUSSION AND CONCLUSION
- LITERATURE CITED
Indigenous groups throughout South America suffer disproportionately high rates of infection and undernutrition (Hurtado et al., 2005), but several studies also have found evidence of overweight and obesity among adults (Benefice et al., 2007; Zeng et al., 2013). This study draws on panel data to examine the relation between childhood stunting and body composition among a sample of Tsimane' youth. Overall, we found that linear growth retardation early in life has implications for body composition throughout adolescence. Among Tsimane' youth, stunting was associated with lower age and sex adjusted scores of BMI, skinfold body fat reserves, and arm muscularity after a period of 6 years. The effects of linear growth retardation are particularly evident among girls and older youth.
Findings in this article are consistent with literature suggesting early growth restriction may permanently constrain lean mass development and modify body fat throughout adolescence and into adulthood (Cameron, 2007; Wells, 2007). For example, in Guatemala, Li et al. (2003) found that growth retardation in early childhood (0–2 years of age) was associated with leanness and less body fat at 21–27 years of age. In a prospective cohort study in Kingston, Jamaica, Walker et al. (2002) found that, after controlling for the effects of low birth weight, children who were “chronically stunted” (stunted both at 9–24 months and 7 years) had less fat and lower BMI than non-stunted children at 11 years of age. Although stunted children had less body fat than non-stunted children, stunting was also associated with a more central fat distribution (as assessed by the ratio of subscapular: triceps skinfolds), indicating that stunting may modify how fat is distributed across the body.
Our findings and other research among Latin American children (Varela-Silva et al., 2012, Wilson et al., 2012) are relevant to understanding the co-occurrence of childhood stunting and overweight or obese status (Popkin et al., 1996). Although there is variation in these studies with respect to location, study design, and methodology, they point to important role of environment in human growth and downstream health (Cameron, 2007). A potential explanation for differences in the literature is that possible links between stunting and overweight or abdominal fat patterning may be visible only among youth with access to high-fat or calorically dense foods (Popkin et al., 1996; Frisancho, 2003; Kain et al., 2005) and moderate levels of daily activity. A high-fat diet may be particularly important in these associations, as Sawaya et al. (1998) found that a high-fat diet resulted in greater body fat gains in stunted girls than non-stunted girls after controlling for the effects of energy intake and activity levels in Brazil. Among the Tsimane' communities participating in this study, households were relatively independent of market foods throughout the panel study. Although the pattern is beginning to change, food is primarily produced at the household level and consists of crops such as rice, corn, plantains, and manioc supplemented with wild game, fish, or household domestic animals such as chickens and pigs. Additionally, children and adolescents are active throughout the day, which would influence both muscularity and fatness. Some attend school in the mornings and youths spend the remainder of the day fishing or hunting, playing in groups throughout the community, or assisting parents or older siblings in household duties which may include child-care or working in fields (Aiello, 2013). If the consequences of linear growth retardation differ with context, we might expect that the increases in body fat or BMI for age may occur only when at least one of the double burdens of infection and moderate undernutrition is removed.
A second possible explanation may be population variation in stature. Tsimane' adults are also relatively short and about 40% of Tsimane' adults are classified as stunted when compared with sex and age peers in the US (Godoy et. al., 2010b). Recently several scholars have suggested adaptive explanations for small body size (Perry and Dominy, 2008). Although previous research among Tsimane' suggests catch-up growth is influenced by local ecology (Godoy et al. 2010a), research also suggest that adult stunting does not carry negative consequences for socioeconomic indicators of well-being such as education or income (Godoy et al., 2010b; Undurraga et al., 2012). Additional research is needed to understand the longer-term consequences of shortness or stunting.
A second important finding of this study is that sex appeared to modify the association between stunting and body fatness as assessed through skinfold measurements. When boys and girls were analyzed independently, baseline stunting was associated with both lower age- and sex-adjusted measures of body fat and arm muscularity among girls across a period of 6 years. Among boys, baseline stunting was associated with arm muscularity but the association with skinfold measures of body fatness was not statistically significant at conventional levels of P < 0.05. Although this result should be interpreted with caution in this study, it is consistent with research in Guatemala where women who were stunted early in life had lower amounts of both lean and fat mass than women who had not been stunted, while men who experienced early childhood stunting had adult reductions only in lean mass compared to their non-stunted peers (Li et al., 2003).
Although research among Tsimane' children has consistently found little evidence for disparities between girls and boys with respect to nutritional status, infection, immune system activation, or rates of catch-up growth (Foster et al., 2005; McDade et al., 2005; Godoy et al., 2006; McDade et al., 2008), a few studies have also indicated that there may be sex differences in responses to environmental stressors. Prior research has indicated that environmental conditions during growth, and specifically greater variation in yearly rainfall levels, are associated with reduced adult height of Tsimane' women but not of Tsimane' men (Godoy et al., 2008b). In contrast, the association between climatic conditions and child and adolescent height was less clear as the height of boys 2–12 years of age was more susceptible to climate events than the height of girls of the same age (Godoy et al., 2008a). Life history theory and the developmental origins of health research suggest that boys may be more sensitive to environmental insults than girls, especially in utero (Stinson, 1985; reviewed in Kuzawa and Pike, 2005). Evidence for differential susceptibility to environmental influences after birth is somewhat more conflicting, possibly because of the buffering effects of parental behavior and/or cultural traditions that give preference to boys or girls (reviewed by Stinson, 1985).
Overall, our findings also suggest that additional research examining diet, activity, and the metabolic consequences of stunting in diverse contexts is needed. Work by Hoffman and his colleagues in the shantytowns of Brazil (Schroeder et al., 1999; Hoffman et al., 2000; Martins et al., 2004; Hoffman et al., 2007) and others (Schroeder et al., 1999; Walker et al., 2001; Fernald and Neufeld, 2007;Adair, 2008) have found that child stunting correlates with changes to substrate metabolism, metabolic rate, and blood pressure in children and adolescents. This research suggests that stunted children have a reduced capacity to burn (oxidize) fat and this enhanced fat storage capacity might predispose them to increased body fatness later in life (Grillol et al., 2005; Walker et al., 2007).
A strength of this study is the fact that this is one of only a handful of studies to track body composition in an indigenous group through puberty. Our finding that linear growth stunting at 2–10 years of age is associated with body composition across a 6-year period indicates the importance of considering multiple stages of the growth process. An important shortcoming of this study is that we do not have accurate birth weight data or frequent measures of linear growth or weight gain during the first 2 years of life; therefore, we are unable to evaluate or control for the role of prenatal growth, birth weight, and early postnatal growth. We also do not have data on puberty, which could be an important confounding factor among the oldest age category. Additionally, information on metabolic rates and activity level among children and adolescents is needed to shed light on the underlying mechanism linking growth perturbations to life-long body composition. Finally, rounding error and random measurement error in anthropometric measurements would inflate standard errors and weaken the results. These measurement errors suggest that the inverse association between stunting and later anthropometric measurements of muscularity and skinfold body fat likely underestimates the magnitude of the true relation in this sample.
In sum, these results present a short window of insight into the connection between linear growth and body composition in a rural, indigenous population. We found evidence that linear growth stunting was associated with short-run anthropometric measures of body composition among Tsimane' youth, including lower BMI z-scores and measures of arm muscularity and body fatness. Given the importance of developmental plasticity and the potential for intergenerational effects of linear growth retardation (Kuzawa, 2007), additional research that examines the full consequences of growth stunting is needed to examine the links between nutrition, health, and disease.