Physical Growth Curves of Indigenous Xavante Children in Central Brazil: Results from a Longitudinal Study (2009–2012)

Annals of Human Biology

ISSN: 0301-4460 (Print) 1464-5033 (Online) Journal homepage: http://www.tandfonline.com/loi/iahb20

Physical growth curves of indigenous Xavante children in Central Brazil: results from a longitudinal study (2009–2012)

Aline A. Ferreira, James R. Welch, Geraldo Marcelo Cunha & Carlos E. A. Coimbra Jr.

To cite this article: Aline A. Ferreira, James R. Welch, Geraldo Marcelo Cunha & Carlos E. A. Coimbra Jr. (2016) Physical growth curves of indigenous Xavante children in Central Brazil: results from a longitudinal study (2009–2012), Annals of Human Biology, 43:4, 293-303, DOI: 10.1080/03014460.2016.1195445

To link to this article: http://dx.doi.org/10.1080/03014460.2016.1195445

Accepted author version posted online: 30 May 2016. Published online: 20 Jun 2016.

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Download by: [177.130.50.253] Date: 23 July 2016, At: 04:50 ANNALS OF HUMAN BIOLOGY, 2016 VOL. 43, NO. 4, 293–303 http://dx.doi.org/10.1080/03014460.2016.1195445

RESEARCH PAPER Physical growth curves of indigenous Xavante children in Central Brazil: results from a longitudinal study (2009–2012)

Aline A. Ferreiraa , James R. Welchb , Geraldo Marcelo Cunhab and Carlos E. A. Coimbra Jr.b aInstituto de Nutric¸~ao Josue de Castro, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil; bEscola Nacional de Saude Publica, Fundac¸~ao Oswaldo Cruz, Rio de Janeiro, RJ, Brazil

ABSTRACT ARTICLE HISTORY Background: The nutritional profile of Indigenous children in Brazil is comparable to those observed in Received 14 December 2015 some of the least developed regions of the world. Revised 16 May 2016 Aim: Weight and height growth curves were characterised based on longitudinal data from a local Accepted 23 May 2016 Indigenous population experiencing the double burden of child under-nutrition and adult obesity. Published online 15 June 2016 Subjects and methods: Anthropometric data were collected in six waves from 2009–2011 for children <10 in two proximate Xavante villages in Central Brazil. Prevalence rates for stunting, wasting and thin- KEYWORDS ness were calculated using WHO references. Weight and height data were adjusted for generalised Nutritional assessment; body additive mixed models to generate growth curves. height; body weight; Results: Prevalence rates of stunting and wasting were high, but cases of thinness and excess weight malnutrition/epidemiology; were negligible. Weight and height began close to WHO medians, but fell substantially before 12 health status disparities months. Boys but not girls were able to catch-up in weight before age 10. From 3–10 years, height for both sexes remained between 2 and 0 z-scores. Conclusion: Impaired Xavante growth before 1 year followed by inconsistent recovery before 10 years reflects health and wellbeing disparities with regard to the Brazilian national population and a complex epidemiology of growth involving rapid nutritional change.

Introduction Indigenous peoples’ health, child under-nutrition is more prevalent in Indigenous populations than national benchmark Understanding human growth variation in different global populations in Brazil, Australia, China, Chile, Colombia, India populations and regions is an important field of research in and Pakistan (Anderson et al., 2016). Some countries with human biology, as well as epidemiology and public health large Indigenous populations that figure importantly in the (Bogin, 2001; Eveleth & Tanner, 1976; Stinson, 2012; Tanner, international health literature, such as Canada, the US, 1986; WHO, 1995, 2006). Many developing countries, such as Australia and New Zealand, currently receive more attention Brazil, have invested considerable resources in large-scale for high prevalence of child obesity, as opposed to under- studies to describe national and local growth and develop- nutrition (Gill et al., 2009; Howe et al., 2015). Nuanced Downloaded by [177.130.50.253] at 04:50 23 July 2016 ment patterns and, thereby, establish baseline data, assess description of growth dynamics among Indigenous children child health and nutrition programmes and identify vulner- has the potential to identify how this process evolves after able populations (Monteiro et al., 2010). These efforts have birth and, thereby, help ascertain the unique nutritional chal- contributed to important international and national advances lenges they face as adolescence approaches. in policies directed towards health, nutrition and food security Despite logistical and financial obstacles, research into the (Jones, 2015; Kuhnlein et al., 2013). Unfortunately, such stud- physical growth patterns of Indigenous children in South ies in Brazil have not yet specifically contemplated America has increased substantially over the last three deca- Indigenous peoples, despite ample evidence generated des. Such investigations, almost entirely cross-sectional, tend through community studies among different ethnic groups to show high prevalence rates of under-nutrition, expressed that childhood malnutrition persists in association with rapid primarily through linear growth deficit in relation to age. For emergence of excess weight in young adults, thus configuring example, evaluations of Indigenous children’s nutritional sta- a double burden of nutritional disorders in the young age tus for different ethnic groups located in both Andean and groups (Coimbra et al., 2013). This nutritional profile of the lowland regions of South America have repeatedly shown Indigenous population in Brazil is comparable to those high frequencies of height deficits among children under observed in some of the less developed regions of the world, 5 years, irrespective of the reference curves used (Barreto such as southeast Asia, Africa, and Latin America (Fanzo, et al., 2014; Foster et al., 2005; Hodge & Dufour 1991; Larrea 2012; Martınez & Fernandez, 2006; Wong et al., 2015). & Freire, 2002; Orellana et al., 2006; Oyhenart et al., 2003; According to a recent comparative global review of Urlacher et al., 2015; Wilson et al., 2011). Additionally, the first

CONTACT Carlos E. A. Coimbra Jr. [email protected] Escola Nacional de Saude Publica, Fundac¸~ao Oswaldo Cruz, Leopoldo Bulh~oes 1480, Rio de Janeiro, RJ 21041-210, Brazil ß 2016 Informa UK Limited, trading as Taylor & Francis Group 294 A. A. FERREIRA ET AL.

nationwide survey of nutritional status in the Indigenous throughout the population, such as seasonal fluctuations in population in Brazil revealed that 25.7% of children under 5 dietary intake and community episodes of infectious diseases years of age suffered from chronic malnutrition in 2008–2009 such as diarrhoea and pneumonia. (Horta et al., 2013). The objective of this study is to describe and interpret In population-based research on physical growth, particu- physical growth patterns among Indigenous children from larly when carried out in contexts marked by high prevalence two Xavante (auto-denominated A’uwe)~ villages in Central of chronic under-nutrition, a key issue is to determine at Brazil based on longitudinal monitoring of children under 10 what ages children’s growth starts faltering in comparison to years of age from 2009–2011. The Xavante’s socio- expectations. For the general population in Brazil and South environmental context is marked by recent and rapid America, the scientific literature suggests that, immediately ecological, economic and epidemiological change, with direct following weaning, around the 12th month of life, children impacts on the nutritional status of children and adults start to interact more directly with their environmental sur- (Coimbra Jr et al., 2002; Ferreira et al., 2012; Welch et al., roundings and, therefore, begin to accumulate linear growth 2009). Studies conducted among children in different Xavante deficits (Leroy et al., 2014). Although numerous community communities beginning in the 1990s have called attention to studies have documented grave nutritional profiles among the importance of nutritional disorders, including weight and Indigenous children in Brazil, previously published studies of height deficits, as well as anaemia (Coimbra Jr et al., 2002; child growth were based on cross-sectional data, which pre- Ferreira et al., 2012; Gugelmin & Santos, 2001; Leite et al., sent important limitations, including imprecision due to small 2006). The Xavante population also has high levels of infant sample sizes and vulnerability to momentary or cyclical envir- mortality, averaging 96.7/1000 in the period 1999–2004 onmental circumstances (see Coimbra et al. (2013) and Horta (Souza et al., 2011) and high incidence of preventable infec- et al. (2013) for a review). Longitudinal research with the tious diseases such as diarrhoea, pneumonia and tuberculosis methodological potential to precisely describe growth dynam- (Basta et al., 2010; Lunardi et al., 2007). With this study, we ics in small populations, such as local Indigenous commun- provide more precise and nuanced growth data than were ities, has not previously been undertaken in Brazil. previously available for any Indigenous group in Brazil and, Although some divergence persists between the fields of thereby, hope to advance scientific understanding of the human biology and epidemiology in how international child growth dynamics contributing to the double burden of growth curves are interpreted in relation to local and espe- child under-nutrition and adult obesity among Indigenous cially Indigenous populations, the prevailing view in public people in South America and, in particular, Brazil. health is that child growth patterns in a population tend to be more heavily influenced by social and environmental context than by biological inheritance (Bogin, 2001; Eveleth & Population and methods Tanner 1976; Stinson, 2012; Tanner, 1986). This is because evi- Background dence accumulated in recent decades demonstrates that child growth patterns in a given population of any ethnic or racial The Xavante are among the larger ethnic groups in Brazil, composition is influenced by a multitude of environmental with a population of 15 000 living in nine Indigenous factors related to the home and the community setting, reserves (Welch et al., 2013). The tropical landscape is domi- including type of housing, sanitation, education, access to nated by cerrado vegetation and has average annual temper- health and food security services and other socioeconomic atures of 20–22 C. Although the cerrado, a tropical savanna

Downloaded by [177.130.50.253] at 04:50 23 July 2016 factors (Bogin & Loucky, 1997; Graitcer & Gentry, 1981; landscape, shares some biological and ecological features Habicht et al., 1974). with Amazonian tropical rainforests, it has considerably The leading longitudinal study on growth and develop- greater seasonal variation in temperatures and rainfall, greater ment in Brazil accompanies multiple cohorts of children born overall biodiversity and more geographically dispersed plant in the southern city of Pelotas since 1982 (Victora & Barros, and animal resources (Oliveira & Marquis, 2002). Pimentel 2006; Victora et al., 2000). The importance of this project led Barbosa Indigenous Reserve is the largest Xavante reserve, to its inclusion in the global sample, comprising the current with an area of 328 966 ha. In 2009, the villages Pimentel international growth curves recommended by the World Barbosa and Etenhiritip^ a, which comprise the study popula- Health Organization (WHO, 2006). This study’s objectives were tion for this investigation, had total populations of 332 and not limited to generating growth curves, but its main value 306, respectively (Welch et al., 2013). for this purpose derives from the longitudinal nature of its Like many other Ge-speaking^ Indigenous groups in Brazil, data and application of appropriate analytical techniques. the Xavante were considered semi-nomadic by early observ- Although it is possible to construct growth curves based on ers because they depended more on gathering and hunting cross-sectional data (e.g. Guedes et al., 2010; Silva et al., than gardening during most of the year (Maybury-Lewis, 2012), longitudinal studies with multiple measurements of the 1967; Welch et al., 2013). After prolonged contact with non- same children in a single population are able to more accur- Indigenous Brazilian society and confinement within relatively ately describe the population’s growth trajectory (Song et al., small Indigenous reserves, particularly since the late 1960s, 2012). Furthermore, longitudinal data are particularly useful the Xavante subsequently became increasingly sedentary and for constructing child growth curves for small-scale societies came to depend more on agriculture for food production. because they help reduce possible impacts from short-term The populations now residing in Pimentel Barbosa and local events, with the potential to impact child growth Etenhiritip^ a villages settled in their current approximate ANNALS OF HUMAN BIOLOGY 295

locations in the early 1970s due to pressures by governmen- The results presented here are based on six data collec- tal agencies to vacate their previously expansive territory in tion waves conducted in July 2009, January and July 2010, order to facilitate settlement by large-scale ranches (Welch January and July 2011 and January 2012. All children under et al., 2013). Especially after economic development projects 10 years of age resident in the two villages during any col- promoted by the federal government in the 1970s and 1980s, lection wave were allowed to enter or exit the study at any rice became the Xavante’s principal staple crop (Coimbra Jr time. Possible reasons for a child entering the study after et al., 2002; Flowers, 1983). Currently, they also depend on the first wave or exiting before the last included birth, market resources to meet dietary and other needs. Sugar, cof- death, relocation to or from the study villages and parents’ fee, salt, pasta, soft drinks, crackers and cooking oil are now decision to not participate in one or more waves. regular items in the typical Xavante diet (Coimbra Jr et al., Additionally, a child was automatically unenrolled from the 2002; Welch et al., 2009). In addition, they now have access study upon reaching 10 years of age. The number of meas- to increasingly diverse sources of monetary income, including urements varied through time (unbalanced data), as did the salaried employment and social benefits, which further con- intervals between data points for some children (temporally tribute to reliance on purchased food items. unstructured data). Thus, different numbers of children were Despite these notable historical changes, the Xavante of evaluated a maximum of six times (during all data collection Pimentel Barbosa Indigenous Reserve maintain considerable waves) through to the minimum of one time (during only social and economic continuity with the past, including strong cultural emphasis on traditional forms of social organ- one wave). Birthdates were obtained from healthcare records in the isation, such as multiple systems of age sets and classes, and a busy ritual calendar (Maybury-Lewis, 1967; Welch, 2010, possession of parents or guardians or, alternatively, local 2014). Although they now rely in great measure on rice agri- health services (a village health post). Birth weight data were culture and market food resources, they also continue to also obtained from local health service records, but were gather, hunt and fish for food (Welch et al., 2013). Large excluded from the diachronic dataset used to construct extended family households also continue to be more com- growth curves because they were unavailable for children mon than nuclear family residences (Pereira et al., 2009). born before 2008 and did not follow our measurement Because men tend to live with their wives’ families after mar- protocol. riage (uxorilocal residence), three or more generations of lin- Anthropometric data (weight and height) were sought for eal female relatives (grandmothers, mothers, daughters, etc.) all resident children of both sexes <10 years of age and often live in a single residence. Consequently, young children physically capable of being measured and weighed. are often cared for and fed by multiple aunts, grandmothers Participants’ weight and height measurements were collected and sisters on a daily basis. during home visits by three previously trained and standar- Historically, the two villages included in this study, dised researchers following Lohman et al. (1988). Children Pimentel Barbosa and Etenhiritip^ a, descend from a single 24 months were measured in the recumbent position to Xavante population that inhabited nearby sites since the 0.1 cm accuracy using Seca 416 (Hamburg, Germany) paediat- mid-19th century and settled within the Pimentel Barbosa ric anthropometers. Older children were measured in the Indigenous Reserve in the early 1970s (Welch et al., 2013). standing position to 0.1 cm accuracy using Seca 214 anthrop- They separated from one another only recently (in 2006), ometers. Weight was measured to 0.1 kg accuracy using Seca are located less than 1 kilometre apart and share many 872 portable electronic scales, which include a mother/child Downloaded by [177.130.50.253] at 04:50 23 July 2016 genealogical connections. Furthermore, being located in the function. For all measures, children were asked to be barefoot same ecological and geographical setting, they utilise gen- and wear minimal clothing. erally similar natural food resources and participate in the same local and regional market economies (Welch et al., 2013). Although these villages potentially exhibit slightly dif- Analysis ferent income distributions and food sharing networks, Low birth weight was classified using the WHO cut-off-point these are likely much less marked than any differences of 2500 g (United Nations Children’s Fund & World Health with more distant Xavante villages in the same reserve or elsewhere. Organization, 2004). To assess the significance of missing anthropometric data and evaluate possible effects on statistical analyses, weight and height measurement losses in relation to age for each Research design and fieldwork data collection wave were analysed using the non-parametric The study used a prospective longitudinal methodology in Mann-Whitney U-test for independent samples (significance order to establish temporal relationships for individual partici- level of p 0.05). The same test and significance level were pants and, thereby, generate precise growth curves for the used to evaluate differences between villages. population during the study period. The analyses presented Weight and height means with standard deviations were in this paper do not associate observed patterns with specific calculated for each age group using only the first measure- health outcomes, such as infectious disease episodes or adult ment for each child (from the data collection wave in which obesity, because of the poor quality of local health records the child first participated in the study). Differences between and relatively short duration of the study. mean weight and height values according to sex were 296 A. A. FERREIRA ET AL.

analysed using the Student’s t-test for independent samples Adjusted smoothed curves for weight and height were (significance level of p 0.05). graphically compared to WHO reference curves (De Onis & Z-scores were calculated for height-for-age (HAZ), weight- Onyango, 2008; WHO, 2006) according to sex and age. for-age (WAZ) and body mass index (BMI)-for-age (BAZ) based The software program WHO Anthro version 3.2.2 (World on all observations during the course of the study. For each Health Organization, Geneva, Switzerland) was used to calcu- of these three indices, means and standard deviations were late z-scores for anthropometric indices. The IBM SPSS calculated based on observations of children in age groups Statistics version 21 was used for frequencies and statistical with 12-month intervals. For each age group, prevalence rates tests. R statistical software (R Development Core Team, 2004) for stunting, underweight and wasting were calculated using with gamm4 was used to calculate growth curves. the WHO reference (De Onis et al., 2007; WHO, 2006) and Chi-squared tests (significance level of p 0.05) were applied to verify differences between sexes. Ethics In constructing the longitudinal dataset for construction The present study occurred within larger multidisciplinary of growth curves, no data interpolation technique was used research projects addressing diachronic health transition to replace missing data. Because the actual child growth among the Xavante of Pimentel Barbosa Indigenous Reserve. profile of the Indigenous population in Brazil is not yet The study was approved by the Research Ethics Committee at known and cannot, therefore, be presumed, it was not pos- the National School of Public Health (Escola Nacional de sible to use such models as latent growth curves (Johnson, Saude Publica), Oswaldo Cruz Foundation (Fundac¸~ao Oswaldo 2015). For the same reason, other popular models such as Cruz) and the National Research Ethics Council (Conselho the LMS method for modelling growth (Cole & Green, 1992) Nacional de Etica em Pesquisa). Permission to conduct the and its extension, GAMLSS (Rigby & Stasinopoulos, 2005), study within the Indigenous reserve was authorised by were also inappropriate for our complex data structure. In the National Indian Foundation (Fundac¸~ao Nacional do Indio). order to precisely describe weight and height growth pat- The project was presented to residents and leaders of terns of Xavante children, we considered two inherent fea- Pimentel Barbosa and Etenhiritip^ a villages during community tures of our longitudinal data. First, repeated measurements meetings. Village leaders signed a Collective Prior Informed through time for the same individual should be treated as Consent form on behalf of residents. Parents and guardians correlated. Second, the relationships between weight and were allowed to decline participation on behalf of their chil- height are non-linear, depending on age and other factors. dren and were present for anthropometric measurement. Attending to these features, we adjusted weight and height data for generalised additive mixed models (GAMM), which accommodate random effects to take into account the cor- Results relation structure between repeated measurements in longitudinal studies (Pinheiro & Bates, 2000), and additive effects Based on birth weight records from local health services, with non-parametric smoothing splines (Hastie & Tibshirani, which were only available for 115 children born in 2008 and 1990), to generate free-form curves of growth with respect thereafter, the average Xavante child was born with adequate to age. weight (3181 g; SD ¼ 0.449). Only 5.2% were born with low birth weight (data not shown). We employed the following equation: If yit represents the ith growth outcome at time t, The total number of children <10 years from Pimentel

Downloaded by [177.130.50.253] at 04:50 23 July 2016 Barbosa and Etenhiritip^ a villages evaluated anthropometrically

yit ¼ b0 þ u0i þ sðtÞþeit; at least once (during at least one data collection wave) was 389 (97.7% of the target study population of 398). Of these,

where b0 is the intercept, u0i is the random-mixed effect to 202 (51.9%) were female and 197 (50.6%) resided in Pimentel account for repeated longitudinal measurements of the Barbosa village. The total numbers of anthropometric meas- same individual, stðÞ is a cubic spline function to account urements (observations) performed during the course of the for possible non-linear effects of time (i.e. the effect of time study were 1712 for weight and 1701 for height. Considering is not constrained to be equal across the different levels of only the sub-set of children under 3 years, 199 children growth) and eit is a random Gaussian error (Hastie & (51.2% of the total number of children under 10 years) were Tibshirani, 1990). This statistical approach is similar to that evaluated at least once and 629 weight and height observa- used by Song et al. (2012), with the exception that quad- tions were made. ratic polynomial models of effects of age were replaced by During the first wave of data collection, 274 children spline functions, which are methodologically more extensible (70.6% of all participants) were evaluated. Subsequent recruit- and flexible. This procedure was conducted separately for ment of participants was very consistent. Specifically, 23 chil- each sex using the complete dataset including all measure- dren (5.9%) entered the study during the second wave, 24 ments of children <10 years and the sub-set limited to (6.2%) during the third, 22 (5.7%) during the fourth, 17 (4.4%) measurements of children <3 years. These distinct adjusted during the fifth and 29 (7.5%) during the sixth and final models generated different smoothing splines and, therefore, wave. The number of multiple longitudinal anthropometric produced slightly different curves for the first years of life, observations per child were distributed as follows: 170 chil- with the curve based on observations of children <3 years dren were evaluated the maximum of six times (in all six data being more sensitive for this age group. collection waves), 61 were evaluated five times, 41 were ANNALS OF HUMAN BIOLOGY 297

evaluated four times, 31 were evaluated three times, 33 were Comparing mean weight at first measurement after being evaluated two times and 53 were evaluated once. enrolled in the study between sexes by age group, significant A global total of 96 height and 86 weight observations differences (p 0.05) were observed for children 6 and <24, were not completed throughout the six data collection waves. 36 and <48 and 96 and <108 months of age, with girls Unrealised height observations were due to death (n ¼ 11), showing lower values at all ages (Table 1). Significant differ- declination on behalf of child by parent or guardian (n ¼ 2), ences in mean height between sexes were observed for chil- data recording inconsistency (n ¼ 9) and absence at the time dren 12 and <24, 36 and <48 and 96 and <108 of measurement (n ¼ 74). Unrealised weight observations months of age, with girls showing lower values at all ages. were due to death (n ¼ 11), declination (n ¼ 2), absence Anthropometric indices of nutritional status show high (n ¼ 71) and data inconsistency (n ¼ 2). Data losses between prevalence rates of stunting and underweight among obser- collection waves fluctuated within a small range, with the vations of Xavante children, especially during the first years smallest loss being nine individuals in the first wave (1.2% of of life (Table 2). Measurements of children 12 and <48 participants registered at the time) and the largest being 23 months presented lower mean HAZ and WAZ values than in the third (8.3%). As measured by the Mann-Whitney U-test, those in other age groups and, consequently, higher preva- losses were insignificant for all follow-up waves (data not lence rates of stunting and underweight. For boys in the age shown). group 12 and <24 months, the prevalence of stunting sur- Stratified analyses comparing weight, height, sex and age passed 50%. Only in the age groups <12 months, 36 and showed no significant differences between the two villages, <48 and 108 and <120 were significant differences which were, therefore, treated as a single population in sub- encountered between boys and girls in the prevalence of sequent analyses (data not shown). stunting. Based on the BAZ index, there were very few Mean weight and height for boys and girls of all ages observed cases of wasting (Table 2) and no cases of over- (<10 years) did not differ significantly between the six data weight or obesity at any age (data not shown). collection waves, ranging from 16.1–16.8 kg and 97.1–99.7 cm, Comparing the smoothed weight growth curves derived respectively (data not shown). from longitudinal observations of Xavante children <10 years

Table 1. Mean weight and height of Xavante boys and girls <10 years at first measurement, by age group, 2009–2012, Pimentel Barbosa and Et^enhiritipa Villages, Brazil. Weight Height Boys Girls Boys Girls Age (months) n Mean (SD) n Mean (SD) p-value n Mean (SD) n Mean (SD) p-value <6 52 5.9 (1.5) 48 5.7 (1.5) 0.548 52 59.7 (5.5) 48 58.8 (5.9) 0.450 6 and <12 14 8.2 (0.6) 14 7.3 (1.2) 0.027 14 69.1 (1.8) 14 67.1 (3.7) 0.082 12 and <24 14 10.9 (3.6) 23 8.6 (1.2) 0.014 14 79.7 (6.3) 23 74.2 (4.0) 0.044 24 and <36 20 12.4 (1.1) 13 12.1 (1.1) 0.563 20 85.3 (3.1) 13 85.3 (4.4) 0.960 36 and <48 15 15.6 (1.4) 20 14.0 (1.2) 0.003 15 95.8 (3.8) 20 92.7 (3.2) 0.015 48 and <60 9 16.7 (1.1) 20 16.7 (1.7) 0.492 9 101.5 (2.0) 20 102.9 (3.9) 0.322 60 and <72 14 18.0 (1.8) 13 17.8 (1.5) 0.742 14 107.1 (3.9) 13 106.1 (2.5) 0.449 72 and <84 12 20.2 (2.1) 11 19.3 (1.7) 0.306 12 113.7 (4.3) 11 111.5 (5.6) 0.307 84 and <96 18 24.3 (3.1) 13 23.8 (2.6) 0.622 18 120.6 (4.8) 13 121.1 (5.1) 0.773 96 and <108 7 26.3 (1.0) 13 24.2 (2.1) 0.025 7 126.0 (1.8) 13 122.2 (4.2) 0.035

Downloaded by [177.130.50.253] at 04:50 23 July 2016 108 and <120 12 29.9 (2.0) 14 29.7 (5.9) 0.903 12 132.1 (3.3) 14 130.5 (7.9) 0.519 Total 187 202 187 202 SD: standard deviation.

Table 2. Mean z-scores for height-for-age (HAZ), weight-for-age (WAZ) and BMI-for-age (BAZ), with prevalence rates of stunting, underweight and wasting, based on observations of Xavante boys and girls <10 years, 2009–2012, Pimentel Barbosa and Et^enhiritipa Villages, Brazil. HAZ WAZ BAZ Boys Girls Boys Girls Boys Girls Mean Stunting Mean Stunting Underweight Mean Underweight Mean Wasting Mean Wasting Age (months) (SD) (%) (SD) (%) Mean (SD) (%) (SD) (%) (SD) (%) (SD) (%) <12 1.2 (1.2) 24.8* 0.9 (1.2) 12.4* 0.8 (1.1) 15.6 0.6 (1.2) 11.3 0.2 (0.9) 3.7 0.1 (1.0) 2.1 12 and <24 2.0 (1.2) 51.9 1.9 (1.0) 43.1 1.1 (1.0) 20.6 1.1 (1.1) 17.4 0.0 (1.0) 2.9 0.1 (0.9) 2.0 24 and <36 1.7 (0.9) 43.4 1.9 (1.1) 40.8 0.7 (0.9) 7.2 0.6 (0.7) 13.3 0.5 (0.8) 1.5 0.5 (0.7) 0.0 36 and <48 1.3 (0.8) 21.5* 1.7 (0.9) 35.4* 0.3 (0.9) 3.2 0.6 (0.7) 3.3 0.6 (0.8) 0.0 0.6 (0.7) 0.0 48 and <60 1.0 (0.7) 5.9 1.2 (0.7) 9.3 0.2 (0.7) 0.0 0.5 (0.6) 1.2 0.6 (0.8) 0.0 0.4 (0.5) 0.0 60 and <72 0.9 (0.8) 8.9 0.9 (0.7) 5.1 0.2 (0.8) 0.0 0.4 (0.7) 0.0 0.5 (0.8) 0.0 0.3 (0.5) 0.0 72 and <84 0.8 (0.7) 5.5 0.8 (0.7) 5.6 0.3 (0.6) 0.0 0.4 (0.7) 1.2 0.3 (0.6) 0.0 0.2 (0.6) 0.0 84 and <96 0.8 (0.8) 6.2 0.8 (0.8) 6.0 0.3 (0.7) 0.0 0.4 (0.6) 1.5 0.4 (0.6) 0.0 0.1 (0.6) 0.0 96 and <108 0.7 (0.7) 3.0 0.9 (0.8) 8.7 0.1 (0.7) 1.5 0.5 (0.8) 2.9 0.4 (0.7) 1.8 0.1 (0.6) 0.0 108 and <120 0.7 (0.7) 3.1* 0.9 (0.9) 9.9* 0.0 (0.6) 0.0 0.4 (0.9) 4.5 0.6 (0.6) 0.0 0.2 (0.7) 0.0 All 1.2 (1.0) 20.4 1.2 (1.0) 18.7 0.5 (0.9) 5.9 0.6 (0.9) 6.0 0.4 (0.8) 1.1 0.2 (0.8) 0.6 BMI: body mass index; SD: standard deviation. *p-value 0.05. 298 A. A. FERREIRA ET AL.

(A) (A) ht (kg) ht ig e Weight (kg) Weight W

Xavante growth curve Xavante growth curve 0 z-scores 0 z-scores +2 and -2 z-scores +2 and -2 z-scores 051015 051015

0 5 10 15 20 25 30 35 0 5 10 15 20 25 30 35 Age (months) Age (months)

(B) (B) 25 30 35 0 2 20 25 30 35 5 5 1 Weight (kg) Weight (kg)

Xavante growth curve Xavante growth curve 0 z-scores 0 z-scores +2 and -2 z-scores 510 +2 and -2 z-scores 0 05101

0 20406080100120 0 20 40 60 80 100 120 Age (months) Age (months) Figure 1. Smoothed weight growth curves with confidence intervals (grey shad- Figure 2. Smoothed weight growth curves with confidence intervals (grey shad- ing) for Indigenous Xavante boys (A) < 3 and (B) < 10 years, compared to 2, 0 ing) for Indigenous Xavante girls (A) < 3 and (B) < 10 years, compared to 2, 0 and þ2 z-scores of the WHO reference population, 2009–2012, Pimentel Barbosa and þ2 z-scores of the WHO reference population, 2009–2012, Pimentel Barbosa and Et^enhiritipa Villages, Brazil. Downloaded by [177.130.50.253] at 04:50 23 July 2016 and Et^enhiritipa Villages, Brazil.

At no point after the first months of life did the upper confidence interval of Xavante linear growth surpass the with the World Health Organization reference curves, it is observed that weight-for-age remained below the WHO refer- median WHO reference curves (Figures 3(A) and 4(A)). In simi- ence population median for both sexes at almost all ages lar fashion to the pattern observed in their weight curves, (Figures 1 and 2). For both sexes, this measure began very boys’ and girls’ height-for-age began close to the median, but close to the median (Figures 1(A) and 2(A)). Subsequently, the failed to keep up, beginning 6–8 months, subsequently weight curves followed inconsistent ascent patterns, failing to oscillating close to 2 z-scores before 3 years. Thereafter, maintain their initial positions near the 0 z-score before the boys’ and girls’ height growth curves improved somewhat, end of the first year. By the end of the third year of life, the following intermediate trajectories above 2 z-scores, but curves for both sexes were substantially lower with respect to never reaching the 0 z-score of the WHO reference before the reference median than they were at birth, but remained age 10 (Figures 3(B) and 4(B)). above 2 z-scores (reference population threshold for underweight). Beginning at 8 years of age, boys’ weight-for-age Discussion and conclusion followed a trajectory close to or slightly above the 0 z-score of the WHO reference (Figure 1(B)). Girls’ weight growth Prevalence rates of stunting among Xavante boys (20.4%) and curves remained under the 0 z-score at all ages (Figure 2(B)). girls (18.7%) were slightly lower than observed in Brazil’s Thus, considering their respective confidence intervals and Indigenous population nationally (25.7%), but higher than reference curves, Xavante boys but not girls were able to was documented in the northeast region (13.9%) (Horta et al., catch-up in weight by age 10. 2013). Case studies of specific ethnic groups in Brazil have ANNALS OF HUMAN BIOLOGY 299

(A) (A) 100 110 t (cm) Heigh Height (cm)

Xavante growth curve Xavante growth curve 0 z-scores 0 z-scores +2 and -2 z-scores +2 and -2 z-scores -3 z-scores -3 z-scores 40 50 60 70 80 90 100 110 50 60 70 80 90

0 5 10 15 20 25 30 35 0 5 10 15 20 25 30 35 Age (months) Age (months)

(B) (B) 20 140 01 0 1 Height (cm) Height (cm) 0

Xavante growth curve Xavante growth curve 60 8 0 z-scores 0 z-scores +2 and -2 z-scores +2 and -2 z-scores -3 z-scores -3 z-scores 0 40 60 80 100 120 140 4

0 20406080100120 0 20 40 60 80 100 120 Age (months) Age (months) Figure 3. Smoothed height growth curves with confidence intervals (grey shad- Figure 4. Smoothed height growth curves with confidence intervals (grey shad- ing) for Indigenous Xavante boys (A) < 3 and (B) < 10 years, compared to 3, ing) for Indigenous Xavante girls (A) < 3 and (B) < 10 years, compared to 3, 2, 0 and þ2 z-scores of the WHO reference population, 2009–2012, Pimentel 2, 0 and þ2 z-scores of the WHO reference population, 2009–2012, Pimentel Barbosa and Et^enhiritipa Villages, Brazil. Barbosa and Et^enhiritipa Villages, Brazil. Downloaded by [177.130.50.253] at 04:50 23 July 2016

revealed even more discouraging nutritional scenarios in Eveleth & Tanner, 1976; Stinson, 2012). From a public health recent decades, with nutritional deficit frequencies often nutrition perspective, an alert situation is indicated when a exceeding one-fifth of children under 5 years (Barreto et al., population’s child growth curves show little inclination or, 2014; Morais et al., 2003). For example, recent studies in worse, flat or downward slopes. Such conditions suggest Amazonia and Central Brazil have shown high prevalence broad patterns of compromised housing, food security and rates of stunting among the Wari’ (61.7%), Suruı (38.6%), overall health and wellbeing (Ashworth et al., 2008; Tanner, Guarani-Kaiowa (34.1%) and Upper Xingu ethnic groups 1986). (21.7%) (Leite et al., 2007; Mondini et al., 2009; Orellana et al., The present study shows that Xavante children are born 2006;Pıcoli et al., 2006). Despite these variations within the relatively well. Xavante children are born weighing 3181 g on country’s Indigenous population, stunting among the Xavante average, which is above the cut-off for low-weight and near is dramatically higher than reported for non-Indigenous chil- the national average of 3500 g for the Indigenous population dren in Brazil (7.1%) in 2006 (Ministerio da Saude, 2009). in Brazil (ABRASCO, 2010). The prevalence of low birth weight Growth curves of Xavante children show unstable height was 5.2% of the total of 117 births recorded between and weight growth, especially at younger ages. In other 2008–2012. According to growth curves, Xavante children words, curves showed more pronounced upward inclination were close to the median WHO reference curves for weight- at certain ages and notable stagnation at others. for-age and height-for-age. Consistent with our results, several Theoretically, the growth curve slope for children in any studies conducted among Indigenous peoples in South given population should be consistently upwardly sloped, America (Amigo et al., 2010; Cardoso et al., 2013; Sirio et al., increasing in pace with the reference curve (Bogin, 2001; 2015) suggest low birth weight is often below 15%. 300 A. A. FERREIRA ET AL.

However, soon after birth the Xavante weight and height Rapid socioeconomic and ecological changes in conjunc- growth curves for boys and girls fluctuated. From the 6th to tion with the maintenance of many traditional subsistence 36th month of life, Xavante boys’ and girls’ linear growth practices have transformed many aspects of the context in remained below the median WHO reference curves, reaching which Xavante children grow up (Coimbra Jr. et al., 2002; as low as the 2 z-scores. Similar patterns during the first 3 Flowers, 2014; Santos et al., 1997). With increased access to years and often persisting until 5 years, are widely docu- sources of monetary income, Xavante households are now mented throughout the developing world (Prentice et al., more involved in the market economy and, consequently, 2013). This performance is worrying, because the first 3 years rely more on external sources of food than in the past. of life are precisely when children should undergo acceler- Previous studies have shown this recent dynamic to involve ated linear growth. There is consensus in the epidemiological an internal process of socioeconomic differentiation with literature that impaired linear growth during childhood can negative consequences for Xavante dietary patterns and be very difficult to catch up, even with adequate food supple- nutritional status (Ferreira et al., 2012; Welch et al., 2009). mentation (Bogin, 2001; Golden, 1998). However, it remains unclear whether reduced access to trad- The first 3 years of life involve high biological and environ- itional landscape resources diminishes dietary health or mental vulnerability, as evidenced by higher prevalence rates increased access to market resources improves growth among of height deficit and weight fluctuations, as well as greater children. Because nutritional health is a complex problem, burden of morbidity and mortality from infectious and para- both scenarios are simultaneously possible. sitic diseases associated with poor sanitation and limited Sectional studies in different Xavante communities since access to safe water sources for drinking and food prepar- the 1990s have highlighted the relevance of nutritional and ation (Ashworth et al., 2008; Caulfield et al., 2006). According metabolic disorders, including high prevalence rates of to Martorell (1999), height and especially weight growth may anaemia and height deficits in children in conjunction with fluctuate more widely during the first year of life. Children excess weight and type 2 diabetes mellitus in adults (Coimbra who experienced more intense fluctuations often continue to Jr et al., 2002; Dal Fabbro et al., 2014; Ferreira et al., 2012; suffer abrupt growth variations in the second or third year of Gugelmin & Santos, 2001, 2006; Leite et al., 2006; Welch et al., life and, therefore, tend to exhibit low weight gain or low 2009). In 2006, in the same Xavante villages included in the height-for-age as compared to reference populations. For present study, the prevalence rates of chronic undernutrition example, a study of Australian Indigenous children emphas- and low weight-for-age among children <10 were 29.9% and ised the first 3 years as the period of most diminished weight 4.5%, respectively (Ferreira et al., 2012). The prevalence of growth (Gracey, 2000). A similar dynamic may partly explain overweight and obesity in adults (> 20 years) was 75.6% in the high variability in Xavante growth curves observed during the same year (Welch et al., 2009). the first 3 years of life. This double nutrition burden of child under-nutrition, sim- Our results show that, after 3 years, Xavante boys and girls ultaneously coupled with excess weight in adolescence and begin to show improvement in weight and height relative to early adulthood, which the Xavante are currently experienc- the WHO reference, but only boys’ weight-for-age recovered ing, is an enormous challenge for healthcare services directed by surpassing the WHO reference median by age 10. Height towards indigenous people in Brazil. The country’s Universal catch-up before 10 years was also documented among Healthcare System, including the Indigenous Healthcare sub- Tsimane’ children in the Bolivian Amazon, especially in vil- system, has clear limitations in dealing with the complexity of lages located in more remote locations (Godoy et al., 2010). this phenomenon, for which there is no single causal explan-

Downloaded by [177.130.50.253] at 04:50 23 July 2016 The co-existence of poorer growth during the first years of ation. To date, the few nutritional interventions implemented life with improving trajectories after 3 years points to the by the Indigenous sub-system in Brazil have emphasised pre- complex epidemiology of growth, especially in Indigenous vention or control of specific nutritional deficiencies, espe- populations experiencing socioecomomic and environmental cially during childhood and pregnancy, by means of food change. provisioning and iron sulphate supplementation performed Although discussions continue about the applicability of irregularly and according to questionable technical criteria universal standards for comparison of growth and growth (Caldas & Santos, 2012; Horta et al., 2013; Leite et al., 2013). potential between different ethnic groups, precarious sani- Unfortunately, these national healthcare systems have not yet tation conditions and food insecurity present in Xavante implemented measures that appropriately recognise that villages (Coimbra Jr. et al., 2002) help explain poor growth under-nutrition in conjunction with over-nutrition in a single performance among Xavante children, especially during the population indicates a single emergent process involving a first years of life. Child growth directly reflects past and complex interplay of socioeconomic, political, cultural and present living conditions related to diet and, more broadly, biological dimensions (Batista-Filho et al., 2008; Doak et al., the overall living environment (Bogin, 2001; Martorell, 2004; Victora et al., 2008). 1999; Stinson, 2012; Tanner, 1986). Substantial evidence The prospective longitudinal methodology used in the pre- indicates that height and weight growth of children who sent study facilitated a precise description of actual growth are well-nourished, healthy and without physiological or patterns while providing the flexibility required for collecting environmental restriction have similar growth until 5 years data in an Indigenous community whose daily and seasonal of age (Bogin, 2001; Eveleth & Tanner, 1976; Graitcer & routines did not necessarily coincide with epidemiological Gentry, 1981; Habicht et al., 1974; Stinson, 2012; WHO, field collection techniques. Nevertheless, the study has limita- 2006). tions due to the inability to collect information in the field on ANNALS OF HUMAN BIOLOGY 301

important factors associated with under-nutrition in children, Geraldo Marcelo Cunha http://orcid.org/0000-0001-7128- such as morbidity from diarrhoea and acute respiratory infec- 933X tions, breastfeeding and other feeding patterns during Carlos E. A. Coimbra Jr. http://orcid.org/0000-0003-4085- infancy, as well as mothers’ diet and other nutritional and 1080 health conditions during pregnancy. Another restriction of the study was loss due to absence of study subjects at home during field data collection, which may have reduced the References sociodemographic and age composition of the study population. Future studies using similar methodologies should con- Amigo H, Bustos P, Kaufman JS. 2010. Absence of disparities in anthropo- sider reducing time intervals between data collection waves metric measures among Chilean indigenous and non-indigenous newborns. BMC Public Health 10:392. in order to collect more detailed records of weight and Anderson I, Robson B, Connolly M, Al-Yaman F, Bjertness E, height growth, as well as comorbidities. King A, et al. 2016. Indigenous and tribal peoples’ health (The The data reported here indicate major disparities in the Lancet–Lowitja Institute Global Collaboration): a population growth of Xavante children as compared to the non- study. Lancet, Online First, http://dx.doi.org/10.1016/S0140- Indigenous population. Considering the Brazilian national con- 6736(16)00345-7. Ashworth A, Shrimpton R, Jamil K. 2008. Growth monitoring and promo- text, characterised by weight curves for both sexes that tion: review of evidence of impact. Matern Child Nutr exceed the WHO international reference medians at all ages, 4(Suppl 1):86–117. Xavante child growth is substantially worse. The linear growth Associaç~ao Brasileira de Pos-Graduac ¸~ao em Saude Coletiva (ABRASCO). pattern among non-Indigenous children in Brazil also accom- 2010. Inquerito Nacional de Saude e Nutriç~ao dos Povos Indıgenas. panies the WHO reference, even in regions considered under- Relatorio Final. Rio de Janeiro: ABRASCO. Barreto CTG, Cardoso AM, Coimbra CEA, Jr. 2014. Estado nutricional de privileged or vulnerable, such as rural areas (IBGE, 2010; crianças indıgenas Guarani nos estados do Rio de Janeiro e S~ao Paulo, Monteiro et al., 2010). Brasil. Cad Saude Publica 30:657–662. Because chronic under-nutrition can affect cognitive devel- Basta PC, Coimbra CEA, Jr, Welch JR, Alves LCC, Santos RV, Camacho LAB. opment and increases risk of excess weight and associated 2010. Tuberculosis among the Xavante Indians of the Brazilian metabolic diseases in adulthood (Victora et al., 2008), its broad Amazon: an epidemiological and ethnographic assessment. Ann Hum Biol 37:643–657. impacts within disproportionally affected populations can Batista-Filho M, Souza AI, Miglioli TC, Santos MC. 2008. Anemia e obesi- be important. In 2000, the United Nations Millennium dade: um paradoxo da transiç~ao nutricional brasileira. Cad Saude Development Goals established a goal of halving the preva- Publica 24(Suppl 2):S247–S257. lence of under-weight children under 5 years in the develop- Bogin B. 2001. The growth of humanity. New York: Wiley-Liss. Bogin B, Loucky J. 1997. Plasticity, political economy, and physical growth ing world between 1990–2015. Among the signatory countries status of Guatemala Maya children living in the United States. Am J to this initiative, Brazil stood out for over-reaching this and Phys Anthropol 102:17–32. other goals set out in the same document well before the end Caldas ADR, Santos RV. 2012. Vigilância alimentar e nutricional para os of this period (Ministerio da Saude, 2010; United Nations, povos indıgenas no Brasil: analise da construç~ao de uma polıtica 2015). Unfortunately, as illustrated by the present study, the publica em saude. Physis 22:545–565. Cardoso AM, Coimbra CEA, Jr, Werneck GL. 2013. Risk factors for hospital health and social well-being advances obtained for the admission due to acute lower respiratory tract infection in Guarani Brazilian population have not adequately reached Indigenous indigenous children in southern Brazil: a population-based case-control children, who continue to experience elevated rates of infant study. Trop Med Int Health 18:596–607.

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