Physical growth in the first year of life of Terena Indigenous children living in an urban zone: longitudinal study

Deise Bresan Maurício Soares Leite Aline Alves Ferreira Elenir Rose Jardim Cury About the authors

Abstract

The present study aimed to assess the anthropometric nutrition status and physical growth of Terena Indigenous children living in an urban zone of the city of Campo Grande, Mato Grosso do Sul, Brazil, in their first year of life. Children who were born between June 2017 and July 2018 (n = 42) participated in the study. In total, 4.8% of the children presented a low height for age (H/A) in the 12th month of life. According to body mass index (BMI) for age, overweight affected 15.0% of the individuals belonging to the female sex at the age of 12 months, and obesity was observed in 4.8% of the children belonging to both sexes at this same age. Terena Indigenous children’s length curve failed to reach the median value recorded for the reference population. Weight and body mass index curves for age, mainly among individuals belonging to the female sex, were often above the reference median value. The Terena growth curves recorded an average linear growth of lower than expected and a weight gain of higher than the reference median. This profile is compatible with the persistence of unfavorable conditions for children’s growth and nutrition, as well as with an accelerated process of food and nutritional transition, where the racial dimension of health inequities cannot be disregarded.

Key words:
Indigenous peoples; Anthropometry; Child

Introduction

Studies with Indigenous people around the world have indicated a high prevalence of malnutrition11 Anderson I, Robson B, Connolly M, Al-Yaman F, Bjertness E, King A, Tynan M, Madden R, Bang A, Coimbra CE Jr, Pesantes MA, Amigo H, Andronov S, Armien B, Obando DA, Axelsson P, Bhatti ZS, Bhutta ZA, Bjerregaard P, Bjertness MB, Briceno-Leon R, Broderstad AR, Bustos P, Chongsuvivatwong V, Chu J, Deji, Gouda J, Harikumar R, Htay TT, Htet AS, Izugbara C, Kamaka M, King M, Kodavanti MR, Lara M, Laxmaiah A, Lema C, Taborda AM, Liabsuetrakul T, Lobanov A, Melhus M, Meshram I, Miranda JJ, Mu TT, Nagalla B, Nimmathota A, Popov AI, Poveda AM, Ram F, Reich H, Santos RV, Sein AA, Shekhar C, Sherpa LY, Skold P, Tano S, Tanywe A, Ugwu C, Ugwu F, Vapattanawong P, Wan X, Welch JR, Yang G, Yang Z, Yap L. Indigenous and tribal peoples' health (The Lancet-Lowitja Institute Global Collaboration): a population study. Lancet 2016; 388(10040):131-157.

2 Gracey M, King M. Indigenous health part 1: determinants and disease patterns. Lancet 2009; 374(9683):65-75.
-33 Montenegro RA, Stephens C. Indigenous health in Latin America and the Caribbean. Lancet 2006; 367(9525):1859-1869.. In Latin America in particular, they have very high frequencies of low height for age (H/A), in addition to other nutritional issues11 Anderson I, Robson B, Connolly M, Al-Yaman F, Bjertness E, King A, Tynan M, Madden R, Bang A, Coimbra CE Jr, Pesantes MA, Amigo H, Andronov S, Armien B, Obando DA, Axelsson P, Bhatti ZS, Bhutta ZA, Bjerregaard P, Bjertness MB, Briceno-Leon R, Broderstad AR, Bustos P, Chongsuvivatwong V, Chu J, Deji, Gouda J, Harikumar R, Htay TT, Htet AS, Izugbara C, Kamaka M, King M, Kodavanti MR, Lara M, Laxmaiah A, Lema C, Taborda AM, Liabsuetrakul T, Lobanov A, Melhus M, Meshram I, Miranda JJ, Mu TT, Nagalla B, Nimmathota A, Popov AI, Poveda AM, Ram F, Reich H, Santos RV, Sein AA, Shekhar C, Sherpa LY, Skold P, Tano S, Tanywe A, Ugwu C, Ugwu F, Vapattanawong P, Wan X, Welch JR, Yang G, Yang Z, Yap L. Indigenous and tribal peoples' health (The Lancet-Lowitja Institute Global Collaboration): a population study. Lancet 2016; 388(10040):131-157.,33 Montenegro RA, Stephens C. Indigenous health in Latin America and the Caribbean. Lancet 2006; 367(9525):1859-1869.. In Brazil, Indigenous children are also affected by the high prevalence of anthropometric deficits, in addition to high rates of infant mortality, anemia, and infectious-parasitic diseases44 Horta BL, Santos RV, Welch JR, Cardoso AM, Santos JV, Assis AM, Lira PC, Coimbra CE Jr. Nutritional status of indigenous children: findings from the First National Survey of Indigenous People's Health and Nutrition in Brazil. Int J Equity Health 2013; 12:23.

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Low H/A affected 25.7% of all Indigenous children under 5 years of age in Brazil in 2009, a value much higher than that recorded among non-Indigenous children44 Horta BL, Santos RV, Welch JR, Cardoso AM, Santos JV, Assis AM, Lira PC, Coimbra CE Jr. Nutritional status of indigenous children: findings from the First National Survey of Indigenous People's Health and Nutrition in Brazil. Int J Equity Health 2013; 12:23.,88 Universidade Federal do Rio de Janeiro. Estado nutricional antropométrico da criança e da mãe: prevalência de indicadores antropométrico de crianças brasileiras menores de 5 anos de idade e suas mães biológicas. Rio de Janeiro: UFRJ; 2022.. Regional, age, and ethnic variations may reach even higher frequencies99 Barreto CTG, Cardoso AM, Coimbra Jr CEA. Nutritional status of Guarani indigenous children in the States of Rio de Janeiro and São Paulo, Brazil. Cad Saude Publica 2014; 30(3):657-662.

10 Ferreira AA, Welch JR, Santos RV, Gugelmin SA, Coimbra Jr CEA. Nutritional status and growth of indigenous Xavante children, Central Brazil. Nutr J 2012; 11:3.

11 Leite MS, Santos RV, Gugelmin SA, Coimbra Jr CEA. Crescimento físico e perfil nutricional da população indígena Xavánte de Sangradouro-Volta Grande, Mato Grosso, Brasil. Cad Saude Publica 2006; 22(2):265-276.

12 Orellana JDY, Marrero L, Alves CLM, Ruiz CMV, Hacon SS, Oliveira MW, Basta PC. Association of severe stunting in indigenous Yanomami children with maternal short stature: clues about the intergerational transmission. Cien Saude Colet 2019; 24(5):1875-1883.
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17 Bresan D, Bastos JL, Leite MS. Epidemiologia da hipertensão arterial em indígenas Kaingang, Terra Indígena Xapecó, Santa Catarina, Brasil, 2013. Cad Saude Publica 2015; 31(2):331-344.

18 Fávaro TR, Santos RV, Cunha GM, Leite IC, Coimbra Jr CEA. Obesidade e excesso de peso em adultos indígenas Xukuru do Ororubá, Pernambuco, Brasil: magnitude, fatores socioeconômicos e demográficos associados. Cad Saude Publica 2015; 31(8):1685-1697.
-1919 Chagas CA, Castro TG, Leite MS, Barroso MAC, Viana M, Beinner MA, Pimenta AM. Prevalência estimada e fatores associados à hipertensão arterial em indígenas adultos Krenak do Estado de Minas Gerais, Brasil. Cad Saude Publica 2020; 36(1):e00206818.. The double burden of malnutrition, in which overweight and low H/A and weight-for-age (W/A) coexist within a population2020 Popkin BM, Corvalan C, Grummer-Strawn LM. Dynamics of the double burden of malnutrition and the changing nutrition reality. Lancet 2020; 395(10217):65-74., is increasingly documented among Indigenous people in other parts of the world2121 Villena-Esponera MP, Moreno-Rojas R, Molina-Recio G. Food insecurity and the double burden of malnutrition of Indigenous refugee Épera Siapidara. J Immigrant Minority Health 2019; 21(5):1035-1042.

22 Ramirez-Zea M, Kroker-Lobos MF, Close-Fernandez R, Kanter R. The double burden of malnutrition in indigenous and nonindigenous Guatemalan populations. Am J Clin Nutr 2014; 100(6):1644S-1651S.
-2323 Wong CY, Zalilah, MS, Chua, EY, Norhasmah S, Chin YS, Nur'Asyura AS. Double-burden of malnutrition among the indigenous peoples (Orang Asli) of Peninsular Malaysia. BMC Public Health 2015; 15:680..

Physical growth in childhood is strongly influenced by the living conditions to which children are subjected. Environmental factors, such as unfavorable socioeconomic and health conditions, recurrent infectious diseases, food insecurity, and nutritional deficiencies, among others, are among the main causes of childhood low H/A and W/A44 Horta BL, Santos RV, Welch JR, Cardoso AM, Santos JV, Assis AM, Lira PC, Coimbra CE Jr. Nutritional status of indigenous children: findings from the First National Survey of Indigenous People's Health and Nutrition in Brazil. Int J Equity Health 2013; 12:23.,2424 Jensen SKG, Berens AE, Nelson CA. Effects of poverty on interacting biological systems underlying child development. Lancet 2017; 1(3):225-239.. Likewise, some of these factors can also result in excessive weight gain2323 Wong CY, Zalilah, MS, Chua, EY, Norhasmah S, Chin YS, Nur'Asyura AS. Double-burden of malnutrition among the indigenous peoples (Orang Asli) of Peninsular Malaysia. BMC Public Health 2015; 15:680.,2525 Jehn M, Brewis A. Paradoxical malnutrition in mother-child pairs: untangling the phenomenon of over- and under-nutrition in underdeveloped economies. Econ Hum Biol 2009; 7(1):28-35.. Furthermore, a given group may have a low frequency of weight and height deficits, but they cumulatively present growth failures, with negative impacts at the end of childhood or even in adulthood, such as an increased risk of developing chronic Noncommunicable Diseases (NCDs)2626 Barker DJP. Mothers, babies and disease in later life. J R Soc Med 1995; 88(8):458.,2727 Cameron N. Growth patterns in adverse environments. Amer J Hum Biol 2007; 19(5):615-621..

Despite the recognized severity of the nutritional situation of Indigenous children in Brazil, the available data are still insufficient to identify trends, except in a few case studies2828 Ferreira ALF, Leite, MS, Tavares NI, Santos RV. Alimentação e nutrição dos povos indígenas no Brasil. In: Kac G, Sichieri R, Gigante DP, organizadores. Epidemiologia nutricional. Rio de Janeiro: Fiocruz/Atheneu. No prelo 2024.. Even scarcer are studies focused on the Indigenous population living in urban areas, which constituted 40.0% of the Indigenous population in Brazil, according to the 2010 demographic census2929 Instituto Brasileiro de Geografia e Estatística (IBGE). Censo demográfico 2010: características gerais dos indígenas. Rio de Janeiro: IBGE; 2012.. Thus, this study was designed to evaluate the anthropometric nutritional status and physical growth of Terena Indigenous children living in an urban area of Campo Grande, Mato Grosso do Sul, Brazil in their first year of life.

Methods

Study design and population

This prospective cohort study monitored Terena Indigenous children during the first year of life. The study included Terena Indigenous women who lived in four villages (Água Bonita, Darcy Ribeiro, Marçal de Souza, and Tarsila do Amaral) located in an urban area of Campo Grande, Brazil, and who had children born alive between June 1, 2017, and July 31, 2018. These villages are the only ones in urban areas that are recognized by the state3030 Secretaria Especial de Cidadania do Estado de Mato Grosso do Sul. Comunidades indígenas [internet]. 2021. [acessado 2021 jul 18]. Disponível em: https://www.secid.ms.gov.br/comunidades-indigenas-2/
https://www.secid.ms.gov.br/comunidades-...
. Children born from twin pregnancies (n = 2) and preterm births (gestational age < 37 weeks, n = 1) were excluded.

The Terena belong to the Arawak linguistic family and their first contact with non-Indigenous people occurred in the 16th century3131 Oberg K. The Terena and the Caduveo of Southern Mato Grosso, Brazil. Washington: Institute of Social Anthropology; 1949.. Mato Grosso do Sul has at least 13 Indigenous Lands (IL) where the Terena live. They also live in one IL in Mato Grosso and two in São Paulo. The Terena are considered the fifth largest ethnic group in Brazil with the largest number of people living outside the IL (9,626 people)2929 Instituto Brasileiro de Geografia e Estatística (IBGE). Censo demográfico 2010: características gerais dos indígenas. Rio de Janeiro: IBGE; 2012.. The city of Campo Grande is among the ten Brazilian municipalities with the largest Indigenous population living in urban areas (5,657 people) and the Terena represent two-thirds of this population2929 Instituto Brasileiro de Geografia e Estatística (IBGE). Censo demográfico 2010: características gerais dos indígenas. Rio de Janeiro: IBGE; 2012.,3232 Instituto Brasileiro de Geografia e Estatística (IBGE). Banco multidimensional de estatísticas - consultas livres [internet]. 2010. [acessado 2018 jul 5]. Disponível em: https://www.bme.ibge.gov.br/app/adhoc/index.jsp
https://www.bme.ibge.gov.br/app/adhoc/in...
.

The Terena began migrating to Campo Grande in the 1910s, with this flow intensifying from the 1970s onwards. Thus, the Indigenous people settled in a dispersed manner on the city outskirts and in groups3333 Mussi VPL. As estratégias de inserção dos índios Terena: da aldeia ao espaço urbano (1990-2005) [tese]. Assis: Universidade Estadual Paulista; 2006.. From these groups, on the outskirts of the city, in the 1990s, the construction of housing complexes began, with popular houses, specifically for the Indigenous population, which came to be known as urban villages3333 Mussi VPL. As estratégias de inserção dos índios Terena: da aldeia ao espaço urbano (1990-2005) [tese]. Assis: Universidade Estadual Paulista; 2006.. There are no official records on the number of Indigenous people in these villages. However, estimates indicate that Água Bonita, Darcy Ribeiro, Marçal de Souza, and Tarsila do Amaral have, respectively, around 200, 115, 170 and 80 resident families3434 Comissão Pró-Índio de São Paulo. A cidade como local de afirmação dos direitos indígenas. São Paulo: Centro Gaspar Garcia de Direitos Humanos; 2013..

Data collection and study variables

Data were collected through home visits in three waves: at the 1st, 6th, and 12th months of the child’s life. Regarding the representativeness of the data, the study included all children born in the four Terena urban communities in the municipality of Campo Grande, which corresponds to half of the Indigenous births in the municipality during the period3535 Brasil. Ministério da Saúde (MS). Sistema de Informações sobre Nascidos Vivos (SINASC). Nascidos vivos Mato Grosso do Sul [internet]. 2017. [acessado 2019 jul 8]. Disponível em: http://tabnet.datasus.gov.br/cgi/deftohtm.exe?sinasc/cnv/nvms.def
http://tabnet.datasus.gov.br/cgi/deftoht...
.

The interviews were conducted with the children’s mothers, and there was no need for a translator. Mothers who did not agree to participate in the research either chose not to participate or moved to another municipality during the data collection period and were considered losses.

The child’s weight and length were measured at the 6th- and 12th-month visits. An interviewer trained in anthropometry was responsible for taking all anthropometric measurements of the children. The protocol described by Lohman et al. was followed for taking the measurements3636 Lohman TG, Roche AF, Martorell R. Anthropometric Standardization Reference Manual. Champaign: Human Kinetics; 1988.. A portable, detachable anthropometer was used to measure the child’s length, with an accuracy of 0.1 cm. A portable electronic platform scale with a capacity of 200 kg and an accuracy of 50 g was used to measure the child’s weight. The child’s weight was determined using the “mother/baby” function (the child was weighed with as little clothing as possible, on the mother’s arms; later, only the mother was weighed to check the child’s weight (child’s weight = mother’s and child’s weight - mother’s weight).

Birth weight and length were collected from the Child Health Booklet, as were follow-up weight and length measurements during the months of the first year of life.

Data analysis

Data were tabulated with the double entry in the EpiData 3.1 program (EpiData Assoc., Odense, Denmark), and statistical analyses were performed in Stata 16.0 (Stata Corp., College Station, USA). Z-scores were calculated for birth weight for gestational age, birth length for gestational age, and weight (kg)/length (m) for gestational age ratio, according to Intergrowth-21st parameters3737 Villar J, Cheikh Ismail L, Victora CG, Ohuma EO, Bertino E, Altman DG, Lambert A, Papageorghiou AT, Carvalho M, Jaffer YA, Gravett MG, Purwar M, Frederick IO, Noble AJ, Pang R, Barros FC, Chumlea C, Bhutta ZA, Kennedy SH; International Fetal and Newborn Growth Consortium for the 21st Century (INTERGROWTH-21st). International standards for newborn weight, length, and head circumference by gestational age and sex: the Newborn Cross-Sectional Study of the INTERGROWTH-21st Project. Lancet 2014; 384(9946):857-868.. For the anthropometric measurements of the 6th and 12th months, the Z-scores were calculated for the length-for-age (L/A), weight-for-age (W/A), and body mass index (BMI)-for-age (BMI/A) indexes, according to the parameters of the World Health Organization (WHO)3838 World Health Organization (WHO). Child Growth Standards: length/height-for-age, weight-for-age, weight for-length, weight-for-height and body mass index-for-age: methods and development. Geneva: WHO; 2006.. The differences between the mean z-score values for the three indexes over time (at birth, 6 months, and 12 months) were analyzed using the ANOVA test, with Tukey’s post-test, considering p-values ​​< 0.05 as statistically significant.

Z-score values were used to classify the children’s nutritional status. For the L/A index, low L/A values were considered to be Z-scores < -2. For the W/A index, low W/A was considered to be Z-score values < -2, while high W/A was considered to be Z-score values ​​> 2. For the BMI/A index, low weight was considered to be Z-score values < -2, overweight to be Z-score values > 2 and ≤ 3, and obesity to be Z-score values ​​> 33939 Brasil. Ministério da Saúde (MS). Orientações para a coleta e análise de dados antropométricos em serviços de saúde: Norma Técnica do Sistema de Vigilância Alimentar e Nutricional. Brasília: MS; 2011.. The combination of the categories overweight and obesity was considered excess weight.

For the average Z-scores of the anthropometric indices and the prevalence of nutritional status at 6 and 12 months, only the anthropometric data measured in the research were used, since it was an assessment of the nutritional status at a specific age of the children. The set of anthropometric measurements taken and those collected directly from the Child Health Booklet were used to construct the growth curves. The L/A, W/A, and BMI/A were then formulated.

The number of anthropometric measurements of the same individual varied over time, and not all of the measurements were equidistant in time, as they were considered unbalanced and unstructured data. Thus, the Generalized Additive Mixed Models (GAMM) were used to construct the growth curves, considering the relationship between inter-individual and intra-individual measurements over time4040 Pinheiro JC, Bates DM. Mixed effects models in S and S-PLUS. New York: Springer-Verlag; 2000.. The spline adjustment function was used to construct the curves. The procedure was performed separately for each sex, including all measurements for each individual, both those measured and those collected from the Children’s Health Handbooks, following the methodology proposed by Ferreira et al.1111 Leite MS, Santos RV, Gugelmin SA, Coimbra Jr CEA. Crescimento físico e perfil nutricional da população indígena Xavánte de Sangradouro-Volta Grande, Mato Grosso, Brasil. Cad Saude Publica 2006; 22(2):265-276.

The adjusted curves were compared to the WHO reference curves3939 Brasil. Ministério da Saúde (MS). Orientações para a coleta e análise de dados antropométricos em serviços de saúde: Norma Técnica do Sistema de Vigilância Alimentar e Nutricional. Brasília: MS; 2011.,4141 De Onis M, Onyango AW. WHO child growth standards. Lancet 2008; 371(9608):204. based on sex and age. The Anthro 3.2.2 software (WHO Anthro, Switzerland) was used to calculate Z-scores for anthropometric indices. The statistical software R 3.6.8 (R Development Core Team, 2004) and the gamm44242 Wood S, Scheipl F. Package 'gamm4' [internet]. 2017. [cited 2019 out 31]. Available from: https://cran.r-project.org/web/packages/gamm4/gamm4.pdf
https://cran.r-project.org/web/packages/...
and lme44343 Dai B, Scheipl F, Grothendieck G, Green P, Fox J, Bauer A, Krivitsky PN, Tanaka E, Jagan M. Package 'lme4' [internet]. 2019. [cited 2019 out 31]. Available from: https://cran.r-project.org/web/packages/lme4/lme4.pdf
https://cran.r-project.org/web/packages/...
libraries were used to develop the curves.

Ethical aspects

This study was approved by the Human Research Ethics Committee of the Federal University of Mato Grosso do Sul and by the National Research Ethics Commission (CAAE No. 64555517.6.0000.0021). The investigated community leaders approved the study, and the interviewed mothers, as well as their guardians, when the mother was under 18 years of age, provided the free and informed consent to participate in the study.

Results

Among 49 children eligible for the study, 42 participated (85.7%). There were three refusals (6.1%), two withdrawals (4.1%), and two mothers who moved to another municipality during the study (4.1%). Among the children who participated in the study, in one case it was not possible to obtain anthropometric data at 6 months due to a temporary move to a different municipality. For the growth curves, 207 weight measurements and 207 length measurements were used.

The mean L/A index Z-scores, in both sexes, decreased throughout the first year of life. The difference was statistically significant when comparing the averages at birth to the averages at 6 months and 12 months in males (-0.01 versus -0.47; p < 0.05 and -0.01 versus -0.67; p < 0.05; respectively) and in females (0.18 versus -0.36; p < 0.05 and 0.18 versus -0.53; p < 0.05; respectively). There was no difference in the W/A index over time in either sex. The mean BMI/A Z-score was higher at 6 months when compared to the Z-score at birth for males (0.15 versus 0.78; p < 0.05) (Table 1).

Table 1
Mean and standard deviation of Z-score of anthropometric indices of the Terena birth cohort. at birth. 6 months. and 12 months. according to sex. Campo Grande. Mato Grosso do Sul. 2017-2018.

In males, the prevalence of low L/A at the end of the first year of life was 4.5%. In females, there was one case of low L/A at 12 months. No cases of low weight were recorded among the evaluated children, according to the W/A and BMI/A indices, respectively. According to the W/A index, 4.5% of boys and 10.0% of girls had high weight for their age at the end of the first year of life. According to BMI/A, excess weight was recorded in 4.5% of boys and 20.0% of girls at 12 months (Table 2).

Table 2
Low length for age, overweight, and obesity prevalence of the Terena birth cohort, at birth, 6 months, and 12 months, according to sex. Campo Grande, Mato Grosso do Sul, 2017-2018 (n = 41).

The L/A curves, for both boys and girls, do not reach the median of the reference population at any time, except at the moment of birth, when they start close to the Z-score = 0. For girls, the distance from the median seems more pronounced than for boys, with a slight closeness at around 6 months until approximately 10 months, when they diverge again (Figure 1).

Figure 1
Length curves (cm) of Terena boys (A) and girls (B) up to 12 months of age compared with the Z-scores of the World Health Organization reference population. Campo Grande, Mato Grosso do Sul, 2017-2018.

Regarding the W/I index, the curve for males remains close to the median with some fluctuations over time. For girls, the curve starts slightly above the median, overlapping it at approximately 30 days of age and remaining above it from 4 months onwards (Figure 2).

Figure 2
Weight curves (kg) of Terena boys (A) and girls (B) up to 12 months of age compared with the Z-scores of the World Health Organization reference population. Campo Grande, Mato Grosso do Sul, 2017-2018.

The BMI/A curve for males started its trajectory close to the median and then remained below the median until around 3 months when it exceeded it. For girls, the BMI/A curve was always above the reference median (Figure 3).

Figure 3
Body mass index (BMI) curves (kg/m²) of Terena boys (A) and girls (B) up to 12 months of age compared with the Z-scores of the World Health Organization reference population. Campo Grande, Mato Grosso do Sul, 2017-2018.

Discussion

In summary, the data recorded in this study for Terena Indigenous children indicate an average linear growth that is lower than expected, based on the criteria used internationally to assess the physical growth and nutritional status of children. At the same time, they record excess weight in the first year of life, as well as a weight gain of greater than the reference median.

The Terena Indigenous children evaluated in this study present a more favorable profile than that observed in some cross-sectional studies that were carried out in past decades in non-urban Terena communities, which revealed, at the time, a high prevalence of low H/A4444 Ribas DLB, Sganzerla A, Zorzatto JR, Philippi ST. Nutrição e saúde infantil em uma comunidade indígena Teréna, Mato Grosso do Sul, Brasil. Cad Saude Publica 2001; 17(2):323-331.

45 Alves GMS, Morais MB, Fagundes-Neto U. Estado nutricional e teste de hidrogênio no ar expirado com lactose e lactulose em crianças indígenas terenas. J Pediatr (Rio J) 2002; 78(2):113-119.
-4646 Morais, MB, Alves GMS, Fagundes-Neto U. Estado nutricional de crianças índias Terenas: evolução do peso e estatura e prevalência atual de anemia. J Pediatr (Rio J) 2005; 81(5):383-389., which reached 26.1% among children aged one to five years4545 Alves GMS, Morais MB, Fagundes-Neto U. Estado nutricional e teste de hidrogênio no ar expirado com lactose e lactulose em crianças indígenas terenas. J Pediatr (Rio J) 2002; 78(2):113-119.. In comparison with Indigenous children under one year of age, assessed in the first and only National Survey of Health and Nutrition of Indigenous Peoples, carried out in rural areas, the prevalence of low L/A at the end of the first year of life of Terena children was also lower (4.8% versus 14.9%)44 Horta BL, Santos RV, Welch JR, Cardoso AM, Santos JV, Assis AM, Lira PC, Coimbra CE Jr. Nutritional status of indigenous children: findings from the First National Survey of Indigenous People's Health and Nutrition in Brazil. Int J Equity Health 2013; 12:23..

The low prevalence of height deficits observed among Terena children could indicate optimal linear growth, as well as the existence of socioenvironmental conditions favorable to child growth. However, this does not appear to be the case. The L/A curves remained below the reference medians throughout the first year of life. Furthermore, a previously published study of this same population4747 Bresan D, Pontes ERJC, Leite MS. Fatores associados ao peso ao nascer de crianças indígenas Terena, residentes na área urbana de Campo Grande, Mato Grosso do Sul, Brasil. Cad Saude Publica 2019; 3(Supl. 35):e00086819. shows that variables, such as mother’s education, sanitation conditions, housing, and per capita income, present systematically worse indicators than those recorded for the Brazilian and Mato Grosso do Sul populations4848 Instituto Brasileiro de Geografia e Estatística (IBGE). Renda domiciliar per capita 2017 [Internet]. [acessado 2019 jan 30]. Disponível em: https://ftp.ibge.gov.br/Trabalho_e_Rendimento/Pesquisa_Nacional_por_Amostra_de_Domicilios_continua/Renda_domiciliar_per_capita/Renda_domiciliar_per_capita_2017.pdf
https://ftp.ibge.gov.br/Trabalho_e_Rendi...

49 Instituto Brasileiro de Geografia e Estatística (IBGE). Pesquisa nacional de saneamento básico 2017: abastecimento de água e esgotamento sanitário. Rio de Janeiro: IBGE; 2020.
-5050 Instituto Brasileiro de Geografia e Estatística (IBGE). Pesquisa Nacional por Amostra de Domicílios Contínua. Rio de Janeiro: IBGE; 2020.. Almost half the Terena women (46.5%) had up to eight years of education, 74.4% lived in households not connected to the sewage collection system, and a third lived in houses with seven to nine residents4747 Bresan D, Pontes ERJC, Leite MS. Fatores associados ao peso ao nascer de crianças indígenas Terena, residentes na área urbana de Campo Grande, Mato Grosso do Sul, Brasil. Cad Saude Publica 2019; 3(Supl. 35):e00086819.,5151 Bresan D. Crescimento físico e condições de saúde e nutrição de crianças Terena em Campo Grande, MS: um estudo de coorte [tese]. Campo Grande: Universidade Federal de Mato Grosso do Sul; 2019.. Per capita income reached a maximum value of R$800.00, and in 65.5% of households, this value did not exceed R$265.00.4747 Bresan D, Pontes ERJC, Leite MS. Fatores associados ao peso ao nascer de crianças indígenas Terena, residentes na área urbana de Campo Grande, Mato Grosso do Sul, Brasil. Cad Saude Publica 2019; 3(Supl. 35):e00086819. Anemia data from these same children reveal that at least half of them were anemic at six (53.6%) and twelve months of age (61.9%)5151 Bresan D. Crescimento físico e condições de saúde e nutrição de crianças Terena em Campo Grande, MS: um estudo de coorte [tese]. Campo Grande: Universidade Federal de Mato Grosso do Sul; 2019.. Diarrhea was recorded for 19.5% of children in the week before the six-month-old interview and exclusive breastfeeding had a median duration of 2.5 months5151 Bresan D. Crescimento físico e condições de saúde e nutrição de crianças Terena em Campo Grande, MS: um estudo de coorte [tese]. Campo Grande: Universidade Federal de Mato Grosso do Sul; 2019.. This set of variables, therefore, outlines a largely unfavorable scenario for children’s health and nutrition, which will possibly have a cumulative effect during childhood.

Literature has shown that human growth up to the age of five is subject to little genetic influence5252 Bogin B. Patterns of human growth. Cambridge: Cambridge University Press; 1999.,5353 Eveleth PB, Tanner JM. Worldwide variation in human growth. Cambridge: Cambridge University Press; 1990.. The proposal for the universal applicability of anthropometric parameters for assessing child growth, recommended by the WHO, is based on this evidence, which indicates a lower influence of genetic variability when compared to the impact of environmental conditions on children’s physical growth. The Terena growth curves are compatible with the precarious environmental and health conditions to which these children are subjected since birth, and it is plausible to see in them the negative impact of this scenario. In other words, as a whole and in interactions, these factors have a recognized impact on children’s nutritional conditions and physical growth and partly explain the behavior of the growth curves of the Terena children evaluated here.

Equivalent contexts have been highlighted in the analysis of the nutritional situation of Indigenous children throughout the country, and point to precarious socioeconomic and sanitary conditions, in addition to nutritional profiles where height deficits predominate in prevalence rates that are usually high, higher than those recorded among non-indigenous children in the same regions44 Horta BL, Santos RV, Welch JR, Cardoso AM, Santos JV, Assis AM, Lira PC, Coimbra CE Jr. Nutritional status of indigenous children: findings from the First National Survey of Indigenous People's Health and Nutrition in Brazil. Int J Equity Health 2013; 12:23.,1010 Ferreira AA, Welch JR, Santos RV, Gugelmin SA, Coimbra Jr CEA. Nutritional status and growth of indigenous Xavante children, Central Brazil. Nutr J 2012; 11:3.

11 Leite MS, Santos RV, Gugelmin SA, Coimbra Jr CEA. Crescimento físico e perfil nutricional da população indígena Xavánte de Sangradouro-Volta Grande, Mato Grosso, Brasil. Cad Saude Publica 2006; 22(2):265-276.

12 Orellana JDY, Marrero L, Alves CLM, Ruiz CMV, Hacon SS, Oliveira MW, Basta PC. Association of severe stunting in indigenous Yanomami children with maternal short stature: clues about the intergerational transmission. Cien Saude Colet 2019; 24(5):1875-1883.
-1313 Pantoja LN, Orellana JDY, Leite MS, Basta PC. Cobertura do Sistema de Vigilância Alimentar e Nutricional Indígena (SISVAN-I) e prevalência de desvios nutricionais em crianças Yanomami menores de 60 meses, Amazônia, Brasil. Rev Bras Saude Mater Infant 2014; 14(1):53-63.. Evidence in the literature suggests that inadequate basic sanitation conditions have a negative effect on child growth and development, due to greater exposure to pathogens. Social and economic mechanisms are also linked to these conditions5454 Cumming O, Cairncross S. Can water, sanitation and hygiene help eliminate stunting? Current evidence and policy implications. Matern Child Nutr 2016; 12(Suppl. 1):91-105.. A study that analyzed the presence of basic sanitation services in urban households with children up to five years of age, based on data from the 2010 census, revealed that Indigenous households generally had the lowest frequency of adequate sanitation services5555 Raupp L, Cunha GM, Fávaro TR, Santos RV. Saneamento básico e desigualdades de cor/raça em domicílios urbanos com a presença de crianças menores de 5 anos, com foco na população indígena. Cad Saude Publica 2019; 35(Supl. 3):e00058518.. Higher mothers’ maternal education is associated with a series of behaviors that can be positive for the child’s health and nutrition, such as longer breastfeeding duration, use of health services, and appropriate infant feeding, in addition to normally meaning better economic conditions for the family, which together can influence linear growth5656 Mensch BS, Chuang EK, Melnikas AJ, Psaki SR. Evidence for causal links between education and maternal and child health: systematic review. Trop Med Int Health 2019; 24(5):504-522..

Although the assessment of excess weight using the BMI/A index in children under five years of age requires additional assessments for diagnosis, prevalence rates at the end of the first year of life were recorded in Terena children similar to those found among non-Indigenous children under one year of age in the country (12.3% versus 9.1%)99 Barreto CTG, Cardoso AM, Coimbra Jr CEA. Nutritional status of Guarani indigenous children in the States of Rio de Janeiro and São Paulo, Brazil. Cad Saude Publica 2014; 30(3):657-662.. Few studies have assessed excess weight among Indigenous children in Brazil, especially in this age group, and using the BMI/A index, which is recommended for classifying childhood overweight and obesity and comparing it with the WHO reference population5757 World Health Organization (WHO). Training Course on Child Growth Assessment. Geneva: World Health Organization; 2008.,5858 De Onis M, Lobstein, T. Defining obesity risk status in the general childhood population: which cut-offs should we use? Int J Pediatr Obes 2010; 5(6):458.. Among Xukuru do Orurubá children under two years of age, in Pernambuco, according to BMI/A, the prevalence of excess weight was 6.9%1414 Fávaro TR, Ferreira AA, Cunha GM, Coimbra Jr CEA. Excesso de peso em crianças indígenas Xukuru do Ororubá, Pernambuco, Brasil: magnitude e fatores associados. Cad Saude Publica 2019; 35(Supl. 3):e00056619.. Among Pataxó children under five years of age in Minas Gerais, the prevalence of overweight, also according to BMI/A, was 2.9%1515 Santos AP, Mazzeti CMDS, Franco MDCP, Santos NLGO, Conde WL, Leite MS, Pimenta AM, Villela LCM, Castro TG. Estado nutricional e condições ambientais e de saúde de crianças Pataxó, Minas Gerais, Brasil. Cad Saude Publica 2018; 34(6):e00165817.. In both studies1414 Fávaro TR, Ferreira AA, Cunha GM, Coimbra Jr CEA. Excesso de peso em crianças indígenas Xukuru do Ororubá, Pernambuco, Brasil: magnitude e fatores associados. Cad Saude Publica 2019; 35(Supl. 3):e00056619.,1515 Santos AP, Mazzeti CMDS, Franco MDCP, Santos NLGO, Conde WL, Leite MS, Pimenta AM, Villela LCM, Castro TG. Estado nutricional e condições ambientais e de saúde de crianças Pataxó, Minas Gerais, Brasil. Cad Saude Publica 2018; 34(6):e00165817. the authors point out that the prevalence of excess weight recorded reflects, to a large extent, the transformations in subsistence strategies, combined with changes in eating patterns and physical activity among native populations.

When interpreting excess weight among children, it is important to consider the parents’ weight; a child with one obese parent has a 40.0% greater probability of being overweight; when both parents are obese, the probability increases to 70.0%5757 World Health Organization (WHO). Training Course on Child Growth Assessment. Geneva: World Health Organization; 2008.. Obesity, like other NCDs, has been frequently mentioned in studies with Indigenous adults in the country1212 Orellana JDY, Marrero L, Alves CLM, Ruiz CMV, Hacon SS, Oliveira MW, Basta PC. Association of severe stunting in indigenous Yanomami children with maternal short stature: clues about the intergerational transmission. Cien Saude Colet 2019; 24(5):1875-1883.,1818 Fávaro TR, Santos RV, Cunha GM, Leite IC, Coimbra Jr CEA. Obesidade e excesso de peso em adultos indígenas Xukuru do Ororubá, Pernambuco, Brasil: magnitude, fatores socioeconômicos e demográficos associados. Cad Saude Publica 2015; 31(8):1685-1697.,1919 Chagas CA, Castro TG, Leite MS, Barroso MAC, Viana M, Beinner MA, Pimenta AM. Prevalência estimada e fatores associados à hipertensão arterial em indígenas adultos Krenak do Estado de Minas Gerais, Brasil. Cad Saude Publica 2020; 36(1):e00206818.,5959 Coimbra Jr CEA, Santos RV, Cardoso AM, Souza MC, Garnelo L, Rassi E, Follér ML, Horta BL. The First National Survey of Indigenous People´s Health and Nutrition in Brazil: rationale, methodology, and overview of results. BMC Public Health 2013; 13:52.

60 Tavares FG, Coimbra Jr. CEA, Cardoso AM. Níveis tensionais de adultos indígenas Suruí, Rondônia, Brasil. Cien Saude Colet 2013; 18(5):1399-1409.

61 Gimeno SGA, Rodrigues D, Pagliaro H, Cano EN, Lima EED, Baruzzi RG. Perfil metabólico e antropométrico de índios Aruák: Mehináku, Waurá e Yawalapití, Alto Xingu, Brasil Central, 2000/2002. Cad Saude Publica 2007; 23(8):1946-1954.
-6262 Oliveira GF, Oliveira TR, Rodrigues FF, Corrêa LF, Ikejiri AT, Casulari LA. Prevalence of diabetes mellitus and impaired glucose tolerance in indigenous people from Aldeia Jaguapiru, Brazil. Rev Panam Salud Pública 2011; 29(5):315-321.. Furthermore, the results of a study with the same population evaluated in the present study indicated that 61.0% of Terena women were overweight before pregnancy, and maternal pre-gestational obesity was associated with higher birth weight in Terena children4747 Bresan D, Pontes ERJC, Leite MS. Fatores associados ao peso ao nascer de crianças indígenas Terena, residentes na área urbana de Campo Grande, Mato Grosso do Sul, Brasil. Cad Saude Publica 2019; 3(Supl. 35):e00086819.. Excess weight during childhood increases the risk of excess weight in adolescence and adulthood, and is associated with the emergence of NCDs6363 Daniels SR. Complications of obesity in children and adolescents. Int J Obes (Lond) 2009; 33(Suppl .1):S60-S605.

64 Vos MB, Welsh J. Childhood obesity: update on predisposing factors and prevention strategies. Curr Gastroenterol Rep 2010; 12(4):280-287.
-6565 Urlacher SS, Blackwell AD, Liebert MA, Madimenos FC, Cepon-Robins TJ, Gildner TE, et al. Physical growth of the shuar: Height, Weight, and BMI references for an indigenous amazonian population. Am J Hum Biol 2016; 28(1):16-30..

When the data are examined longitudinally, it can be observed that the L/A curve of Terena children did not reach the median of the reference population at any time during the first year of life, with fluctuations being recorded over time: this presents a greater distance from the median up to 6 months, with a subsequent approximation until 10 months, when it diverges again. Added to this picture, the average Z-scores of the L/A index decreased throughout the first year of life. Conversely, the W/A curve, especially among girls, starts slightly above the median, overlapping around the first month of life. From the fourth month onwards, it follows a trajectory above Z-scores 0. The BMI/A curves follow the same trend, and it is also in females that the Terena curve remains systematically above the reference median.

The only published study that longitudinally assessed the physical growth of Indigenous children in Brazil was a study among Xavante children under 10 years of age, conducted in Mato Grosso1111 Leite MS, Santos RV, Gugelmin SA, Coimbra Jr CEA. Crescimento físico e perfil nutricional da população indígena Xavánte de Sangradouro-Volta Grande, Mato Grosso, Brasil. Cad Saude Publica 2006; 22(2):265-276.. The study showed that the H/A curves of Xavante children, for both sexes, start close to the median of the reference population, starting to move away from it around six to eight months of age, but, unlike what was observed among the Terena, they reach Z-scores of -2 around 12 months. Similarly, the W/A curve starts close to the median, but, at around six to eight months, it moves negatively away, although it does not reach Z-scores of -2 at any point in its trajectory1111 Leite MS, Santos RV, Gugelmin SA, Coimbra Jr CEA. Crescimento físico e perfil nutricional da população indígena Xavánte de Sangradouro-Volta Grande, Mato Grosso, Brasil. Cad Saude Publica 2006; 22(2):265-276.. By contrast, among the Terena, the W/A curve, especially among girls, exceeds the median of the reference population. Studies with native peoples from other parts of the world that have carried out longitudinal analyses on the physical growth of children are rare, and methodological differences complicate and limit any attempt at comparison6565 Urlacher SS, Blackwell AD, Liebert MA, Madimenos FC, Cepon-Robins TJ, Gildner TE, et al. Physical growth of the shuar: Height, Weight, and BMI references for an indigenous amazonian population. Am J Hum Biol 2016; 28(1):16-30.,6666 Alfonso-Durruty MP, Valeggia CR. Growth patterns among indigenous Qom children of the Argentine Gran Chaco. Am J Hum Biol 2016; 28(6):895-904..

Studies indicate that failures in linear growth during the first two years of life generate greater risks of morbidity and mortality and can lead to unfavorable outcomes over the long term, such as shorter height in adulthood, reduced economic productivity, and, for women, lower offspring birth weight6767 Victora CG, Adair L, Fall C, Hallal M, Reynaldo, Richter L, Sachdev HS; Maternal and Child Undernutrition Study Group. Maternal and child undernutrition: consequences for adult health and human capital. Lancet 2008; 371(9609):340-357.. There is a higher risk of developing NCDs in adulthood, especially when they experience rapid weight gain after the first two years of life6767 Victora CG, Adair L, Fall C, Hallal M, Reynaldo, Richter L, Sachdev HS; Maternal and Child Undernutrition Study Group. Maternal and child undernutrition: consequences for adult health and human capital. Lancet 2008; 371(9609):340-357.

68 Adair LS, Fall CHD, Osmond C, Stein AD, Martorell R, Ramirez-Zea M, Sachdev HS, Dahly DL, Bas I, Norris SA, Micklesfield L, Hallal P, Victora CG; COHORTS group. Associations of linear growth and relative weight gain during early life with adult health and human capital in countries of low and middle income: findings from five birth cohort studies. Lancet 2013; 382(9891):525-534.
-6969 De Onis M, Branca F. Childhood stunting: a global perspective. Matern Child Nutr 2016; 12(Suppl. 1):12-26..

Growth patterns that simultaneously present height deficits and excess weight have been described in the literature2828 Ferreira ALF, Leite, MS, Tavares NI, Santos RV. Alimentação e nutrição dos povos indígenas no Brasil. In: Kac G, Sichieri R, Gigante DP, organizadores. Epidemiologia nutricional. Rio de Janeiro: Fiocruz/Atheneu. No prelo 2024.,5757 World Health Organization (WHO). Training Course on Child Growth Assessment. Geneva: World Health Organization; 2008.,7070 Popkin BM, Richards MK, Monteiro CA. Stunting is associated with overweight in children of four nations that are going through the nutrition transition. J Nutr 1996; 126(12):3009-3016.. A systematic review of research from low- and middle-income countries found that although child malnutrition is decreasing, there are still populations with high frequencies of linear growth deficits and at the same time with increasing records of overweight, producing a double burden of disease at the population and individual levels7171 Tzioumis E, Kay MC, Bentley ME, Adair LS. Prevalence and trends in the childhood dual burden of malnutrition in low- and middle-income countries, 1990-2012. Public Health Nutr 2016; 19(8):1375-1388..

The situation recorded among Terena children reveals L/A curves systematically below the reference median, indicating growth failures and excess weight appears in the first year of life. Although the universe of children evaluated is small, and we do not have information on the food consumption of this population, this situation is compatible with food and nutritional transition processes that have been reported among Indigenous adults of different ethnicities in the country for at least two decades6060 Tavares FG, Coimbra Jr. CEA, Cardoso AM. Níveis tensionais de adultos indígenas Suruí, Rondônia, Brasil. Cien Saude Colet 2013; 18(5):1399-1409.

61 Gimeno SGA, Rodrigues D, Pagliaro H, Cano EN, Lima EED, Baruzzi RG. Perfil metabólico e antropométrico de índios Aruák: Mehináku, Waurá e Yawalapití, Alto Xingu, Brasil Central, 2000/2002. Cad Saude Publica 2007; 23(8):1946-1954.
-6262 Oliveira GF, Oliveira TR, Rodrigues FF, Corrêa LF, Ikejiri AT, Casulari LA. Prevalence of diabetes mellitus and impaired glucose tolerance in indigenous people from Aldeia Jaguapiru, Brazil. Rev Panam Salud Pública 2011; 29(5):315-321.,7272 Lourenço AEP, Santos RV, Orellana JDY, Coimbra Jr. CEA. Nutrition transition in Amazonia: Obesity and socioeconomic change in the Suruí Indians from Brazil. Amer J Hum Biol 2008; 20(5):564-571.. These records describe a high prevalence of overweight and obesity and the emergence of other NCDs, such as systemic arterial hypertension and diabetes mellitus. At a national level, this situation is highlighted in the National Survey among women of childbearing age1717 Bresan D, Bastos JL, Leite MS. Epidemiologia da hipertensão arterial em indígenas Kaingang, Terra Indígena Xapecó, Santa Catarina, Brasil, 2013. Cad Saude Publica 2015; 31(2):331-344..

Urbanization, experienced by the Terena population evaluated here, may be a critical point in understanding the growth profile found among their children. Although Indigenous peoples in the country have undergone major changes in their subsistence modes throughout history, migration to urban centers can further accelerate the transformations, involving the adoption of high-calorie diets, rich in fats and simple carbohydrates, high in salt, and low in dietary fiber. The changes also extend to physical activity patterns, which can be negatively affected by this process22 Gracey M, King M. Indigenous health part 1: determinants and disease patterns. Lancet 2009; 374(9683):65-75.,7373 Damman S, Eide WB, Kuhnlein HV. Indigenous peoples' nutrition transition in a right to food perspective. Food Policy 2008; 33(2):135-155..

Finally, we highlight that monitoring the physical growth of Indigenous children over longer periods may be important to understand this complex process, which is still scarcely described in the literature. Limitations of the study include follow-up during only the first year of life and the number of children evaluated, although all children born during the period were included in the study and monitored throughout the period. Other limitations lie in the number of anthropometric assessments and the variable interval between them.

Conclusion

Although moving to an urban environment could potentially represent an improvement in environmental conditions and access to goods and services, including healthcare services, in the families monitored here, it does not translate into a guarantee of truly favorable conditions for child growth and nutrition. Their insertion into the urban environment occurred in the outskirts of Campo Grande and in the lower socioeconomic strata, where they experience precarious sanitation and housing conditions and, in broader terms, less access to goods and services, including health services when compared to other social segments. Their socioeconomic and sanitation indicators are systematically worse than both regional and national averages, which points to the racial dimension of the significant socioeconomic inequalities and health inequities that affect Indigenous peoples in the country.

The data also suggest that the urban Terena population is going through a rapid process of nutritional transition, with excess weight present in the first year of life, which represents, in the medium and long term, an undeniable challenge for the health services that serve this and other Indigenous peoplethat currently live in urban environments. Health policies and programs aimed at Indigenous peoples in the country must urgently consider these particularities and be able to contemplate the growing Indigenous population contingent living in urban areas currently not assisted by the National Policy for Health Care for Indigenous Peoples, which is only intended for Indigenous people living in IL.

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  • Funding

    Fundação de Apoio ao Desenvolvimento do Ensino, Ciencia e Tecnologia do Estado de Mato Grosso do Sul; Conselho Nacional de Desenvolvimento Científico e Tecnológico (TO No. 026/17). Coordenação de Aperfeiçoamento de Pessoal de Nível Superior; Universidade Federal de Mato Grosso do Sul (Funding Code 001).

Publication Dates

  • Publication in this collection
    13 Dec 2024
  • Date of issue
    Dec 2024

History

  • Received
    15 Sept 2023
  • Accepted
    29 Feb 2024
  • Published
    02 May 2024
ABRASCO - Associação Brasileira de Saúde Coletiva Rio de Janeiro - RJ - Brazil
E-mail: revscol@fiocruz.br