ABSTRACT:

Objective:

To evaluate the prevalence of anemia, mean hemoglobin levels, and the main nutritional, demographic, and socioeconomic factors among Xavante children in Mato Grosso State, Brazil.

Methods:

A survey was conducted with children under 10 years of age in two indigenous Xavante communities within the Pimentel Barbosa Indigenous Reserve. Hemoglobin concentration levels, anthropometric measurements, and socioeconomic/demographic data were collected by means of clinical measurements and structured interviews. The cut-off points recommended by the World Health Organization were used for anemia classification. Linear regression analyses with hemoglobin as the outcome and Poisson regression with robust variance and with the presence or absence of anemia as outcomes were performed (95%CI).

Results:

Lower mean hemoglobin values were observed in children under 2 years of age, without a significant difference between sexes. Anemia was observed among 50.8% of children overall, with the highest prevalence among children under 2 years of age (77.8%). Age of the child was inversely associated with the occurrence of anemia (adjusted PR = 0.60; 95%CI 0.38-0.95) and mean hemoglobin values increased significantly with age. Greater height-for-age z-score values reduced the probability of having anemia by 1.8 times (adjusted PR = 0.59; 95%CI 0.34-1.00). Presence of another child with anemia within the household increased the probability of the occurrence of anemia by 52.9% (adjusted PR = 1.89; 95%CI 1.16-3.09).

Conclusion:

Elevated levels of anemia among Xavante children reveal a disparity between this Indigenous population and the national Brazilian population. Results suggest that anemia is determined by complex and variable relationships between socioeconomic, sociodemographic, and biological factors.

Keywords:
Anemia; Deficiency diseases; Nutrition surveys; Child health; Health of indigenous peoples; Indians, South American

INTRODUCTION

Anemia is considered the most prevalent nutritional deficiency in the world, affecting approximately a quarter of the population, in particular, children and women in their reproductive age¹1. Milman N. Anemia-still a major health problem in many parts of the world! Ann Hematol 2011; 90(4): 369-77.. In Brazil, the most recent national survey that evaluated the concentration of hemoglobin in the population indicated that 20.9% of children under 5 years of age had anemia²2. Brasil, Ministério da Saúde. Pesquisa Nacional de Demografia e Saúde da Criança e da Mulher - PNDS 2006: dimensões do processo reprodutivo e da saúde da criança/Ministério da Saúde. Centro Brasileiro de Análise e Planejamento. Brasília: Ministério da Saúde; 2009.. In this investigation, important variations in the prevalence of anemia were observed between regions, varying between 10.4% in the North and 25.5% in the Northeast.

Studies about the epidemiology of anemia in Indigenous children in Brazil have been conducted in recent decades, revealing, in many cases, prevalences above 60-70%³3. Barreto CTG, Cardoso AM, Coimbra Jr. CEA. Estado nutricional de crianças indígenas Guarani nos estados do Rio de Janeiro e São Paulo, Brasil. Cad Saúde Pública 2014; 30(3): 657-62.^,44. Orellana JDY, Coimbra Jr. CEA, Lourenço AEP, Santos RV. Nutritional status and anemia in Suruí Indian children, Brazilian Amazon. J Pediatr (Rio J) 2006; 82(5): 383-8.^,55. Pereira JF, Oliveira MAA, Oliveira JS. Anemia em crianças indígenas da etnia Karapotó. Rev Bras Saúde Mater Infant 2012; 12(4): 375-82.. According to the First National Survey of Health and Nutrition of Indigenous Peoples, performed in 2008 and 2009, more than half (51.4%) of Indigenous children under 5 years of age in the country had anemia, with the highest prevalence for those under 2 years of age (74.2%)⁶6. Leite MS, Cardoso AM, Coimbra Jr. CEA, Welch JR, Gugelmin SA, Lira PC, et al. Prevalence of anemia and associated factors among indigenous children in Brazil: results from the First National Survey of Indigenous People's Health and Nutrition. Nutr J 2013; 12: 69.. In the case of the Indigenous children, interregional differences were also observed in the distribution of anemia, but with an opposite pattern to the overall distribution revealed by the National Survey of Demography and Health (PNDS)²2. Brasil, Ministério da Saúde. Pesquisa Nacional de Demografia e Saúde da Criança e da Mulher - PNDS 2006: dimensões do processo reprodutivo e da saúde da criança/Ministério da Saúde. Centro Brasileiro de Análise e Planejamento. Brasília: Ministério da Saúde; 2009., varying from 66.4% in the North to 41.1% in the Northeast⁶6. Leite MS, Cardoso AM, Coimbra Jr. CEA, Welch JR, Gugelmin SA, Lira PC, et al. Prevalence of anemia and associated factors among indigenous children in Brazil: results from the First National Survey of Indigenous People's Health and Nutrition. Nutr J 2013; 12: 69.. Thus, the prevalence of anemia is significantly higher among Indigenous children as compared to the overall values for Brazilian children²2. Brasil, Ministério da Saúde. Pesquisa Nacional de Demografia e Saúde da Criança e da Mulher - PNDS 2006: dimensões do processo reprodutivo e da saúde da criança/Ministério da Saúde. Centro Brasileiro de Análise e Planejamento. Brasília: Ministério da Saúde; 2009..

Considering evidence indicating that the disease profile is distinct among Indigenous children, there persists a need for knowledge production in the epidemiology of anemia among Indigenous populations, considering their specific environmental, economic, social, and dietary contexts. The objective of this study was to evaluate the prevalence of anemia, mean hemoglobin levels, and associated nutritional, demographic, and socioeconomic factors among Indigenous Xavante children.

METHODS

At the time of the study, the Xavante population totaled approximately 15,000, distributed among nine federally recognized Indigenous reserves in western Mato Grosso state. Pimentel Barbosa Indigenous Reserve was the largest of these by area and had the highest fertility rates, which translated into the largest proportion of young people under 15 years of age in the population (10.1% in the period from 2002 to 2004)⁷7. Welch JR, Santos RV, Flowers NM, Coimbra Jr. CEA. Na Primeira Margem do Rio: Território e Ecologia do Povo Xavante de Wedezé. Rio de Janeiro: Museu do Índio/FUNAI; 2013..

The data from this study derived from a transversal survey performed in July 2009 with children under 2 years of age in two Xavante villages (Pimentel Barbosa and Etênhiritipá), located in the Pimentel Barbosa Indigenous Reserve. At the time of the study, the population of these two villages totaled 660 individuals (51.8% residents of Pimentel Barbosa village), of which 39.8% (263) were under 10 years of age. The study did not employ specific sampling techniques in data collection, having the aim to include all children in the age range of interest. Only children with physical or mental deficiencies were excluded.

Children’s ages were calculated based on local health service records and personal identification documents in the possession of the families.

Data on place of residence, household composition, maternal education, and income were collected by means of structured interviews conducted by one of the authors and counting on the assistance of an Indigenous translator when necessary.

Weight and height measurements were taken in participants’ homes by professionals who were previously trained and standardized following the recommendations of Lohman et al.⁸8. Lohman TG, Roche AF, Martorell R. Anthropometric standardization reference manual. Champaign, IL: Human Kinetics; 1988.. Height measurements of children under two years of age were taken with a SECA 416 (Hamburg, Germany) infantometer and of the others with a SECA 214 anthropometer (Hamburg, Germany), both with a precision of 0.1 cm. Bodyweight was measured with a portable digital scale (SECA 872, Hamburg, Germany), with 150 kg capacity and 100 g precision. This scale has a mother/child weight function that allows children under 24 months of age to be weighed together with the mother or caretaker.

Hemoglobin blood concentration was measured for children over 6 months. A drop of blood was obtained from the fingertip using disposable lancets and Accu-Chek Softclix lancing device. Hemoglobin concentration was analyzed with the HemocueHb 201+ hemoglobinometer (Ängelholm, Sweden).

Children’s age was classified in the following groups: < 2 years, ≥ 2 and < 5 years, and ≥ 5 years. The variable place of residence was classified according to the child’s village of residence. The two villages were identified as 1 and 2, without their proper names to guarantee confidentiality.

Stature, weight, and age data were used to calculate z-scores of height-for-age (H/A), weight-for-age (W/A), and body mass index-for-age (BMI/A). Z-scores were generated using the Anthro software package (WHO Anthro 2011, Switzerland) based on the World Health Organization (WHO) reference population⁹9. WHO Multicentre Growth Reference Study Group. WHO Child Growth Standards: Length/height-for-age, weight-for-age, weight-for-length, weight-forheight and body mass index-for-age: methods and development. Geneva: World Health Organization; 2006.^,1010. de Onis M, Onyango AW, Borghi E, Siyam A, Nishida C, Siekmann J. Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ 2007; 85(9): 660-7.. Mother’s BMI was classified according to WHO guidelines¹¹11. World Health Organization (WHO). Physical status: the use and interpretation of anthropometry. Geneva: World Health Organization; 1995. (Technical Report Series No. 854). Maternal age was classified according to the following groups: < 18 years, ≥ 18 and < 30 years, and ≥ 30 years.

Household size was defined as the total number of residents in the child’s home, classified into two groups based on the median number of individuals (14.0). The median (4.0) was also used to classify into two groups the total number of children < 5 years in the home. Mother’s education was classified according to the number of years of school attended: 0 years, 1-4 years, 5-8 years, and > 8 years.

To calculate per capita income, regular monthly incomes (salaries, pensions, social assistance, social welfare benefits, and others) of all members of the household were summed and divided by the number of household members.

Classification of anemia utilized cut-off points proposed by the WHO, in addition to moderate (7-9 mg/dL) and severe (< 7 mg/dL) anemia¹²12. World Health Organization (WHO). Iron deficiency anaemia assessment, prevention, and control: a guide for programme managers. WHO/NHD/013; 2001.^,1313. DeMaeyer EM, organizador. Preventing and controlling iron deficiency anaemia through primary health care: a guide for health administrators and programme managers. Geneva: World Health Organization; 1989..

Student t-test was used to evaluate differences between averages and Chi-squared (χ²) and Fisher’s exact tests were used to evaluate differences in proportions (p ≤ 0.05). Some continuous variables, such as per capita income, BMI/A, H/A, and W/A, were categorized in quartiles. Initially, the association of each independent variable with hemoglobin level was evaluated by means of linear regression and with prevalence of anemia by means of Poisson regression. Independent variables showing p ≤ 0.20 in the unadjusted analyses were considered for inclusion in the final model.

Two models were constructed in the adjusted multivariate analysis: one with hemoglobin concentration as the outcome, using linear regression coefficient (β), and the other with anemia occurrence as the outcome, using Poisson regression with robust variance. The statistical significance of Poisson regression was determined with the Wald test, estimating adjusted prevalence ratios and respective 95% confidence intervals (95%CI). The suitability of multivariate linear regression was evaluated with the F test. Multivariate stepwise analysis was used to adjust for potentially confounding variables retained from bivariate analysis. After simultaneous inclusion of all principal effects, plausible interactions were tested. Statistical modeling was conducted with the software R package (www.r-project.org), version 3.0.1, with the epicalc and sandwich packages.

The study was approved by the Research Ethics Committee at the National School of Public Health, Oswaldo Cruz Foundation, the National Research Ethics Council (CONEP authorization No. 503/2006, process No. 25000.001840/2005-14), and the National Indian Foundation (FUNAI), in accordance with National Health Council recommendations in Resolutions 466/12 and 304/00.

RESULTS

Of a total of 263 children < 10 years of age resident in the two study villages, 257 (97.7%) were evaluated. Losses were due to absence at the time of the study (n = 3; 1.1%), data inconsistencies (n = 1; 0.4%), impossibility of data collection due to physical limitations of the child (n = 1; 0.4%), and refusal to participate (n = 1; 0.4%).

The lowest mean hemoglobin values were found among children < 2 years old, without significant difference between the sexes in any age group (Table 1). Anemia was observed in 50.8% of children and was more frequent among those < 2 years (77.8% for both sexes) and from 2 to 5 years (50.5%). Considering children < 5 years (n = 143; 55.4%), 62.2% had anemia (data not shown in table). Moderate and severe anemia also occurred with greater frequency in children < 2 years old (25.9% of the children in this age group). Among those < 2 years old, the proportion of cases classified as moderate or severe was 13.0%. The male sex showed higher percentages of anemia independently of age, but this difference was not significant (Table 1).

Child’s age was inversely associated with the occurrence of anemia (Table 2). Consequently, mean hemoglobin concentration levels increased significantly with each age increment. Children with H/A z-scores in the first quartile (z-score ≤ -1.82) showed the highest frequency of anemia (data not represented in table). A similar pattern was observed for the W/A index, as well as mean hemoglobin levels (Table 2).

Maternal age showed a direct association with children’s mean hemoglobin levels (Table 2). Maternal age ≥ 30 years resulted in an average increase of 1.15 mg/dL in the child’s hemoglobin concentration. However, an association between maternal and child anemia child was not detected.

Another factor associated with anemia and with mean hemoglobin concentration was presence of another child with anemia in the household (Table 2). On the other hand, mother’s educational level was inversely associated with hemoglobin concentration: 5-8 years of schooling resulted in an average decrease of 0.56 mg/dL in the child’s hemoglobin concentration. Also standing out among socioeconomic indicators was a direct association between per capita income and average hemoglobin concentration.

The variables tested and those that remained in the final model for hemoglobin concentration were the following: age group, H/A, presence of another child with anemia in the household, and per capita household income (Table 3). Together, these variables explained 32% of the variation in hemoglobin concentration among investigated children. All these variables except per capita household income also remained associated with anemia in the final model. The chance of children ≥ 5 years having anemia was reduced by 66.0% (PR adjusted = 0.60; 95%CI 0.38 - 0.95) when compared to the others. Having a better nutritional state as measured by H/A reduced the chance of having anemia by 1.8 times (PR adjusted = 0.59; 95%CI 0.34 - 1.00). Presence of another child in the household increased the chance of anemia by 52.9% (PR adjusted = 1.89; 95%CI 1.16 - 3.09) (Table 3).

DISCUSSION

The low hemoglobin levels and elevated prevalence of anemia observed among Xavante children find parallel in epidemiological studies conducted in other Indigenous groups in Brazil over the last decade⁴4. Orellana JDY, Coimbra Jr. CEA, Lourenço AEP, Santos RV. Nutritional status and anemia in Suruí Indian children, Brazilian Amazon. J Pediatr (Rio J) 2006; 82(5): 383-8.^,1414. Mondini L, Rodrigues DA, Gimeno SGA, Baruzzi RG. Estado nutricional e níveis de hemoglobina em crianças Aruak e Karibe - povos indígenas do Alto Xingu, Brasil Central, 2000-2002. Rev Bras Epidemiol 2009; 12: 469-77.^,1515. Mondini L, Canó EN, Fagundes U, Lima EES, Rodrigues D, Baruzzi RG. Condições de nutrição em crianças Kamaiurá - povo indígena do Alto Xingu, Brasil Central. Rev Bras Epidemiol 2007; 10(1): 39-47.^,1616. Morais PB, Alves GM dos S, 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): 383-9.. Previous surveys conducted in the Pimentel Barbosa Indigenous Reserve and other Xavante communities also point to elevated frequencies of anemia, reaching three quarters of all children¹⁷17. Coimbra Jr. CEA, Flowers NM, Salzano FM, Santos RV. The Xavánte in transition: health, ecology and bioanthropology in Central Brazil. Ann Arbor, MI: University of Michigan Press; 2002.. Thus, anemia is a prominent and persistent nutritional issue for Xavante children.

Comparing the prevalence of anemia among Indigenous children < 5 years old nationally (51.2%) and in the Central-West region (51.5%) with that documented in the present study (62.2%), the Xavante present a less favorable scenario⁶6. Leite MS, Cardoso AM, Coimbra Jr. CEA, Welch JR, Gugelmin SA, Lira PC, et al. Prevalence of anemia and associated factors among indigenous children in Brazil: results from the First National Survey of Indigenous People's Health and Nutrition. Nutr J 2013; 12: 69.. However, epidemiological studies of anemia among Indigenous children < 5 years old in communities in the Southeast and North regions of the country similarly showed prevalence rates higher than 60%³3. Barreto CTG, Cardoso AM, Coimbra Jr. CEA. Estado nutricional de crianças indígenas Guarani nos estados do Rio de Janeiro e São Paulo, Brasil. Cad Saúde Pública 2014; 30(3): 657-62.^,55. Pereira JF, Oliveira MAA, Oliveira JS. Anemia em crianças indígenas da etnia Karapotó. Rev Bras Saúde Mater Infant 2012; 12(4): 375-82..

Anemia prevalence rates among Xavante children are considerably higher when compared with the national non-Indigenous population, reaching a three-fold difference²2. Brasil, Ministério da Saúde. Pesquisa Nacional de Demografia e Saúde da Criança e da Mulher - PNDS 2006: dimensões do processo reprodutivo e da saúde da criança/Ministério da Saúde. Centro Brasileiro de Análise e Planejamento. Brasília: Ministério da Saúde; 2009.. Similarly expressive differences in the occurrence of anemia in Indigenous and non-Indigenous populations have also been observed in other countries. For example, based on a systematic review of anemia epidemiology in 13 countries, including Brazil, Khambalia et al.¹⁸18. Khambalia AZ, Aimone AM, Zlotkin SH. Burden of anemia among indigenous populations. Nutr Rev 2011; 69(12): 693-719.. showed that the prevalence is often higher among Indigenous peoples than among other segments of the population in the same country or region. These authors highlight that iron deficiency anemia is preventable and, most often, associated with food insecurity, poor sanitation, and a high burden of infectious and parasitic diseases¹⁸18. Khambalia AZ, Aimone AM, Zlotkin SH. Burden of anemia among indigenous populations. Nutr Rev 2011; 69(12): 693-719.. Likewise, diverse studies highlight that infectious and parasitic diseases, especially diarrhea and pneumonia, and undernutrition constitute the principal causes of disease and death among Xavante children. This scenario is consistent with the elevated prevalence of anemia observed in this study¹⁹19. Lunardi R, Santos RV, Coimbra Jr. CEA. Morbidade hospitalar de indígenas Xavante, Mato Grosso, Brasil (2000-2002). Rev Bras Epidemiol 2007; 10(4): 441-52.^,2020. Souza LG, Santos RV, Pagliaro H, Carvalho MS, Flowers NM, Coimbra Jr. CEA. Demography and health of the Xavante Indians of Central Brazil. Cad Saúde Pública 2011; 27(10): 1891-905.^,2121. 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..

Age of the child was an important explanatory factor for hemoglobin concentration and prevalence of anemia among the Xavante, which is comparable with observations from other studies of Indigenous⁴4. Orellana JDY, Coimbra Jr. CEA, Lourenço AEP, Santos RV. Nutritional status and anemia in Suruí Indian children, Brazilian Amazon. J Pediatr (Rio J) 2006; 82(5): 383-8.^,55. Pereira JF, Oliveira MAA, Oliveira JS. Anemia em crianças indígenas da etnia Karapotó. Rev Bras Saúde Mater Infant 2012; 12(4): 375-82.^,66. Leite MS, Cardoso AM, Coimbra Jr. CEA, Welch JR, Gugelmin SA, Lira PC, et al. Prevalence of anemia and associated factors among indigenous children in Brazil: results from the First National Survey of Indigenous People's Health and Nutrition. Nutr J 2013; 12: 69.^,1414. Mondini L, Rodrigues DA, Gimeno SGA, Baruzzi RG. Estado nutricional e níveis de hemoglobina em crianças Aruak e Karibe - povos indígenas do Alto Xingu, Brasil Central, 2000-2002. Rev Bras Epidemiol 2009; 12: 469-77. and non-Indigenous populations²²22. Oliveira MAA, Osório MM, Raposo MCF. Concentração de hemoglobina e anemia em crianças no Estado de Pernambuco, Brasil: fatores sócio-econômicos e de consumo alimentar associados. Cad Saúde Pública 2006; 22(10): 2169-78.^,2323. Osório MM. Fatores determinantes da anemia em crianças. J Pediatr (Rio J) 2002; 78(4): 269-78. in Brazil. The age group < 2 years old is recognized as the most vulnerable phase of life for nutritional and infectious disesases²⁴24. Ulijaszek SJ, Johnston FE, Preece MA. The Cambridge encyclopedia of human growth and development. Cambridge: Cambridge University Press; 1998.. Furthermore, this period is characterized by intense physical growth, which increases the demand for micronutrients such as iron, folic acid, and vitamin B12. Introduction of low iron foods during weaning and high prevalence of diarrhea and pneumonia are also important factors associated with childhood anemia²³23. Osório MM. Fatores determinantes da anemia em crianças. J Pediatr (Rio J) 2002; 78(4): 269-78.^,2424. Ulijaszek SJ, Johnston FE, Preece MA. The Cambridge encyclopedia of human growth and development. Cambridge: Cambridge University Press; 1998..

As observed in other studies⁶6. Leite MS, Cardoso AM, Coimbra Jr. CEA, Welch JR, Gugelmin SA, Lira PC, et al. Prevalence of anemia and associated factors among indigenous children in Brazil: results from the First National Survey of Indigenous People's Health and Nutrition. Nutr J 2013; 12: 69.^,1616. Morais PB, Alves GM dos S, 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): 383-9.^,1818. Khambalia AZ, Aimone AM, Zlotkin SH. Burden of anemia among indigenous populations. Nutr Rev 2011; 69(12): 693-719.^,2323. Osório MM. Fatores determinantes da anemia em crianças. J Pediatr (Rio J) 2002; 78(4): 269-78., Xavante children with linear growth deficits also showed higher prevalence of anemia, suggesting a relation between undernutrition and low hemoglobin levels. However, some studies conducted among Indigenous peoples⁵5. Pereira JF, Oliveira MAA, Oliveira JS. Anemia em crianças indígenas da etnia Karapotó. Rev Bras Saúde Mater Infant 2012; 12(4): 375-82.^,1818. Khambalia AZ, Aimone AM, Zlotkin SH. Burden of anemia among indigenous populations. Nutr Rev 2011; 69(12): 693-719.^,2525. Leite MS, Santos RV, Coimbra Jr. CEA, Gugelmin SA. Alimentação e nutrição dos povos indígenas no Brasil. In: Kac G, Sichieri R, Gigante DP, organizadores. Epidemiologia nutricional. Rio de Janeiro: Editora Ficoruz e Atheneu; 2007. p. 503-18. as well as among non-Indigenous peoples²⁶26. Lima ACVMS, Lira PIC, Romani SAM, Eickmann SH, Piscoya MD, Lima MC. Fatores determinantes dos níveis de hemoglobina em crianças aos 12 meses de vida na Zona da Mata Meridional de Pernambuco. Rev Bras Saúde Mater Infant 2004; 4(1): 35-43.^,2727. Spinelli MGN, Marchioni DML, Souza JMP, Souza SB, Szarfarc SC. Fatores de risco para anemia em crianças de 6 a 12 meses no Brasil. Rev Panam Salud Publica 2005; 17(2): 84-91.^,2828. Vasconcelos PN, Cavalcanti DS, Leal LP, Osório MM, Batista Filho M. Tendência temporal e fatores determinantes da anemia em crianças de duas faixas etárias (6-23 e 24-59 meses) no Estado de Pernambuco, Brasil, 1997-2006. Cad Saúde Pública 2014; 30(8): 1777-87. do not document this association, suggesting it is multicausal. The determination of nutritional status, including anemia, is related to numerous factors including socioeconomic condition, basic sanitation, occurrence of infectious and parasitic diseases, and diet, among others.

The relationship between sex and child anemia is also not uniform, with some studies indicating an association²⁷27. Spinelli MGN, Marchioni DML, Souza JMP, Souza SB, Szarfarc SC. Fatores de risco para anemia em crianças de 6 a 12 meses no Brasil. Rev Panam Salud Publica 2005; 17(2): 84-91.^,2929. Leal LP, Batista-Filho M, Lira PIC, Figueiroa JN, Osório MM. Prevalência da anemia e fatores associados em crianças de seis a 59 meses de Pernambuco. Rev Saúde Pública 2011; 45: 457-66. while others do not²²22. Oliveira MAA, Osório MM, Raposo MCF. Concentração de hemoglobina e anemia em crianças no Estado de Pernambuco, Brasil: fatores sócio-econômicos e de consumo alimentar associados. Cad Saúde Pública 2006; 22(10): 2169-78.. In the sample of children investigated in the First National Survey of Health and Nutrition of Indigenous Peoples, boys showed a higher chance of having anemia in Brazil⁶6. Leite MS, Cardoso AM, Coimbra Jr. CEA, Welch JR, Gugelmin SA, Lira PC, et al. Prevalence of anemia and associated factors among indigenous children in Brazil: results from the First National Survey of Indigenous People's Health and Nutrition. Nutr J 2013; 12: 69.. Among the Xavante, the frequency of anemia was greater among boys but the difference was small and not significant.

Concerning maternal characteristics, children of anemic and younger mothers were not shown be more anemic. Iron deficiency during pregnancy is generally associated with low birth weight and preterm birth.²³23. Osório MM. Fatores determinantes da anemia em crianças. J Pediatr (Rio J) 2002; 78(4): 269-78.^,2828. Vasconcelos PN, Cavalcanti DS, Leal LP, Osório MM, Batista Filho M. Tendência temporal e fatores determinantes da anemia em crianças de duas faixas etárias (6-23 e 24-59 meses) no Estado de Pernambuco, Brasil, 1997-2006. Cad Saúde Pública 2014; 30(8): 1777-87. In the case of the Xavante, the absence of a significant relation may be due to the fact that children tend to be born with adequate weight and only suffer growth deceleration in the third or fourth month of life³⁰30. Ferreira AA, Welch JR, Cunha GM, Coimbra Jr. CEA. Physical growth curves of Indigenous Xavante children in Central Brazil: results from a longitudinal study (2009-2012). Ann Hum Biol 2016; 43(4): 293-303.. However, mean hemoglobin levels in children showed a direct relationship with the mother’s age, consistent with findings from other studies of non-Indigenous and Indigenous children⁶6. Leite MS, Cardoso AM, Coimbra Jr. CEA, Welch JR, Gugelmin SA, Lira PC, et al. Prevalence of anemia and associated factors among indigenous children in Brazil: results from the First National Survey of Indigenous People's Health and Nutrition. Nutr J 2013; 12: 69.^,2929. Leal LP, Batista-Filho M, Lira PIC, Figueiroa JN, Osório MM. Prevalência da anemia e fatores associados em crianças de seis a 59 meses de Pernambuco. Rev Saúde Pública 2011; 45: 457-66.. Lower child hemoglobin concentration levels may be related to observation that younger mothers have greater chances of giving birth to children with low weight²⁷27. Spinelli MGN, Marchioni DML, Souza JMP, Souza SB, Szarfarc SC. Fatores de risco para anemia em crianças de 6 a 12 meses no Brasil. Rev Panam Salud Publica 2005; 17(2): 84-91.^,3131. Neuman NA, Tanaka OY, Szarfarc SC, Guimarães PRV, Victora CG. Prevalência e fatores de risco para anemia no Sul do Brasil. Rev Saúde Pública 2000; 34(1): 56-63..

Presence in the household of another child < 10 years with anemia was significantly associated with the occurrence of anemia. This relationship may result from the household environment shared by Xavante children, which involves mutual exposure to a common set of socioeconomic, physical, and dietary factors.

Among the socioeconomic variables analyzed in this study, maternal education and per capita income were shown to be determining factors for mean hemoglobin levels but not anemia occurrence. This pattern is consistent with what is observed in the national Indigenous and non-Indigenous populations, according to which maternal education and socioeconomic status operate as protective factors for the occurrence of anemia in children⁶6. Leite MS, Cardoso AM, Coimbra Jr. CEA, Welch JR, Gugelmin SA, Lira PC, et al. Prevalence of anemia and associated factors among indigenous children in Brazil: results from the First National Survey of Indigenous People's Health and Nutrition. Nutr J 2013; 12: 69.^,3131. Neuman NA, Tanaka OY, Szarfarc SC, Guimarães PRV, Victora CG. Prevalência e fatores de risco para anemia no Sul do Brasil. Rev Saúde Pública 2000; 34(1): 56-63.. As was mentioned above, there is a complex relationship between anemia and socioeconomic conditions, potentially intermediated by diverse factors including sanitation, infectious and parasitic diseases, and diet.

Different results for relationships between socioeconomic variables and the two indicators of iron deficiency, anemia and mean hemoglobin levels, among Xavante children should be interpreted not only in terms of their specific socioeconomic context, but also in light of studies recently undertaken with other Indigenous groups in Brazil that did not indicate a uniform relationship between traditional socioeconomic indicators and child health⁵5. Pereira JF, Oliveira MAA, Oliveira JS. Anemia em crianças indígenas da etnia Karapotó. Rev Bras Saúde Mater Infant 2012; 12(4): 375-82.^,2121. 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.^,3232. Cardoso AM, Coimbra Jr. CEA, Werneck GL. Risk factors for hospital admission due to acute lower respiratory tract infection in Guarani indigenous children in southern Brazil: a population-based case-control study. Trop Med Int Health 2013; 18(5): 596-607., possibly because local Indigenous economies often involve different dynamics from the national economy. Due to a tendency for physical and sanitation characteristics of Xavante households in Pimentel Barbosa village to be uniform, we did not evaluate other variables typically used to characterize the socioeconomic profile of rural households and commonly considered “protective” with regard to the anemia occurrence, such as type of flooring, roofing, waste disposal, and/or source of drinking water.

Other factors considered important in the determination of child anemia and hemoglobin levels, such as mother’s gestational age, birth weight, and breastfeeding, were not investigated in this study. This was mainly due to the impossibility of obtaining reliable data from local health services. Another limitation of this study is that it did not collect data that permitted identifying the etiology of anemia in Xavante children. However, it is very likely that the disease is due to a lack of dietary iron (iron deficiency anemia) given the local inexistence of malaria, a disease known to cause anemia, and the low prevalence of helminths such as hookworm, due to regular use of broad spectrum anthelmintics in the population³³33. Lira PCI, Ferreira LOC. Epidemiologia da anemia ferropriva. In: Kac G, Sichieri R, Gigante DP, organizadores. Epidemiologia nutricional. Rio de Janeiro: Editora Fiocruz e Atheneu; 2007. p. 337-23.^,3434. Batista Filho M, Souza AI, Bresani CC. Anemia como problema de saúde pública: uma realidade atual. Ciênc Saúde Coletiva 2008; 13(6): 1917-22.^,3535. Silva GMV. Parasitos intestinais na comunidade indígena Xavante de Pimentel Barbosa, Mato Grosso, Brasil [dissertação de Mestrado]. Rio de Janeiro: Escola Nacional de Saúde Pública Sergio Arouca/ FIOCRUZ; 2010.. Also, population genetics studies among the Xavante since the 1960s did not find sickle cell trait or any other indication of hereditary anemia¹⁷17. Coimbra Jr. CEA, Flowers NM, Salzano FM, Santos RV. The Xavánte in transition: health, ecology and bioanthropology in Central Brazil. Ann Arbor, MI: University of Michigan Press; 2002..

The high prevalence of anemia observed among Xavante children may find explanation in a series of factors including food insecurity, a high incidence of gastrointestinal infections, and limited access to health programs and services. The recent history of the Xavante people is marked by rapid and profound changes in ecology, subsistence and dietary patterns, and physical activity⁷7. Welch JR, Santos RV, Flowers NM, Coimbra Jr. CEA. Na Primeira Margem do Rio: Território e Ecologia do Povo Xavante de Wedezé. Rio de Janeiro: Museu do Índio/FUNAI; 2013.^,3636. Lucena JRM, Coimbra Jr. CEA, Silva CMFP, Welch JR. Prevalence of physical inactivity and associated socioeconomic indicators in indigenous Xavante communities in Central Brazil. BMC Nutr 2016; 2: 37.. These changes strongly affect children, especially those under 5 years of age, among whom almost 30% have linear growth deficits²¹21. 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.^,3030. Ferreira AA, Welch JR, Cunha GM, Coimbra Jr. CEA. Physical growth curves of Indigenous Xavante children in Central Brazil: results from a longitudinal study (2009-2012). Ann Hum Biol 2016; 43(4): 293-303.. Diarrhea accounts for approximately 75% of hospitalizations caused by infections and parasitic diseases, which are responsible for 20% of all hospitalizations¹⁹19. Lunardi R, Santos RV, Coimbra Jr. CEA. Morbidade hospitalar de indígenas Xavante, Mato Grosso, Brasil (2000-2002). Rev Bras Epidemiol 2007; 10(4): 441-52.. As is amply documented, diarrhea is an important factor in the determination of child nutritional status, including anemia. Data from the First National Survey of Health and Nutrition of Indigenous Peoples demonstrated the association between diarrhea and anemia in Indigenous children³⁷37. Escobar AL, Coimbra Jr. CEA, Welch JR, Horta BL, Santos RV, Cardoso AM. Diarrhea and health inequity among Indigenous children in Brazil: results from the First National Survey of Indigenous People's Health and Nutrition. BMC Public Health 2015; 15: 191., which finds support in the international literature³⁸38. Leal LP, Osório MM. Fatores associados à ocorrência de anemia em crianças menores de seis anos: uma revisão sistemática dos estudos populacionais. Rev Bras Saúde Mater Infant 2010; 10(4): 417-39.. It is also important to mention the National Iron Supplementation Program, an action developed in 2003 as part of the Indigenous Food and Nutrition Surveillance System (SISVAN Indígena)³⁹39. Caldas ADR, Santos RV. Vigilância alimentar e nutricional para os povos indígenas no Brasil: análise da construção de uma política pública em saúde. Physis 2012; 22(2): 545-65. and which for various reasons reaches less than half of the target population of Indigenous children under five years⁶6. Leite MS, Cardoso AM, Coimbra Jr. CEA, Welch JR, Gugelmin SA, Lira PC, et al. Prevalence of anemia and associated factors among indigenous children in Brazil: results from the First National Survey of Indigenous People's Health and Nutrition. Nutr J 2013; 12: 69..

CONCLUSION

Anemia constitutes an important health challenge for Indigenous children, with observed prevalence rates being much higher than in the rest of the Brazilian population in the same age group. It is a nutritional deficiency influenced by complex socioeconomic and demographic factors, as shown in the present study, with potentially important consequences for child growth and development. Identification of determinant factors for anemia in Indigenous populations, which do not always follow observed patterns in the general population, contributes to the development of specific actions that are appropriate for the particularities of these societies and thereby contribute to the improvement of sanitary and nutritional conditions and the reduction of disparities between health indicators for Indigenous and non-Indigenous people in Brazil. Specifically, our results call attention to a higher risk of anemia for children < 2 years with linear growth deficit and living with other anemic children, independently of the socioeconomic condition of the household.

ACKNOWLEDGMENTS

We thank the Xavante people from Pimentel Barbosa and Etênhiritipá villages, who welcomed us and supported our work. We are also grateful to the National Council for Scientific and Technological Development (CNPq) and to the Oswaldo Cruz Foundation (FIOCRUZ) for financial support.

References

Publication Dates

History