ABSTRACT

OBJECTIVE:

To describe the prevalence pattern of anemia among Indigenous children in Latin America.

METHODS:

PRISMA guidelines were followed. Records were identified from the databases PubMed, Google Scholar, and Lilacs by two independent researchers between May and June 2021. Studies were included if the following criteria were met: a) studied Indigenous people b) was about children (from 0 to 12 years old); c) reported a prevalence estimate of anemia; d) had been conducted in any of the countries of Latin America; e) was published either in English, Portuguese, or Spanish; f) is a peer-reviewed article; and g) was published at any date.

RESULTS:

Out of 2,401 unique records retrieved, 42 articles met the inclusion criteria. A total of 39 different Indigenous communities were analyzed in the articles, and in 21 of them (54.0%) child anemia was a severe public health problem (prevalence ≥ 40%). Those communities were the Aymara (Bolivia); Aruak, Guaraní, Kamaiurá, Karapotó, Karibe, Kaxinanuá, Ma-cro-Jê, Suruí, Terena, Xavante (Brazil); Cabécar (Costa Rica), Achuar, Aguaruna, Awajún, Urarina, Yomybato (Peru); Piaroa and Yucpa (Venezuela); and Quechua (Peru and Bolivia). Children below two years had the highest prevalence of anemia (between 16.2% and 86.1%). Among Indigenous people, risk factors for anemia include nutrition, poor living conditions, access to health services, racism, and discrimination. Bolivia and Guatemala are scarcely studied, despite having the highest proportion of Indigenous communities in Latin America.

CONCLUSIONS:

Anemia constitutes a poorly documented public health problem among Indigenous children in 21 Indigenous communities in Bolivia, Brazil, Colombia, Costa Rica, Ecuador, Guatemala, Mexico, and Peru. In all Indigenous communities included in this study child anemia was an issue, especially in younger children.

DESCRIPTORS:
Indigenous, South American; Child; Anemia, epidemiology; Risk Factors; Malnutrition; Poverty

INTRODUCTION

Anemia is a disorder in which the number of red blood cells is insufficient to meet the body's needs¹1 Organización Mundial de la Salud. Concentraciones de hemoglobina para diagnosticar la anemia y evaluar su gravedad. Ginebra (CH): OMS; 2011 [cited 2021 Oct 01]. Available from: https://apps.who.int/iris/handle/10665/85842
https://apps.who.int/iris/handle/10665/8... . Iron deficiency is the most common cause of anemia, but other nutritional deficiencies, acute and chronic inflammation, parasites, and inherited or acquired diseases that affect hemoglobin synthesis and red blood cell production or survival can cause anemia¹1 Organización Mundial de la Salud. Concentraciones de hemoglobina para diagnosticar la anemia y evaluar su gravedad. Ginebra (CH): OMS; 2011 [cited 2021 Oct 01]. Available from: https://apps.who.int/iris/handle/10665/85842
https://apps.who.int/iris/handle/10665/8... . It is the most common blood disorder in developing countries²2 McLean E, Cogswell M, Egli I, Wojdyla D, Benoist B. Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993-2005. Public Health Nutr. 2009;12(4):444-54. https://doi.org/10.1017/S1368980008002401
https://doi.org/10.1017/S136898000800240... and the health condition that affected the greatest number of people around the world (2.36 billion people) in 2015³3 GBD 2015 Disease and Injury Incidence and Prevalence Collaborators. Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet. 2016;388(10053):1542-602. https://doi.org/10.1016/S0140-6736(16)31678-6
https://doi.org/10.1016/S0140-6736(16)31... . Multiple factors often contribute to the etiology of anemia, and sociodemographic conditions play a key role, especially in low-income countries⁴4 World Health Organization. Nutritional anemias: tools for effective prevention. Geneva (CH): WHO; 2017.. For example, Leite et al.⁵5 Leite MS, Cardoso AM, Coimbra Jr CEA, Welch JR, Gugelmin SA, Lira PCI, 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(1):69. https://doi.org/10.1186/1475-2891-12-69
https://doi.org/10.1186/1475-2891-12-69... , who studied Indigenous children in Brazil, documented higher risk of anemia for boys, children with lower maternal schooling, lower household socioeconomic status, poorer sanitary conditions, presence of maternal anemia, and anthropometric deficits.

Numerous factors, ranging from a lack of accurate and easily accessible information to the very nature of Indigenous identities in Latin America and the Caribbean, hinder the determination of the exact number of Indigenous people in that region⁶6 World Bank Group. Indigenous Latin America in the twenty-first century: the first decade. Washington, DC; 2015 [cited 2021 Oct 01]. Available from: http://documents.worldbank.org/curated/en/145891467991974540/pdf/Indigenous-Latin-America-in-the-twenty-first-century-the-first-decade.pdf
http://documents.worldbank.org/curated/e... . To define Indigenous peoples in an efficient manner, the International Labor Organization (ILO) Convention 169 on Indigenous and Tribal Peoples in Independent Countries provides a definition that can be used to identify at least four dimensions within Indigenous peoples: recognition of identity, common origin, territoriality, and the linguistic and cultural dimension, which must be considered when establishing operational criteria⁷7 Comisión Económica para América Latina y el Caribe. Los pueblos indígenas en América Latina. Avances en el último decenio y retos pendientes para la garantía de sus derechos. Santiago de Chile: CEPAL; 2014 [cited 2021 Oct 01]. Available from: https://repositorio.cepal.org/bitstream/handle/11362/37050/4/S1420783_es.pdf
https://repositorio.cepal.org/bitstream/... . Around 58 million Indigenous people live in Latin America, constituting 9.8% of the population⁸8 Comisión Económica para América Latina y el Caribe. Los pueblos indígenas de América Latina – Abya Yala y la Agenda 2030 para el Desarrollo Sostenible: tensiones y desafíos desde una perspectiva territorial. Santiago de Chile: CEPAL; 2020 [cited 2021 Oct 01]. Available from: https://www.cepal.org/es/publicaciones/45664-pueblos-indigenas-america-latina-abya-yala-la-agenda-2030-desarrollo-sostenible
https://www.cepal.org/es/publicaciones/4... . The proportion of the population considered Indigenous in Latin America varies by country and ranges from 41.0% in Bolivia and Guatemala, to 0.5% in Brazil, and 0% in Uruguay⁶6 World Bank Group. Indigenous Latin America in the twenty-first century: the first decade. Washington, DC; 2015 [cited 2021 Oct 01]. Available from: http://documents.worldbank.org/curated/en/145891467991974540/pdf/Indigenous-Latin-America-in-the-twenty-first-century-the-first-decade.pdf
http://documents.worldbank.org/curated/e... . In many countries of the region, Indigenous children are in a highly vulnerable situation, due to very high infant mortality rates, alarming levels of malnutrition in the context of food insecurity, precarious access to water, and high prevalence of diarrheal infections⁹9 Comisión Económica para América Latina y el Caribe. El impacto del COVID-19 en los pueblos indígenas de América Latina-Abya Yala: entre la invisibilización y la resistencia colectiva. Santiago de Chile: CEPAL; 2020 [cited 2021 Oct 01]. Available from: https://repositorio.cepal.org/handle/11362/46543
https://repositorio.cepal.org/handle/113... . The situation has become a humanitarian crisis recognized by several national governments and this illustrates the dire state of Indigenous populations in many countries of Latin America. Until now, few studies from Latin America have considered the prevalence of anemia among Indigenous children. One is from Brazil¹⁰10 Lício JSA, Fávaro TR, Chaves CRMM. Anemia em crianças e mulheres indígenas no Brasil: revisão sistemática. Cienc Saude Colet. 2016;21(8):2571-81. https://doi.org/10.1590/1413-81232015218.00532015
https://doi.org/10.1590/1413-81232015218... and another includes only four countries from the region (Brazil, Guatemala, Mexico, and Venezuela)¹¹11 Khambalia AZ, Aimone AM, Zlotkin SH. Burden of anemia among indigenous populations. Nutr Rev. 2011;69(12):693-719. https://doi.org/10.1111/j.1753-4887.2011.00437.x
https://doi.org/10.1111/j.1753-4887.2011... . Other studies included either Indigenous children without reporting values of prevalence of anemia¹²12 Horta BL, Santos RV, Welch JR, Cardoso AM, Santos JV, Assis AMO, et al. 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(1):23. https://doi.org/10.1186/1475-9276-12-23
https://doi.org/10.1186/1475-9276-12-23... ,¹³13 Pan American Health Organization. Malnutrition in infants and young children in Latin America and the Caribbean: achieving the and Millennium Development Goals. Washington, DC: PAHO; 2008. or without differentiating among Indigenous and non-Indigenous children¹⁴14 Vázquez LI, Valera E, Villalobos M, Tous M, Arija V. Prevalence of anemia in children from Latin America and the Caribbean and effectiveness of nutritional interventions: systematic review and meta-analysis. Nutrients. 2019;11(1):183. https://doi.org/10.3390/nu11010183
https://doi.org/10.3390/nu11010183... –²⁰20 Mena-Meléndez L. Ethnoracial child health inequalities in Latin America: multilevel evidence from Bolivia, Colombia, Guatemala, and Peru. SSM Popul Health. 2020;12:100673. https://doi.org/10.1016/j.ssmph.2020.100673
https://doi.org/10.1016/j.ssmph.2020.100... .

Since anemia is an indicator of both poor health and poor nutrition²2 McLean E, Cogswell M, Egli I, Wojdyla D, Benoist B. Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993-2005. Public Health Nutr. 2009;12(4):444-54. https://doi.org/10.1017/S1368980008002401
https://doi.org/10.1017/S136898000800240... , combining evidence from the literature about the prevalence of anemia in Indigenous children in Latin American countries can provide valuable data to governments and public health policies. Consequently, our objective was to describe the prevalence pattern of anemia among Indigenous children in Latin America.

METHODS

Literature Search

PRISMA guidelines were followed, and the Systematic Review was registered in PROSPERO under the number CRD42022300601. Records were identified from the databases PubMed, Google Scholar, and Lilacs by two independent researchers between May and June 2021. The search strategy combined four main categories which correspond to the inclusion criteria (a) Indigenous people, b) children, c) anemia, and d) Latin America with the Boolean operator AND. Within the main categories we used MeSH terms (if available) and free text for different variations of the category topic, for instance, “children” OR “childhood”, etc. The names of Latin American countries and the names of some representative Indigenous communities in the region were additionally included. Despite the controversies about what Latin America is and that such a position cannot be entirely correct²¹21 Sánchez-Recio P. ¿Qué es América Latina? Concepto y extensión de su núcleo de certeza positiva. Kairós Rev Cienc Econ Jur Adm. 2019;2(3):30-41. https://doi.org/10.37135/kai.003.03.03
https://doi.org/10.37135/kai.003.03.03... , in this study Latin America includes the following countries: Argentina, Belize, Bolivia, Brazil, Colombia, Chile, Costa Rica, Ecuador, El Salvador, French Guyana, Guyana, Guatemala, Honduras, Mexico, Nicaragua, Panamá, Paraguay, Peru, Suriname, Uruguay, and Venezuela. The spelling of countries and the Indigenous communities were varied according to differences in common use, for example “Peru” and “Perú”. However, the different spelling of the words for other places such as Latin America, Central America, and South America was not included since the searches obtained with those search terms were equal; for example, search results with the terms “Latin America” and “América Latina” had the same results. The searches were run by combining the search terms with the Boolean operator “AND”. The different terms within each of the four categories already mentioned were listed separated by the Boolean operator “OR”.

Search terms in PubMed and Google Scholar: (Children OR Child OR Childhood OR Infant) AND (Anemia) AND (Central America OR South America OR Latin America OR Argentina OR Belize OR Belice OR Bélice OR Bolivia OR Brazil OR Brasil OR Colombia OR Chile OR Costa Rica OR Ecuador OR El Salvador OR Guatemala OR Guyana OR Guiana OR Honduras OR Mexico OR Méjico OR México OR Mejico OR Nicaragua OR Panama OR Panamá OR Paraguay OR Peru OR Perú OR Surinam OR Uruguay OR Venezuela) AND (Indigenous OR Mapuche OR Atacameña OR Guaraní OR Guarani OR Yanomami OR Tikuna OR Ticuna OR Zenú OR Zenu OR Nasa OR Pastos OR Pasto OR Emberá OR Emberá-chamí OR Embera OR Emberachami OR Aimara OR Aymara OR Bribris OR Cabecares OR Cabecar OR Ngobes OR Ngobe OR Guaimies OR Guaimi OR Quichua OR Quechua OR Kechua OR Kichwa OR Lencas OR Lenca OR Maya OR Mayas OR Pipiles OR Pipil OR Garifuna OR Xinka OR Jinca OR Ladino OR Lempira OR Intibuca OR La Paz OR Nahuas OR Zapotecas OR Zapoteca OR Mixtecas OR Mixteca OR Otomíes OR Otomí OR Otomi OR Tzotziles OR Tzotzil OR Tzeltales OR Tzeltal OR Mazahuas OR Mazahua OR Mazatecos OR Mazateca OR Huastecos OR Huasteca OR Choles OR Chol OR Purépechas OR Purecha OR Chinantecas OR Chinanteca OR Mixes OR Tlapanecos OR Tlapaneca OR Tarahumaras OR Taraumara OR Chorotega OR Cacaopera OR Matagalpa OR Kunas OR Kuna OR Ngobe-Bugle OR Wounaan OR Naso OR Charrúa OR Wayuu OR Wayu OR Wayú).

Search terms in Lilacs: 214 searches were made combining the search terms, as follows: 1. “Anemia” AND “child” AND each of the countries in Latin America; 2. “Anemia” AND “children” AND each of the countries in Latin America; 3. “Anemia” AND “child” AND each of the Indigenous communities; 4. “Anemia” AND “children” AND each of the Indigenous communities; and 5. “Anemia” AND “crianças” AND “indios”.

Inclusion and Exclusion Criteria

Studies were included if the following criteria were met: a) studied Indigenous people b) was about children (from 0 to 12 years old); c) reported a prevalence estimate of anemia; d) had been conducted in any of the countries of Latin America; e) was published either in English, Portuguese, or Spanish; f) is a peer-reviewed article; and g) was published at any date. PubMed, Google Scholar, and Lilacs searches were carried out with the defined search terms. Studies that did not met the previous criteria were not included in this systematic review. We sorted the search results in Google scholar by relevance and screened the first 200 hits, followed by the next 200 and so forth, until we were unable to find any more relevant results. Title and abstract screening were performed, and, in some cases, the methods section of the article was screened to make sure that the inclusion criteria were met. Duplicates were excluded and a full list of relevant articles was created for data extraction.

Data Extraction and Quality Assessment and Analysis

Relevant information from selected studies was recorded in a data extraction sheet according to the following categories: Study (title, author, year, journal), geographical location (country, region), type of study, study objective, dataset, sampling technique (random or convenience), date of data collection, sample size, age group, exposure, outcome, statistical methods used, study results, study conclusions, study limitations, and study recommendations. Afterwards, the description of selected studies was assessed according to the STROBE statement²²22 Vandenbroucke JP, Elm E, Altman DG, Gøtzsche PC, Mulrow CD, Pocock SJ, et al. Strengthening the Reporting of Observational Studies in Epidemiology (STROBE): explanation and elaboration. PLoS Med. 2007;4(10):e297. https://doi.org/10.1371/journal.pmed.0040297
https://doi.org/10.1371/journal.pmed.004... . Each item of the list was assigned one point: cross-sectional studies were evaluated over a total of 33 points and cohort studies over 35 points. For both types of studies, a threshold of 12 points was established to determine that they were of sufficient quality for consideration in this systematic review. The 12 points included: 1) gives a scientific background and rationale for the reported investigation; 2) states specific objectives, including any prespecified hypotheses; 3) describes the setting, locations, and relevant dates; 4) defines outcomes; 5) describes assessment methods; 6) shows the study size; 7) describes statistical methods; 8) gives the characteristics of study participants; 9) reports summary measures; 10) summarizes key results referring to study objectives; 11) gives a cautious overall interpretation of results; and 12) discuss the external validity of the study results. Thereafter, the systematic search and the study characteristics were analyzed. The descriptive analysis of the prevalence of anemia was grouped by country, by age range, and by Indigenous community.

RESULTS

Literature Search

The initial search yielded 174 records (Figure 1). Out of these, 42 articles met the eligibility criteria⁵5 Leite MS, Cardoso AM, Coimbra Jr CEA, Welch JR, Gugelmin SA, Lira PCI, 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(1):69. https://doi.org/10.1186/1475-2891-12-69
https://doi.org/10.1186/1475-2891-12-69... ,²³23 Cordero D, Aguilar AM, Casanovas C, Vargas E, Lutter CK. Anemia in Bolivian children: a comparative analysis among three regions of different altitudes. Ann N Y Acad Sci. 2019;1450(1):281-90. https://doi.org/10.1111/nyas.14038
https://doi.org/10.1111/nyas.14038... –⁶³63 Diez-Ewald M, Torres-Guerra E, Leets I, Layrisse M, Vizcaíno G, Arteaga-Vizcaíno M. Anemia en poblaciones indígenas del occidente de Venezuela. Invest Clin. 1999;40(3):191-202. and were included in the systematic review. A second reviewer independently replicated the searches. Scores ranged from 13 to 21 points for cross-sectional studies and the two cohort studies received scores of 21 and 35. All articles scored above the established threshold of 12 and thus were judged of good quality for inclusion in the subsequent analyses. Most articles included more than one sample taken to measure the prevalence of anemia. Therefore, Table 1 shows the different samples taken in all the studies, numbered from 1 to 133.

General Characteristics of the Studies

Selected articles were written one the following three languages: English (26, 61.9%), Spanish only (11, 26.2%), Portuguese only (5, 11.9%). The oldest article was published in 1987 and the newest in 2021. The articles covered 10 countries (Bolivia, Brazil, Chile, Colombia, Costa Rica, Ecuador, Guatemala, Mexico, Peru, and Venezuela), and the studies were conducted in 30 specific regions in Latin America. Cross-sectional studies were 40 (95.2%) and cohort studies, two²⁵25 Welch JR, Ferreira AA, Tavares FG, Lucena JRM, Oliveira MVG. Santos RV, et al. The Xavante Longitudinal Health Study in Brazil: objectives, design, and key results. Am J Hum Biol. 2020;32(2):e23339. https://doi.org/10.1002/ajhb.23339
https://doi.org/10.1002/ajhb.23339... ,³⁹39 Franco-Y E, Hertrampf-D E, Hazbún-G J, Segú-S S, Illanes-S JC, Palacios-S L, et al. Suplementación de hierro en lactantes mapuches de la Provincia de Cautin, Chile. Arch Latinoam Nutr. 1996;46(2):118-21.. Ten studies²³23 Cordero D, Aguilar AM, Casanovas C, Vargas E, Lutter CK. Anemia in Bolivian children: a comparative analysis among three regions of different altitudes. Ann N Y Acad Sci. 2019;1450(1):281-90. https://doi.org/10.1111/nyas.14038
https://doi.org/10.1111/nyas.14038... ,⁴⁰40 Cediel G, Perez E, Gaitán D, Sarmiento OL, Gonzalez L. Association of all forms of malnutrition and socioeconomic status, educational level and ethnicity in Colombian children and non-pregnant women. Public Health Nutr. 2020;23(S1):S51-8. https://doi.org/10.1017/S1368980019004257
https://doi.org/10.1017/S136898001900425... ,⁴⁶46 Ramírez-Luzuriaga MJ, Belmont P, Waters WF, Freire WB. Malnutrition inequalities in Ecuador: differences by wealth, education level and ethnicity. Public Health Nutr. 2020;23(S1):S59-67. https://doi.org/10.1017/S1368980019002751
https://doi.org/10.1017/S136898001900275... ,⁴⁸48 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-51S. https://doi.org/10.3945/ajcn.114.083857
https://doi.org/10.3945/ajcn.114.083857... –⁵¹51. De la Cruz-Góngora V, Villalpando S, Mundo-Rosas V, Shamah-Levy T. Prevalencia de anemia en niños y adolescentes mexicanos: comparativo de tres encuestas nacionales. Salud Publica Mex. 2013;55 Supl 2:180-9.,⁵⁴54 Rivera JA, Monterrubio EA, González-Cossio T, García-Feregrino R, García-Guerra A, Sepúlveda-Amor J. Nutritional status of indigenous children younger than five years of age in Mexico: results of a national probabilistic survey. Salud Publica Mex. 2003;45 Suppl 4:S466-76. https://doi.org/10.1590/s0036-36342003001000003
https://doi.org/10.1590/s0036-3634200300... ,⁵⁵55 Villalpando S, Shamah-Levy T, Ramírez-Silva CI, Mejía-Rodríguez F, Rivera JA. Prevalence of anemia in children 1 to 12 years of age: results from a nationwide probabilistic survey in Mexico. Salud Publica Mex. 2003;45 Supl 4:S490-8. https://doi.org/10.1590/s0036-36342003001000005
https://doi.org/10.1590/s0036-3634200300... ,⁵⁷57 Flores Bendezú J, Calderón J, Rojas B, Alarcón Matutti E, Gutiérrez C. Desnutrición crónica y anemia en niños menores de 5 años de hogares indígenas del Perú – análisis de la Encuesta Demográfica y de Salud Familiar 2013. An Fac Med. 2015;76(2):135. https://doi.org//10.15381/anales.v76i2.11139
https://doi.org//10.15381/anales.v76i2.1... used data from national databases such as the Mexican National Health and Nutrition Survey from 2012 or the 2010 Colombian Demographic and Health Survey.

The sample sizes diverged widely across the studies. The smallest sample size was 36⁴⁷47 Robalino Flores XR, Balladares Saltos AM, Guerendiain Margni ME, Morales Marín F. Anthropometric and hematological tests to diagnose nutritional deficiencies in schoolchildren of indigenous communities living in the Andean region of Ecuador. Rev Nutr. 2017;30(6):723-33. https://doi.org/10.1590/1678-98652017000600005
https://doi.org/10.1590/1678-98652017000... , whereas the largest sample sizes were from studies including secondary data from national databases; for example, the highest number was from the National Maternal and Child Health Surveys in Guatemala (n = 5,735)⁴⁸48 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-51S. https://doi.org/10.3945/ajcn.114.083857
https://doi.org/10.3945/ajcn.114.083857... . Age ranges varied greatly: some studies considered children only within a narrow age group, e.g., 6–24 months⁵²52 Aguirre Arenas J, Chávez Villasana A, Medina Carranza BE, García Villegas EA, Carrasco Quintero MR, Guarneros Soto N. Impacto del suministro de harina de maíz fortificada en la anemia de preescolares de zonas indígenas de México. Gac Sanit. 2013;27(6):541-4. https://doi.org/10.1016/j.gaceta.2013.04.013
https://doi.org/10.1016/j.gaceta.2013.04... , whereas other studies, included broader age ranges, e.g., 0–17 years old⁵⁸58 Anticona C, San Sebastian M. Anemia and malnutrition in indigenous children and adolescents of the Peruvian Amazon in a context of lead exposure: a cross-sectional study. Global Health Action. 2014;7(1):22888. https://doi.org/10.3402/gha.v7.22888
https://doi.org/10.3402/gha.v7.22888... . Most of the studies lacked separated data for boys and girls.

De Louize et al. carried out the most recent data collection on the prevalence of anemia in indigenous communities in 2017⁴⁵45 DeLouize AM, Liebert MA, Madimenos FC, Urlacher SS, Schrock JM, Cepon-Robins TJ, et al. Low prevalence of anemia among Shuar communities of Amazonian Ecuador. Am J Hum Biol. 2021;34(1):e23590. https://doi.org/10.1002/ajhb.23590
https://doi.org/10.1002/ajhb.23590... , followed by two articles that collected data in 2013²³23 Cordero D, Aguilar AM, Casanovas C, Vargas E, Lutter CK. Anemia in Bolivian children: a comparative analysis among three regions of different altitudes. Ann N Y Acad Sci. 2019;1450(1):281-90. https://doi.org/10.1111/nyas.14038
https://doi.org/10.1111/nyas.14038... ,⁵⁷57 Flores Bendezú J, Calderón J, Rojas B, Alarcón Matutti E, Gutiérrez C. Desnutrición crónica y anemia en niños menores de 5 años de hogares indígenas del Perú – análisis de la Encuesta Demográfica y de Salud Familiar 2013. An Fac Med. 2015;76(2):135. https://doi.org//10.15381/anales.v76i2.11139
https://doi.org//10.15381/anales.v76i2.1... ; all other studies collected data before 2013. Thirteen studies did not specify the date of data collection. Not all studies mentioned the name of the investigated Indigenous community. For example, studies including data from national databases considered the whole Indigenous population of the country without specifying the names of the different communities. The 42 articles of this systematic review included 39 Indigenous communities from Latin America (Table 2).

Prevalence of anemia was the outcome measured for this systematic review and all the studies presented it as a percentage. The main diagnostic tool used to identify anemia was the Hemocue⁶⁴64 Sanchis-Gomar F, Cortell-Ballester J, Pareja-Galeano H, Banfi G, Lippi G. Hemoglobin point-of-care testing: the HemoCue system. J Lab Autom. 2013;18(3):198-205. https://doi.org/10.1177/2211068212457560
https://doi.org/10.1177/2211068212457560... , and the other methods used were: Cyanmethemoglobin method³⁸38 Franco-Y E, Hertrampf-D E, Rodríguez de la B E, Illanes-S C, Palacios-S L, Llaguno-A S, et al. Nutrición de hierro en lactantes mapuches alimentados con leche materna (2a- etapa). Rev Chil Pediatr. 1990;61(5):248-52. https://doi.org/10.4067/S0370-41061990000500003
https://doi.org/10.4067/S0370-4106199000... ,³⁹39 Franco-Y E, Hertrampf-D E, Hazbún-G J, Segú-S S, Illanes-S JC, Palacios-S L, et al. Suplementación de hierro en lactantes mapuches de la Provincia de Cautin, Chile. Arch Latinoam Nutr. 1996;46(2):118-21.,⁴⁴44 Monge-Rojas R, Barrantes M, Holst I, Nuñez-Rivas H, Alfaro T, Rodríguez S, et al. Biochemical indicators of nutritional status and dietary intake in Costa Rican Cabécar Indian adolescents. Food Nutr Bull. 2005;26(1):3-16. https://doi.org/10.1177/156482650502600101
https://doi.org/10.1177/1564826505026001... ,⁴⁷47 Robalino Flores XR, Balladares Saltos AM, Guerendiain Margni ME, Morales Marín F. Anthropometric and hematological tests to diagnose nutritional deficiencies in schoolchildren of indigenous communities living in the Andean region of Ecuador. Rev Nutr. 2017;30(6):723-33. https://doi.org/10.1590/1678-98652017000600005
https://doi.org/10.1590/1678-98652017000... , Automated biometry⁴⁶46 Ramírez-Luzuriaga MJ, Belmont P, Waters WF, Freire WB. Malnutrition inequalities in Ecuador: differences by wealth, education level and ethnicity. Public Health Nutr. 2020;23(S1):S59-67. https://doi.org/10.1017/S1368980019002751
https://doi.org/10.1017/S136898001900275... , Haemogram test⁴³43 Cardona-Arias JA, Rivera-Palomino Y, Carmona-Fonseca J. Salud indígena en el siglo XXI: parásitos intestinales, desnutrición, anemia y condiciones de vida en niños del resguardo indígena Cañamomo-Lomaprieta, Caldas-Colombia. Med UIS. 2014;27(2):29-39., Ultralogic 800³⁷37 Franco-Y E, Rodríguez-B E, Espinoza R, Stekel A, Hertrampf-D E. Prevalencia de anemia por déficit de hierro en lactantes mapuches alimentados con leche materna. Rev Chil Pediatr. 1987;58(5):361-5., Coulter counter⁶²62 García-Casal MN, Leets I, Bracho C, Hidalgo M, Bastidas G, Gomez A, et al. Prevalence of anemia and deficiencies of iron, folic acid and vitamin B12 in an indigenous community from the Venezuelan Amazon with a high incidence of malaria. Arch Latinoam Nutr. 2008;58(1):12-8., EDTA tube⁶¹61 Verhagen LM, Incani RN, Franco CR, Ugarte A, Cadenas Y, Sierra Ruiz CI, et al. High malnutrition rate in Venezuelan Yanomami compared to Warao Amerindians and Creoles: significant associations with intestinal parasites and anemia. PLoS One. 2013;8(10):e77581. https://doi.org/10.1371/journal.pone.0077581
https://doi.org/10.1371/journal.pone.007... , and the Chromogenic method⁶³63 Diez-Ewald M, Torres-Guerra E, Leets I, Layrisse M, Vizcaíno G, Arteaga-Vizcaíno M. Anemia en poblaciones indígenas del occidente de Venezuela. Invest Clin. 1999;40(3):191-202.. Moreover, almost all the studies followed the recommendations of the World Health Organization to diagnose anemia among children (for children from 6 to 59 months: < 11.0 mg/dL; for children from 5 to 11 years old: < 11.5 mg/dL; and for children from 12 to 14 years old: < 12.0 mg/dL) (1). Two studies used other diagnostic thresholds⁵⁵55 Villalpando S, Shamah-Levy T, Ramírez-Silva CI, Mejía-Rodríguez F, Rivera JA. Prevalence of anemia in children 1 to 12 years of age: results from a nationwide probabilistic survey in Mexico. Salud Publica Mex. 2003;45 Supl 4:S490-8. https://doi.org/10.1590/s0036-36342003001000005
https://doi.org/10.1590/s0036-3634200300... ,⁶³63 Diez-Ewald M, Torres-Guerra E, Leets I, Layrisse M, Vizcaíno G, Arteaga-Vizcaíno M. Anemia en poblaciones indígenas del occidente de Venezuela. Invest Clin. 1999;40(3):191-202. (Table 1).

Prevalence of Anemia by Country and Indigenous Community

Bolivia, Brazil, and Peru showed the highest overall prevalence of anemia (Figure 2), with the highest values among Guaraní children from 6 to 11 months (88.9%) in five villages in the state of Rio de Janeiro (Sapukai, Parati-Mirim, Araponga, Sítio Rio Pequeno, and Mamanguá) and one village in the state of São Paulo (Boa Vista) in Brazil²⁸28 Barreto CTG, Cardoso AM, Coimbra Jr CEA. Estado nutricional de crianças indígenas Guarani nos estados do Rio de Janeiro e São Paulo, Brasil. Cad Saude Publica. 2014;30(3):657-62. https://doi.org/10.1590/0102-311X00117813
https://doi.org/10.1590/0102-311X0011781... . The lowest prevalence of anemia (0%) was observed in Bolivia among children between 11 and 12 years from the Aymara Indigenous community in Caranavi in the Taraco district situated on the shores of Lake Titicaca at a high altitude²⁴24 Teran G, Cuna W, Brañez F, Persson KEM, Rottenberg ME, Nylen S, et al. Differences in nutritional and health status in school children from the highlands and lowlands of Bolivia. Am J Trop Med Hyg. 2018;98(1):326-33. https://doi.org/10.4269/ajtmh.17-0143
https://doi.org/10.4269/ajtmh.17-0143... . The second lowest prevalence of anemia including boys and girls (4.5%) was found in Chile, among Mapuche children from 8 to 14 months old from rural areas in the province of Cautín³⁷37 Franco-Y E, Rodríguez-B E, Espinoza R, Stekel A, Hertrampf-D E. Prevalencia de anemia por déficit de hierro en lactantes mapuches alimentados con leche materna. Rev Chil Pediatr. 1987;58(5):361-5.. We found that the prevalence of anemia among Indigenous children has been reported in 10 countries in Latin America. However, almost one-third of the studies were from Brazil (13 studies). Also, from the 39 Indigenous communities included in this systematic review, only four were part of more than one study: Aymara (2 studies in Bolivia)²⁴24 Teran G, Cuna W, Brañez F, Persson KEM, Rottenberg ME, Nylen S, et al. Differences in nutritional and health status in school children from the highlands and lowlands of Bolivia. Am J Trop Med Hyg. 2018;98(1):326-33. https://doi.org/10.4269/ajtmh.17-0143
https://doi.org/10.4269/ajtmh.17-0143... ,⁶⁵65 Burke RM, Rebolledo PA, Aceituno AM, Revollo R, Iñiguez V, Klein M, et al. Effect of infant feeding practices on iron status in a cohort study of Bolivian infants. BMC Pediatr. 2018;18(1):107. https://doi.org/10.1186/s12887-018-1066-2
https://doi.org/10.1186/s12887-018-1066-... , Quechua (1 study in Bolivia²³23 Cordero D, Aguilar AM, Casanovas C, Vargas E, Lutter CK. Anemia in Bolivian children: a comparative analysis among three regions of different altitudes. Ann N Y Acad Sci. 2019;1450(1):281-90. https://doi.org/10.1111/nyas.14038
https://doi.org/10.1111/nyas.14038... , 1 study in Colombia⁴²42 Bolaños-Gallardo MV, Flórez Echeverry O, Bermúdez Escobar A, Hernández Sampayo L, Salcedo-Cifuentes M. Estado nutricional del hierro en niños de comunidades indígenas de Cali, Colombia. Rev Med Risaralda. 2014;20(2):101-6., and 1 study in Peru⁵⁸58 Anticona C, San Sebastian M. Anemia and malnutrition in indigenous children and adolescents of the Peruvian Amazon in a context of lead exposure: a cross-sectional study. Global Health Action. 2014;7(1):22888. https://doi.org/10.3402/gha.v7.22888
https://doi.org/10.3402/gha.v7.22888... ), Karapotó (2 studies in Brazil²⁷27 Campos SBG, Menezes RCE, Oliveira MAA, Silva DAV, Longo-Silva G, Oliveira JS, et al. Short stature in children of Karapotó ethnic background, São Sebastião, Alagoas, Brazil. Rev Paul Pediatr. 2016;34(2):197-203. https://doi.org/10.1016/j.rppede.2016.02.006
https://doi.org/10.1016/j.rppede.2016.02... ,³⁰30 Pereira JF, Oliveira MAA, Oliveira JS. Anemia in indigenous children of Karapotó ethnic backgrounds. Rev Bras Saude Matern Infant. 2012;12(4):375-82. Portuguese. https://doi.org/10.1590/S1519-38292012000400004
https://doi.org/10.1590/S1519-3829201200... ), and Xavante (2 studies in Brazil²⁵25 Welch JR, Ferreira AA, Tavares FG, Lucena JRM, Oliveira MVG. Santos RV, et al. The Xavante Longitudinal Health Study in Brazil: objectives, design, and key results. Am J Hum Biol. 2020;32(2):e23339. https://doi.org/10.1002/ajhb.23339
https://doi.org/10.1002/ajhb.23339... ,²⁶26 Ferreira AA, Santos RV, Souza JAM, Welch JR, Coimbra Jr CEA. Anemia e níveis de hemoglobina em crianças indígenas Xavante, Brasil Central. Rev Bras Epidemiol. 2017;20(1):102-14. https://doi.org/10.1590/1980-5497201700010009
https://doi.org/10.1590/1980-54972017000... ).

Prevalence of anemia among children is a severe public health problem in 54% (21 out of 39) of the Indigenous communities in Latin America included in this systematic review (prevalence ≥ 40%)⁴4 World Health Organization. Nutritional anemias: tools for effective prevention. Geneva (CH): WHO; 2017.. The Indigenous communities that showed prevalence of anemia above 40% were the Aymara (Bolivia); Aruak, Guaraní, Kamaiurá, Karapotó, Karibe, Kaxinanuá, Ma-cro-Jê, Suruí, Terena, Xavante (Brazil); Cabécar (Costa Rica); Achuar, Aguaruna, Awajún, Urarina, Yomybato (Peru); Piaroa and Yucpa (Venezuela); and Quechua (Peru and Bolivia) (Figure 3). The Aguaruna in Peru; the Guaraní, Kamaiurá, Karibe, Suruí, and Xavante in Brazil; the Aymara in Bolivia; and the Yucpa in Venezuela are Indigenous communities registering prevalence of anemia above 70%, leading the list in terms of anemia as a severe public health problem for young children.

DISCUSSION

This systematic review revealed an alarming situation regarding anemia in Indigenous communities in Latin America. Data obtained from Brazil confirm the gravity of the situation in the Indigenous population, with extremely high prevalence rates among children as described by Lício, Fávaro and Chaves¹⁰10 Lício JSA, Fávaro TR, Chaves CRMM. Anemia em crianças e mulheres indígenas no Brasil: revisão sistemática. Cienc Saude Colet. 2016;21(8):2571-81. https://doi.org/10.1590/1413-81232015218.00532015
https://doi.org/10.1590/1413-81232015218... , who allege that such information is essential to contribute to health care priorities in these communities.

We found that the prevalence of anemia among Indigenous children has been reported in 10 countries in Latin America. However, almost one-third of the studies were from Brazil (13 studies). As Licio et al.¹⁰10 Lício JSA, Fávaro TR, Chaves CRMM. Anemia em crianças e mulheres indígenas no Brasil: revisão sistemática. Cienc Saude Colet. 2016;21(8):2571-81. https://doi.org/10.1590/1413-81232015218.00532015
https://doi.org/10.1590/1413-81232015218... stated, since 2001, studies investigating the occurrence of anemia in Indigenous populations increased significantly in Brazil, occupying an important space in the health status and social inequalities debate. Indigenous communities in Brazil correspond to 0.5% of the entire population (820,000 inhabitants), whereas, for example, 41% of the country population in both Guatemala (5,880,000) and Bolivia (4,120,000) is considered Indigenous⁶6 World Bank Group. Indigenous Latin America in the twenty-first century: the first decade. Washington, DC; 2015 [cited 2021 Oct 01]. Available from: http://documents.worldbank.org/curated/en/145891467991974540/pdf/Indigenous-Latin-America-in-the-twenty-first-century-the-first-decade.pdf
http://documents.worldbank.org/curated/e... . Only one study from Guatemala and two from Bolivia could be included in this systematic review. However, we reported seven studies from Mexico and five from Peru which are the two countries with the highest numbers of Indigenous people in Latin America, namely 16,830,000 (40.3%) and 7,600,000 (18.2%) from a total Indigenous population of 41,810,000⁶6 World Bank Group. Indigenous Latin America in the twenty-first century: the first decade. Washington, DC; 2015 [cited 2021 Oct 01]. Available from: http://documents.worldbank.org/curated/en/145891467991974540/pdf/Indigenous-Latin-America-in-the-twenty-first-century-the-first-decade.pdf
http://documents.worldbank.org/curated/e... . In addition, from the 39 Indigenous communities included in this systematic review, only four of them appeared in more than one study: Aymara in Bolivia; Quechua in Bolivia, Colombia, and Peru; Karapotó and Xavante in Brazil. These results suggest that the data on specific Indigenous communities is scarce. Therefore, a consistent, collaborative approach is crucial to deliver medical research and care of Indigenous communities⁶⁶66 Babyar J. In search of Pan-American indigenous health and harmony. Global Health. 2019;15:16. https://doi.org/10.1186/s12992-019-0454-1
https://doi.org/10.1186/s12992-019-0454-... .

As stated above, numerous factors hinder the determination of the exact number of Indigenous people in Latin America; however, considering the existence of approximately 780 Indigenous groups⁶6 World Bank Group. Indigenous Latin America in the twenty-first century: the first decade. Washington, DC; 2015 [cited 2021 Oct 01]. Available from: http://documents.worldbank.org/curated/en/145891467991974540/pdf/Indigenous-Latin-America-in-the-twenty-first-century-the-first-decade.pdf
http://documents.worldbank.org/curated/e... , this means that this systematic review covered 5.0% of the Indigenous communities in the region. Therefore, studies about the situation of specific Indigenous communities in the region are lacking. We found studies about the prevalence of anemia among children but without making any distinction between non-Indigenous and Indigenous children: for example, a study by Vázquez et al. in 2019¹⁴14 Vázquez LI, Valera E, Villalobos M, Tous M, Arija V. Prevalence of anemia in children from Latin America and the Caribbean and effectiveness of nutritional interventions: systematic review and meta-analysis. Nutrients. 2019;11(1):183. https://doi.org/10.3390/nu11010183
https://doi.org/10.3390/nu11010183... showed that the overall prevalence of anemia in children from Latin America in general is 28.56%, and Mujica et al.¹⁶16 Mujica-Coopman MF, Brito A, López de Romaña D, Ríos-Castillo I, Coris H, Olivares M. Prevalence of anemia in Latin America and the Caribbean. Food Nutr Bull. 2015;36(2 Suppl):S119-28. https://doi.org/10.1177/0379572115585775
https://doi.org/10.1177/0379572115585775... found anemia prevalences from 4.0% to no more than 61.3% in children under six years of age based on 2014 data in Latin America and the Caribbean. Several researchers acknowledge that they have underrepresented Indigenous populations in Latin America, with significant underrepresentation of those groups in their research¹⁷17 San Sebastián M, Hurtig AK. Review of health research on indigenous populations in Latin America, 1995-2004. Salud Publica Mex. 2007;49(4):316-20. https://doi.org/10.1590/s0036-36342007000400012
https://doi.org/10.1590/s0036-3634200700... . We also found that studies including national databases present lower values of anemia prevalence among children compared with the studies specifically targeting Indigenous communities. Using data at the national level provides reliable information only for large geographic domains, thus it can provide information at the national level for the central government, but has less reliability for regional governments and is useless for local governments. Thus, governments and private organizations in Latin American countries should be aware that national databases could be masking extreme prevalences of anemia in vulnerable populations.

Furthermore, recent studies are lacking. Data for studies in all countries, except for Brazil, was outdated. Our findings show that the most recent data collection on prevalence of anemia from Indigenous communities was done in 2017, followed by 2016 and 2013. All other studies collected data before 2013, which means that currently (2021) recent data on the prevalence of anemia among Indigenous children in Latin America is awfully scarce. Moreover, reports covering a wide range of years are lacking. Since almost all the studies included in this systematic review were cross-sectional, possible causes of the prevalence of anemia cannot be determined. On the other hand, the lack of studies with longer-term follow-ups of specific Indigenous communities hinders monitoring of the course of child anemia and comparing anemia between different countries and regions.

Age groups: Our results indicate that the youngest children reported higher prevalence of anemia. The highest values were observed in the age groups between 6 and 35 months. Older children also showed high prevalence of anemia, but not as high as the youngest. For example, particularly among the Aruak people in Brazil, a very high number of children between six and 23 months old show moderate or severe anemia when compared with those between 24 and 59 months³²32 Mondini L, Rodrigues DA, Gimeno SGA, Baruzzi RG. Nutritional status and hemoglobin values of Aruak and Karibe Indian children: Upper Xingu, central Brazil. Rev Bras Epidemiol. 2009;12(3):469-77. https://doi.org/10.1590/S1415-790X2009000300015
https://doi.org/10.1590/S1415-790X200900... . In the Peruvian Amazon, anemia was more prevalent in the 0 to 5-year age group from the Achuar, Urarina, and Quichua Indigenous communities⁵⁸58 Anticona C, San Sebastian M. Anemia and malnutrition in indigenous children and adolescents of the Peruvian Amazon in a context of lead exposure: a cross-sectional study. Global Health Action. 2014;7(1):22888. https://doi.org/10.3402/gha.v7.22888
https://doi.org/10.3402/gha.v7.22888... .

Risk factors: This systematic review suggests several risk factors for high prevalence of anemia among Indigenous communities in Latin America. Babyar⁶⁶66 Babyar J. In search of Pan-American indigenous health and harmony. Global Health. 2019;15:16. https://doi.org/10.1186/s12992-019-0454-1
https://doi.org/10.1186/s12992-019-0454-... affirms that Indigenous populations in Latin America continue to suffer from health disparities compared with general populations. Particularly, in Brazil, Bolivia, Colombia, Ecuador, Peru, Paraguay, and Venezuela, approximately 200 Indigenous communities live in voluntary isolation, and the pressure over natural resources on their territory or in nearby areas puts them at risk of extreme vulnerability⁷7 Comisión Económica para América Latina y el Caribe. Los pueblos indígenas en América Latina. Avances en el último decenio y retos pendientes para la garantía de sus derechos. Santiago de Chile: CEPAL; 2014 [cited 2021 Oct 01]. Available from: https://repositorio.cepal.org/bitstream/handle/11362/37050/4/S1420783_es.pdf
https://repositorio.cepal.org/bitstream/... . According to Díaz Arana et al.⁵⁶56 Díaz A, Arana A, Vargas-Machuca R, Antiporta D. Situación de salud y nutrición de niños indígenas y niños no indígenas de la Amazonia peruana. Rev Panam Salud Publica. 2015;38(1):49-56. living conditions, access to healthcare, and nutritional status of children under five years of age are markedly different between the Indigenous population and the non-Indigenous population in Peru. Likewise, Ferreira et al.²⁶26 Ferreira AA, Santos RV, Souza JAM, Welch JR, Coimbra Jr CEA. Anemia e níveis de hemoglobina em crianças indígenas Xavante, Brasil Central. Rev Bras Epidemiol. 2017;20(1):102-14. https://doi.org/10.1590/1980-5497201700010009
https://doi.org/10.1590/1980-54972017000... found that Xavante children's high rates of anemia reveal an ethnic disparity between them and the Brazilian population in general, suggesting the causes of anemia are largely dependent on complex, variable relationships between socioeconomic, sociodemographic, and biological factors. In general, Indigenous peoples in Latin America have very limited access to health care services, often lacking geographical access, which means the closest health ward is far away from their communities. Moreover, they usually face obstacles in accessing health services due to mistrust generated by a history of racism and structural discrimination⁶⁷67 Oficina de Naciones Unidas para la Coordinación de Asuntos Humanitarios. Pueblos indígenas y COVID-19 en América Latina: un enfoque humanitario. New York: OCHA. 2020 [cited 2021 Oct 01]. Available from: https://reliefweb.int/report/bolivia-plurinational-state/pueblos-ind-genas-y-covid-19-en-am-rica-latina-un-enfoque
https://reliefweb.int/report/bolivia-plu... .

Besides, specific nutritional causes can be considered as risk factors for high prevalence of anemia. Franco et al.³⁷37 Franco-Y E, Rodríguez-B E, Espinoza R, Stekel A, Hertrampf-D E. Prevalencia de anemia por déficit de hierro en lactantes mapuches alimentados con leche materna. Rev Chil Pediatr. 1987;58(5):361-5. suggested that maternal milk might have a protective biologic role in preventing iron deficiency anemia among the Mapuche Indigenous community in Chile. Furthermore, Mujica et al.⁶⁸68 Mujica-C MF, Brito-O A, Castillo-Carniglia A, Olivares-G M, Hertrampf-D E. Consumo y valoración social de la leche purita fortificada y cereal del Programa Nacional de Alimentación Complementaria (PNAC) en Chile. Rev Chil Nutr. 2012;39(4):173-9. https://doi.org/10.4067/S0717-75182012000400010
https://doi.org/10.4067/S0717-7518201200... showed recently that the low prevalence of anemia in Chile is very likely a result of the iron-fortified milk provided by the National Complementary Feeding Program. The Aguarunas in Peru are also an example in which anemia prevalence is associated with their diet, based primarily on cassava and bananas, with little animal protein⁶⁰60 Huamán-Espino L, Valladares-E C. Estado nutricional y características del consumo alimentario de la población Aguaruna. Amazonas, Perú 2004. Rev Peru Med Exp Salud Publica. 2006;23(1):12-21.. On the other hand, in the case of the Yucpa Indigenous community in Venezuela, the high frequency of anemia without nutritional cause is attributed to the prevalence of infectious diseases such as hepatitis, parasites, and skin and respiratory tract infections⁶³63 Diez-Ewald M, Torres-Guerra E, Leets I, Layrisse M, Vizcaíno G, Arteaga-Vizcaíno M. Anemia en poblaciones indígenas del occidente de Venezuela. Invest Clin. 1999;40(3):191-202..

Prevention: Khambalia et al.¹¹11 Khambalia AZ, Aimone AM, Zlotkin SH. Burden of anemia among indigenous populations. Nutr Rev. 2011;69(12):693-719. https://doi.org/10.1111/j.1753-4887.2011.00437.x
https://doi.org/10.1111/j.1753-4887.2011... identified iron deficiency, malaria, and helminth infections as the three main causes of anemia among Indigenous populations, which can be addressed by a combination of interventions, such as fortification of staple foods with iron and other micronutrients, iron supplements targeted to risk groups, use of insecticide-treated materials and bed nets, deworming (anthelminthics) in risk groups, and prevention and treatment of malaria. Anemia can also be prevented and controlled by fully immunizing children; treating communicable diseases; managing obstetric complications, particularly excessive bleeding; and using modern family planning methods. For the first six months of a child's life, breastfeeding must be the sole basis for feeding, iron-rich foods should be given as a supplement, and sanitation facilities must be improved¹¹11 Khambalia AZ, Aimone AM, Zlotkin SH. Burden of anemia among indigenous populations. Nutr Rev. 2011;69(12):693-719. https://doi.org/10.1111/j.1753-4887.2011.00437.x
https://doi.org/10.1111/j.1753-4887.2011... .

Public policies: Several health programs and policies have been implemented in Latin American countries in the past two decades to generally address anemia as a public health problem¹⁴14 Vázquez LI, Valera E, Villalobos M, Tous M, Arija V. Prevalence of anemia in children from Latin America and the Caribbean and effectiveness of nutritional interventions: systematic review and meta-analysis. Nutrients. 2019;11(1):183. https://doi.org/10.3390/nu11010183
https://doi.org/10.3390/nu11010183... . However, Indigenous communities continue experiencing difficult situations. According to CEPAL⁹9 Comisión Económica para América Latina y el Caribe. El impacto del COVID-19 en los pueblos indígenas de América Latina-Abya Yala: entre la invisibilización y la resistencia colectiva. Santiago de Chile: CEPAL; 2020 [cited 2021 Oct 01]. Available from: https://repositorio.cepal.org/handle/11362/46543
https://repositorio.cepal.org/handle/113... , Guatemala has the highest proportion of Indigenous population living in municipalities with high or critical vulnerability (77.9%); Colombia (65.8%) follows in the list, then Mexico (38.8%), Peru (33%), and finally Chile (20.9%). Beyond this variability, a common pattern is the inequality affecting Indigenous peoples, with the widest gaps found in Colombia and Mexico. Although inequalities are also systematic within municipalities, the vulnerability index among Indigenous populations seems to always be higher than that estimated for non-Indigenous populations⁹9 Comisión Económica para América Latina y el Caribe. El impacto del COVID-19 en los pueblos indígenas de América Latina-Abya Yala: entre la invisibilización y la resistencia colectiva. Santiago de Chile: CEPAL; 2020 [cited 2021 Oct 01]. Available from: https://repositorio.cepal.org/handle/11362/46543
https://repositorio.cepal.org/handle/113... . The Indigenous peoples of Latin America and the Caribbean continue to experience political, social, and economic marginalization that has relegated them to conditions of poverty and extreme poverty⁶⁷67 Oficina de Naciones Unidas para la Coordinación de Asuntos Humanitarios. Pueblos indígenas y COVID-19 en América Latina: un enfoque humanitario. New York: OCHA. 2020 [cited 2021 Oct 01]. Available from: https://reliefweb.int/report/bolivia-plurinational-state/pueblos-ind-genas-y-covid-19-en-am-rica-latina-un-enfoque
https://reliefweb.int/report/bolivia-plu... . This is mainly expressed in the adoption of sectoral laws that subordinate Indigenous rights to business and state interests, and in implementation gaps, particularly in delimitating, demarcating, and titling lands⁷7 Comisión Económica para América Latina y el Caribe. Los pueblos indígenas en América Latina. Avances en el último decenio y retos pendientes para la garantía de sus derechos. Santiago de Chile: CEPAL; 2014 [cited 2021 Oct 01]. Available from: https://repositorio.cepal.org/bitstream/handle/11362/37050/4/S1420783_es.pdf
https://repositorio.cepal.org/bitstream/... .

Indigenous communities should be seriously considered in national programs to reduce anemia since, as Vázquez et al.¹⁴14 Vázquez LI, Valera E, Villalobos M, Tous M, Arija V. Prevalence of anemia in children from Latin America and the Caribbean and effectiveness of nutritional interventions: systematic review and meta-analysis. Nutrients. 2019;11(1):183. https://doi.org/10.3390/nu11010183
https://doi.org/10.3390/nu11010183... said, anemia prevalence was reduced in Latin American countries only by national programs that covered a wide geographical area, were well monitored, and were extended over time. According to the United Nations Office for the Coordination of Humanitarian Affairs⁶⁷67 Oficina de Naciones Unidas para la Coordinación de Asuntos Humanitarios. Pueblos indígenas y COVID-19 en América Latina: un enfoque humanitario. New York: OCHA. 2020 [cited 2021 Oct 01]. Available from: https://reliefweb.int/report/bolivia-plurinational-state/pueblos-ind-genas-y-covid-19-en-am-rica-latina-un-enfoque
https://reliefweb.int/report/bolivia-plu... , the purchasing power of Indigenous peoples to access basic commodities, including food, has even been recently decreasing due to quarantine and social mobility limitation measures dictated by governments to contain the SARS-CoV-2 pandemic, thus increasing the risk of food insecurity, particularly in areas where subsistence activities based on traditional land-based livelihoods are not an option. Despite the state responses aimed at containing and mitigating the impact of COVID-19 on Indigenous peoples and the 285 social protection measures adopted in Latin America, the state responses to date have not been tailored to the needs of Indigenous people⁶⁷67 Oficina de Naciones Unidas para la Coordinación de Asuntos Humanitarios. Pueblos indígenas y COVID-19 en América Latina: un enfoque humanitario. New York: OCHA. 2020 [cited 2021 Oct 01]. Available from: https://reliefweb.int/report/bolivia-plurinational-state/pueblos-ind-genas-y-covid-19-en-am-rica-latina-un-enfoque
https://reliefweb.int/report/bolivia-plu... . In addition, the traditional territories of 108 Indigenous peoples in Latin America straddle national boundaries, which means that cooperation and cohesive strategies between governments are needed to design policies to tackle child anemia as a public health problem.

Strengths and Limitations of the Study

The main strength of this study is that it is a systematic review, covering a large geographical area where Indigenous populations are common. Also, it recovers data about specific Indigenous communities and national databases. It provides detailed information about the different samples from all the studies about the prevalence of anemia among Indigenous children performed in the last 35 years in Latin America. Nevertheless, it has some limitations. First, we included only articles that explicitly mentioned any Indigenous community in Latin America. Other articles that did not mention that they were studying Indigenous populations or that Indigenous people were part of the overall study sample may have been overlooked. Second, mainly cross-sectional studies were available, which disallows the establishment of causal relationships. Third, as designed, the National Surveys do not provide information about specific Indigenous ethnic groups. Fourth, this systematic review only included data about the prevalence of anemia among Indigenous children. Combining these data with other studies about malnutrition is important to better understand the relationship between the prevalence of anemia and malnutrition in Indigenous children in Latin America. Fifth, limitations in the evaluation of the quality of articles in this systematic review are possible. The STROBE statement was only a guideline for reporting observational studies, not precisely a quality assessment tool. Therefore, we did not exactly assess for the quality of the selected articles, we just gave scores to a description of each selected study.

Recommendations

We recommend further studies update and extend the overview on anemia as a public health problem in Indigenous communities in Latin America. Besides, studies about the prevalence of anemia among Indigenous children should be combined with other studies about malnutrition to raise more information about how to prevent child anemia. Nutrition programs directed to Indigenous communities should be adjusted to the way of living of these populations without disturbing their cultural traditions. Also, exploring social acceptance, community willingness, and participation of Indigenous populations in nutrition programs is important. Finally, assessing the Indigenous community leaders’ ability to get involved in research and nutrition programs is necessary.

CONCLUSIONS

Anemia constitutes a severe and poorly documented public health problem among Indigenous children in 21 Indigenous communities in Bolivia, Brazil, Colombia, Costa Rica, Ecuador, Guatemala, Mexico, and Peru. All Indigenous communities included in this study showed child anemia as a public health problem, especially in younger children.

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