Stunting in children under five years old is still a health problem in the Western Brazilian Amazon: a population-based study in Assis Brasil, Acre, Brazil

Nanismo em crianças menores de cinco anos de idade ainda é um problema de saúde na Amazônia Ocidental Brasileira: um estudo de base populacional em Assis Brasil, Acre, Brasil

Saulo Augusto Silva Mantovani Alanderson Alves Ramalho Thasciany Moraes Pereira Fernando Luiz Cunha Castelo Branco Humberto Oliart-Guzmán Breno Matos Delfino Athos Muniz Braña Antonio Camargo Martins José Alcântara Filgueira-Júnior Ana Paula Santos ... About the authors

Abstract

Despite the process of nutritional transition in Brazil, in some places, such as the Amazon region, stunting is still an important public health problem. We identified the prevalence and factors associated with stunting in children under five years old residing in the urban area of Assis Brasil. A survey was conducted in which a questionnaire on socioeconomic, maternal and children’s conditions was applied, and height or length was measured. The children with height for age index below -2 Z-scores were considered stunted, according to the criteria by the World Health Organization. Four hundred and twenty-eight children were evaluated. Of these, 62 were stunted. Factors associated with stunting, according to adjusted models, were: the presence of open sewer, the wealth index for households, the receipt of governmental financial aid and the mother’s height, age and education. Therefore, it was observed that family and the mother’s characteristics as well as environmental and socioeconomic factors were closely related to the occurrence of stunting in the population studied, and such nutritional disturbance is still a health problem in the Brazilian Amazon.

Nutritional status; Nutritional deficiency; Child health; Stunting

Resumo

Apesar do processo de transição nutricional no Brasil, em alguns lugares, como a região amazônica, o nanismo ainda é um importante problema de saúde pública. Identificou-se a prevalência e fatores associados ao déficit de crescimento em crianças menores de cinco anos de idade residentes na área urbana de Assis Brasil. Um inquérito foi realizado utilizando instrumento semiestruturado sobre características socioeconômicas, maternas e das crianças, e foram aferidas medidas antropométricas. As crianças com índice de estatura para idade inferior a -2 escores-Z foram consideradas com déficit de crescimento, de acordo com os critérios da Organização Mundial da Saúde. Quatrocentos e vinte e oito crianças foram avaliadas. Destas, 62 apresentaram déficit de crescimento. Os fatores associados à baixa estatura, de acordo com modelos ajustados, foram: presença de esgoto a céu aberto, índice de riqueza para as famílias, recebimento de ajuda financeira governamental, altura materna, idade e escolaridade maternas. Portanto, observou-se que as características familiares e da mãe, bem como fatores ambientais e socioeconômicos estavam intimamente relacionados com a ocorrência de déficit de crescimento na população estudada, e que a desnutrição ainda é um problema de saúde na Amazônia brasileira.

Estado nutricional; Deficiência nutricional, Saúde da criança; Stunting

Introduction

The height-for-age index measures linear growth and its deficit indicates that height increase has been compromised by the cumulative effect of inadequate living, health and nutritional conditions. Because it is associated with long-term processes, it reflects chronic forms of undernutrition, and it is, therefore, a good indicator of chronic undernutrition, having been used in several surveys on child nutrition11. Souza OF, Benício MHD, Castro TG, Muniz PT, Cardoso MA. Desnutrição em crianças menores de 60 meses em dois municípios do Estado do Acre: prevalência e fatores associados. Rev Bras Epidemiol 2012; 15(1):211-221.

2. Araújo TS. Desnutrição infantil em Jordão, Estado do Acre, Amazônia Ocidental Brasileira [thesis]. São Paulo: Faculdade de Saúde Pública da USP; 2010.
-33. Cobayashi F, Augusto RA, Lourenço BH, Muniz PT, Cardoso MA. Factors associated with stunting and overweight in Amazonian children: a population-based, cross-sectional study. Public Health Nutr 2013; 17(3):551-560.. Individuals with height-for-age Z-score <-2 in relation to the World Health Organization growth curves are considered stunted44. World Health Organization (WHO). WHO child growth standards based on length/height, weight and age. Acta Paediatr Suppl 2006; 450:76-85..

Chronic child undernutrition remains a major morbidity in children under five years old, with approximately 165 million children in this age group being affected by stunting worldwide in 201155. Black RE, Victora CG, Walker SP, Bhutta ZQA, Christian P, Onis M, Ezzati M, Grantham-McGregor S, Katz J, Martorell R, Uauy R; Maternal and Child Nutrition Study Group. Maternal and child undernutrition and overweight in low-income and middle-income countries. Lancet 2013; 382(9890):427-451..

In Brazil, the prevalence of child undernutrition (stunting) in 1996 was 13.5%, decreasing to 6.8% in 2006/766. Monteiro CA, Benicio MHD, Conde WL, Konno S, Lovadino AL, Barros AJD, Victora CG. Narrowing socioeconomic inequality in child stunting: the Brazilian experience, 1974-2007. Bull World Health Organ 2010; 88:305-311.. Concomitantly, there was an increase in excess weight in children, suggesting that Brazil is undergoing the nutrition transition. However, this process occurs unevenly in the country77. Victora CG, Aquino EML, Leal MC, Monteiro CA, Barros FC, Szwarcwald CL. Maternal and child health in Brazil: progress and challenges. Lancet 2011; 377(9780):1863-1876.. In 2006, the prevalence of stunting in children under five years old was 7.0% for Brazil and 14.9% in the Northern Region88. Ministério da Saúde (MS). PNDS 2006: Pesquisa Nacional de Demografia e Saúde da Criança e da Mulher. Brasília: Ministério da Saúde, 2008. [cited 2013 Dec 1]. Available in: http://bvsms.saude.gov.br/bvs/pnds/img/relatorio_final_PNDS2006_04julho2008.pdf
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, showing the great disparity between the Amazon region and the rest of the country, even in the 21st century.

Acre, located in the Brazilian Amazon, is one of the Brazilian states where the effects of socioeconomic conditions on health are still quite evident. Studies conducted in the early 2000s in Acre state11. Souza OF, Benício MHD, Castro TG, Muniz PT, Cardoso MA. Desnutrição em crianças menores de 60 meses em dois municípios do Estado do Acre: prevalência e fatores associados. Rev Bras Epidemiol 2012; 15(1):211-221.,22. Araújo TS. Desnutrição infantil em Jordão, Estado do Acre, Amazônia Ocidental Brasileira [thesis]. São Paulo: Faculdade de Saúde Pública da USP; 2010. showed a child undernutritional prevalence rate that was higher than the national average77. Victora CG, Aquino EML, Leal MC, Monteiro CA, Barros FC, Szwarcwald CL. Maternal and child health in Brazil: progress and challenges. Lancet 2011; 377(9780):1863-1876.,88. Ministério da Saúde (MS). PNDS 2006: Pesquisa Nacional de Demografia e Saúde da Criança e da Mulher. Brasília: Ministério da Saúde, 2008. [cited 2013 Dec 1]. Available in: http://bvsms.saude.gov.br/bvs/pnds/img/relatorio_final_PNDS2006_04julho2008.pdf
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. In 2005, the prevalence of stunting in children under five years old in inner Acre was 35.8%22. Araújo TS. Desnutrição infantil em Jordão, Estado do Acre, Amazônia Ocidental Brasileira [thesis]. São Paulo: Faculdade de Saúde Pública da USP; 2010..

In this study, we evaluated the prevalence of stunting in Assis Brasil, located on the border between Acre and Peru and Bolivia, and its associated factors, providing data for planning preventive public health actions targeted at the Amazonian reality.

Material and methods

Study area

Assis Brasil is located on the Acre River Valley, 550.4 km southwest of Rio Branco, the capital of Acre state. It occupies an area of 4,974 km2, and borders the city of Brasileia to the east, the cities of Iñapari (Peru) and Bolpebra (Bolivia) to the south, and the municipality of Sena Madureira to the north. In 2010, Assis Brasil had a total population (urban and rural) of 6,017 (3,057 men and 2,960 women), of whom 12.7% were aged with less than 5 years99. Instituto Brasileiro de Geografia e Estatística. Resultados parciais do Estado do Acre no Censo 2010. Instituto Brasileiro de Geografia e Estatística; 2010. [cited 2011 Jan 1]. Available in: http://www.ibge.gov.br/home/estatistica/populacao/censo2010/tabelas_pdf/total_populacao_acre.pdf
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.

Study population and design

We conducted a population-based study with all children living in the urban area of Assis Brasil in 2011. These children were located by using the census records of the only Public Health Unit, which included all children at this age living in the urban area. There were 454 children identified by the Health system, and we were able to interview all 454 children. However, 26 children were excluded from the study because they were not submitted to the nutritional exam, resulting in a minimal loss of 5.72%.

The study was conducted with a cross-sectional epidemiological design. Data collection occurred between January and February 2011 by applying a questionnaire to investigate maternal, children and socioeconomic characteristics, as well as household and environmental characteristics. Maternal characteristics were collected from the children’s female caregiver (biological mother, grandmother, stepmother or other), except for weight and height, which were collected only from the biological mother.

The length of children under two years old was obtained by using a portable infantometer with 0.1-cm accuracy placed on a smooth surface. The height of children over two years old was measured using a wooden stadiometer with 0.1-cm accuracy and mounted on a wall without footer at a 90° angle in relation to the floor. All anthropometric measurements were performed in duplicate. When the two measurements were discrepant, a third measurement was performed, and the two closest ones were selected. For the analysis, the mean of the duplicate measurements generated the height-for-age index. Values from the World Health Organization44. World Health Organization (WHO). WHO child growth standards based on length/height, weight and age. Acta Paediatr Suppl 2006; 450:76-85. were used as reference and calculated by using the Anthro software v.3.2.2 (Department of Nutrition, WHO, Geneva). The cutoff point used for stunting was ≤ -2 Z scores1010. World Health Organization Expert Committee on Physical Status. Physical status: the use and interpretation of anthropometry: report of a WHO Expert Committee. Geneva: World Health Organization; 1995. [cited 2013 Dec 1]. Available in: http://www.who.int/childgrowth/publications/physical_status/en/
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. The same routine used to measure the height of children older than two years was used for the biological mother’s height (whether or not she was the current caregiver), while weight was estimated on a portable digital scale (Plenna ®) with 100-g precision and maximum capacity of 150 kg, using the values from the World Health Organization as reference1111. World Health Organization. Obesity: Preventing and Managing the Global Epidemic. Geneva: World Health Organization; 1998. [cited 2013 Dec 1]. Available in: http://www.who.int/nutrition/publications/obesity/WHO_TRS_894/en/
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. The anthropometric measurements of 26 children were not performed, and they were excluded from the analysis. These excluded children differed from the others for being predominantly of indigenous origin (p = 0.001), for being mostly from the lower stratum of the socioeconomic index (p = 0.001), for receiving governmental financial assistance (p = 0.017) and for having mothers who did not attend school (p < 0.001).

Statistical analysis

Wealth index: a wealth index was established for each household, as described by Filmer and Pritchett1212. Filmer D, Pritchett LH. Estimating wealth effects without expenditure data - or tears: an application to educational enrollments in states of India. Demography 2001; 38(1):115-132., using principal component analysis by the XLSTAT software, version 7.5.2 (Addinsoft, New York, NY). The creation of the wealth index was based on the presence of 21 consumer goods (TV, radio, DVD player, gas cooker, fridge, washing machine, landline telephone, bicycle, blender, electric iron, car, sofa, satellite dish , mobile telephone, motorcycle, computer, boat, boat motor, water well, power generator and microwave oven) as described in previous studies1010. World Health Organization Expert Committee on Physical Status. Physical status: the use and interpretation of anthropometry: report of a WHO Expert Committee. Geneva: World Health Organization; 1995. [cited 2013 Dec 1]. Available in: http://www.who.int/childgrowth/publications/physical_status/en/
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,1111. World Health Organization. Obesity: Preventing and Managing the Global Epidemic. Geneva: World Health Organization; 1998. [cited 2013 Dec 1]. Available in: http://www.who.int/nutrition/publications/obesity/WHO_TRS_894/en/
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. The first principal component explained 51.77% of the total variance. The scores of each variable were summed to estimate the wealth index, which was stratified into quartiles and later in two groups (the poorer half and the richer half).

Exploratory analysis. The database was created by using the SPSS 13.0 software (SPSS Inc., Chicago, IL). Crude analysis utilizing the Stata software, version 10 (StataCorp, College Station, TX) was performed by examining potential associated factors and confusion. Factors associated with stunting were identified by adjusted models using the conceptual model (Chart 1) adapted from previous studies1313. Muniz PT, Castro TG, Araújo TS, Nunes NB, Silva-Nunes M, Hoffmann EHE, Ferreira MU, Cardoso MA. Child health and nutrition in the Western Brazilian Amazon: population-based surveys in two counties in Acre State. Cad Saude Publica 2007; 23(6):1283-1293.,1414. United Nations Children’s Fund. The State of the World’s Children. Geneva: United Nations Children’s Fund; 1998. [cited 2013 Dec 1]. Available in: http://www.unicef.org/sowc98/sowc98.pdf
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. Poisson regression models with robust error were adjusted for individual, maternal and household variables by applying the stepwise forward method.

Chart 1
Conceptual model of factors associated with undernutritiona.

The quality of fit of the model was evaluated by the value of variance. No significant interactions, influential or extreme points were found. Variables open sewer, wealth index, receipt of financial aid and maternal height, age and education were maintained in the final model.

Since the maternal height of biological mothers is associated with undernutrition and can express both genetic effects and the results of socioeconomic conditions, we performed all the analysis in two separate models. The first model included all 428 children, and the second model included only 398 children who were cared for and lived with their biological mother. Among the 30 children excluded in the second model there were five children with stunting. The results were similar between the two models, except for the sewer variable, which showed p value of 0.052, and therefore only the results from the analysis on all the children are shown, regardless of type of caregiver. There were some missing values in some variables, and the final multivariate model contained 407 children.

Results

Socioeconomic and environmental characteristics of the study population

The sociodemographic and economic characteristics of the study population are shown in Table 1. Although 97.4% of children resided in households with electric power supply and 92.9% had garbage collection at their residences, the other socioeconomic conditions observed were very unfavorable, such as their house construction material, presence of open sewer, lack of shower with running water at the household, use of pit toilets or lack of latrines. About one third of the children interviewed (31.7%) received some type of individual or family governmental financial aid.

Table 1
Prevalence (%) and Prevalence Rate (PR) of stunted children under 5 years old according to socioeconomic and characteristics of caregiver. Assis Brasil, 2011.

Characteristics of caregiver and gestational conditions

The mean age of the caregivers (biological mothers and others) was 27.47 years (median = 26, range = 15 - 78 years). The average height of 407 biological mothers was 156.98 cm, and 50.7% of them were overweight. Only 9.1% of the caregivers were illiterate, while 45.3% had more than eight years of schooling. Only 15 mothers (3.71%) did not attend prenatal care (Table 2).

Table 2
Prevalence (%) and Prevalence Rate (PR) of stunted children under 5 years old according to individual child characteristics. Assis Brasil, 2011.

Children’s characteristics

Table 2 shows the distribution of the 428 children included in the study according to individual characteristics, birth and breastfeeding characteristics, and morbidity and access to health care. Of the children studied, 51.2% were males and 11.4% of all children were of indigenous ethnicity. Some children (6.3%) were born in the rural (or riparian) zones of Assis Brasil or other municipalities or lived outside the urban area sometime in their lives. The average age was 2.97 years (median = 3 years), and the average length of time residing in the urban area was 2.34 years (median = 2.19 years). About 94.7% were cared for by their own biological mother. The median birth weight of 366 children with known information was 3,350 g (mean 3,320 g, range = 1,000 g - 5,000 g). The majority of children (93.7%) had seen a physician at least once in their lives, but 36.4% had been hospitalized at least once. Only 29.3% had had a health care appointment in the Health Care Unit in the previous 12 months.

Prevalence of stunting and associated factors

The prevalence of stunting found in the urban area of the municipality of Assis Brasil among children under five years old was 14.4% in 2011.

In crude analysis (Table 2), children of indigenous origin were more likely to show stunting (PR = 2.89, CI = 1.80 to 4.65, p < 0.001), but this variable did not remain as a factor independently associated with undenutrition when adjusted for socioeconomic factors. Living in the countryside was also a associated factor for stunting (PR = 2.20, p = 0.015) in crude analysis, but after adjustment for socioeconomic factors, it failed to show an association with that outcome.

Some acute morbidities were also associated with chronic undernutrition in the unadjusted analysis (Table 2). Children with height-for-age deficit were more likely to have fever (PR = 1.75, p = 0.015), diarrhea (PR = 2.40, p < 0.001) and cough (PR = 2.50, p < 0.001) in the 30 days preceding the interview. None of these variables, however, remained significantly associated in the adjusted analysis. The other socioeconomic variables (characteristics of household and children - gender, access to daycare or school, pregnancy and breastfeeding conditions, access to health care services and previous hospitalization, Table 3) showed no statistically significant association in the adjusted analysis. The biological mothers’ body mass indexes were also not associated with stunting in children in adjusted analysis. Other socioeconomic and environmental variables did not show association in the adjusted analysis either.

Table 3
Factors associated with stunting in children under 5 years obtained by multivariate modeling. Assis Brasil, AC, 2011.

Adjusted models (Table 3) showed that, for the population studied, the family’s socioeconomic conditions, the caregiver’s age and education and the biological mother’s height were independently associated variables in relation to stunting.

The presence of open sewer in the household (aPR = 1.67, p = 0.045) and economically disadvantaged situation (aPR = 2.05, p = 0.015) significantly increased the probability of a child showing stunting (Table 3). Chronic undernutrition was also more common in children whose families received governmental financial aid (aPR = 1.88, p = 0.014). (Table 3).

Children whose biological mothers were taller were less likely to show stunting (aPR = 0.92, p 0.001). Children cared for by caregivers who did not attend school were more likely to show undernutrition (aPR = 2.11, p = 0.014). Children cared for by older caregivers were less likely to be stunted, a decrease of 7 % with each additional year of the caregiver’ age (p = 0.001) (Table 3).

Discussion

The prevalence of stunting found in this study is similar to the 14.8% prevalence rate found in the Northern Region, as identified by the 2006 National Demographic and Health Survey, and much higher than the national average of 7%88. Ministério da Saúde (MS). PNDS 2006: Pesquisa Nacional de Demografia e Saúde da Criança e da Mulher. Brasília: Ministério da Saúde, 2008. [cited 2013 Dec 1]. Available in: http://bvsms.saude.gov.br/bvs/pnds/img/relatorio_final_PNDS2006_04julho2008.pdf
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. Possible causes for this discrepancy in relation to the national average is that the Northern Region still faces many unfavorable socioeconomic conditions as compared to other Brazilian regions66. Monteiro CA, Benicio MHD, Conde WL, Konno S, Lovadino AL, Barros AJD, Victora CG. Narrowing socioeconomic inequality in child stunting: the Brazilian experience, 1974-2007. Bull World Health Organ 2010; 88:305-311.,88. Ministério da Saúde (MS). PNDS 2006: Pesquisa Nacional de Demografia e Saúde da Criança e da Mulher. Brasília: Ministério da Saúde, 2008. [cited 2013 Dec 1]. Available in: http://bvsms.saude.gov.br/bvs/pnds/img/relatorio_final_PNDS2006_04julho2008.pdf
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which have managed to reduce child undernutrition in recent years, such as the Northeastern and the Southeastern Regions in Brazil77. Victora CG, Aquino EML, Leal MC, Monteiro CA, Barros FC, Szwarcwald CL. Maternal and child health in Brazil: progress and challenges. Lancet 2011; 377(9780):1863-1876.,1515. Lima ALL, Silva ACF, Konno SC, Conde WL, Benicio MHD, Monteiro CA. Causas do declínio acelerado da desnutrição infantil no Nordeste do Brasil (1986-1996-2006). Rev Saude Publica 2010; 44(1):17-27..

In Assis Brasil, the factors associated with stunting are especially related to unfavorable socioeconomic conditions.

Close to 21.7% of the reduction in the prevalence of child undernutrion between 1996 and 2006-07 in Brazil can be attributed to the increased purchasing power of Brazilian families66. Monteiro CA, Benicio MHD, Conde WL, Konno S, Lovadino AL, Barros AJD, Victora CG. Narrowing socioeconomic inequality in child stunting: the Brazilian experience, 1974-2007. Bull World Health Organ 2010; 88:305-311., both in developed1616. Matijasevich A, Santos IS, Menezes AMB, Barros AJD, Gigante DP, Horta BL, Barros FC, Victora CG. Trends in socioeconomic inequalities in anthropometric status in a population undergoing the nutritional transition: data from 1982, 1993 and 2004 Pelotas birth cohort studies. BMD Public Health 2012; 12:511-520. regions and in those still under development1515. Lima ALL, Silva ACF, Konno SC, Conde WL, Benicio MHD, Monteiro CA. Causas do declínio acelerado da desnutrição infantil no Nordeste do Brasil (1986-1996-2006). Rev Saude Publica 2010; 44(1):17-27.. The Brazilian government is partly responsible for this increase by granting benefits to mothers or guardians in the poorest families in the last two decades, such as the Fome Zero and Bolsa Família programs, which have managed to have impact on linear growth in children and adolescents assisted by the programs1717. Piperata BA, Spence JE, DA-Gloria P, Hubbe M. The Nutrition transition in Amazonia: rapid economic change and its impact on growth and development in Ribeirinhos. Am J Phys Anthropol 2011; 146(1):1-13..

In this study, it was observed that many families do not have adequate sanitation facilities, which has been associated with stunting in other studies performed in Acre11. Souza OF, Benício MHD, Castro TG, Muniz PT, Cardoso MA. Desnutrição em crianças menores de 60 meses em dois municípios do Estado do Acre: prevalência e fatores associados. Rev Bras Epidemiol 2012; 15(1):211-221.. Exposure to an open sewer, besides indicating a poorer socioeconomic status, may lead to the acquisition of infectious diseases more frequently and result in stunting. In fact, cohort studies have shown that repeated episodes of diarrhea are associated with a small reduction in linear growth1818. Richard AS, Black RE, Gilman RH, Guerrant RL, Kang G, Lanata CF et al. Diarrhea in Early Childhood: short-term association with weight and long-term association with length. Am J Epidemiol 2013; 178(7):1129-1138.. In our analysis children with stunting were more likely to present a recent episode of diarrhea in the unadjusted analysis, as well as fever and cough. Although it was not possible to confirm this association because of the limited number of events, it is worth emphasizing the clinical importance of this finding. Care to a child with fever and especially non-epidemic diarrhea in socially disadvantaged areas, should raise clinical suspicion of some kind of undernutrition, which should be investigated by the health service.

Maternal education has been shown in some studies to be inversely associated with growth retardation in children under five years old1919. Silveira KBR, Alves JFR, Ferreira HS, Sawaya AL, Florêncio TMMT. Association between malnutrition in children living in favelas, maternal nutritional status, and environmental factors. J Pediatr 2010; 86(3):215-220.,2020. Florêncio TMMT, Ferreira HS, França APT, Cavalcante JC, Sawaya AL. Obesity and undernutrition in a very-low-income population in the city of Maceió, Northeastern Brazil. Br J Nutrition 2001; 86(2):277-283., probably due to lower access to information about the importance of household and personal hygiene habits and proper nutrition for children’s growth and development. Drachler et al.2121. Drachler ML, Macluf SPZ, Leite JCC, Aertz DRGC, Giugliani ERJ, Horta BL. Fatores de risco para sobrepeso em crianças no sul do Brasil. Cad Saude Publica 2003; 19(4):1073-1081., when studying non-indigenous children, claimed that the mother figure represents the bond between children and the environment, besides the fact that it is usually the mother who decides about the family’s eating habits as well as about hygiene care and immunization. In our study, even after adjustment for income and housing conditions, the effect of the lack of maternal education remained associated with undernutrition.

As occurred in Assis Brasil, other studies suggest an association between maternal age and children undernutrition, and the risk of stunting is higher in children of adolescent mothers2222. Olusanyaa BO, Wirzc SL, Rennerb JK. Prevalence, pattern and risk factors for undernutrition in early infancy using the WHO Multicentre Growth Reference: a community-based study. Paediatr Perinat Epidemiol 2010; 24(6):572-583.. The most likely explanation is that young women are generally not prepared to take care of such a dependent being2323. Carvalhaes MABL, Benício MHA. Capacidade materna de cuidar e desnutrição infantil. Rev Saude Publica 2002; 36(2):188-197., which can result in nutritional deficit.

Several studies found an association between the biological mother’s height and stunting in children2424. Ashworth A, Morris SS, Lira PIC. Postnatal growth patterns of full-term low birth weight infants in Northeast Brazil are related to socioeconomic status. J Nutr 1997; 127(10):1950-1956.,2525. Engstrom EM, Anjos LA. Desnutrição por déficit estatural nas crianças brasileiras: Relação com condições sócio-ambientais e estado nutricional materno. Cad Saude Publica 1999; 15(3):559-567.. Maternal height is also associated with weight at birth: children born to mothers with short stature are born with low weight2626. Barros FC, Victora CG, Matijasevich A, Santos IS, Horta BL, Silveira MF, Barros AJD. Preterm births, low birth weight, and intrauterine growth restriction in three birth cohorts in Southern Brazil: 1982, 1993 and 2004. Cad Saude Publica 2008; 24(Supl. 3):S390-S398.,2727. Victora CG, Adair L, Fall C, Hallal PC, Martorell R, Richter L, Sachdev HS; Maternal and Child Undernutrition Study Group. Maternal and child undernutrition: consequences for adult health and human capital. Lancet 2008; 371(9609):340-357.. Maternal height may be a marker of such woman’s nutritional history and previous socioeconomic conditions2626. Barros FC, Victora CG, Matijasevich A, Santos IS, Horta BL, Silveira MF, Barros AJD. Preterm births, low birth weight, and intrauterine growth restriction in three birth cohorts in Southern Brazil: 1982, 1993 and 2004. Cad Saude Publica 2008; 24(Supl. 3):S390-S398.,2727. Victora CG, Adair L, Fall C, Hallal PC, Martorell R, Richter L, Sachdev HS; Maternal and Child Undernutrition Study Group. Maternal and child undernutrition: consequences for adult health and human capital. Lancet 2008; 371(9609):340-357., or even suggest a genetic predisposition to short stature, which ends up being “inherited” by the child2828. Ramakrishnan U, Martorell R, Schroeder DG, Flores R. Role of intergenerational effects on linear growth. J Nutr 1999; 129(Supl. 2S):S544-S549., first reflected in low weight at birth and later in stunted growth. Separating such genetic effect of short maternal stature from families’ socioeconomic and environmental effects that are perpetuated through generations (both the mother’s and child’) and lead to stunting in children55. Black RE, Victora CG, Walker SP, Bhutta ZQA, Christian P, Onis M, Ezzati M, Grantham-McGregor S, Katz J, Martorell R, Uauy R; Maternal and Child Nutrition Study Group. Maternal and child undernutrition and overweight in low-income and middle-income countries. Lancet 2013; 382(9890):427-451. is not an easy task. To that end, a long-term specific epidemiological cohort design is necessary, since low maternal height is significantly associated with poverty and adverse conditions of the socioenvironmental milieu in several publications1919. Silveira KBR, Alves JFR, Ferreira HS, Sawaya AL, Florêncio TMMT. Association between malnutrition in children living in favelas, maternal nutritional status, and environmental factors. J Pediatr 2010; 86(3):215-220.,2424. Ashworth A, Morris SS, Lira PIC. Postnatal growth patterns of full-term low birth weight infants in Northeast Brazil are related to socioeconomic status. J Nutr 1997; 127(10):1950-1956.. As our study has a cross-sectional nature and it is not possible to establish a temporal relationship between the independent variables and the outcome, it is likely that not all the socioeconomic factors that influence maternal height were controlled in the analysis. Therefore, the association between maternal height and stunted children can be confounded by unadjusted socioeconomic factors, such as maternal socioeconomic status at the time of the biological mother’s growth.

This study has limitations. It is not possible to determine, for example, if the higher frequency of acute diarrhea in stunted children is a cause or a consequence of undernutrition, but only to emphasize that children with diarrhea should be investigated for the presence of undernutrition. Another limitation is a possible selection bias, since there was a selective loss of children who were not assessed anthropometrically and who were characterized by predominantly belonging to indigenous ethnic groups, to the lowest socioeconomic group, with uneducated mothers and a history of having resided in rural areas previously. Therefore, there may have been an underestimation of stunting prevalence and of the magnitude of the association of significant variables with the outcome, but which, however, does not invalidate the findings in the study regarding factors associated with chronic undernutrition.

Because of the age of the children analyzed and the cross-sectional nature of the study, some associations tested also have limitations and should be interpreted with caution. It was not possible to collect data on gestational age at birth and determine which children were born with low weight. Moreover, due to recalling bias, it was also not possible to collect data on the duration of breastfeeding and, therefore, the effect of pregnancy, childbirth and peripartum variables was not adequately tested. Since the majority of children were cared for by their biological mothers, the ability of this study to evaluate the effect of caregivers on undernutrition occurrence was also limited. Finally, the relationship between attending a daycare center or a school and stunting also introduced a selection bias, since children can only attend such services after they are two years old.

Finally, it is concluded that, although Brazil is going through a process of nutritional transition with consequent reduction in undernutrition, the prevalence of stunting in Assis Brasil can be regarded as an important public health problem. Socioeconomic conditions and maternal characteristics were shown to be closely related to the occurrence of stunting in this population, and some intervention is possible in the short term, while others depend on greater social and economic transformation in the Amazon region. A few interventions are already being executed by the Brazilian government, such as the inclusion of all children in school and kindergarten, where balanced food is offered everyday, and the social program of monthly wealth distribution for the poor, which is targeting those children at major risk for stunting, as seen in this study. Hopefully, these interventions will be able to eliminate stunting in the Amazon in near future.

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  • Ethical approval
    The study was approved by the Ethics Committee for Human Research of our Institution (Process n. 23107.09782/2009-04). We obtained informed consent from the parents or legal guardian of each participant after the nature and possible consequences of the studies had been fully explained.

History

  • Received
    25 Mar 2014
  • Reviewed
    24 Aug 2015
  • Accepted
    26 Aug 2015
  • Publication
    June 2016
ABRASCO - Associação Brasileira de Saúde Coletiva Rio de Janeiro - RJ - Brazil
E-mail: revscol@fiocruz.br