Abstracts

Introduction

Malnutrition, anemia, and soil-transmitted helminth (STH) infections are major health problems in early childhood. According to the World Health Organization (WHO), about 45% of deaths in children aged under five years relate to undernutrition in any of its forms: stunting, wasting, or underweight ¹1. Organización Mundial de la Salud. Malnutrición. https://www.who.int/es/news-room/fact-sheets/detail/malnutrition (accessed on 10/May/2020).
https://www.who.int/es/news-room/fact-sh... . Moreover, undernutrition predisposes children to infections, creating a vicious cycle which contributes to 35% of early childhood morbidity ²2. Black RE, Allen LH, Bhutta ZA, Caulfield LE, de Onis M, Ezzati M, et al. Maternal and child undernutrition: global and regional exposures and health consequences. Lancet 2008; 371:243-60.^,33. Comisio´n Econo´mica para Ame´rica Latina y el Caribe; Oficina Regional para Ame´rica Latina y el Caribe, Fondo de las Naciones Unidas para la Infancia. Desnutrición infantil en América Latina y el Caribe. Desafios 2006; (2):4-9.. These pathologies can have a lifelong impact on personal health and development ⁴4. Gödecke T, Stein AJ, Qaim M. The global burden of chronic and hidden hunger: trends and determinants. Glob Food Sec 2018; 17:21-9.. Stunting and anemia are particularly significant in early childhood (between six months and two years of age) since the lack of essential nutrients can impair growth and irreversibly deteriorate cognitive capacity ²2. Black RE, Allen LH, Bhutta ZA, Caulfield LE, de Onis M, Ezzati M, et al. Maternal and child undernutrition: global and regional exposures and health consequences. Lancet 2008; 371:243-60.^,33. Comisio´n Econo´mica para Ame´rica Latina y el Caribe; Oficina Regional para Ame´rica Latina y el Caribe, Fondo de las Naciones Unidas para la Infancia. Desnutrición infantil en América Latina y el Caribe. Desafios 2006; (2):4-9.^,55. Perkins JM, Kim R, Krishna A, McGovern M, Aguayo VM, Subramanian SV. Understanding the association between stunting and child development in low- and middle-income countries: next steps for research and intervention. Soc Sci Med 2017; 193:101-9.. STH infections constitute a neglected tropical disease with almost 2 billion people infected in the world ⁶6. Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors 2014; 7:37.. The literature has associated STH infections with cognitive and verbal impairment in early childhood ⁷7. Blouin B, Casapia M, Joseph L, Gyorkos TW. A longitudinal cohort study of soil-transmitted helminth infections during the second year of life and associations with reduced long-term cognitive and verbal abilities. PLoS Negl Trop Dis 2018; 12:e0006688.^,88. Joseph SA, Casapía M, Blouin B, Maheu-Giroux M, Rahme E, Gyorkos TW. Risk factors associated with malnutrition in one-year-old children living in the Peruvian Amazon. PLoS Negl Trop Dis 2014; 8:e3369.. These co-occurring diseases affect children living in poverty, especially in rural and peri-urban areas ⁹9. Chammartin F, Scholte RGC, Guimarães LH, Tanner M, Utzinger J, Vounatsou P. Soil-transmitted helminth infection in South America: a systematic review and geostatistical meta-analysis. Lancet Infect Dis 2013; 13:507-18.. Immediate causes include inadequate food intake and disease burden and underlying ones, household food insecurity, disadvantaged social position, poor access to health care, and unhealthy environments - manifested by social, economic, and political factors such as poverty, inequality or low educational attainment ¹⁰10. Wisbaum W. La desnutrición infantil. Causas, consecuencias y estrategias para su prevención y tratamiento. https://www.unicef.es/publicacion/la-desnutricion-infantil-causas-consecuencias-y-estrategias-para-su-prevencion-y (accessed on 02/Apr/2020).
https://www.unicef.es/publicacion/la-des... .

The other side of malnutrition is obesity. In 2019, an estimated 38.2 million children under five years of age were overweight or obese. Once considered a problem exclusive to high-income countries, overweight and obesity are increasingly prevalent in low- and middle-income nations, especially in urban settings. Childhood obesity is associated with breathing difficulties, hypertension, increased risk of fractures, insulin resistance, psychological effects, and adult premature death and disability ¹¹11. World Health Organization. Proyectos de recomendaciones para la prevención y el tratamiento de la obesidad a lo largo del curso de la vida, incluidas las posibles metas. Geneva: World Health Organization; 2021..

The Convention on the Rights of the Child ¹²12. United Nations General Assembly. Convention on the Rights of the Child. https://www.refworld.org/docid/3ae6b38f0.html (accessed on 21/Oct/2022).
https://www.refworld.org/docid/3ae6b38f0... recognizes the right of every child to a standard of living which would suit their physical, mental, spiritual, moral, and social development. According to the WHO, an adequate level of nutrition and health care results in similar growth patterns in children anywhere ¹³13. World Health Organization. WHO Child Growth Standards. Growth velocity based on weight, length and head circumference: methods and development. Geneva: World Health Organization; 2009.. However, 2018 WHO data classified 155 million children worldwide as stunted and 52 million as wasted ¹1. Organización Mundial de la Salud. Malnutrición. https://www.who.int/es/news-room/fact-sheets/detail/malnutrition (accessed on 10/May/2020).
https://www.who.int/es/news-room/fact-sh... . In 2015, following the Millennium Development Goals campaign, it globally endorsed new Sustainable Development Goals. This initiative aims to end poverty in all its forms worldwide, end hunger, achieve food security, and improve nutrition by 2030 ¹⁴14. Comisio´n Econo´mica para Ame´rica Latina y el Caribe. La Agenda 2030 y los Objetivos de Desarrollo Sostenible: una oportunidad para América Latina y el Caribe. Objetivos, metas e indicadores mundiales. Santiago: Comisio´n Econo´mica para Ame´rica Latina y el Caribe; 2019.. It is an eminently worthwhile (but long) journey. However, undernutrition remains a major threat to the survival, health, growth, and development of millions of children and the progress of countries.

Data published by the 2019 Peruvian Demographic and Family Health Survey (known by its Spanish acronym, ENDES) ¹⁵15. Instituto Nacional de Estadística e Informática. Indicadores de resultados de los programas presupuestales, 2015-2020. https://proyectos.inei.gob.pe/endes/2020/ppr/Indicadores_de_Resultados_de_los_Programas_Presupuestales_ENDES_2020.pdf (accessed on 15/Jun/2021).
https://proyectos.inei.gob.pe/endes/2020... ^,1616. Encuesta Demográfica y de Salud Familiar. Capítulo 10: lactancia, nutrición y desarrollo infantil temprano (DIT) de niñas y niños y nutrición de mujeres. https://www.inei.gob.pe/media/MenuRecursivo/publicaciones_digitales/Est/Endes2019/ (accessed on 02/Feb/2021).
https://www.inei.gob.pe/media/MenuRecurs... showed that stunting affected 12.2% of children under five years of age, with the highest rates in rural, dispersed, indigenous, and low-income populations ¹⁷17. Hernandez-Vasquez A, Tapia-López E. Chronic malnutrition among children under five in Peru: spatial analysis of nutritional data. Rev Esp Salud Pública 2017; 91:e201705035.. Loreto, the largest Peruvian department, has a 23.7% and 0.9% stunting and wasting prevalence, respectively. That of anemia reached 41.4% ¹⁶16. Encuesta Demográfica y de Salud Familiar. Capítulo 10: lactancia, nutrición y desarrollo infantil temprano (DIT) de niñas y niños y nutrición de mujeres. https://www.inei.gob.pe/media/MenuRecursivo/publicaciones_digitales/Est/Endes2019/ (accessed on 02/Feb/2021).
https://www.inei.gob.pe/media/MenuRecurs... , 11.9% above the national average. Loreto is highly endemic for STH infections ¹⁸18. Rodriguez Ferrucci H, Razuri H, Casapia M, Rahme E, Silva H, Ault S, et al. Governance, organization, accountability and sustainability of a region-wide school-based deworming program in Loreto, Peru. Acta Trop 2016; 159:219-26. but the literature has few publications on STH infections in preschool-age children. A study conducted in 2007 found a 32.1% Ascaris lumbricoides, 38.9% Trichuris trichiura, and 3.2% hookworm infection prevalence, respectively ¹⁹19. Casapía M, Joseph SA, Núñez C, Elham R, Gyorkos TW. Parasite and maternal risk factors for malnutrition in preschool-age children in Belen, Peru using the new WHO child growth standards. Br J Nutr 2007; 98:1259-66..

Santo Tomás is a peripheral region in Iquitos, the capital of Loreto. It exemplifies spontaneous urban growth lacking any municipal planning for populations arriving from rural areas, as with many Peruvian cities. In the last eight years, the population of Santo Tomás has multiplied by 10 due to the many low-income families who have settled in the area, having migrated from communities situated along the Amazon River and its tributaries and from previously dismantled settlements in and around Iquitos. These peri-urban settlements lack basic services such as electricity, clean water, and sanitation and, to date, no studies have assessed their health needs.

This study aimed to determine the prevalence of malnutrition (i.e., stunting), anemia, and STH infections in preschool-age children (i.e., aged 6 to 59 months) in Santo Tomás, Loreto, Peru, to (i) evaluate the local magnitude of these conditions and (2) inform health policies and services to adapt national and regional protocols aligned with the Integrated Management of Childhood Illness (IMCI) approach.

Materials and methods

Study population

Our study population was composed of children aged from 6 to 59 months living in Santo Tomás and the surrounding settlements under its jurisdiction in the district of San Juan Bautista, Maynas province, located approximately 15km from the municipality of Iquitos. As of March 2019, the studied area consisted of Santo Tomás and 23 settlements with an approximate combined population of 12,808 people (data from the Santo Tomás health post; Evelyn Maritza Orbe Villasis, personal communication, July 9, 2018).

Sample size

A sample size of 572 children was required by a 23.8% estimated stunting prevalence ²⁰20. Instituto Nacional de Estadística e Informática. Indicadores de resultados de los programas presupuestales: primer semestre 2017. https://proyectos.inei.gob.pe/endes/images/Peru_Indicadores_de_PPR_2011_2016.pdf (accessed on 15/Jun/2021).
https://proyectos.inei.gob.pe/endes/imag... , an estimated population of 2,321 individuals under five years of age, a ±4% precision, and a 1.5 design effect (i.e., the possible recruitment of two children per household).

Recruitment

This study was conducted in March 2019. Households with children in the targeted age group were randomly selected in each settlement to achieve a sample size proportional to its total population. Inclusion criteria for children to participate in this study involved age between 6 and 59 months, habitation in any of the 24 recruitment areas (Santo Tomás and settlements), and parents or legal guardians’ consent. Our only exclusion criterion were serious congenital or chronic medical conditions (e.g., preterm birth - i.e., < 28 weeks gestation -, cerebral palsy, neural tube defects, etc.).

A questionnaire, adapted from previous studies ¹⁹19. Casapía M, Joseph SA, Núñez C, Elham R, Gyorkos TW. Parasite and maternal risk factors for malnutrition in preschool-age children in Belen, Peru using the new WHO child growth standards. Br J Nutr 2007; 98:1259-66.^,2121. Gyorkos TW, Maheu-Giroux M, Casapía M, Joseph SA, Creed-Kanashiro H. Stunting and helminth infection in early preschool-age children in a resource-poor community in the Amazon lowlands of Peru. Trans R Soc Trop Med Hyg 2011; 105:204-8., was administered to the primary caregiver in the household. This survey aimed to determine the child and family’s sociodemographic characteristics and health information. Children’s weight was measured while they were unclothed via a portable digital baby scale (Beurer BY-80, accuracy 5g; https://www.beurer.com) if they weighed less than 20kg or via an electronic standing scale if they exceeded 20kg (only if the child could stand without moving). Participants’ length was measured by their recumbent crown-heel length on a flat surface via an infantometer (ADE BYT-MZ10040, 1mm gradation; https://ade-germany.de) if younger than two years of age or, if older, standing by a wall-mounted roll-up tape measure (ADE BYT-MZ10017; 1mm gradation). Both weight and length were measured twice and their mean, registered. Hemoglobin concentration was determined by finger-prick blood via a HemoCue analyzer (HemoCue Hb 301; https://www.hemocue.com). Stool specimens were analyzed daily by experienced laboratory technologists from the Selva Amazónica Civil Association by the Kato-Katz technique within 24 hours of initial collection, according to WHO recommendations ²²22. World Health Organization. Helminth control in school-age children: a guide for managers of control programmes. https://apps.who.int/iris/handle/10665/44671 (accessed on 23/Oct/2022).
https://apps.who.int/iris/handle/10665/4... , to assess both the prevalence and intensity of STH infection. A single stool specimen was collected from each child. Families of children showing malnutrition, anemia or STH infections received detailed explanations on these conditions and were referred to the local public health system for treatment and follow-up.

Statistical analyses

To classify children’s anthropometric measurements into stunting, underweight, and wasting, the WHO Anthro software, version 3.2.2 (http://www.who.int/childgrowth/software/en/), was used to calculate age- and sex-specific length-for-age, weight-for-age, and weight-for-length z-scores. Our moderate stunting, underweight, and wasting categories were based on < -2 SD (standard deviation) and ≥ -3 SD z-scores, whereas severe ones, as < -3 SD z-scores. Overweight and obesity were defined as a weight-for-height z-score between > 2 SD and ≤ 3 SD and > 3 SD, respectively.

Anemia was defined as a hemoglobin value below 11g/dL and classified as mild, moderate or severe if 10.9-10.0g/dL, 9.9-7.0g/dL or < 7.0g/dL, respectively, as per WHO recommendations ²³23. World Health Organization. Nutritional anaemias: tools for effective prevention. https://www.who.int/nutrition/publications/micronutrients/anaemias-tools-prevention-control/en/ (accessed on 15/Jun/2021).
https://www.who.int/nutrition/publicatio... . STH infection intensity was categorized as light, moderate or heavy based on A. lumbricoides, T. trichiura, and hookworm egg counts per gram of feces. Data were entered into an SPSS, version 25 (https://www.ibm.com/).

Child, maternal, and household characteristics were summarized by frequencies for categorical variables and means with SD for continuous ones. Our baseline population for analyses of the prevalence of STH infection consisted of a subset which provided stool specimens.

Logistic regression analyses were performed to identify the risk factors for our three outcomes (i.e., stunting, anemia, and STH infection). Models were run by a generalized estimating equation to account for the clustering effect at households. All variables were examined for collinearity prior to inclusion in regression models. Marital status and maternal education were collapsed to create dichotomous variables. Multiple component analysis was used to create an asset-based index for household socioeconomic status by construction material, flooring material, cooking fuel, television ownership, radio ownership, electrification, running water, and source of drinking water. Socioeconomic status variables were subsequently divided into quartiles based on index-derived cut-points for inclusion in our regression models.

Univariate analyses were used to assess unadjusted associations between potential risk factors and each outcome of interest. Variables which obtained a p < 0.20 in our univariate analyses, as well as those we considered clinically and epidemiologically relevant, were included in our multivariate analyses. Sparse or collinear variables were removed from the model. Odds ratios (OR) and 95% confidence intervals (95%CI) for the association between independent risk factors and each binary dependent variables were computed for both univariate and multivariate analyses. Variables with a significance level of p < 0.05 in our multivariate models were considered important risk factors. All statistical analyses were performed in R, version 4.0.5 (http://www.r-project.org).

Ethics considerations

This study was approved by the Institutional Ethics Committee for Clinical Research at the Felipe S. Arriola Iglesias Regional Hospital and the local office of the Peruvian Ministry of Health (Regional Health Directorate in Loreto) in Iquitos (protocol ID-011-CIEI-19). Participants’ parents or legal guardians signed written informed consent forms.

Results

Baseline characteristics of the studied population

We recruited 572 children. Table 1 lists their baseline characteristics. They showed a mean age of 32.1 months (SD: 15.8) and 51.7% of them were boys. Only 60.2% had all vaccinations according to the guidelines of the Peruvian Ministry of Health. We found that mothers’ mean age was 29.0 years (SD: 7.1), 2.8% (16) of them became one under 18 years of age, only 32.9% had completed secondary education, and 18.9% worked outside their homes. The mean number of children per mother was 3.1 (SD: 1.8). 17.4% of children had four or more siblings. The average number of persons living in the household was 6.3 (SD: 2.5).

Studied population’s profile of malnutrition, anemia, and STH infection

In total, 33.9% of the studied population (194 children) had one or more forms of malnutrition (i.e., stunting, wasting or underweight). We found a 31.3% prevalence of stunting; severe in 5.2% of the children (Table 2), a 3.2% prevalence of wasting; severe in 1.1%, comorbidities with two or three concurrent forms of malnutrition in 8.2% (n = 47) of participants, and a 1.6% and 0.7% prevalence of overweight and obesity, respectively.

We observed a 47.2% overall prevalence of anemia, moderate in 18.9% of our sample (Table 3). We found no cases of severe anemia for any age.

Of the 572 children, 481 (84.1%) provided a stool specimen which we Kato-Katz examined. We found a 34.1% overall prevalence of STH infections (Table 4), 25.2% of A. lumbricoides, 18.5% of T. trichiura, and 2.3% of hookworm ones (presumably Necator americanus). We observed that 48 children (10%) had A. lumbricoides and T. trichiura coinfection and four (0.8%) suffered with all three infections. Of children older than two years (n = 375) - the starting age of the national deworming program -, 62.7% (n = 235) were dewormed in the previous six months, of which 30.6% (n = 72) had an STH infection despite previous treatment.

Risk factors for stunting, anemia, and STH infections

In identifying risk factors, our adjusted models showed that stunting was significantly statistically associated with a higher number of children per mother and single mothers. Mothers’ educational attainment was disassociated with stunting in either unadjusted or adjusted analyses (Table 5).

Statistically significant risk factors for anemia consisted of younger age and the male sex (Table 5). We found no statistically significant association between anemia and stunting or STH infections in either our unadjusted or adjusted analyses.

Statistically significant risk factors for STH infections included older age and incomplete vaccinations (Table 5). Maternal employment outside the home was associated with a lower risk of infections. We found a statistically significant association between STH infections and lower socioeconomic status when we compared the third highest quartile with the lowest quartile. Our multivariable analyses found a statistically significant association (adjusted OR = 0.57; 95%CI: 0.34; 0.98; p = 0.044) by combining the third and fourth quartiles and comparing them with our reference. We found no statistically significant association between STH infections and stunting or anemia in either our unadjusted or adjusted analyses.

Discussion

We found a high prevalence of different forms of malnutrition in preschoolers from Santo Tomás and its surrounding settlements. We observed a stunting prevalence (31.3%) 18.6% higher than the South American average (12.7%) ²⁴24. Organization for Economic Co-operation and Development; World Bank. Health at a glance: Latin America and the Caribbean 2020. Paris: OECD Publishing; 2020., 19.1% above the national one (12.2%), and 7.6% greater than the 2019 official figures for the Loreto department (23.7%) ¹⁵15. Instituto Nacional de Estadística e Informática. Indicadores de resultados de los programas presupuestales, 2015-2020. https://proyectos.inei.gob.pe/endes/2020/ppr/Indicadores_de_Resultados_de_los_Programas_Presupuestales_ENDES_2020.pdf (accessed on 15/Jun/2021).
https://proyectos.inei.gob.pe/endes/2020... . Although this study focused on stunting as an indicator of malnutrition, it observed a high wasting prevalence, 3.5 times above the official average for Loreto and 7.9 times above the national average in 2019 ¹⁶16. Encuesta Demográfica y de Salud Familiar. Capítulo 10: lactancia, nutrición y desarrollo infantil temprano (DIT) de niñas y niños y nutrición de mujeres. https://www.inei.gob.pe/media/MenuRecursivo/publicaciones_digitales/Est/Endes2019/ (accessed on 02/Feb/2021).
https://www.inei.gob.pe/media/MenuRecurs... . Severe wasting was 10.5 times above the national and Loreto department averages. We found few cases of overweight and obesity, far below national statistics (6.4% for overweight and 1.6% for obesity) and closer to those of Loreto (3.6% for overweight and 0.9% for obesity) in 2019 ²⁵25. Vilchez Dávila W, Valenzuela Vargas RS. 2019: informe gerencial. Estado nutricional de niños y gestantes que acceden a establecimientos de salud. http://www.ins.gob.pe (accessed on 18/Sep/2022).
http://www.ins.gob.pe... .

Note the association between a higher number of children per household and stunting. Loreto is the Peruvian department with the most precarious access to family planning services, the highest rate of adolescent pregnancy, and with significant gaps in women’s access to identity documents and secondary and higher education ²⁶26. Comisio´n de Mujer y Familia del Congreso de la Repu´blica. Diagno´stico de ge´nero en la Amazoni´a al 2017. https://pdf.usaid.gov/pdf_docs/pnaec707.pdf (accessed on 07/Apr/2020).
https://pdf.usaid.gov/pdf_docs/pnaec707.... . Peru has implemented several public health ²⁷27. Ministerio de Salud. Plan nacional para la reducción y control de la anemia materna infantil y la desnutrición crónica infantil en el Perú: 2017-2021. https://www.gob.pe/institucion/minsa/informes-publicaciones/280855-plan-nacional-para-la-reduccion-y-control-de-la-anemia-materno-infantil-y-la-desnutricion-cronica-infantil-en-el-peru-2017-2021-documento-tecnico (accessed on 15/May/2020).
https://www.gob.pe/institucion/minsa/inf... and family support policies ²⁸28. Ministerio de la Mujer y de Poblaciones Vulnerables. Plan nacional de fortalecimiento a las familias 2016-2021. https://www.mimp.gob.pe/files/planes/PLANFAM-2016-2021.pdf (accessed on 18/Sep/2022).
https://www.mimp.gob.pe/files/planes/PLA... but their translation into effective interventions shows gaps which important inequalities in health coverage, infrastructure, and staff and access to support according to geographical area exacerbate. The public budget of healthcare is lower than the Latin American average and inefficiencies in the management of resources are common ²⁹29. Instituto Peruano de Economía. Propuestas de política 2021-2026. https://www.ipe.org.pe/portal/propuestas-de-politica-eje-de-salud/ (accessed on 18/Sep/2022).
https://www.ipe.org.pe/portal/propuestas... .

We found a concerning association between mothers caring for their children by themselves and stunting. Some mothers can often avoid face-to-face or financial support from fathers in raising their children. Moreover, single mothers have fewer job opportunities than nulliparous individuals, preventing them from acquiring their own income ³⁰30. Barrantes-Cáceres R, Matos-Trifu P. "En capilla": desigualdades en la inserción laboral de mujeres jóvenes. Lima: Instituto de Estudio Peruano; 2019., which can cause nutritional problems in their children ³¹31. Pridmore P. Identifying and tackling the social determinants of child malnutrition in urban informal settlements and slums: a cross national review of the evidence for action. https://assets.publishing.service.gov.uk/media/57a08ad940f0b652dd000932/60717_Child_Malnutrition_Pridmore.pdf (accessed on 08/May/2020).
https://assets.publishing.service.gov.uk... ^,3232. Nunes MA, Ferri CP, Manzolli P, Soares RM, Drehmer M, Buss C, et al. Nutrition, mental health and violence: from pregnancy to postpartum cohort of women attending primary care units in Southern Brazil - ECCAGE study. BMC Psychiatry 2010; 10:66.. This situation affects many families in Loreto, can go unnoticed, and is difficult to identify and redress ²⁶26. Comisio´n de Mujer y Familia del Congreso de la Repu´blica. Diagno´stico de ge´nero en la Amazoni´a al 2017. https://pdf.usaid.gov/pdf_docs/pnaec707.pdf (accessed on 07/Apr/2020).
https://pdf.usaid.gov/pdf_docs/pnaec707.... ^,3333. Arbildo Ruiz S. Articulando esfuerzos para combatir la trata de personas y la explotación sexual de niños, niñas y adolescentes en la región Loreto. http://www2.congreso.gob.pe/sicr/cendocbib/con4_uibd.nsf/B8D58E82BE4FD96305257F8800538E74/$FILE/025-silvia_arbildo.pdf (accessed on 15/May/2020).
http://www2.congreso.gob.pe/sicr/cendocb... .

Another cause which might explain the high prevalence of malnutrition in this study include the rapid increase in urban and peri-urban populations over a relatively short period of time. In 2019, the World Bank reported that more than 50% of the world population lives in cities (one third in the 1960s). In total, 90% of urban expansion is taking place in low-income countries and much of it (about 1 billion people) occurs via informal settlements and slums ³⁴34. World Bank Group. The World Bank urban and local government strategy: concept and issues note. http://documents.worldbank.org/curated/en/418241468331187263/The-World-Bank-urban-and-local-government-strategy-concept-and-issues-note (accessed on 15/May/2020).
http://documents.worldbank.org/curated/e... . Cities have failed to address this rapid and unplanned urban growth, resulting in inequalities, widespread social stratification, and the breakdown of social support systems and networks ³⁵35. Martin-Prével Y, Maire B, Delpeuch F. Nutrition, urbanisation et pauvrete en Afrique Subsaharienne. Med Trop 2000; 60:179-91.. Moreover, basic sanitation services, health services, social services, etc. have failed to accompany these settlements and, together with the population’s economic difficulties to access basic foodstuffs, cause serious health problems, such as malnutrition. Such is the case for the peri-urban population in Santo Tomás.

Breastfeeding is of critical importance to early childhood anemia. It occurs during the rapid growth of children, which increase their iron demands. Although we found that a high proportion of infants had been breastfed (over 95%), cultural practices include supplementing breastmilk with other foods within weeks of birth. Anemia in infants and young children may stem from an inadequate amount of iron in breastmilk, deficient intake, and low bioavailability of iron-rich foods ³⁶36. Magalhães RJS, Clements ACA. Mapping the risk of anaemia in preschool-age children: the contribution of malnutrition, malaria, and helminth infections in West Africa. PLoS Med 2011; 8:e1000438.^,3737. Mahmud MA, Spigt M, Mulugeta Bezabih A, López Pavon I, Dinant GJ, Blanco Velasco R. Risk factors for intestinal parasitosis, anaemia, and malnutrition among school children in Ethiopia. Pathog Glob Health 2013; 107:58-65.. Although we found a statistically significant association between anemia and boys, we are unable to offer any explanation regarding their culture, religion or diet. According to Domellöf et al. ³⁸38. Domellöf M, Lönnerdal B, Dewey KG, Cohen RJ, Landa Rivera L, Hernell O. Sex differences in iron status during infancy. Pediatrics 2002; 110:545-52., people may show hormone-mediated differences in their iron metabolism, related to the synthesis of lean versus fat body mass. We found no association between stunting and anemia, a finding previously observed and thought to be the result of similar causal factors ³⁶36. Magalhães RJS, Clements ACA. Mapping the risk of anaemia in preschool-age children: the contribution of malnutrition, malaria, and helminth infections in West Africa. PLoS Med 2011; 8:e1000438..

Few studies have reported the prevalence of STH infections in preschoolers from Loreto. Casapía et al. ¹⁹19. Casapía M, Joseph SA, Núñez C, Elham R, Gyorkos TW. Parasite and maternal risk factors for malnutrition in preschool-age children in Belen, Peru using the new WHO child growth standards. Br J Nutr 2007; 98:1259-66., found a 48% prevalence of STH infections in this age group in the survey they conducted in 2005-2006. Although the government launched two major deworming initiatives since that time (i.e., seven cycles of school-based deworming between 2012 and 2014 in Loreto and an annual national deworming program beginning in 2017) ²⁷27. Ministerio de Salud. Plan nacional para la reducción y control de la anemia materna infantil y la desnutrición crónica infantil en el Perú: 2017-2021. https://www.gob.pe/institucion/minsa/informes-publicaciones/280855-plan-nacional-para-la-reduccion-y-control-de-la-anemia-materno-infantil-y-la-desnutricion-cronica-infantil-en-el-peru-2017-2021-documento-tecnico (accessed on 15/May/2020).
https://www.gob.pe/institucion/minsa/inf... , the 34.1% prevalence we found and its higher incidence among older children indicate that the area still suffers with active transmission. Further assessments of deworming program coverage would help inform public health services. Its association with incomplete vaccination could reflect caregivers’ poor knowledge of basic health issues, economic difficulties in accessing health centers or high population mobility, which would hinder access to both vaccination and deworming programs but the literature needs more studies to assess this association ³⁹39. Isidro Ríos TL, Gutiérrez Aguado A. Prenatal factors associated with breach of the basic vaccination scheme in under 5 years of age. Rev Fac Med Hum 2021; 21:354-63.^,4040. Escobar-Díaz F, Osorio-Merchán MB, de la Hoz-Restrepo F. Reasons some children under 5 do not get vaccinated in four Colombian cities. Rev Panam Salud Pública 2017; 41: e123.. The lower risk among children whose mothers worked outside the home and those with higher socioeconomic status suggests that improved socioeconomic capacity may reduce opportunities for contracting infections. We found no association between STH infections and malnutrition or anemia, despite a combined 20% T. trichiura and hookworm prevalence, known causes of anemia ⁴¹41. Stephenson LS, Latham MC, Ottesen EA. Malnutrition and parasitic helminth infections. Parasitology 2000; 121 Suppl:S23-38.^,4242. Gutiérrez-Rodríguez C, Trujillo-Hernández B, Martínez-Contreras A, Pineda-Lucatero A, Millán-Guerrero RO. Frecuencia de helmintiasis intestinal y su asociación con deficiencia de hierro y desnutrición en niños de la región occidente de México. Gac Méd Méx 2007; 143:297-300.. This may in part be due to the low predictive values associated with the Kato-Katz technique ⁴³43. Tarafder MR, Carabin H, Joseph L, Balolong E, Olveda R, McGarvey ST. Estimating the sensitivity and specificity of Kato-Katz stool examination technique for detection of hookworms, Ascaris lumbricoides and Trichuris trichiura infections in humans in the absence of a "gold standard". Int J Parasitol 2010; 40:399-404., the extremely low prevalence of hookworms, and the light intensity of these infections, which are thus less likely to result in overt morbidity or pathology ⁴⁴44. Chhabra P, Bhasin DK. Hookworm-induced obscure overt gastrointestinal bleeding. Clin Gastroenterol Hepatol 2017; 15:e161-2..

Among the strengths of our study is its household-based recruitment strategy. This enabled us to include all children in the targeted age group, rather than only those who attended school (as with most other studies). Moreover, experienced technical personnel based at an organization which has participated in several seminal research studies on STH in the area performed our laboratory analyses.

This study include limitations, such as the absence of data on iron dietary intake and variability. Some measurement error is attributable to the Kato-Katz estimates of STH infections, which the technical personnel’s substantial expertise mitigated to some extent. Some recall and report biases may be present but well-trained interviewers and objective measurements and outcomes rather attenuated them.

According to 2020 United Nations Development Program (UNDP) data ⁴⁵45. Programa de las Naciones Unidas para el Desarrollo. La próxima frontera: desarrollo humano y el Antropoceno. https://hdr.undp.org/system/files/documents/hdr2020overviewspanishpdf_1.pdf (accessed on 15/Nov/2020).
https://hdr.undp.org/system/files/docume... , Peru has the 79th highest Human Development Index (HDI: 0.777) - a positive condition. HDI measures factors such as life expectancy, education, and per capita income. It is paradoxical that a country with these characteristics (fairly high HDI ranking, classified as a middle-income country in 2008 and no longer as a developing one) should have such large health inequalities among its population. Our study highlights the serious problems malnutrition, anemia, and STH infections still comprise today in extremely poor populations such as ours ³3. Comisio´n Econo´mica para Ame´rica Latina y el Caribe; Oficina Regional para Ame´rica Latina y el Caribe, Fondo de las Naciones Unidas para la Infancia. Desnutrición infantil en América Latina y el Caribe. Desafios 2006; (2):4-9.^,55. Perkins JM, Kim R, Krishna A, McGovern M, Aguayo VM, Subramanian SV. Understanding the association between stunting and child development in low- and middle-income countries: next steps for research and intervention. Soc Sci Med 2017; 193:101-9.^,88. Joseph SA, Casapía M, Blouin B, Maheu-Giroux M, Rahme E, Gyorkos TW. Risk factors associated with malnutrition in one-year-old children living in the Peruvian Amazon. PLoS Negl Trop Dis 2014; 8:e3369.. The lack of public policies which promote adequate living conditions for rural populations in their places of origin is leaving many rural communities without feasible options for survival, generating a growing exodus of riverine families to cities, and aggravating public health problems such as malnutrition, in stark contrast to the national prevalence, which has decreased year after year.

Our study population is highly vulnerable and needs strong health and public policies. Over the last few years, Peru has significantly progressed toward improving access to health care and taken numerous actions to reduce stunting. Its 2017-2021 National Plan to reduce and control maternal and child anemia and chronic child malnutrition outlines specific strategies such as iron and micronutrient supplementation for children under 36 months, iron and folic acid supplementation, and prenatal care for pregnant adolescents, child growth and development control, vitamin A supplementation for children under five years of age, deworming for schoolchildren and families, practices to improve infant and pregnant women’s nutrition, salt iodization, promotion of safe water consumption and hand washing, and capacity-building programs in educational communities, neighborhoods, and municipalities ²⁷27. Ministerio de Salud. Plan nacional para la reducción y control de la anemia materna infantil y la desnutrición crónica infantil en el Perú: 2017-2021. https://www.gob.pe/institucion/minsa/informes-publicaciones/280855-plan-nacional-para-la-reduccion-y-control-de-la-anemia-materno-infantil-y-la-desnutricion-cronica-infantil-en-el-peru-2017-2021-documento-tecnico (accessed on 15/May/2020).
https://www.gob.pe/institucion/minsa/inf... . Most of these actions have been in effect since 2014 but our study highlights the persisting inequality. Urgent interventions by relevant institutions are needed to correct these inequalities and monitor their impact.

Overall, our study found a high prevalence of malnutrition, anemia, and intestinal parasite infections in young children in small rural settlements in the Loreto department of the Peruvian Amazon. With the additional disease burden and emergency demands of the ongoing coronavirus pandemic, we expect a further economic crisis, which may worsen the already local precarious health and food security situation. We attest the urgent need to reprioritize children’s health and development within all relevant government sectors and their partners so appropriate policies and services can ensure a healthy and productive future for children.

Acknowledgments

We are grateful for the support and collaboration of the staff at Selva Amazónica Civil Association. We would like to thank the Suyay Latin America Association and Zerca y Lejos ONGD volunteers who participated in field data collection. We also express our gratitude to all mothers, fathers, and children for their willingness to participate in this study.

References

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