Indicators of anemia and physical growth in schoolchildren from the Ouest and Sud-Est Departments of Haiti: a cross-sectional study
© The Author(s). 2016
Received: 22 May 2016
Accepted: 6 November 2016
Published: 18 November 2016
The identification and correction of malnutrition in children remains a critical public health issue in many developing countries. In this study, the rate of anemia and standardized indicators of physical growth were investigated in schoolchildren from Haiti.
Hemoglobin concentrations, height, and weight were collected from schoolchildren (n = 615) and evaluated by World Health Organization (WHO) standardized classifications for anemia and child growth. Data on glucose-6-dehydrogenase (G6PD) deficiency and current or previous malaria infection available for all students; a subset of anemia and non-anemic males (n = 43) were tested for serum ferritin. School A (n = 504) had a school-based supplemental nutrition program, while School B (n = 111) did not.
Anemia was identified in 48.3% of students (95% CI: 44.3, 52.3), and not associated with BMI Z scores (P = 0.28) or serum ferritin concentrations (P = 0.17). The average Z scores for body mass index (BMI) of students at School A was within the normal range, while Z scores for BMI at School B were below average. Compared to school A, students at School B had significantly higher (P <0.001) rates of anemia (44.4% vs 65.8%) and were significantly (P <0.001) more likely to be underweight (16.5% vs 43.2%).
The high prevalence of anemia in children with and without normal BMIs represents a major public health concern that warrants further investigation with more comprehensive methods. This study may also highlight some potential benefits of in-school nutritional supplementation programs in achieving lower rates of anemia and reaching WHO standards for child growth.
KeywordsAnemia Child growth Haiti School-aged children
In developing countries, malnutrition remains among the most important underlying factors for the global burden of disease, directly attributed to over 300,000 deaths per year and indirectly responsible for more than half of all deaths in children . Poor cognitive development, delays in physical growth, decreased organ and immune system function, and increased morbidity and mortality, have all been associated with malnutrition [2, 3]. Anemia is often linked with malnutrition in these settings, reflecting a series of complex interactions between inadequate dietary intake of key nutrients, exposure to infectious diseases, and underlying genetic factors . Considering that as of 2014, Haiti was ranked 101 out of 107 countries around the world and last in Latin America and the Caribbean in food security, malnutrition in Haitian children represents a major public health concern .
Currently, sparse information is available about the nutritional status of school-aged children in Haiti, who are often at risk of being overlooked when prioritizing national nutrition interventions . In the 2012 National Haitian Health Survey, anemia was identified as a major health concern, where 65% of children under five had some form of anemia . A recent review of anemia in Latin America and the Caribbean reported that Haiti had the highest prevalence of anemia at 45.5%; however anthropomorphic measurements of child development or underlying pathophysiological mechanisms were not investigated . Moreover, Haiti is the only remaining country in the Caribbean with endemic malaria transmission . Since malaria infections or treatment with antimalarial drugs can induce anemia , especially in individuals with glucose-6-phosphate dehydrogenase (G6PD) deficiency , investigation of the relationships between malaria, G6PD deficiency, and anemia in this population could provide useful information for future malaria elimination efforts in Haiti . For these reasons, a cross-sectional study was conducted to evaluate these relationships among schoolchildren in Haiti.
Sample collection and enrollment were approved by the University of Florida based Institutional Review Board, the Haitian-based Institutional Review Committee, and the Office of Research Protections, United States Army Medical Research and Materials Command. Participants and their parents/guardian were given opportunities to ask our enrolling physicians and health professionals questions during informational sessions prior to informed consent. As the study population was mostly children, consent was provided by a parent or legal guardian prior to their participation.
Schoolchildren (n = 615) were enrolled from two schools located in the Ouest and Sud-Est departments of Haiti between February 2013 and May 2013. In the Ouest department, participants (n = 504) were recruited from the Christianville Foundation school (School A) in Gressier. In the Sud-Est department, participants (n = 111) were recruited from the Hossana Baptist School (School B) located in Jacmel. Though a convenience sample was used to investigate indicators of child growth and the prevalence of anemia, certain selection criteria were used to control for potential confounding and gain adequate power for hypothesis testing. In an attempt to include children of similar socioeconomic status, both schools selected were private, operated by non-governmental organizations (NGOs), and charged a similar tuition for attendance. To examine the potential effects of diet on anemia and malnutrition, one school with a supplementary nutrition program and one without such a program were selected. Children attending School A were given one meal every day at school in the form of farmed tilapia, chicken eggs, pasta, green leafy vegetables, or beans, while School B had no organized in-school nutrition program.
Sample collection and laboratory analysis
After informed consent and enrollment, participant age (months), gender, height (cm), weight (kg), and hemoglobin concentration (g/dl) were collected using a tape-measure, portable scale and a digital hemoglobin meter (HemoCue® Hb 201 plus, Hemocue Incorporated, Cypress, Ca, USA), following standard methods . Blood samples were collected by venipuncture and screened for G6PD deficiency (G6PD kit #345B, Trinity Biotech, St. Louis, MO, USA), current malaria infection using a rapid diagnostic test (First Response Malaria Combo, Premier Medical Corporation Ltd., Kachigam, India), and previous malaria infection (presence of antibodies toward Plasmodium falciparum MSP-1 or AMA-1 antigens using indirect ELISA) as previously described [14, 15]. A subset of 43 male students from the 90th and 10th percentiles of hemoglobin concentrations were selected at random and screened for serum ferritin concentrations using an IMMULITE 2000 Immunoassay System (Siemans Healthcare GmbH, Erlangen, Germany). Only male students were selected to examine the association between serum ferritin and anemia to remove the possibility of iron deficiency anemia caused by menstruation in females.
Classification of anemia and child development
The WHO classifications for mild, moderate, and severe anemia determined by measurement of hemoglobin concentration at sea level (g/L) were used. Thresholds for mild, moderate, and severe anemia are defined for population members stratified into four groups: children aged five to eleven years, children aged twelve to fourteen years, males above the age of fifteen, and females above the age of fifteen . Child growth indicators were used as a proxy for malnutrition by comparison to the World Health Organization (WHO) international reference population, which contains anthropometric measurements from children and adolescents from around the world . Measurements of height and weight were used to calculate a body mass index (BMI) that was normalized by gender and age to generate Z scores to determine whether the participant’s physical development was different from the mean growth indicators for a child of the same age and gender . Deficiencies in child growth were defined by Z scores two standard deviations below mean height-for-age (stunting), weight-for-age (wasting), and weight-for-height (underweight); with the additional inclusion of thinness (thin) defined by a Z score one standard deviation below the mean BMI.
Simple logistic regression models were used to determine if gender, age, enrollment location, presence of G6PD deficiency, serum ferritin concentration, and current or previous malaria infection were associated with any form of anemia (mild, moderate, or severe anemia) or moderate to severe anemia. The associations between gender, age, enrollment location, hemoglobin concentration or anemia and the presence of growth deficiencies (stunting, wasting, under/overweight) were also examined using simple logistic regression models. Comparisons of anemia and indicators of child growth between schools were adjusted for gender, age, and other relevant factors using multivariate logistic regression models to account for potential differences between schools. All statistical analyses were conducted with Stata software (Stata v12, StataCorp®, College Station Texas, TX, USA), with P values less than 0.05 considered statistically significant.
Prevalence of mild, moderate, severe anemia by gender, location, and WHO population group
WHO anemia classification
Prevalence by anemia category (%)
5 to 11
12 to 14
Male ≥ 15
Female ≥ 15
Anthropometric indicators of child growth by gender, location, and age group
Body Mass Index (BMI)
5 to 11
12 to 14
Male ≥ 15
Female ≥ 15
While often regarded as a proxy for malnutrition, the causes of chronic anemia can be multifactorial, including nutritional iron deficiency, blood loss from menstruation in females, chronic inflammation, infectious diseases such as malaria or intestinal helminths, and a range of inherited hemoglobinopathies [22, 23]. In this study normal serum ferritin concentrations were identified in the subset of children tested, although future, more comprehensive studies should include other diagnostic measures of anemia such as serum iron, transferrin, total iron binding capacity, and vitamins such as B12 and folic acid . Prior studies with students from School A have demonstrated low levels of carriage of soil-transmitted helminths  and national mass drug administration programs to eliminate lymphatic filariasis are active in both enrollment locations using chemotherapeutic agents also effective against the primary intestinal helminths . In this study, we also found no correlation between anemia and G6PD deficiency, current, or previous malaria infections for which this study was initially designed. In the process we observed that in School A, where a supplemental nutrition program supplied daily meals with proteins and leafy vegetables, children had significantly lower rates of anemia higher growth indicators compared to School B, where no such program existed. Despite the apparent reduction of anemia and children with normalized BMIs less than the global average, high levels of mild and moderate anemia were present in both schools, suggesting that other unknown factors are also operational and represent a priority for future research.
Although this study examined indicators of growth and anemia in Haitian schoolchildren, multiple pathways of anemia mentioned earlier were not able to be explored. The use of a convenience sample that consisted of only two enrollment sites, both schools, might not be representative of children not attending school or children from other departments of Haiti. Besides malaria, diagnostic testing for the presence of soil-transmitted helminth infections could have allowed for more adequate examination of the associations between such infections and anemia. A previous study  found that the prevalence of sickle cell traits in Gressier and Jacmel was between 6 and 14%, however sickle cell anemia or thalassemia were not examined in this study. Finally, though School A had an in-school nutritional supplementation program, food journals were not used to record the dietary intake of individual students, which could have revealed heterogeneity in diets within schools and additional dietary intakes outside of school, and affected the ability to compare anemia and growth indicators between schools.
Given the high prevalence of anemia in children above five years of age, future demographic and health surveys should be expanded to include this potentially vulnerable subpopulation. Future investigations of the etiology of anemia in Haiti should be expanded to include more comprehensive laboratory analyses of erythrocytes, iron metabolism, biomarkers of chronic inflammation, and more adequate assessment of nutritional attainment. Such studies would be useful for creating targeted public health interventions to reduce the prevalence of anemia in Haitian schoolchildren and ensure the attainment of development goals for maternal and child health.
Apical membrane protein one
Body mass index
Enzyme-linked immunosorbent assay
Merozoite surface protein one
Non government organization
Rapid diagnostic test
World Health Organization
The authors would like to extend a special thanks to the dedicated staff at the Christianville Foundation and the Hossana Baptist School, as well as the children and legal guardians of the participants. Without their support, this study would not have been possible.
This study was funded by the Armed Forces Health Surveillance Center, Global Emerging Infections Surveillance and Response Division to Bernard A. Okech and by University of Florida, College of Public Health and Health Profession funds to Michael E von Fricken.
Availability of data and materials
The dataset supporting the conclusions of this article is available in the form of an excel spreadsheet (.xls) or STATA data file (.dta) upon request from the corresponding author, Thomas A. Weppelmann.
TAW, MEV, MVB, GG, JGM, and BAO contributed to the conception and design of the study. MEV, RM, and BAO contributed to the collection of data. TAW and MEV analyzed and interpreted the results. All authors contributed to the drafting and revising of this manuscript. All authors read and approved the final manuscript.
The authors declare that they no competing interests.
Consent for publication
Ethics approval and consent to participate
Sample collection and enrollment were approved by the University of Florida based Institutional Review Board, the Haitian-based Institutional Review Committee, and the Office of Research Protections, United States Army Medical Research and Materials Command. Participants were given opportunities to ask our enrolling physicians/health professionals questions during informational sessions prior to informed consent. The parents/guardians of study participants provided consent on their children’s behalf.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
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