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Original Article Giardia Intestinalis Infection Associated with Malnutrition in Children Living in Northeastern Brazil

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Original Article Giardia Intestinalis Infection Associated with Malnutrition in Children Living in Northeastern Brazil Original Article Giardia intestinalis infection associated with malnutrition in children living in northeastern Brazil Beatriz Coronato-Nunes1, Deiviane Aparecida Calegar1, Kerla Joeline Lima Monteiro1, Lauren Hubert Jaeger1, Elis Regina Chaves Reis2, Samanta Cristina das Chagas Xavier3, Lindsay Nicole Carpp4, Marli Maria Lima5, Márcio Neves Bóia6, Filipe Anibal Carvalho-Costa1,7 1 Laboratory of Epidemiology and Molecular Systematics, Oswaldo Cruz Foundation, Rio de Janeiro, Brasil 2 Coordination of Primary Health Care, Nossa Senhora de Nazaré Municipal Health Office, Nossa Senhora de Nazaré, Brasil 3 Laboratory of Trypanosomatid Biology, Oswaldo Cruz Foundation, Rio de Janeiro, Brasil 4 Fred Hutchinson Cancer Research Center, Seattle, WA, United States 5 Chagas Disease Eco-epidemiology Laboratory, Oswaldo Cruz Foundation, Rio de Janeiro, Brasil 6 Laboratory of Biology and Parasitology of Wild Reservoir Mammals, Oswaldo Cruz Foudation, Rio de Janeiro, Brasil 7 Regional Office Fiocruz Piauí, Teresina, Brasil Abstract Introduction: The present study aimed to determine the prevalence and factors associated with Giardia intestinalis infection, verifying its impact on the nutritional status of children in northeastern Brazil. Methodology: A cross-sectional study was conducted to obtain parasitological, sociodemographic, and anthropometric data in two municipalities in the states of Piauí and Ceará, northeastern Brazil. Results: Prevalence of giardiasis was 55/511 (10.8%). G. intestinalis was more frequent in people living in poverty (30/209 [14.4%], p = 0.041), performing open evacuation (26/173 [15%], p = 0.034), and drinking rainwater stored in cisterns (9/56 [16.1%], p = 0.005). The proportion of stunting and being underweight in children infected with G. intestinalis was significantly higher than that in uninfected children (5/23 [21.7%] vs. 10/179 [5.6%], p = 0.017, OR = 4.69, 95% confidence interval [CI] = 1.44–15.25 and 5/23 [21.7%] vs. 13/179 [7.3%], p = 0.038, OR = 3.54, 95% CI = 1.13–11.09, respectively). Infection with G. intestinalis remained significantly associated with stunting and being underweight after adjustment for poverty, municipality, sex, and age in a logistic regression multivariate model. Conclusions: In rural areas in northeastern Brazil, giardiasis has acquired great public health importance in the soil-transmitted helminths control era, impacting the nutritional status of children and requiring new approaches to diagnosis and treatment and translational research that could generate applicable solutions at the community level. Key words: Giardia intestinalis; nutritional status; intestinal parasites; northeastern Brazil; Brazil; poverty J Infect Dev Ctries 2017; 11(7):563-570. doi:10.3855/jidc.8410 (Received 19 March 2016 – Accepted 28 August 2016) Copyright © 2017 Coronato-Nunes et al. This is an open-access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Introduction G. intestinalis presents high levels of genetic Intestinal parasitoses are neglected conditions diversity, and its genotypes are clustered into distinct linked to poverty and poor sanitation, being more assemblages. Parasites isolated from humans have been prevalent in developing countries [1,2]. Among the characterized into two assemblages, A and B, both of protozoan parasites, Giardia intestinalis is present in which are distributed globally [8]. distinct sociodemographic settings, being a potentially Although G. intestinalis causes diarrhea in zoonotic pathogen [3-6]. This protozoan is transmitted travelers, a comprehensive study in developing by ingestion of cysts that are highly resistant and can countries did not observe any association between acute survive several months in harsh environments. diarrheal disease and G. intestinalis in children, Trophozoytes emerging from ingested cysts inhabit the possibly because infections are often chronic and proximal small intestine, where they multiply by binary apparently asymptomatic [9]. G. intestinalis fission [7]. pathogenicity is poorly understood and appears to be mediated by complex mechanisms, including Coronato-Nunes et al. – Giardiasis in northeastern Brazil J Infect Dev Ctries 2017; 11(7):563-570. enterocyte apoptosis and epithelial cell damage, which Methodology lead to malabsorption [7]. Setting and study design Giardiasis has been associated with protein-energy This cross-sectional survey was performed in malnutrition, micronutrient deficiency, iron deficiency Russas (RSS), in the state of Ceará, and Nossa Senhora anemia, and growth failure [10-12]; it is one of the most de Nazaré (NSN), in the state of Piauí (Figure 1). RSS harmful intestinal parasitosis to the physical has 69,833 inhabitants and a human development index development of children [10,13-15]. (HDI) of 0.674. RSS has a tropical semiarid climate and Policies for controlling intestinal parasites focus on belongs to the semiarid region in the Caatinga biome, soil-transmitted helminths (STHs) and schistosomiasis, “Bsh”, in the Köppen-Geiger system [20], and is and do not take into account the burden of protozoan subjected to prolonged periods of drought. NSN has parasites, which require different drugs/dosages and 4,556 inhabitants, a HDI of 0.586, and a tropical hot treatment durations [16-18]. The aims of the present climate, “As” [19], located in a transition region of study were to assess the prevalence and factors Caatinga to Cerrado biome. associated with G. intestinalis infection and to The study included four rural communities of RSS determine its impact on the nutritional status of children in 2013 (n = 213) and eight rural and one urban in rural northeastern Brazil. community of NSN in 2014 (n = 298). The sampling strategy was visiting all the houses that have children. All the residents were invited to participate, and written informed consent forms were signed. Figure 1. Map showing the localizations of the studied municipalities in northeastern Brazil: Russas, in the state of Ceará, and Nossa Senhora de Nazaré, in the state of Piauí. 564 Coronato-Nunes et al. – Giardiasis in northeastern Brazil J Infect Dev Ctries 2017; 11(7):563-570. Sociodemographic and sanitation data were obtained by Anthropometric measurements questionnaires. Per-capita family income stratified Weight, height, and arm circumference subjects into two groups: families receiving less than measurements were obtained from individuals between USD 38.5 per month (corresponding to the Brazilian 12 months and 14 years of age. Weight was measured poverty line) [20] and families with an income above to the nearest 0.1 kilogram using a digital floor scale. USD 38.5. Height and mid-upper arm circumference (MUAC) were measured to the nearest 0.1 cm. MUAC was Collection and processing of stool samples measured by wrapping a flexible tape around the left During domicile visits, containers without arm. Standing height was measured with a steel preservatives were distributed for stool collection. millimetered tape coupled to a steel framing square. Samples were processed through Ritchie’s modified Standard deviation scores (Z-scores) of height-for- ethyl acetate sedimentation technique [21], the zinc age (HAZ), weight-for-height (WHZ), weight-for-age sulfate centrifugal flotation technique [22], the Kato- (WAZ), and MUAC-for-age (MUACZ) were calculated Katz thick smear [23], and the Baermann-Moraes using the NutStat Module on EpiInfo 2000 (Centers for technique [24]. Disease Control and Prevention, Atlanta, USA) and the Table 1. Distributions of Giardia intestinalis infection based on sociodemographic characteristics in Russas and Nossa Senhora de Nazaré, 2013 and 2014. Russas (Ceará) Nossa Senhora de Nazaré (Piauí) Both cities N of Giardia N of Giardia intestinalis-positive intestinalis-positive P P P subjects/examined subjects/examined subjects (% positive) subjects (% positive) Characteristic Age group (years) 1–6 0/26 (0.0%) 7/70 (10%) 7/96 (7.3%) 7–14 10/56 (17.9%) 9/80(11.2%) 19/136 (14%) 15–21 1/16 (6.2%) 1/17 (5.9%) 2/33 (6.1%) 0.150 0.127 0.786 22–40 9/57 (15.8%) 6/76 (7.9%) 15/133 (11.3%) 41–60 6/40 (15%) 2/39 (5.1%) 8/79 (10.1%) > 60 4/18 (22.2%) 0/16 (0%) 4/34 (11.8%) Sex Female 19/107 (17.8%) 9/160 (5.6%) 28/267 (10.5%) 0.167 0.092 0.887 Male 11/106 (10.4%) 16/138 (11.6%) 27/244 (11.1%) Income per capita per month (USD) *USD 1 = BRL 4 Below the poverty 13/55 (23.6%) 17/154 (11%) 30/209 (14.4%) line (≤ 38.5) Above the poverty 0.024 0.098 0.041 line (> 38.5 and ≤ 17/158 (10.8%) 8/144 (5.6%) 25/302 (8.3%) 330) Site of defecation Latrines 20/166 (12%) 9/172 (5.2%) 29/338 (8.6%) 0.151 0.033 0.034 Open defecation 10/47 (21.3%) 16/126 (12.7%) 26/173 (15%) Main source of drinking water Desalinated brackish 13/138 (9.4%) - 13/138 (9.4%) water Rainwater from 9/56 (16.1%) - 9/56 (16.1%) cisterns Dam 1/4 (25%) 0.001 - 1.000 1/4 (25%) 0.005 Water trucks 7/15 (46.7%) - 7/15 (46.7%) Individual water well - 2/29 (6.9%) 2/29 (6.9%) Collective water well - 23/269 (8.6%) 23/269 (8.6%) / cisterns 55/511 Total 30/213 (14.1%) 25/298 (8.4%) 0.044 (10.8%) 565 Coronato-Nunes et al. – Giardiasis in northeastern Brazil J Infect Dev Ctries 2017; 11(7):563-570. World Health Organization’s 1978 growth chart [25]. Helminths were detected in 12/213 (5.6%) subjects Stunting, wasting, and being underweight were defined in RSS and 52/298 (14.4%) subjects in NSN. Neither by -2 standard deviations from mean HAZ, WHZ, and Ascaris lumbricoides nor Trichuris trichiura was WAZ, respectively, of the reference population [26]. found. Hookworm (3.7% in RSS and 14.1% in NSN), Hymenolepis nana (1.4% in RSS and 0.3% in NSN), Statistical analysis Strongyloides stercoralis (0.5% in RSS and 0.3% in G.
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