Malaria, Helminths and Malnutrition: a Cross-Sectional Survey of School
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Ayeh‑Kumi et al. BMC Res Notes (2016) 9:242 DOI 10.1186/s13104-016-2025-3 BMC Research Notes RESEARCH ARTICLE Open Access Malaria, helminths and malnutrition: a cross‑sectional survey of school children in the South‑Tongu district of Ghana Patrick Ferdinand Ayeh‑Kumi1, Kantanka Addo‑Osafo2, Simon Kwaku Attah2*, Patience Borkor Tetteh‑Quarcoo2, Noah Obeng‑Nkrumah3, Georgina Awuah‑Mensah3, Harriet Naa Afia Abbey3, Akua Forson3, Momodou Cham4, Listowell Asare4, Kwabena Obeng Duedu5 and Richard Harry Asmah1 Abstract Background: As part of malaria characterization study in the South-Tongu district of Ghana, the current study was conducted to explore relationships between malaria, schistosomiasis, soil transmitted helminths and malnutrition in riparian community settings that had hitherto encountered episodes of mass deworming exercises. Methods: School-age children were enrolled in a cross-sectional study from April through July 2012. Stool and urine samples were examined respectively for helminths and Schistosoma haematobium. Blood samples were analyzed for malaria parasites and haemoglobin (Hb) concentrations, respectively. Anthropometric indices were measured. Rela‑ tionships were determined using generalized linear models. Results: The results show low numbers of asymptomatic Plasmodium falciparum (9.2 %, n 37/404) and S. haema- tobium (2.5 %, n 10/404) infections. The associations between significance terms in the =multivariate analysis for P. falciparum infections= were further assessed to test the significance of the product terms directly i.e., age in years [adjusted odds ratio (AOR), 3.1; 95 % confidence interval (CI) 1.1–5.6], Hb concentration (AOR 0.71; 95 % CI 0.42–2.3), and stunted malnutrition (AOR, 8.72; 95 % CI 4.8–25.1). The P. falciparum-associated decrease in= mean Hb concen‑ tration was 2.82 g/dl (95 % CI 1.63–4.1 g/dl; P 0.001) in stunted children, and 0.75 g/dl (95 % CI 1.59–0.085 g/dl; P 0.076) in the non-stunted cohort. The anaemia= -associated decrease in mean parasitaemia in stunted children was 3500= parasites/µl of blood (95 % CI 262.46–6737.54 parasites/µl of blood; P 0.036), and in non-stunted children 2127 parasites/µl of blood (95 % CI 0.27 to 4.53; P 0.085). Stunted malnutrition= was the strongest predictor of S. hae- matobium infection (AOR 11;− 95 % CI 3.1–33.6)= but significant associations as described for P. falciparum infections were absent. The population= attributable risk of anaemia due to P. falciparum was 6.3 % (95 % CI 2.5–9.3), 0.9 % (95 % CI 0.4–2.3) for S. haematobium, and 12.5 % (95 % CI 9.11–19.52) for stunted malnutrition. Conclusion: Plasmodium falciparum, S. haematobium, intestinal helminths and their co-infections were uncom‑ mon in our school-age children. Stunting exacerbated the extent to which malaria was associated with loss in Hb concentration. Keywords: Malaria, Haemoglobin, Schistosomiasis, Malnutrition, Stunting, School, Children, Ghana Background tributaries [1]. In recent times, comprehensive initiatives The South Tongu District is one of the 25 districts of the with health education, personal hygiene instructions, and Volta region of Ghana drained by the Volta river and its mass chemotherapy treatment in school-age children and high-risk adults have been emphasized in the Volta river *Correspondence: [email protected] basin [2–4]. There is the schistosomiasis control initiative 2 Department of Microbiology, University of Ghana School of Biomedical Ghana (SCIG) which aims to implement an integrated and Allied Health Sciences, Accra, Ghana Full list of author information is available at the end of the article national plan for sustainable control of schistosomiasis © 2016 Ayeh-Kumi et al. This 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. Ayeh‑Kumi et al. BMC Res Notes (2016) 9:242 Page 2 of 12 in Ghana [5]. There is also the West African interna- Study design tional parasite control (WACIPAC) whose initiatives have The target population comprised school-age children included the institution of preventive measures on schis- (ages 6–13 years) without manifestations compatible tosomiasis and soil transmitted helminths [6]. Malaria is with malaria in the past 14 days. Children on nutritional endemic in Ghana and represents a major cause of mor- supplements were excluded. Four primary schools across bidity and mortality in children of school-going age. An the district namely Dabala Evangelical, Tefle Presbyte- accurate information on burden of malaria at the district rian Church of Ghana, Sogakope Cuniberto, and the Tsa- level is requisite both to plan local parasitic control efforts vanya district assembly basic in Agbakope were selected and to measure the impact of such efforts especially in (Fig. 1). Children were selected using a 2-stage cluster riparian communities [7–9]. But targeting the correct set sampling procedure. At the first sampling stage, four of of interventions to these major parasitic groups may not seven district circuits in the study area were sampled be done effectively without regard for nutritional status systematically, with a sampling probability proportional [2, 10]. Nutrition plays a major role in maintaining health; to size, based on Ghana statistical service census data of and malnutrition appears to generate vulnerability to a 2009, as measured by the number of primary schools. At wide variety of diseases and general ill health. Whereas the second sampling stage, one primary school was ran- animal studies suggest that improved nutritional sta- domly selected within each circuit. Since malaria and tus is protective against malaria, consensus has yet to be helminth infections detected by blood, urine and stool reached regarding its effects in human populations [11]. analysis were our focus of interest, this study was con- More recent studies indicate either no evidence of benefit fined to children who could provide all study samples. or some benefits resulting from nutritional adequacy [2, 10]. In this paper, we describe as our primary outcome, Data collection data from a district survey on school-age children (SAC) Fieldwork took place from April to June of 2012. Parents (6–13 years) regarding the prevalence of malaria, schisto- and guardians were requested for assistance in provi- somiasis, and intestinal helminths in riparian community sion of information. Interviews were conducted in the settings that had hitherto encountered several episodes local dialect, Ewe, spoken by study participants. Data of preventive chemotherapy including mass deworming were abstracted through interviews using standard- exercises; and explore relationships between such infec- ized questionnaires with the help of trained field workers tions and nutritional inadequacies. (Additional file 1). Data was collected regarding the fol- lowing: demographics (gender and age), malnutrition sta- Methods tus (stunted, underweight, wasted), child’s knowledge of Study area and population causes of malaria, helminth infections and schistosomiasis, The study was conducted during the first annual rainy deworming, availability of toileting facilities in household, season (April through July) of 2012 in the South-Tongu sources of household water, child’s activity in any river and district, an area with seasonal malaria in Volta region, parent/guardian educational level. We also determined Ghana [4, 12]. The study area comprises 594.75 km2 the household socio-economic status using proxy meas- located on Latitude 5°58′37.2′′ and Longitude 0°38′49.2′′. ures based on the World Bank asset scores for Ghana [16]. Rainfall is bimodal with latter rains in September to For each enrolee, anthropometric measurements includ- November [13]. The main river draining the district is the ing height and weight were determined. The anthropo- Volta, which runs along its western border, but it is also metric indices height-for-age (HA), weight-for-age (WA), drained by lakes, streams and lagoons in the southern weight-for-height (WH) were expressed as Z-scores using sector of the district. Preliminary surveillance along the the WHO child growth standards [17, 18]. For all children, river bodies revealed lacustrine conditions favourable to axillary temperature was measured, and inquiry was made mosquito breeding, growth of aquatic weeds and breed- if they had experienced fever in the previous 14 days. ing of snails. Malaria, schistosomiasis, soil-transmitted helminths and onchocerciasis control programmes are Sample collection and examinations active in this area [14, 15]. The district has the Comboni Children were provided with plastic containers and hospital which offers primary health care and diagnostic requested to bring about 3 g of stool and 20 ml of urine at services. According to hospital records, malaria remains 10:00 a.m. in the morning. Stool samples were processed the number one cause of hospital admissions and child within 6 h of collection and examined microscopically morbidity and mortality in the district, with the predomi- within 1 h of preparation. They were examined for Schis- nant parasite being Plasmodium falciparum. Malaria tosoma mansoni and intestinal helminths by wet mount transmission occurs throughout the year with peaks dur- for ova and larvae. The formol-ether concentration tech- ing the two rainy seasons. nique was used to confirm the presence of parasites in Ayeh‑Kumi et al. BMC Res Notes (2016) 9:242 Page 3 of 12 Fig. 1 Map of Ghana showing South‑Tongu district (Study sites indicated with arrows). Tefle and Sogokope are to the eastern border of the district. Dabala and Agbakope occupy the western border of South‑Tongu.