- Research note
- Open Access
Schistosomiasis, intestinal helminthiasis and nutritional status among preschool-aged children in sub-urban communities of Abeokuta, Southwest, Nigeria
BMC Research Notes volume 10, Article number: 637 (2017)
Schistosomiasis and intestinal helminthiasis are major public health problems with school-aged children considered the most at-risk group. Pre-school aged children (PSAC) are excluded from existing control programs because of limited evidence of infections burden among the group. We assessed the prevalence of infections and effect on nutritional status of preschool aged children in Abeokuta, Southwestern Nigeria.
A community-based cross-sectional study involving 241 children aged 0–71 months was conducted in 4 sub-urban communities of Abeokuta. Urine and faecal samples were collected for laboratory diagnosis for parasites ova. Nutritional status determined using age and anthropometric parameters was computed based on World Health Organization 2006 growth standards. Data were subjected to descriptive statistics analysis, Chi square, t-test and ANOVA. Of 167 children with complete data, 8 (4.8%) were infected with Schistosoma haematobium; Schistosoma mansoni 6 (3.6%); Taenia species 84 (50.3%); Ascaris lumbricoides 81 (48.5%) and hookworm 63 (37.7%). Overall, 46.7% of the children were malnourished, 39.5% stunted, 22.8% underweight and 11.4% exhibiting wasting/thinness. Mean values of anthropometric indices were generally lower in children with co-infection than those with single infection. We observed low level of schistosomiasis but high prevalence of intestinal helminthiasis and poor nutritional status that calls for inclusion of PSAC in control programs.
Nigeria is the most endemic Sub-Saharan African country for schistosomiasis and intestinal helminthiasis [1,2,3,4]. These diseases are closely linked to poverty, lack or inadequate safe water, sanitation and hygiene [5,6,7,8]. School-age children (SAC), pregnant women and PSAC are particularly at risk of morbidity of infection ; with chronic infection compromising growth, development, cognition, iron status and naivety of immune system which further increase susceptibility to infections .
Blood losses from haematuria and faecal occult blood from schistosomiasis affects iron balance and subsequently nutrition . Intestinal helminths given their peculiar niche also deprive hosts of essential nutrients. And endemicity in less-developed country like Nigeria is high such that the gastrointestinal tract of a child is often parasitized with at least one of the three most occurring geohelminths including A. lumbricoides, T. trichiura and hookworms [9, 10]. In fact, PSAC comprise between 10 and 20% of the 3.5 billion people living in soil transmitted helminths (STH) endemic areas [10, 12]. PSAC are nutritionally vulnerable segment of the population and defects during this developmental stage may persist for long and sometimes throughout life . Nutritional status of infected individual is altered through decline food intake, increase in nutrient wastage through loss of blood, vomiting, diarrhoea and can be aggravated by helminths infection [14, 15].
Dearth of information on burden of Schistosoma spp. and intestinal helminths infections in PSAC relative to SAC has been given as reason for exclusion from existing control programs [3, 10]. We investigate the prevalence of schistosomiasis, intestinal helminthiasis and nutritional status among PSAC living in sub-urban communities in Abeokuta, Nigeria.
A community-based cross-sectional survey was carried out in Ago-Ika, Ikereku-Idan, Itun-Seriki and Adebowale-Abowaba, communities in Abeokuta, Ogun State (Additional file 1: Figure S1) from February to June 2014. The communities are sub-urban without internal road network, with traditional mud houses and toilet facilities outside of the houses at considerable distance. There were no efficient drainage facilities, and predominant occupations include trading, artisans with few civil workers.
As no consistent definition of PSAC exists in medical literature in terms of age limit and/or school enrolment , PSAC for this study was defined as children aged 0–5 years; inclusive of children aged 5 years but yet to reach 6th birthdate irrespective of school enrolment status [3, 16]. Sample size was calculated from a total population figure of 2877 for children aged 0–5 years (ANLG Primary Health Care Unit, 2013). Using the method of  and estimated prevalence of 17% , a final sample size of 220 was calculated. Exhaustive sampling was done to ensure calculated sampling size was met with all households within each of the community with PSAC visited.
Ethical clearance was obtained from the Ethics review committee of the Federal Medical Centre, Abeokuta with Reference Number FMCA/238/HREC/14/2013. Approval to conduct the study was equally obtained from the Ogun State Ministry of Health and enrolment was after informed consent were obtained from parents/caregivers.
Pre-tested questionnaires (Additional file 2) developed were interviewer-administered to consented participants to obtain demographic data including age, gender and investigate knowledge; attitude and practices (KAP) exposing PSAC to infection with the assistance of parents/caregivers. Sample collection and handling was as previously described [18,19,20]. To explain briefly, two labelled, sterile universal plastic bottles were given to parents/caregiver for collection of midday urine (10.00 a.m.–1.00 p.m.) and faecal samples. Urine, collected in dark containers to prevent hatching of ova on exposure to sunlight, and faecal samples were then taken to the laboratory for analysis.
Anthropometric data of height, recumbent length (children < 2 years) and weight were obtained as described [19, 21]. Urine samples were examined for micro-haematuria and S. haematobium ova using reagent strip and sedimentation method . Faecal samples were processed using sodium-acetate acetic-acid formalin ether concentration method and examined for parasites ova under the microscope .
Data were analysed using IBM SPSS 20.0 (IBM, NY). Descriptive statistics was used to describe categorical variables. Chi square, t-test and ANOVA were used to test for significance. Nutritional status was determined using anthropometric height-for-age (HAZ), weight-for-age (WAZ), weight-for-height (WHZ), and body-mass-index-for-age (BAZ) z-scores calculated and compared with WHO 2006 child growth standard. Significant level was set at p < 0.05.
A total of 241 PSAC were enrolled for the study with 167 (69%) providing urine, faecal samples and complete questionnaire data (Additional file 3: Figure S2). Of these, 83 (49.7%) were males, and 84 (50.3%) were females with mean age of 3 years (Additional file 4).
Eleven (6.6%) PSAC had micro-haematuria with 6 (3.6%) children positive for S. haematobium infection. Females had higher mean intensity of infection (0.464/10 ml of urine) than the males (0.151/10 ml of urine) (p = 0.178). Prevalence of S. mansoni was 8 (4.8%) with males having higher mean egg per gram of faeces (0.259 epg) than the females (0.181) with no significant difference (p = 0.693). Intensity of infection increases with age in both Schistosoma infections. Six intestinal helminths including Taenia spp. (50.3%), A. lumbricoides (48.5%), hookworm (37.7%), T. trichiura (5.4%), Strongyloides stercoralis (4.2%) and Trichostrongylus spp. (4.2%) were observed with no significant difference by age and sex except infection by age in T. trichiura and Taenia spp. (p = 0.025 and p = 0.000 respectively). Taenia spp intensity was significantly different (p = 0.046) across age group (Table 1). Prevalence of co-infection with schistosomiasis and intestinal helminths was 6.0% with females 7 (70%) and 0–24 months 6 (60%) more infected.
Out of the total population, 78 (46.7%) were malnourished with no significant difference between sexes (p > 0.05). Approximately 23% were underweight (WAZ < − 2SD), 39.5% stunted (HAZ < − 2SD) and 11.4% wasting (WHZ < − 2SD)/thin (BAZ < − 2SD). Also, 28 (73.7%) of underweight, 51 (77.3%) of stunted and 14 (73.7%) of wasting/thin were infected with intestinal helminths respectively (Table 2). However, there was no significant difference between infected and non-infected PSAC. Also, 5.3, 4.5 and 5.9% of PSAC underweight, stunted and wasted were infected with Schistosoma spp. respectively. Mean Z-scores of nutritional indicators were generally lower in infected than non-infected children but not significantly different (Additional file 4).
Approximately 66% of the parents interviewed have no knowledge of schistosomiasis or its mode of transmission, and 61% of the studied PSAC had been exposed to the river with more than half before their first birthday (Table 3). Bathing (20.2%) is the major activity predisposing PSAC to infection, and 63.6% were bathed with water fetched from the river at home.
Indiscriminate defaecation is widespread in the study communities as 16.2% of the parent/caregiver engaged in open defaecation in surrounding bushes and 1.8% directly to the river. Although, 49% of household uses public tap water for domestic purposes, 13.2% still depends solely on water from the river for domestic usage. Only 9% of PSAC that have started consumption of staple foods have their hands washed with water and soap before eating. Of all the PSAC studied, 63.5% have dirty fingers and only 59.3% have their fingernails trimmed. 92% of PSAC have slippers/shoe, and 55% wear their shoes always (Table 3).
Schistosomiasis and intestinal helminths are major public health problems in sub-Saharan Africa with Nigeria being the most endemic for both diseases . Inclusion of PSAC in MDA treatment campaigns with anthelmintic, the major control intervention in Nigeria is necessary to actualize WHO vision to control/eliminate infections in endemic countries by 2020 [3, 10]. However, relative to overwhelming evidences of infection burden in SAC; available information in PSAC is less and further evidences are required. This study provides the first report of S. mansoni infection in PSAC in Abeokuta. Though observed prevalence is low, this is a drawback on control efforts as current estimate might not be reflective of actual infection burden. Emergence of genitourinary schistosomiasis in PSAC could be linked to poor sanitary behaviours and unsafe water contact practices in which children were exposed to infection source before their first birthday. Mothers/caregivers inadvertently expose their wards to Schistosoma infection when bathing them with infected water or when these children accompany them to the river for domestic activities . Educating mothers and caregivers on transmission routes and the role they play in exposing children to infection is thus critical to the success of control program.
High prevalence of intestinal helminthiasis observed provides evidence for the need for inclusion of PSAC in control programme using available opportunities . Prevalence of A. lumbricoides infection was higher than other reports in the country [23, 24] and compares with infection in SAC . However, prevalence of hookworm and T. trichiura is lower [10, 26,27,28,29]. Loss of essential nutrients necessary for healthy development, impairments in physical, intellectual and cognitive development are some of the burden of infection on PSAC and should be of public health concern . A. lumbricoides infection could result from contamination of household utensils, food and drinking-water handling equipment with parasite’s ova if safe human waste disposal methods or hand washing facilities are lacking . Hygiene practices were poor among the study population. Even though respondents claim regular hand-washing practice before eating, it is common for children to share foods when playing and they did so without washing hands. Also, majority of the PSAC reported possession and regular wearing of footwears, the veracity of these responses is unverifiable due to unwillingness of respondents to disclose their social status. Furthermore, children wearing protective shoes often remove it when playing on soil because they mostly have one and need to make the shoe last longer; thereby getting exposed to active penetration of infective hookworm larvae when playing in contaminated soil in their environment . Inadequate use of footwears is a risk factor in the transmission of hookworm infections [19, 27].
The prevalence of Taenia spp. observed in the study is higher than previous report . The high occurrence of Taenia spp. in PSAC requires further investigation to ascertain the route of transmission. The infection may have been acquired from consumption of improperly cooked meat/pork as it is common for parents/caregivers to feed PSAC with undercooked adult meals like fish, meat and beans aimed at hastening transition from breastfeeding to staple foods. Improper human faecal disposal predominant in the study communities is one of the factors responsible for sustaining transmission of Taenia spp. which may be acquired at any age from 2 years onward [30, 31]. This reinforces the need for inclusion of PSAC in chemotherapy as praziquantel administration is suitable for the treatment of both schistosomiasis and Taenia spp. infection.
Although probability of co-infection is high, no report exists for co-infection of schistosomiasis and intestinal helminths in PSAC in Nigeria. The prevalence of co-infection and exposure pattern to risk factors observed is similar to reports in SAC [3, 32]. Similarity in infection level and continual exclusion from preventive chemotherapy could be a major reason why PSAC constitute an important reservoir of helminths infection .
There was no significant relationship between the high prevalence of malnutrition and parasites infection, which may be due to low infection intensity. Similar observation has been reported among PSAC infected with geohelminths . Correlation analysis, although not significant, showed negative associations between helminths and nutritional status (Additional file 4); implying that a threshold could exists with which parasitic infection will have significant effect on nutritional status when other factors affecting nutrition are controlled. Age could also be a limiting factor given that the effects of these diseases are more pronounced in the long-term and might not be easily measured in the early developmental stage of PSAC. Causes of malnutrition are multifactorial and the social, economic and physical environment in which individual live are major determinant of the degree of association between parasites and nutritional status . Nevertheless, we found evidence that infection of schistosomiasis and intestinal helminths contributes a portion of risk to the development of malnutrition in PSAC and are as much of a public health problem as in SAC. The long-term effects of infection on growth, development and cognition of PSAC are enormous and cannot be ignored, even though assessing nutritional impacts of endemic infections could be quite difficult . These factors are further complicated by high prevalence of malnutrition and if not dealt with earlier, may contribute to reduced school attendance and higher susceptibility to disease, thereby compromising physical capacity and work opportunities in adulthood. As no intervention exists for helminths control in PSAC in Nigeria, this study in accord with WHO recommendation calls for inclusion of PSAC in helminths interventions in Nigeria.
Limitation of the study
The sample size limits the power of our findings and calls for caution in generalization of study findings. This was majorly due to political tension created during the study period that made considerable number of participants withdrawn (Additional file 2).
pre-school aged children
school aged children
soil transmitted helminths
World Health Organisation
Abeokuta North Local Government
Mass Drug Administration
Hotez PJ, Kamath A. Neglected tropical diseases in sub-Saharan Africa: review of their prevalence, distribution, and disease burden. PLoS Negl Trop Dis. 2009;3(8):e412. https://0-doi-org.brum.beds.ac.uk/10.1371/journal.pntd.0000412.
Hotez PJ, Asojo OA, Adesina AM. Nigeria:“Ground Zero” for the high prevalence neglected tropical diseases. PLoS Negl Trop Dis. 2012;6(7):e1600. https://0-doi-org.brum.beds.ac.uk/10.1371/journal.pntd.0001600.
Ekpo UF, Oluwole AS, Abe EM, Etta HE, Olamiju F, Mafiana CF. Schistosomiasis in infants and pre-school-aged children in sub-Saharan Africa: implication for control. Parasitology. 2012;139(7):835–41. https://0-doi-org.brum.beds.ac.uk/10.1017/s0031182012000029.
Oluwole AS, Ekpo UF, Karagiannis-Voules DA, Abe EM, Olamiju FO, Isiyaku S, Okoronkwo C, Saka Y, Nebe OJ, Braide EI, Mafiana CF. Bayesian geostatistical model-based estimates of soil-transmitted helminth infection in Nigeria, including annual deworming requirements. PLoS Negl Trop Dis. 2015;9(4):e0003740. https://0-doi-org.brum.beds.ac.uk/10.1371/journal.pntd.0003740.
Echazú A, Bonanno D, Juarez M, Cajal SP, Heredia V, Caropresi S, Cimino RO, Caro N, Vargas PA, Paredes G, Krolewiecki AJ. Effect of poor access to water and sanitation as risk factors for soil-transmitted helminth infection: selectiveness by the infective route. PLoS Negl Trop Dis. 2015;9(9):e0004111. https://0-doi-org.brum.beds.ac.uk/10.1371/journal.pntd.0004111.
Opara KN, Udoidung NI, Ukpong IG. Genitourinary schistosomiasis among pre-primary schoolchildren in a rural community within the Cross River Basin, Nigeria. J Helminthol. 2007;81(4):393–7.
Odebunmi JF, Adefioye OA, Adeyeba A. Hookworm infection among school children in Vom, Plateau state Nigeria. Am Eurasian J Sci Res. 2007;1:39–42.
Babatunde TA, Asaolu SO, Sowemimo OA. Urinary schistosomiasis among pre-school and school aged children in two peri-urban communities in Southwest Nigeria. J Parasitol Vector Biol. 2013;5(7):96–101. https://0-doi-org.brum.beds.ac.uk/10.5897/JPVB2013.0113.
Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, Hotez PJ. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet. 2006;367:1521–32.
Albonico M, Allen H, Chitsulo L, Engels D, Gabrielli AF, Savioli L. Controlling soil transmitted helminthiasis in pre-school-age children through preventive chemotherapy. PLoS Negl Trop Dis. 2008;2:e126.
Friedman JF, Kanzaria HK, Acosta LP, Langdon GC, Manalo DL, Wu H, Olveda RM, Mcgarvey ST, Kurtis JD. Relationship between Schistosoma japonicum and nutritional status among children and young adults in Leyte, the Philippines. Am J Trop Med Hyg. 2005;72(5):527–33.
World HEalth Organisation. Schistosomiasis and soil transmitted helminths infection-preliminary estimates of the number of children treated with albendazoles or mebendazole. Wkly epidemiol Rec. 2006;16:145–64.
Ramachandran P, Gopalan HS. Undernutrition & risk of infections in preschool children. Indian J Med Res. 2009;130:579–83.
Stephenson LS, Holland C. Impact of helminth infections on human nutrition. New York: Taylor and Francis Ltd; 1987.
Francis L, Kirunda BE, Orach CG. Intestinal helminth infections and nutritional status of children attending primary schools in Wakiso District. Central Uganda Int J Environ Res Public Health. 2012;9:2910–21. https://0-doi-org.brum.beds.ac.uk/10.3390/ijerph9082910.
Amin MA, Swar M, Kardaman M, Elhussein D, Nouman G, Mahmoud A, Appiah A, Babiker A, Homeida M. Treatment of pre-school children under 6 years of age for schistosomiasis: safety, efficacy and acceptability of praziquantel. Sudan JMS. 2012;7(2):67–76.
Araoye MO. Research methodology with statistics for health and social science. Ilorin: Nathadex Publishers; 2004. p. 115–21.
Ekpo UF, Alabi OM, Oluwole AS, Sam-Wobo SO. Schistosoma haematobium infections in preschool children from two rural communities in Ijebu East, Southwest Nigeria. J Helminthol. 2011. https://0-doi-org.brum.beds.ac.uk/10.1017/S0022149X11000459.
Omitola O, Mogaji HO, Oluwole AS, Adeniran AA, Alabi OM, Ekpo UF. Geohelminthes infections and nutritional status of preschool-aged children in a Peri-Urban settlement of Ogun State. Scientifica. 2016. https://0-doi-org.brum.beds.ac.uk/10.1155/2016/7897351.
Ekpo UF, Akintunde LD, Oluwole AS, Sam-Wobo SO, Mafiana CF. Urinary schistosomiasis among preschool children in a rural community near Abeokuta, Nigeria. Parasit Vectors. 2010;3:58.
Cogill B. Anthropometric Indicators Measurement Guide. Washington, D.C.: Food and Nutrition Technical Assistance Project, Academy for Educational Development; 2003.
Endriss Y, Elizabeth E, Rohr B, Rohr H, Weiss N. Methods in parasitology: SAF method for stool specimen. Basel: Swiss Tropical Institute; 2005.
Kirwan P, Asaolu SO, Abiona TC, Jackson AL, Smith HV, Holland CV. Soil-transmitted helminth infections in Nigerian children aged 0–25 months. J Helminthol. 2009;00:1–6. https://0-doi-org.brum.beds.ac.uk/10.1017/S0022149X08201252.
Udonsi JK, Ogan VN. Assessment of the effectiveness of primary health care interventions in the control of three intestinal nematode infections in rural communities. Publ Health. 1993;107:53–60.
Ekpo UF, Odoemene SN, Mafiana CF, Sam-Wobo SO. Helminthiasis and hygiene conditions of schools in Ikenne, Ogun State, Nigeria. PLoS Negl Trop Dis. 2008;2(1):e146. https://0-doi-org.brum.beds.ac.uk/10.1371/journal.pntd.0000146.
Opara KN, Udoidung NI, Opara DC, Okon OE, Edosomwan EU, Udoh AJ. The Impact of intestinal parasitic infections on the nutritional status of rural and urban school-aged children in Nigeria. Int J MCH AIDS. 2012;1(1):73–82.
Nmorsi OPG, Isaac C, Aashikpelokhai IS, Ukwandu NCD. Geohelminthiasis among Nigerian preschool age children. Int J Med Med Sci. 2009;1(10):407–11.
Sowemimo O, Asaolu S. Soil transmitted helminth infections in preschool and school aged children in Ekiti and Ile-Ife, Southwest Nigeria. J Epidemiol Community Health. 2011;65(1):A365. https://0-doi-org.brum.beds.ac.uk/10.1136/jech.2011.142976m.49.
Suchdev PS, Davis SM, Bartoces M, Ruth LJ, Worrell CM, Kanyi H, Odero K, Wiegand RE, Njenga SM, Montgomery JM, Fox LAM. Soil-Transmitted Helminth infection and nutritional status among urban slum children in Kenya. Am J Trop Med Hyg. 2014;90(2):299–305. https://0-doi-org.brum.beds.ac.uk/10.4269/ajtmh.13-0560.
Biu AA, Hena SA. Prevalence of human taeniasis in Maiduguri, Nigeria. Int J Biomedical Health Sci. 2008;4(1):25–7.
Dada BJO. Taeniasis, cysticercosis, and echinococcosis in Nigeria. J Helminthol. 1980;54(4):281–6.
Brito LL, Barreto ML, Silva RR, Assis AMO, Reis MG, Parraga IM, Blanton RE. Moderate- and low-intensity co-infections by intestinal helminths and Schistosoma mansoni, dietary iron intake, and anaemia in Brazilian children. Am J Trop Med Hyg. 2006;75(5):939–44.
Menzies SK, Rodriguez A, Chico M, Sandoval C, Broncano N, Guadalupe I, Cooper PJ. Risk factors for soil-transmitted helminth infections during the first 3 years of life in the tropics; findings from a birth cohort. PLoS Negl Trop Dis. 2014;8(2):e2718. https://0-doi-org.brum.beds.ac.uk/10.1371/journal.pntd.0002718.
Assis AMO, Prado MS, Barreto ML, Reis MG, Pinheiro SMC, Parrag IM, Blanton RE. Childhood stunting in northeast Brazil: the role of Schistosoma mansoni infection and inadequate dietary intake. Eur J Clin Nutr. 2004;58:1022–9.
Tanner S, Leonard WR, McDade TW, Reyes-Garcia V, Godoy R, Huanca T. Influence of helminth infections on childhood nutritional status in lowland Bolivia. Am J Hum Biol. 2009;21(5):651–6. https://0-doi-org.brum.beds.ac.uk/10.1002/ajhb.20944.
AAA and UFE conceived the study. AAA, OIO, AAA and HOM designed the study plan. AAA, DBO and AMO collect field data and laboratory analysis. AAA, EMA and ASO carried out the statistical analysis. AAA, HOM, ASO and EMA wrote the first draft of the manuscript. All authors read and approved the final manuscript.
We would like to acknowledge the parents and guardian of the preschool age children that participated in the study for their assistance during sampling collection. We also appreciate the Chairmen of the community development association of the study communities. The Assistance of Miss Moronfolu Adenike during field collection in Ago-Ika axis is also greatly appreciated.
The authors declare that they have no competing interests.
Availability of data and materials
Datasets obtained and generated during the study is available on reasonable request to the corresponding author. The data set cannot be made publicly available because of the study participants identifier information contained therein.
Consent to publish
Ethics approval and consent to participate
Ethical approval for the study was obtained from the Ogun State Ministry of Health, Abeokuta and ethical consent from the institutional review board of the Federal Medical Centre, Idi-Aba. Parents/caregivers of the children were thoroughly briefed about the study objectives during community development association meetings and individual house visits. Study participants were enrolled after parents/caregivers signed/thumbprint on informed consent forms.
No funding was received for this study.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Adeniran, A.A., Mogaji, H.O., Aladesida, A.A. et al. Schistosomiasis, intestinal helminthiasis and nutritional status among preschool-aged children in sub-urban communities of Abeokuta, Southwest, Nigeria. BMC Res Notes 10, 637 (2017) doi:10.1186/s13104-017-2973-2
- Preschool aged children
- NTDs control