Multivariate analysis of factors associated with Schistosoma mansoni and hookworm infection among primary school children in rural Bahir Dar, Northwest Ethiopia

Multivariate analysis of factors associated with Schistosoma mansoni and hookworm infection among... Background: Soil-transmitted helminths and Schistosoma mansoni infections are the major causes of morbidity and mortality in Sub-Saharan countries. The highest burden of the disease resides in school-age children. Poor water sanitation and hygiene are believed to be the major contributing factors for the high prevalence. Therefore, the goal of this study was to determine the prevalence of intestinal parasite infections in rural Bahir Dar, Northwest Ethiopia. Methods: A cross-sectional study was conducted from April 2017–June 2017 among 409 randomly selected primary school children. A structured questionnaire was used to obtain socio-demographic information and determinant factors through interviewing the students. Stool examination was done by Ritchie’s concentration method. The data were entered and analyzed using SPSS version 22. Prevalence of helminthic infections was calculated using descriptive statistics. The association between helminthic infection and determinant factors was determined by Bavarian regression. The confounding effect was checked by multivariate regression at 95% confidence interval. Any association was significant when the p-value was < 0.05. Result: The overall prevalence of intestinal parasite infection was 47.2%.(193/409).. The prevalence of Hookworm species and Schistosoma mansoni was 31.1 and 8.0%, respectively. Co-infection of Hookworm species with Schistosoma mansoni was 5.1% (21/409). The highest prevalence of Schistosoma mansoni was recorded for boys (21%), older children (21.4%) and rural children (17.6%) (P <0.05). Schistosoma mansoni infection was also higher among children whose household drinking water was sourced from streams/rivers (P < 0.05). The multivariate analysis showed lower odds of Schistosoma mansoni infection for those with no history of bathing (AOR = 3.7, 95% CI: 1.1–12.2; P = 0.034), washing clothes/utensils (AOR = 3.4; 95% CI: 1.2–9.7; P = 0.022), swimming (AOR = 2.8, 95% CI: 1.2–6.9; P = 0.023), and irrigation (AOR = 2.8, 95% CI: 1.3–6.0; P = 0.01). Significantly, higher odds of Hookworm infection was recorded for older children (AOR = 2.3, 95% CI: 1. 08–4.89; P = 0.029), boys (AOR = 1.9, 95% CI: 1.12–3.24; P = 0.018), and rural children (AOR = 1.8, 95% CI: 1.04–3.0; P = 0.037). Regular shoe wearing (AOR = 0.29, 95% CI: 0.16–0.50; P = 0.00) is protective for hookworm infection. Higher odds of hookworm infection was also recorded for schoolchildren who had the habit of eating raw vegetables (AOR = 1.2 95% CI: 1.1–1.7 P = 0.011). (Continued on next page) * Correspondence: mgbeyney@gmail.com Department of Medical Laboratory Science, Bahir Dar University, Bahir Dar, Ethiopia Full list of author information is available at the end of the article © The Author(s). 2018 Open Access 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. Hailu et al. Tropical Diseases, Travel Medicine and Vaccines (2018) 4:4 Page 2 of 7 (Continued from previous page) Conclusion: Hookworm infection and schistosomiasis are prevalent in the school children in rural Bahir Dar in Northwest Ethiopia. Various activities and behaviors of the children were strongly associated with helminthic infection. Hence health education should be delivered regularly to minimize/avoid the risky behaviors and water-based activities. Deworming programs should also be implemented on a regular basis. Keywords: Helminth, Hookworm, Schistosoma, Sebatamit, Bahir Dar Background factors among school children was conducted in rural Soil-transmitted helminthiasis and schistosomiasis are the Bahir Dar, Amhara Regional National State, Northwest most common parasitic infections especially in developing Ethiopia from April–June 2017. countries [1]. Nearly, 1.5 billion people (24% of the world’s The altitude of the area is between 648 and 1300 m population) are infected with soil-transmitted helminths.- above sea level. The annual temperature and rainfall of More than 267 million preschool-age children and over 568 the study area are 18–22 °C and 1419 mm, respectively. million school-age children live in areas where these para- There is a small-scale irrigation on Andasa and Abay sites are intensively transmitted. [2]. Based on the World rivers in the study area. Health Organization (WHO) estimation, there are 700–900 In this particular study, Sebatamit primary school million hookworm and 200 million Schistosoma infections students age ranging from 7 to 14 years and willing to worldwide [3]. They are the major causes of morbidity and participate in the study were included. A total of 409 mortality in the Sub-Saharan countries [3, 4]. The disease students from grade 1–7 were recruited to the study. burden and the public health importance of these parasites Systematic random sampling technique was used to select are still concerns in developing countries like Ethiopia [5]. the classes in the school and the students in each class. All Poverty, poor living conditions, personal and environ- Sebatamit primary school students aged 7–14 years and mental hygiene, sanitation and water supply facilities are signed the assent form and parents signed written consent some of the contributing factors for the high prevalence of forms were included. soil-transmitted helminths and Schistosoma mansoni [6]. Moreover, the high prevalence of schistosomiasis is mainly Data collection associated with poor water management system during irri- A structured questionnaire was used to obtain gation, close contact habit to freshwater bodies, open socio-demographic information, present and past history defecation and wide distribution of the snail intermediate of the participants and environmental related factors by host [7]. interviewing the students. The questionnaire was filled Infections by soil-transmitted helminths and Schistosoma by nurses. The data collectors were regularly supervised species lead to malnutrition, iron deficiency anemia, within ten participants’ variation by the principal stunted growth and increased vulnerability to other infec- investigator. tions [8] and low educational achievement in school chil- Freshly passed stool specimens were collected using a dren [9].Current control programs for helminths infection clean plastic cup at the school. The stool cups were focused on reducing infection intensity and transmission labeled based on their section and role number. The potential, primarily to reduce morbidity and avoid mortality laboratory professionals took part in all processes of associated with the disease [10]. stool collection, transportation, and examination. The Despite a range of prevention and control efforts of hel- stool samples were processed for microscopic examin- minthicinfections, theprevalenceof soil-transmittedhel- ation by Ritchie’s concentration method. The stool minths and schistosome infections is still high in several examination was done in Bahir Dar University, College localities of Ethiopia. There is also a lack of information on of Medicine and Health Sciences, Department of Micro- the factors of S. mansoni and soil-transmitted helminths in- biology, Immunology, and Parasitology teaching fections in the study area. Therefore, the aim of this study laboratory. was to assess the magnitude of helminth infections and as- sociated risk factors so that to design effective prevention Ritchie’s concentration method and control measures. About 2.5 ml of formalin and 1 ml of ethyl acetate was in the sample collection tube. Then, 0.5 g of stool sample Materials and methods was put inside the sample collection tube and left to stand Study design, area and period for a minute. Both pieces of the device were screwed until A cross-sectional study, aimed at determining the preva- it is well closed and centrifuged at 1000 rpm for 3 min. lence of intestinal parasite infections and determinant The sample collection tube and filtration concentration Hailu et al. Tropical Diseases, Travel Medicine and Vaccines (2018) 4:4 Page 3 of 7 unit were discarded. The supernatant was removed from School children who frequently encounter contact with the conical tube and a small amount of sediment was put stream/river water during bathing (AOR = 3.7, 95% CI: on a glass slide for examination at 10× & 40× objectives. 1.1–12.2; P = 0.034), washing clothes (AOR = 3.4, 95% CI: 1.2–9.7; P = 0.022), swimming (AOR = 2.8, 95% Data quality assurance CI:1.2–6.9; P = 0.023) and irrigation (AOR = 2.8, 95% To ensure reliable data collection, training of nurses and CI:1.3–6.0; P = 0.01) had higher odds of S. mansoni in- laboratory technicians on data collection and explan- fection (Table 2). ation about the study were given before sample collec- The overall prevalence of hookworm infection was tion. The data collection, application of standard 41.1%. Significantly higher proportions of Hookworm in- procedures, and accuracy of test results were supervised fection were recorded for older children (AOR = 2.3, 95% by the principal investigator. Close follow up by the CI: 1.08–4.89; P = 0.029), boys (AOR = 1.9, 95% CI: 1.12– principal investigator within ten patients’ variation dur- 3.24; P = 0.018), rural children (AOR = 1.8, 95% CI: 1.04– ing data collection process was done. Specimens were 3.0; P = 0.037). Regular shoe wearing (AOR = 0.29, 95% CI: cross-checked by the principal investigator to increase 0.16–0.50; P = 0.00) was protective for hookworm infec- the accuracy of laboratory results. tion. Higher odds of hookworm infection was also re- To eliminate observer bias, the smears were examined corded among schoolchildren who did not have the habit independently with experienced laboratory technologists of regular latrine usage (55.8%), those practicing geophagy and 10% of the total slides will be randomly selected and (50.6%) and eat raw vegetables (48.2%) (Table 3). read by the principal investigator. The results of their observation were recorded for later comparison on separate Discussion sheets. A quality control was done by repeating all discord- Epidemiological study on the prevalence and distribution ant results. of helminthic species in different localities is a primary objective to identify high-risk communities and formu- Data analysis late appropriate intervention [11]. Assessing factors Data were entered and analyzed using SPSS version 22 stat- istical software. Overall magnitude, of parasitic infection, Table 1 Prevalence of intestinal parasites among primary was calculated using descriptive statistics. The strength of schoolchildren in rural Bahir Dar, Northwest Ethiopia, 2017 association between parasites infections and determinant Parasite species No infected Percent factors was calculated by binary logistic statistics. Those (n = 409) variables with P<0.2 in thebinarylogisticregressionwere Single infection taken to multiple regression analysis and the AOR was cal- Hookworm Spp 130 31.7 culated to control potential confounders. P-values less than Schistosoma mansoni 33 8.0 0.05 were taken statistical significant. Entamoeba histolytica 22 5.4 Ascaris lumbricoides 5 1.2 Results The overall prevalence of single, double and triple intestinal Strongyloides stercolaris 1 0.2 parasite infection was 47.2, 10.0 and 0.98%, respectively. Taenia spp 1 0.2 Hookworms (31.7%) were the predominant species identi- Giardia lamblia 1 0.2 fied followed by Schistosoma mansoni (8.0%), and Ent- Double infection amoeba histolytica (5.4%) (Table 1). The highest prevalence S. mansoni + Hookworm spp 17 4.2 of S.mansoni was recorded for boys (21%), older children Hookworm spp + E. histolytica 16 3.9 (21.4%) and rural children (17.6%) (P < 0.05). S.mansoni in- fection was also higher among children whose family drink- Hookworm + Giardia lamblia 3 0.7 ing water was sourced from streams (P < 0.05). The odds of E. histolytica + Giardia lamblia 2 0.5 infection was higher in this group (AOR = 0.34, 95% CI: A.lumbricoides + E. histolytica 1 0.2 0.162–0.707; P = 0.004) (Table 2). S. mansoni + E. histolytica 1 0.2 Domestic activities accounted for the majority of re- S. mansoni + A. lumbricoides 1 0.2 ported water contacts. The majority (69.4%) of subjects Triple infection interviewed reported that they bathed in the nearby stream. Similarly, about 65% of the respondents encoun- S. mansoni + Hookworm spp + E. histolytica 1 0.2 tered water contact for washing clothes. Besides, 57.7% S. mansoni + Hookworm spp + G. lamblia 2 0.5 of the school children frequently practiced swimming. S. mansoni + Hookworm spp + S. stercolaris 1 0.2 About half of respondents reported that the water for Negative 172 42.0 drinking and cooking was collected from streams. Hailu et al. Tropical Diseases, Travel Medicine and Vaccines (2018) 4:4 Page 4 of 7 Table 2 The prevalence and factors associated with Schistosoma mansoni among primary schoolchildren in rural Bahir Dar, Northwest Ethiopia, 2017 Variables Schistosma mansoni infection P-value AOR (95% CI) Positive n (%) Negative n (%) Total (n = 409) Age 7–10 28 (10.1) 250 (89.9) 278 (68.0) 0.002 2.1 (1.1–4.2) 11–14 28 (21.4) 103 (78.6) 131 (32.0) Sex Male 39 (21.0) 147 (79.0) 186 (45.5) 0.002 2.9 (1.5–5.7) Female 17 (7.6) 206 (92.4) 223 (54.5) Residence Urban 41 (17.6) 192 (82.4) 223 (57.0) 0.002 0.301 (0.14–0.64) Rural 15 (8.5) 161 (91.5) 176 (43.0) Water source Pipe 15 (7.5) 184 (92.5) 199 (48.7) 0.004 3.0 (1.41–6.2) Stream 41 (19.5) 169 (80.5) 210 (51.3) Bathing Yes 52 (18.3) 232 (81.7) 284 (69.4) 0.034 3.7 (1.1–12.2) No 4 (3.2) 121 (96.8) 125 (30.6) Washing clothes Yes 51 (19.2) 215 (80.8) 266 (65.0) 0.022 3.4 (1.2–9.7) No 5 (3.5) 138 (96.5) 143 (35.0) Swimming Yes 49 (20.8) 187 (79.2) 236 (57.7) 0.023 2.8 (1.2–6.9) No 7 (4.0) 166 (96.0) 173 (42.3) Irrigation Yes 45 (19.7) 183 (80.3) 228 (55.7) 0.010 2.8 (1.3–6.0) No 11 (6.1) 170 (93.9) 181 (44.3) Total Positive 56 (13.7) 353 (86.3) 409 (100) associated with the infection of parasites enables deter- For instance, males encounter frequent water contacts for mining priorities for public health measures to prevent swimming, bathing and agricultural activities (irrigation), parasitic infections [12]. while females reported more contacts for household activ- The overall prevalence of S. mansoni was 8.0% in our ities such as washing clothes and/or utensils and fetching study and it was lower than other studies conducted water for household consumption from rivers/streams. among school children in different parts of Ethiopia which Age was also the other independent variable found to reported prevalence greater than 30% [13–18]. This lower be significantly associated with S. mansoni infection in prevalence might be attributed to the sporadic deworming the multivariate analysis. Accordingly, the prevalence of programs conducted by Amhara Regional Health Bureau. S. mansoni was higher in the oldest age group (11–14) The multivariate analysis showed that sex was independ- years. This is consistent with reports of many re- ently associated with S. mansoni infection in our study. searchers in different localities of Ethiopia in which Consequently, the prevalence of S. mansoni was signifi- schistosomiasis was consistently higher in the second cantly higher in males than females. It was consistent with decade of life [22–25]. This might be justified by the fact findings from different parts of Ethiopia [19–22]. How- children in this age group encounter frequent/regular ever, higher prevalence of Schistosoma mansoni infection water contacts for leisure (swimming, bathing) and agri- in females than males was reported in different localities cultural activities (irrigation) and washing clothes. Simi- of Ethiopia such as Gorgora [19], Tseda [20], and Zarima larly, higher rate of infection was observed for rural [21]. These inconsistent reports might be attributed to dif- children than urban counterparts. This is in agreement ferences in water contact behavior of males and females. with other studies conducted in northwest Ethiopia and Hailu et al. Tropical Diseases, Travel Medicine and Vaccines (2018) 4:4 Page 5 of 7 Table 3 The prevalence and factors associated with Hookworm infection among primary schoolchildren in rural Bahir Dar, Northwest Ethiopia, 2017 Variables Hookworm infection P-value AOR (95% CI) Positive n (%) Negative n (%) Total (n = 409) Age (Yrs) 7–9 154 (44.5) 192 (55.5) 346 (84.6) .029 2.3 (1.09–4.89) 10–14 14 (22.2) 49 (77.8) 63 (15.4) Sex Male 78 (41.9) 108 (58.1) 186 (45.5) .018 1.9 (1.12–3.24) Female 90 (40.4) 133 (59.6) 223 (54.5) Residence Urban 74 (31.8) 159 (68.2) 223 (57.0) .037 1.8 (1.04–3.01) Rural 94 (53.4) 82 (46.6) 176 (43.0) Hand wash before meal Yes 128 (36.1) 227 (63.9) 355 (86.8) .010 2.9 (1.29–6.65) No 40 (74.1) 14 (25.9) 54 (13.2) Regular latrine use Yes 28 (17.7) 130 (82.3) 158 (28.6) .012 2.2 (1.19–4.18) No 140 (55.8) 111 (44.2) 251 (61.4) Frequency of shoe wearing Always 44 (10.8) 163 (67.6) 1 (0.2) .000 0.3 (0.16–0.50) Sometimes 124 (30.3) 78 (32.4) 408 (99.8) Geophagy Yes 44 (50.6) 43 (49.4) 87 (21.3) .052 1.6 (1.0–2.6) No 124 (38.5) 198 (61.5) 322 (78.7) Irrigation Yes 90 (39.5) 138 (60.5) 228 (55.7) .050 1.61 (1.00–2.60) No 78 (43.1) 103 (56.9) 181 (44.3) Eating raw vegetables Yes 137 (48.2) 147 (51.8) 284 (69.4) .011 1.2 (1.1–1.7) No 3 1(24.8) 94 (75.2) 125 (30.6) Total Positive 168 (41.1) 241 (58.9) North Ethiopia [24].This might be due to the higher ten- examination and the time of the study, and sample size dency of infested water exposure of rural children as used. they are frequently engaged in water-based activities Several cross-sectional studies have identified the risk such as irrigation as they inhabit in the proximity of factors of hookworm infection in the world. Hookworm Abay and Andasa rivers. infection is acquired via exposure to the soil where filari- The habit of frequent contact with cercariae-infested form larvae live in and penetrate human skin. In water such as swimming in the river, washing clothes and addition, Ancylostoma duodenale is also acquired by in- utensils using river water, and irrigation activities showed a gestion of food contaminated by the filariform larvae. statistically significant association with S. mansoni infection. Similarly, our study showed several factors are signifi- This is similar to the previous findings reported in Ethiopia cantly related to hookworm infection. Consequently, the [21, 22, 26, 27], and elsewhere [28, 29]. The prevalence of S. odds of hookworm infection was 1.9 times higher in mansoni was higher in school children who had a habit of boys than girls. It was in agreement with studies con- frequent swimming, washing clothes, bathing and engaging ducted in certain parts of Ethiopia [30, 39, 40] and Brazil in irrigation activities than those who did not. This might [41]. The higher prevalence of hookworm in boys in our be due to the presence of cercariae infected water bodies in study might be because boys usually help their parents the surrounding of study areas. in agricultural activities where shoe wearing is not con- The overall prevalence of hookworm in this study is venient. We also observed that most of the school chil- 41.1%. It was comparatively lower than previous reports dren and particularly boys wore non-protective shoes from different areas of Ethiopia [30, 31], and Paraguay (“ergendo” in Amharic). [32]. Higher than the present finding was reported in Multivariate analysis also revealed that children aged Gorgora [19], Mirab Abaya [33], western Ethiopia [34], 10–14 years were 2.3 times at higher odds of hookworm south Ethiopia [35], Plateau State Nigeria [36, 37], and infection compared to their younger counterparts. This Thailand [38]. The observed differences in the rate of might be attributed to their play behavior and lack/ig- infection could be due to variations in geography and norance of shoe wears. On the other hand regular shoe types of soil, socio-economic conditions, hygienic prac- wearing was found to protective for hookworm infection tices of the population, the methods employed for stool in our study (AOR = 0.3, 95% CI: 0.16–0.50; P = 0.00). It Hailu et al. Tropical Diseases, Travel Medicine and Vaccines (2018) 4:4 Page 6 of 7 was in agreement with other studies conducted in differ- letter was obtained from Amhara Regional Educational Bureau, and provided to the specific study area to conduct the research. ent parts of Ethiopia [21, 42]. Parents of children were informed of their children’s participation and gave This might be because the mode of transmission of informed written consent for their children to participate. Assents were also hookworm species is often through barefoot penetration collected from children. Participants positive for any of the soil-transmitted helminths were treated with a single dose of Mebendazole (500 mg) and by infective filariform larvae. Praziquantel (40 mg/kg, single dose) was given for children infected with Eating raw vegetables was also strongly associated with Schistosoma mansoni. hookworm infection. This might be explained by fact that Ancylostoma duodenale can be acquired by inges- Competing interests The authors declare that they have no competing interests. tion of filariform larvae in food, and this epidemiological feature can possibly occur in areas where A. duodenale predominates [43]. However, this study lacks evidence Publisher’sNote Springer Nature remains neutral with regard to jurisdictional claims in on the hookworm species that prevails in the study area. published maps and institutional affiliations. Rural children were at higher odds of hookworm infec- tion than their urban counterparts. This might be attrib- Author details Department of Medical Laboratory Science, Bahir Dar University, Bahir Dar, uted to a higher frequency of exposure to soil` due to Ethiopia. Department of Pharmacy, Bahir Dar University, Bahir Dar, Ethiopia. lack of shoes, and during agricultural activities, playing and coming to the school of the rural children. Received: 3 April 2018 Accepted: 23 May 2018 Conclusion References Hookworm infection and schistosomiasis are public 1. WHO. Prevention and control of intestinal parasitic infections, WHO technical report series 741. Geneva: WHO; 1987. health concerns in the study area. Various demographic 2. WHO. Soil-transmitted-helminth infections. http://www.who.int/en/news- characteristics, water based activities and recreational room/fact-sheets/detail/soil-transmitted-helminth-infections. water contact were strongly associated with S. mansoni 3. Crompton DW. How much helminthiasis is there in the world? J Parasitol. 1999;85:397–403. infection. Similarly, failure to wear shoe regularly and 4. Ross AG, Bartley PB, Sleigh AC, Olds GR, Li Y, Williams GM, McManus DP. other risky behaviors of children, such as geophagy and Schistosomiasis. N Engl J Med. 2002;346:1212–20. eating raw vegetables were also predictors of hookworm 5. Leykun J. Soil transmitted- helminthic infection and S. Mansoni in school children from Chilga district, Northwest Ethiopia. Ethiop J Health Sci. 2001; infection. Hence health education should be delivered 11:79–87. regularly to minimize/avoid the risky behaviors and 6. Ohaeri CC, Orji NB. Intestinal parasites among undergraduate students of water-based activities and deworming programs should Michael Okpara university of agriculture, Umudike Abia state, Nigeria. World Appl Sci J. 2013;25(8):1171–3. also be implemented on a regular basis. 7. WHO. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. Geneva: WHO technical report series; 2002. Abbreviations 8. Obiamuiwe BA. Nmorsi. Human gastro-intestinal parasites in Bendel state, AOR: Adjusted Odds Ratio; CI: Confidence interval; OR: Odds ratio; Nigeria. Nigerian J Parasitol. 1990;32:177–83. SPSS: Statistical Product and Service Solutions 9. Nokes C, Cooper ES, Robinson BA, Budy DAP. Geohelminth infection and academic assessment in Jamaican children. Trans R Soc Trop Med Hyg. Acknowledgments 1991;85:272–3. We are thankful to laboratory personnel and nurses who were actively 10. Albonico M, Allen H, Chitsulo L, Engels D, Gabrielli AF, et al. Controlling soil- involved in data collection. We also forward our gratitude for teachers at transmitted helminthiasis in pre-school-age children through preventive Sebatamit primary school. chemotherapy. PLoS Negl Trop Dis. 2008;2:e126. 11. Brooker S, Moulin A, Luoba D, Bundy M, Kremer D. Epidemiology of single Funding and multiple species of helminth infections among school children in Busia The research project was not funded by any organization. district. Kenya East Afr Med J. 2000;77:157–68. 12. Lima E, Rocha R, Leite M, Carneiro R, Colley D, Gazzinelli G, Katz N. A Availability of data and materials multivariate analysis of socio-demographic factors, water contact patterns To generate findings of this particular study, data was collected and and Schistosoma mansoni infection in an endemic area in Brazil. Rev Inst analyzed based on the stated methods and materials. All the data were Med Trop São Paulo. 1991;33(1):58–63. incorporated in the manuscript and no supplementary files accompanied the 13. Jemaneh L. Schistosoma mansoni and geo-helminthiaisis in school children in submission. The original data supporting this finding will be available at any Dembia plains. Northwestern Ethiopia Ethiop J Health Sci. 1998;12:237–44. time upon request. 14. Jemaneh L. Intestinal helminth infection in school children in Gondar town and surrounding areas, Northwest Ethiopia. Ethiop J Health Sci. 1999;22:209–20. Authors’ contributions 15. Jemaneh L. The epidemiology of Schistosoma mansoni and soil transmitted TH designed the study and wrote the manuscript; MA participated in the helminths in elementary school children from the South Gondar zone of design of the study, data collection and write-up of the manuscript; BA the Amhara national regional state, Ethiopia. Ethiop Med J. 2008:105–16. participated in data analysis and revision of the manuscript, WM analyzed 16. Roma B, Worku S. Magnitude of Schistosoma mansoni and intestinal data and wrote the manuscript, EY participated in data analysis and write-up, helminthic infections among school children in Wondo genet Zuria. AG and FB participated in manuscript write-up. All authors read and Southern Ethiopia Ethiop J Health Dev. 1997;11:125–9. approved the final manuscript. 17. Mammo B, Asseffa B, Loc T. (). Intestinal helminths in Akaki town, with special emphasis on epidemiology of Schistosoma mansoni. Ethiopian Med Ethics approval and consent to participate J. 1989;3:183–91. The proposal was ethically approved by the ethical review committee of 18. Erko B, Tedla S. Intestinal helminths infection in Zeghie, Ethiopia, with Bahir Dar University, College of Medicine and Health Science. Permission emphasis on Schistosoma mansoni. Ethiop J Health Dev. 1993;7:21–6. Hailu et al. Tropical Diseases, Travel Medicine and Vaccines (2018) 4:4 Page 7 of 7 19. Essa T, Birhane Y, Endris M, Moges A, Moges F. Current status of concentrations in residents of Salvador Bahia, Brazil. Rev Inst Med Trop São Schistosoma mansoni and associated risk factors among students in Gorgora Paulo. 2013;55(4):233–8. town, Northwest Ethiopia. International Scholarly Research Notices. 2013; 42. Abera B, Alem G, Yimer M, Herrador Z. Epidemiology of soil-transmitted 2013(Article ID 636103):7. helminths, Schistosoma mansoni, and haematocrit values among 20. Moges F, Belyhun Y, Tiruneh M, Kebede Y, Mulua A, Kassu A. Intestinal schoolchildren in Ethiopia. J Infect Dev Ctries. 2013;7(3):253–60. parasite infections in association with cutaneous fungal infection and 43. Gillespie SH, Pearson RD. Principles and practice of clinical parasitology. 2nd nutritional status among schoolchildren in Tseda, northwest Ethiopia. Ethiop ed. Toronto: Wiley; 2001. J Heal Biomed Sci. 2010;3(1):35–43. 21. Alemu A, Atnafu A, Addis Z, Shiferaw Y, Teklu T, Mathewos B, Birhan W, Gebretsadik S, Gelaw B. Soil transmitted helminthes and Schistosoma mansoni infections among school children in Zarima town, Northwest Ethiopia. BMC Infect Dis. 2011;11:189. 22. Awoke W, Bedimo M, Tarekegn M. Prevalence of schistosomiasis and associated risk factors among students attending at elementary schools in Amibera district, Ethiopia. Open J Prev Med. 2013;3(2):199–204. 23. Grum T. The prevalence of intestinal helminthic infections and associated risk factors among school children in Babile town, eastern Ethiopia. Ethiop J Health Dev. 2005;19:140–7. 24. Assefa A, Dejenie T, Tamass Z. Infection prevalence of Schistosoma mansoniand associated risk factors among schoolchildren in suburbs of Mekelle city, Tigray. North Ethiopia MEJS. 2013;5(1):174–88. 25. Mitiku H, Legesse M, Teklemariam Z, Erko B. Transmission of Schistosoma mansoni in TikurWuha area. Southern Ethiopia. Ethiop J Health Dev. 2010; 24(3):180–4. 26. Legesse L, Erko B, Hailu A. Current status of intestinal schistosomiasis and soil-transmitted helminthiasis among primary school children in Adwa town. Northern Ethiopia Ethiop J Health Dev. 2010;24(3):191–7. 27. Endris M, Lemma W, Belyhun Y, et al. Prevalenceof intestinal parasites and associated risk factors among students of Atse fasil general elementary school Azezo, Northwest Ethiopia. Ethiop J Heal Biomed Sci. 2010;3:25–33. 28. Handzel T, Karanja DMS, Addiss DG, et al. Geographic distribution of schistosomiasis and soil-transmitted helminthes in western Kenya: implications for anthelminthic mass treatment. Am J Trop Med Hyg. 2003;69(3):318–23. 29. Center for infectious disease control report. National prevalence survey on soil- transmitted helminths and schistosomiasis in school children. In: Rwanda; 2008. 30. Legesse M, Erko B. Prevalence of intestinal parasites among schoolchildren in a rural area close to the southeast of Lake Langano. Ethiopia Ethiop J Health Dev. 2004;18(2) 31. Merid Y, Hegazy M, Mekete G, Teklemariam S. Intestinal helminthic infection among children at Lake Awassa area, South Ethiopia. Ethiop J Health Dev. 2001;15:31–7:57–78. 32. Labiano-Abello N, Canese J, Velazquez ME, Hawdon JM, Wilson ML, Hotez PJ. Epidemiology of hookworm infection in Itagua, Paraguay: a cross sectional study. Mem Inst Oswaldo Cruz. 1999;94(5):583–6. 33. Ketema H, Biruksew A, Mekonnen Z. Prevalence of Necator americanus infection and risk factors among school-age children in Mirab Abaya district, South Ethiopia. Asian Pac J Trop Dis. 2015;5(5):363–8. 34. Samue F, Demsew A, Alem Y, Hailesilassie Y. Soil transmitted helminthiasis and associated risk factors among elementary school children in ambo town, western Ethiopia. BMC Public Health. 2017;17:791. 35. Erosie L, Merid Y, Ashiko A, Ayine M, Balihu A, Muzeyin S, Teklemariam S, Sorsa S. Prevalence of hookworm infection and hemoglobin status among rural elementary school children in southern Ethiopia. Ethiop J Health Dev. 2002;16(1):113–5. 36. Bala AY, Yakubu DP. A survey of hookworm infection among pupils of school age in Jos-north, plateau state, Nigeria. Nig J Basic Appl Sci. 2010; 18(2):237–42. 37. Odebunmi JF, Adefioye OA, Adeyeba OA. Hookworm infection among school children in Vom, plateau state. Nigeria Eur J Sci Res. 2007;2(1):39–42. 38. Jiraanankul V, Aphijirawat W, Mungthin M, Khositnithikul R, Rangsin R, Traub RJ, Piyaraj P, Naaglor T, Taamasri P, Leelayoova S. Incidence and risk factors of hookworm infection in a rural community of Central Thailand. Am J Trop Med Hyg. 2011;84(4):594–8. 39. Girum T. Prevalence of intestinal parasitic infections among patients with diarrhea at Wonago health center, southern Ethiopia: a retrospective study. JIID. 2015;3(1):1–6. 40. Asrat A, Tewodros D, Alemayehu W. Prevalence and risk factors of IPs among Delgi school children, northern Gonder, Ethiopia. J Parasitol Vector Biol. 2011;3(5):75–81. 41. Santos FLN, Souza AMGC, Soares NM. Hookworm and threadworm infections and their association with hemoglobin and eosinophil http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Tropical Diseases, Travel Medicine and Vaccines Springer Journals

Multivariate analysis of factors associated with Schistosoma mansoni and hookworm infection among primary school children in rural Bahir Dar, Northwest Ethiopia

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Abstract

Background: Soil-transmitted helminths and Schistosoma mansoni infections are the major causes of morbidity and mortality in Sub-Saharan countries. The highest burden of the disease resides in school-age children. Poor water sanitation and hygiene are believed to be the major contributing factors for the high prevalence. Therefore, the goal of this study was to determine the prevalence of intestinal parasite infections in rural Bahir Dar, Northwest Ethiopia. Methods: A cross-sectional study was conducted from April 2017–June 2017 among 409 randomly selected primary school children. A structured questionnaire was used to obtain socio-demographic information and determinant factors through interviewing the students. Stool examination was done by Ritchie’s concentration method. The data were entered and analyzed using SPSS version 22. Prevalence of helminthic infections was calculated using descriptive statistics. The association between helminthic infection and determinant factors was determined by Bavarian regression. The confounding effect was checked by multivariate regression at 95% confidence interval. Any association was significant when the p-value was < 0.05. Result: The overall prevalence of intestinal parasite infection was 47.2%.(193/409).. The prevalence of Hookworm species and Schistosoma mansoni was 31.1 and 8.0%, respectively. Co-infection of Hookworm species with Schistosoma mansoni was 5.1% (21/409). The highest prevalence of Schistosoma mansoni was recorded for boys (21%), older children (21.4%) and rural children (17.6%) (P <0.05). Schistosoma mansoni infection was also higher among children whose household drinking water was sourced from streams/rivers (P < 0.05). The multivariate analysis showed lower odds of Schistosoma mansoni infection for those with no history of bathing (AOR = 3.7, 95% CI: 1.1–12.2; P = 0.034), washing clothes/utensils (AOR = 3.4; 95% CI: 1.2–9.7; P = 0.022), swimming (AOR = 2.8, 95% CI: 1.2–6.9; P = 0.023), and irrigation (AOR = 2.8, 95% CI: 1.3–6.0; P = 0.01). Significantly, higher odds of Hookworm infection was recorded for older children (AOR = 2.3, 95% CI: 1. 08–4.89; P = 0.029), boys (AOR = 1.9, 95% CI: 1.12–3.24; P = 0.018), and rural children (AOR = 1.8, 95% CI: 1.04–3.0; P = 0.037). Regular shoe wearing (AOR = 0.29, 95% CI: 0.16–0.50; P = 0.00) is protective for hookworm infection. Higher odds of hookworm infection was also recorded for schoolchildren who had the habit of eating raw vegetables (AOR = 1.2 95% CI: 1.1–1.7 P = 0.011). (Continued on next page) * Correspondence: mgbeyney@gmail.com Department of Medical Laboratory Science, Bahir Dar University, Bahir Dar, Ethiopia Full list of author information is available at the end of the article © The Author(s). 2018 Open Access 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. Hailu et al. Tropical Diseases, Travel Medicine and Vaccines (2018) 4:4 Page 2 of 7 (Continued from previous page) Conclusion: Hookworm infection and schistosomiasis are prevalent in the school children in rural Bahir Dar in Northwest Ethiopia. Various activities and behaviors of the children were strongly associated with helminthic infection. Hence health education should be delivered regularly to minimize/avoid the risky behaviors and water-based activities. Deworming programs should also be implemented on a regular basis. Keywords: Helminth, Hookworm, Schistosoma, Sebatamit, Bahir Dar Background factors among school children was conducted in rural Soil-transmitted helminthiasis and schistosomiasis are the Bahir Dar, Amhara Regional National State, Northwest most common parasitic infections especially in developing Ethiopia from April–June 2017. countries [1]. Nearly, 1.5 billion people (24% of the world’s The altitude of the area is between 648 and 1300 m population) are infected with soil-transmitted helminths.- above sea level. The annual temperature and rainfall of More than 267 million preschool-age children and over 568 the study area are 18–22 °C and 1419 mm, respectively. million school-age children live in areas where these para- There is a small-scale irrigation on Andasa and Abay sites are intensively transmitted. [2]. Based on the World rivers in the study area. Health Organization (WHO) estimation, there are 700–900 In this particular study, Sebatamit primary school million hookworm and 200 million Schistosoma infections students age ranging from 7 to 14 years and willing to worldwide [3]. They are the major causes of morbidity and participate in the study were included. A total of 409 mortality in the Sub-Saharan countries [3, 4]. The disease students from grade 1–7 were recruited to the study. burden and the public health importance of these parasites Systematic random sampling technique was used to select are still concerns in developing countries like Ethiopia [5]. the classes in the school and the students in each class. All Poverty, poor living conditions, personal and environ- Sebatamit primary school students aged 7–14 years and mental hygiene, sanitation and water supply facilities are signed the assent form and parents signed written consent some of the contributing factors for the high prevalence of forms were included. soil-transmitted helminths and Schistosoma mansoni [6]. Moreover, the high prevalence of schistosomiasis is mainly Data collection associated with poor water management system during irri- A structured questionnaire was used to obtain gation, close contact habit to freshwater bodies, open socio-demographic information, present and past history defecation and wide distribution of the snail intermediate of the participants and environmental related factors by host [7]. interviewing the students. The questionnaire was filled Infections by soil-transmitted helminths and Schistosoma by nurses. The data collectors were regularly supervised species lead to malnutrition, iron deficiency anemia, within ten participants’ variation by the principal stunted growth and increased vulnerability to other infec- investigator. tions [8] and low educational achievement in school chil- Freshly passed stool specimens were collected using a dren [9].Current control programs for helminths infection clean plastic cup at the school. The stool cups were focused on reducing infection intensity and transmission labeled based on their section and role number. The potential, primarily to reduce morbidity and avoid mortality laboratory professionals took part in all processes of associated with the disease [10]. stool collection, transportation, and examination. The Despite a range of prevention and control efforts of hel- stool samples were processed for microscopic examin- minthicinfections, theprevalenceof soil-transmittedhel- ation by Ritchie’s concentration method. The stool minths and schistosome infections is still high in several examination was done in Bahir Dar University, College localities of Ethiopia. There is also a lack of information on of Medicine and Health Sciences, Department of Micro- the factors of S. mansoni and soil-transmitted helminths in- biology, Immunology, and Parasitology teaching fections in the study area. Therefore, the aim of this study laboratory. was to assess the magnitude of helminth infections and as- sociated risk factors so that to design effective prevention Ritchie’s concentration method and control measures. About 2.5 ml of formalin and 1 ml of ethyl acetate was in the sample collection tube. Then, 0.5 g of stool sample Materials and methods was put inside the sample collection tube and left to stand Study design, area and period for a minute. Both pieces of the device were screwed until A cross-sectional study, aimed at determining the preva- it is well closed and centrifuged at 1000 rpm for 3 min. lence of intestinal parasite infections and determinant The sample collection tube and filtration concentration Hailu et al. Tropical Diseases, Travel Medicine and Vaccines (2018) 4:4 Page 3 of 7 unit were discarded. The supernatant was removed from School children who frequently encounter contact with the conical tube and a small amount of sediment was put stream/river water during bathing (AOR = 3.7, 95% CI: on a glass slide for examination at 10× & 40× objectives. 1.1–12.2; P = 0.034), washing clothes (AOR = 3.4, 95% CI: 1.2–9.7; P = 0.022), swimming (AOR = 2.8, 95% Data quality assurance CI:1.2–6.9; P = 0.023) and irrigation (AOR = 2.8, 95% To ensure reliable data collection, training of nurses and CI:1.3–6.0; P = 0.01) had higher odds of S. mansoni in- laboratory technicians on data collection and explan- fection (Table 2). ation about the study were given before sample collec- The overall prevalence of hookworm infection was tion. The data collection, application of standard 41.1%. Significantly higher proportions of Hookworm in- procedures, and accuracy of test results were supervised fection were recorded for older children (AOR = 2.3, 95% by the principal investigator. Close follow up by the CI: 1.08–4.89; P = 0.029), boys (AOR = 1.9, 95% CI: 1.12– principal investigator within ten patients’ variation dur- 3.24; P = 0.018), rural children (AOR = 1.8, 95% CI: 1.04– ing data collection process was done. Specimens were 3.0; P = 0.037). Regular shoe wearing (AOR = 0.29, 95% CI: cross-checked by the principal investigator to increase 0.16–0.50; P = 0.00) was protective for hookworm infec- the accuracy of laboratory results. tion. Higher odds of hookworm infection was also re- To eliminate observer bias, the smears were examined corded among schoolchildren who did not have the habit independently with experienced laboratory technologists of regular latrine usage (55.8%), those practicing geophagy and 10% of the total slides will be randomly selected and (50.6%) and eat raw vegetables (48.2%) (Table 3). read by the principal investigator. The results of their observation were recorded for later comparison on separate Discussion sheets. A quality control was done by repeating all discord- Epidemiological study on the prevalence and distribution ant results. of helminthic species in different localities is a primary objective to identify high-risk communities and formu- Data analysis late appropriate intervention [11]. Assessing factors Data were entered and analyzed using SPSS version 22 stat- istical software. Overall magnitude, of parasitic infection, Table 1 Prevalence of intestinal parasites among primary was calculated using descriptive statistics. The strength of schoolchildren in rural Bahir Dar, Northwest Ethiopia, 2017 association between parasites infections and determinant Parasite species No infected Percent factors was calculated by binary logistic statistics. Those (n = 409) variables with P<0.2 in thebinarylogisticregressionwere Single infection taken to multiple regression analysis and the AOR was cal- Hookworm Spp 130 31.7 culated to control potential confounders. P-values less than Schistosoma mansoni 33 8.0 0.05 were taken statistical significant. Entamoeba histolytica 22 5.4 Ascaris lumbricoides 5 1.2 Results The overall prevalence of single, double and triple intestinal Strongyloides stercolaris 1 0.2 parasite infection was 47.2, 10.0 and 0.98%, respectively. Taenia spp 1 0.2 Hookworms (31.7%) were the predominant species identi- Giardia lamblia 1 0.2 fied followed by Schistosoma mansoni (8.0%), and Ent- Double infection amoeba histolytica (5.4%) (Table 1). The highest prevalence S. mansoni + Hookworm spp 17 4.2 of S.mansoni was recorded for boys (21%), older children Hookworm spp + E. histolytica 16 3.9 (21.4%) and rural children (17.6%) (P < 0.05). S.mansoni in- fection was also higher among children whose family drink- Hookworm + Giardia lamblia 3 0.7 ing water was sourced from streams (P < 0.05). The odds of E. histolytica + Giardia lamblia 2 0.5 infection was higher in this group (AOR = 0.34, 95% CI: A.lumbricoides + E. histolytica 1 0.2 0.162–0.707; P = 0.004) (Table 2). S. mansoni + E. histolytica 1 0.2 Domestic activities accounted for the majority of re- S. mansoni + A. lumbricoides 1 0.2 ported water contacts. The majority (69.4%) of subjects Triple infection interviewed reported that they bathed in the nearby stream. Similarly, about 65% of the respondents encoun- S. mansoni + Hookworm spp + E. histolytica 1 0.2 tered water contact for washing clothes. Besides, 57.7% S. mansoni + Hookworm spp + G. lamblia 2 0.5 of the school children frequently practiced swimming. S. mansoni + Hookworm spp + S. stercolaris 1 0.2 About half of respondents reported that the water for Negative 172 42.0 drinking and cooking was collected from streams. Hailu et al. Tropical Diseases, Travel Medicine and Vaccines (2018) 4:4 Page 4 of 7 Table 2 The prevalence and factors associated with Schistosoma mansoni among primary schoolchildren in rural Bahir Dar, Northwest Ethiopia, 2017 Variables Schistosma mansoni infection P-value AOR (95% CI) Positive n (%) Negative n (%) Total (n = 409) Age 7–10 28 (10.1) 250 (89.9) 278 (68.0) 0.002 2.1 (1.1–4.2) 11–14 28 (21.4) 103 (78.6) 131 (32.0) Sex Male 39 (21.0) 147 (79.0) 186 (45.5) 0.002 2.9 (1.5–5.7) Female 17 (7.6) 206 (92.4) 223 (54.5) Residence Urban 41 (17.6) 192 (82.4) 223 (57.0) 0.002 0.301 (0.14–0.64) Rural 15 (8.5) 161 (91.5) 176 (43.0) Water source Pipe 15 (7.5) 184 (92.5) 199 (48.7) 0.004 3.0 (1.41–6.2) Stream 41 (19.5) 169 (80.5) 210 (51.3) Bathing Yes 52 (18.3) 232 (81.7) 284 (69.4) 0.034 3.7 (1.1–12.2) No 4 (3.2) 121 (96.8) 125 (30.6) Washing clothes Yes 51 (19.2) 215 (80.8) 266 (65.0) 0.022 3.4 (1.2–9.7) No 5 (3.5) 138 (96.5) 143 (35.0) Swimming Yes 49 (20.8) 187 (79.2) 236 (57.7) 0.023 2.8 (1.2–6.9) No 7 (4.0) 166 (96.0) 173 (42.3) Irrigation Yes 45 (19.7) 183 (80.3) 228 (55.7) 0.010 2.8 (1.3–6.0) No 11 (6.1) 170 (93.9) 181 (44.3) Total Positive 56 (13.7) 353 (86.3) 409 (100) associated with the infection of parasites enables deter- For instance, males encounter frequent water contacts for mining priorities for public health measures to prevent swimming, bathing and agricultural activities (irrigation), parasitic infections [12]. while females reported more contacts for household activ- The overall prevalence of S. mansoni was 8.0% in our ities such as washing clothes and/or utensils and fetching study and it was lower than other studies conducted water for household consumption from rivers/streams. among school children in different parts of Ethiopia which Age was also the other independent variable found to reported prevalence greater than 30% [13–18]. This lower be significantly associated with S. mansoni infection in prevalence might be attributed to the sporadic deworming the multivariate analysis. Accordingly, the prevalence of programs conducted by Amhara Regional Health Bureau. S. mansoni was higher in the oldest age group (11–14) The multivariate analysis showed that sex was independ- years. This is consistent with reports of many re- ently associated with S. mansoni infection in our study. searchers in different localities of Ethiopia in which Consequently, the prevalence of S. mansoni was signifi- schistosomiasis was consistently higher in the second cantly higher in males than females. It was consistent with decade of life [22–25]. This might be justified by the fact findings from different parts of Ethiopia [19–22]. How- children in this age group encounter frequent/regular ever, higher prevalence of Schistosoma mansoni infection water contacts for leisure (swimming, bathing) and agri- in females than males was reported in different localities cultural activities (irrigation) and washing clothes. Simi- of Ethiopia such as Gorgora [19], Tseda [20], and Zarima larly, higher rate of infection was observed for rural [21]. These inconsistent reports might be attributed to dif- children than urban counterparts. This is in agreement ferences in water contact behavior of males and females. with other studies conducted in northwest Ethiopia and Hailu et al. Tropical Diseases, Travel Medicine and Vaccines (2018) 4:4 Page 5 of 7 Table 3 The prevalence and factors associated with Hookworm infection among primary schoolchildren in rural Bahir Dar, Northwest Ethiopia, 2017 Variables Hookworm infection P-value AOR (95% CI) Positive n (%) Negative n (%) Total (n = 409) Age (Yrs) 7–9 154 (44.5) 192 (55.5) 346 (84.6) .029 2.3 (1.09–4.89) 10–14 14 (22.2) 49 (77.8) 63 (15.4) Sex Male 78 (41.9) 108 (58.1) 186 (45.5) .018 1.9 (1.12–3.24) Female 90 (40.4) 133 (59.6) 223 (54.5) Residence Urban 74 (31.8) 159 (68.2) 223 (57.0) .037 1.8 (1.04–3.01) Rural 94 (53.4) 82 (46.6) 176 (43.0) Hand wash before meal Yes 128 (36.1) 227 (63.9) 355 (86.8) .010 2.9 (1.29–6.65) No 40 (74.1) 14 (25.9) 54 (13.2) Regular latrine use Yes 28 (17.7) 130 (82.3) 158 (28.6) .012 2.2 (1.19–4.18) No 140 (55.8) 111 (44.2) 251 (61.4) Frequency of shoe wearing Always 44 (10.8) 163 (67.6) 1 (0.2) .000 0.3 (0.16–0.50) Sometimes 124 (30.3) 78 (32.4) 408 (99.8) Geophagy Yes 44 (50.6) 43 (49.4) 87 (21.3) .052 1.6 (1.0–2.6) No 124 (38.5) 198 (61.5) 322 (78.7) Irrigation Yes 90 (39.5) 138 (60.5) 228 (55.7) .050 1.61 (1.00–2.60) No 78 (43.1) 103 (56.9) 181 (44.3) Eating raw vegetables Yes 137 (48.2) 147 (51.8) 284 (69.4) .011 1.2 (1.1–1.7) No 3 1(24.8) 94 (75.2) 125 (30.6) Total Positive 168 (41.1) 241 (58.9) North Ethiopia [24].This might be due to the higher ten- examination and the time of the study, and sample size dency of infested water exposure of rural children as used. they are frequently engaged in water-based activities Several cross-sectional studies have identified the risk such as irrigation as they inhabit in the proximity of factors of hookworm infection in the world. Hookworm Abay and Andasa rivers. infection is acquired via exposure to the soil where filari- The habit of frequent contact with cercariae-infested form larvae live in and penetrate human skin. In water such as swimming in the river, washing clothes and addition, Ancylostoma duodenale is also acquired by in- utensils using river water, and irrigation activities showed a gestion of food contaminated by the filariform larvae. statistically significant association with S. mansoni infection. Similarly, our study showed several factors are signifi- This is similar to the previous findings reported in Ethiopia cantly related to hookworm infection. Consequently, the [21, 22, 26, 27], and elsewhere [28, 29]. The prevalence of S. odds of hookworm infection was 1.9 times higher in mansoni was higher in school children who had a habit of boys than girls. It was in agreement with studies con- frequent swimming, washing clothes, bathing and engaging ducted in certain parts of Ethiopia [30, 39, 40] and Brazil in irrigation activities than those who did not. This might [41]. The higher prevalence of hookworm in boys in our be due to the presence of cercariae infected water bodies in study might be because boys usually help their parents the surrounding of study areas. in agricultural activities where shoe wearing is not con- The overall prevalence of hookworm in this study is venient. We also observed that most of the school chil- 41.1%. It was comparatively lower than previous reports dren and particularly boys wore non-protective shoes from different areas of Ethiopia [30, 31], and Paraguay (“ergendo” in Amharic). [32]. Higher than the present finding was reported in Multivariate analysis also revealed that children aged Gorgora [19], Mirab Abaya [33], western Ethiopia [34], 10–14 years were 2.3 times at higher odds of hookworm south Ethiopia [35], Plateau State Nigeria [36, 37], and infection compared to their younger counterparts. This Thailand [38]. The observed differences in the rate of might be attributed to their play behavior and lack/ig- infection could be due to variations in geography and norance of shoe wears. On the other hand regular shoe types of soil, socio-economic conditions, hygienic prac- wearing was found to protective for hookworm infection tices of the population, the methods employed for stool in our study (AOR = 0.3, 95% CI: 0.16–0.50; P = 0.00). It Hailu et al. Tropical Diseases, Travel Medicine and Vaccines (2018) 4:4 Page 6 of 7 was in agreement with other studies conducted in differ- letter was obtained from Amhara Regional Educational Bureau, and provided to the specific study area to conduct the research. ent parts of Ethiopia [21, 42]. Parents of children were informed of their children’s participation and gave This might be because the mode of transmission of informed written consent for their children to participate. Assents were also hookworm species is often through barefoot penetration collected from children. Participants positive for any of the soil-transmitted helminths were treated with a single dose of Mebendazole (500 mg) and by infective filariform larvae. Praziquantel (40 mg/kg, single dose) was given for children infected with Eating raw vegetables was also strongly associated with Schistosoma mansoni. hookworm infection. This might be explained by fact that Ancylostoma duodenale can be acquired by inges- Competing interests The authors declare that they have no competing interests. tion of filariform larvae in food, and this epidemiological feature can possibly occur in areas where A. duodenale predominates [43]. However, this study lacks evidence Publisher’sNote Springer Nature remains neutral with regard to jurisdictional claims in on the hookworm species that prevails in the study area. published maps and institutional affiliations. Rural children were at higher odds of hookworm infec- tion than their urban counterparts. This might be attrib- Author details Department of Medical Laboratory Science, Bahir Dar University, Bahir Dar, uted to a higher frequency of exposure to soil` due to Ethiopia. Department of Pharmacy, Bahir Dar University, Bahir Dar, Ethiopia. lack of shoes, and during agricultural activities, playing and coming to the school of the rural children. Received: 3 April 2018 Accepted: 23 May 2018 Conclusion References Hookworm infection and schistosomiasis are public 1. WHO. Prevention and control of intestinal parasitic infections, WHO technical report series 741. Geneva: WHO; 1987. health concerns in the study area. Various demographic 2. WHO. Soil-transmitted-helminth infections. http://www.who.int/en/news- characteristics, water based activities and recreational room/fact-sheets/detail/soil-transmitted-helminth-infections. water contact were strongly associated with S. mansoni 3. Crompton DW. How much helminthiasis is there in the world? J Parasitol. 1999;85:397–403. infection. Similarly, failure to wear shoe regularly and 4. Ross AG, Bartley PB, Sleigh AC, Olds GR, Li Y, Williams GM, McManus DP. other risky behaviors of children, such as geophagy and Schistosomiasis. N Engl J Med. 2002;346:1212–20. eating raw vegetables were also predictors of hookworm 5. Leykun J. Soil transmitted- helminthic infection and S. Mansoni in school children from Chilga district, Northwest Ethiopia. Ethiop J Health Sci. 2001; infection. Hence health education should be delivered 11:79–87. regularly to minimize/avoid the risky behaviors and 6. Ohaeri CC, Orji NB. Intestinal parasites among undergraduate students of water-based activities and deworming programs should Michael Okpara university of agriculture, Umudike Abia state, Nigeria. World Appl Sci J. 2013;25(8):1171–3. also be implemented on a regular basis. 7. WHO. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. Geneva: WHO technical report series; 2002. Abbreviations 8. Obiamuiwe BA. Nmorsi. Human gastro-intestinal parasites in Bendel state, AOR: Adjusted Odds Ratio; CI: Confidence interval; OR: Odds ratio; Nigeria. Nigerian J Parasitol. 1990;32:177–83. SPSS: Statistical Product and Service Solutions 9. Nokes C, Cooper ES, Robinson BA, Budy DAP. Geohelminth infection and academic assessment in Jamaican children. Trans R Soc Trop Med Hyg. Acknowledgments 1991;85:272–3. We are thankful to laboratory personnel and nurses who were actively 10. Albonico M, Allen H, Chitsulo L, Engels D, Gabrielli AF, et al. Controlling soil- involved in data collection. We also forward our gratitude for teachers at transmitted helminthiasis in pre-school-age children through preventive Sebatamit primary school. chemotherapy. PLoS Negl Trop Dis. 2008;2:e126. 11. Brooker S, Moulin A, Luoba D, Bundy M, Kremer D. Epidemiology of single Funding and multiple species of helminth infections among school children in Busia The research project was not funded by any organization. district. Kenya East Afr Med J. 2000;77:157–68. 12. Lima E, Rocha R, Leite M, Carneiro R, Colley D, Gazzinelli G, Katz N. A Availability of data and materials multivariate analysis of socio-demographic factors, water contact patterns To generate findings of this particular study, data was collected and and Schistosoma mansoni infection in an endemic area in Brazil. Rev Inst analyzed based on the stated methods and materials. All the data were Med Trop São Paulo. 1991;33(1):58–63. incorporated in the manuscript and no supplementary files accompanied the 13. Jemaneh L. Schistosoma mansoni and geo-helminthiaisis in school children in submission. The original data supporting this finding will be available at any Dembia plains. Northwestern Ethiopia Ethiop J Health Sci. 1998;12:237–44. time upon request. 14. Jemaneh L. Intestinal helminth infection in school children in Gondar town and surrounding areas, Northwest Ethiopia. Ethiop J Health Sci. 1999;22:209–20. Authors’ contributions 15. Jemaneh L. The epidemiology of Schistosoma mansoni and soil transmitted TH designed the study and wrote the manuscript; MA participated in the helminths in elementary school children from the South Gondar zone of design of the study, data collection and write-up of the manuscript; BA the Amhara national regional state, Ethiopia. Ethiop Med J. 2008:105–16. participated in data analysis and revision of the manuscript, WM analyzed 16. Roma B, Worku S. Magnitude of Schistosoma mansoni and intestinal data and wrote the manuscript, EY participated in data analysis and write-up, helminthic infections among school children in Wondo genet Zuria. AG and FB participated in manuscript write-up. All authors read and Southern Ethiopia Ethiop J Health Dev. 1997;11:125–9. approved the final manuscript. 17. Mammo B, Asseffa B, Loc T. (). Intestinal helminths in Akaki town, with special emphasis on epidemiology of Schistosoma mansoni. Ethiopian Med Ethics approval and consent to participate J. 1989;3:183–91. The proposal was ethically approved by the ethical review committee of 18. Erko B, Tedla S. Intestinal helminths infection in Zeghie, Ethiopia, with Bahir Dar University, College of Medicine and Health Science. Permission emphasis on Schistosoma mansoni. Ethiop J Health Dev. 1993;7:21–6. Hailu et al. Tropical Diseases, Travel Medicine and Vaccines (2018) 4:4 Page 7 of 7 19. Essa T, Birhane Y, Endris M, Moges A, Moges F. Current status of concentrations in residents of Salvador Bahia, Brazil. Rev Inst Med Trop São Schistosoma mansoni and associated risk factors among students in Gorgora Paulo. 2013;55(4):233–8. town, Northwest Ethiopia. International Scholarly Research Notices. 2013; 42. Abera B, Alem G, Yimer M, Herrador Z. Epidemiology of soil-transmitted 2013(Article ID 636103):7. helminths, Schistosoma mansoni, and haematocrit values among 20. Moges F, Belyhun Y, Tiruneh M, Kebede Y, Mulua A, Kassu A. Intestinal schoolchildren in Ethiopia. J Infect Dev Ctries. 2013;7(3):253–60. parasite infections in association with cutaneous fungal infection and 43. Gillespie SH, Pearson RD. Principles and practice of clinical parasitology. 2nd nutritional status among schoolchildren in Tseda, northwest Ethiopia. Ethiop ed. Toronto: Wiley; 2001. J Heal Biomed Sci. 2010;3(1):35–43. 21. Alemu A, Atnafu A, Addis Z, Shiferaw Y, Teklu T, Mathewos B, Birhan W, Gebretsadik S, Gelaw B. Soil transmitted helminthes and Schistosoma mansoni infections among school children in Zarima town, Northwest Ethiopia. BMC Infect Dis. 2011;11:189. 22. Awoke W, Bedimo M, Tarekegn M. Prevalence of schistosomiasis and associated risk factors among students attending at elementary schools in Amibera district, Ethiopia. Open J Prev Med. 2013;3(2):199–204. 23. Grum T. The prevalence of intestinal helminthic infections and associated risk factors among school children in Babile town, eastern Ethiopia. Ethiop J Health Dev. 2005;19:140–7. 24. Assefa A, Dejenie T, Tamass Z. Infection prevalence of Schistosoma mansoniand associated risk factors among schoolchildren in suburbs of Mekelle city, Tigray. North Ethiopia MEJS. 2013;5(1):174–88. 25. Mitiku H, Legesse M, Teklemariam Z, Erko B. Transmission of Schistosoma mansoni in TikurWuha area. Southern Ethiopia. Ethiop J Health Dev. 2010; 24(3):180–4. 26. Legesse L, Erko B, Hailu A. Current status of intestinal schistosomiasis and soil-transmitted helminthiasis among primary school children in Adwa town. Northern Ethiopia Ethiop J Health Dev. 2010;24(3):191–7. 27. Endris M, Lemma W, Belyhun Y, et al. Prevalenceof intestinal parasites and associated risk factors among students of Atse fasil general elementary school Azezo, Northwest Ethiopia. Ethiop J Heal Biomed Sci. 2010;3:25–33. 28. Handzel T, Karanja DMS, Addiss DG, et al. Geographic distribution of schistosomiasis and soil-transmitted helminthes in western Kenya: implications for anthelminthic mass treatment. Am J Trop Med Hyg. 2003;69(3):318–23. 29. Center for infectious disease control report. National prevalence survey on soil- transmitted helminths and schistosomiasis in school children. In: Rwanda; 2008. 30. Legesse M, Erko B. Prevalence of intestinal parasites among schoolchildren in a rural area close to the southeast of Lake Langano. Ethiopia Ethiop J Health Dev. 2004;18(2) 31. Merid Y, Hegazy M, Mekete G, Teklemariam S. Intestinal helminthic infection among children at Lake Awassa area, South Ethiopia. Ethiop J Health Dev. 2001;15:31–7:57–78. 32. Labiano-Abello N, Canese J, Velazquez ME, Hawdon JM, Wilson ML, Hotez PJ. Epidemiology of hookworm infection in Itagua, Paraguay: a cross sectional study. Mem Inst Oswaldo Cruz. 1999;94(5):583–6. 33. Ketema H, Biruksew A, Mekonnen Z. Prevalence of Necator americanus infection and risk factors among school-age children in Mirab Abaya district, South Ethiopia. Asian Pac J Trop Dis. 2015;5(5):363–8. 34. Samue F, Demsew A, Alem Y, Hailesilassie Y. Soil transmitted helminthiasis and associated risk factors among elementary school children in ambo town, western Ethiopia. BMC Public Health. 2017;17:791. 35. Erosie L, Merid Y, Ashiko A, Ayine M, Balihu A, Muzeyin S, Teklemariam S, Sorsa S. Prevalence of hookworm infection and hemoglobin status among rural elementary school children in southern Ethiopia. Ethiop J Health Dev. 2002;16(1):113–5. 36. Bala AY, Yakubu DP. A survey of hookworm infection among pupils of school age in Jos-north, plateau state, Nigeria. Nig J Basic Appl Sci. 2010; 18(2):237–42. 37. Odebunmi JF, Adefioye OA, Adeyeba OA. Hookworm infection among school children in Vom, plateau state. Nigeria Eur J Sci Res. 2007;2(1):39–42. 38. Jiraanankul V, Aphijirawat W, Mungthin M, Khositnithikul R, Rangsin R, Traub RJ, Piyaraj P, Naaglor T, Taamasri P, Leelayoova S. Incidence and risk factors of hookworm infection in a rural community of Central Thailand. Am J Trop Med Hyg. 2011;84(4):594–8. 39. Girum T. Prevalence of intestinal parasitic infections among patients with diarrhea at Wonago health center, southern Ethiopia: a retrospective study. JIID. 2015;3(1):1–6. 40. Asrat A, Tewodros D, Alemayehu W. Prevalence and risk factors of IPs among Delgi school children, northern Gonder, Ethiopia. J Parasitol Vector Biol. 2011;3(5):75–81. 41. Santos FLN, Souza AMGC, Soares NM. Hookworm and threadworm infections and their association with hemoglobin and eosinophil

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Tropical Diseases, Travel Medicine and VaccinesSpringer Journals

Published: Jun 1, 2018

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