Soil-transmitted helminths (STH) and Schistosoma mansoni infections are the major neglected tropical diseases that result in serious consequences on health, education and nutrition in children in developing countries. The Ethiopian Orthodox church students, who are called Yekolotemari in Amharic, live in areas with poor sanitation and hygiene. Moreover, they are not included in the national STH control programs. Thus, STH and S. mansoni infections prevalence is unknown.
A cross-sectional study was conducted on 384 students in June 2014 to determine STH and S. mansoni infections prevalence. Moreover, the knowledge of students about STH and S. mansoni was assessed. Data on knowledge and clinical symptoms were collected using structured questionnaires via face to face interview. Stool specimens were examined by formol-ether concentration method.
The overall prevalence of intestinal helminths infections was 85.9% (95% confidence interval (CI): 82.1–89%). STHs infections prevalence was 65.6% (95% CI: 60.7–70.2%). The prevalence of hookworm, Ascaris lumbricoides and Trichuris trichiura were 31.8% (95% CI: 27.3–36.6%), 29.4% (25–31%) and 3.1% (1.8–5.4%), respectively. On the other hand, S. mansoni prevalence was 14.3% (95% CI: 11.1–18.1%). Majority of students infected with S. mansoni had bloody stool with crud odds-ratio of 2.9 (95% CI: 1.5–5.5). Knowledge assessment showed that 50 (13%) and 18 (4.9%) of the respondents knew about transmission of STH and S. mansoni, respectively.
The prevalence of STH and S. mansoni infections were high thus de-worming program should include the students of Ethiopian Orthodox churches. Furthermore, provision and use of sanitary facilities, health education for students to create awareness of parasitic infections and improved personal hygiene should be in place.
Citation: Afework Bitew A, Abera B, Seyoum W, Endale B, Kiber T, Goshu G, et al. (2016) Soil-Transmitted Helminths and Schistosoma mansoni Infections in Ethiopian Orthodox Church Students around Lake Tana, Northwest Ethiopia. PLoS ONE 11(5): e0155915. https://doi.org/10.1371/journal.pone.0155915
Editor: Raffi V. Aroian, UMASS Medical School, UNITED STATES
Received: September 23, 2015; Accepted: May 8, 2016; Published: May 20, 2016
Copyright: © 2016 Afework Bitew et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the paper.
Funding: These authors have no support or funding to report.
Competing interests: The authors have declared that no competing interests exist.
Soil-transmitted helminths (hookworm, Ascaris lumbricoides and Trichuris trichiura) and S. mansoni infections are the major neglected tropical diseases in sub-Saharan African including Ethiopia. These parasites are more prevalent in populations with low income, poor sanitation and overcrowded conditions. Moreover, limited access to clean water, bare footing, and irrigation practice are risk factors for STH and S. mansoni infections. According to World Health Organization estimates, more than 1.5 billion people are infected with soil-transmitted helminths worldwide .
Among soil-transmitted helminths, A. lumbricoides, T. trichiura and hookworm have particular public health importance because they have negative impact on the health, education, nutrition and economic development [2, 3] of the population. Therefore, STH and S. mansoni have been targeted for control and eradication . The mapping of STH and S. mansoni are determined by climate, geography, poverty, environmental contamination and water bodies [2, 5].
Among sub-Saharan Africa, Ethiopia bears the 2nd, 3rd and 4th high burden of A. lumbricoides, hookworm and T. trichiura, respectively . In Ethiopia, the prevalence and distribution of STH and S. mansoni varies because of differences in climate and humidity. Studies from various school aged children showed prevalence of 9.7 to 28.8% for hookworm, 9.9 to 12.7% for A. lumbricoides and 2.9–7.3% for S. mansoni [7, 8]. Compared to other sub-Saharan African countries, Ethiopia is the second country with high number of children in need of chemotherapy for de-worming helminths [9, 10]. Despite high burden of helminths, control of STH and S. mansoni in Ethiopia is at its infancy .
According to WHO report, schistosomiasis affects 240 million people worldwide. The majority of schistosomiasis cases are found in sub-Saharan Africa and more than 200 000 deaths occur per year . S. mansoni is the most prevalent species in Ethiopia which causes intestinal schitosomiasis. In Ethiopia, 5.01 million people are estimated to be infected and 37.5 million are at risk for S. mansoni . S. mansoni occurs mainly along streams, irrigation schemes and lakes.
The present study was conducted around Lake Tana area, which is situated in central highlands in northwestern Ethiopia. Its location and humid climate create conducive environment for transmission of STH and S. mansoni. Ethiopian Orthodox students are grouped in low socioeconomic classes and majority of students get local foods by begging different households in the name of St. Mery. The habit of bare foot, open defecation, swimming and bathing in river and drinking unsafe water are risk factors for acquiring STH and S. mansoni. Furthermore, Ethiopian Orthodox church students are not targeted so far in the national de-worming program. Therefore, students from the traditional schools may contribute for ongoing transmission of STH and S. mansoni in the community.
Although, data on STH and S. mansoni have been available in several Ethiopian school aged children little is known for students in the Ethiopian Orthodox churches. Therefore, this study was conducted to determine the prevalence of STH and S. mansoni infections in Yekolotemari around Lake Tana in northwestern Ethiopia. Moreover, the study assessed the knowledge of students about STH and S. mansoni transmission.
Materials and Methods
Study area and population
This study was conducted around Lake Tana located north of Bahir Dar City. Bahir Dar is located 565km to the northwest of Addis Ababa. The Lake Tana is famous for the ancient monasteries and churches. It has 20 monasteries and churches.
At the time of the study, there were 2500 male students (Yekolotemari). Ethiopian Orthodox church students (Yekolotemari) include any males who are willing to study all the educational structures. Studying the Ethiopian Orthodox church is a pre-requisite to transmit the role of the church and to become trained scholar for the church. They are grouped in low socio economic status; their livelihood is based on begging food items in the name of St. Mery by going from house to house in the community.
Yekolotemari are traditional students who are from rural family of Ethiopia willing to study all the educational structures in Ethiopian Orthodox churches. They live in church compounds till they compete their education. Learning the Ethiopian Orthodox church is a pre-requisite to transmit the role of the churches and to become trained scholar.
Study design and sample size
A cross-sectional study was conducted in June 2014. The sample size was determined at 95% level of confidence, with 5% margin of error and 50% prevalence of STH infection . Hence, using single population proportion formula the sample size was estimated to be 384. From the twenty schools, eight churches were selected using simple random sampling technique. The number of students to be surveyed was calculated by dividing the sample size by the number of schools to be included in the study. Accordingly, from Azwa Mariam with n = 24, Ura Kidanimihiret n = 10, Selchen Mikaeal n = 7, Kibran Gebrael n = 19, Bata n = 83, Kiduse Georgis n = 41, Kiduse Mikael n = 103and Abuye with n = 97. The study participants were selected using simple random sampling method.
Students’ knowledge about the transmission of intestinal parasites was collected via face to face interview using 6-question items. Clinical data were collected by experienced health officers. For stool examination, 3 grams of stool specimen was collected from each student using clean, dry, wide necked and leak proof plastic container. Upon delivery of the specimens, the containers were labeled and preserved with 10 ml of 10% normal saline solution. Immediately within 2 hours of collection, stool samples were transported to ALKAN University College Laboratory. The stool specimens were examined for intestinal parasites using formol-ether concentration technique by trained laboratory technologists.
Data were analyzed using the Statistical Package for Social Sciences version 20 software (IBM Corp. Released 2011. IBM SPSS Statistics for Windows, Armonk, NY: IBM Corp). Chi-square test and crude odds ratio were computed to test the association between categorical variables and parasitic infections. P-value <0.05 with 95% confidence interval (CI) was considered as statistically significant.
Participants’ knowledge on STH and S. mansoni transmission was surveyed by 6 item-questions. The response alternatives for knowledge items were dichotomous. For knowledge assessment, each correct response was given a score of 1 while a wrong or doubtful response was scored as 0. Mean knowledge scores < 0.5 were considered as below the expected level of knowledge while average scores ≥0.5 deemed knowledgeable
Ethical clearance was obtained from research and ethics review committee of the ALKAN University College and Institutional Research Ethics Review Board of the Amhara Regional State Health Bureau, Research and Technology Transfer Core Process. Written consent was obtained from each participant. In this study, 257 participants whose age was below 18 years gave assent themselves in consultation to their guardians because children (minors) would not face any psychological and physical harmful procedures. Thus, the Institutional Research Ethics Review Board approved the consent form for children who participated in this research.
Hygiene characteristics and knowledge of students
The mean age of the study participants was 20.8 years. More than 42% of students used to live in churches for two years and above. In this survey, 99% of the respondents did not get toilet facility thus used open field defecation. All of them take bath and clothes in Lake Tana. Sources of drinking water and hand washing practices are depicted in Table 1. In this survey, 50 (13.0%) of the respondents were knowledgeable on mode of transmission of STH. In contrast, only 18 (4.7%) had information about transmission of S. mansoni.
Prevalence of STH and S. mansoni infections
Overall, 330 (85.9%) of students at the selected churches were infected with intestinal helminths whereas the prevalence of STH infection was 65.6% (95% CI: 60.7–70.2%). Prevalence of S. mansoni infection was 14.3% (95% CI: 11.2–18.2%). Hookworm with 31.5% was the most prevalent STHs. Detail prevalence of each STH is shown in Table 2. Two or more intestinal helminths were found in 179 (46.6%) of the students. Thus, infection with single helminths was 150 (39%) whereas double and multiple infections (three and above) were 125 (32.6%) and 54 (14.0%), respectively.
Table 3 depicts the associations between clinical symptoms with STH and S. mansoni. Statistically significant association was observed between hookworm infection and abdominal pain (P = 0.021). Moreover, there was significant association between S. mansoni infection and appearance of bloody stool (P = 0.001).
This study revealed the first prevalence of STH and S. mansoni infections in Ethiopian Orthodox church students. As expected, the prevalence of intestinal helminths was very high. The prevalence of STH and S. mansoni infections in this study were significantly higher than the prevalence of helminths reported from school children in the same geographical areas in northwestern Ethiopia [6, 8, 15]. The prevalence of STH in Yekolotemari was above 50%. Therefore, according to WHO guideline, bi-annual chemotherapy is required to reduce STHS’ egg burden in the community .
High prevalence of STHs found in this study might be attributable to open field defecation, poor hand washing practice and low level of awareness about STHs transmission. Furthermore, students in the surveyed Orthodox churches are not included in school-deworming program. Therefore, unless intervention is done, students in Ethiopian Orthodox churches may remain sources for helminths transmission thereby impacting STH control. Hence interventions including mass de-worming and improving sanitation and personal hygiene should be in place.
The prevalence of hookworm infections in this study was higher than the national prevalence of hookworm (16%) . It was also higher than prevalence of hookworm in school children in Gondar Ethiopia [8, 17]. Among STHs, the prevalence of hookworm infection was higher in young adults than children. Likewise, in Brazil high prevalence of hookworm was noted in adults . In contrast, other STHs were higher in young children than adults.
The prevalence of A. lumbricoides in this study was higher than other studies in different part of the country in modern school children in Ethiopia [7, 8, 19, 20]. The prevalence of T. trichiura in this study was higher than school children in same study area . However, prevalence of T. trichiura was comparable with other studies in south Gondar, Ethiopia [8, 20]. The prevalence of S. mansoni in this study was higher than school based reports [7, 8]. This showed that students in Ethiopian Orthodox churches were the highest risk groups in the community and serve as sources of S. mansoni transmission.
Statistical significant association was observed between clinical symptoms in hookworm and S. mansoni infected students. Significant proportions of hookworm infected students had abdominal cramp than non-hookworm infected students with COR 1.4. Majority of students infected with S. mansoni had bloody stool with COR 2.9. Similarly, hookworm and S. mansoni infected children had lower hematocrit values . However, other studies did not show any significant association between the helminths and clinical symptoms [14, 16]. Clinical manifestations in children with STH rely on the load of worms in the intestine. The main limitation of this study was that the intensity of parasitic load was not measured. The exact risk factors for acquisition of STH and S. mansoni in Yekolotemaria were not determined due to the cross-sectional study design effect.
This study has shown high prevalence of STHs and S. mansoni infection in Ethiopian Orthodox church students (yekolotemaria) around Lake Tana in northwestern Ethiopia. All students used open field defecation near Tana Lake. Furthermore, majority of students had knowledge gap on STH and S. mansoni transmission. Thus, students in Ethiopian Orthodox churches are deemed pockets for ongoing transmission of STH and S. mansoni in northwest Ethiopia.
We recommend that de-worming programs should include students in the Ethiopian Orthodox churches.
The de-worming program should also be supplemented with other measures such as provision of sanitary facilities, health education for students to create awareness of parasitic infections and improved personal hygiene.
We acknowledge ALKAN University College and Bahir Dar University for facilitating and providing laboratory facility. We would like to extend our appreciation to the data collectors and all the responds and teachers.
Conceived and designed the experiments: AAB. Performed the experiments: WS BE TK GG AA. Analyzed the data: BA. Contributed reagents/materials/analysis tools: WS BE TK GG AA. Wrote the paper: BA. Critically revised the manuscript: BA AAB.
- 1. World Health Organization. Fact sheet on Soil-transmitted helminths. Geneva, Switzerland. WHO. Available: http://www.who.int/mediacenter/factsheets/fs366/en/. Accessed 20 July 2015.
- 2. Booth M. The role of residential location in apparent helminth and malaria infection. Trends Parasitol 2006; 22:359–62. pmid:16797235
- 3. Bundy DA, Walson JL, Watkins KL. Worms, wisdom, and wealth: why deworming can make economic sense. Trends Parasitol 2013; 29: 142–48. pmid:23332661
- 4. World Health Organization. Accelerating work to overcome the global impact of neglected tropical 415 diseases-A roadmap for implementation. Geneva, Switzerland: WHO, Available: http://www.who.int/hq/2012/WHO_HTM_NTD_2012.1_eng.pdf. Accessed 20 June 2015.
- 5. Brooker S, Michael E. The potential of geographical information systems and remote sensing in epidemiology and control of human helminth infections. Advances in parasitology 2000; 47:245–288. pmid:10997209
- 6. 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. pmid:19707588
- 7. Abera B, Alem G, Yimer M, Herrador Z. Epidemiology of soil-transmitted helminths, Schistosoma mansoni, and haematocrit values among schoolchildren in Ethiopia. J Infect Dev Ctries 2013; 7(3):253–260. pmid:23493004
- 8. King JD, Endeshaw T, Escher E, Alemtaye G, Melaku S, Gelaye , et al. Intestinal Parasite Prevalence in an Area of Ethiopia after Implementing the SAFE Strategy, Enhanced Outreach Services, and Health Extension Program. PLOS Negl Trop Dis 2013;7(6): e2223. pmid:23755308
- 9. World Health Organization. Eliminating soil-transmitted helminthiases as a public health problem in children progress report 2001–2010 and strategic plan 2011–2020. Geneva, Switzerland,WHO. Available: http://www.who.int/publications/2012/9789241503129_eng.pdf. Accessed 15 June 2015.
- 10. Hotez PJ, Herricks JR. Helminth Elimination in the Pursuit of Sustainable 453 Development Goals: A "Worm Index" for Human Development. PLOS Negl Trop Dis 2015; 3: 454 e362.
- 11. Deribe K, Meribo K, Gebre T, Hailu A, Ali A, Assefa AD, et al. The burden of neglected tropical 456 diseases in Ethiopia, and opportunities for integrated control and elimination. Parasites & Vectors 2012; 5: 240.
- 12. World Health Organization. Schistosomiasis a major public health problem. Geneva, Switzerland. WHO: Available: http://www.who.int/schistosomiasis/en/ 2015. Accessed 21 July 2005.
- 13. Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis 2006; 6 (7):411–425. pmid:16790382
- 14. Asrat A, Tewodros D, Alemayehu W. Prevalence and risk factors of intestinal parasites among Delgi school children, North Gondar, Ethiopia. J. Parasitol. Vector Biol 2011; 3 (5):75–81.
- 15. Alelign T, Degarege A, Erko B. Soil-Transmitted Helminth Infections and Associated Risk Factors among Schoolchildren in Durbete Town,Northwestern Ethiopia. Journal of Parasitology Research. 2015; Vol 2015 :
- 16. Tadesse Z, Hailemariam A, Kolaczinski JH. Potential for integrated control of neglected tropical diseases in Ethiopia. Trans R Soc Trop Med Hyg2008; 102: 213–214. pmid:17950392
- 17. Mathewos B, Alemu A, Woldeyohannes D, Alemu A, Addis Z, Tiruneh M, et al. Current status of soil transmitted helminths and Schistosoma mansoni infection among children in two primary schools in North Gondar, Northwest Ethiopia: a cross sectional study. BMC Research Notes 2014; 7: 88. pmid:24512613
- 18. Fleming FM, Brooker S, Geiger SM, Caldas IR, Correa-Oliveira R, Hotez PJ, et al. Synergistic associations between hookworm and other helminth species in a rural community in Brazil. Trop Med Int Health 2006; 11: 56–64. pmid:16398756
- 19. Yesuf A, Abebe M. Prevalence of intestinal parasites in Metema district hospital, northwest Ethiopia. Ethiop. J. Health biomed Sci 2010; 2 (2)
- 20. Alemu A, Atnafu A, Addis Z, Shiferaw Y, Teklu T, Mathewos B, et al. Soil transmitted helminths and schistosoma mansoni infections among school children in zarima town, northwest Ethiopia. BMC Infectious Diseases 2011; 11:189. pmid:21740589