Detection and Transmission Dynamics of Intestinal Schistosomiasis among Primary School Pupils in Tharaka Nithi County in the Mt. Kenya Highlands

Anthony Muthee; Rael Musili; Joseph Muriithi; Nancy Kinyatta; Martin Mutuku; Luna Kamau

doi:10.51867/ajernet.5.4.45

Authors

Anthony Muthee Centre for Biotechnology Research and Development, Kenya Medical Research Institute, Kenya
Rael Musili Centre for Biotechnology Research and Development, Kenya Medical Research Institute, Kenya https://orcid.org/0000-0002-1889-2102
Joseph Muriithi Centre for Biotechnology Research and Development, Kenya Medical Research Institute, Kenya
Nancy Kinyatta Centre for Biotechnology Research and Development, Kenya Medical Research Institute, Kenya https://orcid.org/0000-0002-8927-4790
Martin Mutuku Centre for Biotechnology Research and Development, Kenya Medical Research Institute, Kenya
Luna Kamau Centre for Biotechnology Research and Development, Kenya Medical Research Institute, Kenya https://orcid.org/0000-0002-2186-0283

Keywords:

Biomphalaria Spp, Detection, Intestinal Schistosomiasis, Transmission Dynamics

Abstract

Emerging infections cause considerable public health problems to humanity worldwide. The presence of Biomphalaria spp vector snails, the compatibility of the snails with schistosomes, and the prevalence of intestinal schistosomiasis infection in school-going children were determined. The study sought to determine the presence and transmission dynamics of schistosomiasis in Tharaka Nithi, an emerging schistosomiasis transmission focus in the Mt. Kenya highlands. The Epidemiological Triangle Model (ETM), which sheds light on the transmission of infectious diseases, served as the foundation for this study. A cross-sectional study design was used. The study targeted 178 students in grades 1–8 from the two primary schools in Tharaka Nithi located along the catchment area of Mukothima and Thanantu rivers. The number of study participants was determined using the Cochran formula. Study participants were selected randomly from the class register while ensuring equal numbers of boys and girls to avoid bias in results. The stool samples collected from the participants were processed using Kato Katz's quantitative screening technique for helminths and formal ether concentration technique for intestinal protozoa. Biomphalaria snails were collected and identified based on morphology. Snails were also bred and experimentally infected with a laboratory strain of Schistosoma mansoni and passed to the F5 generation to check the compatibility with the Schistosoma mansoni parasite. The overall mean snail parasite infection rate was 23.51% with a positivity of 19.38% in Mukothima River compared to 27.64% in Thanantu River. Although none of the field sampled snails were found infected with S. mansoni, pupils tested were found to be infected with the parasite with a positivity rate of 15.5%. Other parasites detected included Ascaris lumbricoides with a prevalence rate of 9.23% and Entamoeba histolytica with a prevalence of 8.48%. Results from the snail susceptibility experiment showed that the snails supported the development of S. mansoni to full patency, indicating the potential to support the schistosomiasis transmission cycle. Despite not finding any field-sampled snails infected with S. mansoni, the demonstrated compatibility of the snails with the parasite and the finding of infection in school children suggests that transmission is a possibility. Schistosomiasis prevention strategies including deworming programs, school and community environment sanitation, and latrines provision are highly recommended to prevent further spread of the disease.

Dimensions

REFERENCES

Ansha, M. G., Kuti, K. A., & Girma, E. (2020). Prevalence of Intestinal Schistosomiasis and Associated Factors among School Children in Wondo District, Ethiopia. Journal of Tropical Medicine, 2(6), 1-8. https://doi.org/10.1155/2020/9813743 DOI: https://doi.org/10.1155/2020/9813743

Bethony, J., Brooker, S., Albonico, M., Geiger, S. M., Loukas, A., Diemert, D., & Hotez, P. J. (2006). Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. The Lancet, 367(9521), 1521-1532. https://doi.org/10.1016/S0140-6736(06)68653-4 DOI: https://doi.org/10.1016/S0140-6736(06)68653-4

Bhutta, Z. A., Das, J. K., Bahl, R., Lawn, J. E., Salam, R. A., Paul, V. K., Sankar, M. J., Blencowe, H., Rizvi, A., Chou, V. B., & Walker, N. (2014). Can available interventions end preventable deaths in mothers, newborn babies, and stillbirths, and at what cost? In The Lancet, 384 (9940), 68-69.

https://doi.org/10.1016/S0140-6736(14)60792-3 DOI: https://doi.org/10.1016/S0140-6736(14)60792-3

Calasans, T. A. S., Souza, G. T. R., Melo, C. M., Madi, R. R., & Jeraldo, V. de L. S. (2018). Socioenvironmental factors associated with Schistosoma mansoni infection and intermediate hosts in an urban area of northeastern Brazil. PLOS ONE, 13(5), 19 - 23. https://doi.org/10.1371/journal.pone.0195519 DOI: https://doi.org/10.1371/journal.pone.0195519

Chala, B., & Torben, W. (2018). An Epidemiological Trend of Urogenital Schistosomiasis in Ethiopia. Frontiers in Public Health, 6(7), 78-79. https://doi.org/10.3389/fpubh.2018.00060 DOI: https://doi.org/10.3389/fpubh.2018.00060

Chelkeba, L., Mekonnen, Z., Emana, D., Jimma, W., & Melaku, T. (2022). Prevalence of soil-transmitted helminths infections among preschool and school-age children in Ethiopia: a systematic review and meta-analysis. Global Health Research and Policy, 7(1), 9-15.

https://doi.org/10.1186/s41256-022-00239-1 DOI: https://doi.org/10.1186/s41256-022-00239-1

Colley, D. G., Bustinduy, A. L., Secor, W. E., & King, C. H. (2014). Human schistosomiasis. The Lancet, 383(9936), 2253-2264.

https://doi.org/10.1016/S0140-6736(13)61949-2 DOI: https://doi.org/10.1016/S0140-6736(13)61949-2

De Leo, G. A., Stensgaard, A.-S., Sokolow, S. H., N'Goran, E. K., Chamberlin, A. J., Yang, G.-J., & Utzinger, J. (2020). Schistosomiasis and climate change. BMJ, m4324. https://doi.org/10.1136/bmj.m4324 DOI: https://doi.org/10.1136/bmj.m4324

Deol, A. K., Fleming, F. M., Calvo-Urbano, B., Walker, M., Bucumi, V., Gnandou, I., Tukahebwa, E. M., Jemu, S., Mwingira, U. J., Alkohlani, A., Traoré, M., Ruberanziza, E., Touré, S., Basáñez, M.-G., French, M. D., & Webster, J. P. (2019). Schistosomiasis - Assessing Progress toward the 2020 and 2025 Global Goals. New England Journal of Medicine, 381(26), 2519-2528. https://doi.org/10.1056/NEJMoa1812165 DOI: https://doi.org/10.1056/NEJMoa1812165

El Naga, I. F. A., Eissa, M. M., Mossallam, S. F., & El-Halim, S. I. A. (2010). Inheritance of Schistosoma mansoni infection incompatibility in Biomphalaria alexandrina snails. Memorias Do Instituto Oswaldo Cruz, 105(2), 149-154. https://doi.org/10.1590/s0074-02762010000200007 DOI: https://doi.org/10.1590/S0074-02762010000200007

Goodfriend, G. A. (1986). Variation in Land-snail Shell form and Size and its Causes: a Review. Systematic Biology, 35(2), 204-223.

https://doi.org/10.1093/sysbio/35.2.204 DOI: https://doi.org/10.1093/sysbio/35.2.204

Gryseels, B., Polman, K., Clerinx, J., & Kestens, L. (2006). Human schistosomiasis. Lancet (London, England), 368(9541), 1106-1118.

https://doi.org/10.1016/S0140-6736(06)69440-3 DOI: https://doi.org/10.1016/S0140-6736(06)69440-3

Joof, E., Sanyang, A. M., Camara, Y., Sey, A. P., Baldeh, I., Jah, S. L., Ceesay, S. J., Sambou, S. M., Sanyang, S., Wade, C. M., & Sanneh, B. (2021). Prevalence and risk factors of schistosomiasis among primary school children in four selected regions of The Gambia. PLOS Neglected Tropical Diseases, 15(5), 93-100. https://doi.org/10.1371/journal.pntd.0009380 DOI: https://doi.org/10.1371/journal.pntd.0009380

Jourdan, P. M., Lamberton, P. H. L., Fenwick, A., & Addiss, D. G. (2018). Soil-transmitted helminth infections. The Lancet, 391(10117), 252-265. https://doi.org/10.1016/S0140-6736(17)31930-X DOI: https://doi.org/10.1016/S0140-6736(17)31930-X

Kappagoda, S., & Ioannidis, J. P. (2014). Prevention and control of neglected tropical diseases: overview of randomized trials, systematic reviews and meta-analyses. Bulletin of the World Health Organization, 92(5), 356-366C. https://doi.org/10.2471/BLT.13.129601 DOI: https://doi.org/10.2471/BLT.13.129601

Kibret, K. S., Marohn, C., & Cadisch, G. (2016). Assessment of land use and land cover change in South Central Ethiopia during four decades based on integrated analysis of multi-temporal images and geospatial vector data. Remote Sensing Applications: Society and Environment, 3(2016), 1-19. https://doi.org/10.1016/j.rsase.2015.11.005 DOI: https://doi.org/10.1016/j.rsase.2015.11.005

Kihara, J., Mwandawiro, C., Waweru, B., Gitonga, C. W., & Brooker, S. (2011). Preparing for national school-based deworming in Kenya: The validation and large-scale distribution of school questionnaires with urinary schistosomiasis. Tropical Medicine and International Health, 16(10), 68-70. https://doi.org/10.1111/j.1365-3156.2011.02829.x DOI: https://doi.org/10.1111/j.1365-3156.2011.02829.x

Kisavi, P. M. (2015). Prevalence and factors associated with soil-transmitted helminth infection among primary school children in Kikumuni sub-location, Machakos County, Kenya [Doctoral dissertation, Kenyatta University]. Kenyatta University Institutional Repository. http://ir-library.ku.ac.ke/handle/123456789/13342

Klohe, K., Koudou, B. G., Fenwick, A., Fleming, F., Garba, A., Gouvras, A., Harding-Esch, E. M., Knopp, S., Molyneux, D., D'Souza, S., Utzinger, J., Vounatsou, P., Waltz, J., Zhang, Y., & Rollinson, D. (2021). A systematic literature review of schistosomiasis in urban and peri-urban settings. PLOS Neglected Tropical Diseases, 15(2) 72-76, e0008995. https://doi.org/10.1371/journal.pntd.0008995 DOI: https://doi.org/10.1371/journal.pntd.0008995

KNBS. (2019). 2019 Kenya Population and Housing Census: Volume IV. Kenya National Bureau of Statistics, Nairobi.

Lee, S. M. L., Schelcher, C., Demmel, M., Hauner, M., & Thasler, W. E. (2013). Isolation of Human Hepatocytes by a Two-step Collagenase Perfusion Procedure. Journal of Visualized Experiments, 79(3), 34-39. https://doi.org/10.3791/50615 DOI: https://doi.org/10.3791/50615

Lo, N. C., Bezerra, F. S. M., Colley, D. G., Fleming, F. M., Homeida, M., Kabatereine, N., Kabole, F. M., King, C. H., Mafe, M. A., Midzi, N., Mutapi, F., Mwanga, J. R., Ramzy, R. M. R., Satrija, F., Stothard, J. R., Traoré, M. S., Webster, J. P., Utzinger, J., Zhou, X.-N., … Garba, A. (2022). Review of 2022 WHO guidelines on the control and elimination of schistosomiasis. The Lancet Infectious Diseases, 22(11), e327-e335.

https://doi.org/10.1016/S1473-3099(22)00221-3 DOI: https://doi.org/10.1016/S1473-3099(22)00221-3

Masaku, J., Mwende, F., Odhiambo, G., Musuva, R., Matey, E., Kihara, J. H., Thuita, I. G., & Njomo, D. W. (2017). Knowledge, practices and perceptions of geo-helminthes infection among parents of pre-school age children of coastal region, Kenya. PLOS Neglected Tropical Diseases, 11(3), 17-26. e0005514. https://doi.org/10.1371/journal.pntd.0005514 DOI: https://doi.org/10.1371/journal.pntd.0005514

McCreesh, N., Nikulin, G., & Booth, M. (2015). Predicting the effects of climate change on Schistosoma mansoni transmission in eastern Africa. Parasites & Vectors, 8(1), 54-67. https://doi.org/10.1186/s13071-014-0617-0 DOI: https://doi.org/10.1186/s13071-014-0617-0

Mezui-Mbeng, P. (2015). A Note on Cochran Test for Homogeneity in Two Ways ANOVA and Meta-Analysis. Open Journal of Statistics, 05(07), 787-796. https://doi.org/10.4236/ojs.2015.57078 DOI: https://doi.org/10.4236/ojs.2015.57078

Mitta, G., Gourbal, B., Grunau, C., Knight, M., Bridger, J. M., & Théron, A. (2017). The Compatibility between Biomphalaria glabrata Snails and Schistosoma mansoni (pp. 111-145). https://doi.org/10.1016/bs.apar.2016.08.006 DOI: https://doi.org/10.1016/bs.apar.2016.08.006

Mohammed, M. A., Moles, R. J., & Chen, T. F. (2016). Medication-related burden and patients' lived experience with medicine: a systematic review and metasynthesis of qualitative studies. BMJ Open, 6(2), e010035. https://doi.org/10.1136/bmjopen-2015-010035 DOI: https://doi.org/10.1136/bmjopen-2015-010035

Mutuku, M. W., Dweni, C. K., Mwangi, M., Kinuthia, J. M., Mwangi, I. N., Maina, G. M., Agola, L. E., Zhang, S.-M., Maranga, R., Loker, E. S., & Mkoji, G. M. (2014). Field-derived Schistosoma mansoni and Biomphalaria pfeifferi in Kenya: a compatible association characterized by lack of strong local adaptation, and presence of some snails able to persistently produce cercariae for over a year. Parasites & Vectors, 7(1), 53-63. https://doi.org/10.1186/PREACCEPT-5609029931283243 DOI: https://doi.org/10.1186/s13071-014-0533-3

Mutuku, M. W., Lu, L., Otiato, F. O., Mwangi, I. N., Kinuthia, J. M., Maina, G. M., Laidemitt, M. R., Lelo, E. A., Ochanda, H., Loker, E. S., & Mkoji, G. M. (2017). A Comparison of Kenyan Biomphalaria pfeifferi and B. Sudanica as Vectors for Schistosoma mansoni , Including a Discussion of the Need to Better Understand the Effects of Snail Breeding Systems on Transmission. Journal of Parasitology, 103(6), 669-676.

https://doi.org/10.1645/17-72 DOI: https://doi.org/10.1645/17-72

Mwakitalu, M. E., Malecela, M. N., Mosha, F. W., & Simonsen, P. E. (2014). Urban schistosomiasis and soil transmitted helminthiases in young school children in Dar es Salaam and Tanga, Tanzania, after a decade of anthelminthic intervention. Acta Tropica, 133(12), 35-41.

https://doi.org/10.1016/j.actatropica.2014.01.012 DOI: https://doi.org/10.1016/j.actatropica.2014.01.012

Mwandawiro, C., Okoyo, C., Kihara, J., Simiyu, E., Kepha, S., Campbell, S. J., Freeman, M. C., Brooker, S. J., & Njenga, S. M. (2019). Results of a national school-based deworming programme on soil-transmitted helminths infections and schistosomiasis in Kenya: 2012-2017. Parasites & Vectors, 12(1), 76-79. https://doi.org/10.1186/s13071-019-3322-1 DOI: https://doi.org/10.1186/s13071-019-3322-1

Perez-Saez, J., Mari, L., Bertuzzo, E., Casagrandi, R., Sokolow, S. H., De Leo, G. A., Mande, T., Ceperley, N., Froehlich, J.-M., Sou, M., Karambiri, H., Yacouba, H., Maiga, A., Gatto, M., & Rinaldo, A. (2015). A Theoretical Analysis of the Geography of Schistosomiasis in Burkina Faso Highlights the Roles of Human Mobility and Water Resources Development in Disease Transmission. PLOS Neglected Tropical Diseases, 9(10), 89-93. e0004127. https://doi.org/10.1371/journal.pntd.0004127 DOI: https://doi.org/10.1371/journal.pntd.0004127

Rite, E. E., Kapalata, S. N., & Munisi, D. Z. (2020). Prevalence, Intensity, and Factors Associated with Urogenital Schistosomiasis among Women of Reproductive Age in Mbogwe District Council, Geita Region, Tanzania. BioMed Research International, 20(2), 1-7. https://doi.org/10.1155/2020/5923025 DOI: https://doi.org/10.1155/2020/5923025

Sakubita, P. (2019). Assessment of prevalence and associated factors for urinary schistosomiasis among primary school going children in Mpongwe district, Zambia [Doctoral dissertation, The University of Zambia]. The University of Zambia Institutional Repository. http://dspace.unza.zm/handle/123456789/6552

Savi, S., Comiti, F., & Strecker, M. R. (2021). Pronounced increase in slope instability linked to global warming: A case study from the eastern European Alps. Earth Surface Processes and Landforms, 46(7), 35. https://doi.org/10.1002/esp.5100 DOI: https://doi.org/10.1002/esp.5100

Stensgaard, A.-S., Utzinger, J., Vounatsou, P., Hürlimann, E., Schur, N., Saarnak, C. F. L., Simoonga, C., Mubita, P., Kabatereine, N. B., Tchuem Tchuenté, L.-A., Rahbek, C., & Kristensen, T. K. (2013). Large-scale determinants of intestinal schistosomiasis and intermediate host snail distribution across Africa: does climate matter? Acta Tropica, 128(2), 378-390. https://doi.org/10.1016/j.actatropica.2011.11.010 DOI: https://doi.org/10.1016/j.actatropica.2011.11.010

Swai, B., Poggensee, G., Mtweve, S., & Krantz, I. (2006). Female genital schistosomiasis as an evidence of a neglected cause for reproductive ill-health: a retrospective histopathological study from Tanzania. BMC Infectious Diseases, 6(1), 134. https://doi.org/10.1186/1471-2334-6-134 DOI: https://doi.org/10.1186/1471-2334-6-134

Takougang, I., Barbazan, P., Tchounwou, P., & Noumi, E. (2008). The Value of the Freshwater Snail Dip Scoop Sampling Method in Macroinvertebrates Bioassessment of Sugar Mill Wastewater Pollution in Mbandjock, Cameroon. International Journal of Environmental Research and Public Health, 5(1), 68-75. https://doi.org/10.3390/ijerph5020068 DOI: https://doi.org/10.3390/ijerph5020068

Thiam, F., Fall, C. B., Gaye, P. M., Senghor, B., Diamanka, A., Wotodjo, A. N., Abotsi, K., Parola, P., Faye, B., Sokhna, C., Sow, D., & Doucouré, S. (2022). Study of the behavior of snails intermediate hosts of Schistosoma spp. under different maintenance conditions and their resistance to salinity in an african laboratory environment. Heliyon, 8(8), 56-59. e10289. https://doi.org/10.1016/j.heliyon.2022.e10289 DOI: https://doi.org/10.1016/j.heliyon.2022.e10289

Vilches, T. N., Graeff-Teixeira, C., & Yang, H. M. (2021). Assessing the effects of diagnostic sensitivity on schistosomiasis dynamics. Journal of Theoretical Biology, 52(3), 110-127. https://doi.org/10.1016/j.jtbi.2021.110727 DOI: https://doi.org/10.1016/j.jtbi.2021.110727

Wanlop, A., Dang-Trinh, M. A., Kirinoki, M., Suguta, S., Shinozaki, K., & Kawazu, S. I. (2022). A simple and efficient miracidium hatching technique for preparing a single-genome DNA sample of Schistosoma japonicum. The Journal of veterinary medical science, 84(8), 1108-1110. https://doi.org/10.1292/jvms.21-0536 DOI: https://doi.org/10.1292/jvms.21-0536

Wubet, K., & Damtie, D. (2020). Prevalence of Schistosoma mansoni Infection and Associated Risk Factors among School Children in Jiga Town, Northwest-Ethiopia: A Cross-Sectional Study. Journal of Parasitology Research, 2(20), 1-7. https://doi.org/10.1155/2020/6903912 DOI: https://doi.org/10.1155/2020/6903912

Zeleke, A. J., Derso, A., Bayih, A. G., Gilleard, J. S., & Eshetu, T. (2021). Prevalence, Infection Intensity and Associated Factors of Soil-Transmitted Helminthiasis Among School-Aged Children from Selected Districts in Northwest Ethiopia. Research and Reports in Tropical Medicine, 12(4), 15-23. https://doi.org/10.2147/RRTM.S289895 DOI: https://doi.org/10.2147/RRTM.S289895