Effects of Land-Use and Environmental Factors on Snail Distribution and Trematode Infection in Ethiopia
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Area
2.2. Snail Sampling and Identification
2.3. Examination of Cercarial Infection
2.4. Land Use, Land Cover, and Spatial Mapping
2.5. Environmental Factors
2.6. Data Analysis
3. Results
3.1. Abundance and Distribution of Freshwater Snail Intermediate Hosts
3.2. Cercarial Shedding of Freshwater Snails
3.3. Environmental Determinants of Snail Abundance and Trematode Infection
4. Discussion
5. Implication for the Control of Snail-Borne Diseases
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Strong, E.E.; Gargominy, O.; Ponder, W.F.; Bouchet, P. Global diversity of gastropods (Gastropoda; Mollusca) in freshwater. In Freshwater Animal Diversity Assessment; Developments in Hydrobiology; Balian, E.V., Lévêque, C., Segers, H., Martens, K., Eds.; Springer: Dordrecht, The Netherlands, 2007; Volume 198, pp. 149–166. [Google Scholar]
- Soldánová, M.; Selbach, C.; Kalbe, M.; Kostadinova, A.; Sures, B. Swimmer’s itch: Etiology, impact, and risk factors in Europe. Trends Parasitol. 2013, 29, 65–74. [Google Scholar] [CrossRef]
- World Health Organization. Schistosomiasis. Available online: https://www.who.int/news-room/fact-sheets/detail/schistosomiasis (accessed on 1 April 2022).
- Lu, X.T.; Gu, Q.Y.; Limpanont, Y.; Song, L.G.; Wu, Z.D.; Okanurak, K.; Lv, Z.Y. Snail-borne parasitic diseases: An update on global epidemiological distribution, transmission interruption and control methods. Infect. Dis. Poverty 2018, 7, 28. [Google Scholar] [CrossRef] [Green Version]
- Tsega, M.; Dereso, S.; Getu, A. A Review on ruminant fascioliasis. Open Access Libr. J. 2015, 2, 68558. [Google Scholar]
- Ayele, Y.; Wondmnew, F.; Yeshiwas, T. The prevalence of bovine and ovine fasciolosis and the associated economic loss due to liver condemnation in and around Debire Birhan, Ethiopia. SOJ Immunol. 2018, 6, 1–11. [Google Scholar] [CrossRef]
- Bilal, Z.M.; Musa, K.S. Coprological prevalence and associated risk factor of bovine fascioliasis around Furda veterinary clinic, East Hararghe, Ethiopia. Open. J. Vet. Med. 2021, 6, 39–44. [Google Scholar] [CrossRef]
- Fentie, T.; Erqou, S.; Gedefaw, M.; Desta, A. Epidemiology of human fascioliasis and intestinal parasitosis among schoolchildren in Lake Tana Basin, northwest Ethiopia. Trans. Roy. Soc. Trop. Med. Hyg. 2013, 107, 480–486. [Google Scholar] [CrossRef]
- Arancha, A.; Anegagrie, M.; Zewdie, D.; Benito, A. Schistosoma mansoni in a rural community of Ethiopia. In Proceedings of the 27th European Congress of Clinical Microbiology and Infectious Diseases, Veinna, Austria, 22–25 April 2017. [Google Scholar]
- Meleko, A.; Li, S.; Turgeman, D.B.; Bruck, M.; Kesete, N.Z.; Zaadnoordijk, W.; Rollinson, D.; Sabar, G.; Bentwich, Z.; Golan, R. Schistosomiasis Control in Ethiopia: The Role of Snail Mapping in Endemic Communities. Trop. Med. Infect. Dis. 2022, 7, 272. [Google Scholar] [CrossRef]
- Wamae, L.W.; Hammond, J.A.; Harrison, L.J.; Onyango-Abuje, J.A. Comparison of production losses caused by chronic Fasciola gigantica infection in yearling Friesian and Boran cattle. Trop. Anim. Health Prod. 1998, 30, 23–30. [Google Scholar] [CrossRef]
- Lund, A.J.; Rehkopf, D.H.; Sokolow, S.H.; Sam, M.M.; Jouanard, N.; Schacht, A.-M.; Senghor, S.; Fall, A.; Riveau, G.; De Leo, G.A.; et al. Land use impacts on parasitic infection: A cross-sectional epidemiological study on the role of irrigated agriculture in schistosome infection in a dammed landscape. Infect. Dis. Poverty 2021, 10, 35. [Google Scholar] [CrossRef]
- Mas-Coma, S.; Bargues, M.D.; Valero, M.A. Human fascioliasis infection sources, their diversity, incidence factors, analytical methods and prevention measures. Parasitology 2018, 145, 1665–1699. [Google Scholar] [CrossRef] [Green Version]
- Yigezu, G.; Mandefro, B.; Mengesha, Y.; Yewhalaw, D.; Beyene, A.; Ahmednur, M.; Abdie, Y.; Kloos, H.; Mereta, S.T. Habitat suitability modelling for predicting potential habitats of freshwater snail intermediate hosts in Omo-Gibe river basin, Southwest Ethiopia. Ecol. Inform. 2018, 45, 70–80. [Google Scholar] [CrossRef]
- 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, 411–425. [Google Scholar] [CrossRef]
- Paul, M.J.; Meyer, J.L. Streams in the urban landscape. Ann. Rev. Ecol. Syst. 2001, 32, 333–365. [Google Scholar] [CrossRef]
- Oso, O.G.; Odaibo, A.B. Land use/land cover change, physico-chemical parameters and freshwater snails in Yewa North, South-387 western Nigeria. PLoS ONE 2021, 16, e0246566. [Google Scholar] [CrossRef]
- Perrings, C.; Halkos, G. Agriculture and the threat to biodiversity in subsaharan Africa. Environ. Res. Lett. 2015, 10, 095015. [Google Scholar] [CrossRef]
- Halstead, N.T.; Hoover, C.M.; Arakala, A.; Civitello, D.J.; De Leo, G.A.; Gambhir, M.; Johnson, S.A.; Jouanard, N.; Loerns, K.A.; McMahon, T.A.; et al. Agrochemicals increase risk of human schistosomiasis by supporting higher densities of intermediate hosts. Nat. Commun. 2018, 9, 837. [Google Scholar] [CrossRef]
- Barbosa, F.S.; Barbosa, C.S. The bioecology of snail vector for Schistosomiasis in Brazil. Br. J. Anim. Ecol. 1994, 5, 116–186. [Google Scholar]
- Ahmed, E.F.; Markvichitr, K.; Tumwasorn, S.; Koonawootrittriron, S.; Choothesa, A.; Jittapalapong, S. Prevalence of Fasciola spp Infections of sheep in the Middle Awash River Basin, Ethiopia. Southeast Asian. J. Trop. Med. Public. Health 2007, 38, 51–57. [Google Scholar]
- Appleton, C.C. Review of literature on abiotic factors influencing the distribution and life cycles of bilharziasis intermediate host snails. Malacol. Rev. 1978, 11, 25. [Google Scholar]
- Biniam, T.; Hanna, A.; Sissay, G. Coprological prevalence of bovine fasciolosis in and around woreta, Northwestern Ethiopia. J. Vet. Med. Ani. Health 2012, 4, 89–92. [Google Scholar]
- National Meteorological Agency (NMA). Available online: www.ethiomet.gov.et (accessed on 20 June 2021).
- Ministry of Agriculture. Agro-Ecological Zones of Ethiopia. Natural Resources Management& Regulatory Department. German Agency for Technical Cooperation (GTZ). 1998. Available online: http://publication.eiar.gov.et:8080/xmlui/bitstream/handle/123456789/2517/agroecologicalzones%20of%20ethiopia.pdfabbyyy.pdf?sequence=1&isAllowed=y (accessed on 5 January 2023).
- Devi, R.; Tesfahun, E.; Legesse, W.; Deboch, B.; Beyene, A. Assessment of siltation and nutrient enrichment of Gilgel Gibe dam, Southwest Ethiopia. Bioresource. Technol. 2008, 99, 975–979. [Google Scholar] [CrossRef]
- Ofoezie, I.E. Distribution of freshwater snails in the manmade Oyan reservoir, Ogun state, Nigeria. Hydrobiologia 1999, 416, 181–191. [Google Scholar] [CrossRef]
- Opisa, S.; Odiere, M.R.; Jura, W.G.; Karanja, D.M.S.; Mwinzi, P.N.M. Malacological survey and geographical distribution of vector snails for schistosomiasis within informal settlements of Kisumu City, western Kenya. Parasites Vectors 2011, 4, 226. [Google Scholar] [CrossRef] [Green Version]
- Harrold, N.M.; Guralnick, R.P. A Field Guide to the Freshwater Mollusks of Colorado. Denver: Colorado Division of Wildlife. 2010. Available online: http://www.takeaim.org/ (accessed on 10 September 2021).
- Ahmed, A.A.M.; Ibrahim, N.A.; Idris, M.A. Laboratory Studies on the Prevalence and Cercarial Rhythms of Trematodes from Bulinus truncatus and Biomphalaria pfeifferi Snails from Khartoum State. Sultan. Qaboos. Univ. Med. J. 2006, 6, 65–69. [Google Scholar]
- Devkota, R.; Brant, S.V.; Loker, E.S. The Schistosoma indicum species group in Nepal: Presence of a new lineage of schistosome and use of the Indoplanorbis exustus species complex of snail hosts. Int. J. Parasitol. 2015, 45, 857–870. [Google Scholar] [CrossRef] [Green Version]
- Frandsen, F.; Christensen, N.Ø. An introductory guide to the identification of cercariae from African freshwater snails with special reference to cercariae of trematode species of medical and veterinary importance. Acta Trop. 1984, 41, 181–202. [Google Scholar] [CrossRef]
- Jones, A. Handbook of the Trematodes of North America North of Mexico; Schell, S.C., Ed.; University Press of ldaho: Moscow, IA, USA, 1985; 263p, ISBN 0-89301-095-2. [Google Scholar] [CrossRef]
- Jayawardena, U.A.; Rajakaruna, R.S.; Amerasinghe, P.H. Cercariae of trematodes in freshwater snails in three climatic zones in Sri Lanka. Ceylon. J. Sci. 2011, 39, 95. [Google Scholar] [CrossRef] [Green Version]
- Posa, M.R.C.; Sodhi, N.S. Effects of anthropogenic land use on forest birds and butterflies in Subic Bay, Philippines. Biol. Conserv. 2006, 129, 256–270. [Google Scholar] [CrossRef]
- ter Braak, C.J.F.; Šmilauer, P. CANOCO Reference Manual and CanoDraw for Windows User’s Guide: Software for Canonical Community Ordination (Version 4.5); Microcomputer Power: Ithaca NY, USA, 2002; 500p. [Google Scholar]
- Olkeba, B.K.; Boets, P.; Mereta, S.T.; Mandefro, B.; Debesa, G.; Ahmednur, M.; Ambelu, A.; Korma, W.; Goethals, P.L. Malacological and Parasitological Surveys on Ethiopian Rift Valley Lakes: Implications for Control and Elimination of Snail-Borne Diseases. Int. J. Environ. Res. Public Health 2021, 19, 142. [Google Scholar] [CrossRef]
- Deribew, K.; Erko, B.; Mereta, S.T.; Yewhalaw, D.; Mekonnen, Z. Assessing Potential Intermediate Host Snails of Urogenital Schistosomiasis, Human Water Contact Behavior and Water Physico-chemical Characteristics in Alwero Dam Reservoir, Ethiopia. Environ. Health Insights 2022, 16, 11786302221123576. [Google Scholar] [CrossRef]
- Joubert, P.H.; Pretorius, S.J.; Kruger, F.J. Further studies on the susceptibility of Bulinus africanus to infection with Schistosoma haematobium. Ann. Trop. Med. Parasitol. 1991, 85, 253–258. [Google Scholar] [CrossRef]
- Hussen, S.; Assegu, D.; Tadesse, B.T.; Shimelis, T. Prevalence of Schistosoma mansoni infection in Ethiopia: A systematic review and meta-analysis. Trop. Dis. Travel Med. Vaccines 2021, 7, 4. [Google Scholar] [CrossRef]
- Gebreyesus, T.D.; Tadele, T.; Mekete, K.; Barry, A.; Gashaw, H.; Degefe, W.; Tadesse, B.T.; Gerba, H.; Gurumurthy, P.; Makonnen, E.; et al. Prevalence, Intensity, and Correlates of Schistosomiasis and Soil-Transmitted Helminth Infections after Five Rounds of Preventive Chemotherapy among School Children in Southern Ethiopia. Pathogens. 2020, 9, 920. [Google Scholar] [CrossRef]
- Fried, B.; Graczyk, T.K.; Tamang, L. Food-borne intestinal trematodiases in humans. Parasitol. Res. 2004, 93, 159–170. [Google Scholar] [CrossRef]
- Teledo, R.; Esteban, J.G. An update on human Echinostomiasis. Trans. R. Soc. Trop. Med. Hyg. 2016, 110, 37–45. [Google Scholar] [CrossRef]
- Mereta, S.T.; Bedewi, J.; Yewhalaw, D.; Mandefro, B.; Abdie, Y.; Tegegne, D.; Birke, W.; Mulat, W.L.; Kloos, H. Environmental determinants of distribution of freshwater snails and trematode infection in the Omo Gibe River Basin, southwest Ethiopia. Infect. Dis. Poverty 2019, 8, 93. [Google Scholar] [CrossRef] [Green Version]
- Younes, A.; El-Sherief1, H.; Gawish, F.; Mahmoud, M. Biological control of snail hosts transmitting schistosomiasis by the water bug, Sphaerodema urinator. Parasitol. Res. 2017, 116, 1257–1264. [Google Scholar] [CrossRef]
- Olkeba, B.K.; Boets, P.; Mereta, S.T.; Yeshigeta, M.; Akessa, G.M.; Ambelu, A.; Goethals, P.L.M. Environmental and biotic factors affecting freshwater snail intermediate hosts in the Ethiopian Rift Valley region. Parasites Vectors 2020, 13, 292. [Google Scholar] [CrossRef]
- De La Rocque, S.; Rioux, J.A.; Slingenbergh, J. Climate change: Effects on animal disease systems and implications for surveillance and control. Rev. Sci. Tech. 2008, 27, 339–354. [Google Scholar]
- Kristensen, T.K.; Malone, J.B.; McCarroll, J.C. Use of satellite remote sensing and geographic information systems to model the distribution and abundance of snail intermediate hosts in Africa: A preliminary model for Biomphalaria pfeifferi in Ethiopia. Acta. Trop. 2001, 79, 73–78. [Google Scholar] [CrossRef]
- De Troyer, N.; Mereta, S.T.; Goethals, P.L.M.; Boets, P. Water quality assessment of streams and wetlands in a fast growing east African city. Water 2016, 8, 123. [Google Scholar] [CrossRef] [Green Version]
- Howell, A.; Mugisha, L.; Davies, J.; LaCourse, E.J.; Claridge, J.; Williams, D.J.L.; Kelly-Hope, L.; Betson, M.; Kabatereine, N.B.; Stothard, J.R. Bovine fasciolosis at increasing altitudes: Parasitological and malacological sampling on the slopes of Mount Elgon, Uganda. Parasites Vectors 2012, 5, 196. [Google Scholar] [CrossRef] [Green Version]
- Howell, A.; Baylis, M.; Smith, R.; Pinchbeck, G.; Williams, D. Epidemiology and impact of Fasciola hepatica exposure in high-yielding dairy herds. Prev. Vet. Med. 2015, 121, 41–48. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Omer, N.; Bitew, B.D.; Engdaw, G.T.; Getachew, A. Utilization of latrine and associated factors among rural households in Takussa District, Northwest Ethiopia: A Community-Based Cross-Sectional Study. Environ. Health Insights 2022, 16, 11786302221091742. [Google Scholar] [CrossRef]
- Evan, S.W. Water-based interventions for schistosomiasis control. Pathog. Glob. Health 2014, 108, 246–254. [Google Scholar] [CrossRef] [Green Version]
Snail Species | Gilgel Gibe | Meskan | ||
---|---|---|---|---|
Abundance | Frequency of Occurrence (%) | Abundance | Frequency of Occurrence (%) | |
L. natalensis | 93 | 67 | 159 | 43 |
Bu. globosus | 99 | 33 | 147 | 43 |
B. pfeifferi | 56 | 67 | 61 | 57 |
Total | 248 | _ | 367 | _ |
LULC Type | Gilgel Gibe | Meskan | ||
---|---|---|---|---|
Area (ha) | % | Area (ha) | % | |
Agriculture | 151,702 | 52.6 | 349,075 | 68 |
Bare land | 67,118 | 23.3 | _ | _ |
Forest | 19,772 | 6.9 | 100,131 | 19.5 |
Water | 49,704 | 17.2 | 950 | 0.2 |
Settlement | _ | _ | 62,480 | 12 |
Swampy | _ | _ | 1563 | 0.3 |
Snail Species | Number (%) of Snails Infected by Cercariae | |||
---|---|---|---|---|
Xiphidiocercariae | BAD | Echinostome | Fasciola | |
L. natalensis | 26 | 25 | 0 | 97 |
Bu. globosus | 0 | 0 | 47 | 0 |
B. pfeifferi | 0 | 7 | 0 | 0 |
Total | 26 | 32 | 47 | 97 |
Variable | Gilgel Gibe (n = 6) | Meskan (n = 7) | Z-Adjusted | p-Value |
---|---|---|---|---|
Altitude (m) | 1674.67 ± 33 | 2037.14 ± 117 | −3.00 | 0.002 * |
Oxygen saturation (%) | 49.72 ± 38.5 | 58.44 ± 34 | −0.43 | 0.58 |
EC (µS/cm) | 307.78 ± 167 | 337.03 ± 134 | −0.57 | 0.57 |
pH | 7.19 ± 0.4 | 7.46 ± 0.3 | −1.86 | 0.06 |
Turbidity (NTU) | 66.38 ± 67 | 105.24 ± 92 | −0.57 | 0.57 |
Water depth (m) | 0.45 ± 0.9 | 0.20 ± 0.15 | 2.5 | 0.01 * |
Canopy cover (%) | 16.67 ± 16 | 20.00 ± 9.6 | −0.58 | 0.56 |
Water temperature (°C) | 23.88 ± 1 | 21.20 ± 0.98 | 3.00 | 0.002 * |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Mereta, S.T.; Abaya, S.W.; Tulu, F.D.; Takele, K.; Ahmednur, M.; Melka, G.A.; Nanyingi, M.; Vineer, H.R.; Graham-Brown, J.; Caminade, C.; et al. Effects of Land-Use and Environmental Factors on Snail Distribution and Trematode Infection in Ethiopia. Trop. Med. Infect. Dis. 2023, 8, 154. https://doi.org/10.3390/tropicalmed8030154
Mereta ST, Abaya SW, Tulu FD, Takele K, Ahmednur M, Melka GA, Nanyingi M, Vineer HR, Graham-Brown J, Caminade C, et al. Effects of Land-Use and Environmental Factors on Snail Distribution and Trematode Infection in Ethiopia. Tropical Medicine and Infectious Disease. 2023; 8(3):154. https://doi.org/10.3390/tropicalmed8030154
Chicago/Turabian StyleMereta, Seid Tiku, Samson Wakuma Abaya, Fikirte Demissie Tulu, Kebede Takele, Mahmud Ahmednur, Girma Alemu Melka, Mark Nanyingi, Hannah Rose Vineer, John Graham-Brown, Cyril Caminade, and et al. 2023. "Effects of Land-Use and Environmental Factors on Snail Distribution and Trematode Infection in Ethiopia" Tropical Medicine and Infectious Disease 8, no. 3: 154. https://doi.org/10.3390/tropicalmed8030154
APA StyleMereta, S. T., Abaya, S. W., Tulu, F. D., Takele, K., Ahmednur, M., Melka, G. A., Nanyingi, M., Vineer, H. R., Graham-Brown, J., Caminade, C., & Mor, S. M. (2023). Effects of Land-Use and Environmental Factors on Snail Distribution and Trematode Infection in Ethiopia. Tropical Medicine and Infectious Disease, 8(3), 154. https://doi.org/10.3390/tropicalmed8030154