Programmatic Implications for Schistosomiasis Elimination Based on Community-Based Survey in the Blue Nile, North Kordofan, and Sennar States, Sudan
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Areas
2.2. Study Design
2.3. Sampling and Sample Size
2.4. Diagnosis
2.5. Questionnaire
2.6. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Montresor, A.; Mwinzi, P.; Mupfasoni, D.; Garba, A. Reduction in DALYs lost due to soil-transmitted helminthiases and schistosomiasis from 2000 to 2019 is parallel to the increase in coverage of the global control programmes. PLoS Negl. Trop. Dis. 2022, 16, e0010575. [Google Scholar] [CrossRef] [PubMed]
- World Health Organization. Schistosomiasis 2023. Available online: https://www.who.int/news-room/fact-sheets/detail/schistosomiasis (accessed on 12 March 2023).
- Colley, D.G.; Bustinduy, A.L.; Secor, W.E.; King, C.H. Human schistosomiasis. Lancet 2014, 383, 2253–2264. [Google Scholar] [CrossRef] [PubMed]
- FMOH. The Sudan National Neglected Tropical Diseases (NTDs) Strategic Plan 2021–2025; Federal Ministry of Health: Khartum, Sudan, 2021.
- Cha, S.; Elhag, M.S.; Lee, Y.H.; Cho, D.S.; Ismail, H.A.H.A.; Hong, S.T. Epidemiological findings and policy implications from the nationwide schistosomiasis and intestinal helminthiasis survey in Sudan. Parasit. Vectors 2019, 12, 429. [Google Scholar] [CrossRef] [PubMed]
- Stothard, J.R.; Mgeni, A.F.; Khamis, S.; Seto, E.; Ramsan, M.; Rollinson, D. Urinary schistosomiasis in schoolchildren on Zanzibar Island (Unguja), Tanzania: A parasitological survey supplemented with questionnaires. Trans. R. Soc. Trop. Med. Hyg. 2002, 96, 507–514. [Google Scholar] [CrossRef] [PubMed]
- Rudge, J.W.; Stothard, J.R.; Basáñez, M.G.; Mgeni, A.F.; Khamis, I.S.; Khamis, A.N.; Rollinson, D. Micro-epidemiology of urinary schistosomiasis in Zanzibar: Local risk factors associated with distribution of infections among schoolchildren and relevance for control. Acta Trop. 2008, 105, 45–54. [Google Scholar] [CrossRef] [PubMed]
- Guidi, A.; Andolina, C.; Makame Ame, S.; Albonico, M.; Cioli, D.; Juma Haji, H. Praziquantel efficacy and long-term appraisal of schistosomiasis control in Pemba Island. Trop. Med. Int. Health 2010, 15, 614–618. [Google Scholar] [CrossRef]
- Laamrani, H.; Mahjour, J.; Madsen, H.; Khallaayoune, K.; Gryseels, B. Schistosoma haematobium in Morocco: Moving from control to elimination. Parasitol. Today 2000, 16, 257–260. [Google Scholar] [CrossRef]
- Clennon, J.A.; King, C.H.; Muchiri, E.M.; Kariuki, H.C.; Ouma, J.H.; Mungai, P.; Kitron, U. Spatial patterns of urinary schistosomiasis infection in a highly endemic area of coastal Kenya. Am. J. Trop. Med. Hyg. 2004, 70, 443–448. [Google Scholar] [CrossRef]
- Clennon, J.A.; Mungai, P.L.; Muchiri, E.M.; King, C.H.; Kitron, U. Spatial and temporal variations in local transmission of Schistosoma haematobium in Msambweni, Kenya. Am. J. Trop. Med. Hyg. 2006, 75, 1034–1041. [Google Scholar] [CrossRef]
- Sang, H.C.; Muchiri, G.; Ombok, M.; Odiere, M.R.; Mwinzi, P.N. Schistosoma haematobium hotspots in south Nyanza, western Kenya: Prevalence, distribution and co-endemicity with Schistosoma mansoni and soil-transmitted helminths. Parasit. Vectors 2014, 7, 125. [Google Scholar] [CrossRef]
- Zou, L.; Ruan, S. Schistosomiasis transmission and control in China. Acta Trop. 2015, 143, 51–57. [Google Scholar] [CrossRef] [PubMed]
- Pennance, T.; Person, B.; Muhsin, M.A.; Khamis, A.N.; Muhsin, J.; Khamis, I.S.; Mohammed, K.A.; Kabole, F.; Rollinson, D.; Knopp, S. Urogenital schistosomiasis transmission on Unguja Island, Zanzibar: Characterisation of persistent hot-spots. Parasit Vectors 2016, 9, 646. [Google Scholar] [CrossRef] [PubMed]
- WHO. Ending the Neglect to Attain the Sustainable Development Goals a Road Map for Neglected Tropical Diseases 2021–2030; World Health Organization: Geneva, Switzerland, 2021. [Google Scholar]
- WHO. WHO Guideline on Control and Elimination of Human Schistosomiasis; World Health Organization: Geneva, Switzerland, 2022. [Google Scholar]
- Encyclopædia Britannica; Encyclopædia Britannica, Inc.: Chicago, IL, USA, 2022.
- Cha, S.; Jin, Y.; Elhag, M.S.; Kim, Y.; Ismail, H.A.H.A. Unequal geographic distribution of water and sanitation at the household and school level in Sudan. PLoS ONE 2021, 16, e0258418. [Google Scholar] [CrossRef] [PubMed]
- UNDP. Common Country Analysis for Sudan Desk Review; United Nation Development Programme: New York, NY, USA, 2016. [Google Scholar]
- UNICEF. State Profile: Blue Nile; United Nations Children’s Fund: Khartoum, Sudan, 2022. [Google Scholar]
- UNICEF. State Profile: North Kordofan; United Nations Children’s Fund: Khartoum, Sudan, 2022. [Google Scholar]
- IHA. Sudan-Sennar. London; International Hydropower Association: 2022. Available online: https://www.hydropower.org/sediment-management-case-studies/sudan-sennar (accessed on 12 March 2023).
- Kittur, N.; King, C.H.; Campbell, C.H.; Kinung’hi, S.; Mwinzi, P.N.M.; Karanja, D.M.S.; N’Goran, E.K.; Phillips, A.E.; Gazzinelli-Guimaraes, P.H.; Olsen, A.; et al. Persistent Hotspots in Schistosomiasis Consortium for Operational Research and Evaluation Studies for Gaining and Sustaining Control of Schistosomiasis after Four Years of Mass Drug Administration of Praziquantel. Am. J. Trop. Med. Hyg. 2019, 101, 617–627. [Google Scholar] [CrossRef]
- Assaré, R.K.; N’Tamon, R.N.; Bellai, L.G.; Koffi, J.A.; Mathieu, T.I.; Ouattara, M.; Hürlimann, E.; Coulibaly, J.T.; Diabaté, S.; N’Goran, E.K.; et al. Characteristics of persistent hotspots of Schistosoma mansoni in western Côte d’Ivoire. Parasit. Vectors 2020, 13, 337. [Google Scholar] [CrossRef]
- Mawa, P.A.; Kincaid-Smith, J.; Tukahebwa, E.M.; Webster, J.P.; Wilson, S. Schistosomiasis Morbidity Hotspots: Roles of the Human Host, the Parasite and Their Interface in the Development of Severe Morbidity. Front. Immunol. 2021, 12, 635869. [Google Scholar] [CrossRef]
- Whittington, D.; Radin, M.; Jeuland, M. Evidence-based policy analysis? The strange case of the randomized controlled trials of community-led total sanitation. Oxf. Rev. Econ. Policy 2020, 36, 191–221. [Google Scholar] [CrossRef]
- Surya, A.V.; Vyas, A.; Krishna, M.; Abidi, N. Identifying Determinants of Toilet Usage by Poor in Urban India. Procedia Comput. Sci. 2017, 122, 634–641. [Google Scholar]
- Cha, S.; Jung, S.; Bizuneh, D.B.; Abera, T.; Doh, Y.A.; Seong, J.; Schmidt, W.P. Effect of a Community-led Total Sanitation Intervention on the Incidence and Prevalence of Diarrhea in Children in Rural Ethiopia: A Cluster-randomized Controlled Trial. Am. J. Trop. Med. Hyg. 2021, 105, 532–543. [Google Scholar] [CrossRef]
- Nakagiri, A.; Kulabako, R.N.; Nyenje, P.M.; Tumulhairwe, J.B.; Niwagaba, C.B.; Kansiime, F. Performance of pit latrines in urban poor areas: A case of Kampala, Uganada. Habitat Int. 2015, 49, 529–537. [Google Scholar] [CrossRef]
- Nakagiri, A.; Niwagaba, C.B.; Nyenje, P.M.; Kulabako, R.N.; Tumuhairwe, J.B.; Kansiime, F. Are pit latrines in urban areas of Sub-Saharan Africa performing? A review of usage, filling, insects and odour nuisances. BMC Public Health 2016, 16, 120. [Google Scholar] [CrossRef] [PubMed]
- Potter, A.; Uandela, A.; Naafs, A. Assessing Sanitation Service Levels; Working paper 3; IRC International Water and Sanitation Centre: Hague, The Netherlands, 2011. [Google Scholar]
- KOICA. Project Design Document of the Schistosomiasis Elimination along the Nile-River in Sudan with Empowered People Project; Korea Internation Cooperation Agency: Seongnam, Republic of Korea, 2020.
- Jin, Y.; Lee, Y.H.; Cha, S.; Choi, I.U.; Ismail, H.A.H.A.; Elhag, M.S.; Hong, S.T. Transmission Dynamics of Schistosoma haematobium among School-Aged Children: A Cohort Study on Prevalence, Reinfection and Incidence after Mass Drug Administration in the White Nile State of Sudan. Int. J. Environ. Res. Public Health 2021, 18, 11537. [Google Scholar] [CrossRef] [PubMed]
- Cha, S.; Hong, S.T.; Lee, J.S.; Jeong, H.G.; Kwon, I.S.; Saed, A.A.W.; Elhag, M.S.; Ismail, H.A.H.A.; Amin, M.; Lee, Y.H. Comparison of the Change in the Prevalence and Intensity of Schistosoma haematobium Infection Between High and Low Prevalence Areas of White Nile State, Sudan. Korean J. Parasitol. 2020, 58, 421–430. [Google Scholar] [CrossRef] [PubMed]
- Jin, Y.; Cha, S.; Lee, J.; Elhag, M.S.; Hong, S.T.; Lee, Y.H. Parasitological Observation in Schoolchildren with Urogenital Schistosomiasis Following Treatment with Three Different Brands of Praziquantel. J. Korean Med. Sci. 2020, 35, e394. [Google Scholar] [CrossRef]
- KOICA. Report of the International Conference On Schistosomiasis in Sudan; Korea International Cooperation Agency: Seongnam, Republic of Korea, 2023.
- Amin, M.; H Abubaker. Control fo schistosomiasis in the Gezira irrigation scheme, Sudan. J. Biosoc. Sci. 2017, 49, 83–98. [Google Scholar] [CrossRef]
- Eltayeb, N.M.; Mukhtar, M.M.; Mohamed, A.B. Epidemiology of schistosomiasis in Gezira area Central Sudan and analysis of cy tokine profiles. Asian Pac. J. Trop. Med. 2013, 6, 119–125. [Google Scholar] [CrossRef]
- Fenwick, A.; Cheesmond, A.K.; Amin, M.A. The role of field irriga tion canals in the transmission of Schistosoma mansoni in the Gezira Scheme, Sudan. Bull. World Health Organ. 1981, 59, 777–786. [Google Scholar]
- Hilali, A.H.; Madsen, H.; Daffalla, A.A.; Wassila, M.; Christensen, N.O. Infection and transmission pattern of Schistosoma mansoni in the Managil irrigation scheme, Sudan. Ann. Trop. Med. Parasitol. 1995, 89, 279–286. [Google Scholar] [CrossRef]
- Mohammed, E.H.; Eltayeb, M.; Ibrahim, H. Haematological and biochemical morbidity of schistosoma haematobium in school children in Sudan. Sultan Qaboos Univ. Med. J. 2006, 6, 59–64. [Google Scholar]
- Clements, A.C.; Brooker, S.; Nyandindi, U.; Fenwick, A.; Blair, L. Bayesian spatial analysis of a national urinary schistosomiasis questionnaire to assist geographic targeting of schistosomiasis control in Tanzania, East Africa. Int. J. Parasitol. 2008, 38, 401–415. [Google Scholar] [CrossRef]
- Lengeler, C.; Utzinger, J.; Tanner, M. Questionnaires for rapid screening of schistosomiasis in sub-Saharan Africa. Bull. World Health Organ. 2002, 80, 235–242. [Google Scholar] [PubMed]
- Sturrock, H.J.W.; Pullan, R.L.; Kihara, J.H.; Mwandawiro, C.; Brooker, S.J. Te use of bivariate spatial modeling of questionnaire and parasitology data to predict the distribution of Schistosoma haematobium in Coastal Kenya. PLoS Neglect. Trop. Dis. 2013, 7, e2016. [Google Scholar] [CrossRef] [PubMed]
- King, C.H. Toward the elimination of schistosomiasis. N. Engl. J. Med. 2009, 360, 106–109. [Google Scholar] [CrossRef] [PubMed]
- Rollinson, D.; Knopp, S.; Levitz, S.; Stothard, J.R.; Tchuem Tchuenté, L.A.; Garba, A.; Mohammed, K.A.; Schur, N.; Person, B.; Colley, D.G.; et al. Time to set the agenda for schistosomiasis elimination. Acta Trop. 2013, 128, 423–440. [Google Scholar] [CrossRef] [PubMed]
- Lv, C.; Deng, W.; Wang, L.; Qin, Z.; Zhou, X.; Xu, J. Molecular Techniques as Alternatives of Diagnostic Tools in China as Schistosomiasis Moving towards Elimination. Pathogens 2022, 11, 287. [Google Scholar] [CrossRef]
- Ayabina, D.V.; Clark, J.; Bayley, H.; Lamberton, P.H.L.; Toor, J.; Hollingsworth, T.D. Gender-related differences in prevalence, intensity and associated risk factors of Schistosoma infections in Africa: A systematic review and meta-analysis. PLoS Negl. Trop. Dis. 2021, 15, e0009083. [Google Scholar] [CrossRef]
- Woldeyohannes, D.; Sahiledengle, B.; Tekalegn, Y.; Hailemariam, Z. Prevalence of Schistosomiasis (S. mansoni and S. haematobium) and its association with gender of school age children in Ethiopia: A systematic review and meta-analysis. Parasite Epidemiol. Control 2021, 13, e00210. [Google Scholar] [CrossRef]
- UNICEF. National Road Map: Sanitation for all in Sudan (Making Sudan Open Defecation Free by 2022); United Nations Children’s Fund Sudan: Khartum, Sudan, 2018. [Google Scholar]
- FMOH. Sudan National Sanitation and Hygiene Strategic Framework; Federal Ministry of Health: Khartum, Sudan, 2016.
- FMOWRIE. Sudan Drinking Water Safety Strategic Framework; Federal Ministry of Water Resources, Irrigation and Electricity: Khartum, Sudan, 2017.
- SWA. SWA Report on the 2020 Finance Ministers’ Meetings; Sanitation and Water for All: New York, NY, USA, 2020. [Google Scholar]
All | School-Aged Children | |||||||
---|---|---|---|---|---|---|---|---|
State | District | No. of Villages a | No. of Participants | Age (SD b) | % of Male | No. of Participants | Age (SD) | % of Male |
Blue Nile | Aroaires | 5 | 510 | 22.9 (17.3) | 44.7 | 265 | 10.08 (2.62) | 51.7 |
Wad Al Mlahi | 7 | 735 | 26.2 (17.5) | 42.6 | 306 | 10.06 (2.68) | 47.1 | |
Gissan | 8 | 827 | 24.3 (17.0) | 37.1 | 376 | 10.25 (2.75) | 46.0 | |
Subtotal | 20 | 2072 | 24.7 (17.3) | 40.9 | 947 | 10.14 (2.69) | 47.9 | |
Sennar | Sennar | 7 | 731 | 23.1 (16.8) | 44.9 | 342 | 10.02 (2.61) | 52.6 |
Al Sooki | 6 | 635 | 22.0 (17.3) | 47.1 | 358 | 10.12 (2.70) | 59.2 | |
East Sennar | 7 | 711 | 23.4 (17.9) | 45.0 | 357 | 10.06 (2.74) | 55.5 | |
Subtotal | 20 | 2077 | 22.9 (17.3) | 45.6 | 1057 | 10.07 (2.68) | 55.8 | |
North Kordofan | Al Rahud | 10 | 1053 | 23.1 (17.7) | 43.4 | 560 | 10.27 (2.71) | 50.9 |
Um Rwaba | 10 | 1023 | 27.7 (20.0) | 39.9 | 423 | 10.01 (2.58) | 50.8 | |
Subtotal | 20 | 2076 | 25.4 (19.0) | 41.7 | 983 | 10.16 (2.65) | 50.9 | |
Total | 60 | 6225 | 24.3 (17.9) | 42.7 | 2987 | 10.12 (2.68) | 51.7 |
S. haematobium | S. mansoni | ||||||||
---|---|---|---|---|---|---|---|---|---|
State | District | All Ages | School-Aged Children | All Ages | School-Aged Children | ||||
% | n/N a | % | n/N | % | n/N | % | n/N | ||
Blue Nile | Aroaires | 8.0 | 41/510 | 12.5 | 33/265 | 0.4 | 2/510 | 0 | 0/265 |
Wad Al Mlahi | 0.8 | 6/735 | 1.6 | 5/306 | 0 | 0/735 | 0 | 0/306 | |
Gissan | 5.0 | 41/827 | 7.4 | 28/376 | 0.2 | 2/827 | 0.5 | 2/376 | |
Subtotal | 4.2 | 88/2072 | 7.0 | 66/947 | 0.2 | 4/2072 | 0.2 | 2/947 | |
Sennar | Sennar | 6.8 | 50/731 | 10.8 | 37/342 | 1.5 | 11/731 | 1.5 | 5/342 |
Al Sooki | 5.0 | 32/635 | 6.7 | 24/358 | 0.5 | 3/635 | 0.3 | 1/358 | |
East Sennar | 0.1 | 1/711 | 0.3 | 1/357 | 0.4 | 3/711 | 0.3 | 1/357 | |
Subtotal | 4.0 | 83/2077 | 5.9 | 62/1057 | 0.8 | 17/2077 | 0.7 | 7/1057 | |
North Kordofan | Al Rahud | 9.3 | 98/1053 | 11.4 | 64/560 | 0.3 | 3/1053 | 0.2 | 1/560 |
Um Rwaba | 2.5 | 26/1023 | 2.6 | 11/423 | 0.1 | 1/1023 | 0 | 0/423 | |
Subtotal | 6.0 | 124/2076 | 7.6 | 75/983 | 0.2 | 4/2076 | 0.1 | 1/983 | |
Total | 4.7 | 295/6225 | 6.8 | 203/2987 | 0.4 | 25/6225 | 0.3 | 10/2987 |
State | District | All Ages | School-Aged Children |
---|---|---|---|
Mean (SD a) | Mean (SD) | ||
Blue Nile | Aroaires | 19.3 (24.4) | 21.7 (26.5) |
Wad Al Mlahi | 14.7 (13.6) | 10.4 (9.8) | |
Gissan | 27.8 (45.7) | 29.5 (49.8) | |
Subtotal | 22.9 (35.6) | 24.2 (37.5) | |
Sennar | Sennar | 37.0 (65.8) | 38.3 (73.7) |
Alsooki | 59.8 (114.4) | 59.0 (114.6) | |
East Sennar | 9 (-) | 9.0 (-) | |
Subtotal | 45.4 (87.6) | 45.8 (91.0) | |
North Kordofan | Al Rahud | 16.8 (19.2) | 19.8 (21.1) |
Um Rwaba | 13.1 (17.4) | 19.2 (22.7) | |
Subtotal | 16.0 (18.8) | 16.7 (21.2) | |
Total | 26.4 (53.1) | 29.1 (57.0) |
Variables | % | n/N | Adjusted Odds Ratio a | 95% CI | p-Value | |
---|---|---|---|---|---|---|
Sex | Male | 6.1% | 163/2660 | 1.38 | 1.09–1.74 | 0.008 |
Female | 4.3% | 153/3565 | Ref | |||
Improved water source | No | 6.4% | 136/2122 | 1.58 | 1.24–2.01 | <0.001 |
Yes | 4.3% | 171/3981 | Ref | |||
Improved latrine b | No | 4.5% | 133/1967 | 1.63 | 1.05–2.55 | 0.03 |
Yes | 3.6% | 33/911 | Ref | |||
Latrine existence | No | 6.3% | 141/2225 | 1.53 | 1.20–1.94 | 0.001 |
Yes | 4.3% | 166/3878 | Ref | |||
Open defecation | Yes | 6.2% | 60/962 | 1.36 | 1.01–1.83 | 0.04 |
No | 4.9% | 256/5263 | Ref | |||
Water contact | Yes | 6.9% | 227/3301 | 2.12 | 1.70–2.88 | <0.001 |
No | 3.0% | 89/2924 | Ref | |||
School attendance | Out of school | 3.8% | 17/452 | 0.7 | 0.52–0.95 | 0.02 |
Attending school | 7.8% | 184/2364 | Ref | |||
Bloody urine | Yes | 23.1% | 87/376 | 7.16 | 5.40–9.49 | <0.001 |
No | 3.9% | 229/5849 | Ref |
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Ismail, H.A.H.A.; Cha, S.; Jin, Y.; Hong, S.-T. Programmatic Implications for Schistosomiasis Elimination Based on Community-Based Survey in the Blue Nile, North Kordofan, and Sennar States, Sudan. Life 2023, 13, 1049. https://doi.org/10.3390/life13041049
Ismail HAHA, Cha S, Jin Y, Hong S-T. Programmatic Implications for Schistosomiasis Elimination Based on Community-Based Survey in the Blue Nile, North Kordofan, and Sennar States, Sudan. Life. 2023; 13(4):1049. https://doi.org/10.3390/life13041049
Chicago/Turabian StyleIsmail, Hassan Ahmed Hassan Ahmed, Seungman Cha, Yan Jin, and Sung-Tae Hong. 2023. "Programmatic Implications for Schistosomiasis Elimination Based on Community-Based Survey in the Blue Nile, North Kordofan, and Sennar States, Sudan" Life 13, no. 4: 1049. https://doi.org/10.3390/life13041049