Optimizing Implementation of Preventive Chemotherapy against Soil-Transmitted Helminthiasis and Intestinal Schistosomiasis Using High-Resolution Data: Field-Based Experiences from Côte d’Ivoire
Abstract
:1. Introduction
2. Methods
2.1. Study Design
2.2. Study Area, Population and Sampling Design
2.3. Ethical Consideration
2.4. Field and Laboratory Procedures
2.5. Data Analysis
3. Results
3.1. Demographic Characteristics
3.2. Soil-Transmitted Helminthiasis
3.3. Intestinal Schistosomiasis
4. Discussion
4.1. Intestinal Schistosomiasis Is Hypoendemic in Investigated Health Districts
4.2. Spatial Heterogeneity of Soil-Transmitted Helminthiasis
4.3. Need for Sub-District Implementation of PC and How to Get There
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Pullan, R.L.; Smith, J.L.; Jasrasaria, R.; Brooker, S.J. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors 2014, 7, 37. [Google Scholar] [CrossRef]
- Lo, N.C.; Addiss, D.G.; Hotez, P.J.; King, C.H.; Stothard, J.R.; Evans, D.S.; Colley, D.G.; Lin, W.; Coulibaly, J.T.; Bustinduy, A.L.; et al. A call to strengthen the global strategy against schistosomiasis and soil-transmitted helminthiasis: The time is now. Lancet Infect. Dis. 2017, 17, e64–e69. [Google Scholar] [CrossRef]
- Bethony, J.; Brooker, S.; Albonico, M.; Geiger, S.M.; Loukas, A.; Diemert, D.; Hotez, P.J. Soil-transmitted helminth infections: Ascariasis, trichuriasis, and hookworm. Lancet 2006, 367, 1521–1532. [Google Scholar] [CrossRef]
- Hotez, P.J.; Bundy, D.A.P.; Beegle, K.; Brooker, S.; Drake, L.; de Silva, N.; Montresor, A.; Engels, D.; Jukes, M.; Chitsulo, L.; et al. Helminth infections: Soil-transmitted helminth infections and schistosomiasis. In Disease Control Priorities in Developing Countries; Jamison, D.T., Breman, J.G., Measham, A.R., Alleyne, G., Claeson, M., Evans, D.B., Jha, P., Mills, A., Musgrove, P., Eds.; The World Bank: Washington, DC, USA, 2006. [Google Scholar]
- Jourdan, P.M.; Lamberton, P.H.L.; Fenwick, A.; Addiss, D.G. Soil-transmitted helminth infections. Lancet 2018, 391, 252–265. [Google Scholar] [CrossRef]
- Ziegelbauer, K.; Speich, B.; Mäusezahl, D.; Bos, R.; Keiser, J.; Utzinger, J. Effect of sanitation on soil-transmitted helminth infection: Systematic review and meta-analysis. PLoS Med. 2012, 9, e1001162. [Google Scholar] [CrossRef]
- Geary, T.G.; Haque, M. Human Helminth Infections: A Primer. In Nutrition and Infectious Diseases: Shifting the Clinical Paradigm; Humphries, D.L., Scott, M.E., Vermund, S.H., Eds.; Springer International Publishing: Cham, Switzerland, 2021; pp. 189–215. [Google Scholar]
- WHO. Preventive Chemotherapy to Control Soil-Transmitted Helminth Infections in At-Risk Population Groups; World Health Organization: Geneva, Switzerland, 2017; pp. 15–45. [Google Scholar]
- Toor, J.; Alsallaq, R.; Truscott, J.E.; Turner, H.C.; Werkman, M.; Gurarie, D.; King, C.H.; Anderson, R.M. Are we on our way to achieving the 2020 goals for schistosomiasis morbidity control using current World Health Organization guidelines? Clin. Infect. Dis. 2018, 66, S245–S252. [Google Scholar] [CrossRef] [PubMed]
- WHO. Eliminating Soil-Transmitted Helminthiases As A Public Health Problem in Children: Progress Report 2001–2010 and Strategic Plan 2011–2020; World Health Organization: Geneva, Switzerland, 2012. [Google Scholar]
- Leslie, J.; Garba, A.; Oliva, E.B.; Barkire, A.; Tinni, A.A.; Djibo, A.; Mounkaila, I.; Fenwick, A. Schistosomiasis and soil-transmitted helminth control in Niger: Cost effectiveness of school based and community distributed mass drug administration. PLoS Negl. Trop. Dis. 2011, 5, e1326. [Google Scholar] [CrossRef] [PubMed]
- WHO. Accelerating Work to Overcome the Global Impact of Neglected Tropical Diseases: A Roadmap for Implementation; World Health Organization: Geneva, Switzerland, 2012. [Google Scholar]
- Bergquist, R.; Zhou, X.N.; Rollinson, D.; Reinhard-Rupp, J.; Klohe, K. Elimination of schistosomiasis: The tools required. Infect. Dis. Poverty 2017, 6, 158. [Google Scholar] [CrossRef]
- Faust, C.L.; Osakunor, D.N.M.; Downs, J.A.; Kayuni, S.; Stothard, J.R.; Lamberton, P.H.L.; Reinhard-Rupp, J.; Rollinson, D. Schistosomiasis control: Leave no age group behind. Trends Parasitol. 2020, 36, 582–591. [Google Scholar] [CrossRef]
- WHO. Reaching Girls and Women of Reproductive Age with Deworming: Report of the Advisory Group on Deworming in Girls and Women of Reproductive Age, Rockefeller Foundation Bellagio Center, Bellagio, Italy, 28–30 June 2017; World Health Organization: Geneva, Switzerland, 2017. [Google Scholar]
- WHO. Regional Strategy on Neglected Tropical Diseases in the WHO African Region 2014–2020; World Health Organization: Geneva, Switzerland, 2014. [Google Scholar]
- WHO. Ending the Neglect to Attain the Sustainable Development Goals: A Road Map for Neglected Tropical Diseases 2021–2030; World Health Organization: Geneva, Switzerland, 2020. [Google Scholar]
- WHO. Schistosomiasis: Progress Report 2001–2011, Strategic Plan 2012–2020; World Health Organization: Geneva, Switzerland, 2013. [Google Scholar]
- Fornace, K.M.; Fronterre, C.; Fleming, F.M.; Simpson, H.; Zoure, H.; Rebollo, M.; Mwinzi, P.; Vounatsou, P.; Pullan, R.L. Evaluating survey designs for targeting preventive chemotherapy against Schistosoma haematobium and Schistosoma mansoni across sub-Saharan Africa: A geostatistical analysis and modelling study. Parasit Vectors 2020, 13, 555. [Google Scholar] [CrossRef]
- King, C.H.; Kittur, N.; Binder, S.; Campbell, C.H.; N’Goran, E.K.; Meite, A.; Utzinger, J.; Olsen, A.; Magnussen, P.; Kinung’hi, S.; et al. Impact of different mass drug administration strategies for gaining and sustaining control of Schistosoma mansoni and Schistosoma haematobium infection in Africa. Am. J. Trop. Med. Hyg. 2020, 103, 14–23. [Google Scholar] [CrossRef] [PubMed]
- ESPEN. Accelerating Elimination of NTDs—Towards 2030. Available online: https://espen.afro.who.int/ (accessed on 12 June 2021).
- Patel, C.; Hürlimann, E.; Keller, L.; Hattendorf, J.; Sayasone, S.; Ali, S.M.; Ame, S.M.; Coulibaly, J.T.; Keiser, J. Efficacy and safety of ivermectin and albendazole co-administration in school-aged children and adults infected with Trichuris trichiura: Study protocol for a multi-country randomized controlled double-blind trial. BMC Infect. Dis. 2019, 19, 262. [Google Scholar] [CrossRef] [PubMed]
- Yapi, R.B.; Hürlimann, E.; Houngbedji, C.A.; N’Dri, P.B.; Silué, K.D.; Soro, G.; Kouame, F.N.; Vounatsou, P.; Fürst, T.; N’Goran, E.K.; et al. Infection and co-infection with helminths and Plasmodium among school children in Côte d’Ivoire: Results from a national cross-sectional survey. PLoS Negl. Trop. Dis. 2014, 8, e2913. [Google Scholar] [CrossRef] [PubMed]
- WHO. Preventive Chemotherapy in Human Helminthiasis: Coordinated Use of Anthelminthic Drugs in Control Interventions; World Health Organization: Geneva, Switzerland, 2006. [Google Scholar]
- Coulibaly, J.T.; Knopp, S.; N’Guessan, N.A.; Silué, K.D.; Fürst, T.; Lohourignon, L.K.; Brou, J.K.; N’Gbesso, Y.K.; Vounatsou, P.; N’Goran, E.K.; et al. Accuracy of urine circulating cathodic antigen (CCA) test for Schistosoma mansoni diagnosis in different settings of Côte d’Ivoire. PLoS Negl. Trop. Dis. 2011, 5, e1384. [Google Scholar] [CrossRef] [PubMed]
- Katz, N.; Chaves, A.; Pellegrino, J. A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Rev. Inst. Med. Trop. São Paulo 1972, 14, 397–400. [Google Scholar] [PubMed]
- Keiser, J.; Utzinger, J. Efficacy of current drugs against soil-transmitted helminth infections: Systematic review and meta-analysis. JAMA 2008, 299, 1937–1948. [Google Scholar] [CrossRef] [PubMed]
- Marocco, C.; Bangert, M.; Joseph, S.A.; Fitzpatrick, C.; Montresor, A. Preventive chemotherapy in one year reduces by over 80% the number of individuals with soil-transmitted helminthiases causing morbidity: Results from meta-analysis. Trans. R Soc. Trop. Med. Hyg. 2017, 111, 12–17. [Google Scholar] [CrossRef]
- Truscott, J.E.; Hardwick, R.J.; Werkman, M.; Saravanakumar, P.K.; Manuel, M.; Ajjampur, S.S.R.; Asbjornsdottir, K.H.; Khumbo, K.; Witek-McManus, S.; Simwanza, J.; et al. Forecasting the effectiveness of the DeWorm3 trial in interrupting the transmission of soil-transmitted helminths in three study sites in Benin, India and Malawi. Parasit Vectors 2021, 14, 67. [Google Scholar] [CrossRef]
- WHO. Expanded Special Project for Elimination of Neglected Tropical Diseases. 2020 Annual Report.; World Health Organization: Geneva, Switzerland, 2020. [Google Scholar]
- Chammartin, F.; Houngbedji, C.A.; Hürlimann, E.; Yapi, R.B.; Silué, K.D.; Soro, G.; Kouamé, F.N.; EK, N.G.; Utzinger, J.; Raso, G.; et al. Bayesian risk mapping and model-based estimation of Schistosoma haematobium-Schistosoma mansoni co-distribution in Côte d’Ivoire. PLoS Negl. Trop. Dis. 2014, 8, e3407. [Google Scholar] [CrossRef]
- Coulibaly, J.T.; N’Gbesso, Y.K.; N’Guessan, N.A.; Winkler, M.S.; Utzinger, J.; N’Goran, E.K. Epidemiology of schistosomiasis in two high-risk communities of south Côte d’Ivoire with particular emphasis on pre-school-aged children. Am. J. Trop. Med. Hyg. 2013, 89, 32–41. [Google Scholar] [CrossRef]
- Assaré, R.K.; Hürlimann, E.; Ouattara, M.; N’Guessan, N.A.; Tian-Bi, Y.N.; Yapi, A.; Yao, P.K.; Coulibaly, J.T.; Knopp, S.; N’Goran, E.K.; et al. Sustaining the control of Schistosoma mansoni in western Côte d’Ivoire: Baseline findings before the implementation of a randomized trial. Am. J. Trop. Med. Hyg. 2016, 94, 352–360. [Google Scholar] [CrossRef] [PubMed]
- Walz, Y.; Wegmann, M.; Dech, S.; Vounatsou, P.; Poda, J.N.; N’Goran, E.K.; Utzinger, J.; Raso, G. Modeling and validation of environmental suitability for schistosomiasis transmission using remote sensing. PLoS Negl. Trop. Dis. 2015, 9, e0004217. [Google Scholar] [CrossRef] [PubMed]
- Fuss, A.; Mazigo, H.D.; Mueller, A. Evaluation of serum-based real-time PCR to detect Schistosoma mansoni infection before and after treatment. Infect. Dis. Poverty 2020, 9, 74. [Google Scholar] [CrossRef] [PubMed]
- WHO. WHO Guideline on Control and Elimination of Human Schistosomiasis; World Health Organization: Geneva, Switzerland, 2022. [Google Scholar]
- Koudou, B.G.; Kouakou, M.M.; Ouattara, A.F.; Yeo, S.; Brika, P.; Meite, A.; Aba, E.; King, C.L.; Kouakou, R.; Weil, G.J.; et al. Update on the current status of onchocerciasis in Côte d’Ivoire following 40 years of intervention: Progress and challenges. PLoS Negl. Trop. Dis. 2018, 12, e0006897. [Google Scholar] [CrossRef]
- Loukouri, A.; Meite, A.; Koudou, B.G.; Goss, C.W.; Lew, D.; Weil, G.J.; N’Goran, E.K.; Fischer, P.U. Impact of annual and semi-annual mass drug administration for lymphatic filariasis and onchocerciasis on hookworm infection in Côte d’Ivoire. PLoS Negl. Trop. Dis. 2020, 14, e0008642. [Google Scholar] [CrossRef]
- Nath, T.C.; Padmawati, R.S.; Murhandarwati, E.H. Barriers and gaps in utilization and coverage of mass drug administration program against soil-transmitted helminth infection in Bangladesh: An implementation research. J. Infect. Public Health 2019, 12, 205–212. [Google Scholar] [CrossRef]
- Hardwick, R.J.; Truscott, J.E.; Oswald, W.E.; Werkman, M.; Halliday, K.E.; Pullan, R.L.; Anderson, R.M. Individual adherence to mass drug administration in neglected tropical disease control: A probability model conditional on past behaviour. PLoS Negl. Trop. Dis. 2021, 15, e0009112. [Google Scholar] [CrossRef]
- Kwong, L.H.; Sen, D.; Islam, S.; Shahriar, S.; Benjamin-Chung, J.; Arnold, B.F.; Hubbard, A.; Parvez, S.M.; Islam, M.; Unicomb, L.; et al. Effect of sanitation improvements on soil-transmitted helminth eggs in courtyard soil from rural Bangladesh: Evidence from a cluster-randomized controlled trial. PLoS Negl. Trop. Dis. 2021, 15, e0008815. [Google Scholar] [CrossRef]
- Brooker, S.J.; Nikolay, B.; Balabanova, D.; Pullan, R.L. Global feasibility assessment of interrupting the transmission of soil-transmitted helminths: A statistical modelling study. Lancet Infect. Dis. 2015, 15, 941–950. [Google Scholar] [CrossRef]
- Ruberanziza, E.; Owada, K.; Clark, N.J.; Umulisa, I.; Ortu, G.; Lancaster, W.; Munyaneza, T.; Mbituyumuremyi, A.; Bayisenge, U.; Fenwick, A.; et al. Mapping soil-transmitted helminth parasite infection in Rwanda: Estimating endemicity and identifying at-risk populations. Trop. Med. Infect. Dis. 2019, 4, 93. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hürlimann, E.; Keller, L.; Patel, C.; Welsche, S.; Hattendorf, J.; Ali, S.M.; Ame, S.M.; Sayasone, S.; Coulibaly, J.T.; Keiser, J. Efficacy and safety of co-administered ivermectin and albendazole in school-aged children and adults infected with Trichuris trichiura in Côte d’Ivoire, Laos, and Pemba Island, Tanzania: A double-blind, parallel-group, phase 3, randomised controlled trial. Lancet Infect. Dis. 2021, 22, 123–135. [Google Scholar] [CrossRef]
- Tchuem Tchuente, L.A.; Stothard, J.R.; Rollinson, D.; Reinhard-Rupp, J. Precision mapping: An innovative tool and way forward to shrink the map, better target interventions, and accelerate toward the elimination of schistosomiasis. PLoS Negl. Trop. Dis. 2018, 12, e0006563. [Google Scholar] [CrossRef] [PubMed]
- Papaiakovou, M.; Wright, J.; Pilotte, N.; Chooneea, D.; Schar, F.; Truscott, J.E.; Dunn, J.C.; Gardiner, I.; Walson, J.L.; Williams, S.A.; et al. Pooling as a strategy for the timely diagnosis of soil-transmitted helminths in stool: Value and reproducibility. Parasit Vectors 2019, 12, 443. [Google Scholar] [CrossRef] [PubMed]
- Truscott, J.E.; Dunn, J.C.; Papaiakovou, M.; Schaer, F.; Werkman, M.; Littlewood, D.T.J.; Walson, J.L.; Anderson, R.M. Calculating the prevalence of soil-transmitted helminth infection through pooling of stool samples: Choosing and optimizing the pooling strategy. PLoS Negl. Trop. Dis. 2019, 13, e0007196. [Google Scholar] [CrossRef] [Green Version]
Parasite Species | Dabou (N = 2174) | Jacqueville (N = 2164) | ||
---|---|---|---|---|
No. of Infected Children (%) | 95% CI | No. of Infected Children (%) | 95% CI | |
Intestinal Schistosomiasis | ||||
S. mansoni | 16 (0.74) | 0.38–1.10 | 10 (0.46) | 0.18–0.75 |
Soil-Transmitted Helminths (STHs) | ||||
Trichuris trichiura | 197 (9.06) | 7.85–10.27 | 160 (7.39) | 6.29–8.50 |
Ascaris lumbricoides | 68 (3.13) | 2.40–3.86 | 130 (6.01) | 5.01–7.01 |
Hookworm | 50 (2.30) | 1.67–2.93 | 11 (0.51) | 0.21–0.81 |
Any STH | 271 (12.47) | 11.08–13.86 | 240 (11.09) | 9.77–12.41 |
S. mansoni | Trichuris trichiura | Ascaris lumbricoides | Hookworm | Any STH | |||||||
---|---|---|---|---|---|---|---|---|---|---|---|
Sub-District | No. Examined | No. Infected | % | No. Infected | % | No. Infected | % | No. Infected | % | No. Infected | % |
Dabou | |||||||||||
Ahouya | 297 | 3 | 1.01 | 94 | 31.65 | 34 | 11.45 | 14 | 4.71 | 113 | 38.05 |
Yassap | 131 | 1 | 0.76 | 23 | 17.56 | 2 | 1.53 | 9 | 6.87 | 29 | 22.14 |
Opoyounem | 175 | 1 | 0.57 | 34 | 19.43 | 1 | 0.57 | 6 | 3.43 | 37 | 21.14 |
Toupah | 120 | 3 | 2.50 | 1 | 0.83 | 16 | 13.33 | 0 | 0.00 | 17 | 14.17 |
Nouvel Ousrou | 60 | 1 | 1.67 | 7 | 11.67 | 1 | 1.67 | 2 | 3.33 | 8 | 13.33 |
Vieil Alkodj | 60 | 0 | 0.00 | 3 | 5.00 | 3 | 5.00 | 2 | 3.33 | 8 | 13.33 |
N’Gatty | 111 | 0 | 0.00 | 8 | 7.21 | 2 | 1.80 | 2 | 1.80 | 11 | 9.91 |
Bonn | 172 | 0 | 0.00 | 4 | 2.33 | 5 | 2.91 | 7 | 4.07 | 16 | 9.30 |
Nigui Nanou | 57 | 0 | 0.00 | 5 | 8.77 | 0 | 0.00 | 1 | 1.75 | 5 | 8.77 |
Lopou | 52 | 2 | 3.85 | 2 | 3.85 | 1 | 1.92 | 0 | 0.00 | 3 | 5.77 |
Dabou | 118 | 1 | 0.85 | 6 | 5.08 | 0 | 0.00 | 0 | 0.00 | 6 | 5.08 |
Armébé | 60 | 2 | 3.33 | 0 | 0.00 | 0 | 0.00 | 3 | 5.00 | 3 | 5.00 |
Petit Badjen | 60 | 0 | 0.00 | 1 | 1.67 | 2 | 3.33 | 0 | 0.00 | 3 | 5.00 |
Bouboury | 180 | 0 | 0.00 | 6 | 3.33 | 0 | 0.00 | 0 | 0.00 | 6 | 3.33 |
Panda | 120 | 0 | 0.00 | 2 | 1.67 | 1 | 0.83 | 3 | 2.50 | 4 | 3.33 |
Savane | 176 | 0 | 0.00 | 1 | 0.57 | 0 | 0.00 | 1 | 0.57 | 2 | 1.14 |
CNRA | 60 | 0 | 0.00 | 0 | 0.00 | 0 | 0.00 | 0 | 0.00 | 0 | 0.00 |
Orbaff | 105 | 2 | 1.90 | 0 | 0.00 | 0 | 0.00 | 0 | 0.00 | 0 | 0.00 |
Pass | 60 | 0 | 0.00 | 0 | 0.00 | 0 | 0.00 | 0 | 0.00 | 0 | 0.00 |
Total Dabou | 2174 | 16 | 0.74 | 197 | 9.06 | 68 | 3.13 | 50 | 2.30 | 271 | 12.47 |
Jacqueville | |||||||||||
Tiagba | 52 | 0 | 0.00 | 47 | 90.38 | 36 | 69.23 | 0 | 0.00 | 49 | 94.23 |
Kouvé | 271 | 0 | 0.00 | 72 | 26.57 | 38 | 14.02 | 2 | 0.74 | 89 | 32.84 |
Nigui Assoko | 60 | 0 | 0.00 | 1 | 1.67 | 9 | 15.00 | 0 | 0.00 | 9 | 15.00 |
Tiegba | 60 | 2 | 3.33 | 8 | 13.33 | 1 | 1.67 | 0 | 0.00 | 9 | 15.00 |
Abraco | 120 | 0 | 0.00 | 2 | 1.67 | 10 | 8.33 | 0 | 0.00 | 12 | 10.00 |
Nigui Saff | 59 | 0 | 0.00 | 4 | 6.78 | 1 | 1.69 | 0 | 0.00 | 5 | 8.47 |
Attoutou B | 154 | 2 | 1.30 | 3 | 1.95 | 5 | 3.25 | 3 | 1.95 | 11 | 7.14 |
Jacqueville | 357 | 1 | 0.28 | 0 | 0.00 | 21 | 5.88 | 0 | 0.00 | 21 | 5.88 |
Addah | 295 | 0 | 0.00 | 6 | 2.03 | 6 | 2.03 | 2 | 0.68 | 14 | 4.75 |
Adessé | 170 | 0 | 0.00 | 7 | 4.12 | 0 | 0.00 | 1 | 0.59 | 8 | 4.71 |
Attoutou A | 53 | 1 | 1.89 | 2 | 3.77 | 2 | 3.77 | 0 | 0.00 | 2 | 3.77 |
Irobo | 180 | 3 | 1.67 | 5 | 2.78 | 0 | 0.00 | 2 | 1.11 | 6 | 3.33 |
Sassako | 120 | 1 | 0.83 | 1 | 0.83 | 1 | 0.83 | 1 | 0.83 | 3 | 2.50 |
Avagou | 213 | 0 | 0.00 | 2 | 0.94 | 0 | 0.00 | 0 | 0.00 | 2 | 0.94 |
Total Jacqueville | 2164 | 10 | 0.46 | 160 | 7.39 | 130 | 6.01 | 11 | 0.51 | 240 | 11.09 |
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Coulibaly, J.T.; Hürlimann, E.; Patel, C.; Silué, D.K.; Avenié, D.J.; Kouamé, N.A.; Silué, U.M.; Keiser, J. Optimizing Implementation of Preventive Chemotherapy against Soil-Transmitted Helminthiasis and Intestinal Schistosomiasis Using High-Resolution Data: Field-Based Experiences from Côte d’Ivoire. Diseases 2022, 10, 66. https://doi.org/10.3390/diseases10040066
Coulibaly JT, Hürlimann E, Patel C, Silué DK, Avenié DJ, Kouamé NA, Silué UM, Keiser J. Optimizing Implementation of Preventive Chemotherapy against Soil-Transmitted Helminthiasis and Intestinal Schistosomiasis Using High-Resolution Data: Field-Based Experiences from Côte d’Ivoire. Diseases. 2022; 10(4):66. https://doi.org/10.3390/diseases10040066
Chicago/Turabian StyleCoulibaly, Jean T., Eveline Hürlimann, Chandni Patel, Dieudonné K. Silué, Deles J. Avenié, Nadège A. Kouamé, Ulrich M. Silué, and Jennifer Keiser. 2022. "Optimizing Implementation of Preventive Chemotherapy against Soil-Transmitted Helminthiasis and Intestinal Schistosomiasis Using High-Resolution Data: Field-Based Experiences from Côte d’Ivoire" Diseases 10, no. 4: 66. https://doi.org/10.3390/diseases10040066
APA StyleCoulibaly, J. T., Hürlimann, E., Patel, C., Silué, D. K., Avenié, D. J., Kouamé, N. A., Silué, U. M., & Keiser, J. (2022). Optimizing Implementation of Preventive Chemotherapy against Soil-Transmitted Helminthiasis and Intestinal Schistosomiasis Using High-Resolution Data: Field-Based Experiences from Côte d’Ivoire. Diseases, 10(4), 66. https://doi.org/10.3390/diseases10040066