Modeling and Validation of Environmental Suitability for Schistosomiasis Transmission Using Remote Sensing

PLoS Neglected Tropical Diseases

Volumn 9, Issue 11, 2015, Pages

  Walz, Yvonne ^a,b   Wegmann, Martin ^a   Dech, Stefan ^a,c   Vounatsou, Penelope ^d,e   Poda, Jean Noël ^f   N'Goran, Eliézer K ^g,h   Utzinger, Jürg ^d,e   Raso, Giovanna ^d,e  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNITED NATIONS UNIVERSITY   (Germany)

^c GERMAN AEROSPACE CENTER DLR   (Germany)

^d SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^e UNIVERSITY OF BASEL   (Switzerland)

^f Public Health Research Institute for Health Sciences   (Burkina Faso)

^g UNIVERSITÉ FÉLIX HOUPHOUËT BOIGNY   (Côte d’Ivoire)

^h CENTRE SUISSE DE RECHERCHES SCIENTIFIQUES EN CÔTE D'IVOIRE   (Côte d’Ivoire)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CORRELATION COEFFICIENT; DISEASE CONTROL; DISEASE SURVEILLANCE; DISEASE TRANSMISSION; ENVIRONMENTAL ASPECTS AND RELATED PHENOMENA; ENVIRONMENTAL FACTOR; ENVIRONMENTAL IMPACT; ENVIRONMENTAL SUITABILITY; ENVIRONMENTAL TEMPERATURE; HEALTH CARE SURVEY; INFECTION PREVENTION; INFORMATION PROCESSING; MATHEMATICAL MODEL; NONHUMAN; RADIATION DETECTOR; REMOTE SENSING; SCHISTOSOMIASIS; SPECIES DISTRIBUTION; SPECIES HABITAT; THERMAL EMISSION AND REFLECTION RADIOMETER; TOPOGRAPHY; VALIDATION PROCESS; WATER AVAILABILITY; ADOLESCENT; BURKINA FASO; CHILD; COTE D'IVOIRE; ECOSYSTEM; EPIDEMIOLOGY; HUMAN; PROCEDURES; STATISTICAL MODEL; TRANSMISSION; VALIDATION STUDY;

ADOLESCENT; BURKINA FASO; CHILD; COTE D'IVOIRE; ECOSYSTEM; EPIDEMIOLOGIC METHODS; HUMANS; MODELS, STATISTICAL; REMOTE SENSING TECHNOLOGY; SCHISTOSOMIASIS;

EID: 84949506603     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0004217     Document Type: Article

References (106)

1. Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J, (2006) Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis6: 411–425. 16790382
2. WHO (2002) Prevention and control of schistosomiasis and soil-transmitted helminthiasis: a report of a WHO expert committee. WHO Tech Rep Ser912: 1–57.
3. Doenhoff MJ, Hagan P, Cioli D, Southgate V, Pica-Mattoccia L, et al. (2009) Praziquantel: its use in control of schistosomiasis in sub-Saharan Africa and current research needs. Parasitology136: 1825–1835. doi: 10.1017/S003118200900049319281637
4. Utzinger J, Bergquist R, Xiao SH, Singer BH, Tanner M, (2003) Sustainable schistosomiasis control—the way forward. Lancet362: 1932–1934. 14667754
5. Clements ACA, Bosqué-Oliva E, Sacko M, Landouré A, Dembélé R, et al. (2009) A comparative study of the spatial distribution of schistosomiasis in Mali in 1984–1989 and 2004–2006. PLoS Negl Trop Dis3: e431. doi: 10.1371/journal.pntd.000043119415108
6. Zhang Z, Zhu R, Ward MP, Xu W, Zhang L, et al. (2012) Long-term impact of the World Bank Loan Project for schistosomiasis control: a comparison of the spatial distribution of schistosomiasis risk in China. PLoS Negl Trop Dis6: e1620. doi: 10.1371/journal.pntd.000162022530073
7. Stothard JR, Chitsulo L, Kristensen TK, Utzinger J, (2009) Control of schistosomiasis in sub-Saharan Africa: progress made, new opportunities and remaining challenges. Parasitology136: 1665–1675. doi: 10.1017/S003118200999127219814845
8. Utzinger J, N'Goran EK, Caffrey CR, Keiser J, (2011) From innovation to application: social-ecological context, diagnostics, drugs and integrated control of schistosomiasis. Acta Trop120 (Suppl 1): S121–S137. doi: 10.1016/j.actatropica.2010.08.02020831855
9. Rollinson D, Knopp S, Levitz S, Stothard JR, Tchuem Tchuenté L-A, et al. (2013) Time to set the agenda for schistosomiasis elimination. Acta Trop128: 423–440. doi: 10.1016/j.actatropica.2012.04.01322580511
10. Kalluri S, Gilruth P, Rogers D, Szczur M, (2007) Surveillance of arthropod vector-borne infectious diseases using remote sensing techniques: a review. PLoS Pathog3: e116.
11. Hay SI, Packer MJ, Rogers DJ, (1997) The impact of remote sensing on the study and control of invertebrate intermediate hosts and vectors for disease. Int J Remote Sens18: 2899–2930.
12. Beck LR, Lobitz BM, Wood BL, (2000) Remote sensing and human health: new sensors and new opportunities. Emerg Infect Dis6: 217–226. 10827111
13. Hay SI, Randolph SE, Rogers DJ, (2000) Remote sensing and geographical information systems in epidemiology—guest editors´ preface. Adv Parasitol47: xi–xii.
14. Brooker S, (2002) Schistosomes, snails and satellites. Acta Trop82: 207–214. 12020894
15. Yang GJ, Vounatsou P, Zhou XN, Utzinger J, Tanner M, (2005) A review of geographic information system and remote sensing with applications to the epidemiology and control of schistosomiasis in China. Acta Trop96: 117–129. 16112638
16. Simoonga C, Utzinger J, Brooker S, Vounatsou P, Appleton CC, et al. (2009) Remote sensing, geographical information system and spatial analysis for schistosomiasis epidemiology and ecology in Africa. Parasitology136: 1683–1693. doi: 10.1017/S003118200900622219627627
17. Tran A, Goutard F, Chamaillé L, Baghdadi N, Lo Seen D, (2010) Remote sensing and avian influenza: a review of image processing methods for extracting key variables affecting avian influenza virus survival in water from Earth observation satellites. Int J Appl Earth Obs Geoinf12: 1–8.
18. Seto E, Xu B, Liang S, Gong P, Wu W, et al. (2002) The use of remote sensing for predictive modeling of schistosomiasis in China. Photogramm Eng Remote Sens68: 167–174.
19. Stensgaard AS, Jorgensen A, Kabatereine NB, Malone JB, Kristensen TK, (2005) Modeling the distribution of Schistosoma mansoni and host snails in Uganda using satellite sensor data and geographical information systems. Parassitologia47: 115–125. 16044680
20. Brooker S, (2007) Spatial epidemiology of human schistosomiasis in Africa: risk models, transmission dynamics and control. Trans R Soc Trop Med Hyg101: 1–8. 17055547
21. Walz Y, Wegmann M, Dech S, Raso G, Utzinger J, (2015) Risk profiling of schistosomiasis using remote sensing: approaches, challenges and outlook. Parasit Vectors8: 163. doi: 10.1186/s13071-015-0732-625890278
22. Moodley I, Kleinschmidt I, Sharp B, Craig M, Appleton C, (2003) Temperature-suitability maps for schistosomiasis in South Africa. Ann Trop Med Parasitol97: 617–627. 14511560
23. Stensgaard AS, Jorgensen A, Kabatereine NB, Rahbek C, Kristensen TK, (2006) Modeling freshwater snail habitat suitability and areas of potential snail-borne disease transmission in Uganda. Geospat Health1: 93–104. 18686235
24. Stensgaard AS, Utzinger J, Vounatsou P, Hürlimann E, Schur N, et al. (2013) Large-scale determinants of intestinal schistosomiasis and intermediate host snail distribution across Africa: does climate matter?Acta Trop128: 378–390. doi: 10.1016/j.actatropica.2011.11.01022142789
25. Guo JG, Vounatsou P, Cao CL, Utzinger J, Zhu HQ, et al. (2005) A geographic information and remote sensing based model for prediction of Oncomelania hupensis habitats in the Poyang Lake area, China. Acta Trop96: 213–222. 16140246
26. Yang GJ, Vounatsou P, Tanner M, Zhou XN, Utzinger J, (2006) Remote sensing for predicting potential habitats of Oncomelania hupensis in Hongze, Baima and Gaoyou lakes in Jiangsu province, China. Geospat Health1: 85–92. 18686234
27. Zhang Z, Bergquist R, Chen D, Yao B, Wang Z, et al. (2013) Identification of parasite-host habitats in Anxiang county, Hunan province, China based on multi-temporal China-Brazil Earth Resources Satellite (CBERS) images. PLoS One8: e69447. doi: 10.1371/journal.pone.006944723922712
28. Poda JN, Sawadogo LL, Sellin B, Sanogo S, (1996) Dynamique des populations de Bulinus truncatus rohlfsi Clessin, 1886, dans le barrage de Dyoro en zone nord-soudanienne du Burkina Faso. Rev Agronom Afr8: 61–68. (in French).
29. Poda JN, Sellin B, Sawadogo L, (1994) Dynamique des populations de Bulinus senegalensis, MULLER, 1781, dans une mare temporaire de la zone nord-soudanienne du Burkina Faso. Rev Elev Méd Vét Pays Trop47: 375–378. (in French).
30. Abdel-Malek E, (1958) Factors conditioning the habitat of bilharziasis intermediate hosts of the family Planorbidae. Bull World Health Organ18: 785–818. 13573113
31. Shiff CJ, (1964) Studies on Bulinus (Physopsis) globosus in Rhodesia. I The influence of temperature on the intrinsic rate of natural increase. Ann Trop Med Parasitol58: 94–105. 14149705
32. Shiff CJ, Garnett B, (1967) The influence of temperature on the intrinsic rate of natural increase of the freshwater snail B. pfeifferi. Arch Hydrobiol62: 429–438.
33. Appleton CC, (1978) Review of the literature on abiotic factors influencing the distribution and life-cycles of bilharziasis intermediate host snails. Malacol Rev11: 1–25.
34. Pflüger W, (1980) Experimental epidemiology of schistosomiasis. I. The prepatent period and cercarial production of Schistosoma mansoni in Biomphalaria snails at various constant temperatures. Z Parasitenkd63: 159–169. 7456642
35. Pflüger W, Roushdy MZ, El Emam M, (1984) The prepatent period and cercarial production of Schistosoma haematobium in Bulinus truncatus (Egyptian field strains) at different constant temperatures. Z Parasitenkd70: 95–103. 6695537
36. Malone JB, (2005) Biology-based mapping of vector-borne parasites by geographic information systems and remote sensing. Parassitologia47: 27–50. 16044674
37. Kearney M, (2006) Habitat, environment and niche: what are we modelling?Oikos115: 186–191.
38. USFWS (1981) Standards for the development of habitat suitability index models. Washington D.C.: United States Fish and Wildlife Service.
39. USFWS (2014) USGS National Wetlands Research Center Digital Library: Habitat Suitability Index Models. Biological Report: U.S. Department of the Interior, U.S. Geological Survey.
40. Brown SK, Buja KR, Jury SH, Monaco ME, Banner A, (2000) Habitat suitability index models for eight fish and invertebrate species in Casco and Sheepscot Bays, Maine. North Am J Fish Manag20: 408–435.
41. Vinagre C, Fonseca V, Cabral H, Costa MJ, (2006) Habitat suitability index models for the juvenile soles, Solea solea and Solea senegalensis, in the Tagus estuary: defining variables for species management. Fish Res82: 140–149.
42. Thomasma LE, Drummer TD, Peterson RO, (1991) Testing the habitat suitability index model for the fisher. Wildlife Soc B19: 291–297.
43. Mitchell MS, Zimmerman JW, Powell RA, (2002) Test of a habitat suitability index for black bears in the southern Appalachians. Wildlife Soc B30: 794–808.
44. Dussault C, Courtois R, Ouellet J-P, (2006) A habitat suitability index model to assess moose habitat selection at multiple spatial scales. Can J For Res36: 1097–1107.
45. Store R, Kangas J, (2001) Integrating spatial multi-criteria evaluation and expert knowledge for GIS-based habitat suitability modelling. Landscape Urban Plan55: 79–93.
46. Rüger N, Schlüter M, Matthies M, (2005) A fuzzy habitat suitability index for Populus euphratica in the northern Amudarya delta (Uzbekistan). Ecol Model184: 313–328.
47. Williams NSG, Hahs AK, Morgan JW, (2008) A dispersal-constrained habitat suitability model for predicting invasion of alpine vegetation. Ecol Appl18: 347–359. 18488601
48. Duncan BW, Breininger DR, Schmalzer PA, Larson VL, (1995) Validating Florida scrub jay habitat suitability model, using demography data on Kennedy Space Center. Photogramm Eng Remote Sens11: 1361–1370.
49. Schamberger ML, O´Neil LJ, Verner J, Morrison ML, Ralph CJ, (1986) Concepts and constraints of habitat-model testing. In: Wildlife 2000: Modelling habitat relationships of terrestrial vertebrates. Wisconsin, USA: University of Wisconsin Press. pp. 5–10.
50. Brooks RP, (1997) Improving habitat suitability index models. Wildl Soc Bull25: 163–167.
51. Ortigosa GR, De Leo GA, Gatto M, (2000) VVF: integrating modelling and GIS in a software tool for habitat suitability assessment. Environ Model Softw15: 1–12.
52. Brasseur P, Drhuile P, (1984) [Geographic dispersion of bilharzial endemy in 3 departments of Burkina Faso (ex-Upper Volta)]. Bull Soc Pathol Exot Filiales77: 673–677. (in French). 6543159
53. Garba A, Campagne G, Poda JN, Parent G, Kambire R, et al. (1999) [Schistosomiasis in the region of Ziga (Burkina Faso) before the construction of a dam]. Bull Soc Pathol Exot92: 195–197. (in French). 10472448
54. Utzinger J, N'Goran EK, Ossey YA, Booth M, Traore M, et al. (2000) Rapid screening for Schistosoma mansoni in western Côte d'Ivoire using a simple school questionnaire. Bull World Health Organ78: 389–398. 10812739
55. Raso G, Matthys B, N'Goran EK, Tanner M, Vounatsou P, et al. (2005) Spatial risk prediction and mapping of Schistosoma mansoni infections among schoolchildren living in western Côte d'Ivoire. Parasitology131: 97–108. 16038401
56. N'Goran EK, Diabate S, Utzinger J, Sellin B, (1997) Changes in human schistosomiasis levels after the construction of two large hydroelectric dams in central Côte d'Ivoire. Bull World Health Organ75: 541–545. 9509626
57. N'Goran EK, Utzinger J, Traorée M, Lengeler C, Tanner M, (1998) [Use of a questionnaire for quick identification of the principal foci of urinary bilharziasis in central Ivory Coast]. Med Trop (Mars)58: 253–260. (in French).
58. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A, (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol25: 1965–1978.
59. Dipama JM (2010) The biophysical environment: hydrology. In: Thiombiano A, Kampmann D, editors. Biodiversity Atlas of West Africa, Volume II: Burkina Faso. Ouagadougou Frankfurt/Main.
60. Savane I (2010) The biophysical environment: water resources. In: Konaté S, Kampmann D, editors. Biodiversity Atlas of West Africa, Volume III: Côte d'Ivoire. Abidjan Frankfurt/Main.
61. WHO (2010) Schistosomiasis control at a glance. World Health Organization—Regional Office for Africa. pp. 2.
62. Assaré RK, Lai Y-S, Yapi A, Tian-Bi YNT, Ouattara M, et al. (2015) The spatial distribution of Schistosoma mansoni infection in four regions of western Côte d’Ivoire. Geospat Health10: 69–79.
63. Hürlimann E, Schur N, Boutsika K, Stensgaard AS, Laserna de Himpsl M, et al. (2011) Toward an open-access global database for mapping, control, and surveillance of neglected tropical diseases. PLoS Negl Trop Dis5: e1404. doi: 10.1371/journal.pntd.000140422180793
64. Poda JN (1996) Spatial distribution of intermediate hosts of schistosomes in Burkina Faso: factors influencing the dynamics of Bulinus truncatus rohlfsi and Bulinus senegalensis [PhD thesis]: University of Ouagadougou.
65. Kinanpara K, Yves BK, Félix KK, Edia EO, Théophile G, et al. (2013) Freshwater snail dynamics focused on potential risk of using urine as fertilizer in Katiola, an endemic area of schistosomiasis (Ivory Coast; West Africa). J Entomol Zool Stud1: 110–115.
66. Boelee E, Cecchi P, Kone A, (2009) Health impacts of small reservoirs in Burkina Faso. Colombo: International Water Management Institute. 50 p.
67. Fenwick A, Webster JP, Bosque-Oliva E, Blair L, Fleming FM, et al. (2009) The Schistosomiasis Control Initiative (SCI): rationale, development and implementation from 2002–2008. Parasitology136: 1719–1730. doi: 10.1017/S003118200999040019631008
68. MoH, PNLSc (2010) Plan d’action 2011 du programme national de lutte contre les schistosomoses. Ouagadougou: Ministère de la Santé Burkina Faso—Programme National de Lutte contre les Schistosomoses.
69. Tchuem Tchuenté LA, N'Goran EK, (2009) Schistosomiasis and soil-transmitted helminthiasis control in Cameroon and Côte d'Ivoire: implementing control on a limited budget. Parasitology136: 1739–1745. doi: 10.1017/S003118200900598819490723
70. Blackbridge (2015) Satellite Imagery Product Specifications. Berlin.
71. Richter R, Schläpfer D, (2012) Atmospheric / topographic correction for airborne imagery. Wessling: German Aerospace Center (DLR).
72. DLR (2014) CATENA. Wessling: German Aerospace Center (DLR).
73. Martinuzzi S, Gould WA, Ramos Gonzalez OM, (2007) Creating cloud-free Landsat ETM+ data sets in tropical landscapes: cloud and cloud-shadow removal. United States Department of Agriculture—Forest Service: International Institute of Tropical Forestry.
74. JSS (2014) ASTER GDEM. Japan Space Systems (J-spacesystems).
75. Meyer D, (2011) ASTER global digital elevation model version 2–summary of validation result. NASA land processes distributed active archive center and the joint Japan-US ASTER science team.
76. McFeeters SK, (1996) The use of the normalized difference water index (NDWI) in the delineation of open water features. Int J Remote Sens17: 1425–1432.
77. Breiman L, (2001) Random forests. Mach Learn45: 5–32.
78. GoogleInc. (2010) Google Earth (Version). Google.
79. Kuenzer C, Dech S, Kuenzer C, Dech S, (2013) Theoretical background of thermal infrared remote sensing. In: Thermal infrared remote sensing. Dordrecht: Springer. pp. 1–26.
80. Strahler AN, (1957) Quantitative analysis of watershed geomorphology. EOS, Trans Am Geophys Union38: 913–920.
81. Di Gregorio A, Jansen LJM, (2005) Land cover classification system classification concepts and user manual software version (2). Rome: Food and Agricultural Organization of the United Nations (FAO).
82. Karagiannis-Voules DA, Biedermann P, Ekpo UF, Garba A, Langer E, et al. (2015) Spatial and temporal distribution of soil-transmitted helminth infection in sub-Saharan Africa: a systematic review and geostatistical meta-analysis. Lancet Infect Dis15: 74–84. doi: 10.1016/S1473-3099(14)71004-725486852
83. Jordan P, Webbe G, Jordan P, Webbe G, Sturrock RF, (1993) Epidemiology. In: Human schistosomiasis. Wallingford:CAB International. pp. 87–152.
84. Schur N, Hürlimann E, Garba A, Traoré MS, Ndir O, et al. (2011) Geostatistical model-based estimates of schistosomiasis prevalence among individuals aged ≤20 years in West Africa. PLoS Negl Trop Dis5: e1194. doi: 10.1371/journal.pntd.000119421695107
85. Albertson ML, Simons DB, Chow VT, (1964) Fluid Mechanics. In: Handbook of applied hydrology: a compendium of water-resources technology. New York, USA: McGraw-Hill. pp. 1–49.
86. Scorza JV, Silva J, Gonzalez L, Machado R, (1961) Stream velocity as a gradient in Australorbis glabratus (Say, 1818). Z Tropenmed Parasitol12: 191–196. 13749320
87. Beck-Wörner C, Raso G, Vounatsou P, N'Goran EK, Rigo G, et al. (2007) Bayesian spatial risk prediction of Schistosoma mansoni infection in western Côte d'Ivoire using a remotely-sensed digital elevation model. Am J Trop Med Hyg76: 956–963. 17488922
88. Sturrock RF, Jordan P, Webbe G, Sturrock RF, (1993) The intermediate hosts and host-parasite relationships. In: Human schistosomiasis. Wallingford: CAB International. pp. 33–85.
89. Sturrock RF, Jordan P, Webbe G, Sturrock RF, (1993) The parasites and their life cycle. In: Human schistosomiasis. Wallingford: CAB International. pp. 1–32.
90. WHO (1957) Study group on the ecology of intermediate snail hosts of bilharziasis. WHO Tech Rep Ser120: 1–40.
91. Belton S, Stewart TS, (2002) Multiple criteria decision analysis: an integrated approach. Massachusetts: Kluwer Academic Publishers.
92. Malone JB, Yilma JM, McCarroll JC, Erko B, Mukaratirwa S, et al. (2001) Satellite climatology and the environmental risk of Schistosoma mansoni in Ethiopia and East Africa. Acta Trop79: 59–72. 11378142
93. Kabatereine NB, Brooker S, Tukahebwa EM, Kazibwe F, Onapa AW, (2004) Epidemiology and geography of Schistosoma mansoni in Uganda: implications for planning control. Trop Med Int Health9: 372–380. 14996367
94. Boslaugh S, Watters PA, Treseler M, (2008) Statistics in a nutshell; O`Reilly Media, Inc.
95. Fisher J, Mustard JF, (2004) High spatial resolution sea surface climatology from Landsat thermal infrared data. Remote Sens Environ90: 293–307.
96. Torgersen CE, Faux RN, McIntosh BA, Poage NJ, Norton DJ, (2001) Airborne thermal remote sensing for water temperature assessment in rivers and streams. Remote Sens Environ76: 386–398.
97. William DJ, Rybicki NB, Lombana AV, O'Brien TM, Gomez RB, (2003) Preliminary investigation of submerged aquatic vegetation mapping using hyperspectral remote sensing. Environ Monit Assess81: 383–392. 12620030
98. Vahtmäe E, Kutser T, Martin G, Kotta J, (2006) Feasibility of hyperspectral remote sensing for mapping benthic macroalgal cover in turbid coastal waters—a Baltic Sea case study. Remote Sens Environ101: 342–351.
99. Marcus WA, Fonstad MA, (2008) Optical remote mapping of rivers at sub-meter resolutions and watershed extents. Earth Surf Process Landf33: 4–24.
100. Kiel B, Alsdorf D, LeFavour G, (2006) Capability of SRTM C- and X-band DEM data to measure water elevations in Ohio and the Amazon. Photogramm Eng Remote Sens72: 313–320.
101. Clennon JA, King CH, Muchiri EM, Kitron U, (2007) Hydrological modelling of snail dispersal patterns in Msambweni, Kenya and potential resurgence of Schistosoma haematobium transmission. Parasitology134: 683–693. 17156580
102. King CH, (2010) Parasites and poverty: the case of schistosomiasis. Acta Trop113: 95–104. doi: 10.1016/j.actatropica.2009.11.01219962954
103. Butterworth AE, Jordan P, Webbe G, Sturrock RF, (1993) Immunology of schistosomiasis. In: Human schistosomiasis. Wallingford: CAB International. pp. 331–366.
104. Bundy DAP, Blumenthal U, Barnard C, Behnke JM, (1990) Human behaviour and the epidemiology of helminth infection. In: Parasitism and host behaviour. London: Taylor and Francis. pp. 264–289.
105. Schmidlin T, Hürlimann E, Siluée KD, Yapi RB, Houngbedji C, et al. (2013) Effects of hygiene and defecation behavior on helminths and intestinal protozoa infections in Taabo, Côte d'Ivoire. PLoS One8.
106. Stothard JR, Mgeni AF, Khamis S, Seto E, Ramsan M, et al. (2002) New insights into the transmission biology of urinary schistosomiasis in Zanzibar. Trans R Soc Trop Med Hyg96: 470–475. 12474469