Micro-Geographical Heterogeneity in Schistosoma mansoni and S. haematobium Infection and Morbidity in a Co-Endemic Community in Northern Senegal

PLoS Neglected Tropical Diseases

Volumn 7, Issue 12, 2013, Pages

  Meurs, Lynn ^a   Mbow, Moustapha ^a,b   Boon, Nele ^a,c   van den Broeck, Frederik ^a,c   Vereecken, Kim ^a   Dièye, Tandakha Ndiaye ^b   Abatih, Emmanuel ^a   Huyse, Tine ^a,c   Mboup, Souleymane ^b   Polman, Katja ^a  

^a INSTITUTE OF TROPICAL MEDICINE   (Belgium)

^b Centre Hospitalier Universitaire Aristide Le Dantec de Dakar   (Senegal)

^c UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

LAKE WATER; MEBENDAZOLE; PRAZIQUANTEL;

ADOLESCENT; ADULT; AGED; ARTICLE; CHILD; CROSS-SECTIONAL STUDY; DISEASE ASSOCIATION; DISEASE TRANSMISSION; ENDEMIC DISEASE; FEMALE; HUMAN; INFANT; INTERVIEW; LIVER FIBROSIS; MALE; MIXED INFECTION; MORBIDITY; NEWBORN; PARASITE IDENTIFICATION; RISK FACTOR; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS HAEMATOBIA; SENEGAL;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; CHILD; CHILD, PRESCHOOL; CLUSTER ANALYSIS; COINFECTION; CROSS-SECTIONAL STUDIES; FEMALE; HUMANS; INFANT; INFANT, NEWBORN; MALE; MIDDLE AGED; QUESTIONNAIRES; RURAL POPULATION; SCHISTOSOMA HAEMATOBIUM; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS HAEMATOBIA; SCHISTOSOMIASIS MANSONI; SENEGAL; SPATIAL ANALYSIS; YOUNG ADULT;

EID: 84892720657     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002608     Document Type: Article

References (80)

1. WHO (2010 February) Schistosomiasis fact sheet. http://www.who.int/mediacentre/factsheets/fs115/en/index.html.
2. Hotez PJ, Kamath A, (2009) Neglected tropical diseases in sub-saharan Africa: review of their prevalence, distribution, and disease burden. PLoS Negl Trop Dis 3: e412.
3. Gryseels B, Polman K, Clerinx J, Kestens L, (2006) Human schistosomiasis. Lancet 368: 1106-1118.
4. Simoonga C, Kazembe LN, Kristensen TK, Olsen A, Appleton CC, et al. (2008) The epidemiology and small-scale spatial heterogeneity of urinary schistosomiasis in Lusaka province, Zambia. Geospat Health 3: 57-67.
5. Handzel T, Karanja DM, Addiss DG, Hightower AW, Rosen DH, et al. (2003) Geographic distribution of schistosomiasis and soil-transmitted helminths in Western Kenya: implications for anthelminthic mass treatment. Am J Trop Med Hyg 69: 318-323.
6. Tsang VC, Hillyer GV, Noh J, Vivas-Gonzalez BE, Ahn LH, et al. (1997) Geographic clustering and seroprevalence of schistosomiasis in Puerto Rico (1995). Am J Trop Med Hyg 56: 107-112.
7. Brooker S, Clements AC, (2009) Spatial heterogeneity of parasite co-infection: Determinants and geostatistical prediction at regional scales. Int J Parasitol 39: 591-597.
8. Clements AC, Bosque-Oliva E, Sacko M, Landoure A, Dembele R, et al. (2009) A comparative study of the spatial distribution of schistosomiasis in Mali in 1984-1989 and 2004-2006. PLoS Negl Trop Dis 3: e431.
9. Kloos H, Lo CT, Birrie H, Ayele T, Tedla S, et al. (1988) Schistosomiasis in Ethiopia. Soc Sci Med 26: 803-827.
10. Dennis E, Vorkpor P, Holzer B, Hanson A, Saladin B, et al. (1983) Studies on the epidemiology of schistosomiasis in Liberia: the prevalence and intensity of schistosomal infections in Bong County and the bionomics of the snail intermediate hosts. Acta Trop 40: 205-229.
11. Ahmed ES, Daffalla A, Christensen NO, Madsen H, (1996) Patterns of infection and transmission of human schistosomiasis mansoni and schistosomiasis haematobium in White Nile Province, Sudan. Ann Trop Med Parasitol 90: 173-180.
12. 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 Cote d'Ivoire. Parasitology 131: 97-108.
13. Brooker S, Miguel EA, Waswa P, Namunyu R, Moulin S, et al. (2001) The potential of rapid screening methods for Schistosoma mansoni in western Kenya. Ann Trop Med Parasitol 95: 343-351.
14. Odiere MR, Opisa S, Odhiambo G, Jura WG, Ayisi JM, et al. (2011) Geographical distribution of schistosomiasis and soil-transmitted helminths among school children in informal settlements in Kisumu City, Western Kenya. Parasitology 138: 1569-1577.
15. Gazzinelli A, (2006) The spatial distribution of Schistosoma mansoni infection before and after chemotherapy in the Jequitinhonha Valley in Brazil. Mem Inst Oswaldo Cruz 101 Suppl 1:63-71: 63-71.
16. Gryseels B, Nkulikyinka L, (1988) The distribution of Schistosoma mansoni in the Rusizi plain (Burundi). Ann Trop Med Parasitol 82: 581-590.
17. Chandiwana SK, Taylor P, Clarke VD, (1988) Prevalence and intensity of schistosomiasis in two rural areas in Zimbabwe and their relationship to village location and snail infection rates. Ann Trop Med Parasitol 82: 163-173.
18. Gryseels B, Nkulikyinka L, (1990) The morbidity of schistosomiasis mansoni in the highland focus of Lake Cohoha, Burundi. Trans R Soc Trop Med Hyg 84: 542-547.
19. Kapito-Tembo AP, Mwapasa V, Meshnick SR, Samanyika Y, Banda D, et al. (2009) Prevalence distribution and risk factors for Schistosoma hematobium infection among school children in Blantyre, Malawi. PLoS Negl Trop Dis 3: e361.
20. Coutinho EM, Abath FG, Barbosa CS, Domingues AL, Melo MC, et al. (1997) Factors involved in Schistosoma mansoni infection in rural areas of northeast Brazil. Mem Inst Oswaldo Cruz 92: 707-715.
21. Clennon JA, King CH, Muchiri EM, Kariuki HC, Ouma JH, et al. (2004) Spatial patterns of urinary schistosomiasis infection in a highly endemic area of coastal Kenya. Am J Trop Med Hyg 70: 443-448.
22. Clennon JA, Mungai PL, Muchiri EM, King CH, Kitron U, (2006) Spatial and temporal variations in local transmission of Schistosoma haematobium in Msambweni, Kenya. Am J Trop Med Hyg 75: 1034-1041.
23. Mutuku FM, King CH, Bustinduy AL, Mungai PL, Muchiri EM, et al. (2011) Impact of drought on the spatial pattern of transmission of Schistosoma haematobium in coastal Kenya. Am J Trop Med Hyg 85: 1065-1070.
24. Stothard JR, Sousa-Figueiredo JC, Betson M, Seto EY, Kabatereine NB, (2011) Investigating the spatial micro-epidemiology of diseases within a point-prevalence sample: a field applicable method for rapid mapping of households using low-cost GPS-dataloggers. Trans R Soc Trop Med Hyg 105: 500-506.
25. Yiannakoulias N, Wilson S, Kariuki HC, Mwatha JK, Ouma JH, et al. (2010) Locating irregularly shaped clusters of infection intensity. Geospat Health 4: 191-200.
26. Utzinger J, Muller I, Vounatsou P, Singer BH, N'goran EK, et al. (2003) Random spatial distribution of Schistosoma mansoni and hookworm infections among school children within a single village. J Parasitol 89: 686-692.
27. Pullan RL, Bethony JM, Geiger SM, Cundill B, Correa-Oliveira R, et al. (2008) Human helminth co-infection: analysis of spatial patterns and risk factors in a Brazilian community. PLoS Negl Trop Dis 2: e352.
28. Matthys B, Tschannen AB, Tian-Bi NT, Comoe H, Diabate S, et al. (2007) Risk factors for Schistosoma mansoni and hookworm in urban farming communities in western Cote d'Ivoire. Trop Med Int Health 12: 709-723.
29. Brooker S, Alexander N, Geiger S, Moyeed RA, Stander J, et al. (2006) Contrasting patterns in the small-scale heterogeneity of human helminth infections in urban and rural environments in Brazil. Int J Parasitol 36: 1143-1151.
30. Meurs L, Mbow M, Vereecken K, Menten J, Mboup S, et al. (2012) Epidemiology of mixed Schistosoma mansoni and Schistosoma haematobium infections in northern Senegal. Int J Parasitol 42: 305-311.
31. Meurs L, Mbow M, Vereecken K, Menten J, Mboup S, et al. (2012) Bladder Morbidity and Hepatic Fibrosis in Mixed Schistosoma haematobium and S. mansoni Infections: A Population-Wide Study in Northern Senegal. PLoS Negl Trop Dis 6: e1829.
32. De Clercq D, Vercruysse J, Picquet M, Shaw DJ, Diop M, et al. (1999) The epidemiology of a recent focus of mixed Schistosoma haematobium and Schistosoma mansoni infections around the 'Lac de Guiers' in the Senegal River Basin, Senegal. Trop Med Int Health 4: 544-550.
33. Huyse T, Webster BL, Geldof S, Stothard JR, Diaw OT, et al. (2009) Bidirectional introgressive hybridization between a cattle and human schistosome species. PLoS Pathog 5: e1000571.
34. Southgate V, Tchuem Tchuente LA, Sene M, De Clercq D, Theron A, et al. (2001) Studies on the biology of schistosomiasis with emphasis on the Senegal river basin. Mem Inst Oswaldo Cruz 96 Suppl: 75-78.
35. Ten Hove RJ, Verweij JJ, Vereecken K, Polman K, Dieye L, et al. (2008) Multiplex real-time PCR for the detection and quantification of Schistosoma mansoni and S. haematobium infection in stool samples collected in northern Senegal. Trans R Soc Trop Med Hyg 102: 179-185.
36. Talla I, Kongs A, Verle P, (1992) Preliminary study of the prevalence of human schistosomiasis in Richard-Toll (the Senegal river basin). Trans R Soc Trop Med Hyg 86: 182.
37. Talla I, Kongs A, Verle P, Belot J, Sarr S, et al. (1990) Outbreak of intestinal schistosomiasis in the Senegal River Basin. Ann Soc Belg Med Trop 70: 173-180.
38. Picquet M, Ernould JC, Vercruysse J, Southgate VR, Mbaye A, et al. (1996) Royal Society of Tropical Medicine and Hygiene meeting at Manson House, London, 18 May 1995. The epidemiology of human schistosomiasis in the Senegal river basin. Trans R Soc Trop Med Hyg 90: 340-346.
39. WHO (2006) Preventive chemotherapy in human helminthiasis- Coordinated use of anthelminthic drugs in control interventions: a manual for health professionals and programme managers.
40. Berger C, Ba N, Gugger M, Bouvy M, Rusconi F, et al. (2006) Seasonal dynamics and toxicity of Cylindrospermopsis raciborskii in Lake Guiers (Senegal, West Africa). FEMS Microbiol Ecol 57: 355-366.
41. Kitron UD, Higashi GI, (1985) Schistosoma haematobium in Upper Egypt: analysis of dispersion patterns. Am J Trop Med Hyg 34: 331-340.
42. Richter J, Hatz C, Campagne N, Bergquist R, Jenkins JM (1996) Ultrasound in schistosomiasis: A practical guide to the standardized use of ultrasonography for the assessment of schistosomiasis-related morbidity. TDR/STR/SCH/00.1.
43. Leutscher PD, Reimert CM, Vennervald BJ, Ravaoalimalala VE, Ramarokoto CE, et al. (2000) Morbidity assessment in urinary schistosomiasis infection through ultrasonography and measurement of eosinophil cationic protein (ECP) in urine. Trop Med Int Health 5: 88-93.
44. Medhat A, Zarzour A, Nafeh M, Shata T, Sweifie Y, et al. (1997) Evaluation of an ultrasonographic score for urinary bladder morbidity in Schistosoma haematobium infection. Am J Trop Med Hyg 57: 16-19.
45. Kulldorff M (2010) SaTScan User Guide for version 9.0.
46. Kulldorff M, (1997) A spatial scan statistic. Communications in Statistics- Theory and Methods 26: 1481-1496.
47. Kulldorff M, Huang L, Konty K, (2009) A scan statistic for continuous data based on the normal probability model. Int J Health Geogr 8: 58.
48. Jung I, Kulldorff M, Klassen AC, (2007) A spatial scan statistic for ordinal data. Stat Med 26: 1594-1607.
49. Kulldorff M, Mostashari F, Duczmal L, Katherine YW, Kleinman K, et al. (2007) Multivariate scan statistics for disease surveillance. Stat Med 26: 1824-1833.
50. Cook, G C. and Zumla, A I. (2009) Manson's Tropical Diseases. London: Saunders Elsevier.
51. Farooq M, (1966) Importance of determining transmisson sites in planning bilharziasis control. Field observations from the Egypt-49 project area. Am J Epidemiol 83: 603-612.
52. Polderman AM, Mpamila K, Manshande JP, Gryseels B, Van Schayk O, (1985) Historical, geological and ecological aspects of transmission of intestinal schistosomiasis in Maniema, Kivu Province, Zaire. Ann Soc Belg Med Trop 65: 251-261.
53. Woolhouse ME, Chandiwana SK, (1989) Spatial and temporal heterogeneity in the population dynamics of Bulinus globosus and Biomphalaria pfeifferi and in the epidemiology of their infection with schistosomes. Parasitology 98 (Pt 1) (): 21-34.
54. Johnson PT, Lund PJ, Hartson RB, Yoshino TP, (2009) Community diversity reduces Schistosoma mansoni transmission, host pathology and human infection risk. Proc Biol Sci 276: 1657-1663.
55. Al-Sheikh AH, Dagal MA, (2011) The ecological differences between Bulinus beccari, the intermediate host of Schistsoma haematobium and Biomphalaria pfeifferi the intermediate host of S. mansoni in in Jazan Region, Saudi Arabia. J Egypt Soc Parasitol 41: 543-551.
56. Ernould JC, Ba K, Sellin B, (1999) The impact of the local water-development programme on the abundance of the intermediate hosts of schistosomiasis in three villages of the Senegal River delta. Ann Trop Med Parasitol 93: 135-145.
57. Amankwa JA, Bloch P, Meyer-Lassen J, Olsen A, Christensen NO, (1994) Urinary and intestinal schistosomiasis in the Tono Irrigation Scheme, Kassena/Nankana District, upper east region, Ghana. Trop Med Parasitol 45: 319-323.
58. Bethony J, Williams JT, Blangero J, Kloos H, Gazzinelli A, et al. (2002) Additive host genetic factors influence fecal egg excretion rates during Schistosoma mansoni infection in a rural area in Brazil. Am J Trop Med Hyg 67: 336-343.
59. Grant AV, Araujo MI, Ponte EV, Oliveira RR, Cruz AA, et al. (2011) Polymorphisms in IL10 are associated with total Immunoglobulin E levels and Schistosoma mansoni infection intensity in a Brazilian population. Genes Immun 12: 46-50.
60. Grant AV, Araujo MI, Ponte EV, Oliveira RR, Gao P, et al. (2012) Functional polymorphisms in IL13 are protective against high Schistosoma mansoni infection intensity in a Brazilian population. PLoS One 7: e35863.
61. Lima e Costa MF, Magalhaes MH, Rocha RS, Antunes CM, Katz N, (1987) Water-contact patterns and socioeconomic variables in the epidemiology of schistosomiasis mansoni in an endemic area in Brazil. Bull World Health Organ 65: 57-66.
62. Farooq M, Nielsen J, Samaan SA, Mallah MB, Allam AA, (1966) The epidemiology of Schistosoma haematobium and S. mansoni infections in the Egypt-49 project area. 2. Prevalence of bilharziasis in relation to personal attributes and habits. Bull World Health Organ 35: 293-318.
63. Kloos H, Gazzinelli A, Van Zuyle P, (1998) Microgeographical patterns of schistosomiasis and water contact behavior; examples from Africa and Brazil. Mem Inst Oswaldo Cruz 93 Suppl 1: 37-50.
64. Brouwer KC, Ndhlovu PD, Wagatsuma Y, Munatsi A, Shiff CJ, (2003) Epidemiological assessment of Schistosoma haematobium-induced kidney and bladder pathology in rural Zimbabwe. Acta Trop 85: 339-347.
65. Brouwer KC, Munatsi A, Ndhlovu PD, Wagatsuma Y, Shiff CJ, (2004) Urinary schistosomiasis in Zimbabwean school children: predictors of morbidity. Afr Health Sci 4: 115-118.
66. El Khoby T, Galal N, Fenwick A, Barakat R, El Hawey A, et al. (2000) The epidemiology of schistosomiasis in Egypt: summary findings in nine governorates. Am J Trop Med Hyg 62: 88-99.
67. Garba A, Pion S, Cournil A, Milet J, Schneider D, et al. (2010) Risk factors for Schistosoma haematobium infection and morbidity in two villages with different transmission patterns in Niger. Acta Trop 115: 84-89.
68. Heurtier Y, Lamothe F, Develoux M, Docquier J, Mouchet F, et al. (1986) Urinary tract lesions due to Schistosoma haematobium infection assessed by ultrasonography in a community based study in Niger. Am J Trop Med Hyg 35: 1163-1172.
69. Serieye J, Boisier P, Ravaoalimalala VE, Ramarokoto CE, Leutscher P, et al. (1996) Schistosoma haematobium infection in western Madagascar: morbidity determined by ultrasonography. Trans R Soc Trop Med Hyg 90: 398-401.
70. Traore M, Traore HA, Kardorff R, Diarra A, Landoure A, et al. (1998) The public health significance of urinary schistosomiasis as a cause of morbidity in two districts in Mali. Am J Trop Med Hyg 59: 407-413.
71. King CH, Lombardi G, Lombardi C, Greenblatt R, Hodder S, et al. (1988) Chemotherapy-based control of schistosomiasis haematobia. I. Metrifonate versus praziquantel in control of intensity and prevalence of infection. Am J Trop Med Hyg 39: 295-305.
72. Southgate VR, De Clercq D, Sene M, Rollinson D, Ly A, et al. (2000) Observations on the compatibility between Bulinus spp. and Schistosoma haematobium in the Senegal River basin. Ann Trop Med Parasitol 94: 157-164.
73. King CH, Muchiri EM, Ouma JH, (1992) Age-targeted chemotherapy for control of urinary schistosomiasis in endemic populations. Mem Inst Oswaldo Cruz 87 Suppl 4: 203-210.
74. Bethony JM, Quinnell RJ, (2008) Genetic epidemiology of human schistosomiasis in Brazil. Acta Trop 108: 166-174.
75. Gong YY, Wilson S, Mwatha JK, Routledge MN, Castelino JM, et al. (2012) Aflatoxin exposure may contribute to chronic hepatomegaly in Kenyan school children. Environ Health Perspect 120: 893-896.
76. Booth M, Vennervald BJ, Kenty L, Butterworth AE, Kariuki HC, et al. (2004) Micro-geographical variation in exposure to Schistosoma mansoni and malaria, and exacerbation of splenomegaly in Kenyan school-aged children. BMC Infect Dis 4: 13.
77. WHO (2013) Schistosomiasis: progress report 2001-2011, strategic plan 2012-2020.
78. WHO (2011) Helminth control in school-age children: A guide for managers of control programmes. WHO Library Cataloguing-in-Publication Data.
79. Sturrock RF, (1989) The control of schistosomiasis: epidemiological aspects of reinfection. Mem Inst Oswaldo Cruz 84 Suppl 1: 134-148.
80. Peng WX, Tao B, Clements A, Jiang QL, Zhang ZJ, et al. (2010) Identifying high-risk areas of schistosomiasis and associated risk factors in the Poyang Lake region, China. Parasitology 137: 1099-1107.