Volume 91, Issue 3
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



The progress of the integrated control policy for schistosomiasis implemented since 2005 in China, which is aiming at reducing the roles of bovines and humans as infection sources, may be challenged by persistent presence of infected snails in lake and marshland areas. Based on annual parasitologic data for schistosomiasis during 2004–2011 in Xingzi County, a spatio-temporal kriging model was used to investigate the spatio-temporal pattern of schistosomiasis risk. Results showed that environmental factors related to snail habitats can explain the spatio-temporal variation of schistosomiasis. Predictive maps of schistosomiasis risk illustrated that clusters of the disease fluctuated during 2004–2008; there was an extensive outbreak in 2008 and attenuated disease occurrences afterwards. An area with an annually constant cluster of schistosomiasis was identified. Our study suggests that targeting snail habitats located within high-risk areas for schistosomiasis would be an economic and sustainable way of schistosomiasis control in the future.


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  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 Dis 6: 11425.[Crossref]
  2. McManus DP, Gray DJ, Li Y, Feng Z, Williams GM, Stewart D, Rey-Ladino J, Ross AG, , 2010. Schistosomasis in the People's Republic of China: the era of the Three Gorges Dam. Clin Microbiol Rev 23: 442466.[Crossref]
  3. Chen X, Jiang Q, Wang L, Zhao G, Zhao Q, Gu Y, , 2002. Schistosomiasis situation in the People's public of China in 2001 [in Chinese]. Chin J Schisto Control 14: 241243.
  4. Zhou XN, Wang LY, Chen MG, Wu XH, Jiang QW, Chen XY, Zheng J, Utzinger J, , 2005. The public health significance and control of schistosomiasis in China–then and now. Acta Trop 96: 97105.[Crossref]
  5. Utzinger J, Zhou XN, Chen MG, Bergquist R, , 2005. Conquering schistosomiasis in China: the long march. Acta Trop 96: 6996.[Crossref]
  6. Mao SP, Shao BR, , 1982. Schistosomiasis control in the People's Republic of China. Am J Trop Med Hyg 1: 9299.
  7. Yuan H, Jiagang G, Bergquist R, Tanner M, Xianyi C, , 2005. The 1992–1999 World Bank schistosomiasis research initiative in China: outcome and prospectives. Parasitol Int 49: 195207.[Crossref]
  8. Utzinger J, Bergquist R, Shu-Hua X, Singer BH, Tanner M, , 2003. Sustainable schistosomiasis control–the way forward. Lancet 362: 19321934.[Crossref]
  9. Zhang Z, Zhu R, Ward MP, Xu W, Zhang L, Guo J, Zhao F, Jiang Q, , 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 Dis 6: e1620.[Crossref]
  10. Seto EY, Remais JV, Carlton EJ, Wang S, Liang S, Brindley PJ, Qiu D, Spear RC, Wang LD, Wang TP, Chen HG, Dong XQ, Wang LY, Hao Y, Bergquist R, Zhou XN, , 2011. Toward sustainable and comprehensive control of schistosomiasis in China: lessons from Sichuan. PLoS Negl Trop Dis 5: e1372.[Crossref]
  11. Wang L, Chen H, Guo J, Zeng X, Hong X, , 2009. A strategy to control transmission of Schistosoma japonicum in China. N Engl J Med 360: 121128.[Crossref]
  12. Li SZ, Luz A, Wang XH, Xu LL, Wang Q, Qian YJ, Wu XH, Guo JG, Xia G, Wang LY, Zhou XN, , 2009. Schistosomiasis in China: acute infections during 2005–2008. Chin Med J (Engl) 122: 10091014.
  13. Yang K, Li W, Sun LP, Huang YX, Zhang JF, Wu F, Hang DR, Steinmann P, Liang YS, , 2013. Spatio-temporal analysis to identify determinants of Oncomelania hupensis infection with Schistosoma japonicum in Jiangsu province, China. Parasit Vectors 6: 138.[Crossref]
  14. Liang S, Seto EY, Remais JV, Zhong B, Yang C, Hubbard A, Davis GM, Gu X, Qiu D, Spear RC, , 2007. Environmental effects on parasitic disease transmission exemplified by schistosomiasis in western China. Proc Natl Acad Sci USA 104: 71107115.[Crossref]
  15. Gosoniu L, Vounatsou P, Sogoba N, Smith T, , 2006. Bayesian modeling of geostatistical malaria risk data. Geospat Health 1: 127139.[Crossref]
  16. Reid H, Haque U, Clements AC, Tatem AJ, Vallely A, Ahmed SM, Islam A, Haque R, , 2010. Mapping malaria risk in Bangladesh using Bayesian geostatistical models. Am J Trop Med Hyg 83: 861867.[Crossref]
  17. Zhang Z, Carpenter TE, Chen Y, Clark AB, Lynn HS, Peng W, Zhou Y, Zhao G, Jiang Q, , 2008. Identifying high-risk regions for schistosomiasis in Guichi, China: a spatial analysis. Acta Trop 107: 217223.[Crossref]
  18. Diggle PJ, Thomson MC, Christensen OF, Rowlingson B, Obsomer V, Gardon J, Wanji S, Takougang I, Enyong P, Kamgno J, Remme JH, Boussinesq M, Molyneux DH, , 2007. Spatial modelling and the prediction of Loa loa risk: decision making under uncertainty. Ann Trop Med Parasitol 101: 499509.[Crossref]
  19. Cressie N, Wikle C, , 2011. Statistics for Spatio-Temporal Data. New York: John Wiley.
  20. Le ND, Zidek JV, , 2006. Statistical Analysis of Environmental Space-Time Processes. New York: Springer.
  21. Baker RD, , 2004. Identifying space–time disease clusters. Acta Trop 91: 291299.[Crossref]
  22. Metras R, Porphyre T, Pfeiffer DU, Kemp A, Thompson PN, Collins LM, White RG, , 2012. Exploratory space-time analyses of Rift Valley Fever in South Africa in 2008–2011. PLoS Negl Trop Dis 6: e1808.[Crossref]
  23. Paireau J, Girond F, Collard JM, Mainassara HB, Jusot JF, , 2012. Analysing spatio-temporal clustering of meningococcal meningitis outbreaks in Niger reveals opportunities for improved disease control. PLoS Negl Trop Dis 6: e1577.[Crossref]
  24. Isaaks E, Srivastava R, , 1989. Applied Geostatistics. Oxford, United Kingdom: Oxford University Press.
  25. Kyriakidis PC, Journel AG, , 2001. Stochastic modeling of atmospheric pollution: a spatial time-series framework: part I. Methodology. Atmos Environ 35: 23312337.[Crossref]
  26. Bechini L, Ducco G, Donatelli M, Stein A, , 2000. Modelling, interpolation and stochastic simulation in space and time of global solar radiation. Agric Ecosyst Environ 81: 2942.[Crossref]
  27. Snepvangers JJ, Heuvelink GB, Huisman JA, , 2003. Soil water content interpolation using spatio-temporal kriging with external drift. Geoderma 112: 253271.[Crossref]
  28. Tao P, Jiang QL, Luo CJ, Yin ZH, Wang JM, , 2009. Endemic situation of schistosomiasis in Xingzi County. Chin J Schisto Control 21: 6263.
  29. Chen H, Lin D, , 2004. The prevalence and control of schistosomiasis in Poyang Lake region, China. Parasitol Int 53: 115125.[Crossref]
  30. Yu JM, de Vlas SJ, Jiang QW, Gryseels B, , 2007. Comparison of the Kato-Katz technique, hatching test and indirect hemagglutination assay (IHA) for the diagnosis of Schistosoma japonicum infection in China. Parasitol Int 56: 4549.[Crossref]
  31. Hu Y, Zhang Z, Chen Y, Wang Z, Gao J, Tao B, Jiang Q, Jiang Q, , 2013. Spatial pattern of schistosomiasis in Xingzi, Jiangxi Province, China: the effects of environmental factors. Parasit Vectors 6: 214.[Crossref]
  32. Journel AG, Huijbregts CJ, , 1978. Mining Geostatistics. London: Academic Press.
  33. Deutsch CV, Journel AG, . GSLIB: Geostatistical Software Library and User's Guide. New York: Oxford University Press.
  34. De Cesare L, Myers DE, Posa D, , 2001. Product-sum covariance for space-time modeling: an environmental application. Environmetrics 12: 1123.[Crossref]
  35. Box GE, Cox DR, , 1964. An analysis of transformations (with discussion). J R Stat Soc B 26: 211252.
  36. Fischer MM, Wang JF, , 2011. Spatial Data Analysis: Models, Methods and Techniques. New York: Springer.[Crossref]
  37. Wang JF, Li XH, Christakos G, Liao YL, Zhang T, Gu X, Zheng XY, , 2010. Geographical detectors-based health risk assessment and its application in the neural tube defects study of the Heshun region, China. Int J Geogr Inf Sci 24: 107127.[Crossref]
  38. Pebesma E, , 2011. Spatio-Temporal Geostatistics using gstat. Package Vignettes. Munster, Germany: University of Munster.
  39. Hao Y, Wang LY, Zhou XN, Chen HG, Huang XB, Liang YS, , 2009. Causes and risks of schistosomiasis transmission in Poyang Lake region of Jiangxi Province, China. Chin J Schisto Control 21: 345349.
  40. Zhou YS, Peng GH, Hu ZH, Zhu R, Yu Q, Cao CL, Hu GH, Guo JG, , 2012. Influencing factors of changes of Oncomelania snail densities in Poyang Lake region, Nanchang City, 2011. Chin J Schisto Control 3: 315317.
  41. Zhang S, Wang T, Tao C, Chen G, Chen J, Xu H, , 2005. Observation on comprehensive measures of safe treatment of night-soil and water supply, replacement of bovine with machine for schistosomiasis control. Chin J Schisto Control 17: 437442.
  42. Chen XY, Wang LY, Cai JM, Zhou XN, Zheng J, Guo JG, Wu XH, Engels D, Chen MG, , 2005. Schistosomiasis control in China: the impact of a 10-year World Bank Loan Project (1992–2001). Bull World Health Organ 83: 4348.
  43. Wang L, , 2005. Management of human and animal feces is a key element for effective control of pidemic of endemic schistosomiasis in China. Chin J Epidemiol 26: 929930.
  44. Zhou YB, Liang S, Jiang QW, , 2012. Factors impacting on progress towards elimination of transmission of schistosomiasis japonica in China. Parasit Vectors 5: 275.[Crossref]
  45. Brooker S, Clements AC, Bundy DA, , 2006. Global epidemiology, ecology and control of soil-transmitted helminth infections. Adv Parasitol 62: 221261.[Crossref]
  46. Guemas V, Doblas-Reyes F, Andreu-Burillo I, Asif M, , 2013. Retrospective prediction of the global warming slowdown in the past decade. Nat Clim Change 3: 649653.[Crossref]
  47. Yan HM, Huang HQ, Xiao XM, Jiang LG, , 2008. Spatio-temporal distribution of multiple cropping systems in the Poyang Lake. Acta Ecol Sin 28: 45174523.
  48. Wang XH, Zhou XN, Vounatsou P, Chen Z, Utzinger J, Yang K, Steinmann P, Wu XH, , 2008. Bayesian spatio-temporal modeling of Schistosoma japonicum prevalence data in the absence of a diagnostic ‘gold’ standard. PLoS Negl Trop Dis 2: e250.[Crossref]

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  • Received : 24 Apr 2014
  • Accepted : 02 Jun 2014

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