Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-30T20:01:55.286Z Has data issue: false hasContentIssue false
  • English
  • Français

Identifying high-risk areas of schistosomiasis and associated risk factors in the Poyang Lake region, China

Published online by Cambridge University Press:  04 February 2010

W. X. PENG ,
B. TAO ,
A. CLEMENTS ,
Q. L. JIANG ,
Z. J. ZHANG ,
Y. B. ZHOU  and
Q. W. JIANG
W. X. PENG
Affiliation:
Department of Epidemiology, School of Public Health, Fudan University, 138 Yixueyuan Road, Shanghai200032, People's Republic of China Key Laboratory on Public Health Safety of the Ministry of Education at the Fudan University, 138 Yixueyuan Road, Shanghai200032, People's Republic of China
B. TAO
Affiliation:
Xingzi Anti-schistosomiasis Station, Jiangxi332800, People's Republic of China
A. CLEMENTS
Affiliation:
School of Population Health, University of Queensland, Herston Road, Herston, QLD 4006, Australia Australian Centre for International and Tropical Health, Queensland Institute of Medical Research, Herston Road, Herston, QLD 4006, Australia
Q. L. JIANG
Affiliation:
Xingzi Anti-schistosomiasis Station, Jiangxi332800, People's Republic of China
Z. J. ZHANG
Affiliation:
Department of Epidemiology, School of Public Health, Fudan University, 138 Yixueyuan Road, Shanghai200032, People's Republic of China Key Laboratory on Public Health Safety of the Ministry of Education at the Fudan University, 138 Yixueyuan Road, Shanghai200032, People's Republic of China
Y. B. ZHOU
Affiliation:
Department of Epidemiology, School of Public Health, Fudan University, 138 Yixueyuan Road, Shanghai200032, People's Republic of China Key Laboratory on Public Health Safety of the Ministry of Education at the Fudan University, 138 Yixueyuan Road, Shanghai200032, People's Republic of China
Q. W. JIANG*
Affiliation:
Department of Epidemiology, School of Public Health, Fudan University, 138 Yixueyuan Road, Shanghai200032, People's Republic of China Key Laboratory on Public Health Safety of the Ministry of Education at the Fudan University, 138 Yixueyuan Road, Shanghai200032, People's Republic of China
*
*Corresponding author: Department of Epidemiology, School of Public Health, Fudan University, 138 Yixueyuan Road, Shanghai200032, People's Republic of China. Tel: +86 21 54237435. Fax: +86 21 64037364. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The epidemiology of schistosomiasis japonicum over small areas remains poorly understood, and this is particularly true in China. We aimed to identify high-risk areas for schistosomiasis and associated risk factors in the Poyang Lake region, China. A cross-sectional study was conducted and 60 of 920 persons (6·5%) were found to be infected with Schistosoma japonicum. Locations of households and snail habitats were determined using a hand-held global positioning system. We mapped the data in a geographical information system and used spatial scan statistics to explore clustering of infection, logistic regression and Bayesian geostatistical models to identify risk factors for each individual's infection status and multinomial logistic regression to identify risk factors for living in a cluster area. The risk of schistosomiasis was spatially clustered and higher in fishermen and males, not in persons who lived in close proximity to snail habitats and infected water sources. This study has demonstrated significant spatial variation in the prevalence of schistosomiasis at a small spatial scale. The results suggest that demographic factors (gender, occupation) rather than the distance to infected water are driving human transmission at small-scale spatial levels. Such information can be used to plan locally targeted interventions based on anthelminthic drug administration, snail control and sanitation improvement.

Keywords

schistosomiasisspatial analysisBayesian geostatistical modellinggeographical information systemrisk factors
Type
Research Article
Information
Parasitology , Volume 137 , Issue 7 , June 2010 , pp. 1099 - 1107
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Berhe, N., Medhin, G., Erko, B., Smith, T., Gedamu, S., Bereded, D., Moore, R., Habte, E., Redda, A., Gebre-Michael, T. and Gundersen, S. G. (2004). Variations in helminth faecal egg counts in Kato-Katz thick smears and their implications in assessing infection status with Schistosoma mansoni. Acta Tropica 92, 205–212. doi:10.1016/j.actatropica.2004.06.011.CrossRefGoogle ScholarPubMed
Brooker, S. (2002). Schistosomes, snails and satellites. Acta Tropica 82, 209–216.CrossRefGoogle ScholarPubMed
Brooker, S., Alexander, N., Geiger, S., Moyeed, R. A., Stander, J., Fleming, F., Hotez, P. J., Correa-Oliveira, R. and Bethony, J. (2006 a). Contrasting patterns in the small-scale heterogeneity of human helminth infections in urban and rural environments in Brazil. International Journal for Parasitology 36, 1143–1151.CrossRefGoogle Scholar
Brooker, S., Clarke, S., Njagi, J. K., Polack, S., Mugo, B., Estambale, B., Muchiri, E., Magnussen, P. and Cox, J. (2004). Spatial clustering of malaria and associated risk factors during an epidemic in a highland area of western Kenya. Tropical Medicine & International Health 9, 757–766.CrossRefGoogle Scholar
Brooker, S., Clements, A. C. A. and Bundy, D. A. P. (2006 b). Global epidemiology, ecology and control of soil-transmitted helminth infections. Advances in Parasitology 62, 223–265.Google ScholarPubMed
Brooker, S. (2007). Spatial epidemiology of human schistosomiasis in Africa: risk models, transmission dynamics and control. Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 1–8.CrossRefGoogle ScholarPubMed
Chaput, E. K., Meek, J. I. and Heimer, R. (2002). Spatial analysis of human granulocytic ehrlichiosis near Lyme, Connecticut. Emerging Infectious Diseases 8, 943–948.CrossRefGoogle ScholarPubMed
Clennon, J. A., Mungai, P. L., Muchiri, E. M., King, C. H. and Kitron, U. (2006). Spatial and temporal variations in local transmission of Schistosoma haematobium in Msambweni, Kenya. American Journal of Tropical Medicine and Hygiene 75, 1034–1041.CrossRefGoogle ScholarPubMed
Cousens, S., Smith, P. G., Ward, H., Everington, D., Knight, R. S. G., Zeidler, M., Stewart, G., Smith-Bathgate, E. A. B., Macleod, M. A., Mackenzie, J. and Will, R. G. (2001). Geographical distribution of variant Creutzfeldt-Jakob disease in Great Britain, 1994–2000. Lancet 357, 1002–1007.CrossRefGoogle ScholarPubMed
Davis, G. M., Wu, W. P., Williams, G., Liu, H. Y., Lu, S. B., Chen, H. G., Zheng, F., McManus, D. P. and Guo, J. G. (2006). Schistosomiasis japonica intervention study on Poyang lake, China: the snail's tale. Malacologia 49, 79–105.CrossRefGoogle Scholar
Enemark, H. L., Ahrens, P., Juel, C. D., Petersen, E., Petersen, R. F., Andersen, J. S., Lind, P. and Thamsborg, S. M. (2002). Molecular characterization of Danish Cryptosporidium parvum isolates. Parasitology 125, 331–341.CrossRefGoogle ScholarPubMed
Engels, D., Chitsulo, L., Montresor, A. and Savioli, L. (2002). The global epidemiological situation of schistosomiasis and new approaches to control and research. Acta Tropica 82, 139–146.CrossRefGoogle ScholarPubMed
Gazzinelli, A., Hightower, A., LoVerde, P. T., Haddad, J. P., Pereira, W. R., Bethony, J., Correa-Oliveira, R. and Kloos, H. (2006). The spatial distribution of Schistosoma mansoni infection before and after chemotherapy in the Jequitinhonha Valley in Brazil. Memórias do Instituto Oswaldo Cruz 101 (Suppl. 1), 63–71.CrossRefGoogle ScholarPubMed
Huang, Y. X. and Manderson, L. (2005). The social and economic context and determinants of schistosomiasis japonica. Acta Tropica 96, 223–231.Google ScholarPubMed
Jiang, Q. W., Wang, L. Y., Guo, J. G., Chen, M. G., Zhou, X. N. and Engels, D. (2002). Morbidity control of schistosomiasis in China. Acta Tropica 82, 115–125.Google Scholar
Jennings, J. M., Curriero, F. C., Celentano, D. and Ellen, J. M. (2005). Geographic identification of high gonorrhea transmission areas in Baltimore, Maryland. American Journal of Epidemiology 161, 73–80.CrossRefGoogle ScholarPubMed
Katz, N., Chaves, A. and Pellegrino, J. (1972). A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Revista do Instituto de Medicina Tropical de São Paulo 14, 397–400.Google ScholarPubMed
Kloos, H., Fulford, A. J., Butterworth, A. E., Sturrock, R. F., Ouma, J. H., Kariuki, H. C., Thiongo, F. W., Dalton, P. R. and Klumpp, R. K. (1997). Spatial patterns of human water contact and Schistosoma mansoni transmission and infection in four rural areas in Machakos District, Kenya. Social Science & Medicine 44, 949–968.CrossRefGoogle ScholarPubMed
Kloos, H., Gazzinelli, A. and Van Zuyle, P. (1998). Microgeographical patterns of schistosomiasis and water contact behavior; examples from Africa and Brazil. Memórias do Instituto Oswaldo Cruz 93 (Suppl. 1), 37–50.CrossRefGoogle ScholarPubMed
Kulldorff, M. (1997). A spatial scan statistic. Communications in Statistics: Theory and Methods 26, 1481–1496.CrossRefGoogle Scholar
Kulldorff, M. and Information Management Services, Inc. (2008). SaTScan™ v7·03: Software for the Spatial and Space-Time Scan Statistics. http://www.satscan.org/.Google Scholar
Langkjer, R. B., Vigre, H., Enemark, H. L. and Maddox-Hyttell, C. (2007). Molecular and phylogenetic characterization of Cryptosporidium and Giardia from pigs and cattle in Denmark. Parasitology 134, 339–350.CrossRefGoogle Scholar
Lawson, A. B. (2006). Disease cluster detection: A critique and a Bayesian proposal. Statistics in Medicine 25, 897–916.CrossRefGoogle Scholar
Li, Y. S., Ross, A. G. P., Yu, D. B., Li, Y., Williams, G. M. and McManus, D. P. (1997). An evaluation of Schistosoma japonicum infections in three villages in the Dongting lake region of China I. Prevalence, intensity and morbidity before the implementation of adequate control strategies. Acta Tropica 68, 77–91.CrossRefGoogle ScholarPubMed
Mostashari, F., Kulldorff, M., Hartman, J. J., Miller, J. R., Kulasekera, V. (2003). Dead bird clustering: A potential early warning system for West Nile virus activity. Emerging Infectious Diseases 9, 641–646.CrossRefGoogle Scholar
Peng, W. X., Zhang, Z. J., Zhuang, J. L., Zhou, Y. B. and Jiang, Q. W. (2006). Potential impact of climate changes on spatial distribution of schistosomiasis in China [in Chinese]. Science & Technology Review 24, 58–60.Google Scholar
Pullan, R. L., Bethony, J. M., Geiger, S. M., Cundill, B., Correa-Oliveira, R., Quinnell, R. J. and Brooker, S. (2008). Human helminth co-infection: analysis of spatial patterns and risk factors in a brazilian community. PLoS Neglected Tropical Diseases 2, e352.CrossRefGoogle Scholar
Raso, G., Li, Y., Zhao, Z., Balen, J., Williams, G. M. and McManus, D. P. (2009). Spatial distribution of human Schistosoma japonicum infections in the Dongting Lake Region, China. PLoS One 4, e6947. doi:10.1371/journal.pone.0006947.CrossRefGoogle ScholarPubMed
Raso, G., Matthys, B., N'Goran, E. K., Tanner, M., Vounatsou, P. and Utzinger, J. (2005). Spatial risk prediction and mapping of Schistosoma mansoni infections among schoolchildren living in western Cote d'Ivoire. Parasitology 131, 1–12.CrossRefGoogle ScholarPubMed
Steinmann, P., Keiser, J., Bos, R., Tanner, M. and Utzinger, J. (2006). Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infectious Diseases 6, 411–425.CrossRefGoogle ScholarPubMed
Steinmann, P., Zhou, X. N., Matthys, B., Li, Y. L., Li, H. J., Chen, S. R., Yang, Z., Fan, W., Jia, T. W., Vounatsou, P. and Utzinger, J. (2007). Spatial risk profiling of Schistosoma japonicum in Eryuan county, Yunnan province, China. Geospatial Health 2, 59–73.CrossRefGoogle ScholarPubMed
Utzinger, J., Booth, M., N'Goran, E. K., Muller, I., Tanner, M. and Lengeler, C. (2001). Relative contribution of day-to-day and intra-specimen variation in faecal egg counts of Schistosoma mansoni before and after treatment with praziquantel. Parasitology 122, 537–554.CrossRefGoogle ScholarPubMed
Wang, L. D., Chen, H. G., Guo, J. G., Zeng, X. J., Hong, X. L., Xiong, J. J., Wu, X. H., Wang, X. H., Wang, L. Y., Xia, G., Hao, Y., Chin, D. P. and Zhou, X. N. (2009). A Strategy to Control Transmission of Schistosoma japonicum in China. New England Journal of Medicine 360, 121–128.CrossRefGoogle ScholarPubMed
Williams, G. M., Sleigh, A. C., Li, Y. S., Feng, Z., Davis, G. M., Chen, H. G., Ross, A. G. P., Bergquist, R. and McManus, D. P. (2002). Mathematical modelling of schistosomiasis japonica: comparison of control strategies in the People's Republic of China. Acta Tropica 82, 253–262.CrossRefGoogle ScholarPubMed
Wu, X. H., Wang, X. H., Utzinger, J., Yang, K., Kristensen, T. K., Berquist, R., Zhao, G. M., Dang, H. and Zhou, X. N. (2007) Spatio-temporal correlation between human and bovine schistosomiasis in China: insight from three national sampling surveys. Geospatial Health 2, 75–84.CrossRefGoogle Scholar
Yang, G. J., Vounatsoub, P., Zhou, X. N., Tanner, M. and Utzinger, J. (2005). A Bayesian-based approach for spatio-temporal modeling of county level prevalence of Schistosoma japonicum infection in Jiangsu province, China. International Journal for Parasitology 35, 155–162.CrossRefGoogle ScholarPubMed
Yang, J. Z., Zhao, Z. Y., Li, Y. S., Krewski, D. and Shi, W. W. (2009). A multi-level analysis of risk factors for Schistosoma japonicum infection in China. International Journal of Infectious Diseases 13, e407–e412.CrossRefGoogle ScholarPubMed
Yu, J. M., de Vlas, S. J., Jiang, Q. W. and 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. Parasitology International 56, 45–49.CrossRefGoogle ScholarPubMed
Zhang, Z. J., Carpenter, T. E., Chen, Y., Clark, A. B., Lynn, H. S., Peng, W. X., Zhou, Y. B., Zhao, G. M. and Jiang, Q. W. (2008). Identifying high-risk regions for schistosomiasis in Guichi, China: A spatial analysis. Acta Tropica 107, 217–223.CrossRefGoogle Scholar
Zhang, Z. J., Carpenter, T. E., Lynn, H. S., Chen, Y., Bivand, R., Clark, A. B., Hui, F. M., Peng, W. X., Zhou, Y. B., Zhao, G. M. and Jiang, Q. W. (2009 a). Location of active transmission sites of Schistosoma japonicum in lake and marshland regions in China. Parasitology 136, 737–746.CrossRefGoogle ScholarPubMed
Zhang, Z. J., Clark, A. B., Bivand, R., Chen, Y., Carpenter, T. E., Peng, W. X., Zhou, Y. B., Zhao, G. M. and Jiang, Q. W. (2009 b). Nonparametric spatial analysis to detect high risk regions for schistosomiasis in Guichi, China. Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 1045–1052. doi:10.1016/j.trstmh.2008.11.012.CrossRefGoogle ScholarPubMed
Zhou, X. N., Wang, L. Y., Chen, M. G., Wu, X. H., Jiang, Q. W., Chen, X. Y., Zheng, J. and Utzinger, J. (2005). The public health significance and control of schistosomiasis in China – then and now. Acta Tropica 96, 97–105.CrossRefGoogle Scholar
Zhou, X. N., Guo, J. G., Wu, X. H., Jiang, Q. W., Zheng, J., Dang, H., Wang, X. H., Xu, J., Zhu, H. Q., Wu, G. L., Li, Y. S., Xu, X. J., Chen, H. G., Wang, T. P., Zhu, Y. C., Qiu, D. C., Dong, X. Q., Zhao, G. M., Zhang, S. J., Zhao, N. Q., Xia, G., Wang, L. Y., Zhang, S. Q., Lin, D. D., Chen, M. G. and Hao, Y. (2007 a). Epidemiology of schistosomiasis in the People's Republic of China, 2004. Emerging Infectious Diseases 13, 1470–1476.CrossRefGoogle ScholarPubMed
Zhou, Y. B., Yang, M. X., Wang, Q. Z., Zhao, G. M., Wei, J. G., Peng, W. X. and Jiang, Q. W. (2007 b). Field comparison of immunodiagnostic and parasitological techniques for the detection of schistosomiasis japonica in the people's republic of China. American Journal of Tropical Medicine and Hygiene 76, 1138–1143.CrossRefGoogle ScholarPubMed
Zhou, Y. B., Zhao, G. M. and Jiang, Q. W. (2007 c). Effects of the praziquantel-based control of schistosomiasis japonica in China. Annals of Tropical Medicine and Parasitology 101, 695–703.CrossRefGoogle ScholarPubMed