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Contrasting reservoirs for Schistosoma japonicum between marshland and hilly regions in Anhui, China – a two-year longitudinal parasitological survey

Published online by Cambridge University Press:  02 September 2009

DA-BING LU*
Affiliation:
Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College, Norfolk Place, London W2 1PG, UK
TIAN-PING WANG
Affiliation:
Anhui Institute of Parasitic Diseases, Wuhu, People's Republic of China
JAMES W. RUDGE
Affiliation:
Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College, Norfolk Place, London W2 1PG, UK
CHRISTL A. DONNELLY
Affiliation:
Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College, Norfolk Place, London W2 1PG, UK
GUO-REN FANG
Affiliation:
Anhui Institute of Parasitic Diseases, Wuhu, People's Republic of China
JOANNE P. WEBSTER
Affiliation:
Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College, Norfolk Place, London W2 1PG, UK
*
*Corresponding author: Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College (St Mary's Campus), Norfolk Place, London W2 1PG, UK. Tel: +020 7594 3819. Fax: +020 7402 3927. E-mail: dabing.lu@imperial.ac.uk

Summary

Schistosoma japonicum remains highly endemic in many counties in China and has recently re-emerged, to a large extent, in previously controlled areas. To test the hypothesis that small rodents and less agriculturally important domestic animals such as dogs and cats may play an important role in the transmission and potential re-emergence of this disease, an annual investigation of S. japonicum among humans, domestic animals and rodents, combined with detailed surveys of the snail intermediate host, was performed across 3 marshland villages and 3 hilly villages in Anhui province of China over 2 consecutive years. The highest infection prevalence and intensity observed across all mammals was in rodents in the hilly region; while in the marshland, bovines were suspected as the main reservoirs. However, relatively high infection prevalence levels were also found in dogs and cats in both regions. Such results may have implications for the current human- and bovine-oriented control policy for this medically and veterinarily important disease, particularly within the hilly regions of mainland China.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Anonymous (1990). Manual of Schistosomiasis Control. Bureau of Endemic Disease Control, Ministry of Health. House of Shanghai Science Technique, Shanghai, China.Google Scholar
Balen, J., Zhao, Z. Y., Williams, G. M., McManus, D. P., Raso, G., Utzinger, J., Zhou, J. and Li, Y. S. (2007). Prevalence, intensity and associated morbidity of Schistosoma japonicum infection in the Dongting Lake region, China. Bulletin of the World Health Organization 85, 519526.CrossRefGoogle ScholarPubMed
Calhoun, J. B. (1962). The Ecology and Sociology of the Norway Rat. U.S. Dept. Health, Education and Welfare, Public Health Service, Bethesda, MD, USA.Google Scholar
Cao, S. Q. and Wu, M. Y. (2004). An investigation of our break of acute schistosomiasis in Shitai county of Anhui. Tropical Diseases and Parasitology 1, 6768.Google Scholar
Carabin, H., Balolong, E., Joseph, L., McGarvey, S. T., Johansen, M. V., Fernandez, T., Willingham, A. L. and Olveda, R. (2005). Estimating sensitivity and specificity of a faecal examination method for Schistosoma japonicum infection in cats, dogs, water buffaloes, pigs, and rats in Western Samar and Sorsogon Provinces, The Philippines. International Journal for Parasitology 35, 15171524. doi: 10.1016/j.ijpara.2005.06.010.CrossRefGoogle ScholarPubMed
Chen, G. X., Wang, M. S., Han, S. M., Ou, N. and He, Z. G. (2004). Observation on the effect of the comprehensive measures of replacing cattle with machine and reconstructing water supply and lavatory to control the transmission of schistosomiasis. Tropical Diseases and Parasitology 4, 342345.Google Scholar
Chen, M. G. (2005). Use of praziquantel for clinical treatment and morbidity control of schistosomiasis japonica in China: a review of 30 years' experience. Acta Tropica 96, 168176.Google Scholar
Cheng, D. J. and Gong, Z. G. (1989). An epidemiological investigation of schistosomiasis in Liantieshan region. Chinese Journal of Schistosomiasis Control 1, 10.Google Scholar
Cheng, P. J., Yong, S. M., Huang, Y. Y. and Liu, J. S. (1994). An investigation and management of the re-emerging schistosomiasis in one village. Chinese Journal of Schistosomiasis Control 6, 112113.Google Scholar
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
Ebihara, K., Shiraishi, R. & Okuma, K. (1998). Hydroxypropyl-modified potato starch increases fecal bile acid excretion in rats. The Journal of Nutrition 128, 848854.CrossRefGoogle ScholarPubMed
Fedorko, J. M. (1999). Schistosoma japonicum in the black rat, Rattus rattus mindanensis, from Leyte, Philippines in relation to Oncomelania snail colonies with reference to other endoparasites. The Southeast Asian Journal of Tropical Medicine and Public Health 30, 343349.Google ScholarPubMed
Feldmeier, H. and Poggensee, G. (1993). Diagnostic techniques in schistosomiasis control. A review. Acta Tropica 52, 205220.CrossRefGoogle ScholarPubMed
Gray, D. J., Williams, G. M., Li, Y., Chen, H., Li, R. S., Forsyth, S. J., Barnett, A. G., Guo, J., Feng, Z. and McManus, D. P. (2007). A cluster-randomized bovine intervention trial against Schistosoma japonicum in the People's Republic of China: design and baseline results. American Journal of Tropical Medicine and Hygiene 77, 866874.CrossRefGoogle ScholarPubMed
Gray, D. J., Williams, G. M., Li, Y., Chen, H., Forsyth, S. J., Li, R. S., Barnett, A. G., Guo, J., Ross, A. G., Feng, Z. and McManus, D. P. (2009). A cluster-randomised intervention trial against Schistosoma japonicum in the Peoples' Republic of China: bovine and human transmission. PLoS ONE 4, e5900. doi:10.1371/journal.pone.0005900.CrossRefGoogle ScholarPubMed
Gui, M., Idris, M. A., Shi, Y. E., Muhling, A. and Ruppel, A. (1991). Reactivity of Schistosoma japonicum and S. mansoni antigen preparations in indirect haemagglutination (IHA) with sera of patients with homologous and heterologous schistosomiasis. Annals of Tropical Medicine and Parasitology 85, 599604.CrossRefGoogle Scholar
Guo, J. G., Cao, C. L., Hu, G. H., Lin, H., Li, D., Zhu, R. and Xu, J. (2005). The role of ‘passive chemotherapy’ plus health education for schistosomiasis control in China during maintenance and consolidation phase. Acta Tropica 96, 177183. doi:10.1016/j.actatropica.2005.07.012.CrossRefGoogle Scholar
Guo, J., Li, Y., Gray, D., Ning, A., Hu, G., Chen, H., Davis, G. M., Sleigh, A. C., Feng, Z., McManus, D. P. and Williams, G. M. (2006). A drug-based intervention study on the importance of buffaloes for human Schistosoma japonicum infection around Poyang Lake, People's Republic of China. American Journal of Tropical Medicine and Hygiene 74, 335341.CrossRefGoogle ScholarPubMed
Guo, J. G., Ross, A. G., Lin, D. D., Williams, G. M., Chen, H. G., Li, Y., Davis, G. M., Feng, Z., McManus, D. P. and Sleigh, A. C. (2001). A baseline study on the importance of bovines for human Schistosoma japonicum infection around Poyang Lake, China. American Journal of Tropical Medicine and Hygiene 65, 272278.CrossRefGoogle Scholar
He, Y., Luo, X., Zhang, X., Yu, X., Lin, J., Li, Y., Li, Y. and Liu, S. (1999 a). Immunological characteristics of natural resistance in Microtus fortis to infection with Schistosoma japonicum. Chinese Medicine Journal (Engl) 112, 649654.Google ScholarPubMed
He, Y. K., Li, Y., Liu, S. X., Luo, X. S., Yu, X. L., Lin, J. L., Zhang, X. Y., Yu, D. B. and McManus, D. P. (1999 b). Natural antibodies in Microtus fortis react with antigens derived from four stages in the life-cycle of Schistosoma japonicum. Annals of Tropical Medicine and Parasitology 93, 8387.Google ScholarPubMed
Ho, Y. H. (1963). On the host specificity of Schistosoma japonicum. Chinese Medicine Journal 82, 405414.Google ScholarPubMed
Jha, P. K. (2003). Health and social benefits from improving community hygiene and sanitation: an Indian experience. International Journal of Environmental Health Research 13 (Suppl), S133S140. doi:10.1080/0960312031000102895.CrossRefGoogle ScholarPubMed
Johansen, M. V., Bogh, H. O., Nansen, P. and Christensen, N. O. (2000). Schistosoma japonicum infection in the pig as a model for human schistosomiasis japonica. Acta Tropica 76, 8599.CrossRefGoogle Scholar
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, 397400.Google ScholarPubMed
Li, Y. S., Zhao, Z. Y., Ellis, M. and McManus, D. P. (2005). Applications and outcomes of periodic epidemiological surveys for schistosomiasis and related economic evaluation in the People's Republic of China. Acta Tropica 96, 266275. doi:10.1016/j.actatropica.2005.07.020.CrossRefGoogle ScholarPubMed
Liang, S., Spear, R. C., Seto, E., Hubbard, A. and Qiu, D. (2005). A multi-group model of Schistosoma japonicum transmission dynamics and control: Model calibration and control prediction. Tropical Medicine & International Health 10, 263278. doi:10.1111/j.1365-3156.2005.01386.x.CrossRefGoogle ScholarPubMed
Liang, S., Yang, C., Zhong, B. and Qiu, D. (2006). Re-emerging schistosomiasis in hilly and mountainous areas of Sichuan, China. Bulletin of the World Health Organization 84, 139144. doi:/S0042-96862006000200015.CrossRefGoogle ScholarPubMed
Mao, S. P. (1990). Schistosome Biology and Control of Schistosomiasis. Publishing House for People's Health, Beijing, China.Google Scholar
McGarvey, S. T., Carabin, H., Balolong, E. Jr., Belisle, P., Fernandez, T., Joseph, L., Tallo, V., Gonzales, R., Tarafder, M. R., Alday, P., Willingham, A. L. and Olveda, R. (2006). Cross-sectional associations between intensity of animal and human infection with Schistosoma japonicum in Western Samar province, Philippines. Bulletin of the World Health Organization 84, 446452. doi:S0042-96862006000600013.CrossRefGoogle ScholarPubMed
McManus, D. P. and Bartley, P. B. (2004). A vaccine against Asian schistosomiasis. Parasitology International 53, 163173. doi:10.1016/j.parint.2004.01.006.CrossRefGoogle ScholarPubMed
Meehan, A. P. (1984). Rats and mice: their biology and control. Rentokil Limited, Tonbridge, Kent, UK.Google Scholar
Minggang, C. and Zheng, F. (1999). Schistosomiasis control in China. Parasitology International 48, 1119.CrossRefGoogle ScholarPubMed
Mitchell, G. F., Garcia, E. G., Wood, S. M., Diasanta, R., Almonte, R., Calica, E., Davern, K. M. and Tiu, W. U. (1990). Studies on the sex ratio of worms in schistosome infections. Parasitology 101, 2734.CrossRefGoogle ScholarPubMed
Ross, A. G., Sleigh, A. C., Li, Y., Davis, G. M., Williams, G. M., Jiang, Z., Feng, Z. and McManus, D. P. (2001). Schistosomiasis in the People's Republic of China: prospects and challenges for the 21st century. Clinical Microbiology Reviews 14, 270295. doi:10.1128/CMR.14.2.270-295.2001.CrossRefGoogle Scholar
Rudge, J. W., Carabin, H., Balolong, E., Tallo, V., Shrivastava, J., Lu, D. B., Basanez, M. G., Olveda, R., McGarvey, S. T. and Webster, J. P. (2008). Population genetics of Schistosoma japonicum within the Philippines suggest high levels of transmission between humans and dogs. PLoS Neglected Tropical Diseases 2, e340. doi:10.1371/journal.pntd.0000340.CrossRefGoogle ScholarPubMed
Seto, E., Xu, B. and Liang, S. (2002). The use of remote sensing for predictive modelling of schistosomiasis in China. American Society for Photogrammetry and Remote Sensing 68, 167174.Google Scholar
Shrivastava, J., Barker, G. C., Johansen, M. V., Zhou, X. N. and Aligui, G. D. (2003). Isolation and characterization of polymorphic DNA microsatellite markers from Schistosoma japonicum. Molecular Ecology Notes 3, 406408.CrossRefGoogle Scholar
Shrivastava, J., Qian, B. Z., McVean, G. and Webster, J. P. (2005). An insight into the genetic variation of Schistosoma japonicum in mainland China using DNA microsatellite markers. Molecular Ecology 14, 839849. doi:10.1111/j.1365-294X.2005.02443.x.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, 121128. doi:10.1056/NEJMoa0800135.CrossRefGoogle ScholarPubMed
Wang, T. P., Shrivastava, J., Johansen, M. V., Zhang, S. Q., Wang, F. F. and Webster, J. P. (2006 b). Does multiple hosts mean multiple parasites? Population genetic structure of Schistosoma japonicum between definitive host species. International Journal for Parasitology 36, 13171325.CrossRefGoogle ScholarPubMed
Wang, T. P., Vang Johansen, M., Zhang, S. Q., Wang, F. F., Wu, W. D., Zhang, G. H., Pan, X. P., Ju, Y. and Ornbjerg, N. (2005). Transmission of Schistosoma japonicum by humans and domestic animals in the Yangtze River valley, Anhui Province, China. Acta Tropica 96, 198204. doi:10.1016/j.actatropica.2005.07.017.CrossRefGoogle ScholarPubMed
Wang, X. H., Wu, X. H. and Zhou, X. N. (2006 a). Bayesian estimation of community prevalences of Schistosoma japonicum infection in China. International Journal for Parasitology 36, 895902. doi:10.1016/j.ijpara.2006.04.003. doi:10.1016/j.ijpara.2006.06.011.CrossRefGoogle ScholarPubMed
Webster, J. P. and Macdonald, D. W. (1995). Survey of the parasites and pathogens carried by wild brown rats, Rattus norvegicus, on UK farmsteads. Parasitology 111, 247255.CrossRefGoogle Scholar
Wu, K. (1957). Schistosomiasis japonica among domestic and wild animals in China. Chinese Journal of Veterinary 3, 98–100.Google Scholar
Wu, Z. D., Lu, Z. Y. and Yu, X. B. (2005). Development of a vaccine against Schistosoma japonicum in China: a review. Acta Tropica 96, 106116. doi:10.1016/j.actatropica.2005.08.005.CrossRefGoogle Scholar
Xu, G. Y., Tian, J. C., Cheng, G. M., Yang, H. M., Qiu, L., Hu, H. B., Xie, Z. Y., Zhou, F. and Ying, W. G. (1999). Observation on natural focal disease of schistosomiasis in Rattus norvegicus in Nanjing. Chinese Journal of Parasitic Diseases 7, 46.Google Scholar
Yang, G. R., Wu, X., Xiong, M. T., Fan, C., Wu, H. and Tao, K. (2000). Investigation on Schistosoma japonicum infection in rodents in Yunnan Province. Chinese Journal of Parasitology & Parasitic Diseases 18, 232235.Google ScholarPubMed
Yao, B. Y., Zheng, J. and Qian, K. (1989). An epidemiological investigation of S. japonicum in animals in mountainous areas. Chinese Journal of Schistosomiasis Control 1, 13.Google Scholar
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, 4549. doi:10.1016/j.parint.2006.11.002.CrossRefGoogle ScholarPubMed
Yuan, Y., Xu, X. J., Dong, H. F., Jiang, M. S. and Zhu, H. G. (2005). Transmission control of schistosomiasis japonica: implementation and evaluation of different snail control interventions. Acta Tropica 96, 191197. doi:10.1016/j.actatropica.2005.07.014.CrossRefGoogle ScholarPubMed
Zhao, G. M., Zhao, Q., Jiang, Q. W., Chen, X. Y., Wang, L. Y. and Yuan, H. C. (2005). Surveillance for schistosomiasis japonica in China from 2000 to 2003. Acta Tropica 96, 288295. doi:10.1016/j.actatropica.2005.07.023.CrossRefGoogle Scholar
Zheng, J., Bie, S. Z., Gao, H. J., Yang, S. D., Pu, H. Z. and Zhou, Z. B. (1991). The faecal resources of water contamination and the role in transmission of schistosomiasis in mountainous areas. Chinese Journal of Zoonoses 7, 4749.Google Scholar
Zheng, J., Wu, X. H. and Li, Y. S. (1995). Kato-Katz stool examinations in schistosomiasis control of China. Chinese Journal of Schistosomiasis Control 7, 382384.Google Scholar
Zheng, J., Zheng, Q. S., Wang, X. F. and Hua, Z. H. (1997). Influence of livestock husbandry on schistosomiasis transmission in mountainous regions of Yunnan Province. The Southeast Asian Journal of Tropical Medicine and Public Health 28, 291295.Google Scholar
Zheng, J. (2006). The role of animals in Schistosoma japonicum transmission. Chinese Journal of Zoonoses 16, 8788.Google Scholar
Zhou, X. N., Wang, T. P., Wang, L. Y., Guo, J. G., Yu, Q., Xu, J., Wang, R. B., Chen, Z. and Jia, T. W. (2004). The current status of schistosomiasis epidemics in China. Chinese Journal of Epidemiology 25, 555558.Google 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. doi:10.1016/j.actatropica.2005.07.005.CrossRefGoogle ScholarPubMed
Zhu, Y. C. (2005). Immunodiagnosis and its role in schistosomiasis control in China: a review. Acta Tropica 96, 130136. doi:10.1016/j.actatropica.2005.07.007.CrossRefGoogle Scholar