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Rodents, goats and dogs – their potential roles in the transmission of schistosomiasis in China

Published online by Cambridge University Press:  22 June 2017

CLARE F. VAN DORSSEN ,
CATHERINE A. GORDON ,
YUESHENG LI ,
GAIL M. WILLIAMS ,
YUANYUAN WANG ,
ZHENHUA LUO ,
GEOFFREY N. GOBERT ,
HONG YOU ,
DONALD P. MCMANUS  and
DARREN J. GRAY
CLARE F. VAN DORSSEN
Affiliation:
Molecular Parasitology Laboratory, Infectious Diseases Division, QIMR Berghofer Medical Research Institute, Brisbane, Australia School of Biomedical Sciences, University of Queensland, Brisbane, Australia
CATHERINE A. GORDON
Affiliation:
Molecular Parasitology Laboratory, Infectious Diseases Division, QIMR Berghofer Medical Research Institute, Brisbane, Australia
YUESHENG LI
Affiliation:
Molecular Parasitology Laboratory, Infectious Diseases Division, QIMR Berghofer Medical Research Institute, Brisbane, Australia Hunan Institute of Parasitic Diseases, Yueyang, Hunan, China
GAIL M. WILLIAMS
Affiliation:
School of Public Health, University of Queensland, Brisbane, Australia
YUANYUAN WANG
Affiliation:
Hunan Institute of Parasitic Diseases, Yueyang, Hunan, China
ZHENHUA LUO
Affiliation:
Hunan Institute of Parasitic Diseases, Yueyang, Hunan, China
GEOFFREY N. GOBERT
Affiliation:
Molecular Parasitology Laboratory, Infectious Diseases Division, QIMR Berghofer Medical Research Institute, Brisbane, Australia School of Biological Sciences, Queen's University Belfast, Belfast, United Kingdom
HONG YOU
Affiliation:
Molecular Parasitology Laboratory, Infectious Diseases Division, QIMR Berghofer Medical Research Institute, Brisbane, Australia
DONALD P. MCMANUS*
Affiliation:
Molecular Parasitology Laboratory, Infectious Diseases Division, QIMR Berghofer Medical Research Institute, Brisbane, Australia
DARREN J. GRAY*
Affiliation:
Molecular Parasitology Laboratory, Infectious Diseases Division, QIMR Berghofer Medical Research Institute, Brisbane, Australia School of Public Health, University of Queensland, Brisbane, Australia Research School of Population Health, College of Medicine, Biology and Environment, The Australian National University, Canberra, Australia
*
*Corresponding authors: Molecular Parasitology Laboratory, Infectious Diseases Division, QIMR Berghofer Medical Research Institute, Brisbane, Australia. E-mail: darren.gray@anu.edu.au and donM@qimr.edu.au
*Corresponding authors: Molecular Parasitology Laboratory, Infectious Diseases Division, QIMR Berghofer Medical Research Institute, Brisbane, Australia. E-mail: darren.gray@anu.edu.au and donM@qimr.edu.au
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Summary

Schistosomiasis in China has been substantially reduced due to an effective control programme employing various measures including bovine and human chemotherapy, and the removal of bovines from endemic areas. To fulfil elimination targets, it will be necessary to identify other possible reservoir hosts for Schistosoma japonicum and include them in future control efforts. This study determined the infection prevalence of S. japonicum in rodents (0–9·21%), dogs (0–18·37%) and goats (6·9–46·4%) from the Dongting Lake area of Hunan province, using a combination of traditional coproparasitological techniques (miracidial hatching technique and Kato-Katz thick smear technique) and molecular methods [quantitative real-time PCR (qPCR) and droplet digital PCR (ddPCR)]. We found a much higher prevalence in goats than previously recorded in this setting. Cattle and water buffalo were also examined using the same procedures and all were found to be infected, emphasising the occurrence of active transmission. qPCR and ddPCR were much more sensitive than the coproparasitological procedures with both KK and MHT considerably underestimating the true prevalence in all animals surveyed. The high level of S. japonicum prevalence in goats indicates that they are likely important reservoirs in schistosomiasis transmission, necessitating their inclusion as targets of control, if the goal of elimination is to be achieved in China.

Keywords

Schistosoma japonicumschistosomiasisDongting LakePR ChinagoatsbovinesrodentsdogsqPCRddPCRKKMHT
Type
Special Issue Article
Information
Parasitology , Volume 144 , Special Issue 12: Glasgow encounters with tropical diseases , October 2017 , pp. 1633 - 1642
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Copyright
Copyright © Cambridge University Press 2017 

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Footnotes

†

Authors contributed equally to this work.

References

REFERENCES

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, 1517–1524.CrossRefGoogle ScholarPubMed
Dalton, J. P., Day, S. R., Drew, A. C. and Brindley, P. J. (1997). A method for the isolation of schistosome eggs and miracidia free of contamination host tissues. Parasitology 115, 29–32.Google Scholar
Ebrahim, A., El-Morshedy, H., Omer, E., El-Daly, S. and Barakat, R. (1997). Evaluation of the Kato-Katz smear and formol ether sedimentation techniques for quantitative diagnosis of Schistosoma mansoni infection. American Journal of Tropical Medicine and Hygiene 57, 706–708.CrossRefGoogle ScholarPubMed
Encylopedia Britannica (2013). Feces, Britannica, E. o. E.s, 2013, http://www.britannica.com/EBchecked/topic/203293/feces.Google Scholar
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.Google Scholar
Glinz, D., Silué, K. D., Knopp, S., Lohouringnon, L. K., Yao, K. P., Steinmann, P., Rinaldi, L., Cringoli, G., N'Goran, E. K. and Utzinger, J. (2010). Comparing diagnostic accuracy of Kato-Katz, koga agar plate, ether-concentration, and FLOTAC for Schistosoma mansoni and soli-transmitted helminths. PLoS Neglected Tropical Diseases 4, e754.Google Scholar
Gordon, C. A., Acosta, L. P., Gray, D. J., Olveda, R., Jarilla, B., Gobert, G. N., Ross, A. G. and McManus, D. P. (2012). High prevalence of Schistosoma japonicum infection in carabao from Samar province, the Philippines: implications for transmission and control. PLoS Neglected Tropical Diseases 6, e1778.Google Scholar
Gordon, C. A., Acosta, L. P., Gobert, G. N., Jiz, M., Olveda, R. M., Ross, A. G., Gray, D. J., Williams, G. M., Harn, D., Yuesheng, L. and McManus, D. P. (2015 a). High prevalence of Schistosoma japonicum and Fasciola gigantica in bovines from Northern Samar, the Philippines. PLoS Neglected Tropical Diseases 9, e0003108.CrossRefGoogle ScholarPubMed
Gordon, C. A., Acosta, L. P., Gobert, G. N., Olveda, D. M., Ross, A. G., Williams, G. M., Gray, D. J., Harn, D., Yuesheng, L. and McManus, D. P. (2015 b). Real-time PCR demonstrates high human prevalence of Schistosoma japonicum in the Philippines: implications for surveillance and control. PLoS Neglected Tropical Diseases 9, e0003483.Google Scholar
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, 866–874.Google Scholar
Gray, D. J., Williams, G. M., Li, Y. and McManus, D. P. (2008). Transmission dynamics of Schistosoma japonicum in the lakes and marshlands of China. PLoS ONE 3, e4058.Google Scholar
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). A cluster-randomised intervention trial against Schistosoma japonicum in the Peoples’ Republic of China: bovine and human transmission. PLoS ONE 4, e5900.Google Scholar
Gray, D. J., Williams, G. M., Li, Y. S., Chen, H. G., Forsyth, S., Li, R., Barnett, A., Guo, J. G., Ross, A., Feng, Z. and McManus, D. P. (2009 b). The role of bovines in human Schistosoma japonicum infection in the People's Republic China. American Journal of Tropical Medicine and Hygiene 81, 1046.Google Scholar
Gray, D. J., Thrift, A. P., Williams, G. M., Zheng, F., Li, Y.-S., Guo, J., Chen, H., Wang, T., Xu, X. J., Zhu, R., Zhu, H., Cao, C. L., Lin, D. D., Zhao, Z. Y., Li, R. S., Davis, G. M. and McManus, D. P. (2012). Five-Year longitudinal assessment of the downstream impact on schistosomiasis transmission following closure of the three gorges dam. PLoS Neglected Tropical Disease 6, e1588.CrossRefGoogle ScholarPubMed
Gray, D. J., Li, Y. S., Williams, G. M., Zhao, Z. Y., Harn, D. A., Li, S. M., Ren, M. Y., Feng, Z., Guo, F. Y., Guo, J. G., Zhou, J., Dong, Y. L., Li, Y., Ross, A. G. and McManus, D. P. (2014). A multi-component integrated approach for the elimination of schistosomiasis in the People's Republic of China: design and baseline results of a 4-year cluster-randomised intervention trial. International Journal of Parasitology 44, 659–668.Google Scholar
Guo, J., Ross, A. G., Lin, D., Williams, G. M., Chen, H., 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, 272–278.Google Scholar
Guo, J., Li, Y., Gray, D. J., 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, 335–341.Google Scholar
Guo, Y., Jiang, M., Gu, L., Qiao, Y. and Li, W. (2013). Prevalence of Schistosoma japonicum in wild rodents in five islands of the West Dongting Lake, China. Journal of Parasitology 99, 706–707.Google Scholar
Habtamu, K., Degarege, A., Ye-Ebiyo, Y. and Erko, B. (2011). Comparison of the Kato-Katz and FLOTAC techniques for the diagnosis of soil-transmitted helminth infections. Parasitology International 60, 398–402.Google Scholar
Han, H., Peng, J., Hong, Y., Zhang, M., Han, Y., Fu, Z., Shi, Y., Xu, J., Tao, J. and Lin, J. (2013). Comparison of the differential expression miRNAs in Wistar rats before and 10 days after S. japonicum infection. Parasites & Vectors 6, 1756–3305.Google Scholar
He, Y., Salafsky, B. and Ramaswamy, K. (2001). Host-parasite relationships of Schistosoma japonicum in mammalian hosts. Trends in Parasitology 17, 320–324.Google Scholar
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). 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, 83–87.Google Scholar
Ho, Y. H. and He, Y. X. (1963). On the host specificity of Schistosoma japonicum. Chinese Medical Journal 82, 403–414.Google ScholarPubMed
Jiang, W., Hong, Y., Peng, J., Fu, Z., Feng, X., Liu, J., Shi, Y. and Lin, J. (2010). Study on differences in the pathology, T cell subsets and gene expression in susceptible and non-susceptible hosts infected with Schistosoma japonicum . PLoS ONE 5, e13494.Google Scholar
Jiang, X. P., Liu, G. Q., Ding, J. T., Yang, L. G., Cao, S. X. and Cheng, S. O. (2003). Diversity in six goat populations in the middle and lower Yangtze river valley. Asian-Australasian Journal of Animal Science 16, 277–281.Google Scholar
Jurberg, A. D., de Oliveira, A. A., Lenzi, H. L. and Coelho, P. M. Z. (2008). A new miracidia hatching device for diagnosing schistosomiasis. Memoires Instituto of Oswaldo Cruz 103, 112–114.Google Scholar
Kamiya, H., Tada, Y., Matsuda, H., Tanaka, H., Blas, B. L., Nosenas, J. S. and Santos, A. T. (1980). Annual fluctuation of Schistosoma japonicum infection in field rats, Rattus rattus mindanensis, in Dagami, Leyte, Philippines. The Japanese Journal of Experimental Medicine 50, 375–382.Google 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, 397–400.Google Scholar
Lei, Z. L., Zheng, H., Zhang, L. J., Zhu, R., Xu, Z. M., Xu, J., Fu, Q., Wang, Q., Li, S. Z. and Zhou, X. N. (2014). Endemic status of schistosomiasis in People's Republic of China in 2013. Zhongguo xue xi chong bing fang zhi za zhi 26, 591–597.Google Scholar
Leiper, R. T. and Atkinson, E. L. (1915). Observations on the spread of Asiatic schistosomiasis. British Medical Journal 1, 201–203.Google Scholar
Li, H., Dong, G. D., Liu, J. M., Gao, J. X., Shi, Y. J., Zhang, Y. G., Jin, Y. M., Lu, K., Cheng, G. F. and Lin, J. J. (2015). Elimination of Schistosomiasis japonica from formerly endemic areas in mountainous regions of southern China using a praziquantel regimen. Veterinary Parasitology 208, 254–258.Google Scholar
Li, M. H., Li, K. and Zhao, S. H. (2004). Diversity of Chinese indigenous goat breeds: a conservation perspective – a review. Asian-Australasian Journal of Animal Science 17, 726–732. doi: 10.5713/ajas.2004.726.Google Scholar
Li, Y.-S., McManus, D. P., Lin, D.-D., Williams, G. M., Harn, D. A., Ross, A. G., Feng, Z. and Gray, D. J. (2014). The Schistosoma japonicum self-cure phenomenon in water buffaloes: potential impact on the control and elimination of schistosomiasis in China. International Journal of Parasitology 44, 167–171.Google Scholar
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, 139–144.CrossRefGoogle ScholarPubMed
Lier, T., Simonsen, G. S., Haaheim, H., Hjelmevoll, S. O., Vennervald, B. J. and Johansen, M. V. (2006). Novel real-time PCR for detection of Schistosoma japonicum in stool. Southeast Asian Journal of Tropical Medicine and Public Health 37, 257–264.Google Scholar
Liu, J., Zhu, C., Shi, Y., Li, H., Wang, L., Qin, S., Kang, S., Huang, Y., Jin, Y. and Lin, J. (2012). Surveillance of Schistosoma japonicum infection in domestic ruminants in the Dongting Lake region, Hunan province, China. PLoS ONE 7, e31876.Google Scholar
Lu, D., Wang, T., Rudge, J. W., Donnely, C. A., Fang, G. and Webster, J. P. (2010). Contrasting reservoirs for Schistosoma japonicum between marshland and hilly regions in Anhui, China – a two-year longitudinal parasitological survey. Parasitology 137, 99–110.CrossRefGoogle Scholar
McManus, D. P., Li, Y., Gray, D. J. and Ross, A. G. (2009). Conquering ‘snail fever’: schistosomiasis and its control in China. Expert Review of Anti-infective Therapy 7, 473–485.Google Scholar
Peng, J., Han, H., Gobert, G. N., Hong, Y., Jiang, W., Wang, X., Fu, Z., Liu, J., Shi, Y. and Lin, J. (2011). Differential gene expression in Schistosoma japonicum schistosomula from Wistar rats and BALB/c mice. Parasites & Vectors 4, 155.Google Scholar
Ross, A. G. P., Sleigh, A. C., Li, Y., Davis, G. M., Williams, G., 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, 270–279.Google Scholar
Rudge, J. W., Webster, J. P., Lu, D.-B., Wang, T.-P., Fang, G.-R. and Basáñez, M.-G. (2013). Identifying host species driving transmission of Schistosomiasis japonica, a multihost parasite system, in China. Proceedings of the National Academy of Sciences 110, 11457–11462.CrossRefGoogle ScholarPubMed
Sleigh, A., Li, X., Jackson, S. and Huang, K. (1998). Eradication of schistosomiasis in Guangxi, China. Part 1: Setting, strategies, operations, and outcomes 1953-92. Bulletin of the World Health Organization 76, 361–372.Google Scholar
Stothard, J. R., Kabatereine, N. B., Archer, J., Al-Shehri, H., Tchuem-Tchuenté, L. A., Gyapong, M. and Bustinduy, A. L. (2017). A countdown of Robert T. Leiper's lasting legacy on schistosomiasis and a COUNTDOWN on control of neglected tropical diseases. Parasitology, in press.Google Scholar
Su, Z. W., Hu, C. Q., Fu, Y., Cheng, W. and Huang, X. B. (1994). Role of several hosts in transmission of Schistosomiasis japonica in lake region. Chinese Journal of Parasitology and Parasitic Disease 12, 48–51.Google Scholar
Sze, M. A., Abbasi, M., Hogg, J. C. and Sin, D. D. (2014). A Comparison between droplet digital and quantitative PCR in the analysis of bacterial 16S load in lung tissue samples from control and COPD GOLD 2. PLoS ONE 9, e110351.Google Scholar
Verwaerde, C., Joseph, M., Capron, M., Pierce, R. J., Damonneville, M., Velge, F., Auriault, C. and Capron, A. (1987). Functional properties of a rat monoclonal IgE antibody specific for Schistosoma mansoni . Journal of Immunology 138, 4441–4446.Google Scholar
Wang, L., Chen, H., Guo, J., Zeng, X., Hong, X., Xiong, J., Wu, X., Wang, X., Wang, L., Xia, G., Hao, Y., Chin, D. P. and Zhou, X. (2009). A strategy to control transmission of Schistosoma japonicum in China. New England Journal of Medicine 360, 121–128.Google Scholar
Wang, Q. Z., Wang, T. P. and Zhang, S. Q. (2013). [Research progress on transmission capacity of reservoir host of Schistosoma japonicum]. Zhongguo xue xi chong bing fang zhi za zhi = ChineseJournal of Schistosomiasis Control 25, 86–89.Google Scholar
Wang, T., Johansen, M. V., Zhang, S., Wang, F., Wu, W., Zhang, G., Pan, X., Ju, Y. and Ørnbjerg, N. (2005). Transmission of Schistosoma japonicum by humans and domestic animals in the Yangtze River valley, Anhui province, China. Acta Tropica 96, 198–204.CrossRefGoogle ScholarPubMed
Wang, W., Dai, J. R. and Liang, Y. S. (2014). Apropos: factors impacting on progress towards elimination of transmission of Schistosomiasis japonica in China. Parasites & Vectors 7, 408.Google Scholar
Weerakoon, K. G., Gordon, C. A., Gobert, G. N., Cai, P. and McManus, D. P. (2016). Optimisation of a droplet digital PCR assay for the diagnosis of Schistosoma japonicum infection: a duplex approach with DNA binding dye chemistry. Journal of Microbiological Methods 125, 19–27.Google Scholar
Weerakoon, K. G., Gordon, C. A., Cai, P., Gobert, G. N., Duke, M., Williams, G. M. and McManus, D. P. (2017). A novel duplex ddPCR assay for the diagnosis of Schistosomiasis japonica: proof of concept in an experimental mouse model. Parasitology, in press.Google Scholar
WHO (2013). Schistosomiasis progress report 2001-2011 and strategic plan 2012-2020. Geneva: World Health Organization, pp. 1–80.Google Scholar
Williams, G., Sleigh, A. C., Li, Y., Feng, Z., Davis, G. M., Chen, H., 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.Google Scholar
Xu, B., Feng, Z., Xu, X. J. and Hu, W. (2011). Evaluation of Kato-Katz technique combined with stool hatching test in diagnosis of Schistosomiasis japonica . Zhongguo xue xi chong bing fang zhi za zhi = Chinese Journal of Schistosomiasis Control 23, 321–323.Google ScholarPubMed
Xu, B., Gordon, C. A., Hu, W., McManus, D. P., Chen, H., Gray, D. J., Ju, C., Zeng, X., Gobert, G. N., Ge, J., Lan, W., Xie, S., Jiang, S., Ross, A. G., Acosta, L. P., Olveda, R. and Feng, Z. (2012). A novel procedure for precise quantification of Schistosoma japonicum eggs in bovine feces. PLoS Neglected Tropical Diseases 6, e1885.Google Scholar
Yang, G. J., Liu, L., Zhu, H. R., Griffiths, S. M., Tanner, M., Bergquist, R., Utzinger, J. and Zhou, X. N. (2014). China's sustained drive to eliminate neglected tropical diseases. Lancet Infectious Diseases 14, 881–892.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, 45–49.Google Scholar
Yu, Q., Wang, Q. Z., Lu, D. B., Wang, F. F., Wu, W. D., Wang, T. P. and Guo, J. G. (2009). [Infectious status of infection sources in the epidemic regions of Schistosomiasis japonica in China]. Zhonghua Yu Fang Yi Xue Za Zhi 43, 309–313.Google Scholar
Zhou, X. N. (2016). [Implementation of precision control to achieve the goal of schistosomiasis elimination in China]. Zhongguo xue xi chong bing fang zhi za zhi = Chinese Journal of Schistosomiasis Control 28, 1–4.Google 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). Epidemiology of schistosomiasis in the People's Republic of China, 2004. Emerging Infectious Diseases 13, 1470–1476.Google Scholar
Zhu, H. Q., Xu, J., Zhu, R., Cao, C. L., Bao, Z. P., Yu, Q., Zhang, L. J., Xu, X. L., Feng, Z. and Guo, J. G. (2014). Comparison of the miracidium hatching test and modified Kato-Katz method for detecting Schistosoma japonicum in low prevalence areas of China. Southeast Asian Journal of Tropical Medicine and Public Health 45, 20–25.Google Scholar
Zou, F. C., Dong, G. D., Yang, J. F., Xie, Y. J., Zhang, Y. G., Duan, G. and Zhu, X. Q. (2010). Prevalences of Schistosoma japonicum infection in reservoir hosts in south-western China. Annals of Tropical Medicine and Parasitology 104, 181–185.Google Scholar