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Resistance to niclosamide in Oncomelania hupensis, the intermediate host of Schistosoma japonicum: should we be worried?

Published online by Cambridge University Press:  08 July 2014

JIAN-RONG DAI
Affiliation:
Jiangsu Institute of Parasitic Diseases, 117 Yangxiang, Meiyuan, Wuxi City, Jiangsu Province, 214064, People's Republic of China Key Laboratory on Technology for Parasitic Disease Prevention and Control, Ministry of Health, 117 Yangxiang, Meiyuan, Wuxi City, Jiangsu Province, 214064, People's Republic of China Jiangsu Provincial Key Laboratory of Molecular Biology of Parasites, 117 Yangxiang, Meiyuan, Wuxi City, Jiangsu Province, 214064, People's Republic of China
YOU-ZI LI
Affiliation:
Jiangsu Institute of Parasitic Diseases, 117 Yangxiang, Meiyuan, Wuxi City, Jiangsu Province, 214064, People's Republic of China Key Laboratory on Technology for Parasitic Disease Prevention and Control, Ministry of Health, 117 Yangxiang, Meiyuan, Wuxi City, Jiangsu Province, 214064, People's Republic of China Jiangsu Provincial Key Laboratory of Molecular Biology of Parasites, 117 Yangxiang, Meiyuan, Wuxi City, Jiangsu Province, 214064, People's Republic of China
WEI WANG*
Affiliation:
Jiangsu Institute of Parasitic Diseases, 117 Yangxiang, Meiyuan, Wuxi City, Jiangsu Province, 214064, People's Republic of China Key Laboratory on Technology for Parasitic Disease Prevention and Control, Ministry of Health, 117 Yangxiang, Meiyuan, Wuxi City, Jiangsu Province, 214064, People's Republic of China Jiangsu Provincial Key Laboratory of Molecular Biology of Parasites, 117 Yangxiang, Meiyuan, Wuxi City, Jiangsu Province, 214064, People's Republic of China
YUN-TIAN XING
Affiliation:
Jiangsu Institute of Parasitic Diseases, 117 Yangxiang, Meiyuan, Wuxi City, Jiangsu Province, 214064, People's Republic of China Key Laboratory on Technology for Parasitic Disease Prevention and Control, Ministry of Health, 117 Yangxiang, Meiyuan, Wuxi City, Jiangsu Province, 214064, People's Republic of China Jiangsu Provincial Key Laboratory of Molecular Biology of Parasites, 117 Yangxiang, Meiyuan, Wuxi City, Jiangsu Province, 214064, People's Republic of China
GUO-LI QU
Affiliation:
Jiangsu Institute of Parasitic Diseases, 117 Yangxiang, Meiyuan, Wuxi City, Jiangsu Province, 214064, People's Republic of China Key Laboratory on Technology for Parasitic Disease Prevention and Control, Ministry of Health, 117 Yangxiang, Meiyuan, Wuxi City, Jiangsu Province, 214064, People's Republic of China Jiangsu Provincial Key Laboratory of Molecular Biology of Parasites, 117 Yangxiang, Meiyuan, Wuxi City, Jiangsu Province, 214064, People's Republic of China
YOU-SHENG LIANG*
Affiliation:
Jiangsu Institute of Parasitic Diseases, 117 Yangxiang, Meiyuan, Wuxi City, Jiangsu Province, 214064, People's Republic of China Key Laboratory on Technology for Parasitic Disease Prevention and Control, Ministry of Health, 117 Yangxiang, Meiyuan, Wuxi City, Jiangsu Province, 214064, People's Republic of China Jiangsu Provincial Key Laboratory of Molecular Biology of Parasites, 117 Yangxiang, Meiyuan, Wuxi City, Jiangsu Province, 214064, People's Republic of China
*
*Corresponding authors: Key Laboratory on Technology for Parasitic Disease Prevention and Control, Ministry of Health, 117 Yangxiang, Meiyuan, Wuxi City, Jiangsu Province, 214064, People's Republic of China. E-mail: wxliangyousheng@163.com or wangweijipd@163.com
*Corresponding authors: Key Laboratory on Technology for Parasitic Disease Prevention and Control, Ministry of Health, 117 Yangxiang, Meiyuan, Wuxi City, Jiangsu Province, 214064, People's Republic of China. E-mail: wxliangyousheng@163.com or wangweijipd@163.com

Summary

As the currently only available molluscicide, niclosamide has been widely used for snail control for over 2 decades in China. There is therefore a concern about the emergence of niclosamide-resistant snail populations following repeated, extensive use of the chemical. The purpose of this study was to investigate the likelihood of niclosamide resistance in Oncomelania hupensis in China. Active adult O. hupensis snails derived from 20 counties of 10 schistosomiasis-endemic provinces of China, of 10 snails in each drug concentration, were immersed in solutions of 1, 0·5, 0·25, 0·125, 0·063, 0·032, 0·016 and 0·008 mg L−1 of a 50% wettable powder of niclosamide ethanolamine salt (WPN) for 24 and 48 h at 25 °C, and the median lethal concentration (LC50) was estimated. Then, the 24- and 48-h WPN LC50 values were compared with those determined in the same sampling sites in 2002. The results indicated that the 24- and 48-h WPN LC50 values for O. hupensis were not significantly different from those determined in 2002 (P = 0·202 and 0·796, respectively). It is concluded that the current sensitivity of O. hupensis to niclosamide has not changed after more than 2 decades of repeated, extensive application in the main endemic foci of China, and there is no evidence of resistance to niclosamide detected in O. hupensis.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Cao, Z. G., Wang, T. P., Zhang, S. Q., Tian, X. G., Zhu, L., Zhang, L. S., Yao, G. X., Jin, W. and Yang, W. P. (2012). Experimental study on the resistance of Oncomelania snails to niclosamide. Journal of Pathogen Biology 7, 352353, 376.Google Scholar
Chen, M. G. and Feng, Z. (1999). Schistosomiasis control in China. Parasitology International 48, 1119.Google Scholar
Collins, C., Xu, J. and Tang, S. (2012). Schistosomiasis control and the health system in P.R. China. Infectious Diseases of Poverty 1, 8.Google Scholar
Dai, J. R., Zhou, X. N., Liang, Y. S., Zhang, Y. P., Jiang, Y. J., Xi, W. P., Huang, Y. X., Chen, C., Huang, M. X. and Zhu, Y. C. (2002 a). Sensitivity of Oncomelania snail to niclosamide in China. Chinese Journal of Parasitology and Parasitic Diseases 20, 101105.Google ScholarPubMed
Dai, J. R., Zhang, Y. P., Jiang, Y. J., Xi, W. P., Yang, G. J. and Liang, Y. S. (2002 b). Studies on standardization of methods for screening molluscicides in laboratory. I. Volume of molluscicidal solution to influence the efficacy. Chinese Journal of Schistosomiasis Control 14, 122124.Google Scholar
Dai, J. R., Xi, W. P., Liang, Y. S. and Zhang, Y. P. (2002 c). Studies on standardization of methods for screening molluscicides in laboratory. II. Quantity of snails used to influence the molluscicidal efficacy. Chinese Journal of Schistosomiasis Control 14, 263265.Google Scholar
Dai, J. R., Liang, Y. S., Zhang, Y. P., Xu, M., Li, H. J. and Zhu, Y. C. (2003). Studies on standardization of methods for screening molluscicides in laboratory. III. Breeding time of snails to influence the evaluation of the molluscicidal efficacy. Chinese Journal of Schistosomiasis Control 15, 346348.Google Scholar
Dai, J., Li, Y., Wang, W., Xing, Y., Qu, G. and Liang, Y. (2014). Sensitivity of Oncomelania hupensis to niclosamide: a nation-wide survey in China. International Journal of Environmental Research and Public Health 11, 30863095.Google Scholar
Davis, G. M., Zhang, Y., Guo, Y. H. and Spolsky, C. M. (1995). Population genetics and systematic status of Oncomelania hupensis (Gastropoda: Pomatiopsidae) throughout China. Malacologia 37, 133156.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, 139146.Google Scholar
Engels, D., Wang, L. Y. and Palmer, K. L. (2005). Control of schistosomiasis in China. Acta Tropica 96, 6768.Google Scholar
Gönnert, R. (1961). Results of laboratory and field trials with the molluscicide Bayer 73. Bulletin of the World Health Organization 25, 483501.Google Scholar
Li, S. Z., Wang, Y. X., Yang, K., Liu, Q., Wang, Q., Zhang, Y., Wu, X. H., Guo, J. G., Bergquist, R. and Zhou, X. N. (2009). Landscape genetics: the correlation of spatial and genetic distances of Oncomelania hupensis, the intermediate host snail of Schistosoma japonicum in mainland China. Geospatial Health 3, 221231.Google Scholar
Li, Y. Z., Xing, Y. T., Li, H. J., Qu, G. L., Wang, W., Wei, J. Y., Liang, Y. S. and Dai, J. R. (2012). Studies on standardization of methods for screening molluscicides in laboratory IV Sensitivity of Oncomelania snails from different months to niclosamide. Chinese Journal of Schistosomiasis Control 24, 3539.Google ScholarPubMed
Mao, C. P. (1990). Biology of Schistosome and Control of Schistosomiasis. People's Medical Publishing House, Beijing, China.Google 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, 473485.Google Scholar
MOH. (2000). Handbook for Schistosomiasis Control in China. Shanghai Scientific and Technology Literature Publishing House, Shanghai, China.Google Scholar
Oliveira-Filho, E. C., De-Carvalho, R. R. and Paumgartten, F. J. (1999). The influence of environmental factors on the molluscicidal activity of Euphorbia milii latex . Journal of Environmental Science and Health (Part B) 34, 289303.Google Scholar
Paulini, E. (1958). Bilharziasis control by application of molluscicides; a review of its present status. Bulletin of the World Health Organization 18, 975988.Google Scholar
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, 411425.CrossRefGoogle ScholarPubMed
Utzinger, J., Zhou, X. N., Chen, M. G. and Bergquist, R. (2005). Conquering schistosomiasis in China: the long march. Acta Tropica 96, 6996.Google Scholar
Wang, L. D., Utzinger, J. and Zhou, X. N. (2008). Schistosomiasis control: experiences and lessons from China. Lancet 372, 17931795.Google Scholar
Wang, L. D., Guo, J. G., Wu, X. H., Chen, H. G., Wang, T. P., Zhu, S. P., Zhang, Z. H., Steinmann, P., Yang, G. J., Wang, S. P., Wu, Z. D., Wang, L. Y., Hao, Y., Bergquist, R., Utzinger, J. and Zhou, X. N. (2009). China's new strategy to block Schistosoma japonicum transmission: experiences and impact beyond schistosomiasis. Tropical Medicine and International Health 14, 14751483.Google Scholar
Webbe, G. (1961). Laboratory and field trials of a new molluscicide, Bayer 73, in Tanganyika. Bulletin of the World Health Organization 25, 525531.Google Scholar
World Health Organization (WHO) (1992). The Role of Mollusciciding in Schistosomiasis Control. Division of Control of Tropical Diseases, Geneva, Switzerland.Google Scholar
Wilke, T., Davis, G. M., Chen, C. E., Zhou, X. N. and Zeng, X. P. (2000). Oncomelania hupensis (Gastropoda: Rissooidea) in eastern China: molecular phylogeny, population structure, and ecology. Acta Tropica 77, 215227.Google Scholar
Wu, X. Y., Yang, L. Q., Zhang, L. H. and Ge, Q. J. (2006). Progress of research on molluscicides. Chinese Journal of Schistosomiasis Control 18, 474476.Google Scholar
Xianyi, C., Liying, W., Jiming, C., Xiaonong, Z., Jiang, Z., Jiagang, G., Xiaohua, W., Engels, D. and Minggang, C. (2005). Schistosomiasis control in China: the impact of a 10-year World Bank Loan Project (1992–2001). Bulletin of the World Health Organization 83, 4348.Google Scholar
Yang, G. J., Sun, L. P., Hong, Q. B., Zhu, H. R., Yang, K., Gao, Q. and Zhou, X. N. (2012). Optimizing molluscicide treatment strategies in different control stages of schistosomiasis in the People's Republic of China. Parasites and Vectors 5, 260.Google Scholar
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.Google Scholar
Zhang, Y. P., Dai, J. R., Huang, Y. X., Xi, W. P. and Jiang, Y. J. (1999). Sensitivity of Oncomelania hupensis to niclosamide after breeding in laboratory. Journal of Practical Parasitic Diseases 7, 162164.Google Scholar
Zhao, Q. P., Jiang, M. S., Littlewood, D. T. and Nie, P. (2010). Distinct genetic diversity of Oncomelania hupensis, intermediate host of Schistosoma japonicum in mainland China as revealed by ITS sequences. PLOS Neglected Tropical Diseases 4, e611.Google Scholar
Zheng, H., Zhang, L. J., Zhu, R., Xu, J., Li, S. Z., Guo, J. G., Xiao, N. and Zhou, X. N. (2012). Schistosomiasis situation in People's Republic of China in 2011. Chinese Journal of Schistosomiasis Control 24, 621626.Google Scholar
Zhou, P. S., Ma, L. and Huang, J. L. (2002). Research progress on molluscicides and their application. Chinese Journal of Vector Biology and Control 13, 231233.Google Scholar
Zhou, X. N. (2005). Science of Oncomelania Snail. Science Press, Beijing, China.Google Scholar
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, 97105.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, 14701476.Google Scholar
Zhou, X. N., Bergquist, R., Leonardo, L., Yang, G. J., Yang, K., Sudomo, M. and Olveda, R. (2010). Schistosomiasis japonica control and research needs. Advances in Parasitology 72, 145178.Google Scholar
Zhou, Y. B., Yang, M. X., Zhao, G. M., Wei, J. G. and Jiang, Q. W. (2007). Oncomelania hupensis (Gastropoda: Rissooidea), intermediate host of Schistosoma japonicum in China: genetics and molecular phylogeny based on amplified fragment length polymorphisms. Malacologia 49, 367382.Google Scholar
Zhu, D., Yao, P. and Bao, Z. (1999). Mollusciciding action and toxicity of bromoacetamide. Chinese Journal of Parasitology and Parasitic Diseases 17, 244246.Google Scholar
Zhu, D., Zhou, X. N., Zhang, S. Q., Zhang, G., Liu, H. X., Lu, D. B., Cai, G. Y., Ni, Q. Z., Cao, Z. G. and Wu, W. D. (2006). Study on the molluscicidal effect of META-Li against Oncomelania hupensis . Chinese Journal of Parasitology and Parasitic Diseases 24, 200203.Google Scholar