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Susceptibility to praziquantel of male and female cercariae of praziquantel-resistant and susceptible isolates of Schistosoma mansoni

  • Y.-S. Liang (a1) (a2), W. Wang (a1) (a2), J.-R. Dai (a1) (a2), H.-J. Li (a1) (a2), Y.-H. Tao (a1) (a2), J.-F. Zhang (a1) (a2), W. Li (a1) (a2), Y.-C. Zhu (a1) (a2), G.C. Coles (a3) and M.J. Doenhoff (a4)...


Praziquantel (PZQ) is now widely used for the treatment of human schistosomiasis. However, in recent years, there has been a growing concern about the resistance of Schistosoma to PZQ. The mechanisms of PZQ action against Schistosoma and resistance of Schistosoma to PZQ are poorly understood. Here, we report differential susceptibilities to PZQ between male and female cercariae in the PZQ-susceptible and PZQ-resistant isolates of Schistosoma mansoni, using tail loss as a measurement of PZQ action. The miracidia were collected by hatching eggs collected from faeces of infected mice. Single-sex cercaria lines were made by infecting a single Biomphalaria glabrata snail with a single miracidium. The sex of each single-sex cercaria line was identified by a direct W1-specific polymerase chain reaction (PCR) technique. Single-sex cercariae of two isolates were exposed to four different concentrations of PZQ, respectively. The tail shedding of cercariae was observed under a dissecting microscope for five time points up to 100 min after adding PZQ. The results showed that male cercariae have higher tail-shedding rates than that of female cercariae when PZQ-susceptible isolates of S. mansoni are exposed to the same concentration of PZQ. But this phenomenon was not observed in the PZQ-resistant isolates. This sexual differential resistance phenomenon of S. mansoni suggests that resistance to PZQ is induced by decreasing the PZQ susceptibility of male worms. The experiment described here may also be useful for developing tests to detect PZQ resistance in the field.


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Andrews, P. (1978a) Effect of praziquantel on the metabolism of Schistosoma mansoni. pp. 56in Proceedings of the 4th International Congress of Parasitology, Warsaw, Poland.
Andrews, P. (1978b) Effect of praziquantel on the free-living stages of Schistosoma mansoni. Zeitschrift für Parasitenkunde 56, 99106.
Andrews, P. (1985) Praziquantel: mechanisms of anti-schistosomal activity. Pharmacology and Therapeutics 29, 129156.
Andrews, P. & Thomas, H. (1983) Praziquantel. Medicinal Research Reviews 3, 147200.
Aragon, A.D., Imani, R.A., Blackburn, V.R., Cupit, P.M., Melman, S.D., Goronga, T., Webb, T., Loker, E.S. & Cunningham, C. (2009) Towards an understanding of the mechanism of action of praziquantel. Molecular and Biochemical Parasitology 164, 5765.
Becker, B., Mehlhorn, H., Andrews, P., Thomas, H. & Eckert, J. (1980) Light and electron microscopic studies on the effect of praziquantel on Schistosoma mansoni, Dicrocoelium dendriticum and Fasciola hepatica (Trematode) in vitro. Zeitschrift für Parasitenkunde 63, 113128.
Chen, X.Y., Wang, L.Y., Cai, J.M., Zhou, X.N., Zheng, J., Guo, J.G., Wu, X.H., Engels, D. & Chen, M.G. (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.
Christensen, N.Ø., Frandsen, F. & Nansen, P. (1979) The effect of some environmental conditions and final host and parasite-related factors on the penetration of Schistosoma mansoni cercariae into mice. Zeitschrift für Parasitenkunde 59, 267275.
Coles, G.C. (1979) The effect of praziquantel on Schistosoma mansoni. Journal of Helminthology 53, 3133.
Colley, D.G. & Wikel, S.K. (1974) Schistosoma mansoni: simplified method for the production of schistosomules. Experimental Parasitology 35, 4451.
Combes, C. (1982) Proliferation generalize des sporocysters de rang III chez des mollusques parasites par un traitement au praziquantel. (Abstracts of the Fifth International Congress of Parasitology). Molecular and Biochemical Parasitology Suppl. 314.
Davis, A. (1978) Schistosomicides in the developmental stage. pp. 68. Geneva, WHO Expert Committee.
Davis, A. (1993) Antischistosomal drugs and clinical practice. pp. 367404in Jordon, P., Webbe, G. & Sturrock, R.F. (Eds) Human schistosomiasis. Wallingford, UK, CAB International.
Day, T.A., Bennett, J.L. & Pax, R.A. (1992) Praziquantel: the enigmatic antiparasitic. Parasitology Today 8, 342344.
Delgado, V.S., Suarez, D.P., Cesari, I.M. & Incani, R.N. (1992) Experimental chemotherapy of Schistosoma mansoni with praziquantel and oxamniquine: differential effect of single or combined formulations of drug on various strains and on both sex of the parasite. Parasitology Research 78, 648654.
Fallon, P.G. & Doenhoff, M.J. (1994) Drug-resistant schistosomiasis: resistance to praziquentel and oxamniquine induced in Schistosoma mansoni in mice is drug specific. American Journal of Tropical Medicine Hygiene 51, 8388.
Fallon, P.G., Sturrock, R.F., Capron, A., Niang, M. & Doenhoff, M.J. (1995) Diminished susceptibility of praziquantel in a Senegal isolate of Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 53, 6162.
Fallon, P.G., Mubarak, J.S., Fookes, R.E., Niang, M., Butterworth, A.E., Sturrock, R.F. & Doenhoff, M.J. (1997) Schistosoma mansoni: maturation rate and drug susceptibility of different geographic isolates. Experimental Parasitology 86, 2936.
Fetterer, R.H., Pax, R.A., Thompson, D., Brickeb, C. & Bennett, J.L. (1980) Praziquantel: mode of its antischistosomal action. pp. 695698in Bossche, H.V.D. (Ed.) The host invader interplay, Foundation Series 2. Beerse, Belgium, Janssen Research.
Frandsen, F. (1981) Cultivation of schistosomes for chemotherapeutic studies. Acta Pharmacology and Toxicology 49, 118122.
Gasser, R.B. (1992) Sexing schistosome larvae. Parasitology Today 8, 286288.
Gönnert, R. & Andrews, P. (1977) Praziquantel, a new broad-spectrum antischistosomal agent. Zeitschrift für Parasitenkunde 52, 129150.
Grevelding, C.G., Kampkotter, A. & Kunz, W. (1997) Schistosoma mansoni: sexing cercariae by PCR without DNA extraction. Experimental Parasitology 85, 99100.
Gryseels, B., Stelma, F.F., Talla, I., van Dam, G.J., Polman, K., Sow, S., Diaw, M., Sturrock, R.F., Doehring-Schwerdtfeger, E., Kardorff, R., Decam, C., Niang, M. & Deelder, A.M. (1994) Epidemiology, immunology and chemotherapy of Schitosoma mansoni infections in a recently exposed community in Senegal. Tropical and Geographical Medicine 46, 209219.
Guisse, F., Polman, K., Stelma, F.F., Mbaye, A., Talla, I., Niang, M., Deelder, A.M., Ndir, O. & Gryseels, B. (1997) Therapeutic evaluation of two different dose regimens of praziquantel in a recent Schistosoma mansoni focus in northern Senegal. American Journal of Tropical Medicine and Hygiene 56, 511514.
Howells, R.E., Gerken, F.J., Ramalho-Pinto, F.J., Kawazoe, U., Gazzinelli, G. & Pellegrino, J. (1975) Schistosoma mansoni: tail loss in relation to permeability changes during cercaria-schistosomulum transformation. Parasitology 71, 918.
Huang, M.X., Liu, Z.Q. & Kou, Y.Y. (1983) Protective effect of praziquantel against infection with Schistosoma japonicum. Journal of Wuhan Medical College 1, 7779.
Ismail, M.M., Farghaly, A.M., Bruce, J., Tao, L.F. & Bennett, J.L. (1996) Characterization of isolates of Schistosoma mansoni from Egyptian villagers that tolerated high doses of praziquantel. American Journal of Tropical Medicine and Hygiene 55, 214218.
Kumar, V. & Gryseels, B. (1994) Use of praziquantel against schistosomiasis: a review of current status. International Journal of Antimicrobial Agents 4, 313320.
Liang, Y.S., Coles, G.C., Doenhoff, M.J. & Southgate, V.R. (2001) In vitro responses of praziquantel-resistant and -susceptible Schistosoma mansoni to praziquantel. International Journal for Parasitology 31, 12271235.
Liang, Y.S., Coles, G.C., Dai, J.R., Zhu, Y.C. & Doenhoff, M.J. (2002) Adult worm tegumentel damage and egg-granulomas in praziquamtel-resistant and -susceptible Schistosoma mansoni treated in vivo. Journal of Helminthology 76, 327333.
Ramalho-Pinto, F.J., Gazzinelli, G., Howells, R.E., Mota-Santos, T.A., Figueiredo, E.A. & Pellegrino, J. (1974) Schistosoma mansoni: a defined system for the stepwise transformation of the cercariae to schistosomule in vitro. Experimental Parasitology 36, 360366.
Ross, A.G., Sleigh, A.C., Li, Y.S., Davis, G.M., Williams, G.M., Jiang, Z., Feng, Z. & McManus, D.P. (2001) Schistosomiasis in the People's Republic of China: prospects and challenges for the 21st century. Clinical Microbiology Reviews 14, 270295.
Sobhon, P. & Upatham, E.S. (1990) Effect of praziquantel on adult oriental schistosomes. pp. 247270in Sobhon, P. & Upatham, E.S. (Eds) Snails, hosts, life-cycle and tegumental structure of oriental schistosomes. Thailand, Lincol Promotion.
Standen, O.D. (1949) Experimental schistosomiasis. II. Maintenance of Schistosoma mansoni in the laboratory, with some notes on experimental infection with S. haematobium. Annals of Tropical Medicine and Parasitology 43, 268283.
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 Infectious Disease 6, 411425.
Stelma, F.F., Talla, I., Sow, S., Kongs, A., Niang, M., Polman, K., Deelder, A.M. & Gryseels, B. (1995) Efficacy and side effects of praziquantel in an epidemic focus of Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 53, 167170.
Webbe, G., James, C., Nelson, G.S. & Sturrock, R.F. (1981) The effect of praziquantel on Schistosoma haematobium, S. japonicum and S. mansoni in primates. Arzneimittel Forschung Drug Research 31, 542544.
Webster, P., Mansour, T.E. & Bieber, D. (1989) Isolation of a female-specific, highly repeated Schistosoma mansoni DNA probe and its use in an assay of cercarial sex. Molecular and Biochemical Parasitology 34, 11321136.
World Health Organization (1993) The second report of the WHO Expert Committee. World Health Organization Technical Report Series 830. Geneva, WHO.
Xia, M.Y. & Combes, C. (1987) Effect of praziquantel on larval stages of Schistosoma japonicum. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 645650.
Xiao, S.H., Wang, C.Y., Jiao, P.Y., Yu, Y.G. & Yuan, X.J. (1981) Effect of praziquantel on glycogen content and [1-14C] glucose uptake in Schistosoma japonicum. Acta Pharmacologica Sinica 2, 204211.
Xiao, S.H., Catto, B.A. & Webster, L.T. (1985) Effects of praziquantel on different developmental stages of Schistosoma mansoni in vitro and in vivo. Journal of Infectious Diseases 151, 11301137.
Xiao, S.H., Xue, H.C., Yue, W.J., Qiu, L.S. & Mei, J.Y. (1987a) Conversion of Schistosoma japonicum cercariae to schistosomula under the action of praziquantel. Chinese Journal of Parasitology and Parasitic Diseases 5, 133135.
Xiao, S.H., Yue, W.J., Mei, J.Y. & Zhang, R.Q. (1987b) Effect of praziquantel on Schistosoma japonicum cercariae. Acta Pharmacologica Sinica 8, 358362.
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. & Hao, Y. (2007) Epidemiology of schistosomiasis in the People's Republic of China, 2004. Emerging Infectious Diseases 13, 14701476.


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