Hostname: page-component-76fb5796d-vvkck Total loading time: 0 Render date: 2024-04-25T09:19:10.742Z Has data issue: false hasContentIssue false

Contribution of silver ions to the inhibition of infectivity of Schistosoma japonicum cercariae caused by silver nanoparticles

Published online by Cambridge University Press:  24 January 2013

YULI CHENG
Affiliation:
Department of Pathogenic Biology, School of Medicine, Jianghan University, Wuhan, Hubei, People's Republic of China State Key Laboratory for Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, People's Republic of China
XIAO CHEN*
Affiliation:
Department of Pharmacology, School of Pharmacy, Huazhong University of Science and Technology, Wuhan, Hubei, People's Republic of China
WENJIAN SONG
Affiliation:
Department of Pathogenic Biology, School of Medicine, Jianghan University, Wuhan, Hubei, People's Republic of China
ZHENG KONG
Affiliation:
Department of Pathogenic Biology, School of Medicine, Jianghan University, Wuhan, Hubei, People's Republic of China
PEIJING LI
Affiliation:
State Key Laboratory for Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, People's Republic of China
YANQUN LIU
Affiliation:
Department of Pathogenic Biology, School of Medicine, Jianghan University, Wuhan, Hubei, People's Republic of China
*
*Corresponding author: Department of Pharmacology, School of Pharmacy, Huazhong University of Science and Technology, No. 13 Hangkong Road, Wuhan 430030, People's Republic of China. Tel./Fax: +86 27 83692733. E-mail: chenxiao1976@yahoo.com.cn

Summary

Blockage of pathogen transmission through water decontamination is considered an important strategy for the prevention of schistosome infection. Many believe that this strategy is feasible, but it has yet to be achieved. Silver has a long history of use as a disinfectant. With the emergence of nanotechnology, silver can be shaped into nanoparticles which have been found to possess superb antimicrobial activities. In this light, we investigated the effects of silver nanoparticles (AgNPs) on Schistosoma japonicum cercariae. AgNPs rapidly induced cercarial tail-shedding, agitated behaviour and a decrease in cercarial secretion in a dose-dependent manner. Prolonged treatment was found to be cercariocidal, which nevertheless might be attributable to AgNP-induced cercarial tail loss rather than to toxicity. Higher concentrations of AgNPs (125 μg mL−1 and above) completely blocked cercarial infectivity. Despite decreased infectivity, cercariae exposed to lower concentrations of AgNPs for 30 min were still found capable of infecting hosts even without their tails, suggesting that tail loss does not necessarily signify a total loss of infective ability. We also found that silver ions (Ag+) were heavily involved in the observed cercarial responses of AgNPs. Our observations provide insight into the interactions between the larvae of helminth parasites and nanoparticles.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013

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

Andrews, P. (1978). Effect of praziquantel on the free-living stages of Schistosoma mansoni . Zeitschrift für Parasitenkunde 56, 99106.Google Scholar
Bahgat, M., Francklow, K., Doenhoff, M. J., Li, Y. L., Ramzy, R. M., Kirsten, C. and Ruppel, A. (2001). Infection induces antibodies against the cercarial secretions, but not against the cercarial elastases of Schistosoma mansoni, Schistosoma haematobium, Schistosoma japonicum and Trichobilharzia ocellata . Parasite Immunology 23, 557565.Google Scholar
Birrie, H., Balcha, F., Erko, B., Bezuneh, A. and Gemeda, N. (1998). Investigation into the cercariacidal and miracidiacidal properties of Endod (Phytolacca dodecandra) berries (type 44). East African Medical Journal 75, 311314.Google Scholar
Bone, A. J., Colman, B. P., Gondikas, A. P., Newton, K. M., Harrold, K. H., Cory, R. M., Unrine, J. M., Klaine, S. J., Matson, C. W. and Di Giulio, R. T. (2012). Biotic and abiotic interactions in aquatic microcosms determine fate and toxicity of Ag nanoparticles: part 2-toxicity and Ag speciation. Environmental Science and Technology 46, 69256933.Google Scholar
Caffrey, C. R. and Secor, W. E. (2011). Schistosomiasis: from drug deployment to drug development. Current Opinion in Infectious Diseases 24, 410–407.Google Scholar
Cavalcanti, M. G., Araújo, H. R., Paiva, M. H., Silva, G. M., Barbosa, C. C., Silva, L. F., Brayner, F. A. and Alves, L. C. (2009). Ultrastructural and cytochemical aspects of Schistosoma mansoni cercaria. Micron: The International Research and Review Journal for Microscopy 40, 394400.Google Scholar
Cheng, D., Yang, J. and Zhao, Y. (2004). Antibacterial materials of silver nanoparticles application in medical appliances and appliances for daily use. Chinese Medical Equipment Journal 4, 2632.Google Scholar
Cohen, M. S., Stern, J. M., Vanni, A. J., Kelley, R. S., Baumgart, E., Field, D., Libertino, J. A. and Summerhayes, I. C. (2007). In vitro analysis of a nanocrystalline silver-coated surgical mesh. Surgical Infections 8, 397403.Google Scholar
Eissa, M. M., El Bardicy, S. and Tadros, M. (2011). Bioactivity of miltefosine against aquatic stages of Schistosoma mansoni, Schistosoma haematobium and their snail hosts, supported by scanning electron microscopy. Parasite and Vectors 4, 73.Google Scholar
Elechiguerra, J. L., Burt, J. L., Morones, J. R., Camacho-Bragado, A., Gao, X., Lara, H. H. and Yacaman, M. J. (2005). Interaction of silver nanoparticles with HIV-1. Journal of Nanobiotechnology 3, 6.Google Scholar
Haeberlein, S. and Haas, W. (2008). Chemical attractants of human skin for swimming Schistosoma mansoni cercariae. Parasitology Research 102, 657662.Google Scholar
He, D., Dorantes-Aranda, J. J. and Waite, T. D. (2012). Silver nanoparticle–algae interactions: oxidative dissolution, reactive oxygen species generation and synergistic toxic effects. Environmental Science and Technology 46, 87318738.Google Scholar
King, C. L. and Highashi, G. I. (1992). Schistosoma mansoni: silver ion (Ag+) stimulates and reversibly inhibits lipid-induced cercarial penetration. Experimental Parasitology 75, 3139.CrossRefGoogle ScholarPubMed
Lansdown, A. B. (2006). Silver in health care: antimicrobial effects and safety in use. Current Problems in Dermatology 33, 1734.Google Scholar
Liang, S., Seto, E. Y., Remais, J. V., Zhong, B. and Yang, C. (2007). Environmental effects on parasitic disease transmission exemplified by schistosomiasis in western China. Proceedings of the National Academy of Sciences, USA 104, 71107115.Google Scholar
Liang, Y. S., Wang, W., Dai, J. R., Li, H. J. and Tao, Y. H. (2010). Susceptibility to praziquantel of male and female cercariae of praziquantel-resistant and susceptible isolates of Schistosoma mansoni . Journal of Helminthology 84, 202207.Google Scholar
Liu, J. and Hurt, R. H. (2010). Ion release kinetics and particle persistence in aqueous nano-silver colloids. Environmental Science and Technology 44, 21692175.Google Scholar
Melman, S. D., Steinauer, M. L., Cunningham, C., Kubatko, L. S., Mwangi, I. N., Wynn, N. B., Mutuku, M. W., Karanja, D. M., Colley, D. G., Black, C. L., Secor, W. E., Mkoji, G. M. and Loker, E. S. (2009). Reduced susceptibility to praziquantel among naturally occurring Kenyan isolates of Schistosoma mansoni . PLoS Neglected Tropical Diseases 3, e504.Google Scholar
Moloney, N. A., Doenhoff, M. J., Webbe, G. and Hinchcliffe, P. (1982). Studies on the host–parasite relationship of Schistosoma japonicum in normal and immunosuppressed mice. Parasite Immunology 4, 431440.Google Scholar
Navarro, E., Piccapietra, F., Wagner, B., Marconi, F., Kaegi, R., Odzak, N., Sigg, L. and Behra, R. (2008). Toxicity of silver nanoparticles to Chlamydomonas reinhardtii . Environmental Science and Technology 42, 89598964.Google Scholar
Park, S. J., Shin, J. H., Kang, H., Hwang, J. J. and Cho, D. H. (2011). Niclosamide induces mitochondria fragmentation and promotes both apoptotic and autophagic cell death. BMB Reports 44, 517522.Google Scholar
Peak, E., Chalmers, I. W. and Hoffmann, K. F. (2010). Development and validation of a quantitative, high-throughput, fluorescent-based bioassay to detect schistosoma viability. PLoS Neglected Tropical Diseases 4, e759.Google Scholar
Pollini, M., Paladini, F., Catalano, M., Taurino, A., Licciulli, A., Maffezzoli, A. and Sannino, A. (2011). Antibacterial coatings on haemodialysis catheters by photochemical deposition of silver nanoparticles. Journal of Materials Science: Materials in Medicine 22, 20052012.Google Scholar
Ruppel, A., Shi, Y. E. and Moloney, N. A. (1990). Schistosoma mansoni and S. japonicum: comparison of levels of ultraviolet irradiation for vaccination of mice with cercariae. Parasitology 1, 2326.Google Scholar
Russell, A. D. and Hugo, W. B. (1994). Antimicrobial activity and action of silver. Progress in Medicinal Chemistry 31, 351370.Google Scholar
Seil, J. T. and Webster, T. J. (2012). Antimicrobial applications of nanotechnology: methods and literature. International Journal of Nanomedicine 7, 27672781.Google Scholar
Shaw, M. K. and Erasmus, D. A. (1987). Schistosoma mansoni : structural damage and tegumental repair after in vivo treatment with praziquantel. Parasitology 94, 243254.Google Scholar
Short, R. B. and Cartrett, M. L. (1973). Argentophilic “papillae” of Schistosoma mansoni cercariae. Journal of Parasitology 59, 10411059.Google Scholar
Stephen-Haynes, J. and Toner, L. (2007). Assessment and management of wound infection: the role of silver. Journal of Community Nursing 12, S6, S8, S1012.Google Scholar
Stirewalt, M. A. (1959). Isolation and characterization of deposits of secretion from the acetabular gland complex of cercariae of Schistosoma mansoni . Experimental Parasitology 8, 199214.Google Scholar
World Health Organization (2011). Schistosomiasis: number of people treated in 2009. Weekly Epidemiological Record 86, 7380.Google Scholar
Xiao, S. H., Yue, W. J., Mei, J. Y. and Zhang, R. Q. (1987). Effect of praziquantel on Schistosoma japonicum cercariae. Acta Pharmacologica Sinica 8, 358362.Google Scholar
Xiu, Z., Zhang, Q., Puppala, H. L., Colvin, V. L. and Alvarez, P. J. (2012). Negligible particle-specific antibacterial activity of silver nanoparticles. Nano Letters 12, 42714275.Google Scholar

CHENG et al. supplementary movie

Supplementary movie

Download CHENG et al. supplementary movie(Video)
Video 1.5 MB