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Immunization and challenge shown by hamsters infected with Opisthorchis viverrini following exposure to gamma-irradiated metacercariae of this carcinogenic liver fluke

Published online by Cambridge University Press:  15 October 2014

A. Papatpremsiri ,
P. Junpue ,
A. Loukas ,
P.J. Brindley ,
J.M. Bethony ,
B. Sripa  and
T. Laha
A. Papatpremsiri
Affiliation:
Graduate School, Khon Kaen University, Khon Kaen40002, Thailand Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen40002, Thailand
P. Junpue
Affiliation:
Department of Radiology, Faculty of Medicine, Khon Kaen University, Khon Kaen40002, Thailand
A. Loukas
Affiliation:
Centre for Biodiscovery and Molecular Development of Therapeutics, Queensland Tropical Health Alliance Laboratory, James Cook University, Cairns, Queensland4878, Australia
P.J. Brindley
Affiliation:
Department of Microbiology, Immunology and Tropical Medicine, and Research Center for Neglected Diseases of Poverty, School of Medicine and Health Sciences, George Washington University, Washington, DC20037, USA
J.M. Bethony
Affiliation:
Department of Microbiology, Immunology and Tropical Medicine, and Research Center for Neglected Diseases of Poverty, School of Medicine and Health Sciences, George Washington University, Washington, DC20037, USA AIDS and Cancer Specimen Resource (ACSR), School of Medicine and Health Sciences, George Washington University, Washington, DC20052, USA
B. Sripa
Affiliation:
Tropical Disease Research Laboratory, Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen40002, Thailand Liver Fluke and Cholangiocarcinoma Research Center, Faculty of Medicine, Khon Kaen University, Khon Kaen40002, Thailand
T. Laha*
Affiliation:
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen40002, Thailand Liver Fluke and Cholangiocarcinoma Research Center, Faculty of Medicine, Khon Kaen University, Khon Kaen40002, Thailand
*
* E-mail: thewa_la@kku.ac.th
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Abstract

Here we report findings to optimize and standardize conditions to attenuate metacercariae of Opisthorchis viverrini by ionizing radiation to elicit protective immune responses to challenge infection. Metacercariae were gamma-irradiated and the ability of irradiated metacercariae to prevent patent infection of challenge metacercariae in hamsters was determined, as well as their ability to induce a host antibody response. Metacercariae irradiated in a dose-dependent manner, with 3, 5, 10, 12, 20, 25 and 50 Gray, were used to infect Syrian golden hamsters by stomach gavage to ascertain the effect of irradiation on ability of the worms to establish infection. In addition, other hamsters were infected with metacercariae irradiated with 20–50 Gray, followed by challenge with intact/wild-type (non-irradiated) metacercariae to determine the protective effect as established by the numbers of adult flukes, eggs of O. viverrini in hamster faeces and anti-O. viverrini antibody titres. Significantly fewer worms were recovered from hamsters immunized with metacercariae irradiated at 20, 25 and 50 Gray than from control hamsters infected with intact metacercariae or 0 Gray, and the worms showed damaged reproductive organs. Faecal egg numbers were decreased significantly in hamsters immunized with 25 and 50 Gray metacercariae of O. viverrini. Moreover, hamsters administered metacercariae that were protected elicited a robust, specific anti-fluke immunoglobulin G response compared to control hamsters, suggesting a role for antibody in protection elicited by radiation-attenuated metacercariae.

Type
Research Papers
Information
Journal of Helminthology , Volume 90 , Issue 1 , January 2016 , pp. 39 - 47
Copyright
Copyright © Cambridge University Press 2014 

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References

Bain, R.K. (1999) Irradiated vaccines for helminth control in livestock. International Journal for Parasitology 29, 185–191.CrossRefGoogle ScholarPubMed
Bhamarapravati, N., Thammavit, W. & Vajrasthira, S. (1978) Liver changes in hamsters infected with a liver fluke of man, Opisthorchis viverrini. American Journal of Tropical Medicine and Hygiene 27, 787–794.CrossRefGoogle ScholarPubMed
Bickle, Q.D. (2009) Radiation-attenuated schistosome vaccination – a brief historical perspective. Parasitology 136, 1621–1632.CrossRefGoogle ScholarPubMed
Bickle, Q.D., Dobinson, T. & James, E.R. (1979) The effects of gamma-irradiation on migration and survival of Schistosoma mansoni schistosomula in mice. Parasitology 79, 223–230.CrossRefGoogle ScholarPubMed
Bouvard, V., Baan, R., Straif, K., Grosse, Y., Secretan, B., El Ghissassi, F., Benbrahim-Tallaa, L., Guha, N., Freeman, C., Galichet, L. & Cogliano, V. (2009) A review of human carcinogens – Part B: biological agents. Lancet Oncology 10, 321–322.CrossRefGoogle ScholarPubMed
Chai, J.Y., Kim, S.J., Kook, J. & Lee, S.H. (1995) Effects of gamma-irradiation on the survival and development of Metagonimus yokogawai metacercariae in rats. Korean Journal of Parasitology 33, 297–303.CrossRefGoogle ScholarPubMed
Elkins, D.B., Haswell-Elkins, M. & Anderson, R.M. (1986) The epidemiology and control of intestinal helminths in the Pulicat Lake region of Southern India. I. Study design and pre- and post-treatment observations on Ascaris lumbricoides infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 774–792.CrossRefGoogle Scholar
Flavell, D.J. & Lucas, S.B. (1983) Promotion of N-nitrosodimethylamine-initiated bile duct carcinogenesis in the hamster by the human liver fluke, Opisthorchis viverrini. Carcinogenesis 4, 927–930.CrossRefGoogle ScholarPubMed
Flavell, D.J., Flavell, S.U. & Field, G.F. (1983) Opisthorchis viverrini: the relationship between egg production, worm size and intensity of infection in the hamster. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 538–545.CrossRefGoogle ScholarPubMed
Flavell, D.J., Pattanapanyasat, K. & Flavell, S.U. (1980) Opisthorchis viverrini: partial success in adoptively transferring immunity with spleen cells and serum in the hamster. Journal of Helminthology 54, 191–197.CrossRefGoogle ScholarPubMed
Fujiwara, R.T., Loukas, A., Mendez, S., Williamson, A.L., Bueno, L.L., Wang, Y., Samuel, A., Zhan, B., Bottazzi, M.E., Hotez, P.J. & Bethony, J.M. (2006) Vaccination with irradiated Ancylostoma caninum third stage larvae induces a Th2 protective response in dogs. Vaccine 24, 501–509.CrossRefGoogle ScholarPubMed
Hotez, P.J., Bethony, J.M., Oliveira, S.C., Brindley, P.J. & Loukas, A. (2008a) Multivalent anthelminthic vaccine to prevent hookworm and schistosomiasis. Expert Review of Vaccines 7, 745–752.CrossRefGoogle ScholarPubMed
Hotez, P.J., Brindley, P.J., Bethony, J.M., King, C.H., Pearce, E.J. & Jacobson, J. (2008b) Helminth infections: the great neglected tropical diseases. Journal of Clinical Investigation 118, 1311–1321.CrossRefGoogle ScholarPubMed
Hsu, S.Y., Hsu, H.F. & Osborn, J.W. (1969) Immunization of rhesus monkeys against schistosome infection by cercariae exposed to high doses of X-radiation. Proceedings of the Society for Experimental Biology and Medicine 131, 1146–1149.CrossRefGoogle ScholarPubMed
Hsu, S.Y., Hsu, H.F., Xu, S.T., Shi, F.H., He, Y.X., Clarke, W.R. & Johnson, S.C. (1983) Vaccination against bovine schistosomiasis japonica with highly X-irradiated schistosomula. American Journal of Tropical Medicine and Hygiene 32, 367–370.CrossRefGoogle ScholarPubMed
Hsu, S.Y., Xu, S.T., He, Y.X., Shi, F.H., Shen, W., Hsu, H.F., Osborne, J.W. & Clarke, W.R. (1984) Vaccination of bovines against schistosomiasis japonica with highly irradiated schistosomula in China. American Journal of Tropical Medicine and Hygiene 33, 891–898.CrossRefGoogle ScholarPubMed
IARC. (2012) Biological agents. Volume 100 B. A review of human carcinogens. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans 100, 1–441.Google Scholar
Jarrett, W.F., Jennings, F.W., McIntyre, W.I., Mulligan, W. & Urquhart, G.M. (1958) Irradiated helminth larvae in vaccination. Proceedings of the Royal Society of Medicine 51, 743–744.CrossRefGoogle ScholarPubMed
Keiser, J., Adelfio, R., Vargas, M., Odermatt, P. & Tesana, S. (2013) Activity of tribendimidine and praziquantel combination therapy against the liver fluke Opisthorchis viverrini in vitro and in vivo. Journal of Helminthology 87, 252–256.CrossRefGoogle ScholarPubMed
Loukas, A., Gaze, S., Mulvenna, J.P., Gasser, R.B., Brindley, P.J., Doolan, D.L., Bethony, J.M., Jones, M.K., Gobert, G.N., Driguez, P., McManus, D.P. & Hotez, P.J. (2011) Vaccinomics for the major blood feeding helminths of humans. OMICS 15, 567–577.CrossRefGoogle ScholarPubMed
Lvova, M.N., Tangkawattana, S., Balthaisong, S., Katokhin, A.V., Mordvinov, V.A. & Sripa, B. (2012) Comparative histopathology of Opisthorchis felineus and Opisthorchis viverrini in a hamster model: an implication of high pathogenicity of the European liver fluke. Parasitology International 61, 167–172.CrossRefGoogle Scholar
Mairiang, E., Laha, T., Bethony, J.M., Thinkhamrop, B., Kaewkes, S., Sithithaworn, P., Tesana, S., Loukas, A., Brindley, P.J. & Sripa, B. (2012) Ultrasonography assessment of hepatobiliary abnormalities in 3359 subjects with Opisthorchis viverrini infection in endemic areas of Thailand. Parasitology International 61, 208–211.CrossRefGoogle ScholarPubMed
McManus, D.P. & Dalton, J.P. (2006) Vaccines against the zoonotic trematodes Schistosoma japonicum, Fasciola hepatica and Fasciola gigantica. Parasitology 133 (Suppl), S43–S61.CrossRefGoogle ScholarPubMed
McManus, D.P. & Loukas, A. (2008) Current status of vaccines for schistosomiasis. Clinical Microbiology Reviews 21, 225–242.CrossRefGoogle ScholarPubMed
Park, G.M. & Yong, T.S. (2003) Effects of gamma-irradiation on the infectivity and chromosome aberration of Clonorchis sinensis. Korean Journal of Parasitology 41, 41–45.CrossRefGoogle ScholarPubMed
Plieskatt, J.L., Deenonpoe, R., Mulvenna, J.P., Krause, L., Sripa, B., Bethony, J.M. & Brindley, P.J. (2013) Infection with the carcinogenic liver fluke Opisthorchis viverrini modifies intestinal and biliary microbiome. FASEB Journal 27, 4572–4584.CrossRefGoogle ScholarPubMed
Prichard, R.K., Basanez, M.G., Boatin, B.A., McCarthy, J.S., Garcia, H.H., Yang, G.J., Sripa, B. & Lustigman, S. (2012) A research agenda for helminth diseases of humans: intervention for control and elimination. PLoS Neglected Tropical Diseases 6, e1549.CrossRefGoogle ScholarPubMed
Quan, F.S., Lee, J.B., Bae, J.S., Ohwatari, N., Min, Y.K. & Yang, H.M. (2005) Resistance to reinfection in rats induced by irradiated metacercariae of Clonorchis sinensis. Memorias do Instituto Oswaldo Cruz 100, 549–554.CrossRefGoogle ScholarPubMed
Saichua, P., Sithithaworn, P., Jariwala, A.R., Deimert, D.J., Sithithaworn, J., Sripa, B., Laha, T., Mairiang, E., Pairojkul, C., Periago, M.V., Khuntikeo, N., Mulvenna, J. & Bethony, J.M. (2013) Microproteinuria during Opisthorchis viverrini infection: a biomarker for advanced renal and hepatobiliary pathologies from chronic opisthorchiasis. PLoS Neglected Tropical Diseases 7, e2228.CrossRefGoogle ScholarPubMed
Sirisinha, S. & Wongratanacheewin, S. (1986) Immunization of hamsters against Opisthorchis viverrini infection. Southeast Asian Journal of Tropical Medicine and Public Health 17, 567–573.Google ScholarPubMed
Sithithaworn, P., Pipitgool, V., Srisawangwong, T., Elkins, D.B. & Haswell-Elkins, M.R. (1997) Seasonal variation of Opisthorchis viverrini infection in cyprinoid fish in north-east Thailand: implications for parasite control and food safety. Bulletin of the World Health Organization 75, 125–131.Google ScholarPubMed
Sithithaworn, P., Andrews, R.H., Nguyen, V.D., Wongsaroj, T., Sinuon, M., Odermatt, P., Nawa, Y., Liang, S., Brindley, P.J. & Sripa, B. (2012) The current status of opisthorchiasis and clonorchiasis in the Mekong Basin. Parasitology International 61, 10–16.CrossRefGoogle ScholarPubMed
Smout, M.J., Sripa, B., Laha, T., Mulvenna, J., Gasser, R.B., Young, N.D., Bethony, J.M., Brindley, P.J. & Loukas, A. (2011) Infection with the carcinogenic human liver fluke, Opisthorchis viverrini. Molecular BioSystems 7, 1367–1375.CrossRefGoogle ScholarPubMed
Soukhathammavong, P., Odermatt, P., Sayasone, S., Vonghachack, Y., Vounatsou, P., Hatz, C., Akkhavong, K. & Keiser, J. (2011) Efficacy and safety of mefloquine, artesunate, mefloquine-artesunate, tribendimidine, and praziquantel in patients with Opisthorchis viverrini: a randomised, exploratory, open-label, phase 2 trial. Lancet Infectious Diseases 11, 110–118.CrossRefGoogle ScholarPubMed
Spitz, D.R., Azzam, E.I., Li, J.J. & Gius, D. (2004) Metabolic oxidation/reduction reactions and cellular responses to ionizing radiation: a unifying concept in stress response biology. Cancer and Metastasis Reviews 23, 311–322.CrossRefGoogle ScholarPubMed
Sripa, B. & Kaewkes, S. (2002) Gall bladder and extrahepatic bile duct changes in Opisthorchis viverrini-infected hamsters. Acta Tropica 83, 29–36.CrossRefGoogle ScholarPubMed
Sripa, B., Bethony, J.M., Sithithaworn, P., Kaewkes, S., Mairiang, E., Loukas, A., Mulvenna, J., Laha, T., Hotez, P.J. & Brindley, P.J. (2011) Opisthorchiasis and Opisthorchis-associated cholangiocarcinoma in Thailand and Laos. Acta Tropica 120 (Suppl 1), S158–S168.CrossRefGoogle ScholarPubMed
Sripa, B., Brindley, P.J., Mulvenna, J., Laha, T., Smout, M.J., Mairiang, E., Bethony, J.M. & Loukas, A. (2012) The tumorigenic liver fluke Opisthorchis viverrini – multiple pathways to cancer. Trends in Parasitology 28, 395–407.CrossRefGoogle ScholarPubMed
Thamavit, W., Kongkanuntn, R., Tiwawech, D. & Moore, M.A. (1987) Level of Opisthorchis infestation and carcinogen dose-dependence of cholangiocarcinoma induction in Syrian golden hamsters. Virchows Archiv. B, Cell Pathology Including Molecular Pathology 54, 52–58.CrossRefGoogle ScholarPubMed
Tian, F., Lin, D., Wu, J., Gao, Y., Zhang, D., Ji, M. & Wu, G. (2010) Immune events associated with high level protection against Schistosoma japonicum infection in pigs immunized with UV-attenuated cercariae. PLoS One 5, e13408.CrossRefGoogle ScholarPubMed
Wongratanacheewin, S., Sermswan, R.W. & Sirisinha, S. (2003) Immunology and molecular biology of Opisthorchis viverrini infection. Acta Tropica 88, 195–207.CrossRefGoogle ScholarPubMed
Yole, D.S., Pemberton, R., Reid, G.D. & Wilson, R.A. (1996) Protective immunity to Schistosoma mansoni induced in the olive baboon Papio anubis by the irradiated cercaria vaccine. Parasitology 112, 37–46.CrossRefGoogle ScholarPubMed
Zhang, Y., Taylor, M.G., Bickle, Q.D., Wang, H. & Ge, J. (1999) Vaccination of mice with gamma-irradiated Schistosoma japonicum cercariae. Parasite Immunology 21, 111–117.CrossRefGoogle ScholarPubMed