Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-28T18:21:37.975Z Has data issue: false hasContentIssue false

Protective capacity of cercarial transformation fluid alone or in combination with crude cercarial antigen against challenge infections of Schistosoma mansoni in mice

Published online by Cambridge University Press:  28 January 2016

M.Z. El Azzouni
Affiliation:
Department of Medical Parasitology, Faculty of Medicine, Alexandria University, Egypt
R.F. Mady*
Affiliation:
Department of Medical Parasitology, Faculty of Medicine, Alexandria University, Egypt
M.R. Gaafar
Affiliation:
Department of Medical Parasitology, Faculty of Medicine, Alexandria University, Egypt
F.M. Arafa
Affiliation:
Department of Medical Parasitology, Faculty of Medicine, Alexandria University, Egypt
A. Elhadidi
Affiliation:
2Department of Clinical Pathology, Faculty of Medicine, Alexandria University, Egypt
*

Abstract

Schistosomiasis is the second major parasitic disease in the world after malaria. It affects 201.5 million cases in Africa alone. The aim of this research was to explore alternative vaccination strategies against experimental schistosomiasis mansoni. We assessed the effect of cercarial transformation fluid (CTF) singly and in combination with crude cercarial antigen (CCA) using alum as an adjuvant. The combined antigens gave the best results, as evidenced by a significant reduction in the worm load (62.07%), tissue egg count (78.16%, 86.46%) in liver and intestine respectively, and hepatic granuloma size (29.96%). Scanning electron microscopy revealed changes in the tegument, in the form of roughness and appearance of vesicles and furrows between the tegumental tubercles. Also, resorption of the ventral sucker and dimples replacing its spines were observed. The female tegument was irregular and its posterior end showed loss of spines and sensory bulbs. Moreover, there was a significant decrease in liver enzymes (alanine transaminase (ALT) and aspartate transaminase (AST)) compared to infected control mice. A significant elevation in CD4+T-lymphocytes, denoting amelioration of the immune status, in mice that received combined antigens was also observed. It can be concluded that combined antigens demonstrate potential as a vaccine against Schistosoma mansoni.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2016 

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

Abath, F.G. & Werkhauser, R.C. (1996) The tegument of Schistosoma mansoni: functional and immunological features. Parasite Immunology 18, 1520.CrossRefGoogle ScholarPubMed
Abdeen, S.H., Reda, E.S., El-Shabasy, E.A. & Ouhtit, A. (2012) Ultrastructural changes of adult Schistosoma mansoni worms recovered from C57BL/6 mice passively immunized with normal and vaccinated rabbit sera in vivo. Parasitology Research 110, 3747.Google Scholar
Abdel-Hafeez, E.H., Ahmad, A.K., Abdulla, A.M., Aabdel-Wahab, S. & Mosalem, F.A. (2012) Therapeutic effect of alpha lipoic acid combined with praziquantel on liver fibrosis induced by Schistosoma mansoni challenged mice. Parasitology Research 111, 577586.Google Scholar
Ashour, A.A., Ahmed, S.A., Maghraby, A.S. & Zahran, H.G. (2004) Immunoprophylactic effect of single and mixed schistosomal antigens on Schistosoma mansoni infected mice. Egyptian Journal of Hospital Medicine 14, 86103.Google Scholar
Boros, D.L. (1989) Immunopathology of Schistosoma mansoni infection. Clinical Microbiology Reviews 2, 250269.CrossRefGoogle ScholarPubMed
Brindley, P.J., Strand, M., Norden, A.P. & Sher, A. (1989) Role of host antibody in the chemotherapeutic action of praziquantel against Schistosoma mansoni: identification of target antigens. Molecular and Biochemical Parasitology 34, 99108.Google Scholar
Capron, A., Riveau, G.J., Bartley, P.B. & McManus, D.P. (2002) Prospects for a schistosome vaccine. Current Drug Targets: Immune, Endocrine and Metabolic Disorders 2, 281290.Google ScholarPubMed
Cheever, A.W. (1968) Conditions affecting the accuracy of potassium hydroxide digestion techniques for counting Schistosoma mansoni eggs in tissues. Bulletin of the World Health Organization 39, 328331.Google ScholarPubMed
Cheever, A.W., Hoffmann, K.F. & Wynn, T.A. (2000) Immunopathology of schistosomiasis mansoni in mice and men. Immunology Today 21, 465466.Google Scholar
Cioli, D. & Pica-Mattoccia, L. (2003) Praziquantel. Parasitology Research 90 (Supp. 1), S3S9.Google Scholar
Curwen, R.S. & Wilson, R.A. (2003) Invasion of skin by schistosome cercariae: some neglected facts. Trends in Parasitology 19, 6366.CrossRefGoogle ScholarPubMed
Daly, L.E., Bourke, G.J. & Mcgilvray, J. (1991) Statistical analysis. Interpretation and uses of medical statistics. Oxford, Blackwell Scientific Publications.Google Scholar
Damian, R.T., Roberts, M.L., Powell, M.R., Clark, J.D., Lewis, F.A. & Stirewalt, M.A. (1984) Schistosoma mansoni egg granuloma size reduction in challenged baboons after vaccination with irradiated cryopreserved schistosomula. Proceedings of the National Academy of Sciences, USA 81, 35523556.CrossRefGoogle ScholarPubMed
Darani, H.Y., Curtis, R.H., McNeice, C., Price, H.P., Sayers, J.R. & Doenhoff, M.J. (1997) Schistosoma mansoni: anomalous immunogenic properties of a 27 kDa larval serine protease associated with protective immunity. Parasitology 115, 237247.Google Scholar
Diab, R.G. (2012) Efficacy of the antimalarial drug mefloquine on Schistosoma mansoni infected mice. PhD thesis, Faculty of Medicine, Alexandria University, Egypt.Google Scholar
Doenhoff, M. & Sayers, J. (2002) Schistosomiasis vaccine. US20020182224 (Patent) 2002.Google Scholar
El Aswad Bel, D., Doenhoff, M.J., El Hadidi, A.S., Schwaeble, W.J. & Lynch, N.J. (2011) Use of recombinant calreticulin and cercarial transformation fluid (CTF) in the serodiagnosis of Schistosoma mansoni . Immunobiology 216, 379385.Google Scholar
Etewa, S.E., Abd El-Aal, N.F., Abdel-Rahman, S.A. & El-Shafey, M.A. (2014) Parasitological evaluation of potential candidate vaccines in Schistosoma mansoni-infected mice. Journal of Parasitology and Vector Biology 6, 2330.Google Scholar
Ewaisha, R.E., Bahey-El-Din, M., Mossallam, S.F., Amer, E.I., Aboushleib, H.M. & Khalil, A.M. (2014) Combination of the two schistosomal antigens Sm14 and Sm29 elicits significant protection against experimental Schistosoma mansoni infection. Experimental Parasitology 145, 5160.Google Scholar
Gabr, N.S., Mowafy, N.M., Ramadan, M.A. & Kamal, A.M. (2010) Protective immunity and immuno-modulation of hepatic immuno-pathology with the combination of human and mice anti-idiotypic vaccine model in Schistosoma mansoni infected mice. El-Minia Medical Bulletin 21, 7689.Google Scholar
Ghendler, Y., Parizade, M., Arnon, R., McKerrow, J.H. & Fishelson, Z. (1996) Schistosoma mansoni: evidence for a 28-kDa membrane-anchored protease on schistosomula. Experimental Parasitology 83, 7382.Google Scholar
Gray, D.J., McManus, D.P., Li, Y., Williams, G.M., Bergquist, R. & Ross, A.G. (2010) Schistosomiasis elimination: lessons from the past guide the future. Lancet Infectious Diseases 10, 733736.Google Scholar
Horowitz, S., Smolarsky, M. & Arnon, R. (1982) Protection against Schistosoma mansoni achieved by immunization with sonicated parasite. European Journal of Immunology 12, 327332.Google Scholar
Ismail, O.A. (2011) Schistosomiasis vaccines: literature review and current status. Parasitology United Journal 4, 137154.Google Scholar
Ivory, C. & Chadee, K. (2004) DNA vaccines: designing strategies against parasitic infections. Genetic Vaccines and Therapy 2, 1725.Google Scholar
Jarnicki, A.G., Conroy, H., Brereton, C., Donnelly, G., Toomey, D., Walsh, K., Sweeney, C., Leavy, O., Fletcher, J., Lavelle, E.C., Dunne, P. & Mills, K.H. (2008) Attenuating regulatory T cell induction by TLR agonists through inhibition of p38 MAPK signaling in dendritic cells enhances their efficacy as vaccine adjuvants and cancer immunotherapeutics. Journal of Immunology 180, 37973806.CrossRefGoogle ScholarPubMed
King, C.H., Dickman, K. & Tisch, D.J. (2005) Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365, 15611569.Google Scholar
Kirkpatrick, L.A. & Feeney, B.C. (2013) A simple guide to IBM SPSS statistics for version 20.0. Student edn. Belmont, California, Wadsworth, Cengage Learning.Google Scholar
Knudsen, G.M., Medzihradszky, K.F., Lim, K.C., Hansell, E. & McKerrow, J.H. (2005) Proteomic analysis of Schistosoma mansoni cercarial secretions. Molecular & Cellular Proteomics 4, 18621875.CrossRefGoogle ScholarPubMed
Kuroda, E., Coban, C. & Ishii, K.J. (2013) Particulate adjuvant and innate immunity: past achievements, present findings, and future prospects. International Reviews of Immunology 32, 209220.Google Scholar
Lowry, O.H., Rosebrough, N.J., Farr, A.L. & Randall, R.J. (1951) Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 265275.CrossRefGoogle ScholarPubMed
McManus, D.P. & Loukas, A. (2008) Current status of vaccines for schistosomiasis. Clinical Microbiology Reviews 21, 225242.Google Scholar
Mosmann, T.R. & Coffman, R.L. (1989) TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annual Review of Immunology 7, 145173.Google Scholar
Mossallam, S.F. (2000) Induction of protective immunity in experimental schistosomiasis by cercarial antigen. MSc thesis, Faculty of Medicine, Alexandria University, Egypt.Google Scholar
Olivier, L. & Stirewalt, M.A. (1952) An efficient method for exposure of mice to cercariae of Schistosoma mansoni . Journal of Parasitology 38, 1923.Google Scholar
Piatier-Tonneau, D., (2002) CD Guide. CD4. In Mason, D., André, P., Bensussan, A., Buckley, C., Civin, C. & Clark, E. et al. (Eds) Leucocyte typing VII. White cell differentiation antigens. Proceedings of the 7th International Workshop and Conference. Harrogate, United Kingdom, 19–23 June. New York, Oxford University Press.Google Scholar
Reda, E.S., Ouhtit, A., Abdeen, S.H. & El-Shabasy, E.A. (2012) Structural changes of Schistosoma mansoni adult worms recovered from C57BL/6 mice treated with radiation-attenuated vaccine and/or praziquantel against infection. Parasitology Research 110, 979992.Google Scholar
Rogers, S.H., Shannon, W.A.J. & Reeder, R.L. (1983) Schistosoma mansoni adults: uptake and incorporation of epimeric monosaccharides by the tegument. Proceedings of the Oklahoma Academy of Science 63, 1220.Google Scholar
Rollinson, D., Knopp, S., Levitz, S., Stothard, J.R., Tchuem Tchuente, L.A., Garba, A., Mohammed, K.A., Schur, N., Person, B., Colley, D.G. & Utzinger, J. (2013) Time to set the agenda for schistosomiasis elimination. Acta Tropica 128, 423440.Google Scholar
Sabah, A.A., Fletcher, C., Webbe, G. & Doenhoff, M.J. (1986) Schistosoma mansoni: chemotherapy of infections of different ages. Experimental Parasitology 61, 294303.Google Scholar
Savioli, L., Engels, D., Roungou, J.B., Fenwick, A. & Endo, H. (2004) Schistosomiasis control. Lancet 363, 658.Google Scholar
Skelly, P.J. & Alan Wilson, R. (2006) Making sense of the schistosome surface. Advances in Parasitology 63, 185284.Google Scholar
Smithers, S.R. & Terry, R.J. (1965) The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of the adult worms. Parasitology 55, 695700.Google Scholar
Soliman, M.F., El Shenawy, N.S. & El Arabi, S.E. (2008) Schistosoma mansoni: melatonin enhances efficacy of cercarial and soluble worm antigens in the induction of protective immunity against infection in the hamster. Experimental Parasitology 119, 291295.Google Scholar
Sulbaran, G., Noya, O., Brito, B., Ballen, D.E. & Cesari, I.M. (2013) Immunoprotection of mice against schistosomiasis mansoni using solubilized membrane antigens. PLoS Neglected Tropical Diseases 7, e2254.Google Scholar
Tendler, M., Pinto, R.M., Oliveira Lima, A., Gebara, G. & Katz, N. (1986) Schistosoma mansoni: vaccination with adult worm antigens. International Journal for Parasitology 16, 347352.Google Scholar
Tinsley, R.C. (1983) Ovoviviparity in platyhelminth life-cycles. Parasitology 86, 161196.Google Scholar
Utzinger, J., Chollet, J., You, J., Mei, J., Tanner, M. & Xiao, S. (2001) Effect of combined treatment with praziquantel and artemether on Schistosoma japonicum and Schistosoma mansoni in experimentally infected animals. Acta Tropica 80, 918.Google Scholar
Utzinger, J., N'Goran, E.K., Caffrey, C.R. & Keiser, J. (2011) From innovation to application: social-ecological context, diagnostics, drugs and integrated control of schistosomiasis. Acta Tropica 120, 121137.CrossRefGoogle ScholarPubMed
Vignali, D.A., Crocker, P., Bickle, Q.D., Cobbold, S., Waldmann, H. & Taylor, M.G. (1989) A role for CD4+but not CD8+ T cells in immunity to Schistosoma mansoni induced by 20 krad-irradiated and Ro 11-3128-terminated infections. Immunology 67, 466472.Google Scholar
WHO. (2015) Schistosomiasis. Fact sheet No 115. World Health Organization Media Centre. Available at http://www.who.int/mediacentre/factsheets/fs115/en/ (accessed accessed 20 January 2016).Google Scholar
Wilson, M.S., Mentink-Kane, M.M., Pesce, J.T., Ramalingam, T.R., Thompson, R. & Wynn, T.A. (2007) Immunopathology of schistosomiasis. Immunology and Cell Biology 85, 148154.Google Scholar
Wilson, R.A. & Coulson, P.S. (2006) Schistosome vaccines: a critical appraisal. Memorias do Instituto Oswaldo Cruz, Rio De Janeiro 101, 1320.CrossRefGoogle ScholarPubMed
Wynn, T.A. & Cheever, A.W. (1995) Cytokine regulation of granuloma formation in schistosomiasis. Current Opinion in Immunology 7, 505511.Google Scholar
Wynn, T.A., Thompson, R.W., Cheever, A.W. & Mentink-Kane, M.M. (2004) Immunopathogenesis of schistosomiasis. Immunological Reviews 201, 156167.Google Scholar
Xiao, S., Binggui, S., Chollet, J. & Tanner, M. (2000) Tegumental changes in 21-day-old Schistosoma mansoni harboured in mice treated with artemether. Acta Tropica 75, 341348.Google Scholar
Yang, Y.Q., Yang, H.Z. & Zhang, C.W. (1986) Histological observations on the effects of artemether, fuvinazole and niridazole on Schistosoma japonicum schistosomulae in the mouse liver. Zhongguo Yao Li Xue Bao . Acta Pharmacologica Sinica 7, 276278.Google Scholar
Zhang, C.W., Xiao, S.H., Utzinger, J., Chollet, J., Keiser, J. & Tanner, M. (2009) Histopathological changes in adult Schistosoma japonicum harbored in mice treated with a single dose of mefloquine. Parasitology Research 104, 14071416.Google Scholar