Hostname: page-component-76fb5796d-r6qrq Total loading time: 0 Render date: 2024-04-25T23:21:40.170Z Has data issue: false hasContentIssue false

Cestode vaccines: origins, current status and future prospects

Published online by Cambridge University Press:  02 February 2007

M. W. LIGHTOWLERS
Affiliation:
Veterinary Clinical Centre, University of Melbourne, 250 Princes Highway, Werribee, Victoria 3030, Australia.

Abstract

Recombinant vaccines have been developed which are highly effective in preventing infection with Taenia ovis in sheep, Taenia saginata in cattle, Taenia solium in pigs and Echinococcus granulosus in livestock animals. T. ovis and T. saginata are economically significant parasites and the commercial success or otherwise of vaccines against them will rely on their economic value. E. granulosus and T. solium are zoonotic parasites that cause cystic hydatid disease and neurocysticercosis, respectively, in humans. Vaccines against these parasites have been developed to assist with the control of transmission of the human diseases rather than for prevention of infections in livestock per se. Regions of high prevalence for cystic hydatid disease and neurocysticercosis occur primarily in the developing world. As a consequence, vaccines against them are of little or no commercially interest – they are Orphan Vaccines. Lack of commercial interest in these vaccines has made public sector support for their development necessary well beyond the research phase trough into completion of commercial scale-up and other more commercially-related assessments. Practical use of the vaccines will require commercial-scale production according to international manufacturing standards. Identifying partners and support in this endeavour is now of prime importance in efforts to achieve the potential of these vaccines as new tools for the control of cystic hydatid disease and neurocysticercosis.

Type
Research Article
Copyright
© 2006 Cambridge University Press

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

Batson, A. ( 2002). The costs and economics of modern vaccine development. Developments in Biologicals 110, 1524.Google Scholar
Biggs, M. W. and Eiselein, J. E. ( 1965). Diffusion chamber studies of allogenic tumor immunity in mice. Cancer Research 25, 18881893.Google Scholar
Boa, M., Mukaratirwa, S., Willingham, A. L. and Johansen, M. V. ( 2003). Regional action plan for combating Taenia solium cysticercosis/taeniosis in Eastern and Southern Africa. Acta Tropica 87, 183186.CrossRefGoogle Scholar
Bogh, H. O., Lightowlers, M. W., Sullivan, N. D., Mitchell, G. F. and Rickard, M. D. ( 1990). Stage-specific immunity to Taenia taeniaeformis infection in mice. A histological study of the course of infection in mice vaccinated with either oncosphere or metacestode antigens. Parasite Immunology 12, 153162.Google Scholar
Bogh, H. O., Rickard, M. D. and Lightowlers, M. W. ( 1988). Studies on stage-specific immunity against Taenia taeniaeformis metacestodes in mice. Parasite Immunology 10, 255264.CrossRefGoogle Scholar
Budke, C. M., Jiamin, Q., Zinsstag, J., Qian, W. and Torgerson, P. R. ( 2004). Use of disability adjusted life years in the estimation of the disease burden of echinococcosis for a high endemic region of the Tibetan plateau. American Journal of Tropical Medicine and Hygiene 71, 5664.Google Scholar
Campbell, D. H. ( 1936). Active immunization of albino rats with protein fractions from Taenia taeniaeformis and its larval form Cysticercus fasciolaris. American Journal of Hygiene 23, 104113.Google Scholar
Carabin, H., Budke, C. M., Cowan, L. D., Willingham, A. L. and Torgerson, P. R. ( 2005). Methods for assessing the burden of parasitic zoonoses: echinococcosis and cysticercosis. Trends in Parasitology 21, 327333.CrossRefGoogle Scholar
Cox, F. E. G. ( 1993). Milestones in parasitology. Parasitology Today 9, 347348.Google Scholar
Dempster, R. P., Berridge, M. V., Harrison, G. B. and Heath, D. D. ( 1991). Echinococcus granulosus: development of an intermediate host mouse model for use in vaccination studies. International Journal for Parasitology 21, 549554.CrossRefGoogle Scholar
Dempster, R. P., Harrison, G. B. L. and Berridge, M. V. ( 1995). Maternal transfer of protection from Echinococcus granulosus infection in sheep. Research in Veterinary Science 58, 197202.CrossRefGoogle Scholar
Dempster, R. P., Robinson, C. M. and Harrison, G. B. ( 1996). Parasite vaccine development: large-scale recovery of immunogenic Taenia ovis fusion protein GST-45W(B/X) from Escherichia coli inclusion bodies. Parasitology Research 82, 291296.CrossRefGoogle Scholar
Eckert, J., Gemmell, M. A., Meslin, F.-X. and Pawlowski, Z. S. ( 2001). WHO/OIE manual on echinococcosis in humans and animals: a public health problem of global concern. WHO/FAO, Paris.
Eckert, J., Gemmell, M. A. and Soulsby, E. J. L. ( 1981). FAO/UNEP/WHO Guidelines for the surveillance, prevention and control of echinococcosis/hydatidosis. World Health Organization, Geneva.
Flisser, A., Gauci, C. G., Zoli, A., Martinez-Ocana, J., Garza-Rodriguez, A., Dominguez-Alpizar, J. L., Maravilla, P., Rodriguez-Canul, R., Avila, G., Aguilar-Vega, L., Kyngdon, C., Geerts, S. and Lightowlers, M. W. ( 2004). Induction of protection against porcine cysticercosis by vaccination with recombinant oncosphere antigens. Infection and Immunity 72, 52925297.CrossRefGoogle Scholar
Froyd, G. and Round, M. C. ( 1959). Infection of cattle with Cysticercus bovis by the injection of oncospheres. Nature 184, 1510.Google Scholar
Garcia, H. H., Gonzalez, A. E., Evans, C. A. and Gilman, R. H. ( 2003). Taenia solium cysticercosis. Lancet 362, 547556.CrossRefGoogle Scholar
Gauci, C. G., Flisser, A. and Lightowlers, M. W. ( 1998). A Taenia solium oncosphere protein homologous to host-protective Taenia ovis and Taenia saginata 18 kDa antigens. International Journal for Parasitology 28, 757760.CrossRefGoogle Scholar
Gauci, C. G., Ito, A. and Lightowlers, M. W. ( 2006). Conservation of the vaccine antigen gene, TSOL18, among genetically variant isolates of Taenia solium. Molecular and Biochemical Parasitology 146, 101104.CrossRefGoogle Scholar
Gauci, C. G. and Lightowlers, M. W. ( 2001). Alternative splicing and sequence diversity of transcripts from the oncosphere stage of Taenia solium with homology to the 45W antigen of Taenia ovis. Molecular and Biochemical Parasitology 112, 173181.CrossRefGoogle Scholar
Gauci, C., Merli, M., Muller, V., Chow, C., Yagi, K., Mackenstedt, U. and Lightowlers, M. W. ( 2002). Molecular cloning of a vaccine antigen against infection with the larval stage of Echinococcus multilocularis. Infection and Immunity 70, 39693972.CrossRefGoogle Scholar
Geerts, S., Kumar, V. and Abbeele, O. V. D. ( 1980). Taenia saginata cysticercosis in slaughter cattle in Belgium. Vlaams Diergeneeskundig Tijdschrift 49, 365374.Google Scholar
Gemmell, M. A. ( 1962 a). Natural and acquired immunity factors inhibiting penetration of some hexacanth embryos through the intestinal barrier. Nature 194, 701702.Google Scholar
Gemmell, M. A. ( 1962 b). Natural and acquired immunity factors interfering with development during the rapid growth phase of Echinococcus granulosus in dogs. Immunology 5, 495503.Google Scholar
Gemmell, M. A. ( 1964 a). Species specificity of the immunogenic complexes of the tapeworm hexacanth embryo. Nature 204, 705707.Google Scholar
Gemmell, M. A. ( 1964 b). Immunological responses of the mammalian host against tapeworm infections. I. Species specificity of hexacanth embryos in protecting sheep against Taenia hydatigena. Immunology 36, 489499.Google Scholar
Gemmell, M. A. ( 1966). Immunological responses of the mammalian host against tapeworm infections. IV. Species specificity of hexacanth embryos in protecting sheep against Echinococcus granulosus. Immunology 11, 325335.Google Scholar
Gemmell, M. A., Blundell Hasell, S. K. and MacNamara, F. N. ( 1969). Immunological responses of the mammalian host against tapeworm infections. IX. The transfer via colostrum of immunity to Taenia hydatigena. Experimental Parasitology 26, 5257.Google Scholar
Gemmell, M. A., Lawson, J. R., Roberts, M. G. and Griffin, J. F. ( 1990). Population dynamics in echinococcosis and cysticercosis: regulation of Taenia hydatigena and T. ovis in lambs through passively transferred immunity. Parasitology 101, 145151.Google Scholar
Gemmell, M. A. and Soulsby, E. J. ( 1968). The development of acquired immunity to tapeworms and progress towards active immunization, with special reference to Echinococcus spp. Bulletin of the World Health Organisation 39, 4555.Google Scholar
Gonzalez, A. E., Gauci, C. G., Barber, D., Gilman, R. H., Tsang, V. C., Garcia, H. H., Verastegui, M. and Lightowlers, M. W. ( 2005). Vaccination of pigs to control human neurocysticercosis. American Journal of Tropical Medicine and Hygiene 72, 837839.Google Scholar
Haffner, M. E. ( 1991). Orphan products: origins, progress, and prospects. Annual Reviews of Pharmacological Toxicology 31, 603620.CrossRefGoogle Scholar
Harrison, G. B., Heath, D. D., Dempster, R. P., Gauci, C., Newton, S. E., Cameron, W. G., Robinson, C. M., Lawrence, S. B., Lightowlers, M. W. and Rickard, M. D. ( 1996). Identification and cDNA cloning of two novel low molecular weight host-protective antigens from Taenia ovis oncospheres. International Journal for Parasitology 26, 195204.CrossRefGoogle Scholar
Heath, D. D. and Smyth, J. D. ( 1970). In vitro cultivation of Echinococcus granulosus, Taenia hydatigena, T. ovis, T. pisiformis and T. serialis from oncosphere to cystic larva. Parasitology 61, 329343.Google Scholar
Heath, D. D. ( 1973 a). Resistance to Taenia pisiformis larvae in rabbits. II. Temporal relationships and the development phase affected. International Journal for Parasitology 3, 491498.Google Scholar
Heath, D. D. ( 1973 b). Resistance to Taenia pisiformis larvae in rabbits. I. Examination of the antigenically protective phase of larval development. International Journal for Parasitology 3, 485489.Google Scholar
Heath, D. D., Jensen, O. and Lightowlers, M. W. ( 2003). Progress in control of hydatidosis using vaccination – a review of formulation and delivery of the vaccine and recommendations for practical use in control programmes. Acta Tropica 85, 133143.CrossRefGoogle Scholar
Heath, D. D. and Lawrence, S. B. ( 1981). Echinococcus granulosus cysts: early development in vitro in the presence of serum from infected sheep. International Journal for Parasitology 11, 261266.CrossRefGoogle Scholar
Heath, D. D. and Lawrence, S. B. ( 1996). Antigenic polypeptides of Echinococcus granulosus oncospheres and definition of protective molecules. Parasite Immunology 18, 347357.CrossRefGoogle Scholar
Heath, D. D., Lawrence, S. B. and Yong, W. K. ( 1979 a). Cross-protection between the cysts of Echinococcus granulosus, Taenia hydatigena and T. ovis in lambs. Research in Veterinary Science 27, 210212.Google Scholar
Heath, D. D., Lawrence, S. B. and Yong, W. K. ( 1992). Echinococcus granulosus in sheep: transfer from ewe to lamb of ‘Arc 5’ antibodies and oncosphere-killing activity, but not protection. International Journal for Parasitology 22, 10171021.CrossRefGoogle Scholar
Heath, D. D., Parmeter, S. N., Osborn, P. J. and Lawrence, S. B. ( 1981). Resistance to Echinococcus granulosus infection in lambs. Journal of Parasitology 67, 797799.CrossRefGoogle Scholar
Heath, D. D., Yong, W. K., Osborn, P. J., Parmeter, S. N., Lawrence, S. B. and Twaalfhoven, H. ( 1979 b). The duration of passive protection against Taenia ovis larvae in lambs. Parasitology 79, 177182.Google Scholar
Heath, D. D., Qi, P., Zhang, Z., Wang, J., Feng, J. and Lightowlers, M. W. ( 2002). Role of immunisation of the intermediate host in hydatid disease control. Report of the PAHO/WHO Working Group on Perspectives and Possibilities of Control and Eradication of Hydatidosis, 144148.
Hillyer, G. V., Chiriboga, J., Menendez-Corrada, R., Pellegrino, J. and Liard, F. ( 1970). An attempt to induce resistance in mice to Schistosoma mansoni infection using millipore diffusion chambers. Revista do Instituto de Medecina Tropical Sâo Paulo 12, 149151.Google Scholar
Huerta, M., De Aluja, A. S., Fragoso, G., Toledo, A., Villalobos, N., Hernandez, M., Gevorkian, G., Acero, G., Diaz, A., Alvarez, I., Avila, R., Beltran, C., Garcia, G., Martinez, J. J., Larralde, C. and Sciutto, E. ( 2001). Synthetic peptide vaccine against Taenia solium pig cysticercosis: successful vaccination in a controlled field trial in rural Mexico. Vaccine 20, 262266.CrossRefGoogle Scholar
Jacobs, H. J., Moriarty, K. M., Charleston, W. A. G. and Heath, D. D. ( 1994). Resistance against Taenia hydatigena in sheep after passive transfer of serum or colostrum. Parasite Immunology 16, 351359.CrossRefGoogle Scholar
Johnson, K. S., Harrison, G. B., Lightowlers, M. W., O'Hoy, K. L., Cougle, W. G., Dempster, R. P., Lawrence, S. B., Vinton, J. G., Heath, D. D. and Rickard, M. D. ( 1989). Vaccination against ovine cysticercosis using a defined recombinant antigen. Nature 338, 585587.CrossRefGoogle Scholar
Kan, K. ( 1934). Immunological studies of Cysticercus fasciolaris. Keio Igaka 14, 663687.Google Scholar
Kanev, I., Petrov, P., Komandarev, S., Boeva, K. V., Kurdova, R., Tanchev, T., Filipov, G. and Dinev, D. ( 1995). Basic helminthological issues in eastern Europe after the democratic changes. Helminthologia 32, 117120.Google Scholar
Kerr, K. B. ( 1935). Immunity against a cestode parasite – Cysticercus pisiformis. American Journal of Hygiene 22, 169182.Google Scholar
Kyngdon, C. T., Gauci, C. G., Rolfe, R. A., Velasquez Guzman, J. C., Farfan Salazar, M. J., Verastegui Pimentel, M. R., Gonzalez, A. E., Garcia, H. H., Gilmanl, R. H., Strugnell, R. A. and Lightowlers, M. W. ( 2006). In vitro oncosphere-killing assays to determine immunity to the larvae of Taenia pisiformis, Taenia ovis, Taenia saginata, and Taenia solium. Journal of Parasitology 92, 273281.CrossRefGoogle Scholar
Lang, J. and Wood, S. C. ( 1999). Development of orphan vaccines: an industry perspective. Emerging Infectious Diseases 5, 749756.CrossRefGoogle Scholar
Lawrence, S. B., Heath, D. D., Harrison, G. B. L., Robinson, C. M., Dempster, R. P., Gatehouse, T. K., Lightowlers, M. W. and Rickard, M. D. ( 1996). Pilot field trial of a recombinant Taenia ovis vaccine in lambs exposed to natural infection. New Zealand Veterinary Journal 44, 155157.CrossRefGoogle Scholar
Lightowlers, M. W., Flisser, A., Gauci, C. G., Heath, D. D., Jensen, O. and Rolfe, R. ( 2000). Vaccination against cysticercosis and hydatid disease. Parasitology Today 16, 191196.CrossRefGoogle Scholar
Lightowlers, M. W., Jensen, O., Fernandez, E., Iriarte, J. A., Woollard, D. J., Gauci, C. G., Jenkins, D. J. and Heath, D. D. ( 1999). Vaccination trials in Australia and Argentina confirm the effectiveness of the EG95 hydatid vaccine in sheep. International Journal for Parasitology 29, 531534.CrossRefGoogle Scholar
Lightowlers, M. W., Lawrence, S. B., Gauci, C. G., Young, J., Ralston, M. J., Maas, D. and Heath, D. D. ( 1996 a). Vaccination against hydatidosis using a defined recombinant antigen. Parasite Immunology 18, 457462.Google Scholar
Lightowlers, M. W., Rickard, M. D. and Mitchell, G. F. ( 1986). Taenia taeniaeformis in mice: passive transfer of protection with sera from infected or vaccinated mice and analysis of serum antibodies to oncospheral antigens. International Journal for Parasitology 16, 307315.CrossRefGoogle Scholar
Lightowlers, M. W., Rolfe, R. and Gauci, C. G. ( 1996 b). Taenia saginata: vaccination against cysticercosis in cattle with recombinant oncosphere antigens. Experimental Parasitology 84, 330338.Google Scholar
Lightowlers, M. W., Waterkeyn, J. G., Rothel, J. S., Gauci, C. G. and Harrison, G. B. ( 1996 c). Host-protective fragments and antibody binding epitopes of the Taenia ovis 45W recombinant antigen. Parasite Immunology 18, 507513.Google Scholar
Mikityuk, P. V. and Kuznetsova, V. N. ( 1991). Meat quality in cysticerciasis of cattle. Veterinariya (Moskva) 10, 6265.
Miller, H. M. ( 1931 a). Immunity in the white rat to superinfestation with Cysticercus fasciolaris. Proceedings of the Society for Experimental Biology 28, 467468.Google Scholar
Miller, H. M. ( 1931 b). The production of artificial immunity in the albino rat to a metazoan parasite. Journal of Preventive Medicine 5, 429452.Google Scholar
Miller, H. M. ( 1932). Transmission to offspring of immunity against infection with a metazoan (cestode) parasite. Proceedings of the Royal Society for Experimental Biology 29, 1124.CrossRefGoogle Scholar
Miller, H. M. and Gardiner, M. L. ( 1932). Passive immunity to infection with a metazoan parasite, Cysticercus fasciolaris, in the albino rat. Journal of Preventive Medicine 6, 479496.Google Scholar
Miller, H. M. and Massie, E. ( 1932). Persistence of acquired immunity to Cysticercus fasciolaris after removal of the worms. Journal of Preventative Medicine 6, 3746.Google Scholar
Milstien, J., Batson, A. and Meaney, W. ( 1997). A systematic method for evaluating the potential viability of local vaccine producers. Vaccine 15, 13581363.CrossRefGoogle Scholar
Mitchell, G. F., Goding, J. W. and Rickard, M. D. ( 1977). Studies on immune responses to larval cestodes in mice. Increased susceptibility of certain mouse strains and hypothymic mice to Taenia taeniaeformis and analysis of passive transfer of resistance with serum. Australian Journal of Experimental Biology and Medical Science 55, 165186.CrossRefGoogle Scholar
Mitchell, G. F., Rajasekariah, G. R. and Rickard, M. D. ( 1980). A mechanism to account for mouse strain variation in resistance to the larval cestode, Taenia taeniaeformis. Immunology 39, 481489.Google Scholar
Mobius, G. ( 1993). Epidemiological studies on Cysticercus bovis and Taenia saginata infections in East- and West-Germany. Deutsche Tierarztliche Wochenschrift 100, 110114.Google Scholar
Molinari, J. L., Rodriguez, D., Tato, P., Soto, R., Arechavaleta, F. and Solano, S. ( 1997). Field trial for reducing porcine Taenia solium cysticercosis in Mexico by systematic vaccination of pigs. Veterinary Parasitology 69, 5563.CrossRefGoogle Scholar
Morariu, S., Lightowlers, M. W., Cosoroaba, I., Morariu, F., Darabus, G., Ilie, M. and Belean, M. ( 2005). The first use in Romania of EG95 vaccine to protect sheep against hydatidosis. Revista Romana de Medicina Veterinara 15, 97104.Google Scholar
Mukaratirwa, S., Kassuku, A. A., Willingham, A. L. and Murrell, K. D. ( 2003). Background to the international action planning workshop on Taenia solium cysticercosis/taeniosis with special focus on Eastern and Southern Africa. Acta Tropica 87, 35.CrossRefGoogle Scholar
Murrell, K. D., Dorny, P., Flisser, A., Geerts, S., Kyvsgaard, N. C., McManus, D. P., Nash, T. E. and Pawlowski, Z. S. ( 2005). WHO/FAO/OIE guidelines for the surveillance, prevention and control of taeniosis/cysticercosis. 139 pp. OIE, Paris.Google Scholar
Musoke, A. J. and Williams, J. F. ( 1975). Immunoglobulins associated with passive transfer of resistance to Taenia taeniaeformis in the mouse. Immunology 28, 97101.Google Scholar
Nadzhafov, I. G. ( 1987). Intensity of taeniasis transmission in foci in different climatic/geographic zones of Azerbaijan: a basis for rational control measures. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 2, 3841.Google Scholar
Nemeth, I. ( 1970). Immunological study of rabbit cysticercosis. II. Transfer of immunity to Cysticercus pisiformis (Bloch, 1780) with parenterally administered immune serum or lymphoid cells. Acta Veterinaria Academiae Scientiarum Hungaricae 20, 6979.Google Scholar
Nettesheim, M. P., Nakinodan, T. and Chadwick, C. J. ( 1966). Improved diffusion chamber cultures for cytokinetic analysis of antibody response. Immunology 11, 427439.Google Scholar
Osborn, P. J. and Heath, D. D. ( 1982). Immunisation of lambs against Echinococcus granulosus using antigens obtained by incubation of oncospheres in vitro. Research in Veterinary Science 33, 132133.Google Scholar
Petithory, J. and Rousset, J. J. ( 1965). Immunisation of mice against a homologous strain by living virulent trypanosomes in a diffusion chamber. Bulletin de la Société de Pathologie Exotique Filiales 58, 10491053.Google Scholar
Phiri, I. K., Ngowi, H., Afonso, S., Matenga, E., Boa, M., Mukaratirwa, S., Githigia, S., Saimo, M., Sikasunge, C., Maingi, N., Lubega, G. W., Kassuku, A., Michael, L., Siziya, S., Krecek, R. C., Noormahomed, E., Vilhena, M., Dorny, P. and Willingham, A. L. 3rd. ( 2003). The emergence of Taenia solium cysticercosis in Eastern and Southern Africa as a serious agricultural problem and public health risk. Acta Tropica 87, 1323.CrossRefGoogle Scholar
Rickard, M. D. and Adolph, A. J. ( 1976). Vaccination of calves against Taenia saginata infection using a ‘parasite-free’ vaccine. Veterinary Parasitology 1, 389392.CrossRefGoogle Scholar
Rickard, M. D., Adolph, A. J. and Arundel, J. H. ( 1977). Vaccination of calves against Taenia saginata infection using antigens collected during in vitro cultivation of larvae: passive protection via colostrum from vaccinated cows and vaccination of calves protected by maternal antibody. Research in Veterinary Science 23, 365367.Google Scholar
Rickard, M. D. and Bell, K. J. ( 1971 a). Immunity produced against Taenia ovis and T. taeniaeformis infection in lambs and rats following in vivo growth of their larvae in filtration membrane diffusion chambers. Journal of Parasitology 57, 571575.Google Scholar
Rickard, M. D. and Bell, K. J. ( 1971 b). Successful vaccination of lambs against infection with Taenia ovis using antigens produced during in vitro cultivation of the larval stages. Research in Veterinary Science 12, 401402.Google Scholar
Rickard, M. D. and Bell, K. J. ( 1971 c). Induction of immunity of lambs to a larval cestode by diffusible antigens. Nature 232, 120.Google Scholar
Rickard, M. D. and Arundel, J. G. ( 1974). Passive protection of lambs against infection with Taenia ovis via colostrum. Australian Veterinary Journal 50, 2224.CrossRefGoogle Scholar
Rickard, M. D., Harrison, G. B., Heath, D. D. and Lightowlers, M. W. ( 1995). Taenia ovis recombinant vaccine – ‘quo vadit’. Parasitology 110 (Suppl.), S5S9.CrossRefGoogle Scholar
Torgerson, P. R. ( 2003). The use of mathematical models to simulate control options for echinococcosis. Acta Tropica 85, 211221.CrossRefGoogle Scholar
Torgerson, P. R. and Heath, D. D. ( 2003). Transmission dynamics and control options for Echinococcus granulosus. Parasitology 127 (Suppl.), S143S158.CrossRefGoogle Scholar
Woollard, D. J., Gauci, C. G. and Lightowlers, M. W. ( 2000 a). Synthetic peptides induce antibody against a host-protective antigen of Echinococcus granulosus. Vaccine 18, 785794.Google Scholar
Woollard, D. J., Heath, D. D. and Lightowlers, M. W. ( 2000 b). Assessment of protective immune responses against hydatid disease in sheep by immunization with synthetic peptide antigens. Parasitology 121, 145153.Google Scholar
Woollard, D. J., Gauci, C. G., Heath, D. D. and Lightowlers, M. W. ( 2001). Protection against hydatid disease induced with the EG95 vaccine is associated with conformational epitopes. Vaccine 19, 498507.Google Scholar