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Past and future: vaccination against Eimeria

Published online by Cambridge University Press:  15 June 2009

V. McDONALD  and
M. W. SHIRLEY
V. McDONALD*
Affiliation:
Centre for Gastroenterology, Institute of Cell and Molecular Science, Barts and the London School of Medicine, Newark St, London E1 2AD, UK
M. W. SHIRLEY
Affiliation:
Institute of Animal Health, Compton, Nr Newbury, Berkshire RG20 7NN, UK
*
*Corresponding author: Centre for Gastroenterology, Institute of Cell and Molecular Science, Barts and the London School of Medicine, Newark St, London E1 2AD, UK. Tel: +0207 882 7202. Fax: +0207 882 2187. E-mail: [email protected]
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Summary

Eimeria spp. are the causative agents of coccidiosis, a major disease affecting many intensively-reared livestock, especially poultry. The chicken is host to 7 species of Eimeria that develop within intestinal epithelial cells and produce varying degrees of morbidity and mortality. Control of coccidiosis by the poultry industry is dominated by prophylactic chemotherapy but drug resistance is a serious problem. Strongly protective but species-specific immunity can be induced in chickens by infection with any of the Eimeria spp. At the Institute of Animal Health in Houghton, UK in the 1980s we showed that all 7 Eimeria spp. could be stably attenuated by serial passage in chickens of the earliest oocysts produced (i.e. the first parasites to complete their endogenous development) and this process resulted in the depletion of asexual development. Despite being highly attenuated, the precocious lines retained their immunizing capacity. Subsequent work led to the commercial introduction of the first live attenuated vaccine, Paracox®, that has now been in use for 20 years. As much work still remains to be done before the development of recombinant vaccines becomes a reality, it is likely that reliance upon live, attenuated vaccines will increase in years to come.

Keywords

Eimeriachickenattenuationprecocious developmentvaccination
Type
Research Article
Information
Parasitology , Volume 136 , Special Issue 12: Special Centenary Issue – Parasitology 1908–2008 , October 2009 , pp. 1477 - 1489
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Albanese, A. A. and Smetana, H. (1937). Studies on the effects of X-rays on the pathogenicity of Eimeria tenella. American Journal of Hygiene 26, 27–39.Google Scholar
Blake, D. P., Shirley, M. W. and Smith, A. L. (2006). Genetic identification of antigens protective against coccidia. Parasite Immunology 28, 305–314.CrossRefGoogle ScholarPubMed
Brisbin, J. T., Gong, J. and Sharif, S. (2008). Interactions between commensal bacteria and the gut-associated immune system of the chicken. Animal Health Research Review 9, 101–110.CrossRefGoogle ScholarPubMed
Bedrnik, P. (1993). Livacox, a vaccine against coccidiosis of domestic fowl. Research Institute of Feed Supplements and Veterinary Drugs, Jilovė, near Prague, Czech Republic.Google Scholar
Bushell, A. C., Shirley, M. W. and Bushell, J. E. (1992). The use of a live attenuated coccidiosis vaccine in replacement layers. Zootecnica International 5, 58–62.Google Scholar
Chapman, H. D. (2003). Origins of coccidiosis research in the fowl – the first fifty years. Avian Diseases 47, 1–20.CrossRefGoogle ScholarPubMed
Cheng, S. E. and Edgar, S. A. (1979). Effect of genetic selection on pathogenicity and immunogenicity of Eimeria tenella and Eimeria maxima. Poultry Science 58, 1043.Google Scholar
Constantinoiu, C. C., Lillehoj, H. S., Matsubayashi, M., Tani, H., Matsuda, H., Sasai, K. and Baba, E. (2004). Characterization of stage-specific and cross-reactive antigens from Eimeria acervulina by chicken monoclonal antibodies. Journal of Veterinary Medical Science 66, 403–408.CrossRefGoogle ScholarPubMed
Ding, X., Lillehoj, H. S., Dalloul, R. A., Min, W., Sato, T., Yasuda, A. and Lillehoj, E. P. (2005). In ovo vaccination with the Eimeria tenella EtMIC2 gene induces protective immunity against coccidiosis. Vaccine 23, 3733–3740.CrossRefGoogle ScholarPubMed
Dong, H., Suo, X., Wang, M. and Teng, K. (2006). Characteristics of a line of Eimeria necatrix after 16 successive passages of oocysts collected after peak oocyst production. Journal of Parasitology 92, 1229–1234.CrossRefGoogle ScholarPubMed
Engler, O. B., Dai, W. J., Sette, A., Hunziker, I. P., Reichen, J., Pichler, W. J. and Cerny, A. (2001). Peptide vaccines against hepatitis B virus: from animal model to human studies. Molecular Immunolgy 38, 457–465.CrossRefGoogle ScholarPubMed
Evans, N.A, Harding, R. B., Roberts, B. and Shirley, M. W. (1989). Coccidiosis control in chickens using a live attenuated vaccine. I. Experimental studies. In Coccidia and Intestinal Coccidiomorphs (ed. Yvoré, P.),pp. 683–688. INRA, Paris, France.Google Scholar
Gilbert, J. M., Fuller, A. L., Scott, T. C. and McDougald, L. R. (1998). Biological effects of gamma-irradiation on laboratory and field isolates of Eimeria tenella (Protozoa; Coccidia). Parasitology Research 84, 437–441.CrossRefGoogle Scholar
Govoni, S., Maestrini, N., Gobbi, L. and Tonelli, A. (1987). Prove di campo di un vaccine attenuato contro le coccidiosis del pollo. Atti della Società Italiana delle Scienza Veterinarie 41, 1187–1192.Google Scholar
Holmgren, J. and Czerkinsky, C. (2005). Mucosal immunity and vaccines. Nature Medicine 11, S45–S53.CrossRefGoogle ScholarPubMed
Horton-Smith, C. and Pierce, A. E. (1963). Behavior of invasive stages of Eimeria tenella in the fowl (Gallus domesticus). Experimental Parasitology 14, 66–74.CrossRefGoogle ScholarPubMed
Jankievicz, H. A. and Schofield, R. H. (1934). The administration of heated oocysts of Eimeria tenella as a means of establishing resistance and immunity to cecal coccidiosis. Journal of the American Veterinary Medicine Association 37, 507–526.Google Scholar
Jeffers, T. K. (1975). Attenuation of Eimeria tenella through selection for precociousness. Journal of Parasitology 61, 1083–1090.CrossRefGoogle ScholarPubMed
Jeffers, T. K. (1976). Genetic recombination of precociousness and anticoccidial drug resistance in Eimeria tenella. Zeitschrift für Parasitenkunde 50, 251–255.CrossRefGoogle ScholarPubMed
Jeffers, T. K. and Long, P. L. (1985). Eimeria tenella: immunogenicity of arrested sporozoites in chickens. Experimental Parasitology 60, 175–180.Google ScholarPubMed
Jenkins, M. C. (1998). Progress on developing a recombinant coccidiosis vaccine. International Journal of Parasitology 28, 1111–1119.CrossRefGoogle ScholarPubMed
Jenkins, M. C. (2001). Advances and prospects for subunit vaccines against protozoa of veterinary importance. Veterinary Parasitology 101, 291–310.CrossRefGoogle ScholarPubMed
Jenkins, M. C., Augustine, P. C., Barta, J. R., Castle, M. D. and Danforth, H. D. (1991). Development of resistance to coccidiosis in the absence of merogonic development using X-irradiated Eimeria acervulina oocysts. Experimental Parasitology 72, 285–293.CrossRefGoogle ScholarPubMed
Jenkins, M. C., Chute, M. B. and Danforth, H. D. (1997). Protection against coccidiosis in outbred chickens elicited by gamma-irradiated Eimeria maxima. Avian Diseases 41, 702–708.CrossRefGoogle ScholarPubMed
Johnson, J., Reid, W. M. and Jeffers, T. K. (1979). Practical immunization of chickens against coccidiosis using an attenuated strain of Eimeria tenella. Poultry Science 58, 37–41.CrossRefGoogle ScholarPubMed
Johnson, W. T. (1927). Immunity or resistance of the chicken to coccidial infection. Oregon Agricultural College Experimental Station Bulletin 230, 1–31.Google Scholar
Johnson, W. T. (1932). Immunity to coccidiosis in chickens, produced by inoculation through the ration. Journal of Parasitology 19, 160–161.Google Scholar
Jones, B. D., Ghori, N. and Falkow, S. (1994). Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. Journal of Experimental Medicine 180, 15–23.CrossRefGoogle ScholarPubMed
Kelleher, M. and Tomley, F. M. (1998). Transient expression of beta-galactosidase in differentiating sporozoites of Eimeria tenella. Molecular and Biochemical Parasitology 97, 21–31.CrossRefGoogle ScholarPubMed
Kogut, M. H., Gore, T. C. and Long, P. L. (1983). Serial passage of Eimeria tenella and E. necatrix in turkey embryos. Parasitology 86, 199–209.CrossRefGoogle Scholar
Konjufca, V., Jenkins, M., Wang, S., Juarez-Rodriguez, M. D. and Curtiss, R. III (2008). Immunogenicity of recombinant attenuated Salmonella enterica serovar Typhimurium vaccine strains carrying a gene that encodes Eimeria tenella antigen SO7. Infection and Immunity 76, 5745–5753.CrossRefGoogle ScholarPubMed
Konjufca, V., Wanda, S. Y., Jenkins, M. C. and Curtiss, R. III (2006). A recombinant attenuated Salmonella enterica serovar Typhimurium vaccine encoding Eimeria acervulina antigen offers protection against E. acervulina challenge. Infection and Immunity 74, 6785–6796.Google ScholarPubMed
Lillehoj, H. S. and Choi, K. D. (1998). Recombinant chicken interferon-gamma-mediated inhibition of Eimeria tenella development in vitro and reduction of oocyst production and body weight loss following Eimeria acervulina challenge infection. Avian Diseases 42, 307–314.CrossRefGoogle ScholarPubMed
Lillehoj, H. S., Jenkins, M. C. and Bacon, L. D. (1990). Effects of major histocompatibility genes and antigen delivery on induction of protective mucosal immunity to Eimeria acervulina following immunization with a recombinant merozoite antigen. Immunology 71, 127–132.Google ScholarPubMed
Lillehoj, H. S., Kim, C. H., Keeler, C. L. Jr. and Zhang, S. (2007). Immunogenomic approaches to study host immunity to enteric pathogens. Poultry Science 86, 1491–1500.CrossRefGoogle ScholarPubMed
Lillehoj, H. S. and Trout, J. M. (1996). Avian gut-associated lymphoid tissues and intestinal immune responses to Eimeria parasites. Clinical Microbiology Reviews 9, 349–360.CrossRefGoogle ScholarPubMed
Long, P. L. (1968). The pathogenic effects of Eimeria praecox and E. acervulina in the chicken. Parasitology 58, 691–700.CrossRefGoogle Scholar
Long, P. L. (1972). Eimeria tenella: reproduction, pathogenicity and immunogenicity of a strain maintained in chick embryos by serial passage. Journal of Comparative Pathology 82, 429–437.CrossRefGoogle ScholarPubMed
Long, P. L. (1974). Further studies on the pathogenicity and immunogenicity of an embryo-adapted strain of Eimeria tenella. Avian Pathology 3, 255–268.Google ScholarPubMed
Long, P. L. and Millard, B. J. (1968). Eimeria: effect of meticlorpindol and methyl benzoquate on endogenous stages in the chicken. Experimental Parasitology 23, 331–338.CrossRefGoogle ScholarPubMed
MacDonald, T. T. and Monteleone, G. (2005). Immunity, inflammation, and allergy in the gut. Science 307, 1920–1925.Google ScholarPubMed
Marcial, M. A. and Madara, J. L. (1986). Cryptosporidium: cellular localization, structural analysis of absorptive cell-parasite membrane-membrane interactions in guinea pigs, and suggestion of protozoan transport by M cells. Gastroenterology 90, 583–594.CrossRefGoogle ScholarPubMed
Matsler, P. L. and Chapman, H. D. (2007). Selection for early (precocious) development of Eimeria meleagridis in the turkey. Avian Diseases 51, 122–124.CrossRefGoogle ScholarPubMed
McDonald, V. and Ballingall, S. (1983). Attenuation of Eimeria mivati (=mitis) by selection for precocious development. Parasitology 86, 371–379.CrossRefGoogle ScholarPubMed
McDonald, V., Ballingall, S. and Shirley, M. W. (1982). A preliminary study of the nature of infection and immunity in chickens given an attenuated line of Eimeria acervulina. Parasitology 84, 21–30.Google ScholarPubMed
McDonald, V., Rose, M. E. and Jeffers, T. K. (1986 c). Eimeria tenella: immunogenicity of the first generation of schizogony. Parasitology 93, 1–7.CrossRefGoogle ScholarPubMed
McDonald, V. and Shirley, M. W. (1984). Eimeria mitis: a comparison of the endogenous developmental stages of a line selected for early maturation and the parent strain. Parasitology 88, 37–44.CrossRefGoogle ScholarPubMed
McDonald, V. and Shirley, M. W. (1985). The asexual development of precocious lines of Eimeria spp. in the chicken. In Research in Avian Coccidiosis: Proceedings of the Georgia Coccidiosis Conference, November 19–21, 1985 (ed. McDougald, L. R., Long, P. L. and Joyner, L. P.), pp. 502–509. University of Georgia, Athens, GA, USA.Google Scholar
McDonald, V. and Shirley, M. W. (1987). The endogenous development of virulent strains and attenuated precocious lines of Eimeria tenella and E. necatrix. Journal of Parasitology 73, 993–997.CrossRefGoogle ScholarPubMed
McDonald, V., Shirley, M. W. and Bellatti, M. A. (1986 b). Eimeria maxima: characteristics of attenuated lines obtained by selection for precocious development in the chicken. Experimental Parasitology 61, 192–200.CrossRefGoogle ScholarPubMed
McDonald, V., Shirley, M. W. and Millard, B. J. (1986 a). A comparative study of two lines of Eimeria tenella attenuated either by selection for precocious development in the chicken or by growth in chicken embryos. Avian Pathology 15, 323–335.CrossRefGoogle ScholarPubMed
McDonald, V., Wisher, M. H., Rose, M. E. and Jeffers, T. K. (1988). Eimeria tenella: immunological diversity between asexual generations. Parasite Immunology 10, 649–660.CrossRefGoogle ScholarPubMed
McDougald, L. R. and Jeffers, T. K. (1976). Eimeria tenella (Sporozoa, Coccidia): Gametogony following a single asexual generation. Science 192, 258–259.CrossRefGoogle ScholarPubMed
Medzhitov, R. (2007). TLR-mediated innate immune recognition. Seminars in Immunology 19, 1–2.CrossRefGoogle ScholarPubMed
Min, W., Lillehoj, H. S., Burnside, J., Weining, K. C., Staeheli, P. and Zhu, J. J. (2002). Adjuvant effects of IL-1beta, IL-2, IL-8, IL-15, IFN-alpha, IFN-gamma TGF-beta4 and lymphotactin on DNA vaccination against Eimeria acervulina. Vaccine 20, 267–274.CrossRefGoogle Scholar
Mora, J. R., Bono, M. R., Manjunath, N., Weninger, W., Cavanagh, L. L., Rosemblatt, M. and Von Andrian, U. H. (2003). Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature, London 424, 88–93.CrossRefGoogle ScholarPubMed
Neutra, M. R. and Kozlowski, P. A. (2006). Mucosal vaccines: the promise and the challenge. Nature Reviews Immunology 6, 148–158.CrossRefGoogle ScholarPubMed
Norton, C. C. and Chard, M. J. (1983). The oocyst sporulation time of Eimeria species from the fowl. Parasitology 86, 193–198.CrossRefGoogle ScholarPubMed
Norton, C. C. and Hein, H. E. (1976). Eimeria maxima: a comparison of two laboratory strains with a fresh isolate. Parasitology 72, 345–354.CrossRefGoogle ScholarPubMed
Pakandl, M. and Jelinkova, A. (2006). The rabbit coccidium Eimeria piriformis: selection of a precocious line and life-cycle study. Veterinary Parasitology 137, 351–354.CrossRefGoogle ScholarPubMed
Permar, S. R., Klumpp, S. A., Mansfield, K. G., Carville, A. A., Gorgone, D. A., Lifton, M. A., Schmitz, J. E., Reimann, K. A., Polack, F. P., Griffin, D. E. and Letvin, N. L. (2004). Limited contribution of humoral immunity to the clearance of measles viremia in rhesus monkeys. Journal of Infectious Diseases 190, 998–1005.CrossRefGoogle Scholar
Pogonka, T., Klotz, C., Kovacs, F. and Lucius, R. (2003). A single dose of recombinant Salmonella typhimurium induces specific humoral immune responses against heterologous Eimeria tenella antigens in chicken. International Journal for Parasitology 33, 81–88.CrossRefGoogle ScholarPubMed
Prowse, S. J. (1991). Cell-mediated immunity to Eimeria in the fowl: the absence of cross-species protection is not due to the lack of cross-reactive T cells. International Journal for Parasitology 21, 133–135.CrossRefGoogle ScholarPubMed
Rose, M. E. (1967). Immunity to Eimeria tenella and Eimeria necatrix infections in the fowl. I. Influence of the site of infection and the stage of the parasite. II. Cross-protection. Parasitology 57, 567–583.CrossRefGoogle ScholarPubMed
Rose, M. E. and Hesketh, P. (1979). Immunity to coccidiosis: T-lymphocyte- or B-lymphocyte-deficient animals. Infection and Immunity 26, 630–637.Google ScholarPubMed
Rose, M. E. and Hesketh, P. (1986). Eimerian life cycles: the patency of Eimeria vermiformis, but not Eimeria pragensis, is subject to host (Mus musculus) influence. Journal of Parasitology 72, 949–954.CrossRefGoogle Scholar
Rose, M. E., Hesketh, P. and Wakelin, D. (1992). Immune control of murine coccidiosis: CD4+ and CD8+ T lymphocytes contribute differentially in resistance to primary and secondary infections. Parasitology 105, 349–354.CrossRefGoogle ScholarPubMed
Rose, M. E., Joysey, H. S., Hesketh, P., Grencis, R. K. and Wakelin, D. (1988). Mediation of immunity to Eimeria vermiformis in mice by L3T4+ T cells. Infection and Immunity 56, 1760–1765.CrossRefGoogle ScholarPubMed
Rose, M. E., Smith, A. L. and Wakelin, D. (1991 b). Gamma interferon-mediated inhibition of Eimeria vermiformis growth in cultured fibroblasts and epithelial cells. Infection and Immunity 59, 580–586.CrossRefGoogle ScholarPubMed
Rose, M. E., Wakelin, D. and Hesketh, P. (1991 a). Interferon-gamma-mediated effects upon immunity to coccidial infections in the mouse. Parasite Immunology 13, 63–74.CrossRefGoogle ScholarPubMed
Rothwell, L., Gramzinski, R. A., Rose, M. E. and Kaiser, P. (1995). Avian coccidiosis: changes in intestinal lymphocyte populations associated with the development of immunity to Eimeria maxima. Parasite Immunology 17, 525–533.CrossRefGoogle ScholarPubMed
Schito, M. L. and Barta, J. R. (1997). Nonspecific immune responses and mechanisms of resistance to Eimeria papillata infections in mice. Infection and Immunity 65, 3165–3170.CrossRefGoogle ScholarPubMed
Schito, M. L., Barta, J. R. and Chobotar, B. (1996). Comparison of four murine Eimeria species in immunocompetent and immunodeficient mice. Journal of Parasitology 82, 255–262.CrossRefGoogle ScholarPubMed
Shirley, M. W. (1980). Eimeria necatrix: the development and characteristics of an egg-adapted (attenuated) line. Parasitology 81, 525–535.CrossRefGoogle ScholarPubMed
Shirley, M. W. and Bedrnik, P. (1997). Live attenuated vaccines against avian coccidiosis: Success with precocious and egg-adapted lines of Eimeria. Parasitology Today 13, 481–484.CrossRefGoogle ScholarPubMed
Shirley, M. W. and Bellatti, M. A. (1984). Eimeria necatrix: selection and characteristics of a precocious (and attenuated) line. Avian Pathology 13, 657–668.CrossRefGoogle ScholarPubMed
Shirley, M. W. and Bellatti, M. A. (1988). Live attenuated coccidiosis vaccine: selection of a second precocious line of Eimeria maxima. Research in Veterinary Science 44, 25–28.CrossRefGoogle ScholarPubMed
Shirley, M. W., Blake, D., White, S. E., Sheriff, R. and Smith, A. L. (2004). Integrating genetics and genomics to identify new leads for the control of Eimeria spp. Parasitology 128 (Suppl 1), S33–S42.CrossRefGoogle ScholarPubMed
Shirley, M. W., McDonald, V. and Ballingall, S. (1981). Eimeria spp. from the chicken: from merozoites to oocysts in embryonated eggs. Parasitology 83, 259–267.CrossRefGoogle ScholarPubMed
Shirley, M. W., McDonald, V. and Bellatti, M. A. (1986). Eimeria brunetti: selection and characteristics of a precocious (and attenuated) line. Avian Pathology 15, 705–717.CrossRefGoogle ScholarPubMed
Shirley, M. W., McDonald, V., Chapman, H. D., and Millard, B. J. (1984). Eimeria praecox: selection and characteristics of precocious lines. Avian Pathology 13, 669–682.CrossRefGoogle ScholarPubMed
Shirley, M. W. and Millard, B. J. (1986). Studies on the immunogenicity of seven attenuated lines of Eimeria given as a mixture to chickens. Avian Pathology 15, 629–638.CrossRefGoogle ScholarPubMed
Shirley, M. W., Smith, A. L. and Tomley, F. M. (2005). The biology of avian Eimeria with an emphasis on their control by vaccination. Advances in Parasitology 60, 285–330.CrossRefGoogle ScholarPubMed
Sibley, L. D., Messina, M. and Niesman, I. R. (1994). Stable DNA transformation in the obligate intracellular parasite Toxoplasma gondii by complementation of tryptophan auxotrophy. Proceedings of the National Academy of Sciences, USA 91, 5508–5512.CrossRefGoogle ScholarPubMed
Sicinski, P., Rowinski, J., Warchol, J. B., Jarzabek, Z., Gut, W., Szczygiel, B., Bielecki, K. and Koch, G. (1990). Poliovirus type 1 enters the human host through intestinal M cells. Gastroenterology 98, 56–58.CrossRefGoogle ScholarPubMed
Smith, A. L. and Hayday, A. C. (1998). Genetic analysis of the essential components of the immunoprotective response to infection with Eimeria vermiformis. International Journal for Parasitology 28, 1061–1069.CrossRefGoogle ScholarPubMed
Sukhumavasi, W., Egan, C. E., Warren, A. L., Taylor, G. A., Fox, B. A., Bzik, D. J. and Denkers, E. Y. (2008). TLR adaptor MyD88 is essential for pathogen control during oral Toxoplasma gondii infection but not adaptive immunity induced by a vaccine strain of the parasite. Journal of Immunology 181, 3464–3473.CrossRefGoogle Scholar
Sutton, C. A., Shirley, M. W. and McDonald, V. (1986). Genetic recombination of markers for precocious development, arprinocid resistance, and isoenzymes of glucose phosphate isomerase in Eimeria acervulina. Journal of Parasitology 72, 965–967.CrossRefGoogle ScholarPubMed
Tomley, F. (1994). Antigenic diversity of the asexual developmental stages of Eimeria tenella. Parasite Immunology 16, 407–413.CrossRefGoogle ScholarPubMed
Trout, J. M. and Lillehoj, H. S. (1996). T lymphocyte roles during Eimeria acervulina and Eimeria tenella infections. Veterinary Immunology and Immunopathology 53, 163–172.CrossRefGoogle ScholarPubMed
Tyzzer, E. E. (1929). Coccidiosis in gallinaceous birds. American Journal of Hygiene 10, 269–383.Google Scholar
Tyzzer, E. E., Theiler, H. and Jones, E. E. (1932). A comparative study of species of Eimeria of the chicken. American Journal of Hygiene 15, 319–393.Google Scholar
van Dijk, M. R., Waters, A. P. and Janse, C. J. (1995). Stable transfection of malaria parasite blood stages. Science 268, 1358–1362.CrossRefGoogle ScholarPubMed
Vermeulen, A. N. (1998). Progress in recombinant vaccine development against coccidiosis. A review and prospects into the next millennium. International Journal for Parasitology 28, 1121–1130.Google ScholarPubMed
Wallach, M. (1997). The importance of transmission-blocking immunity in the control of infections by apicomplexan parasites. International Journal for Parasitology 27, 1159–1167.CrossRefGoogle ScholarPubMed
Waxler, S. H. (1941). Immunization against cecal coccidiosis in chickens by the use of X-ray-attenuated oocysts. Journal of the American Veterinary Medical Association 99, 481–485.Google Scholar
Williams, R. B. (1994). Safety of the attenuated anticoccidial vaccine ‘Paracox’ in broiler chickens isolated from extraneous coccidial infection. Veterinary Research Communications 18, 189–198.CrossRefGoogle ScholarPubMed
Williams, R. B. (2002). Fifty years of anticoccidial vaccines for poultry (1952–2002). Avian Diseases 46, 775–802.CrossRefGoogle ScholarPubMed
Xu, Q., Song, X., Xu, L., Yan, R., Shah, M. A. and Li, X. (2008). Vaccination of chickens with a chimeric DNA vaccine encoding Eimeria tenella TA4 and chicken IL-2 induces protective immunity against coccidiosis. Veterinary Parasitology 156, 319–323.CrossRefGoogle ScholarPubMed
Yan, W., Liu, X., Shi, T., Hao, L., Tomley, F. M. and Suo, X. (2009). Stable transfection of Eimeria tenella: Constitutive expression of the YFP-YFP molecule throughout the life cycle. International Journal for Parasitology 39, 109–117.CrossRefGoogle ScholarPubMed
Yang, G., Li, J., Zhang, X., Zhao, Q., Liu, Q. and Gong, P. (2008). Eimeria tenella: construction of a recombinant fowlpox virus expressing rhomboid gene and its protective efficacy against homologous infection. Experimental Parasitology 119, 30–36.CrossRefGoogle ScholarPubMed