Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-24T17:33:09.816Z Has data issue: false hasContentIssue false

Vaccines against the avian enteropathogens Eimeria, Cryptosporidium and Salmonella

Published online by Cambridge University Press:  28 February 2007

Erik P. Lillehoj
Affiliation:
Department of Pharmaceutical Sciences, School of Pharmacy, University of Maryland, Baltimore, Maryland 21201
Cheol H. Yun
Affiliation:
Laboratory of Molecular Biology, National Cancer Institute, National Institute of Health, Bethesda, Maryland 20892
Hyun S. Lillehoj*
Affiliation:
Immunology and Disease Resistance Laboratory, Livestock and Poultry Science Institute, Agricultural Research Service, United States Department of Agriculture, Beltsville, Maryland 20705, USA
*
*BARC-East, Building 1040, IDRL, LPSI, ARS, USDA, Beltsville, MD 20705, USA. E-mail: [email protected]

Abstract

The worldwide poultry industry provides a substantial proportion of the nutritional requirement of the human population. To keep pace with the increasing demand for the high-quality, low-cost protein source that poultry provides, intensive rearing practices have been developed within the past few decades. For example, chickens are housed routinely in crowded environments under adverse conditions, and genetic strains have been selected for rapid growth, high protein-to-fat content and superior egg-laying characteristics. A major negative consequence of these practices has been an increase in the incidence of diseases. Enteric diseases in particular have emerged as a major problem threatening the future viability of the poultry industry. A variety of methods have been used to combat avian diseases in the commercial setting, including improved farm management practices, the use of antibiotic drugs, the selection of disease-resistant strains of chickens, and the manipulation of the chicken’s immune system. In the latter category, the development of vaccines against the major avian diseases has become a priority in the poultry industry. This review will highlight recent progress in vaccine development against three major avian enteric pathogens: Eimeria, Cryptosporidium and Salmonella.

Type
Research Article
Copyright
Copyright © CAB International 2000

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

Alderton, MR, Fahey, KJ and Coloe, PJ (1991). Humoral responses and salmonellosis protection in chickens given a vitamin-dependent Salmonella typhimurium mutant. Avian Diseases 35: 435442.CrossRefGoogle Scholar
Allen, PC, Danforth, HD, Gregory, SA and Comens-Keller, P (1997). Assessment of recombinant bovine somatotropin as an immunomodulator during avian coccidiosis: immunization with living oocysts. Poultry Science 76: 11501155.CrossRefGoogle ScholarPubMed
Arnold, JW and Holt, PS (1995). Response to Salmonella enteritidis infection by the immunocompromised avian host. Poultry Science 74: 656665.CrossRefGoogle ScholarPubMed
Augustine, PC, Danforth, HD and Barta, JR (1991). Development of protective immunity against Eimeria tenella and E. acervulina in White Leghorn chickens inoculated repeatedly with high doses of turkey coccidia. Avian Diseases 35: 535541.CrossRefGoogle Scholar
Augustine, PC, Danforth, HD and Jenkins, MC (1993). Avian Eimeria: effects of gamma irradiation on development of cross-species immunity in foreign and natural host birds. Avian Diseases 37: 349357.CrossRefGoogle ScholarPubMed
Awadalla, SF, Naguib, EF and Hegazi, SH (1998). Effect of trickle infections with Cryptosporidium baileyi for a short duration on development of specific immunity in chickens. Journal of the Egyptian Society of Parasitology 28: 339346.Google Scholar
Bailey, JS, Cason, JA and Cox, NA (1998). Effect of Salmonella in young chicks on competitive exclusion treatment. Poultry Science 77: 394399.CrossRefGoogle ScholarPubMed
Barbour, EK, Frerichs, WM, Nabbut, NH, Poss, PE and Brinton, MK (1993). Evaluation of bacterins containing three predominant phage types of Salmonella enteritidis for prevention of infection in egg-laying hens. American Journal of Veterinary Research 54: 13061309.CrossRefGoogle Scholar
Barrow, PA (1993). Salmonella control—past, present and future. Avian Pathology 22: 651669.CrossRefGoogle ScholarPubMed
Barrow, PA, Hassan, JO and Berchieri, A (1990 a). Reduction in faecal excretion of Salmonella typhimurium strain F98 in chickens vaccinated with live and killed Salmonella typhimurium organisms. Epidemiology and Infection 104: 413426.CrossRefGoogle Scholar
Barrow, PA, Lovell, MA and Berchieri, A (1990 b). Immunisation of laying hens against Salmonella enteritidis with live attenuated vaccines. Veterinary Record 126: 241242.Google ScholarPubMed
Barrow, PA, Lovell, MA and Berchieri, A (1991). The use of two live attenuated vaccines to immunize egg-laying hens against Salmonella enteritidis phage type 4. Avian Pathology 20: 681692.CrossRefGoogle ScholarPubMed
Beach, JR and Corl, JC (1925). Studies in the control of avian coccidiosis. Poultry Science 4: 8393.CrossRefGoogle Scholar
Bedrnik, P, Provaznikova, M and Firmanova, A (1993). Experimental and commercial use of LIVACOX, a live attenuated vaccine against coccidiosis of domestic fowl. In: Barta, JR and Fernando, MA (eds), Proceedings of the 6th International Coccidiosis Conference. Guelph, Canada, p. 165.Google Scholar
Bessay, M, Le Vern, Y, Kerboeuf, D, Yvore, P and Quere, P (1996). Changes in intestinal intra-epithelial and systemic T-cell subpopulations after an Eimeria infection in chickens: comparative study between E. acervulina and E. tenella. Veterinary Research 27: 503514.Google ScholarPubMed
Bhogal, BS, Miller, GA, Anderson, AC, Jessee, EJ, Strausberg, S, McCandliss, R, Nagle, J and Strausberg, RL (1992). Potential of a recombinant antigen as a prophylactic vaccine for day-old broiler chickens against Eimeria acervulina and Eimeria tenella infections. Veterinary Immunology and Immunopathology 31: 323335.CrossRefGoogle ScholarPubMed
Bouzoubaa,, K, Nagaraja, KV, Newman, JA and Poneroy, BS (1987). Use of membrane proteins from Salmonella gallinarum for prevention of fowl typhoid infection in chickens. Avian Diseases 31: 699704.CrossRefGoogle ScholarPubMed
Brake, DA, Strang, G, Lineberger, JE, Fedor, CH, Clare, R, Banas, TA and Miller, T (1997). Immunogenic characterization of a tissue culture-derived vaccine that affords partial protection against avian coccidiosis. Poultry Science 76: 974983.CrossRefGoogle ScholarPubMed
Brandtzaeg, P, Halstensen, TS, Kett, K, Krajci, P, Kvale, D, Rognum, TO, Scott, H and Sollid, LM (1989). Immunobiology and immunopathology of human gut mucosa: humoral immunity and intraepithelial lymphocytes. Gastroenterology 97: 15621584.CrossRefGoogle ScholarPubMed
Briles, DE, Benjamin, W Jr, Posey, B, Michalek, SM and McGhee, JR (1986). Independence of macrophage activation and expression of the alleles of the Ity (immunity to typhimurium) locus. Microbial Pathogenesis 01: 3341.CrossRefGoogle Scholar
Brito, JR, Hinton, M, Stokes, CR and Pearson, GR (1993). The humoral and cell mediated immune response of young chicks to Salmonella typhimurium and S. kedougou. British Veterinary Journal 149: 225234.CrossRefGoogle ScholarPubMed
Bubzy, JC and Roberts, T (1996). U.S. foodborne disease costs for seven pathogens. Food Reviews 19: 2025.Google Scholar
Castle, MD, Jenkins, MC, Danforth, HD and Lillehoj, HS (1991). Characterization of a recombinant Eimeria acervulina antigen expressed in sporozoite and merozoite developmental stages. Journal of Parasitology 77: 384390.CrossRefGoogle ScholarPubMed
Choi, KD, Lillehoj, HS and Zarlenga, DS (1999). Changes in local IFN-and TGF-4 mRNA expression and intraepithelial lymphocytes following E. acervulina infection. Veterinary Immunology and Immunopathology. 71: 263275.CrossRefGoogle Scholar
Cooper, GL (1994). Salmonellosis infection in man and the chicken: pathogenesis and the development of live vaccines—a review. Veterinary Bulletin 64: 123143.Google Scholar
Cooper, GL, Nicholas, RAJ, Cullen, GA and Hormaeche, CE (1990). Vaccination of chickens with a Salmonella enteritidis aroA live oral Salmonella vaccine. Microbial Pathogenesis 9: 255265.CrossRefGoogle ScholarPubMed
Cooper, GL, Venables, LM, Nicholas, RAJ, Cullen, GA and Hormaeche, CE (1992). Vaccination of chickens with chicken derived Salmonella enteritidis phage type 4 aroA live Salmonella vaccines. Vaccine 10: 247254.CrossRefGoogle Scholar
Cooper, GL, Venables, LM, Nicholas, RAJ, Cullen, GA and Hormaeche, CE (1993). Further studies of the application of live Salmonella enteritidis aroA vaccines in chickens. Veterinary Record 133: 3136.CrossRefGoogle ScholarPubMed
Cooper, GL, Venables, LM, Woodward, MJ and Hormaeche, CE (1994). Vaccination of chickens with strain CVL30, a genetically defined Salmonella enteritidis aroA live oral vaccine candidate. Infection and Immunity 62: 47474754.CrossRefGoogle ScholarPubMed
Corrier, DE, Elissalde, MH, Ziprin, RL and Deloach, JR (1991). Effect of immunosuppression with cyclophosphamide, cyclosporin or dexamethasone on Salmonella colonization of broiler chicks. Avian Diseases 35: 4045.CrossRefGoogle ScholarPubMed
Crane, MS, Goggin, B, Pellegrino, RM, Ravino, OJ, Lange, C, Karkhanis, YD, Kirk, KE and Chakrabarty, PR (1991). Cross-protection against four species of chicken coccidia with a single recombinant antigen. Infection and Immunity 59: 12711277.CrossRefGoogle ScholarPubMed
Crane, MS, Murray, PK, Gnozzio, MJ and MacDonald, TT (1988). Passive protection of chickens against Eimeria tenella infection by monoclonal antibody. Infection and Immunity 56: 972976.CrossRefGoogle ScholarPubMed
Current, WL and Snyder, DB (1988). Development of and serologic evaluation of acquired immunity to Cryptosporidium baileyi by broiler chickens. Poultry Science 67: 720729.CrossRefGoogle ScholarPubMed
Current, WL, Upton, SJ and Long, PL (1990). Taxonomy and life cycles. In: Long, PL (ed.), Coccidiosis of Man and Domestic Animals. Boca Raton: CRC Press. pp. 116.Google Scholar
Curtiss, R III and Kelly, SM (1987). Salmonella typhimurium deletion mutants lacking adenylate cyclase and the cyclic AMP receptor protein are avirulent and immunogenic. Infection and Immunity 55: 30353043.CrossRefGoogle ScholarPubMed
Curtiss, R III, Porter, SB, Munson, M, Tinge, SA, Hassan, JO, Gentry-Weeks, C and Kelly, SM (1991). Nonrecombinant and recombinant avirulent Salmonella vaccines for poultry. In: Blankenship, LC, Bailey, JS, Cox, NA, Stern, NJ and Meinersmann, RJ (eds), Colonization Control of Human Bacterial Enteropathogens in Poultry. San Diego: Academic Press. pp. 169198.CrossRefGoogle Scholar
Curtiss, R III, Kelly, SM and Hassan, JO (1993). Live oral avirulent Salmonella vaccines. Veterinary Microbiology 37: 397405.CrossRefGoogle ScholarPubMed
Danforth, HD, Augustine, PC, Ruff, MD, McCandliss, R, Strausberg, RL and Likel, M (1989). Genetically engineered antigen confers partial protection against avian coccidial parasites. Poultry Science 68: 16431652.CrossRefGoogle ScholarPubMed
Fayer, R (1993). Cryptosporidiosis: current strategies to meet a widespread problem. In: Barta, JR and Fernando, MA (eds) Proceedings of the 6th International Coccidiosis Conference. Guelph, Canada. pp. 95101.Google Scholar
Fayer, R, Speer, CA and Dubey, JP (1990). General biology of Cryptosporidium. In: Dubey, JP, Speer, CA and Fayer, R (eds), Cryptosporidiosis of Man and Animals. Boca Raton: CRC Press. pp. 129.Google Scholar
Fry, M, Hudson, AT, Randall, AW and Williams, RB (1984). Potent and selective hydroxynaphthoquinone inhibitors of mitochondrial electron transport in Eimeria tenella (Apicomplexa: Coccidia). Biochemical Pharmacology 33: 21152122.CrossRefGoogle ScholarPubMed
Galmes, MM, Norton, CC and Catchpole, J (1991). Comparison of resistance level and circulating IgG response in chickens experimentally inoculated with a multiple or single immunizing doses of Eimeria acervulina. Annals of Parasitology and Human Comparison 66: 144148.CrossRefGoogle ScholarPubMed
Ganguly, R and Waldman, RH (1980). Local immunity and local immune responses. Progress in Allergy 27: 168.Google ScholarPubMed
Gast, RK, Stone, HD, Holt, PS and Beard, CW (1992). Evaluation of the efficacy of an oil-emulsion bacterin for protecting chickens against Salmonella enteritidis. Avian Diseases 36: 992999.CrossRefGoogle ScholarPubMed
Gast, RK, Stone, HD and Holt, PS (1993). Evaluation of the efficacy of oil-emulsion bacterins for reducing fecal shedding of Salmonella enteritidis by laying hens. Avian Diseases 37: 10851091.CrossRefGoogle ScholarPubMed
Ghosh, SS (1989). Comparative efficacy of four vaccines against Salmonella virchow in chicks in India. Research in Veterinary Science 47: 280282.CrossRefGoogle ScholarPubMed
Gilbert, JM, Fuller, AL, Scott, TC and McDougald, LR (1998). Biological effects of gamma-irradiation on laboratory and field isolates of Eimeria tenella (Protozoa; Coccidia). Parasitology Research 84: 437441.CrossRefGoogle Scholar
Goodwin, MA and Brown, J (1988). Histological incidence and distribution of Cryptosporidium sp. in chickens: 68 cases in 1986. Avian Diseases 32: 365370.CrossRefGoogle ScholarPubMed
Goodwin, MA and Brown, J (1989). Intestinal cryptosporidiosis in chickens. Avian Diseases 33: 770777.CrossRefGoogle ScholarPubMed
Griffin, HG and Barrow, PA (1993). Construction of an aroA mutant of Salmonella serotype Gallinarum: its effectiveness in immunization against experimental fowl typhoid. Vaccine 11: 457462.CrossRefGoogle ScholarPubMed
Hassan, JO and Curtiss, R III (1994 a). Development and evaluation of an experimental vaccination program using a live avirulent Salmonella typhimurium strain to protect immunized chickens against challenge with homologous and heterologous Salmonella serotypes. Infection and Immunity 62: 55195527.CrossRefGoogle ScholarPubMed
Hassan, JO and Curtiss, R III (1990). Control of colonization by virulent Salmonella typhimurium by oral immunization of chickens with avirulent ΔcyaΔcrp S. typhimurium. Research in Microbiology 141: 839850.CrossRefGoogle Scholar
Hassan,, JO and Curtiss, R III (1994 b). Salmonella typhimurium induced lymphocyte depletion and immunosuppression in chickens. Infection and Immunity 62: 20272036.CrossRefGoogle ScholarPubMed
Hassan, JO and Curtiss, R III (1996). Effect of vaccination of hens with an avirulent strain of Salmonella typhimurium on immunity of progeny challenged with wild-type Salmonella strains. Infection and Immunity 64: 938944.CrossRefGoogle ScholarPubMed
Hassan, JO and Curtiss, R III (1997). Efficacy of a live avirulent Salmonella typhimurium vaccine in preventing colonization and invasion of laying hens by Salmonella typhimurium and Salmonella enteritidis. Avian Diseases 41: 783791.CrossRefGoogle ScholarPubMed
Hassan, JO, Mockett, APA, Catty, D and Barrow, PA (1991). Infection and reinfection of chickens with Salmonella typhimurium: bacteriology and immune responses. Avian Diseases 35: 809819.CrossRefGoogle ScholarPubMed
Hassan, JO, Porter, SB and Curtiss, R III (1993). Effect of infective dose on humoral immune responses and colonization in chickens experimentally infected with Salmonella typhimurium. Avian Diseases 37: 1926.CrossRefGoogle ScholarPubMed
Hatkin, J, Giambrone, JJ and Blagburn, BL (1993). Correlation of circulating antibody and cellular immunity with resistance against Cryptosporidium baileyi in broiler chickens. Avian Diseases 37: 800804.CrossRefGoogle ScholarPubMed
Hein, HE (1976). Eimeria acervulina, E. brunetti, E. maxima, and E. necatrix: low doses of oocysts to immunize young chickens. Experimental Parasitology 40: 250260.CrossRefGoogle Scholar
Hornok, S, Bitay, Z, Szell, Z and Varga, I (1998). Assessment of maternal immunity to Cryptosporidium baileyi in chickens. Veterinary Parasitology 79: 203212.CrossRefGoogle ScholarPubMed
Hornok, S, Szell, Z, Nieuwenhuijs, J, Nieuwland, MGB, Cornelissen, AW and Varga, I (1999). Immunogenicity of three oocyst extracts of Cryptosporidium baileyi in experimentally infected chickens. Parasitology Research 85: 7177.CrossRefGoogle ScholarPubMed
Isobe, T and Lillehoj, HS (1993). Dexamethasone suppresses T cell-mediated immunity and enhances disease susceptibility to Eimeria mivati infection. Veterinary Immunology and Immunopathology 39: 431446.CrossRefGoogle ScholarPubMed
Jenkins, MC, Lillehoj, HS and Dame, JB (1988). Eimeria acervulina: DNA cloning and characterization of recombinant sporozoite and merozoite antigens. Experimental Parasitology 66: 96107.CrossRefGoogle ScholarPubMed
Jenkins, MC, Danforth, HD, Lillehoj, HS and Fetterer, RH (1989). cDNA encoding an immunogenic region of a 22 kilodalton surface protein of Eimeria acervulina sporozoites. Molecular and Biochemical Parasitology 32: 153161.CrossRefGoogle ScholarPubMed
Jenkins, MC, Lillehoj, HS, Barta, JR, Danforth, HD and Strohlein, DA (1990). Eimeria acervulina: cloning of a cDNA encoding an immunogenic region of several related merozoite surface and rhoptry proteins. Experimental Parasitology 70: 353362.CrossRefGoogle ScholarPubMed
Jenkins, MC, Augustine, PC, Barta, JR, Castle, MD and Danforth, HD (1991 a). Development of resistance to coccidiosis in the absence of merogonic development using X-irradiated Eimeria acervulina oocysts. Experimental Parasitology 72: 285293.CrossRefGoogle ScholarPubMed
Jenkins, MC, Castle, MD and Danforth, HD (1991 b). Protective immunization against the intestinal parasite Eimeria acervulina with recombinant coccidial antigen. Poultry Science 70: 539547.CrossRefGoogle ScholarPubMed
Jenkins, MC, Chute, MB and Danforth, HD (1997). Protection against coccidiosis in outbred chickens elicited by gamma-irradiated Eimeria maxima. Avian Diseases 41: 702708.CrossRefGoogle ScholarPubMed
Kaiser, MG, Wing, T and Lamont, SJ (1998). Effect of genetics, vaccine dosage and postvaccination sampling interval on early antibody response to Salmonella enteritidis vaccine in broiler breeder chicks. Poultry Science 77: 271275.CrossRefGoogle ScholarPubMed
Kauffman, SH (1995). Immunity to intracellular microbial pathogens. Immunology Today 16: 338342.CrossRefGoogle Scholar
Kawazoe, U, Tomley, FM and Frazier, JA (1992). Fractionation and antigenic characterization of organelles of Eimeria tenella sporozoites. Parasitology 104: 19.CrossRefGoogle ScholarPubMed
Kim, KS, Jenkins, MC and Lillehoj, HS (1989). Immunization of chickens with live Escherichia coli expressing Eimeria acervulina merozoite recombinant antigen induces partial protection against coccidiosis. Infection and Immunity 57: 24342440.CrossRefGoogle ScholarPubMed
Kogut, MH and Slajchert, TS (1992). T lymphocytes induce protection in chickens against Eimeria tenella by production of lymphokines. Immunology of Infectious Diseases 2: 6980.Google Scholar
Kogut, MH, McGruder, ED, Hargis, BM, Corrier, DE and DeLoach, JR (1995). Characterization of the pattern of inflammatory cell influx in chicks following the intraperitoneal administration of live Salmonella enteritidis and Salmonella enteritidis-immune lymphokines. Poultry Science 74: 817.CrossRefGoogle ScholarPubMed
Kramer, TT (1998). Effects of heterophil adaptation on Salmonella enteritidis fecal shedding and egg contamination. Avian Diseases 42: 613.CrossRefGoogle ScholarPubMed
Kramer, TT, Reinke, CR and James, M (1998). Reduction of fecal shedding and egg contamination of Salmonella enteritidis by increasing the number of heterophil adaptations. Avian Diseases 42: 585588.CrossRefGoogle ScholarPubMed
Labelle, C and Colin, P (1985). Relationship between serotypes of Salmonella from hatcheries and rearing farms and those from processed poultry carcasses. British Poultry Science 26: 179186.Google Scholar
Lee, GM, Jackson, GDF and Cooper, GN (1981). The role of serum and biliary antibodies and cell-mediated immunity in the clearance of serotype S. typhimurium from chickens. Veterinary Immunology and Immunopathology 2: 233252.CrossRefGoogle Scholar
Lee, GM, Jackson, GDF and Cooper, GN (1983). Infection and immune responses in chickens exposed to Salmonella typhimurium. Avian Diseases 27: 577583.CrossRefGoogle ScholarPubMed
Lessard, M, Hutchings, DL and Spencer, JL (1995). Cell mediated and humoral immune responses in chickens infected with S. typhimurium. Avian Diseases 39: 230238.CrossRefGoogle Scholar
Lillehoj, HS (1987). Effects of immunosuppression on avian coccidiosis: cyclosporin A but not hormonal bursectomy abrogates host protective immunity. Infection and Immunity 55: 16161621.CrossRefGoogle Scholar
Lillehoj, HS (1994). Analysis of Eimeria acervulina-induced changes in the intestinal T lymphocyte subpopulations in two chicken strains showing different levels of susceptibility to coccidiosis. Research in Veterinary Science 56: 17.CrossRefGoogle ScholarPubMed
Lillehoj, HS (1998). Role of T lymphocytes and cytokines in coccidiosis. International Journal of Parasitology 28: 10711081.CrossRefGoogle ScholarPubMed
Lillehoj, HS and Bacon, LD (1991). Increase of intestinal intra-epithelial lymphocytes expressing CD8 antigen following challenge infection with Eimeria acervulina. Avian Diseases 35: 294301.CrossRefGoogle Scholar
Lillehoj, HS and Choi, KD (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: 307314.CrossRefGoogle ScholarPubMed
Lillehoj, HS, Jenkins, MC, Bacon, LD, Fetterer, RH and Briles, WE (1988). Eimeria acervulina: evaluation of the cellular and antibody responses to recombinant coccidial antigens in B-congenic chickens. Experimental Parasitology 67: 148158.CrossRefGoogle ScholarPubMed
Lillehoj, HS, Jenkins, MC and Bacon, LD (1990). Effects of major histocompatibility genes and antigen delivery on induction of protective mucosal immunity to E. acervulina following immunization with a recombinant merozoite antigen. Immunology 71: 127132.Google Scholar
Lillehoj, HS, Choi, KD, Jenkins, MC, Vakharia, VN, Song, KD, Han, JY and Lillehoj, EP (2000). A recombinant Eimeria protein inducing chicken interferon-γ production. Comparison of different gene expression systems and immunization strategies for vaccination against coccidiosis. Avian Diseases. 4: 379389.CrossRefGoogle Scholar
Lindsay, DS and Blagburn, BL (1990). Cryptosporidiosis in birds. In: Dubey, JP, Speer, CA and Fayer, R (eds), Cryptosporidiosis of Man and Animals. Boca Raton: CRC Press. pp. 133148.Google Scholar
Lindsay, DS, Blagburn, BL and Ernest, JA (1987). Experimental Cryptosporidium parvum infections in chickens. Journal of Parasitology 73: 242244.CrossRefGoogle ScholarPubMed
Lindsay, DS, Blagburn, BL, Sundermann, CA and Giambrone, JJ (1988 a). Effect of broiler chicken age on susceptibility to experimentally induced Cryptosporidium baileyi infection. American Journal of Veterinary Research 49: 14121414.Google ScholarPubMed
Lindsay, DS, Sundermann, CA and Blagburn, BL (1988 b). Cultivation of Cryptosporidium baileyi: studies with cell cultures, avian embryos and pathogenicity of chicken embryo-passaged oocysts. Journal of Parasitology 74: 288293.CrossRefGoogle ScholarPubMed
Long, PL and Jeffers, TK (1982). Studies on the stage of action of ionophorous antibiotics against Eimeria. Journal of Parasitology 68: 363371.CrossRefGoogle ScholarPubMed
Lumsden, JS, Wilkie, BN and Clarke, RC (1991). Resistance to fecal shedding of salmonellae in pigs and chickens vaccinated with an aromatic-dependent mutant of Salmonella typhimurium. American Journal of Veterinary Research 52: 17841787.CrossRefGoogle ScholarPubMed
Mastroeni, P, Villarreal-Ramos, B and Hormaeche, CE (1993). Adoptive transfer of immunity to oral challenge with virulent Salmonella in innately susceptible BALB/c mice requires both immune serum and T cells. Infection and Immunity 61: 39813984.CrossRefGoogle ScholarPubMed
Mathis, GF and McDougald, LR (1987). Evaluation of interspecific hybrids of the chicken, guinea fowl, and Japanese quail for innate resistance to coccidia. Avian Diseases 31: 740745.CrossRefGoogle ScholarPubMed
McDonald, V and Ballingall, S (1983). Attenuation of Eimeria mivati (= mitis) by selection for precocious development. Parasitology 86: 371379.CrossRefGoogle ScholarPubMed
McDonald, V and Shirley, MW (1987). The endogenous development of virulent strains and attenuated precocious lines of Eimeria tenella and E. necatrix. Journal of Parasitology 73: 993997.CrossRefGoogle ScholarPubMed
McDonald, V, Shirley, MW and Bellatti, MA (1986). Eimeria maxima: characteristics of attenuated lines obtained by selection for precocious development in the chicken. Experimental Parasitology 61: 192200.CrossRefGoogle ScholarPubMed
McGruder, ED, Ray, PM, Tellez, GI, Kogut, MH, Corrier, DE, DeLoach, JR and Hargis, BM (1993). Salmonella enteritidis immune leukocyte-stimulated soluble factors: effects of increased resistance to Salmonella organ invasion in day-old leghorn chicks. Poultry Science 72: 22642271.CrossRefGoogle ScholarPubMed
McGruder, ED, Rameriz, GA, Kogut, MH, Moore, RW, Corrier, DE, DeLoach, JR and Hargis, BM (1995). In ovo administration of Salmonella enteritidis-immune lymphokines confers protection to neonatal chicks against Salmonella enteritidis organ infectivity. Poultry Science 74: 1825.CrossRefGoogle ScholarPubMed
McHan, F, Shotts, EB and Brown, J (1991). Effect of feeding selected carbohydrates on the in vivo attachment of Salmonella typhimurium in chick ceca. Avian Diseases 35: 328331.CrossRefGoogle ScholarPubMed
McKenzie, ME and Long, PL (1986). Immunization of chickens against coccidiosis with extracts of Eimeria-infected tissues. Poultry Science 65: 892897.CrossRefGoogle ScholarPubMed
Methner, U, Barrow, PA, Martin, G and Meyer, H (1997). Comparative study of the protective effect against Salmonella colonisation in newly hatched SPF chickens using live, attenuated Salmonella vaccine strains, wild-type Salmonella strains or a competitive exclusion product. International Journal of Food Microbiology 15: 223230.CrossRefGoogle Scholar
Meyer, H (1991). Use of modified live vaccine in young livestock. In: Snoeyenbos, GH (ed.), Proceedings of the Symposium on the Diagnosis and Control of Salmonella. Richmond, VA: Carter Printing Co. pp. 4358.Google Scholar
Miller, GA, Bhogal, BS, McCandliss, R, Strausberg, RL, Jessee, EJ, Anderson, AC, Fuchs, CK, Nagle, J, Likel, MH and Strasser, JM (1989). Characterization and vaccine potential of a novel recombinant coccidial antigen. Infection and Immunity 57: 20142020.CrossRefGoogle ScholarPubMed
Mitchell, GF (1984). Towards molecular vaccines against parasites. Parasite Immunology 6: 493498.CrossRefGoogle ScholarPubMed
Muir, WI, Bryden, WL and Husband, AJ (1998). Evaluation of the efficacy of intraperitoneal immunization in reducing Salmonella typhimurium infection in chickens. Poultry Science 77: 18741883.CrossRefGoogle ScholarPubMed
Naciri, M, Mancassola, R, Reperant, JM and Yvore, P (1994). Analysis of humoral immune response in chickens after inoculation with Cryptosporidium baileyi or Cryptosporidium parvum. Avian Diseases 38: 832838.CrossRefGoogle ScholarPubMed
Nagaraja, KV, Kim, CJ, Kumar, MC and Pomeroy, BS (1991). Is vaccination a feasible approach for the control of Salmonella? In: Blankenship, LC, Bailey, JS, Cox, NA, Stern, NJ and Meinersmann, RJ (eds), Colonization Control of Human Bacterial Enteropathogens in Poultry. San Diego: Academic Press. pp. 243258.CrossRefGoogle Scholar
Nakai, Y, Uchida, T and Kanazawa, K (1992). Immunization of young chickens by trickle infection with Eimeria tenella. Avian Diseases 36: 10341036.CrossRefGoogle ScholarPubMed
Nakamura, M, Nagamine, N, Takahashi, T, Suzuki, S and Sato, S (1994). Evaluation of the efficacy of a bacterin against Salmonella enteritidis infection and the effects of stress after vaccination. Avian Diseases 38: 717724.CrossRefGoogle ScholarPubMed
Nassar, TJ, al-Nakhli, HM and al-Ogaily, ZH (1994). Use of live and inactivated Salmonella enteritidis phage type 4 vaccines to immunise laying hens against experimental infection. Research in Science and Technology 13: 855867.Google ScholarPubMed
Neutra, MR, Pringault, E and Kraehenbuhl, JP (1996). Antigen sampling across epithelial barriers and induction of mucosal immune responses. Annual Review of Immunology 14: 275300.CrossRefGoogle ScholarPubMed
Nina, JMS, McDonald, V, Dyson, DA, Catchpole, J, Uni, S, Iseki, M, Chiodini, PL and McAdam, KP (1992). Analysis of oocyst wall and sporozoite antigens from three Cryptosporidium species. Infection and Immunity 60: 15091513.CrossRefGoogle Scholar
Pomeroy, BS, Nagaraja, KV, Ausherman, LT, Peterson, IL and Friendshuh, KA (1989). Studies on feasibility of producing Salmonella-free turkeys. Avian Diseases 33: 17.CrossRefGoogle ScholarPubMed
Pritchard, DG, Nivas, SC, York, MD and Pomeroy, BS (1978). Effects of Gal-E mutants of Salmonella typhimurium on experimental salmonellosis in chickens. Avian Diseases 22: 562575.CrossRefGoogle ScholarPubMed
Rhalem, A, Sahibi, H, Dakkak, A, Laurent, F, Kazanji, M, Yvore, P and Perry, P (1993). Protective oral immunization of chickens against Eimeria tenella with sporozoite surface antigens. Veterinary Immunology and Immunopathology 38: 327340.CrossRefGoogle ScholarPubMed
Rhee, JK, Jang, BG and Park, BK (1995). Oocyst production and immunogenicity of Cryptosporidium baileyi in chickens and mallards. Korean Journal of Parasitology 33: 4554.CrossRefGoogle ScholarPubMed
Rhee, JK, Kim, HC and Park, BK (1996). Chronologic changes of serum IgG antibody response in chickens reinfected with Cryptosporidium baileyi. Korean Journal of Parasitology 34: 255258.CrossRefGoogle ScholarPubMed
Rhodes, GH, Abai, AM, Margalith, M, Kuwahara-Rundell, A, Morrow, J, Parker, SE and Dwarki, VJ (1993). Characterization of humoral immunity after DNA injection. Developmental Biology Standard 82: 229236.Google Scholar
Sasai, K, Yoshimura, K, Lillehoj, HS, Withanage, GSK, Fukata, T, Baba, E and Arakawa, A (1997). Analysis of splenic and thymic lymphocyte subpopulations in chickens infected with Salmonella enteritidis. Veterinary Immunology and Immunopathology 59: 359367.CrossRefGoogle ScholarPubMed
Smith, CK and Lee, DE (1986). Monosaccharide transport by Eimeria tenella sporozoites. Journal of Parasitology 72: 163169.Google ScholarPubMed
Smith, NC, Wallach, M, Petracca, M, Braun, R and Eckert, J (1994). Maternal transfer of antibodies induced by infection with Eimeria maxima partially protects chickens against challenge with Eimeria tenella. Parasitology 109: 551557.CrossRefGoogle ScholarPubMed
Song, KD, Lillehoj, HS, Choi, KD, Zarlenga, D and Han, JY (1997). Expression and functional characterization of recombinant chicken interferon-gamma. Veterinary Immunology and Immunopathology 58: 321333.CrossRefGoogle ScholarPubMed
Sreter, T, Varga, I and Bekesi, L (1995). Age-dependent resistance to Cryptosporidium baileyi infection in chickens. Journal of Parasitology 81: 827829.CrossRefGoogle ScholarPubMed
Sreter, T, Varga, I and Bekesi, L (1996). Effects of bursectomy and thymectomy on the development of resistance to Cryptosporidium baileyi in chickens. Parasitology Research 82: 174177.Google ScholarPubMed
Sreter, T, Hornok, S, Varga, I, Bekesi, L and Szell, Z (1997). Attempts to immunize chickens against Cryptosporidium baileyi with C. parvum oocysts and ParacoxTM vaccine. Folia Parasitologica 44: 7780.Google Scholar
Suphabphant, W, York, DM and Pomeroy, BS (1983). Use of two vaccines (live G30D or killed RW16) in the prevention of Salmonella typhimurium infection in chickens. Avian Diseases 27: 602615.CrossRefGoogle ScholarPubMed
Tan, S, Gyles, CL and Wilkie, BN (1997). Evaluation of an aroA mutant Salmonella typhimurium vaccine in chickens using modified semisolid Rappaport Vassiliadis medium to monitor faecal shedding. Veterinary Microbiology 54: 247254.CrossRefGoogle ScholarPubMed
Tellez, GI, Kogut, MH and Hargis, BM (1993). Immunoprophylaxis of Salmonella enteritidis infection by lymphokines in leghorn chicks. Avian Diseases 37: 10621070.CrossRefGoogle ScholarPubMed
Tilley, M, Upton, SJ, Blagburn, BL and Anderson, BC (1990). Identification of outer oocyst wall proteins of three Cryptosporidium (Apicomplexa, Cryptosporidiidae) species by 125I surface labeling. Infection and Immunity 58: 252253.CrossRefGoogle ScholarPubMed
Timms, LM, Marshall, RN and Breslin, MF (1990). Laboratory assessment of protection given by an experimental Salmonella enteritidis PT4 inactivated, adjuvant vaccine. Veterinary Record 127: 611614.Google ScholarPubMed
Timms, LM, Marshall, RN and Breslin, MF (1994). Laboratory and field trial assessment of protection given by a Salmonella enteritidis PT4 inactivated, adjuvant vaccine. British Veterinary Journal 150: 93102.CrossRefGoogle ScholarPubMed
Tomley, FM, Bumstead, JM, Billington, KJ and Dunn, PP (1996). Molecular cloning and characterization of a novel acidic microneme protein (Etmic–2) from the apicomplexan protozoan parasite, Eimeria tenella. Molecular and Biochemical Parasitology 79: 195206.CrossRefGoogle ScholarPubMed
Trout, JM and Lillehoj, HS (1996). T lymphocyte roles during Eimeria acervulina and Eimeria tenella infections. Veterinary Immunology and Immunopathology 53: 163172.CrossRefGoogle ScholarPubMed
Truscott, RB (1981). Oral Salmonella antigens for the control of Salmonella in chickens. Avian Diseases 25: 810820.CrossRefGoogle ScholarPubMed
Tzipori, S, Angus, KW, Campbell, I and Gray, EW (1980). Cryptosporidium: evidence for a single species genus. Infection and Immunity 30: 884886.CrossRefGoogle ScholarPubMed
Vervelde, L and Jeurissen, SH (1995). The role of intra-epithelial and lamina propria leucocytes during infection with Eimeria tenella. Advances in Experimental Medicine and Biology 371B: 953958.Google ScholarPubMed
Vervelde, L, Janse, EM, Vermeulen, AN and Jeurissen, SH (1998). Induction of a local and systemic immune response using cholera toxin as vehicle to deliver antigen in the lamina propria of the chicken intestine. Veterinary Immunology and Immunopathology 62: 261272.CrossRefGoogle ScholarPubMed
Waldroup, AL (1996). Contamination of raw poultry with pathogens. World's Poultry Science 59: 525.Google Scholar
Wallach, M, Halabi, A, Pillemer, G, Sar Shalom, O, Mencher, D, Gilad, M, Bendheim, U, Danforth, HD and Augustine, PC (1992). Maternal immunization with gametocyte antigens as a means of providing protective immunity against Eimeria maxima in chickens. Infection and Immunity 60: 20362039.CrossRefGoogle ScholarPubMed
Wallach, M, Smith, NC, Petracca, M, Miller, CM, Eckert, J and Braun, R (1995). Eimeria maxima gametocyte antigens: potential use in a subunit maternal vaccine against coccidiosis in chickens. Vaccine 13: 347354.CrossRefGoogle Scholar
Waltman, WD and Horne, AM (1993). Isolation of Salmonella from chickens reacting in the pullorum-typhoid agglutination test. Avian Diseases 37: 805810.CrossRefGoogle ScholarPubMed
Watkins, KL, Brooks, MA, Jeffers, TK, Phelps, PV and Ricks, CA (1995). The effect of in ovo oocyst or sporocyst inoculation on response to subsequent coccidial challenge. Poultry Science 74: 15971602.CrossRefGoogle ScholarPubMed
Withanage, GSK, Sasai, K, Fukata, T, Miyamoto, T, Baba, E and Lillehoj, HS (1998). T lymphocytes, B lymphocytes and macrophages in the ovaries and oviducts of laying hens experimentally infected with Salmonella enteritidis. Veterinary Immunology and Immunopathology 66: 173184.CrossRefGoogle ScholarPubMed
Yokoyama, H, Umeda, K, Peralta, RC, Hashi, T, Icatlo, FC, Kuroki, M, Ikemori, Y and Kodama, Y (1998). Oral passive immunization against experimental salmonellosis in mice using chicken egg yolk antibodies specific for Salmonella enteritidis and S. typhimurium. Vaccine 16: 388393.CrossRefGoogle ScholarPubMed
Yun, CH, Lillehoj, HS and Lillehoj, EP (2000). Intestinal immune responses to coccidiosis. Developmental and Comparative Immunology 24: 303324.CrossRefGoogle ScholarPubMed
Zhang, S, Lillehoj, HS and Ruff, MD (1995). In vivo role of tumor necrosis–like factor in Eimeria tenella infection. Avian Diseases 39: 859866.CrossRefGoogle ScholarPubMed
Zhang-Barber, L, Turner, AK, Dougan, G and Barrow, PA (1998). Protection of chickens against experimental fowl typhoid using a nuoG mutant of Salmonella serotype Gallinarum. Vaccine 16: 899903.CrossRefGoogle ScholarPubMed
Ziprin, RL (1997). Heterophil response to intraperitoneal challenge with invasion-deficient Salmonella enteritidis and Salmonella-immune lymphokines. Avian Diseases 41: 438441.CrossRefGoogle ScholarPubMed
Ziprin, RL, Corrier, DE and Elissalde, MH (1989). Maturation of resistance to salmonellosis in newly hatched chicks: inhibition by cyclosporin. Poultry Science 68: 16371642.CrossRefGoogle Scholar
Ziprin, RL, Kogut, MH, McGruder, ED, Hargis, BM and DeLoach, JR (1996). Efficacy of Salmonella enteritidis-immune lymphokines from chickens and turkeys on SE organ invasion in day-old chicks and turkey poults. Avian Diseases 40: 186192.CrossRefGoogle Scholar