Poultry coccidiosis: Recent advancements in control measures and vaccine development

Expert Review of Vaccines

Volumn 5, Issue 1, 2006, Pages 143-163

  Dalloul, Rami A ^a   Lillehoj, Hyun S ^a  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Anticoccidials; Coccidiosis; Eimeria; Embryo vaccination; Immunomodulation; Intestinal immunity; Live vaccines; Poultry; Recombinant vaccines

Indexed keywords

CHEMOKINE; COCCIDIOSTATIC AGENT; CPG OLIGODEOXYNUCLEOTIDE; CYTOKINE; DNA VACCINE; LECTIN; LIVE VACCINE; PROBIOTIC AGENT; RECOMBINANT VACCINE; SUBUNIT VACCINE;

ANTIBODY RESPONSE; B LYMPHOCYTE; CELLULAR IMMUNITY; CHEMOPROPHYLAXIS; COCCIDIOSIS; DEFENSE MECHANISM; DNA MICROARRAY; DOSE RESPONSE; DRUG FORMULATION; ECONOMIC ASPECT; EIMERIA; EMBRYO CELL; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOGENICITY; INNATE IMMUNITY; INTESTINE INFECTION; MACROPHAGE; MUSHROOM; NATURAL KILLER CELL; NONHUMAN; PARASITOSIS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; REVIEW; T LYMPHOCYTE;

ANIMALS; COCCIDIA; COCCIDIOSIS; EIMERIA; POULTRY; POULTRY DISEASES; PROTOZOAN VACCINES; TECHNOLOGY, PHARMACEUTICAL;

EID: 33646475173     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/14760584.5.1.143     Document Type: Review

References (193)

1. Williams RB. A compartmentalised model for the estimation of the cost of coccidiosis to the world's chicken production industry. Int. J. Parasitol. 29(8), 1209-1229 (1999).
2. Shirley MW, Ivens A, Gruber A et al. The Eimeria genome projects: a sequence of events. Trends Parasitol. 20(5), 199-201 (2004).
3. Dalloul RA, Lillehoj HS. Recent advances in immunomodulation and vaccination strategies against coccidiosis. Avian Dis. 49(1), 1-8 (2005).
4. Jeffers TK, Challey JR, McGibbon WH. Response of several lines of fowl and their single-cross progeny to experimental infection with Eimeria tenella. Avian Dis. 14(2), 203-210 (1970).
5. Lillehoj HS. Influence of inoculation dose, inoculation schedule, chicken age, and host genetics on disease susceptibility and development of resistance to Eimeria tenella infection. Avian Dis. 32(3), 437-444 (1988).
6. Lillehoj HS, Ruff MD, Bacon LD, Lamont SJ, Jeffers TK. Genetic control of immunity to Eimeria tenella. Interaction of MHC genes and non-MHC linked genes influences levels of disease susceptibility in chickens. Vet. Immunol. Immunopathol. 20(2), 135-148 (1989).
7. McDougald LR. Coccidiosis. In: Diseases of Poultry. Saif YM (Ed.). Iowa State Press, IA, USA, 974-991 (2003).
8. Allen PC, Fetterer RH. Recent advances in biology and immunobiology of Eimeria species and in diagnosis and control of infection with these coccidian parasites of poultry. Clin. Microbiol. Rev. 15(1), 58-65 (2002).
9. Williams RB. Anticoccidial vaccines for broiler chickens: pathways to success. Avian Pathol. 31(4), 317-353 (2002). Detailed review of live coccidiosis vaccines.
10. Levine ND. Taxonomy and life cycles of coccidian. In: The Biology of the Coccidia. Long PL (Ed.), Univeristy Park Press, MD, USA 1-33 (1982).
11. McDonald V, Shirley MW, Bellatti MA. Eimeria maxima: characteristics of attenuated lines obtained by selection for precocious development in the chicken. Exp. Parasitol. 61(2), 192-200 (1986).
12. Pout DD. Villous atrophy and coccidiosis. Nature 213(73), 306-307 (1967).
13. Witlock DR, Lushbaugh WB, Danforth HD, Ruff MD. Scanning electron microscopy of the cecal mucosa in Eimeria tenella-infected and uninfected chickens. Avian Dis. 19(2), 293-304 (1975).
14. Lillehoj HS. Role of T-lymphocytes and cytokines in coccidiosis. Int. J. Parasitol. 28(7), 1071-1081 (1998).
15. Lillehoj HS. Cell-mediated immunity in parasitic and bacterial diseases. In: Avian Cellular Immunology. Sharma JM (Ed.). CRC Press, Boca Raton, FL, USA, 155-182 (1991).
16. Lillehoj HS, Lillehoj EP. Avian coccidiosis. A review of acquired intestinal immunity and vaccination strategies. Avian Dis. 44(2), 408-425 (2000).
17. Lillehoj HS, Min W, Dalloul RA. Recent progress on the cytokine regulation of intestinal immune responses to Eimeria. Poult. Sci. 83(4), 611-623 (2004).
18. Rose ME, Lawn AM, Millard BJ. The effect of immunity on the early events in the life-cycle of Eimeria tenella in the caecal mucosa of the chicken. Parasitology 88 (Pt. 2), 199-210 (1984).
19. Wallach M, Pillemer G, Yarus S et al. Passive immunization of chickens against Eimeria maxima maxima infection with a monoclonal antibody developed against a gametocyte antigen. Infect. Immunol. 58(2), 557-562 (1990).
20. Wallach M, Smith NC, Petracca M et al. Eimeria mazima gametocyte antigens: potential use in a subunit maternal vaccine against coccidiosis in chickens. Vaccine 13(4), 347-354 (1995).
21. Lillehoj HS, Choi KD. Recombinant chicken interferon-γ-mediated inhibition of Eimeria tenella development in vitro and reduction of oocyst production and body weight loss following Eimeria acervulina challenge infection. Avian Dis. 42(2), 307-314 (1998).
22. Houssaint E, Belo M, Le Douarin NM. Investigations on cell lineage and tissue interactions in the developing bursa of Fabricius through interspecific chimeras. Dev. Biol. 53(2), 250-264 (1976).
23. Ratcliffe M. Development of avian B-lymphocyte lineage. CRC Crit. Rev. Poult. Biol. 2, 1207-1234 (1989).
24. Cooper MD, Chen CL, Bucy RP, Thompson CB. Avian T-cell ontogeny. Adv. Immunol. 50, 87-117 (1991).
25. Gobel TW. The T-dependent immune system. In: Poultry Immunology. Davison TF, Morris TR, Payne LN (Eds). Carfax Publishing Co., Abingdon, UK, 31-45 (1996).
26. Davidson NJ, Boyd RL. Delineation of chicken thymocytes by CD3-TCR complex, CD4 and CD8 antigen expression reveals phylogenically conserved and novel thymocyte subsets. Int. Immunol. 4(10), 1175-1182 (1992).
27. van Furth R, Cohn ZA, Hirsch JG et al. The mononuclear phagocyte system: a new classification of macrophages, monocytes, and their precursor cells. Bull. World Health Organ. 46(6), 845-852 (1972).
28. Jeurissen SHM, Verveide L, Janse ME. Structure and function of lymphoid tissues of the chicken. Poult. Sci. Rev. 5, 183-207 (1994).
29. Lillehoj HS, Isobe T, Weinstock D. Tissue distribution and cross-reactivities of new monoclonal antibody detecting chicken T-lymphocytes and macrophages. In: Avian Immunology in Progress. Coudert F (Ed.), INRA Editions, Paris, France 37-42 (1993).
30. Mast J, Goddeeris BM. Monoclonal antibodies reactive with the chicken monocytes/macrophage lineage. In: Advances in Avian Immunology Research. Davison T, Bumstead N, Kaiser P (Eds), Oxford, Carfax, Abingdon, UK, 39-48 (1995).
31. Mast J, Goddeeris BM, Peeters K, Vandesande F, Berghman LR. Characterisation of chicken monocytes, macrophages and interdigitating cells by the monoclonal antibody KUL01. Vet. Immunol. Immunopathol. 61(2-4), 343-357 (1998).
32. Underhill DM, Ozinsky A. Phagocytosis of microbes: Complexity in action. Ann. Rev. Immunol. 20(1), 825-852 (2002).
33. Barton GM, Medzhitov R. Control of adaptive immune responses by Toll-like receptors. Curr. Opin. Immunol. 14(3), 380-383 (2002).
34. Iqbal M, Philbin VJ, Smith AL. Expression patterns of chicken Toll-like receptor mRNA in tissues, immune cell subsets and cell lines. Vet. Immunol. Immunopathol. 104(1-2), 117-127 (2005).
35. Yilmaz A, Shen S, Adelson DL, Xavier S, Zhu JJ. Identification and sequence analysis of chicken Toll-like receptors. Immunogenetics 56(10), 743-753 (2005).
36. Schat KA, Calnek BW, Weinstock D. Cultivation and characterization of avian lymphocytes with natural killer cell activity. Avian Pathol. 15, 539-556 (1986).
37. Lillehoj HS, Chai JY. Comparative natural killer cell activities of thymic, bursal, splenic and intestinal intraepithelial lymphocytes of chickens. Dev. Comp. Immunol. 12(3), 629-643 (1988).
38. Chung KS, Lillehoj HS. Development and functional characterization of monoclonal antibodies recognizing chicken lymphocytes with natural killer cell activity. Vet. Immunol. Immunopathol. 28(3-4), 351-363 (1991).
39. Gobel TWF, Kaspers B, Stangassinger M. NK and T-cells constitute two major, functionally distinct intestinal epithelial lymphocyte subsets in the chicken. Int. Immunol. 13(6), 757-762 (2001).
40. Lam KM, Linna TJ. Transfer of natural resistance to Marek's disease (JMV) with non-immune spleen cells. I. Studies of cell population transferring resistance. Int. J. Cancer 24(5), 662-667 (1979).
41. Lillehoj HS. Intestinal intraepithelial and splenic natural killer cell responses to eimerian infections in inbred chickens. Infection and Immunity 57(7), 1879-1884 (1989).
42. Myers TJ, Schat KA. Natural killer cell activity of chicken intraepithelial leukocytes against rotavirus-infected target cells. Vet. Immunol. Immunopathol. 26(2), 157-170 (1990).
43. Trout JM, Lillehoj HS. T-lymphocyte roles during Eimeria acervulina and Eimeria tenella infections. Vet. Immunol. Immunopathol. 53(1-2), 163-172 (1996).
44. Yun CH, Lillehoj HS, Choi KD. Eimeria tenella infection induces local γ-interferon production and intestinal lymphocyte subpopulation changes. Infect. Immunol. 68(3), 1282-1288 (2000).
45. Yun CH, Lillehoj HS, Lillehoj EP. Intestinal immune responses to coccidiosis. Dev. Comp. Immunol. 24(2-3), 303-324 (2000).
46. Min W, Lillehoj HS, Kim S et al. Profiling local gene expression changes associated with Eimeria maxima and Eimeria acervulina using cDNA microarray. Appl. Microbiol. Biotechnol. 62, 392-399 (2003).
47. Yun CH, Lillehoj HS, Zhu J, Min W. Kinetic differences in intestinal and systemic interferon-γ and antigen-specific antibodies in chickens experimentally infected with Eimeria maxima. Avian Dis. 44(2), 305-312 (2000).
48. Lillehoj HS, Ruff MD. Comparison of disease susceptibility and subclass-specific antibody response in SC and FP chickens experimentally inoculated with Eimeria tenella, E. acervulina, or E. maxima. Avian Dis. 31(1), 112-119 (1987).
49. Dalloul RA, Lillehoj HS, Shellem TA, Doerr JA. Enhanced mucosal immunity against Eimeria acervulina in broilers fed a Lactobacillus-based probiotic. Poult. Sci. 82(1), 62-66 (2003).
50. Rose ME, Long PL. Resistance to Eimeria infections in the chicken: the effects of thymectomy, bursectomy, whole body irradiation and cortisone treatment. Parasitology 60(2), 291-299 (1970).
51. Lillehoj HS. Effects of immunosuppression on avian coccidiosis: cyclosporin A but not hormonal bursectomy abrogates host protective immunity. Infect. Immunol. 55(7), 1616-1621 (1987).
52. Leslie GA, Clem LW. Phylogen of immunoglobulin structure and function. III. Immunoglobulins of the chicken. J. Exp. Med. 130(6), 1337-1352 (1969).
53. Parvari R, Avivi A, Lentner F et al. Chicken immunoglobulin γ-heavy chains: limited VH gene repertoire, combinatorial diversification by D gene segments and evolution of the heavy chain locus. EMBO J. 7(3), 739-744 (1988).
54. Girard F, Fort G, Yvore P, Quere P. Kinetics of specific immunoglobulin A, M and G production in the duodenal and caecal mucosa of chickens infected with Eimeria acervulina or Eimeria tenella. Int. J. Parasitol. 27(7), 803-809 (1997).
55. Rose ME, Orlans E, Buttress N. Immunoglobulin classes in the hen's egg: their segregation in yolk and white. Eur. J. Immunol. 4(7), 521-523 (1974).
56. West J, Anthony P, Herr AB, Bjorkman PJ. The chicken yolk sac IgY receptor, a functional equivalent of the mammalian MHC-related Fc receptor, is a phospholipase A2 receptor homolog. Immunity 20(5), 601-610 (2004).
57. Wallach M, Halabi A, Pillemer G et al. Maternal immunization with gametocyte antigens as a means of providing protective immunity against Eimeria maxima in chickens. Infect. Immunol. 60(5), 2036-2039 (1992).
58. Lillehoj HS, Trout JM. Avian gut-associated lymphoid tissues and intestinal immune responses to Eimeria parasites. Clin. Microbiol. Rev. 9(3), 349-360 (1996).
59. Rose ME, Hesketh P. Immunity to coccidia in chickens: Adoptive transfer with peripheral blood lymphocytes and spleen cells. Parasite Immunol. 4(3), 171-185 (1982).
60. Miller TK, Bowman DD, Schat KA. Inhibition of the in vitro development of Eimeria tenella in chick kidney cells by immune chicken splenocytes. Avian Dis. 38(3), 418-427 (1994).
61. Lillehoj HS. Immune response during coccidiosis in SC and FP chickens. I. In vitro assessment of T-cell proliferation response to stage-specific parasite antigens. Vet. Immunol. Immunopathol. 13(4), 321-330 (1986).
62. Vervelde L, Vermeulen AN, Jeurissen SH. in situ characterization of leucocyte subpopulations after infection with Eimeria tenella in chickens. Parasite Immunol. 18(5), 247-256 (1996).
63. Guy-Grand D, Griscelli C, Vassalli P. The gut-associated lymphoid system: nature and properties of the large dividing cells. Eur. J. Immunol. 4(6), 435-443 (1974).
64. + intraepithelial lymphocytes. Nature 333(6176), 855-858 (1988).
65. Choi KD, Lillehoj HS. Role of chicken IL-2 on γδ T-cells and Eimeria acervulina-induced changes in intestinal IL-2 mRNA expression and γδ T-cells. Vet. Immunol. Immunopathol. 73(3-4), 309-321 (2000).
66. + T-cells from mice vaccinated against Toxoplasma gondii are cytotoxic for parasite-infected or antigen-pulsed host cells. J. Immunol. 147(7), 2310-2316 (1991).
67. Weiss W, Mellouk S, Houghten R et al. Cytotoxic T-cells recognize a peptide from the circumsporozoite protein on malaria-infected hepatocytes. J. Exp. Med. 171(3), 763-773 (1990).
68. Lillehoj HS, Bacon LD. Increase of intestinal intraepithelial lymphocytes expressing CD8 antigen following challenge infection with Eimeria acervulina. Avian Diseases 35(2), 294-301 (1991).
69. Bessay M, Le Vern Y, Kerboeuf D, Yvore P, Quere P. Changes in intestinal intra-epithelial and systemic T-cell subpopulations after an Eimeria infection in chickens: comparative study between E. acervulina and E. tenella. Vet. Res. 27(4-5), 503-514 (1996).
70. Breed DG, Dorrestein J, Vermeulen AN. Immunity to Eimeria tenella in chickens: phenotypical and functional changes in peripheral blood T-cell subsets. Avian Dis. 40(1), 37-48 (1996).
71. Breed DG, Dorrestein J, Schetters TP et al. Peripheral blood lymphocytes from Eimeria tenella infected chickens produce γ-interferon after stimulation in vitro. Parasite Immunol. 19(3), 127-135 (1997).
72. Breed DG, Schetters TP, Verhoeven NA, Vermeulen AN. Characterization of phenotype related responsiveness of peripheral blood lymphocytes from Eimeria tenella infected chickens. Parasite Immunol. 19(12), 563-569 (1997).
73. Chai JY, Lillehoj HS. Isolation and functional characterization of chicken intestinal intra-epithelial lymphocytes showing natural killer cell activity against tumour target cells. Immunology 63(1), 111-117 (1988).
74. Hong YH, Lillehoj HS, Dalloul RA et al. Molecular cloning and characterization of chicken NK-lysin. Vet. Immunol. Immunopathol. (In press).
75. Kaspers B, Lillehoj HS, Lillehoj EP. Chicken macrophages and thrombocytes share a common cell surface antigen defined by a monoclonal antibody. Vet. Immunol. Immunopathol. 36(4), 333-346 (1993).
76. Lillehoj HS, Kang SY, Keller L, Sevoian M. Eimeria tenella and E. acervulina: lymphokines secreted by an avian T-cell lymphoma or by sporozoite-stimulated immune T-lymphocytes protect chickens against avian coccidiosis. Experimental Parasitology 69(1), 54-64 (1989).
77. Dimier IH, Quere P, Naciri M, Bout DT. Inhibition of Eimeria tenella development in vitro mediated by chicken macrophages and fibroblasts treated with chicken cell supernatants with IFN-γ activity. Avian Dis. 42(2), 239-247 (1998).
78. Min W, Lillehoj HS, Ashwell CM et al. EST analysis of Eimeria-stimulated intestinal intraepithelial lymphocytes in chickens. Mol. Biotechnol. 30(2), 143-150 (2005).
79. Lillehoj HS, Dalloul RA, Min W. Enhancing intestinal immunity to coccidiosis. World Poult. 19 (Coccidiosis 4), 18-21 (2003).
80. Staeheli P, Puehler F, Schneider K, Gobel TW, Kaspers B. Cytokines of birds: conserved functions - a largely different look. J. Interf. Cytok. Res. 21(12), 993-1010 (2001).
81. Min W, Lillehoj HS. Isolation and characterization of chicken interleukin-17 cDNA. J Interf. Cytok. Res. 22(11), 1123-1128 (2002).
82. Schneider K, Puehler F, Baeuerle D et al. cDNA cloning of biologically active chicken interleukin-18. J. Interf. Cytok. Res. 20(10), 879-883 (2000).
83. Min W, Lillehoj HS. Identification and characterization of chicken interleukin-16 cDNA. Dev. Comp. Immunol. 28(2), 153-162 (2004).
84. Degen WGJ, van Daal N, van Zuilekom HI, Burnside J, Schijns VEJC. Identification and molecular cloning of functional chicken IL-12. J. Immunol. 172(7), 4371-4380 (2004).
85. Avery S, Rothwell L, Degen WGJ et al. Characterization of the first nonmammalian T2 cytokine gene cluster: The cluster contains functional single-copy genes for IL-3, IL-4, IL-13, and GM-CSF, a gene for IL-5 that appears to be a pseudogene, and a gene encoding another cytokine like transcript, KK34. J. Interf. Cytok. Res. 24(10), 600-610 (2004).
86. Rothwell L, Young JR, Zoorob R et al. Cloning and characterization of chicken IL-10 and its role in the immune response to Eimeria maxima. J. Immunol. 173(4), 2675-2682 (2004).
87. Koskela K, Kohonen P, Salminen H et al. Identification of a novel cytokine-like transcript differentially expressed in avian γδ T-cells. Immunogenetics 55(12), 845-854 (2004).
88. Digby MR, Lowenthal JW. Cloning and expression of the chicken interferon-γ gene. J. Interf. Cytok. Res. 15(11), 939-945 (1995).
89. Song KD, Lillehoj HS, Choi KD, Zarlenga D, Han JY. Expression and functional characterization of recombinant chicken interferon-γ. Vet. Immunol. Immunopathol. 58(3-4), 321-333 (1997).
90. Choi KD, Lillehoj HS, Zalenga DS. Changes in local IFN-γ and TGF-β4 mRNA expression and intraepithelial lymphocytes following Eimeria acervulina infection. Vet. Immunol. Immunopathol. 71(3-4), 263-275 (1999).
91. Farner NL, Hank JA, Sondel PM. Interleukin-2: molecular and clinical aspects. In: Cytokines in Health and Diseases. Remick DG, Friedland JS (Eds), Marcel Dekker, NY, USA 29-40 (1997).
92. Lillehoj HS, Kaspers B, Jenkins MC, Lillehoj EP. Avian interferon and interleukin-2. A review by comparison with mammalian homologues. Poult. Sci. Rev. 4, 67-85 (1992).
93. Sundick R, Gill-Dixon C. A cloned chicken lymphokine homologous to both mammalian IL-2 and IL-15. J. Immunol. 159(2), 720-725 (1997).
94. Lillehoj HS, Min W, Choi KD et al. Molecular, cellular, and functional characterization of chicken cytokines homologous to mammalian IL-15 and IL-2. Vet. Immunol. Immunopathol. 82(3-4), 229-244 (2001).
95. Lillehoj HS, Choi KD, Jenkins MC et al. A recombinant Eimeria protein inducing interferon-γ production: comparison of different gene expression systems and immunization strategies for vaccination against coccidiosis. Avian Dis. 44(2), 379-389 (2000).
96. Min W, Lillehoj HS, Burnside J et al. Adjuvant effects of IL-1β, IL-2, IL-8, IL-15, IFN-α, IFN-γ TGF-β4 and lymphotactin on DNA vaccination against Eimeria acervulina. Vaccine 20(1-2), 267-274 (2001).
97. Byrnes S, Eaton R, Kogut M. In vitro interleukin-1 and tumor necrosis factor-α production by macrophages from chickens infected with either Eimeria maxima or Eimeria tenella. Int. J. Parasitol. 23(5), 639-645 (1993).
98. Zhang S, Lillehoj HS, Ruff MD. In vivo role of tumor necrosis-like factor in Eimeria tenella infection. Avian Dis. 39(4), 859-866 (1995).
99. Zhang S, Lillehoj HS, Ruff MD. Chicken tumor necrosis-like factor. I. In vitro production by macrophages stimulated with Eimeria tenella or bacterial lipopolysaccharide. Poult. Sci. 74(8), 1304-1310 (1995).
100. Robinson P, Okhuysen PC, Chappell CL et al. Transforming growth factor β 1 is expressed in the jejunum after experimental Cryptosporidium parvum infection in humans. Infect. Immunol. 68(9), 5405-5407 (2000).
101. Strober W, Kelsall B, Fuss I et al. Reciprocal IFN-γ and TGF-β responses regulate the occurrence of mucosal inflammation. Immunol. Today 18(2), 61-64 (1997).
102. Jakowlew SB, Mathias A, Lillehoj HS. Transforming growth factor-β isoforms in the developing chicken intestine and spleen: increase in transforming growth factor-β 4 with coccidia infection. Vet. Immunol. Immunopathol. 55(4), 321-339 (1997).
103. Hunter CA, Bermudez L, Beernink H, Waegell W, Remington JS. Transforming growth factor-β inhibits interleukin-12-induced production of interferon-γ by natural killer cells: a role for transforming growth factor-β in the regulation of T-cell-independent resistance to Toxoplasma gondii. Eur. J. Immunol. 25(4), 994-1000 (1995).
104. Narazaki M, Kishimoto T. Interleukin-6 (IL-6). In: Guidebook to Cytokines and their Receptors. Nicola N (Ed.), Oxford University Press, Oxford, UK, 56-61 (1994).
105. Schneider K, Klaas R, Kaspers B, Staeheli P. Chicken interleukin-6. cDNA structure and biological properties. Eur. J. Biochem. 268(15), 4200-4206 (2001).
106. Lynagh GR, Bailey M, Kaiser P. Interleukin-6 is produced during both murine and avian Eimeria infections. Vet. Immunol. Immunopathol. 76(1-2), 89-102 (2000).
107. Laurent F, Mancassola R, Lacroix S, Menezes R, Naciri M. Analysis of chicken mucosal immune response to Eimeria tenella and Eimeria maxima infection by quantitative reverse transcription-PCR. Infect. Immunol. 69(4), 2527-2534 (2001).
108. Oppenheim JJ, Zachariae COC, Mukaida N, Matsushima K. Properties of the novel pro-inflammatory supergene 'Intercrine' cytokine family. Ann. Rev. Immunol. 9(1), 617-648 (1991).
109. Kaiser P, Hughes S, Bumstead N. The chicken 9E3/CEF4 CXC chemokine is the avian orthologue of IL-8 and maps to chicken chromosome 4 syntenic with genes flanking the mammalian chemokine cluster. Immunogenetics 49(7-8), 673-684 (1999).
110. Sick C, Schneider K, Staeheli P, Weining KC. Novel chicken CXC and CC chemokines. Cytokine 12(3), 181-186 (2000).
111. Lowenthal JW, York JJ, O'Neil TE et al. In vivo effects of chicken interferon-γ during infection with Eimeria. J. Interf. Cytok. Res. 17(9), 551-558 (1997).
112. + T-cells and accompanied by overproduction of IL-12, IFN-γ and TNF-α. J. Immunol. 157(2), 798-805 (1996).
113. Weber FH, Evans NA Immunization of broiler chicks by in ovo injection of Eimeria tenella sporozoites, sporocysts, or oocysts. Poult. Sci. 82(11), 1701-1707 (2003).
114. Weber FH, Genteman KC, LeMay MA, Lewis DO Sr, Evans NA Immunization of broiler chicks by in ovo injection of infective stages of Eimeria. Poult. Sci. 83(3), 392-399 (2004).
115. Dalloul RA, Lillehoj HS, Klinman DM et al. In ovo administration of CpG oligodeoxynucleotides and the recombinant microneme protein MIC2 protects against Eimeria infections. Vaccine 23(24), 3108-3113 (2005). First report of enhanced resistance to Eimeria by in ovo CpG injection.
116. Ding X, Lillehoj HS, Dalloul RA et al. In ovo vaccination with the Eimeria tenella EtMIC2 gene induces protective immunity against coccidiosis. Vaccine 23(28), 3733-3740 (2005).
117. Ding X, Lillehoj HS, Quiroz MA, Bevensee E, Lillehoj EP. Protective immunity against Eimeria acervulina following in avo immunization with a recombinant subunit vaccine and cytokine genes. Infect. Immunol. 72(12), 6939-6944 (2004).
118. Lillehoj HS, Ding X, Dalloul RA et al. Embryo vaccination against Eimeria tenella and E. acervulina infections using recombinant proteins and cytokine adjuvants. J. Parasitol. 91(3), 666-673 (2005).
119. Lillehoj HS, Ding X, Quiroz MA, Bevensee E, Lillehoj EP. Resistance to intestinal coccidiosis following DNA immunization with the cloned 3-1E Eimeria gene plus IL-2, IL-15, and IFN-γ. Avian Dis. 49(1), 112-117 (2005).
120. Mast J, Goddeeris BM. Development of immunocompetence of broiler chickens. Vet. Immunol. Immunopathol. 70(3-4), 245-256 (1999).
121. Seto F, Albright JF. An analysis of host and donor contributions to splenic enlargement in chick embryos inoculated with adult chicken spleen cells. Dev. Biol. 11, 1-24 (1965).
122. Seto F, Henderson WG. Natural and immune hemagglutinin forming capacity of immature chickens. J. Exp. Zool. 169(4), 501-511 (1968).
123. Oliver P, LeDouarin N. Avian thymic accessory cells. J. Immunol. 132(4), 1748-1755 (1984).
124. Janse EM, Jeurissen SH. Ontogeny and function of two non-lymphoid cell populations in the chicken embryo. Immunobiology 182(5), 472-481 (1991).
125. Coltey M, Bucy R, Chen C et al. Analysis of the first two waves of thymus homing stem cells and their T-cell progeny in chick-quail chimeras. J. Exp. Med. 170(2), 543-557 (1989).
126. Lowenthal JW, Connick TE, McWaters PG, York JJ. Development of T-cell immune responsiveness in the chicken. Immunol. Cell Biol. 72(2), 115-122 (1994).
127. Sharma JM, Burmester BR. Resistance to Marek's disease at hatching in chickens vaccinated as embryos with the turkey herpesvirus. Avian Dis. 26(1), 134-149 (1982). First report describing successful in ovo vaccination in chicken embryos.
128. Johnston PA, Liu H, O'Connell T et al. Applications in in ovo technology. Poult. Sci. 76(1), 165-178 (1997).
129. Wakenell PS, Sharma JM. Chicken embryonal vaccination with avian infectious bronchitis virus. Am. J. Vet. Res. 47(4), 933-938 (1986).
130. Negash T, al-Garib SO, Gruys E. Comparison of in ovo and post-hatch vaccination with particular reference to infectious bursal disease. A review. Vet. Q. 26(2), 76-87 (2004).
131. Beach JR, Corl JC. Studies in the control of avian coccidiosis. Poult. Sci. 4(3), 83-93 (1925).
132. Chapman HD, Cherry TE, Danforth HD et al. Sustainable coccidiosis control in poultry production: the role of live vaccines. Int. J. Parasitol. 32(5), 617-629 (2002).
133. Rose ME. Immunity to Eimeria infections. Vet. Immunol. Immunopathol. 17(1-4), 333-343 (1987).
134. Joyner LP, Norton CC. The immunity arising from continuous low-level infection with Eimeria tenella. Parasitology 67(3), 333-340 (1973).
135. Joyner LP, Norton CC. The immunity arising from continuous low-level infection with Eimeria maxima and Eimeria acervulina. Parasitology 72(1), 115-125 (1976).
136. Williams RB. Fifty years of anticoccidial vaccines for poultry (1952-2002). Avian Dis. 46(4), 775-802 (2002).
137. Jeffers TK. Attenuation of Eimeria tenella through selection for precociousness. J. Parasitol. 61(6), 1083-1090 (1975).
138. Crouch CF, Andrews SJ, Ward RG, Francis MJ. Protective efficacy of a live attenuated anticoccidial vaccine administered to 1-day-old chickens. Avian Pathol. 32(3), 297-304 (2003).
139. Li GQ, Kanu S, Xiang FY et al. Isolation and selection of ionophore-tolerant Eimeria precocious lines: E. tenella, E. maxima and E. acervulina. Vet. Parasitol. 119(4), 261-276 (2004).
140. Li GQ, Kanu S, Xiao SM, Xiang FY. Responses of chickens vaccinated with a live attenuated multi-valent ionophore-tolerant Eimeria vaccine. Vet. Parasitol. 129(3-4), 179-186 (2005).
141. Danforth HD. Use of live oocyst vaccines in the control of avian coccidiosis: experimental studies and field trials. Int. J. Parasitol. 28(7), 1099-1109 (1998).
142. Dibner J, Ivey FJ, Knight CD. Direct delivery of live coccidiosis vaccine into the hatchling yolk sac. World Poult. 19(Coccidiosis 3), 28-29 (1999).
143. Wolff JA, Malone RW, Williams P et al. Direct gene transfer into mouse muscle in vivo. Science 247(4949 Pt 1), 1465-1468 (1990).
144. Krieg AM. CpG motifs in bacterial DNA and their immune effects. Ann. Rev. Immunol. 20(1), 709-760 (2002).
145. Haygreen L, Davison F, Kaiser P. DNA vaccines for poultry: the jump from theory to practice. Expert Rev. Vaccines 4(1), 51-62 (2005).
146. Kopko SH, Martin DS, Barta JR. Responses of chickens to a recombinant refractile body antigen of Eimeria tenella administered using various immunizing strategies. Poult. Sci. 79(3), 336-342 (2000).
147. Wu SQ, Wang M, Liu Q et al. Construction of DNA vaccines and their induced protective immunity against experimental Eimeria tenella infection. Parasitol. Res. 94(5), 332-336 (2004).
148. Song KD, Lillehoj HS, Choi KD et al. A DNA vaccine encoding a conserved Eimeria protein induces protective immunity against live Eimeria acervulina challenge. Vaccine 19(2-3), 243-252 (2000).
149. Du A, Wang S. Efficacy of a DNA vaccine delivered in attenuated Salmonella typhimurium against Eimeria tenella infection in chickens. Int. J. Parasitol. 35(7), 777-785 (2005).
150. Jenkins MC. Progress on developing a recombinant coccidiosis vaccine. Int. J. Parasitol. 28(7), 1111-1119 (1998).
151. Vermeulen AN. Progress in recombinant vaccine development against coccidiosis. A review and prospects into the next millennium. Int. J. Parasitol. 28(7), 1121-1130 (1998).
152. Min W, Dalloul RA, Lillehoj HS. Application of biotechnological tools for coccidia vaccine development. J. Vet. Sci. 5(4), 279-288 (2004).
153. Schaap D, Arts G, Kroeze J et al. An Eimeria vaccine candidate appears to be lactate dehydrogenase; characterization and comparative analysis. Parasitology 128(Pt. 6), 603-616 (2004).
154. Miller GA, Bhogal BS, McCandliss R et al. Characterization and vaccine potential of a novel recombinant coccidial antigen. Infect. Immunol. 57(7), 2014-2020 (1989).
155. Bhogal BS, Miller GA, Anderson AC et al. Potential of a recombinant antigen as a prophylactic vaccine for day-old broiler chickens against Eimeria acervulina and Eimeria tenella infections. Vet. Immunol. Immunopathol. 31(3-4), 323-335 (1992).
156. Jenkins MC, Lillehoj HS, Dame JB. Eimeria acervulina: DNA cloning and characterization of recombinant sporozoite and merozoite antigens. Exp. Parasitol. 66(1), 96-107 (1988).
157. Jenkins MC, Danforth HD, Lillehoj HS, Fetterer RH. cDNA encoding an immunogenic region of a 22 kilo dalton surface protein of Eimeria acervulina sporozoites. Mol. Biochem. Parasitol. 32(2-3), 153-161 (1989).
158. Lillehoj HS, Jenkins MC, Bacon LD, Fetterer RH, Briles WE. Eimeria acervulina: evaluation of the cellular and antibody responses to the recombinant coccidial antigens in B-congenic chickens. Exp. Parasitol. 67(2), 148-158 (1988).
159. Verveide L, Janse EM, Vermeulen AN, Jeurissen SHM. Induction of a local and systemic immune response using cholera toxin as vehicle to deliver antigen in the lamina propria of the chicken intestine. Vet. Immunol. Immunopathol. 62(3), 261-272 (1998).
160. Laurent F, Bourdieu C, Kazanji M, Yvore P, Pery P. The immunodominant Eimeria acervulina sporozoite antigen previously described as p160/p240 is a 19-kilo dalton antigen present in several Eimeria species. Mol. Biochem. Parasitol. 63(1), 79-86 (1994).
161. Jenkins MC, Lillehoj HS, Barta JR, Danforth HD, Strohlein DA. Eimeria acervulina: cloning of a cDNA encoding an immunogenic region of several related merozoite surface and rhoptry proteins. Exp. Parasitol. 70(3), 353-362 (1990).
162. Fetterer RH, Miska KB, Jenkins MC, Barfield RC. A conserved 19-kda Eimeria tenella antigen is a profilin-like protein. J. Parasitol. 90(6), 1321-1328 (2004).
163. Belli SI, Mai K, Skene CD et al. Characterisation of the antigenic and immunogenic properties of bacterially expressed, sexual stage antigens of the coccidian parasite, Eimeria maxima. Vaccine 22(31-32), 4316-4325 (2004).
164. Wallach M. The development of CoxAbic® a novel vaccine against coccidiosis. World Poult. 18, 2-4 (2002).
165. Talebi A, Mulcahy G. Partial protection against Eimeria acervulina and Eimeria tenella induced by synthetic peptide vaccine. Exp. Parasitol. 110(4), 342-348 (2005).
166. Refega S, Girard-Misguich F, Bourdieu C, Pery P, Labbé M. Gene discovery in Eimeria tenella by immunoscreening cDNA expression libraries of sporozoites and schizonts with chicken intestinal antibodies. Vet. Parasitol. 113(1), 19-33 (2003).
167. Labbé M, de Venevelles P, Girard-Misguich F et al. Eimeria tenella microneme protein EtMIC3: identification, localisation and role in host cell infection. Mol. Biochem. Parasitol. 140(1), 43-53 (2005).
168. Bumstead J, Tomley F. Induction of secretion and surface capping of microneme proteins in Eimeria tenella. Mol. Biochem. Parasitol. 110(2), 311-321 (2000).
169. Tomley F. Recombinant vaccines for poultry. Vaccine 9(1), 4-5 (1991).
170. Tomley FM, Billington KJ, Bumstead JM, Clark JD, Monaghan P. EtMIC4: a microneme protein from Eimeria tenella that contains tandem arrays of epidermal growth factor-like repeats and thrombospondin type-I repeats. Int. J. Parasitol. 31(12), 1303-1310 (2001).
171. Brown PJ, Gill AC, Nugent PG, McVey JH, Tomley FM. Domains of invasion organelle proteins from apicomplexan parasites are homologous with the Apple domains of blood coagulation Factor XI and plasma pre-kallikrein and are members of the PAN module superfamily. FEBS Lett. 497(1), 31-38 (2001).
172. Ryan R, Shirley M, Tomley F. Mapping and expression of microneme genes in Eimeria tenella. Int. J. Parasitol. 30(14), 1493-1499 (2000).
173. Lindquist S, Craig EA. The heat-shock proteins. Ann. Rev. Genet. 22, 631-677 (1988).
174. Miska KB, Fetterer RH, Min W, Lillehoj HS. Heat shock protein 90 genes of two species of poultry Eimeria: expression and evolutionary analysis. J. Parasitol. 91(2), 300-306 (2005).
175. Nathan DF, Vos MH, Lindquist S. In vivo functions of the Saccharomyces cerevisiae Hsp90 chaperone. Proc. Natl Acad. Sci. USA 94(24), 12949-12956 (1997).
176. Miska KB, Fetterer RH, Barfield RC. Analysis of transcripts expressed by Eimeria tenella oocysts using subtractive hybridization methods. J. Parasitol. 90(6), 1245-1252 (2004).
177. Li L, Brunk BP, Kissinger JC et al. Gene Discovery in the apicomplexa as revealed by EST sequencing and assembly of a comparative gene database. Proc. Natl Acad. Sci. USA 13(3), 443-454 (2003).
178. Klotz C, Marhofer RJ, Selzer PM, Lucius R, Pogonka T. Eimeria tenella: identification of secretory and surface proteins from expressed sequence tags.
179. Roberts R, Sciorra VA, Morris AJ. Human Type 2 phosphatidic acid phosphohydrolases. Substrate specificity of the Type 2a, 2b, and 2c enzymes and cell surface activity of the 2a isoform. J. Biol. Chem. 273(34), 22059-22067 (1998).
180. La Ragione RM, Narbad A, Gasson MJ, Woodward MJ. In vivo characterization of Lactobacillus johnsonii FI9785 for use as a defined competitive exclusion agent against bacterial pathogens in poultry. Lett. Appl. Microbiol. 38(3), 197-205 (2004).
181. Dalloul RA, Lillehoj HS, Shellem TA, Doerr JA. Intestinal immunomodulation by vitamin A deficiency and Lactobacillus-based probiotic in Eimeria acervulina-infected broiler chickens. Avian Dis. 47(4), 1313-1320 (2003).
182. Dalloul RA, Lillehoj HS, Okamura M et al. In vivo effects of CpG oligodeoxynucleotide on Eimeria infection in chickens. Avian Dis. 48(4), 783-790 (2004).
183. Xie H, Raybourne RB, Babu US, Lillehoj HS, Heckert RA. CpG-induced immunomodulation and intracellular bacterial killing in a chicken macrophage cell line. Dev. Comp. Immunol. 27(9), 823-834 (2003).
184. Krieg AM, Yi AK, Matson S et al. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374(6522), 546-549 (1995). First work to identify unmethylated CpG motifs as crucial mediators of immune activation.
185. Nguyen S, Lillehoj HS, Donohue J, Yokohama A, Kodama Y. Passive protection against two Eimeria species in chickens by orally administered antibodies specific for a single Eimeria protein. Proc. American Association of Avian Pathologists, Denver, CO, USA, 21 (2003).
186. + T-lymphocytes in vitro. J. Parasitol. 82(1), 82-87 (1996).
187. Min W, Kim J-K, Lillehoj H et al. Characterization of recombinant scFv antibody reactive with an apical antigen of Eimeria acervulina. Biotechnol. Lett. 23(12), 949-955 (2001).
188. Park KJ, Park DW, Kim CH et al. Development and characterization of a recombinant chicken single-chain Fv antibody detecting Eimeria acervulina sporozoite antigen. Biotechnol. Lett. 27(5), 289-295 (2005).
189. Borchers AT, Keen CL, Gershwin ME. Mushrooms, tumors, and immunity: an update. Exp. Biol. Med. 229(5), 393-406 (2004).
190. Guo FC, Kwakkel RP, Williams BA et al. Effects of mushroom and herb polysaccharides on cellular and humoral immune responses of Eimeria tenella-infected chickens. Poult. Sci. 83(7), 1124-1132 (2004).
191. Guo FC, Kwakkel RP, Williams BA et al. Coccidiosis immunization: effects of mushroom and herb polysaccharides on immune responses of chickens infected with Eimeria tenella. Avian Dis. 49(1), 70-73 (2005).
192. Guo FC, Williams BA, Kwakkel RP et al. Effects of mushroom and herb polysaccharides, as alternatives for an antibiotic, on the cecal microbial ecosystem in broiler chickens. Poult. Sci. 83(2), 175-182 (2004).
193. Eisen MB, Brown PO. DNA arrays for analysis of gene expression. Methods Enzymol. 303, 179-205 (1999).