Securing poultry production from the ever-present Eimeria challenge

Trends in Parasitology

Volumn 30, Issue 1, 2014, Pages 12-19

  Blake, Damer P ^a   Tomley, Fiona M ^a  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

Author keywords

Chickens; Coccidiosis; Food security; New approaches; Vaccines

Indexed keywords

AGRICULTURE; COCCIDIOSIS; EIMERIA; FOOD SECURITY; NONHUMAN; PARASITE PREVALENCE; PARASITE TRANSMISSION; POULTRY; REVIEW; VACCINATION;

AVES; EIMERIA; GALLUS GALLUS; PROTOZOA;

CHICKENS; COCCIDIOSIS; FOOD SECURITY; NEW APPROACHES; VACCINES;

ANIMAL HUSBANDRY; ANIMALS; COCCIDIOSIS; EIMERIA; POULTRY; POULTRY DISEASES; PROTOZOAN VACCINES;

EID: 84890982964     PISSN: 14714922     EISSN: 14715007     Source Type: Journal    
DOI: 10.1016/j.pt.2013.10.003     Document Type: Review

References (99)

1. Grace D., et al. DFID Zoonoses Project 4 2012, International Livestock Research Institute.
2. Chapman H., et al. A selective review of advances in coccidiosis research. Adv. Parasitol. 2013, 83:93-171.
3. Shirley M., et al. The biology of avian Eimeria with an emphasis on their control by vaccination. Adv. Parasitol. 2005, 60:285-330.
4. Tyzzer E. Coccidiosis in gallinaceous birds. Am. J. Hyg. 1929, 10:269-383.
5. Jirku M., et al. A model for taxonomic work on homoxenous coccidia: redescription, host specificity, and molecular phylogeny of Eimeria ranae Dobell, 1909, with a review of anuran-host Eimeria (Apicomplexa: Eimeriorina). J. Eukaryot. Microbiol. 2009, 56:39-51.
6. Beck H., et al. Molecular approaches to diversity of populations of apicomplexan parasites. Int. J. Parasitol. 2009, 39:175-189.
7. Bennett R., Ijpelaar J. Updated estimates of the costs associated with thirty four endemic livestock diseases in Great Britain: a note. J. Agric. Econ. 2005, 56:135-144.
8. Dalloul R., Lillehoj H. Poultry coccidiosis: recent advancements in control measures and vaccine development. Expert Rev. Vaccines 2006, 5:143-163.
9. Williams R. A compartmentalised model for the estimation of the cost of coccidiosis to the world's chicken production industry. Int. J. Parasitol. 1999, 29:1209-1229.
10. Perry B., et al. Investing in Animal Health Research to Alleviate Poverty 2002, International Livestock Research Institute.
11. Radostits O., Stockdale P. A brief review of bovine coccidiosis in Western Canada. Can. Vet. J. 1980, 21:227-230.
12. Baba E., et al. Establishment and persistence of Salmonella typhimurium infection stimulated by Eimeria tenella in chickens. Res. Vet. Sci. 1982, 33:95-98.
13. Qin Z., et al. Effect of Eimeria tenella infection on the production of Salmonella enteritidis-contaminated eggs and susceptibility of laying hens to S. enteritidis infection. Avian Dis. 1996, 40:361-367.
14. Collier C., et al. Coccidia-induced mucogenesis promotes the onset of necrotic enteritis by supporting Clostridium perfringens growth. Vet. Immunol. Immunopathol. 2008, 122:104-115.
15. Veterinary Medicines Directorate Sales of Antimicrobial Products Authorised for Use as Veterinary Medicines, Antiprotozoals, Antifungals, Growth Promoters and Coccidiostats in the UK in 2011 2012, Veterinary Medicines Directorate. http://www.vmd.gov.uk/.
16. Chapman H. Biochemical, genetic and applied aspects of drug resistance in Eimeria parasites of the fowl. Avian Pathol. 1997, 26:221-244.
17. Chapman H. Anticoccidial drugs and their effects upon the development of immunity to Eimeria infections in poultry. Avian Pathol. 1999, 28:521-535.
18. Williams R. Anticoccidial vaccines for broiler chickens: pathways to success. Avian Pathol. 2002, 31:317-353.
19. Chapman H., et al. Sustainable coccidiosis control in poultry production: the role of live vaccines. Int. J. Parasitol. 2002, 32:617-629.
20. McDougald L., Jeffers T. Eimeria tenella (Sporozoa, Coccidia): gametogony following a single asexual generation. Science 1976, 192:258-259.
21. Shirley M., Bedrnik P. Live attenuated vaccines against avian coccidiosis: success with precocious and egg-adapted lines of Eimeria. Parasitol. Today 1997, 13:481-484.
22. Long P. Development of Eimeria tenella in avian embryos. Nature 1965, 208:509-510.
23. Long P., et al. Immunisation against coccidiosis in chickens: tests under simulated field conditions. Avian Pathol. 1982, 11:131-144.
24. Bedrnik P. Comment on the review 'Anticoccidial vaccines for broiler chickens: pathways to success by R.B. Williams. (2002). Avian Pathology, 31, 317-53. Avian Pathol. 2003, 32:219.
25. McDonald V., Shirley M. Past and future: vaccination against Eimeria. Parasitology 2009, 136:1477-1489.
26. Jorgensen W., et al. Selection and characterisation of two attenuated vaccine lines of Eimeria tenella in Australia. Aust. Vet. J. 2006, 84:89-94.
27. Kawazoe U., et al. Characterisation and histopathological observations of a selected Brazilian precocious line of Eimeria acervulina. Vet. Parasitol. 2005, 131:5-14.
28. Suo X., et al. The efficacy and economic benefits of Supercox, a live anticoccidial vaccine in a commercial trial in broiler chickens in China. Vet. Parasitol. 2006, 142:63-70.
29. Chen H., et al. Development of Eimeria nieschulzi (Coccidia, Apicomplexa) gamonts and oocysts in primary fetal rat cells. J. Parasitol. Res. 2013, 2013:591520.
30. Sharman P., et al. Chasing the golden egg: vaccination against poultry coccidiosis. Parasite Immunol. 2010, 32:590-598.
31. Blake D., et al. Genetic identification of antigens protective against coccidia. Parasite Immunol. 2006, 28:305-314.
32. Wallach M., et al. Field application of a subunit vaccine against an enteric protozoan disease. PLoS ONE 2008, 3:e3948.
33. Wallach M., et al. Eimeria maxima gametocyte antigens: potential use in a subunit maternal vaccine against coccidiosis in chickens. Vaccine 1995, 13:347-354.
34. ®. Bull. Vet. Inst. Pulawy 2005, 49:299-302.
35. Witcombe D., et al. Eimeria maxima TRAP family protein EmTFP250: subcellular localisation and induction of immune responses by immunisation with a recombinant C-terminal derivative. Int. J. Parasitol. 2004, 34:861-872.
36. Du A., et al. Eimeria tenella: ginsenosides-enhanced immune response to the immunization with recombinant 5401 antigen in chickens. Exp. Parasitol. 2005, 111:191-197.
37. Subramanian B., et al. Cloning, expression and evaluation of the efficacy of a recombinant Eimeria tenella sporozoite antigen in birds. Vaccine 2008, 26:3489-3496.
38. Li J., et al. Efficacy of Eimeria tenella rhomboid-like protein as a subunit vaccine in protective immunity against homologous challenge. Parasitol. Res. 2012, 110:1139-1145.
39. Song X., et al. The optimal immunization procedure of DNA vaccine pcDNA-TA4-IL-2 of Eimeria tenella and its cross-immunity to Eimeria necatrix and Eimeria acervulina. Vet. Parasitol. 2009, 159:30-36.
40. Wu S., et al. Construction of DNA vaccines and their induced protective immunity against experimental Eimeria tenella infection. Parasitol. Res. 2004, 94:332-336.
41. Xu Q., et al. Vaccination of chickens with a chimeric DNA vaccine encoding Eimeria tenella TA4 and chicken IL-2 induces protective immunity against coccidiosis. Vet. Parasitol. 2008, 156:319-323.
42. Ding J., et al. Immunoprotection of chickens against Eimeria acervulina by recombinant α-tubulin protein. Parasitol. Res. 2008, 103:1133-1140.
43. Del Cacho E., et al. A fibronectin-like molecule expressed by Eimeria tenella as a potential coccidial vaccine. Parasitol. Today 1997, 13:405-406.
44. Bhogal B., 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. 1992, 31:323-335.
45. Miller G., et al. Characterization and vaccine potential of a novel recombinant coccidial antigen. Infect. Immun. 1989, 57:2014-2020.
46. Vermeulen A. Progress in recombinant vaccine development against coccidiosis. A review and prospects into the next millennium. Int. J. Parasitol. 1998, 28:1121-1130.
47. Schaap D., et al. An Eimeria vaccine candidate appears to be lactate dehydrogenase; characterization and comparative analysis. Parasitology 2004, 128:603-616.
48. Song K., et al. A DNA vaccine encoding a conserved Eimeria protein induces protective immunity against live Eimeria acervulina challenge. Vaccine 2000, 19:243-252.
49. Min W., 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 2001, 20:267-274.
50. Ding X., et al. Protective immunity against Eimeria acervulina following in ovo immunization with a recombinant subunit vaccine and cytokine genes. Infect. Immun. 2004, 72:6939-6944.
51. Xu S., et al. Protective immunity enhanced by chimeric DNA prime-protein booster strategy against Eimeria tenella challenge. Avian Dis. 2006, 50:579-585.
52. Jang S., et al. Montanide IMS 1313 N VG PR nanoparticle adjuvant enhances antigen-specific immune responses to profilin following mucosal vaccination against Eimeria acervulina. Vet. Parasitol. 2011, 182:163-170.
53. Jang S., et al. Immunoenhancing effects of Montanide ISA oil-based adjuvants on recombinant coccidia antigen vaccination against Eimeria acervulina infection. Vet. Parasitol. 2010, 172:221-228.
54. Del Cacho E., et al. Induction of protective immunity against Eimeria tenella infection using antigen-loaded dendritic cells (DC) and DC-derived exosomes. Vaccine 2011, 29:3818-3825.
55. Belli S., et al. Characterisation of the antigenic and immunogenic properties of bacterially expressed, sexual stage antigens of the coccidian parasite, Eimeria maxima. Vaccine 2004, 22:4316-4325.
56. Jang S., et al. Eimeria maxima recombinant Gam82 gametocyte antigen vaccine protects against coccidiosis and augments humoral and cell-mediated immunity. Vaccine 2010, 28:2980-2985.
57. Xu J., et al. Efficacy of a DNA vaccine carrying Eimeria maxima Gam56 antigen gene against coccidiosis in chickens. Korean J. Parasitol. 2013, 51:147-154.
58. Ding J., et al. Multi-epitope recombinant vaccine induces immunoprotection against mixed infection of Eimeria spp. Parasitol. Res. 2012, 110:2297-2306.
59. Talebi A., Mulcahy G. Partial protection against Eimeria acervulina and Eimeria tenella induced by synthetic peptide vaccine. Exp. Parasitol. 2005, 110:342-348.
60. Berezin V., et al. Immunostimulatory complexes containing Eimeria tenella antigens and low toxicity plant saponins induce antibody response and provide protection from challenge in broiler chickens. Vet. Parasitol. 2010, 167:28-35.
61. Lai L., et al. The role of sialyl glycan recognition in host tissue tropism of the avian parasite Eimeria tenella. PLoS Pathog. 2011, 7:e1002296.
62. Zhu H., et al. Identification and molecular characterization of a novel antigen of Eimeria acervulina. Mol. Biochem. Parasitol. 2012, 186:21-28.
63. Zhu H., et al. Identification and characterization of a cDNA clone-encoding antigen of Eimeria acervulina. Parasitology 2012, 139:1711-1719.
64. Melby P., et al. Identification of vaccine candidates for experimental visceral leishmaniasis by immunization with sequential fractions of a cDNA expression library. Infect. Immun. 2000, 68:5595-5602.
65. Klotz C., et al. Identification of Eimeria tenella genes encoding for secretory proteins and evaluation of candidates by DNA immunisation studies in chickens. Vaccine 2007, 25:6625-6634.
66. Smith A., et al. Antigenic diversity in Eimeria maxima and the influence of host genetics and immunisation schedule on cross protective immunity. Infect. Immun. 2002, 70:2472-2479.
67. Blake D., et al. Genetic mapping identifies novel highly protective antigens for an apicomplexan parasite. PLoS Pathog. 2011, 7:e1001279.
68. Jenkins M., et al. Protective immunization against the intestinal parasite Eimeria acervulina with recombinant coccidial antigen. Poult. Sci. 1991, 70:539-547.
69. Konjufca V., et al. Immunogenicity of recombinant attenuated Salmonella enterica serovar Typhimurium vaccine strains encoding Eimeria tenella antigen SO7. Infect. Immun. 2008, 76:5745-5753.
70. Konjufca V., et al. A recombinant attenuated Salmonella enterica serovar Typhimurium vaccine encoding Eimeria acervulina antigen offers protection against E. acervulina challenge. Infect. Immun. 2006, 74:6785-6796.
71. Du A., Wang S. Efficacy of a DNA vaccine delivered in attenuated Salmonella typhimurium against Eimeria tenella infection in chickens. Int. J. Parasitol. 2005, 35:777-785.
72. Pogonka T., et al. A single dose of recombinant Salmonella typhimurium induces specific humoral immune responses against heterologous Eimeria tenella antigens in chicken. Int. J. Parasitol. 2003, 33:81-88.
73. Wang Q., et al. Protective immunity of recombinant Mycobacterium bovis BCG expressing rhomboid gene against Eimeria tenella challenge. Vet. Parasitol. 2009, 160:198-203.
74. Sathish K., et al. Plant expressed EtMIC2 is an effective immunogen in conferring protection against chicken coccidiosis. Vaccine 2011, 29:9201-9208.
75. Sathish K., et al. Plant expressed coccidial antigens as potential vaccine candidates in protecting chicken against coccidiosis. Vaccine 2012, 30:4460-4464.
76. Zimmermann J., et al. Antibody expressing pea seeds as fodder for prevention of gastrointestinal parasitic infections in chickens. BMC Biotechnol. 2009, 9:79.
77. Bumstead N., Millard B. Variation in susceptibility of inbred lines of chickens to seven species of Eimeria. Parasitology 1992, 104:407-413.
78. Lee S., et al. Effects of dietary supplementation with phytonutrients on vaccine-stimulated immunity against infection with Eimeria tenella. Vet. Parasitol. 2011, 181:97-105.
79. Peek H., Landman W. Coccidiosis in poultry: anticoccidial products, vaccines and other prevention strategies. Vet. Q. 2011, 31:143-161.
80. Chapman H., et al. Guidelines for evaluating the efficacy and safety of live anticoccidial vaccines, and obtaining approval for their use in chickens and turkeys. Avian Pathol. 2005, 34:279-290.
81. British Pharmacopoeia (Veterinary) Coccidiosis vaccine (live) for chickens. Br. Pharmacopoeia 2012, Ph. Eur. monograph 2326. http://bp2012.infostar.com.cn/Bp2012.aspx?a=query%38title=%22Coccidiosis+Vaccine+(Live)+for+Chickens%22%38tab=a-z+index%38l=C%38xh=1.
82. Yan W., et al. Stable transfection of Eimeria tenella: constitutive expression of the YFP-YFP molecule throughout the life cycle. Int. J. Parasitol. 2009, 39:109-117.
83. Clark J., et al. A toolbox facilitating stable transfection of Eimeria species. Mol. Biochem. Parasitol. 2008, 162:77-86.
84. Huang X., et al. Transgenic Eimeria tenella expressing enhanced yellow fluorescent protein targeted to different cellular compartments stimulated dichotomic immune responses in chickens. J. Immunol. 2011, 187:3595-3602.
85. Clark J., et al. Eimeria species parasites as novel vaccine delivery vectors: anti-Campylobacter jejuni protective immunity induced by Eimeria tenella-delivered CjaA. Vaccine 2012, 30:2683-2688.
86. Zou J., et al. Transfection of Eimeria and Toxoplasma using heterologous regulatory sequences. Int. J. Parasitol. 2009, 39:1189-1193.
87. Liu X., et al. Development of transgenic lines of Eimeria tenella expressing M2e-enhanced yellow fluorescent protein (M2e-EYFP). Vet. Parasitol. 2013, 193:1-7.
88. Pinard-van der Laan M., et al. Microsatellite mapping of QTLs affecting resistance to coccidiosis (Eimeria tenella) in a Fayoumi×White Leghorn cross. BMC Genomics 2009, 10:31.
89. Kranis A., et al. Development of a high density 600K SNP genotyping array for chicken. BMC Genomics 2013, 14:59.
90. Jenkins M., et al. cDNA encoding an immunogenic region of a 22kilodalton surface protein of Eimeria acervulina sporozoites. Mol. Biochem. Parasitol. 1989, 32:153-161.
91. Kim K., et al. Immunization of chickens with live Escherichia coli expressing Eimeria acervulina merozoite recombinant antigen induces partial protection against coccidiosis. Infect. Immun. 1989, 57:2434-2440.
92. Todryk S., Hill A. Malaria vaccines: the stage we are at. Nat. Rev. Microbiol. 2007, 5:487-489.
93. Rose M., Hesketh P. Immunity to coccidiosis: stages of the life-cycle of Eimeria maxima which induce, and are affected by, the response of the host. Parasitology 1976, 73:25-37.
94. Beattie S., et al. A comparison of sporozoite transport after homologous and heterologous challenge in chickens immunized with the Guelph strain or the Florida strain of Eimeria maxima. Parasitol. Res. 2001, 87:116-121.
95. Dalloul R., et al. In ovo administration of CpG oligodeoxynucleotides and the recombinant microneme protein MIC2 protects against Eimeria infections. Vaccine 2005, 23:3108-3113.
96. Ding X., et al. In ovo vaccination with the Eimeria tenella EtMIC2 gene induces protective immunity against coccidiosis. Vaccine 2005, 23:3733-3740.
97. Song H., et al. Efficacy of DNA vaccines carrying Eimeria acervulina lactate dehydrogenase antigen gene against coccidiosis. Exp. Parasitol. 2010, 126:224-231.
98. Liu Y., et al. Protective immunity induced by a DNA vaccine encoding Eimeria tenella rhomboid against homologous challenge. Parasitol. Res. 2013, 112:251-257.
99. Crane M., et al. Cross-protection against four species of chicken coccidia with a single recombinant antigen. Infect. Immun. 1991, 59:1271-1277.