Advertisement

Parasitology Research

, Volume 118, Issue 6, pp 1701–1710 | Cite as

A review of Eimeria antigen identification for the development of novel anticoccidial vaccines

  • J. Venkatas
  • M. A. AdelekeEmail author
Protozoology - Review

Abstract

Coccidiosis is a major poultry disease which compromises animal welfare and costs the global chicken industry a huge economic loss. As a result, research entailing coccidial control measures is crucial. Coccidiosis is caused by Eimeria parasites that are highly immunogenic. Consequently, a low dosage of the Eimeria parasite supplied by a vaccine will enable the host organism to develop an innate immune response towards the pathogen. The production of traditional live anticoccidial vaccines is limited by their low reproductive index and high production costs, among other factors. Recombinant vaccines overcome these limitations by eliciting undesired contaminants and prevent the reversal of toxoids back to their original toxigenic form. Recombinant vaccines are produced using defined Eimeria antigens and harmless adjuvants. Thus, studies regarding the identification of potent novel Eimeria antigens which stimulate both cell-mediated and humoral immune responses in chickens are essential. Although the prevalence and risk posed by Eimeria have been well established, there is a dearth of information on genetic and antigenic diversity within the field. Therefore, this paper discusses the potential and efficiency of recombinant vaccines as an anticoccidial control measure. Novel protective Eimeria antigens and their antigenic diversity for the production of cheap, easily accessible recombinant vaccines are also reviewed.

Keywords

Antigenic diversity Coccidiosis Eimeria Poultry Vaccine 

Notes

Funding information

The National Research Foundation (NRF) provided financial support (Grant numbers: 112768 and 116935).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Al-Idreesi SR, Kweider M, Katranji MM (2013) Immune responses to Eimeria tenella sporozoite protein as vaccine to broiler against Coccidiosis. Int J Poult Sci 12:582–591CrossRefGoogle Scholar
  2. Arafat N, Abbas I (2018) Coccidia of Japanese quail: from identification, prevalence, infection, and immunization. J Parasitol 104:23–30CrossRefPubMedGoogle Scholar
  3. Aswathi PB, Bhanja SK, Yadav AS, Rekha V, John JK, Gopinath D, Sadanandan GV, Shinde A, Jacob A (2014) Plant based edible vaccines against poultry diseases?: a review. Adv Anim Vet Sci 2:305–311CrossRefGoogle Scholar
  4. Barta JR, Berghman L, Shivaramaiah S, Faulkner OB, Bielke L, Hargis B (2018) Compositions and methods of enhancing immune responses to Eimeria or limiting Eimeria infection. United States patent US 9,884,099 https://patents.google.com/patent/US9884099B2/en Accessed 28 Dec 2018
  5. Blake DP (2015) Eimeria genomics: where are we now and where are we going? Vet Parasitol 212:68–74CrossRefPubMedGoogle Scholar
  6. Blake DP, Tomley FM (2014) Securing poultry production from the ever-present Eimeria challenge. Trends Parasitol 30:12–19CrossRefPubMedGoogle Scholar
  7. Blake DP, Clark EL, Macdonald SE, Thenmozhi V, Kundu K, Garg R, Jatau ID, Ayoade S, Kawahara F, Moftah A, Reid AJ, Adebambo AO, Alvarez-Zapata R, Srinivasa-Rao AS, Thangaraj K, Banerjee PS, Dhinakar-Raj G, Raman M, Tomley FM (2015) Population, genetic, and antigenic diversity of the apicomplexan Eimeria tenella and their relevance to vaccine development. Proc Natl Acad Sci U S A 112:5343–5350CrossRefGoogle Scholar
  8. Blake DP, Pastor-Fernández I, Nolan MJ, Tomley FM (2017) Recombinant anticoccidial vaccines-a cup half full? Infect Genet Evol 55:358–365CrossRefPubMedGoogle Scholar
  9. Blevin RE, Kim SA, Park SH, Rivera R, Ricke SC (2018) Historical, current, and future prospects for food safety in poultry product processing systems. In Food and Feed Safety Systems and Analysis. Academic Press, London, 323–345Google Scholar
  10. Bottje W, Hargis B, Berghman L, Kwon YM, Cole K, Cox M, Layton S, El-Ashram S, Barta J, Tellez G (2018) Compositions and methods of enhancing immune responses to Eimeria. U.S. Patent Application. https://patents.google.com/patent/US10016493B2/en Accessed on 28 Dec 2018
  11. Brothers VM, Kuhn I, Paul LS, Gabe JD, Andrews WH, Sias SR, McCaman MT, Dragon EA, Files JG (1998) Characterization of a surface antigen of Eimeria tenella sporozoites and synthesis from a cloned cDNA in Escherichia coli. Mol Biochem Parasitol 28:235–247CrossRefGoogle Scholar
  12. Brown-Jordan A, Blake D, Beard J, Beharry A, Serrette L, Soleyn A, Oura C (2018) Molecular identification of Eimeria species in broiler chickens in Trinidad, West Indies. Vet Sci 5:12–21CrossRefPubMedCentralGoogle Scholar
  13. Cheng P, Wang C, Lin X, Zhang L, Fei C, Zhang K, Wang X (2018) Pharmacokinetics of a novel triazine ethanamizuril in rats and broiler chickens. Res Vet Sci 117:99–103CrossRefPubMedGoogle Scholar
  14. Clark JD, Oakes RD, Redhead K, Crouch CF, Francis MJ, Tomley FM, Blake DP (2012) Eimeria species parasites as novel vaccine delivery vectors: anti-Campylobacter jejuni protective immunity induced by Eimeria tenella delivered CjaA. Vaccine 30:2683–2688CrossRefPubMedGoogle Scholar
  15. Clark EL, Macdonald SE, Thenmozhi V, Kundu K, Garg R, Kumar S, Ayoade S, Fornace KM, Jatau ID, Moftah A, Nolan MJ (2016) Cryptic Eimeria genotypes are common across the southern but not northern hemisphere. Int J Parasitol 46:537–544CrossRefPubMedPubMedCentralGoogle Scholar
  16. Clark EL, Tomley FM, Blake DP (2017) Are Eimeria genetically diverse, and does it matter? Trends Parasitol 33:231–241CrossRefPubMedGoogle Scholar
  17. Dkhil MA, Al-Quraishy S (2016) Nanoparticles against Eimeriosis. InNanoparticles in the fight against parasites. Springer, Cham. 1; 207–210Google Scholar
  18. Gadelhaq SM, Arafa WM, Aboelhadid SM (2015) Molecular characterization of Eimeria species naturally infecting Egyptian Baldi chickens. Iran J Parasitol 10:87–95PubMedPubMedCentralGoogle Scholar
  19. Guven E, Beckstead RB, Kar S, Vatansever Z, Karaer Z (2013) Molecular identification of Eimeria species of broiler chickens in Turkey. Ank Univ Vet Fak Derg 60:245–250Google Scholar
  20. Hoelzer K, Bielke L, Blake DP, Cox E, Cutting SM, Devriendt B, Erlacher-Vindel E, Goossens E, Karaca K, Lemiere S, Metzner M (2018) Vaccines as alternatives to antibiotics for food producing animals. Part 2: new approaches and potential solutions. Vet Res 49:70–82CrossRefPubMedPubMedCentralGoogle Scholar
  21. Huang J, Liu T, Li K, Song X, Yan R, Xu L, Li X (2018a) Proteomic analysis of protein interactions between Eimeria maxima sporozoites and chicken jejunal epithelial cells by shotgun LC-MS/MS. Parasit Vectors 11:226–230CrossRefPubMedPubMedCentralGoogle Scholar
  22. Huang X, Liu J, Tian D, Li W, Zhou Z, Huang J, Song X, Xu L, Yan R, Li X (2018b) The molecular characterization and protective efficacy of microneme 3 of Eimeria mitis in chickens. Vet Parasitol 258:114–123CrossRefPubMedGoogle Scholar
  23. Jacob SS, Cherian S, Sumithra TG, Raina OK, Sankar M (2013) Edible vaccines against veterinary parasitic diseases – current status and future prospects. Vaccine 31:1879–1885CrossRefPubMedGoogle Scholar
  24. Jang SI, Lillehoj HS, Lee SH, Lee KW, Park MS, Cha SR, Lillehoj EP, Subramanian BM, Sriraman R, Srinivasan VA (2010) Eimeria maxima recombinant Gam82 gametocyte antigen vaccine protects against coccidiosis and augments humoral and cell-mediated immunity. Vaccine 28:2980–2985CrossRefPubMedGoogle Scholar
  25. Jang SI, Lillehoj HS, Lee SH, Lee KW, Lillehoj EP, Hong YH, An DJ, Jeong W, Chun JE, Bertrand F, Dupuis L, Deville S, Arous JB (2012) Vaccination with Clostridium perfringens recombinant proteins in combination with Montanide™ ISA 71 VG adjuvant increases protection against experimental necrotic enteritis in commercial broiler chickens. Vaccine 30:5401–5406CrossRefPubMedGoogle Scholar
  26. Jenkins MC, Parker C, Ritter D (2017) Eimeria oocyst concentrations and species composition in litter from commercial broiler farms during anticoccidial drug or live Eimeria oocyst vaccine control programs. Avian Dis 61:214–220CrossRefPubMedGoogle Scholar
  27. Jenkins MC, Stevens L, O'Brien C, Parker C, Miska K, Konjufca V (2018) Incorporation of a recombinant Eimeria maxima IMP1 antigen into nanoparticles confers protective immunity against E. Maxima challenge infection. Vaccine 36:1126–1131CrossRefPubMedGoogle Scholar
  28. Klotz C, Gehre F, Lucius R, Pogonka T (2007) Identification of Eimeria tenella genes encoding for secretory proteins and evaluation of candidates by DNA immunisation studies in chickens. Vaccine 25:6625–6634CrossRefPubMedGoogle Scholar
  29. Kundu K, Garg R, Kumar S, Mandal M, Tomley FM, Blake DP, Banerjee PS (2017) Humoral and cytokine response elicited during immunisation with recombinant immune mapped protein-1 (EtIMP-1) and oocysts of Eimeria tenella. Vet Parasitol 244:44–53CrossRefPubMedGoogle Scholar
  30. Li JH, Huang XS, Zhang GC (2010) Immune response and protective efficacy against homologous challenge in BALB/c mice vaccinate with DNA vaccine encoding Toxoplasma gondiiactin depolymerizing factor gene. Vet Parasitol 179:1–6CrossRefGoogle Scholar
  31. Li J, Zheng J, Gong P, Zhang X (2012) Efficacy of Eimeria tenella rhomboid-like protein as a subunit vaccine in protective immunity against homologous challenge. Parasitol Res 110:1139–1145CrossRefPubMedGoogle Scholar
  32. Li WC, Zhang XK, Du L, Pan L, Gong PT, Li JH, Yang J, Li H, Zhang XC (2013) Eimeria maxima: efficacy of recombinant Mycobacterium bovis BCG expressing apical membrane antigen1 against homologous infection. Parasitol Res 112:3825–3833CrossRefPubMedGoogle Scholar
  33. Li J, Wang F, Ma C, Huang Y, Wang D, Ma D (2018) Recombinant lactococcus lactis expressing Eimeria tenella AMA1 protein and its immunological effects against homologous challenge. Exp Parasitol 191:1–8CrossRefPubMedGoogle Scholar
  34. Lillehoj HS, Jang SI, Panebra A, Lillehoj EP, Dupuis L, Arous JB, Lee SK, Oh ST (2017) In ovo vaccination using Eimeria profilin and Clostridium perfringens NetB proteins in Montanide IMS adjuvant increases protective immunity against experimentally-induced necrotic enteritis. Asian Australas J Anim Sci 30:1478–1489CrossRefPubMedPubMedCentralGoogle Scholar
  35. Lillehoj HS, Sungtaek OH, Panebra A (2018) Eimeria tenella elongation factor-1 alpha recombinant immunogenic compositions which induce active protective immunity against avian coccidiosis. United States patent application US 15/887,130. https://patents.google.com/patent/US20180230475A1/en Accessed 3 Jan 2019
  36. Lin RQ, Lillehoj HS, Lee SK, Oh S, Panebra A, Lillehoj EP (2017) Vaccination with Eimeria tenella elongation factor-1α recombinant protein induces protective immunity against E. tenella and E. maxima infections. Vet Parasitol 243:79–84CrossRefPubMedGoogle Scholar
  37. Liu Y, Zheng J, Li J, Gong P, Zhang X (2013) Protective immunity induced by a DNA vaccine encoding Eimeria tenella rhomboid against homologous challenge. Parasitol Res 112:251–257CrossRefPubMedGoogle Scholar
  38. Liu D, Cao L, Zhu Y, Deng C, Su S, Xu J, Jin W, Li J, Wu L, Tao J (2014) Cloning and characterization of an Eimeria necatrix gene encoding a gametocyte protein and associated with oocyst wall formation. Parasit Vectors 7:27–35CrossRefPubMedPubMedCentralGoogle Scholar
  39. Liu L, Huang X, Liu J, Li W, Ji Y, Tian D, Tian L, Yang X, Xu L, Yan R, Li X (2017) Identification of common immunodominant antigens of Eimeria tenella, Eimeria acervulina and Eimeria maxima by immunoproteomic analysis. Oncotarget 8:34935–34941PubMedPubMedCentralGoogle Scholar
  40. Liu T, Huang J, Ehsan M, Wang S, Hong F, Zhou Z, Li X (2018) Protective immunity against Eimeria maxima induced by vaccines of Em14-3-3 antigen. Vet Parasitol 251:241–249Google Scholar
  41. Marugan-Hernandez V, Cockle C, Macdonald S, Pegg E, Crouch C, Blake DP, Tomley FM (2016) Viral proteins expressed in the protozoan parasite Eimeria tenella are detected by the chicken immune system. Parasit Vectors 9:463–478CrossRefPubMedPubMedCentralGoogle Scholar
  42. Matsubayashi M, Teramoto-Kimata I, Uni S, Lillehoj HS, Matsuda H, Furuya M, Sasai K (2013) Elongation factor-1α is a novel protein associated with host cell invasion and a potential protective antigen of Cryptosporidium parvum. J Biol Chem 288:34111–34120CrossRefPubMedPubMedCentralGoogle Scholar
  43. Meunier M, Chemaly M, Dory D (2016) DNA vaccination of poultry: the current status in 2015. Vaccine 34:202–211CrossRefPubMedGoogle Scholar
  44. Muthamilselvan T, Kuo TF, Wu YC, Yang WC (2016) Herbal remedies for coccidiosis control: a review of plants, compounds, and anticoccidial actions. eCAM 2016:301–311Google Scholar
  45. Odden A, Denwood MJ, Stuen S, Robertson LJ, Ruiz A, Hamnes IS, Enemark HL (2018) Field evaluation of anticoccidial efficacy: a novel approach demonstrates reduced efficacy of toltrazuril against ovine Eimeria spp. in Norway. Int J Parasitol Drugs Drug Resist 8:304–311CrossRefPubMedPubMedCentralGoogle Scholar
  46. Panebra A, Lillehoj HS (2019) Eimeria tenella elongation factor-1α (EF-1α) co-administered with chicken IL-7 (chIL-7) DNA vaccine emulsified in Montanide gel 01 adjuvant enhanced the immune response to E. acervulina infection in broiler chickens. Avian Dis 63:145–152CrossRefGoogle Scholar
  47. Pastor-Fernández I, Kim S, Billington K, Bumstead J, Marugán-Hernández V, Küster T, Tomley FM (2018) Development of cross-protective Eimeria-vectored vaccines based on apical membrane antigens. Int J Parasitol 48:505–518CrossRefPubMedGoogle Scholar
  48. Patra G, Kumar A, Ghosh S, Lalnunpuia C, Bachan M, Saikia B, Bhagawati J (2017) Vaccines against protozoan parasites of veterinary importance: a review. J Entomol Zool Stud 5:1016–1021Google Scholar
  49. Prakashbabu BC, Thenmozhi V, Limon G, Kundu K, Kumar S, Garg R, Clark EL, Rao AS, Raj DG, Raman M, Banerjee PS (2017) Eimeria species occurrence varies between geographic regions and poultry production systems and may influence parasite genetic diversity. Vet Parasitol 233:62–72CrossRefGoogle Scholar
  50. Price KR, Hafeez MA, Bulfon J, Barta JR (2016) Live Eimeria vaccination success in the face of artificial non-uniform vaccine administration in conventionally reared pullets. Avian Pathol 45:82–93CrossRefPubMedGoogle Scholar
  51. Qi X, Fu Y, Wang RY, Ng CN, Dang H, He Y (2018) Improving the sustainability of agricultural land use: an integrated framework for the conflict between food security and environmental deterioration. Appl Geogr 90:214–223CrossRefGoogle Scholar
  52. Rafiqi SI, Garg R, Reena KK, Ram H, Singh M, Banerjee PS (2018) Immune response and protective efficacy of Eimeria tenella recombinant refractile body protein, EtSO7, in chickens. Vet Parasitol https://www.sciencedirect.com/science/article/pii/S0304401718302334 Accessed 28 Dec 2018 258:108–113CrossRefPubMedGoogle Scholar
  53. Rafiqi SI, Garg R, Ram H, Reena KK, Asari M, Kumari P, Kundave VR, Singh M, Banerjee PS (2019) Immunoprophylactic evaluation of recombinant gametocyte 22 antigen of Eimeria tenella in broiler chickens. Parasitol Res 118:945–953CrossRefPubMedGoogle Scholar
  54. Reid AJ, Blake DP, Ansari HR, Billington K, Browne HP, Bryant JM, Dunn M, Hung SS, Kawahara F, Miranda-Saavedra D, Malas T (2014) Genomic analysis of the causative agents of coccidiosis in domestic chickens. Genome Res 24:1676–1685CrossRefPubMedPubMedCentralGoogle Scholar
  55. Ritzi MM, Abdelrahman W, Van-Heerden K, Mohnl M, Barrett NW, Dalloul RA (2016) Combination of probiotics and coccidiosis vaccine enhances protection against an Eimeria challenge. Vet Res 47:111–121CrossRefPubMedPubMedCentralGoogle Scholar
  56. Sathish K, Sriraman R, Subramanian BM, Rao NH, Balaji K, Narasu ML, Srinivasan VA (2011) Plant expressed EtMIC2 is an effective immunogen in conferring protection against chicken coccidiosis. Vaccine 29:9201–9208CrossRefPubMedGoogle Scholar
  57. Sathish K, Mohana S, Bala MS, Harini C, Ponanna NM, Srinivasan VA, Rajan S (2017) Subunit vaccine based on plant expressed recombinant Eimeria gametocyte antigen Gam82 elicit protective immune response against chicken coccidiosis. J Vaccines 8:6–13Google Scholar
  58. Shivaramaiah C, Barta J, Hernandez-Velasco X, Téllez G, Hargis B (2014) Coccidiosis: recent advancements in the immunobiology of Eimeria species, preventive measures, and the importance of vaccination as a control tool against these apicomplexan parasites. Dove Press https://www.dovepress.com/coccidiosis-recent-advancements-in-the-immunobiology-of-eimeria-specie-peer-reviewed-fulltext-article-VMRR#ref27 Accessed 12 Jan 2019
  59. Smith AL, Hesketh P, Archer A, Shirley MW (2002) Antigenic diversity in Eimeria maxima and the influence of host genetics and immunization schedule on cross-protective immunity. Infect Immun 70:2472–2479CrossRefPubMedPubMedCentralGoogle Scholar
  60. Song H, Yan R, Xu L, Song X, Shah MAA, Zhu H, Li X (2010) Efficacy of DNA vaccines carrying Eimeria acervulina lactate dehydrogenase antigen gene against coccidiosis. Exp Parasitol 126:224–231CrossRefPubMedGoogle Scholar
  61. Song X, Ren Z, Yan R, Xu L, Li X (2015) Induction of protective immunity against Eimeria tenella, Eimeria necatrix, Eimeria maxima and Eimeria acervulina infections using multivalent epitope DNA vaccines. Vaccine 33:2764–2770CrossRefPubMedGoogle Scholar
  62. Sun H, Wang L, Wang T, Zhang J, Liu Q, Chen P, Zhao X (2014) Display of Eimeria tenella EtMic2 protein on the surface of Saccharomyces cerevisiae as a potential oral vaccine against chicken coccidiosis. Vaccine 32:1869–1876CrossRefPubMedGoogle Scholar
  63. Sundar STB, Harikrishnan TJ, Latha BR, Chandra GS, Kumar TMSA (2017) Anticoccidial drug resistance in chicken coccidiosis and promising solutions: a review. J Entomol Zool Stud 5:1526–1529Google Scholar
  64. Suprihati E, Yunus M (2018) Evaluation of the antigenicity and immunogenicity of Eimeria tenella by reproductive index and histopathological changes of cecal coccidiosis virulent live vaccine in broiler chickens. Afr J Infect Dis 12:104–110PubMedPubMedCentralGoogle Scholar
  65. Tan L, Li Y, Yang X, Ke Q, Lei W, Mughal MN, Zhao J (2017) Genetic diversity and drug sensitivity studies on Eimeria tenella field isolates from Hubei Province of China. Parasit Vectors 10:137–149CrossRefPubMedPubMedCentralGoogle Scholar
  66. Tang X, Liu X, Yin G, Suo J, Tao G, Zhang S, Suo X (2018a) A novel vaccine delivery model of the apicomplexan Eimeria tenella expressing Eimeria maxima antigen protects chickens against infection of the two parasites. Front Immunol 8:1982–1994CrossRefPubMedPubMedCentralGoogle Scholar
  67. Tang X, Suo J, Li C, Du M, Wang C, Hu D, Duan C, Lyu Y, Liu X, Suo X (2018b) Transgenic Eimeria tenella expressing profilin of Eimeria maxima elicits enhanced protective immunity and alters gut microbiome of chickens. Infect Immun 86:00808–00817Google Scholar
  68. Tian L, Li W, Huang X, Tian D, Liu J, Yang X, Song X (2017) Protective efficacy of coccidial common antigen glyceraldehyde 3-phosphate dehydrogenase (GAPDH) against challenge with three Eimeria species. Front Microbiol 8:124–132Google Scholar
  69. Vrba V, Pakandl M (2014) Coccidia of turkey: from isolation, characterisation and comparison to molecular phylogeny and molecular diagnostics. Int J Parasitol 44:985–1000CrossRefPubMedGoogle Scholar
  70. Wang Q, Chen L, Li J, Zheng J, Cai N, Gong P, Li S, Li H, Zhang X (2014) A novel recombinant BCG vaccine encoding Eimeria tenella rhomboid and chicken IL-2 induces protective immunity against coccidiosis. Korean J Parasitol 52:251–258CrossRefPubMedPubMedCentralGoogle Scholar
  71. Wiedmer S, Erdbeer A, Volke B, Randel S, Kapplusch F, Hanig S, Kurth M (2017) Identification and analysis of Eimeria nieschulzi gametocyte genes reveal splicing events of gam genes and conserved motifs in the wall-forming proteins within the genus Eimeria (Coccidia, Apicomplexa). Parasite 2017:24–30Google Scholar
  72. Xu Q, Song X, Xu L, Yan R, Shah MA, Li X (2008) Vaccination of chickens with a chimeric DNA vaccine encoding Eimeria tenella TA4 and chicken IL-2 induces protective immunity against coccidiosis. Vet Parasitol 156:319–323CrossRefPubMedGoogle Scholar
  73. Xu J, Zhang Y, Tao J (2013) Efficacy of a DNA vaccine carrying Eimeria maxima Gam56 antigen gene against coccidiosis in chickens. Korean J parasitol 51:147–156CrossRefPubMedPubMedCentralGoogle Scholar
  74. Yan M, Cui X, Zhao Q, Zhu S, Huang B, Wang L, Zhao H, Liu G, Li Z, Han H, Dong H (2018) Molecular characterization and protective efficacy of the microneme 2 protein from Eimeria tenella. Parasite 25:153–164CrossRefGoogle Scholar
  75. Yang R, Brice B, Ryan U (2016) Morphological and molecular characterization of Eimeria purpureicephali n. sp. (Apicomplexa: Eimeriidae) in a red-capped parrot (Purpureicephalus spurius, Kuhl, 1820) in Western Australia. Int J Parasitol Parasites Wildl 5:34–39CrossRefPubMedPubMedCentralGoogle Scholar
  76. Yang G, Yao J, Yang W, Jiang Y, Du J, Huang H, Gu W, Hu J, Ye L, Shi C, Shan B (2017) Construction and immunological evaluation of recombinant lactobacillus plantarum expressing SO7 of Eimeria tenella fusion DC-targeting peptide. Vet Parasitol 236:7–13CrossRefPubMedGoogle Scholar
  77. Zhang DF, Xu H, Sun BB, Li JQ, Zhou QJ, Zhang HL, Du AF (2012) Adjuvant effect of ginsenoside-based nanoparticles (ginsomes) on the recombinant vaccine against Eimeria tenella in chickens. Parasitol Res 110:2445–2453CrossRefPubMedGoogle Scholar
  78. Zhao YL, Bao YZ, Zhang LJ, Chang LY, Jiang LF, Liu YW, Zhang L, Qin JH (2013) Biosafety of the plasmid pcDNA3-1E of Eimeria acervulina in chicken. Exp Parasitol 133:231–236CrossRefPubMedGoogle Scholar
  79. Zhao Y, Xu R, Zhang Y, Ji X, Zhang J, Liu Y, Bao Y, Qin J (2014) Protective efficacy in chickens of recombinant plasmid pET32a (+)-ADF-3-1E of Eimeria acervulina. Parasitol Res 113:3007–3014CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Discipline of Genetics, School of Life SciencesUniversity of KwaZulu-NatalDurbanSouth Africa

Personalised recommendations