Genetic selection of Eimeria parasites in the chicken for improvement of poultry health: implications for drug resistance and live vaccine development

References

• Augustine, P.C., Smith, C.K., Danforth, H.D. & Ruff, M.D. (1987). Effect of ionophorous anticoccidials on invasion and development of Eimeria: comparison of sensitive and resistant isolates and correlation with drug uptake. Poultry Science, 66, 960–965. PMID: 3658886.
   PubMed Web of Science ®Google Scholar
• Aunin, E., Böhme, U., Blake, D., Dove, A., Smith, M., Corton, C., Oliver, K., Betteridge, E., Quail, M.A., McCarthy, S.A., Wood, J., Tracey, A., Torrance, J., Sims, Y., Howe, K., Challis, R., Berriman, M. & Reid, A. (2021). The complete genome sequence of Eimeria tenella (Tyzzer 1929), a common gut parasite of chickens. Wellcome Open Research, 6, 225. PMID: 34703904; PMCID: PMC8515493.
   PubMedGoogle Scholar
• Bafundo, K.W. & Jeffers, T.K. (1990). Selection for resistance to monensin, nicarbazin and the monensin plus nicarbazin combination. Poultry Science, 69, 1485–1490. PMID: 2247409.
   PubMed Web of Science ®Google Scholar
• Ball, S.J. (1968). The stability of resistance to glycarbylamide and 2-chloro-4-nitrobenzamide in Eimeria tenella. Research in Veterinary Science, 9, 149–151. PMID: 5651191.
   PubMed Web of Science ®Google Scholar
• Blake, D.P., Billington, K.J., Copestake, S.L., Oakes, R.D., Quail, M.A., Wan, K., Shirley, M.W. & Smith, A.L. (2011). Genetic mapping identifies novel highly protective antigens for an apicomplexan parasite. Plos Pathogens, 7, 1–13. PMID: 21347348; PMCID: PMC3037358.
   Web of Science ®Google Scholar
• Blake, D.P., Oakes, R. & Smith, A.L. (2011). A genetic linkage map for the apicomplexan protozoan parasite Eimeria maxima and comparison with E. tenella. International Journal for Parasitology, 41, 263–270. PMID: 20934427.
   PubMed Web of Science ®Google Scholar
• Blake, D.P., Clark, E.L., Macdonald, S.E., Thenmozhi, V., Kundu, K., Garg, R., Jatau, I.D., Ayoade, S., Kawahara, F., Moftah, A., Reid, A.J., Adebambo, A.O., Alvarez Zapata, R., Srinivasa Rao, A.S., Thangaraj, K., Banerjee, P.S., Dhinakar-Raj, G., Raman, M. & Tomley, F.M. (2015). Population, genetic, and antigenic diversity of the apicomplexan Eimeria tenella and their relevance to vaccine development. Proceedings of the National Academy of Sciences USA A, 112, E5343–E5350. PMID: 26354122; PMCID: PMC4586875.
   PubMed Web of Science ®Google Scholar
• Blake, D.P., Pastor-Fernández, I., Nolan, M.J. & Tomley, F.M. (2017). Recombinant anticoccidial vaccines – a cup half full? Infection, Genetics and Evolution, 55, 358–365. PMID: 29017798.
   PubMed Web of Science ®Google Scholar
• Borges, S., Cravo, P., Creasey, A., Fawcett, R., Modrzynska, K., Rodrigues, L., Martinelli, A. & Hunt, P. (2011). Genomewide scan reveals amplification of mdr1 as a common denominator of resistance to mefloquine, lumefantrine, and artemisinin in Plasmodium chabaudi malaria parasites. Antimicrobial Agents and Chemotherapy, 55, 4858–4865. PMID: 21709099; PMCID: PMC3186966.
   PubMed Web of Science ®Google Scholar
• Canning, E.U. & Morgan, K. (1975). DNA synthesis, reduction, and elimination during life cycles of the Eimeriine Coccidian, Eimeria tenella and the haemogregarine, Hepatozoon domerguei. Experimental Parasitology, 38, 217–227. PMID: 809292.
   PubMed Web of Science ®Google Scholar
• Cervantes, H.M. (2015). Antibiotic-free poultry production: is it sustainable? Journal of Applied Poultry Research, 24, 91–97.
   Web of Science ®Google Scholar
• Chapman, H.D. (1976a). Eimeria tenella: experimental studies on the development of resistance to robenidine. Parasitology, 73, 265–273. PMID: 1012746.
   PubMed Web of Science ®Google Scholar
• Chapman, H.D. (1976b). Studies on the mode of action of anticoccidial drugs in the chicken and chicken embryo. Veterinary Parasitology, 1, 299–308.
   Google Scholar
• Chapman, H.D. (1978a). Drug resistance in coccidia. In P.L. Long, K.N. Boorman & B.M. Freeman (Eds.), Avian Coccidiosis (pp. 387–412). Proceedings of the 13th Poultry Science Symposium. Edinburgh: British Poultry Science.
   Google Scholar
• Chapman, H.D. (1978b). Eimeria tenella: experimental studies on the development of resistance to amprolium, clopidol and methyl benzoquate. Parasitology, 76, 177–183. PMID: 274682.
   PubMed Web of Science ®Google Scholar
• Chapman, H.D. (1982). Anticoccidial drug resistance. In P.L. Long (Ed.), The Biology of the Coccidia (pp. 429–452). Baltimore: University Park Press.
   Google Scholar
• Chapman, H.D. (1983). Field isolates of Eimeria resistant to arprinocid. Veterinary Parasitology, 12, 45–50. PMID: 6683036.
   PubMed Web of Science ®Google Scholar
• Chapman, H.D. (1984a). Eimeria tenella: experimental development of resistance to monensin in the chicken. Parasitology, 89, 9–16. PMID: 6472888.
   PubMed Web of Science ®Google Scholar
• Chapman, H.D. (1984b). Development by genetic recombination of a line of Eimeria tenella resistant to robenidine, decoquinate and amprolium. Zeitschrift fur Parasitenkünde, 70, 437–441. PMID: 6475205.
   PubMed Web of Science ®Google Scholar
• Chapman, H.D. (1985). Eimeria tenella: development of resistance to arprinocid and decoquinate in the chicken. Research in Veterinary Science, 38, 226–230. PMID: 4001560.
   PubMed Web of Science ®Google Scholar
• Chapman, H.D. (1986a). Eimeria tenella: experimental studies on the development of resistance to halofuginone. Veterinary Parasitology, 21, 83–90. PMID: 3739208.
   PubMed Web of Science ®Google Scholar
• Chapman, H.D. (1986b). Eimeria tenella: stability of resistance to halofuginone, decoquinate and arprinocid in the chicken. Research in Veterinary Science, 40, 139–140. PMID: 3704320.
   PubMed Web of Science ®Google Scholar
• Chapman, H.D. (1989). Eimeria tenella, E. acervulina and E. maxima: studies on the development of resistance to diclazuril and other anticoccidial drugs in the chicken. Parasitology, 99, 189–192.
   PubMed Web of Science ®Google Scholar
• Chapman, H.D. (1997). Biochemical, genetic and applied aspects of drug resistance in Eimeria parasites of the fowl. Avian Pathology, 26, 221–244. PMID: 18483904.
   PubMed Web of Science ®Google Scholar
• Chapman, H.D. (2003). Origins of coccidiosis research in the fowl-the first fifty years. Avian Diseases, 47, 1–20. PMID: 12713154.
   PubMed Web of Science ®Google Scholar
• Chapman, H.D. (2014). Milestones in avian coccidiosis research: a review. Poultry Science, 93, 501–511. PMID: 24604841.
   PubMed Web of Science ®Google Scholar
• Chapman, H.D. (2018). Applied strategies for the control of coccidiosis in poultry. CAB Reviews, 13, 1–11.
   Google Scholar
• Chapman, H.D., Barta, J.R., Blake, D., Gruber, A.M., Jenkins, M., Smith, N.C., Suo, X. & Tomley, F.M. (2013). A selective review of advances in coccidiosis research. Advances in Parasitology, 83, 93–171. PMID: 23876872.
   PubMed Web of Science ®Google Scholar
• Chapman, H.D., Cherry, T.E., Danforth, H.D., Richards, D., Shirley, M.W. & Williams, R.B. (2002). Sustainable coccidiosis control in poultry production: the role of live vaccines. International Journal for Parasitology, 32, 617–629. PMID: 11943233.
   PubMed Web of Science ®Google Scholar
• Chapman, H.D. & Jeffers, T.K. (2014). Vaccination of chickens against coccidiosis ameliorates drug resistance in commercial poultry production. International Journal for Parasitology: Drugs and Drug Resistance, 4, 214–217. PMID: 25516830; PMCID: PMC4266793.
   PubMed Web of Science ®Google Scholar
• Chapman, H.D. & Rose, M.E. (1986). Cloning of Eimeria tenella in the chicken. Journal of Parasitology, 72, 605–606. PMID: 3783355.
   PubMed Web of Science ®Google Scholar
• Chen, T., Huang, B., Zhao, Q., Dong, H., Zhu, S., Zhao, Z., Lv, L., Yan, M. & Han, H. (2018). Molecular characterization and functional analysis of Eimeria tenella malate dehydrogenase. Parasitology Research, 117, 2053–2063. PMID: 29740696.
   PubMed Web of Science ®Google Scholar
• Clark, J.D., Billington, K., Bumstead, J.M., Oakes, R.D., Soon, P.E., Sopp, P., Tomley, F.M. & Blake, D.P. (2008). A toolbox facilitating stable transfection of Eimeria species. Molecular and Biochemical Parasitology, 162, 77–86. PMID: 18723051.
   PubMed Web of Science ®Google Scholar
• Clark, E.L., Macdonald, S.E., Thenmozhi, V., Kundu, K., Garg, R., Kumar, S., Ayoade, S., Fornace, K.M., Jatau, I.D., Moftah, A., Nolan, M.J., Sudhakar, N.R., Adebambo, A.O., Lawal, I.A., Zapata, R.A., Awuni, J.A., Chapman, H.D., Karimuribo, E., Mugasa, C.M., Namangala, B., Rushton, J., Suo, X., Thangaraj, K., Srinivasa Rao, A.S.R., Tewari, A.K., Banerjee, P.S., Raj, G.D., Raman, M., Tomley, F.M. & Blake, D.P. (2016). Cryptic Eimeria genotypes are common across the southern but not northern hemisphere. International Journal for Parasitology, 46, 537–544. PMID: 27368611; PMCID: PMC4978698.
   PubMed Web of Science ®Google Scholar
• Cuckler, A.C. & Malanga, C.M. (1955). Studies on drug resistance in coccidia. Journal of Parasitology, 41, 302–311. PMID: 13252506.
   PubMed Web of Science ®Google Scholar
• Del Cacho, E., Gallego, M., López-Bernard, F., Quílez, J. & Sánchez-Acedo, C. (2005). Differences in HSP70 expression in the sporozoites of the original strain and precocious lines of Eimeria tenella. Journal of Parasitology, 91, 1127–1131. PMID: 16419759.
   PubMed Web of Science ®Google Scholar
• Del Cacho, E., López-Bernard, F., Gallego, M., Quílez, J. & Sánchez-Acedo, C. (1998). Expression and localization of an S100 protein-like molecule in Eimeria tenella. Journal of Parasitology, 84, 1174–1177. PMID: 9920309.
   PubMed Web of Science ®Google Scholar
• Dong, H., Lin, J., Han, H., Jiang, L., Zhao, Q., Zhu, S. & Huang, B. (2011). Analysis of differentially expressed genes in the precocious line of Eimeria maxima and its parent strain using suppression subtractive hybridization and cDNA microarrays. Parasitology Research, 108, 1033–1040. PMID: 21085989.
   PubMed Web of Science ®Google Scholar
• Fang, S., Gu, X., El-Ashram, S., Li, X., Yu, X., Guo, B., Li, H., Liu, N., Liu, X., Cui, P. & Suo, X. (2019). Immune protection provided by a precocious line trivalent vaccine against rabbit Eimeria. Parasitology Research, 275, 108927. PMID: 31639571.
   Google Scholar
• Fry, M. & Williams, R.B. (1984). Effects of decoquinate and clopidol on electron transport in mitochondria of Eimeria tenella (Apicomplexa: coccidia). Biochemical Pharmacology, 33, 229–240. PMID: 6704148.
   PubMed Web of Science ®Google Scholar
• Gardiner, J.L. & McLoughlin, D.K. (1963). Drug resistance in Eimeria tenella. III. Stability of resistance to glycarbylamide. Journal of Parasitology, 49, 657–659. PMID: 14050245.
   PubMed Web of Science ®Google Scholar
• Hu, D., Tang, X., Ben Mamoun, C., Wang, C., Wang, S., Gu, X., Duan, C., Zhang, S., Suo, J., Deng, M., Yu, Y., Suo, X. & Liu, X. (2020). Efficient single-gene and gene family editing in the apicomplexan parasite Eimeria tenella using CRISPR-Cas9. Frontiers in Bioengineering and Biotechnology, 8, 128. PMID: 32158750; PMCID: PMC7052334.
   PubMed Web of Science ®Google Scholar
• Huang, W., Zhu, S., Chen, T., Zhao, Q., Dong, H., Huang, B., Yao, Y., Liu, Z., Yu, Y. & Han, H. (2022). Molecular characterization of glyceraldehyde-3-phosphate dehydrogenase from Eimeria tenella. Parasitology Research, 121, 1749–1760. PMID: 35366097.
   PubMed Web of Science ®Google Scholar
• Jeffers, T.K. (1974a). Immunization against Eimeria tenella using an attenuated strain. In Proceedings of the XV World’s Poultry Congress (pp. 105–107). New Orleans, USA.
   Google Scholar
• Jeffers, T.K. (1974b). Eimeria acervulina and E. maxima: incidence and anticoccidial drug resistance of isolants in major broiler-producing areas. Avian Diseases, 18, 331–342. PMID: 4851799.
   PubMed Web of Science ®Google Scholar
• Jeffers, T.K. (1974c). Genetic transfer of anticoccidial drug resistance in Eimeria tenella. Journal of Parasitology, 60, 900–904. PMID: 4436755.
   PubMed Web of Science ®Google Scholar
• Jeffers, T.K. (1975). Attenuation of Eimeria tenella through selection for precociousness. Journal of Parasitology, 61, 1083–1090. PMID: 1195070.
   PubMed Web of Science ®Google Scholar
• Jeffers, T.K. (1976a). Reduction of anticoccidial drug resistance by massive introduction of drug-sensitive coccidia. Avian Diseases, 20, 649–653. PMID: 985266.
   PubMed Web of Science ®Google Scholar
• Jeffers, T.K. (1976b). Genetic recombination of precociousness and anticoccidial drug resistance in Eimeria tenella. Zeitschrift fur Parasitenkünde, 50, 251–255. PMID: 997719.
   PubMed Web of Science ®Google Scholar
• Jeffers, T.K. (1978). Genetics of coccidia and the host response. In P.L. Long, K.N. Boorman & B.M. Freeman (Eds.), Avian Coccidiosis (pp. 51–125). Proceedings of the 13th Poultry Science Symposium. Edinburgh: British Poultry Science.
   Google Scholar
• Jeffers, T.K. (1985). Attenuation of coccidia – a review. In L.R. McDougald, P.L. Long & L.P. Joyner (Eds.), Research in Avian Coccidiosis (pp. 482–509). Proceedings of the Georgia Coccidiosis Conference, November 19–21. Athens, GA, USA.
   Google Scholar
• Jeffers, T.K. & Bentley, E.J. (1980). Experimental development of monensin resistance in Eimeria meleagrimitis. Poultry Science, 59, 1731–1735. PMID: 7413579.
   PubMed Web of Science ®Google Scholar
• Jeffers, T.K. & Challey, J.R. (1973). Collateral sensitivity to 4-hydroxy-quinolines in Eimeria acervulina strains resistant to meticlorpindol. Journal of Parasitology, 59, 624–630. PMID: 4722581.
   PubMed Web of Science ®Google Scholar
• Johnson, J., Reid, W.M. & Jeffers, T.K. (1979). Practical immunization of chickens against coccidiosis using an attenuated strain of Eimeria tenella. Poultry Science, 58, 37–41. PMID: 471895.
   PubMed Web of Science ®Google Scholar
• Joyner, L.P. (1957). Induced drug-fastness to nitrofurazone in a laboratory strain of Eimeria tenella. The Veterinary Record, 69, 1415–1418.
   Google Scholar
• Joyner, L.P. & Norton, C.C. (1975). Transferred drug-resistance in Eimeria maxima. Parasitology, 71, 385–392. PMID: 1060042.
   PubMed Web of Science ®Google Scholar
• Joyner, L.P. & Norton, C.C. (1977). Further observations on the genetic transfer of drug resistance in Eimeria maxima. Parasitology, 74, 205–213.
   Web of Science ®Google Scholar
• Joyner, L.P. & Norton, C.C. (1978). The activity of methyl benzoquate and clopidol against Eimeria maxima: synergy and drug resistance. Parasitology, 76, 369–377. PMID: 275786.
   PubMed Web of Science ®Google Scholar
• Karavolias, J., Salois, M.J., Baker, K.T. & Watkins, K. (2018). Raised without antibiotics: impact on animal welfare and implications for food policy. Translational Animal Science, 2, 337–348. PMID: 32704717; PMCID: PMC7200433.
   PubMed Web of Science ®Google Scholar
• Liu, X., Shi, T., Ren, H., Su, H., Yan, W. & Suo, X. (2008). Restriction enzyme-mediated transfection improved transfection efficiency in vitro in apicomplexan parasite Eimeria tenella. Molecular and Biochemical Parasitology, 161, 72–75. PMID: 18606196.
   PubMed Web of Science ®Google Scholar
• Long, P.L. (1965). Development of Eimeria tenella in avian embryos. Nature, 208, 509–510. PMID: 5867599.
   PubMed Web of Science ®Google Scholar
• Long, P.L. (1966). The growth of some species of Eimeria in avian embryos. Parasitology, 56, 575–581. PMID: 5968804.
   PubMed Web of Science ®Google Scholar
• Long, P.L. (1972a). Eimeria tenella: reproduction, pathogenicity and immunogenicity of a strain maintained in chick-embryos by serial passage. Journal of Comparative Pathology, 82, 429–437. PMID: 4648337.
   PubMed Web of Science ®Google Scholar
• Long, P.L. (1972b). Eimeria mivati: reproduction, pathogenicity and immunogenicity of a strain maintained in chick embryos by serial passage. Journal of Comparative Pathology, 82, 439–445. PMID: 4648338.
   PubMed Web of Science ®Google Scholar
• Long, P.L. (1973). Endogenous stages of a ‘chick embryo adapted’ strain of Eimeria tenella. Parasitology, 66, 55–62. PMID: 4786834.
   PubMed Web of Science ®Google Scholar
• Long, P.L. & Johnson, J.K. (1988). Eimeria of American chickens: characteristics of six attenuated strains produced by selection for precocious development. Avian Pathology, 17, 305–314. PMID: 18766688.
   PubMed Web of Science ®Google Scholar
• Long, P.L., Johnson, J.K. & Baxter, S. (1985). Eimeria tenella: relative survival of drug-resistant and drug-sensitive populations in floor-pen chickens. Poultry Science, 64, 2403–2405. PMID: 4095074.
   PubMed Web of Science ®Google Scholar
• Long, P.L., Johnson, J.K. & Gore, T.C. (1982). Attenuation of a strain of Eimeria mivati of USA origin by serial embryo passage. Avian Diseases, 26, 305–313. PMID: 7103889.
   PubMed Web of Science ®Google Scholar
• Long, P.L., Millard, B.J., Joyner, L.P. & Norton, C.C. (1976). A guide to laboratory techniques used in the study and diagnosis of avian coccidiosis. Folia Veterinaria Latina, 6, 201–217. PMID: 1010500.
   PubMedGoogle Scholar
• Marugan-Hernandez, V., Cockle, C., Macdonald, S., Pegg, E., Crouch, C., Blake, D.P. & Tomley, F.M. (2016). Viral proteins expressed in the protozoan parasite Eimeria tenella are detected by the chicken immune system. Parasites & Vectors, 9, 463. PMID: 27553200; PMCID: PMC4994267.
   PubMed Web of Science ®Google Scholar
• Marugan-Hernandez, V., Jeremiah, G., Aguiar-Martins, K., Burell, A., Vaughn, S., Xia, D., Randle, N. & Tomley, F. (2020). The growth of Eimeria tenella: characterization and application of quantitative methods to assess sporozoite invasion and endogenous development in cell culture. Frontiers in Cellular and Infection Microbiology, 10, 579833. PMID: 33154954; PMCID: PMC7590826.
   PubMed Web of Science ®Google Scholar
• Matsler, P.L. & Chapman, H.D. (2007). Selection for early (precocious) development of Eimeria meleagridis in the turkey. Avian Diseases, 51, 122–124. PMID: 17461277.
   PubMed Web of Science ®Google Scholar
• Matsubayashi, M., Kawahara, F., Hatta, T., Yamagishi, J., Miyoshi, T., Anisuzzaman, Sasai, K., Isobe, T., Kita, K. & Tsuji, N. (2016). Transcriptional profiles of virulent and precocious strains of Eimeria tenella at sporozoite stage; novel biological insight into attenuated asexual development. Infection, Genetics and Evolution, 40, 54–62. PMID: 26917363.
   PubMed Web of Science ®Google Scholar
• McDonald, V. & Ballingall, S. (1983). Attenuation of Eimeria mivati (= mitis) by selection for precocious development. Parasitology, 86, 371–379. PMID: 6877864.
   PubMed Web of Science ®Google Scholar
• McDonald, V., Ballingall, S. & Shirley, M.W. (1982). A preliminary study of the nature of infection and immunity in chickens given an attenuated line of Eimeria acervulina. Parasitology, 84, 21–30. PMID: 7063253.
   PubMed Web of Science ®Google Scholar
• McDonald, V. & Shirley, M.W. (1985). The asexual development of precocious lines of Eimeria spp. in the chicken. In L.R. McDougald, P.L. Long & L.P. Joyner (Eds.), Research in Avian Coccidiosis (pp. 502–509). Proceedings of the Georgia Coccidiosis Conference, November 19–21. Athens, GA, USA.
   Google Scholar
• McDonald, V., Shirley, M.W. & Bellatti, M.A. (1986a). Eimeria maxima: characteristics of attenuated lines obtained by selection for precocious development in the chicken. Experimental Parasitology, 61, 192–200. PMID: 3956680.
   PubMed Web of Science ®Google Scholar
• McDonald, V., Shirley, M.W. & Millard, B.J. (1986b). A comparative study of two lines of Eimeria tenella attenuated either by selection for precocious development in the chicken or by growth in chicken embryos. Avian Pathology, 15, 323–335. PMID: 18766535.
   PubMed Web of Science ®Google Scholar
• McDougald, L.R. & Jeffers, T.K. (1976a). Eimeria tenella (Sporozoa, Coccidia): gametogony following a single asexual generation. Science, 192, 258–259. PMID: 1257765.
   PubMed Web of Science ®Google Scholar
• McDougald, L.R. & Jeffers, T.K. (1976b). Comparative in vitro development of precocious and normal strains of Eimeria tenella. (Coccidia). Journal of Protozoology, 23, 530–534. PMID: 1003341.
   PubMedGoogle Scholar
• McLoughlin, D.K. (1970a). Coccidiosis: experimental analysis of drug resistance. Experimental Parasitology, 28, 129–136. PMID: 5459861.
   PubMed Web of Science ®Google Scholar
• McLoughlin, D.K. (1970b). Efficacy of buquinolate against ten strains of Eimeria tenella and the development of a resistant strain. Avian Diseases, 14, 126–130. PMID: 5434433.
   PubMedGoogle Scholar
• McLoughlin, D.K. (1971). Drug resistance in Eimeria tenella. X. Restoration of drug sensitivity following exposure of resistant strains to other coccidiostats. Journal of Parasitology, 57, 383–385. PMID: 5553455.
   PubMed Web of Science ®Google Scholar
• McLoughlin, D.K. & Chute, M.B. (1971). Efficacy of decoquinate against eleven strains of Eimeria tenella and development of a decoquinate-resistant strain. Avian Diseases, 15, 342–345. PMID: 5582058.
   PubMed Web of Science ®Google Scholar
• McLoughlin, D.K. & Chute, M.B. (1973a). Efficacy of clopidol against twelve strains of Eimeria tenella, and the development of a clopidol-resistant strain. Avian Diseases, 17, 425–429. PMID: 4712811.
   PubMed Web of Science ®Google Scholar
• McLoughlin, D.K. & Chute, M.B. (1973b). Efficacy of nequinate against thirteen strains of Eimeria tenella and the development of a nequinate-resistant strain. Avian Diseases, 17, 717–721. PMID: 4766564.
   PubMed Web of Science ®Google Scholar
• McLoughlin, D.K. & Gardiner, J.L. (1961). Drug resistance in Eimeria tenella: I. The experimental development of a glycarbylamide-resistant strain. Journal of Parasitology, 47, 1001–1006.
   Web of Science ®Google Scholar
• McLoughlin, D.K. & Gardiner, J.L. (1962). Drug resistance in Eimeria tenella. II. The experimental development of a zoalene-resistant strain. Journal of Parasitology, 48, 341–346.
   Web of Science ®Google Scholar
• McLoughlin, D.K. & Gardiner, J.L. (1967). Drug resistance in Eimeria tenella. V. The experimental development of a nicarbazin-resistant strain. Journal of Parasitology, 53, 930–932. PMID: 6062077.
   PubMed Web of Science ®Google Scholar
• McLoughlin, D.K. & Gardiner, J.L. (1968). Drug resistance in Eimeria tenella. VI. The experimental development of an amprolium-resistant strain. Journal of Parasitology, 54, 582–584. PMID: 5757730.
   PubMed Web of Science ®Google Scholar
• Miotto, O., Amato, R., Ashley, E.A., MacInnis, B., Almagro-Garcia, J., Amaratunga, C., Lim, P., Mead, D., Oyola, S.O., Dhorda, M., Imwong, M., Woodrow, C., Manske, M., Stalker, J., Drury, E., Campino, S., Amenga-Etego, L., Thanh, T.N., Tran, H.T., Ringwald, P., Bethell, D., Nosten, F., Phyo, A.P., Pukrittayakamee, S., Chotivanich, K., Chuor, C.M., Nguon, C., Suon, S., Sreng, S., Newton, P.N., Mayxay, M., Khanthavong, M., Hongvanthong, B., Htut, Y., Han, K.T., Kyaw, M.P., Faiz, M.A., Fanello, C.I., Onyamboko, M., Mokuolu, O.A., Jacob, C.G., Takala-Harrison, S., Plowe, C.V., Day, N.P., Dondorp, A.M., Spencer, C.C., McVean, G., Fairhurst, R.M., White, N.J. & Kwiatkowski, D.P. (2015). Genetic architecture of artemisinin-resistant Plasmodium falciparum. Nature Genetics, 47, 226–234. PMID: 25599401; PMCID: PMC4545236.
   PubMed Web of Science ®Google Scholar
• Nakamura, T., Konishi, T., Kawaguchi, H. & Hayashi, Y. (1988). Glucose phosphate isomerase isozymes as genetic markers for lines of Eimeria tenella. Parasitology, 96, 281–288. PMID: 3163795.
   PubMed Web of Science ®Google Scholar
• Norton, C.C. & Joyner, L.P. (1975). The development of drug-resistant strains of Eimeria maxima in the laboratory. Parasitology, 71, 153–165. PMID: 1058449.
   PubMed Web of Science ®Google Scholar
• Norton, C.C. & Joyner, L.P. (1978). The appearance of bisporocystic oocysts of Eimeria maxima in drug-treated chicks. Parasitology, 77, 243–248. PMID: 285411.
   PubMed Web of Science ®Google Scholar
• Parker, C.D., Lister, S.A. & Gittins, J. (2021). Impact assessment of the impact of the reduction or removal of ionophores used for controlling coccidiosis in the UK broiler industry. Veterinary Record, 189, e513. PMID: 34101192.
   PubMed Web of Science ®Google Scholar
• Pastor-Fernández, I., Kim, S., Marugan-Hernández, V., Soutter, F., Tomley, F.M. & Blake, D.P. (2020). Vaccination with transgenic Eimeria tenella expressing Eimeria maxima AMA1 and IMP1 confers partial protection against high-level E. maxima challenge in a broiler model of coccidiosis. Parasites & Vectors, 13, 343. PMID: 32650837; PMCID: PMC7350274.
   PubMed Web of Science ®Google Scholar
• Pastor-Fernández, I., Pegg, E., MacDonald, S.E., Tomley, F.M., Blake, D.P. & Marugán-Hernández, V. (2019). Laboratory growth and genetic manipulation of Eimeria tenella. Current Protocols in Microbiology, 53, 1–36. PMID: 30811108.
   Google Scholar
• Price, D.R.G., Küster, T., Øines, Ø, Oliver, E.M., Bartley, K., Nunn, F., Barbero, J.F.L., Pritchard, J., Karp-Tatham, E., Hauge, H., Blake, D.P., Tomley, F.M. & Nisbet, A.J. (2019). Evaluation of vaccine delivery systems for inducing long-lived antibody responses to Dermanyssus gallinae antigen in laying hens. Avian Pathology, 48, S60–S74. PMID: 31032631.
   PubMed Web of Science ®Google Scholar
• Rathinam, T., Gadde, U. & Chapman, H.D. (2016). Attenuation of a drug-sensitive strain of a turkey protozoan parasite Eimeria meleagrimitis by selection for precocious development. Veterinary Parasitology, 216, 1–3. PMID: 26801586.
   PubMed Web of Science ®Google Scholar
• Reid, A.J., Blake, D.P., Ansari, H.R., Billington, K., Browne, H.P., Bryant, J., Dunn, M., Hung, S.S., Kawahara, F., Miranda-Saavedra, D., Malas, T.B., Mourier, T., Naghra, H., Nair, M., Otto, T.D., Rawlings, N.D., Rivailler, P., Sanchez-Flores, A., Sanders, M., Subramaniam, C., Tay, Y.L., Woo, Y., Wu, X., Barrell, B., Dear, P.H., Doerig, C., Gruber, A., Ivens, A.C., Parkinson, J., Rajandream, M.A., Shirley, M.W., Wan, K.L., Berriman, M., Tomley, F.M. & Pain, A. (2014). Genomic analysis of the causative agents of coccidiosis in domestic chickens. Genome Research, 24, 1676–1685. PMID: 25015382; PMCID: PMC4199364.
   PubMed Web of Science ®Google Scholar
• Rollinson, D., Joyner, L.P. & Norton, C.C. (1979). Eimeria maxima: the use of enzyme markers to detect the genetic transfer of drug resistance between lines. Parasitology, 78, 361–367. PMID: 289968.
   PubMed Web of Science ®Google Scholar
• Ryley, J.F. (1980). Drug resistance in coccidia. Advances in Veterinary Science and Comparative Medicine, 24, 99–120. PMID: 7006344.
   PubMedGoogle Scholar
• Sangster, N., Batterham, P., Chapman, H.D., Duraisingh, M., Le Jambre, L., Shirley, M.W., Upcroft, J. & Upcroft, P. (2002). Resistance to antiparasitic drugs: the role of molecular diagnosis. International Journal for Parasitology, 32, 637–653. PMID: 11943235.
   PubMed Web of Science ®Google Scholar
• Schnitzer, R.J. & Grunberg, E. (1957). Drug resistance of microorganisms. New York: Academic Press.
   Google Scholar
• Shirley, M.W. (1980). Eimeria necatrix: the development and characteristics of an egg-adapted (attenuated) line. Parasitology, 81, 525–535. PMID: 7232033.
   PubMed Web of Science ®Google Scholar
• Shirley, M.W. (1989). Development of a live attenuated vaccine against coccidiosis of poultry. Parasite Immunology, 11, 117–124. PMID: 2717196.
   PubMed Web of Science ®Google Scholar
• Shirley, M.W. (1993). Live vaccines for the control of coccidiosis. In J.R. Barta & M.A. Fernando (Eds.), Proceedings of the VI International Coccidiosis Conference (pp. 61–72). Guelph, Ontario, Canada.
   Google Scholar
• Shirley, M.W. (1995). Eimeria species and strains of chicken. In J. Eckert, R. Brown, M.W. Shirley & P. Coudert (Eds.), Guidelines on Techniques in Coccidiosis Research (pp. 1–24). COST 89/820 Biotechnology. Luxembourg: Office for Official Publications of the European Communities.
   Google Scholar
• Shirley, M.W. & Bedrník, P. (1997). Live attenuated vaccines against avian coccidiosis: success with precocious and egg-adapted lines of Eimeria. Parasitology Today, 13, 481–484. PMID: 15275137.
   PubMedGoogle Scholar
• Shirley, M.W. & Bellatti, M.A. (1984). Eimeria necatrix: selection and characteristics of a precocious (and attenuated) line. Avian Pathology, 13, 657–658. PMID: 18766877.
   PubMed Web of Science ®Google Scholar
• Shirley, M.W., Bellatti, M.A. & Millard, B.J. (1982). An egg-adapted (attenuated) line of Eimeria necatrix: further studies on its reproduction, pathogenicity and immunogenicity. Parasitology, 84, 215–226. PMID: 7070840.
   PubMed Web of Science ®Google Scholar
• Shirley, M.W., Blake, D.P., White, S.E., Sheriff, R. & Smith, A.L. (2004). Integrating genetics and genomics to identify new leads for the control of Eimeria spp. Parasitology, 128, S33–S42. PMID: 16454897.
   PubMed Web of Science ®Google Scholar
• Shirley, M.W. & Harvey, D.A. (1996). Eimeria tenella: infection with a single sporocyst gives a clonal population. Parasitology, 112, 523–528. PMID: 8684826.
   PubMed Web of Science ®Google Scholar
• Shirley, M.W. & Harvey, D.A. (2000). A genetic linkage map of the apicomplexan protozoan parasite Eimeria tenella. Genome Research, 10, 1587–1593. PMID: 11042156; PMCID: PMC310971.
   PubMed Web of Science ®Google Scholar
• Shirley, M.W., McDonald, V., Chapman, H.D. & Millard, B.J. (1984). Eimeria praecox: selection and characteristics of precocious lines. Avian Pathology, 13, 669–682. PMID: 18766878.
   PubMed Web of Science ®Google Scholar
• Shirley, M.W., McDonald, V. & Bellatti, M.A. (1986). Eimeria brunetti: selection and characteristics of a precocious (and attenuated) line. Avian Pathology, 15, 705–717. PMID: 18766572.
   PubMed Web of Science ®Google Scholar
• Shirley, M.W. & Millard, B.J. (1976). Some observations on the sexual differentiation of Eimeria tenella using single sporozoite infections in chicken embryos. Parasitology, 73, 337–341. PMID: 1012750.
   PubMed Web of Science ®Google Scholar
• Smith, C.K., II & Galloway, R.B. (1983). Influence of monensin on cation influx and glycolysis of Eimeria tenella sporozoites in vitro. Journal of Parasitology, 69, 666–670. PMID: 6631635.
   PubMed Web of Science ®Google Scholar
• Smith, C.K., II, Galloway, R.B. & White, S.L. (1981). Effect of ionophores on survival, penetration, and development of Eimeria tenella sporozoites in vitro. Journal of Parasitology, 67, 511–516. PMID: 7264837.
   PubMed Web of Science ®Google Scholar
• Smith, C.K., II & Strout, R.G. (1979). Eimeria tenella: accumulation and retention of anticoccidial ionophores by extracellular sporozoites. Experimental Parasitology, 48, 325–330. PMID: 510437.
   PubMed Web of Science ®Google Scholar
• Sutton, C.A., Shirley, M.W. & McDonald, V. (1986). Genetic recombination of markers for precocious development, arprinocid resistance, and isoenzymes of glucose phosphate isomerase. Journal of Parasitology, 72, 965–967. PMID: 3469391.
   PubMed Web of Science ®Google Scholar
• Tang, X., Wang, C., Liang, L., Hu, D., Zhang, S., Duan, C., Suo, J., Liu, X., Suo, X. & Cui, S. (2019). Co-immunization with two recombinant Eimeria tenella lines expressing immunoprotective antigens of E. maxima elicits enhanced protection against E. maxima infection. Parasites & Vectors, 12, 347. PMID: 31300007; PMCID: PMC6626336.
   PubMed Web of Science ®Google Scholar
• Tang, X., Yin, G., Qin, M., Tao, G., Suo, J., Liu, X. & Suo, X. (2016). Transgenic Eimeria tenella as a vaccine vehicle: expressing TgSAG1 elicits protective immunity against Toxoplasma gondii infections in chickens and mice. Scientific Reports, 6, 29379. PMID: 27387302; PMCID: PMC4937369.
   PubMed Web of Science ®Google Scholar
• Waletzky, E., Neal, R. & Hable, I. (1954). A field strain of Eimeria tenella resistant to sulfonamides. Journal of Parasitology, 40, 24.
   Google Scholar
• Wang, C.C. (1975). Studies of the mitochondria from Eimeria tenella and inhibition of the electron transport by quinolone coccidiostats. Biochimica et Biophysica Acta, 396, 210–219. PMID: 1171697.
   PubMed Web of Science ®Google Scholar
• Wang, Z., Shen, J., Suo, X., Zhao, S. & Cao, X. (2006). Experimentally induced monensin-resistant Eimeria tenella and membrane fluidity of sporozoites. Veterinary Parasitology, 138, 186–193. PMID: 16524664.
   PubMed Web of Science ®Google Scholar
• Wang, H., Zhao, Q., Zhu, S., Dong, H., Yu, S., Wang, Q., Yu, Y., Liang, S., Zhao, H., Huang, B. & Han, H. (2021). Molecular characterization and functional analysis of Eimeria tenella citrate synthase. Parasitology Research, 120, 1025–1035. PMID: 33501586.
   PubMed Web of Science ®Google Scholar
• Weppelman, R.M., Battaglia, J.A. & Wang, C.C. (1977). Eimeria tenella: the selection and frequency of drug resistant mutants. Experimental Parasitology, 42, 56–66. PMID: 862710.
   PubMed Web of Science ®Google Scholar
• Williams, R.B. (1998). Epidemiological aspects of the use of live anticoccidial vaccines for chickens. International Journal for Parasitology, 28, 1089–1098. PMID: 9724880.
   PubMed Web of Science ®Google Scholar
• Williams, R.B. (2002). Fifty years of anticoccidial vaccines for poultry (1952–2002). Avian Diseases, 46, 775–802. PMID: 12495038.
   PubMed Web of Science ®Google Scholar
• Williams, R.B. (2006). Tracing the emergence of drug-resistance in coccidia (Eimeria spp.) of commercial broiler flocks medicated with decoquinate for the first time in the United Kingdom. Veterinary Parasitology, 135, 1–14. PMID: 16289564.
   PubMed Web of Science ®Google Scholar
• Williams, R.B., Carlyle, W.W., Bond, D.R. & Brown, I.A. (1999). The efficacy and economic benefits of Paracox, a live attenuated vaccine, in commercial trials with standard broiler chickens in the United Kingdom. International Journal for Parasitology, 29, 341–355. PMID: 10221635.
   PubMed Web of Science ®Google Scholar
• Williams, R.B., Marshall, R.N., Pages, M., Dardi, M. & del Cacho, E. (2009). Pathogenesis of Eimeria praecox in chickens: virulence of field strains compared with laboratory strains of E. praecox and Eimeria acervulina. Avian Pathology, 38, 359–366.
   PubMed Web of Science ®Google Scholar
• Xie, Y., Huang, B., Xu, L., Zhao, Q., Zhu, S., Zhao, H., Dong, H. & Han, H. (2020). Comparative transcriptome analyses of drug-sensitive and drug-resistant strains of Eimeria tenella by RNA-sequencing. Journal of Eukaryote Microbiology, 67, 406–416. PMID: 32027445.
   PubMed Web of Science ®Google Scholar
• Yu, Y., Dong, H., Zhao, Q., Zhu, S., Liang, S., Wang, Q., Wang, H., Yu, S., Huang, B. & Han, H. (2021). Molecular characterization and analysis of the ATPase ASNA1 homolog gene of Eimeria tenella in a drug-sensitive strain and drug resistant strains. International Journal for Parasitology: Drugs and Drug Resistance, 15, 115–125. PMID: 33639573; PMCID: PMC7910411.
   PubMed Web of Science ®Google Scholar
• Yu, Y., Zhao, Q., Zhu, S., Dong, H., Huang, B., Liang, S., Wang, Q., Wang, H., Yu, S. & Han, H. (2020). Molecular characterization of serine/threonine protein phosphatase of Eimeria tenella. Journal of Eukaryotic Microbiology, 67, 510–520. PMID: 32358794.
   PubMed Web of Science ®Google Scholar
• Zhang, S., Tang, X., Wang, S., Shi, F., Duan, C., Bi, F., Suo, J., Hu, D., Liu, J., Wang, C., Suo, X. & Liu, X. (2021). Establishment of recombinant Eimeria acervulina expressing multi-copies M2e derived from avian influenza virus H9N2. Vaccines (Basel), 9, 791. PMID: 34358207; PMCID: PMC8310259.
   PubMed Web of Science ®Google Scholar