Milestones in avian coccidiosis research: A review

Poultry Science

Volumn 93, Issue 3, 2014, Pages 501-511

  Chapman, H D ^a  

^a UNIVERSITY OF ARKANSAS   (United States)

Author keywords

Avian; Eimeria coccidiosis; Poultry

Indexed keywords

ANIMAL; ANIMAL DISEASE; BIRD; BIRD DISEASE; CHICKEN; CLASSIFICATION; COCCIDIOSIS; EIMERIA; EIMERIA COCCIDIOSIS; PARASITOLOGY; PATHOLOGY; PHYSIOLOGY; POULTRY; REVIEW; ULTRASTRUCTURE;

AVIAN; EIMERIA COCCIDIOSIS; POULTRY;

ANIMALS; CHICKENS; COCCIDIOSIS; EIMERIA; POULTRY DISEASES;

EID: 84897577264     PISSN: 00325791     EISSN: 15253171     Source Type: Journal    
DOI: 10.3382/ps.2013-03634     Document Type: Review

References (143)

1. Allen, P. C. 2003. Dietary supplementation with Echinacea and development of immunity to challenge infection with coccidia. Parasitol. Res. 91:74-78.
2. Allen, P. C., H. D. Danforth, and P. C. Augustine. 1998. Dietary modulation of avian coccidiosis. Int. J. Parasitol. 28:1131-1140.
3. Allen, P. C., and R. H. Fetterer. 2002. Effects of dietary vitamin E on chickens infected with Eimeria maxima: Observations over time of primary infection. Avian Dis. 46:839-846.
4. Bafundo, K. W., H. M. Cervantes, and G. F. Mathis. 2008. Sensitivity of Eimeria field isolates in the United States: Responses of nicarbazin-containing anticoccidials. Poult. Sci. 87:1760-1767.
5. Barta, J. R., D. S. Martin, P. A. Liberator, M. Dashkevicz, J. W. Anderson, S. D. Feighner, A. Elbrecht, A. Perkins-Barrow, M. C. Jenkins, H. D. Danforth, M. D. Ruff, and H. Profous-Juchelka. 1997. Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. J. Parasitol. 83:262-271.
6. Becker, E. R. 1934. Coccidia and Coccidiosis of Domesticated, Game and Laboratory Animals and of Man. Collegiate Press, Ames, IA.
7. Belli, S. I., M. G. Wallach, C. Luxford, M. J. Davies, and N. C. Smith. 2003. Roles of tyrosine-rich precursor glycoproteins and dityrosine- and 3,4-dihydroxyphenylalanine-mediated protein cross-linking in development of the oocyst wall in the coccidian parasite Eimeria maxima. Eukaryot. Cell 2:456-464.
8. Blake, D. P., H. Alias, K. J. Billington, E. L. Clark, M. N. Mat-Isa, A. F. Mohamad, M. R. Mohd-Amin, Y. L. Tay, A. L. Smith, F. M. Tomley, and K. L. Wan. 2012. EmaxDB: Availability of a first draft genome sequence for the apicomplexan Eimeria maxima. Mol. Biochem. Parasitol. 184:48-51.
9. Blake, D. P., K. J. Billington, S. L. Copestake, R. D. Oakes, M. A. Quail, K. L. Wan, M. W. Shirley, and A. L. Smith. 2011a. Genetic mapping identifies novel highly protective antigens for an apicomplexan parasite. PLoS Pathog. 7:e1001279.
10. Blake, D. P., R. Oakes, and A. L. Smith. 2011b. A genetic linkage map for the apicomplexan protozoan parasite Eimeria maxima and comparison with Eimeria tenella. Int. J. Parasitol. 41:263-270.
11. Brackett, S, ed. 1949. Coccidiosis. Ann. New York Acad. Sci. 52:429-624. New York, NY.
12. Bushkin, G. G., E. Motari, A. Carpentieri, J. P. Dubey, C. E. Costello, P. W. Robbins, and J. Samuelson. 2013. Evidence for a structural role for acid-fast lipids in oocyst walls of Cryptosporidium, Toxoplasma, and Eimeria. MBio 4:e00387-13. http://dx.doi.org/10.1128/mBio.00387-13.
13. Bushkin, G. G., E. Motari, P. Magnelli, M. J. Gubbels, J. P. Dubey, K. B. Miska, E. Bullitt, C. E. Costello, P. W. Robbins, and J. Samuelson. 2012. β-1,3-glucan, which can be targeted by drugs, forms a trabecular scaffold in the oocyst walls of Toxoplasma and Eimeria. MBio 3:e00258-12. http://dx.doi.org/10.1128/mBio.00258-12.
14. Cai, X., A. L. Fuller, L. R. McDougald, and G. Zhu. 2003. Apicoplast genome of the coccidian Eimeria tenella. Gene 321:39-46.
15. Canning, E. U., and M. Anwar. 1968. Studies on meiotic division in coccidial and malarial parasites. J. Protozool. 15:290-298.
16. Canning, E. U., and K. Morgan. 1975. DNA synthesis, reduction and elimination during life cycles of the Eimeriine coccidian, Eimeria tenella and the Haemogregarine, Hepatozoon domerguei. Exp. Parasitol. 38:217-227.
17. Castañón, C. A. B., J. S. Fraga, S. Fernandez, A. Gruber, and L. F. Costa. 2007. Biological shape characterization for automatic image recognition and diagnosis of protozoan parasites of the genus Eimeria. Pattern Recognit. 40:1899-1910.
18. Chapman, H. D. 1994a. A review of the biological activity of the anticoccidial drug nicarbazin and its application for the control of coccidiosis in poultry. Poult. Sci. Rev. 5:231-243.
19. Chapman, H. D. 1994b. Sensitivity of field isolates of Eimeria to monensin following the use of a coccidiosis vaccine in broiler chickens. Poult. Sci. 73:476-478.
20. Chapman, H. D. 1997. Biochemical, genetic and applied aspects of drug resistance in Eimeria parasites of the fowl. Avian Pathol. 26:221-244.
21. Chapman, H. D. 2000. Practical use of vaccines for the control of coccidiosis in the chicken. World's Poult. Sci. J. 56:7-20.
22. Chapman, H. D. 2001. Use of anticoccidial drugs in broiler chickens in the USA: Analysis for the years 1995 to 1999. Poult. Sci. 80:572-580.
23. Chapman, H. D. 2003. Origins of coccidiosis research in the fowl - The first fifty years. Avian Dis. 47:1-20.
24. Chapman, H. D. 2004. Walter T. Johnson (1892 to 1937): Pioneer of coccidiosis research in the fowl. Avian Pathol. 33:107-116.
25. Chapman, H. D., J. R. Barta, D. P. Blake, A. Gruber, M. Jenkins, N. C. Smith, X. Suo, and F. M. Tomley. 2013. A selective review of advances in coccidiosis research. Adv. Parasitol. 83:93-171.
26. Chapman, H. D., D. L. Fernandes, and T. F. Davison. 1982. A comparison of the effects of infection with Eimeria maxima and dietary restriction on weight gain, plasma metabolites and liver glycogen in the immature fowl, Gallus domesticus. Parasitology 84:205-213.
27. Chapman, H. D., and M. E. Rose. 1986. Cloning of Eimeria tenella in the chicken. J. Parasitol. 72:605-606.
28. Clark, J. D., K. Billington, J. M. Bumstead, R. D. Oakes, P. E. Soon, P. Sopp, F. M. Tomley, and D. P. Blake. 2008. A toolbox facilitating stable transfection of Eimeria species. Mol. Biochem. Parasitol. 162:77-86.
29. Colley, F. C. 1967. Fine structure of sporozoites of Eimeria nieschulzi. J. Protozool. 14:217-220.
30. Colley, F. C. 1968. Fine structure of schizonts and merozoites of Eimeria nieschulzi. J. Protozool. 15:374-382.
31. Cowper, B., S. Matthews, and F. M. Tomley. 2012. The molecular basis for the distinct host and tissue tropisms of coccidian parasites. Mol. Biochem. Parasitol. 186:1-10.
32. Cuckler, A. C., and C. M. Malanga. 1955. Studies on drug resistance in coccidia. J. Parasitol. 41:302-311.
33. Cuckler, A. C., C. M. Malanga, A. J. Basso, and R. C. O'Neill. 1955. Antiparasitic activity of substituted carbanilide complexes. Science 122:244-245.
34. Davies, S. F. M., L. P. Joyner, and S. B. Kendall. 1963. Coccidiosis. Oliver and Boyd, Edinburgh and London, UK.
35. Davis, P. J., M. E. J. Barratt, M. Morgan, and S. H. Parry. 1986. Immune response of chickens to oral immunization by "trickle" infections with Eimeria. Pages 618-633 in Research in avian coccidiosis. L. R. McDougald, L. P. Joyner, and P. L. Long, ed. Proc. Georgia Coccidiosis Conference, University of Georgia, Athens.
36. Davison, T. F., H. D. Chapman, and S. Harvey. 1985. Endocrine changes in the fowl during infection with Eimeria maxima. Res. Vet. Sci. 38:296-300.
37. de Venevelles, P., J. Chich, W. Faigle, B. Lombard, D. Loew, P. Péry, and M. Labbé 2006. Study of proteins associated with the Eimeria tenella refractile body by a proteomic approach. Int. J. Parasitol. 36:1399-1407.
38. Dubremetz, J. F., and G. Torpier. 1978. Freeze fracture study of the pellicle of an eimerian sporozoite (Protozoa, Coccidia). J. Ultrastruct. Res. 62:94-109.
39. Edgar, S. A. 1956. You can now inoculate against coccidiosis. Highlights of Agricultural Research, Agriculture Experiment Station, Alabama Polytechnic Institute, Vol. 3. No. 1.
40. Fantham, H. B. 1910. The morphology and life-history of Eimeria (coccidium) avium: A sporozoön causing a fatal disease among young grouse. Proc. Zool. Soc. Lond. 3:672-691.
41. Ferguson, D. J. P., S. I. Belli, N. C. Smith, and M. G. Wallach. 2003. The development of the macrogamete and oocyst wall in Eimeria maxima: Immuno-light and electron microscopy. Int. J. Parasitol. 33:1329-1340.
42. Ferguson, D. J. P., A. Birch-Andersen, W. M. Hutchison, and J. C. Siim. 1976. Ultrastructural studies on the endogenous development of Eimeria brunetti: 1. Schizogony. Acta Pathol. Microbiol. Scand. 84B:401-413.
43. Ferguson, D. J. P., A. Birch-Andersen, W. M. Hutchison, and J. C. Siim. 1977. Ultrastructural studies on the endogenous development of Eimeria brunetti. II. Microgametogony and the microgamete. Acta Pathol. Microbiol. Scand. 85B:67-77.
44. Ferguson, D. J. P., S. A. Campbell, F. L. Henriquez, L. Phan, E. Mui, T. A. Richards, S. P. Muench, M. Allary, J. Z. Lu, S. T. Prigge, F. M. Tomley, M. W. Shirley, D. Rice, R. McLeod, and C. W. Roberts. 2007. Enzymes of type II fatty acid synthesis and apicoplast differentiation and division in Eimeria tenella. Int. J. Parasitol. 37:33-51.
45. Fernandez, S., A. C. Costa, A. M. Katsuyama, A. Madeira, and A. Gruber. 2003. A survey of the inter- and intraspecific RAPD markers of Eimeria spp. of the domestic fowl and the development of reliable diagnostic tools. Parasitol. Res. 89:437-445.
46. Fernando, M. A., M. E. Rose, and B. J. Millard. 1987. Eimeria spp. of domestic fowl: the migration of sporozoites intra- and extraenterically. J. Parasitol. 73:561-567.
47. Fry, M., and R. B. Williams. 1984. Effects of decoquinate and clopidol on electron transport in mitochondria of Eimeria tenella (Apicomplexa: Coccidia). Biochem. Pharmacol. 33:229-240.
48. Gadde, U., T. Rathinam, G. F. Erf, and H. D. Chapman. 2013. Acquisition of immunity to the protozoan parasite Eimeria adenoeides in turkey poults and cellular responses to infection. Poult. Sci. 92:3149-3157.
49. Grumbles, L. C., J. P. Delaplane, and T. C. Higgins. 1948. Continuous feeding of low concentrations of sulfaquinoxaline for the control of coccidiosis in poultry. Poult. Sci. 27:605-608.
50. Hammond, D., and P. L. Long. 1973. The Coccidia. University Park Press, Baltimore, MD.
51. Hong, Y. H., H. S. Lillehoj, S. H. Lee, R. A. Dalloul, and E. P. Lillehoj. 2006. Analysis of chicken cytokine and chemokine gene expression following Eimeria acervulina and Eimeria tenella infections. Vet. Immunol. Immunopathol. 114:209-223.
52. James, S. 1980. Thiamine uptake in isolated schizonts of Eimeria tenella and the inhibitory effects of amprolium. Parasitology 80:313-322.
53. Jeffers, T. K. 1974. Genetic transfer of anticoccidial resistance in Eimeria tenella. J. Parasitol. 60:900-904.
54. Jeffers, T. K. 1975. Attenuation of Eimeria tenella through selection for precociousness. J. Parasitol. 61:1083-1090.
55. Jeffers, T. K. 1978. Genetics of coccidia and the host response. Pages 5-125 in Avian Coccidiosis. P. L. Long, K. N. Boorman, and B. M. Freeman, ed. British Poultry Science Ltd., Edinburgh, UK.
56. Jeffers, T. K. 1986. Attenuation of coccidia - A review. Pages 482-501 in Research in Avian Coccidiosis. L. R. McDougald, L. P. Joyner, and P. L. Long, ed. Proc. Georgia Coccidiosis Conference, University of Georgia, Athens, GA.
57. Jenkins, M. C. 1988. A cDNA encoding a merozoite surface protein of the protozoan Eimeria acervulina contains tandem-repeated sequences. Nucleic Acids Res. 16:9863.
58. Jenkins, M. C., C. Parker, S. Klopp, C. O'Brien, K. Miska, and R. Fetterer. 2012. Gel-bead delivery of Eimeria oocysts protects chickens against coccidiosis. Avian Dis. 56:306-309.
59. Johnson, J., and W. M. Reid. 1970. Anticoccidial drugs: Lesion scoring techniques in battery and floor-pen experiments with chickens. Exp. Parasitol. 28:30-36.
60. Johnson, W. T. 1923. Avian coccidiosis. Poult. Sci. 2:146-163.
61. Johnson, W. T. 1923/1924. Eimeria avium and the diagnosis of avian coccidiosis. Poult. Sci. 3:41-57.
62. Johnson, W. T. 1927. Immunity or resistance of the chicken to coccidial infection. Pages 5-31 in Station Bulletin 230, Oregon Agricultural College Experiment Station, Corvallis, OR.
63. Joyner, L. P. 1969. Immunological variation between two strains of Eimeria acervulina. Parasitology 59:725-732.
64. Joyner, L. P. 1978. The identification and diagnosis of avian coccidiosis. Pages 29-49 in Avian Coccidiosis. Proc. 13th Poult. Sci. Symposium. P. L. Long, K. N. Boorman, and B. M. Freeman, ed. British Poultry Science Ltd., Edinburgh, UK.
65. Joyner, L. P., and C. C. Norton. 1973. The immunity arising from continuous low-level infection with Eimeria tenella. Parasitology 67:333-340.
66. Joyner, L. P., and C. C. Norton. 1978. The activity of methyl benzoquate and clopidol against Eimeria maxima: Synergy and drug resistance. Parasitology 76:369-377.
67. Kelleher, M., and F. M. Tomley. 1998. Transient expression of betagalactosidase in differentiating sporozoites of Eimeria tenella. Mol. Biochem. Parasitol. 97:21-31.
68. Kouwenhoven, B., and C. J. G. van der Horst. 1969. Strongly acid intestinal content and lowered protein, carotene and vitamin A blood levels in E. acervulina infected chickens. Ztschr. Parasitkde. 32:347-353.
69. Lal, K., E. Bromley, R. Oakes, J. H. Prieto, S. J. Sanderson, D. Kurian, L. Hunt, J. R. Yates, J. M. Wastling, R. E. Sinden, and F. M. Tomley. 2009. Proteomic comparison of four Eimeria tenella life-cycle stages: Unsporulated oocyst, sporulated oocyst, sporozoite and second-generation merozoite. Proteomics 9:4566-4576.
70. Lee, S., and M. A. Fernando. 2000. Viral double-stranded RNAs of Eimeria spp. of the domestic fowl: Analysis of genetic relatedness and divergence among various strains. Parasitol. Res. 86:733-737.
71. Lee, S. H., H. S. Lillehoj, S. I. Jang, K. W. Lee, D. Bravo, and E. P. Lillehoj. 2011. Effects of dietary supplementation with phytonutrients on vaccine-stimulated immunity against infection with Eimeria tenella. Vet. Parasitol. 181:97-105.
72. Levine, N. D., J. O. Corliss, F. E. G. Cox, G. Deroux, J. Grain, B. M. Honigberg, G. F. Leedale, A. R. Loeblich, J. Lom, D. Lynn, E. G. Merinfeld, F. C. Page, G. Poljansky, V. Sprague, J. Vavra, and F. G. Wallace. 1980. A newly revised classification of the protozoa. J. Protozool. 27:37-58.
73. Levine, P. P. 1939. The effect of sulfanilamide on the course of experimental avian coccidiosis. Cornell Vet. 29:309-320.
74. Levine, P. P. 1942. A new coccidium pathogenic for chickens, Eimeria brunetti n. species (Protozoa: Eimeriidae). Cornell Vet. 32:430-439.
75. Lim, L. S., Y. L. Tay, H. Alias, K. L. Wan, and P. H. Dear. 2012. Insights into the genome structure and copy-number variation of Eimeria tenella. BMC Genomics 13:389.
76. Lin, R. Q., L. L. Qiu, G. H. Liu, X. Y. Wu, Y. B. Weng, W. Q. Xie, J. Hou, H. Pan, Z. G. Yuan, F. C. Zou, M. Hu, and X. Q. Zhu. 2011. Characterization of the complete mitochondrial genomes of five Eimeria species from domestic chickens. Gene 480:28-33.
77. Long, P. L. 1982. The Biology of the Coccidia. University Park Press, Baltimore, MD, USA.
78. Long, P. L., K. N. Boorman, and B. M. Freeman. 1978. Avian Coccidiosis. Proc. 13th Poultry Science Symposium. British Poultry Science Ltd., Edinburgh, UK.
79. Long, P. L., J. Johnson, M. E. McKenzie, E. Perry, M. S. Crane, and P. K. Murray. 1986. Immunization of young broiler chickens with low level infections of Eimeria tenella, E. acervulina or E. maxima. Avian Pathol. 15:271-278.
80. Long, P. L., L. P. Joyner, B. J. Millard, and C. C. Norton. 1976. A guide to the laboratory techniques used in the study and diagnosis of avian coccidiosis. Folia Vet. Lat. 6:201-217.
81. MacPherson, J. M., and A. A. Gajadhar. 1993. Differentiation of seven Eimeria species by random amplified polymorphic DNA. Vet. Parasitol. 45:257-266.
82. Mathis, G. F., and C. Broussard. 2006. Increased level of Eimeria sensitivity to diclazuril after using a live coccidial vaccine. Avian Dis. 50:321-324.
83. Matsubayashi, M., T. Hatta, T. Miyoshi, Anisuzzaman, K. Sasai, K. Shimura, T. Isobe, K. Kita, and N. Tsuji. 2013. High-throughput RNA sequencing profiles and transcriptional evidence of aerobic respiratory enzymes in sporulating oocysts and sporozoites of Eimeria tenella. Infect. Gen. Evol. 18:269-276. http://dx.doi.org/10.1016/j.meegid.2013.06.002.
84. McDougald, L. R. 1982. Chemotherapy of coccidiosis. Pages 373-427 in The Biology of the Coccidia. P. L. Long, ed. University Park Press, Baltimore, MD.
85. McDougald, L. R., and T. K. Jeffers. 1976. Eimeria tenella (Sporozoa, Coccidia): Gametogony following a single asexual generation. Science 192:258-259.
86. McDougald, L. R., L. P. Joyner, and P. L. Long. 1986. Research in avian coccidiosis. Proc. Georgia Coccidiosis Conference, University of Georgia, Athens.
87. McDougald, L. R., and W. M. Reid. 1991. Coccidiosis. Pages 780- 797 in Diseases of Poultry. B. W. Calnek, ed. 9th ed. Iowa State University Press, Ames.
88. McLaren, D. J., and G. E. Paget. 1968. A fine structural study on the merozoite of Eimeria tenella with special reference to the conoid apparatus. Parasitology 58:561-571.
89. Miska, K. B., R. S. Schwarz, M. C. Jenkins, T. Rathinam, and H. D. Chapman. 2010. Molecular characterization and phylogenetic analysis of Eimeria from turkeys and gamebirds: Implications for evolutionary relationships in galliform birds. J. Parasitol. 96:982-986.
90. Norton, C. C., and H. E. Hein. 1976. Eimeria maxima: A comparison of two laboratory strains with a fresh isolate. Parasitology 72:345-354.
91. Pellérdy, L. P. 1974. Coccidia and coccidiosis. 2nd ed. Akad. Kiado, Budapest; Paul Parey, Berlin and Hamburg, Germany.
92. Preston-Mafham, R. A., and A. H. Sykes. 1967. Changes in the permeability of the mucosa during intestinal coccidiosis infections in the fowl. Experientia 23:972-973.
93. Railliet, A. 1913. Quel nom doit-on donner üdla coccidie intestinale de la poule? Arch. Parasitol. 16:147-148.
94. Railliet, A., and A. Lucet. 1891a. Développement expérimental des coccidies de l'épithélium intestinal du lapin et de la poule. C. R. Soc. Biol., Paris, 36:820-823.
95. Raillet, A., and A. Lucet. 1891b. Note sur quelques espèces de coccidies encore peu étudiées. Bull. Soc. Zool., France, 16:246-250.
96. Reid, W. M. 1970. Proceedings of the symposium on methodology for the development, selection, and testing of anticoccidial drugs for use in controlling coccidiosis. Exp. Parasitol. 28:1-3.
97. Roberts, S. J., A. L. Smith, A. B. West, L. Wen, R. C. Findly, M. J. Owen, and A. C. Hayday. 1996. T-cell alpha beta + and gamma delta + deficient mice display abnormal but distinct phenotypes toward a natural, widespread infection of the intestinal epithelium. Proc. Natl. Acad. Sci. USA 93:11774-11779.
98. Rose, M. E. 1996. Immunity to coccidia. Pages 265-299 in Poultry Immunology. Vol. 24. Poultry Science Symposium Series. T. F. Davison, T. R. Morris, and L. N. Payne, ed. Carfax Publishing Company, Abingdon, UK.
99. Rose, M. E., and P. Hesketh. 1979. Immunity to coccidiosis: Tlymphocyte- or B-lymphocyte-deficient animals. Infect. Immun. 26:630-637.
100. Rose, M. E., P. Hesketh, and D. Wakelin. 1992. Immune control of murine coccidiosis: CD4+ and CD8+ T lymphocytes contribute differentially in resistance to primary and secondary infections. Parasitology 105:349-354.
101. Rose, M. E., and P. L. Long. 1962. Immunity to four species of Eimeria in fowls. Immunology 5:79-92.
102. Rose, M. E., B. M. Ogilvie, P. Hesketh, and M. F. Festing. 1979. Failure of nude (athymic) rats to become resistant to reinfection with the intestinal coccidian parasite Eimeria nieschulzi or the nematode Nippostronglus brasiliensis. Parasite Immunol. 1:125-132.
103. Rose, M. E., D. Wakelin, and P. Hesketh. 1991. Interferon-gammamediated effects upon immunity to coccidial infections in the mouse. Parasite Immunol. 13:63-74.
104. Rothwell, L. R., A. Graminski, M. E. Rose, and P. Kaiser. 1995. Avian coccidiosis: Changes in intestinal lymphocyte populations associated with the development of immunity to Eimeria maxima. Parasite Immunol. 17:525-533.
105. Ruff, M. D. 1974. Reduced transport of methionine in intestines of chickens infected with Eimeria necatrix. J. Parasitol. 60:838-843.
106. Russell, D. G. 1983. Host cell invasion by Apicomplexa: An expression of the parasite's contractile system? Parasitology 87:199-209.
107. Ryley, J. F. 1969. Ultrastructural studies on the sporozoite of Eimeria tenella. Parasitology 59:67-72.
108. Ryley, J. F., M. Bentley, D. J. Manners, and J. R. Stark. 1969. Amylopectin, the storage polysaccharide of the coccidia Eimeria brunetti and E. tenella. J. Parasitol. 55:839-845.
109. Schildt, C. W., and C. A. Herrick. 1955. The effect of cecal coccidiosis on the motility of the digestive tract of the domestic fowl. J. Parasitol. 41:18-23.
110. Schmatz, D. M., W. F. Baginsky, and M. J. Turner. 1989. Evidence for and characterization of a mannitol cycle in Eimeria tenella. Mol. Biochem. Parasitol. 32:263-270.
111. Schnitzler, B. E., P. L. Thebo, J. G. Mattsson, F. M. Tomley, and M. W. Shirley. 1998. Development of a diagnostic PCR assay for the detection and discrimination of four pathogenic Eimeria species of the chicken. Avian Pathol. 27:490-497.
112. Scholtyseck, E., and H. Mehlhorn. 1970. Ultrastructural study of characteristic organelles (paired organelles, micronemes, micropores) of Sporozoa and related organisms. Z. Parasitenkd. 34:97-127.
113. Shirley, M. W. 1989. Development of a live attenuated vaccine against coccidiosis of poultry. Parasite Immunol. 11:117-124.
114. Shirley, M. W. 1994. The genome of Eimeria tenella: Further studies on its molecular organisation. Parasitol. Res. 80:366-373.
115. Shirley, M. W. 2000. The genome of Eimeria spp., with special reference to Eimeria tenella - A coccidium from the chicken. Int. J. Parasitol. 30:485-493.
116. Shirley, M. W., and D. Harvey. 2000. A genetic linkage map of the apicomplexan protozoan parasite Eimeria tenella. Genome Res. 10:1587-1593.
117. Shirley, M. W., and B. J. Millard. 1976. Some observations on the sexual differentiation of Eimeria tenella using single sporozoite infections in chicken embryos. Parasitology 73:337-341.
118. Shumard, R. F., and M. E. Callender. 1967. Monensin, a new biologically active compound. VI. Anticoccidial activity. Antimicrob. Agents Chemother. 7:369-377.
119. Smith, C. K. II, and R. B. Galloway. 1983. Influence of monensin on cation influx and glycolysis of Eimeria tenella sporozoites in vitro. J. Parasitol. 69:666-670.
120. Soares Medeiros, L. C., F. Gomes, L. R. Maciel, S. H. Seabra, R. Docampo, S. Moreno, H. Plattner, J. Hentschel, U. Kawazoe, H. Barrabin, W. de Souza, R. A. Damatta, and K. Miranda. 2011. Volutin granules of Eimeria parasites are acidic compartments and have physiological and structural characteristics similar to acidocalcisomes. J. Eukaryot. Microbiol. 58:416-423.
121. Southern, L. L., and D. H. Baker. 1983. Eimeria acervulina infection and the zinc-copper interrelationship in the chick. Poult. Sci. 62:401-404.
122. Stephens, J. F. 1965. Some physiological effects of coccidiosis caused by Eimeria necatrix in the chicken. J. Parasitol. 51:331-335.
123. Stotish, R. L., and C. C. Wang. 1977. Characterization of the oocyst wall of Eimeria tenella. Fed. Proc. Fed. Am. Soc. Exp. Biol. 36:3482.
124. Stucki, U., R. Braun, and I. Roditi. 1993. Eimeria tenella: Characterization of a 5S ribosomal RNA repeat unit and its use as a species-specific probe. Exp. Parasitol. 76:68-75.
125. Su, H., X. Liu, W. Yan, T. Shi, X. Zhao, D. P. Blake, F. M. Tomley, and X. Suo. 2012. PiggyBac transposon-mediated transgenesis in the apicomplexan parasite Eimeria tenella. PLoS ONE 7:e40075.
126. Swayne, D. E., J. R. Glisson, L. R. McDougald, L. K. Nolan, D. L. Suarez, and V. L. Nair. 2013. Diseases of Poultry. 13th ed. Wiley-Blackwell, Somerset, NJ.
127. Tomley, F. M., K. J. Billington, J. M. Bumstead, J. D. Clark, and P. Monaghan. 2001. EtMIC4: A microneme protein from Eimeria tenella that contains tandem arrays of epidermal growth factorlike repeats and thrombospondin type-1 repeats. Int. J. Parasitol. 31:1303-1310.
128. Tomley, F. M., L. E. Clarke, U. Kawazoe, R. Dijkema, and J. J. Kok. 1991. Sequence of the gene encoding an immunodominant microneme protein of Eimeria tenella. Mol. Biochem. Parasitol. 49:277-288.
129. Turk, D. E. 1978. The effects of coccidiosis on intestinal function and gut microflora. Pages 227-267 in Avian Coccidiosis. Proc. 13th Poultry Science Symposium. P. L. Long, K. N. Boorman, and B. M. Freeman, ed. British Poultry Science Ltd., Edinburgh, UK.
130. Turk, D. E., and J. F. Stephens. 1967. Upper intestinal tract infection produced by E. acervulina and absorption of 65Zn and 131Ilabelled oleic acid. J. Nutr. 93:161-165.
131. Tyzzer, E. E. 1929. Coccidiosis in gallinaceous birds. Am. J. Hyg. 10:269-383.
132. Tyzzer, E. E., H. Theiler, and E. E. Jones. 1932. Coccidiosis in gallinaceous birds II. A comparative study of species of Eimeria of the chicken. Am. J. Hyg. 15:319-393.
133. Wallach, M. G., A. Halabi, G. Pillemer, O. Sar-Shalom, D. Mencher, M. Gilad, U. Bendheim, and H. D. Danforth. 1992. Maternal immunization with gametocyte antigens as a means of providing protective immunity against Eimeria maxima in chickens. Infect. Immun. 60:2036-2039.
134. Wallach, M. G., D. Mencher, S. Yarus, G. Pillmemer, A. Halabi, and T. Pugatsch. 1989. Eimeria maxima: identification of gametocyte protein antigens. Exp. Parasitol. 68:49-56.
135. Wang, C. C. 1975. Studies of the mitochondria from Eimeria tenella and inhibition of the electron transport by quinolone coccidiostats. Biochim. Biophys. Acta 396:210-219.
136. Wang, C. C. 1976a. Some prokaryotic characteristics of ribosomes from Eimeria tenella. Fed. Proc. Fed. Am. Soc. Exp. Biol. 33:1424.
137. Wang, C. C. 1976b. Inhibition of the respiration of Eimeria tenella by quinolone coccidiostats. Biochem. Pharmacol. 25:343-349.
138. Wang, C. C. 1978. Biochemical and nutritional aspects of coccidia. Pages 135-184 in Avian Coccidiosis. Proc. 13th Poultry Science Symposium. P. L. Long, K. N. Boorman, and B. M. Freeman, ed. British Poultry Science Ltd., Edinburgh, UK.
139. Weppelman, R. M., W. J. A. Van Den Heuvel, and C. C. Wang. 1976. Mass spectrometric analysis of the fatty acids and nonsaponifiable lipids of Eimeria tenella oocysts. Lipids 11:209-215.
140. Williams, R. B. 2002. Fifty years of anticoccidial vaccines for poultry (1952-2002). Avian Dis. 46:775-802.
141. Wils-Plotz, E. L., M. C. Jenkins, and R. N. Dilger. 2013. Modulation of the intestinal environment, innate immune response, and barrier function by dietary threonine and purified fiber during a coccidiosis challenge in broiler chicks. Poult. Sci. 92:735-745.
142. Yvore, P. 1989. Coccidia and intestinal coccidiomorphs. Proc. Vth Int. Coccidiosis Conf., INRA Publications, Paris, France.
143. Zhou, Z., Z. Wang, L. Cao, S. Hu, Z. Zhang, B. Qin, Z. Guo, and K. Nie. 2013. Upregulation of chicken TLR4, TLR15 and MyD88 in heterophils and monocyte-derived macrophages stimulated with Eimeria tenella in vitro. Exp. Parasitol. 133:427-433.