The european rabbit (Oryctolagus cuniculus), a source of zoonotic cryptosporidiosis

Zoonoses and Public Health

Volumn 57, Issue 7-8, 2010, Pages

  Robinson, G ^a   Chalmers, R M ^a  

^a SINGLETON HOSPITAL   (United Kingdom)

Author keywords

Cryptosporidium; Lagomorphs; Oryctolagus cuniculus; Rabbits

Indexed keywords

WATER;

ANIMAL EXPERIMENT; ANIMAL MODEL; COCCIDIA; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM PARVUM; EPIDEMIC; FECES ANALYSIS; GENE IDENTIFICATION; GENE LOCUS; GENOTYPE; HEALTH BEHAVIOR; HOST PARASITE INTERACTION; HYGIENE; INFORMATION; INTESTINE INFECTION; LAGOMORPH; MICROBIAL CONTAMINATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PET ANIMAL; PRIORITY JOURNAL; RABBIT; REVIEW; SPECIES IDENTIFICATION; UNINDEXED SEQUENCE; WILDLIFE; ZOONOSIS;

ANIMALS; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM; EUROPE; GENOTYPE; HUMANS; PHYLOGENY; RABBITS; ZOONOSES;

CRYPTOSPORIDIUM; CRYPTOSPORIDIUM PARVUM; CRYPTOSPORIDIUM SP.; LAGOMORPHA; MAMMALIA; ORYCTOLAGUS CUNICULUS;

EID: 77957755227     PISSN: 18631959     EISSN: 18632378     Source Type: Journal    
DOI: 10.1111/j.1863-2378.2009.01308.x     Document Type: Review

References (67)

1. Anon., 2008a: Outbreak of cryptosporidiosis associated with a water contamination incident in the East Midlands. Health Prot. Rep. 2, 3-5. Available at .
2. Anon., 2008b: Avoiding ill health at open farms - advice to farmers (with teachers' supplement). Health and Safety Executive Agriculture Information Sheet No 23. Available at: .
3. Araya, J., J. Gonzalez, H. Sagua, W. Olivares, C. Rimassa, and M. Videla, 1987: Cryptosporidiosis in northern Chile. I. Prevalence in domestic, synanthropic and wild animals. Bol. Chil. Parasitol. 42, 7-11.
4. Atwill, E. R., B. Hoar, P. M. Das Gracas Cabral, K. W. Tate, F. Rulofson, and G. Nader, 2003: Improved quantitative estimates of low environmental loading and sporadic periparturient shedding of Cryptosporidium parvum in adult beef cattle. Appl. Environ. Microbiol. 69, 4604-4610.
5. Aydin, Y., and I. A. Ozkul, 1996: Infectivity of Cryptosporidium muris directly isolated from the murine stomach for various laboratory animals. Vet. Parasitol. 66, 257-262.
6. Bailey, J. R., L. Warner, G. C. Pritchard, S. Williamson, T. Carson, G. Willshaw, T. Cheasty, and J. R. Bailey, 2002: Wild rabbits - a novel vector for Vero cytotoxigenic Escherichia coli (VTEC) O157. Commun. Dis. Public Health 5, 74-75.
7. Bern, C., Y. Ortega, W. Checkley, J. M. Roberts, A. G. Lescano, L. Cabrera, M. Verastegui, R. E. Black, C. Sterling, and R. H. Gilman, 2002: Epidemiologic differences between cyclosporiasis and cryptosporidiosis in Peruvian children. Emerg. Infect. Dis. 8, 581-585.
8. Chalmers, R. M., 1996: The distribution of Cryptosporidium in livestock and wild animal populations on a Warwickshire farm. PhD thesis, Coventry University, Coventry.
9. Chalmers, R. M., and K. G. J. Pollock, 2008: Cryptosporidium in Scotland 2007: reference laboratory data. HPS Wkly Rep. 42, 385-387.
10. Chalmers, R. M., A. P. Sturdee, S. A. Bull, and A. Miller, 1995: Rodent reservoirs of Cryptosporidium. In: Betts, W. B., D. Casemore, C. Fricker, H. Smith, and J. Watkins (eds), Protozoan Parasites and Water, pp. 63-66. Royal Society of Chemistry, Cambridge.
11. Chalmers, R. M., K. Elwin, A. L. Thomas, E. C. Guy, and B. Mason, 2009a: Long-term Cryptosporidium typing reveals the aetiology and species-specific epidemiology of human cryptosporidiosis in England and Wales, 2000 to 2003. Euro Surveill. 14, 6-14.
12. Chalmers, R. M., G. Robinson, K. Elwin, S. J. Hadfield, L. Xiao, U. Ryan, D. Modha, and C. Mallaghan, 2009b: Cryptosporidium rabbit genotype, a newly identified human pathogen. Emerg. Infect. Dis. 15, 829-830.
13. Cox, P., M. Griffith, M. Angles, D. Deere, and C. Ferguson, 2005: Concentrations of pathogens and indicators in animal feces in the Sydney watershed. Appl. Environ. Microbiol. 71, 5929-5934.
14. Darabus, G., and R. Olariu, 2003: The homologous and interspecies transmission of Cryptosporidium parvum and Cryptosporidium meleagridis. Pol. J. Vet. Sci. 6, 225-228.
15. Davies, C. M., C. Kaucner, D. Deere, and N. J. Ashbolt, 2003: Recovery and enumeration of Cryptosporidium parvum from animal fecal matrices. Appl. Environ. Microbiol. 69, 2842-2847.
16. Deng, M. Q., D. O. Cliver, and T. W. Mariam, 1997: Immunomagnetic capture PCR to detect viable Cryptosporidium parvum oocysts from environmental samples. Appl. Environ. Microbiol. 63, 3134-3138.
17. Deng, M. Q., K. M. Lam, and D. O. Cliver, 2000: Immunomagnetic separation of Cryptosporidium parvum oocysts using MACS MicroBeads and high gradient separation columns. J. Microbiol. Methods 40, 11-17.
18. Epe, C., N. Coati, and T. Schnieder, 2004: Results of parasitological examinations of faecal samples from horses, ruminants, pigs, dogs, cats, hedgehogs and rabbits between 1998 and 2002. Dtsch. Tierarztl. Wochenschr. 111, 243-247.
19. Fayer, R., 2007: General Biology. In: Fayer, R., and L. Xiao (eds.), Cryptosporidium and Cryptosporidiosis, 2nd edn, pp. 1-42. CRC Press, Boca Raton, FL.
20. Fayer, R., M. Santin, and J. M. Trout, 2007: Prevalence of Cryptosporidium species and genotypes in mature dairy cattle on farms in eastern United States compared with younger cattle from the same locations. Vet. Parasitol. 145, 260-266.
21. Feng, Y., K. A. Alderisio, W. Yang, L. A. Blancero, W. G. Kuhne, C. A. Nadareski, M. Reid, and L. Xiao, 2007: Cryptosporidium genotypes in wildlife from a New York watershed. Appl. Environ. Microbiol. 73, 6475-6483.
22. Ferguson, C., 2005: Deterministic model of microbial sources, fate and transport: a quantitative tool for pathogen catchment budgeting. PhD thesis, The University of New South Wales, Sydney.
23. Heine, J., and J. Boch, 1981: Cryptosporidium infections in the calf: diagnosis, occurrence and experimental transmission. Berl. Munch. Tierarztl. Wochenschr. 94, 289-292.
24. Heitman, T. L., L. M. Frederick, J. R. Viste, N. J. Guselle, U. M. Morgan, R. C. Thompson, and M. E. Olson, 2002: Prevalence of Giardia and Cryptosporidium and characterization of Cryptosporidium spp. isolated from wildlife, human, and agricultural sources in the North Saskatchewan River Basin in Alberta, Canada. Can. J. Microbiol. 48, 530-541.
25. Hunter, P. R., S. Hughes, S. Woodhouse, Q. Syed, N. Q. Verlander, R. M. Chalmers, K. Morgan, G. Nichols, N. Beeching, and K. Osborn, 2004: Sporadic cryptosporidiosis case-control study with genotyping. Emerg. Infect. Dis. 10, 1241-1249.
26. Inman, L. R., and A. Takeuchi, 1979: Spontaneous cryptosporidiosis in an adult female rabbit. Vet. Pathol. 16, 89-95.
27. Iseki, M., T. Maekawa, K. Moriya, S. Uni, and S. Takada, 1989: Infectivity of Cryptosporidium muris (strain RN 66) in various laboratory animals. Parasitol. Res. 75, 218-222.
28. Knipschild, P., 1994: Systematic reviews. Some examples. BMJ 309, 719-721.
29. Koudela, B., D. Modry, and J. Vitovec, 1998: Infectivity of Cryptosporidium muris isolated from cattle. Vet. Parasitol. 76, 181-188.
30. Learmonth, J. J., G. Ionas, K. A. Ebbett, and E. S. Kwan, 2004: Genetic characterization and transmission cycles of Cryptosporidium species isolated from humans in New Zealand. Appl. Environ. Microbiol. 70, 3973-3978.
31. Marounek, M., V. Skrivanova, I. Pavlasek, M. Skrivan, E. Tumova, and P. Brezina, 1985: Comparison of three coccidiocidal drugs in rabbits. 5th Symp.Vitamine und weitere Zusatzstoffe bei Mensch und Tier, Jena, Germany, September 28-29. pp. 483-487.
32. Matsui, T., T. Fujino, J. Kajima, and M. Tsuji, 2000: Infectivity to experimental rodents of Cryptosporidium parvum oocysts from Siberian chipmunks (Tamias sibiricus) originated in the People's Republic of China. J. Vet. Med. Sci. 62, 487-489.
33. McLauchlin, J., C. Amar, S. Pedraza-Diaz, and G. L. Nichols, 2000: Molecular epidemiological analysis of Cryptosporidium spp. in the United Kingdom: results of genotyping Cryptosporidium spp. in 1, 705 fecal samples from humans and 105 fecal samples from livestock animals. J. Clin. Microbiol. 38, 3984-3990.
34. Medema, G. J., 1999: Cryptosporidium and Giardia: new challenges to the water industry. PhD thesis, University of Utrecht, the Netherlands.
35. Mosier, D. A., K. Y. Cimon, T. L. Kuhls, R. D. Oberst, and K. R. Simons, 1997: Experimental cryptosporidiosis in adult and neonatal rabbits. Vet. Parasitol. 69, 163-169.
36. Musaev, M. A., G. D. Gaibova, and G. I. Ismailova, 1996: The prevalence of cryptosporidia among agricultural animals in Azerbaijan. Parazitologiia (St. Petersburg) 30, 478-486.
37. Nagy, B., 1995: Epidemiologic data on Cryptosporidium parvum infection of mammalian domestic animals in Hungary. Magy. Allatorvosok Lapja 50, 139-144.
38. Pavlasek, I., M. Lavicka, E. Tumova, and M. Skrivan, 1996: Spontaneous Cryptosporidium infection in weaned rabbits. Vet. Med. (Praha) 41, 361-366.
39. Peeters, J. E., 1987a: Etiology and pathology of diarrhoea in weanling rabbits. In: Auxilia, T. (ed), Rabbit Production Systems Including Welfare, pp. 127-137. European Communities, Luxembourg.
40. Peeters, J. E., 1987b: Troubles digestifs chez le lapin de chair: causes et prévention. Rev. Agric. 40, 1239-1254.
41. Peeters, J. E., 1988: Recent advances in intestinal pathology of rabbits and further perspectives. In: Holdas, S. (ed.), Proceedings of the 4th World Rabbit Congress, Budapest, Hungary, 10-14 October, pp. 293-315. World Rabbit Science Association.
42. Peeters, J. E., G. J. Chalier, and P. Dussart 1986a: Pouvoir pathogene de Cryptosporidium sp. pour lapereaux avant et après sevrage, 4emes Journees de la Recherche Cunicole, Paris.
43. Peeters, J. E., R. Geeroms, R. J. Carman, and T. D. Wilkins, 1986b: Significance of Clostridium spiroforme in the enteritis-complex of commercial rabbits. Vet. Microbiol. 12, 25-31.
44. Pereira, M. D., E. R. Atwill, and T. Jones, 1999: Comparison of sensitivity of immunofluorescent microscopy to that of a combination of immunofluorescent microscopy and immunomagnetic separation for detection of Cryptosporidium parvum oocysts in adult bovine feces. Appl. Environ. Microbiol. 65, 3236-3239.
45. Pereira, M. D., E. R. Atwill, A. P. Barbosa, S. A. Silva, and M. T. Garcia-Zapata, 2002: Intra-familial and extra-familial risk factors associated with Cryptosporidium parvum infection among children hospitalized for diarrhea in Goiania, Goias, Brazil. Am. J. Trop. Med. Hyg. 66, 787-793.
46. Rehg, J. E., G. W. Lawton, and S. P. Pakes, 1979: Cryptosporidium cuniculus in the rabbit (Oryctolagus cuniculus). Lab. Anim. Sci. 29, 656-660.
47. Robinson, G., K. Elwin, and R. M. Chalmers, 2008a: Unusual Cryptosporidium genotypes in human cases of diarrhea. Emerg. Infect. Dis. 14, 1800-1802.
48. Robinson, G., J. Watkins, and R. M. Chalmers, 2008b: Evaluation of a modified semi-automated immunomagnetic separation technique for the detection of Cryptosporidium oocysts in human faeces. J. Microbiol. Methods 75, 139-141.
49. Ryan, M. J., J. P. Sundberg, R. J. Sauerschell, and K. S. Todd, Jr, 1986: Cryptosporidium in a wild cottontail rabbit (Sylvilagus floridanus). J. Wildl. Dis. 22, 267.
50. Ryan, U., L. Xiao, C. Read, L. Zhou, A. A. Lal, and I. Pavlasek, 2003: Identification of novel Cryptosporidium genotypes from the Czech Republic. Appl. Environ. Microbiol. 69, 4302-4307.
51. Schmidt, R. E., 1995: Protozoal diseases of rabbits and rodents. Semin. Avian Exot. Pet Med. 4, 126-130.
52. Shiibashi, T., T. Imai, Y. Sato, N. Abe, M. Yukawa, and S. Nogami, 2006: Cryptosporidium infection in juvenile pet rabbits. J. Vet. Med. Sci. 68, 281-282.
53. Skrivanova, V., M. Marounek, E. Tumova, M. Skrivan, and I. Pavlasek, 1997: The effect of antimicrobial feed additives and anticoccidics supplementation on nutrient digestibility, performance and health of broiler rabbits. Vet. Med. (Praha). 42, 225-231.
54. Skrivanova, V., M. Marounek, and P. Klein, 1999: Effects of virginiamycin and salinomycin on performance, digestibility of nutrients and mortality of rabbits. Anim. Feed Sci. Technol. 77, 139-147.
55. Smith, R. P., R. M. Chalmers, K. Elwin, F. A. Clifton-Hadley, D. Mueller-Doblies, J. Watkins, G. A. Paiba, and M. Giles, 2009: Investigation of the role of companion animals in the zoonotic transmission of cryptosporidiosis. Zoonoses Public Health 56, 24-33.
56. Soltane, R., K. Guyot, E. Dei-Cas, and A. Ayadi, 2007: Prevalence of Cryptosporidium spp. (Eucoccidiorida: Cryptosporiidae) in seven species of farm animals in Tunisia. Parasite 14, 335-338.
57. Sturdee, A. P., R. M. Chalmers, and S. A. Bull, 1999: Detection of Cryptosporidium oocysts in wild mammals of mainland Britain. Vet. Parasitol. 80, 273-280.
58. Teunis, P. F., C. L. Chappell, and P. C. Okhuysen, 2002: Cryptosporidium dose-response studies: variation between hosts. Risk Anal. 22, 475-485.
59. Tian, Z. C., X. C. Zhang, J. M. Wang, J. G. Yin, J. H. Li, J. B. Chen, and J. Yang, 2001: Random amplified polymorphic DNA analysis of Cryptosporidium species and strains. Chin. J. Parasitol. Parasitic Dis. 19, 100-102.
60. Tian, Z. C., X. C. Zhang, J. H. Li, J. G. Yin, J. Yang, and H. X. He, 2002: Cloning of a species-specific gene fragment from Cryptosporidium parvum and the development of diagnostic PCR primers. Chin. J. Parasitol. Parasitic Dis. 20, 72-75.
61. Tyzzer, E. E., 1912: Cryptosporidium parvum (sp.nov.), a coccidium found in the small intestine of the common mouse. Arch. Protistenkunde 26, 394-412.
62. Vetterling, J. M., H. R. Jervis, T. G. Merrill, and H. Sprinz, 1971: Cryptosporidium wrairi sp. n. from the guinea pig Cavia porcellus, with an emendation of the genus. J. Protozool. 18, 243-247.
63. Webster, K. A., H. V. Smith, M. Giles, L. Dawson, and L. J. Robertson, 1996: Detection of Cryptosporidium parvum oocysts in faeces: comparison of conventional coproscopical methods and the polymerase chain reaction. Vet. Parasitol. 61, 5-13.
64. Xiao, L., 2009: Molecular epidemiology of cryptosporidiosis: an update. Exp. Parasitol. [Epub ahead of print, doi: ].
65. Xiao, L., I. M. Sulaiman, U. M. Ryan, L. Zhou, E. R. Atwill, M. L. Tischler, X. Zhang, R. Fayer, and A. A. Lal, 2002: Host adaptation and host-parasite co-evolution in Cryptosporidium: implications for taxonomy and public health. Int. J. Parasitol. 32, 1773-1785.
66. Xiao, L., R. Fayer, U. Ryan, and S. J. Upton, 2004: Cryptosporidium taxonomy: recent advances and implications for public health. Clin. Microbiol. Rev. 17, 72-97.
67. Yu, H., Z. Chen, C. Yue, R. Mi, and Y. Xia, 2008: Cloning and sequence analysis of Cryptosporidium sp. sporozoite surface antigen p23 gene. Unpublished .