Occurrence and molecular characterization of Cryptosporidium spp. and Enterocytozoon bieneusi in dairy cattle, beef cattle and water buffaloes in China

Veterinary Parasitology

Volumn 207, Issue 3-4, 2015, Pages 220-227

  Ma, Jingbo ^a   Li, Pei ^a   Zhao, Xiaoping ^b   Xu, Hailing ^a   Wu, Wenxian ^a   Wang, Yuanfei ^a   Guo, Yaqiong ^a   Wang, Lin ^a   Feng, Yaoyu ^a   Xiao, Lihua ^c  

^a EAST CHINA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b Yueyang Center for Animal Disease Control and Prevention   (China)

^c NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

Author keywords

Cattle; Cryptosporidium; Enterocytozoon bieneusi; ITS; Nested PCR; SSU rRNA gene

Indexed keywords

INTERNAL TRANSCRIBED SPACER; SMALL SUBUNIT RIBOSOMAL RNA; RIBOSOMAL SPACER DNA;

ADOLESCENT; ADULT; ARTICLE; BEEF CATTLE; CHINA; CONTROLLED STUDY; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM; CRYPTOSPORIDIUM ANDERSONI; CRYPTOSPORIDIUM BOVIS; CRYPTOSPORIDIUM RYANAE; CRYPTOSPORIDIUM SUIS; DAIRY CATTLE; ENTEROCYTOZOON; FECES ANALYSIS; GENE TARGETING; GENOTYPE; INFECTION RATE; MICROSPORIDIOSIS; MIXED INFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; RNA GENE; RNA SEQUENCE; SEQUENCE ANALYSIS; SPECIES DIFFERENCE; WATER BUFFALO; YAK; ANIMAL; BOVINE; BUFFALO; CATTLE DISEASES; GENETICS; MICROBIOLOGY; PARASITOLOGY; PHYSIOLOGY; VETERINARY;

ANIMALIA; BOS; BOVINAE; BUBALUS; CRYPTOSPORIDIUM; CRYPTOSPORIDIUM ANDERSONI; CRYPTOSPORIDIUM BOVIS; CRYPTOSPORIDIUM SUIS; ENTEROCYTOZOON BIENEUSI; PROTISTA; VERTEBRATA;

ANIMALS; BUFFALOES; CATTLE; CATTLE DISEASES; CHINA; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM; DNA, RIBOSOMAL SPACER; ENTEROCYTOZOON; GENES, RRNA; GENOTYPE; MICROSPORIDIOSIS;

EID: 84922754200     PISSN: 03044017     EISSN: 18732550     Source Type: Journal    
DOI: 10.1016/j.vetpar.2014.10.011     Document Type: Article

References (73)

1. Abeywardena H., Jex A.R., Firestone S.M., McPhee S., Driessen N., Koehler A.V., Haydon S.R., von Samson-Himmelstjerna G., Stevens M.A., Gasser R.B. Assessing calves as carriers of Cryptosporidium and Giardia with zoonotic potential on dairy and beef farms within a water catchment area by mutation scanning. Electrophoresis 2013, 34:2259-2267.
2. Abeywardena H., Jex A.R., von Samson-Himmelstjerna G., Haydon S.R., Stevens M.A., Gasser R.B. First molecular characterisation of Cryptosporidium and Giardia from Bubalus bubalis (water buffalo) in Victoria, Australia. Infect. Genet. Evol. 2013, 20:96-102.
3. Abu Samra N., Thompson P.N., Jori F., Zhang H., Xiao L. Enterocytozoon bieneusi at the wildlife/livestock interface of the Kruger National Park, South Africa. Vet. Parasitol. 2012, 190:587-590.
4. Amer S., Honma H., Ikarashi M., Tada C., Fukuda Y., Suyama Y., Nakai Y. Cryptosporidium genotypes and subtypes in dairy calves in Egypt. Vet. Parasitol. 2010, 169:382-386.
5. Amer S., Zidan S., Feng Y., Adamu H., Li N., Xiao L. Identity and public health potential of Cryptosporidium spp. in water buffalo calves in Egypt. Vet. Parasitol. 2013, 191:123-127.
6. Anane S., Attouchi H. Microsporidiosis: epidemiology, clinical data and therapy. Gastroenterol. Clin. Biol. 2010, 34:450-464.
7. Baldursson S., Karanis P. Waterborne transmission of protozoan parasites: review of worldwide outbreaks - an update 2004-2010. Water Res. 2011, 45:6603-6614.
8. Blackburn B.G., Mazurek J.M., Hlavsa M., Park J., Tillapaw M., Parrish M., Salehi E., Franks W., Koch E., Smith F., Xiao L., Arrowood M., Hill V., da Silva A., Johnston S., Jones J.L. Cryptosporidiosis associated with ozonated apple cider. Emerg. Infect. Dis. 2006, 12:684-686.
9. Budu-Amoako E., Greenwood S.J., Dixon B.R., Barkema H.W., McClure J.T. Giardia and Cryptosporidium on dairy farms and the role these farms may play in contaminating water sources in Prince Edward Island, Canada. J. Vet. Intern. Med. 2012, 26:668-673.
10. Caccio S.M., Pozio E. Advances in the epidemiology, diagnosis and treatment of cryptosporidiosis. Expert Rev. Anti Infect. Ther. 2006, 4:429-443.
11. Chalmers R.M., Katzer F. Looking for Cryptosporidium: the application of advances in detection and diagnosis. Trends Parasitol. 2013, 29:237-251.
12. Del Coco V.F., Cordoba M.A., Bilbao G., de Almeida Castro P., Basualdo J.A., Santin M. First report of Enterocytozoon bieneusi from dairy cattle in Argentina. Vet. Parasitol. 2014, 199:112-115.
13. Dengjel B., Zahler M., Hermanns W., Heinritzi K., Spillmann T., Thomschke A., Loscher T., Gothe R., Rinder H. Zoonotic potential of Enterocytozoon bieneusi. J. Clin. Microbiol. 2001, 39:4495-4499.
14. Didier E.S., Weiss L.M. Microsporidiosis: not just in AIDS patients. Curr. Opin. Infect. Dis. 2011, 24:490-495.
15. Dixon B., Parrington L., Cook A., Pintar K., Pollari F., Kelton D., Farber J. The potential for zoonotic transmission of Giardia duodenalis and Cryptosporidium spp. from beef and dairy cattle in Ontario, Canada. Vet. Parasitol. 2011, 175:20-26.
16. Fayer R. Taxonomy and species delimitation in Cryptosporidium. Exp. Parasitol. 2010, 124:90-97.
17. Fayer R., Santin M., Macarisin D. Detection of concurrent infection of dairy cattle with Blastocystis, Cryptosporidium, Giardia, and Enterocytozoon by molecular and microscopic methods. Parasitol. Res. 2012, 111:1349-1355.
18. Fayer R., Santin M., Trout J.M. First detection of microsporidia in dairy calves in North America. Parasitol. Res. 2003, 90:383-386.
19. Fayer R., Santin M., Trout J.M. Enterocytozoon bieneusi in mature dairy cattle on farms in the eastern United States. Parasitol. Res. 2007, 102:15-20.
20. Fayer R., Santin M., Trout J.M. 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. 2007, 145:260-266.
21. Fayer R., Santin M., Trout J.M., Greiner E. Prevalence of species and genotypes of Cryptosporidium found in 1-2-year-old dairy cattle in the eastern United States. Vet. Parasitol. 2006, 135:105-112.
22. Feng Y., Karna S.R., Dearen T.K., Singh D.K., Adhikari L.N., Shrestha A., Xiao L. Common occurrence of a unique Cryptosporidium ryanae variant in zebu cattle and water buffaloes in the buffer zone of the Chitwan National Park, Nepal. Vet. Parasitol. 2012, 185:309-314.
23. Feng Y., Ortega Y., He G., Das P., Xu M., Zhang X., Fayer R., Gatei W., Cama V., Xiao L. Wide geographic distribution of Cryptosporidium bovis and the deer-like genotype in bovines. Vet. Parasitol. 2007, 144:1-9.
24. Geurden T., Goma F.Y., Siwila J., Phiri I.G., Mwanza A.M., Gabriel S., Claerebout E., Vercruysse J. Prevalence and genotyping of Cryptosporidium in three cattle husbandry systems in Zambia. Vet. Parasitol. 2006, 138:217-222.
25. Guo Y., Alderisio K.A., Yang W., Cama V., Feng Y., Xiao L. Host specificity and source of Enterocytozoon bieneusi genotypes in a drinking source watershed. Appl. Environ. Microbiol. 2014, 80:218-225.
26. Jiang J., Alderisio K.A., Singh A., Xiao L. Development of procedures for direct extraction of Cryptosporidium DNA from water concentrates and for relief of PCR inhibitors. Appl. Environ. Microbiol. 2005, 71:1135-1141.
27. Jurankova J., Kamler M., Kovarcik K., Koudela B. Enterocytozoon bieneusi in Bovine Viral Diarrhea Virus (BVDV) infected and noninfected cattle herds. Res. Vet. Sci. 2013, 94:100-104.
28. Karim M.R., Wang R.J., Dong H.J., Zhang L.X., Li J., Zhang S.M., Rume F.I., Qi M., Jian F.C., Sun M.F., Yang G.Y., Zou F.C., Ning C.S., Xiao L.H. Genetic polymorphism and zoonotic potential of Enterocytozoon bieneusi from nonhuman primates in China. Appl. Environ. Microb. 2014, 80:1893-1898.
29. Khan S.M., Debnath C., Pramanik A.K., Xiao L., Nozaki T., Ganguly S. Molecular characterization and assessment of zoonotic transmission of Cryptosporidium from dairy cattle in West Bengal, India. Vet. Parasitol. 2010, 171:41-47.
30. Langkjaer R.B., Vigre H., Enemark H.L., Maddox-Hyttel C. Molecular and phylogenetic characterization of Cryptosporidium and Giardia from pigs and cattle in Denmark. Parasitology 2007, 134:339-350.
31. Leoni F., Amar C., Nichols G., Pedraza-Diaz S., McLauchlin J. Genetic analysis of Cryptosporidium from 2414 humans with diarrhoea in England between 1985 and 2000. J. Med. Microbiol. 2006, 55:703-707.
32. Liu A., Wang R., Li Y., Zhang L., Shu J., Zhang W., Feng Y., Xiao L., Ling H. Prevalence and distribution of Cryptosporidium spp. in dairy cattle in Heilongjiang Province, China. Parasitol. Res. 2009, 105:797-802.
33. Ma J., Cai J., Ma J., Feng Y., Xiao L. Enterocytozoon bieneusi genotypes in yaks (Bos grunniens) and their public health potential. J. Eukaryot. Microbiol. 2014, (in press).
34. Ma J., Cai J., Ma J., Feng Y., Xiao L. Occurrence and molecular characterization of Cryptosporidium spp. in yaks (Bos grunniens) in China. Vet. Parasitol. 2014, 202:113-118.
35. Maikai B.V., Umoh J.U., Kwaga J.K., Lawal I.A., Maikai V.A., Cama V., Xiao L. Molecular characterization of Cryptosporidium spp. in native breeds of cattle in Kaduna State, Nigeria. Vet. Parasitol. 2011, 178:241-245.
36. Matos O., Lobo M.L., Xiao L. Epidemiology of Enterocytozoon bieneusi infection in humans. J. Parasitol. Res. 2012, 2012. 981424.
37. Mi R., Wang X., Li C., Huang Y., Zhou P., Li Z., Lei M., Cai J., Chen Z. Prevalence and genetic characterization of Cryptosporidiumin yaks in Qinghai Province of China. PLOS ONE 2013, 8:e74985.
38. Muhid A., Robertson I., Ng J., Ryan U. Prevalence of and management factors contributing to Cryptosporidium sp. infection in pre-weaned and post-weaned calves in Johor, Malaysia. Exp. Parasitol. 2011, 127:534-538.
39. Murakoshi F., Xiao L., Matsubara R., Sato R., Kato Y., Sasaki T., Fukuda Y., Tada C., Nakai Y. Molecular characterization of Cryptosporidium spp. in grazing beef cattle in Japan. Vet. Parasitol. 2012, 187:123-128.
40. Nasir A., Avais M., Khan M.S., Ahmad N. Prevalence of Cryptosporidium parvum infection in Lahore (Pakistan) and its association with diarrhea in dairy calves. Int. J. Agric. Biol. 2009, 11:221-224.
41. Ng J.S., Eastwood K., Walker B., Durrheim D.N., Massey P.D., Porigneaux P., Kemp R., McKinnon B., Laurie K., Miller D., Bramley E., Ryan U. Evidence of Cryptosporidium transmission between cattle and humans in northern New South Wales. Exp. Parasitol. 2012, 130:437-441.
42. Olson M.E., O'Handley R.M., Ralston B.J., McAllister T.A., Thompson R.C. Update on Cryptosporidium and Giardia infections in cattle. Trends Parasitol. 2004, 20:185-191.
43. Ondrackova Z., Kvac M., Sak B., Kvetonova D., Rost M. Prevalence and molecular characterization of Cryptosporidium spp. in dairy cattle in South Bohemia, the Czech Republic. Vet. Parasitol. 2009, 165:141-144.
44. Ong C.S.L., Eisler D.L., Alikhani A., Fung V.W.K., Tomblin J., Bowie W.R., Isaac-Renton J.L. Novel Cryptosporidium genotypes in sporadic cryptosporidiosis cases: first report of human infections with a cervine genotype. Emerg. Infect. Dis. 2002, 8:263-268.
45. Paul S., Chandra D., Tewari A.K., Banerjee P.S., Ray D.D., Raina O.K., Rao J.R. Prevalence of Cryptosporidium andersoni: a molecular epidemiological survey among cattle in India. Vet. Parasitol. 2009, 161:31-35.
46. Pirestani M., Sadraei J., Forouzandeh M. Molecular characterization and genotyping of human related microsporidia in free-ranging and captive pigeons of Tehran, Iran. Infect. Genet. Evol. 2013, 20:495-499.
47. Reetz J., Rinder H., Thomschke A., Manke H., Schwebs M., Bruderek A. First detection of the microsporidium Enterocytozoon bieneusi in non-mammalian hosts (chickens). Int. J. Parasitol. 2002, 32:785-787.
48. Rieux A., Chartier C., Pors I., Paraud C. Dynamics of excretion and molecular characterization of Cryptosporidium isolates in pre-weaned French beef calves. Vet. Parasitol. 2013, 195:169-172.
49. Rinder H., Thomschke A., Dengjel B., Gothe R., Loscher T., Zahler M. Close genotypic relationship between Enterocytozoon bieneusi from humans and pigs and first detection in cattle. J. Parasitol. 2000, 86:185-188.
50. Robinson G., Chalmers R.M., Stapleton C., Palmer S.R., Watkins J., Francis C., Kay D. A whole water catchment approach to investigating the origin and distribution of Cryptosporidium species. J. Appl. Microbiol. 2011, 111:717-730.
51. Robinson G., Thomas A.L., Daniel R.G., Hadfield S.J., Elwin K., Chalmers R.M. Sample prevalence and molecular characterisation of Cryptosporidium andersoni within a dairy herd in the United Kingdom. Vet. Parasitol. 2006, 142:163-167.
52. Ryan U., Xiao L., Read C., Zhou L., Lal A.A., Pavlasek I. Identification of novel Cryptosporidium genotypes from the Czech Republic. Appl. Environ. Microbiol. 2003, 69:4302-4307.
53. Sak B., Brady D., Pelikanova M., Kvetonova D., Rost M., Kostka M., Tolarova V., Huzova Z., Kvac M. Unapparent microsporidial infection among immunocompetent humans in the Czech Republic. J. Clin. Microbiol. 2011, 49:1064-1070.
54. Santin M., Dargatz D., Fayer R. Prevalence and genotypes of Enterocytozoon bieneusiin weaned beef calves on cow-calf operations in the USA. Parasitol. Res. 2012, 110:2033-2041.
55. Santin M., Fayer R. Enterocytozoon bieneusi genotype nomenclature based on the internal transcribed spacer sequence: a consensus. J. Eukaryot. Microbiol. 2009, 56:34-38.
56. Santin M., Fayer R. Microsporidiosis: Enterocytozoon bieneusiin domesticated and wild animals. Res. Vet. Sci. 2011, 90:363-371.
57. Santin M., Trout J.M., Fayer R. A longitudinal study of cryptosporidiosis in dairy cattle from birth to 2 years of age. Vet. Parasitol. 2008, 155:15-23.
58. Santin M., Trout J.M., Xiao L., Zhou L., Greiner E., Fayer R. Prevalence and age-related variation of Cryptosporidium species and genotypes in dairy calves. Vet. Parasitol. 2004, 122:103-117.
59. Silverlas C., Naslund K., Bjorkman C., Mattsson J.G. Molecular characterisation of Cryptosporidium isolates from Swedish dairy cattle in relation to age, diarrhoea and region. Vet. Parasitol. 2010, 169:289-295.
60. Sulaiman I.M., Fayer R., Lal A.A., Trout J.M., Schaefer F.W., Xiao L. Molecular characterization of microsporidia indicates that wild mammals harbor host-adapted Enterocytozoon spp. as well as human-pathogenic Enterocytozoon bieneusi. Appl. Environ. Microbiol. 2003, 69:4495-4501.
61. Thellier M., Breton J. Enterocytozoon bieneusi in human and animals, focus on laboratory identification and molecular epidemiology. Parasite 2008, 15:349-358.
62. Venu R., Latha B.R., Basith S.A., Raj G.D., Sreekumar C., Raman M. Molecular prevalence of Cryptosporidium spp. in dairy calves in Southern states of India. Vet. Parasitol. 2012, 188:19-24.
63. Wang L., Xiao L., Duan L., Ye J., Guo Y., Guo M., Liu L., Feng Y. Concurrent infections of Giardia duodenalis, Enterocytozoon bieneusi, and Clostridium difficile in children during a cryptosporidiosis outbreak in a pediatric hospital in China. PLoS Negl. Trop. Dis. 2013, 7:e2437.
64. Wang L., Zhang H., Zhao X., Zhang L., Zhang G., Guo M., Liu L., Feng Y., Xiao L. Zoonotic Cryptosporidium species and Enterocytozoon bieneusi genotypes in HIV-positive patients on antiretroviral therapy. J. Clin. Microbiol. 2013, 51:557-563.
65. Wang R., Ma G., Zhao J., Lu Q., Wang H., Zhang L., Jian F., Ning C., Xiao L. Cryptosporidium andersoni is the predominant species in post-weaned and adult dairy cattle in China. Parasitol. Int. 2011, 60:1-4.
66. Wang R., Wang H., Sun Y., Zhang L., Jian F., Qi M., Ning C., Xiao L. Characteristics of Cryptosporidium transmission in preweaned dairy cattle in Henan, China. J. Clin. Microbiol. 2011, 49:1077-1082.
67. Xiao L. Molecular epidemiology of cryptosporidiosis: an update. Exp. Parasitol. 2010, 124:80-89.
68. Xiao L., Bern C., Arrowood M., Sulaiman I., Zhou L., Kawai V., Vivar A., Lal A.A., Gilman R.H. Identification of the Cryptosporidium pig genotype in a human patient. J. Infect. Dis. 2002, 185:1846-1848.
69. Xiao L., Fayer R. Molecular characterisation of species and genotypes of Cryptosporidium and Giardia and assessment of zoonotic transmission. Int. J. Parasitol. 2008, 38:1239-1255.
70. Xiao L., Feng Y. Zoonotic cryptosporidiosis. FEMS Immunol. Med. Microbiol. 2008, 52:309-323.
71. Zhang W., Wang R., Yang F., Zhang L., Cao J., Zhang X., Ling H., Liu A., Shen Y. Distribution and genetic characterizations of Cryptosporidium spp. in pre-weaned dairy calves in Northeastern China's Heilongjiang Province. PLOS ONE 2013, 8:e54857.
72. Zhang X., Wang Z., Su Y., Liang X., Sun X., Peng S., Lu H., Jiang N., Yin J., Xiang M., Chen Q. Identification and genotyping of Enterocytozoon bieneusi in China. J. Clin. Microbiol. 2011, 49:2006-2008.
73. Zhao G.H., Ren W.X., Gao M., Bian Q.Q., Hu B., Cong M.M., Lin Q., Wang R.J., Qi M., Qi M.Z., Zhu X.Q., Zhang L.X. Genotyping Cryptosporidium andersoni in cattle in Shaanxi Province, Northwestern China. PLOS ONE 2013, 8:e60112.