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Molecular and phylogenetic characterization of Cryptosporidium and Giardia from pigs and cattle in Denmark

Published online by Cambridge University Press:  01 November 2006

R. B. LANGKJÆR
Affiliation:
Department of Veterinary Diagnostics and Research, Danish Institute for Food and Veterinary Research, Bülowsvej 27, DK-1790 Copenhagen V, Denmark
H. VIGRE
Affiliation:
Department of Epidemiology and Risk Assessment, Danish Institute for Food and Veterinary Research, Mørkhøj Bygade 29, DK-2860 Søborg, Denmark
H. L. ENEMARK
Affiliation:
Department of Veterinary Diagnostics and Research, Danish Institute for Food and Veterinary Research, Bülowsvej 27, DK-1790 Copenhagen V, Denmark Present address: Department of Large Animal Sciences, Royal Veterinary and Agricultural University, Dyrlaegevej 48, DK-1870 Frederiksberg C, Denmark.
C. MADDOX-HYTTEL
Affiliation:
Department of Veterinary Diagnostics and Research, Danish Institute for Food and Veterinary Research, Bülowsvej 27, DK-1790 Copenhagen V, Denmark

Abstract

The genetic diversity of Cryptosporidium spp. and Giardia duodenalis from dairy cattle and pigs in Denmark was determined in the present study. Faecal samples from 1237 pigs and 1150 cattle originating from 50 sow herds and 50 dairy herds, respectively, were analysed for the presence of the two parasites by immunofluorescence microscopy. A large proportion of the (oo)cyst containing samples were selected for molecular characterization. Sequencing and phylogenetic analysis of the 18S rDNA locus and/or the HSP70 gene of 183 pig and 154 cattle isolates of Cryptosporidium revealed the presence of C. suis, pig genotype II, C. parvum (cattle genotype), C. bovis, Cryptosporidium deer-like genotype and a novel C. suis-like genotype. For both cattle and pigs, a host age-related change in distribution of species/genotypes was observed. The zoonotic C. parvum (cattle genotype) was most prevalent in young calves. For Giardia, 82 and 145 isolates from pigs and cattle, respectively, were analysed at the 18S rDNA locus and/or the gdh gene. Giardia isolates belonging to the zoonotic Assemblage A was found in both young and older calves, as well as in weaners and piglets, whereas cows seemed to be infected purely by isolates of the livestock group, Assemblage E.

Type
Research Article
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Abe, N., Read, C., Thompson, R. C. A. and Iseki, M. (2005). Zoonotic genotype of Giardia intestinalis detected in a ferret. Journal of Parasitology 91, 179182.CrossRefGoogle Scholar
Appelbee, A. J., Frederick, L. M., Heitman, T. L. and Olson, M. E. (2003). Prevalence and genotyping of Giardia duodenalis from beef calves in Alberta, Canada. Veterinary Parasitology 112, 289294.CrossRefGoogle Scholar
Barwick, R. S., Mohammed, H. O., White, M. E. and Bryant, R. B. ( 2003). Prevalence of Giardia spp. and Cryptosporidium spp. on dairy farms in southeastern New York state. Preventive Veterinary Medicine 59, 111.Google Scholar
Becher, K. A., Robertson, I. D., Fraser, D. M., Palmer, D. G. and Thompson, R. C. A. ( 2004). Molecular epidemiology of Giardia and Cryptosporidium infections in dairy calves originating from three sources in Western Australia. Veterinary Parasitology 123, 19.CrossRefGoogle Scholar
Cacciò, S. M., Thompson, R. C. A., McLauchlin, J. and Smith, H. V. ( 2005). Unravelling Cryptosporidium and Giardia epidemiology. Trends in Parasitology 21, 430437.CrossRefGoogle Scholar
Cacciò, S. M., Homan, W., Camilli, R., Traldi, G., Kortbeek, T. and Pozio, E. ( 2000). A microsatellite marker reveals population heterogeneity within human and animal genotypes of Cryptosporidium parvum. Parasitology 120, 237244.CrossRefGoogle Scholar
Enemark, H. L., Ahrens, P., Bille-Hansen, V., Heegaard, P. M., Vigre, H., Thamsborg, S. M. and Lind, P. ( 2003). Cryptosporidium parvum: infectivity and pathogenicity of the ‘porcine’ genotype. Parasitology 126, 407416.CrossRefGoogle Scholar
Enemark, H. L., Ahrens, P., Juel, C. D., Petersen, E., Petersen, R. F., Andersen, J. S., Lind, P. and Thamsborg, S. M. ( 2002 a). Molecular characterization of Danish Cryptosporidium parvum isolates. Parasitology 125, 331341.Google Scholar
Enemark, H. L., Ahrens, P., Lowery, C. J., Thamsborg, S. M., Enemark, J. M. D., Bille-Hansen, V. and Lind, P. ( 2002 b). Cryptosporidium andersoni from a Danish cattle herd: identification and preliminary characterisation. Veterinary Parasitology 107, 3749.Google Scholar
Fayer, R. ( 2004). Cryptosporidium: a water-borne zoonotic parasite. Veterinary Parasitology 126, 3756.CrossRefGoogle Scholar
Fayer, R., Santín, M., Trout, J. M. and Greiner, E. ( 2006). Prevalence of species and genotypes of Cryptosporidium found in 1-2-year-old dairy cattle in the eastern United States. Veterinary Parasitology 135, 105112.CrossRefGoogle Scholar
Fayer, R., Santín, M. and Xiao, L. ( 2005). Cryptosporidium bovis n. sp. (Apicomplexa: Cryptosporidiidae) in Cattle (Bos taurus). Journal of Parasitology 91, 624629.Google Scholar
Hall, T. A. ( 1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.Google Scholar
Henriksen, S. A. and Krogh, H. V. ( 1985). Bovine cryptosporidiosis in Denmark. 1. prevalence, age distribution and seasonal variation. Nordisk Veterinaermedicin 37, 3441.Google Scholar
Hopkins, R. M., Meloni, B. P., Groth, D. M., Wetherall, J. D., Reynoldson, J. A. and Thompson, R. C. A. ( 1997). Ribosomal RNA sequencing reveals differences between the genotypes of Giardia isolates recovered from humans and dogs living in the same locality. Journal of Parasitology 83, 4451.CrossRefGoogle Scholar
Huetink, R. E. C., Van Der Giessen, J. W. B., Noordhuizen, J. P. T. M. and Ploeger, H. W. ( 2001). Epidemiology of Cryptosporidium spp. and Giardia duodenalis on a dairy farm. Veterinary Parasitology 102, 5367.Google Scholar
Iburg, T., Gasser, R. B. and Henriksen, S. A. ( 1996). First record of Giardia in cattle in Denmark. Acta Veterinaria Scandinavica 37, 337341.Google Scholar
Itagaki, T., Kinoshita, S., Aoki, M., Itoh, N., Saeki, H., Sato, N., Uetsuki, J., Izumiyama, S., Yagita, K. and Endo, T. ( 2005). Genotyping of Giardia intestinalis from domestic and wild animals in Japan using glutamate dehydrogenase gene sequencing. Veterinary Parasitology 133, 283287.CrossRefGoogle Scholar
Jin, L. and Nei, M. ( 1990). Limitations of the evolutionary parsimony method of phylogenetic analysis. Molecular Biology and Evolution 7, 82102.Google Scholar
Jukes, T. H. and Cantor, C. R. ( 1969). Evolution of protein molecules. In Mammalian Protein Metabolism , (ed. Munro, H. N.), pp. 21123. Academic Press, New York.CrossRef
Kulldorff, M. ( 2003). SaTScan v4.0 Software for the spatial and space-time scan statistics. Information Management Services, Inc. http://www.satscan.org/.
Lalle, M., Pozio, E., Capelli, G., Bruschi, F., Crotti, D. and Cacció, S. M. ( 2005). Genetic heterogeneity at the β-giardin locus among human and animal isolates of Giardia duodenalis and identification of potentially zoonotic subgenotypes. International Journal for Parasitology 35, 207213.CrossRefGoogle Scholar
Maddox-Hyttel, C., Langkjær, R. B., Enemark, H. L. and Vigre, H. ( 2006). Cryptosporidium and Giardia in different age groups of Danish cattle and pigs – occurrence and management associated risk factors. Veterinary Parasitology 141, 4859.CrossRefGoogle Scholar
Mallon, M. E., MacLeod, A., Wastling, J. M., Smith, H., Tait, A. ( 2003). Multilocus genotyping of Cryptosporidium parvum Type 2: population genetics and sub-structuring. Infection, Genetics and Evolution 3, 207218.CrossRefGoogle Scholar
Monis, P. T., Andrews, R. H., Mayrhofer, G. and Ey, P. L. ( 2003). Genetic diversity within the morphological species Giardia intestinalis and its relationship to host origin. Infection, Genetics and Evolution 3, 2938.CrossRefGoogle Scholar
Morgan, U. M., Monis, P. T., Xiao, L., Limor, J., Sulaiman, I., Raidal, S., O'Donoghue, P., Gasser, R. B., Murray, A., Fayer, R., Blagburn, B. L., Lal, A. A. and Thompson, R. C. A. ( 2001). Molecular and phylogenetic characterisation of Cryptosporidium from birds. International Journal for Parasitology 31, 289296.CrossRefGoogle Scholar
Morgan, U. M., Buddle, J. R., Armson, A., Elliot, A. and Thompson, R. C. A. ( 1999). Molecular and biological characterisation of Cryptosporidium in pigs. Australian Veterinary Journal 77, 4447.CrossRefGoogle Scholar
O'Handley, R. M., Olson, M. E., Fraser, D., Adams, P. and Thompson, R. C. A. ( 2000). Prevalence and genotypic characterisation of Giardia in dairy calves from Western Australia and Western Canada. Veterinary Parasitology 90, 193200.CrossRefGoogle Scholar
Olson, M. E., O'Handley, R. M., Ralston, B. J., McAllister, T. A. and Thompson, R. C. A. ( 2004). Update on Cryptosporidium and Giardia infections in cattle. Trends in Parasitology 20, 185191.CrossRefGoogle Scholar
Read, C. M., Monis, P. T. and Thompson, R. C. ( 2004). Discrimination of all genotypes of Giardia duodenalis at the glutamate dehydrogenase locus using PCR-RFLP. Infection, Genetics and Evolution 4, 125130.CrossRefGoogle Scholar
Read, C., Walters, J., Robertson, I. D. and Thompson, R. C. ( 2002). Correlation between genotype of Giardia duodenalis and diarrhoea. International Journal for Parasitology 32, 229231.CrossRefGoogle Scholar
Ryan, U., Read, C., Hawkins, P., Warnecke, M., Swanson, P., Griffith, M., Deere, D., Cunningham, M. and Cox, P. ( 2005). Genotypes of Cryptosporidium from Sydney water catchment areas. Journal of Applied Microbiology 98, 12211229.CrossRefGoogle Scholar
Ryan, U. M., Monis, P., Enemark, H L., Sulaiman, I., Samarasinghe, B., Read, C., Buddle, R., Robertson, I., Zhou, L., Thompson, R. C. and Xiao, L. ( 2004). Cryptosporidium suis n. sp. (Apicomplexa: Cryptosporidiidae) in Pigs (Sus scrofa). Journal of Parasitology 90, 769773.Google Scholar
Ryan, U. M., Samarasinghe, B., Read, C., Buddle, J. R., Robertson, I. D. and Thompson, R. C. A. ( 2003). Identification of a novel Cryptosporidium genotype in pigs. Applied and Environmental Microbiology 69, 39703974.CrossRefGoogle Scholar
Santín, M., Trout, J. M., Xiao, L., Zhou, L., Greiner, E. and Fayer, R. ( 2004). Prevalence and age-related variation of Cryptosporidium species and genotypes in dairy calves. Veterinary Parasitology 122, 103117.CrossRefGoogle Scholar
Tajima, F. and Nei, M. ( 1984). Estimation of evolutionary distance between nucleotide sequences. Molecular Biology and Evolution 1, 269285.Google Scholar
Thompson, R. C. A. ( 2004). The zoonotic significance and molecular epidemiology of Giardia and giardiasis. Veterinary Parasitology 126, 1535.CrossRefGoogle Scholar
Thompson, R. C. A. and Monis, P. T. ( 2004). Variation in Giardia: implications for taxonomy and epidemiology. Advances in Parasitology 58, 69137.CrossRefGoogle Scholar
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. ( 1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24, 48764882.CrossRefGoogle Scholar
Thurston-Enriquez, J. A., Gilley, J. E. and Eghball, B. ( 2005). Microbial quality of runoff following land application of cattle manure and swine slurry. Journal of Water and Health 3, 157171.CrossRefGoogle Scholar
Traub, R., Wade, S., Read, C., Thompson, A. and Mohammed, H. ( 2005). Molecular characterization of potentially zoonotic isolates of Giardia duodenalis in horses. Veterinary Parasitology 130, 317321.CrossRefGoogle Scholar
Traub, R. J., Monis, P. T., Robertson, I., Irwin, P., Mencke, N. and Thompson, R. C. A. ( 2004). Epidemiological and molecular evidence supports the zoonotic transmission of Giardia among humans and dogs living in the same community. Parasitology 128, 253262.CrossRefGoogle Scholar
Trout, J. M., Santín, M., Greiner, E. and Fayer, R. ( 2005). Prevalence and genotypes of Giardia duodenalis in post-weaned dairy calves. Veterinary Parasitology 130, 177183.CrossRefGoogle Scholar
Trout, J. M., Santín, M., Greiner, E. and Fayer, R. ( 2004). Prevalence of Giardia duodenalis genotypes in pre-weaned dairy calves. Veterinary Parasitology 124, 179186.CrossRefGoogle Scholar
Van de Peer, Y. and De Wachter, R. ( 1994). TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Computer Applications in the Biosciences 10, 569570.CrossRefGoogle Scholar
van Keulen, H., Macechko, P. T., Wade, S., Schaaf, S., Wallis, P. M. and Erlandsen, S. L. ( 2002). Presence of human Giardia in domestic, farm and wild animals, and environmental samples suggests a zoonotic potential for giardiasis. Veterinary Parasitology 108, 97107.CrossRefGoogle Scholar
Xiao, L., Fayer, R., Ryan, U. and Upton, S. J. ( 2004). Cryptosporidium taxonomy: recent advances and implications for public health. Clinical Microbiology Reviews 17, 7297.CrossRefGoogle Scholar
Xiao, L., Bern, C., Arrowood, M., Sulaiman, I., Zhou, L., Kawai, V., Vivar, A., Lal, A. A. and Gilman, R. H. ( 2002 a). Identification of the Cryptosporidium pig genotype in a human patient. Journal of Infectious Diseases 185, 18461848.Google Scholar
Xiao, L., Sulaiman, I. M., Ryan, U. M., Zhou, L., Atwill, E. R., Tischler, M. L., Zhang, X., Fayer, R. and Lal, A. A. ( 2002 b). Host adaptation and host-parasite co-evolution in Cryptosporidium: implications for taxonomy and public health. International Journal for Parasitology 32, 17731785.Google Scholar