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Cryptosporidium species and subtype analysis from dairy calves in Spain

Published online by Cambridge University Press:  04 November 2008

J. QUILEZ ,
E. TORRES ,
R. M. CHALMERS ,
G. ROBINSON ,
E. DEL CACHO  and
C. SANCHEZ-ACEDO
J. QUILEZ*
Affiliation:
Department of Animal Pathology, Faculty of Veterinary Sciences, University of Zaragoza, 50013 Zaragoza, Spain
E. TORRES
Affiliation:
Department of Animal Pathology, Faculty of Veterinary Sciences, University of Zaragoza, 50013 Zaragoza, Spain
R. M. CHALMERS
Affiliation:
UK Cryptosporidium Reference Unit, NPHS Microbiology Swansea, Singleton Hospital, Swansea SA2 8QA, UK
G. ROBINSON
Affiliation:
UK Cryptosporidium Reference Unit, NPHS Microbiology Swansea, Singleton Hospital, Swansea SA2 8QA, UK
E. DEL CACHO
Affiliation:
Department of Animal Pathology, Faculty of Veterinary Sciences, University of Zaragoza, 50013 Zaragoza, Spain
C. SANCHEZ-ACEDO
Affiliation:
Department of Animal Pathology, Faculty of Veterinary Sciences, University of Zaragoza, 50013 Zaragoza, Spain
*
*Corresponding author: Department of Animal Pathology, Faculty of Veterinary Sciences, University of Zaragoza, Miguel Servet 177, 50013 Zaragoza, Spain. Tel: +34 976 762150. Fax: +34 976 761612. E-mail: jquilez@unizar.es
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Summary

Faecal specimens from 287 diarrhoeic calves younger than 21 days, collected over a 2-year period (2006–2007) from 82 dairy cattle farms in 14 provinces across the north of Spain, were examined for the presence of Cryptosporidium oocysts. Overall, 63 farms (76·8%) and 166 calves (57·8%) tested positive by microscopy. In order to elucidate the genetic diversity, selected positive specimens from 149 calves originating from 61 farms in the 14 provinces were examined by genotyping and subtyping techniques. Cryptosporidium parvum was the only species identified by PCR-RFLP of SSU rDNA from all 149 isolates and sequencing of a subset of 50 isolates, except for 2 specimens that were identified as C. bovis. Sequence analyses of the glycoprotein (GP60) gene revealed that most C. parvum isolates (98%) belonged to the subtype family IIa and 2 isolates were identified as the novel subtype IIdA23G1. Subtype IIaA15G2R1 was the most common and widely distributed (80·3% of the 61 farms), followed by subtype IIaA16G3R1 (14·7%), whereas the remaining IIa subtypes (IIaA16G2R1, IIaA17G2R1, IIaA18G3R1, IIaA19G3R1) were restricted to 1–3 farms. All these C. parvum IIa subtypes have previously been described in human patients, indicating that most isolates from diarrhoeic calves in northern Spain have zoonotic potential.

Keywords

Cryptosporidiumdairy calvesPCR-RFLPGP60 subtypesSpain
Type
Research Article
Information
Parasitology , Volume 135 , Issue 14 , December 2008 , pp. 1613 - 1620
Copyright
Copyright © 2008 Cambridge University Press

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References

REFERENCES

Alves, M., Xiao, L., Antunes, F. and Matos, O. (2006). Distribution of Cryptosporidium subtypes in humans and domestic and wild ruminants in Portugal. Parasitology Research 99, 287–292.CrossRefGoogle ScholarPubMed
Alves, M., Xiao, L., Sulaiman, I., Lal, A. A., Matos, O. and Antunes, F. (2003). Subgenotype analysis of Cryptosporidium isolates from humans, cattle, and zoo ruminants in Portugal. Journal of Clinical Microbiology 41, 2744–2747.CrossRefGoogle ScholarPubMed
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. and Jones, J. L. (2006). Outbreak of cryptosporidiosis associated with consumption of ozonated apple cider. Emerging Infectious Diseases 12, 684–687.CrossRefGoogle Scholar
Broglia, A., Reckinger, S., Cacciò, S. M. and Nöckler, K. (2008). Distribution of Cryptosporidium subtypes in calves in Germany. Veterinary Parasitology 154, 8–13.CrossRefGoogle ScholarPubMed
Brook, E. J., Hart, C. A., French, N. P. and Christley, R. M. (2008). Molecular epidemiology of Cryptosporidium subtypes in cattle in England. The Veterinary Journal (in the Press). doi:10.1016/j.tvjl.2007.10.023.Google ScholarPubMed
Cacciò, S. M., Thompson, R. C. A., McLauchlin, J. and Smith, H. V. (2005). Unravelling Cryptosporidium and Giardia epidemiology. Trends in Parasitology 21, 430–437.CrossRefGoogle ScholarPubMed
Cama, V., Gilman, R. H., Vivar, A., Ticona, E., Ortega, Y., Bern, C. and Xiao, L. (2006). Mixed Cryptosporidium infections and HIV. Emerging Infectious Diseases 12, 1025–1028.CrossRefGoogle ScholarPubMed
Castro-Hermida, J. A., Almeida, A., González-Warleta, M., Correira Da Costa, J. M. and Mezo, M. (2006). Prevalence and preliminary genetic characterization of Cryptosporidium spp. isolated from asymptomatic heifers in Galicia (NW, Spain). The Journal of Eukaryotic Microbiology 53, S22–S23.Google ScholarPubMed
Castro-Hermida, J. A., Almeida, A., González-Warleta, M., Correira Da Costa, J. M., Rumbo-Lorenzo, C. and Mezo, M. (2007). Occurrence of Cryptosporidium parvum and Giardia duodenalis in healthy adult domestic ruminants. Parasitology Research 101, 1443–1448.CrossRefGoogle ScholarPubMed
Castro-Hermida, J. A., González-Losada, Y. A. and Ares-Mazás, E. (2002). Prevalence and risk factors involved in the spread of neonatal bovine cryptosporidiosis. Veterinary Parasitology 106, 1–10.CrossRefGoogle ScholarPubMed
Chalmers, R. M., Ferguson, C., Cacciò, S., Gasser, R. B., Abs El-Osta, Y. G., Heijnen, L., Xiao, L., Elwin, K., Hadfield, S., Sinclair, M. and Stevens, M. (2005). Direct comparison for selected methods for genetic categorisation of Cryptosporidium parvum and Cryptosporidium hominis species. International Journal for Parasitology 35, 397–410.CrossRefGoogle ScholarPubMed
De la Fuente, R., García, A., Ruiz-Santa-Quiteria, J. A., Luzón, M., Cid, D., García, S., Orden, J. A. and Gómez-Bautista, M. (1998). Proportional morbidity rates of enteropathogens among diarrheic dairy calves in central Spain. Preventive Veterinary Medicine 36, 145–152.CrossRefGoogle ScholarPubMed
Elwin, K., Chalmers, R. M., Roberts, R., Guy, E. C. and Casemore, D. P. (2001). The modification of a rapid method for the identification of gene-specific polymorphisms in Cryptosporidium parvum, and its application to clinical and epidemiological investigations. Applied and Environmental Microbiology 67, 5581–5584.CrossRefGoogle ScholarPubMed
Fayer, R., Santín, M. and Trout, J. M. (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. Veterinary Parasitology 145, 260–266.CrossRefGoogle ScholarPubMed
Fayer, R., Santín, M. and Trout, J. M. (2008). Cryptosporidium ryanae n. sp. (Apicomplexa: Cryptosporidiidae) in cattle (Bos taurus). Veterinary Parasitology 156, 191–198.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, 105–112.CrossRefGoogle Scholar
Feltus, D. C., Giddings, C. W., Khaitsa, M. L. and McEvoy, J. M. (2008). High prevalence of Cryptosporidium bovis and the deer-like genotype in calves compared to mature cows in beef cow-calf operations. Veterinary Parasitology 151, 191–195.CrossRefGoogle ScholarPubMed
Feltus, D. C., Giddings, C. W., Schneck, B. L., Monson, T., Warshauer, D. and McEvoy, J. M. (2006). Evidence supporting zoonotic transmission of Cryptosporidium spp. in Wisconsin. Journal of Clinical Microbiology 44, 4303–4308.CrossRefGoogle ScholarPubMed
Feng, Y., Ortega, Y., He, G., Das, P., Xu, M., Zhang, X., Fayer, R., Gatei, W., Cama, V. and Xiao, L. (2007). Wide geographic distribution of Cryptosporidium bovis and the deer-like genotype in bovines. Veterinary Parasitology 144, 1–9.CrossRefGoogle ScholarPubMed
Geurden, T., Berkvens, D., Martens, C., Casaert, S., Vercruysse, J. and Claerebout, E. (2007). Molecular epidemiology with subtype analysis of Cryptosporidium in calves in Belgium. Parasitology 134, 1981–1987.Google ScholarPubMed
Glaberman, S., Moore, J. E., Lowery, C. J., Chalmers, R. M., Sulaiman, I., Elwin, K., Rooney, P. J., Millar, B. C., Dooley, J. S. G., Lal, A. A. and Xiao, L. (2002). Three drinking-water-associated cryptosporidiosis outbreaks, Northern Ireland. Emerging Infectious Diseases 8, 631–633.CrossRefGoogle ScholarPubMed
Heine, J. (1982). An easy technique for the demonstration of cryptosporidia in faeces. Zentralblatt für Veterinärmedizin B 29, 324–327.CrossRefGoogle Scholar
Langkjær, R. B., Vigre, H., Enemark, H. L. and Maddox-Hyttel, C. (2007). Molecular and phylogenetic characterization of Cryptosporidium and Giardia from pigs and cattle in Denmark. Parasitology 134, 339–350.CrossRefGoogle ScholarPubMed
Le Blancq, S. M., Khramtsov, N. V., Zamani, F., Upton, S. J. and Wu, T. W. (1997). Ribosomal RNA gene organization in Cryptosporidium parvum. Molecular and Biochemical Parasitology 90, 463–478.CrossRefGoogle ScholarPubMed
Llorente, M. T., Clavel, A., Goñi, M. P., Varea, M., Seral, C., Becerril, R., Suárez, L. and Gómez-Lus, R. (2007). Genetic characterization of Cryptosporidium species from humans in Spain. Parasitology International 56, 201–205.CrossRefGoogle ScholarPubMed
Misic, Z. and Abe, N. (2007). Subtype analysis of Cryptosporidium parvum isolates from calves on farms around Belgrade, Serbia and Montenegro, using the 60 kDa glycoprotein gene sequences. Parasitology 134, 351–358.CrossRefGoogle ScholarPubMed
Morrison, L. J., Mallon, M. E., Smith, H. V., MacLeod, A., Xiao, L. and Tait, A. (2008). The population structure of the Cryptosporidium parvum population in Scotland: A complex picture. Infection, Genetics and Evolution 8, 121–129.CrossRefGoogle ScholarPubMed
Navarro-I-Martínez, L., Bornay-Llinares, F. J., Rueda, C., Del Aguila, C., Da Silva, A. J., Oleaga, A., Ramajo, V., Fenoy, S. and Pieniazek, N. J. (2003). Molecular characterization of Cryptosporidium sp. from animals in Spain. The Journal of Eukaryotic Microbiology 50, S553–S554.CrossRefGoogle ScholarPubMed
O'Brien, E., McInnes, L. and Ryan, U. (2008). Cryptosporidium GP60 genotypes from humans and domesticated animals in Australia, North America and Europe. Experimental Parasitology 118, 118–121.CrossRefGoogle Scholar
Peng, M. M., Wilson, M. L., Holland, R. E., Meshnick, S. R., Lal, A. A. and Xiao, L. (2003). Genetic diversity of Cryptosporidium spp. in cattle in Michigan: implications for understanding the transmission dynamics. Parasitology Research 90, 175–180.CrossRefGoogle ScholarPubMed
Plutzer, J. and Karanis, P. (2007). Genotype and subtype analyses of Cryptosporidium isolates from cattle in Hungary. Veterinary Parasitology 146, 357–362.CrossRefGoogle ScholarPubMed
Quílez, J., Sánchez-Acedo, C., Del Cacho, E., Clavel, A. and Causapé, A. C. (1996). Prevalence of Cryptosporidium and Giardia infections in cattle in Aragón (northeastern Spain). Veterinary Parasitology 66, 139–146.CrossRefGoogle ScholarPubMed
Quílez, J., Torres, E., Chalmers, R. M., Hadfield, S. J., del Cacho, E. and Sánchez-Acedo, C. (2008). Cryptosporidium genotypes and subtypes in lambs and goat kids in Spain. Applied and Environmental Microbiology 74, 6026–6031. doi:10.1128/AEM.00606-08.CrossRefGoogle ScholarPubMed
Ryley, J. F., Meade, R., Hazelhurst, J. and Robinson, T. E. (1976). Methods in coccidiosis research: separation of oocysts from faeces. Parasitology 73, 311–326.CrossRefGoogle ScholarPubMed
Santín, M. and Trout, J. M. (2008). Livestock. In Cryptosporidium and Cryptosporidiosis (ed.Fayer, R. and Xiao, L.), pp. 451–483. CRC Press, Boca Ratón, Florida, USA.Google ScholarPubMed
Santín, M., Trout, J. M., Xiao, L., Zhou, L., Greiner, E. and Fayer, R. (2004). Prevalence and age-related variations of Cryptosporidium species and genotypes in dairy calves. Veterinary Parasitology 122, 103–117.CrossRefGoogle ScholarPubMed
Stantic-Pavlinic, M., Xiao, L., Glaberman, S., Lal, A. A., Orazen, T., Rataj-Verglez, A., Logar, J. and Berce, I. (2003). Cryptosporidiosis associated with animal contacts. Wiener Klinische Wochenschrift 115, 125–127.CrossRefGoogle ScholarPubMed
Strong, W. B., Gut, J. and Nelson, R. G. (2000). Cloning and sequence analysis of a highly polymorphic Cryptosporidium parvum gene encoding a 60-kilodalton glycoprotein and characterization of its 15- and 45-kilodalton zoite surface antigen products. Infection and Immunity 68, 4117–4134.CrossRefGoogle ScholarPubMed
Sulaiman, I. M., Hira, P. R., Zhou, L., Al-Ali, F. M., Al-Shelahi, F. A., Shweiki, H. M., Iqbal, J., Khalid, N. and Xiao, L. (2005). Unique endemicity of cryptosporidiosis in children in Kuwait. Journal of Clinical Microbiology 43, 2805–2809.CrossRefGoogle ScholarPubMed
Tanriverdi, S., Markovics, A., Arslan, O., Itik, A., Shkap, V. and Widmer, G. (2006). Emergence of distinct genotypes of Cryptosporidium parvum in structured host populations. Applied and Environmental Microbiology 72, 2507–2513.CrossRefGoogle ScholarPubMed
Thompson, H. P., Dooley, J. S. G., Kenny, J., McCoy, M., Lowery, C. J., Moore, J. E. and Xiao, L. (2007). Genotypes and subtypes of Cryptosporidium spp. in neonatal calves in Northern Ireland. Parasitology Research 100, 619–624.CrossRefGoogle ScholarPubMed
Trotz-Williams, L. A., Martin, D. S., Gatei, W., Cama, V., Peregrine, A. S., Martin, S. W., Nydam, D. V., Jamieson, F. and Xiao, L. (2006). Genotype and subtype analyses of Cryptosporidium isolates from dairy calves and humans in Ontario. Parasitology Research 99, 346–352.CrossRefGoogle ScholarPubMed
Wielinga, P. R., de Vries, A., van der Goot, T. H., Mank, T., Mars, M. H., Kortbeek, L. M. and van der Giessen, J. W. B. (2008). Molecular epidemiology of Cryptosporidium in humans and cattle in The Netherlands. International Journal for Parasitology 38, 809–817.CrossRefGoogle ScholarPubMed
Wu, Z., Nagano, I., Boonmars, T., Nakada, T. and Takahashi, Y. (2003). Intraspecies polymorphism of Cryptosporidium parvum revealed by PCR-restriction fragment polymorphism (RFLP) and RFLP-single-strand conformational polymorphism analyses. Applied and Environmental Microbiology 69, 4720–4726.CrossRefGoogle ScholarPubMed
Xiao, L., Escalante, L., Yang, C., Sulaiman, I., Escalante, A. A., Montali, R. J., Fayer, R. and Lal, A. A. (1999). Phylogenetic analysis of Cryptosporidium parasites based on the small-subunit rRNA gene locus. Applied and Environmental Microbiology 65, 1578–1583.CrossRefGoogle ScholarPubMed
Xiao, L. and Feng, Y. (2008). Zoonotic cryptosporidiosis. FEMS Immunology and Medical Microbiology 52, 309–323.CrossRefGoogle ScholarPubMed
Xiao, L. and Ryan, U. M. (2008). Molecular epidemiology. In Cryptosporidium and Cryptosporidiosis (ed.Fayer, R. and Xiao, L.), pp. 119–171. CRC Press, Boca Ratón, Florida, USA.Google ScholarPubMed
Xiao, L., Singh, A., Limor, J., Graczyk, T. K., Gradus, S. and Lal, A. (2001). Molecular characterisation of Cryptosporidium oocysts in samples of raw surface water and wastewater. Applied and Environmental Microbiology 67, 1097–1101.CrossRefGoogle ScholarPubMed
Xiao, L., Zhou, L., Santín, M., Yang, W. and Fayer, R. (2007). Distribution of Cryptosporidium parvum subtypes in calves in eastern United States. Parasitology Research 100, 701–706.CrossRefGoogle ScholarPubMed