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Molecular identification of Cryptosporidium parvum from avian hosts

Published online by Cambridge University Press:  14 January 2011

J. X. QUAH
Affiliation:
International Medical University, 126, Jalan 19/155B, Bukit Jalil, 57000 Kuala Lumpur, Malaysia
S. AMBU*
Affiliation:
International Medical University, 126, Jalan 19/155B, Bukit Jalil, 57000 Kuala Lumpur, Malaysia
Y. A. L. LIM
Affiliation:
Department of Parasitology, Faculty of Medicine, University of Malaya, 50603 Kuala Lumpur, Malaysia
M. A. K. MAHDY
Affiliation:
Department of Parasitology, Faculty of Medicine, University of Malaya, 50603 Kuala Lumpur, Malaysia
J. W. MAK
Affiliation:
International Medical University, 126, Jalan 19/155B, Bukit Jalil, 57000 Kuala Lumpur, Malaysia
*
*Corresponding author: International Medical University, 126, Jalan 19/155B, Bukit Jalil, 57000 Kuala Lumpur, Malaysia. E-mail: stephen_ambu@imu.edu.my

Summary

Cryptosporidium species are protozoan parasites that infect humans and a wide variety of animals. This study was aimed at identifying Cryptosporidium species and genotypes isolated from avian hosts. A total of 90 samples from 37 different species of birds were collected throughout a 3-month period from April 2008 to June 2008 in the National Zoo of Kuala Lumpur, Malaysia. Prior to molecular characterization, all samples were screened for Cryptosporidium using a modified Ziehl-Neelsen staining technique. Subsequently samples were analysed with nested-PCR targeting the partial SSU rRNA gene. Amplicons were sequenced in both directions and used for phylogenetic analysis using Neighbour-Joining and Maximum Parsimony methods. Although 9 (10%) samples were positive for Cryptosporidium via microscopy, 8 (8·9%) produced amplicons using nested PCR. Phylogenetic trees identified all the isolates as Cryptosporidium parvum. Although C. parvum has not been reported to cause infection in birds, and the role of birds in this study was postulated mainly as mechanical transporters, these present findings highlight the significant public health risk posed by birds that harbour the zoonotic species of Cryptosporidium.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 33893402.CrossRefGoogle ScholarPubMed
Cama, V. A., Bern, C., Sulaiman, I. M., Gilman, R. H., Ticona, E., Vivar, A., Kawai, V., Vargas, D., Zhou, L. and Xiao, L. (2003). Cryptosporidium species and genotypes in HIV-positive patients in Lima, Peru. Journal of Eukaryotic Microbiology 50, (Suppl.) 531533.CrossRefGoogle ScholarPubMed
Clark, D. P. (1999). New insights into human cryptosporidiosis. Clinical Microbiology Review 12, 554563.CrossRefGoogle ScholarPubMed
Current, W. L., Upton, S. J. and Haynes, T. B. (1986). The life cycle of Cryptosporidium baileyi n. sp. (Apicomplexa, Cryptosporidiidae) infecting chickens. Journal of Protozoology 33, 289296.CrossRefGoogle Scholar
Darabus, G. and Olariu, R. (2003). The homologous and interspecies transmission of Cryptosporidium parvum and Cryptosporidium meleagridis. Polish Journal of Veterinary Science 6, 225228.Google Scholar
Dieter, R. A. Jr., Dieter, RS., Dieter, R. A. 3rd and Gulliver, G. (2001). Zoonotic diseases: health aspects of Canadian geese. International Journal of Circumpolar Health 60, 676684.CrossRefGoogle ScholarPubMed
Fayer, R. (2010). Taxonomy and species delimitation in Cryptosporidium. Experimental Parasitology 124, 9097.CrossRefGoogle ScholarPubMed
Fayer, R., Santín, M. and Macarisin, D. (2010). Cryptosporidium ubiquitum n. sp. in animals and humans. Veterinary Parasitology 172, 2332.CrossRefGoogle Scholar
Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 9.CrossRefGoogle ScholarPubMed
Graczyk, T. K., Cranfield, M. R., Fayer, R., Trout, J. and Goodale, H. J. (1997). Infectivity of Cryptosporidium parvum oocysts is retained upon intestinal passage through a migratory water-fowl species (Canada goose, Branta canadensis). Tropical Medicine and International Health 2, 341347.CrossRefGoogle ScholarPubMed
Graczyk, T. K., Fayer, R., Trout, J. M., Lewis, E. J., Farley, C. A., Sulaiman, I. and Lal, A. A. (1998). Giardia sp. cysts and infectious Cryptosporidium parvum oocysts in the feces of migratory Canada geese (Branta canadensis). Applied Environmental Microbiology 64, 27362738.CrossRefGoogle ScholarPubMed
Graczyk, T. K., Majewska, A. C. and Schwab, K. J. (2008). The role of birds in dissemination of human waterborne enteropathogens. Trends in Parasitology 24, 5559.CrossRefGoogle ScholarPubMed
Insulander, M., Lebbad, M., Stenstrom, T. A. and Svenungsson, B. (2005). An outbreak of cryptosporidiosis associated with exposure to swimming pool water. Scandinavian Journal of Infectious Diseases 37, 354360.CrossRefGoogle ScholarPubMed
Jellison, K. L., Distel, D. L., Hemond, H. F. and Schauer, D. B. (2004). Phylogenetic analysis of the hypervariable region of the 18S rRNA gene of Cryptosporidium oocysts in feces of Canada geese (Branta canadensis): evidence for five novel genotypes. Applied Environmental Microbiology 70, 452458.CrossRefGoogle ScholarPubMed
Johnson, D. W., Pieniazek, N. J., Griffin, D. W., Misener, L. and Rose, J. B. (1995). Development of a PCR protocol for sensitive detection of Cryptosporidium oocysts in water samples. Applied Environmental Microbiology 61, 38493855.CrossRefGoogle ScholarPubMed
Kassa, H., Harrington, B. J. and Bisesi, M. S. (2004). Cryptosporidiosis: a brief literature review and update regarding Cryptosporidium in feces of Canada geese (Branta canadensis). Journal of Environmental Health 66, 3440.Google ScholarPubMed
Katsumata, T., Hosea, D., Ranuh, I. G., Uga, S., Yanagi, T. and Kohno, S. (2000). Short report: possible Cryptosporidium muris infection in humans. American Journal of Tropical Medicine and Hygiene 62, 7072.CrossRefGoogle ScholarPubMed
Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111120.CrossRefGoogle ScholarPubMed
Kirschner, A. K., Zechmeister, T. C., Kavka, G. G., Beiwl, C., Herzig, A., Mach, R. L. and Farnleitner, A. H. (2004). Integral strategy for evaluation of fecal indicator performance in bird-influenced saline inland waters. Applied Environmental Microbiology 70, 73967403.CrossRefGoogle ScholarPubMed
Kuhn, R. C., Rock, C. M. and Oshima, K. H. (2002). Occurrence of Cryptosporidium and Giardia in wild ducks along the Rio Grande River valley in southern New Mexico. Applied Environmental Microbiology 68, 161165.CrossRefGoogle Scholar
Lindsay, D. S., Blagburn, B. L. and Ernest, J. A. (1987). Experimental Cryptosporidium parvum infections in chickens. Journal of Parasitology 73, 242244.CrossRefGoogle ScholarPubMed
MacKenzie, W. R., Hoxie, N. J., Proctor, M. E., Gradus, M. S., Blair, K. A., Peterson, D. E., Kazmierczak, J. J., Addiss, D. G., Fox, K. R., Rose, J. B. and David, J. P. (1994). A massive outbreak in Milwaukee of cryptosporidium infection transmitted through the public water supply. New England Journal of Medicine 331, 161167.CrossRefGoogle Scholar
Mahat, M. S. (2006). Cryptosporidium among bird handlers in Zoo Negara Kuala Lumpur. Department of Molecular Medicine, Faculty of Medicine, University Malaya, Kuala Lumpur, Malaya.Google Scholar
Majewska, A. C., Graczyk, T. K., Slodkowicz-Kowalska, A., Tamang, L., Jedrzejewski, S., Zduniak, P., Solarczyk, P., Nowosad, A. and Nowosad, P. (2009). The role of free-ranging, captive, and domestic birds of Western Poland in environmental contamination with Cryptosporidium parvum oocysts and Giardia lamblia cysts. Parasitology Research 104, 10931099.CrossRefGoogle ScholarPubMed
Marshall, M. M., Naumovitz, D., Ortega, Y. and Sterling, C. R. (1997). Waterborne protozoan pathogens. Clinical Microbiology Review, 10, 6785.CrossRefGoogle ScholarPubMed
Matos, O., Alves, M., Xiao, L., Cama, V. and Antunes, F. (2004). Cryptosporidium felis and C. meleagridis in persons with HIV, Portugal. Emerging Infectious Disease Journal 10, 22562257.CrossRefGoogle Scholar
Messner, M. J., Chappell, C. L. and Okhuysen, P. C. (2001). Risk assessment for Cryptosporidium: a hierarchical Bayesian analysis of human dose response data. Water Research 35, 39343940.CrossRefGoogle ScholarPubMed
Morgan, U. M., Monis, P. T., Xiao, L., Limor, J., Sulaiman, I., Raidal, S., O'donoghue, P., Gasser, R., Murray, A., Fayer, R., Blagburn, B. L., Lal, A. A. and Thompson, R. C. (2001). Molecular and phylogenetic characterisation of Cryptosporidium from birds. International Journal for Parasitology 31, 289296.CrossRefGoogle ScholarPubMed
Nei, M. and Kumar, S. (2000). Molecular Evolution and Phylogenetics. Oxford University Press, New York, USA.CrossRefGoogle Scholar
Nichols, R. A., Campbell, B. M. and Smith, H. V. (2003). Identification of Cryptosporidium spp. oocysts in United Kingdom noncarbonated natural mineral waters and drinking waters by using a modified nested PCR-restriction fragment length polymorphism assay. Applied Environmental Microbiology 69, 41834189.CrossRefGoogle ScholarPubMed
Okhuysen, P. C., Chappell, C. L., Crabb, J. H., Sterling, C. R. and Dupont, H. L. (1999). Virulence of three distinct Cryptosporidium parvum isolates for healthy adults. Journal of Infectious Diseases 180, 12751281.CrossRefGoogle ScholarPubMed
Okhuysen, P. C., Rich, S. M., Chappell, C. L., Grimes, K. A., Widmer, G., Feng, X. and Tzipori, S. (2002). Infectivity of a Cryptosporidium parvum isolate of cervine origin for healthy adults and interferon-gamma knockout mice. Journal of Infectious Diseases 185, 13201325.CrossRefGoogle ScholarPubMed
Palkovic, L. and Marousek, V. (1989). The pathogenicity of Cryptosporidium parvum Tyzzer, 1912 and C. baileyi Current, Upton et Haynes, 1986 for chickens. Folia Parasitologica (Praha), 36, 209217.Google Scholar
Pavlásek, I. (1999). Cryptosporidia: biology, diagnosis, host spectrum specificity and the environment. Klinika Mikrobiologie a Infekcni Lekarstvi 3, 290301.Google Scholar
Plutzer, J. and Karanis, P. (2009). Genetic polymorphism in Cryptosporidium species: an update. Veterinary Parasitology 165, 187199.CrossRefGoogle ScholarPubMed
Plutzer, J. and Tomor, B. (2009). The role of aquatic birds in the environmental dissemination of human pathogenic Giardia duodenalis cysts and Cryptosporidium oocysts in Hungary. Parasitology International 58, 227231.CrossRefGoogle ScholarPubMed
Rohela, M., Lim, Y. A., Jamaiah, I., Khadijah, P. Y., Laang, S. T., Nazri, M. H. and Nurulhuda, Z. (2005). Occurrence of Cryptosporidium oocysts in Wrinkled Hornbill and other birds in the Kuala Lumpur National Zoo. Southeast Asian Journal of Tropical Medicine and Public Health 36 (Suppl 4), 3440.Google Scholar
Ryan, U. (2010). Cryptosporidium in birds, fish and amphibians. Experimental Parasitology 124, 113120.CrossRefGoogle ScholarPubMed
Ryan, U., Xiao, L., Read, C., Zhou, L., Lal, A. A. and Pavlasek, I. (2003). Identification of novel Cryptosporidium genotypes from the Czech Republic. Applied Environmental Microbiology 69, 43024307.CrossRefGoogle ScholarPubMed
Slavin, D. (1955). Cryptosporidium meleagridis (sp. nov.). Journal of Comparative Pathology 65, 262266.CrossRefGoogle ScholarPubMed
Sreter, T. and Varga, I. (2000). Cryptosporidiosis in birds--a review. Veterinary Parasitology 87, 261279.CrossRefGoogle ScholarPubMed
Traversa, D. (2010). Evidence for a new species of Cryptosporidium infecting tortoises: Cryptosporidium ducismarci. Parasite & Vectors 3, 21, 14.Google Scholar
Xiao, L. and Fayer, R. (2008). Molecular characterisation of species and genotypes of Cryptosporidium and Giardia and assessment of zoonotic transmission. International Journal for Parasitology 38, 12391255.CrossRefGoogle ScholarPubMed
Zhou, L., Kassa, H., Tischler, M. L. and Xiao, L. (2004). Host-adapted Cryptosporidium spp. in Canada geese (Branta canadensis). Applied Environmental Microbiology 70, 42114215.CrossRefGoogle ScholarPubMed