Molecular and morphological characterization of Echinococcus in cervids from North America | Parasitology | Cambridge Core (original) (raw)

Abstract

Many issues concerning the taxonomy of Echinococcus have been resolved in recent years with the application of molecular tools. However, the status of Echinococcus maintained in transmission cycles involving cervid intermediate hosts remains to be determined. The recent characterization of the parasite from cervids in Finland has highlighted the paucity of data available, particularly that from North America. In this study, we have characterized a large number of Echinococcus isolates from cervids from Western Canada on the basis of morphology and molecular genetic techniques. Our results support earlier studies suggesting that Echinococcus of cervid origin is phenotypically and genetically distinct to Echinococcus maintained in domestic host assemblages, and also confirms that Echinococcus of cervid origin does not constitute a genetically homogeneous group. However, our data do not support the existence of 2 distinct genotypes (strains/subspecies) with separate geographical distributions. Our data appear to support the existence of only 1 species in cervids, but additional isolates from cervids and wolves in other endemic regions should be characterized before a final decision is made on the taxonomic status of Echinococcus in cervids.

References

Bergerud, A. T. andMercer, W. E. (1989).Caribou introductions in eastern North America.Wildlife Society Bulletin 17,111–120.Google Scholar

Bowles, J.,Blair, D. andMcManus, D. P. (1992).Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing.Molecular and Biochemical Parasitology 54,165–174.CrossRefGoogle Scholar

Bowles, J.,Blair, D. andMcManus, D. P. (1994).Molecular genetic characterisation of the cervid strain (“northern form”) of Echinococcus granulosus.Parasitology 109,215–221.CrossRefGoogle Scholar

Bowles, J.,Blair, D. andMcManus, D. P. (1995).A molecular phylogeny of the genus Echinococcus.Parasitology 110,317–328.CrossRefGoogle Scholar

Bowles, J. andMcManus, D. P. (1993 a).Rapid discrimination of Echinococcus species and strains using a polymerase chain reaction-based RFLP method.Molecular and Biochemical Parasitology 57,231–240.Google Scholar

Bowles, J. andMcManus, D. P. (1993 b).NADH dehydrogenase 1 gene sequences compared for species and strains of the genus Echinococcus.International Journal for Parasitology 23,969–972.Google Scholar

Castrodale, L. J.,Beller, M.,Wilson, J. F.,Schantz, P. M.,McManus, D. P.,Zhang, L. H.,Fallico, F. G. andSacco, F. D. (2002).Two atypical cases of cystic echinococcosis (Echinococcus granulosus) in Alaska, 1999.American Journal of Tropical Medicine and Hygiene 66,325–327.CrossRefGoogle Scholar

Cameron, T. W. M. (1960).The incidence and diagnosis of hydatid cyst in Canada Echinococcus granulosus var. canadensis.Parasitologia 2,381–390.Google Scholar

Cameron, T. W. M. andWebster, G. A. (1961).Studies in disease ecology.American Geographical Society 2,141–160.Google Scholar

Eckert, J.,Thompson, R. C. A.,Michael, S. A.,Kumaratilake, L. K. andEl-Sawah, H. M. (1989).Echinococcus granulosus of camel origin: development in dogs and parasite morphology.Parasitology Research 75,536–544.CrossRefGoogle Scholar

Harandi, F. M.,Hobbs, R. P.,Adams, P. J.,Mobedi, I.,Morgan-Ryan, U. M. andThompson, R. C. A. (2002).Molecular and morphological characterization of Echinococcus granulosus of human and animal origin in Iran.Parasitology 125,367–373.Google Scholar

Hobbs, R. P.,Lymbery, A. J. andThompson, R. C. A. (1990).Rostellar hook morphometry of Echinococcus granulosus (Batsch, 1786) from natural and experimental Australian hosts, and its implications for strain recognition.Parasitology 101,273–281.CrossRefGoogle Scholar

Joly, D. O. andMessier, F. (2004).The distribution of Echinococcus granulosus in moose: evidence for parasite-induced vulnerability to predation by wolves?Oecologia 140,586–590.Google Scholar

Kedra, A. H.,Swiderski, Z.,Tkach, V. V.,Dubinsky, P.,Pawlowski, Z.,Stefaniak, J. andPawlowski, J. (1999).Genetic analysis of Echinococcus granulosus from humans and pigs in Poland, Slovakia and Ukraine. A multicentre study.Acta Parasitologica 44,248–254.Google Scholar

Kumaratilake, L. M. (1982).Aspects of the speciation of Echinococcus granulosus in Australia. Ph.D. thesis, Murdoch University,Western Australia.

Kumaratilake, L. M.,Thompson, R. C. A. andEckert, J. (1986).Echinococcus granulosus of equine origin from different countries possess uniform morphological characteristics.International Journal for Parasitology 16,529–540.CrossRefGoogle Scholar

Lavikainen, A.,Lehtinen, M. J.,Meri, T.,Hirvelä-Koski, V. andMeri, S. (2003).Molecular genetic characterization of the Fennoscandian cervid strain, a new genotypic group (G10) of Echinococcus granulosus.Parasitology 127,207–215.CrossRefGoogle Scholar

Le, T. H.,Pearson, M. S.,Blair, D.,Dai, N.,Zhang, L. H. andMcManus, D. P. (2002).Complete mitochondrial genomes confirm the distinctiveness of horse-dog and sheep-dog strains of Echinococcus granulosus.Parasitology 124,97–112.CrossRefGoogle Scholar

Long, J. L. (2003).Introduced Mammals of the World. Their History, Distribution and Influence.CABI, Wallingford,Oxon, UK.

Lymbery, A. J. (1995).Genetic diversity, genetic differentiation and speciation in the genus Echinococcus Rudolph 1801. InEchinococcus and Hydatid Disease ( ed. Thompson, R. C. A. and Lymbery, A. J.), pp.51–87.CAB International, Wallingford,Oxon, UK.

Maniatis, T.,Fritsch, E. F. andSambrook, J. (1982).Molecular Cloning. A Laboratory Manual.Cold Spring Harbor Laboratory,Cold Spring Harbor, NY.

Mankhaeva, V. S. andShumilov, M. F. (1982).Development of Echinococcus granulosus in dogs working with deer. [In Russian].Nauchno-Tekhnicheskii Byulleten, Sibirskoe Otdelenie VASKhNIL 27,25–26.Google Scholar

McManus, D. P. andThompson, R. C. A. (2003).Molecular epidemiology of cystic echinococcosis.Parasitology 127,S37–S51.CrossRefGoogle Scholar

McManus, D. P.,Zhang, L.,Castrodale, L. J.,Le, T. H.,Pearson, M. andBlair, D. (2002).Short Report: Molecular genetic characterization of an unusually severe case of hydatid disease in Alaska caused by the cervid strain of Echinococcus granulosus.American Journal of Tropical Medicine and Hygiene 67,296–298.CrossRefGoogle Scholar

Morgan, U. M.,Constantine, C. C.,O'Donoghue, P.,Meloni, B. P.,O'Brien, P. A. andThompson, R. C. A. (1995).Molecular characterisation of Cryptosporidium isolates from humans and other animals using Random Amplified Polymorphic DNA analysis.American Journal of Tropical Medicine and Hygiene 52,559–564.CrossRefGoogle Scholar

Obwaller, A.,Schneider, R.,Walochnik, J.,Gollackner, B.,Deutz, A.,Janitschke, K.,Aspöck, H. andAuer, H. (2004).Echinococcus granulosus strain differentiation based on sequence heterogeneity in mitochondrial genes of cytochrome c oxidase-1 and NADH dehydrogenase-1.Parasitology 128,569–575.CrossRefGoogle Scholar

Pybus, M. J. (1990).Survey of hepatic and pulmonary helminths of wild cervids in Alberta, Canada.Journal of Wildlife Diseases 26,453–459.CrossRefGoogle Scholar

Rausch, R. L. (1967 a).A consideration of intraspecific categories in the genus Echinococcus rudolphi, 1801 (Cestoda: Taeniidae).Journal of Parasitology 53,484–491.Google Scholar

Rausch, R. L. (1967 b).On the ecology and distribution of Echinococcus spp. (Cestoda:Taeniidae), and characteristics of their development in the intermediate host.Annales of Parasitologie (Paris)42,19–63.Google Scholar

Rausch, R. L. (1986).Life-cycle patterns and geographic distribution of Echinococcus species. In_The Biology of_ Echinococcus and Hydatid Disease ( ed. Thompson, R. C. A.), pp.45–80.Allen and Unwin,London, UK.

Safronov, M. G. andIsakov, S. I. (1982).Subspecies of Echinococcus granulosus and E. multilocularis in Yakutiya [In Russian].Nauchno-Tekhnicheskii Byulleten, Sibirskoe Otdelenie VASKhNIL 9,29–31.Google Scholar

Safronov, M. G. andIsakov, S. I. (1984).Echinococcus granulosus and its varieties in Yakutiya [In Russian].Byulleten Vsesoyuznogo Instituta Gel'mintologii im K. I. Skryabina 37,58–59.Google Scholar

Schantz, P. M.,Chai, J.,Craig, P. S.,Eckert, J.,Jenkins, D. J.,Macpherson, C. N. L. andThakur, A. (1995).Epidemiology and control of hydatid disease. InEchinococcus and Hydatid Disease ( ed. Thompson, R. C. A. and Lymbery, A. J.), pp.233–331.CAB International, Wallingford,Oxon, UK.

Sweatman, G. K. (1964).The significance of the artificial introduction of reindeer (Rangifer tarandus) and moose (Alces alces) in the spread of hydatid disease (Echinococcus granulosus).Annals of Tropical Medicine and Parasitology 58,307–314.CrossRefGoogle Scholar

Sweatman, G. K. andWilliams, R. J. (1963).Comparative studies on the biology and morphology of Echinococcus granulosus from domestic livestock, moose and reindeer.Parasitology 53,339–390.CrossRefGoogle Scholar

Tajima, F. andNei, M. (1984).Estimation of evolutionary distance between nucleotide sequences.Molecular Biology and Evolution 1,269–285.Google Scholar

Thompson, J. D.,Higgins, D. G. andGibson, T. J. (1994).CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice.Nucleic Acids Research 22,4673–4680.CrossRefGoogle Scholar

Thompson, R. C. A. (2001).Echinococcosis. In_Principles and Practice of Clinical Parasitology_ ( ed. Gillespie, S. H. and Pearson, R. D.), pp.595–612.Wiley, Sussex,CrossRef

Thompson, R. C. A.,Kumaratilake, L. M. andEckert, J. (1984).Observations on Echinococcus granulosus of cattle origin in Switzerland.International Journal for Parasitology 14,283–291.CrossRefGoogle Scholar

Thompson, R. C. A. andLymbery, A. J. (1988).The nature, extent and significance of variation within the genus Echinococcus.Advances in Parasitology 27,210–263.CrossRefGoogle Scholar

Thompson, R. C. A.,Lymbery, A. J. andConstantine, C. C. (1995).Variation in Echinococcus: towards a taxonomic revision of the genus.Advances in Parasitology 35,145–176.CrossRefGoogle Scholar

Thompson, R. C. A. andMcManus, D. P. (2001).Aetiology: parasites and life cycles. In_Manual on_ Echinococcus in Humans and Animals: a Public Health Problem of Global Concern ( ed. Eckert, J., Gemmell, M. A., Meslin, F.-X. and Pawlowski, Z. S.), pp.1–19. WHO/OIE,Paris.World Health Organization, Geneva.

Thompson, R. C. A. andMcManus, D. P. (2002).Towards a taxonomic revision of the genus Echinococcus.Trends in Parasitology 18,452–445.CrossRefGoogle Scholar

Van de Peer, Y. andDe Wachter, R. (1993).TREECON: a software package for the construction and drawing of evolutionary trees.Computational Applications for Biosciences 9,177–182.CrossRefGoogle Scholar

Webster, G. A. andCameron, T. W. M. (1961).Observations on experimental infections with Echinococcus in rodents.Canadian Journal of Zoology 39,877–891.CrossRefGoogle Scholar

Wilson, J. F.,Diddams, A. C. andRausch, R. L. (1968).Cystic hydatid disease in Alaska: a review of 101 autochthonous cases of Echinococcus granulosus infection.American Review of Respiratory Diseases 98,1–15.Google Scholar

Xiao, N.,Qiu, J.,Nakao, M.,Tiaoying, L.,Yang, W.,Chen, X.,Schantz, P. M.,Craig, P. S. andIto, A. (2005).Echinococcus shiquicus n. sp., a taeniid cestode from Tibetan fox and plateau pika in China.International Journal for Parasitology 35,693–701.Google Scholar