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Current status of the genetics and molecular taxonomy of Echinococcus species

Published online by Cambridge University Press:  11 June 2013

D. P. McMANUS
D. P. McMANUS*
Affiliation:
Molecular Parasitology Laboratory, Queensland Institute of Medical Research, Brisbane, Queensland 4006, Australia
*
*Corresponding author. Molecular Parasitology Laboratory, Infectious Diseases Division, Queensland Institute of Medical Research, Herston, Brisbane, Queensland 4006, Australia. Tel: +61 7 362 0401. Fax: +61 7 3362 0104. E-mail: donm@qimr.edu.au
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Summary

The taxonomy of Echinococcus has long been controversial. Based mainly on differences in morphology and host-parasite specificity characteristics, 16 species and 13 subspecies were originally described. Subsequently, most of these taxa were regarded as synonyms for Echinococcus granulosus and only 4 valid species were recognised: E. granulosus; E. multilocularis; E. oligarthrus and E. vogeli. But, over the past 50 years, laboratory and field observations have revealed considerable phenotypic variability between isolates of Echinococcus, particularly those of E. granulosus, which include differences in: morphology in both larval and adult stages, development in vitro and in vivo, host infectivity and specificity, chemical composition, metabolism, proteins and enzymes, pathogenicity and antigenicity. The application of molecular tools has revealed differences in nucleic acid sequences that reflect this phenotypic variation and the genetic and phenotypic characteristics complement the previous observations made by the descriptive parasitologists many years ago. The fact that some of these variants or strains are poorly or not infective to humans has resulted in a reappraisal of the public health significance of Echinococcus in areas where such variants occur. A revised taxonomy for species in the Echinococcus genus has been proposed that is generally accepted, and is based on the new molecular data and the biological and epidemiological characteristics of host-adapted species and strains.

Keywords

Echinococcusstraingeneticsmolecular taxonomymitochondrial genomephylogenytaxonomic revision

Information

Type
Research Article
Information
Parasitology , Volume 140 , Special Issue 13: Control of cestode zoonoses in Asia: role of basic and applied science , November 2013 , pp. 1617 - 1623
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Alvarez Rojas, C. A., Gauci, C. G., Nolan, M. J., Harandi, M. F. and Lightowlers, M. W. (2012). Characterization of the eg95 gene family in the G6 genotype of Echinococcus granulosus. Molecular and Biochemical Parasitology 183, 115–121.CrossRefGoogle ScholarPubMed
Boubaker, G., Macchiaroli, N., Prada, L., Cucher, M. A., Rosenzvit, M. C., Ziadinov, I., Deplazes, P., Saarma, U., Babba, H., Gottstein, B. and Spiliotis, M. (2013). A multiplex PCR for the simultaneous detection and genotyping of the Echinococcus granulosus complex. PLoS Neglected Tropical Diseases 7, e2017.CrossRefGoogle ScholarPubMed
Bowles, J., Blair, D. and McManus, D. P. (1992). Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165–173.CrossRefGoogle ScholarPubMed
Bowles, J., Blair, D. and McManus, D. P. (1995). A molecular phylogeny of the genus Echinococcus. Parasitology 110, 317–328.CrossRefGoogle ScholarPubMed
Bowles, J. and McManus, D. P. (1993). Rapid discrimination of Echinococcus species and strains using a polymerase chain reaction-based RFLP method. Molecular and Biochemical Parasitology 57, 231–239.CrossRefGoogle ScholarPubMed
Chow, C., Gauci, C. G., Vural, G., Jenkins, D. J., Heath, D. D., Rosenzvit, M. C., Harandi, M. F. and Lightowlers, M. W. (2008). Echinococcus granulosus: variability of the host-protective EG95 vaccine antigen in G6 and G7 genotypic variants. Experimental Parasitology 119, 499–505.CrossRefGoogle ScholarPubMed
Dinkel, A., Njoroge, E. M., Zimmermann, A., Wälz, M., Zeyhle, E., Elmahdi, I. E., Mackenstedt, U. and Romig, T. (2004). A PCR system for detection of species and genotypes of the Echinococcus granulosus-complex, with reference to the epidemiological situation in eastern Africa. International Journal for Parasitology 34, 645–653.CrossRefGoogle Scholar
Eckert, J. and Thompson, R. C. (1997). Intraspecific variation of Echinococcus granulosus and related species with emphasis on their infectivity to humans. Acta Tropica 64, 19–34.CrossRefGoogle ScholarPubMed
Gauci, C., Heath, D., Chow, C. and Lightowlers, M. W. (2005). Hydatid disease: vaccinology and development of the EG95 recombinant vaccine. Expert Review of Vaccines 4, 103–112.CrossRefGoogle ScholarPubMed
Haag, K. L., Zaha, A., Araújo, A. M. and Gottstein, B. (1997). Reduced genetic variability within coding and non-coding regions of the Echinococcus multilocularis genome. Parasitology 115, 521–529.CrossRefGoogle ScholarPubMed
Hatch, C. and Smyth, J. D. (1975). Attempted infection of sheep with Echinococcus granulosus equinus. Research in Veterinary Science 19, 340.CrossRefGoogle ScholarPubMed
Hüttner, M., Nakao, M., Wassermann, T., Siefert, L., Boomker, J. D., Dinkel, A., Sako, Y., Mackenstedt, U., Romig, T. and Ito, A. (2008). Genetic characterization and phylogenetic position of Echinococcus felidis (Cestoda: Taeniidae) from the African lion. International Journal for Parasitology 38, 861–868.CrossRefGoogle ScholarPubMed
Hüttner, M., Siefert, L., Mackenstedt, U., Romig, T. A. (2009). A survey of Echinococcus species in wild carnivores and livestock in East Africa. International Journal for Parasitology 39, 1269–1276.CrossRefGoogle ScholarPubMed
Knapp, J., Nakao, M., Yanagida, T., Okamoto, M., Saarma, U., Lavikainen, A. and Ito, A. (2011). Phylogenetic relationships within Echinococcus and Taenia tapeworms (Cestoda: Taeniidae): an inference from nuclear protein-coding genes. Molecular Phylogenetics and Evolution 61, 628–638.CrossRefGoogle ScholarPubMed
Lavikainen, A., Lehtinen, M. J., Agren, E. and Meri, S. (2005). Phylogeny of the Fennoscandian cervid strain of Echinococcus granulosus. Bulletin of the Scandinavian-Baltic Society for Parasitology 14, 92–98.Google Scholar
Lavikainen, A., Lehtinen, M. J., Meri, T., Hirvelä-Koski, V. and Meri, 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. and McManus, D. P. (2002). Complete mitochondrial genomes confirm the distinctiveness of the horse-dog and sheep-dog strains of Echinococcus granulosus. Parasitology 124, 97–112.CrossRefGoogle ScholarPubMed
Le Riche, M. and Sewell, M. H. (1978). Identification of Echinococcus granulosus strains by enzyme electrophoresis. Research in Veterinary Science 25, 247–248.CrossRefGoogle ScholarPubMed
Lopez-Neyra, C. R. and Soler Planas, M. A. (1943). Revision del genero Echinococcus Rud y description de una especie nuéva Parasita intestinal del porro en Almeria. Revista Ibérica Parasitologia 3, 169–194.Google Scholar
Macpherson, C. N. and Smyth, J. D. (1985). In vitro culture of the strobilar stage of Echinococcus granulosus from protoscoleces of human, camel, cattle, sheep and goat origin from Kenya and buffalo origin from India. International Journal for Parasitology 15, 137–140.CrossRefGoogle ScholarPubMed
Macpherson, C. N. L. and McManus, D. P. (1982). A comparative study of Echinococcus granulosus from human and animal hosts in Kenya using isoelectric focusing and isoenzyme analysis. International Journal for Parasitology 12, 515–521.CrossRefGoogle ScholarPubMed
McManus, D. P. (1981). A biochemical study of adult and cystic stages of Echinococcus granulosus of human and animal origin from Kenya. Journal of Helminthology 55, 21–27.CrossRefGoogle ScholarPubMed
McManus, D. P., Knight, M. and Simpson, A. J. (1985). Isolation and characterisation of nucleic acids from the hydatid organisms, Echinococcus spp. (Cestoda). Molecular and Biochemical Parasitology 16, 251–266.CrossRefGoogle ScholarPubMed
McManus, D. P. and Rishi, A. K. (1989). Genetic heterogeneity within Echinococcus granulosus: isolates from different hosts and geographical areas characterized with DNA probes. Parasitology 99, 17–29.CrossRefGoogle ScholarPubMed
McManus, D. P. and Simpson, A. J. (1985). Identification of the Echinococcus (hydatid disease) organisms using cloned DNA markers. Molecular and Biochemical Parasitology 17, 71–78.CrossRefGoogle ScholarPubMed
McManus, D. P. and Smyth, J. D. (1978). Differences in the chemical composition and carbohydrate metabolism of Echinococcus granulosus (horse and sheep strains) and E. multilocularis. Parasitology 77, 103–109.CrossRefGoogle ScholarPubMed
McManus, D. P. and Smyth, J. D. (1979). Isoelectric focusing of some enzymes from Echinococcus granulosus (horse and sheep strains) and E. multilocularis. Transactions of the Royal Society of Tropical Medicine and Hygiene 73, 259–265.CrossRefGoogle ScholarPubMed
McManus, D. P. and Smyth, J. D. (1982). Intermediary carbohydrate metabolism in protoscoleces of Echinococcus granulosus (horse and sheep strains) and E. multilocularis. Parasitology 84, 351–366.CrossRefGoogle ScholarPubMed
McManus, D. P. and Thompson, R. C. (2003). Molecular epidemiology of cystic echinococcosis. Parasitology 127 (Suppl), S37–S51.CrossRefGoogle ScholarPubMed
Moks, E., Jõgisalu, I., Valdmann, H. and Saarma, U. (2008). First report of Echinococcus granulosus G8 in Eurasia and a reappraisal of the phylogenetic relationships of ‘genotypes’ G5–G10. Parasitology 135, 647–654.CrossRefGoogle Scholar
Moro, P. and Schantz, P. M. (2009). Echinococcosis: a review. International Journal of Infectious Diseases 13, 125–133.CrossRefGoogle ScholarPubMed
Nakao, M., McManus, D. P., Schantz, P. M., Craig, P. S. and Ito, A. (2007). A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology 134, 713–722.CrossRefGoogle ScholarPubMed
Nakao, M., Xiao, N., Okamoto, M., Yanagida, T., Sako, Y. and Ito, A. (2009). Geographic pattern of genetic variation in the fox tapeworm Echinococcus multilocularis. Parasitology International 58, 384–389.CrossRefGoogle ScholarPubMed
Nakao, M., Yanagida, T., Okamoto, M., Knapp, J., Nkouawa, A., Sako, Y. and Ito, A. (2010). State of-the-art Echinococcus and Taenia: phylogenetic taxonomy of human-pathogenic tapeworms and its application to molecular diagnosis. Infection, Genetics and Evolution 10, 444–452.CrossRefGoogle ScholarPubMed
Ortlepp, R. J. (1934). Echinococcus in dogs from Pretoria and vicinity. Onderstepoort Journal of Veterinary Science 3, 97–108.Google Scholar
Pednekar, R. P., Gatne, M. L., Thompson, R. C. and Traub, R. J. (2009). Molecular and morphological characterisation of Echinococcus from food producing animals in India. Veterinary Parasitology 165, 58–65.CrossRefGoogle ScholarPubMed
Rausch, R. L. (1967). A consideration of infraspecific categories in the genus Echinococcus Rudolphi, 1801(Cestoda: Taeniidae). Journal of Parasitology 53, 484–491.CrossRefGoogle ScholarPubMed
Rausch, R. L. and Bernstein, J. J. (1972). Echinococcus vogeli sp. n. (Cestoda: Taeniidae) from the bush dog, Speothos venaticus (Lund). Zeitschrift für Tropenmedizin und Parasitologie 23, 25–34.Google Scholar
Rinder, H., Rausch, R. L., Takahashi, K., Kopp, H., Thomschke, A. and Löscher, T. (1997). Limited range of genetic variation in Echinococcus multilocularis. Journal of Parasitology 83, 1045–1050.CrossRefGoogle ScholarPubMed
Saarma, U., Jõgisalu, I., Moks, E., Varcasia, A., Lavikainen, A., Oksanen, A., Simsek, S., Andresiuk, V., Denegri, G., González, L. M., Ferrer, E., Gárate, T., Rinaldi, L. and Maravilla, P. (2009). A novel phylogeny for the genus Echinococcus, based on nuclear data, challenges relationships based on mitochondrial evidence. Parasitology 136, 317–328.CrossRefGoogle ScholarPubMed
Smyth, J. D. (1977). Strain differences in Echinococcus granulosus, with special reference to the status of equine hydatidosis in the United Kingdom. Transactions of the Royal Society for Tropical Medicine and Hygiene 71, 93–100.CrossRefGoogle Scholar
Smyth, J. D. and Davies, Z. (1974). Occurrence of physiological strains of Echinococcus granulosus demonstrated by in vitro culture of protoscoleces from sheep and horse hydatid cysts. International Journal for Parasitology 4, 443–445.CrossRefGoogle ScholarPubMed
Smyth, J. D. and Smyth, M. M. (1964). Natural and experimental hosts of Echinococcus granulosus and E. multilocularis, with comments on the genetics of speciation in the genus Echinococcus. Parasitology 54, 493–514.CrossRefGoogle Scholar
Thompson, R. C. (2008). The taxonomy, phylogeny and transmission of Echinococcus. Experimental Parasitology 119, 439–446.CrossRefGoogle ScholarPubMed
Thompson, R. C. and McManus, D. P. (2002). Towards a taxonomic revision of the genus Echinococcus. Trends in Parasitology 18, 452–457.CrossRefGoogle ScholarPubMed
Thompson, R. C. A. (2001). Echinococcosis. In Principles and Practice of Clinical Parasitology (ed. Gillespie, S. H. and Pearson, R. D.), pp. 595–612, John Wiley, New York.Google Scholar
Thompson, R. C. A. and Lymbery, A. J. (1988). The nature, extent and significance of variation within the genus Echinococcus. Advances in Parasitology 27, 209–258.CrossRefGoogle ScholarPubMed
Thompson, R. C. A., Lymbery, A. J. and Constantine, C. C. (1995). Variation in Echinococcus: towards a taxonomic revision of the genus. Advances in Parasitology 35, 145–176.CrossRefGoogle ScholarPubMed
Verster, A. J. M. (1965). Review of Echinococcus species in South Africa. Onderstepoort Journal of Veterinary Research 32, 7–118.Google Scholar
Wachira, T. M., Bowles, J., Zeyhle, E. and McManus, D. P. (1993). Molecular examination of the sympatry and distribution of sheep and camel strains of Echinococcus granulosus in Kenya. American Journal of Tropical Medicine and Hygiene 48, 473–479.CrossRefGoogle ScholarPubMed
Williams, R. J. and Sweatman, G. K. (1963). On the transmission, biology and morphology of Echinococcus granulosus equinus, a new subspecies of hydatid tapeworm in horses in Great Britain. Parasitology 53, 391–407.CrossRefGoogle ScholarPubMed
Xiao, N., Qiu, J., Nakao, M., Li, T., Yang, W., Chen, X., Schantz, P. M., Craig, P. S. and Ito, A. (2005). Echinococcus shiquicus n. sp., a taeniid cestode from Tibetan fox and plateau pika in China. International Journal for Parasitology 35, 693–701.CrossRefGoogle Scholar
Xiao, N., Qiu, J., Nakao, M., Li, T., Yang, W., Chen, X., Schantz, P. M., Craig, P. S. and Ito, A. (2006). Echinococcus shiquicus, a new species from the Qinghai-Tibet plateau region of China: discovery and epidemiological implications. Parasitology International 55 (Suppl), S233–S236.CrossRefGoogle ScholarPubMed
Yang, Y. R., Rosenzvit, M. C., Zhang, L. H., Zhang, J. Z., McManus, D. P. (2005). Molecular study of Echinococcus in west-central China. Parasitology 131, 547–555.CrossRefGoogle ScholarPubMed