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Echinococcus, Giardia and Cryptosporidium: observational studies challenging accepted dogma

Published online by Cambridge University Press:  14 April 2009

R. C. A. THOMPSON*
Affiliation:
World Health Organization Collaborating Centre for the Molecular Epidemiology of Parasitic Infections, School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, WA 6150, Australia
*
*Tel: +61 08 9360 2466. Fax: +61 08 9310 4144. E-mail: [email protected]

Summary

The development of in vitro culture systems that allow the maintenance, and support the development of Echinococcus, Giardia and Cryptosporidium in the laboratory have had a significant impact on their biology and taxonomy and the epidemiology of infections they cause. This short retrospective review demonstrates how radical shifts in our understanding have occurred as a result of being able to grow these organisms in culture, and how molecular tools have helped in the interpretation of such research that often reflects the observations of earlier workers.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Andrews, R. H., Mayrhofer, G., Chilton, N. B., Boreham, P. F. and Grimmond, T. R. (1992). Changes in allozyme pattern of the protozoan parasite Giardia intestinalis. International Journal for Parasitology 22, 403406.CrossRefGoogle ScholarPubMed
Barta, J. R. and Thompson, R. C. A. (2006). What is Cryptosporidium? – Time to reappraise its biology, taxonomy and phylogenetic affinities. Trends in Parasitology 22, 463468.CrossRefGoogle Scholar
Binz, N., Thompson, R. C. A., Meloni, B. P. and Lymbery, A. J. (1991). A simple method for cloning Giardia duodenalis from culture and fecal samples. Journal of Parasitology 77, 627631.CrossRefGoogle ScholarPubMed
Binz, N., Thompson, R. C. A., Lymbery, A. J. and Hobbs, R. P. (1992). Comparative studies on the growth dynamics of two genetically distinct isolates of Giardia duodenalis in vitro. International Journal for Parasitology 22, 195202.CrossRefGoogle ScholarPubMed
Borowski, H., Clode, P. L. and Thompson, R. C. A. (2008). Active invasion and/or encapsulation? A reappraisal of host-cell parasitism by Cryptosporidium. Trends in Parasitology 24, 509516.CrossRefGoogle ScholarPubMed
Bull, S., Chalmers, R., Sturdee, A. P., Curray, A. and Kennaugh, J. (1998). Cross-reaction of an anti-Cryptosporidium monoclonal antibody with sporocysts of Monocystis species. Veterinary Parasitology 77, 195197.CrossRefGoogle ScholarPubMed
Butaeva, F., Paskerova, G. and Entzeroth, R. (2006). Ditrypanocystis sp. (Apicomplexa, Gregarinia, Selenidiidae): the mode of survival in the gut of Enchytraeus albidus (Annelida, Oligochaeta, Enchytraeidae) is close to that of the coccidian genus Cryptosporidium. Tsitologiia 48, 695704.Google ScholarPubMed
Caccio, S. M., Thompson, R. C. A., McLauchlin, J. and Smith, H. V. (2005). Unravelling Cryptosporidium and Giardia epidemiology. Trends in Parasitology 21, 430437.CrossRefGoogle ScholarPubMed
Carreno, R. A., Martin, D. S. and Barta, J. R. (1999). Cryptosporidium is more closely related to gregarines than to coccidia as shown by phylogenetic analysis of apicomplexan parasites inferred using small- subunit ribosomal RNA gene sequences. Parasitology Research 85, 899904.CrossRefGoogle ScholarPubMed
Dionisio, D. (2002). Cryptosporidiosis in HIV-infected patients. Journal of Postgraduate Medicine 48, 215216.Google ScholarPubMed
Harandi, F. M., Hobbs, R. P., Adams, P. J., Mobedi, I., Morgan-Ryan, U. M. and Thompson, R. C. A. (2002). Molecular and morphological characterisation of Echinococcus granulosus of human and animal origin in Iran. Parasitology 125, 367373.Google ScholarPubMed
Hijjawi, N. S., Meloni, B. P., Morgan, U. M. and Thompson, R. C. A. (2001). Complete development and long-term maintenance of Cryptosporidium parvum human and cattle genotypes in cell culture. International Journal for Parasitology 31, 10481055.CrossRefGoogle ScholarPubMed
Hijjawi, N. S., Meloni, B. P., Morgan, U. M., Olson, M. E. and Thompson, R. C. A. (2002). Successful in vitro cultivation of Cryptosporidium andersoni with evidence for the existence of novel extracellular stages in the Cryptosporidium life cycle. International Journal for Parasitology 32, 17191726.CrossRefGoogle Scholar
Hijjawi, N. S., Meloni, B. P., Ng'anzo, M., Ryan, U. M., Olson, M. E., Cox, P. T., Monis, P. T. and Thompson, R. C. A. (2004). Complete development of Cryptosporidium parvum in host cell-free culture, International Journal for Parasitology 34, 769777.CrossRefGoogle ScholarPubMed
Hobbs, R. P., Lymbery, A. J. and Thompson, 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, 273281.CrossRefGoogle Scholar
Hopkins, R. M., Constantine, C. C., Groth, D. A., Wetherall, J. D., Reynoldson, J. A. and Thompson, R. C. A. (1999). PCR-based DNA fingerprinting of Giardia duodenalis isolates using the intergenic rDNA spacer. Parasitology 118, 531539.CrossRefGoogle ScholarPubMed
Howell, M. J. and Smyth, J. D. (1995). Maintenance and cultivation of Echinococcus species in vivo and in vitro. In Echinococcus and Hydatid Disease (ed. Thompson, R. C. A. and Lymbery, A. J.), pp. 201232. CAB International, Wallingford, Oxon, UK.Google Scholar
Hunter, P. R. and Thompson, R. C. A. (2005). The zoonotic transmission of Giardia and Cryptosporidium. International Journal for Parasitology 35, 11811190.CrossRefGoogle ScholarPubMed
Jenkins, D. J., Romig, T. and Thompson, R. C. A. (2005). Emergence/re-emergence of Echinococcus spp. – a global update. International Journal for Parasitology 35, 12051219.CrossRefGoogle ScholarPubMed
Kumaratilake, L. M., Thompson, R. C. A. and Eckert, J. (1986). Echinococcus granulosus of equine origin from different countries possess uniform morphological characteristics. International Journal for Parasitology 16, 529540.CrossRefGoogle ScholarPubMed
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, 207215.CrossRefGoogle Scholar
Leander, B. S. and Keeling, P. J. (2004). Morphostasis in alveolate evolution. Trends in Ecology and Evolution 18, 395402.CrossRefGoogle Scholar
Leonhard, S., Pfister, K., Beelitz, P., Wielinga, C. and Thompson, R. C. A. (2007). The molecular characterisation of Giardia from dogs in Southern Germany. Veterinary Parasitology 150, 3338.CrossRefGoogle ScholarPubMed
Levine, N. D. (1988). The Protozoan Phylum Apicomplexa, Vols 1 and 2, CRC, Boca Raton, FL, USA.Google Scholar
Lymbery, A. J. and Thompson, R. C. A. (1996). Species in the genus Echinococcus: pattern and process. Parasitology Today 12, 486491.CrossRefGoogle ScholarPubMed
Manabe, Y. C., Clark, D. P., Moore, R. D., Lumadue, J. A., Dahlman, H. R., Belitsos, P. C., Chaisson, R. E. and Sears, C. L. (1998). Cryptosporidiosis in patients with AIDS: correlates of disease and survival. Clinical Infectious Diseases 27, 536542.CrossRefGoogle ScholarPubMed
Mayrhofer, G., Andrews, R. H., Ey, P. L. and Chilton, N. B. (1995). Division of Giardia isolates from humans into two genetically distinct assemblages by electrophoretic analysis of enzymes encoded at 27 loci and comparison with Giardia muris. Parasitology 111, 1117.CrossRefGoogle ScholarPubMed
McManus, D. P. and Thompson, R. C. A. (2003). Molecular epidemiology of cystic echinococcosis. Parasitology 127, S37S51.CrossRefGoogle ScholarPubMed
Meloni, B. P., Lymbery, A. J. and Thompson, R. C. A. (1995). Genetic characterization of isolates of Giardia duodenalis by enzyme electrophoresis: implications for reproductive biology, population structure, taxonomy, and epidemiology. Journal of Parasitology 81, 368383.CrossRefGoogle ScholarPubMed
Meyer, E. A. (1970). Isolation and axenic cultivation of Giardia trophozoites from the rabbit, chinchilla and cat. Experimental Parasitology 27, 179183.CrossRefGoogle ScholarPubMed
Meyer, E. A. (1976). Giardia lamblia isolation and axenic cultivation. Experimental Parasitology 39, 101105.CrossRefGoogle ScholarPubMed
Moks, E., Jogisalu, I., Valdmann, H. and Saarma, U. (2008). First report of Echinococcus granulosus genotype G8 in Eurasia and a reappraisal of the phylogenetic relationships of ‘genotypes’ G5–G10. Parasitology 135, 647654.CrossRefGoogle Scholar
Monis, P. T. and Thompson, R. C. A. (2003). Cryptosporidium and Giardia-zoonoses: fact or fiction? Infection, Genetics and Evolution 3, 233244.CrossRefGoogle ScholarPubMed
Monis, P. T., Andrews, R. H., Mayrhofer, G., Mackrill, J., Kulda, J., Isaac-Renton, J. L. and Ey, P. L. (1998). Novel lineages of Giardia intestinalis identified by genetic analysis of organisms isolated from dogs in Australia. Parasitology 116, 7–19.CrossRefGoogle ScholarPubMed
Monis, P. T., Andrews, R. H., Mayrhofer, G. and Ey, P. L. (1999). Molecular systematics of the parasitic protozoan Giardia intestinalis. Molecular Biology and Evolution 16, 11351144.CrossRefGoogle ScholarPubMed
Monis, P. T., Caccio, S. and Thompson, R. C. A. (2009). Variation in Giardia: Towards a taxonomic revision of the genus. Trends in Parasitology 25, 93–100.CrossRefGoogle ScholarPubMed
Morrison, H. G., McArthur, A. G., Gillin, F. D., Aley, S. B., Adam, R. D., Olsen, G. J., Best, A. A., Cande, W. Z., Chen, F., Cipriano, M. J., Davids, B. J., Dawson, S. C., Elmendorf, H. G., Hehl, A. B., Holder, M. E., Huse, S. M., Kim, U. U., Lasek-Nesselquist, E., Manning, G., Nigam, A., Nixon, J. E. J., Palm, D., Passamaneck, N. E., Prabhu, A., Reich, C. I., Reiner, D. S., Samuelson, J., Svard, S. and Sogin, M. L. (2007). Genomic minimialism in the early diverging intestinal parasite Giardia lamblia. Science 317, 19211926.CrossRefGoogle ScholarPubMed
Romig, T., Dinkel, A. and Mackenstedt, U. (2006). The present situation of echinococcosis in Europe. Parasitology International 55, S187S191.CrossRefGoogle ScholarPubMed
Smyth, J. D. (1967). Studies on tapeworm physiology. XI. in vitro cultivation of Echinococcus granulosus from the protoscolex to the strobilate stage. Parasitology 57, 111133.CrossRefGoogle Scholar
Smyth, J. D. (1968). In vitro studies and host-specificity in Echinococcus. Bulletin of the World Health Organization 39, 5–12.Google ScholarPubMed
Smyth, J. D. (1969). Parasites as biological models. Parasitology 59, 7391.CrossRefGoogle ScholarPubMed
Smyth, J. D. (1971). Development of monozoic forms of Echinococcus granulosus during in vitro culture. International Journal for Parasitology 1, 121124.CrossRefGoogle ScholarPubMed
Smyth, J. D. (1972). Changes in the digestive surface of cestodes during larval/adult differentiation. In Functional Aspects of Parasite Surfaces (ed. Taylor, A. E. R. and Muller, R.), Symposium of the British Society of Parasitology 10, pp. 4170. Blackwell Scientific, Oxford, UK.Google Scholar
Smyth, J. D. (1982). Speciation in Echinococcus: biological and biochemical criteria. Revista Iberica Parasitologia, (Special Volume), 2534.Google Scholar
Smyth, J. D. and Barrett, N. J. (1979). Echinococcus multilocularis: further observations on strobilar differentiation in vitro. Revista Iberica Parasitologia 39, 3953.Google Scholar
Smyth, J. D. and Davies, Z. (1974 a). In vitro culture of the strobilar stage of Echinococcus granulosus (sheep strain): a review of basic problems and results. International Journal for Parasitology 4, 631644.CrossRefGoogle Scholar
Smyth, J. D. and Davies, Z. (1974 b). Occurrence of physiological strains of Echinococcus granulosus demonstrated by the in vitro culture of protoscoleces from sheep and horse hydatid cysts. International Journal for Parasitology 4, 443445.CrossRefGoogle ScholarPubMed
Smyth, J. D. and Davies, Z. (1975). In vitro suppression of segmentation in Echinococcus multilocularis with morphological transformation of protoscoleces into monozoic adults. Parasitology 71, 125135.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, 493514.CrossRefGoogle Scholar
Smyth, J. D. and Smyth, M. M. (1968). Some aspects of host specificity in Echinococcus granulosus. Helminthologia 9, 519527.Google Scholar
Smyth, J. D., Howkins, A. B. and Barton, M. (1966). Factors controlling the differentiation of the hydatid organism, Echinococcus granulosus, into cystic or strobilar stages in vitro. Nature, London 211, 13741377.CrossRefGoogle ScholarPubMed
Smyth, J. D., Miller, H. J. and Howkins, A. B. (1967). Further analysis of the factors controlling strobilization, differentiation, and maturation of Echinococcus granulosus in vitro. Experimental Parasitology 21, 3141.CrossRefGoogle ScholarPubMed
Spiliotis, M., Lechner, S., Tappe, D., Scheller, C., Krohne, G. and Brehm, K. (2008). Transient transfection of Echinococcus mulitlocularis primary cells and complete in vitro generation of metacestode vesicles. International Journal for Parasitology 38, 10251039.CrossRefGoogle Scholar
Steuart, R. F. L., O'Handley, R., Lipscombe, R. J. and Thompson, R. C. A. (2008). Alpha 2 Giardin is an assemblage A specific protein of human infective Giardia duodenalis. Parasitology 135, 16211627.CrossRefGoogle ScholarPubMed
Thompson, R. C. A. (1995). Biology and systematics of Echinococcus. In Echinococcus and Hydatid Disease (ed. Thompson, R. C. A. and Lymbery, A. J.), pp. 150. CAB International, Wallingford, Oxon, UK.Google Scholar
Thompson, R. C. A. (2001). Echinococcosis. In Principles and Practice of Clinical Parasitology (ed. Gillespie, S. H. and Pearson, R. D.), pp. 595612. Wiley, Sussex, UK.Google Scholar
Thompson, R. C. A. (2002). Towards a better understanding of host specificity and the transmission of Giardia: the impact of molecular epidemiology. In Giardia: The Cosmopolitan Parasite (ed. Olson, B. E., Olson, M. E. and Wallis, P. M.), pp. 5569. CAB International, Wallingford, UK.CrossRefGoogle Scholar
Thompson, R. C. A. (2008 a). The taxonomy, phylogeny and transmission of Echinococcus. Experimental Parasitology 119, 439446.CrossRefGoogle ScholarPubMed
Thompson, R. C. A. (2008 b). Giardiasis: modern concepts in control and management. Annales Nestle 66, 2330.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, 210263.Google ScholarPubMed
Thompson, R. C. A. and Lymbery, A. J. (1990). Intraspecific variation in parasites – what is a strain? Parasitology Today 6, 345348.CrossRefGoogle ScholarPubMed
Thompson, R. C. A. and Lymbery, A. J. (1991). The epidemiological significance of biological variation in Echinococcus. Archives de la Hidatidosis 30, 195200.Google Scholar
Thompson, R. C. A. and Lymbery, A. J. (1996). Genetic variability in parasites and host-parasite interactions. Parasitology 112, 517522.CrossRefGoogle ScholarPubMed
Thompson, R. C. A. and McManus, 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. 119. WHO/OIE, Paris. World Health Organization, Geneva, Switzerland.Google Scholar
Thompson, R. C. A. and McManus, D. P. (2002). Towards a taxonomic revision of the genu Echinococcus. Trends in Parasitology 18, 452457.CrossRefGoogle Scholar
Thompson, R. C. A. and Monis, P. T. (2004). Variation in Giardia: Implications for taxonomy and epidemiology. Advances in Parasitology, 58, 69–137.CrossRefGoogle ScholarPubMed
Thompson, R. C. A. and Smyth, J. D. (1974). Potential danger of hydatid disease of horse-dog origin. British Medical Journal 3, 807.CrossRefGoogle ScholarPubMed
Thompson, R. C. A. and Smyth, J. D. (1975). Equine hydatidosis: a review of the current status in Great Britain and the results of an epidemiological survey. Veterinary Parasitology 1, 107127.CrossRefGoogle Scholar
Thompson, R. C. A., Kumaratilake, L. M. and Eckert, J. (1984). Observations on Echinococcus granulosus of cattle origin in Switzerland. International Journal for Parasitology 14, 283291.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, 145176.CrossRefGoogle ScholarPubMed
Thompson, R. C. A., Olson, M. E., Zhu, G., Enomoto, S., Abrahamsen, M. S. and Hijjawi, N. S. (2005). Cryptosporidium and cryptosporidiosis. Advances in Parasitology 59, 77–158.CrossRefGoogle ScholarPubMed
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, 258262.CrossRefGoogle ScholarPubMed
Tyzzer, E. E. (1912). Cryptosporidium parvum (sp. nov.), a coccidian found in the small intestine of the common mouse. Archives für Protistenkunde 26, 394418.Google Scholar
Valigurova, A., Hofmannova, L., Koudela, B. and Vavra, J. (2007). An ultrastructural comparison of the attachment sites between Gregarina steini and Cryptosporidium muris. The Journal of Eukaryotic Microbiology, 54, 495510.CrossRefGoogle ScholarPubMed
Valigurova, A., Jirku, M., Koudela, B., Gelnar, M., Modry, D. and Slapeta, J. (2008). Cryptosporidia: epicellular parasites embraced by the host cell membrane. International Journal for Parasitology, 38, 913922.CrossRefGoogle ScholarPubMed
Weiland, M. E., McArthur, A. G., Morrison, H. G., Sogin, M. L. and Svard, S. G. (2005). Annexin-like alpha giardins: a new cytoskeletal gene family in Giardia lamblia. International Journal for Parasitology 35, 617626.CrossRefGoogle ScholarPubMed
Wielinga, C. M. and Thompson, R. C. A. (2007). Comparative evaluation of Giardia duodenalis sequence data. Parasitology 134, 17951821.CrossRefGoogle ScholarPubMed