Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-22T21:09:56.366Z Has data issue: false hasContentIssue false

Investigation of the morphological diversity of the potentially zoonotic Trypanosoma copemani in quokkas and Gilbert's potoroos

Published online by Cambridge University Press:  10 July 2015

JILL M. AUSTEN
Affiliation:
School of Veterinary and Life Sciences, Murdoch University, South Street, Murdoch, Western Australia 6150, Australia
SIMON A. REID
Affiliation:
School of Population Health Faculty of Medicine and Biomedical Science, University of Queensland Australia, St Lucia, Brisbane, Queensland 4072, Australia
DERRICK R. ROBINSON
Affiliation:
UMR-CNRS 5234, University of Bordeaux 2, 33076 Bordeaux, France
JAMES A. FRIEND
Affiliation:
Science and Conservation Division, Department of Parks and Wildlife, 120 Albany Highway, Albany, Western Australia 6330, Australia
WILLIAM G. F. DITCHAM
Affiliation:
School of Veterinary and Life Sciences, Murdoch University, South Street, Murdoch, Western Australia 6150, Australia
PETER J. IRWIN
Affiliation:
School of Veterinary and Life Sciences, Murdoch University, South Street, Murdoch, Western Australia 6150, Australia
UNA RYAN*
Affiliation:
School of Veterinary and Life Sciences, Murdoch University, South Street, Murdoch, Western Australia 6150, Australia
*
* Corresponding author: School of Veterinary and Life Sciences, Murdoch University, Murdoch, Western Australia 6150, Australia. E-mail: [email protected]

Summary

Trypanosomes are blood-borne parasites that can cause severe disease in both humans and animals, yet little is known of the pathogenicity and life-cycles of trypanosomes in native Australian mammals. Trypanosoma copemani is known to be infective to a variety of Australian marsupials and has recently been shown to be potentially zoonotic as it is resistant to normal human serum. In the present study, in vivo and in vitro examination of blood and cultures from Australian marsupials was conducted using light microscopy, immunofluorescence, scanning electron microscopy and fluorescence in situ hybridization. Promastigote, sphaeromastigote and amastigote life-cycle stages were detected in vivo and in vitro. Novel trypanosome-like stages were also detected both in vivo and in vitro representing an oval stage, an extremely thin stage, an adherent stage and a tiny round stage. The tiny round and adherent stages appeared to adhere to erythrocytes causing potential haematological damage with clinical effects similar to haemolytic anaemia. The present study shows for the first time that trypomastigotes are not the only life-cycle stages circulating within the blood stream of trypanosome infected Australian native marsupials and provides insights into possible pathogenic mechanisms of this potentially zoonotic trypanosome species.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Anosa, V. O. and Kaneko, J. J. (1983). Pathogenesis of Trypanosoma brucei infection in deer mice (Peromyscus maniculatus): light and electron microscopic studies on erythrocyte pathologic changes and phagocytosis. American Journal of Veterinary Research 44, 645651.Google ScholarPubMed
Amole, B. O., Clarkson, J. R., and Shear, H. L. (1982). Pathogenesis of anemia in Trypanosoma brucei infected mice. Infection and Immunity 36, 10601068.Google Scholar
Austen, J. M., Jefferies, R., Friend, J. A., Ryan, U., Adams, P. and Reid, S. A. (2009). Morphological and molecular characterisation of Trypanosoma copemani n. sp. (Trypanosomatidae) isolated from Gilbert's potoroo (Potorous gilbertii) and quokka (Setonix brachyurus). Parasitology 136, 783792.Google Scholar
Austen, J. M., Ryan, U. M., Friend, J. A., Ditcham, W. G. F. and Reid, S. A. (2011). Vector of Trypanosoma copemani identified as Ixodes sp. Parasitology 138, 866872.Google Scholar
Austen, J. M., Ryan, U. M., Ditcham, W. G. F., Friend, J. A. and Reid, S. A. (2015). The innate resistance of Trypanosoma copemani to human serum. Experimental Parasitology 153, 105110.Google Scholar
Barbosa, A., Austen, J., Gillett, A., Warren, K., Paparini, A., Irwin, P. and Ryan, U. (2015). First report of Trypanosoma vegrandis in koalas (Phascolarctos cinereus). Parasitology International. In press.Google Scholar
Botero, A., Thompson, C. K., Peacock, C., Clode, P. L., Nicholls, P. K., Wayne, A. F., Lymbery, A. J. and Thompson, R. C. A. (2013). Trypanosomes genetic diversity, polyparasitism and the population decline of the critically endangered Australian marsupial, the brush tailed bettong or woylie (Bettongia penicillata) . International Journal for Parasitology: Parasites and Wildlife 2, 2, 7789.Google Scholar
Clark, P., Adlard, R. D. and Spratt, D. M. (2004). Haemoparasites of Australian mammals. In: Haematology of Australian Mammals (ed. Clark, P.), pp. 147162. CSIRO, Collingwood, Australia.CrossRefGoogle Scholar
De Tores, P. J., Hayward, M. W., Dillon, M. J. and Brazell, R. I. (2007). Review of the distribution, causes for the decline and recommendations for management of the quokka, Setonix brachyurus (Macropodidae: Marsupialia), an endemic macropodid marsupial from south-west Western Australia. Conservation Science Western Australia 6, 1373.Google Scholar
Gull, K. (1999). The cytoskeleton of trypanosomatid parasites. Annual Reviews in Microbiology 53, 629655.CrossRefGoogle ScholarPubMed
Hamilton, P. B., Stevens, J. R., Gidley, J., Holz, P. and Gibson, W. C. (2005). A new lineage of trypanosomes from Australian vertebrates and terrestrial bloodsucking leeches (Haemadipsidae). International Journal for Parasitology 35, 431443.Google Scholar
Hart, R. P., Bradshaw, S. D. and Iveson, J. B. (1985). Salmonella infections in a Marsupial, the Quokka (Setonix brachyurus), in relation to seasonal changes in condition and environmental stress. Applied and Environmental Microbiology 49, 12761281.Google Scholar
Hayward, M. W., De Tores, P. J. and Banks, P. B. (2005). Habitat use of the quokka, Setonix brachyurus (Macropodidae:Marsupialia), in the northern jarrah forrest of Australia. Journal of Mammalogy 86, 683688.Google Scholar
Hoare, C. A. (1972). The Trypanosomes of Mammals: A Zoological Monograph. Blackwell Scientific Publications, Oxford, UK.Google Scholar
Jefferies, R., Ryan, U. M. and Irwin, P. J. (2007). PCR-RFLP for detection and differentiation of the canine piroplasm species and its use with filter paper-based technologies. Veterinary Parasitology 144, 2027.Google Scholar
Ley, V., Andrews, N. W., Robbins, E. S. and Nussenzweig, V. (1988). Amastigotes of Trypanosoma cruzi sustain an infective cycle in mammalian cells. Journal of Experimental Medicine 168, 649659.Google Scholar
Mackerras, M. J. (1959). The haematozoa of Australian mammals. Australian Journal of Zoology 7, 105135.Google Scholar
Mallah, H. S., Brown, M. R., Rossi, T. M. and Block, R. C. (2010). Parenteral fish oil-associated burr cell anemia. Journal of Pediatrics 156, 324326.Google Scholar
McInnes, L. M., Hanger, J., Simmons, G., Reid, S. A. and Ryan, U. M. (2010). Novel trypanosome Trypanosoma gilletti sp. (Euglenozoa: Trypanosomatidae) and the extension of the host range of Trypanosoma copemani to include the koala (Phascolarctos cinereus). Parasitology 138, 5970.Google Scholar
McInnes, L. M., Gillett, A., Hanger, J., Reid, S. A. and Ryan, U. M. (2011). The potential impact of native Australian trypanosome infections on the health of koalas (Phascolarctos cinereus). Parasitology 138, 111.Google Scholar
Noyes, H. A., Stevens, J. R., Teixeira, M., Phelan, J. and Holz, P. (1999). A nested PCR for the ssrRNA gene detects Trypanosoma binneyi in the platypus and Trypanosoma sp.in wombats and kangaroos in Australia. International Journal for Parasitology 29, 331339.Google Scholar
Rodak, B. F., Fritsma, G. A. and Keohane, E. M. (2012). Hematology: Clinical Principles and Applications, 4th Edn. Elsevier Saunders St. Louis, Missouri.Google Scholar
Schneider, C. A., Rasband, W. S. and Eliceiri, K. W. (2012). NIH Image to Image J: 25 years of image analysis. Nature Methods 9, 671675.Google Scholar
Silva, R. A. M. S., Herrera, H. M., Domingos, L. B. da S., Ximenes, F. A. and Darvila, A. M. R. (1995). Pathogenesis of Trypanosoma evansi infection of dogs and horses: heamatological and clinical aspects. Ciencia Rural Santa Maria 25, 233238.CrossRefGoogle Scholar
Sinclair, E. A. (1998). Morphological variation among populations of the quokka, Setonix brachyurus (Macropodidae: Marsupialia), in Western Australia. Australian Journal of Zoology 46, 439449.Google Scholar
Tanowitz, H. B., Kirchhoff, L. V., Simon, D., Morris, S. A., Weiss, L. M. and Wittner, M. (1992). Chagas’ Disease. Clinical Microbiology Reviews 5, 400419.CrossRefGoogle ScholarPubMed
Thompson, C. K., Botero, A., Wayne, A. F., Godfrey, S. S., Lymbery, A. J. and Thompson, R. C. A. (2013). Morphological polymorphism of Trypanosoma copemani and description of the genetically diverse T. vegrandis sp. nov. from the critically endangered Australian potoroid, the brush-tailed bettong (Bettongia penicillata (Gray, 1837)). Parasite and Vectors 6, 121.Google Scholar
Tyler, K. M. and Engman, D. M. (2001). The life-cycle of Trypanosoma cruzi revisited. International Journal for Parasitology 31, 472480.Google Scholar
Woo, P. T. and Kobayashi, A. (1975). Studies on the anemia in experimental African trypanosomiasis. 1. A preliminary communication on the mechanisms of anemia. Annales de la Societe belge de medecine tropicale 55, 3745.Google Scholar
Woodruff, A. W. (1973). Mechanisms involved in anemia associated with infection and splenomegaly in the tropics. Transaction of the Royal Society of Tropical Medicine and Hygiene 67, 313325.Google Scholar