Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-20T04:30:59.013Z Has data issue: false hasContentIssue false
  • English
  • Français

The potential impact of native Australian trypanosome infections on the health of koalas (Phascolarctos cinereus)

Published online by Cambridge University Press:  27 April 2011

L. M. McINNES ,
A. GILLETT ,
J. HANGER ,
S. A. REID  and
U. M. RYAN
L. M. McINNES*
Affiliation:
Division of Health Sciences, School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, Perth WA 6150, Australia
A. GILLETT
Affiliation:
The Australian Zoo Wildlife Hospital, Beerwah, Queensland, Australia
J. HANGER
Affiliation:
The Australian Zoo Wildlife Hospital, Beerwah, Queensland, Australia
S. A. REID
Affiliation:
Division of Health Sciences, School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, Perth WA 6150, Australia
U. M. RYAN
Affiliation:
Division of Health Sciences, School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, Perth WA 6150, Australia
*
*Corresponding author: Division of Health Sciences, School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, Perth WA 6150, Australia. Tel: +61893602495. Fax: +61893104144. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Whole blood collected from koalas admitted to the Australian Zoo Wildlife Hospital (AZWH), Beerwah, QLd, Australia, during late 2006–2009 was tested using trypanosome species-specific 18S rDNA PCRs designed to amplify DNA from Trypanosoma irwini, T. gilletti and T. copemani. Clinical records for each koala sampled were reviewed and age, sex, blood packed cell volume (PCV), body condition, signs of illness, blood loss, trauma, chlamydiosis, bone marrow disease, koala AIDS and hospital admission outcome (‘survival’ / ‘non-survival’) were correlated with PCR results. Overall 73·8% (439/595) of the koalas were infected with at least 1 species of trypanosome. Trypanosoma irwini was detected in 423/595 (71·1%), T. gilletti in 128/595 (21·5%) and T. copemani in 26/595 (4·4%) of koalas. Mixed infections were detected in 125/595 (21%) with co-infections of T. irwini and T. gilletti (101/595, 17%) being most common. There was a statistical association between infection with T. gilletti with lower PCV values and body condition scores in koalas with signs of chlamydiosis, bone marrow disease or koala AIDS. No association between T. gilletti infection and any indicator of health was observed in koalas without signs of concurrent disease. This raises the possibility that T. gilletti may be potentiating other disease syndromes affecting koalas.

Keywords

Trypanosomakoala18S rDNApathogenicitypotentiation
Type
Research Article
Information
Parasitology , Volume 138 , Issue 7 , June 2011 , pp. 873 - 883
Copyright
Copyright © Cambridge University Press 2011

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

Akinbamijo, O. O., Bennison, J. J., Jaitner, J. and Dempfle, L. (1998). Haematological changes in N'Dama and Gobra Zebu bulls during Trypanosoma congolense infection maintained under a controlled feeding regimen. Acta Tropica 69, 181–192.CrossRefGoogle Scholar
Austen, J., Jefferies, R., Friend, T., Adams, P., Ryan, U. and Reid, S. (2009). Morphological and molecular characterisation of Trypanosoma copemani n.sp. (Trypanosomatidae) isolated from Gilbert's potoroo (Potorous gilbertii) and quokka (Setonix brachyurus). Parasitology 136, 783–792.CrossRefGoogle ScholarPubMed
Brown, M. J. F., Schmid-Hempel, R. and Schmid-Hempel, P. (2003). Strong context-dependent virulence in a host-parasite system: reconciling genetic evidence with theory. Journal of Animal Ecology 72, 994–1002.CrossRefGoogle Scholar
Canfield, P. J., O'Neill, M. E. and Smith, E. F. (1989 a). Haematological and biochemical investigations of diseased koalas (Phascolarctos cinereus). Australian Veterinary Journal 66, 269–272.CrossRefGoogle ScholarPubMed
Canfield, P. M., O'Neill, M. E. and Smith, E. F. (1989 b). Haematological and biochemical reference values for the koala (Phascolarctos cinereus). Australian Veterinary Journal 66, 324–326.CrossRefGoogle ScholarPubMed
Carrera, N. J., Carmona, M. C., Guerrero, O. M. and Castillo, A. C. (2009). [The immunosuppressant effect of T. lewisi (Kinetoplastidae) infection on the multiplication of Toxoplasma gondii (Sarcocystidae) on alveolar and peritoneal macrophages of the white rat]. Revista de Biología Tropical 57, 13–22.Google ScholarPubMed
Chisi, J. E., Misiri, H., Zverev, Y., Nkhoma, A. and Sternberg, J. M. (2004). Anaemia in human African trypanosomiasis caused by Trypanosoma brucei rhodesiense. East African Medical Journal 81, 505–508.CrossRefGoogle ScholarPubMed
Clausen, P. H., Chuluun, S., Sodnomdarjaa, R., Greiner, M., Noeckler, K., Staak, C., Zessin, K. H. and Schein, E. (2003). A field study to estimate the prevalence of Trypanosoma equiperdum in Mongolian horses. Veterinary Parasitology 115, 9–18.CrossRefGoogle ScholarPubMed
Clopper, C. and Pearson, S. (1934). The use of confidence or fiducial limits illustrated in the case of the Binomial. Biometrika 26, 404–413.CrossRefGoogle Scholar
Cox, F. E. (1968). Immunity to malaria after recovery from piroplasmosis in mice. Nature, London 219, 646.CrossRefGoogle ScholarPubMed
Cox, F. E. (2001). Concomitant infections, parasites and immune responses. Parasitology 122 (Suppl.) S23–S38.CrossRefGoogle ScholarPubMed
Cox, H. W. and Milar, R. (1968). Cross-protection immunization by Plasmodium and Babesia infections of rats and mice. American Journal of Tropical Medicine and Hygiene 17, 173–179.CrossRefGoogle ScholarPubMed
Da Silva, A. S., Costa, M. M., Wolkmer, P., Zanette, R. A., Faccio, L., Gressler, L. T., Dorneles, T. E., Santurio, J. M., Lopes, S. T. and Monteiro, S. G. (2009). Trypanosoma evansi: hematologic changes in experimentally infected cats. Experimental Parasitology 123, 31–34.CrossRefGoogle ScholarPubMed
Doherty, M. L., Windle, H., Voorheis, H. P., Larkin, H., Casey, M., Clery, D. and Murray, M. (1993). Clinical disease associated with Trypanosoma theileri infection in a calf in Ireland. Veterinary Record 132, 653–656.CrossRefGoogle Scholar
Dwinger, R. H., Agyemang, K., Kaufmann, J., Grieve, A. S. and Bah, M. L. (1994). Effects of trypanosome and helminth infections on health and production parameters of village N'Dama cattle in The Gambia. Veterinary Parasitology 54, 353–365.CrossRefGoogle ScholarPubMed
Egbe-Nwiyi, T. N. and Antia, R. E. (1993). The effect of trypanocidal drug treatment on the haematological changes in Trypanosoma brucei brucei infected splenectomised dogs. Veterinary Parasitology 50, 23–33.CrossRefGoogle ScholarPubMed
Ellis, J. A., Scott, J. R., Machugh, N. D., Gettinby, G. and Davis, W. C. (1987). Peripheral blood leucocytes subpopulation dynamics during Trypanosoma congolense infection in Boran and N'Dama cattle: an analysis using monoclonal antibodies and flow cytometry. Parasite Immunology 9, 363–378.CrossRefGoogle ScholarPubMed
Fakae, B. B., Harrison, L. J., Ross, C. A. and Sewell, M. M. (1999). Heligmosomoides polygyrus and Trypanosoma congolense infections in mice: effect of immunisation by abbreviated larval infection. Veterinary Parasitology 85, 13–23.CrossRefGoogle ScholarPubMed
Faye, D., Fall, A., Leak, S., Losson, B. and Geerts, S. (2005). Influence of an experimental Trypanosoma congolense infection and plane of nutrition on milk production and some biochemical parameters in West African Dwarf goats. Acta Tropica 93, 247–257.CrossRefGoogle ScholarPubMed
Gonzales, J. L., Chacon, E., Miranda, M., Loza, A. and Siles, L. M. (2007). Bovine trypanosomosis in the Bolivian Pantanal. Veterinary Parasitology 146, 9–16.CrossRefGoogle ScholarPubMed
Goodwin, L. G. (1970). The pathology of African trypanosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 64, 797–817.CrossRefGoogle ScholarPubMed
Goodwin, L. G., Green, D. G., Guy, M. W. and Voller, A. (1972). Immunosuppression during trypanosomiasis. British Journal of Experimental Pathology 53, 40–43.Google ScholarPubMed
Goossens, B., Osaer, S., Kora, S., Jaitner, J., Ndao, M. and Geerts, S. (1997). The interaction of Trypanosoma congolense and Haemonchus contortus in Djallonke sheep. International Journal for Parasitology 27, 1579–1584.CrossRefGoogle ScholarPubMed
Goossens, B., Osaer, S., Kora, S. and Ndao, M. (1998). Haematological changes and antibody response in trypanotolerant sheep and goats following experimental Trypanosoma congolense infection. Veterinary Parasitology 79, 283–297.CrossRefGoogle ScholarPubMed
Griffin, L., Allonby, E. W. and Preston, J. M. (1981). The interaction of Trypanosoma congolense and Haemonchus contortus infections in 2 breeds of goat. 1. Parasitology. Journal of Comparative Pathology 91, 85–95.CrossRefGoogle ScholarPubMed
Hamilton, P. B., Stevens, J. R., Gaunt, M. W., Gidley, J. and Gibson, W. C. (2004). Trypanosomes are monophyletic: evidence from genes for glyceraldehyde phosphate dehydrogenase and small subunit ribosomal RNA. International Journal for Parasitology 34, 1393–1404.CrossRefGoogle ScholarPubMed
Hanger, J., McKee, J., Tarlinton, R. and Yates, A. (2003). Cancer and haematological disease in koalas, a clinical and virological update. In Annual Conference of the Australian Association of Veterinary Conservation Biologists (ed. Tribe, A. and Booth, R.), pp. 19–37. School of Animal Studies, University of Queensland Cairns, Australia.Google Scholar
Holland, W. G., Do, T. T., Huong, N. T., Dung, N. T., Thanh, N. G., Vercruysse, J. and Goddeeris, B. M. (2003). The effect of Trypanosoma evansi infection on pig performance and vaccination against classical swine fever. Veterinary Parasitology 111, 115–123.CrossRefGoogle ScholarPubMed
Jackson, S., Reid, K., Spittal, D. and Romer, L. (2003). Koalas. In Australian Mammals: Biology and Captive Management (ed. Jackson, S.), pp. 145–181. CSIRO Publishing, Collingwood, Victoria, Australia.Google Scholar
Jimenez-Coello, M., Poot-Cob, M., Ortega-Pacheco, A., Guzman-Marin, E., Ramos-Ligonio, A., Sauri-Arceo, C. H. and Acosta-Viana, K. Y. (2008). American trypanosomiasis in dogs from an urban and rural area of Yucatan, Mexico. Vector Borne and Zoonotic Diseases 8, 755–761.CrossRefGoogle Scholar
Katunguka-Rwakishaya, E., Murray, M. and Holmes, P. H. (1992). The pathophysiology of ovine trypanosomosis: haematological and blood biochemical changes. Veterinary Parasitology 45, 17–32.CrossRefGoogle ScholarPubMed
Kaufmann, J., Dwinger, R. H., Hallebeek, A., Van Dijk, B. and Pfister, K. (1992). The interaction of Trypanosoma congolense and Haemonchus contortus infections in trypanotolerant N'Dama cattle. Veterinary Parasitology 43, 157–170.CrossRefGoogle ScholarPubMed
Khan, R. A. and Lacey, D. (1986). Effect of concurrent infections of Lernaeocera branchialis (Copepoda) and Trypanosoma murmanensis (Protozoa) on Atlantic cod, Gadus morhua. Journal of Wildlife Diseases 22, 201–208.CrossRefGoogle ScholarPubMed
Lee, A. K. and Carrick, F. N. (1989). Phascolarctidae. In Fauna of Australia, Vol. 1b Mammalia (ed. Walton, D. W. and Richardson, B. J.), pp. 740–754. Australian Government Publishing Service, Canberra, Australia.Google Scholar
Mahama, C. I., Desquesnes, M., Dia, M. L., Losson, B., De Deken, R. and Geerts, S. (2004). A cross-sectional epidemiological survey of bovine trypanosomosis and its vectors in the Savelugu and West Mamprusi districts of northern Ghana. Veterinary Parasitology 122, 1–13.CrossRefGoogle ScholarPubMed
Maitland, K., Williams, T. N. and Newbold, C. I. (1997). Plasmodium vivax and P. falciparum: Biological interactions and the possibility of cross-species immunity. Parasitology Today 13, 227–231.CrossRefGoogle ScholarPubMed
Martin, R. (1981). Age-specific fertility in three populations of the koala, Phascolarctos cinereus Goldfuss, in Victoria. Wildlife Research 8, 275–283.CrossRefGoogle Scholar
Maslov, D. A., Lukes, J., Jirku, M. and Simpson, L. (1996). Phylogeny of trypanosomes as inferred from the small and large subunit rRNAs: implications for the evolution of parasitism in the trypanosomatid protozoa. Molecular and Biochemical Parasitology 75, 197–205.CrossRefGoogle ScholarPubMed
McInnes, L. M., Gillett, A., Ryan, U. M., Austen, J., Campbell, R. S., Hanger, J. and Reid, S. A. (2009). Trypanosoma irwini n. sp (Sarcomastigophora: Trypanosomatidae) from the koala (Phascolarctos cinereus). Parasitology 136, 875–885.CrossRefGoogle Scholar
McInnes, L. M., Hanger, J., Simmons, G., Reid, S. A. and Ryan, U. M. (2011). 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, 59–70.CrossRefGoogle ScholarPubMed
Mutayoba, B. M., Eckersall, P. D., Cestnik, V., Jeffcoate, I. A., Gray, C. E. and Holmes, P. H. (1995). Effects of Trypanosoma congolense on pituitary and adrenocortical function in sheep: changes in the adrenal gland and cortisol secretion. Research in Veterinary Science 58, 174–179.CrossRefGoogle ScholarPubMed
Mwangi, D. M., Munyua, W. K. and Nyaga, P. N. (1990). Immunosuppression in caprine trypanosomiasis: effects of acute Trypanosoma congolense infection on antibody response to anthrax spore vaccine. Tropical Animal Health and Production 22, 95–100.CrossRefGoogle ScholarPubMed
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, 331–339.CrossRefGoogle ScholarPubMed
Obendorf, D. L. (1983). Causes of mortality and morbidity of wild koalas, Phascolarctos cinereus (Goldfuss), in Victoria, Australia. Journal of Wildlife Diseases 19, 123–131.CrossRefGoogle ScholarPubMed
Ogunsanmi, A. O. and Taiwo, V. O. (2001). Pathobiochemical mechanisms involved in the control of the disease caused by Trypanosoma congolense in African grey duiker (Sylvicapra grimmia). Veterinary Parasitology 96, 51–63.CrossRefGoogle ScholarPubMed
Omeke, B. C. and Ugwu, D. O. (1991). Pig trypanosomiasis: comparative anaemia and histopathology of lymphoid organs. Revue d'Elevage et de Medecine Veterinaire des Pays Tropicaux 44, 267–272.CrossRefGoogle ScholarPubMed
Onah, D. N., Hopkins, J. and Luckins, A. G. (1996). Haematological changes in sheep experimentally infected with Trypanosoma evansi. Parasitology Research 82, 659–663.CrossRefGoogle ScholarPubMed
Onah, D. N., Onyenwe, I. W., Ihedioha, J. I. and Onwumere, O. S. (2004). Enhanced survival of rats concurrently infected with Trypanosoma brucei and Strongyloides ratti. Veterinary Parasitology 119, 165–176.CrossRefGoogle ScholarPubMed
Onah, D. N. and Wakelin, D. (2000). Murine model study of the practical implication of trypanosome-induced immunosuppression in vaccine-based disease control programmes. Veterinary Immunology and Immunopathology 74, 271–284.CrossRefGoogle ScholarPubMed
Onyeyili, P. A. and Anika, S. M. (1990). Effects of the combination of DL-alpha-difluoromethylornithine and diminazene aceturate in Trypanosoma congolense infection of dogs. Veterinary Parasitology 37, 9–19.CrossRefGoogle ScholarPubMed
Reid, H. W., Buxton, D., Finlayson, J. and Holmes, P. H. (1979). Effect of chronic Trypanosoma brucei infection on the course of louping ill virus infection in mice. Infection and Immunity 23, 192–196.CrossRefGoogle ScholarPubMed
Rurangirwa, F. R., Musoke, A. J., Nantulya, V. M. and Tabel, H. (1983). Immune depression in bovine trypanosomiasis: effects of acute and chronic Trypanosoma congolense and chronic Trypanosoma vivax infections on antibody response to Brucella abortus vaccine. Parasite Immunology 5, 267–276.CrossRefGoogle ScholarPubMed
Seifi, H. A. (1995). Clinical trypanosomosis due to Trypanosoma theileri in a cow in Iran. Tropical Animal Health and Production 27, 93–94.CrossRefGoogle Scholar
Sekoni, V. O., Saror, D. I., Njoku, C. O., Kumi-Diaka, J. and Opaluwa, G. I. (1990). Comparative haematological changes following Trypanosoma vivax and T. congolense infections in Zebu bulls. Veterinary Parasitology 35, 11–19.CrossRefGoogle Scholar
Sharpe, R. T., Langley, A. M., Mowat, G. N., Macaskill, J. A. and Holmes, P. H. (1982). Immunosuppression in bovine trypanosomiasis: response of cattle infected with Trypanosoma congolense to foot-and-mouth disease vaccination and subsequent live virus challenge. Research in Veterinary Science 32, 289–293.CrossRefGoogle ScholarPubMed
Silva, R. M. A. S., Herrera, H. M., Da Silviera Domingos, L. B., Ximenes, F. A. and Davila, A. M. R. (1995). Pathogenesis of Trypanosoma evansi infection in dogs and horses: Hematological and clinical aspects. Ciência Rura 25, 233–238.CrossRefGoogle Scholar
Singh, N., Pathak, K. M. and Kumar, R. (2004). A comparative evaluation of parasitological, serological and DNA amplification methods for diagnosis of natural Trypanosoma evansi infection in camels. Veterinary Parasitology 126, 365–373.CrossRefGoogle ScholarPubMed
Singla, L. D., Juyal, P. D. and Sharma, N. S. (2010). Immune responses to haemorrhagic septicaemia (HS) vaccination in Trypanosoma evansi infected buffalo-calves. Tropical Animal Health and Production 42, 589–595.CrossRefGoogle ScholarPubMed
Spencer, A. J. and Canfield, P. J. (1995). Bone marrow examination in the koala (Phascolarctos cinereus). Comparative Haematology International 5, 31–37.CrossRefGoogle Scholar
Tarlinton, R., Meers, J. and Young, P. (2008). Biology and evolution of the endogenous koala retrovirus. Cellular and Molecular Life Sciences 65, 3413–3421.CrossRefGoogle ScholarPubMed
Thekisoe, O. M., Honda, T., Fujita, H., Battsetseg, B., Hatta, T., Fujisaki, K., Sugimoto, C. and Inoue, N. (2007). A trypanosome species isolated from naturally infected Haemaphysalis hystricis ticks in Kagoshima Prefecture, Japan. Parasitology 134, 967–974.CrossRefGoogle ScholarPubMed
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle ScholarPubMed
Uche, U. E. and Jones, T. W. (1994). Protection conferred by Trypanosoma evansi infection against homologous and heterologous trypanosome challenge in rabbits. Veterinary Parasitology 52, 21–35.CrossRefGoogle ScholarPubMed
Vogelnest, L. and Woods, R. (2008). Medicine of Australian Mammals, CSIRO Publishing, Collingwood, Victoria, Australia.CrossRefGoogle Scholar
Voller, A., Garnham, P. C. and Targett, G. A. (1966). Cross immunity in monkey malaria. Journal of Tropical Medicine and Hygiene 69, 121–123.Google ScholarPubMed
Ward, W. H., Hill, M. W., Mazlin, I. D. and Foster, C. K. (1984). Anaemia associated with a high parasitaemia of Trypanosoma theileri in a dairy cow. Australian Veterinary Journal 61, 324.CrossRefGoogle Scholar
Zuniga, C., Palau, T., Penin, P., Gamallo, C. and De Diego, J. A. (1997). Protective effect of Trypanosoma rangeli against infections with a highly virulent strain of Trypanosoma cruzi. Tropical Medicine & International Health 2, 482–487.CrossRefGoogle ScholarPubMed