Hostname: page-component-745bb68f8f-cphqk Total loading time: 0 Render date: 2025-02-03T06:01:51.306Z Has data issue: false hasContentIssue false
  • English
  • Français

The finch epidemic strain of Trichomonas gallinae is predominant in British non-passerines

Published online by Cambridge University Press:  07 August 2013

JEAN F. CHI ,
BECKI LAWSON ,
CHRIS DURRANT ,
KATIE BECKMANN ,
SHINTO JOHN ,
ABDULWAHED F. ALREFAEI ,
KIM KIRKBRIDE ,
DIANA J. BELL ,
ANDREW A. CUNNINGHAM  and
KEVIN M. TYLER
JEAN F. CHI
Affiliation:
University of East Anglia, School of Environmental Sciences, Norwich NR4 7TJ, UK
BECKI LAWSON
Affiliation:
Institute of Zoology, Zoological Society of London, Regents Park, London NW1 4RY, UK
CHRIS DURRANT
Affiliation:
Institute of Zoology, Zoological Society of London, Regents Park, London NW1 4RY, UK
KATIE BECKMANN
Affiliation:
Institute of Zoology, Zoological Society of London, Regents Park, London NW1 4RY, UK
SHINTO JOHN
Affiliation:
Institute of Zoology, Zoological Society of London, Regents Park, London NW1 4RY, UK
ABDULWAHED F. ALREFAEI
Affiliation:
University of East Anglia, School of Biological Sciences, Norwich NR4 7TJ, UK
KIM KIRKBRIDE
Affiliation:
Hawk Conservancy Trust, Sarson Lane, Weyhill, Andover SP11 8DY, UK
DIANA J. BELL*
Affiliation:
University of East Anglia, School of Biological Sciences, Norwich NR4 7TJ, UK
ANDREW A. CUNNINGHAM
Affiliation:
Institute of Zoology, Zoological Society of London, Regents Park, London NW1 4RY, UK
KEVIN M. TYLER
Affiliation:
Norwich Medical School at the University of East Anglia, Norwich NR4 7TJ, UK
*
*Corresponding author: University of East Anglia, School of Biological Sciences, Norwich NR4 7TJ, UK. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Avian trichomonosis, caused by the flagellated protozoan Trichomonas gallinae, is a recently emerged infectious disease of British passerines. The aetiological agent, a clonal epidemic strain of the parasite, has caused unprecedented finch mortality and population-level declines in Britain and has since spread to continental Europe. To better understand the potential origin of this epidemic and to further investigate its host range, T. gallinae DNA extracts were collected from parasite culture and tissue samples from a range of avian species in Britain. Sequence typing at the ITS1/5.8S rRNA/ITS2 region resolved three distinct ITS region types circulating in free-ranging British birds. Subtyping by sequence analyses at the Fe-hydrogenase gene demonstrated further strain variation within these ITS region types. The UK finch epidemic strain was preponderant amongst columbids sampled, however, wide strain diversity was encountered in isolates from a relatively small number of pigeons, suggesting further strains present in columbid populations across the UK are yet to be identified. Fe-hydrogenase gene sequence data in isolates from birds of prey with disease were predominantly identical to the UK finch epidemic strain, demonstrating its presence as a virulent strain in UK birds of prey since at least 2009.

Keywords

TrichomonosisTrichomoniasisTrichomonas gallinaemolecular epidemiologyinfectious diseaseITS1/5.8S/ITS2Fe-hydrogenase
Type
Research Article
Information
Parasitology , Volume 140 , Issue 10 , September 2013 , pp. 1234 - 1245
Copyright
Copyright © Cambridge University Press 2013 

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

Anderson, N. L., Grahn, R. A., Van Hoosear, K. and BonDurant, R. H. (2009). Studies of trichomonad protozoa in free ranging songbirds: prevalence of Trichomonas gallinae in house finches (Carpodacus mexicanus) and corvids and a novel trichomonad in mockingbirds (Mimus polyglottos). Veterinary Parasitology 161, 178–186.CrossRefGoogle Scholar
Baillie, S. R., Marchant, J. H., Leech, D. I., Renwick, A. R., Joys, A. C., Noble, D. G., Barimore, C., Conway, G. J., Downie, I. S., Risely, K. and Robinson, R. A. (2010). Breeding Birds in Wider Countryside: their Conservation Status. BTO Research Report No. 565. British Trust of Ornithology, Thetford, UK.Google Scholar
Boal, C. W., Mannan, R. W. and Hudelson, K. S. (1998). Trichomoniasis in Cooper's hawks from Arizona. Journal of Wildlife Diseases 34, 590–593.CrossRefGoogle ScholarPubMed
Carlton, J. M., Hirt, R. P., Silva, J. C., Delcher, A. L., Schatz, M., Zhao, Q., Wortman, J. R., Bidwell, S. L., Alsmark, U. C., Besteiro, S. et al. (2007). Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315, 207–212. doi: 10.1126/science.1132894.CrossRefGoogle ScholarPubMed
Cooper, J. E. and Petty, S. J. (1988). Trichomoniasis in free-living goshawks (Accipiter gentilis gentilis) from Great Britain. Journal of Wildlife Diseases 24, 80–87.CrossRefGoogle ScholarPubMed
Cotgreave, P. (1995). Relative importance of avian groups in the diets of British and Irish predators. Bird Study 42, 246–252.CrossRefGoogle Scholar
Ecco, R., Preis, I. S., Vilela, D. A., Luppi, M. M., Malta, M. C., Beckstead, R. B., Stimmelmayer, R. and Gerhold, R. W. (2012). Molecular confirmation of Trichomonas gallinae and other parabasalids from Brazil using the 5.8S and ITS-1 rRNA regions. Veterinary Parasitology 190, 36–42.CrossRefGoogle ScholarPubMed
Erwin, K. G., Kloss, C., Lyles, J., Felderhoff, J., Fedynich, A. M., Henke, S. E. and Roberson, J. A. (2000). Survival of Trichomonas gallinae in white-winged dove carcasses. Journal of Wildlife Diseases 36, 551–554.CrossRefGoogle ScholarPubMed
Felleisen, R. S. J. (1997). Comparative sequence analysis of 5.8S rRNA genes and internal transcribed spacer (ITS) regions of trichomonadid protozoa. Parasitology 115, 111–119.CrossRefGoogle ScholarPubMed
Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.CrossRefGoogle ScholarPubMed
Forzan, M., Vanderstichel, R., Melekhovets, Y. and McBurney, S. (2010). Trichomoniasis in finches from the Canadian Maritime provinces – an emerging disease. Canadian Veterinary Journal 51, 391–396.Google ScholarPubMed
Garner, M. M. and Sturtevant, F. C. (1992). Trichomoniasis in a blue-fronted Amazon parrot. Journal of the Association of Avian Veterinarians 6, 18–20.CrossRefGoogle Scholar
Gaspar da Silva, D., Barton, E., Bunbury, N., Lunness, P., Bell, D. J. and Tyler, K. M. (2007). Molecular identity and heterogeneity of trichomonad parasites in a closed avian population. Infection Genetics and Evolution 7, 433–440.CrossRefGoogle Scholar
Gerhold, R. W., Yabsley, M. J., Smith, A. J., Ostergaard, E., Mannan, W., Cann, J. D. and Fischer, J. R. (2008). Molecular characterization of the Trichomonas gallinae morphologic complex in the United States. Journal of Parasitology 94, 1335–1341.CrossRefGoogle ScholarPubMed
Grabensteiner, E., Bilic, I., Kolbe, T. and Hess, M. (2010). Molecular analysis of clonal trichomonad isolates indicate the existence of heterogenic species present in different birds and within the same host. Veterinary Parasitology 172, 53–64.CrossRefGoogle ScholarPubMed
Kleina, P., Bettim-Bandinelli, J., Bonatto, S. L., Benchimol, M. and Bogo, M. R. (2004). Molecular phylogeny of Trichomonadidae family inferred from ITS-1, 5.8S rRNA and ITS-2 sequences. International Journal for Parasitology 34, 963–970.CrossRefGoogle ScholarPubMed
Lawson, B., Cunningham, A. A., Chantrey, J., Hughes, L. A., John, S. K., Bunbury, N., Bell, D. J. and Tyler, K. M. (2011 a). A clonal strain of Trichomonas gallinae is the aetiologic agent of an emerging avian epidemic disease. Infection, Genetics and Evolution 11, 1638–1645.CrossRefGoogle ScholarPubMed
Lawson, B., Robinson, R. A., Neimanis, A., Handeland, K., Isomursu, M., Agren, E. O., Hamnes, I. S., Tyler, K. M., Chantrey, J., Hughes, L. A., Pennycott, T. W., Simpson, V. R., John, S. K., Peck, K. M., Toms, M. P., Bennett, M., Kirkwood, J. K. and Cunningham, A. A. (2011 b). Evidence of spread of the emerging infectious disease finch trichomonosis, by migrating birds. Ecohealth 8, 143–153.CrossRefGoogle ScholarPubMed
Lawson, B., Robinson, R. A., Colvile, K. M., Peck, K. M., Chantrey, J., Pennycott, T. W., Simpson, V. R., Toms, M. P. and Cunningham, A. A. (2012). The emergence and spread of finch trichomonosis in the British Isles. Philosophical Transactions of the Royal Society B 367, 2852–2863.CrossRefGoogle ScholarPubMed
Neimanis, A. S., Handeland, K., Isomursu, M., Agren, E., Mattsson, R., Hamnes, I. S., Bergsjo, B. and Hirvela-Koski, V. (2010). First report of epizootic trichomoniasis in wild finches (Family Fringillidae) in Southern Fennoscandia. Avian Diseases 54, 136–141.CrossRefGoogle ScholarPubMed
Peters, M., Kilwinski, J., Reckling, D. and Henning, K. (2009). Epidemic mortality in greenfinches at feeder stations caused by Trichomonas gallinae – a recent problem in Northern Germany. Kleintierpraxis 54, 433–438.Google Scholar
Robinson, R. A., Lawson, B., Toms, M. P., Peck, K. M., Kirkwood, J. K., Chantrey, J., Clatworthy, I. R., Evans, A. D., Hughes, L. A., Hutchinson, O. C., John, S. K., Pennycott, T. W., Perkins, M. W., Rowley, P. S., Simpson, V. R., Tyler, K. M. and Cunningham, A. A. (2010). Emerging infectious disease leads to rapid population declines of common British birds. PLoS ONE 5: e12215. doi: 10.1371/journal.pone.0012215.CrossRefGoogle ScholarPubMed
Saitou, N. and Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.Google Scholar
Saleem, M. H., Khan, M. S., Chaudry, A. S. and Samad, H. A. (2008). Prevalence of trichomoniasis in domestic and wild pigeons and its effects on hematological parameters. Pakistan Veterinary Journal 28, 89–91.Google Scholar
Sansano-Maestre, J., Garijo-Toledo, M. M. and Gomez-Munoz, M. T. (2009). Prevalence and genotyping of Trichomonas gallinae in pigeons and birds of prey. Avian Pathology 38, 201–207.CrossRefGoogle ScholarPubMed
Stabler, R. M. (1954). Trichomonas gallinae: a review. Experimental Parasitology 3, 368–402.CrossRefGoogle ScholarPubMed
Tamura, K., Nei, M. and Kumar, S. (2004). Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Science USA 101, 11030–11035.CrossRefGoogle ScholarPubMed
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011). MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.CrossRefGoogle ScholarPubMed
Voncken, F. G. J., Boxma, B., Van Hoek, A. H. A. M., Akhmanova, A. S., Vogels, G. D., Huynen, M., Veenhuis, M. and Hackstein, J. H. P. (2002). A hydrogenosomal [Fe]-hydrogenase from the anaerobic chytrid Neocallimastix sp. L2. Gene 284, 103–112.CrossRefGoogle ScholarPubMed