Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-17T05:53:14.824Z Has data issue: false hasContentIssue false
  • English
  • Français

Trichomonads in birds – a review

Published online by Cambridge University Press:  28 January 2014

AZIZA AMIN ,
IVANA BILIC ,
DIETER LIEBHART  and
MICHAEL HESS
AZIZA AMIN
Affiliation:
Clinic for Poultry and Fish Medicine, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, Vienna, Austria
IVANA BILIC
Affiliation:
Clinic for Poultry and Fish Medicine, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, Vienna, Austria
DIETER LIEBHART
Affiliation:
Clinic for Poultry and Fish Medicine, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, Vienna, Austria
MICHAEL HESS*
Affiliation:
Clinic for Poultry and Fish Medicine, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, Vienna, Austria
*
*Corresponding author: Clinic for Poultry and Fish Medicine, University of Veterinary Medicine, Veterinärplatz 1, 1210 Vienna, Austria. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Members of the family Trichomonadidae, mainly Trichomonas gallinae and Tetratrichomonas gallinarum, represent important parasites in birds with worldwide presence, since being reported in the 19th century. Especially Columbiformes, Falconiformes and Strigiformes can be severely affected by trichomonads, whereas the majority of infections in Galliformes and Anatiformes are subclinical although severe infections are occasionally reported. With the recent appearance of deadly infections in wild Passeriformes the protozoan parasite T. gallinae obtained greater attention which will be addressed in this review. Although light microscopy remains the method of choice to confirm the presence of trichomonads molecular studies were introduced in recent years, in order to characterize the parasites and to establish relationships between isolates. Isolation of trichomonads is a prerequisite for detailed in vitro and in vivo studies and different media are reported to obtain suitable material. The limited information about virulence factors will be reviewed in context with the pathogenicity of trichomonads which varies greatly, indicating certain strain heterogeneity of the parasites. Options for treatment characterized by the leading role of imidazoles whose activity is sometimes hampered by resistant parasites remains a challenge for the future. Introducing more standardized genetic studies and investigations concentrating on the host-pathogen interaction should be helpful to elucidate virulence factors which might lead to new concepts of treatment.

Keywords

Trichomonas gallinaeTetratrichomonas gallinarummorphologyepidemiology and transmissionpathogenicitydiagnosticsgeneticstreatmentreview
Type
Review Article
Information
Parasitology , Volume 141 , Issue 6 , May 2014 , pp. 733 - 747
Copyright
Copyright © Cambridge University Press 2014 

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

Abraham, R. and Honigberg, M. (1964). Structure of Trichomonas gallinae (Rivolta). Journal of Parasitology 55, 608–619.Google Scholar
Allen, A. (1941). Macroscopic differentiation of lesions of histomoniasis and trichomoniasis in turkeys. American Journal of Veterinary Research 2, 214–217.Google Scholar
Amin, A., Neubauer, C., Liebhart, D., Grabensteiner, E. and Hess, M. (2010). Axenization and optimization of in vitro growth of clonal cultures of Tetratrichomonas gallinarum and Trichomonas gallinae . Experimental Parasitology 124, 202–208.CrossRefGoogle ScholarPubMed
Amin, A., Liebhart, D., Weissenbock, H. and Hess, M. (2011). Experimental infection of turkeys and chickens with a clonal strain of Tetratrichomonas gallinarum induces a latent infection in the absence of clinical signs and lesions. Journal of Comparative Pathology 144, 55–62. doi: 10.1016/j.jcpa.2010.06.002.Google Scholar
Amin, A., Bilic, I., Berger, E. and Hess, M. (2012 a). Trichomonas gallinae in comparison to Tetratrichomonas gallinarum induces distinctive cythopathogenic effects in tissue cultures. Veterinary Parasitology 168, 196–206.Google Scholar
Amin, A., Nobauer, K., Patzl, M., Berger, E., Hess, M. and Bilic, I. (2012 b). Cysteine peptidases, secreted by Trichomonas gallinae, are involved in the cytopathogenic effects on a permanent chicken liver cell culture. PLoS ONE 7, e37417. doi: 10.1371/journal.pone.0037417.Google Scholar
Anderson, L., Grahn, A., Van Hoosear, K. and Bondurant, 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.Google Scholar
Anonymous, A. (2006). Veterinary Laboratory Surveillance Report for August. Veterinary Record 159, 507–510.Google Scholar
Bailey, T. C., Samour, J. H., Bailey, T. A., Remple, J. D. and Remple, J. D. (2000). Trichomonas sp. and falcon health in the United Arab Emirates. In Raptor Biomedicine 3 (ed. Lumeij, J. T., Remple, J. D., Redig, R. T., Lierz, M. and Cooper, J. E.), pp. 53–57. Zoological Education Network, Inc., Lake Worth, FL, USA.Google Scholar
Begum, N., Mamun, A., Rahman, A. and Bari, M. (2008). Epidemiology and pathology of Trichomonas gallinae in the common pigeon (Columba livia). Journal of Bangladesh Agricultural University 6, 301–306.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.Google Scholar
Bondarenko, I. (1964). Pathogenicity and specificity of trichomonads in chickens and ducks. Veterinariya (Moscow) 41, 64–65.Google Scholar
Bondurant, R. H. and Honigberg, B. M. (1994). Trichomonads of veterinary importance. In Parasitic Protozoa (ed. Kreier, J. P.), pp. 111–188. Academic Press, New York, NY, USA.Google Scholar
Borchardt, K. A. and Smith, R. F. (1991). An evaluation of an InPouch TV culture method for diagnosing Trichomonas vaginalis infection. Genitourinary Medicine 67, 149–152.Google ScholarPubMed
Borji, H., Razmi, G. H., Movassaghi, A. H., Moghaddas, E. and Azad, M. (2011). Prevalence and pathological lesion of Trichomonas gallinae in pigeons of Iran. Journal of Parasitology Diseases 35, 186–189.Google Scholar
Brugerolle, G. and Müller, M. (2000). Amitochondriate flagellates. In The Flagellates (ed. Leadbeater, B. S. C. and Green, J. C.), pp. 166–189. Taylor and Francis, London, UK.Google ScholarPubMed
Bunbury, N., Bell, D., Jones, C., Greenwood, A. and Hunter, P. (2005). Comparison of the InPouch TF culture system and wet-mount microscopy for diagnosis of Trichomonas gallinae infections in the pink pigeon Columba mayeri . Journal of Clinical Microbiology 43, 1005–1006. doi: 10.1128/JCM.43.2.1005-1006.2005.Google Scholar
Bunbury, N., Jones, C. G., Greenwood, A. G. and Bell, D. J. (2007). Trichomonas gallinae in Mauritian columbids: implications for an endangered endemic. Journal of Wildlife Diseases 43, 399–407.Google Scholar
Burns, R. E., Braun, J., Armien, A. G. and Rideout, B. A. (2013). Hepatitis and splenitis due to systemic tetratrichomoniasis in an American white pelican (Pelecanus erythrorhynchos). Journal of Veterinary Diagnostic Investigations 25, 511–514. doi: 10.1177/1040638713488368.Google Scholar
Cauthen, G. (1936). Studies on Trichomonas columbae, a flagellate parasitic in pigeons and doves. American Journal of Hygiene 23, 132–142.Google Scholar
Cepicka, I., Kutisova, K., Tachezy, J., Kulda, J. and Flegr, J. (2005). Cryptic species within the Tetratrichomonas gallinarum species complex revealed by molecular polymorphism. Veterinary Parasitology 128, 11–21.Google Scholar
Cepicka, I., Hampl, V., Kulda, J. and Flegr, J. (2006). New evolutionary lineages, unexpected diversity, and host specificity in the parabasalid genus Tetratrichomonas. Molecular Phylogenetics and Evolution 39, 542–551.Google Scholar
Cepicka, I., Hampl, V. and Kulda, J. (2010). Critical taxonomic revision of Parabasalids with description of one new genus and three new species. Protist 161, 400–433. doi: 10.1016/j.protis.2009.11.005.Google Scholar
Chi, J. F., Lawson, B., Durrant, C., Beckmann, K., Alrefaei, A. F., Kirkbride, K., Bell, D. J., Cunningham, A. A. and Tyler, K. M. (2013). The finch epidemic strain of Trichomonas gallinae is predominant in British non-passerines. Parasitology 140, 1234–1245.Google Scholar
Clark, S., De Gussem, K. and Barnes, J. (2003). Flagellated protozoan infections in turkeys. World Poultry – Turkey Special 5, 20–23.Google Scholar
Cole, R. and Friend, M. (1999). Trichomoniasis. In Field Manual of Wildlife Diseases (ed. Friend, M. and Franson, J. C.), pp. 201–206. USGS-National Wildlife Health Center, Washington, DC, USA.Google Scholar
Conti, J. A. and Forrester, D. J. (1981). Interrelationships of parasites of white-winged doves and mourning doves in Florida. Journal of Wildlife Diseases 17, 529–536.Google Scholar
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
Cree, G. E. (1968). Trichomomas vaginalis in gram-stained smears. British Journal of Venereal Diseases 44, 226–227.Google Scholar
Crespo, R., Walker, R. L., Nordhausen, R., Sawyer, S. J. and Manalac, R. B. (2001). Salpingitis in Pekin ducks associated with concurrent infection with Tetratrichomonas sp. and Escherichia coli. Journal of Veterinary Diagnostic Investigation 13, 240–245.Google Scholar
De Carli, G. A. and Tasca, T. (2002). Trichomonas gallinae: a possible contact-dependent mechanism in the hemolytic activity. Veterinary Parasitology 106, 277–283.Google Scholar
De Carli, G. A., da Silva, A. C., Wendorff, A. and Rott, M. (1996). Lysis of erythrocytes by Trichomonas gallinae . Avian Diseases 40, 228–230.CrossRefGoogle ScholarPubMed
Delgado-Viscogliosi, P., Viscogliosi, E., Gerbod, D., Kulda, J., Sogin, M. L. and Edgcomb, V. P. (2000). Molecular phylogeny of parabasalids based on small subunit rRNA sequences, with emphasis on the Trichomonadinae subfamily. Journal of Eukaryotic Microbiology 47, 70–75.Google Scholar
Diamond, L. S. (1957). The establishment of various trichomonads of animals and man in axenic cultures. Journal of Parasitology 43, 488–490.Google Scholar
Donald, G. L. and Miklos, M. (1973). Hydrogenosomes, a cytoplasmic orgenelle of the anaerobic flagellate Tritrichomonas foetus, and its role in pyruvate metabolism. Journal of Biological Chemistry 248, 7724–7728.Google Scholar
Dwyer, M. (1974). Analysis of the antigenic relationships among Trichomonas, Histomonas, Dientamoeba, and Entamoeba . Journal of Protozoology 21, 139–145.Google 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 Parasitolology 190, 36–42. doi: 10.1016/j.vetpar.2012.05.029.Google Scholar
Edgcomb, V. P., Roger, A. J., Simpson, A. J. B., Kysela, D. T. and Sogin, M. L. (2001). Evolutionary relationships among “jakobid” flagellates as indicated by alpha- and beta-tubulin phylogenies. Molecular Biology and Evolution 18, 514–522.Google Scholar
Erwin, G., Kloss, C., Lyles, J., Felderhoff, J., Fedynich, M., Henke, E. and Roberson, A. (2000). Survival of Trichomonas gallinae in white-winged dove carcasses. Journal of Wildlife Diseases 36, 551–554.Google Scholar
Estes, W. A. and Mannan, R. W. (2003). Feeding behavior of Cooper's hawks at urban and rural nests in southeastern Arizona. Condor 105, 107–116.Google Scholar
Felleisen, R. S. (1997). Comparative sequence analysis of 5.8S rRNA genes and internal transcribed spacer (ITS) regions of trichomonadid protozoa. Parasitology 115 (Pt 2), 111–119.Google Scholar
Forrester, D. J. and Foster, G. W. (2008). Trichomonosis. In Parasitic Diseases of Wild Birds (ed. Atkinson, C. T., Thomas, N. J. and Hunter, D. B.), pp. 120–153. Wiley-Blackwell, Ames, IA, USA.Google Scholar
Forzan, M. J., Vanderstichel, R., Melekhovets, Y. F. and McBurney, S. (2010). Trichomoniasis in finches from the Canadian Maritime provinces – an emerging disease. Canadian Veterinary Journal 51, 391–396.Google Scholar
Fouts, A. C. and Kraus, S. J. (1980). Trichomonas vaginalis: reevaluation of its clinical presentation and laboratory diagnosis. Journal of Infectious Diseases 141, 137–143.CrossRefGoogle ScholarPubMed
Franssen, F. and Lumeij, T. (1992). In vitro nitroimidazole resistance of Trichomonas gallinae and successful therapy with an increased dosage of ronidazole in racing pigeons (Columba livia domestica). Journal of Veterinary Pharmacology and Therapeutics 15, 409–415.Google Scholar
Friedhoff, K. T. (1982). Pathogene, intestinale Flagellaten bei Tauben, Sittichen und Papageien. Collegium Veterinarium 63, 329–334.Google Scholar
Friedhoff, K. T., Kuhnigk, C. and Muller, I. (1991). Experimental infections in chickens with Chilomastix gallinarum, Tetratrichomonas gallinarum, and Tritrichomonas eberthi . Parasitology Research 77, 329–334.Google Scholar
Frost, J. K. and Honigberg, B. M. (1962). Comparative pathogenicity of Trichomonas vaginalis and Trichomonas gallinae to mice. II. Histopathology of subcutaneous lesions. Journal of Parasitology 48, 898–918.Google 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.Google Scholar
Gerbod, D., Sanders, E., Moriya, S., Noel, C., Takasu, H., Fast, N. M., Delgado-Viscogliosi, P., Ohkuma, M., Kudo, T., Capron, M., Palmer, J. D., Keeling, P. J. and Viscogliosi, E. (2004). Molecular phylogenies of Parabasalia inferred from four protein genes and comparison with rRNA trees. Molecular Phylogenetics and Evolution 31, 572–580. doi: 10.1016/j.ympev.2003.09.013.Google Scholar
Gerhold, R. W., Allison, A. B., Sellers, H., Linnemann, E., Chang, T. H. and Alderete, J. F. (2009). Examination for double-stranded RNA viruses in Trichomonas gallinae and identification of a novel sequence of a Trichomonas vaginalis virus. Parasitology Research 105, 775–779. doi: 10.1007/s00436-009-1454-5.Google Scholar
Gerhold, W., Tate, M., Gibbs, E., Mead, G., Allison, B. and Fischer, R. (2007 a). Necropsy findings and arbovirus surveillance in mourning doves from the southeastern United States. Journal of Wildlife Diseases 43, 129–135.Google Scholar
Gerhold, W., Yabsley, J., and Fischer, R. (2007 b). Hemolytic activity of Trichomonas gallinae isolates does not correspond with clinical virulence. Veterinary Parasitology 160, 221–224.Google Scholar
Gerhold, W., Yabsley, J., Smith, J., Ostergaard, E., Mannan, W., Cann, D. and Fischer, R. (2008). Molecular characterization of the Trichomonas gallinae morphologic complex in the United States. Journal of Parasitology 94, 1335–1341.Google Scholar
Goedbloed, E. and Bool, P. H. (1962). The protozoan etiology of blackhead. Avian Diseases 6, 302–315.Google Scholar
Goldman, M. and Honigberg, B. M. (1968). Immunologic analysis by gel diffusion technics of the effects of prolonged cultivation on Trichomonas gallinae . Journal of Protozoology 15, 350–352.Google Scholar
Gourlay, P., Decors, A., Jouet, D., Treilles, D., Lemberger, K., Faure, E., Moinet, M., Chi, J., Tyler, K., Cunningham, A. and Lawson, B. (2011). Finch trichomonosis spreads to France. European Section of Wildlife Disease Association Bulletin 1, 9–10.Google Scholar
Grabensteiner, E. and Hess, M. (2006). PCR for the identification and differentiation of Histomonas meleagridis, Tetratrichomonas gallinarum and Blastocystis spp. Veterinary Parasitology 142, 223–230.CrossRefGoogle ScholarPubMed
Grabensteiner, E., Bilic, I., Kolbe, T. and Hess, M. (2010). Molecular analysis of clonal trichomonad isolates indicates the existence of heterogenic species present in different birds and within the same host. Veterinary Parasitology 172, 53–64.Google Scholar
Hamilton, A. and Stabler, M. (1953). Combined trichomoniasis and aspergillosis in a gyrfalcon. Journal of Colo-wyo Academic Science 4, 206–209.Google Scholar
Harmon, M., Clark, A., Hawbecker, C. and Stafford, M. (1987). Trichomonas gallinae in columbiform birds from the Galapagos Islands. Journal of Wildlife Diseases 23, 492–494.Google Scholar
Hauck, R., Balczulat, S. and Hafez, H. M. (2010). Detection of DNA of Histomonas meleagridis and Tetratrichomonas gallinarum in German poultry flocks between 2004 and 2008. Avian Diseases 54, 1021–1025.CrossRefGoogle ScholarPubMed
Hawn, C. (1937). Trichomoniasis of turkeys. Journal of Infectious Diseases 61, 184–197.Google Scholar
Hegemann, A., Hegemann, E. D. and Krone, O. (2007). Trichomonosis in a free-living Stock Dove (Columba oneas). European Journal of Wildlife Research 53, 235–237.Google Scholar
Hess, M., Kolbe, T., Grabensteiner, E. and Prosl, H. (2006). Clonal cultures of Histomonas meleagridis, Tetratrichomonas gallinarum and a Blastocystis sp. established through micromanipulation. Parasitology 133, 547–554.Google Scholar
Höfle, U., Blanco, J., Palma, L. and Melo, P. (2000). Trichomoniasis in Bonelli´s eagle nestlings in south-west Portugal. In Raptor Biomedicine III (ed. Redig, P. T., Cooper, J. E. and Remple, T. D.), pp. 45–51. University of Minnesota Press, Minneapolis, MN, USA.Google Scholar
Höfle, U., Gortazar, C., Ortíz, J., Knispel, B. and Kaleta, E. F. (2004). Outbreak of trichomoniasis in a woodpigeon (Columba palumbus) wintering roost. European Journal of Wildlife Research 50, 73–77.Google Scholar
Honigberg, B. M. (1961). Comparative pathogenicity of Trichomonas vaginalis and Trichomonas gallinae to mice. I. Gross pathology, quantitative evaluation of virulence, and some factors affecting pathogenicity. Journal of Parasitology 47, 545–571.Google Scholar
Honigberg, B. M. (1963). Evaluation and systemic relationships in the flagellate order Trichomondida Kirby. Journal of Protozoology 10, 20–63.Google Scholar
Honigberg, B. M. (1978). Trichomonads of importance in human medicine. In Parasitic Protozoa (ed. Kreier, J. P.), pp. 275–454. Academic Press, New York, NY, USA.Google Scholar
Honigberg, B. M., Becker, D., Livingston, C. and McLure, T. (1964). The behavior and pathogenicity of two strains of Trichomonas gallinae in cell culture. Journal of Protozoology 11, 447–465.Google Scholar
Jaquette, S. (1948). Copper sulfate as a treatment for subclinical trichomoniasis in pigeons. American Journal of Veterinary Research 9, 206–209.Google Scholar
Jaquette, S. (1950). Hepatic trichomoniasis in esophagotomized pigeons. Poultry Science 39, 157–158.CrossRefGoogle Scholar
Karen, C., Meysick, K. and Garber, G. (1990). Growth of Trichomonas vaginalis in a serum-free McCoy cell culture system. Journal of Parasitology 76, 926–928.Google Scholar
Kaufman, R. H., Faro, S. and Brown, D. (2004). Benign Diseases of the Vulva and Vagina, 5th Edn. Mosby, Maryland Heights, MO, USA.Google Scholar
Kemp, L. and Reid, M. (1965). Pathogenicity studies on Trichomonas gallinarum in domestic poultry. Poultry Science 44, 215–221.Google Scholar
Kirk, O. (1962). Effect of streptomycin on leucine incorporation in Euglena gracilis . Biochemica et Biophysica Acta 59, 476–479.Google Scholar
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 of Parasitology 34, 963–970. doi: 10.1016/j.ijpara.2004.04.004.Google Scholar
Krieger, J., Poisson, M. and Rein, M. (1983). Beta-hemolytic activity of Trichomonas vaginalis correlates with virulence. Infection and Immunity 41, 1291–1295.Google Scholar
Krone, O., Altenkamp, R. and Kenntner, N. (2005). Prevalence of Trichomonas gallinae in northern goshawks from the Berlin area of northeastern Germany. Journal of Wildlife Diseases 41, 304–309.Google Scholar
Kulda, J. (1967). Effect of different species of trichomonads on monkey kidney cell cultures. Folia Parasitology 14, 295–310.Google Scholar
Kulda, J. (1999). Trichomonads, hydrogenosomes and drug resistance. International Journal of Parasitology 29, 199–212.Google Scholar
Kulda, J., Suchankova, S. and Svoboda, S. (1974). Studies on pathogenicity of Tetratrichomonas gallinarum in mice and turkey poults. Acta Veterinary Brno 43, 53–64.Google Scholar
Kulda, J., Cerkasov, J., Demes, P. and Cerkasovova, A. (1984). Tritrichomonas foetus: stable anaerobic resistance to metronidazole in vitro . Experimental Parasitology 57, 93–103.CrossRefGoogle ScholarPubMed
Kulda, J., Tachezy, J. and Cerkasovova, A. (1993). In vitro induced anaerobic resistance to metronidazole in Trichomonas vaginalis . Journal of Eukaryotic Microbiology 40, 262–269.Google Scholar
Laing, S. T., Weber, E. S. III, Yabsley, M. J., Shock, B. C., Grosset, C., Petritz, O. A., Barr, B., Reilly, C. M. and Lowenstine, L. J. (2013). Fatal hepatic tetratrichomoniasis in a juvenile Waldrapp ibis (Geronticus eremita). Journal of Veterinary Diagnostic Investigation 25, 277–281. doi: 10.1177/1040638713476711.CrossRefGoogle Scholar
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. doi: 10.1016/j.meegid.2011.06.007.Google Scholar
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. doi: 10.1007/s10393-011-0696-8.Google Scholar
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: Biological Sciences 367, 2852–2863. doi: 10.1098/rstb.2012.0130.Google Scholar
Lee, D. L. (1972). Changes in the ultrastructure of the caecum of chickens caused by Trichomonas gallinarum . Parasitology 65, 71–76.Google Scholar
Lehikoinen, A., Lehikoinen, E., Valkama, J., Väisänen, R. A. and Isomursu, M. (2013). Impacts of trichomonosis epidemics on greenfinch Chloris chloris and chaffinch Fringilla coelebs populations in Finland. IBIS The International Journal of Avian Science 155, 357–366.Google Scholar
Leibovitz, L. (1973). Necrotic enteritis of breeder ducks. American Journal of Veterinary Research 34, 1053–1061.Google Scholar
Lennon, R. J., Dunn, J. C., Stockdale, J. E., Goodman, S. J., Morris, A. J. and Hamer, K. C. (2013). Trichomonad parasite infection in four species of Columbidae in the UK. Parasitology 140, 1368–1376. doi: 10.1017/S0031182013000887.Google Scholar
Levine, D. (1985). Veterinary Protozoology. Iowa State Press, Iowa City, IA, USA.Google Scholar
Levine, D. and Brandly, A. (1939). A pathogenic Trichomonas from the upper digestive tract of chickens. Journal of American Veterinary Medicine Association 95, 77–78.Google Scholar
Liebhart, D., Weissenbock, H. and Hess, M. (2006). In-situ hybridization for the detection and identification of Histomonas meleagridis in tissues. Journal of Comparative Pathology 135, 237–242.Google Scholar
Lockwood, B., North, M. and Coombs, G. (1984). Trichomonas vaginalis, Tritrichomonas foetus, and Trichomitus batrachorum: comparative proteolytic activity. Experimental Parasitology 58, 245–253.Google Scholar
Lumeij, T. and Zwijnenberg, G. (1990). Failure of nitro-imidazole drugs to control trichomoniasis in the racing pigeon (Columba livia domestica). Avian Pathology 19, 165–166.Google Scholar
Malik, S. B., Brochu, C. D., Bilic, I., Yuan, J., Hess, M., Logsdon, J. M. Jr. and Carlton, J. M. (2011). Phylogeny of parasitic parabasalia and free-living relatives inferred from conventional markers vs. Rpb1, a single-copy gene. PLoS ONE 6, e20774. doi: 10.1371/journal.pone.0020774.Google Scholar
Martin, C. and Robertson, M. (1911). Further observations on the caecal parasites of fowls, with some reference to the rectal fauna of other vertebrates. Quarterly Journal of Microscopical Sciences 57, 53–81.Google Scholar
McDougald, L. R. (2008). Histomoniasis (Blackhead) and other protozoan diseases of the intestinal tract. In Diseases of Poultry (ed. Saif, Y. M., Fadly, A. M., Glisson, J. R., McDougald, L. R., Nolan, L. K. and Swayne, D. E.), pp. 1095–1105. Blackwell, Ames, IA, USA.Google Scholar
McDowell, S. (1953). Morphological and taxonomic study of the caecal protozoa of the common fowl, Gallus gallus . Journal of Morphology 92, 337–399.Google Scholar
McKeon, T., Dunsmore, J. and Raidal, S. R. (1997). Trichomonas gallinae in budgerigars and columbid birds in Perth, Western Australia. Australian Veterinary Journal 75, 652–655.Google Scholar
Mehlhorn, H., Al-Quraishy, S., Amin, A. and Michael, H. (2009). Fine structure of the bird parasites Trichomonas gallinae and Tetratrichomonas gallinarum from cultures. Parasitology Research 105, 751–756.Google Scholar
Müller, M. (1990). Biochemistry of Trichomonas vaginalis . In Trichomonads Parasitics in Humans (ed. Honigberg, B. M.), pp. 53–83. Springer, New York, N, USA.Google Scholar
Müller, M. (1993). The hydrogenosome. Journal of General Microbiology 139, 2879–2889.Google Scholar
Munoz, E., Castella, J. and Gutierrez, J. F. (1998). In vivo and in vitro sensitivity of Trichomonas gallinae to some nitroimidazole drugs. Veterinary Parasitology 78, 239–246.Google Scholar
Narcisi, M., Sevoian, M. and Honigberg, B. M. (1991). Pathologic changes in pigeons infected with a virulent Trichomonas gallinae strain (Eiberg). Avian Diseases 35, 55–61.Google Scholar
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.Google Scholar
Noda, S., Mantini, C., Meloni, D., Inoue, J., Kitade, O., Viscogliosi, E. and Ohkuma, M. (2012). Molecular phylogeny and evolution of parabasalia with improved taxon sampling and new protein markers of actin and elongation factor-1 alpha. PLoS ONE 7, e29938. doi: 10.1371/journal.pone.0029938.Google Scholar
North, M. (1982). Comparative biochemistry of the proteinases of eucaryotic microorganisms. Microbiological Reviews 46, 308–340.Google Scholar
Norton, A. (1997). Pathogenicity of a strain of Trichomonas gallinarum in turkeys and its possible interaction with cecal coccidia. Avian Diseases 41, 670–675.Google Scholar
Park, F. J. (2011). Avian trichomoniasis: a study of lesions and relative prevalence in a variety of captive and free-living bird species as seen in an Australian avian practice. Australian Veterinary Journal 89, 82–88. doi: 10.1111/j.1751-0813.2010.00681.x.Google Scholar
Patton, C. S. and Patton, S. (1996). Tetratrichomonas gallinarum encephalitis in a mockingbird (Mimus polyglottos). Journal of Veterinary Diagnostic Investigation 8, 133–137.Google Scholar
Peters, M., Kilwinski, J., Reckling, D. and Henning, K. (2009). Gehäufte Todesfälle von wild lebenden Grünfinken an Futterstellen infolge Trichomonas-gallinae-Infektionen – ein aktuelles Problem in Norddeutschland. Kleintierpraxis 54, 433–438.Google Scholar
Peterson, K. and Alderete, J. (1984). Trichomonas vaginalis is dependent on uptake and degradation of human low density lipoproteins. Journal of Experimental Medicine 160, 1261–1272.Google Scholar
Pindak, F., Gardner, W. and Pindak de Mora, M. (1986). Growth and cytopathogenicity of Trichomonas vaginalis in tissue cultures. Journal of Clinical Microbiology 23, 672–678.Google Scholar
Provenzano, D. and Alderete, F. (1995). Analysis of human immunoglobulin-degrading cysteine protinases of Trichomonas vaginalis . Infection and Immunity 63, 3388–3395.Google Scholar
Real, J. and Manosa, S. (1997). Demography and conservation of western European Bonelli's eagle (Hieraaetus fasciatus) populations. Biological Conservation 97, 59–66.Google Scholar
Real, J., Manosa, S. and Munoz, E. (2000). Trichomoniasis in a Bonelli's eagle population in Spain. Journal of Wildlife Diseases 36, 64–70.Google Scholar
Reece, R. L., Barr, D. A., Forsyth, W. M. and Scott, P. C. (1985). Investigations of toxicity episodes involving chemotherapeutic agents in Victorian poultry and pigeons. Avian Diseases 28, 1239–1252.Google Scholar
Richter, B., Schulze, C., Kammerling, J., Mostegl, M. and Weissenbock, H. (2010). First report of typhlitis/typhlohepatitis caused by Tetratrichomonas gallinarum in three duck species. Avian Pathology 39, 499–503. doi: 10.1080/03079457.2010.518137.Google Scholar
Rivolta, S. (1878). Una forma di croup prodotta da un infusorio. Giornale d'anatomia fisiologia e patologia degli animali 10, 149–154.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.Google Scholar
Rosenwald, S. (1944). Veterinary problems in a signal pigeon company. Journal of American Veterinary Medicine Association 104, 141–143.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.Google Scholar
Schulz, H., Bermudez, J. and Millspaugh, J. (2005). Monitoring presence and annual variation of trichomoniasis in mourning doves. Avian Diseases 49, 387–389.Google Scholar
Simpson, V. and Molenaar, F. (2006). Increase in trichomonosis in finches. Veterinary Record 159, 606.Google Scholar
Stabler, M. (1938). Trichomonas gallinae (Rivolta, 1878) the correct name for the flagellate in the mouth, crop and liver of the pigeon. Journal of Parasitology 24, 553–554.Google Scholar
Stabler, M. (1941). The morphology of Trichomonas gallinae (=Columbae). Journal of Morphology 69, 501–515.Google Scholar
Stabler, M. (1947). Trichomonas gallinae, pathogenic trichomonad of birds. Journal of Parasitology 3, 207–213.Google Scholar
Stabler, M. (1948). Protection in pigeons against virulent Trichomonas gallinae acquired by infection with milder strains. Journal of Parasitology 34, 150–153.Google Scholar
Stabler, M. (1954). Trichomonas gallinae: a review. Experimental Parasitology 3, 368–402.Google Scholar
Stabler, M. and Engley, B. (1946). Studies on Trichomonas gallinae infection in pigeon squabs. Journal of Parasitology 36, 25–26.Google Scholar
Stabler, M., Honigberg, B. M. and King, M. (1964). Effect of certain laboratory procedures on virulence of Jones’ barn strain of Trichomonas gallinae for pigeons. Journal of Parasitology 50, 36–41.Google Scholar
Stepkowski, S. and Honigberg, B. M. (1972). Antigenic analysis of virulent and avirulent strains of Trichomonas gallinae by gel diffusion methods. Journal of Protozoology 19, 306–315.Google Scholar
Stimmelmayr, R., Stefani, L. M., Thrall, M. A., Landers, K., Revan, F., Miller, A., Beckstead, R. and Gerhold, R. (2012). Trichomonosis in free-ranging Eurasian collared doves (Streptopelia decaocto) and African collared dove hybrids (Streptopelia risoria) in the Caribbean and description of ITS-1 region genotypes. Avian Diseases 56, 441–445.Google Scholar
Swinnerton, K. J., Greenwood, A. G., Chapman, R. E. and Jones, C. G. (2005). The incidence of the parasitic disease trichomoniasis and its treatment in reintroduced and wild Pink pigeons Columba mayeri . Ibis 147, 772–782.Google Scholar
Tasca, T. and De Carli, G. (2001). Growth kinetic study of Tetratrichomonas didelphidis isolated from opossum Lutreolina crassicaudata and interaction with a prokaryotic cell. Parasitology Research 87, 626–630.Google Scholar
Tasca, T. and De Carli, G. (2003). Scanning electron microscopy study of Trichomonas gallinae . Veterinary Parasitology 118, 37–42.Google Scholar
Theodorides, J. (1964). Axenic culture of Tetratrichomonas gallinarum: growth and anaerobic utilization of carbohydrates and related compounds. Experimental Parasitology 15, 397–402.Google Scholar
Theodorides, J. and Olson, A. (1965). Observations on the size of Tetratrichomonas gallinarum . Avian Diseases 9, 232–236.Google Scholar
Thomford, W., Talbot, A., Ikeda, S. and Corbeil, B. (1996). Characterization of extracellular proteinases of Tritrichomonas foetus . Journal of Parasitology 82, 112–117.Google Scholar
Tyzzer, E. (1920). The flagellate character and reclassification of the parasite producing “blackhead” in turkeys – Histomonas (gen. nov.) meleagridis (Smith). Journal of Parasitology 6, 124–131.Google Scholar
Tyzzer, E. (1934). Studies on histomoniasis or blackhead infection, in the chicken and the turkey. Proceedings of the American Academy of Arts and Sciences 69, 189–264.Google Scholar
Villanua, D., Hofle, U., Perez-Rodriguez, L. and Gortazar, C. (2006). Trichomonas gallinae in wintering common wood pigeons (Columba palumbus) in Spain. Journal of Parasitology 148, 641–648.Google Scholar
Vogel, K. (1992). Trichomoniasis. In Krankheiten des Wirtschaftsgeflügels (ed. Heider, G. and Monreal, G.), pp. 352–363. Gustav Fischer Verlag, Jena, Germany.Google Scholar
Wang, A., Wand, C. C. and Alderete, J. F. (1987). Trichomonas vaginalis phenotypic variation occurs only among trichomonads infected with double-stranded RNA virus. Journal of Experimental Medicine 166, 142–150.Google Scholar
Weinzirl, J. (1917). Trichomoniasis of chicks. Journal of Bacteriology 2, 441–445.Google Scholar
Wieliczko, A., Piasecki, A., Dorrestein, G. M., Adamski, A. and Mazurkiewcz, A. (2003). Evaluation of the health status of Goshawk (Accipiter gentilis) nestlings in Wrocław vicinity. Bulletin of the Veterinary Institute in Pulawy 47, 247–257.Google Scholar
Work, T. and Hale, J. (1996). Causes of owl mortality in Hawaii, 1992 to 1994. Journal of Wildlife Diseases 32, 266–273.Google Scholar
Zadravec, M., Marhold, C., Slavec, B., Rojs, O. Z. and Racnik, J. (2012). Trichomonosis in finches in Slovenia. Veterinary Record 171, 253–254. doi: 10.1136/vr.e5973.Google Scholar
Zimre-Grabensteiner, E., Arshad, N., Amin, A. and Hess, M. (2011). Genetically different clonal isolates of Trichomonas gallinae, obtained from the same bird, can vary in their drug susceptibility, an in vitro evidence. Parasitology International 60, 213–215.Google Scholar
Supplementary material: File

Amin Supplementary Material

Figure

Download Amin Supplementary Material(File)
File 12.2 KB