Research Article
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Molecular Prevalence of Three Chicken Gastrointestinal Tract Pathogens and Phylogenetic Characterization of Tetratrichomonas gallinarum in Türkiye

Year 2023, Volume: 20 Issue: 1, 13 - 18, 23.06.2023
https://doi.org/10.34233/jpr.1302448

Abstract

Several species of parasites infect chickens and can cause economic losses. Histomonas meleagridis, its intermediate host Heterakis gallinarum, and Tetratrichomonas gallinarum are the most common parasites of poultry. The current study aimed to determine the molecular prevalence and phylogenetic relationships of H. meleagridis, He. gallinarum, and T. gallinarum in chickens in Central Anatolia Region of Türkiye. For this, a total of 100 fecal specimens from chickens were analyzed by using a PCR assay targeting the 18S rRNA gene region of H. meleagridis and T. gallinarum and the mtDNA COI gene region of He. gallinarum. PCR analysis identified T. gallinarum in 11 (1.1%) specimens, whereas other species were not found in all the examined specimens. Positive specimens were detected only in backyard chickens. Sequence analyses identified two novel genotypes named TRTgal1 and TRTgal3, and one known genotype (TRTgal2) of T. gallinarum. The TRTgal2 genotype was found to be identical to the human genotype (AY247746) and the four avian genotypes. Phylogenetic analyses of the obtained genotypes clustered in separate monophyletic clades. Our study provides the first data on T. gallinarum in chickens in Türkiye and contributes to public health with the identified zoonotic genotype and knowledge of the epidemiology of this parasite.

Supporting Institution

This research project was supported by the Kirsehir Ahi Evran University Scientific and Technological Research Fund with the project code KMY.A4.21.004.

Project Number

project code KMY.A4.21.004.

Thanks

We thank Kamila Bobrek (Department of Epizootiology and Clinic of Bird and Exotic Animals, Wrocław University of Environmental and Life Sciences, Poland) for sending us a positive specimen of H. meleagridis and He. gallinarum, and also thank Adnan Ayan (Department of Genetics, Faculty of Veterinary Medicine, Van Yüzüncü Yıl University, Turkey) for sending us a positive specimen of T. gallinarum.

References

  • Amin, A., Liebhart, D., Weissenböck, H., & 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(1), 55-62. https://doi.org/10.1016/j.jcpa.2010.06.002
  • Burns, R. E., Braun, J., Armién, A. G., & Rideout, B. A., (2013). Hepatitis and splenitis due to systemic tetratrichomoniasis in an American white pelican (Pelecanus erythrorhynchos). Journal of Veterinary Diagnostic Investigation, 25(4), 511-514. DOI: 10.1177/1040638713488368
  • Cupo, K. L., & Beckstead, R. B., (2019). Heterakis gallinarum, the cecal nematode of gallinaceous birds: a critical review. Avian Diseases, 63(3), 381-388. https://doi.org/10.1637/0005-2086-63.3.381 Cepicka, I., Kutišová, K., Tachezy, J., Kulda, J., & Flegr, J., (2005). Cryptic species within the Tetratrichomonas gallinarum species complex revealed by molecular polymorphism. Veterinary Parasitology, 128(1-2), 11-21. https://doi.org/10.1016/j.vetpar.2004.11.003
  • Cepicka, I., Hampl, V., & Kulda, J. (2010). Critical taxonomic revision of parabasalids with description of one new genus and three new species. Protist, 161(3), 400-433. https://doi.org/10.1016/j.protis.2009.11.005
  • Daş, G., Wachter, L., Stehr, M., Bilic, I., Grafl, B., Wernsdorf, P., & Liebhart, D. (2021). Excretion of Histomonas meleagridis following experimental co-infection of distinct chicken lines with Heterakis gallinarum and Ascaridia galli. Parasites & Vectors, 14(1), 1-15.
  • Delgado‐Viscogliosi, P., Viscogliosi, E., Gerbod, D., Kulda, J., Sogin, M. L., & Edgcomb, V. P. (2000). Molecular phytogeny of parabasalids based on small subunit rRNA sequences, with emphasis on the Trichomonadinae subfamily. Journal of Eukaryotic Microbiology, 47(1), 70-75. https://doi.org/10.1111/j.1550-7408.2000.tb00013.x
  • Dimasuay, K., G., B., & Rivera, W., L., (2013). Molecular characterization of trichomonads isolated from animal hosts in the Philippines. Veterinary Parasitology, 196(3-4), 289-295.
  • Esquenet, C., De Herdt, P., De Bosschere, H., Ronsmans, S., Ducatelle, R., & Van Erum, J., (2003). An outbreak of histomoniasis in freerange layer hens. Avian Pathology, 32, 305–308. https://doi.org/10.1080/0307945031000097903
  • Galarneau, K. D., Singer, R. S., & Wills, R. W., (2020). A system dynamics model for disease management in poultry production. Poultry science, 99(11), 5547-5559. https://doi.org/10.1016/j.psj.2020.08.011
  • Grabensteiner, E., & Hess, M., (2006). PCR for the identification and differentiation of Histomonas meleagridis, Tetratrichomonas gallinarum and Blastocystis spp. Veterinary Parasitology, 142(3-4). https://doi.org/10.1016/j.vetpar.2006.07.011
  • Grabensteiner, E., Bilic, I., Kolbe, T., & 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(1-2), 53-64. https://doi.org/10.1016/j.vetpar.2010.04.015
  • Grafl, B., Liebhart, D., Windisch, M., Ibesich, C., & Hess, M., (2011). Seroprevalence of Histomonas meleagridis in pullets and laying hens determined by ELISA. Veterinary record, 168(6), 160-160. https://doi.org/10.1136/vr.c6479
  • Gu, X. B., Wang, B. J., Zhao, X. B., Li, Y. F., Yang, G. Y., Lai, W. M., ... & Peng, G. N., (2018). Genetic variation in mitochondrial cox2 of Heterakis gallinarum from poultry in Sichuan, China. Mitochondrial DNA Part A, 29(4), 629-634. https://doi.org/10.1080/24701394.2017.1334771
  • Hu, J., Fuller, L., Armstrong, P. L., & McDougald, L. R., (2006). Histomonas meleagridis in chickens: attempted transmission in the absence of vectors. Avian Diseases, 50(2), 277-279. https://doi.org/10.1637/7431-090605R.1
  • Hu, J., & L. R., (2003) McDougald. Direct lateral transmission of Histomonas meleagridis in turkeys. Avian Dis. 47:489–492. https://doi.org/10.1637/0005-2086(2003)047[0489:DLTOHM]2.0.CO;2 Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K., (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular biology and evolution, 35(6), 1547.
  • Landman, W. J. M., Molenaar, R. J., Cian, A., Van der Heijden, H. M. J. F., & Viscogliosi, E. (2016). Granuloma disease in flocks of productive layers caused by Tetratrichomonas gallinarum. Avian Pathology, 45(4), 465-477. https://doi.org/10.1080/03079457.2016.1163325
  • McDougald, L.R,. (2020). Internal Parasites. In Diseases of Poultry (eds D.E. Swayne, M. Boulianne, C.M. Logue, L.R. McDougald, V. Nair, D.L. Suarez, S. Wit, T. Grimes, D. Johnson, M. Kromm, T.Y. Prajitno, I. Rubinoff and G. Zavala). Marangon, S., & Busani, L., (2007). The use of vaccination in poultry production. Revue Scientifique et Technique-Office International des Epizooties, 26(1), 265.
  • Nguyen, D. T., Bilic, I., Jaskulska, B., Hess, M., Le, D. Q., Le Hua, L. N., ... & Vu-Khac, H. (2015). Prevalence and genetic characterization of Histomonas meleagridis in chickens in Vietnam. Avian diseases, 59(2), 309-314. https://doi.org/10.1637/10964-102414-Reg
  • Patra, G., Prasad, H., Lalsiamthara, J., Kataria, J., Malsawmkima, D., & Lalrinkima, H., (2013). Prevalence of Histomonas meleagridis in broiler chicken in different parts of Mizoram, India. International Journal of Poultry Science, 12, 98-101.
  • Patton, C. S., & Patton, S., (1996). Tetratrichomonas gallinarum encephalitis in a mockingbird (Mimus polyglottos). Journal of Veterinary Diagnostic Investigation, 8(1), 133-137.
  • Posada, D., (2008). jModelTest: phylogenetic model averaging. Molecular biology and evolution, 25(7), 1253-1256. https://doi.org/10.1093/molbev/msn083
  • van der Heijden, H. M., & Landman, W. J., (2011). High seroprevalence of Histomonas meleagridis in Dutch layer chickens. Avian Diseases, 55(2), 324-327. https://doi.org/10.1637/9609-120610-ResNote.1
  • Wichmann, R. W., & Bankowski, R. A., (1956). A report of Trichomonas gallinarum infection in chukar partridges (Alectoris graeca). The Cornell Veterinarian, 46(3), 367-369.
Year 2023, Volume: 20 Issue: 1, 13 - 18, 23.06.2023
https://doi.org/10.34233/jpr.1302448

Abstract

Project Number

project code KMY.A4.21.004.

References

  • Amin, A., Liebhart, D., Weissenböck, H., & 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(1), 55-62. https://doi.org/10.1016/j.jcpa.2010.06.002
  • Burns, R. E., Braun, J., Armién, A. G., & Rideout, B. A., (2013). Hepatitis and splenitis due to systemic tetratrichomoniasis in an American white pelican (Pelecanus erythrorhynchos). Journal of Veterinary Diagnostic Investigation, 25(4), 511-514. DOI: 10.1177/1040638713488368
  • Cupo, K. L., & Beckstead, R. B., (2019). Heterakis gallinarum, the cecal nematode of gallinaceous birds: a critical review. Avian Diseases, 63(3), 381-388. https://doi.org/10.1637/0005-2086-63.3.381 Cepicka, I., Kutišová, K., Tachezy, J., Kulda, J., & Flegr, J., (2005). Cryptic species within the Tetratrichomonas gallinarum species complex revealed by molecular polymorphism. Veterinary Parasitology, 128(1-2), 11-21. https://doi.org/10.1016/j.vetpar.2004.11.003
  • Cepicka, I., Hampl, V., & Kulda, J. (2010). Critical taxonomic revision of parabasalids with description of one new genus and three new species. Protist, 161(3), 400-433. https://doi.org/10.1016/j.protis.2009.11.005
  • Daş, G., Wachter, L., Stehr, M., Bilic, I., Grafl, B., Wernsdorf, P., & Liebhart, D. (2021). Excretion of Histomonas meleagridis following experimental co-infection of distinct chicken lines with Heterakis gallinarum and Ascaridia galli. Parasites & Vectors, 14(1), 1-15.
  • Delgado‐Viscogliosi, P., Viscogliosi, E., Gerbod, D., Kulda, J., Sogin, M. L., & Edgcomb, V. P. (2000). Molecular phytogeny of parabasalids based on small subunit rRNA sequences, with emphasis on the Trichomonadinae subfamily. Journal of Eukaryotic Microbiology, 47(1), 70-75. https://doi.org/10.1111/j.1550-7408.2000.tb00013.x
  • Dimasuay, K., G., B., & Rivera, W., L., (2013). Molecular characterization of trichomonads isolated from animal hosts in the Philippines. Veterinary Parasitology, 196(3-4), 289-295.
  • Esquenet, C., De Herdt, P., De Bosschere, H., Ronsmans, S., Ducatelle, R., & Van Erum, J., (2003). An outbreak of histomoniasis in freerange layer hens. Avian Pathology, 32, 305–308. https://doi.org/10.1080/0307945031000097903
  • Galarneau, K. D., Singer, R. S., & Wills, R. W., (2020). A system dynamics model for disease management in poultry production. Poultry science, 99(11), 5547-5559. https://doi.org/10.1016/j.psj.2020.08.011
  • Grabensteiner, E., & Hess, M., (2006). PCR for the identification and differentiation of Histomonas meleagridis, Tetratrichomonas gallinarum and Blastocystis spp. Veterinary Parasitology, 142(3-4). https://doi.org/10.1016/j.vetpar.2006.07.011
  • Grabensteiner, E., Bilic, I., Kolbe, T., & 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(1-2), 53-64. https://doi.org/10.1016/j.vetpar.2010.04.015
  • Grafl, B., Liebhart, D., Windisch, M., Ibesich, C., & Hess, M., (2011). Seroprevalence of Histomonas meleagridis in pullets and laying hens determined by ELISA. Veterinary record, 168(6), 160-160. https://doi.org/10.1136/vr.c6479
  • Gu, X. B., Wang, B. J., Zhao, X. B., Li, Y. F., Yang, G. Y., Lai, W. M., ... & Peng, G. N., (2018). Genetic variation in mitochondrial cox2 of Heterakis gallinarum from poultry in Sichuan, China. Mitochondrial DNA Part A, 29(4), 629-634. https://doi.org/10.1080/24701394.2017.1334771
  • Hu, J., Fuller, L., Armstrong, P. L., & McDougald, L. R., (2006). Histomonas meleagridis in chickens: attempted transmission in the absence of vectors. Avian Diseases, 50(2), 277-279. https://doi.org/10.1637/7431-090605R.1
  • Hu, J., & L. R., (2003) McDougald. Direct lateral transmission of Histomonas meleagridis in turkeys. Avian Dis. 47:489–492. https://doi.org/10.1637/0005-2086(2003)047[0489:DLTOHM]2.0.CO;2 Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K., (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular biology and evolution, 35(6), 1547.
  • Landman, W. J. M., Molenaar, R. J., Cian, A., Van der Heijden, H. M. J. F., & Viscogliosi, E. (2016). Granuloma disease in flocks of productive layers caused by Tetratrichomonas gallinarum. Avian Pathology, 45(4), 465-477. https://doi.org/10.1080/03079457.2016.1163325
  • McDougald, L.R,. (2020). Internal Parasites. In Diseases of Poultry (eds D.E. Swayne, M. Boulianne, C.M. Logue, L.R. McDougald, V. Nair, D.L. Suarez, S. Wit, T. Grimes, D. Johnson, M. Kromm, T.Y. Prajitno, I. Rubinoff and G. Zavala). Marangon, S., & Busani, L., (2007). The use of vaccination in poultry production. Revue Scientifique et Technique-Office International des Epizooties, 26(1), 265.
  • Nguyen, D. T., Bilic, I., Jaskulska, B., Hess, M., Le, D. Q., Le Hua, L. N., ... & Vu-Khac, H. (2015). Prevalence and genetic characterization of Histomonas meleagridis in chickens in Vietnam. Avian diseases, 59(2), 309-314. https://doi.org/10.1637/10964-102414-Reg
  • Patra, G., Prasad, H., Lalsiamthara, J., Kataria, J., Malsawmkima, D., & Lalrinkima, H., (2013). Prevalence of Histomonas meleagridis in broiler chicken in different parts of Mizoram, India. International Journal of Poultry Science, 12, 98-101.
  • Patton, C. S., & Patton, S., (1996). Tetratrichomonas gallinarum encephalitis in a mockingbird (Mimus polyglottos). Journal of Veterinary Diagnostic Investigation, 8(1), 133-137.
  • Posada, D., (2008). jModelTest: phylogenetic model averaging. Molecular biology and evolution, 25(7), 1253-1256. https://doi.org/10.1093/molbev/msn083
  • van der Heijden, H. M., & Landman, W. J., (2011). High seroprevalence of Histomonas meleagridis in Dutch layer chickens. Avian Diseases, 55(2), 324-327. https://doi.org/10.1637/9609-120610-ResNote.1
  • Wichmann, R. W., & Bankowski, R. A., (1956). A report of Trichomonas gallinarum infection in chukar partridges (Alectoris graeca). The Cornell Veterinarian, 46(3), 367-369.
There are 23 citations in total.

Details

Primary Language English
Subjects Zootechny (Other)
Journal Section Research Article
Authors

Nuri Ercan This is me 0000-0001-6039-3510

Alparslan Yıldırım This is me 0000-0001-9868-0363

Onder Duzlu This is me 0000-0002-6951-0901

Project Number project code KMY.A4.21.004.
Publication Date June 23, 2023
Published in Issue Year 2023 Volume: 20 Issue: 1

Cite

APA Ercan, N., Yıldırım, A., & Duzlu, O. (2023). Molecular Prevalence of Three Chicken Gastrointestinal Tract Pathogens and Phylogenetic Characterization of Tetratrichomonas gallinarum in Türkiye. Journal of Poultry Research, 20(1), 13-18. https://doi.org/10.34233/jpr.1302448
AMA Ercan N, Yıldırım A, Duzlu O. Molecular Prevalence of Three Chicken Gastrointestinal Tract Pathogens and Phylogenetic Characterization of Tetratrichomonas gallinarum in Türkiye. JPR. June 2023;20(1):13-18. doi:10.34233/jpr.1302448
Chicago Ercan, Nuri, Alparslan Yıldırım, and Onder Duzlu. “Molecular Prevalence of Three Chicken Gastrointestinal Tract Pathogens and Phylogenetic Characterization of Tetratrichomonas Gallinarum in Türkiye”. Journal of Poultry Research 20, no. 1 (June 2023): 13-18. https://doi.org/10.34233/jpr.1302448.
EndNote Ercan N, Yıldırım A, Duzlu O (June 1, 2023) Molecular Prevalence of Three Chicken Gastrointestinal Tract Pathogens and Phylogenetic Characterization of Tetratrichomonas gallinarum in Türkiye. Journal of Poultry Research 20 1 13–18.
IEEE N. Ercan, A. Yıldırım, and O. Duzlu, “Molecular Prevalence of Three Chicken Gastrointestinal Tract Pathogens and Phylogenetic Characterization of Tetratrichomonas gallinarum in Türkiye”, JPR, vol. 20, no. 1, pp. 13–18, 2023, doi: 10.34233/jpr.1302448.
ISNAD Ercan, Nuri et al. “Molecular Prevalence of Three Chicken Gastrointestinal Tract Pathogens and Phylogenetic Characterization of Tetratrichomonas Gallinarum in Türkiye”. Journal of Poultry Research 20/1 (June 2023), 13-18. https://doi.org/10.34233/jpr.1302448.
JAMA Ercan N, Yıldırım A, Duzlu O. Molecular Prevalence of Three Chicken Gastrointestinal Tract Pathogens and Phylogenetic Characterization of Tetratrichomonas gallinarum in Türkiye. JPR. 2023;20:13–18.
MLA Ercan, Nuri et al. “Molecular Prevalence of Three Chicken Gastrointestinal Tract Pathogens and Phylogenetic Characterization of Tetratrichomonas Gallinarum in Türkiye”. Journal of Poultry Research, vol. 20, no. 1, 2023, pp. 13-18, doi:10.34233/jpr.1302448.
Vancouver Ercan N, Yıldırım A, Duzlu O. Molecular Prevalence of Three Chicken Gastrointestinal Tract Pathogens and Phylogenetic Characterization of Tetratrichomonas gallinarum in Türkiye. JPR. 2023;20(1):13-8.

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