Survey on Chlamydiaceae in cloacal swabs from Swiss turkeys demonstrates absence of Chlamydia psittaci and low occurrence of Chlamydia gallinacean

Autoři: Barbara Renate Vogler aff001;  Michal Trinkler aff001;  Hanna Marti aff002;  Nicole Borel aff002;  Theresa Pesch aff002;  Barbara Prähauser aff002;  Richard Hoop aff001;  Prisca Mattmann aff001;  Sarah Albini aff001
Působiště autorů: National Reference Centre for Poultry and Rabbit Diseases (NRGK), Institute for Food Safety and Hygiene, Vetsuisse Faculty, University of Zurich, Zurich, Switzerland aff001;  Institute for Veterinary Pathology, Vetsuisse Faculty, University of Zurich, Zurich, Switzerland aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article


In Switzerland, domestic turkey meat is a niche product. Turkeys are fattened on mixed family-based farms scattered across the country, with most providing access to an uncovered outdoor pasture for the birds. Swiss fattening turkeys may therefore get infected with Chlamydiaceae via wild birds or their faeces, potentially shedding these bacteria at a later stage. The aim of the present study was to acquire baseline data about the shedding of Chlamydiaceae in clinically unremarkable Swiss fattening turkeys at slaughter, potentially exposing slaughterhouse workers to infection. In this large-scale study, 1008 cloacal swabs of Swiss turkeys out of 53 flocks from 28 different grow-out farms with uncovered outdoor pasture were collected over the course of 14 months and examined for the occurrence of Chlamydiaceae by a family-specific 23S-rRNA real-time PCR. Positive samples were further analyzed by Chlamydia psittaci (C. psittaci)-specific real-time PCR and the Arraymate DNA Microarray for species identification. All samples were negative for C. psittaci, but seven swabs out of one flock were tested positive for Chlamydia gallinacea (0.7%). Although turkeys with access to pasture may have contact with Chlamydiaceae-harbouring wild birds or their faeces, the infection rate in Swiss turkeys was shown to be low.

Klíčová slova:

Birds – Chlamydia – Chlamydia infection – Livestock – Polymerase chain reaction – Ribosomal RNA – Turkeys – Chlamydophila psittaci


1. Borel N, Polkinghorne A, Pospischil A. A review on chlamydial diseases in animals: Still a challenge for pathologists? Vet Path. 2018; 55: 374–390.

2. Dickx V, Geens T, Deschuyffeleer T, Tyberghien L, Harkinezhad T, Beeckmann DSA, et al. Chlamydophila psittaci zoonotic risk assessment in a chicken and turkey slaughterhouse. J Clin Microbiol. 2010; 48: 3244–3250. doi: 10.1128/JCM.00698-10 20592139

3. Heddema ER, Van Hannen EJ, Bongaerts M, Dijkstra F, Ten Hove RJ, De Wever B, et al. Typing of Chlamydia psittaci to monitor epidemiology of psittacosis and aid disease control in the Netherlands, 2008 to 2013. Euro Surveill. 2015; 20: 21026. 25677053

4. Van Droogenbroeck C, Beeckman DSA, Verminnen K, Marien M, Nauwynck H, de Thibault de Boesinghe L, et al. Simultaneous zoonotic transmission of Chlamydophila psittaci genotypes D, F and E/B to a veterinary scientist. Vet Microbiol. 2009; 135: 78–81. doi: 10.1016/j.vetmic.2008.09.047 18963600

5. Corsaro D, Venditti D. Emerging chlamydial infections. Crit Rev Microbiol. 2004; 30: 75–106. doi: 10.1080/10408410490435106 15239381

6. Vanrompay D, Harkinezhad T, Van de Walle M, Beeckman D, Van Droogenbroek C, Verminnen K, et al. Chlamydophila psittaci transmission from pet birds to humans. Emerg Infect Dis. 2007; 13: 1108–1110. doi: 10.3201/eid1307.070074 18214194

7. Andrews BE, Major R, Palmer SR. Ornithosis in poultry workers. Lancet, 1981, Mar 21;1(8221):632–4. doi: 10.1016/s0140-6736(81)91552-x 6110862

8. Gaede W, Reckling K-F, Dresenkamp B, Kenklies S, Schubert E, Noack U, et al. Chlamydophila psittaci infections in humans during an outbreak of psittacosis from poultry in Germany. Zoonoses Public Health. 2008; 55: 184–188. doi: 10.1111/j.1863-2378.2008.01108.x 18387139

9. Andral B, Louzis C, Trap D, Newman JA, Bennejean G, Gaumont R. Respiratory disease (rhinotracheitis) in turkeys in Brittany, France, 1981–1982. I. Field observations and serology. Avian Dis. 1985; 29: 26–34. 3985881

10. Vanrompay D, Butaye P, Van Nerom A, Ducatelle R, Haesebrouck F. The prevalence of Chlamydia psittaci infections in Belgian commercial turkey poults. Vet Mircobiol. 1997; 54: 85–93.

11. Van Loock M, Geens T, De Smit L, Nauwynck H, Van Empel P, Naylor C, et al. Key role of Chlamydophila psittaci on Belgian turkey farms in association with other respiratory pathogens. Vet Microbiol. 2005; 107: 91–101. doi: 10.1016/j.vetmic.2005.01.009 15795081

12. Vanrompay D, Ducatelle R, Haesebrouck F, Hendrickx W. Primary pathogenicity of an European isolate of Chlamydia psittaci from turkey poults. Vet Microbiol. 1993; 38: 103–113. doi: 10.1016/0378-1135(93)90078-l 8128594

13. Hafez HM, Sting R. Chlamydien-Infektion bei Puten: Literaturübersicht und Auswertungen eigener Untersuchungen. Arch Geflügelk. 1993; 57: 16–21.

14. Ryll M, Hinz K-H, Neumann U, Behr K-P. Pilotstudie über das Vorkommen von Chlamydia psittaci-Infektionen in kommerziellen Putenherden Niedersachsens. Dtsch. Tierärztl. Wschr. 1994; 101: 163–165.

15. Sting R, Lerke E, Hotzel H, Jodas S, Popp C, Hafez HM. Vergleichende Untersuchungen zum Nachweis von Chlamydophila psittaci und Chlamydophila abortus in Putenmastbetrieben mittels Zellkultur, ELISA und PCR. Dtsch. Tierärztl. Wschr. 2006; 113: 50–54.

16. Sachse K, Laroucau K, Riege K, Wehner S, Dilcher M, Huot Creasy H, et al. Evidence for the existence of two new members of the family Chlamydiaceae and proposal of Chlamydia avium sp. nov. and Chlamydia gallinacae sp. nov. Syst. Appl. Microbiol. 2014; 37: 79–88. doi: 10.1016/j.syapm.2013.12.004 24461712

17. Laroucau K, Vorimore F, Aaziz R, Berndt A, Schubert E, Sachse K. Isolation of a new chlamydial agent from infected domestic poultry coincided with cases of atypical pneumonia among slaughterhouse workers in France. Infect. Genet. Evol. 2009; 9: 1240–1247. doi: 10.1016/j.meegid.2009.08.005 19715775

18. Zocevic A, Vorimore F, Marhold C., Horvatek D, Wang D, Slavec B, et al. Molecular characterization of atypical Chlamydia and evidence of their dissemination in different European and Asian chicken flocks by specific real-time PCR. Environ. Microbiol. 2012; 14: 2212–2222. doi: 10.1111/j.1462-2920.2012.02800.x 22690809

19. Heijne M, Van der Goot JA, Fijten H, Van der Giessen JW, Kuijt E, Maassen CBM, et al. A cross sectional study on Dutch layer farms to investigate the prevalence and potential risk factors for different Chlamydia species. PLoS ONE. 2018; 13: e0190774. doi: 10.1371/journal.pone.0190774 29324884

20. Hulin V, Oger S, Vorimore F, Aaziz R, de Barbeyrac B, Berruchon J, et al. Host preference and zoonotic potential of Chlamydia psittaci and C. gallinacae in poultry. Pathog Dis. 2015; 73: 1–11.

21. Guo W, Li J, Kaltenboeck B, Gong J, Fan W, Wang C. Chlamydia gallinacae, not C. psittaci, is the endemic chlamydial species in chicken (Gallus gallus). Sci. Rep. 2016; 6:19638. doi: 10.1038/srep19638 26778053

22. Szymanska-Czerwinska M, Mitura A, Zareba K, Schnee C, Koncicki A, Niemczuk K. Poultry in Poland as Chlamydiaceae carrier. J Vet Res. 2017; 61:411–419. doi: 10.1515/jvetres-2017-0072 29978103

23. Agristat. Kapitel 3: Viehwirtschaft. In: Statistische Erhebungen und Schätzungen über Landwirtschaft und Ernährung SES 2016–92. Schweizer Bauernverband, Agristat, Brugg.

24. Anonymous, 2013. Verordnung über die Direktzahlung an die Landwirtschaft (Direktzahlungsverordnung, DZV) vom 23. Oktober 2013 (stand am 1. Januar 2019), 910.13.

25. Anonymous, 1998. Bundesgesetz über die Landwirtschaft (Landwirtschaftsgesetz, LwG), vom 29. April 1998 (Stand am 1. Januar 2019), 910.1.

26. Anonymous. Tierschutzverordnung 23. April 2008 (TSchV), Anhang 1, Tabelle 9–2. 2008.

27. Hoffmann K, Schott F, Donati M, Di Francesco A, Hässig M, Wanninger S, et al. Prevalence of Chlamydial infections in fattening pigs and their influencing factors. PLoS ONE 2015; 10(11): e0143576. doi: 10.1371/journal.pone.0143576 26619187

28. World Organisation for Animal Health (OIE). Manual of diagnostic tests and vaccines for terrestrial animals (mammals, birds and bees), 8th edition, OIE, Paris, 2018.

29. Ehricht R, Slickers P, Goellner S, Hotzel H, Sachse K. Optimized DNA microarray assay allows detection and genotyping of single PCR-amplifiable target copies. Mol. Cell. Probes. 2006; 20: 60–63. doi: 10.1016/j.mcp.2005.09.003 16330186

30. Blumer S, Greub G, Waldvogel A, Hässig M, Thoma R, Tschuor A, et al. Waddlia, Parachlamydia and Chlamydiaceae in bovine abortion. Vet Microbiol. 2011; 152: 385–393. 21658867

31. Hoffmann B., Depner K, Schirrmeier H, Beer M. A universal heterologous internal control system for duplex real-time RT-PCR assays used in a detection system for pestiviruses. J Virol. Methods 2006; 136: 200–209. doi: 10.1016/j.jviromet.2006.05.020 16806503

32. Pantchev A, Sting R, Bauerfeind R, Tyczka J, Sachse K. New real-time PCR tests for species-specific detection of Chlamydophila psittaci and Chlamydophila abortus from tissue samples. Vet. J. 2009; 181: 145–150. doi: 10.1016/j.tvjl.2008.02.025 18413292

33. Hoffmann B, Beer M, Schelp C, Schirrmeier H, Depner K. Validation of a real-time RT-PCR assay for sensitive and specific detection of classical swine fever. J. Virol. Methods. 2005; 130: 36–44. doi: 10.1016/j.jviromet.2005.05.030 16055202

34. Mattmann P. Chlamydiaceae in wild, feral and domestic pigeons in Switzerland and insight into population dynamics by Chlamydia psittaci multilocus sequence typing. Inaugural Dissertation, Vetsuisse Faculty, University of Zurich, 2019.

35. Borel N, Kempf E, Hotzel H, Schubert E, Torgerson P, Slickers P, et al. Direct identification of chlamydiae from clinical samples using a DNA microarray assay—A validation study. Mol. Cell. Probes. 2008; 22: 55–64. doi: 10.1016/j.mcp.2007.06.003 17714911

36. Pospischil A, Kaiser C, Hofmann-Lehmann R, Lutz H, Hilbe M, Vaughan L, et al. Evidence for Chlamydia in wild mammals of the Serengeti. J Wildl Dis. 2012;48:1074–8. doi: 10.7589/2011-10-298 23060512

37. Takahashi T, Takashima I, Hashimoto N. Shedding and transmission of Chlamydia psittaci in experimentally infected chickens. Av. Dis. 32: 650–658, 1988.

38. Zweifel D, Hoop R, Sachse K, Pospischil A, Borel N. Prevalence of Chlamydophila psittaci in wild birds—potential risk for domestic poultry, pet birds, and public health? Eur. J. Wildl. Res. 2009; 55: 575–581.

39. Travnicek M, Cislakova L, Deptula W, Stosik M, Bhide MR. Wild pigeons and pheasants—a source of Chlamydophila psittaci for humans and animals. Ann. Agric. Environ. Med. 2002; 9: 253–255. 12498596

40. Szymanska-Czerwinska M, Mitura A, Niemczuk K, Zareba K, Jodelko A, Pluta A, et al. Dissemination and genetic diversity of chlamydial agents in Polish waterfowl: isolation and molecular characterisation of avian Chlamydia abortus strains. PLoS ONE, 2017; 12(3): e0174599. doi: 10.1371/journal.pone.0174599 28350846

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