Chlamydiosis in farmed chickens in Slovakia and zoonotic risk for humans
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Department of Epidemiology, Faculty of Medicine, Pavol Jozef Šafárik University, Košice, Slovakia
Department of Biology and Genetics, University of Veterinary Medicine and Pharmacy, Košice, Slovakia
Department of Hygiene and Food Industry Technology, University of Veterinary Medicine and Pharmacy, Košice, Slovakia
Department of Pharmacology and Toxicology, University of Veterinary Medicine and Pharmacy, Košice, Slovakia
Chlamydia psittaci is an obligate intracellular Gram-negative bacterium causing respiratory disease (chlamydiosis) or asymptomatic carriage in poultry. In humans, it is a zoonotic agent of ornithosis/psittacosis. Due to low awareness of the disease and variable clinical presentation, psittacosis is often remains unrecognised as such by general practitioners. Zoonotic transfer occurs through inhalation of contaminated aerosols, and originates from feathers, faecal material and respiratory tract exudates.

The aim of this study was to investigate chickens for the presence of Chlamydia sp. from pharyngeal and cloacal swabs and review the zoonotic risk for humans.

Material and methods:
138 clinically healthy chickens from farms in Slovakia were examined for the presence of Chlamydia sp. The age of the chickens was 6 months. Two different samples were used – pharyngeal swabs and cloacal swabs. Each sample was examined by the molecular PCR method, and in the case of a positive result the identity of the obtained sequences was examined by a BLAST search.

Of the total number of 276 examined samples from 138 chickens, 19 (6.9%) showed positivity for C. psittaci infection, 12 (8.7%) which were positive from pharyngeal swabs and 7 (5.1%) from cloacal swabs. None of the chickens were positive in both samples. Phylogenetic examination of the 19 isolates identified in the study, based on the 23S rRNA gene sequence, revealed that the isolates obtained were identical with C. psittaci, and genetically very close to genotypes B and genotype E.

C. psittaci infections are apparently emerging in chickens. Chicken-processing plant employees should be considered a risk group for human psittacosis. There is a need for higher awareness and for efficient risk assessment and management.

Monika Halánová   
Pavol Jozef Šafárik University in Košice, Faculty of Medicine, Department of Epidemiology, Šrobárova 2, 04180 Košice, Slovak Republic
1. Vorimore F, Hsia RC, Huot-Creasy H, Bastian S, Deruyter L, Passet A, et al. Isolation of a new Chlamydia species from the Feral Sacred Ibis (Threskiornis Aethiopicus): Chlamydia ibidis. PLoS One. 2013; 8(9): e74823.
2. Sachse K, Bavoil PM, Kaltenboeck B, Stephens RS, Kuo Ch, Rosselló-Móra R, et al. Emendation of the family Chlamydiaceae: Proposal of a single genus, Chlamydia, to include all currently recognized species. Sys App Micro. 2015; 38: 99–103.
3. Kaleta EF, Taday EM. Avian host range of Chlamydophila spp. based on isolation, antigen detection and serology. Avian Pathol. 2003; 32 (5): 435–461.
4. Geigenfeind I, Haag-Wackernagel D. Detection of Chlamydophila psittaci from feral pigeons in environmental samples: problems with currently available techniques. Integr Zool. 2010; 5: 63–69.
5. Gaede W, Reckling KF, 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.
6. Dickx V, Geens T, Deschuyffeleer T, Tyberghien L, Harkinezhad T, Beeckman DS, et al. Chlamydophila psittaci zoonotic risk assessment in a chicken and turkey slaughterhouse. J Clin Microbiol. 2010; 48: 3244–3250.
7. Petrovay F, Balla E. Two fatal cases of psittacosis caused by Chlamydophila psittaci. J Med Microbiol. 2008; 57: 1296–1298.
8. 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.
9. Circella E, Pugliese N, Todisco G, Cafiero MA, Sparagano OA, Camarda A. Chlamydia psittaci infection in canaries heavily infested by Dermanyssus gallinae. Exp Appl Acarol. 2011; 55: 329–338.
10. Beeckman DS, Vanrompay DC. Zoonotic Chlamydophila psittaci infections from a clinical perspective. Clin Microbiol Infect. 2009; 15: 11–17.
11. Williams J, Tallis G, Dalton C, Ng S, Beaton S, Catton M et al. Community outbreak of psittacosis in a rural Australian town. Lancet. 1998; 351: 1697–1699.
12. Telfer BL, Moberley SA, Hort KP, Branley JM, Dwyer DE, Muscatello DJ, et al. Probable psittacosis outbreak linked to wild birds. Emerg Infect Dis. 2005; 11: 391–397.
13. Vanrompay D, Ducatelle R, Haesebrouck F. Chlamydia psittaci infections: a review with emphasis on avian chlamydiosis. Vet Microbiol. 1995; 45: 93–119.
14. Knittler MR, Berndt A, Bӧcker S, Dutov P, Hänel F, Heuer D, et al. Chlamydia psittaci: new insights into genomic diversity, clinical pathology, host-pathogen interaction and antibacterial immunity. Int J Med Microbiol. 2014; 304: 877–893.
15. Kovácová E, Majtán J, Botek R, Bokor T, Blaskovicová H, Solavová M, et al. A fatal case of psittacosis in Slovakia, January 2006. Euro Surveill. 2007; 12: E070802.1.
16. Andersen AA, Vanrompay D. 2003. Avian chlamydiosis (psittacosis, ornithosis). Saif YM, ed. Diseases of Poultry, 11th edition, Iowa State University Press, Iowa, USA; 2003. p. 863–879.
17. Andersen AA. Two new serovars of Chlamydia psittaci from North American birds. J Vet Diagn Invest. 1997; 9: 159–164.
18. Zhang F, Li S, Yang J, Pang W, Yang L, He C. Isolation and characterization of Chlamydophila psittaci isolated from laying hens with cystic oviducts. Avian Dis. 2008; 52: 74–78.
19. Zhou J, Qiu C, Lin G, Cao X, Zheng F. Isolation of Chlamydophila psittaci from laying hens in China. Vet Res. 2010; 3: 43–45.
20. Yin L, Kalmar ID, Lagae S, Vandendriessche S, Vanderhaeghen W, Butaye P, et al. Emerging Chlamydia psittaci infections in the chicken industry and pathology of Chlamydia psittaci genotype B and D strains in specific pathogen free chickens. Vet Microbiol. 2013; 162: 740–749.
21. Everett KDE, Bush RM, Andersen AA. Emended description of the order Chlamydiales, proposal of Parachlamydiaceae fam. nov. and Simkaniaceae fam. nov., each containing one monotypic genus, revised taxonomy of the family Chlamydiaceae, including a new genus and five new species, and standards for the identification of organisms. Inter J Syst Bacter. 1999; 49: 415–440.
22. Basic Local Alignment Search Tool. NCBI National Center for Biotechnology Information. =BlastSearch&LINK_LOC=blasthome (accsess 2017.04.15).
23. Sachse K, Laroucau K, Riege K, Wehner S, Dilcher M, Creasy HH, et al. Evidence for the existence of two new members of the family Chlamydiaceae and proposal of Chlamydia avium sp. nov. and Chlamydia gallinacea sp. nov. Syst Appl Microbiol. 2014; 37: 79–88.
24. Sachse K, Laroucau K. Avian chlamydiosis: two more bacterial players discovered. Vet J. 2014; 200: 347–348.
25. 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.
26. Sachse K, Kuehlewind S, Ruettger A, Schubert E, Rohde G. More than classical Chlamydia psittaci in urban pigeons. Vet Microbiol. 2012; 157: 476–480.
27. Guo W, Li J, Kaltenboeck B, Gong J, Fan W, Wang C. Chlamydia gallinacea, not C. psittaci, is the endemic chlamydial species in chicken (Gallus gallus). Sci Rep. 2016; 6: 19638. doi: 10.1038/srep19638.
28. 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.
29. 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. gallinacea in poultry. Pathog Dis. 2015; 73: 1–11. 10.1093/femspd/ftv005 PMID: 2566334.
30. Yang J, Yang Q, Yang J, He C. Prevalence of avian Chlamydophila psittaci in China. Bulletin of the Veterinary Institute in Pulawy. 2007; 51: 347–350.
31. Robertson T, Bibby S, O’Rourke D, Belfiore T, Agnew-Crumpton R, Noormohammadi AH. Identification of Chlamydial species in crocodiles and chickens by PCR-HRM curve analysis. Vet Microbiol. 2010; 145: 373–379.
32. Dickx V, Vanrompay D. Zoonotic transmission of Chlamydia psittaci in a chicken and turkey hatchery. J Med Microbiol. 2011; 60: 775–779.
33. Verminnen K, Van Loock M, Hafez HM, Ducatelle R, Haesebrouck F, Vanrompay D. Evaluation of a recombinant enzyme-linked immunosorbent assay for detecting Chlamydophila psittaci antibodies in turkey sera. Vet Res. 2006; 37: 623–632.
34. Lagae S, Kalmar I, Laroucau K, Vorimore F, Vanrompay D. Emerging Chlamydia psittaci infections in chickens and examination of transmission to humans. J Med Microbiol. 2014; 63: 399–407.
35. 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.
36. Kalmar ID, Dicxk V, Dossche L, Vanrompay D. Zoonotic infection with Chlamydia psittaci at an avian refuge centre. Vet J. 2013; 199: 300–302.
37. Geens T, Desplanques A, Van Loock M, Bonner BM, Kaleta EF, Magnino S, et al. Sequencing of the Chlamydophila psittaci ompA gene reveals a new genotype, E/B, and the need for a rapid discriminatory genotyping method. J Clin Microbiol. 2005; 43: 2456–2461.
38. Čisláková L, Halánová M, Čechová L. Epidemiologická situácia vo výskyte ornitózy-psitakózy u ľudí na Slovensku. In: Aktuálne problémy verejného zdravotníctva vo výskume a praxi III. Martin: Jesseniova lekárska fakulta v Martine, Univerzita Komenského v Bratislave. ISBN 9788089797219; 2017. p. 41–46. (in Slovak).
39. Harkinezhad T, Verminnen K, van Droogenbroeck C, Vanrompay D. Chlamydophila psittaci genotype E/B transmission from African grey parrots to humans. J Med Microbiol. 2007; 56: 1097–1100.
40. Pelle-Duporte D, Gendre I. Ornithosis epidemics in a poultry slaughterhouse. INRS, Documents for the occupational physician. 2001; 85: 49–57.
41. Vanrompay D, Harkinezhad T, van de Walle M, Beeckman D, van Droogenbroeck C, Verminnen K, et al. 2007. Chlamydophila psittaci transmission from pet birds to humans. Emerg Infect Dis. 2007; 13: 1108–1110.
42. HSE. Infection at work: controlling the risks. A guide for employers and the self employed on identifying, assessing and controlling the risks of infection in the workplace. Advisory Committee on Dangerous Pathogens. 2010.
43. Deschuyffeleer TP, Tyberghien LF, Dickx VL, Geens T, Saelen JM, Vanrompay DC, et al. Risk assessment and management of Chlamydia psittaci in poultry processing plants. Ann Occup Hyg. 2012; 56: 340–349.