Detection and identification of Chlamydia spp. from pigeons in Iran by nested PCR and sequencing
,
Abstract
Background and Objectives: Chlamydia psittaci, an obligate intracellular, Gram-negative zoonotic pathogen, has eight serovars and nine genotypes isolated from avian species with higher frequency in parrots and pigeons. The aim of this study was to characterize Chlamydia spp. using nested PCR and sequencing.
Materials and Methods: A total of 270 pharyngeal swab samples collected randomly from asymptomatic pigeons of 30 pigeon aviaries in Tehran province. DNA was extracted with specific kit and amplified by specific primers in the first PCR and outer membrane protein A (ompA) gene in the second PCR. Positive samples were sequenced and phylogenetic tree analyzed based on the ompA gene.
Results: Records showed that 16 of 30 (53%) pigeon aviaries were positive for Chlamydia spp. Phylogenetic tree analysis revealed that 15 of 16 (93.7%) positive samples, belonged to C. psittaci genotype B whereas the other sample belonged to C. avium. C. psittaci detected in 50% of pigeon aviaries that is high rate in Tehran province.
Conclusion: As C. psittaci is a zoonosis and life threaten pathogen for human being, these results indicate the significance of it detection in asymptomatic pigeons. Also, this is the first report of Chlamydia avium presence in Iranian pigeons which its zoonotic potential is still unknown.
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2. Vanrompay D (2020). Avian Chlamydiosis. In: Diseases of poultry. Ed, DE Swayne. Wiley-blackwell publishing, 14th ed. New Jersey, USA, pp. 1086-1107.
3. 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 gallinacea sp. nov. Syst Appl Microbiol 2014; 37: 79-88.
4. Burt SA, Röring RE, Heijne M. Chlamydia psittaci and C. avium in feral pigeon (Columba livia domestica) droppings in two cities in the Netherlands. Vet Q 2018; 38: 63-66.
5. Mattmann P, Marti H, Borel N, Jelocnik M, Albini S, Vogler BR. Chlamydiaceae in wild, feral and domestic pigeons in Switzerland and insight into population dynamics by Chlamydia psittaci multilocus sequence typing. PLoS One 2019; 14(12):e0226088.
6. Vanrompay D, Ducatelle R, Haesebrouck F. Chlamydia psittaci infections: a review with emphasis on avian chlamydiosis. Vet Microbiol 1995; 45: 93-119.
7. Sachse K, Laroucau K, Hotzel H, Schubert E, Ehricht R, Slickers P. Genotyping of Chlamydophila psittaci using a new DNA microarray assay based on sequence analysis of ompA genes. BMC Microbiol 2008; 8: 63.
8. Van Lent S, Piet JR, Beeckman D, van der Ende A, Van Nieuwerburgh F, Bavoil P, et al. Full genome sequences of all nine Chlamydia psittaci genotype reference strains. J Bacteriol 2012; 194: 6930-6931.
9. Radomski N, Einenkel R, Müller A, Knittler MR. Chlamydia–host cell interaction not only from a bird's eye view: some lessons from Chlamydia psittaci. FEBS Lett 2016; 590: 3920-3940.
10. 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.
11. Mina A, Fatemeh A, Jamshid R. Detection of Chlamydia psittaci genotypes among birds in northeast Iran. J Avian Med Surg 2019; 33: 22-28.
12. Andersen AA, Franson JC (2007). Avian chlamydiosis. In: Thomas NJ, Hunter DB, Atkinson CT, editors. Infectious Diseases of Wild Birds. Oxford: Blackwell; pp. 303-316.
13. Geigenfeind I, Vanrompay D, Haag-Wackernagel D. Prevalence of Chlamydia psittaci in the feral pigeon population of Basel, Switzerland. J Med Microbiol 2012; 61: 261-265.
14. Harkinezhad T, Geens T, Vanrompay D. Chlamydophila psittaci infections in birds: a review with emphasis on zoonotic consequences. Vet Microbiol 2009; 135: 68-77.
15. 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.
16. Magnino S, Haag-Wackernagel D, Geigenfeind I, Helmecke S, Dovc A, Prukner-Radovcić E, et al. Chlamydial infections in feral pigeons in Europe: Review of data and focus on public health implications. Vet Microbiol 2009; 135: 54-67.
17. Mahzoonieh M, Moloudizargari M, Ghasemi Shams Abadi M, Baninameh Z, Khoei H. Prevalence and phylogenetic analysis of Chlamydia psittaci in pigeon and house sparrow specimens and the potential human infection risk in Chahrmahal-va-Bakhtiari, Iran. Arch Clin Infect Dis 2020; 15(2): e67565.
18. Ghorbanpoor M, Bakhtiari NM, Mayahi M, Moridveisi H. Detection of Chlamydophila psittaci from pigeons by polymerase chain reaction in Ahvaz. Iran J Microbiol 2015; 7: 18-22.
19. Kaltenbock B, Schmeer N, Schneider R. Evidence for numerous omp1 alleles of porcine Chlamydia trachomatis and novel chlamydial species obtained by PCR. J Clin Microbiol 1997; 35: 1835-1841.
20. Sachse K, Hotzel H. Detection and differentiation of Chlamydiae by nested PCR. Methods Mol Biol 2003; 216: 123-136.
21. Heddema ER, Ter Sluis S, Buys JA, Vandenbroucke-Grauls CM, van Wijnen JH, Visser CE. Prevalence of Chlamydophila psittaci in fecal droppings from feral pigeons in Amsterdam, The Netherlands. Appl Environ Microbiol 2006; 72: 4423-4425.
22. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33: 1870-1874.
23. Everett KD, 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. Int J Syst Bacteriol 1999; 49: 415-440.
24. Mahzonieh M, Ghasemi Shamsabadi M, Heidari FJ. Prevalence of Chlamydia psittaciin pigeons in Chaharmahal va Bakhtiari and Yazd provinces of Iran, by nested-PCR, 2012. Iran J Med Microbiol 2013; 7: 1-6.
25. Khodadadi M, Hemmatinezhad B, Doosti A, Khamesipour F, Awosile B. Molecular detection and prevalence of Chlamydophila psittaci in the blood, liver and muscle tissue of urban pigeons (Columba livia domestica) in Iran. Kafkas Univ Vet Fak Derg 2015; 21: 265-269.
26. Teske L, Ryll M, Rubbenstroth D, Hänel I, Hartmann M, Kreienbrock L, et al. Epidemiological investigations on the possible risk of distribution of zoonotic bacteria through apparently healthy homing pigeons. Avian Pathol 2013; 42: 397-407.
27. Dickx V, Beeckman DSA, Dossche L, Tavernier P, Vanrompay D. Chlamydophila psittaci in homing and feral pigeons and zoonotic transmission. J Med Microbiol 2010; 59: 1348-1353.
28. Vázquez B, Esperón F, Neves E, López J, Ballesteros C, Muñoz MJ. Screening for several potential pathogens in feral pigeons (Columba livia) in Madrid. Acta Vet Scand 2010; 52: 45.
29. Madani SA, Peighambari SM. PCR-based diagnosis, molecular characterization and detection of atypical strains of avian Chlamydia psittaci in companion and wild birds. Avian Pathol 2013; 42: 38-44.
30. Geens T, Desplanques A, Van Loock M, Bönner 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.
31. Sariya L, Prompiram P, Tangsudjai S, Poltep K, Chamsai T, Mongkolphan C, et al. Detection and characterization of Chlamydophila psittaci in asymptomatic feral pigeons (Columba livia domestica) in central Thailand. Asian Pac J Trop Med 2015; 8: 94-97.
32. Floriano AM, Rigamonti S, Comandatore F, Scaltriti E, Longbottom D, Livingstone M, et al. Complete genome sequence of Chlamydia avium PV 4360/2, isolated from a feral pigeon in Italy. Microbiol Resour Announc 2020; 9(16):e01509-19.
33. Hedberg K, White KE, Forfang JC, Korlath JA, Friendshuh KA, Hedberg CW, et al. An outbreak of psittacosis in Minnesota turkey industry workers: implications for modes of transmission and control. Am J Epidemiol 1989; 130: 569-577.
34. Beeckman DS, Vanrompay DC. Zoonotic Chlamydophila psittaci infections from a clinical perspective. Clin Microbiol Infect 2009; 15: 11-17.
2. Vanrompay D (2020). Avian Chlamydiosis. In: Diseases of poultry. Ed, DE Swayne. Wiley-blackwell publishing, 14th ed. New Jersey, USA, pp. 1086-1107.
3. 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 gallinacea sp. nov. Syst Appl Microbiol 2014; 37: 79-88.
4. Burt SA, Röring RE, Heijne M. Chlamydia psittaci and C. avium in feral pigeon (Columba livia domestica) droppings in two cities in the Netherlands. Vet Q 2018; 38: 63-66.
5. Mattmann P, Marti H, Borel N, Jelocnik M, Albini S, Vogler BR. Chlamydiaceae in wild, feral and domestic pigeons in Switzerland and insight into population dynamics by Chlamydia psittaci multilocus sequence typing. PLoS One 2019; 14(12):e0226088.
6. Vanrompay D, Ducatelle R, Haesebrouck F. Chlamydia psittaci infections: a review with emphasis on avian chlamydiosis. Vet Microbiol 1995; 45: 93-119.
7. Sachse K, Laroucau K, Hotzel H, Schubert E, Ehricht R, Slickers P. Genotyping of Chlamydophila psittaci using a new DNA microarray assay based on sequence analysis of ompA genes. BMC Microbiol 2008; 8: 63.
8. Van Lent S, Piet JR, Beeckman D, van der Ende A, Van Nieuwerburgh F, Bavoil P, et al. Full genome sequences of all nine Chlamydia psittaci genotype reference strains. J Bacteriol 2012; 194: 6930-6931.
9. Radomski N, Einenkel R, Müller A, Knittler MR. Chlamydia–host cell interaction not only from a bird's eye view: some lessons from Chlamydia psittaci. FEBS Lett 2016; 590: 3920-3940.
10. 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.
11. Mina A, Fatemeh A, Jamshid R. Detection of Chlamydia psittaci genotypes among birds in northeast Iran. J Avian Med Surg 2019; 33: 22-28.
12. Andersen AA, Franson JC (2007). Avian chlamydiosis. In: Thomas NJ, Hunter DB, Atkinson CT, editors. Infectious Diseases of Wild Birds. Oxford: Blackwell; pp. 303-316.
13. Geigenfeind I, Vanrompay D, Haag-Wackernagel D. Prevalence of Chlamydia psittaci in the feral pigeon population of Basel, Switzerland. J Med Microbiol 2012; 61: 261-265.
14. Harkinezhad T, Geens T, Vanrompay D. Chlamydophila psittaci infections in birds: a review with emphasis on zoonotic consequences. Vet Microbiol 2009; 135: 68-77.
15. 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.
16. Magnino S, Haag-Wackernagel D, Geigenfeind I, Helmecke S, Dovc A, Prukner-Radovcić E, et al. Chlamydial infections in feral pigeons in Europe: Review of data and focus on public health implications. Vet Microbiol 2009; 135: 54-67.
17. Mahzoonieh M, Moloudizargari M, Ghasemi Shams Abadi M, Baninameh Z, Khoei H. Prevalence and phylogenetic analysis of Chlamydia psittaci in pigeon and house sparrow specimens and the potential human infection risk in Chahrmahal-va-Bakhtiari, Iran. Arch Clin Infect Dis 2020; 15(2): e67565.
18. Ghorbanpoor M, Bakhtiari NM, Mayahi M, Moridveisi H. Detection of Chlamydophila psittaci from pigeons by polymerase chain reaction in Ahvaz. Iran J Microbiol 2015; 7: 18-22.
19. Kaltenbock B, Schmeer N, Schneider R. Evidence for numerous omp1 alleles of porcine Chlamydia trachomatis and novel chlamydial species obtained by PCR. J Clin Microbiol 1997; 35: 1835-1841.
20. Sachse K, Hotzel H. Detection and differentiation of Chlamydiae by nested PCR. Methods Mol Biol 2003; 216: 123-136.
21. Heddema ER, Ter Sluis S, Buys JA, Vandenbroucke-Grauls CM, van Wijnen JH, Visser CE. Prevalence of Chlamydophila psittaci in fecal droppings from feral pigeons in Amsterdam, The Netherlands. Appl Environ Microbiol 2006; 72: 4423-4425.
22. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33: 1870-1874.
23. Everett KD, 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. Int J Syst Bacteriol 1999; 49: 415-440.
24. Mahzonieh M, Ghasemi Shamsabadi M, Heidari FJ. Prevalence of Chlamydia psittaciin pigeons in Chaharmahal va Bakhtiari and Yazd provinces of Iran, by nested-PCR, 2012. Iran J Med Microbiol 2013; 7: 1-6.
25. Khodadadi M, Hemmatinezhad B, Doosti A, Khamesipour F, Awosile B. Molecular detection and prevalence of Chlamydophila psittaci in the blood, liver and muscle tissue of urban pigeons (Columba livia domestica) in Iran. Kafkas Univ Vet Fak Derg 2015; 21: 265-269.
26. Teske L, Ryll M, Rubbenstroth D, Hänel I, Hartmann M, Kreienbrock L, et al. Epidemiological investigations on the possible risk of distribution of zoonotic bacteria through apparently healthy homing pigeons. Avian Pathol 2013; 42: 397-407.
27. Dickx V, Beeckman DSA, Dossche L, Tavernier P, Vanrompay D. Chlamydophila psittaci in homing and feral pigeons and zoonotic transmission. J Med Microbiol 2010; 59: 1348-1353.
28. Vázquez B, Esperón F, Neves E, López J, Ballesteros C, Muñoz MJ. Screening for several potential pathogens in feral pigeons (Columba livia) in Madrid. Acta Vet Scand 2010; 52: 45.
29. Madani SA, Peighambari SM. PCR-based diagnosis, molecular characterization and detection of atypical strains of avian Chlamydia psittaci in companion and wild birds. Avian Pathol 2013; 42: 38-44.
30. Geens T, Desplanques A, Van Loock M, Bönner 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.
31. Sariya L, Prompiram P, Tangsudjai S, Poltep K, Chamsai T, Mongkolphan C, et al. Detection and characterization of Chlamydophila psittaci in asymptomatic feral pigeons (Columba livia domestica) in central Thailand. Asian Pac J Trop Med 2015; 8: 94-97.
32. Floriano AM, Rigamonti S, Comandatore F, Scaltriti E, Longbottom D, Livingstone M, et al. Complete genome sequence of Chlamydia avium PV 4360/2, isolated from a feral pigeon in Italy. Microbiol Resour Announc 2020; 9(16):e01509-19.
33. Hedberg K, White KE, Forfang JC, Korlath JA, Friendshuh KA, Hedberg CW, et al. An outbreak of psittacosis in Minnesota turkey industry workers: implications for modes of transmission and control. Am J Epidemiol 1989; 130: 569-577.
34. Beeckman DS, Vanrompay DC. Zoonotic Chlamydophila psittaci infections from a clinical perspective. Clin Microbiol Infect 2009; 15: 11-17.
| Files | ||
| Issue | Vol 12 No 4 (2020) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v12i4.3937 | |
| Keywords | ||
| Chlamydia psittaci; Polymerase chain reaction; Pigeons; Genotype B; Chlamydia avium | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Golestani N, Haghighi Khoshkhoo P, Hosseini H, Akbari Azad G. Detection and identification of Chlamydia spp. from pigeons in Iran by nested PCR and sequencing. Iran J Microbiol. 2020;12(4):331-337.
