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Strain variation and antigenic divergence among Bordetella pertussis circulating strains isolated from patients in Iran

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Abstract

Despite global efforts and widespread vaccination to control whooping cough (pertussis) caused by B. pertussis, the re-emergence of pertussis still is being reported all over the world. Antigenic divergence in B. pertussis virulence factors is one of the reasons of pertussis resurgence, resulting in dissimilarity of local and vaccine strains. In this study, clonal spread and variation of B. pertussis virulence factor in isolated strains from Iranian patients have been analyzed. A total of 100 B. pertussis isolates were obtained from Pertussis Reference Laboratory of Pasteur Institute of Iran. Real-time PCR were performed to confirm the B. pertussis strains. The genomic patterns of B. pertussis strains were analyzed by pulsed-field gel electrophoresis (PFGE). Predominant alleles of local strains were ptxP3, ptxA1, prn2, fim 2-1, fim3-2, and cya2. PFGE results showed 25 patterns clustered into 18 PFGE groups. A few similarities between the circulating isolates, vaccine, and standard strains were obtained. Significantly, 48% of the isolates showed dominant pattern with different allelic profiles from vaccine strains. According to the genomic profiles, the clonal spread was observed among the circulating strains. Predominant virulence factor profile was also comparable with other countries. It may be suggested that strain variation between vaccine and local strains may have an effect on pertussis resurgence in Iran like other parts of the world.

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References

  1. Bjørnstad ON, Harvill ET (2005) Evolution and emergence of Bordetella in humans. Trends Microbiol 13(8):355–359

    Article  CAS  PubMed  Google Scholar 

  2. Baxter R, Hansen J, Timbol J, Pool V, Greenberg DP, Johnson DR, Decker MD (2016) Post-licensure safety surveillance study of routine use of tetanus toxoid, reduced diphtheria toxoid and 5-component acellular pertussis vaccine. Hum Vaccin Immunother 12(11):2742–2748

    Article  PubMed  PubMed Central  Google Scholar 

  3. Fabianova K, Benes C, Kriz B (2010) A steady rise in incidence of pertussis since nineties in the Czech Republic. Epidemiol Mikrobiol Imunol 59(1):25–33

    CAS  PubMed  Google Scholar 

  4. Oza S, Lawn JE, Hogan DR, Mathers C, Cousens SN (2014) Neonatal cause-of-death estimates for the early and late neonatal periods for 194 countries: 2000–2013. Bull World Health Organ 93:19–28

    Article  PubMed  PubMed Central  Google Scholar 

  5. Winter K, Harriman K, Zipprich J, Schechter R, Talarico J, Watt J, Chavez G (2012) California pertussis epidemic, 2010. J Pediatr 161(6):1091–1096

    Article  PubMed  Google Scholar 

  6. Winter K, Glaser C, Watt J, Harriman K (2014) Pertussis epidemic—California, 2014. MMWR Morb Mortal Wkly Rep 63(48):1129–1132

    PubMed  PubMed Central  Google Scholar 

  7. Donegan K, King B, Bryan P (2014) Safety of pertussis vaccination in pregnant women in UK: observational study. Bmj 349:g4219

    Article  PubMed  PubMed Central  Google Scholar 

  8. Guiso N (2014) Bordetella pertussis: why is it still circulating? J Infect 68:S119–S124

    Article  PubMed  Google Scholar 

  9. van Gent M, de Greeff SC, van der Heide HG, Mooi FR (2009) An investigation into the cause of the 1983 whooping cough epidemic in the Netherlands. Vaccine 27(13):1898–1903

    Article  PubMed  Google Scholar 

  10. McNabb S, Jajosky RA, Hall-Baker P, Adams D, Sharp P, Anderson WJ, Javier A, Jones G, Nitschke DA, Worshams C (2007) Summary of notifiable diseases—United States, 2005. MMWR Morb Mortal Wkly Rep 54(53):1–92

    PubMed  Google Scholar 

  11. Guest C, Wylks C, Ewald B (2007) The epidemiology of pertussis in the Australian Capital Territory, 1999 to 2005-epidemics of testing, disease or false positives? Commun Dis Intell Q Rep 31(4):383

    PubMed  Google Scholar 

  12. Gzyl A, Gniadek G, Augustynowicz E, Rabczenko D, Husejnow B, Zawadka M, Slusarczyk J (2004) Increase in the incidence of pertussis and quality of whole-cell pertussis component of the DTP vaccine produced in Poland. Part I. Potency of DTP vaccine. Przegl Epidemiol 58(4):629–639

    PubMed  Google Scholar 

  13. Dudman S, Trøseid M, Jonassen T, Steinbakk M (2006) Whooping cough—an increasing problem in Norway. Tidsskrift for den Norske laegeforening: tidsskrift for praktisk medicin, ny raekke 126(3):305–308

    Google Scholar 

  14. Mooi FR (2010) Bordetella pertussis and vaccination: the persistence of a genetically monomorphic pathogen. Infect Genet Evol 10(1):36–49

    Article  CAS  PubMed  Google Scholar 

  15. Cassiday P, Sanden G, Heuvelman K, Mooi F, Bisgard KM, Popovic T (2000) Polymorphism in Bordetella pertussis pertactin and pertussis toxin virulence factors in the United States, 1935–1999. J Infect Dis 182(5):1402–1408

    Article  CAS  PubMed  Google Scholar 

  16. Gent Mv (2013) Molecular studies into the causes of the resurgence of Bordetella pertussis in the face of vaccination. [Sl: sn]

  17. Bouchez V, Hegerle N, Strati F, Njamkepo E, Guiso N (2015) New data on vaccine antigen deficient Bordetella pertussis isolates. Vaccines 3(3):751–770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Komatsu E, Yamaguchi F, Abe A, Weiss AA, Watanabe M (2010) Synergic effect of genotype changes in pertussis toxin and pertactin on adaptation to an acellular pertussis vaccine in the murine intranasal challenge model. Clin Vaccine Immunol 17(5):807–812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Weiss AA, Hewlett EL (1986) Virulence factors of Bordetella pertussis. Ann Rev Microbiol 40(1):661–686

    Article  CAS  Google Scholar 

  20. Hegerle N, Guiso N (2014) Bordetella pertussis and pertactin-deficient clinical isolates: lessons for pertussis vaccines. Exp Rev Vaccines 13(9):1135–1146

    Article  CAS  Google Scholar 

  21. King AJ, van der Lee S, Mohangoo A, van Gent M, van der Ark A, van de Waterbeemd B (2013) Genome-wide gene expression analysis of Bordetella pertussis isolates associated with a resurgence in pertussis: elucidation of factors involved in the increased fitness of epidemic strains. PLoS One 8(6):e66150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Safarchi A, Octavia S, Luu LDW, Tay CY, Sintchenko V, Wood N, Marshall H, McIntyre P, Lan R (2015) Pertactin negative Bordetella pertussis demonstrates higher fitness under vaccine selection pressure in a mixed infection model. Vaccine 33(46):6277–6281

    Article  CAS  PubMed  Google Scholar 

  23. Barkoff A-M, Mertsola J, Guillot S, Guiso N, Berbers G, He Q (2012) Appearance of Bordetella pertussis strains not expressing the vaccine antigen pertactin in Finland. Clin Vaccine Immunol 19(10):1703–1704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Lam C, Octavia S, Ricafort L, Sintchenko V, Gilbert GL, Wood N, McIntyre P, Marshall H, Guiso N, Keil AD (2014) Rapid increase in pertactin-deficient Bordetella pertussis isolates, Australia. Emerg Infect Dis 20(4):626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Advani A, Hallander HO, Dalby T, Krogfelt KA, Guiso N, Njamkepo E, von Könnig CHW, Riffelmann M, Mooi FR, Sandven P (2013) Pulsed-field gel electrophoresis analysis of Bordetella pertussis isolates circulating in Europe from 1998 to 2009. J Clin Microbiol 51(2):422–428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Haghighi F, Shahcheraghi F, Abbasi E, Eshraghi SS, Zeraati H, Mousavi SAJ, Asgarian-Omran H, Douraghi M, Shokri F (2014) Genetic profile variation in vaccine strains and clinical isolates of Bordetella pertussis recovered from iranian patients. Avicenna J Med Biotechnol 6(3):178

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Advani A, Donnelly D, Hallander H (2004) Reference system for characterization of Bordetella pertussis pulsed-field gel electrophoresis profiles. J Clin Microbiol 42(7):2890–2897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Bisgard KM, Christie CD, Reising SF, Sanden GN, Cassiday PK, Gomersall C, Wattigney WA, Roberts NE, Strebel PM (2001) Molecular epidemiology of Bordetella pertussis by pulsed-field gel electrophoresis profile: Cincinnati, 1989–1996. J Infect Dis 183(9):1360–1367

    Article  CAS  PubMed  Google Scholar 

  29. Caro V, Hot D, Guigon G, Hubans C, Arrivé M, Soubigou G, Renauld-Mongénie G, Antoine R, Locht C, Lemoine Y (2006) Temporal analysis of French Bordetella pertussis isolates by comparative whole-genome hybridization. Microbes Infect 8(8):2228–2235

    Article  CAS  PubMed  Google Scholar 

  30. Lotfi MN, Nikbin VS, Nasiri O, Badmasti F, Shahcheraghi F (2017) Molecular detection of Bordetella holmesii in two infants with pertussis-like syndrome: the first report from Iran. Iranian journal of microbiology 9(4):219

    PubMed  PubMed Central  Google Scholar 

  31. Nikbin VS, Ahmadi NJ, Hosseinpour M, Lotfi MN, Shooraj F, Sadeghpour F, Shahcheraghi F (2015) Virulence factors variation among Bordetella pertussis isolates in Iran. Int J Mol Cell Med 4(2):138

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Sadeghpour Heravi F, Nikbin V, Shahcheraghi F (2015) Allelic variations between vaccine strains and circulating strains in pxtP of Bordetella pertussis in Iran. Vaccine Res 2(3):19–23

    Article  Google Scholar 

  33. Van Amersfoorth S, Schouls L, Van der Heide H, Advani A, Hallander H, Bondeson K, Von König C, Riffelmann M, Vahrenholz C, Guiso N (2005) Analysis of Bordetella pertussis populations in European countries with different vaccination policies. J Clin Microbiol 43(6):2837–2843

    Article  PubMed  PubMed Central  Google Scholar 

  34. Diavatopoulos D, Hijnen M, Mooi F (2006) Adaptive evolution of the Bordetella autotransporter pertactin. J Evol Biol 19(6):1931–1938

    Article  CAS  PubMed  Google Scholar 

  35. Bart MJ, van Gent M, van der Heide HG, Boekhorst J, Hermans P, Parkhill J, Mooi FR (2010) Comparative genomics of prevaccination and modern Bordetella pertussis strains. BMC Genomics 11(1):627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. De Gouw D, Diavatopoulos DA, Bootsma HJ, Hermans PW, Mooi FR (2011) Pertussis: a matter of immune modulation. FEMS Microbiol Rev 35(3):441–474

    Article  CAS  PubMed  Google Scholar 

  37. Higgs R, Higgins S, Ross P, Mills K (2012) Immunity to the respiratory pathogen Bordetella pertussis. Mucosal Immunol 5(5):485

    Article  CAS  PubMed  Google Scholar 

  38. Fedele G, Bianco M, Ausiello CM (2013) The virulence factors of Bordetella pertussis: talented modulators of host immune response. Arch Immunol Ther Exp 61(6):445–457

    Article  CAS  Google Scholar 

  39. Van Gent M, Van Loo IH, Heuvelman KJ, De Neeling AJ, Teunis P, Mooi FR (2011) Studies on Prn variation in the mouse model and comparison with epidemiological data. PLoS One 6(3):e18014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Mooi FR, Van Loo I, King AJ (2001) Adaptation of Bordetella pertussis to vaccination: a cause for its reemergence? Emerg Infect Dis 7(3 Suppl):526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Fry NK, Neal S, Harrison TG, Miller E, Matthews R, George RC (2001) Genotypic variation in the Bordetella pertussis virulence factors pertactin and pertussis toxin in historical and recent clinical isolates in the United Kingdom. Infect Immun 69(9):5520–5528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Kallonen T (2011) Evolution of Bordetella pertussis post vaccination, University of Turku, Turku

  43. de Melker HE, Schellekens J, Neppelenbroek S, Mooi F, Rümke H, Conyn-van Spaendonck M (2000) Reemergence of pertussis in the highly vaccinated population of the Netherlands: observations on surveillance data. Emerg Infect Dis 6(4):348

    Article  PubMed  PubMed Central  Google Scholar 

  44. Dorji D, Mooi F, Yantorno O, Deora R, Graham RM, Mukkur TK (2017) Bordetella pertussis virulence factors in the continuing evolution of whooping cough vaccines for improved performance. Med Microbiol Immunol 207:1–24. https://doi.org/10.1007/s00430-017-0524-z

  45. Mooi FR, Zeddeman A, Mv G (2015) The pertussis problem: classical epidemiology and strain characterization should go hand in hand. J Pediatr 91(4):315–317

    Article  Google Scholar 

  46. Hallander H, Advani A, Riffelmann M, Von König CH, Caro V, Guiso N, Mooi FR, Gzyl A, Kaltoft MS, Fry NK (2007) Bordetella pertussis strains circulating in Europe in 1999 to 2004 as determined by pulsed-field gel electrophoresis. J Clin Microbiol 45(10):3257–3262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Barkoff A-M, Mertsola J, Pierard D, Dalby T, Hoegh SV, Guillot S, Stefanelli P, van Gent M, Berbers G, Vestrheim DF (2018) Surveillance of circulating Bordetella pertussis strains in Europe during 1998 to 2015. J Clin Microbiol 56(5):e01998-01917

    Article  Google Scholar 

  48. Czarkowski M, Cielebak E, Kondej E, Staszewska E (2013) Infectious diseases and poisonings in Poland in 2012. Bulletin of the National Institute of Public Health and Chief Sanitary Inspectorate: Warszawa, Poland

  49. Polak M, Lutyńska A (2017) Znaczenie szczepów Bordetella pertussis niewytwarzających czynników zjadliwości w epidemiologii krztuśca. Advances in Hygiene & Experimental Medicine. Postepy Hig Med Dosw 71:367-379

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Acknowledgments

We would also like to show our gratitude to all the staff in Pertussis Reference Laboratory‚ Department of Bacteriology and Microbiology Research Center who shared their wisdom with us during this research.

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Correspondence to Fereshteh Shahcheraghi.

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The authors declare that they have no conflicts of interest.

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Fatemah Sadeghpour Heravi and Vajihe Sadat Nikbin have equally collaborated and should be considered co-first authors.

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Sadeghpour Heravi, F., Nikbin, V.S., Nakhost Lotfi, M. et al. Strain variation and antigenic divergence among Bordetella pertussis circulating strains isolated from patients in Iran. Eur J Clin Microbiol Infect Dis 37, 1893–1900 (2018). https://doi.org/10.1007/s10096-018-3323-6

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  • DOI: https://doi.org/10.1007/s10096-018-3323-6

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