Fha Deficient Bordetella pertussis Isolates in Iran with 50 Years Whole Cell Pertussis Vaccination
-
Samaneh Saedi
,
Azadeh Safarchi
,
Faranak Tayebzadeh Moghadam
,
Siamak Heidarzadeh
,
Vajihe Sadat Nikbin
,
Fereshteh Shahcheraghi
Abstract
Background: Bordetella pertussis, a highly contagious respiratory. Notably, the resurgence of pertussis has recently been associated with the lacking production of vaccine virulence factors. This study aimed to screen pertactin (Prn) and filamentous hemagglutinin (Fha) production in Iran with 50 years' whole cell vaccine (WCV) immunization program.
Methods: Overall, 130 B. pertussis isolates collected from Pertussis Reference Laboratory of Iran during 2005-2018. Real-time PCR was performed by targeting IS481, ptxP, IS1001 and IS1002 for species confirmation of B. pertussis. Western-blot was used to evaluate the expression of virulence factors (pertactin and filamentous hemagglutinin).
Results: All tested B. pertussis isolates expressed Prn and all except two isolates expressed Fha. We have sequenced genomes of these strains and identified differences compared with genome reference B. pertussis Tohama I.
Conclusion: Many countries reporting Prn and Fha-deficiency due to acellular vaccine (ACV) pressure. Our results demonstrate in a country with WCV history, Fha-deficient isolates may rise independently. However, Prn-deficient isolates are more under the ACV pressure in B. pertussis isolates. Continues surveillance will provide a better understanding of the effect of WCV on the evolution of the pathogen deficiency.
1. Sáfadi MAP (2015). Pertussis in young infants: a severe vaccine-preventable disease. Autops Case Rep, 5(2):1–4.
2. Advani A, Hallander HO, Dalby T, et al (2013). Pulsed-field gel electrophoresis analysis of Bordetella pertussis isolates circulating in Europe from 1998 to 2009. J Clin Microbiol, 51(2):422-8.
3. Ausiello CM, Cassone A (2014). Acellular pertussis vaccines and pertussis resurgence: revise or replace? : mBio, 5(3):e01339-14.
4. Cherry JD (2012). Epidemic pertussis in 2012—the resurgence of a vaccine-preventable disease. N Engl J Med, 367(9):785-7.
5. Safarchi A, Octavia S, Wu SZ, et al (2016). Genomic dissection of Australian Bordetella pertussis isolates from the 2008–2012 epidemic. J Infect, 72(4):468-77.
6. Sealey KL, Harris SR, Fry NK, et al (2015). Genomic analysis of isolates from the United Kingdom 2012 pertussis outbreak reveals that vaccine antigen genes are unusually fast evolving. J Infect Dis, 212(2):294-301.
7. Winter K, Glaser C, Watt J, Harriman K (2014). Pertussis epidemic--California, 2014. MMWR Morb Mortal Wkly Rep, 63(48):1129-32.
8. Bart MJ, Harris SR, Advani A, et al (2014). Global population structure and evolution of Bordetella pertussis and their relationship with vaccination. mBio, 5(2):e01074.
9. Chiappini E, Stival A, Galli L, De Martino M (2013). Pertussis re-emergence in the post-vaccination era. BMC Infect Dis, 13:151.
10. He Q, Mertsola J (2008). Factors contributing to pertussis resurgence. Future Microbiol, 3(3):329-39.
11. Syed MA (2017). Choosing from Whole Cell and Acellular Pertussis Vaccines-Dilemma for the Developing Countries. Iran J Public Health, 46(2):272–3.
12. Lam C, Octavia S, Bahrame Z, et al (2012). Selection and emergence of pertussis toxin promoter ptxP3 allele in the evolution of Bordetella pertussis. Infect Genet Evol, 12(2):492-5.
13. Lam C, Octavia S, Ricafort L, et al (2014). Rapid increase in pertactin-deficient Bordetella pertussis isolates, Australia. Emerg Infect Dis, 20(4):626–33.
14. Pawloski L, Queenan A, Cassiday P, et al (2014). Prevalence and molecular characterization of pertactin-deficient Bordetella pertussis in the United States. Clin Vaccine Immunol, 21(2):119-25.
15. Zeddeman A, Van Gent M, Heuvelman C, et al (2014). Investigations into the emergence of pertactin-deficient Bordetella pertussis isolates in six European countries, 1996 to 2012. Euro Surveill, 19(33):20881.
16. Belcher T, Preston A (2015). Bordetella pertussis evolution in the (functional) genomics era. Pathog Dis, 73(8): ftv064.
17. Bouchez V, Hegerle N, Strati F, et al (2015). New data on vaccine antigen deficient Bordetella pertussis isolates. Vaccines (Ba-sel), 3(3):751-70.
18. Nikbin VS, Ahmadi NJ, Hosseinpour M, et al (2015). Virulence factors variation among Bordetella pertussis isolates in Iran. Int J Mol Cell Med, 4(2):138–42.
19. Zarei S, Jeddi-Tehrani M, Zeraati H, et al (2009). Short term reactogenicity of a triple Diphtheria-Tetanus-Whole cell pertussis vaccine in Iranian infants. Iran J Public Health, 38(1):100-11.
20. Gouya MM (2009). Expanded programme on immunization in Iran: last 3 decades achievements from 1979 to 2008. Iran J Public Health, 38(Suppl 1):81.
21. Moradi-Lakeh M, Esteghamati A (2013). National Immunization Program in Iran: whys and why nots. Hum Vaccin Immunother, 9(1):112-4.
22. Khazaei S, Ayubi E, Mansori K, Khazaei S (2016). Pertussis incidence by time, province and age group in Iran, 2006-2011. Iran J Public Health, 45(11):1525-7.
23. Heravi FS, Nikbin VS, Lotfi MN, et al (2018). Strain variation and antigenic divergence among Bordetella pertussis circulating strains isolated from patients in Iran. Eur J Clin Microbiol Infect Dis, 37(10):1893-1900.
24. Lotfi MN, Nikbin VS, Nasiri O, et al (2017). Molecular detection of Bordetella holmesii in two infants with pertussis-like syndrome: the first report from Iran. Iran J Microbiol, 9(4):219-23.
25. Mooi F, Hallander H, Von König CW, et al (2000). Epidemiological typing of Bordetella pertussis isolates: recommendations for a standard methodology. Eur J Clin Microbiol Infect Dis, 19(3):174-81.
26. van Loo IH, Heuvelman KJ, King AJ, Mooi FR (2002). Multilocus sequence typing of Bordetella pertussis based on surface protein genes. J Clin Microbiol, 40(6):1994-2001.
27. Bottero D, Gaillard ME, Fingermann M, et al (2007). Pulsed-field gel electrophoresis, pertactin, pertussis toxin S1 subunit polymorphisms, and surfaceome analysis of vaccine and clinical Bordetella pertussis strains. Clin Vaccine Immunol, 14(11):1490-8.
28. Guiso N, von Konig CW, Becker C, Hallander H (2001). Fimbrial typing of Bordetella pertussis isolates: agglutination with polyclonal and monoclonal antisera. J Clin Microbiol, 39(4):1684-5.
29. Ghasemi A, Salari MH, Zarnani AH, et al (2013). Immune reactivity of Brucella melitensis–vaccinated rabbit serum with recombinant Omp31 and DnaK proteins. Iran J Microbiol, 5(1):19–23.
30. Octavia S, Lan R (2006). Frequent recombination and low level of clonality within Salmonella enterica subspecies I. Microbiology (Reading), 152(Pt 4):1099-1108.
31. Darling AE, Mau B, Perna NT (2010). ProgressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One, 5(6):e11147.
32. Bankevich A, Nurk S, Antipov D, et al (2012). SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol, 19(5):455-77.
33. Li H, Durbin R (2009). Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics, 25(14):1754-60.
34. Li H, Handsaker B, Wysoker A, et al (2009). The sequence alignment/map format and SAMtools. Bioinformatics, 25(16):2078-9.
35. Gogol EB, Cummings CA, Burns RC, Relman DA (2007). Phase variation and microevolution at homopolymeric tracts in Bordetella pertussis. BMC Genomics, 8:122.
36. Scheller EV, Cotter PA (2015). Bordetella filamentous hemagglutinin and fimbriae: critical adhesins with unrealized vaccine potential. Pathog Dis, 73(8):ftv079.
37. Carbonetti NH (2016). Bordetella pertussis: new concepts in pathogenesis and treatment. Curr Opin Infect Dis, 29(3):287–94.
38. Smith AM, Guzmán CA, Walker MJ (2001). The virulence factors of Bordetella pertussis: a matter of control. FEMS Microbiol Rev, 25(3):309-33.
39. Preston A (2016). The role of B. pertussis vaccine antigen gene variants in pertussis resurgence and possible consequences for vaccine development. Hum Vaccin Immunother, 12(5):1274-6.
40. Leininger E, Roberts M, Kenimer JG, et al (1991). Pertactin, an Arg-Gly-Asp-containing Bordetella pertussis surface protein that promotes adherence of mammalian cells. Proc Natl Acad Sci U S A, 88(2):345-9.
41. Weigand MR, Pawloski LC, Peng Y, et al (2018). Screening and genomic characterization of filamentous hemagglutinin-deficient Bordetella pertussis. Infect Immun, 86(4):e00869-17.
42. Hegerle N, Guiso N (2013). Epidemiology of whooping cough & typing of Bordetella pertussis. Future Microbiol, 8(11):1391-403.
43. De Gouw D, Diavatopoulos DA, Bootsma HJ, et al (2011). Pertussis: a matter of immune modulation. FEMS Microbiol Rev, 35(3):441-74.
44. Hegerle N, Paris A-S, Brun D, et al (2012). Evolution of French Bordetella pertussis and Bordetella parapertussis isolates: increase of Bordetellae not expressing pertactin. Clin Microbiol Infect, 18(9):E340-6.
45. Guiso N (2009). Bordetella pertussis and pertussis vaccines. Clin Infect Dis, 49(10):1565-9.
46. Polak M, Zasada AA, Mosiej E, et al (2019). Pertactin-deficient Bordetella pertussis isolates in Poland—a country with whole-cell pertussis primary vaccination. Microbes Infect, 21(3-4):170-5.
47. Bodilis H, Guiso N (2013). Virulence of pertactin-negative Bordetella pertussis isolates from infants, France. Emerg Infect Dis, 19(3):471–4.
48. Hallander H, Advani A, Riffelmann M, et al (2007). Bordetella pertussis strains circulating in Europe in 1999 to 2004 as determined by pulsed-field gel electrophoresis. J Clin Microbiol, 45(10):3257-62.
49. Shuel M, Jamieson FB, Tang P, et al (2013). Genetic analysis of Bordetella pertussis in Ontario, Canada reveals one predominant clone. Int J Infect Dis, 17(6):e413-7.
50. Octavia S, Sintchenko V, Gilbert GL, et al (2012). Newly emerging clones of Bordetella pertussis carrying prn2 and ptxP3 alleles implicated in Australian pertussis epidemic in 2008–2010. J Infect Dis, 205(8):1220-4.
51. Kurova N, Njamkepo E, Brun D, Tseneva G, Guiso N (2010). Monitoring of Bordetella isolates circulating in Saint Petersburg, Russia between 2001 and 2009. Res Microbiol, 161(10):810-5.
52. Orsi RH, Bowen BM, Wiedmann M (2010). Homopolymeric tracts represent a general regulatory mechanism in prokaryotes. BMC Genomics, 11:102.
53. Xu Z, Octavia S, Luu LDW, et al (2019). Pertactin-Negative and Filamentous Hemagglutinin-Negative Bordetella pertussis, Australia, 2013–2017. Emerg Infect Dis, 25(6):1196–1199.
54. Park J, Zhang Y, Buboltz AM, et al (2012). Comparative genomics of the classical Bordetella subspecies: the evolution and exchange of virulence-associated diversity amongst closely related pathogens. BMC Genomics, 13:545.
2. Advani A, Hallander HO, Dalby T, et al (2013). Pulsed-field gel electrophoresis analysis of Bordetella pertussis isolates circulating in Europe from 1998 to 2009. J Clin Microbiol, 51(2):422-8.
3. Ausiello CM, Cassone A (2014). Acellular pertussis vaccines and pertussis resurgence: revise or replace? : mBio, 5(3):e01339-14.
4. Cherry JD (2012). Epidemic pertussis in 2012—the resurgence of a vaccine-preventable disease. N Engl J Med, 367(9):785-7.
5. Safarchi A, Octavia S, Wu SZ, et al (2016). Genomic dissection of Australian Bordetella pertussis isolates from the 2008–2012 epidemic. J Infect, 72(4):468-77.
6. Sealey KL, Harris SR, Fry NK, et al (2015). Genomic analysis of isolates from the United Kingdom 2012 pertussis outbreak reveals that vaccine antigen genes are unusually fast evolving. J Infect Dis, 212(2):294-301.
7. Winter K, Glaser C, Watt J, Harriman K (2014). Pertussis epidemic--California, 2014. MMWR Morb Mortal Wkly Rep, 63(48):1129-32.
8. Bart MJ, Harris SR, Advani A, et al (2014). Global population structure and evolution of Bordetella pertussis and their relationship with vaccination. mBio, 5(2):e01074.
9. Chiappini E, Stival A, Galli L, De Martino M (2013). Pertussis re-emergence in the post-vaccination era. BMC Infect Dis, 13:151.
10. He Q, Mertsola J (2008). Factors contributing to pertussis resurgence. Future Microbiol, 3(3):329-39.
11. Syed MA (2017). Choosing from Whole Cell and Acellular Pertussis Vaccines-Dilemma for the Developing Countries. Iran J Public Health, 46(2):272–3.
12. Lam C, Octavia S, Bahrame Z, et al (2012). Selection and emergence of pertussis toxin promoter ptxP3 allele in the evolution of Bordetella pertussis. Infect Genet Evol, 12(2):492-5.
13. Lam C, Octavia S, Ricafort L, et al (2014). Rapid increase in pertactin-deficient Bordetella pertussis isolates, Australia. Emerg Infect Dis, 20(4):626–33.
14. Pawloski L, Queenan A, Cassiday P, et al (2014). Prevalence and molecular characterization of pertactin-deficient Bordetella pertussis in the United States. Clin Vaccine Immunol, 21(2):119-25.
15. Zeddeman A, Van Gent M, Heuvelman C, et al (2014). Investigations into the emergence of pertactin-deficient Bordetella pertussis isolates in six European countries, 1996 to 2012. Euro Surveill, 19(33):20881.
16. Belcher T, Preston A (2015). Bordetella pertussis evolution in the (functional) genomics era. Pathog Dis, 73(8): ftv064.
17. Bouchez V, Hegerle N, Strati F, et al (2015). New data on vaccine antigen deficient Bordetella pertussis isolates. Vaccines (Ba-sel), 3(3):751-70.
18. Nikbin VS, Ahmadi NJ, Hosseinpour M, et al (2015). Virulence factors variation among Bordetella pertussis isolates in Iran. Int J Mol Cell Med, 4(2):138–42.
19. Zarei S, Jeddi-Tehrani M, Zeraati H, et al (2009). Short term reactogenicity of a triple Diphtheria-Tetanus-Whole cell pertussis vaccine in Iranian infants. Iran J Public Health, 38(1):100-11.
20. Gouya MM (2009). Expanded programme on immunization in Iran: last 3 decades achievements from 1979 to 2008. Iran J Public Health, 38(Suppl 1):81.
21. Moradi-Lakeh M, Esteghamati A (2013). National Immunization Program in Iran: whys and why nots. Hum Vaccin Immunother, 9(1):112-4.
22. Khazaei S, Ayubi E, Mansori K, Khazaei S (2016). Pertussis incidence by time, province and age group in Iran, 2006-2011. Iran J Public Health, 45(11):1525-7.
23. Heravi FS, Nikbin VS, Lotfi MN, et al (2018). Strain variation and antigenic divergence among Bordetella pertussis circulating strains isolated from patients in Iran. Eur J Clin Microbiol Infect Dis, 37(10):1893-1900.
24. Lotfi MN, Nikbin VS, Nasiri O, et al (2017). Molecular detection of Bordetella holmesii in two infants with pertussis-like syndrome: the first report from Iran. Iran J Microbiol, 9(4):219-23.
25. Mooi F, Hallander H, Von König CW, et al (2000). Epidemiological typing of Bordetella pertussis isolates: recommendations for a standard methodology. Eur J Clin Microbiol Infect Dis, 19(3):174-81.
26. van Loo IH, Heuvelman KJ, King AJ, Mooi FR (2002). Multilocus sequence typing of Bordetella pertussis based on surface protein genes. J Clin Microbiol, 40(6):1994-2001.
27. Bottero D, Gaillard ME, Fingermann M, et al (2007). Pulsed-field gel electrophoresis, pertactin, pertussis toxin S1 subunit polymorphisms, and surfaceome analysis of vaccine and clinical Bordetella pertussis strains. Clin Vaccine Immunol, 14(11):1490-8.
28. Guiso N, von Konig CW, Becker C, Hallander H (2001). Fimbrial typing of Bordetella pertussis isolates: agglutination with polyclonal and monoclonal antisera. J Clin Microbiol, 39(4):1684-5.
29. Ghasemi A, Salari MH, Zarnani AH, et al (2013). Immune reactivity of Brucella melitensis–vaccinated rabbit serum with recombinant Omp31 and DnaK proteins. Iran J Microbiol, 5(1):19–23.
30. Octavia S, Lan R (2006). Frequent recombination and low level of clonality within Salmonella enterica subspecies I. Microbiology (Reading), 152(Pt 4):1099-1108.
31. Darling AE, Mau B, Perna NT (2010). ProgressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One, 5(6):e11147.
32. Bankevich A, Nurk S, Antipov D, et al (2012). SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol, 19(5):455-77.
33. Li H, Durbin R (2009). Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics, 25(14):1754-60.
34. Li H, Handsaker B, Wysoker A, et al (2009). The sequence alignment/map format and SAMtools. Bioinformatics, 25(16):2078-9.
35. Gogol EB, Cummings CA, Burns RC, Relman DA (2007). Phase variation and microevolution at homopolymeric tracts in Bordetella pertussis. BMC Genomics, 8:122.
36. Scheller EV, Cotter PA (2015). Bordetella filamentous hemagglutinin and fimbriae: critical adhesins with unrealized vaccine potential. Pathog Dis, 73(8):ftv079.
37. Carbonetti NH (2016). Bordetella pertussis: new concepts in pathogenesis and treatment. Curr Opin Infect Dis, 29(3):287–94.
38. Smith AM, Guzmán CA, Walker MJ (2001). The virulence factors of Bordetella pertussis: a matter of control. FEMS Microbiol Rev, 25(3):309-33.
39. Preston A (2016). The role of B. pertussis vaccine antigen gene variants in pertussis resurgence and possible consequences for vaccine development. Hum Vaccin Immunother, 12(5):1274-6.
40. Leininger E, Roberts M, Kenimer JG, et al (1991). Pertactin, an Arg-Gly-Asp-containing Bordetella pertussis surface protein that promotes adherence of mammalian cells. Proc Natl Acad Sci U S A, 88(2):345-9.
41. Weigand MR, Pawloski LC, Peng Y, et al (2018). Screening and genomic characterization of filamentous hemagglutinin-deficient Bordetella pertussis. Infect Immun, 86(4):e00869-17.
42. Hegerle N, Guiso N (2013). Epidemiology of whooping cough & typing of Bordetella pertussis. Future Microbiol, 8(11):1391-403.
43. De Gouw D, Diavatopoulos DA, Bootsma HJ, et al (2011). Pertussis: a matter of immune modulation. FEMS Microbiol Rev, 35(3):441-74.
44. Hegerle N, Paris A-S, Brun D, et al (2012). Evolution of French Bordetella pertussis and Bordetella parapertussis isolates: increase of Bordetellae not expressing pertactin. Clin Microbiol Infect, 18(9):E340-6.
45. Guiso N (2009). Bordetella pertussis and pertussis vaccines. Clin Infect Dis, 49(10):1565-9.
46. Polak M, Zasada AA, Mosiej E, et al (2019). Pertactin-deficient Bordetella pertussis isolates in Poland—a country with whole-cell pertussis primary vaccination. Microbes Infect, 21(3-4):170-5.
47. Bodilis H, Guiso N (2013). Virulence of pertactin-negative Bordetella pertussis isolates from infants, France. Emerg Infect Dis, 19(3):471–4.
48. Hallander H, Advani A, Riffelmann M, et al (2007). Bordetella pertussis strains circulating in Europe in 1999 to 2004 as determined by pulsed-field gel electrophoresis. J Clin Microbiol, 45(10):3257-62.
49. Shuel M, Jamieson FB, Tang P, et al (2013). Genetic analysis of Bordetella pertussis in Ontario, Canada reveals one predominant clone. Int J Infect Dis, 17(6):e413-7.
50. Octavia S, Sintchenko V, Gilbert GL, et al (2012). Newly emerging clones of Bordetella pertussis carrying prn2 and ptxP3 alleles implicated in Australian pertussis epidemic in 2008–2010. J Infect Dis, 205(8):1220-4.
51. Kurova N, Njamkepo E, Brun D, Tseneva G, Guiso N (2010). Monitoring of Bordetella isolates circulating in Saint Petersburg, Russia between 2001 and 2009. Res Microbiol, 161(10):810-5.
52. Orsi RH, Bowen BM, Wiedmann M (2010). Homopolymeric tracts represent a general regulatory mechanism in prokaryotes. BMC Genomics, 11:102.
53. Xu Z, Octavia S, Luu LDW, et al (2019). Pertactin-Negative and Filamentous Hemagglutinin-Negative Bordetella pertussis, Australia, 2013–2017. Emerg Infect Dis, 25(6):1196–1199.
54. Park J, Zhang Y, Buboltz AM, et al (2012). Comparative genomics of the classical Bordetella subspecies: the evolution and exchange of virulence-associated diversity amongst closely related pathogens. BMC Genomics, 13:545.
| Files | ||
| Issue | Vol 50 No 7 (2021) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijph.v50i7.6636 | |
| Keywords | ||
| Whooping cough Bordetella pertussis Iran Whole-cell vaccine Filamentous hemagglutinin Pertactin | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Saedi S, Safarchi A, Moghadam FT, Heidarzadeh S, Nikbin VS, Shahcheraghi F. Fha Deficient Bordetella pertussis Isolates in Iran with 50 Years Whole Cell Pertussis Vaccination. Iran J Public Health. 2021;50(7):1454-1462.
