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Surveillance Open Access
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Abstract

Background

is the main agent of whooping cough. Vaccination with acellular pertussis vaccines has been largely implemented in high-income countries. These vaccines contain 1 to 5 antigens: pertussis toxin (PT), filamentous haemagglutinin (FHA), pertactin (PRN) and/or fimbrial proteins (FIM2 and FIM3). Monitoring the emergence of isolates that might partially escape vaccine-induced immunity is an essential component of public health strategies to control whooping cough.

Aim

We aimed to investigate temporal trends of fimbriae serotypes and vaccine antigen-expression in over a 23-year period in France (1996–2018).

Methods

Isolates (n = 2,280) were collected through hospital surveillance, capturing one third of hospitalised paediatric pertussis cases. We assayed PT, FHA and PRN production by Western blot (n = 1,428) and fimbriae production by serotyping (n = 1,058). Molecular events underlying antigen deficiency were investigated by genomic sequencing.

Results

The proportion of PRN-deficient isolates has increased steadily from 0% (0/38) in 2003 to 48.4% (31/64) in 2018 (chi-squared test for trend, p < 0.0001), whereas only 5 PT-, 5 FHA- and 9 FIM-deficient isolates were found. Impairment of PRN production was predominantly due to IS insertion within the gene or a 22 kb genomic inversion involving the promoter sequence, indicative of convergent evolution. FIM2-expressing isolates have emerged since 2011 at the expense of FIM3.

Conclusions

is evolving through the rapid increase of PRN-deficient isolates and a recent shift from FIM3 to FIM2 expression. Excluding PRN, the loss of vaccine antigen expression by circulating isolates is epidemiologically insignificant.

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/content/10.2807/1560-7917.ES.2021.26.37.2001213
2021-09-16
2024-04-25
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2021.26.37.2001213
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References

  1. Yeung KHT, Duclos P, Nelson EAS, Hutubessy RCW. An update of the global burden of pertussis in children younger than 5 years: a modelling study. Lancet Infect Dis. 2017;17(9):974-80.  https://doi.org/10.1016/S1473-3099(17)30390-0  PMID: 28623146 
  2. Esposito S, Stefanelli P, Fry NK, Fedele G, He Q, Paterson P, et al. Pertussis prevention: reasons for resurgence, and differences in the current acellular pertussis vaccines. Front Immunol. 2019;10:1344.  https://doi.org/10.3389/fimmu.2019.01344  PMID: 31333640 
  3. Bart MJ, Harris SR, Advani A, Arakawa Y, Bottero D, Bouchez V, et al. Global population structure and evolution of Bordetella pertussis and their relationship with vaccination. MBio. 2014;5(2):e01074.  https://doi.org/10.1128/mBio.01074-14  PMID: 24757216 
  4. Locht C. Molecular aspects of Bordetella pertussis pathogenesis. Int Microbiol. 1999;2(3):137-44. PMID: 10943406 
  5. Barkoff A-M, He Q. Molecular epidemiology of Bordetella pertussis. Adv Exp Med Biol. 2019;1183:19-33.  https://doi.org/10.1007/5584_2019_402  PMID: 31342459 
  6. Safarchi A, Octavia S, Nikbin VS, Lotfi MN, Zahraei SM, Tay CY, et al. Genomic epidemiology of Iranian Bordetella pertussis: 50 years after the implementation of whole cell vaccine. Emerg Microbes Infect. 2019;8(1):1416-27.  https://doi.org/10.1080/22221751.2019.1665479  PMID: 31543006 
  7. Barkoff A-M, Mertsola J, Pierard D, Dalby T, Hoegh SV, Guillot S, et al. Pertactin-deficient Bordetella pertussis isolates: evidence of increased circulation in Europe, 1998 to 2015. Euro Surveill. 2019;24(7):24.  https://doi.org/10.2807/1560-7917.ES.2019.24.7.1700832  PMID: 30782265 
  8. Ring N, Abrahams JS, Bagby S, Preston A, MacArthur I. How genomics is changing what we know about the evolution and genome of Bordetella pertussis. Adv Exp Med Biol. 2019;1183:1-17.  https://doi.org/10.1007/5584_2019_401  PMID: 31321755 
  9. Hiramatsu Y, Miyaji Y, Otsuka N, Arakawa Y, Shibayama K, Kamachi K. Significant decrease in pertactin-deficient Bordetella pertussis isolates, Japan. Emerg Infect Dis. 2017;23(4):699-701.  https://doi.org/10.3201/eid2304.161575  PMID: 28322702 
  10. Bouchez V, Brun D, Cantinelli T, Dore G, Njamkepo E, Guiso N. First report and detailed characterization of B. pertussis isolates not expressing pertussis toxin or pertactin. Vaccine. 2009;27(43):6034-41.  https://doi.org/10.1016/j.vaccine.2009.07.074  PMID: 19666155 
  11. Williams MM, Sen K, Weigand MR, Skoff TH, Cunningham VA, Halse TA, et al. Bordetella pertussis strain lacking pertactin and pertussis toxin. Emerg Infect Dis. 2016;22(2):319-22.  https://doi.org/10.3201/eid2202.151332  PMID: 26812174 
  12. Weigand MR, Pawloski LC, Peng Y, Ju H, Burroughs M, Cassiday PK, et al. Screening and genomic characterization of filamentous hemagglutinin-deficient Bordetella pertussis. Infect Immun. 2018;86(4):86.  https://doi.org/10.1128/IAI.00869-17  PMID: 29358336 
  13. Gorringe AR, Vaughan TE. Bordetella pertussis fimbriae (Fim): relevance for vaccines. Expert Rev Vaccines. 2014;13(10):1205-14.  https://doi.org/10.1586/14760584.2014.930667  PMID: 25102891 
  14. Miyaji Y, Otsuka N, Toyoizumi-Ajisaka H, Shibayama K, Kamachi K. Genetic analysis of Bordetella pertussis isolates from the 2008-2010 pertussis epidemic in Japan. PLoS One. 2013;8(10):e77165.  https://doi.org/10.1371/journal.pone.0077165  PMID: 24124606 
  15. Shuel M, Lefebvre B, Whyte K, Hayden K, De Serres G, Brousseau N, et al. Antigenic and genetic characterization of Bordetella pertussis recovered from Quebec, Canada, 2002-2014: detection of a genetic shift. Can J Microbiol. 2016;62(5):437-41.  https://doi.org/10.1139/cjm-2015-0781  PMID: 26910633 
  16. Caro V, Elomaa A, Brun D, Mertsola J, He Q, Guiso N. Bordetella pertussis, Finland and France. Emerg Infect Dis. 2006;12(6):987-9.  https://doi.org/10.3201/eid1206.051283  PMID: 16707058 
  17. Tubiana S, Belchior E, Guillot S, Guiso N, Lévy-Bruhl D, Renacoq Participants. Monitoring the impact of vaccination on pertussis in infants using an active hospital-based pediatric surveillance network: results from 17 years’ experience, 1996-2012, France. Pediatr Infect Dis J. 2015;34(8):814-20.  https://doi.org/10.1097/INF.0000000000000739  PMID: 25955837 
  18. Weber C, Boursaux-Eude C, Coralie G, Caro V, Guiso N. Polymorphism of Bordetella pertussis isolates circulating for the last 10 years in France, where a single effective whole-cell vaccine has been used for more than 30 years. J Clin Microbiol. 2001;39(12):4396-403.  https://doi.org/10.1128/JCM.39.12.4396-4403.2001  PMID: 11724851 
  19. Bouchez V, Guglielmini J, Dazas M, Landier A, Toubiana J, Guillot S, et al. Genomic Sequencing of Bordetella pertussis for epidemiology and global surveillance of whooping cough. Emerg Infect Dis. 2018;24(6):988-94.  https://doi.org/10.3201/eid2406.171464  PMID: 29774847 
  20. Bonmarin I, Lévy-Bruhl D, Baron S, Guiso N, Njamkepo E, Caro V, et al. Pertussis surveillance in French hospitals: results from a 10 year period. Euro Surveill. 2007;12(1):678.  https://doi.org/10.2807/esm.12.01.00678-en 
  21. European Commission. 2012/506/EU: Commission Implementing Decision of 8 August 2012 amending Decision 2002/253/EC laying down case definitions for reporting communicable diseases to the Community network under Decision No 2119/98/EC of the European Parliament and of the Council (notified under document C(2012) 5538). Brussels: Official Journal of the European Union; 2012. Available from: https://eur-lex.europa.eu/eli/dec_impl/2012/506/oj
  22. Fine PE, Clarkson JA. The recurrence of whooping cough: possible implications for assessment of vaccine efficacy. Lancet. 1982;1(8273):666-9.  https://doi.org/10.1016/S0140-6736(82)92214-0  PMID: 6121976 
  23. Hegerle N, Paris A-S, Brun D, Dore G, Njamkepo E, Guillot S, et al. Evolution of French Bordetella pertussis and Bordetella parapertussis isolates: increase of Bordetellae not expressing pertactin. Clin Microbiol Infect. 2012;18(9):E340-6.  https://doi.org/10.1111/j.1469-0691.2012.03925.x  PMID: 22717007 
  24. Bouchez V, Hegerle N, Strati F, Njamkepo E, Guiso N. New data on vaccine antigen deficient Bordetella pertussis isolates. Vaccines (Basel). 2015;3(3):751-70.  https://doi.org/10.3390/vaccines3030751  PMID: 26389958 
  25. Bart MJ, van der Heide HGJ, Zeddeman A, Heuvelman K, van Gent M, Mooi FR. Complete genome sequences of 11 Bordetella pertussis strains representing the pandemic ptxP3 lineage. Genome Announc. 2015;3(6):3.  https://doi.org/10.1128/genomeA.01394-15  PMID: 26607899 
  26. Xu Z, Octavia S, Luu LDW, Payne M, Timms V, Tay CY, et al. Pertactin-negative and filamentous hemagglutinin-negative Bordetella pertussis, Australia, 2013-2017. Emerg Infect Dis. 2019;25(6):1196-9.  https://doi.org/10.3201/eid2506.180240  PMID: 31107218 
  27. Zeddeman A, van Gent M, Heuvelman CJ, van der Heide HG, Bart MJ, Advani A, et al. Investigations into the emergence of pertactin-deficient Bordetella pertussis isolates in six European countries, 1996 to 2012. Euro Surveill. 2014;19(33):19.  https://doi.org/10.2807/1560-7917.ES2014.19.33.20881  PMID: 25166348 
  28. Pawloski LC, Queenan AM, Cassiday PK, Lynch AS, Harrison MJ, Shang W, et al. Prevalence and molecular characterization of pertactin-deficient Bordetella pertussis in the United States. Clin Vaccine Immunol. 2014;21(2):119-25.  https://doi.org/10.1128/CVI.00717-13  PMID: 24256623 
  29. Ma L, Caulfield A, Dewan KK, Harvill ET. Pertactin-deficient Bordetella pertussis, vaccine-driven evolution, and reemergence of pertussis. Emerg Infect Dis. 2021;27(6):1561-6.  https://doi.org/10.3201/eid2706.203850  PMID: 34014152 
  30. Cherry JD. The 112-year odyssey of pertussis and pertussis vaccines-mistakes made and implications for the future. J Pediatric Infect Dis Soc. 2019;8(4):334-41.  https://doi.org/10.1093/jpids/piz005  PMID: 30793754 
  31. Hegerle N, Dore G, Guiso N. Pertactin deficient Bordetella pertussis present a better fitness in mice immunized with an acellular pertussis vaccine. Vaccine. 2014;32(49):6597-600.  https://doi.org/10.1016/j.vaccine.2014.09.068  PMID: 25312274 
  32. Safarchi A, Octavia S, Luu LDW, Tay CY, Sintchenko V, Wood N, et al. Pertactin negative Bordetella pertussis demonstrates higher fitness under vaccine selection pressure in a mixed infection model. Vaccine. 2015;33(46):6277-81.  https://doi.org/10.1016/j.vaccine.2015.09.064  PMID: 26432908 
  33. Bodilis H, Guiso N. Virulence of pertactin-negative Bordetella pertussis isolates from infants, France. Emerg Infect Dis. 2013;19(3):471-4.  https://doi.org/10.3201/eid1903.121475  PMID: 23621904 
  34. Centers for Disease Control and Prevention. Pertussis vaccination: use of acellular pertussis vaccines among infants and young children. Recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep. 1997;46(RR-7):1-25. PMID: 9091780 
  35. Heikkinen E, Xing DK, Olander R-M, Hytönen J, Viljanen MK, Mertsola J, et al. Bordetella pertussis isolates in Finland: serotype and fimbrial expression. BMC Microbiol. 2008;8(1):162.  https://doi.org/10.1186/1471-2180-8-162  PMID: 18816412 
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