Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 28, Number 5—May 2022
Research

Pertactin-Deficient Bordetella pertussis with Unusual Mechanism of Pertactin Disruption, Spain, 1986–2018

Alba Mir-Cros1, Albert Moreno-Mingorance1, M. Teresa Martín-Gómez, Raquel Abad, Iván Bloise, Magda Campins, Alejandro González-Praetorius, M. Nieves Gutiérrez, Héctor Martín-González, Carmen Muñoz-Almagro, M. Ángeles Orellana, Manuela de Pablos, Josep Roca-Grande, Carlos Rodrigo, M. Elena Rodríguez, Sonia Uriona, M. José Vidal, Tomàs Pumarola, M. Nieves Larrosa, and Juan José González-LópezComments to Author 
Author affiliations: Hospital Universitari Vall d’Hebron Campus, Barcelona, Spain (A. Mir-Cros, A. Moreno-Mingorance, M.T. Martín-Gómez, M. Campins, H. Martín-González, J. Roca-Grande, S. Uriona, T. Pumarola, M.N. Larrosa, J.J. González-López); Universitat Autònoma de Barcelona, Barcelona (A. Mir-Cros, A. Moreno-Mingorance, T. Pumarola, M.N. Larrosa, J.J. González-López); Instituto de Salud Carlos III, Madrid, Spain (R. Abad); Hospital Universitario La Paz, Madrid (I. Bloise, M. de Pablos); Hospital Universitario de Guadalajara, Guadalajara, Spain (A. González-Praetorius, M.E. Rodríguez); Complejo Asistencial Universitario de Salamanca, Salamanca, Spain (M.N. Gutiérrez); Institut de Recerca Sant Joan de Déu, Esplugues de Llobregat, Spain (C. Muñoz-Almagro); Universitat Internacional de Catalunya, Barcelona (C. Muñoz-Almagro); CIBER de Epidemiología y Salud Pública, Barcelona (C. Muñoz-Almagro); Hospital Universitario 12 de Octubre, Madrid (M.Á. Orellana); Hospital Universitari Germans Trias i Pujol, Badalona, Spain (C. Rodrigo); Agència de Salut Pública de Catalunya, Barcelona (M.J. Vidal); CIBER de Enfermedades Infecciosas, Barcelona (T. Pumarola, M.N. Larrosa, J.J. González-López)

Main Article

Table 2

Genomic mechanisms leading to origin deficiency of pertactin among Bordetalla pertussis isolates in Spain, 2006–2018*

Mechanism type Mechanism name Mechanism description Genomic location† Isolates, no. (%) Reference
Deletion
 prn::499STOP-delG1494 G deletion 1494 6 (6.5) This study
prn::del(–292, 1340) Within promoter and first part of prn gene –292 to 1340 54 (58.1) (18)
prn::promoter_del(–614, –75)
 Within promoter
 –614 to –75
 1 (1.1)
 This study
Insertion
 prn::IS481-1613fwd IS481 within prn, forward direction 1613–1614 5 (5.4) (6)
prn::IS481-1613rev IS481 within prn, reverse direction 1613–1614 12 (12.9) (6)
prn::IS481-2735rev
 IS481 within prn, reverse direction
 2735–2736
 5 (5.4)
 (6,19)
Inversion prn::promoter_inv(-74) 22 kb large inversion within promoter –20892 to –75 5 (5.4) (6)

*del, deletion; fwd, forward insertion; inv, inversion; IS, insertion element; prn, pertactin gene; rev, reverse insertion. †Numbers indicate the position of each mechanism relative to the prn2 start codon.

Main Article

References
  1. van Gent  M, Heuvelman  CJ, van der Heide  HG, Hallander  HO, Advani  A, Guiso  N, et al. Analysis of Bordetella pertussis clinical isolates circulating in European countries during the period 1998-2012. Eur J Clin Microbiol Infect Dis. 2015;34:821–30. DOIPubMedGoogle Scholar
  2. Octavia  S, Sintchenko  V, Gilbert  GL, Lawrence  A, Keil  AD, Hogg  G, et al. Newly emerging clones of Bordetella pertussis carrying prn2 and ptxP3 alleles implicated in Australian pertussis epidemic in 2008-2010. J Infect Dis. 2012;205:1220–4. DOIPubMedGoogle Scholar
  3. Mir-Cros  A, Moreno-Mingorance  A, Martín-Gómez  MT, Codina  G, Cornejo-Sánchez  T, Rajadell  M, et al. Population dynamics and antigenic drift of Bordetella pertussis following whole cell vaccine replacement, Barcelona, Spain, 1986-2015. Emerg Microbes Infect. 2019;8:1711–20. DOIPubMedGoogle Scholar
  4. Barkoff  A-M, Mertsola  J, Pierard  D, Dalby  T, Hoegh  SV, Guillot  S, et al. Surveillance of circulating Bordetella pertussis strains in Europe during 1998-2015. J Clin Microbiol. 2018;56:e01998–17. DOIPubMedGoogle Scholar
  5. 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;27:6034–41. DOIPubMedGoogle Scholar
  6. 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;19:20881. DOIPubMedGoogle Scholar
  7. Otsuka  N, Han  H-J, Toyoizumi-Ajisaka  H, Nakamura  Y, Arakawa  Y, Shibayama  K, et al. Prevalence and genetic characterization of pertactin-deficient Bordetella pertussis in Japan. PLoS One. 2012;7:e31985. DOIPubMedGoogle Scholar
  8. Lam  C, Octavia  S, Ricafort  L, Sintchenko  V, Gilbert  GL, Wood  N, et al. Rapid increase in pertactin-deficient Bordetella pertussis isolates, Australia. Emerg Infect Dis. 2014;20:626–33. DOIPubMedGoogle Scholar
  9. 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;21:119–25. DOIPubMedGoogle Scholar
  10. 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;33:6277–81. DOIPubMedGoogle Scholar
  11. Barkoff  A-M, He  Q. Molecular epidemiology of Bordetella pertussis. Adv Exp Med Biol. 2019;1183:19–33. DOIPubMedGoogle Scholar
  12. Bouchez  V, Guillot  S, Landier  A, Armatys  N, Matczak  S, Toubiana  J, et al.; French pertussis microbiology study group. Evolution of Bordetella pertussis over a 23-year period in France, 1996 to 2018. Euro Surveill. 2021;26:2001213. DOIPubMedGoogle Scholar
  13. 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;24:1700832. DOIPubMedGoogle Scholar
  14. Weigand  MR, Williams  MM, Peng  Y, Kania  D, Pawloski  LC, Tondella  ML; CDC Pertussis Working Group. Genomic survey of Bordetella pertussis diversity, United States, 2000–2013. Emerg Infect Dis. 2019;25:780–3. DOIPubMedGoogle Scholar
  15. Barkoff  A-M, Guiso  N, Guillot  S, Xing  D, Markey  K, Berbers  G, et al. A rapid ELISA-based method for screening Bordetella pertussis strain production of antigens included in current acellular pertussis vaccines. J Immunol Methods. 2014;408:142–8. DOIPubMedGoogle Scholar
  16. Tsang  RSW, Sill  ML, Advani  A, Xing  D, Newland  P, Hallander  H. Use of monoclonal antibodies to serotype Bordetella pertussis isolates: comparison of results obtained by indirect whole-cell enzyme-linked immunosorbent assay and bacterial microagglutination methods. J Clin Microbiol. 2005;43:2449–51. DOIPubMedGoogle Scholar
  17. Heikkinen  E, Xing  DK, Ölander  R-M, Hytönen  J, Viljanen  MK, Mertsola  J, et al. Bordetella pertussis isolates in Finland: serotype and fimbrial expression. BMC Microbiol. 2008;8:162. DOIPubMedGoogle Scholar
  18. Weigand  MR, Peng  Y, Cassiday  PK, Loparev  VN, Johnson  T, Juieng  P, et al. Complete genome sequences of Bordetella pertussis isolates with novel pertactin-deficient deletions. Genome Announc. 2017;5:e00973–17. DOIPubMedGoogle Scholar
  19. Weigand  MR, Peng  Y, Loparev  V, Batra  D, Bowden  KE, Burroughs  M, et al. The history of Bordetella pertussis genome evolution includes structural rearrangement. J Bacteriol. 2017;199:e00806–16. DOIPubMedGoogle Scholar
  20. 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;23:699–701. DOIPubMedGoogle Scholar
  21. Martin  SW, Pawloski  L, Williams  M, Weening  K, DeBolt  C, Qin  X, et al. Pertactin-negative Bordetella pertussis strains: evidence for a possible selective advantage. Clin Infect Dis. 2015;60:223–7. DOIPubMedGoogle Scholar
  22. Zomer  A, Otsuka  N, Hiramatsu  Y, Kamachi  K, Nishimura  N, Ozaki  T, et al. Bordetella pertussis population dynamics and phylogeny in Japan after adoption of acellular pertussis vaccines. Microb Genom. 2018;4:e000180. DOIPubMedGoogle Scholar
  23. 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:e77165. DOIPubMedGoogle Scholar
  24. Centro Nacional de Epidemiología, Instituto de Salud Carlos III. Situación de la Tosferina en España, 1998-2016 [cited 2022 Jan 30]. https://www.isciii.es/QueHacemos/Servicios/VigilanciaSaludPublicaRENAVE/EnfermedadesTransmisibles/Documents/archivos%20A-Z/TOSFERINA/Situación%20de%20la%20Tosferina%20en%20España,%201998-2016.pdf
  25. Polak  M, Zasada  AA, Mosiej  E, Krysztopa-Grzybowska  K, Witkowski  L, Rzeczkowska  M, et al. Pertactin-deficient Bordetella pertussis isolates in Poland-a country with whole-cell pertussis primary vaccination. Microbes Infect. 2019;21:170–5. DOIPubMedGoogle Scholar
  26. 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;8:1416–27. DOIPubMedGoogle Scholar
  27. Carriquiriborde  F, Regidor  V, Aispuro  PM, Magali  G, Bartel  E, Bottero  D, et al. Rare detection of Bordetella pertussis pertactin-deficient strains in Argentina. Emerg Infect Dis. 2019;25:2048–54. DOIPubMedGoogle Scholar
  28. 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;25:1196–9. DOIPubMedGoogle Scholar
  29. Kastrin  T, Barkoff  A-M, Paragi  M, Vitek  MG, Mertsola  J, He  Q. High prevalence of currently circulating Bordetella pertussis isolates not producing vaccine antigen pertactin in Slovenia. Clin Microbiol Infect. 2019;25:258–60. DOIPubMedGoogle Scholar
  30. Elomaa  A, Advani  A, Donnelly  D, Antila  M, Mertsola  J, Hallander  H, et al. Strain variation among Bordetella pertussis isolates in finland, where the whole-cell pertussis vaccine has been used for 50 years. J Clin Microbiol. 2005;43:3681–7. DOIPubMedGoogle Scholar
  31. Gorringe  AR, Vaughan  TE. Bordetella pertussis fimbriae (Fim): relevance for vaccines. Expert Rev Vaccines. 2014;13:1205–14. DOIPubMedGoogle Scholar

Main Article

1These authors contributed equally to this article.

Page created: March 23, 2022
Page updated: April 19, 2022
Page reviewed: April 19, 2022
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
file_external