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Volume 27, Number 3—March 2021
Research

Isolate-Based Surveillance of Bordetella pertussis, Austria, 2018–2020

Adriana CabalComments to Author , Daniela Schmid, Markus Hell, Ali Chakeri, Elisabeth Mustafa-Korninger, Alexandra Wojna, Anna Stöger, Johannes Möst, Eva Leitner, Patrick Hyden, Thomas Rattei, Adele Habington, Ursula Wiedermann, Franz Allerberger, and Werner Ruppitsch
Author affiliations: Institute for Medical Microbiology and Hygiene, Austrian Agency for Health and Food Safety, Vienna, Austria (A. Cabal, D. Schmid, A. Chakeri, A. Stöger, F. Allerberger, W. Ruppitsch); MEDILAB, Teaching Laboratory of the Paracelsus Medical University, Salzburg, Austria (M. Hell, E. Mustafa-Korninger, A. Wojna); Centre for Public Health, Medical University Vienna, Vienna (A. Chakeri); MB-LAB Clinical Microbiology Laboratory, Innsbruck, Austria (J. Möst); Consultant Laboratory for Bordetella of the Robert Koch Institute, Medical University of Graz, Graz, Austria (E. Leitner); Centre for Microbiology and Environmental Systems Science, University of Vienna, Vienna (P. Hyden, T. Rattei); Children’s Health Ireland at Crumlin, Dublin, Ireland (A. Habington); Institute of Specific Prophylaxis and Tropical Medicine, Medical University of Vienna, Vienna (U. Wiedermann)

Main Article

Table 2

Genetic profiles of the 123 Bordetella pertussis isolates obtained through the B. pertussis isolate–based surveillance system, Austria, May 2018–May 2020*

Profile No. (%) B. pertussis vaccine antigen genes
Reference
ptxS1 ptxP prn fim2 fim3
Profile vaccine strain Tohama I 0 ptxS1-D ptxP-1 prn-1 fim2-1 fim3-1 NA
Profile A 64 (52.3) ptxS1-A ptxP-3 prn-2 fim2-1 fim3-1 (13,14)
Profile B 23 (18.7) ptxS1-A ptxP-3 prn-2–631^632STOP:T>- fim2-1 fim3-1 (15)
Profile C 20 (16.2) ptxS1-A ptxP-3 prn-2 fim2-1 fim3-2 (13,14)
Profile D 8 (6.50) ptxS1-A ptxP-3 prn-2–303+1326DEL fim2-1 fim3-1 (16)
Profile E 3† (2.44) ptxS1-A ptxP-3 prn-2-IS481–1613rev fim2-1 fim3-2 (13,14)
Profile F 2 (1.62) ptxS1-A ptxP-3 prn-2-IS481–1613rev fim2-1 fim3-1 (14)
Profile G 1 (0.8) ptxS1-A ptxP-3 prn-2- DEL1742–1839‡ fim2-1 fim3-2 This study
Profile H 1 (0.8) ptxS1-A ptxP-3 prn-2-STOP-T223C fim2-1 fim3-1 (14)
Profile I 1 (0.8) ptxS1-A ptxP-3 prn-2-C1273T fim2-1 fim3-1 (13,14)

*NA, not applicable.
†One isolate was sequence type 83.
‡This isolate showed an insertion longer than 200 bp in the prn gene combined with a partial deletion at positions nt 1742–1839.

Main Article

References
  1. Kilgore  PE, Salim  AM, Zervos  MJ, Schmitt  HJ. Pertussis: microbiology, disease, treatment, and prevention. Clin Microbiol Rev. 2016;29:449–86. DOIPubMedGoogle Scholar
  2. Paisley  RD, Blaylock  J, Hartzell  JD. Whooping cough in adults: an update on a reemerging infection. Am J Med. 2012;125:141–3. DOIPubMedGoogle Scholar
  3. Lee  AD, Cassiday  PK, Pawloski  LC, Tatti  KM, Martin  MD, Briere  EC, et al.; Clinical Validation Study Group. Clinical evaluation and validation of laboratory methods for the diagnosis of Bordetella pertussis infection: Culture, polymerase chain reaction (PCR) and anti-pertussis toxin IgG serology (IgG-PT). PLoS One. 2018;13:e0195979. DOIPubMedGoogle Scholar
  4. 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
  5. Wagner  B, Melzer  H, Freymüller  G, Stumvoll  S, Rendi-Wagner  P, Paulke-Korinek  M, et al. Genetic variation of Bordetella pertussis in Austria. PLoS One. 2015;10:e0132623. DOIPubMedGoogle Scholar
  6. Latasa  P, García-Comas  L, Gil de Miguel  A, Barranco  MD, Rodero  I, Sanz  JC, et al. Effectiveness of acellular pertussis vaccine and evolution of pertussis incidence in the community of Madrid from 1998 to 2015. Vaccine. 2018;36:1643–9. DOIPubMedGoogle Scholar
  7. Esposito  S, Stefanelli  P, Fry  NK, Fedele  G, He  Q, Paterson  P, et al.; World Association of Infectious Diseases and Immunological Disorders (WAidid) and the Vaccine Study Group of the European Society of Clinical Microbiology and Infectious Diseases (EVASG). (WAidid) and the Vaccine Study Group of the European Society of Clinical Microbiology and Infectious Diseases (EVASG). Pertussis prevention: reasons for resurgence, and differences in the current acellular pertussis vaccines. Front Immunol. 2019;10:1344. DOIPubMedGoogle Scholar
  8. Burdin  N, Handy  LK, Plotkin  SA. What is wrong with pertussis vaccine immunity? The problem of waning effectiveness of pertussis vaccines. Cold Spring Harb Perspect Biol. 2017;9:a029454. DOIPubMedGoogle Scholar
  9. Chiappini  E, Stival  A, Galli  L, de Martino  M. Pertussis re-emergence in the post-vaccination era. BMC Infect Dis. 2013;13:151. DOIPubMedGoogle Scholar
  10. Mooi  FR, van Oirschot  H, Heuvelman  K, van der Heide  HGJ, Gaastra  W, Willems  RJL. Polymorphism in the Bordetella pertussis virulence factors P.69/pertactin and pertussis toxin in The Netherlands: temporal trends and evidence for vaccine-driven evolution. Infect Immun. 1998;66:670–5. DOIPubMedGoogle Scholar
  11. Diavatopoulos  DA, Cummings  CA, Schouls  LM, Brinig  MM, Relman  DA, Mooi  FR. Bordetella pertussis, the causative agent of whooping cough, evolved from a distinct, human-associated lineage of B. bronchiseptica. PLoS Pathog. 2005;1:e45. DOIPubMedGoogle Scholar
  12. 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;24:988–94. DOIPubMedGoogle Scholar
  13. Bowden  KE, Weigand  MR, Peng  Y, Cassiday  PK, Sammons  S, Knipe  K, et al. Genome structural diversity among 31 Bordetella pertussis isolates from two recent U.S. whooping cough statewide epidemics. MSphere. 2016;1:e00036–16. DOIPubMedGoogle Scholar
  14. 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;199:199. DOIPubMedGoogle Scholar
  15. 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
  16. Sealey  KL, Harris  SR, Fry  NK, Hurst  LD, Gorringe  AR, Parkhill  J, et al. Genomic analysis of isolates from the United Kingdom 2012 pertussis outbreak reveals that vaccine antigen genes are unusually fast evolving. J Infect Dis. 2015;212:294–301. DOIPubMedGoogle Scholar
  17. Vestrheim  DF, Steinbakk  M, Bjørnstad  ML, Moghaddam  A, Reinton  N, Dahl  ML, et al. Recovery of Bordetella pertussis from PCR-positive nasopharyngeal samples is dependent on bacterial load. J Clin Microbiol. 2012;50:4114–5. DOIPubMedGoogle Scholar
  18. Martini  H, Rodeghiero  C, VAN DEN Poel  C, Vincent  M, Pierard  D, Huygen  K. Pertussis diagnosis in Belgium: results of the National Reference Centre for Bordetella anno 2015. Epidemiol Infect. 2017;145:2366–73. DOIPubMedGoogle Scholar
  19. Lam  C, Octavia  S, Bahrame  Z, Sintchenko  V, Gilbert  GL, Lan  R. Selection and emergence of pertussis toxin promoter ptxP3 allele in the evolution of Bordetella pertussis. Infect Genet Evol. 2012;12:492–5. DOIPubMedGoogle Scholar
  20. Bowden  KE, Williams  MM, Cassiday  PK, Milton  A, Pawloski  L, Harrison  M, et al. Molecular epidemiology of the pertussis epidemic in Washington State in 2012. J Clin Microbiol. 2014;52:3549–57. DOIPubMedGoogle Scholar
  21. 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
  22. 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:e01074–14. DOIPubMedGoogle Scholar
  23. Moriuchi  T, Vichit  O, Vutthikol  Y, Hossain  MS, Samnang  C, Toda  K, et al. Molecular epidemiology of Bordetella pertussis in Cambodia determined by direct genotyping of clinical specimens. Int J Infect Dis. 2017;62:56–8. DOIPubMedGoogle Scholar
  24. 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
  25. Breakwell  L, Kelso  P, Finley  C, Schoenfeld  S, Goode  B, Misegades  LK, et al. Pertussis vaccine effectiveness in the setting of pertactin-deficient pertussis. Pediatrics. 2016;137:e20153973. DOIPubMedGoogle Scholar
  26. Etskovitz  H, Anastasio  N, Green  E, May  M. Role of evolutionary selection scting on vaccine antigens in the re-emergence of Bordetella pertussis. Diseases. 2019;7:35. DOIPubMedGoogle Scholar
  27. 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
  28. 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
  29. Safarchi  A, Octavia  S, Luu  LD, 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
  30. Carvalho  CFA, Andrews  N, Dabrera  G, Ribeiro  S, Stowe  J, Ramsay  M, et al. National Outbreak of Pertussis in England, 2011–2012: a case-control study comparing 3-component and 5-component acellular vaccines with whole-cell pertussis vaccines. Clin Infect Dis. 2020;70:200–7. DOIPubMedGoogle Scholar
  31. van Twillert  I, Bonačić Marinović  AA, Kuipers  B, van Gaans-van den Brink  JAM, Sanders  EAM, van Els  CACM. Impact of age and vaccination history on long-term serological responses after symptomatic B. pertussis infection, a high dimensional data analysis. Sci Rep. 2017;7:40328. DOIPubMedGoogle Scholar
  32. Olin  P, Rasmussen  F, Gustafsson  L, Hallander  HO, Heijbel  H; Ad Hoc Group for the Study of Pertussis Vaccines. Randomised controlled trial of two-component, three-component, and five-component acellular pertussis vaccines compared with whole-cell pertussis vaccine. Lancet. 1997;350:1569–77. DOIPubMedGoogle Scholar
  33. 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
  34. 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
  35. 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
  36. 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
  37. Tsang  RS, Shuel  M, Jamieson  FB, Drews  S, Hoang  L, Horsman  G, et al. Pertactin-negative Bordetella pertussis strains in Canada: characterization of a dozen isolates based on a survey of 224 samples collected in different parts of the country over the last 20 years. Int J Infect Dis. 2014;28:65–9. DOIPubMedGoogle Scholar
  38. 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
  39. Uelze  L, Grützke  J, Borowiak  M, Hammerl  JA, Juraschek  K, Deneke  C, et al. Typing methods based on whole genome sequencing data. One Health Outlook. 2020;2:3. DOIGoogle Scholar
  40. Jolley  KA, Bray  JE, Maiden  MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res. 2018;3:124. DOIPubMedGoogle Scholar

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Page updated: February 21, 2021
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