Skip to main content

Advertisement

SpringerLink
Log in

Pertussis vaccines, epidemiology and evolution

  • Review Article
  • Published:

From Nature Reviews Microbiology

View current issue Sign up to alerts

Abstract

Pertussis, which is caused by Bordetella pertussis, has plagued humans for at least 800 years, is highly infectious and can be fatal in the unvaccinated, especially very young infants. Although the rollout of whole-cell pertussis (wP) vaccines in the 1940s and 1950s was associated with a drastic drop in incidence, concerns regarding the reactogenicity of wP vaccines led to the development of a new generation of safer, acellular (aP) vaccines that have been adopted mainly in high-income countries. Over the past 20 years, some countries that boast high aP coverage have experienced a resurgence in pertussis, which has led to substantial debate over the basic immunology, epidemiology and evolutionary biology of the bacterium. Controversy surrounds the duration of natural immunity and vaccine-derived immunity, the ability of vaccines to prevent transmission and severe disease, and the impact of evolution on evading vaccine immunity. Resolving these issues is made challenging by incomplete detection of pertussis cases, the absence of a serological marker of immunity, modest sequencing of the bacterial genome and heterogeneity in diagnostic methods of surveillance. In this Review, we lay out the complexities of contemporary pertussis and, where possible, propose a parsimonious explanation for apparently incongruous observations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1: Summary of pertussis vaccination policies and vaccine coverage worldwide.
Fig. 2: Global trends in the reported incidence of pertussis infections.
Fig. 3: Pertussis evolution and genome shuffling.
Fig. 4: Differential immune responses to natural Bordetella pertussis infection and immunization with whole-cell and acellular vaccines.

Similar content being viewed by others

Data availability

All data and R programming code for Figs. 1 and 2 and Supplementary Fig. 2 are freely available from Edmond, the Open Data Repository of the Max Planck Society.

References

  1. Parkhill, J. et al. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat. Genet. 35, 32–40 (2003). This research compares whole-genome sequences for congeneric Bordetella species to demonstrate B. parapertussis and B. pertussis are independently derived from B. bronchiseptica-like ancestors and have become host-restricted species. This host adaptation is argued to be a consequence of large-scale gene loss, genome reshuffling and inactivation.

    Article  PubMed  Google Scholar 

  2. Rohani, P. & Scarpino, S. Pertussis: Epidemiology, Immunology, and Evolution (Oxford Univ. Press, 2018).

  3. Gordon, J. E. & Hood, R. I. Whooping cough and its epidemiological anomalies. Am. J. Med. Sci. 222, 333–361 (1951).

    Article  CAS  PubMed  Google Scholar 

  4. Kendrick, P. L. Can whooping cough be eradicated? J. Infect. Dis. 132, 707–712 (1975).

    Article  CAS  PubMed  Google Scholar 

  5. Rohani, P., Earn, D. J. & Grenfell, B. T. Opposite patterns of synchrony in sympatric disease metapopulations. Science 286, 968–971 (1999).

    Article  CAS  PubMed  Google Scholar 

  6. Rohani, P. & Drake, J. M. The decline and resurgence of pertussis in the US. Epidemics 3, 183–188 (2011).

    Article  PubMed  Google Scholar 

  7. van Panhuis, W. G. et al. Contagious diseases in the United States from 1888 to the present. N. Engl. J. Med. 369, 2152–2158 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  8. Frenkel, L. D. The global burden of vaccine-preventable infectious diseases in children less than 5 years of age: implications for COVID-19 vaccination. How can we do better? Allergy Asthma Proc. 42, 378–385 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. WHO & UNICEF. Diphtheria Tetanus Toxoid and Pertussis (DTP) Vaccination Coverage. World Health Organization https://immunizationdata.who.int/global/wiise-detail-page/diphtheria-tetanus-toxoid-and-pertussis-(dtp)-vaccination-coverage (accessed 22 July 2022).

  10. WHO & UNICEF. Vaccination Schedule for Pertussis. World Health Organization https://immunizationdata.who.int/global/wiise-detail-page/vaccination-schedule-for-pertussis?ISO_3_CODE=&TARGETPOP_GENERAL= (accessed 22 July 2022).

  11. WHO & UNICEF. Pertussis Reported Cases and Incidence. World Health Organization https://immunizationdata.who.int/global/wiise-detail-page/pertussis-reported-cases-and-incidence (accessed 22 July 2022).

  12. Tessier, E. et al. Impact of the COVID-19 pandemic on Bordetella pertussis infections in England. BMC Public Health 22, 405 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Matczak, S. et al. Association between the COVID-19 pandemic and pertussis derived from multiple nationwide data sources, France, 2013 to 2020. Eurosurveillance https://doi.org/10.2807/1560-7917.es.2022.27.25.2100933 (2022).

  14. Bhatt, P., Strachan, J., Easton, M., Franklin, L. & Drewett, G. Effect of COVID-19 restrictions and border closures on vaccine preventable diseases in Victoria, Australia, 2020-2021. Commun. Dis. Intell. https://doi.org/10.33321/cdi.2022.46.29 (2022).

  15. Shet, A. et al. Impact of the SARS-CoV-2 pandemic on routine immunisation services: evidence of disruption and recovery from 170 countries and territories. Lancet Glob. Health 10, e186–e194 (2022).

    Article  CAS  PubMed  Google Scholar 

  16. Andersen, E. K. et al. Serological studies on H. pertussis, H. para-pertussis and H. bronchisepticus. Acta Pathol. Microbiol. Scand. 33, 202–224 (1953).

    Article  CAS  PubMed  Google Scholar 

  17. Aftandelians, R. V. & Connor, J. D. Bordetella pertussis serotypes in a whooping cough outbreak. Am. J. Epidemiol. 99, 343–346 (1974).

    Article  CAS  PubMed  Google Scholar 

  18. Stanbridge, T. N. & Preston, N. W. Variation of serotype in strains of Bordetella pertussis. J. Hyg. 73, 305–310 (1974).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Bronne-Shanbury, C. J. & Dolby, J. M. The stability of the serotypes of Bordetella pertussis with particular reference to serotype 1,2,3,4. J. Hyg. 76, 277–286 (1976).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Preston, N. W. Effectiveness of pertussis vaccines. Br. Med. J. 2, 11–13 (1965).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Bronne-Shanbury, C. J., Miller, D. & Standfast, A. F. B. The serotypes of Bordetella pertussis isolated in Great Britain between 1941 and 1968 and a comparison with the serotypes observed in other countries over this period. Epidemiol. Infect. 76, 265–275 (1976).

    CAS  Google Scholar 

  22. Preston, N. W. Prevalent serotypes of Bordetella pertussis in non-vaccinated communities. J. Hyg. 77, 85–91 (1976).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Schouls, L. M., van der Heide, H. G. J., Vauterin, L., Vauterin, P. & Mooi, F. R. Multiple-locus variable-number tandem repeat analysis of Dutch Bordetella pertussis strains reveals rapid genetic changes with clonal expansion during the late 1990s. J. Bacteriol. 186, 5496–5505 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Schmidtke, A. J. et al. Population diversity among Bordetella pertussis isolates, United States, 1935-2009. Emerg. Infect. Dis. 18, 1248–1255 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  25. Barkoff, A.-M. et al. Surveillance of circulating Bordetella pertussis strains in Europe during 1998 to 2015. J. Clin. Microbiol. 56, e01998-17 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  26. Barkoff, A.-M. et al. Pertactin-deficient Bordetella pertussis isolates: evidence of increased circulation in Europe, 1998 to 2015. Eur. Surveill. 24, 1700832 (2019).

    Article  Google Scholar 

  27. Weigand, M. R. et al. The history of Bordetella pertussis genome evolution includes structural rearrangement. J. Bacteriol. 199, e00806-16 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  28. Lefrancq, N. et al. Global spatial dynamics and vaccine-induced fitness changes of Bordetella pertussis. Sci. Transl. Med. 14, eabn3253 (2022).

    Article  CAS  PubMed  Google Scholar 

  29. Safarchi, A. et al. Pertactin negative Bordetella pertussis demonstrates higher fitness under vaccine selection pressure in a mixed infection model. Vaccine 33, 6277–6281 (2015).

    Article  CAS  PubMed  Google Scholar 

  30. Lesne, E. et al. Acellular pertussis vaccines induce anti-pertactin bactericidal antibodies which drives the emergence of pertactin-negative strains. Front. Microbiol. 11, 2108 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  31. Breakwell, L. et al. Pertussis vaccine effectiveness in the setting of pertactin-deficient pertussis. Pediatrics 137, e20153973 (2016).

    Article  PubMed  Google Scholar 

  32. Weigand, M. R. et al. Conserved patterns of symmetric inversion in the genome evolution of Bordetella respiratory pathogens. mSystems 4, e00702-19 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  33. Hanage, W. P. Not so simple after all: bacteria, their population genetics, and recombination. Cold Spring Harb. Perspect. Biol. 8, a018069 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  34. Weigand, M. R. et al. Genomic survey of Bordetella pertussis diversity, United States, 2000-2013. Emerg. Infect. Dis. 25, 780–783 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Ma, L., Caulfield, A., Dewan, K. K. & Harvill, E. T. Pertactin-deficient Bordetella pertussis, vaccine-driven evolution, and reemergence of pertussis. Emerg. Infect. Dis. 27, 1561–1566 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Szwejser-Zawislak, E. et al. Evaluation of whole-cell and acellular pertussis vaccines in the context of long-term herd immunity. Vaccines 11, 1 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Sealey, K. L., Belcher, T. & Preston, A. Bordetella pertussis epidemiology and evolution in the light of pertussis resurgence. Infect. Genet. Evol. 40, 136–143 (2016).

    Article  PubMed  Google Scholar 

  39. Mooi, F. R. et al. Bordetella pertussis strains with increased toxin production associated with pertussis resurgence. Emerg. Infect. Dis. 15, 1206–1213 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Pittet, L. F., Emonet, S., Schrenzel, J., Siegrist, C.-A. & Posfay-Barbe, K. M. Bordetella holmesii: an under-recognised Bordetella species. Lancet Infect. Dis. 14, 510–519 (2014). This paper provides a comprehensive review of B. holmesii, exploring its history, microbiology, epidemiology, diagnosis, clinical manifestation, treatment and unknowns.

    Article  CAS  PubMed  Google Scholar 

  41. Njamkepo, E. et al. Significant finding of Bordetella holmesii DNA in nasopharyngeal samples from French patients with suspected pertussis. J. Clin. Microbiol. 49, 4347–4348 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Rodgers, L. et al. Epidemiologic and laboratory features of a large outbreak of pertussis-like illnesses associated with cocirculating Bordetella holmesii and Bordetella pertussis — Ohio, 2010–2011. Clin. Infect. Dis. 56, 322–331 (2013).

    Article  PubMed  Google Scholar 

  43. Valero-Rello, A. et al. Validation and implementation of a diagnostic algorithm for DNA detection of Bordetella pertussis, B. parapertussis, and B. holmesii in a pediatric referral hospital in Barcelona, Spain. J. Clin. Microbiol. 57, e01231–18 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. David, S., van Furth, R. & Mooi, F. R. Efficacies of whole cell and acellular pertussis vaccines against Bordetella parapertussis in a mouse model. Vaccine 22, 1892–1898 (2004).

    Article  CAS  PubMed  Google Scholar 

  45. Long, G. H., Karanikas, A. T., Harvill, E. T., Read, A. F. & Hudson, P. J. Acellular pertussis vaccination facilitates Bordetella parapertussis infection in a rodent model of bordetellosis. Proc. Biol. Sci. 277, 2017–2025 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Mooi, F. R. et al. Characterization of Bordetella holmesii isolates from patients with pertussis-like illness in The Netherlands. FEMS Immunol. Med. Microbiol. 64, 289–291 (2012).

    Article  CAS  PubMed  Google Scholar 

  47. European Centre for Disease Prevention and Control. Laboratory diagnosis and molecular surveillance of Bordetella pertussis. ECDC https://www.ecdc.europa.eu/en/publications-data/bordetella-pertussis-laboratory-diagnosis-and-molecular-surveillance (2022).

  48. van der Zee, A., Schellekens, J. F. P. & Mooi, F. R. Laboratory diagnosis of pertussis. Clin. Microbiol. Rev. 28, 1005–1026 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Barkoff, A.-M., Gröndahl-Yli-Hannuksela, K. & He, Q. Seroprevalence studies of pertussis: what have we learned from different immunized populations. Pathog. Dis. 73, ftv050 (2015).

    Article  PubMed  Google Scholar 

  50. de Melker, H. E., Versteegh, F. G. A., Schellekens, J. F. P., Teunis, P. F. M. & Kretzschmar, M. The incidence of Bordetella pertussis infections estimated in the population from a combination of serological surveys. J. Infect. 53, 106–113 (2006).

    Article  PubMed  Google Scholar 

  51. von König, C. H. W., Halperin, S., Riffelmann, M. & Guiso, N. Pertussis of adults and infants. Lancet Infect. Dis. 2, 744–750 (2002).

    Article  Google Scholar 

  52. Domenech de Cellès, M., Magpantay, F. M. G., King, A. A. & Rohani, P. The pertussis enigma: reconciling epidemiology, immunology and evolution. Proc. Biol. Sci. 283, 20152309 (2016).

    PubMed  PubMed Central  Google Scholar 

  53. Cutts, F. T. & Hanson, M. Seroepidemiology: an underused tool for designing and monitoring vaccination programmes in low‐ and middle‐income countries. Trop. Med. Int. Health 21, 1086–1098 (2016).

    Article  PubMed  Google Scholar 

  54. Kapil, P. & Merkel, T. J. Pertussis vaccines and protective immunity. Curr. Opin. Immunol. 59, 72–78 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. WHO Pertussis vaccines: WHO position paper, August 2015 — recommendations. Vaccine 34, 1423–1425 (2016).

    Article  Google Scholar 

  56. Teunis, P. F. M., van Eijkeren, J. C. H., de Graaf, W. F., Marinović, A. B. & Kretzschmar, M. E. E. Linking the seroresponse to infection to within-host heterogeneity in antibody production. Epidemics 16, 33–39 (2016).

    Article  CAS  PubMed  Google Scholar 

  57. ECDC seroincidence R package v.2.0.0. European Centre for Disease Prevention and Control https://ecdc.europa.eu/en/publications-data/seroincidence-calculator-tool (2018).

  58. Crowcroft, N. & Miller, E. in Pertussis: Epidemiology, Immunology, Evolution Ch. 4 (eds Rohani, P. & Scarpino, S.) 66–86 (Oxford Univ. Press, 2019).

  59. Storsaeter, J., Hallander, H. O., Gustafsson, L. & Olin, P. Low levels of antipertussis antibodies plus lack of history of pertussis correlate with susceptibility after household exposure to Bordetella pertussis. Vaccine 21, 3542–3549 (2003).

    Article  PubMed  Google Scholar 

  60. Fine, P. E. M. Adult pertussis: a salesman’s dream — and an epidemiologist’s nightmare. Biologicals 25, 195–198 (1997).

    Article  CAS  PubMed  Google Scholar 

  61. Pertussis: adults, infants, and herds. Lancet 339, 526–527 (1992).

  62. Guiso, N. et al. What to do and what not to do in serological diagnosis of pertussis: recommendations from EU reference laboratories. Eur. J. Clin. Microbiol. Infect. Dis. 30, 307–312 (2011).

    Article  CAS  PubMed  Google Scholar 

  63. European Centre for Disease Prevention and Control. Guidance and protocol for the serological diagnosis of human infection with Bordetella pertussis. ECDC https://www.ecdc.europa.eu/en/publications-data/guidance-and-protocol-serological-diagnosis-human-infection-bordetella-pertussis (2012).

  64. Liu, B. C. et al. Effectiveness of acellular pertussis vaccine in older adults: nested matched case-control study. Clin. Infect. Dis. 71, 340–350 (2020). This case–control study of Tdap effectiveness in adults aged ≥45 years in New South Wales, Australia, has found a marked difference in vaccine effectiveness estimates between cases confirmed by PCR only and by serology only, suggesting the unreliability of the latter.

    Article  CAS  PubMed  Google Scholar 

  65. Graaf et al. Controlled human infection with Bordetella pertussis induces asymptomatic, immunizing colonization. Clin. Infect. Dis. 71, 403–411 (2020). This controlled human infection study for pertussis demonstrates that infection requires high inoculum dose, leading to an asymptomatic infection with no evidence of bacterial shedding.

    Article  PubMed  Google Scholar 

  66. Schellekens, J., von König, C.-H. W. & Gardner, P. Pertussis sources of infection and routes of transmission in the vaccination era. Pediatr. Infect. Dis. J. 24, S19–S24 (2005).

    Article  PubMed  Google Scholar 

  67. Tan, T. Summary: epidemiology of pertussis. Pediatr. Infect. Dis. J. 24, S35–S38 (2005).

    Article  PubMed  Google Scholar 

  68. Gill, C. J. et al. Asymptomatic Bordetella pertussis infections in a longitudinal cohort of young African infants and their mothers. eLife 10, e65663 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Mina, M. J. et al. A global immunological observatory to meet a time of pandemics. eLife 9, e58989 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  70. Halloran, M. E., Longini, I. M., Jr & Struchiner, C. J. Design and Analysis of Vaccine Studies (Springer, 2012).

  71. Préziosi, M.-P. & Halloran, M. E. Effects of pertussis vaccination on transmission: vaccine efficacy for infectiousness. Vaccine 21, 1853–1861 (2003).

    Article  PubMed  Google Scholar 

  72. Ionides, E. L., Nguyen, D., Atchadé, Y., Stoev, S. & King, A. A. Inference for dynamic and latent variable models via iterated, perturbed Bayes maps. Proc. Natl Acad. Sci. USA 112, 719–724 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. King, A. A., Nguyen, D. & Ionides, E. L. Statistical inference for partially observed Markov processes via the R package pomp. J. Stat. Softw. 69, 1–43 (2016).

    Article  Google Scholar 

  74. Sutter, R. W. & Cochi, S. L. Pertussis hospitalizations and mortality in the United States, 1985–1988. Evaluation of the completeness of national reporting. JAMA 267, 386–391 (1992).

    Article  CAS  PubMed  Google Scholar 

  75. Somerville, R. L. et al. Infants hospitalised with pertussis: estimating the true disease burden. J. Paediatr. Child Health 43, 617–622 (2007).

    Article  PubMed  Google Scholar 

  76. Gunning, C. E., Erhardt, E. & Wearing, H. J. Conserved patterns of incomplete reporting in pre-vaccine era childhood diseases. Proc. Biol. Sci. 281, 20140886 (2014).

    PubMed  PubMed Central  Google Scholar 

  77. Blackwood, J. C., Cummings, D. A. T., Broutin, H., Iamsirithaworn, S. & Rohani, P. Deciphering the impacts of vaccination and immunity on pertussis epidemiology in Thailand. Proc. Natl Acad. Sci. USA 110, 9595–9600 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Rohani, P., Zhong, X. & King, A. A. Contact network structure explains the changing epidemiology of pertussis. Science 330, 982–985 (2010).

    Article  CAS  PubMed  Google Scholar 

  79. Wearing, H. J. & Rohani, P. Estimating the duration of pertussis immunity using epidemiological signatures. PLoS Pathog. 5, e1000647 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  80. Gambhir, M. et al. A change in vaccine efficacy and duration of protection explains recent rises in pertussis incidence in the United States. PLoS Comput. Biol. 11, e1004138 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  81. Domenech de Cellès, M., Magpantay, F. M. G., King, A. A. & Rohani, P. The impact of past vaccination coverage and immunity on pertussis resurgence. Sci. Transl. Med. 10, eaau9627 (2018). Combining an age-structured model of pertussis transmission with novel statistical inference techniques to estimate the properties of pertussis vaccines from incidence data, this study shows that pertussis resurgence in Massachusetts, USA, was the predictable consequence of incomplete historical coverage with imperfect vaccines that confer slowly waning immunity — that is, an ‘end-of-honeymoon’ effect.

    Article  PubMed  Google Scholar 

  82. Kretzschmar, M., Teunis, P. F. M. & Pebody, R. G. Incidence and reproduction numbers of pertussis: estimates from serological and social contact data in five European countries. PLoS Med. 7, e1000291 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  83. McDonald, S. A. et al. An evidence synthesis approach to estimating the incidence of symptomatic pertussis infection in the Netherlands, 2005–2011. BMC Infect. Dis. 15, 588 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  84. Smallridge, W. E., Rolin, O. Y., Jacobs, N. T. & Harvill, E. T. Different effects of whole-cell and acellular vaccines on Bordetella transmission. J. Infect. Dis. 209, 1981–1988 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Warfel, J. M., Zimmerman, L. I. & Merkel, T. J. Acellular pertussis vaccines protect against disease but fail to prevent infection and transmission in a nonhuman primate model. Proc. Natl Acad. Sci. USA 111, 787–792 (2014). This paper provides a transformative baboon model of pertussis infection, teasing apart the differences in immune response elicited by whole-cell and acellular vaccines and determining their consequences for disease and transmission.

    Article  CAS  PubMed  Google Scholar 

  86. Domenech de Cellès, M., Riolo, M. A., Magpantay, F. M. G., Rohani, P. & King, A. A. Epidemiological evidence for herd immunity induced by acellular pertussis vaccines. Proc. Natl Acad. Sci. USA 111, E716–E717 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  87. Cravitz, L. & Williams, J. W. A comparative study of the ‘immune response’ to various pertussis antigens and the disease. J. Pediatr. 28, 172–186 (1946).

    Article  CAS  PubMed  Google Scholar 

  88. Abbott, J. D., Preston, N. W. & Mackay, R. I. Agglutinin response to pertussis vaccination in the child. Br. Med. J. 1, 86–88 (1971).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Fine, P. E. & Clarkson, J. A. Distribution of immunity to pertussis in the population of England and Wales. J. Hyg. 92, 21–36 (1984).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Vaccination against whooping-cough; relation between protection in children and results of laboratory tests; a report to the Whooping-cough Immunization Committee of the Medical Research Council and to the medical officers of health for Cardiff, Leeds, Leyton, Manchester, Middlesex, Oxford, Poole, Tottenham, Walthamstow, and Wembley. Br. Med. J. 2, 454–462 (1956).

  91. Mills, K. H. Immunity to Bordetella pertussis. Microbes Infect. 3, 655–677 (2001).

    Article  CAS  PubMed  Google Scholar 

  92. Blanchard-Rohner, G. Novel approaches to reactivate pertussis immunity. Expert Rev. Vaccines 21, 1787–1797 (2022).

    Article  CAS  PubMed  Google Scholar 

  93. Wirsing von König, C. H., Postels-Multan, S., Schmitt, H. J. & Bock, H. L. Pertussis in adults: frequency of transmission after household exposure. Lancet 346, 1326–1329 (1995).

    Article  PubMed  Google Scholar 

  94. Jenkinson, D. Natural course of 500 consecutive cases of whooping cough: a general practice population study. Br. Med. J. 310, 299–302 (1995).

    Article  CAS  Google Scholar 

  95. Fine, P. E. & Clarkson, J. A. The recurrence of whooping cough: possible implications for assessment of vaccine efficacy. Lancet 1, 666–669 (1982).

    Article  CAS  PubMed  Google Scholar 

  96. Wendelboe, A. M., Van Rie, A., Salmaso, S. & Englund, J. A. Duration of immunity against pertussis after natural infection or vaccination. Pediatr. Infect. Dis. J. 24, S58–S61 (2005).

    Article  PubMed  Google Scholar 

  97. Fine, P. E. & Clarkson, J. A. Reflections on the efficacy of pertussis vaccines. Rev. Infect. Dis. 9, 866–883 (1987).

    Article  CAS  PubMed  Google Scholar 

  98. Rohani, P., Earn, D. J. & Grenfell, B. T. Impact of immunisation on pertussis transmission in England and Wales. Lancet 355, 285–286 (2000).

    Article  CAS  PubMed  Google Scholar 

  99. Platt, L., Thun, M. & Harriman, K. A population-based study of recurrent symptomatic Bordetella pertussis infections in children in California, 2010–2015. Clin. Infect. Dis. 65, 2099–2104 (2017).

    Article  PubMed  Google Scholar 

  100. Warfel, J. M. & Merkel, T. J. Bordetella pertussis infection induces a mucosal IL-17 response and long-lived Th17 and Th1 immune memory cells in nonhuman primates. Mucosal Immunol. 6, 787–796 (2013).

    Article  CAS  PubMed  Google Scholar 

  101. Althouse, B. M. & Scarpino, S. V. Asymptomatic transmission and the resurgence of Bordetella pertussis. BMC Med. 13, 146 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  102. Klein, N. P., Bartlett, J., Rowhani-Rahbar, A., Fireman, B. & Baxter, R. Waning protection after fifth dose of acellular pertussis vaccine in children. N. Engl. J. Med. 367, 1012–1019 (2012).

    Article  CAS  PubMed  Google Scholar 

  103. Wilk, M. M., Allen, A. C., Misiak, A., Borkner, L. & Mills, K. H. G. The immunology of Bordetella pertussis infection and vaccination. Pertussis https://doi.org/10.1093/oso/9780198811879.003.0003 (2018).

  104. Chit, A. et al. Acellular pertussis vaccines effectiveness over time: a systematic review, meta-analysis and modeling study. PLoS ONE 13, e0197970 (2018). This meta-analysis provides estimates of the rate of waning effectiveness of acellular pertussis vaccines and pointed out the interpretation errors in earlier US studies.

    Article  PubMed  PubMed Central  Google Scholar 

  105. Domenech de Cellès, M., Rohani, P. & King, A. A. Duration of immunity and effectiveness of diphtheria-tetanus-acellular pertussis vaccines in children. JAMA Pediatr. 173, 588–594 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  106. Rane, M. S., Rohani, P. & Halloran, M. E. Durability of protection after 5 doses of acellular pertussis vaccine among 5–9 year old children in King County, Washington. Vaccine 39, 6144–6150 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  107. Crowcroft, N. S. et al. A call for caution in use of pertussis vaccine effectiveness studies to estimate waning immunity: a Canadian Immunization Research Network study. Clin. Infect. Dis. 73, 83–90 (2021). This study demonstrates that the appropriate controls for estimating pertussis waning is via a frequency-matched design, rather than a test-negative design that leads to multiple confounding factors. It further demonstrates a substantially lower estimated waning when the appropriate controls are accounted for.

    Article  PubMed  Google Scholar 

  108. Choi, Y. H., Campbell, H., Amirthalingam, G., van Hoek, A. J. & Miller, E. Investigating the pertussis resurgence in England and Wales, and options for future control. BMC Med. 14, 121 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  109. Campbell, P. T., McCaw, J. M., McIntyre, P. & McVernon, J. Defining long-term drivers of pertussis resurgence, and optimal vaccine control strategies. Vaccine 33, 5794–5800 (2015).

    Article  CAS  PubMed  Google Scholar 

  110. Lavine, J. S. & Rohani, P. Resolving pertussis immunity and vaccine effectiveness using incidence time series. Expert Rev. Vaccines 11, 1319–1329 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Rohani, P. & Scarpino, S. V. in Pertussis: Epidemiology, Immunology, and Evolution (eds Rohani, P. & Scarpino, S.) 6–25 (Oxford Univ. Press, 2019).

  112. King, A. A., Domenech de Cellès, M., Magpantay, F. M. G. & Rohani, P. in Pertussis: Epidemiology, Immunology, and Evolution (eds Rohani, P. & Scarpino, S. V.) Ch. 14 (Oxford Univ. Press, 2018).

  113. Lavine, J. S., King, A. A., Andreasen, V. & Bjørnstad, O. N. Immune boosting explains regime-shifts in prevaccine-era pertussis dynamics. PLoS ONE 8, e72086 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Jackson, D. W. & Rohani, P. Perplexities of pertussis: recent global epidemiological trends and their potential causes. Epidemiol. Infect. 142, 672–684 (2014).

    Article  CAS  PubMed  Google Scholar 

  115. Broset, E. et al. BCG vaccination improves DTaP immune responses in mice and is associated with lower pertussis incidence in ecological epidemiological studies. EBioMedicine 65, 103254 (2021). This study illustrates that BCG vaccines can shift the immune response to aP vaccines towards TH1 and TH17, and it demonstrates that countries deploying both aP and BCG vaccines report an order of magnitude lower incidence of pertussis than countries with aP vaccines alone.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Gillard, J. et al. BCG-induced trained immunity enhances acellular pertussis vaccination responses in an explorative randomized clinical trial. NPJ Vaccines 7, 21 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Gillard, J. et al. Antiviral responses induced by Tdap-IPV vaccination are associated with persistent humoral immunity to Bordetella pertussis. Nat. Commun. 15, 2133 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Borkner, L., Curham, L. M., Wilk, M. M., Moran, B. & Mills, K. H. G. IL-17 mediates protective immunity against nasal infection with Bordetella pertussis by mobilizing neutrophils, especially Siglec-F+ neutrophils. Mucosal Immunol. 14, 1183–1202 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Dubois, V. et al. Suppression of mucosal Th17 memory responses by acellular pertussis vaccines enhances nasal Bordetella pertussis carriage. NPJ Vaccines 6, 6 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Wilk, M. M. et al. Immunization with whole cell but not acellular pertussis vaccines primes CD4 TRM cells that sustain protective immunity against nasal colonization with Bordetella pertussis. Emerg. Microbes Infect. 8, 169–185 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. McCarthy, K. N., Hone, S., McLoughlin, R. M. & Mills, K. H. G. IL-17 and IFN-γ-producing respiratory tissue resident memory CD4 T cells persist for decades in adults immunized as children with whole cell pertussis vaccines. J. Infect. Dis. https://doi.org/10.1093/infdis/jiae034 (2024).

    Article  PubMed  Google Scholar 

  122. Winter, K., Klein, N. P., Ackley, S. & Cherry, J. D. Comment on ‘The impact of past vaccination coverage and immunity on pertussis resurgence’. Sci. Transl. Med. 10, eaau0548 (2018).

    Article  CAS  PubMed  Google Scholar 

  123. Domenech de Cellès, M., King, A. A. & Rohani, P. Response to Comment on ‘The impact of past vaccination coverage and immunity on pertussis resurgence’. Sci. Transl. Med. 10, eaau9627 (2018).

    Article  PubMed  Google Scholar 

  124. Riolo, M. A., King, A. A. & Rohani, P. Can vaccine legacy explain the British pertussis resurgence? Vaccine 31, 5903–5908 (2013).

    Article  PubMed  Google Scholar 

  125. Riolo, M. A. & Rohani, P. Combating pertussis resurgence: one booster vaccination schedule does not fit all. Proc. Natl Acad. Sci. USA 112, E472–E477 (2015). This study combines an age-structured model of pertussis transmission with a genetic optimization algorithm to identify cost-effective booster vaccination strategies, showing that not only the overall effectiveness of vaccine boosters but also the mechanism of vaccine failure predict optimal strategies.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Ward, J. I. et al. Efficacy of an acellular pertussis vaccine among adolescents and adults. N. Engl. J. Med. 353, 1555–1563 (2005).

    Article  CAS  PubMed  Google Scholar 

  127. Koepke, R. et al. Estimating the effectiveness of tetanus-diphtheria-acellular pertussis vaccine (Tdap) for preventing pertussis: evidence of rapidly waning immunity and difference in effectiveness by Tdap brand. J. Infect. Dis. 210, 942–953 (2014).

    Article  CAS  PubMed  Google Scholar 

  128. Acosta, A. M. et al. Tdap vaccine effectiveness in adolescents during the 2012 Washington State pertussis epidemic. Pediatrics 135, 981–989 (2015).

    Article  PubMed  Google Scholar 

  129. Klein, N. P., Bartlett, J., Fireman, B. & Baxter, R. Waning Tdap effectiveness in adolescents. Pediatrics 137, e20153326 (2016).

    Article  PubMed  Google Scholar 

  130. van der Lee, S., Hendrikx, L. H., Sanders, E. A. M., Berbers, G. A. M. & Buisman, A.-M. Whole-cell or acellular pertussis primary immunizations in infancy determines adolescent cellular immune profiles. Front. Immunol. 9, 51 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  131. da Silva Antunes, R. et al. Th1/Th17 polarization persists following whole-cell pertussis vaccination despite repeated acellular boosters. J. Clin. Invest. 128, 3853–3865 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  132. da Silva Antunes, R. et al. A system-view of Bordetella pertussis booster vaccine responses in adults primed with whole-cell versus acellular vaccine in infancy. JCI Insight 6, e141023 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  133. Yeung, K. H. T., Duclos, P., Nelson, E. A. S. & Hutubessy, R. C. W. An update of the global burden of pertussis in children younger than 5 years: a modelling study. Lancet Infect. Dis. 17, 974–980 (2017).

    Article  PubMed  Google Scholar 

  134. Kandeil, W. et al. A systematic review of the burden of pertussis disease in infants and the effectiveness of maternal immunization against pertussis. Expert Rev. Vaccines 19, 621–638 (2020).

    Article  CAS  PubMed  Google Scholar 

  135. Voysey, M. et al. The influence of maternally derived antibody and infant age at vaccination on infant vaccine responses: an individual participant meta-analysis. JAMA Pediatr. 171, 637–646 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  136. Kretsinger, K. et al. Preventing tetanus, diphtheria, and pertussis among adults: use of tetanus toxoid, reduced diphtheria toxoid and acellular pertussis vaccine recommendations of the Advisory Committee on Immunization Practices (ACIP) and recommendation of ACIP, supported by the Healthcare Infection Control Practices Advisory Committee (HICPAC), for use of Tdap among health-care personnel. MMWR Recomm. Rep. 55, 1–37 (2006).

    PubMed  Google Scholar 

  137. Quinn, H. E. et al. Parental Tdap boosters and infant pertussis: a case-control study. Pediatrics 134, 713–720 (2014).

    Article  PubMed  Google Scholar 

  138. Carcione, D. et al. The impact of parental postpartum pertussis vaccination on infection in infants: a population-based study of cocooning in Western Australia. Vaccine 33, 5654–5661 (2015).

    Article  PubMed  Google Scholar 

  139. Healy, C. M., Rench, M. A., Wootton, S. H. & Castagnini, L. A. Evaluation of the impact of a pertussis cocooning program on infant pertussis infection. Pediatr. Infect. Dis. J. 34, 22–26 (2015).

    Article  PubMed  Google Scholar 

  140. Rowe, S. L. et al. Maternal vaccination and infant influenza and pertussis. Pediatrics 148, e2021051076 (2021).

    Article  PubMed  Google Scholar 

  141. Dabrera, G. et al. A case-control study to estimate the effectiveness of maternal pertussis vaccination in protecting newborn infants in England and Wales, 2012-2013. Clin. Infect. Dis. 60, 333–337 (2015).

    Article  CAS  PubMed  Google Scholar 

  142. Amirthalingam, G. et al. Sustained effectiveness of the maternal pertussis immunization program in England 3 years following introduction. Clin. Infect. Dis. 63, S236–S243 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  143. Baxter, R., Bartlett, J., Fireman, B., Lewis, E. & Klein, N. P. Effectiveness of vaccination during pregnancy to prevent infant pertussis. Pediatrics 139, e20164091 (2017).

    Article  PubMed  Google Scholar 

  144. Skoff, T. H. et al. Impact of the US maternal tetanus, diphtheria, and acellular pertussis vaccination program on preventing pertussis in infants <2 months of age: a case-control evaluation. Clin. Infect. Dis. 65, 1977–1983 (2017).

    Article  CAS  PubMed  Google Scholar 

  145. Abu-Raya, B. et al. Global perspectives on immunization during pregnancy and priorities for future research and development: an international consensus statement. Front. Immunol. 11, 1282 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Abu-Raya, B. et al. The effect of tetanus-diphtheria-acellular-pertussis immunization during pregnancy on infant antibody responses: individual-participant data meta-analysis. Front. Immunol. https://doi.org/10.3389/fimmu.2021.689394 (2021).

  147. Briga, M., Goult, E., Brett, T. S., Rohani, P. & Domenech de Cellès, M. Maternal pertussis immunization and the blunting of routine vaccine effectiveness: a meta-analysis and modeling study. Nat. Commun. 15, 921 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Mattoo, S. & Cherry, J. D. Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies. Clin. Microbiol. Rev. 18, 326–382 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Locht, C. & Mielcarek, N. Live attenuated vaccines against pertussis. Expert Rev. Vaccines 13, 1147–1158 (2014).

    Article  CAS  PubMed  Google Scholar 

  150. Keech, C. et al. Immunogenicity and safety of BPZE1, an intranasal live attenuated pertussis vaccine, versus tetanus-diphtheria-acellular pertussis vaccine: a randomised, double-blind, phase 2b trial. Lancet 401, 843–855 (2023).

    Article  CAS  PubMed  Google Scholar 

  151. Sugai, T. et al. A CpG-containing oligodeoxynucleotide as an efficient adjuvant counterbalancing the Th1/Th2 immune response in diphtheria–tetanus–pertussis vaccine. Vaccine 23, 5450–5456 (2005).

    Article  CAS  PubMed  Google Scholar 

  152. Allen, A. C. et al. Sustained protective immunity against Bordetella pertussis nasal colonization by intranasal immunization with a vaccine-adjuvant combination that induces IL-17-secreting TRM cells. Mucosal Immunol. 11, 1763–1776 (2018).

    Article  CAS  PubMed  Google Scholar 

  153. Preston, N. in Pathogenesis and Immunity in Pertussis (eds Wardlaw, A. C. & Parton, R.) 1–19 (Wiley, 1988).

  154. Lavine, J. S., Bjørnstad, O. N., de Blasio, B. F. & Storsaeter, J. Short-lived immunity against pertussis, age-specific routes of transmission, and the utility of a teenage booster vaccine. Vaccine 30, 544–551 (2012).

    Article  PubMed  Google Scholar 

  155. Gokhale, D. V., Brett, T. S., He, B., King, A. A. & Rohani, P. Disentangling the causes of mumps reemergence in the United States. Proc. Natl Acad. Sci. USA 120, e2207595120 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Infectious Disease Epidemiology Group, Max Planck Institute for Infection Biology, Berlin, Germany

    Matthieu Domenech de Cellès

  2. Odum School of Ecology, University of Georgia, Athens, GA, USA

    Pejman Rohani

  3. Center of Ecology of Infectious Diseases, Athens, GA, USA

    Pejman Rohani

  4. Department of Infectious Diseases, College for Veterinary Medicine, University of Georgia, Athens, GA, USA

    Pejman Rohani

Authors
  1. Matthieu Domenech de Cellès
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pejman Rohani
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

The authors contributed equally to all aspects of the article.

Corresponding author

Correspondence to Pejman Rohani.

Ethics declarations

Competing interests

P.R. received funding from Sanofi for a research project on pertussis vaccines. M.D.d.C. received post-doctoral funding (2017–2019) from Pfizer and consulting fees from GSK.

Peer review

Peer review information

Nature Reviews Microbiology thanks Camille Locht, Peter McIntyre, Peter Sebo and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Related links

Edmond, the Open Data Repository of the Max Planck Society: https://doi.org/10.17617/3.A1KMUB

World Bank country and lending groups: https://datahelpdesk.worldbank.org/knowledgebase/articles/906519

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Domenech de Cellès, M., Rohani, P. Pertussis vaccines, epidemiology and evolution. Nat Rev Microbiol (2024). https://doi.org/10.1038/s41579-024-01064-8

Download citation

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41579-024-01064-8

  • Springer Nature Limited

Search

Navigation