1887
Research article Open Access
Like 0

Abstract

Introduction

In 2012 a large epidemic of pertussis occurred in the Netherlands. We assessed pertussis toxin (PT) antibody levels in longitudinal serum samples from Dutch 10–18 year-olds, encompassing the epidemic, to investigate pertussis infection incidence. : Blood was sampled in October 2011 (n = 239 adolescents), then 1 year (2012; n = 228) and 3 years (2014; n = 167) later. PT-IgG concentrations were measured by immunoassay and concentrations ≥50 IU/mL (seropositive) assumed indicative of an infection within the preceding year. : During the 2012 epidemic, 10% of participants became seropositive, while this was just 3% after the epidemic. The pertussis acquisition rate proved to be sixfold higher during the epidemic (97 per 1,000 person-years) compared with 2012–2014 (16 per 1,000 person-years). In 2012, pertussis notifications among adolescents nationwide were 228/100,000 (0.23%), which is at least 40 times lower than the seropositivity percentage. Remarkably, 17 of the 22 seropositive participants in 2011, were still seropositive in 2012 and nine remained seropositive for at least 3 years. : Longitudinal studies allow a better estimation of pertussis infections in the population. A PT-IgG concentration ≥50 IU/mL as indication of recent infection may overestimate these numbers in cross-sectional serosurveillance and should be used carefully.

Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2017.22.47.17-00011
2017-11-23
2024-11-23
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2017.22.47.17-00011
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/22/47/eurosurv-22-47-2.html?itemId=/content/10.2807/1560-7917.ES.2017.22.47.17-00011&mimeType=html&fmt=ahah

References

  1. Cherry JD, Paddock CD. Pathogenesis and histopathology of pertussis: implications for immunization. Expert Rev Vaccines. 2014;13(9):1115-23.  https://doi.org/10.1586/14760584.2014.935766  PMID: 24992986 
  2. Mattoo S, Cherry JD. Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies. Clin Microbiol Rev. 2005;18(2):326-82.  https://doi.org/10.1128/CMR.18.2.326-382.2005  PMID: 15831828 
  3. Roehr B. Whooping cough outbreak hits several US states. BMJ. 2010;341(aug24 2):c4627.  https://doi.org/10.1136/bmj.c4627  PMID: 20736256 
  4. Carcione D, Regan AK, Tracey L, Mak DB, Gibbs R, Dowse GK, et al. The impact of parental postpartum pertussis vaccination on infection in infants: A population-based study of cocooning in Western Australia. Vaccine. 2015;33(42):5654-61.  https://doi.org/10.1016/j.vaccine.2015.08.066  PMID: 26320420 
  5. Elomaa A, He Q, Minh NN, Mertsola J. Pertussis before and after the introduction of acellular pertussis vaccines in Finland. Vaccine. 2009;27(40):5443-9.  https://doi.org/10.1016/j.vaccine.2009.07.010  PMID: 19628060 
  6. Amirthalingam G, Andrews N, Campbell H, Ribeiro S, Kara E, Donegan K, et al. Effectiveness of maternal pertussis vaccination in England: an observational study. Lancet. 2014;384(9953):1521-8.  https://doi.org/10.1016/S0140-6736(14)60686-3  PMID: 25037990 
  7. de Greeff SC, Mooi FR, Schellekens JF, de Melker HE. Impact of acellular pertussis preschool booster vaccination on disease burden of pertussis in The Netherlands. Pediatr Infect Dis J. 2008;27(3):218-23.  https://doi.org/10.1097/INF.0b013e318161a2b9  PMID: 18277916 
  8. Carbonetti NH. Pertussis toxin and adenylate cyclase toxin: key virulence factors of Bordetella pertussis and cell biology tools. Future Microbiol. 2010;5(3):455-69.  https://doi.org/10.2217/fmb.09.133  PMID: 20210554 
  9. Quinn HE, McIntyre PB, Backhouse JL, Gidding HF, Brotherton J, Gilbert GL. The utility of seroepidemiology for tracking trends in pertussis infection. Epidemiol Infect. 2010;138(3):426-33.  https://doi.org/10.1017/S0950268809990707  PMID: 19719902 
  10. Pebody RG, Gay NJ, Giammanco A, Baron S, Schellekens J, Tischer A, et al. The seroepidemiology of Bordetella pertussis infection in Western Europe. Epidemiol Infect. 2005;133(1):159-71.  https://doi.org/10.1017/S0950268804003012  PMID: 15724723 
  11. Barkoff AM, Gröndahl-Yli-Hannuksela K, He Q. Seroprevalence studies of pertussis: what have we learned from different immunized populations. Pathog Dis. 2015;73(7):ftv050.  https://doi.org/10.1093/femspd/ftv050  PMID: 26208655 
  12. de Greeff SC, de Melker HE, van Gageldonk PG, Schellekens JF, van der Klis FR, Mollema L, et al. Seroprevalence of pertussis in The Netherlands: evidence for increased circulation of Bordetella pertussis. PLoS One. 2010;5(12):e14183.  https://doi.org/10.1371/journal.pone.0014183  PMID: 21152071 
  13. van der Maas NA, Mooi FR, de Greeff SC, Berbers GA, Spaendonck MA, de Melker HE. Pertussis in the Netherlands, is the current vaccination strategy sufficient to reduce disease burden in young infants? Vaccine. 2013;31(41):4541-7.  https://doi.org/10.1016/j.vaccine.2013.07.060  PMID: 23933365 
  14. Stoof SP, van der Klis FR, van Rooijen DM, Knol MJ, Sanders EA, Berbers GA. Timing of an adolescent booster after single primary meningococcal serogroup C conjugate immunization at young age; an intervention study among Dutch teenagers. PLoS One. 2014;9(6):e100651.  https://doi.org/10.1371/journal.pone.0100651  PMID: 24963638 
  15. van Ravenhorst MB, Marinovic AB, van der Klis FR, van Rooijen DM, van Maurik M, Stoof SP, et al. Long-term persistence of protective antibodies in Dutch adolescents following a meningococcal serogroup C tetanus booster vaccination. Vaccine. 2016;34(50):6309-15.  https://doi.org/10.1016/j.vaccine.2016.10.049  PMID: 27817957 
  16. van Gageldonk PG, van Schaijk FG, van der Klis FR, Berbers GA. Development and validation of a multiplex immunoassay for the simultaneous determination of serum antibodies to Bordetella pertussis, diphtheria and tetanus. J Immunol Methods. 2008;335(1-2):79-89.  https://doi.org/10.1016/j.jim.2008.02.018  PMID: 18407287 
  17. National Institute for Biological Standards and Control (NIBSC). Pertussis Antiserum(human)1st IS-WHO international Standard. Potters Bar: NIBSC. [Accessed 21 Nov 2017]. Available from: http://www.nibsc.org/products/brm_product_catalogue/detail_page.aspx?catid=06/140
  18. de Melker HE, Versteegh FG, Conyn-Van Spaendonck MA, Elvers LH, Berbers GA, van Der Zee A, et al. Specificity and sensitivity of high levels of immunoglobulin G antibodies against pertussis toxin in a single serum sample for diagnosis of infection with Bordetella pertussis. J Clin Microbiol. 2000;38(2):800-6. PMID: 10655388 
  19. Guiso N, Berbers G, Fry NK, He Q, Riffelmann M, Wirsing von König CHEU Pertstrain group. What to do and what not to do in serological diagnosis of pertussis: recommendations from EU reference laboratories. Eur J Clin Microbiol Infect Dis. 2011;30(3):307-12.  https://doi.org/10.1007/s10096-010-1104-y  PMID: 21069406 
  20. Jeppesen CA, Snape MD, Robinson H, Gossger N, John TM, Voysey M, et al. Meningococcal carriage in adolescents in the United Kingdom to inform timing of an adolescent vaccination strategy. J Infect. 2015;71(1):43-52.  https://doi.org/10.1016/j.jinf.2015.02.006  PMID: 25709085 
  21. Campbell P, McIntyre P, Quinn H, Hueston L, Gilbert GL, McVernon J. Increased population prevalence of low pertussis toxin antibody levels in young children preceding a record pertussis epidemic in Australia. PLoS One. 2012;7(4):e35874.  https://doi.org/10.1371/journal.pone.0035874  PMID: 22558249 
  22. Caboré RN, Piérard D, Huygen K. A Belgian Serosurveillance/Seroprevalence Study of Diphtheria, Tetanus and Pertussis Using a Luminex xMAP Technology-Based Pentaplex. Vaccines (Basel). 2016;4(2):16.  https://doi.org/10.3390/vaccines4020016  PMID: 27171114 
  23. Aase A, Herstad TK, Merino S, Brandsdal KT, Berdal BP, Aleksandersen EM, et al. Opsonophagocytic activity and other serological indications of Bordetella pertussis infection in military recruits in Norway. Clin Vaccine Immunol. 2007;14(7):855-62.  https://doi.org/10.1128/CVI.00081-07  PMID: 17507542 
  24. Warfel JM, Beren J, Merkel TJ. Airborne transmission of Bordetella pertussis. J Infect Dis. 2012;206(6):902-6.  https://doi.org/10.1093/infdis/jis443  PMID: 22807521 
  25. Mossong J, Hens N, Jit M, Beutels P, Auranen K, Mikolajczyk R, et al. Social contacts and mixing patterns relevant to the spread of infectious diseases. PLoS Med. 2008;5(3):e74.  https://doi.org/10.1371/journal.pmed.0050074  PMID: 18366252 
  26. Berbers GA, van de Wetering MS, van Gageldonk PG, Schellekens JF, Versteegh FG, Teunis PF. A novel method for evaluating natural and vaccine induced serological responses to Bordetella pertussis antigens. Vaccine. 2013;31(36):3732-8.  https://doi.org/10.1016/j.vaccine.2013.05.073  PMID: 23742995 
  27. Ward JI, Cherry JD, Chang SJ, Partridge S, Keitel W, Edwards K, et al. APERT Study Group. Bordetella Pertussis infections in vaccinated and unvaccinated adolescents and adults, as assessed in a national prospective randomized Acellular Pertussis Vaccine Trial (APERT). Clin Infect Dis. 2006;43(2):151-7.  https://doi.org/10.1086/504803  PMID: 16779740 
  28. Hendrikx LH, Felderhof MK, Oztürk K, de Rond LG, van Houten MA, Sanders EA, et al. Enhanced memory B-cell immune responses after a second acellular pertussis booster vaccination in children 9 years of age. Vaccine. 2011;30(1):51-8.  https://doi.org/10.1016/j.vaccine.2011.10.048  PMID: 22064265 
  29. Le T, Cherry JD, Chang SJ, Knoll MD, Lee ML, Barenkamp S, et al. APERT Study. Immune responses and antibody decay after immunization of adolescents and adults with an acellular pertussis vaccine: the APERT Study. J Infect Dis. 2004;190(3):535-44.  https://doi.org/10.1086/422035  PMID: 15243929 
  30. Klein NP, Bartlett J, Fireman B, Baxter R. Waning Tdap Effectiveness in Adolescents. Pediatrics. 2016;137(3):e20153326.  https://doi.org/10.1542/peds.2015-3326  PMID: 26908667 
  31. Witt MA, Katz PH, Witt DJ. Unexpectedly limited durability of immunity following acellular pertussis vaccination in preadolescents in a North American outbreak. Clin Infect Dis. 2012;54(12):1730-5.  https://doi.org/10.1093/cid/cis287  PMID: 22423127 
  32. de Greeff SC, Mooi FR, Westerhof A, Verbakel JM, Peeters MF, Heuvelman CJ, et al. Pertussis disease burden in the household: how to protect young infants. Clin Infect Dis. 2010;50(10):1339-45.  https://doi.org/10.1086/652281  PMID: 20370464 
  33. Clark TA, Bobo N. CDC update on pertussis surveillance and Tdap vaccine recommendations. NASN Sch Nurse. 2012;27(6):297-300.  https://doi.org/10.1177/1942602X12452443  PMID: 23193719 
  34. Zepp F, Heininger U, Mertsola J, Bernatowska E, Guiso N, Roord J, et al. Rationale for pertussis booster vaccination throughout life in Europe. Lancet Infect Dis. 2011;11(7):557-70.  https://doi.org/10.1016/S1473-3099(11)70007-X  PMID: 21600850 
  35. Warfel JM, Zimmerman LI, Merkel TJ. Acellular pertussis vaccines protect against disease but fail to prevent infection and transmission in a nonhuman primate model. Proc Natl Acad Sci USA. 2014;111(2):787-92.  https://doi.org/10.1073/pnas.1314688110  PMID: 24277828 
  36. Witt MA, Arias L, Katz PH, Truong ET, Witt DJ. Reduced risk of pertussis among persons ever vaccinated with whole cell pertussis vaccine compared to recipients of acellular pertussis vaccines in a large US cohort. Clin Infect Dis. 2013;56(9):1248-54.  https://doi.org/10.1093/cid/cit046  PMID: 23487373 
  37. Sheridan SL, Ware RS, Grimwood K, Lambert SB. Number and order of whole cell pertussis vaccines in infancy and disease protection. JAMA. 2012;308(5):454-6.  https://doi.org/10.1001/jama.2012.6364  PMID: 22851107 
  38. Klein NP, Bartlett J, Rowhani-Rahbar A, Fireman B, Baxter R. Waning protection after fifth dose of acellular pertussis vaccine in children. N Engl J Med. 2012;367(11):1012-9.  https://doi.org/10.1056/NEJMoa1200850  PMID: 22970945 
/content/10.2807/1560-7917.ES.2017.22.47.17-00011
Loading

Data & Media loading...

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error