1887

Abstract

Incidence data on pertussis cases in Italy do not show pertussis resurgence as recently described in other European countries. The aim of this study was to determine the seroprevalence of IgG antibodies to pertussis toxin (PT-IgG) in selected adult age groups, who can serve as a reservoir of Bordetella pertussis and be responsible for onward transmission to vulnerable infants. The seroprevalence of PT-IgG was studied in sera collected in 2012–2013 in three age groups: 20–29 years and 30–39 years (reproductive age), and ≥60 years. These data were compared to those from sera collected in similar age groups in 1996–1997. More than 80 % of the adult population analysed in the 2012–2013 group presented detectable levels of PT-IgG (>5 IU ml). PT-IgG titres of 50–99 IU ml, considered indicative of infection in the last few years, and PT-IgG titres of  ≥100 IU ml, considered indicative of recent infection (i.e.within the last year), reached 9.1 % [95 % confidence interval (CI) 6.9–11.3‌  %; 58/639] and 5 % (95 % CI 3.3–6.7 %; 32/639) seroprevalence, respectively. Notably, the proportion of subjects with a seroprevalence indicative of recent infection increased significantly from 9.3 % (95 % CI 7.5–11.1 %; 96/1037) in 1996–1997 to 14.1 % (95 % CI 11.4–16.8 %; 90/639) in 2012–2013. Overall, our data clearly indicate a significant increase in the circulation of B. pertussis in adults in Italy; therefore, it is likely that the statutory notification system underestimates the real incidence of the disease. These findings have implications for preventive strategies.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000264
2016-07-01
2019-10-18
Loading full text...

Full text loading...

/deliver/fulltext/jmm/65/7/649.html?itemId=/content/journal/jmm/10.1099/jmm.0.000264&mimeType=html&fmt=ahah

References

  1. Ausiello C., Stefanelli M., Carollo M., Fazio C., Marella A. M., Iannazzo S., Pompa M..( 2014;). Pertosse in Italia: ricognizione dei laboratori di diagnosi del Servizio Sanitario Nazionale e valutazione delle tecniche utilizzate. . Rapporti ISTISAN 2014: 14/3 (http://www.iss.it/binary/publ/cont/14_3_web.pdf).
    [Google Scholar]
  2. Barkoff A. M., Gröndahl-Yli-Hannuksela K., He Q..( 2015;). Seroprevalence studies of pertussis: what have we learned from different immunized populations. . Pathog Dis 73: ftv050. [CrossRef] [PubMed]
    [Google Scholar]
  3. Binkin N. J., Salmaso S., Tozzi A. E., Scuderi G., Greco D., Greco D..( 1992;). Epidemiology of pertussis in a developed country with low vaccination coverage: the Italian experience. . Pediatr Infect Dis J 11: 653–661.[PubMed]
    [Google Scholar]
  4. Chiappini E., Stival A., Galli L., de Martino M..( 2013;). Pertussis re-emergence in the post-vaccination era. . BMC Infect Dis 13: 151. [CrossRef] [PubMed]
    [Google Scholar]
  5. Ciofi degli Atti M. L., Salmaso S., Bella A., Arigliani R., Gangemi M., Chiamenti G., Brusoni G., Tozzi A. E.. the Pediatric Sentinel Surveillance Study Group( 2002;). Pediatric sentinel surveillance of vaccine-preventable diseases in Italy. . Pediatr Infect Dis J 21: 763–768. [CrossRef] [PubMed]
    [Google Scholar]
  6. de Greeff S. C., de Melker H. E., van Gageldonk P. G., Schellekens J. F., vander Klis F. R., Mollema L., Mooi F. R., Berbers G. A..( 2010;). Seroprevalence of pertussis in The Netherlands: evidence for increased circulation of Bordetella pertussis . . PLoS One 5: e14183. [CrossRef] [PubMed]
    [Google Scholar]
  7. ECDC( 2012;). Guidance and Protocol for the Serological Diagnosis of Human Infection with Bordetella Pertussis . Stockholm:: European Centre for Disease Prevention and Control; (https://www.thl.fi/documents/533963/1449651/Pertussis+toksiini+IgG-ELISA.pdf/9e963f9b-4322-4bdf-a32c-0f358c0d96d6).
    [Google Scholar]
  8. Edelman K., He Q., Makinen J., Sahlberg A., Haanpera M., Schuerman L., Wolter J., Mertsola J..( 2007;). Immunity to pertussis 5 years after booster immunization during adolescence. . Clin Infect Dis 44: 1271–1277. [CrossRef] [PubMed]
    [Google Scholar]
  9. Edmunds W. J., Pebody R. G., Aggerback H., Baron S., Berbers G., Conyn-van Spaendonck M. A., Hallander H. O., Olander R., Maple P. A. et al.( 2000;). The sero-epidemiology of diphtheria in Western Europe. . Epidemiol Infect 125: 113–125.[PubMed] [Crossref]
    [Google Scholar]
  10. EUVAC.NET( 2009;). Pertussis Surveillance Report 2003–2007. Stockholm:: European Centre for Disease Prevention and Control; (http://ecdc.europa.eu/en/publications/Publications/pertussis_report_2003_2007_euvacnet.pdf).
    [Google Scholar]
  11. Fedele G., Cassone A., Ausiello C. M..( 2015;). T-cell immune responses to Bordetella pertussis infection and vaccination. . Pathog Dis 73: ftv051.[Crossref]
    [Google Scholar]
  12. Gabutti G., Bergamini M., Bonanni P., Guido M., Fenoglio D., Giammanco A., Sindoni L., Zotti C., Boddi V. et al.( 2008;). Assessment of humoral and cell-mediated immunity against Bordetella pertussis in adolescent, adult, and senior subjects in Italy. . Epidemiol Infect 136: 1576–1584. [CrossRef] [PubMed]
    [Google Scholar]
  13. Giammanco A., Chiarini A., Maple P. A., Andrews N., Pebody R., Gay N., Olander R. M., Fivet-Groyne F., Baron S. et al.( 2003;). European Sero-Epidemiology Network: standardisation of the assay results for pertussis. . Vaccine 22: 112–120. [CrossRef] [PubMed]
    [Google Scholar]
  14. Giammanco A., Nardone A., Pebody R., Kafatos G., Andrews N., Chiarini A., Taormina S., de Ory F., Prosenc K. et al.( 2008;). European Sero-Epidemiology Network 2: standardisation of immunoassay results for pertussis requires homogeneity in the antigenic preparations. . Vaccine 26: 4486–4493. [CrossRef] [PubMed]
    [Google Scholar]
  15. Gonfiantini M. V., Villani A., Gesualdo F., Pandolfi E., Agricola E., Bozzola E., Arigliani R., Tozzi A. E..( 2013;). Attitude of Italian physicians toward pertussis diagnosis. . Hum Vaccin Immunother 9: 1485–1488. [CrossRef] [PubMed]
    [Google Scholar]
  16. Gonfiantini M. V., Carloni E., Gesualdo F., Pandolfi E., Agricola E., Rizzuto E., Iannazzo S., Ciofi degli Atti M. L., Villani A., Tozzi A. E..( 2014;). Epidemiology of pertussis in Italy: disease trends over the last century. . Euro Surveillance 19: 20921. [CrossRef] [PubMed]
    [Google Scholar]
  17. Guiso N., Berbers G., Fry N. K., He Q., Riffelmann M., Wirsing von König C. H.. the EU Pertstrain group( 2011;). 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. [CrossRef] [PubMed]
    [Google Scholar]
  18. Hallander H. O., Andersson M., Gustafsson L., Ljungman M., Netterlid E..( 2009a;). Seroprevalence of pertussis antitoxin (anti-PT) in Sweden before and 10 years after the introduction of a universal childhood pertussis vaccination program. . APMIS 117: 912–922. [CrossRef] [PubMed]
    [Google Scholar]
  19. Hallander, Ljungman, Storsaeter, Gustafsson.( 2009b;). Kinetics and sensitivity of ELISA IgG pertussis antitoxin after infection and vaccination with Bordetella pertussis in young children. . APMIS 117: 797–807. [CrossRef] [PubMed]
    [Google Scholar]
  20. He Q., Barkoff A. M., Mertsola J., Glismann S., Bacci S.. on behalf of the European Bordetella expert group (EUpertstrain) the European surveillance network for vaccine-preventable diseases (EUVAC.NET)( 2012;). High heterogeneity in methods used for the laboratory confirmation of pertussis diagnosis among European countries, 2010: integration of epidemiological and laboratory surveillance must include standardisation of methodologies and quality assurance. . Euro Surveill 17: 20239.[PubMed] [Crossref]
    [Google Scholar]
  21. Huygen K., Rodeghiero C., Govaerts D., Leroux-Roels I., Melin P., Reynders M., Van Der Meeren S., Van Den Wijngaert S., Pierard D..( 2014;). Bordetella pertussis seroprevalence in Belgian adults aged 20-39 years, 2012. . Epidemiol Infect 142: 724–728. [CrossRef] [PubMed]
    [Google Scholar]
  22. ICONA Working Group( 2009;). ICONA 2008: national vaccination coverage survey among children and adolescents. . Rapporti ISTISAN 2009,: 09/29 (http://www.iss.it/binary/publ/cont/09_29_web.pdf ) (in Italian).
    [Google Scholar]
  23. Italian Ministry of Health( 1991;). Ministerial Decree of 15 December 1990. Surveillance system on infectious diseases. . Official Gazette 6: 8–18.
    [Google Scholar]
  24. Italian Ministry of Health( 2014;). Epidemiological Bulletin. Rome:: Ministero della Salute; (http://www.salute.gov.it/portale/documentazione/p6_2_8_3_1.jsp?lingua=italiano&id=20).
    [Google Scholar]
  25. Italian Vaccine Coverage Survey Working Group( 1994;). Childhood vaccination coverage in Italy: results of a seven-region survey. The Italian Vaccine Coverage Survey Working Group. . Bull World Health Organ 72: 885–895.[PubMed]
    [Google Scholar]
  26. Knuf M., Schmitt H. J., Wolter J., Schuerman L., Jacquet J. M., Kieninger D., Siegrist C. A., Zepp F..( 2008;). Neonatal vaccination with an acellular pertussis vaccine accelerates the acquisition of pertussis antibodies in infants. . J Pediatr 152: 655–660. [CrossRef] [PubMed]
    [Google Scholar]
  27. Long S. S., Welkon C. J., Clark J. L..( 1990;). Widespread silent transmission of pertussis in families: antibody correlates of infection and symptomatology. . J Infect Dis 161: 480–486.[PubMed] [Crossref]
    [Google Scholar]
  28. Mattoo S., Cherry J. D..( 2005;). Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies . . Clin Microbiol Rev 18: 326–382. [CrossRef] [PubMed]
    [Google Scholar]
  29. Melvin J. A., Scheller E. V., Miller J. F., Cotter P. A..( 2014;). Bordetella pertussis pathogenesis: current and future challenges. . Nat Rev Microbiol 12: 274–288. [CrossRef] [PubMed]
    [Google Scholar]
  30. Plotkin S. A..( 2014;). The pertussis problem. . Clin Infect Dis 58: 830–833. [CrossRef] [PubMed]
    [Google Scholar]
  31. Reed G. F., Meade B. D., Steinhoff M. C..( 1995;). The reverse cumulative distribution plot: a graphic method for exploratory analysis of antibody data. . Pediatrics 96: 600–603.[PubMed]
    [Google Scholar]
  32. Reizenstein E., Hallander H.-O., Blackwelder W. C., Kühn I., Ljungman M., Möllby R..( 1995;). Comparison of five calculation modes for antibody ELISA procedures using pertussis serology as a model. . J Immunol Methods 183: 279–290.[PubMed] [Crossref]
    [Google Scholar]
  33. Rønn P. F., Dalby T., Simonsen J., Jørgensen C. S., Linneberg A., Krogfelt K. A..( 2014;). Seroepidemiology of pertussis in a cross-sectional study of an adult general population in Denmark. . Epidemiol Infect 142: 729–737. [CrossRef] [PubMed]
    [Google Scholar]
  34. Rota M. C., D'Ancona F., Massari M., Mandolini D., Giammanco A., Carbonari P., Salmaso S., Ciofi degli Atti M. L..( 2005;). How increased pertussis vaccination coverage is changing the epidemiology of pertussis in Italy. . Vaccine 23: 5299–5305. [CrossRef] [PubMed]
    [Google Scholar]
  35. Teepe J., Broekhuizen B. D., Ieven M., Loens K., Huygen K., Kretzschmar M., de Melker H., Butler C. C., Little P. et al.( 2015;). Prevalence, diagnosis, and disease course of pertussis in adults with acute cough: a prospective, observational study in primary care. . Br J Gen Pract 65: e662e667. [CrossRef] [PubMed]
    [Google Scholar]
  36. Tomovici A., Barreto L., Zickler P., Meekison W., Noya F., Voloshen T., Lavigne P..( 2012;). Humoral immunity 10 years after booster immunization with an adolescent and adult formulation combined tetanus, diphtheria, and 5-component acellular pertussis vaccine. . Vaccine 30: 2647–2653. [CrossRef] [PubMed]
    [Google Scholar]
  37. Tozzi A. E., Ravà L., Ciofi degli Atti M. L., Salmaso S.. the Progetto Pertosse Working Group( 2003;). Clinical presentation of pertussis in unvaccinated and vaccinated children in the first six years of life. . Pediatrics 112: 1069–1075. [CrossRef] [PubMed]
    [Google Scholar]
  38. Versteegh F. G. A., Mertens P. L. J. M., de Melker H. E., Roord J. J., Schellekens J. F. P., Teunis P. F. M..( 2005;). Age-specific long-term course of IgG antibodies to pertussis toxin after symptomatic infection with Bordetella pertussis . . Epidemiol Infect 133: 737–748.[PubMed] [Crossref]
    [Google Scholar]
  39. Wendelboe A. M., Hudgens M. G., Poole C., Van Rie A..( 2007;). Estimating the role of casual contact from the community in transmission of Bordetella pertussis to young infants. . Emerg Themes Epidemiol 4: 15. [CrossRef] [PubMed]
    [Google Scholar]
  40. WHO( 2010;). Pertussis vaccines: WHO position paper. . Wkly Epidemiol Rec 85: 385–400.[PubMed]
    [Google Scholar]
  41. WHO SAGE Pertussis Working Group( 2014;). Background Paper – SAGE April 2014. . http://www.who.int/immunization/sage/meetings/2014/april/1_Pertussis_background_FINAL4_web.pdf (accessed 17 November 2015).
  42. Wiley K. E., Zuo Y., Macartney K. K., McIntyre P. B..( 2013;). Sources of pertussis infection in young infants: a review of key evidence informing targeting of the cocoon strategy. . Vaccine 31: 618–625. [CrossRef] [PubMed]
    [Google Scholar]
  43. Xing D., Wirsing von König C. H., Newland P., Riffelmann M., Meade B. D., Corbel M., Gaines-Das R..( 2009;). Characterization of reference materials for human antiserum to pertussis antigens by an international collaborative study. . Clin Vaccine Immunol 16: 303–311. [CrossRef] [PubMed]
    [Google Scholar]
  44. Yaari E., Yafe-Zimerman Y., Schwartz S. B., Slater P. E., Shvartzman P., Andoren N., Branski D., Kerem E..( 1999;). Clinical manifestations of Bordetella pertussis infection in immunized children and young adults. . Chest 115: 1254–1258. [CrossRef] [PubMed]
    [Google Scholar]
  45. Zepp F., Heininger U., Mertsola J., Bernatowska E., Guiso N., Roord J., Tozzi A. E., Van Damme P..( 2011;). Rationale for pertussis booster vaccination throughout life in Europe. . Lancet Infect Dis 11: 557–570. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000264
Loading
/content/journal/jmm/10.1099/jmm.0.000264
Loading

Data & Media loading...

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