Bordetella Pertussis virulence factors in the continuing evolution of whooping cough vaccines for improved performance (original) (raw)

• Mattoo S, Cherry JD (2005) Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies. Clin Microbiol Rev 18(2):326–382
  Article CAS PubMed PubMed Central Google Scholar
• Gross R, Keidel K, Schmitt K (2010) Resemblance and divergence: the “new” members of the genus Bordetella. Med Microbiol Immunol 199(3):155–163
  Article PubMed Google Scholar
• Guiso N, Hegerle N (2014) Other Bordetellas, lessons for and from pertussis vaccines. Expert Rev Vaccines 13(9):1125–1133
  Article CAS PubMed Google Scholar
• Brinig MM, Register KB, Ackermann MR et al (2006) Genomic features of Bordetella parapertussis clades with distinct host species specificity. Genome Biol 7(9):R81
  Article PubMed PubMed Central CAS Google Scholar
• Diavatopoulos DA, Cummings CA, Schouls LM et al (2005) Bordetella pertussis, the causative agent of whooping cough, evolved from a distinct, human-associated lineage of B. bronchiseptica. PLoS Pathog 1(4):e45
  Article PubMed PubMed Central CAS Google Scholar
• Parkhill J, Sebaihia M, Preston A et al (2003) Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 35(1):32–40
  Article PubMed Google Scholar
• WHO (2010) Pertussis vaccines: WHO position paper. Wkly Epidemiol Rec 85(40):385–400. http://www.whoint/wer/2010/wer8540pdf
• van der Ark AA, Hozbor DF, Boog CJ et al (2012) Resurgence of pertussis calls for re-evaluation of pertussis animal models. Expert Rev Vaccines 11(9):1121–1137
  Article PubMed CAS Google Scholar
• Gambhir M, Clark TA, Cauchemez S et al (2015) A change in vaccine efficacy and duration of protection explains recent rises in pertussis incidence in the United States. PLoS Comput Biol 11(4):e1004138
  Article PubMed PubMed Central CAS Google Scholar
• Cornford-Nairns R, Daggard G, Mukkur T (2012) Construction and preliminary immunobiological characterization of a novel, non-reverting, intranasal live attenuated whooping cough vaccine candidate. J Microbiol Biotechnol 22(6):856–865
  Article CAS PubMed Google Scholar
• Bouchez V, Guiso N (2015) Bordetella pertussis, B. parapertussis, vaccines and cycles of whooping cough. Pathog Dis 73(7):ftv055
  Article PubMed CAS Google Scholar
• Guiso N, Wirsing von Konig CH (2016) Surveillance of pertussis: methods and implementation. Expert Rev Anti Infect Ther 14(7):657–667
  Article CAS PubMed Google Scholar
• Fry SR, Chen AY, Daggard G et al (2008) Parenteral immunization of mice with a genetically inactivated pertussis toxin DNA vaccine induces cell-mediated immunity and protection. J Med Microbiol 57(Pt 1):28–35
  Article CAS PubMed Google Scholar
• NNDSS (2013) Australian Government Department of Health and Ageing (2013): National Notifiable Diseases Surveillance System. http://www9.health.gov.au/cda/source/rpt_3.cfm. Accessed 24 Nov 2015
• Halperin BA, Halperin SA (2011) The reemergence of pertussis and infant deaths: is it time to immunize pregnant women? Future Microbiol 6(4):367–369
  Article PubMed Google Scholar
• King AJ, van der Lee S, Mohangoo A et al (2013) Genome-wide gene expression analysis of Bordetella pertussis isolates associated with a resurgence in pertussis: elucidation of factors involved in the increased fitness of epidemic strains. PLoS One 8(6):e66150
  Article CAS PubMed PubMed Central Google Scholar
• Amirthalingam G, Gupta S, Campbell H (2013) Pertussis immunisation and control in England and Wales, 1957 to 2012: a historical review. Euro Surveill 18(38):20587
  Article PubMed Google Scholar
• CDC (2015) Centers for Disease Control and Prevention, National Notifiable Diseases Surveillance System (NNDSS). http://www.cdc.gov/pertussis/downloads/pertuss-surv-report-2015-provisional.pdf.Accessed 16 June 2016
• van Hoek AJ, Campbell H, Amirthalingam G et al (2013) The number of deaths among infants under one year of age in England with pertussis: results of a capture/recapture analysis for the period 2001 to 2011. Euro Surveill 18:9
  Google Scholar
• Ross PJ, Sutton CE, Higgins S et al (2013) Relative contribution of Th1 and Th17 cells in adaptive immunity to Bordetella pertussis: towards the rational design of an improved acellular pertussis vaccine. PLoS Pathog 9(4):e1003264
  Article CAS PubMed PubMed Central Google Scholar
• Sheridan SL, McCall BJ, Davis CA et al (2014) Acellular pertussis vaccine effectiveness for children during the 2009–2010 pertussis epidemic in Queensland. Med J Aust 200(6):334–338
  Article PubMed Google Scholar
• Tartof SY, Lewis M, Kenyon C et al (2013) Waning immunity to pertussis following 5 doses of DTaP. Pediatrics 131(4):e1047–e1052
  Article PubMed Google Scholar
• Bouchez V, Hegerle N, Strati F et al (2015) New data on vaccine antigen deficient Bordetella pertussis isolates. Vaccines 3(3):751–770
  Article PubMed PubMed Central Google Scholar
• Williams MM, Sen K, Weigand MR et al (2016) Bordetella pertussis strain lacking pertactin and pertussis toxin. Emerg Infect Dis 22(2):319–322
  Article CAS PubMed PubMed Central Google Scholar
• Mooi FR, van Loo IH, van Gent M et al (2009) Bordetella pertussis strains with increased toxin production associated with pertussis resurgence. Emerg Infect Dis 15(8):1206–1213
  Article CAS PubMed PubMed Central Google Scholar
• Cattelan N, Dubey P, Arnal L et al (2016) Bordetella biofilms: a lifestyle leading to persistent infections. Pathog Dis 74(1):ftv108
  Article PubMed CAS Google Scholar
• Conover MS, Sloan GP, Love CF et al (2010) The Bps polysaccharide of Bordetella pertussis promotes colonization and biofilm formation in the nose by functioning as an adhesin. Mol Microbiol 77(6):1439–1455
  Article CAS PubMed PubMed Central Google Scholar
• Litt DJ, Neal SE, Fry NK (2009) Changes in genetic diversity of the Bordetella pertussis population in the United Kingdom between 1920 and 2006 reflect vaccination coverage and emergence of a single dominant clonal type. J Clin Microbiol 47(3):680–688
  Article PubMed PubMed Central Google Scholar
• de Gouw D, Hermans PW, Bootsma HJ et al (2014) Differentially expressed genes in Bordetella pertussis strains belonging to a lineage which recently spread globally. PLoS One 9(1):e84523
  Article PubMed PubMed Central CAS Google Scholar
• Bart MJ, van der Heide HG, Zeddeman A et al (2015) Complete genome sequences of 11 _Bordetella pertussis s_trains representing the pandemic ptxP3 lineage. Genome Announc 3(6):e1394–15
  Article Google Scholar
• Safarchi A, Octavia S, Wu SZ et al (2016) Genomic dissection of Australian Bordetella pertussis isolates from the 2008–2012 epidemic. J Infect 72(4):468–477
  Article PubMed Google Scholar
• Weigand MR, Peng Y, Loparev V et al (2017) The history of Bordetella pertussis genome evolution includes structural rearrangement. J Bacteriol 199:8
  Article Google Scholar
• Zeddeman A, van Gent M, Heuvelman CJ et al (2014) Investigations into the emergence of pertactin-deficient Bordetella pertussis isolates in six European countries, 1996 to 2012. Euro Surveill 19:33
  Article Google Scholar
• Safarchi A, Octavia S, Luu LD et al (2016) Better colonisation of newly emerged Bordetella pertussis in the co-infection mouse model study. Vaccine 34(34):3967–3971
  Article PubMed Google Scholar
• Hovingh ES, van Gent M, Hamstra HJ et al (2017) Emerging Bordetella pertussis strains induce enhanced signaling of human pattern recognition receptors TLR2, NOD2 and secretion of IL-10 by dendritic cells. PLoS One 12(1):e0170027
  Article PubMed PubMed Central Google Scholar
• Lam C, Octavia S, Ricafort L et al (2014) Rapid increase in pertactin-deficient Bordetella pertussis isolates, Australia. Emerg Infect Dis 20(4):626–633
  Article CAS PubMed PubMed Central Google Scholar
• Otsuka N, Han HJ, Toyoizumi-Ajisaka H et al (2012) Prevalence and genetic characterization of pertactin-deficient Bordetella pertussis in Japan. PLoS One 7(2):e31985
  Article CAS PubMed PubMed Central Google Scholar
• Martin SW, Pawloski L, Williams M et al (2015) Pertactin-negative Bordetella pertussis strains: evidence for a possible selective advantage. Clin Infect Dis 60(2):223–227
  Article CAS PubMed Google Scholar
• Safarchi A, Octavia S, Luu LD et al (2015) Pertactin negative Bordetella pertussis demonstrates higher fitness under vaccine selection pressure in a mixed infection model. Vaccine 33(46):6277–6281
  Article CAS PubMed Google Scholar
• Irie Y, Preston A, Yuk MH (2006) Expression of the primary carbohydrate component of the Bordetella bronchiseptica biofilm matrix is dependent on growth phase but independent of Bvg regulation. J Bacteriol 188(18):6680–6687
  Article CAS PubMed PubMed Central Google Scholar
• Decker KB, James TD, Stibitz S et al (2012) The Bordetella pertussis model of exquisite gene control by the global transcription factor BvgA. Microbiology 158(Pt 7):1665–1676
  Article CAS PubMed PubMed Central Google Scholar
• Coutte L, Huot L, Antoine R et al (2016) The multifaceted RisA regulon of Bordetella pertussis. Sci Rep 6:32774
  Article CAS PubMed PubMed Central Google Scholar
• Beier D, Gross R (2008) The BvgS/BvgA phosphorelay system of pathogenic Bordetellae: structure, function and evolution. Adv Exp Med Biol 631:149–160
  Article CAS PubMed Google Scholar
• Merkel TJ, Boucher PE, Stibitz S et al (2003) Analysis of bvgR expression in Bordetella pertussis. J Bacteriol 185(23):6902–6912
  Article CAS PubMed PubMed Central Google Scholar
• Kinnear SM, Marques RR, Carbonetti NH (2001) Differential regulation of Bvg-activated virulence factors plays a role in Bordetella pertussis pathogenicity. Infect Immun 69(4):1983–1993
  Article CAS PubMed PubMed Central Google Scholar
• Deora R, Bootsma HJ, Miller JF et al (2001) Diversity in the Bordetella virulence regulon: transcriptional control of a Bvg-intermediate phase gene. Mol Microbiol 40(3):669–683
  Article CAS PubMed Google Scholar
• Cotter PA, Miller JF (1997) A mutation in the Bordetella bronchiseptica bvgS gene results in reduced virulence and increased resistance to starvation, and identifies a new class of Bvg-regulated antigens. Mol Microbiol 24(4):671–685
  Article CAS PubMed Google Scholar
• Stockbauer KE, Fuchslocher B, Miller JF et al (2001) Identification and characterization of BipA, a Bordetella Bvg-intermediate phase protein. Mol Microbiol 39(1):65–78
  Article CAS PubMed Google Scholar
• Cummings CA, Bootsma HJ, Relman DA et al (2006) Species- and strain-specific control of a complex, flexible regulon by Bordetella BvgAS. J Bacteriol 188(5):1775–1785
  Article CAS PubMed PubMed Central Google Scholar
• Scarlato V, Arico B, Prugnola A et al (1991) Sequential activation and environmental regulation of virulence genes in Bordetella pertussis. EMBO J 10(12):3971–3975
  CAS PubMed PubMed Central Google Scholar
• Jones AM, Boucher PE, Williams CL et al (2005) Role of BvgA phosphorylation and DNA binding affinity in control of Bvg-mediated phenotypic phase transition in Bordetella pertussis. Mol Microbiol 58(3):700–713
  Article CAS PubMed Google Scholar
• Stenson TH, Allen AG, Al-Meer JA et al (2005) Bordetella pertussis risA, but not risS, is required for maximal expression of Bvg-repressed genes. Infect Immun 73(9):5995–6004
  Article CAS PubMed PubMed Central Google Scholar
• Jungnitz H, West NP, Walker MJ et al (1998) A second two-component regulatory system of Bordetella bronchiseptica required for bacterial resistance to oxidative stress, production of acid phosphatase, and in vivo persistence. Infect Immun 66(10):4640–4650
  CAS PubMed PubMed Central Google Scholar
• Medhekar B, Shrivastava R, Mattoo S et al (2009) Bordetella Bsp22 forms a filamentous type III secretion system tip complex and is immunoprotective in vitro and in vivo. Mol Microbiol 71(2):492–504
  Article CAS PubMed Google Scholar
• Villarino Romero R, Bibova I, Cerny O et al (2013) The Bordetella pertussis type III secretion system tip complex protein Bsp22 is not a protective antigen and fails to elicit serum antibody responses during infection of humans and mice. Infect Immun 81(8):2761–2767
  Article PubMed PubMed Central CAS Google Scholar
• Fernandez S, Fajardo EM, Mandiarote A et al (2013) A proteoliposome formulation derived from Bordetella pertussis induces protection in two murine challenge models. BMC Immunol 14(Suppl 1):S8
  PubMed PubMed Central Google Scholar
• de Gouw D, Serra O, de Jonge D MI et al (2014) The vaccine potential of Bordetella pertussis biofilm-derived membrane proteins. Emerg Microb Infect 3:e58
  Article CAS Google Scholar
• Cainelli Gebara VC, Risoleo L, Lopes AP et al (2007) Adjuvant and immunogenic activities of the 73 kDa N-terminal alpha-domain of BrkA autotransporter and Cpn60/60 kDa chaperonin of Bordetella pertussis. Vaccine 25(4):621–629
  Article PubMed CAS Google Scholar
• Marr N, Oliver DC, Laurent V et al (2008) Protective activity of the Bordetella pertussis BrkA autotransporter in the murine lung colonization model. Vaccine 26(34):4306–4311
  Article CAS PubMed Google Scholar
• Alvarez Hayes J, Erben E, Lamberti Y et al (2013) Bordetella pertussis iron regulated proteins as potential vaccine components. Vaccine 31(35):3543–3548
  Article CAS PubMed Google Scholar
• Yilmaz C, Apak A, Ozcengiz E et al (2016) Immunogenicity and protective efficacy of recombinant Iron Superoxide Dismutase protein from Bordetella pertussis in mice models. Microbiol Immunol 60:717–721
  Article CAS PubMed Google Scholar
• Hendrikx LH, Berbers GA, Veenhoven RH et al (2009) IgG responses after booster vaccination with different pertussis vaccines in Dutch children 4 years of age: effect of vaccine antigen content. Vaccine 27(47):6530–6536
  Article CAS PubMed Google Scholar
• Marzouqi I, Richmond P, Fry S et al (2010) Development of improved vaccines against whooping cough: current status. Hum Vaccin 6(7):543–553
  Article CAS PubMed Google Scholar
• Linz B, Ivanov YV, Preston A et al (2016) Acquisition and loss of virulence-associated factors during genome evolution and speciation in three clades of Bordetella species. BMC Genom 17(1):767
  Article CAS Google Scholar
• Mangmool S, Kurose H (2011) G(i/o) protein-dependent and -independent actions of pertussis toxin (PTX). Toxins (Basel) 3(7):884–899
  Article CAS Google Scholar
• Carbonetti NH (2010) Pertussis toxin and adenylate cyclase toxin: key virulence factors of Bordetella pertussis and cell biology tools. Future Microbiol 5(3):455–469
  Article CAS PubMed PubMed Central Google Scholar
• Bouchez V, Brun D, Cantinelli T et al (2009) First report and detailed characterization of B. pertussis isolates not expressing Pertussis Toxin or Pertactin. Vaccine 27(43):6034–6041
  Article CAS PubMed Google Scholar
• Dalby T, Andersen PH, Hoffmann S (2016) Epidemiology of pertussis in Denmark, 1995 to 2013. Euro Surveill 21:36
  Article Google Scholar
• Robbins JB, Schneerson R, Keith JM et al (2009) Pertussis vaccine: a critique. Pediatr Infect Dis J 28(3):237–241
  Article PubMed PubMed Central Google Scholar
• Taranger J, Trollfors B, Bergfors E et al (2001) Immunologic and epidemiologic experience of vaccination with a monocomponent pertussis toxoid vaccine. Pediatrics 108(6):E115
  Article CAS PubMed Google Scholar
• Sutherland JN, Chang C, Yoder SM et al (2011) Antibodies recognizing protective pertussis toxin epitopes are preferentially elicited by natural infection versus acellular immunization. Clin Vaccine Immunol 18(6):954–962
  Article CAS PubMed PubMed Central Google Scholar
• Eby JC, Gray MC, Warfel JM et al (2013) Quantification of the adenylate cyclase toxin of Bordetella pertussis in vitro and during respiratory infection. Infect Immun 81(5):1390–1398
  Article CAS PubMed PubMed Central Google Scholar
• Vojtova J, Kamanova J, Sebo P (2006) Bordetella adenylate cyclase toxin: a swift saboteur of host defense. Curr Opin Microbiol 9(1):69–75
  Article CAS PubMed Google Scholar
• Bumba L, Masin J, Fiser R et al (2010) Bordetella adenylate cyclase toxin mobilizes its beta2 integrin receptor into lipid rafts to accomplish translocation across target cell membrane in two steps. PLoS Pathog 6(5):e1000901
  Article PubMed PubMed Central CAS Google Scholar
• Fiser R, Masin J, Bumba L et al (2012) Calcium influx rescues adenylate cyclase-hemolysin from rapid cell membrane removal and enables phagocyte permeabilization by toxin pores. PLoS Pathog 8(4):e1002580
  Article CAS PubMed PubMed Central Google Scholar
• Guiso N, Grimprel E, Anjak I et al (1993) Western blot analysis of antibody responses of young infants to pertussis infection. Eur J Clin Microbiol Infect Dis 12(8):596–600
  Article CAS PubMed Google Scholar
• Grimprel E, Begue P, Anjak I et al (1996) Long-term human serum antibody responses after immunization with whole-cell pertussis vaccine in France. Clin Diagn Lab Immunol 3(1):93–97
  CAS PubMed PubMed Central Google Scholar
• Guiso N, Szatanik M, Rocancourt M (1991) Protective activity of Bordetella adenylate cyclase-hemolysin against bacterial colonization. Microb Pathog 11(6):423–431
  Article CAS PubMed Google Scholar
• Betsou F, Sebo P, Guiso N (1995) The C-terminal domain is essential for protective activity of the Bordetella pertussis adenylate cyclase-hemolysin. Infect Immun 63(9):3309–3315
  CAS PubMed PubMed Central Google Scholar
• Carbonetti NH (2015) Contribution of pertussis toxin to the pathogenesis of pertussis disease. Pathog Dis 73:ftv073 (PMCID: PMC4626579)
  Article PubMed PubMed Central CAS Google Scholar
• Dautin N, Karimova G, Ladant D (2002) Bordetella pertussis adenylate cyclase toxin: a versatile screening tool. Toxicon 40(10):1383–1387
  Article CAS PubMed Google Scholar
• Fayolle C, Bauche C, Ladant D et al (2004) Bordetella pertussis adenylate cyclase delivers chemically coupled CD8+ T-cell epitopes to dendritic cells and elicits CTL in vivo. Vaccine 23(5):604–614
  Article CAS PubMed Google Scholar
• Schlecht G, Loucka J, Najar H et al (2004) Antigen targeting to CD11b allows efficient presentation of CD4+ and CD8+ T cell epitopes and in vivo Th1-polarized T cell priming. J Immunol 173(10):6089–6097
  Article CAS PubMed Google Scholar
• Mascarell L, Bauche C, Fayolle C et al (2006) Delivery of the HIV-1 Tat protein to dendritic cells by the CyaA vector induces specific Th1 responses and high affinity neutralizing antibodies in non human primates. Vaccine 24(17):3490–3499
  Article CAS PubMed Google Scholar
• Luker KE, Collier JL, Kolodziej EW et al (1993) Bordetella pertussis tracheal cytotoxin and other muramyl peptides: distinct structure-activity relationships for respiratory epithelial cytopathology. Proc Natl Acad Sci USA 90(6):2365–2369
  Article CAS PubMed PubMed Central Google Scholar
• Goldman WE, Cookson BT (1988) Structure and functions of the Bordetella tracheal cytotoxin. Tokai J Exp Clin Med 13(suppl):187–191
  PubMed Google Scholar
• Goodell EW (1985) Recycling of murein by Escherichia coli. J Bacteriol 163(1):305–310
  CAS PubMed PubMed Central Google Scholar
• Flak TA, Heiss LN, Engle JT et al (2000) Synergistic epithelial responses to endotoxin and a naturally occurring muramyl peptide. Infect Immun 68(3):1235–1242
  Article CAS PubMed PubMed Central Google Scholar
• Cundell DR, Kanthakumar K, Taylor GW et al (1994) Effect of tracheal cytotoxin from Bordetella pertussis on human neutrophil function in vitro. Infect Immun 62(2):639–643
  CAS PubMed PubMed Central Google Scholar
• Matsuzawa T, Fukui A, Kashimoto T et al (2004) Bordetella dermonecrotic toxin undergoes proteolytic processing to be translocated from a dynamin-related endosome into the cytoplasm in an acidification-independent manner. J Biol Chem 279(4):2866–2872
  Article CAS PubMed Google Scholar
• Boureux A, Vignal E, Faure S et al (2007) Evolution of the Rho family of ras-like GTPases in eukaryotes. Mol Biol Evol 24(1):203–216
  Article CAS PubMed Google Scholar
• Masuda M, Betancourt L, Matsuzawa T et al (2000) Activation of rho through a cross-link with polyamines catalyzed by Bordetella dermonecrotizing toxin. EMBO J 19(4):521–530
  Article CAS PubMed PubMed Central Google Scholar
• Horiguchi Y (2001) Escherichia coli cytotoxic necrotizing factors and Bordetella dermonecrotic toxin: the dermonecrosis-inducing toxins activating Rho small GTPases. Toxicon 39(11):1619–1627
  Article CAS PubMed Google Scholar
• Matsuzawa T, Kashimoto T, Katahira J et al (2002) Identification of a receptor-binding domain of Bordetella dermonecrotic toxin. Infect Immun 70(7):3427–3432
  Article CAS PubMed PubMed Central Google Scholar
• Weiss AA, Goodwin MS (1989) Lethal infection by Bordetella pertussis mutants in the infant mouse model. Infect Immun 57(12):3757–3764
  CAS PubMed PubMed Central Google Scholar
• Inatsuka CS, Xu Q, Vujkovic-Cvijin I et al (2010) Pertactin is required for Bordetella species to resist neutrophil-mediated clearance. Infect Immun 78(7):2901–2909
  Article CAS PubMed PubMed Central Google Scholar
• Hijnen M, He Q, Schepp R et al (2008) Antibody responses to defined regions of the Bordetella pertussis virulence factor pertactin. Scand J Infect Dis 40(2):94–104
  Article CAS PubMed Google Scholar
• Leininger E, Ewanowich CA, Bhargava A et al (1992) Comparative roles of the Arg-Gly-Asp sequence present in the Bordetella pertussis adhesins pertactin and filamentous hemagglutinin. Infect Immun 60(6):2380–2385
  CAS PubMed PubMed Central Google Scholar
• Leininger E, Roberts M, Kenimer JG et al (1991) Pertactin, an Arg-Gly-Asp-containing Bordetella pertussis surface protein that promotes adherence of mammalian cells. Proc Natl Acad Sci USA 88(2):345–349
  Article CAS PubMed PubMed Central Google Scholar
• Everest P, Li J, Douce G et al (1996) Role of the Bordetella pertussis P.69/pertactin protein and the P.69/pertactin RGD motif in the adherence to and invasion of mammalian cells. Microbiology 142(Pt 11):3261–3268
  Article CAS PubMed Google Scholar
• van den Berg BM, Beekhuizen H, Willems RJ et al (1999) Role of Bordetella pertussis virulence factors in adherence to epithelial cell lines derived from the human respiratory tract. Infect Immun 67(3):1056–1062
  PubMed PubMed Central Google Scholar
• Mooi FR, van Oirschot H, Heuvelman K et al (1998) 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 66(2):670–675
  CAS PubMed PubMed Central Google Scholar
• Barkoff AM, Mertsola J, Guillot S et al (2012) Appearance of Bordetella pertussis strains not expressing the vaccine antigen pertactin in Finland. Clin Vaccine Immunol 19(10):1703–1704
  Article CAS PubMed PubMed Central Google Scholar
• Hallander HO, Advani A, Donnelly D et al (2005) Shifts of Bordetella pertussis variants in Sweden from 1970 to 2003, during three periods marked by different vaccination programs. J Clin Microbiol 43(6):2856–2865
  Article CAS PubMed PubMed Central Google Scholar
• Breakwell L, Kelso P, Finley C et al (2016) Pertussis vaccine effectiveness in the setting of Pertactin-deficient pertussis. Pediatrics 137(5):e20153973
  Article PubMed Google Scholar
• Komatsu E, Yamaguchi F, Abe A et al (2010) Synergic effect of genotype changes in pertussis toxin and pertactin on adaptation to an acellular pertussis vaccine in the murine intranasal challenge model. Clin Vaccine Immunol 17(5):807–812
  Article CAS PubMed PubMed Central Google Scholar
• Bottero D, Gaillard ME, Fingermann M et al (2007) Pulsed-field gel electrophoresis, pertactin, pertussis toxin S1 subunit polymorphisms, and surfaceome analysis of vaccine and clinical Bordetella pertussis strains. Clin Vaccine Immunol 14(11):1490–1498
  Article CAS PubMed PubMed Central Google Scholar
• Finn TM, Stevens LA (1995) Tracheal colonization factor: a Bordetella pertussis secreted virulence determinant. Mol Microbiol 16(4):625–634
  Article CAS PubMed Google Scholar
• Chen I, Finn TM, Yanqing L et al (1998) A recombinant live attenuated strain of Vibrio cholerae induces immunity against tetanus toxin and Bordetella pertussis tracheal colonization factor. Infect Immun 66(4):1648–1653
  CAS PubMed PubMed Central Google Scholar
• Fernandez RC, Weiss AA (1994) Cloning and sequencing of a Bordetella pertussis serum resistance locus. Infect Immun 62(11):4727–4738
  CAS PubMed PubMed Central Google Scholar
• Zhai Y, Zhang K, Huo Y et al (2011) Autotransporter passenger domain secretion requires a hydrophobic cavity at the extracellular entrance of the beta-domain pore. Biochem J 435(3):577–587
  Article CAS PubMed Google Scholar
• Oliver DC, Fernandez RC (2001) Antibodies to BrkA augment killing of Bordetella pertussis. Vaccine 20(1–2):235–241
  Article CAS PubMed Google Scholar
• Finn TM, Amsbaugh DF (1998) Vag8, a Bordetella pertussis bvg-regulated protein. Infect Immun 66(8):3985–3989
  CAS PubMed PubMed Central Google Scholar
• Marr N, Shah NR, Lee R et al (2011) Bordetella pertussis autotransporter Vag8 binds human C1 esterase inhibitor and confers serum resistance. PLoS One 6(6):e20585
  Article CAS PubMed PubMed Central Google Scholar
• de Gouw D, de Jonge MI, Hermans PW et al (2014) Proteomics-identified Bvg-activated autotransporters protect against Bordetella pertussis in a mouse model. PLoS One 9(8):e105011
  Article PubMed PubMed Central CAS Google Scholar
• Noofeli M, Bokhari H, Blackburn P et al (2011) BapC autotransporter protein is a virulence determinant of Bordetella pertussis. Microb Pathog 51(3):169–177
  Article CAS PubMed Google Scholar
• de Gouw D, Diavatopoulos DA, Bootsma HJ et al (2011) Pertussis: a matter of immune modulation. FEMS Microbiol Rev 35(3):441–474
  Article CAS PubMed Google Scholar
• Asgarian-Omran H, Amirzargar AA, Arjmand M et al (2013) Expression, purification and characterization of three overlapping immunodominant recombinant fragments from Bordetella pertussis filamentous hemagglutinin. Avicenna J Med Biotechnol 5(1):20–28
  CAS PubMed PubMed Central Google Scholar
• Scheller EV, Melvin JA, Sheets AJ et al (2015) Cooperative roles for fimbria and filamentous hemagglutinin in Bordetella adherence and immune modulation. MBio 6(3):e00500–e00515
  Article CAS PubMed PubMed Central Google Scholar
• Coutte L, Willery E, Antoine R et al (2003) Surface anchoring of bacterial subtilisin important for maturation function. Mol Microbiol 49(2):529–539
  Article CAS PubMed Google Scholar
• Coutte L, Alonso S, Reveneau N et al (2003) Role of adhesin release for mucosal colonization by a bacterial pathogen. J Exp Med 197(6):735–742
  Article CAS PubMed PubMed Central Google Scholar
• Knight JB, Huang YY, Halperin SA et al (2006) Immunogenicity and protective efficacy of a recombinant filamentous haemagglutinin from Bordetella pertussis. Clin Exp Immunol 144(3):543–551
  Article CAS PubMed PubMed Central Google Scholar
• Alonso S, Reveneau N, Pethe K et al (2002) Eighty-kilodalton N-terminal moiety of Bordetella pertussis filamentous hemagglutinin: adherence, immunogenicity, and protective role. Infect Immun 70(8):4142–4147
  Article CAS PubMed PubMed Central Google Scholar
• Nuccio SP, Baumler AJ (2007) Evolution of the chaperone/usher assembly pathway: fimbrial classification goes Greek. Microbiol Mol Biol Rev 71(4):551–575
  Article CAS PubMed PubMed Central Google Scholar
• Chen Q, Decker KB, Boucher PE et al (2010) Novel architectural features of Bordetella pertussis fimbrial subunit promoters and their activation by the global virulence regulator BvgA. Mol Microbiol 77(5):1326–1340
  Article CAS PubMed PubMed Central Google Scholar
• Hazenbos WL, van den Berg BM, Geuijen CW et al (1995) Binding of FimD on Bordetella pertussis to very late antigen-5 on monocytes activates complement receptor type 3 via protein tyrosine kinases. J Immunol 155(8):3972–3978
  CAS PubMed Google Scholar
• Geuijen CA, Willems RJ, Bongaerts M et al (1997) Role of the Bordetella pertussis minor fimbrial subunit, FimD, in colonization of the mouse respiratory tract. Infect Immun 65(10):4222–4228
  CAS PubMed PubMed Central Google Scholar
• Guevara C, Zhang C, Gaddy JA et al (2016) Highly differentiated human airway epithelial cells: a model to study host cell-parasite interactions in pertussis. Infect Dis 48(3):177–188
  Article CAS Google Scholar
• Irie Y, Mattoo S, Yuk MH (2004) The Bvg virulence control system regulates biofilm formation in Bordetella bronchiseptica. J Bacteriol 186(17):5692–5698
  Article CAS PubMed PubMed Central Google Scholar
• van den Berg BM, Beekhuizen H, Mooi FR et al (1999) Role of antibodies against Bordetella pertussis virulence factors in adherence of Bordetella pertussis and Bordetella parapertussis to human bronchial epithelial cells. Infect Immun 67(3):1050–1055
  PubMed PubMed Central Google Scholar
• Rodriguez ME, Hellwig SM, Perez Vidakovics ML et al (2006) Bordetella pertussis attachment to respiratory epithelial cells can be impaired by fimbriae-specific antibodies. FEMS Immunol Med Microbiol 46(1):39–47
  Article CAS PubMed Google Scholar
• Gustafsson L, Hallander HO, Olin P et al (1996) A controlled trial of a two-component acellular, a five-component acellular, and a whole-cell pertussis vaccine. N Engl J Med 334(6):349–355
  Article CAS PubMed Google Scholar
• McCormack PL (2013) DTaP-IPV-Hep B-Hib vaccine (Hexaxim(R)): a review of its use in primary and booster vaccination. Paediatr Drugs 15(1):59–70
  Article PubMed Google Scholar
• Hallander HO, Ljungman M, Jahnmatz M et al (2009) Should fimbriae be included in pertussis vaccines? Studies on ELISA IgG anti-Fim2/3 antibodies after vaccination and infection. APMIS 117(9):660–671
  Article CAS PubMed Google Scholar
• Bart MJ, Harris SR, Advani A et al (2014) Global population structure and evolution of Bordetella pertussis and their relationship with vaccination. MBio 5(2):e01074
  Article PubMed PubMed Central Google Scholar
• van Gent M, Bart MJ, van der Heide HG et al (2012) Small mutations in Bordetella pertussis are associated with selective sweeps. PLoS One 7(9):e46407
  Article PubMed PubMed Central CAS Google Scholar
• Heikkinen E, Xing DK, Olander RM et al (2008) Bordetella pertussis isolates in Finland: serotype and fimbrial expression. BMC Microbiol 8:162
  Article PubMed PubMed Central CAS Google Scholar
• Shuel M, Jamieson FB, Tang P et al (2013) Genetic analysis of Bordetella pertussis in Ontario, Canada reveals one predominant clone. Int J Infect Dis 17(6):e413-417
  Article CAS Google Scholar
• Caro V, Elomaa A, Brun D et al (2006) Bordetella pertussis, Finland and France. Emerg Infect Dis 12(6):987–989
  Article PubMed PubMed Central Google Scholar
• Borisova O, Kombarova SY, Zakharova NS et al (2007) Antigenic divergence between Bordetella pertussis clinical isolates from Moscow, Russia, and vaccine strains. Clin Vaccine Immunol 14(3):234–238
  Article CAS PubMed PubMed Central Google Scholar
• Dakic G, Kallonen T, Elomaa A et al (2010) Bordetella pertussis vaccine strains and circulating isolates in Serbia. Vaccine 28(5):1188–1192
  Article CAS PubMed Google Scholar
• Advani A, Donnelly D, Gustafsson L et al (2007) Changes of the Swedish Bordetella pertussis population in incidence peaks during an acellular pertussis vaccine period between 1997 and 2004. APMIS 115(4):299–310
  Article CAS PubMed Google Scholar
• Puhar A, Sansonetti PJ (2014) Type III secretion system. Curr Biol 24(17):R784–R791
  Article CAS PubMed Google Scholar
• Yuk MH, Harvill ET, Miller JF (1998) The BvgAS virulence control system regulates type III secretion in Bordetella bronchiseptica. Mol Microbiol 28(5):945–959
  Article CAS PubMed Google Scholar
• Kurushima J, Kuwae A, Abe A (2012) The type III secreted protein BspR regulates the virulence genes in Bordetella bronchiseptica. PLoS One 7(6):e38925
  Article CAS PubMed PubMed Central Google Scholar
• Ahuja U, Shokeen B, Cheng N et al (2016) Differential regulation of type III secretion and virulence genes in Bordetella pertussis and Bordetella bronchiseptica by a secreted anti-sigma factor. Proc Natl Acad Sci 113(9):2341–2348
  Article CAS PubMed PubMed Central Google Scholar
• Han HJ, Kuwae A, Abe A et al (2011) Differential expression of type III effector BteA protein due to IS481 insertion in Bordetella pertussis. PLoS One 6(3):e17797
  Article CAS PubMed PubMed Central Google Scholar
• Fennelly NK, Sisti F, Higgins SC et al (2008) Bordetella pertussis expresses a functional type III secretion system that subverts protective innate and adaptive immune responses. Infect Immun 76(3):1257–1266
  Article CAS PubMed PubMed Central Google Scholar
• Brickman TJ, Hanawa T, Anderson MT et al (2008) Differential expression of Bordetella pertussis iron transport system genes during infection. Mol Microbiol 70(1):3–14
  Article CAS PubMed PubMed Central Google Scholar
• Alvarez Hayes J, Erben E, Lamberti Y et al (2011) Identification of a new protective antigen of Bordetella pertussis. Vaccine 29(47):8731–8739
  Article CAS PubMed Google Scholar
• Banerjee S, Weerasinghe AJ, Parker Siburt CJ et al (2014) Bordetella pertussis FbpA binds both unchelated iron and iron siderophore complexes. BioChemistry 53(24):3952–3960
  Article CAS PubMed PubMed Central Google Scholar
• Flak TA, Goldman WE (1999) Signalling and cellular specificity of airway nitric oxide production in pertussis. Cell Microbiol 1(1):51–60
  Article CAS PubMed Google Scholar
• Fedele G, Nasso M, Spensieri F et al (2008) Lipopolysaccharides from Bordetella pertussis and Bordetella parapertussis differently modulate human dendritic cell functions resulting in divergent prevalence of Th17-polarized responses. J Immunol 181(1):208–216
  Article CAS PubMed Google Scholar
• Albitar-Nehme S, Basheer SM, Njamkepo E et al (2013) Comparison of lipopolysaccharide structures of Bordetella pertussis clinical isolates from pre- and post-vaccine era. Carbohydr Res 378:56–62
  Article CAS PubMed Google Scholar
• Mishra M, Parise G, Jackson KD et al (2005) The BvgAS signal transduction system regulates biofilm development in Bordetella. J Bacteriol 187(4):1474–1484
  Article CAS PubMed PubMed Central Google Scholar
• Patel R (2005) Biofilms and antimicrobial resistance. Clin Orthop Relat Res (437):41–47
• Anderson GG, O’Toole GA (2008) Innate and induced resistance mechanisms of bacterial biofilms. Curr Top Microbiol Immunol 322:85–105
  CAS PubMed Google Scholar
• Otto M (2006) Bacterial evasion of antimicrobial peptides by biofilm formation. Curr Top Microbiol Immunol 306:251–258
  CAS PubMed Google Scholar
• Chen L, Wen YM (2011) The role of bacterial biofilm in persistent infections and control strategies. Int J Oral Sci 3(2):66–73
  Article CAS PubMed PubMed Central Google Scholar
• Nicholson TL, Conover MS, Deora R (2012) Transcriptome profiling reveals stage-specific production and requirement of flagella during biofilm development in Bordetella bronchiseptica. PLoS One 7(11):e49166
  Article CAS PubMed PubMed Central Google Scholar
• Serra DO, Conover MS, Arnal L et al (2011) FHA-mediated cell-substrate and cell-cell adhesions are critical for Bordetella pertussis biofilm formation on abiotic surfaces and in the mouse nose and the trachea. PLoS One 6(12):e28811
  Article CAS PubMed PubMed Central Google Scholar
• Hoffman C, Eby J, Gray M et al (2017) Bordetella adenylate cyclase toxin interacts with filamentous haemagglutinin to inhibit biofilm formation in vitro. Mol Microbiol 103(2):214–228
  Article CAS PubMed Google Scholar
• Conover MS, Redfern CJ, Ganguly T et al (2012) BpsR modulates Bordetella biofilm formation by negatively regulating the expression of the Bps polysaccharide. J Bacteriol 194(2):233–242
  Article CAS PubMed PubMed Central Google Scholar
• Little DJ, Milek S, Bamford NC et al (2015) The protein BpsB is a poly-beta-1,6-_N_-acetyl-d-glucosamine deacetylase required for biofilm formation in Bordetella bronchiseptica. J Biol Chem 290(37):22827–22840
  Article CAS PubMed PubMed Central Google Scholar
• Sloan GP, Love CF, Sukumar N et al (2007) The Bordetella Bps polysaccharide is critical for biofilm development in the mouse respiratory tract. J Bacteriol 189(22):8270–8276
  Article CAS PubMed PubMed Central Google Scholar
• Conover MS, Mishra M, Deora R (2011) Extracellular DNA is essential for maintaining Bordetella biofilm integrity on abiotic surfaces and in the upper respiratory tract of mice. PLoS One 6(2):e16861
  Article CAS PubMed PubMed Central Google Scholar
• Dorji D, Graham RM, Richmond P et al (2016) Biofilm forming potential and antimicrobial susceptibility of newly emerged Western Australian Bordetella pertussis clinical isolates. Biofouling 32(9):1141–1152
  Article CAS PubMed Google Scholar
• Arnal L, Grunert T, Cattelan N et al (2015) Bordetella pertussis isolates from Argentinean whooping cough patients display enhanced biofilm formation capacity compared to Tohama I reference strain. Front Microbiol 6:1352
  Article PubMed PubMed Central Google Scholar
• Cattelan N, Jennings-Gee J, Dubey P et al (2017) Hyperbiofilm formation by Bordetella pertussis strains correlates with enhanced virulence traits. Infect Immun. doi:10.1128/IAI.00373-17
  PubMed Google Scholar
• Bhinu VS (2005) Insight into biofilm-associated microbial life. J Mol Microbiol Biotechnol 10(1):15–21
  Article CAS PubMed Google Scholar
• Serra D, Bosch A, Russo DM et al (2007) Continuous nondestructive monitoring of Bordetella pertussis biofilms by Fourier transform infrared spectroscopy and other corroborative techniques. Anal Bioanal Chem 387(5):1759–1767
  Article CAS PubMed Google Scholar
• Serra DO, Lucking G, Weiland F et al (2008) Proteome approaches combined with Fourier transform infrared spectroscopy revealed a distinctive biofilm physiology in Bordetella pertussis. Proteomics 8(23–24):4995–5010
  Article CAS PubMed Google Scholar
• Bosch A, Serra D, Prieto C et al (2006) Characterization of Bordetella pertussis growing as biofilm by chemical analysis and FT-IR spectroscopy. Appl Microbiol Biotechnol 71(5):736–747
  Article CAS PubMed Google Scholar
• Bancroft T, Dillon MB, da Silva Antunes R et al (2016) Th1 versus Th2 T cell polarization by whole-cell and acellular childhood pertussis vaccines persists upon re-immunization in adolescence and adulthood. Cell Immunol 304–305:35–43
  Article PubMed PubMed Central CAS Google Scholar
• Mills KH, Barnard A, Watkins J et al (1993) Cell-mediated immunity to Bordetella pertussis: role of Th1 cells in bacterial clearance in a murine respiratory infection model. Infect Immun 61(2):399–410
  CAS PubMed PubMed Central Google Scholar
• Rieber N, Graf A, Hartl D et al (2011) Acellular pertussis booster in adolescents induces Th1 and memory CD8+ T cell immune response. PLoS One 6(3):e17271
  Article CAS PubMed PubMed Central Google Scholar
• Martin C, Etxaniz A, Uribe KB et al (2015) Adenylate cyclase toxin promotes bacterial internalisation into non phagocytic cells. Sci Rep 5:13774
  Article PubMed PubMed Central Google Scholar
• Culotta CE, Dominick D, ER H (1935) Whooping cough. II. Experimental study. J Pediatr 6:743–752
  Article Google Scholar
• Warfel JM, Zimmerman LI, Merkel TJ (2014) Acellular pertussis vaccines protect against disease but fail to prevent infection and transmission in a nonhuman primate model. Proc Natl Acad Sci USA 111(2):787–792
  Article CAS PubMed Google Scholar
• Hozbor D, Rodriguez ME, Fernandez J et al (1999) Release of outer membrane vesicles from Bordetella pertussis. Curr Microbiol 38(5):273–278
  Article CAS PubMed Google Scholar
• Raeven RH, van der Maas L, Tilstra W et al (2015) Immunoproteomic profiling of Bordetella pertussis outer membrane vesicle vaccine reveals broad and balanced humoral immunogenicity. J Proteome Res 14(7):2929–2942
  Article CAS PubMed Google Scholar
• Ulmer JB, Donnelly JJ, Parker SE et al (1993) Heterologous protection against influenza by injection of DNA encoding a viral protein. Science 259(5102):1745–1749
  Article CAS PubMed Google Scholar
• Kamachi K, Konda T, Arakawa Y (2003) DNA vaccine encoding pertussis toxin S1 subunit induces protection against Bordetella pertussis in mice. Vaccine 21(31):4609–4615
  Article CAS PubMed Google Scholar
• Kamachi K, Arakawa Y (2007) Development of safer pertussis DNA vaccine expressing non-toxic C180 polypeptide of pertussis toxin S1 subunit. Vaccine 25(6):1000–1006
  Article CAS PubMed Google Scholar
• Kamachi K, Arakawa Y (2004) Expression of a C terminally truncated form of pertussis toxin S1 subunit effectively induces protection against pertussis toxin following DNA-based immunization. Infect Immun 72(7):4293–4296
  Article CAS PubMed PubMed Central Google Scholar
• Li Q, Zhu Y, Chu J et al (2006) Protective immunity against Bordetella pertussis by a recombinant DNA vaccine and the effect of coinjection with a granulocyte-macrophage colony stimulating factor gene. Microbiol Immunol 50(12):929–936
  Article CAS PubMed Google Scholar
• Fry SR, Chen AY, Daggard GE et al (2016) Bordetella pertussis filamentous hemagglutinin and pertactin DNA vaccines. Curr Trends Microbiol 10:95
• Guzman CA, Molinari G, Fountain MW et al (1993) Antibody responses in the serum and respiratory tract of mice following oral vaccination with liposomes coated with filamentous hemagglutinin and pertussis toxoid. Infect Immun 61(2):573–579
  CAS PubMed PubMed Central Google Scholar
• Conway MA, Madrigal-Estebas L, McClean S et al (2001) Protection against Bordetella pertussis infection following parenteral or oral immunization with antigens entrapped in biodegradable particles: effect of formulation and route of immunization on induction of Th1 and Th2 cells. Vaccine 19(15–16):1940–1950
  Article CAS PubMed Google Scholar
• Zhao L, Seth A, Wibowo N et al (2014) Nanoparticle vaccines. Vaccine 32(3):327–337
  Article PubMed Google Scholar
• Angsantikul P, Thamphiwatana S, Gao W et al (2015) Cell membrane-coated nanoparticles as an emerging antibacterial vaccine platform. Vaccines (Basel) 3(4):814–828
  Article Google Scholar
• Roberts M, Maskell D, Novotny P et al (1990) Construction and characterization in vivo of Bordetella pertussis aroA mutants. Infect Immun 58(3):732–739
  CAS PubMed PubMed Central Google Scholar
• Siniashina LN, Siniashina LS, Semin EG et al (2010) Construction of the genetically attenuated bacteria Bordetella pertussis devoid of dermonecrotic toxin activity and producing modified nontoxic pertussis toxin form. Mol Gen Mikrobiol Virusol (3):31–36
• Mielcarek N, Debrie AS, Raze D et al (2006) Live attenuated B. pertussis as a single-dose nasal vaccine against whooping cough. PLoS Pathog 2(7):e65
  Article PubMed PubMed Central CAS Google Scholar
• Feunou PF, Kammoun H, Debrie AS et al (2010) Long-term immunity against pertussis induced by a single nasal administration of live attenuated B. pertussis BPZE1. Vaccine 28(43):7047–7053
  Article CAS PubMed Google Scholar
• Fedele G, Bianco M, Debrie AS et al (2011) Attenuated Bordetella pertussis vaccine candidate BPZE1 promotes human dendritic cell CCL21-induced migration and drives a Th1/Th17 response. J Immunol 186(9):5388–5396
  Article CAS PubMed Google Scholar
• Thorstensson R, Trollfors B, Al-Tawil N et al (2014) A phase I clinical study of a live attenuated Bordetella pertussis vaccine-BPZE1; a single centre, double-blind, placebo-controlled, dose-escalating study of BPZE1 given intranasally to healthy adult male volunteers. PLoS One 9(1):e83449
  Article PubMed PubMed Central CAS Google Scholar
• Jahnmatz M, Amu S, Ljungman M et al (2014) B-cell responses after intranasal vaccination with the novel attenuated Bordetella pertussis vaccine strain BPZE1 in a randomized phase I clinical trial. Vaccine 32(27):3350–3356
  Article CAS PubMed Google Scholar
• Tan T, Trindade E, Skowronski D (2005) Epidemiology of pertussis. Pediatr Infect Dis J 24(5 Suppl):S10–S18
  Article PubMed Google Scholar
• Elahi S, Van Kessel J, Kiros TG et al (2014) c-di-GMP enhances protective innate immunity in a murine model of pertussis. PLoS One 9(10):e109778
  Article PubMed PubMed Central CAS Google Scholar
• Dunne A, Mielke LA, Allen AC et al (2015) A novel TLR2 agonist from Bordetella pertussis is a potent adjuvant that promotes protective immunity with an acellular pertussis vaccine. Mucosal Immunol 8(3):607–617
  Article CAS PubMed Google Scholar
• Geurtsen J, Banus HA, Gremmer ER et al (2007) Lipopolysaccharide analogs improve efficacy of acellular pertussis vaccine and reduce type I hypersensitivity in mice. Clin Vaccine Immunol 14(7):821–829
  Article CAS PubMed PubMed Central Google Scholar
• Agnolon V, Bruno C, Leuzzi R et al (2015) The potential of adjuvants to improve immune responses against TdaP vaccines: a preclinical evaluation of MF59 and monophosphoryl lipid A. Int J Pharm 492(1–2):169–176
  Article CAS PubMed Google Scholar
• Cherry JD, Heininger U, Richards DM et al (2010) Antibody response patterns to Bordetella pertussis antigens in vaccinated (primed) and unvaccinated (unprimed) young children with pertussis. Clin Vaccine Immunol 17(5):741–747
  Article CAS PubMed PubMed Central Google Scholar
• Hallander HO, Gustafsson L (2009) Efficacy and effectiveness of acellular pertussis vaccines: a 20-year Swedish experience. Expert Rev Vaccines 8(10):1303–1307
  Article CAS PubMed Google Scholar
• Carbonetti NH, Wirsing von Konig CH, Lan R et al (2016) Highlights of the 11th International Bordetella symposium: from basic biology to vaccine development. Clin Vaccine Immunol 23(11):842–850
  Article CAS PubMed PubMed Central Google Scholar