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Review

Resurgence of pertussis calls for re-evaluation of pertussis animal models

, , , , &
Pages 1121-1137 | Published online: 09 Jan 2014

References

  • WHO. Pertussis vaccines: WHO position paper. Wkly Epidemiol. Rec. 85(40), 385–400 (2010).
  • Halperin S, De Serres, G. Pertussis. In: Bacterial Infections of Humans. Brachman PS, Elias A (Eds). Springer, NY, USA, 577–595 (2009).
  • Yih WK, Silva EA, Ida J, Harrington N, Lett SM, George H. Bordetella holmesii-like organisms isolated from Massachusetts patients with pertussis-like symptoms. Emerging Infect. Dis. 5(3), 441–443 (1999).
  • Diavatopoulos DA, Cummings CA, Schouls LM, Brinig MM, Relman DA, Mooi FR. Bordetella pertussis, the causative agent of whooping cough, evolved from a distinct, human-associated lineage of B. bronchiseptica. PLoS Pathog. 1(4), e45 (2005).
  • Locht C. Molecular aspects of Bordetella pertussis pathogenesis. Int. Microbiol. 2(3), 137–144 (1999).
  • Merkel TJ, Boucher PE, Stibitz S, Grippe VK. Analysis of bvgR expression in Bordetella pertussis. J. Bacteriol. 185(23), 6902–6912 (2003).
  • King AJ, van Gorkom T, van der Heide HG, Advani A, van der Lee S. Changes in the genomic content of circulating Bordetella pertussis strains isolated from The Netherlands, Sweden, Japan and Australia: adaptive evolution or drift? BMC Genomics 11, 64 (2010).
  • Bart MJ, van Gent M, van der Heide HG et al. Comparative genomics of prevaccination and modern Bordetella pertussis strains. BMC Genomics 11, 627 (2010).
  • Mooi FR. Bordetella pertussis and vaccination: the persistence of a genetically monomorphic pathogen. Infect. Genet. Evol. 10(1), 36–49 (2010).
  • Canthaboo C, Xing D, Douglas A, Corbel M. Investigation of an aerosol challenge model as alternative to the intracerebral mouse protection test for potency assay of whole cell pertussis vaccines. Biologicals 28(4), 241–246 (2000).
  • Mills KH. Immunity to Bordetella pertussis. Microbes Infect. 3(8), 655–677 (2001).
  • van der Ark A, van Straaten-van de Kappelle I, Hendriksen C, van de Donk H. Pertussis serological potency test as an alternatively to the intracerebral mouse protection test. Dev. Biol. Stand. 86, 271–281 (1996).
  • Ausiello CM, Lande R, Urbani F et al. Cell-mediated immune responses in four-year-old children after primary immunization with acellular pertussis vaccines. Infect. Immun. 67(8), 4064–4071 (1999).
  • Hendrikx LH, Schure RM, Oztürk K et al. Different IgG-subclass distributions after whole-cell and acellular pertussis infant primary vaccinations in healthy and pertussis infected children. Vaccine 29(40), 6874–6880 (2011).
  • Mascart F, Hainaut M, Peltier A, Verscheure V, Levy J, Locht C. Modulation of the infant immune responses by the first pertussis vaccine administrations. Vaccine 25(2), 391–398 (2007).
  • Lugauer S, Heininger U, Cherry JD, Stehr K. Long-term clinical effectiveness of an acellular pertussis component vaccine and a whole cell pertussis component vaccine. Eur. J. Pediatr. 161(3), 142–146 (2002).
  • Wendelboe AM, Van Rie A, Salmaso S, Englund JA. Duration of immunity against pertussis after natural infection or vaccination. Pediatr. Infect. Dis. J. 24(Suppl. 5), S58–S61 (2005).
  • Kendrick PL, Eldering G. Mouse protection tests in the study of pertussis vaccine; a comparative series using the intracerebral route for challenge. Am. J. Public Health Nations. Health 37(7), 803–810 (1947).
  • Gaines-Das R, Horiuchi Y, Zhang SM et al. Modified intra-cerebral challenge assay for acellular pertussis vaccines: comparisons among whole cell and acellular vaccines. Vaccine 27(49), 6824–6832 (2009).
  • André M, Poirier B, Bornstein N, Marmonier D, El Zaouk A, Fuchs F. Key points for the development of mouse immunogenicity test as potency assay for acellular pertussis vaccines. Biologicals 28(4), 217–225 (2000).
  • Mastrantonio P, Spigaglia P, van Oirschot H et al. Antigenic variants in Bordetella pertussis strains isolated from vaccinated and unvaccinated children. Microbiology (Reading, Engl.) 145(Pt 8), 2069–2075 (1999).
  • Guiso N, Capiau C, Carletti G, Poolman J, Hauser P. Intranasal murine model of Bordetella pertussis infection. I. Prediction of protection in human infants by acellular vaccines. Vaccine 17(19), 2366–2376 (1999).
  • Mills KH, Brady M, Ryan E, Mahon BP. A respiratory challenge model for infection with Bordetella pertussis: application in the assessment of pertussis vaccine potency and in defining the mechanism of protective immunity. Dev. Biol. Stand. 95, 31–41 (1998).
  • Mills KH, Ryan M, Ryan E, Mahon BP. A murine model in which protection correlates with pertussis vaccine efficacy in children reveals complementary roles for humoral and cell-mediated immunity in protection against Bordetella pertussis. Infect. Immun. 66(2), 594–602 (1998).
  • Taranger J, Trollfors B, Bergfors E et al. Mass vaccination of children with pertussis toxoid – decreased incidence in both vaccinated and nonvaccinated persons. Clin. Infect. Dis. 33(7), 1004–1010 (2001).
  • Kim TH, Johnstone J, Loeb M. Vaccine herd effect. Scand. J. Infect. Dis. 43(9), 683–689 (2011).
  • Rashid H, Khandaker G, Booy R. Vaccination and herd immunity: what more do we know? Curr. Opin. Infect. Dis. 25(3), 243–249 (2012).
  • Hewlett EL, Edwards KM. Clinical practice. Pertussis – not just for kids. N. Engl. J. Med. 352(12), 1215–1222 (2005).
  • Tan T, Trindade E, Skowronski D. Epidemiology of pertussis. Pediatr. Infect. Dis. J. 24(Suppl. 5), S10–S18 (2005).
  • Hallander HO, Advani A, Donnelly D, Gustafsson L, Carlsson RM. 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 (2005).
  • Hozbor D, Mooi F, Flores D et al. Pertussis epidemiology in Argentina: trends over 2004–2007. J. Infect. 59(4), 225–231 (2009).
  • van Amersfoorth SC, Schouls LM, van der Heide HG et al. Analysis of Bordetella pertussis populations in European countries with different vaccination policies. J. Clin. Microbiol. 43(6), 2837–2843 (2005).
  • Octavia S, Sintchenko V, Gilbert GL et al. Newly emerging clones of Bordetella pertussis carrying prn2 and ptxP3 alleles implicated in Australian pertussis epidemic in 2008–2010. J. Infect. Dis. 205(8), 1220–1224 (2012).
  • Peppler MS, Kuny S, Nevesinjac A et al. Strain variation among Bordetella pertussis isolates from Québec and Alberta provinces of Canada from 1985 to 1994. J. Clin. Microbiol. 41(7), 3344–3347 (2003).
  • Aguas R, Gonçalves G, Gomes MG. Pertussis: increasing disease as a consequence of reducing transmission. Lancet Infect. Dis. 6(2), 112–117 (2006).
  • Bamberger ES, Srugo I. What is new in pertussis? Eur. J. Pediatr. 167(2), 133–139 (2008).
  • Packard ER, Parton R, Coote JG, Fry NK. Sequence variation and conservation in virulence-related genes of Bordetella pertussis isolates from the UK. J. Med. Microbiol. 53(Pt 5), 355–365 (2004).
  • van Boven M, Mooi FR, Schellekens JF, de Melker HE, Kretzschmar M. Pathogen adaptation under imperfect vaccination: implications for pertussis. Proc. Biol. Sci. 272(1572), 1617–1624 (2005).
  • Hallander H, Advani A, Riffelmann M et al. Bordetella pertussis strains circulating in Europe in 1999 to 2004 as determined by pulsed-field gel electrophoresis. J. Clin. Microbiol. 45(10), 3257–3262 (2007).
  • He Q, Mertsola J. Factors contributing to pertussis resurgence. Future Microbiol. 3(3), 329–339 (2008).
  • Mooi FR, van Loo IH, van Gent M et al. Bordetella pertussis strains with increased toxin production associated with pertussis resurgence. Emerging Infect. Dis. 15(8), 1206–1213 (2009).
  • Van Loo IH, Mooi FR. Changes in the Dutch Bordetella pertussis population in the first 20 years after the introduction of whole-cell vaccines. Microbiology (Reading, Engl.) 148(Pt 7), 2011–2018 (2002).
  • Godfroid F, Denoël P, Poolman J. Are vaccination programs and isolate polymorphism linked to pertussis re-emergence? Expert Rev. Vaccines 4(5), 757–778 (2005).
  • Kallonen T, He Q. Bordetella pertussis strain variation and evolution postvaccination. Expert Rev. Vaccines 8(7), 863–875 (2009).
  • Bouchez V, Brun D, Cantinelli T, Dore G, Njamkepo E, Guiso N. First report and detailed characterization of B. pertussis isolates not expressing pertussis toxin or pertactin. Vaccine 27(43), 6034–6041 (2009).
  • Njamkepo E, Cantinelli T, Guigon G, Guiso N. Genomic analysis and comparison of Bordetella pertussis isolates circulating in low and high vaccine coverage areas. Microbes Infect. 10(14–15), 1582–1586 (2008).
  • Otsuka N, Han HJ, Toyoizumi-Ajisaka H et al. Prevalence and genetic characterization of pertactin-deficient Bordetella pertussis in Japan. PLoS ONE 7(2), e31985 (2012).
  • Plotkin SA. Vaccines: correlates of vaccine-induced immunity. Clin. Infect. Dis. 47(3), 401–409 (2008).
  • Gustafsson L, Hessel L, Storsaeter J, Olin P. Long-term follow-up of Swedish children vaccinated with acellular pertussis vaccines at 3, 5, and 12 months of age indicates the need for a booster dose at 5 to 7 years of age. Pediatrics 118(3), 978–984 (2006).
  • Olin P, Hallander HO, Gustafsson L, Reizenstein E, Storsaeter J. How to make sense of pertussis immunogenicity data. Clin. Infect. Dis. 33(Suppl. 4), S288–S291 (2001).
  • Pebody RG, Gay NJ, Giammanco A et al. The seroepidemiology of Bordetella pertussis infection in Western Europe. Epidemiol. Infect. 133(1), 159–171 (2005).
  • Storsaeter J, Hallander HO, Gustafsson L, Olin P. Levels of antipertussis antibodies related to protection after household exposure to Bordetella pertussis. Vaccine 16(20), 1907–1916 (1998).
  • Hendrikx LH, Öztürk K, de Rond LG et al. Serum IgA responses against pertussis proteins in infected and Dutch wP or aP vaccinated children: an additional role in pertussis diagnostics. PLoS ONE 6(11), e27681 (2011).
  • Leef M, Elkins KL, Barbic J, Shahin RD. Protective immunity to Bordetella pertussis requires both B cells and CD4(+) T cells for key functions other than specific antibody production. J. Exp. Med. 191(11), 1841–1852 (2000).
  • Mahon BP, Brady MT, Mills KH. Protection against Bordetella pertussis in mice in the absence of detectable circulating antibody: implications for long-term immunity in children. J. Infect. Dis. 181(6), 2087–2091 (2000).
  • Buisman AM, de Rond CG, Oztürk K, Ten Hulscher HI, van Binnendijk RS. Long-term presence of memory B-cells specific for different vaccine components. Vaccine 28(1), 179–186 (2009).
  • Hendrikx LH, Oztürk K, de Rond LG et al. Identifying long-term memory B-cells in vaccinated children despite waning antibody levels specific for Bordetella pertussis proteins. Vaccine 29(7), 1431–1437 (2011).
  • Stenger RM, Smits M, Kuipers B et al. Impaired long-term maintenance and function of Bordetella pertussis specific B cell memory. Vaccine 28(40), 6637–6646 (2010).
  • Stenger RM, Smits M, Kuipers B, Kessen SF, Boog CJ, van Els CA. Fast, antigen-saving multiplex immunoassay to determine levels and avidity of mouse serum antibodies to pertussis, diphtheria, and tetanus antigens. Clin. Vaccine Immunol. 18(4), 595–603 (2011).
  • Ausiello CM, Urbani F, la Sala A, Lande R, Cassone A. Vaccine- and antigen-dependent type 1 and type 2 cytokine induction after primary vaccination of infants with whole-cell or acellular pertussis vaccines. Infect. Immun. 65(6), 2168–2174 (1997).
  • Mascart F, Verscheure V, Malfroot A et al. Bordetella pertussis infection in 2-month-old infants promotes type 1 T cell responses. J. Immunol. 170(3), 1504–1509 (2003).
  • Ryan M, Murphy G, Ryan E et al. Distinct T-cell subtypes induced with whole cell and acellular pertussis vaccines in children. Immunology 93(1), 1–10 (1998).
  • Vermeulen F, Verscheure V, Damis E et al. Cellular immune responses of preterm infants after vaccination with whole-cell or acellular pertussis vaccines. Clin. Vaccine Immunol. 17(2), 258–262 (2010).
  • White OJ, Rowe J, Richmond P et al. Th2-polarisation of cellular immune memory to neonatal pertussis vaccination. Vaccine 28(14), 2648–2652 (2010).
  • Nilsson L, Kjellman NI, Björkstén B. A randomized controlled trial of the effect of pertussis vaccines on atopic disease. Arch. Pediatr. Adolesc. Med. 152(8), 734–738 (1998).
  • Ryan EJ, Nilsson L, Kjellman N, Gothefors L, Mills KH. Booster immunization of children with an acellular pertussis vaccine enhances Th2 cytokine production and serum IgE responses against pertussis toxin but not against common allergens. Clin. Exp. Immunol. 121(2), 193–200 (2000).
  • White OJ, McKenna KL, Bosco A, H J van den Biggelaar A, Richmond P, Holt PG. A genomics-based approach to assessment of vaccine safety and immunogenicity in children. Vaccine 30(10), 1865–1874 (2012).
  • Rowe J, Yerkovich ST, Richmond P et al. Th2-associated local reactions to the acellular diphtheria-tetanus-pertussis vaccine in 4- to 6-year-old children. Infect. Immun. 73(12), 8130–8135 (2005).
  • Scheifele DW, Ochnio JJ, Halperin SA. Cellular immunity as a potential cause of local reactions to booster vaccination with diphtheria and tetanus toxoids and acellular pertussis antigens. Pediatr. Infect. Dis. J. 28(11), 985–989 (2009).
  • Andreasen C, Carbonetti NH. Role of neutrophils in response to Bordetella pertussis infection in mice. Infect. Immun. 77(3), 1182–1188 (2009).
  • Banus S, Stenger RM, Gremmer ER et al. The role of Toll-like receptor-4 in pertussis vaccine-induced immunity. BMC Immunol. 9, 21 (2008).
  • Higgins SC, Jarnicki AG, Lavelle EC, Mills KH. TLR4 mediates vaccine-induced protective cellular immunity to Bordetella pertussis: role of IL-17-producing T cells. J. Immunol. 177(11), 7980–7989 (2006).
  • Fedele G, Bianco M, Debrie AS, Locht C, Ausiello CM. 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 (2011).
  • Stenger RM, Poelen MC, Moret EE et al. Immunodominance in mouse and human CD4+ T-cell responses specific for the Bordetella pertussis virulence factor P.69 pertactin. Infect. Immun. 77(2), 896–903 (2009).
  • Panum Pl. Boebachtungen uber das maserncontagium. Vichows Archives 1847(1), 492–503.
  • Paul JR, Riordan JT, Melnick JL. Antibodies to three different antigenic types of poliomyelitis virus in sera from North Alaskan Eskimos. Am. J. Hyg. 54(2), 275–285 (1951).
  • Sawyer WA. Persistence of yellow fever immunity. J. Prevent. Med. 5, 413–428 (1930).
  • De Greeff SC, de Melker HE, van Gageldonk PG et al. Seroprevalence of pertussis in The Netherlands: evidence for increased circulation of Bordetella pertussis. PLoS ONE 5(12), e14183 (2010).
  • Greco D, Salmaso S, Mastrantonio P et al. A controlled trial of two acellular vaccines and one whole-cell vaccine against pertussis. Progetto Pertosse Working Group. N. Engl. J. Med. 334(6), 341–348 (1996).
  • Gustafsson L, Hallander HO, Olin P, Reizenstein E, Storsaeter J. 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 (1996).
  • Hendrikx LH, de Rond LG, Oztürk K et al. Impact of infant and preschool pertussis vaccinations on memory B-cell responses in children at 4 years of age. Vaccine 29(34), 5725–5730 (2011).
  • Simondon F, Yam A, Gagnepain JY, Wassilak S, Danve B, Cadoz M. Comparative safety and immunogenicity of an acellular versus whole-cell pertussis component of diphtheria-tetanus-pertussis vaccines in Senegalese infants. Eur. J. Clin. Microbiol. Infect. Dis. 15(12), 927–932 (1996).
  • Storsaeter J, Hallander HO, 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(25–26), 3542–3549 (2003).
  • Hendrikx LH, Felderhof MK, Oztürk K et al. Enhanced memory B-cell immune responses after a second acellular pertussis booster vaccination in children 9 years of age. Vaccine 30(1), 51–58 (2011).
  • Luijkx TA, van Gaans-van den Brink JA, van Dijken HH, van den Dobbelsteen GP, van Els CA. Hyperproliferation of B cells specific for a weakly immunogenic PorA in a meningococcal vaccine model. Clin. Vaccine Immunol. 15(10), 1598–1605 (2008).
  • Smits K, Smet J, Van Twillert I et al. Evaluation of Bordetella pertussis-specific immune responses after infection or after different vaccination programs in the framework of the FP7 Child-INNOVAC program. Presented at: 9th International Bordetella Symposium, Baltimore, MD, USA, 30 September–3 October 2010.
  • Eskola J. Analysis of Haemophilus influenzae type B conjugate and diphtheria-tetanus-pertussis combination vaccines. J. Infect. Dis. 174(Suppl. 3), S302–S305 (1996).
  • McGuirk P, Mills KH. Direct anti-inflammatory effect of a bacterial virulence factor: IL-10-dependent suppression of IL-12 production by filamentous hemagglutinin from Bordetella pertussis. Eur. J. Immunol. 30(2), 415–422 (2000).
  • McGuirk P, McCann C, Mills KH. Pathogen-specific T regulatory 1 cells induced in the respiratory tract by a bacterial molecule that stimulates interleukin 10 production by dendritic cells: a novel strategy for evasion of protective T helper type 1 responses by Bordetella pertussis. J. Exp. Med. 195(2), 221–231 (2002).
  • de Gouw D, Diavatopoulos DA, Bootsma HJ, Hermans PW, Mooi FR. Pertussis: a matter of immune modulation. FEMS Microbiol. Rev. 35(3), 441–474 (2011).
  • Carbonetti NH. Immunomodulation in the pathogenesis of Bordetella pertussis infection and disease. Curr. Opin. Pharmacol. 7(3), 272–278 (2007).
  • Mattoo S, Cherry JD. Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies. Clin. Microbiol. Rev. 18(2), 326–382 (2005).
  • Pichichero ME. Booster vaccinations: can immunologic memory outpace disease pathogenesis? Pediatrics 124(6), 1633–1641 (2009).
  • Hickey FB, Brereton CF, Mills KH. Adenylate cycalse toxin of Bordetella pertussis inhibits TLR-induced IRF-1 and IRF-8 activation and IL-12 production and enhances IL-10 through MAPK activation in dendritic cells. J. Leukoc. Biol. 84(1), 234–243 (2008).
  • Corbel MJ, Xing DK. Toxicity and potency evaluation of pertussis vaccines. Expert Rev. Vaccines 3(1), 89–101 (2004).
  • Elahi S, Holmstrom J, Gerdts V. The benefits of using diverse animal models for studying pertussis. Trends Microbiol. 15(10), 462–468 (2007).
  • Culotta CS, Harvey DF, Gordon EF. Whooping-cough: II. Experimental study. J.Pediatr. 6, 743–752 (1935).
  • Elahi S, Brownlie R, Korzeniowski J et al. Infection of newborn piglets with Bordetella pertussis: a new model for pertussis. Infect. Immun. 73(6), 3636–3645 (2005).
  • Elahi S, Buchanan RM, Attah-Poku S, Townsend HG, Babiuk LA, Gerdts V. The host defense peptide β-defensin 1 confers protection against Bordetella pertussis in newborn piglets. Infect. Immun. 74(4), 2338–2352 (2006).
  • Feunou PF, Kammoun H, Debrie AS, Mielcarek N, Locht C. Long-term immunity against pertussis induced by a single nasal administration of live attenuated B. pertussis BPZE1. Vaccine 28(43), 7047–7053 (2010).
  • Hall E, Parton R, Wardlaw AC. Cough production, leucocytosis and serology of rats infected intrabronchially with Bordetella pertussis. J. Med. Microbiol. 40(3), 205–213 (1994).
  • Hall E, Parton R, Wardlaw AC. Differences in coughing and other responses to intrabronchial infection with Bordetella pertussis among strains of rats. Infect. Immun. 65(11), 4711–4717 (1997).
  • Hall E, Parton R, Wardlaw AC. Responses to acellular pertussis vaccines and component antigens in a coughing-rat model of pertussis. Vaccine 16(17), 1595–1603 (1998).
  • Hall E, Parton R, Wardlaw AC. Time-course of infection and responses in a coughing rat model of pertussis. J. Med. Microbiol. 48(1), 95–98 (1999).
  • Hamstra HJ, Kuipers B, Schijf-Evers D, Loggen HG, Poolman JT. The purification and protective capacity of Bordetella pertussis outer membrane proteins. Vaccine 13(8), 747–752 (1995).
  • Huang CC, Chen PM, Kuo JK et al. Experimental whooping cough. N. Engl. J. Med. 266, 105–111 (1962).
  • Komatsu E, Yamaguchi F, Abe A, Weiss AA, Watanabe M. 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 (2010).
  • Parton R, Hall E, Wardlaw AC. Responses to Bordetella pertussis mutant strains and to vaccination in the coughing rat model of pertussis. J. Med. Microbiol. 40(5), 307–312 (1994).
  • Rich AR, Long PH, Brown JH, Bliss EA, Holt LE Jr. Experiments upon the cause of whooping cough. Science 76(1971), 330–331 (1932).
  • Shibley GS, Hoelscher H. Studies on whooping cough: i. type-specific (s) and dissociation (R) forms of hemophilus pertussis. J. Exp. Med. 60(4), 403–418 (1934).
  • Stanbridge TN, Preston NW. Experimental pertussis infection in the vaccinated and unvaccinated marmoset: similarities to natural infection in the child. J. Clin. Pathol. 25(6), 551 (1972).
  • van der Ark A, van Straaten-van de Kappelle I, Akkermans A, Hendriksen C, van de Donk H. Development of pertussis serological potency test. Serological assessment of antibody response induced by whole cell vaccine as an alternative to mouse protection in an intracerebral challenge model. Biologicals 22(3), 233–242 (1994).
  • van der Ark A, van Straaten-van de Kappelle I, Olander RM et al. The Pertussis serological potency test. Collaborative study to evaluate replacement of the mouse protection test. Biologicals 28(2), 105–118 (2000).
  • Caro V, Bouchez V, Guiso N. Is the Sequenced Bordetella pertussis strain Tohama I representative of the species? J. Clin. Microbiol. 46(6), 2125–2128 (2008).
  • Fry NK, Duncan J, Vaghji L, George RC, Harrison TG. Antimicrobial susceptibility testing of historical and recent clinical isolates of Bordetella pertussis in the United Kingdom using the Etest method. Eur. J. Clin. Microbiol. Infect. Dis. 29(9), 1183–1185 (2010).
  • Gaillard ME, Bottero D, Castuma CE, Basile LA, Hozbor D. Laboratory adaptation of Bordetella pertussis is associated with the loss of type three secretion system functionality. Infect. Immun. 79(9), 3677–3682 (2011).
  • Xing DK, Corbel MJ, Dobbelaer R, Knezevic I. WHO working group on standardisation and control of acellular pertussis vaccines–report of a meeting held on 16–17 March 2006, St. Albans, United Kingdom. Vaccine 25(15), 2749–2757 (2007).
  • Van Der Ark A, Kuipers B, Van Amerongen G et al. Infection procedure determines disease and immunity induced by B. pertussis strain variants in the coughing rat model. (2010). Presented at: 9th International Bordetella Symposium, Baltimore, MD, USA, 30 September – 3 October 2010.
  • Fennelly NK, Sisti F, Higgins SC et al. Bordetella pertussis expresses a functional type III secretion system that subverts protective innate and adaptive immune responses. Infect. Immun. 76(3), 1257–1266 (2008).
  • Heikkinen E, Xing DK, Olander RM et al. Bordetella pertussis isolates in Finland: serotype and fimbrial expression. BMC Microbiol. 8, 162 (2008).
  • King AJ, van Gorkom T, Pennings JL et al. Comparative genomic profiling of Dutch clinical Bordetella pertussis isolates using DNA microarrays: identification of genes absent from epidemic strains. BMC Genomics 9, 311 (2008).
  • van Gent M, Bart MJ, van der Heide HG et al. SNP-based typing: a useful tool to study Bordetella pertussis populations. PLoS ONE 6(5), e20340 (2011).
  • Warfel JM, Beren J, Kelly VK, Lee G, Merkel TJ. Nonhuman primate model of pertussis. Infect. Immun. 80(4), 1530–1536 (2012).
  • Berry MP, Graham CM, McNab FW et al. An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 466(7309), 973–977 (2010).
  • Nakaya HI, Wrammert J, Lee EK et al. Systems biology of vaccination for seasonal influenza in humans. Nat. Immunol. 12(8), 786–795 (2011).
  • Querec TD, Akondy RS, Lee EK et al. Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nat. Immunol. 10(1), 116–125 (2009).
  • Pulendran B. Learning immunology from the yellow fever vaccine: innate immunity to systems vaccinology. Nat. Rev. Immunol. 9(10), 741–747 (2009).
  • Feunou PF, Bertout J, Locht C. T- and B-cell-mediated protection induced by novel, live attenuated pertussis vaccine in mice. Cross protection against parapertussis. PLoS ONE 5(4), e10178 (2010).
  • Mielcarek N, Debrie AS, Mahieux S, Locht C. Dose response of attenuated Bordetella pertussis BPZE1-induced protection in mice. Clin. Vaccine Immunol. 17(3), 317–324 (2010).
  • Mielcarek N, Debrie AS, Raze D et al. Live attenuated B. pertussis as a single-dose nasal vaccine against whooping cough. PLoS Pathog. 2(7), e65 (2006).
  • Skerry CM, Mahon BP. A live, attenuated Bordetella pertussis vaccine provides long-term protection against virulent challenge in a murine model. Clin. Vaccine Immunol. 18(2), 187–193 (2011).
  • Asensio CJ, Gaillard ME, Moreno G et al. Outer membrane vesicles obtained from Bordetella pertussis Tohama expressing the lipid A deacylase PagL as a novel acellular vaccine candidate. Vaccine 29(8), 1649–1656 (2011).
  • Hozbor D, Rodriguez ME, Fernández J, Lagares A, Guiso N, Yantorno O. Release of outer membrane vesicles from Bordetella pertussis. Curr. Microbiol. 38(5), 273–278 (1999).
  • Roberts R, Moreno G, Bottero D et al. Outer membrane vesicles as acellular vaccine against pertussis. Vaccine 26(36), 4639–4646 (2008).

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