Pertussis Infection and Vaccines pp 99-113 | Cite as
Human Immune Responses to Pertussis Vaccines
- 2 Citations
- 1 Mentions
- 918 Downloads
Abstract
Pertussis still represents a major cause of morbidity and mortality worldwide. Although vaccination is the most powerful tool in preventing pertussis and despite nearly 70 years of universal childhood vaccination, incidence of the disease has been rising in the last two decades in countries with high vaccination coverage. Two types of vaccines are commercially available against pertussis: whole-cell pertussis vaccines (wPVs) introduced in the 1940s and still in use especially in low and middle-income countries; less reactogenic acellular pertussis vaccines (aPVs), licensed since the mid-1990s.
In the last years, studies on pertussis vaccination have highlighted significant gaps and major differences between the two types of vaccines in the induction of protective anti-pertussis immunity in humans. This chapter will discuss the responses of the immune system to wPVs and aPVs, with the aim to enlighten critical points needing further efforts to reach a good level of protection in vaccinated individuals.
Keywords
Anti-pertussis immunity Bordetella pertussis (Bp) Immunization strategies Mechanisms of protection Pertussis vaccinesReferences
- Aase A, Herstad TK, Jørgensen SB, Leegaard TM, Berbers G, Steinbakk M, Aaberge I (2014) Anti-pertussis antibody kinetics following DTaP-IPV booster vaccination in Norwegian children 7-8 years of age. Vaccine 32(45):5931–5936PubMedGoogle Scholar
- Abu Raya B, Bamberger E, Almog M, Peri R, Srugo I, Kessel A (2015) Immunization of pregnant women against pertussis: the effect of timing on antibody avidity. Vaccine 33:1948–1952PubMedGoogle Scholar
- Abu-Raya B, Edwards KM, Scheifele DW, Halperin SA (2017) Pertussis and influenza immunisation during pregnancy: a land- scape review. Lancet Infect Dis 17(7):e209–e222PubMedGoogle Scholar
- Acosta AM, DeBolt C, Tasslimi A, Lewis M, Stewart LK, Misegades LK, Messonnier NE, Clark TA, Martin SW, Patel M (2015) Tdap vaccine effectiveness in adolescents during the 2012 Washington State pertussis epidemic. Pediatrics 135(6):981–989. https://doi.org/10.1542/peds.2014-3358 CrossRefPubMedPubMedCentralGoogle Scholar
- Ad Hoc Group for the Study of Pertussis Vaccines (1988) Placebo-controlled trial of two acellular pertussis vaccines in Sweden--protective efficacy and adverse events. Lancet 1(8592):955–960Google Scholar
- Althouse BM, Scarpino SV (2015) Asymptomatic transmission and the resurgence of Bordetella pertussis. BMC Med 13:146–158. https://doi.org/10.1186/s12916-015-0382-8 CrossRefPubMedPubMedCentralGoogle Scholar
- Amirthalingam G, Andrews N, Campbell H, Ribeiro S, Kara E, Donegan K, Fry NK, Miller E, Ramsay M (2014) Effectiveness of maternal pertussis vaccination in England: an observational study. Lancet 384(9953):1521–1528. https://doi.org/10.1016/S0140-6736(14)60686-60683 CrossRefPubMedGoogle Scholar
- Ausiello CM, Urbani F, la Sala A, Lande R, Cassone A (1997) 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):2168–2174PubMedPubMedCentralGoogle Scholar
- Ausiello CM, Lande R, Urbani F, la Sala A, Stefanelli P, Salmaso S, Mastrantonio P, Cassone A (1999) Cell-mediated immune responses in four-year-old children after primary immunization with acellular pertussis vaccines. Infect Immun 67:4064–4071PubMedPubMedCentralGoogle Scholar
- Bancroft T, Dillon MB, da Silva AR, Paul S, Peters B, Crotty S, Lindestam Arlehamn CS, Sette A (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 304–305:35–43PubMedPubMedCentralGoogle Scholar
- Baxter R, Barlett J, Fireman B, Lewis E, Klein NP (2017) Effectiveness of vaccination during pregnancy to prevent infant pertussis. Pediatrics 139(5):pii: e20164091. https://doi.org/10.1542/peds.2016-4091 CrossRefGoogle Scholar
- Bentebibel SE, Lopez S, Obermoser G, Schmitt N, Mueller C, Harrod C, Flano E, Mejias A, Albrecht RA, Blankenship D, Xu H, Pascual V, Banchereau J, Garcia-Sastre A, Palucka AK, Ramilo O, Ueno H (2013) Induction of ICOS+CXCR3+CXCR5+ TH cells correlates with antibody responses to influenza vaccination. Sci Transl Med 5(176):176ra32. https://doi.org/10.1126/scitranslmed.3005191 CrossRefPubMedPubMedCentralGoogle Scholar
- Black S (1997) Epidemiology of pertussis. Pediatr Infect Dis J 16(Supplement):S85–S89PubMedGoogle Scholar
- Blain AE, Lewis M, Banerjee E, Kudish K, Liko J, McGuire S, Selvage D, Watt J, Martin SW, Skoff TH (2016) An assessment of the cocooning strategy for preventing infant pertussis- United Stated, 2011. Clin Infect Dis 63(suppl 4):S221–S226PubMedPubMedCentralGoogle Scholar
- Bordet J, Gengou O (1906) Le microbe de la coqueluche. Ann Inst Pasteur (Paris) 2:731–741Google Scholar
- Campbell H, Gupta S, Dolan G, Kapadia S, Kumar Singh A, Andrews N, Amirthalingam G (2018) Review of vaccination in pregnancy to prevent pertussis in early infancy. J Med Microbiol 67(10):1426–1456PubMedGoogle Scholar
- Campins-Martí M, Cheng HK, Forsyth K, Guiso N, Halperin S, Huang LM, Mertsola J, Oselka G, Ward J, Wirsing von König CH, Zepp F, International Consensus Group on Pertussis Immunisation International Consensus Group on Pertussis Immunisation (2001) Recommendations are needed for adolescent and adult pertussis immunization: rationale and strategies for consideration. Int Consensus Group Pertussis Immunisation Vaccine 20:641–646Google Scholar
- Carollo M, Pandolfi E, Tozzi AE, Buisman AM, Mascart F, Ausiello CM (2014) Humoral and B-cell memory responses in children five years after pertussis acellular vaccine priming. Vaccine 32(18):2093–2099. https://doi.org/10.1016/j.vaccine.2014.02.005 CrossRefPubMedGoogle Scholar
- Cassone A, Ausiello CM, Urbani F, Lande R, Giuliano M, La Sala A, Piscitelli A, Salmaso S (1997) Cell-mediated and antibody responses to Bordetella pertussis antigens in children vaccinated with acellular or whole-cell pertussis vaccines. The Progetto Pertosse-CMI Working Group. Arch Pediatr Adolesc Med 151:283–289PubMedGoogle Scholar
- Cassone A, Mastrantonio P, Ausiello CM (2000) Are only antibody levels involved in the protection against pertussis in acellular pertussis vaccine recipients? J Infect Dis 182(5):1575–1577PubMedGoogle Scholar
- Centers for Disease Control and Prevention (CDC) (2013) Updated recommendations for use of tetanus toxoid, reduced diphtheria toxoid, and acellular pertussis vaccine (Tdap) in pregnant women--Advisory Committee on Immunization Practices (ACIP), 2012. MMWR Morb Mortal Wkly Rep 62(7):131–135Google Scholar
- Cherry JD (1996) Historical review of pertussis and the classical vaccine. J Infect Dis 174:S259–S263PubMedGoogle Scholar
- Cherry JD, Brunnel P, Golden G (1988) Report of the task force on pertussis and pertussis immunization. Pediatrics 81:S933–S984Google Scholar
- Cody CL, Baraff LJ, Cherry JD, Marcy SM, Manclark CR (1981) Nature and rates of adverse reactions associated with DTP and DT immunizations in infants and children. Pediatrics 68:650–660PubMedGoogle Scholar
- Cromer BA, Goydos J, Hackell J, Mezzatesta J, Dekker C, Mortimer EA (1993) Unrecognized pertussis infection in adolescents. Am J Dis Child 147:575–577PubMedGoogle Scholar
- Crotty S (2014) Follicular helper cell differentiation, function, and roles in disease. Immunity 41:529–542PubMedPubMedCentralGoogle Scholar
- da Silva AR, Babor M, Carpenter C, Khalil N, Cortese M, Mentzer AJ, Seumois G, Petro CD, Purcell LA, Vijayanand P, Crotty S, Pulendran B, Peters B, Sette AJ (2018) Th1/Th17 polarization persists following whole-cell pertussis vaccination despite repeated acellular boosters. Clin Invest 128(9):3853–3865Google Scholar
- de Rond L, Schure RM, Öztürk K, Berbers G, Sanders E, van Twillert I, Carollo M, Mascart F, Ausiello CM, van Els CA, Smits K, Buisman AM (2015) Identification of pertussis specific effector memory T-cells in preschool children. Clin Vaccine Immunol 22:561–569PubMedPubMedCentralGoogle Scholar
- Dirix V, Verscheure V, Goetghebuer T, Hainaut M, Debrie AS, Locht C, Mascart F (2009) Cytokine and antibody profiles in 1-year-old children vaccinated with either acellular or whole-cell pertussis vaccine during infancy. Vaccine 27(43):6042–6047. https://doi.org/10.1016/j.vaccine.2009.07.075 CrossRefPubMedGoogle Scholar
- Dirix V, Verscheure V, Vermeulen F, De Schutter I, Goetghebuer T, Locht C, Mascart F (2012) Both CD4(+) and CD8(+) lymphocytes participate in the IFN-gamma response to filamentous hemagglutinin from Bordetella pertussis in infants, children, and adults. Clin Dev Immunol 2012:795958. https://doi.org/10.1155/2012/795958 CrossRefPubMedPubMedCentralGoogle Scholar
- Eberhardt CS, Blanchard-Rohner G, Lemaitre B, Boukrid M, Combecure C, Othenin-Girard V, Chilin A, Petre J, de Tejada BM, Siegrist CA (2016) Maternal immunization earlier in pregnancy maximizes antibody transfer and expected infant seropositivity against pertussis. Clin Infect Dis 62:829–836PubMedPubMedCentralGoogle Scholar
- Edelman KJ, He Q, Makinen JP, Haanpera MS, Tran Minh NN, Schuerman L, Wolter J, Mertsola JA (2004) Pertussis-specific cell-mediated and humoral immunity in adolescents 3 years after booster immunization with acellular pertussis vaccine. Clin Infect Dis 39(2):179–185PubMedGoogle Scholar
- Edelman K, He Q, Mäkinen J, Sahlberg A, Haanperä M, Schuerman L, Wolter J, Mertsola J (2007) Immunity to pertussis 5 years after booster immunization during adolescence. J Clin Infect Dis 44(10):1271–1277Google Scholar
- Edwards KM, Berbers GAM (2014) Immune responses to pertussis vaccines and disease. J Infect Dis 209:S10–S15PubMedGoogle Scholar
- Edwards KM, Meade BD, Decker MD, Reed GF, Rennels MB, Steinhoff MC, Anderson EL, Englund JA, Pichichero ME, Deloria MA (1995) Comparison of 13 acellular pertussis vaccines: overview and serologic response. Pediatrics 96(3 Pt 2):548–557PubMedGoogle Scholar
- Farooq F, Beck K, Paolino KM, Phillips R, Waters NC, Regules JA, Bergmann-Leitner ES (2016) Circulating follicular T helper cells and cytokine profile in humans following vaccination with the rVSV-ZEBOV Ebola vaccine. Sci Rep 6:27944. https://doi.org/10.1038/srep27944 CrossRefPubMedPubMedCentralGoogle Scholar
- Gangarosa EJ, Galazka AM, Wolfe CR, Phillips LM, Gangarosa RE, Miller E, Chen RT (1998) Impact of anti-vaccine movements on pertussis control: the untold story. Lancet 351:356–361PubMedGoogle Scholar
- Giuliano M, Mastrantonio P, Giammanco A, Piscitelli A, Salmaso S, Wassilak SG (1998) Antibody responses and persistence in the two years after immunization with two acellular vaccines and one whole-cell vaccine against pertussis. J Pediatr 132(6):983–988PubMedGoogle Scholar
- Gonfiantini MV, Carloni E, Gesualdo F, Pandolfi E, Agricola E, Rizzuto E, Iannazzo S, Ciofi Degli Atti ML, Villani A, Tozzi AE (2014) Epidemiology of pertussis in Italy: disease trends over the last century. Euro Surveill 19(40):20921–20929PubMedGoogle Scholar
- Greco D, Salmaso S, Mastrantonio P, Giuliano M, Tozzi AE, Anemona A, Ciofi Degli Atti ML, Giammanco A, Panei P, Blackwelder WC, Klein DL, Wassilak SG (1996) A controlled trial of two acellular vaccines and one whole-cell vaccine against pertussis. Progetto Pertosse Working Group. N Engl J Med 334(6):341–348PubMedGoogle Scholar
- Gustafsson L, Hallander HO, Olin P, Reizenstein E, Storsaeter J (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):349–355PubMedGoogle Scholar
- Hallander HO, Gustafsson L, Ljungman M, Storsaeter J (2005) Pertussis antitoxin decay after vaccination with DTPa: Response to a first booster dose 3 1/2 – 6 1/2 years after the third vaccine dose. Vaccine 23(46–47):5359–5364PubMedGoogle Scholar
- Hallander HO, Ljungman M, Storsaeter J, Gustafsson L (2009) Kinetics and sensitivity of ELISA IgG pertussis antitoxin after infection and vaccination with Bordetella pertussis in young children. APMIS 117:797–807PubMedGoogle Scholar
- Halperin SA (2001) Pertussis immunization for adolescents: what are we waiting for? Paediatr Child Health 6(4):184–186PubMedPubMedCentralGoogle Scholar
- Halperin SA, Langley JM, Ye L, MacKinnon-Cameron D, Elsherif M, Allen VM, Smith B, Halperin BA, McNeil SA, Vanderkooi OG, Dwinnell S, Wilson RD, Tapiero B, Boucher M, Le Saux N, Gruslin A, Vaudry W, Chandra S, Dobson S, Money D (2018) A randomized controlled trial of the safety and immunogenicity of tetanus, diphtheria, and acellular pertussis vaccine immunization during pregnancy and subsequent infant immune response. Clin Infect Dis 67(7):1063–1071. https://doi.org/10.1093/cid/ciy244 CrossRefPubMedGoogle Scholar
- He Q, Viljanen MK, Nikkari S, Lyytikäinen R, Mertsola J (1994) Outcomes of Bordetella pertussis infection in different age groups of an immunized population. J Infect Dis 17:873–877Google Scholar
- He Q, Tran Minh NN, Edelman K, Viljanen MK, Arvilommi H, Mertsola J (1998) Cytokine mRNA expression and proliferative responses induced by pertussis toxin, filamentous hemagglutinin, and pertactin of Bordetella pertussis in the peripheral blood mononuclear cells of infected and immunized school children and adults. Infect Immun 66:3796–3801PubMedPubMedCentralGoogle Scholar
- Healy CM, Rench MA, Swaim LS, Smith O, Sangi-Haghpeykar H, Mathis MH, Martin MD, Baker CJ (2018) Association between third-trimester Tdap immunization and neonatal pertussis antibody concentrations. JAMA 320(14):1464–1470PubMedPubMedCentralGoogle Scholar
- Heininger U, André P, Chlibek R, Kristufkova Z, Kutsar K, Mangarov A, Mészner Z, Nitsch-Osuch A, Petrović V, Prymula R, Usonis V, Zavadska D (2016) Comparative epidemiologic characteristics of pertussis in 10 Central and Eastern European Countries, 2000-2013. PLoS One 11(6):e0155949. https://doi.org/10.1371/journal.pone.0155949 CrossRefPubMedPubMedCentralGoogle Scholar
- Hendrikx LH, Oztürk K, de Rond LG, Veenhoven RH, Sanders EA, Berbers GA, Buisman AM (2011) Identifying long-term memory B-cells in vaccinated children despite waning antibody levels specific for Bordetella pertussis proteins. Vaccine 29(7):1431–1437PubMedGoogle Scholar
- Huang LM, Lee CY, Lin TY, Chen JM, Lee PI, Hsu CY (1996) Responses to primary and a booster dose of acellular, component, and whole-cell pertussis vaccines initiated at 2 months of age. Vaccine 14(9):916–922PubMedGoogle Scholar
- 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(4):724–728PubMedGoogle Scholar
- Jahnmatz M, Ljungman M, Netterlid E, Jenmalm MC, Nilsson L, Thorstensson R (2014) Pertussis-specific memory B-cell and humoral IgG responses in adolescents after a fifth consecutive dose of acellular pertussis vaccine. Clin Vaccine Immunol 21(9):1301–1308. https://doi.org/10.1128/CVI.00280-14 CrossRefPubMedPubMedCentralGoogle Scholar
- Jefferson T, Rudin M, DiPietrantonj C (2003) Systematic review of the effects of pertussis vaccines in children. Vaccine 21:2003–2014PubMedGoogle Scholar
- Kachikis A, Englund JA (2016) Maternal immunization: optimizing protection for the mother and infants. J Inf Secur 72(suppl):S83–S90Google Scholar
- Klein NP, Bartlett J, Fireman B, Rowhani-Rahbar A, Baxter R (2013) Comparative effectiveness of acellular versus whole-cell pertussis vaccines in teenagers. Pediatrics 131:e1716–e1722. https://doi.org/10.1542/peds.2012-3836 CrossRefPubMedGoogle Scholar
- Koepke R, Eickhoff JC, Ayele RA, Petit AB, Schauer SL, Hopfensperger DJ, Conway JH, Davis JP (2014) Estimating the effectiveness of tetanus-diphtheria-acellular pertussis vaccine (Tdap) for preventing pertussis: evidence of rapidly waning immunity and difference in effectiveness by Tdap brand. J Infect Dis 210:942–953PubMedGoogle Scholar
- Kumar NP, Sridhar R, Hanna LE, Banurekha VV, Nutman TB, Babu S (2014) Decreased frequencies of circulating CD4+ T follicular helper cells associated with diminished plasma IL-21 in active pulmonary tuberculosis. PLoS One 9:e111098. https://doi.org/10.1371/journal.pone.0111098 CrossRefPubMedPubMedCentralGoogle Scholar
- Lapidot R, Gill CJ (2016) The 2016 pertussis resurgence: putting together the pieces of the puzzle. Trop Dis Travel Med Vaccines 2:26. https://doi.org/10.1186/s40794-016-0043-8. eCollectionCrossRefPubMedPubMedCentralGoogle Scholar
- Le T, Cherry JD, Chang SJ, Knoll MD, Lee ML, Barenkamp S, Bernstein D, Edelman R, Edwards KM, Greenberg D, Keitel W, Treanor J, Ward JI, APERT Study (2004) Immune responses and antibody decay after immunization of adolescents and adults with an acellular pertussis vaccine: the APERT Study. J Infect Dis 190:535–544PubMedGoogle Scholar
- Locci MH-DC, Landais E, Wu J, Kroenke MA, Arlehamn CL, Su LF, Cubas R, Davis MM, Sette A, Haddad EK, International AIDS Vaccine Initiative Protocol C Principal Investigators, Poignard P, Crotty S (2013) Human circulating PD-1+CXCR3-CXCR5+ memory Tfh cells are highly functional and correlate with broadly neutralizing HIV antibody responses. Immunity 39:758–769PubMedPubMedCentralGoogle Scholar
- Long SS, Welkon CJ, Clark JL (1990) Widespread silent transmission of pertussis in families: antibody correlates of infection and symptomatology. J Infect Dis 161:480–486PubMedGoogle Scholar
- MacLennan IC, Toellner KM, Cunningham AF, Serre K, Sze DM, Zúñiga E, Cook MC, Vinuesa CG (2003) Extrafollicular antibody responses. Immunol Rev 194:8–18PubMedGoogle Scholar
- Maertens K, Hoang TH, Caboré RN, Leuridan E (2015) Avidity of maternal pertussis antibodies after vaccination during pregnancy. Vaccine 33:5489PubMedGoogle Scholar
- Marcellini V, Piano Mortari E, Fedele G, Gesualdo F, Pandolfi E, Midulla F, Leone P, Stefanelli P, Tozzi AE, Carsetti R, Pertussis Study Group (2017) Protection against pertussis in humans correlates to elevated serum antibodies and memory B cells. Front Immunol 8:1158PubMedPubMedCentralGoogle Scholar
- Mascart F, Verscheure V, Malfroot A, Hainaut M, Piérard D, Temerman S, Peltier A, Debrie AS, Levy J, Del Giudice G, Locht C (2003) Bordetella pertussis infection in 2-month-old infants promotes type 1 T cell responses. J Immunol 170:1504–1509PubMedGoogle Scholar
- Mascart F, Hainaut M, Peltier A, Verscheure V, Levy J, Locht C (2007) Modulation of the infant immune responses by the first pertussis vaccine administrations. Vaccine 25(2):391–398PubMedGoogle Scholar
- Mascart F, DIrix V, Locht C (2018) Chapter 7 The human immune responses to pertussis and pertussis vaccines. In: Rohani P, Scarpino S (eds) Pertussis: epidemiology, immunology, and evolution. Oxford University Press, OxfordGoogle Scholar
- Mertsola J, Ruuskanen O, Eerola E, Viljanen MK (1983) Intrafamilial spread of pertussis. J Pediatr 103:359–363PubMedGoogle Scholar
- Miller DL, Ross EM, Alderslade R, Bellman MH, Rawson NS (1981) Pertussis immunisation and serious acute neurological illness in children. Br Med J (Clin Res Ed) 282(6276):1595–1599Google Scholar
- Morita R, Schmitt N, Bentebibel SE, Ranganathan R, Bourdery L, Zurawski G, Foucat E, Dullaers M, Oh S, Sabzghabaei N, Lavecchio EM, Punaro M, Pascual V, Banchereau J, Ueno H (2011) Human blood CXCR5(+)CD4(+) T cells are counterparts of T follicular cells and contain specific subsets that differentially support antibody secretion. Immunity 34:108–121PubMedPubMedCentralGoogle Scholar
- Moriuchi T, Otsuka N, Hiramatsu Y, Shibayama K, Kamachi K (2017) A high seroprevalence of antibodies to pertussis toxin among Japanese adults: qualitative and quantitative analyses. PLoS One 12(7):e0181181. https://doi.org/10.1371/journal.pone.0181181 CrossRefPubMedPubMedCentralGoogle Scholar
- Nelson JD (1978) The changing epidemiology of pertussis in young infants: the role of adults as reservoirs of infection. Am J Dis Child 132:371–373PubMedGoogle Scholar
- Obeng-Adjei N, Portugal S, Tran TM, Yazew TB, Skinner J, Li S, Jain A, Felgner PL, Doumbo OK, Kayentao K, Ongoiba A, Traore B, Crompton PD (2015) Circulating Th1-cell-type Tfh cells that exhibit impaired B cell help are preferentially activated during acute malaria in children. Cell Rep 13:425–439PubMedPubMedCentralGoogle Scholar
- Palazzo R, Carollo M, Bianco M, Fedele G, Schiavoni I, Pandolfi E, Villani A, Tozzi AE, Mascart F, Ausiello CM (2016a) Persistence of T-cell immune response induced by two acellular pertussis vaccines in children five years after primary vaccination. New Microbiol 39(1):35–47PubMedGoogle Scholar
- Palazzo R, Carollo M, Fedele G, Rizzo C, Rota MC, Giammanco A, Iannazzo S, Ausiello CM (2016b) Sero-Epidemiology Working Group. Evidence of increased circulation of Bordetella pertussis in the Italian adult population from seroprevalence data (2012-2013). J Med Microbiol 65(7):649–657PubMedGoogle Scholar
- Pallikkuth S, Parmigiani A, Silva SY, George VK, Fischl M, Pahwa R, Pahwa S (2012) Impaired peripheral blood T-follicular helper cell function in HIV-infected nonresponders to the 2009 H1N1/09 vaccine. Blood 120:985–993. https://doi.org/10.1182/blood-2011-12-396648 CrossRefPubMedPubMedCentralGoogle Scholar
- Pereira A, Pietro Pereira AS, Silva CL, de Melo RG, Lebrun I, Sant’Anna OA, Tambourgi DV (2010) Antibody response from whole-cell pertussis vaccine immunized Brazilian children against different strains of Bordetella pertussis. Am J Trop Med Hyg 82:678–682PubMedPubMedCentralGoogle Scholar
- Pichichero ME (1996) Acellular pertussis vaccines. Towards an improved safety profile. Drug Saf 15(5):311–324PubMedGoogle Scholar
- Pichichero ME (2009) Booster vaccinations: can immunologic memory outpace disease pathogenesis? Pediatrics 124:1633–1641PubMedGoogle Scholar
- Plotkins SA (2013) Complex correlates of protection after vaccination. Clin Infect Dis 56:1458–1465Google Scholar
- Rieber N, Graf A, Belohradsky BH, Hartl D, Urschel S, Riffelmann M, Wirsing von König CH, Liese J (2008) Differences of humoral and cellular immune response to an acellular pertussis booster in adolescents with a whole cell or acellular primary vaccination. Vaccine 26:6929–6935PubMedGoogle Scholar
- Rieber N, Graf A, Hartl D, Urschel S, Belohradsky BH, Liese J (2011) Acellular pertussis booster in adolescents induces Th1 and memory CD8+ T cell immune response. PLoS One 6:e17271. https://doi.org/10.1371/journal.pone.0017271 CrossRefPubMedPubMedCentralGoogle Scholar
- Romanus V, Jonsell R, Bergquist SO (1987) Pertussis in Sweden after the cessation of general immunization in 1979. Pediatr Infect Dis J 6:364–371PubMedGoogle Scholar
- Roopenian DC, Akilesh S (2007) FcRn: the neonatal fc receptor comes of age. Nat Rev Immunol 7(9):715–725PubMedGoogle Scholar
- Ross PJ, Sutton CE, Higgins S, Allen AC, Walsh K, Misiak A, Lavelle EC, McLoughlin RM, Mills KH (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:e1003264PubMedPubMedCentralGoogle Scholar
- Ryan M, Murphy G, Ryan E, Nilsson L, Shackley F, Gothefors L, Oymar K, Miller E, Storsaeter J, Mills KH (1998) Distinct T-cell subtypes induced with whole cell and acellular pertussis vaccines in children. Immunology 93:1–10PubMedPubMedCentralGoogle Scholar
- Ryan EJ, Nilsson L, Kjellman N, Gothefors L, Mills KH (2000) 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):193–200PubMedPubMedCentralGoogle Scholar
- Salmaso S, Mastrantonio P, Wassilak SG, Giuliano M, Anemona A, Giammanco A, Tozzi AE, Ciofi Degli Atti ML, Greco D (1998) Persistence of protection through 33 months of age provided by immunization in infancy with two three-component acellular pertussis vaccines. Stage II Working Group. Vaccine 16(13):1270–1275PubMedGoogle Scholar
- Sato Y, Kimura M, Fukumi H (1984) Development of a pertussis component vaccine in Japan. Lancet 1:122–126PubMedGoogle Scholar
- Schure RM, Hendrikx LH, de Rond LG, Oztürk K, Sanders EA, Berbers GA, Buisman AM (2012a) T-cell responses before and after the fifth consecutive acellular pertussis vaccination in 4-year-old Dutch children. Clin Vaccine Immunol 19:1879–1886PubMedPubMedCentralGoogle Scholar
- Schure RM, de Rond L, Ozturk K, Hendrikx L, Sanders E, Berbers G, Buisman AM (2012b) Pertussis circulation has increased T-cell immunity during childhood more than a second acellular booster vaccination in Dutch children 9 years of age. PLoS One 7:e41928. https://doi.org/10.1371/journal.pone.0041928 CrossRefPubMedPubMedCentralGoogle Scholar
- Schure RM, Hendrikx LH, de Rond LG, Oztürk K, Sanders EA, Berbers GA, Buisman AM (2013) Differential T- and B-cell responses to pertussis in acellular vaccine-primed versus whole-cell vaccine-primed children 2 years after preschool acellular booster vaccination. Clin Vaccine Immunol 20(9):1388–1395PubMedPubMedCentralGoogle Scholar
- Sharma SK, Pichichero ME (2012) Functional deficits of pertussis-specific CD4+ T cells in infants compared to adults following DTaP vaccination. Clin Exp Immunol 169:281–291PubMedPubMedCentralGoogle Scholar
- Simondon F, Preziosi MP, Yam A, Kane CT, Chabirand L, Iteman I, Sanden G, Mboup S, Hoffenbach A, Knudsen K et al (1997) A randomized double-blind trial comparing a two-component acellular to a whole-cell pertussis vaccine in Senegal. Vaccine 15(15):1606–1612PubMedGoogle Scholar
- Slight SR, Rangel-Moreno J, Gopal R, Lin Y, Fallert Junecko BA, Mehra S, Selman M, Becerril-Villanueva E, Baquera-Heredia J, Pavon L, Kaushal D, Reinhart TA, Randall TD, Khader SA (2013) CXCR5+ T helper cells mediate protective immunity against tuberculosis. J Clin Invest 123:712–726PubMedPubMedCentralGoogle Scholar
- Smits K, Pottier G, Smet J, Dirix V, Vermeulen F, De Schutter I, Carollo M, Locht C, Ausiello CM, Mascart F (2013) Different T cell memory in preadolescents after whole-cell or acellular pertussis vaccination. Vaccine 32:111–118PubMedGoogle Scholar
- Spensieri F, Borgogni E, Zedda L, Bardelli M, Buricchi F, Volpini G, Fragapane E, Tavarini S, Finco O, Rappuoli R, Del Giudice G, Galli G, Castellino F (2013) Human circulating influenza-CD4+ ICOS1+IL-21+ T cells expand after vaccination, exert helper function, and predict antibody responses. Proc Natl Acad Sci U S A 110:14330–14335PubMedPubMedCentralGoogle Scholar
- Steinhoff MC, Reed GF, Decker MD, Edwards KM, Englund JA, Pichichero ME, Rennels MB, Anderson EL, Deloria MA, Meade BD (1995) A randomized comparison of reactogenicity and immunogenicity of two whole-cell pertussis vaccines. Pediatrics 96(3 Pt 2):567–570PubMedGoogle Scholar
- Storsaeter J, Hallander HO, Gustafsson L, Olin P (1998) Levels of anti-pertussis antibodies related to protection after household exposure to Bordetella pertussis. Vaccine 16:1907–1916PubMedGoogle Scholar
- Taranger J, Trollfors B, Lagergård T, Sundh V, Bryla DA, Schneerson R, Robbins JB (2000) Correlation between pertussis toxin IgG antibodies in postvaccination sera and subsequent protection against pertussis. J Infect Dis 181(3):1010–1013PubMedGoogle Scholar
- Tran Minh NN, He Q, Ramalho A, Kaufhold A, Viljanen MK, Arvilommi H, Mertsola J (1999) Acellular vaccines containing reduced quantities of pertussis antigens as a booster in adolescents. Pediatrics 104:e70PubMedGoogle Scholar
- Trollfors B, Taranger J, Lagergård T, Lind L, Sundh V, Zackrisson G, Lowe CU, Blackwelder W, Robbins JB (1995) A placebo-controlled trial of a pertussis-toxoid vaccine. N Engl J Med 333(16):1045–1050PubMedGoogle Scholar
- Ueno H (2016) T follicular helper cells in human autoimmunity. Curr Opin Immunol 43:24–31PubMedGoogle Scholar
- van der Lee S, Hendrikx LH, Sanders EAM, Berbers GAM, Buisman AM (2018a) Whole-cell or acellular pertussis primary immunizations in infancy determines adolescent cellular immune profiles. Front Immunol 9:51PubMedPubMedCentralGoogle Scholar
- van der Lee S, Sanders EAM, Berbers GAM, Buisman AM (2018b) Whole-cell or acellular pertussis vaccination in infancy determines IgG subclass profiles to DTaP booster vaccination. Vaccine 36(2):220–226PubMedGoogle Scholar
- van der Lee S, van Rooijen DM, de Zeeuw-Brouwer ML, Bogaard MJM, van Gageldonk PGM, Marinovic AB, Sanders EAM, Berbers GAM, Buisman AM (2018c) Robust humoral and cellular immune responses to pertussis in adults after a first acellular booster vaccination. Front Immunol 9:681PubMedPubMedCentralGoogle Scholar
- Van Hoek AJ, Campbell H, Amirthalingam G, Andrews N, Miller E (2013) The number of deaths among infants under oe year of age in England with pertussis: results of a capture/recapture analysis for the period 2001 to 2011. Euro Surveill 18(9):pii: 20414Google Scholar
- van Twillert I, Han WG, van Els CA (2015) Waning and aging of cellular immunity to Bordetella pertussis. Pathog Dis 73(8):ftv071PubMedPubMedCentralGoogle Scholar
- Vermeulen F, Dirix V, Verscheure V, Damis E, Vermeylen D, Locht C, Mascart F (2013) Persistence at one year of age of antigen-induced cellular immune responses in preterm infants vaccinated against whooping cough: comparison of three different vaccines and effect of a booster dose. Vaccine 31:1981–1986PubMedGoogle Scholar
- Voysey M, Kandasamy R, Yu LM, Baudin M, Sadorge C, Thomas S, John T, Pollard AJ (2016) The predicted persistence and kinetics of antibody decline 9 years after pre-school booster vaccination in UK children. Vaccine 34(35):4221–4228. https://doi.org/10.1016/j.vaccine.2016.06.051 PubMedGoogle Scholar
- Warfel JM, Merkel TJ (2013) Bordetella pertussis infection induces a mucosal IL-17 response and long-lived Th17 and Th1 immune memory cells in nonhuman primates. Mucosal Immunol 6(4):787–796PubMedGoogle 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 U S A 111:787–792. https://doi.org/10.1073/pnas.1314688110 CrossRefPubMedGoogle Scholar
- Warfel JM, Zimmerman LI, Merkel TJ (2016) Comparison of three whole-cell pertussis vaccines in the baboon model of pertussis. Clin Vaccine Immunol 23(1):47–54. https://doi.org/10.1128/CVI.00449-15 CrossRefPubMedPubMedCentralGoogle Scholar
- Weston R (2012) Whooping cough: a brief history to the 19th century. Can Bull Med Hist 29:329–349PubMedGoogle Scholar
- WHO Position paper on Vaccines against Pertussis – September 2015. www.who.int/immunization/documents/positionpapers
- Witt MA, Arias L, Katz PH, Truong ET, Witt DJ (2013) 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 56(9):1248–1254PubMedGoogle Scholar
- Zepp F, Knuf M, Habermehl P, Schmitt JH, Rebsch C, Schmidtke P, Clemens R, Slaoui M (1996) Pertussis-specific cell-mediated immunity in infants after vaccination with a tricomponent acellular pertussis vaccine. Infect Immun 64:4078–4084PubMedPubMedCentralGoogle Scholar
- Zepp F, Heininger U, Mertsola J, Bernatowska E, Guiso N, Roord J, Tozzi AE, Van Damme P (2011) Rationale for pertussis booster vaccination throughout life in Europe. Lancet Infect Dis 11:557–570PubMedGoogle Scholar