Antibody avidity to pertussis toxin after acellular pertussis vaccination and infection

References

• Elomaa A, He Q, Minh NN, et al. Pertussis before and after the introduction of acellular pertussis vaccines in Finland. Vaccine. 2009;27(40):5443–5449. doi:10.1016/j.vaccine.2009.07.010.
   PubMed Web of Science ®Google Scholar
• Mooi FR. Bordetella pertussis and vaccination: the persistence of a genetically monomorphic pathogen. Infect Genet Evol. 2010;10(1):36–49. doi:10.1016/j.meegid.2009.10.007.
   PubMed Web of Science ®Google Scholar
• He Q, Mertsola J. Factors contributing to pertussis resurgence. Future Microbiol. 2008;3(3):329–339. doi:10.2217/17460913.3.3.329.
   PubMed Web of Science ®Google Scholar
• Witt MA, Katz PH, Witt DJ. Unexpectedly limited durability of immunity following acellular pertussis vaccination in preadolescents in a North American outbreak. Clin Infect Dis. 2012;54(12):1730–1735. doi:10.1093/cid/cis287.
   PubMed Web of Science ®Google Scholar
• de Greeff SC, Mooi FR, Westerhof A, et al. Pertussis disease burden in the household: how to protect young infants. Clin Infect Dis. 2010;50(10):1339–1345. doi:10.1086/652281.
   PubMed Web of Science ®Google Scholar
• Plotkin SA. Complex correlates of protection after vaccination. Clin Infect Dis. 2013;56(10):1458–1465. doi:10.1093/cid/cit048.
   PubMed Web of Science ®Google Scholar
• Cherry JD. Pertussis: challenges today and for the future. PLoS Pathog. 2013;9(7):e1003418. doi:10.1371/journal.ppat.1003418.
   PubMed Web of Science ®Google Scholar
• Olin P, Hallander HO, Gustafsson L, et al. How to make sense of pertussis immunogenicity data. Clin Infect Dis. 2001;33(Suppl 4):288–S291. doi:10.1086/322564.
   PubMedGoogle Scholar
• Hallander HO, Ljungman M, Storsaeter J, et al. Kinetics and sensitivity of ELISA IgG pertussis antitoxin after infection and vaccination with Bordetella pertussis in young children. APMIS. 2009;117(11):797–807. doi:10.1111/j.1600-0463.2009.02530.x.
   PubMed Web of Science ®Google Scholar
• Dalby T, Petersen JW, Harboe ZB, et al. Antibody responses to pertussis toxin display different kinetics after clinical Bordetella pertussis infection than after vaccination with an acellular pertussis vaccine. J Med Microbiol. 2010;59(Pt 9):1029–1036. doi:10.1099/jmm.0.020826-0.
   PubMed Web of Science ®Google Scholar
• Ryan M, Murphy G, Ryan E, et al. Distinct T-cell subtypes induced with whole cell and acellular pertussis vaccines in children. Immunology. 1998;93(1):1–10. doi:10.1046/j.1365-2567.1998.00401.x.
   PubMed Web of Science ®Google Scholar
• Salmaso S, Mastrantonio P, Wassilak SG, et al. 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. 1998;16(13):1270–1275. doi:10.1016/S0264-410X(98)00040-1.
   PubMed Web of Science ®Google Scholar
• Ausiello CM, Lande R, Urbani F, et al. Cell-mediated immunity and antibody responses to Bordetella pertussis antigens in children with a history of pertussis infection and in recipients of an acellular pertussis vaccine. J Infect Dis. 2000;181(6):1989–1995. doi:10.1086/315509.
   PubMed Web of Science ®Google Scholar
• Liesenfeld O, Montoya JG, Kinney S, et al. Effect of testing for IgG avidity in the diagnosis of Toxoplasma gondii infection in pregnant women: experience in a US reference laboratory. J Infect Dis. 2001;183(8):1248–1253. doi:10.1086/319672.
   PubMed Web of Science ®Google Scholar
• Almanzar G, Ottensmeier B, Liese J, et al. Assessment of IgG avidity against pertussis toxin and filamentous hemagglutinin via an adapted enzyme-linked immunosorbent assay (ELISA) using ammonium thiocyanate. J Immunol Methods. 2013;387(1-2):36–42. doi:10.1016/j.jim.2012.09.008.
   PubMed Web of Science ®Google Scholar
• Denoel PA, Goldblatt D, de Vleeschauwer I, et al. Quality of the Haemophilus influenzae type b (Hib) antibody response induced by diphtheria-tetanus-acellular pertussis/Hib combination vaccines. Clin Vaccine Immunol. 2007;14(10):1362–1369. doi:10.1128/CVI.00154-07.
   PubMedGoogle Scholar
• Ahmed R, Gray D. Immunological memory and protective immunity: understanding their relation. Science. 1996;272(5258):54–60.
   PubMed Web of Science ®Google Scholar
• Goodnow CC, Vinuesa CG, Randall KL, et al. Control systems and decision making for antibody production. Nat Immunol. 2010;11(8):681–688. doi:10.1038/ni.1900.
   PubMed Web of Science ®Google Scholar
• Barkoff AM, Grondahl-Yli-Hannuksela K, Vuononvirta J, et al. Differences in avidity of IgG antibodies to pertussis toxin after acellular pertussis booster vaccination and natural infection. Vaccine. 2012;30(48):6897–6902. doi:10.1016/j.vaccine.2012.09.003.
   PubMed Web of Science ®Google Scholar
• McHeyzer-Williams MG, McLean MJ, Lalor PA, et al. Antigen-driven B cell differentiation in vivo. J Exp Med. 1993;178(1):295–307. doi:10.1084/jem.178.1.295.
   PubMed Web of Science ®Google Scholar
• Schallert N, Pihlgren M, Kovarik J, et al. Generation of adult-like antibody avidity profiles after early-life immunization with protein vaccines. Eur J Immunol. 2002;32(3):752–760. doi:10.1002/1521-4141(200203)32:3<752::AID-IMMU752>3.0.CO;2-5.
   PubMed Web of Science ®Google Scholar
• Berek C, Berger A, Apel M. Maturation of the immune response in germinal centers. Cell. 1991;67(6):1121–1129. doi:10.1016/0092-8674(91)90289-B.
   PubMed Web of Science ®Google Scholar
• Kepler TB, Perelson AS. Somatic hypermutation in B cells: an optimal control treatment. J Theor Biol. 1993;164(1):37–64. doi:10.1006/jtbi.1993.1139.
   PubMed Web of Science ®Google Scholar
• French DL, Laskov R, Scharff MD. The role of somatic hypermutation in the generation of antibody diversity. Science. 1989;244(4909):1152–1157.
   PubMed Web of Science ®Google Scholar
• Goldblatt D, Vaz AR, Miller E. Antibody avidity as a surrogate marker of successful priming by Haemophilus influenzae type b conjugate vaccines following infant immunization. J Infect Dis. 1998;177(4):1112–1115. doi:10.1086/517407.
   PubMed Web of Science ®Google Scholar
• Dorner T, Radbruch A. Antibodies and B cell memory in viral immunity. Immunity. 2007;27(3):384–392. doi:10.1016/j.immuni.2007.09.002.
   PubMed Web of Science ®Google Scholar
• Prelog M, Almanzar G, Rieber N, et al. Differences of IgG antibody avidity after an acellular pertussis (aP) booster in adolescents after a whole cell (wcP) or aP primary vaccination. Vaccine. 2013;31(2):387–393. doi:10.1016/j.vaccine.2012.10.105.
   PubMed Web of Science ®Google Scholar
• Eisen HN. Determination of antibody affinity for haptens and antigens by means of fluorescence quenching. Methods Med Res. 1964;10:115–121.
   PubMedGoogle Scholar
• Dimitrov JD, Lacroix-Desmazes S, Kaveri SV. Important parameters for evaluation of antibody avidity by immunosorbent assay. Anal Biochem. 2011;418(1):149–151. doi:10.1016/j.ab.2011.07.007.
   PubMed Web of Science ®Google Scholar
• Pullen GR, Fitzgerald MG, Hosking CS. Antibody avidity determination by ELISA using thiocyanate elution. J Immunol Methods. 1986;86(1):83–87. doi:10.1016/0022-1759(86)90268-1.
   PubMed Web of Science ®Google Scholar
• Hendrikx LH, Berbers GA, Veenhoven RH, et al. Igg responses after booster vaccination with different pertussis vaccines in Dutch children 4 years of age: effect of vaccine antigen content. Vaccine. 2009;27(47):6530–6536. doi:10.1016/j.vaccine.2009.08.052.
   PubMed Web of Science ®Google Scholar
• Moriuchi T, Otsuka N, Hiramatsu Y, et al. A high seroprevalence of antibodies to pertussis toxin among Japanese adults: qualitative and quantitative analyses. PLoS One. 2017;12(7):e0181181. doi:10.1371/journal.pone.0181181.
   PubMed Web of Science ®Google Scholar
• Hovingh ES, Kuipers B, Bonacic Marinovic AA, et al. Detection of opsonizing antibodies directed against a recently circulating Bordetella pertussis strain in paired plasma samples from symptomatic and recovered pertussis patients. Sci Rep. 2018;8(1):12039. doi:10.1038/s41598-018-30558-8.
   PubMedGoogle Scholar
• Pichichero M, Papa T, Blatter M, et al. Immune memory in children previously vaccinated with an experimental quadrivalent meningococcal polysaccharide diphtheria toxoid conjugate vaccine. Pediatr Infect Dis J. 2006;25(11):995–1000. doi:10.1097/01.inf.0000243215.46312.4a.
   PubMed Web of Science ®Google Scholar
• Pichichero ME, Voloshen T, Zajac D, et al. Avidity maturation of antibody to Haemophilus influenzae type b (Hib) after immunization with diphtheria-tetanus-acellular pertussis-hib-hepatitis B combined vaccine in infants. J Infect Dis. 1999;180(4):1390–1393. doi:10.1086/314989.
   PubMed Web of Science ®Google Scholar
• Dalby T, Seier-Petersen M, Kristiansen MP, et al. Problem solved: a modified enzyme-linked immunosorbent assay for detection of human antibodies to pertussis toxin eliminates false-positive results occurring at analysis of heat-treated sera. Diagn Microbiol Infect Dis. 2009;63(4):354–360. doi:10.1016/j.diagmicrobio.2008.12.004.
   PubMed Web of Science ®Google Scholar
• He Q, Mertsola J, Himanen JP, et al. Evaluation of pooled and individual components of Bordetella pertussis as antigens in an enzyme immunoassay for diagnosis of pertussis. Eur J Clin Microbiol Infect Dis. 1993;12(9):690–695. doi:10.1007/BF02009381.
   PubMed Web of Science ®Google Scholar
• Versteegen P, Valente Pinto M, Barkoff AM, et al. Responses to an acellular pertussis booster vaccination in children, adolescents, and young and older adults: A collaborative study in Finland, the Netherlands, and the United Kingdom. EBioMedicine. 2021;65:103247.
   PubMed Web of Science ®Google Scholar
• Reizenstein E, Hallander HO, Blackwelder WC, et al. Comparison of five calculation modes for antibody ELISA procedures using pertussis serology as a model. J Immunol Methods. 1995;183(2):279–290. doi:10.1016/0022-1759(95)00067-K.
   PubMed Web of Science ®Google Scholar
• Raya BA, Bamberger E, Almog M, et al. Immunization of pregnant women against pertussis: the effect of timing on antibody avidity. Vaccine. 2015;33(16):1948–1952. doi:10.1016/j.vaccine.2015.02.059.
   PubMed Web of Science ®Google Scholar
• Cabore RN, Maertens K, Dobly A, et al. Influence of maternal vaccination against diphtheria, tetanus, and pertussis on the avidity of infant antibody responses to a pertussis containing vaccine in Belgium. Virulence. 2017;8(7):1245–1254. doi:10.1080/21505594.2017.1296998.
   PubMed Web of Science ®Google Scholar
• Fumimoto R, Otsuka N, Sunagawa T, et al. Age-related differences in antibody avidities to pertussis toxin and filamentous hemagglutinin in a healthy Japanese population. Vaccine. 2019;37(18):2463–2469. doi:10.1016/j.vaccine.2019.03.055.
   PubMed Web of Science ®Google Scholar
• Mosley YC, Radder JE, Berndt A, et al. Genome-wide association mapping of the antibody response to diphtheria, tetanus and acellular pertussis vaccine in mice. J Infect Dis. 2017;215(3):466–474.
   PubMed Web of Science ®Google Scholar
• Ibrahim NM, El-Kady EM, Eissa SA, et al. Assessment of antibody concentration and avidity against Bordetella pertussis in a cohort of Egyptian individuals aged 1-18 years. J Adv Res. 2016;7(1):105–111. doi:10.1016/j.jare.2015.03.002.
   PubMed Web of Science ®Google Scholar
• Maertens K, Hoang THT, Cabore RN, et al. Avidity of maternal pertussis antibodies after vaccination during pregnancy. Vaccine. 2015;33(42):5489. doi:10.1016/j.vaccine.2015.05.075.
   PubMed Web of Science ®Google Scholar
• Abu-Raya B, Giles ML, Kollmann TR, et al. Profiling avidity of antibodies elicited by vaccination using enzyme-linked immunosorbent assay-based elution - insights into a novel experimental and analytical approach. Vaccine. 2020;38(34):5389–5392. doi:10.1016/j.vaccine.2020.06.060.
   PubMed Web of Science ®Google Scholar
• Barkoff AM, Knuutila A, Mertsola J, et al. Evaluation of anti-PT antibody response after pertussis vaccination and infection: The importance of both quantity and quality. Toxins (Basel). 2021;13(8):10. doi:10.3390/toxins13080508.
   Web of Science ®Google Scholar
• Kneitz RH, Schubert J, Tollmann F, et al. A new method for determination of varicella-zoster virus immunoglobulin G avidity in serum and cerebrospinal fluid. BMC Infect Dis. 2004;4(33). doi:10.1186/1471-2334-4-33.
   PubMedGoogle Scholar
• Bobic B, Klun I, Vujanic M, et al. Comparative evaluation of three commercial Toxoplasma-specific IgG antibody avidity tests and significance in different clinical settings. J Med Microbiol. 2009;58(Pt 3):358–364. doi:10.1099/jmm.0.006668-0.
   PubMed Web of Science ®Google Scholar
• Marchant A, Pihlgren M, Goetghebuer T, et al. Predominant influence of environmental determinants on the persistence and avidity maturation of antibody responses to vaccines in infants. J Infect Dis. 2006;193(11):1598–1605. doi:10.1086/503775.
   PubMed Web of Science ®Google Scholar
• Luijkx T, van Dijken H, van Els C, et al. Heterologous prime-boost strategy to overcome weak immunogenicity of two serosubtypes in hexavalent Neisseria meningitidis outer membrane vesicle vaccine. Vaccine. 2006;24(10):1569–1577. doi:10.1016/j.vaccine.2005.10.003.
   PubMed Web of Science ®Google Scholar
• Luijkx TA, Brink v-v, van Dijken HH, et al. Hyperproliferation of B cells specific for a weakly immunogenic PorA in a meningococcal vaccine model. Clin Vaccine Immunol. 2008;15(10):1598–1605. doi:10.1128/CVI.00192-08.
   PubMedGoogle Scholar
• Knuutila A, Dalby T, Barkoff AM, et al. Differences in epitope-specific antibodies to pertussis toxin after infection and acellular vaccinations. Clin Transl Immunology. 2020;9(8):e1161. doi:10.1002/cti2.1161.
   PubMed Web of Science ®Google Scholar
• Matos DC, Silva AM, Neves PC, et al. Pattern of functional antibody activity against Haemophilus influenzae type B (Hib) in infants immunized with diphtheria-tetanus-pertussis/Hib Brazilian combination vaccine. Braz J Med Biol Res. 2009;42(12):1242–1247. doi:10.1590/S0100-879X2009005000039.
   PubMed Web of Science ®Google Scholar
• Marchant A, Kollmann TR. Understanding the ontogeny of the immune system to promote immune-mediated health for life. Front Immunol. 2015;6:77.
   PubMed Web of Science ®Google Scholar
• Prince HE, Lieberman JM, Cherry JD. Age-related differences in patterns of increased Bordetella pertussis antibodies. Clin Vaccine Immunol. 2012;19(4):545–550. doi:10.1128/CVI.05725-11.
   PubMedGoogle Scholar
• Minh NNT, He Q, Ramalho A, et al. Acellular vaccines containing reduced quantities of pertussis antigens as a booster in adolescents. Pediatrics. 1999;104(6):e70. doi:10.1542/peds.104.6.e70.
   PubMed Web of Science ®Google Scholar
• Knuutila A, Versteegen P, Barkoff AM, et al. Pertussis toxin neutralizing antibody response after an acellular booster vaccination in Dutch and Finnish participants of different age groups. Emerg Microbes Infect. 2022;11(1):956–963. doi:10.1080/22221751.2022.2053364.
   PubMed Web of Science ®Google Scholar
• Versteegen P, Barkoff AM, Valente M, et al. Memory B cell activation induced by pertussis booster vaccination in four age groups of three countries. Front Immunol. 2022;13:864674. doi:10.3389/fimmu.2022.864674.
   PubMed Web of Science ®Google Scholar
• Guiso N, Berbers GA, Fry NK, et al. What to do and what not to do in serological diagnosis of pertussis: recommendations from EU reference laboratories. Eur J Clin Microbiol Infect Dis. 2011;30(3):307–312. doi:10.1007/s10096-010-1104-y.
   PubMed Web of Science ®Google Scholar