Protocol for Pertussis Immunisation and Food Allergy (PIFA): a case-control study of the association between pertussis vaccination in infancy and the risk of IgE-mediated food allergy among Australian children

Marie J Estcourt, Julie A Marsh, Dianne E Campbell, Michael S Gold, Katrina J Allen, Peter Richmond, Claire S Waddington, Thomas L Snelling, Marie J Estcourt, Julie A Marsh, Dianne E Campbell, Michael S Gold, Katrina J Allen, Peter Richmond, Claire S Waddington, Thomas L Snelling

Abstract

Introduction: Atopic diseases, including food allergy, have become a predominant cause of chronic illness among children in developed countries. In Australia, a rise in hospitalisations among infants coded as anaphylaxis to foods coincided with the replacement of whole-cell pertussis (wP) vaccine with subunit acellular pertussis (aP) vaccine on the national immunisation schedule in the late 1990s. Atopy is characterised by a tendency to mount T helper type 2 (Th2) responses to otherwise innocuous environmental antigens. Compared with infants who receive aP as their first pertussis vaccine, those who receive wP appear less likely to mount Th2 immune responses to either vaccine or extraneous antigens. We therefore speculate that removal of wP from the vaccine schedule contributed to the observed rise in IgE-mediated food allergy among Australian infants.

Methods and analysis: This is a retrospective individually matched case-control study among a cohort of Australian children born from 1997 to 1999, the period of transition from wP to aP vaccines; we include in the cohort children listed on Australia's comprehensive population-based immunisation register as having received a first dose of either pertussis vaccine by 16 weeks old. 500 cohort children diagnosed as having IgE-mediated food allergy at specialist allergy clinics will be included as cases. Controls matched to each case by date and jurisdiction of birth and regional socioeconomic index will be sampled from the immunisation register. Conditional logistic regression will be used to estimate OR (±95% CI) of receipt of wP (vs aP) as the first vaccine dose among cases compared with controls.

Ethics and dissemination: The study is approved by all relevant human research ethics committees: Western Australia Child and Adolescent Health Services (2015052EP), Women's and Children's Hospital (HREC/15/WCHN/162), Royal Children's Hospital (35230A) and Sydney Children's Hospital Network (HREC/15/SCHN/405). Outcomes will be disseminated through publication and scientific presentation.

Trial registration number: NCT02490007.

Keywords: epidemiology; food allergy; immunology; pertussis; vaccines.

Conflict of interest statement

Competing interests: None declared.

© Article author(s) (or their employer(s) unless otherwise stated in the text of the article) 2018. All rights reserved. No commercial use is permitted unless otherwise expressly granted.

References

    1. Asher MI, Montefort S, Björkstén B, et al. . Worldwide time trends in the prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and eczema in childhood: ISAAC Phases One and Three repeat multicountry cross-sectional surveys. Lancet 2006;368:733–43. 10.1016/S0140-6736(06)69283-0
    1. Robertson CF, Roberts MF, Kappers JH. Asthma prevalence in Melbourne schoolchildren: have we reached the peak? Med J Aust 2004;180:273–6.
    1. Prescott S, Allen KJ. Food allergy: riding the second wave of the allergy epidemic. Pediatr Allergy Immunol 2011;22:155–60. 10.1111/j.1399-3038.2011.01145.x
    1. Mullins RJ. Paediatric food allergy trends in a community-based specialist allergy practice, 1995-2006. Med J Aust 2007;186:618–21.
    1. Mullins RJ, Wainstein BK, Barnes EH, et al. . Increases in anaphylaxis fatalities in Australia from 1997 to 2013. Clin Exp Allergy 2016;46:1099–110. 10.1111/cea.12748
    1. Osborne NJ, Koplin JJ, Martin PE, et al. . Prevalence of challenge-proven IgE-mediated food allergy using population-based sampling and predetermined challenge criteria in infants. J Allergy Clin Immunol 2011;127:668–76. 10.1016/j.jaci.2011.01.039
    1. Venter C, Pereira B, Grundy J, et al. . Prevalence of sensitization reported and objectively assessed food hypersensitivity amongst six-year-old children: a population-based study. Pediatr Allergy Immunol 2006;17:356–63. 10.1111/j.1399-3038.2006.00428.x
    1. Lin RY, Anderson AS, Shah SN, et al. . Increasing anaphylaxis hospitalizations in the first 2 decades of life: New York State, 1990 -2006. Ann Allergy Asthma Immunol 2008;101:387–93. 10.1016/S1081-1206(10)60315-8
    1. Ross MP, Ferguson M, Street D, et al. . Analysis of food-allergic and anaphylactic events in the National Electronic Injury Surveillance System. J Allergy Clin Immunol 2008;121:166–71. 10.1016/j.jaci.2007.10.012
    1. Strachan DP. Family size, infection and atopy: the first decade of the "hygiene hypothesis". Thorax 2000;55 Suppl 1(Suppl 1):2S–10. 10.1136/thorax.55.suppl_1.S2
    1. Allen KJ, Martin PE. Clinical aspects of pediatric food allergy and failed oral immune tolerance. J Clin Gastroenterol 2010;44:391–401. 10.1097/MCG.0b013e3181d7760b
    1. Torvaldsen S, Hull BP, McIntyre PB. Using the Australian Childhood Immunisation Register to track the transition from whole-cell to acellular pertussis vaccines. Commun Dis Intell Q Rep 2002;26:581–3.
    1. Coffman RL, Seymour BW, Lebman DA, et al. . The role of helper T cell products in mouse B cell differentiation and isotype regulation. Immunol Rev 1988;102:5–28. 10.1111/j.1600-065X.1988.tb00739.x
    1. West CE, Videky DJ, Prescott SL. Role of diet in the development of immune tolerance in the context of allergic disease. Curr Opin Pediatr 2010;22:635–41. 10.1097/MOP.0b013e32833d96ef
    1. Mills KH, Ryan M, Mcguirk P, et al. . The immunology of bordetella pertussis infection. Biologicals 1999;27:77 10.1006/biol.1999.0183
    1. Barlow WE, Davis RL, Glasser JW, et al. . The risk of seizures after receipt of whole-cell pertussis or measles, mumps, and rubella vaccine. N Engl J Med 2001;345:656–61. 10.1056/NEJMoa003077
    1. 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 2010;5:e10178 10.1371/journal.pone.0010178
    1. Mills KH, Ryan M, Ryan E, et al. . 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 1998;66:594–602.
    1. Sheridan SL, Ware RS, Grimwood K, et al. . Number and order of whole cell pertussis vaccines in infancy and disease protection. JAMA 2012;308:454–6. 10.1001/jama.2012.6364
    1. Fulton TR, Phadke VK, Orenstein WA, et al. . Protective Effect of Contemporary Pertussis Vaccines: A Systematic Review and Meta-analysis. Clin Infect Dis 2016;62:1100–10. 10.1093/cid/ciw051
    1. Dannemann A, van Ree R, Kulig M, et al. . Specific IgE and IgG4 immune responses to tetanus and diphtheria toxoid in atopic and nonatopic children during the first two years of life. Int Arch Allergy Immunol 1996;111:262–7. 10.1159/000237376
    1. Rowe J, Macaubas C, Monger T, et al. . Heterogeneity in diphtheria-tetanus-acellular pertussis vaccine-specific cellular immunity during infancy: relationship to variations in the kinetics of postnatal maturation of systemic th1 function. J Infect Dis 2001;184:80–8. 10.1086/320996
    1. Bancroft T, Dillon MB, da Silva Antunes R, et al. . Th1 versus Th2 T cell polarization by whole-cell and acellular childhood pertussis vaccines persists upon re-immunization in adolescence and adulthood. Cell Immunol 2016. 304:35–43. 10.1016/j.cellimm.2016.05.002
    1. Mascart F, Hainaut M, Peltier A, et al. . Modulation of the infant immune responses by the first pertussis vaccine administrations. Vaccine 2007;25:391–8. 10.1016/j.vaccine.2006.06.046
    1. Holt PG, Rowe J, Kusel M, et al. . Toward improved prediction of risk for atopy and asthma among preschoolers: a prospective cohort study. J Allergy Clin Immunol 2010;125:653–9. 10.1016/j.jaci.2009.12.018
    1. Sly PD, Boner AL, Björksten B, et al. . Early identification of atopy in the prediction of persistent asthma in children. Lancet 2008;372:1100–6. 10.1016/S0140-6736(08)61451-8
    1. Quinn P, Gold M, Royle J, et al. . Recurrence of extensive injection site reactions following DTPa or dTpa vaccine in children 4-6 years old. Vaccine 2011;29:4230–7. 10.1016/j.vaccine.2011.03.088
    1. 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 2005;73:8130–5. 10.1128/IAI.73.12.8130-8135.2005
    1. Ryan EJ, Nilsson L, Kjellman N, et al. . 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 2000;121:193–200. 10.1046/j.1365-2249.2000.01306.x
    1. Zhang L, Prietsch SO, Axelsson I, et al. . Acellular vaccines for preventing whooping cough in children. Cochrane Database Syst Rev 2014:CD001478 10.1002/14651858.CD001478.pub6
    1. Holt PG, Snelling T, White OJ, et al. . Transiently increased IgE responses in infants and pre-schoolers receiving only acellular Diphtheria-Pertussis-Tetanus (DTaP) vaccines compared to those initially receiving at least one dose of cellular vaccine (DTwP) - Immunological curiosity or canary in the mine? Vaccine 2016;34:4257–62. 10.1016/j.vaccine.2016.05.048
    1. Kiraly N, Koplin JJ, Crawford NW, et al. . Timing of routine infant vaccinations and risk of food allergy and eczema at one year of age. Allergy 2016;71:541–9. 10.1111/all.12830
    1. Nilsson L, Kjellman NI, Björkstén B. A randomized controlled trial of the effect of pertussis vaccines on atopic disease. Arch Pediatr Adolesc Med 1998;152:734–8. 10.1001/archpedi.152.8.734
    1. Venter C, Stowe J, Andrews NJ, et al. . No association between atopic outcomes and type of pertussis vaccine given in children born on the Isle of Wight 2001-2002. J Allergy Clin Immunol Pract 2016;4:1248–50. 10.1016/j.jaip.2016.06.005
    1. Sporik R, Hill DJ, Hosking CS. Specificity of allergen skin testing in predicting positive open food challenges to milk, egg and peanut in children. Clin Exp Allergy 2000;30:1541–6. 10.1046/j.1365-2222.2000.00928.x
    1. Sampson HA. Update on food allergy. J Allergy Clin Immunol 2004;113:805–19. quiz 20 10.1016/j.jaci.2004.03.014
    1. Barlow WE, Ichikawa L, Rosner D, et al. . Analysis of case-cohort designs. J Clin Epidemiol 1999;52:1165–72. 10.1016/S0895-4356(99)00102-X
    1. Lowe AJ, Hosking CS, Bennett CM, et al. . Skin prick test can identify eczematous infants at risk of asthma and allergic rhinitis. Clin Exp Allergy 2007;37:1624–31. 10.1111/j.1365-2222.2007.02822.x
    1. Kjaer HF, Eller E, Andersen KE, et al. . The association between early sensitization patterns and subsequent allergic disease. The DARC birth cohort study. Pediatr Allergy Immunol 2009;20:726–34. 10.1111/j.1399-3038.2009.00862.x
    1. Sharp SJ, Poulaliou M, Thompson SG, et al. . A review of published analyses of case-cohort studies and recommendations for future reporting. PLoS One 2014;9:e101176 10.1371/journal.pone.0101176
    1. Hull BP, McIntyre PB. A re-evaluation of immunisation coverage estimates from the Australian Childhood Immunisation Register. Commun Dis Intell 2000;24:161–4.

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