Advertisement

Prenatal and postnatal bisphenol A exposure and asthma development among inner-city children

  • Kathleen M. Donohue
    Correspondence
    Corresponding author: Kathleen M. Donohue, MD, Instructor of Clinical Medicine, Columbia University, Division of General Medicine, 622 West 168th St, PH9E Rm 105K, New York, NY 10032.
    Affiliations
    Division of Pulmonary, Allergy and Critical Care, Columbia University School of Physicians and Surgeons, New York, NY

    Columbia Center for Children's Environmental Health, Mailman School of Public Health, Columbia University, New York, NY
    Search for articles by this author
  • Rachel L. Miller
    Affiliations
    Division of Pulmonary, Allergy and Critical Care, Columbia University School of Physicians and Surgeons, New York, NY

    Columbia Center for Children's Environmental Health, Mailman School of Public Health, Columbia University, New York, NY

    Department of Environmental Health Sciences, Mailman School of Public Health, Columbia University, New York, NY

    Division of Pediatric Allergy and Immunology, Columbia University School of Physicians and Surgeons, New York, NY
    Search for articles by this author
  • Matthew S. Perzanowski
    Affiliations
    Columbia Center for Children's Environmental Health, Mailman School of Public Health, Columbia University, New York, NY

    Department of Environmental Health Sciences, Mailman School of Public Health, Columbia University, New York, NY
    Search for articles by this author
  • Allan C. Just
    Affiliations
    Columbia Center for Children's Environmental Health, Mailman School of Public Health, Columbia University, New York, NY

    Department of Environmental Health Sciences, Mailman School of Public Health, Columbia University, New York, NY
    Search for articles by this author
  • Lori A. Hoepner
    Affiliations
    Columbia Center for Children's Environmental Health, Mailman School of Public Health, Columbia University, New York, NY

    Department of Environmental Health Sciences, Mailman School of Public Health, Columbia University, New York, NY
    Search for articles by this author
  • Srikesh Arunajadai
    Affiliations
    Department of Biostatistics, Mailman School of Public Health, Columbia University, New York, NY
    Search for articles by this author
  • Stephen Canfield
    Affiliations
    Division of Pulmonary, Allergy and Critical Care, Columbia University School of Physicians and Surgeons, New York, NY
    Search for articles by this author
  • David Resnick
    Affiliations
    Division of Pediatric Allergy and Immunology, Columbia University School of Physicians and Surgeons, New York, NY
    Search for articles by this author
  • Antonia M. Calafat
    Affiliations
    Division of Laboratory Sciences, Centers for Disease Control and Prevention, Atlanta, Ga
    Search for articles by this author
  • Frederica P. Perera
    Affiliations
    Columbia Center for Children's Environmental Health, Mailman School of Public Health, Columbia University, New York, NY

    Department of Environmental Health Sciences, Mailman School of Public Health, Columbia University, New York, NY
    Search for articles by this author
  • Robin M. Whyatt
    Affiliations
    Columbia Center for Children's Environmental Health, Mailman School of Public Health, Columbia University, New York, NY

    Department of Environmental Health Sciences, Mailman School of Public Health, Columbia University, New York, NY
    Search for articles by this author

      Background

      Bisphenol A (BPA) is used widely to manufacture food container linings. Mouse models suggest exposure to BPA might increase allergic inflammation.

      Objectives

      We hypothesized that BPA exposure, as assessed based on urinary BPA concentrations, would be associated with increased odds of wheeze and asthma and increased fraction of exhaled nitric oxide (Feno) values in children.

      Methods

      The Columbia Center for Children's Environmental Health recruited pregnant women for a prospective birth cohort study (n = 568). Mothers during the third trimester and children at ages 3, 5, and 7 years provided spot urine samples. Total urinary BPA concentrations were measured by using online solid-phase extraction, high-performance liquid chromatography, isotope-dilution tandem mass spectrometry. Wheeze in the last 12 months was measured by using questionnaires at ages 5, 6, and 7 years. Asthma was determined by a physician once between ages 5 and 12 years. Feno values were measured at ages 7 to 11 years.

      Results

      Prenatal urinary BPA concentrations were associated inversely with wheeze at age 5 years (odds ratio [OR], 0.7; 95% CI, 0.5-0.9; P = .02). Urinary BPA concentrations at age 3 years were associated positively with wheeze at ages 5 years (OR, 1.4; 95% CI, 1.1-1.8; P = .02) and 6 years (OR, 1.4; 95% CI, 1.0-1.9; P = .03). BPA concentrations at age 7 years were associated with wheeze at age 7 years (OR, 1.4; 95% CI, 1.0-1.9; P = .04) and Feno values (β = 0.1; 95% CI, 0.02-0.2; P = .02). BPA concentrations at ages 3, 5, and 7 years were associated with asthma (OR, 1.5 [95% CI, 1.1-2.0], P = .005; OR, 1.4 [95% CI, 1.0-1.9], P = .03; and OR, 1.5 [95% CI, 1.0-2.1], P = .04, respectively).

      Conclusions

      This is the first report of an association between postnatal urinary BPA concentrations and asthma in children.

      Key words

      Abbreviations used:

      BPA (Bisphenol A), Feno (Fraction of exhaled nitric oxide), OR (Odds ratio), QC (Quality control)
      To read this article in full you will need to make a payment

      Subscribe:

      Subscribe to Journal of Allergy and Clinical Immunology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Vandenberg L.N.
        • Hauser R.
        • Marcus M.
        • Olea N.
        • Welshons W.V.
        Human exposure to bisphenol A (BPA).
        Reprod Toxicol. 2007; 24: 139-177
        • Wilson N.K.
        • Chuang J.C.
        • Lyu C.
        • Menton R.
        • Morgan M.K.
        Aggregate exposures of nine preschool children to persistent organic pollutants at day care and at home.
        J Expo Anal Environ Epidemiol. 2003; 13: 187-202
        • Zalko D.
        • Jacques C.
        • Duplan H.
        • Bruel S.
        • Perdu E.
        Viable skin efficiently absorbs and metabolizes bisphenol A.
        Chemosphere. 2011; 82: 424-430
        • Wilson N.K.
        • Chuang J.C.
        • Morgan M.K.
        • Lordo R.A.
        • Sheldon L.S.
        An observational study of the potential exposures of preschool children to pentachlorophenol, bisphenol-A, and nonylphenol at home and daycare.
        Environ Res. 2007; 103: 9-20
        • Morgan M.K.
        • Jones P.A.
        • Calafat A.M.
        • Ye X.
        • Croghan C.W.
        • Chuang J.C.
        • et al.
        Assessing the quantitative relationships between preschool children's exposures to bisphenol A by route and urinary biomonitoring.
        Environ Sci Technol. 2011; 45: 5309-5316
        • Wolff M.S.
        • Teitelbaum S.L.
        • Windham G.
        • Pinney S.M.
        • Britton J.A.
        • Chelimo C.
        • et al.
        Pilot study of urinary biomarkers of phytoestrogens, phthalates, and phenols in girls.
        Environ Health Perspect. 2007; 115: 116-121
        • Calafat A.M.
        • Ye X.
        • Wong L.Y.
        • Reidy J.A.
        • Needham L.L.
        Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003-2004.
        Environ Health Perspect. 2008; 116: 39-44
        • Matsumoto J.
        • Yokota H.
        • Yuasa A.
        Developmental increases in rat hepatic microsomal UDP-glucuronosyltransferase activities toward xenoestrogens and decreases during pregnancy.
        Environ Health Perspect. 2002; 110: 193-196
        • Braun J.M.
        • Kalkbrenner A.E.
        • Calafat A.M.
        • Bernert J.T.
        • Ye X.
        • Silva M.J.
        • et al.
        Variability and predictors of urinary bisphenol A concentrations during pregnancy.
        Environ Health Perspect. 2011; 119: 131-137
        • Nepomnaschy P.A.
        • Baird D.D.
        • Weinberg C.R.
        • Hoppin J.A.
        • Longnecker M.P.
        • Wilcox A.J.
        Within-person variability in urinary bisphenol A concentrations: measurements from specimens after long-term frozen storage.
        Environ Res. 2009; 109: 734-737
        • Strunk R.C.
        • Szefler S.J.
        • Phillips B.R.
        • Zeiger R.S.
        • Chinchilli V.M.
        • Larsen G.
        • et al.
        Relationship of exhaled nitric oxide to clinical and inflammatory markers of persistent asthma in children.
        J Allergy Clin Immunol. 2003; 112: 883-892
        • Lee M.H.
        • Chung S.W.
        • Kang B.Y.
        • Park J.
        • Lee C.H.
        • Hwang S.Y.
        • et al.
        Enhanced interleukin-4 production in CD4+ T cells and elevated immunoglobulin E levels in antigen-primed mice by bisphenol A and nonylphenol, endocrine disruptors: involvement of nuclear factor-AT and Ca2+.
        Immunology. 2003; 109: 76-86
        • Tian X.
        • Takamoto M.
        • Sugane K.
        Bisphenol A promotes IL-4 production by Th2 cells.
        Int Arch Allergy Immunol. 2003; 132: 240-247
        • Yan H.
        • Takamoto M.
        • Sugane K.
        Exposure to Bisphenol A prenatally or in adulthood promotes T(H)2 cytokine production associated with reduction of CD4CD25 regulatory T cells.
        Environ Health Perspect. 2008; 116: 514-519
        • Sawai C.
        • Anderson K.
        • Walser-Kuntz D.
        Effect of bisphenol A on murine immune function: modulation of interferon-gamma, IgG2a, and disease symptoms in NZB X NZW F1 mice.
        Environ Health Perspect. 2003; 111: 1883-1887
        • Hannu T.
        • Frilander H.
        • Kauppi P.
        • Kuuliala O.
        • Alanko K.
        IgE-mediated occupational asthma from epoxy resin.
        Int Arch Allergy Immunol. 2009; 148: 41-44
        • Kwak E.S.
        • Just A.
        • Whyatt R.
        • Miller R.L.
        Phthalates, pesticides, and bisphenol-A exposure and the development of nonoccupational asthma and allergies: how valid are the links?.
        Open Allergy J. 2009; 2: 45-50
        • Spanier A.J.
        • Kahn R.S.
        • Kunselman A.R.
        • Hornung R.
        • Xu Y.
        • Calafat A.M.
        • et al.
        Prenatal exposure to bisphenol A and child wheeze from birth to three years.
        Environ Health Perspect. 2012; 120: 916-920
        • Perera F.P.
        • Rauh V.
        • Tsai W.Y.
        • Kinney P.
        • Camann D.
        • Barr D.
        • et al.
        Effects of transplacental exposure to environmental pollutants on birth outcomes in a multiethnic population.
        Environ Health Perspect. 2003; 111: 201-205
        • Whyatt R.M.
        • Barr D.B.
        • Camann D.E.
        • Kinney P.L.
        • Barr J.R.
        • Andrews H.F.
        • et al.
        Contemporary-use pesticides in personal air samples during pregnancy and blood samples at delivery among urban minority mothers and newborns.
        Environ Health Perspect. 2003; 111: 749-756
        • Caudill S.P.
        • Schleicher R.L.
        • Pirkle J.L.
        Multi-rule quality control for the age-related eye disease study.
        Stat Med. 2008; 27: 4094-4106
        • Richardson D.B.
        • Ciampi A.
        Effects of exposure measurement error when an exposure variable is constrained by a lower limit.
        Am J Epidemiol. 2003; 157: 355-363
        • Asher M.I.
        • Keil U.
        • Anderson H.R.
        • Beasley R.
        • Crane J.
        • Martinez F.
        • et al.
        International Study of Asthma and Allergies in Childhood (ISAAC): rationale and methods.
        Eur Respir J. 1995; 8: 483-491
        • Fuso L.
        • de Rosa M.
        • Corbo G.M.
        • Valente S.
        • Forastiere F.
        • Agabiti N.
        • et al.
        Repeatability of the ISAAC video questionnaire and its accuracy against a clinical diagnosis of asthma.
        Respir Med. 2000; 94: 397-403
        • Lai C.K.
        • Chan J.K.
        • Chan A.
        • Wong G.
        • Ho A.
        • Choy D.
        • et al.
        Comparison of the ISAAC video questionnaire (AVQ3.0) with the ISAAC written questionnaire for estimating asthma associated with bronchial hyperreactivity.
        Clin Exp Allergy. 1997; 27: 540-545
        • Lovinsky-Desir S.
        • Miller R.L.
        Epigenetics, asthma, and allergic diseases: a review of the latest advancements.
        Curr Allergy Asthma Rep. 2012; 12: 211-220
        • Rosa M.J.
        • Divjan A.
        • Hoepner L.
        • Sheares B.J.
        • Diaz D.
        • Gauvey-Kern K.
        • et al.
        Fractional exhaled nitric oxide exchange parameters among 9-year-old inner-city children.
        Pediatr Pulmonol. 2011; 46: 83-91
        • Perzanowski M.S.
        • Chew G.L.
        • Divjan A.
        • Johnson A.
        • Goldstein I.F.
        • Garfinkel R.S.
        • et al.
        Cat ownership is a risk factor for the development of anti-cat IgE but not current wheeze at age 5 years in an inner-city cohort.
        J Allergy Clin Immunol. 2008; 121: 1047-1052
        • Donohue K.M.
        • Al-alem U.
        • Perzanowski M.S.
        • Chew G.L.
        • Johnson A.
        • Divjan A.
        • et al.
        Anti-cockroach and anti-mouse IgE are associated with early wheeze and atopy in an inner-city birth cohort.
        J Allergy Clin Immunol. 2008; 122: 914-920
        • Rothman K.J.
        No adjustments are needed for multiple comparisons.
        Epidemiology. 1990; 1: 43-46
        • Rastogi D.
        • Wang C.
        • Mao X.
        • Lendor C.
        • Rothman P.B.
        • Miller R.L.
        Antigen-specific immune responses to influenza vaccine in utero.
        J Clin Invest. 2007; 117: 1637-1646
        • Jeffrey P.K.
        The development of large and small airways.
        Am J Respir Crit Care Med. 1998; 157: S174-S180
        • Schonfelder G.
        • Wittfoht W.
        • Hopp H.
        • Talsness C.E.
        • Paul M.
        • Chahoud I.
        Parent bisphenol A accumulation in the human maternal-fetal-placental unit.
        Environ Health Perspect. 2002; 110: A703-A707
        • Zalko D.
        • Soto A.M.
        • Dolo L.
        • Dorio C.
        • Rathahao E.
        • Debrauwer L.
        • et al.
        Biotransformations of bisphenol A in a mammalian model: answers and new questions raised by low-dose metabolic fate studies in pregnant CD1 mice.
        Environ Health Perspect. 2003; 111: 309-319
        • Nishikawa M.
        • Iwano H.
        • Yanagisawa R.
        • Koike N.
        • Inoue H.
        • Yokota H.
        Placental transfer of conjugated bisphenol A and subsequent reactivation in the rat fetus.
        Environ Health Perspect. 2010; 118: 1196-1203
        • Coughtrie M.W.
        • Burchell B.
        • Leakey J.E.
        • Hume R.
        The inadequacy of perinatal glucuronidation: immunoblot analysis of the developmental expression of individual UDP-glucuronosyltransferase isoenzymes in rat and human liver microsomes.
        Mol Pharmacol. 1988; 34: 729-735
        • Clayton E.M.
        • Todd M.
        • Dowd J.B.
        • Aiello A.E.
        The impact of bisphenol A and triclosan on immune parameters in the U.S. population, NHANES 2003-2006.
        Environ Health Perspect. 2011; 119: 390-396
        • Midoro-Horiuti T.
        • Tiwari R.
        • Watson C.S.
        • Goldblum R.M.
        Maternal bisphenol a exposure promotes the development of experimental asthma in mouse pups.
        Environ Health Perspect. 2010; 118: 273-277
        • Ohshima Y.
        • Yamada A.
        • Tokuriki S.
        • Yasutomi M.
        • Omata N.
        • Mayumi M.
        Transmaternal exposure to bisphenol a modulates the development of oral tolerance.
        Pediatr Res. 2007; 62: 60-64
        • Roy A.
        • Bauer S.M.
        • Lawrence B.P.
        Developmental exposure to bisphenol a modulates innate but not adaptive immune responses to influenza a virus infection.
        PLoS One. 2012; 7: e38448
        • Braun J.M.
        • Smith K.W.
        • Williams P.L.
        • Calafat A.M.
        • Berry K.
        • Ehrlich S.
        • et al.
        Variability of urinary phthalate metabolite and bisphenol a concentrations before and during pregnancy.
        Environ Health Perspect. 2012; 120: 739-745
        • Ye X.
        • Wong L.Y.
        • Bishop A.M.
        • Calafat A.M.
        Variability of urinary concentrations of bisphenol a in spot samples, first morning voids, and 24-hour collections.
        Environ Health Perspect. 2011; 119: 983-988
        • Lang I.A.
        • Galloway T.S.
        • Scarlett A.
        • Henley W.E.
        • Depledge M.
        • Wallace R.B.
        • et al.
        Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults.
        JAMA. 2008; 300: 1303-1310
        • Kurukulaaratchy R.J.
        • Fenn M.H.
        • Waterhouse L.M.
        • Matthews S.M.
        • Holgate S.T.
        • Arshad S.H.
        Characterization of wheezing phenotypes in the first 10 years of life.
        Clin Exp Allergy. 2003; 33: 573-578
        • Matricardi P.M.
        • Illi S.
        • Gruber C.
        • Keil T.
        • Nickel R.
        • Wahn U.
        • et al.
        Wheezing in childhood: incidence, longitudinal patterns and factors predicting persistence.
        Eur Respir J. 2008; 32: 585-592
        • Kurukulaaratchy R.J.
        • Matthews S.
        • Holgate S.T.
        • Arshad S.H.
        Predicting persistent disease among children who wheeze during early life.
        Eur Respir J. 2003; 22: 767-771
        • von Mutius E.
        Epidemiology of asthma: ISAAC—International Study of Asthma and Allergies in Childhood.
        Pediatr Allergy Immunol. 1996; 7: 54-56
        • Bjorksten B.
        • Ait-Khaled N.
        • Innes Asher M.
        • Clayton T.O.
        • Robertson C.
        Global analysis of breast feeding and risk of symptoms of asthma, rhinoconjunctivitis and eczema in 6-7 year old children: ISAAC Phase Three.
        Allergol Immunopathol (Madr). 2011; 39: 318-325
        • Civelek E.
        • Cakir B.
        • Orhan F.
        • Yuksel H.
        • Boz A.B.
        • Uner A.
        • et al.
        Risk factors for current wheezing and its phenotypes among elementary school children.
        Pediatr Pulmonol. 2011; 46: 166-174
        • Custovic A.
        • Simpson B.M.
        • Murray C.S.
        • Lowe L.
        • Woodcock A.
        The National Asthma Campaign Manchester Asthma and Allergy Study.
        Pediatr Allergy Immunol. 2002; 13: 32-37
        • Brunekreef B.
        • Smit J.
        • de Jongste J.
        • Neijens H.
        • Gerritsen J.
        • Postma D.
        • et al.
        The prevention and incidence of asthma and mite allergy (PIAMA) birth cohort study: design and first results.
        Pediatr Allergy Immunol. 2002; 13: 55-60
        • Ublagger E.
        • Schreuer M.
        • Eder W.
        • von Mutius E.
        • Benz M.R.
        • Braun-Fahrlander C.
        • et al.
        Validation of questions on asthma and wheeze in farming and anthroposophic children.
        Clin Exp Allergy. 2005; 35: 1033-1039
        • Sears M.R.
        • Greene J.M.
        • Willan A.R.
        • Wiecek E.M.
        • Taylor D.R.
        • Flannery E.M.
        • et al.
        A longitudinal, population-based, cohort study of childhood asthma followed to adulthood.
        N Engl J Med. 2003; 349: 1414-1422
      1. The Childhood Asthma Management Program (CAMP): design, rationale, and methods. Childhood Asthma Management Program Research Group.
        Control Clin Trials. 1999; 20: 91-120
        • Mitchell H.
        • Senturia Y.
        • Gergen P.
        • Baker D.
        • Joseph C.
        • McNiff-Mortimer K.
        • et al.
        Design and methods of the National Cooperative Inner-City Asthma Study.
        Pediatr Pulmonol. 1997; 24: 237-252
        • Crain E.F.
        • Walter M.
        • O'Connor G.T.
        • Mitchell H.
        • Gruchalla R.S.
        • Kattan M.
        • et al.
        Home and allergic characteristics of children with asthma in seven U.S. urban communities and design of an environmental intervention: the Inner-City Asthma Study.
        Environ Health Perspect. 2002; 110: 939-945
        • Remes S.T.
        • Pekkanen J.
        • Remes K.
        • Salonen R.O.
        • Korppi M.
        In search of childhood asthma: questionnaire, tests of bronchial hyperresponsiveness, and clinical evaluation.
        Thorax. 2002; 57: 120-126