The Journal of Allergy and Clinical Immunology
Volume 119, Issue 5 , Pages 1164-1173 , May 2007

Prenatal versus postnatal sensitization to environmental allergens in a high-risk birth cohort

  • Julie Rowe, PhD

      Affiliations

    • From the Telethon Institute for Child Health Research, Centre for Child Health Research, University of Western Australia, Perth
    • ,
  • Merci Kusel, MBBS, PhD

      Affiliations

    • From the Telethon Institute for Child Health Research, Centre for Child Health Research, University of Western Australia, Perth
    • ,
  • Barbara J. Holt, BSc

      Affiliations

    • From the Telethon Institute for Child Health Research, Centre for Child Health Research, University of Western Australia, Perth
    • ,
  • Devinda Suriyaarachchi, BSc(Hons)

      Affiliations

    • From the Telethon Institute for Child Health Research, Centre for Child Health Research, University of Western Australia, Perth
    • ,
  • Michael Serralha, BSc(Hons)

      Affiliations

    • From the Telethon Institute for Child Health Research, Centre for Child Health Research, University of Western Australia, Perth
    • ,
  • Elysia Hollams, PhD

      Affiliations

    • From the Telethon Institute for Child Health Research, Centre for Child Health Research, University of Western Australia, Perth
    • ,
  • Stephanie T. Yerkovich, PhD

      Affiliations

    • From the Telethon Institute for Child Health Research, Centre for Child Health Research, University of Western Australia, Perth
    • ,
  • Lily S. Subrata, PhD

      Affiliations

    • From the Telethon Institute for Child Health Research, Centre for Child Health Research, University of Western Australia, Perth
    • ,
  • Claire Ladyman, BSc

      Affiliations

    • From the Telethon Institute for Child Health Research, Centre for Child Health Research, University of Western Australia, Perth
    • ,
  • Agata Sadowska, BSc(Hons)

      Affiliations

    • From the Telethon Institute for Child Health Research, Centre for Child Health Research, University of Western Australia, Perth
    • ,
  • Jamie Gillett, BSc

      Affiliations

    • Princess Margaret Hospital for Children, Subiaco
    • ,
  • Elizabeth Fisher, BSc

      Affiliations

    • Princess Margaret Hospital for Children, Subiaco
    • ,
  • Richard Loh, FRACP

      Affiliations

    • Princess Margaret Hospital for Children, Subiaco
    • ,
  • Lars Soderstrom, MSc

      Affiliations

    • Phadia AB, Uppsala
    • Karolinska Institute, Stockholm
    • ,
  • Staffan Ahlstedt, PhD

      Affiliations

    • Phadia AB, Uppsala
    • Karolinska Institute, Stockholm
    • ,
  • Peter D. Sly, MD, FRACP, DSc

      Affiliations

    • From the Telethon Institute for Child Health Research, Centre for Child Health Research, University of Western Australia, Perth
    • ,
  • Patrick G. Holt, DSc

      Affiliations

    • From the Telethon Institute for Child Health Research, Centre for Child Health Research, University of Western Australia, Perth
    • Corresponding Author InformationReprint requests: Patrick G. Holt, DSc, Division of Cell Biology, Telethon Institute for Child Health Research, PO Box 855, West Perth WA 6872, Australia.

Received 14 November 2006 ,Revised 24 January 2007 ,Accepted 15 February 2007.

References 

  1. Bjorksten F, Suoniemi I. Dependence of immediate hypersensitivity on the month of birth. Clin Allergy. 1976;6:165–171
  2. Businco L, Cantani A, Farinella F, Businco E. Month of birth and grass pollen or mite sensitisation in children with respiratory allergy: a significant relationship. Clin Allergy. 1988;18:269–274
  3. Kihlstrom A, Lilja G, Pershagen G, Hedlin G. Exposure to high doses of birch pollen during pregnancy, and risk of sensitization and atopic disease is the child. Allergy. 2003;58:871–877
  4. Korsgaard J, Dahl R. Sensitivity to house dust mite and grass pollen. Clin Allergy. 1983;13:529–536
  5. Aalberse RC, Nieuwenhuys EJ, Hey M, Stapel SO. “Horoscope effect” not only for seasonal but also for nonseasonal allergens. Clin Exp Allergy. 1992;22:1003–1006
  6. Hagendorens MM, Ebo DG, Bridts CH, Van de Water L, De Clerck LS, Stevens WJ. Prenatal exposure to house dust mite allergen (Der p 1), cord blood T cell phenotype and cytokine production and atopic dermatitis during the first year of life. Pediatr Allergy Immunol. 2004;15:308–315
  7. Kondo N, Kobayashi Y, Shinoda S, Kasahara K, Kameyama T, Iwasa S, et al. Cord blood lymphocyte responses to food antigens for the prediction of allergic disorders. Arch Dis Child. 1992;67:1003–1007
  8. Miller RL, Chew GL, Bell CA, Biedermann SA, Aggarwal M, Kinney PL, et al. Prenatal exposure, maternal sensitization, and sensitization in utero to indoor allergens in an inner-city cohort. Am J Respir Crit Care Med. 2001;164:995–1001
  9. Piastra M, Stabile A, Fioravanti G, Castagnola M, Pani G, Ria F. Cord blood mononuclear cell responsiveness to beta-lactoglobulin: T-cell activity in “atopy-prone” and “non-atopy-prone” newborns. Int Arch Allergy Immunol. 1994;104:358–365
  10. Prescott SL, Macaubas C, Smallacombe T, Holt BJ, Sly PD, Holt PG. Development of allergen-specific T-cell memory in atopic and normal children. Lancet. 1999;353:196–200
  11. Casas R, Jenmalm MC, Bjorksten B. Cat allergen-induced cytokine secretion and Fel d 1-immunoglobulin G immune complexes in cord blood. Clin Exp Allergy. 2004;34:591–596
  12. Holt PG, O'Keeffe PO, Holt BJ, Upham JW, Baron-Hay MJ, Suphioglu C, et al. T-cell “priming” against environmental allergens in human neonates: sequential deletion of food antigen specificities during infancy with concomitant expansion of responses to ubiquitous inhalant allergens. Pediatr Allergy Immunol. 1995;6:85–90
  13. Vance GHS, Lewis SA, Grimshaw KEC, Wood PJ, Briggs RA, Thornton CA, et al. Exposure of the fetus and infant to hens' egg ovalbumin via the placenta and breast milk in relation to maternal intake of dietary egg. Clin Exp Allergy. 2005;35:1318–1326
  14. Malhotra I, Mungai PL, Wamachi AN, Tisch D, Kioko JM, Ouma JH, et al. Prenatal T cell immunity to Wuchereria bancrofti and its effect on filarial immunity and infection susceptibility during childhood. J Infect Dis. 2006;193:1005–1013
  15. Marchant A, Appay V, van der Sande M, Dulphy N, Liesnard C, Kidd M, et al. Mature CD8(+) T lymphocyte response to viral infection during fetal life. J Clin Invest. 2003;111:1747–1755
  16. Gill TJ, Repetti CF, Metlay LA. Transplacental immunisation of the human fetus to tetanus by immunisation of the mother. J Clin Invest. 1983;72:987–996
  17. Committee on Toxicity of Chemicals in Food, Consumer Products and the Environment. Peanut allergy. London: Department of Health; 1998;
  18. Department of Health . Peanut allergy. London: Department of Health; 1998;CMO's Update 19
  19. Hannah ML. New Zealand Medicines and Medical Devices Safety Authority. Prescriber Update No. 20:22-26. Peanut Allergy. 2000.
  20. American Academy of Pediatrics, Committee on Nutrition . Hypoallergenic infant formulas. Pediatrics. 2000;106:346–349
  21. Herrmann M-E, Dannemann A, Gruters A, Radisch B, Dudenhausen JW, Bergmann R, et al. Prospective study on the atopy preventive effect of maternal avoidance of milk and eggs during pregnancy and lactation. Eur J Pediatr. 1996;155:770–774
  22. Turke J, Venter C, Dean T. Maternal experiences of peanut avoidance during pregnancy/lactation: an in-depth qualitative study. Pediatr Allergy Immunol. 2005;16:512–518
  23. Vance GHS, Grimshaw KEC, Briggs R, Lewis SA, Mullee MA, Thornton CA, et al. Serum ovalbumin-specific immunoglobulin G responses during pregnancy reflect maternal intake of dietary egg and relate to the development of allergy in early infancy. Clin Exp Allergy. 2004;34:1855–1861
  24. Zeiger RS, Heller S. The development and prediction of atopy in high-risk children: follow-up at age seven years in a prospective randomized study of combined maternal and infant food allergen avoidance. J Allergy Clin Immunol. 1995;96:1179–1190
  25. Custovic A, Simpson BM, Simpson A, Kissen P, Woodcock A. Effect of environmental manipulation in pregnancy and early life on respiratory systems and atopy during first year of life: a randomised trial. Lancet. 2001;358:188–193
  26. Szépfalusi Z, Loibichler C, Pichler J, Reisenberger K, Ebner C, Urbanek R. Direct evidence for transplacental allergen transfer. Pediatr Res. 2000;48:404–407
  27. Björkstén B, Holt BJ, Baron-Hay MJ, Munir AKM, Holt PG. Low-level exposure to house dust mites stimulates T-cell responses during early childhood independent of atopy. Clin Exp Allergy. 1996;26:775–779
  28. Platts-Mills TA, Blumenthal K, Perzanowski MS, Woodfolk JA. Determinants of clinical allergic disease. The relevance of indoor allergens to the increase in asthma. Am J Respir Crit Care Med. 2000;162:S128–S133
  29. Muraro A, Dreborg S, Halken S, Host A, Niggemann B, Aalberse R, et al. Dietary prevention of allergic diseases in infants and small children. Part III: critical review of published peer-reviewed observational and interventional studies and final recommendations. Pediatr Allergy Immunol. 2004;15:291–307
  30. Rowe J, Poolman JT, Macaubas C, Sly PD, Loh R, Holt PG. Enhancement of vaccine-specific cellular immunity in infants by passively acquired maternal antibody. Vaccine. 2004;22:3986–3992
  31. Kusel MM, Holt PG, de Klerk N, Sly PD. Support for 2 variants of eczema. J Allergy Clin Immunol. 2006;116:1067–1072
  32. Evans G, Rilven M. Bulk Reagent Random-Access analyzers: UniCAP 100. In: The Immunoassay Handbook. Frome, UK: Tradespools Ltd; 2000;
  33. Yman L. Allergy. The Immunoassay Handbook. Frome, UK: Tradespools Ltd; 2000;
  34. Cressy I, Magnusson B, Soderstrom L, Kober A. IgG4 antibody concentrations to cat and mite allergens measured with the new ImmunoCAP specific IgG4 method. In: Proc XXV Congress of the European Academy of Allergy and Clinical Immunology. Vienna: Austria; 2006;p. 296
  35. Hattevig G, Kjellman B, Björkstén B. Appearance IgE antibodies to ingested and inhaled allergens during the first 12 years of life in atopic and non-atopic children. Pediatr Allergy Immunol. 1993;4:182–186
  36. Sasai K, Furukawa S, Muto T, Baba M, Yabuta K, Fukuwatari Y. Early detection of specific IgE antibody against house dust mite in children at risk of allergic disease. J Pediatr. 1996;128:834–840
  37. Cain TW, Ford J, Dolen WK. A low-level method for measurement of specific immunoglobulin E antibody serum. Allergy Clin Immunol Int J World Allergy Org. 2006;18/6:1–4
  38. Wood RA, Segall N, Ahlstedt S, Williams PB. Not all IgE antibody laboratory results provide accurate information for clinical judgement. Ann Allergy 2007. In press.
  39. Ballardini N, Nilsson C, Nilsson M, Lilja G. ImmunoCAP™ Phadiatop® Infant - a new blood test for detecting IgE sensitisation in children at 2 years of age. Allergy. 2006;61:337–343
  40. Heaton T, Rowe J, Turner S, Aalberse RC, de Klerk N, Suriyaarachchi D, et al. An immunoepidemiological approach to asthma: identification of in-vitro T-cell response patterns associated with different wheezing phenotypes in children. Lancet. 2005;365:142–149
  41. Strickland DH, Stumbles PA, Zosky GR, Subrata LS, Thomas JA, Turner DJ, et al. Reversal of airways hyperresponsiveness by induction of airway mucosal CD4+CD25+ regulatory T-cells. J Exp Med. 2006;203:2649–2660
  42. Thornton CA, Upham JW, Wikström ME, Holt BJ, White GP, Sharp MJ, et al. Functional maturation of CD4+ CD25+ CTLA4+ CD45RA+ T regulatory cells in human neonatal T cell responses to environmental allergens. J Immunol. 2004;173:3084–3092
  43. Gavin MA, Bevan MJ. Increased peptide promiscuity provides a rationale for the lack of N regions in the neonatal T cell repertoire. Immunity. 1995;3:793–800
  44. Kulig M, Bergmann R, Klettke U, Wahn V, Tacke U, Wahn U. Natural course sensitization of food and inhalant allergens during the first 6 years of life. J Allergy Clin Immunol. 1999;103:1173–1179
  45. Julge K, Vasar M, Björkstén B. Development of allergy and IgE antibodies during the first five years of life in Estonian children. Clin Exp Allergy. 2001;31:1854–1861
  46. McMenamin C, Holt PG. The natural immune response to inhaled soluble protein antigens involves major histocompatibility complex (MHC) class I-restricted CD8+ T cell-mediated but MHC class II-restricted CD4+ T cell-dependent immune deviation resulting in selective suppression of IgE production. J Exp Med. 1993;178:889–899
  47. Holt PG, Sedgwick JD. Suppression of IgE responses following antigen inhalation: a natural homeostatic mechanism which limits sensitization to aeroallergens. Immunol Today. 1987;8:14–15
  48. Holt PG. A potential vaccine strategy for asthma and allied atopic diseases in early childhood. Lancet. 1994;344:456–458
  49. Holt PG, Sly PD. Prophylaxis of atopy and asthma in children. NIH Immune Tolerance Network Trial. 2006. Available at: http://www.immunetolerance.org/research/allergy/trials/holt.html.

 Supported by a grant from the National Health & Medical Research Council of Australia with supplementary support from the Food Allergy Initiative, New York.Disclosure of potential conflict of interest: L. Soderstrom and S. Ahlstedt are employed by Phadia AB, Uppsala, Sweden. The rest of the authors have declared that they have no conflict of interest.

PII: S0091-6749(07)00412-5

doi: 10.1016/j.jaci.2007.02.016

The Journal of Allergy and Clinical Immunology
Volume 119, Issue 5 , Pages 1164-1173 , May 2007

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