The Journal of Allergy and Clinical Immunology
Volume 117, Issue 1 , Pages 97-102 , January 2006

Parental tobacco smoking is associated with augmented IL-13 secretion in children with allergic asthma

  • Wojciech Feleszko, MD, PhD

      Affiliations

    • From the Departments of Pediatric Pneumonology and Allergy
    • Dr Feleszko is on a leave of absence at the Department of Pediatric Pneumology and Immunology, Charité Universitäts Medizin, Berlin, Germany.
    • Corresponding Author InformationReprint requests: Wojciech Feleszko MD, PhD, Department of Pediatric Pneumology and Allergy, The Medical University Children's Hospital, ul Działdowska 1/3, PL-01-184 Warsaw, Poland.
  • ,
  • Anna Zawadzka-Krajewska, MD, PhD

      Affiliations

    • From the Departments of Pediatric Pneumonology and Allergy
  • ,
  • Katarzyna Matysiak, MD

      Affiliations

    • Unit of Anaesthesiology, The Medical University Children's Hospital, The Medical University of Warsaw
  • ,
  • Dorota Lewandowska, MD

      Affiliations

    • Unit of Anaesthesiology, The Medical University Children's Hospital, The Medical University of Warsaw
  • ,
  • Joanna Peradzyńska, MD

      Affiliations

    • From the Departments of Pediatric Pneumonology and Allergy
  • ,
  • Q. Thai Dinh, MD, PhD

      Affiliations

    • Pneumology and Immunology, Charité School of Medicine, Free University and Humboldt-University, Berlin
  • ,
  • Eckard Hamelmann, MD, PhD

      Affiliations

    • Department of Pediatric Pneumology and Immunology, Charité Universitäts Medizin, Berlin
  • ,
  • David A. Groneberg, MD, PhD

      Affiliations

    • Pneumology and Immunology, Charité School of Medicine, Free University and Humboldt-University, Berlin
  • ,
  • Marek Kulus, MD, PhD

      Affiliations

    • From the Departments of Pediatric Pneumonology and Allergy

Received 18 February 2005 ,Revised 11 August 2005 ,Accepted 7 September 2005.

References 

  1. Chan-Yeung M, Dimich-Ward H. Respiratory health effects of exposure to environmental tobacco smoke. Respirology. 2003;8:131–139
  2. DiFranza JR, Aligne CA, Weitzman M. Prenatal and postnatal environmental tobacco smoke exposure and children's health. Pediatrics. 2004;113:1007–1015
  3. Strachan DP, Cook DG. Health effects of passive smoking. 5. Parental smoking and allergic sensitisation in children. Thorax. 1998;53:117–123
  4. Floreani AA, Rennard SI. The role of cigarette smoke in the pathogenesis of asthma and as a trigger for acute symptoms. Curr Opin Pulm Med. 1999;5:38–46
  5. Donovan CE, Finn PW. Immune mechanisms of childhood asthma. Thorax. 1999;54:938–946
  6. Wills-Karp M. IL-12/IL-13 axis in allergic asthma. J Allergy Clin Immunol. 2001;107:9–18
  7. Mattes J, Yang M, Mahalingam S, Kuehr J, Webb DC, Simson L, et al. Intrinsic defect in T cell production of interleukin (IL)-13 in the absence of both IL-5 and eotaxin precludes the development of eosinophilia and airways hyperreactivity in experimental asthma. J Exp Med. 2002;195:1433–1444
  8. Wills-Karp M. Interleukin-13 in asthma pathogenesis. Immunol Rev. 2004;202:175–190
  9. Zhu Z, Homer RJ, Wang Z, Chen Q, Geba GP, Wang J, et al. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J Clin Invest. 1999;103:779–788
  10. Webb DC, McKenzie AN, Koskinen AM, Yang M, Mattes J, Foster PS. Integrated signals between IL-13, IL-4, and IL-5 regulate airways hyperreactivity. J Immunol. 2000;165:108–113
  11. Gibson PG, Henry RL, Thomas P. Noninvasive assessment of airway inflammation in children: induced sputum, exhaled nitric oxide, and breath condensate. Eur Respir J. 2000;16:1008–1015
  12. Lemanske RF. Inflammation in childhood asthma and other wheezing disorders. Pediatrics. 2002;109:368–372
  13. Payne DN, Qiu Y, Zhu J, Peachey L, Scallan M, Bush A, et al. Airway inflammation in children with difficult asthma: relationships with airflow limitation and persistent symptoms. Thorax. 2004;59:862–869
  14. Noakes PS, Holt PG, Prescott SL. Maternal smoking in pregnancy alters neonatal cytokine responses. Allergy. 2003;58:1053–1058
  15. Seymour BW, Schelegle ES, Pinkerton KE, Friebertshauser KE, Peake JL, Kurupd VP, et al. Second-hand smoke increases bronchial hyperreactivity and eosinophilia in a murine model of allergic aspergillosis. Clin Dev Immunol. 2003;10:35–42
  16. McKay A, Komai-Koma M, MacLeod KJ, Campbell CC, Kitson SM, Chaudhuri R, et al. Interleukin-18 levels in induced sputum are reduced in asthmatic and normal smokers. Clin Exp Allergy. 2004;34:904–910
  17. National Asthma Education and Prevention Program. Expert Panel report: guidelines for the diagnosis and management of asthma—update on selected topics. Bethesda (MD): National Institutes of Health, National Heart, Lung and Blood Institute; 2002. NIH publication no. 02-5075. Available at: http://www.nhlbi.nih.gov/guidelines/asthma/asthsumm.htm.
  18. Global Initiative for Asthma. Global strategy for asthma management and prevention. Bethesda (MD): National Institutes of Health; January 1995 (updated 2004). NIH publication no. 02-3659. Available at: http://www.ginasthma.org
  19. Tutka P, Wielosz M, Zatonski W. Exposure to environmental tobacco smoke and children health. Int J Occup Med Environ Health. 2002;15:325–335
  20. Xiang X, Qiu D, Chan KP, Chan SH, Hegele RG, Tan WC. Comparison of three methods for respiratory virus detection between induced sputum and nasopharyngeal aspirate specimens in acute asthma. J Virol Methods. 2002;101:127–133
  21. Pizzichini E, Pizzichini MM, Efthimiadis A, Evans S, Morris MM, Squillace D, et al. Indices of airway inflammation in induced sputum: reproducibility and validity of cell and fluid-phase measurements. Am J Respir Crit Care Med. 1996;154:308–317
  22. Komai-Koma M, McKay A, Thomson L, McSharry C, Chalmers GW, Liew FY, et al. Immuno-regulatory cytokines in asthma: IL-15 and IL-13 in induced sputum. Clin Exp Allergy. 2001;31:1441–1448
  23. Krug N, Erpenbeck VJ, Balke K, Petschallies J, Tschernig T, Hohlfeld JM, et al. Cytokine profile of bronchoalveolar lavage-derived CD4(+), CD8(+), and gammadelta T cells in people with asthma after segmental allergen challenge. Am J Respir Cell Mol Biol. 2001;25:125–131
  24. Seymour BW, Friebertshauser KE, Peake JL, Pinkerton KE, Coffman RL, Gershwin LJ. Gender differences in the allergic response of mice neonatally exposed to environmental tobacco smoke. Dev Immunol. 2002;9:47–54
  25. Bartalesi B, Cavarra E, Fineschi S, Lucattelli M, Lunghi B, Martorana PA, et al. Different lung responses to cigarette smoke in two strains of mice sensitive to oxidants. Eur Respir J. 2005;25:15–22
  26. Noakes PS, Holt PG, Prescott SL. Maternal smoking in pregnancy alters neonatal cytokine response. Allergy. 2003;58:1053–1058
  27. Lodrup Carlsen KC, Carlsen KH. Effects of maternal and early tobacco exposure on the development of asthma and airway hyperreactivity. Curr Opin Allergy Clin Immunol. 2001;1:139–143
  28. Sheeran P, Jafri H, Carubelli C, Saavedra J, Johnson C, Krisher K, et al. Elevated cytokine concentrations in the nasopharyngeal and tracheal secretions of children with respiratory syncytial virus disease. Pediatr Infect Dis J. 1999;18:115–122
  29. Oh JW, Lee HB, Yum MK, Kim CR, Kang JO, Park IK. ECP level in nasopharyngeal secretions and serum from children with respiratory virus infections and asthmatic children. Allergy Asthma Proc. 2000;21:97–100
  30. Nagayama Y, Tsubaki T, Toba T, Nakayama S, Kiyofumi O. Analysis of sputum taken from wheezy and asthmatic infants and children, with special reference to respiratory infections. Pediatr Allergy Immunol. 2001;12:318–326
  31. Oh JW, Lee HB, Park IK, Kang JO. Interleukin-6, interleukin-8, interleukin-11, and interferon-gamma levels in nasopharyngeal aspirates from wheezing children with respiratory syncytial virus or influenza A virus infection. Pediatr Allergy Immunol. 2002;13:350–356
  32. Kuperman DA, Huang X, Koth LL, Chang GH, Dolganov GM, Zhu Z, et al. Direct effects of interleukin-13 on epithelial cells cause airway hyperreactivity and mucus overproduction in asthma. Nat Med. 2002;8:885–889
  33. Wills-Karp M, Chiaramonte M. Interleukin-13 in asthma. Curr Opin Pulm Med. 2003;9:21–27
  34. Gibson PG. Use of induced sputum to examine airway inflammation in childhood asthma. J Allergy Clin Immunol. 1998;102(suppl):S100–S101
  35. Shoji S, Kanazawa H, Hirata K, Kurihara N, Yoshikawa J. Clinical implication of protein levels of IL-5 in induced sputum in asthmatic patients. J Asthma. 1998;35:243–249
  36. Chanez P, Vignola AM, Vic P, Guddo F, Bonsignore G, Godard P, et al. Comparison between nasal and bronchial inflammation in asthmatic and control subjects. Am J Respir Crit Care Med. 1999;159:588–595
  37. Wills-Karp M, Luyimbazi J, Xu X, Schofield B, Neben TY, Karp CL, et al. Interleukin-13: central mediator of allergic asthma. Science. 1998;282:2258–2261
  38. Greenfeder S, Umland SP, Cuss FM, Chapman RW, Egan RW. Th2 cytokines and asthma. The role of interleukin-5 in allergic eosinophilic disease. Respir Res. 2001;2:71–79
  39. Cousins DJ, Lee TH, Staynov DZ. Cytokine coexpression during human Th1/Th2 cell differentiation: direct evidence for coordinated expression of Th2 cytokines. J Immunol. 2002;169:2498–2506

 Supported by research grants from the Medical University of Warsaw (1W34/W1/1998-2000 and 1W34/W2/2003-2005).

PII: S0091-6749(05)02054-3

doi: 10.1016/j.jaci.2005.09.008

The Journal of Allergy and Clinical Immunology
Volume 117, Issue 1 , Pages 97-102 , January 2006