Respiratory Medicine
Volume 106, Issue 3 , Pages 319-328 , March 2012

The effects of cigarette smoke on airway inflammation in asthma and COPD: Therapeutic implications

  • Asad Tamimi

      Affiliations

    • Clinical Sciences, Primary Care Business Unit, Pfizer Inc, Ramsgate Road, Sandwich CT13 9NJ, UK
  • ,
  • Dzelal Serdarevic

      Affiliations

    • Clinical Sciences, Primary Care Business Unit, Pfizer Inc, Ramsgate Road, Sandwich CT13 9NJ, UK
    • Corresponding Author InformationCorresponding author. Tel.: +44 1304 648071.
  • ,
  • Nicola A. Hanania

      Affiliations

    • Section of Pulmonary and Critical Care Medicine, Baylor College of Medicine, Houston, TX, USA

Received 28 June 2011 ,Accepted 2 November 2011.

References 

  1. Gandevia B. Historical review of the use of parasympatholytic agents in the treatment of respiratory disorders. Postgrad Med J. 1975;51(7 Suppl.):13–20
  2. Chan-Yeung M, Dimich-Ward H. Respiratory health effects of exposure to environmental tobacco smoke. Respirology. 2003;8(2):131–139
  3. Coultas DB. Health effects of passive smoking. 8. Passive smoking and risk of adult asthma and COPD: an update. Thorax. 1998;53(5):381–387
  4. Adult cigarette smoking in the United States: current estimates. Smoking and Tobacco Use. CDC. Fact Sheet. [cited 2010 13/06]; Available from: 2006;http://www.cdc.gov/tobacco/data_statistics/Factsheets/adult_cig_smoking.html
  5. The European Tobacco Control Report. [cited 2010 13/06]; Available from 2007;http://wwweurowhoint/document/e89842pdf
  6. Thomson NC, Chaudhuri R, Livingston E. Asthma and cigarette smoking. Eur Respir J. 2004;24(5):822–833
  7. Mannino DM, et al. Chronic obstructive pulmonary disease surveillance–United States, 1971-2000. MMWR Surveill Summ. 2002;51(6):1–16
  8. Anthonisen NR, et al. Effects of smoking intervention and the use of an inhaled anticholinergic bronchodilator on the rate of decline of FEV1. The Lung Health Study. Jama. 1994;272(19):1497–1505
  9. Global Initiative for chronic obstructive lung disease, in Global strategy for the Diagnosis, management, and Prevention of chronic obstructive pulmonary disease. 2009;p. 4
  10. Anthonisen NR, et al. The effects of a smoking cessation intervention on 14.5-year mortality: a randomized clinical trial. Ann Intern Med. 2005;142(4):233–239
  11. Barnes PJ. Immunology of asthma and chronic obstructive pulmonary disease. Nat Rev Immunol. 2008;8(3):183–192
  12. Chanez P, et al. Corticosteroid reversibility in COPD is related to features of asthma. Am J Respir Crit Care Med. 1997;155(5):1529–1534
  13. Chalmers GW, et al. Influence of cigarette smoking on inhaled corticosteroid treatment in mild asthma. Thorax. 2002;57(3):226–230
  14. Chaudhuri R, et al. Cigarette smoking impairs the therapeutic response to oral corticosteroids in chronic asthma. Am J Respir Crit Care Med. 2003;168(11):1308–1311
  15. Barnes PJ. Inhaled corticosteroids are not beneficial in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2000;161(2 Pt 1):342–344discussion 344
  16. Apostol GG, et al. Early life factors contribute to the decrease in lung function between ages 18 and 40: the Coronary Artery Risk Development in Young Adults study. Am J Respir Crit Care Med. 2002;166(2):166–172
  17. Lange P, et al. A 15-year follow-up study of ventilatory function in adults with asthma. N Engl J Med. 1998;339(17):1194–1200
  18. Marquette CH, et al. Long-term prognosis of near-fatal asthma. A 6-year follow-up study of 145 asthmatic patients who underwent mechanical ventilation for a near-fatal attack of asthma. Am Rev Respir Dis. 1992;146(1):76–81
  19. Siroux V, et al. Relationships of active smoking to asthma and asthma severity in the EGEA study. Epidemiological study on the Genetics and Environment of Asthma. Eur Respir J. 2000;15(3):470–477
  20. Bateman ED, et al. Can guideline-defined asthma control be achieved? The Gaining Optimal Asthma ControL study. Am J Respir Crit Care Med. 2004;170(8):836–844
  21. Silverman RA, et al. Cigarette smoking among asthmatic adults presenting to 64 emergency departments. Chest. 2003;123(5):1472–1479
  22. Gallefoss F, Bakke PS. Does smoking affect the outcome of patient education and self-management in asthmatics?. Patient Educ Couns. 2003;49(1):91–97
  23. The health consequences of smoking: chronic obstructive lung disease. In: Public health service. Office on smoking and health. Washington, DC: U.S Department of Health and Human Services; 1984;p. 185–200
  24. Henley SJ, et al. Association between exclusive pipe smoking and mortality from cancer and other diseases. J Natl Cancer Inst. 2004;96(11):853–861
  25. Rodriguez J, et al. The association of pipe and cigar use with cotinine levels, lung function, and airflow obstruction: a cross-sectional study. Ann Intern Med. 2010;152(4):201–210
  26. Al-Fayez SF, et al. Effects of sheesha and cigarette smoking on pulmonary function of Saudi males and females. Trop Geogr Med. 1988;40(2):115–123
  27. Thomson NC, Chaudhuri R. Asthma in smokers: challenges and opportunities. Curr Opin Pulm Med. 2009;15(1):39–45
  28. Di Stefano A, et al. Decreased T lymphocyte infiltration in bronchial biopsies of subjects with severe chronic obstructive pulmonary disease. Clin Exp Allergy. 2001;31(6):893–902
  29. Saetta M, et al. Cellular and structural bases of chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2001;163(6):1304–1309
  30. Haldar P, Pavord ID. Noneosinophilic asthma: a distinct clinical and pathologic phenotype. J Allergy Clin Immunol. 2007;119(5):1043–1052quiz 1053-4
  31. Jarvis D, et al. The association of smoking with sensitization to common environmental allergens: results from the European community respiratory health survey. J Allergy Clin Immunol. 1999;104(5):934–940
  32. White KA, Marletta MA. Nitric oxide synthase is a cytochrome P-450 type hemoprotein. Biochemistry. 1992;31(29):6627–6631
  33. Lazarus SC, et al. Smoking affects response to inhaled corticosteroids or leukotriene receptor antagonists in asthma. Am J Respir Crit Care Med. 2007;175(8):783–790
  34. Tsoumakidou M, et al. Cigarette smoking alters bronchial mucosal immunity in asthma. Am J Respir Crit Care Med. 2007;175(9):919–925
  35. Moerloose KB, Pauwels RA, Joos GF. Short-term cigarette smoke exposure enhances allergic airway inflammation in mice. Am J Respir Crit Care Med. 2005;172(2):168–172
  36. Jang AS, et al. The impact of smoking on clinical and therapeutic effects in asthmatics. J Korean Med Sci. 2009;24(2):209–214
  37. Bethesda M. Global initiative for asthma: global strategy for asthma management and prevention. NHLBI/WHO Report 1995;pp. 95–3695
  38. Jones PW, et al. Disease severity and the effect of fluticasone propionate on chronic obstructive pulmonary disease exacerbations. Eur Respir J. 2003;21(1):68–73
  39. Kerstjens HA, et al. Airways hyperresponsiveness, bronchodilator response, allergy and smoking predict improvement in FEV1 during long-term inhaled corticosteroid treatment. Dutch CNSLD Study Group. Eur Respir J. 1993;6(6):868–876
  40. Pedersen B, et al. Eosinophil and neutrophil activity in asthma in a one-year trial with inhaled budesonide. The impact of smoking. Am J Respir Crit Care Med. 1996;153(5):1519–1529
  41. Burge PS, et al. Prednisolone response in patients with chronic obstructive pulmonary disease: results from the ISOLDE study. Thorax. 2003;58(8):654–658
  42. Spencer S, et al. Impact of preventing exacerbations on deterioration of health status in COPD. Eur Respir J. 2004;23(5):698–702
  43. Vestbo J, et al. Long-term effect of inhaled budesonide in mild and moderate chronic obstructive pulmonary disease: a randomised controlled trial. Lancet. 1999;353(9167):1819–1823
  44. Pauwels RA, et al. Long-term treatment with inhaled budesonide in persons with mild chronic obstructive pulmonary disease who continue smoking. European Respiratory Society Study on Chronic Obstructive Pulmonary Disease. N Engl J Med. 1999;340(25):1948–1953
  45. Rees PJ. Review: inhaled corticosteroids do not reduce mortality but increase pneumonia in COPD. Evid Based Med. 2009;14(3):74
  46. Decramer M, de Bock V, Dom R. Functional and histologic picture of steroid-induced myopathy in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1996;153(6 Pt 1):1958–1964
  47. Ito K, Barnes PJ, Adcock IM. Glucocorticoid eceptor recruitment of histone deacetylase 2 inhibits interleukin-1beta-induced histone H4 acetylation on lysines 8 and 12. Mol Cell Biol. 2000;20(18):6891–6903
  48. Barnes PJ. Reduced histone deacetylase in COPD: clinical implications. Chest. 2006;129(1):151–155
  49. Ito K, et al. Cigarette smoking reduces histone deacetylase 2 expression, enhances cytokine expression, and inhibits glucocorticoid actions in alveolar macrophages. Faseb J. 2001;15(6):1110–1112
  50. Barnes PJ, Ito K, Adcock IM. Corticosteroid resistance in chronic obstructive pulmonary disease: inactivation of histone deacetylase. Lancet. 2004;363(9410):731–733
  51. Ichinose M, et al. Increase in reactive nitrogen species production in chronic obstructive pulmonary disease airways. Am J Respir Crit Care Med. 2000;162(2 Pt 1):701–706
  52. Green RH, et al. Analysis of induced sputum in adults with asthma: identification of subgroup with isolated sputum neutrophilia and poor response to inhaled corticosteroids. Thorax. 2002;57(10):875–879
  53. Hamid QA, et al. Increased glucocorticoid receptor beta in airway cells of glucocorticoid-insensitive asthma. Am J Respir Crit Care Med. 1999;159(5 Pt 1):1600–1604
  54. Leung DY, et al. Association of glucocorticoid insensitivity with increased expression of glucocorticoid receptor beta. J Exp Med. 1997;186(9):1567–1574
  55. Sousa AR, et al. Glucocorticoid resistance in asthma is associated with elevated in vivo expression of the glucocorticoid receptor beta-isoform. J Allergy Clin Immunol. 2000;105(5):943–950
  56. Leung DY, et al. Dysregulation of interleukin 4, interleukin 5, and interferon gamma gene expression in steroid-resistant asthma. J Exp Med. 1995;181(1):33–40
  57. Sher ER, et al. Steroid-resistant asthma. Cellular mechanisms contributing to inadequate response to glucocorticoid therapy. J Clin Invest. 1994;93(1):33–39
  58. Byron KA, Varigos GA, Wootton AM. IL-4 production is increased in cigarette smokers. Clin Exp Immunol. 1994;95(2):333–336
  59. Churg A, et al. Tumor necrosis factor-alpha is central to acute cigarette smoke-induced inflammation and connective tissue breakdown. Am J Respir Crit Care Med. 2002;166(6):849–854
  60. Strickland I, et al. High constitutive glucocorticoid receptor beta in human neutrophils enables them to reduce their spontaneous rate of cell death in response to corticosteroids. J Exp Med. 2001;193(5):585–593
  61. Webster JC, et al. Proinflammatory cytokines regulate human glucocorticoid receptor gene expression and lead to the accumulation of the dominant negative beta isoform: a mechanism for the generation of glucocorticoid resistance. Proc Natl Acad Sci U S A. 2001;98(12):6865–6870
  62. Bantel H, et al. Critical role of NF-kappaB and stress-activated protein kinases in steroid unresponsiveness. Faseb J. 2002;16(13):1832–1834
  63. Wang JH, et al. Endotoxin/lipopolysaccharide activates NF-kappa B and enhances tumor cell adhesion and invasion through a beta 1 integrin-dependent mechanism. J Immunol. 2003;170(2):795–804
  64. Schaaf MJ, Cidlowski JA. Molecular mechanisms of glucocorticoid action and resistance. J Steroid Biochem Mol Biol. 2002;83(1–5):37–48
  65. Irusen E, et al. p38 Mitogen-activated protein kinase-induced glucocorticoid receptor phosphorylation reduces its activity: role in steroid-insensitive asthma. J Allergy Clin Immunol. 2002;109(4):649–657
  66. Chapman KR, et al. Suboptimal asthma control: prevalence, detection and consequences in general practice. Eur Respir J. 2008;31(2):320–325
  67. Tonnesen P, et al. Effects of smoking cessation and reduction in asthmatics. Nicotine Tob Res. 2005;7(1):139–148
  68. Chaudhuri R, et al. Effects of smoking cessation on lung function and airway inflammation in smokers with asthma. Am J Respir Crit Care Med. 2006;174(2):127–133
  69. Eisner MD, et al. Predictors of cigarette smoking and smoking cessation among adults with asthma. Am J Public Health. 2000;90(8):1307–1311
  70. Jimenez-Ruiz CA, et al. Smoking characteristics: differences in attitudes and dependence between healthy smokers and smokers with COPD. Chest. 2001;119(5):1365–1370
  71. A clinical practice Guideline for treating tobacco Use and dependence: 2008 update: a U.S. Public health Service Report. Am journal Preventive Medicine. 2008;35(2):158–176
  72. Tashkin DP, et al. Effects of varenicline on smoking cessation in patients with mild to moderate COPD: a randomized controlled trial. Chest. 2011;139(3):591–599
  73. Tomlinson JE, et al. Efficacy of low and high dose inhaled corticosteroid in smokers versus non-smokers with mild asthma. Thorax. 2005;60(4):282–287
  74. Burge PS, et al. Randomised, double blind, placebo controlled study of fluticasone propionate in patients with moderate to severe chronic obstructive pulmonary disease: the ISOLDE trial. Bmj. 2000;320(7245):1297–1303
  75. Pedersen SE, et al. Determinants of response to fluticasone propionate and salmeterol/fluticasone propionate combination in the Gaining Optimal Asthma controL study. J Allergy Clin Immunol. 2007;120(5):1036–1042
  76. Calverley P, et al. Combined salmeterol and fluticasone in the treatment of chronic obstructive pulmonary disease: a randomised controlled trial. Lancet. 2003;361(9356):449–456
  77. Barnes PJ. Scientific rationale for inhaled combination therapy with long-acting beta2-agonists and corticosteroids. Eur Respir J. 2002;19(1):182–191
  78. Johnson M, Rennard S. Alternative mechanisms for long-acting beta(2)-adrenergic agonists in COPD. Chest. 2001;120(1):258–270
  79. Peters SP, et al. Tiotropium bromide step-up therapy for adults with uncontrolled asthma. N Engl J Med. 2010;363(18):1715–1726
  80. Lewis RA, et al. Slow reacting substances of anaphylaxis: identification of leukotrienes C-1 and D from human and rat sources. Proc Natl Acad Sci U S A. 1980;77(6):3710–3714
  81. Owen WF, et al. Synthesis and release of leukotriene C4 by human eosinophils. J Immunol. 1987;138(2):532–538
  82. Brown GP, Monick MM, Hunninghake GW. Human alveolar macrophage arachidonic acid metabolism. Am J Physiol. 1988;254(6 Pt 1):C809–C815
  83. Adelroth E, et al. Airway responsiveness to leukotrienes C4 and D4 and to methacholine in patients with asthma and normal controls. N Engl J Med. 1986;315(8):480–484
  84. Marom Z, et al. Slow-reacting substances, leukotrienes C4 and D4, increase the release of mucus from human airways in vitro. Am Rev Respir Dis. 1982;126(3):449–451
  85. Laitinen LA, et al. Leukotriene E4 and granulocytic infiltration into asthmatic airways. Lancet. 1993;341(8851):989–990
  86. Dahlen SE, et al. Leukotrienes promote plasma leakage and leukocyte adhesion in postcapillary venules: in vivo effects with relevance to the acute inflammatory response. Proc Natl Acad Sci U S A. 1981;78(6):3887–3891
  87. Friedman BS, et al. Oral leukotriene inhibitor (MK-886) blocks allergen-induced airway responses. Am Rev Respir Dis. 1993;147(4):839–844
  88. Israel E, et al. The effects of a 5-lipoxygenase inhibitor on asthma induced by cold, dry air. N Engl J Med. 1990;323(25):1740–1744
  89. Manning PJ, et al. Inhibition of exercise-induced bronchoconstriction by MK-571, a potent leukotriene D4-receptor antagonist. N Engl J Med. 1990;323(25):1736–1739
  90. Israel E, et al. The pivotal role of 5-lipoxygenase products in the reaction of aspirin-sensitive asthmatics to aspirin. Am Rev Respir Dis. 1993;148(6 Pt 1):1447–1451
  91. Fauler J, Frolich JC. Cigarette smoking stimulates cysteinyl leukotriene production in man. Eur J Clin Invest. 1997;27(1):43–47
  92. Gaki E, et al. Leukotriene E(4) in urine in patients with asthma and COPD–the effect of smoking habit. Respir Med. 2007;101(4):826–832
  93. Nguyen M, Woo D. Beyond Asthma: a meta-analysis of leukotriene antagonists in the treatment of COPD. Chest. 2008;134(4):106002
  94. Israel E, et al. Effect of treatment with zileuton, a 5-lipoxygenase inhibitor, in patients with asthma. A randomized controlled trial. Zileuton Clinical Trial Group. Jama. 1996;275(12):931–936
  95. Liu MC, Dube LM, Lancaster J. Acute and chronic effects of a 5-lipoxygenase inhibitor in asthma: a 6-month randomized multicenter trial. Zileuton Study Group. J Allergy Clin Immunol. 1996;98(5 Pt 1):859–871
  96. Woodruff PG, et al. Randomized trial of zileuton for treatment of COPD exacerbations requiring hospitalization. COPD. 2011;8(1):21–29
  97. Cosio BG, et al. Theophylline restores histone deacetylase activity and steroid responses in COPD macrophages. J Exp Med. 2004;200(5):689–695
  98. Fox JC, et al. Oral or inhaled corticosteroid combination therapy with low dose theophylline reverses corticosteroid insensitivity in a smoking mouse model. Proc Am Thorac Soc. 2007;2:p. A637(Abstr
  99. Barnes PJ. Role of HDAC2 in the pathophysiology of COPD. Annu Rev Physiol. 2009;71:451–464
  100. Kirkham P, Rahman I. Oxidative stress in asthma and COPD: antioxidants as a therapeutic strategy. Pharmacol Ther. 2006;111(2):476–494
  101. Meja KK, et al. Curcumin restores corticosteroid function in monocytes exposed to oxidants by maintaining HDAC2. Am J Respir Cell Mol Biol. 2008;39(3):312–323
  102. Charron C, et al. EM-703, a non-antibacterial erythromycin derivative, restores HDAC2 activation diminished by hypoxia and oxidative stress. Proc Am Thorac Soc. 2007;175;p. A640(Abstr
  103. Albert RK, et al. Chronic azithromycin decreases the frequency of chronic obstructive pulmonary disease exacerbations. Am J Respir Crit Care Med. 2011;(A6416):183
  104. Evans RM. The steroid and thyroid hormone receptor superfamily. Science. 1988;240(4854):889–895
  105. Belvisi MG, Hele DJ, Birrell MA. Peroxisome proliferator-activated receptor gamma agonists as therapy for chronic airway inflammation. Eur J Pharmacol. 2006;533(1–3):101–109
  106. Matthews L, et al. Thiazolidinediones are partial agonists for the glucocorticoid receptor. Endocrinology. 2009;150(1):75–86
  107. Spears M, et al. Bronchodilatory effect of the PPAR-gamma agonist rosiglitazone in smokers with asthma. Clin Pharmacol Ther. 2009;86(1):49–53
  108. Torphy TJ, et al. Ariflo (SB 207499), a second generation phosphodiesterase 4 inhibitor for the treatment of asthma and COPD: from concept to clinic. Pulm Pharmacol Ther. 1999;12(2):131–135
  109. Grootendorst DC, et al. Reduction in sputum neutrophil and eosinophil numbers by the PDE4 inhibitor roflumilast in patients with COPD. Thorax. 2007;62(12):1081–1087
  110. Renda T, et al. Increased activation of p38 MAPK in COPD. Eur Respir J. 2008;31(1):62–69
  111. Medicherla S, et al. p38alpha-selective mitogen-activated protein kinase inhibitor SD-282 reduces inflammation in a subchronic model of tobacco smoke-induced airway inflammation. J Pharmacol Exp Ther. 2008;324(3):921–929
  112. Erin EM, et al. The effects of a monoclonal antibody directed against tumor necrosis factor-alpha in asthma. Am J Respir Crit Care Med. 2006;174(7):753–762
  113. Rennard SI, et al. The safety and efficacy of infliximab in moderate to severe chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2007;175(9):926–934
  114. Feldmann M, et al. Anti-TNF therapy: where have we got to in 2005?. J Autoimmun. 2005;25(Suppl.):26–28

PII: S0954-6111(11)00390-8

doi: 10.1016/j.rmed.2011.11.003

Respiratory Medicine
Volume 106, Issue 3 , Pages 319-328 , March 2012