Smoking and nonsmoking asthma: Differences in clinical outcome and pathogenesis

Expert Review of Respiratory Medicine

Volumn 5, Issue 1, 2011, Pages 93-105

  Fattahi, Fatemeh ^a   HylkeM A , MacHteld N ^a   Melgert, Barbro N ^b   Timens, Wim ^a   PostM A , Dirkje S ^a   Ten Hacken, Nick Ht ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

airway inflammation; airway remodeling; asthma; corticosteroid unresponsiveness; smoking; smoking cessation

Indexed keywords

BECLOMETASONE; BECLOMETASONE DIPROPIONATE; BUDESONIDE; CYTOKINE; FLUTICASONE; FLUTICASONE PROPIONATE; FLUTICASONE PROPIONATE PLUS SALMETEROL; HEME OXYGENASE 1; INTERLEUKIN 8; PLACEBO; PREDNISOLONE; ROSIGLITAZONE; THEOPHYLLINE;

ASTHMA; CIGARETTE SMOKING; CYTOKINE RELEASE; DISEASE ASSOCIATION; DISEASE SEVERITY; FORCED EXPIRATORY VOLUME; FORCED VITAL CAPACITY; HOSPITAL ADMISSION; HUMAN; INFLAMMATORY CELL; LOW DRUG DOSE; LUNG FUNCTION; LUNG LAVAGE; MAST CELL; MATERNAL SMOKING; NONHUMAN; PATHOGENESIS; PEAK EXPIRATORY FLOW; QUALITY OF LIFE; REVIEW; SMOKING CESSATION; TREATMENT RESPONSE;

EID: 79952144225     PISSN: 17476348     EISSN: 17476356     Source Type: Journal    
DOI: 10.1586/ers.10.85     Document Type: Review

References (128)

1. Thomson NC, Chaudhuri R, Livingston E. Asthma and cigarette smoking. Eur. Respir. J. 24(5), 822-833 (2004). (Pubitemid 39504438)
2. Althuis MD, Sexton M, Prybylski D. Cigarette smoking and asthma symptom severity among adult asthmatics. J. Asthma 36(3), 257-264 (1999). (Pubitemid 29267546)
3. Suzuki K, Tanaka H, Kaneko S et al. Respiratory symptoms and cigarette smoking in 3,197 pulmonologist-based asthmatic patients with a highly prevalent use of inhaled corticosteroid. J. Asthma 40(3), 243-250 (2003). (Pubitemid 36676403)
4. Yoo S, Kim HB, Lee SY et al. Effect of active smoking on asthma symptoms, pulmonary function, and BHR in adolescents. Pediatr. Pulmonol. 44(10), 954-961 (2009).
5. Mitchell I, Tough SC, Semple LK, Green FH, Hessel PA. Near-fatal asthma: a population-based study of risk factors. Chest 121(5), 1407-1413 (2002). (Pubitemid 34499648)
6. LeSon S, Gershwin ME. Risk factors for asthmatic patients requiring intubation. III. Observations in young adults. J. Asthma 33(1), 27-35 (1996). (Pubitemid 26058824)
7. Ryan G, Musk AW, Perera DM, Stock H, Knight JL, Hobbs MS. Risk factors for death in patients admitted to hospital with asthma: a follow-up study. Aust. NZ J. Med. 21(5), 681-685 (1991).
8. Stallberg B, Lisspers K, Hasselgren M, Johansson G, Svardsudd K. Factors related to the level of severity of asthma in primary care. Respir. Med. 101(10), 2076-2083 (2007). (Pubitemid 47324252)
9. Siroux V, Pin I, Oryszczyn MP, Le Moual N, Kauffmann F. 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. 15(3), 470-477 (2000). (Pubitemid 30158183)
10. Chaudhuri R, McSharry C, McCoard A et al. Role of symptoms and lung function in determining asthma control in smokers with asthma. Allergy 63(1), 132-135 (2008). (Pubitemid 350198240)
11. Eisner MD, Iribarren C. The influence of cigarette smoking on adult asthma outcomes. Nicotine Tob. Res. 9(1), 53-56 (2007). (Pubitemid 47009044)
12. Gallefoss F, Bakke PS. Does smoking affect the outcome of patient education and self-management in asthmatics? Patient Educ. Couns. 49(1), 91-97 (2003). (Pubitemid 36071314)
13. Prescott E, Lange P, Vestbo J. Effect of gender on hospital admissions for asthma and prevalence of self-reported asthma: a prospective study based on a sample of the general population. Copenhagen City Heart Study Group. Thorax 52(3), 287-289 (1997). (Pubitemid 27128183)
14. Sippel JM, Pedula KL, Vollmer WM, Buist AS, Osborne ML. Associations of smoking with hospital-based care and quality of life in patients with obstructive airway disease. Chest 115(3), 691-696 (1999). (Pubitemid 29129946)
15. Silverman RA, Boudreaux ED, Woodruff PG, Clark S, Camargo CA Jr. Cigarette smoking among asthmatic adults presenting to 64 emergency departments. Chest 123(5), 1472-1479 (2003). (Pubitemid 36549765)
16. Shavit O, Swern A, Dong Q, Newcomb K, Sazonov Kocevar V, Taylor SD. Impact of smoking on asthma symptoms, healthcare resource use, and quality of life outcomes in adults with persistent asthma. Qual. Life Res. 16(10), 1555-1565 (2007). (Pubitemid 350059906)
17. Patel SN, Tsai CL, Boudreaux ED et al. Multicenter study of cigarette smoking among patients presenting to the emergency department with acute asthma. Ann. Allergy Asthma Immunol. 103(2), 121-127 (2009).
18. Newman RB, Momirova V, Dombrowski MP et al. The effect of active and passive household cigarette smoke exposure on pregnant women with asthma. Chest 137(3), 601-608 (2010).
19. England L, Zhang J. Smoking and risk of preeclampsia: a systematic review. Front Biosci. 12, 2471-2483 (2007).
20. Broekema M, Ten Hacken NH, Volbeda F et al. Airway epithelial changes in smoking but not in ex-smoking asthmatics. Am. J. Respir. Crit. Care Med. 180(12), 1170-1178 (2009).
21. McKay A, Komai-Koma M, Macleod KJ et al. Interleukin-18 levels in induced sputum are reduced in asthmatic and normal smokers. Clin. Exp. Allergy 34(6), 904-910 (2004). (Pubitemid 38824068)
22. Jang AS, Park JS, Lee JH et al. The impact of smoking on clinical and therapeutic effects in asthmatics. J. Korean Med. Sci. 24(2), 209-214 (2009).
23. Boulet LP, Lemiere C, Archambault F, Carrier G, Descary MC, Deschesnes F. Smoking and asthma: clinical and radiologic features, lung function, and airway inflammation. Chest 129(3), 661-668 (2006).
24. Mitsunobu F, Ashida K, Hosaki Y et al. Influence of long-term cigarette smoking on immunoglobulin E-mediated allergy, pulmonary function, and high-resolution computed tomography lung densitometry in elderly patients with asthma. Clin. Exp. Allergy 34(1), 59-64 (2004). (Pubitemid 38183681)
25. Lynch DA, Newell JD, Tschomper BA, Cink TM, Newman LS, Bethel R. Uncomplicated asthma in adults: comparison of CT appearance of the lungs in asthmatic and healthy subjects. Radiology 188(3), 829-833 (1993). (Pubitemid 23254612)
26. Roorda RJ, Gerritsen J, van Aalderen WM et al. Follow-up of asthma from childhood to adulthood: influence of potential childhood risk factors on the outcome of pulmonary function and bronchial responsiveness in adulthood. J. Allergy Clin. Immunol. 93(3), 575-584 (1994). (Pubitemid 24105062)
27. Postma DS, Lebowitz MD. Persistence and new onset of asthma and chronic bronchitis evaluated longitudinally in a community population sample of adults. Arch. Intern. Med. 155(13), 1393-1399 (1995).
28. Almind M, Viskum K, Evald T, Dirksen A, Kok-Jensen A. A seven-year follow-up study of 343 adults with bronchial asthma. Dan. Med. Bull. 39(6), 561-565 (1992).
29. Ulrik CS. Outcome of asthma: longitudinal changes in lung function. Eur. Respir. J. 13(4), 904-918 (1999). (Pubitemid 29234799)
30. Lange P, Parner J, Vestbo J, Schnohr P, Jensen G. A 15-year follow-up study of ventilatory function in adults with asthma. N. Engl. J. Med. 339(17), 1194-1200 (1998).
31. Peat JK, Woolcock AJ, Cullen K. Rate of decline of lung function in subjects with asthma. Eur. J. Respir. Dis. 70(3), 171-179 (1987). (Pubitemid 17029522)
32. Ulrik CS, Backer V, Dirksen A. A 10 year follow up of 180 adults with bronchial asthma: factors important for the decline in lung function. Thorax 47(1), 14-18 (1992).
33. Apostol GG, Jacobs DR Jr, Tsai AW 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. 166(2), 166-172 (2002). (Pubitemid 34765452)
34. Chalmers GW, Macleod KJ, Little SA, Thomson LJ, McSharry CP, Thomson NC. Influence of cigarette smoking on inhaled corticosteroid treatment in mild asthma. Thorax 57(3), 226-230 (2002). (Pubitemid 34214408)
35. Lazarus SC, Chinchilli VM, Rollings NJ et al. Smoking affects response to inhaled corticosteroids or leukotriene receptor antagonists in asthma. Am. J. Respir. Crit. Care Med. 175(8), 783-790 (2007). (Pubitemid 46631789)
36. Tomlinson JE, McMahon AD, Chaudhuri R, Thompson JM, Wood SF, Thomson NC. Efficacy of low and high dose inhaled corticosteroid in smokers versus non-smokers with mild asthma. Thorax 60(4), 282-287 (2005). (Pubitemid 40522363)
37. Pedersen B, Dahl R, Karlstrom R, Peterson CG, Venge P. Eosinophil and neutrophil activity in asthma in a one-year trial with inhaled budesonide. The impact of smoking. Am. J. Respir. Crit. Care Med. 153(5), 1519-1529 (1996). (Pubitemid 26141335)
38. Pedersen SE, Bateman ED, Bousquet J, Busse WW, Yoxall S, Clark TJ. Determinants of response to fluticasone propionate and salmeterol/fluticasone propionate combination in the Gaining Optimal Asthma Control study. J. Allergy Clin. Immunol. 120(5), 1036-1042 (2007). (Pubitemid 350029898)
39. Dijkstra A, Vonk JM, Jongepier H et al. Lung function decline in asthma: association with inhaled corticosteroids, smoking and sex. Thorax 61(2), 105-110 (2006). (Pubitemid 43235425)
40. Adams RJ, Weiss ST, Fuhlbrigge A. How and by whom care is delivered influences anti-inflammatory use in asthma: results of a national population survey. J. Allergy Clin. Immunol. 112(2), 445-450 (2003). (Pubitemid 36981389)
41. Chaudhuri R, Livingston E, McMahon AD, Thomson L, Borland W, Thomson NC. Cigarette smoking impairs the therapeutic response to oral corticosteroids in chronic asthma. Am. J. Respir. Crit. Care Med. 168(11), 1308-1311 (2003). (Pubitemid 37487324)
42. Livingston E, Chaudhuri R, McMahon AD, Fraser I, McSharry CP, Thomson NC. Systemic sensitivity to corticosteroids in smokers with asthma. Eur. Respir. J. 29(1), 64-71 (2007).
43. Chalmers GW, Macleod KJ, Thomson L, Little SA, McSharry C, Thomson NC. Smoking and airway inflammation in patients with mild asthma. Chest 120(6), 1917-1922 (2001). (Pubitemid 34053454)
44. Cowan DC, Cowan JO, Palmay R, Williamson A, Taylor DR. Effects of steroid therapy on inflammatory cell subtypes in asthma. Thorax 65(5), 384-390 (2010).
45. Adenuga D, Rahman I. Oxidative stress, histone deacetylase and corticosteroid resistance in severe asthma and COPD. Curr. Respir. Med. Rev. 3(1), 57-68 (2007). (Pubitemid 46358532)
46. Livingston E, Darroch CE, Chaudhuri R et al. Glucocorticoid receptor a:b ratio in blood mononuclear cells is reduced in cigarette smokers. J. Allergy Clin. Immunol. 114(6), 1475-1478 (2004). (Pubitemid 39575910)
47. Spears M, Donnelly I, Jolly L et al. Effect of low-dose theophylline plus beclometasone on lung function in smokers with asthma: a pilot study. Eur. Respir. J. 33(5), 1010-1017 (2009).
48. Spears M, Donnelly I, Jolly L et al. Bronchodilatory effect of the PPAR-g agonist rosiglitazone in smokers with asthma. Clin. Pharmacol. Ther. 86(1), 49-53 (2009).
49. Balzano G, Stefanelli F, Iorio C et al. Eosinophilic inflammation in stable chronic obstructive pulmonary disease. Relationship with neutrophils and airway function. Am. J. Respir. Crit. Care Med. 160(5 Pt 1), 1486-1492 (1999).
50. Dippolito R, Foresi A, Chetta A et al. Eosinophils in induced sputum from asymptomatic smokers with normal lung function. Respir. Med. 95(12), 969-974 (2001). (Pubitemid 34013545)
51. Hunninghake GW, Crystal RG. Cigarette smoking and lung destruction. Accumulation of neutrophils in the lungs of cigarette smokers. Am. Rev. Respir. Dis. 128(5), 833-838 (1983). (Pubitemid 14231334)
52. Costabel U, Bross KJ, Reuter C, Ruhle KH, Matthys H. Alterations in immunoregulatory T-cell subsets in cigarette smokers. A phenotypic analysis of bronchoalveolar and blood lymphocytes. Chest 90(1), 39-44 (1986). (Pubitemid 16099943)
53. Kuschner WG, DAlessandro A, Wong H, Blanc PD. Dose-dependent cigarette smoking-related inflammatory responses in healthy adults. Eur. Respir. J. 9(10), 1989-1994 (1996). (Pubitemid 26333532)
54. Roth MD, Arora A, Barsky SH, Kleerup EC, Simmons M, Tashkin DP. Airway inflammation in young marijuana and tobacco smokers. Am. J. Respir. Crit. Care Med. 157(3 Pt 1), 928-937 (1998).
55. Amin K, Ekberg-Jansson A, Lofdahl CG, Venge P. Relationship between inflammatory cells and structural changes in the lungs of asymptomatic and never smokers: a biopsy study. Thorax 58(2), 135-142 (2003). (Pubitemid 36183001)
56. Lams BE, Sousa AR, Rees PJ, Lee TH. Immunopathology of the small-airway submucosa in smokers with and without chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 158(5 Pt 1), 1518-1523 (1998).
57. Culpitt SV, Rogers DF, Shah P et al. Impaired inhibition by dexamethasone of cytokine release by alveolar macrophages from patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 167(1), 24-31 (2003). (Pubitemid 36015913)
58. Kent L, Smyth L, Clayton C et al. Cigarette smoke extract induced cytokine and chemokine gene expression changes in COPD macrophages. Cytokine 42(2), 205-216 (2008).
59. Cohn L, Elias JA, Chupp GL. Asthma: mechanisms of disease persistence and progression. Annu. Rev. Immunol. 22, 789-815 (2004). (Pubitemid 38680442)
60. Kanazawa H, Asai K, Tochino Y, Kyoh S, Kodama T, Hirata K. Increased levels of angiopoietin-2 in induced sputum from smoking asthmatic patients. Clin. Exp. Allergy 39(9), 1330-1337 (2009).
61. Krisiukeniene A, Babusyte A, Stravinskaite K, Lotvall J, Sakalauskas R, Sitkauskiene B. Smoking affects eotaxin levels in asthma patients. J. Asthma 46(5), 470-476 (2009).
62. Rovina N, Dima E, Gerassimou C, Kollintza A, Gratziou C, Roussos C. IL-18 in induced sputum and airway hyperresponsiveness in mild asthmatics: effect of smoking. Respir. Med. 103(12), 1919-1925 (2009).
63. Small-Howard A, Turner H. Exposure to tobacco-derived materials induces overproduction of secreted proteinases in mast cells. Toxicol. Appl. Pharmacol. 204(2), 152-163 (2005). (Pubitemid 40432372)
64. Tsoumakidou M, Elston W, Zhu J et al. Cigarette smoking alters bronchial mucosal immunity in asthma. Am. J. Respir. Crit. Care Med. 175(9), 919-925 (2007). (Pubitemid 46684702)
65. Seow WK, Thong YH, Nelson RD, MacFarlane GD, Herzberg MC. Nicotine-induced release of elastase and eicosanoids by human neutrophils. Inflammation 18(2), 119-127 (1994). (Pubitemid 24186997)
66. Sunyer J, Springer G, Jamieson B et al. Effects of asthma on cell components in peripheral blood among smokers and non-smokers. Clin. Exp. Allergy 33(11), 1500-1505 (2003). (Pubitemid 37421626)
67. Taylor RG, Gross E, Joyce H, Holland F, Pride NB. Smoking, allergy, and the differential white blood cell count. Thorax 40(1), 17-22 (1985). (Pubitemid 15110825)
68. Jensen EJ, Pedersen B, Narvestadt E, Dahl R. Blood eosinophil and monocyte counts are related to smoking and lung function. Respir. Med. 92(1), 63-69 (1998). (Pubitemid 28112044)
69. Melgert BN, Postma DS, Geerlings M et al. Short-term smoke exposure attenuates ovalbumin-induced airway inflammation in allergic mice. Am. J. Respir. Cell Mol. Biol. 30(6), 880-885 (2004). (Pubitemid 38736913)
70. Peters-Golden M. The alveolar macrophage: the forgotten cell in asthma. Am. J. Respir. Cell. Mol. Biol. 31(1), 3-7 (2004). (Pubitemid 38888032)
71. Melgert BN, Oriss TB, Qi Z et al. Macrophages: regulators of sex differences in asthma? Am. J. Respir. Cell Mol. Biol. 42(5), 595-603 (2010).
72. Holt PG, Oliver J, Bilyk N et al. Downregulation of the antigen presenting cell function(s) of pulmonary dendritic cells in vivo by resident alveolar macrophages. J. Exp. Med. 177(2), 397-407 (1993). (Pubitemid 23117089)
73. Korf JE, Pynaert G, Tournoy K et al. Macrophage reprogramming by mycolic acid promotes a tolerogenic response in experimental asthma. Am. J. Respir. Crit. Care Med. 174(2), 152-160 (2006). (Pubitemid 44015388)
74. Goleva E, Hauk PJ, Hall CF et al. Corticosteroid-resistant asthma is associated with classical antimicrobial activation of airway macrophages. J. Allergy Clin. Immunol. 122(3), 550-559 (2008).
75. Kane B, Kolsum U, Southworth T, Armstrong J, Woodcock A, Singh D. The effects of smoking on the lipopolysaccharide response and glucocorticoid sensitivity of alveolar macrophages of patients with asthma. Chest 136(1), 163-170 (2009).
76. Kelly C, Ward C, Stenton CS, Bird G, Hendrick DJ, Walters EH. Number and activity of inflammatory cells in bronchoalveolar lavage fluid in asthma and their relation to airway responsiveness. Thorax 43(9), 684-692 (1988).
77. Melgert BN, Timens W, Kerstjens HA et al. Effects of 4 months of smoking in mice with ovalbumin-induced airway inflammation. Clin. Exp. Allergy 37(12), 1798-1808 (2007). (Pubitemid 350145340)
78. Moerloose KB, Pauwels RA, Joos GF. Short-term cigarette smoke exposure enhances allergic airway inflammation in mice. Am. J. Respir. Crit. Care Med. 172(2), 168-172 (2005). (Pubitemid 40981189)
79. Sjaheim T, Kongerud J, Bjortuft O, Drablos PA, Malterud D, Halstensen TS. Reduced bronchial CD4+ T-cell density in smokers with occupational asthma. Eur. Respir. J. 28(6), 1138-1144 (2006). (Pubitemid 44883848)
80. Van Hal PT, Overbeek SE, Hoogsteden HC et al. Eicosanoids and lipocortin-1 in BAL fluid in asthma: effects of smoking and inhaled glucocorticoids. J. Appl. Physiol. 81(2), 548-555 (1996). (Pubitemid 26303202)
81. Barnes PJ. Alveolar macrophages in chronic obstructive pulmonary disease (COPD). Cell. Mol. Biol. (Noisy-le-grand) 50 Online Pub., OL627-OL637 (2004).
82. Doyle I, Ratcliffe M, Walding A et al. Differential gene expression analysis in human monocyte-derived macrophages: impact of cigarette smoke on host defence. Mol. Immunol. 47(5), 1058-1065 (2010).
83. Harris JO, Gonzalez-Rothi RJ. Abnormal phagolysosome fusion in pulmonary alveolar macrophages of rats exposed chronically to cigarette smoke. Am. Rev. Respir. Dis. 130(3), 467-471 (1984). (Pubitemid 14029779)
84. Hodge S, Hodge G, Scicchitano R, Reynolds PN, Holmes M. Alveolar macrophages from subjects with chronic obstructive pulmonary disease are deficient in their ability to phagocytose apoptotic airway epithelial cells. Immunol. Cell. Biol. 81(4), 289-296 (2003). (Pubitemid 36904336)
85. King TE Jr, Savici D, Campbell PA. Phagocytosis and killing of Listeria monocytogenes by alveolar macrophages: smokers versus nonsmokers. J. Infect. Dis. 158(6), 1309-1316 (1988). (Pubitemid 19023296)
86. Kirkham PA, Spooner G, Rahman I, Rossi AG. Macrophage phagocytosis of apoptotic neutrophils is compromised by matrix proteins modified by cigarette smoke and lipid peroxidation products. Biochem. Biophys. Res. Commun. 318(1), 32-37 (2004). (Pubitemid 38526241)
87. Ortega E, Hueso F, Collazos ME, Pedrera MI, Barriga C, Rodriguez AB. Phagocytosis of latex beads by alveolar macrophages from mice exposed to cigarette smoke. Comp Immunol. Microbiol. Infect. Dis. 15(2), 137-142 (1992).
88. Ortega E, Barriga C, Rodriguez AB. Decline in the phagocytic function of alveolar macrophages from mice exposed to cigarette smoke. Comp. Immunol. Microbiol. Infect. Dis. 17(1), 77-84 (1994). (Pubitemid 24109246)
89. Lim S, Roche N, Oliver BG, Mattos W, Barnes PJ, Chung KF. Balance of matrix metalloprotease-9 and tissue inhibitor of metalloprotease-1 from alveolar macrophages in cigarette smokers. Regulation by interleukin-10. Am. J. Respir. Crit. Care Med. 162(4 Pt 1), 1355-1360 (2000).
90. Mehta H, Nazzal K, Sadikot RT. Cigarette smoking and innate immunity. Inflamm. Res. 57(11), 497-503 (2008).
91. Shaykhiev R, Krause A, Salit J et al. Smoking-dependent reprogramming of alveolar macrophage polarization: implication for pathogenesis of chronic obstructive pulmonary disease. J. Immunol. 183(4), 2867-2883 (2009).
92. Agapov E, Battaile JT, Tidwell R et al. Macrophage chitinase 1 stratifies chronic obstructive lung disease. Am. J. Respir. Cell. Mol. Biol. 41(4), 379-384 (2009).
93. Seibold MA, Donnelly S, Solon M et al. Chitotriosidase is the primary active chitinase in the human lung and is modulated by genotype and smoking habit. J. Allergy Clin. Immunol. 122(5), 944-950 (2008).
94. Knobloch J, Schild K, Jungck D et al. The T-helper cell type 1-immune response to Gram-negative bacterial infections is impaired in COPD. Am. J. Respir. Crit. Care Med. DOI: 10.1164/rccm.201002- 0199OC (2010) (Epub ahead of print).
95. Venarske DL, Busse WW, Griffin MR et al. The relationship of rhinovirus-associated asthma hospitalizations with inhaled corticosteroids and smoking. J. Infect. Dis. 193(11), 1536-1543 (2006). (Pubitemid 43794583)
96. Nuorti JP, Butler JC, Farley MM et al. Cigarette smoking and invasive pneumococcal disease. Active Bacterial Core Surveillance Team. N. Engl. J. Med. 342(10), 681-689 (2000). (Pubitemid 30131420)
97. Bagaitkar J, Demuth DR, Scott DA. Tobacco use increases susceptibility to bacterial infection. Tob. Induc. Dis. 4, 12 (2008).
98. Zhang X, Msc, Moilanen E et al. Regulation of eosinophil apoptosis by nitric oxide: role of c-Jun-N-terminal kinase and signal transducer and activator of transcription 5. J. Allergy Clin. Immunol. 112(1), 93-101 (2003). (Pubitemid 36819813)
99. Verleden GM, Dupont LJ, Verpeut AC, Demedts MG. The effect of cigarette smoking on exhaled nitric oxide in mild steroid-naive asthmatics. Chest 116(1), 59-64 (1999). (Pubitemid 29340261)
100. Sopori M. Effects of cigarette smoke on the immune system. Nat. Rev. Immunol. 2(5), 372-377 (2002). (Pubitemid 37328760)
101. Wang H, Yu M, Ochani M et al. Nicotinic acetylcholine receptor a7 subunit is an essential regulator of inflammation. Nature 421(6921), 384-388 (2003). (Pubitemid 36157937)
102. Mishra NC, Rir-Sima-Ah J, Langley RJ et al. Nicotine primarily suppresses lung Th2 but not goblet cell and muscle cell responses to allergens. J. Immunol. 180(11), 7655-7663 (2008).
103. van der Vaart H, Postma DS, Timens W et al. Acute effects of cigarette smoking on inflammation in healthy intermittent smokers. Respir. Res. 6, 22 (2005).
104. van der Vaart H, Postma DS, Timens W, Ten Hacken NH. Acute effects of cigarette smoke on inflammation and oxidative stress: a review. Thorax 59(8), 713-721 (2004). (Pubitemid 39061538)
105. Choi AM, Alam J. Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am. J. Respir. Cell Mol. Biol. 15(1), 9-19 (1996). (Pubitemid 126439851)
106. Yamamoto C, Yoneda T, Yoshikawa M et al. Airway inflammation in COPD assessed by sputum levels of interleukin-8. Chest 112(2), 505-510 (1997). (Pubitemid 27349446)
107. Kubo S, Kobayashi M, Masunaga Y et al. Cytokine and chemokine expression in cigarette smoke-induced lung injury in guinea pigs. Eur. Respir. J. 26(6), 993-1001 (2005). (Pubitemid 41829928)
108. Rothenberg ME, Hogan SP. The eosinophil. Ann. Rev. Immunol. 24, 147-174 (2006).
109. Kim V, Rogers TJ, Criner GJ. New concepts in the pathobiology of chronic obstructive pulmonary disease. Proc. Am. Thorac. Soc. 5(4), 478-485 (2008). (Pubitemid 351669174)
110. Lee JJ, Liu D, Lee JS et al. Long-term impact of smoking on lung epithelial proliferation in current and former smokers. J. Natl Cancer Inst. 93(14), 1081-1088 (2001). (Pubitemid 32717540)
111. Miller LG, Goldstein G, Murphy M, Ginns LC. Reversible alterations in immunoregulatory T cells in smoking. Analysis by monoclonal antibodies and flow cytometry. Chest 82(5), 526-529 (1982). (Pubitemid 13234177)
112. Puchelle E, Zahm JM, Tournier JM, Coraux C. Airway epithelial repair, regeneration, and remodeling after injury in chronic obstructive pulmonary disease. Proc. Am. Thorac. Soc. 3(8), 726-733 (2006). (Pubitemid 44788232)
113. Nakamura Y, Miyata M, Ohba T et al. Cigarette smoke extract induces thymic stromal lymphopoietin expression, leading to T(H)2-type immune responses and airway inflammation. J. Allergy Clin. Immunol. 122(6), 1208-1214 (2008).
114. Ito T, Wang YH, Duramad O et al. TSLP-activated dendritic cells induce an inflammatory T helper type 2 cell response through OX40 ligand. J. Exp. Med. 202(9), 1213-1223 (2005). (Pubitemid 41586952)
115. Allakhverdi Z, Comeau MR, Jessup HK et al. Thymic stromal lymphopoietin is released by human epithelial cells in response to microbes, trauma, or inflammation and potently activates mast cells. J. Exp. Med. 204(2), 253-258 (2007). (Pubitemid 46294541)
116. Bradding P, Walls AF, Holgate ST. The role of the mast cell in the pathophysiology of asthma. J. Allergy Clin. Immunol. 117(6), 1277-1284 (2006). (Pubitemid 43795741)
117. Feleszko W, Zawadzka-Krajewska A, Matysiak K et al. Parental tobacco smoking is associated with augmented IL-13 secretion in children with allergic asthma. J. Allergy Clin. Immunol. 117(1), 97-102 (2006). (Pubitemid 43017146)
118. Bergeron C, Boulet LP, Page N et al. Influence of cigarette smoke on the arginine pathway in asthmatic airways: increased expression of arginase I. J. Allergy Clin. Immunol. 119(2), 391-397 (2007). (Pubitemid 46204814)
119. Carroll NG, Perry S, Karkhanis A et al. The airway longitudinal elastic fiber network and mucosal folding in patients with asthma. Am. J. Respir. Crit. Care Med. 161(1), 244-248 (2000). (Pubitemid 30055932)
120. St Laurent J, Bergeron C, Page N, Couture C, Laviolette M, Boulet LP. Influence of smoking on airway inflammation and remodelling in asthma. Clin. Exp. Allergy 38(10), 1582-1589 (2008).
121. Eisner MD, Yelin EH, Katz PP, Shiboski SC, Henke J, Blanc PD. Predictors of cigarette smoking and smoking cessation among adults with asthma. Am. J. Public Health 90(8), 1307-1311 (2000). (Pubitemid 30497389)
122. King G, Polednak AP, Gilreath T, Bendel RB. Disparities in smoking cessation among U.S. adults with a history of asthma. Ann. Behav. Med. 33(3), 312-317 (2007). (Pubitemid 47041350)
123. Wakefield M, Ruffin R, Campbell D, Roberts L, Wilson D. Smoking-related beliefs and behaviour among adults with asthma in a representative population sample. Aust. NZ J. Med. 25(1), 12-17 (1995).
124. Chapman KR, Boulet LP, Rea RM, Franssen E. Suboptimal asthma control: prevalence, detection and consequences in general practice. Eur. Respir. J. 31(2), 320-325 (2008).
125. Chaudhuri R, Livingston E, McMahon AD et al. Effects of smoking cessation on lung function and airway inflammation in smokers with asthma. Am. J. Respir. Crit. Care Med. 174(2), 127-133 (2006). (Pubitemid 44015385)
126. Tonnesen P, Pisinger C, Hvidberg S et al. Effects of smoking cessation and reduction in asthmatics. Nicotine Tob. Res. 7(1), 139-148 (2005). (Pubitemid 40613171)
127. Fennerty AG, Banks J, Ebden P, Bevan C. The effect of cigarette withdrawal on asthmatics who smoke. Eur. J. Respir. Dis. 71(5), 395-399 (1987). (Pubitemid 18018874)
128. Global Strategy for Asthma Management and Prevention. Global Initiative for Asthma (updated 2009) www.ginasthma.org/Guidelineitem. aspl1=2&l2= 1&intId=1561