Rheumatology International

, Volume 33, Issue 4, pp 943–948

Does cigarette smoking mitigate the severity of skin disease in systemic sclerosis?

  • Geneviève Gyger
  • Marie Hudson
  • Ernest Lo
  • Russell Steele
  • Canadian Scleroderma Research Group (CSRG)
  • Murray Baron
Original Article

Abstract

Cigarette smoking has significant negative effects on vascular, pulmonary and gastrointestinal outcomes in systemic sclerosis (SSc). The objective of this study was to study the effect of cigarette smoking on the extent of skin disease in SSc. Subjects were patients enrolled in the Canadian Scleroderma Research Group cohort. Smoking history was obtained by patient self-reports. The extent of skin involvement was measured using the modified Rodnan skin score. The effect of smoking on the skin score was assessed using the comprehensive smoking index (CSI), which integrates smoking intensity, duration and time since cessation into a single covariate of smoking effect. The regression model was adjusted for gender, ethnicity and disease duration. This study included 606 SSc patients, of which 87 % were women and 90 % were white; mean disease duration was 11 (±9) years, and mean modified Rodnan skin score was 10 (±9). Of these, 16 % were current, 42 % past and 42 % never smokers. There was a 16 % reduction in skin score (odds ratio 0.84, 95 % confidence interval 0.75, 0.95, p = 0.0029) for every 0.1 unit change in CSI. The effect of smoking on skin disease appeared cumulative and irreversible. Smoking was significantly associated with less extensive skin disease in SSc. This hypothesis-generating study provides new avenues of research, especially insofar as the role of nicotine in SSc is concerned and given that safe nicotine replacement therapy exists.

Keywords

Scleroderma Systemic sclerosis Skin Smoking Comprehensive smoking index 

References

  1. 1.
    Siebold J (2005) Scleroderma. In: Harris E, Budd R, Firestein G, Genovese M, Sergent J, Ruddy S (eds) Kelley’s textbook of rheumatology, 7th edn. Elsevier, PhiladelphiaGoogle Scholar
  2. 2.
    LeRoy EC, Black C, Fleischmajer R et al (1988) Scleroderma (systemic sclerosis): classification, subsets and pathogenesis. J Rheumatol 15:202–205PubMedGoogle Scholar
  3. 3.
    Hudson M, Lo E, Lu Y, Hercz D, Baron M, Steele R (2010) Cigarette smoking in patients with systemic sclerosis. Arthritis Rheum 63:230–238CrossRefGoogle Scholar
  4. 4.
    Clements P, Lachenbruch P, Siebold J et al (1995) Inter and intraobserver variability of total skin thickness score (modified Rodnan TSS) in systemic sclerosis. J Rheumatol 22:1281–1285PubMedGoogle Scholar
  5. 5.
    Leffondre K, Abrahamowicz M, Xiao Y, Siemiatycki J (2006) Modelling smoking history using a comprehensive smoking index: application to lung cancer. Stat Med 25:4132–4146PubMedCrossRefGoogle Scholar
  6. 6.
    Hudson M, Lo E, Baron M, Steele R (2011) Modeling smoking in systemic sclerosis: a comparison of different statistical approaches. Arthritis Care Res (Hoboken) 63(4):570–578Google Scholar
  7. 7.
    McCullagh P, Nelder J (1989) Generalized linear models, 2nd edn. Chapman and Hall/CRC, Boca RatonGoogle Scholar
  8. 8.
    R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  9. 9.
    Smith JB, Fenske NA (1996) Cutaneous manifestations and consequences of smoking [see comments]. J Am Acad Dermatol 34:717–732; quiz 33–34Google Scholar
  10. 10.
    Sonnenfeld G, Hudgens RW (1983) Effect of carcinogenic components of cigarette smoke on in vivo production of murine interferon. Cancer Res 43:4720–4722PubMedGoogle Scholar
  11. 11.
    Bartsch H, Malaveille C, Friesen M, Kadlubar FF, Vineis P (1993) Black (air-cured) and blond (flue-cured) tobacco cancer risk. IV: molecular dosimetry studies implicate aromatic amines as bladder carcinogens. Eur J Cancer 29A:1199–1207PubMedCrossRefGoogle Scholar
  12. 12.
    Penn A, Chen LC, Snyder CA (1994) Inhalation of steady-state sidestream smoke from one cigarette promotes arteriosclerotic plaque development. Circulation 90:1363–1367PubMedCrossRefGoogle Scholar
  13. 13.
    Stefanadis C, Tsiamis E, Vlachopoulos C et al (1997) Unfavorable effect of smoking on the elastic properties of the human aorta. Circulation 95:31–38PubMedCrossRefGoogle Scholar
  14. 14.
    Schafer T, Dirschedl P, Kunz B, Ring J, Uberla K (1997) Maternal smoking during pregnancy and lactation increases the risk for atopic eczema in the offspring. J Am Acad Dermatol 36:550–556PubMedCrossRefGoogle Scholar
  15. 15.
    Solly S (1856) Clinical lectures on paralysis. Lancet 68(1737):641–643Google Scholar
  16. 16.
    Chung JH, Lee SH, Youn CS et al (2001) Cutaneous photodamage in Koreans: influence of sex, sun exposure, smoking, and skin color. Arch Dermatol 137:1043–1051PubMedGoogle Scholar
  17. 17.
    Ernster VL, Grady D, Miike R, Black D, Selby J, Kerlikowske K (1995) Facial wrinkling in men and women, by smoking status. Am J Public Health 85:78–82PubMedCrossRefGoogle Scholar
  18. 18.
    Kadunce DP, Burr R, Gress R, Kanner R, Lyon JL, Zone JJ (1991) Cigarette smoking: risk factor for premature facial wrinkling. Ann Intern Med 114:840–844PubMedGoogle Scholar
  19. 19.
    Raduan AP, Luiz RR, Manela-Azulay M (2008) Association between smoking and cutaneous ageing in a Brazilian population. J Eur Acad Dermatol Venereol 22:1312–1318PubMedCrossRefGoogle Scholar
  20. 20.
    Freiman A, Bird G, Metelitsa AI, Barankin B, Lauzon GJ (2004) Cutaneous effects of smoking. J Cutan Med Surg 8:415–423PubMedCrossRefGoogle Scholar
  21. 21.
    Misery L (2004) Nicotine effects on skin: are they positive or negative? Exp Dermatol 13:665–670PubMedCrossRefGoogle Scholar
  22. 22.
    Metelitsa AI, Lauzon GJ (2010) Tobacco and the skin. Clin Dermatol 28:384–390PubMedCrossRefGoogle Scholar
  23. 23.
    Morita A (2007) Tobacco smoke causes premature skin aging. J Dermatol Sci 48:169–175PubMedCrossRefGoogle Scholar
  24. 24.
    Arredondo J, Hall LL, Ndoye A et al (2003) Central role of fibroblast alpha3 nicotinic acetylcholine receptor in mediating cutaneous effects of nicotine. Lab Invest 83:207–225PubMedGoogle Scholar
  25. 25.
    Jorgensen LN, Kallehave F, Christensen E, Siana JE, Gottrup F (1998) Less collagen production in smokers. Surgery 123:450–455PubMedCrossRefGoogle Scholar
  26. 26.
    Yin L, Morita A, Tsuji T (2000) Alterations of extracellular matrix induced by tobacco smoke extract. Arch Dermatol Res 292:188–194PubMedCrossRefGoogle Scholar
  27. 27.
    Yin L, Morita A, Tsuji T (2003) Tobacco smoke extract induces age-related changes due to modulation of TGF-beta. Exp Dermatol 12(Suppl 2):51–56PubMedCrossRefGoogle Scholar
  28. 28.
    Thomsen SF, Sorensen LT (2010) Smoking and skin disease. Skin Therapy Lett 15:4–7PubMedGoogle Scholar
  29. 29.
    Gabrielli A, Avvedimento EV, Krieg T (2009) Scleroderma. N Engl J Med 360:1989–2003PubMedCrossRefGoogle Scholar
  30. 30.
    Mills CM (1998) Cigarette smoking, cutaneous immunity, and inflammatory response. Clin Dermatol 16:589–594PubMedCrossRefGoogle Scholar
  31. 31.
    Kalra R, Singh SP, Pena-Philippides JC, Langley RJ, Razani-Boroujerdi S, Sopori ML (2004) Immunosuppressive and anti-inflammatory effects of nicotine administered by patch in an animal model. Clin Diagn Lab Immunol 11:563–568PubMedGoogle Scholar
  32. 32.
    Sopori ML, Kozak W, Savage SM et al (1998) Effect of nicotine on the immune system: possible regulation of immune responses by central and peripheral mechanisms. Psychoneuroendocrinology 23:189–204PubMedCrossRefGoogle Scholar
  33. 33.
    Yamaguchi E, Okazaki N, Itoh A, Abe S, Kawakami Y, Okuyama H (1989) Interleukin 1 production by alveolar macrophages is decreased in smokers. Am Rev Respir Dis 140:397–402PubMedCrossRefGoogle Scholar
  34. 34.
    Savage SM, Donaldson LA, Cherian S, Chilukuri R, White VA, Sopori ML (1991) Effects of cigarette smoke on the immune response. II. Chronic exposure to cigarette smoke inhibits surface immunoglobulin-mediated responses in B cells. Toxicol Appl Pharmacol 111:523–529PubMedCrossRefGoogle Scholar
  35. 35.
    Moszczynski P, Zabinski Z, Moszczynski P Jr, Rutowski J, Slowinski S, Tabarowski Z (2001) Immunological findings in cigarette smokers. Toxicol Lett 118:121–127PubMedCrossRefGoogle Scholar
  36. 36.
    Kanekura T, Usuki K, Kanzaki T (2004) Skin disorders with prominent eosinophilic infiltration treated successfully with nicotine. Report of two cases. Dermatology 208:153–157PubMedCrossRefGoogle Scholar
  37. 37.
    Kanekura T, Usuki K, Kanzaki T (1995) Nicotine for pyoderma gangrenosum. Lancet 345:1058PubMedCrossRefGoogle Scholar
  38. 38.
    Kanekura T, Kanzaki T (1999) Successful treatment of orogenital ulceration with transdermal nicotine patches. Br J Dermatol 141:1140–1141PubMedCrossRefGoogle Scholar
  39. 39.
    Calkins BM (1989) A meta-analysis of the role of smoking in inflammatory bowel disease. Dig Dis Sci 34:1841–1854PubMedCrossRefGoogle Scholar
  40. 40.
    Cooke JP (2007) Angiogenesis and the role of the endothelial nicotinic acetylcholine receptor. Life Sci 80:2347–2351PubMedCrossRefGoogle Scholar
  41. 41.
    Mousa S, Mousa SA (2006) Cellular and molecular mechanisms of nicotine’s pro-angiogenesis activity and its potential impact on cancer. J Cell Biochem 97:1370–1378PubMedCrossRefGoogle Scholar
  42. 42.
    Heeschen C, Chang E, Aicher A, Cooke JP (2006) Endothelial progenitor cells participate in nicotine-mediated angiogenesis. J Am Coll Cardiol 48:2553–2560PubMedCrossRefGoogle Scholar
  43. 43.
    Wang X, Zhu J, Chen J, Shang Y (2004) Effects of nicotine on the number and activity of circulating endothelial progenitor cells. J Clin Pharmacol 44:881–889PubMedCrossRefGoogle Scholar
  44. 44.
    Joseph AM, Norman SM, Ferry LH et al (1996) The safety of transdermal nicotine as an aid to smoking cessation in patients with cardiac disease. N Engl J Med 335:1792–1798PubMedCrossRefGoogle Scholar
  45. 45.
    Mahmarian JJ, Moye LA, Nasser GA et al (1997) Nicotine patch therapy in smoking cessation reduces the extent of exercise-induced myocardial ischemia. J Am Coll Cardiol 30:125–130PubMedCrossRefGoogle Scholar
  46. 46.
    Martin JW, Mousa SS, Shaker O, Mousa SA (2009) The multiple faces of nicotine and its implications in tissue and wound repair. Exp Dermatol 18:497–505PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Geneviève Gyger
    • 1
  • Marie Hudson
    • 1
  • Ernest Lo
    • 2
  • Russell Steele
    • 1
  • Canadian Scleroderma Research Group (CSRG)
  • Murray Baron
    • 1
  1. 1.Jewish General Hospital and McGill UniversityMontrealCanada
  2. 2.Jewish General HospitalMontrealCanada

Personalised recommendations