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

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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.

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References

  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, Philadelphia

    Google Scholar 

  2. LeRoy EC, Black C, Fleischmajer R et al (1988) Scleroderma (systemic sclerosis): classification, subsets and pathogenesis. J Rheumatol 15:202–205

    PubMed  CAS  Google Scholar 

  3. Hudson M, Lo E, Lu Y, Hercz D, Baron M, Steele R (2010) Cigarette smoking in patients with systemic sclerosis. Arthritis Rheum 63:230–238

    Article  Google Scholar 

  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 22:1281–1285

    PubMed  CAS  Google Scholar 

  5. Leffondre K, Abrahamowicz M, Xiao Y, Siemiatycki J (2006) Modelling smoking history using a comprehensive smoking index: application to lung cancer. Stat Med 25:4132–4146

    Article  PubMed  Google Scholar 

  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):570–578

    Google Scholar 

  7. McCullagh P, Nelder J (1989) Generalized linear models, 2nd edn. Chapman and Hall/CRC, Boca Raton

    Google Scholar 

  8. R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  9. Smith JB, Fenske NA (1996) Cutaneous manifestations and consequences of smoking [see comments]. J Am Acad Dermatol 34:717–732; quiz 33–34

    Google Scholar 

  10. Sonnenfeld G, Hudgens RW (1983) Effect of carcinogenic components of cigarette smoke on in vivo production of murine interferon. Cancer Res 43:4720–4722

    PubMed  CAS  Google Scholar 

  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:1199–1207

    Article  PubMed  CAS  Google Scholar 

  12. Penn A, Chen LC, Snyder CA (1994) Inhalation of steady-state sidestream smoke from one cigarette promotes arteriosclerotic plaque development. Circulation 90:1363–1367

    Article  PubMed  CAS  Google Scholar 

  13. Stefanadis C, Tsiamis E, Vlachopoulos C et al (1997) Unfavorable effect of smoking on the elastic properties of the human aorta. Circulation 95:31–38

    Article  PubMed  CAS  Google Scholar 

  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 36:550–556

    Article  PubMed  CAS  Google Scholar 

  15. Solly S (1856) Clinical lectures on paralysis. Lancet 68(1737):641–643

    Google Scholar 

  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 137:1043–1051

    PubMed  CAS  Google Scholar 

  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 85:78–82

    Article  PubMed  CAS  Google Scholar 

  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 114:840–844

    PubMed  CAS  Google Scholar 

  19. Raduan AP, Luiz RR, Manela-Azulay M (2008) Association between smoking and cutaneous ageing in a Brazilian population. J Eur Acad Dermatol Venereol 22:1312–1318

    Article  PubMed  CAS  Google Scholar 

  20. Freiman A, Bird G, Metelitsa AI, Barankin B, Lauzon GJ (2004) Cutaneous effects of smoking. J Cutan Med Surg 8:415–423

    Article  PubMed  Google Scholar 

  21. Misery L (2004) Nicotine effects on skin: are they positive or negative? Exp Dermatol 13:665–670

    Article  PubMed  CAS  Google Scholar 

  22. Metelitsa AI, Lauzon GJ (2010) Tobacco and the skin. Clin Dermatol 28:384–390

    Article  PubMed  Google Scholar 

  23. Morita A (2007) Tobacco smoke causes premature skin aging. J Dermatol Sci 48:169–175

    Article  PubMed  CAS  Google Scholar 

  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 83:207–225

    PubMed  CAS  Google Scholar 

  25. Jorgensen LN, Kallehave F, Christensen E, Siana JE, Gottrup F (1998) Less collagen production in smokers. Surgery 123:450–455

    Article  PubMed  CAS  Google Scholar 

  26. Yin L, Morita A, Tsuji T (2000) Alterations of extracellular matrix induced by tobacco smoke extract. Arch Dermatol Res 292:188–194

    Article  PubMed  CAS  Google Scholar 

  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):51–56

    Article  PubMed  Google Scholar 

  28. Thomsen SF, Sorensen LT (2010) Smoking and skin disease. Skin Therapy Lett 15:4–7

    PubMed  CAS  Google Scholar 

  29. Gabrielli A, Avvedimento EV, Krieg T (2009) Scleroderma. N Engl J Med 360:1989–2003

    Article  PubMed  CAS  Google Scholar 

  30. Mills CM (1998) Cigarette smoking, cutaneous immunity, and inflammatory response. Clin Dermatol 16:589–594

    Article  PubMed  CAS  Google Scholar 

  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 11:563–568

    PubMed  CAS  Google Scholar 

  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 23:189–204

    Article  PubMed  CAS  Google Scholar 

  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 140:397–402

    Article  PubMed  CAS  Google Scholar 

  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 111:523–529

    Article  PubMed  CAS  Google Scholar 

  35. Moszczynski P, Zabinski Z, Moszczynski P Jr, Rutowski J, Slowinski S, Tabarowski Z (2001) Immunological findings in cigarette smokers. Toxicol Lett 118:121–127

    Article  PubMed  CAS  Google Scholar 

  36. Kanekura T, Usuki K, Kanzaki T (2004) Skin disorders with prominent eosinophilic infiltration treated successfully with nicotine. Report of two cases. Dermatology 208:153–157

    Article  PubMed  CAS  Google Scholar 

  37. Kanekura T, Usuki K, Kanzaki T (1995) Nicotine for pyoderma gangrenosum. Lancet 345:1058

    Article  PubMed  CAS  Google Scholar 

  38. Kanekura T, Kanzaki T (1999) Successful treatment of orogenital ulceration with transdermal nicotine patches. Br J Dermatol 141:1140–1141

    Article  PubMed  CAS  Google Scholar 

  39. Calkins BM (1989) A meta-analysis of the role of smoking in inflammatory bowel disease. Dig Dis Sci 34:1841–1854

    Article  PubMed  CAS  Google Scholar 

  40. Cooke JP (2007) Angiogenesis and the role of the endothelial nicotinic acetylcholine receptor. Life Sci 80:2347–2351

    Article  PubMed  CAS  Google Scholar 

  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 97:1370–1378

    Article  PubMed  CAS  Google Scholar 

  42. Heeschen C, Chang E, Aicher A, Cooke JP (2006) Endothelial progenitor cells participate in nicotine-mediated angiogenesis. J Am Coll Cardiol 48:2553–2560

    Article  PubMed  CAS  Google Scholar 

  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 44:881–889

    Article  PubMed  CAS  Google Scholar 

  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 335:1792–1798

    Article  PubMed  CAS  Google Scholar 

  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 30:125–130

    Article  PubMed  CAS  Google Scholar 

  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 18:497–505

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was funded in part by the Canadian Institutes of Health Research, the Scleroderma Society of Canada and educational grants from Actelion Pharmaceuticals and Pfizer Inc. Dr. Hudson is supported by New Investigator awards from the Canadian Institutes of Health Research and the Fonds de la Recherche en Santé du Québec. The funding sources had no role in the design of the study, analysis of the data, preparation of the manuscript and decision to submit for publication.

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Authors and Affiliations

  1. Jewish General Hospital and McGill University, Room A-725, 3755 Cote Ste Catherine Road, Montreal, QC, H3T 1E2, Canada

    Geneviève Gyger, Marie Hudson, Russell Steele & Murray Baron

  2. Jewish General Hospital, Room A-725, 3755 Cote Ste Catherine Road, Montreal, QC, H3T 1E2, Canada

    Ernest Lo

Authors
  1. Geneviève Gyger
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  2. Marie Hudson
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  3. Ernest Lo
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  4. Russell Steele
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  5. Murray Baron
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Canadian Scleroderma Research Group (CSRG)

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Correspondence to Marie Hudson.

Additional information

The Investigators of the Canadian Scleroderma Research Group is given in “Appendix.”

Appendix: Investigators of the Canadian Scleroderma Research Group

Appendix: Investigators of the Canadian Scleroderma Research Group

M. Baron, Montreal, Quebec; J. Pope, London, Ontario; J. Markland, Saskatoon, Saskatchewan; D. Robinson, Winnipeg, Manitoba; N. Jones, Edmonton, Alberta; N. Khalidi, Hamilton, Ontario; P. Docherty, Moncton, New Brunswick; E. Kaminska, Hamilton, Ontario; A. Masetto, Sherbrooke, Quebec; D. Smith, Ottawa, Ontario; E. Sutton, Halifax, Nova Scotia; J-P. Mathieu, Montreal, Quebec; M. Hudson, Montreal, Quebec; S. Ligier, Montreal, Quebec; T. Grodzicky, Montreal, Quebec; S. Mittoo, Winnipeg, Manitoba; M. Fritzler, Advanced Diagnostics Laboratory, Calgary, Alberta.

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Gyger, G., Hudson, M., Lo, E. et al. Does cigarette smoking mitigate the severity of skin disease in systemic sclerosis?. Rheumatol Int 33, 943–948 (2013). https://doi.org/10.1007/s00296-012-2481-6

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  • DOI: https://doi.org/10.1007/s00296-012-2481-6

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