Insights into the paradoxical effect of smoking on vasculitis: a comprehensive review
Main Article Content
Keywords
Autoimmune/autoinflammatory rheumatic diseases (AIRDs), Vasculitis, Behcet’s disease, Environmental factors, Smoking, Tobacco, Cigarette smoke
Abstract
Vasculitis is a group of uncommon diseases characterized by inflammation of blood vessels, which contributes to the organ ischemia and damage. Cigarette smoke contains a high concentration of various toxins, which have the potential to affect the immune response and development of autoimmune/autoinflammatory rheumatic diseases including vasculitis. Smoking influences both innate and adaptive immune systems and plays binary functions in modulating immunity by either aggravating pathogenic immune responses or attenuating defensive immunity. Smoking contributes to the pathogenesis of autoimmune diseases by various mechanisms including induction of tissue damage and apoptosis, changes in innate immune function and production of proinflammatory cytokines, changes in humoral immunity and T cell responses and anti-estrogen effects. In this review, we considered the available evidence on the association between smoking with the risk, clinical manifestations, response to treatment and outcomes of vasculitis, and the effect of smoking cessation on these parameters. In conclusion, despite inconclusive evidence of an increased risk of giant cell arthritis and anti-neutrophil cytoplasmic autoantibody associated vasculitis (AAV) in smokers, there is strong evidence that smokers have a lower risk of Behcet’s disease (BD). Furthermore, smoking changes the clinical picture and outcomes of BD and AAV.
References
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2. Ralli M, Campo F, Angeletti D, Minni A, Artico M, Greco A, Polimeni A, de Vincentiis M. Pathophysiology and therapy of systemic vasculitides. EXCLI J. 2020;19:817-854.
3. Floreani A, Leung PS, Gershwin ME. Environmental Basis of Autoimmunity. Clin Rev Allergy Immunol. 2016;50(3):287-300.
4. Costenbader KH, Karlson EW. Cigarette smoking and autoimmune disease: what can we learn from epidemiology? Lupus. 2006;15(11):737-745.
5. Klareskog L, Padyukov L, Alfredsson L. Smoking as a trigger for inflammatory rheumatic diseases. Curr Opin Rheumatol. 2007;19(1):49-54.
6. Turesson C, Schaid DJ, Weyand CM, et al. Association of HLA–C3 and smoking with vasculitis in patients with rheumatoid arthritis. Arthritis Rheum. 2006;54(9):2776-2783.
7. Armstrong AW, Armstrong EJ, Fuller EN, Sockolov ME, Voyles SV. Smoking and pathogenesis of psoriasis: a review of oxidative, inflammatory and genetic mechanisms. Br J Dermatol. 2011;165(6):1162-8.
8. Arnson Y, Shoenfeld Y, Amital H. Effects of tobacco smoke on immunity, inflammation and autoimmunity. J Autoimmun. 2010;34(3):J258-65.
9. Tollerud DJ, Clark JW, Brown LM, Neuland CY, Mann DL, Pankiw-Trost LK, et al. The effects of cigarette smoking on T cell subsets. A population-based survey of healthy Caucasians. Am Rev Respir Dis. 1989;139 (6):1446-51.
10. Robbins CS, Franco F, Mouded M, Cernadas M, Shapiro SD. Cigarette smoke exposure impairs dendritic cell maturation and T cell proliferation in thoracic lymph nodes of mice. J Immunol. 2008;180(10):6623-8.
11. Harrison OJ, Foley J, Bolognese BJ, Long E 3rd, Podolin PL, Walsh PT. Airway infiltration of CD4+ CCR6+ Th17 type cells associated with chronic cigarette smoke induced airspace enlargement. Immunol Lett. 2008 ;121(1):13-21.
12. Shaler CR, Horvath CN, McCormick S, Jeyanathan M, Khera A, Zganiacz A, Kasinska J, Stampfli MR, Xing Z. Continuous and discontinuous cigarette smoke exposure differentially affects protective Th1 immunity against pulmonary tuberculosis. PLoS ONE. 2013 ;8(3):e59185.
13. Kim H, Cho S-K, Kim JW, et al. An increased disease burden of autoimmune inflammatory rheumatic diseases in Korea. Semin Arthritis Rheum. 2020;50(3):526-533.
14. Malek Mahdavi A, Khabbazi A, Yaaghoobian B, et al. Cigarette smoking and risk of Behcet’s disease: a propensity score matching analysis. Mod Rheumatol. 2019;29(4):633-639.
15. Lee YB, Lee JH, Lee SY, Lee JH, Yu DS, Han KD, et al. Association between smoking and Behçet's disease: a nationwide population‐based study in Korea. J Eur Acad Dermatol Venereol. 2019; 33 (11): 2114-2122.
16. Khabbazi A, Alinejati B, Hajialilo M, Ghojazadeh M, Malek Mahdavi A. Cigarette smoking and risk of primary systemic vasculitis: a propensity score matching analysis. Sarcoidosis Vasc Diffuse Lung Dis. 2019;36(3):243-250
17. Lane SE, Watts RA, Bentham G, Innes NJ, Scott DGJA, Rheumatism. Are environmental factors important in primary systemic vasculitis? A case–control study. Arthritis Rheum. 2003;48(3):814-823.
18. Harel-Meir M, Sherer Y, Shoenfeld Y. Tobacco smoking and autoimmune rheumatic diseases. Nature clinical practice Rheumatology. 2007;3(12):707-715.
19. Lee SS, Choi CB, Lee EK, Park SH, Choe JY, Kim SK. The association between smoking and clinical manifestations in patients with Behcet’s disease. KJM. 2008;75(2):202-209.
20. Tuna S, Alan S, Turkoglu E. Effects of smoking and HLA-B51 on clinical manifestations in Behcet's disease: retrospective analysis of 209 patients in a Turkish population. Archives of Rheumatology. 2015;30(4)
21. Rizvi S, McGrath Jr H. The therapeutic effect of cigarette smoking on oral/genital aphthosis and other manifestations of Behçet's disease. Clin Exp Rheumatol. 2001;19(5 Suppl 24):S77-8.
22. Beaudreuil S, Lasfargues G, Lauériere L, El Ghoul Z, Fourquet F, Longuet C, et al. Occupational exposure in ANCA-positive patients: a case-control study. Kidney Int. 2005;67(5):1961-6.
23. Haubitz M, Woywodt A, De Groot K, Haller H, Goebel U. Smoking habits in patients diagnosed with ANCA associated small vessel vasculitis. Ann Rheum Dis. 2005;64(10):1500-1502.
24. McDermott G, Fu X, Stone JH, Wallwork R, Zhang Y, Choi HK, Wallace ZS. Association of Cigarette Smoking With Antineutrophil Cytoplasmic Antibody-Associated Vasculitis. JAMA Intern Med. 2020;180(6):870-876.
25. Tomasson G, Bjornsson J, Zhang Y, Gudnason V, Merkel PA. Cardiovascular risk factors and incident giant cell arteritis: a population-based cohort study. Scand J Rheumatol. 48(3):213-217.
26. Brennan DN, Ungprasert P,Warrington KJ, Koster MJ. Smoking as a risk factor for giant cell arteritis: A systematic review and meta-analysis. Semin Arthritis Rheum. 2018;48(3):529-537.
27. Yates M, Luben R, Hayat S, Mackie SL, Watts RA, Khaw KT, et al. Cardiovascular risk factors associated with polymyalgia rheumatica and giant cell arteritis in a prospective cohort: EPIC-Norfolk Study. Rheumatology (Oxford). 2020;59(2):319-323.
28. Benarous L, Terrier B, Puéchal X, Dunogué B, Cohen P, Le Jeunne C, et al. Tobacco differentially affects the clinical-biological phenotypes of ANCA-associated vasculitides. Clin Exp Rheumatol. 2015;33(2 Suppl 89):S-116-21.
29. Lee YB, Lee JH, Lee SY, Lee JH, Yu DS, Han KD, Park YG. Association between smoking and Behçet's disease: a nationwide population-based study in Korea. J Eur Acad Dermatol Venereol. 2019;33(11):2114-2122.
30. Andreiana I, Stancu S, Avram A, Taran L, Mircescu G. Pneumo-Renal Syndrome in Anti-Neutrophil Cytoplasm Antibody (ANCA)-Associated Small-Vessel Vasculitis. Maedica (Bucur). 2015;10(2):101-106.
31. Patel A, Masiak A, Joshi S, Ziętkiewicz M, Zdrojewski Z. Influence of smoking on disease activity and prognosis of ANCA-associated vasculitis: a retrospective cohort study. Pol Arch Intern Med. 2023;16478.
32. Cox CW, Bartholmai BJ, Baqir M, Geske JR, Specks U. Pulmonary Low Attenuation Areas on CT in ANCA-associated Vasculitis: A quantitative and semi-quantitative analysis correlated with pulmonary function testing for obstructive airway disease. Sarcoidosis Vasc Diffuse Lung Dis. 2020;37(4):e2020016.
33. Ren J, Ding Y, Zhao J, Sun Y. Bronchiectasis in patients with antineutrophil cytoplasmic antibody-associated vasculitis: a case control study on clinical features and prognosis. Expert Rev Respir Med. 2022;16(6):697-705.
34. Kaklamani VG, Tzonou A, Markomichelakis N, Papazoglou S, Kaklamanis PG. The effect of smoking on the clinical features of Adamantiades-Behcet’s disease. Adv Exp Med Biol. 2003;528:323-7.
35. Aramaki K, Kikuchi H, Hirohata S. HLA-B51 and cigarette smoking as risk factors for chronic progressive neurological manifestations in Behçet's disease. Mod Rheumatol. 2007;17(1):81-2.
36. Lee SS, Choi CB, Lee EK, Park SH, Choe JY, Kim SK. The association between smoking and clinical manifestations in patients with Behçet’s disease. Korean J of Med. 2008;75(2):202-209.
37. Bilgin AB, Turkoglu EB, Ilhan HD, Unal M, Apaydin KC. Is Smoking a Risk Factor in Ocular Behçet Disease? Ocul Immunol Inflamm. 2015;23(4):283-286.
38. Torgutalp M, Eroğlu DS, Sezer S, Yayla ME, Karataş G, Özel EM, et al. Patient characteristics in Behçet's Syndrome and their associations with major organ involvement: a single-centre experience of 2118 cases. Scand J Rheumatol. 2022;51(1):50-58.
39. Blank U, Ruckes C, Clauss W, Weber WM. Effects of nicotine on human nasal epithelium: evidence for nicotinic receptors in nonexcitable cells. Pflugers Arch. 1997;434(5):581–6.
40. Kalayciyan A, Orawa H, Fimmel S, Perschel FH, González JB, Fitzner RG, et al. Nicotine and biochanin A, but not cigarette smoke, induce anti-inflammatory effects on keratinocytes and endothelial cells in patients with Behçet's disease. J Invest Dermatol. 2007;127(1):81-9.
41. Özer H, Güneşaçar R, Dinkçi S, Özbalkan Z, Yildiz F, Erken E. The impact of smoking on clinical features of Behcet's disease patients with glutathione S-transferase polymorphisms. Clin Exp Rheumatol. 2012;30(3 Suppl 72):S14-7.
42. Caravaca-Fontán F, Yerovi E, Delgado-Yagu E M, Galeano C, Pampa-Saico S, Tenorio MT, Liaño F. Anti-neutrophil cytoplasmic antibody-associated vasculitis with renal involvement: Analysis of 89 cases. Med Clin (Barc). 2017;148(1):1-7.
43. Mohammad AJ, Segelmark M. Association of cigarette smoking with organ damage in primary systemic vasculitis. Scand J Rheumatol. 2011;40(1):51-6.
44. Hozumi H, Kono M, Hasegawa H, Yasui H, Suzuki Y, Karayama M, et al. Clinical significance of interstitial lung disease and its acute exacerbation in microscopic polyangiitis. Chest. 2021;159(6):2334-2345
45. Lega JC, Seror R, Fassier T, Aumaître O, Quere I, Pourrat J, et al. Characteristics, prognosis, and outcomes of cutaneous ischemia and gangrene in systemic necrotizing vasculitides: a retrospective multicenter study. Semin Arthritis Rheum. 2014;43(5):681-8.
46. Yang L, Xie H, Liu Z, Chen Y, Wang J, Zhang H, et al. Risk factors for infectious complications of ANCA-associated vasculitis: a cohort study. BMC Nephrol. 2018;19(1):1-7.
47. Holguin F, Ramadan B, Gal AA, Roman J. Prognostic factors for hospital mortality and ICU admission in patients with ANCA-related pulmonary vasculitis. Am J Med Sci. 2008;336(4):321-6.
48. Yang S, Chai D, Li Y, Wang Y, Zhan X, Zhang L, et al. Patterns of lung diseases predict survival in patients with MPO-ANCA-associated vasculitis: a single-center retrospective study. Clin Rheumatol. 2022;41(3):783-793.
49. Jebali H, Khadhar M, Mami I, Beji S, Sellami M, Hassenet M, et al. Predictors of renal outcomes in anti-neutrophil cytoplasmic antibody glomerulonephritis. Saudi J Kidney Dis Transpl. 2020;31(1):182-190.
50. Watanabe-Imai K, Harigai M, Sada KE, Yamamura M, Fujii T, Dobashi H, et al. Clinical characteristics of and risk factors for serious infection in Japanese patients within six months of remission induction therapy for antineutrophil cytoplasmic antibody-associated vasculitis registered in a nationwide, prospective, inception cohort study. Mod Rheumatol. 2017;27(4):646-651.
51. Lao M, Huang M, Li C, Li H, Qiu Q, Zhan Z, Chen D. Infectious profile in patients with ANCA-associated vasculitis: a single-center retrospective study from Southern China. Clin Rheumatol. 2020;39(2):499-507.
52. Yamaguchi M, Ando M, Katsuno T, Tsuboi N, Maruyama S. Smoking Is a Risk Factor for Relapse of Antimyeloperoxidase Antibodies-Associated Vasculitis. J Clin Rheumatol. 2018;24(7):361-367.
53. Sattui SE, Conway R, Putman MS, Seet AM, Gianfrancesco MA, Beins K, et al. Outcomes of COVID-19 in patients with primary systemic vasculitis or polymyalgia rheumatica from the COVID-19 Global Rheumatology Alliance physician registry: a retrospective cohort study. Lancet Rheumatol. 2021;3(12):e855-e864.
54. Malek Mahdavi A, Khabbazi A, Hajialilo M. Long-term outcome and predictors of remission in Behçet’s disease in daily practice. Mod Rheumatol. 2021;31(6):1148-1157.
55. Mumcu G, Yay M, Aksoy A, et al. Predictive factors for work-day loss in Behçet's syndrome: A multi-center study. Int J Rheum Dis. 2020;23(2):240-246.
56. El-Shebiny E, El-Fakharany A, Zahran E, Shoeib S, Salem M, Elnaggar M, Morad N. Modifiable cardiovascular risk factors in patients with Behçet’s disease: a multicenter experience. Egypt J Intern Med. 2019;31(4):726-732.
57. Soy M, Erken E, Konca K, Ozbek S. Smoking and Behçet's disease. Clin Rheumatol. 2000;19(6):508-9.
58. Harel-Meir M, Sherer Y, Shoenfeld Y. Tobacco smoking and autoimmune rheumatic diseases. Nature clinical practice Rheumatology. 2007;3(12):707-715.
59. Cosnes J. Tobacco and IBD: relevance in the understanding of disease mechanisms and clinical practice. Best Pract Res Clin Gastroenterol. 2004;18(3):481-96
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Dec 10, 2024
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Khabbazi A, Rahimi M, Malek Mahdavi A, Farzaneh R, Daneshvar S, Naseri A, et al. Insights into the paradoxical effect of smoking on vasculitis: a comprehensive review. Sarcoidosis Vasc Diffuse Lung Dis [Internet]. 2024 Dec. 10 [cited 2025 Jan. 22];41(4):e2024053. Available from: https://mattioli1885journals.com/index.php/sarcoidosis/article/view/15557
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
How to Cite
1.
Khabbazi A, Rahimi M, Malek Mahdavi A, Farzaneh R, Daneshvar S, Naseri A, et al. Insights into the paradoxical effect of smoking on vasculitis: a comprehensive review. Sarcoidosis Vasc Diffuse Lung Dis [Internet]. 2024 Dec. 10 [cited 2025 Jan. 22];41(4):e2024053. Available from: https://mattioli1885journals.com/index.php/sarcoidosis/article/view/15557
