J Rheum Dis.  2019 Jan;26(1):12-19. 10.4078/jrd.2019.26.1.12.

Smoking as a Preventable Risk Factor for Rheumatoid Arthritis: Rationale for Smoking Cessation Treatment in Patients with Rheumatoid Arthritis

• Roh S

• KMID: 2442030
• DOI: http://doi.org/10.4078/jrd.2019.26.1.12

Abstract

Rheumatoid arthritis (RA) is a chronic inflammatory disease of multifactorial etiology. Smoking is considered one of the most established environmental risk factors for RA development and severity. A large proportion of patients with RA have a high prevalence of smoking history. Previous studies have provided evidence suggesting that smoking is associated with the development of RA. Smoking has been associated with several pathogenic mechanisms on RA development such as oxidative stress, inflammation, and epigenetic changes. There is a need for public health campaigns to educate the public regarding these risks and preventive measures that reduce smoking are essential and may result in a decline in RA incidence. Encouragement of smoking cessation is especially warranted in relatives of patients with RA. Recently, RA-specific smoking cessation interventions have been developed. This review will summarize the knowledge accumulated to date concerning associations between smoking and RA.

Keyword

Smoking; Nicotine; Tobacco; Smoking cessation; Rheumatoid arthritis

MeSH Terms

Arthritis, Rheumatoid*
Epigenomics
Humans
Incidence
Inflammation
Nicotine
Oxidative Stress
Prevalence
Public Health
Risk Factors*
Smoke*
Smoking Cessation*
Smoking*
Tobacco
Nicotine
Smoke

Reference

1. Smolen JS, Aletaha D, McInnes IB. Rheumatoid arthritis. Lancet. 2016; 388:2023–2038.

2. Avouac J, Gossec L, Dougados M. Diagnostic and predictive value of anti-cyclic citrullinated protein antibodies in rheumatoid arthritis: a systematic literature review. Ann Rheum Dis. 2006; 65:845–851.

3. Huizinga TW, Amos CI, van der Helm-van Mil AH, Chen W, van Gaalen FA, Jawaheer D, et al. Refining the complex rheumatoid arthritis phenotype based on specificity of the HLA-DRB1 shared epitope for antibodies to citrullinated proteins. Arthritis Rheum. 2005; 52:3433–3438.

4. Padyukov L, Silva C, Stolt P, Alfredsson L, Klareskog L. A gene-environment interaction between smoking and shared epitope genes in HLA-DR provides a high risk of seropositive rheumatoid arthritis. Arthritis Rheum. 2004; 50:3085–3092.

5. Sparks JA, Karlson EW. The roles of cigarette smoking and the lung in the transitions between phases of preclinical rheumatoid arthritis. Curr Rheumatol Rep. 2016; 18:15.

6. Sparks JA, Chang SC, Deane KD, Gan RW, Kristen Demoruelle M, Feser ML, et al. Associations of smoking and age with inflammatory joint signs among unaffected first-degree relatives of rheumatoid arthritis patients: results from studies of the etiology of rheumatoid arthritis. Arthritis Rheumatol. 2016; 68:1828–1838.

7. Ruiz-Esquide V, Sanmartí R. Tobacco and other environmental risk factors in rheumatoid arthritis. Reumatol Clin. 2012; 8:342–350.

8. Costenbader KH, Feskanich D, Mandl LA, Karlson EW. Smoking intensity, duration, and cessation, and the risk of rheumatoid arthritis in women. Am J Med. 2006; 119:503.

9. Di Giuseppe D, Discacciati A, Orsini N, Wolk A. Cigarette smoking and risk of rheumatoid arthritis: a dose-response meta-analysis. Arthritis Res Ther. 2014; 16:R61.

10. Heliövaara M, Aho K, Aromaa A, Knekt P, Reunanen A. Smoking and risk of rheumatoid arthritis. J Rheumatol. 1993; 20:1830–1835.

11. Karlson EW, Lee IM, Cook NR, Manson JE, Buring JE, Hennekens CH. A retrospective cohort study of cigarette smoking and risk of rheumatoid arthritis in female health professionals. Arthritis Rheum. 1999; 42:910–917.

12. Krishnan E, Sokka T, Hannonen P. Smoking-gender interaction and risk for rheumatoid arthritis. Arthritis Res Ther. 2003; 5:R158–R162.

13. Sugiyama D, Nishimura K, Tamaki K, Tsuji G, Nakazawa T, Morinobu A, et al. Impact of smoking as a risk factor for developing rheumatoid arthritis: a meta-analysis of observational studies. Ann Rheum Dis. 2010; 69:70–81.

14. Uhlig T, Hagen KB, Kvien TK. Current tobacco smoking, formal education, and the risk of rheumatoid arthritis. J Rheumatol. 1999; 26:47–54.

15. Vessey MP, Villard-Mackintosh L, Yeates D. Oral contraceptives, cigarette smoking and other factors in relation to arthritis. Contraception. 1987; 35:457–464.

16. Klareskog L, Gregersen PK, Huizinga TW. Prevention of autoimmune rheumatic disease: state of the art and future perspectives. Ann Rheum Dis. 2010; 69:2062–2066.

17. Stolt P, Bengtsson C, Nordmark B, Lindblad S, Lundberg I, Klareskog L, et al. Quantification of the influence of cigarette smoking on rheumatoid arthritis: results from a population based case-control study, using incident cases. Ann Rheum Dis. 2003; 62:835–841.

18. Kochi Y, Thabet MM, Suzuki A, Okada Y, Daha NA, Toes RE, et al. PADI4 polymorphism predisposes male smokers to rheumatoid arthritis. Ann Rheum Dis. 2011; 70:512–515.

19. Klareskog L, Stolt P, Lundberg K, Källberg H, Bengtsson C, Grunewald J, et al. A new model for an etiology of rheumatoid arthritis: smoking may trigger HLA-DR (shared epitope)-restricted immune reactions to autoantigens modified by citrullination. Arthritis Rheum. 2006; 54:38–46.

20. Källberg H, Ding B, Padyukov L, Bengtsson C, Rönnelid J, Klareskog L, et al. Smoking is a major preventable risk factor for rheumatoid arthritis: estimations of risks after various exposures to cigarette smoke. Ann Rheum Dis. 2011; 70:508–511.

21. Bang SY, Lee KH, Cho SK, Lee HS, Lee KW, Bae SC. Smoking increases rheumatoid arthritis susceptibility in individuals carrying the HLA-DRB1 shared epitope, regardless of rheumatoid factor or anti-cyclic citrullinated peptide antibody status. Arthritis Rheum. 2010; 62:369–377.

22. Fisher BA, Bang SY, Chowdhury M, Lee HS, Kim JH, Charles P, et al. Smoking, the HLA-DRB1 shared epitope and ACPA fine-specificity in Koreans with rheumatoid arthritis: evidence for more than one pathogenic pathway linking smoking to disease. Ann Rheum Dis. 2014; 73:741–747.

23. Arnson Y, Shoenfeld Y, Amital H. Effects of tobacco smoke on immunity, inflammation and autoimmunity. J Autoimmun. 2010; 34:J258–J265.

24. Johannsen A, Susin C, Gustafsson A. Smoking and inflammation: evidence for a synergistic role in chronic disease. Periodontol 2000. 2014; 64:111–126.

25. Hedström AK, Stawiarz L, Klareskog L, Alfredsson L. Smoking and susceptibility to rheumatoid arthritis in a Swedish population-based case-control study. Eur J Epidemiol. 2018; 33:415–423.

26. Zeng P, Chen Z, Klareskog L, Alfredsson L, Bengtsson C, Jiang X. Amount of smoking, duration of smoking cessation and their interaction with silica exposure in the risk of rheumatoid arthritis among males: results from the Swedish Epidemiological Investigation of Rheumatoid Arthritis (EIRA) study. Ann Rheum Dis. 2018; 77:1238–1241.

27. Malm K, Bremander A, Arvidsson B, Andersson ML, Bergman S, Larsson I. The influence of lifestyle habits on quality of life in patients with established rheumatoid arthritis-a constant balancing between ideality and reality. Int J Qual Stud Health Well-being. 2016; 11:30534.

28. Hensvold AH, Magnusson PK, Joshua V, Hansson M, Israelsson L, Ferreira R, et al. Environmental and genetic factors in the development of anticitrullinated protein antibodies (ACPAs) and ACPA-positive rheumatoid arthritis: an epidemiological investigation in twins. Ann Rheum Dis. 2015; 74:375–380.

29. Svendsen AJ, Junker P, Houen G, Kyvik KO, Nielsen C, Skytthe A, et al. Incidence of chronic persistent rheumatoid arthritis and the impact of smoking: a historical twin cohort study. Arthritis Care Res (Hoboken). 2017; 69:616–624.

30. Onozaki K. Etiological and biological aspects of cigarette smoking in rheumatoid arthritis. Inflamm Allergy Drug Targets. 2009; 8:364–368.

31. Chang K, Yang SM, Kim SH, Han KH, Park SJ, Shin JI. Smoking and rheumatoid arthritis. Int J Mol Sci. 2014; 15:22279–22295.

32. Kalpakcioglu B, Senel K. The interrelation of glutathione reductase, catalase, glutathione peroxidase, superoxide dismutase, and glucose-6-phosphate in the pathogenesis of rheumatoid arthritis. Clin Rheumatol. 2008; 27:141–145.

33. Pryor WA, Stone K. Oxidants in cigarette smoke. Radicals, hydrogen peroxide, peroxynitrate, and peroxynitrite. Ann N Y Acad Sci. 1993; 686:12–27.

34. Sopori M. Effects of cigarette smoke on the immune system. Nat Rev Immunol. 2002; 2:372–377.

35. Harel-Meir M, Sherer Y, Shoenfeld Y. Tobacco smoking and autoimmune rheumatic diseases. Nat Clin Pract Rheumatol. 2007; 3:707–715.

36. Benedetti G, Miossec P. Interleukin 17 contributes to the chronicity of inflammatory diseases such as rheumatoid arthritis. Eur J Immunol. 2014; 44:339–347.

37. Viatte S, Plant D, Raychaudhuri S. Genetics and epigenetics of rheumatoid arthritis. Nat Rev Rheumatol. 2013; 9:141–153.

38. Zeilinger S, Kühnel B, Klopp N, Baurecht H, Kleinschmidt A, Gieger C, et al. Tobacco smoking leads to extensive genome-wide changes in DNA methylation. PLoS One. 2013; 8:e63812.

39. Saevarsdottir S, Rezaei H, Geborek P, Petersson I, Ernestam S, Albertsson K, et al. Current smoking status is a strong predictor of radiographic progression in early rheumatoid arthritis: results from the SWEFOT trial. Ann Rheum Dis. 2015; 74:1509–1514.

40. Anderson R, Meyer PW, Ally MM, Tikly M. Smoking and air pollution as pro-inflammatory triggers for the development of rheumatoid arthritis. Nicotine Tob Res. 2016; 18:1556–1565.

41. Lee YH, Bae SC, Song GG. Gene-environmental interaction between smoking and shared epitope on the development of anti-cyclic citrullinated peptide antibodies in rheumatoid arthritis: a meta-analysis. Int J Rheum Dis. 2014; 17:528–535.

42. Wagner CA, Sokolove J, Lahey LJ, Bengtsson C, Saevarsdottir S, Alfredsson L, et al. Identification of anticitrullinated protein antibody reactivities in a subset of anti-CCP-negative rheumatoid arthritis: association with cigarette smoking and HLA-DRB1 ‘shared epitope’ alleles. Ann Rheum Dis. 2015; 74:579–586.

43. Taylor LH, Twigg S, Worthington J, Emery P, Morgan AW, Wilson AG, et al. Metaanalysis of the association of smoking and PTPN22 R620W genotype on autoantibody status and radiological erosions in rheumatoid arthritis. J Rheumatol. 2013; 40:1048–1053.

44. Wu S, Luo H, Xiao X, Zhang H, Li T, Zuo X. Attenuation of collagen induced arthritis via suppression on Th17 response by activating cholinergic anti-inflammatory pathway with nicotine. Eur J Pharmacol. 2014; 735:97–104.

45. Zhou Y, Zuo X, Li Y, Wang Y, Zhao H, Xiao X. Nicotine inhibits tumor necrosis factor-α induced IL-6 and IL-8 secretion in fibroblast-like synoviocytes from patients with rheumatoid arthritis. Rheumatol Int. 2012; 32:97–104.

46. Vesperini V, Lukas C, Fautrel B, Le Loet X, Rincheval N, Combe B. Association of tobacco exposure and reduction of radiographic progression in early rheumatoid arthritis: results from a French multicenter cohort. Arthritis Care Res (Hoboken). 2013; 65:1899–1906.

47. Jiang X, Alfredsson L, Klareskog L, Bengtsson C. Smokeless tobacco (moist snuff) use and the risk of developing rheumatoid arthritis: results from a case-control study. Arthritis Care Res (Hoboken). 2014; 66:1582–1586.

48. Lee J, Luria A, Rhodes C, Raghu H, Lingampalli N, Sharpe O, et al. Nicotine drives neutrophil extracellular traps formation and accelerates collagen-induced arthritis. Rheumatology (Oxford). 2017; 56:644–653.

49. de Rooy DP, van Nies JA, Kapetanovic MC, Kristjansdottir H, Andersson ML, Forslind K, et al. Smoking as a risk factor for the radiological severity of rheumatoid arthritis: a study on six cohorts. Ann Rheum Dis. 2014; 73:1384–1387.

50. Söderlin MK, Andersson M, Bergman S. BARFOT study group. Second-hand exposure to tobacco smoke and its effect on disease activity in Swedish rheumatoid arthritis patients. Data from BARFOT, a multicenter study of RA. Clin Exp Rheumatol. 2013; 31:122–124.

51. Carlens C, Hergens MP, Grunewald J, Ekbom A, Eklund A, Höglund CO, et al. Smoking, use of moist snuff, and risk of chronic inflammatory diseases. Am J Respir Crit Care Med. 2010; 181:1217–1222.

52. Maska LB, Sayles HR, O'Dell JR, Curtis JR, Bridges SL Jr, Moreland LW, et al. Serum cotinine as a biomarker of tobacco exposure and the association with treatment response in early rheumatoid arthritis. Arthritis Care Res (Hoboken). 2012; 64:1804–1810.

53. Andersson ML, Bergman S, Söderlin MK. The effect of stopping smoking on disease activity in rheumatoid arthritis (RA). Data from BARFOT, a multicenter study of early RA. Open Rheumatol J. 2012; 6:303–309.

54. Fisher MC, Hochberg MC, El-Taha M, Kremer JM, Peng C, Greenberg JD. CORRONA Investigators. Smoking, smoking cessation, and disease activity in a large cohort of patients with rheumatoid arthritis. J Rheumatol. 2012; 39:904–909.

55. Di Giuseppe D, Orsini N, Alfredsson L, Askling J, Wolk A. Cigarette smoking and smoking cessation in relation to risk of rheumatoid arthritis in women. Arthritis Res Ther. 2013; 15:R56.

56. Walsh CA, Conaghan PG. Smoking: a preventable cause of rheumatoid arthritis. Practitioner. 2011; 255:5.

57. Cuppen BV, Jacobs JW, Ter Borg EJ, Marijnissen AC, Bijlsma JW, Lafeber FP, et al. Necessity of TNF-alpha inhibitor discontinuation in rheumatoid arthritis is predicted by smoking and number of previously used biological DMARDs. Clin Exp Rheumatol. 2017; 35:221–228.

58. Baka Z, Buzás E, Nagy G. Rheumatoid arthritis and smoking: putting the pieces together. Arthritis Res Ther. 2009; 11:238.

59. Naranjo A, Khan NA, Cutolo M, Lee SS, Lazovskis J, Laas K, et al. Smoking cessation advice by rheumatologists: results of an international survey. Rheumatology (Oxford). 2014; 53:1825–1829.

60. Naranjo A, Bilbao A, Erausquin C, Ojeda S, Francisco FM, Rúa-Figueroa I, et al. Results of a specific smoking cessation program for patients with arthritis in a rheumatology clinic. Rheumatol Int. 2014; 34:93–99.

61. Aimer P, Stamp LK, Stebbings S, Cameron V, Kirby S, Croft S, et al. Developing a tailored smoking cessation intervention for rheumatoid arthritis patients. Musculoskeletal Care. 2016; 14:2–14.

62. Aimer P, Treharne GJ, Stebbings S, Frampton C, Cameron V, Kirby S, et al. Efficacy of a rheumatoid arthritis-specific smoking cessation program: a randomized controlled pilot trial. Arthritis Care Res (Hoboken). 2017; 69:28–37.

63. Aimer P, Stamp LK, Stebbings S, Cameron V, Kirby S, Treharne GJ. Exploring perceptions of a rheumatoid arthritis-specific smoking cessation programme. Musculoskeletal Care. 2018; 16:74–81.

64. Aimer P, Stamp L, Stebbings S, Valentino N, Cameron V, Treharne GJ. Identifying barriers to smoking cessation in rheumatoid arthritis. Arthritis Care Res (Hoboken). 2015; 67:607–615.

65. Gath ME, Stamp LK, Aimer P, Stebbings S, Treharne GJ. Reconceptualizing motivation for smoking cessation among people with rheumatoid arthritis as incentives and facilitators. Musculoskeletal Care. 2018; 16:139–146.

66. Roelsgaard IK, Thomsen T, Østergaard M, Christensen R, Hetland ML, Jacobsen S, et al. The effect of an intensive smoking cessation intervention on disease activity in patients with rheumatoid arthritis: study protocol for a randomised controlled trial. Trials. 2017; 18:570.

67. Heatherton TF, Kozlowski LT, Frecker RC, Fagerström KO. The Fagerström test for nicotine dependence: a revision of the Fagerström Tolerance Questionnaire. Br J Addict. 1991; 86:1119–1127.