Skip to main content
Log in

Smoking and the risk of systemic lupus erythematosus: an updated systematic review and cumulative meta-analysis

  • Original Article
  • Published:
Clinical Rheumatology Aims and scope Submit manuscript

Abstract

Published articles reported controversial results about the association of smoking with the risk of systemic lupus erythematosus (SLE). A meta-analysis was performed to assess the aforementioned association and arrive at a more precise estimate of effect. A comprehensive search was performed to identify case–control or cohort studies (from 1990 to 2015) of the aforementioned association. The I 2 statistic was used to examine between-study heterogeneity. Fixed or random effect model was selected based on heterogeneity test among studies. Publication bias was estimated using Egger’s regression asymmetry test. A total of 12 published articles with 13 studies were finally included in our meta-analysis. Results showed that the pooled odds ratio (OR) for SLE risk was 1.56 (95 % confidence interval (CI) = 1.26–1.95) among current smokers compared with nonsmokers. For ex-smokers versus nonsmokers, the pooled OR for SLE risk was 1.23 (95 % CI = 0.93–1.63). Subgroup analysis by geographic location and cumulative meta-analysis were also analyzed. In conclusion, our meta-analysis suggested that smoking increased the risk of SLE. Further studies are needed to confirm this result.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Manzi S (2001) Epidemiology of systemic lupus erythematosus. Am J Manag Care 7(16 Suppl):S474–S479

    CAS  PubMed  Google Scholar 

  2. Theofilopoulos AN, Kono DH (1999) The genes of systemic autoimmunity. Proc Assoc Am Physicians 111(3):228–240

    Article  CAS  PubMed  Google Scholar 

  3. Wakeland EK, Wandstrat AE, Liu K, Morel L (1999) Genetic dissection of systemic lupus erythematosus. Curr Opin Immunol 11(6):701–707. doi:10.1016/s0952-7915(99)00039-4

    Article  CAS  PubMed  Google Scholar 

  4. Sanchez-Guerrero J, Karlson EW, Liang MH, Hunter DJ, Speizer FE, Colditz GA (1997) Past use of oral contraceptives and the risk of developing systemic lupus erythematosus. Arthritis Rheum 40(5):804–808. doi:10.1002/1529-0131(199705)40:5<804::AID-ART4>3.0.CO;2-E

    Article  CAS  PubMed  Google Scholar 

  5. Cooper GS, Dooley MA, Treadwell EL, St Clair EW, Parks CG, Gilkeson GS (1998) Hormonal, environmental, and infectious risk factors for developing systemic lupus erythematosus. Arthritis Rheum 41(10):1714–1724. doi:10.1002/1529-0131(199810)41:10<1714::aid-art3>3.0.co;2-u

    Article  CAS  PubMed  Google Scholar 

  6. Hess EV, Farhey Y (1995) Etiology, environmental relationships, epidemiology, and genetics of systemic lupus erythematosus. Curr Opin Rheumatol 7(5):371–375

    Article  CAS  PubMed  Google Scholar 

  7. Hopkinson ND (1991) Systemic lupus erythematosus: epidemiological clues to aetiology. Br J Hosp Med 45(5):291–293

    CAS  PubMed  Google Scholar 

  8. Karlson EW, Lee I, Cook NR, Manson JE, Buring JE, Hennekens CH (1999) A retrospective cohort study of cigarette smoking and risk of rheumatoid arthritis in female health professionals. Arthritis Rheum 42(5):910–917

    Article  CAS  PubMed  Google Scholar 

  9. Hutchinson D, Shepstone L, Moots R, Lear J, Lynch M (2001) Heavy cigarette smoking is strongly associated with rheumatoid arthritis (RA), particularly in patients without a family history of RA. Ann Rheum Dis 60(3):223–227

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Prummel MF, Wiersinga WM (1993) Smoking and risk of Graves’ disease. JAMA 269(4):479–482

    Article  CAS  PubMed  Google Scholar 

  11. Arnson Y, Shoenfeld Y, Amital H (2010) Effects of tobacco smoke on immunity, inflammation and autoimmunity. J Autoimmun 34(3):J258–J265

    Article  CAS  PubMed  Google Scholar 

  12. Reidenberg MM, Drayer DE, Lorenzo B, Strom BL, West SL, Snyder ES, Freundlich B, Stolley PD (1993) Acetylation phenotypes and environmental chemical exposure of people with idiopathic systemic lupus erythematosus. Arthritis Rheum 36(7):971–973

    Article  CAS  PubMed  Google Scholar 

  13. Nagata C, Fujita S, Iwata H, Kurosawa Y, Kobayashi K, Kobayashi M, Motegi K, Omura T, Yamamoto M, Nose T et al (1995) Systemic lupus erythematosus: a case–control epidemiologic study in Japan. Int J Dermatol 34(5):333–337

    Article  CAS  PubMed  Google Scholar 

  14. Hardy CJ, Palmer BP, Muir KR, Sutton AJ, Powell RJ (1998) Smoking history, alcohol consumption, and systemic lupus erythematosus: a case–control study. Ann Rheum Dis 57(8):451–455

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Sanchez-Guerrero J, Karlson EW, Colditz GA, Hunter DJ, Speizer FE, Liang MH (1996) Hair dye use and the risk of developing systemic lupus erythematosus. Arthritis Rheum 39(4):657–662

    Article  CAS  PubMed  Google Scholar 

  16. Costenbader KH, Kim DJ, Peerzada J, Lockman S, Nobles‐Knight D, Petri M, Karlson EW (2004) Cigarette smoking and the risk of systemic lupus erythematosus: a meta‐analysis. Arthritis Rheum 50(3):849–857

    Article  PubMed  Google Scholar 

  17. Bockle BC, Sepp NT (2015) Smoking is highly associated with discoid lupus erythematosus and lupus erythematosus tumidus: analysis of 405 patients. Lupus 24(7):669–674. doi:10.1177/0961203314559630

    Article  CAS  PubMed  Google Scholar 

  18. Washio M, Horiuchi T, Kiyohara C, Kodama H, Tada Y, Asami T, Takahashi H, Kobashi G, Abe T, Tanaka H, Nogami N, Harada M, Tsukamoto H, Ide S, Nagasawa K, Ushiyama O, Hotokebuchi T, Okamoto K, Sakamoto N, Sasaki S, Miyake Y, Yokoyama T, Mori M, Oura A, Sinomura Y, Suzuki H, Yamamoto M, Inaba Y, Nagai M (2006) Smoking, drinking, sleeping habits, and other lifestyle factors and the risk of systemic lupus erythematosus in Japanese females: findings from the KYSS study. Mod Rheumatol 16(3):143–150. doi:10.1007/s10165-006-0474-6

    Article  PubMed  Google Scholar 

  19. Ekblom-Kullberg S, Kautiainen H, Alha P, Leirisalo-Repo M, Julkunen H (2013) Smoking and the risk of systemic lupus erythematosus. Clin Rheumatol 32(8):1219–1222. doi:10.1007/s10067-013-2224-4

    Article  PubMed  Google Scholar 

  20. Young KA, Terrell DR, Guthridge JM, Kamen DL, Gilkeson GS, Karp DR, Ishimori ML, Weisman MH, Holers VM, Harley JB, Norris JM, James JA (2014) Smoking is not associated with autoantibody production in systemic lupus erythematosus patients, unaffected first-degree relatives, nor healthy controls. Lupus 23(4):360–369. doi:10.1177/0961203314520838

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. Chasset F, Frances C, Barete S, Barete S, Amoura Z, Arnaud L (2015) Influence of smoking on the efficacy of antimalarials in cutaneous lupus: a meta-analysis of the literature. J Am Acad Dermatol 72(4):634–639

    Article  CAS  PubMed  Google Scholar 

  22. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, Schaller JG, Talal N, Winchester RJ (1982) The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 25(11):1271–1277

    Article  CAS  PubMed  Google Scholar 

  23. Formica MK, Palmer JR, Rosenberg L, McAlindon TE (2003) Smoking, alcohol consumption, and risk of systemic lupus erythematosus in the Black Women's Health Study. J Rheumatol 30(6):1222–1226

    PubMed  Google Scholar 

  24. Higgins J, Thompson SG (2002) Quantifying heterogeneity in a meta‐analysis. Stat Med 21(11):1539–1558

    Article  PubMed  Google Scholar 

  25. Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327(7414):557–560. doi:10.1136/bmj.327.7414.557

    Article  PubMed Central  PubMed  Google Scholar 

  26. Patsopoulos NA, Evangelou E, Ioannidis JP (2008) Sensitivity of between-study heterogeneity in meta-analysis: proposed metrics and empirical evaluation. Int J Epidemiol 37(5):1148–1157

    Article  PubMed  Google Scholar 

  27. Tobias A (1999) Assessing the influence of a single study in the meta-analysis estimate. Stata Tech Bull 47:15–17

    Google Scholar 

  28. Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Benoni C, Nilsson A, Nived O (1990) Smoking and inflammatory bowel disease: comparison with systemic lupus erythematosus. A case–control study. Scand J Gastroenterol 25(7):751–755

    Article  CAS  PubMed  Google Scholar 

  30. Cooper GS, Dooley MA, Treadwell EL, St Clair EW, Gilkeson GS (2001) Smoking and use of hair treatments in relation to risk of developing systemic lupus erythematosus. J Rheumatol 28(12):2653–2656

    CAS  PubMed  Google Scholar 

  31. Ghaussy NO, Sibbitt WL Jr, Qualls CR (2001) Cigarette smoking, alcohol consumption, and the risk of systemic lupus erythematosus: a case–control study. J Rheumatol 28(11):2449–2453

    CAS  PubMed  Google Scholar 

  32. Costenbader KH, Karlson EW (2006) Cigarette smoking and autoimmune disease: what can we learn from epidemiology? Lupus 15(11):737–745

    Article  CAS  PubMed  Google Scholar 

  33. Munaafo MR, Flint J (2004) Meta-analysis of genetic association studies. Trends Genet 20(9):439–444

    Article  Google Scholar 

Download references

Author contributions

The authors’ contributions to the present study were as follows: Fan Jiang and Suyun Li contributed to data collection, systematic review, and data extraction; Fan Jiang did the data analyses and drafted the manuscript; and Chongqi Jia is responsible for the whole work.

Disclosures

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chongqi Jia.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiang, F., Li, S. & Jia, C. Smoking and the risk of systemic lupus erythematosus: an updated systematic review and cumulative meta-analysis. Clin Rheumatol 34, 1885–1892 (2015). https://doi.org/10.1007/s10067-015-3008-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10067-015-3008-9

Keywords

Navigation