Skip to main content

Advertisement

SpringerLink
Log in

Association of African-American ethnicity and smoking status with total and individual damage index in systemic lupus erythematosus

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

Abstract

Introduction

Smoking has been associated with increased incidence, severity of cutaneous lupus, and lupus activity. We looked at the association of both smoking and ethnicity with the individual damage items from the SLICC/ACR Damage Index.

Methods

Poisson regression was used to model the total SLICC/ACR Damage Index score against ever smoking. Cox regression was used to assess the relationship between time to individual damage items and ever smoking. Furthermore, we compared SLICC/ACR Damage Index items among African-American and Caucasian ever smokers.

Results

The study included 2629 patients, 52.6% Caucasian and 39.3% African-American. The prevalence of ever smokers was 35.8%. There was no significant difference in total SLICC/ACR Damage Index score between ever smokers and never smokers after adjustment for ethnicity, gender, age at diagnosis, and years of education. Ever smokers had more atherosclerotic cardiovascular damage and skin damage compared to non-smokers. Caucasian SLE patients who ever smoked were more likely to have muscle atrophy and atherosclerosis compared to Caucasian non-smokers. African-American patients who ever smoked were more likely to have skin damage compared to African-American non-smokers. African-Americans who smoked were more likely to have many more damage items (cataract, renal damage, pulmonary hypertension, cardiomyopathy, deforming or erosive arthritis, avascular necrosis, skin damage, and diabetes) compared to Caucasians who smoked.

Conclusion

Our analysis proved the major effect of smoking on cardiovascular and cutaneous damage. Surprisingly, cardiovascular damage items had higher hazard ratios in Caucasian smokers than non-smokers while skin damage items hazard ratios were higher in African-American smokers compared to non-smokers.

Key Points

• This study is the largest cohort study to date evaluating the effect of smoking on the cumulative SLICC/ACR Damage Index and its individual damage items.

• It is the only study that examined the effect of smoking on individual items of the SLICC/ACR Damage Index in terms of Caucasians vs. African-American ethnicity.

• Our analysis proved the major effect of smoking on cardiovascular and cutaneous damage. Compared to non-smokers, Caucasian smokers had higher risk of cardiovascular damage while African-American smokers had more skin damage.

• African-Americans who smoked were more likely to have many more damage items (cataract, renal damage, pulmonary hypertension, cardiomyopathy, deforming or erosive arthritis, avascular necrosis, skin damage, and diabetes) compared to Caucasians who smoked.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Gladman D, Ginzler E, Goldsmith C et al (1996) The development and initial validation of the Systemic Lupus International Collaborating Clinics/American College of Rheumatology damage index for systemic lupus erythematosus. Arthritis Rheum 39:363–369

    Article  CAS  PubMed  Google Scholar 

  2. Gladman DD, Urowitz MB, Goldsmith CH, Fortin P, Ginzler E, Gordon C, Hanly JG, Isenberg DA, Kalunian K, Nived O, Petri M, Sanchez-Guerrero J, Snaith M, Sturfelt G (1997) The reliability of the Systemic Lupus International Collaborating Clinics/American College of Rheumatology Damage Index in patients with systemic lupus erythematosus. Arthritis Rheum 40:809–813

    Article  CAS  PubMed  Google Scholar 

  3. Alarcon GS, McGwin G Jr, Bastian HM et al (2001) Systemic lupus erythematosus in three ethnic groups. VII [correction of VIII]. Predictors of early mortality in the LUMINA cohort. LUMINA Study Group. Arthritis Rheum 45:191–202

    Article  CAS  PubMed  Google Scholar 

  4. Rahman P, Gladman DD, Urowitz MB et al (2001) Early damage as measured by the SLICC/ACR damage index is a predictor of mortality in systemic lupus erythematosus. Lupus 10:93–96

    Article  CAS  PubMed  Google Scholar 

  5. Bruce IN, O’Keeffe AG, Farewell V et al (2015) Factors associated with damage accrual in patients with systemic lupus erythematosus: results from the Systemic Lupus International Collaborating Clinics (SLICC) Inception Cohort. Ann Rheum Dis 74:1706–1713

    Article  CAS  PubMed  Google Scholar 

  6. Petri M, Purvey S, Fang H, Magder LS (2012) Predictors of organ damage in systemic lupus erythematosus: the Hopkins Lupus Cohort. Arthritis Rheum 64:4021–4028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Legge A, Doucette S, Hanly JG (2016) Predictors of Organ damage progression and effect on health-related quality of life in systemic lupus erythematosus. J Rheumatol 43:1050–1056

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  9. Hardy CJ, Palmer BP, Muir KR et al (1998) Smoking history, alcohol consumption, and systemic lupus erythematosus: a case-control study. Ann Rheum Dis 57:451–455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  11. Kiyohara C, Washio M, Horiuchi T, Asami T, Ide S, Atsumi T, Kobashi G, Tada Y, Takahashi H, Kyushu Sapporo SLE (KYSS) Study Group (2012) Cigarette smoking, alcohol consumption, and risk of systemic lupus erythematosus: a case-control study in a Japanese population. J Rheumatol 39:1363–1370

    Article  PubMed  Google Scholar 

  12. Cozier YC, Barbhaiya M, Castro-Webb N, Conte C, Tedeschi SK, Leatherwood C, Costenbader KH, Rosenberg L (2019) Relationship of cigarette smoking and alcohol consumption to incidence of systemic lupus erythematosus in a prospective cohort study of black women. Arthritis Care Res (Hoboken) 71:671–677

    Article  Google Scholar 

  13. Miot HA, Bartoli Miot LD, Haddad GR (2005) Association between discoid lupus erythematosus and cigarette smoking. Dermatology 211:118–122

    Article  PubMed  Google Scholar 

  14. Turchin I, Bernatsky S, Clarke A et al (2009) Cigarette smoking and cutaneous damage in systemic lupus erythematosus. J Rheumatol 36:3–6

    Article  Google Scholar 

  15. Boeckler P, Cosnes A, Francès C, Hedelin G, Lipsker D (2009) Association of cigarette smoking but not alcohol consumption with cutaneous lupus erythematosus. Arch Dermatol 145:1012–1016

    Article  PubMed  Google Scholar 

  16. Piette EW, Foering KP, Chang AY, Okawa J, ten Have T, Feng R, Werth VP (2012) Impact of smoking in cutaneous lupus erythematosus. Arch Dermatol 148:317–322

    Article  PubMed  Google Scholar 

  17. Santiago-Casas Y, Vilá LM, McGwin G et al (2012) Association of discoid lupus erythematosus with clinical manifestations and damage accrual in a multiethnic lupus cohort. Arthritis Care Res (Hoboken) 64:704–712

    Article  Google Scholar 

  18. Ghaussy NO, Sibbitt WL, Bankhurst AD, Qualls CR (2003) Cigarette smoking and disease activity in systemic lupus erythematosus. J Rheumatol 30:1215–1221

    PubMed  Google Scholar 

  19. Bourre-Tessier J, Peschken CA, Bernatsky S et al (2013) Association of smoking with cutaneous manifestations in systemic lupus erythematosus. Arthritis Care Res 65:1275–1280

    Article  Google Scholar 

  20. Rahman P, Gladman DD, Urowitz MB (1998) Smoking interferes with efficacy of antimalarial therapy in cutaneous lupus. J Rheumatol 25:1716–1719

    CAS  PubMed  Google Scholar 

  21. Jewell ML, McCauliffe DE (2000) Patients with cutaneous lupus erythematosus who smoke are less responsive to antimalarial treatment. J Am Acad Dermatol 42:983–987

    Article  CAS  PubMed  Google Scholar 

  22. Moghadam-Kia S, Chilek K, Gaines E, Costner M, Rose ME, Okawa J, Werth VP (2009) Cross-sectional analysis of a collaborative web-based database for lupus erythematosus–associated skin lesions. Arch Dermatol 145:255–260

    Article  PubMed  PubMed Central  Google Scholar 

  23. Chasset F, Francès C, 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 72:634–639

    Article  CAS  PubMed  Google Scholar 

  24. Parodis I, Sjöwall C, Jönsen A et al (2017) Smoking and pre-existing organ damage reduce the efficacy of belimumab in systemic lupus erythematosus. Autoimmun Rev 16:343–351

    Article  CAS  PubMed  Google Scholar 

  25. Parodis I, Gomez A, Frodlund M, Jönsen A, Zickert A, Sjöwall C, Bengtsson AA, Gunnarsson I (2018) Smoking reduces the efficacy of belimumab in mucocutaneous lupus. Expert Opin Biol Ther 18:911–920

    Article  CAS  PubMed  Google Scholar 

  26. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health (1998) Tobacco use among U.S. racial/ethnic minority groups—African Americans, American Indians and Alaska Natives, Asian Americans and Pacific Islanders, and Hispanics: a report of the surgeon general. https://www.cdc.gov/tobacco/data_statistics/sgr/1998/complete_report.

  27. Ekblom-Kullberg S, Kautiainen H, Alha P et al (2014) Smoking, disease activity, permanent damage and dsDNA autoantibody production in patients with systemic lupus erythematosus. Rheumatol Int 34:341–345

    Article  CAS  PubMed  Google Scholar 

  28. Montes RA, Mocarzel LO, Lanzieri PG et al (2016) Smoking and its association with morbidity in systemic lupus erythematosus evaluated by the Systemic Lupus International Collaborating Clinics/American College of Rheumatology Damage Index: preliminary data and systematic review. Arthritis Rheumatol 68:441–448

    Article  PubMed  Google Scholar 

  29. Kim SK, Lee SS, Choe JY, Park SH, Lee H (2017) Effect of alcohol consumption and smoking on disease damage in systemic lupus erythematosus: data from the Korean Lupus Network (KORNET) registry. Lupus 26:1540–1549

    Article  PubMed  Google Scholar 

  30. Ward MM, Studenski S (1992) Clinical prognostic factors in lupus nephritis. The importance of hypertension and smoking. Arch Intern Med 152:2082–2088

    Article  CAS  PubMed  Google Scholar 

  31. Toloza SMA, Uribe AG, McGwin G et al (2004) Systemic lupus erythematosus in a multiethnic US cohort (LUMINA): XXIII. Baseline predictors of vascular events. Arthritis Rheum 50:3947–3957

    Article  PubMed  Google Scholar 

  32. Somers EC, Marder W, Cagnoli P et al (2014) Population-based incidence and prevalence of systemic lupus erythematosus: the Michigan Lupus Epidemiology and Surveillance program. Arthritis Rheumatol (Hoboken, NJ) 66:369–378

    Article  Google Scholar 

  33. Lim SS, Bayakly AR, Helmick CG et al (2014) The incidence and prevalence of systemic lupus erythematosus, 2002-2004: The Georgia Lupus Registry. Arthritis Rheumatol 66:357–368

    Article  PubMed  PubMed Central  Google Scholar 

  34. Petri M (2000) Hopkins Lupus Cohort. Rheum Dis Clin North Am 26:199–213

    Article  CAS  PubMed  Google Scholar 

  35. Alarcón GS, Calvo-Alén J, McGwin G et al (2006) Systemic lupus erythematosus in a multiethnic cohort: LUMINA XXXV. Predictive factors of high disease activity over time. Ann Rheum Dis 65:1168–1174

    Article  PubMed  PubMed Central  Google Scholar 

  36. Alarcón GS, McGwin G, Bartolucci AA et al (2001) Systemic lupus erythematosus in three ethnic groups: IX. Differences in damage accrual. Arthritis Rheum 44:2797–2806

    Article  PubMed  Google Scholar 

  37. Rubin RL, Hermanson TM, Bedrick EJ et al (2005) Effect of cigarette smoke on autoimmunity in murine and human systemic lupus erythematosus. Toxicol Sci 87:86–96

    Article  CAS  PubMed  Google Scholar 

  38. Kalra R, Singh SP, Savage SM, Finch GL, Sopori ML (2000) Effects of cigarette smoke on immune response: chronic exposure to cigarette smoke impairs antigen-mediated signaling in T cells and depletes IP3-sensitive Ca(2+) stores. J Pharmacol Exp Ther 293:166–171

    CAS  PubMed  Google Scholar 

  39. Freemer MM (2006) Association of smoking with dsDNA autoantibody production in systemic lupus erythematosus. Ann Rheum Dis 65:581–584

    Article  CAS  PubMed  Google Scholar 

  40. Kiani AN, Post WS, Magder LS, Petri M (2011) Predictors of progression in atherosclerosis over 2 years in systemic lupus erythematosus. Rheumatology (Oxford) 50:2071–2079

    Article  Google Scholar 

  41. Calvo-Alen J, Alarcon GS, Tew MB et al (2006) Systemic lupus erythematosus in a multiethnic US cohort: XXXIV. Deficient mannose-binding lectin exon 1 polymorphisms are associated with cerebrovascular but not with other arterial thrombotic events. Arthritis Rheum 54:1940–1945

    Article  PubMed  Google Scholar 

  42. Jones MR, Tellez-Plaza M, Navas-Acien A (2013) Smoking, menthol cigarettes and all-cause, cancer and cardiovascular mortality: evidence from the National Health and Nutrition Examination Survey (NHANES) and a meta-analysis. PLoS One 8:e77941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Barbhaiya M, Feldman CH, Guan H et al (2017) Race/ethnicity and cardiovascular events among patients with systemic lupus erythematosus. Arthritis Rheumatol (Hoboken, NJ) 69:1823–1831

    Article  Google Scholar 

  44. Krüger K, Dischereit G, Seimetz M et al (2015) Time course of cigarette smoke-induced changes of systemic inflammation and muscle structure. Am J Physiol Lung Cell Mol Physiol 309:L119–L128

    Article  PubMed  CAS  Google Scholar 

  45. Schiffenbauer A, Faghihi-Kashani S, O’Hanlon TP et al (2018) The effect of cigarette smoking on the clinical and serological phenotypes of polymyositis and dermatomyositis. Semin Arthritis Rheum 48:504–512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Hyland A, Piazza K, Hovey KM, Tindle HA, Manson JE, Messina C, Rivard C, Smith D, Wactawski-Wende J (2016) Associations between lifetime tobacco exposure with infertility and age at natural menopause: the Women’s Health Initiative Observational Study. Tob Control 25:706–714

    Article  PubMed  Google Scholar 

  47. Clair C, Cohen MJ, Eichler F, Selby KJ, Rigotti NA (2015) The effect of cigarette smoking on diabetic peripheral neuropathy: a systematic review and meta-analysis. J Gen Intern Med 30:1193–1203

    Article  PubMed  PubMed Central  Google Scholar 

  48. Kelsen SG, Duan X, Ji R et al (2008) Cigarette smoke induces an unfolded protein response in the human lung. Am J Respir Cell Mol Biol 38:541–550

    Article  CAS  PubMed  Google Scholar 

  49. McAlindon T, Giannotta L, Taub N, D'Cruz D, Hughes G (1993) Environmental factors predicting nephritis in systemic lupus erythematosus. Ann Rheum Dis 52:720–724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Petri M (1995) Musculoskeletal complications of systemic lupus erythematosus in the Hopkins Lupus Cohort: an update. Arthritis Care Res 8:137–145

    Article  CAS  PubMed  Google Scholar 

  51. Alderaan K, Sekicki V, Magder LS, Petri M (2015) Risk factors for cataracts in systemic lupus erythematosus (SLE). Rheumatol Int 35:701–708

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Rheumatology, Johns Hopkins University School of Medicine, 1830 East Monument Street, Suite 7500, Baltimore, MD, 21205, USA

    Romy Kallas, Jessica Li & Michelle Petri

Authors
  1. Romy Kallas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jessica Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michelle Petri
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Romy Kallas.

Ethics declarations

Disclosures

None.

Ethics approval

All patients gave written informed consent before taking part in the Hopkins Lupus Cohort. The Johns Hopkins University School of Medicine Institutional Review Board approved the Hopkins Lupus Cohort on an annual basis.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kallas, R., Li, J. & Petri, M. Association of African-American ethnicity and smoking status with total and individual damage index in systemic lupus erythematosus. Clin Rheumatol 39, 365–373 (2020). https://doi.org/10.1007/s10067-019-04800-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10067-019-04800-1

Keywords

Search

Navigation