Abstract
Objective
We conducted a retrospective cohort study to examine cancer risk in a large cohort of systemic lupus erythematosus (SLE) patients in California.
Methods
The cohort consisted of individuals with SLE derived from statewide patient discharge data during the period 1991–2002. SLE patients were followed using cancer registry data to examine patterns of cancer development. Standardized incidence ratios (SIRs) and 95% CI were calculated to compare the observed to expected numbers of cancers based on age-, race-, and sex-specific incidence rates in the California population.
Results
The 30,478 SLE patients were observed for 157,969 person-years. A total of 1,273 cancers occurred within the observation interval. Overall cancer risk was significantly elevated (SIR = 1.14, 95% CI = 1.07–1.20). SLE patients had higher risks of vagina/vulva (SIR = 3.27, 95% CI = 2.41–4.31) and liver cancers (SIR = 2.70, 95% CI = 1.54–4.24). Elevated risks of lung, kidney, and thyroid cancers and several hematopoietic malignancies were also observed. Individuals had significantly lower risks of several screenable cancers, including breast, cervix, and prostate.
Conclusions
These data suggest that risks of several cancer types are elevated among SLE patients. Detailed studies of endogenous and exogenous factors that drive these associations are needed.
Similar content being viewed by others
References
Abu-Shakra M, Buskila D, Shoenfeld Y (2000) SLE and cancer. In: Shoenfeld Y, Gershwin ME (eds) Cancer and autoimmunity. Elsevier Science, pp 31–40
Abu-Shakra M, Gladman DD, Urowitz MB (2004) Mortality studies in SLE: how far can we improve survival of patients with SLE. Autoimmun Rev 3:418–420
Stahl-Hallengren C, Jonsen A, Nived O, Sturfelt G (2000) Incidence studies of systemic lupus erythematosus in Southern Sweden: increasing age, decreasing frequency of renal manifestations and good prognosis. J Rheumatol 27:685–691
Urowitz MB, Gladman DD (2000) How to improve morbidity and mortality in systemic lupus erythematosus. Rheumatology (Oxford) 39:238–244
Urowitz MB, Gladman DD, Abu-Shakra M, Farewell VT (1997) Mortality studies in systemic lupus erythematosus. Results from a single center. III. Improved survival over 24 years. J Rheumatol 24:1061–1065
Bernatsky S, Boivin JF, Joseph L et al (2005) An international cohort study of cancer in systemic lupus erythematosus. Arthritis Rheum 52:1481–1490
Bernatsky S, Ramsey-Goldman R, Rajan R et al (2005) Non-Hodgkin’s lymphoma in systemic lupus erythematosus. Ann Rheum Dis 64:1507–1509
Bjornadal L, Lofstrom B, Yin L, Lundberg IE, Ekbom A (2002) Increased cancer incidence in a Swedish cohort of patients with systemic lupus erythematosus. Scand J Rheumatol 31:66–71
Mellemkjaer L, Andersen V, Linet MS, Gridley G, Hoover R, Olsen JH (1997) Non-Hodgkin’s lymphoma and other cancers among a cohort of patients with systemic lupus erythematosus. Arthritis Rheum 40:761–768
Pettersson T, Pukkala E, Teppo L, Friman C (1992) Increased risk of cancer in patients with systemic lupus erythematosus. Ann Rheum Dis 51:437–439
Ragnarsson O, Grondal G, Steinsson K (2003) Risk of malignancy in an unselected cohort of Icelandic patients with systemic lupus erythematosus. Lupus 12:687–691
Xu Y, Wiernik PH (2001) Systemic lupus erythematosus and B-cell hematologic neoplasm. Lupus 10:841–850
Zintzaras E, Voulgarelis M, Moutsopoulos HM (2005) The risk of lymphoma development in autoimmune diseases: a meta-analysis. Arch Intern Med 165:2337–2344
Ramsey-Goldman R, Mattai SA, Schilling E et al (1998) Increased risk of malignancy in patients with systemic lupus erythematosus. J Investig Med 46:217–222
Sweeney DM, Manzi S, Janosky J et al (1995) Risk of malignancy in women with systemic lupus erythematosus. J Rheumatol 22:1478–1482
Kinlen LJ (1992) Malignancy in autoimmune diseases. J Autoimmun 5 (Suppl A):363–371
Bernatsky S, Clarke A, Ramsey-Goldman R (2002) Malignancy and systemic lupus erythematosus. Curr Rheumatol Rep 4:351–358
Oertel SH, Riess H (2002) Immunosurveillance, immunodeficiency and lymphoproliferations. Recent Results Cancer Res 159:1–8
Bhalla R, Ajmani HS, Kim WW, Swedler WI, Lazarevic MB, Skosey JL (1993) Systemic lupus erythematosus and Hodgkin’s lymphoma. J Rheumatol 20:1316–1320
Black KA, Zilko PJ, Dawkins RL, Armstrong BK, Mastaglia GL (1982) Cancer in connective tissue disease. Arthritis Rheum 25:1130–1133
Canoso JJ, Cohen AS (1974) Malignancy in a series of 70 patients with systemic lupus erythematosus. Arthritis Rheum 17:383–390
Green JA, Dawson AA, Walker W (1978) Systemic lupus erythematosus and lymphoma. Lancet 2:753–756
Abu-Shakra M, Gladman DD, Urowitz MB (1996) Malignancy in systemic lupus erythematosus. Arthritis Rheum 39:1050–1054
Cibere J, Sibley J, Haga M (2001) Systemic lupus erythematosus and the risk of malignancy. Lupus 10:394–400
Nived O, Bengtsson A, Jonsen A, Sturfelt G, Olsson H (2001) Malignancies during follow-up in an epidemiologically defined systemic lupus erythematosus inception cohort in southern Sweden. Lupus 10:500–504
Sultan SM, Ioannou Y, Isenberg DA (2000) Is there an association of malignancy with systemic lupus erythematosus? An analysis of 276 patients under long-term review. Rheumatology (Oxford) 39:1147–1152
Services USDoHaH (2000) ICD-9-CM: international classification of diseases, 9th Revision, Clinical modification, 6th edition, Washington DC
Cancer Reporting in California (1997) Standards for automated reporting. California cancer reporting system standards, vol II. California Department of Health Services, Cancer Surveillance Section, Sacramento, CA, December 1997
Cancer Reporting in California (1997) Data standards for regional registries and California Cancer Registry. California cancer reporting system standards, vol III. California Department of Health Services, Cancer Surveillance Section, Sacramento, CA, December 1997
Cancer Reporting in California (1998) Reporting procedures for physicians. California cancer reporting system standards, vol IV. California Department of Health Services, Cancer Surveillance Section, Sacramento, CA, January 1998
Cancer Reporting in California (1997) Abstracting and coding procedures for hospitals. California cancer reporting system standards, vol I. California Department of Health Services, Cancer Surveillance Section, Sacramento, CA, June 1997
Chen VW, Howe HL, Wu XC (2000) Cancer in North America, 1993–1997. Volume I: incidence. North American Association of Central Cancer Registries, Springfield
Seiffert JE, Price WT, Gordon B (1990) The California tumor registry: a state-of-the-art model for a regionalized, automated, population-based registry. Top Health Rec Manage 11:59–73
Integrity Program (1999) Data reengineering environment software. Vality Technology Inc., Boston
Allen M (2001) Validation of OSHPD and CCR insurance status. California Association of Central Cancer Registries Technical Conference, Riverside, CA
Fritz A, Percy C, Jack A et al (2000) International classification of diseases for oncology, 3rd edn. World Health Organization, Geneva
Breslow NE, Day NE (1987) Statistical methods in cancer research, Volume II: the design and analysis of cohort studies. International Agency for Research on Cancer, Lyon
Bernatsky S, Boivin JF, Joseph L et al (2002) Prevalence of factors influencing cancer risk in women with lupus: social habits, reproductive issues, and obesity. J Rheumatol 29:2551–2554
Bruce IN, Gladman DD, Urowitz MB (1998) Detection and modification of risk factors for coronary artery disease in patients with systemic lupus erythematosus: a quality improvement study. Clin Exp Rheumatol 16:435–440
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
Petri M, Perez-Gutthann S, Spence D, Hochberg MC (1992) Risk factors for coronary artery disease in patients with systemic lupus erythematosus. Am J Med 93:513–519
Rahman P, Urowitz MB, Gladman DD, Bruce IN, Genest J Jr (1999) Contribution of traditional risk factors to coronary artery disease in patients with systemic lupus erythematosus. J Rheumatol 26:2363–2368
Ahmed MM, Berney SM, Wolf RE et al (2006) Prevalence of active hepatitis C virus infection in patients with systemic lupus erythematosus. Am J Med Sci 331:252–256
Berthier S, Mougin C, Vercherin P et al (1999) Does a particular risk associated with papillomavirus infections exist in women with lupus? Rev Med Interne 20:128–132
Tam LS, Chan AY, Chan PK, Chang AR, Li EK (2004) Increased prevalence of squamous intraepithelial lesions in systemic lupus erythematosus: association with human papillomavirus infection. Arthritis Rheum 50:3619–3625
Thomas RH, Ridley CM, Black MM (1985) Lichen sclerosus et atrophicus associated with systemic lupus erythematosus. J Am Acad Dermatol 13:832–833
Gibbons RB, Westerman E (1988) Acute nonlymphocytic leukemia following short-term, intermittent, intravenous cyclophosphamide treatment of lupus nephritis. Arthritis Rheum 31:1552–1554
Lishner M, Hawker G, Amato D (1990) Chronic lymphocytic leukemia in a patient with systemic lupus erythematosus. Acta Haematol 84:38–39
Rosenthal NS, Farhi DC (1996) Myelodysplastic syndromes and acute myeloid leukemia in connective tissue disease after single-agent chemotherapy. Am J Clin Pathol 106:676–679
Vasquez S, Kavanaugh AF, Schneider NR, Wacholtz MC, Lipsky PE (1992) Acute nonlymphocytic leukemia after treatment of systemic lupus erythematosus with immunosuppressive agents. J Rheumatol 19:1625–1627
Elliott RW, Essenhigh DM, Morley AR (1982) Cyclophosphamide treatment of systemic lupus erythematosus: risk of bladder cancer exceeds benefit. Br Med J (Clin Res Ed) 284:1160–1161
Ortiz A, Gonzalez-Parra E, Alvarez-Costa G, Egido J (1992) Bladder cancer after cyclophosphamide therapy for lupus nephritis. Nephron 60:378–379
Thrasher JB, Miller GJ, Wettlaufer JN (1990) Bladder leiomyosarcoma following cyclophosphamide therapy for lupus nephritis. J Urol 143:119–121
Bernatsky S, Boivin JF, Joseph L et al (2005) Race/ethnicity and cancer occurrence in systemic lupus erythematosus. Arthritis Rheum 53:781–784
Alarcon GS, Calvo-Alen 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(9):1168–1174
Bernatsky SR, Cooper GS, Mill C, Ramsey-Goldman R, Clarke AE, Pineau CA (2006) Cancer screening in patients with systemic lupus erythematosus. J Rheumatol 33:45–49
Katz JN, Barrett J, Liang MH et al (1997) Sensitivity and positive predictive value of Medicare Part B physician claims for rheumatologic diagnoses and procedures. Arthritis Rheum 40:1594–1600
Löfström B, Backlin C, Sundström C, Ekbom A, Lundberg IE (2007) A closer look at non-Hodgkin’s lymphoma cases in a national Swedish systemic lupus erythematosus cohort: a nested case-control study. Ann Rheum Dis 66(12):1627–1632
Hochberg MC (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 40:1725
Acknowledgments
This work was funded by grant 1R21CA100759–01A2 (A. Parikh-Patel) from the National Cancer Institute. The collection of cancer incidence data used in this study was supported by the California Department of Health Services as part of the statewide cancer reporting program mandated by California Health and Safety Code Section 103885; the National Cancer Institute’s Surveillance, Epidemiology, and End Results Program under contract N01-PC-35136 awarded to the Northern California Cancer Center, contract N01-PC-35139 awarded to the University of Southern California, and contract N02-PC-15105 awarded to the Public Health Institute; and the Centers for Disease Control and Prevention’s National Program of Cancer Registries, under agreement #U55/CCR921930-02 awarded to the Public Health Institute. The ideas and opinions expressed herein are those of the author(s) and endorsement by the State of California, Department of Health Services, the National Cancer Institute, and the Centers for Disease Control and Prevention or their Contractors and Subcontractors is not intended nor should be inferred.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Parikh-Patel, A., White, R.H., Allen, M. et al. Cancer risk in a cohort of patients with systemic lupus erythematosus (SLE) in California. Cancer Causes Control 19, 887–894 (2008). https://doi.org/10.1007/s10552-008-9151-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10552-008-9151-8