Skip to main content

Advertisement

SpringerLink
Log in

No association between the risk of breast cancer and systemic lupus erythematosus: evidence from a meta-analysis

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

Abstract

Several studies have estimated breast cancer risk in patients with systemic lupus erythematosus (SLE) relative to the general population. However, the results have been inconclusive. Therefore, we conducted a meta-analysis to ascertain a more comprehensive conclusion. A systematic literature search of electronic databases including PubMed, Web of Science, Embase, Cochrane Library, and Scopus was conducted to identify eligible studies using multiple search strategies. Based on the degree of heterogeneity, a random-effect model was chosen to calculate the pooled standardized incidence rate (SIR) with 95% confidence interval (CI), to estimate the strength of association between SLE and breast cancer incidence risk. A total of 18 eligible studies including 110,720 patients with SLE were enrolled in this meta-analysis. The combined results showed no significant association between SLE and breast cancer incidence (SIRs = 1.012 (95% CI, 0.797–1.284)). Subgroup analysis by study type, ethnicity, follow-up years, sample size, and SLE diagnostic criteria also showed no altered risk for breast cancer incidence (the summary risk estimate of each subgroup ranged from 0.82 to 1.40 with no statistical significance). This meta-analysis suggests no direct association between SLE and risk of breast cancer incidence.

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

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

Similar content being viewed by others

References

  1. D’Cruz DP, Khamashta MA, Hughes GR (9561) Systemic lupus erythematosus. Lancet (London, England) 369:587–596

    Article  Google Scholar 

  2. Maidhof W, Hilas O (2012) Lupus: an overview of the disease and management options. P & T A Peer-Teviewed J Formul Manag 37(4):240–249

    Google Scholar 

  3. Carter EE, Barr SG, Clarke AE (2016) The global burden of SLE: prevalence, health disparities and socioeconomic impact. Nat Rev Rheumatol 12(10):605–620. https://doi.org/10.1038/nrrheum.2016.137

    Article  PubMed  Google Scholar 

  4. Tsokos GC, Lo MS, Reis PC, Sullivan KE (2016) New insights into the immunopathogenesis of systemic lupus erythematosus. Nat Rev Rheumatol 12(12):716–730. https://doi.org/10.1038/nrrheum.2016.186

    Article  CAS  PubMed  Google Scholar 

  5. Kang KY, Kim HO, Yoon HS, Lee J, Lee WC, Ko H-J, Ju JH, Cho CS, Kim HY, Park SH (2010) Incidence of cancer among female patients with systemic lupus erythematosus in Korea. Clin Rheumatol 29(4):381–388. https://doi.org/10.1007/s10067-009-1332-7

    Article  PubMed  Google Scholar 

  6. Kiss E, Kovacs L, Szodoray P (2010) Malignancies in systemic lupus erythematosus. Autoimmun Rev 9(4):195–199. https://doi.org/10.1016/j.autrev.2009.07.004

    Article  CAS  PubMed  Google Scholar 

  7. Cao L, Tong H, Xu G, Liu P, Meng H, Wang J, Zhao X, Tang Y, Jin J (2015) Systemic lupus erythematous and malignancy risk: a meta-analysis. PLoS One 10(4):e0122964. https://doi.org/10.1371/journal.pone.0122964

    Article  PubMed  PubMed Central  Google Scholar 

  8. Bernatsky S, Ramsey-Goldman R, Foulkes WD, Gordon C, Clarke AE (2011) Breast, ovarian, and endometrial malignancies in systemic lupus erythematosus: a meta-analysis. Br J Cancer 104(9):1478–1481. https://doi.org/10.1038/bjc.2011.115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Björnådal L, Löfström 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(2):66–71. https://doi.org/10.1080/03009740252937568

    Article  PubMed  Google Scholar 

  10. Parikh-Patel A, White RH, Allen M, Cress R (2008) Cancer risk in a cohort of patients with systemic lupus erythematosus (SLE) in California. Cancer Causes Control 19(8):887–894. https://doi.org/10.1007/s10552-008-9151-8

    Article  PubMed  PubMed Central  Google Scholar 

  11. Bernatsky S, Ramsey-Goldman R, Labrecque J, Joseph L, Boivin J-F, Petri M, Zoma A, Manzi S, Urowitz MB, Gladman D, Fortin PR, Ginzler E, Yelin E, Bae SC, Wallace DJ, Edworthy S, Jacobsen S, Gordon C, Dooley MA, Peschken CA, Hanly JG, Alarcón GS, Nived O, Ruiz-Irastorza G, Isenberg D, Rahman A, Witte T, Aranow C, Kamen DL, Steinsson K, Askanase A, Barr S, Criswell LA, Sturfelt G, Patel NM, Senécal JL, Zummer M, Pope JE, Ensworth S, el-Gabalawy H, McCarthy T, Dreyer L, Sibley J, St. Pierre Y, Clarke AE (2013) Cancer risk in systemic lupus: an updated international multi-centre cohort study. J Autoimmun 42:130–135. https://doi.org/10.1016/j.jaut.2012.12.009

    Article  PubMed  PubMed Central  Google Scholar 

  12. Dey D, Kenu E, Isenberg D (2013) Cancer complicating systemic lupus erythematosus—a dichotomy emerging from a nested case-control study. Lupus 22(9):919–927. https://doi.org/10.1177/0961203313497118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Ramsey-Goldman R, Mattai SA, Schilling E, Chiu Y-L, Alo CJ, Howe HL, Manzi S (1998) Increased risk of malignancy in patients with systemic lupus erythematosus. J Invest Med 46(5):217–222

    CAS  Google Scholar 

  14. Chen Y-J, Chang Y-T, Wang C-B, Wu C-Y (2010) Malignancy in systemic lupus erythematosus: a nationwide cohort study in Taiwan. Am J Med 123(12):1150. e1–1150. e6

    Article  Google Scholar 

  15. Dreyer L, Faurschou M, Mogensen M, Jacobsen S (2011) High incidence of potentially virus-induced malignancies in systemic lupus erythematosus: a long-term followup study in a Danish cohort. Arthritis Rheumatol 63(10):3032–3037. https://doi.org/10.1002/art.30483

    Article  Google Scholar 

  16. Wells G, Shea B, O’Connell D, Peterson J, Welch V, Losos M (2012) NewCastle–Ottawa quality assessment scale—case control studies

  17. Lewis RB, Castor CW, Knisley RE, Bole GG (1976) Frequency of neoplasia in systemic lupus erythematosus and rheumatoid arthritis. Arthritis Rheum 19(6):1256–1260. https://doi.org/10.1002/art.1780190605

    Article  CAS  PubMed  Google Scholar 

  18. 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(7):500–504. https://doi.org/10.1191/096120301678416079

    Article  CAS  PubMed  Google Scholar 

  19. Bernatsky S, Ramsey-Goldman R, Boivin JF, Joseph L, Moore AD, Rajan R, Clarke A (2003) Do traditional Gail model risk factors account for increased breast cancer in women with lupus? J Rheumatol 30(7):1505–1507

    PubMed  Google Scholar 

  20. Bernatsky S, Clarke A, Ramsey-Goldman R, Joseph L, Boivin JF, Rajan R, Moore AD, Leung MH, Allen A, Gordon C (2004) Hormonal exposures and breast cancer in a sample of women with systemic lupus erythematosus. Rheumatology 43(9):1178–1181. https://doi.org/10.1093/rheumatology/keh282

    Article  CAS  PubMed  Google Scholar 

  21. Bernatsky S, Clarke A, Ramsey-Goldman R, Boivin J, Joseph L, Rajan R et al (2004) Breast cancer stage at time of detection in women with systemic lupus erythematosus. Lupus 13(6):469–472. https://doi.org/10.1191/0961203304lu1008xx

    Article  CAS  PubMed  Google Scholar 

  22. Bernatsky S, Boivin JF, Joseph L, Manzi S, Ginzler E, Urowitz M, Gladman D, Fortin P, Gordon C, Barr S, Edworthy S, Bae SC, Petri M, Sibley J, Isenberg D, Rahman A, Steinsson K, Aranow C, Dooley MA, Alarcon GS, Hanly J, Sturfelt G, Nived O, Pope J, Ensworth S, Rajan R, el-Gabalawy H, McCarthy T, St. Pierre Y, Clarke A, Ramsey-Goldman R (2005) Race/ethnicity and cancer occurrence in systemic lupus erythematosus. Arthritis Rheum 53(5):781–784. https://doi.org/10.1002/art.21458

    Article  CAS  PubMed  Google Scholar 

  23. Chun BC, Bae SC (2005) Mortality and cancer incidence in Korean patients with systemic lupus erythematosus: results from the Hanyang lupus cohort in Seoul, Korea. Lupus 14(8):635–638. https://doi.org/10.1191/0961203305lu2180xx

    Article  PubMed  Google Scholar 

  24. Bernatsky S, Boivin JF, Joseph L, Rajan R, Zoma A, Manzi S, Ginzler E, Urowitz M, Gladman D, Fortin PR, Petri M, Edworthy S, Barr S, Gordon C, Bae SC, Sibley J, Isenberg D, Rahman A, Aranow C, Dooley MA, Steinsson K, Nived O, Sturfelt G, Alarcón G, Senécal JL, Zummer M, Hanly J, Ensworth S, Pope J, el-Gabalawy H, McCarthy T, St. Pierre Y, Ramsey-Goldman R, Clarke A (2005) An international cohort study of cancer in systemic lupus erythematosus. Arthritis Rheum 52(5):1481–1490. https://doi.org/10.1002/art.21029

    Article  CAS  PubMed  Google Scholar 

  25. Ruiz-Irastorza G, Ugarte A, Egurbide M, Garmendia M, Pijoan J, Martinez-Berriotxoa A et al (2007) Antimalarials may influence the risk of malignancy in systemic lupus erythematosus. Ann Rheum Dis 66(6):815–817. https://doi.org/10.1136/ard.2006.067777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Hidalgo-Conde A, de Haro Liger M, Abarca-Costalago M, Alvarez Perez M, Valdivielso-Felices P, Gonzalez-Santos P et al (2013) Incidence of cancer in a cohort of Spanish patients with systemic lupus erythematosus. Reumatologia Clinica 9(6):359–364. https://doi.org/10.1016/j.reuma.2012.10.015

    Article  PubMed  Google Scholar 

  27. Bernatsky S, Ramsey-Goldman R, Petri M, Urowitz MB, Gladman DD, Fortin PF, Ginzler E, Romero-Diaz J, Peschken C, Jacobsen S, Hanly JG, Gordon C, Nived O, Yelin EH, Isenberg D, Rahman A, Bae SC, Joseph L, Witte T, Ruiz-Irastorza G, Aranow C, Kamen D, Sturfeldt G, Foulkes WD, Hansen JE, St Pierre Y, Raymer PC, Tessier-Cloutier B, Clarke AE (2017) Breast cancer in systemic lupus. Lupus 26(3):311–315. https://doi.org/10.1177/0961203316664595

    Article  CAS  PubMed  Google Scholar 

  28. Pettersson T, Pukkala E, Teppo L, Friman C (1992) Increased risk of cancer in patients with systemic lupus erythematosus. Ann Rheum Dis 51(4):437–439. https://doi.org/10.1136/ard.51.4.437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Sweeney D, Manzi S, Janosky J, Selvaggi K, Ferri W, Medsger Jr T et al (1995) Risk of malignancy in women with systemic lupus erythematosus. J Rheumatol 22(8):1478–1482

    CAS  PubMed  Google Scholar 

  30. Abu-Shakra M, Gladman DD, Urowitz MB (1996) Malignancy in systemic lupus erythematosus. Arthritis Rheumatol 39(6):1050–1054. https://doi.org/10.1002/art.1780390625

    Article  CAS  Google Scholar 

  31. Mellemkjér 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 Rheumatol 40(4):761–768. https://doi.org/10.1002/art.1780400424

    Article  Google Scholar 

  32. 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 39(10):1147–1152. https://doi.org/10.1093/rheumatology/39.10.1147

    Article  CAS  PubMed  Google Scholar 

  33. Cibere J, Sibley J, Haga M (2001) Systemic lupus erythematosus and the risk of malignancy. Lupus 10(6):394–400. https://doi.org/10.1191/096120301678646128

    Article  CAS  PubMed  Google Scholar 

  34. Ragnarsson O, Gröndal G, Steinsson K (2003) Risk of malignancy in an unselected cohort of Icelandic patients with systemic lupus erythematosus. Lupus 12(9):687–691. https://doi.org/10.1191/0961203303lu443oa

    Article  CAS  PubMed  Google Scholar 

  35. Tarr T, Gyorfy B, Szekanecz E, Bhattoa HP, Zeher M, Szegedi G et al (2007) Occurrence of malignancies in Hungarian patients with systemic lupus erythematosus. Ann N Y Acad Sci 1108(1):76–82. https://doi.org/10.1196/annals.1422.008

    Article  PubMed  Google Scholar 

  36. Khaliq W, Qayyum R, Clough J, Vaidya D, Wolff AC, Becker DM (2015) Comparison of breast cancer risk in women with and without systemic lupus erythematosus in a Medicare population. Breast Cancer Res Treat 151(2):465–474. https://doi.org/10.1007/s10549-015-3412-5

    Article  PubMed  PubMed Central  Google Scholar 

  37. KH Y, Kuo CF, Huang LH, Huang WK, See LC (2016) Cancer risk in patients with inflammatory systemic autoimmune rheumatic diseases: a nationwide population-based dynamic cohort study in Taiwan. Medicine 95(18):e3540

    Article  Google Scholar 

  38. Gadalla SM, Amr S, Langenberg P, Baumgarten M, Davidson WF, Schairer C, Engels EA, Pfeiffer RM, Goedert JJ (2009) Breast cancer risk in elderly women with systemic autoimmune rheumatic diseases: a population-based case-control study. Br J Cancer 100(5):817–821. https://doi.org/10.1038/sj.bjc.6604906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Cammarata RJ, Rodnan GP, Jensen WN (1963) Systemic rheumatic disease and malignant lymphoma. Arch Intern Med 111(3):330–337. https://doi.org/10.1001/archinte.1963.03620270056009

    Article  CAS  PubMed  Google Scholar 

  40. Bernatsky S, Easton DF, Dunning A, Michailidou K, Ramsey-Goldman R, Gordon C, Clarke AE, Foulkes W (2012) Decreased breast cancer risk in systemic lupus erythematosus: the search for a genetic basis continues. Lupus 21(8):896–899. https://doi.org/10.1177/0961203312443992

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This study was supported by Mashhad University of Medical Sciences (grant number 960911).

Author information

Authors and Affiliations

  1. Rheumatic Diseases Research Center, Mashhad University of Medical Sciences, Mashhad, Iran

    Zahra Rezaieyazdi & Samira Tabaei

  2. Clinical Research Unit, Mashhad University of Medical Sciences, Mashhad, Iran

    Yalda Ravanshad & Hassan Mehrad-Majd

  3. Immunogenetics Research Center, Department of Medical Nanotechnology, School of Advanced Technologies in Medicine, Mazandaran University of Medical Sciences, Sari, Iran

    Javad Akhtari

Authors
  1. Zahra Rezaieyazdi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Samira Tabaei
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yalda Ravanshad
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Javad Akhtari
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hassan Mehrad-Majd
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hassan Mehrad-Majd.

Ethics declarations

Disclosures

None.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rezaieyazdi, Z., Tabaei, S., Ravanshad, Y. et al. No association between the risk of breast cancer and systemic lupus erythematosus: evidence from a meta-analysis. Clin Rheumatol 37, 1511–1519 (2018). https://doi.org/10.1007/s10067-017-3950-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10067-017-3950-9

Keywords

Search

Navigation