Advertisement

Risk Reduction and Survival Benefit of Risk-Reducing Salpingo-oophorectomy in Hereditary Breast Cancer: Meta-analysis and Systematic Review

  • Ye-Lei Xiao
    Affiliations
    Department of Endocrine and Breast Surgery, The First Affiliated Hospital of Chongqing Medical University, Chongqing Medical University, Chongqing, China
    Search for articles by this author
  • Kang Wang
    Affiliations
    Department of Endocrine and Breast Surgery, The First Affiliated Hospital of Chongqing Medical University, Chongqing Medical University, Chongqing, China
    Search for articles by this author
  • Qiang Liu
    Affiliations
    Department of General Surgery, People's Hospital of Dazu District, Chongqing, China
    Search for articles by this author
  • Jie Li
    Affiliations
    Department of Endocrine and Breast Surgery, The First Affiliated Hospital of Chongqing Medical University, Chongqing Medical University, Chongqing, China
    Search for articles by this author
  • Xiang Zhang
    Correspondence
    Address for correspondence: Hong-Yuan Li, MD, or Xiang Zhang, PhD, Department of the Endocrine and Breast Surgery, The First Affiliated hospital of Chongqing Medical University, Chongqing Medical University, Chongqing 400016, China
    Affiliations
    Department of Endocrine and Breast Surgery, The First Affiliated Hospital of Chongqing Medical University, Chongqing Medical University, Chongqing, China
    Search for articles by this author
  • Hong-Yuan Li
    Correspondence
    Address for correspondence: Hong-Yuan Li, MD, or Xiang Zhang, PhD, Department of the Endocrine and Breast Surgery, The First Affiliated hospital of Chongqing Medical University, Chongqing Medical University, Chongqing 400016, China
    Affiliations
    Department of Endocrine and Breast Surgery, The First Affiliated Hospital of Chongqing Medical University, Chongqing Medical University, Chongqing, China
    Search for articles by this author
Published:October 03, 2018DOI:https://doi.org/10.1016/j.clbc.2018.09.011

      Abstract

      Background

      Objections have been raised to performing risk-reducing salpingo-oophorectomy (RRSO) to reduce disease incidence and mortality of women with BRCA mutations. We aimed to examine the relationship between RRSO and breast cancer (BC) risk and mortality with a meta-analysis.

      Materials and Methods

      We conducted a comprehensive literature search using the PubMed and Embase databases for literature published from these databases' creation to September 2017. Hazard ratio (HR) estimates were identified directly from the original articles. Pooled results were calculated on the basis of nonoverlapping studies by fixed-effect meta-analysis.

      Results

      RRSO was associated with a significant reduction in the incidence of BC in women with BRCA1/2 mutations who had no history of BC (HR = 0.58; 95% confidence interval [CI], 0.37 to 0.78). Even in women with a history of BC, RRSO could reduce the risk of recurrence (HR = 0.50; 95% CI, 0.31 to 0.69). We further found that publication year was a critical interaction factor from a corresponding subgroup analyses in BC risk (Pheterogeneity = .024). In addition, we found that RRSO could improve the survival of women with BC (HR = 0.33; 95% CI, 0.28 to 0.38).

      Conclusion

      Summary estimates presented here indicate that RRSO was closely related to the reduced risk of BC caused by BRCA mutations, but publication year was a critical interaction factor and it should be noted that more recent studies have failed to find a significant reduction in BC risk associated with RRSO.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Clinical Breast Cancer
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Torre L.A.
        • Bray F.
        • Siegel R.L.
        • Ferlay J.
        • Lortet-Tieulent J.
        • Jemal A.
        Global cancer statistics, 2012.
        CA Cancer J Clin. 2015; 65: 87-108
        • Siegel R.L.
        • Miller K.D.
        • Jemal A.
        Cancer statistics, 2017.
        CA Cancer J Clin. 2017; 67: 7-30
        • Jemal A.
        • Tiwari R.C.
        • Murray T.
        • et al.
        Cancer statistics, 2004.
        CA Cancer J Clin. 2004; 54: 8-29
        • Ford D.
        • Easton D.F.
        • Stratton M.
        • et al.
        Genetic heterogeneity and penetrance analysis of the BRCA1 and BRCA2 genes in breast cancer families. The Breast Cancer Linkage Consortium.
        Am J Hum Genet. 1998; 2: 676-689
        • Antoniou A.
        • Pharoah P.D.
        • Narod S.
        • et al.
        Average risks of breast and ovarian cancer associated with BRCA1 or BRCA2 mutations detected in case series unselected for family history: a combined analysis of 22 studies.
        Am J Hum Genet. 2003; 72: 1117-1130
        • King M.C.
        • Marks J.H.
        • Mandell J.B.
        • et al.
        Breast and ovarian cancer risks due to inherited mutations in BRCA1 and BRCA2.
        Science. 2003; 302: 643-646
        • Li X.
        • You R.
        • Wang X.
        • et al.
        Effectiveness of prophylactic surgeries in BRCA1 or BRCA2 mutation carriers: a meta-analysis and systematic review.
        Clin Cancer Res. 2016; 22: 3971
        • Rebbeck T.R.
        • Friebel T.
        • Wagner T.
        • et al.
        Effect of short-term hormone replacement therapy on breast cancer risk reduction after bilateral prophylactic oophorectomy in BRCA1 and BRCA2 mutation carriers: the PROSE Study Group.
        J Clin Oncol. 2005; 23: 7804-7810
        • Kotsopoulos J.
        • Huzarski T.
        • Gronwald J.
        • et al.
        Bilateral oophorectomy and breast cancer risk in BRCA1 and BRCA2 mutation carriers.
        J Natl Cancer Inst. 2017; 109: djw177
        • Heemskerk-Gerritsen B.A.
        • Seynaeve C.
        • van Asperen C.J.
        • et al.
        Breast cancer risk after salpingo-oophorectomy in healthy BRCA1/2 mutation carriers: revisiting the evidence for risk reduction.
        J Natl Cancer Inst. 2015; 107: djv033
        • Domchek T.M.
        • Friebel T.M.
        • Singer C.F.
        • et al.
        Association of risk-reducing surgery in BRCA1 or BRCA2 mutation carriers with cancer risk and mortality.
        J Minimal Invasive Gynecol. 2010; 18: 140
        • Metcalfe K.
        • Lynch H.T.
        • Foulkes W.D.
        • et al.
        Effect of oophorectomy on survival after breast cancer in BRCA1 and BRCA2 mutation carriers.
        JAMA Oncol. 2015; 1: 306
        • Finch A.P.
        • Lubinski J.
        • Maller P.
        • et al.
        Impact of oophorectomy on cancer incidence and mortality in women with a BRCA1 or BRCA2 mutation.
        J Clin Oncol. 2014; 32: 1547-1553
        • Moher D.
        • Liberati A.
        • Tetzlaff J.
        • Altman D.G.
        Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement.
        Open Med. 2009; 3: e123-e130
        • Wells G.
        • Shea B.
        • O'Connell D.
        • et al.
        The Newcastle-Ottawa Scale (NOS) for assessing the quality of non-randomised studies in meta-analyses.
        (Available at:)
        http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp
        Date: 2000
        Date accessed: October 11, 2018
        • Johns D.
        • Agarwal J.
        • Anderson L.
        • Ying J.
        • Kohlmann W.
        Breast cancer risk reduction decisions of the BRCA-positive patient: an observational study at a single institution.
        J Womens Health (Larchmt). 2017; 26: 702-706
        • Metcalfe K.
        • Lynch H.T.
        • Ghadirian P.
        • et al.
        Risk of ipsilateral breast cancer in BRCA1 and BRCA2 mutation carriers.
        Breast Cancer Res Treat. 2011; 127: 287-296
        • Huzarski T.
        • Byrski T.
        • Gronwald J.
        • et al.
        The impact of oophorectomy on survival after breast cancer in BRCA1-positive breast cancer patients.
        Breast Cancer Res Treat. 2016; 156: 371-378
        • Mavaddat N.
        • Peock S.
        • Frost D.
        • et al.
        Cancer risks for BRCA1 and BRCA2 mutation carriers: results from prospective analysis of EMBRACE.
        J Natl Cancer Inst. 2013; 105: 812-822
        • Kramer J.L.
        • Velazquez I.A.
        • Chen B.E.
        • et al.
        Prophylactic oophorectomy reduces breast cancer penetrance during prospective, long-term follow-up of BRCA1 mutation carriers.
        J Clin Oncol. 2005; 23: 8629-8635
        • Møller P.
        • Borg Åke
        • Evans D.G.
        • et al.
        Survival in prospectively ascertained familial breast cancer: analysis of a series stratified by tumour characteristics, BRCA mutations and oophorectomy.
        Int J Cancer. 2002; 101: 555-559
        • Kauff N.D.
        • Domchek S.M.
        • Friebel T.M.
        • et al.
        Risk-reducing salpingo-oophorectomy for the prevention of BRCA1- and BRCA2-associated breast and gynecologic cancer: a multicenter, prospective study.
        J Clin Oncol. 2008; 26: 1331-1337
        • Finkelman B.S.
        • Rubinstein W.S.
        • Friedman S.
        • et al.
        Breast and ovarian cancer risk and risk reduction in Jewish BRCA1/2 mutation carriers.
        J Clin Oncol. 2012; 30: 1321
        • Metcalfe K.
        • Lynch H.T.
        • Ghadirian P.
        • et al.
        Contralateral breast cancer in BRCA1 and BRCA2 mutation carriers.
        J Clin Oncol. 2004; 22: 2328-2335
        • Brekelmans C.T.M.
        • Seynaeve C.
        • Menke-Pluymers M.
        • et al.
        Survival and prognostic factors in BRCA1-associated breast cancer.
        Ann Oncol. 2006; 17: 391
        • Chang-Claude J.
        • Andrieu N.
        • Rookus M.
        • et al.
        Age at menarche and menopause and breast cancer risk in the international BRCA1/2 Carrier Cohort study.
        Cancer Epidemiol Biomarkers Prev. 2007; 16: 740-746
        • Eisen A.
        • Lubinski J.
        • Klijn J.
        • et al.
        Breast cancer risk following bilateral oophorectomy in BRCA1 and BRCA2 mutation carriers: an international case–control study.
        J Clin Oncol. 2005; 23: 7491-7496
        • Evans D.G.R.
        • Ingham S.L.
        • Baildam A.
        • et al.
        Contralateral mastectomy improves survival in women with BRCA1/2-associated breast cancer.
        Breast Cancer Res Treat. 2013; 140: 135-142
        • van Sprundel T.C.
        • Schmidt M.K.
        • Rookus M.A.
        • et al.
        Risk reduction of contralateral breast cancer and survival after contralateral prophylactic mastectomy in BRCA1 or BRCA2 mutation carriers.
        Br J Cancer. 2005; 93: 287-292
        • Mavaddat N.
        • Barrowdale D.
        • Andrulis I.L.
        • et al.
        Pathology of breast and ovarian cancers among BRCA1 and BRCA2 mutation carriers: results from the Consortium of Investigators of Modifiers of BRCA1/2 (CIMBA).
        Cancer Epidemiol Biomarkers Prev. 2012; 21: 134-147
        • Brekelmans C.T.
        • Tilanus-Linthorst M.M.
        • Seynaeve C.
        • et al.
        Tumour characteristics, survival and prognostic factors of hereditary breast cancer from BRCA2-, BRCA1- and non-BRCA1/2 families as compared to sporadic breast cancer cases.
        Eur J Cancer. 2007; 43: 867-876
        • Fisher B.
        • Jeong J.H.
        • Bryant J.
        • et al.
        Treatment of lymph-node–negative, oestrogen-receptor–positive breast cancer.
        Lancet. 2004; 364: 858-868
        • Davidson N.E.
        • O'Neill A.M.
        • Vukov A.M.
        • et al.
        Chemoendocrine therapy for premenopausal women with axillary lymph node–positive, steroid hormone receptor–positive breast cancer.
        J Clin Oncol. 2005; 23: 5973-5982
        • Rossouw J.E.
        • Prentice R.L.
        • Manson J.E.
        • et al.
        Postmenopausal hormone therapy and risk of cardiovascular disease by age and years since menopause.
        JAMA. 2007; 297: 1465-1477
        • Manson J.E.
        • Allison M.A.
        • Rossouw J.E.
        • et al.
        Estrogen therapy and coronary-artery calcification.
        N Engl J Med. 2007; 356: 2591-2602