Advertisement
Review Article| Volume 151, ISSUE 1, P166-175, October 2018

Download started.

Ok

Surgical prevention strategies in ovarian cancer

  • Author Footnotes
    1 Drs. Mallen and Soong contributed equally and are co-first authors.
    Adrianne Mallen
    Footnotes
    1 Drs. Mallen and Soong contributed equally and are co-first authors.
    Affiliations
    Department of Gynecologic Oncology, Moffitt Cancer Center, Tampa, FL, United States of America
    Search for articles by this author
  • Author Footnotes
    1 Drs. Mallen and Soong contributed equally and are co-first authors.
    T. Rinda Soong
    Footnotes
    1 Drs. Mallen and Soong contributed equally and are co-first authors.
    Affiliations
    Department of Pathology, University of Washington, Seattle, WA, United States of America
    Search for articles by this author
  • Mary K. Townsend
    Affiliations
    Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, FL, United States of America
    Search for articles by this author
  • Robert M. Wenham
    Affiliations
    Department of Gynecologic Oncology, Moffitt Cancer Center, Tampa, FL, United States of America
    Search for articles by this author
  • Author Footnotes
    2 Drs. Crum and Tworoger contributed equally and are co-last authors.
    Christopher P. Crum
    Footnotes
    2 Drs. Crum and Tworoger contributed equally and are co-last authors.
    Affiliations
    Department of Pathology, Division of Women's and Perinatal Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, United States of America
    Search for articles by this author
  • Author Footnotes
    2 Drs. Crum and Tworoger contributed equally and are co-last authors.
    Shelley S. Tworoger
    Correspondence
    Corresponding author at: 12902 Magnolia Drive, Tampa, FL 33612, United States of America.
    Footnotes
    2 Drs. Crum and Tworoger contributed equally and are co-last authors.
    Affiliations
    Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, FL, United States of America

    Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, United States of America
    Search for articles by this author
  • Author Footnotes
    1 Drs. Mallen and Soong contributed equally and are co-first authors.
    2 Drs. Crum and Tworoger contributed equally and are co-last authors.
Published:August 06, 2018DOI:https://doi.org/10.1016/j.ygyno.2018.08.005

      Highlights

      • Understanding of the etiology and pathogenesis of ovarian cancer has significantly evolved over the past two decades.
      • Surgical prophylactic surgery has saved lives in high-risk populations of women.
      • Although the evidence-base is limited, surgical risk-reduction methods have increasingly been applied to average-risk women.
      • There are different side effect profiles associated with various types of surgical prevention strategies.
      • Current prospective trials may offer evidence for less toxic alternative prophylactic surgical options in the future.

      Abstract

      Given the current lack of effective screening for ovarian cancer, surgical removal of at-risk tissue is the most successful strategy to decrease risk of cancer development. However, the optimal timing of surgery and tissues to remove, as well as the appropriate patients to undergo preventive procedures are poorly understood. In this review, we first discuss the origin and precursors of ovarian epithelial carcinomas, focusing on high-grade serous carcinomas and endometriosis-associated carcinomas, which cause the majority of the mortality and incidence of ovarian cancer. In addition, we summarize the implications of current understanding of specific pathogenic origins for surgical prevention and remaining gaps in knowledge. Secondly, we review evidence from the epidemiologic literature on the associations of various surgical prevention strategies, including endometriosis excision, tubal procedures, and bilateral salpingo-oophorectomy, with risk of future ovarian cancer development, as well as the short- and long-term consequences of these strategies on women's health and quality and life. We conclude with recommendations for surgical prevention in women with high-risk genetic mutations and average-risk women, and a brief discussion of ongoing research that will help clarify optimal surgical approaches that balance risk-reduction with maintenance of women's quality of life.

      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 Gynecologic Oncology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Kurman R.J.
        • Shih Ie M.
        Pathogenesis of ovarian cancer: lessons from morphology and molecular biology and their clinical implications.
        Int. J. Gynecol. Pathol. 2008; 27: 151-160
        • Prat J.
        • Ribe A.
        • Gallardo A.
        Hereditary ovarian cancer.
        Hum. Pathol. 2005; 36: 861-870
        • Walsh T.
        • Casadei S.
        • Lee M.K.
        • Pennil C.C.
        • Nord A.S.
        • Thornton A.M.
        • et al.
        Mutations in 12 genes for inherited ovarian, fallopian tube, and peritoneal carcinoma identified by massively parallel sequencing.
        Proc. Natl. Acad. Sci. U. S. A. 2011; 108: 18032-18037
        • Ring K.L.
        • Garcia C.
        • Thomas M.H.
        • Modesitt S.C.
        Current and future role of genetic screening in gynecologic malignancies.
        Am. J. Obstet. Gynecol. 2017; 217: 512-521
        • Flesken-Nikitin A.
        • Hwang C.I.
        • Cheng C.Y.
        • Michurina T.V.
        • Enikolopov G.
        • Nikitin A.Y.
        Ovarian surface epithelium at the junction area contains a cancer-prone stem cell niche.
        Nature. 2013; 495: 241-245
        • Sasaki R.
        • Narisawa-Saito M.
        • Yugawa T.
        • Fujita M.
        • Tashiro H.
        • Katabuchi H.
        • et al.
        Oncogenic transformation of human ovarian surface epithelial cells with defined cellular oncogenes.
        Carcinogenesis. 2009; 30: 423-431
        • Crum C.P.
        • Herfs M.
        • Ning G.
        • Bijron J.G.
        • Howitt B.E.
        • Jimenez C.A.
        • et al.
        Through the glass darkly: intraepithelial neoplasia, top-down differentiation, and the road to ovarian cancer.
        J. Pathol. 2013; 231: 402-412
        • Kindelberger D.W.
        • Lee Y.
        • Miron A.
        • Hirsch M.S.
        • Feltmate C.
        • Medeiros F.
        • et al.
        Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: evidence for a causal relationship.
        Am. J. Surg. Pathol. 2007; 31: 161-169
        • Medeiros F.
        • Muto M.G.
        • Lee Y.
        • Elvin J.A.
        • Callahan M.J.
        • Feltmate C.
        • et al.
        The tubal fimbria is a preferred site for early adenocarcinoma in women with familial ovarian cancer syndrome.
        Am. J. Surg. Pathol. 2006; 30: 230-236
        • Labidi-Galy S.I.
        • Papp E.
        • Hallberg D.
        • Niknafs N.
        • Adleff V.
        • Noe M.
        • et al.
        High grade serous ovarian carcinomas originate in the fallopian tube.
        Nat. Commun. 2017; 8: 1093
        • Marquez R.T.
        • Baggerly K.A.
        • Patterson A.P.
        • Liu J.
        • Broaddus R.
        • Frumovitz M.
        • et al.
        Patterns of gene expression in different histotypes of epithelial ovarian cancer correlate with those in normal fallopian tube, endometrium, and colon.
        Clin. Cancer Res. 2005; 11: 6116-6126
        • Ducie J.
        • Dao F.
        • Considine M.
        • Olvera N.
        • Shaw P.A.
        • Kurman R.J.
        • et al.
        Molecular analysis of high-grade serous ovarian carcinoma with and without associated serous tubal intra-epithelial carcinoma.
        Nat. Commun. 2017; 8: 990
        • Mehra K.K.
        • Chang M.C.
        • Folkins A.K.
        • Raho C.J.
        • Lima J.F.
        • Yuan L.
        • et al.
        The impact of tissue block sampling on the detection of p53 signatures in fallopian tubes from women with BRCA 1 or 2 mutations (BRCA+) and controls.
        Mod. Pathol. 2011; 24: 152-156
        • Lee Y.
        • Miron A.
        • Drapkin R.
        • Nucci M.R.
        • Medeiros F.
        • Saleemuddin A.
        • et al.
        A candidate precursor to serous carcinoma that originates in the distal fallopian tube.
        J. Pathol. 2007; 211: 26-35
        • Vang R.
        • Shih Ie M.
        • Kurman R.J.
        Fallopian tube precursors of ovarian low- and high-grade serous neoplasms.
        Histopathology. 2013; 62: 44-58
        • Xian W.
        • Miron A.
        • Roh M.
        • Semmel D.R.
        • Yassin Y.
        • Garber J.
        • et al.
        The Li-Fraumeni syndrome (LFS): a model for the initiation of p53 signatures in the distal Fallopian tube.
        J. Pathol. 2010; 220: 17-23
        • Meserve E.E.K.
        • Brouwer J.
        • Crum C.P.
        Serous tubal intraepithelial neoplasia: the concept and its application.
        Mod. Pathol. 2017; 30: 710-721
        • Chen F.
        • Gaitskell K.
        • Garcia M.J.
        • Albukhari A.
        • Tsaltas J.
        • Ahmed A.A.
        Serous tubal intraepithelial carcinomas associated with high-grade serous ovarian carcinomas: a systematic review.
        BJOG. 2017; 124: 872-878
        • Mahe E.
        • Tang S.
        • Deb P.
        • Sur M.
        • Lytwyn A.
        • Daya D.
        Do deeper sections increase the frequency of detection of serous tubal intraepithelial carcinoma (STIC) in the “sectioning and extensively examining the FIMbriated end” (SEE-FIM) protocol?.
        Int. J. Gynecol. Pathol. 2013; 32: 353-357
        • Powell C.B.
        • Kenley E.
        • Chen L.M.
        • Crawford B.
        • McLennan J.
        • Zaloudek C.
        • et al.
        Risk-reducing salpingo-oophorectomy in BRCA mutation carriers: role of serial sectioning in the detection of occult malignancy.
        J. Clin. Oncol. 2005; 23: 127-132
        • Soong T.R.H.B.
        • Ditzel H.M.
        • Campbell F.
        • Miron A.
        • Crum C.P.
        Serial sectioning and TP53 sequencing of occult intraepithelial lesions in distal fallopian tubes: Implications for the origin of high-grade serous ovarian serous carcinoma.
        in: United States and Canadian Academy of Pathology (USCAP) 2016 Annual Meeting. 2016
        • Eckert M.A.
        • Pan S.
        • Hernandez K.M.
        • Loth R.M.
        • Andrade J.
        • Volchenboum S.L.
        • et al.
        Genomics of ovarian cancer progression reveals diverse metastatic trajectories including intraepithelial metastasis to the fallopian tube.
        Cancer Discov. 2016; 6: 1342-1351
        • Anglesio M.S.
        • Bashashati A.
        • Wang Y.K.
        • Senz J.
        • Ha G.
        • Yang W.
        • et al.
        Multifocal endometriotic lesions associated with cancer are clonal and carry a high mutation burden.
        J. Pathol. 2015; 236: 201-209
        • Jarboe E.
        • Folkins A.
        • Nucci M.R.
        • Kindelberger D.
        • Drapkin R.
        • Miron A.
        • et al.
        Serous carcinogenesis in the fallopian tube: a descriptive classification.
        Int. J. Gynecol. Pathol. 2008; 27: 1-9
        • Tone A.A.
        Taking the tube: from normal fallopian tube epithelium to ovarian high-grade serous carcinoma.
        Clin. Obstet. Gynecol. 2017; 60: 697-710
        • McGuire V.
        • Felberg A.
        • Mills M.
        • Ostrow K.L.
        • Dicioccio R.
        • John E.M.
        • et al.
        Relation of contraceptive and reproductive history to ovarian cancer risk in carriers and noncarriers of BRCA1 gene mutations.
        Am. J. Epidemiol. 2004; 160: 613-618
        • McLaughlin J.R.
        • Risch H.A.
        • Lubinski J.
        • Moller P.
        • Ghadirian P.
        • Lynch H.
        • et al.
        Reproductive risk factors for ovarian cancer in carriers of BRCA1 or BRCA2 mutations: a case-control study.
        Lancet Oncol. 2007; 8: 26-34
        • Tung K.H.
        • Wilkens L.R.
        • Wu A.H.
        • McDuffie K.
        • Nomura A.M.
        • Kolonel L.N.
        • et al.
        Effect of anovulation factors on pre- and postmenopausal ovarian cancer risk: revisiting the incessant ovulation hypothesis.
        Am. J. Epidemiol. 2005; 161: 321-329
        • Trabert B.
        • Ness R.B.
        • Lo-Ciganic W.H.
        • Murphy M.A.
        • Goode E.L.
        • Poole E.M.
        • et al.
        Aspirin, nonaspirin nonsteroidal anti-inflammatory drug, and acetaminophen use and risk of invasive epithelial ovarian cancer: a pooled analysis in the Ovarian Cancer Association Consortium.
        J. Natl. Cancer Inst. 2014; 106 (djt431)
        • Wernli K.J.
        • Newcomb P.A.
        • Hampton J.M.
        • Trentham-Dietz A.
        • Egan K.M.
        Inverse association of NSAID use and ovarian cancer in relation to oral contraceptive use and parity.
        Br. J. Cancer. 2008; 98: 1781-1783
        • Cramer D.W.
        • Vitonis A.F.
        • Terry K.L.
        • Welch W.R.
        • Titus L.J.
        The association between talc use and ovarian cancer: a retrospective case-control study in two US states.
        Epidemiology. 2016; 27: 334-346
        • Kim H.S.
        • Kim T.H.
        • Chung H.H.
        • Song Y.S.
        Risk and prognosis of ovarian cancer in women with endometriosis: a meta-analysis.
        Br. J. Cancer. 2014; 110: 1878-1890
        • Mandai M.
        • Yamaguchi K.
        • Matsumura N.
        • Baba T.
        • Konishi I.
        Ovarian cancer in endometriosis: molecular biology, pathology, and clinical management.
        Int. J. Clin. Oncol. 2009; 14: 383-391
        • Wilbur M.A.
        • Shih I.M.
        • Segars J.H.
        • Fader A.N.
        Cancer Implications for patients with endometriosis.
        Semin. Reprod. Med. 2017; 35: 110-116
        • Aarnio M.
        • Sankila R.
        • Pukkala E.
        • Salovaara R.
        • Aaltonen L.A.
        • de la Chapelle A.
        • et al.
        Cancer risk in mutation carriers of DNA-mismatch-repair genes.
        Int. J. Cancer. 1999; 81: 214-218
        • Chui M.H.
        • Ryan P.
        • Radigan J.
        • Ferguson S.E.
        • Pollett A.
        • Aronson M.
        • et al.
        The histomorphology of Lynch syndrome-associated ovarian carcinomas: toward a subtype-specific screening strategy.
        Am. J. Surg. Pathol. 2014; 38: 1173-1181
        • Ogawa S.
        • Kaku T.
        • Amada S.
        • Kobayashi H.
        • Hirakawa T.
        • Ariyoshi K.
        • et al.
        Ovarian endometriosis associated with ovarian carcinoma: a clinicopathological and immunohistochemical study.
        Gynecol. Oncol. 2000; 77: 298-304
        • Stern R.C.
        • Dash R.
        • Bentley R.C.
        • Snyder M.J.
        • Haney A.F.
        • Robboy S.J.
        Malignancy in endometriosis: frequency and comparison of ovarian and extraovarian types.
        Int. J. Gynecol. Pathol. 2001; 20: 133-139
        • Guo S.W.
        Endometriosis and ovarian cancer: potential benefits and harms of screening and risk-reducing surgery.
        Fertil. Steril. 2015; 104: 813-830
        • Wentzensen N.
        • Poole E.M.
        • Trabert B.
        • White E.
        • Arslan A.A.
        • Patel A.V.
        • et al.
        Ovarian cancer risk factors by histologic subtype: an analysis from the ovarian cancer cohort consortium.
        J. Clin. Oncol. 2016; 34: 2888-2898
        • Mogensen J.B.
        • Kjaer S.K.
        • Mellemkjaer L.
        • Jensen A.
        Endometriosis and risks for ovarian, endometrial and breast cancers: a nationwide cohort study.
        Gynecol. Oncol. 2016; 143: 87-92
        • Sampson J.A.
        Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation.
        Am. J. Pathol. 1927; 3: 93-110
        • LaGrenade A.
        • Silverberg S.G.
        Ovarian tumors associated with atypical endometriosis.
        Hum. Pathol. 1988; 19: 1080-1084
        • Munksgaard P.S.
        • Blaakaer J.
        The association between endometriosis and ovarian cancer: a review of histological, genetic and molecular alterations.
        Gynecol. Oncol. 2012; 124: 164-169
        • Anglesio M.S.
        • Papadopoulos N.
        • Ayhan A.
        • Nazeran T.M.
        • Noe M.
        • Horlings H.M.
        • et al.
        Cancer-associated mutations in endometriosis without cancer.
        N. Engl. J. Med. 2017; 376: 1835-1848
        • Sato N.
        • Tsunoda H.
        • Nishida M.
        • Morishita Y.
        • Takimoto Y.
        • Kubo T.
        • et al.
        Loss of heterozygosity on 10q23.3 and mutation of the tumor suppressor gene PTEN in benign endometrial cyst of the ovary: possible sequence progression from benign endometrial cyst to endometrioid carcinoma and clear cell carcinoma of the ovary.
        Cancer Res. 2000; 60: 7052-7056
        • Wiegand K.C.
        • Shah S.P.
        • Al-Agha O.M.
        • Zhao Y.
        • Tse K.
        • Zeng T.
        • et al.
        ARID1A mutations in endometriosis-associated ovarian carcinomas.
        N. Engl. J. Med. 2010; 363: 1532-1543
        • Anglesio M.S.
        • Wang Y.K.
        • Maassen M.
        • Horlings H.M.
        • Bashashati A.
        • Senz J.
        • et al.
        Synchronous endometrial and ovarian carcinomas: evidence of clonality.
        J. Natl. Cancer Inst. 2016; 108 (djv428): 6
        • Izumi G.
        • Koga K.
        • Takamura M.
        • Makabe T.
        • Satake E.
        • Takeuchi A.
        • et al.
        Involvement of immune cells in the pathogenesis of endometriosis.
        J. Obstet. Gynaecol. Res. 2018; 44: 191-198
        • Bacci M.
        • Capobianco A.
        • Monno A.
        • Cottone L.
        • Di Puppo F.
        • Camisa B.
        • et al.
        Macrophages are alternatively activated in patients with endometriosis and required for growth and vascularization of lesions in a mouse model of disease.
        Am. J. Pathol. 2009; 175: 547-556
        • Capobianco A.
        • Rovere-Querini P.
        Endometriosis, a disease of the macrophage.
        Front. Immunol. 2013; 4: 9
        • Melin A.S.
        • Lundholm C.
        • Malki N.
        • Swahn M.L.
        • Sparen P.
        • Bergqvist A.
        Hormonal and surgical treatments for endometriosis and risk of epithelial ovarian cancer.
        Acta Obstet. Gynecol. Scand. 2013; 92: 546-554
        • Baldi A.
        • Campioni M.
        • Signorile P.G.
        Endometriosis: pathogenesis, diagnosis, therapy and association with cancer (review).
        Oncol. Rep. 2008; 19: 843-846
        • Rice M.S.
        • Murphy M.A.
        • Tworoger S.S.
        Tubal ligation, hysterectomy and ovarian cancer: a meta-analysis.
        J. Ovarian Res. 2012; 5: 13
        • Merritt M.A.
        • De Pari M.
        • Vitonis A.F.
        • Titus L.J.
        • Cramer D.W.
        • Terry K.L.
        Reproductive characteristics in relation to ovarian cancer risk by histologic pathways.
        Hum. Reprod. 2013; 28: 1406-1417
        • Rice M.S.
        • Murphy M.A.
        • Vitonis A.F.
        • Cramer D.W.
        • Titus L.J.
        • Tworoger S.S.
        • et al.
        Tubal ligation, hysterectomy and epithelial ovarian cancer in the New England Case-Control Study.
        Int. J. Cancer. 2013; 133: 2415-2421
        • Lessard-Anderson C.R.
        • Handlogten K.S.
        • Molitor R.J.
        • Dowdy S.C.
        • Cliby W.A.
        • Weaver A.L.
        • et al.
        Effect of tubal sterilization technique on risk of serous epithelial ovarian and primary peritoneal carcinoma.
        Gynecol. Oncol. 2014; 135: 423-427
        • Dilley S.E.
        • Straughn Jr., J.M.
        • Leath 3rd., C.A.
        The Evolution of and evidence for Opportunistic Salpingectomy.
        Obstet. Gynecol. 2017; 130: 814-824
        • Anggraeni T.D.
        • Al Fattah A.N.
        • Surya R.
        Prophylactic salpingectomy and ovarian cancer: an evidence-based analysis.
        South Asian J. Cancer. 2018; 7: 42-45
        • Castellano T.
        • Zerden M.
        • Marsh L.
        • Boggess K.
        Risks and benefits of salpingectomy at the time of sterilization.
        Obstet. Gynecol. Surv. 2017; 72: 663-668
        • Yoon S.H.
        • Kim S.N.
        • Shim S.H.
        • Kang S.B.
        • Lee S.J.
        Bilateral salpingectomy can reduce the risk of ovarian cancer in the general population: a meta-analysis.
        Eur. J. Cancer. 2016; 55: 38-46
        • Madsen C.
        • Baandrup L.
        • Dehlendorff C.
        • Kjaer S.K.
        Tubal ligation and salpingectomy and the risk of epithelial ovarian cancer and borderline ovarian tumors: a nationwide case-control study.
        Acta Obstet. Gynecol. Scand. 2015; 94: 86-94
        • Walker J.L.
        • Powell C.B.
        • Chen L.M.
        • Carter J.
        • Bae Jump V.L.
        • Parker L.P.
        • et al.
        Society of gynecologic oncology recommendations for the prevention of ovarian cancer.
        Cancer. 2015; 121: 2108-2120
        • Committee on Gynecologic P
        Committee opinion no. 620: salpingectomy for ovarian cancer prevention.
        Obstet. Gynecol. 2015; 125: 279-281
        • American College of O, Gynecologists
        ACOG Practice bulletin no. 133: benefits and risks of sterilization.
        Obstet. Gynecol. 2013; 121: 392-404
        • Curtis K.M.
        • Mohllajee A.P.
        • Peterson H.B.
        Regret following female sterilization at a young age: a systematic review.
        Contraception. 2006; 73: 205-210
        • Jamieson D.J.
        • Kaufman S.C.
        • Costello C.
        • Hillis S.D.
        • Marchbanks P.A.
        • Peterson H.B.
        • et al.
        A comparison of women's regret after vasectomy versus tubal sterilization.
        Obstet. Gynecol. 2002; 99: 1073-1079
        • Schmidt J.E.
        • Hillis S.D.
        • Marchbanks P.A.
        • Jeng G.
        • Peterson H.B.
        Requesting information about and obtaining reversal after tubal sterilization: findings from the U.S. Collaborative Review of Sterilization.
        Fertil. Steril. 2000; 74: 892-898
        • Morelli M.
        • Venturella R.
        • Mocciaro R.
        • Di Cello A.
        • Rania E.
        • Lico D.
        • et al.
        Prophylactic salpingectomy in premenopausal low-risk women for ovarian cancer: primum non nocere.
        Gynecol. Oncol. 2013; 129: 448-451
        • McAlpine J.N.
        • Hanley G.E.
        • Woo M.M.
        • Tone A.A.
        • Rozenberg N.
        • Swenerton K.D.
        • et al.
        Opportunistic salpingectomy: uptake, risks, and complications of a regional initiative for ovarian cancer prevention.
        Am. J. Obstet. Gynecol. 2014; 210: 471.e1-471.e11
        • Hanley G.E.
        • McAlpine J.N.
        • Pearce C.L.
        • Miller D.
        The performance and safety of bilateral salpingectomy for ovarian cancer prevention in the United States.
        Am. J. Obstet. Gynecol. 2017; 216: 270.e1-270.e9
        • Dar P.
        • Sachs G.S.
        • Strassburger D.
        • Bukovsky I.
        • Arieli S.
        Ovarian function before and after salpingectomy in artificial reproductive technology patients.
        Hum. Reprod. 2000; 15: 142-144
        • Sezik M.
        • Ozkaya O.
        • Demir F.
        • Sezik H.T.
        • Kaya H.
        Total salpingectomy during abdominal hysterectomy: effects on ovarian reserve and ovarian stromal blood flow.
        J. Obstet. Gynaecol. Res. 2007; 33: 863-869
        • Strandell A.
        • Lindhard A.
        • Waldenstrom U.
        • Thorburn J.
        Prophylactic salpingectomy does not impair the ovarian response in IVF treatment.
        Hum. Reprod. 2001; 16: 1135-1139
        • Yi Q.H.
        • Ling S.R.
        • Chen K.M.
        • He W.R.
        • Li L.
        • Yi C.J.
        Evaluation of the clinical value of simultaneous hysterectomy and bilateral salpingectomy in perimenopausal women.
        Zhonghua Fu Chan Ke Za Zhi. 2012; 47: 110-114
        • Morse A.N.
        • Schroeder C.B.
        • Magrina J.F.
        • Webb M.J.
        • Wollan P.C.
        • Yawn B.P.
        The risk of hydrosalpinx formation and adnexectomy following tubal ligation and subsequent hysterectomy: a historical cohort study.
        Am. J. Obstet. Gynecol. 2006; 194: 1273-1276
        • Chan C.C.
        • Ng E.H.
        • Li C.F.
        • Ho P.C.
        Impaired ovarian blood flow and reduced antral follicle count following laparoscopic salpingectomy for ectopic pregnancy.
        Hum. Reprod. 2003; 18: 2175-2180
        • Gelbaya T.A.
        • Nardo L.G.
        • Fitzgerald C.T.
        • Horne G.
        • Brison D.R.
        • Lieberman B.A.
        Ovarian response to gonadotropins after laparoscopic salpingectomy or the division of fallopian tubes for hydrosalpinges.
        Fertil. Steril. 2006; 85: 1464-1468
        • Lowder J.L.
        • Oliphant S.S.
        • Ghetti C.
        • Burrows L.J.
        • Meyn L.A.
        • Balk J.
        Prophylactic bilateral oophorectomy or removal of remaining ovary at the time of hysterectomy in the United States, 1979–2004.
        Am. J. Obstet. Gynecol. 2010; 202: 538.e1-538.e9
        • Mikhail E.
        • Salemi J.L.
        • Mogos M.F.
        • Hart S.
        • Salihu H.M.
        • Imudia A.N.
        National trends of adnexal surgeries at the time of hysterectomy for benign indication, United States, 1998–2011.
        Am. J. Obstet. Gynecol. 2015; 213: 713.e1-713.e13
        • Evans E.C.
        • Matteson K.A.
        • Orejuela F.J.
        • Alperin M.
        • Balk E.M.
        • El-Nashar S.
        • et al.
        Salpingo-oophorectomy at the time of benign hysterectomy: a systematic review.
        Obstet. Gynecol. 2016; 128: 476-485
        • Fuso L.
        • Mazzola S.
        • Ferrero A.
        • Magistris A.
        • Jacomuzzi M.E.
        • Carus A.P.
        • et al.
        Attitudes of Italian gynaecologists towards prophylactic oophorectomy at hysterectomy for non-malignant conditions.
        Eur. J. Obstet. Gynecol. Reprod. Biol. 2006; 124: 82-87
        • Moscucci O.
        • Clarke A.
        Prophylactic oophorectomy: a historical perspective.
        J. Epidemiol. Community Health. 2007; 61: 182-184
        • Jacoby V.L.
        • Grady D.
        • Wactawski-Wende J.
        • Manson J.E.
        • Allison M.A.
        • Kuppermann M.
        • et al.
        Oophorectomy vs ovarian conservation with hysterectomy: cardiovascular disease, hip fracture, and cancer in the Women's Health Initiative Observational Study.
        Arch. Intern. Med. 2011; 171: 760-768
        • Chan J.K.
        • Urban R.
        • Capra A.M.
        • Jacoby V.
        • Osann K.
        • Whittemore A.
        • et al.
        Ovarian cancer rates after hysterectomy with and without salpingo-oophorectomy.
        Obstet. Gynecol. 2014; 123: 65-72
        • Judd H.L.
        Hormonal dynamics associated with the menopause.
        Clin. Obstet. Gynecol. 1976; 19: 775-788
        • Carlson K.J.
        • Miller B.A.
        • Fowler Jr., F.J.
        The Maine Women's Health Study: I Outcomes of hysterectomy.
        Obstet. Gynecol. 1994; 83: 556-565
        • Farquhar C.M.
        • Sadler L.
        • Stewart A.W.
        A prospective study of outcomes five years after hysterectomy in premenopausal women.
        Aust. N. Z. J. Obstet. Gynaecol. 2008; 48: 510-516
        • Kjerulff K.H.
        • Langenberg P.W.
        • Rhodes J.C.
        • Harvey L.A.
        • Guzinski G.M.
        • Stolley P.D.
        Effectiveness of hysterectomy.
        Obstet. Gynecol. 2000; 95: 319-326
        • Rhodes J.C.
        • Kjerulff K.H.
        • Langenberg P.W.
        • Guzinski G.M.
        Hysterectomy and sexual functioning.
        JAMA. 1999; 282: 1934-1941
        • Melton 3rd, L.J.
        • Khosla S.
        • Malkasian G.D.
        • Achenbach S.J.
        • Oberg A.L.
        • Riggs B.L.
        Fracture risk after bilateral oophorectomy in elderly women.
        J. Bone Miner. Res. 2003; 18: 900-905
        • Phung T.K.
        • Waltoft B.L.
        • Laursen T.M.
        • Settnes A.
        • Kessing L.V.
        • Mortensen P.B.
        • et al.
        Hysterectomy, oophorectomy and risk of dementia: a nationwide historical cohort study.
        Dement. Geriatr. Cogn. Disord. 2010; 30: 43-50
        • Rocca W.A.
        • Bower J.H.
        • Maraganore D.M.
        • Ahlskog J.E.
        • Grossardt B.R.
        • de Andrade M.
        • et al.
        Increased risk of cognitive impairment or dementia in women who underwent oophorectomy before menopause.
        Neurology. 2007; 69: 1074-1083
        • Rocca W.A.
        • Grossardt B.R.
        • Shuster L.T.
        • Stewart E.A.
        Hysterectomy, oophorectomy, estrogen, and the risk of dementia.
        Neurodegener. Dis. 2012; 10: 175-178
        • Farquhar C.M.
        • Harvey S.A.
        • Yu Y.
        • Sadler L.
        • Stewart A.W.
        A prospective study of 3 years of outcomes after hysterectomy with and without oophorectomy.
        Am. J. Obstet. Gynecol. 2006; 194: 711-717
        • Cooper K.
        • Lee A.
        • Chien P.
        • Raja E.
        • Timmaraju V.
        • Bhattacharya S.
        Outcomes following hysterectomy or endometrial ablation for heavy menstrual bleeding: retrospective analysis of hospital episode statistics in Scotland.
        BJOG. 2011; 118: 1171-1179
        • Rivera C.M.
        • Grossardt B.R.
        • Rhodes D.J.
        • Brown Jr., R.D.
        • Roger V.L.
        • Melton 3rd, L.J.
        • et al.
        Increased cardiovascular mortality after early bilateral oophorectomy.
        Menopause. 2009; 16: 15-23
        • Rocca W.A.
        • Grossardt B.R.
        • de Andrade M.
        • Malkasian G.D.
        • Melton 3rd., L.J.
        Survival patterns after oophorectomy in premenopausal women: a population-based cohort study.
        Lancet Oncol. 2006; 7: 821-828
        • Parker W.H.
        • Broder M.S.
        • Chang E.
        • Feskanich D.
        • Farquhar C.
        • Liu Z.
        • et al.
        Ovarian conservation at the time of hysterectomy and long-term health outcomes in the nurses' health study.
        Obstet. Gynecol. 2009; 113: 1027-1037
        • Howard B.V.
        • Kuller L.
        • Langer R.
        • Manson J.E.
        • Allen C.
        • Assaf A.
        • et al.
        Risk of cardiovascular disease by hysterectomy status, with and without oophorectomy: the Women's Health Initiative Observational Study.
        Circulation. 2005; 111: 1462-1470
        • Parker W.H.
        • Broder M.S.
        • Liu Z.
        • Shoupe D.
        • Farquhar C.
        • Berek J.S.
        Ovarian conservation at the time of hysterectomy for benign disease.
        Clin. Obstet. Gynecol. 2007; 50: 354-361
        • Erekson E.A.
        • Martin D.K.
        • Ratner E.S.
        Oophorectomy: the debate between ovarian conservation and elective oophorectomy.
        Menopause. 2013; 20: 110-114
        • Committee on Practice Bulletins-Gynecology CoGSoGO
        Practice bulletin no 182: hereditary breast and ovarian cancer syndrome.
        Obstet. Gynecol. 2017; 130: e110-e126
        • Kotsopoulos J.
        • Gronwald J.
        • Karlan B.Y.
        • Huzarski T.
        • Tung N.
        • Moller P.
        • et al.
        Hereditary Breast Cancer Clinical Study Group. Hormone Replacement Therapy After Oophorectomy and Breast Cancer Risk Among BRCA1 Mutation Carriers.
        JAMA Oncol. 2018; ([Epub ahead of print], PubMed PMID: 29710224)https://doi.org/10.1001/jamaoncol.2018.0211
        • Antoniou A.
        • Pharoah P.D.
        • Narod S.
        • Risch H.A.
        • Eyfjord J.E.
        • Hopper J.L.
        • 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
        • Chen S.
        • Parmigiani G.
        Meta-analysis of BRCA1 and BRCA2 penetrance.
        J. Clin. Oncol. 2007; 25: 1329-1333
        • Ford D.
        • Easton D.F.
        • Stratton M.
        • Narod S.
        • Goldgar D.
        • Devilee P.
        • 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; 62: 676-689
        • King M.C.
        • Marks J.H.
        • Mandell J.B.
        New York Breast Cancer Study G. Breast and ovarian cancer risks due to inherited mutations in BRCA1 and BRCA2.
        Science. 2003; 302: 643-646
        • Domchek S.M.
        • Friebel T.M.
        • Neuhausen S.L.
        • Wagner T.
        • Evans G.
        • Isaacs C.
        • et al.
        Mortality after bilateral salpingo-oophorectomy in BRCA1 and BRCA2 mutation carriers: a prospective cohort study.
        Lancet Oncol. 2006; 7: 223-229
        • Domchek S.M.
        • Friebel T.M.
        • Singer C.F.
        • Evans D.G.
        • Lynch H.T.
        • Isaacs C.
        • et al.
        Association of risk-reducing surgery in BRCA1 or BRCA2 mutation carriers with cancer risk and mortality.
        JAMA. 2010; 304: 967-975
        • Finch A.P.
        • Lubinski J.
        • Moller P.
        • Singer C.F.
        • Karlan B.
        • Senter L.
        • 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
        • Rebbeck T.R.
        • Kauff N.D.
        • Domchek S.M.
        Meta-analysis of risk reduction estimates associated with risk-reducing salpingo-oophorectomy in BRCA1 or BRCA2 mutation carriers.
        J. Natl. Cancer Inst. 2009; 101: 80-87
        • Nebgen D.R.
        • Hurteau J.
        • Holman L.L.
        • Bradford A.
        • Munsell M.F.
        • Soletsky B.R.
        • et al.
        Bilateral salpingectomy with delayed oophorectomy for ovarian cancer risk reduction: a pilot study in women with BRCA1/2 mutations.
        Gynecol. Oncol. 2018; 150 (PubMed PMID: 29735278): 79-84https://doi.org/10.1016/j.ygyno.2018.04.564
        • Harmsen M.G.
        • Arts-De Jong M.
        • Hoogerbrugge N.
        • Maas A.H.
        • Prins J.B.
        • Bulten J.
        • et al.
        Early salpingectomy (TUbectomy) with delayed oophorectomy to improve quality of life as alternative for risk-reducing salpingo-oophorectomy in BRCA1/2 mutation carriers (TUBA study): a prospective non-randomised multicentre study.
        BMC Cancer. 2015; 15: 593
        • Parker W.H.
        Bilateral oophorectomy versus ovarian conservation: effects on long-term women's health.
        J. Minim. Invasive Gynecol. 2010; 17: 161-166
        • Patil E.
        • Jensen J.T.
        Update on permanent contraception options for women.
        Curr. Opin. Obstet. Gynecol. 2015; 27: 465-470
        • Institute of Medicine, National Academies of Sciences, Engineering, and Medicine
        Ovarian Cancers: Evolving Paradigms in Research and Care.
        The National Academies Press, Washington, DC2016 (396 p)
        • Committee on Gynecologic P
        Committee opinion no 701: choosing the route of hysterectomy for benign disease.
        Obstet. Gynecol. 2017; 129: e155-e159