Opportunistic salpingectomy for ovarian, fallopian tubal, and peritoneal carcinoma risk reduction
- Dianne M Miller, MD, FRCSC
Dianne M Miller, MD, FRCSC
- Division Head of Gynecologic Oncology
- University of British Columbia and the BC Cancer Agency
- Jessica N McAlpine, MD, FACOG, FRCPSC
Jessica N McAlpine, MD, FACOG, FRCPSC
- Associate Professor
- Department of Gynecology and Obstetrics Division of Gynecologic Oncology
- University of British Columbia
- Section Editors
- Barbara Goff, MD
Barbara Goff, MD
- Section Editor — Gynecologic Oncology
- Professor of Gynecologic Oncology
- University of Washington
- Howard T Sharp, MD
Howard T Sharp, MD
- Section Editor — Gynecologic Surgery
- Professor and Vice Chair for Clinical Activities
- Department of Obstetrics and Gynecology
- University of Utah Health Sciences Center
Opportunistic salpingectomy is the removal of the fallopian tubes for primary prevention of epithelial carcinoma of the fallopian tube, ovary, or peritoneum in a woman undergoing pelvic surgery for another indication. This is an approach to prevention in women at average risk, rather than high risk, for these cancers. Women at high risk of ovarian cancer are typically advised to undergo risk-reducing salpingo-oophorectomy.
The preventive strategy of opportunistic salpingectomy was introduced in the 2010s. This was based on data regarding the role of fallopian tube in the development of what had previously been presumed to be primary ovarian cancers, as a site of primary carcinogenesis or a conduit for neoplastic cells or carcinogens.
Opportunistic salpingectomy for ovarian, tubal, and peritoneal carcinoma risk reduction in average-risk women is reviewed here. Risk-reducing salpingo-oophorectomy for women at high risk of carcinoma of the ovary, fallopian tube, or peritoneum and the pathogenesis of serous carcinoma of the ovary, tube, and peritoneum are discussed separately. (See "Risk-reducing bilateral salpingo-oophorectomy in women at high risk of epithelial ovarian and fallopian tubal cancer" and "Pathogenesis of ovarian, fallopian tubal, and peritoneal serous carcinomas".)
OVERVIEW AND RATIONALE
Ovarian cancer is a disease with a poor prognosis and limited options in terms of screening, diagnosis, and treatment. Ovarian cancer is the second most common type of gynecologic malignancy and the most common cause of death from gynecologic cancer. It is the fifth most common cause of cancer deaths in women. In the United States and Canada every year, over 25,000 women are newly diagnosed with ovarian cancer, and 16,000 women die from the disease . (See "Epithelial carcinoma of the ovary, fallopian tube, and peritoneum: Epidemiology and risk factors", section on 'Epidemiology'.)
Ovarian cancer typically presents at an advanced stage and has a poor prognosis (table 1 and table 2). Unfortunately, there are few current approaches to improve clinical outcomes for ovarian cancer. There are no effective screening tests. For women who present with symptoms suggestive of ovarian cancer or with an adnexal mass, evaluation with serum biomarkers and/or pelvic imaging has a low specificity, and many women with a benign adnexal mass undergo unnecessary surgery (in one study, ovarian cancer was found in only 3.5 percent of procedures performed for a suspicious adnexal mass ) [3-6]. (See "Screening for ovarian cancer" and "Approach to the patient with an adnexal mass".)
- Canadian Cancer Society’s Advisory Committee on Cancer Statistics. Canadian Cancer Statistics 2014. Toronto ON: Canadian Cancer Society, 2014.
- Buys SS, Partridge E, Greene MH, et al. Ovarian cancer screening in the Prostate, Lung, Colorectal and Ovarian (PLCO) cancer screening trial: findings from the initial screen of a randomized trial. Am J Obstet Gynecol 2005; 193:1630.
- Kobayashi H, Yamada Y, Sado T, et al. A randomized study of screening for ovarian cancer: a multicenter study in Japan. Int J Gynecol Cancer 2008; 18:414.
- Menon U, Gentry-Maharaj A, Hallett R, et al. Sensitivity and specificity of multimodal and ultrasound screening for ovarian cancer, and stage distribution of detected cancers: results of the prevalence screen of the UK Collaborative Trial of Ovarian Cancer Screening (UKCTOCS). Lancet Oncol 2009; 10:327.
- Menon U, Kalsi J, Jacobs I. The UKCTOCS experience--reasons for hope? Int J Gynecol Cancer 2012; 22 Suppl 1:S18.
- Buys SS, Partridge E, Black A, et al. Effect of screening on ovarian cancer mortality: the Prostate, Lung, Colorectal and Ovarian (PLCO) Cancer Screening Randomized Controlled Trial. JAMA 2011; 305:2295.
- Bruckner HW, Cohen CJ, Goldberg JD, et al. Cisplatin regimens and improved prognosis of patients with poorly differentiated ovarian cancer. Am J Obstet Gynecol 1983; 145:653.
- Vogl SE, Pagano M, Kaplan BH, et al. Cis-platin based combination chemotherapy for advanced ovarian cancer. High overall response rate with curative potential only in women with small tumor burdens. Cancer 1983; 51:2024.
- Bristow RE, Chang J, Ziogas A, et al. High-volume ovarian cancer care: survival impact and disparities in access for advanced-stage disease. Gynecol Oncol 2014; 132:403.
- http://www.ovcare.ca/research/the_cheryl_brown_ovarian_cancer_outcomes_unit/ (Accessed on October 23, 2016).
- http://www.bccancer.bc.ca/HPI/CancerStatistics/default.htm (Accessed on October 23, 2016).
- Gilks CB, Ionescu DN, Kalloger SE, et al. Tumor cell type can be reproducibly diagnosed and is of independent prognostic significance in patients with maximally debulked ovarian carcinoma. Hum Pathol 2008; 39:1239.
- Singh N, Gilks CB, Hirshowitz L, et al. Adopting a Uniform Approach to Site Assignment in Tubo-Ovarian High-Grade Serous Carcinoma: The Time has Come. Int J Gynecol Pathol 2016; 35:230.
- McCluggage WG, Judge MJ, Clarke BA, et al. Data set for reporting of ovary, fallopian tube and primary peritoneal carcinoma: recommendations from the International Collaboration on Cancer Reporting (ICCR). Mod Pathol 2015; 28:1101.
- Singh N, Gilks CB, Hirschowitz L, et al. Primary site assignment in tubo-ovarian high-grade serous carcinoma: Consensus statement on unifying practice worldwide. Gynecol Oncol 2016; 141:195.
- Prat J, FIGO Committee on Gynecologic Oncology. Staging classification for cancer of the ovary, fallopian tube, and peritoneum. Int J Gynaecol Obstet 2014; 124:1.
- Olivier RI, Lubsen-Brandsma MA, Verhoef S, van Beurden M. CA125 and transvaginal ultrasound monitoring in high-risk women cannot prevent the diagnosis of advanced ovarian cancer. Gynecol Oncol 2006; 100:20.
- van der Velde NM, Mourits MJ, Arts HJ, et al. Time to stop ovarian cancer screening in BRCA1/2 mutation carriers? Int J Cancer 2009; 124:919.
- Woodward ER, Sleightholme HV, Considine AM, et al. Annual surveillance by CA125 and transvaginal ultrasound for ovarian cancer in both high-risk and population risk women is ineffective. BJOG 2007; 114:1500.
- Gilbert L, Basso O, Sampalis J, et al. Assessment of symptomatic women for early diagnosis of ovarian cancer: results from the prospective DOvE pilot project. Lancet Oncol 2012; 13:285.
- Hermsen BB, Olivier RI, Verheijen RH, et al. No efficacy of annual gynaecological screening in BRCA1/2 mutation carriers; an observational follow-up study. Br J Cancer 2007; 96:1335.
- Tone AA, Salvador S, Finlayson SJ, et al. The role of the fallopian tube in ovarian cancer. Clin Adv Hematol Oncol 2012; 10:296.
- Garrett LA, Growdon WB, Goodman A, et al. Endometriosis-associated ovarian malignancy: a retrospective analysis of presentation, treatment, and outcome. J Reprod Med 2013; 58:469.
- Wiegand KC, Hennessy BT, Leung S, et al. A functional proteogenomic analysis of endometrioid and clear cell carcinomas using reverse phase protein array and mutation analysis: protein expression is histotype-specific and loss of ARID1A/BAF250a is associated with AKT phosphorylation. BMC Cancer 2014; 14:120.
- Wiegand KC, Shah SP, Al-Agha OM, et al. ARID1A mutations in endometriosis-associated ovarian carcinomas. N Engl J Med 2010; 363:1532.
- Boyd J. Specific keynote: hereditary ovarian cancer: what we know. Gynecol Oncol 2003; 88:S8.
- Finch A, Beiner M, Lubinski J, et al. Salpingo-oophorectomy and the risk of ovarian, fallopian tube, and peritoneal cancers in women with a BRCA1 or BRCA2 Mutation. JAMA 2006; 296:185.
- Finch A, Shaw P, Rosen B, et al. Clinical and pathologic findings of prophylactic salpingo-oophorectomies in 159 BRCA1 and BRCA2 carriers. Gynecol Oncol 2006; 100:58.
- Callahan MJ, Crum CP, Medeiros F, et al. Primary fallopian tube malignancies in BRCA-positive women undergoing surgery for ovarian cancer risk reduction. J Clin Oncol 2007; 25:3985.
- Paley PJ, Swisher EM, Garcia RL, et al. Occult cancer of the fallopian tube in BRCA-1 germline mutation carriers at prophylactic oophorectomy: a case for recommending hysterectomy at surgical prophylaxis. Gynecol Oncol 2001; 80:176.
- Lamb JD, Garcia RL, Goff BA, et al. Predictors of occult neoplasia in women undergoing risk-reducing salpingo-oophorectomy. Am J Obstet Gynecol 2006; 194:1702.
- Leeper K, Garcia R, Swisher E, et al. Pathologic findings in prophylactic oophorectomy specimens in high-risk women. Gynecol Oncol 2002; 87:52.
- Lu KH, Garber JE, Cramer DW, et al. Occult ovarian tumors in women with BRCA1 or BRCA2 mutations undergoing prophylactic oophorectomy. J Clin Oncol 2000; 18:2728.
- Medeiros F, Muto MG, Lee Y, 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.
- Powell CB, Chen LM, McLennan J, et al. Risk-reducing salpingo-oophorectomy (RRSO) in BRCA mutation carriers: experience with a consecutive series of 111 patients using a standardized surgical-pathological protocol. Int J Gynecol Cancer 2011; 21:846.
- Colgan TJ, Murphy J, Cole DE, et al. Occult carcinoma in prophylactic oophorectomy specimens: prevalence and association with BRCA germline mutation status. Am J Surg Pathol 2001; 25:1283.
- Reitsma W, de Bock GH, Oosterwijk JC, et al. Support of the 'fallopian tube hypothesis' in a prospective series of risk-reducing salpingo-oophorectomy specimens. Eur J Cancer 2013; 49:132.
- Powell CB, Swisher EM, Cass I, et al. Long term follow up of BRCA1 and BRCA2 mutation carriers with unsuspected neoplasia identified at risk reducing salpingo-oophorectomy. Gynecol Oncol 2013; 129:364.
- Wethington SL, Park KJ, Soslow RA, et al. Clinical outcome of isolated serous tubal intraepithelial carcinomas (STIC). Int J Gynecol Cancer 2013; 23:1603.
- Powell CB, Kenley E, Chen LM, 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.
- Kindelberger DW, Lee Y, Miron A, et al. Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: Evidence for a causal relationship. Am J Surg Pathol 2007; 31:161.
- Carlson JW, Miron A, Jarboe EA, et al. Serous tubal intraepithelial carcinoma: its potential role in primary peritoneal serous carcinoma and serous cancer prevention. J Clin Oncol 2008; 26:4160.
- Seidman JD, Zhao P, Yemelyanova A. "Primary peritoneal" high-grade serous carcinoma is very likely metastatic from serous tubal intraepithelial carcinoma: assessing the new paradigm of ovarian and pelvic serous carcinogenesis and its implications for screening for ovarian cancer. Gynecol Oncol 2011; 120:470.
- Salvador S, Rempel A, Soslow RA, et al. Chromosomal instability in fallopian tube precursor lesions of serous carcinoma and frequent monoclonality of synchronous ovarian and fallopian tube mucosal serous carcinoma. Gynecol Oncol 2008; 110:408.
- Kauff ND, Domchek SM, Friebel TM, 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.
- Tang S, Onuma K, Deb P, et al. Frequency of serous tubal intraepithelial carcinoma in various gynecologic malignancies: a study of 300 consecutive cases. Int J Gynecol Pathol 2012; 31:103.
- Shaw PA, Rouzbahman M, Pizer ES, et al. Candidate serous cancer precursors in fallopian tube epithelium of BRCA1/2 mutation carriers. Mod Pathol 2009; 22:1133.
- Gilks CB, Irving J, Köbel M, et al. Incidental nonuterine high-grade serous carcinomas arise in the fallopian tube in most cases: further evidence for the tubal origin of high-grade serous carcinomas. Am J Surg Pathol 2015; 39:357.
- Morrison JC, Blanco LZ Jr, Vang R, Ronnett BM. Incidental serous tubal intraepithelial carcinoma and early invasive serous carcinoma in the nonprophylactic setting: analysis of a case series. Am J Surg Pathol 2015; 39:442.
- Crum CP, Drapkin R, Kindelberger D, et al. Lessons from BRCA: the tubal fimbria emerges as an origin for pelvic serous cancer. Clin Med Res 2007; 5:35.
- Crum CP, Drapkin R, Miron A, et al. The distal fallopian tube: a new model for pelvic serous carcinogenesis. Curr Opin Obstet Gynecol 2007; 19:3.
- Tobacman JK, Greene MH, Tucker MA, et al. Intra-abdominal carcinomatosis after prophylactic oophorectomy in ovarian-cancer-prone families. Lancet 1982; 2:795.
- Piver MS, Jishi MF, Tsukada Y, Nava G. Primary peritoneal carcinoma after prophylactic oophorectomy in women with a family history of ovarian cancer. A report of the Gilda Radner Familial Ovarian Cancer Registry. Cancer 1993; 71:2751.
- Struewing JP, Watson P, Easton DF, et al. Prophylactic oophorectomy in inherited breast/ovarian cancer families. J Natl Cancer Inst Monogr 1995; :33.
- Nishida N, Murakami F, Higaki K. Detection of serous precursor lesions in resected fallopian tubes from patients with benign diseases and a relatively low risk for ovarian cancer. Pathol Int 2016; 66:337.
- Rabban JT, Garg K, Crawford B, et al. Early detection of high-grade tubal serous carcinoma in women at low risk for hereditary breast and ovarian cancer syndrome by systematic examination of fallopian tubes incidentally removed during benign surgery. Am J Surg Pathol 2014; 38:729.
- McLaughlin JR, Risch HA, Lubinski J, et al. Reproductive risk factors for ovarian cancer in carriers of BRCA1 or BRCA2 mutations: a case-control study. Lancet Oncol 2007; 8:26.
- Narod SA, Sun P, Ghadirian P, et al. Tubal ligation and risk of ovarian cancer in carriers of BRCA1 or BRCA2 mutations: a case-control study. Lancet 2001; 357:1467.
- McGuire V, Felberg A, Mills 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.
- Tworoger SS, Fairfield KM, Colditz GA, et al. Association of oral contraceptive use, other contraceptive methods, and infertility with ovarian cancer risk. Am J Epidemiol 2007; 166:894.
- Hankinson SE, Hunter DJ, Colditz GA, et al. Tubal ligation, hysterectomy, and risk of ovarian cancer. A prospective study. JAMA 1993; 270:2813.
- Rice MS, Hankinson SE, Tworoger SS. Tubal ligation, hysterectomy, unilateral oophorectomy, and risk of ovarian cancer in the Nurses' Health Studies. Fertil Steril 2014; 102:192.
- Sieh W, Salvador S, McGuire V, et al. Tubal ligation and risk of ovarian cancer subtypes: a pooled analysis of case-control studies. Int J Epidemiol 2013; 42:579.
- Gaitskell K, Coffey K, Green J, et al. Tubal ligation and incidence of 26 site-specific cancers in the Million Women Study. Br J Cancer 2016; 114:1033.
- Gaitskell K, Green J, Pirie K, et al. Tubal ligation and ovarian cancer risk in a large cohort: Substantial variation by histological type. Int J Cancer 2016; 138:1076.
- Falconer H, Yin L, Grönberg H, Altman D. Ovarian cancer risk after salpingectomy: a nationwide population-based study. J Natl Cancer Inst 2015; 107.
- Madsen C, Baandrup L, Dehlendorff C, Kjaer SK. 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.
- Rice MS, Murphy MA, Vitonis AF, et al. Tubal ligation, hysterectomy and epithelial ovarian cancer in the New England Case-Control Study. Int J Cancer 2013; 133:2415.
- Sandoval C, Fung-Kee-Fung M, Gilks B, et al. Examining the use of salpingectomy with hysterectomy in Canada. Curr Oncol 2013; 20:173.
- www.ovcare.ca/prevention/ www.ovcare.ca/prevention/ (Accessed on April 23, 2014).
- Yoon SH, Kim SN, Shim SH, et al. Bilateral salpingectomy can reduce the risk of ovarian cancer in the general population: A meta-analysis. Eur J Cancer 2016; 55:38.
- McAlpine JN, Hanley GE, Woo MM, et al. Opportunistic salpingectomy: uptake, risks, and complications of a regional initiative for ovarian cancer prevention. Am J Obstet Gynecol 2014; 210:471.e1.
- http://www.cancer.ca/en/cancer-information/cancer-type/ovarian/risks/?region=on http://www.cancer.ca/en/cancer-information/cancer-type/ovarian/risks/?region=on (Accessed on March 28, 2014).
- Kapurubandara S, Qin V, Gurram D, et al. Opportunistic bilateral salpingectomy during gynaecological surgery for benign disease: A survey of current Australian practice. Aust N Z J Obstet Gynaecol 2015; 55:606.
- Venturella R, Rocca M, Lico D, et al. Prophylactic bilateral salpingectomy for the prevention of ovarian cancers: What is happening in Italy? Eur J Cancer Prev 2016; 25:410.
- Mikhail E, Salemi JL, Mogos MF, et al. 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.
- Hicks-Courant KD. Growth in salpingectomy rates in the United States since 2000. Am J Obstet Gynecol 2016; 215:666.
- Garcia C, Martin M, Tucker LY, et al. Experience With Opportunistic Salpingectomy in a Large, Community-Based Health System in the United States. Obstet Gynecol 2016; 128:277.
- Song T, Kim MK, Kim ML, et al. Impact of opportunistic salpingectomy on anti-Müllerian hormone in patients undergoing laparoscopic hysterectomy: a multicentre randomised controlled trial. BJOG 2016.
- DeStefano F, Huezo CM, Peterson HB, et al. Menstrual changes after tubal sterilization. Obstet Gynecol 1983; 62:673.
- Garza-Flores J, Vázquez-Estrada L, Reyes A, et al. Assessment of luteal function after surgical tubal sterilization. Adv Contracept 1991; 7:371.
- Dede FS, Dilbaz B, Akyuz O, et al. Changes in menstrual pattern and ovarian function following bipolar electrocauterization of the fallopian tubes for voluntary surgical contraception. Contraception 2006; 73:88.
- Nelson DB, Sammel MD, Freeman EW, et al. Tubal ligation does not affect hormonal changes during the early menopausal transition. Contraception 2005; 71:104.
- Dede FS, Akyuz O, Dilbaz B, et al. Color doppler flow analysis of uterine and ovarian arteries before and after tubal sterilization: electrocautery versus pomeroy. Gynecol Obstet Invest 2006; 61:45.
- Geber S, Caetano JP. Doppler colour flow analysis of uterine and ovarian arteries prior to and after surgery for tubal sterilization: a prospective study. Hum Reprod 1996; 11:1195.
- Reade CJ, Finlayson S, McAlpine J, et al. Risk-reducing salpingectomy in Canada: a survey of obstetrician-gynaecologists. J Obstet Gynaecol Can 2013; 35:627.
- Ye XP, Yang YZ, Sun XX. A retrospective analysis of the effect of salpingectomy on serum antiMüllerian hormone level and ovarian reserve. Am J Obstet Gynecol 2015; 212:53.e1.
- Morelli M, Venturella R, Mocciaro R, et al. Prophylactic salpingectomy in premenopausal low-risk women for ovarian cancer: primum non nocere. Gynecol Oncol 2013; 129:448.
- McAlpine, J, University of British Columbia, 2016, personal communication.
- GOC Evidentiary Statement https://www.g-o-c.org/uploads/11sept15_gocevidentiarystatement_final_en.pdf (Accessed on June 24, 2014).
- SGO Clinical Practice Statement https://www.sgo.org/clinical-practice/guidelines/sgo-clinical-practice-statement-salpingectomy-for-ovarian-cancer-prevention/ (Accessed on June 24, 2014).
- Committee on Gynecologic Practice. Committee opinion no. 620: Salpingectomy for ovarian cancer prevention. Obstet Gynecol 2015; 125:279.
- Pölcher M, Hauptmann S, Fotopoulou C, et al. Opportunistic salpingectomies for the prevention of a high-grade serous carcinoma: a statement by the Kommission Ovar of the AGO. Arch Gynecol Obstet 2015; 292:231.
- The Royal Australian and New Zealand College of Obstetricians and Gynaecologists. Managing the adnexae at hysterectomy for benign disease. July, 2009 (reviewed July, 2014).
- Hillis SD, Marchbanks PA, Tylor LR, Peterson HB. Poststerilization regret: findings from the United States Collaborative Review of Sterilization. Obstet Gynecol 1999; 93:889.
- Kwon JS, McAlpine JN, Hanley GE, et al. Costs and benefits of opportunistic salpingectomy as an ovarian cancer prevention strategy. Obstet Gynecol 2015; 125:338.
- Manchanda R, Menon U. Opportunistic bilateral salpingectomy (OBS) for the prevention of ovarian cancer should be offered in the context of a clinical trial: FOR: There is lack of clarity on a number of key issues. BJOG 2016; 123:463.
- Kehoe S. Opportunistic salpingectomy at benign gynaecological surgery for ovarian cancer prevention should be performed within a clinical trial: AGAINST: Can we afford to wait for the results? BJOG 2016; 123:464.
- OVERVIEW AND RATIONALE
- ROLE OF THE FALLOPIAN TUBE
- Fallopian tube and preinvasive lesions
- Tubal ligation and ovarian cancer risk
- OPPORTUNISTIC SALPINGECTOMY
- Informed consent
- - Ovarian cancer risk reduction
- - Implementation and morbidity
- - Ovarian function
- CLINICAL APPROACH
- SUMMARY AND RECOMMENDATIONS