Abstract
Objective
To evaluate the benefit of risk-reducing salpingo-oophorectomy (RRSO) by estimating
the pathological positive rate of occult lesions, including serous tubal intraepithelial
carcinoma (STIC) and occult cancers (OCCs).
Methods
BRCA1/2 mutation carriers who underwent RRSO in a Chinese study center between 2014
and 2018 were included. A literature review was performed, followed by a meta-analysis
of the literature to further validate the findings.
Results
Twenty-four BRCA1/2 mutation carriers who underwent RRSO were identified; one patient
(4.2%) had STIC, and one patient (4.2%) had occult fallopian tube cancer complicated
by STIC. Thirty-four articles were ultimately included in the meta-analysis. Of the
reported cases of OCC, 61.3% occurred in the fallopian tubes and 32.3% in the ovaries,
and 81.5% were in the early stages. The estimated rate of overall pathological positive
events was 5%. The estimated rates of overall STIC events and OCC were 1% and 3%,
respectively. The rates of STIC and OCC were 1% and 3%, respectively, for BRCA1 mutation
carriers and 1% and 1%, respectively, for BRCA2 mutation carriers. No significant
difference was observed between the results of a routine examination of pathological
sections and those of the Sectioning and Extensively Examining the Fimbriae (SEE-FIM)
protocol.
Conclusions
This study is the first report of RRSO results in China. In this systematic review,
the positive rates of STIC or OCC after RRSO were no more than 3%, which are 200-fold
higher than the risk of the general population. The use of a strict SEE-FIM protocol
would likely increase positive results.
Keywords
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References
- Screening for ovarian cancer: updated evidence report and systematic review for the US preventive services task force.J Am Med Assoc. 2018; 319: 595-606
- Cancer statistics in China, 2015.CA A Cancer J Clin. 2016; 66: 115-132
- Breast and ovarian cancer risks due to inherited mutations in BRCA1 and BRCA2.Science. 2003; 302: 643-646
- Prevalence and penetrance of germline BRCA1 and BRCA2 mutations in a population series of 649 women with ovarian cancer.Am J Hum Genet. 2001; 68: 700-710
- The risk of cancer associated with specific mutations of BRCA1 and BRCA2 among Ashkenazi Jews.N Engl J Med. 1997; 336: 1401-1408
- Meta-analysis of BRCA1 and BRCA2 penetrance.J Clin Oncol. 2007; 25: 1329-1333
- 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
- Cancer risk estimates for BRCA1 mutation carriers identified in a risk evaluation program.J Natl Cancer Inst. 2002; 94: 1365-1372
- 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
- Prevalence and penetrance of BRCA1 and BRCA2 mutations in a population-based series of breast cancer cases. Anglian Breast Cancer Study Group.Br J Canc. 2000; 83: 1301-1308
- Ovarian cancer risk in Ashkenazi Jewish carriers of BRCA1 and BRCA2 mutations.Clin Cancer Res. 2002; 8: 3776-3781
- Ovarian cancer screening--current status, future directions.Gynecol Oncol. 2014; 132: 490-495
- Effect of screening on ovarian cancer mortality: the prostate, lung, colorectal and ovarian (PLCO) cancer screening randomized controlled trial.J Am Med Assoc. 2011; 305: 2295-2303
- Prophylactic oophorectomy in carriers of BRCA1 or BRCA2 mutations.N Engl J Med. 2002; 346: 1616-1622
- Risk-reducing salpingo-oophorectomy in women with a BRCA1 or BRCA2 mutation.N Engl J Med. 2002; 346: 1609-1615
- Salpingo-oophorectomy and the risk of ovarian, fallopian tube, and peritoneal cancers in women with a BRCA1 or BRCA2 Mutation.J Am Med Assoc. 2006; 296: 185-192
- Prophylactic oophorectomy reduces breast cancer penetrance during prospective, long-term follow-up of BRCA1 mutation carriers.J Clin Oncol. 2005; 23: 8629-8635
- Age at menarche and menopause and breast cancer risk in the International BRCA1/2 Carrier Cohort Study.Cancer Epidemiol Biomark Prev. 2007; 16: 740-746
- Breast cancer risk following bilateral oophorectomy in BRCA1 and BRCA2 mutation carriers: an international case-control study.J Clin Oncol. 2005; 23: 7491-7496
- Mortality after bilateral salpingo-oophorectomy in BRCA1 and BRCA2 mutation carriers: a prospective cohort study.Lancet Oncol. 2006; 7: 223-229
- Gynecologic surgeries and risk of ovarian cancer in women with BRCA1 and BRCA2 Ashkenazi founder mutations: an Israeli population-based case-control study.J Natl Cancer Inst. 2003; 95: 1072-1078
- 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
- Hereditary ovarian cancer.Crit Rev Oncol Hematol. 2009; 69: 28-44
- Association of risk-reducing surgery in BRCA1 or BRCA2 mutation carriers with cancer risk and mortality.J Am Med Assoc. 2010; 304: 967-975
- 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
- NIH consensus conference. Ovarian cancer. Screening, treatment, and follow-up. NIH Consensus Development Panel on Ovarian Cancer.J Am Med Assoc. 1995; 273: 491-497
- 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
- Occult ovarian tumors in women with BRCA1 or BRCA2 mutations undergoing prophylactic oophorectomy.J Clin Oncol. 2000; 18: 2728-2732
- Predictors of occult neoplasia in women undergoing risk-reducing salpingo-oophorectomy.Am J Obstet Gynecol. 2006; 194: 1702-1709
- Microscopic and early-stage ovarian cancers in BRCA1/2 mutation carriers: building a model for early BRCA-associated tumorigenesis.Cancer Prev Res. 2011; 4: 463-470
- 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: 846-851
- Outcome of unexpected adnexal neoplasia discovered during risk reduction salpingo-oophorectomy in women with germ-line BRCA1 or BRCA2 mutations.Gynecol Oncol. 2014; 132: 280-286
- Clinical outcome of isolated serous tubal intraepithelial carcinomas (STIC).Int J Gynecol Cancer. 2013; 23: 1603-1611
- Occult and subsequent cancer incidence following risk-reducing surgery in BRCA mutation carriers.Gynecol Oncol. 2016; 143: 231-235
- The role of routine peritoneal and omental biopsies at risk-reducing salpingo-oophorectomy.J Minim Invasive Gynecol. 2017; 24: 772-776
- Characteristics of african American women at high-risk for ovarian cancer in the southeast: results from a gynecologic cancer risk assessment clinic.Gynecol Oncol. 2018; 149: 337-340
- Intra-operative evaluation of prophylactic hysterectomy and salpingo-oophorectomy specimens in hereditary gynaecological cancer syndromes.Histopathology. 2018; 73: 109-123
- Risk-reducing surgery for ovarian cancer: outcomes in 300 surgeries suggest a low peritoneal primary risk.Eur J Hum Genet. 2009; 17: 1381-1385
- Outcome of risk-reducing salpingo-oophorectomy in BRCA carriers and women of unknown mutation status.BJOG. 2011; 118: 814-824
- High rates of occult fallopian tube cancer diagnosed at prophylactic bilateral salpingo-oophorectomy.Int J Gynecol Cancer. 2009; 19: 826-829
- Impact of lifestyle factors on preneoplastic changes in prophylactic oophorectomies of BRCA mutation carriers.Eur J Cancer Prev. 2012; 21: 199-204
- Challenging salpingectomy as a risk-reducing measure for ovarian cancer: histopathological analysis of the tubo-ovarian interface in women undergoing risk-reducing salpingo-oophorectomy.Int J Gynecol Cancer. 2017; 27: 703-707
- Occult carcinoma in prophylactic oophorectomy specimens: prevalence and association with BRCA germline mutation status.Am J Surg Pathol. 2001; 25: 1283-1289
- Clinical and pathologic findings of prophylactic salpingo-oophorectomies in 159 BRCA1 and BRCA2 carriers.Gynecol Oncol. 2006; 100: 58-64
- Autofluorescence imaging can identify preinvasive or clinically occult lesions in fallopian tube epithelium: a promising step towards screening and early detection.Gynecol Oncol. 2011; 120: 385-392
- Prophylactic salpingo-oophorectomy in a series of 89 women carrying a BRCA1 or a BRCA2 mutation.Cancer. 2007; 109: 1784-1790
- Effectiveness of risk-reducing salpingo-oophorectomy in preventing ovarian cancer in a high-risk French Canadian population.Int J Gynecol Cancer. 2012; 22: 974-978
- Risk reduction surgery (RRS) for tubo-ovarian cancer in an Irish gynaecological practice: an analysis of indications and outcomes.Ir J Med Sci. 2018; 187: 789-794
- Incidental carcinomas in prophylactic specimens in BRCA1 and BRCA2 germ-line mutation carriers, with emphasis on fallopian tube lesions: report of 6 cases and review of the literature.Am J Surg Pathol. 2006; 30: 1222-1230
- Assessing the risk of occult cancer and 30-day morbidity in women undergoing risk-reducing surgery: a prospective experience.J Minim Invasive Gynecol. 2017; 24: 837-842
- Clinical and pathological characteristics of incidental diagnostic early occult malignancy after risk-reducing salpingo-oophorectomy in BRCA mutation carriers.Int J Gynecol Cancer. 2016; 26: 233-239
- Clinical outcome of prophylactic oophorectomy in BRCA1/BRCA2 mutation carriers and events during follow-up.Br J Canc. 2004; 90: 1492-1497
- Tubal epithelial lesions in salpingo-oophorectomy specimens of BRCA-mutation carriers and controls.Gynecol Oncol. 2012; 127: 88-93
- Support of the 'fallopian tube hypothesis' in a prospective series of risk-reducing salpingo-oophorectomy specimens.Eur J Cancer. 2013; 49: 132-141
- Outcome and prognostic impact of surgical staging in serous tubal intraepithelial carcinoma: a cohort study and systematic review.Clin Oncol. 2018; 30: 463-471
- Uptake of risk-reducing salpingo-oophorectomy among female BRCA mutation carriers: experience at the National Cancer Center of Korea.J Cancer Res Clin Oncol. 2016; 142: 333-340
- Pathologic findings at risk-reducing salpingo-oophorectomy (RRSO) in germline BRCA mutation carriers with breast cancer: significance of bilateral RRSO at the optimal age in germline BRCA mutation carriers.J Gynecol Oncol. 2017; 28: e3
- Pathology findings and clinical outcomes after risk reduction salpingo-oophorectomy in BRCA mutation carriers: a multicenter Spanish study.Clin Transl Oncol. 2018; 20: 1337-1344
- Prophylactic salpingo-oophorectomy in 51 women with familial breast-ovarian cancer: importance of fallopian tube dysplasia.Int J Gynecol Cancer. 2006; 16: 183-188
- The first nationwide multicenter prevalence study of germline BRCA1 and BRCA2 mutations in Chinese ovarian cancer patients.Int J Gynecol Cancer. 2017; 27: 1650-1657
- BRCA1 and BRCA2 germline mutations in Korean ovarian cancer patients.J Cancer Res Clin Oncol. 2009; 135: 1593-1599
- BRCA1 and BRCA2 mutations in Japanese patients with ovarian, fallopian tube, and primary peritoneal cancer.Cancer. 2016; 122: 84-90
- Prevalence of BRCA1 mutations in familial and sporadic Greek ovarian cancer cases.PLoS One. 2013; 8e58182
- Hereditary ovarian cancer in Poland.Int J Cancer. 2003; 106: 942-945
- Comprehensive BRCA1 and BRCA2 mutational profile in Lithuania.Cancer Genet. 2014; 207: 195-205
- BRCA1 and BRCA2 mutations among 233 unselected Finnish ovarian carcinoma patients.Eur J Hum Genet. 2001; 9: 424-430
- Prevalence of founder BRCA1 and BRCA2 mutations among breast and ovarian cancer patients in Hungary.Int J Cancer. 2000; 86: 737-740
- BRCA1 and BRCA2 mutations account for a large proportion of ovarian carcinoma cases.Cancer. 2005; 104: 2807-2816
- Breast and ovarian cancer in relatives of cancer patients, with and without BRCA mutations.Cancer Epidemiol Biomark Prev. 2006; 15: 359-363
- Contribution of BRCA1 and BRCA2 mutations to breast and ovarian cancer in Pakistan.Am J Hum Genet. 2002; 71: 595-606
- Parity, oral contraceptives, and the risk of ovarian cancer among carriers and noncarriers of a BRCA1 or BRCA2 mutation.N Engl J Med. 2001; 345: 235-240
- Founder BRCA 1 and 2 mutations among a consecutive series of Ashkenazi Jewish ovarian cancer patients.Gynecol Oncol. 2000; 78: 148-151
- Clinicopathologic features of BRCA-linked and sporadic ovarian cancer.J Am Med Assoc. 2000; 283: 2260-2265
- Population BRCA1 and BRCA2 mutation frequencies and cancer penetrances: a kin-cohort study in Ontario, Canada.J Natl Cancer Inst. 2006; 98: 1694-1706
- BRCA1 and BRCA2 mutations among ovarian cancer patients from Colombia.Gynecol Oncol. 2012; 124: 236-243
- Frequencies of BRCA1 and BRCA2 mutations among 1,342 unselected patients with invasive ovarian cancer.Gynecol Oncol. 2011; 121: 353-357
- Founder BRCA1 and BRCA2 mutations in French Canadian ovarian cancer cases unselected for family history.Clin Genet. 1999; 55: 318-324
- A survey of willingness about genetic counseling and tests in patients of epithelial ovarian cancer.Zhonghua Yixue Zazhi. 2017; 97: 3412-3415
- Questionnaire survey on the attitude to genetic counseling and testing for gynecologic oncology by Chinese healthcare providers.J Reprod Med. 2018; 27: 49-54
- Germline BRCA1/2 mutation testing is indicated in every patient with epithelial ovarian cancer: a systematic review.Eur J Cancer. 2016; 61: 137-145
- Universal BRCA1/BRCA2 testing for ovarian cancer patients is welcomed, but with care: how women and staff contextualize experiences of expanded access.J Genet Couns. 2017; 26: 1280-1291
- Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: evidence for a causal relationship.Am J Surg Pathol. 2007; 31: 161-169
- Tumors of the fimbriated end of the fallopian tube: a clinicopathologic analysis of 20 cases, including nine carcinomas.Int J Gynecol Pathol. 1997; 16: 189-196
- BRCA-mutation-associated fallopian tube carcinoma: a distinct clinical phenotype?.Obstet Gynecol. 2005; 106: 1327-1334
- 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
- Fallopian tube intraluminal tumor spread from noninvasive precursor lesions: a novel metastatic route in early pelvic carcinogenesis.Am J Surg Pathol. 2013; 37: 1123-1130
- Clinical outcomes in patients with isolated serous tubal intraepithelial carcinoma (STIC): a comprehensive review.Gynecol Oncol. 2015; 139: 568-572
- European society of gynaecological oncology (ESGO) guidelines for ovarian cancer surgery.Int J Gynecol Cancer. 2017; 27: 1534-1542
- Development of peritoneal carcinoma in women diagnosed with serous tubal intraepithelial carcinoma (STIC) following risk-reducing salpingo-oophorectomy (RRSO).J Ovarian Res. 2019; 12: 50
- Impact of oophorectomy on cancer incidence and mortality in women with a BRCA1 or BRCA2 mutation.J Clin Oncol. 2014; 32: 1547-1553
- Pathologic findings at risk-reducing salpingo-oophorectomy: primary results from gynecologic oncology group trial GOG-0199.J Clin Oncol. 2014; 32: 3275-3283
- Occult ovarian cancers identified at risk-reducing salpingo-oophorectomy in a prospective cohort of BRCA1/2 mutation carriers.Breast Canc Res Treat. 2010; 124: 195-203
- BRCA1, TP53, and CHEK2 germline mutations in uterine serous carcinoma.Cancer. 2013; 119: 332-338
- Uterine cancer after risk-reducing salpingo-oophorectomy without hysterectomy in women with BRCA mutations.JAMA Oncol. 2016; 2: 1434-1440
- Breast cancer after use of estrogen plus progestin and estrogen alone: analyses of data from 2 women's health initiative randomized clinical trials.JAMA Oncol. 2015; 1: 296-305
- Screening for ovarian cancer: US preventive services task force recommendation statement.J Am Med Assoc. 2018; 319: 588-594
- Estimating cost-effectiveness of a multimodal ovarian cancer screening program in the United States: secondary analysis of the UK collaborative trial of ovarian cancer screening (UKCTOCS).JAMA Oncol. 2018; 4: 190-195
Article info
Publication history
Published online: September 05, 2019
Accepted:
September 4,
2019
Received in revised form:
August 23,
2019
Received:
May 10,
2019
Identification
Copyright
© 2019 Elsevier Ltd, BASO ~ The Association for Cancer Surgery, and the European Society of Surgical Oncology. All rights reserved.
