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Clinical and pathological outcomes of risk-reducing salpingo-oophorectomy for Japanese women with hereditary breast and ovarian cancer

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Abstract

Background

To clarify the clinical as well as pathological outcomes in Japanese women with germline pathogenic BRCA1/2 variants who underwent risk-reducing salpingo-oophorectomy (RRSO).

Methods

This prospective study examined the rate of occult cancer and primary peritoneal cancer after RRSO at our institution in the period from 2011 to 2020. Clinical records of genetically confirmed patients with germline pathogenic BRCA1/2 variants who desired to undergo RRSO were reviewed. Specimens obtained during RRSO were pathologically diagnosed as per SEE-FIM protocol. All the participants underwent magnetic resonance imaging (MRI) about 1 month preoperatively.

Results

One hundred and seventeen women underwent RRSO during this period. Of these, the numbers of women with germline pathogenic BRCA1 and BRCA2 variants were 72 and 45, respectively. The mean observational time after RRSO was 35.8 months. Despite negative preoperative screening results, three (2.6%) serous tubal intraepithelial carcinoma and three (2.6%) invasive carcinomas were identified. Of the three invasive carcinomas cases, two were International Federation of Gynecology and Obstetrics (FIGO) stage I primary fallopian tube cancer, and the third case was double cancer (ovarian cancer and fallopian tube cancer) with FIGO stage IC3.

Conclusions

The rate of occult neoplasms was similar to those reported by studies performed in other countries. Although women with occult cancer were diagnosed with FIGO stage I, the MRI performed 1 month preoperatively did not show any such malignant findings. Thus, RRSO is the only promising method that can improve the prognosis in women with germline pathogenic BRCA1/2 variants.

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References

  1. Chen S, Parmigiani G (2007) Meta-analysis of BRCA1 and BRCA2 penetrance. J Clin Oncol 25:1329–1333

    Article  Google Scholar 

  2. Chen J, Bae E, Zhang L et al (2020) Penetrance of breast and ovarian cancer in women who carry a BRCA1/2 mutation and do not use risk-reducing salpingo-oophorectomy: an updated meta-analysis. JNCI Cancer Spectr. https://doi.org/10.1093/jncics/pkaa029

    Article  PubMed  PubMed Central  Google Scholar 

  3. Alsop K, Fereday S, Meldrum C et al (2012) BRCA mutation frequency and patterns of treatment response in BRCA mutation-positive women with ovarian cancer: a report from the Australian Ovarian Cancer Study Group. J Clin Oncol 30:2654–2663

    Article  CAS  Google Scholar 

  4. Enomoto T, Aoki D, Hattori K et al (2019) The first Japanese nationwide multicenter study of BRCA mutation testing in ovarian cancer: CHARacterizing the cross-sectionaL approach to Ovarian cancer genetic Testing of BRCA (CHARLOTTE). Int J Gynecol Cancer 29:1043–1049

    Article  Google Scholar 

  5. McLaughlin JR, Rosen B, Moody J et al (2013) Long-term ovarian cancer survival associated with mutation in BRCA1 or BRCA2. J Natl Cancer Inst 105:141–148

    Article  CAS  Google Scholar 

  6. Biglia N, Sgandurra P, Bounous VE et al (2016) Ovarian cancer in BRCA1 and BRCA2 gene mutation carriers: analysis of prognostic factors and survival. Ecancermedicalscience 10:639. https://doi.org/10.3332/ecancer.2016.639.eCollection2016

    Article  PubMed  PubMed Central  Google Scholar 

  7. Kim SI, Lee M, Kim HS et al (2019) Effect of BRCA mutational status on survival outcome in advanced-stage high-grade serous ovarian cancer. J Ovarian Res 12:40. https://doi.org/10.1186/s13048-019-0511-7

    Article  PubMed  PubMed Central  Google Scholar 

  8. Kotsopoulos J, Rosen B, Fan I et al (2016) Ten-year survival after epithelial ovarian cancer is not associated with BRCA mutation status. Gynecol Oncol 140:42–47

    Article  CAS  Google Scholar 

  9. Olivier RI, Lubsen-Brandsma MA, Verhoef S et al (2006) CA125 and transvaginal ultrasound monitoring in high-risk women cannot prevent the diagnosis of advanced ovarian cancer. Gynecol Oncol 100:20–26

    Article  CAS  Google Scholar 

  10. Stirling D, Evans DG, Pichert G et al (2005) Screening for familial ovarian cancer: failure of current protocols to detect ovarian cancer at an early stage according to the international federation of gynecology and obstetrics system. J Clin Oncol 23:5586–5596

    Article  Google Scholar 

  11. van Nagell JR Jr, Miller RW, DeSimone CP et al (2011) Long-term survival of women with epithelial ovarian cancer detected by ultrasonographic screening. Obstet Gynecol 118:1212–1221

    Article  Google Scholar 

  12. Domchek SM, Friebel TM, Singer CF et al (2010) Association of risk-reducing surgery in BRCA1 or BRCA2 mutation carriers with cancer risk and mortality. JAMA 304:967–975

    Article  CAS  Google Scholar 

  13. Rebbeck TR, Kauff ND, Domchek SM (2009) Meta-analysis of risk reduction estimates associated with risk-reducing salpingo-oophorectomy in BRCA1 or BRCA2 mutation carriers. J Natl Cancer Inst 21:80–87

    Article  Google Scholar 

  14. Finch AP, Lubinski J, Moller P et al (2014) Impact of oophorectomy on cancer incidence and mortality in women with a BRCA1 or BRCA2 mutation. J Clin Oncol 32:1547–1553

    Article  Google Scholar 

  15. Lee Y, Medeiros F, Kindelberger D et al (2006) Advances in the recognition of tubal intraepithelial carcinoma: applications to cancer screening and the pathogenesis of ovarian cancer. Adv Anat Pathol 13:1–7

    Article  Google Scholar 

  16. Nomura H, Sekine M, Yokoyama S et al (2019) Clinical background and outcomes of risk-reducing salpingo-oophorectomy fir hereditary breast and ovarian cancers in Japan. Int J Clin Oncol 24:1105–1110

    Article  Google Scholar 

  17. National Comprehensive Cancer Network (NCCN) clinical practice guidelines in oncology. Geneic/Familyial High-Risk Assessment: Breast, Ovarian, and Pancreatic. Version 1.2022. https://www.nccn.org/professionals/physician_gls/pdf/genetics_bop.pdf. Accessed 11 Jan 2021

  18. Garcia C, Wendt J, Lyon L et al (2014) Risk management options elected by women after testing positive for a BRCA mutation. Gynecol Oncol 32:428–433

    Article  Google Scholar 

  19. Lee YJ, Lee SW, Kim KR et al (2017) 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 28:e3. https://doi.org/10.3802/jgo.2017.28.e3

    Article  PubMed  Google Scholar 

  20. Shigehiro M, Kita M, Takeuchi S et al (2016) Study on the psychosocial aspects of risk-reducing salpingo-oophorectomy (RRSO) in BRCA1/2 mutation carriers in Japan: a preliminary report. Jpn J Clin Oncol 46:254–259

    Article  Google Scholar 

  21. Kobayashi Y, Hirasawa A, Chiyoda T et al (2021) Retrospective evaluation of risk-reducing salpingo-oophorectomy for BRCA1/2 pathogenic variant carriers among a cohort study in a single institution. Jpn J Clin Oncol 51:213–217

    Article  Google Scholar 

  22. Arai M, Yokoyama S, Watanabe C et al (2018) Genetic and clinical characteristics in Japanese hereditary breast and ovarian cancer: first report after establishment of HBOC registration system in Japan. J Hum Genet 64:447–457

    Article  Google Scholar 

  23. Sherman ME, Piedmonte M, Mai PL et al (2014) Pathologic findings at risk-reducing salpingo-oophorectomy: primary results from gynecologic oncology group trial GOG-0199. J Clin Oncol 32:3275–3283

    Article  Google Scholar 

  24. Powel CB, Chen LM, McLennan J et al (2011) 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 21:846–851

    Article  Google Scholar 

  25. Shu CA, Pike MC, Jotwani AR et al (2016) Uterine cancer after risk-reducing salpingo-oophorectomy without hysterectomy in women with BRCA mutations. JAMA Oncol 2:1134–1140

    Article  Google Scholar 

  26. Laitman Y, Michaelson-Cohen R, Levi E et al (2019) Uterine cancer in Jewish Israeli BRCA1/2 mutation carriers. Cancer 125:698–703

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Dr, Masami Arai, Dr. Reiko Yoshida, Keika Kaneko, Hiromi Arakawa, Eri Habano, Mizuho Kita and Yuumi Ashihara for their cooperation for this study.

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Authors and Affiliations

  1. Department of Gynecology, Cancer Institute Hospital, Japanese Foundation for Cancer Research, Ariake 3-8-31, Koto City, Tokyo, 135-8550, Japan

    Hidetaka Nomura, Ai Ikki, Atsushi Fusegi, Makiko Omi, Yoichi Aoki, Sachiho Netsu, Terumi Tanigawa, Maki Matoda, Sanshiro Okamoto, Kohei Omatsu & Hiroyuki Kanao

  2. Department of Clinical Genetics, Cancer Institute Hospital, Japanese Foundation for Cancer Research, Ariake 3-8-31, Koto City, Tokyo, Japan

    Takeshi Nakajima & Arisa Ueki

  3. Division of Pathology, Cancer Institute, Japanese Foundation for Cancer Research, Ariake 3-8-31, Koto City, Tokyo, Japan

    Akiko Tonooka

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  1. Hidetaka Nomura
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  2. Ai Ikki
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Correspondence to Hidetaka Nomura.

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Nomura, H., Ikki, A., Fusegi, A. et al. Clinical and pathological outcomes of risk-reducing salpingo-oophorectomy for Japanese women with hereditary breast and ovarian cancer. Int J Clin Oncol 26, 2331–2337 (2021). https://doi.org/10.1007/s10147-021-02020-9

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  • DOI: https://doi.org/10.1007/s10147-021-02020-9

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