Risk-reducing surgery in hereditary gynecological cancer: Clinical applications in Lynch syndrome and hereditary breast and ovarian cancer (Review)

Adachi,Masataka; Banno,Kouji; Yanokura,Megumi; Iida,Miho; Nakamura,Kanako; Nogami,Yuya; Umene,Kiyoko; Masuda,Kenta; Kisu,Iori; Ueki,Arisa; Hirasawa,Akira; Tominaga,Eiichiro; Aoki,Daisuke

doi:10.3892/mco.2014.460

Risk-reducing surgery in hereditary gynecological cancer: Clinical applications in Lynch syndrome and hereditary breast and ovarian cancer (Review)

Authors:
- Masataka Adachi
- Kouji Banno
- Megumi Yanokura
- Miho Iida
- Kanako Nakamura
- Yuya Nogami
- Kiyoko Umene
- Kenta Masuda
- Iori Kisu
- Arisa Ueki
- Akira Hirasawa
- Eiichiro Tominaga
- Daisuke Aoki
View Affiliations

Affiliations: Department of Obstetrics and Gynecology, School of Medicine, Keio University, Tokyo 160‑8582, Japan
Published online on: November 20, 2014 https://doi.org/10.3892/mco.2014.460
Pages: 267-273

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Risk‑reducing surgery (RRS) is defined as a prophylactic approach with removal of organs at high risk of developing cancer, which is performed in cases without lesions or absence of clinically significant lesions. Hereditary gynecological cancers for which RRS is performed include hereditary breast and ovarian cancer (HBOC) and Lynch syndrome. For HBOC, RRS in the United States (US) is recommended for women with mutations in the breast cancer susceptibility (BRCA)1 and BRCA2 genes and bilateral salpingo‑oophorectomy (BSO) is generally performed. This procedure may reduce the risk of breast, ovarian, Fallopian tube and primary peritoneal cancer, although ovarian deficiency symptoms occur postoperatively. For Lynch syndrome, RRS in the US is considered for postmenopausal women or for women who do not desire to bear children and BSO and hysterectomy are usually performed. This approach may reduce the risk of endometrial and ovarian cancer, although ovarian deficiency symptoms also occur. For RRS, there are several issues that must be addressed to reduce the risk of cancer development in patients with HBOC or Lynch syndrome. To the best of our knowledge, this is the first review to discuss RRS with a focus on hereditary gynecological cancer.

View Figures

View References

1	Rubin SC, Blackwood MA, Bandera C, et al: BRCA 1, BRCA 2, and hereditary nonpolyposis colorectal cancer gene mutations in an unselected ovarian cancer population: relationship to family history and implications for genetic testing. Am J Obstet Gynecol. 178:670–677. 1998. View Article : Google Scholar : PubMed/NCBI
2	Struewing JP, Hartge P, Wacholder S, et al: The risk of cancer associated with specific mutations of BRCA1 and BRCA2 among Ashkenazi Jews. N Engl J Med. 336:1401–1408. 1997. View Article : Google Scholar : PubMed/NCBI
3	Boyd J, Sonoda Y, Federici MG, et al: Clinicopathologic features of BRCA-linked and sporadic ovarian cancer. JAMA. 283:2260–2265. 2000. View Article : Google Scholar : PubMed/NCBI
4	Werness BA, Ramus SJ, DiCioccio RA, et al: Histopathology, FIGO stage, and BRCA mutation status of ovarian cancers from the Gilda Radner Familial Ovarian Cancer Registry. Int J Gynecol Pathol. 23:29–34. 2004. View Article : Google Scholar : PubMed/NCBI
5	Pal T, Permuth-Wey J, Betts JA, et al: BRCA1 and BRCA2 mutations account for a large proportion of ovarian carcinoma cases. Cancer. 104:2807–2816. 2005. View Article : Google Scholar : PubMed/NCBI
6	Peltomaki P and Vasen H: Mutations associated with HNPCC predisposition - Update of ICG-HNPCC/INSiGHT mutation database. Dis Markers. 20:269–276. 2004. View Article : Google Scholar : PubMed/NCBI
7	Banno K, Yanokura M, Kobayashi Y, et al: Endometrial cancer as a familial tumor: pathology and molecular carcinogenesis (review). Curr Genomics. 10:127–132. 2009. View Article : Google Scholar : PubMed/NCBI
8	Hirata K, Kanemitsu S, Nakayama Y, et al: A novel germline mutation of MSH2 in a hereditary nonpolyposis colorectal cancer patient with liposarcoma. Am J Gastroenterol. 101:193–196. 2006. View Article : Google Scholar : PubMed/NCBI
9	Banno K, Kisu I, Yanokura M, et al: Epimutation and cancer: A new carcinogenic mechanism of Lynch syndrome (Review). Int J Oncol. 41:793–797. 2012.PubMed/NCBI
10	Aarnio M, Sankila R, Pukkala E, et al: Cancer risk in mutation carriers of DNA-mismatch-repair genes. Int J Cancer. 81:214–218. 1999. View Article : Google Scholar : PubMed/NCBI
11	Dunlop MG, Farrington SM, Carothers AD, et al: Cancer risk associated with germline DNA mismatch repair gene mutations. Hum Mol Genet. 6:105–110. 1997. View Article : Google Scholar : PubMed/NCBI
12	Broaddus RR, Lynch HT, Chen LM, et al: Pathologic features of endometrial carcinoma associated with HNPCC: a comparison with sporadic endometrial carcinoma. Cancer. 106:87–94. 2006. View Article : Google Scholar : PubMed/NCBI
13	Watson P, Butzow R, Lynch HT, et al: The clinical features of ovarian cancer in hereditary nonpolyposis colorectal cancer. Gynecol Oncol. 82:223–228. 2001. View Article : Google Scholar : PubMed/NCBI
14	National Comprehensive Cancer Network (NCCN) Clinical Practice Guidelines in Oncology, . Genetic/familial high-risk assesment: breast and ovarian. http://www.nccn.org/professionals/physician_gls/pdf/genetics_screening.pdfAccessed. January 2–2014
15	Ford D, Easton DF, 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. 62:676–689. 1998. View Article : Google Scholar
16	King MC, Marks JH and Mandell JBNew York Breast Cancer Study Group: Breast and ovarian cancer risks due to inherited mutations in BRCA1 and BRCA2. Science. 302:643–646. 2003. View Article : Google Scholar : PubMed/NCBI
17	Finch AP, Lubinski J, Moller P, et al: Impact of oophorectomy on cancer incidence and mortality in women with a BRCA1 or BRCA2 mutation. J Clin Oncol. Feb 24–2014.(Epub ahead of print). View Article : Google Scholar : PubMed/NCBI
18	Kauff ND, Mitra N, Robson ME, et al: Risk of ovarian cancer in BRCA1 and BRCA2 mutation-negative hereditary breast cancer families. J Natl Cancer Inst. 97:1382–1384. 2005. View Article : Google Scholar : PubMed/NCBI
19	National Comprehensive Cancer Network (NCCN) Clinical Practice Guidelines in Oncology, . Colorectal cancer screening. http://www.nccn.org/professionals/physician_gls/pdf/colorectal_screening.pdfAccessed. October 2–2014
20	Schmeler KM, Lynch HT, Chen LM, et al: Prophylactic surgery to reduce the risk of gynecologic cancers in the Lynch syndrome. N Engl J Med. 354:261–269. 2006. View Article : Google Scholar
21	Meyer LA, Broaddus RR and Lu KH: Endometrial cancer and Lynch syndrome: clinical and pathologic considerations. Cancer Control. 16:14–22. 2009.PubMed/NCBI
22	Offit K and Kauff ND: Reducing the risk of gynecologic cancer in the Lynch syndrome. N Engl J Med. 354:293–295. 2006. View Article : Google Scholar : PubMed/NCBI
23	Kehoe SM and Kauff ND: Screening and prevention of hereditary gynecologic cancers. Semin Oncol. 34:406–410. 2007. View Article : Google Scholar : PubMed/NCBI
24	Hirasawa A, Masuda K, Akahane T, et al: Experience of risk-reducing salpingo-oophorectomy for BRCA1 mutation carrier and establishment of a system performing a preventive surgery for hereditary breast and ovarian cancer syndrome in Japan: Our challenges for the future. Jpn J Clin Oncol. 43:515–519. 2013. View Article : Google Scholar : PubMed/NCBI
25	Kenkhuis MJ, de Bock GH, Elferink PO, et al: Short-term surgical outcome and safety of risk-reducing salpingo-oophorectomy in BRCA1/2 mutation carriers. Maturitas. 66:310–314. 2010. View Article : Google Scholar : PubMed/NCBI
26	Escobar PF, Starks DC, Fader AN, Barber M and Rojas-Espalliat L: Single-port risk-reducing salpingo-oophorectomy with and without hysterectomy: surgical outcomes and learning curve analysis. Gynecol Oncol. 119:43–47. 2010. View Article : Google Scholar : PubMed/NCBI
27	Finch A, Shaw P, Rosen B, Murphy J, Narod SA and Colgan TJ: Clinical and pathologic findings of prophylactic salpingo-oophorectomies in 159 BRCA1 and BRCA2 carriers. Gynecol Oncol. 100:58–64. 2006. View Article : Google Scholar : PubMed/NCBI
28	Kauff ND, Satagopan JM, Robson ME, et al: Risk-reducing salpingo-oophorectomy in women with a BRCA1 or BRCA2mutation. N Engl J Med. 346:1609–1615. 2002. View Article : Google Scholar : PubMed/NCBI
29	Lavie O, Hornreich G, Ben-Arie A, et al: BRCA germline mutations in Jewish women with uterine serous papillary carcinoma. Gynecol Oncol. 92:521–524. 2004. View Article : Google Scholar : PubMed/NCBI
30	Beiner ME, Finch A, Rosen B, et al: The risk of endometrial cancer in women with BRCA1 and BRCA2 mutations. A prospective study. Gynecol Oncol. 104:7–10. 2007. View Article : Google Scholar : PubMed/NCBI
31	Villella JA, Parmar M, Donohue K, Fahey C, Piver MS and Rodabaugh K: Role of prophylactic hysterectomy in patients at high risk for hereditary cancers. Gynecol Oncol. 102:475–479. 2006. View Article : Google Scholar : PubMed/NCBI
32	Lu KH and Broaddus RR: Gynecologic cancers in Lynch syndrome/HNPCC. Fam Cancer. 4:249–254. 2005. View Article : Google Scholar : PubMed/NCBI
33	Nieboer TE, Johnson N, Lethaby A, et al: Surgical approach to hysterectomy for benign gynaecological disease. Cochrane Database Syst Rev. (3):CD0036772009.PubMed/NCBI
34	Lu KH, Dinh M, Kohlmann W, et al: Gynecologic cancer as a ‘sentinel cancer’ for women with hereditary nonpolyposis colorectal cancer syndrome. Obstet Gynecol. 105:569–574. 2005. View Article : Google Scholar : PubMed/NCBI
35	Rebbeck TR, Kauff ND and Domchek SM: Meta-analysis of risk reduction estimates associated with risk-reducing salpingo-oophorectomy in BRCA1 or BRCA2 mutation carriers. J Natl Cancer Inst. 101:80–87. 2009. View Article : Google Scholar : PubMed/NCBI
36	Domchek SM, Friebel TM, Singer CF, et al: Association of risk-reducing surgery in BRCA1 or BRCA2 mutation carriers with cancer risk and mortality. JAMA. 304:967–975. 2010. View Article : Google Scholar : PubMed/NCBI
37	Chen LM, Yang KY, Little SE, Cheung MK and Caughey AB: Gynecologic cancer prevention in Lynch syndrome/hereditary nonpolyposis colorectal cancer families. Obstet Gynecol. 110:18–25. 2007. View Article : Google Scholar : PubMed/NCBI
38	Chapman JS, Powell CB, McLennan J, et al: Surveillance of survivors: follow-up after risk-reducing salpingo-oophorectomy in BRCA 1/2 mutation carriers. Gynecol Oncol. 122:339–343. 2011. View Article : Google Scholar : PubMed/NCBI
39	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. 296:185–192. 2006. View Article : Google Scholar : PubMed/NCBI
40	Lindor NM, Petersen GM, Hadley DW, et al: Recommendations for the care of individuals with an inherited predisposition to Lynch syndrome: a systematic review. JAMA. 296:1507–1517. 2006. View Article : Google Scholar : PubMed/NCBI
41	Schmeler KM, Daniels MS, Soliman PT, et al: Primary peritoneal cancer after bilateral salpingo-oophorectomy in two patients with Lynch syndrome. Obstet Gynecol. 115:432–434. 2010. View Article : Google Scholar : PubMed/NCBI
42	Anderson GL, Limacher M, Assaf AR, et al Women's Health Initiative Steering Committee: Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women's Health Initiative randomized controlled trial. JAMA. 291:1701–1712. 2004. View Article : Google Scholar : PubMed/NCBI
43	Kauff ND and Barakat RR: Risk-reducing salpingo-oophorectomy in patients with germline mutations in BRCA1 or BRCA2. J Clin Oncol. 25:2921–2927. 2007. View Article : Google Scholar : PubMed/NCBI
44	Grady D, Gebretsadik T, Kerlikowske K, Ernster V and Petitti D: Hormone replacement therapy and endometrial cancer risk: a meta-analysis. Obstet Gynecol. 85:304–313. 1995. View Article : Google Scholar : PubMed/NCBI
45	Barakat RR, Bundy BN, Spirtos NM, Bell J and Mannel RSGynecologic Oncology Group Study: Randomized double-blind trial of estrogen replacement therapy versus placebo in stage I or II endometrial cancer: a Gynecologic Oncology Group Study. J Clin Oncol. 24:587–592. 2006. View Article : Google Scholar : PubMed/NCBI
46	Beral V, Bull D and Reeves GMillion Women Study Collaborators: Endometrial cancer and hormone-replacement therapy in the Million Women Study. Lancet. 365:1543–1551. 2005. View Article : Google Scholar : PubMed/NCBI
47	Voigt LF, Weiss NS, Chu J, Daling JR, McKnight B and van Belle G: Progestagen supplementation of exogenous oestrogens and risk of endometrial cancer. Lancet. 338:274–277. 1991. View Article : Google Scholar : PubMed/NCBI
48	Chlebowski RT, Anderson GL, Gass M, et al: Estrogen plus progestin and breast cancer incidence and mortality in postmenopausal women. JAMA. 304:1684–1692. 2010. View Article : Google Scholar : PubMed/NCBI
49	Eden JA: Why does oestrogen-only hormone therapy have such a small impact on breast cancer risk? A hypothesis. Gynecol Endocrinol. 27:170–175. 2011. View Article : Google Scholar : PubMed/NCBI
50	Rebbeck TR, Friebel T, Wagner T, et al PROSE Study Group: Effect of short-term hormone replacement therapy on breast cancer risk reduction after bilateral prophylactic oophorectomy in BRCA1 and BRCA2mutation carriers: the PROSE Study Group. J Clin Oncol. 23:7804–7810. 2005. View Article : Google Scholar : PubMed/NCBI
51	Eisen A, Lubinski J, Gronwald J, et al: Hormone therapy and the risk of breast cancer in BRCA1 mutation carriers. J Natl Cancer Inst. 100:1361–1367. 2008. View Article : Google Scholar : PubMed/NCBI
52	Win AK, Young JP, Lindor NM, et al: Colorectal and other cancer risks for carriers and noncarriers from families with a DNA mismatch repair gene mutation: a prospective cohort study. J Clin Oncol. 30:958–964. 2012. View Article : Google Scholar : PubMed/NCBI
53	Sestak I and Cuzick J: Preventive therapy for breast cancer. Curr Oncol Rep. 14:568–573. 2012. View Article : Google Scholar : PubMed/NCBI
54	Pickar JH, Yeh IT, Bachmann G and Speroff L: Endometrial effects of a tissue selective estrogen complex containing bazedoxifene/conjugated estrogens as a menopausal therapy. Fertil Steril. 92:1018–1024. 2009. View Article : Google Scholar : PubMed/NCBI
55	Nelson HD, Vesco KK, Haney E, et al: Nonhormonal therapies for menopausal hot flashes: systematic review and meta-analysis. JAMA. 295:2057–2071. 2006. View Article : Google Scholar : PubMed/NCBI
56	Pearce CL, Chung K, Pike MC and Wu AH: Increased ovarian cancer risk associated with menopausal estrogen therapy is reduced by adding a progestin. Cancer. 115:531–539. 2009. View Article : Google Scholar : PubMed/NCBI
57	Lacey JV Jr, Brinton LA, Leitzmann MF, et al: Menopausal hormone therapy and ovarian cancer risk in the National Institutes of Health-AARP Diet and Health Study Cohort. J Natl Cancer Inst. 98:1397–1405. 2006. View Article : Google Scholar : PubMed/NCBI
58	Hildebrand JS, Gapstur SM, Feigelson HS, Teras LR, Thun MJ and Patel AV: Postmenopausal hormone use and incident ovarian cancer: Associations differ by regimen. Int J Cancer. 127:2928–2935. 2010. View Article : Google Scholar : PubMed/NCBI
59	Miller SM, Roussi P, Daly MB and Scarpato J: New strategies in ovarian cancer: uptake and experience of women at high risk of ovarian cancer who are considering risk-reducing salpingo-oophorectomy. Clin Cancer Res. 16:5094–5106. 2010. View Article : Google Scholar : PubMed/NCBI
60	Kuerer HM, Hwang ES, Anthony JP, et al: Current national health insurance coverage policies for breast and ovarian cancer prophylactic surgery. Ann Surg Oncol. 7:325–332. 2000. View Article : Google Scholar : PubMed/NCBI
61	Anderson K, Jacobson JS, Heitjan DF, et al: Cost-effectiveness of preventive strategies for women with a BRCA1 or a BRCA2mutation. Ann Intern Med. 144:397–406. 2006. View Article : Google Scholar : PubMed/NCBI
62	Yurgelun MB, Mercado R, Rosenblatt M, et al: Impact of genetic testing on endometrial cancer risk-reducing practices in women at risk for Lynch syndrome. Gynecol Oncol. 127:544–551. 2012. View Article : Google Scholar : PubMed/NCBI
63	Ichikawa Y, Hirai Y, Hasumi K and Utsunomiya J: Prophylactic salpingo-oophorectomy in a woman with high-risk for ovarian carcinoma: A case report. Kanto J Obstet Gynecol. 42:9–14. 2005.(In Japanese).
64	Arai M, Iwase H, Nishimura S, Iwase T and Takizawa K: Risk-reducing surgery for patients with hereditary breast and ovarian cancer. Jpn Soc Fam Tumors. 12:A272012.(In Japanese).
65	Nakamura K, Hirasawa A, Akahane T, et al: A case of Lynch syndrome intervened early after genetic testing. Tokyo J Obstet Gynecol. 60:293–297. 2011.(In Japanese).
66	Kwong A, Wong CH, Shea C, Suen DT and Choi CL: Choice of management of southern Chinese BRCA mutation carriers. World J Surg. 34:1416–1426. 2010. View Article : Google Scholar : PubMed/NCBI
67	Kim D, Kang E, Hwang E, et al: Factors affecting the decision to undergo risk-reducing salpingo-oophorectomy among women with BRCA gene mutation. Fam Cancer. 12:621–628. 2013. View Article : Google Scholar : PubMed/NCBI