Abstract
The objective of this study was to identify factors that affect the decision to undergo risk-reducing salpingo-oophorectomy (RRSO) in BRCA1 or BRCA2 mutations carriers in South Korea. The medical records of 124 women who had been found to have BRCA1 or BRCA2 gene mutation at our institution between May 2003 and December 2011 were reviewed. The carriers were divided into RRSO and non-RRSO groups for comparison of their clinicopathologic, socio-economic, and psychosocial factors. Of the 71 carriers eligible for RRSO, 21 had undergone RRSO. In univariate analysis, classification of carriers into 3 groups by decade of life (4th, 5th, or 6th and later decade) and subsequent analysis revealed that 52.6 % of carriers in the 5th decade had undergone RRSO, a rate significantly higher than that of the other age groups (p = 0.007). The RRSO rate was higher in carriers with a personal history of breast cancer than in those without (39.2 % vs. 5.0 %, p = 0.004), in carriers with a family history of breast cancer than in those without (35.5 % vs. 11.8 %, p = 0.065), and in carriers with a family history of ovarian cancer than in those carriers without a family history (66.7 % vs. 24.2 %, p = 0.016). Multivariate analysis identified age and personal history of breast cancer as independent factors affecting the decision to undergo RRSO. Age and personal history of breast cancer are important factors in the decision to undergo, and should thus be considered when counseling BRCA1/2 mutation carriers.
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Antoniou A, Pharoah PD, Narod S, Risch HA, Eyfjord JE, Hopper JL, Loman N, Olsson H, Johannsson O, Borg A, Pasini B, Radice P, Manoukian S, Eccles DM, Tang N, Olah E, Anton-Culver H, Warner E, Lubinski J, Gronwald J, Gorski B, Tulinius H, Thorlacius S, Eerola H, Nevanlinna H, Syrjakoski K, Kallioniemi OP, Thompson D, Evans C, Peto J, Lalloo F, Evans DG, Easton DF (2003) 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 72(5):1117–1130. doi:10.1086/375033
Han SA, Park SK, Ahn S-H, Son BH, Lee MH, Choi DH, Noh D-Y, Han W, Lee ES, Han SK, Kim LS, Jung Y, Kim KS, Suh YJ, Moon B-I, Nam S-J, Noh W-C, Lee JE, Kim S-W (2009) The breast and ovarian cancer risks in Korea due to inherited mutations in BRCA1 and BRCA2: a preliminary report. J Breast Cancer 12(2):92. doi:10.4048/jbc.2009.12.2.92
Grann VR, Jacobson JS, Thomason D, Hershman D, Heitjan DF, Neugut AI (2002) Effect of prevention strategies on survival and quality-adjusted survival of women with BRCA1/2 mutations: an updated decision analysis. J Clin Oncol 20(10):2520–2529
Nelson HD, Huffman LH, Fu R, Harris EL (2005) Genetic risk assessment and BRCA mutation testing for breast and ovarian cancer susceptibility: systematic evidence review for the U.S. Preventive Services Task Force. Ann Intern Med 143(5):362–379
Stirling D, Evans DG, Pichert G, Shenton A, Kirk EN, Rimmer S, Steel CM, Lawson S, Busby-Earle RM, Walker J, Lalloo FI, Eccles DM, Lucassen AM, Porteous ME (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(24):5588–5596. doi:10.1200/JCO.2005.05.097
King MC, Wieand S, Hale K, Lee M, Walsh T, Owens K, Tait J, Ford L, Dunn BK, Costantino J, Wickerham L, Wolmark N, Fisher B (2001) Tamoxifen and breast cancer incidence among women with inherited mutations in BRCA1 and BRCA2: National Surgical Adjuvant Breast and Bowel Project (NSABP-P1) Breast Cancer Prevention Trial. JAMA 286(18):2251–2256
Narod SA, Dube MP, Klijn J, Lubinski J, Lynch HT, Ghadirian P, Provencher D, Heimdal K, Moller P, Robson M, Offit K, Isaacs C, Weber B, Friedman E, Gershoni-Baruch R, Rennert G, Pasini B, Wagner T, Daly M, Garber JE, Neuhausen SL, Ainsworth P, Olsson H, Evans G, Osborne M, Couch F, Foulkes WD, Warner E, Kim-Sing C, Olopade O, Tung N, Saal HM, Weitzel J, Merajver S, Gauthier-Villars M, Jernstrom H, Sun P, Brunet JS (2002) Oral contraceptives and the risk of breast cancer in BRCA1 and BRCA2 mutation carriers. J Natl Cancer Inst 94(23):1773–1779
Hartmann LC, Schaid DJ, Woods JE, Crotty TP, Myers JL, Arnold PG, Petty PM, Sellers TA, Johnson JL, McDonnell SK, Frost MH, Jenkins RB (1999) Efficacy of bilateral prophylactic mastectomy in women with a family history of breast cancer. New Engl J Med 340(2):77–84. doi:10.1056/NEJM199901143400201
Rebbeck TR, Lynch HT, Neuhausen SL, Narod SA, Van’t Veer L, Garber JE, Evans G, Isaacs C, Daly MB, Matloff E, Olopade OI, Weber BL, Prevention, Observation of Surgical End Points Study G (2002) Prophylactic oophorectomy in carriers of BRCA1 or BRCA2 mutations. New Engl J Med 346(21):1616–1622. doi:10.1056/NEJMoa012158
Rebbeck TR, Levin AM, Eisen A, Snyder C, Watson P, Cannon-Albright L, Isaacs C, Olopade O, Garber JE, Godwin AK, Daly MB, Narod SA, Neuhausen SL, Lynch HT, Weber BL (1999) Breast cancer risk after bilateral prophylactic oophorectomy in BRCA1 mutation carriers. J Natl Cancer Inst 91(17):1475–1479
Wainberg S, Husted J (2004) Utilization of screening and preventive surgery among unaffected carriers of a BRCA1 or BRCA2 gene mutation. Cancer Epidemiol Biomarkers Prev 13(12):1989–1995
Narod SA, Offit K (2005) Prevention and management of hereditary breast cancer. J Clin Oncol 23(8):1656–1663. doi:10.1200/JCO.2005.10.035
Beattie MS, Crawford B, Lin F, Vittinghoff E, Ziegler J (2009) Uptake, time course, and predictors of risk-reducing surgeries in BRCA carriers. Genet Test Mol Biomarkers 13(1):51–56. doi:10.1089/gtmb.2008.0067
Lerman C, Hughes C, Croyle RT, Main D, Durham C, Snyder C, Bonney A, Lynch JF, Narod SA, Lynch HT (2000) Prophylactic surgery decisions and surveillance practices one year following BRCA1/2 testing. Prev Med 31(1):75–80. doi:10.1006/pmed.2000.0684
Botkin JR, Smith KR, Croyle RT, Baty BJ, Wylie JE, Dutson D, Chan A, Hamann HA, Lerman C, McDonald J, Venne V, Ward JH, Lyon E (2003) Genetic testing for a BRCA1 mutation: prophylactic surgery and screening behavior in women 2 years post testing. Am J Med Genet A 118A(3):201–209. doi:10.1002/ajmg.a.10102
Kram V, Peretz T, Sagi M (2006) Acceptance of preventive surgeries by Israeli women who had undergone BRCA testing. Fam Cancer 5(4):327–335. doi:10.1007/s10689-006-0002-z
Burke W, Daly M, Garber J, Botkin J, Kahn MJ, Lynch P, McTiernan A, Offit K, Perlman J, Petersen G, Thomson E, Varricchio C (1997) Recommendations for follow-up care of individuals with an inherited predisposition to cancer. II. BRCA1 and BRCA2. Cancer Genetics Studies Consortium. JAMA 277(12):997–1003
Dowdy SC, Stefanek M, Hartmann LC (2004) Surgical risk reduction: prophylactic salpingo-oophorectomy and prophylactic mastectomy. Am J Obstet Gynecol 191(4):1113–1123. doi:10.1016/j.ajog.2004.04.028
Verheijen RH, Boonstra H, Menko FH, de Graaff J, Vasen HF, Kenter GG (2002) Recommendations for the management of women with an increased genetic risk of gynaecological cancer. Ned Tijdschr Geneeskd 146(50):2414–2418
Bradbury AR, Ibe CN, Dignam JJ, Cummings SA, Verp M, White MA, Artioli G, Dudlicek L, Olopade OI (2008) Uptake and timing of bilateral prophylactic salpingo-oophorectomy among BRCA1 and BRCA2 mutation carriers. Genet Med 10(3):161–166. doi:10.1097/GIM.0b013e318163487d
Skytte AB, Gerdes AM, Andersen MK, Sunde L, Brondum-Nielsen K, Waldstrom M, Kolvraa S, Cruger D (2010) Risk-reducing mastectomy and salpingo-oophorectomy in unaffected BRCA mutation carriers: uptake and timing. Clin Genet 77(4):342–349. doi:10.1111/j.1399-0004.2009.01329.x
Stuckey A, Dizon D, Scalia Wilbur J, Kent J, Tejada-Berges T, Gass J, Legare R (2010) Clinical characteristics and choices regarding risk-reducing surgery in BRCA mutation carriers. Gynecol Obstet Invest 69(4):270–273. doi:10.1159/000276573
Manchanda R, Burnell M, Abdelraheim A, Johnson M, Sharma A, Benjamin E, Brunell C, Saridogan E, Gessler S, Oram D, Side L, Rosenthal A, Jacobs I, Menon U (2012) Factors influencing uptake and timing of risk reducing salpingo-oophorectomy in women at risk of familial ovarian cancer: a competing risk time to event analysis. BJOG. doi:10.1111/j.1471-0528.2011.03257.x
Han SA, Kim SW, Kang E, Park SK, Ahn SH, Lee MH, Nam SJ, Han W, Bae YT, Kim HA, Cho YU, Chang MC, Paik NS, Hwang KT, Kim SJ, Noh DY, Choi DH, Noh WC, Kim LS, Kim KS, Suh YJ, Lee JE, Jung Y, Moon BI, Yang JH, Son BH, Yom CK, Kim SY, Lee H, Jung SH (2013) The prevalence of BRCA mutations among familial breast cancer patients in Korea: results of the Korean Hereditary Breast Cancer study. Fam Cancer 12(1):75–81. doi:10.1007/s10689-012-9578-7
Son BH, Ahn SH, Kim SW, Kang E, Park SK, Lee MH, Noh WC, Kim LS, Jung Y, Kim KS, Noh DY, Moon BI, Suh YJ, Lee JE, Choi DH, Kim SY, Jung SH, Yom CK, Lee H, Yang JH (2012) Prevalence of BRCA1 and BRCA2 mutations in non-familial breast cancer patients with high risks in Korea: The Korean Hereditary Breast Cancer (KOHBRA) Study. Breast Cancer Res Treat 133(3):1143–1152. doi:10.1007/s10549-012-2001-0
Madalinska JB, van Beurden M, Bleiker EM, Valdimarsdottir HB, Lubsen-Brandsma L, Massuger LF, Mourits MJ, Gaarenstroom KN, van Dorst EB, van der Putten H, Boonstra H, Aaronson NK (2007) Predictors of prophylactic bilateral salpingo-oophorectomy compared with gynecologic screening use in BRCA1/2 mutation carriers. J Clin Oncol 25(3):301–307. doi:10.1200/JCO.2006.07.4922
Kauff ND, Satagopan JM, Robson ME, Scheuer L, Hensley M, Hudis CA, Ellis NA, Boyd J, Borgen PI, Barakat RR, Norton L, Castiel M, Nafa K, Offit K (2002) Risk-reducing salpingo-oophorectomy in women with a BRCA1 or BRCA2 mutation. New Engl J Med 346(21):1609–1615. doi:10.1056/NEJMoa020119
Tiller K, Meiser B, Butow P, Clifton M, Thewes B, Friedlander M, Tucker K (2002) Psychological impact of prophylactic oophorectomy in women at increased risk of developing ovarian cancer: a prospective study. Gynecol Oncol 86(2):212–219
Watson M, Foster C, Eeles R, Eccles D, Ashley S, Davidson R, Mackay J, Morrison PJ, Hopwood P, Evans DG, Psychosocial Study C (2004) Psychosocial impact of breast/ovarian (BRCA1/2) cancer-predictive genetic testing in a UK multi-centre clinical cohort. Br J cancer 91(10):1787–1794. doi:10.1038/sj.bjc.6602207
Meijers-Heijboer EJ, Verhoog LC, Brekelmans CT, Seynaeve C, Tilanus-Linthorst MM, Wagner A, Dukel L, Devilee P, van den Ouweland AM, van Geel AN, Klijn JG (2000) Presymptomatic DNA testing and prophylactic surgery in families with a BRCA1 or BRCA2 mutation. Lancet 355(9220):2015–2020
Schwartz MD, Kaufman E, Peshkin BN, Isaacs C, Hughes C, DeMarco T, Finch C, Lerman C (2003) Bilateral prophylactic oophorectomy and ovarian cancer screening following BRCA1/BRCA2 mutation testing. J Clin Oncol 21(21):4034–4041. doi:10.1200/JCO.2003.01.088
Evans DG, Lalloo F, Ashcroft L, Shenton A, Clancy T, Baildam AD, Brain A, Hopwood P, Howell A (2009) Uptake of risk-reducing surgery in unaffected women at high risk of breast and ovarian cancer is risk, age, and time dependent. Cancer Epidemiol Biomarkers Prev 18(8):2318–2324. doi:10.1158/1055-9965.EPI-09-0171
Swisher EM, Babb S, Whelan A, Mutch DG, Rader JS (2001) Prophylactic oophorectomy and ovarian cancer surveillance. Patient perceptions and satisfaction. J Reprod Med 46(2):87–94
Uyei A, Peterson SK, Erlichman J, Broglio K, Yekell S, Schmeler K, Lu K, Meric-Bernstam F, Amos C, Strong L, Arun B (2006) Association between clinical characteristics and risk-reduction interventions in women who underwent BRCA1 and BRCA2 testing: a single-institution study. Cancer 107(12):2745–2751. doi:10.1002/cncr.22352
Metcalfe KA, Foulkes WD, Kim-Sing C, Ainsworth P, Rosen B, Armel S, Poll A, Eisen A, Gilchrist D, Chudley A, Ghadirian P, Maugard C, Lemire EG, Sun P, Narod SA (2008) Family history as a predictor of uptake of cancer preventive procedures by women with a BRCA1 or BRCA2 mutation. Clin Genet 73(5):474–479. doi:10.1111/j.1399-0004.2008.00988.x
Metcalfe KA, Birenbaum-Carmeli D, Lubinski J, Gronwald J, Lynch H, Moller P, Ghadirian P, Foulkes WD, Klijn J, Friedman E, Kim-Sing C, Ainsworth P, Rosen B, Domchek S, Wagner T, Tung N, Manoukian S, Couch F, Sun P, Narod SA (2008) International variation in rates of uptake of preventive options in BRCA1 and BRCA2 mutation carriers. Int J Cancer 122(9):2017–2022. doi:10.1002/ijc.23340
Scheuer L, Kauff N, Robson M, Kelly B, Barakat R, Satagopan J, Ellis N, Hensley M, Boyd J, Borgen P, Norton L, Offit K (2002) Outcome of preventive surgery and screening for breast and ovarian cancer in BRCA mutation carriers. J Clin Oncol 20(5):1260–1268
Schmeler KM, Sun CC, Bodurka DC, White KG, Soliman PT, Uyei AR, Erlichman JL, Arun BK, Daniels MS, Rimes SA, Peterson SK, Slomovitz BM, Milam MR, Gershenson DM, Lu KH (2006) Prophylactic bilateral salpingo-oophorectomy compared with surveillance in women with BRCA mutations. Obstet Gynecol 108(3 Pt 1):515–520. doi:10.1097/01.AOG.0000228959.30577.13
Madalinska JB, van Beurden M, Bleiker EM, Valdimarsdottir HB, Hollenstein J, Massuger LF, Gaarenstroom KN, Mourits MJ, Verheijen RH, van Dorst EB, van der Putten H, van der Velden K, Boonstra H, Aaronson NK (2006) The impact of hormone replacement therapy on menopausal symptoms in younger high-risk women after prophylactic salpingo-oophorectomy. J Clin Oncol 24(22):3576–3582. doi:10.1200/JCO.2005.05.1896
Metcalfe KA, Narod SA (2007) Breast cancer prevention in women with a BRCA1 or BRCA2 mutation. Open Med 1(3):e184–e190
Fang CY, Cherry C, Devarajan K, Li T, Malick J, Daly MB (2009) A prospective study of quality of life among women undergoing risk-reducing salpingo-oophorectomy versus gynecologic screening for ovarian cancer. Gynecol Oncol 112(3):594–600. doi:10.1016/j.ygyno.2008.11.039
Madalinska JB, Hollenstein J, Bleiker E, van Beurden M, Valdimarsdottir HB, Massuger LF, Gaarenstroom KN, Mourits MJ, Verheijen RH, van Dorst EB, van der Putten H, van der Velden K, Boonstra H, Aaronson NK (2005) Quality-of-life effects of prophylactic salpingo-oophorectomy versus gynecologic screening among women at increased risk of hereditary ovarian cancer. J Clin Oncol 23(28):6890–6898. doi:10.1200/JCO.2005.02.626
Miller SM, Roussi P, Daly MB, Buzaglo JS, Sherman K, Godwin AK, Balshem A, Atchison ME (2005) Enhanced counseling for women undergoing BRCA1/2 testing: impact on subsequent decision making about risk reduction behaviors. Health Educ Behav 32(5):654–667. doi:10.1177/1090198105278758
Hallowell N, Mackay J, Richards M, Gore M, Jacobs I (2004) High-risk premenopausal women’s experiences of undergoing prophylactic oophorectomy: a descriptive study. Genet Test 8(2):148–156. doi:10.1089/1090657041797202
Lobb EA, Butow PN, Barratt A, Meiser B, Gaff C, Young MA, Haan E, Suthers G, Gattas M, Tucker K (2004) Communication and information-giving in high-risk breast cancer consultations: influence on patient outcomes. Br J Cancer 90(2):321–327. doi:10.1038/sj.bjc.6601502
Kang E (2010) The KOHBRA Study has changed the practice patterns for managing Hereditary Breast Cancer in Korea. J Breast Cancer 13, December edn. doi:10.4048/jbc.2010.13.4.351
Meijers-Heijboer H, Brekelmans CT, Menke-Pluymers M, Seynaeve C, Baalbergen A, Burger C, Crepin E, van den Ouweland AW, van Geel B, Klijn JG (2003) Use of genetic testing and prophylactic mastectomy and oophorectomy in women with breast or ovarian cancer from families with a BRCA1 or BRCA2 mutation. J Clin Oncol 21(9):1675–1681. doi:10.1200/JCO.2003.09.052
Manchanda R, Burnell M, Abdelraheim A, Johnson M, Sharma A, Benjamin E, Brunell C, Saridogan E, Gessler S, Oram D, Side L, Rosenthal A, Jacobs I, Menon U (2012) Factors influencing uptake and timing of risk reducing salpingo-oophorectomy in women at risk of familial ovarian cancer: a competing risk time to event analysis. BJOG 119(5):527–536. doi:10.1111/j.1471-0528.2011.03257.x
Dignam JJ, Kocherginsky MN (2008) Choice and interpretation of statistical tests used when competing risks are present. J Clin Oncol 26(24):4027–4034. doi:10.1200/JCO.2007.12.9866
Manchanda R, Abdelraheim A, Johnson M, Rosenthal AN, Benjamin E, Brunell C, Burnell M, Side L, Gessler S, Saridogan E, Oram D, Jacobs I, Menon U (2011) Outcome of risk-reducing salpingo-oophorectomy in BRCA carriers and women of unknown mutation status. BJOG 118(7):814–824. doi:10.1111/j.1471-0528.2011.02920.x
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This study was supported by a grant from the National R&D Program for Cancer Control, Ministry for Health, Welfare and Family Affairs, Republic of Korea (1020350).
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Kim, D., Kang, E., Hwang, E. et al. Factors affecting the decision to undergo risk-reducing salpingo-oophorectomy among women with BRCA gene mutation. Familial Cancer 12, 621–628 (2013). https://doi.org/10.1007/s10689-013-9625-z
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DOI: https://doi.org/10.1007/s10689-013-9625-z