Cited by 62BRCA gene mutations in cancerMenopause: Health Impacts and TreatmentsBreast Cancer Treatment Studies

Impact of risk-reducing salpingo-oophorectomy in premenopausal women

Open access
Vermeulen, R. F. M., Beurden, M. van, Korse, C. M., Kenter, G. G.·2017·Climacteric

Abstract

OBJECTIVES: To describe implications of premenopausal risk-reducing salpingo-oophorectomy (RRSO) on quality of life, endocrine symptoms, sexual function, osteoporosis, cardiovascular health, metabolic syndrome, cognitive impairment and safety of hormone replacement therapy. METHODS: We searched the following electronic databases: The Cochrane Library, EMBASE, PsycInfo, and MEDLINE. We selected controlled and uncontrolled trials of premenopausal women undergoing RRSO. Two authors independently assessed studies for inclusion. Reference lists of included reports were searched manually for additional studies. RESULTS: Surgical menopause leads to more menopausal complaints and sexual dysfunction than natural menopause. Overall quality of life is not affected by surgery. In the limited literature, there is no evidence that RRSO leads to more osteopenia in comparison with natural menopause at a young age. Cohort studies show a slight impaired cardiovascular health. Cognitive function decreases later in life in premenopausal oophorectomized women. Short-term hormone replacement therapy seems to decline postmenopausal complaints and does not seem to increase the risk for breast carcinoma in mutation carriers without a personal history of breast carcinoma. CONCLUSIONS: The conclusions of this systematic review are limited by the absence of randomized, controlled trials. There is growing evidence from observational studies that RRSO may impact negatively on all-cause non-survival endpoints.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1080/13697137.2017.1285879

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Undergoing surgical menopause is associated with increased risk of cognitive complaints and cognitive performance declines, particularly if surgery occurs before age 40 or natural menopause.

    “However, undergoing surgical menopause is associated with increased risk of cognitive complaints, cognitive performance declines, and possibly increased dementia risk, particularly if surgery occurs before age 40 or natural menopause [2–7].”

    From Treating new-onset cognitive complaints after risk-reducing salpingo-oophorectomy: A randomized controlled crossover trial of lisdexamfetamine (2024) · cites this paper as [2]

    The Discussion reports lower memory-task scores after surgical than natural menopause and says scores were lower when oophorectomy occurred at a younger age. The Cognitive function section reports increased later-life impairment, with the greatest risk before age 45 among women not treated with estrogen until at least 45. The copy does not establish a specific before-40 threshold or separately report an increased risk of cognitive complaints. (LLM, conf=0.86)

    Experimental — accuracy not yet measured
  • Risk-reducing bilateral salpingo-oophorectomy lowers the likelihood of ovarian and breast cancer among women who carry BRCA1 or BRCA2 gene mutations.

    “Risk-reducing bilateral salpingo-oophorectomy (RRSO) lowers the likelihood of ovarian and breast cancer among women who carry BRCA1 or BRCA2 gene mutations”

    From Treating new-onset cognitive complaints after risk-reducing salpingo-oophorectomy: A randomized controlled crossover trial of lisdexamfetamine (2024) · cites this paper as [2]

    The Introduction (page unavailable) says high-risk women undergo RRSO to lower ovarian cancer risk by 80–96% and identifies BRCA1/2 carriers as eligible. The Safety of hormone replacement therapy section reports lower breast cancer risk in a cohort of BRCA1/2 carriers who underwent RRSO and took HRT than in women who had neither; it does not establish a breast cancer reduction from RRSO alone. (LLM, conf=0.82)

    Experimental — accuracy not yet measured
  • For those without contraindications who undergo RRSO before age 45, estradiol must be initiated soon after surgery to obtain optimal protection against cognitive concerns.

    “Moreover, for those without contraindications who undergo RRSO before age 45, estradiol must be initiated soon after surgery to obtain the optimal protection against cognitive concerns, and studies indicate that estradiol therapy is only partially protective against several domains of cognitive decline [2,4,12,13].”

    From Treating new-onset cognitive complaints after risk-reducing salpingo-oophorectomy: A randomized controlled crossover trial of lisdexamfetamine (2024) · cites this paper as [2]

    The Cognitive function section (page unavailable) reports the greatest later-life cognitive risk among women who underwent oophorectomy before 45 and were not treated with estrogen until at least age 45. It concludes that HRT appears beneficial after RRSO before 45, but does not say estradiol must be started soon after surgery or establish that this timing provides optimal protection. (LLM, conf=0.88)

    Experimental — accuracy not yet measured
  • Estradiol therapy is only partially protective against several domains of cognitive decline.

    “Moreover, for those without contraindications who undergo RRSO before age 45, estradiol must be initiated soon after surgery to obtain the optimal protection against cognitive concerns, and studies indicate that estradiol therapy is only partially protective against several domains of cognitive decline [2,4,12,13].”

    From Treating new-onset cognitive complaints after risk-reducing salpingo-oophorectomy: A randomized controlled crossover trial of lisdexamfetamine (2024) · cites this paper as [2]

    The Cognitive function section (page unavailable) says HRT appears beneficial for cognitive impairment after RRSO before age 45, supporting a protective effect. The Discussion (page unavailable) reports no cognitive decline in one HRT-supplemented group, but neither passage establishes that estradiol specifically is only partially protective across several cognitive domains. (LLM, conf=0.85)

    Experimental — accuracy not yet measured
  • Undergoing surgical menopause is possibly associated with increased dementia risk.

    “However, undergoing surgical menopause is associated with increased risk of cognitive complaints, cognitive performance declines, and possibly increased dementia risk, particularly if surgery occurs before age 40 or natural menopause [2–7].”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 69

  1. Lux MP, Fasching PA, Beckmann MW. Hereditary breast and ovar- ian cancer: review and future perspectives. J Mol Med (Berl) 2006;84:16-28
  2. Sutcliffe S, Pharoah PD, Easton DF, Ponder BA. Ovarian and breast cancer risks to women in families with two or more cases of ovar- ian cancer. Int J Cancer 2000;87:110-17
  3. Chen S, Parmigiani G. Meta-analysis of BRCA1 and BRCA2 pene- trance. J Clin Oncol 2007;25:1329-33
  4. Olivier RI, Lubsen-Brandsma MA, Verhoef S, van Beurden M. CA125 and transvaginal ultrasound monitoring in high-risk women can- not prevent the diagnosis of advanced ovarian cancer. Gynecol Oncol 2006;100:20-6
  5. van Driel CM, de Bock GH, Arts HJ, et al. Stopping ovarian cancer screening in BRCA1/2 mutation carriers: effects on risk manage- ment decisions & outcome of risk-reducing salpingo-oophorec- tomy specimens. Maturitas 2015;80:318-22
  6. Kauff ND, Satagopan JM, Robson ME, et al. Risk-reducing salpingo- oophorectomy in women with a BRCA1 or BRCA2 mutation. N Engl J Med 2002;346:1609-15
  7. Rebbeck TR, Lynch HT, Neuhausen SL, et al. Prophylactic oophor- ectomy in carriers of BRCA1 or BRCA2 mutations. N Engl J Med 2002;346:1616-22
  8. Madalinska JB, van Beurden M, Bleiker EM, et al. Predictors of prophylactic bilateral salpingo-oophorectomy compared with gynecologic screening use in BRCA1/2 mutation carriers. J Clin Oncol 2007;25:301-7
  9. Cohen JV, Chiel L, Boghossian L, et al. Non-cancer endpoints in BRCA1/2 carriers after risk-reducing salpingo-oophorectomy. Fam Cancer 2012;11:69-75
  10. Madalinska JB, van Beurden M, Bleiker EM, et al. The impact of hormone replacement therapy on menopausal symptoms in younger high-risk women after prophylactic salpingo-oophorec- tomy. J Clin Oncol 2006;24:3576-82
  11. Holmberg L, Iversen OE, Rudenstam CM, et al. Increased risk of recurrence after hormone replacement therapy in breast cancer survivors. J Natl Cancer Inst 2008;100:475-82
  12. Elit L, Esplen MJ, Butler K, Narod S. Quality of life and psychosex- ual adjustment after prophylactic oophorectomy for a family his- tory of ovarian cancer. Fam Cancer 2001;1:149-56
  13. Benshushan A, Rojansky N, Chaviv M, et al. Climacteric symptoms in women undergoing risk-reducing bilateral salpingo-oophorec- tomy. Climacteric 2009;12:404-9
  14. Robson M, Hensley M, Barakat R, et al. Quality of life in women at risk for ovarian cancer who have undergone risk-reducing oophor- ectomy. Gynecol Oncol 2003;89:281-7
  15. Michelsen TM, Dorum A, Trope CG, Fossa SD, Dahl AA. Fatigue and quality of life after risk-reducing salpingo-oophorectomy in women at increased risk for hereditary breast-ovarian cancer. Int J Gynecol Cancer 2009;19:1029-36
  16. Madalinska JB, Hollenstein J, Bleiker E, et al. Quality-of-life effects of prophylactic salpingo-oophorectomy versus gynecologic screen- ing among women at increased risk of hereditary ovarian cancer. J Clin Oncol 2005;23:6890-8
  17. Finch A, Metcalfe KA, Chiang J, et al. The impact of prophylactic salpingo-oophorectomy on quality of life and psychological dis- tress in women with a BRCA mutation. Psychooncology 2013;22: 212-19
  18. Fang CY, Cherry C, Devarajan K, et al. A prospective study of qual- ity of life among women undergoing risk-reducing salpingo- oophorectomy versus gynecologic screening for ovarian cancer. Gynecol Oncol 2009;112:594-600
  19. Bresser PJ, Seynaeve C, Van Gool AR, et al. The course of distress in women at increased risk of breast and ovarian cancer due to an (identified) genetic susceptibility who opt for prophylactic mastectomy and/or salpingo-oophorectomy. Eur J Cancer 2007;43:95-103
  20. Fry A, Busby-Earle C, Rush R, Cull A. Prophylactic oophorectomy versus screening: psychosocial outcomes in women at increased risk of ovarian cancer. Psychooncology 2001;10:231-41
  21. Heiniger L, Butow PN, Coll J, et al. Long-term outcomes of risk- reducing surgery in unaffected women at increased familial risk of breast and/or ovarian cancer. Fam Cancer 2015;14:105-15
  22. Hallowell N, Baylock B, Heiniger L, et al. Looking different, feeling different: women's reactions to risk-reducing breast and ovarian surgery. Fam Cancer 2012;11:215-24
  23. Pezaro C, James P, McKinley J, et al. The consequences of risk reducing salpingo-oophorectomy: the case for a coordinated approach to long-term follow up post surgical menopause. Fam Cancer 2012;11:403-10
  24. Johansen N, Liavaag AH, Tanbo TG, et al. Sexual activity and func- tioning after risk-reducing salpingo-oophorectomy: impact of hor- mone replacement therapy. Gynecol Oncol 2016;140:101-16
  25. Lorenz T, McGregor B, Swisher E. Relationship satisfaction predicts sexual activity following risk-reducing salpingo-oophorectomy. J Psychosom Obstet Gynaecol 2014;35:62-8
  26. Tucker PE, Bulsara MK, Salfinger SG, et al. Prevalence of sexual dys- function after risk-reducing salpingo-oophorectomy. Gynecol Oncol 2016;140:95-100
  27. Finch A, Metcalfe KA, Chiang JK, et al. The impact of prophylactic salpingo-oophorectomy on menopausal symptoms and sexual function in women who carry a BRCA mutation. Gynecol Oncol 2011;121:163-8
  28. Shifren JL, Braunstein GD, Simon JA, et al. Transdermal testoster- one treatment in women with impaired sexual function after oophorectomy. N Engl J Med 2000;343:682-8
  29. Michelsen TM, Dorum A, Dahl AA. A controlled study of mental distress and somatic complaints after risk-reducing salpingo- oophorectomy in women at risk for hereditary breast ovarian can- cer. Gynecol Oncol 2009;113:128-33
  30. Hooker GW, King L, Vanhusen L, et al. Long-term satisfaction and quality of life following risk reducing surgery in BRCA1/2 mutation carriers. Hered Cancer Clin Pract 2014;12:9
  31. Shigehiro M, Kita M, Takeuchi S, et al. 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 2016;46:254-9
  32. Westin SN, Sun CC, Lu KH, et al. Satisfaction with ovarian carcin- oma risk-reduction strategies among women at high risk for breast and ovarian carcinoma. Cancer 2011;117:2659-67
  33. Challberg J, Ashcroft L, Lalloo F, et al. Menopausal symptoms and bone health in women undertaking risk reducing bilateral sal- pingo-oophorectomy: significant bone health issues in those not taking HRT. Br J Cancer 2011;105:22-7
  34. Touboul C, Uzan C, Ichante JL, et al. Factors associated with altered long-term well-being after prophylactic salpingo-oophorec- tomy among women at increased hereditary risk for breast and ovarian cancer. Oncologist 2011;16:1250-7
  35. Gallagher JC. Effect of early menopause on bone mineral density and fractures. Menopause 2007;14:567-71
  36. Fakkert IE, Abma EM, Westrik IG, et al. Bone mineral density and fractures after risk-reducing salpingo-oophorectomy in women at increased risk for breast and ovarian cancer. Eur J Cancer 2015;51:400-8
  37. Rocca WA, Grossardt BR, de Andrade M, Malkasian GD, Melton LJ. 3rd. Survival patterns after oophorectomy in premenopausal women: a population-based cohort study. Lancet Oncol 2006;7:821-8
  38. Chapman JS, Powell CB, McLennan J, et al. Surveillance of survi- vors: follow-up after risk-reducing salpingo-oophorectomy in BRCA 1/2 mutation carriers. Gynecol Oncol 2011;122:339-43
  39. Garcia C, Lyon L, Conell C, Littell RD, Powell CB. Osteoporosis risk and management in BRCA1 and BRCA2 carriers who undergo risk- reducing salpingo-oophorectomy. Gynecol Oncol 2015;138:723-6
  40. Michelsen TM, Tonstad S, Pripp AH, Trope CG, Dorum A. Coronary heart disease risk profile in women who underwent salpingo- oophorectomy to prevent hereditary breast ovarian cancer. Int J Gynecol Cancer 2010;20:233-9
  41. Michelsen TM, Pripp AH, Tonstad S, Trope CG, Dorum A. Metabolic syndrome after risk-reducing salpingo-oophorectomy in women at high risk for hereditary breast ovarian cancer: a controlled obser- vational study. Eur J Cancer 2009;45:82-9
  42. Rocca WA, Bower JH, Maraganore DM, et al. Increased risk of cog- nitive impairment or dementia in women who underwent oophor- ectomy before menopause. Neurology 2007;69:1074-83
  43. Rocca WA, Shuster LT, Grossardt BR, et al. Long-term effects of bilateral oophorectomy on brain aging: unanswered questions from the Mayo Clinic Cohort Study of Oophorectomy and Aging. Womens Health (Lond Engl) 2009;5:39-48
  44. Eisen A, Lubinski J, Gronwald J, et al. Hormone therapy and the risk of breast cancer in BRCA1 mutation carriers. J Natl Cancer Inst 2008;100:1361-7
  45. Rebbeck TR, Friebel T, Wagner T, et al. Effect of short-term hor- mone replacement therapy on breast cancer risk reduction after bilateral prophylactic oophorectomy in BRCA1 and BRCA2 muta- tion carriers: the PROSE Study Group. J Clin Oncol 2005;23:7804-10
  46. Ness RB, Albano JD, McTiernan A, Cauley JA. Influence of estrogen plus testosterone supplementation on breast cancer. Arch Intern Med 2009;169:41-6
  47. Loibl S, Schwedler K, von Minckwitz G, et al. Venlafaxine is super- ior to clonidine as treatment of hot flashes in breast cancer patients-a double-blind, randomized study. Ann Oncol 2007;18:689-93
  48. Armstrong K, Schwartz JS, Randall T, Rubin SC, Weber B. Hormone replacement therapy and life expectancy after prophylactic oophorectomy in women with BRCA1/2 mutations: a decision ana- lysis. J Clin Oncol 2004;22:1045-54
  49. Arts-de Jong M, Maas AH, Massuger LF, Hoogerbrugge N, de Hullu JA. BRCA1/2 mutation carriers are potentially at higher cardiovas- cular risk. Crit Rev Oncol Hematol 2014;91:159-71
  50. Cummings SR, Browner WS, Bauer D, et al. Endogenous hormones and the risk of hip and vertebral fractures among older women. Study of Osteoporotic Fractures Research Group. N Engl J Med 1998;339:733-8
  51. Hadjidakis D, Kokkinakis E, Sfakianakis M, Raptis SA. The type and time of menopause as decisive factors for bone mass changes. Eur J Clin Invest 1999;29:877-85
  52. Melton LJ, 3rd., Khosla S, Malkasian GD, et al. Fracture risk after bilateral oophorectomy in elderly women. J Bone Miner Res 2003;18:900-5
  53. Yoshida T, Takahashi K, Yamatani H, Takata K, Kurachi H. Impact of surgical menopause on lipid and bone metabolism. Climacteric 2011;14:445-52
  54. Ossewaarde ME, Bots ML, Verbeek AL, et al. Age at menopause, cause-specific mortality and total life expectancy. Epidemiology 2005;16:556-62
  55. Atsma F, Bartelink ML, Grobbee DE, van der Schouw YT. Postmenopausal status and early menopause as independent risk factors for cardiovascular disease: a meta-analysis. Menopause 2006;13:265-79
  56. Franklin RM, Ploutz-Snyder L, Kanaley JA. Longitudinal changes in abdominal fat distribution with menopause. Metabolism 2009;58:311-15
  57. Matthews KA, Crawford SL, Chae CU, et al. Are changes in cardio- vascular disease risk factors in midlife women due to chrono- logical aging or to the menopausal transition? J Am Coll Cardiol 2009;54:2366-73
  58. Nappi RE, Sinforiani E, Mauri M, et al. Memory functioning at menopause: impact of age in ovariectomized women. Gynecol Obstet Invest 1999;47:29-36
  59. Farrag AK, Khedr EM, Abdel-Aleem H, Rageh TA. Effect of surgical menopause on cognitive functions. Dement Geriatr Cogn Disord 2002;13:193-8
  60. Sherwin BB. Estrogen and/or androgen replacement therapy and cognitive functioning in surgically menopausal women. Psychoneuroendocrinology 1988;13:345-57
  61. Shumaker SA, Legault C, Rapp SR, et al. Estrogen plus progestin and the incidence of dementia and mild cognitive impairment in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial. JAMA 2003;289:2651-62
  62. LaCroix AZ, Chlebowski RT, Manson JE, et al. Health outcomes after stopping conjugated equine estrogens among postmeno- pausal women with prior hysterectomy: a randomized controlled trial. JAMA 2011;305:1305-14
  63. Chlebowski RT, Kuller LH, Prentice RL, et al. Breast cancer after use of estrogen plus progestin in postmenopausal women. N Engl J Med 2009;360:573-87
  64. Anderson GL, Chlebowski RT, Rossouw JE, et al. Prior hormone therapy and breast cancer risk in the Women's Health Initiative randomized trial of estrogen plus progestin. Maturitas 2006;55:103-15
  65. Beral V. Million Women Study Collaborators. Breast cancer and hormone-replacement therapy in the Million Women Study. Lancet 2003;362:419-27
  66. Panay N, Hamoda H, Arya R, et al. The 2013 British Menopause Society & Women's Health Concern recommendations on hormone replacement therapy. Menopause Int 2013;19:59-68
  67. Reitsma W, de Bock GH, Oosterwijk JC, et al. Support of the 'fallo- pian tube hypothesis' in a prospective series of risk-reducing sal- pingo-oophorectomy specimens. Eur J Cancer 2013;49:132-41
  68. Leblanc E, Narducci F, Farre I, et al. Radical fimbriectomy: a reason- able temporary risk-reducing surgery for selected women with a germ line mutation of BRCA 1 or 2 genes? Rationale and prelimin- ary development. Gynecol Oncol 2011;121:472-6
  69. Holman LL, Friedman S, Daniels MS, Sun CC, Lu KH. Acceptability of prophylactic salpingectomy with delayed oophorectomy as risk- reducing surgery among BRCA mutation carriers. Gynecol Oncol 2014;133:283-6

Cited by

Sorted by citations

Authors
Vermeulen, R. F. M., Beurden, M. V., Korse, C. M., & Kenter, G. G.
Affiliations
The Netherlands Cancer Institute (NL)
Corresponding author
Beurden, M. van
Venue
Climacteric
Published
2017-03-02
Volume
20
Issue
3
Pages
212-221
ISSN
  • 1369-7137 (ISSN-L)
  • 1473-0804
OpenAlex
W2601659517
Cited by
62
References
1
Citations by year
2026: 7 · 2025: 6 · 2024: 12 · 2023: 4 · 2022: 7 · 2021: 10 · 2020: 7 · 2019: 5 · 2018: 4
FWCI
0.56
Type
journal article
Language
en
Open access
Licence
other-oa
Locations
  • Climacteric (publishedVersion)
  • PubMed (publishedVersion)
  • Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
  • Pure Amsterdam UMC (submittedVersion, other-oa)
  • Data Archiving and Networked Services (DANS) (submittedVersion)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › BRCA gene mutations in cancer
  • Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Menopause: Health Impacts and Treatments
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Breast Cancer Treatment Studies
Keywords
risk-reducing salpingo-oophorectomy, premenopausal women, surgical menopause, quality of life, menopausal symptoms, sexual dysfunction, osteoporosis, cardiovascular health, metabolic syndrome, cognitive impairment, hormone replacement therapy, breast cancer risk, BRCA mutation carriers, BRCA2 mutation carriers, BRCA1 mutation carriers
MeSH terms
Female, Humans, Menopause, Premature, Ovarian Neoplasms, Ovariectomy, Quality of Life, Estrogen Replacement Therapy, Risk Reduction Behavior, Salpingectomy

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review