Abstract
More than 40 years ago Lynch et al. described several multigenerational breast cancer family pedigrees which demonstrated autosomal dominant inheritance of a trait(s) that increased risks for both breast and ovarian cancers. Mutation carriers in at least 90 % of these hereditary breast ovarian cancer (HBOC) syndrome families have been linked to cancer-associated mutations in the genes BRCA1 and BRCA2. This review focuses on the contributions of Lynch, colleagues and collaborators and pertinent literature, toward defining the HBOC syndrome, the cancer risks that the inherited adverse mutations convey, the gynecologic tissues and organs from which the malignancy may arise to disseminate throughout the pelvic and abdominal organs and peritoneum and how this information can be used to reduce the risk and morbidities of intra-abdominal carcinomatosis in effected individuals.
Similar content being viewed by others
References
Lynch HT, Shaw MW, Magnuson CW, Larsen AL, Krush AJ (1966) Hereditary factors in cancer: study of two large Midwestern kindreds. Arch Intern Med 117:206–212
Lynch HT, Krush AJ (1967) Heredity and adenocarcinoma of the colon. Gastroenterology 53:517–527
Lynch HT, Lynch PM (1979) The cancer-family syndrome: a pragmatic basis for syndrome identification. Dis Colon Rectum 22:106–110
Lynch HT, de la Chapelle A (1999) Genetic susceptibility to non-polyposis colorectal cancer. J Med Genet 36:801–818
Aarnio M, Sankila R, Pukkala E, Salovaara R, Aaltonen LA, de la Chapelle A, Peltomäki P, Mecklin J-P, Järvinen H-J (1999) Cancer risk in mutation carriers of DNA-mismatch-repair genes. Int J Cancer 81:214–218
Watson P, Lynch HT (2001) Cancer risk in mismatch repair gene mutation carriers. Fam Cancer 1:57–60
Lynch HT, Lynch JF, Lynch PM, Attard T (2008) Hereditary colorectal cancer syndromes: molecular genetics, genetic counseling, diagnosis and management. Fam Cancer 7:27–39
Watson P, Vasen HFA, Mecklin J-P, Bernstein I, Aarnio M, Järvinen HJ, Myrhøj T, Sunde L, Wijnen JT, Lynch HT (2008) The risk of extra-colonic, extra-endometrial cancer in the Lynch syndrome. Int J Cancer 123:444–449
Bellizzi AM, Frankel WL (2009) Colorectal cancer due to deficiency in DNA mismatch repair function: a review. Adv Anat Pathol 16:405–417
Lynch HT, Krush AJ (1971) Carcinoma of the breast and ovary in three families. Surg Gynecol Obstet 133:644–648
Lynch HT, Krush AJ, Lemon HM, Kaplan AR, Condit PT, Bottomley RH (1972) Tumor variation in families with breast cancer. JAMA 222:1631–1635
Lynch HT, Guirgis HA, Albert S, Brennan M, Lynch J, Kraft C, Pocekay D, Vaughns C, Kaplan A (1974) Familial association of carcinoma of the breast and ovary. Surg Gynecol Obstet 138:717–724
Lynch HT, Harris RE, Guirgis HA, Maloney K, Carmody MK, Lynch JF (1978) Familial association of breast/ovarian carcinoma. Cancer 41:1543–1548
Lynch HT, Watson P, Bewtra C, Conway TA, Hippee CR, Kaur P, Lynch JF, Ponder BAJ (1991) Hereditary ovarian cancer. Heterogeneity in age at diagnosis. Cancer 67:1460–1466
Lynch HT, Conway T, Lynch J (1991) Hereditary ovarian cancer. pedigree studies, Part II. Cancer Genet Cytogenet 53:161–183
Lynch HT, Watson P, Lynch JF, Conway TA, Fili M (1993) Hereditary ovarian cancer. Heterogeneity in age at onset. Cancer 71:573–581
Hall HJ, Lee MK, Newman B, Morrow JE, Anderson LA, Huey B, King MC (1990) Linkage of early-onset breast cancer to chromosome 17q21. Science 250:1684–1689
Narod SA, Feunteum J, Lynch HT, Watson P, Conway T, Lenoir GM (1991) Familial breast-ovarian cancer locus on chromosome 17q12–q23. Lancet 338:82–83
Miki Y, Swensen J, Shattuck-Eidens D, Futreal PA, Harshman K, Tavtigian S, Cochran C, Bennett LM, Ding W et al (1994) A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science 266:66–71
Wooster R, Neuhausen SL, Mangion J, Quirk Y, Ford D, Collins N, Nguyen K, Seal S, Tran T, Averill D et al (1994) Localization of a breast cancer susceptibility gene, BRCA2, to chromosome 13q12–13. Science 265:2088–2090
Wooster R, Bignell G, Lancaster J, Swift S, Seal S, Mangion J, Collins N, Gregory S, Gumbs C, Micklem G (1995) Identification of the breast cancer susceptibility gene BRCA2. Nature 378:789–792
National Center for Biotechnology Information. National Institutes of Health. www.ncbi.nlm.nih.gov/sites/entrez?db=gene. Accessed 1 Sept 2015
Ford D, Easton DF, Stratton M, Narod S, Goldgar D, Devilee P, Bishop DT, Weber B, Lenoir G, Chang-Claude J, Sobol H, Teare MD, Struewing J, Arason A, Scherneck S, Peto J, Rebbeck TR, Tonin P, Neuhausen S, Barkardottir R, Eyfjord J, Lynch H, Ponder BA, Gayther SA, Zelada-Hedman M et al (1998) Genetic heterogeneity and penetrance analysis of the BRCA1 and BRCA2 genes in breast cancer families. Am J Hum Genet 62:676–689
Chen S, Parmigiani G (2007) Meta-analysis of BRCA1 and BRCA2 penetrance. J Clin Oncol 25:1329–1333
Tobacman JK, Tucker MA, Kase R, Greene MH, Costa J, Fraumeni JF Jr (1982) Intra-abdominal carcinomatosis after prophylactic oophorectomy in ovarian-cancer-prone families. Lancet 2:795–797
Chen KT, Schooley JL, Flam MS (1985) Peritoneal carcinomatosis after prophylactic oophorectomy in familial ovarian cancer syndrome. Obstet Gynecol 66:93S–94S
Lynch HT, Bewtra C, Lynch JF (1986) Familial peritoneal ovarian carcinomatosis: a new clinical entity? Med Hypotheses 21:171–177
Casey MJ, Synder C, Bewtra C, Narod SA, Watson P, Lynch HT (2005) Intra-abdominal carcinomatosis after prophylactic oophorectomy in women of hereditary breast ovarian cancer syndrome kindreds associated with BRCA1 and BRCA2 mutations. Gynecol Oncol 97:457–467
Lakhani SR, Manek S, Penault-Llorca F, Flanagan A, Arnout L, Merrett S, McGuffog L, Steele D, Devilee P, Klijn JG, Meijers-Heijboer H, Radice P, Pilotti S, Nevanlinna H, Butzow R, Sobol H, Jacquemier J, Lyonet DS, Neuhausen SL, Weber B, Wagner T, Winqvist R, Bignon YJ, Monti F, Schmitt F, Lenoir G, Seitz S, Hamman U, Pharoah P, Lane G, Ponder B, Bishop DT, Easton DF (2004) Pathology of ovarian cancers in BRCA1 and BRCA2 mutation carriers. Clin Cancer Res 10:2473–2481
Wang C, Horiuchi A, Imai T, Ohira S, Itoh K, Nikaido T, Katsuyama Y, Konishi I (2004) Expression of BRCA1 protein in benign, borderline, and malignant epithelial ovarian neoplasms and its relationship to methylation and allelic loss of the BRCA1 gene. J Pathol 202:215–223
Casey MJ, Bewtra C (2004) Peritoneal carcinoma in women with genetic susceptibility: implications for Jewish populations. Fam Cancer 3:265–281
Vang R, Shih I-M, Kurman RJ (2009) Ovarian low-grade and high-grade serous carcinoma: pathogenesis, clinicopathologic and molecular biologic features, and diagnostic problems. Adv Anat Pathol 16:267–282
Werness BA, Parvatiyar P, Ramus SJ, Whittemore AS, Garlinghouse-Jones K, Oakley-Girvan I, DiCioccio RA, Wiest J, Tsukada Y, Ponder BAJ, Piver MS (2000) Ovarian carcinoma in situ with germline BRCA1 mutation and loss of heterozygosity at BRCA1 and TP53. J Natl Cancer Inst 92:1088–1091
Foyle A, Al-Jabi M, McCaughey WTE (1981) Papillary peritoneal tumors in women. Am J Surg Pathol 5:241–249
Schoenwolf GC, Bleyl SB, Brauer PR, Francis-West PH (2015) Development of the reproductive system. In: Schoenwolf GC (ed), Larsen’s human embryology, 5th edn. Philadelphia, Elsevier/Churchill-Livingston. https://www.clinicalkey.com/#!/content/book/3-s2.0-B9781455706846000163. Accessed September 12, 2015
Healy A (2012) Embryology of the female reproductive tract. In: Mann GS, Blair JC, Garden AS (eds) Imaging of gynecological disorders in infants and children. Springer, Berlin, pp 21–30. doi:10.1007/174_2010_128. Accessed 10 Sept 2015
Piek JMJ, Torrenga B, Hermsen B, Verheijen RHM, Zweemer RP, Gille JJP, Kenemans P, van Diest PJ, Menko FH (2003) Histopathological characteristics of BRCA1- and BRCA2-associated intraperitoneal cancer: a clinic-based study. Fam Cancer 2:73–78
Casey MJ, Bewtra C, Lynch HT, Snyder C, Stacy M, Watson P (2013) Phenotypic heterogeneity of hereditary gynecologic cancers: a report from the Creighton hereditary cancer registry. Fam Cancer 12:719–740
Fraumeni JF Jr, Grundy GW, Creagan ET, Everson RB (1975) Six families prone to ovarian cancer. Cancer 36:364–369
Zweemer RP, van Diest PJ, Verheijen RHM, Ryan A, Gulle JJP, Sijmons RH, Jacobs IJ, Menko FH, Kenemans P (2000) Molecular evidence linking primary cancer of the fallopian tube to BRCA1 germline mutations. Gynecol Oncol 76:45–50
Rose PG, Shrigley R, Wiesner GL (2000) Germline BRCA2 mutation in a patient with fallopian tube carcinoma: a case report. Gynecol Oncol 77:319–320
Paley PJ, Swisher EM, Garcia RL, Agoff SN, Greer BE, Peters KL, Goff BA (2001) Occult cancer of the fallopian tube in BRCA-1 mutation carriers at prophylactic oophorectomy: a case for recommending hysterectomy at surgical prophylaxis. Gynecol Oncol 80:176–180
Leeper K, Garcia R, Swisher E, Goff B, Greer B, Paley P (2002) Pathologic findings in prophylactic oophorectomy specimens in high-risk women. Gynecol Oncol 87:52–56
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 20:1260–1268
Agoff SN, Mendelin JE, Grieco VS, Garcia RL (2002) Unexpected gynecologic neoplasms in patients with proven or suspected BRCA-1 or -2 mutations: implications for gross examination, cytology, and clinical follow-up. Am J Surg Pathol 26:171–178
Thompson D, Easton DF, the Breast Cancer Linkage Consortium (2002) Cancer incidence in BRCA1 mutation carriers. J Natl Cancer Inst 94:1358–1365
Piek JMJ, Verheijen RHM, Kenemans P, Massuger LF, Bulten H, van Diest PJ (2003) BRCA1/2-related ovarian cancers are of tubal origin: a hypothesis. Gynecol Oncol 90:491
Lee Y, Medeiros F, Kindelberger D, Callahan MJ, Muto M, Crum CP (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
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 118:814–824
Yates MS, Meyer LA, Deavers MT, Daniels MS, Keeler ER, Mok SC, Gershenson DM, Lu KH (2011) Microscopic and early-stage ovarian cancers in BRCA1/2 mutation carriers: building a model for early BRCA-associated tumorigenesis. Cancer Prev Res 4:463–470
Reitsma W, de Bock GH, Ossterwijk JC, Bart J, Hollema H, Mourits MJE (2013) Support of the ‘fallopian tube hypothesis’ in a prospective series of risk-reducing salpingo-oophorectomy specimens. Eur J Cancer 49:132–141
Powell CB, Swisher EM, Cass I, McLennan J, Norquist B, Garcia RL, Lester J, Karlan BY, Chen L (2013) Long term follow up of BRCA1 and BRCA2 mutation carriers with unsuspected neoplasia identified at risk reducing salpingo-oophorectomy. Gynecol Oncol 129:364–371
Sherman ME, Piedmonte M, Mai PL, Ioffe OB, Ronnett BM, Van Le L, Ivanov I, Bell MC, Blank SV, DiSilvestro P, Hamilton CA, Tewari KS, Wakeley K, Kauff ND, Yamada SD, Rodriguez G, Skates SJ, Alberts DS, Walker JL, Minasian L, Lu K, Greene MH (2014) Pathologic findings at risk-reducing salpingo-oophorectomy: primary results from Gynecologic Oncology Group Trial GOG-0199. J Clin Oncol 32:3275–3283
Conner JR, Meserve E, Pizer E, Garber J, Roh M, Urban N, Drescher C, Quade BJ, Muto M, Howitt BE, Pearlman MD, Berkowitz RS, Horowitz N, Crum CP, Feltmate C (2014) Outcome of unexpected adnexal neoplasia discovered during risk reduction salpingo-oophorectomy in women with germ-line BRCA1 or BRCA2 mutations. Gynecol Oncol 132:280–286
Kindelberger DW, Le Y, Miron A, Hirsch MS, Feltmate C, Medeiros F, Callahan MJ, Garner EO, Gordon RW, Birch C, Berkowitz RS, Muto MG, Crum CP (2007) Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: evidence for a causal relationship. Am J Surg Pathol 31:161–169
Carlson JW, Miron A, Jarboe EA, Parast MM, Hirsch MS, Lee Y, Muto MG, Kindelberger D, Crum CP (2008) Serous tubal intraepithelial carcinoma: its potential role in primary peritoneal serous carcinoma and serous cancer prevention. J Clin Oncol 26:4160–4165
Kuhn E, Kurman RJ, Vang R, Sehdev AS, Han G, Soslow R, Wang T-L, Shih l-M (2012) TP53 mutations in serous tubal intraepithelial carcinoma and concurrent pelvic high-grade serous carcinoma—evidence supporting the clonal relationship of the two lesions. J Pathol 226:421–426
Nik NN, Vang R, Shih I-M, Kurman RJ (2014) Origin and pathogenesis of pelvic (ovarian, tubal, and primary peritoneal) serous carcinoma. Annu Rev Pathol Mech Dis 9:27–45
Cass I, Walts AE, Barbuto D, Lester J, Karlan B (2014) A cautious view of putative precursors of serous carcinomas in the fallopian tubes of BRCA mutation carriers. Gynecol Oncol 134:492–497
Seidman JD, Zhao P, Yemelyanova A (2011) “Primary peritoneal” high-grade serous carcinoma is very likely metastatic from serous tubal intraepithelial carcinoma: assessing the new paradigm of ovarian and pelvic serous carcinogenesis and its implications for screening for ovarian cancer. Gynecol Oncol 120:470–473
Vicus D, Finch A, Cass I, Rosen B, Murphy J, Fan I, Royer R, McLaughlin J, Karlan B, Narod SA (2010) Prevalence of BRCA1 and BRCA2 germ line mutations among women with carcinoma of the fallopian tube. Gynecol Oncol 118:299–302
Hornreich G, Beller U, Lavie O, Renbaum P, Cohen Y, Levy-Lahad E (1999) Is uterine serous papillary carcinoma a BRCA1-related disease? Case report and review of the literature. Gynecol Oncol 75:300–304
Lavie O, Hornreich G, Ben-Arie A, Rennert G, Cohen Y, Keidar R, Sagi S, Lahad EL, Auslander R, Beller U (2004) BRCA germline mutations in Jewish women with uterine serous papillary carcinoma. Gynecol Oncol 92:521–524
Lavie O, Ben-Arie A, Pilip A, Rennert G, Cohen Y, Feiner B, Auslnader R (2005) BRCA2 germline mutation in a woman with uterine serous papillary carcinoma—case report. Gynecol Oncol 99:486–488
Goshen R, Chu W, Elit L, Pal T, Hakimi J, Ackerman I, Fyles A, Mitchell M, Narod SA (2000) Is uterine papillary serous adenocarcinoma a manifestation of the hereditary breast-ovarian cancer syndrome? Gynecol Oncol 79:477–481
Levine DA, Lin O, Barakat RR, Robson ME, McDermott D, Cohen L, Satagopan J, Offit K, Boyd J (2001) Risk of endometrial carcinoma associated with BRCA mutation. Gynecol Oncol 80:395–398
Barak F, Milgrom R, Laitman Y, Gemer O, Rabinovich A, Piura B, Anteby E, Baruch GB, Korach J, Friedman E (2010) The rate of the predominant Jewish mutations in the BRCA1, BRCA2, MSH2 and MSH6 genes in unselected Jewish endometrial cancer patients. Gynecol Oncol 119:511–515
Bruchim I, Amichay K, Kidron D, Attias Z, Biron-Shental T, Drucker L, Friedman E, Werner H, Fishman A (2010) BRCA1/2 germline mutation in Jewish patients with uterine serous carcinoma. Int J Gynecol Cancer 20:1148–1153
Lavie O, Ben-Arie A, Segev Y, Faro J, Barak F, Haya N, Auslender R, Gemer O (2010) BRCA germline mutations in women with uterine serous carcinoma—still a debate. Int J Gynecol Cancer 20:1531–1534
Pennington KP, Walsh T, Lee M, Pennil C, Novetsky AP, Agnew KJ, Thronton A, Garcia R, Mutch D, King M-C, Goodfellow P, Swisher EM (2013) BRCA1, TP53, and CHEK2 germline mutations in uterine serous carcinoma. Cancer 119:332–338
Casey MJ, Bewtra C, Lynch HT, Snyder CL, Stacey M (2015) Endometrial cancers in mutation carriers from hereditary breast ovarian cancer syndrome kindreds: report from the Creighton University Hereditary Cancer Registry with review of the implications. Int J Gynecol Cancer 25:650–656
Creasman WT, Odicino F, Maisonneuve P, Quinn MA, Beller U, Benedet JL, Heintz APM, Ngan HYS, Pecorelli S (2006) Carcinoma of the corpus uteri. FIGO 26th annual report on the results of treatment in gynecological cancer. Int J Gynaecol Obstet 95(Suppl 1):S105–S143
Brinton LA, Felix AS, McMeekin DS, Creasman WT, Sherman ME, Mutch D, Cohn DE, Walker JL, Moor RG, Downs LS, Soslow RA, Zaino R (2013) Etiologic heterogeneity in endometrial cancer: evidence from a Gynecologic Oncology Group trial. Gynecol Oncol 129:277–284
del Carmen MG, Birrer M, Schorge JO (2012) Uterine papillary serous cancer: a review of the literature. Gynecol Oncol 127:651–661
Semaan A, Mert I, Munkarah AR, Bandyopadhyay S, Mahdi HS, Winer IS, Nucci MR, Hussein Y, Quershi F, Hayek K, Tabassum F, Alosh B, Schultz DS, Cote ML, Vijver KK, Morris RT, Oliva E, Ali-Fehmi R (2013) Clinical and pathologic characteristics of serous carcinoma confined to the endometrium: a multi-institutional study. Int J Gynecol Pathol 32:181–187
Sagae S, Susumu N, Viswanathan AN, Aoki D, Backes FJ, Provencher DM, Vaughan M, Creutzberg CL, Kurzeder C, Kristensen G, Lee C, Kurtz J-E, Glasspool RM, Small W Jr (2014) Gynecologic Cancer InterGroup (GCIG) consensus review for uterine serous carcinoma. Int J Gynecol Cancer 24(9 suppl 3):S83–S89
Boruta DM II, Gehrig PA, Groben PA, Bae-Jump V, Boggess JF, Fowler WC Jr, Van Le L (2004) Uterine serous and grade 3 endometrioid carcinomas: is there a survival difference? Cancer 101:2214–2221
Zheng W, Schwartz PE (2005) Serous EIC as an early form of uterine papillary serous carcinoma: recent progress in understanding its pathogenesis and current opinions regarding pathologic and clinical management. Gynecol Oncol 96:579–582
Jarboe EA, Miron A, Carlson JW, Hirsch MS, Kindelberger D, Mutter GL, Crum CP, Nucci MR (2009) Coexisting intraepithelial serous carcinoma of the endometrium and fallopian tube: frequency and potential significance. Int J Gynecol Pathol 28:308–315
Massuger L, Roelofsen T, van Ham M, Bulten J (2010) The origin of serous ovarian cancer may be found in the uterus: a novel hypothesis. Med Hypothesis 74:859–861
Roelofsen T, van Kempen LCLT, van der Laak JAWM, van Ham MA, Bulten J, Massuger LFAG (2012) Concurrent endometrial intraepithelial carcinoma (EIC) and serous ovarian cancer: can EIC be seen as the precursor lesion? Int J Gynecol Cancer 22:457–464
Tolcher MC, Swisher EM, Medeiros F, Lima JF, Hilderbrand JL, Donovan JL, Garcia RL, Cliby WA, Dowdy SC (2015) Characterization of precursor lesions in the endometrium and fallopian tube epithelium of early-stage uterine serous carcinoma. Int J Gyencol Pathol 34:57–64
Stewart CJR, Doherty DA, Havlat M, Koay MHE, Leung YC, Naran A, O’Brien D, Ruba S, Salfinger S, Tan J (2013) Transtubal spread of endometrial carcinoma: correlation of intra-luminal tumour cells with tumour grade, peritoneal fluid cytology, and extra-uterine metastasis. Pathology 45:382–387
Jia L, Yuan Z, Wang Y, Cragun JM, Kong B, Zheng W (2015) Primary sources of pelvic serous cancer in patients with endometrial intraepithelial carcinoma. Mod Pathol 28:118–127
Mingles MJJM, van Ham MAPC, de Kievit IM, Snijders MPML, van Tilborg AAG, Bulten J, Massuger LFAG (2014) Müllerian precursor lesions in serous ovarian cancer patients: using the SEE-Fim and SEE-End protocol. Mod Pathol 27:1002–1013
Zhou C, Gilks CB, Hayes M, Clement PB (1998) Papillary serous carcinoma of the uterine cervix: a clinicopathologic study of 17 cases. Am J Surg Pathol 22:113–120
Kaplan EJ, Caputo TA, Shen PUF, Sassoon RI, Soslow RA (1998) Familial papillary serous carcinoma of the cervix, peritoneum, and ovary: a report of the first case. Gynecol Oncol 70:289–294
Friebel TM, Domchek SM, Rebbeck TR (2014) Modifiers of cancer risk in BRCA1 and BRCA2 mutation carriers: systematic review and meta-analysis. J Natl Cancer Inst 106:dju091
Garcia C, Powell CB (2015) A comprehensive approach to the identification and management of the BRCA patient. Obstet Gynecol Surv 70:131–143
Nelson HD, Pappas M, Zakher B, Mitchell JP, Okinaka-Hu L, Fu R (2014) Risk assessment, genetic counseling, and genetic testing for BRCA-related cancer in women: a systematic review to update the U.S. Preventive Services Task Force recommendation. Ann Intern Med 160:255–266
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 101:80–87
Kauff ND, Satagopan JM, Robson ME, Scheuer L, Hensley M, Hudi 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. N Engl J Med 346:1609–1615
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, the prevention and observation of surgical end points study group (2002) Prophylactic oophorectomy in carriers of BRCA1 or BRCA2 mutations. N Engl J Med 346:1616–1622
Anderson CK, Wallace S, Guiahi M, Sheeder J, Bahbakht K, Spillman MA (2013) Risk-reducing salpingectomy as preventive strategy for pelvic serous cancer. Int J Gynecol Cancer 23:417–421
Schenberg T, Mitchell G (2014) Prophylactic bilateral salpingectomy as a prevention strategy in women at high-risk of ovarian cancer: a mini-review. Front Oncol 4:21
Kwon JS, Tinker A, Pansegrau G, McAlpine J, Housty M, McCullum M, Gilks CB (2013) Prophylactic salpingectomy and delayed oophorectomy as an alternative for BRCA mutation carriers. Obstet Gynecol 121:14–24
Lostumbo L, Carbine NE, Wallace J (2010) Prophylactic mastectomy for the prevention of breast cancer. Cochrane Database Syst Rev 10(11):CD002748
Zagouri F, Chrysikos DT, Sergentanis TN, Giannakopoulou G, Zografos CG, Papadimitriou CA, Zografos GC (2013) Prophylactic mastectomy: an appraisal. Am Surg 79:205–212
De Felice F, Marchetti C, Musella A, Palaia I, Perniola G, Musio D, Muzii L, Tombolini V, Panici PB (2015) Bilateral risk-reduction mastectomy in BRCA1 and BRCA2 mutation carriers: a meta-analysis. Ann Surg Oncol 22:2876–2880
Domchek SM, Friebel TM, Singer CF, Evans DG, Lynch HT, Isaacs C, Garber JE, Neuhausen SL, Matloff E, Eeles R, Pichert G, Van t’veer L, Tung N, Weitzel JN, Couch FJ, Rubinstein WS, Ganz PA, Daly MB, Olopade OI, Tomlison G, Schildkraut J, Blum JL, Rebbeck TR (2010) Association of risk-reducing surgery in BRCA1 or BRCA2 mutation carriers with cancer risk and mortality. JAMA 304:967–975
Ingram SL, Sperrin M, Baildam A, Ross GL, Clayton R, Lalloo F, Buchan I, Howell A, Evans DGR (2013) Risk-reducing surgery increases survival in BRCA1/2 mutation carriers unaffected at time of family referral. Breast Cancer Res Treat 142:611–618
Finch APM, Lubinski J, Møller P, Singer CF, Karlan B, Senter L, Rosen B, Maehle L, Ghadiraian P, Cybulski C, Huzarski T, Eisen A, Foulkes WD, Kim-Sing C, Ainsworth P, Tung N, Lynch HT, Neuhausen S, Metcalfe KA, Thompson I, Murphy J, Sun P, Narod SA (2014) Impact of oophorectomy on cancer incidence and mortality in women with BRCA1 or BRCA2 mutation. J Clin Oncol 32:1547–1553
Schrag D, Kuntz KM, Garber JE, Weeks JC (1997) Decision analysis—effects of prophylactic mastectomy and oophorectomy on life expectancy among women with BRCA1 or BRCA2 mutations. N Engl J Med 336:1465–1471
van Roosmalen MS, Verhoef LCG, Stalmeier PFM, Hoogerbrugge N, van Daal WAJ (2002) Decision analysis of prophylactic surgery or screening for BRCA1 mutation carriers: a more prominent role for oophorectomy. J Clin Oncol 20:2092–2100
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 20:2520–2529
Armstrong K, Schwartz JS, Randall T, Rubin SC, Weber B (2004) Hormone replacement therapy and life expectancy after prophylactic oophorectomy in women with BRCA1/2 mutations: a decision analysis. J Clin Oncol 22:1045–1054
Kurian AW, Sigal BM, Plevritis SK (2010) Survival analysis of cancer risk reduction strategies for BRCA1/2 mutation carriers. J Clin Oncol 28:222–231
Sigal BM, Munoz DF, Kurian AW, Plevritis SK (2012) A simulation model to predict the impact of prophylactic surgery and screening on the life expectancy of BRCA1 and BRCA2 mutation carriers. Cancer Epidemiol Biomark Prev 21:1066–1077
Holman LL, Friedman S, Daniels MS, Sun CC, Lu KH (2014) Acceptability of prophylactic salpingectomy with delayed oophorectomy as risk-reducing surgery among BRCA mutation carriers. Gynecol Oncol 133:283–286
Arts-de Jong M, Harmsen MG, Hoogerbrugge N, Massuger LF, Hermens RP, de Hullu JA (2015) Risk-reducing salpingectomy with delayed oophorectomy in BRCA1/2 mutation carriers: patients’ and professionals’ perspectives. Gynecol Oncol 136:305–310
Harmsen MG, Arts-de Jong M, Hoogerbrugge N, Maas AHEM, Prins JB, Bulten J, Teerenstra S, Adang EMM, Piek JMJ, van Doorn HC, van Beurden M, Mourits MJE, Zweemer RP, Gaarenstroom KN, Slangen BFM, Vos MC, van Lonkhuijzen LRCW, Massuger LFAG, Hermens RPMG, de Hullu JA (2015) Early salpingectomy (TUbectectomy) with delayed oophorectomy to improve quality of life as alternative for risk-reducing salpingo-oophorectomy in BRCA1/2 mutation carriers (TUBA study): a prospective non-randomised multicentre study. BMC Cancer 15:593
Kim SH, Frey MK, Blank SV (2014) Occult tubal carcinoma found at risk reducing salpingectomy in a BRCA1 carrier. Gynecol Oncol Case Rep 9:1–2
Antoniou A, Pharoah PD, Narod S, Risch HA, Eyfijord 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, Syrjäkoski 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 72:1117–1130
King M-C, Marks JH, Mandell JB, New York Breast Cancer Study Group (2003) Breast and ovarian cancer risks due to inherited mutations in BRCA1 and BRCA2. Science 302:643–646
Rebbeck TR, Friebel T, Wagner T, Lynch HT, Garber JE, Daly MB, Isaacs C, Olopade OI, Neuhausen SL, van’t Veer L, Eeles R, Evans DG, Tomlinson G, Matloff E, Narod SA, Eisen A, Domchek S, Armstrong K, Weber BL, PROSE Study Group (2005) Effect of short-term hormone replacement therapy on breast cancer risk reduction after bilateral prophylactic oophorectomy in BRCA1 and BRCA2 mutation carriers: the PROSE study group. J Clin Oncol 23:7804–7810
Eisen A, Lubinski J, Gronwald J, Moller P, Lynch HT, Klijn J, Kim-Sing C, Neuhausen SL, Gilbert L, Ghadirian P, Manoukian S, Rennert G, Friedman E, Isaacs C, Rosen E, Rosen B, Daly M, Sun P, Narod SA, the Hereditary Breast Cancer Clinical Study Group (2008) Hormone therapy and the risk of breast cancer in BRCA1 mutation carriers. J Natl Cancer Inst 100:1361–1367
Gabriel CA, Tigges-Cardwell J, Stopfer J, Erlichman J, Nathanson K, Domchek SM (2009) Use of total abdominal hysterectomy and hormone replacement therapy in BRCA1 and BRCA2 mutation carriers undergoing risk-reducing salpingo-oophorectomy. Fam Cancer 8:23–28
Foulkes WD, Metcalfe K, Sun P, Hanna WM, Lynch HT, Ghadirian P, Tung N, Olopade OI, Weber BL, McLennan J, Olivotto IA, Bégin LR, Narod SA (2004) Estrogen receptor status in BRCA1- and BRCA2-related breast cancer: the influence of age, grade, and histological type. Clin Cancer Res 10:2029–2034
Eerola H, Heikkilä P, Tamminen A, Aittomäki K, Blomqvist C, Nevanlinna H (2005) Histopathological features of breast tumours in BRCA1, BRCA2 and mutation-negative breast cancer families. Breast Cancer Res 7:R93–R100
Segev Y, Rosen B, Lubinski J, Gronwald J, Lynch HT, Moller P, Kim-Sing C, Ghadirian P, Karlan B, Eng C, Gilchrist D, Neuhausen SL, Eisen A, Friedman E, Euhus D, Ping S, Narod SA, Hereditary Breast Cancer Study Group (2015) Risk factors for endometrial cancer among women with a BRCA1 or BRCA2 mutation: a case control study. Fam Cancer 14:383–391
Beiner ME, Finch A, Rosen B, Lubinski J, Moller P, Ghadirian P, Lynch HT, Friedman E, Sun P, Narod SA, Hereditary Ovarian Cancer Clinical Study Group (2007) The risk of endometrial cancer in women with BRCA1 and BRCA2 mutations. A prospective study. Gynecol Oncol 104:7–10
Segev Y, Iqbal J, Gronwald J, Lynch HT, Moller P, Ghadirian P, Rosen B, Tung N, Kim-Sing C, Foulkes WD, Neuhausen SL, Senter L, Singer CF, Karlan B, Ping S, Narod SA, Hereditary Breast Cancer Study Group (2013) The incidence of endometrial cancer in women with BRCA1 and BRCA2 mutations: an international prospective study. Gynecol Oncol 130:127–131
Narod SA, Pal T, Graham T, Mitchell M, Fyles A (2001) Tamoxifen and risk of endometrial cancer. Lancet 357:65–66
Quinn MA, Benedet JL, Odicino F, Maisonneuve P, Beller U, Creasman WT, Heintz APM, Ngan HYS, Pecorelli S (2006) Carcinoma of the cervix uteri. FIGO 26th annual report on the results of treatment in gynecological cancer. Int J Gynaecol Obstet 95(Suppl 1):S43–S103
Wuttke M, Phillips K-A (2015) Clinical management of women at high risk of breast cancer. Curr Opin Obstet Gynecol 27:6–13
Casey MJ, Bewtra C, Garcia-Padial J, Lynch HT (1995) Laparoscopic examination and assisted bilateral salpingo-oophorectomy hysterectomy for prophylactic removal of the ovaries and uterus in women at genetic risk for ovarian cancer. J Gynecol Tech 1:111–114
Casey MJ, Garcia-Padial J, Hakert D, Watson P (1998) Changing trends in surgical approaches to hysterectomy: an analysis of laparoscopic assisted vaginal hysterectomy in clinical practice. J Gynecol Surg 14:15–24
Finch A, Evans G, Narod SA (2012) BRCA carriers, prophylactic salpingo-oophorectomy and menopause: clinical management considerations and recommendations. Womens Health 8:543–555
Marchetti C, Iadarola R, Palaia I, di Donato V, Perniola G, Muzii L, Panici PB (2014) Hormone therapy in oophorectomized BRCA1/2 mutation carriers. Menopause 21:763–768
Garcia C, Lyon L, Conell C, Littell RD, Powell CB (2015) Osteoporosis risk and management in BRCA1 and BRCA2 carriers who undergo risk-reducing salpingo-oophorectomy. Gynecol Oncol 138:723–726
Cano A, Hermenegildo C (2000) The endometrial effects of SERMs. Hum Reprod Update 6:244–254
Gizzo S, Saccardi C, Patrelli TS, Berretta R, Capobianco G, Di Gangi S, Vacilotto A, Bertocco A, Noventa M, Ancona E, D’Antona D, Nardelli GB (2013) Update on raloxifene: mechanism of action, clinical efficacy, adverse effects, and contraindications. Obstet Gynecol Surv 68:467–481
Author information
Authors and Affiliations
Corresponding author
Additional information
Presented during the Dr. Henry T. Lynch Symposium: Advances in Hereditary Cancer, Omaha, NE, USA, September 17–18, 2015.
Rights and permissions
About this article
Cite this article
Casey, M.J., Colanta, A.B. Müllerian intra-abdominal carcinomatosis in hereditary breast ovarian cancer syndrome: implications for risk-reducing surgery. Familial Cancer 15, 371–384 (2016). https://doi.org/10.1007/s10689-016-9878-4
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10689-016-9878-4