Association of BRCA1/2 mutations with prognosis and surgical cytoreduction outcomes in ovarian cancer patients: An updated meta-analysis.
BRCA mutation
ovarian cancer
surgical cytoreduction
survival
Journal
The journal of obstetrics and gynaecology research
ISSN: 1447-0756
Titre abrégé: J Obstet Gynaecol Res
Pays: Australia
ID NLM: 9612761
Informations de publication
Date de publication:
Sep 2022
Sep 2022
Historique:
revised:
05
04
2022
received:
11
02
2022
accepted:
29
05
2022
pubmed:
15
6
2022
medline:
8
9
2022
entrez:
14
6
2022
Statut:
ppublish
Résumé
This meta-analysis was conducted to evaluate the impact of BRCA mutations on survival outcomes of ovarian cancer patients and assess whether the BRCA status was an independent predictor of complete cytoreduction. We searched the PubMed, Cochrane, EMBASE, Scopus, Web of Science, and Google Scholar databases for studies that evaluated the associations among BRCA mutations, ovarian cancer survival and surgical cytoreduction before August 2021 based on specific inclusion and exclusion criteria. We identified 61 articles that compared the clinical features, survival outcomes, and optimal surgical cytoreduction rates between BRCA-positive patients and BRCA-negative patients. The results showed that BRCA mutation carriers were diagnosed with ovarian cancer at a younger age than the age at which nonmutation carriers were diagnosed. In addition, BRCA mutation carriers were more likely to be in the International Federation of Gynecology and Obstetrics (FIGO) stage III-IV, and the pathological grade was commonly grade 3. The pathological type of BRCA mutation carriers was more likely to be high-grade serous carcinoma. Patients with BRCA mutations had higher response rates to platinum-based chemotherapy than the noncarriers. However, patients in both groups had equivalent rates of surgical cytoreduction, and BRCA-positive patients had longer overall survival (OS) time (HR = 0.65; 95% confidence interval [CI]: 0.59, 0.73; p < 0.001) and longer progression-free survival (PFS) (HR = 0.72; 95% CI: 0.63, 0.82; p < 0.001). BRCA mutations appear to be associated with improved OS and PFS in patients with ovarian cancer. However, we did not find any difference in the surgical resection rate between participants in the two groups.
Substances chimiques
BRCA1 Protein
0
BRCA1 protein, human
0
Types de publication
Journal Article
Meta-Analysis
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
2270-2284Informations de copyright
© 2022 Japan Society of Obstetrics and Gynecology.
Références
Marchetti C, Muzii L, Romito A, Panici PB. First-line treatment of women with advanced ovarian cancer: focus on bevacizumab. Onco Targets Ther. 2019;12:1095-103.
Murphy CG, Moynahan ME. BRCA gene structure and function in tumor suppression: a repair-centric perspective. Cancer J. 2010;16:39-47.
Pearce CL, Stram DO, Ness RB, Stram DA, Roman LD, Templeman C, et al. Population distribution of lifetime risk of ovarian cancer in the United States. Cancer Epidemiol Biomark Prev. 2015;24:671-6.
Antoniou A, Pharoah PD, Narod S, et al. 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. 2003;72:1117-30.
Satagopan JM, Boyd J, Kauff ND, et al. Ovarian cancer risk in Ashkenazi Jewish carriers of BRCA1 and BRCA2 mutations. Clin Cancer Res. 2002;8:3776-81.
Alsop K, Fereday S, Meldrum C, de Fazio A, Emmanuel C, George J, et al. 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. 2012;30:2654-63.
Vencken PMLH, Kriege M, Hoogwerf D, Beugelink S, van der Burg MEL, Hooning MJ, et al. Chemosensitivity and outcome of BRCA1- and BRCA2-associated ovarian cancer patients after first-line chemotherapy compared with sporadic ovarian cancer patients. Ann Oncol. 2011;22:1346-52.
Rudaitis V, Zvirblis T, Kanopiene D, Janulynaite D, Griskevicius L, Janavicius R. BRCA1/2 mutation status is an independent factor of improved survival for advanced (stage III-IV) ovarian cancer. Int J Gynecol Cancer. 2014;24:1395-400.
Gallagher DJ, Konner JA, Bell-McGuinn KM, et al. Survival in epithelial ovarian cancer: a multivariate analysis incorporating BRCA mutation status and platinum sensitivity. Ann Oncol. 2011;22:1127-32.
Chetrit A, Hirsh-Yechezkel G, Ben-David Y, Lubin F, Friedman E, Sadetzki S. Effect of BRCA1/2 mutations on long-term survival of patients with invasive ovarian cancer: the national israeli study of ovarian cancer. J Clin Oncol. 2008;26:20-5.
Yang D, Khan S, Sun Y, Hess K, Shmulevich I, Sood AK, et al. Association of BRCA1 and BRCA2 mutations with survival, chemotherapy sensitivity, and gene mutator phenotype in patients with ovarian cancer. JAMA. 2011;306:1557-65.
Kim SR, Malcolmson J, Li X, Bernardini MQ, Hogen L, May T. The correlation between BRCA status and surgical cytoreduction in high-grade serous ovarian carcinoma. Gynecol Oncol. 2021;162:702-6.
Liberati L, Altman D, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. Ann Intern Med. 2009;151:W65-94.
Oremus M, Oremus C, Hall GBC, McKinnon MC. Inter-rater and test-retest reliability of quality assessments by novice student raters using the Jadad and Newcastle-Ottawa Scales.BMJ Open. 2012;2:e001368.
Parmar MKB, Torri V, Stewart L. Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med. 1998;17:2815-34.
Egger M, Davey Smith G, Schneider M, et al. Bias in metaanalysis detected by a simple, graphical test. BMJ. 1997;315:629-34.
Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50:1088-101.
Toss A, Piombino C, Tenedini E, Bologna A, Gasparini E, Tarantino V, et al. The prognostic and predictive role of somatic BRCA mutations in ovarian cancer: results from a multicenter cohort study. Diagnostics (Basel). 2021;11:565.
Rao Y, Li X, Xu DH, et al. Analysis of BRCA gene mutation status and clinical significance in 74 patients with epithelial ovarian cancer. Int Obstet Gynecol. 2021;48:351-5.
Sunar V, Korkmaz V, Topcu V, Cavdarli B, Arik Z, Ozdal B, et al. Frequency of germline BRCA1/2 mutations and association with clinicopathological characteristics in Turkish women with epithelial ovarian cancer. Asia Pac J Clin Oncol. 2022;18:84-92.
Gorodnova T, Sokolenko A, Ni V, Ivantsov A, Kotiv K, Petrik S, et al. BRCA1-associated and sporadic ovarian carcinomas: outcomes of primary cytoreductive surgery or neoadjuvant chemotherapy. Int J Gynecol Cancer. 2019;29:779-86.
Enomoto T, Aoki D, Hattori K, Jinushi M, Kigawa J, Takeshima N, et al. 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. 2019;29:1043-9.
Tedaldi G, Tebaldi M, Zampiga V, Danesi R, Arcangeli V, Ravegnani M, et al. Multiple-gene panel analysis in a case series of 255 women with hereditary breast and ovarian cancer. Oncotarget. 2017;8:47064-75.
Sirisabya N, Manchana T, Termrungreunglert W, Triratanachat S, Charuruks N, Tresukosol D. Prevalence of BRCA1 expression in epithelial ovarian cancer: immunohistochemical study. J Med Assoc Thail. 2007;90:9-14.
Lakhani SR, Manek S, Penault-Llorca F, Flanagan A, Arnout L, Merrett S, et al. Pathology of ovarian cancers in BRCA1 and BRCA2 carriers. Clin Cancer Res. 2004;10:2473-81.
Buller RE, Shahin MS, Geisler JP, Zogg M, De Young BR, Davis CS. Failure of BRCA1 dysfunction to alter ovarian cancer survival. Clin Cancer Res. 2002;8:1196-202.
Zweemer RP, Verheijen RHM, Coebergh JWW, Jacobs IJ, van Diest PJ, Gille JJP, et al. Survival analysis in familial ovarian cancer, a case control study. Eur J Obstet Gynecol Reprod Biol. 2001;98:219-23.
Boyd J, Sonoda Y, Federici MG, Bogomolniy F, Rhei E, Maresco DL, et al. Clinicopathologic features of BRCA-linked and sporadic ovarian cancer. JAMA. 2000;283:2260-5.
Pharoah PD, Easton DF, Stockton DL, Gayther S, Ponder BA. Survival in familial, BRCA1-associated, and BRCA2-associated epithelial ovarian cancer. United Kingdom coordinating Committee for Cancer Research (UKCCCR) familial ovarian cancer study group. Cancer Res. 1999;59:868-71.
Aida H, Takakuwa K, Nagata H, et al. Clinical features of ovarian cancer in Japanese women with germ-line mutations of BRCA1. Clin Cancer Res. 1998;4:235-40.
Plotti F, Terranova C, Guzzo F, et al. Role of BRCA mutation and HE4 in predicting chemotherapy response in ovarian cancer: a retrospective pilot study. Biomedicine. 2021;9:55.
Somasegar S, Weiss AS, Norquist BM, Khasnavis N, Radke M, Manhardt E, et al. Germline mutations in black patients with ovarian, fallopian tube and primary peritoneal carcinomas. Gynecol Oncol. 2021;163:130-3.
Ashour M, Shafik HE. Frequency of germline mutations in BRCA1 and BRCA2 in ovarian cancer patients and their effect on treatment outcome. Cancer Manag Res. 2019;11:6275-84.
Lee YJ, Kim HS, Rim JH, Lee JY, Nam EJ, Kim SW, et al. Germline BRCA, chemotherapy response scores, and survival in the neoadjuvant treatment of ovarian cancer. BMC Cancer. 2020;20:185.
Lertkhachonsuk AA, Suprasert P, Manchana T, Kittisiam T, Kantathavorn N, Chansoon T, et al. Prevalence of tissue BRCA gene mutation in ovarian, fallopian tube, and primary peritoneal cancers: a multi-institutional study. Asian Pac J Cancer Prev. 2020;21:2381-8.
Shi T, Wang P, Tang W, Jiang R, Yin S, Shi D, et al. Survival benefit of germline BRCA mutation is associated with residual disease in ovarian cancer. Cell Physiol Biochem. 2018;47:2088-96.
Helpman L, Zidan O, Friedman E, Kalfon S, Perri T, Ben-Baruch G, et al. Young Israeli women with epithelial ovarian cancer: prevalence of BRCA mutations and clinical correlates. J Gynecol Oncol. 2017;28:e61.
Eoh KJ, Park HS, Park JS, Lee ST, Han J, Lee JY, et al. Comparison of clinical outcomes of BRCA1/2 pathologic mutation, variants of unknown significance, or wild type epithelial ovarian cancer patients. Cancer Res Treat. 2017;49:408-15.
Synowiec A, Wcisło G, Bodnar L, Górski B, Szenajch J, Szarlej-Wcisło K, et al. Clinical features and outcomes of germline mutation BRCA1-linked versus sporadic ovarian cancer patients. Hered Cancer Clin Pract. 2016;14:1.
Sabatier R, Lavit E, Moretta J, Lambaudie E, Noguchi T, Eisinger F, et al. Ovarian cancer patients at high risk of BRCA mutation: the constitutional genetic characterization does not change prognosis. Familial Cancer. 2016;15:497-506.
Kotsopoulos J, Rosen B, Fan I, Moody J, McLaughlin JR, Risch H, et al. Ten-year survival after epithelial ovarian cancer is not associated with BRCA mutation status. Gynecol Oncol. 2016;140:42-7.
Rzepecka IK, Szafron LM, Stys A, Felisiak-Golabek A, Podgorska A, Timorek A, et al. Prognosis of patients with BRCA1 -associated ovarian carcinomas depends on TP53 accumulation status in tumor cells. Gynecol Oncol. 2017;144:369-76.
Candido-dos-Reis FJ, Song H, Goode EL, Cunningham JM, Fridley BL, Larson MC, et al. Germline mutation in BRCA1 or BRCA2 and ten-year survival for women diagnosed with epithelial ovarian cancer. Clin Cancer Res. 2015;21:652-7.
Biglia N, Sgandurra P, Bounous VE, Maggiorotto F, Piva E, Pivetta E, et al. Ovarian cancer in BRCA1 and BRCA2 gene mutation carriers: analysis of prognostic factors and survival. Ecancermedicalscience. 2016;10:639.
Zhang S, Yuan Y, Hao D. A genomic instability score in discriminating nonequivalent outcomes of BRCA1/2 mutations and in predicting outcomes of ovarian cancer treated with platinum-based chemotherapy. PLoS One. 2014;9:e113169.
Safra T, Lai WC, Borgato L, Nicoletto MO, Berman T, Reich E, et al. BRCA mutations and outcome in epithelial ovarian cancer (EOC): experience in ethnically diverse groups. Ann Oncol. 2013;24:viii63-8.
McLaughlin JR, Rosen B, Moody J, et al. Long-term ovarian cancer survival associated with mutation in BRCA1 or BRCA2. J Natl Cancer Inst. 2013;105:141-8.
Hyman DM, Zhou Q, Iasonos A, Grisham RN, Arnold AG, Phillips MF, et al. Improved survival for BRCA2-associated serous ovarian cancer compared with both BRCA-negative and BRCA1-associated serous ovarian cancer. Cancer. 2012;118:3703-9.
Dann RB, DeLoia JA, Timms KM, et al. BRCA1/2 mutations and expression: response to platinum chemotherapy in patients with advanced stage epithelial ovarian cancer. Gynecol Oncol. 2012;125:677-82.
Reitsma W, de Bock GH, Oosterwijk JC, ten Hoor KA, Hollema H, Mourits MJ. Clinicopathologic characteristics and survival in BRCA1- and BRCA2-related adnexal cancer. Int J Gynecol Cancer. 2012;22:579-85.
Liu G, Yang D, Sun Y, Shmulevich I, Xue F, Sood AK, et al. Differing clinical impact of BRCA1 and BRCA2 mutations in serous ovarian cancer. Pharmacogenomics. 2012;13:1523-35.
Lacour RA, Westin SN, Meyer LA, Wingo SN, Schorge JO, Brooks R, et al. Improved survival in non-Ashkenazi Jewish ovarian cancer patients with BRCA1 and BRCA2 gene mutations. Gynecol Oncol. 2011;121:358-63.
Hennessy BTJ, Timms KM, Carey MS, Gutin A, Meyer LA, Flake DD II, et al. Somatic mutations in BRCA1 and BRCA2 could expand the number of patients that benefit from poly (ADP ribose) polymerase inhibitors in ovarian cancer. J Clin Oncol. 2010;28:3570-6.
Tan DSP, Rothermundt C, Thomas K, Bancroft E, Eeles R, Shanley S, et al. "BRCAness" syndrome in ovarian cancer: a case-control study describing the clinical features and outcome of patients with epithelial ovarian cancer associated with BRCA1 and BRCA2 mutations. J Clin Oncol. 2008;26:5530-6.
Brozek I, Ochman K, Debniak J, Morzuch L, Ratajska M, Stepnowska M, et al. High frequency of BRCA1/2 germline mutations in consecutive ovarian cancer patients in Poland. Gynecol Oncol. 2008;108:433-7.
Soegaard M, Kjaer SK, Cox M, Wozniak E, Høgdall E, Høgdall C, et al. BRCA1 and BRCA2 mutation prevalence and clinical characteristics of a population-based series of ovarian cancer cases from Denmark. Clin Cancer Res. 2008;14:3761-7.
Pal T, Permuth-Wey J, Kapoor R, Cantor A, Sutphen R. Improved survival in BRCA2 carriers with ovarian cancer. Familial Cancer. 2007;6:113-9.
Chiang JW, Karlan BY, Cass L, Baldwin RL. BRCA1 promoter methylation predicts adverse ovarian cancer prognosis. Gynecol Oncol. 2006;101:403-10.
Majdak EJ, Debniak J, Milczek T, Cornelisse CJ, Devilee P, Emerich J, et al. Prognostic impact ofBRCA1 pathogenic andBRCA1/BRCA2 unclassified variant mutations in patients with ovarian carcinoma. Cancer. 2005;104:1004-12.
Cass I, Baldwin RL, Varkey T, Moslehi R, Narod SA, Karlan BY. Improved survival in women with BRCA-associated ovarian carcinoma. Cancer. 2003;97:2187-95.
Ramus SJ, Fishman A, Pharoah PDP, Yarkoni S, Altaras M, Ponder BAJ. Ovarian cancer survival in Ashkenazi Jewish patients with BRCA1 and BRCA2 mutations. Eur J Surg Oncol. 2001;27:278-81.
Szatkowski W, Muzykiewicz K, Jasiówka M, Karolewski K, Kojs Z, Klimek M, et al. Comparison of effectiveness of treatment of patients with sporadic and germline BRCA1-related ovarian cancer. Ginekol Pol. 2016;87:422-5.
Yoo JG, Lee HN, Lee SJ, et al. Germline BRCA2 mutation is associated with greater progression-free survival in korean women with advanced high-grade serous ovarian cancer. Eur J Gynaecol Oncol. 2020;41:675.
Unni SK, Schauerhamer MB, Deka R, Tyczynski JE, Fernandes AW, Stevens V, et al. BRCA testing, treatment patterns and survival in platinum-sensitive recurrent ovarian cancer - an observational cohort study. J Ovarian Res. 2016;9:18.
Adams SF, Marsh EB, Elmasri W, Halberstadt S, VanDecker S, Sammel MD, et al. A high response rate to liposomal doxorubicin is seen among women with BRCA mutations treated for recurrent epithelial ovarian cancer. Gynecol Oncol. 2011;123:486-91.
David YB, Chetrit A, Hirsh-Yechezkel G, et al. Effect of BRCA mutations on the length of survival in epithelial ovarian tumors. J Clin Oncol. 2002;20:463-6.
Rubin SC, Benjamin I, Behbakht K, Takahashi H, Morgan MA, LiVolsi VA, et al. Clinical and pathological features of ovarian cancer in women with germ-line mutations of BRCA1. N Engl J Med. 1996;335:1413-6.
You Y, Li L, Lu J, Wu H, Wang J, Gao J, et al. Germline and somatic BRCA1/2 mutations in 172 Chinese women with epithelial ovarian cancer. Front Oncol. 2020;10:295.
Pennington KP, Walsh T, Harrell MI, Lee MK, Pennil CC, Rendi MH, et al. Germline and somatic mutations in homologous recombination genes predict platinum response and survival in ovarian, fallopian tube, and peritoneal carcinomas. Clin Cancer Res. 2014;20:764-75.
Weberpals J, Garbuio K, O'Brien A, Clark-Knowles K, Doucette S, Antoniouk O, et al. The DNA repair proteins BRCA1 and ERCC1 as predictive markers in sporadic ovarian cancer. Int J Cancer. 2009;124:806-15.
Swisher EM, Gonzalez RM, Taniguchi T, Garcia RL, Walsh T, Goff BA, et al. Methylation and protein expression of DNA repair genes: association with chemotherapy exposure and survival in sporadic ovarian and peritoneal carcinomas. Mol Cancer. 2009;8:48.
Xu K, Yang S, Zhao Y. Prognostic significance of BRCA mutations in ovarian cancer: an updated systematic review with meta-analysis. Oncotarget. 2017;8:285-302.
Huang YW. Association of BRCA1/2 mutations with ovarian cancer prognosis: an updated meta-analysis. Medicine. 2018;97:e9380.
Rimar KJ, Tran PT, Matulewicz RS, Hussain M, Meeks JJ. The emerging role of homologous recombination repair and PARP inhibitors in genitourinary malignancies. Cancer. 2017;123:1912-24.
Riaz N, Blecua P, Lim RS, Shen R, Higginson DS, Weinhold N, et al. Pan-cancer analysis of bi-allelic alterations in homologous recombination DNA repair genes. Nat Commun. 2017;8:857.