Clinicopathologic Characteristics and Survival in BRCA1- and BRCA2-Related Adnexal Cancer

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1 ORIGINAL STUDY Clinicopathologic Characteristics and Survival in BRCA1- and BRCA2-Related Adnexal Cancer Are They Different? Welmoed Reitsma, MD, MSc,* Geertruida H. de Bock, MD, PhD,Þ Jan C. Oosterwijk, MD, PhD,þ Klaske A. ten Hoor, BSc,* Harry Hollema, MD, PhD, and Marian J. E. Mourits, MD, PhD* Objective: Our aim was to examine the clinicopathologic characteristics and survival of ovarian, tubal, and peritoneal (further denoted adnexal ) cancer in BRCA1 compared with BRCA2 carriers. Methods: A consecutive series of adnexal cancers in BRCA1/2 mutation carriers diagnosed in 1980 to 2010 at the University Medical Center Groningen was analyzed. Results: We evaluated 55 BRCA1- and 16 BRCA2-related adnexal cancers, consisting of 51 ovarian, 13 tubal, and 7 peritoneal cancers. Peritoneal cancer was restricted to BRCA1 carriers. Ovarian and tubal cancer was equally present in both carrier groups. Median age at diagnosis was younger in BRCA1 compared with BRCA2 carriers (50 vs 54 years; P = 0.03). No other clinicopathologic differences were found. Regarding survival, a nonsignificant trend was noted for BRCA2 carriers to have fewer relapses, a longer time to first relapse, and a longer disease-free and overall survival. Conclusions: Except for age at diagnosis and prevalence of peritoneal cancer, no significant clinicopathologic differences were found between BRCA1- versus BRCA2-associated adnexal cancer. On survival, it might be suggested that BRCA2 carriers have a more favorable outcome than BRCA1 carriers, marked by fewer relapses, a longer time to first relapse, and a longer disease-free and overall survival. Key Words: BRCA, Clinicopathologic features, Ovarian cancer, Survival, Tumor characteristics Received September 5, 2011, and in revised form October 11, Accepted for publication October 14, (Int J Gynecol Cancer 2012;22: 579Y585) pproximately 13% of all ovarian cancers are associated with an autosomal dominant genetic predisposition, A of which BRCA germ-line mutations contribute to at least 90% of these cases. 1,2 Two large meta-analyses have been conducted to estimate the cumulative risk for BRCA1 and BRCA2 carriers of developing ovarian cancer. Antoniou et al 3 compared 22 studies and found a cumulative ovarian cancer risk of 39% (95% confidence interval [CI], 18%Y54%) in BRCA1 and 11% (95% CI, 2.4%Y19%) in BRCA2 carriers by the age of 70 years. Chen and Parmigiani 4 performed *Division of Gynecologic Oncology, Departments of Obstetrics and Gynecology, Epidemiology, Clinical Genetics, and Pathology, University Medical Center Groningen, The University of Groningen, Groningen, the Netherlands. Address correspondence and reprint requests to Marian J. E. Mourits, MD, PhD, Department of Gynecologic Oncology, University Medical Center Groningen, The University of Groningen, Copyright * 2012 by IGCS and ESGO ISSN: X DOI: /IGC.0b013e31823d1b5c Hanzeplein 1, 9700 RB Groningen, the Netherlands. m.j.e.mourits@umcg.nl. Financial support was not received for this study. The authors report no conflicts of interests. Contributors: all authors have made substantial contributions to this manuscript. According to Dutch law, this study did not require approval from the institutional review board of the University Medical Center Groningen. Technical appendix, statistical code, and data set are available from the corresponding author. International Journal of Gynecological Cancer & Volume 22, Number 4, May

2 Reitsma et al International Journal of Gynecological Cancer & Volume 22, Number 4, May 2012 a meta-analysis of 10 studies and estimated the cumulative ovarian cancer risk to be 40% (95% CI, 35%Y46%) in BRCA1 and 18% (95% CI, 13%Y23%) in BRCA2 carriers by age 70 years. In addition to breast and ovarian cancer, women with BRCA1/2 mutations are also known to be at risk for tubal and peritoneal cancer. In case of a diagnosis of tubal cancer, a BRCA1 mutation is to be found in 11% to 39% and a BRCA2 mutation in 4% to 5% of the cases. 5,6 The fallopian tube is currently being suggested as the primary source of most, if not all, ovarian, tubal, and peritoneal (further denoted adnexal ) cancers in BRCA1/2 carriers. Adnexal cancers in BRCA1/2 carriers have been compared with sporadic cases. Typically, BRCA-related adnexal cancers are of a more advanced stage, respond better to platinum-based chemotherapy, show longer treatment-free intervals between relapses, have distinct patterns of metastasis, and show a better overall survival (OS) when compared with sporadic cases. 7Y9 As a group, BRCA-related adnexal cancers receive the same diagnostic and treatment strategies. However, the distinct disease penetrance between BRCA1 and BRCA2 cancers might suggest or even require a distinct approach to both carrier groups. With regard to breast cancer, the majority of BRCA1- related cancers are triple-negative: clinically lacking the expression of estrogen and progesterone receptors and HER2 protein, in contrast to BRCA2 cases. 10 In view of a penetrance difference of BRCA1 compared with BRCA2-related adnexal cancer, and in analogy to breast cancer with a distinct clinicopathologic profile of BRCA1 versus BRCA2 carriers, one might expect clinicopathologic differences in adnexal cancer. Little is known about possible differences in clinicopathologic characteristics or survival between BRCA1-andBRCA2- related adnexal cancer. The aim of this study was to ascertain the nature of any differences between BRCA1 and BRCA2 adnexal cancers. METHODS Study Design In this cohort study, a consecutive series of BRCA1- and BRCA2-related adnexal cancers were evaluated, based on clinical and histopathologic characteristics and survival rates. Included were women with a diagnosis of primary ovarian, tubal, or peritoneal cancer at the University Medical Center Groningen between January 1980 and December Only cancers from women with a pathogenic BRCA1 of BRCA2 germline mutation detected before or after diagnosis of adnexal cancer were included. Context of Care Women with adnexal cancer were treated according to the Dutch guideline, based on the International Federation of Gynecology and Obstetrics (FIGO) guidelines. Treatment usually included surgery (primary debulking or interval debulking) and platinum-based chemotherapy (in combination with paclitaxel after 1996). BRCA1/2 testing was done in the course of genetic counseling, if the woman met the national testing criteria. Follow-up visits after completing treatment 580 were performed alternating between a gynecologic oncologist and a medical oncologist at the University Medical Center Groningen outpatient department. Regular physical and gynecologic examination combined with serum CA-125 measurements were conducted by a gynecologic oncologist. Visits were scheduled every 3 months for the first 2 years, 6 months in the 3rd until the 5th year, and once a year in the 6th to 10th year after diagnosis of adnexal cancer. Data Collection Clinical, histopathologic, genetic, and follow-up data were retrieved from medical records, surgical reports, and pathology reports using a structured electronic registration form and were entered into an anonymous, password-protected database. Protection of the patient s identity was guaranteed by assigning study-specific, unique patient numbers. According to Dutch law, no further Institutional review board approval was needed for this study. Outcome Measurements Clinical characteristics evaluated in the analyses were age at diagnosis, completeness of primary debulking, completeness of interval debulking, type of first-line chemotherapy, response to first-line chemotherapy, time to first recurrence, and the occurrence of platinum-resistant disease. Histopathologic characteristics in the evaluation were tumor localization, unilateral or bilateral disease, stage, histological subtype, and grade of differentiation. Follow-up data concerned total follow-up time, relapsing disease, time to first relapse, disease-free survival (DFS), and OS. Data Definition Surgical stage, histological tumor type, and grade of differentiation were defined according to the FIGO nomenclature (Rio de Janeiro, 1988) and World Health Organization standards. The diagnosis of ovarian versus fallopian tube versus peritoneal cancer was reviewed centrally in this study by an experienced gynecopathologist. Ovarian cancer is diagnosed when the cancer predominantly grows in the ovarian epithelium, and no in situ cancer is detected in the fallopian tube. Cancer is considered to be of tubal origin when the tumor predominantly grows in the fallopian tube epithelium, when transition from dysplasia to invasive carcinoma is present, or if a tubal carcinoma in situ is observed. 11 Peritoneal cancer is diagnosed when the cancer grows on peritoneal surfaces and/or the omentum, without cancer in the fallopian tubes or the ovaries, and in situ lesions are absent. The predominant pattern of histological grade or cell type was used for categorization in case of histopathologically mixed tumors. Response to surgery and chemotherapy were evaluated and categorized according to the Response Evaluation Criteria In Solid Tumors. The data are presented as best response. Platinum-resistant disease was defined by recurrence of 6 months or less after completion of treatment. Disease-free survival was calculated from time of diagnosis to time of recurrence, and OS from time of diagnosis to time of death or last follow-up. Death of disease was defined as death as a result of progressive disease, recurrence, or treatment-related complications. * 2012 IGCS and ESGO

3 International Journal of Gynecological Cancer & Volume 22, Number 4, May 2012 Adnexal Cancer: BRCA1 Versus BRCA2 Statistical Analyses Data analyses were performed using SPSS statistical package for Windows version 18.0 (SPSS, Chicago, IL). Data were stratified according to mutation type (BRCA1 or BRCA2). For the baseline assessments, descriptive statistics were calculated. Variables were expressed as frequencies and percentages for discrete data and as median and range for continues data. Differences in clinicopathologic characteristics between both carrier groups were tested with the W 2 test (and Fisher exact test) for discrete variables and with the Mann-Whitney U test (and Kruskal-Wallis test) for continues data. Duration of follow-up was calculated for each mutation carrier. Cumulative survival was calculated using the Kaplan- Meier method. To test whether the effect of mutation type on survival (DFS and OS) was independent of the clinicopathologic profile, a bivariate Cox proportional hazards model was performed. All tests were performed with a 2-sided 95% CI. P G 0.05 was considered statistically significant. RESULTS We evaluated 71 adnexal cancers, consisting of 55 BRCA1- and 16 BRCA2-related tumors, diagnosed between January 1980 and December The main characteristics of the patients are listed in Table 1. Adnexal cancer was diagnosed at a significantly earlier age in BRCA1 mutation carriers (median, 50 years; range, 36Y72 years) compared with BRCA2 carriers (median, 54; range, 29Y76 years; P = 0.03). At time of adnexal cancer diagnosis, 46% (33/71) of all carriers had a history of breast cancer, with no significant difference between both carrier groups (46% vs 50%). Twenty-eight breast cancers were unilateral, and 6 were bilateral. All 33 patients were initially treated with a breastconserving therapy or mastectomy; 9 of 33 patients were additionally treated with chemotherapy, and 8 of 33 received hormonal therapy. The median age at diagnosis of first breast cancer was significantly younger for BRCA1 (43 years; range, 24Y69 years) compared with BRCA2-related cases (50 years; range, years; P = 0.03). Histopathologic data are summarized in Table 2. The total group of adnexal cancers consisted of 51 ovarian cancers (72%), 13 tubal cancers (18%), and 7 peritoneal cancers (10%). The occurrence of ovarian or tubal cancer was equal in both carrier groups (P = 0.28), but peritoneal cancer was restricted to BRCA1 carriers. Adnexal cancer was predominantly of serous histology (63%; 45/71) and poor differentiation (87%; 62/71), without difference between both carrier groups. More BRCA2-associated cancers were assigned to be of tubal origin compared with BRCA1 (31% vs 15%), and more tumors were unilateral (63% vs 40%), although not significant. In asymptomatic BRCA1 carriers, 7 cancers were detected at risk-reducing salpingo-oophorectomy (RRSO), and 7 cancers were detected during screening. Because 6 of 7 screen-detected cancers were of advanced stage (FIGO III/IV) versus 1 of 7 cancers detected at RRSO, this further supports the lack of utility of screening for early detection of ovarian cancer. One BRCA1 cancer was coincidentally found during another surgical procedure (FIGO III). In BRCA2 carriers, 2 cancers were found by coincidence during abdominal surgery (FIGO I/II), and no cancers were found at RRSO. Table 3 summarizes treatment-related data for both carrier groups. Primary surgical debulking (cytoreduction) was performed in 93% (51/55) of BRCA1 carriers and 75% (12/16) of BRCA2 carriers (P = 0.07) and was complete in 51% (26/51) of the BRCA1 and 50% (6/12) of the BRCA2 carriers. Neoadjuvant chemotherapy was the primary treatment in the remaining 8 patients, having a stage IV disease. Almost all women (96%) underwent first-line chemotherapy, which was platinum based in all cases. Platinum resistance TABLE 1. Patient characteristics in BRCA1- and BRCA2-related adnexal cancer (n = 71) BRCA1 (n = 55), n (%) BRCA2 (n = 16), n (%) P Age at diagnosis adnexal cancer, median (range), y 50 (36Y72) 54 (29Y76) 0.03* Year of diagnosis adnexal cancer 1980Y (9.1) 1 (6.3) Y (35) 4 (25) 2000Y (56) 11 (69) Mutation analysis Before adnexal cancer diagnosis 25 (45) 5 (31) 0.40 After adnexal cancer diagnosis 30 (55) 11 (69) Previous breast cancer at time of adnexal cancer No 30 (54) 8 (50) 0.78 Yes 25 (46) 8 (50) Unilateral 19 (76) 8 (100) 0.30 Bilateral 6 (24) 0 (0.0) Age at diagnosis of first breast cancer, median (range), y 43 (24Y69) 50 (45Y76) 0.03* *P G 0.05 is significant. * 2012 IGCS and ESGO 581

4 Reitsma et al International Journal of Gynecological Cancer & Volume 22, Number 4, May 2012 TABLE 2. Tumor characteristics of BRCA1- and BRCA2-related adnexal cancer (n = 71) BRCA1 (n = 55), n (%) BRCA2 (n = 16), n (%) Localization of primary tumor Ovary 40 (73) 11 (69) 0.28 Fallopian tube 8 (15) 5 (31) Peritoneum 7 (13) 0 (0.0) Lateralization (ovarian/tubal n = 64) Unilateral 19 (40) 10 (63) 0.13 Bilateral 23 (48) 4 (25) Unknown 6 (13) 2 (13) Stage (FIGO) I/II 14 (26) 7 (44) 0.21 III/IV 41 (75) 9 (56) Histological subtype Serous 35 (64) 10 (63) 0.59 Mucinous 1 (1.8) 1 (6.3) Endometrioid 1 (1.8) 1 (6.3) Clear cell 0 (0.0) 0 (0.0) Mixed 1 (1.8) 1 (6.3) Adenocarcinoma, 17 (31) 3 (19) undifferentiated Grade 2 (Moderately differentiated) 7 (13) 2 (13) (Poorly differentiated) 48 (87) 14 (88) after first-line chemotherapy occurred in 4 of 67 patients (6.0%; 3 BRCA1; 1 BRCA2). Thirty-four women underwent second-line chemotherapy, of whom 26 received platinumbased chemotherapy for first recurrence and 7 (27%) were platinum resistant (5 BRCA1; 2 BRCA2). Table 4 summarizes follow-up data. The total follow-up was 6238 months (520 years), with a median follow-up per woman of 65 months (range, 1Y412 months). No statistically significant differences were found regarding relapsing disease, time to first relapse, DFS, and OS. Relapsing disease occurred in 54% of the patients (38/71), more often in BRCA1 (58%) than in BRCA2 carriers (38%; P = 0.17). When adjusted for stage at presentation, there was no statistical significant difference found between BRCA2- and BRCA2- associated adnexal cancers regarding recurrence rates. The median time to first relapse was 25 months (range, 3Y96 months) in BRCA1 compared with 42 months (range, 9Y95 months) in BRCA2 carriers (P = 0.46). In the 38 women who had relapsing disease, DFS was longer in the BRCA2 as compared with the BRCA1 group, 95 and 65 months, respectively, although not significant (P = 0.34). Overall survival was 71 and 116 months in BRCA1 and BRCA2 carriers, respectively (P = 0.56). During the study period, 37 women died (52%), of whom 31 of 55 were BRCA1 (56%) and 6 of 582 P 16 were BRCA2 carriers (38%; P = 0.26). Ninety-two percent (34/37) of them died of a FIGO III/IV tumor; 3 women had an early-stage tumor. Although not statistically significant, the Kaplan-Meier curves of DFS (Fig. 1) and OS (Fig. 2) showed a more favorable course for BRCA2 compared with BRCA1 carriers. No difference was seen between BRCA1 and BRCA2, when the cases were stratified for a certain clinical or histopathologic characteristic (as listed in Tables 2 and 3) on survival (DFS and OS). Data are not displayed in the tables. DISCUSSION In this consecutive series of 55 BRCA1- and 16 BRCA2- related adnexal cancers, the median age at diagnosis of adnexal cancer was significantly younger in BRCA1 compared with BRCA2 mutation carriers, and peritoneal cancer was exclusively found in BRCA1 mutation carriers. No other clinicopathologic differences were found. Concerning survival, it might be hypothesized that BRCA2 carriers have a more favorable outcome compared with BRCA1 carriers, considering the fewer relapses in BRCA2 carriers, the longer time to first relapse, and the longer DFS and OS, although not significantly. In line with previous studies, adnexal cancer was diagnosed at a significantly earlier age in BRCA1 compared with BRCA2 carriers (50 vs 54 years; P = 0.03). A similar correlation was found for the age at previous breast cancer (43 vs 50 years; P = 0.03), also a well-established finding. The primary tumor localization in BRCA1- and BRCA2-related adnexal cancer concerned the ovaries in, respectively, 73% and 69% of the cases, and the fallopian tube in 15% and 31% (P = 0.28). As the primary origin of the tumor in advanced cases is often not distinguishable, the exact percentage of cancers arising in the ovaries or fallopian tubes has not been ascertained. Werness et al 12 described 70 BRCA1- and 16 BRCA2-related adnexal cancers, of which, respectively, 99% and 94% of the cancers were designated as ovarian. Remarkably, no tubal carcinomas were described in this study, which might be explained by the high proportion (76%) of advanced-stage disease. Piek et al 13 examined 47 BRCA1/2-related adnexal cancers, of which 89% were assigned to be of ovarian origin, 6.3% of tubal origin, and 4.3% of peritoneal origin. All adnexal cancers were predominantly advanced stage, and the authors did not distinguish between BRCA1 and BRCA2 mutation. The diagnosis of ovarian versus fallopian tube versus peritoneal cancer is often difficult to recall as most tumors are detected in an advanced stage. Moreover, the distinction has been poorly defined, which is likely to affect the interpretation of published literature. Advanced-stage cancers are often classified as ovarian because both the ovaries and fallopian tubes are involved, and precursor lesions are no longer detectable. However, the fallopian tube is emerging as an important site of origin, especially in hereditary cases. 14 In fact, several studies on RRSO specimens have demonstrated a cancer source in the distal fallopian tube in 27% up to 100%. 13,15,16 In our series, 18% of the adnexal cancers could be identified as primary tubal carcinoma. Forty-six percent (6/13) of the tubal cancers were early stage (FIGO I/II) * 2012 IGCS and ESGO

5 International Journal of Gynecological Cancer & Volume 22, Number 4, May 2012 Adnexal Cancer: BRCA1 Versus BRCA2 TABLE 3. Clinical characteristics of BRCA1- and BRCA2-related adnexal cancer (n = 71) BRCA1 (n = 55), n (%) BRCA2 (n = 16), n (%) P Primary debulking (n = 63) Complete 26 (51) 6 (50) 0.71 Incomplete 25 (49) 6 (50) Interval debulking (n = 21) Complete 6 (46) 7 (88) 0.09 Incomplete 7 (54) 1 (13) Chemotherapy (first line; n = 68) Platinum with paclitaxel 36 (69) 13 (81) 0.48 Platinum without paclitaxel 16 (31) 3 (19) NonYplatinum-based chemotherapy 0 (0.0) 0 (0.0) Chemotherapy (second line; n = 34) Platinum with paclitaxel 9 (33) 3 (43) 0.89 Platinum without paclitaxel 12 (44) 2 (29) NonYplatinum-based chemotherapy 6 (22) 2 (29) Primary disease platinum resistant (n = 67) Yes 3 (5.9) 1 (6.3) 0.67 No 48 (94) 15 (94) First recurrence platinum resistant (n = 26) Yes 5 (24) 2 (40) 0.41 No 16 (76) 3 (60) Three BRCA1 carriers and 1 BRCA2 carrier did not receive chemotherapy because the disease was stage FIGO I. compared with 28% (14/51) of the ovarian cancers, which corresponds with the suggestion of adnexal cancer originating in the fallopian tube. Seven primary peritoneal cancers were diagnosed in this series; all occurred in BRCA1 mutation carriers (7/55; 13%). Peritoneal cancer is a rare presentation of adenocarcinoma, histologically identical to papillary serous ovarian cancer, and has been reported mainly in women with a BRCA mutation. 17,18 Possibly, peritoneal cancer is metastatic from tubal intraepithelial carcinoma: in nearly one half of the peritoneal cancers, TABLE 4. Follow-up BRCA1 (n = 55), n (%) BRCA2 (n = 16), n (%) P Follow-up, mo Median (range) 65 (1Y412) 53 (8Y307) 0.43 Total Relapse 32 (58) 6 (38) 0.17 Median time from diagnosis to first relapse, mo (n = 38) 25 (3Y96) 42 (9Y95) 0.46 Patients status at last hospital visit Alive 24 (44) 10 (63) 0.26 Diseased 31 (56) 6 (38) Death of disease 28 (90) 2 (33) Death of other malignancy 1 (3.2) 2 (33) Death, cause unknown 2 (6.5) 2 (33) DFS, median (range), mo (n = 38) 65 (23Y107) 95 (not calculable) 0.34 OS, median (range), mo 71 (43Y99) 116 (41Y191) 0.56 Because of the small sample size of BRCA2 carriers and the even smaller number of events in the DFS analysis, the 95% CI was not calculable. * 2012 IGCS and ESGO 583

6 Reitsma et al International Journal of Gynecological Cancer & Volume 22, Number 4, May 2012 FIGURE 1. Cumulative DFS probability (months) of patients with BRCA1 (n = 55) versus BRCA2-related adnexal cancer (n = 16; P = 0.34). it is suggested that the fimbrial end of the fallopian tube is the source. 19 Incidence of primary peritoneal cancer remains unclear; however, this cancer is more often diagnosed in BRCA1 than BRCA2 carriers. 17,18,20 Our finding of 7 peritoneal cancers only in BRCA1 and none in BRCA2 carriers is intriguing and may suggest that peritoneal cancer predominantly (or exclusively) occurs in BRCA1 carriers. However, given the rate of peritoneal cancer reported in this series for BRCA1 carriers (7/55; 13%), one would expect only 2 of 16 cases for BRCA2 carriers. Therefore, because of the small sample size of our study, the complete absence of BRCA2-related peritoneal cancers might be due to chance alone. Occurrence of peritoneal and tubal cancer in BRCA1 and BRCA2 carriers is worthy of follow-up in larger, collaborative studies. No significant differences in histological characteristics between both carrier groups were found. Lakhani et al 21 compared 178 BRCA1- with 29 BRCA2-related ovarian cancers but found no statistical difference in histological subtype. Also, Vencken et al 9 found no histopathologic differences (tumor grade, FIGO stage, and histology) between 99 BRCA1- and 13 BRCA2-related ovarian cancers. A nonsignificant trend was noted to a more favorable outcome of BRCA2 carriers with fewer relapses (38% vs 58%) and a longer time to first relapse (42 vs 25 months). Also, Vencken et al 9 described fewer relapses for BRCA2- than BRCA1-related ovarian cancer. A somewhat better DFS (65 vs 95 months, P = 0.34) and OS (71 vs 116 months, P = 0.56) were seen for BRCA2 compared with BRCA1 female mutation carriers. The survival analysis of Byrd et al 22 reports the largest series of BRCA2 ovarian cancer cases (N = 48) that has ever been compared with BRCA1. They found a significant better survival in proven BRCA2 carriers over proven BRCA1 carriers. The survival benefit for proven BRCA2 carriers with ovarian cancer is in accordance with the trend we see in our study. The chemosensitivity study by Vencken et al 9 between BRCA1 and BRCA2 ovarian cancer patients revealed 584 a trend to a longer DFS and OS for BRCA2 compared with BRCA1 ovarian cancer patients. Pharoah et al, 23 however, found no difference in survival between BRCA1 vs BRCA2 ovarian cancer cases (P = 0.91). Stage at presentation is the main influence on OS in adnexal cancer. 24 The majority (70%) of our patients presented with advanced-stage disease, with no significant difference between the BRCA1 (75%) and BRCA2 (56%) group. Therefore, it is unlikely that a survival benefit in BRCA2 carriers is related to any substantial effect of diagnosis of early-stage disease. However, Byrd et al 22 showed a highly significant better survival in BRCA2-related early-stage ovarian cancer compared with that in BRCA1, although the long-term outlook for advanced-stage disease was similar across both carrier groups (65% of BRCA1-related ovarian cancer being advanced stage and 73% of BRCA2). As our sample size of BRCA2-related ovarian cancer was relatively small, we could not perform a subanalysis on stage. Strengths of this study are the clearly defined consecutive series of proven BRCA1 and BRCA2 carriers, diagnosis within a single-center institution, and the availability of follow-up for all patients over a long period. Limitations are the rather small number of BRCA2-related cases and the retrospective nature of the study. In conclusion, except for age at diagnosis and prevalence of peritoneal cancer, no significant clinicopathologic or survival differences were found between BRCA1- versus BRCA2-associated adnexal cancer. Possibly, there are no differences at clinicopathologic level other than the already wellestablished higher age-specific penetrance in BRCA1 ovarian cancer, the higher proportion of BRCA1 carriers compared with BRCA2 found in tubal cancer. Our study has shown a nonsignificant trend in BRCA2 carriers to fewer relapses, a longer time to first relapse, and a longer DFS and OS. Although this trend was not significant, it might indicate that our sample was too small to demonstrate such differences. FIGURE 2. Cumulative OS probability (in months) of patients with BRCA1- (n = 55) versus BRCA2-related adnexal cancer (n = 16; P = 0.56). * 2012 IGCS and ESGO

7 International Journal of Gynecological Cancer & Volume 22, Number 4, May 2012 Adnexal Cancer: BRCA1 Versus BRCA2 Future research of a larger series of BRCA1 and BRCA2 carriers is warranted to strengthen the statistical significance of both phenotypes. ACKNOWLEDGEMENTS The authors thank Ms Ryanne S. Hijmans, medical student at the University of Groningen, for contributing to the retrieval of a part of the patient data. REFERENCES 1. Claus EB, Schildkraut JM, Thompson WD, et al. The genetic attributable risk of breast and ovarian cancer. Cancer. 1996;77:2318Y Zhang S, Royer R, Li S, et al. Frequencies of BRCA1 and BRCA2 mutations among 1,342 unselected patients with invasive ovarian cancer. Gynecol Oncol. 2011;121:353Y 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;72:1117Y Chen S, Parmigiani G. Meta-analysis of BRCA1 and BRCA2 penetrance. J Clin Oncol. 2007;25:1329Y Aziz S, Kuperstein G, Rosen B, et al. A genetic epidemiological study of carcinoma of the fallopian tube. Gynecol Oncol. 2001;80:341Y Cass I, Holschneider C, Datta N, et al. BRCA-mutation-associated fallopian tube carcinoma: a distinct clinical phenotype? Obstet Gynecol. 2005;106:1327Y Boyd J, Sonoda Y, Federici MG, et al. Clinicopathologic features of BRCA-associated and sporadic ovarian cancer. JAMA. 2000;283:2260Y Cass I, Baldwin RL, Varkey T, et al. Improved survival in women with BRCA-associated ovarian carcinoma. Cancer. 2003;97:2187Y Vencken PM, Kriege M, Hoogwerf D, 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;22:1346Y Rijnsburger AJ, Obdeijn IM, Kaas R, et al. BRCA1-associated breast cancers present differently from BRCA2-associated and familial cases: long-term follow-up of the Dutch MRISC Screening Study. J Clin Oncol. 2010;28:5265Y Woolas R, Smith J, Saharnis P, et al. Fallopian tube carcinoma: an under-recognized primary neoplasm. Int J Gynecol Cancer. 1997;7:284Y 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. 2004;23:29Y Piek JM, Torrenga B, Hermsen B, et al. Histopathological characteristics of BRCA1- and BRCA2-associated intraperitoneal cancer: a clinic-based study. Fam Cancer. 2003;2:73Y Jarboe EA, Folkins AK, Drapkin R, et al. Tubal and ovarian pathways to pelvic epithelial cancer: a pathological perspective. Histopathology. 2008;53:127Y Finch A, Shaw P, Rosen B, et al. Clinical and pathologic findings of prophylactic salpingo-oophorectomies in 159 BRCA1 and BRCA2 carriers. Gynecol Oncol. 2006;100:58Y Callahan MJ, Crum CP, Medeiros F, et al. Primary fallopian tube malignancies in BRCA-positive women undergoing surgery for ovarian cancer risk reduction. J Clin Oncol. 2007;25:3985Y Rebbeck TR, Lynch HT, Neuhausen SL, et al. Prophylactic oophorectomy in carriers of BRCA1 or BRCA2 mutations. N Engl J Med. 2002;346:1616Y Casey MJ, Synder C, Bewtra C, et al. Intra-abdominal carcinomatosis after prophylactic oophorectomy in women of hereditary breast ovarian cancer syndrome kindreds associated with BRCA1 and BRCA2 mutations. Gynecol Oncol. 2005;97:457Y Seidman JD, Zhao P, Yemelyanova A. 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. 2011;120:470Y Olivier RI, Lubsen-Brandsma LA, van Boven H, et al. Additional salpingectomy after previous prophylactic oophorectomy in high-risk women: sense or nonsense? Gynecol Oncol. 2005;96:439Y Lakhani SR, Manek S, Penault-Llorca F, et al. Pathology of ovarian cancers in BRCA1 and BRCA2 carriers. Clin Cancer Res. 2004;10:2473Y Byrd LM, Shenton A, Maher ER, et al. Better life expectancy in women with BRCA2 compared with BRCA1 mutations is attributable to lower frequency and later onset of ovarian cancer. Cancer Epidemiol Biomarkers Prev. 2008;17: 1535Y Pharoah PD, Easton DF, Stockton DL, et al. 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;59:868Y Board RE, Bruijns CT, Pronk AE, et al. Stage- and CA125-related survival in patients with epithelial ovarian cancer treated at a cancer center. Int J Gynecol Cancer. 2006;16(suppl 1):18Y24. For the complete list of references, please contact m.j.e.mourits@ umcg.nl. * 2012 IGCS and ESGO 585

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