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Ovarian Cystadenoma As a Characteristic Feature of Families with Hereditary Ovarian Cancers Unassociated with BRCA1 and BRCA2 Mutations

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Ovarian Cystadenoma As a Characteristic Feature of Families with Hereditary Ovarian Cancers Unassociated with BRCA1 and BRCA2 Mutations J. Appl. Genet. 45(2), 2004, pp. 255-263 Ovarian cystadenoma as a characteristic feature of families with hereditary ovarian cancers unassociated with BRCA1 and BRCA2 mutations Janusz MENKISZAK1, Marek BRZOSKO3, Bohdan GÓRSKI2, Jacek FLICIÑSKI3, Anna JAKUBOWSKA2, Dariusz ¯EBIE£OWICZ5, Jacek GRONWALD2, Tomasz HUZARSKI2, Tomasz BYRSKI2, Leszek TERESIÑSKI4, Maria CHOSIA4, Izabella RZEPKA-GÓRSKA1, Jan LUBIÑSKI2 1Chair and Department of Surgical Gynecology and Gynecological Oncology of Adults and Adolescents and 2Hereditary Cancer Center, Department of Genetics and Pathology and 3Department of Rheumatology and 4Department of Pathology and 5Chair and Department of Obstetrics and Perinatology, Pomeranian Medical University, Szczecin, Poland Abstract. The study aimed to determine whether hereditary ovarian cancers that are not caused by BRCA1/BRCA2 constitutional mutations are associated with a predisposition to cystadenoma. The study consisted of two parts. Part one concerned the incidence of ovarian cystadenoma in females from families with hereditary ovarian cancer unassociated with BRCA1 mutations. The study group included 62 female patients from 29 families, without any previously diagnosed malignancy, with no proven constitutional mutation of the BRCA1 gene. The first control group was composed of 62 female patients from 53 families, without any previously diagnosed malignancy, with an identified constitutional mutation of the BRCA1 gene. The second control group comprised 124 female patients for whom the only reason for the examination was a prophylactic check-up. All studied women were subjected to intravaginal ultra- sonographic investigations. In 8 patients with benign and/or borderline ovarian cystadenoma, a complete sequencing of coding fragments of the BRCA2 gene from the peripheral blood DNA was performed. Part two of this study concerned the incidence and pattern of malignant tumors in the families of female patients with ovarian cystadenoma. The final study group included 117 patients who had 726 I0 relatives (359 females and 367 males). We concluded that cystadenoma is likely to be a characteristic feature of the subgroup of families with hereditary ovarian cancers unassociated with BRCA1/BRCA2 constitutional mutations. Key words: hereditary ovarian cancer, ovarian cystadenoma. Received: January 20, 2003. Revised: December 17, 2003. Accepted: February 4, 2004. Correspondence: J. MENKISZAK, Chair and Department of Surgical Gynecology and Gynecological Oncology of Adults and Adolescents, Pomeranian Medical University, Al. Powstañców Wielkopolskich 72, 70-111 Szczecin, Poland, e-mail: [email protected] 256 J. Menkiszak et al. Introduction Cystadenoma, a benign epithelial tumor of the ovary, may undergo malignant transformation in some cases, which leads to cystadenocarcinoma (DUTT, BERNEY 2000, ELTABBAKH et al. 1999, HONG et al. 1998, SEIDMAN,KURMAN 1996). So far, it has been confirmed that hereditary ovarian cancers develop most frequently in BRCA1 or BRCA2 gene mutation carriers. However, in a substantial proportion of familial ovarian cancers, no cases of constitutional mutations of BRCA1 or BRCA2 genes have been found (MENKISZAK et al. 2003). Moreover, the majority of patients with cystadenoma do not carry any BRCA1 or BRCA2 mu- tations (RISCH et al. 2001). This study aimed to determine whether the predisposi- tion to cystadenoma is related to hereditary ovarian cancers unassociated with BRCA1/BRCA2 constitutional mutations. Material and methods Part one incidence of ovarian cystadenoma in females from families with hereditary ovarian cancer unassociated with BRCA1mutations The study group included 62 female patients from 29 families, without any previ- ously diagnosed malignancy, with no identified constitutional mutation of the BRCA1 gene. The first control group comprised 62 female patients from 53 families, without any previously diagnosed malignancy, with an identified constitutional mutation of BRCA1 gene. The second control group was composed of 124 female patients from various workplaces of the city of Szczecin, for whom the only reason for the examination was a prophylactic check-up. The patients from the study group and from the first control group were consecutive patients of the Hereditary Cancer Center in Szczecin. The mean age in the study group was 43.6 years. The study group and both control groups were matched with respect to age ±2 years, with group size ratios 1:1and1:2,respectively. All studied women were subjected to intravaginal ultrasonographic investiga- tions with a 7.0 MHz frequency transducer and 3535 type medical diagnostic ul- trasound system (serial no. 1635620, Bruel & Kjaer, Denmark), and in cases of suspected pathology – additionally with a C125 transducer (color Doppler) and 128XP/10 model medical diagnostic ultrasound system (serial no. 19990 Acuson Corporation, USA). The investigations were performed in the Ultra- sonography Department, the Chair and Department of Surgical Gynecology and Gynecological Oncology for Adults and Adolescents, and the Chair and De- partment of Obstetrics and Perinatology, Pomeranian Medical University. In cases of ovarian lesions (detected by ultrasonography) that most probably represented a benign pattern (SPACZYÑSKI,SPACZYÑSKI 2000), follow-up imag- Ovarian cystadenoma in hereditary ovarian cancers families 257 ing was scheduled after the consecutive menstruation. In cases of persistent changes recorded by ultrasonography, the lesions were surgically excised during laparotomy/laparoscopy, and then histologically verified. In the study group and in the first control group, the incidence of the three BRCA1 mutations that are prevalent in Poland (5382insC, C61G, 4153delA) have been estimated (GÓRSKI et al. 2000). The above changes constitute almost 90% of BRCA1 mutations in Polish families with aggregation of breast/ovarian cancer (GÓRSKI et al. 2004). The BRCA1 test was performed in peripheral blood or paraf- fin specimens of ovarian tissues In each family (I0 or II0 relatives) of patients from the study group and the first control group, there were two or more ovarian can- cers, or an ovarian cancer and breast cancer in individuals aged under 50 years of life. In 8 patients with both benign and borderline ovarian cystadenoma, a com- plete exon-by-exon sequencing of coding fragments of the BRCA2 gene from the peripheral blood DNA was performed (JAKUBOWSKA et al. 2002, 2003). The study group and both control groups were statistically compared with re- gard to incidence of cystadenoma and other pathological lesions within sex organs by using Stata Statistical Software 5 (Stata Corporation, College Station, TX). Odds ratio (OR), confidence interval (CI), level of significance (p), specificity, and sensitivity were calculated. Incidence and pattern of malignant tumors in families of female patients with ovarian cystadenoma Between 1998 and 2001, 152 consecutive patients with histologically confirmed ovarian cystadenoma were recorded in the histopathology laboratories of the De- partment of Pathology and Department of Genetics and Pathology, Pomeranian Medical University. For 19 of the patients some information was missing, so our initial study group included 133 female patients with known personal data. Out of these 133 patients, 7 could not provide information on I0 relatives, and 9 refused cooperation. Consequently, the final study group included 117 patients who had 726 I0 relatives (359 females and 367 males). Serous ovarian cystadenoma was diagnosed in 66 patients, including 15 cases of borderline type. Mucinous tumors were diagnosed in 48 patients, including 5 borderline cases. In one case, in a 35-year-old patient, serous cystadenoma of borderline malignancy and mucinous cystadenoma were diagnosed simulta- neously. There were also 2 cases of endometrioid cystadenoma. Pedigree data were obtained on the basis of interviews. The following parame- ters were evaluated: year of birth, age at onset, location of the malignant lesion, and present age (or age at death). The incidence and type of the malignancy in the study group were compared with the expected values basing on epidemio- logical data for malignancy-related morbidity in Poland in 1999 (DIDKOWSKA et al. 2002). BRCA1 testing for occurrence of germline 5382insC, C61G and 4153delA was performed in cystadenoma patients with first-degree relatives 258 J. Menkiszak et al. affected by breast or ovarian cancers. The statistical significance of the achieved results was evaluated with regard to OR, CI, and p according to ROTHMAN and GREENLAND (1998). Results Incidence of ovarian cystadenoma in females from families with hereditary ovarian cancer unassociated with BRCA1mutations The results are shown in Tables 1 and 2. In the study group, cystadenoma was found in 8 patients (12.9% of the group), including 4 serous and 4 mucinous cases. Three of them were “borderline malignancy” cases. No cystadenoma cases were found in the two control groups, including pa- tients with constitutional mutations of the BRCA1 gene. Constitutional mutations of the BRCA2 gene were not detected by complete “exon by exon” sequencing of DNA extracted from peripheral blood of patients with cystadenoma (JAKUBOWSKA et al. 2002, 2003). Comparison of incidence of other pathology within sex organs between the study and control groups revealed no statistically significant differences except for an increased frequency of uterine myomas in the study group, in comparison to BRCA1 mutation carriers (OR 4.72; p = 0.0132). Incidence and
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