{"paper_id":"77e1acd6-3b9f-46fb-870a-2bdbedd1f9ef","body_text":"Abstract. Background/Aim: Ovarian seromucinous tumor \nis a histological type of ovarian neoplasm. Although \nseromucinous borderline tumors (BSMT) are associated with \nendometriosis, the frequency of their occurrence is low, and \nmany aspects of their behavior remain unclear. In this study, \nwe aimed to clarify the clinicopathological factors of BSMT. \nPatients and Methods: We retrospectively reviewed 32 \npatients with pathologically diagnosed BSMT who underwent \nsurgery at Jikei University Hospital. The survey items were \npatient characteristics, such as age, initial symptoms, \npreoperative tumor markers, surgical procedure and stage of \nsurgery, presence of endometriosis, and recurrence. Results: \nThe median age was 45 years. Lower abdominal pain was \nthe most common chief complaint, about one-third of patients \nwere asymptomatic; one-sixth were discovered during \nfollow-up for endometriosis. The majority had a high serum \nCA19-9 level. Twenty-five patients (78.1%) had unilateral \nmasses, whereas seven patients (21.9%) had bilateral \nmasses. More than 90% of the cases had coexisting \nendometriosis histologically. Thirty cases (93.8%) were stage \nI, only two were stage II, and none were stage III or IV. \nRecurrence was observed in two cases: one was borderline \nmalignant and the other was a carcinoma. Conclusion: \nBSMT is a rare form of borderline malignancy. Its \npreoperative diagnosis is often difficult because of various \nclinical findings, but a history of endometriosis and an \nelevated serum CA19-9 level may aid in some cases. \nBorderline ovarian seromucinous tumor (BSM T) is a papillary \nneoplasm composed of an admixture of M üllerian type \nepithelia, lacking confluent or destructive invasion (1).\nH istorically, it was known as endocervical-type borderline \nmucinous tumor, borderline M üllerian mucinous tumor, or \nmixed-epithelial borderline tumor of M üllerian type. In the \nWorld H ealth O rganization (WH O ) Classification of \nG ynecologic Tumors, BSM T was first introduced in the fourth \nedition published in 2014 (2). Its benign counterparts, namely \nseromucous cystadenoma and seromucinous cystadenofibroma,\nare rare, while its malignant counterpart is classified as a variant \nof endometrioid carcinoma in the fifth edition published in 2020 \n(1). BSM T is often associated with endometriosis (3, 4).\nAlthough various clinical, pathological, and molecular \nfeatures of BSM T were elucidated, studies focusing on its \nclinicopathological features with a large number of cases \ntreated at a single institution are few because of its relatively \nrare occurrence. H erein, we retrospectively examined cases \nof BSM T  treated at a single institution to explore its \nclinicopathological features.\nPatients and Methods \nT his study was conducted with the approval of the Ethics \nCommittee of the Jikei University School of M edicine [Approval \nN o. 32-465(10557)].\nCase selection. Surgical pathology archives of the Jikei University \nH ospital between January 2001 and December 2017 were searched \nfor ovarian borderline tumors. All hematoxylin and eosin-stained \nslides were reviewed by two pathologists (T K and N F) to confirm \nthe histological type of tumors based on WH O  2020 criteria (1).\n360 \nCorrespondence to: Yoko N agayoshi, G ynecologic O ncology \nCenter/G ynecology, International University of H ealth and Welfare \nM ita H ospital, 1-4-3 M ita, M inato-ku, Tokyo, 108-8329 Japan. Tel: \n+81 334518121, Fax: +81 334540067, e-mail: ykaks1128@ gmail.com \nKey Words: CA-19-9 antigen, cystadenofibroma, endometriosis,\novarian neoplasms, recurrence.\nClinical Features of Borderline Ovarian Seromucinous Tumor \nYO KO  N AG AYO SH I 1,2 , KYO SUKE YAM ADA 1, TAKAKO  KIYO KAWA 3, \nN EI FUKASAWA 3, TAKAFUM I KURO DA 1, DAITO  N O G UCH I 1and AIKO U O KAM O TO 1\n1Department of Obstetrics and Gynecology, The Jikei University School of Medicine, Minato, Japan; \n2Gynecologic Oncology Center/Gynecology, \nInternational University of Health and Welfare, Mita Hospital, Minato, Japan; \n3Department of Pathology, The Jikei University School of Medicine, Minato, Japan \nCANCER DIAGNOSIS & PROGNOSIS \n3: 360-364 (2023)                                                                                                                           doi : 10.21873/cdp.10224 \nT his article is an open access article distributed under the terms and \nconditions of the Creative Commons Attribution (CC BY-N C-N D) 4.0 \ninternational license (https://creativecommons.org/licenses/by-nc-nd/4.0).\n©2023 International Institute of Anticancer Research \nwww.iiar-anticancer.org \n\nPatients’ background data, preoperative serum tumor marker levels \nand imaging findings, surgical procedure, status of intraoperative \nconsultation, surgical stage according to the International Federation \nof G ynecology and O bstetrics staging system (2014) (5), and \nprognosis were obtained from medical records.\nPathological findings . G ross descriptions of tumors were obtained \nfrom pathology reports. T he following histological findings were \nalso examined: Presence of micropapillary pattern in BSM T; \npresence of endometriosis in the ipsilateral ovary, contralateral \novary, or pelvic peritoneum; presence of endometrial neoplasm in \nthose with hysterectomy, lymph node status, and tumors at the time \nof recurrence.\nResults \nT hirty-two patients with ovarian BSM T were included. T he \npatients’ median age was 45 years (range= 22-72 years), and \n25 out of 32 patients (78%) were premenopausal (Table I).\nLower abdominal pain was the most common symptom (13 \npatients, 40.6%), but about one-third of patients were \nasymptomatic (n= 11, 34.4%) and were diagnosed during a \nmedical check-up. In five patients (15.6%), malignant \ntumor was suspected based on ultrasound during follow-up \nfor endometriosis. O ne patient presented with abnormal \ngenital bleeding. In two patients, the chief complaint was \nunknown. Twenty-two patients (68.8%) had no history of \npregnancy.\nPreoperative serum carbohydrate antigen 19-9 (CA19-9) \nlevels were elevated in 19 cases (59%), and serum CA125 \nwas elevated in 15 (47%) cases. Twelve patients (37.5%) had \nelevated levels of both CA19-9 and CA125, whereas in 10 \npatients (31.3%), both tumor markers were within normal \nlimits. Endometriosis was diagnosed in 25 cases (78.1%) \nbased on preoperative transvaginal ultrasonography and \nimaging studies.\nO perative details and results are shown in Table II. O f 32 \npatients, 12 (37.5%) underwent staging laparotomy (bilateral \nsalpingo-oophorectomy, total abdominal hysterectomy, and \nomentectomy), followed by lymph node biopsy or dissection.\nFour patients underwent bilateral salpingo-oophorectomy,\ntotal abdominal hysterectomy, and omentectomy. Sixteen \npatients underwent tumorectomy or unilateral salpingo- \noophorectomy to preserve their fertility. Intraoperative \nconsultation was performed in 28 patients; 26 were \ndiagnosed with borderline tumor, and two were borderline \ntumors or carcinoma. T he tumors varied in size, ranging \nfrom 2.5 to 20 cm, with a median of 6.4 cm. Tumor was \nunilateral in most cases (78.1%). H istological examination \nconfirmed coexistent endometriosis in 30 patients (93.7%); \nit was in the ipsilateral ovary in 24 (80%) and in the \ncontralateral ovary and pelvic peritoneum in addition to the \nipsilateral ovary in six (20%). T hirty cases were stage I, and \nonly two cases were diagnosed as stage II.\nFollow-up information was available for all 32 patients,\nwith a range of 1-211 months (median= 71 months). O nly \ntwo (6.3%) had recurrences; one only underwent \ntumorectomy initially, and unilateral salpingo-oophorectomy \nand omentectomy were performed when BSM T recurred in \nthe ipsilateral ovary 8 years later. In another patient, the \ninitial surgery was staging laparotomy to prove stage IIB \nBSM T  with noninvasive peritoneal implants and a \nconcurrent endometrial endometrioid carcinoma grade 1 \n(pT 1apN 0). H er ovarian BSM T  had both exophytic and \nintracystic growth, with the latter having a micropapillary \ncomponent. She also had a mesenteric mass and enlarged \npara-aortic lymph nodes found intraoperatively; these were \npathologically proven to be follicular lymphoma. Fifteen \nmonths after the initial surgery, another mesenteric tumor \nwas found, and the resected tumor was grade 1 endometrioid \ncarcinoma with an BSM T component. Paclitaxel/carboplatin \nchemotherapy regimen was unsuccessful, and the patient \ndied 2 years and 7 months after the initial surgery.\nDiscussion \nAlthough histological and genetic characteristics of BSM T \nhave been reported, there are few characteristic biomarkers,\nand it is not easy to estimate BSM T clinically. T herefore, it \nis important for the surgeon to know the clinical \ncharacteristics such as fluctuating tumor markers and \nfrequent complications of endometriosis, as well as the gross \nappearance of the explanted specimen. Regarding tumor \nmarkers, this study showed that the serum CA19-9 level is \noften elevated in patients with BSM T (59.4%); this finding \nwas only given limited attention in previous reports. Indeed,\nin 19 out of 32 patients with elevated serum CA19-9 level \nin this study, in five it exceeded 1,000 U/ml, and the highest \nwas 3,471 U/ml. CA19-9 is best known as a useful marker \nfor mucinous tumors of the pancreas and biliary tract, with \na relatively high sensitivity and specificity. It is localized in \nthe pancreatic and biliary parenchyma (6). CA19-9 is also \nelevated in various diseases, including mucinous ovarian \ntumors, teratoma, endometriosis, benign hepatic and \npulmonary diseases, thyroiditis, diabetes mellitus, and \nautoimmune diseases (6). Its elevation is explained by \ninflammation and proliferation of non-tumorous tissues or \nmetabolic malfunction. BSM T is histologically characterized \nby neutrophilic infiltration into the stroma and epithelium,\nand these inflammatory findings in tumors may be associated \nwith an elevated serum CA19-9 level. Regarding the \nrelationship of serum CA19-9 to the histological subtypes of \novarian tumors, N akagawa et al. reported that the serum \nCA19-9 levels in patients with borderline ovarian mucinous \ntumors and endometriotic cysts were significantly elevated \ncompared with those in control individuals and that CA19-9 \ncan be useful for preoperative evaluation (7). It is \nCANCER DIAGNOSIS & PROGNOSIS 3: 360-364 (2023) \n361 \n\nparticularly interesting that serum CA19-9 levels were higher \nin those with endocervical type tumors, which corresponds \nto the current definition of BSM T, than in the intestinal type.\nBSM T is frequently associated with endometriosis, as shown \nin literature (3, 4, 8) and in the present study, and is usually \naccompanied by prominent neutrophil infiltration, thus it \nmay be responsible for CA19-9 elevation. H owever, in some \ncases in this study, serum CA19-9 was not elevated despite \nthe presence of endometriosis or neutrophil infiltration in \ntumors. T he mechanism of this elevation requires further \ninvestigation. \nBSM T  is included in endometriosis-related ovarian \nneoplasms, along with clear-cell carcinoma and endometrioid \ncarcinoma (8). In this study, 25 patients (78.1%), including \nfive who had endometriotic cysts, had preoperative imaging \nstudies indicating the presence of endometriosis. In 93% \n(30/32) of patients with surgically removed ovaries, a \nhistological diagnosis of coexistent endometriosis was found; \nthis was more frequent than what was previously reported.\nO f the 30 patients with endometriosis, six (20%) had \nendometriosis in the contralateral ovary or pelvic \nperitoneum. O ne possible reason for the higher frequency of \ncoexisting endometriosis in this study is the number of tissue \nsections taken at our institution, which was at least one \nsection per 1 cm of tumor diameter.\nIn this study, two patients (6.3%) had recurrence. While the \nrecurrence rate of borderline ovarian tumors is 5-33% \ngenerally (9), H ada et al. reported a rate of 18% for BSM T,\nsuggesting that the association with endometriosis may be a \nfactor that increases recurrence (10). Ren et al. reported that \nconservative surgical procedures, cyst rupture, advanced \nInternational Federation of O bstetrics and G ynecology stage,\nmicroinvasion, and peritoneal implants are risk factors for \nN agayoshi et al : Clinicopathological Factors of BSM T \n362 \nTable I. Characteristics of patients in this study (n=32 patients). \nCharacteristics                                                                     N  (%) \nAge, years \n   M edian (range)                                                             45 (22-72) \n   <40 Years                                                                     10 (31.2%) \n   ≥40 Years                                                                     22 (68.8%) \nM enopausal status \n   Premenopausal                                                             25 (78.1%) \n   Postmenopausal                                                            7 (21.9%) \nChief complaint \n   Abdominal pain                                                           13 (40.6%) \n   N o symptoms                                                               11 (34.4%) \n   Endometriosis*                                                             5 (15.6%) \n   O ther                                                                               1 (3.1%) \n   Unknown                                                                        2 (6.3%) \nParity \n   0                                                                                   22 (68.8%) \n   ≥1                                                                                  10 (31.2%) \nPreoperative serum tumor markers                                         \nCA19-9 \n   ≤37.0 U/ml                                                                   13 (40.6%) \n   > 37.0 U/ml                                                                   19 (59.4%) \n   M edian (range), U/ml                                               169 (42-3,471) \nCA125 \n   ≤35.0 U/ml                                                                     17 (53%) \n   > 35.0 U/ml                                                                    15 (47%) \n   M edian (range), U/ml                                              198 (38-10,035) \nCA19-9/CA125 \n   Positive for both                                                          12 (37.5%) \n   N egative for both                                                         10 (31.3%) \nEndometriosis* \n   Yes                                                                                25 (78.1%) \n   N o                                                                                  4 (12.5%) \n   Unknown                                                                        3 (9.4%) \nRecurrence \n   Yes                                                                                  2 (6.3%) \n   N o                                                                                 30 (93.7%) \n*H istory, ultrasound/magnetic resonance imaging findings.\nTable II.Operative details and results. \n                                                                                            N  (%) \nSurgical procedure, n (%) \n   Staging laparotomy a                                                   12 (37.5%) \n   Standard laparotomy b                                                  4 (12.5%) \n   Fertility-sparing staging laparotomy c                          16 (50%) \nIntraoperative diagnosis, n (%) \n   Benign                                                                                  0\n   Borderline                                                                    26 (81.3%) \n   Carcinoma                                                                            0\n   Borderline/carcinoma                                                    2 (6.2%) \n   N ot made                                                                       4 (12.5%) \nTumor size, cm \n   M edian (range)                                                            6.4 (2.8-20) \nSite of tumor, n (%) \n   Unilateral                                                                      25 (78.1%) \n   Bilateral                                                                         7 (21.9%) \n   Yes                                                                                30 (93.7%) \nEndometriosis*, n (%) \n   Ipsilateral                                                                       24 (80%) \n   Contralateral or pelvis                                                    6 (20%) \n   N o                                                                                   2 (6.3%) \nStage, n (%) \n   I                                                                                    30 (93.8%) \n   IA                                                                                  18 (56.3%) \n   IB                                                                                    3 (9.4%) \n   IC d                                                                                9 (28.1%) \n   II                                                                                     2 (6.2%) \n   III-IV                                                                                    0\n*H istologically confirmed in the surgical specimens. aBilateral salpingo- \noophorectomy with hysterectomy, omentectomy, lymph node biopsy or \nlymphadenectomy. bBilateral salpingo-oophorectomy with \nhysterectomy, omentectomy. cUnilateral salphingo-oophorectomy and \ntumorectomy or bilateral tumorectomy with or without omentectomy.\ndN on-invasive implant present.\n\nrecurrence of BSM T (11). Another report showed a \nrecurrence rate of 14-20.5% with conservative surgery \ncompared to 0-7% with radical surgery (12). In fact, one of \nthe patients with recurrence in the present study only \nunderwent tumorectomy initially. It is noteworthy that one \npatient in our study whose initial surgery was staging \nlaparotomy to prove stage IIB BSM T with non-invasive \nperitoneal implants and pT 1apN 0 developed peritoneal \ncarcinoma at the time of recurrence. It is possible that the \nnon-invasive peritoneal implant progressed to cancer; another \npossibility is that ovarian or peritoneal diseases had a \ncarcinoma component, which was not pathologically \ndetectable. Koskas et al. reported that three cases of \nendocervical-like borderline mucinous tumors and mixed- \nepithelial borderline tumors, which are currently called \nBSM T, recurred during a 10-year follow-up, with two \nrecurring as invasive carcinomas (13). It is known that 2-3% \nof borderline ovarian tumors develop as invasive carcinoma \nat the time of recurrence (14, 15). In a review of 130 cases \nof borderline malignancies, including those who underwent \nconservative surgery, O h et al. reported 11 (8.5%) \nrecurrences; four cases recurred as borderline malignancies,\nwhile seven cases had a histological diagnosis of carcinoma \n(9). Based on these reports, it is more likely that the non- \ninvasive peritoneal implant progressed to cancer in our \npatient. Although borderline ovarian tumors are generally \nconsidered to have a favorable prognosis and survival rates,\nwhich do not differ significantly among histological types \n(16), it should be noted that rare BSM Ts of advanced stages \nmay develop as cancer in the peritoneum and result in a \npoor prognosis. When only performing tumorectomy or \nunilateral salpingo-oophorectomy in a patient with BSM T \nfor fertility sparing, it is essential to understand that BSM T \nis often associated with endometriosis in the ipsilateral ovary \nor other foci in the pelvis; this may result in tumor \nrecurrence, either as borderline tumor or carcinoma.\nT his study has several limitations. O ne is that the follow- \nup period (median= 6 years) is not long enough for borderline \ntumors given that one patient had recurrence 8 years after \nthe initial surgery. A larger study of BSM T  with a longer \nfollow-up should be carried out. T he accumulation of such \nstudies will help elucidate the exact clinical features of this \ndisease. Secondly, as mentioned previously, it was not \npossible to identify the mechanism of CA19-9 elevation.\nFinally, we only focused on clinical features of patients with \nBSM T, and no molecular analysis was performed. In \nprevious studies, gene mutations of cancer-related genes,\nsuch as of KRAS proto-oncogene, G T Pase (KRAS), AT-rich \ninteraction domain 1A (ARID1A), and phosphatidylinositol- \n4,5-bisphosphate 3-kinase catalytic subunit alpha (PIK3CA) \nmutations, were reported in BSM T, suggesting that \nmolecular analysis may clarify the biological characteristics,\ndevelopment, and progression of this entity (4, 17, 18).\nIn summary, BSM T  can occur in a wide range of age \ngroups (19, 20), and it can be identified based on symptoms \nassociated with pelvic masses or discovered incidentally \nwithout any symptoms (21, 22). T he preoperative diagnosis \nof BSM T  is often difficult because of variable clinical \nfindings, but a history of endometriosis and elevated serum \nCA19-9 level may aid in some cases.\nConflicts of Interest \nT he Authors have no conflicts of interest to declare.\nAuthors’ Contributions \nYoko N agayoshi and Kyosuke Yamada designed this study. Yoko \nN agayoshi wrote the initial draft of the article. Takafumi Kuroda \nand Daito N oguchi collected the data. N ei Fukasawa and Takako \nKiyokawa reviewed hematoxylin and eosin-stained slides to confirm \nthe histological type of tumors based on WH O  2020 criteria. Yoko \nN agayoshi contributed to the analysis and interpretation of data and \nassisted in the preparation of the article. Aikou O kamoto critically \nreviewed the article and made revisions. All other Authors have \ncontributed to data collection and interpretation and critically \nreviewed the article. All Authors approved the final version of the \narticle and agreed to be accountable for all aspects of the work by \nensuring that questions related to the accuracy or integrity of any \npart of the work are appropriately investigated and resolved.\nAcknowledgements \nT he article was edited by Enago (www.enago.jp) for English \nlanguage review. T he Authors would like to thank the staff of the \nDepartment of O bstetrics and G ynecology and Department of \nPathology, T he Jikei University School of M edicine H ospital for \ntheir support and cooperation.\nReferences \n1 Kobel M , Kim K-R, M cCluggage WG , Shih I and Singh N : \nSeromucinous borderline tumour /carcinoma. In : WH O \nClassification of Tumours Editorial Board: WH O  Classification \nof Tumours . 5 th Edition. Female G enital Tumours . Lyon, France,\nIARC, pp. 69-70, 2020. \n2 Kobel M , Prat J, Bell DA, Shih IM , Carcangiu M L, Soslow R,\nO liva E and Vang R: Seromucinous tumours . In: Kurman RJ,\nCarcangiu M L, H errington CS, Young RH  (eds). WH O \nclassification of Tumours of Female Reproductive O rgans,\nFourth Edition. 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DO I: \n10.1002/1097-0142(19880115)61:2< 340:: aid-cncr282061 \n0225> 3.0.co;2-u \n22 Rutgers JL and Scully RE: O varian mixed-epithelial papillary \ncystadenomas of borderline malignancy of mullerian type. A \nclinicopathologic analysis. Cancer 61(3) : 546-554, 1988. PM ID: \n3338022. DO I: 10.1002/1097-0142(19880201)61:3< 546:: aid- \ncncr2820610321> 3.0.co;2-i \nReceived February 19, 2023 \nRevised March 4, 2023 \nAccepted March 6, 2023 \nN agayoshi et al : Clinicopathological Factors of BSM T \n364","source_license":"public-domain-us","license_restricted":false}