Primary and recurrent serous borderline tumors during pregnancy: a case report and literature review

The diagnosis and management of borderline ovarian tumors during pregnancy are still not standardized, because these tumors are rarely encountered. We report the case of a 27-year-old pregnant woman who presented with an ovarian mass in her first trimester. Magnetic resonance imaging revealed a multilocular cystic component with papillary lesions in the background of endometriosis, suggesting a seromucinous borderline tumor or ovarian cancer. A right salpingo-oophorectomy and partial omentectomy were performed at 7 weeks of gestation. Pathological examination demonstrated a serous borderline tumor. The subsequent pregnancy course was uneventful, and she gave birth to a healthy baby at 39 weeks of gestation. She wanted to retain fertility, and close follow-up was performed. Four years later, she became pregnant, and a lesion suggesting recurrence in the left ovary was detected. An abdominal left ovarian cystectomy was performed at 13 weeks of gestation, which demonstrated recurrence of the serous borderline tumor. She gave birth to a healthy baby at 39 weeks of gestation. Two months after delivery, she underwent total abdominal hysterectomy with left salpingo-oophorectomy, which revealed no malignant findings. We also reviewed 10 reports that included 58 cases of borderline ovarian tumors diagnosed during pregnancy. The borderline ovarian tumors diagnosed during pregnancy exhibited different characteristics according to each subtype, suggesting the importance of diagnosing borderline ovarian tumor subtypes preoperatively.

Borderline ovarian tumor, Pregnancy, Recurrence, Serous, Histologic subtype

The probability of discovering ovarian tumors during pregnancy is reported to be 0.2–10% [1, 2]. Ovarian masses during pregnancy are mostly functional cysts, and approximately 90% disappear spontaneously [1]. Among pregnancies complicated by ovarian tumors, approximately 8% involve borderline ovarian tumors (BOTs) [3]. During pregnancy, despite the limitations of diagnostic procedures, BOTs need to be differentiated from masses such as luteinized follicular cysts and decidualization of endometriotic cysts, because most BOTs require prompt surgery. The desired treatment procedure for malignant ovarian tumors (MOTs) has shifted from artificial abortion followed by treatment to chemotherapy during pregnancy. Because BOTs during pregnancy are rare, standardized treatment has not been established, and treatment is decided on a case-by-case basis. In many cases of BOTs during pregnancy, fertility needs to be preserved. It makes a substantial difference in a patient’s life if the choice of avoiding hysterectomy while still receiving the necessary and sufficient treatment is available. The common histologic subtypes of BOTs during pregnancy are serous, mucinous, and seromucinous tumors. Each subtype has its own distinct background, imaging characteristics, pathological findings and prognosis. However, currently, these tumors are all treated as the same disease regardless of histologic subtype, merely as BOTs during pregnancy. If an information regarding the characteristics and prognoses of each histological subtype of BOTs during pregnancy becomes available, more precise treatments will be possible. Each subtype has different feature in MRI. If the cystic lesion contains serous fluid with papillary mural nodules, it is likely to be a serous borderline tumor (SBT), which is the most common type and accounts for approximately 50–55% of all BOTs [4]. Multilocular cysts with a stained-glass appearance are likely to be mucinous borderline tumors (MBTs) [5], which is the second most common type and accounts for approximately 35–45% of BOTs [4]. Seromucinous borderline ovarian tumors (SMBTs), which are also known as endocervical-type MBT or Mullerian MBT, account for approximately 5–7% of all BOTs. SMBTs are now formally established as a separate category in the revised 2014 WHO Classification of Tumors of the Female Genital Organs. Associated endometriosis is noted in 30–70% of cases [4, 5]. Therefore, on MRI, if the lesion shows endometriosis in the background with papillary mural nodules, it is likely an SMBT. SBTs are characterized by the expression of WT1, whereas SMBTs are not [4]. We encountered a case involving the onset and relapse of an SBT during pregnancy. We herein report the case together with a review of BOTs during pregnancy. Case report A 27-year-old primigravida woman became pregnant naturally and visited our hospital for the first time. There was no past medical history, and the family history was unremarkable. On a routine transvaginal ultrasound image, the gestational sac and a right ovarian tumor (14 cm in size, multilocular, and internal papillary projections of approximately 2 cm) were detected (Fig. 1a). The patient was asymptomatic. A complete blood count and blood biochemical test revealed no abnormal findings. The cancer antigen-125 level was 612 U/ml. A plain pelvic magnetic resonance imaging (MRI) examination was performed (Fig. 1b, c), which revealed a 16-cm multilocular right ovary that had a papillary mural nodule 2.7 cm in diameter. Most cyst fluid content exhibited a high T2-weighted image signal/a low T1-weighted signal, and the other cyst fluid content exhibited a high T2-weighted image signal/a high T1-weighted image signal and a high fat-suppressed T1-weighted image signal, suggesting to be an endometriotic cyst. The papillary part of the tumor exhibited diffusion restriction and had a lower T2-weighted image signal compared with the decidua. Thus, an SMBT or MOT rather than an endometriotic cyst with decidualization was suspected. Since the patient wished to continue the pregnancy, we decided to perform fertility-preserving surgery. The patient underwent abdominal right salpingo-oophorectomy (SO) at 7 weeks of gestation without intraoperative capsule rupture. The right ovary was swollen to the size of a newborn’s head and was multilocular. It contained moderately viscous fluid as well as many intracystic papillary excrescences, each with a size of a few millimeters to 3 cm. The result of the intraoperative cytological examination of the ascites was class 3, and the result of the intraoperative histological examination was an SBT. Additional partial omental resection was performed. Pathological findings included a complex papillary architecture and hierarchical tufting (Fig. 2a). The epithelial lining was composed of monolayered cuboidal epithelial cells and ciliated cells (Fig. 2b). Nuclear positivity for Wilms' Tumor 1 Protein (WT1) staining was noted in the tumor (Fig. 2c), and we diagnosed the tumor as an SBT. Neither interstitial infiltration nor stromal invasion was recognized. The stage was determined to be IA. Approximately 90% of the tumor cells had estrogen receptors (ERs) and progesterone receptors (PgRs) (Fig. 3a). Given that the patient wished to preserve fertility, we chose careful follow-up of pregnancy. The pregnancy course was unremarkable, and the patient delivered a 2820 g girl at 39 weeks of gestation. No abnormal findings were found in the infant. Thereafter, the patient was followed with tumor markers assessments and physical examinations every 3 months and CT examinations every 6 months. There were no findings that suggested abnormalities of the left ovary or recurrence. Four years later, the patient became pregnant naturally. When she visited our department and underwent examinations, transvaginal ultrasound revealed a 3-cm left ovarian cystic tumor with a 2-cm solid component that was poorly vascularized according to color Doppler ultrasound images that had not been detected 3 months before (Fig. 4a). A plain pelvic MRI examination was performed (Fig. 4b). In the 3-cm left ovary, an endometriotic cyst was found, adjacent to which was a cystic lesion containing a 2-cm mural nodule with diffusion restriction, suggesting tumor recurrence. We performed abdominal cystectomy of the left ovarian tumor at 13 weeks of gestation with a plan of subsequent hysterectomy with left SO after delivery. Rapid cytological examination of the ascites resulted in class 2 classification. No evident dissemination was noted in the pelvis. There was no intraoperative capsule rupture. The left ovarian tumor was bilocular and contained a solid component. The tumor exhibited a papillary structure with prominent interstitial edema (Fig. 5a) and endometriosis. Branching papillae are lined by serous-type monolayered cuboidal cells (Fig. 5b). Immunohistochemical staining for WT1 showed nuclear positivity (Fig. 5c). We made a diagnosis of SBT. Approximately 90% of the tumor cells were positive for ERs and PgRs (Fig. 3b). No abnormal findings were found during pregnancy, and the patient gave birth to a healthy boy with a weight of 3050 g at 39 weeks of gestation by vaginal delivery. At 2 month postpartum, a curative operation (total abdominal hysterectomy with left SO) was performed. No residual lesions were found. No recurrence was detected 3 months after the surgery. Review of the literature on BOTs during pregnancy We searched the PubMed database using the keywords “pregnancy” and “borderline tumor” in the “All Fields” search and “pregnancy” and “borderline” in the “Title” search. We identified 17 relevant reports in journals [6–22]. Among the 17 reports, ten mentioned treatment procedures and prognoses in English, and these reports contained 58 cases [6–15]. We summarized the 59 cases and included our case (Table 1). Table 1. | Mean age | 30.4 years (range 20 ~ 42) | || |---|---|---|---| | Surgical approach | Laparotomy | 37 | (62.7%) | | Laparoscopy | 16 | (27.1%) | | | Laparoscopy + Laparotomy | 6 | (10.2%) | | | Type of surgery | ||| | Unilateral | Cystectomy | 25 | (48.1%) | | SO | 27 | (51.9%) | | | Bilateral | Bi-Cystectomy | 1 | (14.3%) | | BSO | 2 | (28.6%) | | | Uni-Cystectomy + Uni-SO | 3 | (42.9%) | | | Bi-biopsy | 1 | (14.3%) | | | Histologic type | Serous | 31 | (52.5%) | | Mucinous | 22 | (37.3%) | | | Seromucinous | 6 | (10.2%) | | | FIGO stage | IA | 43 | (72.9%) | | IB | 2 | (3.4%) | | | IC | 6 | (10.2%) | | | II | 4 | (6.8%) | | | III | 4 | (6.8%) | | | Restaging surgery | No | 33 | (55.9%) | | Fertility-preserving surgery | 21 | (35.6%) | | | Radical surgery | 5 | (8.5%) | | | Restaging | ||| | Upstage | Yes | 6 | (23.1%) | | No | 20 | (76.9%) | | | Recurrence | Yes | 6 | (10.2%) | All the patients were asymptomatic except for one case. Abdominal surgery was performed in 37 cases (including 10 cesarean sections), and laparoscopy was performed in 16 cases, and 6 cases underwent both laparotomy and laparoscopy. All laparoscopies were conducted in the first trimester of pregnancy or postpartum. Among the unilateral BOT cases, there were 25 cases of cystectomy and 27 cases of SO. Regarding histology, 31 cases (52.5%) were serous, 22 cases (37.3%) were mucinous, and 6 cases (10.2%) were seromucinous. Fifty-one cases (86.4%) were stage I, 4 cases (6.8%) were stage II, and 4 cases (6.8%) were stage III. According to the histologic subtype, 25 (80.6%) SBTs and 5 (83.3%) SMBTs were stage I, whereas 21 (95.4%) MBTs were stage I. Similarly, 19 (61.3%) SBTs and 4 (66.7%) SMBTs were stage IA, whereas 20 (90.9%) MBTs were stage IA (Table 2). After the initial surgery, observational follow-up was performed in 33 cases, whereas 26 cases required additional treatment (21 cases of fertility-preserving surgery and 5 cases of curative surgery). Six cases (23.1%) were upstaged by restaging surgery. Recurrence was identified in 6 of the 59 cases (Table 3). Only one case (3.8%) of recurrence was observed among patients who underwent restaging surgery, whereas 5 cases (15.1%) of recurrence were noted in patients with observational follow-up. The rate of recurrence according to the surgical method was as follows: 4 (10.8%) with open abdominal surgery, 1 (6.3%) with laparoscopic surgery, and 1 (16.7%) with both open abdominal and laparoscopic surgeries. Among the unilateral BOT cases, the recurrence rate was 11.1% when cystectomy was performed and 4.0% when unilateral SO was performed. Recurrence was observed in 6 cases of SBTs and no cases of MBTs and SMBTs. The ovarian tumor and its treatment did not lead to abnormalities of the fetus in any of the cases. Table 2. | FIGO stage | Serous | Seromucinous | Mucinous | |---|---|---|---| | IA | 19 | 4 | 20 | | IB | 1 | 1 | 0 | | IC | 5 | 0 | 1 | | II | 3 | 0 | 1 | | III | 3 | 1 | 0 | Table 3. | Authors | Surgical approach | Type ofsurgery | FIGOstage | Histologictype | Histologic characteristics | Restaging surgery | Prognosis | |---|---|---|---|---|---|---|---| | Fauvet [11] | Laparoscopy + Laparotomy | Cystectomy | IIC | SBT | Micropapillary invasive implants | No | Recurrence at opposite ovary | | Laparotomy | SO + cystectomy | IIIC | SBT | Micropapillary invasive implants | No | Recurrence at opposite ovary | | | Laparotomy | Cystectomy | IA | SBT | NA | peritoneal biopsy | Recurrence at the same ovary | | | Cosentino [14] | Laparotomy | Cystectomy | IC | SBT | exophytic growth | No | Recurrence after 1 year, which is treated by cystectomy. She got pregnant and recurrence in 30 weeks of gestation. After delivery she got radical surgery and now without disease | | Moro [15] | Laparoscopy | Cystectomy | IA | SBT | NA | No | Recurrence after 19 months | | Presented case | Laparotomy | SO | IA | SBT | micropapillary | No | Recurrence after 4 years when she got pregnancy. She conducted cystectomy in 13 weeks of gestation, and she got radical surgery after delivery. After 3 months no signs of disease relapse | SO salpingo-oophorectomy, SBT serous borderline tumor, NA not available

The accurate diagnosis of BOTs during pregnancy is important, because it affects both the treatment of tumors and the course of pregnancy. Most adnexal masses identified in pregnant patients are either functional cysts or benign cysts. Most functional cysts will resolve after the first 14–16 weeks of gestation [23], and careful follow-up without surgical intervention is a choice. Therefore, the differential diagnosis of benign ovarian tumors between BOTs and MOTs is particularly important. To distinguish benign ovarian tumors from BOTs and MOTs with ultrasonography, various findings that increase the likelihood of BOTs/MOTs have been reported [18]. More precise diagnosis is afforded by MRI. Generally, findings that distinguish BOTs/MOTs from benign cysts include a mass diameter greater than 10 cm, a solid or papillary area, wall thickness or irregularity [24]. Gadolinium enhancement is also useful in nonpregnant conditions, but it should be avoided, because it may increase the risk of fetal stillbirth or neonatal death [25]. It should be especially noted that during pregnancy, endometriomas can exhibit a strongly changed appearance resembling malignant tumors because of decidualized walls due to high progesterone levels [26]. Marked pathological changes by ectopic decidualization are easily mistaken for malignancy, and many of these cases result in surgical intervention [27]. Recently, MRI has been reported to serve as a key tool to address this problem [28]. The following findings of mural nodules on MRI have been reported to suggest SMBTs rather than endometriotic cysts with decidual changes: (1) lower signal intensity ratios on T1WI, (2) a higher nodule height, (3) lobulated margins, (4) a pedunculated configuration and (5) a T2 hypointense core [29]. Exophytic growth of the solid portion has been reported to suggest SBTs rather than SMBTs. If the endometriosis is observed, SMBTs are more frequent, because 30–70% of SMBTs are associated with endometriosis [5]. In our case, there were endometriotic cysts and no exophytic growth, so we believed that these lesions were most likely SMBTs. These lesions were thought to be SMBTs rather than endometriotic cysts with decidual changes due to the findings of a higher height of the mural nodule, a pedunculated configuration, and a T2 hypointense core. It was difficult to differentiate SBTs or SMBTs preoperatively. The patient underwent SO in 7 weeks and gave birth to a healthy baby. In the second pregnancy, an adnexal mass was also detected at 6 weeks of gestation, and we could distinguish it from decidualized changes from similar findings in the first pregnancy. In our review, an MRI scan was performed in only one case, and none of the review cases reached a preoperative diagnosis of a BOT. Since MRI scans without contrast medium may not affect the fetus, we should consider MRI to select appropriate treatment. The differential diagnosis between BOTs and MOTs is another issue to be addressed. Although Kurata et al. reported several findings to distinguish between them [30], it is practically difficult unless obvious signs of MOTs, such as distant metastasis or surrounding invasion, are observed. Therefore, even if we suspect a BOT, the standard treatment option is surgical confirmation of histology. When we perform surgical resection of benign ovarian tumors during pregnancy, we can choose laparoscopic surgery, because it is reported to be safe for both the mother and fetus [31]. However, the feasibility and safety of the laparoscopic approach for BOTs during pregnancy have not been completely evaluated. In our case, we chose laparotomy, because the primary tumor was 14 cm, and malignancy could not be excluded. According to our review, laparoscopic surgery has been increasingly applied recently, and no significant difference in the recurrence rate was noted based on the surgical method. However, laparoscopy was performed only in the first trimester of pregnancy, and laparotomy was performed throughout the entire period of pregnancy. In their relatively large series of BOTs during pregnancy, Fauvet et al. also described that less than one-quarter of patients only underwent laparoscopy, and only two patients had complete initial staging [11]. Therefore, the application of laparoscopy during pregnancy should be considered in only limited cases in the early stages of pregnancy. Given the rarity of BOTs, there is no definite therapeutic policy for BOTs in pregnancy. In pregnancy, conservative management, such as SO or cystectomy, is typically chosen. In nonpregnant conditions, the recurrence rate is higher in cystectomy than in SO, but there is no difference in prognosis [32]. In our review, in pregnant conditions, the recurrence rate was also increased for cystectomy (12.5%) compared with SO (3.7%). In addition, recurrence was observed only in SBTs (6 cases) and not in MBTs and SMBTs. Therefore, if SBTs are suspected, SO rather than cystectomy should be considered. However, no large study comparing these conditions has been reported. The clinical course of our case was characteristic. Recurrence was not observed for 4 years during the close follow-up and was not detected 3 months before pregnancy. In our review, as mentioned above, recurrence was observed only in SBTs and not in MBTs and SMBTs, suggesting that the effect of pregnancy differs according to the histologic subtypes of BOTs. In our case, the tumor cells expressed ERs and PgRs in both primary and recurrent tumors, which supports previous reports that SBTs and SMBTs present ERs and PgRs but that MBTs do not [33]. During pregnancy, estrogen and progesterone levels increase, which may induce the aggressiveness of SBTs in pregnancy. In our review, there were 2 other cases of recurrence during pregnancy. Although SMBTs present ERs and PgRs, there are no reports about the recurrence of SMBTs during pregnancy. Therefore, if a patient has a previous history of an SBT, subsequent pregnancy may be a risk factor for recurrence, and careful follow-up during pregnancy is needed. Compliance with ethical standards Conflict of interest The authors declare that they have no conflict of interest. Human and animal rights This article does not contain any studies with human participants performed by any of the authors. Informed consent Informed consent was obtained from the patient. Footnotes Publisher's Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Contributor Information Aya Matsumoto, Email: [email protected]. Takuma Ito, Email: [email protected]. Fumika Hamaguchi, Email: [email protected]. Maya Kasuga, Email: [email protected]. Teppei Mikami, Email: [email protected]. Mayo Hino, Email: [email protected]. Reiko Yokoyama, Email: [email protected]. Shogo Yamamura, Email: [email protected]. Harumi Sakata, Email: [email protected]. Sachiko Minamiguchi, Email: [email protected]. Masaki Mandai, Email: [email protected]. Takaaki Yoshida, Email: [email protected].

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