A case of paraovarian tumor of borderline malignancy with decrease of apparent diffusion coefficient value and marked 18F-fluorodeoxyglucose accumulation

Abstract

Para-ovarian cysts are occasionally encountered in clinical practice; however, malignant tumors derived from them are rare. Due to its rarity, the characteristic imaging findings of para-ovarian tumors with borderline malignancy (PTBM) are largely unknown. Herein, we report a case of PTBM, along with imaging findings. A 37-year-old woman came to our department with a suspected malignant adnexal tumor. Pelvic contrast-enhanced magnetic resonance imaging (MRI) revealed a solid part within the cystic tumor with a decrease in the apparent diffusion coefficient (ADC) value (1.16 × 10^–3 mm²/s). We also performed Positron Emission Tomography–MRI and showed a strong accumulation of 18F-fluorodeoxyglucose (FDG) in the solid part (SUVmax = 14.8). In addition, the tumor appeared to develop independently of the ovary. Because tumor was derived from para-ovarian cyst, we suspected PTBM preoperatively and planned fertility sparing treatment. Pathological examination revealed a serous borderline tumor and PTBM was confirmed. PTBM can have unique imaging characteristics, including a low ADC value and high FDG accumulation. When a tumor appears to develop from para-ovarian cysts, borderline malignancy can be suspected, even if imaging findings suggest malignant potential.

Introduction

Para-ovarian cysts are occasionally encountered in clinical practice; however, malignant tumors derived from them are rare [1]. Only a few cases have been reported and most of them are borderline malignancies (para-ovarian tumor of borderline malignancy; PTBM) [2–4]. In those case series, they reported that histological types are mainly serous borderline tumors (SBT). However, most patients were diagnosed with PTBM at the time of surgery. To the best of our knowledge, no case has been reported in which the possibility of PTBM was suspected preoperatively.

Herein, we present a case that can be assumed to be a malignant borderline tumor preoperatively. The findings of preoperative imaging tests, pelvic contrast-enhanced magnetic resonance imaging (MRI) and Positron Emission Tomography (PET)/MRI, suggested malignancy rather than borderline malignancy with a decrease in apparent diffusion coefficient (ADC) and a marked accumulation of 18F-fluorodeoxyglucose (FDG) in the solid part. Because PTBM is rare and its characteristic imaging findings are largely unknown, we report this case with a literature review.

Case report

The patient was a 37-year-old woman (gravida 0, para 0). During her regular health checkup, an adnexal tumor was found, and the patient was referred to our department in X year. Transvaginal ultrasonography revealed a solid mass of 1-cm in size within the cyst with a diameter of 4 cm, and further studies were planned. The results of pelvic contrast-enhanced MRI showed a cyst with a solid part that arises from its wall in the left adnexal region. On T1-weighted images (T1WI), the signal of the solid part was the same as that of the cystic region (Fig. 1a). On T2-weighted images (T2WI), the signal of the solid part was moderately low signal intensity, while that of the cystic part was high signal intensity (Fig. 1b). The ADC value in the solid part decreased to 1.16 × 10^–3 mm²/s (Fig. 1c). Contrast enhancement was also observed (Fig. 1d). Adjacent to the tumor, the left ovary with follicles was observed (Fig. 1e, f). Since there was no bird’s beak sign at the margin of the cyst, we suspected that the tumor was independent of the ovary. Furthermore, PET/MRI examination was performed. A strong accumulation of FDG (SUVmax = 14.8) was observed in the solid region (Fig. 1g). No other abnormal FDG accumulations were observed. Tumor markers were evaluated and all were within the normal range (CA125: 7.7 U/ml; CA19-9: 4.1 U/ml; and CEA: 1.2 ng/ml).

Fig. 1.

Imaging findings of MRI and FDG-PET/MRI. a (Axial) fat-suppressed T1-weighted image. The signal of fluid and solid part is equal. b (Axial) T2-weighted image. There is a solid part inside the cyst wall. c (Axial) ADC map image. ADC value of solid part is apparently lower. d (Axial) contrast-enhanced fat-suppressed T1-weighted image. There is a contrast effect in the solid part. T2-weight image, axial view (e) and sagittal view (f). Apart from cyst, there are multiple small cysts, suggesting follicles. This lesion is thought to be normal ovary. g FDG PET/MRI image. The marked FDG accumulation is found at the solid part

Among several imaging findings, the decrease in the ADC value, contrast enhancement, and marked accumulation of FDG in the solid part strongly suggest the possibility of malignant potential. However, the tumor appeared to originate from the fallopian tube and not from the ovary. To the best of our knowledge, there have been no reports of para-ovarian cyst-derived malignant tumors, and they were all borderline malignancies (PTBM). We then suspected PTBM. Because we believed that we could resect the tumor without rupture laparoscopically, we planned a laparoscopic left salpingo-oophorectomy and partial omentectomy.

There were no apparent disseminations in the omentum or the abdominal cavity. The right adnexa and the left ovary were intact and the tumor developed from the left mesosalpinx, in addition to the ovary (Fig. 2a, b). The left adnexa and tumor were resected without rupture. The tumor was placed in a bag to prevent rupture and removed from the abdominal cavity (Fig. 2c).

Fig. 2.

Intraoperative findings. a Abdominal findings. No ascites, no dissemination. Intact uterus, the right adnexum. b The status of left adnexum. The left ovary is intact. Tumor developed from fallopian tube, which is independent from ovary. c The situation of tumor retrieval. We brought tumor into the bag to prevent tumor rupture

Macroscopically, the ovaries and the tumors were clearly independent of each other and the tumor originated in the mesosalpinx (Fig. 3a). A millet-sized solid portion was present inside the tumor (Fig. 3b). Microscopically, atypical cells had proliferated in the papillary region (Fig. 3c). In some parts, cilia-resembling fallopian tube epithelial cells were observed (Fig. 3d). The tumor cells did not invade the surrounding stroma. A diagnosis of SBT arising from left para-ovarian cyst, International Federation of Gynecology and Obstetrics stage IA, was made.

Fig. 3.

Pathological Findings. a, b Macroscopic findings. Tumor is independent from the ovary. The nodule was observed within the cyst. c Microscopic findings, × 40 magnification, scale bar equals 300um. d Microscopic findings, × 200 magnification, scale bar equals 100um. Tumor proliferated inside the wall papillary, and there is no invasion into the stroma of fallopian tube

Considering the patient’s age, parity status (37 years old and null parous), and pathological findings, fertility sparing treatment can be considered. After a thorough consultation with the patient, no further treatment was performed and careful follow-up was performed. Currently, 1.5 years postoperatively, there is no apparent evidence of recurrence.

Discussion

We encountered a case of a borderline tumor arising from a para-ovarian cyst, PTBM. Preoperative imaging findings strongly suggested a malignancy. It was difficult to determine whether the treatment plan should be based on malignancy, largely based on imaging findings.

Imaging findings are important for preoperative malignancy assessment for adnexal tumors. Among several MRI factors, low ADC values have been reported to be highly relevant for malignancy [5–7]. Turkoglu et al. reported that ADC values on MRI are useful in differentiating malignant from benign tumors, and the average ADC value for malignant tumors is reported to be 0.92 × 10^–3 mm²/s [5]. We have also previously examined the ADC values of sero-mucinous borderline tumor (SMBT) and SBT, two frequently observed borderline malignancies of the ovary [8]. In that report, we showed an average of 1.80 × 10^–3 mm²/s for SMBT and 1.60 × 10^–3 mm²/s for SBT. The ADC values observed in this case were 1.19 × 10^–3 mm²/s, much lower than those of borderline tumors and closer to those of malignant tumors. Including the finding of the contrast enhancement, the MRI findings in this case strongly suggest a malignant tumor, not a borderline malignancy, if this tumor was an ovarian tumor.

The accumulation of FDG has also been used to distinguish the malignant potential [7, 9–11]. Virarkar et al. reported that FDG-PET is useful for distinguishing malignancy in ovarian tumors, and the cut-off value for SUVmax is 3.0–4.5 [10]. In this case, we found a significant accumulation of FDG with SUVmax = 14.8 in the solid part. Furthermore, by performing PET/MRI instead of PET/CT, we confirmed that FDG accumulation was consistent with the solid part visualized on MRI. PET/MRI FDG accumulation findings also suggest a malignant rather than a borderline malignant ovarian tumor.

Because PTBM is rare, there have been no reports on the typical imaging findings of PTBM. Suzuki et al. reported that one PTBM tumor showed a solid part with high signal intensity in the DWI in the cyst wall [3]. Kajiyama et al. also reported that PTBM tumors had solid parts with low ADC values in the cyst wall [4]. Our case had findings similar to those of previous reports. The solid part with high signals on the DWI/low ADC map in the cyst wall may be characteristic of PTBM. As for the degree of FDG accumulation, it can vary among malignant tumors, depending on differences in metabolic activity [12, 13]. The significant accumulation of FDG in our case may have been due to differences in metabolic activity. However, this is the first report of FDG accumulation in PTBM, and it is unclear whether this is unique to PTBM or a feature observed only in this case; hence, further studies are needed.

In this case, we took other findings into considerations and finally have emphasized the origin of the tumor. To date, there have been no reports of malignant tumors arising from para-ovarian cysts. We believe that it is important to perform a comprehensive assessment, including imaging findings, clinical findings and epidemiological information.

Although indications for laparoscopic surgery for ovarian cancer are still limited, laparoscopic surgery for early-stage ovarian cancer is being advocated when the tumor is resected without rupture [14, 15]. In this case, we planned laparoscopic surgery because we assumed that the tumor could be resected without rupture according to the preoperative assessment. As a result, we were able to provide not only minimally invasive treatment, but also oncologically successful treatment.

In conclusion, we reported a case of PTBM with a decrease in the ADC value and marked accumulation of FDG. Even if the tumor shows decreased ADC and accumulation of FDG, these findings may be characteristic of PTBM, and a comprehensive assessment, including other clinical findings, is important.

Declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This article does not contain any studies with animals performed by any of the authors.

Informed consent

Written informed consent was obtained from the patient for the publication of this case report and its accompanying images.