MR findings of primary ovarian granulosa cell tumor with focus on the differentiation with other ovarian sex cord-stromal tumors

MR findings of primary ovarian granulosa cell tumor with focus on the differentiation with other... Background: To describe magnetic resonance imaging (MRI) features of ovarian granulosa cell tumors (OGCTs) and compare with other sex cord-stromal tumors (OSCs) in ovary. Methods: MR findings of 18 patients with surgically confirmed ovarian granulosa cell tumor were retrospectively reviewed by two radiologists with consensus reading. All MR examinations were prospectively performed within one month. Clinical and imaging characteristics of OGCTs were evaluated and compared with OSCs (control group). Results: In 18 patients, 20 ovarian granulosa cell tumors were detected on MRI. Sixteen tumors appeared as solid or mostly solid mass (16/20), while 4 tumors as cystic mass. Pathological pelvic fluid was detected in 1 OGCT (1/18) and 11 OSCs (11/34) (p = 0.031).On T2 weighted imaging (T2WI), most of OGCTs displayed hyperintense signal and mixed signal (19/20); on T1 weighted imaging (T1WI), 11 OGCTs (11/20) displayed similar signal as on T2WI imaging. The lesion signal between OGCT and OSC differed significantly on both T1WI (p = 0.017) and T2WI (p = 0.002). Tumoral bleeding was detected in 6 OGCTs on MRI. On diffusion weighted imaging (DWI) images, OGCTs mostly appeared as high signal (16/20). Average apparent diffusion coefficient (ADC) value derived from DWI images in the OGCT group − 3 2 − 3 2 (0.84 ± 0.26× 10 mm /s was less than the control group (1.22 ± 0.47 × 10 mm /s) with statistical difference (p =0.002). Conclusions: MRI could provide important information in OGCT diagnosis. ADC value might be useful in differentiating OGCT from OSC. Keywords: Ovarian granulosa cell tumor, Sex-cord tumor, MRI, Diagnostic imaging Background with stages II–IV granulosa cell tumor [4–7]. Owing Ovarian granulosa cell tumor (OGCT) is a rare sex to the superb soft-tissue resolution and free radiation, cord-stromal tumor in ovary, accounting only 2–3% of magnetic resonance imaging (MRI) is widely used as all ovarian tumors [1]. Pathologically, OGCTs are classi- a problem-solving modality in assessment of complex fied into two subtypes: adult and juvenile form, in which adnexal masses that are indeterminate on ultrasonog- adult type occupying 95% of all OGCTs [2]. Despite raphy (US) or computed tomography (CT) [8]. Till OGCT have a favorable prognosis, an incidence of now, most of reported OGCTs in the literatures are 25–30% metastases or recurrences make it as a low published as case report and no detailed MRI knowl- malignant potential ovarian tumor [3]. Chemotherapy edges of OGCTs have been comprehensively described is recommended as adjuvant treatment for patients [6–13]. In this study, by evaluating OGCTs in our single institution, we aimed to: (1) thoroughly evalu- ate the MRI appearances of OGCTs in a large cohort * Correspondence: dr.zhanghe@yahoo.com of samples and record ADC values for each lesion; He Zhang and Hongyu Zhang contributed equally to this work. Department of Radiology, Obstetrics and Gynecology Hospital, Fudan (2) compare these features with OSCs. University, Shanghai 200011, People’s Republic of China Institute of functional and molecular medical imaging, Fudan University, Shanghai 200040, People’s Republic of China Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Zhang et al. Journal of Ovarian Research (2018) 11:46 Page 2 of 9 Methods the lesion; and presence of capsule, pelvic-free fluid and Study subjects lymph node were also noted. On T1WI, hypo-, iso-, and Between December 2009 and December 2015, 1217 con- hyperintensity were similar for the pelvic fluid, pelvic wall secutive patients with clinically suspected adnexal disease muscle, and fat signal; on T2WI, hypo-, iso-, and hyperin- prospectively underwent 1.5 T MRI examinations before tensity were similar for the pelvic bone, pelvic wall muscle, − 2 pelvic or laparoscopic surgery at our institution. The time and fat signal; on b =800 mm /s DWI images, the low, interval between the MRI evaluation and surgery was less intermediate, and high-signal intensity were similar for than one month (2–27 days; mean, 5 ± 12 days). the pelvic bone, myometrium, and endometrium. After Among them, 18 patients with histologically proven the intravenous injection of the contrast medium, the le- OGCT (24–79 years of age; average age, 45.9 ± 15.3 years) sion enhancement type was graded as follows: 1, minor were included in this study when we retrospectively re- enhancement (clearly less than the myometrium); 2, mild trieved the database on the Picture Archiving and Com- enhancement (less than the myometrium); 3, moderate munication System (PACS). Two recurrent OGCTs were enhancement (similar to the myometrium); or 4, avid excluded for further analysis because the primary imaging enhancement (more than the myometrium). ADCs were data was evaluated in another hospital. Thirty four measured manually on post-processing workstation patients with OSCs, including histologically proven scler- (Leonardo, Siemens, Germany) by one reviewer (H.Z.). osing stroma tumors (SST, n = 4), fibrothecomas (n =21), Two observers (S. X. G. and H.Z., with 6 and 10 years of and fibromas (n = 9), were included as the comparative experience in gynecological imaging, respectively), who group. Patients with any previous pelvic surgery or were blinded to the histological results independently, radiation history were arbitrarily excluded because the analyzed MRI datasets of each participant. At the end of inherent structure of the uterus may has been altered. the study, two observers were also required to determine Details of the samples studied are summarized in Table 1. the tumor etiology (benign or malignant) according to previous established criteria [14–16]. For interobserver Image acquisition discrepancies in the evaluation of uterine lesions, consen- MRI was performed using a 1.5-T MR system (Magnetom sus was achieved. Avanto, Siemens, Erlangen, Germany) with a phased-array coil. The routine MRI protocols used for assessment Statistical analyses of pelvic masses included axial turbo spin-echo (TSE) Continuous variables were expressed as the means ± T1WI, sagittal TSE T2WI, and axial/sagittal TSE standard deviation (S.D.) and compared with the un- fat-suppressed T2WI (FS T2WI). For axial images, paired t test if normally distributed or the Mann–Whit- the transverse plane was perpendicular to the long ney test if not normally distributed. A nonparametric axis of uterine body; for sagittal images, the longitudinal test (Mann–Whitney) was used to test other nonpara- plane was parallel to the main body of uterus. DWI using metric variables within each group. The area under the an echo-planar imaging two-dimensional (EP2D) se- receiver operating characteristic (ROC) curve (AUC) quence performed in the axial plane with parallel acquisi- was calculated for ADCs to discriminate OGCTs from tion technique by using b value = 0, 100, and 800 s/mm . OSCs. SPSS (version 13.0, SPSS, Chicago, USA) was Contrast-enhanced pelvic imaging was acquired at mul- used to perform statistical analyses. P values ≤0.05 were tiple phases of contrast medium enhancement in both sa- considered statistically significant. gittal and axial planes. Results Image analysis The histological results revealed 20 OGCTs in 18 pa- The location, size (the largest dimension in two orthog- tients (24–79 years of age; average age, 48.2 ± 15.1 years), onal planes), margin (regular or irregular); visibility of including 17 adult types and 1 juvenile type (Fig. 1). hemorrhagic component (high signal on T1WI) within Laparotomy was performed in 13 patients while others with laparoscopic surgery. Nine patients had regular or irregular menses, while menopause in nine patients. Table 1 Summaries of histological results in 54 ovarian sex-cord According to the international federation of obstetrics lesions detected on MRI in 52 patients and gynecology (FIGO) staging system [17], twelve Pathology diagnosis Numbers patients were classified as Ia, 4 as Ic, 1 as IIIa and 1 as Granulosa cell tumor 20 IIIc. All primary tumors were solitary lesion detected on Fibrothecoma 21 MRI, except for three primary lesions in one patient at Sclerosing stroma tumor 4 initial evaluation (Fig. 2). Most of OGCTs at presenta- Fibroma 9 tion appeared as the large mass with the average diam- indicates 20 lesions in 18 patients eter of 9.33 ± 5.43 mm. Among them, five patients were Zhang et al. Journal of Ovarian Research (2018) 11:46 Page 3 of 9 Fig. 1 A 32-year-old woman histologically proved OGCT in juvenile type (IIIc). On sagittal FS-T2WI image (a), the giant mass with irregular margin (arrow) occupy the majority of pelvis with the uterus being pushed forwardly (arrow head). (b) On contrast-enhanced images, the mass show homogeneously moderate enhancement; the necrotic area do not show enhancement (star) also accompanied by other ovarian etiologies, including Accordingly, OSCs mainly displayed as isointense (12/34) endometrial polyps (n = 2), uterine fibroids (n = 2), fol- and hyperintense signal intensity (10/34) on T2WI licular cyst (n = 1), Brenner tumor (n = 1) and fibroid images. and mucinous cystadenoma (n = 1). Vaginal discharge Neoplastic bleeding can be seen in six OGCTs, appear- was recorded in one OG patient. The details of base- ing as the patchy high signal intensity on T1WI images line characteristics for all studied samples are summa- in the tumor body (Fig. 3), which was not identified in rized in Table 2. OSC group (p = 0.000). Seventeen OGCTs were round or oval masses with regular margin (17/20) and intact MRI characteristics capsule (16/20), while 33 (33/34) and 34(34/34) observed In this studied samples, OGCTs showed varying signal in OSCs, respectively (p = 0.015). Regarding the tumor intensities on both T1WI and T2WI images. On T1WI, component, OGCTs mostly appeared as the solid or OGCTs showed various signal from low to mixed signal, mostly solid component (16/20, Fig. 4), while OSCs al- which was different to OSCs mostly appearing as hypoin- ways showed purely solid component (28/34) (p = 0.000). tense and isointense mass (p = 0.017). On T2WI, OGCTs On the post-contrast images, fourteen lesions (14/20) in mainly displayed as high and mixed signal (19/20). OGCT group displayed mild enhancement and six Fig. 2 A 61-year-old woman with primary adult type OGCT (Ia). There are oval, solid masses on right adnexal region (a, b) and right iliac fossa (c, d). Two lesions appears as similar signals with intermediate signal on both T1WI (a, c) and FS-T2WI (b, d)with intact capsule.On DWI image (e), the mass at the right iliac fossa shows relatively high signal (arrow) and low signal on the ADC map (f). The gross specimen reveals the yellow, solid mass with smooth capsule and a thin septa (g). Photomicrograph, hematoxylin and eosin stained section (× 40) shows the oval cells arrange closely with pleomorphic nuclei, prominent nucleoli and scanty cytoplasm. Note, the small vessels embed among the intercellular space (arrow head) Zhang et al. Journal of Ovarian Research (2018) 11:46 Page 4 of 9 Table 2 Basic and imaging characteristics of OGCTs Table 2 Basic and imaging characteristics of OGCTs (Continued) a a OGCTs OSCs P value OR OGCTs OSCs P value OR Imaging findings Pelvic fluid 0.031 8.130 T1 signals 20 34 0.017 Physiological/ Pathological 17/1 23/11 hypointensity 4 8 Clinical findings isointensity 5 26 Age(years) 48.2 ± 15.1 54.8 ± 15.0 0.139 (24–79) (21–81) hyperintensity 5 Vaginal discharge/bleeding 1 0 0.106 mixed 6 Menstruation T2 signals 0.002 Regular(irregular) 9(4) 18(5) 0.607 hypointensity 5 Menopause 9 16 isointensity 1 12 Accompanying lesions 0.280 hyperintensity 12 10 Yes/ No 7/12 9/25 mixed 7 7 Indicates odds ratio DWI signals 0.003 hypointensity 1 7 showed moderate enhancement. In OSC group, most of isointensity 3 11 fibromas showed minor enhancement and 4 SSTs ap- hyperintensity 16 16 peared inhomogeneously avid enhancement (Fig. 5). On mixed DWI images, 80 % of OGCTs (16/20, 80.0%) showed Margin 0.326 0.172 high signal intensities in comparison with 47% (16/34, Regular/Iregular 17/3 33/1 47.1%) in OCS group. The average ADC value (817 ± − 3 2 144 × 10 s/m ) in OGCT group was obviously less Capsule 0.015 0.800 − 3 2 than OSC group (1223 ± 473 × 10 s/m , p = 0.002) and Present/Absent 16/4 34/0 − 3 2 fibrothecoma (1209 ± 437 × 10 s/m , p = 0.001, Fig. 6). Hemorrhage 0.001 3.429 − 3 2 When use the ADC cutoff value as 619 × 10 s/m , Present/Absent 6/14 0/34 MRI could yield a sensitivity of 79.4% and a specificity Component 0.000 2.50 of 60.0% for diagnosis of OGCT, respectively; the AUC Solid(80–100% solid 828 is 0.784(95% CI:0.658–0.910) (Fig. 7). Enlarged lymph component) nodes were not observed in all OGCTs at MRI images. Cyst (80–100% cystic 41 Pathological fluid was only noted in one OGCT, component) obviously less than 11 cases in OSCs group. At multi- Solid with cystic 85 variate analysis, neoplastic hemorrhagic contents (OR: changes (others) 3.429), component (OR: 2.50) and no pathological fluid Enhancement 0.034 (OR: 8.130) are more indicative of OGCT diagnosis (homogeneous/inhomogeneous) (Table 2). On MRI, two readers accurately determined minor 16(16/0) the malignant condition in 17 cases. If combining ADC mild 14(12/2) 10(7/3) values, then they could yield a sensitivity of 95.0% and a moderate 6(5/1) 4(4/0) specificity of 94.1% for OGCT diagnosis. Three lesions were misdiagnosed as uterine fibroids and two lesion as avid 4(1/3) fibrothecoma before invasive procedures. The overall Maximum diameter (mm) 9.33 ± 5.43 8.5 ± 8.9 0.753 diagnostic performance of MRI for diagnosing OGCT is <5 6 17 listed as Table 3. 5–10 9 12 >10 5 5 Discussion −3 2 ADC values(×10 s/m ) 817 ± 144 1223 ± 473 0.002 OGCTs account for less than 5% of all malignant ovar- (558–1120) (460–2230) ian tumors, representing the most common malignant Septa 0.121 sex cord–stromal tumor in ovary origin; clinically, it may require additional chemotherapy after tumor re- Present/Absent 6/14 5/29 moval surgery [13]. Radiological knowledge of this rare Lymph node 0.913 ovarian tumor is still limited in the reported literature, Present/Absent 0/18 0/34 especially focusing on MR acquisition. Herein, we col- lected 20 OGCTs in 18 patients with prospective MR Zhang et al. Journal of Ovarian Research (2018) 11:46 Page 5 of 9 Fig. 3 A 54 -year-old woman with primary adult type OGCT (Ic). The mass shows as the purely cystic lesion with mostly high signal on T1WI (a) and T2WI (b). Note, the hemorrhagic contents locates on the left side of the tumor, representing the relatively high signal on T1WI and low signal on T2WI (arrowhead) and high signal on DWI (c). After injection of contrast medium, the cystic wall shows minor enhancement (d) Fig. 4 A 50-year-old woman with primary adult type OGCT (IIIa). (a) The spongelike changes (arrowhead) are observed in the interior of the tumor appearing as the mostly solid mass (b). The cystic contents (arrowhead) give the low signal on DWI (c) and relatively high signal on ADC map (d), while the solid part (arrow) with the relatively high signal on DWI and low signal on ADC map Zhang et al. Journal of Ovarian Research (2018) 11:46 Page 6 of 9 Fig. 5 An 18-year-old woman with histological proven SST at the right ovary. On coronal T2WI (a) and sagittal FS-T2WI (b), the solid mass (arrow) appears as the “comb” sign with centrally hyperintense signal surrounded by peripherally isointense signal. After injection of the contrast medium, the mass shows flush-in on early stage enhancement (c) and flush-out effect on late stage postcontrast image (d) acquisition data at our single institution within nearly polyps in two patients and vaginal bleeding in one patient. 10 years. To the best of our knowledge, this is the first All other accompanied lesions were incidentally detected study to describe the detailed MRI characteristics in the on MRI. In terms of tumor component, OGCTs appeared largest OGCT samples. as purely solid (8/20) to entirely cystic (4/22) mass with Owing to production of estrogen, OGCTs can be associ- various morphology. Our findings are in accordance with ated with endometrial hyperplasia, polyps, and carcinoma the literature that OGCTs has more heterogeneity than [18]. In our studied samples, we did observe endometrial OSCs. It is reported that a spongelike, multilocular cystic − 3 Fig. 6 Stem-and-Leaf Plots of the calculated ADC values (10 / mm /s) within four groups. The mean ADC value in OGCT is lower than that in other three groups (p = 0.002) with some overlap with Fig. 7 The diagnostic performance of ADC value in discriminating fibrothecoma and fibroma OGCT from OSC Zhang et al. Journal of Ovarian Research (2018) 11:46 Page 7 of 9 Table 3 Diagnostic performance of MRI in diagnosis OGCTs according to two reading protocols Protocol SEN (%) SPE (%) PPV (%) NPV (%) ACC (%) Conventional MRI 85.0(17/20) 94.0(32/34) 89.5(17/19) 91.4(32/35) 90.7(49/54) [63.9–95.0] [81.0–98.0] [68.6–97.1] [77.6–97.0] [80.1–95.9] Conventional MRI plus ADC value 95.0(19/20) 94.1%(32/34) 90.5(19/21) 96.9(32/33) 94.4(51/54) [76.4–99.1] [80.9–98.4] [71.1–97.4] [84.7–99.5] [84.9–98.1] Numbers in parentheses are the data used to calculate the percentages; Numbers in brackets are 95% confidence intervals; Conventional MRI includes T1WI, T2WI, contrast-enhanced MRI and DWI mass filled with blood degradation products is characteris- tissues with ADC value. Theoretically, as a result of high tic MR imaging sign for OGCT [2, 9, 19]. We observed cell densities and abundant cellular membranes, the similar MRI appearances in 6 cases (Fig. 3). In our study, movement of water molecule in cancer tissues is re- over 50% of OGCTs (11/20) displayed high or mixed sig- stricted on DWI images and then, the derived ADC nal intensity on T1WI images, which may be related with value should be generally lower in malignant disease the blood degradative components. Kim et al. reported than in benign or healthy tissue [8, 24]. Many studies that hemorrhage in the tumor was a common MRI finding have reported ADC value could help to distinguish in their seven cases [20]. This feature may be useful in ovarian malignant lesions from benign conditions on discriminating OGCT from OSC since it is not noticed in both 1.5 T [25–27] and 3.0 T MR system [28, 29]. In the latter group. Regarding the lesion enhancement, 22 tu- one study, the authors reported that the mean ADC − 3 2 mors examined in the present study showed mild (14/22, value of OGCT was 1000 ± 120 × 10 s/m in their 63.6%) and moderate (8/22, 36.4%) enhancement relative three cases with a 1.5 T MR machine using the same b to that of the myometrium. Avid and minor enhancement value [30], which is higher than our results(817 ± 144 × − 3 2 were not identified in OGCTs; while 4 SSTs noticed with 10 s/m ). As for MR imaging, sometimes, OGCT need avid enhancement and 12 fibromas and 4 fibrothecomas to be differentiated with fibrothecoma and ligamental with minor enhancement. Although the enhancement myoma. Our results show that the mean ADC value of type between OGCT and OSC did not differ significantly, OGCT is lower than OSC with statistically significant it could be useful in discriminating them from broad liga- difference. The similar results is not reported in previ- ment fibroids because the latter always show marked en- ously published studies. However, owing to the limited hancement after injection of contrast medium. reported cases, the comparative ADC value should be Being a problem-solving modality, MRI could provide concluded in the large cohort data. If combining the valuable information in differentiating malignant tumors ADC value, MRI yield a sensitivity of 95.0% and a speci- from benign gynecological diseases. Numerous studies ficity of 94.1% in diagnosis of OGCT, higher than with focusing on this issue have been reported with promis- conventional MRI reading session alone. Our findings ing results [15, 21, 22]. In current study, MRI could well demonstrate that there is an overlap in the ADC value indicate the morphology and components of the OGCTs between OGCT and fibroma and fibrothecoma; however, with an accuracy of approximately 90% in distinguishing there is no overlap observed between OGCT and SST. OGCT from OSC. Four lesions were preoperatively mis- The possible reason may be that cystic changes often diagnosed as fibroid (three lesions) and fibrothecoma occur in the large tumor in both OGCT and fibrothe- (one lesion) because of either small size or homogeneous coma, resulting in a wide range of measurable ADC signal intensity. Pathological fluid (a large amount of values. ascites) was a rare condition in OGCT group (one case); There are several limitations to this study. First, we re- however, it more often occur in OSC group (11 cases). trieved MR reports with suggested OGCT and OSC The true mechanism is still unknown and may result diagnosis on PACS system (within 6 years) and then, from more estrogen secretion in the latter group. No compared the MR results with pathological reports case lymphadenopathy was detected on MRI in all OGCT by case. We do believe some cases may be missed for cases, which means it is a low potential malignant tumor those not mentioned on MRI reports. So, the limited unlike ovarian epithelial cancer. In one recent study, the study samples in both OGCT and OSC group might authors also concluded that lymphadenectomy was not have influenced the final results. Second, the ADC value recommended in initial staging surgery of ovarian sex was manually measured on the selected area based on cord stromal tumor due to the low lymph node metasta- individual habits. Standardization in measurement may sis rate [23]. influence the final results. Third, our study is based on By displaying water molecule mobility (Brownian mo- 1.5 T MRI system while 3.0 T MRI has been used for a tion), DWI is considered as a functional imaging tech- decade. Owing to the variable selected b – value on nique, permitting the quantitative evaluation of tumor DWI images and the limited case studies on 3.0 T, we Zhang et al. Journal of Ovarian Research (2018) 11:46 Page 8 of 9 cannot compare the ADC value between these two mo- Received: 18 July 2017 Accepted: 20 May 2018 dalities. However, for fibrothecoma, the mean ADC value do not differ with the results reported by our pre- References vious study with 3.0 T [31]. Studies with more OGCT 1. Jung SE, Rha SE, Lee JM, Park SY, Oh SN, Cho KS, et al. CT and MRI findings of samples on 3.0 T unit still be needed to determine the sex cord–stromal tumor of the ovary. 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MR findings of primary ovarian granulosa cell tumor with focus on the differentiation with other ovarian sex cord-stromal tumors

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Abstract

Background: To describe magnetic resonance imaging (MRI) features of ovarian granulosa cell tumors (OGCTs) and compare with other sex cord-stromal tumors (OSCs) in ovary. Methods: MR findings of 18 patients with surgically confirmed ovarian granulosa cell tumor were retrospectively reviewed by two radiologists with consensus reading. All MR examinations were prospectively performed within one month. Clinical and imaging characteristics of OGCTs were evaluated and compared with OSCs (control group). Results: In 18 patients, 20 ovarian granulosa cell tumors were detected on MRI. Sixteen tumors appeared as solid or mostly solid mass (16/20), while 4 tumors as cystic mass. Pathological pelvic fluid was detected in 1 OGCT (1/18) and 11 OSCs (11/34) (p = 0.031).On T2 weighted imaging (T2WI), most of OGCTs displayed hyperintense signal and mixed signal (19/20); on T1 weighted imaging (T1WI), 11 OGCTs (11/20) displayed similar signal as on T2WI imaging. The lesion signal between OGCT and OSC differed significantly on both T1WI (p = 0.017) and T2WI (p = 0.002). Tumoral bleeding was detected in 6 OGCTs on MRI. On diffusion weighted imaging (DWI) images, OGCTs mostly appeared as high signal (16/20). Average apparent diffusion coefficient (ADC) value derived from DWI images in the OGCT group − 3 2 − 3 2 (0.84 ± 0.26× 10 mm /s was less than the control group (1.22 ± 0.47 × 10 mm /s) with statistical difference (p =0.002). Conclusions: MRI could provide important information in OGCT diagnosis. ADC value might be useful in differentiating OGCT from OSC. Keywords: Ovarian granulosa cell tumor, Sex-cord tumor, MRI, Diagnostic imaging Background with stages II–IV granulosa cell tumor [4–7]. Owing Ovarian granulosa cell tumor (OGCT) is a rare sex to the superb soft-tissue resolution and free radiation, cord-stromal tumor in ovary, accounting only 2–3% of magnetic resonance imaging (MRI) is widely used as all ovarian tumors [1]. Pathologically, OGCTs are classi- a problem-solving modality in assessment of complex fied into two subtypes: adult and juvenile form, in which adnexal masses that are indeterminate on ultrasonog- adult type occupying 95% of all OGCTs [2]. Despite raphy (US) or computed tomography (CT) [8]. Till OGCT have a favorable prognosis, an incidence of now, most of reported OGCTs in the literatures are 25–30% metastases or recurrences make it as a low published as case report and no detailed MRI knowl- malignant potential ovarian tumor [3]. Chemotherapy edges of OGCTs have been comprehensively described is recommended as adjuvant treatment for patients [6–13]. In this study, by evaluating OGCTs in our single institution, we aimed to: (1) thoroughly evalu- ate the MRI appearances of OGCTs in a large cohort * Correspondence: dr.zhanghe@yahoo.com of samples and record ADC values for each lesion; He Zhang and Hongyu Zhang contributed equally to this work. Department of Radiology, Obstetrics and Gynecology Hospital, Fudan (2) compare these features with OSCs. University, Shanghai 200011, People’s Republic of China Institute of functional and molecular medical imaging, Fudan University, Shanghai 200040, People’s Republic of China Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Zhang et al. Journal of Ovarian Research (2018) 11:46 Page 2 of 9 Methods the lesion; and presence of capsule, pelvic-free fluid and Study subjects lymph node were also noted. On T1WI, hypo-, iso-, and Between December 2009 and December 2015, 1217 con- hyperintensity were similar for the pelvic fluid, pelvic wall secutive patients with clinically suspected adnexal disease muscle, and fat signal; on T2WI, hypo-, iso-, and hyperin- prospectively underwent 1.5 T MRI examinations before tensity were similar for the pelvic bone, pelvic wall muscle, − 2 pelvic or laparoscopic surgery at our institution. The time and fat signal; on b =800 mm /s DWI images, the low, interval between the MRI evaluation and surgery was less intermediate, and high-signal intensity were similar for than one month (2–27 days; mean, 5 ± 12 days). the pelvic bone, myometrium, and endometrium. After Among them, 18 patients with histologically proven the intravenous injection of the contrast medium, the le- OGCT (24–79 years of age; average age, 45.9 ± 15.3 years) sion enhancement type was graded as follows: 1, minor were included in this study when we retrospectively re- enhancement (clearly less than the myometrium); 2, mild trieved the database on the Picture Archiving and Com- enhancement (less than the myometrium); 3, moderate munication System (PACS). Two recurrent OGCTs were enhancement (similar to the myometrium); or 4, avid excluded for further analysis because the primary imaging enhancement (more than the myometrium). ADCs were data was evaluated in another hospital. Thirty four measured manually on post-processing workstation patients with OSCs, including histologically proven scler- (Leonardo, Siemens, Germany) by one reviewer (H.Z.). osing stroma tumors (SST, n = 4), fibrothecomas (n =21), Two observers (S. X. G. and H.Z., with 6 and 10 years of and fibromas (n = 9), were included as the comparative experience in gynecological imaging, respectively), who group. Patients with any previous pelvic surgery or were blinded to the histological results independently, radiation history were arbitrarily excluded because the analyzed MRI datasets of each participant. At the end of inherent structure of the uterus may has been altered. the study, two observers were also required to determine Details of the samples studied are summarized in Table 1. the tumor etiology (benign or malignant) according to previous established criteria [14–16]. For interobserver Image acquisition discrepancies in the evaluation of uterine lesions, consen- MRI was performed using a 1.5-T MR system (Magnetom sus was achieved. Avanto, Siemens, Erlangen, Germany) with a phased-array coil. The routine MRI protocols used for assessment Statistical analyses of pelvic masses included axial turbo spin-echo (TSE) Continuous variables were expressed as the means ± T1WI, sagittal TSE T2WI, and axial/sagittal TSE standard deviation (S.D.) and compared with the un- fat-suppressed T2WI (FS T2WI). For axial images, paired t test if normally distributed or the Mann–Whit- the transverse plane was perpendicular to the long ney test if not normally distributed. A nonparametric axis of uterine body; for sagittal images, the longitudinal test (Mann–Whitney) was used to test other nonpara- plane was parallel to the main body of uterus. DWI using metric variables within each group. The area under the an echo-planar imaging two-dimensional (EP2D) se- receiver operating characteristic (ROC) curve (AUC) quence performed in the axial plane with parallel acquisi- was calculated for ADCs to discriminate OGCTs from tion technique by using b value = 0, 100, and 800 s/mm . OSCs. SPSS (version 13.0, SPSS, Chicago, USA) was Contrast-enhanced pelvic imaging was acquired at mul- used to perform statistical analyses. P values ≤0.05 were tiple phases of contrast medium enhancement in both sa- considered statistically significant. gittal and axial planes. Results Image analysis The histological results revealed 20 OGCTs in 18 pa- The location, size (the largest dimension in two orthog- tients (24–79 years of age; average age, 48.2 ± 15.1 years), onal planes), margin (regular or irregular); visibility of including 17 adult types and 1 juvenile type (Fig. 1). hemorrhagic component (high signal on T1WI) within Laparotomy was performed in 13 patients while others with laparoscopic surgery. Nine patients had regular or irregular menses, while menopause in nine patients. Table 1 Summaries of histological results in 54 ovarian sex-cord According to the international federation of obstetrics lesions detected on MRI in 52 patients and gynecology (FIGO) staging system [17], twelve Pathology diagnosis Numbers patients were classified as Ia, 4 as Ic, 1 as IIIa and 1 as Granulosa cell tumor 20 IIIc. All primary tumors were solitary lesion detected on Fibrothecoma 21 MRI, except for three primary lesions in one patient at Sclerosing stroma tumor 4 initial evaluation (Fig. 2). Most of OGCTs at presenta- Fibroma 9 tion appeared as the large mass with the average diam- indicates 20 lesions in 18 patients eter of 9.33 ± 5.43 mm. Among them, five patients were Zhang et al. Journal of Ovarian Research (2018) 11:46 Page 3 of 9 Fig. 1 A 32-year-old woman histologically proved OGCT in juvenile type (IIIc). On sagittal FS-T2WI image (a), the giant mass with irregular margin (arrow) occupy the majority of pelvis with the uterus being pushed forwardly (arrow head). (b) On contrast-enhanced images, the mass show homogeneously moderate enhancement; the necrotic area do not show enhancement (star) also accompanied by other ovarian etiologies, including Accordingly, OSCs mainly displayed as isointense (12/34) endometrial polyps (n = 2), uterine fibroids (n = 2), fol- and hyperintense signal intensity (10/34) on T2WI licular cyst (n = 1), Brenner tumor (n = 1) and fibroid images. and mucinous cystadenoma (n = 1). Vaginal discharge Neoplastic bleeding can be seen in six OGCTs, appear- was recorded in one OG patient. The details of base- ing as the patchy high signal intensity on T1WI images line characteristics for all studied samples are summa- in the tumor body (Fig. 3), which was not identified in rized in Table 2. OSC group (p = 0.000). Seventeen OGCTs were round or oval masses with regular margin (17/20) and intact MRI characteristics capsule (16/20), while 33 (33/34) and 34(34/34) observed In this studied samples, OGCTs showed varying signal in OSCs, respectively (p = 0.015). Regarding the tumor intensities on both T1WI and T2WI images. On T1WI, component, OGCTs mostly appeared as the solid or OGCTs showed various signal from low to mixed signal, mostly solid component (16/20, Fig. 4), while OSCs al- which was different to OSCs mostly appearing as hypoin- ways showed purely solid component (28/34) (p = 0.000). tense and isointense mass (p = 0.017). On T2WI, OGCTs On the post-contrast images, fourteen lesions (14/20) in mainly displayed as high and mixed signal (19/20). OGCT group displayed mild enhancement and six Fig. 2 A 61-year-old woman with primary adult type OGCT (Ia). There are oval, solid masses on right adnexal region (a, b) and right iliac fossa (c, d). Two lesions appears as similar signals with intermediate signal on both T1WI (a, c) and FS-T2WI (b, d)with intact capsule.On DWI image (e), the mass at the right iliac fossa shows relatively high signal (arrow) and low signal on the ADC map (f). The gross specimen reveals the yellow, solid mass with smooth capsule and a thin septa (g). Photomicrograph, hematoxylin and eosin stained section (× 40) shows the oval cells arrange closely with pleomorphic nuclei, prominent nucleoli and scanty cytoplasm. Note, the small vessels embed among the intercellular space (arrow head) Zhang et al. Journal of Ovarian Research (2018) 11:46 Page 4 of 9 Table 2 Basic and imaging characteristics of OGCTs Table 2 Basic and imaging characteristics of OGCTs (Continued) a a OGCTs OSCs P value OR OGCTs OSCs P value OR Imaging findings Pelvic fluid 0.031 8.130 T1 signals 20 34 0.017 Physiological/ Pathological 17/1 23/11 hypointensity 4 8 Clinical findings isointensity 5 26 Age(years) 48.2 ± 15.1 54.8 ± 15.0 0.139 (24–79) (21–81) hyperintensity 5 Vaginal discharge/bleeding 1 0 0.106 mixed 6 Menstruation T2 signals 0.002 Regular(irregular) 9(4) 18(5) 0.607 hypointensity 5 Menopause 9 16 isointensity 1 12 Accompanying lesions 0.280 hyperintensity 12 10 Yes/ No 7/12 9/25 mixed 7 7 Indicates odds ratio DWI signals 0.003 hypointensity 1 7 showed moderate enhancement. In OSC group, most of isointensity 3 11 fibromas showed minor enhancement and 4 SSTs ap- hyperintensity 16 16 peared inhomogeneously avid enhancement (Fig. 5). On mixed DWI images, 80 % of OGCTs (16/20, 80.0%) showed Margin 0.326 0.172 high signal intensities in comparison with 47% (16/34, Regular/Iregular 17/3 33/1 47.1%) in OCS group. The average ADC value (817 ± − 3 2 144 × 10 s/m ) in OGCT group was obviously less Capsule 0.015 0.800 − 3 2 than OSC group (1223 ± 473 × 10 s/m , p = 0.002) and Present/Absent 16/4 34/0 − 3 2 fibrothecoma (1209 ± 437 × 10 s/m , p = 0.001, Fig. 6). Hemorrhage 0.001 3.429 − 3 2 When use the ADC cutoff value as 619 × 10 s/m , Present/Absent 6/14 0/34 MRI could yield a sensitivity of 79.4% and a specificity Component 0.000 2.50 of 60.0% for diagnosis of OGCT, respectively; the AUC Solid(80–100% solid 828 is 0.784(95% CI:0.658–0.910) (Fig. 7). Enlarged lymph component) nodes were not observed in all OGCTs at MRI images. Cyst (80–100% cystic 41 Pathological fluid was only noted in one OGCT, component) obviously less than 11 cases in OSCs group. At multi- Solid with cystic 85 variate analysis, neoplastic hemorrhagic contents (OR: changes (others) 3.429), component (OR: 2.50) and no pathological fluid Enhancement 0.034 (OR: 8.130) are more indicative of OGCT diagnosis (homogeneous/inhomogeneous) (Table 2). On MRI, two readers accurately determined minor 16(16/0) the malignant condition in 17 cases. If combining ADC mild 14(12/2) 10(7/3) values, then they could yield a sensitivity of 95.0% and a moderate 6(5/1) 4(4/0) specificity of 94.1% for OGCT diagnosis. Three lesions were misdiagnosed as uterine fibroids and two lesion as avid 4(1/3) fibrothecoma before invasive procedures. The overall Maximum diameter (mm) 9.33 ± 5.43 8.5 ± 8.9 0.753 diagnostic performance of MRI for diagnosing OGCT is <5 6 17 listed as Table 3. 5–10 9 12 >10 5 5 Discussion −3 2 ADC values(×10 s/m ) 817 ± 144 1223 ± 473 0.002 OGCTs account for less than 5% of all malignant ovar- (558–1120) (460–2230) ian tumors, representing the most common malignant Septa 0.121 sex cord–stromal tumor in ovary origin; clinically, it may require additional chemotherapy after tumor re- Present/Absent 6/14 5/29 moval surgery [13]. Radiological knowledge of this rare Lymph node 0.913 ovarian tumor is still limited in the reported literature, Present/Absent 0/18 0/34 especially focusing on MR acquisition. Herein, we col- lected 20 OGCTs in 18 patients with prospective MR Zhang et al. Journal of Ovarian Research (2018) 11:46 Page 5 of 9 Fig. 3 A 54 -year-old woman with primary adult type OGCT (Ic). The mass shows as the purely cystic lesion with mostly high signal on T1WI (a) and T2WI (b). Note, the hemorrhagic contents locates on the left side of the tumor, representing the relatively high signal on T1WI and low signal on T2WI (arrowhead) and high signal on DWI (c). After injection of contrast medium, the cystic wall shows minor enhancement (d) Fig. 4 A 50-year-old woman with primary adult type OGCT (IIIa). (a) The spongelike changes (arrowhead) are observed in the interior of the tumor appearing as the mostly solid mass (b). The cystic contents (arrowhead) give the low signal on DWI (c) and relatively high signal on ADC map (d), while the solid part (arrow) with the relatively high signal on DWI and low signal on ADC map Zhang et al. Journal of Ovarian Research (2018) 11:46 Page 6 of 9 Fig. 5 An 18-year-old woman with histological proven SST at the right ovary. On coronal T2WI (a) and sagittal FS-T2WI (b), the solid mass (arrow) appears as the “comb” sign with centrally hyperintense signal surrounded by peripherally isointense signal. After injection of the contrast medium, the mass shows flush-in on early stage enhancement (c) and flush-out effect on late stage postcontrast image (d) acquisition data at our single institution within nearly polyps in two patients and vaginal bleeding in one patient. 10 years. To the best of our knowledge, this is the first All other accompanied lesions were incidentally detected study to describe the detailed MRI characteristics in the on MRI. In terms of tumor component, OGCTs appeared largest OGCT samples. as purely solid (8/20) to entirely cystic (4/22) mass with Owing to production of estrogen, OGCTs can be associ- various morphology. Our findings are in accordance with ated with endometrial hyperplasia, polyps, and carcinoma the literature that OGCTs has more heterogeneity than [18]. In our studied samples, we did observe endometrial OSCs. It is reported that a spongelike, multilocular cystic − 3 Fig. 6 Stem-and-Leaf Plots of the calculated ADC values (10 / mm /s) within four groups. The mean ADC value in OGCT is lower than that in other three groups (p = 0.002) with some overlap with Fig. 7 The diagnostic performance of ADC value in discriminating fibrothecoma and fibroma OGCT from OSC Zhang et al. Journal of Ovarian Research (2018) 11:46 Page 7 of 9 Table 3 Diagnostic performance of MRI in diagnosis OGCTs according to two reading protocols Protocol SEN (%) SPE (%) PPV (%) NPV (%) ACC (%) Conventional MRI 85.0(17/20) 94.0(32/34) 89.5(17/19) 91.4(32/35) 90.7(49/54) [63.9–95.0] [81.0–98.0] [68.6–97.1] [77.6–97.0] [80.1–95.9] Conventional MRI plus ADC value 95.0(19/20) 94.1%(32/34) 90.5(19/21) 96.9(32/33) 94.4(51/54) [76.4–99.1] [80.9–98.4] [71.1–97.4] [84.7–99.5] [84.9–98.1] Numbers in parentheses are the data used to calculate the percentages; Numbers in brackets are 95% confidence intervals; Conventional MRI includes T1WI, T2WI, contrast-enhanced MRI and DWI mass filled with blood degradation products is characteris- tissues with ADC value. Theoretically, as a result of high tic MR imaging sign for OGCT [2, 9, 19]. We observed cell densities and abundant cellular membranes, the similar MRI appearances in 6 cases (Fig. 3). In our study, movement of water molecule in cancer tissues is re- over 50% of OGCTs (11/20) displayed high or mixed sig- stricted on DWI images and then, the derived ADC nal intensity on T1WI images, which may be related with value should be generally lower in malignant disease the blood degradative components. Kim et al. reported than in benign or healthy tissue [8, 24]. Many studies that hemorrhage in the tumor was a common MRI finding have reported ADC value could help to distinguish in their seven cases [20]. This feature may be useful in ovarian malignant lesions from benign conditions on discriminating OGCT from OSC since it is not noticed in both 1.5 T [25–27] and 3.0 T MR system [28, 29]. In the latter group. Regarding the lesion enhancement, 22 tu- one study, the authors reported that the mean ADC − 3 2 mors examined in the present study showed mild (14/22, value of OGCT was 1000 ± 120 × 10 s/m in their 63.6%) and moderate (8/22, 36.4%) enhancement relative three cases with a 1.5 T MR machine using the same b to that of the myometrium. Avid and minor enhancement value [30], which is higher than our results(817 ± 144 × − 3 2 were not identified in OGCTs; while 4 SSTs noticed with 10 s/m ). As for MR imaging, sometimes, OGCT need avid enhancement and 12 fibromas and 4 fibrothecomas to be differentiated with fibrothecoma and ligamental with minor enhancement. Although the enhancement myoma. Our results show that the mean ADC value of type between OGCT and OSC did not differ significantly, OGCT is lower than OSC with statistically significant it could be useful in discriminating them from broad liga- difference. The similar results is not reported in previ- ment fibroids because the latter always show marked en- ously published studies. However, owing to the limited hancement after injection of contrast medium. reported cases, the comparative ADC value should be Being a problem-solving modality, MRI could provide concluded in the large cohort data. If combining the valuable information in differentiating malignant tumors ADC value, MRI yield a sensitivity of 95.0% and a speci- from benign gynecological diseases. Numerous studies ficity of 94.1% in diagnosis of OGCT, higher than with focusing on this issue have been reported with promis- conventional MRI reading session alone. Our findings ing results [15, 21, 22]. In current study, MRI could well demonstrate that there is an overlap in the ADC value indicate the morphology and components of the OGCTs between OGCT and fibroma and fibrothecoma; however, with an accuracy of approximately 90% in distinguishing there is no overlap observed between OGCT and SST. OGCT from OSC. Four lesions were preoperatively mis- The possible reason may be that cystic changes often diagnosed as fibroid (three lesions) and fibrothecoma occur in the large tumor in both OGCT and fibrothe- (one lesion) because of either small size or homogeneous coma, resulting in a wide range of measurable ADC signal intensity. Pathological fluid (a large amount of values. ascites) was a rare condition in OGCT group (one case); There are several limitations to this study. First, we re- however, it more often occur in OSC group (11 cases). trieved MR reports with suggested OGCT and OSC The true mechanism is still unknown and may result diagnosis on PACS system (within 6 years) and then, from more estrogen secretion in the latter group. No compared the MR results with pathological reports case lymphadenopathy was detected on MRI in all OGCT by case. We do believe some cases may be missed for cases, which means it is a low potential malignant tumor those not mentioned on MRI reports. So, the limited unlike ovarian epithelial cancer. In one recent study, the study samples in both OGCT and OSC group might authors also concluded that lymphadenectomy was not have influenced the final results. Second, the ADC value recommended in initial staging surgery of ovarian sex was manually measured on the selected area based on cord stromal tumor due to the low lymph node metasta- individual habits. Standardization in measurement may sis rate [23]. influence the final results. Third, our study is based on By displaying water molecule mobility (Brownian mo- 1.5 T MRI system while 3.0 T MRI has been used for a tion), DWI is considered as a functional imaging tech- decade. Owing to the variable selected b – value on nique, permitting the quantitative evaluation of tumor DWI images and the limited case studies on 3.0 T, we Zhang et al. Journal of Ovarian Research (2018) 11:46 Page 8 of 9 cannot compare the ADC value between these two mo- Received: 18 July 2017 Accepted: 20 May 2018 dalities. However, for fibrothecoma, the mean ADC value do not differ with the results reported by our pre- References vious study with 3.0 T [31]. Studies with more OGCT 1. Jung SE, Rha SE, Lee JM, Park SY, Oh SN, Cho KS, et al. CT and MRI findings of samples on 3.0 T unit still be needed to determine the sex cord–stromal tumor of the ovary. 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Sex cord-stromal tumors of the ovary: a comprehensive submit this article. review and update for radiologists. Diagn Interv Radiol. 2015;21(4):277–86. 20. Kim SH, Kim SH. Granulosa cell tumor of the ovary: common findings and unusual appearances on CT and MR. J Comput Assist Tomogr. 2002;26(5): Competing interests 756–61. The authors declare that they have no competing interests. 21. Zhang H, Zhang G-F, He Z-Y, Li Z-Y, Zhang G-X. Prospective evaluation of 3T MRI findings for primary adnexal lesions and comparison with the final Publisher’sNote histological diagnosis. Arch Gynecol Obstet. 2014;289(2):357–64. Springer Nature remains neutral with regard to jurisdictional claims in 22. Thomassin-Naggara I, Toussaint I, Perrot N. Characterization of complex published maps and institutional affiliations. adnexal masses: value of adding perfusion- and diffusion-weighted MR imaging to conventional MR imaging. Radiology. 2011;258(3):793–803. Author details https://doi.org/10.1148/radiol.10100751. Department of Radiology, Obstetrics and Gynecology Hospital, Fudan 23. Cheng H, Peng J, Yang Z, Zhang G. Prognostic significance of University, Shanghai 200011, People’s Republic of China. Department of lymphadenectomyin malignant ovarian sex cord stromal tumor: a Ultrasound, Daqing Oilfield General Hospital, Daqing, Heilongjiang Province retrospective cohort study and meta-analysis. Gynecol Oncol. 2018; 163001, People’s Republic of China. Institute of functional and molecular 148(1):91-96. https://doi.org/10.1016/j.ygyno.2017.10.022. medical imaging, Fudan University, Shanghai 200040, People’s Republic of 24. Levy A, Medjhoul A, Caramella C, Zareski E, Berges O, Chargari C, et al. China. Interest of diffusion-weighted echo-planar MR imaging and apparent Zhang et al. Journal of Ovarian Research (2018) 11:46 Page 9 of 9 diffusion coefficient mapping in gynecological malignancies: a review. 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Journal of Ovarian ResearchSpringer Journals

Published: Jun 5, 2018

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