MRI characteristics of ovarian metastasis: differentiation from stomach and colorectal cancer

Predominantly solid lesions with larger diameters of solid components, black scrunchie sign, flow void, hyperintensity within solid components on T2-weighted images, and strong contrast enhancement were characteristic findings of OMSCs compared with OMCCs. Meanwhile, predominantly cystic lesions with larger diameters of cystic components, hyperintensity within cystic components on T1-weighted images, and stained-glass appearance were characteristics of OMCCs compared with OMSCs. The black scrunchie sign was only observed in OMSCs, whereas the mille-feuille sign and stained-glass appearance were only observed in OMCCs.

In the present study, OMSCs always exhibited predominantly solid lesions, whereas OMCCs usually exhibited predominantly cystic lesions. A previous study evaluating CT findings of ovarian metastasis reported that OMSCs were more solid in nature (cystic, 0% [0/13 lesions]; mainly cystic, 30.8% [4/13 lesions]; mainly solid, 15.4% [2/13 lesions]; solid, 53.8% [7/13 lesions]) than OMCCs (cystic, 6.5% [2/31 lesions]; mainly cystic, 83.9% [26/31 lesions]; mainly solid, 6.5% [2/31 lesions]; solid, 3.2% [1/31 lesions]) [6]. Another study evaluating CT findings of OMCCs reported that had a more cystic nature (cystic: 5.0% [1/21 lesions], mainly cystic: 81.0% [17/21 lesions], mainly solid: 9.5% [2/21 lesions], or solid: 5.0% [1/21 lesions]) [17]. Therefore, OMSCs predominantly exhibited solid as opposed to OMCCs.

A previous study evaluating CT findings of ovarian metastasis reported that the longest diameter in axial CT images of OMCCs (mean, 91 mm) was significantly larger than that of OMSCs (mean, 56 mm) [6]. Other studies reported that the mean longest diameter in axial CT images of OMCCs was 92 mm [17] and the mean tumor size in MRI images was 77 mm [12]. The mean maximum tumor diameter in the present study (94 mm in OMSCs and 110 mm in OMCCs) was larger than that reported in the previous studies. This was because we measured tumor size using axial, coronal, and sagittal T2-weighted images. Although OMCCs tended to be larger than OMSCs, differentiating OMSCs from OMCC based only on tumor size is challenging.

In this study, the black scrunchie sign was occasionally observed in OMSCs but not in OMCCs. Our histological investigation revealed that central hyperintense areas on T2-weighted images corresponded to edematous stroma, whereas peripheral hypointense areas on T2-weighted images corresponded to fibrous stroma or high tumor cellularity. A previous study evaluating MRI findings of Krukenberg tumors reported that 12 of 21 (57%) Krukenberg tumors exhibited various amounts of hypointense solid components in random distribution or predominantly in the periphery on T2- and T1-weighted images, which suggested the presence of induced desmoplastic reaction or fibrosis [7]. Meanwhile, as mentioned below, OMSCs are usually hypervascular; therefore, the central areas of hypervascular OMSCs can become ischemic, thereby decreasing tumor cellularity. The characteristic black scrunchie sign of OMSCs may be caused by these histological features in the central and peripheral tumor sites. However, ovarian metastases from other primary hypervascular tumors, such as breast cancer, renal cell carcinoma, and malignant melanoma, may exhibit the black scrunchie sign. For ovarian metastases to present the black scrunchie sign, fibrous stroma or higher tumor cellularity in the peripheral areas and edematous stroma in the central areas are necessary. Further investigation is required to determine the specificity of the black scrunchie sign in OMSCs.

Takeuchi et al. reported “black garland sign”, which refers to a marked T2 hypointense thick rim of fibrous tissue surrounding the ovary in the setting of ovarian fibromatosis [18]. Ovarian fibromatosis commonly occurs in young women and is characterized by a proliferation of collagen-producing spindle cells surrounding normal ovarian structure; therefore, central ovarian parenchyma is usually accompanied by ovarian follicles. Although the “black garland sign” and “black scrunchie sign” look similar, we proposed “black scrunchie sign” for OMSCs in the present study. One of the characteristic features of OMSCs with “black scrunchie sign” is lobulated margins; however, it's difficult for “black garland sign” to convey the nuances of lobulated margins. Although ovarian fibromatosis with “black garland sign” occasionally lacks lobulated margins [19, 20], “black garland sign” is suitable for ovarian fibromatosis regardless of whether ovarian fibromatosis has lobulated margins because “black garland sign” did not define the marginal configuration. Meanwhile, “black scrunchie sign” must be naming that indicates characteristics of OMSCs, because OMSCs with “black scrunchie sign” always had lobulated margins. In addition, according to only one case report that described diffusion-weighted imaging findings of ovarian fibromatosis, the inner portion of ovarian fibromatosis, which was consistent with normal ovarian stroma, showed hyperintensity, whereas the outer fibrous portion showed hypointensity on diffusion-weighted images [19]. Meanwhile, in the present study, the peripheral areas corresponding to hypointense rim on T2-weighted images showed hyperintensity on diffusion-weighted images and low ADC values, indicating high cellularity. Therefore, SIs in the peripheral areas on diffusion-weighted images may contribute to the differentiation between OMSCs and ovarian fibromatosis.

In the present study, the SIR of solid components on gadolinium-enhanced T1-weighted images and the frequency of strong contrast enhancement and flow voids were significantly higher in OMSCs than in OMCCs. A previous study of contrast-enhanced CT reported that OMSCs displayed more prominent enhancement (none, 0% [0/13 lesions]; mild, 30.8% [4/13 lesions]; moderate, 15.4% [2/13 lesions]; dense, 53.8% [6/13 lesions]) than OMCCs (none, 0% [0/29 lesions]; mild, 6.9% [2/29 lesions]; moderate, 82.8% [24/29 lesions]; dense, 10.3% [3/29 lesions]) [6]. Strong enhancement with initial rapid rise and early washout (type 3 time-intensity curve) on dynamic contrast-enhanced imaging was observed in solid components of Kruckenberg tumors [11]. Stomach cancers are one of representative hypervascular tumors. High expression of vascular endothelial growth factor A (VEGF-A), which is a key contributor in the formation of new blood vessels from preexisting vasculature, was observed in more than half of stomach cancers, and it is intimately relevant to clinicopathological features, including TNM stage, tumor size, positive lymph nodes, and lymphovascular invasion [21]. The hypervascular nature of OMSCs may contribute to the differentiation of OMSCs from other solid ovarian tumors.

In this study, the mille-feuille sign and stained-glass appearance were observed only in OMCCs. A previous study evaluating the differentiation of MRI findings between OMCCs and primary ovarian cancers reported that the mille-feuille sign was more frequently observed in OMCCs than in primary ovarian tumors (8/41 [19.5%] vs. 1/36 [2.8%], p = 0.011) [12]. The frequency of the mille-feuille sign in OMCCs in this study (6/25, 24%) was almost consistent with that in the previous study. Therefore, the mille-feuille sign can be considered a low-frequency but high-specificity MRI feature of OMCCs.

Our study had several limitations. First, this was a single-center retrospective analysis, and the number of patients enrolled was relatively small. In particular, the number of histopathologically proven cases among patients with OMSC was considerably small because OMSCs tend to be accompanied by peritoneal dissemination and treated by chemotherapy. This limitation significantly impacts the study's statistical power and generalizability of the findings. Second, the study did not include ovarian metastases from the mucinous histological subtype of stomach cancer. This is an important limitation, as mucinous gastric carcinomas can resemble colon carcinomas, often containing more cystic components. Third, because dynamic contrast-enhanced MRI was performed on six patients only, its usefulness could not be determined. Dynamic contrast-enhanced imaging may reveal the hypervascular nature of OMSCs. Third, the MRI findings were obtained using MRI scanners with different magnetic field strengths (1.5 T or 3 T), which could potentially influence the calculated ADC values.

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