Anaplastic ovarian mucinous carcinoma with yolk sac differentiation: a rare case report and literature review

Introduction

Ovarian mucinous tumors are relatively common epithelial tumors of the female reproductive system. Like other epithelial tumors, mucinous tumors are classified into benign, borderline, and malignant types. Comparing to other epithelial tumors, for instance ovarian serous carcinoma, mucinous tumors exhibit greater heterogeneity. In a few percent of the mucinous tumor cases, whether the tumor is benign, borderline or malignant, it may be accompanied by mural nodules, for instance sarcomatoid nodules, sarcoma and anaplastic carcinoma (1). Of the three kinds of mural nodules, sarcomatoid nodule is benign, meanwhile, the latter two are highly aggressive and malignant components. Due to the varying sizes and morphological diversity of the mural nodules, during the clinical pathological treatment of the cases, they might sometimes been miss noticed or misdiagnosed.

Meanwhile, recently, there have been increasing amounts of case reports of epithelial tumors from female genital tract coexisting with germ cell tumors. The most common subtype of epithelial tumor is endometrioid carcinoma of the uterus or ovary, and the most frequent germ cell tumor is yolk sac tumor (YST) (2,3). However, as for the ovarian mucinous tumors associated with YST like components, up to date, only 7 cases have been reported (3-9). Regarding the origin of ovarian mucinous tumors combined with YST, there have been varying perspectives. Some people think the two tumor types develop independently, some researchers suggest the tumor is a special type of mixed germ cell tumor and the mucinous and YST components may both arise from germ cells. Meanwhile, there were also perspectives that the mucinous tumor might represent intestinal epithelial differentiation within the YST, or even, the YST could be a dedifferentiated form of mucinous tumor (8).

Here we present a rare case of ovarian anaplastic mucinous carcinoma with YST component and reviewed the literature for all the seven currently reported cases (Table 1). Detailed displaying of the clinical features of these tumors shall aiding better understanding of the diagnosis, clinicopathological features as well as prognosis of the extremely rare disease. We present this article in accordance with the CARE reporting checklist (available at https://acr.amegroups.com/article/view/10.21037/acr-2025-255/rc).

Case presentation

A 62-year-old female patient was admitted due to intermittent lower abdominal pain with progressive abdominal distension for over 2 years, and since the past 2 months before admitted in hospital, the symptoms including frequent and urgent urinary as well as diarrhea had been increasingly stronger. Ultrasound of uterus and adnexa detected a cystic echoic area (244.6 mm × 94.5 mm) superior to the right uterus, and abdominal and pelvic computed tomography (CT) scan also indicated a round, cystic-solid and hypodense lesion with septations [CT value 10–35 Hounsfield Units (HU)] in the pelvis. More importantly, multiple enlarged lymph nodes were noted in the retroperitoneum and along bilateral iliac vessels, indicating potential cancer retroperitoneal and lymph nodes metastasis. Preoperative blood test of the patient revealed multiple elevated tumor biomarkers including cancer antigen 125 (CA125), carbohydrate antigen 19-9 (CA199), carbohydrate antigen 242 (CA242) and carcinoembryonic antigen (CEA). No similar medical history or other cancer experience including Lynch syndrome was found by herself or family before.

To deal with the giant pelvic mass, the patient then went through hysterectomy with bilateral salpingo-oophorectomy, pelvic and para-aortic lymphadenectomy, omentectomy, and appendectomy, after aspiration of nearly 2,000 mL of yellow gelatinous ascitic fluid, a giant 21 cm × 15 cm × 6.5 cm cystic-solid tumor with surface rupture and dense adhesions to the omentum and intestines was found in the right ovarian (Figure 1A). Although the tumor was mostly cystic, the solid area with friable, gray-white cut surfaces comprised nearly 1/3 of the tumor mass.

Figure 1 The gross tumor mass and representative morphology features of the case. (A) The gross features of the postoperative cystic-solid ovarian tumor mass. (B-F) H&E staining for showing the classic morphology features of the three distinct components of the tumor, including (B) the cystic areas which was revealed to be borderline mucinous tumor featuring epithelial rupture, mucin extravasation, and surrounding desmoplastic reaction (magnification: 40×, bar represents 160 µm). (C) The solid component exhibited heterogeneous morphology, and the majority was consisted of polygonal cells with abundant vacuolated or eosinophilic cytoplasm, large vesicular nuclei, and prominent nucleoli of varying sizes (magnification: 100×, bar represents 80 µm). (D) Some cells in the solid region displayed eccentric nuclei resembling, the morphology were rhabdoid like, and the pathological mitotic figures in these cells were usually high (>15/10 HPF, magnification: 100×, bar represents 80 µm). (E) Some cells with greater atypia were also noted in the solid region, hyperchromatic nuclei, tumor giant cells, syncytial-like cells and prominent necrosis were observed in this region (magnification: 100×, bar represents 80 µm). (F) The microcystic reticular regions with flattened to low cuboidal cells containing small nucleoli, the microcystic spaces were filled with mucin (magnification: 100×, bar represents 80 µm). H&E, hematoxylin-eosin; HPF, high-power fields.

Pathological examination of the tumor revealed three different kinds of components, including cystic areas, solid areas, and microcystic reticular areas. Based on pathological microscope observation, most of the cystic areas were revealed to be intestinal-type borderline mucinous tumor with mucin extravasation and surrounding desmoplastic reaction (Figure 1B). Meanwhile, highly heterogeneous cells were observed in the solid areas, some were sheet-like, polygonal cells with vacuolated or eosinophilic cytoplasm as well as vesicular nuclei (Figure 1C), prominent nucleoli and frequent pathological mitoses [>15/10 high-power fields (HPF), Figure 1D], and some cells were rhabdoid like, significantly atypia tumor giant cells with bizarre hyperchromatic nuclei, syncytial-like cells and tumor necrosis could be observed in this area (Figure 1E). Moreover, as for the microcystic reticular areas, they were mostly composed of flattened or cuboidal cells with small nucleoli, and mucin-filled microcysts were the characteristic morphology feature in this area (Figure 1F).

Immunohistochemical (IHC) analysis result revealed that although all three cystic, solid and microcystic reticular areas (Figure 2A-2C) were positively stained with AE1/AE3 (also named as CK, Figure 2D-2F), the other proteins were differently stained in these areas. For instance, the mucinous epithelium cells lining in the cyst areas were PAX-8 and CK20 positively staining. Meanwhile, the sheet-like and polygonal cells in the solid area were mostly stained with CD99, and SALL4, Vimentin, CK20 were focally stained in this area. Interestingly, as for the microcystic reticular areas, a significantly different mode of proteins staining was observed, the cells in this area were diffusely strong stained with SALL4 and CD99, meanwhile, Glypican-3 and CD117 were partial positive. A nearly 70% positive rate of Ki67 were observed in all three areas, meanwhile, none CK7, WT-1, AFP, OCT3/4, CD30, Syn, CgA, CD56, ER, PR, Inhibin-α, GFAP or NSE staining was observed in either of the areas (Figure 2G-2X). Furthermore, molecular genes analysis revealed that no TP53, KRAS, NRAS, BRAF or PIK3CA genes mutations was observed in either of the three area cells.

Figure 2 Representative IHC staining results in the three distinct regions of the case. (A-C) The representative H&E morphology features of the three distinct regions of the case, including in the (A) cystic regions, (B) solid regions and (C) microcystic reticular regions. (D-F) IHC staining of CK in the three different regions of the case, including in the (D) cystic regions, (E) solid regions and (F) microcystic reticular regions. (G-I) IHC staining of Vimentin in the three different regions of the case, including in the (G) cystic regions, (H) solid regions and (I) microcystic reticular regions. (J-L) IHC staining of PAX8 in the three different regions of the case, including in the (J) cystic regions, (K) solid regions and (L) microcystic reticular regions. (M-O) IHC staining of SALL4 in the three different regions of the case, including in the (M) cystic regions, (N) solid regions and (O) microcystic reticular regions. (P-R) IHC staining of AFP in the three different regions of the case, including in the (P) cystic regions, (Q) solid regions and (R) microcystic reticular regions. (S-U) IHC staining of Glypican-3 in the three different regions of the case, including in the (S) cystic regions, (T) solid regions and (U) microcystic reticular regions. (V-X) IHC staining of P53 in the three different regions of the case, including in the (V) cystic regions, (W) solid regions and (X) microcystic reticular regions. Magnification: 40×, bars represent 160 µm in all pictures. AFP, alpha-fetal protein; H&E, hematoxylin-eosin; IHC, immunohistochemical.

Based on the distinct morphology and IHC staining results of the tumor, the cystic area was pathologically diagnosed as ovarian mucinous tumor with borderline features, the solid area was supported to be anaplastic carcinoma, and the microcystic reticular area was revealed to be YST. The case was finally diagnosed as ovarian mucinous carcinoma with anaplastic region and YST differentiation. Considering previous reported cases have described ovary epithelial tumours with yolk sac elements in Lynch syndrome (10,11), IHC experiment of the mismatch repair (MMR) proteins was additionally performed in the case, and the result revealed that in all three solid, microcystic reticular and cystic areas (Figure 3A-3C), four MMR proteins including MLH1 (Figure 3D-3F), PMS2 (Figure 3G-3I), MSH2 (Figure 3J-3L) and MSH6 (Figure 3M-3O) were all positively stained, indicating the proficient mismatch repair (pMMR) state of the case.

Figure 3 IHC staining of MMR proteins in the three regions of the case. (A-C) Representative H&E features of the three regions in the case, including in the (A) solid region, (B) microcystic reticular region and (C) cystic region. (D-F) IHC staining of MLH1 in the three different regions of the case, including in the (D) solid region, (E) microcystic reticular region and (F) cystic region. (G-I) IHC staining of PMS2 in the three different regions of the case, including in the (G) solid region, (H) microcystic reticular region and (I) cystic region. (J-L) IHC staining of MSH2 in the three different regions of the case, including in the (J) solid region, (K) microcystic reticular region and (L) cystic region. (M-O) IHC staining of MSH6 in the three different regions of the case, including in the (M) solid region, (N) microcystic reticular region and (O) cystic region. Magnification: 100×, bars represent 100 µm in all pictures. H&E, hematoxylin-eosin; IHC, immunohistochemical; MMR, mismatch repair.

The patient was treated with postoperative intraperitoneal hyperthermic chemotherapy with bleomycin, etoposide and cisplatin, 33 days after the surgery, blood test revealed a declined level of tumor markers CA125 (132 IU/mL dropped to 52.30 IU/mL) and CA199 (180 IU/mL dropped to 34.40 IU/mL). However, 62 days after the surgery, the tumor recurred and the patient was admitted in the hospital again. Now it’s 3 months after the patient’s first surgery, since the patient is not suitable for a second surgery, the recurred tumor has now again filled with the patient abdominal cavity. The patient is still alive, but her health condition is extremely poor.

All procedures performed in this study were in accordance with the ethical standards of the institutional and/or national research committee(s) and with the Declaration of Helsinki and its subsequent amendments. Presentation of the case and use of her post-operation samples in the study was approval by the Ethics Committee of Second Hospital of Shanxi Medical University (No. [2025]YX248). Written informed consent was obtained from the patient for the publication of this case report and accompanying images. A copy of the written consent is available for review by the editorial office of this journal.

Discussion

Ovarian mucinous tumor with anaplastic carcinoma mural nodule was firstly reported by Prat et al. (12), some similar cases were reported after that. To date, the largest cohort which included 34 cases were released by Provenza et al. (1). In that study, besides the carefully discussion of clinicopathological characteristics and prognosis of the disease, the researchers in detailed described the pathological morphology of ovarian mucinous tumors with anaplastic carcinoma mural nodules, especially different types of histological morphology patterns of the disease, including firstly the diffusely arranged rhabdoid cells with large, clear or eosinophilic cytoplasm, eccentrically placed nuclei, and one or more prominent nucleoli. Secondly, the sarcomatoid cells which were predominantly arranged in a herringbone pattern and composed of atypical cells with vesicular nuclei. Thirdly, the pleomorphic cells which exhibit mixed features of rhabdoid and sarcomatoid cells. Due to the variable size and morphological diversity of mural nodules, the lesions are seriously prone to misdiagnosis (13).

Here were presented a female case which besides the rhabdoid and pleomorphic cells, also exhibited a special microcystic reticular cellular structure. At first, we almost misdiagnosed the case as mixed germ cell tumor, since based on pathological hematoxylin-eosin (H&E) staining, the microcystic reticular cellular structure was most likely to be YST, and the solid nests of cells with vesicular nuclei were similar with embryonal carcinoma, the polygonal rhabdoid cells with inflammatory stroma might be dysgerminoma, the syncytiotrophoblast-like cells surrounding necrotic areas were likely to be choriocarcinoma, meanwhile, the mucinous cystic regions could also be intestinal-type differentiation in a teratoma, all these structures indicated the possible diagnosis of the case as mixed germ cell tumor (14,15). However, mixed germ cell tumor predominantly occur in young patients and are exceedingly rare in the elderly, and also, next step IHC analysis revealed that although the microcystic reticular cells were positive for SALL4, Glypican-3, and CD117 which supported the YST differentiation of the region, the other cells were negative for neither of WT-1, AFP, OCT3/4, CD30, Syn, CgA and CD56 indicators, therefore, the possible diagnosis of neither mixed germ cell tumor nor other cancers for instance teratoma with malignant transformation, poorly differentiated Sertoli-Leydig cell tumor with mucinous heterologous elements, malignant Brenner tumor with mucinous metaplasia , juvenile granulosa cell tumor with mucinous cysts, dysgerminoma with mucinous cysts were all ruled out.

To clarify the final diagnosis of the disease, we carefully reorganized the clinical and pathological information of the case which indicated that this is an elderly female patient presented with a unilateral ovarian cystic-solid tumor, the blood test revealed that the level of multiple tumor biomarkers including CA125 and CA199 were elevated, supporting the primary diagnosis as ovarian cancer. Pathologically, the tumor was composed of three different kinds of components, including cystic areas, solid areas, and microcystic reticular areas. Based on pathological H&E staining and IHC analysis result, the microcystic reticular area was supported to be YST component, meanwhile, the cystic area represented a borderline mucinous tumor, and the rest solid areas were composed of rhabdoid and pleomorphic cells which were positively stained with CK, suggesting the probable diagnosis as anaplastic carcinoma. Given the anaplastic carcinoma occupied nearly one-third of the tumor without grossly discernible nodules, instead of ovarian mucinous tumor with anaplastic carcinoma mural nodules combined with YST component, the case was finally diagnosed as mucinous anaplastic carcinoma combined with YST component to emphasize the clinical significance of its aggressive nature attributing to the big portion of anaplastic carcinoma regions.

To better understand the biological features of the disease, we conducted an extensive literature review. And the published studies revealed that although certain malignant tumors that were originated from female genital tract which were mostly epithelial tumors have been reported to coexist with YST in the elderly patients, the tumors were hardly mucinous type (14,16-20). For instance, in 2016, McNamee et al. reported 18 cases of YST in women over 40 years old, and 11 of the 18 cases were combined with epithelial tumors, including 5 cases of high-grade serous carcinomas (HGSC), 2 cases of endometrioid adenocarcinomas (EC), 1 borderline clear cell adenofibroma (CCA), 1 clear cell carcinoma (CCC), 1 serous tubal intraepithelial carcinoma (STIC), and 1 large cell neuroendocrine carcinoma (NEC) (16).

As for the ovarian mucinous tumors combining with YST components, to data, only 7 cases have been reported. Together with the case we presented in the study, a total of 8 cases were currently known. Here, we carefully reviewed the clinical and pathological information of the 8 cases for aiding better understanding of the disease (4-9). The ages of the 8 cases range between 32 to 82 years old with the median age as 64 years old. The blood tests revealed that alpha-fetal protein (AFP) was elevated in 3 of the cases, and regarding the mucinous tumor that was coexisted with YST component, 1 of the 8 cases was benign mucinous cystadenoma, 4 of the 8 cases were borderline mucinous tumor, meanwhile, the other 3 cases were malignant mucinous carcinoma. The combined YST components almost exclusively localized to solid areas of these cases, and under microscope, YST components could be microcystic, reticular, glandular or solid, and S-D bodies were observed in 2 cases.

Moreover, as for the FIGO stages of the cases, 4 of the cases were stage I (including 1 stage IA and 3 stages IC), 3 cases were stage III, and the other case was stage IV. Molecular genes analysis results revealed various results, TP53 mutation was detected in 1 case, and KRAS was found mutated in another case, meanwhile, CDKN2A/CDKN2B deletion was found in some other cases (21-23). In our case, we detected the KRAS, NRAS, BRAF and PIK3CA status in each of the three regions and none mutation was found in either of the cellular components. The different genes detection results in these cases suggested the various molecular mechanism behind the tumor development. The most threatening fact was that of the 8 cases, 5 cases underwent tumor recurrence or metastasis within 1 year, and 3 cases were dead. The aggressive behavior of these tumors evidenced by rapid recurrence and poor survival underscores the need for careful morphological and IHC evaluation to avoid misdiagnosis. The presence of TP53/KRAS mutations and blood test AFP elevation may aid in the diagnosis and prognostic stratification of the cases.

Conclusions

In conclusion, in line with non-mucinous epithelial tumors, ovarian mucinous tumors, whether benign, borderline, or malignant, may also harbor germ cell tumor components (13,24-27). In the study, we present a case of ovarian mucinous anaplastic carcinoma with YST differentiation, literature review of this type of tumor indicated the highly aggressive nature of this tumor, pathologists should pay high attention on the gross examination and under microscope diagnosis of this kind of tumors.

Acknowledgments

We sincerely appreciate the patient for agreeing to publish her case for science purpose. Her tissue sample was very important resource for the study, and it is our honor to acknowledge her contribution.

Footnote

Reporting Checklist: The authors have completed the CARE reporting checklist. Available at https://acr.amegroups.com/article/view/10.21037/acr-2025-255/rc

Peer Review File: Available at https://acr.amegroups.com/article/view/10.21037/acr-2025-255/prf

Funding: The work was supported by National Natural Science Foundation China (No. 82572996), and Natural Science Foundation of Shanxi Province in China (Nos. 202203021222393, 202303021222333, 202403021211135 and 202403021222467).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://acr.amegroups.com/article/view/10.21037/acr-2025-255/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. All procedures performed in this study were in accordance with the ethical standards of the institutional and/or national research committee(s) and with the Declaration of Helsinki and its subsequent amendments. Presentation of the case and use of her post-operation samples in the study was approval by the Ethics Committee of Second Hospital of Shanxi Medical University (No. [2025]YX248). Written informed consent was obtained from the patient for the publication of this case report and accompanying images. A copy of the written consent is available for review by the editorial office of this journal.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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