Open Access

Malignant mixed Müllerian tumor of the fallopian tube: Case report and literature review

  • Authors:
    • Alexandra Lavinia Cozlea
    • Mihai Gheorghe
    • Szilard Leo Kiss
    • Anas Fandi
    • Mihai Stanca
    • Simona Mocan
    • Mihai Emil Căpîlna
    • Nicolae Bacalbașa
    • Andreea Anamaria Moldovan
  • View Affiliations

  • Published online on: December 28, 2021     https://doi.org/10.3892/etm.2021.11100
  • Article Number: 177
  • Copyright: © Cozlea et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Carcinosarcoma, also known as malignant mixed Müllerian tumor (MMMT), includes both malignant epithelial and mesenchymal elements. While the endometrium is the most frequent known site for carcinosarcomas, their development in the fallopian tube is rare condition, only accounting for 0.1 to 0.5% among all gynecological malignancies. Fallopian tube MMMT is associated with an aggressive progression. A total of 94 previous case reports were reviewed and divided, after applying the exclusion criteria, into 2 groups: No evidence of disease (NED) Group including 33 patients reported to be without any residual disease at the end of the follow‑up period; death of disease (DOD) Group including 51 patients who died due to the progression of fallopian carcinosarcoma or its complications. The gathered data were statistically analyzed together with a case from our clinical experience: a 65‑year‑old postmenopausal patient with a final histological diagnosis of fallopian carcinosarcoma staged FIGO IC2, synchronous with a serous endometrial intraepithelial carcinoma. Patient age between 41 and 60 years, symptoms at presentation and computed tomography (CT)/magnetic resonance imaging (MRI) tumor evidence are prognostic factors (P<0.05). Omentectomy [odds ratio (OR)=0.3545] and pelvic lymphadenectomy (OR=0.3732) were found to be significant factors for survival (P<0.05). Fimbrial localization of the tumor is a negative prognosis factor (OR=4.263), as well as the heterologous type of tumor (OR=2.880). Chemotherapy was found to improve survival (OR=0.2679) while radiotherapy had no influence on patient prognosis. Reporting these rare cases could be essential for obtaining more precise information regarding the treatment and prognosis of patients with MMMT of the fallopian tube, in order to improve patient survival and quality of life.

Introduction

Malignant mixed Müllerian tumors (MMMT), widely known as carcinosarcomas, are extremely rare and highly malignant neoplasms when diagnosed in the female genital tract (1). Field literature recognizes the uterus, cervix and ovary as the most common primary sites of these malignancies (2). While the endometrium is the most frequent known site for carcinosarcomas, their development in the fallopian tube is a rare condition, only accounting for 0.1 to 0.5% among all gynecological malignancies (3,4). Usually fallopian carcinosarcomas develop in the fifth to sixth decade in postmenopausal women, and the preoperative non-specific aspects and multiple similarities to hydrosalpinx, ovarian malignancies or tuboovarian abscess lead in most cases to a misdiagnosis. Symptomatology has no specific elements; the presenting symptom being usually abdominal pain mostly in the hypogastric area, followed by abnormal vaginal bleeding or abdominal distension, and exceptionally with an acute clinical picture (5,6). Due to all the mentioned elements, a diagnosis of certitude is extremely difficult to confirm, often being verified only by the final histology result, but in some cases cervical cytology or endometrial curettage may guide the specialist (7).

Regarding the histological features, MMMTs integrate both stromal and epithelial, carcinomatous and sarcomatous elements, typically high grade, with a significantly aggressive progress and a poor patient prognosis. In addition, this type of tumor usually metastasizes and disseminates rapidly among the pelvic organs in approximately 60% of the cases, but also to the peritoneum, paraaortic lymphatic nodes, even distant metastasis to the lungs, liver or bones (8,9).

The present article presents one case of fallopian MMMT with heterologous elements synchronous with an endometrial serous carcinoma surgically operated on in the First Obstetrics and Gynecology Clinic, ‘George Emil Palade’ University of Medicine, Pharmacy, Science, and Technology, Târgu Mureș, Romania. In addition, a meta-analysis of the medical literature was performed in order to find correlations between the patient medical data and prognosis.

Patients and methods

A synchronous fallopian MMMT together with an early-stage endometrial serous carcinoma is further described. Moreover, the present study incorporates all the data found in field literature regarding MMMTs, statistically analyzed in order to identify potential associations between specific characteristics and the described management of each patient and the post-treatment survival. The data available in English literature was found through Medline search, using the following keywords: ‘fallopian carcinosarcoma’, ‘tubal carcinosarcoma’ and ‘fallopian malignant mixed tumor’.

During the Medline search, 94 patients were reported between 1902 and 2019. Ten cases were excluded because the patients were lost to follow-up, or because of the lack of reported information. Finally, 84 cases presented in Table I (4,5,7,8,10-69), together with the one case surgically operated on by our team were included in the present analysis. The reported cases were divided into 2 groups according to patient outcome at the end of the follow-up period in each case: No Evidence of Disease (NED) group including 33 patients reported to be without any residual disease at the end of the follow-up period; death of disease (DOD) group including 51 patients who died due to the progression of fallopian carcinosarcoma or its complications. The collected data concerned the patient age at diagnosis, signs and symptoms at presentation, imaging findings, the accuracy of the first diagnosis, surgical, histological and oncological aspects.

Table I

Previously reported cases of fallopian MMMT.

Table I

Previously reported cases of fallopian MMMT.

Patient no.Author (Refs.)Year of reportAge of patients (years)FIGO stageOutcome
1Motta (10)192614IVDOD
2Zacho (11)1933N/DIIICDOD
3Platz (12)194058IVDOD
4Bochner (13)196158N/DDOD
5Williams and Woodruff (14)196335IVDOD
6Malnasy and Gaal (15)196345IIBDOD
7McQueeney et al (16)196469IIBDOD
8De Queiroz and Roth (17)197064IIICDOD
9Wu et al (18)197357IANED
10Acosta et al (19)197446IIBDOD
11Acosta et al (19)197462IVDOD
12Acosta et al (19)197448ICDOD
13Aggarwal et al (20)197650IIICDOD
14Manes and Taylor (21)197676IADOD
15Manes and Taylor (21)197674IADOD
16Manes and Taylor (21)197647IANED
17Manes and Taylor (21)197658IANED
18Henderson et al (22)197762IIBDOD
19Jain (23)197752IANED
20Oka et al (24)197857IANED
21Hanjani et al (25)198062IVDOD
22Viniker et al (26)198063IANED
23Holst and Erichsen (27)198165IIICNED
24O'Toole et al (28)198271IVDOD
25Egorov (29)198253N/DDOD
26Kahanpää et al (30)198365IIINED
27Deppe et al (31)198468IIIBNED
28Punnonen et al (32)198568IIICDOD
29Buchino and Buchino (33)198761IIICDOD
30Yabushita et al (34)198753IIANED
31Chen and Wolk (35)198856ICDOD
32Muntz et al (36)198957IIICDOD
33Muntz et al (36)198960IIIADOD
34Muntz et al (36)198961IVDOD
35Axelrod et al (37)198962IIICNED
36Kinoshita et al (38)198979ICNED
37van Dijk et al (39)199045IIADOD
38van Dijk et al (39)199067IIIBDOD
39Seraj et al (40)199062IIICDOD
40Seraj et al (40)199053IIICDOD
41Liang et al (41)199063IIICDOD
42Chang et al (42)199166IIIDOD
43Chiou et al (43)199163IIICDOD
44Imachi et al (5)199260IIICDOD
45Imachi et al (5)199267IVDOD
46Moore et al (44)199266IIICDOD
47Carlson et al (45)199372IIICDOD
48Carlson et al (45)199356IIICNED
49Carlson et al (45)199360IBNED
50Carlson et al (45)199344IANED
51Carlson et al (45)199359IIIBNED
52Weber et al (46)199374IIANED
53Zorlu et al (47)199438IIIDOD
54Horn et al (48)199662IIIBDOD
55Horn et al (48)199664IIBDOD
56Horn et al (48)199669IIICDOD
57Horn et al (48)199671IVDOD
58Ebert et al (49)199870IANED
59Maitra et al (50)200429IIIADOD
60Moustafa et al (51)200475IIADOD
61Humble and Carter (52)200463IIICDOD
62Lim et al (53)200457IANED
63Gagner and Mittal (54)200577IVDOD
64Kuroda et al (55)200565IIBDOD
65Das et al (56)200549IIINED
66Das et al (56)200580IIBDOD
67Hudelist et al (57)200657IIBNED
68Kuroda et al (58)200777IIICDOD
70Kawaguchi et al (59)200869ICNED
71Kourea et al (60)200872IIICNED
72Piura et al (61)200946IIICNED
73Shen et al (8)201058IIIDOD
74Malhotra et al (62)201260IIICDOD
75Watanabe et al (7)201253IIICNED
76Tsai et al (63)201257IIIANED
77Gupta and Jenison (64)201174IIICDOD
78Takemoto et al (65)201556IIICDOD
79Narin et al (66)201568IIANED
80Vale-Fernandes et al (67)201557IIANED
81Ji et al (4)201560IIICNED
82Monsalve et al (68)201571IIINED
83Zhang et al (1)201870IIIBNED
84Bécsi et al (69)201970IIIBNED

[i] MMMT, malignant mixed Müllerian tumors; NED, no evidence of disease; DOD, death of disease; N/D, not determined.

Statistical analysis

Data were gathered from the previously reported cases in the literature and processed using Microsoft Excel. For the statistical analysis, the GraphPad InStat software (GraphPad Software, Inc.) was used, made available by ‘George Emil Palade’ University of Medicine, Pharmacy, Science, and Technology of Târgu Mureș, Romania. Quantitative variables were revealed as mean and median, qualitative and categorical variables being expressed as integer and percentage values. For all variable groups the normality of distribution was evaluated by applying Kolmogonov-Smirnov test. Quantitative analysis was performed using the Student's t-test for groups with Gaussian distribution of values and Mann-Whitney test for groups with abnormal distribution. Inferential statistics consisting in odds ratio (OR) calculations for mentioned pre-treatment, surgical, histopathological and oncological data was conducted with Fisher's exact test, this offering a higher accuracy. The level of statistical significance was established at a P-value of 0.05, with a 95% confidence interval for all the investigated parameters.

Case report Clinical and paraclinical findings

A female patient aged 65, primigravidae, primiparous presented with a moderate lower abdomen discomfort and a light atypical vaginal bleeding for 2 weeks. The patient was postmenopausal from the age of 50, this being the first bleeding episode. At the clinical gynecologic exam, no vaginal or cervical macroscopic pathologies were detected, but abdominal palpation revealed a moderate sensitivity in the hypogastric area, accentuated in both iliac fossa. Transvaginal ultrasonography uncovered images suggesting a bilateral hydrosalpinx of 92x33 mm on the right side and 45x12 mm on the left side, also showing an intracavitary image pleading for a large endometrial polyp of 19x23 mm. These ultrasonography findings did not raise any suspicions or the necessity of substantial imagistic explorations, due to the absence of criteria which could indicate a neoplastic disease. After appropriate counseling and considering the patient age and associated medical conditions, the patient was scheduled for an operative hysteroscopy followed by laparoscopy and histopathological exam.

Intraoperative appearance

On October 2019, the patient was admitted to the First Obstetrics and Gynecology Clinic, Targu Mures Emergency Clinical County Hospital, Romania, for a combined hysteroscopic and laparoscopic approach. Under general anesthesia, a diagnostic hysteroscopy was performed, which revealed an atrophic endometrium with permeable tubal ostia together with an endometrial tumor suggesting a polyp. Thus, a hysteroscopic polypectomy was performed and the specimen was sent for histopathological examination.

During the laparoscopic phase, extended perianexial adhesions on the left side were found and an atrophic uterus and ovaries. Both fallopian tubes were enlarged and tumoral, similar to a hydrosalpinx with thick walls, sinuous, measuring 7x2x3 cm on the left side and 8x7x4 cm on the right side, without noticeable vegetation on the tubal surface but with mixed content, both fluid and cerebroid, expelled through the pavilion. A bilateral adnexectomy was performed and the specimen was carefully extracted through a mini laparotomy in the left iliac fossa and sent for frozen section, which confirmed malignancy. Subsequently, a laparotomy approach was chosen and a total hysterectomy, pelvic and paraaortic lymphadenectomy, appendectomy, total omentectomy were performed, without intraoperative complications and with no residual disease in the abdomen. Her postoperative recovery was uneventful under antibiotic prophylaxis and anticoagulant treatment. The patient was discharged on the 7th postoperative day. After surgery and the final pathology result, the patient completed 6 cycles of systemic chemotherapy with carboplatin and paclitaxel and has NED.

Histopathological examination

Macroscopic and microscopic features of the two excised fallopian tubes are presented in Figs. 1 and 2. The right fallopian tube measured 110x45 mm, exhibited an increase in volume and dilated on the entire length, presenting a ruptured serosa in several portions and a friable white tumoral mass which filled and enlarged the lumen in all performed sections, with many necrotic associated with hemorrhagic areas. The left fallopian tube measured 50x15 mm, with dilated portions and the examined sections unveiling a white vegetant tumoral mass extended in the entire length of the organ.

Microscopically, in both fallopian tubes, the same type of infiltrative tumor was found, with mixed aspect: an epithelial component of high-grade serous carcinoma associated with heterologous elements, such as chondrosarcoma, liposarcoma and undifferentiated sarcoma, with extended areas of necrosis and hemorrhage. In the tubal epithelium, multiple serous intraepithelial carcinoma zones with an increased mitotic index were observed. In the right tube, the tumor was found to infiltrate the entire wall, and tumoral cells were found on the serosa. In the left tube, the tumor infiltrated only the muscular wall. The microscopic examination revealed lymphovascular emboli but without tumoral invasion in the ovaries and without metastases in all the 58 pelvic and paraaortic removed lymph nodes. The omentum and appendix were tumor-free.

Regarding the uterus, the endometrial mass appeared as a polypoid lesion with predominant atrophic glands, but with serous endometrial intraepithelial carcinoma features on the surface, with no invasion. The microscopic aspect is presented in Fig. 3. The final histological diagnosis was bilateral tubal carcinosarcoma (MMMT) and synchronous serous endometrial intraepithelial carcinoma, FIGO stage IC2 and pTNM stage pT1c2.

Results

The pre-treatment assessment of the cases previously reported in the literature (4,5,7,8,10-69) is presented in Table II. The mean age was not significantly different in the study groups. Regarding the patients' repartition by decades, the age interval 41-60 years was a statistically significant protective factor towards death (OR=0.3684, P=0.0419). Patients' age <40 years and 61-80 years represented a higher risk for a negative outcome, although the results were not statistically significant. Regarding the symptoms, the abdominal distention reported in the died of disease (DOD) group was confirmed to be the only one directly affecting prognosis and could be considered a risk factor for death with an OR=3.955 (P=0.0226). In addition, ascites was found to influence the outcome, being present in 17.6% of the patients included in the DOD group, but the calculated P-value for its OR was above the level of statistical significance. Tumor evidence on imaging could better guide treatment, prolonging the life of patients (OR=0.2500, P=0.0216). Cancer antigen (CA)125 level was not shown to be a statistically significant prognostic factor, but the published data when performed by routine in patients with suspicious tubal malignancies were poor. The accuracy of the initial diagnosis was low due to the multiple non-specific elements of the disease as previously mentioned, more frequent patients being diagnosed with ovarian or pelvic tumor, followed by hydrosalpinx in both the NED and DOD groups. None of the initial misdiagnoses affected prognosis from the statistical perspective.

Table II

Pre-treatment evaluation in the field literature.

Table II

Pre-treatment evaluation in the field literature.

FeaturesNo evidence of disease (NED) group (n=33), n (%)Death of disease (DOD) group (n=51), n (%)Odds ratio (OR)P-value
Age of the patients (years)    
     <400 (0)3 (5.9)4.8350NS
     41-6019 (57.6)17 (33.3)0.36840.0419
     61-8014 (42.4)31 (60.8)2.1040NS
Mean age60.2761.25-NS
Signs and symptoms    
     Atypical vaginal bleeding16 (48.5)21 (41.2)0.7438NS
     Pelvic mass10 (30.3)12 (23.5)0.7077NS
     Abdominal pain13 (39.4)25 (49.0)1.4790NS
     Abdominal distention4 (12.1)18 (35.3)3.95500.0226
     Fever1 (3.0)2 (3.9)1.3060NS
     Ascites2 (6.0)9 (17.6)3.3210NS
Other pre-treatment findings    
     CT/RMN tumor evidence10 (30.3)5 (9.8)0.25000.0216
CA125    
     Normal3 (9.1)1 (2.0)0.2000NS
     Elevated (>35 U/ml)4 (12.1)4 (7.8)0.6170NS
     No evidence25 (75.8)48 (94.1)--
Accuracy of first diagnosis    
     Accurate diagnosis1 (3.0)3 (5.9)2.0000NS
     Ovarian tumor8 (24.2)8 (15.7)0.5814NS
     Pelvic tumor4 (12.1)6 (11.8)0.9667NS
     Hydrosalpinx3 (9.1)1 (2.0)0.2000NS
     Uterine tumor1 (3.0)1 (2.0)0.6400NS

[i] CT/MRI, computed tomography/magnetic resonance imaging; CA, cancer antigen. NS, not significant (P>0.05). Significant P-values (P<0.05) are presented in bold print.

In Table III, the surgical management and pathology reports are shown. Concerning the surgical treatment, a total hysterectomy and bilateral salpingo-oophorectomy were performed for most of the patients. Omentectomy proved to be a statistically significant protective factor, increasing the survival (OR=0.3545, P=0.0269). Similar data were found regarding pelvic lymphadenectomy, performed more frequent in the NED group (42.4%), with an OR=0.3732 and P=0.05. The need for bowel resection in fallopian MMMT patients could highly predispose to a poor prognosis, but the calculated chance rates (OR=7.925) were not statistically significant. Other surgical procedures, such as appendectomy, paraaortic lymphadenectomy, peritonectomy or metastases resection did not present statistical importance in the patient evolution.

Table III

Surgical management of fallopian MMMT.

Table III

Surgical management of fallopian MMMT.

FeatureNo evidence of disease (NED) group (n=33), n (%)Death of disease (DOD) group (n=51), n (%)Odds ratio (OR)P-value
Surgical procedure    
     Hysterectomy32 (96.9)42 (82.4)0.1458NS
     Bilat. salpingo-oophorectomy32 (96.9)47 (92.2)0.3672NS
     Omentectomy20 (60.6)18 (35.3)0.35450.0269
     Appendectomy7 (21.2)8 (15.7)0.6910NS
     Pelvic lymphadenectomy14 (42.4)11 (21.6)0.37320.0500
     Paraaortic lymphadenectomy6 (18.2)7 (13.7)0.7159NS
     Peritonectomy1 (3.0)2 (3.9)1.3060NS
     Bowel resection0 (0)5 (9.8)7.9250NS
     Metastases resection5 (15.2)6 (11.8)0.7467NS
Presence of extragenital metastases    
     Omentum7 (21.2)18 (35.3)2.0260NS
     Appendix2 (6.1)2 (3.9)0.6327NS
     Lymph nodes5 (15.2)18 (35.3)3.05500.0491
     Peritoneum7 (21.2)17 (33.3)2.0000NS
     Bowel2 (6.1)11 (21.6)4.26300.0500
     Distant0 (0)9 (17.6)14.97600.0103
FIGO staging    
     I (A-C)13 (39.4)4 (7.8)0.13090.0007
     II (A-B)6 (18.2)8 (16.7)0.8372NS
     III (A-B)6 (18.2)7 (13.7)0.7159NS
     IIIC8 (24.2)23 (45.1)2.56700.0500
     IV0 (0)9 (17.7)14.97600.0103
Tumor localization    
     Intraluminal16 (48.5)14 (27.4)0.0636NS
     Fimbria2 (6.1)11 (21.6)4.2630NS
     No evidence15 (45.4)26 (51.0)--
Histological type    
     Homologous18 (54.5)15 (29.4)0.34720.0247
     Heterologous15 (45.5)36 (70.6)2.88000.0247
     Chondrosarcoma13 (39.4)26 (51.0)1.6000NS
     Rhabdomyosarcoma4 (12.1)12 (23.5)2.2231NS
     Osteosarcoma2 (6.1)1(2)0.3100NS
     Liposarcoma, angiosarcoma4 (12.1)0 (0)0.06360.0212

[i] MMMT, malignant mixed Müllerian tumors; NS, not significant (P>0.05). Significant P-values (P<0.05) are presented in bold print.

The presence of extragenital metastases proved to be risk factors for death, especially involving the lymph nodes (OR=3.055, P=0.0491), bowel (OR=4.263, P=0.05) or distant organs and tissues (OR=14.976, P=0.0103). Although omentectomy has been proven to be a protective factor, the evidence of omentum metastases was not highly reported in the reviewed articles, thus the OR for this parameter (OR=2.026) was not statistically significant. FIGO staging was another important aspect searched in previous reports. FIGO stage I can be considered a positive prognosis factor, the results fitting into protective factor intervals towards death (OR=0.1309, P=0.0007). Patients with FIGO staged IIIC (OR=2.567, P=0.05) and IV (OR=14.976, P=0.0103) were more susceptible to negative post-treatment outcomes.

The histologic features were also analyzed, depending on the existing evidence in the reviewed articles. Despite the lack of existing data regarding the tumor localization in different segments of the fallopian tube, an intraluminal development of the tumor could be a protective factor in relation to death (OR=0.0636), while fimbrial localization is more probable to be a risk factor (OR=4.263), but none of the parameters presented statistical significance. Analyzing the histological type of the MMMT, homologous type was a protective factor for death (OR=0.3472) while heterologous type could be considered a risk factor (OR=2.880), both parameters being extremely significant (P=0.0247). Due to insufficient evidence concerning the heterologous-specific elements, the obtained results are not of statistical importance.

Oncological approach and patient follow-up data are presented in Table IV. In the NED group, the majority of patients (72.7%) received systemic chemotherapy, the statistical analysis results confirming that chemotherapy administration is a very significant protective factor against death, with an OR=0.2679 and P=0.0070, while the absence of chemotherapy in the treatment of fallopian MMMT is an uncontestable risk factor (OR=3.733). Regarding the chemotherapy agents reported, the only regimen with a statistical positive impact on the survival of patients was carboplatin + paclitaxel (OR=0.2857, P=0.0293). The necessity of using multiple therapeutic lines during the treatment may suggest a negative outcome (OR=2.1330, OR=2.2140), but without statistical significance. Concerning radiotherapy, the evidence gathered from the literature did not suggest any significant involvement in disease progression from a statistical perspective.

Table IV

Oncological approach and follow-up.

Table IV

Oncological approach and follow-up.

Treatment approachNo evidence of disease (NED) group (n=33), n (%)Death of disease (DOD) group (n=51), n (%)Odds ratio (OR)P-value
Chemotherapy    
     Received24 (72.7)20 (39.2)0.26790.0070
     Not received9 (27.3)28 (54.9)3.73300.0070
     No evidence0 (0)3 (5.9)--
First-line chemotherapy agents    
     Carboplatin+paclitaxel11 (45.8)6 (30.0)0.28570.0293
     Cisplatin+doxorubicin+cyclophosphamide7 (29.2)8 (40.0)0.7429NS
     Cyclophosphamide+vincristine+doxorubicin2 (8.3)1 (5.0)0.3298NS
     Vincristine+actynomicin D+cyclophosphamide1 (4.2)2 (10.0)2.1330NS
     Unknown agents3 (12.5)3 (15.0)--
     Multiple therapeutic lines2 (8.3)6 (30.0)2.2140NS
Radiotherapy    
     Received12 (36.4)16 (31.4)0.8750NS
     Not received21 (63.6)32 (62.7)1.1430NS
     No evidence0 (0)3 (5.9)--
Follow-up (months)    
     Average33.4013.19- <0.0001
     Median298  
FIGO stage    
     Stage I (A-C)46.5326-NS
     Stage II (A-B)2911.33-0.0256
     Stage III (A-B)40.1729.42-NS
     Stage IIIC31.7512.13-0.0034
     Stage IV-18.5--

[i] NS, not significant (P>0.05). Significant P-values (P<0.05) are presented in bold print.

Regarding the follow-up period, after eliminating the outlier values, the average was 33.40 months in the NED group and 13.19 months in the DOD group, the differences being statistically significant (P<0.0001). The median survival was 29 months in the NED and 8 months in the DOD group. The follow-up period depending on FIGO stage also presented several differences between the two groups. For stages I (A-C) and III (A-B), there were no statistically significant differences regarding the average follow-up period in the NED and DOD group. For FIGO stage II (A-B), the average follow-up was 29 months in the NED and 11.33 months in the DOD group, differences being statistically significant (P=0.0256). For stage IIIC, the average follow-up was significantly higher in the NED (31.75 months) than in the DOD group (12.13 months) (P=0.0034). It is also notable that were no FIGO stage IV patients in the NED group.

Fig. 4 presents the Kaplan-Meier survival analysis and survival rates at different checkpoints. The survival rate was 0.9879 at 1 month of follow-up, 0.8049 at 6 months, 0.4657 at 2 years, while at 5 years of follow-up it was 0.2865.

MMMT accounts for about 2.4% of all fallopian tube malignancies, and only 4% from this histologic type develop in the fallopian tube as a primary tumor. The rarity of fallopian MMMTs could be correlated with the reduced cyclical activity and lower hormonal responsiveness of the tubal stroma, as compared with endometrial stroma where these tumors occur almost 10 times more frequently (16). These tumors are associated with high invasiveness and poor patient prognosis, especially if the diagnosis is delayed. Due to the extremely low incidence of fallopian carcinosarcoma, clinical protocols for these tumors are not clearly established (22,70).

Discussion

Previously published literature reviews (Table I) (4,5,7,8,10-69) have revealed that the average age of the 85 patients was 59.7 years. Regarding the symptomatology at presentation, our results are in accordance with previous reports by reporting atypical vaginal bleeding and pelvic pain or discomfort, although there is no relevant evidence for which these symptoms may be correlated with prognosis. MMMTs can present, although rarely, as acute abdomen, cases in which are associated with torsion or rupture, leading to hemoperitoneum (64,66). Due to the common symptoms of MMMTs, rarity and localization, an initial definitive diagnosis is very difficult to achieve and prove, in the majority of cases remaining uncertain until the histological examination is performed; the most frequent preoperative and intraoperative diagnosis is related to an ovarian tumor, underlining its inaccuracy (67). Concerning imaging examination, MRI is more sensitive compared to CT to distinguish various tumor characteristics that may facilitate the preoperative diagnosis and further treatment, although imaging reports of carcinosarcoma of the fallopian tube are limited, as well as the role of CA125(71).

Despite the lack of therapeutic protocols for fallopian MMMTs and the small number of reported cases, the strategy involves a primary surgical procedure aimed to resect all visible tumors, followed by oncological treatment intensely debated in the past decades (72). For proper staging, ascites or peritoneal washings must be collected for cytological examinations, followed by a thorough exploration of all peritoneal surfaces; a total hysterectomy and bilateral salpingo-oophorectomy must be performed, together with omentectomy, lymphadenectomy and peritoneal biopsies, depending on the intraoperative findings, achieving a maximal cytoreduction when possible (48,73). As already demonstrated, omentectomy could be an important positive prognostic factor, together with pelvic lymphadenectomy, but the extent of surgery might be variable and sometimes demanding because of pelvic modified anatomy, requiring a retroperitoneal dissection (74). Regarding the possible metastatic sites, the most frequent are the contralateral tube, ovaries, uterus, but also the peritoneal surface, emphasizing that pelvic and paraaortic lymphatic nodes are not often involved, while distant metastasis is extremely rare (63), but our meta-analysis has confirmed that omentum, lymph node and distant metastases in fallopian MMMTs are often described. Sometimes, when the fallopian tumor invades other pelvic organs, different types of exenterative procedure must be performed, but these situations are rare (75).

A proper staging concerning fallopian carcinosarcomas is essential to adopt a therapeutic strategy, the survival rates being directly dependent on this parameter. As the results of the meta-analysis demonstrated, FIGO stage I presented the best survival outcomes, while FIGO stages IIIC and IV were prone to death due to disease. The prognosis of a primary fallopian tube malignancy is usually poor and depends rather on staging than on histological criteria, such as tumor type or grade (76).

Previous histological macroscopic descriptions of the tumor were similar with the present case report, revealing a dilated lumen of the tube containing polypoid or infiltrative grey or white colored mass, more frequent with necrosis and hemorrhage areas (69). Microscopically two mentioned components of the MMMT were often reported-a serous carcinoma with high-grade malignancy associated with a neoplastic proliferation of the conjunctive tissue, the presence of chondrosarcoma detected in about 50% of cases (38,60). The current meta-analysis has shown that a fimbrial localization of the tumor could predispose to a more aggressive tumor evolution, an issue explained by the fact that intraluminal fluid can be discharged through the uterus in the case of fimbrial atresia. But when the end of the fimbria remains open or the tumor develops at this level, it is more likely for tumor cells to be implanted into the abdominal cavity, situations in which the prognosis is poor (77). The histological type is also known to be a prognostic factor in many gynecological malignancies. Current meta-analysis results reporting that the heterologous type of fallopian carcinosarcoma could negatively affect survival and, by contrary, homologous MMMTs are thought to be associated with a better prognosis (78).

Systemic chemotherapy significantly improves survival, especially associated with an optimal cytoreductive surgery, as mentioned before. Over the past several decades, multiple regimens have been tried, demonstrating that adjuvant chemotherapy containing platinum agents is the most effective treatment for fallopian carcinosarcomas (79). GOG Study analyzed the association between ifosfamide and cisplatin, confirming no survival advantage, with the cost of increased toxicity (80). Currently, the combination of paclitaxel and carboplatin has been intensely studied and gained popularity in a great variety of gynecological malignant diseases, due to its important activity, acceptable toxicity and ease of administration; the results of current meta-analysis have also revealed that patients who received this drug combination exhibit better survival outcomes (59). Radiotherapy has no influence on prognosis and no benefit on survival (25,54,57,65,81).

To date, the few reported fallopian MMMTs emphasize its extremely low incidence and its high malignancy, fulminant progression, and high incidence of local and distant metastases, all associated with poor survival outcomes. As an early definite diagnosis is extremely difficult to achieve even with high performance imaging examinations, most of the cases are finally diagnosed after histological evaluation. Fallopian MMMTs should be considered as a differential diagnosis in all postmenopausal patients who present with a pelvic mass, vaginal bleeding, abdominal pain or distension and with no other significant findings. Due to the non-specific presentation, symptomatology and low incidence of this neoplasia, the success of conducting large randomized trials in order to improve diagnosis accuracy, treatment options and establish international therapeutic protocols is limited. Reporting this rare pathology could be essential for obtaining more precise information regarding the diagnostic methods, targeted treatment and prognosis, in order to improve the survival and quality of life in patients with MMMTs.

Acknowledgements

Not applicable.

Funding

Funding: No funding was received to complete the present literature research.

Availability of data and materials

Data was gathered from previously published reports and collected into a database. The dataset used and analyzed during the current study is available from the corresponding author on reasonable request, all the results being included in this article.

Authors' contributions

ALC conceived, directed the project and prepared the manuscript. MEC was the leading surgeon for the surgical procedure described in our case report. AAM and NB supervised the work and revised the article. SM prepared and histologically analyzed the specimens. ALC, MG, SLK, AF and MS are part of the surgical team since 2016 and collected data from previously published articles. MG, SLK and MS were involved in designing and drafting the manuscript. All authors read and approved the final manuscript.

Ethics approval and consent to participate

Not applicable. Yet, informed consent was obtained for publication of the patient's data.

Patient consent for publication

The patient provided written informed consent for the scientific publication of any associated data and accompanying images.

Competing interests

Authors declare no competing interests relevant to this article.

References

1 

Zhang Q, Liu A, Wu JJ, Niu M, Zhao Y, Tian SF, Chen A and Zhong L: Primary malignant mixed Müllerian tumors of the fallopian tube with cervix metastasis: A rare case report and literature review. Medicine (Baltimore). 97(e11311)2018.PubMed/NCBI View Article : Google Scholar

2 

Lorusso D, Martinelli F, Mancini M, Sarno I, Ditto A and Raspagliesi F: Carboplatin-paclitaxel versus cisplatin-ifosfamide in the treatment of uterine carcinosarcoma: A retrospective cohort study. Int J Gynecol Cancer. 24:1256–1261. 2014.PubMed/NCBI View Article : Google Scholar

3 

Schink JC and Lurain JR: Rare gynecologic malignancies. Curr Opin Obstet Gynecol. 3:78–90. 1991.PubMed/NCBI

4 

Ji J, Zuo P, Li L and Wang Y: Primary malignant mixed Müllerian tumor of the fallopian tube after subtotal hysterectomy: A case report and literature review. Arch Gynecol Obstet. 291:1187–1190. 2015.PubMed/NCBI View Article : Google Scholar

5 

Imachi M, Tsukamoto N, Shigematsu T, Watanabe T, Uehira K, Amada S, Umezu T and Nakano H: Malignant mixed Müllerian tumor of the fallopian tube: Report of two cases and review of literature. Gynecol Oncol. 47:114–124. 1992.PubMed/NCBI View Article : Google Scholar

6 

Xue Q, Wu QY and Wang J: Ultrasonographic diagnosis of carcinosarcoma of the fallopian tube: A report of 1 case. Chin J Med Imaging. 21(942)2013.

7 

Watanabe T, Sugino T, Furukawa S, Soeda S, Nishiyama H and Fujimori K: Malignant mixed Müllerian tumor of the fallopian tube: A case report. Eur J Gynaecol Oncol. 33:223–226. 2012.PubMed/NCBI

8 

Shen YM, Xie YP, Xu L, Yang KX, Yu N, Yu Y and Wang JH: Malignant mixed Müllerian tumor of the fallopian tube: Report of two cases and review of literature. Arch Gynecol Obstet. 281:1023–1028. 2010.PubMed/NCBI View Article : Google Scholar

9 

Hellström AC, Tegerstedt G, Silfverswärd C and Pettersson F: Malignant mixed Müllerian tumors of the ovary: Histopathologic and clinical review of 36 cases. Int J Gynecol Cancer. 9:312–316. 1999.PubMed/NCBI View Article : Google Scholar

10 

Motta G: Contributto alla conoscenza dei tumori misti rari dell' apperato genitale fimminile (carcinosarcoma della salpinge). Ann Obstet Ginecol. 48:611–625. 1926.

11 

Zacho A: Sur le carcinoma primaire dans la trompe de fallope: Avec exposé D'un cas. Acta Obstet Gynecol Scand. 13:283–291. 1933.

12 

Platz J: Über sechs weitere Fälle von primärem Tubencarcinom. Arch Gynaekol. 170:604–615. 1940.

13 

Bochner K: Primary uterine tube malignancy. Obstet Gynecol. 18:767–769. 1961.PubMed/NCBI

14 

Williams TJ and Woodruff JD: Malignant mixed mesenchymal tumor of the uterine tube: Report of a case. Obstet Gynecol. 21:618–621. 1963.PubMed/NCBI

15 

Malnasy J and Gaal M: Primary carcinosarcoma of the fallopian tube. Gynaecologia. 156:203–208. 1963.PubMed/NCBI View Article : Google Scholar

16 

McQueeney AJ, Carswell BL and Sheehan WJ: Malignant mixed Müllerian tumor primary in uterine tube: Review of the literature and report of an additional case. Obstet Gynecol. 23:338–343. 1964.PubMed/NCBI

17 

De Queiroz AC and Roth LM: Malignant mixed Müllerian tumor of the fallopian tube. Report of a case. Obstet Gynecol. 36:554–557. 1970.PubMed/NCBI

18 

Wu JP, Tanner WS and Fardal PM: Malignant mixed Müllerian tumor of the uterine tube. Obstet Gynecol. 41:707–712. 1973.PubMed/NCBI

19 

Acosta AA, Kaplan AL and Kaufmann RH: Mixed Müllerian tumors of the oviduct. Obstet Gynaecol. 44:84–90. 1974.PubMed/NCBI

20 

Aggarwal S, Devi PK and Aikat M: Malignant mixed Müllerian tumour of the fallopian tube. J Obstet Gynaecol India. 85:224–236. 1976.

21 

Manes JL and Taylor HB: Carcinosarcoma and mixed Müllerian tumors of the fallopian tube: Report of four cases. Cancer. 38:1687–1693. 1976.PubMed/NCBI View Article : Google Scholar

22 

Henderson SR, Harper RC, Salazar OM and Rudolph JH: Primary carcinoma of the fallopian tube: Difficulties of diagnosis and treatment. Gynecol Oncol. 5:168–179. 1977.PubMed/NCBI View Article : Google Scholar

23 

Jain U: Mixed mesodermal tumor of the fallopian tube: Report of a case and review of literature. Md State Med J. 26:43–46. 1977.PubMed/NCBI

24 

Oka M, Bassett EP and Gross S: Malignant mixed Müllerian tumors. N Y State J Med. 78:1431–1434. 1978.PubMed/NCBI

25 

Hanjani P, Petersen RO and Bonnell SA: Malignant mixed Müllerian tumor of the fallopian tube. Report of a case and review of literature. Gynecol Oncol. 9:381–393. 1980.PubMed/NCBI View Article : Google Scholar

26 

Viniker DA, Mantell BS and Greenstein RJ: Carcinosarcoma of the fallopian tube: A case report and review of the literature. Br J Obstet Gynaecol. 87:530–534. 1980.PubMed/NCBI View Article : Google Scholar

27 

Holst N and Erichsen A: Mixed mesodermal tumour of the fallopian tube. A case report. Ann Chir Gynaecol. 70:207–209. 1981.PubMed/NCBI

28 

O'Toole RV, Tuttle SE and Shah NT: Heterologous carcinosarcoma of the fallopian tube. A case report. J Reprod Med. 27:749–752. 1982.PubMed/NCBI

29 

Egorov VP: Heterotopic mesodermal tumor of the fallopian tube. Arkh Patol. 44:54–56. 1982.PubMed/NCBI(In Russian).

30 

Kahanpää KV, Laine R and Saksela E: Malignant mixed Müllerian tumor of the fallopian tube: Report of a case with 5-year survival. Gynecol Oncol. 16:144–149. 1983.PubMed/NCBI View Article : Google Scholar

31 

Deppe G, Zbella E, Friberg J and Thomas W: Combination chemotherapy for mixed Müllerian tumor of the fallopian tube. Cancer. 54:1517–1520. 1984.PubMed/NCBI View Article : Google Scholar

32 

Punnonen R, Lauslahti K and Pystynen P: Primary malignancies of the fallopian tube. Ann Chir Gynaecol Suppl. 197:15–18. 1985.PubMed/NCBI

33 

Buchino JJ and Buchino JJ: Malignant mixed Müllerian tumor of the fallopian tube. Arch Pathol Lab Med. 111:386–387. 1987.PubMed/NCBI

34 

Yabushita H, Ogawa A, Hoshina S, Okamoto T, Nakanishi M and Ishihara M: Malignant mixed mesodermal tumour of the fallopian tube. Case report. Br J Obstet Gynaecol. 94:179–183. 1987.PubMed/NCBI View Article : Google Scholar

35 

Chen KT and Wolk RW: Extragenital malignant mixed Müllerian tumor. Gynecol Oncol. 30:422–426. 1988.PubMed/NCBI View Article : Google Scholar

36 

Muntz HG, Rutgers JL, Tarraza HM and Fuller AF Jr: Carcinosarcomas and mixed Müllerian tumors of the fallopian tube. Gynecol Oncol. 34:109–115. 1989.PubMed/NCBI View Article : Google Scholar

37 

Axelrod JH, Herbold DR and Freel JH: Carcinosarcoma of the fallopian tube. Gynecol Oncol. 32:398–400. 1989.PubMed/NCBI View Article : Google Scholar

38 

Kinoshita M, Asano S, Yamashita M and Matsuda T: Mesodermal mixed tumor primary in the fallopian tube. Gynecol Oncol. 32:331–335. 1989.PubMed/NCBI View Article : Google Scholar

39 

van Dijk CM, Kooijman CD and van Lindert AC: Malignant mixed Müllerian tumour of the fallopian tube. Histopathology. 16:300–302. 1990.PubMed/NCBI

40 

Seraj IM, King A and Chase D: Malignant mixed Müllerian tumor of the oviduct. Gynecol Oncol. 37:296–301. 1990.PubMed/NCBI View Article : Google Scholar

41 

Liang WW, Lin YN and Lee YN: Malignant mixed Müllerian tumor of fallopian tube. Report of a case and review of literature. Zhonghua Yi Xue Za Zhi (Taipei). 45:272–275. 1990.PubMed/NCBI

42 

Chang HC, Hsueh S and Soong YK: Malignant mixed Müllerian tumor of the fallopian tube. Case report and review of the literature. Changgeng Yi Xue Za Zhi. 14:259–263. 1991.PubMed/NCBI

43 

Chiou YK, Su IJ, Chen CA and Hsieh CY: Malignant mixed Müllerian tumor of the fallopian tube. J Formos Med Assoc. 90:793–795. 1991.

44 

Moore DT, Taslimi MM and Kosanovich M: Malignant mixed Müllerian tumor of the fallopian tube of the heterologous type. J Tenn Med Assoc. 85:513–514. 1992.PubMed/NCBI

45 

Carlson JA Jr, Ackerman BL and Wheeler JE: Malignant mixed Müllerian tumor of the fallopian tube. Cancer. 71:187–192. 1993.PubMed/NCBI View Article : Google Scholar

46 

Weber AM, Hewett WF, Gajewski WH and Curry SL: Malignant mixed Müllerian tumors of the fallopian tube. Gynecol Oncol. 50:239–243. 1993.PubMed/NCBI View Article : Google Scholar

47 

Zorlu CG, Cobanoglu O, Kușcu E and Aribas D: Malignant mixed Müllerian tumor of the fallopian tube. Acta Obstet Gynecol Scand. 73:352–354. 1994.PubMed/NCBI View Article : Google Scholar

48 

Horn LC, Werschnik C, Bilek K and Emmert C: Diagnosis and clinical management in malignant Müllerian tumors of the fallopian tube. A report of four cases and review of recent literature. Arch Gynecol Obstet. 258:47–53. 1996.PubMed/NCBI View Article : Google Scholar

49 

Ebert AD, Perez-Canto A, Schaller G, Entezami M, Hopp HS and Weitzel HK: Stage I primary malignant mixed Müllerian tumor of the fallopian tube. Report of a case with five-year survival after minimal surgery without adjuvant treatment. J Reprod Med. 43:598–600. 1998.PubMed/NCBI

50 

Maitra RN, Lee J, McConnell DT, Kenwright DN and Dady P: Malignant mixed Müllerian tumour of the fallopian tube occurring in a patient with Peutz-Jegher's syndrome. Aust N Z J Obstet Gynaecol. 44:77–79. 2004.PubMed/NCBI View Article : Google Scholar

51 

Moustafa M, Beynon DW and Elmahallawy M: Primary malignant mixed Müllerian tumour of the fallopian tube. J Obstet Gynaecol. 24:940–941. 2004.PubMed/NCBI View Article : Google Scholar

52 

Humble S and Carter E: Pathologic quiz case: A right adnexal mass in a postmenopausal patient. Malignant mixed Müllerian tumor with heterologous elements arising in the fallopian tube. Arch Pathol Lab Med. 128:e161–162. 2004.PubMed/NCBI View Article : Google Scholar

53 

Lim BJ, Kim JW, Yang WI and Cho NH: Malignant mixed Müllerian tumor of fallopian tube with multiple distinct heterologous components. Int J Gynecol Cancer. 14:690–693. 2004.PubMed/NCBI View Article : Google Scholar

54 

Gagner JP and Mittal K: Malignant mixed Müllerian tumor of the fimbriated end of the fallopian tube: Origin as an intraepithelial carcinoma. Gynecol Oncol. 97:219–222. 2005.PubMed/NCBI View Article : Google Scholar

55 

Kuroda N, Moriki T, Oguri H, Maeda N, Toi M, Miyazaki E, Hiroi M, Fukaya T and Enzan H: Malignant Müllerian mixed tumor (carcinosarcoma) of the fallopian tube: An immunohistochemical study of neoplastic cells. APMIS. 113:643–646. 2005.PubMed/NCBI View Article : Google Scholar

56 

Das TK, Raha K, Bandyopadhyay A, Dasgupta A, Ghosh D and Mondal AK: Malignant mixed Müllerian tumour of the fallopian tube of heterologous variety-a case report. Indian J Pathol Microbiol. 48:354–356. 2005.PubMed/NCBI

57 

Hudelist G, Unterrieder K, Kandolf O, Alpi G, Pucher S, Pollak G, Czerwenka K and Keckstein J: Malignant mixed Müllerian tumor with heterologous component arising in the fallopian tube-a case report. Eur J Gynaecol Oncol. 27:509–512. 2006.PubMed/NCBI

58 

Kuroda N, Inui Y, Ohara M, Hirouchi T, Mizuno K, Kubo A, Hayashi Y, Enzan H and Lee GH: Hyaline globule-like structures in undifferentiated sarcoma cells of malignant Müllerian mixed tumor of the fallopian tube. Med Mol Morphol. 40:46–49. 2007.PubMed/NCBI View Article : Google Scholar

59 

Kawaguchi W, Itamochi H, Kigawa J, Kanamori Y, Oishi T, Shimada M, Sato S, Sato S and Terakawa N: Chemotherapy consisting of paclitaxel and carboplatin benefits a patient with malignant mixed Müllerian tumor of the fallopian tube. Int J Clin Oncol. 13:461–463. 2008.PubMed/NCBI View Article : Google Scholar

60 

Kourea HP, Adonakis G, Androutsopoulos G, Zyli P, Kourounis G and Decavalas G: Fallopian tube malignant mixed Müllerian tumor (carcinosarcoma): A case report with immunohistochemical profiling. Eur J Gynaecol Oncol. 29:538–542. 2008.PubMed/NCBI

61 

Piura B, Rabinovich A, Apel-Sarid L and Shaco-Levy R: Carcinosarcoma of the fallopian tube with metastasis of its epithelial component to the ovary, appendix and omentum. J Obstet Gynaecol. 29:566–567. 2009.PubMed/NCBI View Article : Google Scholar

62 

Malhotra V, Nanda S, Chauhan MB, Marwah N and Sen R: Heterologous malignant mixed Müllerian tumor of the uterus and fallopian tube: A case report. J Gynacol Surg. 28:296–298. 2012.PubMed/NCBI

63 

Tsai CP, Ho ES, Ke YM, Hsu ST, Wang RC and Lu CH: Stage III malignant mixed Müllerian tumor of the fallopian tube: A case of 5-year survival after optimal debulking and adjuvant chemotherapy with paclitaxel plus carboplatin. Taiwan J Obstet Gynecol. 51:294–296. 2012.PubMed/NCBI View Article : Google Scholar

64 

Gupta R and Jenison E: A rare case of carcinosarcoma of the fallopian tube presenting with torsion, rupture and hemoperitoneum. Gynecol Oncol Case Rep. 2:4–5. 2011.PubMed/NCBI View Article : Google Scholar

65 

Takemoto Y, Ota T, Aoki Y, Ogura K, Ogishima D and Matsumoto T: Carcinosarcoma of the fallopian tube with disappearance of carcinoma cells by neoadjuvant chemotherapy: Case study. Eur J Gynaecol Oncol. 36:618–622. 2015.PubMed/NCBI

66 

Narin MA, Basaran D, Karalok A, Turan T and Tulunay G: Primary fallopian tube carcinosarcoma: Report of two cases. Yeditepe Med J. 11:945–948. 2015.

67 

Vale-Fernandez E, Rodrigues F, Serrano P and Silva AI: Primary malignant mixed Müllerian tumour of the fallopian tube: A rare and difficult but possible diagnosis. BMJ Case Rep. 2015(bcr2014209268)2015.PubMed/NCBI View Article : Google Scholar

68 

Monsalve N, Santos M, Petrosino P, Arenas A and Sánchez Z: Tumor Mülleriano mixto heterólogo primario de trompa uterine. Rev Obstet Ginecol Venez. 75:212–216. 2015.

69 

Bécsi J, Szabó B, Szabó T, Onuș M, Mocan S and Căpîlna M: Malignant mixed Müllerian tumor of fallopian tube: Report of a case and review of the literature. Eur J Gynaecol Oncol. 11:143–147. 2019.

70 

Mackay HJ, Buckanovich RJ, Hirte H, Correa R, Hoskins P, Biagi J, Martin LP, Fleming GF, Morgan R, Wang L, et al: A phase II study single agent of aflibercept (VEGF Trap) in patients with recurrent or metastatic gynecologic carcinosarcomas and uterine leiomyosarco. A trial of the Princess Margret Hospital, Chicago and California cancer phase II consortia. Gynecol Oncol. 125:136–140. 2012.PubMed/NCBI View Article : Google Scholar

71 

Makhija S, Howden N, Edwards R, Kelley J, Townsend DW and Meltzer CC: Positron emission tomography/computed tomography imaging for the detection of recurrent ovarian and fallopian tube carcinoma: A retrospective review. Gynecol Oncol. 85:53–58. 2002.PubMed/NCBI View Article : Google Scholar

72 

Matulonis UA, Krag KJ, Krasner CN, Atkinson T, Horowitz NS, Lee H and Penson RT: Phase II prospective study of paclitaxel and carboplatin in older patients with newly diagnosed Müllerian tumors. Gynecol Oncol. 112:394–399. 2009.PubMed/NCBI View Article : Google Scholar

73 

Chiva L, Zanagnolo V, Querleu D, Martin-Calvo N, Arevalo-Serrano J, Căpîlna ME, Fagotti A, Kucukmetin A, Mom C, Chakalova G, et al: SUCCOR study: An international European cohort observational study comparing minimally invasive surgery versus open abdominal radical hysterectomy in patients with stage IB1 cervical cancer. Int J Gynecol Cancer. 30:1269–1277. 2020.PubMed/NCBI View Article : Google Scholar

74 

Căpîlna ME, Szabo B, Rusu SC, Becsi J, Moldovan B, Neagoe RM and Muhlfay G: Anatomical variations of the obturator veins and their surgical implications. Eur J Gynaecol Oncol. 38:263–265. 2017.PubMed/NCBI

75 

Căpîlna ME, Moldovan B and Szabo B: Pelvic exenteration-our initial experience in 15 cases. Eur J Gynaecol Oncol. 36:142–145. 2015.PubMed/NCBI

76 

Skafida E, Grammatoglou X, Katsamagkou E, Glava C, Firfiris N and Vasilakaki T: Primary malignant mixed Müllerian tumour of the fallopian tube. Report of a case. Eur J Gynaecol Oncol. 31:126–128. 2010.PubMed/NCBI

77 

Ma Y and Duan W: Clinical and survival analysis of 36 cases of primary fallopian tube carcinoma. World J Surg Onc. 12(311)2014.PubMed/NCBI View Article : Google Scholar

78 

Mok JE, Kim YM, Jung MH, Kim KR, Kim DY, Kim JH, Kim YT and Nam JH: Malignant mixed Müllerian tumors of the ovary: Experience with cytoreductive surgery and platinum-based combination chemotherapy. Int J Gynecol Cancer. 16:101–105. 2006.PubMed/NCBI View Article : Google Scholar

79 

Yokoyama Y, Yokota M, Futagami M and Mizunuma H: Carcinosarcoma of the fallopian tube: Report of four cases and review of literature. Asia Pac J Clin Oncol. 8:303–311. 2012.PubMed/NCBI View Article : Google Scholar

80 

Sutton G, Brunetto VL, Kilgore L, Soper JT, McGehee R, Olt G, Lentz SS, Sorosky J and Hsiu JG: A phase III trial of ifosfamide with or without cisplatin in carcinosarcoma of the uterus: A gynecologic oncology group study. Gynecol Oncol. 79:147–153. 2000.PubMed/NCBI View Article : Google Scholar

81 

Căpîlna ME, Rusu SC, Laczko C, Szabo B and Marian C: Three synchronous primary pelvic cancers-a case report. Eur J Gynaecol Oncol. 36:216–218. 2015.PubMed/NCBI

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Cozlea AL, Gheorghe M, Kiss SL, Fandi A, Stanca M, Mocan S, Căpîlna ME, Bacalbașa N and Moldovan AA: Malignant mixed Müllerian tumor of the fallopian tube: Case report and literature review. Exp Ther Med 23: 177, 2022
APA
Cozlea, A.L., Gheorghe, M., Kiss, S.L., Fandi, A., Stanca, M., Mocan, S. ... Moldovan, A.A. (2022). Malignant mixed Müllerian tumor of the fallopian tube: Case report and literature review. Experimental and Therapeutic Medicine, 23, 177. https://doi.org/10.3892/etm.2021.11100
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Cozlea, A. L., Gheorghe, M., Kiss, S. L., Fandi, A., Stanca, M., Mocan, S., Căpîlna, M. E., Bacalbașa, N., Moldovan, A. A."Malignant mixed Müllerian tumor of the fallopian tube: Case report and literature review". Experimental and Therapeutic Medicine 23.2 (2022): 177.
Chicago
Cozlea, A. L., Gheorghe, M., Kiss, S. L., Fandi, A., Stanca, M., Mocan, S., Căpîlna, M. E., Bacalbașa, N., Moldovan, A. A."Malignant mixed Müllerian tumor of the fallopian tube: Case report and literature review". Experimental and Therapeutic Medicine 23, no. 2 (2022): 177. https://doi.org/10.3892/etm.2021.11100