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ORIGINAL ARTICLE  
Year : 2013  |  Volume : 56  |  Issue : 4  |  Page : 365-371
Clinico-pathological spectrum of primary ovarian malignant mixed mullerian tumors (OMMMT) from a tertiary cancer institute: A series of 27 cases


1 Department of Pathology, Tata Memorial Hospital, Mumbai, Maharashtra, India
2 Department of Medical Oncology, Tata Memorial Hospital, Mumbai, Maharashtra, India
3 Department of Gynecologic Surgery, Tata Memorial Hospital, Mumbai, Maharashtra, India
4 Department of Radiation Oncology, Tata Memorial Hospital, Mumbai, Maharashtra, India
5 Department of Biostatistics, Tata Memorial Hospital, Mumbai, Maharashtra, India

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Date of Web Publication18-Jan-2014
 

   Abstract 

Aims and Objectives: To study the clinico-pathological characteristics of primary ovarian malignant mixed mullerian tumor (OMMMT) and assess the prognostic factors associated with treatment outcome and survival. Materials and methods: The pathology database was searched for primary ovarian carcinosarcoma diagnosed and/or managed at our institute from period of January 2004 to July 2010. The histological sections were reviewed, with emphasis on type and grade of epithelial and sarcomatous components. The medical records were retrospectively analyzed for clinical details and follow up. Results: A total of 27 cases of primary ovarian carcinosarcoma were identified. The median age at diagnosis was 51 years. Fourteen patients had advanced stage (stage III and IV) at presentation. Cytoreductive surgery was done in 18 cases, and 7 had received upfront chemotherapy. Histologically, 10 cases had epithelial predominance (> 50% epithelial component) and 11 had sarcoma predominance. The most frequent epithelial component was endometroid type, and most common sarcoma component was rhabdomyosarcomatous. Hyaline droplets within sarcomatous stroma were seen prominently in 15 cases. Three cases showed germ cell /yolk sac-like areas. Eighteen cases had follow up with a median of 15 months (4-40 months). The recurrence-free survival in advanced stage and sarcoma predominant was 10.5 months in comparison to 13 months in early stage and epithelial predominant OMMMT. Conclusion: Primary ovarian carcinosarcoma is a rare biphasic malignancy with variable proportions of epithelial and spindle elements. Presence of hyaline droplets within spindle sarcoma in a biopsy from ovarian mass should alert the pathologists regarding MMMT. Advanced stage, suboptimal cytoreduction, and sarcoma predominant tumors are likely to have a worse outcome in ovarian MMMT.

Keywords: Mixed, mullerian, ovary, primary

How to cite this article:
Menon S, Deodhar K, Rekhi B, Dhake R, Gupta S, Ghosh J, Maheshwari A, Mahantshetty U, Shrivastva S, Budukh A, Tongaonkar HB, Kerkar R. Clinico-pathological spectrum of primary ovarian malignant mixed mullerian tumors (OMMMT) from a tertiary cancer institute: A series of 27 cases. Indian J Pathol Microbiol 2013;56:365-71

How to cite this URL:
Menon S, Deodhar K, Rekhi B, Dhake R, Gupta S, Ghosh J, Maheshwari A, Mahantshetty U, Shrivastva S, Budukh A, Tongaonkar HB, Kerkar R. Clinico-pathological spectrum of primary ovarian malignant mixed mullerian tumors (OMMMT) from a tertiary cancer institute: A series of 27 cases. Indian J Pathol Microbiol [serial online] 2013 [cited 2021 Jul 24];56:365-71. Available from: https://www.ijpmonline.org/text.asp?2013/56/4/365/125293



   Introduction Top


Ovarian carcinosarcomas, also known as malignant mixed mesodermal tumors or malignant mixed mullerian tumors (OMMMT), are exceedingly rare and comprise 1-3% of ovarian malignancies. [1] These tumors are defined histologically by the admixture of malignant epithelial and stromal elements. They are sub-classified as "heterologous" or "homologous" based on the presence or absence of a stromal component containing mesenchymal tissue not normally found at the primary tumor site. Recent studies propose a monoclonal theory of histogenesis of ovarian carcinosarcomas, and these may be best regarded as metaplastic epithelial carcinomas. [2],[3],[4] These tumors follow an aggressive clinical course, and survival is significantly reduced when compared to that in epithelial ovarian cancers. Treatment for advanced disease consists of complete surgical staging and debulking and postoperative adjuvant chemotherapy. Clinico-pathologic case series on this malignancy indicate that advanced stage and suboptimal cytoreductive surgery to be the most significant poor prognostic factors. Presence of heterologous elements that was previously believed to carry prognostic importance does not appear to be significant. [5],[6],[7] Studies on the morphological prognostic variables are scarce in literature. [8] Recently, presence of stromal predominance and serous epithelial component in advanced cases have been suggested to have a worse outcome. [9]

In the current study, we retrospectively analyzed the data concerning the clinical and pathological characteristics, management and follow up of patients of ovarian carcinosarcoma diagnosed and/or treated at our institute.


   Materials and Methods Top


The pathology database was searched for primary ovarian carcinosarcoma diagnosed and/or managed at our institute from period of July 2004 to June 2010

The histological sections were reviewed, with emphasis on type and grade of epithelial and stromal components and their relative percentages of distribution in the tumor sections.

The medical records were retrospectively reviewed with emphasis on surgical optimal or sub-optimal debulking, chemotherapy regimens, and survival. Optimal debulking was defined as residual tumor of less than 1 cm in its largest dimension. The follow up data in available cases was obtained from the medical and electronic records of the patient. Survival was calculated from the date of diagnosis until the date of death or date of last follow up for the patients who were still alive with or without evidence of disease. SPSS 14 was used to compute the statistical data. Survival curves were generated by the Kaplan-Meier method.


   Results Top


Patient demographics

A total of 27 cases of primary ovarian carcinosarcoma were identified. The age at time of diagnosis varied from 33 to 70 years with a median age of 51 years. Majority of patients presented with increasing abdominal girth and /or pain with abdominal discomfort. Radiologically, a complex solid- cystic mass was demonstrable in most patients.

CA 125 level was obtained only in 12 patients preoperatively, and 9 (75%) had an elevated baseline CA 125 level. The mean preoperative serum CA 125 level was 5125.2 U/ml (range, 29.6-34851 U/ml).

International Federation of Gynecology and Obstetrics stage distribution was as follows: Stage IC, 2 patients (8%); Stage II, 2 patients (8%), Stage III, 17 (69%); and Stage IV, 3 patients (13%). No staging details were available in 3 cases.

Seven cases were for pathology consultation only with limited clinical and treatment details, and follow up details were not available in them. Two cases had no follow up after surgery.

Pathological features

The most common epithelial component was endometrioid adenocarcinoma (10 cases) followed by serous adenocarcinoma (7 cases). Admixture of 2 or more epithelial components was seen in 10 cases. [Figure 1]a-d
Figure 1: Various types of malignant epithelial components seen in OMMMT. (a) Serous epithelial component (H and E, x 40) with inset showing peculiar basement membrane material around epithelial foci, (b) Endometroid epithelial component with squamous areas (H and E, x 40), (c) Clear cell carcinoma areas, (H and E, x 40) and (d) Transiti onal epithelial component (d), (H and E, x 40)

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Heterologous sarcomatous elements were seen more commonly (59%) compared to homologous elements (41%) (16 cases vs. 11 cases). The most common heterologous element was rhabdomyosarcomatous, seen in 8 cases. Majority of the cases had admixture of more than one sarcomatous component with rhabdomyosarcoma and endometrial stromal sarcoma being the commonest combination. Interestingly, the stromal sarcoma component had undifferentiated appearance in most of the cases. [Figure 2]a-d.
Figure 2: Various types of sarcomatous components seen in OMMMT. (a) Chondrosarcomatous component in opposition to malignant epithelial component (H and E, x 40), (b) Osteosarcomatous areas (H and E, x 40), (c) Undiff erenti ated sarcomatous component, (H and E, x 40) and (d) Liposarcomatous component, (H and E, x 40)

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Epithelial predominant tumors (> 50% to < 95% epithelial component) were seen in 10 cases. Out of these 10 cases, 8 presented in advanced stage (III or IV). Sarcoma- predominant tumors (> 50% to < 95% sarcomatous component) were seen in 11 cases with 8 of these being advanced at presentation. Equal epithelial and sarcomatous components were seen in 6 cases. However, the stage at presentation did not correlate with either epithelial or sarcoma predominance.

Hyaline droplets/globules were seen in 15 cases, frequently in areas of undifferentiated sarcoma or foci of rhabdomyosarcoma. The droplets were seen both intra- and extracellularly. In some cases, these droplets were abundant and seen in small group and clusters. [Figure 3]a and 3b].
Figure 3: Hyaline globules in sarcomatous stroma of OMMMT (a) (H and E, x 40), (b) (H and E, x 100) resembling 'Archipelago in sea of spindle cells.'Immature neuroepithelium and areas of embryonal carcinoma in teratoid carcinosarcoma (c and d, respecti vely) (H and E, x 40)

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Three cases were labeled as teratoid carcinosarcoma that had foci morphologically resembling germ cell tumors, including embryonal, yolk sac and immature teratomatous areas in the form of neuroepithelium with rosette-like pattern. These patients had all presented as stage III disease [Figure 4]c and 4]d]. A peculiar basement membrane thickening around epithelial islands was seen in 1 case.
Figure 4: Immuno-histochemical staining in OMMMT. (a) Vimenti n positi vity in endometrioid epithelial component and sarcomatous stroma (Indirect immunoperoxidase, x 40), (b) Rhabdomyosarcomatous
component- desmin-positive (Indirect immunoperoxidase, x 40), (c) Cytokerati n positi vity in serous epithelial component, (Indirect immunoperoxidase x 40) and (d) Smooth muscle actin-positive leiomyosarcomatous component, (Indirect immunoperoxidase, x 40)


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The morphological features are summarized in [Table 1]
Table 1: Histopathological characteristi cs of OMMMT

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Treatment and follow up

As majority of cases were advanced at presentation, they received multimodal management protocols. Eighteen patients had upfront cytoreductive surgery, which varied from total abdominal hysterectomy with bilateral salpingo-oophorectomy (TAH+BSO) with omentectomy with or without bilateral pelvic nodal dissection BPLND (14 cases) to salpingo-ovariectomies (3 cases) and total abdominal hysterectomy with unilateral salpingo-oophorectomy (TAH+USO) in 1 case. Seven patients received neoadjuvant chemotherapy (NACT) due to poor surgical risk and performance status.

Optimal debulking surgery (upfront or interval post NACT) could be achieved in 12 cases. These included 6 stage III cases and 2 stage IV patients. Four cases were stage I/II. Suboptimal debulking surgery was done in 7 cases (all were stage III disease). Paclitaxel in combination to carboplatin was given to 6 patients as NACT and as adjuvant therapy in 8 patients. Three stage III patients who had best survivals of 38 months (NED), 40 months (AWD), and 20 months had been given NACT (Pacli + Carbo). Other drugs used in various combinations included gemcitabine, ifosfamide, epirubicin, and liposomal doxorubicin. ([Table 2] depicts the surgical and chemotherapy management protocols). The follow-up of patients (optimal vs. suboptimal debulking) is shown in [Table 3].
Table 2: Management of OMMMT

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Table 3: Follow up of pati ents (opti mal vs. sub-opti mal debulking)

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In 18 patients (2 Stage II and 15 Stage III/IV), follow up of 4 or more months was available with a median follow up of 15 months (4-40 months). Three patients died at 33 months, 12 months, and 10 months of diagnosis. Nine out of 17 had one or more recurrences or metastases with common sites being omentum, vault, retroperitoneal nodes, liver, and brain. In 3 other patients, there was no recurrence at 10, 20, and 38 months (post-NACT + optimal interval debulking). Earliest recurrence was at 9 months (post-optimal surgery) in advanced stage disease patients (median 10.5 months). Overall survival (All stages) at 38 months was 63% [Table 4] [Figure 5].
Table 4: Comparison of studies

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Figure 5: Overall survival (all stages) at 38 months

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For epithelial predominant tumors, median recurrence-free interval (RFS) was 13 months and if they were optimally debulked, the median RFS was 17.6 months. In comparison for sarcoma predominant tumors, median RFS was 10.5 months and if they were optimally debulked, the median RFS was 15.6 months. This, however, was not found to be statistically significant. Presence of hyaline globules did not correlate with the clinical behavior or outcome


   Discussion Top


Carcinosarcoma of the female genital tract, also known as (malignant) mixed mullerian (mesodermal) tumors, are biphasic tumors comprised of varying proportion of both malignant epithelial and mesenchymal (stromal) components. Current evidence implicates metaplastic transformation of epithelial component, which initiates tumorigenesis and gives rise to sarcomatous component. [2],[3] They most commonly are identified in the uterine corpus. Primary ovarian MMMT are uncommon and account for about 1-3% of all ovarian malignancies. [1],[5]

The diagnosis of primary ovarian MMMT is rarely suspected or confirmed preoperatively, as the clinical presentation and radiology on CT scan is similar to ovarian epithelial tumors. Tumor markers such as CA- 125 may be measured, but they may be raised or may be in the normal range. Even cytological analysis of ascitic fluid in positive cases may yield malignant epithelial components in majority of cases. [10] In the present series, CA-125 was raised in 9 out of the 12 cases, in which it was measured preoperatively. In 4 patients, the hemorrhagic ascitic fluid revealed adenocarcinomatous component.

Boucher et al., in their series of 15 cases found equal representation of the epithelial endometrioid (4 cases) and serous (4 cases) component types. The mesenchymal component was largely heterologous, of which 5 were of chondromatous and 5 of rhabdomyoblastic differentiation. [8] However, Kunkel et al. in a recent series had an overwhelming serous carcinoma component in 57% of their cases with a predominance of heterologous cartilaginous component in 36%. [11] In comparison, we found endometrioid carcinoma and heterologous rhabdomyosarcoma in the present series.

Hyaline globules, as seen in 15 of our cases, may been seen in OMMMT and may be reactive to alpha-1-antitrypsin. [8] If seen in a small biopsy sample, this morphological finding may aid in pre-operative diagnosis of OMMMT. The presence of peculiar basement membrane thickening seen in one of cases of OMMMT has not been previously reported, although stromal hyalinization and deposition of basement membrane material has been seen in clear cell ovarian carcinomas. We surmise that this morphological alteration in basement membrane may be biologically related to the phenomenon of epithelial-mesenchymal transition, which plausibly underlies the pathogenesis of these tumors. [12],[13] Malignant germ cell tumor and neuroectodermal elements resembling immature teratoma have been rarely seen in combination with OMMMT. [14],[15] Most of these reported cases have presented in advanced stages. Three similar cases seen in our series presented in stage III.

The influence of proportion of the malignant epithelial or sarcomatous component, as also heterologous vs. homologous, on the disease progression is a matter of debate. [7],[9],[16],[17] In a recent study of 47 cases of OMMMT, features of sarcomatous components including type of sarcoma, homologous or heterologous, mitotic count, necrosis, and presence of sarcomatous component outside the ovary were studied in relation to disease-specific survival. They concluded that presence of sarcomatous component outside the ovary was an adverse prognostic factor. [11]

In another study of 34 cases, 17 of which were treated with primary surgery followed by adjuvant chemotherapy for FIGO stage III or IV, statistical analysis showed that stromal predominant tumors, suboptimal debulking, age, and tumors with serous epithelial component were adverse independent prognostic factors. [9] Although limited by follow up time interval, our study also demonstrates the trend of sarcoma predominant OMMMT behaving more aggressively (median RFS 10.5 months vs. 13 months for epithelial predominant). Optimal debulking of these tumors, in our series, delayed the time to recurrence. A comparison of various studies is listed in [Table 4].[22]

In conclusion, we have described the pathological features of a series of primary ovarian carcinosarcoma, a rare biphasic malignancy with variable proportions of epithelial and spindle elements, seen at our institute. Majority of the patients present in advanced stage of disease. Presence of hyaline globules within spindle sarcoma in a small biopsy from an ovarian/pelvic mass should alert the pathologists regarding MMMT. Although our study has several limitations in terms of being a retrospective study with patients who were managed heterogeneously (institutional and referral), it does suggest a trend that advanced stage, suboptimal cytoreduction, and stromal predominant tumors are poor prognostic indicators in OMMMT. Treatment includes a multimodal approach with combination of optimal debulking surgery and chemotherapy, either neoadjuvant or adjuvant. Large multi-institutional studies would be required to enhance our understanding of the disease process and optimize treatment.

 
   References Top

1.Mano MS, Rosa DD, Azambuja E, Ismael G, Braga S, D'Hondt V, et al. Current management of ovarian carcinosarcoma. Int J Gynecol Cancer 2007;17:316-24.  Back to cited text no. 1
    
2.Kounelis S, Jones MW, Papadaki H, Bakker A, Swalsky P, Finkelstein SD. Carcinosarcomas (malignant mixed mullerian tumors) of the female genital tract: Comparative molecular analysis of epithelial and mesenchymal components. Hum Pathol 1998;29:82-7.  Back to cited text no. 2
    
3.Kupryjanczyk J, Thor AD, Beauchamp R, Poremba C, Scully RE, Yandell DW. Ovarian, peritoneal, and endometrial serous carcinoma: Clonal origin of multifocal disease. Mod Pathol 1996;9:166-73.  Back to cited text no. 3
    
4.Jin Z, Ogata S, Tamura G, Katayama Y, Fukase M, Yajima M, et al. Carcinosarcomas (malignant mullerian mixed tumors) of the uterus and ovary: A genetic study with special reference to histogenesis. Int J Gynecol Pathol 2003;22:368-73.  Back to cited text no. 4
    
5.Barnholtz-Sloan JS, Morris R, Malone JM Jr, Munkarah AR. Survival of women diagnosed with malignant, mixed mullerian tumors of the ovary (OMMMT). Gynecol Oncol 2004;93:506-12.  Back to cited text no. 5
    
6.Silasi DA, Illuzzi JL, Kelly MG, Rutherford TJ, Mor G, Azodi M, et al. Carcinosarcoma of the ovary. Int J Gynecol Cancer 2008;18:22-9.   Back to cited text no. 6
    
7.Morrow CP, d'Ablaing G, Brudy LA, Blessing JA, Hreschyschyn MM. A clinical and pathologic study of 30 cases of malignant mixed mullerian epithelial and mesenchymal ovarian tumors: A gynecologic oncology group study. Gynecol Oncol 1984;18:278-91.  Back to cited text no. 7
    
8.Boucher D, Tetu B. Morphologic prognostic factors of malignant mixed mullerian tumors of the ovary: A clinicopathologic study of 15 cases. Int J Gynecol Pathol 1994;13:22-8.   Back to cited text no. 8
    
9.Athavale R, Thomakos N, Godfrey K, Kew F, Cross P, de Barros Lopes A, et al. The effect of epithelial and stromal tumor components on FIGO stages III and IV ovarian carcinosarcomas treated with primary surgery and chemotherapy. Int J Gynecol Cancer 2007;17:1025-30.  Back to cited text no. 9
    
10.Reed N, Millan D, Verheijen R, Castiglione M. ESMO Guidelines Working Group. Non-epithelial ovarian cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2010;21Suppl 5:v31-6.   Back to cited text no. 10
    
11.Kunkel J, Peng Y, Tao Y, Krigman H, Cao D. Presence of a sarcomatous component outside the ovary is an adverse prognostic factor for primary ovarian malignant mixed mesodermal/mullerian tumors: A clinicopathologic study of 47 cases. Am J Surg Pathol 2012;36:831-7.  Back to cited text no. 11
    
12.Mikami Y, Hata S, Melamed J, Moriya T, Manabe T. Basement membrane material in ovarian clear cell carcinoma: Correlation with growth pattern and nuclear grade. Int J Gynecol Pathol 1999;18:52-7.  Back to cited text no. 12
    
13.Stewart CJ, McCluggage WG. Epithelial-mesenchymal transition in carcinomas of the female genital tract. Histopathology 2013;62:31-43.  Back to cited text no. 13
    
14.García-Galvis OF, Cabrera-Ozoria C, Fernández JA, Stolnicu S, Nogales FF. Malignant Müllerian mixed tumor of the ovary associated with yolk sac tumor, neuroepithelial and trophoblastic differentiation (teratoid carcinosarcoma). Int J Gynecol Pathol 2008;27:515-20.  Back to cited text no. 14
    
15.Matsuura Y, Kitajima M, Hachisuga T, Tanimoto A, Okura N, Kihara I. Malignant mixed müllerian tumor with malignant neuroectodermal components (teratoid carcinosarcoma) of the ovary: Report of a case with clinicopathologic findings. J Obstet Gynaecol Res 2010;36:907-11.  Back to cited text no. 15
    
16.Harris MA, Delap LM, Sengupta PS, Wilkinson PM, Welch RS, Swindell R. Carcinosarcoma of the ovary. Br J Cancer 2003;88:654-7.  Back to cited text no. 16
    
17.Hellström AC, Tegerstedt G, Silfverswärd C, Pettersson F. Malignant mixed müllerian tumors of the ovary: Histopathologic and clinical review of 36 cases. Int J Gynecol Cancer 1999;9:312-6.  Back to cited text no. 17
    
18.Rutledge TL, Gold MA, McMeekin DS, Huh WK, Powell MA, Lewin SN, et al. Carcinosarcoma of the ovary-a case series. Gynecol Oncol 2006;100:128-32  Back to cited text no. 18
    
19.Thigpen TJ, Blessing JA, DeGeest K, Look KY, Homesley HD. Gynecologic Oncology Group. Cisplatin as initial chemotherapy in ovarian carcinosarcomas: A Gynecologic Oncology Group study. Gynecol Oncol 2004;93:336-9.  Back to cited text no. 19
    
20.Brown E, Stewart M, Rye T, Al-Nafussi A, Williams AR, Bradburn M, et al. Carcinosarcoma of the ovary: 19 years of prospective data from a single center. Cancer 2004;100:2148-53.  Back to cited text no. 20
    
21.Sood AK, Sorosky JI, Gelder MS, Buller RE, Anderson B, Wilkinson EJ, et al. Primary ovarian sarcoma: Analysis of prognostic variables and the role of surgical cytoreduction. Cancer 1998;82:1731-7.  Back to cited text no. 21
    
22.Le T, Krepart GV, Lotocki RJ, Heywood MS. Malignant mixed mesodermal ovarian tumor treatment and prognosis: A 20 year experience. Gynecol Oncol 1997;65:237-40.  Back to cited text no. 22
    

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Correspondence Address:
Santosh Menon
Department of Pathology, 8th Floor, Annexe Building, Tata Memorial Hospital, Dr Ernest Borges Marg, Parel - 400 012,Mumbai, Maharashtra
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0377-4929.125293

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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]

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