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A 20 YEARS' EXPERIENCE ON GRANULOSA CELL TUMOUR.

BACKGROUND

Ovarian sex cord stromal cells are known for their rarity comprising of 2-3% of all primary ovarian cancers.

They are known for their heterogeneity as well. From benign to malignant subtypes, there are several varieties known. They develop from the proliferating cells which produce cells to support and surround oocytes, which includes the cells that produce ovarian hormones. The different types of sex cord stromal tumours include fibromathecoma, granulosa cell tumour (adult and juvenile, which differentiates into female characteristics), Sertoli-Leydig cell tumour (which differentiates into male characteristics). Granulosa cell tumour have the most common malignant potential among the sex cord stromal cell tumours as described by Rokitansky in 1855. [1]

The adult subtype is often seen in the middle aged and old aged women with a median age of 50-54 years. The juvenile subtype comprises of only 5% of the total sex cord stromal tumours, typically develop before puberty, common in children and young women being highly proliferative but with a lower risk of recurrence. [2]

Malignant sex cord tumour cells are diagnosed at an earlier stage and are considered to be low-grade malignancies compared to the primary ovarian cancers. Granulosa cell tumour present with features of hyperoestrogenism such as abnormal vaginal bleeding and precocious puberty. [3]

Complete surgery is the main stay of the management in early stages. Adjuvant platinum-based chemo is indicated in advanced stages. Though granulosa cell tumours have favourable prognosis, late relapses are known to occur due to the indolent nature of the disease. Advanced disease has a poor prognosis with 5-year survival rate of 0-20% in comparison to epithelial ovarian cancer. [4]

The most common prognostic factors known in granulosa tumours are age, tumour size, tumour stage, bilaterality, postop residual tumour status and high mitotic index. [5-15]

The prognostic factors and the recurrent nature is unclear and unpredictable added to the fact that these tumours are rare and have an indolent course. There is only a scarce data on the optimum treatment for this group of patients. The present study is conducted to pursue the clinico-pathological features and prognostic factors for the recurrence patterns and the optimal management of these cases.

MATERIALS AND METHODS

This is a descriptive study with secondary data from records. All cases of histologically proven and treated patients between 1993 and 2015 in the Department of Obstetrics and Gynaecology were analysed retrospectively with the medical records. Information on the patient's characteristics, clinical presentation, International Federation of Gynaecology and Obstetrics Staging (FIGO), surgical details, adjuvant details, recurrences, management of recurrences and follow-up until 2015 were analysed.

Size of the tumour was ascertained by preoperative ultrasound or computer tomography. All patients had surgery. The complete staging laparotomy included total abdominal hysterectomy + bilateral salpingo-oophorectomy with optimal resection (RO), omentectomy, +/- lymphadenectomy and multiple biopsies. All other surgeries constituted partial surgical staging. Fertility preserving surgery or fertility sparing surgery was defined as preservation of the uterus and at least one adnexa. In advanced stages, patient received chemotherapy. Other patients were put on active surveillance.
Characteristics

Age          Percentage

<10              3
10-19            3
20-29            17
30-39            20
40-49            28
50-59            28
60-70            26
>70              1
Median Age


Total 126 patients- Premenopausal 58 patients and Postmenopausal 44 patients.
Symptoms                  N%

Abdominal pain            40
Palpable mass             20
Abdominal distension      6
Precocious puberty        2
Virilisation              2
Mastalgia                 1
Menorrhagia               33
Postmenopausal bleeding   24
Secondary amenorrhea      0
Constipation              0
Urinary tract symptoms    0

Surgical Approach: Laparotomy and     126 (100%)
Laparoscopy                             n (%)

FIGO Stage                              N (%)
Ia                                        79
Ib                                        14
Ic                                        11
Ila                                       1
IIb                                       1
IIc                                       2
IIIa                                      7
IIIb                                      4
IIIc                                      4
IV                                        3
Surgical staging                         n(%)
Complete surgical staging                 85
Incomplete surgical staging               41
PLND                                     n(%)
No                                        44
Yes                                       82
Fertility sparing surgery                n(%)
Yes                                       10
No                                       116
Postoperative residual tumour            n(%)
Yes                                       41
No                                        85
Intraoperative tumour rupture            n(%)
Yes                                       5
No                                       121


Out of the 84 patients who had complete surgery, those who had chemotherapy did not show recurrence. Out of the 77 patients who were on observation, 3 patients had recurrences.
Details of Chemotherapy in the Patients

1    45    IIIc AGCT     > 10 cm     Incomplete    15 months
                                      Surgery

2    55    IIIc AGCT      12 cm      Incomplete     5 months
                                      Surgery

3    35     Ic SCST        9 cm       Complete     89 months
                                      Surgery

4    56    IIIc SCST    8.1 x 8.1    Incomplete     3 months
                            cm        Surgery

5    42     Ic AGCT       25 cm      Incomplete    11 months
                                      Surgery

6    65     Ia AGCT       8 x 9       Complete     12 months
                                      Surgery

7    26     IV AGCT       20 cm         FSO        25 months

8    25    IIIc AGCT        NA       Incomplete    24 months
                                      Surgery

9    42     IV SCST       10 cm      Incomplete    26 months
                                      surgery

10   18     Ic SCST        9 cm         FSO        Progressed
                                                  at 11 months

11   14     Ia JGCT       10 cm         FSO        Progressed
                                                  at 7 months

12   23   Ic androgen    7 x 9 cm       FSO         8 months
           secreting

13   40     Ia AGCT      9 x 9cm      Complete     10 months
                                      surgery

14   44     Ic AGCT         NA          FSO        26 months

15   30     IV AGCT         NA       Incomplete    Progressed
                                      surgery

16   48    IIIa AGCT        NA        Complete      At 76th
                                      surgery        month

17   40    IIIc AGCT     18 x 20     Incomplete    Progressed
                            cm        surgery

18   60    IIIa AGCT        NA        Complete     No relapse
                                      Surgery

19   57     Ia AGCT     15 x 10 cm    Complete     No relapse
                                      surgery

20   42    IIIc AGCT        NA       Incomplete    Defaulted
                                      surgery

21   50    IIIc AGCT        NA        Complete     No relapse
                                      surgery

22   58    IIIC AGCT     8 x 8 cm     Complete     30th month
                                      surgery

23   48     Ic AGCT         NA        Complete     37th month
                                      surgery

24   21    IIIc JGCT        NA          FSO        Defaulted

25   38    IIa AGCT       10.6 x      Optimal      10 months
                         11.94 cm     surgery

26   21     Ia AGCT       10 cm         FSO        12 months

27   52     Ia AGCT         NA       Incomplete    24 months
                                      Surgery

28   55     Ia AGCT        6 cm      Incomplete    24 months
                                      surgery

29   19     Ia AGCT       10 cm         FSO        13 months

30   28     Ia AGCT        7 cm       Complete     75 months
                                      Surgery

31   44     Ic AGCT      11 x 12     Incomplete    23 months
                            cm        Surgery

32   54    IIIc AGCT      9 x 10     Incomplete    16 months
                            cm        Surgery

33   60    IIIC AGCT     13 x 13     Incomplete    12 months
                                      Surgery

34   67    IIC AGCT      10 x 10     Incomplete    24 months
                                      Surgery

1    Pelvis and LN and     2 lines of chemo, CDDP +
        Left adnexa          VCR, then CDDP + VP16
                                 oral Endoxan

2        Myometrial        2 lines of chemo, CDDP +
        infiltration         VCR, then CDDP + VP16
      present upfront,

3     Omentum + Pelvis        CDDP + Ctx 6 cycles
                              chemo, then CDDP +
                                   Etoposide

4          Pelvis                     BEP

5          Pelvis          Initially no chemo, Ctx +
                           CDDP 6 cycles, then CDDP
                            + Etoposide x 6 cycles

6          Pelvis         No initial chemo, 4 cycles
                               CDDP + CTx chemo

7          Pelvis            CDDP + Bleo + Vinb 3
                          cycles initially PR, then 2
                               years on Endoxan

8      Omentum + PAN       Initially no chemo, PEB;
                            VAC; CDDP + Ctx each 6
                                    cycles

9          Liver           3 cycles chemo initially,
                               then 6 cycles EP

10         Pelvis                2 lines chemo

11         Pelvis                     EP

12         Pelvis                PEB 4 cycles

13          nil              CDDP + CT x 6 cycles
                                     alone

14         Pelvis         No initial chemo, 6 cycles
                                  CDDP + Ctx

15         Pelvis            CDDP + VP16 4 cycles,
                                 then 3 cycles

16         Pelvis         No initial chemo, 6 cycles
                                  CDDP + Ctx

17        Omentum             6 cycles CDDP + Ctx

18          nil                 6 cycles alone

19          nil                 5 cycles alone

20    Omentum, Pelvis              Defaulted

21          nil              6 cycles chemo alone

22         Pelvis          6 cycles chemo initially
                          post-surgery after relapse
                             CDDP + Etoposide; PVB

23          nil                 6 cycles alone

24         Pelvis                  2 cycles

25    Pelvis, Omentum         6 cycles initially

26         Liver              CDDP + Etoposide 6
                                    cycles

27      Omentum and       Initially no chemo, 2 lines
            PAN                      chemo

28         Liver                   Defaulted

29      Omentum and       Initially no chemo, 3 lines
           Pelvis                    chemo

30         Pelvis         Initially no chemo, 2 lines

31         Pelvis          Initially no chemo, CDDP+
                             Ctx, then CDDP + Etop

32         Pelvis          Initially no chemo, CDDP+
                             Ctx, then CDDP + Etop
                                   then PVB

33         Pelvis           CDDP + CTx, then CDDP +
                                     Etop

34         Pelvis          CDDP + CTX 6 cycles, then
                                  CDDP + Etop

1       Alive with      Alive
        disease 90
          months

2    Lost for follow-   LTFU
         up by 16
          months

3       123 months      Alive
          alive

4      at 3 months      Died

5     133 months on     Alive
     follow-up alive

6       Alive 150       Alive
          months

7       Dead at 8       Died
          months

8       Alive 132       Alive
          months

9       Dead at 35      Died
          months

10      Dead at 23      Died
          months

11      Dead at 7       Died
          months

12       Alive 85       Alive
          months

13       Alive 87       Alive
          months

14      Alive 120       Alive
          months

15     Dead at 2nd      Died
          month

16      98 months       Alive
          alive

17    5 months dead     Died

18      43 months       Alive
          Alive

19      72 months       Alive
          alive

20      Dead at 3       Died
          months

21      126 months      Alive
          Alive

22     At 61 months     Alive
          alive

23      Alive 148       Alive
          months

24   Lost for follow-   LTFU
            up

25      83 months       Alive
          alive

26      Dead at 14      Died
          months

27     Alive at 140     Alive
          months

28      Dead at 26      Died
          months

29       Alive 98       Alive
          months

30       Alive 75       Alive
          months

31       Alive 85       Alive
          months

32      LTFUat 28       LTFU
          months

33      Dead at 27      Died
          months

34      Dead at 33      Died
          months


Statistical Analysis

The collected data was analysed with IBM SPSS statistics software 23.0 Version. To describe about the data descriptive statistics frequency analysis, percentage analysis was used. For survival analysis, the Kaplan-Meyer curve with log-rank method was used for the comparison of groups. In the above statistical tools, the probability value of .05 will be considered as significant level. Kaplan-Meier analysis is one of the best ways to measure the proportion of patients living for a certain amount of time after treatment. The time starting from a defined point to the occurrence of a given event, for example death is called as survival time and the analysis of group data as survival analysis. The effect of an intervention is assessed by measuring the number of patients survived after that intervention over a period of time.

The chance of occurrence of events over a period of time is computed and multiplying these successive probabilities by any earlier computed probabilities will give the final estimated values, which are used for plotting survival curves.

RESULTS

This is an analysis of the survival rate and the treatment results of Granulosa cell tumour between 1995 and 2015 over a period of 20 years. We have analysed the results of 126 patients, of which 53 patients (42%) were premenopausal and 73 patients (58 %) were postmenopausal. Out of the 126 patients, 84 patients had complete surgical staging which constitutes transabdominal hysterectomy and bilateral salpingo-oophorectomy and a staging laparotomy, 35 patients had incomplete or suboptimal surgery, 7 patients had fertility sparing operation. The 67 patients who had complete surgery and early stage disease with no risk factors were on observation. These patients have not had relapse. 7 patients after complete surgical staging had chemotherapy with Cisplatin and Cyclophosphamide. Amongst them 2 patients had recurrence and were given chemo with good response surviving. Out of the 35 patients who had incomplete surgery, 13 patients had adjuvant chemo with Cisplatin and Cyclophosphamide and 22 patients were on observation. Amongst the 22 patients who were on observation 6 patients recurred and were treated with 2-3 lines of chemo. Out of the 6 patients, 4 patients are alive, and 2 patients died due to progressive treatment. In the 13 patients who had chemo, one relapsed and died without any 2nd line chemo. 9 patients recurred were given 2nd line chemo with Cisplatin and Etoposide and 3 rd line with Cisplatin, Vinblastine and Bleomycin or Bleomycin, Etoposide and Cisplatin. 7 patients had fertility sparing surgery and one of them had adjuvant chemo with no relapse. The 6 patients who did not have adjuvant chemo recurred. Amongst, the 6 patients 1 was lost for follow-up, 3 patients died after 2nd line chemo and 2 patients are alive.

On analysing the chemotherapy details and the pattern of failure, there were few points which were clear. In the complete surgery group, those with adjuvant chemo did not relapse. Those who relapsed were treated with chemo and had good response to treatment and survived. Those with incomplete surgery had increased risk of recurrence, especially when the size of the tumour was > 9 cm, when there was tumour spill and when the stage was advanced. In the fertility sparing group also, those with lower stage with chemo did better than those with late stage disease, those without chemo or with increased risk factors.

A dataset of 34 patients is analysed, out of these 19 patients have survived cancer. Out of 34 cases, 10 patients had complete surgery and 15 patients had incomplete surgery. Kaplan-Meier survival analysis results show that cancer was cured by complete surgery followed by chemotherapy wherever high-risk factors were present, whereas the survival rate drastically declined in the cases of incomplete surgery without adjuvant chemotherapy. For patients, stage of cancer, size of the tumour, type of surgery done, tumour spill, histopathology, chemotherapy in positive high-risk parameters, has relatively more effect on survival chance.

Analysis of the Treatment Details of Relapsed Patients

Time of Relapse (Vs) Treatement
Treatment.given.on.relapse   11 months   12 months   13 months

4cyclescddp+ctxchemo                     1
6xcddp+ctx
6xcddp+ctx_and_                          1
  6xcddp+etop
6xcddp+ctx_and_                                      1
  6xcddp+etop_and_4xpvb
6xep                         1           1
6xep_and_pvb
cddp+vp164cyclesthen
  3cycles
defaulted
nil
peb_and_vac_and_cddp_
  ctxeach6cycles
prthen2yrsonendoxan

Treatment.given.on.relapse   16 months   23 months   24 months

4cyclescddp+ctxchemo
6xcddp+ctx
6xcddp+ctx_and_                                      2
  6xcddp+etop                            1
6xcddp+ctx_and_              1
  6xcddp+etop_and_4xpvb
6xep
6xep_and_pvb
cddp+vp164cyclesthen
  3cycles
defaulted                                            1
nil
peb_and_vac_and_cddp_                                1
  ctxeach6cycles
prthen2yrsonendoxan

Treatment.given.on.relapse   25 months   26 months   30th month

4cyclescddp+ctxchemo
6xcddp+ctx                               1
6xcddp+ctx_and_
  6xcddp+etop
6xcddp+ctx_and_
  6xcddp+etop_and_4xpvb
6xep                                     1
6xep_and_pvb                                         1
cddp+vp164cyclesthen
  3cycles
defaulted
nil
peb_and_vac_and_cddp_
  ctxeach6cycles
prthen2yrsonendoxan          1

Treatment.given.on.relapse   75 months   89 months   at 76th
                                                     month

4cyclescddp+ctxchemo
6xcddp+ctx                                           1
6xcddp+ctx_and_              1
  6xcddp+etop
6xcddp+ctx_and_
  6xcddp+etop_and_4xpvb
6xep                                     1
6xep_and_pvb
cddp+vp164cyclesthen
  3cycles
defaulted
nil
peb_and_vac_and_cddp_
  ctxeach6cycles
prthen2yrsonendoxan

Treatment.given.on.relapse   defaulted   no relapse   progressed

4cyclescddp+ctxchemo
6xcddp+ctx                   1
6xcddp+ctx_and_
  6xcddp+etop
6xcddp+ctx_and_
  6xcddp+etop_and_4xpvb
6xep
6xep_and_pvb
cddp+vp164cyclesthen                                  1
  3cycles
defaulted                    1
nil                                      10
peb_and_vac_and_cddp_                                 1
  ctxeach6cycles
prthen2yrsonendoxan

Treatment.given.on.relapse   progressed    progressed
                             at 7 months   at 11 months

4cyclescddp+ctxchemo
6xcddp+ctx
6xcddp+ctx_and_
  6xcddp+etop
6xcddp+ctx_and_
  6xcddp+etop_and_4xpvb
6xep                                       1
6xep_and_pvb
cddp+vp164cyclesthen
  3cycles
defaulted
nil                          1
peb_and_vac_and_cddp_
  ctxeach6cycles
prthen2yrsonendoxan

Time.to. Relapse

Sum of Number of Patients for each Time.to.Relapse. Color shows details
about Treatment.given.on.relapse. The marks are
labeled by sum of Number of Patients.

Time of Relapse (Vs) Survival

Time.to.Relapse

                             alive   died   ltfu

11 months                    1
12 months                    1       2
13 months                    1
16 months                                   1
23 months                    1
24 months                    2       2
25 months                            1
26 months                    1       1
30th month                   1
75 months                    1
89 months                    1
at 76th month                1
defaulted                            1      1
no relapse                   8       1      1
progressed                           2
progressed at 7 months               1
progressed at 11 months              1

Sum of Number of Patients for each Time.to.Relapse. Color shows details
about Survival. The marks are labeled by sum of
Number of Patients.

Survival_Sugery_Stage_Tumor size

Survival/Surgery

                           Survival

alive                 alive   died    ltfu

complete surgery      10
fso                   3
incomplete surgery    5
optimal surgery       1

died

fso                            4
incomplete surgery             8

ltfu

fso                                    1
incomplete surgery                     2

                           Stage

             ia   ic   iia   iic   iiia   iiic   iv

6 cm         1
7 cm         1
7x9 cm            1
8.1x8.1 cm                                1
8x8 cm                                    1
8x9          1
9 cm              2
9 x 10 cm                                 1
9x9 cm       1
10 cm        2                                   1
10.6x11.9              1
10cm      1
10x10                        1
11x12 cm          1
12 cm                                     1
13x13                                     1
15x10 cm     1
18x20 cm                                  1
20 cm                                            1
25 cm             1
>10cm                                     1
NA                2                2      4      1

Survival (Vs) Stage

Stage   alive   died   ltfu

ia        6      3
ic        6      1
iia       1
iic              1
iiia      2      4
iiic      4      3      3
iv

Note: Table made from bar graph.

Survival Plot with Respect to Stage

            0   20   40   60   80

                      Time

Stage=Ia    9   3    1    1    0
Stage=Ic    7   3    1    1    1
Stage=IIa   1   0    0    0    0
Stage=IIC   1   1    0    0    0
Stage=IIa   2   1    1    1    0
Stage=IIc   8   2    0    0    0
Stage=IV    2   2    0    0    0

Survival Plot with Respect to Surgery

                             0    20   40   60   80

Surgery=Complete Surgery     10   4    3    3    1
Surgery=FSO                  7    2    0    0    0
Surgery=Incomplete Surgery   12   5    0    0    0
Surgery=Optimal surgery      1    0    0    0    0

Survival Plot with Respect to Histopathology

                                6    20   40   60   80

HPE=AGCT                        24   10   2    2    0
HPE=androgen secreting tumor    1    0    0    0    0
HPE=JGCT                        1    0    0    0    0
HPE=SCST                        4    2    1    1    1


DISCUSSION

Granulosa cell tumours are a subtype of malignant sex cord stromal tumours. It has two histological types, namely adult 95% and juvenile 5%. Adult type occurs in postmenopausal women in the 5th decade with favourable prognosis. Juvenile type occurs in younger age with severe symptoms and signs and increased risk of recurrence implicating poorer prognosis. Hyperoestrogenic symptoms have been reported in a retrospective study of 118 patients with abnormal uterine bleeding, hyperplastic endometrium. It can also produce precocious puberty, mastalgia and galactorrhoea. [4]

Granulosa cell tumours radiologically presents as a solid tumour with cystic component with a median size of 12 cm. [5] Diagnosis of granulosa cell tumour is through histopathology. The adult form has 5 subtypes the most common is microfollicular with call exner bodies. The Juvenile form is with macrofollicular with lobulated architecture and few callexner bodies. The common immunohistochemical markers expressed by these cells are alpha inhibin, CD 99, Vimentin; serum tumour markers are inhibin, estradiol, anti-Mullerian hormone. [6] Serum CA-125 are not of any significance in this tumour variety. [7] FOXL2 gene mutation has been identified in 97% of adult granulosa cell tumour and 10% of juvenile type. The common differential diagnosis with this entity are stromal sarcoma, carcinoid tumour, endometrial cancer and adenocarcinoma. The main modality of treatment here is complete staging laparotomy with transabdominal hysterectomy and bilateral salpingo-oophorectomy with pelvic and para-aortic lymph node resection. For women who would like to preserve the fertility in stage I unilateral salpingo-oophorectomy with uterine preservation is done. In majority of the cases, where the tumour is limited to one ovary the patients are just kept of close follow-up with observation. In case, the stage is IC (Tumour size > 10-15 cm) or there are high risk features such as tumour rupture or poorly differentiated tumour or advanced stages (Stage III or IV). The outcome is unfavourable, therefore in such cases adjuvant chemotherapy is given. [11] However, the value-add and the significance of the use of the adjuvant chemo is yet to be validated given the rarity of the disease and the difficulty in conducting randomised trial in such rarity. The recommended chemotherapy options available are Paclitaxel + Carboplatin, Bleomycin + Etoposide + Cisplatin (BEP) Etoposide + Cisplatin (EP), Cyclophosphamide + Doxorubicin + Cisplatin (CAP) and platin alone. [10]

In children with juvenile granulosa cell tumour, the usage of adjuvant chemo yields complete and a long-lasting response which is usually given in Stage Ic with a high mitotic index (> 20 per high power field). Long surveillance is recommended in granulosa cell tumour, as these tumours have an indolent course. The median time to relapse ranges from 4 years to 30 years. [12] The sites of recurrence commonly are pelvis, retroperitoneum and upper abdomen. Local relapse is managed with complete resection when feasible. The other chemo regimens in inoperable tumours or the recurrent tumours would be Docetaxel, Paclitaxel + Ifosfamide, Paclitaxel + Carboplatin and VAC. [13] The hormonal treatment used are Tamoxifen alone, Megestrol or in combination which does produce sustained long-term clinical response. The investigational agents in relapse cases includes anti-angiogenic therapy, LHRH antagonist and mTOR inhibitors. [14] Large tumour size > 10 cm is associated with poor prognosis. In Sehouili's trial, survival was lower with suboptimal surgery or residual tumour or tumour rupture. [15,16,17]

CONCLUSION

Granulosa cell tumours are known for their rarity. They occur both in premenopausal and postmenopausal women. Patients who had tumour size of > 10 cm seem to have more recurrence. Juvenile granulosa cell tumour and sex cord stromal tumours have poorer prognosis as compared to adult granulosa tumour. The role of chemotherapy is explicit in operated cases, as adjuvant in high risk group decreasing the recurrence rates. Chemotherapy has a compelling role in locally advanced cases, inoperable cases, metastatic cases, in cases with tumour spill or rupture, certain histopathological variants (such as juvenile granulosa cell tumour, yolk sac tumour), tumours > 10 cm. Other factors which do contribute to the prognosis would be age at diagnosis, nuclear atypia, mitotic index, surgical method and presence of residual disease after initial surgery. [18,19,20]

REFERENCES

[1] Seagle BL, Ann P, Butler S, et al. Ovarian granulosa cell tumor: A National Cancer Database study. Gynecol Oncol 2017;146(2):285-91.

[2] Calaminus G, Wessalowski R, Harms D, et al. Juvenile granulosa cell tumors of the ovary in children and adolescents: results from 33 patients registered in a prospective cooperative study. Gynecol Oncol 1997;65(3):447-52.

[3] Segal R, DePetrillo AD, Thomas G. Clinical review of adult granulosa cell tumors of the ovary. Gynecol Oncol 1995;56(3):338-44.

[4] Khosla D, Dimri K, Pandey AK, et al. Ovarian granulosa cell tumor: clinical features, treatment, outcome and prognostic factors. N Am J Med Sci 2014;6(3):133-8.

[5] Pautier P, Lhomme C, Culine S, et al. Adult granulosa-cell tumor of the ovary: a retrospective study of 45 cases. Int J Gynecol Cancer 1997;7(1):58-65.

[6] Shim SH, Lee SJ, Kim DY, et al. A long-term follow-up study of 91 cases with ovarian granulosa cell tumors. Anticancer Res 2014;34(2):1001-10.

[7] Sekkate S, Kairouani M, Serji B, et al. Ovarian granulosa cell tumors: a retrospective study of 27 cases and a review of the literature. World J Surg Oncol 2013;11(1):142.

[8] D'Angelo E, Mozos A, Nakayama D, et al. Prognostic significance of FOXL2 mutation and mRNA expression in adult and juvenile granulosa cell tumors of the ovary. Modern Pathol 2011;24(10):1360-7.

[9] Gershenson DM. Sex cord-stromal tumors of the ovary: Granulosa-stromal cell tumors. Up To Date. https://www.uptodate.com/contents/sex-cordstromal-tumors-of-the-ovary- granulosa-Cell tumors.

[10] NCCN Guidelines for Patients[R] | Ovarian Cancer. www.nccn.org/patients/guidelines/ovarian/index.ht ml

[11] Van Meurs HS, Buist MR, Westermann AM, et al. Effectiveness of chemotherapy in measurable granulosa cell tumors: a retrospective study and review of literature. Intl J Gynecol Cancer 2014;24(3):496-505.

[12] Mangili G, Ottolina J, Gadducci A, et al. Long-term follow-up is crucial after treatment for granulosa cell tumours of the ovary. Br J Cancer 2013;109(1):29-34.

[13] Koutroumpa I, Thomakos N, Sotiropoulou M, et al. Clinicopathological prognostic factors for recurrence in adult granulosa cell tumor of the ovary. Gynecol Oncol 2014;133(Suppl 1):84.

[14] Kottarathil VD, Antony MA, Nair IR, et al. Recent advances in granulosa cell tumor ovary: a review. Indian J Surg Oncol 2013;4(1):37-47.

[15] Malmstrom H, Hogberg T, Risberg B, et al. Granulosa cell tumors of the ovary: prognostic factors and outcome. Gynecol Oncol 1994;52(1):50-5.

[16] Zhang M, Cheung MK, Shin JY, et al. Prognostic factors responsible for survival in sex cord stromal tumors of the ovary- an analysis of 376 women. Gynecol Oncolo 2007;104(2):396-400.

[17] Sehouli J, Drescher FS, Mustea A, et al. Granulosa cell tumor of the ovary: 10 years follow-up data of 65 patients. Anticancer Res 2004;24(2C):1223-30.

[18] Bjorkholm E, Silfversward C. Prognostic factors in granulosa cell tumors. Gynecol Oncol 1981;11(3):26174.

[19] Ayhan A, Salman MC, Velipasaoglu M, et al. Prognostic factors in adult granulosa cell tumors of the ovary: a retrospective analysis of 80 cases. J Gynecol Oncol 2009;20(3):158-63.

[20] Lauszus FF, Peterson AC. Granulosa cell tumor of the ovary: a population-based study of 37 women with stage I disease. Gynecol Oncol 2001;81(3):456-60.

P. Jovita M. Martin (1), Kalaichelvi K (2), Lakshminarasimhan (3), Ramkumar (4), Dheenadhayalan (5)

(1) Assistant Professor, Department of Medical Oncology, SRMC, Chennai, Tamilnadu, India.

(2) Professor, Department of Medical Oncology, Madras Medical College, Chennai, Tamilnadu, India.

(3) Professor, Department of Medical Oncology, SRMC, Chennai, Tamilnadu, India.

(4) Associate Professor, Department of Medical Oncology, IOG, Egmore, Chennai, Tamilnadu, India.

(5) Resident, Department of Medical Oncology, Madras Medical College, Chennai, Tamilnadu, India.

'Financial or Other Competing Interest': None.

Submission 29-05-2018, Peer Review 10-06-2018, Acceptance 13-06-2018, Published 25-06-2018.

Corresponding Author:

P. Jovita M. Martin, AG Alsa Deer Park, #108, Velechery Main Road, Huindy, Chennai-32, Tamilnadu, India.

E-mail: jovimartin4@gmail.com

DOI: 10.14260/jemds/2018/676

Caption: Flow Chart showing the number of patients who relapsed and their Treatment Results
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Title Annotation:Original Research Article
Author:Martin, P. Jovita M.; Kalaichelvi, K.; Lakshminarasimhan; Ramkumar; Dheenadhayalan
Publication:Journal of Evolution of Medical and Dental Sciences
Article Type:Report
Date:Jun 25, 2018
Words:4199
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