Open Access

Current status of tertiary debulking surgery and prognosis after secondary debulking surgery for recurrent Müllerian epithelial cancer in Japan: a retrospective analysis of 164 patients (KCOG-G1402)

  • Tomoko Hirakawa1, 2Email authorView ORCID ID profile,
  • Takeo Minaguchi3,
  • Yoshio Itani1, 4,
  • Yuka Kasamatsu5,
  • Saki Murase6,
  • Shoko Sakurada7,
  • Hiroaki Nagano1, 8,
  • Kazuhiro Takehara9,
  • Tomohiko Tsuruta1, 10,
  • Atsushi Arakawa1, 11,
  • Kouichiro Kawano12,
  • Hiroshi Tsubamoto1, 13,
  • Takashi Ushiwaka1, 14,
  • Taisuke Mori1, 15,
  • Kana Iwai16,
  • Motoaki Saito17,
  • Hiroyuki Morisawa18,
  • Fumitaka Saito19,
  • Kenta Yoshida1, 20,
  • Masanori Kaneuchi21,
  • Hiroki Sato2,
  • Kimihiko Ito1, 10 and
  • Kaei Nasu1, 2
World Journal of Surgical Oncology201715:132

DOI: 10.1186/s12957-017-1200-x

Received: 6 November 2016

Accepted: 3 July 2017

Published: 17 July 2017

Abstract

Background

This study aimed to evaluate the current status of secondary debulking surgery (SDS) and tertiary debulking surgery (TDS; performed for recurrence after SDS) and to assess the overall survival after recurrence of Müllerian epithelial cancer in Japan. We also evaluated the data of patients who underwent a fourth debulking surgery (i.e., quaternary debulking surgery (QDS)).

Methods

We conducted a retrospective study of 164 patients with recurrent Müllerian epithelial cancers (i.e., ovarian, tubal, and peritoneal cancers). The SDS was performed between January 2000 and September 2014 in 20 Japanese hospitals. Clinicopathological data were collected and analyzed.

Results

Of the 164 patients, 66 patients did not have a recurrence or died after SDS. Ninety-eight patients had a recurrence after SDS. Forty-three of the 98 patients underwent TDS; 55 of the 98 patients did not undergo TDS and were classified into the non-TDS group. The overall survival (OS) after SDS was significantly better in the TDS group than in the non-TDS group. The median OS after SDS was 123 and 42 months in the TDS group and non-TDS group, respectively. Of the 43 patients who received TDS, 11 patients were further treated with QDS. The median OS after SDS was 123 months for patients who underwent QDS.

Conclusions

This multicenter study on the prognosis of post-SDS is apparently the first report on QDS in Japan. Patients undergoing TDS have a good prognosis, compared to patients in the non-TDS group. Novel drugs are being evaluated; however, debulking surgery remains a necessary treatment for recurrence.

Keywords

Müllerian epithelial cancer Recurrence Secondary debulking surgery Tertiary debulking surgery Quaternary debulking surgery

Background

The treatment of recurrent ovarian cancer consists mainly of chemotherapy. However, secondary debulking surgery (SDS; also known as secondary cytoreductive surgery) is an effective option if the patients are selected carefully [14]. There are very few reports on Japanese patients treated with SDS, although there is one previous report on 44 Japanese patients [5]. Secondary debulking surgery seems to be effective if complete resection has been achieved. The AGO DESKTOP OVAR Trial (DESKTOP I trial) showed that only complete surgery was associated with prolonged survival in patients with recurrent ovarian cancer [6]. Moreover, the trial presented a predictive score for the resectability of recurrent ovarian cancer. This score model was based on the performance status, the presence of ascites, and the outcome of the primary surgery [6, 7]. The DESKTOP II trial was subsequently the first prospective multicenter trial that successfully validated a clinical score that could be used to predict complete resection [8].

Surgery after SDS (i.e., tertiary debulking surgery (TDS)) is performed in highly selected cases and is rarely reported [913]. Moreover, reports of a fourth debulking surgery (i.e., quaternary debulking surgery (QDS)) are even rarer [1417]. If the efficacy of SDS can be proven, the effectiveness of TDS or additional debulking surgeries should be studied.

With this in mind, the aims of this study were to retrospectively analyze the data of patients with recurrent Müllerian epithelial cancers (i.e., ovarian, tubal, and peritoneal cancers) and to assess the prognostic factors and the current status of recurrence after SDS in Japan.

Methods

We designed a multicenter retrospective study, which included 164 patients with recurrent Müllerian epithelial cancer who were enrolled from 20 hospitals in Japan. The Institutional Review Boards of each hospital approved this study. The patient selection criteria were as follows: a complete response was achieved by the primary treatment, patients were histologically diagnosed with Müllerian epithelial cancers (i.e., ovarian, tubal, and peritoneal cancers), and SDS was performed between January 2000 and September 2014. The performance status of the patients was estimated to be 0 or 1, based on the Eastern Cooperative Oncology Group Performance Status (ECOG-PS) criteria. The exclusion criteria were as follows: a history of other cancer, patients who did not achieve complete response by SDS or subsequent chemotherapy, and patients who underwent palliative surgery at first recurrence (therefore, it was not regarded as SDS). The collected data about the initial treatment included age at the initial diagnosis, clinical and pathological stage (i.e., International Federation of Gynecology and Obstetrics (FIGO) stage), histology, serum cancer antigen-125 (CA125) level, and presence of residual tumor (0, <10, or ≥10 mm) at the primary debulking surgery (PDS). The data collected at recurrence included age, platinum-free interval, serum CA125 level, presence of peritonitis carcinomatosa, and presence of residual tumors at SDS (0, <10, or ≥10 mm). The collected data at the TDS (i.e., recurrence after SDS) were age, serum CA125 level, presence of peritonitis carcinomatosa, site of recurrence, and number of recurrence. Survival time after SDS and data regarding TDS and QDS were also collected. The absence of residual tumor (0 mm) was defined as a complete surgery. The TDS group consisted of patients who underwent debulking surgery for recurrence after SDS. Patients undergoing a fourth or fifth debulking surgery were also included in the TDS group. The non-TDS group consisted of patients who did not undergo a TDS; these patients had not undergone surgery for recurrence after the SDS.

The primary objective was to compare the overall survival (OS) in the TDS group with that in the non-TDS group. The OS was the interval between the date of the SDS and death. Most studies define OS as the survival time from the initial diagnosis. However, in this study, all patients underwent a SDS. The time between the primary treatment and recurrence ranged widely among them; therefore, the definition of OS as the survival time between the date of SDS and death was appropriate.

The secondary objective was to identify the characteristics of the TDS group and the non-TDS group. The platinum-free interval was the interval between the date of the last infusion of platinum for the primary treatment and the date of recurrence. Platinum resistance was defined as recurrence within 6 months after the last platinum treatment. Platinum partial sensitivity was defined as recurrence between 6 and 12 months after platinum treatment. Platinum sensitivity was defined as recurrence after 12 months.

The differences in the background characteristics of the patients were analyzed using the chi-square test. The survival data were analyzed using the Kaplan–Meier method and log-rank test. For all analyses, Statistical Package for Social Science software (IBM SPSS Statistics 24; IBM, Armonk, NY) was used, and P < 0.05 was considered statistically significant.

Results

Figure 1 shows the inclusion criteria for data collection in this study. One hundred sixty-four patients underwent SDS in 20 hospitals. Sixty-six patients did not have a recurrence or died after SDS. Ninety-eight patients had a recurrence after SDS. Forty-three of the 98 patients were classified into the TDS group. Tertiary debulking surgery was performed in 15 hospitals. Among the TDS group, 11 (25.6%) patients underwent QDS, 15 (34.9%) patients did not undergo QDS, and 17 (39.5%) patients did not have a recurrence or died after TDS.
Fig. 1

The inclusion criteria of patients in this study

Fifty-five of the 98 patients did not undergo TDS when they had a recurrence after SDS, and they were classified into the non-TDS group. The non-TDS patients were treated with chemotherapy or the best supportive care.

Table 1 shows the main characteristics of the patients in two groups at the time of initial diagnosis, SDS, and recurrence after SDS. The median ages of the patients at initial diagnosis were 56.9 years (range, 35–74 years) and 54.2 (range, 27–77 years) in the TDS and non-TDS groups, respectively. Forty-two (97.7%) patients in the TDS group and 51 (92.7%) patients in the non-TDS group were diagnosed with ovarian cancer. No cases of tubal cancer were included in the TDS group. There were only two (3.6%) cases of tubal cancer in the non-TDS group. One (2.3%) patient in the TDS group and two (3.6%) patients in the non-TDS group had peritoneal cancer. Serous cystadenocarcinoma was the most common histological type (22 [51.2%] cases in the TDS group and 36 [65.5%] cases in the non-TDS group). Complete surgery at PDS was performed in 34 (79.1%) patients in the TDS group and 33 (60.0%) patients in the non-TDS group. Complete surgery at SDS was performed in 38 (88.4%) patients in the TDS group and 44 (80.0%) patients in the non-TDS group.
Table 1

Clinical characteristics of the tertiary debulking surgery (TDS) group and non-TDS group

Characteristics

TDS (n = 43)

Non-TDS (n = 55)

P value

Primary

 Age, median (range), years

56.9 (35–74)

54.2 (27–77)

 

  <60

24 (55.8%)

35 (63.6%)

0.432

  60

19 (44.2%)

20 (36.4%)

 

 Cancer

  Ovary

42 (97.7%)

51 (92.7%)

0.415

  Fallopian tube

0 (0%)

2 (3.6%)

 

  Peritoneum

1 (2.3%)

2 (3.6%)

 

 FIGO stage

 I, II

10 (23.3%)

13 (23.6%)

0.965

 III, IV

33 (76.7%)

42 (76.4%)

 

 Histology

  Serous

22 (51.2%)

36 (65.5%)

0.333

  Endometrioid

6 (14.0%)

4 (7.3%)

 

  Clear cell

10 (23.3%)

6 (10.9%)

 

  Mucinous

2 (4.7%)

3 (5.5%)

 

  Others

3 (7.0%)

6 (10.9%)

 

 CA 125 (U/ml)

   < 100

10 (23.3%)

7 (12.7%)

0.086

  100

21 (48.8%)

38 (69.1%)

 

  Missing

12 (27.9%)

10 (18.2%)

 

 Residual disease at PDS, mm

  0

34 (79.1%)

33 (60.0%)

0.035

  0-10

8 (18.6%)

11 (20%)

 

  10

1 (2.3%)

10 (18.2%)

 

  Missing

0 (0%)

1 (1.8%)

 

Recurrence at SDS

 Age, median (range), years

59.5 (40–76)

56.8 (32–79)

 

  <60

20 (46.5%)

30 (54.5%)

0.430

  60

23 (53.5%)

25 (45.5%)

 

 Platinum-free interval

  <6 months

4 (9.3%)

3 (5.5%)

0.09

  6–12 months

13 (30.2%)

9 (16.4%)

 

  12 months

22 (51.2%)

42 (76.4%)

 

  Missing

4 (9.3%)

1 (1.8%)

 

 CA 125 (U/ml)

  <100

32 (74.4%)

37 (67.3%)

0.410

  100

8 (18.6%)

14 (25.5%)

 

  Missing

3 (7.0%)

4 (7.3%)

 

 Peritonitis carcinomatosa

  No

39 (90.7%)

48 (87.3%)

0.920

  Yes

3 (7.0%)

4 (7.3%)

 

  Missing

1 (2.3%)

3 (5.5%)

 

 Residual disease at SDS, mm

  0

38 (88.4%)

44 (80.0%)

0.092

  0–10

1 (2.3%)

8 (14.5%)

 

  10

2 (4.7%)

1 (1.8%)

 

  Missing

2 (4.7%)

2 (3.6%)

 

Recurrence at TDS

 Age, median (range), years

61.5 (40–78)

58.6 (33–80)

 

  <60

17 (39.5%)

28 (50.9%)

0.262

  60

26 (60.5%)

27 (49.1%)

 

 CA 125 (U/ml)

  <100

31 (72.1%)

30 (54.5%)

0.040

  100

7 (16.3%)

19 (34.5%)

 

  Missing

5 (11.6%)

6 (10.9%)

 

 Peritonitis carcinomatosa

  No

40 (93.0%)

46 (83.6%)

0.042

  Yes

0 (0%)

5 (9.1%)

 

  Missing

3 (7.0%)

4 (7.3%)

 

 Sites of recurrence

  Peritoneal

28 (65.1%)

48 (87.3%)

0.009

  Extra-peritoneal

15 (34.9%)

7 (12.7%)

 

 Number of recurrence

  Single

24 (55.8%)

17 (30.9%)

0.013

  Multiple

19 (44.2%)

38 (69.1%)

 

The median ages at TDS recurrence (i.e., recurrence after SDS) were 61.5 years (range, 40–78 years) and 58.6 years (range, 33–80 years) in the TDS and non-TDS groups, respectively. The CA125 levels at TDS recurrence (i.e., recurrence after SDS) significantly differed between the two groups (P = 0.040). Peritonitis carcinomatosa was significantly different in the non-TDS patients (P = 0.042). With regard to the sites of recurrence, more patients showed recurrence in the peritoneal cavity in the non-TDS group than in the TDS group (P = 0.009). In the TDS and non-TDS groups, peritoneal recurrence occurred in 28 (65.1%) patients and 48 (87.3%) patients, respectively, while extra-peritoneal recurrence occurred in 15 (34.9%) patients and seven (12.7%) patients, respectively. Among cases of extra-peritoneal recurrence in the TDS group, five (33.3%) cases occurred in the lung; five (33.3%) cases occurred in the brain; four (26.7%) cases occurred in the inguinal lymph nodes; and one (6.7%) case occurred in the axilla. In the non-TDS group, the extra-peritoneal recurrence site was the lung in three (42.9%) cases, the mediastinal space in three (42.9%) cases, and the bone in one (14.3%) case. With regard to the number of recurrence sites, more patients presented with single-site recurrence in the TDS group than in the non-TDS group (P = 0.013). Solitary recurrence occurred in 24 (55.8%) TDS patients and 17 (30.9%) non-TDS patients, and multiple recurrences occurred in 19 (44.2%) TDS patients and 38 (69.1%) non-TDS patients.

Among the 164 patients included in this study, 43 patients underwent TDS. The OS after SDS was significantly better in the TDS group, compared to the non-TDS group (P = 0.001; Fig. 2). The median OS after SDS was 123 months and 42 months in the TDS group and non-TDS group, respectively.
Fig. 2

Kaplan–Meier plot of survival rates after SDS. The survival rate was significantly better in the TDS group than in the non-TDS group (P < 0.001). The median OS after SDS was 123 months in the TDS group and 42 months in the non-TDS group. SDS secondary debulking surgery, TDS tertiary debulking surgery, OS overall survival

Our study included 11 patients who underwent QDS (Table 2). Moreover, two of the 11 QDS patients underwent a fifth debulking surgery. Eight of the 11 patients were alive at the conclusion of the study. The median age of the 11 patients at QDS was 57 years (range, 52–65 years), and the median OS after SDS was 123 months (range, 43–138 months; Table 2).
Table 2

Patients characteristics at the time of quaternary debulking surgery (QDS)

Author

Year

Number

FIGO stage (n)

Agea

Residual disease (n)

Median CA125 (U/ml)

Chemotherapy (n)

Median OS (m)b

Shih et al.

2010

15

I (1)

54.1

0 mm (10)

NA

Yes (9)

34.8, 10.1 (from TDS)c

II (2)

 

>0 mm (5)

 

No (6)

 

III (9)

     

IV (1)

     

Fotopoulou et al.

2013

49

I (6)

57

0 mm (16)

736

Yes (18)

23.05 (from QDS)

II (6)

 

>0 mm (33)

 

No (31)

 

III (33)

     

IV (1)

     

Bacarubasa et al.

2015

20

I (4)

54.3

0 mm (7)

NA

NA

16 (from QDS)

II (5)

 

>0 mm (13)

   

III (11)

     

IV (0)

     

Hirakawa et al.

2017

11

I (0)

57

0 mm (7)

11.2 (6 cases)

Yes (4)

123 (from SDS)

II (1)

 

>0 mm (2)

 

No (7)

 

III (7)

 

Missing (2)

   

IV (3)

     

QDS quaternary debulking surgery, NA data were not available

aThe values are the median age at QDS

bThe values are the median overall survival (OS)

cFor residual disease ≤10 mm, the median OS was 34.8 months; for residual disease >10 mm, the median OS was 10.1 months

Discussion

This study aimed to clarify the current status of SDS and TDS in Japan because few patients have undergone SDS or TDS in Japan and the current status of SDS and TDS is unknown. We found no significant difference in the characteristics between the TDS and non-TDS groups at the primary treatment and at the first recurrence, except for residual disease at PDS. However, a significant difference was noted between the TDS and non-TDS groups in the survival time from the SDS (P < 0.001, Fig. 2). It has been previously demonstrated that SDS shows an advantage in terms of longer OS for highly selected patients [18, 19]; however, the predictors of survival in these patients remain unclear.

It has been reported that ascites (<500 ml) is a prognostic factor and predictor of complete surgery [6, 7]. In this study, it was difficult to collect data concerning ascites because amount of ascites was not measured in most patients. Therefore, we evaluated ascites by using the presence of peritonitis carcinomatosa. In the present study, only three (7.0%) patients and four (7.3%) patients relapsed with carcinomatous peritonitis in the TDS and non-TDS groups at SDS, respectively. It is possible that the patients with ascites were treated largely by chemotherapy instead of SDS, although this study has no data on the non-SDS patients (i.e., patients who did not receive SDS at first recurrence). At the time of TDS (i.e., recurrence after SDS), more patients in the non-TDS group had a recurrence in the peritoneal cavity, compared to the TDS group (P = 0.009). Moreover, more patients showed single-site recurrence in the TDS group than in the non-TDS group (P = 0.013). Many cases of peritoneal cavity recurrence involved wide peritoneal dissemination. These patients may have selected chemotherapy instead of TDS.

In the TDS group, 11 patients underwent QDS and two of these 11 patients underwent a fifth debulking surgery. Ten (90.9%) of the 11 patients with FIGO stage III and IV cancers were in the QDS group. This study included higher ratio of advanced stage cancer patients, compared to other reports on patients with QDS (Table 2). Based on these results, we believe that this is a valuable study to clarify the current status of TDS or additional debulking surgeries.

There are several limitations of this study. One of two main limitations is the retrospective nature of the study. The second main limitation is the small sample size per year and the small number of institutions. Among the 164 patients over 14 years, only approximately 12 patients underwent SDS per year across 20 institutions. We assumed that very few Japanese patients were treated with SDS. Therefore, we collected data from many hospitals in Japan. Despite the smaller sample size per institution, this study provides valuable data concerning TDS and QDS.

A third limitation is the potential for selection bias, such as similar tumor sizes and number of relapse sites. This bias might influence the presence of residual tumor after debulking surgery and/or the survival time. In future studies, selection bias in evaluating the efficacy of SDS and TDS needs to be overcome. We could not rule out the possibility that only highly selected patients were operated on in the present study; nevertheless, this is a valuable study on the current status of SDS and TDS. To the best of our knowledge, this is the first report on TDS and QDS in Japan.

Conclusions

In conclusion, several novel agents such as monoclonal antibodies are being evaluated, although debulking surgery remains an important treatment option for multiple relapses. The present study demonstrated that, at second recurrence, patients who were treated with TDS showed a favorable OS, compared to patients treated with chemotherapy or best supportive care. Further reports of patients treated with SDS or additional debulking surgery need to be accumulated to evaluate treatment results and confirm our findings.

Abbreviations

OS: 

Overall survival

QDS: 

Quaternary debulking surgery

SDS: 

Secondary debulking surgery

TDS: 

Tertiary debulking surgery

Declarations

Acknowledgements

Not applicable

Funding

This study was not funded by an outside source.

Availability of data and materials

The authors respect the patients’ right to privacy. We presented all important information in this published article. Please contact the corresponding author if the data are needed.

Authors’ contributions

TH, KI, and KN designed this protocol. TH, TM, YI, YK, SM, SS, HN, KT, TT, AA, KK, HT, UT, TM, KI, MS, HM, FS, KY, and MK collected the data. TH and HS analyzed the data. TH wrote this manuscript. All authors read and approved the final manuscript.

Ethics approval and consent to participate

In this retrospective study, clinical data were anonymized and this study was approved by the Institutional Review Board of every hospital.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Kansai Clinical Oncology Group (KCOG)
(2)
Department of Obstetrics and Gynecology, Faculty of Medicine, Oita University
(3)
Department of Obstetrics and Gynecology, Faculty of Medicine, University of Tsukuba
(4)
Department of Obstetrics and Gynecology, Nara Prefecture General Medical Center
(5)
Division of Gynecology, Shizuoka Cancer Center Hospital
(6)
Department of Obstetrics and Gynecology, Gifu University
(7)
Department of Obstetrics and Gynecology, Tohoku University School of Medicine
(8)
Department of Obstetrics and Gynecology, Tokyo Women׳s Medical University Medical Center East
(9)
Department of Gynecologic Oncology, Shikoku Cancer Center
(10)
Department of Obstetrics and Gynecology, Kansai Rosai Hospital
(11)
Department of Obstetrics and Gynecology, Nagoya City University Graduate School of Medical Sciences
(12)
Department of Obstetrics and Gynecology, Kurume University School of Medicine
(13)
Department of Obstetrics and Gynecology, Hyogo College of Medicine
(14)
Department of Obstetrics and Gynecology, Kochi Medical School
(15)
Department of Obstetrics and Gynecology, Kyoto Prefectural University of Medicine
(16)
Department of Obstetrics and Gynecology, Nara Medical University
(17)
Department of Obstetrics and Gynecology, Jikei University School of Medicine
(18)
Department of Obstetrics and Gynecology, Jichi Medical University
(19)
Department of Obstetrics and Gynecology, Faculty of Life Science, Kumamoto University
(20)
Department of Obstetrics and Gynecology, Mie University School of Medicine
(21)
Department of Obstetrics and Gynecology, Nagasaki University

References

  1. Bristow RE, Puri I, Chi DS. Cytoreductive surgery for recurrent ovarian cancer: a meta-analysis. Gynecol Oncol. 2009;112:265–74.View ArticlePubMedGoogle Scholar
  2. Nasu K, Kai K, Hirakawa T, Nishida M, Matsumoto H, Kawano Y, et al. Retrospective analysis of outcomes of secondary debulking surgery for recurrent epithelial ovarian cancer with favorable prognostic factors. J Obstet Gynaecol Res. 2014;40:791–6.View ArticlePubMedGoogle Scholar
  3. Laas E, Luyckx M, De Cuypere M, Selle F, Daraï E, Querleu D, et al. Secondary complete cytoreduction in recurrent ovarian cancer: benefit of optimal patient selection using scoring system. Int J Gynecol Cancer. 2014;24:238–46.View ArticlePubMedGoogle Scholar
  4. Zang RY, Li ZT, Tang J, Cheng X, Cai SM, Zhang ZY, et al. Secondary cytoreductive surgery for patients with relapsed epithelial ovarian carcinoma: who benefits? Cancer. 2004;100:1152–61.View ArticlePubMedGoogle Scholar
  5. Onda T, Yoshikawa H, Yasugi T, Yamada M, Matsumoto K, Taketani Y, et al. Secondary cytoreductive surgery for recurrent epithelial ovarian carcinoma: proposal for patients selection. Br J Cancer. 2005;92:1026–32.View ArticlePubMedPubMed CentralGoogle Scholar
  6. Harter P, du Bois A, Hahmann M, Hasenburg A, Burges A, Loibl S, Arbeitsgemeinschaft Gynaekologische Onkologie Ovarian Committee, AGO Ovarian Cancer Study Group, et al. Surgery in recurrent ovarian cancer: the Arbeitsgemeinschaft Gynaekologische Onkologie (AGO) DESKTOP OVAR trial. Ann Surg Oncol. 2006;13:1702–10.View ArticlePubMedGoogle Scholar
  7. Harter P, Hahmann M, Lueck HJ, Poelcher M, Wimberger P, Ortmann O, et al. Surgery for recurrent ovarian cancer: role of peritoneal carcinomatosis: exploratory analysis of the DESKTOP I trial about risk factors, surgical implications, and prognostic value of peritoneal carcinomatosis. Ann Surg Oncol. 2009;16:1324–30.View ArticlePubMedGoogle Scholar
  8. Harter P, Sehouli J, Reuss A, Hasenburg A, Scambia G, Cibula D, et al. Prospective validation study of a predictive score for operability of recurrent ovarian cancer: the Multicenter Intergroup Study DESKTOP II. A project of the AGO Kommission OVAR, AGO Study Group, NOGGO, AGO-Austria, and MITO. Int J Gynecological cancer. 2011;21:289–95.View ArticleGoogle Scholar
  9. Dogan NU, Schneider A, Chiantera V, Dogan S, Dursun P. Tertiary cytoreduction in the setting of recurrent ovarian cancer (Review). Oncol Lett. 2013;6:642–7.PubMedPubMed CentralGoogle Scholar
  10. Tang J, Liu DL, Shu S, Tian WJ, Liu Y, Zang RY. Outcomes and patterns of secondary relapse in platinum-sensitive ovarian cancer: implications for tertiary cytoreductive surgery. Eur J Surg Oncol. 2013;39:786–91.View ArticlePubMedGoogle Scholar
  11. Hızlı D, Boran N, Yılmaz S, Turan T, Altınbaş SK, Celik B, et al. Best predictors of survival outcome after tertiary cytoreduction in patients with recurrent platinum-sensitive epithelial ovarian cancer. Eur J Obstet Gynecol Reprod Biol. 2012;163:71–5.View ArticlePubMedGoogle Scholar
  12. Shih KK, Chi DS, Barakat RR, Leitao Jr MM. Tertiary cytoreduction in patients with recurrent epithelial ovarian, fallopian tube, or primary peritoneal cancer: an updated series. Gynecol Oncol. 2010;117:330–5.View ArticlePubMedGoogle Scholar
  13. Gultekin M, Velipaşaoğlu M, Aksan G, Dursun P, Dogan NU, Yuce K, et al. A third evaluation of tertiary cytoreduction. J Surg Oncol. 2008;98:530–4.View ArticlePubMedGoogle Scholar
  14. Shih KK, Chi DS, Barakat RR, Leitao Jr MM, et al. Beyond tertiary cytoreduction in patients with recurrent epithelial ovarian, fallopian tube, or primary peritoneal cancer. Gynecol Oncol. 2010;116:364–9.View ArticlePubMedGoogle Scholar
  15. Bacalbaşa N, Balescu I, Dima S, Brasoveanu V, Popescu I. The role of quaternary cytoreduction in recurrent epithelial ovarian cancer: a single-center experience. Anticancer Res. 2015;35:3519–23.PubMedGoogle Scholar
  16. Fotopoulou C, Savvatis K, Kosian P, Braicu IE, Papanikolaou G, Pietzner K, et al. Quaternary cytoreductive surgery in ovarian cancer: does surgical effort still matter? Br J Cancer. 2013;108:32–8.View ArticlePubMedPubMed CentralGoogle Scholar
  17. Shih KK, Chi DS. Maximal cytoreductive effort in epithelial ovarian cancer surgery. J Gynecol Oncol. 2010;21:75–80.View ArticlePubMedPubMed CentralGoogle Scholar
  18. da Costa AA, Valadares CV, Mantoan H, Saito A, Salvadori MM, Guimarães AP, et al. The value of secondary cytoreductive surgery in recurrent ovarian cancer and application of a prognostic score. Int J Gynecol Cancer. 2016;26:449–55.PubMedGoogle Scholar
  19. Chuang CM, Chou YJ, Yen MS, Chao KC, Twu NF, Wu HH, et al. The role of secondary cytoreductive surgery in patients with recurrent epithelial ovarian, tubal, and peritoneal cancers: a comparative effectiveness analysis. Oncologist. 2012;17:847–55.View ArticlePubMedPubMed CentralGoogle Scholar

Copyright

© The Author(s). 2017

Advertisement