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Meta-Analysis
. 2011 Oct 5;2011(10):CD003175.
doi: 10.1002/14651858.CD003175.pub2.

Adjuvant chemotherapy for endometrial cancer after hysterectomy

Nick Johnson  1 , Andrew Bryant, Tracie Miles, Thomas Hogberg, Paul Cornes
Affiliations
Meta-Analysis

Adjuvant chemotherapy for endometrial cancer after hysterectomy

Nick Johnson et al. Cochrane Database Syst Rev. .

Abstract

Background: Endometrial adenocarcinoma (womb cancer) is a malignant growth of the lining (endometrium) of the womb (uterus). It is distinct from sarcomas (tumours of the uterine muscle). Survival depends the risk of microscopic metastases after surgery. Adjuvant (postoperative) chemotherapy improves survival from some other adenocarcinomas, and there is evidence that endometrial cancer is sensitive to cytotoxic therapy. This systematic review examines the effect of chemotherapy on survival after hysterectomy for endometrial cancer.

Objectives: To assess efficacy of adjuvant (postoperative) chemotherapy for endometrial cancer.

Search strategy: We searched the Cochrane Central Register of Controlled Trials (CENTRAL, The Cochrane Library 2010, Issue 3), MEDLINE and EMBASE up to August 2010, registers of clinical trials, abstracts of scientific meetings, reference lists of included studies and contacted experts in the field.

Selection criteria: Randomised controlled trials (RCTs) comparing adjuvant chemotherapy with any other adjuvant treatment or no other treatment.

Data collection and analysis: We used a random-effects meta-analysis to assess hazard ratios (HR) for overall and progression-free survival and risk ratios (RR) to compare death rates and site of initial relapse.

Main results: Five RCTs compared no additional treatment with additional chemotherapy after hysterectomy and radiotherapy. Four trials compared platinum based combination chemotherapy directly with radiotherapy. Indiscriminate pooling of survival data from 2197 women shows a significant overall survival advantage from adjuvant chemotherapy (RR (95% CI) = 0.88 (0.79 to 0.99)). Sensitivity analysis focused on trials of modern platinum based chemotherapy regimens and found the relative risk of death to be 0.85 ((0.76 to 0.96); number needed to treat for an additional beneficial outcome (NNT) = 25; absolute risk reduction = 4% (1% to 8%)). The HR for overall survival is 0.74 (0.64 to 0.89), significantly favouring the addition of postoperative platinum based chemotherapy. The HR for progression-free survival is 0.75 (0.64 to 0.89). This means that chemotherapy reduces the risk of being dead at any censorship by a quarter. Chemotherapy reduces the risk of developing the first recurrence outside the pelvis (RR = 0.79 (0.68 to 0.92), 5% absolute risk reduction; NNT = 20). The analysis of pelvic recurrence rates is underpowered but the trend suggests that chemotherapy may be less effective than radiotherapy in a direct comparison (RR = 1.28 (0.97 to 1.68)) but it may have added value when used with radiotherapy (RR = 0.48 (0.20 to 1.18)).

Authors' conclusions: Postoperative platinum based chemotherapy is associated with a small benefit in progression-free survival and overall survival irrespective of radiotherapy treatment. It reduces the risk of developing a metastasis, could be an alternative to radiotherapy and has added value when used with radiotherapy.

PubMed Disclaimer

Conflict of interest statement

Nck Johnson, Andrew Bryant and Tracie Miles have no conflicts of interest.

Thomas Hogberg has participated in advisory boards for Bristol Myers Squibb and Bayer Schering Pharma

Figures

1
1
The QUOROM flow diagram
2
2
Forest plot from all trials of the hazard ratio for death from any cause (representing overall survival).
3
3
Forest plot from all the trials of the hazard ratios for death or recurrence (representing progression‐free survival).
4
4
Indiscriminate forest plot for overall survival (risk of death 5 years after randomisation) from all trials of chemotherapy versus any other arm.
5
5
Forest plot of overall survival excluding mixed tumours (carcinosarcomas)
6
6
Forest plot showing overall survival (risk of death) restricted to trials of high dose chemotherapy.
7
7
Forest plot comparing the risk of developing the first metastasis outside the pelvis
8
8
Forest plot comparing the risk of an recurrence initially seen in the pelvis with chemotherapy or radiotherapy.
9
9
Forest plot examining the risk of a metastasis at any site with chemotherapy compared to radiotherapy.
10
10
Forest plot comparing the risk of a recurrence after surgery and radiotherapy at any site with chemotherapy compared to no adjuvant treatment ).
1.1
1.1. Analysis
Comparison 1 Comparing survival curves (indiscriminate combination of all RCT hazard ratios), Outcome 1 Death from any cause (HR).
1.2
1.2. Analysis
Comparison 1 Comparing survival curves (indiscriminate combination of all RCT hazard ratios), Outcome 2 Death or recurrence (HR).
2.1
2.1. Analysis
Comparison 2 Overall survival 5 years after randomisation (risk of death), all trials, Outcome 1 Risk of death; Chemotherapy versus any other arm (RR).
2.2
2.2. Analysis
Comparison 2 Overall survival 5 years after randomisation (risk of death), all trials, Outcome 2 Risk difference for death at 5 years for all trials.
2.3
2.3. Analysis
Comparison 2 Overall survival 5 years after randomisation (risk of death), all trials, Outcome 3 Restricted to trials of conventional chemotherapy (RR).
2.4
2.4. Analysis
Comparison 2 Overall survival 5 years after randomisation (risk of death), all trials, Outcome 4 Risk difference restricted to trials of conventional chemotherapy.
2.5
2.5. Analysis
Comparison 2 Overall survival 5 years after randomisation (risk of death), all trials, Outcome 5 Analysis excluding unconventional radiotherapy regimens (RR).
3.1
3.1. Analysis
Comparison 3 Separating the trials; Chemotherapy versus radiotherapy, Outcome 1 Death from any cause; Chemotherapy versus radiotherapy (HR).
3.2
3.2. Analysis
Comparison 3 Separating the trials; Chemotherapy versus radiotherapy, Outcome 2 Death or recurrence; Chemotherapy versus radiotherapy (HR).
3.3
3.3. Analysis
Comparison 3 Separating the trials; Chemotherapy versus radiotherapy, Outcome 3 Overall 5 year survival; Chemotherapy versus radiotherapy (RR).
4.1
4.1. Analysis
Comparison 4 Separating the trials; Chemotherapy versus no additional treatment; all women receiving surgery and radiotherapy, Outcome 1 Death from any cause; Chemotherapy versus no additional treatment (HR).
4.2
4.2. Analysis
Comparison 4 Separating the trials; Chemotherapy versus no additional treatment; all women receiving surgery and radiotherapy, Outcome 2 Death or recurrence; Chemotherapy versus no additional treatment (HR).
4.3
4.3. Analysis
Comparison 4 Separating the trials; Chemotherapy versus no additional treatment; all women receiving surgery and radiotherapy, Outcome 3 Overall 5 year survival; Chemotherapy versus no additional treatment (RR).
5.1
5.1. Analysis
Comparison 5 Sensitivity analysis, Outcome 1 Death from any cause (HR) excluding mixed tumours (carcinosarcomas).
5.2
5.2. Analysis
Comparison 5 Sensitivity analysis, Outcome 2 Overall 5 year survival (risk of death) excluding mixed tumours (carcinosarcomas) (RR).
5.3
5.3. Analysis
Comparison 5 Sensitivity analysis, Outcome 3 Overall 5 year survival (risk of death) excluding mixed tumours and trials of unconventional chemotherapy (RR).
6.1
6.1. Analysis
Comparison 6 Site of first recurrence, Outcome 1 Distant (extrapelvic) recurrence (RR; all trials).
6.2
6.2. Analysis
Comparison 6 Site of first recurrence, Outcome 2 Distant (extrapelvic) recurrence; (Risk difference; all trials).
6.3
6.3. Analysis
Comparison 6 Site of first recurrence, Outcome 3 Distant (extrapelvic) recurrence excluding mixed tumours (RR; all trials).
6.4
6.4. Analysis
Comparison 6 Site of first recurrence, Outcome 4 Pelvic recurrence (chemotherapy v no treatment) (RR).
6.5
6.5. Analysis
Comparison 6 Site of first recurrence, Outcome 5 Pelvic recurrence (chemotherapy v radiotherapy) (RR).
6.6
6.6. Analysis
Comparison 6 Site of first recurrence, Outcome 6 Any recurrence (chemotherapy v no adjuvant treatment) (RR).
6.7
6.7. Analysis
Comparison 6 Site of first recurrence, Outcome 7 Any recurrence (chemotherapy v radiotherapy) (RR).
7.1
7.1. Analysis
Comparison 7 Subgroup analysis of NON‐endometriod cancer (clear and serous), Outcome 1 Death from any cause (HR) for subgroup serous/clear cell.
7.2
7.2. Analysis
Comparison 7 Subgroup analysis of NON‐endometriod cancer (clear and serous), Outcome 2 Death or recurrence (HR) for subgroup serous/clear cell cancer.
11
11
Treatment hazard ratio from GOG 122 with 95% CI by prognostic group and end point. (A) Progression‐free survival; (B) overall survival. AP, doxorubicin and cisplatin; WAI, whole‐abdominal irradiation; HR, hazard ratio; Relative Hazard, treatment hazard ratio estimate; Var[In(HR)], variance of the log treatment hazard ratio estimate.
See this image and copyright information in PMC

Update of

References

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EORTC 55991 {unpublished data only}
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GICOG {published data only}
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GOG 122 {published and unpublished data}
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    1. Randall ME, Brunetto G, Muss H, Mannel RS, Spirtos N, Jeffrey F, Thigpen JT, Benda J. Whole abdominal radiotherapy versus combination doxorubicin‐cisplatin chemotherapy in advanced endometrial carcinoma: A randomized phase III trial of the Gynecologic Oncology Group. Proceedings of the American Society of Clinical Oncology. 2003; Vol. 22:2. Abstract 3.
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GOG 150 {published data only}
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    1. Wolfson AH, Brady MF, Rocereto T, Mannel RS, Lee YC, Futoran RJ, et al. A gynecologic oncology group randomized phase III trial of whole abdominal irradiation (WAI) vs. cisplatin‐ifosfamide and mesna (CIM) as post‐surgical therapy in stage I‐IV carcinosarcoma (CS) of the uterus. Gynecologic Oncology 2007;107(2):177‐85. - PMC - PubMed
GOG 34 {published data only}
    1. Morrow CP, Bundy B, Creasman W, Homesley H. A randomized study of adriamycin adjuvant chemotherapy for patients with high‐risk stage I and II (occult) endometrial carcinoma: a GOG study. Proceedings, International Gynecological Cancer Society: Amsterdam, the Netherlands. 1987:87.
    1. Morrow CP, Bundy BN, Homesley HD, Creasman WT, Hornback NB, Kurman R, et al. Doxorubicin as an adjuvant following surgery and radiation therapy in patients with high‐risk endometrial carcinoma, stage I and occult stage II: A Gynecologic Oncology Group Study. Gynecologic Oncology 1990;36(2):166‐71. - PubMed
J GOG 2033 {published data only}
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    1. Susumu N, Sagae S, Udagawa Y, Niwa K, Kuramoto H, Satoh S, et al. Randomized phase III trial of pelvic radiotherapy versus cisplatin‐based combined chemotherapy in patients with intermediate‐ and high‐risk endometrial cancer: a Japanese Gynecologic Oncology Group study. Gynecologic Oncology 2008;108(1):226‐33. - PubMed
Kuoppala 2008 {published data only}
    1. Kuoppala T, Maenpaa J, Tomas E, Puistola U, Salmi T, Grenman S, et al. Surgically staged high‐risk endometrial cancer: randomized study of adjuvant radiotherapy alone vs. sequential chemo‐radiotherapy. Gynecol Oncol 2008;110(2):190‐5. - PubMed
MaNGO {unpublished data only}
    1. Hogberg T, Signorelli M, Freire de Oliveira C, Fossati R, Lissoni AA, Sorbe B, et al. Sequential adjuvant chemotherapy and radiotherapy in endometrial cancer – Results from two randomised studies. European Journal of Cancer 2010;46(13):2422‐31. - PMC - PubMed
NSGO {published and unpublished data}
    1. Hogberg T. Case #4 Endometrial CarcinomaStage IIIC. http://www.primeoncology.org/Files/Doc/SLIDES/EPGM06282008/Case4.pdf. 2008.
    1. Hogberg T, Rosenberg P, Kristensen G, Oliveira CF, Pont Christensen R, Sorbe B, et al. A randomized phase‐III study on adjuvant treatment with radiation (RT) ± chemotherapy (CT) in early‐stage high‐risk endometrial cancer. Journal of Clinical Oncology, 2007 ASCO Annual Meeting Proceedings Abstracts of the 43rd Annual Meeting of the American Society of Clinical Oncology; 1‐5 June 2007; Chicago, Illinois. www.asco.org, 2007; Vol. Part I.2007;25 (18 Suppl):Abstract 5503.
    1. Hogberg T, Signorelli M, Freire de Oliveira C, Fossati R, Lissoni AA, Sorbe B, et al. Sequential adjuvant chemotherapy and radiotherapy in endometrial cancer – Results from two randomised studies. European Journal of Cancer 2010;46(13):2422‐31. - PMC - PubMed
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NSGO, MaNGO and EORTC {published data only}
    1. Hogberg T, Signorelli M, Freire de Oliveira C, Fossati R, Lissoni AA, Sorbe B, et al. Sequential adjuvant chemotherapy and radiotherapy in endometrial cancer – Results from two randomised studies. European Journal of Cancer 2010; Vol. 46, issue 13:2422‐31. - PMC - PubMed
NSGO & EORTC {unpublished data only}
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References to studies excluded from this review

Aapro 2003 {published data only}
    1. Aapro MS, Wijk FH, Bolis G, Chevallier B, Burg MEL, Poveda A et al on behalf of the EORTC‐GCCG. Doxorubicin versus doxorubicin and cisplatin in endometrial carcinoma: definitive results of a randomised study (55872) by the EORTC‐GCCG. Annals of Oncology 2003;14:441‐8. - PubMed
Bruner 2007 {published data only}
    1. Bruner DW, Barsevick A, Tian C, Randall M, Mannel R, Cohn DE, et al. Randomized trial results of quality of life comparing whole abdominal irradiation and combination chemotherapy in advanced endometrial carcinoma: A gynecologic oncology group study. Quality of Life Research 2007;16(1):89‐100. - PubMed
Brunetto 2000 {published data only}
    1. Brunetto V, Kilgore L, Soper J, McGehee R, Olt G, Lentz SS, et al. A phase III trial of ifosfamide alone or in combination with cisplatin in the treatment of advanced, persistent or recurrent carcinosarcoma of the uterus: a Gynecologic Oncology Group study. Gynecologic Oncology 2000;98;68(1):137, Abstract 266.
Chauvergne 2008 {published data only}
    1. Chauvergne J, Cappelaere P, Durand M, Brunet R, Hoerni B. Chemotherapy of cervico‐uterin carcinoma by two associations:cisplatine or detorubicine. Results of a comparative controlled trial. Bulletin du cancer 2008;81;68(2):363.
Cohen 1984 {published data only}
    1. Cohen CJ, Bruckner HW, Deppe G, Blessing JA, Homesley H, Lee JH, et al. Multidrug treatment of advanced and recurrent endometrial carcinoma: a Gynecologic Oncology Group study. Obstetrics and Gynecology 1984;63(5):719‐26. - PubMed
Deng 2000 {published data only}
    1. Deng XH, Duan W, Li BZ. Estramustine phosphate in the treatment of endometrium carcinoma. Chinese Journal of Cancer Research 2000;12(1):58‐63.
Edmonson 1987 {published data only}
    1. Edmonson JH, Krook JE, Hilton JF, Malkasian GD, Everson LK, Jefferies JA, et al. Randomized phase II studies of cisplatin and a combination of cyclophosphamide‐doxorubicin‐cisplatin (CAP) in patients with progestin‐refractory advanced endometrial carcinoma. Gynecologic Oncology 1887;28(1):20‐4. - PubMed
Fleming 2004a {published data only}
    1. Fleming GF, Brunetto VL, Cella D, Look KY, Reid GC, Munkarah AR, et al. Phase III trial of Doxorubicin Plus Cisplatin With or Without Paclitaxel Plus Filgrastim in Advanced Endometrial Carcinoma: A Gynecologic Oncology Group Study. Journal of Clinical Oncology 2004;22(11):2159‐66. - PubMed
Fleming 2004b {published data only}
    1. Fleming GF, Filiaci VL, Bentley RC, Herzog T, Vaccarello L, Gallion H. Phase III randomised trial of doxorubicin + cisplatin versus doxorubicin + 24‐h paclitaxel + filgrastim in ednometrial carcinoma: a Gynecologic Oncology Group study. Annals of Oncology 2004;15:1173‐8. - PubMed
Fujimura 2000 {published data only}
    1. Fujimura H, Kikkawa F, Oguchi H, Nakashima N, Mizutani S. Adjuvant chemotherapy including cisplatin in endometrial carcinoma. Gynecologic & Obstetric Investigation 2000;50(2):127‐32. - PubMed
Gallion 2003 {published data only}
    1. Gallion HH, Brunetto VL, Cibull M, Lentz SS, Reid G, Soper JT, et al. Randomized phase III trial of standard timed doxorubicin plus cisplatin versus circadian timed doxorubicin plus cisplatin in stage III and IV or recurrence endometrial carcinaoma: a Gynecologic Oncology Group study. Journal of Clinical Oncology 2003;21(20):3808‐13. - PubMed
GCSF {published data only}
    1. Fleming GF, Brunetto VL, Cella D, Look KY, Reid GC, Munkarah AR, et al. Phase III trial of doxorubicin plus cisplatin with or without paclitaxel plus filgrastim in advanced endometrial carcinoma: a Gynecologic Oncology Group Study. Journal of Clinical Oncology 2004;22(11):2159‐66. - PubMed
GOG 107 {published data only}
    1. Thigpen JT, Brady MF, Homesley HD, Malfetano J, DuBeshter B, Burger RA, et al. Phase III trial of doxorubicin with or without cisplatin in advanced endometrial carcinoma: a gynecologic oncology group study. Journal of Clinical Oncology 2004;22(19):3902‐8. - PubMed
GOG 156 {unpublished data only}
    1. GOG Protocol FAQ. http://www.gog.org/protocolfaq.html.
GOG 161 {published data only}
    1. Homesley HD, Filiaci V, Markman M, Bitterman P, Eaton L, Kilgore LC, et al. Phase III trial of ifosfamide with or without paclitaxel in advanced uterine carcinosarcoma: a Gynecologic Oncology Group Study. Journal of Clinical Oncology 2007;25(5):526‐31. - PubMed
GOG 194 {unpublished data only}
    1. GOG Protocol FAQ. http://www.gog.org/protocolfaq.html.
    1. Greven K, Winter K, Underhill K, Fontenesci J, Cooper J, Burke T, et al. Preliminary analysis of RTOG 9708: Adjuvant postoperative radiotherapy combined with cisplatin/paclitaxel chemotherapy after surgery for patients with high‐risk endometrial cancer. International Journal of Radiation Oncology, Biology, Physics. 2004;59(1):168‐73. - PubMed
Horton 1978 {published data only}
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Long 1995 {published data only}
    1. Long HJ, Nelimark RA, Cha SS. Comparison of methotrexate, vinblastine, doxorubicin and cisplatin (MVAC) vs doxorubicin and cisplatin (AC) in advanced endometrial carcinoma (Meeting abstract). Proceedings of the Annual Meeting of the American Society of Clinical Oncology. 1995; Vol. 14:282, Abstract 797.
Omura {published data only}
    1. Omura GA, Blessing JA, Major F, Silverberg S. A randomized trial of adriamycin versus no adjuvant chemotherapy in stage I and II uterine sarcomas. Proceedings of the American Society of Clinical Oncology. 1985; Vol. 83 (2):149, Abstract C‐580.
Pawinski 1999 {published data only}
    1. Pawinski A, Tumolo S, Hoesel G, Cervantes A, Oosterom AT, Hoctin Boes G, et al. Cyclophosphamide or ifosfamide in patients with advanced and/or recurrent endometrial carcinoma: a randomised phaseII study of the EORTC Gynecological Cancer Cooperative Group. European Journal of Obstetrics and Gynecology and Reproductive Biology 1999;86:179‐83. - PubMed
Samuels 2004 {published data only}
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Sutton 2000 {published data only}
    1. Sutton G, Brunetto VL, Kilgore L, Soper JT, McGehee R, Olt G, et al. A phase III trial of ifosfamide with or without cisplatin in carcinosarcoma of the uterus: A Gynecologic Oncology Group Study. Gynecologic Oncology 2000;79(2):147‐53. - PubMed
Thigpen 1994 {published data only}
    1. Thigpen JT, Blessing JA, DiSaia PJ, Yordan E, Carson LF, Evers C. A randomized comparison of doxorubicin alone versus doxorubicin plus cyclophosphamide in the management of advanced or recurrent endometrial carcinoma: A Gynecologic Oncology Group study. Journal of Clinical Oncology 1994;12(7):1408‐14. - PubMed
Thigpen 2004 {published data only}
    1. Thigpen JT, Brady MF, Homesley HD, Malfetano J, DuBeshter B, Burger RA, et al. Phase III trial of doxorubicin with or without cisplatin in advanced endometrial carcinoma: A Gynecologic Oncology Group Study (GOG). Journal of Clinical Oncology 2004;22(19):3902‐8. - PubMed

References to ongoing studies

GOG 249 {unpublished data only}
    1. Pelvic Radiation Therapy or Vaginal Implant Radiation Therapy, Paclitaxel, and Carboplatin in Treating Patients With High‐Risk Stage I or Stage II Endometrial Cancer. http://clinicaltrials.gov/ct2/show/NCT00807768.
    1. http://www.cancer.gov/clinicaltrials/ft‐GOG‐0249.
GOG 258 {unpublished data only}
    1. GOG 0258 (RTOG 1073 Endorsed). A Randomized Phase III Trial of Cisplatin and Tumor Volume Directed Irradiation Followed by Carboplatin andPaclitaxel vs. Carboplatin and Paclitaxel for Optimally Debulked, Advanced Endometrial Carcinoma. http://www.rtog.org/LinkClick.aspx?fileticket=7aqw‐i1bTZ8%3D&tabid=331.
Hogberg {unpublished data only}
    1. Thomas Hogberg, MMC‐08‐03‐060, NCT01041027. Is the sequential combination of RT after four courses of CT better then 2 additional courses of CT in the adjuvant therapy of high‐risk endometrial cancer. A Phase III intergroup trial on adjuvant therapy in radically operated endometrial cancer patients with high risk for micro‐metastatic disease: 4 courses of adjuvant CT (CT) followed by radiation therapy (RT) versus 2 more courses of CT.
PORTEC 3 {unpublished data only}
    1. CKTO‐2006‐04ISRCTN14387080, CKTO‐PORTEC‐3, EU‐20664, NCT00411138. Phase III Randomized Study of Concurrent Chemoradiotherapy Followed By Adjuvant Chemotherapy Versus Pelvic Radiotherapy Alone in Patients With High‐Risk Stage IB‐III Endometrial Carcinoma Alternate Title. Chemotherapy and Radiation Therapy Compared With Radiation Therapy Alone in Treating Patients With High‐Risk Stage I, Stage II, or Stage III Endometrial Cancer.

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