Recurrence, death, and secondary malignancy after ovarian conservation for young women with early-stage low-grade endometrial cancer

Koji Matsuo; James C. Cripe; Katherine C. Kurnit; Michiko Kaneda; Audrey S. Garneau; Gretchen E. Glaser; Aaron Nizam; Rachel M. Schillinger; Michelle L. Kuznicki; Akira Yabuno; Shiori Yanai; Denise M. Garofalo; Jiro Suzuki; Jessica D. St. Laurent; Ting Tai Yen; Annie Y. Liu; Masako Shida; Mamoru Kakuda; Tetsuro Oishi; Shin Nishio; Jenna Z. Marcus; Sosuke Adachi; Tetsuji Kurokawa; Malcolm S. Ross; Max P. Horowitz; Marian S. Johnson; Min K. Kim; Alexander Melamed; Karime K. Machado; Kosuke Yoshihara; Yoshio Yoshida; Takayuki Enomoto; Kimio Ushijima; Shinya Satoh; Yutaka Ueda; Mikio Mikami; Bobbie J. Rimel; Rebecca L. Stone; Whitfield B. Growdon; Aikou Okamoto; Saketh R. Guntupalli; Kosei Hasegawa; Mian M.K. Shahzad; Dwight D. Im; Marina Frimer; Bobbie S. Gostout; Frederick R. Ueland; Shoji Nagao; Pamela T. Soliman; Premal H. Thaker; Jason D. Wright; Lynda D. Roman

doi:10.1016/j.ygyno.2019.08.007

Recurrence, death, and secondary malignancy after ovarian conservation for young women with early-stage low-grade endometrial cancer

Koji Matsuo, James C. Cripe, Katherine C. Kurnit, Michiko Kaneda, Audrey S. Garneau, Gretchen E. Glaser, Aaron Nizam, Rachel M. Schillinger, Michelle L. Kuznicki, Akira Yabuno, Shiori Yanai, Denise M. Garofalo, Jiro Suzuki, Jessica D. St. Laurent, Ting Tai Yen, Annie Y. Liu, Masako Shida, Mamoru Kakuda, Tetsuro Oishi, Shin NishioJenna Z. Marcus, Sosuke Adachi, Tetsuji Kurokawa, Malcolm S. Ross, Max P. Horowitz, Marian S. Johnson, Min K. Kim, Alexander Melamed, Karime K. Machado, Kosuke Yoshihara, Yoshio Yoshida, Takayuki Enomoto, Kimio Ushijima, Shinya Satoh, Yutaka Ueda, Mikio Mikami, Bobbie J. Rimel, Rebecca L. Stone, Whitfield B. Growdon, Aikou Okamoto, Saketh R. Guntupalli, Kosei Hasegawa, Mian M.K. Shahzad, Dwight D. Im, Marina Frimer, Bobbie S. Gostout, Frederick R. Ueland, Shoji Nagao, Pamela T. Soliman, Premal H. Thaker, Jason D. Wright, Lynda D. Roman

Research output: Contribution to journal › Article › peer-review

18 Scopus citations

Abstract

Objective: To examine the association between ovarian conservation and oncologic outcome in surgically-treated young women with early-stage, low-grade endometrial cancer. Methods: This multicenter retrospective study examined women aged <50 with stage I grade 1–2 endometrioid endometrial cancer who underwent primary surgery with hysterectomy from 2000 to 2014 (US cohort n = 1196, and Japan cohort n = 495). Recurrence patterns, survival, and the presence of a metachronous secondary malignancy were assessed based on ovarian conservation versus oophorectomy. Results: During the study period, the ovarian conservation rate significantly increased in the US cohort from 5.4% to 16.4% (P = 0.020) whereas the rate was unchanged in the Japan cohort (6.3–8.7%, P = 0.787). In the US cohort, ovarian conservation was not associated with disease-free survival (hazard ratio [HR] 0.829, 95% confidence interval [CI] 0.188–3.663, P = 0.805), overall survival (HR not estimated, P = 0.981), or metachronous secondary malignancy (HR 1.787, 95% CI 0.603–5.295, P = 0.295). In the Japan cohort, ovarian conservation was associated with decreased disease-free survival (HR 5.214, 95% CI 1.557–17.464, P = 0.007) and an increased risk of a metachronous secondary malignancy, particularly ovarian cancer (HR 7.119, 95% CI 1.349–37.554, P = 0.021), but was not associated with overall survival (HR not estimated, P = 0.987). Ovarian recurrence or metachronous secondary ovarian cancer occurred after a median time of 5.9 years, and all cases were salvaged. Conclusion: Our study suggests that adoption of ovarian conservation in young women with early-stage low-grade endometrial cancer varies by population. Ovarian conservation for young women with early-stage, low-grade endometrial cancer may be potentially associated with increased risks of ovarian recurrence or metachronous secondary ovarian cancer in certain populations; nevertheless, ovarian conservation did not negatively impact overall survival.

Original language	English
Pages (from-to)	39-50
Number of pages	12
Journal	Gynecologic oncology
Volume	155
Issue number	1
DOIs	https://doi.org/10.1016/j.ygyno.2019.08.007
State	Published - Oct 2019

Keywords

Endometrial cancer
Ovarian conservation
Recurrence
Secondary primary cancer
Survival

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10.1016/j.ygyno.2019.08.007

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Matsuo, K., Cripe, J. C., Kurnit, K. C., Kaneda, M., Garneau, A. S., Glaser, G. E., Nizam, A., Schillinger, R. M., Kuznicki, M. L., Yabuno, A., Yanai, S., Garofalo, D. M., Suzuki, J., St. Laurent, J. D., Yen, T. T., Liu, A. Y., Shida, M., Kakuda, M., Oishi, T., ... Roman, L. D. (2019). Recurrence, death, and secondary malignancy after ovarian conservation for young women with early-stage low-grade endometrial cancer. Gynecologic oncology, 155(1), 39-50. https://doi.org/10.1016/j.ygyno.2019.08.007

@article{c24df4ae4a2147f79677a989b4543223,

title = "Recurrence, death, and secondary malignancy after ovarian conservation for young women with early-stage low-grade endometrial cancer",

abstract = "Objective: To examine the association between ovarian conservation and oncologic outcome in surgically-treated young women with early-stage, low-grade endometrial cancer. Methods: This multicenter retrospective study examined women aged <50 with stage I grade 1–2 endometrioid endometrial cancer who underwent primary surgery with hysterectomy from 2000 to 2014 (US cohort n = 1196, and Japan cohort n = 495). Recurrence patterns, survival, and the presence of a metachronous secondary malignancy were assessed based on ovarian conservation versus oophorectomy. Results: During the study period, the ovarian conservation rate significantly increased in the US cohort from 5.4% to 16.4% (P = 0.020) whereas the rate was unchanged in the Japan cohort (6.3–8.7%, P = 0.787). In the US cohort, ovarian conservation was not associated with disease-free survival (hazard ratio [HR] 0.829, 95% confidence interval [CI] 0.188–3.663, P = 0.805), overall survival (HR not estimated, P = 0.981), or metachronous secondary malignancy (HR 1.787, 95% CI 0.603–5.295, P = 0.295). In the Japan cohort, ovarian conservation was associated with decreased disease-free survival (HR 5.214, 95% CI 1.557–17.464, P = 0.007) and an increased risk of a metachronous secondary malignancy, particularly ovarian cancer (HR 7.119, 95% CI 1.349–37.554, P = 0.021), but was not associated with overall survival (HR not estimated, P = 0.987). Ovarian recurrence or metachronous secondary ovarian cancer occurred after a median time of 5.9 years, and all cases were salvaged. Conclusion: Our study suggests that adoption of ovarian conservation in young women with early-stage low-grade endometrial cancer varies by population. Ovarian conservation for young women with early-stage, low-grade endometrial cancer may be potentially associated with increased risks of ovarian recurrence or metachronous secondary ovarian cancer in certain populations; nevertheless, ovarian conservation did not negatively impact overall survival.",

keywords = "Endometrial cancer, Ovarian conservation, Recurrence, Secondary primary cancer, Survival",

author = "Koji Matsuo and Cripe, {James C.} and Kurnit, {Katherine C.} and Michiko Kaneda and Garneau, {Audrey S.} and Glaser, {Gretchen E.} and Aaron Nizam and Schillinger, {Rachel M.} and Kuznicki, {Michelle L.} and Akira Yabuno and Shiori Yanai and Garofalo, {Denise M.} and Jiro Suzuki and {St. Laurent}, {Jessica D.} and Yen, {Ting Tai} and Liu, {Annie Y.} and Masako Shida and Mamoru Kakuda and Tetsuro Oishi and Shin Nishio and Marcus, {Jenna Z.} and Sosuke Adachi and Tetsuji Kurokawa and Ross, {Malcolm S.} and Horowitz, {Max P.} and Johnson, {Marian S.} and Kim, {Min K.} and Alexander Melamed and Machado, {Karime K.} and Kosuke Yoshihara and Yoshio Yoshida and Takayuki Enomoto and Kimio Ushijima and Shinya Satoh and Yutaka Ueda and Mikio Mikami and Rimel, {Bobbie J.} and Stone, {Rebecca L.} and Growdon, {Whitfield B.} and Aikou Okamoto and Guntupalli, {Saketh R.} and Kosei Hasegawa and Shahzad, {Mian M.K.} and Im, {Dwight D.} and Marina Frimer and Gostout, {Bobbie S.} and Ueland, {Frederick R.} and Shoji Nagao and Soliman, {Pamela T.} and Thaker, {Premal H.} and Wright, {Jason D.} and Roman, {Lynda D.}",

note = "Funding Information: We thank Drs. Yongmei Huang and Brendan H. Grubbs for their scientific inputs for this study. Research grant, Pfizer, Yakult Honsha, OncoThreapy Science, honoraria, Chugai, Daiichi-Sankyo, Ono Pharmaceutical, Eisai, Kyowa Hakko Kirin, and Bayer Yakuhin, advisory board, Merck Sharp and Dohme (K.H.); honorariums, Chugai and Astra Zeneca (T.E.); consultant, Tesaro and Clovis Oncology, research funding, Merck (J.D.W.); honorarium, Chugai, textbook editorial, Springer, and investigator meeting attendance expense, VBL therapeutics (K.M.); consultant, Quantgene (L.D.R.); research grant, Merck and Tesaro, advisory board/consultant, Tesaro, Stryker, Astra Zeneca, Celsion, Abbvie, Iovance, Clovis, Genentech, and speaker bureau, Astra Zeneca, Tesaro, and Merck (P.H.T.). Conceptualization: K.M. J.D.W.; Data curation: K.M. J.C.C. K.C.K. M.K. A.S.G. G.E.G. A.N. R.M.S. M.L.K. A.K. S.Y. D.M.G. J.S. J.D.S.L. T.T.Y. A.Y.L. M.S. M.K. T.O. S.N. J.Z.M. S.A. T.K. M.S.J. M.K.K. K.K.M.; Formal analysis: K.M.; Funding acquisition: K.M. L.D.R.; Investigation: all authors; Methodology: K.M. J.D.W.; Project administration: K.M. P.H.T. P.T.S. S.N. F.R.U. G.E.G. M.F. D.D.I. M.M.K.S. K. H. S.Y. S.R.G. A.O. A.M. R.L.S. B.J.R. M.M. Y.U. S.S. J.Z.M. T.E. Y.Y.; Resources: K.M.; Software: K.M.; Supervision: P.H.T. P.T.S. S.N. F.R.U. B.S.G. M.F. D.D.I. M.M.K.S. K. H. S.Y. S.R.G. A.O. A.M. W.B.G. R.L.S. B.J.R. M.M. Y.U. S.S. J.Z.M. T.E. Y.Y. J.D.W. L.D.R.; Validation: K.M.; Visualization: K.M.; Writing - original draft: K.M.; Writing - review & editing: all authors. Ensign Endowment for Gynecologic Cancer Research (K.M.). Funding Information: Research grant, Pfizer, Yakult Honsha, OncoThreapy Science, honoraria, Chugai, Daiichi-Sankyo, Ono Pharmaceutical, Eisai, Kyowa Hakko Kirin, and Bayer Yakuhin, advisory board, Merck Sharp and Dohme (K.H.); honorariums, Chugai and Astra Zeneca (T.E.); consultant, Tesaro and Clovis Oncology, research funding, Merck (J.D.W.); honorarium, Chugai, textbook editorial, Springer, and investigator meeting attendance expense, VBL therapeutics (K.M.); consultant, Quantgene (L.D.R.); research grant, Merck and Tesaro, advisory board/consultant, Tesaro, Stryker, Astra Zeneca, Celsion, Abbvie, Iovance, Clovis, Genentech, and speaker bureau, Astra Zeneca, Tesaro, and Merck (P.H.T.). Publisher Copyright: {\textcopyright} 2019",

year = "2019",

month = oct,

doi = "10.1016/j.ygyno.2019.08.007",

language = "English",

volume = "155",

pages = "39--50",

journal = "Gynecologic oncology",

issn = "0090-8258",

number = "1",

}

Matsuo, K, Cripe, JC, Kurnit, KC, Kaneda, M, Garneau, AS, Glaser, GE, Nizam, A, Schillinger, RM, Kuznicki, ML, Yabuno, A, Yanai, S, Garofalo, DM, Suzuki, J, St. Laurent, JD, Yen, TT, Liu, AY, Shida, M, Kakuda, M, Oishi, T, Nishio, S, Marcus, JZ, Adachi, S, Kurokawa, T, Ross, MS, Horowitz, MP, Johnson, MS, Kim, MK, Melamed, A, Machado, KK, Yoshihara, K, Yoshida, Y, Enomoto, T, Ushijima, K, Satoh, S, Ueda, Y, Mikami, M, Rimel, BJ, Stone, RL, Growdon, WB, Okamoto, A, Guntupalli, SR, Hasegawa, K, Shahzad, MMK, Im, DD, Frimer, M, Gostout, BS, Ueland, FR, Nagao, S, Soliman, PT, Thaker, PH, Wright, JD & Roman, LD 2019, 'Recurrence, death, and secondary malignancy after ovarian conservation for young women with early-stage low-grade endometrial cancer', Gynecologic oncology, vol. 155, no. 1, pp. 39-50. https://doi.org/10.1016/j.ygyno.2019.08.007

TY - JOUR

T1 - Recurrence, death, and secondary malignancy after ovarian conservation for young women with early-stage low-grade endometrial cancer

AU - Matsuo, Koji

AU - Cripe, James C.

AU - Kurnit, Katherine C.

AU - Kaneda, Michiko

AU - Garneau, Audrey S.

AU - Glaser, Gretchen E.

AU - Nizam, Aaron

AU - Schillinger, Rachel M.

AU - Kuznicki, Michelle L.

AU - Yabuno, Akira

AU - Yanai, Shiori

AU - Garofalo, Denise M.

AU - Suzuki, Jiro

AU - St. Laurent, Jessica D.

AU - Yen, Ting Tai

AU - Liu, Annie Y.

AU - Shida, Masako

AU - Kakuda, Mamoru

AU - Oishi, Tetsuro

AU - Nishio, Shin

AU - Marcus, Jenna Z.

AU - Adachi, Sosuke

AU - Kurokawa, Tetsuji

AU - Ross, Malcolm S.

AU - Horowitz, Max P.

AU - Johnson, Marian S.

AU - Kim, Min K.

AU - Melamed, Alexander

AU - Machado, Karime K.

AU - Yoshihara, Kosuke

AU - Yoshida, Yoshio

AU - Enomoto, Takayuki

AU - Ushijima, Kimio

AU - Satoh, Shinya

AU - Ueda, Yutaka

AU - Mikami, Mikio

AU - Rimel, Bobbie J.

AU - Stone, Rebecca L.

AU - Growdon, Whitfield B.

AU - Okamoto, Aikou

AU - Guntupalli, Saketh R.

AU - Hasegawa, Kosei

AU - Shahzad, Mian M.K.

AU - Im, Dwight D.

AU - Frimer, Marina

AU - Gostout, Bobbie S.

AU - Ueland, Frederick R.

AU - Nagao, Shoji

AU - Soliman, Pamela T.

AU - Thaker, Premal H.

AU - Wright, Jason D.

AU - Roman, Lynda D.

N1 - Funding Information: We thank Drs. Yongmei Huang and Brendan H. Grubbs for their scientific inputs for this study. Research grant, Pfizer, Yakult Honsha, OncoThreapy Science, honoraria, Chugai, Daiichi-Sankyo, Ono Pharmaceutical, Eisai, Kyowa Hakko Kirin, and Bayer Yakuhin, advisory board, Merck Sharp and Dohme (K.H.); honorariums, Chugai and Astra Zeneca (T.E.); consultant, Tesaro and Clovis Oncology, research funding, Merck (J.D.W.); honorarium, Chugai, textbook editorial, Springer, and investigator meeting attendance expense, VBL therapeutics (K.M.); consultant, Quantgene (L.D.R.); research grant, Merck and Tesaro, advisory board/consultant, Tesaro, Stryker, Astra Zeneca, Celsion, Abbvie, Iovance, Clovis, Genentech, and speaker bureau, Astra Zeneca, Tesaro, and Merck (P.H.T.). Conceptualization: K.M. J.D.W.; Data curation: K.M. J.C.C. K.C.K. M.K. A.S.G. G.E.G. A.N. R.M.S. M.L.K. A.K. S.Y. D.M.G. J.S. J.D.S.L. T.T.Y. A.Y.L. M.S. M.K. T.O. S.N. J.Z.M. S.A. T.K. M.S.J. M.K.K. K.K.M.; Formal analysis: K.M.; Funding acquisition: K.M. L.D.R.; Investigation: all authors; Methodology: K.M. J.D.W.; Project administration: K.M. P.H.T. P.T.S. S.N. F.R.U. G.E.G. M.F. D.D.I. M.M.K.S. K. H. S.Y. S.R.G. A.O. A.M. R.L.S. B.J.R. M.M. Y.U. S.S. J.Z.M. T.E. Y.Y.; Resources: K.M.; Software: K.M.; Supervision: P.H.T. P.T.S. S.N. F.R.U. B.S.G. M.F. D.D.I. M.M.K.S. K. H. S.Y. S.R.G. A.O. A.M. W.B.G. R.L.S. B.J.R. M.M. Y.U. S.S. J.Z.M. T.E. Y.Y. J.D.W. L.D.R.; Validation: K.M.; Visualization: K.M.; Writing - original draft: K.M.; Writing - review & editing: all authors. Ensign Endowment for Gynecologic Cancer Research (K.M.). Funding Information: Research grant, Pfizer, Yakult Honsha, OncoThreapy Science, honoraria, Chugai, Daiichi-Sankyo, Ono Pharmaceutical, Eisai, Kyowa Hakko Kirin, and Bayer Yakuhin, advisory board, Merck Sharp and Dohme (K.H.); honorariums, Chugai and Astra Zeneca (T.E.); consultant, Tesaro and Clovis Oncology, research funding, Merck (J.D.W.); honorarium, Chugai, textbook editorial, Springer, and investigator meeting attendance expense, VBL therapeutics (K.M.); consultant, Quantgene (L.D.R.); research grant, Merck and Tesaro, advisory board/consultant, Tesaro, Stryker, Astra Zeneca, Celsion, Abbvie, Iovance, Clovis, Genentech, and speaker bureau, Astra Zeneca, Tesaro, and Merck (P.H.T.). Publisher Copyright: © 2019

PY - 2019/10

Y1 - 2019/10

N2 - Objective: To examine the association between ovarian conservation and oncologic outcome in surgically-treated young women with early-stage, low-grade endometrial cancer. Methods: This multicenter retrospective study examined women aged <50 with stage I grade 1–2 endometrioid endometrial cancer who underwent primary surgery with hysterectomy from 2000 to 2014 (US cohort n = 1196, and Japan cohort n = 495). Recurrence patterns, survival, and the presence of a metachronous secondary malignancy were assessed based on ovarian conservation versus oophorectomy. Results: During the study period, the ovarian conservation rate significantly increased in the US cohort from 5.4% to 16.4% (P = 0.020) whereas the rate was unchanged in the Japan cohort (6.3–8.7%, P = 0.787). In the US cohort, ovarian conservation was not associated with disease-free survival (hazard ratio [HR] 0.829, 95% confidence interval [CI] 0.188–3.663, P = 0.805), overall survival (HR not estimated, P = 0.981), or metachronous secondary malignancy (HR 1.787, 95% CI 0.603–5.295, P = 0.295). In the Japan cohort, ovarian conservation was associated with decreased disease-free survival (HR 5.214, 95% CI 1.557–17.464, P = 0.007) and an increased risk of a metachronous secondary malignancy, particularly ovarian cancer (HR 7.119, 95% CI 1.349–37.554, P = 0.021), but was not associated with overall survival (HR not estimated, P = 0.987). Ovarian recurrence or metachronous secondary ovarian cancer occurred after a median time of 5.9 years, and all cases were salvaged. Conclusion: Our study suggests that adoption of ovarian conservation in young women with early-stage low-grade endometrial cancer varies by population. Ovarian conservation for young women with early-stage, low-grade endometrial cancer may be potentially associated with increased risks of ovarian recurrence or metachronous secondary ovarian cancer in certain populations; nevertheless, ovarian conservation did not negatively impact overall survival.

AB - Objective: To examine the association between ovarian conservation and oncologic outcome in surgically-treated young women with early-stage, low-grade endometrial cancer. Methods: This multicenter retrospective study examined women aged <50 with stage I grade 1–2 endometrioid endometrial cancer who underwent primary surgery with hysterectomy from 2000 to 2014 (US cohort n = 1196, and Japan cohort n = 495). Recurrence patterns, survival, and the presence of a metachronous secondary malignancy were assessed based on ovarian conservation versus oophorectomy. Results: During the study period, the ovarian conservation rate significantly increased in the US cohort from 5.4% to 16.4% (P = 0.020) whereas the rate was unchanged in the Japan cohort (6.3–8.7%, P = 0.787). In the US cohort, ovarian conservation was not associated with disease-free survival (hazard ratio [HR] 0.829, 95% confidence interval [CI] 0.188–3.663, P = 0.805), overall survival (HR not estimated, P = 0.981), or metachronous secondary malignancy (HR 1.787, 95% CI 0.603–5.295, P = 0.295). In the Japan cohort, ovarian conservation was associated with decreased disease-free survival (HR 5.214, 95% CI 1.557–17.464, P = 0.007) and an increased risk of a metachronous secondary malignancy, particularly ovarian cancer (HR 7.119, 95% CI 1.349–37.554, P = 0.021), but was not associated with overall survival (HR not estimated, P = 0.987). Ovarian recurrence or metachronous secondary ovarian cancer occurred after a median time of 5.9 years, and all cases were salvaged. Conclusion: Our study suggests that adoption of ovarian conservation in young women with early-stage low-grade endometrial cancer varies by population. Ovarian conservation for young women with early-stage, low-grade endometrial cancer may be potentially associated with increased risks of ovarian recurrence or metachronous secondary ovarian cancer in certain populations; nevertheless, ovarian conservation did not negatively impact overall survival.

KW - Endometrial cancer

KW - Ovarian conservation

KW - Recurrence

KW - Secondary primary cancer

KW - Survival

UR - http://www.scopus.com/inward/record.url?scp=85070724287&partnerID=8YFLogxK

U2 - 10.1016/j.ygyno.2019.08.007

DO - 10.1016/j.ygyno.2019.08.007

M3 - Article

C2 - 31427143

AN - SCOPUS:85070724287

SN - 0090-8258

VL - 155

SP - 39

EP - 50

JO - Gynecologic oncology

JF - Gynecologic oncology

IS - 1

ER -

Recurrence, death, and secondary malignancy after ovarian conservation for young women with early-stage low-grade endometrial cancer

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