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Prognostic value of the 21-Gene Breast Recurrence Score® assay for hormone receptor-positive/human epidermal growth factor 2-negative advanced breast cancer: subanalysis from Japan Breast Cancer Research Group-M07 (FUTURE trial)

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Abstract

Purpose

This study aimed to determine whether the 21-Gene Breast Recurrence Score® assay from primary breast tissue predicts the prognosis of patients with hormone receptor-positive and human epidermal growth factor 2-negative advanced breast cancers (ABCs) treated with fulvestrant monotherapy (Group A) and the addition of palbociclib combined with fulvestrant (Group B), which included those who had progression in Group A from the Japan Breast Cancer Research Group-M07 (FUTURE trial).

Methods

Progression-free survival (PFS) and overall survival (OS) were compared using the log-rank test and Cox regression analysis based on original recurrence score (RS) categories (Low: 0–17, Intermediate: 18–30, High: 31–100) by treatment groups (A and B) and types of ABCs (recurrence and de novo stage IV).

Results

In total, 102 patients [Low: n = 44 (43.1%), Intermediate: n = 38 (37.5%), High: n = 20 (19.6%)] in Group A, and 45 in Group B, who had progression in Group A were analyzed. The median follow-up time was 23.8 months for Group A and 8.9 months for Group B. Multivariate analysis in Group A showed that low-risk [hazard ratio (HR) 0.15, 95% confidence interval (CI) 0.04–0.53, P = 0.003] and intermediate-risk (HR 0.22, 95% CI 0.06–0.78) with de novo stage IV breast cancer were significantly associated with better prognosis compared to high-risk. However, no significant difference was observed among patients with recurrence. No prognostic significance was observed in Group B.

Conclusion

We found a distinct prognostic value of the 21-Gene Breast Recurrence Score® assay by the types of ABCs and a poor prognostic value of the high RS for patients with de novo stage IV BC treated with fulvestrant monotherapy. Further validations of these findings are required.

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Data availability

The datasets generated during and/or analyzed during the current study are not publicly available due to no approval from the Ethics Committee for sharing data.

Consent to publish

All study participants consent for publication of this study.

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Acknowledgements

We greatly appreciate all women who participated in this trial, and all investigators and their collaborators for their dedication to this study, Mebics for their data entry assistance, SRL, Inc. (Tokyo, Japan) for their assistance in cutting and transporting the tissue and the Japan Breast Cancer Research Group (JBCRG) for their administrative assistance.

Funding

This trial was founded by Pfizer, Inc. and AstraZeneca K.K.

Author information

Authors and Affiliations

  1. Breast and Thyroid Surgery, Kawasaki Medical School Hospital, 577 Matsushima, Kurashiki, Okayama, 701-0192, Japan

    Takayuki Iwamoto

  2. Breast and Endocrine Surgery, Okayama University Hospital, Okayama, Japan

    Takayuki Iwamoto

  3. Department of Breast Oncology, Tokai University School of Medicine, Isehara, Kanagawa, Japan

    Naoki Niikura & Takuho Okamura

  4. Breast Surgery, Hokkaido Cancer Center, Sapporo, Hokkaido, Japan

    Kenichi Watanabe & Nobumoto Tomioka

  5. Breast and Endocrine Surgery, Kumamoto City Hospital, Kumamoto, Kumamoto, Japan

    Takashi Takeshita

  6. Department of Breast Surgery, Kansai Medical University Hospital, Hirakata, Osaka, Japan

    Yuichiro Kikawa

  7. Department of Medical Oncology, Saitama Red Cross Hospital, Saitama, Saitama, Japan

    Kokoro Kobayashi

  8. Breast Center, Department of Breast Surgery, NHO Kyushu Medical Center, Fukuoka, Fukuoka, Japan

    Nobutaka Iwakuma

  9. Department of Breast Medical Oncology, Cancer Institute Hospital of JFCR, Koto-ku, Tokyo, Japan

    Takayuki Kobayashi

  10. Department of Breast Surgery, Kurume University Hospital, Kurume, Fukuoka, Japan

    Yuriko Katagiri

  11. Breast Disease Center, Asahikawa Medical University, Asahikawa, Hokkaido, Japan

    Masahiro Kitada

  12. Division of Breast and Endocrine Surgery, Department of Surgery, School of Medicine, Hyogo Medical University, Nishinomiya, Hyogo, Japan

    Yasuo Miyoshi

  13. Department of Surgical Oncology, Research Institute for Radiation and Medicine, Hiroshima University Hospital, Hiroshima, Hiroshima, Japan

    Hideo Shigematsu

  14. Division of Breast and Endocrine Surgery, Department of Surgery, Tohoku University Hospital, Sendai, Miyagi, Japan

    Minoru Miyashita

  15. Breast Oncology Service, Saitama Medical University International Medical Center, Hidaka, Saitama, Japan

    Hiroshi Ishiguro

  16. Department of Breast and Endocrine Surgery, Nagoya University Graduate School of Medicine, Nagoya, Aichi, Japan

    Norikazu Masuda

  17. Department of Medical Oncology, Fukushima Medical University School of Medicine, Fukushima, Fukushima, Japan

    Shigehira Saji

Authors
  1. Takayuki Iwamoto
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  2. Naoki Niikura
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Contributions

Drafting the work: T Iwamoto; conception or design of the work: T Iwamoto, N Niikura, K Watanabe, T Takeshita, Y Kikawa, N Iwakuma, H Ishiguro, N Masuda, and S Saji; acquisition of data and samples: K Kobayashi, T Okamura, T Kobayashi, Y Katagiri, M Kitada, N Tomioka, Y Miyoshi, H Shigematsu, and M Miyashita; Final approval of the version to be published: all authors.

Corresponding author

Correspondence to Takayuki Iwamoto.

Ethics declarations

Conflict of interest

Grants or contracts from any entity

NN: Chugai, Pfizer, Eisai, Mochida, Daiichi Sankyo, Novartis; YMDaiichi-Sankyo, Eisai, Chugai, MSD, Kyowa-Kirin, Eli Lilly, Taiho; HI: Eisai Co., Ltd., Daiichi sankyo co., Ltd., Chugai Pharmaceutical Co., Ltd., Takeda Pharmaceutical Company Limited, AstraZeneca plc, MSD K.K., AstraZeneca plc, Eisai Co., Ltd., Kyowa Kirin Co., Ltd., MSD K.K., Taiho Pharmaceutical Co., Ltd.., Chugai Pharmaceutical Co., Ltd., Nippon Kayaku Co., Ltd., Novartis Pharma K.K., Sawai Pharmaceutical Co., Ltd., Covance Japan Co., Ltd., Maruho Co.,Ltd., LabCorp Japan, G.K., Sanofi S.A., Takeda Pharmaceutical Company Limited, Eli Lilly Japan KK; NM: Chugai, Eli Lilly, Astra Zeneca, Pfizer, Daiichi-Sankyo, MSD, Eisai, Novartis, Gilead Sciences, Ono-Pharma; SS: Taiho, Eisai, Chugai, Takeda, MSD, Astra Zeneca, Daiichi Sankyo. Payment or honoraria NN: Chugai, Eli Lilly, MSD, Daiichi-Sankyo, AstraZeneca, Pfizer; KW: Chugai, Eli Lilly, Nippon-Kayaku, Kyowa-Kirin, Novartis, Taiho, Eisai, Pfizer, Shionogi, Daiichi-Sankyo, AstraZeneca; YK: Eisai, Daiichi Sankyo, Lilliy, Chugai, Pfizer, AstraZeneca, Taiho; KK: Pfizer, Eli lily, Taiho, AstraZeneca, Eisai, Chugai, Novartis: YM: Daiichi-Sankyo, Chugai, Eisai, Eli Lilly, AstraZeneca, Pfizer, Taiho, Kyowa-Kirin; MM: Chugai, Eli Lilly, MSD, Daiichi Sankyo, AstraZeneca, Pfizer, Taiho, Eisai; HI: Eisai Co., Ltd., Chugai Pharmaceutical Co., Ltd., Pfizer Inc., Kyowa Kirin Co., Ltd., Daiichi sankyo co., Ltd., Taiho Pharmaceutical Co., Ltd., Mitsubishi Tanabe Pharma Corporation, AstrazenecaKK, MSD K.K; NM: Chugai, Pfizer, Astra Zeneca, Eli Lilly, Daiichi Sankyo; SS: Chugai, Kyowa Kirin, MSD, Novartis, Eisai, Takeda, Daiichi Sankyo, Eli Lilly, Astra Zeneca, Pfizer, Taiho, Ono, Nipponkayaku Leadership or fiduciary role NM: JBCRG, Japanese Breast Cancer Society (JBCS), Japan Society of Clinical Oncology (JSCO); SS: JBCRG, JBCS, JSMO, BIG The other authors have no competing interests.

Grants or contracts from any entity

NN: Chugai, Pfizer, Eisai, Mochida, Daiichi Sankyo, Novartis; YM: Daiichi-Sankyo, Eisai, Chugai, MSD, Kyowa-Kirin, Eli Lilly, Taiho; HI: Eisai Co., Ltd., Daiichi Sankyo Co., Ltd., Chugai Pharmaceutical Co., Ltd., Takeda Pharmaceutical Company Limited, AstraZeneca Plc, MSD K.K., AstraZeneca Plc, Eisai Co., Ltd., Kyowa Kirin Co., Ltd., MSD K.K., Taiho Pharmaceutical Co., Ltd.., Chugai Pharmaceutical Co., Ltd., Nippon Kayaku Co., Ltd., Novartis Pharma K.K., Sawai Pharmaceutical Co., Ltd., Covance Japan Co., Ltd., Maruho Co., Ltd., LabCorp Japan, G.K., Sanofi S.A., Takeda Pharmaceutical Company Limited, Eli Lilly Japan KK; NM: Chugai, Eli Lilly, AstraZeneca, Pfizer, Daiichi-Sankyo, MSD, Eisai, Novartis, Gilead Sciences, Ono-Pharma; SS: Taiho, Eisai, Chugai, Takeda, MSD, AstraZeneca, Daiichi Sankyo.

Payment or honoraria

NN: Chugai, Eli Lilly, MSD, Daiichi-Sankyo, AstraZeneca, Pfizer; KW: Chugai, Eli Lilly, Nippon-Kayaku, Kyowa-Kirin, Novartis, Taiho, Eisai, Pfizer, Shionogi, Daiichi-Sankyo, AstraZeneca; YK: Eisai, Daiichi Sankyo, Lilliy, Chugai, Pfizer, AstraZeneca, Taiho; KK: Pfizer, Eli lily, Taiho, AstraZeneca, Eisai, Chugai, Novartis: YM: Daiichi-Sankyo, Chugai, Eisai, Eli Lilly, AstraZeneca, Pfizer, Taiho, Kyowa-Kirin; MM: Chugai, Eli Lilly, MSD, Daiichi Sankyo, AstraZeneca, Pfizer, Taiho, Eisai; HI: Eisai Co., Ltd., Chugai Pharmaceutical Co., Ltd., Pfizer, Inc., Kyowa Kirin Co., Ltd., Daiichi Sankyo Co., Ltd., Taiho Pharmaceutical Co., Ltd., Mitsubishi Tanabe Pharma Corporation, AstraZeneca K.K., MSD K.K; NM: Chugai, Pfizer, AstraZeneca, Eli Lilly, Daiichi Sankyo; SS: Chugai, Kyowa Kirin, MSD, Novartis, Eisai, Takeda, Daiichi Sankyo, Eli Lilly, AstraZeneca, Pfizer, Taiho, Ono, Nippon Kayaku.

Leadership or fiduciary role

NM: JBCRG, Japanese Breast Cancer Society (JBCS), Japan Society of Clinical Oncology (JSCO); SS: JBCRG, JBCS, JSMO, BIG.

The other authors have no competing interests.

Ethical approval

This study received an approval from the Ethics Committee of Fukushima Medical University School of Medicine, Okayama University Hospital and the respective institution.

Informed consent

Informed consent was obtained from all individual participants included in the study.

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Supplementary Information

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(TIF 72 kb) Supplementary Fig. 1 CONSORT flow diagram in Group A. TR translational research

(TIF 81 kb) Supplementary Fig. 2 CONSORT flow diagram in Group B. TR translational research

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(TIF 78 kb) Supplementary Fig. 3 Histogram of the recurrence score (RS) in Group B. The x-axis represents the RS at intervals of 5, and the y-axis represents the frequency

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(TIF 79 kb) Supplementary Fig. 4 Kaplan–Meier curves for patients with recurrence treated with fulvestrant monotherapy according to recurrence score categories (Group A). Kaplan–Meier curves for A progression-free survival and B overall survival. P-values were calculated using the log-rank test. Hazard ratios (HRs) and 95% confidence intervals (CIs) were estimated using Cox regression analysis. Black solid line: low-risk group; red solid line: intermediate-risk group; green solid line: high-risk group

10549_2024_7414_MOESM5_ESM.tif

(TIF 80 kb) Supplementary Fig. 5 Kaplan–Meier curves for patients with visceral advanced breast cancer (ABC) treated with fulvestrant monotherapy according to recurrence score categories (Group A). Kaplan–Meier curves for A progression-free survival and B overall survival. P-values were calculated using the log-rank test. Hazard ratios (HRs) and 95% confidence intervals (CIs) were estimated using Cox regression analysis. Black solid line: low-risk group; red solid line: intermediate-risk group; green solid line: high-risk group

10549_2024_7414_MOESM6_ESM.tif

(TIF 93 kb) Supplementary Fig. 6 Kaplan–Meier curves for patients with non-visceral advanced breast cancer (ABC) treated with fulvestrant monotherapy according to recurrence score categories (Group A). Kaplan–Meier curves for A progression-free survival and B overall survival. P-values were calculated using the log-rank test. Hazard ratios (HRs) and 95% confidence intervals (CIs) were estimated using Cox regression analysis. Black solid line: low-risk group; red solid line: intermediate-risk group; green solid line: high-risk group

10549_2024_7414_MOESM7_ESM.tif

(TIF 79 kb) Supplementary Fig. 7 Kaplan–Meier curves for patients treated with first-line endocrine treatment according to recurrence score categories (Group A). Kaplan–Meier curves for A progression-free survival and B overall survival. P-values were calculated using the log-rank test. Hazard ratios (HRs) and 95% confidence intervals (CIs) were estimated using Cox regression analysis. Black solid line: low-risk group; red solid line: intermediate-risk group; green solid line: high-risk group

10549_2024_7414_MOESM8_ESM.tif

(TIF 76 kb) Supplementary Fig. 8 Kaplan–Meier curves for patients treated with second-line endocrine treatment according to recurrence score categories (Group A). Kaplan–Meier curves for A progression-free survival and B overall survival. P-values were calculated using the log-rank test. Hazard ratios (HRs) and 95% confidence intervals (CIs) were estimated using Cox regression analysis. Black solid line: low-risk group; red solid line: intermediate-risk group; green solid line: high-risk group

10549_2024_7414_MOESM9_ESM.tif

(TIF 78 kb) Supplementary Fig. 9 Kaplan–Meier curves for patients with advanced breast cancer (ABC) treated with combination therapy according to recurrence score categories (Group B). Kaplan–Meier curves for A progression-free survival and B overall survival. P-values were calculated using the log-rank test. Hazard ratios (HRs) and 95% confidence intervals (CIs) were estimated using Cox regression analysis. Black solid line: low-risk group; red solid line: intermediate-risk group; green solid line: high-risk group

10549_2024_7414_MOESM10_ESM.tif

(TIF 69 kb) Supplementary Fig. 10 Kaplan–Meier curves for patients with de novo stage IV breast cancer treated with combination therapy according to recurrence score categories (Group B). Kaplan–Meier curves for A progression-free survival and B overall survival. P-values were calculated using the log-rank test. Hazard ratios (HRs) and 95% confidence intervals (CIs) were estimated using Cox regression analysis. Black solid line: low-risk group; red solid line: intermediate-risk group; green solid line: high-risk group

10549_2024_7414_MOESM11_ESM.tif

(TIF 48 kb) Supplementary Fig. 11 Kaplan–Meier curves for patients with recurrence treated with combination therapy according to recurrence score categories (Group B). Kaplan–Meier curves for A progression-free survival and B overall survival. P-values were calculated using the log-rank test. Hazard ratios (HRs) and 95% confidence intervals (CIs) were estimated using Cox regression analysis. Black solid line: low-risk group; red solid line: intermediate-risk group; green solid line: high-risk group

10549_2024_7414_MOESM12_ESM.tif

(TIF 82 kb) Supplementary Fig. 12 Kaplan–Meier curves for visceral metastatic patients treated with combination therapy according to recurrence score categories (Group B). Kaplan–Meier curves for A progression-free survival and B overall survival. P-values were calculated using the log-rank test. Hazard ratios (HRs) and 95% confidence intervals (CIs) were estimated using Cox regression analysis. Black solid line: low-risk group; red solid line: intermediate-risk group; green solid line: high-risk group

10549_2024_7414_MOESM13_ESM.tif

(TIF 82 kb) Supplementary Fig. 13 Kaplan–Meier curves for patients with non-visceral metastatic breast cancer treated with combination therapy according to recurrence score categories (Group B). Kaplan–Meier curves for A progression-free survival and B overall survival. P-values were calculated using the log-rank test. Hazard ratios (HRs) and 95% confidence intervals (CIs) were estimated using Cox regression analysis. Black solid line: low-risk group; red solid line: intermediate-risk group; green solid line: high-risk group

10549_2024_7414_MOESM14_ESM.tif

(TIF 83 kb) Supplementary Fig. 14 Multivariate analysis for recurrence score categories in the palbociclib cohort (Group B). A Progression free survival, and B Overall survival; Multivariate Cox regression analysis was conducted to determine whether the 21-Gene Breast Recurrence Score® assay could predict prognosis. P value was adjusted by age, Progesterone receptor status, de novo/recurrence and visceral/non-visceral. HR hazard ratio, CI confidence interval

10549_2024_7414_MOESM15_ESM.tif

(TIF 85 kb) Supplementary Fig. 15 Kaplan–Meier curves for patients treated with fulvestrant monotherapy (Group A) according to two recurrence score categories. Kaplan–Meier curves for A progression-free survival and B overall survival. P-values were calculated using the log-rank test. Hazard ratios (HRs) and 95% confidence intervals (CIs) were estimated using Cox regression analysis. Black solid line: low-risk group (RS: 25 or below); red solid line: high-risk group (RS: 26 or above)

10549_2024_7414_MOESM16_ESM.tif

(TIF 85 kb) Supplementary Fig. 16 Kaplan–Meier curves for patients with recurrence breast cancer treated with fulvestrant monotherapy (Group A) according to two recurrence score categories. Kaplan–Meier curves for A progression-free survival and B overall survival. P-values were calculated using the log-rank test. Hazard ratios (HRs) and 95% confidence intervals (CIs) were estimated using Cox regression analysis. Black solid line: low-risk group (RS: 25 or below); red solid line: high-risk group (RS: 26 or above)

10549_2024_7414_MOESM17_ESM.tif

(TIF 82 kb) Supplementary Fig. 17 Kaplan–Meier curves for patients with de novo stage IV breast cancer treated with fulvestrant monotherapy (Group A) according to two recurrence score categories. Kaplan–Meier curves for A progression-free survival and B overall survival. P-values were calculated using the log-rank test. Hazard ratios (HRs) and 95% confidence intervals (CIs) were estimated using Cox regression analysis. Black solid line: low-risk group (RS: 25 or below); red solid line: high-risk group (RS: 26 or above)

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Iwamoto, T., Niikura, N., Watanabe, K. et al. Prognostic value of the 21-Gene Breast Recurrence Score® assay for hormone receptor-positive/human epidermal growth factor 2-negative advanced breast cancer: subanalysis from Japan Breast Cancer Research Group-M07 (FUTURE trial). Breast Cancer Res Treat (2024). https://doi.org/10.1007/s10549-024-07414-7

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