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Baseline gut microbiota as a predictive marker for the efficacy of neoadjuvant chemotherapy in patients with early breast cancer: a multicenter prospective cohort study in the Setouchi Breast Project-14

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Abstract

Purpose

Various studies have demonstrated the causal relationship between gut microbiota and efficacy of chemotherapy; however, the impact of gut microbiota on breast cancer has not been fully elucidated. This study aimed to evaluate the associations between the gut microbiota before neoadjuvant chemotherapy and its consequent efficacy in breast cancer.

Methods

This prospective observational study included patients who received neoadjuvant chemotherapy for primary early breast cancer at eight institutions between October 1, 2019, and March 31, 2022. We performed 16S rRNA analysis of fecal samples and α and β diversity analyses of the gut microbiota. The primary endpoint was the association between the gut microbiota and pathological complete response (pCR) to neoadjuvant chemotherapy.

Results

Among the 183 patients, the pCR rate after neoadjuvant chemotherapy was 36.1% in all patients and 12.9% (9/70), 69.5% (41/59), and 29.6% (16/54) in those with the luminal, human epidermal growth factor receptor 2, and triple-negative types, respectively. The α diversity of the gut microbiota did not significantly differ between patients with pCR and those without pCR. Among the gut microbiota, two species (Victivallales, P = 0.001 and Anaerolineales, P = 0.001) were associated with pCR, and one (Gemellales, P = 0.002) was associated with non-pCR.

Conclusion

Three species in the gut microbiota had potential associations with neoadjuvant chemotherapy efficacy, but the diversity of the gut microbiota was not associated with response to chemotherapy. Further research is needed to validate our findings.

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Data availability

The data that support the findings of this study are available from the Setouchi Breast Project Comprehensive Support Organization but restrictions apply to the availability of these data, which were used under license for the current study, and so are not publicly available. Data are however available from the authors upon reasonable request and with permission of the Setouchi Breast Project Comprehensive Support Organization.

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Acknowledgements

We would like to thank Ms. Miki Fujiwara, Ms. Mayumi Doumae, and Ms. Eriko Ishioka at the Setouchi Breast Project Comprehensive Support Organization. The results were presented in Japan at the 2023 Breast Cancer Society Regional Meeting and in Italy at the 14th European Breast Cancer Conference. We would like to thank Enago (www.enago.com) for editing the draft of this manuscript.

Funding

This study was conducted as a research support project for the Setouchi Breast Project Comprehensive Support Organization.

Author information

Authors and Affiliations

  1. Department of General Thoracic Surgery and Breast and Endocrinological Surgery, Graduate School of Medicine Dentistry and Pharmaceutical Sciences, Okayama University, Okayama, Japan

    Shogo Nakamoto & Shinichi Toyooka

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

    Yukiko Kajiwara, Hiroyoshi Doihara, Tadahiko Shien, Naruto Taira & Takayuki Iwamoto

  3. Department of Breast Surgery, Hiroshima City Hiroshima Citizens Hospital, Hiroshima, Japan

    Yukiko Kajiwara & Takanori Kin

  4. Department of Pathology, Hiroshima City Hiroshima Citizens Hospital, Hiroshima, Japan

    Kohei Taniguchi

  5. Department of Pathology, Matsuyama Shimin Hospital, Matsuyama, Japan

    Akira I. Hida

  6. Department of Breast Oncology, NHO Shikoku Cancer Center, Matsuyama, Japan

    Yuichiro Miyoshi & Daisuke Takabatake

  7. Department of Breast Endocrine Surgery, Kagawa Prefectural Center Hospital, Takamatsu, Japan

    Yuichiro Miyoshi & Yutaka Ogasawara

  8. Department of Breast and Thyroid Surgery, Fukuyama City Hospital, Fukuyama, Japan

    Mari Yamamoto, Shinichiro Kubo & Masahiko Ikeda

  9. Department of Breast and Thyroid Surgery, Onomichi Municipal Hospital, Onomichi, Japan

    Mari Yamamoto

  10. Department of Breast and Thyroid Surgery, Kochi Health Science Center, Kochi, Japan

    Daisuke Takabatake

  11. Department of Breast Surgery, Matsue Red Cross Hospital, Matsue, Japan

    Hajime Hikino

  12. Department of General Surgery, Kawasaki Medical School General Medical Center, Okayama, Japan

    Hiroyoshi Doihara

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

    Naruto Taira & Takayuki Iwamoto

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  1. Shogo Nakamoto
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Contributions

NT, YK, MI, HD, and TI contributed to the study conception and design. SN, NT, YK, YM, TK, MY, DT, SK, HH, YO, HD, and TI prepared the material preparation and collected the data. AH and KT performed pathological studies of the specimens in this study. SN and TI performed the formal analysis. SN, NT, MI, HD, TS, TI, and ST contributed to the interpretation and discussion of the results. SN wrote the first draft of the manuscript, and all authors commented on the previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Takayuki Iwamoto.

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Conflict of interest

SN: Lecture fee: Daiichi-Sankyo, Eisai and Chugai; AH received honoraria from Daiichi-Sankyo, Pfizer, Chugai and is a member of the Advisory Board of Daiichi-Sankyo, Exact Science; Research grant: Visiopharm, MI: Research grant: Lilly, Honoraria: Daiichi-Sankyo, Lilly, Pfizer, Ezai, Kyowa Kirin, Astra Zeneca, Taiho, Celltrion Healthcare Japan, MSD, Tsumura, Nihon Mediphysics, Exact Science, Chugai, Nihon Kayaku; Advisory Board: Daiichi-Sankyo; Manuscript fee: Pfizer, Chugai, Medic Media; TI received a research grant from Pfizer. The other authors declare no conflicts of interest associated with this manuscript.

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Informed consent was obtained from all individual participants included in the study. All authors consent to the publication of this manuscript. The patient informed consent also included a section on consenting to the publication of the patients’ anonymized data.

Ethics approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This study received an approval from the Ethics Committee of Okayama University Hospital (1909-032, October, 4 2019) and the respective institution, and each participant provided written informed consent.

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10549_2024_7395_MOESM1_ESM.tif

Supplemental Figure 1. α-diversity of the gut microbiome by breast cancer subtypes with (a) Shannon and (b) Chao 1. Abbreviations: HER2, human epidermal growth factor receptor type2; pCR, pathological complete response; TN, triple negative. (TIF 2569 KB)

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Nakamoto, S., Kajiwara, Y., Taniguchi, K. et al. Baseline gut microbiota as a predictive marker for the efficacy of neoadjuvant chemotherapy in patients with early breast cancer: a multicenter prospective cohort study in the Setouchi Breast Project-14. Breast Cancer Res Treat (2024). https://doi.org/10.1007/s10549-024-07395-7

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