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The Gut Microbiome Is Associated with Clinical Response to Anti–PD-1/PD-L1 Immunotherapy in Gastrointestinal Cancer

Zhi Peng, Siyuan Cheng, Yan Kou, Ziqi Wang, Rong Jin, Han Hu, Xiaotian Zhang, Ji-fang Gong, Jian Li, Ming Lu, Xicheng Wang, Jun Zhou, ZhiHao Lu, Quan Zhang, David T.W. Tzeng, Dongtao Bi, Yan Tan and Lin Shen
Zhi Peng
1Department of Gastrointestinal Oncology, Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Peking University Cancer Hospital and Institute, Beijing, China.
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Siyuan Cheng
1Department of Gastrointestinal Oncology, Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Peking University Cancer Hospital and Institute, Beijing, China.
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Yan Kou
2Xbiome, Shenzhen, China.
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Ziqi Wang
1Department of Gastrointestinal Oncology, Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Peking University Cancer Hospital and Institute, Beijing, China.
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Rong Jin
3Department of Immunology, School of Basic Medical Sciences, Peking University Health Science Center, Key Laboratory of Medical Immunology (Ministry of Health), Peking University, Beijing, China.
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Han Hu
2Xbiome, Shenzhen, China.
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Xiaotian Zhang
1Department of Gastrointestinal Oncology, Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Peking University Cancer Hospital and Institute, Beijing, China.
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Ji-fang Gong
1Department of Gastrointestinal Oncology, Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Peking University Cancer Hospital and Institute, Beijing, China.
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Jian Li
1Department of Gastrointestinal Oncology, Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Peking University Cancer Hospital and Institute, Beijing, China.
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Ming Lu
1Department of Gastrointestinal Oncology, Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Peking University Cancer Hospital and Institute, Beijing, China.
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Xicheng Wang
1Department of Gastrointestinal Oncology, Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Peking University Cancer Hospital and Institute, Beijing, China.
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Jun Zhou
1Department of Gastrointestinal Oncology, Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Peking University Cancer Hospital and Institute, Beijing, China.
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ZhiHao Lu
1Department of Gastrointestinal Oncology, Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Peking University Cancer Hospital and Institute, Beijing, China.
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Quan Zhang
2Xbiome, Shenzhen, China.
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David T.W. Tzeng
2Xbiome, Shenzhen, China.
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Dongtao Bi
2Xbiome, Shenzhen, China.
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Yan Tan
2Xbiome, Shenzhen, China.
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  • For correspondence: shenlin@bjmu.edu.cn yant@xbiome.com
Lin Shen
1Department of Gastrointestinal Oncology, Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Peking University Cancer Hospital and Institute, Beijing, China.
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  • For correspondence: shenlin@bjmu.edu.cn yant@xbiome.com
DOI: 10.1158/2326-6066.CIR-19-1014 Published October 2020
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Abstract

We report on a comprehensive analysis of the gut microbiomes of patients with gastrointestinal (GI) cancer receiving anti–PD-1/PD-L1 treatment. The human gut microbiota has been associated with clinical responses to anti–PD-1/PD-L1 immunotherapy in melanoma, non–small cell lung cancer, and renal cell carcinoma. We aimed to investigate this association in GI cancers. We also identified bacterial taxa with patient stratification potential. We recruited 74 patients with advanced-stage GI cancer receiving anti–PD-1/PD-L1 treatment and collected their fecal samples prior to and during immunotherapy, along with clinical evaluations. Our 16S rRNA taxonomy survey on the fecal samples revealed an elevation of the Prevotella/Bacteroides ratio in patients, with a preferred response to anti–PD-1/PD-L1 treatment, and a particular subgroup of responders harboring a significantly higher abundance of Prevotella, Ruminococcaceae, and Lachnospiraceae. The shotgun metagenomes of the same samples showed that patients exhibiting different responses had differential abundance of pathways related to nucleoside and nucleotide biosynthesis, lipid biosynthesis, sugar metabolism, and fermentation to short-chain fatty acids (SCFA). Gut bacteria that were capable of SCFA production, including Eubacterium, Lactobacillus, and Streptococcus, were positively associated with anti–PD-1/PD-L1 response across different GI cancer types. We further demonstrated that the identified bacterial taxa were predictive of patient stratification in both our cohort and melanoma patients from two previously published studies. Our results thus highlight the impact of gut microbiomes on anti–PD-1/PD-L1 outcomes, at least in a subset of patients with GI cancer, and suggest the potential of the microbiome as a marker for immune-checkpoint blockade responses.

See articles by Tomita et al., p. 1236, and Hakozaki et al., p. 1243

Footnotes

  • Note: Supplementary data for this article are available at Cancer Immunology Research Online (http://cancerimmunolres.aacrjournals.org/).

  • Cancer Immunol Res 2020;8:1251–61

  • Received December 20, 2019.
  • Revision received March 27, 2020.
  • Accepted August 3, 2020.
  • Published first August 27, 2020.
  • ©2020 American Association for Cancer Research.
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Cancer Immunology Research: 8 (10)
October 2020
Volume 8, Issue 10
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The Gut Microbiome Is Associated with Clinical Response to Anti–PD-1/PD-L1 Immunotherapy in Gastrointestinal Cancer
Zhi Peng, Siyuan Cheng, Yan Kou, Ziqi Wang, Rong Jin, Han Hu, Xiaotian Zhang, Ji-fang Gong, Jian Li, Ming Lu, Xicheng Wang, Jun Zhou, ZhiHao Lu, Quan Zhang, David T.W. Tzeng, Dongtao Bi, Yan Tan and Lin Shen
Cancer Immunol Res October 1 2020 (8) (10) 1251-1261; DOI: 10.1158/2326-6066.CIR-19-1014

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The Gut Microbiome Is Associated with Clinical Response to Anti–PD-1/PD-L1 Immunotherapy in Gastrointestinal Cancer
Zhi Peng, Siyuan Cheng, Yan Kou, Ziqi Wang, Rong Jin, Han Hu, Xiaotian Zhang, Ji-fang Gong, Jian Li, Ming Lu, Xicheng Wang, Jun Zhou, ZhiHao Lu, Quan Zhang, David T.W. Tzeng, Dongtao Bi, Yan Tan and Lin Shen
Cancer Immunol Res October 1 2020 (8) (10) 1251-1261; DOI: 10.1158/2326-6066.CIR-19-1014
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