Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Oncology Letters
      • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Biomedical Reports
      • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • Information for Authors
    • Information for Reviewers
    • Information for Librarians
    • Information for Advertisers
    • Conferences
  • Language Editing
Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • For Authors
    • For Reviewers
    • For Librarians
    • For Advertisers
    • Conferences
  • Language Editing
Login Register Submit
  • This site uses cookies
  • You can change your cookie settings at any time by following the instructions in our Cookie Policy. To find out more, you may read our Privacy Policy.

    I agree
Search articles by DOI, keyword, author or affiliation
Search
Advanced Search
presentation
Oncology Letters
Join Editorial Board Propose a Special Issue
Print ISSN: 1792-1074 Online ISSN: 1792-1082
Journal Cover
February-2024 Volume 27 Issue 2

Full Size Image

Sign up for eToc alerts
Recommend to Library

Journals

International Journal of Molecular Medicine

International Journal of Molecular Medicine

International Journal of Molecular Medicine is an international journal devoted to molecular mechanisms of human disease.

International Journal of Oncology

International Journal of Oncology

International Journal of Oncology is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

Molecular Medicine Reports

Covers molecular medicine topics such as pharmacology, pathology, genetics, neuroscience, infectious diseases, molecular cardiology, and molecular surgery.

Oncology Reports

Oncology Reports

Oncology Reports is an international journal devoted to fundamental and applied research in Oncology.

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine is an international journal devoted to laboratory and clinical medicine.

Oncology Letters

Oncology Letters

Oncology Letters is an international journal devoted to Experimental and Clinical Oncology.

Biomedical Reports

Biomedical Reports

Explores a wide range of biological and medical fields, including pharmacology, genetics, microbiology, neuroscience, and molecular cardiology.

Molecular and Clinical Oncology

Molecular and Clinical Oncology

International journal addressing all aspects of oncology research, from tumorigenesis and oncogenes to chemotherapy and metastasis.

World Academy of Sciences Journal

World Academy of Sciences Journal

Multidisciplinary open-access journal spanning biochemistry, genetics, neuroscience, environmental health, and synthetic biology.

International Journal of Functional Nutrition

International Journal of Functional Nutrition

Open-access journal combining biochemistry, pharmacology, immunology, and genetics to advance health through functional nutrition.

International Journal of Epigenetics

International Journal of Epigenetics

Publishes open-access research on using epigenetics to advance understanding and treatment of human disease.

Medicine International

Medicine International

An International Open Access Journal Devoted to General Medicine.

Journal Cover
February-2024 Volume 27 Issue 2

Full Size Image

Sign up for eToc alerts
Recommend to Library

  • Article
  • Citations
    • Cite This Article
    • Download Citation
    • Create Citation Alert
    • Remove Citation Alert
    • Cited By
  • Similar Articles
    • Related Articles (in Spandidos Publications)
    • Similar Articles (Google Scholar)
    • Similar Articles (PubMed)
  • Download PDF
  • Download XML
  • View XML
Review Open Access

Gut microbiota influences the efficiency of immune checkpoint inhibitors by modulating the immune system (Review)

  • Authors:
    • Haihong Jiang
    • Qinlu Zhang
  • View Affiliations / Copyright

    Affiliations: Department of Oncology, Huaihe Hospital of Henan University, Kaifeng, Henan 475001, P.R. China, Department of Endocrinology, Huaihe Hospital of Henan University, Kaifeng, Henan 475001, P.R. China
    Copyright: © Jiang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Article Number: 87
    |
    Published online on: January 5, 2024
       https://doi.org/10.3892/ol.2024.14221
  • Expand metrics +
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )
Cited By (CrossRef): 0 citations Loading Articles...

This article is mentioned in:



Abstract

Immune checkpoint inhibitors (ICIs) are commonly utilized in tumor treatment. However, they still have limitations, including insufficient effectiveness and unavoidable adverse events. It has been demonstrated that gut microbiota can influence the effectiveness of ICIs, although the precise mechanism remains unclear. Gut microbiota plays a crucial role in the formation and development of the immune system. Gut microbiota and their associated metabolites play a regulatory role in immune balance. Tumor occurrence and development are linked to their ability to evade recognition and destruction by the immune system. The purpose of ICIs treatment is to reinitiate the immune system's elimination of tumor cells. Thus, the immune system acts as a communication bridge between gut microbiota and ICIs. Varied composition and characteristics of gut microbiota result in diverse outcomes in ICIs treatment. Certain gut microbiota‑related metabolites also influence the therapeutic efficacy of ICIs to some extent. The administration of antibiotics before or during ICIs treatment can diminish treatment effectiveness. The utilization of probiotics and fecal transplantation can partially alter the outcome of ICIs treatment. The present review synthesized previous studies to examine the association between gut microbiota and ICIs, elucidated the role of gut microbiota and its associated factors in ICIs treatment, and offered direction for future research.
View Figures

Figure 1

View References

1 

Christofi T, Baritaki S, Falzone L, Libra M and Zaravinos A: Current perspectives in cancer immunotherapy. Cancers (Basel). 11:14722019. View Article : Google Scholar : PubMed/NCBI

2 

Gupta SL, Basu S, Soni V and Jaiswal RK: Immunotherapy: An alternative promising therapeutic approach against cancers. Mol Biol Rep. 49:9903–9913. 2022. View Article : Google Scholar : PubMed/NCBI

3 

Kennedy LB and Salama AKS: A review of cancer immunotherapy toxicity. CA Cancer J Clin. 70:86–104. 2020. View Article : Google Scholar : PubMed/NCBI

4 

Shi Z, Li H, Song W, Zhou Z, Li Z and Zhang M: Emerging roles of the gut microbiota in cancer immunotherapy. Front Immunol. 14:11398212023. View Article : Google Scholar : PubMed/NCBI

5 

Vivarelli S, Salemi R, Candido S, Falzone L, Santagati M, Stefani S, Torino F, Banna GL, Tonini G and Libra M: Gut microbiota and cancer: From pathogenesis to therapy. Cancers (Basel). 11:382019. View Article : Google Scholar : PubMed/NCBI

6 

Kumagai T, Rahman F and Smith AM: The microbiome and radiation induced-bowel injury: Evidence for potential mechanistic role in disease pathogenesis. Nutrients. 10:14052018. View Article : Google Scholar : PubMed/NCBI

7 

Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, et al: A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 464:59–65. 2010. View Article : Google Scholar : PubMed/NCBI

8 

Jandhyala SM, Talukdar R, Subramanyam C, Vuyyuru H, Sasikala M and Nageshwar Reddy D: Role of the normal gut microbiota. World J Gastroenterol. 21:8787–8803. 2015. View Article : Google Scholar : PubMed/NCBI

9 

Tuddenham S and Sears CL: The intestinal microbiome and health. Curr Opin Infect Dis. 28:464–470. 2015. View Article : Google Scholar : PubMed/NCBI

10 

Jain N: The early life education of the immune system: Moms, microbes and (missed) opportunities. Gut Microbes. 12:18245642020. View Article : Google Scholar : PubMed/NCBI

11 

Gao Y, O'Hely M, Quinn TP, Ponsonby AL, Harrison LC, Frøkiær H, Tang MLK, Brix S, Kristiansen K, Burgner D, et al: Maternal gut microbiota during pregnancy and the composition of immune cells in infancy. Front Immunol. 13:9863402022. View Article : Google Scholar : PubMed/NCBI

12 

Rio-Aige K, Azagra-Boronat I, Massot-Cladera M, Selma-Royo M, Parra-Llorca A, González S, García-Mantrana I, Castell M, Rodríguez-Lagunas MJ, Collado MC and Pérez Cano FJ: Association of maternal microbiota and diet in cord blood cytokine and immunoglobulin profiles. Int J Mol Sci. 22:17782021. View Article : Google Scholar : PubMed/NCBI

13 

Henrick BM, Rodriguez L, Lakshmikanth T, Pou C, Henckel E, Arzoomand A, Olin A, Wang J, Mikes J, Tan Z, et al: Bifidobacteria-mediated immune system imprinting early in life. Cell. 184:3884–3898.e11. 2021. View Article : Google Scholar : PubMed/NCBI

14 

Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R, Angenent LT and Ley RE: Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci USA. 108 (Suppl 1):S4578–S4585. 2011. View Article : Google Scholar

15 

Odamaki T, Kato K, Sugahara H, Hashikura N, Takahashi S, Xiao JZ, Abe F and Osawa R: Age-related changes in gut microbiota composition from newborn to centenarian: A cross-sectional study. BMC Microbiol. 16:902016. View Article : Google Scholar : PubMed/NCBI

16 

Xu Y, Wang Y, Li H, Dai Y, Chen D, Wang M, Jiang X, Huang Z, Yu H, Huang J and Xiong Z: Altered fecal microbiota composition in older adults with frailty. Front Cell Infect Microbiol. 11:6961862021. View Article : Google Scholar : PubMed/NCBI

17 

Cheng H, Guan X, Chen D and Ma W: The Th17/Treg cell balance: A gut microbiota-modulated story. Microorganisms. 7:5832019. View Article : Google Scholar : PubMed/NCBI

18 

Lee GR: The balance of Th17 versus Treg cells in autoimmunity. Int J Mol Sci. 19:7302018. View Article : Google Scholar : PubMed/NCBI

19 

Ivanov II, Frutos Rde L, Manel N, Yoshinaga K, Rifkin DB, Sartor RB, Finlay BB and Littman DR: Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe. 4:337–349. 2008. View Article : Google Scholar : PubMed/NCBI

20 

Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y, Cheng G, Yamasaki S, Saito T, Ohba Y, et al: Induction of colonic regulatory T cells by indigenous Clostridium species. Science. 331:337–341. 2011. View Article : Google Scholar : PubMed/NCBI

21 

Round JL, Lee SM, Li J, Tran G, Jabri B, Chatila TA and Mazmanian SK: The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science. 332:974–977. 2011. View Article : Google Scholar : PubMed/NCBI

22 

Erturk-Hasdemir D, Oh SF, Okan NA, Stefanetti G, Gazzaniga FS, Seeberger PH, Plevy SE and Kasper DL: Symbionts exploit complex signaling to educate the immune system. Proc Natl Acad Sci USA. 116:26157–26166. 2019. View Article : Google Scholar : PubMed/NCBI

23 

Sun M, Wu W, Chen L, Yang W, Huang X, Ma C, Chen F, Xiao Y, Zhao Y, Ma C, et al: Microbiota-derived short-chain fatty acids promote Th1 cell IL-10 production to maintain intestinal homeostasis. Nat Commun. 9:35552018. View Article : Google Scholar : PubMed/NCBI

24 

Martin-Gallausiaux C, Béguet-Crespel F, Marinelli L, Jamet A, Ledue F, Blottière HM and Lapaque N: Butyrate produced by gut commensal bacteria activates TGF-beta1 expression through the transcription factor SP1 in human intestinal epithelial cells. Sci Rep. 8:97422018. View Article : Google Scholar : PubMed/NCBI

25 

Duscha A, Gisevius B, Hirschberg S, Yissachar N, Stangl GI, Dawin E, Bader V, Haase S, Kaisler J, David C, et al: Propionic acid shapes the multiple sclerosis disease course by an immunomodulatory mechanism. Cell. 180:1067–1080.e16. 2020. View Article : Google Scholar : PubMed/NCBI

26 

Levy M, Thaiss CA, Zeevi D, Dohnalová L, Zilberman-Schapira G, Mahdi JA, David E, Savidor A, Korem T, Herzig Y, et al: Microbiota-modulated metabolites shape the intestinal microenvironment by regulating NLRP6 inflammasome signaling. Cell. 163:1428–1443. 2015. View Article : Google Scholar : PubMed/NCBI

27 

Guo C, Xie S, Chi Z, Zhang J, Liu Y, Zhang L, Zheng M, Zhang X, Xia D, Ke Y, et al: Bile acids control inflammation and metabolic disorder through inhibition of NLRP3 inflammasome. Immunity. 45:802–816. 2016. View Article : Google Scholar : PubMed/NCBI

28 

Yan F, Cao H, Cover TL, Whitehead R, Washington MK and Polk DB: Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology. 132:562–575. 2007. View Article : Google Scholar : PubMed/NCBI

29 

Salemi R, Vivarelli S, Ricci D, Scillato M, Santagati M, Gattuso G, Falzone L and Libra M: Lactobacillus rhamnosus GG cell-free supernatant as a novel anti-cancer adjuvant. J Transl Med. 21:1952023. View Article : Google Scholar : PubMed/NCBI

30 

Ottman N, Reunanen J, Meijerink M, Pietilä TE, Kainulainen V, Klievink J, Huuskonen L, Aalvink S, Skurnik M, Boeren S, et al: Pili-like proteins of Akkermansia muciniphila modulate host immune responses and gut barrier function. PLoS One. 12:e01730042017. View Article : Google Scholar : PubMed/NCBI

31 

Alexander M, Ang QY, Nayak RR, Bustion AE, Sandy M, Zhang B, Upadhyay V, Pollard KS, Lynch SV and Turnbaugh PJ: Human gut bacterial metabolism drives Th17 activation and colitis. Cell Host Microbe. 30:17–30.e9. 2022. View Article : Google Scholar : PubMed/NCBI

32 

Vinay DS, Ryan EP, Pawelec G, Talib WH, Stagg J, Elkord E, Lichtor T, Decker WK, Whelan RL, Kumara HMCS, et al: Immune evasion in cancer: Mechanistic basis and therapeutic strategies. Semin Cancer Biol. 35 (Suppl):S185–S198. 2015. View Article : Google Scholar : PubMed/NCBI

33 

Wei G, Zhang H, Zhao H, Wang J, Wu N, Li L, Wu J and Zhang D: Emerging immune checkpoints in the tumor microenvironment: Implications for cancer immunotherapy. Cancer Lett. 511:68–76. 2021. View Article : Google Scholar : PubMed/NCBI

34 

Iwai Y, Ishida M, Tanaka Y, Okazaki T, Honjo T and Minato N: Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc Natl Acad Sci USA. 99:12293–12297. 2002. View Article : Google Scholar : PubMed/NCBI

35 

Herbst RS, Soria JC, Kowanetz M, Fine GD, Hamid O, Gordon MS, Sosman JA, McDermott DF, Powderly JD, Gettinger SN, et al: Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature. 515:563–567. 2014. View Article : Google Scholar : PubMed/NCBI

36 

Park JJ, Thi EP, Carpio VH, Bi Y, Cole AG, Dorsey BD, Fan K, Harasym T, Iott CL, Kadhim S, et al: Checkpoint inhibition through small molecule-induced internalization of programmed death-ligand 1. Nat Commun. 12:12222021. View Article : Google Scholar : PubMed/NCBI

37 

Lee HT, Lee SH and Heo YS: Molecular interactions of antibody drugs targeting PD-1, PD-L1, and CTLA-4 in immuno-oncology. Molecules. 24:11902019. View Article : Google Scholar : PubMed/NCBI

38 

Das R, Verma R, Sznol M, Boddupalli CS, Gettinger SN, Kluger H, Callahan M, Wolchok JD, Halaban R, Dhodapkar MV and Dhodapkar KM: Combination therapy with anti-CTLA-4 and anti-PD-1 leads to distinct immunologic changes in vivo. J Immunol. 194:950–959. 2015. View Article : Google Scholar : PubMed/NCBI

39 

Shi AP, Tang XY, Xiong YL, Zheng KF, Liu YJ, Shi XG, Lv Y, Jiang T, Ma N and Zhao JB: Immune checkpoint LAG3 and Its Ligand FGL1 in cancer. Front Immunol. 12:7850912022. View Article : Google Scholar : PubMed/NCBI

40 

Kandel S, Adhikary P, Li G and Cheng K: The TIM3/Gal9 signaling pathway: An emerging target for cancer immunotherapy. Cancer Lett. 510:67–78. 2021. View Article : Google Scholar : PubMed/NCBI

41 

Tan AC, Bagley SJ, Wen PY, Lim M, Platten M, Colman H, Ashley DM, Wick W, Chang SM, Galanis E, et al: Systematic review of combinations of targeted or immunotherapy in advanced solid tumors. J Immunother Cancer. 9:e0024592021. View Article : Google Scholar : PubMed/NCBI

42 

Syn NL, Teng MWL, Mok TSK and Soo RA: De-novo and acquired resistance to immune checkpoint targeting. Lancet Oncol. 18:e731–e741. 2017. View Article : Google Scholar : PubMed/NCBI

43 

Sanmamed MF and Chen L: A paradigm shift in cancer immunotherapy: From enhancement to normalization. Cell. 175:313–326. 2018. View Article : Google Scholar : PubMed/NCBI

44 

Boutros C, Tarhini A, Routier E, Lambotte O, Ladurie FL, Carbonnel F, Izzeddine H, Marabelle A, Champiat S, Berdelou A, et al: Safety profiles of anti-CTLA-4 and anti-PD-1 antibodies alone and in combination. Nat Rev Clin Oncol. 13:473–486. 2016. View Article : Google Scholar : PubMed/NCBI

45 

Brahmer JR, Lacchetti C, Schneider BJ, Atkins MB, Brassil KJ, Caterino JM, Chau I, Ernstoff MS, Gardner JM, Ginex P, et al: Management of immune-related adverse events in patients treated with immune checkpoint inhibitor therapy: American society of clinical oncology clinical practice guideline. J Clin Oncol. 36:1714–1768. 2018. View Article : Google Scholar : PubMed/NCBI

46 

Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, et al: Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 366:2443–2454. 2012. View Article : Google Scholar : PubMed/NCBI

47 

Ott PA, Bang YJ, Berton-Rigaud D, Elez E, Pishvaian MJ, Rugo HS, Puzanov I, Mehnert JM, Aung KL, Lopez J, et al: Safety and antitumor activity of pembrolizumab in advanced programmed death ligand 1-positive endometrial cancer: Results from the KEYNOTE-028 study. J Clin Oncol. 35:2535–2541. 2017. View Article : Google Scholar : PubMed/NCBI

48 

Antonia SJ, Balmanoukian A, Brahmer J, Ou SI, Hellmann MD, Kim SW, Ahn MJ, Kim DW, Gutierrez M, Liu SV, et al: Clinical activity, tolerability, and long-term follow-up of durvalumab in patients with advanced NSCLC. J Thorac Oncol. 14:1794–1806. 2019. View Article : Google Scholar : PubMed/NCBI

49 

Schöffski P, Tan DSW, Martín M, Ochoa-de-Olza M, Sarantopoulos J, Carvajal RD, Kyi C, Esaki T, Prawira A, Akerley W, et al: Phase I/II study of the LAG-3 inhibitor ieramilimab (LAG525) ± anti-PD-1 spartalizumab (PDR001) in patients with advanced malignancies. J Immunother Cancer. 10:e0037762022. View Article : Google Scholar : PubMed/NCBI

50 

Curigliano G, Gelderblom H, Mach N, Doi T, Tai D, Forde PM, Sarantopoulos J, Bedard PL, Lin CC, Hodi FS, et al: Phase I/Ib clinical trial of sabatolimab, an anti-TIM-3 antibody, alone and in combination with spartalizumab, an anti-PD-1 antibody, in advanced solid tumors. Clin Cancer Res. 27:3620–3629. 2021. View Article : Google Scholar : PubMed/NCBI

51 

Kelly CM, Qin LX, Whiting KA, Richards AL, Avutu V, Chan JE, Chi P, Dickson MA, Gounder MM, Keohan ML, et al: A phase II study of epacadostat and pembrolizumab in patients with advanced sarcoma. Clin Cancer Res. 29:2043–2051. 2023. View Article : Google Scholar : PubMed/NCBI

52 

Zakharia Y, McWilliams RR, Rixe O, Drabick J, Shaheen MF, Grossmann KF, Kolhe R, Pacholczyk R, Sadek R, Tennant LL, et al: Phase II trial of the IDO pathway inhibitor indoximod plus pembrolizumab for the treatment of patients with advanced melanoma. J Immunother Cancer. 9:e0020572021. View Article : Google Scholar : PubMed/NCBI

53 

Lynch TJ, Bondarenko I, Luft A, Serwatowski P, Barlesi F, Chacko R, Sebastian M, Neal J, Lu H, Cuillerot JM and Reck M: Ipilimumab in combination with paclitaxel and carboplatin as first-line treatment in stage IIIB/IV non-small-cell lung cancer: Results from a randomized, double-blind, multicenter phase II study. J Clin Oncol. 30:2046–2054. 2012. View Article : Google Scholar : PubMed/NCBI

54 

Wan MT and Ming ME: Nivolumab versus ipilimumab in the treatment of advanced melanoma: A critical appraisal: ORIGINAL ARTICLE. Wolchok JD, Chiarion-Sileni V, Gonzalez R, et al: Overall survival with combined nivolumab and ipilimumab in advanced melanoma. N Engl J Med 2017; 377: 1345-1356. Br J Dermatol. 179:296–300. 2018.PubMed/NCBI

55 

Hellmann MD, Ciuleanu TE, Pluzanski A, Lee JS, Otterson GA, Audigier-Valette C, Minenza E, Linardou H, Burgers S, Salman P, et al: Nivolumab plus ipilimumab in lung cancer with a high tumor mutational burden. N Engl J Med. 378:2093–2104. 2018. View Article : Google Scholar : PubMed/NCBI

56 

Tannir NM, Signoretti S, Choueiri TK, McDermott DF, Motzer RJ, Flaifel A, Pignon JC, Ficial M, Frontera OA, George S, et al: Efficacy and safety of nivolumab plus ipilimumab versus sunitinib in first-line treatment of patients with advanced sarcomatoid renal cell carcinoma. Clin Cancer Res. 27:78–86. 2021. View Article : Google Scholar : PubMed/NCBI

57 

Rini BI, Powles T, Atkins MB, Escudier B, McDermott DF, Suarez C, Bracarda S, Stadler WM, Donskov F, Lee JL, et al: Atezolizumab plus bevacizumab versus sunitinib in patients with previously untreated metastatic renal cell carcinoma (IMmotion151): A multicentre, open-label, phase 3, randomised controlled trial. Lancet. 393:2404–2415. 2019. View Article : Google Scholar : PubMed/NCBI

58 

Garon EB, Hellmann MD, Rizvi NA, Carcereny E, Leighl NB, Ahn MJ, Eder JP, Balmanoukian AS, Aggarwal C, Horn L, et al: Five-year overall survival for patients with advanced non-small-cell lung cancer treated with pembrolizumab: Results from the phase I KEYNOTE-001 study. J Clin Oncol. 37:2518–2527. 2019. View Article : Google Scholar : PubMed/NCBI

59 

Yuan L, Jia GD, Lv XF, Xie SY, Guo SS, Lin DF, Liu LT, Luo DH, Li YF, Deng SW, et al: Camrelizumab combined with apatinib in patients with first-line platinum-resistant or PD-1 inhibitor resistant recurrent/metastatic nasopharyngeal carcinoma: A single-arm, phase 2 trial. Nat Commun. 14:48932023. View Article : Google Scholar : PubMed/NCBI

60 

Liu Y, Song Y, Zuo S, Zhang X, Liu H, Wang J, Wang J, Tang Y, Zheng W, Ying Z, et al: Antitumor activity and safety of camrelizumab combined with apatinib in patients with relapsed or refractory peripheral T-cell lymphoma: An open-label, multicenter, phase II study. Front Immunol. 14:11281722023. View Article : Google Scholar : PubMed/NCBI

61 

Zhao Y, Ma Y, Fan Y, Zhou J, Yang N, Yu Q, Zhuang W, Song W, Wang ZM, Li B, et al: A multicenter, open-label phase Ib/II study of cadonilimab (anti PD-1 and CTLA-4 bispecific antibody) monotherapy in previously treated advanced non-small-cell lung cancer (AK104-202 study). Lung Cancer. 184:1073552023. View Article : Google Scholar : PubMed/NCBI

62 

Shui L, Yang X, Li J, Yi C, Sun Q and Zhu H: Gut microbiome as a potential factor for modulating resistance to cancer immunotherapy. Front Immunol. 10:29892020. View Article : Google Scholar : PubMed/NCBI

63 

Park EM, Chelvanambi M, Bhutiani N, Kroemer G, Zitvogel L and Wargo JA: Targeting the gut and tumor microbiota in cancer. Nat Med. 28:690–703. 2022. View Article : Google Scholar : PubMed/NCBI

64 

Zhou Y, Liu Z and Chen T: Gut microbiota: A promising milestone in enhancing the efficacy of PD1/PD-L1 blockade therapy. Front Oncol. 12:8473502022. View Article : Google Scholar : PubMed/NCBI

65 

Vétizou M, Pitt JM, Daillère R, Lepage P, Waldschmitt N, Flament C, Rusakiewicz S, Routy B, Roberti MP, Duong CP, et al: Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science. 350:1079–1084. 2015. View Article : Google Scholar : PubMed/NCBI

66 

Huang C, Li M, Liu B, Zhu H, Dai Q, Fan X, Mehta K, Huang C, Neupane P, Wang F, et al: Relating gut microbiome and its modulating factors to immunotherapy in solid tumors: A systematic review. Front Oncol. 11:6421102021. View Article : Google Scholar : PubMed/NCBI

67 

Routy B, Le Chatelier E, Derosa L, Duong CPM, Alou MT, Daillère R, Fluckiger A, Messaoudene M, Rauber C, Roberti MP, et al: Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science. 359:91–97. 2018. View Article : Google Scholar : PubMed/NCBI

68 

Grenda A, Iwan E, Chmielewska I, Krawczyk P, Giza A, Bomba A, Frąk M, Rolska A, Szczyrek M, Kieszko R, et al: Presence of Akkermansiaceae in gut microbiome and immunotherapy effectiveness in patients with advanced non-small cell lung cancer. AMB Express. 12:862022. View Article : Google Scholar : PubMed/NCBI

69 

Grenda A, Iwan E, Krawczyk P, Frąk M, Chmielewska I, Bomba A, Giza A, Rolska-Kopińska A, Szczyrek M, Kieszko R, et al: Attempting to identify bacterial allies in immunotherapy of NSCLC patients. Cancers (Basel). 14:62502022. View Article : Google Scholar : PubMed/NCBI

70 

Newsome RC, Gharaibeh RZ, Pierce CM, da Silva WV, Paul S, Hogue SR, Yu Q, Antonia S, Conejo-Garcia JR, Robinson LA and Jobin C: Interaction of bacterial genera associated with therapeutic response to immune checkpoint PD-1 blockade in a United States cohort. Genome Med. 14:352022. View Article : Google Scholar : PubMed/NCBI

71 

Lee KA, Thomas AM, Bolte LA, Björk JR, de Ruijter LK, Armanini F, Asnicar F, Blanco-Miguez A, Board R, Calbet-Llopart N, et al: Cross-cohort gut microbiome associations with immune checkpoint inhibitor response in advanced melanoma. Nat Med. 28:535–544. 2022. View Article : Google Scholar : PubMed/NCBI

72 

Cani PD, Depommier C, Derrien M, Everard A and de Vos WM: Akkermansia muciniphila: paradigm for next-generation beneficial microorganisms. Nat Rev Gastroenterol Hepatol. 19:625–637. 2022. View Article : Google Scholar : PubMed/NCBI

73 

Xu X, Lv J, Guo F, Li J, Jia Y, Jiang D, Wang N, Zhang C, Kong L, Liu Y, et al: Gut microbiome influences the efficacy of PD-1 antibody immunotherapy on MSS-type colorectal cancer via metabolic pathway. Front Microbiol. 11:8142020. View Article : Google Scholar : PubMed/NCBI

74 

Peiffer LB, White JR, Jones CB, Slottke RE, Ernst SE, Moran AE, Graff JN and Sfanos KS: Composition of gastrointestinal microbiota in association with treatment response in individuals with metastatic castrate resistant prostate cancer progressing on enzalutamide and initiating treatment with anti-PD-1 (pembrolizumab). Neoplasia. 32:1008222022. View Article : Google Scholar : PubMed/NCBI

75 

Gopalakrishnan V, Spencer CN, Nezi L, Reuben A, Andrews MC, Karpinets TV, Prieto PA, Vicente D, Hoffman K, Wei SC, et al: Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science. 359:97–103. 2018. View Article : Google Scholar : PubMed/NCBI

76 

Matson V, Fessler J, Bao R, Chongsuwat T, Zha Y, Alegre ML, Luke JJ and Gajewski TF: The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science. 359:104–108. 2018. View Article : Google Scholar : PubMed/NCBI

77 

Hakozaki T, Richard C, Elkrief A, Hosomi Y, Benlaïfaoui M, Mimpen I, Terrisse S, Derosa L, Zitvogel L, Routy B and Okuma Y: The gut microbiome associates with immune checkpoint inhibition outcomes in patients with advanced non-small cell lung cancer. Cancer Immunol Res. 8:1243–1250. 2020. View Article : Google Scholar : PubMed/NCBI

78 

Jin Y, Dong H, Xia L, Yang Y, Zhu Y, Shen Y, Zheng H, Yao C, Wang Y and Lu S: The diversity of gut microbiome is associated with favorable responses to anti-programmed death 1 immunotherapy in Chinese patients with NSCLC. J Thorac Oncol. 14:1378–1389. 2019. View Article : Google Scholar : PubMed/NCBI

79 

Mao J, Wang D, Long J, Yang X, Lin J, Song Y, Xie F, Xun Z, Wang Y, Wang Y, et al: Gut microbiome is associated with the clinical response to anti-PD-1 based immunotherapy in hepatobiliary cancers. J Immunother Cancer. 9:e0033342021. View Article : Google Scholar : PubMed/NCBI

80 

Shen YC, Lee PC, Kuo YL, Wu WK, Chen CC, Lei CH, Yeh CP, Hsu C, Hsu CH, Lin ZZ, et al: An exploratory study for the association of gut microbiome with efficacy of immune checkpoint inhibitor in patients with hepatocellular carcinoma. J Hepatocell Carcinoma. 8:809–822. 2021. View Article : Google Scholar : PubMed/NCBI

81 

Wang F, He MM, Yao YC, Zhao X, Wang ZQ, Jin Y, Luo HY, Li JB, Wang FH, Qiu MZ, et al: Regorafenib plus toripalimab in patients with metastatic colorectal cancer: A phase Ib/II clinical trial and gut microbiome analysis. Cell Rep Med. 2:1003832021. View Article : Google Scholar : PubMed/NCBI

82 

Wu YY, Lin CW, Cheng KS, Lin C, Wang YM, Lin IT, Chou YH and Hsu PN: Increased programmed death-ligand-1 expression in human gastric epithelial cells in Helicobacter pylori infection. Clin Exp Immunol. 161:551–559. 2010. View Article : Google Scholar : PubMed/NCBI

83 

Park JS, Gazzaniga FS, Wu M, Luthens AK, Gillis J, Zheng W, LaFleur MW, Johnson SB, Morad G, Park EM, et al: Targeting PD-L2-RGMb overcomes microbiome-related immunotherapy resistance. Nature. 617:377–385. 2023. View Article : Google Scholar : PubMed/NCBI

84 

Peng Z, Cheng S, Kou Y, Wang Z, Jin R, Hu H, Zhang X, Gong JF, Li J, Lu M, et al: The gut microbiome is associated with clinical response to anti-PD-1/PD-L1 immunotherapy in gastrointestinal cancer. Cancer Immunol Res. 8:1251–1261. 2020. View Article : Google Scholar : PubMed/NCBI

85 

Nomura M, Nagatomo R, Doi K, Shimizu J, Baba K, Saito T, Matsumoto S, Inoue K and Muto M: Association of short-chain fatty acids in the gut microbiome with clinical response to treatment with nivolumab or pembrolizumab in patients with solid cancer tumors. JAMA Netw Open. 3:e2028952020. View Article : Google Scholar : PubMed/NCBI

86 

He Y, Fu L, Li Y, Wang W, Gong M, Zhang J, Dong X, Huang J, Wang Q, Mackay CR, et al: Gut microbial metabolites facilitate anticancer therapy efficacy by modulating cytotoxic CD8+ T cell immunity. Cell Metab. 33:988–1000.e7. 2021. View Article : Google Scholar : PubMed/NCBI

87 

Coutzac C, Jouniaux JM, Paci A, Schmidt J, Mallardo D, Seck A, Asvatourian V, Cassard L, Saulnier P, Lacroix L, et al: Systemic short chain fatty acids limit antitumor effect of CTLA-4 blockade in hosts with cancer. Nat Commun. 11:21682020. View Article : Google Scholar : PubMed/NCBI

88 

Lee PC, Wu CJ, Hung YW, Lee CJ, Chi CT, Lee IC, Yu-Lun K, Chou SH, Luo JC, Hou MC and Huang YH: Gut microbiota and metabolites associate with outcomes of immune checkpoint inhibitor-treated unresectable hepatocellular carcinoma. J Immunother Cancer. 10:e0047792022. View Article : Google Scholar : PubMed/NCBI

89 

Jiang SS, Xie YL, Xiao XY, Kang ZR, Lin XL, Zhang L, Li CS, Qian Y, Xu PP, Leng XX, et al: Fusobacterium nucleatum-derived succinic acid induces tumor resistance to immunotherapy in colorectal cancer. Cell Host Microbe. 31:781–797.e9. 2023. View Article : Google Scholar : PubMed/NCBI

90 

Yang M, Wang Y, Yuan M, Tao M, Kong C, Li H, Tong J, Zhu H and Yan X: Antibiotic administration shortly before or after immunotherapy initiation is correlated with poor prognosis in solid cancer patients: An up-to-date systematic review and meta-analysis. Int Immunopharmacol. 88:1068762020. View Article : Google Scholar : PubMed/NCBI

91 

Tinsley N, Zhou C, Tan G, Rack S, Lorigan P, Blackhall F, Krebs M, Carter L, Thistlethwaite F, Graham D and Cook N: Cumulative antibiotic use significantly decreases efficacy of checkpoint inhibitors in patients with advanced cancer. Oncologist. 25:55–63. 2020. View Article : Google Scholar : PubMed/NCBI

92 

Hakozaki T, Okuma Y, Omori M and Hosomi Y: Impact of prior antibiotic use on the efficacy of nivolumab for non-small cell lung cancer. Oncol Lett. 17:2946–2952. 2019.PubMed/NCBI

93 

Derosa L, Hellmann MD, Spaziano M, Halpenny D, Fidelle M, Rizvi H, Long N, Plodkowski AJ, Arbour KC, Chaft JE, et al: Negative association of antibiotics on clinical activity of immune checkpoint inhibitors in patients with advanced renal cell and non-small-cell lung cancer. Ann Oncol. 29:1437–1444. 2018. View Article : Google Scholar : PubMed/NCBI

94 

Kim J and Lee HK: The role of gut microbiota in modulating tumor growth and anticancer agent efficacy. Mol Cells. 44:356–362. 2021. View Article : Google Scholar : PubMed/NCBI

95 

Son MY and Cho HS: Anticancer effects of gut microbiota-derived short-chain fatty acids in cancers. J Microbiol Biotechnol. 33:849–856. 2023. View Article : Google Scholar : PubMed/NCBI

96 

Li T, Han L, Ma S, Lin W, Ba X, Yan J, Huang Y, Tu S and Qin K: Interaction of gut microbiota with the tumor microenvironment: A new strategy for antitumor treatment and traditional Chinese medicine in colorectal cancer. Front Mol Biosci. 10:11403252023. View Article : Google Scholar : PubMed/NCBI

97 

Andrews MC, Duong CPM, Gopalakrishnan V, Iebba V, Chen WS, Derosa L, Khan MAW, Cogdill AP, White MG, Wong MC, et al: Gut microbiota signatures are associated with toxicity to combined CTLA-4 and PD-1 blockade. Nat Med. 27:1432–1441. 2021. View Article : Google Scholar : PubMed/NCBI

98 

Dubin K, Callahan MK, Ren B, Khanin R, Viale A, Ling L, No D, Gobourne A, Littmann E, Huttenhower C, et al: Intestinal microbiome analyses identify melanoma patients at risk for checkpoint-blockade-induced colitis. Nat Commun. 7:103912016. View Article : Google Scholar : PubMed/NCBI

99 

Liu T, Xiong Q, Li L and Hu Y: Intestinal microbiota predicts lung cancer patients at risk of immune-related diarrhea. Immunotherapy. 11:385–396. 2019. View Article : Google Scholar : PubMed/NCBI

100 

Sivan A, Corrales L, Hubert N, Williams JB, Aquino-Michaels K, Earley ZM, Benyamin FW, Lei YM, Jabri B, Alegre ML, et al: Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science. 350:1084–1089. 2015. View Article : Google Scholar : PubMed/NCBI

101 

Tomita Y, Goto Y, Sakata S, Imamura K, Minemura A, Oka K, Hayashi A, Jodai T, Akaike K, Anai M, et al: Clostridium butyricum therapy restores the decreased efficacy of immune checkpoint blockade in lung cancer patients receiving proton pump inhibitors. Oncoimmunology. 11:20810102022. View Article : Google Scholar : PubMed/NCBI

102 

Dizman N, Meza L, Bergerot P, Alcantara M, Dorff T, Lyou Y, Frankel P, Cui Y, Mira V, Llamas M, et al: Nivolumab plus ipilimumab with or without live bacterial supplementation in metastatic renal cell carcinoma: A randomized phase 1 trial. Nat Med. 28:704–712. 2022. View Article : Google Scholar : PubMed/NCBI

103 

Tomita Y, Ikeda T, Sakata S, Saruwatari K, Sato R, Iyama S, Jodai T, Akaike K, Ishizuka S, Saeki S and Sakagami T: Association of probiotic Clostridium butyricum therapy with survival and response to immune checkpoint blockade in patients with lung cancer. Cancer Immunol Res. 8:1236–1242. 2020. View Article : Google Scholar : PubMed/NCBI

104 

Wang F, Yin Q, Chen L and Davis MM: Bifidobacterium can mitigate intestinal immunopathology in the context of CTLA-4 blockade. Proc Natl Acad Sci USA. 115:157–161. 2018. View Article : Google Scholar : PubMed/NCBI

105 

Spencer CN, McQuade JL, Gopalakrishnan V, McCulloch JA, Vetizou M, Cogdill AP, Khan MAW, Zhang X, White MG, Peterson CB, et al: Dietary fiber and probiotics influence the gut microbiome and melanoma immunotherapy response. Science. 374:1632–1640. 2021. View Article : Google Scholar : PubMed/NCBI

106 

Gao G, Shen S, Zhang T, Zhang J, Huang S, Sun Z and Zhang H: Lacticaseibacillus rhamnosus Probio-M9 enhanced the antitumor response to anti-PD-1 therapy by modulating intestinal metabolites. EBioMedicine. 91:1045332023. View Article : Google Scholar : PubMed/NCBI

107 

Huang J, Zheng X, Kang W, Hao H, Mao Y, Zhang H, Chen Y, Tan Y, He Y, Zhao W and Yin Y: Metagenomic and metabolomic analyses reveal synergistic effects of fecal microbiota transplantation and anti-PD-1 therapy on treating colorectal cancer. Front Immunol. 13:8749222022. View Article : Google Scholar : PubMed/NCBI

108 

Shaikh FY, Gills JJ, Mohammad F, White JR, Stevens CM, Ding H, Fu J, Tam A, Blosser RL, Domingue JC, et al: Murine fecal microbiota transfer models selectively colonize human microbes and reveal transcriptional programs associated with response to neoadjuvant checkpoint inhibitors. Cancer Immunol Immunother. 71:2405–2420. 2022. View Article : Google Scholar : PubMed/NCBI

109 

Baruch EN, Youngster I, Ben-Betzalel G, Ortenberg R, Lahat A, Katz L, Adler K, Dick-Necula D, Raskin S, Bloch N, et al: Fecal microbiota transplant promotes response in immunotherapy-refractory melanoma patients. Science. 371:602–609. 2021. View Article : Google Scholar : PubMed/NCBI

110 

Davar D, Dzutsev AK, McCulloch JA, Rodrigues RR, Chauvin JM, Morrison RM, Deblasio RN, Menna C, Ding Q, Pagliano O, et al: Fecal microbiota transplant overcomes resistance to anti-PD-1 therapy in melanoma patients. Science. 371:595–602. 2021. View Article : Google Scholar : PubMed/NCBI

111 

Wang Y, Wiesnoski DH, Helmink BA, Gopalakrishnan V, Choi K, DuPont HL, Jiang ZD, Abu-Sbeih H, Sanchez CA, Chang CC, et al: Fecal microbiota transplantation for refractory immune checkpoint inhibitor-associated colitis. Nat Med. 24:1804–1808. 2018. View Article : Google Scholar : PubMed/NCBI

112 

Fasanello MK, Robillard KT, Boland PM, Bain AJ and Kanehira K: Use of fecal microbial transplantation for immune checkpoint inhibitor colitis. ACG Case Rep J. 7:e003602020. View Article : Google Scholar : PubMed/NCBI

113 

Koo H and Morrow CD: Incongruence between dominant commensal donor microbes in recipient feces post fecal transplant and response to anti-PD-1 immunotherapy. BMC Microbiol. 21:2512021. View Article : Google Scholar : PubMed/NCBI

114 

Jamal R, Messaoudene M, de Figuieredo M and Routy B: Future indications and clinical management for fecal microbiota transplantation (FMT) in immuno-oncology. Semin Immunol. 67:1017542023. View Article : Google Scholar : PubMed/NCBI

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Jiang H and Zhang Q: Gut microbiota influences the efficiency of immune checkpoint inhibitors by modulating the immune system (Review). Oncol Lett 27: 87, 2024.
APA
Jiang, H., & Zhang, Q. (2024). Gut microbiota influences the efficiency of immune checkpoint inhibitors by modulating the immune system (Review). Oncology Letters, 27, 87. https://doi.org/10.3892/ol.2024.14221
MLA
Jiang, H., Zhang, Q."Gut microbiota influences the efficiency of immune checkpoint inhibitors by modulating the immune system (Review)". Oncology Letters 27.2 (2024): 87.
Chicago
Jiang, H., Zhang, Q."Gut microbiota influences the efficiency of immune checkpoint inhibitors by modulating the immune system (Review)". Oncology Letters 27, no. 2 (2024): 87. https://doi.org/10.3892/ol.2024.14221
Copy and paste a formatted citation
x
Spandidos Publications style
Jiang H and Zhang Q: Gut microbiota influences the efficiency of immune checkpoint inhibitors by modulating the immune system (Review). Oncol Lett 27: 87, 2024.
APA
Jiang, H., & Zhang, Q. (2024). Gut microbiota influences the efficiency of immune checkpoint inhibitors by modulating the immune system (Review). Oncology Letters, 27, 87. https://doi.org/10.3892/ol.2024.14221
MLA
Jiang, H., Zhang, Q."Gut microbiota influences the efficiency of immune checkpoint inhibitors by modulating the immune system (Review)". Oncology Letters 27.2 (2024): 87.
Chicago
Jiang, H., Zhang, Q."Gut microbiota influences the efficiency of immune checkpoint inhibitors by modulating the immune system (Review)". Oncology Letters 27, no. 2 (2024): 87. https://doi.org/10.3892/ol.2024.14221
Follow us
  • Twitter
  • LinkedIn
  • Facebook
About
  • Spandidos Publications
  • Careers
  • Cookie Policy
  • Privacy Policy
How can we help?
  • Help
  • Live Chat
  • Contact
  • Email to our Support Team