Dual contribution of the gut microbiome to immunotherapy efficacy and toxicity: supportive care implications and recommendations.
Adverse events
Efficacy
Gut microbiome
Immune checkpoint inhibitors
Immunotherapy
Supportive cancer care
Toxicity
Journal
Supportive care in cancer : official journal of the Multinational Association of Supportive Care in Cancer
ISSN: 1433-7339
Titre abrégé: Support Care Cancer
Pays: Germany
ID NLM: 9302957
Informations de publication
Date de publication:
Aug 2022
Aug 2022
Historique:
received:
02
09
2021
accepted:
27
02
2022
pubmed:
11
3
2022
medline:
24
6
2022
entrez:
10
3
2022
Statut:
ppublish
Résumé
The efficacy of immune checkpoint inhibitors (immunotherapy) is increasingly recognized to be linked to the composition the gut microbiome. Given the high rates of resistance, interventions targeting the gut microbiome are now being investigated for its ability to improve the efficacy of immunotherapy. In light of recently published data demonstrating a strong correlation between the efficacy and toxicity of immunotherapy, there is a risk that efforts to enhance immunotherapy efficacy may be undermined by increases in immune-related adverse events (IrAEs) This is particularly important for microbial interventions aimed at increasing immunotherapy efficacy, with many microbes implicated in tumour response also linked to IrAEs, especially colitis. IrAEs have a profound impact on patient quality of life, causing physical, psychosocial, and financial distress. Here, we outline strategies at the discovery, translational, and clinical research phases to ensure the impact of augmenting immunotherapy efficacy is approached in a manner that considers adverse implications. Adopting these strategies will ensure that our ongoing efforts to overcome immunotherapy resistance are not impacted by unacceptable toxicity.
Identifiants
pubmed: 35266052
doi: 10.1007/s00520-022-06948-0
pii: 10.1007/s00520-022-06948-0
pmc: PMC9213341
doi:
Substances chimiques
Immunologic Factors
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
6369-6373Informations de copyright
© 2022. The Author(s).
Références
Waldman AD, Fritz JM, Lenardo MJ (2020) A guide to cancer immunotherapy: from T cell basic science to clinical practice. Nat Rev Immunol 20:651–668. https://doi.org/10.1038/s41577-020-0306-5
doi: 10.1038/s41577-020-0306-5
pubmed: 32433532
pmcid: 7238960
Ralli M et al (2020) Immunotherapy in the treatment of metastatic melanoma: current knowledge and future directions. J Immunol Res 2020:9235638. https://doi.org/10.1155/2020/9235638
doi: 10.1155/2020/9235638
pubmed: 32671117
pmcid: 7338969
Sgambato A et al (2016) Anti PD-1 and PDL-1 immunotherapy in the treatment of advanced non- small cell lung cancer (NSCLC): a review on toxicity profile and its management. Curr Drug Saf 11:62–68. https://doi.org/10.2174/1574886311207040289
doi: 10.2174/1574886311207040289
pubmed: 26412670
Indini A, Rijavec E, Grossi F (2021) Circulating biomarkers of response and toxicity of immunotherapy in advanced non-small cell lung cancer (NSCLC): a comprehensive review. Cancers (Basel) 13:1794. https://doi.org/10.3390/cancers13081794
doi: 10.3390/cancers13081794
Hegde PS, Chen DS (2020) Top 10 challenges in cancer immunotherapy. Immunity 52:17–35. https://doi.org/10.1016/j.immuni.2019.12.011
doi: 10.1016/j.immuni.2019.12.011
pubmed: 31940268
Zheng D, Liwinski T, Elinav E (2020) Interaction between microbiota and immunity in health and disease. Cell Res 30:492–506. https://doi.org/10.1038/s41422-020-0332-7
doi: 10.1038/s41422-020-0332-7
pubmed: 32433595
pmcid: 7264227
Ruff WE, Greiling TM, Kriegel MA (2020) Host-microbiota interactions in immune-mediated diseases. Nat Rev Microbiol 18:521–538. https://doi.org/10.1038/s41579-020-0367-2
doi: 10.1038/s41579-020-0367-2
pubmed: 32457482
Limeta A, Ji B, Levin M, Gatto F, Nielsen J (2020) Meta-analysis of the gut microbiota in predicting response to cancer immunotherapy in metastatic melanoma. JCI Insight 5:e140940. https://doi.org/10.1172/jci.insight.140940
doi: 10.1172/jci.insight.140940
pmcid: 7714408
Huang XZ et al (2019) Antibiotic use and the efficacy of immune checkpoint inhibitors in cancer patients: a pooled analysis of 2740 cancer patients. Oncoimmunology 8:e1665973. https://doi.org/10.1080/2162402X.2019.1665973
doi: 10.1080/2162402X.2019.1665973
pubmed: 31741763
pmcid: 6844307
Daillere R et al (2020) Trial watch: the gut microbiota as a tool to boost the clinical efficacy of anticancer immunotherapy. Oncoimmunology 9:1774298. https://doi.org/10.1080/2162402X.2020.1774298
doi: 10.1080/2162402X.2020.1774298
pubmed: 32934879
pmcid: 7466862
Fillon M (2021) Fecal microbiota transplants may aid melanoma immunotherapy resistance. CA Cancer J Clin 71:285–286. https://doi.org/10.3322/caac.21676
doi: 10.3322/caac.21676
pubmed: 34101828
Davar D et al (2021) Fecal microbiota transplant overcomes resistance to anti-PD-1 therapy in melanoma patients. Science 371:595–602. https://doi.org/10.1126/science.abf3363
doi: 10.1126/science.abf3363
pubmed: 33542131
pmcid: 8097968
Baruch EN et al (2021) Fecal microbiota transplant promotes response in immunotherapy-refractory melanoma patients. Science 371:602–609. https://doi.org/10.1126/science.abb5920
doi: 10.1126/science.abb5920
pubmed: 33303685
Uribe-Herranz M et al (2018) Gut microbiota modulates adoptive cell therapy via CD8alpha dendritic cells and IL-12. JCI Insight 3:e94952. https://doi.org/10.1172/jci.insight.94952
doi: 10.1172/jci.insight.94952
pmcid: 5916241
Sivan A et al (2015) Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science 350:1084–1089. https://doi.org/10.1126/science.aac4255
doi: 10.1126/science.aac4255
pubmed: 26541606
pmcid: 4873287
Iida N et al (2013) Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science 342:967–970. https://doi.org/10.1126/science.1240527
doi: 10.1126/science.1240527
pubmed: 24264989
pmcid: 6709532
Bowen J et al (2019) The pathogenesis of mucositis: updated perspectives and emerging targets. Support Care Cancer 27:4023–4033. https://doi.org/10.1007/s00520-019-04893-z
doi: 10.1007/s00520-019-04893-z
pubmed: 31286231
Secombe KR, Coller JK, Gibson RJ, Wardill HR, Bowen JM (2019) The bidirectional interaction of the gut microbiome and the innate immune system: implications for chemotherapy-induced gastrointestinal toxicity. Int J Cancer 144:2365–2376. https://doi.org/10.1002/ijc.31836
doi: 10.1002/ijc.31836
pubmed: 30155890
Rapoport BL, Anderson R, Cooksley T, Johnson DB (2020) MASCC 2020 recommendations for the management of immune-related adverse events of patients undergoing treatment with immune checkpoint inhibitors. Support Care Cancer 28:6107–6110. https://doi.org/10.1007/s00520-020-05727-z
doi: 10.1007/s00520-020-05727-z
pubmed: 32886228
Chhabra N, Kennedy J (2021) A review of cancer immunotherapy toxicity: immune checkpoint inhibitors. J Med Toxicol. https://doi.org/10.1007/s13181-021-00833-8
doi: 10.1007/s13181-021-00833-8
pubmed: 33826117
pmcid: 8021214
Chhabra N, Kennedy J (2021) A review of cancer immunotherapy toxicity II: adoptive cellular therapies, kinase inhibitors, monoclonal antibodies, and oncolytic viruses. J Med Toxicol. https://doi.org/10.1007/s13181-021-00835-6
doi: 10.1007/s13181-021-00835-6
pubmed: 33826117
pmcid: 8021214
Kennedy LB, Salama AKS (2020) A review of cancer immunotherapy toxicity. CA Cancer J Clin 70:86–104. https://doi.org/10.3322/caac.21596
doi: 10.3322/caac.21596
pubmed: 31944278
Andrews MC et al (2021) Gut microbiota signatures are associated with toxicity to combined CTLA-4 and PD-1 blockade. Nat Med. https://doi.org/10.1038/s41591-021-01406-6
doi: 10.1038/s41591-021-01406-6
pubmed: 34239137
Chaput N et al (2019) Baseline gut microbiota predicts clinical response and colitis in metastatic melanoma patients treated with ipilimumab. Ann Oncol 30:2012. https://doi.org/10.1093/annonc/mdz224
doi: 10.1093/annonc/mdz224
pubmed: 31408090
Roviello G, Iannone LF, Bersanelli M, Mini E, Catalano M (2021) The gut microbiome and efficacy of cancer immunotherapy. Pharmacol Ther 231:107973. https://doi.org/10.1016/j.pharmthera.2021.107973
doi: 10.1016/j.pharmthera.2021.107973
pubmed: 34453999
Zhou X et al (2020) Are immune-related adverse events associated with the efficacy of immune checkpoint inhibitors in patients with cancer? A systematic review and meta-analysis. BMC Med 18:87. https://doi.org/10.1186/s12916-020-01549-2
doi: 10.1186/s12916-020-01549-2
pubmed: 32306958
pmcid: 7169020
Kainis I et al (2018) Erlotinib-associated rash in advanced non-small cell lung cancer: relation to clinicopathological characteristics, treatment response, and survival. Oncol Res 26:59–69. https://doi.org/10.3727/096504017X14913452320194
doi: 10.3727/096504017X14913452320194
pubmed: 28390118
pmcid: 7844560
Sonnenblick A et al (2016) Lapatinib-related rash and breast cancer outcome in the ALTTO phase III randomized trial. J Natl Cancer Inst 108:djw037. https://doi.org/10.1093/jnci/djw037
doi: 10.1093/jnci/djw037
pubmed: 27098150
pmcid: 5017935
Kudo K et al (2016) Development of a skin rash within the first week and the therapeutic effect in afatinib monotherapy for EGFR-mutant non-small cell lung cancer (NSCLC): Okayama Lung Cancer Study Group experience. Cancer Chemother Pharmacol 77:1005–1009. https://doi.org/10.1007/s00280-015-2910-9
doi: 10.1007/s00280-015-2910-9
pubmed: 27029623
Fujii H et al (2016) Relationship between the incidence of hypomagnesemia and acneiform rash and the therapeutic effect of anti-EGFR monoclonal antibody in patients with metastatic colorectal cancer. Gan To Kagaku Ryoho 43:229–233
pubmed: 27067688
Gibson RJ et al (2018) Selective MMP inhibition, using AZD3342, to reduce gastrointestinal toxicity and enhance chemoefficacy in a rat model. Chemotherapy 63:284–292. https://doi.org/10.1159/000495470
doi: 10.1159/000495470
pubmed: 30731451
Selby P, Velikova G (2018) Taking patient reported outcomes centre stage in cancer research - why has it taken so long? Res Involv Engagem 4:25. https://doi.org/10.1186/s40900-018-0109-z
doi: 10.1186/s40900-018-0109-z
pubmed: 30038798
pmcid: 6052546
Basch E et al (2006) Patient versus clinician symptom reporting using the National Cancer Institute Common Terminology Criteria for Adverse Events: results of a questionnaire-based study. Lancet Oncol 7:903–909. https://doi.org/10.1016/S1470-2045(06)70910-X
doi: 10.1016/S1470-2045(06)70910-X
pubmed: 17081915
Cammarota G et al (2020) Gut microbiome, big data and machine learning to promote precision medicine for cancer. Nat Rev Gastroenterol Hepatol 17:635–648. https://doi.org/10.1038/s41575-020-0327-3
doi: 10.1038/s41575-020-0327-3
pubmed: 32647386
Forster SC et al (2019) A human gut bacterial genome and culture collection for improved metagenomic analyses. Nat Biotechnol 37:186–192. https://doi.org/10.1038/s41587-018-0009-7
doi: 10.1038/s41587-018-0009-7
pubmed: 30718869
pmcid: 6785715