Gut microbiota and immunotherapy of renal cell carcinoma

References

• Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012;489(7415):220. doi:10.1038/NATURE11550.
   PubMed Web of Science ®Google Scholar
• Ianiro G, Bruno G, Lopetuso L, Beghella F, Laterza L, D’Aversa F, Gigante G, Cammarota G, Gasbarrini A. Role of yeasts in healthy and impaired gut microbiota: the gut mycome. Curr Pharm Des. 2014;20(28):4565–10. doi:10.2174/13816128113196660723.
   PubMed Web of Science ®Google Scholar
• Ianiro G, Iorio A, Porcari S, Masucci L, Sanguinetti M, Perno CF, Gasbarrini A, Putignani L, Cammarota G. How the gut parasitome affects human health. Therap Adv Gastroenterol. 2022;15:175628482210915. doi:https://doi.org/10.1177/17562848221091524.
   Web of Science ®Google Scholar
• De Siena M, Laterza L, Matteo MV, Mignini I, Schepis T, Rizzatti G, Ianiro G, Rinninella E, Cintoni M, Gasbarrini A, et al. Gut and reproductive tract microbiota adaptation during pregnancy: new insights for pregnancy-related complications and therapy. Microorganisms. 2021;9(3):1–15. doi:10.3390/MICROORGANISMS9030473.
   Web of Science ®Google Scholar
• Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto J-M, et al. Enterotypes of the human gut microbiome. Nature. 2011;473(7346):174. doi:10.1038/NATURE09944.
   PubMed Web of Science ®Google Scholar
• Ianiro G, Molina-Infante J, Gasbarrini A. Gastric microbiota. Helicobacter. 2015;20(Suppl 1):68–71. doi:10.1111/HEL.12260.
   PubMedGoogle Scholar
• Lopetuso LR, Severgnini M, Pecere S, Ponziani FR, Boskoski I, Larghi A, Quaranta G, Masucci L, Ianiro G, Camboni T, et al. Esophageal microbiome signature in patients with Barrett’s esophagus and esophageal adenocarcinoma. PloS One. 2020;15(5):e0231789. doi:10.1371/JOURNAL.PONE.0231789.
   PubMed Web of Science ®Google Scholar
• Viggiano D, Ianiro G, Vanella G, Bibbò S, Bruno G, Simeone G, Mele G. Gut barrier in health and disease: focus on childhood. Eur Rev Med Pharmacol Sci. 2015;19:1077–85.
   PubMed Web of Science ®Google Scholar
• Cardinale V, Capurso G, Ianiro G, Gasbarrini A, Arcidiacono PG, Alvaro D. Intestinal permeability changes with bacterial translocation as key events modulating systemic host immune response to SARS-CoV-2: a working hypothesis. Digestive Liver Dis. 2020;52(12):1383. doi:10.1016/J.DLD.2020.09.009.
   Web of Science ®Google Scholar
• Cianci R, Franza L, Schinzari G, Rossi E, Ianiro G, Tortora G, Gasbarrini A, Gambassi G, Cammarota G. The interplay between immunity and microbiota at intestinal immunological niche: the case of cancer. Int J Mol Sci. 2019;20(3):501. doi:https://doi.org/10.3390/IJMS20030501.
   PubMed Web of Science ®Google Scholar
• Bibbò S, Lopetuso LR, Ianiro G, Di Rienzo T, Gasbarrini A, Cammarota G. Role of microbiota and innate immunity in recurrent Clostridium difficile infection. J Immunol Res. 2014;2014:1–8. doi:https://doi.org/10.1155/2014/462740.
   Web of Science ®Google Scholar
• D’Aversa F, Tortora A, Ianiro G, Ponziani FR, Annicchiarico BE, Gasbarrini A. Gut microbiota and metabolic syndrome. Intern Emerg Med. 2013;8(Suppl 1):11–15. doi:10.1007/S11739-013-0916-Z.
   PubMedGoogle Scholar
• Valdes AM, Walter J, Segal E, Spector TD. Role of the gut microbiota in nutrition and health. BMJ. 2018;361:36–44. doi:10.1136/BMJ.K2179.
   Google Scholar
• Ianiro G, Mangiola F, Di Rienzo TA, Bibbò S, Franceschi F, Greco AV, Gasbarrini A. Levothyroxine absorption in health and disease, and new therapeutic perspectives. Eur Rev Med Pharmacol Sci. 2014;18:451–6.
   PubMed Web of Science ®Google Scholar
• Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R, Angenent LT, Ley RE. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci USA. 2011;108(Suppl 1):4578–85. doi:https://doi.org/10.1073/PNAS.1000081107.
   PubMed Web of Science ®Google Scholar
• Jeong S. Factors influencing development of the infant microbiota: from prenatal period to early infancy. Clin Exp Pediatr. 2022;65(9):438. doi:10.3345/CEP.2021.00955.
   Google Scholar
• Bibbò S, Abbondio M, Sau R, Tanca A, Pira G, Errigo A, Manetti R, Pes GM, Dore MP, Uzzau S, et al. Fecal microbiota signatures in celiac disease patients with poly-autoimmunity. Front Cell Infect Microbiol. 2020;10. doi:10.3389/FCIMB.2020.00349.
   PubMed Web of Science ®Google Scholar
• Bibbò S, Dore MP, Pes GM, Delitala G, Delitala AP. Is there a role for gut microbiota in type 1 diabetes pathogenesis? Ann Med. 2017;49(1):11–22. doi:10.1080/07853890.2016.1222449.
   PubMed Web of Science ®Google Scholar
• Christovich A, Luo XM. Gut microbiota, Leaky gut, and autoimmune diseases. Front Immunol. 2022;13. doi:10.3389/FIMMU.2022.946248.
   PubMedGoogle Scholar
• Ali A, Ara A, Kashyap MK. Gut microbiota: role and association with tumorigenesis in different malignancies. Mol Biol Rep. 2022;49(8):8087–107. doi:10.1007/S11033-022-07357-6.
   PubMed Web of Science ®Google Scholar
• Hanahan D. Hallmarks of cancer: new dimensions. Cancer Discov. 2022;12(1):31–46. doi:10.1158/2159-8290.CD-21-1059.
   PubMed Web of Science ®Google Scholar
• Fulbright LE, Ellermann M, Arthur JC. The microbiome and the hallmarks of cancer. PLoS Pathog. 2017;13(9):e1006480. doi:https://doi.org/10.1371/JOURNAL.PPAT.1006480.
   PubMed Web of Science ®Google Scholar
• Lu Y, Yuan X, Wang M, He Z, Li H, Wang J, Li Q. Gut microbiota influence immunotherapy responses: mechanisms and therapeutic strategies. J Hematol Oncol. 2022;15(1). doi:10.1186/S13045-022-01273-9.
   Web of Science ®Google Scholar
• Eble JN, Sauter G, Epstein J, Sesterhenn I, editors. Pathology and genetics of tumours of the urinary system and male genital organs. Vol. 7. 3rd ed. WHO Classifications of Tumors IARC; 2004.
   Google Scholar
• Escudier B, Porta C, Schmidinger M, Rioux-Leclercq N, Bex A, Khoo V, Grünwald V, Gillessen S, Horwich A. Renal cell carcinoma: ESMO clinical practice guidelines for diagnosis, treatment and follow-up†. Ann Oncol. 2019;30(5):706–20. doi:10.1093/ANNONC/MDZ056.
   PubMed Web of Science ®Google Scholar
• Linehan WM, Spellman PT, Ricketts CJ, Creighton CJ, Fei SS, Davis C, Wheeler DA, Murray BA, Schmidt L, et al. Comprehensive molecular characterization of papillary renal-cell carcinoma. N Engl J Med. 2016;374(2):135–45. doi:10.1056/NEJMOA1505917.
   PubMed Web of Science ®Google Scholar
• Creighton CJ, Morgan M, Gunaratne PH, Wheeler DA, Gibbs RA, Robertson AG, Chu A, Beroukhim R., Cibulskis K., Signoretti S., et al. Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature. 2013;499(7456):43–9. doi:10.1038/NATURE12222.
   PubMedGoogle Scholar
• Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2022. CA Cancer J Clin. 2022;72(1):7–33. doi:10.3322/CAAC.21708.
   PubMed Web of Science ®Google Scholar
• Fay AP, McKay RR, Lin X, Simantov R, Choueiri TK. Impact of geographic regions on overall survival in patients with metastatic renal cell carcinoma: results from an International clinical trials database. J Glob Oncol. 2018;4(4):1–14. doi:10.1200/JGO.17.00119.
   Google Scholar
• Key Statistics About Kidney Cancer. n.d. [accessed 2023 January 18]. https://www.cancer.org/cancer/kidney-cancer/about/key-statistics.html.
   Google Scholar
• Zhuang TZ, Case K, Olsen TA, Brown JT, Carthon BC, Kucuk O, Goldman J, Harris W, Bilen MA, Nazha B, et al. Metastatic clear-cell renal cell carcinoma in the era of immune checkpoint inhibitors: therapies and ongoing trials. Cancers Basel. 2022;14(12):2867. doi:https://doi.org/10.3390/CANCERS14122867.
   PubMed Web of Science ®Google Scholar
• Padala SA, Barsouk A, Thandra KC, Saginala K, Mohammed A, Vakiti A, Rawla P, Barsouk A. Epidemiology of renal cell carcinoma. World J Oncol. 2020;11(3):79–87. doi:10.14740/WJON1279.
   PubMedGoogle Scholar
• Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin. 2016;66(1):7–30. doi:10.3322/CAAC.21332.
   PubMed Web of Science ®Google Scholar
• Lipworth L, Tarone RE, Lund L, McLaughlin JK. Epidemiologic characteristics and risk factors for renal cell cancer. Clin Epidemiol. 2009;1:33. doi:10.2147/CLEP.S4759.
   PubMedGoogle Scholar
• Choueiri TK, Tomczak P, Park SH, Venugopal B, Ferguson T, Chang Y-H, Hajek J, Symeonides SN, Lee JL, Sarwar N, et al. Adjuvant pembrolizumab after nephrectomy in renal-cell carcinoma. N Engl J Med. 2021;385(8):683–94. doi:https://doi.org/10.1056/NEJMoa2106391.
   PubMed Web of Science ®Google Scholar
• Powles T. Recent eUpdate to the ESMO clinical practice guidelines on renal cell carcinoma on cabozantinib and nivolumab for first-line clear cell renal cancer: renal cell carcinoma: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2021;32(3):422–3. doi:10.1016/J.ANNONC.2020.11.016.
   PubMed Web of Science ®Google Scholar
• Singer EA, Rumble RB, Van Veldhuizen PJ. Management of metastatic clear cell renal cell carcinoma: ASCO guideline Q&A. JCO Oncol Pract. 2023;19(3):127–31. doi:10.1200/OP.22.00660.
   PubMedGoogle Scholar
• Choi WS, Boland J, Lin J. Hypoxia-inducible factor-2α as a novel target in renal cell carcinoma. J Kidney Cancer VHL. 2021;8(2):1–7. doi:10.15586/jkcvhl.v8i2.170.
   PubMed Web of Science ®Google Scholar
• Rini BI, Campbell SC, Escudier B. Renal cell carcinoma. Lancet. 2009;373(9669):1119–32. doi:10.1016/S0140-6736(09)60229-4.
   PubMed Web of Science ®Google Scholar
• Motzer RJ, Hutson TE, Glen H, Michaelson MD, Molina A, Eisen T, Jassem J, Zolnierek J, Maroto JP, Mellado B, et al. Lenvatinib, everolimus, and the combination in patients with metastatic renal cell carcinoma: a randomised, phase 2, open-label, multicentre trial. Lancet Oncol. 2015;16(15):1473–82. doi:10.1016/S1470-2045(15)00290-9.
   PubMed Web of Science ®Google Scholar
• Sternberg CN, Davis ID, Mardiak J, Szczylik C, Lee E, Wagstaff J, Barrios CH, Salman P, Gladkov OA, Kavina A, et al. Pazopanib in locally advanced or metastatic renal cell carcinoma: results of a randomized phase III trial. J Clin Oncol. 2010;28(6):1061–8. doi:https://doi.org/10.1200/JCO.2009.23.9764.
   PubMed Web of Science ®Google Scholar
• Escudier B, Bellmunt J, Négrier S, Bajetta E, Melichar B, Bracarda S, Ravaud A, Golding S, Jethwa S, Sneller V, et al. Phase III trial of bevacizumab plus interferon alfa-2a in patients with metastatic renal cell carcinoma (AVOREN): final analysis of overall survival. J Clin Oncol. 2010;28(13):2144–50. doi:10.1200/JCO.2009.26.7849.
   PubMed Web of Science ®Google Scholar
• Choueiri TK, Halabi S, Sanford BL, Hahn O, Michaelson MD, Walsh MK, Feldman DR, Olencki T, Picus J, Small EJ, et al. Cabozantinib versus sunitinib as initial targeted therapy for patients with metastatic renal cell carcinoma of poor or intermediate risk: the alliance A031203 CABOSUN trial. J Clin Oncol. 2017;35(6):591–7. doi:10.1200/JCO.2016.70.7398.
   PubMed Web of Science ®Google Scholar
• Rini BI, Escudier B, Tomczak P, Kaprin A, Szczylik C, Hutson TE, Michaelson MD, Gorbunova VA, Gore ME, Rusakov IG, et al. Comparative effectiveness of axitinib versus sorafenib in advanced renal cell carcinoma (AXIS): a randomised phase 3 trial. Lancet. 2011;378(9807):1931–9. doi:10.1016/S0140-6736(11)61613-9.
   PubMed Web of Science ®Google Scholar
• Burris HA. Overcoming acquired resistance to anticancer therapy: focus on the PI3K/AKT/mTOR pathway. Cancer Chemother Pharmacol. 2013;71(4):829–42. doi:10.1007/s00280-012-2043-3.
   PubMed Web of Science ®Google Scholar
• Rosenberg SA, Lotze MT, Muul LM, Chang AE, Avis FP, Leitman S, Linehan WM, Robertson CN, Lee RE, Rubin JT, et al. A progress report on the treatment of 157 patients with advanced cancer using lymphokine-activated killer cells and interleukin-2 or high-dose interleukin-2 alone. N Engl J Med. 1987;316(15):889–97. doi:10.1056/NEJM198704093161501.
   PubMed Web of Science ®Google Scholar
• Motzer RJ, Escudier B, McDermott DF, George S, Hammers HJ, Srinivas S, Tykodi SS, Sosman JA, Procopio G, Plimack ER, et al. Nivolumab versus everolimus in advanced renal-cell carcinoma. N Engl J Med. 2015;373(19):1803–13. doi:10.1056/NEJMOA1510665.
   PubMed Web of Science ®Google Scholar
• Motzer RJ, Tannir NM, McDermott DF, Arén Frontera O, Melichar B, Choueiri TK, Plimack ER, Barthélémy P, Porta C, George S, et al. Nivolumab plus ipilimumab versus sunitinib in advanced renal-cell carcinoma. N Engl J Med. 2018;378(14):1277–90. doi:10.1056/NEJMOA1712126.
   PubMed Web of Science ®Google Scholar
• Rini BI, Plimack ER, Stus V, Gafanov R, Hawkins R, Nosov D, Pouliot F, Alekseev B, Soulières D, Melichar B, et al. Pembrolizumab plus axitinib versus sunitinib for advanced renal-cell carcinoma. N Engl J Med. 2019;380(12):1116–27. doi:10.1056/NEJMoa1816714.
   PubMed Web of Science ®Google Scholar
• Motzer RJ, Penkov K, Haanen J, Rini B, Albiges L, Campbell MT, Venugopal B, Kollmannsberger C, Negrier S, Uemura M, et al. Avelumab plus axitinib versus sunitinib for advanced renal-cell carcinoma. N Engl J Med. 2019;380(12):1103–15. doi:10.1056/NEJMOA1816047.
   PubMed Web of Science ®Google Scholar
• Liu B, Zhang Y, Wang D, Hu X, Zhang Z. Single-cell meta-analyses reveal responses of tumor-reactive CXCL13+ T cells to immune-checkpoint blockade. Nat Cancer. 2022;3(9):1123–36. doi:10.1038/S43018-022-00433-7.
   PubMedGoogle Scholar
• Kramer P, Bressan P. Humans as Superorganisms: how microbes, viruses, imprinted genes, and other selfish entities shape our behavior. Perspect Psychol Sci. 2015;10(4):464–81. doi:10.1177/1745691615583131.
   PubMedGoogle Scholar
• Wu HJ, Wu E. The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes. 2012;3(1):4. doi:10.4161/GMIC.19320.
   PubMed Web of Science ®Google Scholar
• Riazi-Rad F, Behrouzi A, Mazaheri H, Katebi A, Ajdary S. Impact of gut microbiota on immune system. Acta Microbiol Immunol Hung. 2021;68(3):135–44. doi:10.1556/030.2021.01532.
   Web of Science ®Google Scholar
• Larsen JM. The immune response to Prevotella bacteria in chronic inflammatory disease. Immunology. 2017;151(4):363–74. doi:10.1111/IMM.12760.
   PubMed Web of Science ®Google Scholar
• Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, Liu H, Cross JR, Pfeffer K, Coffer PJ, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 2013;504(7480):451–5. doi:10.1038/NATURE12726.
   PubMed Web of Science ®Google Scholar
• Shahbaz A, Mahmood T, Javed MU, Abbasi BH. Current advances in microbial-based cancer therapies. Med Oncol. 2023;40(7):207. doi:10.1007/S12032-023-02074-X.
   PubMed Web of Science ®Google Scholar
• Vétizou M, Pitt JM, Daillère R, Lepage P, Waldschmitt N, Flament C, Rusakiewicz S, Routy B, Roberti MP, Duong CPM, et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Sci. 2015;350(6264):1079–84. doi:10.1126/SCIENCE.AAD1329.
   PubMed Web of Science ®Google Scholar
• Pinato DJ, Howlett S, Ottaviani D, Urus H, Patel A, Mineo T, Brock C, Power D, Hatcher O, Falconer A, et al. Association of prior antibiotic treatment with survival and response to immune checkpoint Inhibitor therapy in patients with cancer. JAMA Oncol. 2019;5(12):1774–8. doi:10.1001/JAMAONCOL.2019.2785.
   PubMed Web of Science ®Google Scholar
• Sivan A, Corrales L, Hubert N, Williams JB, Aquino-Michaels K, Earley ZM, Benyamin FW, Man Lei Y, Jabri B, Alegre M-L, et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti–PD-L1 efficacy. Science. 2015;350(6264):1084–9. doi:https://doi.org/10.1126/SCIENCE.AAC4255.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Liu Z, Chen T. Gut microbiota: a promising milestone in enhancing the efficacy of PD1/PD-L1 blockade therapy. Front Oncol. 2022;12:476. doi:10.3389/fonc.2022.847350.
   Web of Science ®Google Scholar
• Matson V, Fessler J, Bao R, Chongsuwat T, Zha Y, Alegre M-L, Luke JJ, Gajewski TF. The commensal microbiome is associated with anti–PD-1 efficacy in metastatic melanoma patients. Science. 2018;359(6371):104–8. doi:10.1126/SCIENCE.AAO3290.
   PubMed Web of Science ®Google Scholar
• Derosa L, Routy B, Fidelle M, Iebba V, Alla L, Pasolli E, Segata N, Desnoyer A, Pietrantonio F, Ferrere G, et al. Gut bacteria composition drives primary resistance to cancer immunotherapy in renal cell carcinoma patients. Eur Urol. 2020;78(2):195–206. doi:https://doi.org/10.1016/J.EURURO.2020.04.044.
   PubMed Web of Science ®Google Scholar
• Zheng Y, Wang T, Tu X, Huang Y, Zhang H, Tan D, Jiang W, Cai S, Zhao P, Song R, et al. Gut microbiome affects the response to anti-PD-1 immunotherapy in patients with hepatocellular carcinoma. J Immunother Cancer. 2019;7(1). doi:https://doi.org/10.1186/S40425-019-0650-9.
   Google Scholar
• He D, Li X, An R, Wang L, Wang Y, Zheng S, Chen X, Wang X. Response to PD-1-Based immunotherapy for non-small cell lung cancer altered by gut microbiota. Oncol Ther. 2021;9(2):647–57. doi:10.1007/S40487-021-00171-3.
   PubMed Web of Science ®Google Scholar
• Derosa L, Routy B, Thomas AM, Iebba V, Zalcman G, Friard S, Mazieres J, Audigier-Valette C, Moro-Sibilot D, Goldwasser F, et al. Intestinal Akkermansia muciniphila predicts clinical response to PD-1 blockade in patients with advanced non-small-cell lung cancer. Nat Med. 2022;28(2):315–24. doi:10.1038/S41591-021-01655-5.
   PubMed Web of Science ®Google Scholar
• Frankel AE, Coughlin LA, Kim J, Froehlich TW, Xie Y, Frenkel EP, Koh AY. Metagenomic shotgun sequencing and unbiased metabolomic profiling identify specific human gut microbiota and metabolites associated with immune checkpoint therapy efficacy in melanoma patients. Neoplasia. 2017;19(10):848–55. doi:10.1016/J.NEO.2017.08.004.
   PubMed Web of Science ®Google Scholar
• Li X, Zhang S, Guo G, Han J, Yu J. Gut microbiome in modulating immune checkpoint inhibitors. EBioMedicine. 2022;82:104163. doi:https://doi.org/10.1016/J.EBIOM.2022.104163.
   PubMed Web of Science ®Google Scholar
• Cammarota G, Ianiro G, Bibbò S, Gasbarrini A. Gut microbiota modulation: probiotics, antibiotics or fecal microbiota transplantation? Intern Emerg Med. 2014;9(4):365–73. doi:10.1007/S11739-014-1069-4.
   PubMed Web of Science ®Google Scholar
• Bibbò S, Ianiro G, Giambò F, Settanni CR, Cammarota G, Gasbarrini A. Role of gut microbiome on immunotherapy efficacy in melanoma. Hum Vaccin Immunother. 2022;18(3). doi:10.1080/21645515.2021.1926759.
   PubMed Web of Science ®Google Scholar
• 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. 2018;29(6):1437–44. doi:10.1093/ANNONC/MDY103.
   PubMed Web of Science ®Google Scholar
• Wilson BE, Routy B, Nagrial A, Chin VT. The effect of antibiotics on clinical outcomes in immune-checkpoint blockade: a systematic review and meta-analysis of observational studies. Cancer Immunol Immunother. 2020;69(3):343–54. doi:10.1007/S00262-019-02453-2.
   PubMed Web of Science ®Google Scholar
• Tsikala-Vafea M, Belani N, Vieira K, Khan H, Farmakiotis D. Use of antibiotics is associated with worse clinical outcomes in patients with cancer treated with immune checkpoint inhibitors: a systematic review and meta-analysis. Int J Infect Dis. 2021;106:142–54. doi:10.1016/J.IJID.2021.03.063.
   PubMed Web of Science ®Google Scholar
• Wu Q, Liu J, Wu S, Xie X. The impact of antibiotics on efficacy of immune checkpoint inhibitors in malignancies: a study based on 44 cohorts. Int Immunopharmacol. 2021;92. doi:10.1016/J.INTIMP.2020.107303.
   Web of Science ®Google Scholar
• Guven DC, Acar R, Yekeduz E, Bilgetekin I, Baytemur NK, Erol C, Ceylan F, Sendur MA, Demirci U, Urun Y, et al. The association between antibiotic use and survival in renal cell carcinoma patients treated with immunotherapy: a multi-center study. Curr Probl Cancer. 2021;45(6):100760. doi:https://doi.org/10.1016/J.CURRPROBLCANCER.2021.100760.
   PubMed Web of Science ®Google Scholar
• Lalani AKA, Xie W, Braun DA, Kaymakcalan M, Bossé D, Steinharter JA, Martini DJ, Simantov R, Lin X, Wei XX, et al. Effect of antibiotic use on outcomes with systemic therapies in metastatic renal cell carcinoma. Eur Urol Oncol. 2019;3(3):372–81. doi:https://doi.org/10.1016/J.EUO.2019.09.001.
   PubMed Web of Science ®Google Scholar
• Cortellini A, Di Maio M, Nigro O, Leonetti A, Cortinovis DL, Aerts JG, Guaitoli G, Barbieri F, Giusti R, Ferrara MG, et al. Differential influence of antibiotic therapy and other medications on oncological outcomes of patients with non-small cell lung cancer treated with first-line pembrolizumab versus cytotoxic chemotherapy. J Immunother Cancer. 2021;9(4):e002421. doi:https://doi.org/10.1136/JITC-2021-002421.
   PubMed Web of Science ®Google Scholar
• Cortellini A, Ricciuti B, Facchinetti F, Alessi JVM, Venkatraman D, Dall’Olio FG, Cravero P, Vaz VR, Ottaviani D, Majem M, et al. Antibiotic-exposed patients with non-small-cell lung cancer preserve efficacy outcomes following first-line chemo-immunotherapy. Ann Oncol. 2021;32(11):1391–9. doi:10.1016/J.ANNONC.2021.08.1744.
   PubMed Web of Science ®Google Scholar
• Cordaillat-Simmons M, Rouanet A, Pot B. Live biotherapeutic products: the importance of a defined regulatory framework. Exp Mol Med. 2020;52(9):1397–406. doi:10.1038/S12276-020-0437-6.
   PubMed Web of Science ®Google Scholar
• 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. Sci. 2021;374(6575):1632–40. doi:10.1126/SCIENCE.AAZ7015.
   PubMed Web of Science ®Google Scholar
• Wan L, Wu C, Wu Q, Luo S, Liu J, Xie X. Impact of probiotics use on clinical outcomes of immune checkpoint inhibitors therapy in cancer patients. Cancer Med. 2022;12:1841–9. doi:https://doi.org/10.1002/CAM4.4994.
   PubMed Web of Science ®Google Scholar
• Zhang L, Jin Q, Chai D, Kuang T, Li C, Guan Y, Liu L, Wang W, Deng W. The correlation between probiotic use and outcomes of cancer patients treated with immune checkpoint inhibitors. Front Pharmacol. 2022;13. doi:10.3389/fphar.2022.937874.
   Web of Science ®Google Scholar
• Hahn AW, Froerer C, VanAlstine S, Rathi N, Bailey EB, Stenehjem DD, Agarwal N. Targeting Bacteroides in stool microbiome and response to treatment with first-line VEGF tyrosine kinase inhibitors in metastatic renal-cell carcinoma. Clin Genitourin Cancer. 2018;16(5):365–8. doi:10.1016/J.CLGC.2018.05.001.
   PubMed Web of Science ®Google Scholar
• Dizman N, Hsu JA, Bergerot PG, Gillece JD, Folkerts M, Reining L, Trent J, Highlander SK., Pal SK. Randomized trial assessing impact of probiotic supplementation on gut microbiome and clinical outcome from targeted therapy in metastatic renal cell carcinoma. Cancer Med. 2021;10(1):79–86. doi:10.1002/CAM4.3569.
   PubMed Web of Science ®Google Scholar
• Hagihara M, Kuroki Y, Ariyoshi T, Higashi S, Fukuda K, Yamashita R, Matsumoto A, Mori T, Mimura K, Yamaguchi N, et al. Clostridium butyricum modulates the microbiome to protect intestinal barrier function in mice with Antibiotic-Induced Dysbiosis. Science. 2020;23(1):100772. doi:https://doi.org/10.1016/J.ISCI.2019.100772.
   Google Scholar
• 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. 2022;28(4):704–12. doi:https://doi.org/10.1038/s41591-022-01694-6.
   PubMed Web of Science ®Google Scholar
• Meza LA, Malhotra J, Zengin ZB, Dizman N, Hsu J, Chawla NS, Chehrazi-Raffle A, Muddasani R, Govindarajan A, Castro DV, et al. A phase I trial to evaluate the biologic effect of CBM588 (Clostridium butyricum) in combination with cabozantinib plus nivolumab for patients with metastatic renal cell carcinoma (mRCC). 2022;40(16_suppl):TPS4606–TPS4606. doi:10.1200/JCO.2022.40.16_SUPPL.TPS4606.
   Google Scholar
• Lythgoe M, Dama P, Frampton AE, Pickford E, Tookman L, Cunnea P, Fotopoulou C, Liu D, Clark J, Lozano-Kuehne J, et al. Immune modulation and the oral live biotherapeutic product, MRx0518, in treatment-naïve patients with cancer: updated safety data. J Clin Oncol. 2023;41(16_suppl):3145–3145. doi:https://doi.org/10.1200/JCO.2023.41.16_SUPPL.3145.
   Google Scholar
• Saedisomeolia A, Wood LG, Garg ML, Gibson PG, Wark PAB. Anti-inflammatory effects of long-chain n -3 PUFA in rhinovirus-infected cultured airway epithelial cells. Br J Nutr. 2009;101(4):533–40. doi:10.1017/S0007114508025798.
   PubMed Web of Science ®Google Scholar
• Comerlato CB, Zhang X, Walker K, Brandelli A, Figeys D. Comparative proteomic analysis reveals metabolic variability of probiotic Enterococcus durans during aerobic and anaerobic cultivation. J Proteomics. 2020;220:103764. doi:https://doi.org/10.1016/J.JPROT.2020.103764.
   PubMed Web of Science ®Google Scholar
• Intestinal microbiome modification with resistant starch in patients treated with dual immune checkpoint inhibitors - full text view - ClinicalTrials.Gov. n.d [accessed 2022 December 11. https://clinicaltrials.gov/ct2/show/NCT04552418.
   Google Scholar
• Han K, Nam J, Xu J, Sun X, Huang X, Animasahun O, Achreja A, Jeon JH, Pursley B, Kamada N, et al. Generation of systemic antitumour immunity via the in situ modulation of the gut microbiome by an orally administered inulin gel. Nat Biomed Eng. 2021;5(11):1377–88. doi:10.1038/S41551-021-00749-2.
   PubMed Web of Science ®Google Scholar
• Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, et al. Evolution of mammals and their gut microbes. Sci. 2008;320(5883):1647–51. doi:10.1126/SCIENCE.1155725.
   PubMed Web of Science ®Google Scholar
• Nava GM, Carbonero F, Ou J, Benefiel AC, O’Keefe SJ, Gaskins HR. Hydrogenotrophic microbiota distinguish native Africans from African and European Americans. Environ Microbiol Rep. 2012;4(3):307–15. doi:10.1111/J.1758-2229.2012.00334.X.
   PubMed Web of Science ®Google Scholar
• Devkota S, Wang Y, Musch MW, Leone V, Fehlner-Peach H, Nadimpalli A, Antonopoulos DA, Jabri B, Chang EB. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10−/− mice. Nature. 2012;487(7405):104–8. doi:10.1038/NATURE11225.
   PubMed Web of Science ®Google Scholar
• Olivares-Hernández A, Figuero-Pérez L, González-Sarmiento R, León-Jiménez D, Cruz-Hernández JJ, Miramontes-González JP. The influence of diet and probiotics on the response of solid Tumours to immunotherapy: present and future perspectives. Appl Sci. 2021;11(18):8445. doi:10.3390/APP11188445.
   Google Scholar
• Zhang X, Browman G, Siu W, Basen-Engquist KM, Hanash SM, Hoffman KL, Okhuysen PC, Scheet P, Petrosino JF, Kopetz S, et al. The BE GONE trial study protocol: a randomized crossover dietary intervention of dry beans targeting the gut microbiome of overweight and obese patients with a history of colorectal polyps or cancer. BMC Cancer. 2019;19(1):1–11. doi:https://doi.org/10.1186/s12885-019-6400-z.
   PubMed Web of Science ®Google Scholar
• Fasting-mimicking diet with chemo-immunotherapy in non-small cell lung cancer (NSCLC) - full text view - ClinicalTrials.Gov n.d. [accessed 2022 December 11]. https://clinicaltrials.gov/ct2/show/NCT03700437.
   Google Scholar
• Safety and potential efficacy of MS-20 in combination with pembrolizumab for the treatment of NSCLC - Full text view - ClinicalTrials.Gov. n.d. [accessed 2022 December 11]. https://clinicaltrials.gov/ct2/show/NCT04909034.
   Google Scholar
• Dietary intervention in patients with a history of melanoma - full text view - ClinicalTrials.Gov n.d. [accessed 2022 December 11]. https://clinicaltrials.gov/ct2/show/NCT03950635.
   Google Scholar
• Spencer CN, Gopalakrishnan V, McQuade J, Andrews MC, Helmink B, Khan MAW, Sirmans E, Haydu L, Cogdill A, Burton E, et al. Abstract 2838: the gut microbiome (GM) and immunotherapy response are influenced by host lifestyle factors. Cancer Res. 2019;79(13_Supplement):2838–2838. doi:10.1158/1538-7445.AM2019-2838.
   Web of Science ®Google Scholar
• Ianiro G, Maida M, Burisch J, Simonelli C, Hold G, Ventimiglia M, Gasbarrini A, Cammarota G. Efficacy of different faecal microbiota transplantation protocols for Clostridium difficile infection: a systematic review and meta-analysis. United Eur Gastroent J. 2018;6(8):1232–44. doi:10.1177/2050640618780762.
   PubMed Web of Science ®Google Scholar
• Bibbò S, Settanni CR, Porcari S, Bocchino E, Ianiro G, Cammarota G, Gasbarrini A. Fecal microbiota transplantation: screening and selection to choose the optimal donor. J Clin Med. 2020;9(6):1–14. doi:10.3390/JCM9061757.
   Web of Science ®Google Scholar
• Lythgoe MP, Ghani R, Mullish BH, Marchesi JR, Krell J. The potential of fecal microbiota transplantation in oncology. Trends Microbiol. 2022;30(1):10–12. doi:10.1016/J.TIM.2021.10.003.
   PubMed Web of Science ®Google Scholar
• 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. 2021;371(6529):602–9. doi:10.1126/SCIENCE.ABB5920.
   PubMed Web of Science ®Google Scholar
• Davar D, Dzutsev AK, McCulloch JA, Rodrigues RR, Chauvin J-M, 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. 2021;371(6529):595–602. doi:https://doi.org/10.1126/SCIENCE.ABF3363.
   PubMed Web of Science ®Google Scholar
• Elkrief A, Routy B. First clinical proof-of-concept that FMT can overcome resistance to ICIs. Nat Rev Clin Oncol. 2021;18(6):325–6. doi:https://doi.org/10.1038/s41571-021-00502-3.
   PubMed Web of Science ®Google Scholar
• Routy B, Lenehan JG, Miller WH, Jamal R, Messaoudene M, Daisley BA, Hes C, Al KF, Martinez-Gili L, Punčochář M, et al. Fecal microbiota transplantation plus anti-PD-1 immunotherapy in advanced melanoma: a phase I trial. Nat Med. 2023;29:2121–32. doi:https://doi.org/10.1038/s41591-023-02453-x.
   PubMed Web of Science ®Google Scholar
• Ianiro G, Rossi E, Thomas AM, Schinzari G, Masucci L, Quaranta G, Settanni CR, Lopetuso LR, Armanini F, Blanco-Miguez A, et al. Faecal microbiota transplantation for the treatment of diarrhoea induced by tyrosine-kinase inhibitors in patients with metastatic renal cell carcinoma. Nat Commun. 2020;11(1):1–6. doi:https://doi.org/10.1038/s41467-020-18127-y.
   PubMed Web of Science ®Google Scholar
• Porcari S, Ciccarese C, Pinto F, Quaranta G, De Giorgi S, Rondinella D, Settanni CR, Cortesi E, Roberto M, Primi F, et al. Fecal microbiota transplantation to improve efficacy of immune checkpoint inhibitors in renal cell carcinoma (TACITO trial). J Clin Oncol. 2022;40(6_suppl):TPS407–TPS407. doi:https://doi.org/10.1200/JCO.2022.40.6_SUPPL.TPS407.
   Web of Science ®Google Scholar
• Fecal microbiota transplantation in patients with malignancies not responding to immune checkpoint Inhibitor therapy - full text view - ClinicalTrials.Gov n.d. [accessed 2023 January 18]. https://clinicaltrials.gov/ct2/show/NCT05273255.
   Google Scholar
• FMT combined with immune checkpoint Inhibitor and TKI in the treatment of CRC patients with advanced stage - full text view - ClinicalTrials.Gov n.d. [accessed 2023 January 18]. https://clinicaltrials.gov/ct2/show/NCT05279677.
   Google Scholar
• Gloy V, Schmitt AM, Düblin P, Hirt J, Axfors C, Kuk H, Pereira TV, Locher C, Caquelin L, Walter‐Claudi M, et al. The evidence base of US food and Drug administration approvals of novel cancer therapies from 2000 to 2020. Int J Cancer. 2023;152(12):2474–84. doi:10.1002/IJC.34473.
   PubMed Web of Science ®Google Scholar