Is the survival of patients treated with ipilimumab affected by antibiotics? An analysis of 1585 patients from the French National hospital discharge summary database (PMSI)

References

• Michot JM, Lazarovici J, Tieu A, Champiat S, Voisin AL, Ebbo M, Godeau B, Michel M, Ribrag V, Lambotte O. Haematological immune-related adverse events with immune checkpoint inhibitors, how to manage? Eur J Cancer. 2019;122:72–8. doi:10.1016/j.ejca.2019.07.014.
   PubMed Web of Science ®Google Scholar
• Denis H, Davoine C, Bermudez E, Grosjean G, Schwager M, Ifrah N, Dahan M, Negellen S. Les immunothérapies spécifiques dans le traitement des cancers. Bull Cancer. 2019;106(1):37–47. doi:10.1016/j.bulcan.2018.12.007.
   PubMed Web of Science ®Google Scholar
• Chambers CA, Kuhns MS, Egen JG, Allison JP. CTLA-4-mediated inhibition in regulation of T cell responses: mechanisms and manipulation in tumor immunotherapy. Annu Rev Immunol. 2001;19(1):565–594. doi:10.1146/annurev.immunol.19.1.565.
   PubMedGoogle Scholar
• Mellman I, Coukos G, Dranoff G. Cancer immunotherapy comes of age. Nature. 2011;480:480–489. doi:10.1038/nature10673.
   PubMed Web of Science ®Google Scholar
• Iizumi T, Battaglia T, Ruiz V, Perez Perez GI. Gut microbiome and antibiotics. Arch Med Res. 2017;48(8):727–734. doi:10.1016/j.arcmed.2017.11.004.
   PubMed Web of Science ®Google Scholar
• Zimmermann P, Curtis N. The effect of antibiotics on the composition of the intestinal microbiota - a systematic review. J Infect. 2019;79(6):471–489. doi:10.1016/j.jinf.2019.10.008.
   PubMed Web of Science ®Google Scholar
• Nord CE, Gajjar DA, Grasela DM. Ecological impact of the des-F(6)-quinolone, BMS-284756, on the normal intestinal microflora. Clin Microbio Infect. 2002;8(4):229–239. doi:10.1046/j.1469-0691.2002.00414.x.
   PubMed Web of Science ®Google Scholar
• Kelly D, Mulder IE. Microbiome and immunological interactions. Nutr Rev. 2012;70(Suppl 1):S18–30. doi:10.1111/j.1753-4887.2012.00498.x.
   PubMedGoogle Scholar
• Rescigno M. The intestinal epithelial barrier in the control of homeostasis and immunity. Trends Immunol. 2011;32(6):256–264. doi:10.1016/j.it.2011.04.003.
   PubMed Web of Science ®Google Scholar
• Diehl GE, Longman RS, Zhang J-X, Breart B, Galan C, Cuesta A, Schwab SR, Littman DR. Microbiota restricts trafficking of bacteria to mesenteric lymph nodes by CX 3 CR1 hi cells. Nature. 2013;494(7435):116–120. doi:10.1038/nature11809.
   PubMed Web of Science ®Google Scholar
• Vetizou M, Pitt JM, Daillere 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. Science. 2015;350(6264):1079–1084. doi:10.1126/science.aad1329.
   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):1084–1089. doi:10.1126/science.aac4255.
   PubMed Web of Science ®Google Scholar
• 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. 2018;359:91–97. doi:10.1126/science.aan3706.
   PubMed Web of Science ®Google Scholar
• Ahmed J, Kumar A, Parikh K, Anwar A, Knoll BM, Puccio C, Chun H, Fanucchi M, Lim SH. Use of broad-spectrum antibiotics impacts outcome in patients treated with immune checkpoint inhibitors. Oncoimmunology. 2018;7(11):e1507670. doi:10.1080/2162402X.2018.1507670.
   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):1437–1444. doi:10.1093/annonc/mdy103.
   PubMed Web of Science ®Google Scholar
• Elkrief A, Derosa L, Kroemer G, Zitvogel L, Routy B. The negative impact of antibiotics on outcomes in cancer patients treated with immunotherapy: a new independent prognostic factor? Ann Oncol. 2019;30(10):1572–1579. doi:10.1093/annonc/mdz206.
   PubMed Web of Science ®Google Scholar
• Elkrief A, El Raichani L, Richard C, Messaoudene M, Belkaid W, Malo J, Belanger K, Miller W, Jamal R, Letarte N, et al. Antibiotics are associated with decreased progression-free survival of advanced melanoma patients treated with immune checkpoint inhibitors. Oncoimmunology. 2019;8(4):e1568812. doi:10.1080/2162402X.2019.1568812.
   PubMed Web of Science ®Google Scholar
• Farmakiotis D. The human microbiome and checkpoint inhibition: potential benefits from antibiotic stewardship. Clin Infect Dis. 2019. doi:10.1093/cid/ciz1003.
   PubMed Web of Science ®Google Scholar
• Galli G, Triulzi T, Proto C, Signorelli D, Imbimbo M, Poggi M, Fucà G, Ganzinelli M, Vitali M, Palmieri D, et al. Association between antibiotic-immunotherapy exposure ratio and outcome in metastatic non small cell lung cancer. Lung Cancer. 2019;132:72–78. doi:10.1016/j.lungcan.2019.04.008.
   PubMed Web of Science ®Google Scholar
• Guo J-C, Lin -C-C, Lin C-Y, Hsieh M-S, Kuo H-Y, Lien M-Y, Shao -Y-Y, Huang T-C, Hsu C-H. Neutrophil-to-lymphocyte ratio and use of antibiotics associated with prognosis in esophageal squamous cell carcinoma patients receiving immune checkpoint inhibitors. Anticancer Res. 2019;39(10):5675–5682. doi:10.21873/anticanres.13765.
   PubMed Web of Science ®Google Scholar
• Hakozaki T, Okuma Y, Omori M, Hosomi Y. Impact of prior antibiotic use on the efficacy of nivolumab for non-small cell lung cancer. Oncol Lett. 2019;17:2946–2952. doi:10.3892/ol.2019.9899.
   PubMed Web of Science ®Google Scholar
• Huemer F, Rinnerthaler G, Westphal T, Hackl H, Hutarew G, Gampenrieder SP, Weiss L, Greil R. Impact of antibiotic treatment on immune-checkpoint blockade efficacy in advanced non-squamous non-small cell lung cancer. Oncotarget. 2018;9(23):16512–16520. doi:10.18632/oncotarget.24751.
   PubMedGoogle Scholar
• Kaderbhai C, Richard C, Fumet JD, Aarnink A, Foucher P, Coudert B, Favier L, Lagrange A, Limagne E, Boidot R, Ghiringhelli Fet al. Antibiotic use does not appear to influence response to nivolumab. Anticancer Res. 2017;37:3195–3200. doi:10.21873/anticanres.11680.
   PubMed Web of Science ®Google Scholar
• Milano G. Efficacy of immunotherapy, gut microbiota and impact of antibiotic use: are there confounding factors? Cancer Chemother Pharmacol. 2019;84(1):223–224. doi:10.1007/s00280-019-03833-2.
   PubMed Web of Science ®Google Scholar
• Ouaknine Krief J, Helly de Tauriers P, Dumenil C, Neveux N, Dumoulin J, Giraud V, Labrune S, Tisserand J, Julie C, Emile J-F, et al. Role of antibiotic use, plasma citrulline and blood microbiome in advanced non-small cell lung cancer patients treated with nivolumab. J Immunother Cancer. 2019;7:176. doi:10.1186/s40425-019-0658-1.
   PubMed Web of Science ®Google Scholar
• Pinato DJ, Howlett S, Ottaviani D, Urus H, Patel A, Mineo T. Association of prior antibiotic treatment with survival and response to immune checkpoint inhibitor therapy in patients with cancer. JAMA Oncol. 2019;5(12):1774. doi:10.1001/jamaoncol.2019.2785.
   PubMed Web of Science ®Google Scholar
• Sen S, Carmagnani Pestana R, Hess K, Viola GM, Subbiah V. Impact of antibiotic use on survival in patients with advanced cancers treated on immune checkpoint inhibitor phase I clinical trials. Ann Oncol. 2018;29(12):2396–2398. doi:10.1093/annonc/mdy453.
   PubMed Web of Science ®Google Scholar
• Tinsley N, Zhou C, Tan G, Rack S, Lorigan P, Blackhall F, Krebs M, Carter L, Thistlethwaite F, Graham D, et al. Cumulative antibiotic use significantly decreases efficacy of checkpoint inhibitors in patients with advanced cancer. Oncologist. 2019. doi:10.1634/theoncologist.2019-0160.
   PubMed Web of Science ®Google Scholar
• Yan C, Tu -X-X, Wu W, Tong Z, Liu -L-L, Zheng Y, Jiang W-Q, Zhao P, Fang W-J, Zhang H-Y, et al. Antibiotics and immunotherapy in gastrointestinal tumors: friend or foe? World J Clin Cases. 2019;7:1253–1261. doi:10.12998/wjcc.v7.i11.1253.
   PubMed Web of Science ®Google Scholar
• Zhao S, Gao G, Li W, Li X, Zhao C, Jiang T, Jia Y, He Y, Li A, Su C, et al. Antibiotics are associated with attenuated efficacy of anti-PD-1/PD-L1 therapies in Chinese patients with advanced non-small cell lung cancer. Lung Cancer. 2019;130:10–17. doi:10.1016/j.lungcan.2019.01.017.
   PubMed Web of Science ®Google Scholar
• Baro E, Degoul S, Beuscart R, Chazard E. Toward a literature-driven definition of big data in healthcare. Biomed Res Int. 2015;2015:639021. doi:10.1155/2015/639021.
   PubMed Web of Science ®Google Scholar
• Meystre SM, Lovis C, Bürkle T, Tognola G, Budrionis A, Lehmann CU. Clinical data reuse or secondary use: current status and potential future progress. Yearb Med Inform. 2017:26. doi:10.15265/IY-2017-007.
   Google Scholar
• Safran C. Reuse of clinical data. Yearb Med Inform. 2014;9:52–54. doi:10.15265/IY-2014-0013.
   PubMedGoogle Scholar
• Chazard E, Ficheur G, Caron A, Lamer A, Labreuche J, Cuggia M, Genin M, Bouzille G, Duhamel A, et al. Secondary use of healthcare structured data: the challenge of domain-knowledge based extraction of features. Stud Health Technol Inform. 2018;255:15–19.
   PubMedGoogle Scholar
• Thillard E-M, Gautier S, Babykina E, Carton L, Amad A, Bouzillé G, Beuscart J-B, Ficheur G, Chazard E. Psychiatric adverse events associated with infliximab: a cohort study from the french nationwide discharge abstract database. Front Pharmacol. 2020;11:513. doi:10.3389/fphar.2020.00513.
   PubMed Web of Science ®Google Scholar
• CIM-10. 2008 [accessed 2018 Mar 27]. http://apps.who.int/classifications/icd10/browse/2008/fr
   Google Scholar
• CPAM. CCAM Principes généraux. 2011 [accessed 2018 Mar 27]. https://www.ameli.fr/fileadmin/user_upload/documents/CCAM-Principes_generaux_mars2011.pdf
   Google Scholar
• Assurance Maladie. Guide pratique pour la facturation des médicaments rétrocédés par les établissements de santé; 2009. [accessed 2020 Jun 17]. https://www.ameli.fr/sites/default/files/Documents/5229/document/facturation-medicaments-retrocedes_assurance-maladie.pdf
   Google Scholar
• R Development Core Team. R: A language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing; 2011.
   Google Scholar
• Mohiuddin JJ, Chu B, Facciabene A, Poirier K, Wang X, Doucette A, Zheng C, Xu W, Anstadt EJ, Amaravadi RK, et al. Association of antibiotic exposure with survival and toxicity in patients with melanoma receiving immunotherapy. J Natl Cancer Inst. n.d. doi:10.1093/jnci/djaa057.
   Google Scholar