Emergence of immune-related adverse events correlates with pathological complete response in patients receiving pembrolizumab for early triple-negative breast cancer

References

• Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin. 2016;66(1):7–7. doi:10.3322/caac.21332.
   PubMed Web of Science ®Google Scholar
• Schmid P, Adams S, Rugo HS, Schneeweiss A, Barrios CH, Iwata H, Diéras V, Hegg R, Im S-A, Shaw Wright G, et al. Atezolizumab and nab-paclitaxel in advanced triple-negative breast cancer. N Engl J Med. 2018;379(22):2108–2121. doi:10.1056/NEJMoa1809615.
   PubMed Web of Science ®Google Scholar
• Cortes J, Cescon DW, Rugo HS, Nowecki Z, Im SA, Yusof MM, Gallardo C, Lipatov O, Barrios CH, Holgado E, et al. Pembrolizumab plus chemotherapy versus placebo plus chemotherapy for previously untreated locally recurrent inoperable or metastatic triple-negative breast cancer (KEYNOTE-355): a randomised, placebo-controlled, double-blind, phase 3 clinical trial. Lancet. 2020;396(10265):1817–1828. doi:10.1016/S0140-6736(20)32531-9.
   PubMed Web of Science ®Google Scholar
• Schmid P, Cortes J, Pusztai L, McArthur H, Kummel S, Bergh J, Denkert C, Park YH, Hui R, Harbeck N, et al. Pembrolizumab for early triple-negative breast cancer. N Engl J Med. 2020;382(9):810–821. doi:10.1056/NEJMoa1910549.
   PubMed Web of Science ®Google Scholar
• Khan Z, Di Nucci F, Kwan A, Hammer C, Mariathasan S, Rouilly V, Carroll J, Fontes M, Ley Acosta S, Guardino E, et al. Polygenic risk for skin autoimmunity impacts immune checkpoint blockade in bladder cancer. Proc Natl Acad Sci U S A. 2020;117(22):12288–12294. doi:10.1073/pnas.1922867117.
   PubMed Web of Science ®Google Scholar
• Schneider BJ, Naidoo J, Santomasso BD, Lacchetti C, Adkins S, Anadkat M, Atkins MB, Brassil KJ, Caterino JM, Chau I, et al. Management of immune-related adverse events in patients treated with immune checkpoint inhibitor therapy: ASCO guideline update. J Clin Oncol. 2021;39(36):4073–4126. doi:10.1200/JCO.21.01440.
   PubMed Web of Science ®Google Scholar
• Untch M, Jackisch C, Schneeweiss A, Conrad B, Aktas B, Denkert C, Eidtmann H, Wiebringhaus H, Kümmel S, Hilfrich J, et al. Nab-paclitaxel versus solvent-based paclitaxel in neoadjuvant chemotherapy for early breast cancer (GeparSepto—GBG 69): a randomised, phase 3 trial. Lancet Oncol. 2016;17(3):345–356. doi:10.1016/S1470-2045(15)00542-2.
   PubMed Web of Science ®Google Scholar
• Cortazar P, Zhang L, Untch M, Mehta K, Costantino JP, Wolmark N, Bonnefoi H, Cameron D, Gianni L, Valagussa P, et al. Pathological complete response and long-term clinical benefit in breast cancer: the CTNeoBC pooled analysis. Lancet. 2014;384(9938):164–172. doi:10.1016/S0140-6736(13)62422-8.
   PubMed Web of Science ®Google Scholar
• Loibl S, O’Shaughnessy J, Untch M, Sikov WM, Rugo HS, McKee MD, Huober J, Golshan M, von Minckwitz G, Maag D, et al. Addition of the PARP inhibitor veliparib plus carboplatin or carboplatin alone to standard neoadjuvant chemotherapy in triple-negative breast cancer (BrighTness): a randomised, phase 3 trial. Lancet Oncol. 2018;19(4):497–509. doi:10.1016/S1470-2045(18)30111-6.
   PubMed Web of Science ®Google Scholar
• Loibl S, Untch M, Burchardi N, Huober J, Sinn BV, Blohmer JU, Grischke E-M, Furlanetto J, Tesch H, Hanusch C, et al. A randomised phase II study investigating durvalumab in addition to an anthracycline taxane-based neoadjuvant therapy in early triple-negative breast cancer: clinical results and biomarker analysis of GeparNuevo study. Ann Oncol. 2019;30(8):1279–1288. doi:10.1093/annonc/mdz158.
   PubMed Web of Science ®Google Scholar
• Gianni L, Huang CS, Egle D, Bermejo B, Zamagni C, Thill M, Anton A, Zambelli S, Bianchini G, Russo S, et al. Pathologic complete response (pCR) to neoadjuvant treatment with or without atezolizumab in triple-negative, early high-risk and locally advanced breast cancer: NeoTRIP Michelangelo randomized study. Ann Oncol. 2022;33(5):534–543. doi:10.1016/j.annonc.2022.02.004.
   PubMed Web of Science ®Google Scholar
• Bartsch R, Singer CF, Pfeiler G, Hubalek M, Stoeger H, Pichler A, Petru E, Bjelic-Radisic V, Greil R, Rudas M, et al. Conventional versus reverse sequence of neoadjuvant epirubicin/cyclophosphamide and docetaxel: sequencing results from ABCSG-34. Br J Cancer. 2021;124(11):1795–1802. doi:10.1038/s41416-021-01284-2.
   PubMed Web of Science ®Google Scholar
• Sung M, Zer A, Walia P, Khoja L, Maganti M, Labbe C, Shepherd FA, Bradbury PA, Liu G, Leighl NB, et al. Correlation of immune-related adverse events and response from immune checkpoint inhibitors in patients with advanced non-small cell lung cancer. J Thorac Dis. 2020;12(5):2706–2712. doi:10.21037/jtd.2020.04.30.
   PubMed Web of Science ®Google Scholar
• Eggermont AMM, Kicinski M, Blank CU, Mandala M, Long GV, Atkinson V, Dalle S, Haydon A, Khattak A, Carlino MS, et al. Association between immune-related adverse events and recurrence-free survival among patients with stage III melanoma randomized to receive pembrolizumab or placebo: a secondary analysis of a randomized clinical trial. JAMA Oncol. 2020;6(4):519–527. doi:10.1001/jamaoncol.2019.5570.
   PubMed Web of Science ®Google Scholar
• Maher VE, Fernandes LL, Weinstock C, Tang S, Agarwal S, Brave M, Ning Y-M, Singh H, Suzman D, Xu J, et al. Analysis of the Association between adverse events and outcome in patients receiving a programmed death protein 1 or programmed death ligand 1 antibody. J Clin Oncol. 2019;37(30):2730–2737. doi:10.1200/JCO.19.00318.
   PubMed Web of Science ®Google Scholar
• Socinski MA, Jotte RM, Cappuzzo F, Nishio M, Mok TSK, Reck M, Finley GG, Kaul MD, Yu W, Paranthaman N, et al. Association of immune-related adverse events with efficacy of atezolizumab in patients with non–small cell lung cancer. JAMA Oncol. 2023;9(4):527–535. doi:10.1001/jamaoncol.2022.7711.
   PubMed Web of Science ®Google Scholar
• Cortellini A, Chiari R, Ricciuti B, Metro G, Perrone F, Tiseo M, Bersanelli M, Bordi P, Santini D, Giusti R, et al. Correlations between the immune-related adverse events spectrum and efficacy of anti-PD1 immunotherapy in NSCLC patients. Clin Lung Cancer. 2019;20(4):237–47 e1. doi:10.1016/j.cllc.2019.02.006.
   PubMed Web of Science ®Google Scholar
• Grangeon M, Tomasini P, Chaleat S, Jeanson A, Souquet-Bressand M, Khobta N, Bermudez J, Trigui Y, Greillier L, Blanchon M, et al. Association between immune-related adverse events and efficacy of immune checkpoint inhibitors in non–small-cell lung cancer. Clin Lung Cancer. 2019;20(3):201–207. doi:10.1016/j.cllc.2018.10.002.
   PubMed Web of Science ®Google Scholar
• Foster CC, Couey MA, Kochanny SE, Khattri A, Acharya RK, Tan YC, Brisson RJ, Leidner RS, Seiwert TY. Immune-related adverse events are associated with improved response, progression-free survival, and overall survival for patients with head and neck cancer receiving immune checkpoint inhibitors. Cancer. 2021;127(24):4565–4573. doi:10.1002/cncr.33780.
   PubMed Web of Science ®Google Scholar
• Xu S, Lai R, Zhao Q, Zhao P, Zhao R, Guo Z. Correlation between immune-related adverse events and prognosis in hepatocellular carcinoma patients treated with immune checkpoint inhibitors. Front Immunol. 2021;12:794099. doi:10.3389/fimmu.2021.794099.
   PubMed Web of Science ®Google Scholar
• Cortellini A, Buti S, Agostinelli V, Bersanelli M. A systematic review on the emerging association between the occurrence of immune-related adverse events and clinical outcomes with checkpoint inhibitors in advanced cancer patients. Semin Oncol. 2019;46(4–5):362–371. doi:10.1053/j.seminoncol.2019.10.003.
   PubMed Web of Science ®Google Scholar
• Hussaini S, Chehade R, Boldt RG, Raphael J, Blanchette P, Maleki Vareki S, Fernandes R. Association between immune-related side effects and efficacy and benefit of immune checkpoint inhibitors – a systematic review and meta-analysis. Cancer Treat Rev. 2021;92:102134. doi:10.1016/j.ctrv.2020.102134.
   PubMed Web of Science ®Google Scholar
• Dall’olio FG, Di Nunno V, Massari F. Immortal time bias question in the Association between toxicity and outcome of immune checkpoint inhibitors. J Clin Oncol. 2020;38(1):105–106. doi:10.1200/JCO.19.01728.
   PubMed Web of Science ®Google Scholar
• Rugo HS, Cescon DW, Im SA, Yusof MM, Araneda CEG, Lipatov O, Cruz F, Barrios CH, Hegg R, Martín EH, et al. 191MO KEYNOTE-355: outcomes in patients who discontinued chemotherapy before pembrolizumab and in patients with immune-mediated AEs. ESMO Open. 2023;8(1):101380. doi:10.1016/j.esmoop.2023.101380.
   Google Scholar
• Sharma P, Barlow WE, Godwin AK, Pathak H, Isakova K, Williams D, Timms KM, Hartman AR, Wenstrup RJ, Linden HM, et al. Impact of homologous recombination deficiency biomarkers on outcomes in patients with triple-negative breast cancer treated with adjuvant doxorubicin and cyclophosphamide (SWOG S9313). Ann Oncol. 2018;29(3):654–660. doi:10.1093/annonc/mdx821.
   PubMed Web of Science ®Google Scholar
• Sharma P, Barlow WE, Godwin AK, Parkes EE, Knight LA, Walker SM, Kennedy RD, Harkin DP, Logan GE, Steele CJ, et al. Validation of the DNA damage immune response signature in patients with triple-negative breast cancer from the SWOG 9313c trial. J Clin Oncol. 2019;37(36):3484–3492. doi:10.1200/JCO.19.00693.
   PubMed Web of Science ®Google Scholar
• Karn T, Denkert C, Weber KE, Holtrich U, Hanusch C, Sinn BV, Higgs BW, Jank P, Sinn HP, Huober J, et al. Tumor mutational burden and immune infiltration as independent predictors of response to neoadjuvant immune checkpoint inhibition in early TNBC in GeparNuevo. Ann Oncol. 2020;31(9):1216–1222. doi:10.1016/j.annonc.2020.05.015.
   PubMed Web of Science ®Google Scholar
• El Sayed R, Haibe Y, Amhaz G, Bouferraa Y, Shamseddine A. Metabolic factors affecting tumor immunogenicity: what is happening at the cellular level? Int J Mol Sci. 2021;22(4):2142. doi:10.3390/ijms22042142.
   PubMed Web of Science ®Google Scholar
• Kawaguchi K, Maeshima Y, Toi M. Tumor immune microenvironment and systemic response in breast cancer. Med Oncol. 2022;39(12):208. doi:10.1007/s12032-022-01782-0.
   PubMed Web of Science ®Google Scholar
• Kawase K, Kawashima S, Nagasaki J, Inozume T, Tanji E, Kawazu M, Hanazawa T, Togashi Y. High expression of MHC class I overcomes cancer immunotherapy resistance due to IFNγ signaling pathway defects. Cancer Immunol Res. 2023;11(7):895–908. doi:10.1158/2326-6066.CIR-22-0815.
   PubMed Web of Science ®Google Scholar
• Kostine M, Mauric E, Tison A, Barnetche T, Barre A, Nikolski M, Rouxel L, Dutriaux C, Dousset L, Prey S, et al. Baseline co-medications may alter the anti-tumoural effect of checkpoint inhibitors as well as the risk of immune-related adverse events. Eur J Cancer. 2021;157:474–484. doi:10.1016/j.ejca.2021.08.036.
   PubMed Web of Science ®Google Scholar
• Popat S, Liu SV, Scheuer N, Gupta A, Hsu GG, Ramagopalan SV, Griesinger F, Subbiah V. Association between smoking history and overall survival in patients receiving pembrolizumab for first-line treatment of advanced non–small cell lung cancer. JAMA Netw Open. 2022;5(5):e2214046. doi:10.1001/jamanetworkopen.2022.14046.
   PubMed Web of Science ®Google Scholar
• Zhang X, Li H, Lv X, Hu L, Li W, Zi M, He Y. Impact of diets on response to immune checkpoint inhibitors (ICIs) therapy against tumors. Life (Basel). 2022;12(3):409. doi:10.3390/life12030409.
   PubMed Web of Science ®Google Scholar
• Alpuim Costa D, Nobre JG, Batista MV, Ribeiro C, Calle C, Cortes A, Marhold M, Negreiros I, Borralho P, Brito M, et al. Human microbiota and breast cancer—is there any relevant link?—A literature review and new horizons toward personalised Medicine. Front Microbiol. 2021;12:584332. doi:10.3389/fmicb.2021.584332.
   PubMed Web of Science ®Google Scholar
• Simpson RC, Shanahan ER, Scolyer RA, Long GV. Towards modulating the gut microbiota to enhance the efficacy of immune-checkpoint inhibitors. Nat Rev Clin Oncol. 2023;20(10):697–715. doi:10.1038/s41571-023-00803-9.
   PubMed Web of Science ®Google Scholar