Immune-related Adverse Events and Survival in Solid Tumors Treated With Immune Checkpoint Inhibitors: A Systematic Review and Meta-Analysis.


Journal

Journal of immunotherapy (Hagerstown, Md. : 1997)
ISSN: 1537-4513
Titre abrégé: J Immunother
Pays: United States
ID NLM: 9706083

Informations de publication

Date de publication:
01 2020
Historique:
pubmed: 2 10 2019
medline: 2 6 2021
entrez: 2 10 2019
Statut: ppublish

Résumé

Immune-related adverse events (irAEs) are autoimmune-toxic effects associated with immune checkpoint inhibitors (ICIs) used for the treatment of advanced solid tumors. We performed a systematic review and meta-analysis of the published literature to assess the outcome for cancer patients treated with ICIs who develop irAEs. Two independent reviewers selected prospective or retrospective studies from PubMed, EMBASE, and the Cochrane Library database from their inception to November 2018. Data were pooled using hazard ratios (HRs) for overall survival or progression-free survival or odds ratio for overall response rate of irAEs versus no irAEs according to fixed or random-effect model. HRs for OS (the primary outcome measure) were pooled to provide an aggregate value. A total of 30 studies that included a total of 4324 patients treated with ICIs were selected. Patients who developed irAEs presented a reduced risk of death [HR=0.49, 95% confidence interval (CI): 0.38-0.62; P<0.001]. Similarly, the occurrence of irAEs was associated with a reduced risk of progression (HR=0.51, 95% CI: 0.42-0.64; P<0.001). The odds of response was 4.56 (95% CI: 3.72-5.59; P<0.001). In patients treated with ICIs, irAEs predict survival and response. Although this correlation cannot be fully explained, it may be related to the strongest T-cell activation.

Identifiants

pubmed: 31574022
doi: 10.1097/CJI.0000000000000300
pii: 00002371-202001000-00001
doi:

Substances chimiques

Immune Checkpoint Inhibitors 0

Types de publication

Journal Article Meta-Analysis Systematic Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

1-7

Références

Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12:252–264.
Keir ME, Butte MJ, Freeman GJ, et al. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol. 2008;26:677–704.
Wolchok JD, Saenger Y. The mechanism of anti-CTLA-4 activity and the negative regulation of T-cell activation. Oncologist. 2008;13(suppl 4):2–9.
Rittmeyer A, Barlesi F, Waterkamp D, et al. Atezolizumab versus docetaxel in patients with previously treated non-small-cell lung cancer (OAK): a phase 3, open-label, multicentre randomised controlled trial. Lancet. 2017;389:255–265.
Bersanelli M, Brighenti M, Buti S, et al. Patient performance status and cancer immunotherapy efficacy: a meta-analysis. Med Oncol. 2018;35:132.
Conforti F, Pala L, Bagnardi V, et al. Cancer immunotherapy efficacy and patients' sex: a systematic review and meta-analysis. Lancet Oncol. 2018;19:737–746.
Espinosa E, Marquez-Rodas I, Soria A, et al. Predictive factors of response to immunotherapy-a review from the Spanish Melanoma Group (GEM). Ann Transl Med. 2017;5:389.
Luen SJ, Savas P, Fox SB, et al. Tumour-infiltrating lymphocytes and the emerging role of immunotherapy in breast cancer. Pathology. 2017;49:141–155.
Petty AJ, Yang Y. Tumor-associated macrophages: implications in cancer immunotherapy. Immunotherapy. 2017;9:289–302.
Krummel MF, Allison JP. CTLA-4 engagement inhibits IL-2 accumulation and cell cycle progression upon activation of resting T cells. J Exp Med. 1996;183:2533–2540.
Dong H, Strome SE, Salomao DR, et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med. 2002;8:793–800.
Hodi FS, O'Day SJ, McDermott DF, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363:711–723.
Brahmer JR, Tykodi SS, Chow LQ, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med. 2012;366:2455–2465.
Topalian SL, Hodi FS, Brahmer JR, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 2012;366:2443–2454.
Downey SG, Klapper JA, Smith FO, et al. Prognostic factors related to clinical response in patients with metastatic melanoma treated by CTL-associated antigen-4 blockade. Clin Cancer Res. 2007;13(pt 1):6681–6688.
Weber JS, Kahler KC, Hauschild A. Management of immune-related adverse events and kinetics of response with ipilimumab. J Clin Oncol. 2012;30:2691–2697.
Weber JS, Hodi FS, Wolchok JD, et al. Safety profile of nivolumab monotherapy: a pooled analysis of patients with advanced melanoma. J Clin Oncol. 2017;35:785–792.
Haratani K, Hayashi H, Chiba Y, et al. Association of immune-related adverse events with nivolumab efficacy in non-small-cell lung cancer. JAMA Oncol. 2018;4:374–378.
Sato K, Akamatsu H, Murakami E, et al. Correlation between immune-related adverse events and efficacy in non-small cell lung cancer treated with nivolumab. Lung Cancer. 2018;115:71–74.
Teraoka S, Fujimoto D, Morimoto T, et al. Early immune-related adverse events and association with outcome in advanced non-small cell lung cancer patients treated with nivolumab: a prospective cohort study. J Thorac Oncol. 2017;12:1798–1805.
Judd J, Zibelman M, Handorf E, et al. Immune-related adverse events as a biomarker in non-melanoma patients treated with programmed cell death 1 inhibitors. Oncologist. 2017;22:1232–1237.
Hartling L, Milne A, Hamm MP, et al. Testing the Newcastle Ottawa Scale showed low reliability between individual reviewers. J Clin Epidemiol. 2013;66:982–993.
Attia P, Phan GQ, Maker AV, et al. Autoimmunity correlates with tumor regression in patients with metastatic melanoma treated with anti-cytotoxic T-lymphocyte antigen-4. J Clin Oncol. 2005;23:6043–6053.
Beck KE, Blansfield JA, Tran KQ, et al. Enterocolitis in patients with cancer after antibody blockade of cytotoxic T-lymphocyte-associated antigen 4. J Clin Oncol. 2006;24:2283–2289.
Bronstein Y, Ng CS, Hwu P, et al. Radiologic manifestations of immune-related adverse events in patients with metastatic melanoma undergoing anti-CTLA-4 antibody therapy. AJR Am J Roentgenol. 2011;197:W992–W1000.
Dick J, Lang N, Slynko A, et al. Use of LDH and autoimmune side effects to predict response to ipilimumab treatment. Immunotherapy. 2016;8:1033–1044.
Freeman-Keller M, Kim Y, Cronin H, et al. Nivolumab in resected and unresectable metastatic melanoma: characteristics of immune-related adverse events and association with outcomes. Clin Cancer Res. 2016;22:886–894.
Grangeon M, Tomasini P, Chaleat S, et al. Association between immune-related adverse events and efficacy of immune checkpoint inhibitors in non-small-cell lung cancer. Clin Lung Cancer. 2018;20:201–207.
Horvat TZ, Adel NG, Dang TO, et al. Immune-related adverse events, need for systemic immunosuppression, and effects on survival and time to treatment failure in patients with melanoma treated with ipilimumab at memorial sloan kettering cancer center. J Clin Oncol. 2015;33:3193–3198.
Hua C, Boussemart L, Mateus C, et al. Association of vitiligo with tumor response in patients with metastatic melanoma treated with pembrolizumab. JAMA Dermatol. 2016;152:45–51.
Kim HI, Kim M, Lee SH, et al. Development of thyroid dysfunction is associated with clinical response to PD-1 blockade treatment in patients with advanced non-small cell lung cancer. Oncoimmunology. 2017;7:e1375642.
Kostine M, Rouxel L, Barnetche T, et al. Rheumatic disorders associated with immune checkpoint inhibitors in patients with cancer-clinical aspects and relationship with tumour response: a single-centre prospective cohort study. Ann Rheum Dis. 2018;77:393–398.
Ksienski D, Wai ES, Croteau N, et al. Efficacy of nivolumab and pembrolizumab in patients with advanced non-small-cell lung cancer needing treatment interruption because of adverse events: a retrospective multicenter analysis. Clin Lung Cancer. 2019;20:e97–e106.
Lesueur P, Escande A, Thariat J, et al. Safety of combined PD-1 pathway inhibition and radiation therapy for non-small-cell lung cancer: a multicentric retrospective study from the GFPC. Cancer Med. 2018;7:5505–5513.
Lisberg A, Tucker DA, Goldman JW, et al. Treatment-related adverse events predict improved clinical outcome in NSCLC patients on KEYNOTE-001 at a single center. Cancer Immunol Res. 2018;6:288–294.
Min Lee CK, Li S, Tran DC, et al. Characterization of dermatitis after PD-1/PD-L1 inhibitor therapy and association with multiple oncologic outcomes: a retrospective case-control study. J Am Acad Dermatol. 2018;79:1047–1052.
Nakamura Y, Kitano S, Takahashi A, et al. Nivolumab for advanced melanoma: pretreatment prognostic factors and early outcome markers during therapy. Oncotarget. 2016;7:77404–77415.
Osorio JC, Ni A, Chaft JE, et al. Antibody-mediated thyroid dysfunction during T-cell checkpoint blockade in patients with non-small-cell lung cancer. Ann Oncol. 2017;28:583–589.
Owen DH, Wei L, Bertino EM, et al. Incidence, risk factors, and effect on survival of immune-related adverse events in patients with non-small-cell lung cancer. Clin Lung Cancer. 2018;19:e893–e900.
Sanlorenzo M, Vujic I, Daud A, et al. Pembrolizumab cutaneous adverse events and their association with disease progression. JAMA Dermatol. 2015;151:1206–1212.
Shafqat H, Gourdin T, Sion A. Immune-related adverse events are linked with improved progression-free survival in patients receiving anti-PD-1/PD-L1 therapy. Semin Oncol. 2018;45:156–163.
Suh KJ, Kim SH, Kim YJ, et al. Post-treatment neutrophil-to-lymphocyte ratio at week 6 is prognostic in patients with advanced non-small cell lung cancers treated with anti-PD-1 antibody. Cancer Immunol Immunother. 2018;67:459–470.
Toi Y, Sugawara S, Kawashima Y, et al. Association of immune-related adverse events with clinical benefit in patients with advanced non-small-cell lung cancer treated with nivolumab. Oncologist. 2018;23:1358–1365.
Yamazaki N, Kiyohara Y, Uhara H, et al. Efficacy and safety of nivolumab in Japanese patients with previously untreated advanced melanoma: a phase II study. Cancer Sci. 2017;108:1223–1230.
Indini A, Di Guardo L, Cimminiello C, et al. Immune-related adverse events correlate with improved survival in patients undergoing anti-PD1 immunotherapy for metastatic melanoma. J Cancer Res Clin Oncol. 2019;145:511–521.
Okada N, Kawazoe H, Takechi K, et al. Association between immune-related adverse events and clinical efficacy in patients with melanoma treated with nivolumab: a multicenter retrospective study. Clin Ther. 2019;41:59–67.
Petrelli F, Borgonovo K, Cabiddu M, et al. Relationship between skin rash and outcome in non-small-cell lung cancer patients treated with anti-EGFR tyrosine kinase inhibitors: a literature-based meta-analysis of 24 trials. Lung Cancer. 2012;78:8–15.
Borcoman E, Nandikolla A, Long G, et al. Patterns of response and progression to immunotherapy. Am Soc Clin Oncol Educ Book. 2018;38:169–178.
Brahmer JR, Lacchetti C, Thompson JA. Management of immune-related adverse events in patients treated with immune checkpoint inhibitor therapy: American Society of Clinical Oncology Clinical Practice Guideline Summary. J Oncol Pract. 2018;14:247–249.
Haanen J, Carbonnel F, Robert C, et al. Management of toxicities from immunotherapy: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2017;28(suppl 4):iv119–iv142.
Schadendorf D, Wolchok JD, Hodi FS, et al. Efficacy and safety outcomes in patients with advanced melanoma who discontinued treatment with nivolumab and ipilimumab because of adverse events: a pooled analysis of randomized phase II and III trials. J Clin Oncol. 2017;35:3807–3814.
Tachihara M, Negoro S, Inoue T, et al. Efficacy of anti-PD-1/PD-L1 antibodies after discontinuation due to adverse events in non-small cell lung cancer patients (HANSHIN 0316). BMC Cancer. 2018;18:946.
Martini DJ, Hamieh L, McKay RR, et al. Durable clinical benefit in metastatic renal cell carcinoma patients who discontinue PD-1/PD-L1 therapy for immune-related adverse events. Cancer Immunol Res. 2018;6:402–408.
Postow MA, Sidlow R, Hellmann MD. Immune-related adverse events associated with immune checkpoint blockade. N Engl J Med. 2018;378:158–168.
Lynch SA, Bouchard BN, Vijayasaradhi S, et al. Antigens of melanocytes and melanoma. Cancer Metastasis Rev. 1991;10:141–150.
Rosenberg SA, White DE. Vitiligo in patients with melanoma: normal tissue antigens can be targets for cancer immunotherapy. J Immunother Emphasis Tumor Immunol. 1996;19:81–84.
Naidoo J, Wang X, Woo KM, et al. Pneumonitis in patients treated with anti-programmed death-1/programmed death ligand 1 therapy. J Clin Oncol. 2017;35:709–717.
Wang DY, Salem JE, Cohen JV, et al. Fatal toxic effects associated with immune checkpoint inhibitors: a systematic review and meta-analysis. JAMA Oncol. 2018;4:1721–1728.
Xu C, Chen YP, Du XJ, et al. Comparative safety of immune checkpoint inhibitors in cancer: systematic review and network meta-analysis. BMJ. 2018;363:k4226.
Bertrand A, Kostine M, Barnetche T, et al. Immune related adverse events associated with anti-CTLA-4 antibodies: systematic review and meta-analysis. BMC Med. 2015;13:211.

Auteurs

Fausto Petrelli (F)

Oncology Unit, ASST Bergamo Ovest, Treviglio (BG).

Giulia Grizzi (G)

Oncology Unit, ASST Cremona, Cremona.

Michele Ghidini (M)

Medical Oncology Unit, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico.

Antonio Ghidini (A)

Oncology Unit, Casa di cura Igea, Milan.

Margherita Ratti (M)

Oncology Unit, ASST Cremona, Cremona.

Stefano Panni (S)

Oncology Unit, ASST Cremona, Cremona.

Mary Cabiddu (M)

Oncology Unit, ASST Bergamo Ovest, Treviglio (BG).

Mara Ghilardi (M)

Oncology Unit, ASST Bergamo Ovest, Treviglio (BG).

Karen Borgonovo (K)

Oncology Unit, ASST Bergamo Ovest, Treviglio (BG).

Maria C Parati (MC)

Oncology Unit, ASST Bergamo Ovest, Treviglio (BG).

Gianluca Tomasello (G)

Oncology Unit, ASST Cremona, Cremona.

Sandro Barni (S)

Oncology Unit, ASST Bergamo Ovest, Treviglio (BG).

Alfredo Berruti (A)

Department of Medical and Surgical Specialties, Radiological Sciences, and Public Health, Medical Oncology, University of Brescia at ASST-Spedali Civili, Brescia, Italy.

Matteo Brighenti (M)

Oncology Unit, ASST Cremona, Cremona.

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