Immune-related ocular toxicities in solid tumor patients treated with immune checkpoint inhibitors: a systematic review

References

• Eggermont AM, Chiarion-Sileni V, Grob -J-J, et al. Adjuvant ipilimumab versus placebo after complete resection of high-risk stage III melanoma (EORTC 18071): a randomised, double-blind, phase 3 trial. Lancet Oncol. 2015;16(5):522–530.
   PubMed Web of Science ®Google Scholar
• Voena C, Chiarle R. Advances in cancer immunology and cancer immunotherapy. Discov Med. 2016;21(114):125–133.
   PubMed Web of Science ®Google Scholar
• Motzer RJ, Escudier B, McDermott DF, et al. Nivolumab versus everolimus in advanced renal-cell carcinoma. N Engl J Med. 2015;373(19):1803–1813.
   PubMed Web of Science ®Google Scholar
• Seetharamu N, Budman DR, Sullivan KM. Immune checkpoint inhibitors in lung cancer: past, present and future. Future Oncol. 2016;12(9):1151–1163.
   PubMed Web of Science ®Google Scholar
• Sgambato A, Casaluce F, Sacco PC, et al. 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. 2016;11(1):62–68.
   PubMed Web of Science ®Google Scholar
• Pilotto S, Kinspergher S, Peretti U, et al. Immune checkpoint inhibitors for non-small-cell lung cancer: does that represent a ‘new frontier’?. Anticancer Agents Med Chem. 2015;15(3):307–313.
   PubMed Web of Science ®Google Scholar
• Intlekofer AM, Thompson CB. At the bench: preclinical rationale for CTLA-4 and PD-1 blockade as cancer immunotherapy. J Leukoc Biol. 2013;94(1):25–39.
   PubMed Web of Science ®Google Scholar
• Hodi FS, O’Day SJ, McDermott DF, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363(8):711–723.
   PubMed Web of Science ®Google Scholar
• Garon EB, Rizvi NA, Hui R, et al. Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med. 2015;372(21):2018–2028.
   PubMed Web of Science ®Google Scholar
• Brahmer J, Reckamp KL, Baas P, et al. Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med. 2015;373(2):123–135.
   PubMed Web of Science ®Google Scholar
• Fehrenbacher L, Spira A, Ballinger M, et al. Atezolizumab versus docetaxel for patients with previously treated non-small-cell lung cancer (POPLAR): a multicentre, open-label, phase 2 randomised controlled trial. The Lancet. 2016;387(10030):1837–1846.
   Web of Science ®Google Scholar
• Abdel-Rahman O, ElHalawani H, Fouad M. Risk of cutaneous toxicities in patients with solid tumors treated with immune checkpoint inhibitors: a meta-analysis. Future Oncol. 2015;11(17):2471–2484.
   Web of Science ®Google Scholar
• Abdel-Rahman O, ElHalawani H, Fouad M. Risk of elevated transaminases in cancer patients treated with immune checkpoint inhibitors: a meta-analysis. Expert Opin Drug Saf. 2015;14(10):1507–1518.
   PubMed Web of Science ®Google Scholar
• Abdel-Rahman O, ElHalawani H, Fouad M. Risk of endocrine complications in cancer patients treated with immune check point inhibitors: a meta-analysis. Future Oncol. 2016;12(3):413–425.
   PubMed Web of Science ®Google Scholar
• Abdel-Rahman O, ElHalawani H, Fouad M. Risk of gastrointestinal complications in cancer patients treated with immune checkpoint inhibitors: a meta-analysis. Immunotherapy. 2015;7(11):1213–1227.
   PubMed Web of Science ®Google Scholar
• Abdel-Rahman O, Fouad M. Risk of pneumonitis in cancer patients treated with immune checkpoint inhibitors: a meta-analysis. Ther Adv Respir Dis. 2016;10:183–193.
   PubMed Web of Science ®Google Scholar
• Abdel-Rahman O, Helbling D, Schmidt J, et al. Treatment-related death in cancer patients treated with immune checkpoint inhibitors: a systematic review and meta-analysis. Clin Oncol (R Coll Radiol). 2016. Doi:10.1016/j.clon.2016.11.007.
   Google Scholar
• Abdel-Rahman O, Fouad M. A network meta-analysis of the risk of immune-related renal toxicity in cancer patients treated with immune checkpoint inhibitors. Immunotherapy. 2016;8(5):665–674.
   PubMed Web of Science ®Google Scholar
• Abdel-Rahman O, Helbling D, Schmidt J, et al. Treatment-associated fatigue in cancer patients treated with immune checkpoint inhibitors; a systematic review and meta-analysis. Clin Oncol (R Coll Radiol). 2016;28(10):e127–38.
   PubMed Web of Science ®Google Scholar
• Higgins JPT, Green S (editors). Cochrane handbook for systematic reviews of interventions version 5.1.0 [updated March 2011]. The Cochrane Collaboration, 2011. Available from: www.cochrane-handbook.org.
   Google Scholar
• DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–188.
   PubMedGoogle Scholar
• Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ: Br Med J. 2003;327(7414):557.
   PubMed Web of Science ®Google Scholar
• Kwon ED, Drake CG, Scher HI, et al. Ipilimumab versus placebo after radiotherapy in patients with metastatic castration-resistant prostate cancer that had progressed after docetaxel chemotherapy (CA184-043): a multicentre, randomised, double-blind, phase 3 trial. Lancet Oncol. 2014;15(7):700–712.
   PubMed Web of Science ®Google Scholar
• Robert C, Schachter J, Long GV, et al. Pembrolizumab versus ipilimumab in advanced melanoma. N Engl J Med. 2015;372(26):2521–2532.
   PubMed Web of Science ®Google Scholar
• Gibney GT, Kudchadkar RR, DeConti RC, et al. Safety, correlative markers, and clinical results of adjuvant nivolumab in combination with vaccine in resected high-risk metastatic melanoma. Clin Cancer Res. 2015;21(4):712–720.
   PubMed Web of Science ®Google Scholar
• Wolchok JD, Kluger H, Callahan MK, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med. 2013;369(2):122–133.
   PubMed Web of Science ®Google Scholar
• Weber J, Gibney G, Kudchadkar R, et al. Phase I/II study of metastatic melanoma patients treated with nivolumab who had progressed after ipilimumab. Cancer Immunol Res. 2016;4(4):345–353.
   PubMed Web of Science ®Google Scholar
• Ribas A, Kefford R, Marshall MA, et al. Phase III randomized clinical trial comparing tremelimumab with standard-of-care chemotherapy in patients with advanced melanoma. J Clin Oncol. 2013;31(5):616–622.
   PubMed Web of Science ®Google Scholar
• Ribas A, Puzanov I, Dummer R, et al. Pembrolizumab versus investigator-choice chemotherapy for ipilimumab-refractory melanoma (KEYNOTE-002): a randomised, controlled, phase 2 trial. Lancet Oncol. 2015;16(8):908–918.
   PubMed Web of Science ®Google Scholar
• Herbst RS, Baas P, Kim DW, et al. Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer (KEYNOTE-010): a randomised controlled trial. Lancet (London, England). 2016;387(10027):1540–1550.
   PubMed Web of Science ®Google Scholar
• Ribas A, Hamid O, Daud A, et al. Association of pembrolizumab with tumor response and survival among patients with advanced melanoma. Jama. 2016;315(15):1600–1609.
   PubMed Web of Science ®Google Scholar
• Hamid O, Robert C, Daud A, et al. Safety and tumor responses with lambrolizumab (anti–PD-1) in melanoma. N Engl J Med. 2013;369(2):134–144.
   PubMed Web of Science ®Google Scholar
• Robert C, Ribas A, Wolchok JD, et al. Anti-programmed-death-receptor-1 treatment with pembrolizumab in ipilimumab-refractory advanced melanoma: a randomised dose-comparison cohort of a phase 1 trial. The Lancet. 2014;384(9948):1109–1117.
   PubMed Web of Science ®Google Scholar
• Goldberg SB, Gettinger SN, Mahajan A, et al. Pembrolizumab for patients with melanoma or non-small-cell lung cancer and untreated brain metastases: early analysis of a non-randomised, open-label, phase 2 trial. Lancet Oncol. 2016;17(7):976–983.
   PubMed Web of Science ®Google Scholar
• Seiwert TY, Burtness B, Mehra R, et al. Safety and clinical activity of pembrolizumab for treatment of recurrent or metastatic squamous cell carcinoma of the head and neck (KEYNOTE-012): an open-label, multicentre, phase 1b trial. Lancet Oncol. 2016;17(7):956–965.
   PubMed Web of Science ®Google Scholar
• Taube JM, Klein A, Brahmer JR, et al. Association of PD-1, PD-1 ligands, and other features of the tumor immune microenvironment with response to anti-PD-1 therapy. Clin Cancer Res. 2014;20(19):5064–5074.
   PubMed Web of Science ®Google Scholar
• Borghaei H, Paz-Ares L, Horn L, et al. Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer. N Engl J Med. 2015;373(17):1627–1639.
   PubMed Web of Science ®Google Scholar
• Hamanishi J, Mandai M, Ikeda T, et al. Safety and antitumor activity of anti–pd-1 antibody, nivolumab, in patients with platinum-resistant ovarian cancer. J Clin Oncol. 2015;33(34):4015–4022.
   PubMed Web of Science ®Google Scholar
• Larkin J, Chiarion-Sileni V, Gonzalez R, et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. New England J Med. 2015;373(1):23–34.
   PubMed Web of Science ®Google Scholar
• Gettinger SN, Hellmann MD, Shepherd FA, et al., editors. First-line monotherapy with nivolumab (NIVO; anti-programmed death-1 [PD-1]) in advanced non-small cell lung cancer (NSCLC): safety, efficacy and correlation of outcomes with PD-1 ligand (PD-L1) expression. ASCO Annual Meeting Proceedings; 2015.
   Google Scholar
• Postow MA, Chesney J, Pavlick AC, et al. Nivolumab and ipilimumab versus ipilimumab in untreated melanoma. N Engl J Med. 2015;372(21):2006–2017.
   PubMed Web of Science ®Google Scholar
• Weber JS, D’Angelo SP, Minor D, et al. Nivolumab versus chemotherapy in patients with advanced melanoma who progressed after anti-CTLA-4 treatment (CheckMate 037): a randomised, controlled, open-label, phase 3 trial. Lancet Oncol. 2015;16(4):375–384.
   PubMed Web of Science ®Google Scholar
• McDermott DF, Drake CG, Sznol M, et al. Survival, durable response, and long-term safety in patients with previously treated advanced renal cell carcinoma receiving nivolumab. J Clin Oncol. 2015;33(18):2013–2020.
   PubMed Web of Science ®Google Scholar
• Rizvi NA, Mazieres J, Planchard D, et al. Activity and safety of nivolumab, an anti-PD-1 immune checkpoint inhibitor, for patients with advanced, refractory squamous non-small-cell lung cancer (CheckMate 063): a phase 2, single-arm trial. Lancet Oncol. 2015;16(3):257–265.
   PubMed Web of Science ®Google Scholar
• Robert C, Long GV, Brady B, et al. Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med. 2015;372(4):320–330.
   PubMed Web of Science ®Google Scholar
• Topalian SL, Sznol M, McDermott DF, et al. Survival, durable tumor remission, and long-term safety in patients with advanced melanoma receiving nivolumab. J Clin Oncol. 2014;32(10):1020–1030.
   PubMed Web of Science ®Google Scholar
• Joshua AM, Monzon JG, Mihalcioiu C, et al. A phase 2 study of tremelimumab in patients with advanced uveal melanoma. Melanoma Res. 2015;25(4):342–347.
   PubMed Web of Science ®Google Scholar
• Calabrò L, Morra A, Fonsatti E, et al. Efficacy and safety of an intensified schedule of tremelimumab for chemotherapy-resistant malignant mesothelioma: an open-label, single-arm, phase 2 study. Lancet Respir Med. 2015;3(4):301–309.
   PubMed Web of Science ®Google Scholar
• Sangro B, Gomez-Martin C, De La Mata M, et al. A clinical trial of CTLA-4 blockade with tremelimumab in patients with hepatocellular carcinoma and chronic hepatitis C. J Hepatol. 2013;59(1):81–88.
   PubMed Web of Science ®Google Scholar
• Chung KY, Gore I, Fong L, et al. Phase II study of the anti-cytotoxic t-lymphocyte–associated antigen 4 monoclonal antibody, tremelimumab, in patients with refractory metastatic colorectal cancer. J Clin Oncol. 2010;28(21):3485–3490.
   PubMed Web of Science ®Google Scholar
• Rosenberg JE, Hoffman-Censits J, Powles T, et al. Atezolizumab in patients with locally advanced and metastatic urothelial carcinoma who have progressed following treatment with platinum-based chemotherapy: a single-arm, multicentre, phase 2 trial. The Lancet. 2016;387(10031):1909–1920.
   PubMed Web of Science ®Google Scholar
• Yamazaki N, Kiyohara Y, Uhara H, et al. Phase II study of ipilimumab monotherapy in Japanese patients with advanced melanoma. Cancer Chemother Pharmacol. 2015;76(5):997–1004.
   PubMed Web of Science ®Google Scholar
• Yamazaki N, Uhara H, Fukushima S, et al. Phase II study of the immune-checkpoint inhibitor ipilimumab plus dacarbazine in Japanese patients with previously untreated, unresectable or metastatic melanoma. Cancer Chemother Pharmacol. 2015;76(5):969–975.
   PubMed Web of Science ®Google Scholar
• Zimmer L, Vaubel J, Mohr P, et al. Phase II decog-study of ipilimumab in pretreated and treatment-naïve patients with metastatic uveal melanoma. PLoS One. 2015;10(3):e0118564.
   PubMed Web of Science ®Google Scholar
• Hodi FS, Lee S, McDermott DF, et al. Sargramostim plus ipilimumab vs ipilimumab alone for treatment of metastatic melanoma: a randomized clinical trial. JAMA. 2014;312(17):1744–1753.
   PubMed Web of Science ®Google Scholar
• Hodi FS, Lawrence D, Lezcano C, et al. Bevacizumab plus ipilimumab in patients with metastatic melanoma. Cancer Immunol Res. 2014;2(7):632–642.
   PubMed Web of Science ®Google Scholar
• Jochems C, Tucker JA, Tsang K-Y, et al. A combination trial of vaccine plus ipilimumab in metastatic castration-resistant prostate cancer patients: immune correlates. Ancer Immunol Immunother. 2014;63(4):407–418.
   PubMed Web of Science ®Google Scholar
• Lynch TJ, Bondarenko I, Luft A, et al. Ipilimumab in combination with paclitaxel and carboplatin as first-line treatment in stage IIIB/IV non–small-cell lung cancer: results from a randomized, double-blind, multicenter phase II study. J Clin Oncol. 2012;30(17):2046–2054.
   PubMed Web of Science ®Google Scholar
• Reck M, Bondarenko I, Luft A, et al. Ipilimumab in combination with paclitaxel and carboplatin as first-line therapy in extensive-disease-small-cell lung cancer: results from a randomized, double-blind, multicenter phase 2 trial. Ann Oncol. 2013;24(1):75–83.
   PubMed Web of Science ®Google Scholar
• Margolin K, Ernstoff MS, Hamid O, et al. Ipilimumab in patients with melanoma and brain metastases: an open-label, phase 2 trial. Lancet Oncol. 2012;13(5):459–465.
   PubMed Web of Science ®Google Scholar
• Madan RA, Mohebtash M, Arlen PM, et al. Ipilimumab and a poxviral vaccine targeting prostate-specific antigen in metastatic castration-resistant prostate cancer: a phase 1 dose-escalation trial. Lancet Oncol. 2012;13(5):501–508.
   PubMed Web of Science ®Google Scholar
• Robert C, Thomas L, Bondarenko I, et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med. 2011;364(26):2517–2526.
   PubMed Web of Science ®Google Scholar
• Royal RE, Levy C, Turner K, et al. Phase 2 trial of single agent ipilimumab (anti-ctla-4) for locally advanced or metastatic pancreatic adenocarcinoma. J Immunother. 2010;33(8):828–833.
   PubMed Web of Science ®Google Scholar
• Basilious A, Lloyd JC. Posterior subcapsular cataracts and hypotony secondary to severe pembrolizumab induced uveitis: case report. Can J Ophthalmol. 2016;51(1):e4–e6.
   PubMed Web of Science ®Google Scholar
• Abu Samra K, Valdes-Navarro M, Lee S, et al. A case of bilateral uveitis and papillitis in a patient treated with pembrolizumab. Eur J Ophthalmol. 2016;26(3):e46–8. doi:10.5301/ejo.5000724.
   Google Scholar
• Zimmer L, Goldinger SM, Hofmann L, et al. Neurological, respiratory, musculoskeletal, cardiac and ocular side-effects of anti-PD-1 therapy. Eur J Cancer. 2016;60:210–225.
   PubMed Web of Science ®Google Scholar
• Hahn L, Pepple KL. Bilateral neuroretinitis and anterior uveitis following ipilimumab treatment for metastatic melanoma. J Ophthalmic Inflamm Infect. 2016;6:14.
   PubMed Web of Science ®Google Scholar
• Fierz FC, Meier F, Chaloupka K, et al. Intraocular inflammation associated with new therapies for cutaneous melanoma – case series and review. Klin Monatsbl Augenheilkd. 2016;233(04):540–544.
   PubMed Web of Science ®Google Scholar
• Hanna KS. A rare case of pembrolizumab-induced uveitis in a patient with metastatic melanoma. Pharmacotherapy. 2016;36:e183-e188.
   PubMed Web of Science ®Google Scholar
• Aaberg MT, Aaberg TM Jr. Pembrolizumab administration associated with posterior uveitis. Retin Cases Brief Rep. 2016. [Epub ahead of print].
   PubMedGoogle Scholar
• Arai T, Harada K, Usui Y, et al. Case of acute anterior uveitis and Vogt-Koyanagi-Harada syndrome-like eruptions induced by nivolumab in a melanoma patient. J Dermatol. 2016 doi: 10.1111/1346-8138.13612. [Epub ahead of print]
   Google Scholar
• Karlin J, Gentzler R, Golen J. Bilateral anterior uveitis associated with nivolumab therapy. Ocul Immunol Inflamm. 2016;1–3. [Epub ahead of print].
   PubMedGoogle Scholar
• De Velasco G, Bermas B, Choueiri TK. Autoimmune arthropathy and uveitis as complications of programmed death 1 inhibitor treatment. Arthritis Rheum (Hoboken, NJ). 2016;68(2):556–557.
   PubMed Web of Science ®Google Scholar
• Miserocchi E, Cimminiello C, Mazzola M, et al. New-onset uveitis during CTLA-4 blockade therapy with ipilimumab in metastatic melanoma patient. Can J Ophthalmol. 2015;50(1):e2–4.
   PubMed Web of Science ®Google Scholar
• Nallapaneni NN, Mourya R, Bhatt VR, et al. Ipilimumab-induced hypophysitis and uveitis in a patient with metastatic melanoma and a history of ipilimumab-induced skin rash. J Natl Compr Canc Netw. 2014;12(8):1077–1081.
   PubMed Web of Science ®Google Scholar
• Roberts P, Fishman GA, Joshi K, et al. Chorioretinal lesions in a case of melanoma-associated retinopathy treated with pembrolizumab. JAMA Ophthalmol. 2016;134(10):1184–1188.
   PubMed Web of Science ®Google Scholar
• Nguyen BH, Kuo J, Budiman A, et al. Two cases of clinical myasthenia gravis associated with pembrolizumab use in responding melanoma patients. Melanoma Res. 2016. [Epub ahead of print].
   PubMedGoogle Scholar
• Papavasileiou E, Prasad S, Freitag SK, et al. Ipilimumab-induced ocular and orbital inflammation–a case series and review of the literature. Ocul Immunol Inflamm. 2016;24(2):140–146.
   PubMed Web of Science ®Google Scholar
• Weber JS, Kähler KC, Hauschild A. Management of immune-related adverse events and kinetics of response with ipilimumab. J Clin Oncol. 2012;30(21):2691–2697.
   PubMed Web of Science ®Google Scholar
• Nguyen AT, Elia M, Materin MA, et al. Cyclosporine for dry eye associated with nivolumab: a case progressing to corneal perforation. Cornea. 2016;35(3):399–401.
   PubMed Web of Science ®Google Scholar
• Antoun J, Titah C, Cochereau I. Ocular and orbital side-effects of checkpoint inhibitors: a review article. Curr Opin Oncol. 2016;28(4):288–294.
   PubMed Web of Science ®Google Scholar
• Orloff M, Weight R, Valsecchi ME, et al. Immune check point inhibitors combination in melanoma: worth the toxicity? Rev Recent Clin Trials. 2016;11(2):81–86.
   PubMed Web of Science ®Google Scholar
• Diem S, Keller F, Ruesch R, et al. Pembrolizumab-triggered uveitis: an additional surrogate marker for responders in melanoma immunotherapy? J Immunother. 2016;39(9):379–382.
   PubMed Web of Science ®Google Scholar