Immune checkpoint inhibitors and endocrine side effects, a narrative review

References

• Sharma P, Allison JP. The future of immune checkpoint therapy. Science. 2015;348(6230):56–61.
   PubMed Web of Science ®Google Scholar
• Chang LS, Barroso-Sousa R, Tolaney SM, et al. Endocrine toxicity of cancer immunotherapy targeting immune checkpoints. Endocr Rev. 2019;40(1):17–65.
   PubMed Web of Science ®Google Scholar
• Herzberg B, Fisher DE. Metastatic melanoma and immunotherapy. Clin Immunol. 2016;172:105–110.
   PubMed Web of Science ®Google Scholar
• Qin A, Coffey DG, Warren EH, et al. Mechanisms of immune evasion and current status of checkpoint inhibitors in non-small cell lung cancer. Cancer Med. 2016;5(9):2567–2578.
   PubMed Web of Science ®Google Scholar
• Coley WB. The treatment of inoperable sarcoma by bacterial toxins (the Mixed Toxins of the Streptococcus erysipelas and the Bacillus prodigiosus). Proc R Soc Med. 1910;3(SurgSect):1–48.
   PubMedGoogle Scholar
• Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12(4):252–264.
   PubMed Web of Science ®Google Scholar
• Chen L. Co-inhibitory molecules of the B7-CD28 family in the control of T-cell immunity. Nat Rev Immunol. 2004;4(5):336–347.
   PubMed Web of Science ®Google Scholar
• FS H, SJ O, DF M, 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
• 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(4):247–249.
   PubMed Web of Science ®Google Scholar
• Ueda H, Howson JMM, Esposito L, et al. Association of the T-cell regulatory gene CTLA4 with susceptibility to autoimmune disease. Nature. 2003;423(6939):506–511.
   PubMed Web of Science ®Google Scholar
• Schubert D, Bode C, Kenefeck R, et al. Autosomal-dominant immune dysregulation syndrome in humans with CTLA4 mutations. Nat Med. 2014;20(12):1410–1416.
   PubMed Web of Science ®Google Scholar
• Waterhouse P, Penninger JM, Timms E, et al. Lymphoproliferative disorders with early lethality in mice deficient in Ctla-4. Science. 1995;270(5238):985.
   PubMed Web of Science ®Google Scholar
• Blansfield JA, Beck KE, Tran K, et al. Cytotoxic T-lymphocyte–associated antigen-4 blockage can induce autoimmune hypophysitis in patients with metastatic melanoma and renal cancer. J Immunother. 2005;28(6):593.
   PubMed Web of Science ®Google Scholar
• Corsello SM, Barnabei A, Marchetti P, et al. Endocrine side effects induced by immune checkpoint inhibitors. J Clin Endocrinol Metab. 2013;98(4):1361–1375.
   PubMed Web of Science ®Google Scholar
• Fecher LA, Agarwala SS, Hodi FS, et al. Ipilimumab and its toxicities: a multidisciplinary approach. Oncologist. 2013;18(6):733–743.
   PubMed Web of Science ®Google Scholar
• 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(3):583–589.
   PubMed Web of Science ®Google Scholar
• Postow MA, Sidlow R, Hellmann MD. Immune-related adverse events associated with immune checkpoint blockade. N Engl J Med. 2018;378(2):158–168.
   PubMed Web of Science ®Google Scholar
• Menzies AM, Johnson DB, Ramanujam S, et al. Anti-PD-1 therapy in patients with advanced melanoma and preexisting autoimmune disorders or major toxicity with ipilimumab. Ann Oncol. 2017;28(2):368–376.
   PubMed Web of Science ®Google Scholar
• Johnson DB, Sullivan RJ, Ott PA, et al. Ipilimumab therapy in patients with advanced melanoma and preexisting autoimmune disorders. JAMA Oncol. 2016;2(2):234–240.
   PubMed Web of Science ®Google Scholar
• Pantuck M, McDermott D, Drakaki A. To treat or not to treat: patient exclusion in immune oncology clinical trials due to preexisting autoimmune disease. Cancer. 2019;125(20):3506–3513.
   PubMed Web of Science ®Google Scholar
• 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(7):785–792.
   PubMed Web of Science ®Google Scholar
• 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(28):3193–3198.
   PubMed Web of Science ®Google Scholar
• Del Castillo M, Romero FA, Arguello E, et al. The spectrum of serious infections among patients receiving immune checkpoint blockade for the treatment of melanoma. Clin Infect Dis. 2016;63(11):1490–1493.
   PubMed Web of Science ®Google Scholar
• Pennock GK, Chow LQ. The evolving role of immune checkpoint inhibitors in cancer treatment. Oncologist. 2015;20(7):812–822.
   PubMed Web of Science ®Google Scholar
• Ryder M, Callahan M, Postow MA, et al. Endocrine-related adverse events following ipilimumab in patients with advanced melanoma: a comprehensive retrospective review from a single institution. Endocr Relat Cancer. 2014;21(2):371–381.
   PubMed Web of Science ®Google Scholar
• Khair DO, Bax HJ, Mele S, et al. Combining immune checkpoint inhibitors: established and emerging targets and strategies to improve outcomes in melanoma. Front Immunol. 2019;10:453.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Chen C, Zhang X, et al. Immune-checkpoint inhibitor plus chemotherapy versus conventional chemotherapy for first-line treatment in advanced non-small cell lung carcinoma: a systematic review and meta-analysis. J Immunother Cancer. 2018;6(1):155.
   PubMedGoogle Scholar
• Rassy E, Bakouny Z, Assi T, et al. The interaction of immune checkpoint inhibitor plus chemotherapy in non-small-cell lung cancer: subadditivity, additivity or synergism? Immunotherapy. 2019;11(10):913–920.
   PubMed Web of Science ®Google Scholar
• Iglesias P. Cancer immunotherapy-induced endocrinopathies: clinical behavior and therapeutic approach. Eur J Intern Med. 2018;47:6–13.
   PubMed Web of Science ®Google Scholar
• Mahzari M, Liu D, Arnaout A, et al. Immune checkpoint inhibitor therapy associated hypophysitis. Clin Med Insights Endocrinol Diabetes. 2015;8:21–28.
   PubMed Web of Science ®Google Scholar
• Spain L, Diem S, Larkin J. Management of toxicities of immune checkpoint inhibitors. Cancer Treat Rev. 2016;44:51–60.
   PubMed Web of Science ®Google Scholar
• Faje A, Reynolds K, Zubiri L, et al. Hypophysitis secondary to nivolumab and pembrolizumab is a clinical entity distinct from ipilimumab-associated hypophysitis. Eur J Endocrinol. 2019;181:211–219.
   PubMed Web of Science ®Google Scholar
• Byun DJ, Wolchok JD, Rosenberg LM, et al. Cancer immunotherapy - immune checkpoint blockade and associated endocrinopathies. Nat Rev Endocrinol. 2017;13(4):195–207.
   PubMed Web of Science ®Google Scholar
• Okano Y, Satoh T, Horiguchi K, et al. Nivolumab-induced hypophysitis in a patient with advanced malignant melanoma. Endocr J. 2016;63(10):905–912.
   PubMed Web of Science ®Google Scholar
• Joshi MN, Whitelaw BC, Palomar MT, et al. Immune checkpoint inhibitor-related hypophysitis and endocrine dysfunction: clinical review. Clin Endocrinol (Oxf). 2016;85(3):331–339.
   PubMed Web of Science ®Google Scholar
• Konda B, Nabhan F, Shah MH. Endocrine dysfunction following immune checkpoint inhibitor therapy. Curr Opin Endocrinol Diabetes Obes. 2017;24(5):337–347.
   PubMed Web of Science ®Google Scholar
• Sznol M, Postow MA, Davies MJ, et al. Endocrine-related adverse events associated with immune checkpoint blockade and expert insights on their management. Cancer Treat Rev. 2017;58:70–76.
   PubMed Web of Science ®Google Scholar
• Chodakiewitz Y, Brown S, Boxerman JL, et al. Ipilimumab treatment associated pituitary hypophysitis: clinical presentation and imaging diagnosis. Clin Neurol Neurosurg. 2014;125:125–130.
   PubMed Web of Science ®Google Scholar
• Widmann G, Nguyen VA, Plaickner J, et al. Imaging features of toxicities by immune checkpoint inhibitors in cancer therapy. Curr Radiol Rep. 2016;5(11):59.
   PubMedGoogle Scholar
• Albarel F, Gaudy C, Castinetti F, et al. Long-term follow-up of ipilimumab-induced hypophysitis, a common adverse event of the anti-CTLA-4 antibody in melanoma. Eur J Endocrinol. 2015;172(2):195–204.
   PubMed Web of Science ®Google Scholar
• Sarnaik AA, Yu B, Yu D, et al. Extended dose ipilimumab with a peptide vaccine: immune correlates associated with clinical benefit in patients with resected high-risk stage IIIc/IV melanoma. Clin Cancer Res off J Am Assoc Cancer Res. 2011;17(4):896–906.
   PubMed Web of Science ®Google Scholar
• Illouz F, Briet C, Cloix L, et al. Endocrine toxicity of immune checkpoint inhibitors: essential crosstalk between endocrinologists and oncologists. Cancer Med. 2017;6(8):1923–1929.
   PubMed Web of Science ®Google Scholar
• Dillard T, Yedinak CG, Alumkal J, et al. Anti-CTLA-4 antibody therapy associated autoimmune hypophysitis: serious immune related adverse events across a spectrum of cancer subtypes. Pituitary. 2010;13(1):29–38.
   PubMed Web of Science ®Google Scholar
• Barnard ZR, Walcott BP, Kahle KT, et al. Hyponatremia associated with Ipilimumab-induced hypophysitis. Med Oncol. 2012;29(1):374–377.
   PubMed Web of Science ®Google Scholar
• Gonzalez-Rodriguez E, Rodriguez-Abreu D. Immune checkpoint inhibitors: review and management of endocrine adverse events. Oncologist. 2016;21(7):804–816.
   PubMed Web of Science ®Google Scholar
• Maker AV, Yang JC, Sherry RM, et al. Intrapatient dose escalation of anti-CTLA-4 antibody in patients with metastatic melanoma. J Immunother. 2006;29(4):455–463.
   PubMed Web of Science ®Google Scholar
• Orlov S, Salari F, Kashat L, et al. Induction of painless thyroiditis in patients receiving programmed death 1 receptor immunotherapy for metastatic malignancies. J Clin Endocrinol Metab. 2015;100(5):1738–1741.
   PubMed Web of Science ®Google Scholar
• Cukier P, Santini FC, Scaranti M, et al. Endocrine side effects of cancer immunotherapy. Endocr Relat Cancer. 2017;24(12):T331–t47.
   PubMed Web of Science ®Google Scholar
• Barroso-Sousa R, Barry WT, Garrido-Castro AC, et al. Incidence of endocrine dysfunction following the use of different immune checkpoint inhibitor regimens: a systematic review and meta-analysis. JAMA Oncol. 2018;4(2):173–182.
   PubMed Web of Science ®Google Scholar
• Min L, Vaidya A, Becker C. Thyroid autoimmunity and ophthalmopathy related to melanoma biological therapy. Eur J Endocrinol. 2011;164(2):303–307.
   PubMed Web of Science ®Google Scholar
• Borodic G, Hinkle DM, Cia Y. Drug-induced graves disease from CTLA-4 receptor suppression. Ophthalmic Plast Reconstr Surg. 2011;27(4):e87–e8.
   PubMed Web of Science ®Google Scholar
• McMillen B, Dhillon MS, Yong-Yow S. A rare case of thyroid storm. BMJ Case Rep. 2016;2016. DOI:https://doi.org/10.1136/bcr-2016-214603.
   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
• Reck M, Rodriguez-Abreu D, Robinson AG, et al. Pembrolizumab versus chemotherapy for PD-L1-positive non-small-cell lung cancer. N Engl J Med. 2016;375(19):1823–1833.
   PubMed Web of Science ®Google Scholar
• O’Donnell HP, Plimack RE, Bellmunt J, et al. Pembrolizumab (Pembro; MK-3475) for advanced urothelial cancer: results of a phase IB study. Journal of Clinical Oncology. 2015;33(7_suppl):296-296. Abstract 296. DOI:https://doi.org/10.1200/jco.2015.33.7_suppl.296
   Google Scholar
• El-Khoueiry AB, Sangro B, Yau T, et al. Nivolumab in patients with advanced hepatocellular carcinoma (CheckMate 040): an open-label, non-comparative, phase 1/2 dose escalation and expansion trial. Lancet. 2017;389(10088):2492–2502.
   PubMed Web of Science ®Google Scholar
• Callahan MK, Yang A, Tandon S, et al. Evaluation of serum IL-17 levels during ipilimumab therapy: correlation with colitis. J Clin Oncol. 2011;29(15_suppl):2505.
   Web of Science ®Google Scholar
• Bacanovic S, Burger IA, Stolzmann P, et al. Ipilimumab-induced adrenalitis: a possible pitfall in 18F-FDG-PET/CT. Clin Nucl Med. 2015;40(11):e518–e9.
   PubMed Web of Science ®Google Scholar
• Trainer H, Hulse P, Higham CE, et al. Hyponatraemia secondary to nivolumab-induced primary adrenal failure. Endocrinol Diabetes Metab Case Rep. 2016;2016:1-4.
   Google Scholar
• Clotman K, Janssens K, Specenier P, et al. Programmed cell death-1 inhibitor-induced Type 1 diabetes mellitus. J Clin Endocrinol Metab. 2018;103(9):3144–3154.
   PubMed Web of Science ®Google Scholar
• Kapke J, Shaheen Z, Kilari D, et al. Immune checkpoint inhibitor-associated Type 1 diabetes mellitus: case series, review of the literature, and optimal management. Case Rep Oncol. 2017;10(3):897–909.
   PubMed Web of Science ®Google Scholar
• Win MA, Thein KZ, Qdaisat A, et al. Acute symptomatic hypocalcemia from immune checkpoint therapy-induced hypoparathyroidism. Am J Emerg Med. 2017;35(7):1039.e5-.e7.
   Web of Science ®Google Scholar