Neurological toxicities associated with immune-checkpoint inhibitors

Current Opinion in Neurology

Volumn 30, Issue 6, 2017, Pages 659-668

  Touat, Mehdi ^a,b,c,d   Talmasov, Daniel ^e   Ricard, Damien ^c,f   Psimaras, Dimitri ^a,b,c  

^a SORBONNE UNIVERSITÉ   (France)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^c PERCY MILITARY HOSPITAL   (France)

^d Dana Farber Brigham and Women's Cancer Center   (France)

^e HARVARD MEDICAL SCHOOL   (United States)

^f CNRS   (France)

Author keywords

atezolizumab; avelumab; cytotoxic T lymphocyte associated antigen 4; durvalumab; ipilumumab; nivolumab; pembrolizumab; programmed death 1 receptor; programmed death ligand 1

Indexed keywords

ANTINEOPLASTIC AGENT; CORTICOSTEROID; IMMUNE CHECKPOINT INHIBITOR; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG; IMMUNOLOGIC FACTOR;

CENTRAL NERVOUS SYSTEM; DEMYELINATING DISEASE; ENCEPHALITIS; HUMAN; MENINGITIS; MORBIDITY; MYASTHENIA GRAVIS; MYOSITIS; NEUROLOGIC DISEASE; PERIPHERAL NERVOUS SYSTEM; PERIPHERAL NEUROPATHY; POLYRADICULONEUROPATHY; REVIEW; ADVERSE DRUG REACTION; IMMUNOLOGY; IMMUNOTHERAPY; NEOPLASM; TOXICITY AND INTOXICATION;

DRUG-RELATED SIDE EFFECTS AND ADVERSE REACTIONS; HUMANS; IMMUNOLOGIC FACTORS; IMMUNOTHERAPY; NEOPLASMS; NEUROTOXICITY SYNDROMES;

EID: 85033798830     PISSN: 13507540     EISSN: 14736551     Source Type: Journal    
DOI: 10.1097/WCO.0000000000000503     Document Type: Review

References (72)

1. Leach DR, Krummel MF, Allison JP. Enhancement of antitumor immunity by CTLA-4 blockade. Science 1996; 271:1734-1736.
2. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012; 12:252-264.
3. Chen L, Han X. Anti-PD-1/PD-L1 therapy of human cancer: past, present, and future. J Clin Invest 2015; 125:3384-3391.
4. Waterhouse P, Penninger JM, Timms E, et al. Lymphoproliferative disorders with early lethality in mice deficient in Ctla-4. Science 1995; 270:985-988.
5. 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:iv119-iv142.
6. Michot JM, Bigenwald C, Champiat S, et al. Immune-related adverse events with immune checkpoint blockade: a comprehensive review. Eur J Cancer 2016; 54:139-148.
7. Boutros C, Tarhini A, Routier E, et al. Safety profiles of anti-CTLA-4 and anti-PD-1 antibodies alone and in combination. Nat Rev Clin Oncol 2016; 13:473-486.
8. Champiat S, Lambotte O, Barreau E, et al. Management of immune checkpoint blockade dysimmune toxicities: a collaborative position paper. Ann Oncol 2016; 27:559-574.
9. Khoja L, Day D, Wei-Wu Chen T, et al. Tumour-and class-specific patterns of immune-related adverse events of immune checkpoint inhibitors: a systematic review. Ann Oncol 2017.
10. Robert C, Schachter J, Long GV, et al. Pembrolizumab versus ipilimumab in advanced melanoma. N Engl J Med 2015; 372:2521-2532.
11. 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.
12. 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.
13. Eggermont AM, Chiarion-Sileni V, Grob JJ, et al. Prolonged survival in stage III melanoma with ipilimumab adjuvant therapy. N Engl J Med 2016; 375:1845-1855.
14. Larkin J, Chiarion-Sileni V, Gonzalez R, et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N Engl J Med 2015; 373:23-34.
15. 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; 28:368-376.
16. Spain L, Walls G, Julve M, et al. Neurotoxicity from immune-checkpoint inhibition in the treatment of melanoma: a single centre experience and review of the literature. Ann Oncol 2017; 28:377-385.
17. Larkin J, Chmielowski B, Lao CD, et al. Neurologic serious adverse events associated with nivolumab plus ipilimumab or nivolumab alone in advanced melanoma, including a case series of encephalitis. Oncologist 2017; 22:709-718.
18. Cuzzubbo S, Javeri F, Tissier M, et al. Neurological adverse events associated with immune checkpoint inhibitors: review of the literature. Eur JCancer 2017; 73:1-8.
19. Voskens CJ, Goldinger SM, Loquai C, et al. The price of tumor control: an analysis of rare side effects of anti-CTLA-4 therapy in metastatic melanoma from the ipilimumab network. PLoS One 2013; 8:e53745.
20. 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.
21. Liao B, Shroff S, Kamiya-Matsuoka C, Tummala S. Atypical neurological complications of ipilimumab therapy in patients with metastatic melanoma. Neuro Oncol 2014; 16:589-593.
22. Conry RM, Sullivan JC, Nabors LB. Ipilimumab-induced encephalopathy with a reversible splenial lesion. Cancer Immunol Res 2015; 3:598-601.
23. LaPorte J, Solh M, Ouanounou S. Posterior reversible encephalopathy syndrome following pembrolizumab therapy for relapsed Hodgkin's lymphoma. J Oncol Pharm Pract 2017; 23:71-74.
24. Gettings EJ, Hackett CT, Scott TF. Severe relapse in a multiple sclerosis patient associated with ipilimumab treatment of melanoma. Mult Scler 2015; 21:670.
25. Gerdes LA, Held K, Beltrán E, et al. CTLA4 as immunological checkpoint in the development of multiple sclerosis. Ann Neurol 2016; 80:294-300.
26. Maurice C, Schneider R, Kiehl TR, et al. Subacute CNS demyelination after treatment with nivolumab for melanoma. Cancer Immunol Res 2015; 3:1299-1302.
27. Mandel JJ, Olar A, Aldape KD, Tremont-Lukats IW. Lambrolizumab induced central nervous system (CNS) toxicity. J Neurol Sci 2014; 344:229-231.
28. Salam S, Lavin T, Turan A. Limbic encephalitis following immunotherapy against metastatic malignant melanoma. BMJ Case Rep 2016.
29. Schneider S, Potthast S, Komminoth P, et al. PD-1 checkpoint inhibitor associated autoimmune encephalitis. Case Rep Oncol 2017; 10:473-478.
30. Stein MK, Summers BB, Wong CA, et al. Meningoencephalitis following ipilimumab administration in metastatic melanoma. Am J Med Sci 2015; 350:512-513.
31. Williams TJ, Benavides DR, Patrice KA, et al. Association of autoimmune encephalitis with combined immune checkpoint inhibitor treatment for metastatic cancer. JAMA Neurol 2016; 73:928-933.
32. Brown MP, Hissaria P, Hsieh AH, et al. Autoimmune limbic encephalitis with anticontactin-associated protein-like 2 antibody secondary to pembrolizumab therapy. J Neuroimmunol 2017; 305:16-18.
33. Yang JC, Hughes M, Kammula U, et al. Ipilimumab (anti-CTLA4 antibody) causes regression of metastatic renal cell cancer associated with enteritis and hypophysitis. J Immunother 2007; 30:825-830.
34. Bot I, Blank CU, Boogerd W, Brandsma D. Neurological immune-related adverse events of ipilimumab. Pract Neurol 2013; 13:278-280.
35. Oishi K, Nakao M, Maeda S, et al. A case of aseptic meningitis without neck rigidity occurring in a metastatic melanoma patient treated with ipilimumab. Eur J Dermatol 2017; 27:193-194.
36. Suzuki S, Ishikawa N, Konoeda F, et al. Nivolumab-related myasthenia gravis with myositis and myocarditis in Japan. Neurology 2017. [Epub ahead of print]
37. Johnson DB, Saranga-Perry V, Lavin PJ, et al. Myasthenia gravis induced by ipilimumab in patients with metastatic melanoma. J Clin Oncol 2015; 33:e122-e124.
38. Loochtan AI, Nickolich MS, Hobson-Webb LD. Myasthenia gravis associated with ipilimumab and nivolumab in the treatment of small cell lung cancer. Muscle Nerve 2015; 52:307-308.
39. March KL, Samarin MJ, Sodhi A, Owens RE. Pembrolizumab-induced myasthenia gravis: a fatal case report. J Oncol Pharm Pract 2017. [Epub ahead of print]
40. Shirai T, Sano T, Kamijo F, et al. Acetylcholine receptor binding antibodyassociated myasthenia gravis and rhabdomyolysis induced by nivolumab in a patient with melanoma. Jpn J Clin Oncol 2016; 46:86-88.
41. Kimura T, Fukushima S, Miyashita A, et al. Myasthenic crisis and polymyositis induced by one dose of nivolumab. Cancer Sci 2016; 107:1055-1058.
42. Alnahhas I, Wong J. A case of new-onset antibody-positive myasthenia gravis in a patient treated with pembrolizumab for melanoma. Muscle Nerve 2017; 55:E25-E26.
43. Chang E, Sabichi AL, Sada YH. Myasthenia gravis after nivolumab therapy for squamous cell carcinoma of the bladder. J Immunother 2017; 40:114-116.
44. Lau KH, Kumar A, Yang IH, Nowak RJ. Exacerbation of myasthenia gravis in a patient with melanoma treated with pembrolizumab. Muscle Nerve 2016; 54:157-161.
45. Zhu J, Li Y. Myasthenia gravis exacerbation associated with pembrolizumab. Muscle Nerve 2016; 54:506-507.
46. Phadke SD, Ghabour R, Swick BL, et al. Pembrolizumab therapy triggering an exacerbation of preexisting autoimmune disease: a report of 2 patient cases. J Investig Med High Impact Case Rep 2016; 4:2324709616674316.
47. Maeda O, Yokota K, Atsuta N, et al. Nivolumab for the treatment of malignant melanoma in a patient with preexisting myasthenia gravis. Nagoya J Med Sci 2016; 78:119-122.
48. Makarious D, Horwood K, Coward JIG. Myasthenia gravis: an emerging toxicity of immune checkpoint inhibitors. Eur J Cancer 2017; 82:128-136.
49. Lecouflet M, Verschoore M, Giard C, et al. Orbital myositis associated with ipilimumab. Ann Dermatol Venereol 2013; 140:448-451.
50. Vallet H,Gaillet A, Weiss N, et al. Pembrolizumab-induced necrotic myositis in a patient with metastatic melanoma. Ann Oncol 2016; 27:1352-1353.
51. Bilen MA, Subudhi SK, Gao J, et al. Acute rhabdomyolysis with severe polymyositis following ipilimumab-nivolumab treatment in a cancer patient with elevated antistriated muscle antibody. J Immunother Cancer 2016; 4:36.
52. Pushkarevskaya A, Neuberger U, Dimitrakopoulou-Strauss A, et al. Severe ocular myositis after ipilimumab treatment for melanoma: a report of 2 cases. J Immunother 2017; 40:282-285.
53. Fox E, Dabrow M, Ochsner G. A Case of nivolumab-induced myositis. Oncologist 2016; 21:e3.
54. Haddox CL, Shenoy N, Shah KK, et al. Pembrolizumab induced bulbar myopathy and respiratory failure with necrotizing myositis of the diaphragm. Ann Oncol 2017; 28:673-675.
55. Hottinger AF. Neurologic complications of immune checkpoint inhibitors. Curr Opin Neurol 2016; 29:806-812.
56. Yeh OL, Francis CE. Ipilimumab-associated bilateral optic neuropathy. J Neuroophthalmol 2015; 35:144-147.
57. Altman AL, Golub JS, Pensak ML, Samy RN. Bilateral facial palsy following ipilimumab infusion for melanoma. Otolaryngol Head Neck Surg 2015; 153:894-895.
58. Boisseau W, Touat M, Berzero G, et al. Safety of treatment with nivolumab after ipilimumab-related meningoradiculitis and bilateral optic neuropathy. Eur J Cancer 2017; 83:28-31.
59. Bompaire F, Mateus C, Taillia H, et al. Severe meningo-radiculo-neuritis associated with ipilimumab. Invest New Drugs 2012; 30:2407-2410.
60. Manousakis G, Koch J, Sommerville RB, et al. Multifocal radiculoneuropathy during ipilimumab treatment of melanoma. Muscle Nerve 2013; 48:440-444.
61. de Maleissye MF, Nicolas G, Saiag P. Pembrolizumab-induced demyelinating polyradiculoneuropathy. N Engl J Med 2016; 375:296-297.
62. Wilgenhof S, Neyns B. Anti-CTLA-4 antibody-induced Guillain-Barrésyndrome in a melanoma patient. Ann Oncol 2011; 22:991-993.
63. Gaudy-Marqueste C, Monestier S, Franques J, et al. A severe case of ipilimumab-induced Guillain-Barrésyndrome revealed by an occlusive enteric neuropathy: a differential diagnosis for ipilimumab-induced colitis. J Immunother 2013; 36:77-78.
64. Gu Y, Menzies AM, Long GV, et al. Immune mediated neuropathy following checkpoint immunotherapy. J Clin Neurosci 2017. [Epub ahead of print]
65. Tanaka R, Maruyama H, Tomidokoro Y, et al. Nivolumab-induced chronic inflammatorydemyelinatingpolyradiculoneuropathymimicking rapid-onset Guillain-Barrésyndrome: a case report. Jpn J Clin Oncol 2016; 46:875-878.
66. Sepúlveda M, Martinez-Hernandez E, Gaba L, et al. Motor polyradiculopathy during pembrolizumab treatment of metastatic melanoma. Muscle Nerve 2017. [Epub ahead of print]
67. Gutzmer R, Koop A, Meier F, et al. Programmed cell death protein-1 (PD-1) inhibitor therapy in patients with advanced melanoma and preexisting autoimmunity or ipilimumab-triggered autoimmunity. Eur J Cancer 2017; 75:24-32.
68. 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.
69. Tchapyjnikov D, Borst AJ. Immune-related neurological symptoms in an adolescent patient receiving the checkpoint inhibitor nivolumab. J Immunother 2017; 40:286-288.
70. Esfahani K, Miller WH. Reversal of autoimmune toxicity and loss of tumor response by interleukin-17 blockade. N Engl J Med 2017; 376:1989-1991.
71. Maul LV, Weichenthal M, Kähler KC, Hauschild A. Successful anti-PD-1 antibody treatment in a metastatic melanoma patient with known severe autoimmune disease. J Immunother 2016; 39:188-190.
72. Johnson DB, Sullivan RJ, Ott PA, et al. Ipilimumab therapy in patients with advanced melanoma and preexisting autoimmune disorders. JAMA Oncol 2016; 2:234-240.