Immune checkpoint inhibitors-induced neuromuscular toxicity: From pathogenesis to treatment.


Journal

Journal of the peripheral nervous system : JPNS
ISSN: 1529-8027
Titre abrégé: J Peripher Nerv Syst
Pays: United States
ID NLM: 9704532

Informations de publication

Date de publication:
Oct 2019
Historique:
received: 03 06 2019
accepted: 15 07 2019
pubmed: 9 8 2019
medline: 23 4 2020
entrez: 9 8 2019
Statut: ppublish

Résumé

Immune checkpoint inhibitors (ICIs) are increasingly used and are becoming the standard of care in the treatment of various tumor types. Despite the favorable results in terms of oncological outcomes, these treatments have been associated with a variety of immune-related adverse events (irAEs). Neurological irAEs are rare but potentially severe. Neuromuscular disorders represent the most common neurological irAEs following anti-PD-1, anti-PD-L1, and anti-CTLA-4 treatment, and include myositis, myasthenia gravis, and demyelinating polyradiculoneuropathy. Instrumental findings may differ from typical neuromuscular disorders occurring outside ICIs treatment. Despite initial severity, neurological irAEs often respond to immune-modulating therapies. Prompt irAEs diagnosis, ICIs discontinuation, and early treatment with corticosteroids, together with patient education and a multi-disciplinary approach, are important for optimizing clinical outcomes. Intravenous immunoglobulin, plasma exchange, and other immune-modulating treatments should be considered in more severe cases. Consideration of re-challenging with the same immunotherapy drug may be given in some cases, based on clinical picture and initial severity of irAEs.

Identifiants

pubmed: 31393660
doi: 10.1111/jns.12339
doi:

Substances chimiques

Antibodies, Monoclonal, Humanized 0
Antineoplastic Agents, Immunological 0
Immunoglobulins, Intravenous 0
Immunologic Factors 0
PDCD1 protein, human 0
Programmed Cell Death 1 Receptor 0

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

S74-S85

Informations de copyright

© 2019 Peripheral Nerve Society.

Références

Kakimi K, Karasaki T, Matsushita H, Sugie T. Advances in personalized cancer immunotherapy. Breast Cancer. 2017;24(1):16-24.
Emens LA, Ascierto PA, Darcy PK, et al. Cancer immunotherapy: opportunities and challenges in the rapidly evolving clinical landscape. Eur J Cancer. 2017;81:116-129.
Hargadon KM, Johnson CE, Williams CJ. Immune checkpoint blockade therapy for cancer: an overview of FDA-approved immune checkpoint inhibitors. Int Immunopharmacol. 2018;62:29-39.
Markham A, Duggan S. Cemiplimab: first global approval. Drugs. 2018;78(17):1841-1846.
Wolchok JD, Kluger H, Callahan MK, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med. 2013;369(2):122-133.
Schmid P, Adams S, Rugo HS, et al. Atezolizumab and Nab-Paclitaxel in advanced triple-negative breast cancer. N Engl J Med. 2018;379(22):2108-2121.
Brahmer JR, Lacchetti C, Schneider BJ, et al.; National Comprehensive Cancer NetworkManagement of immune-related adverse events in patients treated with immune checkpoint inhibitor therapy: American Society of Clinical Oncology clinical practice guideline. J Clin Oncol. 2018;36(17):1714-1768.
Touat M, Talmasov D, Ricard D, Psimaras D. Neurological toxicities associated with immune-checkpoint inhibitors. Curr Opin Neurol. 2017;30(6):659-668.
Hellmann MD, Ciuleanu T-E, Pluzanski A, et al. Nivolumab plus ipilimumab in lung cancer with a high tumor mutational burden. N Engl J Med. 2018;378(22):2093-2104.
Kang Y-K, Boku N, Satoh T, et al. Nivolumab in patients with advanced gastric or gastro-oesophageal junction cancer refractory to, or intolerant of, at least two previous chemotherapy regimens (ONO-4538-12, ATTRACTION-2): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet. 2017;390(10111):2461-2471.
Weber J, Mandala M, Del Vecchio M, et al. Adjuvant nivolumab versus ipilimumab in resected stage III or IV melanoma. N Engl J Med. 2017;377(19):1824-1835.
Wolchok JD, Chiarion-Sileni V, Gonzalez R, et al. Overall survival with combined nivolumab and ipilimumab in advanced melanoma. N Engl J Med. 2017;377(14):1345-1356.
Ferris RL, Blumenschein G, Fayette J, et al. Nivolumab for recurrent squamous-cell carcinoma of the head and neck. N Engl J Med. 2016;375(19):1856-1867.
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.
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.
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.
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.
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.
Bellmunt J, de Wit R, Vaughn DJ, et al. Pembrolizumab as second-line therapy for advanced urothelial carcinoma. N Engl J Med. 2017;376(11):1015-1026.
Reck M, Rodríguez-Abreu D, Robinson AG, et al.; KEYNOTE-024 InvestigatorsPembrolizumab versus chemotherapy for PD-L1-positive non-small-cell lung cancer. N Engl J Med. 2016;375(19):1823-1833.
Rini BI, Plimack ER, Stus V, et al.; KEYNOTE-426 InvestigatorsPembrolizumab plus axitinib versus sunitinib for advanced renal-cell carcinoma. N Engl J Med. 2019;380(12):1116-1127.
Cohen EEW, Soulières D, Le Tourneau C, et al. Pembrolizumab versus methotrexate, docetaxel, or cetuximab for recurrent or metastatic head-and-neck squamous cell carcinoma (KEYNOTE-040): a randomised, open-label, phase 3 study. Lancet. 2019;393(10167):156-167.
Shitara K, Özgüroğlu M, Bang Y-J, et al. Pembrolizumab versus paclitaxel for previously treated, advanced gastric or gastro-oesophageal junction cancer (KEYNOTE-061): a randomised, open-label, controlled, phase 3 trial. Lancet. 2018;392(10142):123-133.
Gandhi L, Rodríguez-Abreu D, Gadgeel S, et al. Pembrolizumab plus chemotherapy in metastatic non-small-cell lung cancer. N Engl J Med. 2018;378(22):2078-2092.
Eggermont AMM, Blank CU, Mandala M, et al. Adjuvant pembrolizumab versus placebo in resected stage III melanoma. N Engl J Med. 2018;378(19):1789-1801.
Schachter J, Ribas A, Long GV, et al. Pembrolizumab versus ipilimumab for advanced melanoma: final overall survival results of a multicentre, randomised, open-label phase 3 study (KEYNOTE-006). Lancet. 2017;390(10105):1853-1862.
Larkin J, Chiarion-Sileni V, Gonzalez R, et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N Engl J Med. 2015;373(1):23-34.
Wang Y, Zhou S, Yang F, et al. Treatment-related adverse events of PD-1 and PD-L1 inhibitors in clinical trials: a systematic review and meta-analysis. JAMA Oncol. 2019;5(7):1008-1019. https://doi.org/10.1001/jamaoncol.2019.0393.
Ascierto PA, Del Vecchio M, Robert C, et al. Ipilimumab 10 mg/kg versus ipilimumab 3 mg/kg in patients with unresectable or metastatic melanoma: a randomised, double-blind, multicentre, phase 3 trial. Lancet Oncol. 2017;18(5):611-622.
Beer TM, Kwon ED, Drake CG, et al. Randomized, double-blind, phase III trial of ipilimumab versus placebo in asymptomatic or minimally symptomatic patients with metastatic chemotherapy-naive castration-resistant prostate cancer. J Clin Oncol. 2017;35(1):40-47.
Kwon ED, Drake CG, Scher HI, et al.; CA184-043 InvestigatorsIpilimumab 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.
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.
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.
Touat M, Maisonobe T, Knauss S, et al. Immune checkpoint inhibitor-related myositis and myocarditis in patients with cancer. Neurology. 2018;91(10):e985-e994.
Seki M, Uruha A, Ohnuki Y, et al. Inflammatory myopathy associated with PD-1 inhibitors. J Autoimmun. 2019;100:105-113.
Liewluck T, Kao JC, Mauermann ML. PD-1 inhibitor-associated myopathies: emerging immune-mediated myopathies. J Immunother. 2018;41(4):208-211.
Kadota H, Gono T, Shirai Y, Okazaki Y, Takeno M, Kuwana M. Immune checkpoint inhibitor-induced myositis: a case report and literature review. Curr Rheumatol Rep. 2019;21(4):10.
Psimaras D. Neuromuscular complications of immune checkpoint inhibitors. Presse Med. 2018;47(11-12):e253-e259.
Moreira A, Loquai C, Pföhler C, et al. Myositis and neuromuscular side-effects induced by immune checkpoint inhibitors. Eur J Cancer. 2019;106:12-23.
Shah M, Tayar JH, Abdel-Wahab N, Suarez-Almazor ME. Myositis as an adverse event of immune checkpoint blockade for cancer therapy. Semin Arthritis Rheum. 2019;48(4):736-740.
Pushkarevskaya A, Neuberger U, Dimitrakopoulou-Strauss A, Enk A, Hassel JC. Severe ocular myositis after ipilimumab treatment for melanoma: a report of 2 cases. J Immunother. 2017;40(7):282-285.
Luo W, Wang Z, Tian P, Li W. Safety and tolerability of PD-1/PD-L1 inhibitors in the treatment of non-small cell lung cancer: a meta-analysis of randomized controlled trials. J Cancer Res Clin Oncol. 2018;144(10):1851-1859.
Moslehi JJ, Salem J-E, Sosman JA, Lebrun-Vignes B, Johnson DB. Increased reporting of fatal immune checkpoint inhibitor-associated myocarditis. Lancet. 2018;391(10124):933.
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.
Hu J-R, Florido R, Lipson EJ, et al. Cardiovascular toxicities associated with immune checkpoint inhibitors. Cardiovasc Res. 2019;115(5):854-868.
Anquetil C, Salem J-E, Lebrun-Vignes B, et al. Immune checkpoint inhibitor-associated myositis: expanding the spectrum of cardiac complications of the immunotherapy revolution. Circulation. 2018;138(7):743-745.
Bilen MA, Subudhi SK, Gao J, Tannir NM, Tu S-M, Sharma P. Acute rhabdomyolysis with severe polymyositis following ipilimumab-nivolumab treatment in a cancer patient with elevated anti-striated muscle antibody. J Immunother Cancer. 2016;4(1):36.
Fellner A, Makranz C, Lotem M, et al. Neurologic complications of immune checkpoint inhibitors. J Neurooncol. 2018;137(3):601-609.
Sidhu P, Menzies AM, Long G, Carlino M, Lorens S, Kapoor R. Radiological manifestations of immune-related adverse effects observed in patients with melanoma undergoing immunotherapy. J Med Imaging Radiat Oncol. 2017;61(6):759-766.
Kao JC, Brickshawana A, Liewluck T. Neuromuscular complications of programmed cell death-1 (PD-1) inhibitors. Curr Neurol Neurosci Rep. 2018;18(10):63.
Thompson JA, Schneider BJ, Brahmer J, et al. Management of immunotherapy-related toxicities, version 1.2019, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw. 2019;17(3):255-289.
Suzuki S, Ishikawa N, Konoeda F, et al. Nivolumab-related myasthenia gravis with myositis and myocarditis in Japan. Neurology. 2017;89(11):1127-1134.
Gonzalez NL, Puwanant A, Lu A, Marks SM, Živković SA. Myasthenia triggered by immune checkpoint inhibitors: new case and literature review. Neuromuscul Disord. 2017;27(3):266-268.
Shirai T, Sano T, Kamijo F, et al. Acetylcholine receptor binding antibody-associated myasthenia gravis and rhabdomyolysis induced by nivolumab in a patient with melanoma. Jpn J Clin Oncol. 2016;46(1):86-88.
Nakatani Y, Tanaka N, Enami T, Minami S, Okazaki T, Komuta K. Lambert-Eaton Myasthenic syndrome caused by nivolumab in a patient with squamous cell lung cancer. Case Rep Neurol. 2018;10(3):346-352.
Chen J-H, Lee K-Y, Hu C-J, Chung C-C. Coexisting myasthenia gravis, myositis, and polyneuropathy induced by ipilimumab and nivolumab in a patient with non-small-cell lung cancer: a case report and literature review. Medicine (Baltimore). 2017;96(50):e9262.
Mitsune A, Yanagisawa S, Fukuhara T, et al. Relapsed myasthenia gravis after nivolumab treatment. Intern Med. 2018;57(13):1893-1897.
Mammen AL, Rajan A, Pak K, et al. Pre-existing antiacetylcholine receptor autoantibodies and B cell lymphopaenia are associated with the development of myositis in patients with thymoma treated with avelumab, an immune checkpoint inhibitor targeting programmed death-ligand 1. Ann Rheum Dis. 2019;78(1):150-152.
Saruwatari K, Sato R, Nakane S, et al. The risks and benefits of immune checkpoint blockade in anti-AChR antibody-seropositive non-small cell lung cancer patients. Cancer. 2019;11(2):140.
Nishijima TF, Shachar SS, Nyrop KA, Muss HB. Safety and tolerability of PD-1/PD-L1 inhibitors compared with chemotherapy in patients with advanced cancer: a meta-analysis. Oncologist. 2017;22(4):470-479.
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(6):709-718.
Xu M, Nie Y, Yang Y, Lu Y-T, Su Q. Risk of neurological toxicities following the use of different immune checkpoint inhibitor regimens in solid tumors: a systematic review and meta-analysis. Neurologist. 2019;24(3):75-83.
Man J, Ritchie G, Links M, Lord S, Lee CK. Treatment-related toxicities of immune checkpoint inhibitors in advanced cancers: a meta-analysis. Asia Pac J Clin Oncol. 2018;14(3):141-152.
Johansen A, Christensen SJ, Scheie D, Højgaard JLS, Kondziella D. Neuromuscular adverse events associated with anti-PD-1 monoclonal antibodies: systematic review. Neurology. 2019;92(14):663-674.
Tanaka R, Maruyama H, Tomidokoro Y, et al. Nivolumab-induced chronic inflammatory demyelinating polyradiculoneuropathy mimicking rapid-onset Guillain-Barré syndrome: a case report. Jpn J Clin Oncol. 2016;46(9):875-878.
Chen X, Haggiagi A, Tzatha E, DeAngelis LM, Santomasso B. Electrophysiological findings in immune checkpoint inhibitor-related peripheral neuropathy. Clin Neurophysiol. 2019;130(8):1440-1445.
Alhammad RM, Dronca RS, Kottschade LA, et al. Brachial plexus neuritis associated with anti-programmed cell death-1 antibodies: report of 2 cases. Mayo Clin Proc Innov Qual Outcomes. 2017;1(2):192-197.
Appelbaum J, Wells D, Hiatt JB, et al. Fatal enteric plexus neuropathy after one dose of ipilimumab plus nivolumab: a case report. J Immunother Cancer. 2018;6(1):82.
Daxini A, Cronin K, Sreih AG. Vasculitis associated with immune checkpoint inhibitors-a systematic review. Clin Rheumatol. 2018;37(9):2579-2584.
Yeh OL, Francis CE. Ipilimumab-associated bilateral optic neuropathy. J Neuroophthalmol. 2015;35(2):144-147.
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.
Teufel A, Zhan T, Härtel N, Bornschein J, Ebert MP, Schulte N. Management of immune related adverse events induced by immune checkpoint inhibition. Cancer Lett. 2019;456:80-87.
Yokosuka T, Takamatsu M, Kobayashi-Imanishi W, Hashimoto-Tane A, Azuma M, Saito T. Programmed cell death 1 forms negative costimulatory microclusters that directly inhibit T cell receptor signaling by recruiting phosphatase SHP2. J Exp Med. 2012;209(6):1201-1217.
Johnson DB, Balko JM. Biomarkers for immunotherapy toxicity: are cytokines the answer? Clin Cancer Res. 2019;25(5):1452-1454.
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.
Caturegli P, Di Dalmazi G, Lombardi M, et al. Hypophysitis secondary to cytotoxic T-lymphocyte-associated protein 4 blockade. Am J Pathol. 2016;186(12):3225-3235.
Spain L, Diem S, Larkin J. Management of toxicities of immune checkpoint inhibitors. Cancer Treat Rev. 2016;44:51-60.
Uemura M, Trinh VA, Haymaker C, et al. Selective inhibition of autoimmune exacerbation while preserving the anti-tumor clinical benefit using IL-6 blockade in a patient with advanced melanoma and Crohn's disease: a case report. J Hematol Oncol. 2016;9(1):81.
Dulos J, Carven GJ, van Boxtel SJ, et al. PD-1 blockade augments Th1 and Th17 and suppresses Th2 responses in peripheral blood from patients with prostate and advanced melanoma cancer. J Immunother. 2012;35(2):169-178.
Pai C-CS, Simons DM, Lu X, et al. Tumor-conditional anti-CTLA4 uncouples antitumor efficacy from immunotherapy-related toxicity. J Clin Invest. 2018;129(1):349-363.
Rowshanravan B, Halliday N, Sansom DM. CTLA-4: a moving target in immunotherapy. Blood. 2018;131(1):58-67.
Martins F, Sykiotis GP, Maillard M, et al. New therapeutic perspectives to manage refractory immune checkpoint-related toxicities. Lancet Oncol. 2019;20(1):e54-e64.
Läubli H, Balmelli C, Kaufmann L, et al. Influenza vaccination of cancer patients during PD-1 blockade induces serological protection but may raise the risk for immune-related adverse events. J Immunother Cancer. 2018;6:40.
Johnson DB, Balko JM, Compton ML, et al. Fulminant myocarditis with combination immune checkpoint blockade. N Engl J Med. 2016;375(18):1749-1755.
Subudhi SK, Aparicio A, Gao J, et al. Clonal expansion of CD8 T cells in the systemic circulation precedes development of ipilimumab-induced toxicities. Proc Natl Acad Sci. 2016;113(42):11919-11924.
Kumar B, Ballas Z. Adverse events associated with immune checkpoint blockade. N Engl J Med. 2018;378(12):1164.
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(2):377-385.
Heinzerling L, de Toni E, Schett G, Hundorfean G, Zimmer L. Checkpoint inhibitors. Dtsch Arztebl Int. 2019;116(8):119-126.
Gallay L, Bourgeois-Vionnet J, Joubert B, Streichenberger N, Hot A. Muscular disorder related to immune checkpoint inhibitors: forewarned is forearmed. Neuro Oncol. 2018;20(6):861-862.
Haanen JBAG, 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.
Society for Immunotherapy of Cancer Toxicity Management Working Group, Puzanov I, Diab A, et al. Managing toxicities associated with immune checkpoint inhibitors: consensus recommendations from the Society for Immunotherapy of Cancer (SITC) Toxicity Management Working Group. J Immunother Cancer. 2017;5(1):95.
Cuzzubbo S, Javeri F, Tissier M, et al. Neurological adverse events associated with immune checkpoint inhibitors: review of the literature. Eur J Cancer. 2017;73:1-8.
Graus F, Dalmau J. Paraneoplastic neurological syndromes in the era of immune-checkpoint inhibitors. Nat Rev Clin Oncol. 2019. https://doi.org/10.1038/s41571-019-0194-4.
Fishman JA, Hogan JI, Maus MV. Inflammatory and infectious syndromes associated with cancer immunotherapies. Clin Infect Dis. 2018. https://doi.org/10.1093/cid/ciy1025. (Epub ahead of print).
Dalakas MC. Neurological complications of immune checkpoint inhibitors: what happens when you ‘take the brakes off’ the immune system. Ther Adv Neurol Disord. 2018;11:1756286418799864.
Delyon J, Brunet-Possenti F, Leonard-Louis S, et al. Immune checkpoint inhibitor rechallenge in patients with immune-related myositis. Ann Rheum Dis. 2018. https://doi.org/10.1136/annrheumdis-2018-214336. (Epub ahead of print).
Pollack MH, Betof A, Dearden H, et al. Safety of resuming anti-PD-1 in patients with immune-related adverse events (irAEs) during combined anti-CTLA-4 and anti-PD1 in metastatic melanoma. Ann Oncol. 2018;29(1):250-255.
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.
Leonardi GC, Gainor JF, Altan M, et al. Safety of programmed death-1 pathway inhibitors among patients with non-small-cell lung cancer and preexisting autoimmune disorders. J Clin Oncol. 2018;36(19):1905-1912.
Makarious D, Horwood K, Coward JIG. Myasthenia gravis: an emerging toxicity of immune checkpoint inhibitors. Eur J Cancer. 2017;82:128-136.
Takamatsu K, Nakane S, Suzuki S, et al. Immune checkpoint inhibitors in the onset of myasthenia gravis with hyperCKemia. Ann Clin Transl Neurol. 2018;5(11):1421-1427.

Auteurs

Dimitri Psimaras (D)

AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière-Charles Foix, Service de Neurologie Mazarin, Paris, France.
Inserm U 1127, CNRS UMR 7225, Sorbonne Universités, UPMC Univ Paris 06 UMR S 1127, Institut du Cerveau et de la Moelle épinière, ICM, Paris, France.
OncoNeuroTox Group, Center for Patients with Neurological Complications of Oncologic Treatments, Hôpitaux Universitaires Pitié-Salpetrière-Charles Foix et Hôpital Percy, Paris, France.

Roser Velasco (R)

Unit of Neuro-Oncology, Hospital Universitari de Bellvitge-Institut Català D'Oncologia L'Hospitalet, IDIBELL, Barcelona, Spain.
Department of Cell Biology, Physiology and Immunology, Institute of Neurosciences, Universitat Autònoma de Barcelona, Barcelona, Spain.
Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Barcelona, Spain.

Cristina Birzu (C)

AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière-Charles Foix, Service de Neurologie Mazarin, Paris, France.
Inserm U 1127, CNRS UMR 7225, Sorbonne Universités, UPMC Univ Paris 06 UMR S 1127, Institut du Cerveau et de la Moelle épinière, ICM, Paris, France.
OncoNeuroTox Group, Center for Patients with Neurological Complications of Oncologic Treatments, Hôpitaux Universitaires Pitié-Salpetrière-Charles Foix et Hôpital Percy, Paris, France.

Stefano Tamburin (S)

Department of Neurosciences, Biomedicine and Movement Sciences, University of Verona, Verona, Italy.

Maryam Lustberg (M)

Division of Medical Oncology, Department of Internal Medicine, The Ohio State University Comprehensive Cancer, Columbus, Ohio.

Jordi Bruna (J)

Unit of Neuro-Oncology, Hospital Universitari de Bellvitge-Institut Català D'Oncologia L'Hospitalet, IDIBELL, Barcelona, Spain.
Department of Cell Biology, Physiology and Immunology, Institute of Neurosciences, Universitat Autònoma de Barcelona, Barcelona, Spain.
Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Barcelona, Spain.

Andreas A Argyriou (AA)

Department of Neurology, "Saint Andrew's" State General Hospital of Patras, Patras, Greece.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH