REVIEW
Therapeutic plasma exchange in the management of immune checkpoint inhibitor-associated immune-related adverse effects: A review
Oluwatoyosi A. Onwuemene,
Chizoba I. Nnoruka,
Christopher J. Patriquin,
Laura S. Connelly-Smith,
Corresponding Author
Oluwatoyosi A. Onwuemene
Division of Hematology, Department of Medicine, Duke University Medical Center, Durham, North Carolina, USA
Correspondence
Oluwatoyosi A. Onwuemene, 40 Duke Medicine Circle, DUMC Box 3422, Durham, NC 27710, USA.
Email: [email protected]
Search for more papers by this authorChizoba I. Nnoruka
Division of Hematology/Oncology, Sibley Memorial Hospital, Sibley Memorial Hospital John Hopkins University, Washington, DC, USA
Search for more papers by this authorChristopher J. Patriquin
Department of Medicine, Division of Medical Oncology & Hematology, University Health Network, University of Toronto, Toronto, ON, Canada
Search for more papers by this authorLaura S. Connelly-Smith
Department of Medicine, University of Washington and Fred Hutchinson Cancer Center, Seattle, Washington, USA
Search for more papers by this authorOluwatoyosi A. Onwuemene,
Chizoba I. Nnoruka,
Christopher J. Patriquin,
Laura S. Connelly-Smith,
Corresponding Author
Oluwatoyosi A. Onwuemene
Division of Hematology, Department of Medicine, Duke University Medical Center, Durham, North Carolina, USA
Correspondence
Oluwatoyosi A. Onwuemene, 40 Duke Medicine Circle, DUMC Box 3422, Durham, NC 27710, USA.
Email: [email protected]
Search for more papers by this authorChizoba I. Nnoruka
Division of Hematology/Oncology, Sibley Memorial Hospital, Sibley Memorial Hospital John Hopkins University, Washington, DC, USA
Search for more papers by this authorChristopher J. Patriquin
Department of Medicine, Division of Medical Oncology & Hematology, University Health Network, University of Toronto, Toronto, ON, Canada
Search for more papers by this authorLaura S. Connelly-Smith
Department of Medicine, University of Washington and Fred Hutchinson Cancer Center, Seattle, Washington, USA
Search for more papers by this authorFunding information: American Society of Hematology
CONFLICT OF INTEREST
The authors have disclosed no conflicts of interest.
REFERENCES
- 1Robert C. A decade of immune-checkpoint inhibitors in cancer therapy. Nat Commun. 2020; 11(1): 3801. https://doi.org/10.1038/s41467-020-17670-y
- 2Conroy M, Naidoo J. Immune-related adverse events and the balancing act of immunotherapy. Nat Commun. 2022; 13(1): 392. https://doi.org/10.1038/s41467-022-27960-2
- 3Schneider BJ, Naidoo J, Santomasso BD, Atkins MB, Brassil KJ, Caterino JM, et al. Management of immune-related adverse events in patients treated with immune checkpoint inhibitor therapy: ASCO guideline update. JCO. 2021; 39(36): 4073–126. https://doi.org/10.1200/JCO.21.01440
- 4Kisielow M, Kisielow J, Capoferri-Sollami G, Karjalainen K. Expression of lymphocyte activation gene 3 (LAG-3) on B cells is induced by T cells. Eur J Immunol. 2005; 35(7): 2081–8. https://doi.org/10.1002/eji.200526090
- 5Walker LSK, Sansom DM. The emerging role of CTLA4 as a cell-extrinsic regulator of T cell responses. Nat Rev Immunol. 2011; 11(12): 852–63. https://doi.org/10.1038/nri3108
- 6Amarnath S, Mangus CW, Wang JCM, Wei F, He A, Kapoor V, et al. The PDL1-PD1 axis converts human TH1 cells into regulatory T cells. Sci Transl Med. 2011; 3(111): 111ra120. https://doi.org/10.1126/scitranslmed.3003130
- 7Boukouris AE, Theochari M, Stefanou D, Papalambros A, Felekouras E, Gogas H, et al. Latest evidence on immune checkpoint inhibitors in metastatic colorectal cancer: a 2022 update. Critic Rev Oncol Hematol. 2022; 173:103663. https://doi.org/10.1016/j.critrevonc.2022.103663
- 8Paik J. Nivolumab plus relatlimab: first approval. Drugs. 2022; 82(8): 925–31. https://doi.org/10.1007/s40265-022-01723-1
- 9Heery CR, O'Sullivan-Coyne G, Madan RA, Cordes L, Rajan A, Rauckhorst M, et al. Avelumab for metastatic or locally advanced previously treated solid tumours (JAVELIN solid tumor): a phase 1a, multicohort, dose-escalation trial. Lancet Oncol. 2017; 18(5): 587–98. https://doi.org/10.1016/S1470-2045(17)30239-5
- 10Centanni M, Moes DJAR, Trocóniz IF, Ciccolini J, van Hasselt JGC. Clinical pharmacokinetics and pharmacodynamics of immune checkpoint inhibitors. Clin Pharmacokinet. 2019; 58(7): 835–57. https://doi.org/10.1007/s40262-019-00748-2
- 11 YERVOY® (ipilimumab) injection, for intravenous use. Accessed 31 Aug 2022. https://www.accessdata.fda.gov/drugsatfda_docs/label/2015/125377s073lbl.pdf.
- 12Feng Y, Masson E, Dai D, Parker SM, Berman D, Roy A. Model-based clinical pharmacology profiling of ipilimumab in patients with advanced melanoma. Br J Clin Pharmacol. 2014; 78(1): 106–17. https://doi.org/10.1111/bcp.12323
- 13 LIBTAYO® (cemiplimab-rwlc) injection, for intravenous use. Accessed 31 Aug 2022. https://www.accessdata.fda.gov/drugsatfda_docs/label/2021/761097s007lbl.pdf.
- 14Yang F, Paccaly AJ, Rippley RK, Davis JD, DiCioccio AT. Population pharmacokinetic characteristics of cemiplimab in patients with advanced malignancies. J Pharmacokinet Pharmacodyn. 2021; 48(4): 479–94. https://doi.org/10.1007/s10928-021-09739-y
- 15 JEMPERLI (dostarlimab-gxly) injection, for intravenous use. Accessed 31 Aug 2022. https://www.accessdata.fda.gov/drugsatfda_docs/label/2021/761174s000lbl.pdf.
- 16Costa B, Vale N. Dostarlimab: a review. Biomolecules. 2022; 12(8):1031. https://doi.org/10.3390/biom12081031
- 17 OPDIVO (nivolumab) injection, for intravenous use. Accessed 31 Aug 2022. https://www.accessdata.fda.gov/drugsatfda_docs/label/2022/125554s112lbl.pdf.
- 18 KEYTRUDA® (pembrolizumab) injection, for intravenous use. Accessed 31 Aug 2022. https://www.accessdata.fda.gov/drugsatfda_docs/label/2022/125514s110lbl.pdf.
- 19 TECENTRIQ® (atezolizumab) injection, for intravenous use. Accessed 31 Aug 2022. https://www.accessdata.fda.gov/drugsatfda_docs/label/2018/761034s010lbl.pdf.
- 20 BAVENCIO® (avelumab) injection, for intravenous use. Accessed 31 Aug 2022. https://www.accessdata.fda.gov/drugsatfda_docs/label/2019/761049s006lbl.pdf.
- 21 IMFINZI® (durvalumab) injection, for intravenous use. Accessed 31 Aug 2022. https://www.accessdata.fda.gov/drugsatfda_docs/label/2020/761069s018lbl.pdf.
- 22Chocarro L, Bocanegra A, Blanco E, Fernández-Rubio L, Arasanz H, Echaide M, et al. Cutting-edge: preclinical and clinical development of the first approved lag-3 inhibitor. Cells. 2022; 11(15):2351. https://doi.org/10.3390/cells11152351
- 23 OPDUALAG™ (nivolumab and relatlimab-rmbw) injection, for intravenous use. Accessed 31 Aug 2022. https://www.accessdata.fda.gov/drugsatfda_docs/label/2022/761234s000lbl.pdf.
- 24Stroh M, Winter H, Marchand M, Claret L, Eppler S, Ruppel J, et al. Clinical pharmacokinetics and pharmacodynamics of atezolizumab in metastatic urothelial carcinoma. Clin Pharmacol Ther. 2017; 102(2): 305–12. https://doi.org/10.1002/cpt.587
- 25Okiyama N, Tanaka R. Immune-related adverse events in various organs caused by immune checkpoint inhibitors. Allergol Inter. 2022; 71(2): 169–78. https://doi.org/10.1016/j.alit.2022.01.001
- 26El Osta B, Hu F, Sadek R, Chintalapally R, Tang SC. Not all immune-checkpoint inhibitors are created equal: meta-analysis and systematic review of immune-related adverse events in cancer trials. Critic Rev Oncol Hematol. 2017; 119: 1–12. https://doi.org/10.1016/j.critrevonc.2017.09.002
- 27Hayata M, Shimanuki M, Ko T, Date R, Hamaguchi A, Tominaga A, et al. Pembrolizumab-associated thrombotic microangiopathy in a patient with urothelial cancer: a case report and literature review. Renal Replacement Therapy. 2020; 6(1): 29. https://doi.org/10.1186/s41100-020-00278-9
10.1186/s41100-020-00278-9 Google Scholar
- 28Badra S, Ruchi R, Zeng X, Gordan L, Shah CV. Immune checkpoint inhibitor associated renally limited thrombotic microangiopathy – a clinical dilemma. Eur J Cancer. 2022; 169: 126–30. https://doi.org/10.1016/j.ejca.2022.03.031
- 29Muniz TP, Patriquin CJ, Saibil SD. Presumed complement-mediated, checkpoint inhibitor-induced, thrombotic microangiopathy in a patient with metastatic melanoma. BMJ Case Rep CP. 2021; 14(7):e242075. https://doi.org/10.1136/bcr-2021-242075
- 30Brahmer JR, Lacchetti C, Schneider BJ, Atkins MB, Brassil KJ, Caterino JM, et al. Management of immune-related adverse events in patients treated with immune checkpoint inhibitor therapy: American Society of Clinical Oncology clinical practice guideline. JCO. 2018; 36(17): 1714–68. https://doi.org/10.1200/JCO.2017.77.6385
- 31 Common Terminology Criteria for Adverse Events (CTCAE). Protocol Development CTEP. Accessed 24 Jun 2022. https://ctep.cancer.gov/protocoldevelopment/electronic_applications/ctc.htm#ctc_60.
- 32Amerikanou R, Neill L, Shafat M, Roddy H, Hyare H, Hughes S, et al. Multi-organ graft-versus-host disease after nivolumab for relapsed Hodgkin lymphoma: the role of plasma exchange. Lancet Haematol. 2021; 8(11):e862. https://doi.org/10.1016/S2352-3026(21)00202-7
- 33Orme JJ, Enninga E, Lucien-Matteoni F, Dale H, Burgstaler E, Harrington SM, et al. Therapeutic plasma exchange clears circulating soluble PD-L1 and PD-L1-positive extracellular vesicles. J Immunother Cancer. 2020; 8(2):e001113. https://doi.org/10.1136/jitc-2020-001113
- 34Kimura T, Fukushima S, Miyashita A, Aoi J, Jinnin M, Kosaka T, et al. Myasthenic crisis and polymyositis induced by one dose of nivolumab. Cancer Sci. 2016; 107(7): 1055–8. https://doi.org/10.1111/cas.12961
- 35Youssef A, Kasso N, Torloni AS, Stanek M, Dragovich T, Gimbel M, et al. Thrombotic thrombocytopenic purpura due to checkpoint inhibitors. Case Rep Hematol. 2018; 2018:2464619. https://doi.org/10.1155/2018/2464619
- 36Takahashi N, Tsuji K, Tamiya H, Shinohara T, Kuroda N, Takeuchi E. Goodpasture's disease in a patient with advanced lung cancer treated with nivolumab: an autopsy case report. Lung Cancer. 2018; 122: 22–4. https://doi.org/10.1016/j.lungcan.2018.05.015
- 37Padmanabhan A, Connelly-Smith L, Aqui N, Balogun RA, Klingel R, Meyer E, et al. Guidelines on the use of therapeutic apheresis in clinical practice – evidence-based approach from the writing Committee of the American Society for apheresis: the eighth special issue. J Clin Apher. 2019; 34(3): 171–354. https://doi.org/10.1002/jca.21705
- 38Dang T, Macwan S, Dasanu CA. Late-onset double-seronegative myasthenia gravis syndrome and myasthenic crisis due to nivolumab use for Hodgkin's lymphoma. J Oncol Pharm Pract. 2021; 27(6): 1534–8. https://doi.org/10.1177/1078155220976797
- 39Dhenin A, Samartzi V, Lejeune S, Seront E. Cascade of immunologic adverse events related to pembrolizumab treatment. BMJ Case Rep. 2019; 12(6). https://doi.org/10.1136/bcr-2018-229149
- 40Fukazawa R, Takezawa H, Tsuji Y, Noto Y, Banba M, Fujii A. A case of myasthenia gravis developed during pembrolizumab administration, suggesting an excitation-contraction connection disorder. Rinsho Shinkeigaku. 2020; 60(1): 37–40. https://doi.org/10.5692/clinicalneurol.cn-001323
- 41Hasegawa Y, Kawai S, Ota T, Tsukuda H, Fukuoka M. Myasthenia gravis induced by nivolumab in patients with non-small-cell lung cancer: a case report and literature review. Immunotherapy. 2017; 9(9): 701–7. https://doi.org/10.2217/imt-2017-0043
- 42Johnson DB, Saranga-Perry V, Lavin PJ, Burnette WB, Clark SW, Uskavitch DR, et al. Myasthenia gravis induced by Ipilimumab in patients with metastatic melanoma. J Clin Oncol. 2015; 33(33): e122–4. https://doi.org/10.1200/JCO.2013.51.1683
- 43March KL, Samarin MJ, Sodhi A, Owens RE. Pembrolizumab-induced myasthenia gravis: a fatal case report. J Oncol Pharm Pract. 2018; 24(2): 146–9. https://doi.org/10.1177/1078155216687389
- 44Noda T, Kageyama H, Miura M, Tamura T, Ito H. A case of myasthenia gravis and myositis induced by pembrolizumab. Rinsho Shinkeigaku. 2019; 59(8): 502–8. https://doi.org/10.5692/clinicalneurol.cn-001251
- 45Safa H, Johnson DH, Trinh VA, Rodgers TE, Lin H, Suarez-Almazor ME, et al. Immune checkpoint inhibitor related myasthenia gravis: single center experience and systematic review of the literature. J Immunother Cancer. 2019; 7(1): 319. https://doi.org/10.1186/s40425-019-0774-y
- 46Tahir N, Mahboob A, Piao X, Ying G, Shrestha J, Sherchan R, et al. Nivolumab, a double-edged sword: a case report of nivolumab-induced myasthenia gravis. J Med Cases. 2021; 12(10): 424–8. https://doi.org/10.14740/jmc3783
- 47Ziobro AS, LaPlante RL, DeMari SR, Clark LM, Kingsley DJ, Smith AJ. Myasthenia gravis associated with programmed death-1 (PD-1) receptor inhibitor pembrolizumab: a 40-day case report. J Pharm Pract. 2021; 34(1): 166–70. https://doi.org/10.1177/0897190020970750
- 48Aldrich J, Pundole X, Tummala S, Palaskas N, Andersen CR, Shoukier M, et al. Inflammatory myositis in cancer patients receiving immune checkpoint inhibitors. Arthritis Rheumatol. 2021; 73(5): 866–74. https://doi.org/10.1002/art.41604
- 49Diamanti L, Picca A, Bini P, Gastaldi M, Alfonsi E, Pichiecchio A, et al. Characterization and management of neurological adverse events during immune-checkpoint inhibitors treatment: an Italian multicentric experience. Neurol Sci. 2022; 43(3): 2031–41. https://doi.org/10.1007/s10072-021-05561-z
- 50Esfahani K, Buhlaiga N, Thébault P, Lapointe R, Johnson NA, Miller WH. Alemtuzumab for immune-related myocarditis due to PD-1 therapy. New Engl J Med. 2019; 380(24): 2375–6. https://doi.org/10.1056/NEJMc1903064
- 51Jeyakumar N, Etchegaray M, Henry J, Lelenwa L, Zhao B, Segura A, et al. The terrible triad of checkpoint inhibition: a case report of myasthenia gravis, myocarditis, and myositis induced by Cemiplimab in a patient with metastatic cutaneous squamous cell carcinoma. Case Reports Immunol. 2020; 2020: 5126717. https://doi.org/10.1155/2020/5126717
- 52Kang KH, Grubb W, Sawlani K, Gibson MK, Hoimes CJ, Rogers LR, et al. Immune checkpoint-mediated myositis and myasthenia gravis: a case report and review of evaluation and management. Am J Otolaryngol. 2018; 39(5): 642–5. https://doi.org/10.1016/j.amjoto.2018.06.003
- 53Komatsu M, Hirai M, Kobayashi K, Hashidate H, Fukumoto J, Sato A, et al. A rare case of nivolumab-related myasthenia gravis and myocarditis in a patient with metastatic gastric cancer. BMC Gastroenterol. 2021; 21(1): 333. https://doi.org/10.1186/s12876-021-01904-4
- 54Konoeda F, Suzuki S, Nishimoto Y, Hoshino H, Takagi M. A case of myasthenia gravis and myositis induced by nivolumab. Rinsho Shinkeigaku. 2017; 57(7): 373–7. https://doi.org/10.5692/clinicalneurol.cn-000991
- 55Saishu Y, Yoshida T, Seino Y, Nomura T. Nivolumab-related myasthenia gravis with myositis requiring prolonged mechanical ventilation: a case report. J Med Case Rep. 2022; 16(1): 61. https://doi.org/10.1186/s13256-022-03286-x
- 56Schiopu S, Käsmann L, Schönermarck U, Fischereder M, Grabmaier U, Manapov F, et al. Pembrolizumab-induced myocarditis in a patient with malignant mesothelioma: plasma exchange as a successful emerging therapy-case report. Transl Lung Cancer Res. 2021; 10(2): 1039–46. https://doi.org/10.21037/tlcr-20-1095
- 57Shirai T, Kiniwa Y, Sato R, Sano T, Nakamura K, Mikoshiba Y, et al. Presence of antibodies to striated muscle and acetylcholine receptor in association with occurrence of myasthenia gravis with myositis and myocarditis in a patient with melanoma treated with an anti-programmed death 1 antibody. Eur J Cancer. 2019; 106: 193–5. https://doi.org/10.1016/j.ejca.2018.10.025
- 58So H, Ikeguchi R, Kobayashi M, Suzuki M, Shimizu Y, Kitagawa K. PD-1 inhibitor-associated severe myasthenia gravis with necrotizing myopathy and myocarditis. J Neurolog Sci. 2019; 399: 97–100. https://doi.org/10.1016/j.jns.2019.02.023
- 59Sugiyama Y, Esa Y, Watanabe A, Kobayashi J, Suzuki S, Takahashi D. Immune checkpoint inhibitor-induced anti-striational antibodies in myasthenia gravis and myositis: a case report. Rinsho Shinkeigaku. 2021; 61(9): 630–4. https://doi.org/10.5692/clinicalneurol.cn-001604
- 60Wakefield C, Shultz C, Patel B, Malla M. Life-threatening immune checkpoint inhibitor-induced myocarditis and myasthenia gravis overlap syndrome treated with abatacept: a case report. BMJ Case Rep. 2021; 14(11). https://doi.org/10.1136/bcr-2021-244334
- 61Xing Q, Zhang ZW, Lin QH, Shen LH, Wang PM, Zhang S, et al. Myositis-myasthenia gravis overlap syndrome complicated with myasthenia crisis and myocarditis associated with anti-programmed cell death-1 (sintilimab) therapy for lung adenocarcinoma. Ann Transl Med. 2020; 8(5): 250. https://doi.org/10.21037/atm.2020.01.79
- 62Yanase T, Moritoki Y, Kondo H, Ueyama D, Akita H, Yasui T. Myocarditis and myasthenia gravis by combined nivolumab and ipilimumab immunotherapy for renal cell carcinoma: a case report of successful management. Urol Case Rep. 2021; 34:101508. https://doi.org/10.1016/j.eucr.2020.101508
- 63Chang VA, Simpson DR, Daniels GA, Piccioni DE. Infliximab for treatment-refractory transverse myelitis following immune therapy and radiation. J Immunother Cancer. 2018; 6(1): 153. https://doi.org/10.1186/s40425-018-0471-2
- 64Charabi S, Engell-Noerregaard L, Nilsson AC, Stenör C. Case report: longitudinal extensive transverse myelitis with novel autoantibodies following two rounds of pembrolizumab. Front Neurol. 2021; 12:655283. https://doi.org/10.3389/fneur.2021.655283
- 65Esechie A, Fang X, Banerjee P, Rai P, Thottempudi N. A case report of longitudinal extensive transverse myelitis: immunotherapy related adverse effect vs. COVID-19 related immunization complications. Int J Neurosci. 2022; 1–4. https://doi.org/10.1080/00207454.2022.2050907
- 66Moodie T, Alshaqi O, Alchaki A. Longitudinal extensive transverse myelitis after chemoradiation therapy with durvalumab, a rare complication: case report. BMC Neurol. 2022; 22(1): 107. https://doi.org/10.1186/s12883-022-02576-7
- 67Nasralla S, Abboud H. Is neuromyelitis optica without AQP4-IgG a T-cell mediated disease? Insights from checkpoint inhibitor immune-related adverse events. Mult Scler Relat Disord. 2020; 46:102451. https://doi.org/10.1016/j.msard.2020.102451
- 68Picca A, Valyraki N, Birzu C, Kramkimel N, Hermine O, Zahr N, et al. Anti-Interleukin-6 and Janus kinase inhibitors for severe neurologic toxicity of checkpoint inhibitors. Neurol Neuroimmunol Neuroinflamm. 2021; 8(6):e1073. https://doi.org/10.1212/NXI.0000000000001073
- 69Wang L, Lou H, Li B, Li J, Yang YM. Paraneoplastic myelitis associated with durvalumab treatment for extensive-stage small cell lung cancer. Invest New Drugs. 2022; 40(1): 151–6. https://doi.org/10.1007/s10637-021-01154-x
- 70Burke M, Hardesty M, Downs W. A case of severe encephalitis while on PD-1 immunotherapy for recurrent clear cell ovarian cancer. Gynecol Oncol Rep. 2018; 24: 51–3. https://doi.org/10.1016/j.gore.2018.03.007
- 71Chung M, Jaffer M, Verma N, Mokhtari S, Ramsakal A, Peguero E. Immune checkpoint inhibitor induced anti-glutamic acid decarboxylase 65 (anti-GAD 65) limbic encephalitis responsive to intravenous immunoglobulin and plasma exchange. J Neurol. 2020; 267(4): 1023–5. https://doi.org/10.1007/s00415-019-09666-6
- 72Özdirik B, Jost-Brinkmann F, Savic LJ, Mohr R, Tacke F, Ploner CJ, et al. Atezolizumab and bevacizumab-induced encephalitis in advanced hepatocellular carcinoma: case report and literature review. Medicine. 2021; 100(24):e26377. https://doi.org/10.1097/MD.0000000000026377
- 73Vogrig A, Muñiz-Castrillo S, Joubert B, Picard G, Rogemond V, Marchal C, et al. Central nervous system complications associated with immune checkpoint inhibitors. J Neurol Neurosurg Psychiatry. 2020; 91(7): 772–8. https://doi.org/10.1136/jnnp-2020-323055
- 74Appelbaum J, Wells D, Hiatt JB, Steinbach G, Stewart FM, Thomas H, et al. Fatal enteric plexus neuropathy after one dose of ipilimumab plus nivolumab: a case report. J Immunother Cancer. 2018; 6(1): 82. https://doi.org/10.1186/s40425-018-0396-9
- 75Diamantopoulos PT, Tsatsou K, Benopoulou O, Anastasopoulou A, Gogas H. Inflammatory myopathy and axonal neuropathy in a patient with melanoma following pembrolizumab treatment. J Immunother. 2017; 40(6): 221–3. https://doi.org/10.1097/CJI.0000000000000172
- 76Durães J, Coutinho I, Mariano A, Geraldo A, Macário MC. Demyelinating disease of the central nervous system associated with Pembrolizumab treatment for metastatic melanoma. Mult Scler. 2019; 25(7): 1005–8. https://doi.org/10.1177/1352458518803724
- 77Liao B, Shroff S, Kamiya-Matsuoka C, Tummala S. Atypical neurological complications of ipilimumab therapy in patients with metastatic melanoma. Neuro Oncol. 2014; 16(4): 589–93. https://doi.org/10.1093/neuonc/nou001
- 78Sepúlveda M, Martinez-Hernandez E, Gaba L, Victoria I, Sola-Valls N, Falgàs N, et al. Motor polyradiculopathy during pembrolizumab treatment of metastatic melanoma. Muscle Nerve. 2017; 56(6): E162–7. https://doi.org/10.1002/mus.25672
- 79Vogrig A, Muñiz-Castrillo S, Joubert B, Picard G, Rogemond V, Skowron F, et al. Cranial nerve disorders associated with immune checkpoint inhibitors. Neurology. 2021; 96(6): e866–75. https://doi.org/10.1212/WNL.0000000000011340
- 80De Filippis S, Moore C, Ezell K, Aggarwal K, Kelkar AH. Immune checkpoint inhibitor-associated thrombotic thrombocytopenic purpura in a patient with metastatic non-small-cell lung cancer. Cureus. 2021; 13(6):e16035. https://doi.org/10.7759/cureus.16035
- 81Dickey MS, Raina AJ, Gilbar PJ, Wisniowski BL, Collins JT, Karki B, et al. Pembrolizumab-induced thrombotic thrombocytopenic purpura. J Oncol Pharm Pract. 2020; 26(5): 1237–40. https://doi.org/10.1177/1078155219887212
- 82Gergi M, Landry KK, Ades S, Barry M, Zakai NA, Herrera DA. Nivolumab-induced thrombotic thrombocytopenic purpura in a patient with anal squamous cell carcinoma: a lesson on hematologic toxicity from immunotherapy. Oncologist. 2020; 25(12): 1009–12. https://doi.org/10.1002/onco.13553
- 83Lancelot M, Miller MJ, Roback J, Stowell SR. Refractory thrombotic thrombocytopenic purpura related to checkpoint inhibitor immunotherapy. Transfusion. 2021; 61(1): 322–8. https://doi.org/10.1111/trf.16117
- 84Ali Z, Zafar MU, Wolfe Z, Akbar F, Lash B. Thrombotic thrombocytopenic purpura induced by immune checkpoint inhibitiors: a case report and review of the literature. Cureus. 2020; 12(10):e11246. https://doi.org/10.7759/cureus.11246
- 85King J, de la Cruz J, Lutzky J. Ipilimumab-induced thrombotic thrombocytopenic purpura (TTP). J Immunother Cancer. 2017; 5: 19. https://doi.org/10.1186/s40425-017-0224-7
- 86Mullally WJ, Cooke FJ, Crosbie IM, Kumar S, Abernethy VE, Jordan EJ, et al. Case report: thrombotic-thrombocytopenic purpura following Ipilimumab and nivolumab combination immunotherapy for metastatic melanoma. Front Immunol. 2022; 13:871217. https://doi.org/10.3389/fimmu.2022.871217
- 87Baek DW, Chae YS. Pembrolizumab-related autoimmune hemolytic anemia in a patient with metastatic lung adenocarcinoma: a case report. Yeungnam Univ J Med. 2021; 38(4): 366–70. https://doi.org/10.12701/yujm.2021.00899
- 88Mintjens-Jager EMW, Vos ME, Kats-Ugurlu G, Hospers GAP, Rutgers A, van Meurs M. Severe mesenteric ischemia with multiple organ failure in a patient previously treated with a humanized monoclonal antibody against programmed death receptor-1 (pembrolizumab), a case of pembrolizumab associated catastrophic antiphospholipid syndrome? SAGE Open Med Case Rep. 2020; 8:2050313X20972225. https://doi.org/10.1177/2050313X20972225
- 89Cao J, Li Q, Zhi X, Yang F, Zhu W, Zhou T, et al. Pembrolizumab-induced autoimmune Stevens-Johnson syndrome/toxic epidermal necrolysis with myositis and myocarditis in a patient with esophagogastric junction carcinoma: a case report. Transl Cancer Res. 2021; 10(8): 3870–6. https://doi.org/10.21037/tcr-21-470
- 90Chen R, Peng L, Qiu Z, Wang Y, Wei F, Zhou M, et al. Case report: cardiac toxicity associated with immune checkpoint inhibitors. Front Cardiovasc Med. 2021; 8:727445. https://doi.org/10.3389/fcvm.2021.727445
- 91Compton F, He L, Sarode R, Wodajo A, Usmani A, Burner J, et al. Immune checkpoint inhibitor toxicity: a new indication for therapeutic plasma exchange? J Clin Apheres. 2021; 36(4): 645–8. https://doi.org/10.1002/jca.21890
- 92Haddox CL, Shenoy N, Shah KK, Kao JC, Jain S, Halfdanarson TR, et al. Pembrolizumab induced bulbar myopathy and respiratory failure with necrotizing myositis of the diaphragm. Ann Oncol. 2017; 28(3): 673–5. https://doi.org/10.1093/annonc/mdw655
- 93Kao JC, Liao B, Markovic SN, Klein CJ, Naddaf E, Staff NP, et al. Neurological complications associated with anti–programmed death 1 (PD-1) antibodies. JAMA Neurol. 2017; 74(10): 1216–22. https://doi.org/10.1001/jamaneurol.2017.1912
- 94Kamo H, Hatano T, Kanai K, Aoki N, Kamiyama D, Yokoyama K, et al. Pembrolizumab-related systemic myositis involving ocular and hindneck muscles resembling myasthenic gravis: a case report. BMC Neurol. 2019; 19(1): 184. https://doi.org/10.1186/s12883-019-1416-1
- 95Liu Y, Jiang L. Tofacitinib for treatment in immune-mediated myocarditis: the first reported cases. J Oncol Pharm Pract. 2020;1078155220947141. https://doi.org/10.1177/1078155220947141
- 96Matsui H, Kawai T, Sato Y, Ishida J, Kadowaki H, Akiyama Y, et al. A fatal case of myocarditis following myositis induced by pembrolizumab treatment for metastatic upper urinary tract urothelial carcinoma. Int Heart J. 2020; 61(5): 1070–4. https://doi.org/10.1536/ihj.20-162
- 97Ohira J, Kawamoto M, Sugino Y, Kohara N. A case report of fulminant cytokine release syndrome complicated by dermatomyositis after the combination therapy with immune checkpoint inhibitors. Medicine. 2020; 99(15):e19741. https://doi.org/10.1097/MD.0000000000019741
- 98Vallet H, Gaillet A, Weiss N, Vanhaecke C, Saheb S, Touitou V, et al. Pembrolizumab-induced necrotic myositis in a patient with metastatic melanoma. Ann Oncol. 2016; 27(7): 1352–3. https://doi.org/10.1093/annonc/mdw126
- 99Yogasundaram H, Alhumaid W, Chen JW, Church M, Alhulaimi N, Kimber S, et al. Plasma exchange for immune checkpoint inhibitor-induced myocarditis. CJC Open. 2021; 3(3): 379–82. https://doi.org/10.1016/j.cjco.2020.11.004
- 100Nativi-Nicolau J, Stehlik J, Kelkhoff AJ, Khong B, Truax CM, Revelo MP, et al. Fatal allograft rejection and cardiac allograft vasculopathy after treatment with pembrolizumab for metastatic melanoma in a heart transplant recipient: a case report. Transplant Proc. 2022; 54(1): 193–6. https://doi.org/10.1016/j.transproceed.2021.09.069
- 101Ridpath AV, Rzepka PV, Shearer SM, Scrape SR, Olencki TE, Kaffenberger BH. Novel use of combination therapeutic plasma exchange and rituximab in the treatment of nivolumab-induced bullous pemphigoid. Int J Dermatol. 2018; 57(11): 1372–4. https://doi.org/10.1111/ijd.13970
- 102Tchapyjnikov D, Borst AJ. Immune-related neurological symptoms in an adolescent patient receiving the checkpoint inhibitor nivolumab. J Immunother. 2017; 40(7): 286–8. https://doi.org/10.1097/CJI.0000000000000177
- 103Thakker M, Quadri K, Desai A, Illyas W, Kim MY, Desai S, et al. Pembrolizumab and severe hypertriglyceridemia requiring apheresis: an immune-related adverse event. J Oncol Pract. 2019; 15(11): 613–4. https://doi.org/10.1200/JOP.19.00245
- 104Zhou H, Li N, Tang H, Chen H, Chen X, Zhang L, et al. Delayed thrombocytopenia as a rare but serious adverse event secondary to immune checkpoint inhibitor: a case report. Ann Palliat Med. 2021; 10(5): 5881–6. https://doi.org/10.21037/apm-21-794
- 105Al-Nattah S, Lata Sharma K, Caldis M, Spengler E, Nicholas RW. Plasmapheresis for Pembrolizumab-induced hepatitis in a patient with squamous cell carcinoma and prior orthotopic liver transplantation. Case Rep Hepatol. 2022; 2022:5908411. https://doi.org/10.1155/2022/5908411
- 106Tan YW, Chen L, Zhou XB. Efficacy of artificial liver support system in severe immune-associated hepatitis caused by camrelizumab: a case report and review of the literature. World J Clin Cases. 2021; 9(17): 4415–22. https://doi.org/10.12998/wjcc.v9.i17.4415
- 107Thorsteinsdottir T, Løitegård T, Reims HM, Porojnicu AC. Fatal Cholestatic liver injury during treatment with PD1 immune checkpoint inhibitor for malignant melanoma: a case report. Case Rep Oncol. 2020; 13(2): 659–63. https://doi.org/10.1159/000507695
- 108Wu Z, Lai L, Li M, Zhang L, Zhang W. Acute liver failure caused by pembrolizumab in a patient with pulmonary metastatic liver cancer: a case report. Medicine. 2017; 96(51):e9431. https://doi.org/10.1097/MD.0000000000009431
- 109Antaki F, Ferreira BG, Sahyoun JY, Hammamji K. Bilateral diffuse uveal melanocytic proliferation: report of a novel optical coherence tomography finding and clinical response to plasmapheresis. Am J Ophthalmol Case Rep. 2022; 25:101349. https://doi.org/10.1016/j.ajoc.2022.101349
- 110Katzburg E, Zur D, Gutfeld O, Kirgner I, Habot-Wilner Z. Bilateral diffuse uveal melanocytic proliferation in a woman with metastatic scalp squamous cell carcinoma treated with cemiplimab. Case Rep Ophthalmol. 2021; 12(3): 961–6. https://doi.org/10.1159/000520467
- 111Fasano G, Pabon IM, Longhitano Y, Zanza C, Carlidi G, Ravera E, et al. Pembrolizumab-related side effects: acute renal failure and severe neurological toxicity. Medicina. 2022; 58(2). https://doi.org/10.3390/medicina58020209
- 112Laamech R, Terrec F, Emprou C, Toffart AC, Pierret T, Naciri-Bennani H, et al. Efficacy of plasmapheresis in nivolumab-associated ANCA glomerulonephritis: a case report and pathophysiology discussion. Case Rep Nephrol Dial. 2021; 11(3): 376–83. https://doi.org/10.1159/000518304
- 113Mamlouk O, Lin JS, Abdelrahim M, Tchakarov AS, Glass WF, Selamet U, et al. Checkpoint inhibitor-related renal vasculitis and use of rituximab. J Immunother Cancer. 2020; 8(2):e000750. https://doi.org/10.1136/jitc-2020-000750
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