Research progress on the ocular adverse effects associated with immune checkpoint inhibitor therapy_Chinese Journal of Ocular Fundus Diseases

Authors：

Guo Weiyan ^1,2,3 , Lin Xuemei ^1,3 ,  Wu Songdi ^1,3

1. Department of Neuro-ophthalmology, The First Affiliated Hospital of Northwest University (Xi'anNo.1 Hospital), Xi'an 710002, China;
2. Department of Pharmacy, The First Affiliated Hospital of Northwest University (Xi'an No.1 Hospital), Xi'an 710002, China;
3. Xi'an Key Laboratory of Innovation and Transformation of Neuroimmunological Diseases, Xi'an 710002, China;

Corresponding author：

Wu Songdi, Email: wusongdi@gmail.com

Keywords：

Immune checkpoint inhibitors; Ocular adverse effect; Review

DOI：

10.3760/cma.j.cn511434-20230313-00120

Video：

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Abstract Full text Figures/Tables Video References Cited by

Immune checkpoint inhibitors (ICI) have revolutionized the field of oncology by regulating the interaction between immune cells and cancer cells and promoting the disinhibition of the immune system, thus targeting various types of malignant tumors. However, the regulation of the immune system can also trigger related adverse reactions. Currently, there are no specific clinical guidelines for the treatment of these adverse reactions. Treatment decisions largely depend on clinical judgment and experience.The pathogenesis of ICI-related ocular adverse events is not fully understood at present. Further research on the specific mechanisms of action can provide new insights into the early diagnosis and treatment of ICI-related ocular adverse events.

Citation： Guo Weiyan, Lin Xuemei, Wu Songdi. Research progress on the ocular adverse effects associated with immune checkpoint inhibitor therapy. Chinese Journal of Ocular Fundus Diseases, 2023, 39(12): 1033-1038. doi: 10.3760/cma.j.cn511434-20230313-00120 Copy

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1. Esfahani K, Elkrief A, Calabrese C, et al. Moving towards personalized treatments of immune-related adverse events[J]. Nat Rev Clin Oncol, 2020, 17(8): 504-515. DOI: 10.1038/s41571-020-0352-8.
2. Buchbinder E, Hodi FS. Cytotoxic T lymphocyte antigen-4 and immune checkpoint blockade[J]. J Clin Invest, 2015, 125(9): 3377-3383. DOI: 10.1172/JCI80012.
3. Ohaegbulam KC, Assal A, Lazar-Molnar E, et al. Human cancer immunotherapy with antibodies to the PD-1 and PD-L1 pathway[J]. Trends Mol Med, 2015, 21(1): 24-33. DOI: 10.1016/j.molmed.2014.10.009.
4. Cousin S, Italiano A. Molecular pathways: immune checkpoint antibodies and their toxicities[J]. Clin Cancer Res, 2016, 22(18): 4550-4555. DOI: 10.1158/1078-0432.CCR-15-2569.
5. Puwanant A, Isfort M, Lacomis D, et al. Clinical spectrum of neuromuscular complications after immune checkpoint inhibition[J]. Neuromuscul Disord, 2019, 29(2): 127-133. DOI: 10.1016/j.nmd.2018.11.012.
6. Zhou L, Wei X. Ocular immune-related adverse eevents associated with iimmune checkpoint inhibitors in lung cancer[J/OL]. Front Immunol, 2021, 12: 701951[2021-08-04]. https://pubmed.ncbi.nlm.nih.gov/34504488/. DOI: 10.3389/fimmu.2021.701951.
7. Bomze D, MeirsonT, Hasan AliO, et al. Ocular aadverse events iinduced by immune checkpoint inhibitors: a ccomprehensive pharmacovigilance analysis[J]. Ocul Immunol Inflamm, 2022, 30(1): 191-197. DOI: 10.1080/09273948.2020.1773867.
8. Francis JH, JabenK, Santomasso BD, et al. Immune checkpoint inhibitor-associated optic neuritis[J]. Ophthalmology, 2020, 127(11): 1585-1589. DOI: 10.1016/j.ophtha.2020.05.003.
9. 刘小伟, 王铮, 赵潺, 等. 肿瘤靶向治疗和免疫治疗眼科系统毒性反应的诊治[J]. 中国肺癌杂志, 2019, 22(10): 653-660. DOI: 10.3779/j.issn.1009-3419.2019.10.09.Liu XW, Wang Z, Zhao C, et al. Clinical diagnosis and treatment recommendations for ocular toxicities of target therapy and immune checkpoint inhibitor therapy[J]. Chin J Lung Cancer, 2019, 22(10): 653-660. DOI: 10.3779/j.issn.1009-3419.2019.10.09.
10. 汪龙, 周宁宁, 王慕华, 等. 免疫检查点抑制剂致神经系统不良反应[J]. 中国医院药学杂志, 2018, 38(16): 1735-1738. DOI: 10.13286/j.cnki.chinhosppharmacyj.2018.16.14.Wang L, Zhou NN, Wang MH, et al. Neurological adverse effect induced by immune checkpoint blockades[J]. Chin Hosp Pharm J, 2018, 38(16): 1735-1738. DOI: 10.13286/j.cnki.chinhosppharmacyj.2018.16.14.
11. Park RB, JainS, Han H, et al. Ocular surface disease associated with immune checkpoint inhibitor therapy[J]. Ocul Surf, 2021, 20: 115-129. DOI: 10.1016/j.jtos.2021.02.004.
12. Papavasileiou E, Prasad S, Freitag SK, et al. Ipilimumab-induced ocular and orbital inflammation--a case series and review of the literature[J]. Ocul Immunol Inflamm, 2016, 24(2): 140-146. DOI: 10.3109/09273948.2014.1001858.
13. Mantopoulos D, KendraKL, Letson AD, et al. Bilateral choroidopathy and serous retinal detachments during ipilimumab treatment for cutaneous melanoma[J]. JAMA Ophthalmol, 2015, 133(8): 965-967. DOI: 10.1001/jamaophthalmol.2015.1128.
14. Crews J, Agarwal A, Jack L, et al. Ipilimumab-associated retinopathy[J]. Ophthalmic Surg Lasers Imaging Retina, 2015, 46(6): 658-660. DOI: 10.3928/23258160-20150610-10.
15. Alba-Linero C, Alba E. Ocular side effects of checkpoint inhibitors[J]. SurvOphthalmol, 2021, 66(6): 951-959. DOI: 10.1016/j.survophthal.2021.01.001.
16. Wu SZ, MasurkarAV, BalcerLJ. Afferent and efferent visual markers of Alzheimer's disease: a review and update in early stage disease[J/OL]. Front Aging Neurosci, 2020, 12: 572337[2020-09-11]. https://pubmed.ncbi.nlm.nih.gov/33061906/. DOI: 10.3389/fnagi.2020.572337.
17. Yu CW, Yau M, Mezey N, et al. Neuro-ophthalmic complications of immune checkpoint inhibitors: a systematic review[J]. Eye Brain, 2020, 12: 139-167. DOI: 10.2147/EB.S277760.
18. Wilhelm H, Schabet M. The diagnosis and treatment of optic neuritis[J]. DtschArztebl Int, 2015, 112(37): 616-625. DOI: 10.3238/arztebl.2015.0616.
19. Shimada T, Hoshino Y, Tsunemi T, et al. Neuromyelitis optica spectrum disorder after treatment with pembrolizumab[J/OL]. Mult Scler Relat Disord, 2020, 37: 101447[2019-10-14]. https://pubmed.ncbi.nlm.nih.gov/31655267/. DOI: 10.1016/j.msard.2019.101447.
20. Hirano S, Kojima A, Nakayama Y, et al. A case report of neuromyelitis optica spectrum disorder induced by pembrolizumab treatment for lung adenocarcinoma: a clinical and immunohistochemical study[J]. BMC Neurol, 2022, 22(1): 483. DOI: 10.1186/s12883-022-02987-6.
21. Khimani K, Patel SP, Whyte A, et al. Case report: neuromyelitis optica after treatment of uveal melanoma with Nivolumab and Ipilimumab[J/OL]. Front Oncol, 2022, 12: 806501[2022-03-23]. https://pubmed.ncbi.nlm.nih.gov/35402220/. DOI: 10.3389/fonc.2022.806501.
22. Goldstein BL, Gedmintas L, Todd DJ. Drug-associated polymyalgia rheumatica/giant cell arteritis occurring in two patients after treatment with ipilimumab, an antagonist of CTLA-4[J]. Arthritis Rheumatol, 2014, 66(3): 768-769. DOI: 10.1002/art.38282.
23. Micaily I CM. An unknown reaction to pembrolizumab: giant cell arteritis[J]. Ann Oncol, 2017, 28: 2621–2622. DOI: 10.1093/annonc/mdx306.
24. Hid Cadena R, AbdulahadWH, HospersGAP, et al. Checks and balances in autoimmune vasculitis[J/OL]. Front Immunol, 2018, 9: 315[2018-02-22]. https://pubmed.ncbi.nlm.nih.gov/29520282/. DOI: 10.3389/fimmu.2018.00315.
25. Betrains AE, Blockmans DE. Immune checkpoint inhibitor-associated polymyalgia rheumatica/giant cell arteritis occurring in a patient after treatment with nivolumab[J]. J Clin Rheumatol, 2021, 27(8S): S555-556. DOI: 10.1097/RHU.0000000000001012.
26. Chow KL, Perju-Dumbrava L, Malhotra A. Giant cell arteritis secondary to combined nivolumab and ipilimumab in metastatic pleural mesothelioma[J]. Neurol Asia, 2020: 25.
27. Hahn L, Pepple KL. Bilateral neuroretinitis and anterior uveitis following ipilimumab treatment for metastatic melanoma[J]. J Ophthalmic Inflamm Infect, 2016, 6(1): 14. DOI: 10.1186/s12348-016-0082-3.
28. Pula JH, Yuen CA. Eyes and stroke: the visual aspects of cerebrovascular disease[J]. Stroke Vasc Neurol, 2017, 2(4): 210-220. DOI: 10.1136/svn-2017-000079.
29. Drobni ZD, Alvi RM, Taron J, et al. Association between immune checkpoint inhibitors with cardiovascular events and atherosclerotic plaque[J]. Circulation, 2020, 142(24): 2299-2311. DOI: 10.1161/CIRCULATIONAHA.120.049981.
30. Johnson DB, Manouchehri A, Haugh AM, et al. Neurologic toxicity associated with immune checkpoint inhibitors: a pharmacovigilance study[J]. J Immunother Cancer, 2019, 7(1): 134. DOI: 10.1186/s40425-019-0617-x.
31. Safa H, Johnson DH, Trinh VA, et al. Immune checkpoint inhibitor related myasthenia gravis: single center experience and systematic review of the literature[J]. J Immunother Cancer, 2019, 7(1): 319. DOI: 10.1186/s40425-019-0774-y.
32. Suzuki S, Ishikawa N, Konoeda F, et al. Nivolumab-related myasthenia gravis with myositis and myocarditis in Japan[J]. Neurology, 2017, 89(11): 1127-1134. DOI: 10.1212/WNL.0000000000004359.
33. Pathak R, Katel A, Massarelli E, et al. Immune checkpoint inhibitor-induced myocarditis with myositis/myasthenia gravis overlap syndrome: a systematic review of cases[J]. Oncologist, 2021, 26(12): 1052-1061. DOI: 10.1002/onco.13931.
34. Onda A, Miyagawa S, Takahashi N, et al. Pembrolizumab-induced ocular myasthenia gravis with anti-titin antibody and necrotizing myopathy[J]. Intern Med, 2019, 58(11): 1635-1638. DOI: 10.2169/internalmedicine.1956-18.
35. Stelmachowska-Banaś M, Czajka-Oraniec I. Management of endocrine immune-related adverse events of immune checkpoint inhibitors: an updated review[J]. Endocr Connect, 2020, 9(10): 207-228. DOI: 10.1530/EC-20-0342.
36. Peiffert M, Cugnet-Anceau C, Dalle S, et al. Graves' disease during immune checkpoint inhibitor therapy (a case series and literature review)[J/OL]. Cancers (Basel), 2021, 13(8): 1944[2021-04-17]. https://pubmed.ncbi.nlm.nih.gov/33920721/. DOI: 10.3390/cancers13081944.
37. Chau CYC, Shih KC, Chow LLW, et al. Considerations for use of immune checkpoint inhibitors in cancer therapy for patients with coexisting thyroid eye disease[J]. Ophthalmol Ther, 2021, 10(1): 5-12. DOI: 10.1007/s40123-020-00317-y.
38. Wladis EJ, Kambam ML. Ophthalmic complications of immune checkpoint inhibitors[J]. Orbit, 2022, 41(1): 28-33. DOI: 10.1080/01676830.2020.1867192.
39. Moreira A, Loquai C, Pfohler C, et al. Myositis and neuromuscular side-effects induced by immune checkpoint inhibitors[J]. Eur J Cancer, 2019, 106: 12-23. DOI: 10.1016/j.ejca.2018.09.033.
40. Kang KH, Grubb W, Sawlani K, et al. Immune checkpoint-mediated myositis and myasthenia gravis: a case report and review of evaluation and management[J]. Am J Otolaryngol, 2018, 39(5): 642-645. DOI: 10.1016/j.amjoto.2018.06.003.
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