Characteristics, diagnosis and treatment of ocular fundus diseases associated with COVID-19_Chinese Journal of Ocular Fundus Diseases

Authors：

 Xu Gezhi , Zhuang Hong

Department of Ophthalmology, Shanghai Eye & ENT Hospital of Fudan University, Shanghai Key Laboratory of Visual Impairment and Reconstruction, Shanghai 200031, China;

Corresponding author：

Xu Gezhi, Email: drxugezhi@163.com

Keywords：

COVID-19; Ocular fundus diseases; Acute macular neuroretinopathy; Uveitis; Editorial

DOI：

10.3760/cma.j.cn511434-20230816-00347

Video：

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The COVID-19 causes multiple organ dysfunction such as respiratory system, meanwhile it causes ocular fundus diseases threatening visual function. The occurrence of COVID-19 related fundus diseases is associated with retinal capillary ischemia, thrombosis, and immune inflammatory response. COVID-19 related fundus diseases mainly include cotton wool spots and microhaemorrhages, retinal vascular occlusion, paracentral acute middle maculopathy, acute macular neuroretinopathy, uveitis, and endogenous endophthalmitis. We will summarize the clinical characteristics of COVID-19 related fundus diseases based on literature reports and clinical practice, and share some thoughts on its diagnosis and treatment.

Citation： Xu Gezhi, Zhuang Hong. Characteristics, diagnosis and treatment of ocular fundus diseases associated with COVID-19. Chinese Journal of Ocular Fundus Diseases, 2023, 39(9): 715-719. doi: 10.3760/cma.j.cn511434-20230816-00347 Copy

1.	Yang N, Wang C, Huang J, et al. Clinical and pulmonary CT characteristics of patients infected with the SARS-CoV-2 omicron variant compared with those of patients infected with the alpha viral strain[J/OL]. Front Public Health, 2022, 10: 931480[2022-07-12]. https://pubmed.ncbi.nlm.nih.gov/35903393/. DOI: 10.3389/fpubh.2022.931480.
2.	李雪杰, 汪明, 陈长征, 等. 伴发或首发病毒性结膜炎的新型冠状病毒感染下眼科医师的防控策略[J]. 中华实验眼科杂志, 2020, 38(3): 276-280. DOI: 10.3760/cma.j.issn.2095-0160.2020.0002.Li XJ, Wang M, Chen CZ, et al. Prevention and control strategy of ophthalmologists under novel coronavirus infection with conjunctivitis or first viral conjunctivitis[J]. Chin J Exp Ophthalmol, 2020, 38(3): 276-280. DOI: 10.3760/cma.j.issn.2095-0160.2020.0002.
3.	Wu P, Duan F, Luo C, et al. Characteristics of ocular findings of patients with coronavirus disease 2019 (COVID-19) in Hubei province, China[J]. JAMA Ophthalmol, 2020, 138(5): 575-578. DOI: 10.1001/jamaophthalmol.2020.1291.
4.	Zhou L, Xu Z, Guerra J, et al. Expression of the SARS-CoV-2 receptor ACE2 in human retina and diabetes-implications for retinopathy[J]. Invest Ophthalmol Vis Sci, 2021, 62(7): 6. DOI: 10.1167/iovs.62.7.6.
5.	Varga Z, Flammer AJ, Steiger P, et al. Endothelial cell infection and endotheliitis in COVID-19[J]. Lancet, 2020, 395(10234): 1417-1418. DOI: 10.1016/S0140-6736(20)30937-5.
6.	Jayasundera KT, Abuzaitoun RO, Musch DC. COVID-19 diagnosis and incidence of retinal thromboembolism[J]. JAMA Ophthalmol, 2022, 140(5): 527-528. DOI: 10.1001/jamaophthalmol.2022.0666.
7.	Galeotti C, Bayry J. Autoimmune and inflammatory diseases following COVID-19[J]. Nat Rev Rheumatol, 2020, 16(8): 413-414. DOI: 10.1038/s41584-020-0448-7.
8.	Marinho PM, Marcos AAA, Romano AC, et al. Retinal findings in patients with COVID-19[J/OL]. Lancet, 2020, 395(10237): 1610[2020-05-23]. https://pubmed.ncbi.nlm.nih.gov/32405105/. DOI: 10.1016/S0140-6736(20)31014-X.
9.	Riotto E, Mégevand V, Mégevand A, et al. Retinal manifestations in patients with COVID-19: a prospective cohort study[J/OL]. J Clin Med, 2022, 11(7): 1828[2022-03-25]. https://pubmed.ncbi.nlm.nih.gov/35407441/. DOI: 10.3390/jcm11071828.
10.	张黎, 刘宇奇, 袁容娣. 新型冠状病毒感染相关Purtscher样视网膜病变临床特征[J]. 中华眼底病杂志, 2023, 39(3): 227-231. DOI: 10.3760/cma.j.cn511434-20230112-00021.Zhang L, Liu YQ, Yuan RD. Clinical features of Purtscher-like retinopathy associated with COVID-19[J]. Chin J Ocul Fundus Dis, 2023, 39(3): 227-231. DOI: 10.3760/cma.j.cn511434-20230112-00021.
11.	Invernizzi A, Torre A, Parrulli S, et al. Retinal findings in patients with COVID-19: results from the SERPICO-19 study[J/OL]. EClinicalMedicine, 2020, 27: 100550[2020-09-20]. https://pubmed.ncbi.nlm.nih.gov/32984785/. DOI: 10.1016/j.eclinm.2020.100550.
12.	Fonollosa A, Hernández-Rodríguez J, Cuadros C, et al. Characterizing COVID-19-related retinal vascular occlusions: a case series and review of the literature[J]. Retina, 2022, 42(3): 465-475. DOI: 10.1097/IAE.0000000000003327.
13.	Invernizzi A, Pellegrini M, Messenio D, et al. Impending central retinal vein occlusion in a patient with coronavirus disease 2019 (COVID-19)[J]. Ocul Immunol Inflamm, 2020, 28(8): 1290-1292. DOI: 10.1080/09273948.2020.1807023.
14.	Ucar F, Cetinkaya S. Central retinal artery occlusion in a patient who contracted COVID-19 and review of similar cases[J/OL]. BMJ Case Rep, 2021, 14(7): e244181[2021-07-27]. https://pubmed.ncbi.nlm.nih.gov/34315751/. DOI: 10.1136/bcr-2021-244181.
15.	Padhy SK, Dcruz RP, Kelgaonkar A. Paracentral acute middle maculopathy following SARS-CoV-2 infection: the D-dimer hypothesis[J/OL]. BMJ Case Rep, 2021, 14(3): e242043[2021-07-27]. https://pubmed.ncbi.nlm.nih.gov/34315751/. DOI: 10.1136/bcr-2021-242043.
16.	Virgo J, Mohamed M. Paracentral acute middle maculopathy and acute macular neuroretinopathy following SARS-CoV-2 infection[J]. Eye (Lond), 2020, 34(12): 2352-2353. DOI: 10.1038/s41433-020-1069-8.
17.	Sarraf D, Rahimy E, Fawzi AA, et al. Paracentral acute middle maculopathy: a new variant of acute macular neuroretinopathy associated with retinal capillary ischemia[J]. JAMA Ophthalmol, 2013, 131(10): 1275-1287. DOI: 10.1001/jamaophthalmol.2013.4056.
18.	Ashfaq I, Vrahimi M, Waugh S, et al. Acute macular neuroretinopathy associated with acute influenza virus infection[J]. Ocul Immunol Inflamm, 2021, 29(2): 333-339. DOI: 10.1080/09273948.2019.1681470.
19.	Li M, Zhang X, Ji Y, et al. Acute macular neuroretinopathy in dengue fever: short-term prospectively followed up case series[J]. JAMA Ophthalmol, 2015, 133(11): 1329-1333. DOI: 10.1001/jamaophthalmol.2015.2687.
20.	Azar G, Bonnin S, Vasseur V, et al. Did the COVID-19 pandemic increase the incidence of acute macular neuroretinopathy?[J/OL]. J Clin Med, 2021, 10(21): 5038[2021-10-28]. https://pubmed.ncbi.nlm.nih.gov/34768555/. DOI: 10.3390/jcm10215038.
21.	熊凤, 帅娜, 周抒, 等. 新型冠状病毒感染相关急性黄斑神经视网膜病变的临床及眼底影像特征[J]. 中华眼底病杂志, 2023, 39(3): 214-217. DOI: 10.3760/cma.j.cn511434-20230103-00675.Xiong F, Shuai N, Zhou S, et al. Clinical and fundus imaging features of acute macular neuroretinopathy associated with COVID-19[J]. Chin J Ocul Fundus Dis, 2023, 39(3): 214-217. DOI: 10.3760/cma.j.cn511434-20230103-00675.
22.	钟育晟, 程湧, 赵明威, 等. 新型冠状病毒感染相关急性黄斑神经视网膜病变的临床特征[J]. 中华眼底病杂志, 2023, 39(3): 218-222. DOI: 10.3760/cma.j.cn511434-20230204-00043.Zhong YS, Cheng Y, Zhao MW, et al. Clinical features of acute macular neuroretinopathy associated with COVID-19[J]. Chin J Ocul Fundus Dis, 2023, 39(3): 218-222. DOI: 10.3760/cma.j.cn511434-20230204-00043.
23.	Fawzi AA, Pappuru RR, Sarraf D, et al. Acute macular neuroretinopathy: long-term insights revealed by multimodal imaging[J]. Retina, 2012, 32(8): 1500-1513. DOI: 10.1097/IAE.0b013e318263d0c3.
24.	刘扶摇, 帅娜, 闫华婧, 等. 新型冠状病毒感染伴多发性一过性白点综合征1例[J]. 中华眼底病杂志, 2023, 39(3): 249-250. DOI: 10.3760/cma.j.cn511434-20230103-00682.Liu FY, Shuai N, Yan HJ, et al. A case of novel coronavirus infection with multiple transient white spot syndrome[J]. Chin J Ocul Fundus Dis, 2023, 39(3): 249-250. DOI: 10.3760/cma.j.cn511434-20230103-00682.
25.	Jain A, Shilpa IN, Biswas J. Multiple evanescent white dot syndrome following SARS-CoV-2 infection-a case report[J]. Indian J Ophthalmol, 2022, 70(4): 1418-1420. DOI: 10.4103/ijo.IJO_3093_21.
26.	Miyata M, Ooto S, Muraoka Y. Punctate inner choroidopathy immediately after COVID-19 infection: a case report[J]. BMC Ophthalmol, 2022, 22(1): 297. DOI: 10.1186/s12886-022-02514-8.
27.	Anthony E, Rajamani A, Baskaran P, et al. Vogt Koyanagi Harada disease following a recent COVID-19 infection[J]. Indian J Ophthalmol, 2022, 70(2): 670-672. DOI: 10.4103/ijo.IJO_2550_21.
28.	Dutta Majumder P. Endogenous fungal endophthalmitis in COVID-19 patients: an unexplored possibility[J]. Indian J Ophthalmol, 2022, 70(4): 1083-1085. DOI: 10.4103/ijo.IJO_510_22.
29.	Bilgic A, Sudhalkar A, Gonzalez-Cortes JH, et al. Endogenous endophthalmitis in the setting of COVID-19 infection: a case series[J]. Retina, 2021, 41(8): 1709-1714. DOI: 10.1097/IAE.0000000000003168.
30.	Zhuang H, Ding X, Gao F, et al. Optical coherence tomography features of retinal lesions in Chinese patients with endogenous Candida endophthalmitis[J]. BMC Ophthalmol, 2020, 20(1): 52. DOI: 10.1186/s12886-020-01337-9.

1. Yang N, Wang C, Huang J, et al. Clinical and pulmonary CT characteristics of patients infected with the SARS-CoV-2 omicron variant compared with those of patients infected with the alpha viral strain[J/OL]. Front Public Health, 2022, 10: 931480[2022-07-12]. https://pubmed.ncbi.nlm.nih.gov/35903393/. DOI: 10.3389/fpubh.2022.931480.
2. 李雪杰, 汪明, 陈长征, 等. 伴发或首发病毒性结膜炎的新型冠状病毒感染下眼科医师的防控策略[J]. 中华实验眼科杂志, 2020, 38(3): 276-280. DOI: 10.3760/cma.j.issn.2095-0160.2020.0002.Li XJ, Wang M, Chen CZ, et al. Prevention and control strategy of ophthalmologists under novel coronavirus infection with conjunctivitis or first viral conjunctivitis[J]. Chin J Exp Ophthalmol, 2020, 38(3): 276-280. DOI: 10.3760/cma.j.issn.2095-0160.2020.0002.
3. Wu P, Duan F, Luo C, et al. Characteristics of ocular findings of patients with coronavirus disease 2019 (COVID-19) in Hubei province, China[J]. JAMA Ophthalmol, 2020, 138(5): 575-578. DOI: 10.1001/jamaophthalmol.2020.1291.
4. Zhou L, Xu Z, Guerra J, et al. Expression of the SARS-CoV-2 receptor ACE2 in human retina and diabetes-implications for retinopathy[J]. Invest Ophthalmol Vis Sci, 2021, 62(7): 6. DOI: 10.1167/iovs.62.7.6.
5. Varga Z, Flammer AJ, Steiger P, et al. Endothelial cell infection and endotheliitis in COVID-19[J]. Lancet, 2020, 395(10234): 1417-1418. DOI: 10.1016/S0140-6736(20)30937-5.
6. Jayasundera KT, Abuzaitoun RO, Musch DC. COVID-19 diagnosis and incidence of retinal thromboembolism[J]. JAMA Ophthalmol, 2022, 140(5): 527-528. DOI: 10.1001/jamaophthalmol.2022.0666.
7. Galeotti C, Bayry J. Autoimmune and inflammatory diseases following COVID-19[J]. Nat Rev Rheumatol, 2020, 16(8): 413-414. DOI: 10.1038/s41584-020-0448-7.
8. Marinho PM, Marcos AAA, Romano AC, et al. Retinal findings in patients with COVID-19[J/OL]. Lancet, 2020, 395(10237): 1610[2020-05-23]. https://pubmed.ncbi.nlm.nih.gov/32405105/. DOI: 10.1016/S0140-6736(20)31014-X.
9. Riotto E, Mégevand V, Mégevand A, et al. Retinal manifestations in patients with COVID-19: a prospective cohort study[J/OL]. J Clin Med, 2022, 11(7): 1828[2022-03-25]. https://pubmed.ncbi.nlm.nih.gov/35407441/. DOI: 10.3390/jcm11071828.
10. 张黎, 刘宇奇, 袁容娣. 新型冠状病毒感染相关Purtscher样视网膜病变临床特征[J]. 中华眼底病杂志, 2023, 39(3): 227-231. DOI: 10.3760/cma.j.cn511434-20230112-00021.Zhang L, Liu YQ, Yuan RD. Clinical features of Purtscher-like retinopathy associated with COVID-19[J]. Chin J Ocul Fundus Dis, 2023, 39(3): 227-231. DOI: 10.3760/cma.j.cn511434-20230112-00021.
11. Invernizzi A, Torre A, Parrulli S, et al. Retinal findings in patients with COVID-19: results from the SERPICO-19 study[J/OL]. EClinicalMedicine, 2020, 27: 100550[2020-09-20]. https://pubmed.ncbi.nlm.nih.gov/32984785/. DOI: 10.1016/j.eclinm.2020.100550.
12. Fonollosa A, Hernández-Rodríguez J, Cuadros C, et al. Characterizing COVID-19-related retinal vascular occlusions: a case series and review of the literature[J]. Retina, 2022, 42(3): 465-475. DOI: 10.1097/IAE.0000000000003327.
13. Invernizzi A, Pellegrini M, Messenio D, et al. Impending central retinal vein occlusion in a patient with coronavirus disease 2019 (COVID-19)[J]. Ocul Immunol Inflamm, 2020, 28(8): 1290-1292. DOI: 10.1080/09273948.2020.1807023.
14. Ucar F, Cetinkaya S. Central retinal artery occlusion in a patient who contracted COVID-19 and review of similar cases[J/OL]. BMJ Case Rep, 2021, 14(7): e244181[2021-07-27]. https://pubmed.ncbi.nlm.nih.gov/34315751/. DOI: 10.1136/bcr-2021-244181.
15. Padhy SK, Dcruz RP, Kelgaonkar A. Paracentral acute middle maculopathy following SARS-CoV-2 infection: the D-dimer hypothesis[J/OL]. BMJ Case Rep, 2021, 14(3): e242043[2021-07-27]. https://pubmed.ncbi.nlm.nih.gov/34315751/. DOI: 10.1136/bcr-2021-242043.
16. Virgo J, Mohamed M. Paracentral acute middle maculopathy and acute macular neuroretinopathy following SARS-CoV-2 infection[J]. Eye (Lond), 2020, 34(12): 2352-2353. DOI: 10.1038/s41433-020-1069-8.
17. Sarraf D, Rahimy E, Fawzi AA, et al. Paracentral acute middle maculopathy: a new variant of acute macular neuroretinopathy associated with retinal capillary ischemia[J]. JAMA Ophthalmol, 2013, 131(10): 1275-1287. DOI: 10.1001/jamaophthalmol.2013.4056.
18. Ashfaq I, Vrahimi M, Waugh S, et al. Acute macular neuroretinopathy associated with acute influenza virus infection[J]. Ocul Immunol Inflamm, 2021, 29(2): 333-339. DOI: 10.1080/09273948.2019.1681470.
19. Li M, Zhang X, Ji Y, et al. Acute macular neuroretinopathy in dengue fever: short-term prospectively followed up case series[J]. JAMA Ophthalmol, 2015, 133(11): 1329-1333. DOI: 10.1001/jamaophthalmol.2015.2687.
20. Azar G, Bonnin S, Vasseur V, et al. Did the COVID-19 pandemic increase the incidence of acute macular neuroretinopathy?[J/OL]. J Clin Med, 2021, 10(21): 5038[2021-10-28]. https://pubmed.ncbi.nlm.nih.gov/34768555/. DOI: 10.3390/jcm10215038.
21. 熊凤, 帅娜, 周抒, 等. 新型冠状病毒感染相关急性黄斑神经视网膜病变的临床及眼底影像特征[J]. 中华眼底病杂志, 2023, 39(3): 214-217. DOI: 10.3760/cma.j.cn511434-20230103-00675.Xiong F, Shuai N, Zhou S, et al. Clinical and fundus imaging features of acute macular neuroretinopathy associated with COVID-19[J]. Chin J Ocul Fundus Dis, 2023, 39(3): 214-217. DOI: 10.3760/cma.j.cn511434-20230103-00675.
22. 钟育晟, 程湧, 赵明威, 等. 新型冠状病毒感染相关急性黄斑神经视网膜病变的临床特征[J]. 中华眼底病杂志, 2023, 39(3): 218-222. DOI: 10.3760/cma.j.cn511434-20230204-00043.Zhong YS, Cheng Y, Zhao MW, et al. Clinical features of acute macular neuroretinopathy associated with COVID-19[J]. Chin J Ocul Fundus Dis, 2023, 39(3): 218-222. DOI: 10.3760/cma.j.cn511434-20230204-00043.
23. Fawzi AA, Pappuru RR, Sarraf D, et al. Acute macular neuroretinopathy: long-term insights revealed by multimodal imaging[J]. Retina, 2012, 32(8): 1500-1513. DOI: 10.1097/IAE.0b013e318263d0c3.
24. 刘扶摇, 帅娜, 闫华婧, 等. 新型冠状病毒感染伴多发性一过性白点综合征1例[J]. 中华眼底病杂志, 2023, 39(3): 249-250. DOI: 10.3760/cma.j.cn511434-20230103-00682.Liu FY, Shuai N, Yan HJ, et al. A case of novel coronavirus infection with multiple transient white spot syndrome[J]. Chin J Ocul Fundus Dis, 2023, 39(3): 249-250. DOI: 10.3760/cma.j.cn511434-20230103-00682.
25. Jain A, Shilpa IN, Biswas J. Multiple evanescent white dot syndrome following SARS-CoV-2 infection-a case report[J]. Indian J Ophthalmol, 2022, 70(4): 1418-1420. DOI: 10.4103/ijo.IJO_3093_21.
26. Miyata M, Ooto S, Muraoka Y. Punctate inner choroidopathy immediately after COVID-19 infection: a case report[J]. BMC Ophthalmol, 2022, 22(1): 297. DOI: 10.1186/s12886-022-02514-8.
27. Anthony E, Rajamani A, Baskaran P, et al. Vogt Koyanagi Harada disease following a recent COVID-19 infection[J]. Indian J Ophthalmol, 2022, 70(2): 670-672. DOI: 10.4103/ijo.IJO_2550_21.
28. Dutta Majumder P. Endogenous fungal endophthalmitis in COVID-19 patients: an unexplored possibility[J]. Indian J Ophthalmol, 2022, 70(4): 1083-1085. DOI: 10.4103/ijo.IJO_510_22.
29. Bilgic A, Sudhalkar A, Gonzalez-Cortes JH, et al. Endogenous endophthalmitis in the setting of COVID-19 infection: a case series[J]. Retina, 2021, 41(8): 1709-1714. DOI: 10.1097/IAE.0000000000003168.
30. Zhuang H, Ding X, Gao F, et al. Optical coherence tomography features of retinal lesions in Chinese patients with endogenous Candida endophthalmitis[J]. BMC Ophthalmol, 2020, 20(1): 52. DOI: 10.1186/s12886-020-01337-9.

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