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, 陳長征, 等. 伴發或首發病毒性結膜炎的新型冠狀病毒感染下眼科醫師的防控策略[J]. 中華實驗眼科雜志, 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.	張黎, 劉宇奇, 袁容娣. 新型冠狀病毒感染相關Purtscher樣視網膜病變臨床特征[J]. 中華眼底病雜志, 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.	熊鳳, 帥娜, 周抒, 等. 新型冠狀病毒感染相關急性黃斑神經視網膜病變的臨床及眼底影像特征[J]. 中華眼底病雜志, 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.	鐘育晟, 程湧, 趙明威, 等. 新型冠狀病毒感染相關急性黃斑神經視網膜病變的臨床特征[J]. 中華眼底病雜志, 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.	劉扶搖, 帥娜, 閆華婧, 等. 新型冠狀病毒感染伴多發性一過性白點綜合征1例[J]. 中華眼底病雜志, 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, 陳長征, 等. 伴發或首發病毒性結膜炎的新型冠狀病毒感染下眼科醫師的防控策略[J]. 中華實驗眼科雜志, 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. 張黎, 劉宇奇, 袁容娣. 新型冠狀病毒感染相關Purtscher樣視網膜病變臨床特征[J]. 中華眼底病雜志, 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. 熊鳳, 帥娜, 周抒, 等. 新型冠狀病毒感染相關急性黃斑神經視網膜病變的臨床及眼底影像特征[J]. 中華眼底病雜志, 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. 鐘育晟, 程湧, 趙明威, 等. 新型冠狀病毒感染相關急性黃斑神經視網膜病變的臨床特征[J]. 中華眼底病雜志, 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. 劉扶搖, 帥娜, 閆華婧, 等. 新型冠狀病毒感染伴多發性一過性白點綜合征1例[J]. 中華眼底病雜志, 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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