Multimodal imaging characteristics of retinal diseases associated with COVID-19_Chinese Journal of Ocular Fundus Diseases

Authors：

 Yang Kaizhuan , Yan Shu , Shao Ling , Li Yan , Liu Yu , Du Min , Chen Mengping

Department of Ophthalmology, The Second People's Hospital of Zhengzhou, Zhengzhou 450000, China;

Corresponding author：

Yang Kaizhuan, Email: yangkaizhuan@163.com

Keywords：

COVID-19; Acute macular neuroretinopathy; Purtscher-like retinopathy; Multimodal imaging

DOI：

10.3760/cma.j.cn511434-20221230-00676

Video：

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Objective To observe the multimodal imaging features of retinal diseases associated with COVID-19. Methods A retrospective case study. Sixteen patients (30 eyes) of retinal diseases associated with COVID-19 admitted to the Ophthalmology Department of the Second People's Hospital of Zhengzhou in December 2022 were included in the study. There were 5 males and 11 females, with the mean age of (26.69±9.88) years; 14 patients were bilateral and 2 patients were unilateral. The time of ocular symptoms after the diagnosis of COVID-19 was (2.63±0.89) days. All patients underwent the examinations of best corrtected visual acuity (BCVA), fundus color photography (FP), infrared fundus photography (IR), optical coherence tomography (OCT). Fluorescein fundus angiography (FFA) was performed in 2 patients (4 eyes). There were 20 eyes with acute macular neuroretinopathy (AMN), including 6 eyes with cotton wool spots; 10 eyes with Purtscher-like retinopathy (PLR). The BCVA of the patients was 0.1-1.0. No obvious abnormality was found in anterior segment examination. The features of FP, IR and OCT were analyzed retrospectively. Results In 20 eyes of AMN, irregular reddish brown lesions in the central or paracentral area of the macula in 14 eyes; FP showed no obvious abnormality in 6 eyes; IR showed irregular map like low reflection in the central or paracentral area of macular in all eyes; OCT showed hyperreflectivity in outer plexiform layer and outer nuclear layer, hyporeflectivity in the ellipsoid zone and photoreceptor layers in all eyes; no abnormal fluorecence was observed in 2 eyes examined by FFA. In 10 eyes with PLR, cotton wool spots and retinal hemorrhage were observed in the posterior pole and/or peripapillary area, and the peripheral retina was generally normal, Purtscher spot was found in 5 eyes and macular edema in 4 eyes; OCT showed strong reflex signal in neuroepithelial layers, edema in neuroepithelial layers in 6 eyes; in the 2 eyes examined by FFA, fluorescein leakage from the retinal vein wall was observed, the posterior pole and peripapillary area retinal arteriole occlusions showed patchy hypofluorescence, the fluorescence was obscured by retinal hemorrhage below at inferior retina. Conclusions For AMN associated with COVID-19, IR can show the lesion contour , OCT shows lesions in the outer retina. PLR associated with COVID-19 are usually at the posterior pole and/or peripapillary area in FP, OCT shows neurocortical edema.

Citation： Yang Kaizhuan, Yan Shu, Shao Ling, Li Yan, Liu Yu, Du Min, Chen Mengping. Multimodal imaging characteristics of retinal diseases associated with COVID-19. Chinese Journal of Ocular Fundus Diseases, 2023, 39(3): 194-198. doi: 10.3760/cma.j.cn511434-20221230-00676 Copy

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5.	蓝倩倩, 曾思明, 廖欣, 等. 新型冠状病毒肺炎患者中新型冠状病毒相关性结膜炎的筛查[J]. 中华眼科杂志, 2020, 56(6): 433-437. DOI: 10.3760/cma.j.cn112142-20200322-00213.Lan QQ, Zeng SM, Yan X, et al. Screening for novel coronavirus related conjunctivitis among the patients with coronavirus disease 2019[J]. Chin J Ophthalmol, 2020, 56(6): 433-437. DOI: 10.3760/cma.j.cn112142-20200322-00213.
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7.	Jalink MB, Bronkhorst IHG. A sudden rise of patients with acute macular neuroretinopathy during the COVID-19 pandemic[J]. Case Rep Ophthalmol, 2022, 13(1): 96-103. DOI: 10.1159/000522080.
8.	Bottini AR, Steinmetz S, Blinder KJ, et al. Purtscher-like retinopathy in a patient with COVID-19[J/OL]. Case Rep Ophthalmol Med, 2021, 2021: 6661541[2021-03-20]. https://europepmc.org/article/MED/33859855. DOI:10.1155/2021/6661541.
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10.	姜利斌, 魏文斌, 王光璐. 急性黄斑区神经视网膜病变[J]. 中国实用眼科杂志, 2006, 24(3): 240-243. DOI: 10.3760/cma.j.issn.1006-4443.2006.03.003.Jiang LB, Wei WB, Wang GL. Acute macular neuroretinopathy[J]. Chin J Pract Ophthalmol, 2006, 24(3): 240-243. DOI: 10.3760/cma.j.issn.1006-4443.2006.03.003.
11.	戴荣平, 董方田, 郑霖, 等. Purtscher样视网膜病变[J]. 中华眼科杂志, 2007, 43(5): 447-450. DOI: 10.3760/j.issn:0412-4081.2007.05.014.Dai RP, Dong FT, Zheng L, et al. Purtscher-like retinopathy[J]. Chin J Ophthalmol, 2007, 43(5): 447-450. DOI: 10.3760/j.issn:0412-4081.2007.05.014.
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13.	滕岩, 滕羽菲. 急性黄斑区神经视网膜病变的临床特征及病理机制研究进展[J]. 中华眼科杂志, 2019, 55(4): 311-315. DOI: 10.3760/cma.j.issn.0412-4081.2019.04.016.Tang Y, Teng YF. The clinical characteristics and pathologic mechanisms of acute macular neuroretinopathy[J]. Chin J Ophthalmol, 2019, 55(4): 311-315. DOI: 10.3760/cma.j.issn.0412-4081.2019.04.016.
14.	Pang CE, Navajas EV, Warner SJ, et al. Acute macular neuroretinopathy associated with chikungunya fever[J]. Ophthalmic Surg Lasers Imaging Retina, 2016, 47(6): 596-599. DOI: 10.3928/23258160-20160601-15.
15.	Bhavsar KV, Lin S, Rahimy E, et al. Acute macular neuroretinopathy: a comprehensive review of the literature[J]. Surv Ophthalmol, 2016, 61(5): 538-565. DOI: 10.1016/j.survophthal.2016.03.003.
16.	Amer R, Lois N. Punctate inner choroidopathy[J]. Surv Ophthalmol, 2011, 56(1): 36-53. DOI: 10.1016/j.survophthal.2010.03.009.
17.	Corver HD, Ruys J, Kestelyn-Stevens AM, et al. Two cases of acute macular neuroretinopathy[J]. Eye (Lond), 2007, 21(9): 1226-1229. DOI: 10.1038/sj.eye.6702543.
18.	Riotto E, Mégevand V, Mégevand A, et al. A COVID-19-related retinopathy case report[J]. Case Rep Ophthalmol, 2022, 13(1): 297-304. DOI: 10.1159/000524195.
19.	D'Souza HS, Tailor PD, Olsen TW. Seeing blue dots after COVID-19 infection[J]. JAMA Ophthamol, 2023, 141(1): 97-98. DOI: 10.1001/jamaophthalmol.2022.5235.
20.	Shroff D, Kumar S, Naidu A, et al. Unilateral purtscher-like retinopathy post-COVID-19[J]. Indian J Ophthalmol, 2022, 70(10): 3710-3712. DOI: 10.4103/ijo.IJO_1486_22.
21.	Kuriakose RK, Chin EK, Almeida DRP. An atypical presentation of acute macular neuroretinopathy after non-ocular trauma[J]. Case Rep Ophthalmol, 2019, 10(1): 1-4. DOI: 10.1159/000496144.
22.	Mbekeani JN, Raval NK, Vo TA, et al. Purtscher-like retinopathy in a patient with COVID-19-associated coagulopathy[J]. Arq Bras Oftalmol, 2022, 85(5): 513-516. DOI: 10.5935/0004-2749.2020-0328.
23.	Seah I, Agrawal R. Can the coronavirus disease 2019 (COVID-19) affect the eyes? A review of coronaviruses and ocular implications in humans and animals[J]. Ocul Immunol Inflamm, 2020, 28(3): 391-395. DOI: 10.1080/09273948.2020.1738501.
24.	Zhang H, Penninger JM, Li Y, et al. Angiotensin-converting enzyme 2 (ACE2) as a SARS-CoV-2 receptor: molecular mechanisms and potential therapeutic target[J]. Intensive Care Med, 2020, 46(4): 586-590. DOI: 10.1007/s00134-020-05985-9.
25.	Tang N, Li D, Wang X, et al. Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia[J]. J Thromb Haemost, 2020, 18(4): 844-847. DOI: 10.1111/jth.14768.
26.	Landecho MF, Yuste JR, Gándara E, et al. COVID-19 retinal microangiopathy as an in vivo biomarker of systemic vascular disease?[J]. J Intern Med, 2021, 289(1): 116-120. DOI: 10.1111/joim.13156.

1. Jin Y, Yang H, Ji W, et al. Virology, epidemiology, pathogenesis, and control of COVID-19[J]. Viruses, 2020, 12(4): 372. DOI: 10.3390/v1240372.
2. Guan WJ, Ni ZY, Hu Y, et al. Clinical characteristics of coronavirus disease 2019 in China[J]. N Engl J Med, 2020, 382(18): 1708-1720. DOI: 10.1056/NEJMoa2002032.
3. 季樱红, 孙杨, 卢奕. 新型冠状病毒的眼睛侵入途径与眼科防护重点[J]. 中国眼耳鼻喉科杂志, 2020, 20(3): 156-161. DOI: 10.14166/j.issn.1671-2420.2020.03.003.Ji YH, Sun Y, Lu Y. Eye invasion route of 2019 novel corona virus and the emphasis of ophthalmic protection[J]. Chin J Ophthalmol and Otorhinolaryngol, 2020, 20(3): 156-161. DOI: 10.14166/j.issn.1671-2420.2020.03.003.
4. Lu CW, Liu XF, Jia ZF. 2019-nCoV transmission through the ocular surface must not be ignored[J/OL]. Lancet, 2020, 395(10224): e39[2020-02-06]. https://linkinghub.elsevier.com/retrieve/pii/S0140-6736(20)30313-5. DOI: 10.1016/S0140-6736(20)30313-5.
5. 蓝倩倩, 曾思明, 廖欣, 等. 新型冠状病毒肺炎患者中新型冠状病毒相关性结膜炎的筛查[J]. 中华眼科杂志, 2020, 56(6): 433-437. DOI: 10.3760/cma.j.cn112142-20200322-00213.Lan QQ, Zeng SM, Yan X, et al. Screening for novel coronavirus related conjunctivitis among the patients with coronavirus disease 2019[J]. Chin J Ophthalmol, 2020, 56(6): 433-437. DOI: 10.3760/cma.j.cn112142-20200322-00213.
6. Gaba WH, Ahmed D, Al Nuaimi RK, et al. Bilateral central retinal vein occlusion in a 40-year- old man with severe coronavirus disease 2019 (COVID-19) pneumonia[J/OL]. Am J Case Rep, 2020, 21: e927691[2020-10-29]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7603800/. DOI:10.12659/AJCR.927691.
7. Jalink MB, Bronkhorst IHG. A sudden rise of patients with acute macular neuroretinopathy during the COVID-19 pandemic[J]. Case Rep Ophthalmol, 2022, 13(1): 96-103. DOI: 10.1159/000522080.
8. Bottini AR, Steinmetz S, Blinder KJ, et al. Purtscher-like retinopathy in a patient with COVID-19[J/OL]. Case Rep Ophthalmol Med, 2021, 2021: 6661541[2021-03-20]. https://europepmc.org/article/MED/33859855. DOI:10.1155/2021/6661541.
9. 中华人民共和国国家卫生健康委员会. 新型冠状病毒感染诊疗方案(试行第十版)[J]. 中华临床感染病杂志, 2023, 16(1): 1-9. DOI: 10.3760/cma.j.issn.1674-2397.2023.01.001.National Health Commission of the People’s Republic of China. Diagnosis and treatment plan for COVID-19 (trial version 10) [J]. Chin J Clin Infect Dis, 2023, 16(1) : 1-9. DOI: 10.3760/cma.j.issn.1674-2397.2023.01.001.
10. 姜利斌, 魏文斌, 王光璐. 急性黄斑区神经视网膜病变[J]. 中国实用眼科杂志, 2006, 24(3): 240-243. DOI: 10.3760/cma.j.issn.1006-4443.2006.03.003.Jiang LB, Wei WB, Wang GL. Acute macular neuroretinopathy[J]. Chin J Pract Ophthalmol, 2006, 24(3): 240-243. DOI: 10.3760/cma.j.issn.1006-4443.2006.03.003.
11. 戴荣平, 董方田, 郑霖, 等. Purtscher样视网膜病变[J]. 中华眼科杂志, 2007, 43(5): 447-450. DOI: 10.3760/j.issn:0412-4081.2007.05.014.Dai RP, Dong FT, Zheng L, et al. Purtscher-like retinopathy[J]. Chin J Ophthalmol, 2007, 43(5): 447-450. DOI: 10.3760/j.issn:0412-4081.2007.05.014.
12. Ozturker ZK. Conjunctivitis as sole symptom of COVID-19: a case report and review of literature[J]. Eur J Ophthalmol, 2021, 31(2): NP161-NP166. DOI: 10.1177/1120672120946287.
13. 滕岩, 滕羽菲. 急性黄斑区神经视网膜病变的临床特征及病理机制研究进展[J]. 中华眼科杂志, 2019, 55(4): 311-315. DOI: 10.3760/cma.j.issn.0412-4081.2019.04.016.Tang Y, Teng YF. The clinical characteristics and pathologic mechanisms of acute macular neuroretinopathy[J]. Chin J Ophthalmol, 2019, 55(4): 311-315. DOI: 10.3760/cma.j.issn.0412-4081.2019.04.016.
14. Pang CE, Navajas EV, Warner SJ, et al. Acute macular neuroretinopathy associated with chikungunya fever[J]. Ophthalmic Surg Lasers Imaging Retina, 2016, 47(6): 596-599. DOI: 10.3928/23258160-20160601-15.
15. Bhavsar KV, Lin S, Rahimy E, et al. Acute macular neuroretinopathy: a comprehensive review of the literature[J]. Surv Ophthalmol, 2016, 61(5): 538-565. DOI: 10.1016/j.survophthal.2016.03.003.
16. Amer R, Lois N. Punctate inner choroidopathy[J]. Surv Ophthalmol, 2011, 56(1): 36-53. DOI: 10.1016/j.survophthal.2010.03.009.
17. Corver HD, Ruys J, Kestelyn-Stevens AM, et al. Two cases of acute macular neuroretinopathy[J]. Eye (Lond), 2007, 21(9): 1226-1229. DOI: 10.1038/sj.eye.6702543.
18. Riotto E, Mégevand V, Mégevand A, et al. A COVID-19-related retinopathy case report[J]. Case Rep Ophthalmol, 2022, 13(1): 297-304. DOI: 10.1159/000524195.
19. D'Souza HS, Tailor PD, Olsen TW. Seeing blue dots after COVID-19 infection[J]. JAMA Ophthamol, 2023, 141(1): 97-98. DOI: 10.1001/jamaophthalmol.2022.5235.
20. Shroff D, Kumar S, Naidu A, et al. Unilateral purtscher-like retinopathy post-COVID-19[J]. Indian J Ophthalmol, 2022, 70(10): 3710-3712. DOI: 10.4103/ijo.IJO_1486_22.
21. Kuriakose RK, Chin EK, Almeida DRP. An atypical presentation of acute macular neuroretinopathy after non-ocular trauma[J]. Case Rep Ophthalmol, 2019, 10(1): 1-4. DOI: 10.1159/000496144.
22. Mbekeani JN, Raval NK, Vo TA, et al. Purtscher-like retinopathy in a patient with COVID-19-associated coagulopathy[J]. Arq Bras Oftalmol, 2022, 85(5): 513-516. DOI: 10.5935/0004-2749.2020-0328.
23. Seah I, Agrawal R. Can the coronavirus disease 2019 (COVID-19) affect the eyes? A review of coronaviruses and ocular implications in humans and animals[J]. Ocul Immunol Inflamm, 2020, 28(3): 391-395. DOI: 10.1080/09273948.2020.1738501.
24. Zhang H, Penninger JM, Li Y, et al. Angiotensin-converting enzyme 2 (ACE2) as a SARS-CoV-2 receptor: molecular mechanisms and potential therapeutic target[J]. Intensive Care Med, 2020, 46(4): 586-590. DOI: 10.1007/s00134-020-05985-9.
25. Tang N, Li D, Wang X, et al. Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia[J]. J Thromb Haemost, 2020, 18(4): 844-847. DOI: 10.1111/jth.14768.
26. Landecho MF, Yuste JR, Gándara E, et al. COVID-19 retinal microangiopathy as an in vivo biomarker of systemic vascular disease?[J]. J Intern Med, 2021, 289(1): 116-120. DOI: 10.1111/joim.13156.

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Multimodal imaging characteristics of retinal diseases associated with COVID-19

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