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Abrishami M, Daneshvar R, Emamverdian Z, Shoeibi N, Sedighi S, Saeidi Rezvani T, Saeedian N, Eslami S. Optic Nerve Head Optical Coherence Tomography Angiography Findings after Coronavirus Disease. JOVR [Internet]. 2021Oct.25 [cited 2024Apr.16];16(4):592–601. Available from: https://knepublishing.com/index.php/JOVR/article/view/9749
https://doi.org/10.18502/jovr.v16i4.9749
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authors
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Mojtaba Abrishami
Mojtaba Abrishami
Eye Research Center, Mashhad University of Medical Sciences, Mashhad, Iran
-
Ramin Daneshvar
Ramin Daneshvar
Eye Research Center, Mashhad University of Medical Sciences, Mashhad, Iran
-
Zahra Emamverdian
Zahra Emamverdian
Eye Research Center, Mashhad University of Medical Sciences, Mashhad, Iran
-
Nasser Shoeibi
Nasser Shoeibi
Eye Research Center, Mashhad University of Medical Sciences, Mashhad, Iran
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Shima Sedighi
Shima Sedighi
Department of Emergency Medicine, University of Florida College of Medicine, Jacksonville, Jacksonville, FL, USA
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Talieh Saeidi Rezvani
Talieh Saeidi Rezvani
Department of Education and Psychology, Ferdowsi University of Mashhad, Mashhad, Iran
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Neda Saeedian
Neda Saeedian
Department of Internal Medicine, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
-
Saeid Eslami
Saeid Eslami
Department of Medical Informatics, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
Published Date
- Oct 25, 2021
Optic Nerve Head Optical Coherence Tomography Angiography Findings after Coronavirus Disease
Abstract
Purpose: To quantify the microvasculature density of the optic nerve head (ONH) using optical coherence tomography angiography (OCTA) analysis in patients recovered from Coronavirus Disease 2019 (COVID-19).
Methods: In a comparative cross-sectional, observational study, patients recovered from COVID- 19 whose initial diagnosis was confirmed by an rRT-PCR of a nasopharyngeal sample were included in this study. OCTA of ONH was performed in included patients and normal controls. Vascular density (VD) of the all vessels (AV) and small vessels (SV) inside the disc and radial peripapillary capillary (RPC) network density was measured in COVID-19 recovered patients and compared with similar parameters in an age-matched group of normal controls.
Results: Twenty-five COVID-19 patients and twenty-two age-matched normal controls were enrolled in the study and one eye per participant was evaluated. The mean whole image SV VD in the COVID-19 group (49.31 ± 1.93) was not statistically significantly different from that in the control group (49.94 ±. 2.22; P = 0.308). A decrease in RPC VD was found in all AV and SV VD measured, which became statistically significant in whole peripapillary SV VD, peripapillary inferior nasal SV VD, peripapillary inferior temporal SV VD, peripapillary superior nasal SV VD, and grid-based AV VD inferior sector (P < 0.05). Inside disc SV VD in the COVID-19 group (49.43 ± 4.96) was higher than in the control group (45.46 ± 6.22) which was statistically significant (P = 0.021).
Conclusion: Unremarkable decrease was found in ONH microvasculature in patients who had recovered from COVID-19. These patients may be at risk of ONH vascular complications. Increase in inner disc SV VD may be an indicator of ONH hyperemia and edema.
Keywords:
Coronavirus Disease 2019 (COVID-19), Optic Nerve Head, Optical Coherence Tomography Angiography (OCTA), Radial Peripapillary Capillary Network, Severe Acute Respiratory Syndrome Corona Virus 2 (SARS-CoV-2)
References
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19. 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. Ocul Immunol Inflamm 2020;28:391–395.
20. Turker IC, Dogan CU, Guven D, Kutucu OK, Gul C. Optical coherence tomography angiography findings in patients with COVID-19. Can J Ophthalmol 2021;56:83–87.
21. Zapata MÁ, Banderas García S, Sánchez-Moltalvá A, et al. Retinal microvascular abnormalities in patients after COVID-19 depending on disease severity [published online ahead of print, 2020 Dec 16]. Br J Ophthalmol 2020;bjophthalmol-2020-317953.
22. Sim SS, Cheung CMG. Does COVID-19 infection leave a mark on the retinal vasculature? Can J Ophthalmol 2021;56:4–5.
23. Ma ZW, Qiu WH, Zhou DN, Yang WH, Pan XF, Chen H. Changes in vessel density of the patients with narrow antenior chamber after an acute intraocular pressure elevation observed by OCT angiography. BMC Ophthalmol 2019;19:132.
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25. van de Kreeke JA, Nguyen HT, Konijnenberg E, Tomassen J, den Braber A, Kate MT, et al. Optical coherence tomography angiography in preclinical Alzheimer’s disease. Br J Ophthalmol 2020;104:157–161.
26. Pellegrini M, Vagge A, Ferro Desideri LF, Bernabei F, Triolo G, Mastropasqua R, et al. Optical coherence tomography angiography in neurodegenerative disorders. J Clin Med 2020;9:1706.
27. Criscuolo C, Cennamo G, Montorio D, Carotenuto A, Strianese A, Salvatore E, et al. Assessment of retinal vascular network in amnestic mild cognitive impairment by optical coherence tomography angiography. PLoS One 2020;15:e0233975.
28. Abrishami M, Daneshvar R, Emamverdian Z, Tohidinezhad F, Eslami S. Optic nerve head parameters and peripapillary retinal nerve fiber layer thickness in patients with Coronavirus disease 2019. Ocul Immunol Inflamm 2021 Feb:1–4.
29. Burgos-Blasco B, Guemes-Villahoz N, Donate-Lopez J, Vidal-Villegas B, Garcia-Feijoo J. Optic nerve analysis in COVID-19 patients. J Med Virol 2020;93:190–191.
30. Sawalha K, Adeodokun S, Kamoga GR. COVID-19-induced acute bilateral optic neuritis. J Investig Med High Impact Case Rep 2020;8:2324709620976018.
31. Cabrera DeBuc D, Gaca-Wysocka M, Grzybowski A, Kanclerz P. Identification of retinal biomarkers in Alzheimer’s disease using optical coherence tomography: recent insights, challenges, and opportunities. J Clin Med 2019;8:996.
32. Pietroboni AM, Carandini T, Dell’Arti L, Bovis F, Colombi A, De Riz MA, et al. Evidence of retinal anterograde neurodegeneration in the very early stages of multiple sclerosis: a longitudinal OCT study. Neurol Sci 2020;41:3175–3183.
33. Salvi L, Plateroti P, Balducci S, Bollanti L, Conti FG, Vitale M, et al. Abnormalities of retinal ganglion cell complex at optical coherence tomography in patients with type 2 diabetes: a sign of diabetic polyneuropathy, not retinopathy. J Diabetes Complications 2016;30:469–476.
34. Tisdale AK, Dinkin M, Chwalisz BK. Afferent and efferent neuro-ophthalmic complications of Coronavirus disease 19. J Neuroophthalmol 2021;41:154–165.
35. Tohidinezhad F, Khorsand A, Zakavi SR, Rezvani R, Zarei-Ghanavati S, Abrishami M, et al. The burden and predisposing factors of non-communicable diseases in Mashhad University of Medical Sciences personnel: a prospective 15-year organizational cohort study protocol and baseline assessment. BMC Public Health 2020;20:1637.
2. Gheblawi M, Wang K, Viveiros A, Nguyen Q, Zhong J-C, Turner AJ, et al. Angiotensin-converting enzyme 2: SARSCoV- 2 receptor and regulator of the renin-angiotensin system: celebrating the 20th anniversary of the discovery of ACE2. Circ Res 2020;126:1456–1474.
3. Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020;395:497–506.
4. Li JO, Lam DSC, Chen Y, Ting DSW. Novel Coronavirus disease 2019 (COVID-19): the importance of recognising possible early ocular manifestation and using protective eyewear. Br J Ophthalmol 2020;104:297–298.
5. Mungmungpuntipantip R, Wiwanitkit V. Ocular manifestation, eye protection, and COVID-19. Graefes Arch Clin Exp Ophthalmol 2020;258:1339.
6. Wan Y, Shang J, Graham R, Baric RS, Li F. Receptor recognition by the novel Coronavirus from Wuhan: an analysis based on decade-long structural studies of SARS Coronavirus. J Virol 2020;94:e00127–e00120.
7. Hamming I, Timens W, Bulthuis ML, Lely AT, Navis G, van Goor H. Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J Pathol 2004;203:631–637.
8. Chamsi-Pasha MA, Shao Z, Tang WH. Angiotensin-converting enzyme 2 as a therapeutic target for heart failure. Curr Heart Fail Rep 2014;11:58–63.
9. Choudhary R, Kapoor MS, Singh A, Bodakhe SH. Therapeutic targets of renin-angiotensin system in ocular disorders. J Curr Ophthalmol 2017;29:7–16.
10. Zhou Z, Kang H, Li S, Zhao X. Understanding the neurotropic characteristics of SARS-CoV-2: from neurological manifestations of COVID-19 to potential neurotropic mechanisms. J Neurol 2020;267:2179–2184.
11. Abrishami M, Tohidinezhad F, Daneshvar R, Omidtabrizi A, Amini M, Sedaghat A, et al. Ocular manifestations of hospitalized patients with COVID-19 in northeast of Iran. Ocul Immunol Inflamm 2020;28:739–744.
12. Marinho PM, Marcos AAA, Romano AC, Nascimento H, Belfort R Jr. Retinal findings in patients with COVID-19. Lancet 2020;395:1610.
13. Abrishami M, Emamverdian Z, Shoeibi N, Omidtabrizi A, Daneshvar R, Rezvani TS, et al. Optical coherence tomography angiography analysis of the retina in patients recovered from COVID-19: a case-control study. Can J Ophthalmol 2021;56:24–30.
14. Casagrande M, Fitzek A, Puschel K, Aleshcheva G, Schultheiss H-P, Berneking L, et al. Detection of SARSCoV- 2 in human retinal biopsies of deceased COVID-19 patients. Ocul Immunol Inflamm 2020;28:721–725.
15. Savastano A, Crincoli E, Savastano MC, Younis S, Gambini G, De Vico U, et al. Peripapillary retinal vascular involvement in early post-COVID-19 patients. J Clin Med 2020;9:2895.
16. Su XW, Palka SV, Rao RR, Chen FS, Brackney CR, Cambi F. SARS-CoV-2-associated Guillain-Barre syndrome with dysautonomia. Muscle Nerve 2020;62:E48–E49.
17. Fernandez-Dominguez J, Ameijide-Sanluis E, Garcia- Cabo C, Garcia-Rodriguez R, Mateos V. Miller–Fisher-like syndrome related to SARS-CoV-2 infection (COVID 19). J Neurol 2020;267:2495–2496.
18. DosSantos MF, Devalle S, Aran V, Capra D, Roque NR, de Mattos Coelho-Aguiar J, et al. Neuromechanisms of SARSCoV-2: a review. Front Neuroanat 2020;14:37.
19. 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. Ocul Immunol Inflamm 2020;28:391–395.
20. Turker IC, Dogan CU, Guven D, Kutucu OK, Gul C. Optical coherence tomography angiography findings in patients with COVID-19. Can J Ophthalmol 2021;56:83–87.
21. Zapata MÁ, Banderas García S, Sánchez-Moltalvá A, et al. Retinal microvascular abnormalities in patients after COVID-19 depending on disease severity [published online ahead of print, 2020 Dec 16]. Br J Ophthalmol 2020;bjophthalmol-2020-317953.
22. Sim SS, Cheung CMG. Does COVID-19 infection leave a mark on the retinal vasculature? Can J Ophthalmol 2021;56:4–5.
23. Ma ZW, Qiu WH, Zhou DN, Yang WH, Pan XF, Chen H. Changes in vessel density of the patients with narrow antenior chamber after an acute intraocular pressure elevation observed by OCT angiography. BMC Ophthalmol 2019;19:132.
24. Lommatzsch C, Rothaus K, Koch JM, Heinz C, Grisanti S. Vessel density in OCT angiography permits differentiation between normal and glaucomatous optic nerve heads. Int J Ophthalmol 2018;11:835–843.
25. van de Kreeke JA, Nguyen HT, Konijnenberg E, Tomassen J, den Braber A, Kate MT, et al. Optical coherence tomography angiography in preclinical Alzheimer’s disease. Br J Ophthalmol 2020;104:157–161.
26. Pellegrini M, Vagge A, Ferro Desideri LF, Bernabei F, Triolo G, Mastropasqua R, et al. Optical coherence tomography angiography in neurodegenerative disorders. J Clin Med 2020;9:1706.
27. Criscuolo C, Cennamo G, Montorio D, Carotenuto A, Strianese A, Salvatore E, et al. Assessment of retinal vascular network in amnestic mild cognitive impairment by optical coherence tomography angiography. PLoS One 2020;15:e0233975.
28. Abrishami M, Daneshvar R, Emamverdian Z, Tohidinezhad F, Eslami S. Optic nerve head parameters and peripapillary retinal nerve fiber layer thickness in patients with Coronavirus disease 2019. Ocul Immunol Inflamm 2021 Feb:1–4.
29. Burgos-Blasco B, Guemes-Villahoz N, Donate-Lopez J, Vidal-Villegas B, Garcia-Feijoo J. Optic nerve analysis in COVID-19 patients. J Med Virol 2020;93:190–191.
30. Sawalha K, Adeodokun S, Kamoga GR. COVID-19-induced acute bilateral optic neuritis. J Investig Med High Impact Case Rep 2020;8:2324709620976018.
31. Cabrera DeBuc D, Gaca-Wysocka M, Grzybowski A, Kanclerz P. Identification of retinal biomarkers in Alzheimer’s disease using optical coherence tomography: recent insights, challenges, and opportunities. J Clin Med 2019;8:996.
32. Pietroboni AM, Carandini T, Dell’Arti L, Bovis F, Colombi A, De Riz MA, et al. Evidence of retinal anterograde neurodegeneration in the very early stages of multiple sclerosis: a longitudinal OCT study. Neurol Sci 2020;41:3175–3183.
33. Salvi L, Plateroti P, Balducci S, Bollanti L, Conti FG, Vitale M, et al. Abnormalities of retinal ganglion cell complex at optical coherence tomography in patients with type 2 diabetes: a sign of diabetic polyneuropathy, not retinopathy. J Diabetes Complications 2016;30:469–476.
34. Tisdale AK, Dinkin M, Chwalisz BK. Afferent and efferent neuro-ophthalmic complications of Coronavirus disease 19. J Neuroophthalmol 2021;41:154–165.
35. Tohidinezhad F, Khorsand A, Zakavi SR, Rezvani R, Zarei-Ghanavati S, Abrishami M, et al. The burden and predisposing factors of non-communicable diseases in Mashhad University of Medical Sciences personnel: a prospective 15-year organizational cohort study protocol and baseline assessment. BMC Public Health 2020;20:1637.