The impact of the new coronavirus infection COVID-19 on the microcirculation of the eye
https://doi.org/10.21516/2072-0076-2023-16-2-177-182
Abstract
The challenge of the coronavirus pandemic, and the research into the mechanism of development of the symptom complex that appears in patients who had COVID-19 (post-COVID syndrome), is a topical issue of modern medicine. Obviously, as the incidence of COVID increases, the number of patients suffering from the post-COVID syndrome increases, too. According to recent estimates, 10 to 20 % of patients who have experienced an acute symptomatic phase of SARS-CoV-2 suffer from the effects of the disease over 12 weeks from the primary diagnosis. COVID-19 has been shown to have a variety of long-term effects on virtually all body systems, including the eye. The ocular surface can serve as a gateway for the virus to enter the body, so that patients experience nonspecific changes in the conjunctiva, cornea, retina, and eye vessels. Thus, the issues of diagnosis and treatment of the COVID-19 infection itself and, notably, its complications and conditions that have arisen and continue after the disease, are of essential research and clinical interest. SARS-CoV-2 has a negative impact on the state of the vascular wall and contributes to the development of hypercoagulable conditions, which increases the risk of thrombosis and possible complications in the cardiovascular system. The review summarizes the analyses of eye vessels blood flow in patients who have undergone COVID-19.
About the Authors
O. I. Markelova
Helmholtz National Medical Research Center of Eye Diseases
Russian Federation
Russian Federation
Oksana I. Markelova, PhD student, department of glaucoma,
14/19, Sadovaya-Chernogryazskaya St., Moscow, 105062
S. Yu. Petrov
Helmholtz National Medical Research Center of Eye Diseases
Russian Federation
Russian Federation
Sergey Yu. Petrov, Dr. of Med. Sci., head, department of glaucoma,
14/19, Sadovaya-Chernogryazskaya St., Moscow, 105062
T. D. Okhotsimskaya
Helmholtz National Medical Research Center of Eye Diseases
Russian Federation
Russian Federation
Tatiana D. Okhotsimskaya, Cand. of Med. Sci., ophthalmologist, department or retina and optic nerve pathology,
14/19, Sadovaya-Chernogryazskaya St., Moscow, 105062
References
1. Wang C, Horby PW, Hayden FG, et al. A novel coronavirus outbreak of global health concern. Lancet. 2020; 395 (10223): 470–3. doi: 10.1016/S0140-6736(20)30185-9
2. WHO Coronavirus (COVID-19) Dashboard. Available at: https://covid19.who.int/ (accessed: 30.10.2021).
3. Bulanov A.Yu., Roitman E.V. New coronavirus infection, hemostasis system and heparin dosing problems: it is important to say this now. Thrombosis, hemostasis and rheology. 2020; 2: 11–8 (In Russ.). doi: 10.2555/THR.2020.2.0913
4. Guo YR, Cao QD, Hong ZS, et al. The origin, transmission and clinical therapies on coronavirus disease 2019 (COVID-19) outbreak — an update on the status. Mil. Med. Res. 2020; 7(1): 1. doi: 10.1186/s40779-020-00240-0
5. Ge XY, Li JL, Yang XL, et al. Isolation and characterization of a Bat SARS-like Coronavirus that uses the ACE2 receptor. Version 2. Naturе. 2013; 503 (7477): 535–8. doi: 10.1038/nature12711
6. Lee PI, Hsueh PR. Emerging threats from zoonotic coronaviruses-from SARS and MERS to 2019-nCoV. J. Microbiol. Immunol. Infect. 2020; 53 (3): 365–7. doi: 10.1016/j.jmii.2020.02.001
7. Korelina V.E., Gazizova I.R., Kuroyedov A.V., et al. Glaucoma progression during the COVID-19 pandemics. Clinical ophthalmology. 2021; 21 (3): 147–52 (In Russ.). doi: 10.32364/2311-7729-2021-21-3-147-152
8. Neroev V.V., Krichevskaya G.I., Balatskaya N.V. COVID-19 and problems of ophthalmology. Russian ophthalmological journal. 2020; 13 (4): 99–104 (In Russ.). doi: 10.21516/2072-0076-2020-13-4-99-104
9. Neroev V.V., Kiseleva T.N., Eliseeva E.K. Ophthalmological aspects of coronavirus infections. Russian ophthalmological journal. 2021; 14 (1): 7–14 (In Russ.). doi: 10.21516/2072-0076-2021-14-1-7-14
10. Kurysheva N.I. COVID-19 and lesions of the organ of vision. Moscow: Largo; 2021 (In Russ.).
11. Tu H, Tu S, Gao S, et al. Current epidemiological and clinical features of COVID-19; a global perspective from China. J Infect. 2020; 81 (1): 1–9. doi: 10.1016/j.jinf.2020.04.011
12. Hamming I, Timens W, Bulthuis ML, et al. Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J Pathol. 2004; 203 (2): 631–7. doi: 10.1002/path.1570
13. Senanayake P, Drazba J, Shadrach K, et al. Angiotensin II and its receptor subtypes in the human retina. Invest Ophthalmol Vis Sci. 2007; 48 (7): 3301–11. doi: 10.1167/iovs.06-1024
14. Sen M, Honavar SG, Sharma N, et al. COVID-19 and Eye: A review of ophthalmic manifestations of COVID-19. Indian J Ophthalmol. 2021; 69 (3): 488–509. doi: 10.4103/ijo.IJO_297_21
15. Prevention, diagnosis and treatment of new coronavirus infection (COVID-19). The provisional guidelines. Version 7; 03.06.2020 (in Russ.).
16. Sarzi-Puttini P, Giorgi V, Sirotti S, et al. COVID-19, cytokines and immunosuppression: what can we learn from severe acute respiratory syndrome. Clin Exp Rheumatol. 2020; 38 (2): 337–42. doi: 10.55563/clinexprheumatol/xcdary
17. Xu Z, Shi L, Wang Y, et al. Pathological findings of COVID-19 associated with acute respiratory distress syndrome. Lancet Respir Med. 2020; 8 (4): 420–2. doi: 10.1016/S2213-2600(20)30076-X
18. Wu Y, Wu X, Chen Z, et al. Nervous system involvement after infection with COVID-19 and other viruses. Brain Behav Immun. 2020; 87: 1822. doi: 10.1016/j.bbi.2020.03.031
19. Rodriguez-Morales AJ, Cardona-Ospina JA, Gutuerrez-Ocampo E, et al. Clinical, laboratory and imaging features of COVID-19: a systemic review and meta-analysis. Travel Med Infect Dis. 2020: 101623. doi: 10.1016/jrtmaid.2020.101623
20. Siordia JA. Epidemiology and clinical features of COVID-19: A review of current literature. J Clin Virol. 2020; 127: 104357. doi: 10.1016/j.jcv.2020.104357
21. Kayaaslan B, Eser F, Kalem AK, et al. Post-COVID syndrome: A single-center questionnaire study on 1007 participants recovered from COVID-19. J Med Virol. 2021; 93 (12): 6566–74.
22. SEMG Encuesta COVID-19 Persistente. Presentación de Resultados. 11 de Noviembre de 2020. (accessed on 30 December 2020); Available at: https: //www.semg.es/images/2020/Noticias/20201111_Resultados_Encuesta_COVID_Persistente.pdf
23. Davis HE, Assaf GS, McCorkell L, et al. Characterizing long COVID in an international cohort: 7 months of symptoms and their impact. EClinicalMedicine. 2021; 38: 101019. doi: 10.1101/2020.12.24.20248802
24. Jimeno-Almazán A, Pallarés JG, Buendía-Romero Á, et al. Post-COVID-19 syndrome and the potential benefits of exercise. Int J Environ Res Public Health. 2021; 18 (10): 5329. doi: 10.3390/ijerph18105329
25. Sivan M, Taylor S. NICE guideline on long COVID. BMJ. 2020; 371: m4938. doi: org/10.1136/bmj.m4938
26. Carfì A, Bernabei R, Landi F, et al. Persistent symptoms in patients after acute COVID-19. JAMA. 2020; 324 (6): 603–5. doi:org/10.1001/jama.2020.12603
27. Kamal M, Abo Omirah M, Hussein A, et al. Assessment and characterisation of post-COVID-19 manifestations. Int J Clin Pract. 2020; 75: e13746. doi:org/10.1111/ijcp.13746
28. Belyakov N.A., Trofimova T.N., Rassokhin V.V., et al. Postcovid syndrome — polymorphism of disorders in a new coronavirus infection. HIV Infection and Immunosuppressive Disorders. 2021; 13 (4): 7–20 (in Russ.). doi:org/10.22328/2077-9828-2021-13-4-7-20
29. World Health Organization. A clinical case definition of post COVID-19 condition by a Delphi consensus, 6 October 2021. Available at: https: //www.who.int/publications/i/item/WHO-2019-nCoV-Post_COVID-19_condition Clinical_case_definition-2021.1
30. NICE guideline [NG188]. COVID-19 rapid guideline: managing the long-term effects of COVID-19 [cited 2020 Dec 18]. Available at: https://www.nice.org.uk/guidance/ng188
31. UK Office for National Statistics. Prevalence of Ongoing Symptoms Following Coronavirus (COVID-19) Infection in the UK. 2021. ONS; London, UK: 2021. Available at: https://www.ons.gov.uk/peoplepopulationandcommunity/healthandsocialcare/conditionsanddiseases/bulletins/prevalenceofongoingsym ptomsfollowingcoronaviruscovid19infectionintheuk/7july2022.
32. Fernández-de-Las-Peñas C, Palacios-Ceña D, Gómez-Mayordomo V, et al. Defining post-COVID symptoms (post-acute COVID, long COVID, persistent post-COVID): an integrative classification. Int J Environ Res Public Health. 2021; 18 (5): 2621. doi: 10.3390/ijerph18052621
33. Greenhalgh T, Knight M, A'Court C, et al. Management of post-acute COVID-19 in primary care. BMJ. 2020; 370: m3026. doi: 10.1136/bmj.m3026
34. Datta SD, Talwar A, Lee JT. A proposed framework and timeline of the spectrum of disease due to SARS-CoV-2 infection: illness beyond acute infection and public health implications. JAMA. 2020; 324 (22): 2251–2. doi: 10.1001/jama.2020.22717
35. Coroneo MT. The eye as the discrete but defensible portal of coronavirus infection. Ocul Surf. 2020; S1542-0124(20)30089-6. doi: 10.1016/j.jtos.2020.05.011
36. Loon SC, Teoh SC, Oon LL, et al. The severe acute respiratory syndrome coronavirus in tears. BJO. 2004; 88 (7): 861–3. doi:10.1136/bjo.2003.035931
37. Van der Hoek L, Pyrc K, Jebbink MF, et al. Identification of a new human coronavirus. Nat Med. 2004; 10: 368–73.
38. Chin MS, Hooper LC, Hooks JJ, et al. Identification of α-fodrin as an autoantigen in experimental coronavirus retinopathy (ECOR). J Neuroimmunol. 2014; 272: 42–50.
39. Shindler KS, Kenyon LC, Dutt M, et al. Experimental optic neuritis induced by a demyelinating strain of mouse hepatitis virus. J Virol. 2008; 82 (17): 8882–6.
40. Detrick B, Lee MT, Chin MS, et al. Experimental coronavirus retinopathy (ECOR): retinal degeneration susceptible mice have an augmented interferon and chemokine (CXCL9, CXCL10) response early after virus infection. J Neuroimmunol. 2008; 193: 28–37.
41. Vinores SA, Wang Y, Vinores MA, et al. Blood-retinal barrier breakdown in experimental coronavirus retinopathy: association with viral antigen, inflammation, and VEGF in sensitive and resistant strains. J Neuroimmunol. 2001; 119: 175–82.
42. Hooks JJ, Percopo C, Wang Y, et al. Retina and retinal pigment epithelial cell autoantibodies are produced during murine coronavirus retinopathy. J Immunol. 1993; 151: 3381–9.
43. Aydemir E, Aydemir GA, Atesoglu HI, et al. The impact of coronavirus disease 2019 (COVID-19) on retinal microcirculation in human subjects. Klin Monbl Augenheilkd. 2021; 238 (12): 1305–11. doi: 10.1055/a-1579-0805
44. Li YP, Ma Y, Wang N, et al. Eyes on coronavirus. Stem Cell Res. 2021; 51: 102200. doi: 10.1016/j.scr.2021.102200
45. Becker RC. COVID-19 update: COVID-19-associated coagulopathy. J Thromb Thrombolysis. 2020; 50 (1): 54–67. doi: 10.1007/s11239-020-02134-3
46. Artifoni M, Danic G, Gautier G, et al. Systematic assessment of venous thromboembolism in COVID-19 patients receiving thromboprophylaxis: incidence and role of D-dimer as predictive factors. J Thrombosis Thrombolysis. 2020; (50): 211–6. doi: 10.1007/s11239-020-02146-z
47. Tufek M, Capraz M, Kaya AT, et al. Retrobulbar ocular blood flow and choroidal vascular changes in patients recovering from COVID-19 infection. Photodiagnosis Photodyn Ther. 2022; 39: 102976. doi: 10.1016/j.pdpdt.2022.102976
48. Kurysheva N.I., Evdokimova O.A., Nikitina A.D. Eye damage in COVID-19. Part 2: posterior segment complications, neuro-ophthalmic manifestations, vaccination and risk factors. Russian ophthalmological journal. 2023; 16 (1): 157–67 (In Russ.). https://doi.org/10.21516/2072-0076-2023-16-1-157-167
49. Marinho PM, Marcos AA, Romano AC, et al. Retinal findings in patients with COVID-19. Lancet. 2020; 395 (10237): 1610.
50. Invernizzi A, Torre A, Parrulli S, et al. Retinal findings in patients with COVID-19: Results from the SERPICO-19 study. EClinical Medicine. 2020; (20): 100550. doi: 10.1016/j.eclinm.2020.100550
51. Montesel A, Bucolo C, Mouvet V, et al. Case Report: central retinal artery occlusion in a COVID-19 patient. Front Pharmacol. 2020; 11: 588384. doi: 10.3389/fphar.2020.588384
52. Turedi N, Onal Gunay B. Paracentral acute middle maculopathy in the setting of central retinal artery occlusion following COVID-19 diagnosis. Eur J Ophthalmol. 2022; 32 (3): NP62-NP66. doi: 10.1177/1120672121995347
53. Yusef Yu.N., Andzhelova D.V., Kazaryan E.E., et al. Changes in ocular hemodynamics in patients recovered from COVID-19. Vestnik oftal’mologii. 2022; 138 (3): 41–5 (In Russ.). doi: org/10.17116/oftalma202213803141
54. Cennamo G, Reibaldi M, Montorio D, et al. Optical coherence tomography angiography features in post-COVID-19 pneumonia patients: A Pilot Study. Am J Ophthalmol. 2021; (227): 182–90. doi: 10.1016/j.ajo.2021.03.015
55. González-Zamora J, Bilbao-Malavé V, Gándara E, et al. Retinal microvascular impairment in COVID-19 bilateral pneumonia assessed by optical coherence tomography angiography. Biomedicines. 2021; 9 (3): 247. doi: 10.3390/biomedicines9030247
56. Turgel V.А., Tultseva S.N. Study of the retina and optic nerve microvascular bed using optical coherence tomography-angiography in post-COVID-19 patients. Regional blood circulation and microcirculation. 2021; 20 (4): 21–32 (In Russ.). doi: 10.24884/1682-6655-2021-20-4-21-32
57. Savastano A, Crincoli E, Savastano MC, et al. Peripapillary retinal vascular involvement in early postCOVID-19 patients. J Clin Med. 2020; 9: 2895. doi:10.3390/jcm9092895
58. Oren B, Aksoy Aydemır G, Aydemır E, et al. Quantitative assessment of retinal changes inCOVID-19 patients. Clin Exp Optom. 2021 Aug; 104 (6): 717–22. doi: 10.1080/08164622.2021.1916389
59. Abrishami M, Emamverdian Z, Shoeibi N, 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 (1): 24–30. doi: 10.1016/j.jcjo.2020.11.006
60. Zapata MÁ, Banderas García S, Sánchez-Moltalvá A, et al. Retinal microvascular abnormalities in patients after COVID-19 depending on disease severity. BJO. 2020. doi: 10.1136/bjophthalmol-2020-317953
Review
For citations:
Markelova O.I., Petrov S.Yu., Okhotsimskaya T.D. The impact of the new coronavirus infection COVID-19 on the microcirculation of the eye. Russian Ophthalmological Journal. 2023;16(2):177-182. (In Russ.) https://doi.org/10.21516/2072-0076-2023-16-2-177-182
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