Retinal Changes in Patients With Covid-19 and Different Expressiveness of Metabolic Changes

English version

Autoři: Kateryna Hutsaliuk ^1,2; Nataliia Skalska ³; Nadiia Ulianova ^2,4
Působiště autorů: The Regional Ophthalmology Center, ME "Volyn Regional Clinical Hospital" of the Volyn Regional Council, Lutsk, Ukraine ¹; The Filatov Institute of Eye Diseases and Tissue Therapy of the National Academy of Medical Sciences of Ukraine, Odesa, Ukraine ²; Infectious Department, ME "Volyn Regional Clinical Hospital" of the Volyn Regional Council, Lutsk, Ukraine ³; Department of Post-traumatic eye pathology, SI "The Filatov Institute of Eye Diseases and Tissue Therapy of the National Academy of Medical Sciences of Ukraine", Odesa, Ukraine ⁴
Vyšlo v časopise: Čes. a slov. Oftal., 80, 2024, No. Ahead of print, p. 1001-1010
Kategorie: Originální práce
doi: https://doi.org/10.31348/2024/12

Souhrn

Aims: To study the relationship between the severity of COVID-induced metabolic changes and the structure and frequency of retinal changes, according to funduscopy data in patients with different clinical courses of COVID-19.

Materials and methods: 117 patients with COVID-19 were examined. While examining patients, severity of the course of COVID-19, the expressiveness of changes in the metabolic status were determined; fundus image registration was performed with portable fundus cameras Pictor Plus Fundus Camera and VistaView (Volk Optical).

Results: As a result of the research, retinal changes were found in 49 (41.9 %) patients with COVID-19. In 8 (16.3 %) cases, clinically significant (vitreous hemorrhage, prethrombosis of the central retinal vein or branches of the central retinal vein, thrombosis of the central retinal vein or branches of the central retinal vein) COVID-induced retinal and ophthalmological changes were observed, which caused a decrease in visual acuity. In 41 (83.7 %) cases, clinically insignificant changes (cotton wool spots, narrowed retinal vessels, intraretinal and petechial hemorrhages, tortuosity and dilatation of retinal venules) COVID-induced retinal changes were observed. Clinically significant retinal changes occur in patients with a statistically significantly higher level of D-dimer and a greater percentage of lung parenchyma lesion than in the group of patients with clinically insignificant retinal changes (p < 0.05).

Conclusions: The structure of retinal changes in patients with COVID-19 correlates with the severity of the clinical course of the disease and changes in the metabolic status of patients. Metabolic changes are correlated with retinal changes and can be predictive for preventing general vascular complications in COVID-19.

Zdroje

Invernizzi A, Schiuma M, Parrulli S et al. Retinal vessels modifications in acute and post-COVID-19. Sci Rep. 2021 Sep 29;11(1):19373. doi: 10.1038/s41598-021-98873-1
Szczęśniak M, Brydak-Godowska J. SARS-CoV-2 and the Eyes: A Review of the Literature on Transmission, Detection, and Ocular Manifestations. Med Sci Monit. 2021 Sep 11;27:e931863. doi: 10.12659/MSM.931863
Feng Y, Armenti ST, Mian SI. COVID-19 and the Eye: A Comprehensive Review of the Literature. Int Ophthalmol Clin. 2021 Jan 1;61(1):1-14. doi:10.1097/IIO.0000000000000339
Farvardin M, Johari M, Tahamtan M et al. Ophthalmic manifestations of COVID-19; a less-appreciated yet significant challenge. Int Ophthalmol. 2021 Mar;41(3):1141-1147. doi: 10.1007/s10792-020-01664-2
Marinho PM, Marcos AAA, Romano AC, Nascimento H, Belfort R Jr. Retinal findings in patients with COVID-19. Lancet. 2020 May 23;395(10237):1610. doi: 10.1016/S0140-6736(20)31014-X. Epub 2020 May 12
Mack HG, Fraser-Bell S. “COVID new normal” in ophthalmology: Implications for ophthalmologists, eye care, ophthalmic education and research. Clin Exp Ophthalmol. 2021 Jan;49(1):9-11. doi: 10.1111/ceo.13898
Lima LCF, Moraes Junior HV, Moraes HMV. COVID-19 Ocular Manifestations in the Early Phase of Disease. Ocul Immunol Inflamm. 2021 May 19;29(4):666-668. doi: 10.1080/09273948.2021.1887278
Ung L, Chodosh J. COVID-19 and the eye: alternative facts The 2022 Bowman Club, David L. Easty lecture. BMJ Open Ophthalmol. 2022 May;7(1):e001042. doi: 10.1136/bmjophth-2022-001042
Zhang Y, Stewart JM. Retinal and choroidal manifestations of COVID-19. Curr Opin Ophthalmol. 2021 Nov 1;32(6):536-540. doi: 10.1097/ICU.0000000000000801
Sen M, Honavar SG, Sharma N, Sachdev MS. COVID-19 and Eye: A Review of Ophthalmic Manifestations of COVID-19. Indian J Ophthalmol. 2021 Mar;69(3):488-509. doi: 10.4103/ijo. IJO_297_21
Özgür Y, Gamze UG, Funda C, Bahattin H, Selim D. Different Cases, Different Manifestations of Post-COVID-19 Retinal Artery Occlusion: A Case Series. Turk J Ophthalmol. 2023;53(2):124-129. doi: 10.4274/tjo.galenos.2022.36930
İbrahim EA, Demet A. Prospective Study: Frequency of Ophthalmic Findings, Relationship with Inflammation Markers, and Effect on Prognosis in Patients Treated in the COVID-19 Intensive Care Unit Turk J Ophthalmol. 2022;52:6-13.
Sen S, Kannan NB, Kumar J et al. Retinal manifestations in patients with SARS-CoV-2 infection and pathogenetic implications: a systematic review. Int Ophthalmol. 2022 Jan;42(1):323-336. doi: 10.1007/s10792-021-01996-7
Ung L, Chodosh J. COVID-19 and the eye: alternative facts The 2022 Bowman Club, David L. Easty lecture. BMJ Open Ophthalmol. 2022 May;7(1):e001042. doi: 10.1136/bmjophth-2022-001042
Lani-Louzada R, Ramos CDVF, Cordeiro RM, Sadun AA. Retinal changes in COVID-19 hospitalized cases. PLoS One. 2020 Dec 3;15(12):e0243346. doi: 10.1371/journal.pone.0243346
D’Aloisio R, Nasillo V, Gironi M, Mastropasqua R. Bilateral macular hemorrhage in a patient with COVID-19. Am J Ophthalmol Case Rep. 2020 Dec;20:100958. doi: 10.1016/j.ajoc.2020.100958. Epub 2020 Oct 9
Gascon P, Briantais A, Bertrand E et al. Covid-19-Associated Retinopathy: A Case Report, Ocular Immunology and Inflammation, 2020;28:8,1293-1297. doi: 10.1080/09273948.2020.1825751
Acharya S, Diamond M, Anwar S, Glaser A, Tyagi P. Unique case of central retinal artery occlusion secondary to COVID-19 disease. IDCases. 2020;21:e00867. Epub 2020 Jun 18. doi: 10.1016/j.idcr.2020.e00867
Gaba WH, Ahmed D, Al Nuaimi RK, Dhanhani AA, Eatamadi H. Bilateral Central Retinal Vein Occlusion in a 40-Year-Old Man with Severe Coronavirus Disease 2019 (COVID-19) Pneumonia. Am J Case Rep. 2020 Oct 29;21:e927691. doi: 10.12659/AJCR.927691
Walinjkar JA, Makhija SC, Sharma HR, Morekar SR, Natarajan S. Central retinal vein occlusion with COVID-19 infection as the presumptive etiology. Indian J Ophthalmol. 2020 Nov;68(11):2572-2574. doi: 10.4103/ijo.IJO_2575_20
Invernizzi A, Pellegrini M, Messenio D et al. Impending Central Retinal Vein Occlusion in a Patient with Coronavirus Disease 2019 (COVID-19), Ocular Immunology and Inflammation, 2020;28(8):1290-1292. doi: 10.1080/09273948.2020.1807023
Insausti-García A, Reche-Sainz JA, Ruiz-Arranz C, López Vázquez Á, Ferro-Osuna M. Papillophlebitis in a COVID-19 patient: Inflammation and hypercoagulable state. Eur J Ophthalmol. 2022 Jan;32(1):NP168-NP172. Epub 2020 Jul 30. doi: 10.1177/1120672120947591
Sheth JU, Narayanan R, Goyal J, Goyal V. Retinal vein occlusion in COVID-19: A novel entity. Indian J Ophthalmol. 2020 Oct;68(10):2291-2293. doi: 10.4103/ijo.IJO_2380_20
Virgo J, Mohamed M. Paracentral acute middle maculopathy and acute macular neuroretinopathy following SARS-CoV-2 infection. Eye (Lond). 2020 Dec;34(12):2352-2353. Epub 2020 Jul 3. doi: 10.1038/s41433-020-1069-8
Filho LAZ, Lima LH, Melo GB, Zett C, Farah ME. Vitritis and Outer Retinal Abnormalities in a Patient with COVID-19, Ocular Immunology and Inflammation, 2020;28(8):12981300. doi: 10.1080/09273948.2020.1821898
Valapala VNG, Dasari N, Kolli VK, Mandapaka M. Clinical and biochemical profile of COVID-19 patients admitted in a tertiary care hospital in Visakhapatnam, India during post unlock 2.0 a retrospective study. J Med Life. 2022 Feb;15(2):264-268. doi: 10.25122/ jml-2021-0341
Ali HN, Ali KM, Rostam HM et al. Clinical laboratory parameters and comorbidities associated with severity of coronavirus disease 2019 (COVID-19) in Kurdistan Region of Iraq. Pract Lab Med. 2022 Aug;31:e00294. doi: 10.1016/j.plabm.2022.e00294
Desideri LF, Tovani-Palone MR. COVID-19 and the increased risk of myopia and digital eye strain. Einstein (Sao Paulo). 2021 May 24;19:eCE6491. doi: 10.31744/einstein_journal/2021CE6491
Sethi K, Levine ES, Roh S, Marx JL, Ramsey DJ. Modeling the impact of COVID-19 on Retina Clinic Performance. BMC Ophthalmol. 2021 May 10;21(1):206. doi: 10.1186/s12886-021-01955-x
Order of the Ministry of Health of Ukraine of March 28, 2020 No. 722, Available from: https://www.dec.gov.ua/mtd/koronavirus- na-hvoroba-2019-covid-19/
Clinical management of patients with COVID-19 “live” clinical guideline from 2021, Available from: https://www.dec.gov.ua/ mtd/koronavirusna-hvoroba-2019-covid-19/
Al-Samkari H, Karp Leaf RS, Dzik WH et al. COVID-19 and coagulation: bleeding and thrombotic manifestations of SARS-CoV-2 infection. Blood. 2020 Jul 23;136(4):489-500. doi: 10.1182/ blood.2020006520
Rostami M, Mansouritorghabeh H. D-dimer level in COVID-19 infection: a systematic review. Expert Rev Hematol. 2020 Nov;13(11):1265-1275. doi: 10.1080/17474086.2020.1831383
Zhan H, Chen H, Liu C et al. Diagnostic Value of D-Dimer in COVID-19: A Meta-Analysis and Meta-Regression. Clin Appl Thromb Hemost. 2021 Jan-Dec;27:10760296211010976. doi: 10.1177/10760296211010976
Shi C, Wang C, Wang H, et al. The potential of low molecular weight heparin to mitigate cytokine storm in severe COVID-19 patients: a retrospective clinical study. medRxiv. 2020 2020.2003.2028.20046144
Zhang Y, Xiao M, Zhang S, et al. Coagulopathy and antiphospholipid antibodies in patients with Covid-19. N Engl J Med. 2020;382(17):e38.
Connors JM, Levy JH. COVID-19 and its implications for thrombosis and anticoagulation. Blood. 2020 Jun 4;135(23):2033-2040. doi: 10.1182/blood.2020006000
Zhao H, Zhang LD, Liu LF et al. Blood Levels of Glycated Hemoglobin, D-Dimer, and Fibrinogen in Diabetic Retinopathy. Diabetes Metab Syndr Obes. 2021 Jun 2;14:2483-2488. doi: 10.2147/DMSO. S309068
Dan-Brezis I, Zahavi A, Axer-Siegel R et al. Inflammation, angiogenesis and coagulation interplay in a variety of retinal diseases. Acta Ophthalmol. 2020 Aug;98(5): e559-e562. doi: 10.1111/ aos.14331
Yang L, Chen Y, Zhang Y, Shen T, Shen X. Changes in retinal circulation and choroidal thickness in patients with acute myeloid leukemia detected by optical coherence tomography angiography. Front Med (Lausanne). 2023 Mar 13;10:1117204. doi: 10.3389/ fmed.2023.1117204
Zhou P, Yang XL, Wang XG et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature. 2020 Mar;579(7798):270-273. doi: 10.1038/s41586-020-2012-7. Epub 2020 Feb 3. Erratum in: Nature. 2020 Dec;588(7836):E6
Li YP, Ma Y, Wang N, Jin ZB. Eyes on coronavirus. Stem Cell Res. 2021 Mar;51:102200. Epub 2021 Jan 27. doi: 10.1016/j.scr.2021.102200
Ahmad Mulyadi Lai HI, Chou SJ, Chien Y et al. Expression of Endogenous Angiotensin-Converting Enzyme 2 in Human Induced Pluripotent Stem Cell-Derived Retinal Organoids. Int J MolSci. 2021 Jan 28;22(3):1320. doi: 10.3390/ijms22031320
Hill JM, Clement C, Arceneaux L, Lukiw WJ. Angiotensin Converting Enzyme 2 (ACE2) Expression in the Aged Brain and Visual System. J AgingSci. 2021;Vol 9(Suppl 7):001. Epub 2021 Sep 30.
Hu K, Patel J, Swiston C, Patel BC. Ophthalmic Manifestations of Coronavirus (COVID-19). 2022 May 24. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2024 Jan. PMID: 32310553.
Lani-Louzada R, Ramos CDVF, Cordeiro RM, Sadun AA. Retinal changes in COVID-19 hospitalized cases. PLoS One. 2020 Dec 3;15(12): e0243346. doi: 10.1371/journal.pone.0243346
Landecho MF, Yuste JR, Gándara E et al. COVID-19 retinal microangiopathy as an in vivo biomarker of systemic vascular disease? (Rapid Communication). J Intern Med. 2021;289:116-120. doi: 10.1111/joim.13156
Lin CH, Sun IT. Bilateral Simultaneous Central Retinal Vein Occlusion Secondary to COVID-19: A Case Report. Case Rep Ophthalmol. 2023 Feb 17;14(1):56-61. doi: 10.1159/000529298
Venkatesh R, Reddy NG, Agrawal S, Pereira A. COVID-19-associated central retinal vein occlusion treated with oral aspirin. BMJ Case Rep. 2021 May 19;14(5): e242987. doi: 10.1136/bcr-2021-242987
Saha R, Singh SK, Samanta S. Fundus Examination to Guide Anticoagulation Therapy in Suspected COVID-19 in a Critical Care Unit. Indian J Crit Care Med 2021;25(6):737-738.
de Oliveira MR, Lucena ARV, Higino TM, Ventura CV. Central retinal artery occlusion with cilioretinal artery sparing secondary to COVID-19: Additional ocular complication. Indian J Ophthalmol. 2023 Feb;71(2):663-666. doi: 10.4103/ijo.IJO_1246_22
Padhy SK, Dcruz RP, Kelgaonkar A. Paracentral acute middle maculopathy following SARS-CoV-2 infection: the D-dimer hypothesis. BMJ Case Rep. 2021 Mar 4;14(3):e242043. doi: 10.1136/bcr-2021242043
Korol AR, Bezditko PA, Bezkorovayna IM et al. Management of patients with chronic retinal diseases in the current conditions of the COVID-19 pandemic in the world and in Ukraine. Oftalmol Zh. 2021;90(2):82-85. doi: 10.31288/oftalmolzh202128284