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

České info

Cíl studie: Zkoumání vztahu mezi závažností metabolických změn vyvolaných COVID-19 a strukturou a četností změn na sítnici podle dat z vyšetření očních pozadí pacientů s různým klinickým průběhem onemocnění COVID-19.

Materiál a metody: Vyšetřeno bylo 117 pacientů s onemocněním COVID-19. Při vyšetření pacientů byla zjišťována závažnost průběhu onemocnění COVID-19 a expresivita metabolických změn; záznam obrazu očních pozadí byl pořizován pomocí přenosných fundus kamer Pictor Plus Fundus Camera a VistaView (Volk Optical).

Výsledky: Výsledkem výzkumu je zjištění změn na sítnici u 49 (41,9 %) pacientů s onemocněním COVID-19. V 8 (16,3 %) případech byly pozorovány klinicky významné změny sítnice a oka indukované infekcí COVID-19 (krvácení do sklivce, pretrombóza centrální sítnicové žíly nebo větví centrální sítnicové žíly, trombóza centrální sítnicové žíly nebo větví centrální sítnicové žíly), které vedly ke snížení zrakové ostrosti. Ve 41 (83,7 %) případech byly pozorovány klinicky nevýznamné změny sítnice indukované infekcí COVID-19 (vatovitá ložiska, zúžené sítnicové cévy, intraretinální a petechiální krvácení, tortuozita a dilatace sítnicových venul). Klinicky významné změny na sítnici se vyskytly u pacientů se statisticky významně vyšší hladinou D-dimerů a vyšším procentuálním výskytem lézí plicního parenchymu oproti skupině pacientů s klinicky nevýznamnými sítnicovými změnami (p < 0,05).

Závěry: Struktura retinálních změn u pacientů s COVID-19 koreluje se závažností klinického průběhu onemocnění a metabolických změn pacientů. Metabolické změny korelují se změnami sítnice a mohou mít prediktivní význam v prevenci celkových cévních komplikací spojených s onemocněním COVID-19.

Klíčová slova:

metabolismus – sítnice – Retina – COVID-19 – oftalmoskopie – sítnicové cévy

Authors: Kateryna Hutsaliuk ^1,2; Nataliia Skalska ³; Nadiia Ulianova ^2,4
Authors place of work: 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
Published in the journal: Čes. a slov. Oftal., 80, 2024, No. 3, p. 156-166
Category: Původní práce
doi: https://doi.org/10.31348/2024/12

Summary

Aims: To study the relationship between the severity of COVID-induced metabolic changes and the structure and frequency of retinal chan-
ges, 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.

Keywords:

Metabolism – Retinal vessels – Retina – COVID-19 – ophthalmoscopy

Zdroje

Poděkování: Doc. Vitaly Guryanov, Oddělení péče o zdraví, O. O. Bogomolcova národní lékařská univerzita

1. 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

2. 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

3. 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

4. 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

5. 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

6. 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

7. 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

8. 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

9. 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

10. 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

11. 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

12. 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.

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

14. 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

15. 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

16. 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

17. 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

18. 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

19. 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

20. 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

21. 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

22. 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

23. 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

24. 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

25. 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):1298-1300. doi: 10.1080/09273948.2020.1821898

26. 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

27. 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

28. 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

29. 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

30. Order of the Ministry of Health of Ukraine of March 28, 2020 No. 722, Available from: https://www.dec.gov.ua/mtd/koronavirusna-hvoroba-2019-covid-19/

31. 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/

32. 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

33. 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

34. 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

35. 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

36. 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.

37. 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

38. 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

39. 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

40. 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

41. 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

42. 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

43. 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

44. 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.

45. 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.

46. 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

47. 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

48. 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

49. 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

50. 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.

51. 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

52. 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-2021-242043

53. 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