Purpose: The involvement of the ocular anterior segment by SARS-CoV-2 has been the subject of many studies, however, the repercussions on the posterior segment, particularly on the different layers of the retina and optic nerve, are still little known. The purpose of this study was to evaluate the impact of severe COVID-19 on the retinal ganglion cell layer (RGCL) thickness. Methods: This observational, prospective and analytical study was performed in the Ophthalmology Department of the FACISA University Center, Campina Grande. Three groups were included: group I (control), 29 healthy individuals who had not severe COVID-19; group II (infirmary), 24 individuals who had COVID-19 and were hospitalized in the infirmary; and group III, 25 individuals who had severe COVID-19 and required Intense Care Unit (ICU). All individuals had ophthalmologic examination and assessment of RGCL thickness using Optical Coherence Tomography (OCT). Statistical tests required p ≤ 0.05 to reject the null hypothesis. Results: The mean of RGCL thickness was significantly reduced in individuals from GIII (77.9 ± 8.9 μm), as compared with GII (83.9 ± 10.9 μm) and GI (82.8 ± 6.5 μm) (p = 0.0027). The mean measurements from the retinal neve fiber layer (RNFL) of the optic nerve head were similar. However, when evaluated sectoral, the mean of RNFL at the temporal sector of the optic disc was significantly lower in group GIII (p < 0.001). Conclusion: The RGCL thickness from patients with severe COVID-19 was significantly reduced. This finding supports that the SARS-CoV-2 has systemic action and affinity for nerve cells, including those from the retina and are related to the severity of the infection.
References
[1]
da Silva, S.J.R., do Nascimento, J.C.F., Germano Mendes, R.P., Guarines, K.M., Targino Alves da Silva, C., da Silva, P.G., et al. (2022) Two Years into the COVID-19 Pandemic: Lessons Learned. ACS Infectious Diseases, 8, 1758-1814. https://doi.org/10.1021/acsinfecdis.2c00204
[2]
Sharma, A., Ahmad Farouk, I. and Lal, S.K. (2021) COVID-19: A Review on the Novel Coronavirus Disease Evolution, Transmission, Detection, Control and Prevention. Viruses, 13, Article 202. https://doi.org/10.3390/v13020202
[3]
da Silva, F.F., de Abreu, L.C., Daboin, B.E.G., Morais, T.C., Cavalcanti, M.P.E., Bezerra, I.M.P., et al. (2023) Temporal Analysis of COVID-19 Epidemiological Indicators in a Low-Income Brazilian Context: A Retrospective Analysis in Paraiba State. Viruses, 15, Article 2016. https://doi.org/10.3390/v15102016
[4]
Zhong, Y., Wang, K., Zhu, Y., Lyu, D., Yu, Y., Li, S., et al. (2021) Ocular Manifestations in COVID-19 Patients: A Systematic Review and Meta-Analysis. Travel Medicine and Infectious Disease, 44, Article ID: 102191. https://doi.org/10.1016/j.tmaid.2021.102191
[5]
Sen, H.N., Vannella, K.M., Wang, Y., Chung, J., Kodati, S., Ramelli, S.C., et al. (2023) Histopathology and SARS-CoV-2 Cellular Localization in Eye Tissues of COVID-19 Autopsies. The American Journal of Pathology, 193, 1809-1816. https://doi.org/10.1016/j.ajpath.2023.02.016
[6]
Sawant, O.B., Singh, S., Wright, R.E., Jones, K.M., Titus, M.S., Dennis, E., et al. (2021) Prevalence of SARS-CoV-2 in Human Post-Mortem Ocular Tissues. The Ocular Surface, 19, 322-329. https://doi.org/10.1016/j.jtos.2020.11.002
[7]
Marinho, P.M., Marcos, A.A.A., Romano, A.C., Nascimento, H. and Belfort, R. (2020) Retinal Findings in Patients with COVID-19. The Lancet, 395, 1610. https://doi.org/10.1016/s0140-6736(20)31014-x
[8]
Teo, K.Y., Invernizzi, A., Staurenghi, G. and Cheung, C.M.G. (2022) Covid-19-Related Retinal Micro-Vasculopathy—A Review of Current Evidence. American Journal of Ophthalmology, 235, 98-110. https://doi.org/10.1016/j.ajo.2021.09.019
[9]
Patel, S., Finn, A., Kim, S. and Sternberg, P. (2023) Retina Procedure Volume Changes during the COVID-19 Pandemic. Ophthalmology Retina, 7, 553-554. https://doi.org/10.1016/j.oret.2023.01.016
[10]
Hohberger, B., Ganslmayer, M., Lucio, M., Kruse, F., Hoffmanns, J., Moritz, M., et al. (2021) Retinal Microcirculation as a Correlate of a Systemic Capillary Impairment after Severe Acute Respiratory Syndrome Coronavirus 2 Infection. Frontiers in Medicine, 8, Article 676554. https://doi.org/10.3389/fmed.2021.676554
[11]
Albertos-Arranz, H., Martínez-Gil, N., Sánchez-Sáez, X., Noailles, A., Monferrer Adsuara, C., Remolí Sargues, L., et al. (2023) Microglia Activation and Neuronal Alterations in Retinas from COVID-19 Patients: Correlation with Clinical Parameters. Eye and Vision, 10, Article No. 12. https://doi.org/10.1186/s40662-023-00329-2
[12]
Xu, B., Zhang, J., Zhang, Y., Cheng, Y. and Huang, Q. (2023) Transient Increase in Patient Numbers with “Acute Macular Neuroretinopathy” Post SARS-CoV-2 Infection—Case Series during the First Surge of Infection in December 2022. Journal of Inflammation Research, 16, 2763-2771. https://doi.org/10.2147/jir.s413050
[13]
Bilbao-Malavé, V., González-Zamora, J., Saenz de Viteri, M., de la Puente, M., Gándara, E., Casablanca-Piñera, A., et al. (2021) Persistent Retinal Microvascular Impairment in COVID-19 Bilateral Pneumonia at 6-Months Follow-Up Assessed by Optical Coherence Tomography Angiography. Biomedicines, 9, Article 502. https://doi.org/10.3390/biomedicines9050502
[14]
Li, Y., Ma, Y., Wang, N. and Jin, Z. (2021) Eyes on Coronavirus. Stem Cell Research, 51, Article ID: 102200. https://doi.org/10.1016/j.scr.2021.102200
[15]
Struyf, T., Deeks, J.J., Dinnes, J., Takwoingi, Y., Davenport, C., Leeflang, M.M., et al. (2022) Signs and Symptoms to Determine If a Patient Presenting in Primary Care or Hospital Outpatient Settings Has Covid-19. Cochrane Database of Systematic Reviews, 5, CD013665. https://doi.org/10.1002/14651858.cd013665.pub3
[16]
Menuchin-Lasowski, Y., Schreiber, A., Lecanda, A., Mecate-Zambrano, A., Brunotte, L., Psathaki, O.E., et al. (2022) SARS-CoV-2 Infects and Replicates in Photoreceptor and Retinal Ganglion Cells of Human Retinal Organoids. Stem Cell Reports, 17, 789-803. https://doi.org/10.1016/j.stemcr.2022.02.015
[17]
Mao, L., Jin, H., Wang, M., Hu, Y., Chen, S., He, Q., et al. (2020) Neurologic Manifestations of Hospitalized Patients with Coronavirus Disease 2019 in Wuhan, China. JAMA Neurology, 77, 683-690. https://doi.org/10.1001/jamaneurol.2020.1127
[18]
Cronin, J.N., Camporota, L. and Formenti, F. (2021) Mechanical Ventilation in COVID-19: A Physiological Perspective. Experimental Physiology, 107, 683-693. https://doi.org/10.1113/ep089400
[19]
Sumer, F. and Subasi, S. (2023) Effects of COVID-19 on Retinal and Choroidal Thickness by Optical Coherence Tomography. Journal of Glaucoma, 32, 569-574. https://doi.org/10.1097/ijg.0000000000002204
[20]
Obsa, M.S., kanche, Z.Z., Olana Fite, R., Tura, T.S., Adema, B.G., Kinfe, A.A., et al. (2020) Effect of Laryngeal Mask Airway Insertion on Intraocular Pressure Response: Systematic Review and Meta-Analysis. Anesthesiology Research and Practice, 2020, Article ID: 7858434. https://doi.org/10.1155/2020/7858434
[21]
Cifuentes-González, C., Rojas-Carabali, W., Pérez, Á.O., Carvalho, É., Valenzuela, F., Miguel-Escuder, L., et al. (2023) Risk Factors for Recurrences and Visual Impairment in Patients with Ocular Toxoplasmosis: A Systematic Review and Meta-Analysis. PLOS ONE, 18, e0283845. https://doi.org/10.1371/journal.pone.0283845
[22]
de Araújo, T.E., dos Santos, L.I., Gomes, A.O., Carneiro, A.C.A.V., Machado, A.S., Coelho-dos-Reis, J.G., et al. (2020) Putative Biomarkers for Early Diagnosis and Prognosis of Congenital Ocular Toxoplasmosis. Scientific Reports, 10, Article No. 16757. https://doi.org/10.1038/s41598-020-73265-z
[23]
Mohammadzadeh, V., Fatehi, N., Yarmohammadi, A., Lee, J.W., Sharifipour, F., Daneshvar, R., et al. (2020) Macular Imaging with Optical Coherence Tomography in Glaucoma. Survey of Ophthalmology, 65, 597-638. https://doi.org/10.1016/j.survophthal.2020.03.002
[24]
Ekici Gok, Z., Gok, A., Acun Delen, L., Kasapoglu, U.S., Gurbuz, E. and Mutlu, K. (2021) Evaluation of Eye Care and Ocular Findings in Critically Ill COVID-19 Patients. International Journal of Clinical Practice, 75, e14909. https://doi.org/10.1111/ijcp.14909
[25]
Umbrello, M., Venco, R., Antonucci, E., Cereghini, S., Filardo, C., Guglielmetti, L., et al. (2022) Incidence, Clinical Characteristics and Outcome of Barotrauma in Critically Ill Patients with COVID-19: A Systematic Review and Meta-Analysis. Minerva Anestesiologica, 88, 706-718. https://doi.org/10.23736/s0375-9393.22.16258-9