Bilateral neurorethinovasculitis associated with COVID-19 infection in a girl 17 years old

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access


Despite dominant lung lesions, new coronavirus infection (COVID-19) can influence almost any organ, including eyes. According to modern data, frequency of eye damage by COVID-19 reaches 32%, and spectrum of clinical manifestations is diverse. Changes are observed both in the anterior (mainly conjunctivitis) and posterior (mostly retinal vascular thrombosis, optic neuritis, neuroretinitis) segments of the eye, and the timing of their occurrence varies from the first (sometimes the only) clinical symptoms of the disease to the development at the peak or during the period of convalescence from COVID-19.

In children symptomatic COVID-19 infection is diagnosed less frequently than in adults, and ophthalmic manifestations are less investigated. This article describes a case of bilateral neuroretinovasculitis in a 17-year-old girl with a mild course of COVID-19, that arose 3 weeks after the onset of the disease, which broadens the understanding of ocular manifestations of COVID-19 in children.

We emphasize that an ophthalmologist should know ocular manifestations of COVID-19, which can help in the diagnosis and further study of the frequency and spectrum of ophthalmic symptoms, especially in children

Full Text

Restricted Access

About the authors

Ekaterina Denisova

Helmholtz National Medical Research Center of Eye Diseases

ORCID iD: 0000-0003-3735-6249

PhD, researcher, department of children’s eye pathology

Russian Federation, Moscow

E. N Demchenko

Helmholtz National Medical Research Center of Eye Diseases

ORCID iD: 0000-0001-6523-5191


Russian Federation, Moscow

Elizaveta A. Geraskina

Helmholtz National Medical Research Center of Eye Diseases

ORCID iD: 0000-0002-5306-2534

graduate student

Russian Federation, Moscow

Mariia A. Khrabrova

Helmholtz National Medical Research Center of Eye Diseases

ORCID iD: 0000-0001-9422-4264

graduate student

Russian Federation, Moscow

Anna Y. Panova

Helmholtz National Medical Research Center of Eye Diseases

Author for correspondence.
ORCID iD: 0000-0003-2103-1570

junior reseacher

Russian Federation, Moscow


  1. Abrishami M, Tohidinezhad F, Daneshvar R, et al. Ocular Manifestations of Hospitalized Patients with COVID-19 in Northeast of Iran. Ocul Immunol Inflamm. 2020;28(5):739-744. doi: 10.1080/09273948.2020.1773868
  2. Atum M, Boz AAE, Cakir B, et al. Evaluation of Conjunctival Swab PCR Results in Patients with SARS-CoV-2 Infection. Ocul Immunol Inflamm. 2020;28(5):745-748. doi: 10.1080/09273948.2020.1775261
  3. Casalino G, Monaco G, Di Sarro PP, et al. Coronavirus disease 2019 presenting with conjunctivitis as the first symptom. Eye (Lond). 2020;34(7):1235-1236. doi: 10.1038/s41433-020-0909-x
  4. Chen L, Liu M, Zhang Z, et al. Ocular manifestations of a hospitalised patient with confirmed 2019 novel coronavirus disease. Br J Ophthalmol. 2020;104(6):748-751. doi: 10.1136/bjophthalmol-2020-316304
  5. Chen L, Deng C, Chen X, et al. Ocular manifestations and clinical characteristics of 535 cases of COVID-19 in Wuhan, China: a cross-sectional study. Acta Ophthalmol. 2020;98(8):e951-e959. doi: 10.1111/aos.14472
  6. Daruich A, Martin D, Bremond-Gignac D. Ocular manifestation as first sign of Coronavirus Disease 2019 (COVID-19): Interest of telemedicine during the pandemic context. J Fr Ophtalmol. 2020;43(5):389-391. doi: 10.1016/j.jfo.2020.04.002
  7. Guemes-Villahoz N, Burgos-Blasco B, Arribi-Vilela A, et al. Detecting SARS-CoV-2 RNA in conjunctival secretions: Is it a valuable diagnostic method of COVID-19? J Med Virol. 2021;93(1):383-388. doi: 10.1002/jmv.26219
  8. Khavandi S, Tabibzadeh E, Naderan M, Shoar S. Corona virus disease-19 (COVID-19) presenting as conjunctivitis: atypically high-risk during a pandemic. Cont Lens Anterior Eye. 2020;43(3):211-212. doi: 10.1016/j.clae.2020.04.010
  9. Mahmoud H, Ammar H, El Rashidy A, et al. Assessment of Coronavirus in the Conjunctival Tears and Secretions in Patients with SARS-CoV-2 Infection in Sohag Province, Egypt. Clin Ophthalmol. 2020;14:2701-2708. doi: 10.2147/OPTH.S270006
  10. Marquezan MC, Marquezam JP, Nascimento H, et al. Conjunctivitis Related to not Severe COVID-19: A Case Report. Ocul Immunol Inflamm. 2020:1-3. doi: 10.1080/09273948.2020.1837186
  11. Maychuk DY, Atlas SN, Loshkareva AO. Ocular manifestations of coronavirus infection COVID-19 (clinical observation). Vestn Oftalmol. 2020;136(4):118-123. (In Russ). doi: 10.17116/oftalma2020136041118
  12. Meduri A, Oliverio GW, Mancuso G, et al. Ocular surface manifestation of COVID-19 and tear film analysis. Sci Rep. 2020;10(1):20178. doi: 10.1038/s41598-020-77194-9
  13. Ozturker ZK. Conjunctivitis as sole symptom of COVID-19: A case report and review of literature. Eur J Ophthalmol. 2021;31(2):NP161-NP166. doi: 10.1177/1120672120946287
  14. Scalinci SZ, Trovato Battagliola E. Conjunctivitis can be the only presenting sign and symptom of COVID-19. IDCases. 2020;20:e00774. doi: 10.1016/j.idcr.2020.e00774
  15. Sindhuja K, Lomi N, Asif MI, Tandon R. Clinical profile and prevalence of conjunctivitis in mild COVID-19 patients in a tertiary care COVID-19 hospital: A retrospective cross-sectional study. Indian J Ophthalmol. 2020;68(8):1546-1550. doi: 10.4103/ijo.IJO_1319_20
  16. Sirakaya E, Sahiner M, Aslan Sirakaya H. A Patient With Bilateral Conjunctivitis Positive for SARS-CoV-2 RNA in a Conjunctival Sample. Cornea. 2021;40(3):383-386. doi: 10.1097/ICO.0000000000002485
  17. Wu P, Duan F, Luo C, et al. Characteristics of Ocular Findings of Patients With Coronavirus Disease 2019 (COVID-19) in Hubei Province, China. JAMA Ophthalmol. 2020;138(5):575-578. doi: 10.1001/jamaophthalmol.2020.1291
  18. Xia J, Tong J, Liu M, et al. Evaluation of coronavirus in tears and conjunctival secretions of patients with SARS-CoV-2 infection. J Med Virol. 2020;92(6):589-594. doi: 10.1002/jmv.25725
  19. Zhang X, Chen X, Chen L, et al. The evidence of SARS-CoV-2 infection on ocular surface. Ocul Surf. 2020;18(3):360-362. doi: 10.1016/j.jtos.2020.03.010
  20. Karimi S, Arabi A, Shahraki T, Safi S. Detection of severe acute respiratory syndrome Coronavirus-2 in the tears of patients with Coronavirus disease 2019. Eye (Lond). 2020;34(7):1220-1223. doi: 10.1038/s41433-020-0965-2
  21. Seah IYJ, Anderson DE, Kang AEZ, et al. Assessing Viral Shedding and Infectivity of Tears in Coronavirus Disease 2019 (COVID-19) Patients. Ophthalmology. 2020;127(7):977-979. doi: 10.1016/j.ophtha.2020.03.026
  22. Zhou Y, Duan C, Zeng Y, et al. Ocular Findings and Proportion with Conjunctival SARS-COV-2 in COVID-19 Patients. Ophthalmology. 2020;127(7):982-983. doi: 10.1016/j.ophtha.2020.04.028
  23. Cheema M, Aghazadeh H, Nazarali S, et al. Keratoconjunctivitis as the initial medical presentation of the novel coronavirus disease 2019 (COVID-19). Can J Ophthalmol. 2020;55(4):e125-e129. doi: 10.1016/j.jcjo.2020.03.003
  24. Guo D, Xia J, Wang Y, et al. Relapsing viral keratoconjunctivitis in COVID-19: a case report. Virol J. 2020;17(1):97. doi: 10.1186/s12985-020-01370-6
  25. Mendez Mangana C, Barraquer Kargacin A, Barraquer RI. Episcleritis as an ocular manifestation in a patient with COVID-19. Acta Ophthalmol. 2020;98(8):e1056-e1057. doi: 10.1111/aos.14484
  26. Otaif W, Al Somali AI, Al Habash A. Episcleritis as a possible presenting sign of the novel coronavirus disease: A case report. Am J Ophthalmol Case Rep. 2020;20:100917. doi: 10.1016/j.ajoc.2020.100917
  27. Kumar K, Prakash AA, Gangasagara SB, et al. Presence of viral RNA of SARS-CoV-2 in conjunctival swab specimens of COVID-19 patients. Indian J Ophthalmol. 2020;68(6):1015-1017. doi: 10.4103/ijo.IJO_1287_20
  28. Li X, Chan JF, Li KK, et al. Detection of SARS-CoV-2 in conjunctival secretions from patients without ocular symptoms. Infection. 2021;49(2):257-265. doi: 10.1007/s15010-020-01524-2
  29. Xie HT, Jiang SY, Xu KK, et al. SARS-CoV-2 in the ocular surface of COVID-19 patients. Eye Vis (Lond). 2020;7:23. doi: 10.1186/s40662-020-00189-0
  30. Kaya H, Caliskan A, Okul M, et al. Detection of SARS-CoV-2 in the tears and conjunctival secretions of Coronavirus disease 2019 patients. J Infect Dev Ctries. 2020;14(9):977-981. doi: 10.3855/jidc.13224
  31. Sun CB, Wang YY, Liu GH, Liu Z. Role of the Eye in Transmitting Human Coronavirus: What We Know and What We Do Not Know. Front Public Health. 2020;8:155. doi: 10.3389/fpubh.2020.00155
  32. Ulhaq ZS, Soraya GV. The prevalence of ophthalmic manifestations in COVID-19 and the diagnostic value of ocular tissue/fluid. Graefes Arch Clin Exp Ophthalmol. 2020;258(6):1351-1352. doi: 10.1007/s00417-020-04695-8
  33. Colavita F, Lapa D, Carletti F, et al. SARS-CoV-2 Isolation From Ocular Secretions of a Patient With COVID-19 in Italy With Prolonged Viral RNA Detection. Ann Intern Med. 2020;173(3):242-243. doi: 10.7326/M20-1176
  34. Gonzalez-Lopez JJ, Felix Espinar B, Ye-Zhu C. Symptomatic Retinal Microangiophaty in a Patient with Coronavirus Disease 2019 (COVID-19): Single Case Report. Ocul Immunol Inflamm. 2020:1-3. doi: 10.1080/09273948.2020.1852260
  35. Invernizzi A, Torre A, Parrulli S, et al. Retinal findings in patients with COVID-19: Results from the SERPICO-19 study. EClinicalMedicine. 2020;27:100550. doi: 10.1016/j.eclinm.2020.100550
  36. Landecho MF, Yuste JR, Gandara E, et al. COVID-19 retinal microangiopathy as an in vivo biomarker of systemic vascular disease? J Intern Med. 2021;289(1):116-120. doi: 10.1111/joim.13156
  37. Lani-Louzada R, Ramos C, Cordeiro RM, Sadun AA. Retinal changes in COVID-19 hospitalized cases. PLoS One. 2020;15(12):e0243346. doi: 10.1371/journal.pone.0243346
  38. Marinho PM, Marcos AAA, Romano AC, et al. Retinal findings in patients with COVID-19. Lancet. 2020;395(10237):1610. doi: 10.1016/S0140-6736(20)31014-X
  39. Gaba WH, Ahmed D, Al Nuaimi RK, et al. Bilateral Central Retinal Vein Occlusion in a 40-Year-Old Man with Severe Coronavirus Disease 2019 (COVID-19) Pneumonia. Am J Case Rep. 2020;21:e927691. doi: 10.12659/AJCR.927691
  40. Invernizzi A, Pellegrini M, Messenio D, et al. Impending Central Retinal Vein Occlusion in a Patient with Coronavirus Disease 2019 (COVID-19). Ocul Immunol Inflamm. 2020;28(8):1290-1292. doi: 10.1080/09273948.2020.1807023
  41. Raval N, Djougarian A, Lin J. Central retinal vein occlusion in the setting of COVID-19 infection. J Ophthalmic Inflamm Infect. 2021;11:10. doi: 10.1186/s12348-021-00241-7
  42. Sheth JU, Narayanan R, Goyal J, Goyal V. Retinal vein occlusion in COVID-19: A novel entity. Indian J Ophthalmol. 2020;68(10):2291-2293. doi: 10.4103/ijo.IJO_2380_20
  43. Yahalomi T, Pikkel J, Arnon R, Pessach Y. Central retinal vein occlusion in a young healthy COVID-19 patient: A case report. Am J Ophthalmol Case Rep. 2020;20:100992. doi: 10.1016/j.ajoc.2020.100992
  44. Acharya S, Diamond M, Anwar S, et al. Unique case of central retinal artery occlusion secondary to COVID-19 disease. IDCases. 2020;21:e00867. doi: 10.1016/j.idcr.2020.e00867
  45. Dumitrascu OM, Volod O, Bose S, et al. Acute ophthalmic artery occlusion in a COVID-19 patient on apixaban. J Stroke Cerebrovasc Dis. 2020;29(8):104982. doi: 10.1016/j.jstrokecerebrovasdis.2020.104982
  46. Gascon P, Briantais A, Bertrand E, et al. Covid-19-Associated Retinopathy: A Case Report. Ocul Immunol Inflamm. 2020;28(8):1293-1297. doi: 10.1080/09273948.2020.1825751
  47. Virgo J, Mohamed M. Paracentral acute middle maculopathy and acute macular neuroretinopathy following SARS-CoV-2 infection. Eye (Lond). 2020;34(12):2352-2353. doi: 10.1038/s41433-020-1069-8
  48. Insausti-Garcia A, Reche-Sainz JA, Ruiz-Arranz C, et al. Papillophlebitis in a COVID-19 patient: Inflammation and hypercoagulable state. Eur J Ophthalmol. 2020:1120672120947591. doi: 10.1177/1120672120947591
  49. Bettach E, Zadok D, Weill Y, et al. Bilateral anterior uveitis as a part of a multisystem inflammatory syndrome secondary to COVID-19 infection. J Med Virol. 2021;93(1):139-140. doi: 10.1002/jmv.26229
  50. Zago Filho LA, Lima LH, Melo GB, et al. Vitritis and Outer Retinal Abnormalities in a Patient with COVID-19. Ocul Immunol Inflamm. 2020;28(8):1298-1300. doi: 10.1080/09273948.2020.1821898
  51. Sawalha K, Adeodokun S, Kamoga GR. COVID-19-Induced Acute Bilateral Optic Neuritis. J Investig Med High Impact Case Rep. 2020;8:2324709620976018. doi: 10.1177/2324709620976018
  52. Benito-Pascual B, Gegundez JA, Diaz-Valle D, et al. Panuveitis and Optic Neuritis as a Possible Initial Presentation of the Novel Coronavirus Disease 2019 (COVID-19). Ocul Immunol Inflamm. 2020;28(6):922-925. doi: 10.1080/09273948.2020.1792512
  53. Zhou S, Jones-Lopez EC, Soneji DJ, et al. Myelin Oligodendrocyte Glycoprotein Antibody-Associated Optic Neuritis and Myelitis in COVID-19. J Neuroophthalmol. 2020;40(3):398-402. doi: 10.1097/WNO.0000000000001049
  54. Novi G, Rossi T, Pedemonte E, et al. Acute disseminated encephalomyelitis after SARS-CoV-2 infection. Neurol Neuroimmunol Neuroinflamm. 2020;7(5). doi: 10.1212/NXI.0000000000000797
  55. Gutierrez-Ortiz C, Mendez-Guerrero A, Rodrigo-Rey S, et al. Miller Fisher syndrome and polyneuritis cranialis in COVID-19. Neurology. 2020;95(5):e601-e605. doi: 10.1212/WNL.0000000000009619
  56. Martinez Diaz M, Copete Piqueras S, Blanco Marchite C, Vahdani K. Acute dacryoadenitis in a patient with SARS-CoV-2 infection. Orbit. 2021:1-4. doi: 10.1080/01676830.2020.1867193
  57. Ludvigsson JF. Systematic review of COVID-19 in children shows milder cases and a better prognosis than adults. Acta Paediatr. 2020;109(6):1088-1095. doi: 10.1111/apa.15270
  58. Chiotos K, Bassiri H, Behrens EM, et al. Multisystem Inflammatory Syndrome in Children During the Coronavirus 2019 Pandemic: A Case Series. J Pediatric Infect Dis Soc. 2020;9(3):393-398. doi: 10.1093/jpids/piaa069
  59. Riphagen S, Gomez X, Gonzalez-Martinez C, et al. Hyperinflammatory shock in children during COVID-19 pandemic. Lancet. 2020;395(10237):1607-1608. doi: 10.1016/S0140-6736(20)31094-1
  60. Ma N, Li P, Wang X, et al. Ocular Manifestations and Clinical Characteristics of Children With Laboratory-Confirmed COVID-19 in Wuhan, China. JAMA Ophthalmol. 2020;138(10):1079-1086. doi: 10.1001/jamaophthalmol.2020.3690
  61. Valente P, Iarossi G, Federici M, et al. Ocular manifestations and viral shedding in tears of pediatric patients with coronavirus disease 2019: a preliminary report. J AAPOS. 2020;24(4):212-215. doi: 10.1016/j.jaapos.2020.05.002
  62. Wu P, Liang L, Chen C, Nie S. A child confirmed COVID-19 with only symptoms of conjunctivitis and eyelid dermatitis. Graefes Arch Clin Exp Ophthalmol. 2020;258(7):1565-1566. doi: 10.1007/s00417-020-04708-6
  63. Quaranta L, Rovida F, Riva I, et al. Identification of SARS-CoV-2 RNA in the conjunctival swab of an Italian pediatric patient affected with COVID-19: A case report. Eur J Ophthalmol. 2020:1120672120977822. doi: 10.1177/1120672120977822
  64. Walinjkar JA, Makhija SC, Sharma HR, et al. Central retinal vein occlusion with COVID-19 infection as the presumptive etiology. Indian J Ophthalmol. 2020;68(11):2572-2574. doi: 10.4103/ijo.IJO_2575_20
  65. de Ruijter NS, Kramer G, Gons RAR, Hengstman GJD. Neuromyelitis optica spectrum disorder after presumed coronavirus (COVID-19) infection: A case report. Mult Scler Relat Disord. 2020;46:102474. doi: 10.1016/j.msard.2020.102474
  66. Turbin RE, Wawrzusin PJ, Sakla NM, et al. Orbital cellulitis, sinusitis and intracranial abnormalities in two adolescents with COVID-19. Orbit. 2020;39(4):305-310. doi: 10.1080/01676830.2020.1768560
  67. Leonardi A, Rosani U, Brun P. Ocular Surface Expression of SARS-CoV-2 Receptors. Ocul Immunol Inflamm. 2020;28(5):735-738. doi: 10.1080/09273948.2020.1772314
  68. Roehrich H, Yuan C, Hou JH. Immunohistochemical Study of SARS-CoV-2 Viral Entry Factors in the Cornea and Ocular Surface. Cornea. 2020;39(12):1556-1562. doi: 10.1097/ICO.0000000000002509
  69. Salamanna F, Maglio M, Landini MP, Fini M. Body Localization of ACE-2: On the Trail of the Keyhole of SARS-CoV-2. Front Med (Lausanne). 2020;7:594495. doi: 10.3389/fmed.2020.594495
  70. 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):3301-3311. doi: 10.1167/iovs.06-1024
  71. Zhou L, Xu Z, Castiglione GM, et al. ACE2 and TMPRSS2 are expressed on the human ocular surface, suggesting susceptibility to SARS-CoV-2 infection. Ocul Surf. 2020;18(4):537-544. doi: 10.1016/j.jtos.2020.06.007
  72. Sawant OB, Singh S, Wright RE, 3rd, et al. Prevalence of SARS-CoV-2 in human post-mortem ocular tissues. Ocul Surf. 2021;19:322-329. doi: 10.1016/j.jtos.2020.11.002
  73. Neroev VV, Krichevskaya GI, Balatskaya NV. COVID-19 and problems of ophthalmology. Russian Ophthalmological Journal. 2020;13(4):99-104. doi: 10.21516/2072-0076-2020-13-4-99-104
  74. Neroev VV, Kiseleva TN, Eliseeva EK. Ophthalmological aspects of coronavirus infections. Russian Ophthalmological Journal. 2021;14(1):7-14. doi: 10.21516/2072-0076-2021-14-1-7-14
  75. Conde Cardona G, Quintana Pajaro LD, Quintero Marzola ID, et al. Neurotropism of SARS-CoV 2: Mechanisms and manifestations. J Neurol Sci. 2020;412:116824. doi: 10.1016/j.jns.2020.116824
  76. Varga Z, Flammer AJ, Steiger P, et al. Endothelial cell infection and endotheliitis in COVID-19. Lancet. 2020;395(10234):1417-1418. doi: 10.1016/S0140-6736(20)30937-5
  77. Casagrande M, Fitzek A, Puschel K, et al. Detection of SARS-CoV-2 in Human Retinal Biopsies of Deceased COVID-19 Patients. Ocul Immunol Inflamm. 2020;28(5):721-725. doi: 10.1080/09273948.2020.1770301

Supplementary files

Supplementary Files
1. Fig. a

Download (88KB)
2. Fig. 1. Photographs of the fundus of the right (a) and left (b) eyes of patient G. during visit to Helmholtz National Medical Research Center of Eye Diseases. The optic disc is pale pink, prominates, borders are difficult to trace, epipapillary fibrosis (more on the right), parapapillary from the temporal side, subretinal fibrosis in the form of two light vertical lines, folding of the retina in the area of the papillomacular bundle, foveolar reflex is smoothed, macular reflex is absent, folding of the retina in the macula. Left — intraretinal deposits of yellowish exudate in the macula and the area of the papillomacular bundle.

Download (96KB)
3. Fig. 2. Optical coherence tomography of the macula of the right (a) and left (b) eyes and the optic nerve disc of the right (c) and left (d) eyes of patient G. during visit to Helmholtz National Medical Research Center of Eye Diseases. Macula of both eyes — the fovea profile is preserved, retinal layers are differentiated, on the left in the nasal half of the macula — destruction of the ellipsoid zone, intraretinal hyperreflective inclusions. Central retinal thickness: on the right — 236, on the left — 213 microns. The optic nerve disc — prominence, epipapillary fibrous membrane, an increase in the thickness of the retinal nerve fibers layer parapapillary: on the right on average — 164, on the left — 217 microns.

Download (112KB)

Copyright (c) 2021 Eco-Vector

СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 28266 от 17.05.2007 г
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ЭЛ № ФС 77 - 80630 от 15.03.2021 г

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies