Skip to main content
SpringerLink
Log in

Eye Disorders and Neuro-ophthalmic Manifestations of COVID-19

  • Chapter
  • First Online:
Frontiers of COVID-19

  • 470 Accesses

Abstract

Growing data are confirming the association between the novel coronavirus disease (COVID-19) and eye disorders, including ocular alterations and neuro-ophthalmic manifestations. The main pathophysiological mechanisms considered included a direct infection through the ocular surface, a post-viremia secretion of the virus from the lacrimal glands, and a viral dissemination through the bloodstream. According to the different ways of contagion, different structures could be involved.

The most common ocular symptoms reported in COVID-19 patients were dry eye, redness, tearing, itching and pain. Among symptomatic patients, most of them presented conjunctivitis. Considering the posterior chamber, retinal artery and vein occlusions were described in few clinical reports; moreover, some studies presented cases of paracentral acute middle maculopathy occurring in COVID-19 patients. The involvement of the choroid seems to be rare, and a single case of atypical choroiditis was currently described. Between neuro-ophthalmic manifestations, optic neuritis appear to be relatively frequent and generally not associated with magnetic resonance imaging abnormalities. Some reports showed the involvement of the ocular motor nerves, often presenting with palsy. Miller Fisher syndrome has been showed in rare cases; however, this association could be corroborated by the several reports describing Guillain–Barré syndrome occurrence in COVID-19 patients.

In line with well-known previous viral infection, COVID-19 seems to be associated with eye involvement. Thus, ocular and neuro-ophthalmic symptoms and signs should be carefully assessed and monitored in these patients. To reach this purpose, it is critical to implement remote diagnostic techniques. Moreover, the comprehension of the pathogenetic mechanisms is still scarce and no standardized diagnostic protocol was established for these patients, making necessary further studies to improve current understandings.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Badawi AE, Elsheikh SS, Addeen SZ, Soliman MA, Abd-Rabu R, Abdella WS, Gad EA. An ophthalmic insight into novel coronavirus 2019 disease: a comprehensive review of the ocular manifestations and clinical hazards. J Curr Ophthalmol. 2020;32(4):315–28. https://doi.org/10.4103/JOCO.JOCO_255_20.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Nasiri N, Sharifi H, Bazrafshan A, Noori A, Karamouzian M, Sharifi A. Ocular manifestations of COVID-19: a systematic review and meta-analysis. J Ophthalmic Vis Res. 2021;16(1):103–12. https://doi.org/10.18502/JOVR.V16I1.8256.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Wu P, Duan F, Luo C, Liu Q, Xingguang Q, Liang L, Kaili W. Characteristics of ocular findings of patients with coronavirus disease 2019 (COVID-19) in Hubei Province, China. JAMA Ophthalmol. 2020;138(5):575. https://doi.org/10.1001/jamaophthalmol.2020.1291.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Azzolini C, Donati S, Premi E, Baj A, Siracusa C, Genoni A, Grossi PA, et al. SARS-CoV-2 on ocular surfaces in a cohort of patients with COVID-19 from the Lombardy region, Italy. JAMA Ophthalmol. 2021;139(9):1–9. https://doi.org/10.1001/jamaophthalmol.2020.5464.

    Article  PubMed Central  Google Scholar 

  5. Deng C, Yang Y, Chen H, Chen W, Chen Z, Ma K, Wang J. Ocular detection of SARS-CoV-2 in 114 cases of COVID-19 pneumonia in Wuhan, China: an observational study. SSRN Electron J. 2020; https://doi.org/10.2139/ssrn.3543587.

  6. Qu JY, Xie HT, Zhang MC. Evidence of SARS-CoV-2 transmission through the ocular route. Clin Ophthalmol. 2021;15:687–96. https://doi.org/10.2147/OPTH.S295283.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Kitazawa K, Deinhardt-Emmer S, Inomata T, Deshpande S, Sotozono C. The transmission of SARS-CoV-2 infection on the ocular surface and prevention strategies. Cell. 2021;10(4):796. https://doi.org/10.3390/cells10040796.

    Article  CAS  Google Scholar 

  8. Casagrande M, Fitzek A, Spitzer MS, Püschel K, Glatzel M, Krasemann S, Nörz D, Lütgehetmann M, Pfefferle S, Schultheiss M. Presence of SARS-CoV-2 RNA in the cornea of Viremic patients with COVID-19. JAMA Ophthalmol. 2021;139(4):383–8. https://doi.org/10.1001/jamaophthalmol.2020.6339.

    Article  PubMed  Google Scholar 

  9. Zeng W, Wang X, Li J, Yang Y, Qiu X, Song P, Jianjun X, Wei Y. Association of dailywear of eyeglasses with susceptibility to coronavirus disease 2019 infection. JAMA Ophthalmol. 2020;138(11):1196–9. https://doi.org/10.1001/jamaophthalmol.2020.3906.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Han Y, Ning W, Zhu W, Li Y, Zuo L, Ye J, Qiu Z, Xie J, Li T. Detection of HIV-1 viruses in tears of patients even under long-term HAART. AIDS. 2011;25(15):1925–7. https://doi.org/10.1097/QAD.0b013e32834b3578.

    Article  PubMed  Google Scholar 

  11. Reinhold A, Tzankov A, Matter M, Mihic-Probst D, Scholl HPN, Meyer P. Ocular pathology and occasionally detectable intraocular SARS-CoV-2 RNA in five fatal COVID-19 cases. Ophthalmic Res. 2021;64:785–92. https://doi.org/10.1159/000514573.

    Article  CAS  PubMed  Google Scholar 

  12. Jidigam VK, Singh R, Batoki JC, Milliner C, Sawant OB, Bonilha VL, Rao S. Histopathological assessments reveal retinal vascular changes, inflammation and gliosis in patients with lethal COVID-19. MedRxiv. 2021. https://doi.org/10.1101/2021.02.25.21251531.

  13. Arora R, Goel R, Kumar S, Chhabra M, Saxena S, Manchanda V, Pumma P. Evaluation of SARS-CoV-2 in tears of patients with moderate to severe COVID-19. Ophthalmology. 2021;128(4):494–503. https://doi.org/10.1016/j.ophtha.2020.08.029.

    Article  PubMed  Google Scholar 

  14. Yan Y, Zeng B, Zhang Z, Cheng H, Yan M, Li B, Zhang X, Chen X. Detection of SARS-CoV-2 in simultaneously collected tear and throat swab samples from the patients with 2019- new SARS-CoV-2 infection disease: a single center cross-sectional study. Ophthalmic Epidemiol. 2021;28(5):369–75. https://doi.org/10.1080/09286586.2021.1875011.

    Article  CAS  PubMed  Google Scholar 

  15. Chen L, Deng C, Chen X, Zhang X, Chen B, Huimin Y, Qin Y, Xiao K, Zhang H, Sun X. Ocular manifestations and clinical characteristics of 535 cases of COVID-19 in Wuhan, China: a cross-sectional study. Acta Ophthalmol. 2020;98(8):e951–9. https://doi.org/10.1111/aos.14472.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Güemes-Villahoz N, Burgos-Blasco B, Arribi-Vilela A, Arriola-Villalobos P, Rico-Luna CM, Cuiña-Sardiña R, Delgado-Iribarren A, García-Feijoó J. Detecting SARS-CoV-2 RNA in conjunctival secretions: is it a valuable diagnostic method of COVID-19? J Med Virol. 2021;93(1):383–8. https://doi.org/10.1002/jmv.26219.

    Article  CAS  PubMed  Google Scholar 

  17. Kocamış Ö, Örnek K, Aşıkgarip N, Hızmalı L, Sezgin FM, Şahin Y. Evaluation of nasopharyngeal and conjunctival swab samples of hospitalised patients with confirmed COVID-19. Ocul Immunol Inflamm. 2021;29:1–4. https://doi.org/10.1080/09273948.2020.1838558.

    Article  CAS  Google Scholar 

  18. Li M, Yang Y, He T, Wei R, Shen Y, Qi T, Han T, et al. Detection of SARS-CoV-2 in the ocular surface in different phases of COVID-19 patients in Shanghai, China. Ann Transl Med. 2021;9(2):100. https://doi.org/10.21037/atm-20-6026.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Savastano MC, Gambini G, Savastano A, Falsini B, De Vico U, Sanguinetti M, Cattani P, et al. Evidence-based of conjunctival COVID-19 positivity: an Italian experience: Gemelli against COVID group. Eur J Ophthalmol. 2021;31(6):2886–93. https://doi.org/10.1177/1120672120976548.

    Article  PubMed  Google Scholar 

  20. Seah I, Agrawal R. Can the coronavirus disease 2019 (COVID-19) affect the eyes? A review of coronaviruses and ocular implications in humans and animals. Ocul Immunol Inflamm. 2020;28(3):391–5. https://doi.org/10.1080/09273948.2020.1738501.

    Article  CAS  PubMed  Google Scholar 

  21. Zhang X, Chen X, Chen L, Deng C, Zou X, Liu W, Huimin Y, Chen B, Sun X. The evidence of SARS-CoV-2 infection on ocular surface. Ocul Surf. 2020;18(3):360–2. https://doi.org/10.1016/j.jtos.2020.03.010.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Zhou Y, Duan C, Zeng Y, Tong Y, Nie Y, Yang Y, Chen Z, Chen C. Ocular findings and proportion with conjunctival SARS-COV-2 in COVID-19 patients. Ophthalmology. 2020;127(7):982–3. https://doi.org/10.1016/j.ophtha.2020.04.028.

    Article  PubMed  Google Scholar 

  23. Loffredo L, Pacella F, Pacella E, Tiscione G, Oliva A, Violi F. Conjunctivitis and COVID-19: a meta-analysis. J Med Virol. 2020;92(9):1413–4. https://doi.org/10.1002/jmv.25938.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Cheema M, Aghazadeh H, Nazarali S, Ting A, Hodges J, McFarlane A, Kanji JN, Zelyas N, Damji KF, Solarte C. Keratoconjunctivitis as the initial medical presentation of the novel coronavirus disease 2019 (COVID-19). Can J Ophthalmol. 2020;55(4):e125–9. https://doi.org/10.1016/j.jcjo.2020.03.003.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Montesel A, Bucolo C, Mouvet V, Moret E, Eandi CM. Case report: central retinal artery occlusion in a COVID-19 patient. Front Pharmacol. 2020;11(December):2149. https://doi.org/10.3389/fphar.2020.588384.

    Article  CAS  Google Scholar 

  26. Bapaye MM, Nair AG, Bapaye CM, Bapaye MM, Shukla JJ. Simultaneous bilateral central retinal artery occlusion following COVID-19 infection. Ocul Immunol Inflamm. 2021;29(4):671–4. https://doi.org/10.1080/09273948.2021.1891262.

    Article  CAS  PubMed  Google Scholar 

  27. Murchison AP, Sweid A, Dharia R, Theofanis TN, Tjoumakaris SI, Jabbour PM, Bilyk JR. Monocular visual loss as the presenting symptom of COVID-19 infection. Clin Neurol Neurosurg. 2021;201:106440. https://doi.org/10.1016/j.clineuro.2020.106440.

    Article  PubMed  Google Scholar 

  28. Finn AP, Khurana RN, Chang LK. Hemi-retinal vein occlusion in a young patient with COVID-19. Am J Ophthalmol Case Rep. 2021;22(June):101046. https://doi.org/10.1016/j.ajoc.2021.101046.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Bakhoum MF, Bailey Freund K, Dolz-Marco R, Leong BCS, Baumal CR, Duker JS, Sarraf D. Paracentral acute middle maculopathy and the ischemic Cascade associated with retinal vascular occlusion. Am J Ophthalmol. 2018;195(November):143–53. https://doi.org/10.1016/j.ajo.2018.07.031.

    Article  PubMed  Google Scholar 

  30. Moura-Coelho N, Gaspar T, Ferreira JT, Dutra-Medeiros M, Cunha JP. Paracentral acute middle maculopathy—review of the literature. Graefes Arch Clin Exp Ophthalmol. 2020;258(12):2583–96. https://doi.org/10.1007/s00417-020-04826-1.

    Article  PubMed  Google Scholar 

  31. Padhy SK, Dcruz RP, Kelgaonkar A. Paracentral acute middle maculopathy following SARS-CoV-2 infection: the D-dimer hypothesis. BMJ Case Rep. 2021;14(3):e242043. https://doi.org/10.1136/bcr-2021-242043.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Turedi N, Onal Gunay B. Paracentral acute middle maculopathy in the setting of central retinal artery occlusion following COVID-19 diagnosis. Eur J Ophthalmol. 2021;32(3):NP62–6. https://doi.org/10.1177/1120672121995347.

    Article  PubMed  Google Scholar 

  33. Giacuzzo C, Eandi CM, Kawasaki A. Bilateral acute macular neuroretinopathy following COVID-19 infection. Acta Ophthalmol. 2022;100(2):e611–2. https://doi.org/10.1111/aos.14913.

    Article  CAS  PubMed  Google Scholar 

  34. Tan BK, Mainbourg S, Friggeri A, Bertoletti L, Douplat M, Dargaud Y, Grange C, Lobbes H, Provencher S, Lega JC. Arterial and venous thromboembolism in COVID-19: a study-level meta-analysis. Thorax. 2021:76, 1–10. https://doi.org/10.1136/thoraxjnl-2020-215383.

  35. Souza EC, De VE, Campos D, Duker JS. Atypical unilateral multifocal choroiditis in a COVID-19 positive patient. Am J Ophthalmol Case Rep. 2021;22:101034. https://doi.org/10.1016/j.ajoc.2021.101034.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Žorić L, Rajović-Mrkić I, Čolak E, Mirić D, Kisić B. Optic neuritis in a patient with seropositive myelin oligodendrocyte glycoprotein antibody during the post-COVID-19 period. Int Med Case Rep J. 2021;14:349–55. https://doi.org/10.2147/IMCRJ.S315103.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Benito-Pascual B, Gegúndez JA, Díaz-Valle D, Arriola-Villalobos P, Carreño E, Culebras E, Rodríguez-Avial I, Benitez-Del-Castillo JM. Panuveitis and optic neuritis as a possible initial presentation of the novel coronavirus disease 2019 (COVID-19). Ocul Immunol Inflamm. 2020;28(6):922–5. https://doi.org/10.1080/09273948.2020.1792512.

    Article  CAS  PubMed  Google Scholar 

  38. Sawalha K, Adeodokun S, Kamoga GR. COVID-19-induced acute bilateral optic neuritis. J Investig Med High Impact Case Rep. 2020;8:2324709620976018. https://doi.org/10.1177/2324709620976018.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Rodrigo-Armenteros P, Uterga-Valiente JM, Zabala-Del-Arco J, Taramundi-Argüeso S, Antón-Méndez L, Gómez-Muga JJ, Garcia-Monco JC. Optic neuropathy in a patient with COVID-19 infection. Acta Neurol Belg. 2022;122(3):789–91. https://doi.org/10.1007/s13760-021-01600-w.

    Article  PubMed  Google Scholar 

  40. Shaw VC, Chander G, Puttanna A. Neuromyelitis optica spectrum disorder secondary to COVID-19. Br J Hosp Med. 2020;81(9):1–3. https://doi.org/10.12968/hmed.2020.0401.

    Article  Google Scholar 

  41. Zhou S, Jones-Lopez EC, Soneji DJ, Azevedo CJ, Patel VR. Myelin oligodendrocyte glycoprotein antibody-associated optic neuritis and myelitis in COVID-19. J Neuroophthalmol. 2020;40(3):398–402. https://doi.org/10.1097/WNO.0000000000001049.

    Article  PubMed  Google Scholar 

  42. Corrêa DG, Hygino LC, da Cruz F, Lopes CR, de Carvalho C, Rangel AL, de Tessarollo AH, Coelho KCG, Brandão RZ, et al. Magnetic resonance imaging features of COVID-19-related cranial nerve lesions. J Neurovirol. 2021;27(1):171–7. https://doi.org/10.1007/s13365-020-00934-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Kogure C, Kikushima W, Fukuda Y, Hasebe Y, Takahashi T, Shibuya T, Sakurada Y, Kashiwagi K. Myelin oligodendrocyte glycoprotein antibody-associated optic neuritis in a COVID-19 patient: a case report. Medicine. 2021;100(19):e25865. https://doi.org/10.1097/MD.0000000000025865.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Rodríguez-Rodríguez MS, Romero-Castro RM, Alvarado-de C, la Barrera M, González-Cannata G, García-Morales AK, Ávila-Ríos S. Optic neuritis following SARS-CoV-2 infection. J Neurovirol. 2021;27(2):359–63. https://doi.org/10.1007/s13365-021-00959-z.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Burgos-Blasco B, Güemes-Villahoz N, Donate-Lopez J, Vidal-Villegas B, García-Feijóo J. Optic nerve analysis in COVID-19 patients. J Med Virol. 2021;93(1):190–1. https://doi.org/10.1002/jmv.26290.

    Article  CAS  PubMed  Google Scholar 

  46. Burgos-Blasco B, Güemes-Villahoz N, Vidal-Villegas B, Garcia-Feijoo J, Donate-Lopez J, Martin-Sanchez FJ, Gonzalez-Armengol JJ, Mendez-Hernandez CD. Optic nerve head vessel density assessment in recovered COVID-19 patients: a prospective study using optical coherence tomography angiography. J Glaucoma. 2021;30(8):711–7. https://doi.org/10.1097/IJG.0000000000001858.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Roussel A, Germanaud D, Bouchoucha Y, Ouldali N, Vedrenne-Cloquet M, Castelle M, Baruchel A. Cranial polyneuropathy as the first manifestation of a severe COVID-19 in a child. Pediatr Blood Cancer. 2021;68(3):e28707. https://doi.org/10.1002/pbc.28707.

    Article  CAS  PubMed  Google Scholar 

  48. Belghmaidi S, Nassih H, Boutgayout S, El Fakiri K, El Qadiri R, Hajji I, Bourahouate A, Moutaouakil A. Third cranial nerve palsy presenting with unilateral diplopia and strabismus in a 24-year-old woman with COVID-19. Am J Case Rep. 2020;21:1–5. https://doi.org/10.12659/AJCR.925897.

    Article  Google Scholar 

  49. Douedi S, Naser H, Mazahir U, Hamad AI, Sedarous M. Third cranial nerve palsy due to COVID-19 infection. Cureus. 2021;13(4):e14280. https://doi.org/10.7759/cureus.14280.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Fitzpatrick JC, Comstock JM, Longmuir RA, Donahue SP, Fitzpatrick JM, Bond JB. Cranial nerve III palsy in the setting of COVID 19 infection. J Neuroophthalmol. 2021;41(3):e286–7. https://doi.org/10.1097/WNO.0000000000001160.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Lonardi V, Meneghesso D, Debertolis G, Pin JN, Nosadini M, Sartori S. Isolated third cranial nerve palsy and COVID-19 infection in a child. Pediatr Neurol. 2021. https://doi.org/10.1016/j.pediatrneurol.2021.03.011.

  52. Oliveira MR, De AR, Lucena VP, Higino TMM, Ventura CV. Oculomotor nerve palsy in an asymptomatic child with COVID-19. J AAPOS. 2021;25(3):169–70. https://doi.org/10.1016/j.jaapos.2021.02.001.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Pascual-Prieto J, Narváez-Palazón C, Porta-Etessam J, Gómez-de-Liaño R. COVID-19 epidemic: should ophthalmologists be aware of oculomotor paresis? Arch Soc Esp Oftalmol. 2020;95(7):361–2. https://doi.org/10.1016/j.oftal.2020.05.002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Falcone MM, Rong AJ, Humberto Salazar D, Redick W, Falcone S, Cavuoto KM. Acute Abducens nerve palsy in a patient with the novel coronavirus disease (COVID-19). J AAPOS. 2020;24(4):216–7. https://doi.org/10.1016/j.jaapos.2020.06.001.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Greer CE, Bhatt JM, Oliveira CA, Dinkin MJ. Isolated cranial nerve 6 palsy in 6 patients with COVID-19 infection. J Neuroophthalmol. 2020;40(4):520–2. https://doi.org/10.1097/WNO.0000000000001146.

    Article  PubMed  Google Scholar 

  56. Pascual-Goñi E, Fortea J, Martínez-Domeño A, Rabella N, Tecame M, Gómez-Oliva C, Querol L, Gómez-Ansón B. COVID-19-associated Ophthalmoparesis and hypothalamic involvement. Neurol Neuroimmunol Neuroinflamm. 2020;7(5):e823. https://doi.org/10.1212/NXI.0000000000000823.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Vasanthpuram VH, Badakere A. Internuclear Ophthalmoplegia as a presenting feature in a COVID-19-positive patient. BMJ Case Rep. 2021;14(4):e241873. https://doi.org/10.1136/bcr-2021-241873.

    Article  PubMed Central  Google Scholar 

  58. Costello F, Dalakas MC. Cranial neuropathies and COVID-19: neurotropism and autoimmunity. Neurology. 2020;95(5):195–6. https://doi.org/10.1212/WNL.0000000000009921.

    Article  CAS  PubMed  Google Scholar 

  59. Al Othman B, Raabe J, Kini A, Lee AG. Update: the miller fisher variants of Guillain-Barré syndrome. Curr Opin Ophthalmol. 2019;30(6):462–6. https://doi.org/10.1097/ICU.0000000000000611.

    Article  PubMed  Google Scholar 

  60. Teener JW. Miller Fisher’s syndrome. Semin Neurol. 2012;32(5):512–6. https://doi.org/10.1055/s-0033-1334470.

    Article  PubMed  Google Scholar 

  61. Mori M, Kuwabara S, Fukutake T, Yuki N, Hattori T. Clinical features and prognosis of miller fisher syndrome. Neurology. 2001;56(8):1104–6. https://doi.org/10.1212/WNL.56.8.1104.

    Article  CAS  PubMed  Google Scholar 

  62. Gutiérrez-Ortiz C, Méndez-Guerrero A, Rodrigo-Rey S, Pedro-Murillo ES, Bermejo-Guerrero L, Gordo-Mañas R, de Aragón-Gómez F, Benito-León J. Miller fisher syndrome and polyneuritis Cranialis in COVID-19. Neurology. 2020;95(5):e601–5. https://doi.org/10.1212/WNL.0000000000009619.

    Article  CAS  PubMed  Google Scholar 

  63. Lantos JE, Strauss SB, Lin E. COVID-19-associated miller fisher syndrome: MRI findings. Am J Neuroradiol. 2020;41(7):1184–6. https://doi.org/10.3174/AJNR.A6609.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Reyes-Bueno JA, García-Trujillo L, Urbaneja P, Ciano-Petersen NL, Postigo-Pozo MJ, Martínez-Tomás C, Serrano-Castro PJ. Miller-fisher syndrome after SARS-CoV-2 infection. Eur J Neurol. 2020;27(9):1759–61. https://doi.org/10.1111/ene.14383.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Manganotti P, Bellavita G, D’Acunto L, Tommasini V, Fabris M, Sartori A, Bonzi L, Stella AB, Pesavento V. Clinical neurophysiology and cerebrospinal liquor analysis to detect Guillain-Barré syndrome and polyneuritis Cranialis in COVID-19 patients: a case series. J Med Virol. 2021;93(2):766–74. https://doi.org/10.1002/jmv.26289.

    Article  CAS  PubMed  Google Scholar 

  66. Ray A. Miller fisher syndrome and COVID-19: is there a link? BMJ Case Rep. 2020;13(8):e236419. https://doi.org/10.1136/bcr-2020-236419.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Senel M, Abu-Rumeileh S, Michel D, Garibashvili T, Althaus K, Kassubek J, Otto M. Miller-fisher syndrome after COVID-19: neurochemical markers as an early sign of nervous system involvement. Eur J Neurol. 2020;27(11):2378–80. https://doi.org/10.1111/ene.14473.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Fernández-Domínguez J, Ameijide-Sanluis E, García-Cabo C, García-Rodríguez R, Mateos V. Miller–fisher-like syndrome related to SARS-CoV-2 infection (COVID 19). J Neurol. 2020;267(9):2495–6. https://doi.org/10.1007/s00415-020-09912-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Lowery MM, Malik MT, Seemiller J, Tsai CS. Atypical variant of Guillain Barre syndrome in a patient with COVID-19. J Crit Care Med. 2020;6(4):231–6. https://doi.org/10.2478/jccm-2020-0038.

    Article  Google Scholar 

  70. Abu-Rumeileh S, Abdelhak A, Foschi M, Tumani H, Otto M. Guillain–Barré syndrome spectrum associated with COVID-19: an up-to-date systematic review of 73 cases. J Neurol. 2021;268(4):1133–70. https://doi.org/10.1007/s00415-020-10124-x.

    Article  CAS  PubMed  Google Scholar 

  71. Sansone P, Giaccari LG, Aurilio C, Coppolino F, Esposito V, Fiore M, Paladini A, Passavanti MB, Pota V, Pace MC. Post-infectious Guillain–Barré syndrome related to Sars-Cov-2 infection: a systematic review. Life. 2021;11(2):167. https://doi.org/10.3390/life11020167.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Sheikh AB, Chourasia PK, Javed N, Chourasia MK, Suriya SS, Upadhyay S, Ijaz F, Pal S, Moghimi N, Shekhar R. Association of Guillain-Barre Syndrome with COVID-19 infection: an updated systematic review. J Neuroimmunol. 2021;355:577577. https://doi.org/10.1016/j.jneuroim.2021.577577.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Li Z, Li X, Shen J, Chan MTV, Wu WKK. Miller fisher syndrome associated with COVID-19: an up-to-date systematic review. Environ Sci Pollut Res. 2021;28(17):20939–44. https://doi.org/10.1007/s11356-021-13233-w.

    Article  CAS  Google Scholar 

  74. De Arrigunaga S, Aziz K, Lorch AC, Friedman DS, Armstrong GW. A review of ophthalmic telemedicine for emergency department settings. Semin Ophthalmol. 2022;37:1–8. https://doi.org/10.1080/08820538.2021.1922712.

    Article  Google Scholar 

  75. McAnany JJ, Smith BM, Garland A, Kagen SL. IPhone-based pupillometry: a novel approach for assessing the pupillary light reflex. Optom Vis Sci. 2018;95(10):953–8. https://doi.org/10.1097/OPX.0000000000001289.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Newman-Casey PA, De Lott L, Cho J, Ballouz D, Azzouz L, Saleh S, Woodward MA. Telehealth-based eye care during the COVID-19 pandemic: utilization, safety and the patient experience. Am J Ophthalmol. 2021;230:234–42. https://doi.org/10.1016/j.ajo.2021.04.014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Arntz A, Khaliliyeh D, Cruzat A, Rao X, Rocha G, Grau A, Altschwager P, Azócar V. Open-care telemedicine in ophthalmology during the COVID-19 pandemic: a pilot study. Arch Soc Esp Oftalmol. 2020;95(12):586–90. https://doi.org/10.1016/j.oftal.2020.09.005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Golash V, Athwal S, Khandwala M. Teleophthalmology and COVID-19: the patient perspective. Future Healthc J. 2021;8(1):e54–9. https://doi.org/10.7861/fhj.2020-0139.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Kalavar M, Hua HU, Sridhar J. Teleophthalmology: an essential tool in the era of the novel coronavirus 2019. Curr Opin Ophthalmol. 2020;31(5):366–73. https://doi.org/10.1097/ICU.0000000000000689.

    Article  PubMed  Google Scholar 

  80. Kilduff CLS, Thomas AAP, Dugdill J, Casswell EJ, Dabrowski M, Lovegrove C, Sim DA, Hay GR, Thomas PBM. Creating the Moorfields’ virtual eye casualty: video consultations to provide emergency teleophthalmology care during and beyond the COVID-19 pandemic. BMJ Health Care Informat. 2020;27(3):e100179. https://doi.org/10.1136/bmjhci-2020-100179.

    Article  Google Scholar 

  81. Donegani MI, Miceli A, Pardini M, Bauckneht M, Chiola S, Pennone M, Marini C, et al. Brain metabolic correlates of persistent olfactory dysfunction after SARS-Cov2 infection. Biomedicine. 2021;9(3):287. https://doi.org/10.3390/biomedicines9030287.

    Article  CAS  Google Scholar 

  82. Guedj E, Campion JY, Dudouet P, Kaphan E, Bregeon F, Tissot-Dupont H, Guis S, et al. 18F-FDG brain PET Hypometabolism in patients with long COVID. Eur J Nucl Med Mol Imaging. 2021;48:1–11. https://doi.org/10.1007/s00259-021-05215-4.

    Article  CAS  Google Scholar 

  83. Sollini M, Morbelli S, Ciccarelli M, Cecconi M, Aghemo A, Morelli P, Chiola S, Gelardi F, Chiti A. Long COVID hallmarks on [18F]FDG-PET/CT: a case-control study. Eur J Nucl Med Mol Imaging. 2021;48(10):3187–97. https://doi.org/10.1007/s00259-021-05294-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

All the authors are thankful to their teammates and collaborators. They also thank all health workers around the world who are dealing with this pandemic; all the authors express their deepest condolences and offer a heartfelt thanks to all colleagues fallen fighting against this invisible enemy, as well as to their families.

Funding

This research received no external funding.

Disclosure Statement

E.P., R.A., G.K.W., I.A.I., and F.L. declare no conflict of interest, and do not receive any financial aid. B.D.M. is supported to conduct COVID-19 neuroscience research by the UKRI/MRC (MR/V03605X/1); for additional neurological inflammation research due to viral infection B.D.M. is also supported by grants from the MRC/UKRI (MR/V007181//1), MRC (MR/T028750/1), and Wellcome (ISSF201902/3).

Author Contributions

Conceptualization: E.P., R.A., B.D.M. and F.L.; literature research, screening, and selection: E.P., R.A., G.K.W. and I.A.I.; original draft preparation: E.P. and F.L.; review: G.K.W. and I.A.I.; writing and editing: all authors.

All authors have read and approved the definitive version of the manuscript.

Author information

Authors and Affiliations

  1. Ophthalmology Unit, ASST Sette Laghi, Circolo Hospital and Macchi Foundation, Varese, Italy

    Elias Premi

  2. Department of Biotechnologies and Life Sciences, University of Insubria, Varese, Italy

    Elias Premi

  3. Milan Center for Neuroscience (NeuroMI), Milan, Italy

    Roberto Acampora

  4. Neurology and Stroke-Unit, Hospital Ospedale del Mare, Naples, Italy

    Roberto Acampora

  5. Department of Neurology, The Walton Centre NHS Foundation Trust, Liverpool, UK

    Greta Karen Wood & Benedict Daniel Michael

  6. Clinical Infection Microbiology and Neuroimmunology, Institute of Infection, Veterinary and Ecological Science, Liverpool, UK

    Greta Karen Wood & Benedict Daniel Michael

  7. The NIHR Health Protection Research Unit for Emerging and Zoonotic Infection, Liverpool, UK

    Greta Karen Wood & Benedict Daniel Michael

  8. Department of Life Sciences and Biotechnology, School of Biology, University of Ferrara, Ferrara, Italy

    Ingrid Andreea Ilie

  9. Department of Health Sciences (DISSAL), University of Genoa, Genoa, Italy

    Francesco Lanfranchi

Authors
  1. Elias Premi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roberto Acampora
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Greta Karen Wood
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ingrid Andreea Ilie
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Benedict Daniel Michael
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Francesco Lanfranchi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Francesco Lanfranchi .

Editor information

Editors and Affiliations

  1. School of Information Technology, Deakin University, Melbourne, VIC, Australia

    Sasan Adibi

  2. School of Medicine, University of Queensland, Brisbane, QLD, Australia

    Paul Griffin

  3. Clinical - Vaccines, Clover Biopharmaceuticals, Zürich, Switzerland

    Melvin Sanicas

  4. Inflammation Division, Walter and Eliza Hall Institute of Medical Research, Melbourne, VIC, Australia

    Maryam Rashidi

  5. Department of Health Sciences (DISSAL), University of Genoa, Genoa, Italy

    Francesco Lanfranchi

Rights and permissions

Reprints and permissions

Copyright information

© 2022 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Premi, E., Acampora, R., Wood, G.K., Ilie, I.A., Michael, B.D., Lanfranchi, F. (2022). Eye Disorders and Neuro-ophthalmic Manifestations of COVID-19. In: Adibi, S., Griffin, P., Sanicas, M., Rashidi, M., Lanfranchi, F. (eds) Frontiers of COVID-19. Springer, Cham. https://doi.org/10.1007/978-3-031-08045-6_12

Download citation

  • DOI: https://doi.org/10.1007/978-3-031-08045-6_12

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-031-08044-9

  • Online ISBN: 978-3-031-08045-6

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Search

Navigation