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Yvon C, Patel B, Ng J, Altman M, Malhotra R. Oculoplastic Conditions in Covid-19 Patients: Case Series and Literature Review. JOVR [Internet]. 2024Jun.21 [cited 2024Jun.30];19(2):235–245. Available from: https://knepublishing.com/index.php/JOVR/article/view/10908
https://doi.org/10.18502/jovr.v19i2.10908
statistics
- 11 Abstract Views
- 15 PDF Views
authors
-
Camille Yvon
Camille Yvon
Corneoplastic unit, Queen Victoria Hospital NHS Trust, East Grinstead, Sussex, United Kingdom
-
Bhupendra Patel
Bhupendra Patel
Moran Eye Center, University of Utah, Salt Lake City, Utah, United States
-
John Ng
John Ng
Casey Eye Institute, Oregon Health and Science University, Portland, Oregon, United States
-
Marcus T Altman
Marcus T Altman
Casey Eye Institute, Oregon Health and Science University, Portland, Oregon, United States
-
Raman Malhotra
Raman Malhotra
Corneoplastic unit, Queen Victoria Hospital NHS Trust, East Grinstead, Sussex, United Kingdom
Published Date
- Jun 21, 2024
Oculoplastic Conditions in Covid-19 Patients: Case Series and Literature Review
Abstract
Purpose: To investigate oculoplastic conditions in patients diagnosed with coronavirus disease 2019 (COVID-19) seen at ophthalmology departments of three tertiary referral centers in the United Kingdom and the United States, and review of the literature.
Methods: Retrospective multicenter case series studied over 18 months.
Results: A total of four patients developed eyelid, orbital, or lacrimal gland pathology within four weeks of testing positive for COVID-19. All were male, and the mean age at presentation was 49 (range, 31–58 years). Suspected diagnoses included anterior idiopathic orbital inflammation, facial angioedema, dacryoadenitis, and anophthalmic socket inflammation. Three patients recovered fully and one patient recovered partially (mean 2.7 weeks) from ocular manifestations with steroids hastening recovery.
Conclusion: Adnexal manifestations of COVID-19 include self-limiting orbital inflammation and eyelid lymphedema.
Keywords:
Case Studies, Coronavirus, Eyelid Disease, Inflammation, Orbital Disease
References
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17. Adeliño R, Andrés-Cordón JF, Aracelis De La Cruz Martínez C. Acute urticaria with angioedema in the setting of coronavirus disease 2019. J Allergy Clin Immunol Pract 2020;8:2386–2387.
18. Hassan K. Urticaria and angioedema as a prodromal cutaneous manifestation of SARS-CoV-2 (COVID-19) infection. BMJ Case Rep 2020;13:e236981.
19. Azmy V, Benson J, Love K, Steele R. Idiopathic nonhistaminergic acquired angioedema in a patient with coronavirus disease 2019. Ann Allergy Asthma Immunol. 2020;125:600–602.
20. Armstrong BK, Murchison AP, Bilyk JR. Suspected orbital myositis associated with COVID-19. Orbit 2021;40:532–535.
21. Bostanci Ceran B, Ozates S. Ocular manifestations of coronavirus disease 2019. Graefes Arch Clin Exp Ophthalmol 2020;258:1959–1963.
22. Martínez Díaz M, Copete Piqueras S, Blanco Marchite C, Vahdani K. Acute dacryoadenitis in a patient with SARS-CoV-2 infection. Orbit 2021:1–4.
23. Turbin RE, Wawrzusin PJ, Sakla NM, Traba CM, Wong KG, Mirani N, et al. Orbital cellulitis, sinusitis and intracranial abnormalities in two adolescents with COVID-19. Orbit 2020;39:305–310.
24. Shires CB, Klug T, Dryden S, Ford J. Unusual cause of acute sinusitis and orbital abscess in COVID-19 positive patient: Case report. Int J Surg Case Rep 2021;79:164– 168.
25. Mekonnen ZK, Ashraf DC, Jankowski T, Grob SR, Vagefi MR, Kersten RC, et al. Acute invasive rhinoorbital mucormycosis in a patient with COVID-19- associated acute respiratory distress syndrome. Ophthalmic Plast Reconstr Surg 2021;37:e40–80.
26. Revannavar SM, PS S, Samaga L, v K V. COVID-19 triggering mucormycosis in a susceptible patient: a new phenomenon in the developing world? BMJ Case Rep 2021;14:e241663.
27. Werthman-Ehrenreich A. Mucormycosis with orbital compartment syndrome in a patient with COVID-19. Am J Emerg Med 2021;42:264.e5-.e8.
28. Selarka L, Sharma S, Saini D, Sharma S, Batra A, Waghmare VT, et al. Mucormycosis and COVID-19: An epidemic within a pandemic in India. Mycoses. 2021;64:1253–1260.
29. Raut A, Huy NT. Rising incidence of mucormycosis in patients with COVID-19: Another challenge for India amidst the second wave? Lancet Respir Med 2021;9:e77.
30. Patel A, Agarwal R, Rudramurthy SM, Shevkani M, Xess I, Sharma R, et al.; MucoCovi Network3. Multicenter epidemiologic study of coronavirus disease-associated mucormycosis, India. Emerg Infect Dis 2021;27:2349– 2359.
31. Al-Tawfiq JA, Alhumaid S, Alshukairi AN, Temsah MH, Barry M, Al Mutair A, et al. COVID-19 and mucormycosis superinfection: the perfect storm. Infection 2021;49:833–853.
32. Pakdel F, Zand A, Sharifi A, Asadi M, Abri Aghdam K. Challenges and pitfalls in the management of rhinoorbital mucormycosis in ophthalmology: A highlighted problem in the COVID-19 era. J Ophthalmic Vis Res 2022;17:424–431.
33. Chakrabarti A, Singh R. Mucormycosis in India: Unique features. Mycoses 2014;57:85–90.
34. Prakash H, Singh S, Rudramurthy SM, Singh P, Mehta N, Shaw D, et al. An aero mycological analysis of Mucormycetes in indoor and outdoor environments of northern India. Med Mycol 2020;58:118–123.
35. Prakash H, Ghosh AK, Rudramurthy SM, Paul RA, Gupta S, Negi V, et al. The environmental source of emerging Apophysomyces variabilis infection in India. Med Mycol 2016;54:567–575.
36. Prakash H, Chakrabarti A. Epidemiology of mucormycosis in India. Microorganisms 2021;9:523.
37. Sen M, Honavar SG, Bansal R, Sengupta S, Rao R, Kim U, et al.; members of the Collaborative OPAI-IJO Study on Mucormycosis in COVID-19 (COSMIC) Study Group. Epidemiology, clinical profile, management, and outcome of COVID-19-associated rhino-orbitalcerebral mucormycosis in 2826 patients in India - Collaborative OPAI-IJO Study on Mucormycosis in COVID-19 (COSMIC), Report 1. Indian J Ophthalmol 2021;69:1670–1692.
38. Singh AK, Singh R, Joshi SR, Misra A. Mucormycosis in COVID-19: A systematic review of cases reported worldwide and in India. Diabetes Metab Syndr 2021;15:102146.
39. Yan R, Zhang Y, Li Y, Xia L, Guo Y, Zhou Q. Structural basis for the recognition of SARS-CoV-2 by full-length human ACE2. Science 2020;367:1444–1448.
40. Cicardi M, Zuraw BL. Angioedema due to bradykinin dysregulation. J Allergy Clin Immunol Pract 2018;6:1132–1141.
41. Wedi B, Raap U, Wieczorek D, Kapp A. Urticaria and infections. Allergy Asthma Clin Immunol 2009;5:10.
42. Mehta P, McAuley DF, Brown M, Sanchez E, Tattersall RS, Manson JJ; HLH Across Speciality Collaboration, UK. COVID-19: Consider cytokine storm syndromes and immunosuppression. Lancet 2020;395:1033–1034.
43. Harrison AG, Lin T, Wang P. Mechanisms of SARSCoV- 2 transmission and pathogenesis. Trends Immunol 2020;41:1100–1015.
44. Yaguchi S, Ogawa Y, Shimmura S, Hatou S, Nakamura S, Inaba T, et al. Presence and physiologic function of the renin-angiotensin system in mouse lacrimal gland. Invest Ophthalmol Vis Sci 2012;53:5416–5425.
45. Shen J, Wu J, Yang Y, Wang P, Luo T, Guo Y, et al. The paradoxical problem with COVID-19 ocular infection: Moderate clinical manifestation and potential infection risk. Comput Struct Biotechnol J 2021;19:1063–1071.
46. Colavita F, Lapa D, Carletti F, Lalle E, Bordi L, Marsella P, 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;173:242–243.
47. Xie HT, Jiang SY, Xu KK, Liu X, Xu B, Wang L, et al. SARS-CoV-2 in the ocular surface of COVID-19 patients. Eye Vis 2020;7:23.
48. Deng W, Bao L, Gao H, Xiang Z, Qu Y, Song Z, et al. Ocular conjunctival inoculation of SARS-CoV- 2 can cause mild COVID-19 in Rhesus macaques. bioRxiv. 2020:2020.03.13.990036. https://doi.org/10. 1101/2020.03.13.990036
49. Cano EJ, Fonseca Fuentes X, Corsini Campioli C, O’Horo JC, Abu Saleh O, Odeyemi Y, et al. Impact of corticosteroids in coronavirus disease 2019 outcomes: Systematic review and meta-analysis. Chest 2021;159:1019–1040.
50. van Paassen J, Vos JS, Hoekstra EM, Neumann KM, Boot PC, Arbous SM. Corticosteroid use in COVID- 19 patients: A systematic review and meta-analysis on clinical outcomes. Crit Care 2020;24:696.
51. Horby P, Lim WS, Emberson JR, Mafham M, Bell JL, Linsell L, et al.; RECOVERY Collaborative Group. Dexamethasone in hospitalized patients with covid-19. N Engl J Med 2021;384:693–704.
52. Abtahi SH, Nouri H, Moradian S, Yazdani S, Ahmadieh H. Eye disorders in the post-COVID era. J Ophthalmic Vis Res 2021;16:527–530.
53. Shah W, Hillman T, Playford ED, Hishmeh L. Managing the long term effects of covid-19: summary of NICE, SIGN, and RCGP rapid guideline. BMJ 2021;372:n136.
54. Nalbandian A, Sehgal K, Gupta A, Madhavan MV, McGroder C, Stevens JS, et al. Post-acute COVID-19 syndrome. Nat Med 2021;27:601–615.
55. Novak P. Post COVID-19 syndrome associated with orthostatic cerebral hypoperfusion syndrome, small fiber neuropathy and benefit of immunotherapy: A case report. eNeurologicalSci 2020;21:100276.
56. Bitirgen G, Korkmaz C, Zamani A, Ozkagnici A, Zengin N, Ponirakis G, et al. Corneal confocal microscopy identifies corneal nerve fibre loss and increased dendritic cells in patients with long COVID. Br J Ophthalmol 2021.
2. Wang H, Paulson KR, Pease SA, Watson S, Comfort H, Zheng P, et al. COVID-19 excess mortality collaborators. estimating excess mortality due to the COVID-19 pandemic: A systematic analysis of COVID-19-related mortality, 2020-21. Lancet 2022;399:1513–1536.
3. Dong E, Du H, Gardner L. An interactive web-based dashboard to track COVID-19 in real time. Lancet Infect Dis 2020;20:533–534.
4. Johns Hopkins Coronavirus Resource Center [Internet]. 2022. Available from: https://coronavirus.jhu.edu
5. Bertoli F, Veritti D, Danese C, Samassa F, Sarao V, Rassu N, et al. Ocular findings in COVID-19 patients: A review of direct manifestations and indirect effects on the eye. J Ophthalmol 2020;2020:4827304.
6. Sen M, Honavar SG, Sharma N, Sachdev MS. COVID- 19 and eye: A review of ophthalmic manifestations of COVID-19. Indian J Ophthalmol 2021;69:488–509.
7. Wu P, Duan F, Luo C, Liu Q, Qu X, Liang L, et al. Characteristics of ocular findings of patients with coronavirus disease 2019 (COVID-19) in Hubei Province, China. JAMA Ophthalmol 2020;138:575– 578.
8. 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;16:103–112.
9. Ho D, Low R, Tong L, Gupta V, Veeraraghavan A, Agrawal R. COVID-19 and the ocular surface: A review of transmission and manifestations. Ocul Immunol Inflamm 2020;28:726–734.
10. Chen L, Deng C, Chen X, Zhang X, Chen B, Yu H, et al. Ocular manifestations and clinical characteristics of 535 cases of COVID-19 in Wuhan, China: A crosssectional study. Acta Ophthalmol 2020;98:e951–9.
11. Aggarwal K, Agarwal A, Jaiswal N, Dahiya N, Ahuja A, Mahajan S, et al. Ocular surface manifestations of coronavirus disease 2019 (COVID-19): A systematic review and meta-analysis. PLoS One 2020;15:e0241661.
12. Singh Y, Ganesh V, Kumar S, Patel N, Aggarwal R, Soni KD, et al. Coronavirus disease-associated mucormycosis from a tertiary care hospital in India: A case series. Cureus 2021;13:e16152.
13. Mishra Y, Prashar M, Sharma D, Akash, Kumar VP, Tilak TV. Diabetes, COVID 19 and mucormycosis: Clinical spectrum and outcome in a tertiary care medical center in Western India. Diabetes Metab Syndr 2021;15:102196.
14. Jose A, Singh S, Roychoudhury A, Kholakiya Y, Arya S, Roychoudhury S. Current understanding in the pathophysiology of SARS-CoV-2-associated rhinoorbito- cerebral mucormycosis: A comprehensive review. J Maxillofac Oral Surg 2021;20:373–380.
15. Pal P, Singh B, Singla S, Kaur R. Mucormycosis in COVID-19 pandemic and its neurovascular spread. Eur Arch Otorhinolaryngol 2021:1–8.
16. Cohen AJ, DiFrancesco MF, Solomon SD, Vaduganathan M. Angioedema in COVID-19. Eur Heart J 2020;41:3283–3284.
17. Adeliño R, Andrés-Cordón JF, Aracelis De La Cruz Martínez C. Acute urticaria with angioedema in the setting of coronavirus disease 2019. J Allergy Clin Immunol Pract 2020;8:2386–2387.
18. Hassan K. Urticaria and angioedema as a prodromal cutaneous manifestation of SARS-CoV-2 (COVID-19) infection. BMJ Case Rep 2020;13:e236981.
19. Azmy V, Benson J, Love K, Steele R. Idiopathic nonhistaminergic acquired angioedema in a patient with coronavirus disease 2019. Ann Allergy Asthma Immunol. 2020;125:600–602.
20. Armstrong BK, Murchison AP, Bilyk JR. Suspected orbital myositis associated with COVID-19. Orbit 2021;40:532–535.
21. Bostanci Ceran B, Ozates S. Ocular manifestations of coronavirus disease 2019. Graefes Arch Clin Exp Ophthalmol 2020;258:1959–1963.
22. Martínez Díaz M, Copete Piqueras S, Blanco Marchite C, Vahdani K. Acute dacryoadenitis in a patient with SARS-CoV-2 infection. Orbit 2021:1–4.
23. Turbin RE, Wawrzusin PJ, Sakla NM, Traba CM, Wong KG, Mirani N, et al. Orbital cellulitis, sinusitis and intracranial abnormalities in two adolescents with COVID-19. Orbit 2020;39:305–310.
24. Shires CB, Klug T, Dryden S, Ford J. Unusual cause of acute sinusitis and orbital abscess in COVID-19 positive patient: Case report. Int J Surg Case Rep 2021;79:164– 168.
25. Mekonnen ZK, Ashraf DC, Jankowski T, Grob SR, Vagefi MR, Kersten RC, et al. Acute invasive rhinoorbital mucormycosis in a patient with COVID-19- associated acute respiratory distress syndrome. Ophthalmic Plast Reconstr Surg 2021;37:e40–80.
26. Revannavar SM, PS S, Samaga L, v K V. COVID-19 triggering mucormycosis in a susceptible patient: a new phenomenon in the developing world? BMJ Case Rep 2021;14:e241663.
27. Werthman-Ehrenreich A. Mucormycosis with orbital compartment syndrome in a patient with COVID-19. Am J Emerg Med 2021;42:264.e5-.e8.
28. Selarka L, Sharma S, Saini D, Sharma S, Batra A, Waghmare VT, et al. Mucormycosis and COVID-19: An epidemic within a pandemic in India. Mycoses. 2021;64:1253–1260.
29. Raut A, Huy NT. Rising incidence of mucormycosis in patients with COVID-19: Another challenge for India amidst the second wave? Lancet Respir Med 2021;9:e77.
30. Patel A, Agarwal R, Rudramurthy SM, Shevkani M, Xess I, Sharma R, et al.; MucoCovi Network3. Multicenter epidemiologic study of coronavirus disease-associated mucormycosis, India. Emerg Infect Dis 2021;27:2349– 2359.
31. Al-Tawfiq JA, Alhumaid S, Alshukairi AN, Temsah MH, Barry M, Al Mutair A, et al. COVID-19 and mucormycosis superinfection: the perfect storm. Infection 2021;49:833–853.
32. Pakdel F, Zand A, Sharifi A, Asadi M, Abri Aghdam K. Challenges and pitfalls in the management of rhinoorbital mucormycosis in ophthalmology: A highlighted problem in the COVID-19 era. J Ophthalmic Vis Res 2022;17:424–431.
33. Chakrabarti A, Singh R. Mucormycosis in India: Unique features. Mycoses 2014;57:85–90.
34. Prakash H, Singh S, Rudramurthy SM, Singh P, Mehta N, Shaw D, et al. An aero mycological analysis of Mucormycetes in indoor and outdoor environments of northern India. Med Mycol 2020;58:118–123.
35. Prakash H, Ghosh AK, Rudramurthy SM, Paul RA, Gupta S, Negi V, et al. The environmental source of emerging Apophysomyces variabilis infection in India. Med Mycol 2016;54:567–575.
36. Prakash H, Chakrabarti A. Epidemiology of mucormycosis in India. Microorganisms 2021;9:523.
37. Sen M, Honavar SG, Bansal R, Sengupta S, Rao R, Kim U, et al.; members of the Collaborative OPAI-IJO Study on Mucormycosis in COVID-19 (COSMIC) Study Group. Epidemiology, clinical profile, management, and outcome of COVID-19-associated rhino-orbitalcerebral mucormycosis in 2826 patients in India - Collaborative OPAI-IJO Study on Mucormycosis in COVID-19 (COSMIC), Report 1. Indian J Ophthalmol 2021;69:1670–1692.
38. Singh AK, Singh R, Joshi SR, Misra A. Mucormycosis in COVID-19: A systematic review of cases reported worldwide and in India. Diabetes Metab Syndr 2021;15:102146.
39. Yan R, Zhang Y, Li Y, Xia L, Guo Y, Zhou Q. Structural basis for the recognition of SARS-CoV-2 by full-length human ACE2. Science 2020;367:1444–1448.
40. Cicardi M, Zuraw BL. Angioedema due to bradykinin dysregulation. J Allergy Clin Immunol Pract 2018;6:1132–1141.
41. Wedi B, Raap U, Wieczorek D, Kapp A. Urticaria and infections. Allergy Asthma Clin Immunol 2009;5:10.
42. Mehta P, McAuley DF, Brown M, Sanchez E, Tattersall RS, Manson JJ; HLH Across Speciality Collaboration, UK. COVID-19: Consider cytokine storm syndromes and immunosuppression. Lancet 2020;395:1033–1034.
43. Harrison AG, Lin T, Wang P. Mechanisms of SARSCoV- 2 transmission and pathogenesis. Trends Immunol 2020;41:1100–1015.
44. Yaguchi S, Ogawa Y, Shimmura S, Hatou S, Nakamura S, Inaba T, et al. Presence and physiologic function of the renin-angiotensin system in mouse lacrimal gland. Invest Ophthalmol Vis Sci 2012;53:5416–5425.
45. Shen J, Wu J, Yang Y, Wang P, Luo T, Guo Y, et al. The paradoxical problem with COVID-19 ocular infection: Moderate clinical manifestation and potential infection risk. Comput Struct Biotechnol J 2021;19:1063–1071.
46. Colavita F, Lapa D, Carletti F, Lalle E, Bordi L, Marsella P, 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;173:242–243.
47. Xie HT, Jiang SY, Xu KK, Liu X, Xu B, Wang L, et al. SARS-CoV-2 in the ocular surface of COVID-19 patients. Eye Vis 2020;7:23.
48. Deng W, Bao L, Gao H, Xiang Z, Qu Y, Song Z, et al. Ocular conjunctival inoculation of SARS-CoV- 2 can cause mild COVID-19 in Rhesus macaques. bioRxiv. 2020:2020.03.13.990036. https://doi.org/10. 1101/2020.03.13.990036
49. Cano EJ, Fonseca Fuentes X, Corsini Campioli C, O’Horo JC, Abu Saleh O, Odeyemi Y, et al. Impact of corticosteroids in coronavirus disease 2019 outcomes: Systematic review and meta-analysis. Chest 2021;159:1019–1040.
50. van Paassen J, Vos JS, Hoekstra EM, Neumann KM, Boot PC, Arbous SM. Corticosteroid use in COVID- 19 patients: A systematic review and meta-analysis on clinical outcomes. Crit Care 2020;24:696.
51. Horby P, Lim WS, Emberson JR, Mafham M, Bell JL, Linsell L, et al.; RECOVERY Collaborative Group. Dexamethasone in hospitalized patients with covid-19. N Engl J Med 2021;384:693–704.
52. Abtahi SH, Nouri H, Moradian S, Yazdani S, Ahmadieh H. Eye disorders in the post-COVID era. J Ophthalmic Vis Res 2021;16:527–530.
53. Shah W, Hillman T, Playford ED, Hishmeh L. Managing the long term effects of covid-19: summary of NICE, SIGN, and RCGP rapid guideline. BMJ 2021;372:n136.
54. Nalbandian A, Sehgal K, Gupta A, Madhavan MV, McGroder C, Stevens JS, et al. Post-acute COVID-19 syndrome. Nat Med 2021;27:601–615.
55. Novak P. Post COVID-19 syndrome associated with orthostatic cerebral hypoperfusion syndrome, small fiber neuropathy and benefit of immunotherapy: A case report. eNeurologicalSci 2020;21:100276.
56. Bitirgen G, Korkmaz C, Zamani A, Ozkagnici A, Zengin N, Ponirakis G, et al. Corneal confocal microscopy identifies corneal nerve fibre loss and increased dendritic cells in patients with long COVID. Br J Ophthalmol 2021.