The Effects of the COVID-19 Pandemic on the Follow-Up of Patients with Age-Related Macular Degeneration in a Tertiary Hospital in London, the UK
Abstract
1. Introduction
2. Materials and Methods
- No-Delay Group: This group comprised patients who strictly adhered to their scheduled appointments. For analysis, two specific time points were selected—the last appointment before the first London lockdown (23 March–30 August 2020) and the first appointment following this period.
- Delay Group: This group included patients who either missed, refused, or postponed their medical appointments due to fear of COVID-19 infection. For these patients, the last appointment before the first lockdown (23 March–30 August 2020) and the first appointment during the recovery phase were selected for analysis.
2.1. Patient Inclusion
2.2. Inclusion and Exclusion Criteria
- Confirmed diagnosis of AMD with at least one visit before March 2020, during which a macular optical coherence tomography (OCT) scan was performed.
- Having had at least one face-to-face appointment between June 2020 and September 2021.
- Having had at least one macular OCT scan conducted during the “recovery phase” of the COVID-19 pandemic.
- Missed or delayed at least one scheduled face-to-face appointment in the macula clinical unit due to concerns about COVID-19 infection during the first lockdown.
- No AMD diagnosis (e.g., patients followed up for other macular diseases such as branch retinal vein occlusion or diabetic macular oedema).
- Follow-up conducted in another ophthalmology centre.
- The presence of other ocular or systemic conditions that could negatively influence disease progression.
2.3. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
AMD | Age-related macular degeneration |
BCVA | Best corrected visual acuity |
OCT | Optical coherence tomography |
References
- Zhu, H.; Wei, L.; Niu, P. The Novel Coronavirus Outbreak in Wuhan, China. Glob. Health Res. Policy 2020, 5, 6. [Google Scholar] [CrossRef] [PubMed]
- Flynn, D.; Moloney, E.; Bhattarai, N.; Scott, J.; Breckons, M.; Avery, L.; Moy, N. COVID-19 Pandemic in the United Kingdom. Health Policy Technol. 2020, 9, 673–691. [Google Scholar] [CrossRef] [PubMed]
- Wang, W.; Xu, Y.; Gao, R.; Lu, R.; Han, K.; Wu, G.; Tan, W. Detection of SARS-CoV-2 in Different Types of Clinical Specimens. J. Am. Med. Assoc. 2020, 323, 1843–1844. [Google Scholar] [CrossRef] [PubMed]
- National Center for Health Statistics. How Coronavirus Spread. Available online: https://stacks.cdc.gov/view/cdc/85631 (accessed on 3 November 2021).
- Lu, C.W.; Liu, X.F.; Jia, Z.F. 2019-NCoV Transmission through the Ocular Surface Must Not Be Ignored. Lancet 2020, 395, e39. [Google Scholar] [CrossRef]
- Xia, J.; Tong, J.; Liu, M.; Shen, Y.; Guo, D. Evaluation of Coronavirus in Tears and Conjunctival Secretions of Patients with SARS-CoV-2 Infection. J. Med. Virol. 2020, 92, 589–594. [Google Scholar] [CrossRef]
- Danesh-Meyer, H.V.; McGhee, C.N.J. Implications of COVID-19 for Ophthalmologists. Am. J. Ophthalmol. 2021, 223, 108–118. [Google Scholar] [CrossRef]
- Zhou, Y.; Zeng, Y.; Tong, Y.; Chen, C. Ophthalmologic Evidence against the Interpersonal Transmission of 2019 Novel Coronavirus through Conjunctiva. medRxiv 2002. [Google Scholar] [CrossRef]
- Colantuono, D.; Miere, A.; Semoun, O.; Amoroso, F.; Souied, E.H. AMD Management During the COVID-19 Pandemic. Acta Ophthalmol. 2020, 98, e925. [Google Scholar] [CrossRef]
- Corazza, P.; D’Alterio, F.M.; Younis, S. Proposed Algorithm during COVID-19 Pandemic for Patient Management in Medical Retina Clinic. Int. J. Retin. Vitr. 2020, 6, 20. [Google Scholar] [CrossRef]
- American Academy of Ophthalmology Recommendations for Urgent and Nonurgent Patient Care—American Academy of Ophthalmology. Available online: https://www.aao.org/headline/new-recommendations-urgent-nonurgent-patient-care (accessed on 3 November 2021).
- Duncan, L.J.; Cheng, K.F.D. Public Perception of NHS General Practice during the First Six Months of the COVID-19 Pandemic in England. F1000Research 2021, 10, 279. [Google Scholar] [CrossRef]
- Shah, N.; Ahmed, I.; Nazir, T. Heart Failure-Related Hospitalisation and Management during the COVID-19 Pandemic: A Reflection. Letter Regarding the Article ‘The Impact of COVID-19 on Heart Failure Hospitalization and Management: Report from a Heart Failure Unit in London during the Peak of the Pandemic’. Eur. J. Heart Fail. 2021, 23, 343–344. [Google Scholar] [CrossRef]
- Wasser, L.M.; Weill, Y.; Brosh, K.; Magal, I.; Potter, M.; Strassman, I.; Gelman, E.; Koslowsky, M.; Zadok, D.; Hanhart, J. The Impact of COVID-19 on Intravitreal Injection Compliance. SN Compr. Clin. Med. 2020, 2, 2546–2549. [Google Scholar] [CrossRef] [PubMed]
- Wai, K.M.; Begaj, T.; Patil, S.; Chen, E.M.; Miller, J.B.; Kylstra, J.; Aronow, M.E.; Young, L.H.; Huckfeldt, R.; Husain, D.; et al. The Effect of Sample Medication Use on Subsequent Anti-VEGF Agent Selection for Neovascular Age-Related Macular Degeneration. Semin. Ophthalmol. 2022, 37, 902–908. [Google Scholar] [CrossRef] [PubMed]
- Borrelli, E.; Grosso, D.; Vella, G.; Sacconi, R.; Querques, L.; Zucchiatti, I.; Prascina, F.; Bandello, F.; Querques, G. Impact of COVID-19 on Outpatient Visits and Intravitreal Treatments in a Referral Retina Unit: Let’s Be Ready for a Plausible “Rebound Effect”. Graefes Arch. Clin. Exp. Ophthalmol. 2020, 258, 2655–2660. [Google Scholar] [CrossRef]
- Yeter, D.Y.; Dursun, D.; Bozali, E.; Ozec, A.V.; Erdogan, H. Effects of the COVID-19 Pandemic on Neovascular Age-Related Macular Degeneration and Response to Delayed Anti-VEGF Treatment. J. Fr. Ophtalmol. 2021, 44, 299–306. [Google Scholar] [CrossRef]
- Xu, D.; Starr, M.R.; Boucher, N.; Chiang, A.; Yonekawa, Y.; Klufas, M.A.; Khan, M.A.; Cohen, M.N.; Mehta, S.; Kuriyan, A.E. Real-World Vitreoretinal Practice Patterns during the 2020 COVID-19 Pandemic: A Nationwide, Aggregated Health Record Analysis. Curr. Opin. Ophthalmol. 2020, 31, 427–434. [Google Scholar] [CrossRef]
- Toro, M.D.; Brézin, A.P.; Burdon, M.; Cummings, A.B.; Evren Kemer, O.; Malyugin, B.E.; Prieto, I.; Teus, M.A.; Tognetto, D.; Törnblom, R.; et al. Early Impact of COVID-19 Outbreak on Eye Care: Insights from EUROCOVCAT Group. Eur. J. Ophthalmol. 2021, 31, 5–9. [Google Scholar] [CrossRef]
- Vallianou, N.G.; Evangelopoulos, A.; Kounatidis, D.; Stratigou, T.; Christodoulatos, G.S.; Karampela, I.; Dalamaga, M. Diabetes Mellitus and SARS-CoV-2 Infection: Pathophysiologic Mechanisms and Implications in Management. Curr. Diabetes Rev. 2021, 17, e123120189797. [Google Scholar] [CrossRef]
- Dalamaga, M.; Christodoulatos, G.S.; Karampela, I.; Vallianou, N.; Apovian, C.M. Understanding the Co-Epidemic of Obesity and COVID-19: Current Evidence, Comparison with Previous Epidemics, Mechanisms, and Preventive and Therapeutic Perspectives. Curr. Obes. Rep. 2021, 10, 214–243. [Google Scholar] [CrossRef]
- Syriga, M.; Karampela, Ι.; Dalamaga, Μ.; Karampelas, M. The Effect of COVID-19 Pandemic on the Attendance and Clinical Outcomes of Patients with Ophthalmic Disease: A Mini-Review. Metabol. Open 2021, 12, 100131. [Google Scholar] [CrossRef]
- Viola, F.; Milella, P.; Pozzo Giuffrida, F.; Ganci, S.; Invernizzi, A. The Impact of Coronavirus Disease (COVID-19) Pandemic on Intravitreal Injections Treatment for Macular Diseases: Report from a Referral Hospital in Milan. Retina 2021, 41, 701–705. [Google Scholar] [CrossRef]
- Korobelnik, J.F.; Loewenstein, A.; Aslam, T.; Barratt, J.; Eldem, B.; Finger, R.; Gale, R.; Lövestam-Adrian, M.; Okada, M.; Parker, N.; et al. Communicating with Patients with NAMD and Their Families during the COVID-19 Pandemic. Graefe’s Arch. Clin. Exp. Ophthalmol. 2020, 258, 1335–1337. [Google Scholar] [CrossRef] [PubMed]
- Antaki, F.; Dirani, A. Treating Neovascular Age-Related Macular Degeneration in the Era of COVID-19. Graefe’s Arch. Clin. Exp. Ophthalmol. 2020, 258, 1567–1569. [Google Scholar] [CrossRef] [PubMed]
- Sacconi, R.; Borrelli, E.; Vella, G.; Querques, L.; Prascina, F.; Zucchiatti, I.; Bandello, F.; Querques, G. TriPla Regimen: A New Treatment Approach for Patients with Neovascular Age-Related Macular Degeneration in the COVID-19 “Era”. Eur. J. Ophthalmol. 2021, 31, 849–852. [Google Scholar] [CrossRef] [PubMed]
- Mintz, J.; Labiste, C.; DiCaro, M.V.; McElroy, E.; Alizadeh, R.; Xu, K. Teleophthalmology for Age-Related Macular Degeneration during the COVID-19 Pandemic and Beyond. J. Telemed. Telecare 2020, 28, 670–679. [Google Scholar] [CrossRef] [PubMed]
- Solomon, S.D.; Lindsley, K.; Vedula, S.S.; Krzystolik, M.G.; Hawkins, B.S. Anti-Vascular Endothelial Growth Factor for Neovascular Agerelated Macular Degeneration. Cochrane Database Syst. Rev. 2019, 3, CD005139. [Google Scholar] [CrossRef]
- Massamba, N.; Dirani, A.; Knoeri, J.; Pasquier, B.; Ingram, A.; Soubrane, G. Evaluating the Impact of Summer Vacation on the Visual Acuity of AMD Patients Treated with Ranibizumab. Eye 2015, 29, 1453–1457. [Google Scholar] [CrossRef]
- Borrelli, E.; Grosso, D.; Vella, G.; Sacconi, R.; Battista, M.; Querques, L.; Zucchiatti, I.; Prascina, F.; Bandello, F.; Querques, G. Short-Term Outcomes of Patients with Neovascular Exudative AMD: The Effect of COVID-19 Pandemic. Graefe’s Arch. Clin. Exp. Ophthalmol. 2020, 258, 2621–2628. [Google Scholar] [CrossRef]
- Chatziralli, I.; Dimitriou, E.; Kazantzis, D.; Machairoudia, G.; Theodossiadis, G.; Theodossiadis, P. Effect of COVID-19-Associated Lockdown on Patients with Diabetic Retinopathy. Cureus 2021, 13, e14831. [Google Scholar] [CrossRef]
- Sevik, M.O.; Aykut, A.; Özkan, G.; Dericioğlu, V.; Şahin, Ö. The Effect of COVID-19 Pandemic Restrictions on Neovascular AMD Patients Treated with Treat-and-Extend Protocol. Int. Ophthalmol. 2021, 41, 2951–2961. [Google Scholar] [CrossRef]
Patients Who Did Not Experience Any Delays During Lockdown | Patients Who Did Experience Delays During Lockdown | |||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Pre-COVID-19 Appointment | Post-COVID-19 Appointment | Pre-COVID-19 Appointment | Post-COVID-19 Appointment | |||||||||||||
n | % | Median(IQR) | n | % | Median (IQR) | p-Value | 95%CI | n | % | Median (IQR) | n | % | Median (IQR) | p-Value | 95%CI | |
Age (Years) | 80 (75–80) | 80 (74–87) | ||||||||||||||
64 (30.25–104.75) | ||||||||||||||||
Cataract surgery (No/Yes) | 51/49 | 51/49 | 84/16 | 84/16 | 56/44 | 56/44 | 84/16 | 84/16 | ||||||||
Time between pre-COVID-19 appointments (weeks) | 8 (4–8) | 8(4–8) | ||||||||||||||
Macular fluid (No/Yes) | 19/81 | 19/81 | 38/62 | 38/62 | 35/65 | 35/65 | 38/62 | 38/62 | ||||||||
Injection (No/Yes) | 6/94 | 6/94 | 15/85 | 15/85 | 21/79 | 21/79 | 15/85 | 15/85 | ||||||||
Type injection | ||||||||||||||||
Aflibercept | 78.00 | 78.00 | 73.00 | 73.00 | 63 | 63 | 73 | 73 | ||||||||
Ranibizumab | 8.00 | 8.00 | 8.00 | 8.00 | 11 | 11 | 8 | 8 | ||||||||
Bevacizumab | 8 | 8.00 | 4.00 | 4.00 | 5 | 5 | 4 | 4 | ||||||||
Time until next examination (weeks) | 8 (4–8) | 8 (6–10) | 0.013 * | (0.00 to 2.00) | 8 (6–10) | 8 (4–10) | 0.275 | (−2.000 to 0.000) | ||||||||
Visual acuity in logMar | 0.300 (0.200–0.600) | 0.3000 (0.2000–0.6000) | 0.103 | (−0.008 to 0.093) | 0.400 (0.200–0.700) | 0.5000 (0.3000–0.9000) | 0.0002 *** | (0.000 to 0.1000) | ||||||||
Retinal thickness C0 | 296.00 (253.25–359.50) | 277.50 (245.25–359.75) | 0.029 * | (−41.00 to −4.000) | 285.50 (252.50–338.75) | 300.00 (252.25–363.25) | 0.232 | (−6.000 to 12.00) | ||||||||
Retinal thickness S1 | 324.00 (301.00–351.75) | 312.50 (291.25–347.25) | 0.030 * | (−8.000 to 2.000) | 324.00 (293.50–345.00) | 328.50 (298.75–373.75) | 0.084 | (−3.000 to 6.000) | ||||||||
Retinal thickness S2 | 281.00 (264.00–296.00) | 279.00 (257.00–292.00) | 0.033 * | (−3.000 to 1.000) | 280.50 (263.25–300.00) | 282.50 (263.50–305.75) | 0.556 | (−2.000 to 0.000) | ||||||||
Retinal thickness N1 | 328.00 (305.00–360.75) | 321.50 (294.00–353.00) | 0.020 * | (−10.00 to 2.000) | 324.00 (304.00–358.00) | 337.50 (305.50–375.50) | 0.030 * | (−2.000 to 7.000) | ||||||||
Retinal thickness N2 | 301.00 (283.00–314.00) | 298.00 (277.00–310.00) | 0.263 | (−2.000 to 1.000) | 297.00 (276.00–311.00) | 299.00 (278.00–318.00) | 0.241 | (−1.000 to 1.000) | ||||||||
Retinal thickness I1 | 327.50 (305.00–374.25) | 325.00 (285.25–367.75) | 0.033 * | (−12.00 to 0.000) | 327.50 (293.25–364.75) | 327.00 (295.00–380.00) | 0.142 | (−2.000 to 4.000) | ||||||||
Retinal thickness I2 | 274.00 (255.00–296.75) | 273.00 (250.00–293.50) | 0.043 * | (−3.000 to 0.000) | 270.50 (250.00–287.75) | 272.00 (251.50–294.75) | 0.335 | (−4.000 to 2.000) | ||||||||
Retinal thickness T1 | 320.50 (293.00–354.50) | 314.00 (286.00–358.50) | 0.140 | (−9.000 to 3.000) | 310.00 (282.00–341.00) | 310.50 (282.25–365.00) | 0.880 | (−2.000 to 1.000) | ||||||||
Retinal thickness T2 | 273.50 (260.00–285.75) | 271.50 (256.75–286.00) | 0.147 | (−2.000 to 1.000) | 268.0 (257.3–290.0) | 272.5 (256.3–296.0) | 0.999 | (−2.000 to 1.000) |
Patients with no Delays in Appointments | Patients with Late Appointments | |||
---|---|---|---|---|
Median (IQR) | Median(IQR) | p-Value | 95%CI | |
Age (years) | 80 (75–80) | 80 (74–87) | 0.928 | (−2.000 to 2.000) |
Visual acuity in logMar | 0.3000 (0.2000–0.6000) | 0.5000 (0.3000–0.9000) | 0.004 ** | (0.000 to 0.2000) |
Retinal thickness C0 | 277.50 (245.25–359.75) | 300.00 (252.25–363.25) | 0.116 | (−4.000 to 38.00) |
Retinal thickness S1 | 312.50 (291.25–347.25) | 328.50 (298.75–373.75) | 0.064 | (−1.000 to 26.00) |
Retinal thickness S2 | 279.00 (257.00–292.00) | 282.50 (263.50–305.75) | 0.091 | (−1.000 to 15.00) |
Retinal thickness N1 | 321.50 (294.00–353.00) | 337.50 (305.50–375.50) | 0.027 * | (2.000 to 28.00) |
Retinal thickness N2 | 298.00 (277.00–310.00) | 299.00 (278.00–318.00) | 0.457 | (−5.000 to 11.00) |
Retinal thickness I1 | 325.00 (285.25–367.75) | 327.00 (295.00–380.00) | 0.402 | (−9.000 to 24.00) |
Retinal thickness I2 | 273.00 (250.00–293.50) | 272.00 (251.50–294.75) | 0.708 | (−8.000 to 12.00) |
Retinal thickness T1 | 314.00 (286.00–358.50) | 310.50 (282.25–365.00) | 0.828 | (−14.00 to 17.00) |
Retinal thickness T2 | 271.50 (256.75–286.00) | 272.5 (256.3–296.0) | 0.315 | (−4.000 to 13.00) |
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López-Cuenca, I.; Fabozzi, L.; Younis, S.; Ali, A.; Ramírez, J.M.; Cordeiro, M.F.; Hoz, R.d. The Effects of the COVID-19 Pandemic on the Follow-Up of Patients with Age-Related Macular Degeneration in a Tertiary Hospital in London, the UK. J. Clin. Med. 2025, 14, 6497. https://doi.org/10.3390/jcm14186497
López-Cuenca I, Fabozzi L, Younis S, Ali A, Ramírez JM, Cordeiro MF, Hoz Rd. The Effects of the COVID-19 Pandemic on the Follow-Up of Patients with Age-Related Macular Degeneration in a Tertiary Hospital in London, the UK. Journal of Clinical Medicine. 2025; 14(18):6497. https://doi.org/10.3390/jcm14186497
Chicago/Turabian StyleLópez-Cuenca, Inés, Lorenzo Fabozzi, Saad Younis, Ahmad Ali, José M. Ramírez, Maria Francesca Cordeiro, and Rosa de Hoz. 2025. "The Effects of the COVID-19 Pandemic on the Follow-Up of Patients with Age-Related Macular Degeneration in a Tertiary Hospital in London, the UK" Journal of Clinical Medicine 14, no. 18: 6497. https://doi.org/10.3390/jcm14186497
APA StyleLópez-Cuenca, I., Fabozzi, L., Younis, S., Ali, A., Ramírez, J. M., Cordeiro, M. F., & Hoz, R. d. (2025). The Effects of the COVID-19 Pandemic on the Follow-Up of Patients with Age-Related Macular Degeneration in a Tertiary Hospital in London, the UK. Journal of Clinical Medicine, 14(18), 6497. https://doi.org/10.3390/jcm14186497