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    Corneal axonal loss as an imaging biomarker of neurodegeneration in multiple sclerosis: a longitudinal study
    (Sage Publications Ltd, 2023) Petropoulos, Ioannis N.; Al-Shibani, Fatima; Bitirgen, Gulfidan; Ponirakis, Georgios; Khan, Adnan; Gad, Hoda; Mahfoud, Ziyad R.
    Background:Resourceful endpoints of axonal loss are needed to predict the course of multiple sclerosis (MS). Corneal confocal microscopy (CCM) can detect axonal loss in patients with clinically isolated syndrome and established MS, which relates to neurological disability. Objective:To assess corneal axonal loss over time in relation to retinal atrophy, and neurological and radiological abnormalities in MS. Methods:Patients with relapsing-remitting (RRMS) (n = 68) or secondary progressive MS (SPMS) (n = 15) underwent CCM and optical coherence tomography. Corneal nerve fibre density (CNFD-fibres/mm(2)), corneal nerve branch density (CNBD-branches/mm(2)), corneal nerve fibre length (CNFL-mm/mm(2)) and retinal nerve fibre layer (RNFL-mu m) thickness were quantified along with neurological and radiological assessments at baseline and after 2 years of follow-up. Age-matched, healthy controls (n = 20) were also assessed. Results:In patients with RRMS compared with controls at baseline, CNFD (p = 0.004) and RNFL thickness (p < 0.001) were lower, and CNBD (p = 0.003) was higher. In patients with SPMS compared with controls, CNFD (p < 0.001), CNFL (p = 0.04) and RNFL thickness (p < 0.001) were lower. For identifying RRMS, CNBD had the highest area under the receiver operating characteristic (AUROC) curve (0.99); and for SPMS, CNFD had the highest AUROC (0.95). At follow-up, there was a further significant decrease in CNFD (p = 0.04), CNBD (p = 0.001), CNFL (p = 0.008) and RNFL (p = 0.002) in RRMS; in CNFD (p = 0.04) and CNBD (p = 0.002) in SPMS; and in CNBD (p = 0.01) in SPMS compared with RRMS. Follow-up corneal nerve loss was greater in patients with new enhancing lesions and optic neuritis history. Conclusion:Progressive corneal and retinal axonal loss was identified in patients with MS, especially those with more active disease. CCM may serve as an imaging biomarker of axonal loss in MS.
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    Corneal confocal microscopy identifies corneal nerve fibre loss and increased dendritic cells in patients with long COVID
    (Bmj Publishing Group, 2022) Bitirgen, Gulfidan; Korkmaz, Celalettin; Zamani, Adil; Ozkagnici, Ahmet; Zengin, Nazmi; Ponirakis, Georgios; Malik, Rayaz A.
    Background/Aims Long COVID is characterised by a range of potentially debilitating symptoms which develop in at least 10% of people who have recovered from acute SARS-CoV-2 infection. This study has quantified corneal sub-basal nerve plexus morphology and dendritic cell (DC) density in patients with and without long COVID. Methods Forty subjects who had recovered from COVID-19 and 30 control participants were included in this cross-sectional comparative study undertaken at a university hospital. All patients underwent assessment with the National Institute for Health and Care Excellence (NICE) long COVID, Douleur Neuropathique 4 (DN4) and Fibromyalgia questionnaires, and corneal confocal microscopy (CCM) to quantify corneal nerve fibre density (CNFD), corneal nerve branch density (CNBD), corneal nerve fibre length (CNFL), and total, mature and immature DC density. Results The mean time after the diagnosis of COVID-19 was 3.7 +/- 1.5 months. Patients with neurological symptoms 4 weeks after acute COVID-19 had a lower CNFD (p=0.032), CNBD (p=0.020), and CNFL (p=0.012), and increased DC density (p=0.046) compared with controls, while patients without neurological symptoms had comparable corneal nerve parameters, but increased DC density (p=0.003). There were significant correlations between the total score on the NICE long COVID questionnaire at 4 and 12 weeks with CNFD (rho=-0.436; p=0.005, rho=-0.387; p=0.038, respectively) and CNFL (rho=-0.404; p=0.010, rho=-0.412; p=0.026, respectively). Conclusion Corneal confocal microscopy identifies corneal small nerve fibre loss and increased DCs in patients with long COVID, especially those with neurological symptoms. CCM could be used to objectively identify patients with long COVID.
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    Subclinical Corneal Nerve Fiber Damage and Immune Cell Activation in Systemic Lupus Erythematosus: A Corneal Confocal Microscopy Study
    (Assoc Research Vision Ophthalmology Inc, 2021) Bitirgen, Gulfidan; Kucuk, Adem; Ergun, Mustafa Cagri; Baloglu, Ruveyda; Gharib, Miral H.; Al Emadi, Samar; Ponirakis, Georgios
    Purpose: The purpose of this study was to evaluate the utility of corneal confocal microscopy (CCM) in identifying small nerve fiber damage and immune cell activation in patients with systemic lupus erythematosus (SLE). Methods: This cross-sectional comparative study included 39 consecutive patients with SLE and 30 healthy control participants. Central corneal sensitivity was assessed using a Cochet-Bonnet contact corneal esthesiometer and a laser scanning CCM (Heidelberg, Germany) was used to quantify corneal nerve fiber density (CNFD), nerve branch density (CNBD), nerve fiber length (CNFL), and Langerhans cell (LC) density. Results: Age was comparable among patients with SLE (33.7 +/- 12.7) and controls (35.0 +/- 13.7 years, P = 0.670) and the median duration of disease was 3.0 years (2.0-10.0 years). CNBD (P = 0.003) and CNFL (P = 0.019) were lower and mature LC density (P = 0.002) was higher, but corneal sensitivity (P = 0.178) and CNFD (P = 0.198) were comparable in patients with SLE compared with controls. The SELENA-SLEDAI score correlated with CNFD (rho = -0.319, P = 0.048) and CNFL (rho = -0.373, P = 0.019), and the total and immature LC densities correlated with CNBD (rho = -0.319. P = 0.048, and rho = -0.328, P = 0.041, respectively). Immature LC density was higher (P = 0.025), but corneal sensitivity and nerve fiber parameters were comparable between patients with (33%) and without neuropsychiatric symptoms and SLE. Conclusions: Corneal confocal microscopy identifies distal corneal nerve fiber loss and increased immune cell density in patients with SLE and corneal nerve loss was associated with disease activity. Translational Relevance: Corneal confocal microscopy may enable the detection of subclinical corneal nerve loss and immune cell activation in SLE. Translational Relevance: Corneal confocal microscopy may enable the detection of subclinical corneal nerve loss and immune cell activation in SLE.