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Topic Editors

Department of Ophthalmology, Dijon University Hospital, Dijon, France

Prof. Dr. Ryo Kawasaki

Artificial Intelligence Center for Medical Research and Application, Osaka University Hospital 2-2 Yamada-oka, Suita-city, Osaka 565-0871, Japan

Prof. Dr. Fabrice Meriaudeau

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ImViA, Université Bourgogne-Franche-Comté, 71200 Le Creusot, France

Prof. Dr. João Barbosa-Breda

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Cardiovascular R&D Center, Faculty of Medicine, University of Porto, Porto, Portugal

Retinal Imaging and Systemic Vascular Disease: Recent Advances and Perspective

Abstract submission deadline

closed (30 November 2022)

Manuscript submission deadline

closed (31 January 2023)

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21147

Topic Information

Dear Colleagues,

The healthcare burden of cardio and cerebrovascular disease remains a priority. Understanding their underlying mechanisms and improving identification of people with higher systemic vascular risk profile with non-invasive examinations seem to be crucial. In Ophthalmology, retinal imaging is simple, non-invasive and it can provide in vivo insight of the retinal microcirculation. For more than ten years, research teams have been working on software developed to allow automatic analysis of the retinal vascular network from different imaging technique (fundus photographs, oct-angiography or adaptive optics…) and to provide a description of the geometric characteristics of its arterial and venous components. At the same time, research teams have explored the pathophysiological association between macro vascular and micro vascular alterations. Thus, retinal microcirculation could be considered as a witness of the systemic vascular status. New approach with retinal images dataset and artificial intelligence algorithms recently strengthened the interest of retinal microvascular biomarker. In spite of the large volume of associated research, the interest of retinal biomarker in terms of screening, monitoring or prediction of systemic vascular disease remain uncertain.

The aim of this Topic is to gather retinal imaging research as well as epidemiological or artificial intelligence papers focused on the relationship between retinal vascular network and systemic vascular disease.

Dr. Louis Arnould
Prof. Dr. Ryo Kawasaki
Prof. Dr. Fabrice Meriaudeau
Prof. Dr. João Barbosa-Breda
Topic Editors

Keywords

Oct-Angiography
Fundus photographs
Cardiovascular disease
Stroke
Deep learning
Machine learning
Population-based study
Retinal vascular network
Vascular predicting capacity
Vascular prevention

Participating Journals

Journal Name	Impact Factor	CiteScore	Launched Year	First Decision (median)	APC
Diagnostics diagnostics	3.6	3.6	2011	20.7 Days	CHF 2600
Journal of Clinical Medicine jcm	3.9	5.4	2012	17.9 Days	CHF 2600
Journal of Personalized Medicine jpm	3.4	2.6	2011	17.8 Days	CHF 2600
International Journal of Molecular Sciences ijms	5.6	7.8	2000	16.3 Days	CHF 2900

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Published Papers (10 papers)

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12 pages, 272 KiB

Open AccessArticle

Evaluation of Subclinical Retinal Disease in Patients Affected by Systemic Lupus Erythematosus with No Evidence of Ocular Involvement—An Optical Coherence Tomography Angiography Original Study

by Małgorzata Mimier-Janczak, Dorota Kaczmarek, Krzysztof Proc, Marta Misiuk-Hojło and Radosław Kaczmarek

J. Clin. Med. 2022, 11(24), 7417; https://0-doi-org.brum.beds.ac.uk/10.3390/jcm11247417 - 14 Dec 2022

Cited by 5 | Viewed by 1430

Abstract

Lupus retinopathy is the second most common eye involvement in systemic lupus erythematosus (SLE), associated with significant visual deterioration and well-known negative prognostic factor for survival. Ocular manifestation in SLE, relating the retina, ranges from asymptomatic vascular involvement to vision devastating vascular occlusions. Subclinical microvascular changes are undetectable in slit lamp examination, hence are underdiagnosed. Optical coherence tomography angiography (OCTA) is a novel, easy to interpret and non-invasive technique that allows retinal vessels visualization. OCTA simplifies clinical approach and measures the severity of decreased perfusion. The aim of the study was to demonstrate the retinal vascularization in a subclinical stage of ocular involvement in a cohort of SLE patients. Thirty-three patients (57 eyes) diagnosed with SLE were enrolled into the study group and 31 healthy individuals (56 eyes) into the control group. Vessel density reduction in parafovea, inferior and nasal quadrants of superficial retinal capillary plexus in a cohort of SLE patients was found. Among study group kidney involvement was associated with further microvasculature reduction. Knowing that retinal involvement may precede other organs impairment, early detection of retinal impairment and use of OCTA as a screening modality, may decrease overall disease morbidity. Full article

(This article belongs to the Topic Retinal Imaging and Systemic Vascular Disease: Recent Advances and Perspective)

15 pages, 14796 KiB

Open AccessArticle

Detection of Stroke with Retinal Microvascular Density and Self-Supervised Learning Using OCT-A and Fundus Imaging

by Samiksha Pachade, Ivan Coronado, Rania Abdelkhaleq, Juntao Yan, Sergio Salazar-Marioni, Amanda Jagolino, Charles Green, Mozhdeh Bahrainian, Roomasa Channa, Sunil A. Sheth and Luca Giancardo

J. Clin. Med. 2022, 11(24), 7408; https://0-doi-org.brum.beds.ac.uk/10.3390/jcm11247408 - 14 Dec 2022

Cited by 7 | Viewed by 2288

Abstract

Acute cerebral stroke is a leading cause of disability and death, which could be reduced with a prompt diagnosis during patient transportation to the hospital. A portable retina imaging system could enable this by measuring vascular information and blood perfusion in the retina and, due to the homology between retinal and cerebral vessels, infer if a cerebral stroke is underway. However, the feasibility of this strategy, the imaging features, and retina imaging modalities to do this are not clear. In this work, we show initial evidence of the feasibility of this approach by training machine learning models using feature engineering and self-supervised learning retina features extracted from OCT-A and fundus images to classify controls and acute stroke patients. Models based on macular microvasculature density features achieved an area under the receiver operating characteristic curve (AUC) of 0.87–0.88. Self-supervised deep learning models were able to generate features resulting in AUCs ranging from 0.66 to 0.81. While further work is needed for the final proof for a diagnostic system, these results indicate that microvasculature density features from OCT-A images have the potential to be used to diagnose acute cerebral stroke from the retina. Full article

(This article belongs to the Topic Retinal Imaging and Systemic Vascular Disease: Recent Advances and Perspective)

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13 pages, 2667 KiB

Open AccessArticle

Repeatability and Reproducibility of Retinal Fractal Dimension Measured with Swept-Source Optical Coherence Tomography Angiography in Healthy Eyes: A Proof-of-Concept Study

by Louis Arnould, Déa Haddad, Florian Baudin, Pierre-Henry Gabrielle, Marc Sarossy, Alain M. Bron, Behzad Aliahmad and Catherine Creuzot-Garcher

Diagnostics 2022, 12(7), 1769; https://0-doi-org.brum.beds.ac.uk/10.3390/diagnostics12071769 - 21 Jul 2022

Cited by 1 | Viewed by 1659

Abstract

The retinal vascular network fractal dimension (FD) could be a promising imaging biomarker. Our objective was to evaluate its repeatability and reproducibility in healthy eyes. A cross-sectional study was undertaken with young, healthy volunteers who had no reported cardiac risk factors or ocular disease history. For each participant, three SS-OCTA images (12 × 12 mm) were acquired using the Plex Elite 9000 (Carl Zeiss Meditec AG, Jena, Germany) by two ophthalmologists. Automated segmentation was obtained from both the superficial and deep capillary plexuses. FD was estimated by box counting. The intraclass correlation coefficients (ICC) were used as measures for repeatability and reproducibility. A total of 43 eyes of healthy volunteers were included. The mean ± standard deviation (SD) age was 30 ± 6.2 years. The results show good repeatability. The ICC was 0.722 (95% CI, 0.541–0.839) in the superficial capillary plexus and 0.828 (95% CI, 0.705–0.903) in the deep capillary plexus. For reproducibility, the ICC was 0.651 (95% CI, 0.439–0.795) and 0.363 (95% CI, 0.073–0.596) at the superficial and deep capillary plexus, respectively. In this study, the FD of the vascular network measured via SS-OCTA showed good repeatability and reproducibility in healthy participants. Full article

(This article belongs to the Topic Retinal Imaging and Systemic Vascular Disease: Recent Advances and Perspective)

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11 pages, 1555 KiB

Open AccessArticle

Retinal Microvascular Changes in Familial Hypercholesterolemia: Analysis with Swept-Source Optical Coherence Tomography Angiography

by Pétra Eid, Louis Arnould, Pierre-Henry Gabrielle, Ludwig S. Aho, Michel Farnier, Catherine Creuzot-Garcher and Yves Cottin

J. Pers. Med. 2022, 12(6), 871; https://0-doi-org.brum.beds.ac.uk/10.3390/jpm12060871 - 26 May 2022

Cited by 3 | Viewed by 1645

Abstract

Familial hypercholesterolemia (FH) is a common but underdiagnosed genetic disorder affecting cholesterol metabolism, leading to atherosclerotic disease. The relationship between retinal microvascular changes and the presence of atheroma in patients with FH (FH group), and in comparison to volunteers without FH (CT group), needs further investigation. This cross-sectional study was conducted in a university hospital between October 1, 2020 and May 31, 2021. Cardiovascular data, including the Coronary Artery Calcium (CAC) score, were recorded for FH patients. Macula angiograms were acquired using swept-source optical coherence tomography angiography (SS OCT-A) to analyze both the superficial capillary plexus (SCP) and deep capillary plexus (DCP). A total of 162 eyes of 83 patients were enrolled in the FH group and 121 eyes of 78 volunteers in the CT group. A statistically significant association was found between the CAC score and both vessel density (β = −0.002 [95% CI, −0.004; −0.0005], p = 0.010) and vessel length (β = −0.00005 [95% CI, −0.00008; −0.00001], p = 0.010) in the DCP. The FH group had a significantly lower foveal avascular zone circularity index than the CT group in multivariate analysis (0.67 ± 0.16 in the FH group vs. 0.72 ± 0.10 in the CT group, β = 0.04 [95% CI, 0.002; 0.07], p = 0.037). Retinal microvascularization is altered in FH and retinal vascular densities are modified according to the CAC score. Full article

(This article belongs to the Topic Retinal Imaging and Systemic Vascular Disease: Recent Advances and Perspective)

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12 pages, 1712 KiB

Open AccessArticle

Concordance between SIVA, IVAN, and VAMPIRE Software Tools for Semi-Automated Analysis of Retinal Vessel Caliber

by Thibaud Mautuit, Pierre Cunnac, Carol Y. Cheung, Tien Y. Wong, Stephen Hogg, Emanuele Trucco, Vincent Daien, Thomas J. MacGillivray, José Labarère and Christophe Chiquet

Diagnostics 2022, 12(6), 1317; https://0-doi-org.brum.beds.ac.uk/10.3390/diagnostics12061317 - 25 May 2022

Cited by 6 | Viewed by 2623

Abstract

We aimed to compare measurements from three of the most widely used software packages in the literature and to generate conversion algorithms for measurement of the central retinal artery equivalent (CRAE) and central retinal vein equivalent (CRVE) between SIVA and IVAN and between SIVA and VAMPIRE. We analyzed 223 retinal photographs from 133 human participants using both SIVA, VAMPIRE and IVAN independently for computing CRAE and CRVE. Agreement between measurements was assessed using Bland–Altman plots and intra-class correlation coefficients. A conversion algorithm between measurements was carried out using linear regression, and validated using bootstrapping and root-mean-square error. The agreement between VAMPIRE and IVAN was poor to moderate: The mean difference was 20.2 µm (95% limits of agreement, LOA, −12.2–52.6 µm) for CRAE and 21.0 µm (95% LOA, −17.5–59.5 µm) for CRVE. The agreement between VAMPIRE and SIVA was also poor to moderate: the mean difference was 36.6 µm (95% LOA, −12.8–60.4 µm) for CRAE, and 40.3 µm (95% LOA, 5.6–75.0 µm) for CRVE. The agreement between IVAN and SIVA was good to excellent: the mean difference was 16.4 µm (95% LOA, −4.25–37.0 µm) for CRAE, and 19.3 µm (95% LOA, 0.09–38.6 µm) for CRVE. We propose an algorithm converting IVAN and VAMPIRE measurements into SIVA-estimated measurements, which could be used to homogenize sets of vessel measurements obtained with different software packages. Full article

(This article belongs to the Topic Retinal Imaging and Systemic Vascular Disease: Recent Advances and Perspective)

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14 pages, 3980 KiB

Open AccessArticle

Associations between Choriocapillaris Flow on Optical Coherence Tomography Angiography and Cardiovascular Risk Profiles of Patients with Acute Myocardial Infarction

by Dae Sung Kim, Byung Sik Kim, Heeyoon Cho, Jeong-Hun Shin and Yong Un Shin

J. Pers. Med. 2022, 12(5), 839; https://0-doi-org.brum.beds.ac.uk/10.3390/jpm12050839 - 20 May 2022

Cited by 3 | Viewed by 1723

Abstract

We evaluated the association between macular perfusion assessed via optical coherence tomography angiography (OCTA) and the cardiovascular risk profiles of patients with acute myocardial infarction (AMI). Patients with AMI who underwent comprehensive ophthalmological examinations and retinal OCTA were evaluated retrospectively. Retinal OCTA was performed for each patient within 3 days of admission. Quantitative analyses of the vessel density (VD) of the superficial capillary plexus (SCP) layers, deep capillary plexus layers (DCP), and choriocapillaris were performed after image processing. The 10-year risk of atherosclerotic cardiovascular disease (ASCVD), Global Registry of Acute Coronary Events (GRACE) score, reduction of atherothrombosis for continued health (REACH) score, and thrombolysis in myocardial infarction (TIMI) risk score were assessed. Sixty patients were included. VD in SCP and DCP was not associated with a 10-year ASCVD risk; however, choriocapillaris flow void features were significantly correlated with the 10-year ASCVD risk: decreased count, increased average size, and increased signal void area were correlated with increased 10-year ASCVD risk, GRACE score, REACH score, and TIMI risk score. In the multivariate analysis, a 10-year ASCVD risk (adjusted odds ratio [OR], 1.04; 95% confidence interval [CI], 1.01–1.08) and brain natriuretic peptide (adjusted OR, 1.00; 95% CI, 1.00–1.01) were significantly associated with the highest tertile of the average size of the choriocapillaris. Choriocapillaris flow void features measured using OCTA were associated with cardiovascular risk profiles in patients with AMI. OCTA may be used as an indicator of cardiovascular risk profiles and could improve cardiovascular risk assessments. Full article

(This article belongs to the Topic Retinal Imaging and Systemic Vascular Disease: Recent Advances and Perspective)

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8 pages, 1458 KiB

Open AccessBrief Report

Retinal Vessel Density and Treatment Intensity among Adults with Retinal Vein Occlusion: A Swept-Source Optical Coherence Tomography Angiography Study

by Brian T. Cheng, Shubhendu Mishra, John M. Bryan, Saena A. Sadiq, Nathan C. Sklar, Emily G. Suen, Taha O. Mohammed and Rukhsana G. Mirza

J. Clin. Med. 2022, 11(10), 2892; https://0-doi-org.brum.beds.ac.uk/10.3390/jcm11102892 - 20 May 2022

Cited by 2 | Viewed by 1425

Abstract

Previous studies have shown retinal vein occlusion (RVO) is associated with changes in vessel density visible on swept-source optical coherence tomography angiography (ss-OCTA). This study aimed to characterize retinal changes on ss-OCTA among RVO patients stratified by the need for continuous anti-VEGF therapy. This cross-sectional study of 24 RVO patients ≥ 18 years were imaged with SS-OCT-A. Patients were categorized into continuous vs. limited therapy (≥1 vs. no injections in previous 12 months) based on recurrence of intraretinal fluid (IRF) on OCT. Images were analyzed using ImageJ. T-tests were used to compare vessel density of the macula and peripheral retina. Overall, RVO patients undergoing continuous therapy (n = 14) had higher diabetes prevalence, worse baseline visual acuity, and higher baseline macular thickness compared to the limited (n = 10) therapy group. Continuous therapy was associated with lower macular VD in the combined retina layer and the superficial capillary plexus (SCP), but not in the deep capillary plexus (DCP). Further, the continuous therapy group exhibited lower peripheral VD in the combined retina layer, and no difference in the SCP and DCP layers when analyzed separately. In conclusion, RVO patients requiring continuous anti-VEGF injections demonstrate reduced VD of the macula and in the periphery on SS-OCTA imaging. SS-OCTA may be valuable for monitoring and prognosticating treatment for RVO patients. Full article

(This article belongs to the Topic Retinal Imaging and Systemic Vascular Disease: Recent Advances and Perspective)

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9 pages, 16985 KiB

Open AccessArticle

An Evaluation of Choroidal and Retinal Nerve Fiber Layer Thicknesses Using SD-OCT in Children with Childhood IgA Vasculitis

by Ali Simsek and Mehmet Tekin

Diagnostics 2022, 12(4), 901; https://0-doi-org.brum.beds.ac.uk/10.3390/diagnostics12040901 - 05 Apr 2022

Cited by 1 | Viewed by 1870

Abstract

Background: We aimed to evaluate choroidal and retinal nerve fiber layer (RNFL) thicknesses in children undergoing the childhood IgA vasculitis (IgAV). Methods: Fifty-two patients with IgAV aged 1–6 years and 54 healthy children were included. Cases’ age, sex, erythrocyte sedimentation rate (ESR), C-reactive protein (CRP), RNFL thicknesses, and choroidal thickness values were recorded. Results: Median foveal center choroidal thickness was 374.0 µm (315.0 to 452.0 µm) in the IgAV group and 349.5 µm (285.0 to 442.0 µm) in the control group (p = 0.001). Median average RNFL thickness was 110.0 µm (91.0 to 134.0 µm) in the IgAV group and 104.0 µm (89.0 to 117.0 µm) in the control group (p < 0.001). Choroidal and RNFL thicknesses were significantly greater in all quadrants in the IgAV group than in the control group. No correlation was determined between ESR or CRP and foveal center choroidal and average RNFL thicknesses. Conclusions: Our findings show that choroidal and RNFL thicknesses increased significantly in children undergoing childhood IgA vasculitis compared to the healthy control group. These findings show that the choroid and RNFL are also affected by the inflammatory process in IgAV, which is a systemic vasculitis. We think that the choroidal and RNFL thicknesses can be used as a biomarker for childhood IgAV. Full article

(This article belongs to the Topic Retinal Imaging and Systemic Vascular Disease: Recent Advances and Perspective)

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11 pages, 2269 KiB

Open AccessArticle

Comparing Measurements of Vascular Diameter Using Adaptative Optics Imaging and Conventional Fundus Imaging

by Thibaud Mautuit, Rachel Semecas, Stephen Hogg, Vincent Daien, Olivier Gavard, Nicolas Chateau, Tom MacGillivray, Emanuele Trucco and Christophe Chiquet

Diagnostics 2022, 12(3), 705; https://0-doi-org.brum.beds.ac.uk/10.3390/diagnostics12030705 - 13 Mar 2022

Cited by 8 | Viewed by 2302

Abstract

The aim of this prospective study was to compare retinal vascular diameter measurements taken from standard fundus images and adaptive optics (AO) images. We analysed retinal images of twenty healthy subjects with 45-degree funduscopic colour photographs (CR-2 Canon fundus camera, Canon™) and adaptive optics (AO) fundus images (rtx1 camera, Imagine Eyes^®). Diameters were measured using three software applications: the VAMPIRE (Vessel Assessment and Measurement Platform for Images of the REtina) annotation tool, IVAN (Interactive Vessel ANalyzer) for funduscopic colour photographs, and AO_Detect_Artery™ for AO images. For the arterial diameters, the mean difference between AO_Detect_Artery™ and IVAN was 9.1 µm (−27.4 to 9.2 µm, p = 0.005) and the measurements were significantly correlated (r = 0.79). The mean difference between AO_Detect_Artery™ and VAMPIRE annotation tool was 3.8 µm (−34.4 to 26.8 µm, p = 0.16) and the measurements were poorly correlated (r = 0.12). For the venous diameters, the mean difference between the AO_Detect_Artery™ and IVAN was 3.9 µm (−40.9 to 41.9 µm, p = 0.35) and the measurements were highly correlated (r = 0.83). The mean difference between the AO_Detect_Artery™ and VAMPIRE annotation tool was 0.4 µm (−17.44 to 25.3 µm, p = 0.91) and the correlations were moderate (r = 0.41). We found that the VAMPIRE annotation tool, an entirely manual software, is accurate for the measurement of arterial and venular diameters, but the correlation with AO measurements is poor. On the contrary, IVAN, a semi-automatic software tool, presents slightly greater differences with AO imaging, but the correlation is stronger. Data from arteries should be considered with caution, since IVAN seems to significantly under-estimate arterial diameters. Full article

(This article belongs to the Topic Retinal Imaging and Systemic Vascular Disease: Recent Advances and Perspective)

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14 pages, 1881 KiB

Open AccessArticle

Retinal Microcirculation Changes in Crohn’s Disease Patients under Biologics, a Potential Biomarker of Severity: A Pilot Study

by Eloi Debourdeau, Chloé Chamard, Isabelle Carriere, Julien Plat, Max Villain, Lucile Boivineau, Romain Altwegg and Vincent Daien

J. Pers. Med. 2022, 12(2), 230; https://0-doi-org.brum.beds.ac.uk/10.3390/jpm12020230 - 07 Feb 2022

Cited by 2 | Viewed by 1814

Abstract

Crohn’s disease (CD) is associated with increased cardiovascular risk and the retinal microcirculation is a reflection of the systemic microcirculation. Is the retinal microcirculation altered in relation to the severity of Crohn’s disease? This cross-sectional case-controlled study was conducted in a university hospital center from November 2020 to February 2021. We prospectively included patients with moderate (biologic therapy) or severe (biologic therapy + peri-anal disease and/or digestive resection) CD and age- and sex-matched controls. Individuals with diabetes, renal disease, cardiovascular disease, ophthalmological history or poor quality images were excluded. All participants underwent OCT angiography (OCT-A) imaging (Optovue, Fremont, CA). Analysis of covariance was used. 74 CD patients (33 moderate, 41 severe) and 74 controls (66 (44.6%) men; mean (SD) age 44 (14) years) were included. Compared with the controls, the severe CD patients showed a significantly reduced mean foveal avascular zone area (p = 0.001), superficial macular capillary plexus vessel density (p = 0.009) and parafoveal thickness (p < 0.001), with no difference in mean superficial capillary flow index (p = 0.06) or deep macular capillary plexus vessel density (p = 0.67). The mean foveal avascular zone was significantly lower in the severe than the moderate CD patients (p = 0.010). OCT-A can detect alterations in retinal microcirculation in patients with severe versus moderate CD and versus age- and sex-matched controls. Full article

(This article belongs to the Topic Retinal Imaging and Systemic Vascular Disease: Recent Advances and Perspective)

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Journal Name	Impact Factor	CiteScore	Launched Year	First Decision (median)	APC
Diagnostics diagnostics	3.6	3.6	2011	20.7 Days	CHF 2600
Journal of Clinical Medicine jcm	3.9	5.4	2012	17.9 Days	CHF 2600
Journal of Personalized Medicine jpm	3.4	2.6	2011	17.8 Days	CHF 2600
International Journal of Molecular Sciences ijms	5.6	7.8	2000	16.3 Days	CHF 2900

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Retinal Imaging and Systemic Vascular Disease: Recent Advances and Perspective

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