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Sen S, Khalid H, Udaya P, Raman R, Rajendram R, ElHousseini Z, Nicholson L, Kannan NB, Ramasamy K, Kumaragurupari T. Ultrastructural imaging biomarkers in diabetic macular edema: A major review. Indian J Ophthalmol 2025; 73:S7-S23. [PMID: 39723865 PMCID: PMC11834929 DOI: 10.4103/ijo.ijo_878_24] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/14/2024] [Revised: 10/02/2024] [Accepted: 10/10/2024] [Indexed: 12/28/2024] Open
Abstract
Diabetic macular edema (DME) is a vision-threatening complication of diabetic retinopathy and causes significant morbidity in patients. Anti-vascular endothelial growth factor (VEGF) agents are the mainstay of treatment for DME, with steroid implants being used for the treatment of anti-VEGF resistant eyes. Over the years, several classification systems have been devised to describe the patterns of DME using optical coherence tomography (OCT). With the advent of effective treatments, it has become imperative that imaging cues are not merely used for classifying the disease but also as biomarkers for prognostication of disease activity and treatment response. In this aspect, newer imaging findings such as hyperreflective dots, photoreceptor integrity, and disorganization of retinal inner layers have been characterized in detail by several authors. Macular perfusion analysis using OCT angiography is the latest in the armamentarium for imaging DME. In this narrative review, we have summarized all relevant literature related to the ultrastructural imaging-based biomarkers of DME and their correlation to treatment.
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Affiliation(s)
- Sagnik Sen
- Department of Medical Retina, Moorfields Eye Hospital, London, UK
- Department of Vitreoretina, St Thomas Hospital, London, UK
- UCL Institute of Ophthalmology, London, UK
- Department of Vitreoretina, Aravind Eye Hospital, Madurai, India
| | - Hagar Khalid
- Department of Medical Retina, Moorfields Eye Hospital, London, UK
- Department of Ophthalmology, Tanta University, Egypt
| | - Prithviraj Udaya
- Department of Vitreoretina, Aravind Eye Hospital, Madurai, India
| | - Rajiv Raman
- Department of Vitreoretina, Sankara Nethralaya, Chennai, Tamil Nadu, India
| | - Ranjan Rajendram
- Department of Medical Retina, Moorfields Eye Hospital, London, UK
| | - Zein ElHousseini
- Department of Ophthalmology, Royal Free London NHS Foundation Trust, London, UK
| | - Luke Nicholson
- Department of Medical Retina, Moorfields Eye Hospital, London, UK
| | | | - Kim Ramasamy
- Department of Vitreoretina, Aravind Eye Hospital, Madurai, India
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Pastore MR, Milan S, Gouigoux S, Colombo O, Rinaldi S, Cirigliano G, Tognetto D. Brolucizumab for the Treatment of Diabetic Macular Edema: An Optical Coherence Tomography-Based Analysis. Diagnostics (Basel) 2024; 14:2858. [PMID: 39767218 PMCID: PMC11674811 DOI: 10.3390/diagnostics14242858] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/18/2024] [Revised: 12/13/2024] [Accepted: 12/17/2024] [Indexed: 01/11/2025] Open
Abstract
Objectives: The objectives of this study were to evaluate the structural and functional outcomes after the loading phase with brolucizumab in switched patients with diabetic macular edema (DME) and to identify potential predictive biomarkers of treatment response. Methods: A total of 28 eyes with DME, switched to brolucizumab, were retrospectively reviewed. Main outcomes during the follow-up period, up to 6 weeks after the fifth injection, included changes in best-corrected visual acuity (BCVA), central subfield thickness (CST), macular volume, subfoveal choroidal thickness, intraretinal and subretinal fluid (IRF and SRF), cyst dimension including maximal horizontal cyst diameter (MHCD), maximal vertical cyst diameter (MVCD), width-to-height ratio (WHR), foveal avascular zone (FAZ) dimension, and vessel density (VD). Results: At the last follow-up, BCVA was significantly improved (p = 0.003). Significant reduction of CST was demonstrated after each injection time point (p < 0.05), and a dry macula was detected in 64.3% of patients at the last follow-up. The WHR was 1.23 ± 0.46, and a negative correlation to final CST (p < 0.0001) was found. In FAZ and VD analysis, no significant variation was detected. At the last disease activity assessment, the treatment regimen was q12 in 64% of patients. Conclusions: Brolucizumab leads to anatomical and functional improvements in switched eyes affected by DME. WHR may represent a predictive biomarker of treatment response.
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Motamed Shariati M, Khazaei S, Yaghoobi M. Choroidal vascularity index in health and systemic diseases: a systematic review. Int J Retina Vitreous 2024; 10:87. [PMID: 39558436 PMCID: PMC11575059 DOI: 10.1186/s40942-024-00607-8] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/23/2024] [Accepted: 11/06/2024] [Indexed: 11/20/2024] Open
Abstract
BACKGROUND The choroid, a highly vascular structure within the eye, is significantly influenced by various systemic conditions. The advent of enhanced depth optical coherence tomography has improved our ability to evaluate choroidal pathophysiology. The choroidal vascularity index (CVI), a noninvasive and reliable tool, serves as an effective means of assessing the choroidal vascular structure. Recent studies have increasingly focused on exploring CVI alterations under different systemic conditions. This study aims to provide a comprehensive summary of the latest research findings in this area. METHODS A systematic literature review was conducted on October 1, 2023, using two databases, MEDLINE (via PubMed) and Scopus. Search terms were tailored specifically for each database to ensure a thorough exploration of relevant literature. The studies identified were qualitatively assessed, with particular emphasis on outcomes related to CVI and choroidal thickness. RESULTS A total of 48 studies were included in the review, encompassing a diverse range of systemic conditions such as diabetes, central nervous system disorders, cardiovascular diseases, autoimmune disorders, and infectious diseases. Notable reductions in CVI were observed in diabetic retinopathy, autoimmune diseases, and neurodegenerative disorders. Additionally, the review highlighted variations in CVI values related to the severity of systemic diseases, indicating its potential use as a biomarker for disease progression. CONCLUSION This review highlights the significant correlation between variations in the choroidal vascularity index and diverse systemic conditions affecting hemodynamics. An enhanced understanding of CVI provides deeper insights into the pathophysiological mechanisms underlying these disorders and positions CVI as a promising biomarker for early detection and monitoring. Nevertheless, its clinical utility warrants careful assessment. Future research should address the potential limitations of CVI to fully capitalize on its diagnostic and prognostic potential.
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Affiliation(s)
- Mehrdad Motamed Shariati
- Eye Research Center, Khatam Al-Anbia Eye Hospital, Mashhad University of Medical Sciences, Gharani Boulevard, Mashhad, Iran
| | - Sahel Khazaei
- Eye Research Center, Khatam Al-Anbia Eye Hospital, Mashhad University of Medical Sciences, Gharani Boulevard, Mashhad, Iran.
| | - Mariye Yaghoobi
- Eye Research Center, Khatam Al-Anbia Eye Hospital, Mashhad University of Medical Sciences, Gharani Boulevard, Mashhad, Iran
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Sinha S, Nishant P, Morya AK, Singh A. Relationship between age and subfoveal choroidal thickness and its clinical implications. World J Diabetes 2024; 15:2251-2254. [PMID: 39582570 PMCID: PMC11580566 DOI: 10.4239/wjd.v15.i11.2251] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/31/2024] [Revised: 09/17/2024] [Accepted: 09/23/2024] [Indexed: 10/16/2024] Open
Abstract
The retrospective study by Lei et al is an investigation of the relationship between age and subfoveal choroidal thickness (SFCT) in Chinese patients with proliferative diabetic retinopathy. Elements of the study design prevent the generalizability of the study findings, limiting their clinical implications. We recommend consideration of stricter eligibility criteria, other variables like duration of diabetes, interpretation of gender-differences in SFCT, longitudinal follow-up, use of newer choroidal flow indices, comparison of values with normal controls, subgroup analysis to determine the effect of prior treatment, as well as consideration of various real-world scenarios in future studies.
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Affiliation(s)
- Sony Sinha
- Department of Ophthalmology-Vitreo-Retina, Neuro-Ophthalmology and Oculoplasty, All India Institute of Medical Sciences, Patna 801507, Bihar, India
| | - Prateek Nishant
- Department of Ophthalmology, ESIC Medical College, Patna 801103, Bihar, India
| | - Arvind K Morya
- Department of Ophthalmology, All India Institute of Medical Sciences, Hyderabad 508126, Telangana, India
| | - Arshi Singh
- Department of Ophthalmology, Guru Nanak Eye Centre, New Delhi 110001, New Delhi, India
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Samanta A, Gregori G, Muzi A, Gujar R, Mariotti C, Fruttini D, Vupparaboina KK, Chhablani J, Nicolò M, Eandi CM, Cardillo Piccolino F, Lupidi M. Optical Coherence Tomography Study of Choroidal Response to Exercise-Induced Hypertension in Chronic Central Serous Chorioretinopathy. J Clin Med 2024; 13:6580. [PMID: 39518719 PMCID: PMC11545873 DOI: 10.3390/jcm13216580] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/08/2024] [Revised: 10/23/2024] [Accepted: 10/30/2024] [Indexed: 11/16/2024] Open
Abstract
Background/Objectives: The aim of this study was to evaluate the choroidal vascular response using optical coherence tomography (OCT) in patients with chronic central serous chorioretinopathy (CSCR) during transient increases in blood pressure. Methods: This observational, case-control study enrolled chronic CSCR patients and age-matched healthy controls. OCT scans of the macula were performed at rest and during hand-grip (HG) isometric exercise. Mean ocular perfusion pressure (MOPP) and subfoveal choroidal thickness (SCT) were measured at baseline and during stress. Quantitative OCT assessment included the bright area (BA, stroma), dark area (DA, vascular lumen), and total choroidal area (CA). The choroidal vascularity index (CVI) was calculated as DA/CA to assess vascular response to stress. A comparative analysis between CSCR patients and controls was conducted. Conclusions: MOPP was significantly higher (p = 0.008) at baseline in CSCR patients and further increased under stress compared to controls. SCT and CA were both significantly higher in CSCR patients than in healthy subjects at rest and under stress (p < 0.001), but no change occurred after HG. A significant decrease in CVI (p = 0.005) was noted in controls under stress, but not in CSCR patients. Additionally, a negative correlation between CVI and MOPP was found in healthy subjects (-0.648; p = 0.043). The study demonstrated a choroidal vasoconstrictive response to stress in healthy subjects, as evidenced by a decrease in CVI, but not in CSCR patients. This suggests that CSCR patients may experience impaired choroidal blood flow regulation, resulting in potentially higher perfusion pressures during stress without compensatory vasoconstriction, potentially affecting the choriocapillaris.
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Affiliation(s)
- Anindya Samanta
- Department of Ophthalmology, Baylor College of Medicine, Lubbock, TX 77030, USA
| | - Giulia Gregori
- Eye Clinic, Department of Experimental and Clinical Medicine, Polytechnic University of Marche, 60020 Ancona, Italy; (G.G.)
| | - Alessio Muzi
- Eye Clinic, Humanitas-Gradenigo Hospital, 10153 Torino, Italy
| | - Ramkailash Gujar
- Cornea and Stem Cells Department, Dr. Shroff’s Charity Eye Hospital, Daryaganj, New Delhi 110002, India
| | - Cesare Mariotti
- Eye Clinic, Department of Experimental and Clinical Medicine, Polytechnic University of Marche, 60020 Ancona, Italy; (G.G.)
| | - Daniela Fruttini
- Department of Medicine and Surgery, Section of Internal Medicine, University of Perugia, S. Maria Della Misericordia Hospital, 06156 Perugia, Italy
| | | | - Jay Chhablani
- UPMC Eye Center, University of Pittsburgh, Pittsburgh, PA 15260, USA (J.C.)
| | - Massimo Nicolò
- Fondazione Italiana Macula ETS, Di.N.O.G.Mi., University Eye Clinic, Viale Benedetto XV 5, 16132 Genova, Italy
| | - Chiara M. Eandi
- Fondazione Italiana Macula ETS, Di.N.O.G.Mi., University Eye Clinic, Viale Benedetto XV 5, 16132 Genova, Italy
| | - Felice Cardillo Piccolino
- Fondazione Italiana Macula ETS, Di.N.O.G.Mi., University Eye Clinic, Viale Benedetto XV 5, 16132 Genova, Italy
| | - Marco Lupidi
- Eye Clinic, Department of Experimental and Clinical Medicine, Polytechnic University of Marche, 60020 Ancona, Italy; (G.G.)
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Toprak A, Koc H, Alpay A, Ugurbas SH. The effect of intravitreal anti-VEGF injections on choroidal vascular index in patients with diabetic macular edema. Cutan Ocul Toxicol 2024; 43:204-210. [PMID: 39028139 DOI: 10.1080/15569527.2024.2380325] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/27/2023] [Revised: 06/10/2024] [Accepted: 07/10/2024] [Indexed: 07/20/2024]
Abstract
PURPOSE This study aims to examine and compare the effects of intravitreal bevacizumab injection (IVB) at subfoveal 1500 micron (μm) and submacular 6000 μm in patients with diabetic macular edema (DME). METHODS Fifty eyes of 45 patients with DME who completed six doses of IVB were included in the study group, and 50 eyes of 42 patients who had diabetic retinopathy (DR) but did not receive any treatment were included in the control group. Central macular thickness (CMT), central choroidal thickness (CCT), subfoveal and total choroidal area (TCA), and choroidal vascular index (CVI) were calculated and their changes at zero, three and six months were evaluated. RESULTS At baseline, CVI was significantly lower in both the subfoveal and total macular areas in the study group (p = 0.004, p = 0.003). In the study group, a significant decrease was observed in CVI between zero and six months in the subfoveal area (p = 0.001). In the submacular area, the decrease in CVI in the study group was significant between zero to three months and zero to six months. There was moderate correlation between measurements of CVI in the subfoveal and total macular areas (r = 0.66, p < 0.001). CONCLUSION These findings indicate that intravitreal bevacizumab injection reduces the CVI and the effects of intravitreal anti-VEGF on CVI emerge earlier and more prominently in the submacular 6000 µm area.
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Affiliation(s)
- Aydin Toprak
- Kırıkhan State Hospital, Kırıkhan, Hatay, Turkey
| | - Hakan Koc
- Faculty of Medicine, Department of Ophthalmology, Giresun University, Giresun, Turkey
| | - Atilla Alpay
- Faculty of Medicine, Department of Ophthalmology, Zonguldak Bulent Ecevit University, Zonguldak, Turkey
| | - Suat Hayri Ugurbas
- Faculty of Medicine, Department of Ophthalmology, Zonguldak Bulent Ecevit University, Zonguldak, Turkey
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Bilici S, Erol TG, Bilici ME, Ugurbas SC, Ugurbas SH. Evaluation of Choroidal Structures in Children with Newly Diagnosed Type-1 Diabetes Mellitus. BEYOGLU EYE JOURNAL 2024; 9:144-148. [PMID: 39239630 PMCID: PMC11372406 DOI: 10.14744/bej.2024.36036] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 03/29/2024] [Revised: 07/17/2024] [Accepted: 07/20/2024] [Indexed: 09/07/2024]
Abstract
Objectives The objective of this study was to evaluate the subfoveal choroidal thickness (SFCT) and choroidal vascularity index (CVI) in children with newly diagnosed type 1 diabetes mellitus (T1DM). Methods A total of 80 children (40 with T1DM and 40 healthy controls) were included in this cross-sectional study. Enhanced depth imaging optical coherence tomography (EDI-OCT) images of all participants were analyzed. The SFCT, total choroidal area (TCA), luminal area (LA), stromal area (SA), and CVI measurements were obtained from EDI-OCT images and compared between groups. The effects of HbA1c, fasting plasma glucose, and axial length measurements on choroidal measurements were investigated. Results There was no significant difference between the groups according to TCA (0.84 [0.57-1.26] vs. 0.88 [0.65-1.16] mm2, p=0.745), LA (0.55 [0.41-0.79] vs. 0.59 [0.43-0.74] mm2, p=0.745), SA (0.27 [0.15-0.47] vs. 0.28 [0.15-0.47] mm2, p=0.935), and CVI (68.03 [66.5-70.5] vs. 67.75 [66.2-69.5] %, p=0.794), respectively. However, T1DM patients had thinner SFCT compared to control subjects (309.0 [327-489] and 398.5 [219-491], p<0.044). No correlation was found between HbA1c, fasting plasma glucose, axial length measurements, and SFCT, TCA, LA, SA, or CVI. Conclusion Children with newly diagnosed T1DM have thinner SCFT in comparison to healthy children, however, no significant difference in CVI was observed between the groups. Long-term follow-up should be used to confirm the impact of the DM duration on CVI.
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Affiliation(s)
- Serdar Bilici
- Department of Ophthalmology, Zonguldak Bulent Ecevit University, Faculty of Medicine, Zonguldak, Türkiye
| | - Tuba Gultekin Erol
- Department of Ophthalmology, Zonguldak Bulent Ecevit University, Faculty of Medicine, Zonguldak, Türkiye
| | - Meliha Esra Bilici
- Department of Pediatric Endocrinology, Zonguldak Bulent Ecevit University, Faculty of Medicine, Zonguldak, Türkiye
| | - Silay Canturk Ugurbas
- Department of Ophthalmology, Zonguldak Bulent Ecevit University, Faculty of Medicine, Zonguldak, Türkiye
| | - Suat Hayri Ugurbas
- Department of Ophthalmology, Zonguldak Bulent Ecevit University, Faculty of Medicine, Zonguldak, Türkiye
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Boz AAE, Çelik E, Atum M, Çakır B, Aksoy NÖ, Özmen S, Doğan E, Yuvacı İ. Use of a dexamethasone implant to treat macular edema following pars plana vitrectomy and removal of the primary epiretinal membrane. Int Ophthalmol 2024; 44:340. [PMID: 39102035 DOI: 10.1007/s10792-024-03258-8] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/23/2024] [Accepted: 07/28/2024] [Indexed: 08/06/2024]
Abstract
PURPOSE The purpose of this study was to evaluate the effectiveness and safety of an intravitreal dexamethasone (DEX) implant for the treatment of macular edema (ME) following pars plana vitrectomy (PPV) and removal of the primary epiretinal membrane (ERM) and to assess the impact of the integrity of the ellipsoid zone (EZ) and disorganization of the retinal inner layer (DRIL) grade on visual and anatomical outcomes. METHODS Forty-two pseudophakic patients who developed ME following PPV and removal of the primary stage 2-3 ERM were included. Patients were divided into two groups when ME was diagnosed via spectral domain optic coherence tomography (SD-OCT). In the DEX group (n = 22), DEX was implanted for the treatment of ME. In the control group (n = 20), only observation was conducted, without any treatment. The best-corrected visual acuity (BCVA) and macular thickness (MT) of the two groups were compared at baseline and 1, 6, and 12 months after DEX implantation. The effects of OCT parameters such as EZ integrity and DRIL grade were also evaluated in terms of decreases in MT and increases in VA in the treatment of ME with DEX implantation. Intraocular pressure (IOP), number of DEX implantations and adverse effects were also recorded. RESULTS While a statistically significant increase in the mean BCVA was observed in the DEX group (p < 0.001 at months 1, 6, and 12, respectively), no such increase was detected in the control group (p = 0.169, p = 0.065, and p = 0.058 at months 1, 6 and 12, respectively) compared with the baseline. A statistically significant decrease in the mean MT was observed in the DEX group (p < 0.001 at months 1, 6, and 12); however, no significant difference was observed in the control group (p = 0.081, p = 0.065, and p = 0.054 at months 1, 6 and 12, respectively) compared with the baseline. Significant differences were found between the two groups in terms of the increase in BCVA (p < 0.01) and decrease in MT (p < 0.01) at all visits, with the outcomes being more favorable in the DEX group. A statistically significant relationship was found between the increase in VA and EZ integrity and DRIL grade in both groups. Ten patients (45.4%) received two injections of DEX during the follow-up. An increase in IOP was observed in five patients (22.7%) who were treated with topical antiglaucomatous drops. No significant side effects were observed. CONCLUSION DEX implantation was found to be effective and safe for the treatment of ME following PPV and primary ERM removal, although some eyes may require repeated injections to achieve visual and anatomical success. Additionally, a relationship was found between EZ integrity, DRIL grade and visual-anatomical outcomes.
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Affiliation(s)
- Ali Altan Ertan Boz
- Sakarya University Training and Research Hospital, Department of Ophthalmology, Korucuk street, Korucuk, Adapazarı, 54290, Sakarya, Turkey.
| | - Erkan Çelik
- Sakarya University Training and Research Hospital, Department of Ophthalmology, Korucuk street, Korucuk, Adapazarı, 54290, Sakarya, Turkey
| | - Mahmut Atum
- Sakarya University Training and Research Hospital, Department of Ophthalmology, Korucuk street, Korucuk, Adapazarı, 54290, Sakarya, Turkey
| | - Burçin Çakır
- Sakarya University Training and Research Hospital, Department of Ophthalmology, Korucuk street, Korucuk, Adapazarı, 54290, Sakarya, Turkey
| | - Nilgün Özkan Aksoy
- Sakarya University Training and Research Hospital, Department of Ophthalmology, Korucuk street, Korucuk, Adapazarı, 54290, Sakarya, Turkey
| | - Sedat Özmen
- Sakarya University Training and Research Hospital, Department of Ophthalmology, Korucuk street, Korucuk, Adapazarı, 54290, Sakarya, Turkey
| | - Emine Doğan
- Sakarya University Training and Research Hospital, Department of Ophthalmology, Korucuk street, Korucuk, Adapazarı, 54290, Sakarya, Turkey
| | - İsa Yuvacı
- Sakarya University Training and Research Hospital, Department of Ophthalmology, Korucuk street, Korucuk, Adapazarı, 54290, Sakarya, Turkey
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Dou N, Li G, Fang D, Zhang S, Liang X, Yu S. Association between choroidopathy and photoreceptors during the early stage of diabetic retinopathy: a cross-sectional study. Graefes Arch Clin Exp Ophthalmol 2024; 262:1121-1129. [PMID: 37999773 DOI: 10.1007/s00417-023-06282-z] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/18/2023] [Revised: 09/18/2023] [Accepted: 10/12/2023] [Indexed: 11/25/2023] Open
Abstract
PURPOSE To explore the role of choroidopathy in diabetic retinopathy (DR) by investigating the correlation between alterations of choroidal vessel and photoreceptors during the early stage of DR. METHODS We performed a cross-sectional comparison of diabetic patients without DR (NDR group; n=16) and those with mild nonproliferative diabetic retinopathy (NPDR group; n=39). Optical coherence tomography (OCT) images of choroidal vessel alterations and photoreceptor structures were evaluated using the choroidal vascularity index (CVI) and adjusted ellipsoid zone (EZ) reflectivity, respectively. To evaluate the function of cone photoreceptors, the fundamental, harmonic amplitudes, the parameters S and Rmp3 were calculated from the electroretinogram (ERG). These factors were compared between groups. The correlation between the CVI and parameters describing the function and structure of the photoreceptors was evaluated. RESULTS The significant decrease was observed in the CVI in the NPDR group compared to the NDR group (0.67 ± 0.04 vs. 0.70 ± 0.06; p = 0.028), but not in the adjusted EZ reflectivity or ERG parameters. In NPDR group and merging the 2 groups, CVI was moderately positively correlated with the fundamental amplitude obtained by the flicker ERG (NPDR only: r = 0.506; p = 0.001; merge the 2 groups: r = 0.423; p = 0.001), which was regulated by the response of the cone photoreceptors. The CVI was positively and moderately correlated with the logS (NPDR only: r = 0.462; p = 0.003; merge the 2 groups: r = 0.355; p = 0.008), indicating the sensitivity of cone cell light transduction. CONCLUSION Compared to eyes without DR, CVI decreased representing choroidal vascular changes in eyes with mild NPDR. These changes may be related to the functional impairment of cone photoreceptors, especially phototransduction sensitivity, as the DR develops.
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Affiliation(s)
- Ningxin Dou
- Shenzhen Eye Hospital, Jinan University, Shenzhen Eye Institute, Shenzhen, 518040, China
- State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, 510060, China
| | - Guangyang Li
- Bio-manufacturing Engineering Laboratory, Tsinghua Shenzhen International Graduate School, Tsinghua University, Shenzhen, 518000, Guangdong, China
| | - Dong Fang
- Shenzhen Eye Hospital, Jinan University, Shenzhen Eye Institute, Shenzhen, 518040, China
| | - Shaochong Zhang
- Shenzhen Eye Hospital, Jinan University, Shenzhen Eye Institute, Shenzhen, 518040, China.
| | - Xiaoling Liang
- State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, 510060, China.
| | - Shanshan Yu
- State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, 510060, China.
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Wang Y, Yang Z, Liu X, Li Z, Wu C, Wang Y, Jin K, Chen D, Jia G, Chen X, Ye J, Huang X. PGKD-Net: Prior-guided and Knowledge Diffusive Network for Choroid Segmentation. Artif Intell Med 2024; 150:102837. [PMID: 38553151 DOI: 10.1016/j.artmed.2024.102837] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/27/2023] [Revised: 03/01/2024] [Accepted: 03/03/2024] [Indexed: 04/02/2024]
Abstract
The thickness of the choroid is considered to be an important indicator of clinical diagnosis. Therefore, accurate choroid segmentation in retinal OCT images is crucial for monitoring various ophthalmic diseases. However, this is still challenging due to the blurry boundaries and interference from other lesions. To address these issues, we propose a novel prior-guided and knowledge diffusive network (PGKD-Net) to fully utilize retinal structural information to highlight choroidal region features and boost segmentation performance. Specifically, it is composed of two parts: a Prior-mask Guided Network (PG-Net) for coarse segmentation and a Knowledge Diffusive Network (KD-Net) for fine segmentation. In addition, we design two novel feature enhancement modules, Multi-Scale Context Aggregation (MSCA) and Multi-Level Feature Fusion (MLFF). The MSCA module captures the long-distance dependencies between features from different receptive fields and improves the model's ability to learn global context. The MLFF module integrates the cascaded context knowledge learned from PG-Net to benefit fine-level segmentation. Comprehensive experiments are conducted to evaluate the performance of the proposed PGKD-Net. Experimental results show that our proposed method achieves superior segmentation accuracy over other state-of-the-art methods. Our code is made up publicly available at: https://github.com/yzh-hdu/choroid-segmentation.
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Affiliation(s)
- Yaqi Wang
- College of Media Engineering, Communication University of Zhejiang, Hangzhou, China.
| | - Zehua Yang
- Hangzhou Dianzi University, Hangzhou, China.
| | - Xindi Liu
- Department of Ophthalmology, School of Medicine, The Second Affiliated Hospital of Zhejiang University, Hangzhou, China.
| | - Zhi Li
- Hangzhou Dianzi University, Hangzhou, China.
| | - Chengyu Wu
- Department of Mechanical, Electrical and Information Engineering, Shandong University, Weihai, China.
| | - Yizhen Wang
- Hangzhou Dianzi University, Hangzhou, China.
| | - Kai Jin
- Department of Ophthalmology, School of Medicine, The Second Affiliated Hospital of Zhejiang University, Hangzhou, China.
| | - Dechao Chen
- Hangzhou Dianzi University, Hangzhou, China.
| | | | | | - Juan Ye
- Department of Ophthalmology, School of Medicine, The Second Affiliated Hospital of Zhejiang University, Hangzhou, China.
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Cui Y, Feng D, Wu C, Wang P, Cui R, Wang X, Chang W, Shang W, Zhao B, Liu J, Qin X. Quantitative assessment of OCT and OCTA parameters in diabetic retinopathy with and without macular edema: single-center cross-sectional analysis. Front Endocrinol (Lausanne) 2024; 14:1275200. [PMID: 38523868 PMCID: PMC10960358 DOI: 10.3389/fendo.2023.1275200] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/09/2023] [Accepted: 12/08/2023] [Indexed: 03/26/2024] Open
Abstract
Aim The retinal and choroidal parameters were analyzed to understand the impairment of microcirculation of both retina and choroid in patients with diabetic retinopathy (DR). Methods Fifty-five treatment-naive non-proliferative diabetic retinopathy (NPDR) patients (75 eyes) with type 2 diabetes mellitus (T2DM), including 28 patients (36 eyes) with diabetic macular edema (DME) and 27 patients (39 eyes) without DME, and 25 healthy subjects (47 eyes) were enrolled in this study. The following parameters of DR patients with and without DME were evaluated: the foveal avascular zone area (FAZ-a), FAZ perimeter (FAZ-p), FAZ circularity index (FAZ-CI), total subfoveal choroidal area (TCA), luminal area (LA), stromal area (SA), choroidal vascularity index (CVI), choriocapillaris flow area percentage, superficial capillary plexus (SCP), and deep capillary plexus (DCP). Results SCP, DCP, and the percentage of choriocapillaris flow area were significantly different between DR patients with and without DME. The DR patients presented lower LA, CVI, and FAZ-CI compared to those of healthy controls (all p < 0.05). The percentage of choriocapillaris flow area in DR patients with and without DME was significantly lower than that in healthy controls (p < 0.05). SCP and DCP were significantly correlated with FAZ-a and FAZ-p but presented insignificant associations with FAZ-CI. Conclusions Optical coherence tomography (OCT) and OCT angiography (OCTA) parameters, such as LA, CVI, FAZ-CI, and the percentage of choriocapillaris flow area, were reduced compared to those in controls, indicating that the microcirculations of the retina and choroid in the macular area were impaired in DR patients with DME and without DME.
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Affiliation(s)
- Yanyan Cui
- Department of Ophthalmology, The Second Hospital of Shandong University, Jinan, China
| | | | | | - Ping Wang
- Ophthalmological Center, Affiliated Hospital of Weifang Medical University, Weifang, China
| | - Ruoxi Cui
- Nanchang University Queen Mary School, Nanchang, China
| | - Xiaokun Wang
- Civil Aviation Medical Center of CAAC Northeast Regional Administration, Shenyang, China
| | - Weiwei Chang
- Department of Ophthalmology, Affiliated Hospital of Jining Medical University, Jining, China
| | | | - Bojun Zhao
- Department of Ophthalmology, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, China
| | - Jing Liu
- Department of Biostatistics, School of Public Health, Cheeloo College of Medicine, Shandong University, Jinan, China
| | - Xuejiao Qin
- Department of Ophthalmology, The Second Hospital of Shandong University, Jinan, China
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12
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Jing R, Sun X, Cheng J, Li X, Wang Z. Vascular changes of the choroid and their correlations with visual acuity in diabetic retinopathy. Front Endocrinol (Lausanne) 2024; 15:1327325. [PMID: 38464970 PMCID: PMC10920230 DOI: 10.3389/fendo.2024.1327325] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/24/2023] [Accepted: 02/08/2024] [Indexed: 03/12/2024] Open
Abstract
Objective To investigate changes in the choroidal vasculature and their correlations with visual acuity in diabetic retinopathy (DR). Methods The cohort was composed of 225 eyes from 225 subjects, including 60 eyes from 60 subjects with healthy control, 55 eyes from 55 subjects without DR, 46 eyes from 46 subjects with nonproliferative diabetic retinopathy (NPDR), 21 eyes from 21 subjects with proliferative diabetic retinopathy (PDR), and 43 eyes from 43 subjects with clinically significant macular edema (CSME). Swept-source optical coherence tomography (SS-OCT) was used to image the eyes with a 12-mm radial line scan protocol. The parameters for 6-mm diameters of region centered on the macular fovea were analyzed. Initially, a custom deep learning algorithm based on a modified residual U-Net architecture was utilized for choroidal boundary segmentation. Subsequently, the SS-OCT image was binarized and the Niblack-based automatic local threshold algorithm was employed to calibrate subfoveal choroidal thickness (SFCT), luminal area (LA), and stromal area (SA) by determining the distance between the two boundaries. Finally, the ratio of LA and total choroidal area (SA + LA) was defined as the choroidal vascularity index (CVI). The choroidal parameters in five groups were compared, and correlations of the choroidal parameters with age, gender, duration of diabetes mellitus (DM), glycated hemoglobin (HbA1c), fasting blood sugar, SFCT and best-corrected visual acuity (BCVA) were analyzed. Results The CVI, SFCT, LA, and SA values of patients with DR were found to be significantly lower compared to both healthy patients and patients without DR (P < 0.05). The SFCT was significantly higher in NPDR group compared to the No DR group (P < 0.001). Additionally, the SFCT was lower in the PDR group compared to the NPDR group (P = 0.014). Furthermore, there was a gradual decrease in CVI with progression of diabetic retinopathy, reaching its lowest value in the PDR group. However, the CVI of the CSME group exhibited a marginally closer proximity to that of the NPDR group. The multivariate regression analysis revealed a positive correlation between CVI and the duration of DM as well as LA (P < 0.05). The results of both univariate and multivariate regression analyses demonstrated a significant positive correlation between CVI and BCVA (P = 0.003). Conclusion Choroidal vascular alterations, especially decreased CVI, occurred in patients with DR. The CVI decreased with duration of DM and was correlated with visual impairment, indicating that the CVI might be a reliable imaging biomarker to monitor the progression of DR.
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Affiliation(s)
- Ruixia Jing
- Jinan Central Hospital, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, China
| | - Xiubin Sun
- Department of Biostatistics, School of Public Health, Cheeloo Collage of Medicine, Shandong University, Jinan, China
| | - Jimin Cheng
- Department of Ophthalmology, Central Hospital Affiliated to Shandong First Medical University, Jinan, China
| | - Xue Li
- Jinan Central Hospital, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, China
| | - Zhen Wang
- Department of Ophthalmology, Central Hospital Affiliated to Shandong First Medical University, Jinan, China
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Karasu B, Akbas YB, Aykut A, Çelebi ARC. Subthreshold Photocoagulation, Laser Endpoint Management Based on Optical Coherence Tomography Angiography in Cases of Diabetic Macular Edema Refractory to Anti-VEGF. Klin Monbl Augenheilkd 2024; 241:197-208. [PMID: 35453154 DOI: 10.1055/a-1792-3009] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/18/2022]
Abstract
PURPOSE This study aimed to determine the changes that occur in the vasculature, as based on optical coherence tomography angiography (OCTA) after non-damaging endpoint management (EpM), using a continuous wave yellow laser. The study was on eyes with diabetic macular edema (DME) that were resistant to anti-vascular endothelial growth factors (anti-VEGFs). MATERIALS AND METHODS This was a retrospective analysis of OCTA images of 44 eyes in 44 patients with DME refractory to anti-VEGF. The eyes were treated with a PASCAL Streamline yellow laser (577 nm wavelength, 200 mm spot size). Treatment was administered to the DME area and utilized 10% continuous wave laser energy and 0.50 µm beam diameter spot spacing. Best-corrected visual acuity (BCVA) and enhanced in-depth imaging with optical coherence tomography (EDI-OCT) and fundus autofluorescence (FAF) images were recorded at baseline, and 3 and 6 months posttreatment. Total choroidal area (TCA), luminal area (LA), stromal area (SA), and the choroidal vascularity index (CVI) were calculated using Image J software. The macula was divided into five quadrants in accordance with the mapping system in the Early Treatment Diabetic Retinopathy Study (ETDRS). RESULTS All patients (mean age: 58.90 ± 9.55 years) were diagnosed with diabetes mellitus type 2. Mean BCVA at baseline was 0.30 ± 0.11 logarithm of the minimum angle of resolution (logMAR) versus 0.23 ± 0.10 logMAR at 3 months (p = 0.032) and 0.17 ± 0.10 logMAR at 6 months (p = 0.013). The foveal avascular zone area (FAZ) decreased in the deep capillary plexus (DCP) from baseline to 6 months (p = 0.028). Vessel densities (VDs) of the superficial capillary plexus (SCP), DCP, and choriocapillaris decreased significantly in the fovea at 3 and 6 months compared to baseline (p < 0.05 for both follow-up time points). There were significant decreases in SCP and DCP in the superior quadrant at the end of month 6 (p = 0.001 and p = 0.038, respectively). There was a significant decrease in the nasal quadrant of the DCP and choriocapillaris at the end of month 6 (p = 0.024 and p = 0.049, respectively). Although there was a significant decrease in central macular thickness (CMT) (p < 0.001), subfoveal choroidal thickness (SFCT) (p < 0.001), and LA (p = 0.034) at months 3 and 6, there was no significant change in the CVI (p = 0.19). According to the DME recovery rate, 36 eyes (81%) were irradiated once, whereas 8 eyes (19%) were irradiated twice. CONCLUSIONS Non-damaging EpM therapy using a continuous wave yellow laser in eyes with DME that are resistant to anti-VEGFs induces significant changes in the SCP, choriocapillaris, and, most commonly, the DCP, which caused a significant decrease in VDs during 6 months of follow-up.
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Affiliation(s)
- Bugra Karasu
- Ophthalmology, Beyoglu Eye Training and Research Hospital, Içmeler Mahallesi, Piri Reis Caddesi, Tuzla State Hospital, Tuzla, Turkey
| | - Yusuf Berk Akbas
- Ophthalmology, Beyoglu Eye Training and Research Hospital, Bereketzade, Beyoglu, Turkey
| | - Aslan Aykut
- Ophthalmology, Marmara University School of Medicine, Istanbul, Turkey
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Szeto SK, Lai TY, Vujosevic S, Sun JK, Sadda SR, Tan G, Sivaprasad S, Wong TY, Cheung CY. Optical coherence tomography in the management of diabetic macular oedema. Prog Retin Eye Res 2024; 98:101220. [PMID: 37944588 DOI: 10.1016/j.preteyeres.2023.101220] [Citation(s) in RCA: 5] [Impact Index Per Article: 5.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/28/2023] [Revised: 10/24/2023] [Accepted: 10/24/2023] [Indexed: 11/12/2023]
Abstract
Diabetic macular oedema (DMO) is the major cause of visual impairment in people with diabetes. Optical coherence tomography (OCT) is now the most widely used modality to assess presence and severity of DMO. DMO is currently broadly classified based on the involvement to the central 1 mm of the macula into non-centre or centre involved DMO (CI-DMO) and DMO can occur with or without visual acuity (VA) loss. This classification forms the basis of management strategies of DMO. Despite years of research on quantitative and qualitative DMO related features assessed by OCT, these do not fully inform physicians of the prognosis and severity of DMO relative to visual function. Having said that, recent research on novel OCT biomarkers development and re-defined classification of DMO show better correlation with visual function and treatment response. This review summarises the current evidence of the association of OCT biomarkers in DMO management and its potential clinical importance in predicting VA and anatomical treatment response. The review also discusses some future directions in this field, such as the use of artificial intelligence to quantify and monitor OCT biomarkers and retinal fluid and identify phenotypes of DMO, and the need for standardisation and classification of OCT biomarkers to use in future clinical trials and clinical practice settings as prognostic markers and secondary treatment outcome measures in the management of DMO.
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Affiliation(s)
- Simon Kh Szeto
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China
| | - Timothy Yy Lai
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China
| | - Stela Vujosevic
- Department of Biomedical, Surgical and Dental Sciences, University of Milan, Milan, Italy; Eye Clinic, IRCCS MultiMedica, Milan, Italy
| | - Jennifer K Sun
- Beetham Eye Institute, Harvard Medical School, Boston, USA
| | - SriniVas R Sadda
- Doheny Eye Institute, University of California Los Angeles, Los Angeles, USA
| | - Gavin Tan
- Singapore Eye Research Institute, SingHealth Duke-National University of Singapore, Singapore
| | - Sobha Sivaprasad
- NIHR Biomedical Research Centre, Moorfields Eye Hospital NHS Foundation Trust, London, UK
| | - Tien Y Wong
- Tsinghua Medicine, Tsinghua University, Beijing, China; Singapore Eye Research Institute, Singapore
| | - Carol Y Cheung
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China.
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Raciborska A, Sidorczuk P, Konopińska J, Dmuchowska DA. Interocular Symmetry of Choroidal Parameters in Patients with Diabetic Retinopathy with and without Diabetic Macular Edema. J Clin Med 2023; 13:176. [PMID: 38202183 PMCID: PMC10779809 DOI: 10.3390/jcm13010176] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/02/2023] [Revised: 12/19/2023] [Accepted: 12/23/2023] [Indexed: 01/12/2024] Open
Abstract
This study focuses on the interocular comparison of choroidal parameters in diabetic patients with diabetic retinopathy (DR) with and without diabetic macular edema (DME), as well as in patients with unilateral DME (present in only one eye). The aim of this study was to determine the symmetry in order to obtain better insights into the pathophysiology of diabetic choroidopathy. This retrospective single-center cross-sectional study included 170 eyes from 85 patients (61 with DR and 24 controls), divided into subgroups depending on the presence of DME. The patients underwent fluorescein angiography and spectral domain optical coherence tomography examination, and the analysis included various choroidal parameters: choroidal thickness, volume, and the choroidal vascularity index (CVI). In terms of the choroidal thickness, one eye of a patient with DR, regardless of the presence, absence, or unilaterality of DME, may be treated as representative for that patient. CVI proved symmetrical for controls and patients with DR without DME. However, there was some asymmetry of CVI in patients with bilateral or unilateral DME. There was no straightforward relationship between choroidopathy and DME. Other mechanisms were also involved in the pathogenesis.
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Affiliation(s)
| | | | | | - Diana Anna Dmuchowska
- Ophthalmology Department, Medical University of Bialystok, 24a M. Sklodowskiej-Curie, 15-276 Bialystok, Poland; (A.R.); (J.K.)
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16
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Bolac R, Bas S, Ozkan EMA, Balci S, Alpogan O. Evaluation of the effect of sodium-glucose cotransporter-2 inhibitor treatment on choroidal vascular parameters in patients with type 2 diabetes mellitus. Photodiagnosis Photodyn Ther 2023; 44:103804. [PMID: 37714281 DOI: 10.1016/j.pdpdt.2023.103804] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/19/2023] [Revised: 08/29/2023] [Accepted: 09/12/2023] [Indexed: 09/17/2023]
Abstract
BACKGROUND To evaluate the effect of sodium-glucose cotransporter-2 inhibitor treatment on choroidal vascular parameters in patients with type 2 diabetes mellitus (T2DM). METHODS Twenty eyes of 20 patients with T2DM without diabetic retinopathy and 20 eyes of 20 age- and sex-matched patients as the control group were included in the study. The patients were evaluated using enhanced depth imaging optic coherence tomography before treatment and at the third month of treatment. The choroidal images were binarized into luminal areas (LAs) and stromal areas (SAs). The choroidal vascularity index (CVI) was defined as the ratio of the LA to the total circumscribed choroid area (TCA). RESULTS The mean age of the patients was 56.65±8.41 years. The patients' mean disease duration was 6.65±5.72 years, the mean HbA1c level was 8.89±1.62%, and the mean body mass index was 33.13±4.84 kg/m2. The subfoveal TCA, subfoveal LA, subfoveal SA, total TCA, total LA, and total SA values of the patient group were found to be significantly lower than those of the control group (p = 0.006, p = 0.003, p = 0.028, p = 0.001, p = 0.001, and p = 0.006, respectively). There was a significant increase in the subfoveal TCA, subfoveal LA, subfoveal SA, subfoveal CVI, total TCA, total LA, and total SA values after empagliflozin treatment compared to before empagliflozin treatment (p = 0.005, p = 0.003, p = 0.021, p = 0.032, p < 0.001, p < 0.001, and p = 0.001 respectively). CONCLUSIONS Empagliflozin provides an improvement in diabetic choroidal changes through its effect on choroidal vascularity parameters.
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Affiliation(s)
- Ruveyde Bolac
- University of Health Sciences, Haydarpasa Numune Training and Research Hospital, Department of Ophthalmology, Istanbul, Turkey.
| | - Suleyman Bas
- Sancaktepe Sehit Prof. Dr. Ilhan Varank Training and Research Hospital, Department of Internal Medicine, Istanbul, Turkey.
| | - Esma Merve Arda Ozkan
- University of Health Sciences, Haydarpasa Numune Training and Research Hospital, Department of Internal Medicine, Istanbul, Turkey
| | - Sevcan Balci
- University of Health Sciences, Haydarpasa Numune Training and Research Hospital, Department of Ophthalmology, Istanbul, Turkey
| | - Oksan Alpogan
- University of Health Sciences, Haydarpasa Numune Training and Research Hospital, Department of Ophthalmology, Istanbul, Turkey
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17
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Liang GB, Hormel TT, Wei X, Guo Y, Wang J, Hwang T, Jia Y. Single-shot OCT and OCT angiography for slab-specific detection of diabetic retinopathy. BIOMEDICAL OPTICS EXPRESS 2023; 14:5682-5695. [PMID: 38021127 PMCID: PMC10659794 DOI: 10.1364/boe.503476] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 08/18/2023] [Revised: 09/29/2023] [Accepted: 09/29/2023] [Indexed: 12/01/2023]
Abstract
In this study, we present an optical coherence tomographic angiography (OCTA) prototype using a 500 kHz high-speed swept-source laser. This system can generate a 75-degree field of view with a 10.4 µm lateral resolution with a single acquisition. With this prototype we acquired detailed, wide-field, and plexus-specific images throughout the retina and choroid in eyes with diabetic retinopathy, detecting early retinal neovascularization and locating pathology within specific retinal slabs. Our device could also visualize choroidal flow and identify signs of key biomarkers in diabetic retinopathy.
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Affiliation(s)
- Guangru B. Liang
- Department of Biomedical Engineering, Oregon Health & Science University, 3303 S.W. Bond Avenue, Portland, OR 97239, USA
- Casey Eye Institute, Oregon Health & Science University, 515 S.W. Campus Drive, Portland, OR 97239, USA
| | - Tristan T. Hormel
- Casey Eye Institute, Oregon Health & Science University, 515 S.W. Campus Drive, Portland, OR 97239, USA
| | - Xiang Wei
- Department of Biomedical Engineering, Oregon Health & Science University, 3303 S.W. Bond Avenue, Portland, OR 97239, USA
- Casey Eye Institute, Oregon Health & Science University, 515 S.W. Campus Drive, Portland, OR 97239, USA
| | - Yukun Guo
- Department of Biomedical Engineering, Oregon Health & Science University, 3303 S.W. Bond Avenue, Portland, OR 97239, USA
- Casey Eye Institute, Oregon Health & Science University, 515 S.W. Campus Drive, Portland, OR 97239, USA
| | - Jie Wang
- Department of Biomedical Engineering, Oregon Health & Science University, 3303 S.W. Bond Avenue, Portland, OR 97239, USA
- Casey Eye Institute, Oregon Health & Science University, 515 S.W. Campus Drive, Portland, OR 97239, USA
| | - Thomas Hwang
- Casey Eye Institute, Oregon Health & Science University, 515 S.W. Campus Drive, Portland, OR 97239, USA
| | - Yali Jia
- Department of Biomedical Engineering, Oregon Health & Science University, 3303 S.W. Bond Avenue, Portland, OR 97239, USA
- Casey Eye Institute, Oregon Health & Science University, 515 S.W. Campus Drive, Portland, OR 97239, USA
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18
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Bilici S, Serbest E, Ugurbas SH. Short-term Effects of Intravitreal Dexamethasone Implant on Choroidal Structure in Eyes with Refractory Diabetic Macular Edema. BEYOGLU EYE JOURNAL 2023; 8:193-197. [PMID: 37766765 PMCID: PMC10521124 DOI: 10.14744/bej.2023.73644] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 11/29/2022] [Revised: 05/20/2023] [Accepted: 07/05/2023] [Indexed: 09/29/2023]
Abstract
Objectives The objective of the study was to evaluate choroidal structural changes after intravitreal dexamethasone implant (IDI) in eyes with diabetic macular edema (DME) refractory to antivascular endothelial growth factor (VEGF) therapy. Methods Twenty-three eyes of 14 patients with DME refractory to anti-VEGF therapy were included in this retrospective study. Detailed ophthalmological examinations were recorded, and optical coherence tomography images were obtained before and 3 months after IDI. Choroidal images were binarized into the luminal area and total choroidal area. Subfoveal choroidal thickness and choroidal vascularity index (CVI) were calculated. Results The mean best-corrected visual acuity (BCVA) and central macular thickness (CMT) were improved significantly (from 0.94 to 0.81 LogMAR, p=0.02, and from 464 to 371 μ, p=0.01, respectively) after IDI. There were no significant changes in both SCFT and CVI at the end of the follow-up period (from 446.3 to 428.8 μ, p=0.51 and from 63.1 to 63.7 p=0.35, respectively). Conclusion IDI in eyes with DME refractory to anti-VEGF therapy improves BCVA and CMT but has no significant effect on SCFT and CVI in the short term.
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Affiliation(s)
- Serdar Bilici
- Department of Ophthalmology, Zonguldak Bulent Ecevit University Faculty of Medicine, Zonguldak, Türkiye
| | - Enes Serbest
- Department of Ophthalmology, Zonguldak Bulent Ecevit University Faculty of Medicine, Zonguldak, Türkiye
| | - Suat Hayri Ugurbas
- Department of Ophthalmology, Zonguldak Bulent Ecevit University Faculty of Medicine, Zonguldak, Türkiye
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Kessler LJ, Auffarth GU, Khoramnia R. Functional and Morphological Responses to Fluocinolone Acetonide 0.19 mg in Noninfectious Uveitic Macular Edema Evaluated as the Area-Under-the-Curve. J Ocul Pharmacol Ther 2023; 39:449-455. [PMID: 37384926 PMCID: PMC10516239 DOI: 10.1089/jop.2023.0027] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/06/2023] [Accepted: 05/04/2023] [Indexed: 07/01/2023] Open
Abstract
Purpose: This study investigated the impact of baseline clinical and optical coherence tomography (OCT) factors on the response to a 0.19-mg fluocinolone acetonide (FAc) implant in patients with noninfectious uveitic macular edema evaluated by the area under the curve over 24 months. Methods: A retrospective study was conducted of eyes of patients with noninfectious uveitic macular edema undergoing FAc treatment, with follow-up from baseline to 24 months. The area under the curve (AUC) of best-corrected visual acuity (BCVA) and the central macular thickness (CMT) were calculated using the trapezoidal rule. Clinical and OCT data at the time of FAc administration were collected, and associations with AUC of BCVA and CMT changes were investigated. Results: Twenty-three patients were enrolled. BCVA and CMT significantly improved after FAc implantation (P < 0.05). AUCBCVA and AUCCMT were 0.41 ± 0.33 logarithm of minimal angle of resolution/6 months and 320.15 ± 321.64 μm/6 months, respectively. Better baseline BCVA (coefficient [coef.] = 0.83, P < 0.001) and macular thickness reduction after FAc administration (coef. = -0.0001, P < 0.05) were associated with better BCVA after FAc treatment. In contrast, baseline OCT biomarkers such as ellipsoid zone reflectivity and choroidal vascularity index, sex, or disease duration before FAc injection showed no correlation with AUCBCVA and AUCCMT (P > 0.05). The younger the patient at the time of FAc injection, the greater the reduction in CMT (coef. = 1.76, P < 0.05). Conclusions: Among all clinical and morphological baseline factors, Baseline BCVA was the strongest predictor for AUCBCVA, while no association with baseline OCT features was observed. Overall, improvement of BCVA and CMT after FAc injection was maintained over 24 months. This study is registered in the German Clinical Trials Register under the DRKS-ID: DRKS00024399.
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Affiliation(s)
| | - Gerd Uwe Auffarth
- Department of Ophthalmology, University of Heidelberg, Heidelberg, Germany
| | - Ramin Khoramnia
- Department of Ophthalmology, University of Heidelberg, Heidelberg, Germany
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Bayat K, Hassanpour K, Sabbaghi H, Fekri S, Daftarian N, Motevasseli T, Suri F, Kheiri B, Yaseri M, Ahmadieh H. Choroidal structure investigated by choroidal vascularity index in patients with inherited retinal diseases. Int J Retina Vitreous 2023; 9:18. [PMID: 36978199 PMCID: PMC10044756 DOI: 10.1186/s40942-023-00457-w] [Citation(s) in RCA: 5] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/06/2023] [Accepted: 03/21/2023] [Indexed: 03/30/2023] Open
Abstract
PURPOSE To evaluate the choroidal structure in patients with inherited retinal diseases (IRDs) by investigating the choroidal vascularity index (CVI). METHODS The present study was conducted on 113 IRD patients and 113 sex- and age-matched healthy individuals. Patients' data was extracted from the Iranian National Registry for IRDs (IRDReg®). Total choroidal area (TCA) was determined between retinal pigment epithelium and choroid-scleral junction,1500 microns on either side of the fovea. Luminal area (LA) was considered as the black area corresponding to the choroidal vascular spaces, following Niblack binarization. CVI was calculated as the ratio of the LA to the TCA. CVI and other parameters were compared among different types of IRD and the control group. RESULTS The IRD diagnosis included retinitis pigmentosa (n = 69), cone-rod dystrophy (n = 15), Usher syndrome (n = 15), Leber congenital amaurosis (n = 9), and Stargardt disease (n = 5). Sixty-one (54.0%) individuals of each of the study and control groups were male. The average CVI was 0.65 ± 0.06 in the IRD patients and 0.70 ± 0.06 in the control group (P < 0.001). Accordingly, the average of TCA and LA were 2.32 ± 0.63 and 1.52 ± 0.44 mm [1] in patients with IRDs, respectively. The measurements for the TCA and the LA were significantly lower in all subtypes of IRD (P-values < 0.05). CONCLUSION CVI is significantly lower in patients with IRD than in healthy age-matched individuals. Choroidal changes in IRDs may be related to the changes in the lumen of the choroidal vessels rather than the stromal changes.
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Affiliation(s)
- Kia Bayat
- Ophthalmic Research Center, Research Institute for Ophthalmology and Vision Science, Shahid Beheshti University of Medical Sciences, Tehran, Iran
- School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
| | - Kiana Hassanpour
- Ophthalmic Research Center, Research Institute for Ophthalmology and Vision Science, Shahid Beheshti University of Medical Sciences, Tehran, Iran
- Department of Ophthalmology, Labbafinejad Medical Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran
| | - Hamideh Sabbaghi
- Ophthalmic Epidemiology Research Center, Research Institute for Ophthalmology and Vision Science, Shahid Beheshti University of Medical Sciences, Tehran, Iran
| | - Sahba Fekri
- Ophthalmic Research Center, Research Institute for Ophthalmology and Vision Science, Shahid Beheshti University of Medical Sciences, Tehran, Iran
- Department of Ophthalmology, Labbafinejad Medical Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran
| | - Narsis Daftarian
- Ocular Tissue Engineering Research Center, Research Institute for Ophthalmology and Vision Science, Shahid Beheshti University of Medical Sciences, Tehran, Iran
| | - Tahmineh Motevasseli
- Ophthalmic Research Center, Research Institute for Ophthalmology and Vision Science, Shahid Beheshti University of Medical Sciences, Tehran, Iran
| | - Fatemeh Suri
- Ophthalmic Research Center, Research Institute for Ophthalmology and Vision Science, Shahid Beheshti University of Medical Sciences, Tehran, Iran
| | - Bahareh Kheiri
- Ophthalmic Research Center, Research Institute for Ophthalmology and Vision Science, Shahid Beheshti University of Medical Sciences, Tehran, Iran
| | - Mehdi Yaseri
- Department of Epidemiology and Biostatistics, Tehran University of Medical Sciences, Tehran, Iran
| | - Hamid Ahmadieh
- Ophthalmic Research Center, Research Institute for Ophthalmology and Vision Science, Shahid Beheshti University of Medical Sciences, Tehran, Iran.
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21
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Choroidal structural analysis in ultra-high risk and first-episode psychosis. Eur Neuropsychopharmacol 2023; 70:72-80. [PMID: 36931136 DOI: 10.1016/j.euroneuro.2023.02.016] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/03/2023] [Revised: 02/02/2023] [Accepted: 02/22/2023] [Indexed: 03/19/2023]
Abstract
Both structural and functional alterations in the retina and the choroid of the eye, as parts of the central nervous system, have been shown in psychotic disorders, especially in schizophrenia. In addition, genetic and imaging studies indicate vascular and angiogenesis anomalies in the psychosis spectrum disorders. In this ocular imaging study, choroidal structure and vascularity were investigated using enhanced depth imaging (EDI) optical coherence tomography (OCT) in first-episode psychosis (FEP), ultra-high risk for psychosis (UHR-P), and age- and gender- matched healthy controls (HCs). There were no significant differences between groups in central choroidal thickness, stromal choroidal area (SCA), luminal choroidal area (LCA) and total subfoveal choroidal area. The LCA/SCA ratio (p<0.001) and the choroidal vascularity index (CVI) (p<0.001) were significantly different between FEP, UHR-P and HCs. CVI and LCA/SCA ratio were significantly higher in patients with FEP compared to help-seeking youth at UHR-P. CVI and LCA/SCA ratio were not different between UHR-P and HCs. However, CVI was higher in UHR-P compared to HCs after excluding the outliers for the sensitivity analysis (p = 0.002). Current findings suggest that choroidal thickness is normal, but there are abnormalities in choroidal microvasculature in prodromal and first-episode psychosis. Further longitudinal studies are needed to investigate oculomics, especially CVI, as a promising biomarker for the prediction of conversion to psychosis in individuals at clinical high-risk.
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22
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Szeto SKH, Hui VWK, Siu V, Mohamed S, Chan CKM, Cheung CYL, Hsieh YT, Tan CS, Chhablani J, Lai TYY, Ng DSC. Recent Advances in Clinical Applications of Imaging in Retinal Diseases. Asia Pac J Ophthalmol (Phila) 2023; 12:252-263. [PMID: 36650100 DOI: 10.1097/apo.0000000000000584] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/24/2022] [Accepted: 10/24/2022] [Indexed: 01/19/2023] Open
Abstract
Many diseases that cause visual impairment, as well as systemic conditions, manifest in the posterior segment of the eye. With the advent of high-speed, high-resolution, reliable, and noninvasive imaging techniques, ophthalmologists are becoming more dependent on ocular imaging for disease diagnosis, classification, and management in clinical practice. There are rapid advances on the indications of multimodal retinal imaging techniques, including the application of ultra-widefield fundus angiography, fundus autofluorescence, optical coherence tomography, as well as optical coherence tomography angiography. This review summarizes and highlights the clinical applications, latest indications, and interpretations of multimodal imaging in age-related macular degeneration, polypoidal choroidal vasculopathy, diabetic macular edema, central serous chorioretinopathy, diabetic retinopathy, retinal vein occlusion, and uveitis.
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Affiliation(s)
- Simon Ka-Ho Szeto
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong, China
- Hong Kong Eye Hospital, Hong Kong, China
| | - Vivian Wing Ki Hui
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong, China
- Hong Kong Eye Hospital, Hong Kong, China
| | - Vivianna Siu
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong, China
| | - Shaheeda Mohamed
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong, China
- Hong Kong Eye Hospital, Hong Kong, China
| | - Carmen K M Chan
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong, China
- Hong Kong Eye Hospital, Hong Kong, China
| | - Carol Yim Lui Cheung
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong, China
| | - Yi Ting Hsieh
- Department of Ophthalmology, National Taiwan University Hospital, Taipei, Taiwan
| | - Colin S Tan
- National Healthcare Group Eye Institute, Tan Tock Seng Hospital, Singapore
| | - Jay Chhablani
- Department of Ophthalmology, University of Pittsburgh School of Medicine, Pittsburgh, PA
| | - Timothy Y Y Lai
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong, China
- Hong Kong Eye Hospital, Hong Kong, China
- 2010 Retina and Macula Centre, Hong Kong, China
| | - Danny Siu-Chun Ng
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong, China
- Hong Kong Eye Hospital, Hong Kong, China
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23
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Estaji M, Hosseini B, Bozorg-Qomi S, Ebrahimi B. Pathophysiology and diagnosis of diabetic retinopathy: a narrative review. J Investig Med 2023; 71:265-278. [PMID: 36718824 DOI: 10.1177/10815589221145040] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/01/2023]
Abstract
Diabetes is an endocrine disorder which is known by abnormal high blood glucose levels. There are two main categories of diabetes: type I (10%-15%) and type II (85%-90%). Although type II is more common, type I is the most common form in children. Diabetic retinopathy (DR), which remains the foremost cause of losing vision in working-age populations, can be considered as the main complication of diabetes mellitus. So choosing the best method for diagnosing, tracking, and treating the DR is vital to enhance the quality of life and decrease the medical expenses. Each method for diagnosing DR has some advantages and the best way must be selected according to the points that we need to find. For writing this manuscript, we made a list of relevant keywords including diabetes, DR, pathophysiology, ultrawide field imaging, fluorescein angiography, optical coherence tomography, and optical coherence tomography-angiography, and then we started searching for studies in PubMed, Scopus, and Web of Science databases. This review article covers the pathophysiology of DR and medical imaging techniques to monitor DR. First, we introduce DR and its pathophysiology and then we present the medical imaging techniques to monitor it.
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Affiliation(s)
- Mohadese Estaji
- Department of Medical Physics and Biomedical Engineering, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran
| | - Bita Hosseini
- Bioscience Research Group, School of Health and Life Sciences, Aston University, Birmingham, UK
| | - Saeed Bozorg-Qomi
- Department of Medical Genetics, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
| | - Babak Ebrahimi
- Department of Anatomy, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran
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24
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Peng ZY, Gan L, Xue K, Sodhi A, Ye XF, Ren H, Qian J. Optical coherence tomography enhanced depth imaging of chorioretinal folds in patients with orbital tumors. Int J Ophthalmol 2023; 16:233-237. [PMID: 36816213 PMCID: PMC9922642 DOI: 10.18240/ijo.2023.02.09] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/11/2022] [Accepted: 11/29/2022] [Indexed: 02/05/2023] Open
Abstract
AIM To characterize spectral-domain optical coherence tomography (SD-OCT) features of chorioretinal folds in orbital mass imaged using enhanced depth imaging (EDI). METHODS Prospective observational case-control study was conducted in 20 eyes of 20 patients, the uninvolved eye served as a control. All the patients underwent clinical fundus photography, computed tomography, EDI SD-OCT imaging before and after surgery. Two patients with cavernous hemangiomas underwent intratumoral injection of bleomycin A5; the remaining patients underwent tumor excision. Patients were followed 1 to 14mo following surgery (average follow up, 5.8mo). RESULTS Visual acuity prior to surgery ranged from 20/20 to 20/200. Following surgery, 5 patients' visual acuity remained unchanged while the remaining 15 patients had a mean letter improvement of 10 (range 4 to 26 letters). Photoreceptor inner/outer segment defects were found in 10 of 15 patients prior to surgery. Following surgical excision, photoreceptor inner/outer segment defects fully resolved in 8 of these 10 patients. CONCLUSION Persistence of photoreceptor inner/outer segment defects caused by compression of the globe by an orbital mass can be associated with reduced visual prognosis. Our findings suggest that photoreceptor inner/outer segment defects on EDI SD-OCT could be an indicator for immediate surgical excision of an orbital mass causing choroidal compression.
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Affiliation(s)
- Zhi-Yu Peng
- Department of Ophthalmology, Eye and ENT Hospital of Fudan University, Shanghai 200031, China,Shanghai Key Laboratory of Visual Impairment and Restoration, Shanghai 200031, China
| | - Lu Gan
- Department of Ophthalmology, Eye and ENT Hospital of Fudan University, Shanghai 200031, China,Shanghai Key Laboratory of Visual Impairment and Restoration, Shanghai 200031, China
| | - Kang Xue
- Department of Ophthalmology, Eye and ENT Hospital of Fudan University, Shanghai 200031, China,Shanghai Key Laboratory of Visual Impairment and Restoration, Shanghai 200031, China
| | - Akrit Sodhi
- Wilmer Eye Institute, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA
| | - Xiao-Feng Ye
- Department of Ophthalmology, Eye and ENT Hospital of Fudan University, Shanghai 200031, China,Shanghai Key Laboratory of Visual Impairment and Restoration, Shanghai 200031, China
| | - Hui Ren
- Department of Ophthalmology, Eye and ENT Hospital of Fudan University, Shanghai 200031, China,Shanghai Key Laboratory of Visual Impairment and Restoration, Shanghai 200031, China
| | - Jiang Qian
- Department of Ophthalmology, Eye and ENT Hospital of Fudan University, Shanghai 200031, China,Shanghai Key Laboratory of Visual Impairment and Restoration, Shanghai 200031, China
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Vujosevic S, Parra MM, Hartnett ME, O'Toole L, Nuzzi A, Limoli C, Villani E, Nucci P. Optical coherence tomography as retinal imaging biomarker of neuroinflammation/neurodegeneration in systemic disorders in adults and children. Eye (Lond) 2023; 37:203-219. [PMID: 35428871 PMCID: PMC9012155 DOI: 10.1038/s41433-022-02056-9] [Citation(s) in RCA: 43] [Impact Index Per Article: 21.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/26/2021] [Revised: 03/10/2022] [Accepted: 03/31/2022] [Indexed: 01/28/2023] Open
Abstract
The retina and the optic nerve are considered extensions of the central nervous system (CNS) and thus can serve as the window for evaluation of CNS disorders. Spectral domain optical coherence tomography (OCT) allows for detailed evaluation of the retina and the optic nerve. OCT can non-invasively document changes in single retina layer thickness and structure due to neuronal and retinal glial cells (RGC) modifications in systemic and local inflammatory and neurodegenerative diseases. These can include evaluation of retinal nerve fibre layer and ganglion cell complex, hyper-reflective retinal spots (HRS, sign of activated microglial cells in the retina), subfoveal neuroretinal detachment, disorganization of the inner retinal layers (DRIL), thickness and integrity of the outer retinal layers and choroidal thickness. This review paper will report the most recent data on the use of OCT as a non invasive imaging biomarker for evaluation of the most common systemic neuroinflammatory and neurodegenerative/neurocognitive disorders in the adults and in paediatric population. In the adult population the main focus will be on diabetes mellitus, multiple sclerosis, optic neuromyelitis, neuromyelitis optica spectrum disorders, longitudinal extensive transverse myelitis, Alzheimer and Parkinson diseases, Amyotrophic lateral sclerosis, Huntington's disease and schizophrenia. In the paediatric population, demyelinating diseases, lysosomal storage diseases, Nieman Pick type C disease, hypoxic ischaemic encephalopathy, human immunodeficiency virus, leukodystrophies spinocerebellar ataxia will be addressed.
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Affiliation(s)
- Stela Vujosevic
- Department of Biomedical, Surgical and Dental Sciences, University of Milan, Milan, Italy.
- Eye Clinic, IRCCS MultiMedica, Milan, Italy.
| | - M Margarita Parra
- Department of Ophthalmology and Visual Sciences, John A. Moran Eye Center, University of Utah, Salt Lake City, UT, USA
| | - M Elizabeth Hartnett
- Department of Ophthalmology and Visual Sciences, John A. Moran Eye Center, University of Utah, Salt Lake City, UT, USA
| | - Louise O'Toole
- Department of Ophthalmology Mater Private Network, Dublin, Ireland
| | - Alessia Nuzzi
- Eye Clinic, IRCCS MultiMedica, Milan, Italy
- University of Milan, Milan, Italy
| | - Celeste Limoli
- Eye Clinic, IRCCS MultiMedica, Milan, Italy
- University of Milan, Milan, Italy
| | - Edoardo Villani
- Eye Clinic, IRCCS MultiMedica, Milan, Italy
- Department of Clinical Sciences and Community Health, University of Milan, Milan, Italy
| | - Paolo Nucci
- Department of Biomedical, Surgical and Dental Sciences, University of Milan, Milan, Italy
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İlgüy S, Işık MU. Prognostic value of choroidal vascular index in determining response to intravitreal dexamethasone implant treatment used in refractory diabetic macular edema. Lasers Med Sci 2023; 38:47. [PMID: 36680633 DOI: 10.1007/s10103-023-03711-7] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/09/2022] [Accepted: 01/11/2023] [Indexed: 01/22/2023]
Abstract
To investigate the effect of intravitreal dexamethasone (IVD) implant injection, which was used in the treatment of DME, on CVI and to investigate whether CVI can be used as a prognostic marker in the treatment of anti-VEGF resistant DME. A retrospective observational and comparative study. Twenty-five eyes of 25 patients with refractory diabetic macular edema who underwent intravitreal dexamethasone (IVD) implant and 50 eyes of 50 healthy patients were included in the study. Central macular thickness (CMT), subfoveal choroidal thickness (SFCT), luminal choroidal area (LCA), total choroidal area (TCA), stromal choroidal area (SCA), and choroidal vascularity index (CVI) were measured on optical coherence tomography. There was no significant difference between the groups in terms of age and gender. When the pre-treatment values in the IVD group were compared with the healthy group, LCA and SCA values were higher, and CVI ratios were lower in the IVD group compared to the control group. When baseline, 1st, and 3rd months after injection were compared, it was determined that there was a significant decrease in CMT and LCA. There was no statistically significant difference in SFCT, TCA, and CVI. There was a significant negative correlation between baseline CVI and 3rd month CMT after IVD (rho: - 0.643, p: 0.001). It was observed that the baseline and 1st month LCA values were significantly higher than the 3rd month. The choroidal vascular structure may be affected by IVD treatment. CVI may also have value as a prognostic marker in monitoring the response to treatment.
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Affiliation(s)
- Serdar İlgüy
- Retina Department, Department of Ophthalmology, Kastamonu Training and Research Hospital, Kastamonu, Turkey.
| | - Mehmed Uğur Işık
- Retina Department, Department of Ophthalmology, Faculty of Medicine, Kastamonu University, Kastamonu, Turkey
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27
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Gomułka K, Ruta M. The Role of Inflammation and Therapeutic Concepts in Diabetic Retinopathy-A Short Review. Int J Mol Sci 2023; 24:ijms24021024. [PMID: 36674535 PMCID: PMC9864095 DOI: 10.3390/ijms24021024] [Citation(s) in RCA: 19] [Impact Index Per Article: 9.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/07/2022] [Revised: 12/20/2022] [Accepted: 01/03/2023] [Indexed: 01/07/2023] Open
Abstract
Diabetic retinopathy (DR) as a microangiopathy is the most common complication in patients with diabetes mellitus (DM) and remains the leading cause of blindness among adult population. DM in its complicated pathomechanism relates to chronic hyperglycemia, hypoinsulinemia, dyslipidemia and hypertension-all these components in molecular pathways maintain oxidative stress, formation of advanced glycation end-products, microvascular changes, inflammation, and retinal neurodegeneration as one of the key players in diabetes-associated retinal perturbations. In this current review, we discuss the natural history of DR with special emphasis on ongoing inflammation and the key role of vascular endothelial growth factor (VEGF). Additionally, we provide an overview of the principles of diabetic retinopathy treatments, i.e., in laser therapy, anti-VEGF and steroid options.
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Affiliation(s)
- Krzysztof Gomułka
- Clinical Department of Internal Medicine, Pneumology and Allergology, Wroclaw Medical University, ul. M. Curie-Skłodowskiej 66, 50-369 Wrocław, Poland
- Correspondence:
| | - Michał Ruta
- Clinical Department of Ophthalmology, 4th Military Clinical Hospital with Polyclinic, ul. Rudolfa Weigla 5, 50-981 Wrocław, Poland
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28
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Lin Z, Yu H, Shi C, Chen H, Lin G, Shen M, Wang C. Acute hyperglycemia compromises the responses of choroidal vessels using swept-source optical coherence tomography during dark and light adaptations. Front Endocrinol (Lausanne) 2023; 14:1049326. [PMID: 36843596 PMCID: PMC9947340 DOI: 10.3389/fendo.2023.1049326] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/20/2022] [Accepted: 01/24/2023] [Indexed: 02/11/2023] Open
Abstract
PURPOSE To clarify the effects of acute hyperglycemia on the responses of choroidal structural components and vascularity index during light modulation in healthy participants using techniques including image binarization and artificial intelligence (AI) segmentation based on swept-source optical coherence tomography (SS-OCT). METHODS Twenty-four eyes of 24 healthy participants were imaged at different stages after ambient light, 40 min of dark adaptation, and 5 min of light adaptation in two imaging sessions: control and after receiving 75 g of oral glucose solution. The choroidal structural parameters, including luminal volume (LV), stromal volume (SV), total choroidal volume (TCV), and choroidal vascularity index (CVI) within a 6 mm area were determined using a custom algorithm based on image binarization and AI segmentation of SS-OCT. These measurements were compared among the conditions after adjusting for axial length, age to identify the differences. RESULTS In the dark, CVI decreased (-0.36 ± 0.09%) significantly in acute hyperglycemia compared to the control condition. During the transition to ambient light, there was an increasing trend in the choroidal parameters compared with the control experiment. However, only TCV (0.38 ± 0.17 mm3) and LV (0.27 ± 0.10 mm3) showed a significant increase at the time point of 5 min after ambient light. CONCLUSION Analysis of choroidal structural parameters and CVI based on SS-OCT images is a potentially powerful method to objectively reflect subtle changes in neurovascular coupling between the choroid and photoreceptor during dark adaptation.
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Affiliation(s)
- Zhiyang Lin
- Eye Hospital and School of Ophthalmology and Optometry, Wenzhou Medical University, Wenzhou, China
| | - Huankai Yu
- Eye Hospital and School of Ophthalmology and Optometry, Wenzhou Medical University, Wenzhou, China
- Oujiang Laboratory (Zhejiang Lab for Regenerative Medicine, Vision and Brain Health), Eye Hospital, Wenzhou Medical University, Wenzhou, Zhejiang, China
| | - Ce Shi
- Eye Hospital and School of Ophthalmology and Optometry, Wenzhou Medical University, Wenzhou, China
| | - Hongling Chen
- Eye Hospital and School of Ophthalmology and Optometry, Wenzhou Medical University, Wenzhou, China
| | - Guangqing Lin
- Eye Hospital and School of Ophthalmology and Optometry, Wenzhou Medical University, Wenzhou, China
| | - Meixiao Shen
- Eye Hospital and School of Ophthalmology and Optometry, Wenzhou Medical University, Wenzhou, China
- Oujiang Laboratory (Zhejiang Lab for Regenerative Medicine, Vision and Brain Health), Eye Hospital, Wenzhou Medical University, Wenzhou, Zhejiang, China
- *Correspondence: Meixiao Shen, ; Chenxiao Wang,
| | - Chenxiao Wang
- Eye Hospital and School of Ophthalmology and Optometry, Wenzhou Medical University, Wenzhou, China
- *Correspondence: Meixiao Shen, ; Chenxiao Wang,
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Udaondo Mirete P, Muñoz-Morata C, Albarrán-Diego C, España-Gregori E. Influence of Intravitreal Therapy on Choroidal Thickness in Patients with Diabetic Macular Edema. J Clin Med 2023; 12:jcm12010348. [PMID: 36615148 PMCID: PMC9821174 DOI: 10.3390/jcm12010348] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/26/2022] [Revised: 11/27/2022] [Accepted: 11/28/2022] [Indexed: 01/03/2023] Open
Abstract
OBJECTIVE This study aimed to analyze the variation in subfoveal choroidal thickness (SFCT) and its relationship with the variation in central macular thickness (CME) in response to intravitreal therapy with an antiangiogenic (anti-VEGF) drug or corticosteroid in type 2 diabetic patients with diabetic macular edema (DME). MATERIAL AND METHODS This retrospective study included 70 eyes of 35 patients: 26 eyes received 4-5 intravitreal injections of aflibercept, 26 eyes were treated with a single intravitreal implant injection of dexamethasone, and 18 eyes without DME did not receive intravitreal therapy. SPECTRALIS® optical coherence tomography (OCT) (Heidelberg Engineering, Heidelberg, Germany) was used to measure the SFCT and CME before and at the end of the follow-up period. RESULTS The mean reductions in CME were 18.8 +/- 14.7% (aflibercept) and 29.7 +/- 16.9% (dexamethasone). The mean reductions in SFCT were 13.8 +/- 13.1% (aflibercept) and 19.5 +/- 9.6% (dexamethasone). The lowering effects of both parameters were significantly greater in the group treated with the dexamethasone implant (p = 0.022 and p = 0.046 for CMT and SFCT, respectively). Both therapies significantly decreased both CME and SFCT, independent of factors such as age, sex, previous intravitreal therapy, antidiabetic treatment, and the time of diabetes progression. There were no changes in the mean values of CME and SFCT in the untreated eyes. CONCLUSIONS SFCT significantly decreased in response to intravitreal therapy with anti-VEGF or corticosteroids, irrespective of age, sex, previous intravitreal therapy, antidiabetic treatment, and the time of diabetes progression. There was a correlation between the changes in CME and SFCT after intravitreal therapy with aflibercept or dexamethasone implantation. SFCT was not a good predictor of the CME response but could be used to monitor the response to treatment. Local intravitreal therapy only affected the treated eye.
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Affiliation(s)
- Patricia Udaondo Mirete
- Department of Ophthalmology, Hospital Universitario y Politécnico La Fe, 46026 Valencia, Spain
- Aiken Clinic, 46004 Valencia, Spain
- Department of Surgery, Universidad de Valencia, 46010 Valencia, Spain
- Correspondence: ; Tel.: +34-647869228
| | | | | | - Enrique España-Gregori
- Department of Ophthalmology, Hospital Universitario y Politécnico La Fe, 46026 Valencia, Spain
- Department of Surgery, Universidad de Valencia, 46010 Valencia, Spain
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Khalatyan AS, Yusef YN. [Choroidal changes in patients with diabetes mellitus]. Vestn Oftalmol 2023; 139:158-165. [PMID: 38235643 DOI: 10.17116/oftalma2023139061158] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/19/2024]
Abstract
Diabetic retinopathy (DR) is a microvascular complication of diabetes mellitus (DM) and considered one of the leading causes of vision loss worldwide. The choroid supplies blood to the retina, photoreceptors and the retinal pigment epithelium, it is essential for metabolic exchange in the retina. Many experimental studies have reported that choroidal pathology in diabetic patients may play a role in the development of DR. Choroidal thickness (CT) can be used to assess the vascularization of the choroid. Choroidal vascularity index (CVI) is also used as a marker in assessment of choroidal vascularization. Many studies have been conducted to evaluate choroidal changes in various eye diseases. However, the data on CT in DM patients, especially in those with DR, are conflicting. Thus, the choroidal status in diabetic patients with or without DR remains controversial. In this systematic review we analyze a number of articles dedicated to the relationship between structural changes in the choroid in patients with diabetes mellitus and diabetic retinopathy of different stages, paying particular attention to choroidal thickness and certain other parameters that allow assessment of choroidal changes.
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Affiliation(s)
- A S Khalatyan
- Krasnov Research Institute of Eye Diseases, Moscow, Russia
| | - Yu N Yusef
- Krasnov Research Institute of Eye Diseases, Moscow, Russia
- I.M. Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia
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Gujar R, Cagini C, Fruttini D, Corbucci R, Rasheed MA, Vupparaboina KK, Mariotti C, Chhablani J, Lupidi M. Choroidal vascularity profile in diabetic eyes using wide field optical coherence tomography. Eur J Ophthalmol 2022; 33:11206721221143161. [PMID: 36457221 DOI: 10.1177/11206721221143161] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/17/2024]
Abstract
PURPOSE To report the wide-field choroidal vascularity up to the mid-equator area in diabetic retinopathy (DR) subjects using wide-field optical coherence tomography (WF-OCT). DESIGN Prospective, Cross-sectional study. PARTICIPANTS Forty-seven eyes of 25 DR subjects. METHODS WF-OCT images (55 degrees) were obtained using Spectralis HRA + OCT (Heidelberg Engineering, Germany) in extremes of gazes in all quadrants and manual montages were created to obtain wide field images up to mid equator. A previously reported semi-automated algorithm was used to calculate choroidal vascularity profile (CVI). Regression analysis was performed to identify the factors influencing CVI. RESULTS Forty-seven eyes from 25 patients were enrolled in the study. The mean age was 68.4 ± 10.6 years. The refractive error (spherical equivalent) ranged from -2.25 to +3.75 diopters. Most common DR grade among study subjects was moderate NPDR (29.41%) and 74.5% eyes had diabetic macular edema (DME). The mean CVI in the macular area (58.29 ± 3.63) was significantly lower than in any of the other fundus areas (all p ˂ 0.01). The maximum CVI was seen in the nasal region (66.60 ± 5.61), followed by temporal (65.69 ± 3.81), superior (65.01 ± 4.87), and inferior (63.80 ± 5.42). The vertical macular area had the least coefficient of variation (CV) of CVI (0.06) while the inferior quadrant had the highest CV (0.08). CONCLUSION The current study describes the CVI profile on WF-OCT in DR eyes up to mid-equator. The significant increase of the CVI compared to healthy subjects and its significant regional variations introduce this novel quantitative parameter as a reliable biomarker of the diabetes-induced choroidal microangiopathy.
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Affiliation(s)
- Ramkailash Gujar
- Department of Medicine and Surgery, Section of Ophthalmology, 60250University of Perugia, S. Maria della Misericordia Hospital, Perugia, Italy
| | - Carlo Cagini
- Department of Medicine and Surgery, Section of Ophthalmology, 60250University of Perugia, S. Maria della Misericordia Hospital, Perugia, Italy
| | - Daniela Fruttini
- Department of Internal Medicine, 60250University of Perugia, S. Maria della Misericordia Hospital, Perugia, Italy
| | - Roberta Corbucci
- Department of Medicine and Surgery, Section of Ophthalmology, 60250University of Perugia, S. Maria della Misericordia Hospital, Perugia, Italy
| | | | | | - Cesare Mariotti
- Eye Clinic, Department of Experimental and Clinical Medicine, Polytechnic University of Marche, Ancona, Italy
| | - Jay Chhablani
- Department of Ophthalmology, 6595UPMC Eye Center, University of Pittsburgh, Pittsburgh, USA
| | - Marco Lupidi
- Eye Clinic, Department of Experimental and Clinical Medicine, Polytechnic University of Marche, Ancona, Italy
- Fondazione per la Macula Onlus, Di.N.O.G.Mi., UniversityEye Clinic, Genova, Italy
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Wang Y, Chen S, Lin J, Chen W, Huang H, Fan X, Cao X, Shen M, Ye J, Zhu S, Xue A, Lu F, Shao Y. Vascular Changes of the Choroid and Their Correlations With Visual Acuity in Pathological Myopia. Invest Ophthalmol Vis Sci 2022; 63:20. [DOI: 10.1167/iovs.63.12.20] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/16/2022] Open
Affiliation(s)
- Yiyi Wang
- School of Ophthalmology and Optometry, Wenzhou Medical University, Wenzhou, China
| | - Sisi Chen
- School of Ophthalmology and Optometry, Wenzhou Medical University, Wenzhou, China
- Wenzhou Institute, University of Chinese Academy of Sciences, Wenzhou, China
| | - Jue Lin
- School of Ophthalmology and Optometry, Wenzhou Medical University, Wenzhou, China
| | - Wen Chen
- School of Ophthalmology and Optometry, Wenzhou Medical University, Wenzhou, China
| | - Huimin Huang
- School of Ophthalmology and Optometry, Wenzhou Medical University, Wenzhou, China
| | - Xin Fan
- School of Ophthalmology and Optometry, Wenzhou Medical University, Wenzhou, China
| | - Xinyuan Cao
- School of Ophthalmology and Optometry, Wenzhou Medical University, Wenzhou, China
| | - Meixiao Shen
- School of Ophthalmology and Optometry, Wenzhou Medical University, Wenzhou, China
| | - Jie Ye
- School of Ophthalmology and Optometry, Wenzhou Medical University, Wenzhou, China
| | - Shuangqian Zhu
- School of Ophthalmology and Optometry, Wenzhou Medical University, Wenzhou, China
| | - Anquan Xue
- School of Ophthalmology and Optometry, Wenzhou Medical University, Wenzhou, China
| | - Fan Lu
- School of Ophthalmology and Optometry, Wenzhou Medical University, Wenzhou, China
- Wenzhou Institute, University of Chinese Academy of Sciences, Wenzhou, China
| | - Yilei Shao
- School of Ophthalmology and Optometry, Wenzhou Medical University, Wenzhou, China
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Jiang J, Liu J, Yang J, Jiang B. Optical coherence tomography evaluation of choroidal structure changes in diabetic retinopathy patients: A systematic review and meta-analysis. Front Med (Lausanne) 2022; 9:986209. [PMID: 36341274 PMCID: PMC9630657 DOI: 10.3389/fmed.2022.986209] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/04/2022] [Accepted: 10/03/2022] [Indexed: 03/13/2025] Open
Abstract
INTRODUCTION Diabetic retinopathy (DR) is one of the major causes of blindness among working-aged adults worldwide. This study aimed to evaluate the differences in the subfoveal choroidal thickness (SFCT) and choroidal vascularity index (CVI) using optical coherence tomography (OCT) of patients with diabetic eyes with no retinopathy (NDR) and with diabetic retinopathy (DR). METHODS We performed a comprehensive literature search of the PubMed, Embase, and Cochrane Library databases up to October 2021. The weighted mean difference (WMD) with the 95% confidence interval (CI) was pooled for continuous outcomes. RESULTS Twenty-three cross-sectional studies comprising 2,534 eyes including 1,070 NDR eyes, 1,464 DR eyes were included in the systematic review and meta-analysis. The pooled results showed SFCT was significantly thicker in DR than in NDR patients after adjusting for axial length (WMD = 27.90 μm; 95% CI: 11.51 to 44.28; P = 0.001), and the CVI was significantly lower in DR patients (WMD = -1.59; 95% CI: -2.67 to -0.52; P = 0.004). CONCLUSION We described changes in the SFCT and CVI in DR. Resultantly, the CVI and SFCT may be valuable parameters for monitoring the onset of DR and helpful for a better understanding of the role of the choroid in the pathological process of DR. SYSTEMATIC REVIEW REGISTRATION https://www.crd.york.ac.uk/prospero/#myprospero, CRD42021228738.
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Affiliation(s)
- Jikuan Jiang
- Department of Ophthalmology of Second Xiangya Hospital, Central South University, Changsha, China
- Hunan Clinical Research Center of Ophthalmic Disease, Changsha, China
| | - Jingyuan Liu
- Department of Ophthalmology of Second Xiangya Hospital, Central South University, Changsha, China
- Hunan Clinical Research Center of Ophthalmic Disease, Changsha, China
| | - Jia Yang
- Department of Ophthalmology of Second Xiangya Hospital, Central South University, Changsha, China
- Hunan Clinical Research Center of Ophthalmic Disease, Changsha, China
| | - Bing Jiang
- Department of Ophthalmology of Second Xiangya Hospital, Central South University, Changsha, China
- Hunan Clinical Research Center of Ophthalmic Disease, Changsha, China
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Correlation between Choroidal Vascularity Index and Outer Retina in Patients with Diabetic Retinopathy. J Clin Med 2022; 11:jcm11133882. [PMID: 35807164 PMCID: PMC9267134 DOI: 10.3390/jcm11133882] [Citation(s) in RCA: 9] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/02/2022] [Revised: 06/26/2022] [Accepted: 07/01/2022] [Indexed: 02/04/2023] Open
Abstract
The choroid supplies blood to the outer retina. We quantified outer retinal and choroidal parameters to understand better the pathogenesis of diabetic retinopathy (DR) and diabetic macular edema (DME). The retrospective cross-sectional single-center study included 210 eyes from 139 diabetic patients and 76 eyes from 52 healthy controls. Spectral-domain optical coherence tomography (OCT) was carried out with a Spectralis HRA + OCT imaging device. The outer retinal layer (ORL), outer nuclear layer (ONL), and choroidal thicknesses were assessed along with the choroidal vascularity index (CVI). The presence of DR, whether with DME or without, was associated with choroidal thinning (p < 0.001). Compared with the controls, patients with DR without DME presented with lower ORL and ONL thickness (p < 0.001), whereas those with DR and DME had higher values of both parameters (p < 0.001). Significant correlations between outer retinal and choroidal parameters were found only in patients with DR without DME (ORL with choroidal thickness: p = 0.003, rho = 0.34; ORL with CVI: p < 0.001, rho = 0.49, ONL with CVI: p < 0.027, rho = 0.25). No correlations between choroidal and outer retinal parameters were observed in the controls and patients with DR and concomitant DME. Aside from diabetic choroidopathy, other pathogenic mechanisms seem to predominate in the latter group.
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Hui VWK, Szeto SKH, Tang F, Yang D, Chen H, Lai TYY, Rong A, Zhang S, Zhao P, Ruamviboonsuk P, Lai CC, Chang A, Das T, Ohji M, Huang SS, Sivaprasad S, Wong TY, Lam DSC, Cheung CY. Optical Coherence Tomography Classification Systems for Diabetic Macular Edema and Their Associations With Visual Outcome and Treatment Responses - An Updated Review. Asia Pac J Ophthalmol (Phila) 2022; 11:247-257. [PMID: 34923521 DOI: 10.1097/apo.0000000000000468] [Citation(s) in RCA: 17] [Impact Index Per Article: 5.7] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/26/2022] Open
Abstract
ABSTRACT Optical coherence tomography (OCT) is an invaluable imaging tool in detecting and assessing diabetic macular edema (DME). Over the past decade, there have been different proposed OCT-based classification systems for DME. In this review, we present an update of spectral-domain OCT (SDOCT)-based DME classifications over the past 5 years. In addition, we attempt to summarize the proposed OCT qualitative and quantitative parameters from different classification systems in relation to disease severity, risk of progression, and treatment outcome. Although some OCT-based measurements were found to have prognostic value on visual outcome, there has been a lack of consensus or guidelines on which parameters can be reliably used to predict treatment outcomes. We also summarize recent literatures on the prognostic value of these parameters including quantitative measures such as macular thickness or volume, central subfield thickness or foveal thickness, and qualitative features such as the morphology of the vitreoretinal interface, disorganization of retinal inner layers, ellipsoid zone disruption integrity, and hyperreflec-tive foci. In addition, we discuss that a framework to assess the validity of biomarkers for treatment outcome is essentially important in assessing the prognosis before deciding on treatment in DME. Finally, we echo with other experts on the demand for updating the current diabetic retinal disease classification.
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Affiliation(s)
- Vivian W K Hui
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong, china
- Hong Kong Eye Hospital, Hong Kong, China
| | - Simon K H Szeto
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong, china
- Hong Kong Eye Hospital, Hong Kong, China
| | - Fangyao Tang
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong, china
| | - Dawei Yang
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong, china
| | - Haoyu Chen
- Joint Shantou International Eye Centre of Shantou University and The Chinese University of Hong Kong, Shantou, Guangdong, China
| | - Timothy Y Y Lai
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong, china
- 2010 Retina & Macula Center, Kowloon, Hong Kong
| | - Ao Rong
- Department of Ophthalmology, Tongji Hospital Affiliated to Tongji University, Shanghai, China
- Shanghai Xin Shi Jie Eye Hospital, Shanghai, China
| | | | - Peiquan Zhao
- Department of Ophthalmology, Xin Hua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Paisan Ruamviboonsuk
- Department of Ophthalmology, College of Medicine, Rangsit University, Rajavithi Hospital, Bangkok, Thailand
| | - Chi-Chun Lai
- Department of Ophthalmology, Chang Gung Memorial Hospital, Linkou Medical Center, Taoyuan, Taiwan
| | - Andrew Chang
- Sydney Retina Clinic, Sydney Eye Hospital, University of Sydney, Sydney, NSw, Australia
| | - Taraprasad Das
- Smt. Kanuri Santhamma Center for Vitreoretinal Diseases, Kallam Anji Reddy Campus, LV Prasad Eye Institute, Hyderabad, India
| | - Masahito Ohji
- Department of Ophthalmology, Shiga University of Medical Science, Otsu, Japan
| | - Suber S Huang
- Retina Center of Ohio, Cleveland, OH, US
- Bascom Palmer Eye Institute, University of Miami, Miami, FL, US
| | - Sobha Sivaprasad
- NIHR Moorfields Biomedical Research Centre, Moorfields Eye Hospital, London, UK
| | - Tien Yin Wong
- Singapore Eye Research Institute, Singapore National Eye Centre, Singapore
- Duke-NUS Medical School, Singapore
| | - Dennis S C Lam
- C-MER International Eye Research Center of The Chinese University of Hong Kong (Shenzhen), Shenzhen, China
- C-MER Dennis Lam & Partners Eye Center, C-MER International Eye Care Group, Hong Kong, China
| | - Carol Y Cheung
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong, china
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Kung EW, Chan VT, Tang Z, Yang D, Sun Z, Wang YM, Chan C, Kwan MC, Shi J, Cheung CY. Alterations in the Choroidal Sublayers in Relationship to Severity and Progression of Diabetic Retinopathy: A Swept-Source OCT Study. OPHTHALMOLOGY SCIENCE 2022; 2:100130. [PMID: 36249687 PMCID: PMC9560641 DOI: 10.1016/j.xops.2022.100130] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 09/04/2021] [Revised: 02/14/2022] [Accepted: 02/18/2022] [Indexed: 12/03/2022]
Abstract
Purpose To examine the association of baseline choroidal sublayers metrics with the risk of diabetic retinopathy (DR) progression over 2 years, with adjustment for confounding factors that affect choroidal measurements. Design Prospective, observational cohort study. Participants One hundred three eyes from 62 patients with diabetes mellitus (DM). Methods Patients were followed up at 6-month intervals for at least 2 years. Choroidal metrics including choroidal area, choroidal thickness (CT), and choroidal vascularity index were measured for both (1) the choriocapillaris plus Sattler's layer and (2) the Haller's layer within the subfoveal and parafoveal region. Cox proportional models were constructed to estimate the relationship between baseline choroidal metrics and DR progression, adjusted for intereye correlation, established risk factors (i.e., duration of DM, glycated hemoglobin [HbA1c] level, body mass index [BMI], use of insulin, and mean arterial blood pressure [MABP]) and confounding factors of choroidal measurements (i.e., age and axial length). Additional predictive value of choroidal metrics was assessed using the C-statistic. Main Outcome Measures Hazard ratios (HRs) calculated by Cox proportional hazards model to demonstrate the associations between baseline choroidal metrics and DR progression. Results After adjusting for age, axial length, and intereye correlation, choroidal metrics in Haller's layer at baseline that were associated with a higher risk of DR progression included increases in subfoveal choroidal area (HR, 2.033; 95% confidence interval [CI], 1.179-3.505; P = 0.011), subfoveal plus parafoveal choroidal area (HR, 1.909; 95% CI, 1.096-3.326; P = 0.022), subfoveal CT (HR, 2.032; 95% CI, 1.181-3.498; P = 0.010), and subfoveal plus parafoveal CT (HR, 1.908; 95% CI, 1.097-3.319; P = 0.022). These associations remained statistically significant after additionally adjusting for duration of DM, HbA1c level, BMI, use of insulin, and MABP. Addition of these choroidal metrics significantly improved the discrimination for DR progression when compared with established risk factors alone (e.g., duration of DM and HbA1c; increase in C-statistic ranged from 8.08% to 9.67% [P < 0.05]). Conclusions Eyes with a larger choroidal area and CT in Haller's layer at baseline were associated with a higher risk of DR progression over 2 years.
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Key Words
- BMI, body mass index
- CI, confidence interval
- CSI, choroid–sclera interface
- CT, choroidal thickness
- CVI, choroidal vascularity index
- Choroid
- DM, diabetes mellitus
- DME, diabetic macular edema
- DR progression
- DR, diabetic retinopathy
- Diabetic choroidopathy
- Diabetic retinopathy
- HR, hazard ratio
- HbA1c, glycated hemoglobin
- MABP, mean arterial blood pressure
- NPDR, nonproliferative diabetic retinopathy
- PDR, proliferative diabetic retinopathy
- SS, swept-source
- Swept-source OCT
- VA, visual acuity
- VEGF, vascular endothelial growth factor
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Affiliation(s)
- Erica W.T. Kung
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China
| | - Victor T.T. Chan
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China
| | - Ziqi Tang
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China
| | - Dawei Yang
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China
| | - Zihan Sun
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China
| | - Yu Meng Wang
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China
| | - C.H. Chan
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China
| | - Michael C.H. Kwan
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China
| | - Jian Shi
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China
| | - Carol Y. Cheung
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China
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37
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Wang W, Li L, Wang J, Chen Y, Kun X, Gong X, Wei D, Wang D, Liang X, Liu H, Huang W. Macular Choroidal Thickness and the Risk of Referable Diabetic Retinopathy in Type 2 Diabetes: A 2-Year Longitudinal Study. Invest Ophthalmol Vis Sci 2022; 63:9. [PMID: 35420642 PMCID: PMC9034727 DOI: 10.1167/iovs.63.4.9] [Citation(s) in RCA: 10] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/17/2021] [Accepted: 02/19/2022] [Indexed: 11/27/2022] Open
Abstract
Purpose The purpose of this study was to evaluate the associations between choroidal thickness (CT) and the 2-year incidence of referable diabetic retinopathy (RDR). Methods This was a prospective cohort study. Patients with type 2 diabetes in Guangzhou, China, aged 30 to 80 years underwent comprehensive examinations, including standard 7-field fundus photography. Macular CT was measured using a commercial swept-source optical coherence tomography (SS-OCT) device (DRI OCT Triton; Topcon, Tokyo, Japan). The relative risk (RR) with 95% confidence intervals (CIs) was used to quantify the association between CT and new-onset RDR. The prognostic value of CT was assessed using the area under the receiver operating characteristic curve (AUC), net reclassification improvement (NRI), and integrated discrimination improvement (IDI). Results A total of 1345 patients with diabetes were included in the study, and 120 (8.92%) of them had newly developed RDR at the 2-year follow-up. After adjusting for other factors, the increased RDR risk was associated with greater HbA1c (RR = 1.35, 95% CI = 1.17-1.55, P < 0.001), higher systolic blood pressure (SBP; RR = 1.02, 95% CI = 1.01-1.03, P = 0.005), lower triglyceride (TG) level (RR = 0.81, 95% CI = 0.69-0.96, P = 0.015), presence of diabetic retinopathy (DR; RR = 8.16, 95% CI = 4.47-14.89, P < 0.001), and thinner average CT (RR = 0.903, 95% CI = 0.871-0.935, P < 0.001). The addition of average CT improved NRI (0.464 ± 0.096, P < 0.001) and IDI (0.0321 ± 0.0068, P < 0.001) for risk of RDR, and it also improved the AUC from 0.708 (95% CI = 0.659-0.757) to 0.761 (95% CI = 0.719-0.804). Conclusions CT thinning measured by SS-OCT is an early imaging biomarker for the development of RDR, suggesting that alterations in CT play an essential role in DR occurrence.
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Affiliation(s)
- Wei Wang
- Zhongshan Ophthalmic Center, State Key Laboratory of Ophthalmology, Sun Yat-Sen University, Guangzhou, People's Republic of China
| | - Longyue Li
- School of Medicine, Sun Yat-Sen University, Guangzhou, People's Republic of China
| | - Jun Wang
- Zhongshan Ophthalmic Center, State Key Laboratory of Ophthalmology, Sun Yat-Sen University, Guangzhou, People's Republic of China
| | - Yifan Chen
- John Radcliffe Hospital, Oxford University Hospitals NHS Foundation Trust, Oxford, United Kingdom
| | - Xiong Kun
- Zhongshan Ophthalmic Center, State Key Laboratory of Ophthalmology, Sun Yat-Sen University, Guangzhou, People's Republic of China
| | - Xia Gong
- Zhongshan Ophthalmic Center, State Key Laboratory of Ophthalmology, Sun Yat-Sen University, Guangzhou, People's Republic of China
| | - Daheng Wei
- Institute of Eyes, Jinzhou Medical University, Jinzhou, Liaoning, People's Republic of China
| | - Dongning Wang
- Institute of Eyes, Jinzhou Medical University, Jinzhou, Liaoning, People's Republic of China
| | - Xiaolin Liang
- Zhongshan Ophthalmic Center, State Key Laboratory of Ophthalmology, Sun Yat-Sen University, Guangzhou, People's Republic of China
| | - Hua Liu
- Institute of Eyes, Jinzhou Medical University, Jinzhou, Liaoning, People's Republic of China
| | - Wenyong Huang
- Zhongshan Ophthalmic Center, State Key Laboratory of Ophthalmology, Sun Yat-Sen University, Guangzhou, People's Republic of China
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38
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Nicolini N, Tombolini B, Barresi C, Pignatelli F, Lattanzio R, Bandello F, Cicinelli MV. Assessment of Diabetic Choroidopathy Using Ultra-Widefield Optical Coherence Tomography. Transl Vis Sci Technol 2022; 11:35. [PMID: 35353150 PMCID: PMC8976931 DOI: 10.1167/tvst.11.3.35] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/18/2022] Open
Abstract
Purpose The purpose of this study was to investigate a confocal scanning laser ophthalmoscopy (cSLO) ultra-widefield (UWF) swept-source optical coherence tomography (S-SOCT) in assessment of diabetic choroidopathy and to evaluate the agreement of measurements with a spectral-domain OCT (SD-OCT) instrument. Methods We conducted a cross-sectional study of patients with diabetes evaluating the choroidal vascularity index (CVI) in the nasal, temporal, and central macula segments of a UWF SS-OCT scan centered to the fovea. UWF pseudocolored fundus images were used for diabetic retinopathy (DR) severity staging. The CVI values were compared between different degrees of severity of DR and different posterior-pole sectors with linear mixed models. Central macula CVI measurements were repeated on SD-OCT scans; the interobserver intraclass coefficient (ICC) was calculated between SS-OCT and SD-OCT. Results A total of 151 eyes of 85 patients were included. The CVI values decreased from nonproliferative DR to proliferative DR, with high-risk proliferative DR having significantly lower CVI values than moderate to severe nonproliferative DR (P = 0.03). The central macula region was the most evidently affected; the nasal sector was the least affected. The agreement between SS-OCT and SD-OCT was moderate (ICC = 0.50). Conclusions Diabetic choroidopathy progresses with worsening of DR toward proliferative disease; choroidal depletion is more prominent in the macula. Caution is recommended in comparing CVI values between different devices. Translational Relevance Choroidal vascularity informs about the severity of DR and its complications, such as macular edema. The agreement between readers and between instruments may be suboptimal in certain cases.
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Affiliation(s)
- Nicolò Nicolini
- School of Medicine, Vita-Salute San Raffaele University, Milan, Italy.,Department of Ophthalmology, IRCCS San Raffaele Scientific Institute, Milan, Italy
| | - Beatrice Tombolini
- School of Medicine, Vita-Salute San Raffaele University, Milan, Italy.,Department of Ophthalmology, IRCCS San Raffaele Scientific Institute, Milan, Italy
| | - Costanza Barresi
- School of Medicine, Vita-Salute San Raffaele University, Milan, Italy.,Department of Ophthalmology, IRCCS San Raffaele Scientific Institute, Milan, Italy
| | | | - Rosangela Lattanzio
- Department of Ophthalmology, IRCCS San Raffaele Scientific Institute, Milan, Italy
| | - Francesco Bandello
- School of Medicine, Vita-Salute San Raffaele University, Milan, Italy.,Department of Ophthalmology, IRCCS San Raffaele Scientific Institute, Milan, Italy
| | - Maria Vittoria Cicinelli
- School of Medicine, Vita-Salute San Raffaele University, Milan, Italy.,Department of Ophthalmology, IRCCS San Raffaele Scientific Institute, Milan, Italy
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39
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Marques JH, Marta A, Castro C, Baptista PM, José D, Almeida D, Ribeiro A, Barbosa I. Choroidal changes and associations with visual acuity in diabetic patients. Int J Retina Vitreous 2022; 8:6. [PMID: 34998439 PMCID: PMC8742927 DOI: 10.1186/s40942-021-00355-z] [Citation(s) in RCA: 6] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/02/2021] [Accepted: 12/28/2021] [Indexed: 12/14/2022] Open
Abstract
Background The variable visual function observed in diabetic retinopathy (DR) patients is not fully explained by the classic staging system. Our purpose was to evaluate choroidal changes, in standardized sectors, in DR patients and to find associations between choroidal measurements and visual function. Methods Cross-sectional study that included the right eye of diabetic patients (n = 265) without active edema, ischemia or neovascularization and age-matched controls (n = 73). Optical coherence tomography (OCT) imaging was performed with enhanced depth imaging protocol. Choroidal vascularity index (CVI) was calculated in a 5 mm scan centered in the fovea. Results CVI decreased with age (p < 0.001) but was not influenced by axial length. A multivariate analysis adjusting for age confirmed a significant difference in CVI between DR eyes that had previous treatments (intravitreal injections and/or photocoagulation) compared to control eyes (p = 0.013) and to DR eyes that never required treatment (p = 0.002). There was no significant difference between non-DR diabetic patients and normal controls. Considering the group of DR patients that had previous treatments, in eyes without optic media opacification, BCVA correlated with CVI (r = − 0.362, p < 0.001), whereas full retina thickness and individual retinal layer thickness did not (p > 0.066). Conclusions A reduction in CVI was observed in patients with a more advanced stage of DR. In treated DR patients with stable disease, choroidal biomarkers correlated with best-corrected visual acuity whereas retinal biomarkers did not. Trial registration: N/A Supplementary Information The online version contains supplementary material available at 10.1186/s40942-021-00355-z.
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Affiliation(s)
- João Heitor Marques
- Ophthalmology Department, Centro Hospitalar Universitário do Porto, Largo Prof. Abel Salazar, 4099-001, Porto, Portugal.
| | - Ana Marta
- Ophthalmology Department, Centro Hospitalar Universitário do Porto, Largo Prof. Abel Salazar, 4099-001, Porto, Portugal
| | - Catarina Castro
- Ophthalmology Department, Centro Hospitalar Universitário do Porto, Largo Prof. Abel Salazar, 4099-001, Porto, Portugal
| | - Pedro Manuel Baptista
- Ophthalmology Department, Centro Hospitalar Universitário do Porto, Largo Prof. Abel Salazar, 4099-001, Porto, Portugal
| | - Diana José
- Ophthalmology Department, Centro Hospitalar Universitário do Porto, Largo Prof. Abel Salazar, 4099-001, Porto, Portugal
| | - Daniel Almeida
- Ophthalmology Department, Centro Hospitalar Universitário do Porto, Largo Prof. Abel Salazar, 4099-001, Porto, Portugal
| | - António Ribeiro
- Ophthalmology Department, Centro Hospitalar Universitário do Porto, Largo Prof. Abel Salazar, 4099-001, Porto, Portugal.,Instituto de Ciências Biomédicas Abel Salazar, Universidade do Porto, Porto, Portugal
| | - Irene Barbosa
- Ophthalmology Department, Centro Hospitalar Universitário do Porto, Largo Prof. Abel Salazar, 4099-001, Porto, Portugal.,Instituto de Ciências Biomédicas Abel Salazar, Universidade do Porto, Porto, Portugal
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40
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Correlation of Renal Profiles with Choroidal Vascularity Index in Eyes with Diabetic Retinopathy. J Clin Med 2021; 10:jcm10215155. [PMID: 34768674 PMCID: PMC8584344 DOI: 10.3390/jcm10215155] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/26/2021] [Revised: 10/03/2021] [Accepted: 11/01/2021] [Indexed: 11/30/2022] Open
Abstract
The vascular system is affected by systemic conditions, including diabetes, hypertension, and cardiovascular disease. The choroid is an important vascular tissue surrounding the sensory retina. However, the relationship between the choroid and systemic factors in patients with diabetes has rarely been investigated. Here, we assessed the correlation of renal profiles with choroidal vasculature in eyes with diabetic retinopathy (DR) using a retrospective study design. The study included 131 patients with diabetes who underwent swept-source optical coherence tomography and routine medical work-up within a 4-week period between 1 February 2016 and 30 October 2018. Consecutive patients with treatment-naïve DR who did not receive any subsequent treatment were included. The distribution of patients according to the DR stage was as follows: no DR, 32 patients; mild-to-moderate non-proliferative DR (NPDR), 33 patients; severe NPDR, 34 patients; and treatment-naïve proliferative DR, 32 patients. Multivariate regression analyses showed that the choroidal vascularity index (CVI) of naïve eyes with DR was negatively correlated with age (p = 0.013) and the serum levels of phosphorus (p = 0.002) and positively correlated with subfoveal choroidal thickness (p < 0.001). Taken together, our findings suggest that a lower CVI is associated with phosphorus retention in patients with chronic kidney disease.
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Quantitative Assessment of Choroidal Parameters in Patients with Various Types of Diabetic Macular Oedema: A Single-Centre Cross-Sectional Analysis. BIOLOGY 2021; 10:biology10080725. [PMID: 34439957 PMCID: PMC8389323 DOI: 10.3390/biology10080725] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 07/08/2021] [Accepted: 07/26/2021] [Indexed: 11/22/2022]
Abstract
Simple Summary Choroidopathy is one of the components in the pathogenesis of diabetic macular oedema (DME). This study investigated the optical coherence tomography-based choroidal parameters: thickness, volume, choroidal vascularity index (CVI), luminal area (LA), stromal area (SA), and total choroidal area (TCA) in relation to the presence and type of DME (cystoid, diffuse, and with subretinal fluid). Diabetic choroidopathy seems to play a role in the development of DME but is less likely involved in the pathogenesis of specific types thereof. Abstract Diabetic macular oedema (DME) is an outcome of multiple, complex and not fully understood mechanisms. The aim of this study was to define the role of choroidopathy in the pathogenesis of various DME types. The retrospective cross-sectional single-centre study included 140 eyes from 105 patients with DME and 76 eyes from 52 non-diabetic controls. The eyes were stratified according to the type of DME: cystoid, diffuse, and with subretinal fluid. Optical coherence tomography-based choroidal parameters: thickness, volume, choroidal vascularity index (CVI), luminal area (LA), stromal area (SA), and total choroidal area (TCA) were compared. Eyes with DME, regardless of the type thereof, had lower choroidal thickness, volume, and CVI values than the controls. Further, the eyes with some specific DME types differed significantly from the controls in terms of LA and SA. While the eyes with various DME types did not differ significantly in terms of their choroidal thickness, volume and CVI, some between-group differences were found in LA, SA and TCA. Diabetic choroidopathy seems to play a role in the development of DME but is less likely involved in the pathogenesis of specific types thereof.
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Diabetic retinopathy and diabetic macular oedema pathways and management: UK Consensus Working Group. Eye (Lond) 2021; 34:1-51. [PMID: 32504038 DOI: 10.1038/s41433-020-0961-6] [Citation(s) in RCA: 92] [Impact Index Per Article: 23.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/12/2022] Open
Abstract
The management of diabetic retinopathy (DR) has evolved considerably over the past decade, with the availability of new technologies (diagnostic and therapeutic). As such, the existing Royal College of Ophthalmologists DR Guidelines (2013) are outdated, and to the best of our knowledge are not under revision at present. Furthermore, there are no other UK guidelines covering all available treatments, and there seems to be significant variation around the UK in the management of diabetic macular oedema (DMO). This manuscript provides a summary of reviews the pathogenesis of DR and DMO, including role of vascular endothelial growth factor (VEGF) and non-VEGF cytokines, clinical grading/classification of DMO vis a vis current terminology (of centre-involving [CI-DMO], or non-centre involving [nCI-DMO], systemic risks and their management). The excellent UK DR Screening (DRS) service has continued to evolve and remains world-leading. However, challenges remain, as there are significant variations in equipment used, and reproducible standards of DMO screening nationally. The interphase between DRS and the hospital eye service can only be strengthened with further improvements. The role of modern technology including optical coherence tomography (OCT) and wide-field imaging, and working practices including virtual clinics and their potential in increasing clinic capacity and improving patient experiences and outcomes are discussed. Similarly, potential roles of home monitoring in diabetic eyes in the future are explored. The role of pharmacological (intravitreal injections [IVT] of anti-VEGFs and steroids) and laser therapies are summarised. Generally, IVT anti-VEGF are offered as first line pharmacologic therapy. As requirements of diabetic patients in particular patient groups may vary, including pregnant women, children, and persons with learning difficulties, it is important that DR management is personalised in such particular patient groups. First choice therapy needs to be individualised in these cases and may be intravitreal steroids rather than the standard choice of anti-VEGF agents. Some of these, but not all, are discussed in this document.
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Discordance in Retinal and Choroidal Vascular Densities in Patients with Type 2 Diabetes Mellitus on Optical Coherence Tomography Angiography. J Ophthalmol 2021; 2021:8871602. [PMID: 33747557 PMCID: PMC7945675 DOI: 10.1155/2021/8871602] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/07/2020] [Revised: 12/03/2020] [Accepted: 01/28/2021] [Indexed: 12/12/2022] Open
Abstract
Purpose In the present study, the retinal and choroidal vascular densities (VDs) in type 2 diabetes mellitus (DM) patients were analyzed using optical coherence tomography angiography (OCTA). Methods The study included 282 eyes of 152 patients with type 2 DM (114 without retinopathy, 79 nonproliferative diabetic retinopathy (NPDR), 48 severe NPDR, and 41 proliferative diabetic retinopathy (PDR) eyes). The superficial and deep retinal vessel, choriocapillaris, and choroidal VDs were measured using a binarization method on OCTA images. VDs were compared based on retinopathy severity. Correlations among densities were analyzed. Results Retinal and choriocapillaris VDs were lower in PDR than in NPDR (all P < 0.05). Correlation analysis showed significant positive correlations among densities of superficial and deep retinal vessels and choriocapillaris (all P < 0.001). Choroidal VD showed a negative correlation with superficial and deep retinal vessels and choriocapillaris (all P < 0.001). Retinal and choriocapillaris VDs showed a negative correlation with diabetic retinopathy (DR) grade (all P < 0.001); however, the choroidal VD showed a weak positive correlation (P=0.030). Conclusion Choroidal VD increased as retinal and choriocapillaris VDs decreased, indicating that the outer layer of the choroid is less affected by DR severity and VD of larger choroidal vessels may even be increased as a compensatory mechanism for decreased retinal and choriocapillaris VDs in type 2 DM patients.
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Betzler BK, Ding J, Wei X, Lee JM, Grewal DS, Fekrat S, Sadda SR, Zarbin MA, Agarwal A, Gupta V, Schmetterer L, Agrawal R. Choroidal vascularity index: a step towards software as a medical device. Br J Ophthalmol 2021; 106:149-155. [PMID: 33514528 DOI: 10.1136/bjophthalmol-2021-318782] [Citation(s) in RCA: 55] [Impact Index Per Article: 13.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/02/2021] [Revised: 01/07/2021] [Accepted: 01/09/2021] [Indexed: 11/04/2022]
Abstract
The choroidal vascularity index (CVI) is a relatively new parameter, calculated off optical coherence tomography (OCT) images, for the quantitative evaluation of choroid vascularity. It is defined as the ratio of vascular area to the total choroidal area, presented as a percentage. The choroid is an important vascular bed, often implicated in ocular and systemic conditions. Since the introduction of CVI, multiple studies have evaluated its efficacy as a tool for disease prognostication and monitoring progression, with promising results. The CVI was born out of the need for more robust and accurate evaluations of choroidal vasculature, as prior parameters such as choroidal thickness and choroidal vessel diameter had their limitations. In this review, we summarise current literature on the CVI, explain how the CVI is derived and explore its potential integration into future research and translation into clinical care. This includes the application of CVI in various disease states, and ongoing attempts to produce an automated algorithm which can calculate CVI from OCT images.
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Affiliation(s)
| | - Jianbin Ding
- Lee Kong Chian School of Medicine, Nanyang Technological University, Singapore
| | - Xin Wei
- National Healthcare Group Eye Institute, Tan Tock Seng Hospital, Singapore
| | - Jia Min Lee
- National Healthcare Group Eye Institute, Tan Tock Seng Hospital, Singapore
| | - Dilraj S Grewal
- Department of Ophthalmology, Duke University School of Medicine, Durham, North Carolina, USA
| | - Sharon Fekrat
- Department of Ophthalmology, Duke University School of Medicine, Durham, North Carolina, USA
| | - Srinivas R Sadda
- Department of Ophthalmology, Duke University School of Medicine, Durham, North Carolina, USA
| | - Marco A Zarbin
- Rutgers-New Jersey Medical School, Rutgers University, Newark, New Jersey, USA
| | - Aniruddha Agarwal
- Department of Ophthalmology, Post Graduate Institute of Medical Education and Research, Chandigarh, India
| | - Vishali Gupta
- Department of Ophthalmology, Post Graduate Institute of Medical Education and Research, Chandigarh, India
| | - Leopold Schmetterer
- Singapore Eye Research Institute, Singapore National Eye Center, Singapore.,Ophthalmology and Visual Sciences Academic Clinical Program, Duke-NUS Medical School, Singapore.,SERI-NTU Advanced Ocular Engineering (STANCE), Singapore
| | - Rupesh Agrawal
- Yong Loo Lin School of Medicine, National University of Singapore, Singapore .,Lee Kong Chian School of Medicine, Nanyang Technological University, Singapore.,National Healthcare Group Eye Institute, Tan Tock Seng Hospital, Singapore.,Singapore Eye Research Institute, Singapore National Eye Center, Singapore.,Ophthalmology and Visual Sciences Academic Clinical Program, Duke-NUS Medical School, Singapore
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Damian I, Roman G, Nicoară SD. Analysis of the Choroid and Its Relationship with the Outer Retina in Patients with Diabetes Mellitus Using Binarization Techniques Based on Spectral-Domain Optical Coherence Tomography. J Clin Med 2021; 10:jcm10020210. [PMID: 33435599 PMCID: PMC7826830 DOI: 10.3390/jcm10020210] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/24/2020] [Revised: 12/29/2020] [Accepted: 01/05/2021] [Indexed: 12/31/2022] Open
Abstract
(1) Background: We aimed to reveal the relationship between the choroid and the outer retina with optical coherence tomography (OCT) in patients with diabetes mellitus (DM) with mild or no diabetic retinopathy (DR) in order to find early biomarkers for progressing retinopathy. (2) Methods: We performed a prospective study including 61 eyes of patients with type 1 or type 2 DM and 36 eyes of healthy controls. All subjects were imaged with Spectralis OCT. The choroid was assesseed using enhanced depth imaging OCT (EDI-OCT). Binarization of subfoveal choroidal images was done with public domain software, ImageJ (version 1.53a; National Institutes of Health, Bethesda, Maryland, USA). (3) Results: Luminal area, stromal area and total choroidal area were significantly decreased in diabetic patients compared to control: 0.23 ± 0.07 vs. 0.28 ± 0.08, p = 0.012; 0.08 ± 0.03 vs. 0.10 ± 0.04, p = 0.026; 0.31 ± 0.09 vs. 0.38 ± 0.11, p = 0.008. The thickness of retinal pigment epithelium (RPE) correlated positively with the choroidal vascularity index (CVI). The correlations between outer nuclear layer (ONL), photoreceptors (PR) and foveal choroidal thickness (FChT) were moderately negative. (4) Conclusion: Thicker RPE and a thinner PR layer may be assigned the role of early biomarkers signaling the conversion time to progressing retinopathy.
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Affiliation(s)
- Ioana Damian
- Department of Ophthalmology, “Iuliu Hațieganu” University of Medicine and Pharmacy, 8 V. Babes str., 400012 Cluj-Napoca, Romania;
- Medical Doctoral School 1, University of Oradea, Universitatii Str, 410087 Oradea, Romania
| | - Gabriela Roman
- Department of Diabetes, Nutrition and Metabolic Diseases, “Iuliu Haţieganu” University of Medicine and Pharmacy, 8 V.Babes str., 400012 Cluj-Napoca, Romania;
- Diabetes Center, Emergency County Hospital Cluj, 3-5 Clinicilor Str., 400006 Cluj-Napoca, Romania
| | - Simona Delia Nicoară
- Department of Ophthalmology, “Iuliu Hațieganu” University of Medicine and Pharmacy, 8 V. Babes str., 400012 Cluj-Napoca, Romania;
- Clinic of Ophthalmology, Emergency County Hospital Cluj, 3-5 Clinicilor Str., 400006 Cluj-Napoca, Romania
- Correspondence: or
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Dou N, Yu S, Tsui CK, Yang B, Lin J, Lu X, Xu Y, Wu B, Zhao J, Liang X. Choroidal Vascularity Index as a Biomarker for Visual Response to Antivascular Endothelial Growth Factor Treatment in Diabetic Macular Edema. J Diabetes Res 2021; 2021:3033219. [PMID: 34869776 PMCID: PMC8642029 DOI: 10.1155/2021/3033219] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/10/2021] [Accepted: 11/06/2021] [Indexed: 12/12/2022] Open
Abstract
PURPOSE To investigate the choroidal vascularity index (CVI) as a prognostic factor for the visual efficacy of antivascular endothelial growth factor (VEGF) treatment in diabetic macular edema (DME). METHODS We retrospectively reviewed 92 DME eyes receiving anti-VEGF treatment, which were stratified as responders (≥5 letters gained) and nonresponders (<5 letters gained or lost). Baseline systematic features and optical coherence tomography features, including the CVI, adjusted ellipsoid zone (EZ) reflectivity, subretinal fluid (SRF), and disorganization of the retinal inner layers (DRIL), were evaluated between the two groups. RESULTS The baseline CVI was significantly lower in nonresponders than in responders (0.66 ± 0.05, 0.69 ± 0.05, and 0.72 ± 0.05, p = 0.014). After adjusting for other factors, the baseline CVI, DRIL, SRF, and adjusted EZ reflectivity were significantly associated with visual outcomes (CVI: odds ratio (OR) = 0.17, p = 0.006; adjusted EZ reflectivity: OR = 0.56, p = 0.007; DRIL: OR = 6.71, p = 0.001; and SRF: OR = 0.29, p = 0.008). CONCLUSION DME patients with a higher CVI, higher adjusted EZ reflectivity, the presence of SRF, and the absence of DRIL at baseline were more likely to gain >5 letters in visual acuity after anti-VEGF treatment. CVI may serve as a novel biomarker for visual response to anti-VEGF treatment in DME.
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Affiliation(s)
- Ningxin Dou
- State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou 510060, China
| | - Shanshan Yu
- State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou 510060, China
| | - Ching-Kit Tsui
- State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou 510060, China
| | - Boyu Yang
- State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou 510060, China
| | - Jianqiang Lin
- State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou 510060, China
| | - Xi Lu
- State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou 510060, China
| | - Yue Xu
- State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou 510060, China
| | - Benjuan Wu
- State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou 510060, China
| | - Jinfeng Zhao
- State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou 510060, China
| | - Xiaoling Liang
- State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou 510060, China
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Sidorczuk P, Pieklarz B, Konopinska J, Saeed E, Mariak Z, Dmuchowska D. Foveal Avascular Zone Does Not Correspond to Choroidal Characteristics in Patients with Diabetic Retinopathy: A Single-Center Cross-Sectional Analysis. Diabetes Metab Syndr Obes 2021; 14:2893-2903. [PMID: 34234487 PMCID: PMC8254029 DOI: 10.2147/dmso.s318860] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/06/2021] [Accepted: 05/22/2021] [Indexed: 12/27/2022] Open
Abstract
PURPOSE The aim of the study was to compare two non-overlapping blood supply systems of the retina to obtain a better insight into the relation between diabetic macular retinopathy and choroidopathy. Specifically, the study focused on the relationships between (1) retinal vascular changes around the fovea in fluorescein angiography (FA) and (2) choroidal thickness, volume and other parameters assessed by optical coherence tomography (OCT). PATIENTS AND METHODS The retrospective cross-sectional single-center study included 210 eyes from 152 patients with diabetic retinopathy (mean age 60.7±12.4 years, 49.3% of women; foveal avascular zone [FAZ] outline: 44.3% grade ≤2, 55.7% grade ≥3). The outline of FAZ, a measure of capillary loss due to ischemic processes, was analyzed on FA according to the Early Treatment Diabetic Retinopathy Study Research Group (ETDRS) standards. The eyes were stratified according to the FAZ outline and size and the presence of clinically significant diabetic macular edema (CSME). Then, resultant groups were compared in terms of the spectral domain OCT parameters: choroidal thickness and volume (within ETDRS subfields), luminal, stromal and total choroidal areas and choroidal vascularity index (based on the foveal scan). Statistical analysis was based on univariate models with the choroidal parameters as independent variables, and age, sex, panretinal photocoagulation, the severity of diabetic retinopathy and CSME as covariates. RESULTS No significant relationships were found between the FAZ outline and area and choroidal characteristics of patients with diabetic retinopathy. In patients without CSME, no correlation was observed between the FAZ area and choroidal characteristics. In patients with CSME, no correlation was found between the FAZ area and choroidal characteristics other than the choroidal vascularity index. CONCLUSION In patients with diabetic retinopathy, damage to the macular retinal vasculature (FAZ) does not seem to be associated with changes in the choroidal vasculature, and these two processes appear to occur independently.
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Affiliation(s)
- Patryk Sidorczuk
- Department of Ophthalmology, Medical University of Bialystok, Bialystok, 15-276, Poland
| | - Barbara Pieklarz
- Department of Ophthalmology, Medical University of Bialystok, Bialystok, 15-276, Poland
| | - Joanna Konopinska
- Department of Ophthalmology, Medical University of Bialystok, Bialystok, 15-276, Poland
| | - Emil Saeed
- Department of Ophthalmology, Medical University of Bialystok, Bialystok, 15-276, Poland
| | - Zofia Mariak
- Department of Ophthalmology, Medical University of Bialystok, Bialystok, 15-276, Poland
| | - Diana Dmuchowska
- Department of Ophthalmology, Medical University of Bialystok, Bialystok, 15-276, Poland
- Correspondence: Diana Dmuchowska Department of Ophthalmology, Medical University of Białystok, 24a M. Sklodowskiej-Curie, Bialystok, 15-276, PolandTel +48857468372Fax +48857468604 Email
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Choroidal and retinal structural, cellular and vascular changes in a rat model of Type 2 diabetes. Biomed Pharmacother 2020; 132:110811. [PMID: 33069967 DOI: 10.1016/j.biopha.2020.110811] [Citation(s) in RCA: 14] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/06/2020] [Revised: 09/16/2020] [Accepted: 09/25/2020] [Indexed: 12/28/2022] Open
Abstract
Increasing evidence points to inflammation as a key factor in the pathogenesis of diabetic retinopathy (DR). Choroidal changes in diabetes have been reported and several attempts were made to validate in vivo choroidal thickness (CT) as a marker of retinopathy. We aimed to study choroidal and retinal changes associated with retinopathy in an animal model of spontaneous Type 2 diabetes, Goto-Kakizaki (GK) rats. Sclerochoroidal whole mounts and cryosections were prepared from 52-week-old GK and age-matched control Wistar Han rats. CT was measured by optical coherence tomography. Microglia reactivity, pericyte and endothelial cells distribution, and immunoreactivity of vascular endothelial growth factor (VEGF) and VEGF receptor 2 (VEGFR2) were evaluated by immunofluorescence. Choroidal vessels were visualized by direct perfusion with 1,1'-dioctadecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate (Dil). Choroidal vascular density was evaluated by fluorescence microscopy. GK rats had increased CT (58.40 ± 1.15 μm versus 50.90 ± 1.58 μm, p < 0.001), reduced vascular density of the choriocapillaris (CC) (p = 0.045), increased Iba1+ cells density in the outer retina (p = 0.003) and increased VEGFR2 immunoreactivity in most retinal layers (p = 0.021 to 0.037). Choroidal microglial cells and pericytes showed polarity in their distribution, sparing the innermost choroid. This cell-free gap in the inner choroid was more pronounced in GK rats. In summary, GK rats have increased CT with decreased vascular density in the innermost choroid, increased VEGFR2 immunoreactivity in the retina and increased Iba1+ cells density in the outer retina.
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Hamadneh T, Aftab S, Sherali N, Vetrivel Suresh R, Tsouklidis N, An M. Choroidal Changes in Diabetic Patients With Different Stages of Diabetic Retinopathy. Cureus 2020; 12:e10871. [PMID: 33178524 PMCID: PMC7652371 DOI: 10.7759/cureus.10871] [Citation(s) in RCA: 16] [Impact Index Per Article: 3.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/14/2022] Open
Abstract
Diabetic retinopathy (DR) is one of the long-term microvascular complications of diabetes mellitus (DM) and is considered a leading cause of vision loss worldwide. Chronic hyperglycemia can cause microvascular abnormalities to the retina and the choroid as well. The vascular tissue of the choroid supplies blood to the outer retina, photoreceptors, and retinal pigment epithelium. It plays an important role in the metabolic exchange of the retina. Many experimental studies reported that choroidal pathology in diabetic patients might play a role in developing DR. Choroidal thickness (CT) can reflect changes in the vasculature of the choroid and can be used to assess the vascularity of the choroid itself. CT differs between healthy and diseased states of the eye as well as with the aging process. This means that thinner or thicker choroid may indicate an ocular disease. Choroidal vascularity index (CVI) is also used as a marker for choroidal vascularity assessment and indirectly measures choroidal vascularity quantitatively. Many studies have been conducted to evaluate the choroid in many different ocular diseases. However, the results regarding CT in DM, especially in patients with DR, are various as thickened, thinned, or no changes. Thus, the status of the choroid in patients with DM with or without DR remains controversial between researchers. In this systematic review, we reviewed 18 articles that were done to investigate the relationship between structural choroidal changes in diabetic patients with different stages of DR, focusing on CT, CVI, and some other parameters evaluating choroidal changes.
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Affiliation(s)
- Tariq Hamadneh
- Ophthalmology, The Third Affiliated Hospital of Southern Medical University, Guangzhou, CHN.,Ophthalmology, California Institute of Behavioral Neurosciences & Psychology, Fairfield, USA
| | - Saba Aftab
- Medicine, Hamdard College of Medicine and Dentistry, Karachi, PAK.,Medicine, California Institute of Behavioral Neurosciences & Psychology, Fairfield, USA
| | - Nazleen Sherali
- Medicine, Liaquat University of Medical and Health Sciences, Jamshoro, PAK.,Medicine, California Institute of Behavioral Neurosciences & Psychology, Fairfield, USA
| | | | - Nicholas Tsouklidis
- Health Care Administration, University of Cincinnati Health, Cincinnati, USA.,Medicine, California Institute of Behavioral Neurosciences & Psychology, Fairfield, USA.,Medicine, Atlantic University School of Medicine, Gros Islet, LCA
| | - MeiXia An
- Ophthalmology, The Third Affiliated Hospital of Southern Medical University, Guangzhou, CHN
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Sabaner MC, Akdogan M, Doğan M, Oral AY, Duman R, Koca T, Bozkurt E. Inflammatory cytokines, oxidative and antioxidative stress levels in patients with diabetic macular edema and hyperreflective spots. Eur J Ophthalmol 2020; 31:2535-2545. [PMID: 33008266 DOI: 10.1177/1120672120962054] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/16/2022]
Abstract
PURPOSE To determine the levels of serum oxidative, antioxidative markers and inflammatory cytokines in patients diagnosed with diabetic macular edema (DME) whose hyperreflective spots (HRS) were detected by optical coherence tomography (OCT). METHODS In this prospective cross-sectional clinical study included a total of 88 patients; 31 patients (group-1) with DME and HRS detected by OCT, 29 patients (group-2) with DME without HRS, and 28 patients (group-3) diagnosed with diabetes mellitus (DM) without any diabetic retinopathy findings. The main outcomes were best-corrected visual acuity (BCVA), CMT (central macular thickness), CMV (central macular volume), TMV (total macular volume), CT (choroidal thickness), serum TAS (total antioxidant status), TOS (total oxidant status), VEGF (vascular endothelial growth factor), FGF (fibroblast growth factor) and IL-1b levels. OCT parameters and biochemical measurements were compared statistically between the three groups. RESULTS A total of 88 patients (43 females (48.9%) and 45 males (51.1%)) were included in the study. The mean age was 56.29 ± 9.23 years. There was no difference between the three groups in age-and-sex. In group-1 and 2, BCVA(LogMAR) was statistically higher than group 3. CMT, CMV, TMV, TAS, TOS, VEGF and FGF were significantly higher in group-1 than in group-3. CMT, CMV, TMV, VEGF and FGF were significantly higher in group-2 than group 3. TOS and VEGF were significantly higher in group-1 than group-2. CONCLUSIONS This study demonstrates that in patients with DME and HRS, TOS and VEGF levels were higher than those without HRS. Hence, hyperreflective spots may be an inflammatory biomarker.
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Affiliation(s)
| | - Muberra Akdogan
- Department of Ophthalmology, Afyonkarahisar Health Sciences University, Faculty of Medicine, Afyonkarahisar, Turkey
| | - Mustafa Doğan
- Department of Ophthalmology, Afyonkarahisar Health Sciences University, Faculty of Medicine, Afyonkarahisar, Turkey
| | - Ayse Yesim Oral
- Department of Ophthalmology, Afyonkarahisar Health Sciences University, Faculty of Medicine, Afyonkarahisar, Turkey
| | - Resat Duman
- Department of Ophthalmology, Ministry of Health Bursa City Hospital, Bursa, Turkey
| | - Tulay Koca
- Department of Physiology, Afyonkarahisar Health Sciences University, Faculty of Medicine, Afyonkarahisar, Turkey
| | - Erhan Bozkurt
- Department of Internal Medicine, Afyonkarahisar Health Sciences University, Faculty of Medicine, Afyonkarahisar, Turkey
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