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Table 2 Definitions used for carotid disease and diabetic retinopathy

From: The relationship between carotid disease and retinopathy in diabetes: a systematic review

First authorDiabetic retinopathy variable/sDiabetic retinopathy assessmentCarotid disease variable/sCarotid disease assessment
Cardoso [23]New or worsening DRDR graded as none, mild NPDR, moderate NPDR, severe NPDR or PDR by ophthalmologist at annual review. Worsening defined as worse by at least two grades (e.g. from mild to severe NPDR)IMT of ICA, BIF and CCA
Plaque score
Number of plaques
Mean of 3 IMT measurements used, IMT measured according to Mannheim consensus
Extracranial carotid artery plaque score assigned for each segment of ICA, CCA and BIF and highest grade assigned; 0: no plaque, 1: one small plaque, stenosis < 30%, 2: one medium plaque, 30–49% stenosis or multiple small plaques, 3: one large plaque, 50–99% stenosis or multiple plaques with at least one medium plaque, 4: 100% occlusion
Single vascular radiologist performed ultrasound, good intra-observer test–retest reliability
Hjelmgren [32]AnyMedical records from all eye clinics in the areaStenosis > 50%Greater stenosis from left or right artery used
Ichinohasama [8]Mild NPDR versus no DRRight eye assessed by ophthalmologist, according to ETDRS protocolCCA IMTMaximum measurement of right CCA IMT
Carbonell [7]None, mild or advanced (moderate NPDR or worse)Examination by ophthalmologist, according to ETDRS protocolPlaquePlaque was defined according to the Mannheim consensus
Single sonographer at each study site performed ultrasound
Liu [34]AnyRetinal images graded by ophthalmologist according to International Clinical Diabetic Retinopathy Disease Severity ScaleCCA IMT > 1 mm
Plaque
Subclinical atherosclerosis
Maximum CCA IMT value of left or right artery used, IMT was measured 1.5 cm proximal to the bifurcation, elevated CCA IMT defined as > 1 mm
Plaque was classified as focal increase in thickness more than 0.5 mm or 50% of surrounding IMT
Subclinical atherosclerosis was defined as CCA IMT > 1 mm and/or presence of carotid plaque
Single sonographer performed ultrasound
Alonso [28]Any and mild NPDR, moderate NPDR or severe NPDR or PDRMulti-field stereoscopic retinal images and ophthalmologist examinationIMT of ICA, BIF and CCA
Plaque
Semiautomatic software provided data for mean and mean-maximum IMT from segments of ICA, BIF and CCA. Values from the left and right arteries were averaged
Plaque was defined according to the Mannheim consensus
Single sonographer performed ultrasound
Jung [27]AnyExamination by ophthalmologistCCA IMT ≥ 1 mm,
Plaques > 2
CCA IMT measured 1 cm proximal to bulb on left and right, mean of these were used
Protrusions > 100% defined as plaque. Plaques were categorised into n ≤ 2 and n > 2 plaques
Cardoso [29]AnyExamination by ophthalmologistIMT of CCA, BIF, ICA
Plaque score ≤ 2 or > 2
Mean of 3 IMT measurements used. IMT measured according to Mannheim consensus
Extracranial carotid artery plaque score assigned for each segment of ICA, CCA and BIF and highest grade assigned; 0: no plaque, 1: one small plaque, stenosis < 30%, 2: one medium, plaque 30–49% stenosis or multiple small plaques, 3: one large plaque, 50–99% stenosis or multiple plaques with at least one medium plaque, 4: 100% occlusion
Single vascular radiologist performed ultrasound, good intra-observer test–retest reliability
Yun [10]AnyRetinal images graded according to ETDRS protocolCCA IMT
Plaque
CCA IMT measured by software at thickest point ~ 1 cm from bulb, analysed in tertiles
Plaque defined as protrusions into lumen that were 100% thicker than surrounding area
Physicians performed ultrasound
Son [10]AnyTwo-field retinal images and ophthalmologist examinationCCA IMT ≤ 0.9 mm and no plaque compared to CCA IMT > 0.9 mm ± carotid plaqueIMT measured bilaterally 5–10 mm proximal to bulb, 3 measurements done at site of greatest thickness and 10 mm proximal and distal to this point, highest mean CCA IMT used
Plaque was a focal increase of ≥ 0.5 mm or ≥ 50% of surrounding IMT
Single sonographer performed ultrasound
Araszkiewicz [30]AnyTwo-field retinal images and ophthalmologist examination according to American Academy of OphthalmologyCCA IMTRight CCA IMT measured and automatically calculated with software program—Carotid Analyzer for Research (CAD 5)
Lacroix [33]AnyExamination by ophthalmologistno atherosclerotic lesion or stenosis < 60% or stenosis ≥ 60%Stenosis was considered ≥ 60% when the maximal velocity within the lesion was > 2.6 m/s and the end-diastolic velocity > 0.7 m/s
Performed by experienced vascular physicians
Distiller [31]AnyRetinal images assessedCCA IMT
Plaque
IMT risk (low, medium or high)
CCA IMT measured > 1 cm proximal to flow divider, mean of left and right used
Plaque defined as localised thickening of wall of ≥ 1.5 mm
IMT risk: low < 0.6 mm, medium 0.6–0.8, high > 0.8 and/or plaque
Two sonographers, intra-observer & inter-observer variability 3.1% and 3.9%
Rema [9]AnyFour-field retinal images graded according to ETDRS protocol by two graders, a third grader made final decision if discrepancyIMT of CCA, BIF, ICAMean of six IMT measurements of right ICA, CCA and BIF
All scans were quality controlled by a central laboratory in Canada
  1. DR diabetic retinopathy, NPDR non-proliferative diabetic retinopathy, PDR proliferative diabetic retinopathy, CSMO clinically significant macular oedema, VTDR vision-threatening diabetic retinopathy, ETDRS Early Treatment Diabetic Retinopathy Study, CCA common carotid artery, ICA internal carotid artery, IMT intima-media thickness