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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 author

Diabetic retinopathy variable/s

Diabetic retinopathy assessment

Carotid disease variable/s

Carotid disease assessment

Cardoso [23]

New or worsening DR

DR 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]

Any

Medical records from all eye clinics in the area

Stenosis > 50%

Greater stenosis from left or right artery used

Ichinohasama [8]

Mild NPDR versus no DR

Right eye assessed by ophthalmologist, according to ETDRS protocol

CCA IMT

Maximum measurement of right CCA IMT

Carbonell [7]

None, mild or advanced (moderate NPDR or worse)

Examination by ophthalmologist, according to ETDRS protocol

Plaque

Plaque was defined according to the Mannheim consensus

Single sonographer at each study site performed ultrasound

Liu [34]

Any

Retinal images graded by ophthalmologist according to International Clinical Diabetic Retinopathy Disease Severity Scale

CCA 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 PDR

Multi-field stereoscopic retinal images and ophthalmologist examination

IMT 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]

Any

Examination by ophthalmologist

CCA 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]

Any

Examination by ophthalmologist

IMT 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]

Any

Retinal images graded according to ETDRS protocol

CCA 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]

Any

Two-field retinal images and ophthalmologist examination

CCA IMT ≤ 0.9 mm and no plaque compared to CCA IMT > 0.9 mm ± carotid plaque

IMT 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]

Any

Two-field retinal images and ophthalmologist examination according to American Academy of Ophthalmology

CCA IMT

Right CCA IMT measured and automatically calculated with software program—Carotid Analyzer for Research (CAD 5)

Lacroix [33]

Any

Examination by ophthalmologist

no 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]

Any

Retinal images assessed

CCA 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]

Any

Four-field retinal images graded according to ETDRS protocol by two graders, a third grader made final decision if discrepancy

IMT of CCA, BIF, ICA

Mean 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