Alteration in Hemodynamic Parameters in Ophthalmic and Central Retinal Arteries in Indian Patients with Increasing Grade of Diabetic Retinopathy

Research Article

Austin J Clin Ophthalmol. 2014;1(1): 1001.

Alteration in Hemodynamic Parameters in Ophthalmic and Central Retinal Arteries in Indian Patients with Increasing Grade of Diabetic Retinopathy

Khan Adeeb Alam*, Sharma Mayank1, Rizvi Syed Wajahat Ali1, Amitava Abadan Khan1, Siddiqui Ziya1, and Siddiqui Mohammed Azfar2

1Institute of Ophthalmology, JNMCH, AMU, Aligarh, India

2Department of Radiodiagnosis, JNMCH, AMU, Aligarh, India

*Corresponding author: Khan Adeeb Alam, Institute of Ophthalmology, JNMCH, AMU, Aligarh, India

Received: January 02, 2013; Accepted: January 17, 2013; Published: January 20, 2013


Background: Diabetes, with and without retinopathy, is often associated with hemodynamic alterations in ocular blood flow. Color Doppler Imaging (CDI) is an established noninvasive technique that enables measuring blood flow velocities in small orbital vessels.

Aim: We set out tomeasure ocular blood flow hemodynamics by Color Doppler Imaging in the ophthalmic artery (OA) and central retinal artery (CRA) in patients with diabetic retinopathy (DR) and to compare it with healthy subjects.

Methods: We evaluated 61 eyes of 61 subjects, (controls: 21 and diabetics: 40). Diabetic patients were further classified in two groups: diabetics with either no retinopathy or background retinopathy (NDR⁄BDR; n=20), and diabetics with preproliferative or proliferative retinopathy (PPDR⁄PDR; n=20). Three Color Doppler parameters: peak systolic velocity (PSV in cm⁄s), end diastolic velocity (EDV, cm⁄s) and resistivity index (RI) were measured in the OA and CRA. Statistical analysis was done using ANOVA and Post–Hoc (Tukey) test to compare the results between NDR⁄BDR, PPDR⁄PDR and control groups.

Results: No significant difference was seen in the age of the subjects. We found statistically significant differences only in the OA. Specifically, PSV was significantly greater in NDR⁄BDR Vs controls (95%CI: 2.25 to 14.92); EDV was significantly decreased in PPDR⁄PDR as compared to controls (95%CI: 0.43 to 4.12) and NDR⁄BDR (95%CI: 0.13 to 3.80); RI was significantly increased in PPDR⁄PDR (95%CI: 0.09 to 0.23) and NDR⁄BDR (95%CI: 0.03 to 0.17) ascompared to controls.

Conclusion: We found significant circulatory alterations in the OA in diabetic patients suggesting hemodynamic dysfunction. RI was significantly increased indiabetics as compared to controls.

Keywords: Color Doppler; Diabetic Retinopathy; Hemodynamics; Metabolic Disorders.

Abbreviations: DM– Diabetes Mellitus; DR– Diabetic Retinopathy ; CDIColor Doppler Imaging; OA– Ophthalmic Artery; NDR– No Diabetic Retinopathy; BDR– Background Diabetic Retinopathy; PPDR– Preproliferative Diabetic Retinopathy; PDR– Proliferative Diabetic Retinopathy; CRA– Central Retinal Artery; PSV– Peak Systolic Velocity; EDV– End Diastolic Velocity; RI– Resistive Index; CI– Confidence Interval.


Diabetes mellitus (DM) is a systemic metabolic disorder, which may result in generalized macrovascular and microvascular complications. The macrovascular complications, accounting for most of the morbidity and mortality, [1–3] include ischaemic heart disease, cerebrovascular disorders and peripheral vascular disease [4]. Microvascular complications include retinopathy, neuropathy and nephropathy. Diabetic Retinopathy (DR), although a microangiopathy, has been shown to independently predict macrovascular events including ischaemic heart disease and stroke [5–7].

DR affects retinal microvasculature leading to characteristic alterations in retinal blood flow [8]. Ocular vascular hemodynamic parameters are often evaluated using Color Doppler Imaging (CDI) and laser Doppler velocimetry [8,9]. CDI is an established noninvasive technique that enables both quantitative and qualitative assessment of blood flow velocities in small orbital vessels as well as simultaneous visualization of 2–D imaging. Using this technique, good reproducibility has been reported in the localization and hemodynamic measurement within the central retinal artery (CRA) and ophthalmic artery (OA) [10]. Many conditions like central retinal artery and vein occlusions, vasculitis, and ischemic optic neuropathy are associated with changes in orbital hemodynamics and CDI has successfully demonstrated them [11].


After clearance from the Institutional Ethics Committee following the tenets of the Declaration of Helsinki and obtaining informed consent, we recruited 61 subjects: 21 controls and 40 cases of diabetes. The control group was randomly selected from those without any ocular pathology, systemic hypertension, diabetes mellitus or vascular disease. Diabetics were diagnosed if they had a fasting plasma glucose ≥ 126 mg⁄dl or 2–h plasma glucose ≥ 200mg⁄dl [12]. We included only one eye from both controls and cases (in case of difference in retinopathy, the eye with greater severity was chosen). The cases were further divided into diabetics with no retinopathy or background diabetic retinopathy (NDR⁄BDR) (corresponds to retinopathy level 2–3) and preproliferative diabetic retinopathy(PPDR) (retinopathy level 4–5)⁄ proliferative diabetic retinopathy (PDR) (retinopathy level 6–7) as per modified Airlie House system on the basis of dilated retinal examination using the biomicroscopic indirect ophthalmoscope and fundus photographs by a single experienced ophthalmologist [13,14]. The PPDR and PDR were grouped together because of few patients with proliferative (n=4) changes. We excluded diabetic patients who had undergone laser photocoagulation, had any ocular trauma or ocular surgery; we also excluded diabetics who had glaucoma, uveitis, retinal pathology like central retinal vein occlusion, and optic nerve disease. We evaluated only those patients who had systolic blood pressure below 140mmHg and diastolic pressure below 90mmHg. As only single reading of blood pressure was taken and higher blood pressure causes varied volume flow at different times, therefore we excluded this factor.

The CDI of OA and CRA was performed using Color Doppler (Logic 500 pro series, GE) with 5–9 MHz linear array multi frequency probe. After explaining the procedure, scan was performed with the patient supine, eyes closed and gaze directed towards the ceiling. We used a standardized Doppler technique [11]. The transducer was coupled to the closed upper eyelid with sterile ophthalmic methyl cellulose gel. Once optimal visualization of blood flow was obtained on the visual display unit, specific ocular vessels could then be rapidly examined using pulsed Doppler. With slight angular adjustment of the probe, from the spectral analysis of the resulting Doppler frequency shift, a velocity waveform was obtained. The probe angle was always less than 60 degrees, and every measurement was made at constant angle to the vessel. The color Doppler display was set so that blood towards the transducer appeared red, while blood flow away appeared blue. The main outcomes measured were peak systolic velocity (PSV): representing the maximum flow velocity recorded during each cardiac cycle; end diastolic velocity (EDV): recorded immediately before the next systolic upstroke; and resistivity index (RI) = PSV–EDV⁄PSV calculated by Pourcelot’s formula. RI (also known as Pourcelot’s ratio) usually varies from 0% (no resistance) to 100% (high resistance) [11]. Measurements of PSV, EDV, and RI were obtained using the mean of 3 cardiac cycles.

We analyzed the results using ANOVA and Post–Hoc (Tukey) test, significance was set at p≤0.05 (two tailed) and95% CI are also reported.


Table 1 shows baseline characteristics of controls and diabetics. The blood flow parameters of the OA were significantly different among controls, NDR⁄BDR, and PPDR⁄PDR (p<0.05) (Table 2), while no such difference was seen in the CRA. Specifically, in the OA, a significantly increased PSV was found in NDR⁄BDR but only when compared to controls (95%CI: 2.25 to 14.92), a significant reduction in EDV of PPDR⁄PDR group was noticed as compared to both, controls (95%CI: 0.43 to 4.12) and NDR⁄BDR group(95%CI: 0.13 to 3.80), while significantly higher RI was seen in both NDR⁄BDR (95%CI: 0.03 to 0.17) and PPDR⁄PDR (95%CI: 0.09 to 0.23) as compared to controls (Table 3).