Aim: To examine the relation between stenosis of the internal carotid artery (ICA) and pulsatile ocular blood flow (POBF).
Methods: In 57 eyes of 30 patients who were referred for Doppler ultrasound examination of the ICA we measured POBF and analysed the correlation with degree of ipsilateral ICA stenosis.
Results: There was a significant negative correlation between POBF and ipsilateral ICA stenosis (Pearson correlation coefficient, r = −0.516, p <0.0001). In 14 eyes POBF could not be measured by the OBF tonometer, and in 11 of these cases (79%) severe stenosis (>75%) of the ipsilateral ICA was present. When these eyes were excluded from analysis, there was no correlation between POBF and ICA stenosis (r = −0.02, p = 0.91). Among these 43 eyes in which POBF could be measured it ranged 667–2095 µl/min with a mean of 970.72 µl/min.
Conclusion: Low or unrecordable POBF may signify severe stenosis of the internal carotid artery. POBF is not a direct reflection of ipsilateral ICA blood flow.
- pulsatile ocular blood flow
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The OBF system (OBF Labs Ltd, Malmesbury, UK) is one of two systems that have been introduced for the measurement of pulsatile ocular blood flow (POBF). The instrument repeatedly measures the intraocular pressure (IOP) with a pneumatic applanation tonometer during the cardiac pulse cycle and, based on IOP variation with time, calculates the pulsatile ocular blood flow.1 It has gained popularity for use in ocular blood flow studies because of its ease of use and good reproducibility.2–4 Recent clinical publications have reported significant abnormalities in POBF in patients with normal tension glaucoma (NTG),5 age related macular degeneration,6 retinitis pigmentosa,7 and following regional ocular anaesthesia.8
To further characterise the role of POBF in health and disease, in this work we examined the relation of POBF to ICA stenosis. This relation has not been systematically characterised previously.
We recruited consecutive patients who had carotid Doppler ultrasound examination in our institute. Only patients who could be tested in the sitting position were referred for POBF examination. Patients with arrhythmia or nystagmus were excluded. In addition, any significant ocular abnormality revealed on slit lamp examination such as corneal scar, glaucoma, or previous surgery excluded that eye from the study.
Ultrasound Doppler examination of the ICA included the peak systolic velocity (PSV), end diastolic velocity (EDV), and estimated percentage stenosis.
Ocular pulse amplitude (PA) and POBF were measured by the OBF machine. All measurements were made by the same investigator (YB) using the OBF tonometer mounted on a slit lamp with the patient seated after topical anaesthesia with Benoxinate HCl 0.4%. Values reported by the machine were average of five best pulses during approximately 10 seconds of probe applanation to the eye. If the machine could not detect five measurable pulses during that period on three consecutive attempts, we marked the result as zero, denoting it as unrecordable.
Correlation between OBF values and ipsilateral ICA US-Doppler parameters was evaluated using Pearson correlation coefficient. SPSS for Windows software, version 10.0, was used for the analysis.
Fifty seven eyes of 30 patients were included in the study. There were 21 males and nine females with mean age of 66 (SD 12) years.
Figure 1 is a scattergram demonstrating values of POBF and degree of ipsilateral ICA stenosis. There was a significant negative correlation between these two parameters (Pearson correlation coefficient, r = −0.516, p<0.0001).
POBF was unrecordable by the OBF tonometer in 14 eyes, and in 11 of these cases (78.6%) ultrasound showed ipsilateral severe ICA stenosis (greater than 75% of the lumen). When these 14 eyes were excluded from analysis, there was no correlation between POBF and degree of ICA stenosis (r = −0.02, p = 0.91).
Among the 43 eyes in which OBF was recorded, it ranged from 667–2095 µl/min with a mean of 970.72. Severe stenosis of the ICA was observed in six of the 43 eyes (14%).
In 17 of the examined ICA we observed stenosis greater than 75% of the lumen; in 11 ipsilateral eyes, POBF could not be recorded by the machine (64.7%).
In seven patients, there was severe ICA stenosis on one side only (Table 1). In five of these patients, POBF was unrecordable in the eye ipsilateral to the stenosis, and was normal on the contralateral side. In one patient, POBF was 1306 µl/min on the side with 90% ICA stenosis and 1809 µl/min on the side with 30% ICA stenosis. In one patient POBF was 1650 µl/min on the side with 99% ICA stenosis and was unrecordable on the other side with only 30% stenosis.
In five patients, measurements were made before and after endarterectomy. In these cases POBF was not detectable preoperatively, and normalised following surgery (1185–1951 µl/min, average 1410).
Similar results were obtained when PA, PSV, or EDV were used for analysis, and consequently they are not included.
Heart rate, as measured by the OBF instrument, ranged from 42–90 beats per minute (mean 67.65 (13.9)).
There is current interest in determining whether reduced ocular blood flow is partly responsible for various eye diseases, such as glaucoma and age related macular degeneration. Proponents of the vascular pathogenetic hypothesis of open angle glaucoma (OAG) claim that chronic or intermittent decrease in blood flow to the optic nerve is partially responsible for the glaucomatous optic neuropathy. For example, the incidence of OAG has been reported to be higher in patients with lower perfusion pressure (blood pressure minus IOP).11 Progression of visual field loss has been related to greater than normal nocturnal decrease in systemic blood pressure.12,13 Reduced blood flow has been observed by various methods in larger ocular arteries and nerve head microcirculation in patients with POAG and NTG.14–17
Accordingly, there is much interest in measuring ocular blood flow in humans non-invasively. The OBF tonometer reflects the main—pulsatile—portion of the choroidal blood flow, which in turn is the main contributor of ocular blood flow.18,19 Thus, it may be used to study total ocular blood flow and blood flow to the optic nerve head.
We found a strong correlation between severe stenosis of the ICA and the inability of the OBF machine to record the pulsatile IOP. In certain situations, listed in the operating manual of the OBF tonometer, the machine may not record the pulsatile IOP of the eye. These include cardiac arrhythmia, poor patient fixation, dry eyes, and nystagmus. According to our results, significant stenosis of the ICA may be added to this list. After ruling out the above situations, in 64.7% of cases with significant ICA stenosis OBF could not be recorded. Presumably, the pulsatile component of blood flow to these eyes is severely reduced. Further research is needed to confirm this assumption and examine its implications for ocular disease.
Even more significant from a clinical standpoint, when OBF could not be recorded, there was a 79% chance of significant ICA stenosis on the ipsilateral side. This figure undoubtedly reflects the fact that our patients were recruited from the vascular ultrasound clinic and is higher than would be expected in the general population. Nevertheless, clinicians should consider performing cardiovascular examinations, specifically carotid ultrasound, in patients in whom pulsatile OBF can not be measured. Since the use of the OBF machine is fast and straightforward, it might even be incorporated into a screening programme of cardiovascular disease in high risk populations.
When we analysed only those eyes with recordable POBF, there was no correlation between POBF and ipsilateral ICA stenosis. Presumably, ocular blood flow is controlled by local autoregulation, and in cases of chronic severe stenosis may be maintained by collateral circulation. In this regard, it is interesting that Harris and co-workers reported that in glaucoma patients with stable visual fields, nocturnal ocular blood flow remains unchanged despite dips in systemic blood pressure.20,21 In addition, invasive animal studies have shown that retinal and choroidal blood flow is maintained when systemic blood pressure or IOP are changed.22,23
The clinical relation between POBF and extra cranial blood vessels has not been thoroughly studied. There is one case report where an inter-eye difference in measured PA was attributed to a stenotic innominate artery, with equal values measured following the dilation of the stenotic vessel.24 Two cases were reported by Clarideg and James where POBF was measured before and after surgery for ICA stenosis.25 In one case POBF was unrecordable before surgery and 173 µl/min postoperatively. In the second case POBF increased significantly from 280 to 758 µl/min. In our study we observed the normalisation of POBF in five cases following ICA surgery after being unrecordable preoperatively.
POBF values in our study were somewhat higher than previously reported in healthy eyes. Mori et al reported POBF values ranging from 290.7–1201.6 µl/min with a mean of 593.3 µl/min in 80 normal subjects using the Langham OBF tonometer (Langham Ophthalmic Technologies, Timonium, MD, USA).26 Yang et al reported a range of 306–1645 with a mean of 775.9 µl/min in 83 healthy eyes using the OBF tonograph (OBF Laboratories, UK Ltd, Wilts, UK) which is similar to the one we used.3 POBF values in the present study ranged 667–2095 with a mean of 970.72 µl/min.
In conclusion, we have demonstrated that inability to record POBF in healthy eyes may be related to severe stenosis of the ICA, and that severe ICA stenosis may signify a marked reduction in the pulsatile component of ocular blood flow. Clinicians using the OBF tonometer should be aware of this association and consider its implications for the general health of their patients. The significance of carotid artery stenosis to ocular blood flow in health and disease requires further investigation.
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