Noninvasive analysis of conjunctival microcirculation during carotid artery surgery reveals microvascular evidence of collateral compensation and stenosis-dependent adaptation

Abstract

Objective: Hemodynamically relevant internal carotid artery (ICA) stenosis is a major cause of ischemic stroke. Despite its long-term benefit, carotid endarterectomy may also be associated with severe neurologic deficits. Intraoperative and early recognition of ischemia in the region of the ICA may reduce this risk. To date, direct imaging and quantitative analysis of microvascular structures and function in the human ICA region have not been possible. We purposed to visualize and quantify ischemia/reperfusion-induced microcirculatory changes in the terminal vascular bed of the ICA in patients undergoing unilateral ICA endarterectomy. Methods: Sequential analysis of the ipsilateral and contralateral conjunctival microcirculation was performed with orthogonal polarized spectral imaging in 33 patients undergoing unilateral ICA endarterectomy because of moderate or severe ICA stenosis (North American Symptomatic Carotid Endarterectomy Trial score, 75% ± 13%), before clamping the ICA (baseline), during clamping of the external carotid artery and ICA, during reperfusion of the ICA (intraluminal shunt), during the second clamping of the ICA (shunt removal), after declamping (reperfusion) of the external carotid artery and ICA, and 15 to 20 minutes after the second ICA reperfusion. Results: During ICA clamping for shunt placement, ipsilateral and contralateral conjunctival capillary perfusion was significantly decreased, but it was completely restored after reperfusion with carotid shunting. Reclamping of the ICA for shunt removal caused microvascular dysfunction, which was significantly less pronounced than that observed during the first clamping. The individual degree of ICA stenosis was inversely correlated with the ipsilateral and contralateral decrease in conjunctival functional capillary density during the first ICA clamping. Conclusions: These results suggest adaptive mechanisms of capillary perfusion with increasing stenosis and development of collateral compensatory circulation in the vascular region of the human ICA. Conjunctival orthogonal polarized spectral imaging during unilateral ICA reconstruction enables continuous noninvasive analysis of bilateral conjunctival microcirculation in the terminal region of the ICA and enables monitoring for efficient carotid shunt perfusion during and after endarterectomy.