Cerebral Hyperperfusion after Revascularization Inhibits Development of Cerebral Ischemic Lesions Due to Artery-to-Artery Emboli during Carotid Exposure in Endarterectomy for Patients with Preoperative Cerebral Hemodynamic Insufficiency: Revisiting the "Impaired Clearance of Emboli" Concept

Abstract

The purpose of the present study was to determine whether cerebral hyperperfusion after revascularization inhibits development of cerebral ischemic lesions due to artery-to-artery emboli during exposure of the carotid arteries in carotid endarterectomy (CEA). In patients undergoing CEA for internal carotid artery stenosis (≥70%), cerebral blood flow (CBF) was measured using single-photon emission computed tomography (SPECT) before and immediately after CEA. Microembolic signals (MES) were identified using transcranial Doppler during carotid exposure. Diffusion-weighted magnetic resonance imaging (DWI) was performed within 24 h after surgery. Of 32 patients with a combination of reduced cerebrovascular reactivity to acetazolamide on preoperative brain perfusion SPECT and MES during carotid exposure, 14 (44%) showed cerebral hyperperfusion (defined as postoperative CBF increase ≥100% compared with preoperative values), and 16 (50%) developed DWI-characterized postoperative cerebral ischemic lesions. Postoperative cerebral hyperperfusion was significantly associated with the absence of DWI-characterized postoperative cerebral ischemic lesions (95% confidence interval, 0.001-0.179; p = 0.0009). These data suggest that cerebral hyperperfusion after revascularization inhibits development of cerebral ischemic lesions due to artery-to-artery emboli during carotid exposure in CEA, supporting the "impaired clearance of emboli" concept. Blood pressure elevation following carotid declamping would be effective when embolism not accompanied by cerebral hyperperfusion occurs during CEA.

Keywords: artery-to-artery embolism; carotid endarterectomy; cerebral hemodynamic insufficiency; cerebral hyperperfusion; ischemic lesion.

Figure 1

Trial profile showing the flow chart of patient numbers from initial screening to final analysis. Patients who did not have preoperative reduced cerebrovascular reactivity (CVR), did not undergo carotid endarterectomy (CEA), did not have reliable intraoperative transcranial Doppler (TCD) monitoring, had hemispheric ischemia during carotid clamping, and did not have microembolic signals (MES) during carotid exposure were excluded from the study.

Figure 2

Relationships between the number of microembolic signals (MES), postoperative CBF (cerebral blood flow), cerebral hyperperfusion, and the development of diffusion-weighted imaging (DWI)-characterized postoperative cerebral ischemic lesions. Closed and open circles indicate patients with and without DWI-characterized postoperative cerebral ischemic lesions, respectively. Red and black circles indicate patients with and without postoperative cerebral hyperperfusion (defined as postoperative CBF increase ≥100% compared with preoperative values), respectively. Whereas 15 (83%) of 18 patients without postoperative cerebral hyperperfusion showed DWI-characterized postoperative cerebral ischemic lesions, only one (7%) of 14 patients with hyperperfusion had these ischemic lesions.

Figure 3

(A) Preoperative brain perfusion single-photon emission computed tomography in a 74-year-old man with symptomatic left internal carotid artery stenosis (90%) shows reduced cerebral blood flow (left) and reduced cerebrovascular reactivity to acetazolamide (center) in the left cerebral hemisphere where hyperperfusion develops immediately after surgery (right); (B) Transcranial Doppler recording during exposure of the carotid arteries in the patient of Figure 3A shows three microembolic signals (arrows) in the power spectrum display of left middle cerebral artery blood flow. This patient had a total of 10 microembolic signals during exposure of the carotid arteries; (C) A diffusion-weighted image 6 h after surgery in the patient of Figure 3A,B shows development of new postoperative multiple high-intensity lesions in the left cerebral hemisphere (right) when compared with a preoperative image (left). These lesions did not change on diffusion-weighted imaging 24 h after surgery. This patient suffered slight motor weakness in the right upper extremity after recovery from general anesthesia, and this deficit resolved completely within 12 h.

Figure 3

(A) Preoperative brain perfusion single-photon emission computed tomography in a 74-year-old man with symptomatic left internal carotid artery stenosis (90%) shows reduced cerebral blood flow (left) and reduced cerebrovascular reactivity to acetazolamide (center) in the left cerebral hemisphere where hyperperfusion develops immediately after surgery (right); (B) Transcranial Doppler recording during exposure of the carotid arteries in the patient of Figure 3A shows three microembolic signals (arrows) in the power spectrum display of left middle cerebral artery blood flow. This patient had a total of 10 microembolic signals during exposure of the carotid arteries; (C) A diffusion-weighted image 6 h after surgery in the patient of Figure 3A,B shows development of new postoperative multiple high-intensity lesions in the left cerebral hemisphere (right) when compared with a preoperative image (left). These lesions did not change on diffusion-weighted imaging 24 h after surgery. This patient suffered slight motor weakness in the right upper extremity after recovery from general anesthesia, and this deficit resolved completely within 12 h.

Figure 4

Diagrams show the regions of interests (ROIs) for a three-dimensional, stereotactic ROI template to automatically place constant ROIs on brain perfusion single-photon emission computed tomography images. White ROIs indicate middle cerebral artery territories (precentral, central, parietal, angular, and temporal).