Evaluation of cross-circulation through circle of Willis using an ultrasonic Doppler technique. Part II. Comparison between blood flow velocity by ultrasonic Doppler flowmetry and cerebrovascular resistance

The correlation between the increase in velocity of blood flow in both the internal carotid and vertebral arteries during a carotid compression and the cerebrovascular resistance (CVR) was investigated in 11 patients with chronic ischemic cerebrovascular disease and 4 without organic brain lesions. The velocity of blood flow was measured by an ultrasonic Doppler flowmeter. CVR was calculated from cerebral blood flow and arterial blood pressure. There was no correlation between the increased velocity of blood flow in the internal carotid and vertebral arteries and CVR. The increased velocity of blood flow in patients with low CVR was, however, significantly higher than that of patients with high CVR. The investigation of cross-circulation by ultrasonic Doppler flowmetry is a useful non-invasive method for the detection of changes in cerebral vascular resistance.     

Cerebral hemodynamics in relation to patterns of collateral flow.

BACKGROUND AND PURPOSE: We sought to investigate the relation between collateral flow via different pathways and hemodynamic parameters measured by dynamic susceptibility contrast-enhanced MRI in patients with severe carotid artery disease. METHODS: Dynamic susceptibility contrast-enhanced MRI was performed in 66 patients and 33 control subjects. Patients had severe stenosis (>70%, n=12), unilateral occlusion (n=38), or bilateral occlusion (n=16) of the internal carotid artery (ICA). Cerebripetal flow and collateral flow via the circle of Willis were investigated with MR angiography. Collateral flow via the ophthalmic artery was investigated with transcranial Doppler sonography. RESULTS: Patients with ICA stenosis had well-preserved cerebral perfusion and were in general not dependent on collateral supply. Patients with unilateral ICA occlusion had impaired cerebral perfusion. However, appearance time, peak time, and mean transit time in white matter were less increased in patients with than in patients without collateral flow via the circle of Willis (P<0.05). Furthermore, patients with collateral flow via both anterior and posterior communicating arteries had less increased regional cerebral blood volume than patients with collateral flow via the posterior communicating artery only (P<0.05). Patients with bilateral ICA occlusion had severely compromised hemodynamic status despite recruitment of collateral supply. CONCLUSIONS: In patients with unilateral ICA occlusion, the pattern of collateral supply has significant influence on hemodynamic status. Collateral flow via the anterior communicating artery is a sign of well-preserved hemodynamic status, whereas no collateral flow via the circle of Willis or flow via only the posterior communicating artery is a sign of deteriorated cerebral perfusion.     

Collateral variations in circle of willis in atherosclerotic population assessed by means of transcranial color-coded duplex ultrasonography

BACKGROUND AND PURPOSE: Transcranial color-coded duplex ultrasonography combined with common carotid artery (CCA) compression can be used to assess the collateral function of the circle of Willis. The aim of this study was to assess the unknown fraction of hemodynamic functional anterior and posterior communicating arteries (AcoA and PcoA, respectively) in an atherosclerotic population with no cerebrovascular symptoms. METHODS: In 76 patients with a mean age of 61 (35 to 89) years, the blood flow velocity changes in the precommunicating parts (A1 and P1, respectively) of the anterior and posterior cerebral arteries were measured during CCA compression. The AcoA was defined as functional if blood flow was reversed in the ipsilateral A1 and enhanced in the contralateral A1 during CCA compression. The PcoA was defined as functional if the flow velocity in the P1 was enhanced >20% during ipsilateral CCA compression. RESULTS: It was possible to assess cross flow through the anterior part of the circle of Willis in 95% of the subjects. Failure of this collateral pathway was caused by a hypofunctional AcoA in 4% and a hypofunctional A1 in 1% of the subjects. Anomalies in the posterior part of the circle of Willis hampering collateral flow from the basilar to the internal carotid artery were found in 45% of the hemispheres. Thirty-eight percent of PcoAs were hypofunctional, and 7% of the posterior cerebral arteries had a persistent fetal anatomy. CONCLUSIONS: We found that in subjects with no cerebrovascular symptoms, the anterior collateral pathway of the circle of Willis was nearly always functional. In contrast, the posterior collateral pathway was nonfunctional in almost half of the total number of hemispheres. Comparing these basic data with data from patients with cerebral ischemic disease might further help to elucidate the importance of the collateral capacity of the circle of Willis.     

Transcranial Doppler in cerebrovascular disease

Doppler analysis of flow in intracranial arteries is now possible using a 2 MHz probe allowing sufficient penetration of bone to obtain signals noninvasively. Thirty-two normal subjects, and 11 patients with cerebrovascular diseases including vasospasm following subarachnoid hemorrhage, middle cerebral artery stenosis, and extracranial internal carotid artery stenosis were studied by transcranial Doppler. Increased peak velocity and spectral broadening of the reflected signal corresponded to clinical and angiographic evidence of middle cerebral artery vasospasm or stenosis. Decreased peak velocity and blunted waveforms occurred in the middle cerebral artery ipsilateral to severe extracranial internal carotid stenosis with poor crossfilling from the contralateral carotid artery. Abnormalities resolved following carotid endarterectomy. Transcranial Doppler identifies vasospasm or stenosis of the middle cerebral artery and may allow noninvasive evaluation of collateral flow across the anterior circle of Willis in patients with extracranial carotid artery stenosis.     

The arterial patterns associated with internal carotid disease and cerebral infarcts

In 20 necropsies with 15 stenosed and 17 thrombotic occluded internal carotid arteries there were 46 cerebral infarcts larger than 1 cm diameter. Using portmortem arteriographic and pathological techniques the patterns of the neck and brain artery systems were correlated with the situation and extent of the brain infarcts. Massive infarcts involving two major cerebral artery territories were associated with distal internal carotid artery occlusion and grossly ineffective cervical and circle of Willis anastomoses. Isolated middle cerebral artery territory infarcts were associated with internal carotid occlusion or stenosis and impairment of the circle of Willis anastomoses, perhaps with middle cerebral artery stenosis. The pattern of adequate size arteries determined if these infarcts were total, deep central, anterior, medium or posterior partial territory infarcts. Boundary zone infarcts were associated with internal carotid artery disease and limitation of anterior or posterior circle of Willis anastomoses. These limitations determined which boundary zones were affected. Isolated anterior cerebral artery territory infarcts were associated with bilateral internal carotid disease and an anterior cerebral artery stenosis or small caliber anterior communicating artery. Isolated posterior cerebral artery territory infarcts were associated with internal carotid disease and a direct impairment of the ipsilateral posterior cerebral artery capability.     

Three-dimensional transcranial Doppler blood flow mapping in patients with cerebrovascular disorders

We investigated 60 patients with cerebrovascular disorders using a three-dimensional transcranial Doppler blood flow mapping system. A composite display of the circle of Willis is created with computer assistance, allowing accurate vessel identification and optimal data documentation of blood flow velocity and direction in the basal cerebral arteries. The basilar artery was insonated in every patient; the middle cerebral artery and the most distal internal carotid artery were found in 95% of the patients, the anterior cerebral artery in 85%, and the posterior cerebral artery in 84%. Insonation problems occurred predominantly in elderly women. Transcranial Doppler blood flow mapping showed an abnormal result in 23 of 60 patients (38%). An intracranial stenosis with greater than 50% diameter reduction or occlusion was found in 10 of 31 patients (32%) with completed stroke, reversible ischemic neurologic deficit, or transient ischemic attack. Collateral blood flow mechanisms could be demonstrated in patients with extracranial carotid artery occlusions. Intra-arterial cerebral angiography performed in 21 patients confirmed the transcranial Doppler blood flow mapping diagnosis in 19 (90.5%). In one patient an arteriovenous malformation diagnosed by transcranial Doppler blood flow mapping was confirmed by magnetic resonance imaging.     

Collateral configuration of the circle of Willis: transcranial color-coded duplex ultrasonography and comparison with postmortem anatomy

BACKGROUND AND PURPOSE: The anterior communicating artery (AcoA) and posterior communicating arteries (PcoA) of the circle of Willis provide the main route for collateral blood flow in cases of carotid artery obstruction. Transcranial color-coded duplex ultrasonography (TCCD) allows real-time measurement of the collateral function of the AcoA and PcoA. The primary objective of this study was to determine the collateral artery threshold diameters for supplying collateral flow. METHODS: In 12 acute stroke patients with a median age of 75 years (51 to 91 years), the collateral integrity of the circle of Willis as assessed by TCCD and carotid compression tests was compared with their postmortem anatomy. The lengths and diameters of the collateral arteries were measured. RESULTS: TCCD demonstrated absent anterior collateral flow in 3 patients. In 1 of these patients, absence of anterior cross-flow was due to an occluded anterior cerebral artery, which was revealed at autopsy. Absent posterior collateral flow was found in 14 hemispheres. In 2 of these hemispheres, autopsy revealed a fetal configuration of the posterior cerebral artery hampering posterior collateral flow. The median (range) diameters as found at autopsy of the functional (n=19) and nonfunctional (n=16) collateral arteries of the circle of Willis were 1.1 (0.4 to 2.0) and 0.5 (0.3 to 0.7) mm, respectively (P=0.003). PcoA diameters were found to correlate negatively (rho=-0. 50, P=0.01) to the diameters of their accessory P1 segments. CONCLUSIONS: The threshold diameter allowing for cross-flow through the primary collateral arteries of the circle of Willis is between 0. 4 and 0.6 mm.     

颈动脉-海绵窦瘘的经颅多普勒超声研究

采用彩色三维经颅多普勒超声观察18例颈动脉-海绵窦瘘血流情况,发现其引流静脉多以眼上静脉为主,患侧颈内动脉流速明显高于健侧;患侧MCA、ACA流速低于健侧;压迫患侧颈总动脉,患侧颈内动脉(瘘口以上)出现不同程度的倒灌血流,眼上静脉的动脉化且血流反向的频谱特征为颈动脉-海绵窦瘘最典型的表现,其流速与瘘口大小,引流路径及流量的高低相关.经眶窗检测颈内动脉虹吸段时,其流速受瘘口所在位置的影响,观察颅内盗血情况可粗略估计瘘口大小.TCD检测颈动脉-海绵窦瘘还可了解病人 Willis环代偿能力,为必要时行一侧颈内动脉闭塞提供客观依据.     

Cerebral aneurysms and variations in the circle of Willis

In order to obtain information about the relationship between variations in the circle of Willis and aneurysms, 44 complete circles of Willis with aneurysm were studied macroscopically. The incidence of variations was significantly higher in the aneurysm series than in the control circles without aneurysm. There was a definite correlation between asymmetric proximal segments of the anterior cerebral artery and aneurysms of the anterior communicating artery, and a tendency to correlation was found in the case of asymmetric posterior communicating arteries and aneurysms on the internal carotid artery-posterior communicating artery junction. In the light of these findings it seems likely that through hemodynamic changes variation in the circle of Willis plays some role in the development of cerebral aneurysms.     

Absence of both internal carotid arteries

Summary A 63-year-old man developed a slight left hemiparesis. CT scan showed an intracerebral tumour, which was later identified as glioblastoma multiforme. Angiographic examination revealed the absence of both internal carotid arteries. Blood supply of anterior and middle cerebral arteries was provided by communication between a tortuous megadolichobasilar artery and the circle of Willis through enlarged posterior communicating arteries. The case is reported with reference to clinical symptoms as well as angiographic and anatomical findings of 17 comparable cases mentioned in literature.     

Relationship between ophthalmic artery blood flow and recanalization of occluded carotid artery. Ultrasonic Doppler study

Ophthalmic artery blood flow in 5 patients with internal carotid artery occlusion of sudden onset was monitored by an ultrasonic Doppler flowmeter to investigate the possible relationship to spontaneous recanalization of the occluded artery. The occluded internal carotid arteries of 2 patients were confirmed angiographically to recanalize and the reversed flow of their ophthalmic arteries changed to physiological flow after the recanalization. The ophthalmic artery blood flow remained reversed in 2 patients whose occluded internal carotid arteries did not recanalize on the follow up angiograms. In the other patient, whose ophthalmic artery blood flow was not detected by the ultrasonic Doppler flowmeter in the acute stage, physiological flow through the ophthalmic artery was detected later. The occluded internal carotid artery did not recanalize and this physiological ophthalmic artery blood flow was filled through the circle of Willis.     

Echo-enhanced transcranial color-coded duplexsonography to study collateral blood flow in patients with symptomatic obstructions of the internal carotid artery and limited acoustic bone windows

We prospectively evaluated 30 consecutive patients with echo-enhanced transcranial color-coded duplexsonography (TCCD) and correlative transfemoral digital subtraction angiography to assess the diagnostic efficacy of echo-enhanced TCCD for evaluation of collateral pathways through the circle of Willis in patients with limited acoustic bone windows and critical symptomatic carotid disease. Echo-enhanced TCCD detected collateral blood flow through the anterior communicating artery in 16 of 18 patients (sensitivity 89%, 95% CI 65-99%) and was false positive in one out of 12 patients without collateral flow (specificity 92%, 95% CI 59-100%). For the posterior communicating artery, sensitivity was 11/14 (79%, 95% CI 49-95%) and specificity was 15/16 (94%, 95% CI 70-100%). Echo-enhanced TCCD enables to study collateral blood flow through the communicating arteries of the circle of Willis with high sensitivity and specificity in patients with obstructions of the internal carotid artery and limited acoustic bone windows.     

The anatomy of the circle of Willis as a predictive factor for intra-operative cerebral ischemia (shunt need) during carotid endarterectomy

The collateral flow to the cerebral hemisphere after carotid cross clamping during carotid endarterectomy is mainly through the circle of Willis, and the circle is incomplete in the majority of cases. A correlation between the status of the circle of Willis and the necessity of shunting was evaluated in 67 carotid endarterectomies with pre-operative four-vessel cerebral angiogram. All carotid endarterectomies were performed with selective shunting, based on the change of consciousness and motor function after carotid test clamping under regional anesthesia. Of the 55 patients with either an anterior or a posterior communicating artery, only four (7.3%) required shunting. Twelve patients had neither anterior nor posterior communicating artery, and 10 (83.3%) showed signs of cerebral ischemia necessitating shunting. Mandatory shunt was significantly higher in patients with absence of collaterals (p = 0.00). The rate of intraoperative cerebral ischemia was significantly higher in patients with poor collateral circulation defined by the anatomy of the circle of Willis.     

A model of the cerebral and cerebrospinal fluid circulations to examine asymmetry in cerebrovascular reactivity.

The authors examined the steal phenomenon using a new mathematical model of cerebral blood flow and the cerebrospinal fluid circulation. In this model, the two hemispheres are connected through the circle of Willis by an anterior communicating artery (ACoA) of varying size. The right hemisphere has no cerebrovascular reactivity and the left is normally reactive. The authors studied the asymmetry of hemispheric blood flow in response to simulated changes in arterial blood pressure and carbon dioxide concentration. The hemispheric blood flow was dependent on the local regulatory capacity but not on the size of the ACoA. Flow through the ACoA and carotid artery was strongly dependent on the size of the communicating artery. A global interhemispheric "steal effect" was demonstrated to be unlikely to occur in subjects with nonstenosed carotid arteries. Vasoreactive effects on intracranial pressure had a major influence on the circulation in both hemispheres, provoking additional changes in blood flow on the nonregulating side. A method for the quantification of the crosscirculatory capacity has been proposed.     

Histochemical studies of the adrenergic innervation of canine cerebral arteries

The glyoxylic acid method was used to examine the adrenergic innervation of the major cerebral arteries of the circle of Willis in dogs. Fluorescent nerve fibers were observed in whole-mount preparations of the part of the internal carotid artery lying in the cavernosus sinus, the anterior, middle and posterior cerebral arteries, the posterior communicating artery and the basilar artery. Adrenergic nerve fibers were most abundant in the proximal portions of the anterior, middle and posterior cerebral arteries as well as in the posterior communicating artery. The distal smaller arteries were less densely innervated than larger ones. The basilar artery contained a moderate number of fluorescent fibers while the internal carotid artery lying in the cavernosus sinus had a very sparse innervation. The peak wavelengths of the excitation and emission spectra of the fluorescence were analyzed by means of a microepifluorescence spectrophotometer and were about 415 and 465 nm, respectively. These values suggest that the fluorescent fibers are adrenergic ones containing norepinephrine.     

Bilateral internal carotid artery agenesis with artery compression of the brain parenchyma

Bilateral internal carotid artery (ICA) agenesis is an extremely rare congenital anomaly. The most common type of collateral circulation is developed through the circle of Willis via the basilar and posterior communicating arteries. Both anterior circulations are usually supplied by enlarged posterior communicating arteries (PCOMs). We present an unusual case of bilateral ICA agenesis, which is associated with dolichoectatic left PCOM and left posterior cerebral artery (PCA) compression of left basal ganglia and thalamus. These complex cerebral and vascular anomalies can be noninvasively revealed and evaluated by CT and MR.     

PET study on cerebral hemodynamics in internal carotid artery occlusion--the pathogenesis of watershed infarction

We studied positron emission tomography in nine patients with unilateral internal carotid artery occlusion, selected as having good collateral circulation through the anterior portion of the circle of Willis. Analyses of regional cerebral blood flow, cerebral oxygen metabolic rate, oxygen extraction fraction, and cerebral blood volume allowed quantitative evaluation of the regional hemodynamic status, especially in relation to watershed area. The patient group has a significantly (p less than 0.01) decreased regional blood flow in the middle cerebral artery territory and the surrounding watershed areas of the occluded hemisphere, as compared with eight control subjects. Values of oxygen extraction fraction became progressively greater farther from the circle of Willis, attaining the highest level in the superior parietal and posterior temporal-occipital watershed area. Oxygen extraction fraction gave information on the balance of energy supply and demand, serving as an index of the oxygen carriage reserve. A concomitant decrease in the ratio of cerebral blood flow to volume suggested reduction in mean flow velocity with possible development of "stagnation thrombus". These findings suggest 1) hemodynamic vulnerability of watershed areas after internal carotid artery occlusion and 2) importance of systemic hemodynamic factors such as blood pressure and circulating blood volume in the genesis of watershed infarctions.     

Effect of internal carotid artery occlusion on intracranial hemodynamics. Transcranial Doppler evaluation and clinical correlation

Neurologic deficits that occur simultaneously with or subsequent to internal carotid artery occlusion may be influenced by the adequacy of the intracerebral collateral circulation. Transcranial Doppler ultrasonography was used to evaluate mean middle cerebral artery blood velocity and blood flow in major collateral arteries in 78 patients, including 39 patients with 40 internal carotid artery occlusions and 39 control patients with less severe extracranial cerebrovascular disease, matched for age and sex distribution. Middle cerebral artery blood velocity was 38.9 +/- 17.9 cm/sec ipsilateral to an occlusion, 50.9 +/- 18.3 cm/sec contralateral to an occlusion (p less than 0.01), and 56.8 +/- 14.4 cm/sec in the controls (p less than 0.01). Pulsatility index ipsilateral to an occlusion (0.86 +/- 0.32) was reduced compared with contralateral and control pulsatility indexes (1.05 +/- 0.33 and 1.03 +/- 0.18) respectively; p less than 0.05). Major intracerebral collateral arteries were detectable in 94.9% of occlusion patients and in 53.8% of controls (p less than 0.01). A posterior communicating artery was demonstrated ipsilateral to an occlusion in 80.0% of the patients and contralateral to an occlusion in 39.5% (p less than 0.01). An ipsilateral posterior communicating artery was identified in all 10 asymptomatic occlusions and in 75.8% of the symptomatic ones. Pulsatility index was 1.02 +/- 0.34 for asymptomatic occlusions and 0.76 +/- 0.30 for symptomatic occlusions (p less than 0.01). Transcranial Doppler ultrasonography permits noninvasive quantification of the cerebral hemodynamic consequences of internal carotid artery occlusion and direct evaluation of the collateral blood supply, which can be correlated with symptomatology.     

Spect measurements of regional cerebral perfusion and carbondioxide reactivity: Correlation with cerebral collaterals in internal carotid artery occlusive disease

Background The aim of the present study was to assess the regional variation in cerebral perfusion, vasomotor reactivity (VMR) and the role of cerebral collaterals in patients with symptomatic internal carotid artery (ICA). Methods Seventeen functionally independent patients (60±9 years, mean±SD) with a unilateral symptomatic internal carotid artery occlusion and a <30% contralateral ICA stenosis were investigated. (99 m) Tc-hexamethyl propyleneamine oxime (HMPAO) single photon emission computed tomography (SPECT) was performed to study cerebral blood flow in rest and during a CO₂ challenge in the cerebellum, temporal lobe, occipital lobe, basal ganglia, frontal lobe and parietal lobe. Time of flight and phase contrast MRA were used to study collateral flow via circle of Willis. Results In rest, cerebral perfusion on the side ipsilateral to the ICA occlusion was decreased compared with the contralateral side in the basal ganglia (p<0.05), frontal lobe (p<0.01) and parietal lobe (p<0.01). During a CO₂ challenge only the ipsilateral frontal lobe demonstrated a perfusion decrease compared with the contralateral frontal lobe (p<0.05). Furthermore, in patients without collateral flow via the anterior circle of Willis the perfusion of the ipsilateral frontal lobe was significantly decreased (p<0.01) during the CO₂ challenge and crossed cerebellar diaschisis with a decreased perfusion on the contralateral cerebellar hemisphere was detected (p<0.05). No cerebral blood flow (CBF) differences were found for present/absent collateral flow via the posterior communicating artery. Conclusion Regional assessment of cerebral perfusion and VMR with SPECT demonstrated the heterogeneity of cerebral hemodynamics and the importance of collateral flow via the anterior circle of Willis. Received in revised form: 22 November 2005     

Anatomic variations in the circle of Willis in patients with symptomatic carotid artery stenosis assessed with multidetector row CT angiography

PURPOSE: To assess the presence of anterior and posterior collateral pathways in the circle of Willis in patients with symptomatic carotid artery stenosis (SCAS) and to compare this to patients without carotid artery stenosis. MATERIALS AND METHODS: Multislice CT angiography was performed in 91 patients and 91 control subjects. Using consensus reading, 2 observers evaluated the presence and diameter of the anterior communicating artery (AcomA), the A1 segments of the anterior cerebral arteries, the posterior communicating arteries (PcomA) and the P1 segments of the posterior cerebral arteries. Anterior or posterior pathways were assumed to be present if the diameter of continuous arterial segments was >1 mm; both A1 segments and AcomA anterior, and ipsilateral P1 segment and PcomA posterior. Comparison between patients and controls was performed using the chi(2) test. RESULTS: In the patients we found significantly more hypoplastic (<1 mm) or invisible A1 segments (16 and 14 vs. 4 and 1, respectively, p < 0.01). The AcomA was invisible in 4 patients versus 1 control. An isolated compromised anterior pathway and a combined compromised anterior and posterior pathway occurred more frequently in the patients as compared to the controls; 9 versus 1% (p < 0.01) and 26 versus 4% (p < 0.01). CONCLUSION: A compromised anterior collateral pathway, usually combined with a compromised posterior pathway, occurs more frequently in patients with SCAS as compared to controls, which suggests a relation between symptomatic carotid stenosis and an incomplete circle of Willis.