Background After the occlusion of an internal carotid arterythe principal source of collateral flow is through the arteriesof the circle of Willis, but the size and patency of these arteriesare quite variable. Study of the anatomy of the collateral pathwaysin patients with internal-carotid-artery occlusion with or withoutinfarction in the watershed area of the deep white matter mayidentify patterns that afford protection from ischemic infarction.
Methods Using conventional magnetic resonance imaging and three-dimensionalphase-contrast magnetic resonance angiography, we evaluated29 consecutive patients (32 hemispheres at risk) with angiographicallyproved occlusion of the internal carotid artery. Four collateralpathways to the occluded vessel were evaluated: the proximalsegment of the anterior cerebral artery, the posterior communicatingartery, the ophthalmic artery, and leptomeningeal collateralvessels from the posterior cerebral artery.
Results Only features of the ipsilateral posterior communicatingartery were related to the risk of watershed infarction. Thepresence of posterior communicating arteries measuring at least1 mm in diameter was associated with the absence of watershedinfarction (13 hemispheres, no infarcts; P<0.001). Conversely,there were 4 watershed infarcts in the 6 hemispheres with posteriorcommunicating arteries measuring less than 1 mm in diameterand 10 infarcts in the 13 hemispheres with no detectable flowin the ipsilateral posterior communicating artery.
Conclusions A small (<1 mm in diameter) or absent ipsilateralposterior communicating artery is a risk factor for ischemiccerebral infarction in patients with internal-carotid-arteryocclusion.
The risk of cerebral infarction is multifactorial and includesgenetic, anatomical, and environmental considerations. If amajor vessel such as a carotid artery is occluded, flow maystill be possible through primary or secondary collateral vessels.Primary collateral vessels are those that can respond quicklyto low perfusion pressure with simple reversal of flow. Secondarycollateral vessels require time for recruitment and are acquiredin response to the stress of chronic hypoperfusion. Collateralpathways can protect perfusion in the event of severe stenosisor occlusion of a carotid artery. Therefore, the size and patencyof primary collateral pathways may be risk factors for cerebralinfarction in patients with severe stenosis or occlusion ofa carotid artery.
To test this hypothesis, we studied subjects with occlusionof the internal carotid artery to assess their individual patternsof collateral pathways. Since these patients are dependent oncollateral flow for cerebral perfusion, this population is agood one in which to evaluate cerebrovascular reserve from collateralflow. We correlated patterns of primary and secondary collateralflow with the presence and radiologic character of cerebralinfarctions to ascertain the importance of individual collateralpathways in the perfusion of the cerebral hemisphere.
Methods
Twenty-nine consecutive patients presenting to Stanford UniversityHospital with 32 hemispheres at risk due to occlusion of theinternal carotid artery were enrolled in the study. Two of thepatients had both internal carotid arteries occluded. Anotherpatient, followed with serial examinations, was treated fora giant aneurysm with intraluminal occlusion of an internalcarotid artery, followed several weeks later by surgical alterationof the circle of Willis. All patients had angiographically provedocclusion of the internal carotid artery.
Twenty-four patients had progressive stenosis leading to chronicocclusion of the internal carotid artery; the cause was atheroscleroticdisease in 23 and radiation therapy for a head and neck tumorin 1. Five patients had acute occlusion of the internal carotidartery: three from therapeutic balloon occlusion to reduce pressurein cerebral aneurysms and two from acute dissection (one traumaticand one due to fibromuscular dysplasia).
All patients underwent routine spin-echo magnetic resonanceimaging of the brain with conventional T1-weighted (repetitiontime, 800 msec; echo time, 20 msec; 1 excitation), double-echoT2-weighted (repetition time, 2500 msec; echo time, 30 and 80msec; 1 excitation) pulse sequences and three-dimensional phase-contrastmagnetic resonance angiography through the circle of Willis.The three-dimensional phase-contrast magnetic resonance angiographicevaluation of the circle of Willis was accomplished with a repetitiontime of 25 msec, a minimal echo time (<10 msec), a flip angleof 25 degrees, and one excitation. Flow encoding producing a180-degree phase shift for a velocity of 40 cm per second wasused to produce images sensitive to all directions of flow.A matrix of 256 by 256 was used to maximize the resolution ofsmall vessels while not exceeding reasonable scanning times.All images were acquired on a 1.5-T magnetic resonance imagingsystem (Signa, GE Medical Systems, Milwaukee).
Individual collateral pathways were identified by three-dimensionalphase-contrast magnetic resonance angiography1,2,3. Two primaryand two secondary collateral pathways were analyzed: retrogradeflow (toward the internal carotid artery) in the proximal segmentof the anterior cerebral artery; posterior-to-anterior (retrograde)flow in the posterior communicating artery; retrograde flowin the ophthalmic artery; and flow in the leptomeningeal collateralvessels from the posterior cerebral artery, which is a potentialpathway from the posterior to the anterior circulation. Theproximal segment of the anterior cerebral artery is a potentialcollateral conduit from the contralateral internal carotid arterythrough the anterior communicating artery. The ophthalmic-arterycollateral represents a potential conduit between the externalcarotid artery and the ipsilateral internal carotid artery.The vessels forming the circle of Willis represent primary collateralsources (Figure 1). Recruitment of flow from the ophthalmicartery and leptomeningeal collateral vessels takes longer andrepresents secondary collateral pathways.
The circle of Willis represents the primary collateral pathway in the case of occlusion of a major vessel. The proximal segment of the anterior cerebral artery (A1) can provide hemispheric cerebral blood flow from the contralateral internal carotid artery if the anterior communicating artery is patent. The basilar artery can supply collateral flow to the anterior circulation (territory normally supplied by the internal carotid arteries) through the proximal segment of the posterior cerebral artery (P1), with reversal of flow through the posterior communicating artery. The ophthalmic artery provides a potential collateral pathway to the internal carotid artery by means of multiple anastomoses with the ipsilateral external carotid artery. Leptomeningeal collateral vessels between distal branches of the middle and posterior cerebral arteries are not shown.
The magnetic resonance image of each patient's brain was evaluatedfor infarction by a senior neuroradiologist who was unawareof the results of angiography. All infarcts were characterizedas cortical, watershed (infarction in the watershed area ofthe deep white matter), mixed (those containing both corticaland watershed components), or other (infarcts not falling intothe first three categories). It was assumed that watershed infarctsare due to low perfusion in the distal territories of the majorintracranial arteries4 and therefore indicate a hemodynamiccause of infarction. Infarcts categorized as mixed all had substantialwatershed components and were included with that group for statisticalanalysis. Non-watershed infarcts can be related to factors suchas thromboembolism and thus were not considered to be hemodynamicin origin.
The magnetic resonance angiographic images were analyzed qualitativelyfor the presence or absence of four specific anatomical patternswith the use of axial collapsed-projection images. Velocityencoding during the image acquisition allows the productionof images sensitive to the direction of the flow. When theseimages are reconstructed, they may be displayed as axial compositeimages that show flow in three orthogonal directions: rightor left, anterior or posterior, and superior or inferior. Oncethe presence of a specific anatomical pathway was establishedon the projection images, flow-sensitive images were evaluatedto determine whether that anatomical pathway served as a collateralvessel to the hemisphere jeopardized by internal-carotid-arteryocclusion.
Since the status of the posterior communicating artery varies,the patients in the study were divided into three groups onthe basis of the size of this vessel: large, small, or not visualizedby either conventional or magnetic resonance angiography. Formagnetic resonance angiography the minimal threshold of resolutionof small posterior communicating arteries is uncertain. Verysmall vessels are occasionally seen on conventional angiographybut not on magnetic resonance angiography. These vessels areless than 1 mm in diameter on conventional angiograms. Therefore,for magnetic resonance angiography, a threshold of less than1 mm was used to define the small posterior communicating arteries.All patients with posterior communicating arteries visualizedby angiography but not magnetic resonance angiography and thosewith posterior communicating arteries just visible by magneticresonance angiography were considered to have small posteriorcommunicating arteries. Patients whose posterior communicatingarteries were easily visualized (those 1 mm in diameter) bymagnetic resonance angiography were considered to have largeposterior communicating arteries. This grouping of patientsaccording to the size of the posterior communicating arterieswas done separately from the analysis of the magnetic resonanceimages for infarcts to avoid any potential bias.
Two of the six patients assigned to the group with small posteriorcommunicating arteries had posterior communicating arteriesthat were visualized with conventional angiography but weretoo small to be seen on magnetic resonance angiography. Thus,the direction of the flow could not be determined in these twopatients; retrograde flow was assumed to exist in these smallvessels for the purpose of statistical analysis. This assumptionis conservative, since anterograde flow (away from the occludedinternal carotid artery) in these tiny posterior communicatingarteries is hemodynamically unlikely. Furthermore, if anterogradeflow was present, it would essentially exclude this vessel asa collateral source for the occluded internal carotid artery.One patient had a posterior communicating artery originatingdirectly from the occluded internal artery (also known as fetalorigin), with no communication to the basilar artery. This patientwas classified as having an absent posterior communicating arteryfor the purposes of statistical analysis, since the two conditionsare hemodynamically equivalent.
Each patient was assigned to a group on the basis of his orher collateral-flow pattern. Fisher's exact test was used toestablish whether the presence of an infarct was related tothe collateral-flow pattern. Confidence intervals for odds ratioswere calculated with the use of asymptotic methods based onthe logistic model. When no infarcts were observed for a giventwo-by-two classification, a value of 0.5 was added to eachcount for the calculation of odds ratios and confidence intervalsin order to avoid dividing these values by zero. Calculationswere done with SAS version 6.07,5 which uses the algorithm ofMehta and Patel6 to perform Fisher's exact test for contingencytables larger than two by two.
Results
Twenty-nine patients with 32 hemispheres at risk due to occlusionof the internal carotid artery were evaluated. Twenty-one infarctswere observed in this series of patients; 14 were of the watershedtype. The severity of symptoms in the watershed-infarct groupranged from no apparent symptoms in one patient to dense hemiplegiaand global aphasia in another. Most patients with watershedinfarcts were left with mild-to-moderate motor or speech deficits.Posterior communicating arteries were visualized in 19 of 32hemispheres (59 percent); 13 (41 percent) were large and 6 (19percent) were small. Twenty (62 percent) had retrograde flowin the proximal segment of the anterior cerebral artery. Twenty-seven(84 percent) had evidence of secondary collateral development:12 (37 percent) had reversed flow in the ophthalmic artery,and 15 (47 percent) leptomeningeal collateral flow.
Despite the range in the prevalence of collateral pathways,only the presence and size of the posterior communicating arteriescorrelated (either positively or negatively) with watershedinfarction (Table 1 and Table 2). Table 1 shows infarct-prevalencedata according to the status of the posterior communicatingartery. Large ( 1 mm) posterior communicating arteries wereseen in 13 hemispheres at risk, none of which had watershedinfarcts. Figure 2 shows the typical findings in a patient witha large posterior communicating artery and no evidence of awatershed infarction despite occlusion of the internal carotidartery. Four non-watershed infarcts (31 percent) were observedin this group.
Figure 2. Typical Findings in a Patient with Occlusion of the Right Internal Carotid Artery, a Large Right Posterior Communicating Artery (White Arrow), and No Watershed Infarct.
A direction-sensitive magnetic resonance angiogram (Panel A) through the circle of Willis shows retrograde flow (posterior to anterior) in the posterior communicating artery. Anterior-to-posterior flow in the proximal segment of the right anterior communicating artery (curved arrow) is bright, whereas posterior-to-anterior flow in other segments is dark. The proximal segment of the left posterior cerebral artery (black arrow) and the proximal segment of the left middle cerebral artery (arrowhead) are also shown. A selected T-weighted magnetic resonance image (Panel B) through the watershed area of the deep white matter reveals no evidence of infarction.
Six hemispheres at risk had small (<1 mm) posterior communicatingarteries, four (67 percent) of which had watershed infarcts.Two of the watershed infarcts were large, and two were small(Table 1). The other two infarcts in this group were large corticalinfarcts.
The remaining 13 hemispheres at risk had no radiologically demonstrableposterior-communicating-artery collateral flow. Ten hemispheresat risk (77 percent) in this group had watershed infarctions.Seven had large watershed infarcts, and one had a small watershedinfarct. Two patients had mixed infarcts with large watershedcomponents. Figure 3 shows the typical findings in a patientwith an occluded right internal carotid artery, no radiologicallydiscernible right posterior communicating artery, and a largewatershed infarct.
Figure 3. Typical Findings in a Patient with Occlusion of the Right Internal Carotid Artery, No Radiologically Discernible Posterior Communicating Artery, and a Large Watershed Infarct.
A magnetic resonance angiogram (Panel A) through the circle of Willis shows no evidence of a posterior communicating artery. The right ophthalmic artery is dilated (arrow) and had anterior-to-posterior flow on a direction-sensitive angiogram (not shown), suggesting that this vessel serves as a collateral pathway. Asymmetry of flow between the right and left posterior cerebral arteries suggests leptomeningeal collateral flow from the right posterior cerebral artery (curved arrow) to the middle cerebral artery (arrowhead). A selected T-weighted magnetic resonance image (Panel B) reveals a large watershed infarct in the right hemisphere (arrow).
Only two patients without collateral flow in the posterior communicatingartery did not have watershed infarctions. Both had large ophthalmicarteries with retrograde flow. One had bilateral internal-carotid-arteryocclusion and reverse flow in both ophthalmic arteries. Thispatient had a large posterior communicating artery supplyingone hemisphere at risk but no posterior communicating arterysupplying the other hemisphere. The patient was blind ipsilateralto the absent posterior communicating artery. Vision was describedas only mildly impaired ipsilateral to the large posterior communicatingartery.
The presence of posterior-to-anterior collateral flow in largeposterior communicating arteries correlated with the absenceof watershed infarcts (P<0.001). Table 2 shows the odds ofinfarction according to the status of the posterior communicatingartery. No other combinations of collateral flow showed thistype of correlation.
Discussion
Our data, obtained with three-dimensional phase-contrast magneticresonance angiography, show that one collateral pathway, a largeposterior communicating artery, may protect against watershedinfarction in patients with ipsilateral occlusion of the internalcarotid artery. Conversely, a very small or absent ipsilateralposterior communicating artery increases the risk of a watershedinfarction in these patients. Another study7 recently demonstratedthe importance of the size of the posterior communicating arteryto collateral perfusion. In that study, the size of the artery,measured preoperatively, was a good predictor of tolerance ofischemia after deliberate occlusion of the upper (P = 0.004)or lower (P = 0.036) basilar artery in patients with basilar-arteryaneurysms.
No other pattern of collateral flow correlated with either thepresence or absence of watershed infarction. However, otherpatterns of primary and secondary collateral flow were foundtoo infrequently in this study population to draw any finalconclusions about them.
Atheromatous disease is the single largest cause of internal-carotid-arteryocclusion. A recent study8 reports progression to complete occlusionin 4.4 percent of 993 patients undergoing medical treatmentfor atheromatous carotid-artery disease. Twenty-three percentof these patients (10 of 44) were asymptomatic at the time ofangiographic diagnosis of occlusion. Another study9 describesprogression of stenosis of the internal carotid artery to occlusionin 27 asymptomatic patients. This suggests that internal-carotid-arteryocclusion may be an underrecognized complication of conservativemanagement. The question is why are some of these patients asymptomatic?
The circle of Willis provides the principal collateral pathwayin the event of internal-carotid-artery occlusion. Circulationfrom the contralateral internal carotid artery may be providedby a patent anterior communicating artery in which there isanterograde flow in the contralateral proximal segment of theanterior cerebral artery and retrograde flow in the ipsilateralproximal segment of the anterior cerebral artery (Figure 1).Collateral flow from the vertebrobasilar system is providedby posterior-to-anterior flow in the posterior communicatingartery. The circle of Willis is considered balanced if all segmentsare patent and of low resistance. Unfortunately, this occursin only about 20 percent of subjects10. Therefore, the amountof protection in the form of collateral circulation providedby the circle of Willis varies. This variability may prove important,either to patients at risk for progression to internal-carotid-arteryocclusion or to candidates for the surgical removal of the internalcarotid artery.
When stenosis of the internal carotid artery progresses slowlyto occlusion, secondary collateral pathways may be recruited.Principal among these are leptomeningeal collateral flow fromthe posterior-cerebral-artery circulation and retrograde flowin the ophthalmic artery from the ipsilateral external carotidartery. Other collateral pathways may be created and may proveimportant in specific cases. For example, Takahashi et al.11.described a patient with occlusion of the internal carotid arterywhose dominant collateral pathway was from the posterior circulationby means of an enlarged anterior choroidal artery. Such pathways,however, are atypical and were not observed in our study.
Cerebral infarction represents a severe complication of internal-carotid-arteryocclusion. The availability of collateral flow affects the likelihoodof ischemic infarction in patients with internal-carotid-arteryocclusion12,13,14,15,16. Therefore, the correlation of specificcollateral pathways with cerebral infarction in these patientsmay provide data with clinical relevance for management, especiallyif the collateral pathways can be imaged noninvasively.
Source Information
From the Departments of Radiology (D.F.S., M.P.M., M.R.R., N.J.P., D.R.E.) and Neurosurgery (G.K.S.), Stanford University Medical Center, and the Department of Statistics, Stanford University (I.M.J., D.B.B.), Stanford, Calif.
Address reprint requests to Dr. Enzmann at the Department of Radiology, S072 Stanford University Medical Center, Stanford, CA 94305-5105.
References
Ross MR, Pelc NJ, Enzmann DR. Qualitative phase contrast MRA in the normal and abnormal circle of Willis. AJNR Am J Neuroradiol 1993;14:19-25. [Abstract]
Marks MP, Pelc NJ, Ross MR, Enzmann DR. Determination of cerebral blood flow with a phase-contrast cine MR imaging technique: evaluation of normal subjects and patients with arteriovenous malformations. Radiology 1992;182:467-476. [Free Full Text]
Baird AE, Donnan GA, Saling M. Mechanisms and clinical features of internal watershed infarction. Clin Exp Neurol 1991;28:50-55. [Medline]
SAS/STAT user's guide: version 6. 4th ed. Vol. 1. Cary, N.C.: SAS Institute, 1990.
Mehta CR, Patel NR. A network algorithm for performing Fisher's exact test in r x c contingency tables. J Am Stat Assoc 1983;78:427-34.
Steinberg GK, Drake CG, Peerless SJ. Deliberate basilar or vertebral artery occlusion in the treatment of intracranial aneurysms: immediate results and long-term outcome in 201 patients. J Neurosurg 1993;79:161-173. [Medline]
Perler BA, Burdick JF, Williams GM. Progression to total occlusion is an underrecognized complication of the medical management of carotid disease. J Vasc Surg 1991;14:821-826. [Medline]
Rautenberg W, Mess W, Hennerici M. Prognosis of asymptomatic carotid occlusion. J Neurol Sci 1990;98:213-220. [CrossRef][Medline]
Takahashi S, Tobita M, Takahashi A, Sakamoto K. Retrograde filling of the anterior choroidal artery: vertebral angiographic sign of obstruction in the carotid system. Neuroradiology 1992;34:504-507. [CrossRef][Medline]
Hedera P, Traubner P, Bujdakova J. Short-term prognosis of stroke due to occlusion of internal carotid artery based on transcranial Doppler ultrasonography. Stroke 1992;23:1069-1072. [Free Full Text]
Cavestri R, Radice L, Ferrarini F, et al. CBF side-to-side asymmetries in stenosis-occlusion of internal carotid artery: relevance of CT findings and collateral supply. Ital J Neurol Sci 1991;12:383-388. [Medline]
Schwartz RB, Jones KM, LeClercq GT, et al. The value of cerebral angiography in predicting cerebral ischemia during carotid endarterectomy. AJR Am J Roentgenol 1992;159:1057-1061. [Free Full Text]
Harrison MJ, Marshall J. The variable clinical and CT findings after carotid occlusion: the role of collateral blood supply. J Neurol Neurosurg Psychiatry 1988;51:269-272. [Abstract]
Heiserman JE, Drayer BP, Keller PJ, Fram EK. Intracranial vascular stenosis and occlusion: evaluation with three-dimensional time-of-flight MR angiography. Radiology 1992;185:667-673. [Free Full Text]
Hendrikse, J., Petersen, E. T., van Laar, P. J., Golay, X.
(2007). Cerebral Border Zones between Distal End Branches of Intracranial Arteries: MR Imaging. Radiology
0: 2461062100-
[Abstract][Full Text]
Proweller, A., Wright, A. C., Horng, D., Cheng, L., Lu, M. M., Lepore, J. J., Pear, W. S., Parmacek, M. S.
(2007). Notch signaling in vascular smooth muscle cells is required to pattern the cerebral vasculature. Proc. Natl. Acad. Sci. USA
104: 16275-16280
[Abstract][Full Text]
Papantchev, V., Hristov, S., Todorova, D., Naydenov, E., Paloff, A., Nikolov, D., Tschirkov, A., Ovtscharoff, W.
(2007). Some variations of the circle of Willis, important for cerebral protection in aortic surgery -- a study in Eastern Europeans. Eur. J. Cardiothorac. Surg.
31: 982-989
[Abstract][Full Text]
van Laar, P. J., Hendrikse, J., Klijn, C. J. M., Kappelle, L. J., van Osch, M. J. P., van der Grond, J.
(2007). Symptomatic Carotid Artery Occlusion: Flow Territories of Major Brain-Feeding Arteries. Radiology
242: 526-534
[Abstract][Full Text]
Tanaka, H., Fujita, N., Enoki, T., Matsumoto, K., Watanabe, Y., Murase, K., Nakamura, H.
(2006). Relationship between Variations in the Circle of Willis and Flow Rates in Internal Carotid and Basilar Arteries Determined by Means of Magnetic Resonance Imaging with Semiautomated Lumen Segmentation: Reference Data from 125 Healthy Volunteers.. Am. J. Neuroradiol.
27: 1770-1775
[Abstract][Full Text]
Kazui, T.
(2006). Editorial comment: Which is more appropriate as a cerebral protection method -- unilateral or bilateral perfusion?. Eur. J. Cardiothorac. Surg.
29: 1039-1040
[Full Text]
Jaramillo, A., Gongora-Rivera, F., Labreuche, J., Hauw, J. -J., Amarenco, P.
(2006). Predictors for malignant middle cerebral artery infarctions: A postmortem analysis. Neurology
66: 815-820
[Abstract][Full Text]
Schoder, M., Grabenwoger, M., Holzenbein, T., Cejna, M., Ehrlich, M. P., Rand, T., Stadler, A., Czerny, M., Domenig, C. M., Loewe, C., Lammer, J.
(2006). Endovascular repair of the thoracic aorta necessitating anchoring of the stent graft across the arch vessels. J. Thorac. Cardiovasc. Surg.
131: 380-387
[Abstract][Full Text]
Momjian-Mayor, I., Baron, J.-C.
(2005). The Pathophysiology of Watershed Infarction in Internal Carotid Artery Disease: Review of Cerebral Perfusion Studies. Stroke
36: 567-577
[Abstract][Full Text]
Kamouchi, M., Kishikawa, K., Okada, Y., Inoue, T., Ibayashi, S., Iida, M.
(2005). Poststenotic Flow and Intracranial Hemodynamics in Patients with Carotid Stenosis: Transoral Carotid Ultrasonography Study. Am. J. Neuroradiol.
26: 76-81
[Abstract][Full Text]
van der Grond, J., van Raamt, A. F., van der Graaf, Y., Mali, W. P.T.M., Bisschops, R. H.C.
(2004). A fetal circle of Willis is associated with a decreased deep white matter lesion load. Neurology
63: 1452-1456
[Abstract][Full Text]
Rutgers, D.R., Klijn, C.J.M., Kappelle, L.J., van der Grond, J.
(2004). Recurrent Stroke in Patients With Symptomatic Carotid Artery Occlusion Is Associated With High-Volume Flow to the Brain and Increased Collateral Circulation. Stroke
35: 1345-1349
[Abstract][Full Text]
Liu, Y., Karonen, J. O., Vanninen, R. L., Nuutinen, J., Koskela, A., Soimakallio, S., Aronen, H. J.
(2004). Acute Ischemic Stroke: Predictive Value of 2D Phase-Contrast MR Angiography--Serial Study with Combined Diffusion and Perfusion MR Imaging. Radiology
231: 517-527
[Abstract][Full Text]
Lee, J. H., Choi, C. G., Kim, D. K., Kim, G. E., Lee, H. K., Suh, D. C.
(2004). Relationship Between Circle of Willis Morphology on 3D Time-of-Flight MR Angiograms and Transient Ischemia During Vascular Clamping of the Internal Carotid Artery During Carotid Endarterectomy. Am. J. Neuroradiol.
25: 558-564
[Abstract][Full Text]
Akgul, A., Ozatik, M. A., Kucuker, S. A., Bahar, I., Tasdemir, O.
(2004). Repair of the aortic arch with left unilateral selective cerebral perfusion. Perfusion
19: 77-79
[Abstract]
Staessen, J. A., Wang, J.
(2003). Editorial Comment--Blood Pressure Lowering for the Secondary Prevention of Stroke: One Size Fits All?. Stroke
34: 2590-2592
[Full Text]
Liebeskind, D. S.
(2003). Collateral Circulation. Stroke
34: 2279-2284
[Abstract][Full Text]
Hendrikse, J., Rutgers, D. R., Klijn, C. J.M., Eikelboom, B. C., van der Grond, J.
(2003). Effect of Carotid Endarterectomy on Primary Collateral Blood Flow in Patients With Severe Carotid Artery Lesions. Stroke
34: 1650-1654
[Abstract][Full Text]
Bisschops, R. H.C., Klijn, C. J.M., Kappelle, L. J., van Huffelen, A. C., van der Grond, J.
(2003). Collateral flow and ischemic brain lesions in patients with unilateral carotid artery occlusion. Neurology
60: 1435-1441
[Abstract][Full Text]
Hoksbergen, A. W.J., Majoie, C. B.L., Hulsmans, F.-J. H., Legemate, D. A.
(2003). Assessment of the Collateral Function of the Circle of Willis: Three-Dimensional Time-of-Flight MR Angiography Compared with Transcranial Color-Coded Duplex Sonography. Am. J. Neuroradiol.
24: 456-462
[Abstract][Full Text]
Tasdemir, O., Saritas, A., Kucuker, S., Ozatik, M. A., Sener, E.
(2002). Aortic arch repair with right brachial artery perfusion. Ann. Thorac. Surg.
73: 1837-1842
[Abstract][Full Text]
Milhaud, D., de Freitas, G. R., van Melle, G., Bogousslavsky, J.
(2002). Occlusion Due to Carotid Artery Dissection: A More Severe Disease Than Previously Suggested. Arch Neurol
59: 557-561
[Abstract][Full Text]
Bisschops, R. H.C., Kappelle, L.J., Mali, W. P.T.M., van der Grond, J.
(2002). Hemodynamic and Metabolic Changes in Transient Ischemic Attack Patients: A Magnetic Resonance Angiography and 1H-Magnetic Resonance Spectroscopy Study Performed Within 3 Days of Onset of a Transient Ischemic Attack. Stroke
33: 110-115
[Abstract][Full Text]
Hendrikse, J., Hartkamp, M. J., Hillen, B., Mali, W. P.T.M., Grond, J. v. d.
(2001). Collateral Ability of the Circle of Willis in Patients With Unilateral Internal Carotid Artery Occlusion: Border Zone Infarcts and Clinical Symptoms. Stroke
32: 2768-2773
[Abstract][Full Text]
Vernieri, F., Pasqualetti, P., Matteis, M., Passarelli, F., Troisi, E., Rossini, P. M., Caltagirone, C., Silvestrini, M.
(2001). Effect of Collateral Blood Flow and Cerebral Vasomotor Reactivity on the Outcome of Carotid Artery Occlusion. Stroke
32: 1552-1558
[Abstract][Full Text]
Nasel, C., Azizi, A., Wilfort, A., Mallek, R., Schindler, E.
(2001). Measurement of Time-to-peak Parameter by Use of a New Standardization Method in Patients with Stenotic or Occlusive Disease of the Carotid Artery. Am. J. Neuroradiol.
22: 1056-1061
[Abstract][Full Text]
Marshall, R. S., Lazar, R. M., Pile-Spellman, J., Young, W. L., Duong, D. H., Joshi, S., Ostapkovich, N.
(2001). Recovery of brain function during induced cerebral hypoperfusion. Brain
124: 1208-1217
[Abstract][Full Text]
Tsiskaridze, A., Devuyst, G., de Freitas, G. R., van Melle, G., Bogousslavsky, J.
(2001). Stroke With Internal Carotid Artery Stenosis. Arch Neurol
58: 605-609
[Abstract][Full Text]
van Everdingen, K J, Kappelle, L J, Klijn, C J M, Mali, W P T M, van der Grond, J
(2001). Clinical features associated with internal carotid artery occlusion do not correlate with MRA cerebropetal flow measurements. J. Neurol. Neurosurg. Psychiatry
70: 333-339
[Abstract][Full Text]
Rutgers, D. R., Blankensteijn, J. D., van der Grond, J.
(2000). Preoperative MRA Flow Quantification in CEA Patients : Flow Differences Between Patients Who Develop Cerebral Ischemia and Patients Who Do Not Develop Cerebral Ischemia During Cross-Clamping of the Carotid Artery. Stroke
31: 3021-3028
[Abstract][Full Text]
Kim, J. S., Moon, D. H., Kim, G. E., Cho, Y. P., Kim, J. S., Ryu, J. S., Lee, H. K.
(2000). Acetazolamide Stress Brain-Perfusion SPECT Predicts the Need for Carotid Shunting During Carotid Endarterectomy. JNM
41: 1836-1841
[Abstract][Full Text]
Rutgers, D. R., Klijn, C. J. M., Kappelle, L. J., van Huffelen, A. C., van der Grond, J.
(2000). A Longitudinal Study of Collateral Flow Patterns in the Circle of Willis and the Ophthalmic Artery in Patients With a Symptomatic Internal Carotid Artery Occlusion. Stroke
31: 1913-1920
[Abstract][Full Text]
Hoksbergen, A. W. J., Legemate, D. A., Ubbink, D. T., Jacobs, M. J. H. M.
(2000). Collateral Variations in Circle of Willis in Atherosclerotic Population Assessed by Means of Transcranial Color-Coded Duplex Ultrasonography. Stroke
31: 1656-1660
[Abstract][Full Text]
Hoksbergen, A. W. J., Fulesdi, B., Legemate, D. A., Csiba, L.
(2000). Collateral Configuration of the Circle of Willis : Transcranial Color-Coded Duplex Ultrasonography and Comparison With Postmortem Anatomy. Stroke
31: 1346-1351
[Abstract][Full Text]
Henderson, R. D., Eliasziw, M., Fox, A. J., Rothwell, P. M., Barnett, H. J. M.
(2000). Angiographically Defined Collateral Circulation and Risk of Stroke in Patients With Severe Carotid Artery Stenosis. Stroke
31: 128-132
[Abstract][Full Text]
Hartkamp, M. J., van der Grond, J., van Everdingen, K. J., Hillen, B., Mali, W. P. T. M.
(1999). Circle of Willis Collateral Flow Investigated by Magnetic Resonance Angiography. Stroke
30: 2671-2678
[Abstract][Full Text]
Kluytmans, M., van der Grond, J., van Everdingen, K. J., Klijn, C. J. M., Kappelle, L. J., Viergever, M. A.
(1999). Cerebral Hemodynamics in Relation to Patterns of Collateral Flow. Stroke
30: 1432-1439
[Abstract][Full Text]
Derdeyn, C. P., Shaibani, A., Moran, C. J., Cross, D. T. III, Grubb, R. L. Jr, Powers, W. J.
(1999). Lack of Correlation Between Pattern of Collateralization and Misery Perfusion in Patients With Carotid Occlusion. Stroke
30: 1025-1032
[Abstract][Full Text]
Caplan, L. R., Hennerici, M.
(1998). Impaired Clearance of Emboli (Washout) Is an Important Link Between Hypoperfusion, Embolism, and Ischemic Stroke. Arch Neurol
55: 1475-1482
[Abstract][Full Text]
Kluytmans, M., van der Grond, J., Eikelboom, B. C., Viergever, M. A.
(1998). Long-Term Hemodynamic Effects of Carotid Endarterectomy. Stroke
29: 1567-1572
[Abstract][Full Text]
van Everdingen, K. J., Klijn, C. J. M., Kappelle, L. J., Mali, W. P. T. M., van der Grond, J.
(1997). MRA Flow Quantification in Patients With a Symptomatic Internal Carotid Artery Occlusion. Stroke
28: 1595-1600
[Abstract][Full Text]
Mull, M., Schwarz, M., Thron, A.
(1997). Cerebral Hemispheric Low-Flow Infarcts in Arterial Occlusive Disease: Lesion Patterns and Angiomorphological Conditions. Stroke
28: 118-123
[Abstract][Full Text]
van der Grond, J., Eikelboom, B.C., Mali, W.P.Th.M.
(1996). Flow-Related Anaerobic Metabolic Changes in Patients With Severe Stenosis of the Internal Carotid Artery. Stroke
27: 2026-2032
[Abstract][Full Text]
Klotzsch, C., Popescu, O., Berlit, P.
(1996). Assessment of the Posterior Communicating Artery by Transcranial Color-Coded Duplex Sonography. Stroke
27: 486-489
[Abstract][Full Text]
Mounier-Vehier, F., Leys, D., Pruvo, J. P.
(1995). Stroke Patterns in Unilateral Atherothrombotic Occlusion of the Internal Carotid Artery. Stroke
26: 422-425
[Abstract][Full Text]
Brown, W. D., Gilles, F. H., Nelson, M. D., Bowen, J.R.C., Schomer, D. F., Enzmann, D.R.
(1994). Posterior Communicating Artery and Ischemic Stroke. NEJM
331: 1020-1021
[Full Text]
1 mm in diameter) by magnetic resonance angiography were considered to have large posterior communicating arteries. This grouping of patients according to the size of the posterior communicating arteries was done separately from the analysis of the magnetic resonance images for infarcts to avoid any potential bias. 
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