| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Neuroradiology |
1 From the Neuroradiology Section (C.P.D., A.K.) and Division of Radiological Sciences (C.P.D., T.O.V., R.L.G., W.J.P.), Mallinckrodt Institute of Radiology; the Department of Neurology and Neurological Surgery (T.O.V., S.M.F., D.L.C., R.L.G., W.J.P.) and the Lillian Strauss Institute of the Jewish Hospital of St Louis (W.J.P.), Washington University School of Medicine, 510 S Kingshighway Blvd, St Louis, MO 63110. Received September 1, 2000; revision requested October 6; revision received November 3; accepted December 14. Supported by National Institutes of Health grants NS02029 and NS28947. Address correspondence to C.P.D. (e-mail: derdeync@mir.wustl.edu).
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
|---|
MATERIALS AND METHODS: At enrollment in a prospective study of cerebral hemodynamics, 110 patients with carotid occlusion underwent (a) positron emission tomography for the measurement of cerebral oxygen extraction fraction and (b) computed tomographic (CT) or magnetic resonance (MR) examinations of the brain. Infarcts were categorized retrospectively by vascular territory, location, and pattern. The association of these findings with hemodynamic impairment (increased oxygen extraction fraction) was investigated.
RESULTS: No border zone–region infarctions were found in 35 asymptomatic patients. In 75 symptomatic patients, cortical border zone–region infarction was found in seven of 36 patients with increased oxygen extraction fraction, and in two of 39 with normal oxygen extraction fraction (P = .08, difference not significant). The pattern of multiple white matter lesions arranged parallel to the lateral ventricle was observed only in symptomatic patients with increased oxygen extraction fraction (eight of 36 patients; P = .002; sensitivity, 22%; specificity, 100%). This finding was more frequent with MR imaging (seven of 14 patients) than with CT (one of 22 patients).
CONCLUSION: Multiple white matter infarctions, arranged parallel to the lateral ventricle, are associated with severe hemodynamic impairment. This pattern of infarction is likely due to a hemodynamic mechanism.
Index terms: Brain, blood flow • Brain, CT, 17.1211 • Brain, infarction, 17.78 • Brain, MR, 17.121411 • Brain, PET, 17.12163 • Brain, white matter, 13.78 • Carotid arteries, 17.4312, 90.411 • Cerebral blood vessels, MR, 17.12142, 17.12143
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
|---|
In addition to this cortical arterial border zone, some authors have suggested that a second arterial border zone is present within the white matter of the centrum semiovale and corona radiata (3,4). This has been called the internal arterial border zone (between lenticulostriate perforators and deep penetrating branches of the distal middle cerebral artery) (3). The evidence supporting the theory of an internal border zone is not as clear as the evidence supporting the idea of the cortical border zone, however.
While researchers in studies of acute hypotension have not reported isolated ischemic lesions in these locations (1,2), several investigators have reported an association between the presence of chronic hemodynamic impairment in a cerebral hemisphere distal to an occlusive arterial lesion and infarctions of the white matter in these regions (5–9). However, these studies have been retrospective in design (patients are often selected on the basis of imaging studies) or have included a small number of patients. Many have included patients with different degrees of arterial stenosis or occlusion in whom the relative importance of embolic and hemodynamic risk factors for stroke may vary. Finally, different methods of hemodynamic assessment have been used.
The purpose of the present study was to investigate the relationship between the patterns of cerebral infarction (possible cortical and internal border zone infarctions) that have been associated with hemodynamic impairment and the presence of severe chronic hemodynamic compromise (increased oxygen extraction fraction [OEF]) in a large prospectively enrolled group of patients with carotid artery occlusion.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
|---|
Background of the STLCOS
Patients.—The primary inclusion criterion was atherosclerotic occlusion of one or both common or internal carotid arteries demonstrated by contrast medium–enhanced angiography, MR angiography, or Doppler ultrasonography (US). Exclusion criteria included nonatherosclerotic conditions causing or likely to cause cerebral ischemia. All 123 patients (33 women, 90 men; mean age, 65 years; age range, 40–84 years) were interviewed and examined by a STLCOS physician-investigator (C.P.D., D.L.C., W.J.P.). Baseline stroke risk factors were assessed. Whether the occlusion was symptomatic or asymptomatic was determined from the interview and the neurologic examination findings. Pertinent medical records, CT or MR images, and angiograms were reviewed. A nonenhanced CT or MR examination of the brain was performed if a CT or MR image had not been obtained as part of usual clinical care sufficiently long after an ischemic event to permit accurate definition of infarct location. Findings of this examination were used to determine the site of tissue infarction to exclude these regions from subsequent PET analysis.
Control subjects.—Eighteen healthy control subjects (eight women, 10 men; mean age, 45 years ± 18 [SD]; age range, 19–77 years) were recruited for the STLCOS by means of public advertisement for the purposes of establishing a normal range of cerebral hemodynamic and metabolic values. All subjects underwent neurologic evaluation, MR imaging of the head, and duplex US of the extracranial carotid arteries. None had (a) signs or symptoms of neurologic disease other than mild distal sensory loss in the legs consistent with age, (b) pathologic lesions depicted on the MR image (mild atrophy was not considered pathologic), or (c) greater than 50% stenosis of the extracranial carotid arteries. All studies were performed according to protocols approved by our institution’s Human Studies Committee (institutional review board). Informed consent was obtained from all subjects.
PET measurements of OEF.—After the patient was positioned in the gantry of the scanner, an individually molded thermoplastic face mask was applied to ensure that the patient’s head remained in a constant position during scanning. The exact position of the patient’s head relative to the scanning plane was recorded on a lateral skull radiograph obtained after head immobilization. Venous and arterial catheters were placed for intravenous radiotracer administration and for arterial blood gas analyses and arterial time-activity curve determination. Catheters were placed by one of four investigators (C.P.D., S.M.F., D.L.C., or W.J.P.).
PET studies were performed with one of two scanners (ECAT 953B or ECAT EXACT HR; Siemens, Iselin, NJ). A transmission scan was obtained before radiotracer administration by using germanium 68 and gallium 68 rotating rod sources. The skull radiograph and attenuation data from this scan were used to define the limits of the calvaria for quantitative processing of PET data (12).
Each PET study consisted of three separate physiologic studies for the measurement of cerebral blood flow (CBF), cerebral blood volume, and OEF. During each study, arterial blood samples were collected to convert quantitative regional radioactivity data to quantitative physiologic measurements. Additional arterial samples were drawn at intervals during the examination for determination of PaCO2 stability, mean hematocrit level, arterial oxygen content calculations, and carboxyhemoglobin content.
CBF was measured by using an intravenous bolus injection of oxygen 15–labeled water (13). Cerebral blood volume was measured after inhalation of air containing trace amounts of carbon monoxide labeled with 15O (14). OEF was measured after inhalation of one or two breaths of 15O-labeled oxygen in combination with data from the cerebral blood volume and CBF measurements (15). When technical difficulties precluded the determination of quantitative OEF, a ratio image of the counts in the oxygen image divided by the counts in the water image and normalized to a whole-brain mean of 0.40 was substituted for the quantitative OEF image (16).
PET image data processing.—PET images were reconstructed to a uniform resolution of 16 mm full width half maximum by using a three-dimensional Gaussian filter. All PET data were converted to uniform stereotactic atlas space to allow reproducible placement of regions of interest. For each patient and healthy volunteer, seven spherical regions of interest 19 mm in diameter were placed in the cortical territory of the middle cerebral artery in each hemisphere by using stereotactic coordinates (12,17,18). Areas of prior infarction were identified by means of review (C.P.D., W.J.P.) of the cerebral metabolic rate for oxygen images, as well as by using CT or MR examination findings. Neither the regions of interest within these areas nor the corresponding contralateral regions were used for analysis.
The mean OEF in each cerebral hemisphere was calculated from the remaining regions. Hemodynamic stage for each individual patient was assigned by comparison of the ratios of mean left-to-right hemispheric OEF in each study patient with ratios from the 18 healthy control subjects. For each patient, the OEF ratio was considered abnormal if it was outside the range observed in the sample of healthy control subjects (10). Patients with count-based OEF ratios were categorized in a similar fashion, on the basis of comparison of findings with data from the healthy population (a normal range for the count-based ratio image of 15O-labeled oxygen and 15O-labeled water was also generated) (16).
Imaging studies.—Patients recruited for the STLCOS were required to have CT or MR imaging studies performed after the most recent ischemic symptom and prior to the measurement of OEF at enrollment. A physician-investigator (C.P.D., D.L.C., W.J.P.) prospectively examined these images for any evidence of infarction (ipsilateral or contralateral to the occlusion). Normal images from outside institutions were returned, generally with no copies made for study records. Abnormal images from outside institutions were generally copied, and the copies were kept with study records. Normal and abnormal sets of images from our institution were kept with study records.
Retrospective Analysis
In 110 of 123 patients, either CT or MR images (n = 84) were available for review, or images (n = 26) were prospectively interpreted as normal by a STLCOS investigator and returned to the outside institution. The study group was composed of these 110 examinations (84 retrospectively reviewed and 26 prospectively interpreted as having normal findings) for the current analysis. The interval between CT or MR imaging and the PET examination was recorded. Two radiologists (C.P.D., A.K.), blinded to the hemodynamic status of the patient and the side of carotid occlusion, independently reviewed all available imaging studies. Discordant results were resolved by consensus. A standardized worksheet was used for each study. At the time the retrospective review was performed, our institutional review board did not require its approval for such review.
Infarctions were identified as a discrete focal region of hypoattenuation (no size limit) on a CT image or as hyperintensity greater than 3 mm in diameter on a T2-weighted MR image. Infarct size was determined by using the scale on the MR image. Infarcts in the posterior fossa were not recorded. The location of the infarct was categorized as involving the cortex, white matter, or basal ganglia. The most superficial structure involved was used to categorize infarctions. For example, infarctions of the cortex and adjacent subcortical white matter were classified as cortical infarctions. The vascular territory for all infarctions involving the cortex was categorized as being definitely in the middle, anterior, or posterior cerebral artery or in the indeterminate region between them (possible border zone region), by using a template developed on the basis of the anatomic studies of van der Zwan et al (19).
White matter infarctions were classified as definitely in the middle cerebral artery territory or internal border zone, on the basis of studies of Zulch (3) and Wodarz (4). In these studies and in the present analysis, the internal border zone was considered to be in the white matter of the corona radiata and centrum semiovale. The rosary-like pattern of internal border zone infarction was defined as three or more lesions 3 mm or greater in diameter arranged in a linear fashion parallel to the lateral ventricle and located in the centrum semiovale or corona radiata. Confluent periventricular white matter hypoattenuation (at CT) or hyperintensity (at T2-weighted MR imaging) was also recorded.
Angiographic images were also reviewed at study entry by a physician-investigator (C.P.D., D.L.C., W.J.P.). Sources of collateral flow to the middle cerebral artery were recorded. To investigate the relationship between the rosary-like pattern and collateral pathways, available findings in patients with MR imaging and increased OEF were reviewed (C.P.D.) for the present study. The status of the ipsilateral (relative to the carotid occlusion) A1 segment of the anterior cerebral artery was recorded as unknown, absent, normal, small (compared with the contralateral A1 segment), or stenotic.
Data Analysis
Clinical data in symptomatic and asymptomatic patients were separately analyzed because of the difference in frequency of cerebral infarctions inherent in these two groups. Patients were further divided into two groups on the basis of the original PET measurements of OEF (normal or increased left-to-right hemispheric ratio of OEF compared with that of healthy control subjects). The frequency of infarct location, vascular territory, multiplicity, the rosary-like pattern, and confluent periventricular white matter disease was compared between groups.
The 
2 and Fisher exact tests were used to assess statistical significance (P < .05). A Bonferroni correction was applied to adjust for multiple comparisons.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
|---|
|
The imaging findings (at CT or MR imaging) in the symptomatic patients are summarized in Table 2. Forty-nine patients underwent CT imaging. Scans from 18 patients were interpreted as normal, and scans from 13 of 18 were not reviewed. Twenty-six patients underwent MR imaging. Of these, images in five were normal, and images in two of five were not reviewed.
|
White matter infarctions in possible internal border zone regions (excluding the rosary-like pattern) occurred with equal frequency in patients with increased OEF (four of 36 patients) and in those with normal OEF (five of 39 patients). The rosary-like pattern of white matter lesions arranged parallel to the body of the lateral ventricle was identified in eight patients (Figs 1, 2). All eight patients had increased OEF measured in the ipsilateral hemisphere. This relationship was statistically significant (P = .002). The sensitivity and specificity of this sign for increased OEF were 22% (eight of 36 patients) and 100% (39 of 39 patients), respectively. Lacunar infarctions were also more frequent in patients with increased OEF; however, the number of these patients was small (n = 4; P = .05; the difference was not significant). Patients with increased OEF tended to have more multiple infarctions (seven of 36 patients compared with three of 39; P = .13; the difference was not significant).
|
|
|
|
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
|---|
The presence of severe hemodynamic impairment in the present study was determined by measurements of cerebral OEF. When autoregulatory capacity is exceeded, blood flow decreases and OEF increases, maintaining normal oxygen metabolism and function (Fig 1b). Recent work has shown that increased OEF measured in the hemisphere distal to an occluded or stenotic carotid artery is a powerful and independent predictor of subsequent ischemic stroke (10,20).
It is safe to conclude from the findings of the present study and of prior work that most cortical infarctions occurring in possible arterial border zone regions in patients with carotid occlusion are not due to chronic hemodynamic impairment. We observed no significant difference in the frequency of infarctions in possible cortical arterial border zone regions in patients with and without increased OEF. Furthermore, the existence of chronic hemodynamic impairment that is worse in cortical border zone regions than in the central middle cerebral artery territory has not been conclusively demonstrated (21).
In the present study, the location of the cortical and adjacent subcortical border zone was liberally estimated from the maps generated by van der Zwan et al (19). Many atlases place the border zone between the middle and anterior cerebral arteries in the superior frontal sulcus, for example (22). However, in the recent study by van der Zwan et al (19), this location was valid in only 30 of 50 hemispheres. We considered any infarction occurring beyond the confines of the most minimal middle cerebral artery territory map to be a possible border zone–region infarction.
It is possible that some cortical border zone–region infarctions are due to severe reductions in perfusion pressure at the time of the occlusion and that the hemodynamic status of these patients improved between the time of infarction and the PET examination (hence, the lack of an association in the present data). CBF and OEF may improve with time in some patients with carotid occlusion, likely due to improved flow through existing collateral channels (23). The data from this large patient cohort in the present study indicate that this is not a frequent phenomenon; the incidence of possible cortical border zone–region infarctions (despite a liberal definition of the location of the border zone) in patients with symptomatic carotid occlusion was very low (nine of 75 patients). Furthermore, increased OEF was found in 36 of 75 patients, indicating that hemodynamic compensation does not invariably occur. Many of these infarctions may have been due to embolic phenomena. Embolic causes of cortical border zone–region infarction are well documented (24–28).
The association of the linear, or rosary-like, pattern of deep white matter infarction and hemodynamic impairment is consistent with prior studies. Waterston and co-workers (8) were the first, to our knowledge, to report this association. Nine patients with carotid occlusion had multiple small lesions in the centrum semiovale or corona radiata at CT. Four of the nine patients had impaired CBF responses to hypercapnia, suggesting preexisting autoregulatory vasodilation. Yamauchi and colleagues (6) studied 11 patients with symptomatic carotid occlusion by using MR and PET imaging. Multiple high-signal-intensity lesions in the centrum semiovale were found on T2-weighted MR images in five of 11 patients. Mean OEF was higher in the five patients with this finding. Weiller et al (5) examined 37 symptomatic patients with severe carotid disease by using CT and MR imaging. Seventeen patients were classified as having low-flow infarcts (subcortical lesions, solitary or multiple). These patients, as a group, had lower values of blood velocity changes with hypercapnia than the 12 patients with carotid occlusion and a territorial infarction. Isaka et al (9) examined 23 patients with symptomatic carotid disease by using MR imaging. The rosary-like pattern was found in 11 of 12 patients with abnormal CBF responses to acetazolamide. Finally, Krapf et al (7) reviewed the MR studies of 16 patients with carotid occlusion and reduced blood velocity responses to hypercapnia. Eight patients had typical rosary-like centrum semiovale lesions.
The data from these studies, as well as those from the present investigation, indicate that the finding of several white matter lesions arranged in a linear pattern in the centrum semiovale or corona radiata is a common finding in patients with chronic carotid occlusion and hemodynamic impairment. This pattern was more frequently found at MR imaging than at CT, likely due to the superior sensitivity of MR imaging in the depiction of white matter disease. Furthermore, this finding appears to be a specific indicator of hemodynamic compromise, rarely observed in the absence of hemodynamic impairment.
While a hemodynamic mechanism has clearly been implicated, the pathophysiologic factors responsible for this particular pattern of infarction are unclear. Moody and colleagues (29) have suggested that the nature of the arterial supply to the centrum semiovale and adjacent white matter may predispose these areas to a greater risk for ischemia, due to hemodynamic factors, than the overlying cortex. They performed detailed anatomic studies of these penetrating arteries and found little potential for collateral flow, as opposed to that for the arteries of the pial surface. However, researchers in the limited number of neuropathologic studies of acute systemic hypotension have consistently reported white matter injury only in conjunction with infarction of the overlying cortex (1). In addition, in a prior study of patients from the STLCOS, we found no evidence for a selective increase in OEF in normal-appearing white matter of the centrum semiovale in patients with carotid occlusion (30). This discordance is difficult to resolve.
One hypothesis that may reconcile these data is that collateral flow from the distal anterior or posterior cerebral arteries to the middle cerebral artery (pial collateral vessels) is required for the development of the selective white matter ischemia proposed by Moody and colleagues (29). Mull and colleagues (31) performed a detailed analysis of the cerebral angiograms in 30 patients with periventricular white matter infarctions. Eleven of 13 patients with unilateral severe occlusive disease of the carotid artery had some restriction of flow across the A1 segment of the anterior cerebral artery. In each of the 11 patients with A1 segment abnormalities, this was associated with pial collateral flow from the distal branches of the anterior cerebral artery to the middle cerebral artery territory.
Stenosis or hypoplasia of the A1 segment of the anterior cerebral artery on the side of the occluded carotid artery could, in the presence of a normal anterior communicating artery, result in a greater reduction in perfusion pressure of the middle cerebral artery relative to the ipsilateral anterior cerebral artery, provided that other sources of collateral flow to the middle cerebral artery (posterior communicating or the ophthalmic arteries) were inadequate (in terms of maintaining normal perfusion pressure in the middle cerebral artery). The relatively lower pressures in the middle cerebral artery system could lead to the development of pial collateral flow. In this scenario, the pressure in the penetrating arteries to the white matter in the periventricular regions, fed by the most distal branches of the middle cerebral artery that now fill retrograde from small pial collateral channels, may decrease to ischemic levels. This hypothesis would be consistent with the observations of Mull et al (31) but has yet to be proved. We reviewed the angiographic data for the patients in the present study, and they neither support nor discount this theory (Table 4).
The findings of the present study contradict one of our conclusions from a prior investigation of white matter hemodynamics involving many of these same patients (32). In that study, we carefully measured OEF in structurally normal white matter of the centrum semiovale and found no evidence for higher OEF values in the possible internal border zone compared with OEF values in the cortical and subcortical regions. From these data, we concluded that deep white matter infarctions were not due to chronic selective (worse in the white matter) hemodynamic impairment. This conclusion may still be valid. Selective white matter ischemia may be an acute phenomenon, occurring at the time of occlusion, that either improves or results in infarction during the time before the PET examination. In addition, however, we also argued that acute selective white matter ischemia was also an unlikely mechanism for infarction, given the lack of neuropathologic evidence for isolated white matter infarction with acute systemic hypotension. The present data indicate that this conclusion may have been in error.
In conclusion, the finding of multiple ischemic lesions in a linear pattern in the white matter of the centrum semiovale or corona radiata is strongly associated with severe hemodynamic impairment in patients with symptomatic carotid occlusion. This association implies a hemodynamic mechanism for this pattern of ischemic injury. Shift of the pial arterial border zone due to reductions of perfusion pressure affecting the middle cerebral artery greater than the anterior cerebral artery territory may lead to ischemia of the underlying white matter supplied by penetrating arterioles arising from the most distal middle cerebral artery branches.
|
FOOTNOTES |
|---|
Author contributions: Guarantor of integrity of entire study, C.P.D.; study concepts, C.P.D., W.J.P., A.K., R.L.G.; study design, W.J.P., A.K., C.P.D.; literature research, W.J.P., A.K., C.P.D.; clinical studies, S.M.F., D.L.C.; data acquisition, C.P.D., A.K., T.O.V., S.M.F., D.L.C., W.J.P.; data analysis/interpretation, C.P.D., A.K., W.J.P.; statistical analysis, C.P.D.; manuscript preparation, C.P.D., A.K., W.J.P.; manuscript definition of intellectual content and editing, R.L.G., C.P.D., A.K., W.J.P.; manuscript revision/review, R.L.G., W.J.P., D.L.C., T.O.V., C.P.D.; manuscript final version approval, all authors.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
|---|
This article has been cited by other articles:
|
|
 |
|
  J. Hendrikse, E. T. Petersen, P. J. van Laar, and X. Golay Cerebral Border Zones between Distal End Branches of Intracranial Arteries: MR Imaging Radiology, December 13, 2007; (2007) 2461062100. [Abstract] [Full Text]
|
|
|
|
 |
|
 W.S. Bartynski and J.F. Boardman Distinct Imaging Patterns and Lesion Distribution in Posterior Reversible Encephalopathy Syndrome AJNR Am. J. Neuroradiol., August 1, 2007; 28(7): 1320 - 1327. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. F. Floyd, P. N. Shah, C. C. Price, F. Harris, S. J. Ratcliffe, M. A. Acker, J. E. Bavaria, H. Rahmouni, B. Kuersten, S. Wiegers, et al. Clinically Silent Cerebral Ischemic Events After Cardiac Surgery: Their Incidence, Regional Vascular Occurrence, and Procedural Dependence Ann. Thorac. Surg., June 1, 2006; 81(6): 2160 - 2166. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. W. Yong, O. Y. Bang, P. H. Lee, and W. Y. Li Internal and Cortical Border-Zone Infarction: Clinical and Diffusion-Weighted Imaging Features Stroke, March 1, 2006; 37(3): 841 - 846. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Yamauchi, T. Kudoh, Y. Kishibe, J. Iwasaki, and S. Kagawa Selective Neuronal Damage and Borderzone Infarction in Carotid Artery Occlusive Disease: A 11C-Flumazenil PET Study J. Nucl. Med., December 1, 2005; 46(12): 1973 - 1979. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. Momjian-Mayor and J.-C. Baron The Pathophysiology of Watershed Infarction in Internal Carotid Artery Disease: Review of Cerebral Perfusion Studies Stroke, March 1, 2005; 36(3): 567 - 577. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Alchanatis, N. Deligiorgis, N. Zias, A. Amfilochiou, E. Gotsis, A. Karakatsani, and A. Papadimitriou Frontal brain lobe impairment in obstructive sleep apnoea: a proton MR spectroscopy study Eur. Respir. J., December 1, 2004; 24(6): 980 - 986. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. M. Provenzale, R. Jahan, T. P. Naidich, and A. J. Fox Assessment of the Patient with Hyperacute Stroke: Imaging and Therapy Radiology, November 1, 2003; 229(2): 347 - 359. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. H. Lee, O. Y. Bang, S. H. Oh, I. S. Joo, and K. Huh Subcortical White Matter Infarcts: Comparison of Superficial Perforating Artery and Internal Border-Zone Infarcts Using Diffusion-Weighted Magnetic Resonance Imaging Stroke, November 1, 2003; 34(11): 2630 - 2635. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. H. C. Bisschops, C. J. M. Klijn, L. J. Kappelle, A. C. van Huffelen, and J. van der Grond Prevalence and Volume of Internal Border Zone Lesions in Patients With Impaired Cerebral Carbon Dioxide Vasomotor Reactivity: A Follow-up Study Arch Neurol, September 1, 2003; 60(9): 1233 - 1236. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. G. Steen, T. Emudianughe, G. M. Hankins, L. W. Wynn, W. C. Wang, X. Xiong, and K. J. Helton Brain Imaging Findings in Pediatric Patients with Sickle Cell Disease Radiology, July 1, 2003; 228(1): 216 - 225. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. H.C. Bisschops, C. J.M. Klijn, L. J. Kappelle, A. C. van Huffelen, and J. van der Grond Collateral flow and ischemic brain lesions in patients with unilateral carotid artery occlusion Neurology, May 13, 2003; 60(9): 1435 - 1441. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Arakawa, K. Minematsu, T. Hirano, Y. Tanaka, Y. Hasegawa, K. Hayashida, and T. Yamaguchi Topographic Distribution of Misery Perfusion in Relation to Internal and Superficial Borderzones AJNR Am. J. Neuroradiol., March 1, 2003; 24(3): 427 - 435. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. H. C. Bisschops, C. J. M. Klijn, L. J. Kappelle, A. C. van Huffelen, and J. van der Grond Association Between Impaired Carbon Dioxide Reactivity and Ischemic Lesions in Arterial Border Zone Territories in Patients With Unilateral Internal Carotid Artery Occlusion Arch Neurol, February 1, 2003; 60(2): 229 - 233. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Hendrikse, M. J. Hartkamp, B. Hillen, W. P.T.M. Mali, and J. v. d. Grond Collateral Ability of the Circle of Willis in Patients With Unilateral Internal Carotid Artery Occlusion: Border Zone Infarcts and Clinical Symptoms Stroke, December 1, 2001; 32(12): 2768 - 2773. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| RADIOLOGY | RADIOGRAPHICS | RSNA JOURNALS ONLINE |
