(Stroke. 1996;27:1088-1093.)
© 1996 American Heart Association, Inc.
Articles |
Assessment of Regional Cerebral Blood Volume in Acute Human Stroke by Use of Single-Slice Dynamic Susceptibility Contrast-Enhanced Magnetic Resonance Imaging
From the Departments of Neurology (J.R., W.N., A.S., M.H.) and Radiology (F.G.), Klinikum Mannheim, University of Heidelberg, Germany.
Correspondence to Joachim Röther, MD, Stanford University School of Medicine, Lucas MRS Imaging Center, 1201 Welch Rd, Mail Code 5488, Stanford, CA 94305. E-mail joachim@s-word.stanford.edu.
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Abstract |
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 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
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Background and Purpose The purpose of this study was to evaluate the clinical usefulness of dynamic susceptibility contrast-enhanced MRI (DSC-MRI) in acute cerebral ischemia.
Methods During bolus injection of gadolinium-diethylenetriamine pentaacetic acid, a series of rapid T2*-weighted images was recorded from one slice. Concentration-time curves and images of regional cerebral blood volume (rCBV) were calculated from this data set. DSC-MRI, MR angiography, conventional spin-echo MRI (SE-MRI), and CT were performed in 11 patients within 6 hours after stroke onset and before thrombolytic or anticoagulant treatment was begun. A follow-up MRI examination was performed 24 to 48 hours after stroke onset.
Results In 7 of 11 patients (group 1) with territorial infarcts of the middle (n=6) or posterior cerebral artery (n=1), DSC-MRI showed reduced rCBV in the affected territory before conventional SE-MRI displayed ischemic lesions. DSC-MRI was helpful to differentiate severely ischemic tissue from peri-infarct parenchyma. Partial reperfusion (n=3), unchanged reduction of rCBV (n=2), and progressive reduction of rCBV (n=2) were observed in the follow-up study. Normal DSC-MRI findings were present in 4 of 11 patients (group 2) with lacunar infarcts.
Conclusions DSC-MRI accomplished the detection of the ischemic territory in the very early stage (<6 hours) before SE-MRI delivered unequivocal results. DSC-MRI might be helpful to discriminate completely ischemic tissue from potentially salvageable ischemic parenchyma at risk and may play an important role in stroke therapy and evaluation.
Key Words: cerebral blood volume • plasminogen activator, tissue-type • cerebral ischemia • magnetic resonance imaging
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Although MRI is highly sensitive for changes associated with ischemic stroke,1 detection of acute cerebral infarction in humans usually is impossible <6 to 12 hours postictus on conventional spin-echo images.2 This time interval is too long to influence acute stroke therapy, and there is a strong demand for an imaging modality that provides information about location and spatial extent of the ischemic lesion, severity of the perfusion disturbance, vessel pathology, and extent of the collateral blood supply, as well as the presumed stroke mechanism. As long as the assessment of these pathophysiological changes is not available within the first few hours after ictus, acute stroke therapy will continue to deal with a black hole.
Recent perfusion and diffusion MR imaging studies demonstrated their potential to discriminate complete from partial ischemia in animal models3 4 and in humans.5 In the present study, DSC-MRI was used as an easy-to-perform, add-on examination to routine SE-MRI that provides data about the relative rCBV and tissue perfusion within the early stage of ischemia.6 7 8 9 10 The purpose of the present study was to prospectively evaluate the potential of single-slice DSC-MRI in combination with SE-MRI and MRA in the management of acute stroke patients.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Subjects
Fifteen patients with acute stroke were studied within the first 6 hours after onset of symptoms. Fourteen patients presented with severe hemiparesis that was eventually accompanied by additional neurological deficits, while in 1 patient, acute hemianopia was the predominant clinical finding. Of the original 15 patients, 4 were eliminated because motion artifacts resulted in poor-quality MR images that were deemed uninterpretable. The remaining 11 patients (7 women, 4 men; mean age, 65.9 years; range, 53 to 79 years old) provided informed consent before entry into the study. The neurological deficit was evaluated according to the SSS (mean score, 29.8; range, 17 to 40) before the MR examination and again on day 2 and day 30. All patients had SSS scores <40 (except 1 with acute hemianopia). Stroke therapy was begun immediately after the end of the MR study and within 6 hours of stroke onset. An initial CT scan was performed before the first MR examination. The MR protocol was repeated 24 to 48 hours after the initial study.
Seven patients participated in the ECASS trial, and five of these patients received rTPA (Alteplase; Dr Karl Thomae GmbH, Biberach an der Riss, Germany) intravenously (1 mg/kg). Two patients received placebo and were treated with intravenous heparin after 24 hours as described below. The remaining four patients who were not part of the ECASS trial were treated with intravenous heparin therapy from the beginning and received an intravenous bolus of 5000 U and continued subsequent heparin infusion that was designed to duplicate the activated partial thromboplastin time.
MRI and MRA
MR examination was performed with a 1.5-T superconductive unit
(Magnetom 63 SP, Siemens Medical Systems). The study protocol began
with a sagittal T2-weighted gradient-echo sequence (2D
FLASH; TR, 400 ms; TE, 18 ms; flip angle, 15°) and was followed by a
conventional T2- and proton density–weighted
spin-echo sequence (TR, 2200 ms; TE, 20/80 ms). 3D
time-of-flight MRA was accomplished by use of a
first-order, flow-compensated, gradient-echo technique (3D
fast imaging with steady-state precession; TR, 30 ms; TE, 7 ms;
flip angle, 15°; 200-mm field of view; 192x256 matrix; slab
thickness, 64 mm; number of excitations, 1; 64 partitions). Velocity
compensation was performed in the readout and slice-selection
direction. One or two transverse acquisition slabs with a thickness of
64 mm were measured. A maximum intensity projection algorithm was
used for MRA image formation.
DSC-MRI
MRA was followed by DSC-MRI using a T2*-weighted
gradient-echo sequence (FLASH 2D images; TR, 27 ms; TE, 22 ms; flip
angle, 8°; 210-mm field of view; 64x256 matrix and half-Fourier
technique [39 phase-encoding steps and zero filling to 64 Fourier
lines]; acquisition time, 1 minute; effective time resolution, 1.1
seconds). Gd-DTPA (0.1 mmol/kg) was administered as a bolus via an
antecubital vein over a time period of 4 to 5 seconds. Before, during,
and after the intravenous bolus injection, a series of 50
sequential images was taken in a single slice to follow the bolus
passage of the contrast medium through the brain parenchyma. The signal
intensity changes during the first bolus passage were computed pixel by
pixel, which resulted in a signal intensity–time curve. We
calculated concentration-time curves assuming an exponential
relationship between the relative signal reduction and the local
contrast agent concentration. By application of tracer kinetic
principles, rCBV images of the measured slice were calculated on the
basis of a gamma variate fit (for more details, see Reference 1010 ). The
positioning of the slice in the ischemic region was guided by
the neurological symptoms and indirect stroke signs derived from the
SE-MRI (intravascular signal abnormalities) and MRA studies (signal
loss in intracranial arteries). For the follow-up measurement, the
same slice position was used.
The study ended with a gadolinium-enhanced T1-weighted spin-echo sequence (TR, 550 ms; TE, 14 ms). The total study time did not exceed 30 to 40 minutes.
Data Evaluation
CT and MR data were reviewed retrospectively by a neurologist
(J.R.) and two neuroradiologist/radiologists (A.S., F.G.). Evaluation
of the CT scans, SE-MRI, MRA, and DSC-MRI was performed in separate
reading sessions without patients' names and clinical information. The
reviewers compared the imaging data after separate evaluation and made
the diagnosis by consensus in case of disagreement. For the evaluation
of CT scans, previously described criteria, such as loss of the insular
ribbon11 and early subtle hypodensity,12 were
adopted.
MRI criteria for ischemic stroke were detection of signal intensity in T2- or proton density–weighted images and local cortical swelling. Particular attention was directed to the arterial, meningeal, and parenchymal enhancement in contrast-enhanced T1-weighted SE-MRI and to the presence of flow void signals in the intracranial arteries. Additionally, extracranial or intracranial artery occlusion or stenosis was evaluated according to signal loss in MRA.
For evaluation of the DSC-MRI findings, rCBV images and
concentration-time curves of ROIs in the major arterial
territories on both hemispheres were used. The rCBV images were judged
for the presence of reduced perfusion as indicated by black areas and
compared with the follow-up examination. In two patients with
infarction of the MCA territory, concentration-time curves of
multiple ROIs in the infarct core and the peri-infarct tissue were
evaluated. The peak height, peak width, and peak delay of the
concentration-time curves were compared with corresponding
contralateral areas. Care was taken not to include large vessels in ROI
measurements. Examples are depicted in Figs 1
and 2.
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) and in corresponding contralateral areas (
). ROI 1 shows
a complete signal loss during the contrast agent bolus passage in an
ROI within the black area of the rCBV images (pattern 1, no signal
intensity change during the bolus passage). Adjacent ROIs in the
temporal lobe (ROI 2) and in the posterior part of the MCA territory
(ROI 3) show a delayed bolus passage with a reduced peak and increased
width of the concentration-time curve (pattern 2).
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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The clinical, MRI, and CT findings are summarized in Tables 1
and 2.
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Imaging Data: Group 1 With Positive DSC-MRI Findings
Group 1 comprised seven patients with reduced rCBV in the
clinically suspected arterial territory in the initial
DSC-MRI study. Two patients presented an rCBV reduction in the
MCA territory (patients 1 and 6) and one patient in the posterior
cerebral artery territory (patient 7). The lenticulostriate territory
was affected in four patients (patients 2, 3, 4, and 5).
The concentration-time curves measured from multiple ROIs within
the areas of reduced rCBV did not show a signal change due to the bolus
passage. In two patients (patients 1 and 6) with reduced rCBV in the
complete MCA territory, the evaluation of multiple ROIs established
three different patterns: pattern 1, no variation in the signal
intensity during the bolus passage ("1" in Fig 1c
and "1"
in Fig 2c); pattern 2, delayed bolus passage with a reduced peak and
increased width of the concentration-time curve ("2" and
"3" in Fig 1c); and pattern 3, reduced peak of the
concentration-time curve without significant changes of the width
of the curve ("2" and "3" in Fig 2c).
The comparison of the rCBV images, the plots of the
concentration-time curves in different ROIs, and the conventional
SE-MRI in the initial study and the follow-up investigation in
patients 1 and 6 revealed the following correlations: regions that
showed pattern 1, with total loss of signal variation during the bolus
passage, did not recover and resulted in a complete ischemia in
the follow-up study, as demonstrated by hyperintense lesions on the
T2-weighted SE-MRI. Pattern 2, with a bolus delay, reduced
peak, and increased width of the concentration-time curve, was
found in areas adjacent to pattern 1. These areas did not show any
signal abnormalities in the follow-up SE-MRI but demonstrated
pattern 3 instead of pattern 2 in the DSC-MRI follow-up study, thus
indicating tissue recovery (Figs 1 and 2).
Two patients (patients 4 and 5) showed an increase of the perfusion deficit on rCBV images in the follow-up examination. Both patients had findings suggestive of internal carotid or MCA occlusion in MRA. Three patients demonstrated unchanged findings in the follow-up investigation. The infarct area in the follow-up SE-MRI mimicked the area of reduced rCBV in the initial rCBV image.
One patient presented with a discrete hyperintensity of the insula in T2- and proton-density–weighted SE-MRI (patient 6) and another had a hyperdense media sign on CT (patient 2) within the acute stage. AE in the initial contrast-enhanced T1-weighted SE-MRI was present in six patients (patients 1, 2, 4, 5, 6, and 7) and ME was present in one patient (patient 2). All patients with AE or ME demonstrated intravascular signal abnormalities in the carotid siphon (4 of 7 patients) and/or MRA findings that indicated intracranial artery obstruction (5 of 7). AE and ME persisted in the follow-up MRI study, and additional ME or parenchymal enhancement was found in three patients (patients 1, 4, and 5).
MRA demonstrated a partial recanalization in four patients (patients 4, 5, 6, and 7) and unchanged occlusion in one patient (patient 2). In one patient (patient 1), recanalization was evidenced by reconstitution of normal flow void signal in the carotid siphon on T1- and T2-weighted SE-MRI.
Imaging Data: Group 2 With Negative DSC-MRI Findings
Four patients did not show any initial abnormalities either
on DSC-MRI or on CT or SE-MRI studies. Follow-up examination
revealed lacunar brain-stem infarcts (n=2) or a small subcortical
infarct (n=2) on SE-MRI with consistently normal DSC-MRI. The
patient with a paramedian pontine brain-stem infarction (patient 8)
presented with a basilar artery stenosis on MRA.
Because of the small number of patients and the incongruity of the study group, a correlation between MRI findings and clinical results with the drug regimen was not attempted. The therapeutic regimen of the individual patients is listed in the tables.
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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The efficacy of thrombolytic therapy to reduce ischemic cell injury is greatest in the first hours after stroke onset.13 The safe and efficient use of thrombolytic agents, however, is limited, because standard neuroimaging procedures such as CT scans and SE-MRI fail to reliably detect stroke within the first day after onset of symptoms.2
DSC-MRI has the potential to deliver information about perfusion deficits within the acute stage of stroke.5 8 9 10 When DSC-MRI is combined with SE-MRI and MRA, important information about the location and extent of the ischemia can be acquired within a single MRI study that otherwise could be obtained only by the combination of lengthy, costly, and often invasive procedures such as angiography, positron emission tomography, or single photon emission computed tomography.
To the best of our knowledge, this is the first study to use DSC-MRI to monitor tissue perfusion before and after acute thrombolytic or anticoagulant therapy. The extent and localization of the acute infarct area was characterized in 7 of 11 patients (group 1) before the infarcted tissue was unequivocally delineated by SE-MRI. Pretreatment DSC-MRI displayed reduced rCBV in well-defined arterial territories, whereas follow-up measurements after treatment provided information about partial reperfusion (decreased areas of rCBV deficit; n=3), progressive worsening (increased areas of rCBV deficit; n=2), or unchanged perfusion deficits (n=2). Patients without obvious rCBV changes in major intracerebral vascular territories (group 2) displayed lacunar infarcts in the follow-up examination.
The disappointing result of the ECASS trial has emphasized the strong demand for a noninvasive imaging modality that delivers early information on the extent of the perfusion deficit.14 The combination of DSC-MRI with MRA and SE-MRI characterizes the acute infarct within the therapeutic window and has the potential to improve early patient selection and guide stroke therapy, because patients with reduced rCBV in an arterial territory and with vessel obstruction in MRA can be discriminated from patients without major perfusion disturbances in the suspected territory. While the first group of patients may be considered candidates for thrombolytic therapy, it seems reasonable to assume that the latter group will not benefit from thrombolysis and therefore high-risk interventions can be avoided.
The different patterns of the relative concentration-time curves found in two patients with large perfusion deficits are in agreement with recently published experimental4 and human5 stroke data. We observed a complete loss of the bolus passage as a pattern that indicated severe ischemia (pattern 1). The ROIs with this pattern developed permanent infarction as shown by the SE-MRI follow-up study, and we conclude that this pattern might be predictive for the infarct core. A delayed bolus passage, reduced peak, and increased width of the concentration-time curve were found in the adjacent parenchyma (pattern 2). The bolus delay is caused by an increased transit time for the contrast bolus that is, for instance, due to a proximal artery stenosis or artery occlusion with collateral filling. The reduced area under the concentration-time curve correlates with the reduced rCBV of the ischemic injured tissue, whereas the increased width of the curve correlates with the prolonged contrast-agent transit time through the affected parenchyma and reflects a reduced tissue perfusion.
Tissue that exemplifies pattern 2 is thought to represent
potentially salvageable tissue, especially since the follow-up
study after treatment showed a normal signal in T2-weighted
SE-MRI (Fig 2). DSC-MRI follow-up studies of the areas with pattern
2 demonstrated a third pattern (pattern 3) that was not present in
the acute stage of infarction in these two patients. Pattern 3
characteristically showed a slightly reduced peak and a minimal bolus
delay without increased width of the concentration-time curve. This
pattern seems to indicate a discrete residual perfusion
disturbance around the infarct core with a slightly increased
vascular transit time and a minimal decrease of rCBV. It seems likely
that a gradual transition between these three patterns exists that
depends on the severity of the ischemia and the quality of
collateral blood flow. Previously described results in patients with
hemodynamically severe extracranial or intracranial
artery stenosis show that these patterns probably relate to the
severity of proximal stenosis and the efficacy of collateral
pathways.5 8 9 10
The present study was performed on a conventional MR scanner and was limited to a single-slice technique. This must be considered a drawback, because clinical symptoms do not reliably predict infarct location and the ischemic area might be missed because of incorrect slice positioning. However, the combination of clinical topodiagnosis with MRA and indirect early stroke signs such as intravascular signal abnormalities from SE-MRI are helpful in choosing the imaging slice. In the future, use of an MR scanner with an echo planar imaging option will permit the use of multiple slices during a single contrast bolus injection5 and improve the conspicuity of the technique for small ischemic lesions in unexpected locations in the brain. Recent technical modifications15 allow a quantification of rCBV and might expand the clinical value of DSC-MRI.
MRA proved to be a valuable tool to detect intracranial artery pathology16 17 18 and to support the differentiation between territorial, lacunar, or small subcortical infarcts.19 In the present study, all patients with territorial reduction of rCBV displayed severe vessel obstruction in MRA, whereas patients with negative DSC-MRI findings had normal MRA or showed findings such as a basilar artery stenosis that directed attention to an unexpected infarct location.
The earliest stroke changes that can be detected on SE-MRI are loss of flow void signals in case of major vessel occlusion. Hyperintense intravascular signals in SE-MRI were found in 5 of 11 patients in the distal internal carotid artery or the MCA, which confirmed MRA findings and occasionally specified the vessel pathology.
AE in contrast-enhanced T1-weighted SE sequences has been detected within the first 1 to 3 days after infarction and has been shown to be related to arterial slow flow and vasodilatation.2 20 21 22 In the present study, AE was present in six of seven patients in group 1 and one of four patients in group 2 within the first 6 hours. The presence of AE obviously depends on the extent of the infarcted area,20 and only one patient (patient 3) with reduced rCBV in the territory of the lenticulostriate arteries and with a small lenticulostriate infarct in the follow-up SE-MRI study did not display AE. Time evolution of ME was reported 1 to 3 days postictus, and parenchymal enhancement was reported 2 to 3 days postictus.20 We found ME as early as 6 hours postictus in one patient with a complete MCA infarct, and parenchymal enhancement developed after 48 hours in another patient. These results in a small number of acute patients demonstrate that the MRI features of acute infarction are still poorly characterized and that the variation of characteristics over time seems to be widespread.
Although discrete signs of cerebral ischemia in CT have been described within the first 6 hours after stroke onset,12 23 we did not find CT helpful to reliably determine the localization and extent of the infarct. This may be because CT was performed before MR examination, as early as 3 hours after stroke onset in 3 patients. SE-MRI did not prove to be more useful than CT in early infarct detection: only 2 of 11 patients showed a discrete hyperintensity in SE-MRI. In summary, CT and SE-MRI did not serve as reliable tools to characterize cerebral infarction in the very acute stage. In particular, they did not contribute to the discrimination between territorial and lacunar infarcts, a differentiation that might be of future importance for the safety of thrombolytic treatment.14
On the basis of our experience in very acute stroke patients, we conclude that the combination of DSC-MRI with SE-MRI and MRA serves as a valuable tool for early stroke characterization, stroke monitoring, and evaluation of stroke therapy. The combination of DSC-MRI and diffusion-weighted MRI might improve our understanding of acute ischemic injury and help to further establish typical stroke patterns that predict potentially salvageable ischemic tissue. The future prospects of acute stroke therapy could include treatment of stroke patients in the MR scanner and monitoring of the effect of thrombolytic and/or cytoprotective drugs on tissue perfusion and diffusion by means of ultrafast MR sequences.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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We thank Susan K. Lemieux, PhD, for helpful discussion and rereading of the English text.
Received October 17, 1995; revision received January 9, 1996; accepted February 26, 1996.
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References |
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 J. Rother, L. Jonetz-Mentzel, A. Fiala, J. R. Reichenbach, M. Herzau, W. A. Kaiser, and C. Weiller Hemodynamic Assessment of Acute Stroke Using Dynamic Single-Slice Computed Tomographic Perfusion Imaging Arch Neurol, August 1, 2000; 57(8): 1161 - 1166. [Abstract] [Full Text] [PDF]
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 J. Ye, G. Dai, L. N. Ryner, P. Kozlowski, L. Yang, R. Summers, J. Sun, T. A. Salerno, R. L. Somorjai, and R. Deslauriers Unilateral Antegrade Cerebral Perfusion Through the Right Axillary Artery Provides Uniform Flow Distribution to Both Hemispheres of the Brain : A Magnetic Resonance and Histopathological Study in Pigs Circulation, November 9, 1999; 100 (2009): II-309 - II-315. [Abstract] [Full Text] [PDF]
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J. R. Reichenbach, J. Röther, L. Jonetz-Mentzel, M. Herzau, A. Fiala, C. Weiller, and W. A. Kaiser Acute Stroke Evaluated by Time-to-Peak Mapping during Initial and Early Follow-up Perfusion CT Studies AJNR Am. J. Neuroradiol., November 1, 1999; 20(10): 1842 - 1850. [Abstract] [Full Text]
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 J. L. Sunshine, R. W. Tarr, C. F. Lanzieri, D. M. D. Landis, W. R. Selman, and J. S. Lewin Hyperacute Stroke: Ultrafast MR Imaging to Triage Patients prior to Therapy Radiology, August 1, 1999; 212(2): 325 - 332. [Abstract] [Full Text]
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T. Ueda, W. T. C. Yuh, J. E. Maley, J. P. Quets, P. Y. Hahn, and V. A. Magnotta Outcome of Acute Ischemic Lesions Evaluated by Diffusion and Perfusion MR Imaging AJNR Am. J. Neuroradiol., June 1, 1999; 20(6): 983 - 989. [Abstract] [Full Text]
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J. H. Kim, T. Shin, J. H. Park, S. H. Chung, N.-C. Choi, and B. H. Lim Various Patterns of Perfusion-Weighted MR Imaging and MR Angiographic Findings in Hyperacute Ischemic Stroke AJNR Am. J. Neuroradiol., April 1, 1999; 20(4): 613 - 620. [Abstract] [Full Text]
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J. Hatazawa, E. Shimosegawa, H. Toyoshima, B. A. Ardekani, A. Suzuki, T. Okudera, and Y. Miura Cerebral Blood Volume in Acute Brain Infarction : A Combined Study With Dynamic Susceptibility Contrast MRI and 99mTc-HMPAO-SPECT Stroke, April 1, 1999; 30(4): 800 - 806. [Abstract] [Full Text] [PDF]
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 P. A. Barber, S. M. Davis, D. G. Darby, P. M. Desmond, R. P. Gerraty, Q. Yang, D. Jolley, G. A. Donnan, and B. M. Tress Absent middle cerebral artery flow predicts the presence and evolution of the ischemic penumbra Neurology, April 1, 1999; 52(6): 1125 - 1125. [Abstract] [Full Text] [PDF]
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