(Stroke. 1996;27:474-479.)
© 1996 American Heart Association, Inc.
Articles |
Hemodynamic Parameter Assessment With Dynamic Susceptibility Contrast Magnetic Resonance Imaging in Unilateral Symptomatic Internal Carotid Artery Occlusion
From the Department of Neurology, Cerebrovascular Disease and Ataxia Research Center (N.N., P.T.), and the Departments of Radiology (Y.B., J.C.F.) and Nuclear Medicine (B.P.), Neurological Hospital, and the Laboratoire d'Informatique Médicale, UFR Alexis Carrel (P.A.), Lyon, France.
Correspondence to Dr N. Nighoghossian, Service de Neurologie du Pr Paul Trouillas (Urgences Neurovasculaires et Centre de Recherches sur l'Ataxie), Hôpital Neurologique, 59 Bd Pinel, Lyon 69003, France.
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Abstract |
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 Top Abstract IntroductionSubjects and Methods Results Discussion References |
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Background and Purpose Hemodynamic parameters such as regional cerebral blood volume (rCBV), mean transit time (MTT), and regional cerebral blood flow (rCBF) can be assessed by dynamic susceptibility contrast MRI. The aim of the present study was to apply this method in patients who had symptomatic unilateral internal carotid artery occlusion.
Methods Relative hemodynamic parameters (rCBV, MTT, and rCBF) were evaluated on the occluded side and thus compared with contralateral hemispheric values. We also attempted to detect any relationship between collateral flow and the hemodynamic parameters.
Results Although rCBV was clearly increased in five patients over the whole hemisphere, we did not observe a statistically significant difference regarding the whole sample between sides (mean rCBV, 14.1±4.58 on the occluded side versus 11.8±2.99 on the contralateral side; P>.10). MTT was clearly increased on the occluded side (mean MTT, 4.29±0.83 on the lesion side versus 3.14±0.81 on the contralateral side; P<.010). A statistically significant decrease of rCBF on the occluded side was observed (mean rCBF, 3.27±0.73 versus 3.93±1.03 on the contralateral side; P<.01).
Conclusions A significant hemodynamic compromise in patients who had unilateral symptomatic carotid occlusion was observed according to CBF and MTT values. This approach might be promising in the understanding of cerebral hemodynamics in patients with vascular disorders.
Key Words: carotid artery occlusion • hemodynamics • magnetic resonance imaging
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Introduction |
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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The importance of hemodynamic factors in the pathogenesis of focal cerebral ischemia remains unclear. According to cerebral circulation rules, CBV and the CBV/CBF ratio increase when CPP drops.1 This phenomenon is known as autoregulation and is mediated through changes in cerebrovascular resistance. This ratio is mathematically equivalent to the MTT of red blood cells through the cerebral vessels. Until now, these parameters were determined with PET.2 3 However, this method cannot be applied routinely to stroke patients because it is expensive and not commonly available. Dynamic susceptibility contrast material–enhanced gradient-echo MRI techniques might be an attractive tool that combines the good spatial resolution of MRI with an ability to assess tissue microcirculation that is comparable to that of PET, and this method requires no exposure to ionizing radiation. The basic principles were described in the pioneering works of other groups.4 5 6 The assessment of cerebral hemodynamics is supported by the study of signal-intensity changes after the first pass of a paramagnetic contrast medium. While passing through the capillary network, a short bolus of contrast material produces local magnetic fields in homogeneities that lead to a reduction in the transverse relation time T2* of the bulk tissue. This susceptibility effect can be recorded by a series of rapid T2*-weighted gradient-echo images. The resulting signal-intensity time curves can be converted into concentration-time curves. By using the indicator dilution theory,7 one can determine two important dynamic parameters, CBV and MTT, and thus calculate CBF as CBV/MTT.
Although this method is well established and has been extensively examined,8 9 most results have been obtained in animal studies, and there is only preliminary experience with patients.10 11 12 Cerebral hemodynamic parameters have been assessed with this technique in patients with ICA occlusion and ipsilateral infarction.12 However, the indicator dilution theory for nondiffusible tracers is not suitable for tissue with ruptured blood-brain barrier. Accordingly, our aim was to assess the relative values of hemodynamic parameters such as MTT, rCBV, and rCBF with dynamic susceptibility contrast-enhanced MRI in patients with unilateral ICA occlusion without significant ipsilateral border-zone or territorial infarcts.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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From November 1994 through June 1995, we prospectively studied 12 patients (12 men aged 59 to 80 years; mean±SD, 68±6.5 years) who were referred to our stroke unit and in whom documented occlusion of the ICA was found. Patients had experienced either transient ischemic attacks (n=5) or reversible ischemic neurological disorder (n=7). CT scan of the head was performed at a mean of 2 days (range, 6 hours to 4 days) after the last ischemic event. Patients who had a history of stroke or cerebral evidence of recent or old border-zone or territorial infarcts were excluded, as were those who had symptoms from the contralateral cerebral hemisphere or the brain stem. No patient had conditions that suggested a hemodynamic mechanism such as hypotension, positional changes, or exertion. Electrocardiography and transthoracic echocardiography ruled out any cardioembolic cause of cerebral ischemia. Occlusion was assessed using pulsed Doppler ultrasound and conventional angiography. Collateral flow through either the anterior or posterior communicating arteries or through the ophthalmic artery was studied in each case.
MR Imaging
MR imaging was carried out 6 to 9 weeks (median, 7
weeks) after
angiography with a superconductive unit operating at 1.5 T (Siemens AG,
Medical Group) with a standard circular head coil.
T2-weighted MR images (turbo spin-echo) in the axial
plane were obtained with a 7-mm section thickness, 25-cm field of view,
and 192x256 acquisition matrix, with repetition time of 6000
milliseconds and echo time of 90 milliseconds with one acquisition.
A FLASH sequence was used to produce susceptibility-weighted (T2*-weighted) MR images during an intravenous bolus injection of gadopentetate dimeglumine (Magnevist, Schering). The imaging parameters were as follows: 40/26; flip angle, 10°; one acquisition, 7-mm section thickness, 25-cm field of view, and 64x128 acquisition matrix. The acquisition time of each image was 3.8 seconds.
The contrast agent gadopentetate dimeglumine (0.1 mmol/kg) was manually injected as a compact bolus through a 16-gauge antecubital intravenous catheter in less than 2 seconds; then a 20-mL saline flush was administered.
Study Protocol
Before injection of gadopentetate dimeglumine,
all subjects
underwent conventional MRI in the axial plane to exclude patients who
had ipsilateral border-zone or territorial infarcts misdiagnosed on
CT scan. Patients who had no significant ischemic changes
underwent dynamic susceptibility contrast-enhanced
gradient-echo imaging. Twenty-five images were acquired at the
same anatomic level (above the ventricles to minimize vascularization
from the vertebrobasilar system), and the contrast-agent bolus was
administered after acquisition of the fifth FLASH image. Dynamic
susceptibility contrast-enhanced gradient-echo imaging was also
performed in volunteers who were comparable in terms of mean age and
type of cerebrovascular risk factors and who had no evidence of carotid
artery lesion on neck ultrasound or ischemic lesion on head CT
scan. Informed consent was obtained from patients and control
subjects.
MR Image Analysis
Global signal intensities were measured
across the entire brain
section and the right and left cerebral hemispheres. Regional signal
intensities were also measured for ROIs of 15 pixels displayed (Fig
1
) within the gray (premotor frontal cortex and primary
sensory areas of parietal cortex) and the white matter (centrum
semiovale).
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The ROI boundaries were selected on the basis of the images obtained before injection of contrast agent and were repeated in the same location on all subsequent images.
The changes in T2*
were expressed as a change in degree of
relaxation (
R2*, where
R2*=l/T2*) and calculated as
R2*(t)={[-ln(SI[t]/SIpre)]/TE},
where ln is the natural logarithm, SIpre is the signal
intensity before injection of contrast agent, and SI(t) is
the signal intensity at time t after injection of the
contrast agent.
Concentration-time curves
(C(t) versus
t) were generated by plotting R2* as a
function of time, since R2*(t)=k
C(t), where
C(t) is the concentration of contrast agent in the tissue at
time t and k is a tissue-specific constant.
Thus, rCBVs were estimated by numerical integration (from the area
under the curve, 
C(t)
dt). The numerical integration method using trapezoidal integration of
the baseline corrected the R2* curve. Baseline
correction was performed by subtracting the linear interpolation of the
MR signal baseline between the end points of the R2*
peak. MTTs were calculated from the first moment of the peak in the
R2* curves. The numerator for the first moment of the
R2* peak was calculated by summing the product of
the mean time and the baseline-corrected
C(t) dt value for each
pair of images to form t
C(t) dt. The first
moment of the peak in the R2* curve is the ratio of
t C(t) dt
to the area under the peak:
MTT=C(t)
dt/C(t) dt. The
inverse of the MTT is as follows:
C(t)
dt/t C(t)
dt. The flow component for this equation is represented by
a factor estimating the rCBF, calculated as follows:
rCBF=1/(t
C(t) dt). rCBV values,
expressed in arbitrary units, were derived from numerical integration
of the concentration-time curve. MTT values were calculated from
the first moment of the concentration-time curve. rCBF values,
expressed in arbitrary units, were calculated from the inverse of the
numerator for the first moment of the concentration-time curve.
Dynamic sequences of scans after an intravenous bolus of
gadolinium-DTPA are depicted in Fig 2.
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Statistical Analysis
The results are presented as
mean±SD. The significance
of the differences regarding MTT, rCBV, and rCBF between the occluded
and contralateral sides in patients and between the right and left
hemispheres in healthy volunteers was assessed with a two-tailed
t test. Computations were performed with the SPSS
statistical software package.
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Results |
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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Conventional T2-weighted images showed border-zone or territorial infarcts in 2 patients; dynamic susceptibility contrast-enhanced gradient-echo imaging was performed in 10 patients and 5 volunteers. In control subjects, the cerebral hemispheric ratio, as well as the right to left hemispheric ratios, for both gray and white matter for the three parameters (CBV, MTT, and CBF) ranged between 1 and 1.1. The gray to white matter ratio for CBV was 2.63±0.2 for the right hemisphere versus 2.48±0.26 for the left. The gray to white matter ratio for MTT was 1.01±0.02 for the right hemisphere versus 1.07±0.01 for the left. The gray to white matter ratio for rCBF was 3.09±0.40 in the right hemisphere versus 3.2±0.50 in the left. Relative cerebral hemodynamic parameters in normal subjects over the whole hemisphere and then according to frontal gray and white matter ROIs are listed in Table 1
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Hemodynamic parameter evaluation in patients was first performed over the whole hemisphere and then according to ROIs. Although CBV was clearly increased in five patients (patients 2, 4, 6, 7, and 10), we did not observe a statistically significant difference between hemispheres (mean rCBV, 14.1±4.58 on the occluded side versus 11.8±2.99 on the contralateral side; P>.10). MTT was clearly increased on the occluded side (mean MTT, 4.29±0.23 occluded versus 3.14±0.81 contralateral; P<.01). A statistically significant decrease of CBF was observed on the occluded side (mean rCBF, 3.27±0.73 occluded versus 3.93±1.03 contralateral; P<.01). Angiographic study depicted a retrograde filling through the ophthalmic artery in six patients (patients 2, 4, 5, 6, 8, and 10); four of them had an increase in rCBV on the occluded side.
Clinical and angiographic data and global hemispheric relative
hemodynamic parameters are listed in Table 2.
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The same changes for CBF and MTT were observed according to the ROIs
within the gray and white matter. The mean values of
hemodynamic parameters in patients
according to ROI are listed in Table 3. Fig 3
shows the decrease of signal intensities measured over
the entire right and left hemispheres in patient 1, who had a right
carotid artery occlusion, during transit of gadopentetate dimeglumine
(FLASH, 40/26; flip angle, 10°). The peak of the curve over the right
hemisphere occurs later and thus indicates a delayed bolus transit,
which suggests a hemodynamic compromise in this
patient.
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Discussion |
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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During the past decade, technological advances have helped to assess the influence of cerebral hemodynamics on stroke risk in patients with cerebrovascular disease. Hemodynamic parameters are currently monitored by transcranial Doppler ultrasonography,13 dynamic or xenon CT,14 15 single-photon emission CT,16 17 and PET.2 3 18 19 Recently, dynamic susceptibility contrast-enhanced imaging techniques have achieved improved temporal and spatial resolution compared with other functional imaging methods. However, the application of the indicator theory for nondiffusible tracers is suitable only for tissue with an intact blood-brain barrier, since the relationship between rCBF and rCBV is lost in the first few weeks after cerebral infarction.20 21 Therefore, we selected patients without border-zone or territorial infarcts for a more reliable evaluation of hemodynamic parameters.
Our results demonstrate significant global changes for MTT and CBF on the occluded side. According to current knowledge, patients who have arterial occlusive disease are protected against ischemic episodes to a certain point by compensatory mechanisms that help to prevent ischemia when CPP drops. This condition, studied by PET with 15O-labeled tracers in patients with carotid artery disease,2 3 is indicated by regional vasodilatation manifesting itself as a focal increase in CBV in the supply territory of the occluded artery. Since a critical CBV distinguishing occluded from patent arterial territories could not be defined, the ratio of CBV to CBF was used as an indicator of local CPP. This quantity represents the local vascular MTT.22 The highest ratios are usually expected in patients who have a mainly hemodynamic component to their ischemia, in whom maximal vasodilatation and low regional CPP might be observed. Moreover, the rCBV/rCBF ratio is believed to be a more sensitive index of reduced regional CPP than rCBV alone, since increased ratios may occur when rCBV is within the upper range of the normal value.1 23 Our results support this view, since MTT was significantly increased on the occluded side, whereas global rCBV values were not statistically different between sides.
Using PET, Hirano et al24 have shown that reduced acetazolamide reactivity was more likely related to stage II of hemodynamic failure.1 At this stage, a significant decrease of CPP and CBF and an increase in oxygen extraction fraction are associated with a subsequent prolonged MTT. The significant increase of MTT in the occluded side in our study might also suggest an impairment of perfusion reserve, since the CBV/CBF ratio is an index of the perfusion reserve of the cerebral circulation.25 Although the lack of hemodynamic factors accounting for symptoms suggests that convincing signs of carotid distribution "insufficiency" are rare,13 26 patients with impaired perfusion reserve may be more likely to have stagnant flow close to the carotid lesion, which would increase their risk of artery-to-artery thromboembolism.1 There is also evidence suggesting that areas of brain tissue with marginal perfusion may be more susceptible to the effect of microemboli.27 We have also attempted to detect any relationship between collateral flow and hemodynamic parameters. In six patients, a retrograde filling through the ophthalmic artery was observed; four patients in this group had an increased CBV value on the lesion side. CBF,28 PET,2 and Doppler29 analyses are consistent with the view that the ophthalmic artery is functional only when Willisian collaterals are absent or inefficient.
Our study might be in accordance with these data, since the increased CBV observed in these patients might mean a maximal development of Willisian collaterals.
This dynamic technique also has several faults. Only a single section can be obtained, and the relatively low temporal resolution bound to our hardware may raise concerns about the accuracy of the hemodynamic parameters (MTT, rCBV, and rCBF). Partial sampling of K space can also be used to further reduce the acquisition time, thereby improving accuracy. Increases in temporal resolution could be achieved with the use of echo-planar imaging techniques, but this would require specialized hardware and software. A more reliable evaluation of cerebral hemodynamic parameters also needs an absolute quantification. Rempp et al6 have recently established a technique for absolute quantification of rCBF and rCBV with dynamic susceptibility contrast-enhanced imaging. Their method allows the assessment of the arterial input function and tissue concentration-time curves with the use of a simultaneous dual FLASH MRI sequence. Their results were in good agreement with data from PET. The magnitude and duration of the signal loss due to spin dephasing of diffusing protons in the perfused microcapillary bed vary with the local dynamic concentration of contrast agent.30 Although CBV values for gray matter decrease with age, the white matter CBV value remains more or less unchanged. A ratio of about 2:1 for the CBV of cortical gray versus white matter measured with the use of different techniques has been described in the recent literature.6 31 32 33 The mean values measured for the gray to white matter ratio for CBV in the present study were slightly higher. The values measured for the gray to white matter ratio for CBV in the present study ranged between 2.63±0.2 and 2.48±0.26 in control subjects. Gückel et al12 found that the ratio for CBV between gray and white matter yielded a mean value of 2.30±0.65 for the volunteers. In children Tzika et al10 found an average ratio of 2.84±0.93. These values are very close to those observed in our study. The difference between some literature data and our own findings might be related to the location of the cortical ROIs, the latter possibly involving venous or arterial structures and thus leading to overestimation of CBV. The analysis of the concentration-time curves and their use for calculation of cerebral hemodynamic parameters are based on the central volume theorem,34 which associates the transit time or outflow rate of tracers from the tissue blood pool with the tissue blood volume and the inflow rate. In this derivation, the calculation of the MTT35 and other parameters depends largely on the successful administration of a fast and compact bolus of the MR contrast agent. In practice, this requirement for bolus administration is sometimes difficult to satisfy, and variation may arise in the data as a consequence of differences in bolus administration.10 Although correlative hemodynamic procedures were not performed, the data provided here are useful because it is a clinical application of a theory recently adapted for MRI. This approach may provide a relatively simple method to improve the understanding of cerebral hemodynamics in patients with vascular disorders. Accordingly, this technique may be added to any clinical MR examination without adding appreciable time, so large series of patients with an atheromatous stenosis or occlusion of the ICA can be further studied.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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The authors are grateful for the assistance of Prof M. Laville and Serge Balter, pharmacist, from Mediathèque Université Claude Bernard Lyon I, in the preparation of MRI scans that appear in this article.
Received July 17, 1995; revision received November 13, 1995; accepted November 23, 1995.
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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T. Neumann-Haefelin, H.-J. Wittsack, G. R. Fink, F. Wenserski, T.-Q. Li, R. J. Seitz, M. Siebler, U. Modder, and H.-J. Freund Diffusion- and Perfusion-Weighted MRI : Influence of Severe Carotid Artery Stenosis on the DWI/PWI Mismatch in Acute Stroke Stroke, June 1, 2000; 31(6): 1311 - 1317. [Abstract] [Full Text] [PDF]
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P. M. Rothwell and C. P. Warlow Low Risk of Ischemic Stroke in Patients With Reduced Internal Carotid Artery Lumen Diameter Distal to Severe Symptomatic Carotid Stenosis : Cerebral Protection Due to Low Poststenotic Flow? Stroke, March 1, 2000; 31(3): 622 - 630. [Abstract] [Full Text] [PDF]
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H. C. Roberts, W. P. Dillon, and W. S. Smith Dynamic CT Perfusion to Assess the Effect of Carotid Revascularization in Chronic Cerebral Ischemia AJNR Am. J. Neuroradiol., February 1, 2000; 21(2): 421 - 425. [Abstract] [Full Text]
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M. Kluytmans, J. van der Grond, K. J. van Everdingen, C. J. M. Klijn, L. J. Kappelle, and M. A. Viergever Cerebral Hemodynamics in Relation to Patterns of Collateral Flow Stroke, July 1, 1999; 30(7): 1432 - 1439. [Abstract] [Full Text] [PDF]
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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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M. Kluytmans, J. van der Grond, B. C. Eikelboom, and M. A. Viergever Long-Term Hemodynamic Effects of Carotid Endarterectomy Stroke, August 1, 1998; 29(8): 1567 - 1572. [Abstract] [Full Text] [PDF]
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J. van der Grond, B.C. Eikelboom, and W.P.Th.M. Mali Flow-Related Anaerobic Metabolic Changes in Patients With Severe Stenosis of the Internal Carotid Artery Stroke, November 1, 1996; 27(11): 2026 - 2032. [Abstract] [Full Text]
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