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Published online before print October 14, 2004, 10.1148/radiol.2333031276
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(Radiology 2004;233:899-904.)
© RSNA, 2004

Technical Developments

Internal Carotid Artery Occlusion Assessed at Pulsed Arterial Spin-labeling Perfusion MR Imaging at Multiple Delay Times1

Jeroen Hendrikse, MD, PhD, Matthias J. P. van Osch, PhD, Dirk R. Rutgers, MD, Chris J. G. Bakker, PhD, L. Jaap Kappelle, MD, PhD, Xavier Golay, PhD and Jeroen van der Grond, PhD

1 From the Depts of Radiology (Hp E 01.132) (J.H., M.J.P.v.O., D.R.R., C.J.G.B., J.v.d.G.) and Neurology (L.J.K.), Univ Medical Center Utrecht, PO Box 85500, 3508 GA Utrecht, the Netherlands; Dept of Radiology, Johns Hopkins Univ School of Medicine, Baltimore, Md (X.G.); and F. M. Kirby Research Center for Functional Brain Imaging, Kennedy Krieger Institute, Baltimore, Md (X.G.). Received Aug 11, 2003; revision requested Oct 28; final revision received Feb 11, 2004; accepted Mar 8. Address correspondence to J.H. (e-mail: j.hendrikse@azu.nl).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 Materials and Methods
Results
 Discussion
 REFERENCES
 
Magnetic resonance (MR) imaging with pulsed arterial spin labeling (ASL) was performed at six different inversion times in nine patients with internal carotid artery (ICA) occlusion and in 11 control subjects. The hospital’s commission on scientific research on human subjects approved the study protocol, and all study subjects gave informed consent. Cerebral blood flow (CBF) in the middle cerebral artery territories was calculated from the combined signal intensities measured with ASL at the multiple inversion times. In the patients with ICA occlusion, mean CBF values were decreased in the gray matter of the hemisphere ipsilateral to the occlusion, as compared with values in the gray matter of the contralateral hemisphere (P < .05) and with values in the gray matter of the control subjects (P < .05). Quantification of CBF with ASL at multiple inversion times can compensate for the blood transit delays in patients with ICA occlusion.

© RSNA, 2004

Index terms: Brain, diffusion, 10.12144 • Carotid arteries, flow dynamics • Carotid arteries, MR, 172.121411, 172.121412, 172.121413, 172.121416, 172.12142, 172.12144, 172.12146 • Carotid arteries, stenosis or obstruction, 172.721 • Magnetic resonance (MR), perfusion study, 10.12144


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
Materials and Methods
Results
 Discussion
 REFERENCES
 
Patients with symptomatic occlusion of the internal carotid artery (ICA) and compromised cerebral blood flow (CBF) are at risk for future ischemic infarcts in the brain (1,2). Reduced CBF indicates stage II or III hemodynamic cerebral impairment (3), with which both collateral blood flow and compensatory vasodilatation of resistance vessels are insufficient. Currently, the modalities used to perform CBF measurements in patients with ICA occlusion are invasive in that they involve injection of radioactive tracers or contrast agents (4–7). Arterial spin labeling (ASL) is a relatively recently developed magnetic resonance (MR) imaging technique that enables measurement of CBF in a noninvasive manner (8–10). With ASL, the protons of the arterial water in the feeding vasculature of the brain are magnetically labeled and used as an endogenous tracer. After the ASL, a certain delay—that is, an inversion time (TI)—is necessary before MR images can be acquired. This delay allows the labeled arterial water protons to flow through the arterial vascular tree and exchange magnetization with the unlabeled tissue water. The subsequent change in tissue magnetization can be detected at MR imaging and yields information about the CBF.

In clinical ASL studies (11–13), a CBF decrease has been observed in patients with dementia and epilepsy. In patients who have had acute strokes, a perfusion-diffusion mismatch has been detected by using ASL combined with diffusion-weighted MR imaging (14). Furthermore, ASL has been shown to be useful for the noninvasive assessment of CBF in patients with ICA stenosis (15–17). To our knowledge, no ASL examinations have been performed in patients with ICA occlusion thus far. In these patients, the quantification of CBF is complicated because of the relatively large contribution of collateral blood flow to the cerebral perfusion. Labeled blood flowing through collateral vessels has a delayed arrival in the brain tissue that results in an underestimation of the CBF. A theoretic study (18) revealed that such CBF underestimation could be corrected by performing ASL measurements with multiple TIs between the ASL and the actual MR image acquisition. The purpose of the present study was to perform quantitative ASL perfusion MR imaging in patients with ICA occlusion and to evaluate the delayed collateral blood flow by acquiring ASL images at multiple TIs.


   Materials and Methods
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
 Discussion
 REFERENCES
 
Study Subjects
Nine consecutive patients (mean age, 64 years; age range, 52–76 years) with symptomatic unilateral ICA occlusion—six men (mean age, 63 years; age range, 52–76 years) and three women (mean age, 67 years; age range, 64–74 years)—were examined during a 6-month study period. The ICA occlusion was on the right side in five patients and on the left side in four patients. These patients presented with symptoms of hemispheric transient ischemic attack (n = 4) or minor stroke (n = 5). All patients had transient or minor disabling neurologic deficits in the supply territory of the occluded ICA. Transient neurologic deficits were defined as symptoms that lasted less than 1 day. A minor disabling deficit was associated with a Rankin scale score of 3 or higher and indicated that symptoms lasted longer than 1 day (19).

Patients were referred to the radiology department of University Medical Center Utrecht by vascular surgeons or neurologists for diagnosis and grading of the ICA obstruction with intraarterial digital subtraction angiography. All patients had less than 30% stenosis in the contralateral vessel at intraarterial digital subtraction angiography according to North American Symptomatic Carotid Endarterectomy Trial criteria (20).

Eight male (mean age, 48 years; age range, 27–60 years) and three female (mean age, 43 years; age range, 26–59 years) control subjects also were included in our study. These control subjects were four MR imaging technicians (three men, one woman; mean age, 28 years; age range, 26–30 years) and seven patients (five men, two women; mean age, 54 years; age range, 42–60 years). The control patients were a random sample group from a vascular screening MR imaging study involving patients referred to our hospital because of peripheral vascular disease (n = 3) or stable angina pectoris (n = 4). The predefined exclusion criteria for the control subjects were a history of neurologic disease or a vascular abnormality seen on T1- or T2-weighted MR images or on MR angiograms.

We obtained informed consent from all patients and control subjects, and the hospital’s commission on scientific research on human subjects approved the study protocol.

Imaging Techniques
MR imaging was performed by using a 1.5-T system (Gyroscan ACS-NT; Philips Medical Systems, Best, the Netherlands). For all MR image acquisitions, a quadrature head coil was used for radiofrequency transmission and signal reception. A pulsed labeling method, the transfer insensitive labeling technique (TILT), was used with a 140-mm-wide labeling slab and a 6-mm gap between imaging sections. The TILT ASL sequence and its labeling efficiency have been previously described in detail (21,22). The perfusion imaging section, which was 10 mm thick, was positioned above the ventricles through the centrum semiovale and aligned parallel to the orbitomeatal angle (Fig 1).



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  		Figure 1. Left: Sagittal MR angiogram (13.7/7, 20° flip angle) shows position of the thick ASL slab (1) and location of ASL perfusion imaging section (2). The gap between the labeling slab and the imaging section is 6 mm. The ASL perfusion image was obtained through the centrum semiovale parallel to the orbitomeatal angle. Right: ASL sequence for magnetization TILT is shown. A presaturation pulse is used to decrease the tissue signal intensity and to avoid contamination by the labeling pulse. ASL of the arterial water protons is achieved with two section-selective 90° radiofrequency pulses in the thick labeling slab proximal to the imaging section. The perfusion-weighted ASL images were acquired at six TIs: 200, 400, 600, 800, 1200, and 1600 msec. A 3000-msec repetition time (TR) and a 36-msec echo time were used. EPI = echo-planar imaging.

 
ASL perfusion MR imaging was performed at six TIs (200, 400, 600, 800, 1200, and 1600 msec) between the labeling and the image acquisition. The TI range of 200–1600 msec was chosen on the basis of the exchange of the labeled water protons with the tissue water (lower limit) and the T1 decay of the magnetically labeled water (upper limit) (18). For image acquisition, a four-shot echo-planar MR imaging readout was used. The ASL signal intensity was corrected for imperfections in section profiles (23). Other imaging parameters used to perform ASL perfusion MR imaging were 3000/36 (repetition time msec/echo time msec), a 90o flip angle, a 240 x 240-mm field of view, and a 128 x 128 matrix. Five signals were acquired to result in a total imaging time per TI of 2 minutes.

For control preparation—that is, unlabeled MR image acquisition—the phase of the second 90° pulse was shifted by 180° to result in a 0° (90° – 90°) net effect and insensitivity to magnetization transfer. Before the 90o pulses, a presaturation pulse was applied to the image section to decrease the tissue signal intensity and to measure the T1 of tissue under the influence of perfusion and the equilibrium magnetization of the brain tissue. For manual segmentation of the gray matter, a spin-echo inversion-recovery MR image was acquired with 2300/17/300 (repetition time msec/echo time msec/TI msec) and the same geometry used to obtain the perfusion-weighted ASL MR images. At visual inspection, no substantial distortions between the echo-planar gradient-echo perfusion data and the spin-echo inversion-recovery data were found.

To exclude regions of infarction, a corresponding T2-weighted spin-echo MR image (2000/100, 90° flip angle) was used. Vessels were excluded from the volume of interest according to findings on phase-contrast MR angiograms (20/8, 15° flip angle, 25 cm/sec flow velocity in all directions). The total imaging time for the ASL protocol was 14 minutes. Reference ASL perfusion values were obtained in seven control subjects. In four other control subjects, the MR technicians, the reproducibility of the ASL CBF measurements was assessed by obtaining three consecutive measurements during the same MR imaging examination.

Quantification of the CBF values measured on the ASL images at multiple TIs was performed in three consecutive steps: First, perfusion-weighted ASL images were obtained by subtracting the labeled images from the control images at the six different TIs. Second, a region of interest (ROI) in the gray matter of the middle cerebral artery flow territory was selected. One observer (J.H.) selected the middle cerebral artery flow territory in all subjects (both healthy volunteers and patients) on the basis of established flow territory templates (24). In the single section above the ventricles, the ROI was placed on the cortical surface, excluding the anterior cerebral artery flow territory localized in the midline. ROI sizes in a single hemisphere ranged from 15 to 17 cm2.

Third, quantification of the CBF was performed by using a fit of the ROI signal intensities measured at the six TIs to the ASL perfusion model described by Buxton et al (18). This model assumes instantaneous exchange, which gives rise to an error of less than 1% for the field strength used in the present study and normal CBF values (25). CBF fitting was performed for each subject separately. The perfusion signal intensity of the tissue ({Delta}M) at a certain time after inversion (t) was then derived by using the following equations:

{r04dc29e01}

{r04dc29e02}

{r04dc29e03}
where k = (1/T1a) – (1/T1app), {lambda} is the brain-blood partition coefficient of water, {Delta}t is the transit delay of the labeled blood, {tau} is the duration of the delivery of the labeled blood, {alpha} is the inversion efficiency, T1a is the longitudinal relaxation constant of arterial blood, and T1app is the T1 of tissue under the influence of arterial perfusion. For each subject and each hemisphere, the T1app and the equilibrium magnetization of the brain tissue (M0,tiss) were measured in a gray matter ROI by using a fit of the signal intensity on the control (ie, unlabeled) images at the six TIs (200–1600 msec) to a saturation-recovery curve. The other parameters in Equations (1)–(3) were fixed and were obtained from the literature: T1a = 1.4 seconds, {alpha} = 1, and {lambda} = 0.9 mL/g (26–28).

Statistical Analyses
In the four control subjects in whom an ASL CBF reproducibility measurement was obtained, a mean intrasubject coefficient of variation was calculated for the CBF (29,30). The coefficient of variation is a measure of variability that is calculated by dividing the sample standard deviation by the sample mean. It expresses mean differences between measurements. We multiplied the coefficient of variation by 100 to yield a percentage.

A power calculation was based on the assumption that the standard deviation of the CBF in both hemispheres was 15 mL/min per 100 g of tissue. A sample size of at least six patients is sufficient to observe a difference in CBF of 30 mL/min per 100 g of tissue with {alpha} < .05 (type I error) and ß < .10 (type II error). Differences in CBF values between the male and female patients and between the left and right hemispheres in the control subjects were tested by using the nonparametric Mann-Whitney U test (SPSS, version 10.1.0; SPSS, Chicago, Ill). The effect of age on CBF values in the patient group was evaluated by using linear regression analysis. Differences in fitted CBF in the gray matter between the hemisphere ipsilateral to the ICA occlusion, the contralateral hemisphere, and the cerebral hemispheres in the control subjects also were analyzed by using the nonparametric Mann-Whitney U test. Furthermore, ratios of the ASL signal intensity of the ipsilateral hemisphere to the ASL signal intensity of the contralateral hemisphere at the six TIs were calculated. CBF values were expressed as means ± standard deviations. A two-sided P value of less than .05 was considered to indicate statistical significance.


   Results
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
Discussion
 REFERENCES
 
In the control subjects, the ASL MR images obtained at the six TIs and the corresponding CBF map show symmetric perfusion between the two hemispheres (Fig 2). In the patients with ICA occlusion (Fig 3), a clear asymmetry in perfusion signal intensity was present, with decreased signal intensity on the side of the occlusion. In the four healthy control subjects (the MR technicians) in whom three consecutive CBF measurements were obtained, there was no obvious relationship between the variability of the CBF measurements and the mean CBF (Fig 4). CBF data were generated by using the combined perfusion-weighted MR imaging data obtained at the six TIs (see Materials and Methods). The coefficient of variation for the ASL CBF measurements in the gray matter was 11%.



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  		Figure 2. Images obtained in 55-year-old male control subject. A, Turbo TILT MR images (3000/36, 90° flip angle, 20 signals acquired) obtained with ASL show differences in signal intensity at six TIs as a function of the postlabeling delay, or TI, in the acquisition of a transverse section positioned through the centrum semiovale. B, Voxel-by-voxel flow map, with flow in milliliters per minute per 100 g of tissue, generated on the basis of the differences in signal intensity at the six TIs. L = left, R = right.

 


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  		Figure 3. Images obtained in 63-year-old man with ICA occlusion. A, Turbo TILT MR images (3000/36, 90° flip angle, 20 signals acquired) obtained with ASL show differences in signal intensity at six TIs as a function of the postlabeling delay, or TI, in the acquisition of a transverse section positioned through the centrum semiovale. B, Voxel-by-voxel flow map, with flow in milliliters per minute per 100 g of tissue, generated on the basis of the differences in signal intensity at the six TIs. There is a clear asymmetry in perfusion signal intensity, with decreased signal intensity on the side of the occlusion. L = left, R = right.

 


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  		Figure 4. Scatterplot shows relationship between the three successive measurements of CBF (in milliliters per minute per 100 g of brain tissue) obtained in the control subjects with the described ASL quantification method. The average of the three CBF measurements is plotted horizontally, and the differences between the three measurements are plotted vertically. There is no relationship between the variability of the CBF measurements and the mean CBF. On the basis of the plotted data, the coefficient of variation for the ASL CBF measurements—that is, the standard deviation (SD) of the difference given as a percentage of the mean CBF—is 11%.

 
Hemodynamic Response Curves
Average hemodynamic response curves for signal intensity at perfusion-weighted MR imaging (hereafter, perfusion-weighted signal intensity) as a function of TI were generated for the gray matter in the ipsilateral and contralateral hemispheres in the nine patients with ICA occlusion and for the gray matter in the seven control subjects (Fig 5). The shape of the hemodynamic response curves indicates a general increase in perfusion-weighted signal intensity at the short TIs that was caused by the arrival of the labeled blood, followed by a decrease in signal intensity at the long TIs that was caused by a combination of washout of the tracer and T1 relaxation. In the patients, the mean ratio of ipsilateral-to-contralateral ASL signal intensity was 0.81 at a TI of 200 msec, 0.54 at a TI of 400 msec, 0.67 at a TI of 600 msec, 0.70 at a TI of 800 msec, 0.60 at a TI of 1200 msec, and 0.51 at a TI of 1600 msec.



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  		Figure 5. Average hemodynamic response curves for the ASL images. The percentage change in signal intensity [({Delta}M/M0) x 100%] on the perfusion-weighted ASL MR images was measured as a function of TI in a gray matter ROI in the flow territory of the middle cerebral artery of the ipsilateral and contralateral hemispheres in nine patients with ICA occlusion and in a gray matter ROI in seven control subjects. Curves fitted to the data points at the six TIs are shown for the ipsilateral hemisphere, the contralateral hemisphere, and the gray matter of the control subjects. Vertical error bars represent standard deviations.

 
Comparison of CBF Measurements
The hemodynamic response curves (Fig 5) describing the perfusion-weighted signal intensity at the six TIs were used for quantitative CBF fitting (see Eqq [1–3]). The mean CBF in the gray matter of the ipsilateral hemisphere in the patients with ICA occlusion (53.6 mL/min per 100 g ± 20.9 [standard deviation]) was significantly decreased compared with that in the gray matter of the contralateral hemisphere (79.7 mL/min per 100 g ± 14.7, P < .05) and compared with that in the gray matter of the control subjects (79.8 mL/min per 100 g ± 30.2, P < .05). We found no significant difference in CBF between the gray matter in the contralateral hemisphere of the patients with ICA occlusion and the gray matter of the control subjects. Furthermore, in the patient group, sex and age had no influence on CBF. In the control subjects, no significant differences in mean CBF between the left hemisphere (82.3 mL/min per 100 g ± 31.4) and the right hemisphere (77.3 mL/min per 100 g ± 31.2) were observed.


   Discussion
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
 Discussion
REFERENCES
 
Our findings in the present study show the capability of noninvasive ASL to enable quantification of CBF in patients with ICA occlusion with use of data obtained at multiple TIs to compensate for delayed collateral flow. With use of this ASL method, we observed a significant decrease in CBF in the hemisphere ipsilateral to the ICA occlusion as compared with both the CBF in the contralateral hemisphere and the CBF in the control subjects.

The CBF decrease measured in the gray matter of the flow territory of the middle cerebral artery ipsilateral to the ICA occlusion is in agreement with the findings in previously performed positron emission tomography (PET) and xenon-based perfusion imaging studies (31–34).

In both the control subjects and the contralateral hemisphere of the patients with ICA occlusion, we observed a mean CBF of 80 mL/min per 100 g of tissue. The absence of a significant difference between the CBF in the contralateral hemisphere of the patients with ICA occlusion and the CBF in the control subjects is in agreement with the results of previous PET studies (32,35). In the present study, the control subjects were, on average, 10 years younger than the patients with ICA occlusion. A correction for the decrease in CBF with age, as has been done in previous studies, would have resulted in 5%–10% lower CBF values in the control subjects and relatively high CBF values in the contralateral hemisphere of the patients with unilateral ICA occlusion (36,37).

Nevertheless, the "at-rest" CBF values measured in the control subjects in the present study are in agreement with gray matter CBF values of 66–81 mL/min per 100 g of tissue, which were measured at multiple TIs in previously performed ASL studies (38,39). Although ASL CBF measurements are highly correlated with CBF measurements obtained with other techniques (40), ASL is well known to yield slightly overestimated CBF values in the gray matter owing to the presence of label in the vasculature (38).

With respect to the reproducibility of the CBF measurements, we calculated a relative coefficient of variation of 11%. It is likely that measurement errors were the primary cause of this variation because small physiologic fluctuations in CBF occur within 40 minutes, during which the three ASL data sets were acquired. In contrast, the daily variation in CBF has been reported to be about 12% (41,42).

The CBF measurement error observed in the present study was also related to the small number of signals acquired (n = 5) per TI. Increasing the number of signals acquired leads to decreases in measurement error. However, in clinical examinations, the maximum imaging time is limited by the patient throughput, and there has to be a trade-off between the number of signals acquired, the number of TIs, and the total imaging time to obtain the ASL perfusion measurements. In previous studies with healthy control subjects, large numbers of signals were acquired, with resulting total ASL imaging times longer than 60 minutes (39,43).

An indication that the variations in CBF observed with the described ASL protocol are reasonable is the finding of similar CBF values in the gray matter of the contralateral hemispheres in the patient group and in the gray matter of the control group. Compared with the use of other perfusion methods, the use of ASL, owing to its noninvasive nature, excludes additional potential sources of variation, such as contrast material or radioactive tracer injection and blood arrival efficiency. In the present study, we used a single-section ASL method, which, as shown in a previous study (21) of the TILT ASL sequence, can easily be extended to multisection imaging.

The most important advantage of using CBF measurements obtained at multiple TIs rather than ASL at a single TI is the correction for differences in the transit time of the blood flow from the position of labeling to the brain tissue. In patients with severe obstructive ICA disease, the presence of collateral blood flow may increase the transit time of the labeled blood flow to the brain tissue (44). With ASL performed at a single TI, delayed collateral flow causes a signal intensity decrease on ASL images to erroneously indicate a CBF decrease, whereas the signal decay is primarily due to transit time effects (18). In addition to ASL at multiple TIs, quantitative imaging of perfusion by using a single subtraction has been introduced to render the ASL technique relatively insensitive to blood transit delays (45).

In the present study, the following three-step approach was used to obtain quantitative CBF measurements in each brain hemisphere of the patients and in the control subjects: (a) subtraction of labeled ASL images from control ASL images, (b) ROI segmentation in the gray matter of the middle cerebral artery flow territory, and (c) CBF fitting of the ROI signal intensity at six TIs. Although a pixel-by-pixel fit to the model proposed by Buxton et al (18) would be optimal to account for the distribution of transit times across the section, the differences in transit time within the segmented flow territory of the middle cerebral artery are considered to be small. Furthermore, with a signal-to-noise ratio of 20 with use of the described ASL method, the stability of the CBF fitting would substantially improve at ROI analysis.

A general drawback that ASL studies share with PET and single photon emission computed tomography perfusion studies is the difficulty in quantifying white matter CBF. With current ASL methods, areas with nearly zero blood flow are depicted in the white matter. In future clinical studies, the use of higher field strength magnets may also allow quantification of CBF in white matter by means of increased signal-to-noise ratios in the white matter at ASL (46).

Another potential problem with ASL CBF measurements is the presence of label in the vasculature (38). To decrease the vascular ASL signal intensity, vascular crushers can be added to the ASL sequence. In the present study, no vascular crushers were used and the intraarterial signal intensity was excluded from the ASL CBF measurements according to MR angiogram findings. This and other postprocessing strategies have been shown to be useful for excluding the signal intensity of large and medium-sized arteries (7,47). However, small vasculature can still cause overestimations of CBF measurements. Because a vascular ASL contribution of the feeding arterial tree will decrease proportionally with the true CBF decrease, the effect of this potential error on ASL CBF measurements is likely to be small.

In conclusion, we acquired ASL perfusion MR images at multiple TIs in patients with delayed collateral flow due to ICA occlusion. In clinical examinations, changes in CBF are highly correlated with changes in arterial blood transit time. Therefore, the described method may broaden the clinical use of ASL as a completely noninvasive and quantitative approach to imaging cerebral hemodynamics.


   FOOTNOTES
 
Abbreviations: ASL = arterial spin labeling, CBF = cerebral blood flow, ICA = internal carotid artery, ROI = region of interest, TI = inversion time, TILT = transfer insensitive labeling technique

Authors stated no financial relationship to disclose.

Author contributions: Guarantors of integrity of entire study, J.H., M.J.P.v.O., J.v.d.G.; study concepts, J.H., J.v.d.G.; study design, J.H., M.J.P.v.O., J.v.d.G.; literature research, J.H.; clinical studies, D.R.R., L.J.K.; data acquisition, J.H., D.R.R.; data analysis/interpretation, X.G., C.J.G.B., J.H.; statistical analysis, X.G., C.J.G.B., J.H.; manuscript preparation and editing, J.H., M.J.P.v.O., J.v.d.G.; manuscript definition of intellectual content and final version approval, all authors; manuscript revision/review, X.G., L.J.K., J.v.d.G.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
 Discussion
 REFERENCES
 

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