Acta Radiologica

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High‐Resolution Contrast‐Enhanced Magnetic

Resonance Angiography of the Carotid Arteries
Using Fluoroscopic Monitoring of Contrast Arrival:
Diagnostic Accuracy and Interobserver Variability

B. Butz, U. Dorenbeck, I. Borisch, N. Zorger, M. Lenhart, S. Feuerbach & J.

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To cite this article: B. Butz, U. Dorenbeck, I. Borisch, N. Zorger, M. Lenhart, S. Feuerbach & J.
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Arteries Using Fluoroscopic Monitoring of Contrast Arrival: Diagnostic Accuracy and Interobserver
Variability, Acta Radiologica, 45:2, 164-170

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 ORIGINAL ARTICLE ACTA RADIOLOGICA

High-Resolution Contrast-Enhanced Magnetic Resonance

Angiography of the Carotid Arteries Using Fluoroscopic Monitoring
of Contrast Arrival: Diagnostic Accuracy and Interobserver
Variability
B. BUTZ, U. DORENBECK, I. BORISCH, N. ZORGER, M. LENHART, S. FEUERBACH & J. LINK
Department of Radiology, University of Regensburg Hospital, Regensburg, Germany; Department of
Neuroradiology, University of Homburg Hospital, Homburg, Germany; Department of Radiology, Spitalregion
St. Gallen, St. Gallen, Switzerland

Butz B, Dorenbeck U, Borisch I, Zorger N, Lenhart M, Feuerbach S, Link J. High-

resolution contrast-enhanced magnetic resonance angiography of the carotid arteries
using fluoroscopic monitoring of contrast arrival: Diagnostic accuracy and interobserver
variability. Acta Radiol 2004;45:164–170.
Purpose: To evaluate the diagnostic accuracy of high-resolution contrast-enhanced
magnetic resonance angiography (CE-MRA) of the supra-aortic arteries using the
CareBolus technique. Digital subtraction angiography was the standard of reference.
Material and Methods: Fifty consecutive patients with suspected internal carotid artery
stenosis underwent CE-MRA and digital subtraction angiography. CE-MRA was
performed on a 1.5-T superconducting scanner with the CareBolus technique.
CareBolus combines a nearly real-time 2D-FLASH (fast low angle shot) sequence for
fluoroscopic triggering and a high-resolution 3D-FLASH with elliptical centric view
order for the angiographic pulse sequence (6.0/2.16 ms [TR/TE], 30‡ flip angle, 30.98 s
acquisition time, 0.88 mm effective (interpolated) partition thickness and a 1606512
matrix). Intra-arterial digital subtraction angiography and CE-MRA studies were
evaluated independently by four blinded readers. Internal carotid artery stenoses were
graded according to the NASCET criteria.
Results: CE-MRA had an accuracy of 92.53%, a sensitivity of 95.64%, and a specificity
of 90.39% for the identification of carotid artery stenoses §70% (grade 3). Image
quality for suppression of stationary tissue and venous contrast was good, but was
reduced in five cases due to patient motion.
Conclusion: The CareBolus technique is a useful non-invasive method for high-
resolution imaging of the supra-aortic vessels because of its easy application and high
sensitivity and specificity. Limitations can occur in non-compliant patients due to
motion artifacts during the measurement time.
Key words: Angiography; elliptic centric view ordering; magnetic resonance imaging;
supra-aortic arteries
B. Butz, Department of Radiology, University of Regensburg Hospital, D-93042
Regensburg, Germany (fax. z49 0941 944 7402, e-mail. bebu0000@t-online.de)
Accepted for publication 26 October 2003

It has been shown in clinical trials that patients with
severe symptomatic carotid artery stenosis benefit
from thromboendarterectomy. The NASCET (North
American Symptomatic Endarterectomy Trial)
showed a significant reduction of risk in stroke
in patients with a severe carotid artery stenosis
§70%) (1).
Currently, intra-arterial digital subtraction angio-
graphy (DSA) is still the gold standard for the
diagnosis of carotid artery stenosis. Nevertheless,
non-invasive tests have become important in
preoperative imaging of carotid artery stenosis.
Ongoing quality improvement of these methods
requires frequent reassessment of accuracy, reli-
ability, and their potential for replacement of DSA.
Contrast-enhanced magnetic resonance angiogra-
phy (CE-MRA) is one of the most important non-
invasive tests for determining the degree of stenosis
of the internal carotid arteries. A large number of
trials concerning the value of MRA have been

DOI 10.1080/02841850410003699 # 2004 Taylor & Francis


published in recent years. According to this
literature, CE-MRA is recommended for screening
procedures and postoperative imaging (18–20).
Non-contrast-enhanced MRA shows a high rate
of overestimation of the degree of stenosis and
problems with the evaluation of severe stenoses or
preocclusive disease with a low flow rate. To obtain
high-resolution images with reduced venous over-
lay, a precise timing of the contrast bolus and a
sequence filling those k-space parts that determine
the image contrast of the arterial system is
necessary.
The CareBolus technique combines a 2D turbo-
FLASH (fast low angle shot) with a 3D FLASH
sequence. The 2D sequence acquires one single axial
scan of the aortic arch each second, and this allows
arrival of the contrast agent in the aortic arch to be
observed. At that time the 3D scan can be started,
incorporating a centric reordering scheme to obtain
a high signal in the arterial system. The present
prospective and randomized study describes our
results with this technique.
Material and Methods
Patients
During a period of 7 months, 50 consecutive patients
(37 M, 13 F; age range 41–81 years; mean 68¡8 years;
mean weight 74¡11 kg) with suspected stenoses of the
internal carotid artery (ICA) were examined by intra-
arterial digital subtraction angiography and gadoli-
nium-enhanced MR angiography of the ICA. Thirty
patients showed clinical symptoms caused by ICA
stenosis, e.g. amaurosis fugax, transient ischemic
attack, minor or major stroke, and 20 patients had no
clinical symptoms. The examinations were performed
preoperatively or before ICA stenting. Written
informed consent was obtained from all patients
before examination. The clinical study was approved
by the ethics committee at our facility. Patients with
known contraindications for CE-MRA or DSA were
excluded. Both examinations were performed within
one week. No treatment was performed during this
period.
Imaging technique
Transfemoral catheter arteriograms using a digital
subtraction technique (Angiostar Plus; Siemens,
Erlangen, Germany), aortic arch injection, selective
catheterization of both common carotid arteries
and documentation of three different views (poster-
ior–anterior, lateral and 45‡ oblique) of both
internal carotid arteries were obtained in all
patients and served as the standard of reference.
MR Angiography of the Carotid Arteries 165
CareBolus is a trademark in computed tomo-
graphy (Siemens Erlangen, Germany) that has been
transferred to MRI (6). CareBolus CE-MRA was
performed on a 1.5-T whole body superconducting
scanner (Magnetom Symphony; Siemens, Erlangen,
Germany) with a combined circular polarized head
and neck coil. Contrast agent, gadopentate dime-
glumine (Magnevist; Schering, Berlin, Germany)
was injected into a cubital vein with a dose of
0.2 mmol/kg body weight. The bolus was delivered
by a power injector (Spectris MR injector; Medrad,
Pittsburgh, Pa., USA) at a flow rate of 2.5 ml/s, and
was followed by a saline flush (40 ml) at the same
flow rate. A central line was not used in any of our
patients. For positioning the CE-MRA slab and the
monitoring plane, an axial trueFISP sequence (true
fast imaging with steady-state precession) and a PC
sequence (phase contrast) in coronal and sagittal
orientations were used as localizers. The CE-MRA
slab was positioned in the typical angulated way
(coronal and parallel to the carotid artery) to
capture the entire length of the carotid artery from
the aortic arch to the skull base, including the entire
length of the vertebral arteries. The monitoring
plane was positioned in an axial orientation
through the aortic arch. The monitoring plane
comprises a 2206220 mm field of view, with a 10-
mm-thick section and delivers one image per second.
Figure 1 shows the inflow of the contrast agent
bolus in the aortic arch on the axial ‘‘fluoroscopic’’
images. Table 1 gives the parameters of the 3D
FLASH sequence.
An unenhanced study for subtraction of the
background was acquired before administration of
the contrast agent. The unenhanced study was
acquired in the same fashion as the enhanced study.
On starting the axial fluoroscopic sequence, gado-
linium and saline were injected and the arrival of
the contrast bolus in the aortic arch was observed
(Fig. 1). When the aortic arch was completely
enhanced, the 3D FLASH sequence was started
by manual triggering. The acquisition time was
30.98 s and the calculation time about 3.50 min. All
patients were instructed to breath quietly through-
out the whole acquisition. A breath-holding
technique was not used. The source coronal
images were post-processed with a standard max-
imum intensity projection (MIP) algorithm (Mag-
netom Symphony, Numaris 3.5 software, Version
VA11A; Siemens, Erlangen). Each carotid artery
was segmented individually at 15‡ rotational
intervals around the cephalocaudal axis. MIP
images and individual coronal partitions were
analysed.
Acta Radiol 2004 (2)
166 B. Butz et al.

Fig. 1. This image shows the inflow of the contrast agent bolus in the aortic arch on the axial fluoroscopic images.

Evaluation consensus of all observers. All images were printed

Four experienced radiologists assessed CE-MRA on film. Stenoses of the internal carotid arteries
independently in a randomized and blinded order. were evaluated with a jeweller’s eyepiece callibrated
The right and left carotid arteries were evaluated to the tenth of a millimetre. Vessels with signal void
separately. Image analysis was based on original on the CE-MRA and evidence of flow in the ICA
subtracted enhanced MRA data sets, maximum distal to the bifurcation were considered patent and
intensity projection and intra-arterial DSA. DSA defined as high-grade (70%–99%) stenosis according
was the standard of reference, evaluated in to the literature review (15). Quantification of
stenoses was based on the narrowest diameter and
Table 1. Parameters of MRA sequences performed at the supra- the normal width distal to the post-stenotic dilata-
aortal arteries using the head-neck coil tion. This technique derived from the NASCET
CareBolus FLASH 3D criteria for carotid artery stenosis (7, 16). To
evaluate stenosis, the stenoses were classified as
TR (ms) 6.0
TE (ms) 2.16
(16): NASCET grade 1 (0%–29%), grade 2 (30%–
Flip angle (‡) 30 69%), grade 3 (70%–99%) and grade 4
Slabs 1 (100%~occlusion). The image quality, including
Slab thickness (mm) 70 suppression of stationary tissue and venous suppres-
Effective partition 0.88
sion, was evaluated using a 4-point scale: Suppres-
thickness (mm)
Partitions 40 sion of stationary tissue: no stationary tissue seen,
Matrix 1606512 slight stationary tissue seen, severe stationary tissue
(phase encoding 6 frequency encoding) overlay but adequate for diagnosis, non-diagnostic.
Field of view (mm) 1886300 Venous suppression: no veins seen, slight venous
(rectangular, coronal plane)
Typical pixel size (mm) 0.59 (x)61.17 (y)60.88 (z)
overlay, severe venous overlay but adequate for
Time of acquisition (s) 30.98 diagnosis, non-diagnostic. Image quality was eval-
uated on the original subtracted enhanced studies.

Acta Radiol 2004 (2)


Statistical analysis
All analyses were performed with Excel software
(Microsoft, USA) and SPSS for Windows (SPSS,
USA). Sensitivity, specificity, and accuracy were
calculated for ICA stenosis of each grade on the
basis of the classifications of each observer. For
each comparison of DSA and CE-MRA we used
the two-tailed Wilcoxon rank sum test. The level for
statistical significance was set at a P-value of v0.5.
Cohen’s kappa value (k), linear regression coeffi-
cients (r), and the mean values of the absolute
differences of the DSA and CE-MRA results of
each observer versus those of the others were
calculated as indicators of interobserver agreement
and variability. An interval scale was used for this
analysis. Interobserver agreement was considered
slight at a value equal or less than 0.2; fair 0.21–0.4;
moderate 0.41–0.6; substantial 0.61–0.8, or almost
perfect 0.81–1.0 (12).
Results
In all patients entered in our study, both carotid
arteries could be evaluated. No neurological event
occurred during or after the imaging tests investi-
gated. The average bolus arrival time was 18¡3.5 s,
with a range between 13 and 28 s. In all cases,
arrival of the gadolinium bolus was readily detected
in the fluoroscopic frame.
Image quality
In 98% of all cases, CareBolus CE-MRA of the
supra-aortic arteries revealed excellent delineation
of the internal, external, and common carotid
arteries, as well as of the carotid siphon. The
middle and anterior cerebral arteries were also well
visualized. In 20% of all cases the image quality
(suppression of stationary tissue) of the aortic arch
was slightly reduced. At aortic arch level, suppres-
sion of stationary tissue was evaluated as ‘‘slight
stationary tissue seen’’ to ‘‘severe stationary tissue
overlay but adequate for diagnosis’’. Suppression of
stationary tissue at the level of the carotid artery
bifurcation or ICA was evaluated as ‘‘no stationary
tissue seen’’ (94%) to ‘‘slight stationary tissue seen’’
(6%). There was a significant difference between
image quality at aortic arch level and ICA level.
Only in one case did severe venous overlay occur;
the veins at the level of the jugular bulb and at the
upper level were enhanced. In no case did venous
contrast obscure arterial anatomy. No case showed
insufficient contrast enhancement in the internal
carotid arteries, because of a timing failure (too
early timing) and in no case was there a ‘‘non-
diagnostic’’ image quality.
MR Angiography of the Carotid Arteries 167
Assessment of stenosis by DSA
Consensus evaluation of 100 vessels with DSA
revealed 36 ICA (mostly carotid bifurcation) with a
severe stenosis. Carotid arteries were totally
occluded in 9 cases. Moderate stenosis was
observed in 19 cases and mild stenosis in 36.
CE-MRA versus DSA
Evaluation of stenosis yielded 92.6% concordant
gradings (Spearman’s rank test) with CE-MRA and
DSA. Concordant results occurred in 93.6% of mild
stenoses, in 65.5% of moderate stenoses, in 86.8% of
severe stenoses and 100% for occlusion (all
observers). Of 400 evaluations there were 12
overestimations (3%) and 41 underestimations
(10.3%). For identifying 70%–99% (grade 3) steno-
sis, as determined by DSA, the mean values for
sensitivity, specificity, and accuracy of CE-MRA
were 95.64%, 90.39%, and 92.53%. Occlusion
specificity was 100%. There were 6 (1.5%) false-
positive estimations of a 70%–99% stenosis in MRA
and 6 (1.5%) of a 30%–69% stenosis. There were 19
(4.8%) false-negative estimations of a 70%–99%
stenosis and 23 (5.8%) of a 30%–69% stenosis. All
occlusions (grade 4) were correctly identified.
Figure 2 shows a left-side severe stenosis of the
carotid bifurcation in CE-MRA and DSA. A good
example for a false-positive estimation is Fig. 3.
Signal void in MRA
A signal void was identified in nine CE-MRA
evaluations. For these carotid arteries the degree of
stenosis on DSA ranged from 60% to 99%.
Classification into grade 3 (70%–99%) stenosis
was concordant with DSA in 89%. In one case, a
short-length signal void was detected presenting
with a grade 2 stenosis on DSA, thus leading to
overestimation.
Interobserver agreement
The average values of all four readers for Cohen’s
k-value, linear regression, and absolute difference
did not show significant differences between MRA
and DSA. The P-values were 0.363, 0.393, and
0.167. According to Cohen’s k-value, interobserver
agreement was substantial (k~0.809) for CE-MRA.
For values, see Table 2.
Discussion
Elliptic centric contrast-enhanced MRA has been
shown to offer reliable high-quality images of the
carotid arteries with DSA analogous lumen filling
characteristics (4, 5, 21, 22). Before the era of
Acta Radiol 2004 (2)
168 B. Butz et al.

Fig. 2. Example of the excellent delineation of the carotid arteries using the CareBolus technique. A left-side high-grade stenosis of the
carotid bifurcation in CE-MRA (left hand) and in DSA (right hand) is shown.

Fig. 3. In this case, a grade 2 stenosis (DSA) was overestimated in MRA (grade 3).

Acta Radiol 2004 (2)


Table 2. Kappa value, linear regression coefficient, and absolute
difference in grade (NASCET) of stenosis
CE-MRA
Observer pairs k (r)
Observer 1 vs. observer 2 0.832 0.958
Observer 1 vs. observer 3 0.771 0.935
Observer 1 vs. observer 4 0.794 0.938
Observer 2 vs. observer 3 0.828 0.959
Observer 2 vs. observer 4 0.849 0.962
Observer 3 vs. observer 4 0.780 0.946
Mean value 0.809 0.950
k~Kappa value; (r)~linear regression coefficient; (dd)~absolute
difference in grade (NASCET) of stenosis.
contrast-enhanced MRA, 2- and 3-dimensional
TOF (time of flight) or phase contrast techniques
were used to image the supra-aortic arteries. These
blood flow based methods are limited by low flow
and disturbance caused by vascular lesions in
stenotic areas. Because of intravoxel dephasing
and complex flow (6, 22), the grade of stenosis has
been overestimated. Rising peak systolic velocity
increases the length of signal void (6, 8, 17, 22). The
use of contrast agent has reduced this signal loss
substantially owing to the reduction of echo time
and the diminution of saturation effects resulting in
more accurate imaging of the stenoses (5, 11). The
vessel signal is related to a contrast agent enhanced
T1 shortening effect in the vessel lumen. Spin
saturation effects from in-plane flow or slow flow
are reduced and short echo times reduce intravoxel
spin-dephasing in turbulance flow caused by
vascular lesions (6, 13, 22).
Advancement in CE-MRA initially occurred
with the peripheral arterial system. Initial attempts
to use CE-MRA in supra-aortic arteries were
hampered by the rapid enhancement of the
venous system, especially in the internal jugular
veins. There was need for a long acquisition time
(up to several minutes) in addition with extensive
application of contrast agent (3, 6, 9, 22) in order
to acquire the central k-space lines during the
arterial phase of the bolus. One method of getting
high-resolution images of the carotid arteries is for
the contrast agent bolus to be sufficiently drawn
out such that the high k-space views are still
acquired with reasonable contrast enhancement
(21). This is the way data are acquired with the
CareBolus technique. Elliptical centric view order
measures the central k-space lines during the
arterial phase of the gadolinium bolus in the first
part. The image contours were measured during
the second part. This allows sufficient venous
MR Angiography of the Carotid Arteries 169
suppression. An acquisition time up to 49 s (6, 10,
22) is possible using this method.
High-resolution CE-MRA allows the carotid
artery to be imaged along its entire length, i.e.
(dd)
from the aortic arch to the skull base. This is
0.09 necessary because studies have shown that a second
0.11
stenosis can be found in up to 9% (14) of all cases.
0.10
0.09 A known problem is the signal loss, which occurs
0.08 when limited spatial resolution and intravoxel
0.12 dephasing is combined at the point of severe
0.10 stenosis. Signal void leads to overestimation of
the degree of a stenosis. This effect, which is
confirmed by our results, can be reduced by using a
high spatial resolution.
Generally, the CareBolus technique proved to be
a robust method for high-resolution CE-MRA. In
all cases the time of triggering was readily
detectable at the axial 2D fluoroscopic layer. In
no case was image quality ‘‘non-diagnostic’’. In
five cases only, image quality was moderate due to
movements in non-compliant patients. In these
cases, background stationary tissue was increased
and there was a slight double contour at the length
of the carotid artery. Substantial parenchymal
enhancement did not limit delineation of the
carotid artery in any case. One limitation of the
CareBolus technique is the long measurement time.
The time of acquisition is 30.98 s for non-contrast
and contrast images and the calculation time is
about 4 min each. Total measurement time is
therefore about 10 min, without preparing and
post-processing time. Suppression of venous signal
was good, even in late bolus timing. Using this
bolus-timing technique, patient limitations, such as
severe heart failure or prolonged blood circulation
time, did not influence the excellent arterial
contrast. This effect is often observed in non-
bolus timing techniques; for example, in time-
resolved methods. DSA and CE-MRA were
evaluated by four readers. The resulting total
number of observations was 400 for CE-MRA.
Comparing with the results of other groups (6, 21,
22), our interobserver variability (linear regression
coefficient) regarding the degree of ICA stenosis
was not significantly different. The interobserver
agreement in our group was substantial. According
to BLAND et al. (2), comparison of a new
measurement technique with an established one
using correlation coefficients is inappropriate. Even
using kappa statistics is clearly arbitrary (12).
Thus, we additionally used the absolute differences
in degree of stenosis between the two estimates for
each pair of observers to describe the interobserver
variability.
In conclusion, high-resolution CE-MRA with the
Acta Radiol 2004 (2)
170 B. Butz et al.
CareBolus technique has proved to be a reliable
method for imaging ICA stenosis. It is reliable for
clinically relevant severe stenosis. Overall image
quality is high. Owing to the long measurement
time, slight limitations of image quality may occur
occasionally in non-compliant patients due to
patient motion.
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