Visualization of LenticulostriateArteries at 3T:
Optimization of Slice-selective Off-resonance Sinc Pulse–prepared TOF-MRA
and Its Comparison with Flow-sensitive Black-blood MRA
Sachi Okuchi, MD, Tomohisa Okada, MD, PhD, Koji Fujimoto, MD, PhD, Yasutaka Fushimi, MD, PhD,Aki Kido, MD, PhD, Akira Yamamoto, MD, PhD, Mitsunori Kanagaki, MD, PhD, Toshiki Dodo, MD,
Taha M. Mehemed, MD, Mitsue Miyazaki, PhD, Xiangzhi Zhou, PhD, Kaori Togashi, MD, PhD
Ac
FrScJaToJaT.
ªht
81
Rationale and Objectives: To optimize visualization of lenticulostriate artery (LSA) by time-of-flight (TOF) magnetic resonance angiog-
raphy (MRA) with slice-selective off-resonance sinc (SORS) saturation transfer contrast pulses and to compare capability of optimalTOF-MRA and flow-sensitive black-blood (FSBB) MRA to visualize the LSA at 3T.
Materials andMethods: This study was approved by the local ethics committee, and written informed consent was obtained from all the
subjects. TOF-MRA was optimized in 20 subjects by comparing SORS pulses of different flip angles: 0, 400�, and 750�. Numbers of LSAswere counted. The optimal TOF-MRA was compared to FSBB-MRA in 21 subjects. Images were evaluated by the numbers and length of
visualized LSAs.
Results: LSAs were significantly more visualized in TOF-MRA with SORS pulses of 400� than others (P < .003). When the optimal TOF-
MRA was compared to FSBB-MRA, the visualization of LSA using FSBB (mean branch numbers 11.1, 95% confidence interval (CI)10.0–12.1; mean total length 236 mm, 95% CI 210–263 mm) was significantly better than using TOF (4.7, 95% CI 4.1–5.3; 78 mm, 95%
CI 67–89 mm) for both numbers and length of the LSA (P < .0001).
Conclusions: LSA visualizationwas best with 400� SORSpulses for TOF-MRAbut FSBB-MRAwas better than TOF-MRA,which indicatesits clinical potential to investigate the LSA on a 3T magnetic resonance imaging.
KeyWords: Lenticulostriate artery; slice-selective off-resonance sinc pulse; saturation transfer contrast; flow-sensitive black-blood; MR
angiography.
ªAUR, 2014
Impairment of the lenticulostriate artery (LSA) often leads
to lacunar infarction and cerebral hemorrhage, which is
recognized as ‘small vessels, big problems (1).’ The LSA
branches supply blood to the basal ganglia and its vicinity
(2,3), and their occlusion results in infarction of these
structures (4,5). Recently, LSA branches have successfully
been visualized using 7T (6,7) and 3T (8,9) magnetic
resonance imaging (MRI) systems with three-dimensional
(3D) time-of-flight (TOF) magnetic resonance angiography
(MRA). Whereas at 1.5T, a recent study reported that flow-
sensitive black blood (FSBB) MRA, which decreases blood
ad Radiol 2014; 21:812–816
om the Department of Diagnostic Radiology, Kyoto University Graduatehool of Medicine, 54 Shogoin Kawaharacho, Sakyo-ku, Kyoto 606-8507,pan (S.O., T.O., K.F., Y.F., A.K., A.Y., M.K., T.D., T.M.M., K.T.) andshiba America Research Institute, Vernon Hills, IL (M.M., X.Z.). Receivednuary 14, 2014; accepted March 4, 2014. Address correspondence to:O. e-mail: [email protected]
AUR, 2014tp://dx.doi.org/10.1016/j.acra.2014.03.007
2
flow signal with weak motion-dephasing gradient, performed
better than TOF-MRA for visualization of the LSA (10).
Moreover, FSBB-MRA at 1.5T could detect differences in
the LSA between patients with lacunar infarction and/or
hypertension and control subjects (11). However, at 3T, there
is no study so far that has compared LSA visualization using
TOF-MRA to FSBB-MRA.
In TOF-MRA acquisition, the saturation transfer contrast
pulse is often used to reduce background signal, but the blood
signal is also reduced, although the blood to background
contrast is usually increased. To less reduce the blood signal,
slice-selective off-resonance sinc (SORS) pulse (12) can be
applied, and enhanced visualization of LSA branches at 1.5T
has been achieved (13).
Therefore, we hypothesized that SORS pulse–prepared
TOF-MRA may have high visualization capability of LSA
branches comparable to FSBB-MRA. In this study, TOF-
MRA was firstly investigated for the optimal SORS pulse.
Then, comparative study was conducted for visualization of
the LSA between the optimized TOF-MRA and FSBB-
MRA.
Academic Radiology, Vol 21, No 6, June 2014 MRA TO VISUALIZE LSA AT 3T: FSBB VERSUS TOF
MATERIALS AND METHODS
This study was approved by the local ethics committee, and
written informed consent was obtained from all the subjects
enrolled. TOF-MRAwith SORS pulse was firstly optimized
for the flip angle by counting number of visualized LSA
branches, then the optimized TOF-MRA was compared to
FSBB-MRA. Images were evaluated for numbers and length
of visualized LSAs.
Subjects
Twenty volunteers (16 men and 4 women; age range
29–74 years, mean 52 years) were enrolled for the optimiza-
tion study of TOF-MRA. The subjects had history of smok-
ing (n= 5), hypertension (n= 4), diabetes mellitus (n= 2), and
brain infarction (n= 1). Twenty-one volunteers (13men and 8
women; age range 29–82 years, mean 55 years) were enrolled
for the comparative study of the optimized TOF-MRA and
FSBB-MRA. The subjects had history of smoking (n = 8),
hypertension (n= 7), hyperlipidemia (n= 4), diabetes mellitus
(n = 3), cerebral infarction (n = 2), and cerebral hemorrhage
(n = 1).
Image Acquisition
All scanswere takenwith a 3TMRIunit (EXCELARTVantage
Powered by ATLAS, Toshiba Medical Systems Corporation,
Otawara-shi, Japan), equipped with a 32-channel head coil.
For optimization, 3D TOF-MRAwas acquired with three
different flip angles of SORS pulses: 0, 400�, and 750�. The0� flip angle means the SORS pulse is off; the 400� flip angle
was applied before each excitation pulse; the 750� pulse wasonly applied at the k-space center (1/6 of the total k-space
lines) because of ‘‘specific absorption rate’’ (SAR) limitation.
After obtaining localizing images of three orthogonal axis,
TOF-MRA was scanned in the anterior commissure (AC)–
posterior commissure (PC) slice orientation with the
following parameters: repetition time (TR)/echo time (TE),
35/6.8 milliseconds; flip angle, 20�; matrix, 384 � 384; field
of view, 192 � 192 mm; and one axial 3D slab with 60 slices
(0.8 mm slice thickness).
FSBB-MRA was scanned with the same spatial resolution
to the 3D TOF-MRA, but it was in coronal orientation,
because coronal orientation was better compared to axial
orientation when resolution was the same (14). Scan parame-
ters of FSBB-MRAwere as follows: TR/TE, 35/13 millisec-
onds; flip angle, 15�; and b value of the motion-dephasing
gradient, 0.3 s/mm2 (14). FSBB-MRA was acquired with
the same high resolution to that of TOF-MRA. To improve
signal-to-nose ratio, TE was shortened by adopting a smaller
b value than that at 1.5T (10).
For both TOF-MRA and FSBB-MRA, a parallel imaging
factor of 2 was used, and scan time was 7 minutes and 24
seconds. Final image volumes were reconstructed into
0.25 � 0.25 � 0.4 mm resolution.
Image Analysis
In the analysis of TOF-MRA optimization, 3D image volume
data were transferred to a commercially available workstation
(AZE VirtualPlace Lexus; AZE Ltd., Tokyo, Japan) and the
following processing and evaluations were conducted. After
reorienting the 3D axial image volumes into coronal (perpen-
dicular to the AC–PC line), each of consecutive five slices was
projected by maximum intensity (ie, maximum intensity pro-
jection [MIP] of 2 mm thickness). Using these images, LSA
branches longer than 5 mm were traced and analyzed (10).
When an artery branches within 5 mm from the horizontal
segment of the middle cerebral artery (MCA) and the prox-
imal (A1) part of anterior cerebral artery (ACA) origin,
each branch was counted and measured separately, because
>70% of branches were found to originate from common
trunks (3).
For the comparison between TOF-MRA and FSBB-
MRA, TOF-MRA image volumes were reoriented into cor-
onal and the sameMIP processing was conducted as described
previously. FSBB-MRA image volumes were processed by
minimum intensity projection (ie, MinIP of 2 mm thickness).
Using these images, LSA branches were traced and measured
for length with the same manner described previously.
The evaluation was conducted by two radiologists indepen-
dently (S.O. and T.D. both with 7 years of experience).
Statistical Analysis
Agreements of independent measurements by two radiologists
were evaluated using intraclass correlation coefficients. The
numbers of visualized branches per subject were compared
pairwise among TOF-MRAs with SORS pulses of 0,
400�,and 750� using two-tailed paired t test. Both average
numbers and total length of visualized LSA branches were
compared between FSBB and TOF with two-tailed paired t
test. Statistical analyses were conducted using a commercially
available software package MedCalc (MedCalc Software,
Mariakerke, Belgium). A P value <.05 after Holm correction
for multiple comparisons was considered statistically
significant.
RESULTS
The intraclass correlation coefficients of agreement between
the two evaluators in counting LSA branches were 0.88
(95% confidence intervals [CI]: 0.70–0.95), 0.85 (95% CI:
0.62–0.94), and 0.94 (95% CI: 0.86–0.98), respectively for
TOF-MRAs with SORS pulse of 0, 400�, and 750�, whichwas an almost perfect agreement (15). The comparison among
intraclass correlation coefficients was not statistically different
(P > .05).
The average numbers of visualized LSA branches per
subject were 3.7 (95% CI: 2.9–4.4), 5.3 (95% CI: 4.5–6.1),
and 4.1 (95% CI: 3.2–5.0) for SORS pulses of 0, 400�, and
813
TABLE 1. Number of Visualized LSA Branches for TOF-MRA
0� 400� 750�
Branch numbers 3.7 (2.9–4.4) 5.3 (4.5–6.1)*,y 4.1 (3.2–5.0)
LSA, lenticulostriate artery; MRA, magnetic resonance angiog-
raphy; TOF, time-of-flight.
The numbers in the parentheses are 95% confidence intervals.
*P = .0001 compared with 0�.yP = .0025 compared with 750�.
Figure 1. Representative images of LSA branches (white arrows) inTOF-MRAwith SORS pulses of (a) 0�, (b) 400�, and (c) 750�. The LSAbranches in TOF-MRA with SORS pulse of 400� were visualized bet-
ter than those of 0� and 750�. LSA, lenticulostriate artery; MRA, mag-
netic resonance angiography; SORS, slice-selective off-resonancesinc; TOF, time-of-flight.
TABLE 2. Branch Numbers and Length of Visualized LSABranches for TOF (400�) and FSBB-MRA
Branch Numbers Length (mm)
TOF 4.7 (4.1–5.3) 78 (67–89)
FSBB 11.1 (10.0–12.1) 236 (210–263)
P value <.0001 <.0001
FSBB, flow-sensitive black blood; LSA, lenticulostriate artery; MRA,
magnetic resonance angiography; TOF, time-of-flight.
The numbers in the parentheses are 95% confidence intervals.
OKUCHI ET AL Academic Radiology, Vol 21, No 6, June 2014
750�, respectively. The average LSA branch number with
SORS pulse of 400� was statistically greater than those of
0� and 750� (P = .0001 and 0.0025, respectively; Table 1
and Fig. 1). The difference between 0� and 750� was not
statistically significant.
In the comparison between the optimal TOF-MRA
(ie, with SORS pulse of 400�) and FSBB-MRA, intraclass
correlation coefficients of agreement between two evaluators
814
for counting LSA branches were 0.78 (95% CI: 0.45–0.91)
and 0.89 (95% CI: 0.73–0.96) and those for measuring LSA
branch length were 0.68 (95% CI: 0.22–0.87) and 0.87
(95% CI: 0.67–0.95) for TOF-MRA and FSBB-MRA,
which was substantial to almost perfect agreement (15). The
comparison of intraclass correlation coefficient was not statis-
tically different (P = .25 and 0.15, respectively for numbers
and length) between the two MRAs.
Average numbers of visualized LSA branches per subject
were 4.7 (95% CI: 4.1–5.3) and 11.1 (95% CI: 10.0–12.1),
and averages of total length of visualized LSA branches were
78 mm (95% CI: 67–89 mm) and 236 mm (95% CI:
210–263 mm), respectively for TOF-MRA and FSBB-
MRA. In both comparisons, the difference was highly signif-
icant (P < .0001; Table 2 and Fig. 2).
DISCUSSION
The saturation transfer contrast method has proven to be a
powerful method to increase contrast in MRI and MRA, us-
ing relaxation differences in tissues (16–18). It was first used in
imaging using continuous wave off-resonance irradiation
(16). The saturation pulse is spatially nonselective in general
and reduces the signal of brain background tissues as well as
that of inflowing blood. However, the SORS pulse suppresses
brain background signal while maintaining signal of inflowing
blood (12). As was expected, the LSA branches were visual-
ized better in TOF-MRAwith the SORS pulse than without
it (ie, 0�). The LSA branches were visualized better in TOF-
MRAwith 400� SORS pulse than with 750� pulse, probablybecause the 400� SORS pulse was placed in front of each exci-
tation, whereas the 750� SORS pulse was placed at the
k-space center only. That is the tradeoff between higher
SORS pulse saturation power and the SAR limit.
In the following comparison study, the average number of
visualized LSA branches was more than doubled and the total
length of LSA visualization was tripled by FSBB-MRA than
the optimized TOF-MRA. The reason is because TOF-
MRA is a blood inflow technique (19); for the very slow
blood flow in LSA branches, the blood signal is more likely
to be saturated. For a black-blood scan, the fast-spin echo
sequence was initially used (20,21); however, very slow or
recirculating vessels were difficult to visualize without
incorporating inversion recovery preparation pulses (22,23).
Figure 2. Representative images of LSA branches (white arrows) in
(a) TOF-MRA (400�) and (b) FSBB-MRA. LSA branches were visual-ized better with FSBB than TOF. FSBB, flow-sensitive black blood;
LSA, lenticulostriate artery; MRA, magnetic resonance angiography;
TOF, time-of-flight.
Academic Radiology, Vol 21, No 6, June 2014 MRA TO VISUALIZE LSA AT 3T: FSBB VERSUS TOF
Weighting on susceptibility contrast has also been used
(24,25), but it is more suitable for small veins rather than
arteries. FSBB is an alternative black-blood method, where
the flow-sensitive gradient can dephase blood signal with a
wide range of flow velocity with an appropriate b value
(26). Such a difference in visualization mechanism has resulted
in the higher visualizing capability of FSBB-MRA. There is
an interesting variant of FSBB-MRA, which is hybrid of
opposite-contrast MRA. It combines TOF and FSBB
methods by subtracting the latter from the former images
(27), whose evaluation is yet to be conducted.
A recent study reported that FSBB-MRA was better than
TOF-MRA at 1.5T for visualization of the LSA (10). We
had similar findings to this study at 3T. Using FSBB-MRA,
the average numbers of visualized LSA branches per subject
were 6.9 at 1.5T (10) compared to 11.1 at 3T. The numbers
of LSA branches were reported to range from 2 to 12 (mean
7.1) on one side of hemisphere in autopsied brains (3), mean-
ing 14.2 LSA branches in total on average. FSBB-MRA at 3T
has some more to be improved.
Detailed visualization of LSA branches is clinically very
important. The relationship between decreased LSA visualiza-
tion and hypertension or infarction at the basal ganglia and/or
its vicinity has been well demonstrated (8,11,28–30). If some
morphologic changes in the LSA, such as hypovisualization,
were detected in asymptomatic patients with hypertension or
diabetes mellitus, it would motivate patients and physicians
for better disease control and may allow more rigorous
therapeutic interventions to prevent symptomatic events.
Based on the findings in this study, FSBB-MRA can be a
good method for visualizing the LSA in clinical setting,
although further studies are required to clarify predictability
of FSBB findings for future morbidity. Another advantage
of FSBB-MRA is visualization capability of the micro-
anatomy around the proximal MCA and its branches, which
is very important for planning an aneurysm surgery. It may
help to avoid clipping or blood flow disturbance of LSA or
other small branches (31,32).
Compared to FSBB-MRA, TOF-MRA is more sensitive
to inflow speed, which is disadvantageous for the LSA visual-
ization. However, this effect itself may have clinically impor-
tant information. The spatial resolution of TOF-MRA
images in this study was larger than most of the LSA branches.
Arterial signal inside of an imaging voxel is averaged with the
background and obscured. A smaller voxel improves visualiza-
tion of the LSA, but the scan time is increased, which is usually
not acceptable as a clinical scan. Recently, compressed sensing
(CS) has been brought into MRI. CS reconstructs images
from undersampled data using iterative steps. This method
may improve visualization of the LSA, but the background
signal has to be lower than those of LSA branches (33).
Reduction of the background signal by the SORS pulse
would also contribute to that purpose.
There are a few limitations in this study. First, there are
several structures visualized as black on FSBB images. Perivas-
cular space or cerebrospinal fluid (CSF) might be detected as
the same signal void. In aged subjects, the perivascular space is
frequently dilated, but the CSF signal in the space is usually
higher than the dephased arterial blood signal of the LSA
branch. Calcification, small hemorrhage, and iron deposit
are also visualized as a signal void, but these can be identified
as spotty, nodular, or even mass-like lesions and may not
exhibit the ‘‘string-like’’ shape of LSA branches. Veins can
also be visualized as a signal void if the blood flow velocity
is close to that in LSA. However in this study, vessels arising
from the MCA and the part A1 of ACA were included. Sec-
ond, some volunteers had history of disorders, which may
affect the visualization of LSAs, but the condition was the
same for both TOF-MRA and FSBB-MRA.
In conclusion, the LSA visualization using TOF-MRAwas
best with SORS pulse of 400� flip angle than with those of
0� and 750�. However, the optimized TOF-MRA with
SORS pulse is not comparable to FSBB-MRA for the visual-
ization of LSA. This indicates that FSBB-MRA would be a
better choice at 3T for visualization of the LSA.
ACKNOWLEDGMENTS
We express our sincere gratitude toMrs. Kyoko Takakura, RT
and Mr. Hajime Sagawa, RT at Department of Radiology,
Kyoto University Hospital and Mr. Naotaka Sakashita at
815
OKUCHI ET AL Academic Radiology, Vol 21, No 6, June 2014
Toshiba Medical Systems, Ohtawara-shi, Japan for their help
of this study.
Grants: Thiswork is fundedbya sponsored researchprogram
‘‘Research for Improvement of MR Visualization (No.
150100700014)’’ of Toshiba Medical Systems, Japan, and
Grant-in-Aid for Scientific Research on Innovative Areas
‘‘Initiative forHigh-DimensionalData-Driven Science through
Deepening of SparseModeling (No. 4503)’’ of TheMinistry of
Education,Culture, Sports, Science andTechnology, Japanpro-
vided toK.T.The former grant contributed to the acquisition of
volunteer images of TOF-MRA and FSBB-MRA. The latter
grant contributed to analysis of the acquired data.
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