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Visualization of Lenticulostriate Arteries 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 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 optimal TOF-MRA and flow-sensitive black-blood (FSBB) MRA to visualize the LSA at 3T. Materials and Methods: 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 LSAs were 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 visualization was best with 400 SORS pulses for TOF-MRA but FSBB-MRA was better than TOF-MRA, which indicates its clinical potential to investigate the LSA on a 3T magnetic resonance imaging. Key Words: Lenticulostriate artery; slice-selective off-resonance sinc pulse; saturation transfer contrast; flow-sensitive black-blood; MR angiography. ªAUR, 2014 I mpairment 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 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. Acad Radiol 2014; 21:812–816 From the Department of Diagnostic Radiology, Kyoto University Graduate School of Medicine, 54 Shogoin Kawaharacho, Sakyo-ku, Kyoto 606-8507, Japan (S.O., T.O., K.F., Y.F., A.K., A.Y., M.K., T.D., T.M.M., K.T.) and Toshiba America Research Institute, Vernon Hills, IL (M.M., X.Z.). Received January 14, 2014; accepted March 4, 2014. Address correspondence to: T.O. e-mail: [email protected] ªAUR, 2014 http://dx.doi.org/10.1016/j.acra.2014.03.007 812
Transcript
Page 1: Visualization of Lenticulostriate Arteries at 3T

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.

Page 2: Visualization of Lenticulostriate Arteries at 3T

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

Page 3: Visualization of Lenticulostriate Arteries at 3T

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).

Page 4: Visualization of Lenticulostriate Arteries at 3T

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

Page 5: Visualization of Lenticulostriate Arteries at 3T

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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