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Original Research  n  Neuroradiology

Subarachnoid Hemorrhage in
Patients with Good Clinical
Grade: Accuracy of 3.0-T MR
Angiography for Detection and
Characterization1
Minghua Li, MD
Purpose: To evaluate the diagnostic accuracy of aneurysm detection
Yueqi Zhu, MD
and the fidelity of morphologic characterization of three-
Hongmei Song, MD dimensional (3D) time-of-flight (TOF) magnetic resonance
Binxian Gu, MD (MR) angiography at 3.0 T in patients with a Glasgow coma
Haitao Lu, MD score of 15 and noncontrast material–enhanced computed
Yuehua Li, MD tomography (CT) findings that showed acute nontraumatic
Huaqiao Tan, MD subarachnoid hemorrhage.
Yingsheng Cheng, MD
Materials and The institutional review board approved this prospective study,
Methods: and patients provided informed consent. A total of 277 pa-
tients who had not experienced trauma but in whom non-
enhanced CT showed subarachnoid hemorrhage, who had a
Glasgow coma score of 15, and who underwent both 3D TOF
MR angiography and digital subtraction angiography (DSA)
(the reference standard) were included. Three observers who
were blinded to clinical and DSA results independently an-
alyzed all 3D TOF MR angiographic data sets. The receiver
operating characteristic curve was applied to analysis of the
detection of aneurysms with 3D TOF MR angiography by using
patient- and aneurysm-based evaluations. Multivariate logistic
regression analysis was performed to identify aneurysm-spe-
cific variables, including size, shape (daughter sac/lobulation/
margin), neck width (wide if . 4 mm or if fundus-to-neck ratio
was , 2), and relation to adjacent artery, that significantly af-
fected morphologic assessment with 3D TOF MR angiography.

Results: Aneurysms were depicted with DSA in 225 patients. In pa-

1
 From the Department of Radiology, Shanghai Jiao Tong
University–Sixth Affiliated People’s Hospital, No. 600
Yishan Road, Shanghai 200233, China. Received June
25, 2016; revision requested August 22; revision received
October 7; accepted November 2; final version accepted
January 5, 2017. Address correspondence to Y.Z. (e-mail:
zhuyueqi@hotmail.com).
Z.Y. supported by the Shanghai Pujiang Program
(16PJD036), by the Medicine Summit Program of the
Medical School of Shanghai Jiaotong University, and by
grants from the National Natural Science Foundation of
China (81370041). L.M. supported by grants from the
National Natural Science Foundation of China (81471760,
81671655).
tient- and aneurysm-based evaluations, respectively, 3D TOF
MR angiography yielded accuracies of 96.8% (268 of 277) and
96.6% (309 of 320), sensitivities of 98.2% (219 of 223) and
98.1% (260 of 265), specificities of 91% (49 of 54) and 89%
(49 of 55), positive predictive values of 97.8% (219 of 224) and
97.7% (260 of 266), and negative predictive values of 92% (49
of 53) and 91% (49 of 54). Accuracy of display of morphologic
features was 92.5% (236 of 255) for size, 86.3% (220 of 255)
for neck width, 94.5% for shape (241 of 255), and 96.9% (247
of 255) for relationship to adjacent vessel. Width of aneurysm
neck was the only variable that significantly affected the mor-
phologic assessment of 3D TOF MR angiography (odds ratio,
0.378; 95% confidence interval: 0.337, 8.347; P = .004).
Conclusion: Three-dimensional TOF MR angiography can accurately de-
pict cerebral aneurysms and accurately display their mor-
phologic features in stable patients with subarachnoid hem-
orrhage and a Glasgow coma score of 15.

q
 RSNA, 2017
q
 RSNA, 2017

Radiology: Volume 284: Number 1—July 2017  n  radiology.rsna.org 191

NEURORADIOLOGY: MR Angiography for Aneurysm Detection and Characterization Li et al
A
cute subarachnoid hemorrhage
caused by rupture of a cerebral
aneurysm is associated with high
morbidity and mortality, and effective
treatment depends on efficient and
accurate detection of the ruptured an-
eurysm (1,2). Conventional catheter
angiography is generally considered
the reference-standard technique for
detection of cerebral aneurysms, but
noninvasive methods, such as com-
puted tomographic (CT) angiography or
magnetic resonance (MR) angiography,
have become promising alternatives
following the development of improved
equipment and imaging sequences (3–
5). CT angiography is recommended
as the first choice because of its fast
scanning speed and convenience; how-
ever, it is associated with exposure to
ionizing radiation and nephrotoxicity
risks. MR angiography is free of these
problems and is therefore a promising
alternative. Our previous studies have
revealed that the diagnostic accuracy
of MR angiography for the detection
of cerebral aneurysm can be as great
as 96%–97% with the use of a three-
dimensional (3D) time-of-flight (TOF)
MR angiographic technique (6,7). Ac-
curate evaluation of the morphologic
Advances in Knowledge
nn Three-dimensional time-of-flight
(TOF) MR angiography at 3.0 T
has high accuracy and sensi-
tivity—96.8% (268 of 277) and
98.2% (219 of 223), respec-
tively—for the detection of
cerebral aneurysms in patients
with subarachnoid hemorrhage
who have a Glasgow coma score
of 15.
nn Three-dimensional TOF MR an-
giographic images were usable
for reconstruction in 98.3% of
patients (282 of 287).
nn Accurate display of morphologic
features at three-dimensional
TOF MR angiography was 92.5%
(236 of 255) for size, 86.3% (220
of 255) for neck width, 94.5%
(241 of 255) for shape, and
96.9% (247 of 255) for relation-
ship to adjacent vessel.
192 radiology.rsna.org  n Radiology: Volume 284: Number 1—July 2017
features of cerebral aneurysms and the
associated circulation is critical for the
selection and optimization of the en-
dovascular or surgical technique. Few
studies have focused on the capability
of 3D TOF MR angiography, as com-
pared with conventional angiography,
for detailed morphologic display of ce-
rebral aneurysms.
In this study, we aimed to evaluate
the diagnostic accuracy of aneurysm
detection and the fidelity of morpho-
logic characterization of 3D TOF MR
angiography at 3.0 T in patients with
a Glasgow coma score of 15 and non-
contrast material–enhanced CT findings
of acute nontraumatic subarachnoid
hemorrhage.
Materials and Methods
Patients
The institutional review board approved
the study protocol, and patients or their
relatives gave informed consent before
their participation in this prospective
study. This discussion about the study
was held immediately after the unen-
hanced CT examination was finished
and involved undergoing MR angiogra-
phy instead of CT angiography.
Between February 1, 2009, and Au-
gust 31, 2015, a total of 545 patients
had nontraumatic subarachnoid hemor-
rhage that was confirmed with nonen-
hanced CT in our hospital. Of the 391
patients with subarachnoid hemorrhage
and a Glasgow coma score of 15, 314
were eligible and agreed to inclusion in
this study. Twenty-seven patients were
excluded for the following reasons: (a)
pacemaker or steel implants (n = 10),
(b) allergy to contrast material (n = 1),
(c) renal dysfunction that precluded the
use of contrast material (n = 4), and (d)
Implication for Patient Care
nn Three-dimensional TOF MR angi-
ography can efficiently depict
cerebral aneurysms and accu-
rately display the morphologic
structure in stable patients with
subarachnoid hemorrhage and a
Glasgow coma score of 15.
symptom deterioration that occurred
while the patient was waiting or moving
locations for MR angiography and that
the neurologist believed was caused by
rebleeding (n = 12).
The patients directly underwent
digital subtraction angiographic (DSA)
embolism (n = 9) or surgical clipping
(n = 3) after emergent consultation
with the neurointerventional radiolo-
gist and neurosurgeon. Among the re-
maining 287 patients, satisfactory MR
angiographic images were successfully
acquired in 98.3% (282 of 287). Motion
artifacts, leading to uninterpretable im-
age quality, occurred in 15 patients.
In 10 of these 15 patients, a second
examination was successful, with im-
age quality sufficient for diagnosis.
However, the other five patients were
also intolerant of the procedure the
second time and were finally excluded
from the study. Meanwhile, another
five patients declined to undergo DSA
and were also excluded. No patient ex-
perienced rebleeding during MR angi-
ography. Thus, as the study flowchart
(Fig 1) shows, a total of 277 patients
who underwent both 3D TOF MR an-
giography and DSA were included in
the final analysis. The study group com-
prised 117 men and 160 women, with
a mean age of 53.87 years 6 11.87
(standard deviation) (age range, 24–79
https://doi.org/10.1148/radiol.2017161469
Content codes:
Radiology 2017; 284:191–199
Abbreviations:
DSA = digital subtraction angiography
ICA = internal carotid artery
3D = three-dimensional
TOF = time of flight
Author contributions:
Guarantor of integrity of entire study, Y.Z.; study concepts/
study design or data acquisition or data analysis/inter-
pretation, all authors; manuscript drafting or manuscript
revision for important intellectual content, all authors; man-
uscript final version approval of final version of submitted
manuscript, all authors; agrees to ensure any questions
related to the work are appropriately resolved, all authors;
literature research, M.L., Y.Z., Y.C.; clinical studies, M.L.,
Y.Z., H.S., B.G., H.L., Y.L., H.T.; statistical analysis, M.L., Y.Z.;
and manuscript editing, M.L., Y.Z., Y.C.
Conflicts of interest are listed at the end of this article.
NEURORADIOLOGY: MR Angiography for Aneurysm Detection and Characterization Li et al
Figure 1
Figure 1:  Flowchart of the study. CTA = CT angiography, MRA = MR angiography, Pts = patients, SAH =
subarachnoid hemorrhage.
years) and 56.89 years 6 12.81 (range,
25–84 years), respectively (P , .05).
DSA revealed 265 cerebral aneu-
rysms in 225 of the 277 patients. No
aneurysm was seen in 52 patients.
For analysis of the accuracy of display
of morphologic features, only aneu-
rysms that were true-positive at MR
Radiology: Volume 284: Number 1—July 2017  n  radiology.rsna.org 193
angiography, confirmed with DSA, were
included.
Image Acquisition
MR angiography.—MR angiography
began 50.87 minutes 6 21.48 (range,
20–124 minutes) after completion of the
nonenhanced CT examination. A 3.0-T
system (Achieva X Series; Philips Medi-
cal Systems, Best, the Netherlands) with
a Sense-Head-8 receiver head coil was
used. The 3D TOF MR angiograms were
obtained by using 3D T1-weighted fast
field-echo sequences (repetition time
msec/echo time msec, 35/7; flip angle,
20°; field of view, 250 3 190 3 108; four
slabs [180 sections]; section thickness,
0.8 mm; and matrix, 732 3 1024). Total
acquisition time was 8 minutes 56 sec-
onds. The acquired image data sets were
transferred to an extended workstation
(Philips Medical Systems) and were pro-
cessed to a volume-rendering image at
3D volume inspection. The maximum
intensity projection image was also re-
constructed for the evaluation.
To reduce arterial overlay and for
efficient identification of aneurysms,
we used the single-artery highlighting
method, which is also referred to as
catheter cerebral angiography (6,8).
Thus, for the left or right internal ca-
rotid artery (ICA), we “removed” the
contralateral ICA system together with
the posterior circulation system, and for
the posterior circulation system, we “re-
moved” the anterior circulation system.
We analyzed three vessels in each pa-
tient from six basic views (anteropos-
terior projection, posterior-anterior
projection, bilateral projections, and bi-
lateral oblique projections) and from ar-
bitrary angles to clearly depict the aneu-
rysm origins and morphologic features.
DSA.—DSA was performed 5.53
hours 6 4.98 (range, 1–36 hours) af-
ter MR angiography. Four vessels—the
ICAs and the vertebral arteries on both
sides—were catheterized for DSA. Pos-
teroanterior and lateral projections
were acquired with a biplanar unit
(Artis zee; Siemens Healthcare, Forch-
heim, Germany) with a 1024 3 1024
matrix and a 17–20-cm field of view in
all patients. Rotational angiography was
performed with an 8-second 200-degree
rotational run, acquiring 200 images;
for affected arteries, further 3D images
with volume-rendering reconstruction
were produced on a workstation with a
128 3 128 3 128 to 512 3 512 3 512
matrix (Syngo XWP VA70B; Siemens
Healthcare). Contrast medium (iodixa-
nol; Henrui Medicine, Lianyungang,
NEURORADIOLOGY: MR Angiography for Aneurysm Detection and Characterization Li et al
Jiangsu, China) was injected for a total
of 10 mL for the ICA (rate, 4–5 mL/
sec), 7 mL for the vertebral artery
(rate, 2–3 mL/sec), and 10–15 mL per
artery for rotational angiography (rate,
2–3 mL/sec). Two observers (reviewers
H.T. and H.L., with 17 and 10 years of
experience, respectively, in interven-
tional neuroradiology) evaluated the
cerebral aneurysms together.
Image Review
Three observers (M.L. [observer A],
Y.L. [observer B], and Y.Z. [observer
C], with 20, 9, and 8 years of experi-
ence, respectively, in interventional
neuroradiology) who were blinded to
clinical findings and DSA results inde-
pendently analyzed the 3D TOF MR
angiography with volume-rendering im-
age data sets at an offline workstation
from multiple on-screen viewing angles
by using the single-artery highlighting
approach. The source images and max-
imum intensity projection images were
presented on screen, allowing for ad-
justment of the appropriate threshold
of the window width and window level
to diagnose or differentiate aneurysms
with infundibula. Cases with one or
more aneurysms detected were consid-
ered positive; all others were consid-
ered negative (regardless of other ce-
rebral vascular disease). For analysis of
the morphologic assessment of 3D TOF
MR angiography, the average of the
values of the three reviewers was used
for aneurysm size and neck width. An-
eurysm configuration and relationship
to adjacent arteries were decided by
consensus among the three reviewers.
Definitions
We considered an aneurysm to be a
saccular protrusion from the side wall
or from a bifurcation of the cerebral
arteries, without the artery emerging at
its top. Aneurysm locations were clas-
sified as the ICA, including the poste-
rior communicating artery; the anterior
cerebral artery, including the anterior
communicating artery; the middle cere-
bral artery, including the M1–2 segment;
and the vertebral and basilar arteries,
including the vertebral, basilar, cere-
bellar, and posterior cerebral arteries.
194 radiology.rsna.org  n Radiology: Volume 284: Number 1—July 2017
Aneurysm size and neck width were
recorded as the maximum two-dimen-
sional angiographic dimension. Errors of
less than 15% for maximum aneurysm
size and 10% for aneurysm neck width
was considered acceptable, considering
that measurement was made by using
data from MR angiographic and DSA
sources and by different persons.
An aneurysm was considered giant
if the greatest diameter was 25 mm or
larger, large if it was 10–25 mm, small if
it was 3.0–10 mm, and tiny if it was less
than 3.0 mm. The aneurysm neck was
considered wide if it was larger than
4 mm or if the fundus-to-neck ratio
was smaller than 2. For assessment of
morphologic features of the aneurysm,
three features were considered: the
presence of a daughter sac, the pres-
ence of lobulation, and the margin (9).
A daughter sac was deemed to be pre-
sent if two-dimensional or 3D MR an-
giographic and/or DSA images revealed
an irregular protrusion from the wall of
the aneurysm that was less than 25% of
the total volume of the main sac. Lob-
ulation was defined as a protuberance
arising directly from the primary neck
of the aneurysm or from the main body
and representing 25% or more of the
volume of the main sac. The margin of
the aneurysm was classified as a smooth
or irregular shape. With regard to the
relationship between aneurysm and
parent artery, there were two grades:
(a) aneurysm arising from the side wall
of the artery and (b) aneurysm arising
from an arterial bifurcation. The latter
could be of three types: (a) aneurysm
neck arising from the angle of the bifur-
cation, (b) more than 75% of the aneu-
rysm neck arising from one limb of the
bifurcation, and (c) aneurysm involving
the entire angle of the bifurcation. Pre-
cise morphologic display of the cerebral
aneurysm at 3D TOF MR angiography
was considered a failure if any of the
morphologic parameters—location,
size, neck width, shape, and relation
to adjacent artery—did not conform to
the DSA findings.
Statistical Analysis
Interobserver agreement was expressed
in terms of the Cohen k value for
categoric variables. Patient-by-patient
and aneurysm-by-aneurysm analyses
were performed. The diagnostic perfor-
mance of 3D TOF MR angiography was
summarized in terms of the overall accu-
racy, sensitivity, specificity, positive pre-
dictive value, negative predictive value,
and area under the receiver operating
characteristic curve. For patient-based
evaluation, if a patient had multiple an-
eurysms and one of the aneurysms was
missed or overdiagnosed, this patient
was considered to have false-negative
or false-positive findings. The 95% con-
fidence interval of each index was cal-
culated by using the score confidence
interval (10). Multivariate logistic regres-
sion analysis was performed to identify
the variables that significantly affected
the morphologic assessment with 3D
TOF MR angiography. All analyses were
performed by using statistical software
(SPSS 16.0; SPSS, Chicago, Ill), and P
, .05 was considered to indicate a sig-
nificant difference.
Results
Aneurysm Detection with 3D TOF MR
Angiography
DSA images revealed 265 aneurysms
in 225 patients (87 men [mean age,
57.08 years 6 13.19; range, 25–84
years]; 138 women [mean age, 54.21
years 6 12.25; range, 27–79 years];
P = .10). Altogether, five patients had
three aneurysms each, 30 patients had
two aneurysms each, and 190 patients
had one aneurysm each. In patient-
based evaluations, 3D TOF MR an-
giography yielded accuracy of 96.8%
(268 of 277), sensitivity of 98.2% (219
of 223), specificity of 91% (49 of 54),
positive predictive value of 97.8% (219
of 224), and negative predictive value
of 92% (49 of 53) (mean k = 0.959;
range, 0.951–0.964). In aneurysm-
based evaluations, 3D TOF MR an-
giography yielded accuracy of 96.6%
(309 of 320), sensitivity of 98.1% (260
of 265), specificity of 89% (49 of 55),
positive predictive value of 97.7% (260
of 266), and negative predictive value
of 91% (49 of 54) (mean k = 0.947;
range, 0.932–0.967). On the 3D TOF
NEURORADIOLOGY: MR Angiography for Aneurysm Detection and Characterization Li et al

Table 1
Diagnostic Performance of 3D TOF MR Angiography in Patient- and Aneurysm-based Evaluations

Evaluation and Observer Sensitivity (%)* Specificity (%) PPV (%) NPV (%) Accuracy (%)

Patient-based evaluations†
  Observer A 99.6 [0.976, 0.999] 90.4 [0.794, 0.958] 97.8 [0.950, 0.991] 97.9 [0.891, 0.996] 97.8 [0.953, 0.990]
(224/225) (47/52) (224/229) (47/48) (271/277)
  Observer B 98.7 [0.962, 0.996] 94.2 [0.843, 0.980] 98.7 [0.962, 0.996] 94.2 [0.843, 0.980] 97.8 [0.953, 0.990]
(222/225) (49/52) (222/225) (49/52) (271/277)
  Observer C 99.1 [0.968, 0.998] 94.2 [0.843, 0.980] 98.7 [0.962, 0.996] 96.1 [0.868, 0.989] 98.2 [0.959, 0.992]
(223/225) (49/52) (223/226) (49/51) (272/277)
Aneurysm-based evaluations‡
  Observer A 99.6 [0.979, 0.999] 90.9 [0.804, 0.960] 98.1 [0.957, 0.992] 98.0 [0.896, 0.996] 98.1 [0.959, 0.991]
(264/265) (50/55) (264/269) (50/51) (314/320)
  Observer B 98.9 [0.968, 0.996] 92.7 [0.827, 0.971] 98.5 [0.962, 0.994] 94.4 [0.848, 0.981] 97.8 [0.955, 0.989]
(262/265) (51/55) (262/266) (51/54) (313/320)
  Observer C 98.9 [0.968, 0.996] 94.5 [0.851, 0.981] 98.8 [0.968, 0.996] 94.5 [0.851, 0.981] 98.1 [0.959, 0.991]
(262/265) (52/55) (262/265) (52/55) (314/320)

Note.—Unless otherwise indicated, data in parentheses are raw data. AUC = area under the receiver operating characteristic curve, NPV = negative predictive value, PPV = positive predictive value.
* Data in brackets are 95% confidence intervals.
†
k Values (coefficients of interreader agreement) ranged from 0.951 to 0.964.
‡
k Values (coefficients of interreader agreement) ranged from 0.932 to 0.967.

Table 2 Morphologic Display of Aneurysms at 3D

TOF MR Angiography
Aneurysm-specific Characteristics at 3D TOF MR Angiography and DSA A total of 255 aneurysms in 219 pa-
Aneurysm-specific Characteristics 3D TOF MR Angiography (n = 255) DSA (n = 255) P Value tients, accurately diagnosed with both
3D TOF MR angiography and DSA,
Aneurysm size (mm) .55
were included in the final analysis of
  ,3 44 35
the morphologic assessment of 3D TOF
 3–10 191 199
MR angiography (Table 2). Overall, 132
 10–25 19 20
  .25 1 1
aneurysms were located at the ICA
Aneurysm location ..99 (Fig 2), 71 were located at the anterior
 ICA 132 132 cerebral artery (Fig 3), 27 were located
 ACA/AComA 71 71 at the middle cerebral artery (Fig 4),
 MCA 27 27 and 25 were located at the vertebral
 VBA 25 25 and basilar arteries. The mean maximal
Aneurysm sac shape .54 diameter of the aneurysm sac was 5.01
 Margin 165 154 mm 6 3.34 (range, 1–36 mm). With
 Lobulated 59 63 regard to size, 44 aneurysms were tiny,
  Daughter sac 31 38 191 were small, 19 were large, and one
Aneurysm and side branches .48 was giant. With regard to shape, 165
  Side wall 137 136 aneurysms had smooth margins, 39
  Bifurcation tip 102 109 had lobulation, and 61 had a daughter
  Involves one limb of the bifurcation 11 5 sac at DSA. A total of 137 aneurysms
  Involves entire bifurcation 5 5 arose from the side wall of the artery,
Note.—ACA = anterior cerebral artery, AComA = anterior communicating artery, MCA = middle cerebral artery, VBA = 109 were located at the bifurcation tip,
vertebrobasilar artery. and nine were deviated to one side
or incorporated the entire bifurcation
tip. Three-dimensional TOF MR angio-
MR angiography images, the three ob- had a single false-negative result, and graphic images were within 15% of the
servers diagnosed five, four, and three two observers had three false-negative maximum size as measured at DSA in
false-positive aneurysms. One observer results (Table 1). 92.5% of aneurysms (236 of 255), were

Radiology: Volume 284: Number 1—July 2017  n  radiology.rsna.org 195

NEURORADIOLOGY: MR Angiography for Aneurysm Detection and Characterization Li et al

Figure 2

Figure 2:  A ruptured aneurysm in the C6 segment of the left ICA in a 46-year-old woman. A, Three-dimensional TOF MR angiogram shows a small aneurysm
(arrow) with a daughter sac (arrowhead) at the C6 segment of the left ICA. B, DSA image with volume-rendering reconstruction and, C, two-dimensional DSA image
show the aneurysm (arrow) and its daughter sac (arrowhead) seen at 3D TOF MR angiography with volume-rendering reconstruction. D, DSA image shows total
occlusion of the aneurysm (arrow) after embolization with coils.

Figure 3

Figure 3:  A ruptured aneurysm in the anterior communicating artery in a 41-year-old man. A, Three-dimensional TOF MR angiogram shows a small aneurysm
(arrow) with a lobulated shape arising from the anterior communicating artery. B, DSA image with volume-rendering reconstruction shows the aneurysm (arrow) seen
at 3D TOF MR angiography with volume-rendering reconstruction. C, Two-dimensional DSA image shows an aneurysm (arrow) in the anterior communicating artery.
D, DSA image shows total occlusion of the aneurysm (arrow) after embolization with coils.

within 10% of the neck width as mea-
sured at DSA in 86.3% of aneurysms
(220 of 255), and accurately character-
ized shape in 94.5% aneurysms (241
of 255) and relation to adjacent vessel
in 96.9% aneurysms (247 of 255). For
the 35 aneurysms with incorrectly dis-
played neck size, 94% (33 of 35) were
overestimated. Mean aneurysm neck
width was 3.17 mm 6 2.28 (range,
0.6–33.7 mm) displayed at MR angiog-
raphy versus 2.96 mm 6 2.32 (range,
0.6–35.0 mm) at DSA (P , .01) (Fig 5).
Univariate analysis revealed that an-
eurysm size (odds ratio, 2.050; 95%
confidence interval: 1.062, 3.955; P
= .032) and neck width (odds ratio,
0.378; 95% confidence interval: 0.195,
0.731; P = .004) measurements at 3D
TOF MR angiography were significantly
different from the DSA values. This
analysis indicated that the larger size
of the aneurysm body or smaller aneu-
rysm neck width was associated with
a greater chance of inaccurate display
of the aneurysm morphologic features
at 3D TOF MR angiography. Multiple
logistic regression analysis revealed
that aneurysm neck width (odds ratio,
0.378; 95% confidence interval: 0.195,
0.731; P = .004) was the only variable
associated with the accuracy of mor-
phologic assessment of 3D TOF MR
angiography.
Discussion
The major findings of our study revealed
that 3D TOF MR angiography at 3.0 T
has a sensitivity of more than 95% for
detection of aneurysms in patients with
subarachnoid hemorrhage who have a
Glasgow coma score of 15. In our study
population, the procedure was success-
fully performed in 98.3% of patients.

196 radiology.rsna.org  n Radiology: Volume 284: Number 1—July 2017

NEURORADIOLOGY: MR Angiography for Aneurysm Detection and Characterization Li et al

Figure 4

Figure 4:  A ruptured aneurysm in the M1 segment of the right middle cerebral artery in a 42-year-old man. A, Three-dimensional
TOF MR angiogram shows a small aneurysm (arrow) with an irregular margin at the bifurcation site of the M1 segment of the right
middle cerebral artery. B, DSA image with volume-rendering reconstruction shows the aneurysm (arrow) seen at 3D TOF MR angiogra-
phy with volume-rendering reconstruction. C, Two-dimensional DSA image shows an aneurysm (arrow) in the M1 segment of the right
middle cerebral artery.

Figure 5 locations for the MR angiographic ex-

Figure 5:  Bland-Altman analysis of aneurysm neck size measurements between DSA and MR angiography
(MRA). Numbers of aneurysms with neck measurements greater or lower than those at DSA were counted
separately and are listed in the table below the graph. SD = standard deviation.
Although no rebleeding occurred dur-
ing imaging, symptoms deteriorated
in 12 patients because of rebleeding
while they were waiting or were moving
amination. Moreover, the morphologic
characteristics of aneurysms displayed
at 3D TOF MR angiography had good
concordance with those on conven-
tional angiographic images, indicating
that 3D TOF MR angiography could po-
tentially be used for selection and opti-
mization of the endovascular or surgical
technique to be used.
Conventional angiography is con-
sidered the reference standard in the
diagnostic work-up of patients with
subarachnoid hemorrhage who are
suspected of having aneurysms. CT an-
giography is recommended as the first
option for noninvasive angiography; it
has an accuracy of 94%, sensitivity of
96%, and specificity of 92% for the
detection of cerebral aneurysms (11).
Chen et al (12) found that the accuracy,
sensitivity, and specificity for depict-
ing aneurysms could be increased to
99%, 99%, and 100%, respectively, if
the subtracted volumetric CT angio-
graphic technique is applied. However,
improved image resolution with CT is
at the expense of increased section
numbers and decreased section thick-
ness and, therefore, increased radiation
exposure. MR angiography does not ex-
pose the patient to ionizing radiation
or iodine-based contrast medium and
can thus be repeated if necessary (13).

Radiology: Volume 284: Number 1—July 2017  n  radiology.rsna.org 197

NEURORADIOLOGY: MR Angiography for Aneurysm Detection and Characterization Li et al
Previous studies grouped ruptured and
unruptured aneurysms together when
investigating the diagnostic perfor-
mance of MR angiography. In our study,
we focused on ruptured aneurysms to
clarify the following issues: (a) whether
the diagnostic performance of MR an-
giography is similar to that of DSA, (b)
whether MR angiography is feasible
and safe in patients with subarachnoid
hemorrhage, and (c) whether MR angi-
ography can provide accurate prepro-
cedure geometric information to guide
surgical or endovascular treatment.
The performance of 3D TOF MR an-
giography in the detection of ruptured
aneurysms is likely to be inferior to its
performance in cases of unruptured
aneurysms because hemorrhage in the
subarachnoid space may adversely af-
fect aneurysm display (6,7). However,
we found that 3D TOF MR angiography
had an accuracy of 97.9%, sensitivity of
99.1%, and specificity of 92.9%, which
is similar to the diagnostic performance
of CT angiography for the detection of
ruptured aneurysm (4). More interest-
ingly, we found that with 3D TOF MR
angiography, overdiagnosis is more
likely than missed diagnosis. This may
have been because (a) high spatial and
temporal resolution was achieved with
the application of high-magnetic-field
MR imaging and the previously opti-
mized imaging parameters and (b) 3D
volume-rendering reconstruction and
the single-artery-highlighting approach
greatly reduced the chances of missed
diagnosis. Meanwhile, clear display of
blood flow protrusion within arterial
wall plaque and tortuous appearance
of the initiation part of branches can
mimic an aneurysm sac; infundibula
can also be mistaken for aneurysms at
MR angiography if the vessel emerging
at the apex of the infundibula is not
seen (14).
Data are still not available on the
feasibility and safety of 3D TOF MR
angiography in cases of ruptured an-
eurysms. Whether it can increase the
risk for hemorrhage is a crucial issue to
be considered before its application. In
our 3D TOF MR angiographic protocol,
the imaging time was approximately 9
minutes; this is why we included only
198 radiology.rsna.org  n Radiology: Volume 284: Number 1—July 2017
awake patients (Glasgow coma score of
15) who could fully cooperate during
the examination. Despite this, imaging
attempts for the second examination
failed in five patients; these patients
were excluded from the study because
of safety concerns.
Previous CT angiographic or MR
angiographic studies were usually per-
formed only for detection of aneu-
rysms. However, with superior spatial
resolution and better visualization of
distal vessels by using 3.0-T MR imag-
ing, detailed and reliable information
on the morphologic features of an an-
eurysm can be obtained, which can be
useful for treatment planning (15,16).
In the case of a ruptured aneurysm, the
display of a daughter sac or lobulation
can help locate the hemorrhage site,
accurate display of the aneurysm neck
can help plan endovascular remodeling
or clipping techniques, and accurate
display of the relationship between the
aneurysm sac and the adjacent artery
can help to evaluate ischemia risk dur-
ing coiling or clipping. Aneurysm neck
was found to be the only parameter that
could not be accurately assessed with
3D TOF MR angiography according to
multivariate logistic regression analysis.
This is probably because measurement
of data from different sources will be
associated with some degree of error. It
is also possible that when the aneurysm
sac tightly touches the parent artery, a
false appearance of a wide-necked an-
eurysm can be created because of the
limited resolution of 3D TOF MR angi-
ography. This is also a probable reason
for why neck width measurements at
3D TOF MR angiography were mostly
greater than those at DSA in our study.
Our study had limitations. This was
a single-center experience, and recruit-
ment was probably biased because in-
formed consent was obtained after non-
enhanced CT. Moreover, considering
that a large proportion of patients who
present with subarachnoid hemorrhage
will not be awake or will not be able to
hold still to undergo good-quality MR
angiography, CT angiography remains
the first-line noninvasive examination
for this patient population. The risk of
waiting for the MR imaging examination
must also be considered in these pa-
tients; during our study, the condition
of 12 patients decompensated during
this time period, and they proceeded
to surgery instead of imaging, and an
additional five patients were unable to
complete the MR imaging examination.
In conclusion, 3D TOF MR angiog-
raphy has high diagnostic accuracy in
the detection of ruptured cerebral an-
eurysms in selected patients with sub-
arachnoid hemorrhage (stable Glasgow
coma score of 15), and its accuracy
in displaying the morphologic features
of aneurysms appears to be similar to
that of DSA. We recommend the use
of 3D TOF MR angiography as a tool
for screening for ruptured cerebral an-
eurysm and for treatment planning be-
cause of its noninvasive nature and its
high accuracy and sensitivity.
Disclosures of Conflicts of Interest: M.L. dis-
closed no relevant relationships. Y.Z. disclosed
no relevant relationships. H.S. disclosed no rele-
vant relationships. B.G. disclosed no relevant re-
lationships. H.L. disclosed no relevant relation-
ships. Y.L. disclosed no relevant relationships.
H.T. disclosed no relevant relationships. Y.C.
disclosed no relevant relationships.
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