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ORIGINAL RESEARCH
INTERVENTIONAL
Subarachnoid Hyperattenuation on Flat Panel Detector–Based
Conebeam CT Immediately after Uneventful Coil Embolization
of Unruptured Intracranial Aneurysms
Y. Shinohara, M. Sakamoto, H. Takeuchi, T. Uno, T. Watanabe, T. Kaminou, and T. Ogawa
ABSTRACT
BACKGROUND AND PURPOSE: Flat panel detector– based CBCT can provide CT-like images of the brain without transferring patients
from the angiography suite to a conventional CT facility. Conventional brain CT after uneventful endovascular treatment sometimes
shows focal subarachnoid hyperattenuation with contrast leakage, mimicking SAH. Differentiating this finding from SAH is important for
immediate postprocedural medical management. We investigated CBCT for detecting subarachnoid hyperattenuation immediately after
coil embolization of unruptured cerebral aneurysms.
MATERIALS AND METHODS: Thirty-six patients with unruptured cerebral aneurysms undergoing CBCT immediately after uncomplicated
coil embolization were included. The relationship between the presence of subarachnoid hyperattenuation and total volume of contrast
medium injected, aneurysm size and location, and balloon and stent assistance during embolization was investigated. Statistical analyses
were performed with the
2
test (P⬍.05).
RESULTS: Nine of the 36 patients (25.0%) showed focal subarachnoid hyperattenuation within the relevant parent artery territory
harboring the aneurysm. Subarachnoid hyperattenuation locations included the ipsilateral superior frontal sulcus (n⫽5), the bilateral
superior frontal sulcus (n⫽1), and the ipsilateral superior frontal and precentral sulci (n⫽3). Statistically significant differences were
observed between the presence of a subarachnoid hyperattenuation and the total volume of contrast medium injected (P⬍.001) and
aneurysm size (P⬍.05).
CONCLUSIONS: Subarachnoid hyperattenuation can be detected by CBCT immediately after coil embolization for unruptured aneu-
rysms. The increased amounts of contrast medium to be given before CBCT and the specific location of the hyperattenuation may help
differentiate benign subarachnoid contrast leakage from SAH.
ABBREVIATIONS: ACA ⫽anterior cerebral artery; AcomA ⫽anterior communicating artery; CBCT ⫽conebeam CT; FPD ⫽flat panel detector; VB ⫽vertebro-
basilar artery
A
dvances in FPD-equipped angiographic technology have re-
sulted in its increasing use for neuroendovascular treatment.
FPD-based CBCT is a 3D imaging tool for the reconstruction of
projection data with a rotational C-arm with an FPD. With this
technique, CT-like images of the brain parenchyma can be ob-
tained without transferring patients from the angiography suite to
a conventional CT facility.
1-7
Therefore, unpredictable complica-
tions, such as intracerebral hematoma and SAH, can be rapidly
detected with CBCT during or immediately after a neuroendovas-
cular procedure.
4-6
Previous reports suggest that conventional noncontrast CT of
the brain sometimes shows subarachnoid hyperattenuation that
mimics SAH after uneventful endovascular treatment for cerebral
aneurysms. This subarachnoid hyperattenuation is presumably
due to the transient impairment of the CSF barrier or a change in
vascular permeability by nonionic iodinated contrast medi-
um.
8-12
Although this radiologic finding is a clinically benign one
after neuroendovascular procedures, it is important to differenti-
ate it from SAH, which requires significant immediate postproce-
dural medical management, including the use of anticoagulants
and antiplatelet agents.
There are relatively few systematic evaluations of sub-
arachnoid hyperattenuation on conventional CT following
uncomplicated coil embolization of unruptured intracranial an-
eurysms.
10-12
Moreover, as far as we know, there are no reports
Received March 29, 2012; accepted after revision May 31.
From the Division of Radiology (Y.S., T.K., T.O.), Department of Pathophysiological
Therapeutic Science, and Division of Neurosurgery (M.S., T.U., T.W.), Department
of Brain and Neurosciences, Faculty of Medicine, Tottori University, Yonago, Japan;
and Department of Neurosurgery (H.T.), Nojima Hospital, Kurayoshi, Japan.
Address correspondence to: Yuki Shinohara, MD, Division of Radiology, Depart-
ment of Pathophysiological Therapeutic Science, Faculty of Medicine, Tottori Uni-
versity, 36-1 Nishi-cho, Yonago 683-8504, Japan; e-mail: shino-y@olive.plala.or.jp
http://dx.doi.org/10.3174/ajnr.A3243
AJNR Am J Neuroradiol 34:577– 82 Mar 2013 www.ajnr.org 577
describing subarachnoid hyperattenuation on postprocedural
CBCT. Although contrast resolution of CBCT is still considered
inferior to that in conventional CT, current CBCT provides an
almost CT-like contrast resolution, allowing differentiation
between gray and white matter and detection of ventricles and
intracerebral hemorrhages.
5,13
The goal of this study was to inves-
tigate the ability of CBCT to detect subarachnoid hyperattenua-
tion immediately after coil embolization of unruptured intracra-
nial aneurysms.
MATERIALS AND METHODS
Patients
This retrospective study analyzed data obtained from all patients
with unruptured intracranial aneurysms admitted to our institu-
tion between May 1, 2010, and March 23, 2012. Patients with
uncomplicated endovascular coil embolization for an unruptured
intracranial aneurysm who underwent FPD-based CBCT imme-
diately after embolization were eligible if they had no acute cere-
brovascular disease, including intracerebral hematoma, SAH, or
infarction on pretreatment CT or MR images and if they under-
went intracranial MR imaging, including DWI, T2*-weighted im-
aging, and FLAIR imaging, within 1 week after treatment. Our
study was approved by our institutional review board, and in-
formed consent for endovascular treatment and imaging exami-
nations was obtained from each patient.
Endovascular Procedures
Endovascular procedures were performed with the patient under
general anesthesia. All patients were given intravenous heparin
for systemic anticoagulation to maintain an activated clotting
time at twice the normal value during catheterization and coil
placement. A 5F or 6F guiding catheter was placed in the internal
carotid or vertebral artery via a unilateral or bilateral transfemoral
approach. HyperGlide (ev3, Irvine, California) and HyperForm
(ev3) balloons were used for balloon-assisted procedures, and in-
tracranial stents (Enterprise Vascular Reconstruction Device;
Codman Neurovascular, Miami Lakes, Florida) were used for
stent-assisted procedures. Nonionic water-soluble iodinated con-
trast medium (iohexol, Omnipaque 300; Daiichi-Sankyo, Tokyo,
Japan) was used. After embolization, conventional 2D DSA and
3D rotational DSA were performed to check the status of the
treated aneurysm and parent artery.
Imaging Examinations
CBCT was performed by using a biplane FPD angiography system
with 3D rotational capability (Allura Xper 20/10; Philips Health-
care, Best, the Netherlands or Axiom Artis dBA; Siemens, Erlan-
gen, Germany) after 3D rotational DSA. We did not give addi-
tional contrast medium to perform CBCT. CBCT data were
acquired by using the following parameters: Allura Xper 20/10:
acquisition time, 20 seconds; tube voltage, 120 kV; projection
matrix, 1024 ⫻1024; rotation angle, 210°; total frames, 620; dose,
0.9
Gy/pulse; Axiom Artis dBA: acquisition time, 20 seconds;
tube voltage, 70 kV; projection matrix, 1024 ⫻1024; rotation
angle, 217°; total frames, 543; dose, 1.2
Gy/pulse. Postprocessing
of the CBCT dataset was performed on a commercially available
dedicated workstation (XtraVision; Philips Healthcare or
X-Leonardo; Siemens). Postprocessing resulted in a volume data-
set with a 0.98-mm thickness in a 256 ⫻256 matrix format for
XtraVision and a 0.47-mm thickness in a 512 ⫻512 matrix format
for X-Leonardo. Reconstructions were performed by using the
soft-tissue algorithm for XtraVision and kernel-type Hounsfield
units with image-characteristics “normal” for X-Leonardo. The
dataset was then further processed as multiplanar reconstructions
with 5.0-mm section thicknesses. Images were viewed in axial and
coronal orientations.
Follow-up MR imaging examinations were performed within
1 week after endovascular therapy by using 3T (Signa Excite HD;
GE Healthcare, Milwaukee, Wisconsin). The following sequences
were included in the protocol of these studies: DWI: TR/TE/excita-
tion, 6000/65.6 –71 ms/1; flip angle, 90°; section thickness/inter-
section gap, 5/1.5 mm; FOV, 21 cm; matrix size, 512 ⫻512; two
b-values of 0 and 1000 s/mm
2
; T2*-weighted imaging: TR/TE/
excitation, 750 – 850/20 –30 ms/1; section thickness/intersection
gap, 5/1.5 mm; FOV, 23 cm; matrix size, 512 ⫻512; FLAIR imag-
ing: TR/TE, 10,002/116 ms; section thickness/intersection gap,
5/1.5 mm; FOV, 21 cm; matrix size, 512 ⫻512.
Data Analysis
CBCT images obtained immediately after embolization were eval-
uated for any abnormal findings associated with the procedures,
such as SAH, intracerebral hematoma, and large infarctions. Sub-
arachnoid hyperattenuation was regarded as the presence of focal
hyperattenuation in the sulci according to the territory of the
parent artery harboring the aneurysm and no evidence of SAH on
follow-up MR images. Images of all patients were retrospectively
reviewed by 2 neuroradiologists (Y.S. and T.O.), who reached
consensus regarding image interpretation. The neuroradiologists
were not blinded to the location of the treated aneurysm in each
case.
Relationship between each parameter and subarachnoid
hyperattenuation on FPD-based CBCT immediately after coil
embolization
Parameter
Subarachnoid
Hyperattenuation P
Value+−
Location of aneurysm
ICA 4 19 .0728
MCA 0 2
AcomA 3 3
ACA 2 0
VB 0 3
Size of aneurysm (mm)
⬍5012⬍.05
5–10 4 13
10–15 1 0
ⱖ15 4 2
Amount of contrast medium (mL)
⬍150 0 17 ⬍.001
150–250 4 8
ⱖ250 5 2
Balloon assistance
Performed 3 12 .567
Not performed 6 15
Stent assistance
Performed 4 5 .150
Not performed 5 22
Note:—⫹indicates presence; ⫺, absence.
578 Shinohara Mar 2013 www.ajnr.org
In addition, the relationship between subarachnoid hyperat-
tenuation on CBCT and several parameters, including the loca-
tion and size of the aneurysm, total volume of contrast medium
injected, and use of balloon or stent assistance during emboliza-
tion, was investigated. Aneurysm size was classified into 4 groups:
⬍5 mm, 5–10 mm, 10 –15 mm, and ⱖ15 mm. The amount of
contrast medium was also classified into 3 groups: ⬍150 mL,
150 –250 mL, and ⱖ250 mL. Statistical analyses were performed
by using the
2
test. P⬍.05 was considered significant.
RESULTS
Thirty-six patients (27 women and 9 men; mean age, 62.3 ⫾10.4
years; range, 41– 83 years) were included in this study. According
to the relevant artery territory, the location of the aneurysms was
the ICA in 23 patients, MCA in 2 patients, AcomA in 6 patients,
ACA in 2 patients (the horizontal segment of the right ACA in 1
patient and the precallosal segment of the right ACA in the other),
and the VB in 3 patients. The diameters of the aneurysms were ⬍5
mm in 12 patients, 5–10 mm in 17 patients, 10 –15 mm in 1 pa-
tient, and ⱖ15 mm in 6 patients. The amounts of contrast me-
dium were ⬍150 mL in 17 patients, 150 –250 mL in 12 patients,
and ⱖ250 mL in 7 patients. Fifteen patients were treated with
balloon assistance, and 9 patients were treated with stent
assistance.
On immediate postembolization CBCT, 9 of 36 patients
(25.0%) showed focal subarachnoid hyperattenuation within the
relevant parent artery territory harboring the treated aneurysm.
The location of the subarachnoid hyperattenuation was the ipsi-
lateral superior frontal sulcus in 5 patients (Fig 1), the bilateral
superior frontal sulci in 1 patient (Fig 2), and the ipsilateral supe-
rior frontal sulcus and precentral sulcus in 3 patients. Although
we could not evaluate the presence of subarachnoid hyperattenu-
ation adjacent to the coiled aneurysm on CBCT due to metallic
artifacts, there was no evidence of subarachnoid hyperattenuation
or SAH in the basal cistern or Sylvian fissure around the metallic
artifacts.
Subarachnoid hemorrhage was not found on postprocedural
MR imaging, which was performed after 110 minutes in 1 patient,
2 days in 2 patients, 3 days in 1 patient, 4 days in 2 patients, and 5
FIG 1. A 63-year-old man with an unruptured 6-mm AcomA complex aneurysm. The patient underwent endovascular embolization for the
aneurysm with the guiding catheter in the left ICA. The aneurysm was coiled with balloon assistance. The total volume of contrast medium
injected was approximately 300 mL. A, DSA after embolization reveals coil mesh in the left A1-A2 bifurcation (black arrow ). B, CBCT immediately
after the procedure shows focal subarachnoid hyperattenuation in the left superior frontal sulcus (white arrow ). C, Conventional CT 45 minutes
after the procedure also shows focal subarachnoid hyperattenuation in the left superior frontal sulcus (white arrow ). D, DWI reveals no
abnormal high-intensity area indicating acute infarction. E, FLAIR imaging shows no high signal intensity in the sulci indicating SAH. F, T2*-
weighted imaging demonstrates no low signal intensity in the sulci indicating SAH. These MR images were obtained 111 minutes after the
procedure.
AJNR Am J Neuroradiol 34:577– 82 Mar 2013 www.ajnr.org 579
days in 3 patients after coil embolization in these 9 patients. Sta-
tistically significant differences were observed between the pres-
ence of subarachnoid hyperattenuation and the total volume of
contrast medium injected (P⬍.001) and the size of the aneurysm
(P⬍.05). On the other hand, the location of the aneurysm, bal-
loon inflation, and stent assistance were not significantly related
to the presence of subarachnoid hyperattenuation (P⫽.0728,
.567, and .150, respectively).
DISCUSSION
Endovascular coil embolization for unruptured intracranial an-
eurysms has been increasingly used in recent years. Although the
safety and efficacy of this technique are now well-documented,
intraprocedural complications such as aneurysmal rupture,
thromboembolic events, and vasospasms can occur.
4-6
It is im-
portant for the endovascular therapist to recognize and manage
these serious complications as early as possible because a favor-
able clinical outcome can be expected if appropriate treatment is
initiated within 30 minutes.
14
From this point of view, CBCT
immediately after embolization can be used to rule out unpredict-
able intracranial complications without the need to transport the
patient to a conventional CT facility.
Relatively few systematic evaluations of conventional CT find-
ings after coil embolization for intracranial aneurysm have been
reported.
10-12
In a study, Baik et al
11
found a focal subarachnoid
hyperattenuation in 8 of 61 (13%) conventional CT scans after
uneventful endovascular treatment. Subarachnoid hyperattenua-
tion may indicate transient contrast leakage into the subarach-
noid space, resulting from temporary disruption of the blood-
CSF interface by repeated contrast medium injection into a single
vessel.
8-12
To the best of our knowledge, there are no reports describing
subarachnoid hyperattenuation on postprocedural noncontrast
CBCT. CBCT immediately after endovascular treatment in our
study showed more frequent focal subarachnoid hyperattenua-
tion (9 of 36 CBCT scans, 25.0%) compared with that shown by
conventional CT in the previous report.
11
Ozturk et al
10
described
a significant inverse relationship between the occurrence of this
finding and the elapsed time until the initial posttreatment con-
FIG 2. A 42-year-old woman with an unruptured 7-mm AcomA aneurysm. The patient underwent endovascular embolization for the aneurysm
with the guiding catheter in the left ICA. The aneurysm was coiled with balloon assistance. The total volume of contrast medium injected was
approximately 250 mL. A, Postembolization DSA of the left ICA injection reveals coil mesh in the AcomA region (black arrow ). Notice that the
bilateral distal ACA is symmetrically visualized, presumably due to the hypoplastic right A1 segment. Band C, Axial and coronal CBCT scans,
respectively, immediately after the procedure show focal subarachnoid hyperattenuation in the bilateral superior frontal sulci (black arrows ).
D, DWI reveals no abnormal high-intensity area indicating acute infarction. E, FLAIR imaging shows no high signal intensity in the sulci indicating
SAH. F, T2*-weighted imaging demonstrates no low signal intensity in the sulci indicating SAH. These MR images were obtained 2 days after the
procedure.
580 Shinohara Mar 2013 www.ajnr.org
ventional CT was performed; in other words, the more time
elapsed, the less frequently those findings were observed. The re-
sult of our study is consistent with their description. Thus, the
most likely reason for a high frequency of observed subarachnoid
hyperattenuation is the very short interval between the end of the
treatment and the CBCT scan, which was not enough time to
wash out excessive iodine from the subarachnoid space. In addi-
tion, Baik et al
11
reported that the attenuation of subarachnoid
contrast leakage after embolization was higher than that of the
usual SAH. Hyperattenuation of contrast medium itself may lead
to the detectability of subarachnoid hyperattenuation on CBCT
after embolization, though the contrast resolution of CBCT is
considered to be inferior to that of conventional CT.
4,5,15
In our study, CBCT showed subarachnoid hyperattenuation
only at the superior frontal sulcus with or without involvement of
the precentral sulcus. No previous study has performed a com-
prehensive investigation of the location of subarachnoid hyperat-
tenuation, to our knowledge. Because all patients with subarach-
noid hyperattenuation received aneurysm coil embolization in
the anterior circulation, the contrast medium was mostly injected
from the ICA and therefore may have tended to accumulate in the
anterior watershed or ACA-MCA borderzone territory. Although
the number of patients with an aneurysm in the posterior circu-
lation in this study was small and focal subarachnoid hyperat-
tenuation was not detected in the posterior circulation territory,
focal subarachnoid hyperattenuation in the posterior watershed
territory or posterior fossa should also be visible on postproce-
dural CBCT if the contrast medium is injected repeatedly from
the vertebral artery. Thus, the specific location of subarachnoid
hyperattenuation (eg, the watershed area within the relevant par-
ent artery territory) may be an important clue for differentiation
between benign contrast leakage and SAH.
Previous studies have described several patterns of postproce-
dural conventional CT findings, such as cortical, striatal, and in-
traventricular hyperattenuation as well as subarachnoid hyperat-
tenuation, which showed either a single or a mixed pattern. In
particular, cortical hyperattenuation was more frequent than the
other findings.
10-12
However, apparent cortical hyperattenuation
in addition to subarachnoid hyperattenuation was not found on
CBCT in this study. The image quality of CBCT, especially regard-
ing the contrast resolution and generated image artifacts, may
influence the visualization of the brain parenchyma, resulting in
difficulty distinguishing cortical hyperattenuation due to contrast
leakage from the normal attenuation of the cerebral cortex.
5,15
In this study, we observed a statistical relationship between the
amount of contrast medium injected and the occurrence of sub-
arachnoid hyperattenuation, as previously reported.
10-12
The blood-
CSF or blood-brain interface, which is impermeable to contrast
medium under normal conditions, can be injured by the hyper-
viscosity, hyperosmolarity, and chemotoxicity of the contrast me-
dium when contrast is repeatedly injected into a single artery.
8-12
However, a statistically significant relationship was not found be-
tween the use of balloon or stent assistance and the presence of
subarachnoid hyperattenuation on CBCT. Ozturk et al
10
reported
that cortical hyperattenuation on postprocedural conventional
CT is related to the number of inflations or total inflation time in
procedures requiring balloon assistance, likely because vascular
permeability increases due to temporary ischemia induced by fre-
quent balloon inflation. No previous study has examined the re-
lationship between stent assistance and the occurrence of sub-
arachnoid hyperattenuation, to our knowledge. In this study, the
stent-assisted technique did not always require increased injec-
tion of contrast medium and it did not always induce transient
ischemia, which are factors related to subarachnoid contrast leak-
age. Further studies in larger groups of patients are needed to
determine the effect of stent assistance and balloon assistance in
this phenomenon.
One of the limitations of this study is that because of the ret-
rospective study design, not all patients underwent immediate
postprocedural conventional CT or MR imaging and no patients
underwent lumbar CSF drainage after endovascular treatment to
definitively exclude SAH. From our study, however, it seems that
we can distinguish SAH from benign subarachnoid hyperattenu-
ation by the location of subarachnoid hyperattenuation and the
amount of contrast medium injected.
CONCLUSIONS
Subarachnoid hyperattenuation due to contrast leakage can
be detected by noncontrast CBCT immediately after coil emboli-
zation for unruptured aneurysms. It is important to recognize
subarachnoid hyperattenuation because it mimics SAH, which
requires significant immediate postprocedural medical manage-
ment. Greater amounts of contrast medium given before CBCT
and the specific location of subarachnoid hyperattenuation may
help differentiate clinically benign focal subarachnoid hyperat-
tenuation due to contrast leakage from SAH.
ACKNOWLEDGMENTS
We thank Naoki Iwata of the Division of Clinical Radiology, Tot-
tori University Hospital, who provided support with regard to the
technical terms related to the scanning system.
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