Neurosurg Rev
DOI 10.1007/s10143-017-0911-3
ORIGINAL ARTICLE
High-flow bypass with radial artery graft followed by internal
carotid artery ligation for large or giant aneurysms of cavernous
or cervical portion: clinical results and cognitive performance
Hideaki Ono 1 & Tomohiro Inoue 2 & Takeo Tanishima 1 & Akira Tamura 1 & Isamu Saito 1 &
Nobuhito Saito 3
Received: 22 August 2017 / Revised: 18 September 2017 / Accepted: 20 September 2017
# Springer-Verlag GmbH Germany 2017
Abstract High-flow bypass followed by ligation of the inter-
nal carotid artery (ICA) is an effective treatment, but the im-
pact of abrupt occlusion of the ICA is unpredictable, especial-
ly on postoperative cognitive function. The present study eval-
uated the clinical results as well as cognitive performances
after high-flow bypass using radial artery graft (RAG) with
supportive superficial temporal artery (STA)-middle cerebral
artery (MCA) bypass, followed by ICA ligation. Ten consec-
utive patients underwent high-flow bypass surgery for large or
giant ICA aneurysms of cavernous or cervical portion.
Demographics, clinical information, magnetic resonance
(MR) imaging, computed tomography, digital subtraction an-
giography (DSA), intraoperative somatosensory evoked po-
tentials, neuropsychological examinations including the
Wechsler Adult Intelligence Scale-Third Edition and the
Wechsler Memory Scale-Revised (WMS-R), and follow-up
data were analyzed. The aneurysm was located on the cavern-
ous segment in eight cases and cervical segment in two cases,
and mean aneurysm size was 27.9 mm. Postoperative DSA
demonstrated robust bypass flow from the external carotid
artery to MCA via the RAG, and no anterograde flow into
the aneurysm. No patient showed new symptoms after the
operation. Follow-up clinical study and MR imaging were
performed in nine patients and showed no additional ischemic
* Hideaki Ono
hideono-tky@umin.ac.jp
1
Department of Neurosurgery, Fuji Brain Institute and Hospital,
270-12 Sugita, Fujinomiya, Shizuoka 418-0021, Japan
2
Department of Neurosurgery, NTT Medical Center Tokyo,
Tokyo, Japan
3
Department of Neurosurgery, The University of Tokyo Hospital,
Tokyo, Japan
lesion compared with preoperative imaging. Seven patients
completed neuropsychological examinations before and after
surgery. All postoperative scores except WMS-R composite
memory score slightly improved. High-flow bypass followed
by ICA ligation can achieve good clinical outcomes.
Successful high-flow bypass using RAG with supportive
STA-MCA bypass and ICA ligation does not adversely affect
postoperative cognitive function.
Keywords Giant aneurysm . Large aneurysm . Internal
carotid artery aneurysm . Neurocognitive function . High-flow
bypass . Internal carotid artery ligation
Introduction
Small cavernous carotid aneurysms rarely rupture and may be
considered benign, whereas large or giant aneurysms exert a
mass effect causing symptoms such as ophthalmoplegia
which rarely improve without treatment [1]. Giant or large
internal carotid artery (ICA) aneurysms of cervical portion
may undergo progressive enlargement resulting in devastating
sequela with possible rupture, lower cranial nerve injury, and
intracranial embolic spray from intra-aneurysmal thrombi [2].
Treatment of such aneurysms is still challenging, but high-
flow bypass followed by ligation of the ICA is one of the
effective treatment options.
High-flow bypass using radial artery graft (RAG) is a
promising method to replace the sacrificed ICA [3].
Recently, high-flow bypass has become relatively safe with
good long-term graft patency rates and acceptable morbidity
and mortality rates [3–5], but remains technically complex. In
addition, complications such as ischemic stroke and cortical
laminar necrosis may occur due to reperfusion injury after
temporary occlusion during bypass anastomosis [6, 7]. The

high-flow bypass can replace the blood supply from the ICA,
but the impact of abrupt occlusion of the ICA cannot be pre-
dicted, especially on postoperative cognitive function.
The present study evaluated the clinical results as well as
cognitive performances after high-flow bypass using RAG
with supportive superficial temporal artery (STA)-middle ce-
rebral artery (MCA) bypass, followed by ICA ligation.
Materials and methods
This retrospective study was approved by the institutional
review board at Fuji Brain Institute and Hospital, and all pa-
tients provided informed consent before inclusion in the study.
In total, 10 consecutive patients underwent high-flow bypass
surgery for large or giant ICA aneurysms of cavernous or
cervical portion between June 2007 and June 2016. Some
aspects of three of the patients have been previously reported
[2, 8]. The surgical risk was explained to the patients based on
a surgical mortality rate of less than 1% and a surgical mor-
bidity rate of less than 3% at our institution from October 2006
to May 2007.
High-flow bypass followed by cervical ICA ligation was
performed [8]. All patients began to take aspirin 100 mg daily
1 week before the procedure. Under general anesthesia, so-
matosensory evoked potentials (SSEPs) were recorded using a
commercially available device. SSEP responses were moni-
tored to contralateral median nerve stimulation at the elbow.
After exposure of the cervical carotid bifurcation, a curvilinear
frontotemporal skin incision was made, and the STA was me-
ticulously prepared under the operating microscope. The RAG
was harvested concurrently by another neurosurgeon.
Frontotemporal craniotomy was performed, and a
subzygomatic tunnel was made for the RAG. The sylvian
fissure was split under the operating microscope and the M2
and M3 segments of the MCA were exposed. First, a support-
ive STA-M3 bypass was made distal to the M2 segment for
RAG anastomosis. Then, the harvested RAG was gently
pulled through the subzygomatic tunnel [8, 9]. The distal
end of the RAG was anastomosed to the M2 of the MCA
which is proximal to the site of STA-M3 anastomosis, and
the proximal end was anastomosed to the external carotid
artery (ECA). The area distal to the anastomosis site was per-
fused through the STA-M3 bypass during RAG-MCA anas-
tomosis, and the cerebral hemisphere was perfused by blood
flow from the ICA during RAG-ECA anastomosis. Therefore,
the entire cerebrum was perfused during both RAG-MCA and
RAG-ECA anastomoses. Then, the cervical ICA was tempo-
rarily clamped, and patency of the high-flow bypass was con-
firmed by microvascular Doppler flowmetry. After confirming
that the SSEPs remained stable over 20 min, the cervical ICA
was ligated. Additional ligation of the ICA at the distal end of
the aneurysm was conducted for aneurysms of the cervical
Neurosurg Rev
ICA. All surgical procedures were performed or supervised
by the senior neurosurgeon (T.I.)
Preoperative aneurysm size was measured as the maximum
diameter on T2-weighted magnetic resonance (MR) imaging
(T2WI). Pre-existing multiple ischemic lesions and lacunar
regions were also assessed as representative of previous ische-
mic cerebrovascular disease on preoperative T2WI.
Intramural thrombus was evaluated with computed tomogra-
phy (CT). Collateral status was evaluated in detail with digital
subtraction angiography (DSA). Collateral flow through the
anterior communicating artery was evaluated by contralateral
carotid injection during ipsilateral manual compression of the
common carotid artery (CCA) (Matas study). Collateral flow
through the posterior communicating artery was evaluated by
vertebral injection during ipsilateral manual compression of
the CCA (Allcock study). Collateral flow was judged as ro-
bust with symmetrical/synchronous opacification of the ipsi-
lateral MCA area compared to the contralateral MCA area
during the Matas study or the posterior cerebral artery during
the Allcock study. Collateral status was judged as fair with
delayed/faint opacification of the ipsilateral MCA compared
to the contralateral MCA/posterior cerebral artery during the
Matas/Allcock study. Collateral status was judged as poor
with absence of opacification during either by the Matas or
Allcock study.
Ischemic impact during surgery was defined as consider-
able with a 50% or greater decrease in SSEP N20-P25 ampli-
tude compared with the steady state control value [10].
Occlusion time of each bypass was measured in minutes,
rounded up at 30 s. MCA occlusion time was defined as the
time of STA-MCA bypass, except for one case in which STA-
MCA bypass was not performed due to burn scar of the scalp.
In that case, MCA occlusion time was defined as the time of
RAG-MCA bypass.
Postoperative serial CT evaluations (including on postop-
erative day 1) were performed in all cases. Postoperative
diffusion-weighted MR imaging (DWI), T2WI, and MR an-
giography were performed on postoperative day 1. DSA for
assessment of bypass function and flow to the aneurysm was
performed approximately 1 week postoperatively in patients
with normal renal function. Bypass patency was defined as
Brobust^ with detectable retrograde bypass flow into the
MCA area.
Follow-up MR imaging study was performed in most pa-
tients at about 6 months after surgery. Bypass patency was
defined as Brobust^ with detectable flow into the MCA area
through the bypass. Any T2WI changes, such as slight
perifocal atrophy related to surgical manipulation, were doc-
umented on the medical record.
Neuropsychological examinations were performed with
the Japanese version of the Wechsler Adult Intelligence
Scale-Third Edition [11] (WAIS-III) and Wechsler Memory
Scale-Revised [12] (WMS-R) by experienced speech
Neurosurg Rev

therapists or by psychotherapists. These evaluators were Table 1 Patient characteristics and variables
aware of the fact that the patients had undergone high-flow Mean age in years, mean ± SD 65.9 ± 5.1
bypass surgery but were unaware of the postoperative clinical Female sex 8 (80)
course and the findings of preoperative and postoperative CT Presenting symptom
and MR imaging. Verbal (VIQ) and performance intelligence Ophthalmoplegia 7 (70)
quotients (PIQ) were obtained from the WAIS-III. Composite Enlarging cervical mass 2 (20)
memory score and attention/concentration score were obtain-
Pituitary dysfunction 1 (10)
ed from the WMS-R. Averages of these four scores were also
Aneurysm location
calculated. The upper limit of age is 74 years to convert scores
Cavernous 8 (80)
of subtests into age-matched standardized scores in the WMS-
Cervical 2 (20)
R. Therefore, the scores of subtests of each patient older than
Left side 7 (70)
75 years were converted into standardized scores using the
Aneurysm size in mm, mean ± SD 27.9 ± 10.0
conversion table for the 70- to 74-year-old age group that is
Intraluminal thrombus 4 (40)
derived from the general population. Preoperative neuropsy-
Hypertension 7 (70)
chological examinations were performed within 1 week be-
Diabetes 0 (0)
fore the surgery, and postoperative examinations performed
Dyslipidemia 5 (50)
approximately 6 months after the surgery.
Smoking history 2 (20)
Demographics, clinical information, MR imaging, CT,
Pre-existing white matter change on T2WI 6 (60)
DSA, SSEPs, neuropsychological examination, and follow-
Collateral flow
up findings were analyzed. The study tried to determine the
net result of various factors associated with high-flow bypass Robust 5 (50)
followed by ICA ligation at 6 months postoperatively using Fair 3 (30)
group rate analysis. The Wilcoxon signed rank test was used Poor 2 (20)
to analyze differences in the four neuropsychological scores SSEP amplitude decline > 50% 1 (10)
(VIQ, PIQ, composite memory score, and attention/ MCA occlusion time in min, mean ± SD 23 ± 5
concentration score), and average of the four scores. Two- Postoperative ischemic lesion on DWI 0 (0)
sided p values of less than 0.05 were considered significant. Postoperative DSA
Statistical analysis was performed using JMP Pro version 11.0 Robust bypass flow 10 (100)
(SAS Institute, Inc., Cary, NC). Anterograde flow into aneurysm 0 (0)
T2WI at 6 months after operation (n = 9)
Robust bypass flow 9 (100)
Results Postoperative change 0 (0)

Values are n (%) unless otherwise stated

Patient characteristics and variables are shown in Table 1, and
preoperative demographics are shown in Table 2. A total of 10
patients, 8 women and 2 men (mean age 65.9 years), underwent
high-flow bypass followed by ICA ligation for large or giant
ICA aneurysms of cavernous or cervical portion. Illustrations
of a representative case (case no. 8 in Tables 2 and 3) are shown
in Figs. 1, 2, 3, and 4. Seven patients had hypertension, 5 had
dyslipidemia, 2 had smoking history, and none had diabetes
mellitus (Table 1). The aneurysm was located on the cavernous
segment in 8 cases and cervical segment in 2 cases, and mean
size was 27.9 mm. Patients with aneurysm of the cavernous
segment presented with pituitary dysfunction in 1 case, and
ophthalmoplegia in 7 cases, 3 of whom also had ptosis
(Table 2). The 2 patients with aneurysm of the cervical segment
complained of enlarging cervical mass. Intramural thrombus
was observed in 4 cases. Pre-existing white matter change
was detected in 6 patients. Collateral flow was classified as
robust in 5 cases, fair in 3, and poor in 2.
Intra- and postoperative results are shown in Table 3.
Intraoperatively, STA-MCA bypass preceding RAG
DSA digital subtraction angiography, MCA middle cerebral artery, SD
standard deviation, SSEP somatosensory evoked potential, T2WI T2-
weighted image
anastomosis was performed in all but one patient with scalp
burn so harvesting STA might have been harmful (case no.1).
Mean temporary occlusion time was 22, 26, and 27 min for
STA-MCA bypass, RAG-MCA anastomosis, and RAG-ECA
anastomosis, respectively. Mean MCA occlusion time of all
10 patients was 23 min (Table 1). A 50% or greater decrease in
SSEP N20-P25 amplitude considered to indicate moderate to
severe hypoperfusion occurred in 1 patient during MCA
clamping for RAG-MCA anastomosis, in whom the support-
ive STA-MCA bypass was not performed.
Postoperative CT, MR angiography, and DWI were obtain-
ed on day 1 in all patients. CT showed thrombosis of the
aneurysm without hemorrhage in all cases. MR angiography
confirmed widely patent RAG, and DWI detected no new
ischemic lesion in all patients. Postoperative DSA
 Neurosurg Rev
HT DL Smoking

demonstrated robust bypass flow from the ECA to MCA via

Yes Yes Yes

Yes No Yes

the RAG, and no anterograde flow into the aneurysm in all

No No No

Yes Yes No
No No No

Yes Yes No
Yes No No
Yes Yes No

No Yes No
Yes No No

patients. No patient showed new symptom after the operation.

Follow-up clinical study and MR imaging were performed
in 9 patients at about 6 months (range 5–7 months) after the
operation. One patient could not undergo this follow up be-
cause she died of respiratory failure 6 months after the surgery.
Pre-existing white matter change on

Clinical examination found that the preoperative symptoms

had resolved in 8 of the 9 patients. T2WI detected no additional
ischemic lesion compared with preoperative imaging. MR an-
giography demonstrated robust bypass flow in all 9 patients.
One patient did not undergo preoperative neuropsychologi-
cal examinations because of impaired consciousness due to
pituitary dysfunction, one patient died of respiratory failure
III oculomotor nerve, VI abducens nerve, DL dyslipidemia, HT hypertension, ICA internal carotid artery, Lt left, Rt right, T2WI T2-weighted image

due to chronic obstructive pulmonary disease 6 months after

T2WI

Yes

Yes

Yes
Yes
Yes
Yes

the operation, and one patient could not undergo neuropsycho-

No
No

No
No

logical examinations because of severe dizziness due to diplo-

pia, although the postoperative course was uneventful. Thus, a
Collateral

total of 7 patients completed neuropsychological examinations

Robust

Robust
Robust

Robust
Robust
Poor
Poor
flow

Fair

Fair

before and after surgery. All postoperative neuropsychological

Fair

scores except composite memory score slightly improved in

these 7 patients. Group rate analysis showed all postoperative
neuropsychological scores did not change significantly com-
Intramural

pared with preoperative scores, and PIQ showed tendency to

thrombus

improve although not significant change (p = 0.0625) (Table 4).

Yes

Yes
Yes
Yes

No
No
No

No
No

No

Discussion
Aneurysm size

Safety and feasibility of high-flow bypass followed by ICA

(mm)

ligation for large or giant aneurysms of cavernous

Lt ICA cavernous 23

48
Lt ICA cavernous 22

Lt ICA cavernous 15
38

Rt ICA cavernous 27
Rt ICA cavernous 20
Lt ICA cavernous 28

Rt ICA cavernous 22

Lt ICA cavernous 36

or cervical portion
Lt ICA cervical
Lt ICA cervical

Large or giant ICA aneurysms of cavernous or cervical por-

Aneurysm

tion causing mass effect are often treated by open surgery such
location

as clipping, trapping or aneurysmectomy, with or without by-

pass or patch closure, and endovascular intervention, but the
treatment of large ICA aneurysm is still challenging. The op-
Ptosis, diplopia (Rt III palsy)
Ptosis, diplopia (Rt III palsy)

timum method for cervical ICA aneurysms has not been

Diplopia (Lt III, VI palsy)
Diplopia (Lt III, VI palsy)

Ptosis, diplopia (Lt III, VI

Enlarging cervical mass
Enlarging cervical mass

established although various surgical approaches have been

Diplopia (Rt III palsy)

Diplopia (Lt III palsy)

Pituitary dysfunction
used [13]. Endovascular coil embolization with or without
stenting for giant cavernous carotid aneurysms has unfortu-
nately resulted in high recanalization and re-treatment rates
Preoperative demographics

Sex Symptom

palsy)
[14, 15]. Recently, flow diverting stents have offered possibil-
ities for formidable and complex aneurysms. Pipeline for
uncoilable or failed aneuryms trial showed complete aneu-

M
M
rysm occlusion of 73.6% at 6 months, and 86.8% at 1 year,

F
F
F

F
F
F

F
F
and a 5.6% rate of major complications such as major ipsilat-
eral thrombosis, intraparenchymal hemorrhage, and neurolog-
(years)
Age

ical death [16]. Several studies reported aneurysm rupture

68
59
69

63
56
70
72
67
66
69
following stent deployment and this leads to relatively serious
Table 2

condition [17–19]. Intrastent stenosis is also reported [20–22],

Case
no.

10
and these hemorrhagic and thrombotic complications raises

1
2
3
4
5
6
7

8
9
Neurosurg Rev

Table 3 Intra- and postoperative results

Case Temporary occlusion MCA SSEP amplitude DWI lesion Postoperative DSA Symptom Follow-up MR NPE
no. time (min) occlusion decline (> 50%) on POD 1 at imaging completion
time (min) 6 months
STA- RAG- RAG- Bypass Anterograde Bypass T2WI
MCA MCA ECA flow flow into flow change
aneurysm

1 N/A 26 27 26 Yes No Robust No No Robust No Yes

2 25 23 29 25 No No Robust No No Robust No Yes
3 30 30 17 30 No No Robust No Yes Robust No No
4 24 21 29 24 No No Robust No No Robust No Yes
5 21 28 29 21 No No Robust No No Robust No Yes
6 21 23 32 21 No No Robust No No Robust No Yes
7 17 24 22 17 No No Robust No No Robust No Yes
8 16 24 31 16 No No Robust No No Robust No Yes
9 18 28 28 18 No No Robust No N/A N/A N/A No
10 30 35 22 30 No No Robust No No Robust No No

DSA digital subtraction angiography, DWI diffusion-weighted image, ECA external carotid artery, MCA middle cerebral artery, N/A not available, NPE
neuropsychological examination, RAG radial artery graft, SSEP somatosensory evoked potential, STA superficial temporal artery, T2WI T2-weighted
image

concern about the duration of dual antiplatelet therapy but
consensus is yet to be reached. Direct surgical options, such
as neck clipping or trapping, offer definitive treatment of such
aneurysms, but are technically challenging and carry higher
risks of cranial nerve palsy and ICA compromise [23, 24].
Indirect surgical treatments, such as high-flow bypass with
ICA ligation can achieve aneurysm obliteration with accept-
able rates of morbidity and mortality, as well as graft patency
[3, 25, 26]. The present series adopted this method of surgical
treatment.

Fig. 1 Representative case in a

68-year-old female with ptosis
and diplopia (case 8). T2WI at
4 years before admission showing
large flow void of the right cav-
ernous carotid artery (a). DSA of
the right carotid artery,
anteroposterior (b), and lateral
views (c), demonstrating a large
cavernous carotid aneurysm and a
distal anterior cerebral artery an-
eurysm (arrow in c) incidentally.
DSA of the vertebral artery
showing robust collateral flow
through the right posterior com-
municating artery during manual
compression of the right CCA (d)

Fig. 2 Case 8. Preoperative CT scan (a) and T2WI (b, c) showing
enlargement of the right cavernous carotid aneurysm, 27 mm in
maximum diameter. CT scan on postoperative day 1 showing marked
high density (d), and T2WI showing signal change at the aneurysms,
suggesting thrombosis (e). MR angiograms on postoperative day 1
The balloon occlusion test (BOT) is commonly used to
assess tolerance to ligation of the ICA. However, no universal
standard has been determined, the accuracy of this test is com-
plicated and controversial, and sometimes complications oc-
cur such as cerebral infarction [27, 28]. Moreover, postopera-
tive ischemic complications as well as delayed aneurysm for-
mation are known after simple ICA occlusion without revas-
cularization [29, 30]. Furthermore, the impact of abrupt occlu-
sion of the ICA on postoperative cognitive function cannot be
predicted because the minimal structural damage visualized
on T2WI such as pial/microvascular injury could have subtle
effects on postoperative neurocognitive function after intra-
cranial surgery [31]. For these reasons, we employed graft
bypass without performing preoperative BOT in all patients,
although the collateral flow was robust in 5 cases.
In the present series, we performed high-flow bypass
followed by ICA ligation for large or giant symptomatic
Neurosurg Rev
showing robust flow from the right ECA to MCA via the RAG, ICA
ligation at the cervical portion, and no anterograde flow into the
aneurysm (f, g). Arterial spin labeling showing no laterality of blood
flow (h). DWI on postoperative day 1 showing no new ischemic lesion
(i–l)
aneurysms of cavernous or cervical portion. All 10 patients
progressed favorably without developing new symptoms after
the operation. Immediately after the operation, DWI on post-
operative day 1 showed no new ischemic lesion, MR angiog-
raphy showed robust bypass flow and no anterograde flow
into the aneurysm in all patients. Follow-up study was con-
ducted in 9 of 10 patients, and MR angiography showed ro-
bust bypass flow as on postoperative day 1. The preoperative
symptoms improved in 9 of 10 patients at follow-up. These
results indicate the efficacy and safety of this surgery.
Additionally, we continue to follow the 9 patients. Last out-
patient follow-up was performed in 9 patients at median
48 months (range 12–118 months). None of the 9 patients had
suffered additional clinical stroke events such as cerebral infarc-
tion or aneurysm rupture, and 8 of 9 patients were free from the
preoperative symptoms, this was the same result as 6 months
after the operation. Follow up MR imaging study was also
Neurosurg Rev
Fig. 3 Intraoperative photographs of case 8. a Right common, external,
and internal carotid arteries were exposed. Hypoglossal nerve (arrow)
was also exposed. Arrowhead shows the ECA where the RAG is anasto-
mosed. b Right frontotemporal craniotomy was performed and the trocar
(arrows) was passed through the subzygomatic tunnel from the cranium
to the neck. c The sylvian fissure was widely opened and the M2 (arrow)
and M3 (arrowhead) of the MCA, where the RAG and STA are
conducted in 6 patients at median 62 months (range 21–
114 months). T2WI showed no additional ischemic lesions,
and MR angiography demonstrated robust bypass in these pa-
tients. Therefore, high-flow bypass with RAG followed by ICA
ligation is safe and effective treatment for large or giant aneu-
rysms of cavernous or cervical portion, as described in previous
studies [2, 3].
Minimizing hypoperfusion impact by supportive STA-M3
bypass before RAG-M2 anastomosis
In this series, we performed supportive STA-M3 bypass be-
fore RAG-M2 anastomosis in all patients but one with scalp
anastomosed, were exposed. d, e Supportive STA-M3 bypass (d) and
RAG-M2 anastomosis (e) were conducted using 9–0 nylon under high
magnification. f RAG-ECA anastomosis was conducted with running
suture using 6–0 nylon. g Good bypass flow via RAG (arrow), as well
as STA (arrowhead), was confirmed. h The cervical ICAwas permanently
ligated (arrow). Arrowhead shows the proximal end of the RAG anasto-
mosed to the ECA. i Final image of the operation
burn preventing safe harvesting of the STA. Performance of
supportive STA-M3 anastomosis increased the total time of
the operation, but may prevent major ischemic injury during
anastomosis of large caliber arteries because tolerance to tem-
porary occlusion of the recipient M2 during anastomosis is
impossible to establish [3, 32, 33]. Actually, slowly progres-
sive neuronal death during postischemic hyperperfusion after
RAG-M2 bypass for cortical laminar necrosis has been report-
ed [6]. The ischemic and reperfusion injury occurred after
occlusion of the M2 for 47 min in that report.
In the present study, mean occlusion time during STA-
M3 anastomosis (22 min, 9 cases) was shorter than that of
RAG-M2 anastomosis (26 min, 10 cases), and the
 Neurosurg Rev

Fig. 4 Case 8. MR angiogram at 6 months after the operation showing robust flow to the right MCA area via the RAG (a). T2WI showing no further
change after the operation (b–f)

supportive STA-M3 bypass perfused the area distal to the
anastomosis during RAG-M2 anastomosis and prevented
ischemia due to temporary M2 occlusion. Cerebral hypo-
perfusion verified by reduction in SSEP amplitude was
observed in one patient without STA-M3 bypass.
Moreover, DWI on postoperative day 1 detected no wide
range of infarction caused by ischemia or reperfusion inju-
ry due to the temporary MCA occlusion. Also, we would
like to make the anastomosis between RAG and M2 as
wide and accurate as possible, because this graft could
replace the ICA in the future. The supportive STA-M3
bypass allowed the surgeon to concentrate on the RAG-

Table 4 Group rate analysis of

pre- and postoperative neuropsy- Test Preoperative score Postoperative score p valueb
chological scores (n = 7)
WAIS-III
VIQ 104 (100–114) 106 (101–122) 0.7813
PIQ 109 (102–116) 113 (109–125) 0.0625
WMS-R
Composite memory score 111 (95–119) 109 (97–120) 1
Attention/concentration score 113 (93–118) 113 (93–118) 0.6875
Averagea 107.5 (101.5–116.25) 114.5 (102.25–115) 0.2188

Values of scores are median (interquartile range)

PIQ performance intelligence quotient, VIQ verbal intelligence quotient, WAIS-III Wechsler Adult Intelligence
Scale-Third Edition, WMS-R Wechsler Memory Scale-Revised
a
Average, (VIQ + PIQ + composite memory score + attention/concentration score) ÷ 4
b
Significant at p < 0.05
Neurosurg Rev
M2 anastomosis procedure without considering the dura-
tion of occlusion, and might have contributed to the good
patency of the graft after the operation as well as
preventing ischemia due to temporary occlusion during
anastomosis.
Neurocognitive function change after high-flow bypass
followed by ICA ligation
The present study investigated neurocognitive function
change after high-flow bypass followed by ICA ligation.
Several studies have reported cognitive change after
extracranial-intracranial bypass surgery [34–38]. Some
studies reported no positive impact on cognition in the
bypass surgery, but some demonstrated improvements after
operation in various cognitive domains, such as verbal
memory, visual memory, executive function, attention,
and psychomotor speed, but no consensus has been
reached regarding the neurocognitive change after bypass
surgery.
The present study demonstrated that postoperative neu-
ropsychological scores were mostly higher, although not
significantly, than preoperative scores according to group
rate analysis. Minimal structural change visualized on
T2WI, such as pial/microvascular injury, not long opera-
tion time or specific approach, can cause subtle effects on
postoperative neurocognitive function after intracranial
surgery [31]. In the present series, no apparent change oc-
curred on T2WI at mid-term, possibly affecting the post-
operative neuropsychological scores. Considering this as-
pect, universal high-flow bypass might have achieved
preservation of the neurocognitive performance, because
chronic ischemic burden without high-flow bypass, even
in the presence of robust collateral flow, may cause struc-
tural change detectable by T2WI and decline in
neurocognitive performance over the medium and long
term. Therefore, we can conclude that high-flow bypass
followed by ICA ligation does not adversely affect the
postoperative cognitive function as a whole.
Limitations
This study has several important limitations. First, this study
has the inherent limitations of a retrospective analysis.
Second, this study included a relatively small number of pa-
tients, mainly because the rare character of the diseases and
surgery. Because of the small number of patients, we should
suggest the only conclusion that can be made is that cognitive
function did not show global worsening after surgery. The
impact of high-flow bypass with ICA ligation on cognitive
function has not been previously investigated, and we should
suggest the result of this study as just a possibility at this time.
Additional cases are required to definitively determine the
safety and feasibility as well as impact on cognition of the
present surgical strategy.
Conclusions
High-flow bypass followed by ICA ligation for large or giant
aneurysms of cavernous or cervical portion had good clinical
outcomes. Successful high-flow bypass using RAG with sup-
portive STA-MCA bypass and ICA ligation does not adverse-
ly affect postoperative cognitive function.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.
Ethical approval All procedures performed in studies involving hu-
man participants were in accordance with the ethical standards of the
institutional and/or national research committee and with the 1964
Helsinki declaration and its later amendments or comparable ethical
standards.
Informed consent Informed consent was obtained from all individual
participants included in the study.
Abbreviations BOT, balloon occlusion test; CCA, common
carotid artery; CT, computed tomography; DSA, digital sub-
traction angiography; DWI, diffusion-weighted magnetic res-
onance imaging; ECA, external carotid artery; ICA, internal
carotid artery; MCA, middle cerebral artery; MR, magnetic
resonance; PIQ, performance intelligence quotients; RAG, ra-
dial artery graft; SSEPs, somatosensory evoked potentials;
STA, superficial temporal artery; T2WI, T2-weighted magnetic
resonance imaging; VIQ, verbal intelligence quotients; WAIS-
III, Wechsler Adult Intelligence Scale-Third Edition; WMS-R,
Wechsler Memory Scale-Revised
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