Case Report

Risky Cerebrovascular Anatomic Orientation: Implications for Brain Revascularization
Alhusain Nagm1,2, Tetsuyoshi Horiuchi1, Takao Yanagawa1, Kazuhiro Hongo1

Key words
- Anterior cerebral artery
- Cerebral ischemia
- Cerebral watershed infarction
- Extracranial (EC)-Intracranial (IC) bypass
- Revascularization
- STA-ACA bypass graft

Abbreviations and Acronyms
ACA: Anterior cerebral artery
CM: Callosomarginal artery
CT: Computed tomography
DSA: Digital subtraction angiography
MCA: Middle cerebral artery
OA: Occipital artery
PC: Paracentral artery
PIFA: Posterior internal frontal artery
POD: Postoperative day
Ra: Recipient artery
SPECT: Single-photon emission computed
tomography
STA: Superficial temporal artery
TIA: Transient ischemic attack
From the 1Department of Neurosurgery, Shinshu University
School of Medicine, Matsumoto, Japan; and 2Department of
Neurosurgery, Al-Azhar University Faculty of MedicineeNasr
City, Cairo, Egypt
To whom correspondence should be addressed:
Alhusain Nagm, M.D., M.Sc.
[E-mail: nagm@shinshu-u.ac.jp]
Conflict of interest statement: All authors certify that
they have NO affiliations with or involvement in any
organization or entity with any financial interest (such as
honoraria; educational grants; participation in speakers’
bureaus; membership, employment, consultancies, stock
ownership, or other equity interest; and expert testimony or
patent-licensing arrangements) or nonfinancial interest (such
as personal or professional relationships, affiliations,
knowledge, or beliefs) in the subject matter or materials
discussed in this manuscript.
Citation: World Neurosurg. (2016).
http://dx.doi.org/10.1016/j.wneu.2016.09.023
Journal homepage: www.WORLDNEUROSURGERY.org
Available online: www.sciencedirect.com
1878-8750/$ - see front matter ª 2016 Elsevier Inc. All
rights reserved.

INTRODUCTION
Besides the rarity of isolated anterior
cerebral artery (ACA) occlusion, its revascularization remains a surgical challenge.1,2 Surgical options, including
“intracranial (IC)-IC”1,3 or “extracranial
(EC)-IC with or without graft”2,4-8 bypass,
need to be individualized for each patient.

This study documents a risky vascular anatomic orientation that might play an
important role in the postoperative hemodynamics following anterior cerebral
artery (ACA) revascularization. A 71-year-old woman presented with uncontrollable frequent right lower limb transient ischemic attacks (TIAs) attributed to
a left cerebral ischemic lesion due to severe left ACA stenosis. She underwent
successful left-sided superficial temporal arteryeACA bypass using interposed
vascular graft. The patient awoke satisfactory from anesthesia; however, on
postoperative day 1, she developed right-sided hemiparesis. Extensive postoperative investigations disclosed that watershed shift infarction was considered the etiology for this neurologic deterioration.

Controversy remains concerning the
effectiveness of ACA revascularization
procedures regarding prevention of
strokes2 despite successful results.1-4,6-8
To the best of our knowledge, this report
represents the first study that highlighted
watershed infarction following ACA
revascularization,
proposing
risky
vascular
anatomic
etiology
and
discussing better options.
CASE REPORT
History and Examination
In 2010, a 71-year-old woman was referred
to our hospital because of frequent transient ischemic attacks (TIAs), in the form
of right-sided predominant lower limb
motor weakness, despite medical treatment (clopidogrel for 1-month duration).
She was examined with magnetic resonance imaging, computed tomography
(CT) angiography, digital subtraction
angiography (DSA), and single-photon
emission CT (SPECT). Those studies
revealed a small, left, high-parietal
ischemic lesion, severe stenosis of the
left ACA, mild stenosis of the middle cerebral artery (MCA), insufficient collateral
flow (Figure 1AeD), and left-sided areas of
cerebral hypoperfusion (Figure 2).
Preoperative Planning
Following 1 week of intravenous heparinization, EC-IC bypass with occipital artery
(OA) vascular graft was tailored for this
patient. Other procedures, including

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endovascular management or indirect
bypass coupled with medication, were
considered risky and potentially ineffective
in our atherosclerotic patient with severe
A2 stenosis.
Operation
She was positioned prone-lateral, and her
head was fixed with a 4-pin Sugita head
holder. Doppler flowmeter was used to
map the parietal branch of the superficial
temporal artery (STA) and OA. The skin
incision was made along the course of the
parietal branch and extended upward to
the midline and then along the midline
downward to the bregma (Figure 3A
and B). The medial frontal craniotomy
was performed. The dura was opened,
and the posterior internal frontal artery
(PIFA) (0.9 mm in size) was selected as
the recipient (Figure 3C). This arterial
flow was weak. Indocyanine green
videoangiography showed slow antegrade
flow of ACA. A free OA graft (5 cm in
length, 1.0 mm in diameter) was
harvested after placing a linear skin
incision. The parietal branch of STA (1.5
mm) was prepared for anastomosis. Endto-end STA-OA anastomosis was done
with a total of 10 stitches (Figure 3D). Endto-side OA-PIFA anastomosis was achieved with 9 stitches of 10e0 nylon,
including 2 stay sutures (Figure 3E). The
occlusion time was 39 minutes. Patency
of the anastomosis was confirmed with
Doppler flowmeter and indocyanine
green videoangiography.

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RISKY CEREBROVASCULAR ANATOMIC ORIENTATION AND BRAIN REVASCULARIZATION

consideration during graft selection.7,10-12
Although the carotid occlusion surgery
study13 reported a 15% risk of
perioperative
strokes
in
patients
undergoing STA-MCA bypass for chronic
ischemia, the subemergent ischemia and
the necessity for ACA revascularization in
our patient seemed irrelevant to the Carotid Occlusion Surgery Study inclusion
criteria. Accordingly, the STA-OA-PIFA
bypass (Figure 6A and B) was considered
the best option.

Figure 1. Preoperative neuroimaging. (A) Diffusion-weighted imagingemagnetic resonance imaging
axial view showing the high-intensity ischemic lesion (red circle). (B) 3-dimensional computed
tomography angiography disclosing severe stenosis of the left anterior cerebral artery (ACA)-“A2”
(red arrow). (C and D) Digital subtraction angiography via left common carotid artery injection (C:
anteroposterior view, D: lateral view) showing severe stenosis of the left ACA, mild stenosis of the
middle cerebral artery, and insufficient leptomeningeal collateral flow.

Postoperative Course and Follow-up
She awoke from anesthesia without any
neurologic deficits. Immediate postoperative CT excluded iatrogenic complications. No further TIAs developed after
surgery. However, on postoperative day
(POD) 1, she developed sudden rightsided hemiparesis. Urgent CT and magnetic resonance imaging (Figure 4A)
disclosed worsening of the baseline
ischemic lesion. Aspirin and cilostazol
were administrated immediately. Post
operative MR angiography on POD1
exhibited patency of the anastomotic site
and its territories (Figure 4B). Persistent
patency of the bypass was confirmed
with DSA (Figure 4C and D) on POD3.
Postoperative SPECT disclosed increased
cortical uptake and confirmed watershed

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shift (Figure 5). The patient was referred
for rehabilitation, and her symptoms did
not resolve at the time of discharge.
DISCUSSION
Despite marked advances in recent revascularization techniques and perioperative
treatment, some patients suffer cerebral
infarction in the early postoperative
period.9,10
ACA Revascularization Procedure
In order to perform successful surgery in
our high-risk patient and to overcome
additional risk factors for postoperative
neurologic worsening,2 we studied our
options for ACA bypass1-8 and their
limitations and then took great

Postoperative Watershed Infarctions
Watershed
shifteinduced
cerebral
ischemia can lead to transient or permanent postoperative neurologic deteriorations.6,9,14-21 Interestingly, posto
perative infarction in patients from Asian
countries (as our patient) showed a more
aggressive clinical course.9
The neurologic deterioration in the early
postoperative period is referred to a focal
decrease in cerebral perfusion9 remote from
the anastomotic site (Figure 6C).
Perioperative SPECT studies detected these
focal chances (see Figures 2 and 5).
Herein,
extensive
postoperative
investigations ruled out all intraoperative
events, including hypotension,18 as the
patient
awoke
satisfactory
and
deterioration occurred on the next day.
Also, clear-cut causes (as intracranial hematomas) were also excluded by the early
postoperative CT. Additionally, on the basis
of postoperative neuroimaging, obvious
causes (occlusion or vascular spasm) of
neurologic deterioration were ruled out.
The region adjacent to the revascularization
site showed an increased uptake on
SPECT (see Figure 5), MR angiography
exhibited a marked increase in signal
intensity of the anastomosed vessel (see
Figure 4B), and patent STA-OA-PIFA
bypass was confirmed (see Figure 4C and
D). Embolic source arising from
the anastomotic site was also excluded on
the basis of the infarction pattern.
Accordingly, a new reversing flow pattern
(see Figure 6C), after bypass grafting,15
induced significant hypoperfusion in the
remote ACA territory and was considered
the key for the postoperative neurologic
deterioration in our patient. This was
supported by the following: 1) Our patient
was at a very high risk for decreased
focal perfusion9 due to unstable
hemodynamic7,21 as she presented with

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CASE REPORT
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RISKY CEREBROVASCULAR ANATOMIC ORIENTATION AND BRAIN REVASCULARIZATION

Figure 2. Preoperative resting 123I-iodoamphetamine single-photon
emission computed tomography study, revealing left-sided regions of

hypoperfusion. Colors represent perfusion levels according to the color
scale on the right.

frequent
TIAs
(3e4
attacks/day)
and preoperative cerebral infarction (see
Figure 1A) during the month preceding
surgery; 2) this watershed shift contributed
to neurologic deterioration in the early
postoperative period; and 3) the
perioperative SPECT studies detected a
distant focal decrease in cerebral
perfusion9,16 (see Figure 5).

Figure 3. Operative procedure. (A) and (B), 3-dimensional computed tomography angiography
showing the correlation between intraoperative head orientation, targeted vessels, locations of the
skin incisions (dashed lines), and the craniotomy (blue box). (C, D, and E), Intraoperative microscopic
video-captured images. (C) The posterior internal frontal artery (PIFA) was selected as a recipient.
(D) Starting the end-to-end superficial temporal arteryeoccipital artery (OA) graft anastomosis. (E)
End-to-side OA graftePIFA anastomosis (toe suture).

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Vascular Anatomic Orientation. Reviewing
the microsurgical anatomy of the distal
ACA22 revealed that the relationship of its
terminal branches and their origins is
greatly variable. This 3D vascular
anatomic orientation might have a great
role in determining the postoperative
hemodynamics (Figure 7A and B).
Herein, the recipient artery “PIFA” was
almost in a straight angle with the parent
artery “callosomarginal artery (CM).”
This made the new retrograde blood flow
“after bypass” and the normal antegrade
blood flow facing each other directly.
Subsequently, watershed shift occurred
due to hemodynamic changes and
reversal of flow at a specific point
“branch point of paracentral artery.” This

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Figure 4. Postoperative neuroimaging. (A) Diffusion-weighted
imagingemagnetic resonance (MR) imaging axial view “POD 1” showing
left high parietal watershed ischemic stroke. (B) MR angiography on POD 1
exhibiting a marked increase in signal intensity of the anastomosed vessel
(red arrow). (C and D) Digital subtraction angiography via left common
carotid artery injection (C: anteroposterior view, D: lateral view) “POD 3”

type might be referred to as a “risky
vascular orientation” (see Figure 7A).
This risky vascular orientation, defined as
the microsurgical anatomic angles
among the recipient artery (Ra), parent

artery, and branching point of the target
artery
that
makes
postoperative
hemodynamic changes, including reversal
of flow with subsequent watershed shift,
is more likely to occur. Here, reversal of

Figure 5. Postoperative resting 99m Tc depreotide single-photon emission
computed tomography study obtained 3 days after surgery, revealing
improvement of the left cortical uptake. However, the higher portions of

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showing excellent patency of the superficial temporal arteryeoccipital
artery (OA)eanterior cerebral artery (ACA) bypass with antegrade flow
through the left STA (black arrow)eOA (white arrow) graft to the territory of
the left ACA. The anastomotic sites are patent, yet perfusion to the entire
territory of the left A2 was not clearly demonstrated (blue arrow) due to
local hemodynamic disturbance.

flow was occurred as the correlation
between intraoperative findings and
retrograde analysis of neuroimaging
disclosed that the angle between the Ra
and parent artery was almost straight

regions (C, D, and E) became markedly hypoperfused (marked decrease in
uptake). Watershed shift was confirmed. Colors represent perfusion levels
according to the color scale on the right.

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CASE REPORT
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RISKY CEREBROVASCULAR ANATOMIC ORIENTATION AND BRAIN REVASCULARIZATION

(which made “the blood flow after bypass”
and “the normal antegrade blood flow”
facing each other directly). Additionally,
the acute angle between the Ra and
target artery was considered an obstacle
for smooth filling following bypass. On
the other hand, if the angles between
these arteries were ideal (Figure 7B),
watershed shift did not likely occur.

Figure 6. Schematic drawing of postoperative hemodynamic changes. (A) Preoperative condition:
hypoperfusion due to severe A2 stenosis, antegrade blood flow (blue arrows) and a small ischemic
infarction (yellow area). (B) Ideal expected condition “missed in our patient”: an increase in the A2
flow with direct bypass, the blood flow after anastomosis is adequately distributed (red arrows) with
sufficient perfusion (subsequent resolution of the ischemic area). (C) Postoperative condition:
watershed shift with induced significant hypoperfusion in the remote territory of the anterior
cerebral artery (large yellow area) due to reversing flow pattern (2-headed bidirectional blue arrow) at
the branching point (black arrow). Notice the vascular anatomic orientation “angles” of the
contributing vessels, which might have a great role in these hemodynamic changes. (D)
Recommended bypass: direct eloquent area revascularization using the posterior cerebral artery
(PCA) as a recipient. CM, callosomarginal artery; PC, paracentral artery; PIFA, posterior internal
frontal artery. The vascular diameters refer to the degree of perfusion (A, B and D, and C showed
hypoperfusion, sufficient perfusion, and watershed shift, respectively).

Figure 7. Schematic drawing showing the vascular anatomic orientation that might affect the
postoperative “extracranialeanterior cerebral artery bypass (large red arrow)” hemodynamics. (A)
Vascular relationship according to the real findings in our case of “risky vascular orientation.” The
recipient artery, the posterior internal frontal artery (PIFA), was in the same line with the parent artery,
the callosomarginal artery (CM). This almost straight angle (green-colored angle) made the blood flow
after bypass (dashed red arrows) and the normal antegrade blood flow opposing each other directly.
Subsequently, watershed shift occurred due to hemodynamic changes and reversal of flow (2-headed
bidirectional blue arrow) at the branch point of the paracentral (PC) artery. Watershed shift induced
significant hypoperfusion (large yellow area) in the remote territory of the PC artery. Additionally, the
acute angle between the PIFA and PC (yellow-colored angle) was considered an obstacle for smooth
filling of the PC artery with the new blood flow coming from PIFA. (B) Ideal vascular anatomic
orientation “missed in our patient.” Here, watershed shift is not seen because the reversal of flow is
unlikely to occur as the angle between the PIFA and CM (green-colored angle) is slightly obtuse, “not
straight.” Also, PIFA and PC (yellow-colored angle) allows easy direct flow (dashed red arrows) from
the PIFA “recipient artery” to the PC territory “target.” The vascular diameters refer to the degree of
perfusion (A and B, showed watershed shift and sufficient perfusion, respectively).

WORLD NEUROSURGERY -: ---, MONTH 2016

Better ACA Revascularization Options. Procedures like extensive double bypass can
reduce the risk of watershed shift; however, it is not applicable during ACA
revascularization. Although IC-IC bypass
can provide adequate distal perfusion, it
might add a new risk to a high-risk patient. Another option is direct eloquent
area revascularization, using the paracentral artery as a recipient (see
Figure 6D). This last option might carry a
risk for postoperative neurologic deficits
due to direct temporary occlusion of the
feeding artery during anastomosis.
However, in highly skilled hands, this
postoperative neurologic deficit might be
transient.
Advantages and Limitations of Our
Study. On the basis of this study, ACA
revascularization in a high-risk patient is
not a completely safe procedure. A risky
vascular anatomic orientation might be
involved in the postoperative hemodynamics and direct the patient outcome.
Accordingly, direct eloquent area revascularization might be a better option to
prevent significant permanent postoperative neurologic deficits.
The so-called “risky vascular anatomic
orientation” and its effect on the postoperative hemodynamic need further
studies incorporating a larger number of
patients for more solid conclusions. Also,
the efficacy of direct eloquent area revascularization in such cases needs to be
proved as a better option. Despite we
consider these 2 points as limitations of
our study, it carries new questions that
might be solved in the near future.
CONCLUSION
Our study disclosed that ACA revascularization in a high-risk patient is not a
completely safe procedure as it might
cause hemodynamic changes and permanent postoperative neurologic deficits. A
risky vascular anatomic orientation might

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RISKY CEREBROVASCULAR ANATOMIC ORIENTATION AND BRAIN REVASCULARIZATION

play an important role in the postoperative
hemodynamics; accordingly, the surgical
plan should be modified.

8. Terasaka S, Satoh M, Echizenya K, Murai H,
Fujimoto S, Asaoka K. Revascularization of the
anterior cerebral artery using a free superficial
temporal artery graft: a case report. Surg Neurol.
1997;48:164-169 [discussion: 169-170].

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Informed patient consent: The patient has consented to the
submission of the case report to the journal.

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Received 8 July 2016; accepted 6 September 2016
Citation: World Neurosurg. (2016).
http://dx.doi.org/10.1016/j.wneu.2016.09.023
Journal homepage: www.WORLDNEUROSURGERY.org
Available online: www.sciencedirect.com
1878-8750/$ - see front matter ª 2016 Elsevier Inc. All
rights reserved.

WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2016.09.023