Neurologia medico-chirurgica Advance Publication Date: October 26, 2019

T echnical N ote doi: 10.2176/nmc.tn.2019-0162

Neurol Med Chir (Tokyo) xx, xxx–xxx, xxxx Online October 26, 2019

The Targeted Bypass Strategy for Preventing

Hemorrhage in Moyamoya Disease: Technical Note
Takeshi FUNAKI,1 Hiroharu KATAOKA,1 Kazumichi YOSHIDA,1
Takayuki KIKUCHI,1 Yohei MINEHARU,1 Masakazu OKAWA,1
Yukihiro YAMAO,1 and Susumu MIYAMOTO1

1
Department of Neurosurgery, Kyoto University Graduate School of Medicine,
Kyoto, Kyoto, Japan

Abstract
Although direct bypass is effective at preventing intracranial hemorrhage in moyamoya disease, the opti-
mal strategy for achieving this purpose has rarely been addressed. The tailored targeting bypass strategy
is a novel technical modification of direct bypass focused on hemorrhage prevention. The strategy is
based on the promising theory of periventricular anastomosis, which explains the mechanism of hemor-
rhage in moyamoya disease. The strategy is defined as the use of multi-imaging modalities to predeter-
mine in a tailored manner a target vessel at the point at which the medullary artery directly extends from
the periventricular anastomosis of interest. Direct bypass with a wide craniotomy was performed on 13
hemispheres in eight patients according to this strategy. Marked shrinkage of the periventricular anas-
tomosis of interest was observed in all but one hemisphere after surgery, and no new hemorrhages have
occurred as of this writing. The present case series illustrates the technical aspects and preliminary
results of the tailored targeting bypass strategy, an approach that might expand the potential of direct
bypass in preventing hemorrhage.

Key words:  moyamoya disease, cerebral revascularization, cerebral hemorrhage, targeting bypass

Introduction perforating or choroidal artery, that serves as a supply

to the cortex (Fig. 1A). Periventricular vasculature
Intracranial hemorrhage is the factor most severely can be restored to normal with successful direct
affecting outcome in moyamoya disease.1) Hemorrhage bypass that eliminates pathological anastomoses via
is a serious problem in every type of this disease, bypass flow.8) The improvement might be enhanced
as it can occur even in those initially manifesting with bypass targeting the cortical area where the
ischemic symptom.2) Direct bypass is beneficial as periventricular anastomosis is distributed.
a means of secondary prevention of hemorrhage;3–5) The objective of the present technical report is to
however, bleeding can recur even after bypass surgery. present our new tailored targeting bypass strategy,
According to the Japan Adult Moyamoya Trial, about a modified direct bypass procedure for hemorrhage
10% of patients who had undergone bypass surgery prevention, and its preliminary results.
experienced rebleeding within 5 years.5) To prevent
hemorrhage effectively, this surgical procedure must Surgical Technique
be optimized.
“Periventricular anastomosis” is a term repre- Definition
senting the fragile vasculature causing hemorrhage in “Tailored targeting bypass strategy” is defined as
moyamoya disease.6,7) This vasculature is characterized a technical modification of direct bypass in which
by the connection between the medullary artery and surgeons select the recipient artery with reference to
the distribution of the periventricular anastomosis of
Received July 9, 2019; Accepted August 26, 2019 interest (Fig. 1B). The scalp artery is anastomosed
Copyright© 2019 by The Japan Neurosurgical Society This to one of the cortical arteries (“target vessel”) at the
work is licensed under a Creative Commons Attribution- point at which the medullary artery directly extends
NonCommercial-NoDerivatives International License. from the periventricular anastomosis of interest.

1
 Neurologia medico-chirurgica Advance Publication Date: October 26, 2019

2 T. Funaki et al.

signal of the abnormally extended artery in

the MRA overlapped with the hypo-intensity
area in the SWI.
3. 
Selection of target vessel: The target vessel,
a cortical artery at the point at which the
periventricular anastomosis of interest directly
extended, was determined through meticulous
assessment of conventional and three-dimensional
rotational angiography. Subsequently, MR angi-
A B ography data were used to generate a brain
surface image on the workstation to determine
Fig. 1  Schematic illustration of periventricular ­anastomosis a location at which the target vessel was
(A) and tailored targeting bypass strategy (B). exposed on the surface of the brain, which
represented the recipient site. This step was
Patient selection important because performing an anastomosis
This strategy was indicated when the primary to an artery located at depth in the sulcus is
purpose of bypass surgery was hemorrhage prevention difficult. The cortical veins served as good
and when at least one periventricular anastomosis landmarks in this process. Knowledge of
in the affected hemisphere apparently extended to anatomy was also useful in determining the
the cortex. target vessel; a lenticulostriate anastomosis
is typically distributed anterior to the central
Preoperative assessment sulcus, whereas a choroidal anastomosis is
For the preoperative assessment, patients under- typically distributed within or posterior to
went magnetic resonance (MR) imaging that included the central sulcus.
whole-brain 3 Tesla time-of-flight MR angiography
as well as susceptibility-weighted imaging (SWI); Operative procedure
resting-state and acetazolamide-challenging single Patients were positioned supine with the head
photon emission computed tomography (SPECT); rotated to the contralateral side. Skin incisions varied
and conventional digital subtraction angiography. according to the number of required bypasses and the
Three-dimensional rotational angiography was also surgeons’ preference. A large craniotomy exposing
considered for adult patients. After imaging data was the predetermined target vessel was performed to
obtained, three stepwise preoperative assessments facilitate wide revascularization.11) After the dura
were performed: was opened, the target vessel was identified on the
surface of the brain with reference to a surface image
1. Identification of periventricular anastomosis: generated preoperatively. For hemispheres with a
Periventricular anastomosis was identified with periventricular anastomosis of only one subtype, we
sliding-thin-slab maximum-intensity-projection performed a single anastomosis to the target vessel,
coronal MR angiography6) and conventional usually belonging to M4 of the middle cerebral
angiography according to the criteria set out artery (MCA), using the superficial temporal artery
in the Japan Adult Moyamoya Trial Group.9) (STA) as a donor (STA–MCA single anastomosis).
The periventricular anastomosis was then clas- For hemispheres with multiple periventricular
sified into one of the three subtypes according anastomoses of equal interest, e.g. lenticulostriate
to its origin: lenticulostriate, thalamic, or and choroidal, we considered STA–MCA double
choroidal.6,7,9) Some hemispheres had two or anastomosis targeting both types; alternatively, we
three subtypes simultaneously. considered single anastomosis targeting only anas-
2. Determination of periventricular anastomosis of tomosis at higher risk of bleeding with the addition
interest: For patients who had suffered intrac- of an indirect bypass preserving the middle menin-
ranial hemorrhage and exhibited anastomoses geal artery coursing above the other. For pediatric
of multiple subtypes simultaneously, the one cases, encephalo-myo-synangiosis was added after
responsible for hemorrhage was typically the anastomosis.
anastomosis of focus. Fusion images of SWI
and the axial source image of the MR angiog- Postoperative assessment
raphy were useful in determining the respon- Magnetic resonance imaging, SPECT, and conven-
sible vessel.10) In these images, the bleeding tional angiography were performed on all patients
point was defined as the point at which the between 3 and 9 months (mean, 4.9 months) after

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Targeted Bypass for Moyamoya Disease 3

surgery to confirm the shrinkage of the periventricular SPECT revealed almost normal resting-stage cerebral
anastomosis. Thereafter, patients were regularly blood flow and reduced cerebral vascular reserve
followed with annual MR imaging including MR after acetazolamide challenge in the hemisphere.
angiography and SWI. Although less symptomatic, the patient desired
bypass surgery to reduce the hemodynamic burden
Case Presentation on the aneurysm.
The anterior parietal artery, to which the choroidal
A 41-year-old female (Case 1 in Table 1) was diag- anastomosis extended, was determined as the target
nosed with moyamoya disease when she suffered vessel through angiographic assessment (Fig. 2A). The
trauma and underwent brain MRI. Although she brain surface image revealed the vessel was exposed
had experienced mild transient ischemic attack in on the postcentral gyrus (Figs. 2B and 3A). A large
childhood, she had no apparent ischemic symptoms craniotomy was performed to expose predominantly
after reaching adulthood. Left internal carotid angi- the parietal lobe (Fig. 3B). After the dura was opened,
ography revealed severe stenosis in the terminal the target vessel was identified on the parietal lobe
portion of the internal carotid artery. It also revealed between two cortical veins (Fig. 3C). This anatom-
choroidal anastomosis, a connection between the ical configuration completely corresponded to that
anterior choroidal artery and the medullary arteries seen in the surface image generated preoperatively
extending to the cortical branch of the MCA (Fig. 3A). The parietal branch of the STA was then
(Fig. 2A). An aneurysm was also observed at the anastomosed to the target vessel (Fig. 3D), and indo-
site of the anastomosis. No other periventricular cyanine green video angiography revealed the good
anastomoses were observed in the hemisphere. patency of the bypass. The postoperative course was

Table 1  Summary of the cases indicated tailored targeting bypass strategy

F/u
Age/ PA of Direct PA (Re)
Case Side Symptom Hemorrhage site Recipient period
Sex interest bypass change bleed†
(months)
1 41/F L Asymptomatic N/A Choroidal Single Ant. 13 Shrink None
parietal
2 29/F R Hemorrhage Putamen LSA and Double Prefrontal/ 16 Shrink None
choroidal Central
L Asymptomatic N/A LSA and Double Prefrontal/ 11 Shrink None
choroidal Central
3 12/M R Hemorrhage IVH Choroidal Single Ant. 58 Shrink None
parietal
4 11/M R Hemorrhage IVH LSA and Single* Ant. 25 Shrink None
choroidal parietal
L Asymptomatic N/A LSA and Single* Ant. 24 Shrink None
choroidal parietal
5 65/F L Hemorrhage Temporal Choroidal Single Central 44 Shrink None
R Asymptomatic N/A Choroidal Single Ant. 41 Shrink None
parietal
6 9/F L Hemorrhage IVH Choroidal Single Ant. 26 Shrink None
parietal
R Asymptomatic N/A Choroidal Single Central 25 Shrink None
7 54/M R Hemorrhage Temporoparietal Choroidal Single Central 13 Persisted None
L Asymptomatic N/A Choroidal Single Ant. 11 Shrink None
parietal
8 9/F R Asymptomatic N/A LSA and Single* Post. 11 Shrink None
side in choroidal parietal
ischemic
disease
†
Including asymptomatic bleeds detected with susceptibility weighted imaging. *Choroidal anastomosis is targeted by direct bypass,
while LSA anastomosis at lower risk of bleeding is targeted by indirect bypass using the middle meningeal artery. Ant.: anterior, IVH:
intraventricular hemorrhage, LSA: lenticulostriate, N/A: not available, PA: periventricular anastomosis, Post.: posterior.

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4 T. Funaki et al.

A B C D

Fig. 2  Case 1. (A) Lateral-view angiography of the left internal carotid artery before surgery revealing choroidal
anastomosis (black arrowheads), extending to the target vessel (arrow). Note the aneurysm observed at the site
of the anastomosis (asterisk). (B) Corresponding brain surface image generated with MR angiography data. White
arrowheads indicate the central sulcus. The target vessel is exposed on the postcentral gyrus (arrow). (C) Lateral-
view angiography of the left external carotid artery obtained 9 months after surgery revealing patency of the bypass
and accurate anastomosis to the target vessel (arrow). (D) Lateral-view angiography of the left internal carotid
artery obtained 9 months after surgery revealing marked shrinkage of the choroidal anastomosis and aneurysm.

A B C D

Fig. 3  Case 1. (A) Brain surface image generated with MR angiography data. The arrow indicates the target
vessel; the arrowheads, the central sulcus; and the dotted line, the presumed operative field. (B) Postsurgical
three-dimensional CT image revealing the skin incision line and craniotomy. (C) Intraoperative view after opening
of the dura. The arrow indicates the target vessel; the arrowheads, the central sulcus. Note that the relationship
between the target vessel and cortical veins corresponds to that in the preoperative brain surface image in Panel A.
(D) Intraoperative view after anastomosis.

uneventful. Angiography performed 9 months after Discussion

surgery revealed the results: the bypass remained
patent and perfused the cortex via the target vessel The tailored targeting bypass strategy is a unique
(Fig. 2C), and the choroidal anastomosis and aneu- modification of direct bypass in that it focuses
rysm had shrunk markedly (Fig. 2D). on hemorrhage prevention in moyamoya disease.
The results of the Japan Adult Moyamoya Trial
Results have revealed the effectiveness of direct bypass
at preventing rebleeding.5) However, no study has
The tailored targeting bypass strategy was indicated addressed the optimal direct-bypass procedure
as a first-line surgical treatment for 13 hemispheres focused on hemorrhage prevention. Although the
in eight cases (Table 1). In all cases, anastomosis to literature suggests excellent modifications of direct
the intended target vessel was successful. Marked bypass as well as craniotomy,12–20) most of these are
shrinkage of the periventricular anastomosis was focused on treating ischemic symptoms.
observed in 12 of the 13 hemispheres in postoperative The seminal characteristic of tailored targeting
angiography and MR angiography. Mean follow-up bypass strategy is the flexibility afforded the surgeon
period after the surgery was 24.5 months, and as in selecting the recipient artery to accommodate the
of this writing no postsurgical hemorrhagic attack hemorrhage mechanism. The distribution of fragile
or increased asymptomatic bleed detected with SWI periventricular anastomoses varies by its subtype:
has been observed. lenticulostriate anastomoses are distributed to the

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Targeted Bypass for Moyamoya Disease 5

anterior part of the brain, whereas choroidal anas- chosen through exploration of the predetermined
tomoses are distributed to the posterior part.9) The region during surgery.
surgeon may therefore select the target vessel of The tailored targeting bypass strategy might
bypass surgery to better accommodate the subtype expand the potential for bypass surgery to prevent
of periventricular anastomosis of interest. For hemorrhage. This strategy could also be applied as a
patients with a choroidal anastomosis distributed second-line surgical treatment for patients suffering
to the parietal lobe, this strategy permits bypass repeated hemorrhages from the medial anastomotic
even to the parietal lobe, a less likely target of branch despite successful STA-MCA anastomosis.29)
conventional bypass surgery. This finding might be Larger and long-term follow-up studies are required
noteworthy because several studies have revealed to prove the efficacy of this strategy.
that choroidal anastomosis carries an extremely high
risk of bleeding.21–23) Kato et al.24) reported a case in Conflicts of Interest Disclosure
which multiple aneurysms on the choroidal anas-
tomosis had shrunk after successful direct bypass The authors report no conflict of interest concerning
to the parietal lobe. the materials or methods used in this study or the
The tailored targeting bypass strategy seems beneficial findings specified in this article.
especially for those with mild hemodynamic failure,
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