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8cases - Complex MCA-Tub-2020-Changhai
8cases - Complex MCA-Tub-2020-Changhai
Interventional Neuroradiology
1–8
Endovascular treatment of complex ! The Author(s) 2020
Article reuse guidelines:
middle cerebral artery aneurysms sagepub.com/journals-permissions
DOI: 10.1177/1591019920946216
using TuBridge flow diverters journals.sagepub.com/home/ine
Feng Liang1,*, Yibing Yang1,*, Lijuan Luo1, Bingye Liao2, Guofeng Zhang1,
Siqi Ou1, Weiping Xiao1, Ning Guo1 and Tiewei Qi1
Abstract
Background: The safety and efficacy of the TuBridge flow diverter in treating middle cerebral artery aneurysms remains
unknown. In this study, we report our preliminary experience treating complex middle cerebral artery aneurysms using the
TuBridge flow diverter.
Methods: A prospectively maintained database of intracranial aneurysms treated with the TuBridge flow diverter was retro-
spectively reviewed, and patients with middle cerebral artery aneurysms were included in this study. Demographics, aneurysm
features, complications, and clinical and angiographic outcomes were assessed. Evaluation of the angiographic results
included occlusion grade of aneurysm (O’Kelly–Marotta grading scale), patency of jailed branch(es), and in-stent stenosis.
Results: Eight patients with eight middle cerebral artery aneurysms were included in this study. The mean aneurysm size
was 11.8 6.8 mm. There were no procedure-related complications and there was no morbidity or mortality at a mean
follow-up of 11.3 3.6 months. All patients had follow-up angiograms at a mean of 7.5 4.0 months after surgery. Of the
eight patients, there was 1 (12.5%) O’Kelly–Marotta grading scale A, 3 (37.5%) O’Kelly–Marotta grading scale B, 1 (12.5%)
O’Kelly–Marotta grading scale C, and 3 (37.5%) O’Kelly–Marotta grading scale D. Of the seven patients with jailed branch,
the blood flow of jailed branch was unchanged in 4 (57.1%), decreased in 2 (28.6%), and occluded in 1 (14.3%). In-stent
stenosis was mild in 2 (25%) patients and moderate in 1 (12.5%) patient.
Conclusion: Midterm results suggest that endovascular treatment of middle cerebral artery aneurysms using the TuBridge
flow diverter is safe and associated with good outcomes. The TuBridge flow diverter may be an option for complex middle
cerebral artery aneurysms that are difficult to treat with either clipping or coiling.
Keywords
TuBridge flow diverter, endovascular treatment, middle cerebral artery aneurysm
Received 3 March 2020; accepted 8 July 2020
Background
self-expandable stent-like device with flared ends
Middle cerebral artery (MCA) aneurysms are primarily (Figure 1).7 TFDs are available in diameters of
treated with either microsurgical clipping or endovas- 2.5 mm to 6.5 mm and lengths of 12 mm to 45 mm.
cular coiling.1 However, fusiform aneurysms, recurrent The TFD is composed of either 64 microfilaments
aneurysms, or aneurysms with distal branches arising (diameter 3.5 mm) or 48 microfilaments (diame-
from the aneurysm sac remain difficult to treat.2 ter < 3.5 mm). The TFD also contains two double-
Morbidity or insufficient occlusion is not uncommon helix platinum–iridium radiopaque microfilaments
after treatment of these types of aneurysms.3
In the past decade, the flow diverter device (FDD)
1
had become an important option for the treatment of Department of Neurosurgery, the First Affiliated Hospital of Sun Yat-sen
University, Guangzhou, China
aneurysm.4 By producing a flow diversion effect, an 2
Department of Operation Theater, the First Affiliated Hospital of Sun Yat-
FDD induces intra-aneurysmal thrombosis while pre- sen University, Guangzhou, China
serving the normal flow in the parent artery and its
*These authors contributed equally to this paper.
branches, eventually leading to healing of the neoin-
Corresponding author:
tima across the neck of the aneurysm.5,6 Tiewei Qi, Department of Neurosurgery, the First Affiliated Hospital of
The TuBridge flow diverter (TFD; MicroPort, Sun Yat-sen University, 58 Zhongshan 2nd Road, Guangzhou, China.
Shanghai, China) is a nickel–titanium braided, Email: qitiewei@163.com
2 Interventional Neuroradiology 0(0)
Angiographic outcomes and one had ruptured one month before the proce-
dure. There were 2 (25%) recurrent aneurysms,
Angiographic outcome was assessed using the
which were previously treated by clipping. The diam-
O’Kelly–Marotta grading scale (OKM).10 Aneurysm
eters of these two aneurysms before clipping were
filling was graded as: A, complete (>95%); B, incom-
plete (5–95%); C, neck remnant (<5%); D, no filling 26 mm and 10 mm, respectively. Patient demographics
(0%). Stasis was graded as: 1, no stasis (clearance of and aneurysm features are summarized in Table 1.
contrast within the arterial phase); 2, moderate stasis
(clearance of contrast prior to the venous phase); 3, Angiography results
significant stasis (contrast persists in the aneurysm TFDs were successfully deployed in all eight patients
into the venous phase and beyond). OKM aneurysm and all eight patients were treated with a single TFD.
filling of C or D was considered favorable aneurysm Seven patients had “jailed” arteries; one patient with
occlusion. an M2 aneurysm did not have a jailed branch (case 3).
On follow-up angiography, the “jailed” artery was Concomitant coiling was performed in 1 (12.5%)
also evaluated. Jailed artery flow was classified into patient (case 1, Figure 2). Coil-assisted stent deploy-
three levels: unchanged (concentration of contrast ment was performed in a patient with an M1 fusiform
within the artery and diameter of the vessel are both aneurysm (case 7, Figure 3). Balloon angioplasty was
similar to that before the procedure); decreased needed to improve wall apposition of the TFD in 1
(either the concentration of contrast within the (12.5%) patient (case 2, Figure 4).
artery or the diameter of the vessel is lower than Immediate angiogram after TFD deployment dem-
that before the procedure, or filling of contrast is
onstrated OKM filling grade A in 4 (50%) patients
delayed to a greater degree) and occluded (the vessel
and grade B in 4 (50%) patients. The stasis grading
was not seen).
scale was 1 in 4 (50%) patients and 3 in 4 (50%)
In-stent stenosis was also evaluated on follow-up
patients.
angiography. In-stent stenosis was defined as endo-
Follow-up angiograms were performed a mean of
thelium growth beyond the limits of the stent wall,
7.5 4.0 months after surgery in all patients. Of the
which was seen as a “gap” between the intra-lumen
filling of contrast and the metallic mesh of the stent 8 aneurysms, 1 (12.5%) was OKM A, 3 (37.5%) were
on angiogram. Less than 25% loss of lumen was con- OKM B, 1 (12.5%) was OKM C, and 3 (37.5%) were
sidered intimal hyperplasia. In-stent stenosis was cat- OKM D. Thus, favorable aneurysm occlusion (OKM
egorized as mild (26–50%), moderate (51–75%), and C þ D) was obtained in 4 (50%) aneurysms. Stasis
severe (>75%).11 grade was 1 in 2 (25%) patients, 2 in 1 (12.5%)
patient, and 3 in 2 (25%) patients. Of the seven
Statistical analysis patients with jailed branch, the blood flow in the
jailed branch was unchanged in 4 (57.1%) patients,
Continuous variables were presented as means and decreased in 2 (28.6%) patients, and occluded in 1
standard deviation (SD). Categorical variables were (14.3%) patient. In-stent stenosis was detected in
presented as numbers and percentages. All statistical three patients (37.5%) at a mean of six months. The
tests were performed using STATA 13.0 software in-stent stenosis was mild in 2 (25%) patients and
(Stata Corporation, College Station, Texas, USA). moderate in 1 (12.5%) patient. Angiography results
are summarized in Table 1.
Results
Complications and clinical outcomes
Patient characteristics and aneurysm features
There were no procedure-related complications. At
Eight patients with MCA aneurysms treated with the last follow-up, a mean of 11.3 3.6 months after
TFDs from July 2018 to December 2019 were identi- surgery, there were no morbidities and no mortalities.
fied in the database and included in the analysis.
There were four males and four females, with a Illustrative case
mean age of 54.4 10.4 years. The aneurysm was
located in M1 in 3 (37.5%) patients, in MCA bifur- A 55-year-old female complained of intermittent
cation in 4 (50%) patients, and in M2 in 1(12.5%) headache for five months (case 1, Figure 2).
patient. The mean aneurysm size was 11.8 6.8 mm, Computed tomography angiography (CTA) demon-
and there were 2 (25%) small aneurysms, 5 (62.5%) strated a left MCA bifurcation fusiform aneurysm of
large aneurysms, and 1 (12.5%) giant aneurysm. 26 mm, involving distal M1 and both trunks of M2.
Aneurysm morphology was saccular in 2 (75%) The aneurysm was reconstructed by clipping, which
patients and fusiform in 6 (75%) patients. The mean achieved a volume reduction of >80% and preserva-
diameters of the proximal parent artery and the distal tion of both trunks of M2. Postoperative CTA dem-
parent artery were 3.0 0.1 mm and 2.8 0.3 mm, onstrated the clipped aneurysm, a segmental stenotic
respectively. Seven of the aneurysms were unruptured distal M1, a patent superior trunk of M2, and a
4 Interventional Neuroradiology 0(0)
Moderate
patent inferior trunk of M2. The patient was dis-
stenosis
In-stent
charged without any neurological deficits.
Mild
Mild
No
No
No
No
No
At six-month follow-up after surgery, angiography
branch flow demonstrated a major recurrence of the aneurysm
Unchanged
Unchanged
Unchanged
Unchanged
with a daughter sac close to the proximal end.
Decreased
Decreased
FU jailed
Occluded
Conventional clipping, coiling, or stent-assisted coil-
ing was not feasible for the recurrent aneurysm.
N/A Trapping of the aneurysm combined with extracrani-
al–intracranial (EC-IC) bypass would be difficult
(months)
FU OKM
D (18)
B1 (6)
B3 (6)
B3 (6)
A1 (6)
C2 (6)
D (6)
No (18)
No (12)
(12)
(12)
(12)
(12)
(6)
(6)
75 mg/day). The operative plan was to land the
No
No
No
No
No
No
B3
B3
B3
B3
A1
A1
A1
A1
Yes
Yes
Yes
Yes
Yes
Yes
Yes
No
No
No
No
No
No
No
Yes (clipping)
(previous
No
No
No
No
No
3.0/3.2
3.0/3.1
2.9/2.6
3.1/2.8
3.2/3.0
2.9/2.5
3.2/3.0
2.8/2.5
12
10
11
14
10
3
Unruptured
Unruptured
Unruptured
Unruptured
Unruptured
Unruptured
Ruptured
Discussion
TFDs have been reported to be safe and effective for
aneurysm
Fusiform
Fusiform
Fusiform
Fusiform
Fusiform
Fusiform
Saccular
Saccular
MCA B
MCA B
MCA B
M1
M2
M1
M1
55
52
62
50
61
30
61
64
M
M
M
3
4
5
6
7
8
Liang et al. 5
Figure 2. (a) CTA demonstrated a left MCA bifurcation giant aneurysm involving distal M1 and the superior trunk of M2. The inferior trunk
of M2 was not visible. (b) Post-clipping CTA demonstrated the reconstructed aneurysm with stenotic M1 and patent distal vessels. The
inferior trunk of M2 emerged (white arrow). (c) Six-month follow-up angiogram demonstrated a major recurrence of the aneurysm with a
daughter sac in the proximal part (white arrowhead). (d) Post-procedure un-subtracted image showed the TFD landed in M1 and the
superior trunk of M2 and loose packing of the aneurysm with coils. (e) Immediate postoperative angiogram demonstrated decreased flow
of the inferior trunk of M2 (black arrows). (f) Angiogram six months after surgery showed the proximal part of the aneurysm was
thrombosed, M1 was stenotic, and the inferior trunk of M2 was invisible. (g) On 18-month follow-up angiogram, the aneurysm was
completely occluded; the distal M1 and the superior trunk of M2 were reconstructed. However, the distal M1 was still moderately stenotic
and the inferior trunk of M2 was occluded (black arrowheads). (h) Eighteen-month follow-up angiogram of the external carotid artery
showed that a collateral blood supply was established from the middle meningeal artery to the distal vessels of inferior trunk of M2
(hollow arrows).
Figure 3. (a and b) Pre-procedure angiogram demonstrated a right proximal M1 fusiform aneurysm involving part of the ICA bifurcation.
(c and d) When the TFD was passing through the acute angle of the vessel, the aneurysm was temporally filled with a coil to support the
stent. (e) After the stent passed the acute angle, the coil was retrieved to inspect the wall apposition of the TFD. (f) Lateral view of the TFD
deployed with support of a coil in the aneurysm. (g and h) Post-procedure angiogram demonstrated decreased filling of the aneurysm
and patent jailed artery of A1. (i and j) Angiogram at six months after surgery showed the filling of aneurysm was decreased, the blood
flow of the jailed A1 was decreased, and ICA was mildly stenotic.
6 Interventional Neuroradiology 0(0)
Figure 4. (a and b) CTA and DSA demonstrated a left M1 perforator artery aneurysm of 3 mm (white arrow). (c) After stent deployment,
the wall apposition of the proximal end was not sufficient (white arrowhead). (d) Balloon angioplasty was performed to improve wall
apposition of the proximal end of the stent. (e and f) Immediate postoperative angiogram demonstrated improved wall apposition (black
arrow) and patent jailed perforators. (g and h) Angiogram at six months after surgery demonstrated that the aneurysm was completed
occluded (black arrowhead), the blood flow of the jailed perforators was unchanged, and M1 was mildly stenotic.
diverters, the larger TFD (3.5 mm) has more braid- Occlusion of the jailed branch
ed microfilaments, which decreases the shortening
The long-term rate of side branch occlusion after cov-
rate of the flow diverter after full opening and offers
erage by a flow diverter in the treatment of ICA aneu-
more appropriate pore attenuation. A design includ-
rysm was 15.8–20%.18,19 Beyond the Circle of Willis,
ing a greater number of braided microfilaments is also 50% of covered branches were occluded or nar-
seen in P64 diverter. rowed.20 Occlusion or reduced caliber of a jailed
branch was seen in 14–50% cases of MCA aneurysms
Therapeutic strategy for treating MCA aneurysms treated with a FDD and was one of the main causes
In our center, microsurgical clipping is the preferred of morbidity.16,17,21 In this study, there were seven
method for treating MCA aneurysms. Coiling or aneurysms located at the M1 or MCA bifurcation,
stent-assisted coiling is an alternative choice for elder- in which the bifurcating branches or lenticulostriate
ly patients with multiple comorbidities, comatose arteries emanated from the neck of the aneurysm or
patients with ruptured aneurysms, patients with directly from the sac of the aneurysm. Immediate
recurrent aneurysms after previous clipping, and for reduction of blood flow in these arteries was seen in
patients with aneurysms deemed difficult to clip. two cases. During follow-up, the jailed branch was
occluded or reduced in caliber in 42.9% (3/7) of the
However, fusiform aneurysms, recurrent aneurysms,
cases; however, there was no symptomatic cerebral
and aneurysms with branches arising from the sac are
ischemia noted in any patient.
difficult to treat with the aforementioned methods.
About 5% of patients developed symptomatic
For these aneurysms, treatment with an FDD has
cerebral ischemia caused by jailed artery occlusion
become a new option.
or decreased flow.15 However, most patients tolerated
jailed artery occlusion or decreased flow without
FDDs and MCA aneurysms symptoms or radiological findings.21 Gradual reduc-
FDDs have become the first-line treatment for the tion of blood flow, instead of an abrupt change,
ICA aneurysms, but not for MCA aneurysms because occurred in most cases.14 Thus, the territories sup-
the mechanism of FDD healing the aneurysm is not plied by the jailed branch were able to recruit collat-
consistent with the structure of MCA aneurysms. eral vessels from adjacent branches over time.22
MCA aneurysms are mostly located at the MCA
bifurcation and the bifurcating branches usually ema- Occlusion of the aneurysm
nate directly from the base of the aneurysm. Landing The relatively low occlusion rate comparing to clip-
the FDD in M1 and one trunk of M2 makes the other ping was another reason why FDDs have not been
trunk of M2 “jailed.” The “jailed” branch might be used for the treatment of MCA aneurysms. The com-
occluded after FDD implantation, leading to cerebral plete occlusion rate of FDDs in the treatment of
ischemia. Conversely, if the “jailed” branch remained MCA aneurysms was reported to be 36.4–84%.12–17
patent, the aneurysm might not be obliterated due to In this series, the complete occlusion rate was 37.5%,
the persistent flow.15 and favorable occlusion rate was 50%. The low
Liang et al. 7
complete occlusion rate might relate to three factors. TFD is that due to the nature of the nickel–titanium
First, persistent flow in the jailed branch might hinder alloy, the visibility of the stent mesh is poor
thrombosis inside the aneurysm.15 The neck of the under fluoroscopy; only the two platinum–iridium
aneurysm usually involves more than 1 of the bifur- radiopaque helix wires are highly visible. Therefore,
cating branches. An FDD is usually deployed in one it is sometimes difficult to assess wall apposition of
major branch and usually covers only part of the neck the device. This may be a contributing factor to the
of the aneurysm. The uncovered part of the neck high incidence of stent stenosis in this study. It has
might have a persistent flow connection with the been reported that the rate of in-stent stenosis of flow
jailed branch, making it more difficult to initiate diverters is as high as 57%.27 However, with longer
intra-aneurysmal thrombosis. As such, jailed branch follow-up in-stent stenosis might resolve spontane-
occlusion could facilitate obliteration of the aneu- ously, and thus the rate will be lower.28,29
rysm.15 In case 1 in which the patient had an MCA
bifurcation aneurysm, the jailed inferior trunk of M2 Limitations of the study
and the aneurysm were noted to be occluded on
The limitations of this study are a relatively small
follow-up angiography. Second, in a curved vascular
number of patients, and a short follow-up period.
segment, the constituent filaments of the device slide
However, the results of our preliminary experience
over one another, making the porosity of the outer
of the treatment of complex MCA aneurysms using
curve less than that of the inner curve, and thus less
the TFD are encouraging. Patients with complex
than the nominal porosity.23 This causes the flow
MCA aneurysms may benefit because of less
diverting effect of the outer curve to decrease. In
procedure-related risk.
our series, six of eight aneurysms were located at
the outer curve of the vessel, which may have contrib-
uted to the low complete occlusion rate. Third, the Conclusion
occlusion rate increases with the length of follow- Our preliminary results demonstrated that the TFD is
up.24 Fifty percent of aneurysms are completely safe and effective for the treatment of MCA aneur-
occluded no earlier than 12 months after surgery.12 ysms. Given the high safety profile, the TFD could be
In our study, only one aneurysm had angiographic a new option for the treatment of complex MCA
follow-up of more than 12 months. Thus, the low aneurysms which are difficult to treat with clipping
complete occlusion rate may also be related to the or coiling. However, further study with a larger pop-
relatively short follow-up period. ulation and long-term follow-up is needed to define
Six aneurysms in this study were fusiform, includ- the role of the TFD in the treatment of MCA
ing one recurrent aneurysm. In case 1, we clipped and aneurysms.
reconstructed the giant fusiform aneurysm. However,
the aneurysm recurred in less than six months. In this Contributors
aneurysm, the lesion might have involved the entire
FL, LL, BL, GZ, SO, and WX acquired the data. FL and
vessel wall, which may have allowed the unclipped
YY analyzed the data and drafted the manuscript. NG and
part of the artery wall to enlarge and form another TQ developed the project. All authors revised the paper
giant aneurysm. A flow diverter might be the optimal critically for important intellectual content and provided
solution for this kind of aneurysm. Flow diversion final approval of the version published. All authors agree
might protect the vessel wall by both reducing the to be accountable for all aspects of the work in ensuring
direct impact of the blood flow and inducing intra- that questions related to the accuracy or integrity of any
aneurysmal thrombosis. However, unlike saccular part of the work are appropriately investigated and
aneurysm, the formation of neointima which may resolved. FL and YY contributed equally as first authors.
be crucial for minimizing the recurrence of the aneu-
rysm, was not found in histological studies of fusi- Declaration of conflicting interests
form aneurysms.25 The author(s) declared no potential conflicts of interest with
respect to the research, authorship, and/or publication of
In-stent stenosis this article.
It is worth noting that although there were no delayed
ischemic events, we found in-stent stenosis in 37.5% Ethics approval
of the cases. Neointimal formation was necessary to This study was approved by the Ethics Committee of the
cover the neck of aneurysm and block the inflow to First Affiliated Hospital of Sun Yat-sen University.
aneurysm sac. However, overreaction of intimal
hyperplasia might lead to in-stent stenosis. A possible Funding
reason for in-stent stenosis formation after flow The author(s) disclosed receipt of the following financial
diverter deployment is insufficient wall apposition, support for the research, authorship, and/or publication
which might lead to thrombus in-between the stent of this article: This work was supported by Department of
mesh and arterial wall.26 One disadvantage of the Health of Guangdong Province (Grant number A2018067).
8 Interventional Neuroradiology 0(0)