Original Article

Clinical Outcome of Elderly Patients with Subarachnoid Hemorrhage: Validation of

Modality Assignment Based on Aneurysmal Morphology and Location
Takuma Maeda, Tetsu Satow, Go Ikeda, Eika Hamano, Naoki Hashimura, Takeshi Hara, Masatake Sumi,
Masaki Nishimura, Jun C. Takahashi

- BACKGROUND: The number of elderly patients with
subarachnoid hemorrhage is increasing. Elderly patients
have been postulated to benefit more from endovascular
coiling, compared with neurosurgical clipping. However,
we based our therapeutic modality on the morphology and
location of the aneurysms, rather than patients’ age or their
World Federation of Neurological Surgeons grade. The aim
of this study was to investigate the validity of our thera-
peutic modality over earlier approaches by assessing their
clinical outcomes.
- METHODS: The study sample included 539 patients who
underwent surgical procedures between January 2010 and
May 2019. Baseline characteristics, aneurysmal
morphology and location, surgical and clinical complica-
tions, and clinical outcomes were compared between
elderly (defined as aged 75 years or older) and young
patients.
- RESULTS: There were 124 elderly patients (23.0%) in the
sample. Eighty-five elderly patients (68.5%) received
neurosurgical clipping, whereas 67.0% of the young pa-
tients (P [ 0.827) received neurosurgical clipping. Of the
elderly patients who had a poor World Federation of
Neurological Surgeons grade, 49.4% and 48.7% underwent
neurosurgical clipping and endovascular coiling, respec-
tively (P [ 1.000). Elderly patients had fewer favorable
outcomes (21.8%) relative to young patients (61.8%; P <
0.001). There were no significant differences in the rate of
favorable outcomes between patients undergoing neuro-
surgical clipping relative to endovascular coiling (21.2%
vs. 23.1%; P [ 0.818).
- CONCLUSIONS: Neurosurgical clipping and endovas-
cular coiling yield comparable clinical outcomes in elderly
and young patients with subarachnoid hemorrhage. These
findings indicate that using a therapeutic modality based
on aneurysmal morphology and location may be an effec-
tive treatment approach.
INTRODUCTION
T he number of elderly patients with subarachnoid hemor-
rhage (SAH) has been increasing.1 However, the
management of elderly patients with SAH is still
clinically challenging. Several studies have shown that patients
older than 75 years have poorer clinical outcomes compared
with young patients.2-4 This difference may be because elderly
patients have various comorbidities, and it can be difficult to
identify which therapeutic modality should be used (e.g., neuro-
surgical clipping including extra-intracranial bypass and proximal
ligation, or endovascular coiling including internal trapping.)2-4
Elderly patients may benefit more from endovascular coiling
because it is less invasive. However, in this study, the therapeutic
modality selected for the target lesion is chosen based on the
morphology and location of the aneurysms, rather than on the

Key words WEB: Woven EndoBridge

- Aneurysmal morphology WFNS: World Federation of Neurological Societies
- Elderly patients
- Endovascular coiling Department of Neurosurgery, National Cerebral and Cardiovascular Center, Suita, Osaka,
- Neurosurgical clipping Japan
- Subarachnoid hemorrhage (SAH)
To whom correspondence should be addressed: Tetsu Satow, M.D., Ph.D.
[E-mail: tetsus@ncvc.go.jp]
Abbreviations and Acronyms
Acom: Anterior communicating artery Citation: World Neurosurg. (2020).
https://doi.org/10.1016/j.wneu.2020.07.189
AR: Aspect ratio
FD: Flow diverter Journal homepage: www.journals.elsevier.com/world-neurosurgery
ICA: Internal carotid artery Available online: www.sciencedirect.com
mRS: Modified Rankin Scale 1878-8750/$ - see front matter ª 2020 Elsevier Inc. All rights reserved.
SAH: Subarachnoid hemorrhage

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 ORIGINAL ARTICLE
TAKUMA MAEDA ET AL. THERAPEUTIC MODALITY FOR ELDERLY PATIENTS WITH SAH BASED ON ANEURYSMAL MORPHOLOGY AND LOCATION

Table 1. Characteristics of Elderly and Young Groups by Therapeutic Modality

Elderly Group Young Group
P Value
All Clipping Coiling P Value All Clipping Coiling P Value (Elderly vs. Young)

Number of patients 124 (23.0) 85 (68.5) 39 (31.5) 415 (77.0) 278 (67.0) 137 (33.0) 0.827
Age (years), mean  SD 81.2  4.6 80.5  4.2 82.7  5.1 0.033 56.7  11.4 57.0  11.1 56.1  11.4 0.335 0.512
Female sex 105 (81.2) 73 (85.9) 32 (82.1) 0.598 263 (63.4) 182 (43.9) 81.0 (59.1) 0.234 <0.001
Location of aneurysm
Internal carotid artery 49 (39.5) 37 (43.5) 12 (30.8) 0.235 113 (27.2) 87 (31.3) 26 (19.0) 0.009 0.019
Middle cerebral artery 33 (26.6) 32 (37.6) 1 (2.6) <0.001 103 (24.8) 98 (35.3) 5 (3.7) <0.001 0.816
Distal anterior cerebral artery 13 (10.5) 8 (9.4) 5 (12.8) 0.545 18 (4.3) 15 (5.4) 3 (2.2) 0.199 0.002
Anterior communicating artery 10 (8.1) 6 (7.1) 4 (10.3) 0.724 100 (24.1) 63 (22.7) 37 (27.0) 0.332 <0.001
Vertebrobasilar artery 19 (15.3) 2 (2.4) 17 (43.6) <0.001 81 (19.5) 15 (5.4) 66 (48.2) <0.001 0.242
World Federation of Neurological 0.358 0.878 0.071
Societies grade
I 30 (24.2) 17 (20.0) 13 (33.3) 118 (28.4) 79 (28.4) 39 (28.5)
II 25 (20.2) 19 (22.4) 6 (15.4) 109 (26.3) 72 (25.9) 37 (27.0)
III 8 (6.5) 7 (8.2) 1 (2.6) 28 (6.7) 20 (7.2) 8 (5.8)
IV 19 (15.3) 12 (14.1) 7 (17.9) 48 (11.6) 35 (12.6) 13 (9.5)
V 42 (33.9) 30 (35.3) 12 (30.8) 112 (27.0) 72 (25.9) 40 (29.2)
Poor clinical grade 61 (49.2) 42 (49.4) 19 (48.7) 1.000 160 (38.6) 107 (38.5) 53 (38.7) 1.000 0.037
Vascular risk factors 76 (61.3) 51 (60.0) 25 (64.1) 0.696 173 (41.7) 115 (41.4) 58 (42.3) 0.916 <0.001

Values are number (%) except where indicated otherwise.

patients’ age, for both elderly and young patients with SAH,
aiming at secure obliteration of the lesion.
We present the clinical outcomes for elderly and young patients
with SAH by therapeutic modalities. The aim of this study was to
investigate the clinical outcomes of each therapeutic modality to
assess the validity of our therapeutic regimen.
METHODS
This retrospective study was approved by the ethics committee of
the National Cerebral and Cardiovascular Center (M30-013). We
retrospectively reviewed the medical records of all patients (n ¼
539) with SAH who underwent neurosurgical clipping or endo-
vascular coiling at our hospital between January 2010 and May
2019. Patients with SAH who did not undergo surgical treatment
were excluded. The elderly group was defined as patients older
than 75 years, and elderly and young groups were compared on the
following factors: the patients’ age, sex, vascular risk factors
(hypertension, diabetes mellitus, and hyperlipidemia), World
Federation of Neurological Societies (WFNS) grade, aneurysmal
morphology and location, therapeutic modality, symptomatic ce-
rebral vasospasm, shunt dependence, surgical complications
(aneurysm rupture, postoperative acute infarction, thromboem-
bolic problem, severe contusion, coil migration, new neurological
deficit, intracerebral hemorrhage, subdural/epidural hematoma,
and wound infection), clinical complications (meningitis, pneu-
monia, urinary tract infection, sepsis, deep vein thrombosis,
gastrointestinal perforation, and other infection), and modified
Rankin Scale (mRS) score at discharge.
Patients were divided into 2 groups based on their clinical grade
on admission: fair (grade IeIII) and poor (grade IV and V) on the
WFNS grade. Patients were divided into 2 further groups based on
their clinical outcome at discharge, including favorable (0e2) and
unfavorable (3e6) according to the mRS score at discharge. The
locations of aneurysms were defined to pertain to the internal
carotid artery (ICA), the middle cerebral artery, the distal anterior
cerebral artery, the anterior communicating artery (Acom), and the
vertebrobasilar artery.
All cases of SAH were detected using a computed tomography
scan. Patients also underwent a digital subtraction angiography to
diagnose ruptured cerebral aneurysms and to investigate their
detailed morphology. After this investigation, neurosurgeons and
neurovascular physicians discussed and identified the most suit-
able therapeutic modality for each patient. Neurosurgical clipping
was performed under general anesthesia.
Patients with endovascular coiling were treated under general
anesthesia or deep sedation defined by achievement of modified

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TAKUMA MAEDA ET AL. THERAPEUTIC MODALITY FOR ELDERLY PATIENTS WITH SAH BASED ON ANEURYSMAL MORPHOLOGY AND LOCATION

Table 2. Aneurysmal Characteristics Excluding Dissection, Blisterlike and Fusiform Aneurysms

Clipping (n [ 321) Coiling (n [ 135) P Value

Neck (mm), mean  SD 3.39  1.71 3.26  1.96 0.079

Aspect ratio, mean  SD 1.44  0.78 1.6  0.96 0.043
<1 80 (25.7) 19 (14.6) 0.012
1e2 174 (55.9) 84 (64.6) 0.112
2 57 (18.3) 27 (20.8) 0.595
Anterior circulation, size 330 (96.8) 93 (68.9) <0.001
<3 mm 33 (10.5) 1 (1.1) 0.002
3e7 mm 178 (56.9) 63 (70.0) 0.028
7e13 mm 85 (27.2) 23 (25.6) 0.893
13 mm 17 (54.3) 3 (3.3) 0.585
Posterior circulation, size 11 (3.2) 42 (31.1) <0.001
<3 mm 2 (22.2) 8 (19.5) 1.000
3e7 mm 7 (77.8) 20 (48.8) 0.152
7e13 mm 0 (0) 12 (29.3) 0.092
13 mm 0 (0) 1 (2.4) 1.000
Bleb 274 (82.5) 102 (77.9) 0.290
Incorporated branch 126 (38.1) 30 (22.7) 0.002
Intracerebral hematoma 106 (31.3) 11 (8.1) <0.001

Values are number (%) except where indicated otherwise.

Table 3. Clinical Outcomes of Elderly and Young Groups by Therapeutic Modality

Elderly Group Young Group

All, Clipping, Coiling, All, Clipping, Coiling,

n (%) n (%) n (%) P Value n (%) n (%) n (%) P Value P Value (Elderly vs. Young)

Outcome at discharge 0.818 0.669 <0.001

Favorable 27 (21.8) 18 (21.2) 9 (23.1) 255 (61.4) 173 (62.2) 82 (59.9)
Unfavorable 97 (78.2) 67 (78.8) 30 (76.9) 160 (38.6) 105 (37.8) 55 (40.1)
Clinical complication 37 (29.8) 26 (30.6) 11 (28.2) 0.836 49 (11.8) 27 (9.7) 22 (16.1) 0.075 <0.001
Surgical complication 23 (18.5) 15 (17.6) 8 (20.5) 0.804 85 (20.5) 64 (23.0) 21 (15.3) 0.071 0.702
Aneurysm rupture 3 (2.4) 1 (1.2) 2 (5.1) 0.233 3 (0.7) 2 (0.7) 1 (0.7) 1.000 0.138
Infarction 8 (6.5) 8 (9.4) 0 (0) 0.056 40 (9.6) 37 (13.3) 3 (2.2) <0.001 0.369
Thromboembolic problem 3 (2.4) 0 (0) 3 (7.7) 0.030 9 (2.2) 0 (0) 9 (6.6) <0.001 1.000
Others 9 (7.3) 6 (7.1) 3 (7.7) 1.000 33 (7.9) 25 (9.0) 8 (5.8) 0.336 1.000
Rebleeding 3 (2.4) 2 (2.4) 1 (2.6) 1.000 4 (0.9) 3 (1.1) 1 (0.7) 1.000 0.202
Within 30 days after the procedure 2 (1.6) 2 (2.4) 0 (0) 1.000 3 (0.7) 3 (1.1) 0 (0) 0.554 0.325
30 days to 1 year 1 (0.8) 0 (0) 1 (2.6) 0.315 0 (0) 0 (0) 0 (0) 1.000 0.230
After 1 year 0 (0) 0 (0) 0 (0) 1.000 1 (0.2) 0 (0) 1 (0.7) 0.330 1.000
Symptomatic vasospasm 23 (18.6) 19 (22.4) 4 (10.3) 0.138 62 (14.9) 41 (14.7) 21 (15.3) 0.884 0.530
Shunt dependence 40 (32.3) 29 (34.1) 11 (28.2) 0.543 97 (23.4) 64 (23.0) 33 (9.5) 0.806 0.059

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TAKUMA MAEDA ET AL. THERAPEUTIC MODALITY FOR ELDERLY PATIENTS WITH SAH BASED ON ANEURYSMAL MORPHOLOGY AND LOCATION

Table 4. Univariate Analysis for Favorable and Unfavorable Outcomes in All Patients
Favorable, n (%) Unfavorable, n (%) P Value

Number of patients (%) 282 (52.3) 257 (47.7)

Age >75 years 27 (21.8) 97 (78.2) <0.001
Female sex 182 (33.8) 186 (34.5) 0.052
Poor clinical grade 48 (8.9) 173 (32.1) <0.001
Location of aneurysm
Internal carotid artery 81 (15.0) 81 (15.0) 0.511
Middle cerebral artery 71 (13.2) 65 (12.1) 1.000
Distal anterior cerebral artery 10 (1.9) 21 (3.9) 0.026
Anterior communicating artery 71 (13.2) 39 (7.2) 0.005
Vertebrobasilar artery 49 (9.1) 51 (9.5) 0.506
Vascular risk factors 122 (22.6) 127 (23.6) 0.167
Clinical complication 26 (4.8) 60 (11.1) <0.001
Surgical complication 43 (8.0) 65 (12.1) 0.004
Therapeutic modality 0.855
Neurosurgical clipping 191 (35.4) 172 (31.9)
Endovascular coiling 91 (16.9) 85 (15.8)
Rebleeding within 30 days after the procedure 1 (0.4) 4 (1.6) 0.197
Symptomatic vasospasm 25 (4.6) 60 (11.1) <0.001
Shunt dependence 33 (6.1) 104 (19.3) <0.001

Richmond Agitation-Sedation Scale e4. Heparin administration
was started before the catheter or sheath was advanced into the
target vessel to achieve an activated clotting time >250 seconds.
Usually, antiplatelet agents were not used before or during
endovascular coiling to prevent excessive bleeding because the
effects of antiplatelet agents cannot be reversed promptly.
Unpaired samples t tests using the Welch correction were used for
parametric data, and Mann-Whitney U tests were used for
nonparametric data. P < 0.05 was considered statistically signif-
icant. A multivariate analysis was also used to identify variables
predicting prognosis. SPSS version 24 (IBM Corp., Armonk, New
York, USA) was used for all statistical analyses.

Statistical Analysis
Quantitative variables were expressed as mean  standard devia- RESULTS
tion. The c2 or the Fisher exact test was used to identify covariates Five hundred and thirty-nine patients with a mean age of 62.4
that could be used as binary categorical dependent variables. years were enrolled in the study. There were more female (64.2%)

Table 5. Multivariate Analysis for Unfavorable Outcomes in All Patients

Odds Ratio 95% Confidence Interval P Value

Age >75 years 8.880 4.690e16.800 <0.001

Female sex 1.080 0.633e1.860 0.769
Poor clinical grade 12.300 7.140e21.100 <0.001
Anterior cerebral artery aneurysm 2.430 0.802e7.340 0.117
Anterior communicating artery aneurysm 1.080 0.590e1.970 0.805
Clinical complication 2.020 1.020e3.980 0.043
Surgical complication 4.800 2.550e9.040 <0.001
Symptomatic vasospasm 3.430 1.730e6.800 <0.001
Shunt dependence 4.180 2.370e7.400 <0.001

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TAKUMA MAEDA ET AL. THERAPEUTIC MODALITY FOR ELDERLY PATIENTS WITH SAH BASED ON ANEURYSMAL MORPHOLOGY AND LOCATION

Table 6. Favorable Outcomes at Discharge by Location of Aneurysms in Anterior Circulation

Elderly Group Young Group

All, Clipping, Coiling, All, Coiling, P Value (Elderly vs.

n (%) n (%) n (%) P Value n (%) Clipping n (%) P Value Young)

Internal carotid artery 13 (26.5) 9 (24.3) 4 (33.3) 0.708 68 (60.2) 50 (57.5) 18 (69.2) 0.363 <0.001
Middle cerebral artery 8 (24.2) 7 (21.9) 1 (100) 0.242 63 (61.2) 61 (62.2) 2 (40.0) 0.374 <0.001
Distal anterior cerebral artery 1 (7.7) 1 (12.5) 0 (0) 1.000 9 (50.0) 7 (46.7) 2 (66.7) 1.000 0.012
Anterior communicating 3 (30.0) 1 (16.7) 2 (50.0) 0.500 58 (56.0) 48 (76.2) 20 (54.1) 0.028 0.020
artery

compared with male patients. Of all patients, 124 (23.0%) were
aged 75 years or older. The baseline characteristics of the elderly
and young groups are shown in Table 1. The most common
location of the aneurysm was the ICA (25.2% of all patients) in
both elderly and young groups. A total of 363 patients (67.3%)
underwent neurosurgical clipping, and 176 patients (32.7%)
underwent endovascular coiling. Eighty-five patients (68.5%)
received neurosurgical clipping in the elderly group and 278
(67.0%) in the young group (P ¼ 0.827). On admission, more
elderly patients (n ¼ 61; 49.2%) had a poor clinical grade relative
to young patients (n ¼ 160; 38.6%) (P ¼ 0.037).
In the elderly group, 42 patients with neurosurgical clipping
(49.4%) and 19 patients with endovascular coiling (48.7%) had a
poor clinical grade on admission. Similarly, the young group also
had poor clinical grade on admission in neurosurgical clipping
(38.5%) and endovascular coiling (38.7%) (P ¼ 1.000). The char-
acteristics of the aneurysms excluding dissection, blood blistere
like, and fusiform aneurysms are shown in Table 2. There were
significant differences in the aspect ratio (AR: dome height/
maximum neck width; P ¼ 0.043), location (P < 0.001), size in
anterior circulation (<3 mm, P ¼ 0.00 and 3e7 mm, P ¼
0.028), existence of incorporated branch (branch arising from
the sac; P ¼ 0.002), and intracerebral hematoma (P < 0.001)
between neurosurgical clipping and endovascular coiling,
respectively.
The clinical outcomes for each therapeutic modality for elderly
and young groups are shown in Table 3. There were significant
differences in mRS score at discharge, fewer elderly patients
(n ¼ 27; 21.8%) had favorable outcomes compared with young
patients (n ¼ 255; 61.4%) (P < 0.001). In the elderly group, 18
patients (21.2%) and 9 patients (23.1%) had favorable outcomes
for neurosurgical clipping and endovascular coiling at discharge,
respectively (P ¼ 0.818). In the young group, 173 patients
(62.2%) and 82 patients (59.9%) had favorable outcomes for
neurosurgical clipping and endovascular coiling, respectively
(P ¼ 0.669). No elderly patients with a poor clinical grade on
admission achieved favorable outcomes compared with 48 of
160 patients (30.0%) in the young group who achieved favorable
outcomes despite having poor clinical grades on admission.
Univariate and multivariate analyses were performed to identify
factors associated with unfavorable outcomes (see Tables 4 and
5). There were significant differences in patients’ age,
preoperative clinical grade, clinical and surgical complications,
symptomatic cerebral vasospasm, and shunt dependence.
Logistic regression analyses including both elderly and young
groups showed that a poor clinical grade before surgery
predicted unfavorable outcomes (odds ratio, 12.30; 95%
confidence interval, 7.14e21.10). In addition, older age was also
associated with unfavorable outcomes (odds ratio, 8.88; 95%
confidence interval, 4.69e16.80).
In the subgroup analysis investigating the location of aneurysms
in the anterior circulation, there were significant differences in the
mRS score at discharge between elderly and young groups. In all
sites (middle cerebral artery, ICA, Acom, and distal anterior ce-
rebral artery), elderly patients had poorer outcomes compared
with young patients (P < 0.001, P < 0.001, P ¼ 0.020, and P ¼
0.012, respectively). In addition, there were no statistically sig-
nificant differences in the mRS score at discharge between elderly

Table 7. Age Limit and Clinical Outcomes in All Patients

Cutoff (years) Number of Patients (%) Favorable Outcome (%) Unfavorable Outcome (%) c2

>60 319 (59.2) 39.2 60.8 52.8

>65 249 (46.2) 35.7 64.3 49.7
>70 186 (34.5) 30.6 69.4 52.2
>75 124 (23) 21.8 78.2 58.7
>80 75 (13.9) 17.3 82.7 41.1
>85 25 (4.6) 16.0 84.0 12.4

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TAKUMA MAEDA ET AL. THERAPEUTIC MODALITY FOR ELDERLY PATIENTS WITH SAH BASED ON ANEURYSMAL MORPHOLOGY AND LOCATION
patients who had neurosurgical clipping or endovascular coiling
for aneurysms in any of these sites (see Table 6).
There were no age-related or treatment-related differences in
the incidence of surgical complications. In the elderly group, 15
patients (17.6%) and 8 (20.5%) patients had surgical complica-
tions after neurosurgical clipping and endovascular coiling,
respectively (P ¼ 0.804). Similarly, 64 (23.0%) and 21 (15.3%)
young patients had complications after neurosurgical clipping and
endovascular coiling (P ¼ 0.071). However, there were no age-
related differences in the overall incidence of rebleeding, symp-
tomatic cerebral vasospasm, or shunt dependence. A total of 5
patients who underwent neurosurgical clipping required retreat-
ment because of rebleeding that occurred within 30 days after the
procedure. No patients who underwent endovascular coiling
experienced rerupture within 30 days although there were 2 cases
of rebleeding in the chronic stage (11 and 32 months after the
procedure). There were no significant differences in the rate of
rebleeding within 30 days after the procedure between the elderly
and young groups (P ¼ 0.325). In the elderly group, 2 patients
(2.4%) and 0 patients (0%) underwent retreatment because of
rebleeding within 30 days after the procedure after neurosurgical
clipping and endovascular coiling, respectively (P ¼ 1.000).
Symptomatic vasospasm and shunt dependence were more
frequently recorded in the elderly group compared with the young
group (P ¼ 0.530 and P ¼ 0.059, respectively), but there were no
significant differences between neurosurgical clipping and endo-
vascular coiling.
However, there were significant age-related differences in the
frequency of clinical complications and vascular risk factors.
Thirty-seven elderly patients (29.8%) and 49 young patients
(11.8%) had clinical complications during hospitalization (P <
0.001). In addition, more elderly (n ¼ 76; 61.3%) had vascular risk
factors compared with young patients (n ¼ 173; 41.7%) (P <
0.001).
We performed exploratory analyses to identify the age cutoff
that distinguishes patients who have favorable outcomes at
discharge, taking into account low-risk and high-risk groups
(Table 7). A c2 test was performed to inspect the best cutoff age.
We found that patients younger than 75 years were more likely to
have favorable outcomes compared with patients older than 75
years (P < 0.001). Supplementary Tables 1 and 2 show the
characteristics and outcomes by generation.
DISCUSSION
Recent developments in the techniques and devices used for
endovascular coiling have resulted in an increase in the use of this
method for elderly patients with SAH.5 Because endovascular
coiling has been postulated to reduce surgical trauma, it may be
a good alternative to neurosurgical clipping, especially in elderly
patients.6 However, endovascular coiling is associated with a
risk of early recanalization or the need for retreatment, which
should be avoided in frail, elderly patients. ISAT (International
Subarachnoid Aneurysm Trial) suggested that the risk of late
rebleeding was higher for patients undergoing endovascular
coiling compared with neurosurgical clipping.7
We selected the appropriate therapeutic modality for elderly
patients with SAH, considering the morphology and the location
e6 www.SCIENCEDIRECT.com WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2020.07.189
ORIGINAL ARTICLE
of aneurysms, instead of patients’ age or their WFNS grade to
prevent rerupture. More patients with SAH who also had intra-
cerebral hematomas were treated with neurosurgical clipping and
by removing the hematoma because aneurysm and hematoma can
be addressed simultaneously. However, aneurysms located within
the posterior circulation, where a surgical approach is considered
more difficult, were more likely to have endovascular coiling.
Regarding the aneurysmal morphology, endovascular coiling
was preferentially selected only when the AR was >1. A previous
study8 suggested that aneurysms with a very wide neck, with an
AR <1.2, almost always require adjunctive techniques such as a
stent placement, which also requires antiplatelet therapy.
However, these approaches were not used for patients who had
endovascular coiling in the present study. Similar to this report,
the aneurysmal AR treated with endovascular coiling was
significantly higher than that treated with neurosurgical
clipping. When aneurysmal size was taken into account, smaller
aneurysms <3 mm within the anterior circulation were less
likely to be treated with endovascular coiling. This finding is
supported by previous work showing that small aneurysms
predicted intraprocedural rerupture and that they are linked to a
greater risk of coil embolization.9,10 Aneurysms with a branch
incorporated into the sac were most likely to be treated with
neurosurgical clipping rather than endovascular coiling. These
aneurysms may be treated more effectively with neurosurgical
clipping because endovascular coiling on an incorporated
branch can be challenging and because periprocedural
antiplatelet therapy is also typically necessary.11,12 Based on
these findings, endovascular coiling seems safe for the
management of aneurysms with a higher AR and a larger size if
the procedure is performed in the absence of incorporated
branch or other complications (e.g., intracerebral hematoma).
Flow diverters (FDs) may become an important tool in the
treatment of such aneurysms. A previous study has shown the
safety and feasibility of FDs in the treatment of unruptured an-
eurysms, but FD placement requires dual antiplatelet therapy to be
applied at least a few days before the procedure to prevent
thrombosis.13 Because inhibitors of IIb/IIIa glycoproteins have a
strong inhibitory effect on platelet aggregation, they have a
rapid onset of action, which would be beneficial in acute
procedures such as treatment of ruptured aneurysms. These
inhibitors may produce a more expedient effect, although there
is a risk of excessive rebleeding.
The use of a recently developed endovascular device, the
intrasaccular flow disruptor Woven EndoBridge (WEB [Sequent
Medical, Aliso Viejo, California, USA]), which was specifically
designed for treatment of wide-necked bifurcation aneurysms,
may also improve procedural outcome. WEB placement seems to
be a safe and feasible therapeutic modality for both ruptured and
unruptured aneurysms. The benefit of using WEB for ruptured
cases may be that dual antiplatelet therapy would not be required,
as determined by previous studies, although the number of
ruptured cases treated was small.14-16 Further studies are needed
to clarify the long-term outcomes with WEB, particularly with
respect to late rebleeding.
There are many studies investigating the clinical outcomes of
elderly patients with SAH. Several studies have identified that
clinical outcomes are significantly different when the cutoff age is

TAKUMA MAEDA ET AL. THERAPEUTIC MODALITY FOR ELDERLY PATIENTS WITH SAH BASED ON ANEURYSMAL MORPHOLOGY AND LOCATION
set to 75 years.2-4 In response to these studies, we defined elderly
patients as being aged 75 years or older, and they made up 23.0%
of the sample.
There was an inverse association between age and the clinical
grade on admission. Elderly patients (49.2%) were more likely to
have a poor grade compared with young patients (38.6%). Several
factors may explain this result, including findings that elderly
patients are more likely to have thick clots in the context of brain
atrophy compared with young patients.17-19 In line with this
finding, elderly patients show volumetric reductions in the brain
compared with young patients.18-20 These findings may help
explain why SAH may be more severe in certain contexts.
We selected the therapeutic modality regardless of the patients’
age or clinical grade. In response to this strategy, there were no
significant differences in the rate of poor clinical grade of patients
who underwent endovascular coiling or neurosurgical clipping in
either the elderly or the young groups. Clinical outcomes were
significantly worse in the elderly group; however, there were no
significant differences in the mRS score at discharge between
patients who had neurosurgical clipping compared with endo-
vascular coiling. Several studies18,21-23 have shown that clinical
grade on admission is one of the most important factors pre-
dicting clinical outcomes. In our study, all the elderly patients with
a poor clinical grade on admission showed unfavorable outcomes.
Similarly, in a systematic review, Ohkuma et al.18 reported that
only 1.5% of elderly patients with a poor clinical grade showed
favorable outcomes. Another study24 showed that fewer elderly
patients were likely to have an mRS score of 0e2 before
treatment and after 30 days. These data suggest that the
indication for aneurysmal treatment among elderly patients with
a poor clinical grade should be carefully considered.
In our study, elderly patients were more likely to have ruptured
aneurysms in the ICA. Similarly, Horiuchi and Hongo21 also
reported that the ICA was the most common site for aneurysms
in a study of 347 patients older than 75 years. However, other
studies6,19,25 have indicated that the most common site for
aneurysms in elderly patients is the anterior cerebral artery.
Several other studies have shown that elderly people are more
likely to have aneurysms in the vertebrobasilar artery and the
Acom, rather than the ICA.26 These studies may have reported
discrepant findings because they did not all examine patients
who were the same age. Further studies are needed to
investigate the potential reasons for these discrepancies.
There were no significant differences in clinical outcomes
between elderly patients who had neurosurgical clipping
compared with endovascular coiling. In a subgroup analysis of
elderly patients in the ISAT, 60.1% patients with endovascular
coiling and 56.1% patients with neurosurgical clipping had
favorable outcomes. In BRAT (Barrow Ruptured Aneurysm
Trial),27 7.8% of elderly patients had a favorable outcome with
both procedures. Comparatively, in the elderly patients in our
study, 21.2% showed favorable outcomes with endovascular
coiling and 23.1% with neurosurgical clipping. These
differences may be associated with how each study defined
elderly groups, and the rate of fair and poor grade on
admission. Supplementary Table 3 shows the characteristics
and clinical outcomes of the elderly patients in ISAT and
BRAT compared with our study. However, another subgroup
WORLD NEUROSURGERY -: e1-e11, - 2020
ORIGINAL ARTICLE
analysis in ISAT6 showed that elderly patients with aneurysms
in the ICA and posterior communicating artery were more
likely to have favorable outcomes when using endovascular
coiling. These differences may be the result of the random
allocation of patients in ISAT. Our selection of therapeutic
modalities may have led to favorable outcomes, irrespective of
the location of the aneurysm.
Surgical complications play an important role in determining
clinical outcomes.17 Previous work17,28,29 has shown that surgical
complications, involving aneurysm ruptures, are associated with
less favorable outcomes. In our study, there were no differences
in the frequency of surgical complications between elderly and
young groups. Moreover, there were also no differences in the
frequency of surgical complications between patients who
underwent neurosurgical clipping compared with endovascular
coiling in either elderly or young groups. However, the
frequency of postoperative acute infarctions caused by either
arterial or venous occlusions was higher for clipping compared
with coiling. In contrast, thromboembolic problems were
observed only in the context of coiling procedures.
Clinical complications and vascular risk factors, which were
more frequently observed in the elderly group, predicted poor
clinical outcomes in a multivariable analysis. Reducing the fre-
quency of clinical complications may improve clinical outcomes
for elderly patients.23,30 The differences between therapeutic
modalities were not statistically significant, implying that
adequate periprocedural management was used in both
therapeutic modalities. Therefore, the selection of the
therapeutic modality may not influence the rate of clinical
complications, including symptomatic vasospasm or shunt
dependence.
Rebleeding after procedures is one of the most serious compli-
cations. It is linked to unfavorable clinical outcomes, including
mortality.18,31 In our study, there were no differences in the need for
retreatment because of rebleeding when comparing patients who
had neurosurgical clipping with those who underwent
endovascular coiling, although late rebleeding after 30 days from
the procedure was observed only in endovascular coiling. Previous
work32 has shown that the frequency of rebleeding is more
common after endovascular coiling compared with neurosurgical
clipping; however, the risk of rebleeding after both procedures is
small. In ISAT, although the data were not stratified by age, 45 of
1073 patients who had endovascular coiling (4.2%) and 39 of 1070
patients who had neurosurgical clipping (3.6%) had confirmed
rebleeding from the target aneurysm within 1 year after the
procedure. Similarly, in BRAT, there was no rebleeding in
patients who underwent endovascular coiling, and 2 patients who
underwent neurosurgical clipping (0.8%) had rebleeding within 1
year. In our study, we observed only 1 of 176 patients who
underwent endovascular coiling (0.6%) and 5 of 363 patients who
underwent neurosurgical clipping (1.4%) with postsurgical
rebleeding. We used endovascular coiling only if the rupture point
of the aneurysms could be covered by the coils. This practice may
be why we showed equal or lower rates of rebleeding in the
context of endovascular coiling, compared with previous
studies.7,10,33
Previous study21 has shown that age is not a contraindication to
neurosurgical clipping. However, endovascular coiling may be
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 ORIGINAL ARTICLE
TAKUMA MAEDA ET AL. THERAPEUTIC MODALITY FOR ELDERLY PATIENTS WITH SAH BASED ON ANEURYSMAL MORPHOLOGY AND LOCATION

tolerated better than neurosurgical clipping among elderly
patients. Our findings indicated that all therapeutic modalities
could be clinically useful, irrespective of the patient’s age.
Instead, the therapeutic modality should be selected based on
the location and morphology of the aneurysm to prevent a late
rerupture that may require additional treatment.
We acknowledge several limitations of this study. First, the
study is limited to data acquired retrospectively from a single
institution. Second, the therapeutic modality used was selected on
a case-by-case basis, which may introduce bias, although both
neurosurgeons and neurovascular physicians were involved in
selecting the appropriate treatment for each case. Third, the pa-
tients’ age may influence this decision because this information
was not blinded to the surgeons, although we found no difference
in the success rate of clipping or coiling between the young and
elderly groups. Further studies are needed to investigate the
clinical efficacy of neurosurgical clipping relative to endovascular
coiling procedures in elderly patients with SAH.
using a therapeutic modality that takes into account the
morphology and the location of the aneurysm, not age or WFNS
grade. Clinical outcomes in the elderly patients with a poor WFNS
grade were poor, irrespective of the therapeutic modality, and they
were linked to higher rates of periprocedural complications as well
as a higher prevalence of underlying physical health problems.
CRediT AUTHORSHIP CONTRIBUTION STATEMENT
Takuma Maeda: Conceptualization, Writing - original draft,
Methodology. Tetsu Satow: Conceptualization, Writing - review &
editing. Go Ikeda: Conceptualization, Writing - review & editing.
Eika Hamano: Writing - review & editing. Naoki Hashimura:
Writing - review & editing. Takeshi Hara: Writing - review &
editing. Masatake Sumi: Writing - review & editing. Masaki
Nishimura: Writing - review & editing. Jun C. Takahashi: Writing
- review & editing.

CONCLUSIONS ACKNOWLEDGMENTS
The clinical outcomes for elderly patients with SAH did not differ We would like to thank Editage (www.editage.jp) for language
between neurosurgical clipping and endovascular coiling when support.

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Conflict of interest statement: T.S. reports grants from Canon
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conflict of interest to declare.
Received 31 March 2020; accepted 26 July 2020
Citation: World Neurosurg. (2020).
https://doi.org/10.1016/j.wneu.2020.07.189
Journal homepage: www.journals.elsevier.com/world-
neurosurgery
Available online: www.sciencedirect.com
1878-8750/$ - see front matter ª 2020 Elsevier Inc. All
rights reserved.
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TAKUMA MAEDA ET AL. THERAPEUTIC MODALITY FOR ELDERLY PATIENTS WITH SAH BASED ON ANEURYSMAL MORPHOLOGY AND LOCATION

SUPPLEMENTARY DATA

Supplementary Table 1. Characteristics of All Patients by Generation

Clipping Coiling

Age (years) £69 70e74 75e79 80e84 ‡85 £69 70e74 75e79 80e84 ‡85

Number of patients 239 39 37 36 12 114 23 12 14 13

Female sex, n (%) 153 (64.0) 29 (74.4) 31 (83.8) 30 (83.3) 12 (100) 47 (41.2) 17 (73.9) 8 (66.7) 12 (85.7) 7 (53.8)
Location of aneurysm, n (%)
Internal carotid artery 73 (30.5) 14 (35.9) 19 (51.4) 13 (36.1) 5 (4.2) 17 (14.9) 9 (39.1) 1 (8.3) 4 (28.6) 7 (53.8)
Middle cerebral artery 83 (34.7) 15 (38.5) 13 (35.1) 15 (41.7) 4 (33.3) 5 (4.4) 0 (0) 0 (0) 0 (0) 1 (7.7)
Distal anterior cerebral artery 15 (6.3) 0 (0) 3 (8.1) 3 (8.3) 2 (16.7) 3 (2.6) 0 (0) 1 (8.3) 2 (14.3) 2 (15.4)
Anterior communicating artery 43 (18.0) 8 (20.5) 1 (2.7) 3 (8.3) 1 (8.3) 26 (22.8) 6 (26.1) 1 (8.3) 2 (14.3) 1 (7.7)
Vertebrobasilar artery 13 (5.4) 2 (5.1) 0 (0) 2 (5.6) 0 (0) 58 (50.9) 8 (34.8) 9 (75.0) 6 (42.9) 2 (15.4)
Poor clinical grade, n (%) 92 (38.5) 15 (38.5) 16 (43.2) 17 (47.2) 9 (75.0) 42 (36.8) 11 (47.8) 10 (83.3) 4 (28.6) 5 (38.5)

Supplementary Table 2. Clinical Outcomes of All Patients by Generation

Clipping Coiling

Age (years) £69 70e74 75e79 80e84 ‡85 £69 70e74 75e79 80e84 ‡85

Outcome at discharge, n (%)

Favorable 154 (64.4) 19 (48.7) 13 (35.1) 5 (13.9) 0 (0) 71 (62.3) 11 (47.8) 1 (8.3) 4 (28.6) 4 (30.8)
Unfavorable 85 (35.6) 20 (51.3) 24 (64.9) 31 (86.1) 12 (100) 43 (37.7) 12 (52.2) 11 (91.7) 10 (71.4) 9 (69.2)
Clinical complication, n (%) 20 (8.4) 7 (17.9) 9 (24.3) 12 (33.3) 5 (41.7) 16 (14.0) 6 (26.1) 5 (41.7) 4 (28.6) 2 (15.4)
Surgical complication, n (%) 55 (23.0) 9 (23.1) 5 (13.5) 9 (25.0) 1 (8.3) 16 (14.0) 5 (21.7) 4 (33.3) 3 (21.4) 1 (7.7)
Rebleeding, n (%) 2 (0.8) 1 (2.6) 1 (2.7) 1 (2.8) 0 (0) 0 (0) 1 (4.3) 0 (0) 1 (7.1) 0 (0)
Within 30 days after the procedure 2 (0.8) 1 (2.6) 1 (2.7) 1 (2.8) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0)
30 days to 1 year 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 1 (4.3) 0 (0) 0 (0) 0 (0)
After 1 year 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 1 (7.1) 0 (0)
Symptomatic vasospasm, n (%) 32 (13.4) 9 (23.1) 9 (24.3) 9 (25.0) 1 (8.3) 19 (16.7) 2 (8.7) 1 (8.3) 1 (7.1) 2 (15.4)
Shunt dependence, n (%) 50 (21.0) 14 (35.9) 12 (32.4) 13 (36.1) 4 (33.3) 27 (23.7) 6 (26.1) 5 (41.7) 3 (21.4) 3 (23.1)

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TAKUMA MAEDA ET AL. THERAPEUTIC MODALITY FOR ELDERLY PATIENTS WITH SAH BASED ON ANEURYSMAL MORPHOLOGY AND LOCATION

Supplementary Table 3. Characteristics and Clinical Outcomes of Elderly Patients in ISAT and BRAT Compared with Our Study
ISAT (Age >65 years) BRAT (Age >65 years) Our Study (Age >75 years)

Number of patients (%) 278 (13.0) 77 (19.0) 124 (23.0)

Age (years) — 71.4  4.8 81.2  4.6
Female sex, n (%) 199 (71.6) — 105 (81.2)
Location of aneurysm, n (%)
Internal carotid artery* 101 (36.3) 28 (36.4) 49 (39.5)
Middle cerebral artery 37 (13.3) 11 (14.3) 33 (26.6)
Distal anterior cerebral artery 136 (48.9) 4 (5.2) 13 (10.5)
Anterior communicating artery 23 (29.9) 10 (8.1)
Vertebrobasilar artery 4 (1.5) 11 (14.3) 19 (15.3)
Poor clinical grade, n (%) 20 (7.2) 18 (28.4) 61 (49.2)
Favorable outcome, n (%) 161 (58.1) 6 (7.8) 27 (21.8)
Rebleeding within 1 year after the procedure, n (%)y 39 (1.8) 2 (0.5) 6 (1.1)

*Including posterior communicating artery aneurysm.

yIncluding all elderly and young patients.

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