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ORIGINAL ARTICLE
Subarachnoid hemorrhage and intracerebral hematoma caused
by aneurysms of the anterior circulation: influence of hematoma
localization on outcome
Markus Bruder &Patrick Schuss &Joachim Berkefeld &
Marlies Wagner &Hartmut Vatter &Volker Seifert &
Erdem Güresir
Received: 2 April 2013 /Revised: 3 April 2014 /Accepted: 18 May 2014 /Published online: 12 July 2014
#Springer-Verlag Berlin Heidelberg 2014
Abstract Additional space-occupying intracerebral hemato-
ma (ICH) in patients suffering from subarachnoid hemorrhage
(SAH) is a known predictor for poor outcome. Emergent clot
evacuation might be mandatory. However, data concerning
the influence of ICH location on outcome is scarce. Therefore,
we analyzed the influence of ICH location on clinical course
and outcome in patients with SAH and additional ICH. One
hundred seventy-four patients were treated with aneurysmal
SAH and additional ICH between September 1999 and May
2012. Information including patient characteristics, treatment,
and radiological findings were prospectively entered into a
database. Patients were stratified according to ICH location
and neurological outcome. Neurological outcome was
assessed according to modified Rankin Scale (mRS). ICH
location was temporal (58.6 %), frontal (28.7 %), and
perisylvian ICH (12.6 %); 63.8 % presented in poor admission
status and favorable outcome was achieved in 35.6 %. In the
multivariate analysis, favorable outcome was associated with
young age, ICH <50 ml, and good admission status. The
location of ICH was not associated with outcome. The current
data confirms that a significant number of patients with ICH
after aneurysm rupture achieve favorable outcome. Prognostic
factor for favorable outcome are “age,”“size of the hemato-
ma,”and “admission status.”The location of the ICH seems
not to be associated with outcome.
Keywords Subarachnoid hemorrhage .Intracerebral
hemorrhage .Aneurysm .Evacuation .Craniectomy
Introduction
Additional intracerebral hematoma (ICH) in patients suffering
from subarachnoid hemorrhage (SAH) due to ruptured intra-
cranial aneurysm is associated with poor neurological out-
come [19]. Patients suffering from SAH and additional ICH
usually present in a critical clinical condition [1,3,6,9,11,14,
22,27]. Beside the initial brain damage, brain edema seems to
be one cause of secondary deterioration and disability [15,
27]. Mortality rates are higher compared to SAH patients
without ICH and rise dramatically in conservative treatment
strategies [9,16,18]. Therefore, initial clot evacuation and
aneurysm occlusion seem mandatory [2,9,14,16,18,22,24,
26], as favorable outcome can be achieved even in poor-grade
patients (Fig. 1)[11,17,21,25]. However, treatment strategies
are still controversially discussed [6,17,24,25]. Several
factors have been associated with favorable outcome, includ-
ing young age, good admission status, and smaller volume of
ICH [1,2,6,11,21,22]. However, data concerning the
influence ofthe location of ICH location on outcome is scarce.
We therefore analyzed our prospectively conducted
neurovascular database of consecutive patients with aneurys-
mal SAH and additional ICH, with special attention to the
location of ICH.
M. Bruder :P. Schuss :H. Vatter :V. Seifert :E. Güresir
Department of Neurosurgery, Johann Wolfgang Goethe University,
Frankfurt am Main, Germany
J. Berkefeld :M. Wagner
Department of Neuroradiology, Johann Wolfgang Goethe University,
Frankfurt am Main, Germany
M. Bruder (*)
Department of Neurosurgery, Goethe-University Frankfurt am Main,
Schleusenweg 2-16, 60528 Frankfurt, Germany
e-mail: markus.bruder@kgu.de
Neurosurg Rev (2014) 37:653–659
DOI 10.1007/s10143-014-0560-8
Patients and methods
From 1999 to 2012, 989 patients with aneurysmal SAH were
treated at our institution. One hundred seventy-four of 989
patients (17.6 %) with SAH suffered from additional ICH
caused by an intracranial aneurysm located in the anterior
circulation. SAH was proven by computed tomography (CT)
or lumbar puncture (Fig. 2). Information including patient
characteristics, treatment specifics, and radiological findings
were prospectively entered into a computerized database
(SPSS, version 19, Chicago, IL). Treatment decision (coiling,
clipping, or hematoma evacuation) was based on an interdis-
ciplinary consensus in each individual case as reported previ-
ously [6]. Patients with signs of cerebral herniation underwent
CT angiography and surgical clipping with simultaneous
evacuation of the space-occupying hematoma. In case of brain
swelling, decompressive craniectomy (DC) was performed by
removing a large bone flap and intracranial pressure (ICP)
probes were inserted as reported previously [7,8]. Patients
who were deemed not suitable to extended surgical proce-
dures due to critical admission status or minor mass effect of
the ICH underwent cerebral angiography and endovascular
treatment. After endovascular treatment, ICP probes were
inserted and ICH was evacuated within a few days using a
burr-hole craniotomy if necessary. Patients were divided into
“good grade”(Hunt and Hess grades I–III) versus (vs.) “poor
grade”(Hunt and Hess grades IV and V) on admission.
According to the ICH volume [12], ICH was divided into
“large”(ICH >50 ml) and “small”(ICH ≤50 ml). According to
the location of the ICH hematoma, patients were divided into
the following groups: frontal, temporal, or perisylvian.
Outcome was assessed according to the modified Rankin
Scale (mRS) after 6 months. Patients were stratified into
favorable outcome (mRS 0–2) and “unfavorable”outcome
(mRS 3–6).
Statistics
Data analyses were performed using the computer software
package SPSS (version 19, SPSS, Chicago, IL). Unpaired t
test was used for parametric statistics. Categorical variables
were analyzed in contingency tables using Fisher’s exact test.
Results with p<0.05 were considered statistically significant.
In a second step, multivariate analyses were performed using a
binary logistic regression analysis to find confounding factors
between potentially independent predictors for unfavorable
outcome. Variables with significant pvalues in univariate
analyses were considered as potentially independent variables
Fig. 1 Favorable outcome according to ICH location (temporal, frontal,
and perisylvian)
Fig. 2 Computed tomographic
(CT) scans obtained
preoperatively, demonstrating
intracerebral hemorrhage in
patients with frontal (a,d),
temporal (b,e), and perisylvian
ICH (c,f) caused by aneurysm
rupture
654 Neurosurg Rev (2014) 37:653–659
in the multivariate analysis. A backward stepwise method was
used to construct multivariate logistic regression models with
the inclusion criterion of a pvalue of <0.05.
Results
Patient characteristics
One hundred seventy-four patients were treated for aneurys-
mal SAH and additional ICH at our institution. Patient char-
acteristics including age, sex, and clinical admission status are
given in detail in Table 1. One hundred fourteen patients
underwent surgical clipping (65.5 %) and 49 were treated
endovascularly (28.2 %; Table 2). Eight of 49 patients
(16.3 %) who underwent endovascular treatment were in
critical clinical condition and therefore not suitable for extend-
ed surgical procedure. In 41 of 49 patients (83.7 %) who
underwent endovascular treatment, ICH was considered to
be with only minor mass effect. However, 8 of these 49
patients (16.3 %) underwent additional hematoma evacuation
during the course of treatment.
Angiographic and radiological findings are given in detail
in Table 3.
Location and size of ICH
One hundred forty of 174 patients (80.5 %) presented with
diffuse SAH and additional ICH (Fisher grade 3), whereas 34
patients (19.5 %) presented with isolated ICH caused by a
ruptured intracranial aneurysm (Fisher grade 4). Location of
ICH was frontal in 102 patients (58.6 %), temporal in 50
patients (28.7 %), and perisylvian in 22 patients (12.6 %).
Fifty-four patients (31 %) suffered from large ICH >50 ml.
Patients with temporal location of ICH suffered significantly
more often from large ICH >50 ml compared to patients with
frontal location of ICH (p< 0.05, OR 2.1, 95 % CI 1.0–4.3;
Table 1).
Patients harboring perisylvian ICH were significantly more
often female compared to patients with ICH at any other
location (p<0.05, OR 3.6, 95 % CI 1.2–11.2).
Aneurysm size and location
Mean aneurysm size was 7.5 ±4.9 mm.
Aneurysms were located at the middle cerebral artery
(MCA) in 76 patients (43.7 %), at the anterior communicating
artery (AcomA) in 54 patients (31.0 %), at the anterior cere-
bral artery (ACA) in 13 patients (7.5 %), and at the internal
carotid artery (ICA) in 31 patients (17.8 %). Patients with ICH
located frontally suffered more often from ruptured aneurysm
of AcomA (52.9 %). Patients with temporal and/or perisylvian
location of ICH presented most frequent with ruptured aneu-
rysm located at the MCA (76 and 91 %). All patients harbor-
ing aneurysms at the AcomA, A2, and distal ACA suffered
from frontal location of ICH (Table 3).
Aneurysm treatment and additional ICH evacuation
One hundred fourteen of 174 patients (65.5 %) presenting
with SAH and additional ICH underwent surgical clipping,
whereas 49 patients (28.2 %) underwent endovascular aneu-
rysm treatment.
However, 11 patients (6.3 %) did not undergo any treat-
ment of the ruptured aneurysm or evacuation of the bleeding
due to severe comorbidity and/or long-lasting signs of cerebral
herniation.
Table 1 Patient characteristics
ICH location Frontal (n=102) Temporal (n=50) Perisylvian (n= 22) Total (n=174)
Mean age±SD (year) 54.8±12.8 56.1±13.0 56.9±14.4 55.5±13.0
Female sex 58 (56.9 %) 26 (52.0 %) 18 (81.8 %)* 102 (58.6 %)
Admission status
H&H grade mean±SD 3.7± 1.2 4.0±1.3 3.8± 1.1 3.8± 1.2
H&H grade I–III (good) 41 (40.2 %) 16 (32.0 %) 6 (27.3 %) 63 (36.2 %)
H&H grade IV–V (poor) 61 (59.8 %) 34 (68.0 %) 16 (72.7 %) 111 (63.8 %)
GCS mean 7.8± 4.9 7.2±4.8 8.9± 5.2 7.7± 4.9
Signs of cerebral herniation 15 (14.7 %) 14 (28.0 %) 3 (13.6 %) 32 (18.4 %)
ICH modalities
ICH >50 ml 26 (25.5 %)* 21 (42.0 %)* 7 (31.8 %) 54 (31.0 %)
Isolated ICH (Fisher 4) 20 (19.6 %) 11 (22.0 %) 3 (13.6 %) 34 (19.5 %)
*p<0.01
Neurosurg Rev (2014) 37:653–659 655
Patients with good grade presentation underwent
endovascular treatment more often compared to patients with
poor grade admission status (55.1 vs. 29.8 %; p<0.005) and
had significantly more often ICH volume less than 50 ml
compared to patients treated surgically (83.7 vs. 63.2 %;
p<0.05).
Overall, ICH evacuation was performed in 75 patients
(43.1 %).
Sixty-seven of 114 surgically treated patients (58.7 %)
underwent subsequent ICH evacuation. In all of these 67
surgically treated patients, ICH evacuation was performed
during the clipping procedure.
Eight of 49 endovascularly treated patients (16.3 %)
underwent subsequent ICH evacuation. In seven of eight
endovascular-treated patients with ICH evacuation, surgical
hematoma evacuation was performed immediately following
the endovascular treatment, whereas one patient received ICH
evacuation before the endovascular procedure.
Patients with poor clinical status on admission underwent
significantly more often surgical ICH evacuation compared to
patients with good clinical status (81 vs. 51 %; p<0.001).
Patients with large ICH >50 ml underwent ICH evacuation
significantly more often compared to patients with small ICH
≤50 ml (70 vs. 31 %; p<0.001, OR 5.3, 95 % CI 2.6–10.7).
Patients with frontal-located ICH underwent surgical ICH
evacuation less often when compared to patients with tempo-
ral or persylvian location (30.4 vs. 60 vs. 63.9 %; p<0.01).
Decompressive craniectomy
Forty-eight patients (27.6 %) weretreated with decompressive
craniectomy (DC).
Patients with large ICH underwent DC significantly more
often than patients with small ICH (41 vs. 22 %; p< 0.01, OR
2.5, 95 % CI 1.2–5.0).
Patients with poor grade admission status underwent DC
more often than patients with initial good grade admission
status (79 vs. 21 %; p<0.01, OR 2.8, 95 % CI 1.3–6.0).
DC was performed in a primary fashion together with the
initial aneurysm treatment or ICH evacuation in 38 of 48
patients (79 %). Ten patients (21 %) were treated with sec-
ondary DC due to intractable elevated ICP during treatment
course. In detail, six patients underwent secondary DC due to
space-occupying infarction and four patients due to progres-
sive brain edema.
DC was performed significantly more often in patients with
ICH located perisylvian (p<0.05, OR 3.1, 95 % CI 1.2–7.8;
Table 2).
Functional outcome
Overall, favorable outcome was achieved in 62 patients
(35.6 %).
According to the location of ICH, favorable outcome was
achieved in 24 of 50 patients (48 %) with temporal ICH vs. 37
of 102 patients (36 %) with frontal ICH vs. 4 of 22 patients
(18 %) with perisylvian ICH.
In patients with good grade admission status, favorable
outcome was achieved in 38 of 63 patients (60 %) vs. in 27
of 111 patients (24 %) with poor grade admission status
(p<0.001, OR 4.7, 95 % CI 2.4–9.2).
Patients with favorable outcome were significantly youn-
ger compared to patients with unfavorable outcome (52±
11 years vs. 57±14 years; p<0.05).
Table 2 Treatment modalities
ICH location Frontal (n=102) Temporal (n=50) Perisylvian (n= 22) Total (n=174)
Aneurysm occlusion
Microsurgery 61 (59.8 %) 36 (72.0 %) 17 (77.3 %) 114 (65.5 %)
Endovascular 35 (34.3 %) 10 (20.0 %) 4 (18.2 %) 49 (28.2 %)
No aneurysm treatment 6 (5.9 %) 4 (8.0 %) 1 (4.5 %) 11 (6.3 %)
Decompressive therapy
ICH evacuation 31 (30.4 %)* 30 (60.0 %)* 14 (63.6 %)* 75 (43.1 %)
Hemicraniectomy 24 (23.5 %)** 13 (26.0 %)** 11 (50.0 %)** 48 (27.6 %)
*p<0.01 Chi Quadrat, Pearson; **p<0.05 Chi Quadrat, Pearson
Table 3 Aneurysm site
Frontal (n=102) Temporal (n=50) Perisylvian (n=22) Total (n= 174)
ICA 17 (16.7 %) 12 (24.0 %) 2 (9.0 %) 31 (17.8 %)
ACA 13 (12.7 %) 0 0 13 (7.5 %)
AcomA 54 (52.9 %) 0 0 54 (31.0 %)
MCA 18 (17.7 %) 38 (76.0 %) 20 (91.0 %) 76 (43.7 %)
656 Neurosurg Rev (2014) 37:653–659
Patients with small ICH (≤50 ml) achieved favorable out-
come significantly more often when compared to patients with
large ICH (43 vs. 26 %; p<0.05, OR 2.1, 95 % CI 1.04–4.3).
Patients with endovascular aneurysm treatment achieved
favorable outcome in 51 % compared to 34 % of patients with
microsurgical aneurysm treatment (p<0.05).
The overall mortality was 31.6 %.
Signs of cerebral herniation
Overall, 32 patients (18.4 %) presented with signs of cerebral
herniation. Favorable outcome was achieved in 7 of 32 pa-
tients (22 %) with signs of cerebral herniation compared to 58
of 132 patients without signs of cerebral herniation (44 %;
p<0.001, OR 3.919, 95 % CI 1.623–9.460).
Multivariate analysis
We performed a multivariate logistic regression analysis of
those variables significantly associated with favorable out-
come in patients with SAH and ICH in the univariate analysis.
The multivariate regression model did illustrate the variable
“younger age”(p< 0.01, OR 1.03, CI 95 % 1.01–1.1), “good
clinical status on admission”(p<0.001, OR 3.4, CI 95 % 1.7–
7.1), and the absence of “signs of cerebral herniation”
(p<0.05, OR 2.8, 95 % CI 1.1–7.3) to be significantly related
to favorable outcome.
Discussion
Patients with SAH and additional ICH caused by ruptured
intracranial aneurysms usually present in poor clinical condi-
tion and achieve unfavorable outcome [1,6,11,14,15,19,
22]. However, several studies reported favorable outcome in
these critically ill patients [1,6,11,14,19,25]. We analyzed
our institutional data of 174 patients with SAH and additional
ICH. The multivariate analysis revealed “younger age,”“good
clinical status on admission,”and “no signs of cerebral herni-
ation”as independent and significant predictors for favorable
outcome.
Of patients with SAH and additional ICH, 35.6 % achieved
favorable outcome in the present series. Therefore, despite the
critical clinical condition, patients with SAH and additional
ICH might achieve favorable outcome [1,9,13,16,18,24,
26].
Treatment modality
If a surgical procedure is necessary in order to evacuate a space-
occupying ICH, concomitant surgical treatment of the ruptured
aneurysm seems desirable to avoid a second therapeutic
procedure in these critically ill patients. In the present series,
endovascular treatment of the ruptured aneurysm was per-
formed in 28.2 % of patients with SAH and ICH, because of
minor mass effect of ICH or their critical clinical condition.
However, if patients with SAH suffer from additional space-
occupying ICH, surgical treatment of the ruptured aneurysm
seems mandatory due to the possibility of clot evacuation and/
or incorporation of decompressive craniectomy into the proce-
dure. Tawk et al. reported favorable outcome in 61 % of patients
treated with endovascular treatment and subsequent ICH evac-
uation during treatment course [25]. A combined endovascular
and surgical technique in patients with SAH and additional ICH
might be a promising alternative for this particular patient
population [5,25]. Nevertheless, careful individual and inter-
disciplinary decision making is necessary in these critically ill
patients.
Influence of clinical status on admission and DC
Patients suffering from SAH with additional ICH usually
present in poor clinical condition [1,13,22]. The admission
status has been reported to be a predictor for functional out-
come in these patients [1]. In the present study, patients with
poor clinical status on admission underwent significantly
more often surgical ICH evacuation compared to patients with
good clinical status (81 vs. 51 %; p<0.001).
Several studies suggested early and aggressive ICH evac-
uation in combination with decompressive craniectomy in
order to reduce elevated ICP and to improve functional out-
come [4,17,22,23]. In the present series, DC was performed
in a primary fashion together with the initial aneurysm treat-
ment in 79 % of patients with DC. Subsequently, 21 % of
patients with DC underwent secondary DC due to intractable
elevated ICP during treatment course.
In patients with SAH and additional ICH, signs of cerebral
herniation might occur due to the space-occupying effect of
ICH alone or secondary due to intractable elevated ICP. Signs
for cerebral herniation are known to predict poor outcome,
most often reported in patients with traumatic brain injury [6,
10,20]. However, favorable outcome was achieved in 22 % of
these critically ill patients. Therefore, especially in patients
with signs of cerebral herniation for only a short-term period,
immediate treatment might be warranted. Nevertheless, these
results should be interpreted carefully and careful individual
decision making is necessary in these critical clinical
situations.
Localization and size of ICH
The most frequent aneurysm localization causing additional
ICH is the MCA followed by the AComAwhich is in line with
the literature [1,9,12–14,16–18]. Only few reports
concerning the impact of hematoma localization are available
Neurosurg Rev (2014) 37:653–659 657
and results are inconclusive [11,22]. In a recent study [11],
favorable outcome was achieved in 50 % of patients with
SAH and frontal ICH, in 30 % of patients with perisylvian
ICH, and in none with temporal ICH. In contrast, Shimoda
et al. [22] reported a higher rate of favorable outcome in
patients with temporal hematoma. The present study revealed
no significant impact of ICH location on outcome in the
multivariate analysis.
The volume of ICH has previously been identified as a
predictor for unfavorable outcome [6]. In the present analysis,
ICH >50 ml was associated with unfavorable outcome. ICH
>50 ml was significantly more often identified in patients with
temporal ICH compared to patients with ICH located frontal-
ly. However, neither size nor location of ICH is an indepen-
dent predictor of favorable outcome in the present multivariate
analysis.
Limitations
The present study has several limitations, especially its retro-
spective design. Patients were not randomized and, therefore,
selection bias is possible. Furthermore, the results of the
present study represent only a single-center experience. The
acute clinical circumstances of admission in this highly se-
lected patient group might have affected treatment strategy
and favored surgical repair of the ruptured aneurysm.
However, treatment was on an interdisciplinary consensus in
each individual case.
Conclusions
Patients with SAH and additional ICH usually present in a
critical condition with poor prognosis. Nevertheless, a consid-
erable number of patients might achieve favorable outcome.
The location of the ICH seems not to be associated with
outcome.
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Comments
Lotfi Hacein-Bey, Sacramento, USA
The article by Bruder et al. in this issue of Neurosurgical Review
underscores a number of challenges encountered in managing patients
with cerebrovascular hemorrhage. This large series from a recognized
academic European center confirms that the best predictors of good
outcomes in patients with SAH complicated by ICH are young age, good
grade on admission, and absence of complicating signs, i.e., herniation.
Conversely, the factors which had the greatest impact on outcome were
poor grade upon admission, surgical versus endovascular management of
the ruptured aneurysm, and hematoma location (perisylvian location
being the worst).
The role of clinical grade upon admission, the effects of SAH, and the
differences between treatment techniques have been amply recognized.
However, the impact of cerebral hematomas is less clearly
appreciated.
First, hematomas alone may result in cerebral edema, tissue damage,
and increased vascularity as macrophage infiltration and astrocyte prolif-
eration around hematomas produce secretory factors such as vascular
endothelial growth factor (VEGF), matrix metallopeptidase 9 (MMP-9),
various interleukins, tumor necrosis factor-a, and aquaporin water chan-
nels. VEGF induces angiogenesis and neo-vascularity in the wall of the
hematoma, seen as ring-enhancing lesions on imaging studies. MMPs
degrade extracellular matrix proteins, including the neurovascular basal
lamina and tight junction proteins of the blood-brain barrier (BBB). BBB
disruption results in edema formation. Therefore, hematoma removal not
only results in alleviating mass effect, but also reduces brain edema, tissue
damage, and increased risk of re-hemorrhage.
Another major fact about hematomas is that they may induce
derangements in brain function by causing damage to neural
networks. Frontal and temporal hematomas may affect major brain
networks such as the default mode network (medial prefrontal
cortex, posterior cingulum, and medial temporal lobe) and the
central executive network (dorsolateral prefrontal cortex). The
observation that perisylvian hemorrhage was associated with par-
ticularly poor outcomes in this series may be explained in part by
the proximity to deep nuclei and eloquent midline structures.
However, an important reason for this phenomenon may be the
disruption of structural connectivity between the insula and other
brain regions. The insular cortex has been recently described as
the “limbic integration cortex”after anatomical connectivity stud-
ies have shown major efferent and afferent connections to the
amygdala, olfactory cortex, or cingulum. A major neural network,
the salience network, which consists of three main cortical areas
(the dorsal anterior cingulate cortex, the anterior right insula, and
the left insula) plays an important role in the initiation of cogni-
tive control, the implementation of tasks, and the coordination of
behavioral responses. As continued progress is made in noninva-
sive mapping of white matter pathways around the insular cortex,
there is no doubt that the importance of the salience network in
integrating physiological control and monitoring emotional life
will be further elucidated.
This article is a useful and humbling reminder of how difficult the task
of a surgeon is and how little we still know about brain functional
networks.
Andreas Raabe, Bern, Switzerland
The prognosis of patients with spontaneous intracerebral hemorrhage
(ICH) is usually poor, and we would expect that a combination of ICH
and subarachnoid hemorrhage (SAH) further deteriorates the chance of a
favorable outcome. Patients with ICH and SAH usually present in a
poorer clinical admission state and with a more dramatic clinical picture.
Thus, we would again expect a rather poor outcome, given the fact, that
the initial presentation influences the prognosis considerably. However,
the present study demonstrated that a “combined”poor outcome effect of
SAH and ICH is less likely. It favors an active management with surgical
removal of a space-occupying hematoma and aneurysm clipping instead
of a more pessimistic ICH-like approach.
Neurosurg Rev (2014) 37:653–659 659
