Acta Neurochir
DOI 10.1007/s00701-014-2225-3
CLINICAL ARTICLE - VASCULAR
Frequency, risk of hemorrhage and treatment considerations
for cerebral arteriovenous malformations with associated
aneurysms
Johannes Platz & Joachim Berkefeld & Oliver C. Singer &
Robert Wolff & Volker Seifert & Jürgen Konczalla &
Erdem Güresir
Received: 16 July 2014 / Accepted: 1 September 2014
# Springer-Verlag Wien 2014
Abstract
Background Data on arteriovenous malformations (AVMs) of
the brain with AVM-associated aneurysms (AAA) are scarce.
This study addresses the incidence, rate of hemorrhage, treat-
ment strategies and stability during follow-up in a
neurovascular center.
Methods We retrospectively reviewed patients harboring an
AVM with at least one AAA treated at our neurovascular
center between 2002 and 2013.
Results Of 216 patients, 59 (27.3 %) had at least one AAA
(n=92 aneurysms total). Compared to patients without AAA,
hemorrhagic presentation occurred more frequently (61.0 %
versus 43.9 %, p=0.025), and the rate of infratentorial AVMs
was higher (37.3 % versus 16.6 %, p=0.001). The aneurysm
was the origin of the bleeding in most cases, most often
Parts of this study were presented as an abstract at the annual meeting of
the DGNC in 2013.
Electronic supplementary material The online version of this article
(doi:10.1007/s00701-014-2225-3) contains supplementary material,
which is available to authorized users.
J. Platz (*) : V. Seifert : J. Konczalla : E. Güresir
Johann Wolfgang Goethe-University, Department of Neurosurgery,
Schleusenweg 2-16 D, 60528 Frankfurt am Main, Germany
e-mail: platz@med.uni-frankfurt.de
J. Berkefeld
Johann Wolfgang Goethe-University,
Department of Neuroradiology, Frankfurt am Main, Germany
O. C. Singer
Johann Wolfgang Goethe-University,
Department of Neurology, Frankfurt am Main, Germany
R. Wolff
Gamma Knife Center, Johann Wolfgang Goethe-University,
Frankfurt am Main, Germany
categorized as a feeding artery aneurysm. Overall, the first
and recurrent hemorrhage were associated with a high mor-
tality and morbidity (15.3 % and 39 %, respectively). Aneu-
rysms were treated by coiling (n=21), surgery (n=18), or
embolizaton with liquid embolization agents (n=11). All an-
eurysms treated by embolization and surgery remained oc-
cluded during follow-up (mean follow-up 39.0±45.0 months).
However, in incomplete AVM obliteration, significant recur-
rence of the treated aneurysm was noted after endovascular
coiling (37.5 %), which may be related to the persistence of
pathological blood flow.
Conclusion In our series, AAA was a significant risk factor
for hemorrhage and was associated with a poor outcome. It
seems worthwhile to consider whether the aneurysm itself is a
risk factor or only an epiphenomenon of severely altered
hemodynamics induced by these special AVMs and therefore
only the most common site of rupture. As the complication
rate was low for aneurysm occlusion, we recommend treating
these aneurysms whenever possible. Furthermore, obliteration
of the AVM should be strived for as this subtype may be
associated with an increased risk of hemorrhage.
Keywords Aneurysm treatment . AVM treatment . Cerebral
arteriovenous malformation . Intracranial aneurysm .
Intracranial hemorrhage
Abbreviations
AAA AVM-associated aneurysm
AVM Arteriovenous malformation
DSA Digital subtraction angiography
LEA Liquid embolic agents
mRS Modified Rankin Scale

Background
Cerebral AVMs are rare congenital lesions associated with a
risk of hemorrhage of 1 to more than 4 % per year [1–4]. This
rate varies according to various features of the AVM such as the
location, draining pattern, or history of previous hemorrhage.
Since the publication of the long-anticipated randomized trial
on unruptured brain AVMs (ARUBA), many issues and ques-
tions have arisen [5]. One of the most important issues may
become the selection of AVM patients considered for treatment.
Therefore, risk factors of AVMs need to be identified clearly.
The presence of AVM-associated aneurysms (AAAs) is
thought to influence the hemorrhage rate. AAAs can be clas-
sified as feeding artery aneurysms (type 1), nidal aneurysms
(type 2), and aneurysms not associated with the AVM (type 3,
Fig. 1) [6]. Type 1 aneurysms can be further divided into
proximal (type 1a, aneurysm closer to the circle of Willis than
to the AVM) and distal (type 1b, aneurysm closer to the AVM).
Due to limitations and biases of case series, data concerning
the bleeding risk of AAAs are inconsistent. Publications deal-
ing with the question of whether AAAs present an independent
risk for hemorrhage yielded contradictory results [7–20].
We reviewed our series of AVM patients to determine the
frequency of associated aneurysms, treatment strategies and
clinical results.
Patients and methods
We retrospectively identified all patients with cerebral AVMs
who presented at our center between February 2002 and
March 2013. This study was approved by the local ethics
committee. Initially, each case was evaluated on the basis of
digital subtraction angiography (DSA) by a neurovascular
team consisting of neurosurgeons, neuroradiologists, neurol-
ogists and radiosurgeons. DSA consisted of a four-vessel
angiogram in all patients, which was carefully reviewed for
the presence of AAA. Only in selected patients with a poor
clinical status after hemorrhage were CT angiography or MR
angiography accepted as sufficient if the AVM and aneurysm
could be clearly identified.
Patients with at least one type 1 or type 3 aneurysm were
included. AAAs were defined as arterial saccular dilations of
the lumen with at least the double diameter of the vessel
carrying it. Cases with insufficient workup or with infundib-
ula, arterial ectasias and venous aneurysmal ectasias were
excluded. In our institution, we do not aggressively search
for intranidal (type 2) AAAs, which may easily be missed
without selective catheterization of the different feeding arter-
ies. Therefore, those AAAs were not inclusion criteria.
According to the patients’ records and imaging findings,
we determined the rate of ruptured and unruptured aneurysms.
Hemorrhage was defined as a symptomatic event with blood
Acta Neurochir
on imaging or in the cerebrospinal fluid. To define the origin
of the hemorrhage, multimodal imaging was used (including
multiplanar reconstructions and angiography techniques in
CT, DSA or MRI) as well as analysis of the blood distribution,
anatomic relationship of the AVM and the aneurysm(s) to the
hemorrhage and, if available, intraoperative findings. In an
interdisciplinary consensus, the origin of the hemorrhage
could be distinguished as either aneurysmal or AVM-related
in most cases (Fig. 2).
Five patients were partially treated at other institutions: one
surgical aneurysm occlusion, one partial aneurysm emboliza-
tion, one partial aneurysm and AVM embolization (all because
of hemorrhage prior to presentation to our center), one surgi-
cal AVM excision and one combined treatment.
Aneurysm treatment
The indication for aneurysm treatment was determined by
interdisciplinary consensus between the neurovascular special-
ists based on the patient’s clinical condition and imaging find-
ings. The best treatment option was chosen interdisciplinarily
between endovascular and microneurosurgical techniques.
In ruptured aneurysms, we usually focused on the aneu-
rysm without striving for definite treatment of the AVM,
aiming for aneurysm occlusion within 24 h.
In unruptured aneurysms, we developed an individualized
treatment strategy independently from the AVM assuming that
the risk of AAA rupture might be at least as high as in the ISUIA
study [21]: in case of surgical excision of the AVM, the aneurysm
was treated in the same procedure when technically feasible. For
all others, more remote AAAs, the treatment was planned indi-
vidually, bearing in mind that there are reports of aneurysm
shrinkage after successful AVM treatment [6, 20, 22–24].
Endovascular aneurysm treatment
Endovascular treatment was performed under general anes-
thesia after administration of 5,000 IU of heparin and included
aneurysm coiling or embolization with liquid embolization
agents (LEA), sometimes including parent artery occlusion.
Various types of platinum coils were used during the treatment
period as well as different LEAs (Onyx and Histoacryl).
Aneurysms were packed with coils as densely as possible. In
selected patients, the balloon remodeling technique was ap-
plied and/or an endovascular stent was placed. Heparinization
was routinely continued for 24 to 48 h afterwards (goal:
activated clotting time 1.5× normal).
Microsurgical aneurysm treatment
Clipping of the aneurysm was the primary goal using standard
microneurosurgical methods [25, 26]. For confirmation of
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Fig. 1 Types of aneurysms

associated with AVMs. (a) Type
1a: “Proximal feeding artery
aneurysm,” meaning that the
aneurysm is located closer to the
circle of Willis on the feeding
artery than to the AVM nidus. (b)
Type 1b: “Distal feeding artery
aneurysm,” meaning that the
aneurysm is located closer to the
AVM nidus than to the circle of
Willis on the feeding artery (white
arrow). Note the additional type
1a aneurysm in this patient (black
arrow). (c) Type 1b: Multiple
aneurysms. (d) Type 3: Aneurysm
not associated with the AVM
(white arrow). In this case, the
AVM was supplied by vessels
of the MCA and ACA only;
therefore, the ruptured basilar
tip aneurysm was categorized
as type 3

complete aneurysm occlusion, all patients underwent DSA
about 1 week after surgery.
AVM treatment
AVM treatment was always planned by the interdisciplinary
neurovascular team. After AVM rupture, treatment of the
AVM was deferred for 4 to 6 weeks if there was no life-
threatening condition. AVM treatment was chosen among
neurosurgical excision with or without preoperative partial
embolization, embolization alone or radiosurgery (see Sup-
plemental Figure 2 for radiosurgery details). In case of AVM
rupture, radiosurgery was only chosen if the location or
angioarchitecture of the AVM prevented definitive neurosur-
gical or endovascular AVM treatment.
Follow-up
Follow-up was obtained during outpatient visits using the mod-
ified Rankin cale (mRS). Alternatively, a telephone interview

Fig. 2 Determining the origin of

hemorrhage. Using
multidirectional reconstruction,
the origin of the hemorrhage
could be detected in most cases as
shown here: In this patient, clearly
the aneurysm (white arrow) is the
source of the intraventricular
hemorrhage (*), while the nidus
of the AVM is located remotely
(black arrow)

was performed. Outcome was dichotomized into favorable
(mRS 0 to 2) and poor (mRS 3 to 6). Neurologic deficits were
classified as hemorrhage and/or treatment related.
As occlusion of all AAAs and AVMs could not always be
achieved safely, patients with selective treatment of AAAs
and/or the AVM were included. In case of incomplete treat-
ment, serial MR imaging studies were acquired using intervals
of 1 to 2 years.
Statistical analysis
Demographic parameters and AVM characteristics between
AVM patients with and without AAA were compared. All
statistical analyses were performed using commercially avail-
able software (SPSS 20.0, IBM, 2012). P-values<0.05 were
considered significant. The χ2 and Mann-Whitney U tests
were used as appropriate.
Results
Patient characteristics
At least one AAA was found in 59 of 216 AVM patients
(27.3 %, Table 1). Patients with AAAs were older (47.3±
15.0 years vs. 38.3±15.7 years, p<0.001). There was a slight
male preponderance in our series (52.1 %), while aneurysms
tended to be more frequent in females. Grading of the AVMs
according to the Spetzler-Martin Scale was similar between
the two groups. However, the AVM was located significantly
more often infratentorially in patients with AAA (37.3 % vs.
16.6 %, p=0.001). Patients with AAA presented significantly
more often with hemorrhage (p=0.044).
Ninety-two aneurysms were detected in 59 patients (mean
1.6 aneurysms/patient; range: 1–5 aneurysms/patient). Multi-
ple AAAs were present in 20 patients. The mean diameter of
all aneurysms was 5.0±3.5 mm (2–21 mm, median 4.0 mm).
Angiographically, most of these AVMs were classified as
high-flow malformations. Feeding artery aneurysms were pre-
dominant: 61 aneurysms were categorized as type 1a and 15
aneurysms as type 1b. Seven aneurysms were categorized as
intranidal (type 2) and nine as unrelated (type 3).
Aneurysm-related hemorrhage
The aneurysm was the origin of the bleeding in 33 of 35
patients (94.2 %) who presented with hemorrhage initially.
Hemorrhage was subarachnoidal in 26, intraventricular in 1
and intracerebral in 6 patients. The aneurysm was classified as
type 1a in 25, type 1b in 4 and type 3 in 4 patients. In two
patients with intracerebral hematomas and a type 1b aneurysm,
the source of the hemorrhage could not be identified definitely.
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Overall, 39 aneurysm-related hemorrhages were docu-
mented in this series: additionally to the 33 initial ruptures, 6
delayed ruptures occurred (Fig. 3). Ruptured aneurysms were
larger in diameter (6.25±4.2 vs. 4.17±2.6 mm, p<0.001) and
were supplied by vessels of the posterior circulation more
often (66.7 % vs. 19.6 %, p<0.001).
AVM-related hemorrhage
Delayed AVM hemorrhage occurred in nine patients. Of
those, six had suffered from previous AAA-related hemor-
rhage but without obliteration of the AVM. Outcome after
delayed AVM-related hemorrhage was poor in four patients
including two fatal cases.
Aneurysm treatment
Ruptured aneurysms Three patients were not treated after
aneurysmal hemorrhage: because of the poor clinical status
in two patients (both fatal) and the patient’s refusal [80 years
of age; no re-hemorrhage during follow-up (73 months)].
Surgery was performed in 7 of 33 patients presenting with
aneurysm-related hemorrhage. The aneurysm was clipped suc-
cessfully in six patients, but in one patient, the AAA and AVM
could not be secured because of intraoperative hemorrhage, and
the patient died shortly after. Twenty-three patients presenting
with a ruptured aneurysm were treated endovascularly (n=9 by
embolization with LEA and n=14 by coiling; Table 2).
Unruptured aneurysms
In 26 patients, 59 AAAs were discovered without previous
rupture. Two were found in patients with a fatal hemorrhage
from another aneurysm. Of the remaining 57 aneurysms (36
type 1a, 9 type 1b, 7 type 2 and 5 type 3 AAAs), 21 were
treated: 7 by coiling (6 type 1a, 1 type 3 AAAs), 2 by
embolization (2 type 1b AAAs) and 12 surgically (6 type 1a,
4 type 1b, 1 type 2, 1 type 3 AAAs; Table 2).
Thirty-eight aneurysms were observed without treatment.
Untreated aneurysms were small (mean 4.6±3.5 mm). Rea-
sons for conservative treatment were denial of the patient,
multiple small aneurysms in complex high-grade AVMs,
small aneurysm size or an increased interventional risk be-
cause of patient or aneurysm characteristics.
AVM treatment
Overall, 34 AVMs were treated (radiosurgery n=13, emboli-
zation n=9, surgery n=8, embolization and surgery n=4)
including 27 unruptured AVMs. Complete AVM occlusion
was achieved in 17 (50 %) patients (8 surgical, 4 embolization
and surgery, 4 radiosurgery, 1 embolization). In the patients
without complete obliteration, radiosurgery was repeated
Acta Neurochir

Table 1 Comparison of the patients harboring an AVM with and without associated aneurysms. Patients with AAAs were older at diagnosis and had
AVMs supplied only by one vessel territory (no borderzone AVM) more often, and the AVMs were more often located infratentorially

AVMs

With aneurysm Without aneurysm p-value OR (95 % CI)

n=59 n=157
Age (mean) 47.3+15.0 38.3±15.7 <0.001°
Sex 31 f:28 m 73 f:84 m 0.428* OR 0.79 (0.43-1.43)
Spetzler-Martin grade 10:17:22:9:1 35:46:55:21:0 0.490*
Borderzone AVM38 15 (25.4 %) 62 (39.5 %) 0.064* OR 0.54 (0.27-1.04)
Supratentorial 37 (62.7 %) 131 (83.4 %) 0.001* OR 3.00 (1.53-5.88)
Infratentorial 22 (37.3 %) 26 (16.6 %)
Hemorrhage at presentation 36 (61.0 %) 69 (43.9 %) 0.025* OR 2.00 (1.08-3.68)

More patients with AAAs presented with hemorrhage. The Spetzler-Martin grade gives the number of patients with grade 1–5. *χ2 test; °Mann-Whitney
U test

because of incomplete AVM occlusion in one patient, while
eight patients are still being followed after radiosurgery
waiting for obliteration.
Outcome
Overall outcome Mean follow-up was 37.8±44.7 months (0–
250 months, median 26.0 months). Outcome was favorable in
42 patients (71.2 %). The initial hemorrhage was fatal in six
patients (10.2 %). Three patients (5.1 %) died after delayed
hemorrhages (total hemorrhage-related mortality: 15.3 %). A
new deficit related to the hemorrhage occurred in 23 patients
(39.0 %), due to treatment in 3 patients (5.1 %; mRS 1, 2 and 3
in one patient, each) and due to hemorrhage and AVM treat-
ment in 2 patients (3.4 %; mRS 2 and 6; both patients were
initially unconscious when admitted but showed new lesions

Fig. 3 Aneurysm treatment and follow-up. Fifty-nine patients with a
total of 92 AVM-associated aneurysms (AAA) were included in this
study. In this figure, each AVM is shown with one index aneurysm only.
In 19 patients, more than one AAA was detected. In these cases, only the
first symptomatic aneurysm or the first treated AAA was included in this
figure for reasons of clarity. The AVMs were stratified by the initial
symptoms into (1) incidental, (2) initial hemorrhage and (3) delayed
hemorrhage, meaning initially incidental findings in which hemorrhage
occurred before treatment. *Delayed hemorrhage occurred in 6 patients.
°Including one clipping of one initially incompletely coil-occluded AAA
and one AAA recurrence during GK latency that was then treated by
clipping; later on, the AVM was obliterated completely. $Repeated hem-
orrhage of the AVM occurred in this patient. GK,Gamma Knife; OP,
surgical treatment; ev,endovascular treatment, including coiling and em-
bolization with glue

Table 2 Treatment and follow-up of the 92 aneurysms in this series. Stable means unchanged occlusion after treatment or no change in aneurysm size
without treatment
Aneurysm rupture Aneurysm treatment
No initial hemorrhage No treatment (n=38)
(n=59)
Aneurysm treated by Surgery (n=12)
Coiling (n=7)
Embolization (n=2)
Initial hemorrhage No treatment (n=3)
(n=33)
Aneurysm treated by Surgery (n=6)
Coiling (n=14)
Embolization (n=9)
Unsuccessful (n=1)
*First, aneurysm growth or de novo formation was noted, respectively, then the aneurysm was treated. °In one patient, early recurrence after coiling was
noted before she died subacutely from the initial hemorrhage
after treatment on imaging, making it impossible to discrim-
inate between the effect of hemorrhage and treatment on the
patients’ outcome). Overall, treatment-associated morbidity in
this series adds up to 8.5 %.
Outcome without initial hemorrhage
There were 24 patients in whom the AVM and AAA
were diagnosed without previous rupture. Mean follow-
up for those patients was 53.9 ± 57.6 months. During
follow-up, delayed hemorrhage occurred in six patients
(3 AAA and 3 AVM related, Fig. 3). In 12 patients, the
AAA was secured, and in 17 patients, the AVM was
treated. Complete AVM obliteration was achieved in
seven patients, while six patients are still under observa-
tion after radiosurgery. Outcome was favorable in 22
patients (91.7 %) and unfavorable in two patients (mRS
3 and 6). Unfavorable outcome was related to AVM
treatment in one patient, and another patient suffered
from fatal hemorrhage of the AVM briefly before the
scheduled Gamma Knife therapy.
Follow-up of the aneurysms
Ruptured aneurysms As 6 patients died initially, 29 ruptured
aneurysms were available for follow-up. One untreated AAA
remained stable (73 months, as mentioned above). The aneu-
rysm was stable in another 23 patients. Aneurysm recurrence
was detected in five patients; additionally, early recurrence
was noted in one patient, who did not survive the initial
hemorrhage.
Acta Neurochir
Aneurysm follow-up
Fatal hemorrhage Stable Recurrence Regression Growth De novo formation
2° 34 1 1*
11 1*
5 1° 1*
2
2° 1
6
3° 7 5°
1° 8
1°
Unruptured aneurysms
Of 57 unruptured aneurysms available for follow-up, 35 were
not treated initially. One aneurysm showed spontaneous
shrinkage after spontaneous partial thrombosis of the AVM.
Two aneurysms were classified as de novo as they developed
during follow-up. Recurrence was detected in one patient after
aneurysm coiling. All other treated aneurysms were stable
during follow-up.
Overall
Overall, 50 aneurysms were treated (Table 2). Thirty-nine
(78 %) remained occluded during follow-up: 21 ruptured
aneurysms and 18 unruptured aneurysms. All aneurysms
treated surgically or with LEA stayed occluded independently
of the degree of AVM obliteration. However, in 6 of 21 AAAs
treated by aneurysm coiling, recurrence of the formerly oc-
cluded aneurysm was noted (28.6 %, Fig. 4a-f, Table 2). All
six had type 1a aneurysms and incompletely occluded AVMs.
A second procedure was performed in three patients: one
repeated coiling and one clipping (Fig. 5a-f). In the third
patient, the initially ruptured PICA aneurysm had been treated
by subtotal coiling elsewhere. Later, the patient presented to
our center, where the AVM and residual aneurysm were
treated surgically.
Furthermore, de novo aneurysm formation was noticed in
two patients (both type 1a), while another aneurysm (type 3)
in one of these patients increased in diameter. Only one type
1a aneurysm diminished after spontaneous partial thrombosis
of the AVM. Four untreated type 1a aneurysms stayed
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Fig. 4 After acute SAH (a), an

occipital AVM (Spetzler-Martin
grade 4) with a type 1a aneurysm
of the basilar tip was diagnosed
(b, c) in this 51-year-old patient.
The ruptured aneurysm was
coiled completely (d). The com-
plex AVM was partially
embolized two times without
achieving complete obliteration.
After 35 months, significant re-
currence of the AAA was detected
(e, f), which was then treated by a
second coiling procedure

unchanged after complete AVM obliteration in four patients
(Fig. 6a-f).
Delayed aneurysmal hemorrhage occurred in five patients:
One patient suffered from recurrent hemorrhage prior to diag-
nosis of the AVM, and complete occlusion of the AAA and
AVM was achieved by embolization and radiosurgery. One
patient with multiple AAAs suffered from delayed hemor-
rhage from a different AAA. Delayed aneurysmal hemorrhage
occurred in one patient 203 months after AVM excision
(mRS=2). Two patients presented without initial hemorrhage.
The outcome was favorable in four (mRS 0=1, mRS 2=3)
and unfavorable (mRS 5=1, mRS 6=1) in two patients.
Discussion
In this series, AAAs were detected in 27.3 % and were more
frequent in patients harboring infratentorial AVMs.
Aneurysm-related hemorrhage was frequent (56 % of all

Fig. 5 This 44-year-old patient

was admitted with acute SAH (a).
On the angiogram, a frontal AVM
(Spetzler-Martin grade 2) and a
type 1a-aneurysm of the left
MCA were detected (b, c). The
AAA was regarded as the source
of the hemorrhage and treated by
coiling achieving complete oblit-
eration (d). After 6 months, a re-
currence of the aneurysm was
noted (e). Therefore, surgical
clipping was performed, and
since then, the aneurysm has
remained safely occluded (f). The
AVM was later treated by Gamma
Knife radiosurgery, achieving to-
tal occlusion

Fig. 6 Case of a 62-year-old pa-
tient with a left temporal AVM
(Spetzler-Martin grade 2; a, b)
and a type 1a aneurysm of the left
MCA without initial hemorrhage
(c). The AVM was treated surgi-
cally, achieving complete obliter-
ation (d, e). After 64-month fol-
low-up, the 6-mm MCA aneu-
rysm is still unchanged, although
the parent vessel itself seems less
dilated than initially (f)
patients presented with aneurysmal hemorrhage, and 9.6 % of
the survivors suffered from delayed hemorrhage), and
aneurysm-related mortality and morbidity were substantial.
Hemorrhage was most often AAA related, and ruptured
AAAs were larger. Type 1 aneurysms were most commonly
associated with hemorrhage.
In general, AVMs with AAA are rare, although the rates
vary in the literature between 10-58 %[4, 7, 8, 15, 17, 18, 27].
Due to their small number, information on the natural history
of these lesions is limited; therefore, various recommendations
for their treatment exist. In our series, AAAs were detected in
27 %, which may be a hint that AAAs are not so rare as
previously thought, especially when modern diagnostic tools
are used. Some authors suggest focusing on AVM treatment as
they described that AAAs will diminish after successful AVM
obliteration [6, 13, 22–24]. Others, however, consider AAAs
to be significant risk factors for hemorrhage and advocate their
treatment [6, 8, 17–19, 28].
AAAs differ from spontaneous aneurysms without AVMs
in several aspects, which may be related to pathological intra-
cerebral hemodynamics induced by the AVM. First, many of
them are located more distant from the circle of Willis com-
pared to spontaneous aneurysms. In our series, 14.1 % were
classified as distal feeding artery aneurysms, and 63.6 % of the
aneurysms of the ACA were located beyond the A2 segments.
Furthermore, the distribution of AAA varies, as aneurysms of
the posterior circulation were far more frequent in this series
than in series without associated AVMs (40.7 %, compared,
e.g., to 11.9 % in the ISUIA [21]). Other authors, too, have
stressed the importance of hemodynamic phenomena for the
occurrence of AAA [7, 20, 29–32], and the different aneurysm
sites as well as unusual shapes or thin walls have been
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described before [19, 20, 31] (Fig. 2). Aneurysm growth and
de novo aneurysm formation in the current study as well as
other series further highlight this likely pathomechanism [19].
Additionally, the persistence of altered hemodynamics in
patients without complete AVM obliteration might explain the
unusually high rate of AAA recurrence noted after
endovascular coiling of type 1 aneurysms in this series [33].
However, surgical obliteration might not always be feasible in
these patients. Furthermore, neurointerventionalists often de-
scribe difficulties in achieving stable catheter positions for
coiling of these aneurysms because of the wide neck config-
uration and high blood flow within the parent vessels. Ac-
cordingly, most of the AVMs with AAA in our series were
described as high-flow AVMs, as noted before by others [19,
30].
This pathological blood flow in patients with AAA might
also explain why the incidence of hemorrhage was higher in
these patients compared to AVM patients without associated
aneurysms [OR 2.00 (1.08–3.68), p=0.025]. The aneurysm
was the bleeding source in the vast majority of these cases.
This finding differs from other series in which the aneurysm
was attributable to the hemorrhage in 0–46 % [6, 7, 9, 12, 14,
17, 19, 34]. However, this number might be higher in our
series because of better imaging technologies than in many of
the older studies and varying definitions of AAA in the
literature. However, many authors regarded AAA as an im-
portant risk factor for future hemorrhage [6, 10, 13, 18, 20, 29,
35, 36].
As mentioned above, AVMs and aneurysms of the poste-
rior circulation were overrepresented in our series and showed
the highest hemorrhage rate. This might be due to a difference
in the vasculature in the posterior circulation. Similarly as in
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spontaneous aneurysms, the risk of hemorrhage seems to be
increased [21], and in case of posterior fossa hemorrhage, the
outcome is often poor. In this series, all patients who died
because of the initial hemorrhage had posterior fossa lesions.
This corroborates earlier observations [1, 14, 20, 27, 37].
Considering the high rate of aneurysmal hemorrhage and
its devastating outcome in our series (33.5 % poor outcome
including 15.3 % mortality), we think that aneurysm treatment
is warranted. This can be reached with acceptable risks for the
patient (8.5 % treatment-associated morbidity in this series).
Although this opinion has been advocated by other groups
before [12, 17, 29, 30, 37], it is contradictory to suggestions of
some authors [15]. Regression of feeding artery aneurysms
was very rare in this series (1 of 38 untreated aneurysms), and
AAA might lead to hemorrhage even late after complete
obliteration of the AVM. However, one needs to be aware that
there might be an increased risk of aneurysm recurrence after
aneurysm coiling without complete AVM obliteration.
The AVM itself should be targeted for various reasons:
first, there is a significant risk of hemorrhage related to the
AVM. Furthermore, AVMs with AAA might represent a spe-
cial subgroup of AVMs with a high blood flow. This might
lead to (1) an increased risk of rupture of these aneurysms, (2)
the formation of de novo aneurysms, (3) increased recurrence
rates after aneurysm coiling and (4) an increased risk of
hemorrhage of the AVM itself. It seems worthwhile to con-
sider whether the aneurysm itself is a risk factor or only an
epiphenomenon of severely altered hemodynamics induced
by these special AVMs and therefore only the most common
site of rupture.
Limitations of the current study are mainly due to its
retrospective character and include the typical problems asso-
ciated with this design such as selection and referral bias.
Furthermore, the number of patients is limited, and the
follow-up time is relatively short considering the low annual
hemorrhage risk of these lesions [5]. However, although this
series includes only 59 patients, it is one of the largest series
published to date. The detailed follow-up including patients
without or only selective treatment makes it noteworthy.
Conclusions
Aneurysms in the presence of an AVM are associated with a
high risk of hemorrhage. In most cases, hemorrhage is aneu-
rysm related and associated with a high mortality and morbid-
ity. Hence, based on the data of this series, we feel that these
aneurysms should be treated whenever possible. Furthermore,
we now would recommend prophylactic obliteration of
AAAs, especially if the aneurysm is located in the posterior
circulation. However, the AVM needs to be considered for
treatment, too, as incomplete obliteration of the AVM seems
to represent a risk factor for aneurysm recurrence, the
development of new lesions or future AVM hemorrhage. An
AVM-induced change of hemodynamics might be responsible
for these phenomena.
Conflicts of interest None.
Disclosures None.
Funding This research received no specific grant from any funding
agency from the public, commercial or not-for-profit sectors.
Competing Interests Statement None.
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