Acta Neurochir (Wien) (2004) 146: 1–7

DOI 10.1007/s00701-003-0164-5

Clinical Article
Incidence of residual intracranial AVMs after surgical resection
and efficacy of immediate surgical re-exploration

B. L. Hoh1;2 , B. S. Carter1, and C. S. Ogilvy1

1
Cerebrovascular Surgery, Neurosurgical Service, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts
2
Endovascular Neurosurgery and Interventional Neuroradiology, Massachusetts General Hospital, Harvard
Medical School, Boston, Massachusetts

Published online December 9, 2003

# Springer-Verlag 2003

Summary (AVMs) is not well documented in the literature. Partial

Background. The true incidence of residual lesions after surgical
resection of AVMs is not well documented in the literature. Partial
surgical resection is thought to not confer any improvement over the
natural history risk of hemorrhage of AVMs, and in certain cases may
actually increase the risk of hemorrhage. Over the past 11 years, we have
adopted a policy of immediate postoperative angiography with immedi-
ate surgical re-exploration if a residual lesion is seen. The purpose of the
present study was to review our experience to determine the incidence of
residual lesions and subsequent outcome.
Methods. From June 1991 to June 2002, 324 patients underwent
craniotomy and surgical AVM resection. As per protocol, all patients
underwent immediate postoperative angiography. We have a protocol for
immediate surgical re-exploration if a residual lesion is seen on post-
operative angiographic exam.
Findings. There were total six patients (1.8% of patients operated with
intracranial AVMs) with residual lesions on postoperative angiography.
All six patients underwent immediate surgical re-exploration with com-
plete 100% obliteration; two patients required two re-exploration proce-
dures. There was one operative complication: posterior cerebral artery
and superior cerebellar artery infarcts after re-exploration of residual
lesion after surgical resection of a large occipito-temperal-parietal AVM.
There were no other morbidities and no mortalities.
Conclusions. The incidence of residual lesions seen on postoperative
angiography after AVM surgery at an experienced center is 1.8%.
Because of the potential imminent danger of hemorrhage from a residual
lesion, we recommend a policy of immediate postoperative angiography
(or intraoperative angiography if image quality is satisfactory) for all
AVM surgery and early surgical re-exploration if a residual lesion is seen.
Keywords: Angiography; AVM; embolization; hemorrhage; reopera-
tion; surgery.
Introduction
The true incidence of residual lesions after surgical
resection of intracranial arteriovenous malformations
surgical resection does not confer any improvement over
the natural history risk of hemorrhage of AVMs, and in
certain cases may actually increase the risk of hemo-
rrhage [3, 14]. Residual AVMs or residual early draining
veins can remain after surgical resection, unrecognized
at the time of operation, only to be seen on postopera-
tive angiography. Immediate postoperative angiography
(or intraoperative angiography if available with
high-standard image quality) is thus critical to assess
for residual AVM and can facilitate prompt surgical
attention.
Over the past 11 years, we have obtained immediate
postoperative angiography for all AVMs with a protocol
for immediate surgical re-exploration if any residual
lesion or remaining early draining vein is found. We
reviewed our surgical experience to determine the true
incidence of residual intracranial AVMs after operative
resection. We also evaluated the efficacy and outcome
using a protocol for immediate surgical re-exploration
for residual lesions.
Methods
From June 1991 to June 2002, 324 patients underwent craniotomy and
surgical resection of intracranial AVMs at the Massachusetts General
Hospital. Our combined neurovascular unit of neurosurgeons, interven-
tional neuroradiologists, radiation oncologists, and neurologists jointly
decided upon surgical resection with or without preoperative adjunctive
embolization as the optimal treatment strategy in these patients.
Surgical technique was performed according to modern principles of
microsurgical AVM resection under general anesthesia [7]. When our
2 B. L. Hoh et al.
combined neurovascular unit decided that adjunctive embolization was
indicated, this was performed preoperatively in either one or multiple
stages at an earlier date than the date of surgery. Endovascular emboli-
zation was performed intra-arterially via a transfemoral route and con-
sisted of super-selective injection of n-butylcyanoacrylate in intended
vessels with the patient under general anesthesia [4].
In every patient, postoperative angiography was performed immedi-
ately after AVM surgery. Our protocol has been for direct return to the
operating room for immediate surgical re-exploration under strict blood
pressure control if residual AVM or early draining vein is identified on
postoperative angiography. After re-exploration, another immediate
angiogram is performed.
The radiographic studies, medical records, operative notes, and office
charts were retrospectively reviewed as well as clinical data from a
prospectively collected clinical AVM computer database. Spetzler–
Martin grade was assigned to each AVM on the basis of size, venous
drainage, and eloquence of location as previously described [16]. Clin-
ical outcome was determined independently by a neurovascular nurse
practioner who enters Glasgow Outcome Score [8] prospectively into the
AVM computer database.
Results
There were total six patients (1.8% of patients operated
with intracranial AVMs) with residual lesions seen on
postoperative angiography following surgical resection
of their intracranial AVMs. Table 1 summarizes the clin-
ical, demographic, anatomic, and radiographic details of
the six patients. All residual lesions were small (<1 cm).
Initial presentation was: hemorrhage 4, and seizures 2.
Initial management of hematomas was conservative in
one patient (Patient 6 in Table 1), external ventricular
drainage with eventual ventriculoperitoneal shunt place-
ment in two patients (Patients 2 and 3), and endovascular
coiling of feeding pedicle aneurysm and external ventri-
cular drainage without eventual ventriculoperitoneal
shunting in one patient (Patient 5). No patient of the
six noted required surgical evacuation of hematoma.
Preoperative embolization was performed in four
patients. Four AVMs were supratentorial, two were
infratentorial. AVM sizes were one small (<3 cm), three
medium (3–6 cm), and two large (>6 cm). Deep venous
drainage was present in four AVMs. Three AVMs were
in eloquent locations. Spetzler–Martin grades were II: 2,
III: 2, and V: 2.
All six patients were surgically re-explored immedi-
ately. All six patients had complete obliteration on fol-
lowup angiography (100%); two patients required two
re-exploration procedures (Patients 4 and 6). Patient 4
had a tiny early draining vein which persisted on angio-
gram after immediate re-exploration and underwent a
second re-exploration, this time with placement of a
Cosman-Roberts-Wells stereotactic head frame during
angiography, for stereotactic localization of the lesion
for the second re-exploration procedure. He had com-
plete obliteration of the lesion after this procedure.
Patient 6 had a small residual lesion deep to the resec-
tion cavity seen on immediate postoperative angio-
graphy with persistent residual after immediate
re-exploration. A second re-exploration was performed
two weeks later for complete obliteration of the AVM.
Four patients were neurologically intact preopera-
tively and remained neurologically intact postopera-
tively (Patients 1, 2, 4, 5, in Table 1). One patient was
dependent with a left hemiparesis preoperatively from a
severe intracerebral hemorrhage from her right motor
strip AVM, and did not have a change in her neurologic
condition postoperatively (Patient 6). One patient with a
large right occipito-temporal-parietal AVM required re-
operation for a residual lesion. The patient incurred right
posterior cerebral artery (PCA) and superior cerebellar
artery (SCA) infarcts with accompanying swelling
requiring posterior fossa decompression (Patient 3). He
had a left visual field deficit preoperatively, but was
dependent and with a left hemiparesis after his infarcts.
This was the one operative complication among the six
patients.
Overall clinical outcome was excellent (GOS 5) in
four patients, fair (GOS 3) in two patients. There were
no poor outcomes or deaths.
Illustrative cases
Case 1 (Patient 1). A 31 year-old woman presented
with her first generalized tonic-clonic seizure. She was
neurologically intact and placed on carbamazepine. She
was found to have a 3 cm right posterior temporal AVM
fed predominantly by three large right middle cerebral
artery (MCA) opercular temporal branches with drainage
to the vein of Trolard and the vein of Labbe (Fig. 1).
Single-stage endovascular embolization with n-butylcya-
noacrylate was performed in three pedicles with 70%
reduction in flow to the AVM. Two days later, she under-
went right temporal craniotomy and surgical resection.
Immediate postoperative angiography revealed a small
remnant of AVM fed by the right anterior choroidal
artery and a branch off of the angular artery. Immediate
surgical re-exploration was performed for complete
obliteration of the AVM. She was neurologically intact
and was discharged home on postoperative day three.
Discussion
The actual incidence of incomplete surgical resec-
tion of AVMs is not well-documented in the literature.
Table 1. Patients with residual lesions after surgical resection of intracranial AVMs

Pt. Age Sex Presentation AVM AVM Eloquent Deep Spetzler- Preoperative Postoperative Re-exploration Re-resection Operative Neurologic
(yrs) location size location venous Martin embolization angiographic procedures efficacy complication exam
(cm) drainage grade finding preoperatively

Pt 1 31 F seizure right 3 no no 2 yes persistent small 1 complete obliteration – intact

posterior AVM deep fed
temporal by branch of
anterior
choroidal
Pt 2 47 F hemorrhage right 1.5 no yes 2 no persistent small 1 complete obliteration – intact
cerebellar AVM fed by
small vermian
branch of PICA
Pt 3 31 M multiple right >6 yes yes 5 yes persistent small 1 complete obliteration right PCA and left visual field
hemorrhages occipito- AVM deep fed superior deficit
temporal- by falcine cerebellar
parietal meningeal infarcts
branch
Pt 4 26 M transient left 3 no yes 3 yes persistent early 2 (second complete obliteration – intact
visual occipital draining vein procedure
deficits on lateral wall performed with
of resection stereotactic
cavity angiography for
localization)
Pt 5 40 F hemorrhage right 3 no yes 2 yes persistent 1 complete obliteration – intact
cerebellar AVM
Pt 6 22 F hemorrhage, right 7 yes yes 5 no persistent small 2 (second complete obliteration – dependent, left
coma motor deep AVM fed procedure hemiparesis
strip by one branch performed two
of pericallosal weeks later)
artery and small
lenticulostriate
branches
Incidence of residual intracranial AVMs after surgical resection and efficacy of immediate surgical re-exploration
3
4 B. L. Hoh et al.

We believe it is important to determine the true rate of patients and 2) to justify the routine utilization
residual lesions occurring after operative resection of of immediate postoperative angiography for AVM
AVMs: 1) to facilitate preoperative discussions with surgery.

Fig. 1. Patient 1. 31 year old woman who presented with her first generalized tonic-clonic seizure. (a) T2-weighted axial MRI demonstrates
serpiginous flow voids in the right posterior temporal lobe suggestive of AVM. (b) Anteroposterior, and (c) lateral right internal carotid artery
injection digital subtraction angiograms demonstrate a 3 cm right posterior temporal AVM fed predominantly by three large right middle cerebral
artery (MCA) opercular temporal branches with drainage to the vein of Trolard and the vein of Labbe. Single-stage n-butylcyanoacrylate (n-BCA)
embolization was performed followed by, two days later, right temporal craniotomy and surgical resection. Immediate postoperative angiography
was performed. (d) Anteroposterior, and (e) lateral immediate postoperative right internal carotid artery digital subtraction angiograms demonstrate
a small remnant of AVM fed by the right anterior choroidal artery and a branch off of the angular artery. Immediate surgical re-exploration and
resection of the AVM residual was performed, followed by immediate post-re-exploration angiography. (f) Anteroposterior, and (g) lateral post-re-
exploration right internal carotid artery digital subtraction angiograms demonstrate complete obliteration of the AVM
Incidence of residual intracranial AVMs after surgical resection and efficacy of immediate surgical re-exploration 5

Fig. 1 (continued)

Partial resection of an intracranial AVM does not con-
fer any protection from hemorrhage over the natural
history of an untreated AVM [3, 14]. This is also sub-
stantiated by the radiosurgical literature [2, 12, 13]. In
certain cases, we believe that the risk of hemorrhage of a
partially resected AVM is even higher, particularly if
there is new increased venous hypertension, for example
if there is newly created venous outflow obstruction
from the partial resection or if a single draining vein is
left where there originally was multiple venous outlets.
Residual AVM or a remaining early draining vein may
be unrecognized at the time of surgery and only be
detected by angiography. An early draining vein, a small
remnant of AVM, or remaining component of AV shunt-
ing, can be subtle and difficult to identify. Furthermore,
deep portions of AVM or portions located in eloquent
areas of brain may remain because of the surgeon’s hes-
itation to proceed further with high-risk exploration.
This is why we believe postoperative angiography is
important.
6 B. L. Hoh et al.
We perform postoperative angiography immediately
after surgery. We believe this is important because of
the potential imminent danger of hemorrhage. Heros
has described a patient who incurred a catastrophic
hemorhage immediately after AVM surgery from a resi-
dual lesion during transport from the operating room to
the intensive care unit [6]. Likewise, Solomon et al.
described a patient who had a major hemorrhage within
48 hours after AVM surgery [15]. For the same reason,
we have adopted a protocol of immediate surgical re-
exploration if a residual lesion is found.
Some groups have adopted the use of intraoperative
angiography for AVM surgery [1, 5, 9–11, 17]. While there
are some advantages to intraoperative angiography which
are quite appealing, such as the ability to immediately re-
explore while the craniotomy and dura are exposed, we
have not found the image quality produced by our intra-
operative fluoroscopic unit (portable C-arm) to be good
enough to adequately assess for residual lesions after
AVM resection. Artifact from surgical instruments and
retractors can also obscure the image. Furthermore, multi-
ple angled projections are often necessary for optimal
views of the AVM, and our intraoperative fluoroscopic unit
is limited in its range of motion about the operative bed.
When a residual lesion is seen on postoperative angio-
graphy, our protocol has been to return to the operating
room directly for immediate surgical re-exploration. This
has been our practice because of the potential for immi-
nent hemorrhage. Additionally, immediate re-exploration
is not hindered by scar formation and adhesions that com-
plicate delayed re-operations. Two of the six patients re-
quired two re-exploration procedures. In one of the second
re-exploration procedures, we employed the Cosman-
Roberts-Wells stereotactic head frame during angiogra-
phy for stereotactic localization of the residual lesion.
Solomon et al. have described their management of
residual dysplastic arterial vessels that can be seen on
immediate postoperative angiography after AVM sur-
gery [15]. We have witnessed this too on our postopera-
tive angiographic exams, and agree with their group that
if the dysplastic vessels are arterial, there is no arterio-
venous communication, and their is no early draining
vein, that these do not represent residual AVM and can
be managed conservatively.
In the six patients with residual lesions, we found
them to be small and subtle lesions, most often deep,
and difficult to identify at initial surgery. With the aid of
the postoperative angiographic exam, we were able to
localize the residual lesions on the re-exploration proce-
dure for complete obliteration.
Conclusions
Using a protocol of immediate postoperative angio-
graphy after AVM surgery, we witnessed 1.8% residual
lesions (six patients) out of 324 consecutive patients
who underwent surgical AVM resection. Immediate sur-
gical re-exploration was performed in all six patients
with complete 100% obliteration. There was one opera-
tive complication, however, due to the potential immi-
nent danger of hemorrhage from a residual AVM, we
recommend a policy of immediate postoperative angio-
graphy (or intraoperative angiography if the image-
quality is satisfactory), with immediate surgical
re-exploration and resection if residual lesion is seen.
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Surgical management of neurovascular disease. Baltimore,
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Dion J, Becker D (1990) Intraoperative digital subtraction angio-
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(1998) The value of intraoperative angiography for surgical treat-
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(1994) Patient outcomes after stereotactic radiosurgery for ‘‘oper-
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T, Toya S (1992) Natural history for residual intracranial AVM:
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Comments
The authors address an indeed intricate clinical issue. It is certainly
beyond doubt that in any case of A VM resection a postoperative angio-
graphy is mandatory. A matter of controversy, however, remains the
question when to perform it: intraoperatively, immediately postopera-
tively, or some days after the operation? Advocates of an intraoperative
angiography, on the one hand, assert that an intraoperative angiogram is the
most effective and most convenient method to identify remnants of an A
VM and to continue resection before the craniotomy is closed. Proponents
of an immediately postoperative angiogram, on the other hand, allege that
conventional angiography is superior due to optimal views with high
quality images thus avoiding pitfalls in terms of mistaking benign vascular
changes for true residual AVM. In case of true residuals the patient is
brought back to the operating room for immediate re-exploration and
resection. The rationale of both perceptions is to entirely remove the
AVM before possible postoperative haemorrhage might occur. However,
even though a few cases of ultra-early haemorrhage after partial resection
of an AVM were attributed to remaining components of AV shunting it is
our considered opinion that the most common cause of postoperative
haemorrhage is hyperaemia due to disturbed vasoreactivity as described
by Spetzler. We are not convinced that the danger of haemorrhage from a
residual AVM is such imminent that it warrants immediate diagnostics and
surgical action and is, furthermore, not substantiated in that way the
authors claim that it were. Hence it is our policy to obtain a postoperative
angiogram one week after the operation and to perform delayed surgical
re-exploration and resection if residual lesions are detectable. In our point
of view this strategy is more advantageous for various reasons. First of all it
is practical knowledge that directly after surgical AVM resection the brain
is swollen. To perform an immediate re-operation in this acute stage which
is unavoidable associated with considerable brain retraction means
undoubtedly an increased risk for the patient. Additionally brain oedema
and vessel spasm may entail the risk of false-negative findings on an
immediate postoperative arteriogram signifying that remnants of an
AVM may appear on an angiogram obtained later. And finally, the risk
of a ‘‘break-through’’ bleeding as the major cause of postoperative hae-
morrhage will be in no way reduced by performing an angiography imme-
diately after surgery.
Since the issue when to perform the postoperative angiogram is still
controversial and is solely based on institutional judgement the authors
are acknowledged to stimulate this discussion.
G. Marquardt and V. Seifert
7
The authors describe 6 patients with residual A V Malformations out
of 324 who underwent craniotomy for surgical excision of an A VM
(1.8%). These patients were subjected to immediate post-operative
angiography and taken back to theatre with only 1 increased morbidity.
Their contention, therefore, is that the early post-operative angiogram
should be recommended. They correctly point out that intra-operative
angiography (if the quality of the image is satisfactory) would represent
an aft-emative whereby residual A VM could be excised before dural
closure. This bas  successful in my own experience and can be further
refined with image guided equipment which has become available in
more recent times.
Despite these best attempts to totally excise A V Malformations, there
is still some value in delayed post-operative angiography in addition to
either immediate post-operative or intra-operative angiography because
a small percentage of patients will open up vascular channels which had
become obliterated intra-operatively.
D. Mendelow
The distinguished neurovascular group of the Neurosurgical and
Endovascular Services Massachusetts General Hospital presents a very
interesting series of patients suffering from symptomatic A VM and
reports the results of their treatment protocol concerning management
of residual A VMs. Out of 324 patients who had craniotomy and surgical
resection of the A VM in the past 11 years, 6 had a residual lesion on the
immediate postoperative angiography. According to the protocol all six
patients had a successful re-exploration and a complete resection of the
AVM. Two patients had 2 re-explorations. In 1 case the protocol was not
strictly followed, as the second re-exploration was performed 2 weeks
after the initial operations. Two patients presented with seizures and 4
patients with a haemorrhage. The incidence of residual A VMs was
1.8%; and the outcome was excellent: 4 patients had GOS 5 and 2
patients suffering from a Spetzler–Martin Grade 5 A VM that had bled
had a final GOS 3 outcome.
The readers should be aware of the changing algorithms in A VM
treatment especially in Spetzler–Martin Grade IV and V cases.
Endovascular neurosurgeons=interventional neuroradiologists tend to
offer and also accept partial embolisation=occlusion of these A VMs,
though no evidence have indicated that partial treatment of an A VM
reduced a patient’s risk of haemorrhage. In fact, partial treatment may
even worsen the natural history of an A VM!
According to a recent intention-to-treat analysis by Han PP et al. of
Spetzler–Martin grades IV and V A VMs it was shown that the haemor-
rhage risk of 1.5% per year, which was associated with Grades IV and V
A VMs appeared to be lower than that reported for Grades IV and V A
VMs. Complete treatment was only warranted for patients with progres-
sive neurological deficits caused by haemorrhage of the A VM. These
authors did not support palliative treatment of A VMs, except in the
specific circumstances of arterial or intranidal aneurysms or progressive
neurological deficits related to vascular steal.
Reference
1. Han PP, Ponce FA, Spetzler RF (2003) Intention-to-treat analysis of
Spetzler-Martin grades IV and V arteriovenous malformations:
natural history and treatment paradigm. J Neurosurg 98: 3–7
T. P. Doczi
Correspondence: Christopher S. Ogilvy, M.D., Cerebrovascular Sur-
gery, Brain Aneurysm=AVM Center, VBK-710, Massachusetts General
Hospital, 55 Fruit Street, Boston, Massachusetts 02114. e-mail:
cogilvy@partners.org