J Neurosurg 90:78–84, 1999

Early rebleeding from intracranial dural arteriovenous fistulas:
report of 20 cases and review of the literature
HUGUES DUFFAU, M.D., MANUEL LOPES, M.D., VESNA JANOSEVIC, M.D.,
JEAN-PIERRE SICHEZ, M.D., THIERRY FAILLOT, M.D., LAURENT CAPELLE, M.D.,
MOUNIR ISMAÏL, M.D., AHMAD BITAR, M.D., FRANÇOIS ARTHUIS, M.D.,
AND DENIS FOHANNO, M.D.
Department of Neurosurgery, Hôpital de la Salpêtrière, Paris, France
Object. In this study the authors sought to estimate the frequency, seriousness, and delay of rebleeding in a homogeneous series of 20 patients whom they treated between May 1987 and May 1997 for arteriovenous fistulas (AVFs)
that were revealed by intracranial hemorrhage (ICH). The natural history of intracranial dural AVFs remains obscure.
In many studies attempts have been made to evaluate the risk of spontaneous hemorrhage, especially as a function of
the pattern of venous drainage: a higher occurrence of bleeding was reported in AVFs with retrograde cortical venous
drainage, with an overall estimated rate of 1.8% per year in the largest series in the literature. However, very few studies have been designed to establish the risk of rebleeding, an omission that the authors seek to remedy.
Methods. Presenting symptoms in the 20 patients (17 men and three women, mean age 54 years) were acute headache
in 12 patients (60%), acute neurological deficit in eight (40%), loss of consciousness in five (25%), and generalized
seizures in one (5%). Results of the clinical examination were normal in five patients and demonstrated a neurological
deficit in 12 and coma in three. Computerized tomography scanning revealed intracranial bleeding in all cases (15 intraparenchymal hematomas, three subarachnoid hemorrhages, and two subdural hematomas). A diagnosis of AVF was
made with the aid of angiographic studies in 19 patients, whereas it was a perioperative discovery in the remaining
patient. There were 12 Type III and eight Type IV AVFs according to the revised classification of Djindjian and
Merland, which meant that all AVFs in this study had retrograde cortical venous drainage. The mean duration between
the first hemorrhage and treatment was 20 days. Seven patients (35%) presented with acute worsening during this delay
due to radiologically proven early rebleeding. Treatment consisted of surgery alone in 10 patients, combined embolization and surgery in eight, embolization only in one, and stereotactic radiosurgery in one. Three patients died, one worsened, and in 16 (80%) neurological status improved, with 15 of 16 AVFs totally occluded on repeated angiographic
studies (median follow up 10 months).
Conclusions. The authors found that AVFs with retrograde cortical venous drainage present a high risk of early
rebleeding (35% within 2 weeks after the first hemorrhage), with graver consequences than the first hemorrhage. They
therefore advocate complete and early treatment in all cases of AVF with cortical venous drainage revealed by an ICH.

KEY WORDS • dural arteriovenous fistula • hemorrhage • rebleeding

I

NTRACRANIAL dural arteriovenous fistulas (AVFs) con-

stitute approximately 10 to 15% of all intracranial vascular malformations,2,22,31,40,53 including approximately
6% of all supratentorial and 35% of infratentorial arteriovenous malformations (AVMs).1,51
Although the natural history of these predominantly acquired lesions remains obscure,32,37,56 two distinct modes of
presentation related to the pattern of drainage may be distinguished:7,14 1) AVF without retrograde cortical venous
drainage, with a traditionally benign clinical course;1,6,16,19,
28,35,46
and 2) AVF with retrograde cortical venous drainage,
which presents a high risk of aggressive clinical course
with intracranial hemorrhage (ICH).2,13,17,18,29,34,47 Many investigators have tried to estimate the risk of bleeding of
AVFs,2,7–9,14,38,42,47 but to our knowledge there is no series in
78

which they have tried to evaluate the rate of rebleeding of
these AVMs. We report a homogeneous series of 20 patients with AVF revealed by an ICH, with the goal of estimating the frequency, severity, and delay of rebleeding.
Clinical Material and Methods
We retrospectively reviewed the cases of 24 patients
with intracranial dural AVFs who were treated at the PitiéSalpêtrière Hospital between May 1987 and May 1997.
Our aim was to study the risk of rebleeding, so only patients with initial hemorrhagic presentation were selected:
four patients were therefore excluded.
All dural AVFs had been documented using cerebral
angiography, except in one patient, who was nevertheless
J. Neurosurg. / Volume 90 / January, 1999

Early rebleeding from intracranial dural AVFs

FIG. 1. Case 2. Left: Admission CT scan obtained after the patient presented with acute headache, transitory loss of
consciousness, and left-sided hemiplegia, showing a right frontal hematoma with intraventricular rupture. Center:
Angiographic study revealing a frontal AVF fed by both middle meningeal arteries, with ectatic cortical venous drainage
toward the SSS (Type IV). Right: Repeated CT scan obtained 48 hours later, after neurological deterioration and acute
coma, demonstrating rebleeding.

included because of discovery of the AVF during surgery
by two senior neurosurgeons. In all cases angiographic
studies demonstrated the AVF location, arterial supply,
and venous drainage. In addition, these AVFs were graded in five types according to the classification of Djindjian
and Merland15 as modified by Cognard, et al.12 Type I:
free-flow drainage into a sinus; Type II: drainage into a
sinus, with retrograde flow into sinus (IIa) or cortical vein
(IIb); Type III: cortical venous drainage; Type IV: cortical
venous drainage with giant venous ectasia; and Type V:
perimedullary venous drainage. The patient’s age, gender,
presenting symptoms, initial clinical examination, computerized tomography (CT) findings, and clinical and/or
CT course before treatment, methods and timing of treatment, and clinical and angiographic follow up were noted
in all cases.
Illustrative Case
This 60-year-old man (Case 2) was admitted because of
acute headache, transitory loss of consciousness, and leftsided hemiplegia. The patient had presented with an
episode of dysphasia 3 weeks previously. His admission
CT scan revealed a right frontal hematoma with intraventricular rupture. Angiographic studies demonstrated a
right frontal dural AVF with feeding vessels that originated from both middle meningeal arteries. Venous drainage
was routed through a cortical venous ectasia toward the
superior sagittal sinus ([SSS] Type IV). No emergency
treatment was administered because the hematoma was
well tolerated. However, the patient’s neurological status
worsened dramatically 48 hours later, deteriorating into
acute coma. A repeated CT scan revealed rebleeding (Fig.
1) with an increase in the size of the hematoma. Emergency surgery was performed, with evacuation of the hematoma and coagulation of the draining vein as close as
possible to the malformation. The postoperative course
was uneventful, with recovery of consciousness and partial improvement of the left-sided hemiparesis. Complete
J. Neurosurg. / Volume 90 / January, 1999

occlusion of the AVF was confirmed on postoperative angiographic studies.
Results
Clinical, radiological and treatment characteristics of
the 20 patients are summarized in Table 1.
Presenting Symptoms at Admission

Presenting symptoms in the 20 patients (17 men and
three women, mean age 54 years) were acute headaches in
12 (60%); acute neurological deficit in eight (40%), which
included three dysphasias, two motor deficits, two gait
ataxias, and one hemianesthesia; loss of consciousness
(three transient) in five (25%); and generalized seizures in
one (5%). Results of the clinical examination were normal
in five patients, demonstrated a neurological deficit in 12
(11 motor deficits, three aphasias, two hemihypesthesias,
two cerebellar syndromes, and two hemianopsias), and a
coma in three patients.
Computerized tomography scanning demonstrated intracranial bleeding in all cases: 15 intraparenchymal hematomas (13 supratentorial with intraventricular rupture
in two cases, two in the vermis) combined in two patients
with acute subdural bleeding, three subarachnoid hemorrhages (SAHs), and two subdural hematomas.
Diagnosis of AVF was made angiographically in 19 patients within 24 hours after hospitalization, whereas it was
a perioperative discovery in the remaining patient. There
were 12 Type III and eight Type IV AVFs according to
the classification of Djindjian and Merland,15 revised by
Gobin, et al.,21 which meant that all AVFs had retrograde
cortical venous drainage.
Concerning location, angiography revealed eight anterior AVFs (five in the prerolandic region and three in the
central area), all with venous drainage into the SSS; four
AVFs in the middle fossa that drained into the transverse
sinus; and eight posterior AVFs (four parietooccipital that
79

H. Duffau, et al.
TABLE 1
Clinical, radiological, and treatment characteristics of 20 patients with intracranial dural AVF revealed by hemorrhage*
Age
Case (yrs),
No. Sex

Type
of Rebleeding
AVF
(delay)

Treatment

Presenting Symptoms

Outcome

1
2
3
4
5
6
7
8
9
10

61, M
60, M
46, M
67, M
55, M
42, M
68, M
42, M
54, M
54, M

headaches
loss of consciousness
headaches & deficit
headaches & deficit
headaches & deficit
loss of consciousness
headaches
headaches & coma
headaches & deficit
headaches

hematoma of vermis
frontal hematoma
hematoma of vermis
thalamic hematoma
subdural hematoma
frontal hematoma
SAH
parietal hematoma
temporal hematoma
occipital hematoma

IV
IV
III
IV
III
III
III
IV
III
IV

yes (Day 4)
yes (Day 2)
yes (Day 13)
yes (Day 13)
no
no
no
no
no
no

E&S
S
S&E
S
E&S
S
E
S&E
S
E&S

normal
improved
normal
died (Day 22)
improved
worsened
normal
improved
improved
normal

21 mos
25 mos
10 mos
NA
18 mos
6 mos
2 mos
3 mos
12 mos
9 mos

normal
normal
normal
NA
normal
normal
none
normal
normal
normal

11

64, M

headaches & deficit

III

no

E&S

died (Day 15)

NA

NA

III
III

no
no

S
E&S

improved
normal

16 mos
6 mos

normal
normal

III
IV
III
IV

no
no
no
yes (Hr 8)

S
E&S
S
S

improved
improved
improved
improved

7 mos
10 days
2 mos
2 mos

normal
normal
normal
normal

normal

temporal hematoma
& acute sub bleed
frontal hematoma
rolandic hematoma
& SAH
frontal hematoma
parietal hematoma
frontal hematoma
frontal hematoma &
acute sub bleed
tentorial SAH

12
13

44, F
52, M

loss of consciousness
deficit

14
15
16
17

44, M
46, M
46, M
64, M

generalized seizures
deficit
deficit
headaches

aphasia & hemiplegia
hemiparesis, hemihypesthesia
coma & hemiparesis
monoparesis
aphasia & hemiparesis
coma & hemiparesis

18

74, F

headaches

III

no

12 mos

headaches

normal

subdural hematoma

III

NA

AVF not
occl
NA

loss of consciousness

hemianopsia, hemiplegia, hemihypesthesia

parietal hematoma

IV

yes (Days
7 & 8)
yes (Day 1)

radiosur- normal
gery
S
died (Day 10)

19

56, F

20

52, M

S

24 mos

normal

Findings on
Clinical Examination

normal
hemiplegia
cerebellar syndrome
cerebellar syndrome
monoparesis
normal
normal
coma
aphasia
hemianopsia, monoparesis
hemiplegia

CT Findings

Status at Follow Up

improved

Period Angiogram

* E = embolization; NA = not applicable; occl = occluded; S = surgery; sub bleed = subdural bleeding.

drained into the transverse sinus, and four tentorial with
drainage joining the torcular in two cases, the vein of
Galen in one, and the basilar vein in one).
Evolution of the Lesion
Immediate Treatment. The three comatose patients
(Cases 8, 14, and 17) underwent emergency surgery after
the first hemorrhage. One of them (Case 17) had presented before the operation with two consecutive episodes of
headache; his CT scan revealed two possible ruptures,
which were confirmed at surgery. All three of these patients improved postoperatively, with recovery of normal
neurological status in two cases.
Delayed Treatment. For the other 17 patients, the mean
duration between the first hemorrhage and treatment was
20 days (range 8 hours–5 months). During this delay one
patient spontaneously improved (Case 6) and nine remained stable (Cases 5, 7, 9–11, 13, 15, 16, and 18).
Treatment consisted of surgery alone in two patients, combined embolization and surgery in five, embolization
alone in one, and radiosurgery in one. One patient died of
pulmonary embolism, one worsened with residual frontal
syndrome, whereas the other eight had a favorable course
(three with mild residual neurological deficits and five
with complete recovery).
Episodes of Rebleeding. Seven patients (35%) experienced a dramatic worsening of their neurological status.
80

Among these seven, four deteriorated into acute coma
(Cases 1–4) at Days 4, 2, 13, and 13, respectively. Repeated CT scans obtained in all four cases revealed the
occurrence of rebleeding with an increase in the size of the
hematoma, combined in two cases with hydrocephalus
that necessitated implantation of an external ventricular drain. All patients underwent surgical resection of the
AVF, with concurrent embolization in two cases. One
patient died and three improved (two had complete recovery).
One patient (Case 19) had two consecutive radiologically and surgically proven episodes of subdural rebleeding (Days 7 and 8) but because no angiogram had been
obtained, the AVF was discovered only during the third
operation. The patient died 10 days later.
One patient (Case 20) presented in an acute coma 24
hours after the first hemorrhage, and two consecutive
angiograms revealed an increase in the mass effect on the
pericallosal arteries, but no repeated CT scans were obtained. Emergency surgery was performed, with postoperative results including regressive aphasia and hemiparesis.
One patient (Case 12) worsened progressively because
of edema but did not experience rebleeding: she underwent surgery and improved, with persistent mild hemiparesis.
In total, we consider that the objective rate of radiologically proven recurrent hemorrhage is four (20%) of 20,
with a high probability of early rebleeding in three other
J. Neurosurg. / Volume 90 / January, 1999

J. Neurosurg. / Volume 90 / January, 1999

61, M

60, M

46, M

67, M

64, M

56, F

52, M

1

2

3

4

17

19

20

transient coma followed by aphasia

acute headaches,
2nd episode of
acute headaches
8 hrs later
acute headaches &
vomiting 4 hrs
after head injury
w/o coma

repeated acute headaches, gait ataxia

transient dysphasia,
headaches &
coma 3 wks later
acute headaches,
vomiting, dysarthria, dysgraphia

acute headaches

Presenting
Symptoms

rt hemianopsia, hemiplegia, hemihypesthesia

meningeal syndrome

coma (GCS 7), lt
hemiparesis

cerebellar syndrome,
confusion

cerebellar syndrome

stuporous, lt hemiplegia

meningeal syndrome

Findings on
Clinical Examination

lt parietooccipital
hematoma

lt acute SDH on CT
scan obtained 5
days later

rt frontal hematoma
w/ 2 ruptures on
CT, acute rt SDH

lt thalamic hematoma, tentorial
SAH

rt frontal hematoma
w/ intraventricular
rupture
hematoma of vermis

hematoma of vermis

CT Findings

lt occipital/IV/lt ECA,
ICA, & VA/lt occipital vein & TS

no angio

rt frontal/IV/bilat
MMA/SSS

tentorial/III/rt ECA, rt
MHA (& rt carotidoophthalmic aneurysm)/vein of Galen
& SS
tentorial/IV/lt ECA &
ICA/basilar vein

tentorial/IV/rt APA,
bilat MMA, & OcA/
torcular
rt frontal/IV/bilat
MMA/SSS

Arteriographic Findings
(location/type/feeding
artery/draining vein)

worsened Day 1: coma & rt
hemiplegia, no CT scan
2nd angio: increase of
mass effect, rebleeding

Day 5: evacuation of SDH;
Day 7: worsened CT
scan: new acute SDH, 1st
rebleeding

worsened Day 13: coma &
rt hemiplegia; CT scan:
rebleeding w/ hydrocephalus led to implantation
of EVD
immediate treatment

worsened Day 13: coma
CT scan: rebleeding w/
hydrocephalus led to
implantation of EVD

worsened Day 4: acute
headaches & coma;
CT scan: rebleeding
worsened Day 2: coma
CT scan: rebleeding

Outcome
Pretreatment

emergency surgery (Coag A
& V)

old & new blood in hematoma at emergency surgery: rebleeding (Coag A
& V)
Day 7: 2nd surgery for SDH;
Day 8: 2nd worsening; CT
scan: new SDH, 2nd rebleeding

Day 20: surgery (Coag V)

Day 17: surgical evacuation
of hematoma & 3 embolizations (Day 25, 3rd & 8th
mos)

3 partial embolizations
(Days 8, 21, & 30);
Day 64: surgery (Coag V)
Day 2: emergency surgery
(Coag A & V)

Treatment

persistent lt hemiparesis (2 mos),
no aphasia, normal angio
Day 8: 3rd emergency surgery for
SDH w/ discovery of middle
fossa Type III
AVF; Day 10:
death
regressive hemiparesis & aphasia
(24 mos); angio:
persistence of
AVF postop; normalization at 2
yrs by thrombosis

Day 22: death by lt
temporal hemorrhagic venous
infarction

normal neuro exam,
normal angio (21
mos)
regressive lt hemiparesis, normal
angio (25 mos)
normal neuro exam,
normal angio (10
mos)

Follow Up

* Angio = angiogram; APA = ascending pharyngeal artery; Coag A = coagulation of the artery; Coag V = coagulation of the vein; ECA = external carotid artery; EVD = external ventricular drain; GCS =
Glasgow Coma Scale; ICA = internal carotid artery; MHA = meningohypophyseal artery; MMA = middle meningeal artery; neuro = neurological; OcA = occipital artery; SDH = subdural hematoma; SS =
straight sinus; TS = transverse sinus; VA = vertebral artery.

Age
(yrs),
Sex

Case
No.

TABLE 2
Clinical, radiological, and treatment characteristics of seven patients with early rebleeding*

Early rebleeding from intracranial dural AVFs

81

H. Duffau, et al.
cases; therefore the overall rate of recurrent hemorrhage
was seven (35%) of 20 in our series. The clinical, radiological, and treatment characteristics of these seven patients with early rebleeding are summarized in Table 2.
Overall Outcomes. The overall results showed three
deaths, one impairment, and 16 patients with a favorable
course (80%); seven of these had mild neurological deficits and nine recovered normal neurological status at a
mean follow-up time of 10 months. Sixteen follow-up angiograms were obtained in the patients still alive, and 15
(94%) of 16 of the AVFs were found to be totally occluded.
Discussion
The rate of bleeding of dural AVFs has been studied by
many authors2,7,8,12,14,17,18,26,27,29,34,38,42,47 and is estimated at
approximately 1.8% per year, with a higher risk associated with AVMs with cortical venous drainage2,7,9,12,14,31,38,47,54
and tentorial location.2,12,14,38,47
However, publications in which investigators have tried
to estimate the rate of rebleeding of dural AVFs revealed
by an ICH are very rare. Grisoli, et al.,23 reported one case
of recurrent bleeding observed 12 days after the first hemorrhage from an AVF. Halbach, et al.,24 described eight
patients (29%) in a series of 28 with AVF presenting with
hemorrhage, and the occurrence of repeated hemorrhages
(three of repeated SAH, one of repeated intraventricular
rupture) over the course of several weeks in four (50%) of
eight patients. King and Martin38 speculated that the risk
of early rebleeding is presumably the same as that of pial
AVMs, that is, 1 to 2% within 1 month after initial hemorrhage. They concluded that because this risk is low,
conservative medical management should be initiated if
the patient does not have a large hematoma. On the other
hand, Borden, et al.,7 reported more recently that three of
seven AVFs revealed by an ICH in a series of 14 patients
presented with recurrent bleeding after a delay of a few
days. These authors were surprised that the literature on
the rate of dural AVF rebleeding was so sparse and concluded that AVFs presenting with ICH must be treated
quickly.
We describe an original series of 20 patients with dural AVFs with cortical venous drainage, all revealed by
ICH, in which seven patients suffered rebleeding within 2
weeks after the first hemorrhage (four cases were radiologically proven and three were highly likely, comprising
20 to 35% of early recurrent hemorrhages).
Interestingly, four of these patients had already presented with one or more episodes of acute headache during the
month before the first diagnosed hemorrhage. We postulate that these symptoms were in fact related to previous
episodes of bleeding.
In all cases, as has been reported by Borden, et al.,7 and
Grisoli, et al.,23 recurrent hemorrhage occurred within a
latency period of several hours to several days (Hour 8,
Days 1, 2, 2, 4, 13, and 13). Moreover, clinical consequences were always severe; all patients presented with
disorders of consciousness at the time of rebleeding.
As for the risk factors of rebleeding, we found them
to be similar to the risk factors of a first hemorrhage as
previously mentioned: a predominance of Type IV (five
82

Types IV and two Types III in the seven AVFs that rebled), and a predominance of posterior, notably tentorial,
locations (75% of tentorial AVFs in our series rebled).
Considering the high rate of recurrent hemorrhage in
AVFs with cortical venous drainage, the short delay, and
the grave consequences of the rebleedings, our series provides further support for initiating radical treatment as
soon as possible in all cases of dural AVF revealed by a
first ICH.
Many treatment strategies for AVF have been described
in the literature, including ligature of the feeding arteries,5,11,33,49,59,61 coagulation of the nidus and/or venous
drainage,13,23,38,50,56–58 transarterial25,30,36,48,52 or transvenous
embolization,21,27,55,60 stereotactic radiosurgery,10,38,39,43,44 or
combinations thereof.3,4,20,41,45,54 Although in some cases
palliative treatment for control of symptoms seems
acceptable (in Type I and even Type II AVFs), the primary goal of treatment remains the complete and early obliteration of AVFs with cortical venous drainage, because of
the high risk of bleeding and/or rebleeding. We therefore
advocate occlusion of the neck of the draining vein as
close as possible to the nidus. We obtained the best results
in our series when we opted for surgical treatment.
Conclusions
Intracranial AVFs with leptomeningeal drainage (Types
III and IV) represent a subgroup of AVFs with a high rate
of hemorrhage, estimated at approximately 1.8% per year
in the literature.
Moreover, our series demonstrates the high risk of rebleeding associated with AVFs that have cortical venous
drainage (up to 35%) and documents two major points:
the possible imminence of rebleeding and the worsening
of neurological status at the time of the second hemorrhage.
Consequently, we tend to treat all cases of AVF featuring retrograde leptomeningeal venous drainage as early as
possible, particularly when the lesion is revealed by a
hemorrhage, even if the first intracranial bleeding is neurologically well tolerated. In these circumstances we advocate surgical treatment with coagulation of the neck of
the draining vein as close as possible to the nidus malformation, rather than transvenous embolization or stereotactic radiosurgery.
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Manuscript received December 2, 1997.
Accepted in final form August 18, 1998.
Address reprint requests to: Hugues Duffau, M.D., Service de
Neurochirurgie 1, Hôpital de la Salpêtrière, 47 Boulevard de
l’Hôpital, 75651 Paris, Cedex 13, France.

J. Neurosurg. / Volume 90 / January, 1999