Case Report

Spontaneous Resolution of Cerebral Pial Arteriovenous Fistula After Angiography: Report
of Two Cases
Takeshi Satow1, Megumu Suzuki1, Taro Komuro1, Masafumi Ogawa2, Akira Kobayashi1, Sei Nishida3

Key words

- BACKGROUND: Cerebral pial arteriovenous fistula (AVF) is a rare disorder,

- Cerebral angiogram

and its natural course is uncertain. The present article reports 2 rare cases of
pial AVF that underwent spontaneous cure after diagnostic cerebral angiogram.

- Cerebral blood flow
- Headache
- Pial arteriovenous fistula
- Spontaneous resolution

- CASE DESCRIPTIONS: A 73-year-old man presented with generalized seizure

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and reported severe but intermittent headache in the right temporo-occipital
area. Single-photon emission computed tomography (SPECT) showed hyperperfusion in that area. The main finding of a cerebral angiogram was an arteriovenous shunt at the cortical surface of the right temporal area. Soon after this
diagnostic angiogram, the symptoms vanished. A further cerebral angiogram
showed the disappearance of this pial AVF, and a SPECT study showed resolution of the hyperperfusion of the affected area.
A 69-year-old man, with a history of intracerebral hemorrhage on the left parietal
area 3 years earlier, presented with speech disturbance and headache on his left
side. SPECT showed hyperperfusion in the left temporoparietal area. A cerebral
angiogram showed an arteriovenous shunt at the surface of the left parietal area.
During the same cerebral angiogram session, the pial AVF disappeared after the
third injection of a contrast medium with magnification. Two days after the
cerebral angiogram, the patient’s headache disappeared and speech disturbance gradually improved. SPECT also showed disappearance of the
hyperperfusion.

1878-8750/$ - see front matter ª 2017 Elsevier Inc. All
rights reserved.

- CONCLUSIONS: It

Abbreviations and Acronyms
AVF: Arteriovenous fistula
CT: Computed tomography
MRI: Magnetic resonance imaging
SPECT: Single-photon emission computed
tomography
From the Departments of 1Neurosurgery and 2Neurology,
Nagahama City Hospital, Nagahama; and 3Department of
Neurosurgery, Kyoto University Graduate School of
Medicine, Kyoto, Japan
To whom correspondence should be addressed:
Takeshi Satow, M.D., Ph.D.
[E-mail: satowtake@gmail.com]
Citation: World Neurosurg. (2017).
http://dx.doi.org/10.1016/j.wneu.2017.04.155
Journal homepage: www.WORLDNEUROSURGERY.org

INTRODUCTION
Pial arteriovenous fistula (AVF) is an
extremely rare intracranial vascular lesion,
consisting of 1 or more supply arteries in
direct connection to the venous drainage
without any intervening nidus. Because of
its rarity, its natural history and appropriate treatment are yet to be established.
Most investigators have proposed the
efficacy of disconnection of AVF via direct
surgery or endovascular surgery, but not
observation.1,2
Many cases of spontaneous closure of
dural AVF3-8 or carotid cavernous sinus fistula9-12 have been reported in the literature,
whereas spontaneous resolution of pial AVF
is extremely rare; only a single case has been
reported.13 We present here 2 further cases
of pial AVF that resolved spontaneously
soon after cerebral angiogram, in
association with normalization of cerebral
blood flow. We emphasize the importance
of considering pial AVF as a possible cause

is possible that pial AVF is a cause of headache and
neurologic symptoms in association with focal hyperperfusion. Diagnostic cerebral angiography should be performed to make a definite diagnosis; after this,
pial AVF sometimes disappears.

in patients manifesting localized headache
and neurologic deficits or seizure disorders.

CASE DESCRIPTIONS
Patient 1
A 73-year-old man with a history of atrial
fibrillation, hypertension, and migraine
was taken to our hospital by ambulance
because of a sudden disturbance of consciousness followed by generalized tonicclonic seizure. Diazepam readily put an
end to the seizure, and he was admitted
for further evaluation. He also had a history of head injury without neurosurgical
intervention at age around 20 years. For
the last 3 years, he had had several episodes of migraine, with visual aura.

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Lomerizine was prescribed and gave partial relief of this symptom.
On the next day after admission, the
patient was alert and oriented. He did not
show any deficit in cranial nerves or
sensorimotor function of extremities. He
showed hemispatial neglect on the left side
and reported severe but intermittent headache in the right temporoparieto-occipital
area. Acetaminophen was partially effective for relieving this headache, but rizatriptan was not. Antiepileptic drugs
(levetiracetam and topiramate) controlled
his epileptic seizure; he did not experience
any seizure after hospitalization.
Blood examination was unexceptional.
Viral encephalitis and metabolic encephalopathy were considered as possible causes,
but the results of a cerebrospinal fluid study

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CASE REPORT
TAKESHI SATOW ET AL.

were not abnormal, including cell count,
protein, glucose, and lactic and pyruvic
acids. Brain computed tomography (CT)
did not show any hemorrhagic abnormality.
Magnetic resonance imaging (MRI) of the
brain showed a slight hyperintensity area in
the right temporal area on diffusionweighted imaging, distinct from old
ischemic changes (Figure 1A and B).
Electroencephalography showed focal
slowing in the frontotemporal area on the

SPONTANEOUS CLOSURE OF PIAL AVF

right side. 99mTc-single-photon emission
CT (SPECT) showed hyperperfusion in the
right temporoparietal area (Figure 1C).
Antiepileptic drugs were gradually
increased and other migraine relief was
added, but the patient’s migrainous
headache did not improve. About 2 weeks
after admission, MRI of the brain showed
an apparent relative high intensity of
the cortical ribbon in the right
temporoparietal area (Figure 1D and E).

Figure 1. Patient 1. (A) Fluid-attenuated inversion recovery and
(B) diffusion-weighted imaging (DWI) magnetic resonance
imaging on admission showed only slight hyperintensity in the
right temporal lobe (white arrow) according to DWI.
Single-photon emission computed tomography (SPECT) 2 days
after admission (C) showed hyperperfusion in the corresponding
area (white arrowhead). Repeated magnetic resonance imaging

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SPECT at this time showed persistent
hyperperfusion in the corresponding areas
(Figure 1F). A cerebral angiogram was
then performed with the use of
Oypalomin 300 (FujiPharma Co., Ltd.,
Toyama, Japan). On a right internal
carotid angiogram, the vein of Labbé was
opacified through the branches of the
middle cerebral artery in the later arterial
phase (Figure 2A and B). As a result, a pial
AVF was diagnosed. Other pathologic

taken 18 days after admission clearly showed hyperintensity not
only with DWI (E) (double white arrows) but also with
fluid-attenuated inversion recovery (D) (thick white arrow),
whereas SPECT (F) showed persistent hyperperfusion (double
white arrowhead). SPECT (G) taken when the headache had
disappeared showed that hyperperfusion had ceased.

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CASE REPORT
TAKESHI SATOW ET AL.

SPONTANEOUS CLOSURE OF PIAL AVF

arterial phase (Figure 4A and B). Injection
into the left carotid artery of a contrast
medium was repeated twice more, to
elucidate
the
shunt
point
on
magnification. Surprisingly, at the third
injection before a left carotid angiogram,
the arteriovenous shunt disappeared
(Figure 4C and D). No other pathologic
conditions were found.
Two days after the cerebral angiogram,
the patient’s headache disappeared and his
speech disturbance gradually improved.
MRI (Figure 3D and E) did not show any
obvious change, but SPECT (Figure 3F)
conducted 11 days after the cerebral
angiogram showed that the hyperperfusion
had disappeared. Repeated cerebral
angiography also confirmed that the pial
AVF had been cured.
The patient did not experience any
episode of hypotension during hospitalization. During the follow-up period of
6 months, the patient did not experience
any recurrent symptoms.
DISCUSSION

Figure 2. Right internal carotid angiogram of patient 1. Arterial (A) and late arterial phase (B) of initial
angiogram. Vein of Labbé (arrow) was opacified through the cortical branch of the middle cerebral
artery. Repeated angiogram showed that the early filling of vein of Labbé disappeared in the arterial
(C) and late arterial phase (D).

findings, such as dural sinus thrombosis,
atherosclerotic steno-occlusive disease,
and so on, were not observed.
Immediately after the angiogram, the
patient’s headache subsided, without prescription of analgesics. SPECT was repeated
at 17 days after the cerebral angiogram and
showed the normalization of cerebral blood
flow (Figure 1G). A cerebral angiogram
performed 21 days after the first angiogram
confirmed complete disappearance of all
arteriovenous shunt (Figure 2C and D). The
hemispatial neglect also recovered, and the
patient was discharged home without any
neurologic deficits.
During hospitalization, the patient did
not experience any episode of hypotension.
During the follow-up period, lasting
21 months, his headache and other
symptoms did not recur and he was able
to resume social activities as before.
However, MRI showed an atrophic change
of the right temporo-occipital area.

Patient 2
A 69-year-old man, who had a history of
hypertensive subcortical intracranial hemorrhage in the left parietal area 3 years
earlier, visited our outpatient clinic reporting aphasia, alexia, and a headache in the
left temporoparietal area. CT and MRI
(Figure 3A and B) did not show any recent
hemorrhagic or ischemic strokes, and
electroencephalography did not show any
epileptiform discharges. Antiepileptics
were prescribed on the assumption of
subclinical seizure, but were not effective.
99m
Tc-SPECT showed a region of hyperperfusion in the left parietal area
(Figure 3C). A diagnostic cerebral
angiogram was conducted with the use of
Oypalomin 300 (FujiPharma Co., Ltd.,
Toyama, Japan). On an angiogram of the
left internal carotid artery, the ascending
cortical vein at the parietal area was
opacified through the cortical branch of
the middle cerebral artery in the late

WORLD NEUROSURGERY -: ---, MONTH 2017

We have documented 2 cases of pial
AVF manifesting headache and neurologic
deficits/seizure. Both showed hyperperfusion in the affected area, which
resolved reasonably soon after a diagnostic
cerebral angiogram, in parallel with
improvement in neurologic symptoms.
Intracranial pial AVFs have only recently
been considered as distinct from AVMs.14
They consist of 1 or more arterial
connections to a single venous channel
without any intervening nidus. Isolated
pial AVF comprises rare congenital
lesions, usually presenting during infancy
or early childhood, which may occur
sporadically or be associated with
hereditary disorders such as Rendu-OslerWeber disease,15 or other genetic
vasculopathies. Extremely rarely, acquired
pial AVF in adults has been reported as
an idiopathic form16 or in association
with trauma,17 or as cerebral venous
thrombosis18 or as part of a history of
neurosurgical treatment.19 According to
the recent review by Yang et al.,20 cerebral
pial AVF presents most commonly with a
mass (45.8%), seizure disorder (27.7%),
or hemorrhage (32.5%). After treatment
with surgical or endovascular flow
disconnection, the total obliteration rate
was found to be 90.2%. In the present 2

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CASE REPORT
TAKESHI SATOW ET AL.

SPONTANEOUS CLOSURE OF PIAL AVF

Figure 3. Patient 2. (A) Fluid-attenuated inversion recovery and (B) diffusion-weighted imaging (DWI)
magnetic resonance imaging on admission show only slight hyperintensity of the cortical ribbon
around a trace of previous intracerebral hemorrhage on DWI (white arrow) in association with
hyperperfusion on single-photon emission computed tomography (C) (white arrowhead). When the
patient’s symptoms subsided after diagnostic cerebral angiography, magnetic resonance imaging
(D, fluid-attenuated inversion recovery; E, DWI) did not show any apparent change, but
single-photon emission computed tomography (F) showed recovery of hyperperfusion in the left
parietal area.

cases, patient 1 had a history of head
trauma about 50 years previously
(no detailed description could be given),
and patient 2 had a history of
intracerebral hemorrhage. Neither had a
history of neurosurgical intervention. The
causal relationship between their medical
history and the emergence of pial AVF
remains uncertain.

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Several cases of spontaneous closure of
cavernous sinus fistula after angiography
have been reported.9-12 Postulated mechanisms include systemic hypotension,9 local
pressure gradient induced by cerebral
angiography,12 and irritability induced by
the contrast medium.10,11 Spontaneous
cure of dural AVF has also been
reported.3-8 Plausible mechanisms for this

situation include recanalization of the
occluded dural sinus,8 thrombosis caused
by
intravascular
turbulence,4
and
compression of the unique feeding artery
by hematoma or edema.3 The 2 patients in
the present report did not have systemic
hypotension during hospitalization, acute
hemorrhage, edema, or occlusion of dural
sinuses before the spontaneous cure of
their pial AVF. We therefore believe that
diagnostic cerebral angiography per se
could be a factor in the spontaneous cure
of pial AVF, at least, in our 2 patients.
Radiologic contrast media are known to
have endothelial toxicity, causing inflammation, thrombosis, altered vasomotor balance with predominant vasoconstrictive
response, and other effects,21 particularly in
the presence of underlying vascular
disease.22 Among various factors of
contrast agent, it is well known that
hyperosmolality of the contrast media
(Oypalomin 300 used in the present study
is about twice the serum osmolality) can
cause injury or dysfunction of vascular
endothelial cells23; one of the mechanisms is
advocated to be apoptosis.24 Furthermore,
although contrast media injection is
known to cause both vasodilation and
vasoconstriction,
vasoconstriction
is
reported to predominate in patients with
atherosclerosis.25 Because the patients’
symptoms improved soon after the cerebral
angiogram, it is reasonable that diagnostic
cerebral angiography or contrast media used
plays some role in closure of pial AVF in
these patients.
Santosh et al.13 reported the only case of
pial AVF to disappear spontaneously 10
days after cerebral angiogram. Three
days before confirmation that pial AVF
had been cured (i.e., 7 days after the
initial cerebral angiogram), the patient
experienced sudden onset of localized
headache and cessation of tinnitus. The
investigators
suggested
that
the
angiogram hastened the natural process
of spontaneous thrombosis within the
fistula.
Reul et al.5 included, in their case
series of anterior cranial fossa dural
AVF, the situation of spontaneous cure
during cerebral angiogram, as in our
patient 2. These investigators did not
discuss any mechanism related to
cerebral angiography. Based on the
finding that pial AVF disappeared
relatively soon after cerebral angiography

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CASE REPORT
TAKESHI SATOW ET AL.

SPONTANEOUS CLOSURE OF PIAL AVF

normalization of impaired cerebral blood
flow. This situation might be caused by a
reaction to the contrast medium during
cerebral angiography.
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Although no neurologic sequelae have
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SPONTANEOUS CLOSURE OF PIAL AVF

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23. Zhang H, Holt CM, Malik N, Shepherd L,
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Conflict of interest statement: The authors declare that the
article content was composed in the absence of any
commercial or financial relationships that could be construed
as a potential conflict of interest.
Received 22 February 2017; accepted 24 April 2017
Citation: World Neurosurg. (2017).
http://dx.doi.org/10.1016/j.wneu.2017.04.155
Journal homepage: www.WORLDNEUROSURGERY.org

25. Limbruno U, Petronio AS, Amoroso G, Baglini R,
Paterni G, Merelli A, et al. The impact of coronary
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to nonionic contrast media. Circulation. 2000;101:
491-497.

Available online: www.sciencedirect.com
1878-8750/$ - see front matter ª 2017 Elsevier Inc. All
rights reserved.

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