0148-396X/79/0504-0476$02.00/0
NEUROSURGERY

Vol, 5. No. 4, 1979
Copyright © 1979 by the Congress of Neurological Surgeons

Printed in U.S.A,

Angiographically Cryptic Cerebrovascular Malformations

Henry M. Shuey, Jr., M.D., Arthur L. Day, M.D., Ronald G. Quisling, M.D., and George W. Sypert, M.D.

Division of Neurological Surgery, University of Florida Medical Center, Gainesville, Florida

Three cases of angiographically cryptic cerebrovascular malformations are presented and a review of the cases in the
English literature is tabulated. The typical patient is a 30- to 40-year-old woman with a history of seizures and headache.
There is no antecedent history suggesting hemorrhage. On nonenhanced computerized tomographic scans, these lesions
are denser than normal brain. They enhance with contrast administration. The angiogram demonstrates an avascular
mass. The history, physical findings, and radiographic studies suggest brain tumor. An accurate diagnosis requires
operation and pathological examination of the lesion.

Key words: Angiography, Arteriovenous malformation, Cryptic cerebrovascular malformation, CT scanning, Headache,
Seizures

INTRODUCTION

Most clinically significant cerebrovascular malformations
(CVMs) are readily diagnosed by angiography. When the
arteriogram does not show the characteristic features of a
vascular malformation, this is presumed to be the result of

LEFT .U.F .MED.CNT.RIGHT

CASE REPORTS
Case |
A 20-year-old, left-handed man presented with nocturnal

seizures, generalized headaches, and decreased mental acuity
of 6 months duration. There was no history suggesting intra-

Fic. 1. Case 1. Left, CT scan reveals a denser-than-brain lesion that enhances with contrast administration in the deep temporo-occipital region.
The lesion demonstrates local mass effect by obliterating the ipsilateral circum-mesencephalic cistern. Right, subtracted selective angiography of the
brain demonstrated no CVM, but did reveal an enlarged posterior meningeal artery (arrow).

thrombosis or hemorrhage within the lesion. In this paper we
review a small subgroup of patients with angiographically
cryptic CVMs who underwent computerized tomographic (CT)
scanning and whose clinical history failed to suggest a vascular
etiology for their symptoms. The preoperative diagnosis in this
group of patients was uniformly incorrect. Thrombosis of the
entire malformation, because of its rarity, had not been enter-
tained. The clinical, radiographic, and pathological features of
this subgroup of patients are reviewed, and three new cases
(two with pathological verification) are presented.

cranial hemorrhage. Neurological examination revealed a
healthy male with a dull affect. A mild dysnomia and dyscal-
culia were present, without evidence of other parietal or occip-
ital lobe dysfunction.

Skull x-ray films were normal. An electroencephalogram
(EEG) showed a left temporal lobe seizure focus. CT scanning
revealed a partially calcified mass 4 cm in diameter in the deep
left temporo-occipital region (Fig. 1, /eft). The lesion enhanced
with contrast administration, especially toward the incisura.
On magnified subtraction angiography, an avascular mass was

October 1979

identified near the left medial tentorial margin (Fig. 1, right).
An enlarged posterior meningeal artery was present, but it did
not visibly contribute to the lesion. Pneumoencephalography
showed a lobulated mass elevating the left ambient cistern
wing. The cerebrospinal fluid was normal. Tentorial menin-
gioma was the preoperative diagnosis.

Using a subtemporal approach, we encountered a vascular
lesion measuring 5S cm in diameter on the inferior surface of
the left mesial temporal lobe. On incision, we found gritty
calcification, and arterial hemorrhage ensued. A subtotal re-
section was accomplished. On microscopic examination, mul-
tiple dilated vessels that contained no elastic layer within their
thickened walls were identified (Fig. 2). Gliosis, old hemor-
rhage, and foci of calcification were also present. The tissue
diagnosis was venous angioma.

The postoperative course was complicated by focal seizures,
transient right homonymous hemianopsia, right-left confusion,
and finger agnosia. These deficits resolved after the anticon-
vulsant medications were increased. Six months later, the pa-
tient was free of convulsions. His mental dullness had im-
proved, and he had returned to work.

J
wah

Fic. 2. Case |. Venous angioma. There are variably sized multiple
thin-walled vascular channels with no intervening normal brain. Vary-
ing stages of resolving small hematomas were identified, as were foci
of calcification. Special stains demonstrated no arterial structures.

CRYPTIC MALFORMATIONS 477

Case 2

A 59-year-old, right-handed woman presented with an 8-
year history of complex partial temporal lobe seizures and
episodic headaches. More recently, she had developed an in-
creased frequency of seizures and an unsteady gait. There was
no history suggesting hemorrhage. Neurological examination
demonstrated a poor attention span, impaired judgment, in-
appropriate affect, mild right hemiparesis, and a partial right
gaze paresis. Astasia-abasia was also present.

Skull x-ray films revealed small punctate calcifications in the
left temporal lobe. An EEG showed left temporal polymorphic
delta activity associated with sharp wave activity. An isotope
scan showed two or three superficial lesions in the left fronto-
temporal region. CT scanning detailed two partially calcified
masses in the left middle fossa that were denser than brain and
that enhanced with contrast administration (Fig. 3, eft). Sub-
tracted selective external and internal carotid angiography
revealed an avascular lesion of the middle fossa (Fig. 3, right).
Meningioma was the preoperative diagnosis

At operation we identified a partially calcified chronic he-
matoma measuring 4 cm in diameter in the left middle temporal
gyrus. Active arterial hemorrhage ensued during its evacuation.
A subtotal resection of the lesion was accomplished. On micro-
scopic examination a large network of fibrosed, hyalinized,
calcified blood vessels was present (Fig. 4). The intervening
brain was gliotic, with many hemosiderin-laden macrophages.
Elastic stain demonstrated sporadic elastic content within some
vessel walls. Our pathological diagnosis was arteriovenous
malformation.

Postoperatively there was no neurological improvement. The
patient’s seizure control improved with a new medical regimen.

Case 3

Four years before admission, this 64-year-old woman devel-
oped a sudden right hemiparesis, which gradually improved
over several months. Three years later, she developed mild
diplopia. Five months before admission, the right hemiparesis
and diplopia increased. Initial examination on admission re-
vealed severe right spastic hemiparesis, right hemihypesthesia
and hemihypalgesia, and a right Babinski sign.

Skull x-ray films were normal. CT scanning showed a
densely calcified 2-cm lesion in the left midbrain, which ex-

LEFT.U.F .MED.CNT.RIGHT

Fic. 3. Case 2. Left, CT scan shows two partially calcified mass lesions in the left inferior frontotemporal region, which have enhanced with
contrast administration. Right, two avascular masses (arrows) are seen in the late arterial phase in the left carotid angiogram. Subtracted selective
external and internal carotid artery angiograms failed to demonstrate any CVM.

478 SHUEY etal.

tended to the left tentorium (Fig. 5, /eft). The mass enhanced
minimally with contrast administration. Angiography revealed
an avascular intra-axial pontine lesion (Fig. 5, right). Pneu-
moencephalography demonstrated a left midbrain mass with
left tentorial notch extension. Brain stem glioma was the pre-
operative diagnosis.

At operation we noted that the left cerebral peduncle was
swollen and blue-black in appearance. Many arterioles and
“red” venules were observed on the ventral midbrain surface.
Longitudinal microsurgical incision of the thinned peduncle
yielded a free flow of chocolate-colored fluid. A residual solid
calcified hematoma within the midbrain was deemed nonre-
sectable. Microscopic examination of the tissue showed fibril-
lary gliosis with hemosiderin deposition; however, the biopsy
specimen was too small for definitive diagnosis.

The patient’s preoperative hemiparesis was increased im-
mediately after operation, but had improved at the time of
discharge. Six months later, the patient was ambulatory with
a minimal right spastic hemiparesis that was less marked than
preoperatively.

DISCUSSION

CT scanning suggests the correct diagnosis in greater than
90% of angiographically proven cerebrovascular malforma-

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‘ase 2. Arteriovenous malformation. There is a large net-
iably sized vascular channels with intervening gliotic brain.
Special stains demonstrated elastic tissue within the vessel walls.

LEFT.U.F.MED.CNT.RIGHT

Neurosurgery, Vol. 5, No. 4

tions (2). The enlarged vessels of the CVM characteristically
exhibit a serpiginous pattern during contrast enhancement.
Calcification within the lesion is also frequently present. Most
CVMs produce no significant mass effect: in fact, local atrophy
may be present with attendant ipsilateral ventricular dilatation.
Those cases that do not demonstrate the angiographic features
of CVMs presumably have undergone thrombosis, either spon-
taneously or as a result of hemorrhage. Twelve pathologically
proven cryptic CVMs that had no apparent history of hemor-
rhage and were studied with both angiography and CT scan-
ning have been reported (1, 3, 4). Our Cases | and 2 meet these
criteria. Table | summarizes the clinical, angiographic, and
pathological features of these 14 patients.

In this group, the major presenting symptoms were seizures
and headache. Only one patient presented with a progressive
neurological deficit. Although the age range was I to 60 years,
most patients were between the ages of 20 and 40. There was
an 11:3 female predominance. Five malformations were iden-
tified in the parietal lobe, five in the temporal lobe, three in the
frontal lobe, and one at the frontotemporal junction. These
lesions, therefore, closely corresponded with the hemispheric
middle cerebral artery distribution of other CVMs.

Although angiography failed to demonstrate the arteriove-
nous malformation, an avascular mass was detectable in 71%
of the cases. Most lesions were discovered to have large patent
vessels at operation in spite of the negative angiography. One
of our cases also had an enlarged meningeal vessel, which
confused the preoperative diagnosis. At operation, we deter-
mined that this vessel was unrelated to the lesion. Kramer and
Wing reported a similar case (3). The pathological diagnoses
of these surgical specimens were arteriovenous malformation
in 11 cases, venous angioma in 2 cases, and cavernous angioma
in | patient.

The CT scans showed uniform findings. The precontrast
scans showed lesions that were denser than the normal sur-
rounding brain. Some scans demonstrated calcific deposits.
Twelve of the 14 lesions enhanced with contrast administration.
Ten of 14 exhibited a mass effect, but the degree of distortion
was disproportionately small for the true size of the lesion.
When radiographic low density surrounded a lesion, chronic
hematoma was found.

The preoperative diagnosis of these lesions was consistently
incorrect. Diffuse enhancement and minimal mass effect led to
a diagnosis of glioma in most cases. When the lesions were

Fic. 5. Case 3. Left, CT scan shows a calcified mass lesion in the left midbrain, as well as extension of the lesion into the interpeduncular cistern.

Right, angiography failed to demonstrate any abnormal vessels.

October 1979

CRYPTIC MALFORMATIONS 479

TABLE |

Clinical, Angiographic, and Pathological Features of 14 Cases of Cryptic Cerebrovascular Malformation

CT Scan Findings
- Chief = Preoperative Findings Pathelseye
Authors. Sex Age Complaint Before After Angiography Diagnosis at Location athology’
sentra Metis Operation
contrast contrast
Golden and E 32 Headaches Dense Enhanced Normal Glioma Vascular Superficial AVM
Kramer. frontal
1978
Kramer and SF. 11-39. Seizures, 6: Dense Enhanced (8/10), Mass (7/10), Glioma Most had Temporal. 4: AVM. 8:
Wing. 1977 2M headaches, 3; (8/8) not enhanced normal (2/10), patent frontal, 2: VA, |;
progressive (1/10), unde- enlarged vessels parietal. 4 CALL
deficit. | termined artery (1/10)
(1/10)
Lukin et al. F 60 Seizures for Dense Enhanced Mass None Avascular Left parietal AVM
1977 40 yr superficial
Shuey et al., M 20 Seizures Dense Enhanced Mass Tentorial Vascular Inferiortem- VA
1979 meningioma poral
Fe 59 Seizures Dense Enhanced Mass Meningioma — Vascular. Frontowem- = AVM
poral
* Abbreviations: AVM, arteriovenous malformation; VA, venous angioma; CA, cavernous angioma
adjacent to dura or had an enlarged meningeal blood supply, COMMENTS

meningioma was suspected. Only at operation was the true
nature of each lesion disclosed.

The marked female predominance within this subgroup is
unexplained. Most of these woman are in the hormonally
active age range. Inasmuch as these lesions demonstrate path-
ological evidence of old hemorrhage and thrombosis, this may
reflect a manifestation of a hypercoagulable state. Because of
the small number of patients within this group, this conjecture
is statistically unsubstantiated.

In summary, angiographically cryptic cerebrovascular mal-
formations present with a history suggesting brain tumor. The
typical patient is a hormonally active woman who presents
with a seizure disorder and headaches. Angiography reveals an
avascular mass usually in the temporal or parietal region. CT
scanning identifies an enhancing lesion with a mass effect
disproportionately smaller than the size of the lesion. Although
careful interpretation of the radiographic findings may suggest
the correct diagnosis, microscopic confirmation is required for
definite verification.

ACKNOWLEDGMENTS

We gratefully acknowledge Dr. W. Ballinger and the Divi-
sion of Neuropathology at the University of Florida, Gaines-
ville, Florida, for their review of the pathological findings.

Received for publication, May 23, 1979; accepted, June 12, 1979.

Reprint requests: Arthur L. Day, M.D., Division of Neurological
Surgery, University of Florida Medical Center, Gainesville, Florida
32610.

REFERENCES

|. Golden, J. B. and Kramer, R. A. The angiographically occult
cerebrovascular malformation: Report of three cases. J. Neuro-
surg., 48: 292-296, 1978.

2. Kendell, B. E. and Claveria, L. E. The use of computed axial
tomography (CAT) for the diagnosis and management of intracra-
nial angiomas. Neuroradiology, 12: 141-160, 1976.

3. Kramer, R. A. and Wing, S. D. Computed tomography of angio-
graphically occult cerebral vascular malformations. Radiology,
123: 649-652. 1977.

4. Lukin, R. R., Chambers, A. A.. and Tomsick, T. A. Cerebral
vascular lesions: Infarction, hemorrhage, aneurysm, and arterio-
venous malformation. Semin. Roentgenol., 12: 77-89, 1977.

When an arteriovenous malformation (AVM) presents itself
as an avascular mass, having lost its characteristic angiographic
features, it can be considered angiographically “cryptic.” Yet
an isotope scintigram, particularly the CT scan, invariably
reveals a mass lesion. The authors have described three such
cases.

The unanswered riddle is why some AVMs obliterate their
blood supply and become angiographically “cryptic.” The
commonest cause is hemorrhage into the lesion. This seems to
be the explanation in all three cases detailed by the authors.

In their monograph, Pool and Potts (1) cite an instance of
atheromatous occlusion of a vessel as evidence of “cryptoge-
nesis.” I have reported a case (Neurosurgery, 1: 287-290, 1977)
in which increasing tortuosity and hemodynamic turbulence
probably caused sufficient resistance to blood flow and led to
thrombosis of the entire lesion. The patient was a child.

I do not believe that the authors offer sufficient evidence for
epidemological conclusions. Their literature search is incom-
plete. Why these lesions bleed profusely when their blood
supply seems to have been obliterated remains unanswered.
Yet their paper does reiterate a clinical lesson that merits re-
emphasis.

Peter Dyck, M.D.
Los Angeles, California

1, Pool, J. L. and Potts, D. G. Aneurysms and Arteriovenous Anomalies
of the Brain. New York, Harper and Row, 1965.

The authors have addressed themselves to only one type of
angiographically cryptic malformation, namely one that has
subclinically bled in the past and subsequently demonstrated
variable degrees of partial thrombosis, fibrosis, and calcifica-
tion. Other malformations may be angiographically cryptic
because they are extremely small or because a recent hemor-
thage has resulted in some degree of thrombosis and oblitera-
tion.

[also point out that in Case | the lesion is a venous angioma;
however, the venous phase of the angiogram is not included
and the arterial phase would be expected to be normal in this
situation.

Robert Lukin, M.D.
Cincinnati, Ohio