Keywords
dural arteriovenous fistula - myelopathy - angiography - surgical excision of fistula
Introduction
Spinal dural arteriovenous fistula (dAVF) is the most common type of spinal arteriovenous
(AV) malformation but still is a rare entity. Its clinical presentation is vague and
nonspecific. It frequently goes undiagnosed and is often misdiagnosed. This leads
to late diagnosis and consequently delayed treatment and incomplete recovery. Initial
suspicion of this disease invariably is made when dilated venous architecture is incidentally
picked up on a magnetic resonance imaging (MRI) while investigating a patient for
some other clinical diagnosis. The diagnosis can be missed even after doing an MRI,
unless those familiar with this entity scrutinize the MRI for more obvious cord changes
that have already developed. We discuss our experience including diagnostic challenges,
therapeutics, and outcome of three such cases over 6 months and highlight the fact
that an early intervention leads to rapid and good recovery.
Anatomy
The blood supply to the spine and the spinal cord is derived from various segmental
arteries (vertebral arteries, deep and ascending cervical arteries, intercostal arteries,
lumbar and iliolumbar arteries). At each segment, there is a radicular artery that
gives rise to a radiculomeningeal branch that supplies the dura mater and nerve root.
Some of these radicular arteries will also supply the spinal cord as radiculomedullary
or radiculopial arteries. A normal spinal cord has single anterior and paired posterior
spinal arteries that receive their reinforcements from radicular branches of various
segmental arteries. The venous drainage of the spinal cord is through intrinsic radially
arranged veins that connect to pial venous network on the surface of spinal cord.
The extrinsic venous drainage is by pial venous network and anterior and posterior
spinal veins. The superficial veins surrounding the spinal cord drain into the radiculomedullary
veins. These radiculomedullary veins accompany the nerve root exiting from the respective
neural foramina and the dural sheath at this site. In addition, in about 40% individuals
there are bridging veins that exit from the dura at sites other than nerve root sleeve.[1]
[2] In case of spinal dAVF, the fistula lies inside the dura close to the intervertebral
foramen, where one or more radiculomeningeal arteries have a fistulous communication
with the radiculomeningeal vein. The consequent decrease in the AV pressure gradient
leads to engorgement of the perimedullary venous plexuses, the extrinsic and intrinsic
veins, and is thus responsible for a venous congestion resulting in myelopathy.
Material and Methods
Three cases of spinal dAVF were diagnosed over a period of 6 months. The patients
were further evaluated with selective angiography to confirm the diagnosis, localize
the pathology, and delineate the anatomy of fistula. Two cases had significant neurologic
deficit, and the fistula was deemed to be the cause. The third case was incidentally
detected and was not intervened. Neurosurgeons and interventional radiologists jointly
discussed all three cases. The two operated cases were found to be unsuitable for
intervention by neuroradiologists and were worked up for early surgical excision.
The third case is under periodic follow-up.
Results
Case 1
A 65-year-old woman became symptomatic with paresthesia/tingling and numbness of the
left (Lt) lower limb. Over the next 1 month, she developed similar symptoms in the
right (Rt) lower limb and sought medical attention. The symptoms followed an indolent
course for next 3 months wherein the patient started to have difficulty in prolonged
or brisk walk. Climbing stairs became increasingly difficult, and she had tiredness
of legs. Thereafter, she rapidly developed weakness in both lower limbs, and by the
end of 4 months she had become wheelchair bound and required catheterization. So far,
she had been treated for degenerative disc disease, and this rapid worsening prompted
her referral to our center with a clinical diagnosis of multiple sclerosis. On examination,
she had reduced sensation below D6 by around 20% and could barely perceive touch and
pinprick in sacral dermatomes. Tone was increased in lower limbs, and reflexes were
brisk. Ankle clonus was present bilaterally. The patient had significant weakness
of both lower limbs and could not stand even with support. An MRI of the spine revealed
multiple dilated perimedullary veins along the dorsal spine. There was T2 hyperintensity
extending from D5 to conus medullaris. There was postcontrast enhancement of the perimedullary
veins. Angiography confirmed a spinal dAVF with feeder from radiculomeningeal artery
along Lt D10 nerve root. The patient underwent a D10 laminectomy. A single arterial
feeder was identified along the Lt D10 nerve root, and intradurally a single draining
vein led to a conglomeration of perimedullary veins along dorsal aspect of the cord
that appeared turgid and arterialized. The single draining vein was disconnected close
to the dura. Although the conglomeration of arterialized veins appeared less turgid
after disconnection, no significant change was felt intraoperatively. The patient
subjectively claimed to be feeling better within 48 hours of surgery and was discharged
on fifth postoperative day without any objective improvement in her neurologic status.
She improved to some extent by second week post-surgery. Thereafter the improvement
occurred rapidly and steadily. By around fourth week, she was walking with support,
and by the end of 3 months, she had recovered complete power and had been voiding
normally ([Table 1]).
Table 1
Clinical course of operated cases
|
Case 1
|
Case 2
|
|
Preoperative
|
2 wk
|
4 wk
|
8 wk
|
12 wk
|
Preoperative
|
2 wk
|
4 wk
|
8 wk
|
12 wk
|
|
Abbreviation: SCIC, self-clean intermittent catheterization.
|
|
Motor
|
Hip
|
(Rt)
|
2/5
|
3/5
|
4+/5
|
5/5
|
5/5
|
2/5
|
2/5
|
2/5
|
3/5
|
4+/5
|
|
(Lt)
|
2/5
|
3/5
|
4+/5
|
5/5
|
5/5
|
2/5
|
2/5
|
2/5
|
2/5
|
4+/5
|
|
Knee
|
(Rt)
|
2/5
|
2/5
|
4/5
|
5/5
|
5/5
|
1/5
|
1/5
|
1/5
|
2/5
|
4/5
|
|
(Lt)
|
2/5
|
2/5
|
4/5
|
5/5
|
5/5
|
1/5
|
1/5
|
1/5
|
2/5
|
4/5
|
|
Ankle
|
(Rt)
|
2/5
|
2/5
|
2/5
|
3/5
|
5/5
|
1/5
|
1/5
|
1/5
|
2/5
|
4/5
|
|
(Lt)
|
2/5
|
2/5
|
2/5
|
3/5
|
5/5
|
1/5
|
1/5
|
1/5
|
2/5
|
4/5
|
|
Bladder control
|
|
|
On catheter
|
SCIC
|
SCIC
|
SCIC
|
Self-voiding
|
On catheter
|
On Catheter
|
SCIC
|
SCIC
|
Self-voiding
|
|
Sensations
|
|
|
50% below D6
|
Better
|
Better
|
Nearly normal
|
Normal
|
20% below D10
|
Better
|
50% below D10
|
50% below normal
|
Marginally below normal
|
Case 2
A 69-year-old man had pin- and needle-like sensations in both the feet. These sensations
were insidious in onset and persisted for a period of 3 to 4 months. By this time,
the patient had developed reduced sensations in both the feet, and sensations of pins
and needles had subsided completely. Subsequently, by around 6 months, he started
to develop weakness of both the lower limbs. Initially the weakness was in the Rt
ankle that progressed to involve the Rt knee and then hip over a period of 12 months.
This was closely mirrored by weakness in the opposite limb. He was using a walking
stick by the end of 12 months and could walk only by using a walker by 18 months.
During this period, he was treated at various centers for multiple diagnoses such
as degenerative disc disease, hyponatremia, and multiple sclerosis. By the time of
presentation to our hospital, he had been symptomatic for a period of about 26 months
and was wheelchair bound. He had been on steroids for 4 weeks with no improvement.
Significant wasting of the thigh and calf muscles bilaterally was present. On examination
he was found to have spastic quadriparesis with reduced sensation below D10 dermatome.
A review of the previous MRI and a repeat MRI showed dilated perimedullary veins along
the dorsal cord. A T2 hyperintensity was present from D9 to conus medullaris with
contrast enhancement at D11–12 along with cord thickening at this level. A spinal
angiography confirmed a spinal dAVF with feeder from radiculomeningeal artery along
the Rt D9 nerve root. Laminectomy DV9 and partial laminectomy DV8 and DV10 was done.
Intraoperatively single draining vein led to a plethora of arterialized veins on the
dorsal surface of cord. The draining vein was ligated close to the dura. There were
one dominant arterial feeder and an additional doubtful feeder along D10 nerve root.
Both feeders were ligated. The patient had a slow but definite recovery. After 3 months,
he still had residual paraparesis and reduced sensations but was significantly better.
He had started to void on his own ([Table 1]).
Case 3
A 51-year-old woman reported to OPD with pain on lower back radiating to the Lt lower
limb for about 3 months. The patient gave history of a fall from a height about 6
months previously. She had no neurologic deficits. She was evaluated with an MRI study
and was found to have a fracture LV2 with anterior wedging and a syrinx from CV4 to
DV4. Flow voids were noted at lower dorsal level suggestive of spinal dAVF. She further
underwent an angiography, and presence of dAVF along the Lt D7 nerve root was confirmed.
She was counseled in detail about the entity and future course. As she had no symptoms
from the dAVF yet, a decision in line with patient's desire was taken to keep her
under close periodic follow-up for onset of any neurologic deficits and intervene
only if she develops any symptoms.
Discussion
Spinal dAVF is the most common spinal vascular anomaly and constitutes about 70% of
all vascular malformations of the spine.[3]
[4]
[5] Its incidence is very low and is a rare entity in clinical practice, which is often
misdiagnosed.[6]
[7]
[8] Both the patients who underwent surgery had been treated at other centers for 4
and 26 months before being diagnosed. Both operated cases based on their clinical
findings of mixed upper motor neuron (UMN) and lower motor neuron (LMN) features had
been previously evaluated for multiple sclerosis. The second patient had even been
administered a course of steroids without any benefit. This was despite the patient
having undergone MRI study where the significance of perimedullary veins was not appreciated,
thus leading to a delayed diagnosis and truncated recovery. The patient was transferred
to our center because of the progressive course of the disease despite a perceived
optimal treatment. Reevaluation of previous study and a repeat study revealed possibility
of dAVF, which was confirmed with a selective angiography. The presence of fistula
was picked up incidentally in the third case, which had so far not been symptomatic.
Two cases were in seventh decade and one was in sixth decade. One was male and two
were females. Mean age of occurrence in the literature has been reported to be 55
to 60 years, and it is five times more common in men. More than 80% cases occur between
T6 and L2 with sacral and high cervical incidence being less than 4 and 2%, respectively.[3] All these three patients had fistula located between T6 and L2 levels. MRI picked
up prominent perimedullary flow voids in all the three patients ([Figs. 1]
[2]
[3]). Cord edema was seen in two of the patients who underwent surgical ligation subsequently.
All the three patients on spinal digital subtraction angiography had a single radiculomeningeal
feeder with dilated, tortuous perimedullary veins. Postoperative MRI was done after
1 month in both operated cases. First patient revealed complete resolution of the
cord edema and perimedullary flow voids ([Fig. 1e]) whereas the second patient revealed reduction in the cord edema and disappearance
of the perimedullary flow voids ([Fig. 2e]).
Fig. 1 (a) T2-weighted sagittal image showing edema in the dorsal cord. (b) CISS sagittal image showing perimedullary flow voids. (c) T2-weighted axial image showing dorsal cord edema. (d) DSA showing the spinal dAVF with feeder from (Lt) D10 radicular artery. (e) Postsagittal T2-weighted MRI showing complete resolution of the cord edema and perimedullary
flow voids.
Fig. 2 (a) Sagittal CISS sequence showing prominent perimedullary veins. (b) T2-weighted sagittal sequence showing edema of the dorsal cord. (c) Postcontrast image showing enhancement of the edematous cord with perimedullary
veins. (d) DSA showing spinal dAVF with feeder from (Rt) D9 radicular artery and dilated perimedullary
veins. (e) Postoperative MRI sagittal T2-weighted sequence showing reduction in the perimedullary
flow voids.
Fig. 3 (a) T2-weighted sequence of upper dorsal spine showing prominent perimedullary flow
voids. (b) T2-weighted sequence of lower dorsal and upper lumbar spine showing continuation
inferiorly of prominent perimedullary flow voids. Incidentally detected old fracture
LV2. (c) DSA showing dAVF at D7 vertebral level.
Pathologically a spinal dAVF involves an abnormal communication between a radiculomeningeal
branch of the segmental artery with a draining vein and has been discussed under anatomy.
The exact cause of this fistula is not known, but it is presumed to be acquired. The
excessive flow of arterial blood directly into draining veins causes high-pressure
situation in a low-pressure system, leading to congestive changes in the respective
draining area of the spinal cord.
The symptomatology is nonspecific with little to make a confident clinical diagnosis.
Early symptoms include easy fatigability with nonspecific low backache that might
aggravate after exertion because of rise in arterial pressure leading to increased
pressure and flow through the fistula. Radicular pain may or may not occur. Sensory
symptoms such as paresthesias/tingling/numbness, patchy or diffuse sensory loss and
motor symptoms such as weakness of lower limbs, and difficulty in climbing stairs
and/or walking have been reported. Involvement of bowel and bladder in the form of
incontinence or retention of urine generally occurs later in the course of disease.[3] The disease runs a slow indolent course with progressive worsening. However, sudden
onset, rapid worsening, and occasional remissions may also occur.[9] Among our cases, one case had a slow progression of the disease, taking almost 2
years to develop significant deficits. First case, however, had a very rapid progression
from onset of first symptom to becoming wheelchair bound. In both these cases, patients
had sought medical attention in the early presentation of the disease. However, it
was only when they became wheelchair bound that they got referred to tertiary care
center leading to diagnosis of the disease. The initial symptomatology is so vague
and inconspicuous that a rare entity such as spinal dAVF is not even considered in
the differential diagnosis.
As the disease progresses slowly, by the time diagnosis is made, the patient has advanced
deficits. Motor weakness along with bowel and bladder deficits might already be present
before the diagnosis is made or even suspected. Foix and Alajouanine[10]
[11] in their original description have described presence of both UMN and LMN lesions
simultaneously in these patients.
Diagnosis is invariably made after MRI, which identifies the pathologic changes of
dilated and congested venous channels with cord edema and/or myelopathy. Perimedullary
veins appear as dilated serpentine flow voids predominantly located dorsal to the
cord on T2-weighted sequences and seen as flow voids. These vessels can be further
confirmed by using heavy T2-weighted sequences such as CISS (constructive interference
in steady state) or FIESTA (fast imaging employing steady state acquisition). Cord
edema is identified as hyperintensity seen on T2-weighted sequences extending over
multiple segments with or without a hypointense rim around it because of deoxygenated
blood present in the surrounding capillaries. The location of cord edema, however,
is not suggestive of the location of fistula that may be located distant from the
site of cord edema.[12] Following contrast administration, enhancement will be seen in the perimedullary
veins and sometimes in the cord due to breakdown in the blood-spinal cord barrier.
Superselective angiography remains the gold standard to delineate the anatomy of fistula
and differentiate these from other AV malformations. However, this entails injecting
contrast in each segmental artery to look for the fistula. Herein lies the significance
of magnetic resonance angiography (MRA) and computed tomographic angiography (CTA)
to suggest the possible location of fistula.[13]
[14]
[15]
[16]
[17] CTA, however, has the disadvantage of radiation exposure, and hence, although it
is informative, it has limited utility. A spinal dAVF on angiography appears as a
slow-flow lesion with an arterial feeder from radiculomeningeal artery, bunch of feeding
vessels from a lesion located invariably in the dura and converging into a draining
vein. Dilated perimedullary veins due to back pressure may be seen either ascending
or descending.
The treatment of spinal dAVF aims at its exclusion from the vascular system either
by surgical excision or embolization. Surgical excision involves ligation of arterial
feeder and the draining vein. The feeder artery has to be ligated closest to the dura
as numerous collaterals may be present, and if it is ligated farther from the dura,
it might give only transient relief until the collaterals become more active and nullify
the benefits of ligation of the feeder. Similarly, the vein has to be ligated closest
to the dura where the fistula zone lies. Embolization of this fistula involves superselective
cannulation of the feeder, and nidus has to be passed before liquid embolic agent
can be placed at the proximal part of the draining vein. Endovascular therapy is reported
to have a success rate varying from 25 to 75%.[9]
[18] Surgical excision of fistula has been found to have a success rate of 98%.[19]
Conclusion
Spinal dAVF is more common than what is perceived. Numerous patients remain undiagnosed
till advanced stages of clinical deterioration. Spinal dAVFs are surgically curable
and show remarkable recovery. An early diagnosis can be made with increased awareness
of this entity and early intervention.
Contributions
-
Dr Manish Sharma: Conceptualization, data collection, manuscript writing.
-
Dr Ankit Mathur: Radiologic evaluation, manuscript writing.
