Keywords dural arteriovenous fistula - foramen magnum - ethylene vinyl alcohol - vertebral
artery - occipital artery
Introduction
Dural arteriovenous fistulas (DAVFs) are rare vascular malformations, and the location
at the craniovertebral junction (CVJ) is extremely uncommon.[1 ] These are usually acquired and idiopathic, but history of venous sinus thrombosis,
craniotomy, and trauma do exist in number of patients.[2 ] The most common locations are sigmoid, transverse, and cavernous sinuses and are
classified based on venous drainage pattern. The most common classifications used
are Cognard and Borden. The Cognard classification is based on direction of dural
sinus drainage, the presence or absence of cortical venous drainage (CVD), and venous
outflow architecture and divide lesions in to five types.[3 ]
[4 ]
The initial clinical presentation of DAVF at FM is wide ranging, but most patients
present with symptoms of progressive ascending myelopathy. Signs and symptoms of SAH
in patients with intracranial venous drainage with or without associated aneurysms
are not so common.[5 ] Transarterial embolization is a preferred route but standalone transvenous or combined
approaches are being used to achieve complete obliteration.[6 ]
[7 ] As this is very uncommon location for DAVF and has sparse data, we analyzed data
of eight patients with their presentation, angioarchitecture, and outcomes after endovascular
treatment.
Patients and Methods
From January 2009 to December 2020, data of eight patients with DAVF at FM, treated
endovascularly by transarterial approach at our institution were retrieved. The parameters
analyzed were, clinical presentation, radiological and angiographic features, procedural
outcomes, and follow-up results. Clinical data of the patients is summarized in [Table 1 ]
Table 1
Clinical data of eight patients with AV fistula at foramen magnum
No
Age/
Sex
Presentation
Investigation
Feeders
Drainage
Angiographic result
Complication
MRS at 6 mo
1
52Y/M
Acute headache
CT—Normal
LP—-Xanthochromia
MRI—4th V Bleed
VA
Median anterior medullary with aneurysm.
Spinal peri medullary
Complete
Lateral medullary syndrome.
Stuck microcatheter
0
2
59Y/F
Myelopathy
Ascending quadriparesis
+Sphincters
Cervical cord edema, Flow voids
OA, VA
Spinal peri medullary down to
cauda equina
Complete
No
3
3
45Y/F
Myelopathy
Ascending Quadriparesis
With +Sphincters
Cervical cord edema
Flow voids
OA
Spinal peri medullary
Complete
No
3
4
53Y/M
Acute Quadriplegia
LCN +
Pre medullary hematoma
Cervical cord edema
Flow voids
VA, ASA, APhA
Median anterior medullary and spinal peri medullary
Complete
No
0
5
38Y/M
Acute headache
CT-SAH
VA
Posterior medullary vein
Complete
No
0
6
53Y/F
Right ear bruit
MRI—C cord flow voids
No edema
OA
SPS and peri medullary veins
Complete
No
O
7
44Y/M
Myelopathy—Ascending quadriparesis
Cervical cord edema
VA
Spinal peri medullary veins
Complete
No
O
8
65Y/M
Myelopathy-paraparesis
Cord edema dorsal level
VA
Spinal peri medullary vein
Complete
No
O
Abbreviations: CT, computed tomography; LCN, lower cranial nerve; LP, lumbar puncture;
MRI, magnetic resonance imaging; MRS, Modified Rankin Scale; OA, occipital artery;
SAH, subarachnoid hemorrhage; SPS, superior petrosal sinus; VA, vertebral artery.
Transarterial Approach
All interventions were done under general anesthesia. Bilateral femoral artery access
was used, one for embolization and another for control angiography. Injection heparin
sulfate was administered in a dose as per weight of the patient. One liter flushing
solution of saline in guide catheter was infused with 3 mg of nimodipine. Guiding
catheter was positioned in major artery, as distal as possible to get good support.
Working angles for embolization were chosen based on careful analysis of pre-embolization
angiograms. Marathon microcatheter (MTI-ev3, Irvine, California, United States) was
navigated inside the feeder artery over Traxcess 014 inch micro-guidewire under road
map guidance. For OA, as far as possible trans osseous branch was catheterized. Neuro-meningeal
trunk catheterization of ascending pharyngeal artery (APhA) was performed. Once the
microcatheter tip was navigated to a position as close to the fistula site, super
selective (SS) runs were performed. The microcatheter was slowly flushed with 10 mL
saline and 0.3 mL of dimethyl sulfoxide was injected to fill dead space of microcatheter.
Onyx embolization was performed once precise position was attained. Under blank roadmap
guidance onyx 14/18 was injected slowly in pulsatile fashion. Reflux of embolization
material was closely monitored, and injection was stopped after reaching permitted
reflux. Pressure cooker technique was used to prevent further reflux and facilitate
forward progression of onyx when required.[8 ] Intermittent control angiograms were done. Embolization was stopped once complete
obliteration was achieved.
Postoperative Management
All patients were managed postoperatively in ICU. Antibiotics were administered as
per our protocol for three doses. If there was venous stagnation low molecular weight
heparin, enoxaparin 60 mg was administered subcutaneously twice daily for 3 days.
Intense physiotherapy was given to patients with quadriparesis and quadriplegia. Speech
and swallowing therapy was given to patient with lower cranial nerve involvement.
Supportive treatment was given as necessary. Plain CT brain was performed in all patients,
immediately postoperatively and a day prior to discharge unless otherwise indicated.
MRI of CVJ with cervical spine was performed at the time of discharge of patients
with myelopathy. Follow-up DSA was done in six patients at 6 month follow-up visit.
Case 1
A 52-year-old male presented with history of three episodes of sudden onset severe
headache and neck pain over a period of 1 month. Patient was referred to us on fourth
day of third episode. MRI FLAIR sequence showed hemorrhage in fourth ventricle ([Fig. 1A ]). Lumbar puncture revealed xanthochromic cerebrospinal fluid. Computed tomography
angiography, showed abnormal ascending draining vein over the clivus ([Fig. 1B ]) and fistula at FM very close to right vertebral artery (VA) ([Fig. 1C ]). DSA of right VA showed a high flow AV fistula at FM fed principally by meningeal
branch from lateral medullary artery, directly arising from V4 segment and multiple
small feeders from V3 segment ([Fig. 1D,E ]). It was drained predominantly cranially with draining vein aneurysm at its commencement.
Spinal peri medullary vein was filling retrogradely from principal cranial peri medullary
vein ([Fig. 1F ]). Since patient had multiple episodes of hemorrhage probably from the aneurysm on
draining vein, it was decided to treat this lesion with transarterial onyx embolization.
Complete obliteration of fistula was achieved with Onyx 18 injection through Marathon
microcatheter over a period of 45 minutes ([Fig. 1G ]). Microcatheter tip got trapped by refluxed onyx cast and it was difficult to retrieve
it. Catheter was detached at groin while maintaining slight traction and allowed to
retract. Post procedure patient had severe vertigo, difficulty in swallowing, and
ataxia due to a small infarct at lateral medulla ([Fig. 1I ]). Ataxia and swallowing started improvement in the second postoperative week. At
6 months follow-up, his symptoms completely disappeared. Follow-up DSA done at 6 months
showed no trace of AVF.
Fig. 1 (A ) Fluid-attenuated inversion recovery magnetic resonance imaging sequence demonstrating
bright appearing lesion in the 4th ventricle. (B ) Computed tomography angiography showing abnormal early enhancing vein along the
course of the basilar artery (arrows ). (C ) Reformatted CTA showing fistula very close to the V3–V4 segment junction (arrow ). DSA of right vertebral artery AP (D ) and Lat (E ) showing fistula principally fed by lateral medullary branch arising from V4 segment
with aneurysm of draining vein (arrow ). Super selective run (F ) showing caudal perimedullary venous drainage along with the cranial drainage (arrow ). (G ) Post procedure, vertebral artery angiogram showing complete obliteration of the
fistula. (H ) Subtracted image showing Onyx cast into the fistula, aneurysm, and foot of the draining
vein. (I ) Diffusion weighted image showing acute infarct in the lateral medulla.
Case 2
A 59-year-old lady had history of progressive ascending paresthesia and ascending
weakness of 1 year duration with paraplegia and bowel and urinary dysfunction since
past 1 month. On neurological evaluation, she had grade 0 power in both lower limbs
and grade 2 in upper limbs. All sensations below T2 were absent. All deep tendon reflexes
were exaggerated. Bilateral plantar reflexes were extensor. MRI brain with spinal
cord showed diffuse swelling of cervical and dorsal cord with edema and significant
flow voids over whole length of cord ([Fig. 2A ]). DSA showed DAVF at FM supplied by transmastoid branch of occipital artery (OA)
and dural branch of right VA at C1 level. It was drained by a pair of peri medullary
veins all the way down to conus medullaris ([Fig. 2B–D ]).
Fig. 2 Magnetic resonance imaging T2 (A ) showing cervical and dorsal cord edema and abnormal flow voids. (B ) External carotid artery angiogram showing a dural arteriovenous fistula, fed by
the meningeal branches of the right OA. (C ) Angiogram demonstrating drainage by a pair of medullary veins all the way dawn to
the cauda equina. (D ) Right vertebral artery angiogram revealing additional feeders from the dural branches
of the right vertebral artery at C1 level. (E ) A 4 mm × 20 mm HyperGlide balloon inside the vertebral artery at the origin of the
feeder (arrow ). Post procedure ECA (F ) and Vertebral artery angiogram (G ) showing complete occlusion of the fistula. (H ) Subtracted image showing Onyx cast.
Embolization through OA branch was decided as feeder from VA was very small and short.
The distance between origin of feeder from VA and the fistula site was very short;
hence it was decided to deploy balloon at VA feeder origin to prevent inadvertent
onyx migration in the VA. Hyper glide balloon 4 × 20 mm was deployed at the origin
of right VA feeder ([Fig. 2E ]). Onyx 18 was injected through Marathon microcatheter, positioned close to fistula
from right OA branch. Post procedure ECA and VA angiograms showed complete obliteration
of fistula ([Fig. 2F,G ]). She gradually recovered and started walking with assistance at the end of one
month. Her urinary dysfunction did not show much improvement and was catheter dependent.
Follow-up DSA showed stable result. She was lost to follow-up after 6 months.
Case 4
A 53-year-old physician presented with sudden onset of neck pain, blurred vision,
hoarseness of voice, difficulty in swallowing and imbalance while walking. MRI ([Fig. 3A ]) at the time of presentation showed acute hematoma at pre medullary space with few
flow voids over anterior surface of medulla and upper cervical cord suggesting vascular
lesion. His condition progressively worsened over next 1 week. Repeat MRI ([Fig. 3B,C ]) showed appearance of medullary and cervical cord edema up to C5 level. His symptoms
improved with conservative management over a period of 1 month. He was then referred
to us for decisive treatment. DSA demonstrated high flow DAVF fed by dural branch
of left VA at C1, small branches from junction of V3–V4 segment and branch from anterior
spinal artery at C1 which arose from the VA ([Fig. 3D ]). Venous drainage was both upward and downward over anterior surface of medulla
and anterior surface of spinal cord, respectively. There was an outpouching at origin
of draining vein likely an aneurysm and the site of bleeding (arrow in [Fig. 3E ]). There were no feeders from external carotid artery ([Fig. 3F ]). SS angiograms of each catheterized feeder showed opacification of anterior spinal
artery in spite of catheter navigation close to fistula site. Procedure was abandoned
due to the lack of safety in filling of ASA, as embolization could have led to spinal
cord infarction. Trial of second session was planned after 1 week. Three days later
patient became symptomatic again. Repeat MRI showed extensive medullary and cervical
cord edema ([Fig. 3G ]). Repeat DSA demonstrated the fistula with new feeders from neuromeningeal trunk
of right APhA ([Fig. 3H ]). Dangerous anastomosis between muscular branches of hypoglossal artery with muscular
branches of VA at C1–C2, descending branch from hypoglossal artery with ascending
branch of VA at C2–C3 and between lateral clival artery to ICA either direct or indirect
through MHT and also indirect from superior laryngeal branch through ILT branches
were specifically looked and were absent on selective APhA angiogram. Complete obliteration
of fistula and aneurysm was achieved with 1 mL of Onyx 18 injected through APhA feeder
([Fig. 3I–L ]). Follow-up MRI on 4th day showed significant reduction in cord edema ([Fig. 3M ]). Patient gradually improved and was discharged after 2 weeks with grade 4 power
in all limbs and with significantly improved LCN functions. Patient was asymptomatic
at 6 months follow-up. DSA at follow-up showed stable result.
Fig. 3 MRI T2 (A ) showing abnormal vascular lesion at the level of the anterior foramen magnum with
mild edema of the medulla and cervical cord. Follow up MRI (B ) at 1 week showing premedullary haemorrhage with increased medullary and cervical
cord edema. 3D CTA (C ) showing AF fistula. (D ) Left VA run showing a DAVF fed by the meningeal branches of both intra and extradural
portion of left VA and a small branch from anterior spinal artery (arrow ). Lat VA run showing venous aneurysm (arrow in E ) Normal ECA run (F ). Repeat MRI showing significantly increased cord edema (G ). ECA angiogram (H ) showing newly developed feeders from meningeal trunk of APhA. SS cannulation of
right APhA meningeal trunk (I ). SS run showing filling of fistula (J ). Post ECA run (K ) showing complete occlusion of the fistula. Post VA run showing no filling of fistula
from VA branches (L ). MRI on fourth day showing significant reduction in cord edema (M ).
Results
The age of patients ranged from 38 to 65 years, with mean age of 51 years. There were
five male and three female patients. Slight male predominance was noted (M: F 5:3).
Duration of symptoms ranged from 1 day to 3 years. Patient number six had history
of sigmoid sinus thrombosis. Presentation with progressive ascending myelopathy (N = 4) (50%), acute headache (subarachnoid hemorrhage) (N = 2) (25%), acute quadriplegia with bulbar symptoms (N = 1), and right ear bruit (N = 1) was seen.
Exclusive feeders from VA and OA were seen in four and two patients, respectively.
Dual feeders from a combination of ascending pharyngeal artery and VA; from a combination
of OA and VA were seen in one patient each. The exclusive venous drainage was toward
spinal peri medullary veins (N = 3), brainstem peri medullary veins (N = 1), and both combined (N = 4). Two patients had a draining vein aneurysm.
In seven patients embolization was done using Marathon microcatheter. In patient number
five, Scepter balloon was used for embolization. In patient number two, balloon was
placed in VA across origin of feeders to AVF to prevent migration of Onyx into VA.
Technical complications such as stuck microcatheter and lateral medullary syndrome
were developed in patient number one. Complete obliteration of fistula and foot of
draining veins was achieved in all patients in single session.
Outcomes
The two patients with SAH had no complications and were discharged on 10th postoperative day without any neurological deficit. Patient with right ear bruit
had immediate relief and had no symptoms thereafter till last follow-up. Three patients
with myelopathy achieved complete resolution symptoms. Patient number 2 and 3 showed
significant improvement but both had moderate disability at last follow-up (MRS grade
3). Follow-up angiogram was done in six patients and showed persistent obliteration
of the AVF. Two patients did not report for follow-up DSA.
Discussion
DAVFs accounts for around 10 to 15% of all cranial vascular malformation lesions.[9 ] DAVFs at FM are uncommon and represent 5% of all DAVF lesions.[10 ] The usual feeders are from VA, OA, and APhA. Venous drainage could occur caudally
or rostrally or in both directions. But most of the lesions at this location drain
caudally into the spinal peri medullary veins.[11 ] These are classified as Type V according to Cognard classification of DAVF.
Most patients presents with varied sensory symptoms and slowly progressive myelopathy.
Some may present with acute onset paraplegia or quadriplegia secondary to cord hemorrhage.
Presentation with sign and symptoms of SAH can be rarely seen in these patients and
should always be kept in mind in patient with subtle posterior fossa SAH.[12 ]
[13 ] The patterns of venous drainage dictate clinical presentation. These symptoms are
related to arterialized veins and increased venous pressure leading to cord edema.
Long standing venous hypertension could lead to cord ischemia and subsequent poor
recovery post treatment.
CT angiography, MRI, and MRA and catheter angiography play a key role in the evaluation
of these patients. Due to varying nonspecific clinical and imaging features, the diagnosis
of DAVF can be delayed or missed. The typical MRI findings are spinal cord edema (T2
hyperintensities), that usually extends over 5 to 7 vertebrae and multiple flow voids
of serpentine and engorged peri medullary vessels on T2 imaging. The mere presence
of flow voids without cord edema and signs or symptoms of myelopathy, is a poor predictor
of DAVF.[14 ]
[15 ]
Catheter angiography is the gold standard in the diagnosis of DAVFs. Incongruity between
sites of clinical localization and site of lesion often lead to delay in diagnosis.
In our series, patient number seven had dorsal cord and conus edema, but the location
of fistula was at foramen magnum level. This suggests that, for suspected spinal cord
vascular malformation lesion, along with complete spinal angiogram, six vessel cerebral
angiography must be performed.
Aggressive treatment in DAVF at FM is indicated in all patients who present with signs
of myelopathy non-hemorrhagic neurologic deficit and SAH/ICH to prevent progression
and rebleed. Also, patient with more benign symptom like tinnitus but with high-risk
angiographic features like venous congestion and CVD warrants aggressive treatment.
In patient number six, the severity of symptoms and decreased quality of life necessitated
the treatment. Incidentally presented DAVFs should be managed conservatively with
follow-up imaging if new symptoms appear. In our series we do not have patients with
incidental DAVFs at FM.
The optimal treatment approach to treat DAVFs at foramen magnum is debatable with
both surgical and endovascular modalities having been reported with good results.
Microsurgical disconnection of arterialized vein by either coagulation, cutting, or
clipping is utilized in reported cases with good success. Deep location of the lesion
and proximity to vital structures, microsurgery pose relatively higher risks.[16 ]
[17 ] The advancements in neurovascular technology, devices, and embolization materials
have simplified the use of minimally invasive techniques in the treatment of these
lesions. Of the variety of embolization material, onyx is used more and more frequently.
The advantages of onyx over glue (e.g., n -butyl-cyanoacrylate [NBCA]) is that when it refluxes, injection can be stopped till
it solidifies and then injection can be continued with the expectation that it will
flow forward to fill fistula and the proximal part of the draining vein. The non-adhesive
property and slow polymerization of Onyx allow precise control and longer duration
of injection than NBCA. Due to adhesiveness and fast polymerization of NBCA, intranidal
flow is fast and unpredictable. Glue can prematurely occlude feeding vessel before
reaching to fistula or venous site resulting into incomplete treatment. Multiple studies
have showed that Onyx embolization is associated with more compete obliteration and
lower neurological complications.[18 ]
[19 ]
[20 ]
Trapping of microcatheter to glue cast is often reported in literature.[21 ] Though onyx has non-adhesive property, microcatheter can get stuck to it. Fortunately,
number of trapped microcatheters attributed solely to onyx cast are few.[22 ] The various factors responsible for trapping are reflux of onyx, longer injection
times, acute bends, and small feeding pedicle.[23 ] In such scenarios cutting of microcatheter at the groin puncture site and leaving
in situ is a suitable alternative.[24 ]
Our understanding has stressed several important aspects in diagnosing and treating
these lesions. The delay or misdiagnosis of these lesion is common as initial motor
and sensory symptoms are vague and slowly progress to myelopathy with bowel and bladder
involvement. The resemblance of MRI finding in early stages of disease process with
common spinal cord inflammatory, neoplastic, or compressive lesion has resulted in
delayed diagnosis. On occasion patients are subjected to spinal cord biopsy or unnecessary
surgical treatment. There should be low threshold to perform DSA in highly suspected
patients as delayed diagnosis results in poor outcome and disability even with complete
obliteration of fistula.[25 ]
Microcatheter should be placed as close to the fistula site as possible, to minimize
the risk of accidental embolization of non-target tissues. If there is high chance
of onyx penetration to normal vessel, balloon should be deployed to protect unwarranted
migration as we used in patient number two. Balloon tipped microcatheter is useful
as it plugs and blocks feeding artery preventing reflux and ensuring better distal
penetration. This becomes extremely useful in situation where even short length of
reflux is not permissible. In patient number five it was used because the length of
feeding pedicle from origin at VA and fistula was short. Another advantage it offered
was that it reduced the rapid flow ensuring slow and steady filling of fistulous connections.
In DAVF with feeders from APhA, dangerous anastomosis, both direct and indirect as
mentioned above in patient number 4, particularly to VA and ICA should be carefully
looked after. Reflux of embolizing agent into these anastomotic arteries must be keenly
observed to avoid unwarranted migration. To prevent migration into the VA, reflux
should not be allowed to go past the margin of foramen magnum, and it is better to
stop injecting when reflux has reached up to 1 cm above foramen magnum.
There should be a low threshold for abandoning procedure, if risk of adverse events
is considered to be very high. Procedure was abandoned in patient number four, as
risk of spinal cord infarction was unacceptable. It was also observed that, FM DAVFs
have relatively smaller number of arterial feeders as compared with fistulas of transverse-sigmoid
sinuses. Accordingly complete obliteration in single session with less volumes of
embolizing material can be achieved in these patients.
Limitations
This is a small retrospective study of eight patients.
Conclusion
The clinical presentation of dural AVF at foramen magnum is wide ranging. They can
present with spinal cord involvement, SAH or ear symptoms. Incongruity between site
of fistula and clinical anatomical localization should be kept in mind during evaluation
of suspected case. DSA should be performed and repeated if inconclusive. These lesions
can be treated effectively and safely by transarterial Onyx embolization. Balloon
assistance facilitates safer and quicker embolization. Symptomatic improvement and
prognosis seem to be positive in such patients when treated in time.
