Key-words: Conus medullaris - filum terminale arteriovenous fistula - intramedullary hemorrhage
- perimedullary arteriovenous fistula - Type IV spinal cord arteriovenous malformations
Introduction
Spinal cord arteriovenous malformations have been classified into four subtypes including
Type I, spinal dural arteriovenous fistulas (SDAVFs); Type II, intramedullary glomus
malformations; Type III, extensive juvenile malformations; and Type IV, intradural
perimedullary arteriovenous fistulas (PMAVFs). Type IV spinal cord arteriovenous malformations
have been further divided into three subtypes including Type IVa, small or low-flow
arteriovenous fistula (AVF) supplied by a single arterial branch of the anterior spinal
artery (ASA); Type IVb, intermediated-sized fistula supplied by multiple arterial
feeders; and Type IVc, giant high-flow fistula fed by several feeding vessels of the
ASA and posterior spinal artery.[[1 ]]
Intradural extramedullary AVFs were first described by Djindjian et al.[[2 ]] in 1977 and later were classified as Type IV PMAVF, direct communication of the
intrinsic arterial supply of the spinal cord and a vein without an intervening small-vessel
network, by Heros et al.[[3 ]] in 1986. Based on the modified classification of spinal cord vascular lesions by
Spetzler et al.,[[4 ]] they classified Type IV lesions as intradural ventral AVFs which are located ventrally
and in the midline.
PMAVFs at the level of the conus medullaris are rare and classified as Type IV lesions
and presented with either subarachnoid hemorrhage (SAH) or, more commonly, progressive
myelopathy secondary to venous hypertension.[[5 ]],[[6 ]] We described a case of PMAVF of the conus medullaris with remote intramedullary
spinal cord hemorrhage in the thoracic cord. The pathogenesis of thoracic intramedullary
hemorrhage caused by conus PMAVF in our case was discussed.
Case Report
A 37-year-old woman complained of progressive paresthesia of the lower extremities
for 3 months. She went to the local hospital and was treated with some medicines without
improvement. She had no history of any injury. Two weeks later, the patient was hospitalized
to the same local hospital with sudden severe pain in the left lower leg and weakness
of the lower extremities. She also developed urination incontinence requiring urinary
catheterization. Magnetic resonance imaging (MRI) of the spine was performed and showed
an abnormal T2 signal representing spinal cord congestion extending from the conus
medullaris to the level of T6. There were abnormal serpiginous intradural flow voids
along the anterior surface of the spinal cord extending from the level of L2 to the
lower cervical with suspecting two venous varices at the level of T8–9 and T10. At
the level of T8–9, there was abnormal heterogeneous signal intensity on T1- and T2-weighted
image on the left side of the spinal cord, representing intramedullary hemorrhage
[[Figure 1 ]] and [[Figure 2 ]]. The patient was diagnosis of ruptured spinal cord arteriovenous malformations
and was transferred to our institute and admitted for further investigation and management.
The neurological examination revealed the evidence of spastic paraparesis (muscle
strength 4/5), impairment of proprioception, hyperreflexia, and presence of Babinski
sign in the lower extremities.
Figure 1: Sagittal (a) T1-weighted and (b) T2-weighted images of the thoracolumbar spine reveal
serpiginous intradural flow voids along the anterior surface of the spinal cord extending
from the level of L2 to the mid-thoracic. Axial (c) T1-weighted and (d) T2-weighted
images at the level of T8‒9 demonstrate abnormal heterogeneous signal intensity (arrowheads)
on the left side of the spinal cord, probably representing intramedullary hemorrhage
Figure 2: Sagittal T1-weighted images of (a) the cervical and (b) thoracic spine show intradural
flow voids (arrowheads) along the anterior surface of the spinal cord extending from
the lower thoracic to lower cervical level. (c) Sagittal T2-weighted images of the
thoracic spine demonstrate two venous varices (arrows) at the level of T8‒9 and T10.
Axial T2-weighted images at the level of (d) T6-7, (e) T7-8, and (f) T9-10 reveal
abnormal hypersignal intensity within the spinal cord, representing spinal venous
congestion
Spinal angiography was obtained and demonstrated a PMAVF of the distal end of the
conus medullaris at the level of L2, supplied by the enlarged sulco-commissural feeder
arising from the enlarged ASA originating from the left T11 intercostal artery with
cranial drainage through the dilated anterior spinal vein (ASV) into the tortuous
perimedullary veins up to the lower cervical level. There was a venous dilatation
at the proximal draining vein [[Figure 3 ]]. The venous phase of the left T11 intercostal artery angiography disclosed the
large venous varix at the level of T8–9 pointing to the left side, probably corresponding
with the area of intramedullary hemorrhage [[Figure 4 ]]a. Due to the enlarged ASA, we decided to proceed with endovascular as the first
choice. We used Magic microcatheter 1.2 Fr (Balt, Montmorency, France). The microcatheter
was navigated through the ASA and the tip of microcatheter could be wedged into the
enlarged left sulco-commissural artery just proximal to the fistula.With heparinization,
transarterial embolization with N-butyl cyanoacrylate (NBCA) through the ASA was successfully
performed with reaching the venous pouch of ASV [[Figure 4 ]]b and [[Figure 4 ]]c. A mixture of NBCA and an oil-based contrast agent (Lipiodol Ultra Fluid; Guerbet,
Aulnay-sous-Bois, France) was prepared in proportions of 1:0.7 ratio of NBCA to Lipiodol.
Spinal angiography after embolization confirmed complete obliteration of the fistula
and preservation of the ASA. To prevent further venous thrombosis, the patient received
the prophylactic anticoagulation after the procedure.
Figure 3: Anteroposterior views of the left T11 intercostal artery angiography in (a) arterial
and (b and c) venous phases reveal a perimedullary arteriovenous fistula (asterisks)
of the distal end of the conus medullaris at the level of L2, supplied by the enlarged
sulco-commissural feeder arising from the enlarged anterior spinal artery with cranial
drainage into the dilated anterior spinal vein. There is a venous dilatation (curve
arrows) at the proximal draining vein. The normal-sized ASA (arrows) distal to the
fistula is noted. (d) Selective angiography with microcatheter through the ASA clearly
demonstrates the fistulous point (asterisk) located above the arterial basket of the
conus medullaris forming from the ASA and posterior spinal arteries (arrowheads).
Figure 4: (a) Anteroposterior view of the left T11 intercostal artery angiography in the venous
phase reveals the large venous varix (arrow) at the level of T8‒9 pointing to the
left side, probably corresponding with the area of intramedullary hemorrhage. (b)
Oblique view of selective angiography with the microcatheter through the enlarged
left sulco-commissural artery clearly demonstrates the fistulous point (arrowhead)
and proximal draining vein. (c) During embolization, the glue cast can occlude the
fistula (arrowhead) and the venous pouch of anterior spinal vein
MRI of the thoracic and lumbar spine, obtained 2 months after endovascular treatment,
showed the disappearance of intradural flow voids and thrombosed venous aneurysm at
the level of T8–9 on the anterolateral cord and above the distal end of the conus
medullaris [[Figure 5 ]]. The patient had gradually improved until being ability to walk independently without
residual pain of the left lower leg 6 months later. Bladder function had completely
recovered at 1 year after treatment. MRI and magnetic resonance angiography of the
thoracolumbar spine obtained 2 years after embolization revealed complete obliteration
of the fistula and significant resolution of spinal cord congestion. At T8–9 level
on the left anterolateral part of the spinal cord, there was hyposignal intensity
on T1-weighted, gradient-recalled echo T2*-weighted, and proton density-weighted images,
probably corresponding to hemosiderin [[Figure 6 ]]. Spinal angiography, obtained 3 years after endovascular treatment, demonstrated
the normal size of the ASA without recurrence of the fistula [[Figure 7 ]].
Figure 5: Magnetic resonance imaging of the thoracic spine obtained 2 months after endovascular
treatment. At the level of T8‒9 on the anterolateral cord, (a) Sagittal and (c) axial
T1-weighted images show hypersignal intensity, and (b) sagittal and (d) axial T2-weighted
images demonstrate hypersignal intensity surrounding with hyposignal intensity (black
and white arrowheads), probably indicating thrombosed venous aneurysm. There are multiple
small hypersignal intensity foci (black arrow) at the level of L2 just above the distal
end of the conus medullaris, probably representing thrombosed venous pouch.
Figure 6: Magnetic resonance imaging of the thoracic spine obtained 2 years after endovascular
treatment. (a) Coronal T1-weighted, axial (b) gradient-recalled echo T2*-weighted,
and (c) proton density-weighted images demonstrate hyposignal intensity (arrowheads)
at the level of T8‒9 on the left anterolateral part of the spinal cord, probably corresponding
to hemosiderin
Figure 7: Spinal angiography obtained 3 years after endovascular treatment. Anteroposterior
views of the left T11 intercostal artery angiography (a) with and (b) without subtraction
demonstrate the normal size of the anterior spinal artery (white arrowheads) with
a characteristic hairpin turn (black arrowhead) without recurrence of the fistula
Discussion
Type IVa perimedullary fistulas are typically slow-flow lesions and usually located
on the ventral surface of the conus medullaris or filum terminale.[[7 ]] At the level of the conus medullaris, the ASA may form an anastomotic basket with
the posterior spinal arteries (PSAs) via anastomotic branches. The arterial basket
of the conus medullaris consists of 1 (unilateral) or 2 (bilateral) arterial branches
circumferentially connecting the ASA and PSAs.[[8 ]] In our case, the fistula was located at the level of L2. Therefore, it is difficult
to differentiate between filum terminale AVF (FTAVF) and PMAVF at the distal end of
the conus medullaris. Angiographic pattern of conus PMAVF in our case was similar
to FTAVF, which was located ventrally at the midline and supplied by the ASA with
cranial drainage into the perimedullary veins without intervening nidus. Using selective
angiography with the microcatheter through the ASA, we can identify the arterial basket
of the conus medullaris and found that the fistula was located above the arterial
basket of the conus with the presence of the PSAs and normal-sized ASA distal to the
fistula. In addition, hemorrhagic events have never been reported from FTAVF.[[9 ]],[[10 ]],[[11 ]]
Conus PMAVFs usually manifest by progressive myelopathy or acute nonhemorrhagic paraplegia.[[12 ]] Our case initially presented with progressive paresthesia of the lower extremities
secondary to venous congestion and subsequently developed sudden severe pain in the
left lower leg from intramedullary hemorrhage. Conus PMAVF in our case was supplied
by a single feeder from the ASA. Therefore, it should be classified as intradural
ventral Type IVa AVF which is a slow-flow shunt. However, we speculated that this
fistula should be considered as a relatively high-flow fistula due to markedly enlarged
feeder and draining vein. The high pressure can cause multiple venous varices. A high-flow
fistula in our case may produce high pressure in the venous varix, embedded into the
spinal cord parenchyma, at the level of T8-9 leading to intramedullary hemorrhage.
A high-flow fistula in our case may produce high pressure in the venous varix at the
level of T8–9 leading to intramedullary hemorrhage.
Similarly, hemorrhage from SDAVFs is usually rare and may occur as SAH from the fistulas
in the cervical and craniocervical region.[[13 ]],[[14 ]],[[15 ]] Intramedullary hemorrhage or hematomyelia caused by SDAVFs is extremely rare. A
previous study was reviewed in the literature of SDAVFs with intramedullary hemorrhage
and showed only six cases. All but one of the SDAVFs had venous varices of draining
veins, being the source of hematomyelia.[[16 ]]
Type IVa PMAVFs can be treated by surgery, endovascular treatment, or combined approaches.
The goal of treatment is complete obliteration of the fistula with preservation of
normal arterial supply to spinal cord. The key to complete occlusion is obliteration
of the proximal vein.[[5 ]] In Type IVa PMAVFs located at the level or below the conus medullaris, surgical
treatment has been the preferred method of treatment with higher complete obliteration
rates and low rate of recurrence.[[6 ]] However, some authors suggested that it was easy to operate the fistula on filum
terminale but difficult on the conus medullaris.[[17 ]] Endovascular treatment should be considered as second-line choice because of the
difficulty in navigating a microcatheter through the long and tortuous course of the
thin ASA; the possibility of reflux of the liquid embolic material into the ASA; the
risk or tearing, dissecting, thrombosis, or vasospasm of the ASA during embolization;
concerning about recanalization of the fistula; and requiring expertise and experience
in neurointerventional procedure.[[9 ]],[[10 ]],[[11 ]] According to a review about treatment on spinal cord PMAVFs by Ji et al.,[[18 ]] they found that endovascular treatment is more effective in high-flow PMAVFs, leading
to a good outcome.
In the present study, we decided to try endovascular treatment as the first choice
because there were the accessible dilated ASA and the sulco-commissural artery. The
important factor for the successful transarterial embolization is an introduction
of the tip of microcatheter in a more stable and distal position to the shunt point.
During embolization with NBCA, the safety margin for glue reflux was short. The glue
should close the fistula without reflux into the ASA. In addition, the glue should
be stopped just the proximal draining vein for avoiding anterograde venous occlusion.
The safety margin is related strictly to the anatomy of the ASA and the posterior
curve into the sulco-commissural artery that supplies the AV shunt. We cannot allow
any embolic material refluxes more than short segment of this posterior curve which
will immediately arrive in the ASA axis.
Even though the NBCA cast occupied only in the localized area (only in the sulco-commissural
artery and proximal draining vein), the prophylactic anticoagulation was used in our
case because the fistula is quite large and amount of NBCA injected into the dilated
proximal draining vein could further create too extensive thrombosis within the rest
of perimedullary vein and disturb the normal spinal cord drainage.
Conclusions
The authors reported an extremely rare case of conus PMAVF presenting with remote
intramedullary hemorrhage secondary to ruptured venous varix, confirmed by imaging
studies. This fistula was relatively high flow due to markedly enlarged feeder and
multiple venous pouches. We speculated that an increased venous flow into a varix
may be considered an important risk factor of hemorrhage.
Consent
The patient has given consent to be enrolled and has her data published.
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent forms.
In the form, the patient has given her consent for her images and other clinical information
to be reported in the journal. The patient understands that name and initials will
not be published, and due efforts will be made to conceal identity, but anonymity
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