Keywords type IV spinal cord arteriovenous malformations - perimedullary arteriovenous fistula
- conus medullaris - intramedullary hemorrhage - filum terminale arteriovenous fistula
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
AVF supplied by 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
(PSA).[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 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 Description
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
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 ([Figs. 1 ] and [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.
Fig. 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.
Fig. 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 image 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 which 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 ([Fig. 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 ([Fig. 4A ]). Due to the enlarged ASA, we decided to proceed with endovascular surgery as the
first choice. We used Magic microcatheter 1.2 Fr (Balt, Montmorency, France). The
microcatheter was navigated through the course of the ASA and the tip of the microcatheter
could be wedged stably 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 ([Fig. 4B, C ]). 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.
Fig. 3 Anteroposterior views of the left T11 intercostal artery angiography in (A ) arterial and (B , 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 (ASA) 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 ).
Fig. 4 (A ) Anteroposterior view of the left T11 intercostal artery angiography in the venous
phase reveal 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 ([Fig. 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 MR angiography of the thoracolumbar spine
obtained 2 years after embolization revealed complete obliteration of the fistula
and significant resolution of spinal cord congestion. At the 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 ([Fig. 6 ]). Spinal angiography, obtained 3 years after endovascular treatment, demonstrated
the normal size of the ASA without recurrence of the fistula ([Fig. 7 ]).
Fig. 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.
Fig. 6 Magnetic resonance imaging of the thoracic spine obtained 2 years after endovascular
treatment. (A ) Coronal T1-weighted, axial (B ) gradient recalled echo (GRE) T2*-weighted, and (C ) proton density (PD)-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.
Fig. 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 PSAs via anastomotic branches. The arterial basket of the conus medullaris consists
of one (unilateral) or two (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 arteriovenous fistula (FTAVF) and PMAVF at
the distal end of 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 single feeder from the ASA. Therefore, it should be classified as intradural ventral
type IVa AVF which is 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. Our case clearly
revealed rupture of a venous varix, embedded into the spinal cord parenchyma caused
hematomyelia by evidence from imaging studies. 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 cervical and craniocervical region.[13 ]
[14 ]
[15 ] Intramedullary hemorrhage or hematomyelia caused by SDAVFs is extremely rare. 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 the 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 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 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 first choice because
there was the accessible dilated ASA and 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 before 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 arteriovenous 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 through 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 the amount of NBCA injected into the dilated
proximal draining vein could further create too extensive thrombosis within the rest
of the perimedullary vein and disturb the normal spinal cord drainage.
Conclusion
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.
