Curable Cause of Paraplegia
Spinal Dural Arteriovenous Fistulae
Nozar Aghakhani, MD; Fabrice Parker, MD, PhD; Philippe David, MD;
Pierre Lasjaunias, MD, PhD; Marc Tadie, MD, PhD
Downloaded from http://stroke.ahajournals.org/ by guest on June 17, 2017
Background and Purpose—The rarity of spinal dural arteriovenous fistulae makes physicians often overlook this potential
diagnosis in patients with progressive gait disturbance and paraparesis. Consequently, patients with spinal dural
arteriovenous fistulae can gradually become completely paraplegic if the final diagnosis is delayed considerably. The
objective of the current study is to demonstrate that, particularly in patients with paraplegia, surgical treatment of fistula
is necessary and often has a favorable outcome.
Methods—Of 42 patients with spinal dural arteriovenous fistulae treated in our institution (surgery or endovascular
treatment), 6 were paraplegic preoperatively (Grade IV on the McCormick scale and Grade V on the Aminoff scale,
Grade 5 of modified Rankin Scale with motor ASIA between 0 and 10 for both lower limbs). Their clinical history
revealed that paraplegia appeared progressively within a period of ⬍3 months. All patients were clinically evaluated at
6 weeks, 6 months, and then annually during an average follow-up of 3 years. Patients received at least one spinal
angiography and MRI test during the follow-up period.
Results—Total exclusion of the fistula was performed surgically in all cases and was confirmed by spinal angiography. No
surgical complications were recorded. All patients improved postoperatively. Three patients showed almost normal
walking (Grade I on the McCormick scale, I on the Aminoff scale, Grade 1 of modified Rankin Scale) and 3 were able
to walk with a cane (Grade II on McCormick, Grade III on Aminoff scale, Grade 2 of modified Rankin Scale). MRI
tests were normal in all patients.
Conclusions—Our results indicate that treatment of fistula is a necessary intervention, even in patients with complete
paraplegia. (Stroke. 2008;39:2756-2759.)
Key Words: paraplegia 䡲 spinal dural arteriovenous fistulae 䡲 surgery 䡲 treatment
S
pinal dural arteriovenous fistulae (SDAVF) are the
most common type of spinal vascular malformations.1
Although considered a well-known pathology in the neurological and neurosurgical milieu, SDAVF is frequently
ignored and misdiagnosed by other physicians. Early
diagnosis is difficult due to the rarity of SDAVF and the
nonspecific symptoms (progressive myelopathy). In a large
series reported by Jellema et al,2 the median delay of
diagnosis was 15 months by which time 62 of 80 patients
had severe weakness of the legs and 15 had become
wheelchair-bound.
There are several reports on the clinical presentation,
treatment, and outcome of patients with SDAVF in the
literature. Steinmetz1 analyzed data collected from 20 papers
and 532 patients. The typical clinical presentation of SDAVF
is progressive myelopathy with neurological deterioration
such as paraparesis, sensory disturbance, and sphincter dysfunction. If the SDAVF diagnosis is missed on initial evaluation, the neurological deterioration can worsen over time. As
reported by Aminoff et al3 within 3 years after the onset of
symptoms, over 90% of patients are unable to walk
independently.
The appropriate treatment option in these deteriorated
patients is a matter of controversy. To contribute to this
debate, we analyzed data from 6 patients with paraplegia with
SDAVF treated in our institution. Clinical and radiological
data, patient outcomes, and our pathophysiological hypothesis are presented and discussed.
Patients and Methods
We reviewed all patients treated for SDAVFs in our institution
(through endovascular or surgical intervention) between December 1992 and December 2004. During this period, 42 patients
were treated (22 by endovascular procedure and 20 by surgery).
We analyzed 6 patients who were already paraplegic at the time
of the treatment. Clinical symptoms were evaluated with regard to
motor deficit (using the Aminoff scale,3 McCormick scale,4 modified
Received February 8, 2008; accepted March 11, 2008.
From the Departments of Neurosurgery (N.A., F.P., P.D., M.T.) and Interventional Neuroradiology (P.L.), Bicêtre University Hospital, Le
Kremlin-Bicetre, France.
Correspondence to Nozar Aghakhani, MD, Departments of Neurosurgery, Bicêtre University Hospital, 78 rue du Général Leclerc, 94275 Le
Kremlin-Bicetre, France. E-mail [email protected]
© 2008 American Heart Association, Inc.
Stroke is available at http://stroke.ahajournals.org
DOI: 10.1161/STROKEAHA.108.517037
2756
Aghakhani et al
Table 1.
Grade
I
II
III
IV
McCormick Classification
Definition
Neurologically normal; mild focal deficit not significantly
affecting function of involved limb; mild spasticity or
reflex abnormality; normal gait
Presence of sensorimotor deficit affecting function of
involved limb; mild to moderate gait difficulty, severe
pain or dysesthesia syndrome impairing patient’s
quality of life; still functions and ambulates
independently discomfort in professional activity
More severe neurological deficit; requires cane/brace
for ambulation or significant bilateral upper extremity
impairment; may or may not function independently
Severe deficit, requires wheelchair or cane/brace with
bilateral upper extremity impairment, usually
not independent
Downloaded from http://stroke.ahajournals.org/ by guest on June 17, 2017
Rankin Scale5, and ASIA classification6; Tables 1 and 2), sphincter
disturbances (Aminoff-Logue scale3), and pain.
The optimal treatment for each patient was selected after discussion between neurosurgical and neuroradiological staff. Fistula
occlusion was checked by postoperative angiography before discharge. Patients were evaluated at 6 weeks and 6 months after
treatment. They also underwent at least one MRI during the follow-up
period. In cases exhibiting persistence of intramedullary hyperintensity on T2-weighted MRI and vascular images posterior to the spinal
cord, another angiography was performed.
Results
Table 3 shows the clinical presentation, the localization of the
fistulae, and follow-up results in our patients.
The mean duration of symptoms before surgery was 39
months (range, 11 to 144 months). The mean duration of
paraplegia before surgery was 1.6 months (range, 24 hours to
3 months). At the time of treatment, all patients had paraplegia (Grade IV on the McCormick scale and Grade V on the
Aminoff scale, Grade 5 on modified Rankin Scale) with a
motor ASIA score between 0 and 10 for both legs. Five
patients had a gradual and progressive degradation. One patient
(No 1) had acute paraplegia after spinal angiography. Pain
typically presented as a radicular pain in the legs and was
present in 4 (66%) of our patients. Sphincter disturbance was
present in 5 cases.
T2-weighted sagittal MRI sequences showed in all
patients perimedullary flow voids on the dorsal aspect of
the cord and a diffuse intramedullary hyperintensity that
extended to the conus medullaris. The hyperintensity
extended up to the lower thoracic region in 2 cases, to the
cervical region in 2 cases, and were limited on the conus
region in 2 others.
Surgery was used in all cases. Endovascular treatment was
considered unsuitable because, in 3 cases, the fistula originated at the same level as the Adamkiewicz artery (Case Nos
1, 5, and 6), and in the remaining 3 cases, the feeding arteries
were tortuous or narrow. Surgery was performed under
general anesthesia in the prone position through a one-level
laminectomy. After a dural opening, the drainage vein was
microsurgically interrupted at the level of the shunt with
coagulation of the inner and outer layers of the dura. There
Spinal Dural Arteriovenous Fistulae
2757
Table 2. Aminoff-Logue Disability Scales for Gait
and Micturition
Gait
Leg weakness, no restriction in gait
1
Reduced tolerance to exercise
2
Need for a cane to walk
3
Need for 2 canes or crutches to walk
4
Inability to stand, patient in wheelchair or in bed
5
Micturition
Normal
0
Hesitancy, urgency, frequency, altered sensation,
but continent
1
Occasional urinary incontinence or retention
2
Total incontinence or persistent retention
3
were no surgical complications. After discharge, all patients
were transferred to a rehabilitation center for at least 2
months. Functional improvement started immediately during the postoperative period and continued over 3 to 6
months. Six months after the operation, all patients were
able to walk; 3 had a normal gait (Grade I on the McCormick
scale, Grade I on the Aminoff scale, Grade 1 on modified
Rankin Scale) and 3 needed a cane to walk (Grade II on the
McCormick, Grade III on Aminoff scale, Grade 2 of modified
Rankin Scale). In all cases, the motor ASIA scores for lower
limbs were improved and ranged between 40 and 45 (mean,
42.8). These results remained totally stable over the
follow-up period (mean, 3 years). There was no patient with
secondary clinical degradation in our experience.
Of 4 patients experiencing pain, 3 patients (75%) reported
that their pain was lessened after surgery and the fourth
reported it was unchanged. Only 2 of 5 patients (40%)
experiencing sphincter disturbance before surgery reported an
improvement.
The extension of the intramedullary T2-weighted hyperintensity on pretreatment MRI and its evolution on posttreatment MRI was not correlated with the outcome.
Considering all 36 other patients, long-term follow-up
showed that 78% of patients with pretreatment gait disturbance improved, 10% worsened, and 10% remained stable.
No patient becomes paraplegic after treatment.
Discussion
Although several studies have analyzed SDAVFs, none have
focused particularly on patients with paraplegia. Steinmetz,1
Cenzato,7 and Mourier8 reported on patients with Grades of
IV and V on the Aminoff scale. Among patients confined to
bed, Mourier et al reported that 60% were able to walk with
crutches, but only one could return to work. Among the 18
patients reported by Steinmetz, 4 were Grade V on the
Aminoff scale. After treatment, one patient reached Grade 0,
another reached Grade II, and 2 reached Grade III on the
Aminoff scale. In these 2 series, no information concerning
the duration of the paraplegia was available. Jellema et al9
reported in 2004 a series of 44 treated patients and mentioned
13 patients who were wheelchair-bound at the time of
2758
Stroke
October 2008
Table 3.
Clinical Characters, Radiological Findings, and Results of Our Series
Preoperative
Case
No.
Sex/Age,
years
Paraplegia
Duration
Aminoff
Scale
McCormick
Scale
MRS
ASIA
Score
Pain
Sphincter*
Fistulae
Localization
Adamkiewicz
Localization
1
F/61
24 hours
5
IV
5
0
⫹
2
TH12,L
TH12,L
2
M/70
3 months
5
IV
5
8
⫺
0
TH6,R
TH10,L
3
M/60
2 months
5
IV
5
10
⫹
3
C6,L
C6,R
4
M/75
1 months
5
IV
5
6
⫺
2
TH11,L
TH10,L
5
M/66
2 months
5
IV
5
8
⫹
2
L1,L
L1,L
6
F/58
2 months
5
IV
5
8
⫹
2
L2,L
L2,L
*Micturition classification after Aminoff.
F indicates female; M, male; ⫹, present; ⫺, absent; TH, thoracic; C, cervical; L, lumbar.
Downloaded from http://stroke.ahajournals.org/ by guest on June 17, 2017
treatment. All we know about the outcome of these patients is
that at the time of follow-up, this number (wheelchair-bound
patients) was 5, including 3 of the original patients. All Grade
V patients of the series published by Song10 remained in the
same grade after treatment. Afshar11 reported over a series of
19 patients, 6 who were Grade V. Three of these patients
remained in the same grade after treatment; however, 3
improved (2 went to Grade IV and one Grade III). Using the
qualitative Aminoff scale alone to classify these patients is a
debatable decision, because Grade V of this classification
system includes patients who are unable to stand and are
confined to a wheelchair or bed, although it is unclear
whether these patients are completely paraplegic. Atkinson
et al12 published a series of 94 dural arteriovenous fistulas
(spinal and cranial fistulas) and proposed a modified
Aminoff-Logue scale dividing the Grade V into 2 subgroups: Grade 5T (patients with ability to aid in transfer
with some movement of legs but confined to bed or
wheelchair and unable to stand) and Grade 5P (those who
are paraplegic with no ability to aid in transfer nor
functional lower extremity movement and who are also
confined to bed or a wheelchair). They reported 7 patients
with paraplegia (Grade 5P patients of their modified
Aminoff-Logue scale). One patient was lost for long-term
follow-up, 3 remained paraplegic (Grade 5T), and 2 could
ambulate with aids (Grade IV). In these cases, the duration
of paraplegia was not precise.
We used the ASIA score to precisely quantify the motor
deficit. All of our patients had a motor ASIA score of ⬍10.
They had no voluntary movement of legs and the duration
of their paraplegia before treatment is clearly noted.
Paraplegia in our patients aged from 24 hours to 3 months,
and we admit that recovery is more hazardous in longstanding paraplegia.
SDAVFs are an abnormal communication between a radicular artery and a vein within the dura matter near a nerve
root. This direct communication provokes venous hyperpressure at the level of the valveless spinal cord veins. Using
intraoperative pressure recording, Hassler et al13,14 clearly
demonstrated an increase in intrinsic venous pressure (the
venous pressure in dural arteriovenous fistula was approximately 70% of the systemic arterial pressure) and the fact that
this venous pressure increases concomitantly with blood
pressure. This leads to a reduction in the intramedullary arteriovenous pressure gradient and thus in blood stagnation at
the spinal cord level. A decrease in tissue perfusion and
progressive hypoxia of neural tissue may follow. This
provokes histological changes, including a thickening of
intramedullary and pial vessel walls with hyalinization and
often with thrombus within the vessels. There can also be
neuronal depopulation, gliosis, and lipid-laden macrophages. Necrosis of the white or gray matter may follow.15
All these modifications explain the progression of the
neurological deficit. Given the gradual and progressive
installation of these phenomena, it is possible that treatment of the venous hyperpressure could arrest the progression of symptoms. If there are no definitive histological
lesions, it is possible that all signs of disease would decline
once the fistula is treated.
The value of MRI changes as a predicting factor of
outcome remains controversial. Willinsky et al16 considered that there was some correlation between MRI and
clinical outcome but at the same time they pointed out that
MRI evaluation could not distinguish those who had
improved from those who stabilized. However, the majority of authors7,10,12 admit that no correlation is found
between clinical outcome and pre- or posttreatment MRI
changes. There is especially no correlation between the
extent of abnormal T2-weighted hyperintensity on pretreatment MRI and the clinical outcome.10 Our results
support this feature.
Conclusion
Our results demonstrate that endovascular or surgical
treatment is beneficial for completely paraplegic SDAVF
patients. All of our patients were able to walk independently within 6 months after surgery. Thus, in light of
these encouraging results, we believe that paraplegia due
to SDAVF is typically a reversible symptom, and therefore
treatment should be performed even in patients with
paraplegia.
Disclosures
None.
Aghakhani et al
Table 3.
Spinal Dural Arteriovenous Fistulae
2759
Continued
Postoperative
First
ASIA
First Aminoff
Scale
First McCormick
Scale
Last
ASIA
Last Aminoff
Scale
Last McCormick
Scale
MRS
Pain
3
5
IV
45
8
5
IV
45
1
I
1
Improved
1
3
II
2
40
3
II
2
䡠䡠䡠
Improved
0
10
5
IV
6
5
IV
40
1
I
1
5
IV
42
3
II
2
䡠䡠䡠
Unchanged
2
8
8
5
IV
45
1
I
1
Improved
2
References
Downloaded from http://stroke.ahajournals.org/ by guest on June 17, 2017
1. Steinmetz MP, Chow MM, Krishnaney AA, Andrews-Hinders D,
Benzel EC, Masaryk TJ, Mayberg MR, Rasmussen PA. Outcome after
the treatment of spinal dural arteriovenous fistulae: a contemporary
single-institution series and meta-analysis. Neurosurgery. 2004;55:
77– 87.
2. Jellema K, Canta LR, Tijssen CC, Van Rooij WJ, Koudstaal PJ, Van Gijn
J. Spinal dural arteriovenous fistulas: clinical features in 80 patients.
J Neurol Neurosurg Psychiatry. 2003;74:1438 –1440.
3. Aminoff MJ, Logue V. The prognosis of patients with spinal vascular
malformations. Brain. 1974;97:211–218.
4. McCormick PC, Torres R, Post KD, Stein BM. Intramedullary
ependymoma of the spinal cord. J Neurosurg. 1990;72:523–532.
5. Bonita R, Beaglehole R. Modification of Rankin Scale: recovery of motor
function after stroke. Stroke. 1988;19:1497–1500.
6. American Spinal Injury Association. International Standards for Neurological Classification of Spinal Cord Injury, revised 2002. Chicago:
American Spinal Injury Association; 2002.
7. Cenzato M, Versari P, Righi C, Simionato F, Casali C, Giovanelli M.
Spinal dural arteriovenous fistulae: analysis of outcome in relation to
pretreatment indicators. Neurosurgery. 2004;55:815– 822.
8. Mourier KL, Gelbert F, Rey A, Assouline E, George B, Reizine D,
Merland JJ, Cophignon J. Spinal dural arteriovenous malformations with
perimedullary drainage. Indications and results of surgery in 30 cases.
Acta Neurochir (Wien). 1989;100:136 –141.
Sphincter*
2
2
9. Jellema K, Tijssen CC, van Rooij WJ, Sluzewski M, Koudstaal PJ, Algra
A, van Gijn J. Spinal dural arteriovenous fistulas: long-term follow-up of
44 treated patients. Neurology. 2004;62:1839 –1841.
10. Song JK, Vinuela F, Gobin YP, Duckwiler GR, Murayama Y, Kureshi I,
Frazee JG, Martin NA. Surgical and endovascular treatment of spinal
dural arteriovenous fistulas: long-term disability assessment and prognostic factors. J Neurosurg. 2001;94(suppl):199 –204.
11. Afshar JK, Doppman JL, Oldfield EH. Surgical interruption of intradural
draining vein as curative treatment of spinal dural arteriovenous fistulas.
J Neurosurg. 1995;82:196 –200.
12. Atkinson JLD, Miller GM, Krauss WE, Marsh WR, Piepgras DG,
Atkinson PP, Brown RD, Lane JI. Clinical and radiological features of
dural arteriovenous fistula, a treatable cause of myelopathy. Mayo Clin
Proc. 2001;76:1120 –1130.
13. Hassler W, Thron A, Grote EH. Hemodynamics of spinal dural arteriovenous fistulas. An intraoperative study. J Neurosurg. 1989;70:
360 –370.
14. Hassler W, Thron A. Flow velocity and pressure measurements in spinal
dural arteriovenous fistulas. Neurosurg Rev. 1994;17:29 –36.
15. Hurst RW, Kenyon LC, Lavi E, Raps EC, Marcotte P. Spinal dural
arteriovenous fistula: the pathology of venous hypertensive myelopathy.
Neurology. 1995;45:1309 –1313.
16. Willinsky RA, terBrugge K, Montanera W, Mikulis D, Wallace MC.
Posttreatment MR findings in spinal dural arteriovenous malformations.
AJNR Am J Neuroradiol. 1995;16:2063–2071.
Curable Cause of Paraplegia: Spinal Dural Arteriovenous Fistulae
Nozar Aghakhani, Fabrice Parker, Philippe David, Pierre Lasjaunias and Marc Tadie
Downloaded from http://stroke.ahajournals.org/ by guest on June 17, 2017
Stroke. 2008;39:2756-2759; originally published online July 17, 2008;
doi: 10.1161/STROKEAHA.108.517037
Stroke is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231
Copyright © 2008 American Heart Association, Inc. All rights reserved.
Print ISSN: 0039-2499. Online ISSN: 1524-4628
The online version of this article, along with updated information and services, is located on the
World Wide Web at:
http://stroke.ahajournals.org/content/39/10/2756
Permissions: Requests for permissions to reproduce figures, tables, or portions of articles originally published
in Stroke can be obtained via RightsLink, a service of the Copyright Clearance Center, not the Editorial Office.
Once the online version of the published article for which permission is being requested is located, click
Request Permissions in the middle column of the Web page under Services. Further information about this
process is available in the Permissions and Rights Question and Answer document.
Reprints: Information about reprints can be found online at:
http://www.lww.com/reprints
Subscriptions: Information about subscribing to Stroke is online at:
http://stroke.ahajournals.org//subscriptions/