Spinal Dural Arteriovenous Fistulas

1
Spinal Dural Arteriovenous Fistulas

• Terence Sasaki, M.D.
• Tibor Becske, M.D.
• Peter Kim Nelson, M.D.

2
Spinal Dural Arteriovenous Fistulas

• Abstract
• The most common of the spinal vascular
  malformation, the spinal dural arteriovenous
  fistula (SdAVF), is a rarely thought about cause
  of back pain and myelopathy. This devastating
  entity is often overlooked and the result can be
  permanent paraplegia with loss of sphincter
  control. Perhaps the most important factor in
  diagnosis is inclusion in ones etiologic
  considerations. In this review, we depict the
  history, dissect the anatomy, explain the
  pathogenesis, and discuss the treatment options
  of SdAVFs.
• Keywords
• AVF, AVM, dural arteriovenous fistulas,
  neurointerventional, neuroendovascular, spinal
  arteriovenous fistulas, spinal arteriovenous
  malformations, review

3
Anatomy of this Presentation

• Review of Anatomy
• Classification of the types of Spinal vascular
  malformations
• SdAVFs
• Epidemiology -- Diagnosis
• Clinical Features -- Treatment
• Pathophysiology
• Conclusions

4
Basic Anatomy

• The circulation of the spinal cord consists of
  the intrinsic and extrinsic systems.
• The extrinsic or macrocirculation subsists of the
  radiculomedullary (ASA) and radiculopial (PSA)
  system fed by their respective medullary and pial
  branches of the radicular arteries.
• A potential watershed exists between the adjacent
  medullary arteries.

Drawing from WE Krauss Vascular anatomy of the
spinal cord In Nsurg Clin N Am 10(1)9-15, 1999
Jan
5
Arterial Macrocirculation

• The cervicothoracic region has the greatest
  variability in supply, the midthoracic has a
  single anterior medullary artery, and the
  thoracolumbar and sacral regions share the artery
  of Adamkiewicz (T9-L2).
• At the medullocranial junction, the dorsal cord
  is subserved by extradural vessels.
• Anterior spinal artery supplied by 7-8 anterior
  medullary arteries
• Posterior spinal arteries supplied by posterior
  medullary (radiculopial) arteries

Drawing from WE Krauss Vascular anatomy of the
spinal cord In Nsurg Clin N Am 10(1)9-15, 1999
Jan
6
Arterial Microcirculation

• The intrinsic or microcirculation consists of
  the central arteries off the ASA, the pial
  (coronal) plexi from the ASA PSA, and the
  radial branches which travel to deeper spinal
  cord structures.

Drawing from WE Krauss Vascular anatomy of the
spinal cord In Nsurg Clin N Am 10(1)9-15, 1999
Jan
7
Venous System

• The venous drainage is accomplished by several
  systems. The anteromedian group of intrinsic
  veins drain the anterior columns, the grey and
  white commissures, and the medial anterior horns.

Drawing from WE Krauss Vascular anatomy of the
spinal cord In Nsurg Clin N Am 10(1)9-15, 1999
Jan
8
More Veins...

• First traveling in the anterior sulcus as the
  central vein, it continues as the anteromedial
  spinal vein, then eventually as the anterior
  medullary vein entering the epidural plexus and
  terminating in the azygos/vena caval system.
• The rest of the cord is drained by the radial
  veins into the anterior and posterior coronal
  plexi which also contribute to the medullary
  veins.

Drawing from BE Kendall and V Logue Spinal
Epidural Malformations Draining into Intrathecal
Veins. Neurorad 13, 181-189 (1977)
9

• The medullary veins number two in the cervical,
  one each in the upper mid thoracic, two in the
  lower thoracic, and one at about the level of the
  third lumbar vertebral body.
• Batsons (perivertebral) plexus is located in the
  region of the neuroforamen and are a conglomerate
  of the epidural plexus, medullary veins, and
  vertebral veins.
• Rich anastomoses exist between the anterior and
  posterior plexi in the lower thoracic region.

Reference Kendall and Logue, Neurorad 13,
181-189 (1977)
10

• The cranial dural layers separate at the region
  of the foramen magnum to become the spinal dura
  and the periosteal dura of the spinal canal
  separated by the epidural space.
• Within the subarachnoid space a venous reticulum
  called the coronary plexus is normally separated
  from the epidural venous system, perhaps by
  valves.
• Thus the dural and nerve root arteries do not
  normally communicate with the medullary veins
  the dura and extradural tissues have separate
  drainage pathways from the cord.

11

• As elegantly described by Manelfe in 1972, the
  dura is supplied by the intraspinal division of
  each dorsospinal branch of the segmental artery
  at every level and from both sides.
• Both supplying and running alongside nerve
  sleeves, they split to longitudinal and
  transverse anastomoses both ventrally and
  dorsally.

JC Watson EH Oldfield The Surg Management of
Spinal Dural Vascular Malform. In Neurosurg Clin
N Am 10(1)73-88, Jan 1999
12
Classification

• Vascular malformations of the CNS have been
  classified by McCormick () and Russell
  Rubinstein () into four major pathologic types
  (a) AVM (b) cavernous angioma (c) capillary
  telangiectasia and (d) venous angioma.
• Aside from these congenital (developmental)
  lesions, a distinct entity is the dural AVM.
• The dural AVM (or fistula) represents an acquired
  vascular lesion, characterized by arteriovenous
  (AV) shunting involving vessels within the dural
  venous sinuses and coverings of the brain/spinal
  cord.
• Various classification systems and eponyms for
  these lesions have been used over the years with
  resultant confusion and difficulty in comparing
  and evaluating the various subgroups.

13
Timetable of Spinal vascular history
Hebold 1885, Gaupp 1888 ? 1st description of spinal vascular malformations (angiomas)
Elsberg, 1914 ? 1st successful surgery
Foix-Alajouanine, 1926 ? subacute (angiodysgenetic) necrotizing myelopathy
Perthes, 1927 ? identified spinal AVM on myelogram
Michon, 1928 ? described the syndrome of spinal SAH
Wyburn and Mason, 1943 ? clinical features described
Djindjian et al, 1962 ? selective spinal angiography
Doppman and Di Chiro, 1965 ? focus on nidus
Doppman et al, 1968 ? endovascular treatment (embolization)
Yasargil Krayenbuhl, 1969 ? microsurgical technique
Kendall and Logue, 1977 ? distinction of dural and intradural AVM
Anson and Spetzler, 1992 ? current classification
14
Types of Spinal Vascular Malformations

• Spinal dural arteriovenous fistula (SdAVF)
• Spinal extradural (epidural or paravertebral)
  AV fistula
• Spinal cord (or intramedullary) arteriovenous
  malformation (SCAVM)
• Spinal cord (perimedullary) arteriovenous
  fistula (SCAVF)
• Cavernous malformation (CM)

Modified after Anson and Spetzler 1992
Berenstein and Lasjaunias 1992.
15

• Anson and Spetzler Type I vascular malformations
  are SdAVFs. They account for 60-80 of spinal
  vascular malformations.
• Thought to be acquired lesions, spinal dural
  arteriovenous fistulas (SdAVF) are defined as
  small AVFs involving a dural branch of the
  radicular artery drained by a single radicular
  vein which then drains into the intradural
  perimedullary veins.

Drawing Rosenblum et al. J Nsurg 67195-802, 1987
16
SdAVFs

• Unlike spinal CORD vascular malformations, they
  are NOT supplied by the anterior and posterior
  spinal arteries (ASA PSA).
• Their shunts and draining veins are usually
  within the dura at the level of the nerve root
  foramen on the posterolateral aspect in the
  axilla of the exiting nerve root.

17
Perimedullary AV Fistula

• Type IV or intradural perimedullary AVFs, which
  account for 10-15 of cases, are supplied by the
  radiculomedullary or radiculopial arteries.
• These are further subdivided into three types
  depending on the size and number of feeders.
• The intradural location of the shunt, the
  constant involvement of spinal cord arteries, and
  the lack of intervening nidus are
  angioarchitectural features that differentiate
  them from both SdAVFs as well as intramedullary
  AVMs.

Text reference Anson and Spetzler 1992 Drawing
Rosenblum et al. J Nsurg 67195-802, 1987
18
Intramedullary AVM

• The rarest form, type II or intramedullary AVM,
  is found within the parenchyma or pia and
  believed to be congenital.
• They can be glomus or juvenile in nature.
• Type III stands for extensive AVM with vertebral
  or paraspinal involvement

Drawing Rosenblum et al. J Nsurg 67195-802, 1987
19
Comparison of SdAVF spinal cord arteriovenous
malformations (SCAVM)
Feature SDAVF SCAVM
Age gt4th decade 2nd-3rd decade
Symptom onset Slow progressive Acute
Male predominance Yes (marked) Minimal
Hemorrhage No Yes (frequent)
Bruit No 5-10
Origin Acquired Congenital
Site of nidus Dura, root sleeve Spinal cord
Medullary arterial involvement 10-20 100
Adapted from Muraszko and Oldfield
20
Epidemiology

• Spinal vascular malformations make up
  approximately 3 to 16 of spinal mass lesions.
• Of these at least 35 represent SdAVFs, although
  some estimates range as high as 80. SdAVF, the
  most common type of spinal AVM, affects patients
  late in adulthood typically during their middle
  ages with the mean age of onset of 55.
• Males are the predominant victims, 4-91, and
  typically the SdAVF lesion is located in the
  thoracolumbar region.

21
Clinical Features

• Patients initially present with back or sacral
  pain, leg numbness or weakness causing gait
  difficulty.
• Often patients initially notice weakness then
  sensory problems with these progressing to overt
  paraplegia in 2-4 years.
• The weakness can be from both upper as well as
  lower motor neuron dysfunction.

22

• Patients can be wrought with paresthesias and
  spasms which may culminate in wasting and
  fasciculations
• Both the sensory deficits and pain can result
  from cord and/or radicular involvement.
  Hyperesthesia may develop especially in the trunk
• The sensory level is seldom above T10. Patients
  often complain that symptoms worsen with exercise
  or illness

23

• When sphincter or sexual dysfunction occurs
  later, they rarely regress.
• This underlines the importance of an early
  diagnosis. Rarely these may precede the other
  symptoms.
• SdAVFs must be differentiated from MS, myopathy,
  cord compression whether intrinsic or extrinsic,
  motor neuron disease, infection (tropical spastic
  parapareis/HAM), or syringomyelia.

24

• The chronic progressive course, which
  characterizes the clinical course in 80, can be
  occasionally interrupted by acute exacerbations.
  
• Although episodic deterioration can occur, the
  step-wise progression of nidal hemorrhages seen
  with intramedullary lesions does not occur.
• The absence of hemorrhage seen in other spinal
  AVMs is thought to be attributable to the
  location (no pial supply) and slow flow nature of
  the shunt. The chronicity of cord vascular
  congestion is thought to be another factor.

25
Foix-Alajouanine Syndrome

• In 10-15, patients have an acute/subacute
  presentation of symptoms with rapid progression,
  sometimes termed the Foix-Alajouanine syndrome.
• This entity is characterized by a subacute
  necrotizing myelopathy of venous thrombosis and
  resultant infarction.

26
Pathophysiology

• Believed to be an acquired rete along dura, the
  SdAVF often begins at the axilla of a nerve root
  sleeve, dorsal to the nerve root.
• The feeder of the fistula is a dural branch of
  the radicular division of an intercostal or
  lumbar artery.
• Initially, it is a tiny, very slow flow shunt but
  with the buildup of pressure, flow reverses in
  the medullary veins in a centripetal fashion and
  thus the lesion drains intradurally.

27

• Due to the limited capacitance, the
  arteriolization of the radicular vein causes the
  perimedullary veins to engorge resulting in a
  distended and stagnant venous plexus.
• As hypertension develops in the venous system, it
  causes the intrinsic cord veins to become
  congested eventually slowing flow in the
  anterior spinal artery.

Note the enlarged venous structures surrounding
the cord.
28

• This venous stasis results in decreased perfusion
  and resultant hypoxia of neural tissue.
• Intramedullary vasodilation, coinciding with the
  loss of the autoregulatory reflexes, may also
  occur.
• This further contributes to the cord edema,
  stagnation of blood flow, and the disruption of
  the blood-CNS barrier.
• Cord edema results in upper motor neuron symptoms
  which progress to lower motor neuron symptoms
  once anterior horn cells are damaged by ischemia.

29

• Regardless of the site of fistula, edema starts
  at the most dependent area of the cord (conus).
• The result is a subacute ascending progression of
  symptoms including weakness.
• There may be a discrepancy between the observed
  spinal level and the fistula level.
• The cord edema commonly terminate at or below the
  level of the heart about T5. This is believed to
  be the result of venous return to the heart
  assisted by gravity above T5.
• Myelomalacia can occur with longstanding lesions.

30

• Mean arterial pressures can rise with exertion
  complicating cord perfusion further and resulting
  in claudication.
• In the past, this mechanism was thought to be due
  to a steal phenomenon.
• At times, local compression due to distended
  vasculature can result in nerve root or cord
  compression.
• SdAVFs almost never bleed because of the slow
  flow dynamics described above.
• Multiple lesions are uncommon.

31

• A SdAVF differs from a cranial dural AVF because
  it drains directly into a subarachnoid vein
  without an intervening dural sinus.
• Although cranial AVFs are thought to result from
  thrombosis triggering angiogenesis and subsequent
  shunting, this is likely not the mechanism which
  explains SdAVF pathogenesis. Preceding epidural
  lakes or varices are sometimes observed.

32
Diagnosis

• CSF A mild to moderate protein elevation (up to
  500) with little cell elevation is seen in CSF
  analysis.
• Myelogram
• MRI
• Angiogram

33
Myelogram

• Myelogram displays serpentine or totuous filling
  defects or bag of worms appearance.
• Because the posterior medullary veins are more
  abundant and the posterior longitudinal vein is
  generally larger, myelograms are more sensitive
  if performed in the supine position.

34
MRI Sagittal T2-weighted images

• The MR often displays an expansile conus which
  may have nonspecific enhancement and is often
  mistaken for tumor, inflammation, or
  demyelination.
• The profound superior extension of cord edema,
  which is visualized as T2 hyperintensity, as well
  as the multiple enhancing vessels, which produce
  a tortuous or studded appearance, are
  characteristic.
• Chronic disease can present with an atrophic cord.

35
Seen here is a swollen cord with high intensity
signal on T2-weighted images indicative of edema.
Also seen are multiple dilated vascular channels
adjacent to the cord.

• The dilated pial veins, often on the dorsal cord
  surface, may be seen best on T2-weighted images
  as areas of tortuous flow void adjacent to the
  high signal cerebrospinal fluid (CSF).

36
Angiography

• When spinal angiography is performed, the entire
  neural axis should be systematically searched.
• However, a scanning aortogram can often spot the
  feeder saving valuable time.
• Barring this, each of the segmental arteries
  should be selectively catheterized in turn.
• Bowel movement can be reduced with glucagon but
  should be used sparingly due to tachyphylaxis.
  Liberal use of apnea is suggested.
• Be sure to include the internal iliac and the
  sacral arteries (median lateral) to exclude
  pelvic contribution.
• The skull base branches of the vertebral and the
  carotid (internal external) arteries as well as
  the ascending cervical and the thyrocervical
  trunks also have been known to feed cephalad
  based SdAVFs.

37

• Late arterial phase image of Rt T6 intercostal
  artery injection reveals a dural AVF
• Note the tortuous and dilated perimedullary veins
  extending both cranially and caudally

38

• Late venous images reveal the craniocaudal extent
  of venous congestion

39

• Once the lesion has been located, it is important
  to identify the anterior and posterior spinal
  arteries.
• If either of these arteries are communicating
  with the lesion or from the same pedicle,
  embolization is contraindicated due to the risk
  of infarction.
• In 10 to 15 of cases, the SdAVF is fed by a
  radicular artery that also contributes the spinal
  cord supply via a radiculomedullary or
  radiculopial branch.

40
Stereoscopic views early to midarterial phase

• By taking images at 6 degrees angles, the two
  images can be visually combined by slightly
  crossing the eyes.

41
Stereoscopic views late arterial phase

• The resultant three dimensional image can help
  understand spatial relationships.

42
Treatment Endovascular

• Because of recanalization risks and inadvertent
  migration, both coils and particles are not
  recommended for SdAVF embolization.
• Relapse often occurs in 2-8 months.
• In an attempt to isolate the draining vein and
  the perimedullary veins, typically the fistula
  and the distal 1-2 cm of the adjacent vein are
  filled with acrylate liquid glue.
• Histoacryl (0.5 mL), otherwise known as
  N-butyl-2-cyanoacrylate (NBCA), and Lipiodol
  (1.2mL), an iodized oil to delay polymerizing
  time, are combined with a radioopaque substance
  such as tantalum powder.

43
Pre-treatment angiographic evaluation

• Early arterial phase

• Late arterial phase

• Venous phase

44
Embolization with NBCA

• Post Embolization

• Microcatheterization

• Pre Embolization

45

• Endovascular treatment is technically not
  feasible in up to 40 of cases
• Reasons include
• -ASA/PSA contribution from the same pedicle
• -failure of microcatheterization (tortuous
  anatomy dissection of arterial pedicle)
• -failure of glue penetration across fistula .
• If embolization has failed or cannot take place,
  a platinum coil can sometimes be used to
  fluoroscopically mark the feeding artery to
  facilitate subsequent surgery.
• This risks worsening the hemodynamics of the
  lesion however if surgery is not performed soon.
  

46
Outcome

• Clinical stabilization or improvement occurs in
  60-87 of endovascular cases with a complication
  rate ranging from 1.6-5.5.
• The extent of recovery is dependent on the
  nature, severity and duration of symptoms before
  treatment.
• Recurrence of symptoms may affect up to 40 of
  patients.
• In these, collateralization of the incompletely
  embolized fistula or, rarely, true recanalization
  (?) can be the etiology.
• Alternatively a new fistula or progressive venous
  thrombosis can account for the recurrence of
  symptoms. If this is the suspected cause,
  systemic anticoagulation should be initiated.

47
Treatment Surgical

• Goal complete and permanent occlusion of the
  fistula.
• This is accomplished by coagulating and dividing
  the intradural draining vein.
• Exposure of the nerve root followed by
  coagulation and resection of the dura containing
  the fistula can also be performed. This may be
  necessary with fistulas that have epidural
  drainage in addition to the intradural one.

Drawing from Watson JC, Oldfield EH The surg
management of spinal dural vascular malform
Nsurg Clin N Am 101, January 1999
48

• The surgical procedure is not technically
  challenging provided the surgeon understands the
  pathophysiology and has a good quality angiogram
  to refer to during the case.
• Stripping of the dilated and tortuous venous
  stuctures is contraindicated (this used to be
  routine practice).

Microsurgical photograph Note the tortuous veins
on the dorsal surface of the dural sac.
49
Outcome

• An improvement is seen in 70-95 with
  complications happening 0-16 of the cases.
• The extent of recovery is dependent on the
  nature, severity and duration of symptoms before
  treatment.
• Surgical mortality is close to 0.

50
Follow-up

• Postoperative or postembolization MRI (3-6 mos
  post procedure) to confirm resolution of cord
  edema and disappearance of dilated vascular
  channels.
• If symptoms recur, MRI followed by spinal
  angiography is indicated to assess for
  recanalization, venous thrombosis or de novo
  fistula formation.

51
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