spinal dural arteriovenous fistulas: a congestive myelopathy that

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doi:10.1093/brain/awl220 Brain (2006), 129, 3150–3164 REVIEW ARTICLE Spinal dural arteriovenous fistulas: a congestive myelopathy that initially mimics a peripheral nerve disorder K. Jellema, 1 C. C. Tijssen 1 and J. van Gijn 2 1 Department of Neurology, St Elisabeth Hospital Tilburg, Tilburg and 2 Department of Neurology, University Medical Center Utrecht, Utrecht, The Netherlands Correspondence to: K. Jellema, St Elisabeth Hospital, PO Box 90151, 5000 LC Tilburg, The Netherlands E-mail: [email protected] Spinal dural arteriovenous fistula (SDAVF) is a rare and enigmatic disease entity. The clinical features and structural changes have been recognized since 1926, and the pathophysiology and the essentials of treatment since 1974, but up to the present day it is unknown why these fistulas develop. The fistula between a radicular artery and the corresponding radicular vein within the dural root sleeve leads to congestion of the venous outflow of the spinal cord and eventually ischaemia. Patients, who are mostly middle-aged men, develop a progressive myelopathy, which at the early stages of the disease often mimics a polyradiculopathy or anterior horn cell disorder. By the time involvement of upper motoneurons or sacral segments makes the diagnosis of SDAVF inescapable, patients suffer from considerable neurological deficits. The diagnosis relies on MRI, which shows swelling of the spinal cord, with a centrally located hyperintense signal on T 2 -weighted images, and with hypointense ‘flow void’ phenomena dorsal to the cord, representing enlarged and tortuous veins. Catheter angiography is required to determine the exact location of the fistula as well as the angio-architecture, on which the mode of treatment depends. If the arterial feeder of the fistula is a tributary of the anterior spinal artery, embolization is not possible. After embolization recanalization may occur, but this is rarely seen after filling of the draining vein with glue. Alternatively, operation is a safe and permanent mode of treatment. No prognostic factors have been reliably established. Muscle strength and gait disturbances respond better to treatment than pain and symptoms related to damage of sacral segments. In any middle aged male patient with ascending motor or sensory deficits in the legs, SDAVF should be considered in order to prevent irreversible handicap. Keywords: spinal dural arteriovenous fistulas; clinical features; treatment; review Abbreviations: AVMs = arteriovenous malformations; SDAVF = spinal dural arteriovenous fistula Received February 21, 2006. Revised July 4, 2006. Accepted July 18, 2006. Advance Access publication August 18, 2006. Introduction Up to the present day physicians continue to be perplexed by the extensive changes in structure and function caused by the development of an abnormal but often tiny connection between a radicular artery and a radicular vein, at some level along the spinal axis. First, it took several decades before the morphological changes in the spinal cord of patients who had died from the complications of progressive paraplegia were attributed not to an infectious or degenerative condition of spinal blood vessels but to venous congestion. Secondly, it is the caudal end of the spinal cord that is commonly first affected by congestive oedema and ultimately infarction, regardless of the level of the fistula, so that the initial clinical features often consist of sensory and motor symptoms ascending from the feet, suggesting a polyneuropathy or polyradiculopathy. Thirdly, treatment now largely consists of endovascular occlusion rather than surgical closure of the fistula, but the optimal techniques have not yet been found, since recurrences continue to occur. Finally, it is unclear which factors lead to the development of these fistulae and more specifically why they occur most often in middle- aged men. # The Author (2006). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For Permissions, please email: [email protected] Downloaded from https://academic.oup.com/brain/article-abstract/129/12/3150/266472 by guest on 18 March 2018

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Page 1: Spinal dural arteriovenous fistulas: a congestive myelopathy that

doi:10.1093/brain/awl220 Brain (2006), 129, 3150–3164

REV IEW ARTICLE

Spinal dural arteriovenous fistulas: a congestivemyelopathy that initially mimics a peripheralnerve disorder

K. Jellema,1 C. C. Tijssen1 and J. van Gijn2

1Department of Neurology, St Elisabeth Hospital Tilburg, Tilburg and 2Department of Neurology,University Medical Center Utrecht, Utrecht, The Netherlands

Correspondence to: K. Jellema, St Elisabeth Hospital, PO Box 90151, 5000 LC Tilburg, The NetherlandsE-mail: [email protected]

Spinal dural arteriovenous fistula (SDAVF) is a rare and enigmatic disease entity. The clinical features andstructural changes have been recognized since 1926, and the pathophysiology and the essentials of treatmentsince 1974, but up to the present day it is unknown why these fistulas develop. The fistula between a radicularartery and the corresponding radicular vein within the dural root sleeve leads to congestion of the venousoutflow of the spinal cord and eventually ischaemia. Patients, who are mostly middle-aged men, develop aprogressive myelopathy, which at the early stages of the disease often mimics a polyradiculopathy or anteriorhorn cell disorder. By the time involvement of upper motoneurons or sacral segments makes the diagnosis ofSDAVF inescapable, patients suffer from considerable neurological deficits. The diagnosis relies on MRI, whichshows swelling of the spinal cord, with a centrally located hyperintense signal on T2-weighted images, and withhypointense ‘flow void’ phenomena dorsal to the cord, representing enlarged and tortuous veins. Catheterangiography is required to determine the exact location of the fistula as well as the angio-architecture, on whichthe mode of treatment depends. If the arterial feeder of the fistula is a tributary of the anterior spinal artery,embolization is not possible. After embolization recanalization may occur, but this is rarely seen after filling ofthe draining vein with glue. Alternatively, operation is a safe and permanentmode of treatment. No prognosticfactors have been reliably established. Muscle strength and gait disturbances respond better to treatment thanpain and symptoms related to damage of sacral segments. In any middle aged male patient with ascendingmotor or sensory deficits in the legs, SDAVF should be considered in order to prevent irreversible handicap.

Keywords: spinal dural arteriovenous fistulas; clinical features; treatment; review

Abbreviations: AVMs = arteriovenous malformations; SDAVF = spinal dural arteriovenous fistula

Received February 21, 2006. Revised July 4, 2006. Accepted July 18, 2006. Advance Access publication August 18, 2006.

IntroductionUp to the present day physicians continue to be perplexed

by the extensive changes in structure and function caused

by the development of an abnormal but often tiny

connection between a radicular artery and a radicular vein,

at some level along the spinal axis. First, it took several

decades before the morphological changes in the spinal cord

of patients who had died from the complications of

progressive paraplegia were attributed not to an infectious

or degenerative condition of spinal blood vessels but to

venous congestion. Secondly, it is the caudal end of the

spinal cord that is commonly first affected by congestive

oedema and ultimately infarction, regardless of the level of

the fistula, so that the initial clinical features often consist

of sensory and motor symptoms ascending from the

feet, suggesting a polyneuropathy or polyradiculopathy.

Thirdly, treatment now largely consists of endovascular

occlusion rather than surgical closure of the fistula, but the

optimal techniques have not yet been found, since

recurrences continue to occur. Finally, it is unclear which

factors lead to the development of these fistulae and

more specifically why they occur most often in middle-

aged men.

# The Author (2006). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For Permissions, please email: [email protected]

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Page 2: Spinal dural arteriovenous fistulas: a congestive myelopathy that

Foix and Alajouanine’s description of theclinical and anatomical featuresIt is not exactly known who gave the first description of a

patient with what we now call spinal dural arteriovenous

fistula (SDAVF). Retrospective interpretations depend on

clinical features and sometimes on findings at autopsy, but

even then these represented only the consequences of the

disease and not its cause. Early reports of patients with

appropriate spinal vascular lesions may have been mis-

interpreted and perhaps remain to be detected. The first

detailed clinical and pathological report of what is most

likely to represent SDAVF is the detailed description by Foix

and Alajouanine (Foix and Alajouanine, 1926), who have, in

the course of time, become eponymously linked with the

condition until its cause was found.

In 1926, Foix and Alajouanine described first the clinical

and then the post-mortem findings in two young men with

an ascending myelopathy, who died 33 and 11 months after

the onset of an ascending paraparesis.

The first patient presented at age 29 with a 7-month

history of progressive ‘claudication intermittente de la moelle’,

which the patient first noted after climbing stairs. He had

problems with micturition but no sensory symptoms. On

examination he showed wasting of the thighs and buttocks,

weakness of foot dorsiflexion and knee flexion, with an

ankle clonus and brisk knee jerks but no Babinski signs.

Within 1 year and 6 months after disease onset he was

fully paraplegic. By that time sensory disturbances had also

developed, first with loss of pain and temperature sensation

in the buttocks and at the back of the legs, gradually

ascending to the level of the groins for all modalities of

skin sensation. He developed bedsores and constipation

and eventually died, 2 years and 9 months after the onset of

the disease.

The second patient was a 27- or 37-year-old male plumber

(there is some inconsistency about his age in the report) who

experienced weakness of the legs after a day’s work. Initially

the weakness resolved but after a few months the legs

became progressively weak. He had some difficulty voiding.

On examination there was paraparesis with marked

weakness of knee flexion; plantar reflexes and ankle jerks

were absent, with normal knee jerks; sensation was

unimpaired. The disease progressed and 8 months after

disease onset there was a complete and flaccid paraplegia,

with marked wasting (especially on the right), areflexia

(including abdominal and cremasteric reflexes), loss of

pain and temperature sensation below the umbilicus, with

touch first impaired only in the right foot and leg, and later

also in all regions below the umbilicus. By then he had

also urinary incontinence and constipation. He developed

bedsores and died 11 months after the onset of the disease.

Post-mortem examination was remarkably similar in

the two patients. The lower spinal cord showed extensive

necrosis, predominantly in the grey matter but also in the

white matter (Fig. 1). The abnormalities were most severe at

the sacral level and slightly less severe at the lumbar level,

Fig. 1 Lumbosacral spinal cord of Patient 1 (Weigert stain); ventral aspect at top of picture. Complete necrosis of the grey matter; no nervecells can be identified. Less severe changes in the white matter, predominantly in the lateral and dorsal columns; relative sparing of theventral and anterolateral columns. Dilatation and hypertrophy of intramedullary and extramedullary vessels may be noted. (Reproduction ofFig. 12 of the publication by Foix and Alajouanine in 1926.)

Spinal dural arteriovenous fistulas Brain (2006), 129, 3150–3164 3151

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and they gradually disappeared at the mid-thoracic level,

with the exception of secondary degeneration of long tracts

in the white matter. The anterior and, to a lesser degree,

posterior spinal roots were degenerated. Even more

conspicuous were the changes of blood vessels. The intrinsic

as well as the extramedullary vessels were thickened, through

hypertrophy of the intimal and muscular layers (‘endo-meso-

vascularite’), as well as widened and tortuous; the lumen had

increased rather than decreased (Fig. 2). The abnormal

blood vessels were found from the cauda equina up to the

upper thoracic cord, where the parenchymal changes were

only minimal. Therefore, the authors supposed that the

vascular alterations had preceded the necrotic changes.

They were in the dark about the cause of the disease but

hypothesized an infectious origin, primarily affecting the

spinal blood vessels or involving both vascular and neural

structures; also, they proposed future experiments in which

a spinal cord emulsion might be injected into an animal to

see whether the disease was transmissible.

Sub-acute necrotizing myelopathy probably exists in other

forms, without concomitant vascular abnormalities. There

have been reports of patients who suffered from a progressive

myelopathy, clinically resembling the cases described by

Foix and Alajouanine, but who did not have enlarged vessels

at autopsy (Hoffman, 1955; Katz and Ropper, 2000).

Subsequent historyThe observations from Foix and Alajouanine were confirmed

5 years later by Lhermitte et al. (1931). They described a

50-year-old man who presented with slowly progressive

right-sided leg weakness. When the disease progressed

further he was operated for a suspected spinal cord tumour.

At operation they found multiple, dilated vessels on the

dorsal surface of the spinal cord. As the expected spinal cord

tumour was not found, the operation was terminated. After

the operation the patient became paraplegic and ultimately

died of urinary tract infection. Post-mortem examination

again showed multiple, enlarged vessels and necrosis of the

grey and white matter of the spinal cord.

Probably the first successful operation on an SDAVF was

performed by Elsberg, as early as in 1916 (Elsberg, 1916).

He ligated and excised an enlarged and thickened vein at

the level of T8 in a patient with a sensory level at T9. The

patient made a full recovery. Elsberg also reported that in

120 laminectomies for other reasons he had found enlarged

veins on the dorsal surface of the spinal cord in six patients

(Elsberg, 1916).

In a 1943 monograph on vascular abnormalities and

tumours of the spinal cord the author lamented that ‘the

subject is clouded by a loose and confusing nomenclature’

(Wyburn-Mason, 1943). Indeed many names have been

proposed for the disorder, before and since. Apart from

Foix and Alajouanine’s ‘myelite necrotique subaigue’, SDAVF

has been called angiodysgenetic necrotizing myelopathy

(Scholz and Wechsler 1959; Jellinger et al., 1968), angioma

racemosum venosum (Krause, 1911), dorsal extramedullary

angioma, long dorsal AVM (Malis, 1982), type 1 arter-

iovenous fistula and venous angioma (Pia and Vogelsang,

1965). Wyburn-Mason was not far from the truth in his

Fig. 2 Dorsal aspect of spinal cord of Patient 2 (stain not recorded, probably haematoxylin–eosin). Typical ‘endo-mesovasculitis’with hypertrophic, ‘onion-bulb’ aspect. The adjacent parenchyma shows severe necrotic changes. (Reproduction of Fig. 28 of the publicationby Foix and Alajouanine in 1926.)

3152 Brain (2006), 129, 3150–3164 K. Jellema et al.

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Page 4: Spinal dural arteriovenous fistulas: a congestive myelopathy that

presumption that the cases described by Foix and

Alajouanine represented a complication of an angioma.

After the introduction of catheter angiography in the

1950s, knowledge about spinal AVMs and fistulas increased

at a fast pace. The first somewhat larger series (15 patients)

of angiographically demonstrated spinal vascular lesions

(through vertebral arteriography, via the subclavian route,

or aortography) was published in 1966 (Houdart et al.,

1966). The authors distinguished spinal vascular lesions on

the basis of the angioarchitecture of the malformation,

arterial supply and draining veins, location of draining veins

and width of the lesion. They did not provide sufficient

clinical data to allow an estimation of the number of spinal

fistulas in their series. In 1972, Djindjian was the first to

recognize that some arteriovenous malformations (AVMs)

consist of an arteriovenous shunt without an intervening

capillary plexus (Djindjian, 1972). The first embolization of

an AVM—a congenital condition, not a fistula—was

performed by Doppman et al. (1968) in a 16-year-old boy,

by means of six stainless steel metal pellets, 1.5 mm in

diameter.

The pathophysiology of ‘necrotizing myelopathy’ con-

tinued to be poorly understood until 1974, when Aminoff

and Logue at the National Hospital for Nervous Diseases

(as it was then called) hypothesized that the arteriovenous

shunt leads to increased intramedullary venous pressure,

with a reduced arteriovenous pressure gradient (Aminoff

et al., 1974). They described a 49-year-old patient who had

died after a 12-year history of progressive, bilateral leg

weakness. Post-mortem examination showed ischaemic

changes of the spinal cord without features of thrombotic

occlusion of vessels. In addition, there was extensive

concentric hyalinization of the intramedullary capillaries.

Given the absence of thrombotic occlusion they attributed

these changes to increased intramedullary pressure.

Although a landmark article, it was not the first to assume

venous hypertension as the pathophysiological factor behind

the thickened venous walls. Antoni wrote from Sweden in

1962: ‘In any event they (the thick walled and enlarged

vessels) indicate a pronounced, longstanding increase of

intravascular pressure, of a type which occurs primarily

between the arterial and venous systems’ (Antoni, 1962).

In 1976, Aminoff published a monograph on spinal

angiomas, with more details on the natural history,

presumed pathogenesis of venous congestion and the

surgical treatment, which then consisted in excision of the

draining veins (Aminoff, 1976).

Finally, in a beautifully illustrated article in 1977 Kendall

and Logue showed that the site of the fistula was not located

in the spinal cord but on or in the dural root sleeve (Kendall

and Logue, 1977).

ClassificationSeveral classification systems have been used in the past

for spinal vascular lesions (Wyburn-Mason, 1943; Pia and

Vogelsang, 1965; Rosenblum et al., 1987; Borden et al., 1995;

Spetzler et al., 2002). We prefer the classification system

described by Spetzler et al. (Table 1), because it encompasses

the cumulative knowledge thus far about the angioarchi-

tecture of the vascular lesions. Like every classification

system it has its drawbacks: the designation of cavernous

malformations as neoplastic is disputable, while the

classification system contains a new entity called conus

medullaris AVM that had not been described before

(Barrow, 2002).

According to the Spetzler classification, spinal vascular

lesions can be subdivided into neoplasms, aneurysms and

arteriovenous lesions (Table 1). Arteriovenous lesions are

further classified as arteriovenous fistulas and AVMs.

Arteriovenous fistulas can either be extradural or intradural.

Extradural arteriovenous fistulas have also been called

epidural fistulas and consist of a shunt between an

extradural artery and vein. This is a high-flow fistula,

which in turn is responsible for enlargement of the epidural

venous plexus, leading to external compression of the spinal

cord. Myelopathy may occasionally develop because of

vascular steal (Arnaud et al., 1994a; Goyal et al., 1999).

Intradural arteriovenous fistulas are the typical lesions

causing progressive myelopathy. They may be located

ventrally or dorsally. Ventral intradural arteriovenous

fistulas consist of a shunt between the anterior spinal artery

and an enlarged venous draining system (Djindjian et al.,

1977). They are subdivided into type A, B or C, depending

on the size. Ventral intradural lesions were formerly known

as type IV lesions (Heros et al., 1986; Barrow et al., 1994);

with dorsal intradural arteriovenous fistulas (SDAVF) the

abnormal connection is formed between an artery and vein

at the level of a dural root sleeve, with low flow, which is in

contrast to the high-flow ventral type of fistulas. The dorsal

fistulas can be subdivided into fistulas with a single feeding

artery (dorsal type A) and those with multiple feeding

arteries (dorsal type B) (Spetzler et al., 2002). In this article,

we will only deal with dorsal fistulas, further called SDAVF.

Table 1 Classification of spinal vascular lesions(Spetzler et al., 2002)

Neoplastic vascular lesionsHaemangioblastomaCavernous malformations

AneurysmsArteriovenous lesions

Arteriovenous malformationsArteriovenous fistulas

ExtraduralIntradural

VentralA: SmallB: MediumC: Large

DorsalA: Single arterial feederB: Multiple arterial feeders

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Page 5: Spinal dural arteriovenous fistulas: a congestive myelopathy that

Another classification system, less static because it is not

based on descriptive morphological features, is the system

that divides spinal cord vascular lesions into three main

groups (Berenstein et al., 2004). The first group consists of

single shunts that are caused by a genetic disorder, for

example arteriovenous lesions associated with hereditary

haemorrhagic telangiectasia (Rendu–Osler–Weber disease).

The second group includes multiple spinal cord vascular

lesions that are not genetically determined but share

metameric links (involvement with cord, bone, paraspinal,

subcutaneous and skin tissues). The third group consists

of single lesions, which are either AVMs or arteriovenous

fistulas.

EpidemiologySDAVFs are rare, but they still make up the most common

vascular anomaly of the spine, with a proportion of 60–80%

(Kendall and Logue, 1977; Merland et al., 1980; Oldfield

and Doppman, 1988). Absolute figures are not available, but

an estimation based on retrospective analysis of German

patients with a progressive myelopathy arrived at 5–10/

million/year in the general population (Thron, 2001). The

disease is probably underdiagnosed (Grandin et al., 1997).

We ourselves addressed the question whether undiagnosed

SDAVF occurred in patients who were admitted to a

specialized rehabilitation institute for patients with spinal

cord lesions. Of 614 patients who suffered from a spinal cord

lesion not due to trauma we found at least three patients

with either a SDAVF or a cerebral fistula with spinal

drainage (by extrapolation there might have been three more

if the films and records had not been destroyed in the mean

time) (Jellema et al., 2006). None of them had been

previously recognized as suffering from SDAVF. One patient

was diagnosed only after post-mortem examination (Fig. 3).

Patients affected by SDAVF are mostly middle-aged men.

Table 2 lists all reported series with more than 5 patients;

there were 968 men against 210 women (ratio almost 5 : 1).

The mean age at the time of diagnosis is 55–60 years

(see Table 2); patients under the age of 30 are rarely reported

(in total 14 patients under age 30 were found in the

1178 patients, or 1%) which is in contrast to the mean age of

30 in patients with an intramedullary AVM (Oldfield et al.,

1983; Symon et al., 1984; Rosenblum et al., 1987; Bedersen

and Spetzler, 1996; Niimi et al., 1997; Kataoka et al., 1999;

Sleiman et al., 1999; Lev et al., 2001; Van Dijk et al., 2002).

The youngest patients reported were 22 years at the time of

diagnosis (Rosenblum et al., 1987; Bedersen and Spetzler,

1996). The archetypal patients described by Foix and

Alajouanine were also rather young in comparison, being

29 and (probably) 37 years at the onset of the disease (Foix

and Alajouanine, 1926). In our series of 80 patients the

youngest patient developed symptoms of SDAVF under the

age of 30, but he was not diagnosed until the age of 34

(Jellema et al., 2003). No patient under the age of 20 has ever

been reported.

Most SDAVFs are located in the thoracolumbar region.

In the tabulated series with more than 5 patients we found

23 patients with cervical SDAVF (2% of total) and

47 patients with SDAVF in the sacral region (4% of total).

Together, cervical and sacral SDAVF constitute just under

6% (70 of 1178) of patients with SDAVF.

Multiple SDAVFs in a single patient are uncommon

(Table 2). In the 1178 patients listed in Table 2 they were

encountered six times (0.5%). Yet this is probably an

underestimation, because spinal angiography is mostly

A

B

Fig. 3 (A) Spinal cord of a patient with an SDAVF demonstrated atautopsy. The lower panel shows marked necrosis and enlargedvessels at the thoracolumbar spinal cord. The panel above shows anormal cord. (B) Gross macroscopic view of the same patient.

3154 Brain (2006), 129, 3150–3164 K. Jellema et al.

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terminated after a single fistula has been found. In our series

of 80 patients we found 3 patients with a double SDAVF

(4%). Two other series reported one patient (2%) and two

patients (4%) with a double SDAVF among almost

50 patients (Westphal and Koch 1999; Van Dijk et al., 2002).

Apart from the series with more than five patients listed in

Table 2, four case reports described five patients with a

double SDAVF (Barnwell et al., 1991; Pierot et al., 1993;

Chaloupka et al., 1995; Krings et al., 2004).

Causal factors and pathophysiologyThe onset in middle age suggests that SDAVF is an acquired

condition, in contrast to intradural ventral fistulas or AVMs,

which are assumed to be congenital abnormalities

(Rosenblum et al., 1987). There are several other differences

between SDAVF and AVMs. An SDAVF is never located

within the spinal parenchyma, in contrast to AVMs. Patients

with SDAVF very rarely present with spinal haemorrhage in

contrast to patients with AVMs. Associated vascular lesions

are seen in AVMs, not in SDAVF. Intradural AVMs occur

much more often in the cervical region than SDAVF

(Rosenblum et al., 1987).

In cerebral dural fistulas a strong association exists with

cerebral vein thrombosis (Tsai et al., 2004); also, an

association with factor V Leiden and protein C has been

demonstrated (Kraus et al., 1998; Kraus et al., 2000). This

Table 2 Gender, location and diagnostic delay in reported series of patients with SDAVF reporting more than five patients

Author (year) Men Women Mean age Range Cervical Sacral Delay (in months) Multiple SDAVF

Afshar et al. (1995) 17 2 56 29–70 0 1 22 0Arnaud et al. (1994) 7 1 66.5 51–80 0 0 14 0Atkinson et al. (2001) 75 19 63 31–81 1 7 23 0Bedersen and Spetzler (1996) 3 9 51 22–75 0 0 34 0Behrens and Thron (1999) 18 3 57 33–75 0 1 15.5 0Berenstein and Lasjaunias (1992) 26 5 56 35–87 n.d. 0Bowen et al. (1995) 6 2 60 45–71 0 0 n.d. 0Bradac et al. (1993) 13 0 41 30–71 0 2 17 0Cenzato et al. (2004) 29 8 57 24–70 1 0 22Coats and King (1991) 6 1 69 67–72 0 0 44 0Brunereau et al. (1996) 5 2 61 44–79 n.d. n.d. 26 0Criscuolo et al. (1989) 5 0 61 56–68 0 0 n.d. 0Djindjian (1976) 38 6 52 34–73 n.d. 0Eskandar et al. (2002) 22 4 65 39–79 5 3 21 0Gilbertson et al. (1995) 51 15 62 37–81 5 6 27 0Guillevin et al. (2005) 22 4 62 38–87 n.d. n.d. 25 0Huffmann et al. (1995) 19 2 58 38–78 1 2 14 0Jellema et al. (2003) 66 14 60 34–79 2 3 15 3Kataoka et al. (2001) 3 4 47 25–58 0 0 39 0Koch et al. (2003) 42 12 60 35–83 4 4 20 0Koenig et al. (1989) 18 2 54 34–71 0 1 34.5 0Lee et al. (1998) 7 2 61 40–73 0 0 38 0Lev et al. (2001) 8 1 60 46–75 0 0 16 0Li et al. (2005) 61 11 56 28–72 n.d. n.d. 16 0Linden and Berlit (1996) 7 4 60 32–81 0 1 28 0Logue (1979) 21 3 57.5 33–73 n.d. n.d. 22 0Lundqvist et al. (1990) 8 3 61 44–70 0 0 25.5 0Mascalchi et al. (1995) 6 0 64 43–75 0 0 n.d. 0Merland et al. (1980) 10 3 56 39–72 0 1 n.d. 0Morgan et al. (1989) 12 5 60 51–72 0 0 24 0Mourier et al. (1989) 27 3 60 34–77 0 1 12 0N’Diaye et al. (1984) 22 3 62 32–79 0 0 n.d. 0Nichols et al. (1992) 9 5 63 51–74 0 0 21 0Niimi et al. (1997) 42 7 60 26–82 0 9 n.d. 0Oldfield et al. (1983) 6 0 56 29–74 0 0 33 0Rosenblum et al. (1987) 23 4 49 22–72 0 1 32 0Schick and Hassler (2003) 16 2 60 32–84 n.d. n.d. n.d. 0Sleiman et al. (1999) 8 2 60 24–75 0 0 23 0Song et al. (2001) 27 5 65 46–83 n.d. n.d. 29 0Symon et al. (1984) 53 2 57 29–75 0 2 n.d. 0Tacconi et al. (1997) 21 4 63.1 42–78 0 0 33 0Ushikoshi et al. (1999) 9 4 57 38–73 2 0 23 0Van Dijk et al. (2002) 39 10 63 28–78 1 1 27.6 1Westphal and Koch (1999) 35 12 60 35–? 1 1 24 2

n.d. = no data.

Spinal dural arteriovenous fistulas Brain (2006), 129, 3150–3164 3155

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Page 7: Spinal dural arteriovenous fistulas: a congestive myelopathy that

association with thrombophilia has not been found in

patients with SDAVF (Jellema et al., 2004a).

Trauma does not seem to play a major role. First, in a

retrospective study trauma to the spine was reported in only

4% of patients (Jellema et al., 2003). Secondly, although the

cervical spine is the most mobile part of the spinal column,

cervical fistulas are rare. Another proposed factor is partial

thrombosis of an AVM (Brion et al., 1952), but no evidence

for this has been put forward since.

Since the introduction of selective angiography, much has

been learned about the pathophysiology. Aminoff and others

proposed in 1974 that venous hypertension and not vascular

steal, cord compression or haemorrhage was the main

pathophysiological factor (Aminoff et al., 1974). The shunt

is most often formed within the dorsal surface of the dural

root sleeve in the intervertebral foramen, where the radicular

vein pierces the dura, together with one or more dural

branches of the radicular artery. However, the shunt is

sometimes situated along the dura between two adjacent

nerve roots (Berenstein et al., 2004).

The increased pressure causes the venous system to

‘arterialize’, that is, the walls of intramedullary veins become

thickened and also tortuous. The radicular feeding artery is

often a dural branch and in a minority, the medullary artery.

The shunt results in venous hypertension in the spinal cord,

because the intramedullary veins and the radicular vein

share a common venous outflow. The reduced arteriovenous

pressure gradient results in a decrease in tissue perfusion

and venous infarction (Hurst et al., 1995). This has been

confirmed by direct intra-operative measurement of vascular

pressure of the fistula, which was as high as 74% of the

systemic arterial pressure (Hassler et al., 1989; Hassler and

Thron, 1994). An increase in arterial pressure during the

operation directly leads to an increase in venous pressure

(Hassler et al., 1989), which may explain why some patients

report that symptoms become worse after physical activity

(Aminoff and Logue, 1974a; Khurana et al., 2002). Apart

from the increased pressure caused by the shunt, the venous

outflow may be less efficient to start with than is the case

in healthy individuals (Merland et al., 1980; Thron, 2001).

The lower thoracic region has relatively fewer venous

outflow channels at a segmental level than the cervical or

lumbosacral region (Tadie et al., 1985). These differences in

segmental outflow probably contribute to the phenomenon

that venous congestion is transmitted in a caudo-cranial

direction throughout the spinal cord and that the first

symptoms of myelopathy tend to reflect dysfunction of the

lowest part of the cord, that is, the conus medullaris, even

though the shunt is at the thoracic level, or in some cases

even near the skull base (Vasdev et al., 1994; Asakawa et al.,

2002). Venous outflow through the medullary vein and

venous plexus is dorsal from the cord in 80–90%, and

combined ventral and dorsal in �10–20% (Anson and

Spetzler, 1993).

In a post-mortem study on thoracic radicular vasculature

we found physiological shunts between the radicular artery

and a corresponding vein in subjects without previous

symptoms of myelopathy (Fig. 4) (K. Jellema, R. L. A. W.

Bleys, C. C. Tijssen, P. J. Koudstaal and J. van Gijn; submitted

for publication). The role of these shunts is unknown, and they

have also been found in the lumbosacral spinal cord (Parke

and Watanabe, 1985). Possibly arteriovenous shunts are not

uncommon but they become symptomatic only through

congenital or environmental factors that lead to impairment of

venous outflow.

Clinical features at onsetThe clinical features of SDAVF can be distinguished in those

at the onset of the disease, in retrospect, and those present

at the time of diagnosis. Initial symptoms are often non-

specific. They include gait difficulties, symmetrical or

asymmetrical sensory symptoms such as paraesthesias in

one or both feet, diffuse or patchy sensory loss, but also

radicular pain (Table 3). Disturbances of micturition and

defaecation may occur at the start but most often they

develop in later phases of the disease (Rosenblum et al.,

1987; Lundqvist et al., 1990; Huffmann et al., 1995; Niimi

et al., 1997; Westphal and Koch, 1999; Jellema et al., 2003;

Koch et al., 2003). In the majority of patients (40–63%)

progression lasts for 1–3 years before the diagnosis is made,

but a protracted course with a duration of >3 years occurs in

10–34% (Logue, 1979; Symon et al., 1984; Koenig et al.,

1989; Arnaud et al., 1994b; Lee et al., 1998; Sleiman et al.,

1999; Van Dijk et al., 2002; Jellema et al., 2003). A gradually

progressive course with stepwise deterioration is recorded in

11–32% of patients (Symon et al., 1984; Gilbertson et al.,

1995; Jellema et al., 2003).

An acute onset is reported in 5–18% of patients (Jellema

et al., 2003). If symptoms develop within minutes to hours

Fig. 4 The T7 segment of a 78-year-old woman. There is a shuntbetween the radicular artery and the venous plexus covering theouter surface of the dura (arrow).

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they can mimic an anterior spinal artery syndrome (Jellema

et al., 2003). The sudden episodes mostly occur after

exercise, prolonged standing and even singing (Khurana

et al., 2002), and may disappear after rest. Acute worsening

of symptoms may also be related to changes in posture such

as bending over; even eating has been related with worsening

of symptoms (Aminoff and Logue, 1974a; Symon et al.,

1984; Rosenblum et al., 1987).

Unusual presentations include an acute myelopathy after

epidural anaesthesia (Sghirlanzoni et al., 1989) or develop-

ment of an SDAVF after lumbar disc excision at the level

of the left S1 root (Asakuno et al., 2002). A single case

report described a 46-year-old woman who presented with

intermittent episodes of weakness and sensory disturbances

at the beginning of her menstrual periods (Kim et al., 1991).

The explanation may be that uterine hyperaemia during the

menstrual cycle increased the venous return in an already

compromised pelvic venous system, which was indeed found

at pelvic surgery. The patient was successfully treated with

embolization of the fistula and removal of the uterus (Kim

et al., 1991).

In one patient an SDAVF was incidentally found 2 years

before symptoms developed. He was treated after he

eventually experienced progressive bilateral leg weakness

and dysuria (Houdart et al., 2001).

Intraspinal haemorrhage is distinctly rare, since it

occurred in none of the 1178 patients described in the

cumulative series with more than 5 patients (Table 2). A

unique case report describes the only patient on record with

an SDAVF at lumbar level (L4) who presented with spinal

subarachnoid haemorrhage (Koch et al., 2004). Patients may

present with acute headache as a result of intracranial

subarachnoid headache (SAH), mostly in patients with a

dural fistula at the craniocervical junction (Cahan et al.,

1987; Willinsky et al., 1990; Morimoto et al., 1992; Ikeda

et al., 1994; Kinouchi et al., 1998; Do et al., 1999; Hashimoto

et al., 2000; Kim et al., 2003). Acute headache secondary to

subarachnoid haemorrhage has been reported only twice in

patients with a lower cervical SDAVF (Willinsky et al., 1990;

Morimoto et al., 1992) and once in a patient with an SDAVF

at T12 (Vates et al., 2001).

Clinical features at the time of diagnosisAt the time of diagnosis there are often considerable

neurological deficits (Table 3). At that stage two-thirds of

patients show a combination of gait difficulties, sensory

disturbances and involvement of sacral segments (micturition,

defaecation or sexual dysfunction) (Jellema et al., 2003).

Almost all patients by that time suffer from gait difficulties

and weakness of one or both legs. Between 10–32% of

patients are wheelchair-bound (Aminoff and Logue, 1974a;

Rosenblum et al., 1987; Koenig et al., 1989; Mourier et al.,

1989; Huffmann et al., 1995; Ushikoshi et al., 1999; Atkinson

et al., 2001; Jellema et al., 2003; Koch et al., 2003).

Upper motoneuron involvement (relatively increased

tendon jerks or clonus, Babinski signs) and lower moto-

neuron involvement may be present at the same time, in

agreement with the original observations of Foix and

Alajouanine (Morgan and Marsh, 1989; Atkinson et al.,

2001; Jellema et al., 2003). In one study, 69% of patients had

both lower and upper motoneuron involvement (Atkinson

et al., 2001). Upper motoneuron involvement may even be

preceded by lower motoneuron involvement, other than in

the two patients of Foix and Alajouanine; in a study that

specifically addressed this question such a sequence was

found in 11 of 33 patients (Jellema et al., 2003).

Bowel and micturition problems frequently occur, mostly

later in the course of the disease (Table 3). Micturition

disturbances consist of urinary retention. Erectile dysfunc-

tion exists in �11–80% of men patients, and unwanted and

involuntary ejaculations may occur after exercise (Jellema

et al., 2003).

A spontaneous and complete disappearance of the fistula

has occasionally been described, though the clinical deficits

remained unchanged in these patients (Renowden and

Molyneux, 1993; Meder et al., 1995).

Clinical diagnosisSDAVF is notoriously hard to diagnose, because of the

misleading nature of the initial symptoms and the rarity of

the disease. The median time between onset and diagnosis

ranges between 12 and 44 months (Table 2). Since the first

symptoms often consist of paraesthesiae and lower motor

signs in the legs, this often suggests a neuromuscular

disorder. Erroneous diagnoses often made initially are

sensory polyneuropathy, acute or chronic inflammatory

demyelinating polyneuropathy, spinal muscular atrophy and

medullary tumour (Grandin et al., 1997; van der Meulen

et al., 1999; Atkinson et al., 2001; Jellema et al., 2003). Not

infrequently patients are unsuccessfully operated for a

lumbar disc prolapse (Jellema et al., 2003).

Although the clinical picture of a poly(radiculo)neuro-

pathy may resemble that of SDAVF, especially in the early

phase of the disease, there are some important differences.

First, involvement of the arms is rare in SDAVF, and occurs

only in cervical SDAVFs, whereas most polyneuropathies are

eventually associated with a stocking-and-glove-like sensory

Table 3 Proportion of patients with symptoms present atthe onset of the disease and symptoms present at thetime of diagnosis

Initialsymptoms (%)

Symptomsat diagnosis (%)

Sensory disturbances 17–72 63–100Gait difficulties and motordisturbances

50–81 78–100

Pain (either pain in theback or radicular pain)

13–64 17–86

Micturition difficulties 4–75 62–91Defaecation problems 0–38 30–100Sexual dysfunction 0–17 11–80

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loss. Secondly, though the sensory loss in SDAVF often

begins distally, over time it extends more and more

proximally, ultimately to the buttocks and the perineal

region. Sensory involvement of the sacral dermatomes is

exceptional in polyneuropathy. Thirdly, micturition pro-

blems are uncommon in polyneuropathies but occur

eventually in almost 80% of patients with SDAVF (Symon

et al., 1984; Rosenblum et al., 1987; Criscuolo et al., 1989;

Huffmann et al., 1995; Linden and Berlit, 1996; Song et al.,

2001; Van Dijk et al., 2002; Jellema et al., 2003). Mostly the

disturbance consists of urinary retention, resulting from

involvement of motor, sensory and autonomic neurons in

the conus medullaris. Fourthly, asymmetrical sensory or

motor deficits in the legs are a frequent feature in patients

with SDAVF at the start of the disease, whereas in

polyneuropathy symptoms are usually symmetrical. Fifthly

and lastly, when upper motoneuron signs supervene

(because the venous congestion in the spinal cord extends

above the level of the conus medullaris) this is definitive

proof that the lesion should not be localized in roots or

nerves (Jellema et al., 2003).

InvestigationsThe essential investigations to establish the diagnosis are

MRI and catheter angiography, which should be performed

when a progressive myelopathy is suspected. MRI findings

include hypo-intensities on T1-weighted images and hyper-

intensities on T2-weighted images (Fig. 5). Increased signal

intensity in the centre of the spinal cord and peripheral

sparing on T2-weighted images is found in 67–100% of

patients (Fig. 6) (Bowen et al., 1995; Gilbertson et al., 1995;

Jones et al., 1997; Hurst and Grossman, 2000; Luetmer et al.,

2005). Hyperintensities extend over an average level of 5–7

vertebrae, with conus involvement over 80%, and are

typically homogeneous (Gilbertson et al., 1995; Hurst and

Grossman, 2000).

In addition, abnormalities suggesting abnormal blood

vessels may be seen on either the ventral or the dorsal side of

the spinal cord. These ‘flow void phenomena’ representing

tortuous and dilated veins at the dorsal surface of the spinal

cord are found in 35–91% of patients (Fig. 5) (Gilbertson

et al., 1995; Hurst and Grossman, 2000). It seems that the

flow voids are found more often, as studies are more recent,

which may reflect advancement in MR techniques (Hurst

and Grossman, 2000). The central hyperintense lesions are

sometimes difficult to interpret, and may resemble anterior

spinal artery infarction, myelitis or spinal cord neoplasms

(Grandin et al., 1997), or, if slit-like, a persistent central

canal (Holly and Batzdorf, 2002). Gadolinium-enhanced

MRI scanning may reveal some contrast enhancement of

the spinal cord (Terwey et al., 1989). This is only minor

immediately after injection of contrast agent, but marked

enhancement occurs some 40–45 min after contrast injection

(Terwey et al., 1989).

MR angiography reveals flow in serpentine perimedullary

structures in up to 100% of patients (Bowen et al., 1995;

Mascalchi et al., 1995; Binkert et al., 1999; Mascalchi et al.,

2001; Saraf-Lavi et al., 2002). MR angiography may also give

an indication about the level of the SDAVF, which helps to

confine the extent and duration of catheter angiography;

the level of the fistula was correctly predicted in more than

A B

Fig. 5 MRI and angiography of SDAVF. (A) T2-weighted MRI image of a 66-year-old man with SDAVF. Multiple flow voids resemblingan enlarged medullary draining vein can be seen. (B) Angiogram of a 57-year-old man showing an SDAVF at T7 on the right.

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two-thirds of patients in several prospective series (Bowen

et al., 1995; Mascalchi et al., 1999; Luetmer et al., 2005).

Especially first-pass gadolinium-enhanced MR angiography

results in correct prediction of the site of the fistula in nine

patients with standard digital subtraction angiography used

as gold standard (Farb et al., 2002). On the other hand, false-

positive MR angiography is also possible in that normal

vessels may be interpreted as being pathologically enlarged

(Binkert et al., 1999; Luetmer et al., 2005).

Sometimes multidetector row computed tomography is

used in patients to find the site of the fistula (Bertrand et al.,

2004; Lai et al., 2005). There is little experience with this

technique in SDAVF, but it is evolving fast.

Before the introduction of MRI, diagnosis was often made

by means of myelography (N’Diaye et al., 1984; Gilbertson

et al., 1995). This investigation would show an irregular,

varicose dilation of the lumbar veins, giving the lumbar

roots sometimes a ‘postage stamp’ appearance (with serrated

edges) (N’Diaye et al., 1984). The enlarged vessels often

extended over an average of 8 vertebrae (range: 3–20)

(Gilbertson et al., 1995). Nowadays sometimes contrast-

enhanced MR myelography is used (Chen and Hsu, 2002).

In patients with a negative MRI scan (no swelling of the

cord and hyperintensities on the T2-weighted images, no

flow void phenomena ventral or dorsal to the surface of the

spinal cord) and no findings resembling SDAVF on MR

angiography, it is very unlikely that SDAVF is responsible for

the symptoms (Bowen et al., 1995; Gilbertson et al., 1995;

Saraf-Lavi et al., 2002). It seems justified to forgo catheter

angiography in these patients. If there is still strong

suspicion of an SDAVF, a myelogram can be performed

(Gilbertson et al., 1995). This may show the above-

mentioned features. A myelogram is also useful in patients

in whom an SDAVF is suspected but in whom angiography

is unsuccessful in detecting the fistula, for example because

the orifice of lumbar arteries is obstructed by atherosclerosis

(Oldfield et al., 2002).

Catheter angiography is still the gold standard in the

diagnosis of SDAVF (Fig. 5). Not only the intercostal and

lumbar arteries should be visualized as potential feeding

arteries of an abnormal shunt but also the median and

lateral sacral artery, the deep cervical and ascending cervical

arteries. If SDAVF is not found then intracranial vessels

should be visualized, including the ascending pharyngeal

artery, meningohypophyseal trunk, middle meningeal artery

and occipital artery. The angioarchitecture of the fistula

should be thoroughly investigated, especially with regard to

the question whether the arterial feeder is a dural branch or

a segmental medullary artery, which also contributes to the

anterior spinal artery (Clavier et al., 1986). In the latter case

endovascular treatment is not possible, because infarction of

the spinal cord is likely to occur. Furthermore, it is essential

to identify the artery of Adamkiewicz, because the fistula

may originate from this important tributary to the anterior

spinal artery (Aggarwal et al., 1992). In such patients, in

whom the fistula originates from a common segmental

artery, a radiopaque microcoil can be placed as a marker in

the major feeding artery, which can then easily be visualized

with conventional X-rays, allowing easy location of the

fistula during a subsequent operation (Britz et al., 2004).

Careful review of the angiographic images is essential. In a

report about three patients who were strongly suspected of

harbouring SDAVF on clinical and radiological grounds,

no fistula could be demonstrated with angiography. They

were nevertheless operated and the site of the fistula

was identified and divided. In retrospect, in each case, the

feeding vessel to the AVM had been visualized but not

detected (Alleyne et al., 1999).

Methods of treatmentThe choice of treatment is between endovascular embol-

ization and surgical ligation of the fistula. Obviously the

former option is the least invasive. Embolization with liquid

polymers [such as isobutyl 2-cyanoacrylate (IBCA), n-butyl

2-cyanoacrylate (NBCA)] is advocated over particles such as

polyvinyl alcohol (PVA), because the use of particles leads

to a recurrence rate as high as 30–93% (Nichols et al., 1992).

In contrast, occlusion is successful with liquid polymers

in 44–100% (Merland et al., 1986; Hall et al., 1989; Biondi

et al., 1990; Niimi et al., 1997; Westphal and Koch, 1999;

Van Dijk et al., 2002). The proportion of patients in

whom recanalization occurs differs between studies, if only

because of the different criteria that were used to define

successful embolization. In one study, filling of the draining

vein with glue was considered a successful embolization

Fig. 6 Increased signal intensity in the centre of the spinalcord with peripheral sparing on a T2-weighted MRI image of a60-year-old male with a left-sided SDAVF at T8.

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(Van Dijk et al., 2002). Other studies consider filling of the

fistula itself as a measure of successful embolization (Niimi

et al., 1997; Westphal and Koch, 1999).

Embolization of SDAVF is not possible in every patient.

First, if the arterial feeder of the fistula is a segmental

medullary artery, embolization entails a high risk of spinal

cord ischaemia. Secondly, technical difficulties such as

arterial wall dissection of the feeding vessels during the

embolization procedure may prohibit introduction of the

microcatheter close enough to the fistula.

If embolization is possible, then the success of treatment

depends on endovascular occlusion of the draining vein,

which means that recanalization will rarely occur when the

draining vein is filled with glue (Fig. 7) (Jellema et al., 2005).

The reason is probably that the fistula is often made up of

several small feeding arteries and a single draining vein, so

that occlusion of only (one of) the arterial feeder(s) to the

fistula will generally lead to development of new arterial

feeders (McCutcheon et al., 1996).

Surgical treatment before the pathophysiology of SDAVF

was clear consisted of a multi-level laminectomy with

stripping of the draining vein and decompression of the

spinal cord (Krayenbuhl et al., 1969). Because it is now

understood that with intradural fistulas the myelopathy is

not caused by compression by the tangle of dilated veins

on the dorsal surface of the cord, decompression is not

indicated. Presently an intradural interruption of the vein

draining the fistula is advocated (Huffmann et al., 1995).

This is as effective as total removal of the draining vein

(Afshar et al., 1995).

A recent meta-analysis of patients with SDAVF who

were treated with either embolization or operation showed

that almost 98% of surgical procedures were technically

successful; this stands in contrast to the 46% of patients

who were successfully treated with embolization (Steinmetz

et al., 2004).

Outcome after treatmentThe eventual outcome depends on several factors: duration

of symptoms, pre-treatment disability and success of the

procedure to close the fistula. Treatment is directed at

halting the progression of symptoms or even reversing them.

Aminoff and Logue (1974b) were the first to describe

the long-term follow-up of a group of patients. For this

purpose they introduced the Aminoff–Logue disability scale

(Table 4). A mean reduction of 1 grade on the Aminoff–

Logue motor scale can be expected in a large proportion of

patients (Song et al., 2001; Van Dijk et al., 2002; Cenzato

et al., 2004; Jellema et al., 2004b).

A comparison between operative treatment and emboliza-

tion in the long term is not possible, because of lack of

longitudinal data for endovascular treatment (Steinmetz et al.,

2004). In the review by these same authors improvement

after operation was found in 55% of patients and worsening

of symptoms in 11%. It seems plausible that patients with

complete closure of the fistula by embolization (which is

not always achieved; see previous section) show the same

proportion of improvement, stabilization or worsening of

symptoms as patients treated by operation. Recanalization

will lead to neurological deterioration and requires addi-

tional treatment, through either endovascular intervention or

operation. In some patients multiple endovascular inter-

ventions are needed to achieve permanent closure of the

fistula (Jellema et al., 2004b, 2005).

Symptoms that generally respond well to treatment are

gait difficulties and muscle strength, resulting in less

disability and dependence. In our own study of 44 patients

who had been treated, mostly by embolization, after an

Fig. 7 Intradural localization of the glue cast, indicating that thedraining vein is filled with glue.

Table 4 Aminoff–Logue disability scales for gait andmicturition (Aminoff and Logue, 1974b)

Gait0 Normal1 Leg weakness, abnormal gait or stance, but no restriction

of activity2 Restricted activity but not requiring support3 Requiring one stick for walking4 Requiring two sticks, crutches or walker5 Confined to wheelchair

Micturition0 Normal1 Hesitancy, urgency, frequency, altered sensation, but

continent2 Occasional urinary incontinence or retention3 Total incontinence or persistent retention

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average interval of almost 6 years, we found that walking

disturbances improved in 64% of patients, and muscle

strength in 56% (Jellema et al., 2004b). Others reported

improvement in gait in 50–100% of patients (Niimi et al.,

1997; Lee et al., 1998; Behrens and Thron, 1999; Ushikoshi

et al., 1999; Westphal and Koch, 1999; Atkinson et al., 2001;

Lev et al., 2001; Song et al., 2001; Cenzato et al., 2004;

Guillevin et al., 2005).

Micturition, pain and muscle spasms are symptoms that

often respond less well to treatment than gait disability

(Lundqvist et al., 1990; Song et al., 2001; Eskandar et al., 2002;

Jellema et al., 2004b; Guillevin et al., 2005), but one study

nevertheless reported marked improvement of micturition

and bowel function (Van Dijk et al., 2002).

No reliable prognostic factors have been identified. A

relatively short delay in diagnosis predicted better outcome

in one study (Niimi et al., 1997), but not in others (Eskandar

et al., 2002; Cenzato et al., 2004; Jellema et al., 2004b). One

might expect that pretreatment disability rather than the

length of the interval before diagnosis is a good measure of

the eventual outcome, but this was confirmed in only a few

studies (Eskandar et al., 2002; Cenzato et al., 2004), and not

in another (Jellema et al., 2004b).

The location of the fistula was a prognostic factor in one

study (Cenzato et al., 2004). In this Italian series patients

with a fistula located between T9 and T12 responded

better to treatment than those with a fistula elsewhere.

The authors explained this by the better vascularization

of the lower thoracic cord than that of the upper thoracic

cord.

Future studies on long-term follow-up should include a

complete neurological examination in a large group of

patients to determine prognostic factors. Outcome measures

should reflect disability and handicap rather than neuro-

logical deficits, should not be disease-specific but generic

and should be sufficiently established to be used for

comparing separate studies. The modified Rankin scale,

alternatively called the Oxford handicap scale, is a good

example (Bamford et al., 1989).

In conclusion, SDAVF is an intriguing and enigmatic

disease entity, which is only slowly relinquishing its secrets.

The pathophysiology is now well understood, much better

than the causes for the development of the fistulas. Because

the disease is rare, the knowledge about this disease is

progressing at a slow pace. Yet the knowledge about the

condition deserves to be wide. Every neurologist should

be aware of this potential curable disease and should be

able to diagnose this disease at an early stage, to prevent

the impending disaster of paraplegia. In The Netherlands,

there are �600 neurologists in a population of 16 million.

With an estimated incidence of 5–10/million/year (Thron,

2001), a neurologist will see about one patient with

SDAVF in 4–8 years. Despite the low frequency at which a

neurologist will encounter a patient with SDAVF, contin-

uous education is imperative to ensure a high degree of

awareness to diagnose this condition.

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