Arteriovenous malformations of the filum terminale: clinical characteristics, angioarchitecture, and management of a rare spinal vascular pathology

View More View Less
  • 1 Department of Diagnostic and Interventional Neuroradiology,
  • | 2 Department of Neurology, and
  • | 3 Department of Neurosurgery, RWTH Aachen University Hospital, Aachen;
  • | 4 Department of Neurosurgery, Klinikum Ibbenbüren; and
  • | 5 Department of Neurosurgery, Justus-Liebig-University, Giessen, Germany
Free access

OBJECTIVE

The goal of this study was to describe clinical and neuroradiological features of arteriovenous malformations of the filum terminale (FT AVMs) and to present the authors’ diagnostic and therapeutic management in this rare disease.

METHODS

The presented cases were retrieved from a retrospectively collected database of all spinal vascular malformations treated between June 1992 and December 2021 at the Rheinisch-Westfälische Technische Hochschule (RWTH) University Hospital Aachen. Pretreatment and follow-up clinical and neuroradiological data were analyzed for this study.

RESULTS

Data in 15 patients with FT AVM with a mean age of 60 years were included, with an overall incidence of FT AVM of 19% among all spinal AVMs in our cohort. Twelve of 15 (80%) patients were men. Nonspecific but typical clinical and MR findings of thoracolumbar congestive myelopathy were found in all patients. Spinal MR angiography, performed in 10 patients, identified in all cases the arterialized FT vein as well as a lumbar/lumbosacral location of an AV shunt. Digital subtraction angiography (DSA) showed an arterial supply solely via the FT artery in 12/15 (80%) patients and via an additional feeder from the lumbosacral region in the other 3/15 (20%) patients. All patients were treated surgically. During 1-year follow-up, 2 patients presented with recurrent FT AVM due to further arterial supply from the lumbosacral region, and were treated surgically. Neurological status was improved in all patients within the 1-year follow-up, with marginal further changes during long-term follow-up.

CONCLUSIONS

Congestive myelopathy is the major pathological mechanism of symptoms in these patients, with no evidence for intradural bleeding. Missing the presence of possible multiple arterial supply of FT AVM during DSA may result in misdiagnosis and/or insufficient treatment. Due to the frequently prolonged course of FT artery, resection of the FT AVM may be a favorable treatment modality in comparison with endovascular treatment. Follow-up examinations are obligatory within the first 3 years after treatment, and further MR angiography and DSA examinations are indicated if congestive myelopathy persists.

ABBREVIATIONS

ALS = Aminoff-Logue scale; ASA = anterior spinal artery; AV = arteriovenous; AVM = arteriovenous malformation; CE-MRA = contrast-enhanced MR angiography; DSA = digital subtraction angiography; FT = filum terminale; FTA = filum terminale artery; FTV = filum terminale vein; ICG = indocyanine green; RWTH = Rheinisch-Westfälische Technische Hochschule; SDAVF = spinal dural arteriovenous fistula; SEAVF = spinal epidural arteriovenous fistula; TWIST = time-resolved angiography with stochastic trajectories.

OBJECTIVE

The goal of this study was to describe clinical and neuroradiological features of arteriovenous malformations of the filum terminale (FT AVMs) and to present the authors’ diagnostic and therapeutic management in this rare disease.

METHODS

The presented cases were retrieved from a retrospectively collected database of all spinal vascular malformations treated between June 1992 and December 2021 at the Rheinisch-Westfälische Technische Hochschule (RWTH) University Hospital Aachen. Pretreatment and follow-up clinical and neuroradiological data were analyzed for this study.

RESULTS

Data in 15 patients with FT AVM with a mean age of 60 years were included, with an overall incidence of FT AVM of 19% among all spinal AVMs in our cohort. Twelve of 15 (80%) patients were men. Nonspecific but typical clinical and MR findings of thoracolumbar congestive myelopathy were found in all patients. Spinal MR angiography, performed in 10 patients, identified in all cases the arterialized FT vein as well as a lumbar/lumbosacral location of an AV shunt. Digital subtraction angiography (DSA) showed an arterial supply solely via the FT artery in 12/15 (80%) patients and via an additional feeder from the lumbosacral region in the other 3/15 (20%) patients. All patients were treated surgically. During 1-year follow-up, 2 patients presented with recurrent FT AVM due to further arterial supply from the lumbosacral region, and were treated surgically. Neurological status was improved in all patients within the 1-year follow-up, with marginal further changes during long-term follow-up.

CONCLUSIONS

Congestive myelopathy is the major pathological mechanism of symptoms in these patients, with no evidence for intradural bleeding. Missing the presence of possible multiple arterial supply of FT AVM during DSA may result in misdiagnosis and/or insufficient treatment. Due to the frequently prolonged course of FT artery, resection of the FT AVM may be a favorable treatment modality in comparison with endovascular treatment. Follow-up examinations are obligatory within the first 3 years after treatment, and further MR angiography and DSA examinations are indicated if congestive myelopathy persists.

Arteriovenous (AV) shunts of the filum terminale (FT) are one of the rarest vascular spinal pathologies, with still incomplete descriptions of their clinical and radiological features in the literature.1 Recent available data are characterized by heterogeneous terminology and little information on the natural history.

As a tertiary referral center for spinal vascular malformations, we classify AV shunts at the FT as a subgroup of intradural arteriovenous malformations (FT AVMs). The term FT AVM comprises, in our own local diagnostic workup, all AV shunts at the FT with an arterial supply via the filum terminale artery (FTA) with or without further arterial supply from the lumbosacral region, and a venous drainage via the filum terminale vein (FTV). FT AVM should be strictly distinguished from spinal dural arteriovenous fistula (SDAVF) and spinal epidural arteriovenous fistula (SEAVF) in the deep lumbosacral region, as well as the less frequent radicular AV shunts in the lumbar region.

We demonstrate in this study the clinical and neuroradiological characteristics of these malformations in 15 patients and present our experience in diagnosing and treating this rare disease.

Methods

The present cases were retrieved from a retrospectively collected database of all spinal vascular malformations treated between June 1992 and December 2021 at Rheinisch-Westfälische Technische Hochschule (RWTH) University Hospital Aachen. Pretreatment and follow-up data were evaluated for demographics, duration of symptoms, neurological status, and neuroradiological findings at time of diagnosis and at last follow-up. This study was approved by the ethics committee of the RWTH University Hospital Aachen.

We used the Aminoff-Logue scale (ALS) of gait and micturition to assess the neurological status in our cohort based on patient records and a telephone survey.2,3 According to the modified ALS, gait disturbances are graded as follows: 0, normal; 1, leg weakness, abnormal walk or stance, but no restriction of activity; 2, restricted exercise tolerance; 3, requiring 1 stick for walking; 4, requiring 2 sticks, crutches, or walker; or 5, confined to wheelchair. Disturbances of micturition are graded as follows: 0, normal; 1, hesitancy, frequency, or urgency; 2, occasional urinary incontinence or retention; or 3, total urinary incontinence.

All patients with a suspicion of spinal vascular disease seen in our institution, including the present cases, undergo a standardized diagnostic workup algorithm comprising 1) review of all CT, MR, and digital subtraction angiography (DSA) images performed elsewhere before admission to our center; 2) spinal MR angiography (MRA) before DSA—by locally developed contrast-enhanced MRA (CE-MRA) sequences until 2015, and recently via additional time-resolved CE-MRA sequences (time-resolved angiography with stochastic trajectories [TWIST]);4 and 3) a focused spinal DSA guided by MRA findings. Since 2015 additional cone-beam CT angiography (DynaCT) studies were performed routinely during the spinal DSA.

All patients with a spinal vascular malformation receive a routine postoperative MR examination before discharge. Additional early postoperative MRA and/or DSA examinations are performed according to the surgeon’s preference to verify the occlusion of the AV shunt. We usually plan clinical and MR follow-up examinations at 3 months, at 6 months, and then annually in the first 3 years after treatment. Long-term follow-up MRA/DSA studies are indicated in cases with suspected residual or recurrent AV shunt.

All patients in this series were treated surgically via laminectomy, durotomy, and interruption of the shunt zone. Intraoperative Doppler sonography was routinely used until 2012 to verify the arterialization of the FTV. Intraoperative indocyanine green (ICG) videography was used in all patients with FT AVM treated after 2012 in our institution.

Preoperative MR images were evaluated for the evidence of an AV shunt, the appearance of the FTV, and the availability of differentiation between FTV and FTA in the lumbosacral region. The precise location of the AV shunt, the supplying arteries, and the origin and diameter of the anterior spinal artery (ASA) on DSA images, were also reviewed for this analysis. The diameter of the ASA at the level of the conus medullaris was measured and dichotomized as follows: no dilation: < 1 mm; dilation: = 1–2 mm; and severe dilation: > 2 mm.

Furthermore, we performed a literature review in PubMed on December 20, 2021, using the following terms: “filum terminale AND arteriovenous fistula,” or “filum terminale AND arteriovenous malformation."

Results

We found records of 15 patients with FT AVM in our database. Baseline characteristics of all patients are listed in Table 1. In summary, the mean age in this cohort was 60 ± 13 years (median 61 years; range 40–78 years), with male predominance (80%). The mean duration of symptoms was 23 ± 20 months (median 19 months; range 1–70 months) when excluding one statistical outlier in this series with a symptom duration of 120 months (Table 1).

TABLE 1.

Clinical findings in 15 patients with FT AVMs, assessed by the ALS

Case No.Age (yrs)/SexDuration of Sxs (mos)Sxs & ALS Score at Time of DxTxSxs at Discharge; ALS ScoreOutcome at 1-Yr FU; ALS ScoreLong-Term FU Period (yrs)Outcome at Long-Term FU; ALS Score
144/M8Proximal paraparesis 4/5, ataxia, hypesthesia S1 bilat, UD; G2, M2SurgeryImprovement of ataxia & hypesthesia, complete regression of UD; G1, M1Improvement of gait, UD, & hypesthesia; G1, M027Deterioration of gait, ED w/ genital hypesthesia; G4, M0
244/M4Pain L5 bilat, ataxia, UD, proximal paraparesis 3/5; G4, M3SurgeryImprovement: no pain, improvement of ataxia & UD; G3, M1Residual AV shunt & surgical Tx 6 mos after initial op; G3, M123Improvement of gait; G1, M1
354/M24Distal paraparesis 4/5, ataxia, diffuse hypesthesia of both legs, UD; G2, M3SurgeryImprovement of hypesthesia; G2, M3Improvement of hypesthesia & UD; G2, M021Improvement of gait; G1, M0
457/M20Paraparesis 3/5, diffuse hypesthesia of both legs, UD; G4, M3SurgeryImprovement of gait; G3, M3Improvement of gait; G2, M3NDND
545/M30Pain; G0, M0SurgeryImprovement (no pain); G0, M0No Sxs; G0, M013No Sxs; G0, M0
669/M18Paraparesis, ataxia, hypesthesia; G5, M0SurgeryUnchanged; G5, M0Recurrent AV shunt & 2nd op; G4, M210Improvement of gait & UD; G2, M1
761/M4Pain; G0, M0SurgeryImprovement (no pain); G0, M0No Sxs; G0, M013No Sxs; G0, M0
878/M24Paraparesis 3/5, ataxia, UD; G4, M3SurgeryImprovement of paraparesis; G3, M3NDNDND
977/M1Paraparesis 4/5, diffuse hypesthesia of both legs; G5, M0SurgeryUnchanged; G5, M0NDNDND
1040/M64Paraparesis 4/5, ataxia, UD; G1, M1SurgeryUnchanged; G1, M1Unchanged; G1, M14Deterioration of gait & UD; G2, M3
1172/M70Proximal paraparesis 4/5, ataxia, genital hypesthesia; G2, M0SurgeryDeterioration: postop UD; G2, M2NDNDND
1268/F13Paraparesis, UD; G4, M3SurgeryUnchanged; G4, M3Unchanged; G4, M31ND
1371/F18Proximal paresis of lt leg 4/5; G2, M0SurgeryUnchanged; G2, M0Improvement of gait; G1, M02Unchanged; G1, M0
1451/M120Distal paraparesis 3/5, ataxia; G2, M0SurgeryUnchanged; G2, M0Improvement of gait; G1, M01ND
1562/F24Ataxia, hypesthesia of lt leg, UD; G1, M1SurgeryImprovement of UD; G1, M0Improvement; G0, M02Unchanged

Dx = diagnosis; ED = erectile dysfunction; FU = follow-up; G = gait; M = micturition; ND = no data; Sxs = symptoms; Tx = treatment; UD = urinary dysfunction. Basic characteristics and neurological status at time of diagnosis in our center, at time of discharge after treatment, and at 1-year as well as long-term follow-up, assessed by ALS.

Gait disabilities due to paresis, paraparesis, and/or spinal ataxia were the most frequent neurological finding at time of diagnosis and were documented in 13/15 (87%) patients. Urinary dysfunction was reported in 8/15 (53%). Sensory disturbances in the lower extremities were found in 7/15 (47%) patients. Pain in the lower extremities without sensorimotor deficits was reported in 2/15 (13%) patients.

Neuroradiological findings are provided in Table 2. MR images showed extensive medullary edema, intramedullary contrast enhancement, and perimedullary flow voids evident for elongated perimedullary veins to various extents in all patients (Figs. 1 and 2).

TABLE 2.

Neuroradiological features in 15 patients with FT AVMs

Case No.CE-MRADSA
Suspected Fistula LocationID of Elongated FTVDifferentiation of FTV vs ASAFistula LocationArterial Supply of AV ShuntOrigin of Great Radiculomedullary ArteryDiam of ASA
1NANANAL5/S1FTAT6 lt (ant)1–2 mm
2NANANAL4/5FTA + intradural branches of segmental artery L4 rtT8 rt (ant)1–2 mm
3NANANAL4/5FTAT10 lt (ant)>2 mm
4NANANAS4/5FTA + internal iliac artery ltL1 rt (ant)1–2 mm
5LumbarYesNoL3/4FTAT12 lt (ant)1–2 mm
6LumbarYesNoS1/2FTA + iliolumbar artery ltL1 rt (pst)<1 mm
7Deep lumbosacralYesNoL5FTAT11 lt (ant)1–2 mm
8LumbarYesNoL4FTAL1 lt (ant)<1 mm
9Deep lumbosacralYesNoS2FTAL3 lt (ant)<1 mm
10LumbarYesNoS1/2FTAL2 lt (ant)<1 mm
11NANANAL4FTAT10 rt (ant)1–2 mm
12LumbarYesYes (TWIST MRA)S1/2FTAL2 rt (ant)<1 mm
13LumbarYesYes (TWIST MRA)L4FTAL3 lt, T9 lt (ant)1–2 mm
14LumbarYesNo (TWIST MRA)L3/4FTAT6 lt (ant)<1 mm
15Deep lumbosacralYesYes (TWIST MRA)S1/2FTAT8 lt (ant)1–2 mm

Ant = anterior; diam = diameter; ID = identification; NA = not applicable; pst = posterior.

FIG. 1.
FIG. 1.

A and B: Sagittal T2- and CE T1-weighted MR images reveal thoracolumbar contrast-enhancing congestive myelopathy (arrow) associated with a dilated vein from the lumbosacral to the thoracolumbar region (arrowheads) suggesting an AV shunt in the deep lumbosacral region (circles). C: CE-MRA image (arterial phase) shows the early filling of the arterialized FTV beginning at the S2 level and running upward to the perimedullary venous plexus in the thoracolumbar region (arrowheads). D–F: DSA in lateral and posteroanterior projections identifies the AV shunt at the S1/2 level (curved arrow), supplied via the FTA (arrowheads). Note the normal caliber of the Adamkiewicz artery originating from the left L2 radicular artery.

FIG. 2.
FIG. 2.

Case 15. MR workup. A and B: Sagittal T2- and CE T1-weighted images show congestive thoracic myelopathy. C–E: Spinal CE-MRA (sagittal and coronal multiplanar reconstruction) reveals an abnormally arterialized vein in the deep lumbosacral region (arrowheads) associated with thoracic arterialized perimedullary veins, suggesting a sacral location of the AV shunt. The ascending filling of the dilated FTV supports the assumption of a sacral AV shunt (curved arrows). F: Note the prominent T8 intercostal artery (Adamkiewicz artery) which supplies the FTA descending to the AV shunt (circle). G–I: Sagittal and coronal reconstructions of CE T1- and T2-weighted images demonstrate the arterialized and elongated FTV at the S2 level and its caudocranial course (arrowheads).

Spinal CE-MRA was performed before treatment in 11 patients. CE-MRA identified the arterialized FTV in all cases, as well as a lumbar/lumbosacral location of an AV shunt. Additional TWIST MRA studies were performed in the most recent 4 patients, and provided in 3 of these 4 cases a sufficient differentiation between the FTA and the arterialized FTV in the lumbar region (Fig. 2).

DSA examinations identified an exclusive arterial supply via FTA in 12/15 (80%) cases. In 3/15 (20%) other cases, the arterial supply occurred via the FTA as well as the right L4 radicular artery (case 2) and branches of the left internal iliac artery (cases 4 and 6). The venous drainage in all cases occurs via the FTV (Fig. 3). No caudal or lateral venous drainage toward the epidural venous plexus was observed in the current cohort. The diameter of the ASA was dilated in 9/15 (60%) patients and it was normal in the remaining 6/15 (40%).

FIG. 3.
FIG. 3.

Case 15. DSA workup. A–C: DSA (posteroanterior projection) studies identify the ASA (arrows), supplied via a radiculomedullary branch of the left T8 intercostal segmental artery (Adamkiewicz artery), as well as a paralleling course of the FTA and dilated FTV. The AV shunt is located at the S1/2 level (curved arrows). D–F: Axial, sagittal, and coronal multiplanar reconstructions of DynaCT (2 mm, 8-second rotation) precisely identify the location of the AV shunt at the S1/2 level (arrowheads).

After surgical treatment, early postoperative MR images showed a regression of medullary edema in all patients. Early postoperative DSA examinations were performed in 8/15 (53%) patients and confirmed the occlusion of the AV shunt in all cases.

Neurological status at time of discharge was available for 15 patients. Gait disabilities improved in 4/13 (31%) cases and were unchanged in the remaining 9/13 (69%). A regression of sensory disturbances was reported in 3/7 (43%) and was unchanged in 4/7 (57%) patients. Urinary dysfunction improved in 3/8 (38%) and was unchanged in 4/8 (50%) patients. Deterioration of urinary dysfunction was reported in 1/8 (13%) patients in the early postoperative course, without evidence for residual AV shunt or other perioperative complication.

Data on long-term outcome were available for 12 patients within the 1-year follow-up after treatment as well as for 9 patients after a mean follow-up period of 10 years (median 9 years; range 1–27 years) (Table 1). Within the 1st year after treatment, gait was improved in 6/10 (60%) and unchanged in 4/10 (40%) patients who presented with initial gait disabilities. Of the 8 patients who initially presented with urinary dysfunction, this was improved in 2/8 (25%) and unchanged in 3/8 (38%) patients. Additionally, the patient in case 6, who presented with no micturition disturbances at the time of diagnosis, developed urinary dysfunction with no evidence of a residual or recurrent FT AVM on the subsequent DSA images obtained at 1-year follow-up (i.e., 7 patients overall had urinary dysfunction at their 1-year follow-up).

Cases 2 and 6 presented with persisting and/or progressive symptoms and myelopathic signs on MR images. In both cases DSA revealed a recurrent/residual AV shunt. In case 2 further arterial supply of the initially occluded AV shunt via branches of the right L4 radicular artery could be visualized. In case 6 a residual AV shunt was found, with further arterial supply via branches of the left iliolumbar artery. Both patients underwent a second surgical exploration and occlusion of the remaining AV shunt with no further treatment-related complications. Postoperative DSA confirmed the definite occlusion of the FT AVM in both cases.

In the long-term outcome analysis, gait was improved in 3/7 (43%) and unchanged in 2/7 (29%) patients. Late deterioration with no evidence of a residual/recurrent FT AVM was documented in 2/7 (29%) cases and interpreted as chronic progressive myelopathy. Urinary dysfunction was improved in 1/7 (14%) and unchanged in 4/7 (57%) patients. Deterioration of urinary function was reported in the remaining 3/7 (43%) patients (including the patient in case 6, who developed new urinary dysfunction).

Our literature review revealed overall 71 cases with FT AVM reported in 34 studies (Table 3). In summary, the mean age of all these patients was 57 ± 13 years (median 58 years; range 24–84 years), and 49/71 (69%) patients were male. Data about treatment modality were available for 69 patients. Surgical treatment was performed in 50/69 (72%) patients. Another 13/69 (19%) patients received endovascular treatment, and the remaining 6/69 (9%) patients underwent endovascular and surgical treatment. A multiple arterial supply was reported in 13/71 (18%) patients.

TABLE 3.

Literature review of all cases of FT AVMs reported up to December 2021

Authors & YearPt Age (yrs)SexArterial Feeder (location fed by AA)Fistula LocationTx
Djindjian et al., 1977137MASAL2ND
40FASA + LSAL3
Gueguen et al., 19871540FASA (T8)L3S
24FASA (T9)L2S
Meisel et al., 19951630MASAL2S
Tender et al., 20051770MASA (T11)L4S
58MASA (T9)L2S
Mitha et al., 20061842MNDS1S
Jin et al., 20101961MLSAL5/S1E + S
Witiw et al., 20112062MASA (T8)S2/3S
Lim et al., 20112160MASA (L1)L4S
48MASA (T10) L4/5S
53FASA (L1)L4/5E
63FASA (L4) + LSAL3/4E
Trinh et al., 20112257MASA (T10)S1/2S
63MASAL4/5S
Saito et al., 20112368MASA (T9) + LSAL1S
Kumar et al., 20112444MASA (T9)L4/5S
Haddad et al., 20122560MASA (T11)S1S
Takami et al., 20122666FASA (L1)L2S
63MASA (T11)L2/3S
Fischer et al., 20132769MASA (T9)L4E
Macht et al., 20122857MLSAS3/4E
Chanthanaphak et al., 20132970FASA (T12)L5E
55MASA (T10)L4E
63MASA (T11)L5S
39FASA (T11)L2/3E
31MASA (T10)L2/3E
67MASA (T9)L3E
72MASA (L1)L5E
57FASA (L4)S2S
66MASA (T9)L2S
62MASA (T8)S2/3S
Takeuchi et al., 20143071MASA (T9)L4S
Krishnan et al., 20133154MASA (T12)L4S
Sharma et al., 20143248MASA (T9)L5S
Wajima et al., 20173378MASA (T8/9) + LSAS1E
Sharma et al., 20163442MASA (L3)L3S
Ding et al., 20163543MASA (L1)L3S
Hong et al., 20173611 pts, mean age 52.93F, 8M8 w/ ASA, 3 w/ extraarterial supplyL2–S29 S 2 E + S
Li et al., 20173765MASA (L2)L5S
Hong et al., 20183845MASA (T10)L4S
31MASA (T9)L2/4S
Lamsam et al., 20183950MASAL1S
Takai et al., 20194073MASA (T10)NDS
63FASA (T9 + L1)S
76MASA (T10)S
84MASA (L2)S
83MLSAS
54MLSAS
40ML3 + MSAS
Scullen et al., 20194162MASA (T9)L4S
Gao et al., 20194262MASA (T8)L4S + E
53MLSA + MSAL4E + S
Lee et al., 20191053MASA (T10)L3S
Lakhdar et al., 20194343MASAL5S
Iampreechakul et al., 20204443MASA (T10)L3/4S
Iampreechakul et al., 20204558MASA (L2) + LSAL4/5S
70MASA (T9) + LSAL4/5E
52FLSA bothS2/3E + S
Namba et al., 202046NDNDASA (L1)NDE

AA = artery of Adamkiewicz; E = endovascular; LSA = lateral sacral artery; MSA = middle sacral artery; pt = patient; S = surgery.

Discussion

The incidence rate of FT AVM among all spinal AVMs treated in our center accounts for up to 19%, which is relatively high compared to other estimations reported by Djindjian et al. (4%) and Rodesch et al. (3.2%).1,5 Our review identified 71 cases reported in the literature, from the first description of FT AVM by Djindjian et al. in 1977,1 up to July 2021. Since the majority of other reported FT AVMs were published in single or small case reports, we found no further estimates of the incidence rate of FT AVM in the retrospective database (Table 3).

We have observed, however, an increasing recognition of FT AVM in the last 10 years, with an increased number of reported cases; 62/71 (87%) FT AVMs were reported after 2010. This may reflect a growing awareness among neuroradiologists of the benefit of identifying spinal vascular diseases, and emphasizes on the other hand the impact of more modern diagnostic tools. This may also explain the increased incidence rate of FT AVM in our center after establishing spinal MRA in 2005 and DynaCT in 2015 as standard diagnostic tools for spinal vascular diseases. Nevertheless, the complex and comparatively unfamiliar vascular anatomy of the spinal cord still presents a major challenge when dealing with spinal vascular pathologies.6

Key Clinical Features

In our (at the time of this writing) largest single-center series reported in the literature, we could identify various key clinical features that may distinguish an FT AVM from other more frequent spinal AV shunts.

Neuroradiological Findings

Because of similar pathophysiology, MR findings in FT AVM are also comparable to those found in patients with SDAVF/SEAVF: a dilatation of perimedullary veins as well as medullary enhancement and edema are often found to various extents in patients with FT AVM.

The major specific MR finding among patients with FT AVM was a dilatation and elongation of the FTV, with a parallel course to the FTA identified in all patients with CE-MR.

In earlier times it was not possible to differentiate the FTA from the FTV via MRA. The MRA images at that time could differentiate an early arterial phase from a later predominantly venous phase. This technique was a cornerstone in identifying the location of SDAVF and was described earlier by our group. Nevertheless, due to the proximity of these vessels and the prominent FTV in FT AVM, this technique could not provide a sufficient differentiation between the FTA and the draining FTV in these patients. Further development of spinal CE-MRA (TWIST technique) facilitates a better time resolution and now allows us to detect the blood flow direction in the earlier arterial phase. In 3 of 4 cases who received time-resolved CE-MRA in our center, the FTA could be sufficiently differentiated from the dilated FTV. Moreover, this technique enabled a precise opacification of the ASA supplying the lumbar and thoracic radiculomedullary artery in 3 cases.

However, spinal DSA remains obligatory for a precise diagnosis in all spinal vascular pathologies.4 Whenever FT AVM is suspected, all potential supplying arteries of the thoracolumbar and lumbosacral region should be examined.

We note that in the angiographic workup it is always necessary to follow the ASA down to the conus and the FTA down to the lumbosacral region so as not to overlook a distant AV shunt into the FTV. It is a remarkable finding that in 40% of our cases the ASA showed a normal caliber despite the AV shunt.

Another important DSA finding in our current study was the multiple arterial supply of FT AVM that has been found in 3/15 (20%) cases in our cohort and in 13/71 (18%) of all other FT AVMs reported previously in the literature. In addition to the FTA, the arterial supply in these cases occurred from the lumbosacral region via branches of the internal iliac artery, lateral sacral arteries, and middle sacral artery.

Incomplete identification of this multiple arterial supply may raise the risk of treatment failure and can be avoided by routinely completing the DSA examinations of all supplying arteries of the lumbosacral region in these cases.

The venous drainage occurred in all current FT AVM cases via the proximal part of the FTV. Interestingly, although the venous blood flow within the FTV occurs physiologically in both rostral and caudal directions, no caudal or lateral venous drainage to the epidural venous plexus from the AV shunt has been found in our series, or reported in the literature previously.1 In pathological cranial and spinal AV shunts, progressive alterations of the venous wall such as hyalinization, wall hypertrophy, and microthrombosis due to pathological arterialization have been well described in various histopathological studies.13 In the case of FT AVM it is conceivable that the venous drainage in an earlier and still asymptomatic phase of the disease may occur in both rostral and caudal directions. In the course of the time, gravitational force may additionally induce a venous stasis, thrombosis, and occlusion of the distal part of the draining FTV below the AV shunt. This all could reinforce the venous drainage solely rostrally into the perimedullary venous plexus at the conus medullaris and accelerate the congestive myelopathy and its symptoms. Angiomorphological studies of such asymptomatic FT AVM cases may be of great interest regarding underlying hemodynamics and pathophysiology of FT AVM. Unfortunately, no asymptomatic patients with FT AVM have been found in our series or reported in the past.

Nevertheless, the etiology of FT AVM is still unclear. Some authors suggest an acquired natural history for FT AVM in association with degenerative lumbar stenosis or intraspinal lipomatous diseases.14 In contrast, our histopathological studies imply a congenital etiology for FT AVM, with similar findings to hamartoma. The findings in all available tissues from this series are the subject of an ongoing analysis.

Treatment Strategy and Long-Term Outcome

Surgical interruption of the AV shunt is the preferred treatment modality for these lesions in our institution, with an occlusion rate of up to 87%. Endovascular embolization was avoided in all cases due to the distant location of the FT AVM from the origin of the supplying FTA, which is associated with a high risk of perforation, thrombosis, or vasospasm of the ASA as well as the FTA. This is also in line with most reported cases in the literature. Of those, 72% were treated surgically, with a high success rate up to 100%. We note that both cases with a recurrent/residual AV shunt were diagnosed and treated in the 1990s, and no complications have been documented in our present series in the last 2 decades—which in part could be explained by our own learning curve in diagnosing and treating these rare malformations.

Beside pretreatment modern diagnostic tools, the use of intraoperative ICG was very helpful in these lesions and could markedly facilitate the identification of the AV shunt and visualize the exact angiomorphology of the shunt zone intraoperatively (Fig. 4). Moreover, it provided in all cases a real-time confirmation of a sufficient occlusion of the FT AVM.

FIG. 4.
FIG. 4.

Case 15. Intraoperative findings. Intraoperative (A) and ICG angiography (B) images demonstrate the parallel course of the FTA (arrows) and the arterialized and elongated FTV (arrowheads) as well as the AVM at the S1/2 level (*).

Intraoperative monitoring of somatosensory and motor evoked potentials presents a further intraoperative tool to avoid possible iatrogenic injuries of adjacent nerve roots or spinal cord tissue.

Our long-term outcome analysis showed a regression/stabilization of symptoms in the majority of cases. We observed an association between improvement of symptoms and regression of MR signs of congestive myelopathy, with a clear reduction of edema and perimedullary flow voids over time. Based on our experience, a persistence of congestive myelopathy in MR follow-up images associated with persisting or progressive symptoms should raise the suspicion of a possible residual or recurrent AV shunt and should trigger further spinal MRA and DSA examinations.

Limitations

The retrospective design of our study leads to some serious limitations such as incomplete and/or imprecise data as well as speculative interpretations for some clinical findings. However, given that the data of patients with spinal vascular diseases have been separately archived in our center over the last decades, we could decrease those limitations to some extent in our current analysis. Also, long-term follow-up data may comprise imprecise findings about the functional outcome of patients, which could be also affected by further comorbidities and/or could be under- or overestimated during reevaluation for this study. We aimed, therefore, in our long-term outcome analysis to evaluate and present the tendency of the clinical course in these patients without specific statistical evaluation. Nevertheless, due to the overall very low incidence of FT AVM, our series of 15 patients could summarize typical clinical and neuroradiological findings and diagnostic and therapeutic challenges of this rare disease. Our study may serve as a cornerstone for physicians dealing with spinal vascular pathologies and encourage them to report on their experience in these pathologies.

Conclusions

FT AVMs are an uncommon entity among all other spinal vascular pathologies, with various clinically and neuroradiologically specific features. Neurological disturbances such as chronic progressive paraparesis, ataxia, hypesthesia in the lower extremities, and urinary dysfunction are frequent findings in these patients. FT AVMs are usually fed by the FTA and, less frequently, via an additional arterial feeder from the lumbosacral region. A dilation and elongation of both FTA and FTV with a parallel course in spinal MRA images is a key feature in FT AVM, which should evoke the necessity of an extensive DSA examination of the lower thoracic and lumbosacral region. Surgical treatment of these lesions is recommended due to the distant location of the AV shunt from the origin of the supplying artery, which is associated with an increased risk from the endovascular approach.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Mull, Jablawi. Acquisition of data: Mull, Jablawi. Analysis and interpretation of data: Jablawi. Drafting the article: Jablawi. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Statistical analysis: Jablawi. Administrative/technical/material support: Dafotakis, Schubert, Hans, Jablawi. Study supervision: Mull.

References

  • 1

    Djindjian M, Djindjian R, Rey A, Hurth M, Houdart R. Intradural extramedullary spinal arterio-venous malformations fed by the anterior spinal artery. Surg Neurol. 1977;8(2):8593.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Aminoff MJ, Logue V. Clinical features of spinal vascular malformations. Brain. 1974;97(1):197210.

  • 3

    Aminoff MJ, Logue V. The prognosis of patients with spinal vascular malformations. Brain. 1974;97(1):211218.

  • 4

    Mull M, Nijenhuis RJ, Backes WH, Krings T, Wilmink JT, Thron A. Value and limitations of contrast-enhanced MR angiography in spinal arteriovenous malformations and dural arteriovenous fistulas. AJNR Am J Neuroradiol. 2007;28(7):12491258.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Rodesch G, Hurth M, Alvarez H, Tadié M, Lasjaunias P. Classification of spinal cord arteriovenous shunts: proposal for a reappraisal--the Bicêtre experience with 155 consecutive patients treated between 1981 and 1999. Neurosurgery. 2002;51(2):374380.

    • Search Google Scholar
    • Export Citation
  • 6

    Giordan E, Brinjikji W, Ciceri E, Lanzino G. Arteriovenous fistulae of the filum terminale. J Neurointerv Surg. 2018;10(2):191197.

  • 7

    Rodesch G, Lasjaunias P. Spinal cord arteriovenous shunts: from imaging to management. Eur J Radiol. 2003;46(3):221232.

  • 8

    Mull M, Othman A, Dafotakis M, Hans FJ, Schubert GA, Jablawi F. Spinal epidural arteriovenous fistula with perimedullary venous reflux: clinical and neuroradiologic features of an underestimated vascular disorder. AJNR Am J Neuroradiol. 2018;39(11):20952102.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Lee YJ, Terbrugge KG, Saliou G, Krings T. Clinical features and outcomes of spinal cord arteriovenous malformations: comparison between nidus and fistulous types. Stroke. 2014;45(9):26062612.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Lee YJ, Lin KC, Tsai CC, Lin HY. Clipping of spinal arteriovenous fistula of the filum terminale under intraoperative angiography guidance. Formos J Surg. 2019;52(4):151153.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11

    Rosenblum B, Oldfield EH, Doppman JL, Di Chiro G. Spinal arteriovenous malformations: a comparison of dural arteriovenous fistulas and intradural AVM’s in 81 patients. J Neurosurg. 1987;67(6):795802.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12

    Mathur S, Bharatha A, Huynh TJ, Aviv RI, Symons SP. Comparison of time-resolved and first-pass contrast-enhanced MR angiography in pretherapeutic evaluation of spinal dural arteriovenous fistulas. AJNR Am J Neuroradiol. 2017;38(1):206212.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Nijenhuis RJ, Mull M, Wilmink JT, Thron AK, Backes WH. MR angiography of the great anterior radiculomedullary artery (Adamkiewicz artery) validated by digital subtraction angiography. AJNR Am J Neuroradiol. 2006;27(7):15651572.

    • Search Google Scholar
    • Export Citation
  • 14

    Rodriguez FJ, Crum BA, Krauss WE, Scheithauer BW, Giannini C. Venous congestive myelopathy: a mimic of neoplasia. Mod Pathol. 2005;18(5):710718.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15

    Gueguen B, Merland JJ, Riche MC, Rey A. Vascular malformations of the spinal cord: intrathecal perimedullary arteriovenous fistulas fed by medullary arteries. Neurology. 1987;37(6):969979.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16

    Meisel HJ, Lasjaunias P, Brock M. Modern management of spinal and spinal cord vascular lesions. Minim Invasive Neurosurg. 1995;38(4):138145.

  • 17

    Tender GC, Vortmeyer AO, Oldfield EH. Spinal intradural arteriovenous fistulas acquired in late adulthood: absent spinal venous drainage in pathogenesis and pathophysiology. Report of two cases. J Neurosurg Spine. 2005;3(6):488494.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18

    Mitha AP, Murphy EE, Ogilvy CS. Type A intradural spinal arteriovenous fistula. Case report. J Neurosurg Spine. 2006;5(5):447450.

  • 19

    Jin YJ, Kim KJ, Kwon OK, Chung SK. Perimedullary arteriovenous fistula of the filum terminale: case report. Neurosurgery. 2010;66(1):E219E220.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20

    Witiw CD, Fallah A, Radovanovic I, Wallace MC. Sacral intradural arteriovenous fistula treated indirectly by transection of the filum terminale: technical case report. Neurosurgery. 2011;69(3):E780E784.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21

    Lim SM, Choi IS, David CA. Spinal arteriovenous fistulas of the filum terminale. AJNR Am J Neuroradiol. 2011;32(10):18461850.

  • 22

    Trinh VT, Duckworth EA. Surgical excision of filum terminale arteriovenous fistulae after lumbar fusion: Value of indocyanine green and theory on origins (a technical note and report of two cases). Surg Neurol Int. 2011;2:63.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23

    Saito H, Hida K, Asano T, et al. Conus perimedullary arteriovenous fistula with multiple shunt points including the cauda equina: a case report. Article in Japanese. No Shinkei Geka. 2011;39(4):375380.

    • Search Google Scholar
    • Export Citation
  • 24

    Kumar A, Deopujari CE, Mhatre M. Misdiagnosis in a case of non-compressive myelopathy due to a lumbar spinal intradural fistula supplied by the Artery of Adamkiewicz. Surg Neurol Int. 2011;2:12.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25

    Haddad S, Condette-Auliac S, Ozanne A, Roccatagliata L, Rodesch G. Arteriovenous fistula of the filum terminale: radiological diagnosis and therapeutic management by embolization. J Neuroradiol. 2012;39(5):368372.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26

    Takami T, Yamagata T, Mitsuhashi Y, Hayasaki K, Ohata K. Direct surgery for spinal arteriovenous fistulas of the filum terminale with intraoperative image guidance. Spine (Phila Pa 1976).2012;37(24):E1524E1528.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27

    Fischer S, Aguilar Perez M, Bassiouni H, Hopf N, Bäzner H, Henkes H. Arteriovenous fistula of the filum terminale: diagnosis, treatment, and literature review. Clin Neuroradiol. 2013;23(4):309314.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28

    Macht S, Chapot R, Bieniek F, Hänggi D, Turowski B. Unique sacral location of an arteriovenous fistula of the filum terminale associated with diastematomyelia and lowered spinal cords. Neuroradiology. 2012;54(5):517519.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29

    Chanthanaphak E, Pongpech S, Jiarakongmun P, Kobkitsuksakul C, Chi CT, Terbrugge KG. Filum terminale arteriovenous fistulas: the role of endovascular treatment. J Neurosurg Spine. 2013;19(1):4956.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30

    Takeuchi M, Niwa A, Matsuo N, et al. Pathomorphological description of the shunted portion of a filum terminale arteriovenous fistula. Spine J. 2014;14(2):e7e10.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31

    Krishnan P, Banerjee TK, Saha M. Congestive myelopathy (Foix-Alajouanine Syndrome) due to intradural arteriovenous fistula of the filum terminale fed by anterior spinal artery: Case report and review of literature. Ann Indian Acad Neurol. 2013;16(3):432436.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32

    Sharma P, Ranjan A, Lath R. Arteriovenous fistula of the filum terminale misdiagnosed and previously operated as lower lumbar degenerative disease. Asian Spine J. 2014;8(3):365370.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33

    Wajima D, Nakagawa I, Park HS, et al. A case of filum terminale arterial venous fistula needed a long arterial access for trans-arterial shunt obliteration. Interv Neuroradiol. 2017;23(2):221227.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34

    Sharma BB, Sharma S, Ramachandran P, Jilowa S. Arterial venous fistula (AVF) of filum terminale-MRi diagnosis - a case report. Andrology. 2016;5:1.

    • Search Google Scholar
    • Export Citation
  • 35

    Ding D, Law AJ, Scotter J, Brew S. Lumbar disc herniation exacerbating venous hypertension from a spinal perimedullary arteriovenous fistula of the filum terminale. J Neurol Sci. 2016;369:276277.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36

    Hong T, Park JE, Ling F, et al. Comparison of 3 different types of spinal arteriovenous shunts below the conus in clinical presentation, radiologic findings, and outcomes. AJNR Am J Neuroradiol. 2017;38(2):403409.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37

    Li J, Li G, Bian L, et al. Concomitant lumbosacral perimedullary arteriovenous fistula and spinal dural arteriovenous fistula. World Neurosurg.2017;105:1041.e71041.e14.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38

    Hong T, Yu JX, Liu W, et al. Filum terminale arteriovenous fistulas with multiple shunt points: a report of two exceptional cases. World Neurosurg.2018;118:235239.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39

    Lamsam L, Quon J, Fischbein N, Iv M, Dodd R, Ratliff J. Conus medullaris dural arteriovenous fistula arising from the artery of the filum terminale: 2-dimensional operative video. Oper Neurosurg (Hagerstown). 2018;15(4):471.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40

    Takai K, Komori T, Taniguchi M. Angioarchitecture of filum terminale arteriovenous fistulas: relationship with a tethered spinal cord. World Neurosurg. 2019;122:e795e804.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 41

    Scullen T, Mathkour M, Amenta PS, Dallapiazza RF. Arteriovenous fistula of the filum terminale: a case report and review of the literature. World Neurosurg. 2019;130:4249.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 42

    Gao P, Li X, Li G. Retrograde cannulation of the draining vein for embolization of filum terminale arteriovenous fistula in the lower sacral region. World Neurosurg.2019;130:254258.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 43

    Lakhdar F, Benzagmout M, Chakour K, Chaoui MEF. Spinal arteriovenous fistulas of the filum terminale: case report and literature review. Asian J Neurosurg. 2019;14(4):12771282.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 44

    Iampreechakul P, Tirakotai W, Lertbutsayanukul P, Khunvutthidee S, Thammachantha S, Siriwimonmas S. Spinal sparganosis coexisting with acquired arteriovenous fistula of the filum terminale. World Neurosurg.2020;136:341347.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 45

    Iampreechakul P, Tirakotai W, Wangtanaphat K, Lertbutsayanukul P, Siriwimonmas S. Filum terminale arteriovenous fistula in association with degenerative lumbosacral spinal canal stenosis: report of 3 cases and review of the literature. World Neurosurg. 2020;138:231241.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 46

    Namba K, Niimi Y, Ishiguro T, Higaki A, Toma N, Komiyama M. Cauda equina and filum terminale arteriovenous fistulas: anatomic and radiographic features. AJNR Am J Neuroradiol. 2020;41(11):21662170.

    • Crossref
    • Search Google Scholar
    • Export Citation

Illustration from Agosti et al. (E5). Used with permission of Mayo Foundation for Medical Education and Research. All rights reserved.

  • View in gallery

    A and B: Sagittal T2- and CE T1-weighted MR images reveal thoracolumbar contrast-enhancing congestive myelopathy (arrow) associated with a dilated vein from the lumbosacral to the thoracolumbar region (arrowheads) suggesting an AV shunt in the deep lumbosacral region (circles). C: CE-MRA image (arterial phase) shows the early filling of the arterialized FTV beginning at the S2 level and running upward to the perimedullary venous plexus in the thoracolumbar region (arrowheads). D–F: DSA in lateral and posteroanterior projections identifies the AV shunt at the S1/2 level (curved arrow), supplied via the FTA (arrowheads). Note the normal caliber of the Adamkiewicz artery originating from the left L2 radicular artery.

  • View in gallery

    Case 15. MR workup. A and B: Sagittal T2- and CE T1-weighted images show congestive thoracic myelopathy. C–E: Spinal CE-MRA (sagittal and coronal multiplanar reconstruction) reveals an abnormally arterialized vein in the deep lumbosacral region (arrowheads) associated with thoracic arterialized perimedullary veins, suggesting a sacral location of the AV shunt. The ascending filling of the dilated FTV supports the assumption of a sacral AV shunt (curved arrows). F: Note the prominent T8 intercostal artery (Adamkiewicz artery) which supplies the FTA descending to the AV shunt (circle). G–I: Sagittal and coronal reconstructions of CE T1- and T2-weighted images demonstrate the arterialized and elongated FTV at the S2 level and its caudocranial course (arrowheads).

  • View in gallery

    Case 15. DSA workup. A–C: DSA (posteroanterior projection) studies identify the ASA (arrows), supplied via a radiculomedullary branch of the left T8 intercostal segmental artery (Adamkiewicz artery), as well as a paralleling course of the FTA and dilated FTV. The AV shunt is located at the S1/2 level (curved arrows). D–F: Axial, sagittal, and coronal multiplanar reconstructions of DynaCT (2 mm, 8-second rotation) precisely identify the location of the AV shunt at the S1/2 level (arrowheads).

  • View in gallery

    Case 15. Intraoperative findings. Intraoperative (A) and ICG angiography (B) images demonstrate the parallel course of the FTA (arrows) and the arterialized and elongated FTV (arrowheads) as well as the AVM at the S1/2 level (*).

  • 1

    Djindjian M, Djindjian R, Rey A, Hurth M, Houdart R. Intradural extramedullary spinal arterio-venous malformations fed by the anterior spinal artery. Surg Neurol. 1977;8(2):8593.

    • Search Google Scholar
    • Export Citation
  • 2

    Aminoff MJ, Logue V. Clinical features of spinal vascular malformations. Brain. 1974;97(1):197210.

  • 3

    Aminoff MJ, Logue V. The prognosis of patients with spinal vascular malformations. Brain. 1974;97(1):211218.

  • 4

    Mull M, Nijenhuis RJ, Backes WH, Krings T, Wilmink JT, Thron A. Value and limitations of contrast-enhanced MR angiography in spinal arteriovenous malformations and dural arteriovenous fistulas. AJNR Am J Neuroradiol. 2007;28(7):12491258.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5

    Rodesch G, Hurth M, Alvarez H, Tadié M, Lasjaunias P. Classification of spinal cord arteriovenous shunts: proposal for a reappraisal--the Bicêtre experience with 155 consecutive patients treated between 1981 and 1999. Neurosurgery. 2002;51(2):374380.

    • Search Google Scholar
    • Export Citation
  • 6

    Giordan E, Brinjikji W, Ciceri E, Lanzino G. Arteriovenous fistulae of the filum terminale. J Neurointerv Surg. 2018;10(2):191197.

  • 7

    Rodesch G, Lasjaunias P. Spinal cord arteriovenous shunts: from imaging to management. Eur J Radiol. 2003;46(3):221232.

  • 8

    Mull M, Othman A, Dafotakis M, Hans FJ, Schubert GA, Jablawi F. Spinal epidural arteriovenous fistula with perimedullary venous reflux: clinical and neuroradiologic features of an underestimated vascular disorder. AJNR Am J Neuroradiol. 2018;39(11):20952102.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9

    Lee YJ, Terbrugge KG, Saliou G, Krings T. Clinical features and outcomes of spinal cord arteriovenous malformations: comparison between nidus and fistulous types. Stroke. 2014;45(9):26062612.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10

    Lee YJ, Lin KC, Tsai CC, Lin HY. Clipping of spinal arteriovenous fistula of the filum terminale under intraoperative angiography guidance. Formos J Surg. 2019;52(4):151153.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11

    Rosenblum B, Oldfield EH, Doppman JL, Di Chiro G. Spinal arteriovenous malformations: a comparison of dural arteriovenous fistulas and intradural AVM’s in 81 patients. J Neurosurg. 1987;67(6):795802.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12

    Mathur S, Bharatha A, Huynh TJ, Aviv RI, Symons SP. Comparison of time-resolved and first-pass contrast-enhanced MR angiography in pretherapeutic evaluation of spinal dural arteriovenous fistulas. AJNR Am J Neuroradiol. 2017;38(1):206212.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Nijenhuis RJ, Mull M, Wilmink JT, Thron AK, Backes WH. MR angiography of the great anterior radiculomedullary artery (Adamkiewicz artery) validated by digital subtraction angiography. AJNR Am J Neuroradiol. 2006;27(7):15651572.

    • Search Google Scholar
    • Export Citation
  • 14

    Rodriguez FJ, Crum BA, Krauss WE, Scheithauer BW, Giannini C. Venous congestive myelopathy: a mimic of neoplasia. Mod Pathol. 2005;18(5):710718.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15

    Gueguen B, Merland JJ, Riche MC, Rey A. Vascular malformations of the spinal cord: intrathecal perimedullary arteriovenous fistulas fed by medullary arteries. Neurology. 1987;37(6):969979.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16

    Meisel HJ, Lasjaunias P, Brock M. Modern management of spinal and spinal cord vascular lesions. Minim Invasive Neurosurg. 1995;38(4):138145.

  • 17

    Tender GC, Vortmeyer AO, Oldfield EH. Spinal intradural arteriovenous fistulas acquired in late adulthood: absent spinal venous drainage in pathogenesis and pathophysiology. Report of two cases. J Neurosurg Spine. 2005;3(6):488494.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18

    Mitha AP, Murphy EE, Ogilvy CS. Type A intradural spinal arteriovenous fistula. Case report. J Neurosurg Spine. 2006;5(5):447450.

  • 19

    Jin YJ, Kim KJ, Kwon OK, Chung SK. Perimedullary arteriovenous fistula of the filum terminale: case report. Neurosurgery. 2010;66(1):E219E220.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20

    Witiw CD, Fallah A, Radovanovic I, Wallace MC. Sacral intradural arteriovenous fistula treated indirectly by transection of the filum terminale: technical case report. Neurosurgery. 2011;69(3):E780E784.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21

    Lim SM, Choi IS, David CA. Spinal arteriovenous fistulas of the filum terminale. AJNR Am J Neuroradiol. 2011;32(10):18461850.

  • 22

    Trinh VT, Duckworth EA. Surgical excision of filum terminale arteriovenous fistulae after lumbar fusion: Value of indocyanine green and theory on origins (a technical note and report of two cases). Surg Neurol Int. 2011;2:63.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23

    Saito H, Hida K, Asano T, et al. Conus perimedullary arteriovenous fistula with multiple shunt points including the cauda equina: a case report. Article in Japanese. No Shinkei Geka. 2011;39(4):375380.

    • Search Google Scholar
    • Export Citation
  • 24

    Kumar A, Deopujari CE, Mhatre M. Misdiagnosis in a case of non-compressive myelopathy due to a lumbar spinal intradural fistula supplied by the Artery of Adamkiewicz. Surg Neurol Int. 2011;2:12.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25

    Haddad S, Condette-Auliac S, Ozanne A, Roccatagliata L, Rodesch G. Arteriovenous fistula of the filum terminale: radiological diagnosis and therapeutic management by embolization. J Neuroradiol. 2012;39(5):368372.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26

    Takami T, Yamagata T, Mitsuhashi Y, Hayasaki K, Ohata K. Direct surgery for spinal arteriovenous fistulas of the filum terminale with intraoperative image guidance. Spine (Phila Pa 1976).2012;37(24):E1524E1528.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27

    Fischer S, Aguilar Perez M, Bassiouni H, Hopf N, Bäzner H, Henkes H. Arteriovenous fistula of the filum terminale: diagnosis, treatment, and literature review. Clin Neuroradiol. 2013;23(4):309314.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28

    Macht S, Chapot R, Bieniek F, Hänggi D, Turowski B. Unique sacral location of an arteriovenous fistula of the filum terminale associated with diastematomyelia and lowered spinal cords. Neuroradiology. 2012;54(5):517519.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29

    Chanthanaphak E, Pongpech S, Jiarakongmun P, Kobkitsuksakul C, Chi CT, Terbrugge KG. Filum terminale arteriovenous fistulas: the role of endovascular treatment. J Neurosurg Spine. 2013;19(1):4956.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30

    Takeuchi M, Niwa A, Matsuo N, et al. Pathomorphological description of the shunted portion of a filum terminale arteriovenous fistula. Spine J. 2014;14(2):e7e10.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31

    Krishnan P, Banerjee TK, Saha M. Congestive myelopathy (Foix-Alajouanine Syndrome) due to intradural arteriovenous fistula of the filum terminale fed by anterior spinal artery: Case report and review of literature. Ann Indian Acad Neurol. 2013;16(3):432436.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32

    Sharma P, Ranjan A, Lath R. Arteriovenous fistula of the filum terminale misdiagnosed and previously operated as lower lumbar degenerative disease. Asian Spine J. 2014;8(3):365370.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33

    Wajima D, Nakagawa I, Park HS, et al. A case of filum terminale arterial venous fistula needed a long arterial access for trans-arterial shunt obliteration. Interv Neuroradiol. 2017;23(2):221227.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34

    Sharma BB, Sharma S, Ramachandran P, Jilowa S. Arterial venous fistula (AVF) of filum terminale-MRi diagnosis - a case report. Andrology. 2016;5:1.

    • Search Google Scholar
    • Export Citation
  • 35

    Ding D, Law AJ, Scotter J, Brew S. Lumbar disc herniation exacerbating venous hypertension from a spinal perimedullary arteriovenous fistula of the filum terminale. J Neurol Sci. 2016;369:276277.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36

    Hong T, Park JE, Ling F, et al. Comparison of 3 different types of spinal arteriovenous shunts below the conus in clinical presentation, radiologic findings, and outcomes. AJNR Am J Neuroradiol. 2017;38(2):403409.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37

    Li J, Li G, Bian L, et al. Concomitant lumbosacral perimedullary arteriovenous fistula and spinal dural arteriovenous fistula. World Neurosurg.2017;105:1041.e71041.e14.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38

    Hong T, Yu JX, Liu W, et al. Filum terminale arteriovenous fistulas with multiple shunt points: a report of two exceptional cases. World Neurosurg.2018;118:235239.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39

    Lamsam L, Quon J, Fischbein N, Iv M, Dodd R, Ratliff J. Conus medullaris dural arteriovenous fistula arising from the artery of the filum terminale: 2-dimensional operative video. Oper Neurosurg (Hagerstown). 2018;15(4):471.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40

    Takai K, Komori T, Taniguchi M. Angioarchitecture of filum terminale arteriovenous fistulas: relationship with a tethered spinal cord. World Neurosurg. 2019;122:e795e804.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 41

    Scullen T, Mathkour M, Amenta PS, Dallapiazza RF. Arteriovenous fistula of the filum terminale: a case report and review of the literature. World Neurosurg. 2019;130:4249.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 42

    Gao P, Li X, Li G. Retrograde cannulation of the draining vein for embolization of filum terminale arteriovenous fistula in the lower sacral region. World Neurosurg.2019;130:254258.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 43

    Lakhdar F, Benzagmout M, Chakour K, Chaoui MEF. Spinal arteriovenous fistulas of the filum terminale: case report and literature review. Asian J Neurosurg. 2019;14(4):12771282.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 44

    Iampreechakul P, Tirakotai W, Lertbutsayanukul P, Khunvutthidee S, Thammachantha S, Siriwimonmas S. Spinal sparganosis coexisting with acquired arteriovenous fistula of the filum terminale. World Neurosurg.2020;136:341347.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 45

    Iampreechakul P, Tirakotai W, Wangtanaphat K, Lertbutsayanukul P, Siriwimonmas S. Filum terminale arteriovenous fistula in association with degenerative lumbosacral spinal canal stenosis: report of 3 cases and review of the literature. World Neurosurg. 2020;138:231241.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 46

    Namba K, Niimi Y, Ishiguro T, Higaki A, Toma N, Komiyama M. Cauda equina and filum terminale arteriovenous fistulas: anatomic and radiographic features. AJNR Am J Neuroradiol. 2020;41(11):21662170.

    • Crossref
    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 433 433 318
PDF Downloads 314 314 217
EPUB Downloads 0 0 0