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Spine
Original research
Concomitant origin of the anterior or posterior spinal artery with the feeder of a spinal dural arteriovenous fistula (SDAVF)
  1. Yudhi Adrianto1,2,
  2. Ku Hyun Yang1,
  3. Hae-Won Koo1,
  4. Wonhyoung Park1,
  5. Sung Chul Jung1,
  6. Jie Eun Park1,
  7. Kwang-Kuk Kim3,
  8. Sang Ryong Jeon4,
  9. Dae Chul Suh1
  1. 1Department of Radiology, Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
  2. 2Departement of Neurology, Soetomo General Hospital/Airlangga University Hospital, Airlangga University Medical Faculty, Surabaya, Indonesia
  3. 3Department of Neurology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
  4. 4Department of Neurological Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
  1. Correspondence to Dr Dae Chul Suh, Department of Radiology, Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, 88, Olympic-ro 43-gil, Songpa-gu, Seoul 138-736, Korea; dcsuh{at}amc.seoul.kr

Abstract

Background/objective The concomitant origin of the anterior spinal artery (ASA) or the posterior spinal artery (PSA) from the feeder of a spinal dural arteriovenous fistula (SDAVF) is rare and the exact incidence is not known. We present our experience with the management of SDAVFs in such cases.

Methods In 63 patients with SDAVF between 1993 and 2015, the feeder origin of the SDAVF was evaluated to determine whether it was concomitant with the origin of the ASA or PSA. Embolization was attempted when the patient did not want open surgery and an endovascular approach was regarded as safe and possible. The outcome of the procedure was evaluated as complete, partial, or no obliteration. The clinical outcome was evaluated by Aminoff–Logue (ALS) gait and micturition scale scores.

Results Nine patients (14%) had a concomitant origin of the ASA or PSA with the feeder. There were two cervical, five thoracic, and two lumbar level SDAVFs. A concomitant origin of the feeder was identified with the ASA (n=7) and PSA (n=2). Embolization was performed in four patients and open surgery was performed in five. Embolization resulted in complete obliteration in three patients and partial obliteration in one. Using the ALS gait and micturition scale, the final outcome improved in six while three cases remained in an unchanged condition over 2–148 months.

Conclusions The concomitant origin of the ASA or PSA with the feeder occurs occasionally. Complete obliteration of the fistula can be achieved either by embolization or open surgery. Embolization can be carefully performed in selected patients who are in a poor condition and do not want to undergo open surgery.

  • Spine
  • Fistula
  • Arteriovenous Malformation
  • Intervention

https://doi.org/10.1136/neurintsurg-2016-012267

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    Introduction

    Spinal dural arteriovenous fistulas (SDAVFs), also called type 1 spinal arteriovenous malformations, are the most frequent vascular malformation of the spine and account for approximately 70–80% of all vascular spinal malformations.1–3 Typically, SDAVFs become symptomatic in elderly men with a mean age ranging from 55 to 60 years. Only 1% of patients present at <30 years of age. There is a male preponderance (male:female ratio of 5:1).4 Most SDAVFs are found in the thoracolumbar region; cervical or sacral lesions occur in <6% of SDAVFs.5

    The success of SDAVF treatment depends on the occlusion of the shunting area, which can be achieved through either a surgical or endovascular approach.6 The benefit of embolization therapy is that it is a less invasive approach with comparable outcomes to those of surgical treatment.7 Although endovascular embolization is an effective therapy and can be used as a definitive treatment in most patients,8 embolization is severely limited if the SDAVF originates from the radicular branches of the segmental artery that supplies both the fistula and the anterior spinal artery (ASA) or the posterior spinal artery (PSA).8 The purpose of this report is to present our experience of SDAVFs that have a concomitant origin of the ASA or PSA with the feeder of the SDAVF.

    Methods

    We conducted a retrospective review of data from a series of patients with SDAVF who underwent endovascular embolization at the Asan Medical Center between 1993 and 2015. Among 63 patients with SDAVF in the prospectively collected database we included SDAVFs that had a concomitant origin of the ASA or PSA with the feeder of the SDAVF. The local institutional review board approved the study and patients provided written informed consent.

    Angiographic findings of the segmental artery, including the lesion level, were reviewed. Other information obtained included patient demographics, onset, duration of follow-up, imaging follow-up, and functional outcome. The functional outcome was determined by the Aminoff–Logue (ALS) gait and micturition scale scores, which were compared before and after treatment.

    The procedural outcome, as shown by embolization results, was evaluated as complete, partial, or no obliteration. Complete obliteration was achieved when glue penetrated into the vein beyond the fistula and follow-up MRI showed improvement of cord edema and/or disappearance of abnormal vessels around the spinal cord. We regarded obliteration as partial when the glue did not penetrate into the vein or abnormal vessel remained around the spinal cord during follow-up MRI.

    Embolization was attempted when the patient did not want open surgery and an endovascular approach was regarded as safe and possible. Intraoperative monitoring was done during surgery. Intraoperative monitoring with provocative testing was not done during embolization.

    Endovascular embolization procedure

    Patients received general anesthesia for SDAVF embolization. Appropriate monitoring including ECG, arterial oxygen saturation, and blood pressure were performed. A 5 F introducer sheath was placed in the femoral artery.

    Spinal angiography was performed to evaluate the ASA and PSA and the location of the SDAVF. After the diagnostic procedure, a 4 F or 5 F catheter was positioned in the segmental artery supplying the SDAVF. Three-dimensional rotation angiography was performed in recent patients if available.9 Embolization of the SDAVF was attempted if a selective position in the feeding artery could be achieved, and was continued if a secure microcatheter position could be achieved superselectively in the feeder to the SDAVF without disturbing the ASA or PSA.

    A microcatheter was subsequently navigated over a microguidewire to reach the most distal aspect of the pedicle supplying the SDAVF. The position of the microcatheter was angiographically confirmed to be in a complete wedged position—that is, with no reflux of contrast agent from the tip of the microcatheter into the radiculomedullary or radiculopial artery. Endovascular embolization of the SDAVF was performed with a mixture of cyanoacrylate glue (NBCA; Codman Neurovascular, Raynham, Massachusetts, USA) and Lipiodol (Guerbet, Roissy CDG, France). The concentration of NBCA ranged between 20% and 30%. The injection of NBCA was performed under subtraction fluoroscopy, with special care taken not to have any reflux to the ASA or PSA.

    Surgical operation

    A surgical approach was performed in patients with the common origin of the artery supplying the fistula and ASA or PSA if an endovascular approach could not be achieved. A laminectomy was performed one level above and below the SDAVF. Following laminectomy, the dura was opened in a standard longitudinal fashion and the intradural arterialized vein was identified near the nerve root where the former exits the dura. A sharp dissection of the vein was then performed. When the entire vein had been mobilized, it was cauterized with bipolar forceps and, if possible, sharply divided. Inspection and cauterization of the inner dural layer were usually the final step.10

    Statistical analysis

    The χ2 test, exact Fisher test, and χ2 test for trend were used for analyzing categorical data while the t test and Wilcoxon–Mann–Whitney U test were used for continuous data.

    Results

    Between 1993 and 2015 a total of 63 patients were treated for a SDAVF. Nine patients (14%) had a common origin of the ASA/PSA with the same radicular branches of the segmental artery of the SDAVF feeder (table 1). There were eight men and one woman whose ages ranged from 45 to 67 years (mean 55.3 years). A concomitant origin of the feeder was identified with the ASA (n=7) and PSA (n=2). There were two cervical, five thoracic, and two lumbar level fistulas. The mean duration of symptoms before treatment (onset) was 15 months (range 1–78 months). Four patients were treated with an endovascular approach (figure 1) and five patients were treated with a surgical approach. Embolization resulted in complete obliteration in three patients including one who underwent embolization of the residual feeder at one level above after the first embolization (figure 2) and partial obliteration in one because the glue did not penetrate into the vein (figure 3). Open surgery resulted in complete obliteration in three patients and partial obliteration in two because there remained abnormal vessels around the spinal cord on MRI 5 and 6 months after surgery, respectively (figure 4). A possible cause of partial obliteration during surgical operation seemed to be partial resection of the fistula and vein in cases of multiple numerous fistula channels around the fistula point. Using the ALS gait and micturition scale, the final outcome improved in six while three cases remained in an unchanged condition during a mean follow-up period of 37 months (range 2–148 months) (table 1). Seven patients underwent MRI follow-up during a mean period of 12 months (range 1 week–6 years) and angiography follow-up was done in one patient after 6 years. Two patients refused to undergo further examination (figures 5 and 6).

    View this table:
    Table 1

    Summary of the nine patients with a concomitant origin of the fistula feeder and the radiculomedullary or medicullopial arteries

    Figure 1
    Figure 1

    A middle-aged patient (patient 1) with a tingling sensation of the left arm was diagnosed with a spinal dural arteriovenous fistula (SDAVF) by C-spine MRI. (A) Cervical angiogram showing the site of the SDAVF, the feeder from the radicular artery at the C4–C5 level on the left side. (B) Right vertebral artery angiogram showing an opposite symmetric limb of the anterior spinal artery (ASA) at the same level of the fistula on the left side. (C) Superselective angiogram of the radicular artery at the C5 level on the left side revealed the concomitant origin of the ASA with the feeder of the SDAVF. (D) Note a small glue cast (white arrow) in the vein after glue embolization. Post-embolization right (E) and left (F) vertebral angiograms show complete obliteration of the SDAVF without disturbance of the ASA (black arrow in E). (G) Schematic diagram showing the relationship of the fistula feeder and ASA. Note flow direction and shunt (asterisk) before microcatheter selection (arrow). (H) After selection of the feeder at the wedged position, the flow of ASA was reversed (curved arrow). Such a reverse flow could introduce embolic agent into the fistula (asterisk) while protecting the ASA.

    Figure 2
    Figure 2

    An elderly patient (patient 3) underwent T10–11 spinal dural arteriovenous fistula (SDAVF) embolization of the residual feeder with cyanoacrylate glue (NBCA). (A) Thoracic T10 segmental artery angiogram shows the feeder of the fistula and anterior spinal artery (ASA) arising from the same level. Complete wedged position at the feeder of the fistula could be achieved without regurgitation of any contrast agent from the microcatheter tip into the proximally located ASA. (B) After embolization the ASA remained preserved. (C) Glue cast smoothly proceeded and occluded the fistula and the draining vein. (D) Schematic diagram shows the concomitant origin of the feeder and ASA. Note the fistula point (asterisk) at the color change which reciprocally communicated with the previous fistula feeder from one level below (dotted red-colored vessel). (E) The wedged position of the microcatheter into the feeder may prevent regurgitation of the embolic agent into the ASA while introducing the agent into the fistula (asterisk).

    Figure 3
    Figure 3

    An elderly patient (patient 4) with a concomitant feeder with the radiculomedullary artery at right L1. (A) Selective angiogram of the fistula at the complete wedged position. (B) After embolization there remained another channel (arrowhead) filling the draining vein (arrows) beyond the embolized fistula point. (C) Final angiogram shows the intact radiculomedullary artery and slow filling of the draining vein (arrows). Note a hairpin turn (asterisk) of the prominent radiculomedullary artery which remains intact after embolization. Procedural outcome was regarded as partial. There was no remarkable improvement from the complete paraplegia and flaccid sphincter function during 7 month follow-up. The patient refused further treatment.

    Figure 4
    Figure 4

    An elderly patient (patient 6) with a spinal dural arteriovenous fistula at the T5 level. (A) Three-dimensional rotational angiogram shows concomitant origin of the anterior spinal artery and the feeder. (B) Congestive venous myelopathy in the conus medullaris with numerous tortuous abnormal vessels around the spinal cord. (C) There remained considerable abnormal vessels around the spinal cord even though edema in the conus medullaris disappeared 2 weeks after open surgery. The outcome following the procedure was regarded as partial. The patient's symptoms improved during 10 months. Follow-up angiogram was not obtained.

    Figure 5
    Figure 5

    (A) Sagittal T2-weighted MRI shows multiple flow-void type lesions and venous hypertension at the thoracic level. (B, C) T6 segmental angiogram shows the feeder of the spinal dural arteriovenous fistula arising from the same pedicle with the anterior spinal artery (ASA) (arrow). The embolization was aborted because of failure to secure the position of the ASA from the feeder of the fistula.

    Figure 6
    Figure 6

    Representative images (anteroposterior view) of five patients (patients 2, 5, 6, 8, and 9) whose images are not shown in earlier figures. Arrows indicate the radicullomedullary or radiculopial artery.

    Comparison of patient demographics, lesion levels, and surgical and endovascular results between the group of patients in whom the feeder origin of the SDAVF was concomitant with the origin of the ASA or PSA (n=9) and those in whom it was not (n=54) did not show any statistical significance. However, comparison of improvement in the two groups before and after treatment showed less improvement in AL micturition (p=0.059) than AL gait (p=0.039) in the group in whom the feeder origin of the SDAVF was concomitant with the origin of the ASA or PSA compared with improvement in AL gait (p=0.000) and AL micturition (p=0.000) in the group in whom the feeder origin of the SDAVF was not concomitant with the origin of the ASA or PSA.

    Discussion

    In our patient series, 14% of patients had a concomitant origin of the ASA or PSA with the SDAVF feeder. SDAVF, which is known to arise from the radicular artery, should be further scrutinized for a concomitant origin of the radiculomedullary or radiculopial arteries that supply the spinal cord. Three-dimensional rotational angiography, as used in some patients in our study, may be necessary to reveal the exact relationship of the two vessels for further management.9 Cervical SDAVFs are more likely to have the ASA/PSA arising from the involved radicular branches of the segmental artery as the radiculomedullary and radiculopial arteries are more numerous in the cervical spine than in the thoracic spine in adults. Also, the collateral supply to the ASA or PSA from other segmental arteries is much more significant in the cervical spine, with less risk of post-procedural ischemia.9

    Management of such patients may require surgical resection as the first treatment option. However, some patients tend to resist undergoing open surgery, especially when they are in a poor condition. Our study showed that embolization can also be performed in selected patients with a secure catheter position or under favorable hemodynamic conditions, especially in patients who refuse surgery. However, it should be emphasized that inadvertent complications may occur during embolization even though safe embolization using a completely wedged microcatheter position appears to be possible by experienced operators who understand the anatomic relationship including potential collaterals in the vertebral column and spinal cord.11

    Our study showed that there are two situations that can provide a possible option for safe embolization. One is a favorable hemodynamic condition, as with patient 1 in whom the radicullomedullary artery with symmetric bilateral limbs arose from both sides. Therefore, a wedged position of a microcatheter in the ipsilateral limb of the radicullomedullary artery could induce reversed flow from the opposite side. Such a reversed flow protected the inadvertent advance of the liquid embolic agent while it was injected.

    The other option is to induce flow arrest by creating a wedged position with superselection of the microcatheter beyond the origin of the radiculomedullary or radiculopial artery into the SDAVF feeder, as performed in the other three patients. In this situation, it should be mandatory to confirm the wedged position to ensure that neither regurgitated nor inadvertently migrated embolic agent enters into the radicullomedullary artery while injecting the agent or retrieving the microcatheter after agent injection. However, this situation is not always achievable because the lumen size may prevent introduction of the microcatheter into the feeder or vascular tortuousness may prevent superselection of the microcatheter.

    Although either glue or Onyx can be used according to the operator's experience, we preferred to use glue in this study for two reasons. One is that it is empirically easy to control glue on fluoroscopy12 and the other is that Onyx is known to be associated with poor venous penetration in the treatment of SDAVFs.13 We used 20–30% glue/Lipiodol mixture because the viscosity of glue/Lipiodol increased, polymerization time was prolonged, and diffusing capacity increased as the glue density decreased.14 ,15

    Patient recovery after treatment for SDAVF can vary according to disease stage, onset period, or patient status.5 ,16 Therefore, some patients had an unchanged clinical outcome although the result of the surgical or endovascular approach was complete. Symptomatic improvement was also expected in patients with partial obliteration of the lesion. However, follow-up is required for the recurrence of symptoms or the presence of residual lesions of spinal cord edema or abnormal vessels around the spinal cord, as seen in two of our study patients after open surgery.17 A possible cause of partial obliteration during the surgical operation may be partial resection of the fistula and vein in cases with multiple fistula channels around the fistula point. This phenomenon can also be found after endovascular embolization and may be the cause of later recurrence, even after complete obliteration of the fistula and the vein.18 ,19

    There are several limitations to our study. First, this study was based on limited experience in a tertiary referral center so care must be taken when generalizing our treatment concepts to other hospitals, especially those in which surgery is performed routinely. Second, the comparison of treatment outcomes between embolization and surgery was not complete because SDAVF is not a common disease and a concomitant origin of the feeder with the ASA or PSA is quite rare. Third, it is uncertain whether there is more recurrence of SDAVF when there is concomitant occurrence of the feeder with the ASA or PSA. If there were more channels of the fistula between the ASA/PSA and the draining vein, more radical dissection to separate the ASA/PSA and the draining vein during open surgery or deeper penetration of the embolic material beyond the fistula point during embolization would be required. Fourth, the possibility of multiple feeders of the SDAVF needs to be considered because residual or recurred feeders were not identified in patients with recurrence in our study by complete angiography. It is known that there are about 2% of multiple feeders in SDAVF.20 ,21

    Conclusion

    A concomitant origin of the ASA or PSA with the feeder of an SDAVF occurs occasionally (14%). Complete obliteration of the fistula can be achieved either by embolization or surgery. Embolization can be considered in selected patients when the radiculomedullary or radiculopial arteries can be secured.

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    Footnotes

    • Contributors DCS designed the study, collected data and edited the paper. YA analyzed the data, reviewed the literature, and drafted the paper. KHY, WP, JEP, H-WK, SCJ, K-KK, and SRJ critically reviewed the paper. All authors approved the final version of the manuscript.

    • Competing interests None declared.

    • Ethics approval Ethics approval was obtained from the local ethical review committee of Asan Medical Center.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Data sharing statement Data may be available for sharing on a per-request basis.