Treatment of high cervical arteriovenous fistulas in the craniocervical junction region

Abstract

The craniocervical junction (CCJ) is a complex region. Rarely, arteriovenous fistulas (AVFs) can occur in the CCJ region. Currently, it is accepted that CCJ AVFs should only refer to AVFs at the C1-C2 levels. It is reasonable to assume that high cervical CCJ AVFs are being referred to when discussing CCJ AVFs. High cervical CCJ AVFs can be divided into the following four types: dural AVF, radicular AVF, epidural AVF and perimedullary AVF. Until now, it was difficult to understand high cervical CCJ AVFs and provide a proper treatment for them. Therefore, an updated review of high cervical CCJ AVFs is necessary. In this review, the following issues are discussed: the definition of high cervical CCJ AVFs, vessel anatomy of the CCJ region, angioarchitecture of high cervical CCJ AVFs, treatment options, prognoses and complications. Based on the review and our experience, we found that the four types of high cervical CCJ AVFs share similar clinical and imaging characteristics. Patients may present with intracranial hemorrhage or congestive myelopathy. Treatment, including open surgery and endovascular treatment (EVT), can be used for symptomatic AVFs. Most high cervical CCJ AVFs can be effectively treated with open surgery. EVT remains challenging due to a high rate of incomplete obliteration and complications, and it can only be performed in superselective AVFs with simple angioarchitecture. Appropriate treatment can lead to a good prognosis.

Keywords: arteriovenous fistula; craniocervical junction; high cervical cord; review; treatment.

Figure 1

CCJ region definition. (A) MRI showing that the CCJ region was located between two black lines and formed by the occipital bone and C1-2 vertebrae. The red frame indicates the area often involved in CCJ AVF. (B,C) CTA showing the bony CCJ region (frames). AVF, arteriovenous fistula; C1-2, first and second cervical vertebrae; CCJ, craniocervical junction; CTA, computed tomography angiography; MRI, magnetic resonance imaging.

Figure 2

Arteries involved in the high cervical CCJ region. (A) DSA showing the radicular arteries from the VA at the C1-C5 levels. (B) DSA showing the ASA (arrowhead) from VA termination. The ASA had double trunks, and the radicular arteries of the C2-C3 levels could be seen. (C) DSA showing the ASA (arrowhead) originating from the C1 radicular artery. (D,E) DSA of anterior posterior (D) and lateral (E) views showing the C1 radicular artery (arrow). (F) DSA showing the extradural low PICA (PICA with arrow) and the PMA (PMA with arrow) from the VA. (G) DSA showing the anastomosis (asterisk) between the AphA and VA. (H) DSA showing the anastomosis (asterisk) between the OA and muscular branch of the VA. AphA, ascending pharyngeal artery; ASA, anterior spinal artery; C1-C5, first-fifth cervical vertebrae; CCJ, craniocervical junction; DSA, digital subtracted angiography; OA, occipital artery; PICA, posterior inferior cerebellar artery; PMA, posterior meningeal artery; VA, vertebral artery.

Figure 3

Venous plexuses in the CCJ region. (A) Posterior anterior view (left panel) and oblique view (right panel) CTA showing the anastomosed SVP, PVVP, and DJV. (B) Oblique view (left panel) and lateral view (right panel) CTA showing the anastomosed PVVP and DJV. C1, C2, first and second cervical vertebrae; CCJ, craniocervical junction; CTA, computed tomography angiography; DJV, deep jugular vein; EJV, external jugular vein; IJV, internal jugular vein; PVVP, paravertebral venous plexus; SVP, suboccipital venous plexus.

Figure 4

Locations of different high cervical CCJ AVFs. On the hybrid mode pattern of magnetic resonance imaging, the locations of different high cervical CCJ AVFs are shown. PAVF (red P with asterisk) located at the ventral spinal cord surface, RAVF (red R with thick line segments) located at C1-C2 nerves, DAVF (red D with double asterisks) located at the dorsal dura, EAVF (red E with asterisk) in ventral epidural space. AVF, arteriovenous fistula; C1-C2, first and second cervical vertebrae; CCJ, craniocervical junction; CSC, cervical spinal cord; D, dorsal; DAVF, dural AVF; EAVF, epidural AVF; PAVF, perimedullary AVF; RAVF, radicular AVF; V, ventral.

Figure 5

Types of high cervical CCJ AVFs. (A) Left panel showing the structure of DAVF in drawing, a radiculomeningeal artery and a radicular vein connected directly on dural sleeve of nerve root; Right panel showing the angioarchitecture of DAVF, the feeding artery was the C1 radicular artery, the asterisk indicated fistula point, and the arrowhead indicate the drainage into intracranial vein to sigmoid sinus. (B) Left panel showing the structure of the RAVF in drawing, a radicular (radiculomeningeal) artery and a radicular vein connected directly on the spinal nerve root. The ASA branch can be involved as the feeder (dotted line); right panel showing the angioarchitecture of the RAVF. The feeding artery was the C1 radicular artery, the asterisk indicates the fistula point, and the arrowhead indicates drainage into the intracranial vein. (C) Left panel showing the structure of the EAVF in the drawing. There is a direct arteriovenous shunt between the radicular and/or meningeal arteries and the epidural venous plexus. The ASA branch can be involved as the feeder (dotted line); right panel showing the angioarchitecture of the EAVF. The feeding artery is the C2 radicular artery, the asterisk indicates the fistula point, and the arrowhead indicates the drainage. (D) Left panel showing the structure of the PAVF in the drawing. The PAVF is a direct arteriovenous communication without an intervening nidus on the surface of the spinal cord; right panel showing the angioarchitecture of the PAVF. The feeding artery was the C2 radiculomedullary artery, the asterisk indicates the fistula point, and the arrowhead indicates the drainage. A, feeding artery; ASA, anterior spinal artery; AVF, arteriovenous fistula; C1, C2, and C5, first, second and fifth cervical vertebrae; CCJ, craniocervical junction; DAVF, dural AVF; EAVF, epidural AVF; F, fistula point; N, nerve; PAVF, perimedullary AVF; RAVF, radicular AVF; V, draining vein.

Figure 6

PICA involvement in the feeding artery of high cervical CCJ RAVF. DSA (left panel) and three-dimensional reconstructive DSA (right panel) showing a high cervical CCJ RAVF (asterisk in left panel) fed by the branch of the PICA (arrows); arrowheads in left panel indicate upward and downward draining veins. AVF, arteriovenous fistula; CCJ, craniocervical junction; DSA, digital subtracted angiography; PICA, posterior inferior cerebellar artery; RAVF, radicular AVF.

Figure 7

Multiple draining pathways in a high cervical CCJ AVF. Oblique-view DSA of the VA showing a CCJ AVF (asterisk in left panel) supplied by the C1 radicular artery (arrow in left panel); the drainage of the AVF had three pathways: downward into the perimedullary vein (arrowhead with number 1), lateral into the epidural venous plexus (arrowhead with number 2), and upward into the intracranial vein (arrowhead with number 3). AVF, arteriovenous fistula; C1, first cervical vertebrae; CCJ, craniocervical junction; DSA, digital subtracted angiography; VA, vertebral artery.

Figure 8

Open surgery in a high cervical CCJ DAVF with downward drainage. (A) MRI showing edema (arrow) of the medulla oblongata and abnormal vessels (arrowhead) in the front of the brainstem. (B) Arterial phase DSA of the left VA showing a CCJ DAVF (asterisk) fed by the C1 radicular artery. The drainage went into the intracranial vein (arrowhead). (C) Late arterial phase DSA of the anterior posterior view showing downward drainage into the perimedullary vein (arrowhead). (D) Late arterial phase DSA of the lateral view showing downward drainage, including downward ASV and PSV, and lateral drainage by the bridging and radicular veins (arrowhead). (E) Intraoperative image showing the thick arterialized draining vein (arrowhead). (F) Postoperative DSA showing that the DAVF was obliterated after the draining vein was coagulated and cut. ASV, anterior spinal vein; C1, first cervical vertebra; CCJ, craniocervical junction; DAVF, dural arteriovenous fistula; DSA, digital subtraction angiography; L, left; MRI, magnetic resonance imaging; PSV, posterior spinal vein; VA, vertebral artery.

Figure 9

Ruptured CCJ AVF with upward drainage. (A) Left panel: CT showing subarachnoid hemorrhage and fourth ventricle hemorrhage; Right panel: CTA showing that a CCJ AVF (asterisk) had upward venous drainage (black arrowhead) with varices (white arrowheads). (B) Left upper panel: CT showing subarachnoid hemorrhage; right upper panel: CTA showing that a CCJ AVF (asterisk) had upward venous drainage (arrowheads); two-dimensional DSA (left below panel) and three-dimensional DSA (right below panel) showing a RAVF (asterisks) fed by the C1 radicular artery (arrows). The drainage went into the intracranial vein (arrowheads). AVF, arteriovenous fistula; C1, first cervical vertebrae; CCJ, craniocervical junction; CT, computed tomography; CTA, CT angiography; DSA, digital subtracted angiography; RAVF, radicular AVF.

Figure 10

Ruptured CCJ RAVF with upward drainage. (A) CT showing subarachnoid and cisterna magna hemorrhage. (B) Lateral view (upper panel) and anterior posterior view (below panel) DSA of the VA showing an RAVF (asterisks) fed by the C2 and C3 radicular arteries (arrows) and with upward venous drainage (arrowhead in below panel). AVF, arteriovenous fistula; C2 and C3, second and third cervical vertebrae; CCJ, craniocervical junction; CT, computed tomography; DSA, digital subtracted angiography; RAVF, radicular AVF; VA, vertebral artery.

Figure 11

Incomplete EVT in a high cervical CCJ RAVF. (A) DSA of the left VA showing that the ASA supplied the AVF (asterisk). (B) DSA of the right VA showing that the AVF (asterisk) was fed by a brainstem perforating branch of the VA (arrow with number 1), the C2 (arrow with number 2) and C1 (arrow with number 3) radicular arteries, and the arrowhead indicates the draining vein. (C) Selective angiography of the brainstem perforating branch of the VA (arrow with number 1 in B) showing it to supply a part of the AVF. (D) Selective angiography of the C2 radicular artery (arrow with number 2) showing it to supply a part of the AVF. (E) After casting Onyx via two feeding arteries (numbers 1 and 2 in B), DSA of the left VA showing that the AVF was supplied by the C1 radicular artery (number 3 with arrow), confirming RAVF presentation. (F) DSA of the left VA showing that the VA was completely occluded by coiling, and the AVF could not be seen. (G) DSA of the right VA showing a part of the AVF (asterisk) was left. (H) Post-EVT CT reconstruction showing casting Onyx (ellipse), indicating the location of the RAVF. ASA, anterior spinal artery; AVF, arteriovenous fistula; C1-2, first and second cervical vertebrae; CCJ, craniocervical junction; CT, computed tomography; DSA, digital subtracted angiography; EVT, endovascular treatment; L, left; R, right; RAVF, radicular AVF; VA, vertebral artery.

Figure 12

Complete EVT in a CCJ DAVF with a single feeding artery. (A) CT showing subarachnoid hemorrhage and fourth ventricle hemorrhage. (B) CTA showing multiple dilated abnormal veins (arrowheads). (C) Arterial phase DSA of the right VA showing a CCJ DAVF (asterisk) fed by the C1 radicular artery. The drainage went upward into the intracranial vein (arrowhead with number 1) and downward into the perimedullary vein (arrowhead with number 2). (D) Venous phase DSA of the lateral view showing drainage into the deep jugular vein (arrowhead with number 3). (E) Selective angiography of the microcatheter via the C1 radicular artery showing that the fistula was a DAVF (asterisk), and the microcatheter was obtained in the wedge position to perform Onyx casting. (F) Postoperative DSA showing that the DAVF was obliterated completely. C1, first cervical vertebrae; CCJ, craniocervical junction; CT, computed tomography; CTA, CT angiography; DAVF, dural arteriovenous fistula; DSA, digital subtracted angiography; EVT, endovascular treatment; R, right; VA, vertebral artery.

Figure 13

Open surgery in a CCJ PAVF. (A) CT showing subarachnoid hemorrhage and fourth ventricle hemorrhage. (B) Arterial phase DSA of the right VA showing a CCJ PAVF (asterisk) fed by the C2 radicular artery. (C,D) Late arterial phase DSA of the anterior posterior view (C) and lateral view (D) via a microcatheter showing the angioarchitecture of the PAVF. The feeding artery was the C2 radiculomedullary artery, there was aneurysm dilatation (arrows) in the fistula, and the draining veins included the upward and downward ASV and LSV. (E) Intraoperative image showing aneurysm dilatation (arrow) on the dorsal surface of the spinal cord, and the feeding artery was clipped. (F) Postoperative DSA showing that the PAVF was obliterated. ASV, anterior spinal vein; C2, second cervical vertebra; CCJ, craniocervical junction; CT, computed tomography; DSA, digital subtracted angiography; LSV, lateral spinal vein; PAVF, perimedullary arteriovenous fistula; R, right; VA, vertebral artery.