Abstract
BACKGROUND
Manifestations of craniocervical junction (CCJ) arteriovenous fistulas (AVFs) include bleeding and congestive myelopathy. CCJ AVFs are classified as epidural, dural, radicular, and perimedullary. On diagnostic imaging, differentiation between dural and radicular AVFs is difficult because of the shortness of the feeding artery from the vertebral artery dural ring. Herein, the authors investigated the feeding artery of these AVFs.
OBSERVATIONS
Angiographic findings were described for 11 cases of CCJ AVFs (perimedullary, n = 1; radicular, n = 4; dural, n = 4; epidural 2), and direct surgery was performed in 8 patients (perimedullary, n = 1; radicular, n = 3, dural; n = 4). It is important to determine whether the posterior spinal artery branches have an epidural or intradural origin, and 2 cases (25%) of postoperative complications (brainstem ischemia, subarachnoid bleeding) were observed. In direct surgery, perimedullary AVFs must be treated just before the shunt point, and it is important to treat only the refluxing bridging veins in dural AVFs.
LESSONS
CCJ AVF requires classification of shunt points and understanding of vascular anatomy, including variations of posterior spinal artery.
Keywords: craniocervical junction, arteriovenous fistula, venous congestive myelopathy, subarachnoid hemorrhage, posterior spinal artery
Abbreviations: ASA = anterior spinal artery, AVF = arteriovenous fistula, CCJ = craniocervical junction, MIP = maximum intensity projection, PSA = posterior spinal artery, SAH = subarachnoid hemorrhage, VA = vertebral artery, VCM = venous congestive myelopathy, WFNS = World Federation of Neurosurgical Societies.
Arteriovenous fistulas (AVFs) at the craniocervical junction (CCJ) can cause subarachnoid hemorrhage (SAH), venous congestive myelopathy (VCM), and dizziness.1 Kinouchi et al. focused on the draining veins and reported that blood flows cranially in patients with SAH, while in patients with VCM, it flows caudally.2 A report from a multicenter study in Japan classified CCJ AVF shunt points into epidural, dural, radicular, and perimedullary types.3 However, there have been no detailed reports on the feeding arteries of the V3–V4 segments of the vertebral artery (VA).
Herein, we report on the 11 cases of CCJ AVFs that we have experienced, categorizing the vascular imaging findings on anatomical examination of the feeding artery and treatment methods based on the findings of direct surgery in 8 cases.
Study Description
The case group consisted of 11 consecutive cases of CCJ AVFs flowing from the VA V3–V4 segment, excluding complex types that also received feeding from the VA V2 segment and the internal and external carotid arteries. Patient age and sex, onset, neuroradiological diagnosis (shunt point, feeding artery, draining vein), and treatment method of 11 cases are shown Table 1. The onset of symptoms was SAH in 4 cases, VCM in 4 cases, medullary infarction (syrinx) in 1 case, and dizziness in 2 cases. The AVF types were epidural in 2 cases, dural in 4 cases, radicular in 4 cases, and perimedullary in 1 case. The 2 patients with dizziness had epidural AVFs, and all 4 patients with SAH onset had radicular AVFs. All 4 cases of SAH were mild cases (World Federation of Neurosurgical Societies [WFNS] grade I or II).4 The feeding artery involved the branches (muscular, somatic) in the VA V3 segment in one of the epidural AVFs (case 8; Fig. 1A) and the anterior spinal artery (ASA) and posterior spinal artery (PSA) with vaso corona in the patient with a perimedullary AVF (case 1; Fig. 1B and C). Radicular (Fig. 2) and dural (Fig. 3) AVFs were located near the VA dural ring between V3 and V4 segment, and were unclear on angiography and slab maximum intensity projection (MIP) images.
TABLE 1.
Clinical summary of 11 cases of AVFs at the CCJ
| Case No. | Age (yrs)/Sex | Onset (WFNS grade) | Shunt Point | Feeder | Drainer | Surgery | IO PSA Findings | Complication |
|---|---|---|---|---|---|---|---|---|
| 1 | 69/M | VCM | Perimedullary | Lt PSA, rt ASA | ASV | Yes | ID | BSI |
| 2 | 72/M | VCM | Dural | Rt unknown, PMA | ASV | Yes | ED, anastomosis | SAH (POD 10) |
| 3 | 53/F | SAH (II) | Radicular | Rt PSA | AMV | Yes | ED | No |
| 4 | 58/M | Syrinx | Dural | Lt PSA | AMV | Yes | ED | No |
| 5 | 66/F | SAH (II) | Radicular | Rt PSA | AMV | Yes | ID | No |
| 6 | 78/M | SAH (II) | Radicular | Rt PSA | AMV | Yes | ED | No |
| 7 | 71/M | VCM | Dural | Rt unknown, PMA | ASV | Yes | ED, anastomosis | No |
| 8 | 74/M | Vertigo | Epidural | LtV3 | SOCS | No | ||
| 9 | 69/M | Vertigo | Epidural | LtV3 | SOCS | No | ||
| 10 | 44/M | VCM | Dural | Rt unknown, PMA | ASV | Yes | ED, anastomosis | No |
| 11 | 61/M | SAH (I) | Radicular | Lt PSA | AMV | No |
AMV = anterior medullary vein; ASV = anterior spinal vein; BSI = brainstem infarction; ED = extradural; ID = intradural; POD = postoperative day; SOCS = suboccipital cavernous sinus.
FIG. 1.
A:Case 8. Angiogram showing an epidural AVF. A feeder is observed from the somatic and muscular branches (white arrows) of the VAV3 segment, and drainage is observed in the suboccipital cavernous sinus (double white arrows). Anxtradural PSA (yellow arrow) and posterior inferior cerebellar artery anastomosis (asterisk) are shown. B: Case 1. Sagittal MR image showing intramedullary T2 hyperintensity. C: Angiogram of a perimedullary AVF. A right-sided ASA (red arrow) and left-sided intradural PSA (white arrow) with vaso corona feeders are observed, and a drainage was observed to the anterior spinal vein (double arrows). D:MR images obtained 3 months after surgery, revealing a left brainstem infarction (yellow asterisks).
FIG. 2.
A–D:Case 5. CT scan showing SAH in the foramen magnum (A). Angiogram revealing a radicular AVF with the PSA (white arrow) as a feeder (B). Three-dimensional slab MIP image showing findings suggestive of an intradural PSA (black arrow; C). Intraoperative findings confirmed intradural PSA (black arrow; D). E–H: Case 6. CT scan revealing SAH in the prepontine cistern (E). Angiogram revealing a radicular AVF with the PSA (white arrow) as a feeder, and a upward-draining vein (double white arrows; F). Three-dimensional MIP image showing an an extradural PSA (yellow arrow) branching from the proximal side of the dural ring (white arrowhead; G). Intraoperative findings revealing an AVF from the extradural PSA (yellow arrow), with a draining vein (double white arrows; H).
FIG. 3.
A–D: Case 2. Sagittal MR image showing intramedullary T2 hyperintensity after cervical laminoplasty (pound sign; A). Angiogram revealing a dural AVF with the PMA (white arrow) as a feeder, and a downward-draining vein (double white arrows; B). Three-dimensional slab MIP image showing an extradural PSA (yellow arrow) branching from the proximal side of the dural ring (black arrowhead; C). In addition, PSA and PICA anastomosis is observed (asterisk). On the 10th day after surgery, the patient was comatose and presented with obstructive hydrocephalus due to massive SAH in the posterior fossa (D). E–H:Case 7. Sagittal MR image showng intramedullary T2 hyperintensity (E). Angiogram revealing a dural AVF with the PMA (white arrow) as a feeder, and an anterior spinal vein (double white arrow) as the drainer; PSA (yellow arrow) and PICA anastomosis (asterisk) is also observed (F). Intraoperative findings revealed extradural PSA (yellow arrow) and a bridging vein (double asterisks; G). During surgery, the extradural PSA (yellow arrow) was confirmed using indocyanine green videoangiography, and a temporary clip was used to visualize the lateral spinal artery from the PICA anastomosis (white asterisks; H). The temporary clip on the PSA was removed, and permanent clipping was performed on the bridging vein (double asterisks).
Direct surgery was performed in 8 patients (perimedullary in 1, radicular Fig. 2] in 3, and dural [Fig. 3] in 4), and the origin of the feeding artery and PSA were documented based on intraoperative findings (Table 1). Two patients in our early stages experienced complications of postoperative brainstem infarction and delayed SAH. The first complication, brainstem infarction, was an intradural PSA type and was determined to be caused by an occlusion just before the vaso corona (case 1; Fig. 1D). The feeding arteries of the perimedullar type were ASA and PSA with a vaso corona of intradural origin. The second complication (case 2; Fig. 3D), delayed massive SAH, was of the extradural PSA type and was determined to be caused by the formation and rupture of an incompletely coagulated pseudoaneurysm.
In case 5, feeder was a radicular-type feeding artery with an intradural origin (PSA) (Fig. 2B–D). In case 6, the feeder type was also radicular but with an extradural origin and had no anastomosis with the posterior inferior cerebellar artery (PICA) (Fig. 2F–H). Radicular AVFs presenting with SAH had favorable treatment outcomes with intradural occlusion regardless of whether the PSA was involved. In contrast dural-type AVFs were fed by the posterior meningeal artery (PMA). In these 4 cases, the PSA was extradural in origin and unrelated to the AVF. Rather, the AVF drained retrogradely into a bridging vein (case 7; Fig. 3E–H). Dural AVFs with VCM were not associated with a PSA, and successful treatment was achieved by clipping only reflux bridging vein into the dura.
Informed Consent
The necessary informed consent was obtained in this study.
Discussion
Observations
Neuroradiological Diagnosis
Based on the angioarchitecture of AVFs at the CCJ, shunt points were classified as epidural, dural, radicular, and perimedullary.3 Although it is relatively easy to localize epidural (Fig. 1A) and perimedullary (Fig. 1C) AVFs using angiography, the differential diagnosis between dural and radicular AVFs is difficult. The reason for the difficulty in diagnosis is the short distance between the VA and the feeding artery around the dural ring. Based on the onset pattern, SAH can be differentiated from radicular AVF (Fig. 2), while VCM can be differentiated from dural AVFs (Fig. 3).
Branches of the VA V3 Segment and Variations of the PSA
According to autopsy reports, the branches from the VA V3 segment are muscular and osseous or somatic branches, but no radiculomedullary artery is present.5 The PSA branches from near the VA dural ring and usually runs to the descending lateral spinal artery. The PSA has two origins: extradural and intradural. Extradural PSAs form an anastomosis with the posterior inferior cerebellar artery (PICA) within the dura.6 Seçkin et al. reported that an intradural PSA was present in 56% of individuals, extradural PSA in 41%, and extradural PICA in 3%.7 Branching from the VA V3 segment and PSA variation are the most important anatomical markers for the treatment of CCJ AVFs (Fig. 4). In this study, PICA anastomosis was not observed on angiography in patients with SAH, even in cases with extradural PSAs. Therefore, in cases of radicular AVFs presenting with SAH, treatment is possible by occluding the feeder even if the PSA is of intradural or extradural origin.
FIG. 4.
Illustrations. A: A PSA of intradural origin. The arrow indicates the dural ring. B: A PSA of extradural origin. The asterisk indicates PICA anastomosis, and the double asterisks denote the anterior spinal artery. C:A PICA of extradural origin.
Conservative Treatment for CCJ AVFs
In this series, conservative treatment was performed in 3 cases. Two cases were epidural AVFs caused by dizziness, and the patients’ symptoms improved with intravenous treatment. The other patient had SAH (WFNS grade I), but the AVF was spontaneously occluded at the time of angiography.
Surgical Treatment for CCJ AVFs
In this series, direct surgery was performed in 8 cases of CCJ AVFs. Epidural AVFs are indicated for an endovascular approach because the presence of a suboccipital cavernous sinus makes the surgical approach difficult. Furthermore, radicular AVFs that present with SAH are also expected to be good candidates for a direct or endovascular approach. Perimedullary AVFs, where the ASA or PSA supplies blood to the brainstem, can present serious ischemic complications, so direct surgery just before the shunt point is safe.8 The classification by Kiyosue et al. is useful for determining intradural venous return in CCJ AVFs.9 Furthermore, in the case of dural AVFs, the procedure is performed through the draining bridging vein, so care must be taken to avoid unnecessary coagulation and cutting the extradural PSA.10 We believe that the 2 cases of complications (25%) we experienced were due to unnecessary coagulated occlusion of the PSA, which was unrelated to the vascular structure of the AVF.
Lessons
The onset patterns of CCJ AVFs are diverse, and the shunt points also vary. Therefore, it is important to ensure that occlusion is performed immediately before the shunt point in the perimedullary type, and that only the outflow vein is occluded in the dural type.
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: Uchikado, Ando, Ohkubo, Hattori, Morioka. Acquisition of data: Uchikado, Ando, Ohkubo. Analysis and interpretation of data: Uchikado, Ando, Ohkubo. Drafting the article: Uchikado, Ando, Ohkubo, Morioka. Critically revising the article: Uchikado, Ohkubo. Reviewed submitted version of manuscript: Uchikado, Makizono, Ohkubo. Approved the final version of the manuscript on behalf of all authors: Uchikado. Statistical analysis: Uchikado. Administrative/technical/material support: Uchikado, Ohkubo, Nakamura. Study supervision: Uchikado, Hattori.
Correspondence
Hisaaki Uchikado: Uchikado NeuroSpine Clinic, Hakata, Fukuoka, Japan. uchikado@me.com.
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