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Review
Dural arteriovenous fistulas at the craniocervical junction: a systematic review
  1. Jingjing Zhao1,
  2. Feng Xu1,
  3. Jinma Ren2,
  4. Sunil Manjila3,
  5. Nicholas C Bambakidis3
  1. 1Department of Neurosurgery, Huashan Hospital, Shanghai Medical School, Fudan University, Shanghai, China
  2. 2Center for Outcomes Research, University of Illinois College of Medicine at Peoria, Illinois, USA
  3. 3Department of Neurological Surgery, The Neurological Institute, University Hospitals Case Medical Center, Cleveland, Ohio, USA
  1. Correspondence to Dr Nicholas C Bambakidis, Department of Neurological Surgery, University Hospitals Case Medical Center, 11100 Euclid Avenue, Cleveland, OH 44106, USA; Nicholas.Bambakidis2{at}UHhospitals.org

Abstract

Background Dural arteriovenous fistulas (DAVFs) at the craniocervical junction are uncommon but clinically important abnormalities.

Objective To investigate the clinical characteristics of patients with DAVFs at the craniocervical junction and assess angiographic features associated with bleeding at presentation.

Methods We systematically reviewed the literature and searched PubMed and EMBASE for all relevant English language articles published between 1980 and 2014. The clinical presentation, angiographic characteristics, and treatment were assessed. The clinical differences between a subarachnoid hemorrhage (SAH) group and a non-SAH group were statistically examined.

Results Fifty-six patients were identified after a review of the literature (mean age 55.6 years; male to female ratio=3:1). Twenty-one patients (37.5%) presented with hemorrhage including SAH and posterior fossa hemorrhage. There was no significant difference in patient age, sex, or location of the DAVF between the SAH group and the non-SAH group. Intracranial venous drainage was significantly associated with SAH (p<0.001). The presence of a varix was significantly associated with SAH (p=0.001). Open surgery had a significantly higher efficacy of initial complete obliteration than embolization (100% vs 71.4%, p<0.01).

Conclusions DAVFs at the craniocervical junction are rare lesions, which often present with hemorrhage. Intracranial venous drainage and a venous varix are associated with increased risk of SAH. Surgical interruption of the feeding arteries or draining veins is an effective and reliable method for treating DAVFs at the craniocervical junction. Embolization is a feasible alternative to surgery in the treatment of selective DAVFs.

  • Fistula

https://doi.org/10.1136/neurintsurg-2015-011775

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    Introduction

    The craniocervical junction is a complex anatomical structure consisting of the brainstem and spinal cord, the lower cranial and upper spinal nerves, the vertebral artery and its branches, and the ligaments uniting the atlas, axis, and occipital bone.1–3 Dural arteriovenous fistulas (DAVFs) at the craniocervical junction are uncommon but clinically important abnormalities. In contrast to thoracolumbar DAVFs, these lesions have a wide presentation, including acute subarachnoid hemorrhage (SAH),4–12 myelopathy,13–23 brainstem dysfunction,24–26 radiculopathy,5 and cranial nerve palsy.23 Diagnosis of DAVFs at the craniocervical junction remains a challenge due to complex vascular anatomy with tiny and tortuous supplying vessels. The optimal treatment strategy for craniocervical junction DAVFs remains controversial because of their deep-seated locations and complicated supplying arteries and draining veins. In this study, we carried out a comprehensive literature review and investigated the clinical characteristics of patients with DAVFs at the craniocervical junction, including the clinical presentation, vascular supply and drainage, and treatment. We also assessed angiographic features associated with bleeding at presentation.

    Methods

    To investigate the clinical characteristics of patients with DAVFs at the craniocervical junction, we performed a literature review by searching PubMed and EMBASE for articles published between January 1980 and December 2014. The following keywords were used: “dural arteriovenous fistula”, “craniocervical junction”, “cervical spinal dural arteriovenous fistula”, or “spinal dural arteriovenous malformation”. Additional articles were found by searching the reference lists of relevant articles.

    DAVFs at the craniocervical junction were defined as an abnormal communication between a dural branch of a radicular artery and a radicular vein along the dural sleeve of the nerve root between the foramen magnum and C-2 level. Thus, articles on extradural, perimedullary arteriovenous fistulas, and intramedullary arteriovenous malformations were excluded. In addition, articles on DAVFs with no clear description of angiographic findings were excluded.27 Articles in languages other than English were also excluded.

    Two authors (JZ, FX) independently reviewed and extracted the following data on eligible patients: age, sex, location, clinical symptoms, vascular supply and drainage, presence of varices, treatment, and angiographic result. In cases of disagreement, consensus was reached through discussion with the senior author (NCB).

    The data were analyzed using SPSS for Windows, V.22.0 (SPSS Inc). The χ2 test and the Fisher exact test were used to compare categorical variables between the SAH and non-SAH groups and the treatment groups, and the two-sample t test was used to compare distributions of continuous variables. A p value <0.05 was considered to be statistically significant.

    Results

    Our systematic review disclosed 56 cases of DAVFs at the craniocervical junction reported in 26 articles. The characteristics of the patients are summarized in the table 1.

    View this table:
    Table 1

    Summary of reports in the English literature on dural arteriovenous fistulas at the craniocervical junction

    The mean age of presentation of patients with DAVFs at the craniocervical junction was 55.6 years (range 30–78 years). This group included 42 men (75%) and 14 women (25%). In 32/56 patients (57.1%), the fistula was located at the foramen magnum, in 14 patients (25%) at the C-1 level, in 4 patients (7.1%) at the C-2 level, in 4 patients (7.1%) at both foramen magnum and C-1 level, and in another 2 (3.6%) at both C-1 and C-2 levels. Twenty-one patients (37.5%) presented with SAH (n=20) and posterior fossa hemorrhage (n=1), 21 with myelopathy, four with brainstem dysfunction, two with cerebellar dysfunction, two with neck pain, one with headache, one with tinnitus and palsy of cranial nerve VI, and one with occipital neuralgia. In two cases, the DAVF was incidentally discovered. The remaining patient was asymptomatic.

    The mean age of patients at presentation was 56.1 years (range 36–78 years) in the SAH group, and 55.3 years (range 30–76 years) in the non-SAH group. Sixteen patients (76.2%) were men in the SAH group, and 26 (74.3%) in the non-SAH group. There was no significant difference in patient sex or location of the DAVF between the SAH group and the non-SAH group (table 2). In the SAH group, intracranial venous drainage occurred in 15 (71.4%) of 21 patients. The non-SAH group had nine DVAFs with intracranial venous drainage (25.7%). Intracranial venous drainage was significantly associated with SAH (p<0.001). A venous varix was present in 11/20 (55.0%) patients with SAH and in 4/32 (12.5%) patients in the non-SAH group. The presence of a varix was significantly associated with SAH (p=0.001).

    View this table:
    Table 2

    Summary of clinical characteristics in patients with DAVFs at the craniocervical junction

    Of 21 patients reported who received embolization, initial complete obliteration was achieved in 15 patients (71.4%). Various embolic materials were used, including coils (n=2), polyvinyl alcohol particles (n=4), glue (n=1), isobutyl 2-cyanoacrylate (IBCA) (n=2), n-butyl cyanoacrylate (n-BCA) (n=3), and Onyx liquid embolic (n=8). Further surgical treatment was performed to obliterate the DAVF in three patients, including two with unsuccessful embolization and one with recurrence after embolization of the vertebral artery. In 34 patients, the DAVF was treated with surgical ligation of the feeding artery or interruption of the draining vein, and complete angiographic obliteration was achieved in all these patients. In 31 of these patients, surgery was the primary treatment, and in three cases, surgery was performed after endovascular treatment had failed. One patient received cyber-knife treatment and three patients did not receive any treatment. Clearly, surgery was a more efficacious treatment than embolization (100% vs 71.4%, p<0.01).

    Discussion

    Clinical presentation

    Spinal DAVFs most commonly occur dorsally at the thoracolumbar junction in middle-aged men and usually present with progressive myelopathy caused by venous hypertension.20 Clinical symptoms include spastic paraparesis, pain, sensory deficits, and sphincter disturbance.10 In contrast, cervical DAVFs have a wide range of clinical presentations that include SAH,4–12 myelopathy,13–23 radiculopathy,5 and cranial nerve palsy,23 although representing only a minority of spinal DAVFs.

    As previous studies have shown, upper cervical DAVFs are more likely to present with hemorrhage.28 In the 56 previously reported cases of DAVF at the craniocervical junction, almost 37.5% of these patients presented with SAH. The mechanism underlying hemorrhagic presentation is still not entirely understood. It might be partly due to venous hypertension, or specific venous drainage patterns. Myelopathy also remains the main presenting symptom. Atypical presentations included brainstem/cerebellar dysfunction,12 ,22 ,24–26 ,29 radiculopathy,5 cranial nerve palsy,23 and occipital neuralgia.30 ,31 Brainstem dysfunction as the initial symptom has often been reported in intracranial DAVFs, but is rarely documented in craniocervical DAVFs. Kulwin et al24 suggested that the mechanism responsible for brainstem dysfunction might be related to be venous hypertension secondary to arterial pressure via the fistula, causing potentially reversible venous congestion. Occipital neuralgia is an extremely uncommon presentation of craniocervical DAVFs. Hashiguchi et al30 thought that edema around the intramedullary hemorrhage might affect the incoming sensory fibers within the dorsal root entry zone and cause occipital neuralgia.

    Arterial supply

    A precise understanding of vascular anatomy is required for correct interpretation of diagnostic studies and clinical evaluation and management of DAVFs at the craniocervical junction. The dura around the foramen magnum is supplied by the anterior and posterior meningeal branches of the vertebral artery, and the meningeal branches of the ascending pharyngeal and occipital arteries.1–3 The posterior meningeal artery arises from the posterior superior surface of the vertebral artery as it courses around the lateral mass of the atlas and ascends in the dura near the falx cerebelli (figure 1). The ascending pharyngeal branch of the external carotid artery sends branches through the hypoglossal canal and jugular foramen to the dura above the foramen magnum. The meningeal branch of the occipital artery divides into one branch which courses posterosuperiorly to join the branches of the posterior meningeal artery that supplies the dura mater in the posterior part of the posterior fossa, and another branch that courses anterolaterally and joins the meningeal branches of the ascending pharyngeal artery. The extradural part of the vertebral artery gives rise to various branches supplying muscular, meningeal, medullary, and radicular structures (figure 2).32 However, radicular or medullary branches are uncommonly identified in any V3 segment of the vertebral artery in the cadaveric studies.

    Figure 1
    Figure 1

    Schematic illustration showing the blood supply of the dura around the foramen magnum in a posterior view. The dura around the foramen magnum is supplied by the posterior meningeal branches (Post. Men. A.) of the vertebral artery (Vert. A.), and the meningeal branches of the ascending pharyngeal (Ascend. Pharyngeal A.) and occipital arteries (Occip. A.).

    Figure 2
    Figure 2

    Schematic illustration showing the types of branches seen arising from the vertebral artery (VA) in a posterior view. Note the radicular, medullary, and meningeal branches of the VA. (Reproduced with permission from the American Association of Neurological Surgeons: Tubbs et al.32)

    All DAVFs in the cervical levels, except for two, were fed by a reticular network of radiculomeningeal arteries mainly originating from an enlarged radicular artery arising at the same spinal level. In one patient, DAVF at the C-1 level was fed by the radiculomeningeal branch of the C-3 radicular artery. In another patient, DAVF at the C-2 level was fed by the radiculomeningeal branch of the C-3 radicular artery. Most DAVFs at the foramen magnum were supplied by the meningeal branches of the vertebral artery, or the occipital artery and ascending pharyngeal artery.

    Venous drainage

    Anatomically, the venous system of the spinal cord is composed of two radially arranged vascular networks.33 Sulcal veins lie in the anterior median fissure and drain into anterior median spinal veins. Radial veins lie in the dorsal and anterolateral portions of the spinal cord and drain into the coronal venous plexus. Both anterior median spinal veins and the coronal venous plexus drained via medullary veins through the dura to the epidural venous plexus (figure 3).

    Figure 3
    Figure 3

    Venous anatomy of the spinal cord. Radial veins drain the spinal cord to the coronal venous plexus. (Modified from Kim et al.33)

    DAVFs at the craniocervical junction usually drain into the medullary vein, the coronal venous plexus, intracranial venous system, or less likely into the epidural and paravertebral veins. A medullary vein is usually the venous outflow from the fistula and drains arterialized blood through the valveless pial coronal venous plexus into the cord via radial veins, resulting in venous congestion and myelopathy (figures 4 and 5).13 ,33 Sometimes, the drainage may occur superiorly into the intracranial venous system, including cavernous sinus, inferior petrosal sinus, confluence of sinus, or cortical vein. Intracranial drainage causes relatively fast venous flow, and increased hemodynamic stress may lead to varix formation and result in SAH.34 Aviv et al28 showed that either the presence of a venous varix or superiorly directed intracranial venous drainage was significantly associated with a presentation of SAH in patients with cervical DAVFs. Kai et al34 showed that DAVFs at the cervicomedullary junction that manifest an ascending venous drainage into the intracranial sinus present an increased risk for SAH. Consistent with these studies, our systematic review showed that both intracranial venous drainage and a venous varix were associated with bleeding. In cases of epidural venous drainage, an extramedullary mass effect may aggravate the myelopathic symptoms.

    Figure 4
    Figure 4

    Axial illustration of dural arteriovenous fistulas demonstrating an abnormal radicular feeding artery along the nerve root. (Modified from Kim et al.33)

    Figure 5
    Figure 5

    Illustration of the posterior view demonstrating the dilatation of the coronal venous plexus. (Modified from Kim et al.33)

    Imaging studies

    In patients who presented with SAH, CT scanning showed that clots were predominantly located in the posterior fossa with reflux in the fourth ventricle. The remaining locations included foramen magnum, upper cervical spinal canal, basal cisterns, tentorial and perimesencephalic region. CT angiography can help identify the fistula and delineate the anatomy.35 In patients with myelopathy, MR imaging revealed cord swelling and extensive intramedullary hyperintensity on T2-weighted images with contrast enhancement. Perimedullary flow-related signal voids indicated abnormally dilated veins on the surface of the cervical spinal cord. MR angiography might be helpful in the diagnosis of DAVFs at the craniocervical junction with perimedullary drainage.21

    Digital subtraction angiography remains the ‘gold standard’ for the diagnosis and evaluation of spinal DAVFs. It can identify precisely the site of a fistula and delineate the anatomy. However, sometimes diagnostic angiography of DAVFs at the craniocervical junction may be challenging owing to complex anatomy with very small or extremely tortuous feeding arteries.1 In addition, failure to identify the fistula may be due to spontaneous obliteration/thrombosis, mass effect/compression, or inadequate studies.4 In two of four patients with SAH for whom initial cerebral angiography was negative, the right vertebral artery was not selectively catheterized because of distal retrograde filling of the right vertebral artery and the right posterior inferior cerebellar artery during left vertebral angiography. In another patient, the right subclavian artery was injected instead of a selective right vertebral artery angiogram because of its tortuous anatomy. Thus, it is necessary to perform six-vessel angiography, including bilateral internal carotid arteries, external carotid arteries, and vertebral arteries, in the search for a cause of SAH if a craniocervical junction DAVF is suspected.

    Treatment

    It remains controversial whether DVAFs at the craniocervical junction should be treated by direct surgery or endovascular embolization. Although embolization of these DAVFs with polyvinyl alcohol particles, IBCA and n-BCA has been initially described,15 ,17 ,22 ,23 ,36 incomplete occlusion and recanalization after embolization represent two major limitations. Recent advances in embolic materials and embolization techniques have allowed embolization of craniocervical junction DAVFs to become an alternative to surgery. Onyx, a new liquid embolic agent, has been increasingly used to treat spinal DAVFs. It allows for more prolonged and controlled injections. Proper reflux helps the continuous penetration of Onyx into the venous portion to achieve satisfactory embolization compared with n-BCA. Additionally, to achieve complete obliteration, the microcatheter tip should be positioned at, or immediately adjacent to, the fistula. If the microcatheter cannot be navigated to a position close to the site of the fistula or improper reflux is not allowed, balloon-augmented Onyx embolization is helpful in the treatment of these cases. Liang et al11 reported on five patients with DAVF at the foramen magnum undergoing transarterial embolization with Onyx system. In three patients, a balloon-augmented technique was used to assist embolization. Complete obliteration was achieved in all these patients and the results remained stable in all patients on follow-up angiograms. However, this is a small series of cases that focus on the use of Onyx to treat these challenging lesions. In addition, there may be an increase in the risk of vessel rupture, particularly in DAVFs with very small and extremely tortuous feeding arteries. Furthermore, misembolization of the dangerous anastomoses or normal vessels such as vertebral artery and anterior/posterior spinal arteries may result in neurological complications. Thus, surgery is considered the most effective and reliable method by ligation of the feeding artery or draining vein.7 Moreover, no cases of recurrence have been reported after surgical interruption.

    Conclusions

    The age distribution of patients with DAVFs at the craniocervical junction is similar to that of patients with DAVFs in the thoracolumbar region. There is a male predominance, with a ratio of 3:1. DVAFs at the craniocervical junction have a wide presentation, including SAH, myelopathy, brainstem/cerebellar dysfunction, radiculopathy, cranial nerve palsy, and occipital neuralgia. Intracranial venous drainage and a venous varix are associated with increased risk of SAH. A thorough evaluation with six-vessel cerebral angiography, including bilateral internal carotid arteries, external carotid arteries, and vertebral arteries, should be performed to detect DAVFs at the craniocervical junction. Surgical interruption of the feeding arteries or draining veins is an effective and reliable method. Onyx embolization is a feasible and safe alternative to surgery in the treatment of selective DAVF at the craniocervical junction.

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    Footnotes

    • JZ and FX contributed equally.

    • Contributors Conception and design: NCB. Acquisition of data: JZ, FX. Drafting the article: JZ, FX. Critically revising the article: JZ, FX, NCB. Reviewed submitted version of manuscript: NCB. Approved the final version of the manuscript on behalf of all authors: NCB. Statistical analysis: JR. Administrative/technical/material support: SM.

    • Competing interests None declared.

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