High cervical arteriovenous fistulas fed by dural and spinal arteries and draining into a single medullary vein

Report of 3 cases

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Object

The authors previously reported a case of complex arteriovenous fistula (AVF) at C-1 with multiple dural and spinal feeders that were linked with a common medullary venous channel. The purpose of the present study was to collect similar cases and analyze their angioarchitecture to gain a better understanding of this malformation.

Methods

Three such cases, affecting 2 males and 1 female in their 60s who had presented with hematomyelia (2) or progressive myelopathy (1), were treated surgically, and the operative findings from all 3 cases were compared using digital subtraction angiography (DSA) to determine the angioarchitecture.

Results

The C-1 and C-2 radicular arteries and anterior and posterior spinal arteries supplied feeders to a single medullary draining vein in various combinations and via various routes. The drainage veins ran along the affected ventral nerve roots and lay ventral to the spinal cord. The sites of shunting to the vein were multiple: dural, along the ventral nerve root in the subarachnoid space, and on the spinal cord, showing a vascular structure typical of dural AVF, that is, a direct arteriovenous shunt near the spinal root sleeve fed by one or more dural arteries and ending in a single draining vein, except for intradural shunts fed by feeders from the spinal arteries. In 2 cases with hemorrhagic onset the drainer flowed rostrally, and in 1 case associated with congestive myelopathy the drainer flowed both rostrally and caudally. Preoperative determination of the shunt sites and feeding arteries was difficult because of complex recruitment of the feeders and multiple shunt sites. The angioarchitecture in these cases was clarified postoperatively by meticulous comparison of the DSA images and operative video. Direct surgical intervention led to a favorable outcome in all 3 cases.

Conclusions

A high cervical complex AVF has unique angioarchitectural characteristics different from those seen in the other spinal regions.

Abbreviations used in this paper:AVF = arteriovenous fistula; AVM = arteriovenous malformation; DSA = digital subtraction angiography; MMT = manual muscle testing.

Abstract

Object

The authors previously reported a case of complex arteriovenous fistula (AVF) at C-1 with multiple dural and spinal feeders that were linked with a common medullary venous channel. The purpose of the present study was to collect similar cases and analyze their angioarchitecture to gain a better understanding of this malformation.

Methods

Three such cases, affecting 2 males and 1 female in their 60s who had presented with hematomyelia (2) or progressive myelopathy (1), were treated surgically, and the operative findings from all 3 cases were compared using digital subtraction angiography (DSA) to determine the angioarchitecture.

Results

The C-1 and C-2 radicular arteries and anterior and posterior spinal arteries supplied feeders to a single medullary draining vein in various combinations and via various routes. The drainage veins ran along the affected ventral nerve roots and lay ventral to the spinal cord. The sites of shunting to the vein were multiple: dural, along the ventral nerve root in the subarachnoid space, and on the spinal cord, showing a vascular structure typical of dural AVF, that is, a direct arteriovenous shunt near the spinal root sleeve fed by one or more dural arteries and ending in a single draining vein, except for intradural shunts fed by feeders from the spinal arteries. In 2 cases with hemorrhagic onset the drainer flowed rostrally, and in 1 case associated with congestive myelopathy the drainer flowed both rostrally and caudally. Preoperative determination of the shunt sites and feeding arteries was difficult because of complex recruitment of the feeders and multiple shunt sites. The angioarchitecture in these cases was clarified postoperatively by meticulous comparison of the DSA images and operative video. Direct surgical intervention led to a favorable outcome in all 3 cases.

Conclusions

A high cervical complex AVF has unique angioarchitectural characteristics different from those seen in the other spinal regions.

Spinal arteriovenous malformations are rare, and the most common type is dural arteriovenous fistula (AVF).18 A spinal dural AVF has an arteriovenous shunt located within the dura mater close to the dorsal nerve root, which is fed by the radiculomeningeal, not the spinal, arteries and drains through a single radicular vein.5,12,14,21,22,24 It occurs predominantly in the thoracolumbar area and rarely in the cervical spine where the craniocervical junction is the most commonly affected site.2,16,18 Recently, it has become recognized that a dural AVF at the craniovertebral junction has unique clinical and angiographic characteristics different from those of an AVF located in the thoracolumbar region.15 We recently described a case of a high cervical complex AVF fed by both dural and spinal arteries and draining into a single medullary vein.27 At that time we emphasized the need to collect similar cases to gain a better understanding of this type of malformation. Here we report some new cases, focusing on their angioarchitectural features and etiology.

Case Reports

Case 1

History and Examination

A 63-year-old man was admitted to a local hospital for examination of progressive weakness of the extremities and a spastic gait. Disordered fine movement of the bilateral fingers and hyperreflexia below the C-5 level were found on neurological examination. Since a high-intensity area extending from the medulla oblongata to C-4 was demonstrated on T2-weighted MR images (Fig. 1A), the patient was transferred to one of our hospitals for investigation of the lesion. Detailed angiographic examination revealed an AVF at the left C-2 level, which was supplied from the left C-1 and C-2 radicular arteries and anterior spinal artery and drained into the radiculomedullary vein, which had a small varix and merged with the anterior spinal vein flowing both rostrally and caudally (Fig. 1B). We believed the hyperintense lesion evident on MRI was caused by venous hypertension due to the AVF. Transarterial embolization with liquid embolic agents seemed risky because of possible migration of the agents to the anterior spinal artery. Therefore, surgical treatment was planned.

Fig. 1.
Fig. 1.

A: Sagittal T2-weighted MR image showing a high-intensity area extending from the medulla oblongata to C-4. B: Left vertebral angiogram, early (upper) and late (lower) arterial phases, posteroanterior oblique view, showing a left C-2 AVF supplied from the C-1 radicular (white arrowheads), C-2 radicular (small black arrowheads), and anterior spinal (large black arrowheads) arteries and draining to the radiculomedullary vein (clear arrowheads), which had a small varix (black arrow) and merged with the anterior spinal vein flowing both rostrally and caudally. White arrow indicates shunt point.

Operation

A small suboccipital craniectomy and C-1 laminectomy were performed, and the dentate ligament and C-2 dorsal roots were sectioned on the left. The feeders from the anterior spinal and C-1 radicular arteries in or along the C-2 ventral roots, the shunt point around the ventral root sleeve, and the draining vein with varix were identified (Fig. 2A–C). Some feeding arteries on the dura were coagulated, and a temporary clip was applied to the draining vein. Intraoperative bilateral vertebral angiography using a mobile fluoroscope with digital subtraction angiography (DSA) function did not demonstrate any abnormal shunts. Therefore, the feeders and draining vein were coagulated and cut (Fig. 2D).

Fig. 2.
Fig. 2.

Intraoperative microscopy image (A, low-power field) and neighboring fields near the C-2 AVF (B and C, high-power field) showing a feeder from the C-1 radicular artery (C1R: clear circles in B and C), draining vein (DV) with varix (Va), and feeders probably from the anterior spinal artery in or along the C-2 ventral roots (asterisks). Dentate ligament (DL) and C-2 dorsal roots were sectioned in B and C. Schematic (D) showing angioarchitecture and blood vessels disconnected during surgery (solid and dotted blue lines [dotted lines indicate features originally hidden under the roots, spinal cord, and so forth]). C2 = C-2 spinal nerve roots; SAN = spinal accessory nerve; SC = spinal cord; ** = dural feeders. Copyright Kiyoshi Onda. Published with permission.

Postoperative Course

The patient's neurological condition transiently worsened, especially with regard to urinary function and gait. However, he recovered a few weeks after surgery, and the high-intensity area on T2-weighted images disappeared. No residual AVF was found on conventional angiography after surgery (Fig. 3), and the patient was ambulatory on discharge from the hospital. At about 6 years after the operation, the patient's motor function was almost the same as his preoperative status, that is, manual muscle testing (MMT) Grade 4+ to 5.

Fig. 3.
Fig. 3.

Postoperative left vertebral artery angiogram, posteroanterior oblique view, showing disappearance of the AVF.

Case 2

History and Examination

A 60-year-old man was transferred to one of our hospitals by ambulance because of a left occipital headache and left-sided muscle weakness. Neurological examination demonstrated dysarthria, dysphagia, left sensory impairment, and left flaccid hemiparesis. Hemorrhage in the medulla oblongata extending to C-2 and abnormal vasculature at the craniocervical junction were demonstrated on MRI (Fig. 4A and B). One month later, the patient became ambulatory and was able to eat and drink. Bilateral vertebral and common carotid artery angiography demonstrated an AVF at the left C-1 fed by the left C-2 radicular, C-1 radicular, and posterior spinal arteries and draining rostrally into the right petrosal vein and left jugular bulb via the transverse pontine vein (Fig. 4C).

Fig. 4.
Fig. 4.

A: Sagittal T2-weighted MR image showing a hematoma extending from the medulla oblongata to C-2. B: Magnetic resonance angiogram showing an abnormal vessel at the craniocervical junction (arrow). C: Left vertebral artery angiogram, posteroanterior view, showing the left C-1 AVF fed by the C-2 radicular (large black arrowheads), C-1 radicular (white arrowheads), and posterior spinal (small black arrowheads) arteries and draining rostrally into the right petrosal vein and left jugular bulb via the transverse pontine vein (clear arrowheads). White arrow indicates shunt point.

Operation

Surgical treatment of the AVF was performed 2 months after its onset. A small left suboccipital craniectomy and C-1 hemilaminectomy were performed, the dentate ligament was cut, and intradural feeders and the drainer were traced carefully (Fig. 5A–G). A branch of the spinal accessory nerve merged into the C-1 ventral root, which was divided as shown in Fig. 5A and B. There were several C-1 ventral rootlets, but the C-1 dorsal root was absent. The posterior spinal artery supplied a few feeding arteries to the draining vein, one of which merged with the vein around the ventral root sleeve, while the others merged near the spinal cord; a branch probably originating from the C-2 radicular artery also fed the AVF. The intradural feeders were coagulated and cut just before the shunt, and the drainage vein was cauterized and sectioned at the intradural entry site (Fig. 5H). Intraoperative left vertebral artery angiography revealed disappearance of the shunt.

Fig. 5.
Fig. 5.

Intraoperative microscopy images (A and B, low-power field; C–G, high-power field) showing feeders from the posterior spinal artery (single asterisks) and C-2 radicular (black arrowheads) artery, the draining vein (DV), and the dural entry site of the drainer after disconnection (white arrow). A branch of the spinal accessory nerve that had merged into the C-1 ventral root was divided (A and B). There were several C-1 ventral rootlets, but the C-1 dorsal root was absent (B). The posterior spinal artery supplied a few feeding arteries (black arrows) to the draining vein, one of which merged with the vein around the ventral root sleeve, while the others merged near the spinal cord; a branch probably originating from the C-2 radicular artery also fed the AVF (black arrowheads). The dentate ligament is cut in the figures. H: Schematic showing angioarchitecture and blood vessels disconnected during surgery (blue lines). C1 = C-1 ventral roots; C2R = feeder probably from the C-2 radicular artery (clear triangles in H); PICA = posterior inferior cerebellar artery; PSA = posterior spinal artery; SAN = spinal accessory nerve; VA = vertebral artery; ** = dural feeders. Copyright Kiyoshi Onda. Published with permission.

Postoperative Course

The patient's postoperative status worsened slightly but soon returned to his preoperative level. Postoperative DSA revealed no trace of the AVF, but an extradural pseudoaneurysm was demonstrated on the left C-1 radicular artery, probably caused by surgical dissection (Fig. 6). The patient was able to perform activities of daily living and was ambulatory on discharge. At about 6 years after the operation, he had muscle weakness (MMT Grade 4), paresthesia, and dysesthesia on the left, remaining almost unchanged from his preoperative status.

Fig. 6.
Fig. 6.

Postoperative left vertebral artery angiogram, posteroanterior oblique view, showing no AVF and an extradural pseudoaneurysm on the C-1 radicular artery (arrow).

Case 3

History and Examination

This case has already been reported (Reproduced from Onda et al: Complex arteriovenous fistulas at C1 causing hematomyelia through aneurysmal rupture of a feeder from the anterior spinal artery. Acta Neurochir 154:471–475, 2012, with kind permission from Springer Science+Business Media B.V.). Briefly, a 64-year-old woman presented with left occipital headache and right thermoanesthesia. Motor function was normal (MMT Grade 5). Magnetic resonance imaging revealed hematomyelia in the left ventral portion of C-1 with hyperintense edema extending from the medulla to C-5 (Fig. 7A). Digital subtraction angiography demonstrated dural and intradural AVFs, the former being fed mainly by branches of the left occipital and ascending pharyngeal arteries (Fig. 7B). The anterior meningeal artery and meningeal branches from the C-2 and C-1 radicular arteries on the left appeared to be involved in feeding the dural AVF (Fig. 7C). Feeders from the anterior spinal, left posterior spinal, and left C-2 radicular arteries fed the intradural AVFs. A small aneurysm had arisen on one of the feeders from the anterior spinal artery (Fig. 7D). There were small, dilated pial vessels arising from the anterior spinal artery that participated in vascularization of the perimedullary shunt. A thick drainage vein flowed into the right petrosal vein.

Fig. 7.
Fig. 7.

Sagittal T2-weighted MR image (A) showing a hematoma at C-1 and hyperintense edema extending from the medulla oblongata to C-5. Left common carotid artery (B) and left (C) and right (D) vertebral artery angiograms, posteroanterior views, showing the left C-1 AVF fed by the left occipital (large black arrowheads, B), ascending pharyngeal (small black arrowheads, B), anterior meningeal (double black arrows, C), C-2 radicular (black arrows, C), C-1 radicular (small white arrowhead, C), anterior spinal (double white arrows, C and D) and posterior spinal (small single white arrow, C) arteries and draining rostrally into the right petrosal vein (clear arrowheads, B–D). There was an aneurysm on one of the feeders from the anterior spinal artery (large white arrowhead, D). Large white arrow (B and C) indicates dural shunt point. Modified from Onda et al: Complex arteriovenous fistulas at C1 causing hematomyelia through aneurysmal rupture of a feeder from the anterior spinal artery. Acta Neurochir 154: 471–475, 2012, with kind permission from Springer Science+Business Media B.V.

Operation

A small left suboccipital craniectomy and C1–2 hemilaminectomy were performed. The drainage vein appeared to run along the putative route of the C-1 ventral root, although both the ventral and dorsal roots were absent. This drainage vein was coagulated and sectioned at the intradural entry site and then detached from the pial feeders arising from the anterior spinal, posterior spinal, and C-2 radicular arteries by cauterizing and severing them in a stepwise manner just before each shunt point (Fig. 8).

Fig. 8.
Fig. 8.

Intraoperative microscopy images (A and B, low-power field; C, high-power field) showing feeders from the posterior spinal artery (PSA), anterior spinal artery, and C-2 radicular (C2R) artery, the draining vein (DV) along the putative course of the C-1 ventral root, and the dural entry site of the drainer (black arrow). The C-1 nerve roots were absent. The dentate ligament is cut in the figures. Schematic (D) showing angioarchitecture and some of the blood vessels disconnected during surgery (blue lines). SAN = spinal accessory artery; SC spinal cord; VA = vertebral artery; ** (double asterisks) = dural feeders. Modified from Onda et al: Complex arteriovenous fistulas at C1 causing hematomyelia through aneurysmal rupture of a feeder from the anterior spinal artery. Acta Neurochir 154: 471–475, 2012, with kind permission from Springer Science+Business Media B.V.

Postoperative Course

One day after the operation, left flaccid hemiparesis developed, which disappeared gradually. Postoperative DSA demonstrated total disappearance of the feeders, the aneurysm, and the AVFs, and the patient returned to work. At about 4.5 years after the operation, she complained of minimal weakness of the left lower extremity (MMT Grade 5) and paresthesia in the left first and second fingers and bilateral toes.

Table 1 presents a clinical and angiographic summary of the 3 cases.

TABLE 1:

Summary of 3 cases of high cervical complex AVF fed by the dural and spinal arteries and draining into a single medullary vein

Case No.Age (yrs), SexType of OnsetShunt SiteDural FeedersIntradural FeedersDrainage RouteVarix/Aneurysm
163, Mcongestive myelopathylt C-2C-2 radicularanterior spinalrostral & caudal anterior spinal veinvarix
C-1 radiculomedullary
260, Mhematomyelialt C-1C-1 & C-2 radicularposterior spinalrostral to rt petrosal vein & lt jugular bulbnone
hematobulbiaC-2 radiculomedullary
364, Fhematomyelialt C-1occipitalanterior spinalrostral to rt petrosal veinaneurysm
ascending pharyngealposterior spinal
C-1 & C-2 radicularC-2 radiculomedullary
anterior meningeal

Discussion

We have presented 3 cases of cervical AVF, which is a rarer condition than thoracolumbar AVF. Low-power-field and high-power-field intraoperative photographs showing the clearly labeled angioarchitecture are presented, along with accompanying illustrations for ease of understanding. Table 1 summarizes the common dural and intradural feeders for high cervical AVFs. A common characteristic of the presented cases was the dural and intradural feeders linked with a common medullary venous channel. Some possible explanations were proposed in our previous report:27 metameric, metameric plus other mechanisms such as vessel adhesion, and evolution of a dural AVF into a more complex form with intradural shunts. Although we did not confirm the precise locations of the shunt points between the extradural or dural feeders and the intradural drainage vein, standard “dural” AVF12,18,22,34,35 was used to denote this connection instead of “epidural”8 or “intradural” AVF.36

It has been reported that there is a genetic but nonhereditary disorder in which the vascular cells are most likely affected later in their embryological development, during angiogenesis. Among the resulting lesions, one type has multiple shunts, either an AVF or an arteriovenous malformation (AVM), located on the cord and intradural nerve roots in the same myelomere.33,34 Although familial occurrence and involvement of skin and bone were not found in the current cases, the presence of multiple arteriovenous shunts in the same myelomere may suggest metameric linkage. In Case 1, there were arteriovenous shunts along the left C-2 ventral root, one of which appeared to be dural and fed by the left C-2 radicular artery, whereas the others were probably intradural and located around the ventral root sleeve fed by the C-1 radicular and anterior spinal arteries. Since some of the intradural feeders ran in the C-2 ventral roots and were cut together with the roots just before the shunt, their precise shunt points were not confirmed. In Case 2, the arteriovenous shunts lay along the left C-1 ventral root; one appeared to be dural and fed mainly by the C-1 radicular artery, but the majority were intradural, located near the ventral root sleeve, and fed by the posterior spinal and C-2 radicular artery. There were a few shunts near the cord. In Case 3, the AVFs lay along the putative course of the left C-1 ventral root, which was absent, and on the cord; the former contained a dural AVF fed mainly by the occipital and ascending pharyngeal arteries, and an intradural AVF along the putative C-1 fed by the anterior and posterior spinal arteries; the latter, or perimedullary, AVF6,9 was fed by the anterior spinal and C-2 radicular arteries. If this type of complex AVF were partially or totally metameric, the age at presentation might vary from younger to older. All of our patients were in their early sixties, and so far there has been no report of any similar complex AVF showing juvenile onset. Thus, it may be informative to investigate any metameric lineage after an accumulation of future cases affecting younger individuals.

Dural AVF is the most common spinal vascular abnormality.18 Although its etiology and pathogenesis are unclear, it is thought to be an acquired lesion.5,35 In experimental models, multiple arteriovenous shunts, including dural AVF, has been induced by chronic venous hypertension.37 The literature on cervical dural AVF reveals that the median age at presentation is the late 50s2 with a predominant location in the craniovertebral junction and foramen magnum.2,16,18 The present cases correspond to previous reports of cervical dural AVF at least in terms of patient age and craniovertebral location. Moreover, these cases showed the vascular structure typical of dural AVF—as a direct arteriovenous shunt near the spinal root sleeve fed by one or several arterioles and ending in a single draining vein22,24—except for intradural shunts fed by feeders from the spinal arteries. In addition, the ventral location of the dural shunt, instead of lying near the dorsal root sleeves, may be another atypical feature. Although we performed DSA studies in all cases, which were obtained with flat panel detectors in 2 cases, understanding the angioarchitecture was not so easy even after surgery. Therefore, we postulate that some reported cases of dural AVF arising at the craniocervical junction might have been more complex forms, as in the present cases. In our experience, this type of AVF occurs predominantly in the high cervical area, although another complex form has been reported in the thoracic area.17

The anterior and posterior spinal arteries are responsible for supplying the upper cervical cord. The former originates from the intracranial portion of the vertebral artery (fourth segment), and the latter from the same segment or the posterior inferior cerebellar artery and the radicular branches of the vertebral artery. The anterior radicular branches join the anterior spinal artery, and the posterior radicular branches anastomose with the posterior spinal artery or a posterior plexiform network of vessels.26 These vascular connections appear to be related to the formation of a high cervical complex AVF. In the present cases, some of the intradural feeders ascended the ventral rootlets of C-1 or C-2 toward the dura, suggesting that these arteries were originally anterior radicular arteries. The dorsal root of C-1 is absent in about 8% of individuals,39 where the anterior radicular branch may connect with both the anterior and posterior spinal arteries. Interestingly, 2 of the present cases (Cases 2 and 3) lacked the dorsal root of C-1, and thus involvement of the posterior spinal artery might be explained by these anatomical characteristics. The absence of a ventral root in Case 3 seemed to have resulted from degeneration rather than being a congenital characteristic. In Case 1, the anterior spinal artery was involved in the AVF, suggesting that the anterior radicular branch might have had a connection with only the anterior spinal artery. Spinal AVMs have the potential to evolve,33 and the resulting complicated morphology may mask the initial disorder. In the present cases, the dominant shunts appeared to form the dural AVF. As the flow in the shunt and drainage vein increased, twigs of the anterior radicular branches might have become involved through a sump effect7 and received flow from intradural feeders, such as the anterior or posterior spinal arteries via the already present anastomosis, as mentioned above, leading to the formation of arteriovenous shunts along the ventral nerve root. It has been reported that flow velocity in drainage veins decreases with increasing distance from a dural arteriovenous shunt,12 suggesting that drainers close to the dural root sleeves may have the greatest potential to exert a sump effect. In addition, shunt flow in the present cases was higher than that in a thoracolumbar dural AVF, which is typically of the slow-flow type.18 These factors may explain the recruitment of spinal arteries to the complex AVF located predominantly around the origin of the drainage veins. A similar phenomenon could also have occurred in the perimedullary area or on the cord, as seen in Cases 2 and 3. Physiological arteriovenous shunts found in the cauda equina, which are thought to be a second-line venous drainage system,29 have not been documented in cervical spinal nerve roots.

Spinal cord AVMs are often classified into 4 groups: Type I, dural AVFs; Type II, intramedullary glomus malformations; Type III, juvenile malformations; Type IV, perimedullary AVFs.1,4,28 P erimedullary AVF was first described in 1977 by Djindjian et al.,6 and Heros et al.13 introduced the term “Type IV spinal AVM” for this type of malformation. Type IV AVMs are direct arteriovenous shunts located superficially on the spinal cord. Depending on the size of the feeding vessels, shunt volume, and size of the draining veins, the Type IV AVM has been subclassified into 3 types—Type I, II, and III perimedullary AVFs—by Merland and associates,9,23,25,32 which Anson and Spetzler have proposed naming “Type IV-A,” “Type IV-B,” and “Type IV-C” to avoid confusion.1 Most Type IV AVMs are anterior or anterolateral to the spinal cord and supplied by the anterior spinal artery. However, they can occur in a posterior location supplied by the posterior spinal artery.1 Radiculomedullary arteries are their feeding vessels, which differentiates them from dural AVFs fed by the radiculomeningeal arteries.19 As mentioned above, the dominant shunts in the present cases appeared to form the dural AVF fed by one or more combinations of meningeal vessels. Thus, the present cases differed from Type IV AVMs.

Interventional techniques have been used increasingly to treat spinal cord AVMs, and embolization is the treatment of choice for many.19,30,34,38 However, surgery continues to play a key role, and a multidisciplinary approach is essential.30 In the treatment of spinal dural AVFs, or Type I AVMs, tentative embolization is adopted by many centers if the anterior spinal artery does not arise from the same pedicle as the shunt feeder.18,19,34 If a liquid embolic agent does not reach the venous site, early surgical intervention is strongly advocated.18,19,38 In a recent report of cervical dural AVFs, an angiographic cure was achieved with N-butyl 2-cyanoacrylate (NBCA) in 2 patients, and resection was performed in 7 patients because of embolization failure or residual and/or recurrent shunt.15 Embolization plays an important role in the management of Type II and Type III AVMs, either as a primary treatment or as an adjunct to surgery.1,19,28,30,38 The indications for endovascular treatment of Type IV AVMs vary according to the subtype.1,9,10,19,23,25,28,30,38 Because Type IV-A fistulas are small, they are usually inaccessible for embolization. Type IV-B AVMs can potentially be treated with surgery, embolization, or both, depending on their individual anatomical and flow characteristics. Type IV-C AVMs, or giant fistulas, are best treated using embolization. In our present cases, surgery was the preferred initial treatment based on anatomical and flow characteristics.

In our experience, precise preoperative determination of the anatomy of an upper cervical complex AVF is laborious. Digital subtraction angiography is indispensable, and superselective catheterization of the feeders may be prerequisite for evaluation. General anesthesia is also recommended to obtain clear findings.34 In addition to DSA, high-resolution MRI and CT angiography with computed fusion techniques can be useful for obtaining preoperative images of the anatomy of the complex AVF. Although endovascular techniques have improved and are now the first choice for treatment of many spinal AVMs as described above, anatomical verification of the complex AVF may still require operative confirmation. As for surgical procedures, electrophysiological monitoring (especially motor evoked potentials)20 and intraoperative angiography3 appear to be important; the latter has recently been replaced by indocyanine green videoangiography.11,28,31 In surgery for spinal dural AVFs, the drainage veins are coagulated and incised near the dural root sleeve.22,24 For high cervical dural AVFs, which are often complex, it seems better to trace the drainage vein on the cord to ascertain the presence or absence of perimedullary feeders. In complex dural AVFs, postoperative determination of the angioarchitecture by comparing preoperative DSA studies with intraoperative video findings may be necessary. Indocyanine green videoangiography appears to greatly facilitate this procedure.

Conclusions

The characteristics of high cervical AVF with dural and intradural feeders linked with a common medullary venous channel are different from those arising in other spinal regions.

Acknowledgment

We thank all clinicians and ancillary workers at our institutions for their cooperation in this study.

Disclosure

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 to the study and manuscript preparation include the following. Conception and design: Onda. Acquisition of data: Onda, Yoshida, Watanabe, Okada. Analysis and interpretation of data: Onda, Terada. Drafting the article: Onda. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Onda. Study supervision: Arai.

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    Krings TGeibprasert S: Spinal dural arteriovenous fistulas. AJNR Am J Neuroradiol 30:6396482009

  • 19.

    Krings TThron AKGeibprasert SAgid RHans FJLasjaunias PL: Endovascular management of spinal vascular malformations. Neurosurg Rev 33:192010

  • 20.

    Levy WJ Jr: Clinical experience with motor and cerebellar evoked potential monitoring. Neurosurgery 20:1691821987

  • 21.

    Logue V: Angiomas of the spinal cord: review of the pathogenesis, clinical features, and results of surgery. J Neurol Neurosurg Psychiatry 42:1111979

  • 22.

    McCutcheon IEDoppman JLOldfield EH: Microvascular anatomy of dural arteriovenous abnormalities of the spine: a microangiographic study. J Neurosurg 84:2152201996

  • 23.

    Merland JJReizine DEmbolization techniques in the spinal cord. Dondelinger RFRossi PKurdziel JC: Interventional Radiology New YorkThieme1990. 433442

  • 24.

    Merland JJRiche MCChiras J: Intraspinal extramedullary arteriovenous fistulae draining into the medullary veins. J Neuroradiol 7:2713201980

  • 25.

    Mourier KLGobin YPGeorge BLot GMerland JJ: Intradural perimedullary arteriovenous fistulae: results of surgical and endovascular treatment in a series of 35 cases. Neurosurgery 32:8858911993

  • 26.

    Newton THMani RLThe vertebral artery. Newton THPotts DG: Radiology of the Skull and Brain: Angiography New YorkMediBooks1986. 16591709

  • 27.

    Onda KYoshida YArai HTerada T: Complex arteriovenous fistulas at C1 causing hematomyelia through aneurysmal rupture of a feeder from the anterior spinal artery. Acta Neurochir (Wien) 154:4714752012

  • 28.

    O'Toole JEMcCormick PCVascular malformation of the spinal cord. Herkowitz HNGarfin SREismont FJ: Rothman-Simeone The Spine ed 6PhiladelphiaElsevier Saunders2011. 16421654

  • 29.

    Parke WWBono CMGarfin SRApplied anatomy of the spine. Herkowitz HNGarfin SREismont FJ: Rothman-Simeone The Spine ed 6PhiladelphiaElsevier Saunders2011. 1553

  • 30.

    Patsalides AKnopman JSantillan ATsiouris AJRiina HGobin YP: Endovascular treatment of spinal arteriovenous lesions: beyond the dural fistula. AJNR Am J Neuroradiol 32:7988082011

  • 31.

    Raabe ABeck JGerlach RZimmermann MSeifert V: Nearinfrared indocyanine green video angiography: a new method for intraoperative assessment of vascular flow. Neurosurgery 52:1321392003

  • 32.

    Riche MCReizine DMelki JPMerland JJ: Classification of spinal cord vascular malformations. Radiat Med 3:17241985

  • 33.

    Rodesch GHurth MAlvarez HTadié MLasjaunias P: Classification of spinal cord arteriovenous shunts: proposal for a reappraisal—the Bicêtre experience with 155 consecutive patients treated between 1981 and 1999. Neurosurgery 51:3743802002

  • 34.

    Rodesch GLasjaunias P: Spinal cord arteriovenous shunts: from imaging to management. Eur J Radiol 46:2212322003

  • 35.

    Rosenblum BOldfield EHDoppman JLDi Chiro G: Spinal arteriovenous malformations: a comparison of dural arteriovenous fistulas and intradural AVM's in 81 patients. J Neurosurg 67:7958021987

  • 36.

    Spetzler RFDetwiler PWRiina HAPorter RW: Modified classification of spinal cord vascular lesions. J Neurosurg 2 Suppl96:1451562002

  • 37.

    Terada THigashida RTHalbach VVDowd CFTsuura MKomai N: Development of acquired arteriovenous fistulas in rats due to venous hypertension. J Neurosurg 80:8848891994

  • 38.

    Wakhloo AKPatel NVDeLeo MJ IIIShaibani AVascular anatomy of the spine, imaging, and endovascular treatment of spinal vascular diseases. Herkowitz HNGarfin SREismont FJ: Rothman-Simeone The Spine ed 6PhiladelphiaElsevier Saunders2011. 16551687

  • 39.

    Warwick RWilliams PL: The spinal nerves. Gray's Anatomy ed 35EdinburghLongman1973. 10301032

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Article Information

Address correspondence to: Kiyoshi Onda, M.D., Ph.D., Niigata Neurosurgical Hospital, 3057 Yamada, Niigata 950-1101, Japan. email: kiyoshionda@apost.plala.or.jp.

Please include this information when citing this paper: published online January 17, 2014; DOI: 10.3171/2013.11.SPINE13402.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    A: Sagittal T2-weighted MR image showing a high-intensity area extending from the medulla oblongata to C-4. B: Left vertebral angiogram, early (upper) and late (lower) arterial phases, posteroanterior oblique view, showing a left C-2 AVF supplied from the C-1 radicular (white arrowheads), C-2 radicular (small black arrowheads), and anterior spinal (large black arrowheads) arteries and draining to the radiculomedullary vein (clear arrowheads), which had a small varix (black arrow) and merged with the anterior spinal vein flowing both rostrally and caudally. White arrow indicates shunt point.

  • View in gallery

    Intraoperative microscopy image (A, low-power field) and neighboring fields near the C-2 AVF (B and C, high-power field) showing a feeder from the C-1 radicular artery (C1R: clear circles in B and C), draining vein (DV) with varix (Va), and feeders probably from the anterior spinal artery in or along the C-2 ventral roots (asterisks). Dentate ligament (DL) and C-2 dorsal roots were sectioned in B and C. Schematic (D) showing angioarchitecture and blood vessels disconnected during surgery (solid and dotted blue lines [dotted lines indicate features originally hidden under the roots, spinal cord, and so forth]). C2 = C-2 spinal nerve roots; SAN = spinal accessory nerve; SC = spinal cord; ** = dural feeders. Copyright Kiyoshi Onda. Published with permission.

  • View in gallery

    Postoperative left vertebral artery angiogram, posteroanterior oblique view, showing disappearance of the AVF.

  • View in gallery

    A: Sagittal T2-weighted MR image showing a hematoma extending from the medulla oblongata to C-2. B: Magnetic resonance angiogram showing an abnormal vessel at the craniocervical junction (arrow). C: Left vertebral artery angiogram, posteroanterior view, showing the left C-1 AVF fed by the C-2 radicular (large black arrowheads), C-1 radicular (white arrowheads), and posterior spinal (small black arrowheads) arteries and draining rostrally into the right petrosal vein and left jugular bulb via the transverse pontine vein (clear arrowheads). White arrow indicates shunt point.

  • View in gallery

    Intraoperative microscopy images (A and B, low-power field; C–G, high-power field) showing feeders from the posterior spinal artery (single asterisks) and C-2 radicular (black arrowheads) artery, the draining vein (DV), and the dural entry site of the drainer after disconnection (white arrow). A branch of the spinal accessory nerve that had merged into the C-1 ventral root was divided (A and B). There were several C-1 ventral rootlets, but the C-1 dorsal root was absent (B). The posterior spinal artery supplied a few feeding arteries (black arrows) to the draining vein, one of which merged with the vein around the ventral root sleeve, while the others merged near the spinal cord; a branch probably originating from the C-2 radicular artery also fed the AVF (black arrowheads). The dentate ligament is cut in the figures. H: Schematic showing angioarchitecture and blood vessels disconnected during surgery (blue lines). C1 = C-1 ventral roots; C2R = feeder probably from the C-2 radicular artery (clear triangles in H); PICA = posterior inferior cerebellar artery; PSA = posterior spinal artery; SAN = spinal accessory nerve; VA = vertebral artery; ** = dural feeders. Copyright Kiyoshi Onda. Published with permission.

  • View in gallery

    Postoperative left vertebral artery angiogram, posteroanterior oblique view, showing no AVF and an extradural pseudoaneurysm on the C-1 radicular artery (arrow).

  • View in gallery

    Sagittal T2-weighted MR image (A) showing a hematoma at C-1 and hyperintense edema extending from the medulla oblongata to C-5. Left common carotid artery (B) and left (C) and right (D) vertebral artery angiograms, posteroanterior views, showing the left C-1 AVF fed by the left occipital (large black arrowheads, B), ascending pharyngeal (small black arrowheads, B), anterior meningeal (double black arrows, C), C-2 radicular (black arrows, C), C-1 radicular (small white arrowhead, C), anterior spinal (double white arrows, C and D) and posterior spinal (small single white arrow, C) arteries and draining rostrally into the right petrosal vein (clear arrowheads, B–D). There was an aneurysm on one of the feeders from the anterior spinal artery (large white arrowhead, D). Large white arrow (B and C) indicates dural shunt point. Modified from Onda et al: Complex arteriovenous fistulas at C1 causing hematomyelia through aneurysmal rupture of a feeder from the anterior spinal artery. Acta Neurochir 154: 471–475, 2012, with kind permission from Springer Science+Business Media B.V.

  • View in gallery

    Intraoperative microscopy images (A and B, low-power field; C, high-power field) showing feeders from the posterior spinal artery (PSA), anterior spinal artery, and C-2 radicular (C2R) artery, the draining vein (DV) along the putative course of the C-1 ventral root, and the dural entry site of the drainer (black arrow). The C-1 nerve roots were absent. The dentate ligament is cut in the figures. Schematic (D) showing angioarchitecture and some of the blood vessels disconnected during surgery (blue lines). SAN = spinal accessory artery; SC spinal cord; VA = vertebral artery; ** (double asterisks) = dural feeders. Modified from Onda et al: Complex arteriovenous fistulas at C1 causing hematomyelia through aneurysmal rupture of a feeder from the anterior spinal artery. Acta Neurochir 154: 471–475, 2012, with kind permission from Springer Science+Business Media B.V.

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Krings TGeibprasert S: Spinal dural arteriovenous fistulas. AJNR Am J Neuroradiol 30:6396482009

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Krings TThron AKGeibprasert SAgid RHans FJLasjaunias PL: Endovascular management of spinal vascular malformations. Neurosurg Rev 33:192010

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Levy WJ Jr: Clinical experience with motor and cerebellar evoked potential monitoring. Neurosurgery 20:1691821987

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Logue V: Angiomas of the spinal cord: review of the pathogenesis, clinical features, and results of surgery. J Neurol Neurosurg Psychiatry 42:1111979

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McCutcheon IEDoppman JLOldfield EH: Microvascular anatomy of dural arteriovenous abnormalities of the spine: a microangiographic study. J Neurosurg 84:2152201996

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Merland JJReizine DEmbolization techniques in the spinal cord. Dondelinger RFRossi PKurdziel JC: Interventional Radiology New YorkThieme1990. 433442

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Merland JJRiche MCChiras J: Intraspinal extramedullary arteriovenous fistulae draining into the medullary veins. J Neuroradiol 7:2713201980

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Mourier KLGobin YPGeorge BLot GMerland JJ: Intradural perimedullary arteriovenous fistulae: results of surgical and endovascular treatment in a series of 35 cases. Neurosurgery 32:8858911993

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Newton THMani RLThe vertebral artery. Newton THPotts DG: Radiology of the Skull and Brain: Angiography New YorkMediBooks1986. 16591709

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Onda KYoshida YArai HTerada T: Complex arteriovenous fistulas at C1 causing hematomyelia through aneurysmal rupture of a feeder from the anterior spinal artery. Acta Neurochir (Wien) 154:4714752012

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O'Toole JEMcCormick PCVascular malformation of the spinal cord. Herkowitz HNGarfin SREismont FJ: Rothman-Simeone The Spine ed 6PhiladelphiaElsevier Saunders2011. 16421654

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Parke WWBono CMGarfin SRApplied anatomy of the spine. Herkowitz HNGarfin SREismont FJ: Rothman-Simeone The Spine ed 6PhiladelphiaElsevier Saunders2011. 1553

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Patsalides AKnopman JSantillan ATsiouris AJRiina HGobin YP: Endovascular treatment of spinal arteriovenous lesions: beyond the dural fistula. AJNR Am J Neuroradiol 32:7988082011

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Raabe ABeck JGerlach RZimmermann MSeifert V: Nearinfrared indocyanine green video angiography: a new method for intraoperative assessment of vascular flow. Neurosurgery 52:1321392003

32.

Riche MCReizine DMelki JPMerland JJ: Classification of spinal cord vascular malformations. Radiat Med 3:17241985

33.

Rodesch GHurth MAlvarez HTadié MLasjaunias P: Classification of spinal cord arteriovenous shunts: proposal for a reappraisal—the Bicêtre experience with 155 consecutive patients treated between 1981 and 1999. Neurosurgery 51:3743802002

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Rodesch GLasjaunias P: Spinal cord arteriovenous shunts: from imaging to management. Eur J Radiol 46:2212322003

35.

Rosenblum BOldfield EHDoppman JLDi Chiro G: Spinal arteriovenous malformations: a comparison of dural arteriovenous fistulas and intradural AVM's in 81 patients. J Neurosurg 67:7958021987

36.

Spetzler RFDetwiler PWRiina HAPorter RW: Modified classification of spinal cord vascular lesions. J Neurosurg 2 Suppl96:1451562002

37.

Terada THigashida RTHalbach VVDowd CFTsuura MKomai N: Development of acquired arteriovenous fistulas in rats due to venous hypertension. J Neurosurg 80:8848891994

38.

Wakhloo AKPatel NVDeLeo MJ IIIShaibani AVascular anatomy of the spine, imaging, and endovascular treatment of spinal vascular diseases. Herkowitz HNGarfin SREismont FJ: Rothman-Simeone The Spine ed 6PhiladelphiaElsevier Saunders2011. 16551687

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Warwick RWilliams PL: The spinal nerves. Gray's Anatomy ed 35EdinburghLongman1973. 10301032

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