Case Report
Cervical Spinal Epidural Arteriovenous Fistula with Coexisting Spinal Anterior Spinal Artery Aneurysm Presenting as Subarachnoid Hemorrhage—Case Report Ichiro Nakagawa, MD, PhD,* Hun-Soo Park, MD,* Yasuo Hironaka, MD, PhD,* Takeshi Wada, MD,† Kimihiko Kichikawa, MD, PhD,† and Hiroyuki Nakase, MD, PhD*
Hemorrhagic presentation of spinal epidural arteriovenous fistulas (AVFs) is rare in patients with cervical spinal vascular lesions. The present report describes a patient with cervical spine epidural AVFs associated with anterior spinal artery aneurysm at the same vertebral level presenting with subarachnoid hemorrhage. A 54-year-old man presented with sudden onset of headache. Computed tomography of the head showed subarachnoid hemorrhage. Diagnostic angiography revealed an epidural AVF located at the C1-2 level that was fed mainly by the dorsal somatic branches of the segmental arteries from the radicular artery and anterior spinal artery. This AVF drained only into the epidural veins without perimedullary venous reflux. Further, there was a 4-mm anterior spinal artery aneurysm in the vicinity of the fistula that was thought to be the cause of the hemorrhage. Endovascular transarterial fistulas embolization from the right radicular artery was performed to eliminate the AVF and to reduce hemodynamic stress on the aneurysm. No new symptoms developed after the treatment and discharged without neurological deficits. The aneurysm was noted to be reduced in size after the treatment and totally disappeared by 1 year later, according to follow-up angiography. Anterior spinal artery aneurysm from a separate vascular distribution may coexist with spinal epidural AVFs. In the setting of spinal subarachnoid hemorrhage, comprehensive imaging is indicated to rule out such lesions. Key Words: Aneurysm—anterior spinal artery—epidural arteriovenous fistula—subarachnoid hemorrhage— transarterial embolization. Ó 2014 by National Stroke Association
Spinal epidural arteriovenous fistulas (AVFs) are rare cervical spine vascular lesions, and they are generally thought to present with benign clinical symptoms, such From the *Department of Neurosurgery; and †Department of Radiology, Nara Medical University, Kashihara City, Japan. Received June 16, 2014; revision received July 6, 2014; accepted July 9, 2014. Address correspondence to Ichiro Nakagawa, MD, PhD, Department of Neurosurgery, Nara Medical University, 840 Shijocho, Kashihara City, Nara 634-8522, Japan. E-mail: nakagawa@ naramed-u.ac.jp. 1052-3057/$ - see front matter Ó 2014 by National Stroke Association http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2014.07.012
as radiculopathy.1-3 In some cases, spinal epidural AVF can cause acute paraplegia due to reflux into medullary veins with venous congestion.4-7 In patients with craniocervical dural AVF, subarachnoid hemorrhage has been reported to occur because of a direct venous drainage pattern in an intracranially or intramedullary fashion.8-12 However, hemorrhagic presentation of cervical spinal epidural AVF without intramedullary venous drainage is very rare. The present report describes a case of a patient with cervical spine epidural AVFs associated with anterior spinal artery aneurysm at the same vertebral level who presented with subarachnoid hemorrhage.
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Figure 1. (A) Axial computed tomography (CT) scan of the head showing subarachnoid hemorrhage and intraventricular hemorrhage. (B) Coronal CT scan of the cervical spine with contrast demonstrating anterior spinal artery aneurysm (arrowhead) and dilated epidural veins (arrow).
Case Report A 54-year-old man presented with sudden onset of severe headache and vomiting. A computed tomography scan of the head revealed a subarachnoid hemorrhage, mainly in the posterior fossa distribution and secondary hydrocephalus (Fig 1, A). Subsequent computed tomography angiogram of the head and neck to access for a vascular etiology revealed a vascular abnormality at the right C1/2 level and aneurysmal dilatation within the spinal canal at the C1/2 level (Fig 1, B). Magnetic resonance imaging demonstrated a signal defect and was strongly supportive of these findings. Comprehensive cerebral and spinal angiography was subsequently performed. Injection of the vertebral artery (VA) revealed an abnormally enlarged right radicular artery at the C1/2 level and multiple thin feeding arteries from the bilateral VA to the fistula (Fig 2, A and B). Furthermore, an anterior spinal artery aneurysm (4 3 2 mm in diameter) was located anteriorly within the spinal canal in the vicinity of the fistulas at the level of the C1/2 disc. The fistulas directly drained to the epidural veins and paravertebral venous plexus. Perimedullary venous reflux was not identified (Fig 2, C). These findings were consistent with a spinal epidural AVF at the C1/2 level and an anterior spinal artery aneurysm at the same level origin of the subarachnoid hemorrhage. We planned endovascular transarterial embolization to eliminate the fistulas and to reduce hemodynamic stress to the aneurysm, because it was deemed too difficult to access the anterior spinal artery aneurysm after discussing the case with the neurosurgical and endovascular teams. The endovascular procedure was performed 7 days after admission after obtaining written informed consent from the patient. Under local anesthesia with systemic heparinization to maintain the activated clotting time at levels above 2to 3-fold of the baseline value, a 7-Fr guiding catheter was inserted into the right femoral artery and guided into the right VA. Marathon flow directed microcatheters
(Covidien, Dublin, Ireland) were introduced into the main feeder as close to shunt points as possible through each guiding catheter. Right VA angiography revealed the aneurysm had enlarged (5 3 4 mm in diameter) compared with the aneurysm size seen during initial angiography (Fig 3, A). Transarterial embolization was performed from the main feeder right radial artery with a mixture of n-butyl cyanoacrylate and lipiodol. Avoiding retrograde distal migration of embolic material through other feeding arteries, balloon inflation was performed using a Hyperform balloon (Covidien) at the distal orifice of the main feeder of the right radial artery during embolization. Although transarterial embolization did not achieve complete occlusion of the fistulas due to the presence of other small feeding arteries, blood flow to the fistula was markedly reduced. Blood supply from anterior spinal artery to the fistula markedly reduced and there was an almost total disappearance of anterior spinal artery aneurysm without aneursymal stagnant appearance (Fig 3, B). The postoperative course was uneventful. No new neurologic symptoms developed, and ischemic lesions were not identified on diffusion-weighted images. Selective angiography performed 15 days later confirmed poor depiction of the anterior spinal artery aneurysm and fistulas. Selective angiography a year after the embolization revealed complete occlusion of the AVF and the aneurysm, preserving anterior spinal artery flow (Fig 3, C).
Discussion Spinal epidural AVFs are vascular anomalies that preferentially affect cervical portion and that are rare compared with spinal dural AVF. Several cases of cervical spinal epidural AVFs have been published in the literature, which are summarized in Table 1. Most cases are associated with perimedullary venous reflux causing congestive myelopathy.8-13 Hemorrhagic presentation with subarachnoid hemorrhage has only been reported
EPIDURAL AVF WITH SPINAL ARTERY ANEURYSM
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Figure 2. Right vertebral artery angiogram on admission. (A) Lateral view, (B) early phase of the right anterior oblique view, (C) late phase of the right anterior oblique view revealing epidural arteriovenous fistula with multiple feeding arteries from the vertebral artery (white arrowhead) and anterior spinal artery (white arrow). Anterior spinal artery aneurysm was identified in the vicinity of the fistula (black arrow). The fistulas directly drained to the paravertebral venous plexus (black arrowhead) without perimedullary venous reflux.
in one case (Case one) in the literature,10 but there was no description of the presence of ruptured aneurysm. Therefore, the present case is the first report of the concurrent existence of cervical epidural AVF and ruptured anterior spinal artery aneurysm. Unlike spinal dural AVFs, epidural AVFs are located in the ventral epidural space and are fed by multiple epidural branches and drain into the ventral epidural venous pouch. They are generally thought to present with benign clinical symptoms, such as radiculopathy.3 Geibprasert et al14 proposed a new classification of dural AVFs according to craniospinal epidural venous anatomy. Populations with ventral epidural group showed a female predominance, benign clinical presentation, and a lower rate of spinal cord venous reflux compared with lateral epidural group. The venous drainage route in the lateral epidural group, which includes typical spinal dural
AVFs, is always directed to the perimedullary veins; therefore, this type of AVF tends to be aggressive. The present case can be classified as a ventral epidural AVF because of the shunt location, which consists of mainly epidural drainage without perimedullary venous reflux. Furthermore, the shunt itself is asymptomatic. Kiyosue et al15 clearly described the classification of spinal ventral epidural AVFs of the lumbar spine based on the drainage type. Dorsal somatic branches, which supply the vertebral body, were the primary feeding branches to the epidural AVFs, forming a shunted pouch located in the ventral epidural space. They describe 3 types of venous drainage routes: the perimedullary venous drainage (PM), the paravertebral drainage (PV), and the combined perimedullary and paravertebral venous drainage. In PM-type AVFs, the epidural AVFs are shunted to an epidural venous pouch and then drained through the
Figure 3. Right vertebral angiogram before and after endovascular treatment. (A) Pre-embolization angiogram (right anterior oblique view) shows that the aneurysm enlarged to 5 3 4 mm in diameter (white arrow). (B) Angiogram after embolization (right anterior oblique view) did not achieve complete obliteration of the aneurysm (white arrow) but did result in marked reduction of blood flow to the fistula. (C) Angiography a year after the embolization reveals complete occlusion of the arteriovenous fistula and the aneurysm (white arrow), whereas anterior spinal artery flow is maintained (white arrowhead).
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Table 1. Reported cases of cervical spinal epidural arteriovenous fistula Author (y)
Age, y Sex
Neurology
1. Hemphill III (1998)
20
M SAH
2. Willinsky R (1993)
57
3. Goyal M (1999)
Site C1-2
Feeder
Drainer
Rt. VA branch
Epidural vein
M Radiculopathy, C3-4 myelopathy
VA, ascending cervical artery, TA
Epidural vein
68
M Myelopathy
C
4. Asai J (2001)
24
M Myelopathy
C5-T2
5. Suh DC (2004)
50
F
Myelopathy
C5
VA, thyrocervical Epidural vein artery PVVP Ascending cervical Epidural vein artery, deep cervical PVVP artery Costocervical artery, Epidural vein VA PVVP
6. Kawabori M (2009)
65
F
Radiculopathy C5-7
7. Castilla LR (2011) 8. Present case
57 54
M Myelopathy M SAH (ASA aneurysm)
C2-T1 C1-2
Treatment
Outcome
TAE/ Recovery, no surgery recurrence (67 mo) TAE Recovery, no recurrence (1 y) TAE Recovery TAE/ Recovery surgery TVE
Thyrocervical artery
PVVP, PMV
TAE
TA VA branches, ASA
Epidural vein Epidural vein
TVE TAE
Recovery, no recurrence (12 y) Recovery, no recurrence (1 y) Recovery, no recurrence (2.5 y)
Abbreviations: ASA, anterior spinal artery; F, female; M, male; PMV, perimedullary vein; PVVP, paravertebral venous plexus; Rt., right; SAH, subarachnoid hemorrhage; TA, thyroid artery; TAE, transarterial embolization; TVE, transvenous embolization; VA, vertebral artery. Reported cases of cervical spinal epidural arteriovenous fistula.
radiculomedullary vein into the perimedullary vein. The PV-type AVFs are drained via the radiculoemissary vein into the paravertebral veins. The present case can be classified as PV-type AVF, because the AVF was drained via the radiculoemissary vein into the paravertebral veins without perimedullary drainage. This is the first report of the concurrent existence of epidural AVF and anterior spinal artery aneurysm. An association of between dural AVFs and aneurysms has rarely been reported in the literature.16 As low-flow lesions, AVFs seldom produce sufficient hemodynamic stress on the arterial walls to induce aneurysm formation of feeding arteries. Sato et al17 described 9 cases of concurrent of dural AVFs and perimedullary AVFs at the craniocervical junction. In all the 9 cases, fistulas shared dilated perimedullary veins as a main drainage route, and 8 of 9 patients exhibited an arterial aneurysm on the distal side of the feeding arteries to the perimedullary AVF. The aneurysm in each case was intraoperatively confirmed as the bleeding point. They postulated that relatively high-flow dural AVFs cause a venous steal effect or venous hypoxia due to venous hypertension that, in combination with specific anatomic and hemodynamic factors, induces perimedullary AVF at the craniocervical junction. Unlike their cases, concurrent existence of epidural AVF and perimedullary AVF was not identified in the present case, and fistulas directly drained to epidural veins and the paravertebral venous plexus without perimedullary venous reflux. However, it is spec-
ulated that relatively high-flow epidural AVF may cause secondary anterior spinal arterial aneurysmal changes related to flow in the shunt. The therapeutic goal in the management of epidural AVFs is to obliterate the fistulous communication between the feeding artery and the draining vein by means of surgery or endovascular embolization. Most of the epidural AVFs classified with the PM-type venous drainage can be successfully treated by transarterial embolization with either Onyx or glue,18 although transvenous embolization or surgical resection may also be possible.13,14 The patient in the present case showed subarachnoid hemorrhage due to ruptured anterior spinal artery aneurysm in the vicinity of the epidural AVF, but he was treated by transarterial embolization from the right radicular artery. A surgical or endovascular approach to an anterior spinal artery aneurysm is difficult to access and is associated with a high risk of complications. Reduction of hemodynamic stress to feeding arteries from the anterior spinal artery might result in resolution of the aneurysm whereas preserving normal perfusion to the anterior spinal artery (Fig 4). However, there is a possibility of increase in hemodynamic stress to the aneurysm after transarterial embolization. Henkes et al19 reported that there is a direct relationship between pressure changes of feeding artery and degree of embolization in arteriovenous malformation. They concluded that pressure increases during embolization were relatively small compared with mean
EPIDURAL AVF WITH SPINAL ARTERY ANEURYSM
Figure 4. A schematic drawing of the vascular structure. Relatively highflow epidural arteriovenous fistula may cause secondary anterior spinal arterial aneurysmal changes related to flow in the shunt fed by ASA. Abbreviations: ASA, anterior spinal artery; VA, vertebral artery.
arterial systolic pressure; these pressure changes seemed unlikely to be the cause of periprocedural bleedings. This is the first description of cervical spine epidural AVFs associated with anterior spinal artery aneurysm at the same vertebral level in a patient who presented with subarachnoid hemorrhage. Although the long-term results of transarterial fistulas embolization remain to be evaluated, endovascular treatment to reduce hemodynamic stress to the aneurysm might be a useful treatment option to prevent rerupture and to induce obliteration of the aneurysm. In the setting of spinal subarachnoid hemorrhage, comprehensive imaging is indicated to rule out such lesions.
References 1. Clarke MJ, Patrick TA, White JB, et al. Spinal extradural arteriovenous malformations with parenchymal drainage: venous drainage variability and implications in clinical manifestations. Neurosurg Focus 2009;26:E5. 2. Hemphill JC 3rd, Smith WS, Halbach VV. Neurologic manifestations of spinal epidural arteriovenous malformations. Neurology 1998;50:817-819. 3. Lanzino G, D’Urso PI, Kallmes DF, et al. Onyx embolization of extradural spinal arteriovenous malformations with intradural venous drainage. Neurosurgery 2012; 70:329-333.
5 4. Kiyosue H, Tanoue S, Okahara M, et al. Spinal ventral epidural arteriovenous fistulas of the lumbar spine: angioarchitecture and endovascular treatment. Neuroradiology 2013;55:327-336. 5. Lim SM, Choi IS. Spinal epidural arteriovenous fistula: a unique pathway into the perimedullary vein. A case report. Interv Neuroradiol 2009;15:466-469. 6. Pirouzmand F, Wallace MC, Willinsky R. Spinal epidural arteriovenous fistula with intramedullary reflux. Case report. J Neurosurg 1997;87:633-635. 7. Reul J, Braun V. Spinal arteriovenous epidural fistula with acute paraplegia. Diagnosis and neurointerventional emergency treatment. A case report. Interv Neuroradiol 2007;13:75-78. 8. Asai J, Hayashi T, Fujimoto T, et al. Exclusively epidural arteriovenous fistula in the cervical spine with spinal cord symptoms: case report. Neurosurgery 2001; 48:1372-1375. discussion 1375-1376. 9. Chul Suh D, Gon Choi C, Bo Sung K, et al. Spinal osseous epidural arteriovenous fistula with multiple small arterial feeders converging to a round fistular nidus as a target of venous approach. AJNR Am J Neuroradiol 2004;25:69-73. 10. Goyal M, Willinsky R, Montanera W, et al. Paravertebral arteriovenous malformations with epidural drainage: clinical spectrum, imaging features, and results of treatment. AJNR Am J Neuroradiol 1999;20:749-755. 11. Patsalides A, Knopman J, Santillan A, et al. Endovascular treatment of spinal arteriovenous lesions: beyond the dural fistula. AJNR Am J Neuroradiol 2011;32:798-808. 12. Willinsky R, terBrugge K, Montanera W, et al. Spinal epidural arteriovenous fistulas: arterial and venous approaches to embolization. AJNR Am J Neuroradiol 1993;14:812-817. 13. Rangel-Castilla L, Holman PJ, Krishna C, et al. Spinal extradural arteriovenous fistulas: a clinical and radiological description of different types and their novel treatment with Onyx. J Neurosurg Spine 2011;15:541-549. 14. Geibprasert S, Pereira V, Krings T, et al. Dural arteriovenous shunts: a new classification of craniospinal epidural venous anatomical bases and clinical correlations. Stroke 2008;39:2783-2794. 15. Kawabori M, Hida K, Yano S, et al. Cervical epidural arteriovenous fistula with radiculopathy mimicking cervical spondylosis. Neurol Med Chir (Tokyo) 2009;49:108-113. 16. Krings T, Mull M, Bostroem A, et al. Spinal epidural arteriovenous fistula with perimedullary drainage. Case report and pathomechanical considerations. J Neurosurg Spine 2006;5:353-358. 17. Sato K, Endo T, Niizuma K, et al. Concurrent dural and perimedullary arteriovenous fistulas at the craniocervical junction: case series with special reference to angioarchitecture. J Neurosurg 2013;118:451-459. 18. Lai CW, Agid R, van den Berg R, et al. Cerebral arteriovenous fistulas induced by dural arteriovenous shunts. AJNR Am J Neuroradiol 2005;26:1259-1262. 19. Henkes H, Gotwald TF, Brew S, et al. Pressure measurements in arterial feeders of brain arteriovenous malformations before and after endovascular embolization. Neuroradiology 2004;46:673-677.
Cervical Spinal Epidural Arteriovenous Fistula with Coexisting Spinal Anterior Spinal Artery Aneurysm Presenting as Subarachnoid Hemorrhage—Case Report Ichiro Nakagawa, MD, PhD,* Hun-Soo Park, MD,* Yasuo Hironaka, MD, PhD,* Takeshi Wada, MD,† Kimihiko Kichikawa, MD, PhD,† and Hiroyuki Nakase, MD, PhD*
Hemorrhagic presentation of spinal epidural arteriovenous fistulas (AVFs) is rare in patients with cervical spinal vascular lesions. The present report describes a patient with cervical spine epidural AVFs associated with anterior spinal artery aneurysm at the same vertebral level presenting with subarachnoid hemorrhage. A 54-year-old man presented with sudden onset of headache. Computed tomography of the head showed subarachnoid hemorrhage. Diagnostic angiography revealed an epidural AVF located at the C1-2 level that was fed mainly by the dorsal somatic branches of the segmental arteries from the radicular artery and anterior spinal artery. This AVF drained only into the epidural veins without perimedullary venous reflux. Further, there was a 4-mm anterior spinal artery aneurysm in the vicinity of the fistula that was thought to be the cause of the hemorrhage. Endovascular transarterial fistulas embolization from the right radicular artery was performed to eliminate the AVF and to reduce hemodynamic stress on the aneurysm. No new symptoms developed after the treatment and discharged without neurological deficits. The aneurysm was noted to be reduced in size after the treatment and totally disappeared by 1 year later, according to follow-up angiography. Anterior spinal artery aneurysm from a separate vascular distribution may coexist with spinal epidural AVFs. In the setting of spinal subarachnoid hemorrhage, comprehensive imaging is indicated to rule out such lesions. Key Words: Aneurysm—anterior spinal artery—epidural arteriovenous fistula—subarachnoid hemorrhage— transarterial embolization. Ó 2014 by National Stroke Association
Spinal epidural arteriovenous fistulas (AVFs) are rare cervical spine vascular lesions, and they are generally thought to present with benign clinical symptoms, such From the *Department of Neurosurgery; and †Department of Radiology, Nara Medical University, Kashihara City, Japan. Received June 16, 2014; revision received July 6, 2014; accepted July 9, 2014. Address correspondence to Ichiro Nakagawa, MD, PhD, Department of Neurosurgery, Nara Medical University, 840 Shijocho, Kashihara City, Nara 634-8522, Japan. E-mail: nakagawa@ naramed-u.ac.jp. 1052-3057/$ - see front matter Ó 2014 by National Stroke Association http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2014.07.012
as radiculopathy.1-3 In some cases, spinal epidural AVF can cause acute paraplegia due to reflux into medullary veins with venous congestion.4-7 In patients with craniocervical dural AVF, subarachnoid hemorrhage has been reported to occur because of a direct venous drainage pattern in an intracranially or intramedullary fashion.8-12 However, hemorrhagic presentation of cervical spinal epidural AVF without intramedullary venous drainage is very rare. The present report describes a case of a patient with cervical spine epidural AVFs associated with anterior spinal artery aneurysm at the same vertebral level who presented with subarachnoid hemorrhage.
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Figure 1. (A) Axial computed tomography (CT) scan of the head showing subarachnoid hemorrhage and intraventricular hemorrhage. (B) Coronal CT scan of the cervical spine with contrast demonstrating anterior spinal artery aneurysm (arrowhead) and dilated epidural veins (arrow).
Case Report A 54-year-old man presented with sudden onset of severe headache and vomiting. A computed tomography scan of the head revealed a subarachnoid hemorrhage, mainly in the posterior fossa distribution and secondary hydrocephalus (Fig 1, A). Subsequent computed tomography angiogram of the head and neck to access for a vascular etiology revealed a vascular abnormality at the right C1/2 level and aneurysmal dilatation within the spinal canal at the C1/2 level (Fig 1, B). Magnetic resonance imaging demonstrated a signal defect and was strongly supportive of these findings. Comprehensive cerebral and spinal angiography was subsequently performed. Injection of the vertebral artery (VA) revealed an abnormally enlarged right radicular artery at the C1/2 level and multiple thin feeding arteries from the bilateral VA to the fistula (Fig 2, A and B). Furthermore, an anterior spinal artery aneurysm (4 3 2 mm in diameter) was located anteriorly within the spinal canal in the vicinity of the fistulas at the level of the C1/2 disc. The fistulas directly drained to the epidural veins and paravertebral venous plexus. Perimedullary venous reflux was not identified (Fig 2, C). These findings were consistent with a spinal epidural AVF at the C1/2 level and an anterior spinal artery aneurysm at the same level origin of the subarachnoid hemorrhage. We planned endovascular transarterial embolization to eliminate the fistulas and to reduce hemodynamic stress to the aneurysm, because it was deemed too difficult to access the anterior spinal artery aneurysm after discussing the case with the neurosurgical and endovascular teams. The endovascular procedure was performed 7 days after admission after obtaining written informed consent from the patient. Under local anesthesia with systemic heparinization to maintain the activated clotting time at levels above 2to 3-fold of the baseline value, a 7-Fr guiding catheter was inserted into the right femoral artery and guided into the right VA. Marathon flow directed microcatheters
(Covidien, Dublin, Ireland) were introduced into the main feeder as close to shunt points as possible through each guiding catheter. Right VA angiography revealed the aneurysm had enlarged (5 3 4 mm in diameter) compared with the aneurysm size seen during initial angiography (Fig 3, A). Transarterial embolization was performed from the main feeder right radial artery with a mixture of n-butyl cyanoacrylate and lipiodol. Avoiding retrograde distal migration of embolic material through other feeding arteries, balloon inflation was performed using a Hyperform balloon (Covidien) at the distal orifice of the main feeder of the right radial artery during embolization. Although transarterial embolization did not achieve complete occlusion of the fistulas due to the presence of other small feeding arteries, blood flow to the fistula was markedly reduced. Blood supply from anterior spinal artery to the fistula markedly reduced and there was an almost total disappearance of anterior spinal artery aneurysm without aneursymal stagnant appearance (Fig 3, B). The postoperative course was uneventful. No new neurologic symptoms developed, and ischemic lesions were not identified on diffusion-weighted images. Selective angiography performed 15 days later confirmed poor depiction of the anterior spinal artery aneurysm and fistulas. Selective angiography a year after the embolization revealed complete occlusion of the AVF and the aneurysm, preserving anterior spinal artery flow (Fig 3, C).
Discussion Spinal epidural AVFs are vascular anomalies that preferentially affect cervical portion and that are rare compared with spinal dural AVF. Several cases of cervical spinal epidural AVFs have been published in the literature, which are summarized in Table 1. Most cases are associated with perimedullary venous reflux causing congestive myelopathy.8-13 Hemorrhagic presentation with subarachnoid hemorrhage has only been reported
EPIDURAL AVF WITH SPINAL ARTERY ANEURYSM
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Figure 2. Right vertebral artery angiogram on admission. (A) Lateral view, (B) early phase of the right anterior oblique view, (C) late phase of the right anterior oblique view revealing epidural arteriovenous fistula with multiple feeding arteries from the vertebral artery (white arrowhead) and anterior spinal artery (white arrow). Anterior spinal artery aneurysm was identified in the vicinity of the fistula (black arrow). The fistulas directly drained to the paravertebral venous plexus (black arrowhead) without perimedullary venous reflux.
in one case (Case one) in the literature,10 but there was no description of the presence of ruptured aneurysm. Therefore, the present case is the first report of the concurrent existence of cervical epidural AVF and ruptured anterior spinal artery aneurysm. Unlike spinal dural AVFs, epidural AVFs are located in the ventral epidural space and are fed by multiple epidural branches and drain into the ventral epidural venous pouch. They are generally thought to present with benign clinical symptoms, such as radiculopathy.3 Geibprasert et al14 proposed a new classification of dural AVFs according to craniospinal epidural venous anatomy. Populations with ventral epidural group showed a female predominance, benign clinical presentation, and a lower rate of spinal cord venous reflux compared with lateral epidural group. The venous drainage route in the lateral epidural group, which includes typical spinal dural
AVFs, is always directed to the perimedullary veins; therefore, this type of AVF tends to be aggressive. The present case can be classified as a ventral epidural AVF because of the shunt location, which consists of mainly epidural drainage without perimedullary venous reflux. Furthermore, the shunt itself is asymptomatic. Kiyosue et al15 clearly described the classification of spinal ventral epidural AVFs of the lumbar spine based on the drainage type. Dorsal somatic branches, which supply the vertebral body, were the primary feeding branches to the epidural AVFs, forming a shunted pouch located in the ventral epidural space. They describe 3 types of venous drainage routes: the perimedullary venous drainage (PM), the paravertebral drainage (PV), and the combined perimedullary and paravertebral venous drainage. In PM-type AVFs, the epidural AVFs are shunted to an epidural venous pouch and then drained through the
Figure 3. Right vertebral angiogram before and after endovascular treatment. (A) Pre-embolization angiogram (right anterior oblique view) shows that the aneurysm enlarged to 5 3 4 mm in diameter (white arrow). (B) Angiogram after embolization (right anterior oblique view) did not achieve complete obliteration of the aneurysm (white arrow) but did result in marked reduction of blood flow to the fistula. (C) Angiography a year after the embolization reveals complete occlusion of the arteriovenous fistula and the aneurysm (white arrow), whereas anterior spinal artery flow is maintained (white arrowhead).
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Table 1. Reported cases of cervical spinal epidural arteriovenous fistula Author (y)
Age, y Sex
Neurology
1. Hemphill III (1998)
20
M SAH
2. Willinsky R (1993)
57
3. Goyal M (1999)
Site C1-2
Feeder
Drainer
Rt. VA branch
Epidural vein
M Radiculopathy, C3-4 myelopathy
VA, ascending cervical artery, TA
Epidural vein
68
M Myelopathy
C
4. Asai J (2001)
24
M Myelopathy
C5-T2
5. Suh DC (2004)
50
F
Myelopathy
C5
VA, thyrocervical Epidural vein artery PVVP Ascending cervical Epidural vein artery, deep cervical PVVP artery Costocervical artery, Epidural vein VA PVVP
6. Kawabori M (2009)
65
F
Radiculopathy C5-7
7. Castilla LR (2011) 8. Present case
57 54
M Myelopathy M SAH (ASA aneurysm)
C2-T1 C1-2
Treatment
Outcome
TAE/ Recovery, no surgery recurrence (67 mo) TAE Recovery, no recurrence (1 y) TAE Recovery TAE/ Recovery surgery TVE
Thyrocervical artery
PVVP, PMV
TAE
TA VA branches, ASA
Epidural vein Epidural vein
TVE TAE
Recovery, no recurrence (12 y) Recovery, no recurrence (1 y) Recovery, no recurrence (2.5 y)
Abbreviations: ASA, anterior spinal artery; F, female; M, male; PMV, perimedullary vein; PVVP, paravertebral venous plexus; Rt., right; SAH, subarachnoid hemorrhage; TA, thyroid artery; TAE, transarterial embolization; TVE, transvenous embolization; VA, vertebral artery. Reported cases of cervical spinal epidural arteriovenous fistula.
radiculomedullary vein into the perimedullary vein. The PV-type AVFs are drained via the radiculoemissary vein into the paravertebral veins. The present case can be classified as PV-type AVF, because the AVF was drained via the radiculoemissary vein into the paravertebral veins without perimedullary drainage. This is the first report of the concurrent existence of epidural AVF and anterior spinal artery aneurysm. An association of between dural AVFs and aneurysms has rarely been reported in the literature.16 As low-flow lesions, AVFs seldom produce sufficient hemodynamic stress on the arterial walls to induce aneurysm formation of feeding arteries. Sato et al17 described 9 cases of concurrent of dural AVFs and perimedullary AVFs at the craniocervical junction. In all the 9 cases, fistulas shared dilated perimedullary veins as a main drainage route, and 8 of 9 patients exhibited an arterial aneurysm on the distal side of the feeding arteries to the perimedullary AVF. The aneurysm in each case was intraoperatively confirmed as the bleeding point. They postulated that relatively high-flow dural AVFs cause a venous steal effect or venous hypoxia due to venous hypertension that, in combination with specific anatomic and hemodynamic factors, induces perimedullary AVF at the craniocervical junction. Unlike their cases, concurrent existence of epidural AVF and perimedullary AVF was not identified in the present case, and fistulas directly drained to epidural veins and the paravertebral venous plexus without perimedullary venous reflux. However, it is spec-
ulated that relatively high-flow epidural AVF may cause secondary anterior spinal arterial aneurysmal changes related to flow in the shunt. The therapeutic goal in the management of epidural AVFs is to obliterate the fistulous communication between the feeding artery and the draining vein by means of surgery or endovascular embolization. Most of the epidural AVFs classified with the PM-type venous drainage can be successfully treated by transarterial embolization with either Onyx or glue,18 although transvenous embolization or surgical resection may also be possible.13,14 The patient in the present case showed subarachnoid hemorrhage due to ruptured anterior spinal artery aneurysm in the vicinity of the epidural AVF, but he was treated by transarterial embolization from the right radicular artery. A surgical or endovascular approach to an anterior spinal artery aneurysm is difficult to access and is associated with a high risk of complications. Reduction of hemodynamic stress to feeding arteries from the anterior spinal artery might result in resolution of the aneurysm whereas preserving normal perfusion to the anterior spinal artery (Fig 4). However, there is a possibility of increase in hemodynamic stress to the aneurysm after transarterial embolization. Henkes et al19 reported that there is a direct relationship between pressure changes of feeding artery and degree of embolization in arteriovenous malformation. They concluded that pressure increases during embolization were relatively small compared with mean
EPIDURAL AVF WITH SPINAL ARTERY ANEURYSM
Figure 4. A schematic drawing of the vascular structure. Relatively highflow epidural arteriovenous fistula may cause secondary anterior spinal arterial aneurysmal changes related to flow in the shunt fed by ASA. Abbreviations: ASA, anterior spinal artery; VA, vertebral artery.
arterial systolic pressure; these pressure changes seemed unlikely to be the cause of periprocedural bleedings. This is the first description of cervical spine epidural AVFs associated with anterior spinal artery aneurysm at the same vertebral level in a patient who presented with subarachnoid hemorrhage. Although the long-term results of transarterial fistulas embolization remain to be evaluated, endovascular treatment to reduce hemodynamic stress to the aneurysm might be a useful treatment option to prevent rerupture and to induce obliteration of the aneurysm. In the setting of spinal subarachnoid hemorrhage, comprehensive imaging is indicated to rule out such lesions.
References 1. Clarke MJ, Patrick TA, White JB, et al. Spinal extradural arteriovenous malformations with parenchymal drainage: venous drainage variability and implications in clinical manifestations. Neurosurg Focus 2009;26:E5. 2. Hemphill JC 3rd, Smith WS, Halbach VV. Neurologic manifestations of spinal epidural arteriovenous malformations. Neurology 1998;50:817-819. 3. Lanzino G, D’Urso PI, Kallmes DF, et al. Onyx embolization of extradural spinal arteriovenous malformations with intradural venous drainage. Neurosurgery 2012; 70:329-333.
5 4. Kiyosue H, Tanoue S, Okahara M, et al. Spinal ventral epidural arteriovenous fistulas of the lumbar spine: angioarchitecture and endovascular treatment. Neuroradiology 2013;55:327-336. 5. Lim SM, Choi IS. Spinal epidural arteriovenous fistula: a unique pathway into the perimedullary vein. A case report. Interv Neuroradiol 2009;15:466-469. 6. Pirouzmand F, Wallace MC, Willinsky R. Spinal epidural arteriovenous fistula with intramedullary reflux. Case report. J Neurosurg 1997;87:633-635. 7. Reul J, Braun V. Spinal arteriovenous epidural fistula with acute paraplegia. Diagnosis and neurointerventional emergency treatment. A case report. Interv Neuroradiol 2007;13:75-78. 8. Asai J, Hayashi T, Fujimoto T, et al. Exclusively epidural arteriovenous fistula in the cervical spine with spinal cord symptoms: case report. Neurosurgery 2001; 48:1372-1375. discussion 1375-1376. 9. Chul Suh D, Gon Choi C, Bo Sung K, et al. Spinal osseous epidural arteriovenous fistula with multiple small arterial feeders converging to a round fistular nidus as a target of venous approach. AJNR Am J Neuroradiol 2004;25:69-73. 10. Goyal M, Willinsky R, Montanera W, et al. Paravertebral arteriovenous malformations with epidural drainage: clinical spectrum, imaging features, and results of treatment. AJNR Am J Neuroradiol 1999;20:749-755. 11. Patsalides A, Knopman J, Santillan A, et al. Endovascular treatment of spinal arteriovenous lesions: beyond the dural fistula. AJNR Am J Neuroradiol 2011;32:798-808. 12. Willinsky R, terBrugge K, Montanera W, et al. Spinal epidural arteriovenous fistulas: arterial and venous approaches to embolization. AJNR Am J Neuroradiol 1993;14:812-817. 13. Rangel-Castilla L, Holman PJ, Krishna C, et al. Spinal extradural arteriovenous fistulas: a clinical and radiological description of different types and their novel treatment with Onyx. J Neurosurg Spine 2011;15:541-549. 14. Geibprasert S, Pereira V, Krings T, et al. Dural arteriovenous shunts: a new classification of craniospinal epidural venous anatomical bases and clinical correlations. Stroke 2008;39:2783-2794. 15. Kawabori M, Hida K, Yano S, et al. Cervical epidural arteriovenous fistula with radiculopathy mimicking cervical spondylosis. Neurol Med Chir (Tokyo) 2009;49:108-113. 16. Krings T, Mull M, Bostroem A, et al. Spinal epidural arteriovenous fistula with perimedullary drainage. Case report and pathomechanical considerations. J Neurosurg Spine 2006;5:353-358. 17. Sato K, Endo T, Niizuma K, et al. Concurrent dural and perimedullary arteriovenous fistulas at the craniocervical junction: case series with special reference to angioarchitecture. J Neurosurg 2013;118:451-459. 18. Lai CW, Agid R, van den Berg R, et al. Cerebral arteriovenous fistulas induced by dural arteriovenous shunts. AJNR Am J Neuroradiol 2005;26:1259-1262. 19. Henkes H, Gotwald TF, Brew S, et al. Pressure measurements in arterial feeders of brain arteriovenous malformations before and after endovascular embolization. Neuroradiology 2004;46:673-677.
