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Gadolinium-enhanced MR angiography of spinal arteriovenous malformation
Journal of Clinical Imaging 28 (2004) 28 – 32
Gadolinium-enhanced MR angiography of spinal arteriovenous malformation Margaret H. Pui* Department of Radiology, Aga Khan University Hospital, PO Box 3500, Karachi, Pakistan Received 25 November 2002
Abstract Patients with spinal arteriovenous malformation (AVM) have progressive or fluctuating neurological dysfunction because of hemorrhage, venous hypertension, vascular steal phenomenon, or mass effect from venous varicosity. Spinal AVM is classified into four types based on angiographic and operative findings. Conventional diagnostic methods include magnetic resonance imaging (MRI), supine myelogram, and angiogram. MRI can localize the vascular nidus in the cord, but it may sometimes be normal. Spinal angiogram is the definitive diagnostic modality. It is technically demanding and time consuming, requiring catheterization of all spinal vascular pedicles. MR angiography is fast and multiplanar, and it may shorten the duration of catheter angiography by demonstrating the level of feeders. Images of MRI, magnetic resonance angiography (MRA), and catheter angiogram are presented to illustrate the correlation and diagnosis of spinal AVM. D 2004 Elsevier Inc. All rights reserved. Index terms: MR angiography; Magnetic resonance imaging; Spinal arteriovenous malformation; Arteriovenous fistula Keywords: MR angiography; Magnetic resonance imaging; Spinal arteriovenous malformation; Arteriovenous fistula
1. Introduction Magnetic resonance angiography (MRA) using gadolinium-enhanced time-of-flight (TOF) and phase-contrast (PC) methods has been successful in demonstrating spinal arteriovenous malformation (AVM). The examination is long, with an acquisition time of 4– 14 min [1 –6]. High-quality angiographic images of spinal AVM have been obtained by dynamic gadolinium-enhanced MRA [7 – 10]. This fast technique for demonstrating spinal AVM prior to conventional angiography is illustrated.
2. Methods Magnetic resonance imaging (MRI) and MRA were performed on four patients with suspected spinal AVM * Department of Radiology, McMaster University Medical Center, PO Box 2000, Station A, Hamilton, Ontario, Canada L8N 3Z5. Tel.: +1-905521-2100x73200; fax: +1-905-521-1390. E-mail address: [email protected] (M.H. Pui). 0899-7071/04/$ – see front matter D 2004 Elsevier Inc. All rights reserved. doi:10.1016/S0899-7071(03)00029-9
using a 1.5-T magnet system (Toshiba Visart, Tokyo, Japan) with a maximum gradient capacity of 17 mT/m and a slew rate of 23 mT/m/s. Unenhanced sagittal and axial spin – echo T1-weighted (285/15/90°/2; TR/TE/flip angle/excitation) and fast spin –echo T2-weighted (3000/ 120/90°/2) images, as well as gadolinium-enhanced sagittal and axial spin – echo T1-weighted images, were acquired using neck or spine coil. MRA was performed after intravenous bolus injection of 0.1 mmol/kg of gadolinium – DTPA by hand, followed by 20 ml of saline through an 18gauge cannula in an antecubital vein. Three-dimensional fast gradient – echo sequence (6.6/2.3/30°/1) was used to acquire three sets of breathhold sagittal or coronal MRA images. The matrix was 256 128 24 reconstructed to 512 256 48 partitions of 3-mm thickness; field of view was 13 – 21 24 –42 cm; and resolution was 1 – 1.6 mm. Acquisition time was 26 s for each of the three phases beginning 8 s after initiation of contrast injection. There was a delay of 8 s between each phase of acquisition to allow hyperventilation resulting in total examination time of 1 min 42 s. Maximum intensity projection was applied to the MRA images (Fig. 1).
M.H. Pui / Journal of Clinical Imaging 28 (2004) 28–32
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dorsal aspect of the lower thoracic spinal cord and conus medullaris. The vascular nidus is usually located on the dura of the proximal root sleeve in the neural foramen. One (Type IA) or more (Type IB) feeders arise from the dural branch of a radicular– medullary – dural artery. Intradural blood drainage by retrograde flow through the medullary vein results in the engorgement of coronal venous plexus and intraparenchymal radial veins. Type II intramedullary glomus-type AVM is usually supplied by the anterior spinal artery and drains into the coronal venous plexus (Figs. 2 and 3). Type III intramedullary juvenile-type AVM is fed by multiple arteries at different vertebral levels. It may have extramedullary, extradural, and extraspinal components (Fig. 4). Type IV extramedullary fistulas may be small
Fig. 1. A 25-year-old man with normal catheter angiogram and presumed cavernous hemangioma. (A) Sagittal T2-weighted MR image shows hyperintense cord lesion at T4 and CSF pulsation artifacts posterior to the cord. The lesion was also hyperintense on T1-weighted image (not shown). (B) Arterial phase of sagittal MRA demonstrates normal spinal branches of the posterior intercostal arteries as multiple thin transverse stripes at the intervetebral levels. (C) Venous phase of the MRA delineates anterior epidural venous plexus and basivertebral veins as single longitudinal and multiple transverse well-defined stripes posterior to and within the vertebral bodies. No abnormal intradural vessels are seen.
3. Discussion Patients with spinal AVM may present with progressive or fluctuating stocking or saddle paresthesia, bladder, bowel and sexual dysfunction, wasting of buttocks and lower extremities, loss of joint position sense, paraparesis, clonus, and increased deep tendon reflexes. Potential mechanisms for neurological dysfunction include hemorrhage, venous hypertension, vascular steal phenomenon, or mass effect from venous varicosity. Spinal AVM is classified into four types based on angiographic and operative findings. Type I dural arteriovenous fistula (AVF) is mainly found on the
Fig. 2. A 69-year-old woman with a small Type II intramedullary AVM. (A) Sagittal T2-weighted MR image shows diffuse T2 hyperintensity in the cord and flow voids along the cord surfaces. (B) Sagittal thoracic spinal MRA shows dilated posterior median vein (curved arrow) extending superiorly from L1 – L2. (C, D) Magnified views of the thoracolumbar junction demonstrate the feeding artery (straight arrow) arising from the L3 lumbar artery and the small fistula (double arrow) draining into the posterior median vein (curved arrow) at L1 – L2. (E, F ) Anteroposterior and lateral spinal angiogram shows the corresponding dilated vessels and the anterior spinal artery (arrowhead).
30
M.H. Pui / Journal of Clinical Imaging 28 (2004) 28–32
Fig. 2. (continued )
(IVA), intermediate-sized (IVB), or large (IVC) with one or more feeders [1]. Conventional diagnostic methods of spinal AVM include MRI, supine myelography, and angiography. MRI may be normal or shows cord swelling, low T1 and high T2 cord signals extending over several levels, scalloping of cord contours on sagittal images, flow voids on T2-weighted images and variable contrast enhancement of the cord [11]. MRI allows accurate anatomical localization of the vascular nidus in the cord. However, flow voids are frequently not present on MRI because of the dependence of signal intensity on scan parameters and flow velocity. Flow voids may also be spurious due to cerebrospinal fluid pulsation artifacts. Enhancement of the AVM on postcontrast T1-weighted images may be difficult to differentiate from metastases, normal enhancing vessels, and nerve roots. Supine myelogram has 90% sensitivity for detecting spinal AVM. However, tumor, arachnoiditis, and redundant nerve roots can also cause
serpiginous filling defects and mimic AVM on myelogram [1,4,5]. Spinal angiography is the definitive diagnostic modality. It is technically demanding and time consuming, requiring catheterization of all spinal vascular pedicles, intravenous injection of iodinated contrast, and high radiation exposure [5]. Normal epidural, medullary, anterior, and posterior median veins have been demonstrated on contrast-enhanced 3D TOF MRA as continuous stripes along the cord. AVM is suspected if large and increased number of vessels is seen on posterior surface of cord extending over several spinal segments in association with tortuous medullary vein [12]. TOF MRA is less useful in slow flow because signal from slow or saturated flow cannot be separated from that of stationary tissue [1]. PC MRA is more sensitive for detecting slow flow. Although the direction and velocity of flow can be determined, the value of flow velocity encoding has to be chosen prior to study. Normal intradural vessels are not visualized on PC MRA [1,3,6,13]. Both arterial and
M.H. Pui / Journal of Clinical Imaging 28 (2004) 28–32
31
venous structures are visualized without selectivity and temporal resolution on TOF and PC MRA [11]. Contrast-
Fig. 4. A 13-year-old girl with Type III intra- and extramedullary AVM involving the medulla and C1 – C2 spinal cord. (A) Coronal MRA and (B) anteroposterior left vertebral angiogram show arterial feeders arising from both vertebral arteries.
enhanced dynamic MRA exploits the flow-independent T1 shortening of gadolinium concentrated in the vascular space by bolus injection and yields high-quality T1-weighted images. The entire dilated vessels are visualized, and it is possible to distinguish artery and vein by time analysis and anatomical location. With phased-array coil, strong gradient coil, and fast acquisition sequence, MRA is a useful complement to MRI to demonstrate extent of intramedullary and perimedullary vessels. Feeding arteries of intramedullary AVM and level of intradural AVF have been shown on MRA and correlate with catheter angiography [7 –9]. MRA is also useful for follow-up after embolization with liquid adhesive and reduces the number of catheter angiography [10,14]. Fig. 3. A 25-year-old woman with a large Type II AVM. (A, B) Arterial and venous phases of sagittal spinal MRA show a large spinal branch of the T8 posterior intercostal artery (straight arrow) supplying the enlarged anterior spinal artery. The extramedullary AVM (n) at T12 – L1 is supplied by the anterior spinal artery and drains retrograde into the dilated posterior median vein and coronal venous plexus. Numerous distended intradural veins are also demonstrated in the lumbosacral spinal canal. (C, D) Anteroposterior and lateral spinal angiogram confirms the blood supply of the AVM by the left eighth intercostal artery through anterior spinal artery (curved arrow).
References [1] Gelbert F, Guichard JP, Mourier KL, Reizine D, Aymard A, Gobin P, George B, Cophignon J, Merland JJ. Phase-contrast MR angiography of vascular malformations of the spinal cord at 0.5 T. J Magn Reson Imaging 1992;2:631 – 6. [2] Mourier KL, Gelbert F, Reizine D, Gobin PT, Bongioanni F, George
32
[3]
[4]
[5]
[6]
[7]
[8]
M.H. Pui / Journal of Clinical Imaging 28 (2004) 28–32 B, Lot G, Merland JJ. Phase contrast magnetic resonance of the spinal cord: preliminary results in spinal cord arterio- venous malformations. Acta Neurochir (Wien) 1993;123:57 – 63. Provenzale JM, Tien RD, Felsberg G, Hacien-Bey L. Spinal dural arteriovenous fistula: demonstration using phase contrast MRA. J Comput Assist Tomogr 1994;18:811 – 4. Bowen BC, Fraser K, Kochan JP, Pattany PM, Green BA, Quencer RM. Spinal dural arteriovenous fistulas: evaluation with MR angiography. AJNR Am J Neuroradiol 1995;16:2029 – 43. Mascalchi M, Bianchi MC, Quilici N, Mangiafico S, Ferrito G, Padolecchia R, Bartolozzi C. MR angiography of spinal vascular malformations. AJNR Am J Neuroradiol 1995;16:289 – 97. Mascalchi M, Quilici N, Ferrito G, Mangiafico S, Scazzeri F, Torselli P, Petruzzi P, Cosottini M, Tessa C, Bartolozzi C. Identification of the feeding arteries of spinal vascular lesions via phase-contrast MR angiography with three-dimensional acquisition and phase display. AJNR Am J Neuroradiol 1997;18:351 – 8. Binkert CA, Kollias SS, Valavanis A. Spinal cord vascular disease: characterization with fast three-dimensional contrast-enhanced MR angiography. AJNR Am J Neuroradiol 1999;20:1785 – 93. Shigematsu Y, Korogi Y, Yoshizumi K, Kitajima M, Sugahara T,
[9]
[10]
[11]
[12]
[13] [14]
Liang L, Tang D, Takahashi M. Three cases of spinal dural AVF: evaluation with first-pass, gadolinium-enhanced, three-dimensional MR angiography. J Magn Reson Imaging 2000;12:949 – 52. Mascalchi M, Cosottini M, Ferrito G, Quilici N, Bartolozzi C, Villari N. Contrast-enhanced time-resolved MR angiography of spinal vascular malformations. J Comput Assist Tomogr 1999;23:341 – 5. Mascalchi M, Ferrito G, Quilici N, Mangiafico S, Cosottini M, Cellerini M, Politi LS, Guerrini L, Bartolozzi C, Villari N. Spinal vascular malformation: MR angiography after treatment. Radiology 2001;219:346 – 53. Minami S, Sagoh T, Nishimura K, Yamashita K, Fujisawa I, Noma S, Itoh K, Togashi K, Oda Y, Matsumoto M. Spinal arteriovenous malformation: MR imaging. Radiology 1988;169:109 – 15. Bowen BC, DePrima S, Pattany PM, Marcillo A, Madsen P, Quencer RM. MR angiography of normal intradural vessels of the thoracolumbar spine. AJNR Am J Neuroradiol 1996;17:483 – 94. Bowen BC, Pattany PM. MR angiography of the spine. Magn Reson Imaging Clin N Am 1998;6:165 – 78. Thorpe JW, Kendall BE, MacManus DG, McDonald W, Miller D. Dynamic gadolinium-enhanced MRI in the detection of spinal AVM. Neuroradiology 1994;36:522 – 5.
Gadolinium-enhanced MR angiography of spinal arteriovenous malformation Margaret H. Pui* Department of Radiology, Aga Khan University Hospital, PO Box 3500, Karachi, Pakistan Received 25 November 2002
Abstract Patients with spinal arteriovenous malformation (AVM) have progressive or fluctuating neurological dysfunction because of hemorrhage, venous hypertension, vascular steal phenomenon, or mass effect from venous varicosity. Spinal AVM is classified into four types based on angiographic and operative findings. Conventional diagnostic methods include magnetic resonance imaging (MRI), supine myelogram, and angiogram. MRI can localize the vascular nidus in the cord, but it may sometimes be normal. Spinal angiogram is the definitive diagnostic modality. It is technically demanding and time consuming, requiring catheterization of all spinal vascular pedicles. MR angiography is fast and multiplanar, and it may shorten the duration of catheter angiography by demonstrating the level of feeders. Images of MRI, magnetic resonance angiography (MRA), and catheter angiogram are presented to illustrate the correlation and diagnosis of spinal AVM. D 2004 Elsevier Inc. All rights reserved. Index terms: MR angiography; Magnetic resonance imaging; Spinal arteriovenous malformation; Arteriovenous fistula Keywords: MR angiography; Magnetic resonance imaging; Spinal arteriovenous malformation; Arteriovenous fistula
1. Introduction Magnetic resonance angiography (MRA) using gadolinium-enhanced time-of-flight (TOF) and phase-contrast (PC) methods has been successful in demonstrating spinal arteriovenous malformation (AVM). The examination is long, with an acquisition time of 4– 14 min [1 –6]. High-quality angiographic images of spinal AVM have been obtained by dynamic gadolinium-enhanced MRA [7 – 10]. This fast technique for demonstrating spinal AVM prior to conventional angiography is illustrated.
2. Methods Magnetic resonance imaging (MRI) and MRA were performed on four patients with suspected spinal AVM * Department of Radiology, McMaster University Medical Center, PO Box 2000, Station A, Hamilton, Ontario, Canada L8N 3Z5. Tel.: +1-905521-2100x73200; fax: +1-905-521-1390. E-mail address: [email protected] (M.H. Pui). 0899-7071/04/$ – see front matter D 2004 Elsevier Inc. All rights reserved. doi:10.1016/S0899-7071(03)00029-9
using a 1.5-T magnet system (Toshiba Visart, Tokyo, Japan) with a maximum gradient capacity of 17 mT/m and a slew rate of 23 mT/m/s. Unenhanced sagittal and axial spin – echo T1-weighted (285/15/90°/2; TR/TE/flip angle/excitation) and fast spin –echo T2-weighted (3000/ 120/90°/2) images, as well as gadolinium-enhanced sagittal and axial spin – echo T1-weighted images, were acquired using neck or spine coil. MRA was performed after intravenous bolus injection of 0.1 mmol/kg of gadolinium – DTPA by hand, followed by 20 ml of saline through an 18gauge cannula in an antecubital vein. Three-dimensional fast gradient – echo sequence (6.6/2.3/30°/1) was used to acquire three sets of breathhold sagittal or coronal MRA images. The matrix was 256 128 24 reconstructed to 512 256 48 partitions of 3-mm thickness; field of view was 13 – 21 24 –42 cm; and resolution was 1 – 1.6 mm. Acquisition time was 26 s for each of the three phases beginning 8 s after initiation of contrast injection. There was a delay of 8 s between each phase of acquisition to allow hyperventilation resulting in total examination time of 1 min 42 s. Maximum intensity projection was applied to the MRA images (Fig. 1).
M.H. Pui / Journal of Clinical Imaging 28 (2004) 28–32
29
dorsal aspect of the lower thoracic spinal cord and conus medullaris. The vascular nidus is usually located on the dura of the proximal root sleeve in the neural foramen. One (Type IA) or more (Type IB) feeders arise from the dural branch of a radicular– medullary – dural artery. Intradural blood drainage by retrograde flow through the medullary vein results in the engorgement of coronal venous plexus and intraparenchymal radial veins. Type II intramedullary glomus-type AVM is usually supplied by the anterior spinal artery and drains into the coronal venous plexus (Figs. 2 and 3). Type III intramedullary juvenile-type AVM is fed by multiple arteries at different vertebral levels. It may have extramedullary, extradural, and extraspinal components (Fig. 4). Type IV extramedullary fistulas may be small
Fig. 1. A 25-year-old man with normal catheter angiogram and presumed cavernous hemangioma. (A) Sagittal T2-weighted MR image shows hyperintense cord lesion at T4 and CSF pulsation artifacts posterior to the cord. The lesion was also hyperintense on T1-weighted image (not shown). (B) Arterial phase of sagittal MRA demonstrates normal spinal branches of the posterior intercostal arteries as multiple thin transverse stripes at the intervetebral levels. (C) Venous phase of the MRA delineates anterior epidural venous plexus and basivertebral veins as single longitudinal and multiple transverse well-defined stripes posterior to and within the vertebral bodies. No abnormal intradural vessels are seen.
3. Discussion Patients with spinal AVM may present with progressive or fluctuating stocking or saddle paresthesia, bladder, bowel and sexual dysfunction, wasting of buttocks and lower extremities, loss of joint position sense, paraparesis, clonus, and increased deep tendon reflexes. Potential mechanisms for neurological dysfunction include hemorrhage, venous hypertension, vascular steal phenomenon, or mass effect from venous varicosity. Spinal AVM is classified into four types based on angiographic and operative findings. Type I dural arteriovenous fistula (AVF) is mainly found on the
Fig. 2. A 69-year-old woman with a small Type II intramedullary AVM. (A) Sagittal T2-weighted MR image shows diffuse T2 hyperintensity in the cord and flow voids along the cord surfaces. (B) Sagittal thoracic spinal MRA shows dilated posterior median vein (curved arrow) extending superiorly from L1 – L2. (C, D) Magnified views of the thoracolumbar junction demonstrate the feeding artery (straight arrow) arising from the L3 lumbar artery and the small fistula (double arrow) draining into the posterior median vein (curved arrow) at L1 – L2. (E, F ) Anteroposterior and lateral spinal angiogram shows the corresponding dilated vessels and the anterior spinal artery (arrowhead).
30
M.H. Pui / Journal of Clinical Imaging 28 (2004) 28–32
Fig. 2. (continued )
(IVA), intermediate-sized (IVB), or large (IVC) with one or more feeders [1]. Conventional diagnostic methods of spinal AVM include MRI, supine myelography, and angiography. MRI may be normal or shows cord swelling, low T1 and high T2 cord signals extending over several levels, scalloping of cord contours on sagittal images, flow voids on T2-weighted images and variable contrast enhancement of the cord [11]. MRI allows accurate anatomical localization of the vascular nidus in the cord. However, flow voids are frequently not present on MRI because of the dependence of signal intensity on scan parameters and flow velocity. Flow voids may also be spurious due to cerebrospinal fluid pulsation artifacts. Enhancement of the AVM on postcontrast T1-weighted images may be difficult to differentiate from metastases, normal enhancing vessels, and nerve roots. Supine myelogram has 90% sensitivity for detecting spinal AVM. However, tumor, arachnoiditis, and redundant nerve roots can also cause
serpiginous filling defects and mimic AVM on myelogram [1,4,5]. Spinal angiography is the definitive diagnostic modality. It is technically demanding and time consuming, requiring catheterization of all spinal vascular pedicles, intravenous injection of iodinated contrast, and high radiation exposure [5]. Normal epidural, medullary, anterior, and posterior median veins have been demonstrated on contrast-enhanced 3D TOF MRA as continuous stripes along the cord. AVM is suspected if large and increased number of vessels is seen on posterior surface of cord extending over several spinal segments in association with tortuous medullary vein [12]. TOF MRA is less useful in slow flow because signal from slow or saturated flow cannot be separated from that of stationary tissue [1]. PC MRA is more sensitive for detecting slow flow. Although the direction and velocity of flow can be determined, the value of flow velocity encoding has to be chosen prior to study. Normal intradural vessels are not visualized on PC MRA [1,3,6,13]. Both arterial and
M.H. Pui / Journal of Clinical Imaging 28 (2004) 28–32
31
venous structures are visualized without selectivity and temporal resolution on TOF and PC MRA [11]. Contrast-
Fig. 4. A 13-year-old girl with Type III intra- and extramedullary AVM involving the medulla and C1 – C2 spinal cord. (A) Coronal MRA and (B) anteroposterior left vertebral angiogram show arterial feeders arising from both vertebral arteries.
enhanced dynamic MRA exploits the flow-independent T1 shortening of gadolinium concentrated in the vascular space by bolus injection and yields high-quality T1-weighted images. The entire dilated vessels are visualized, and it is possible to distinguish artery and vein by time analysis and anatomical location. With phased-array coil, strong gradient coil, and fast acquisition sequence, MRA is a useful complement to MRI to demonstrate extent of intramedullary and perimedullary vessels. Feeding arteries of intramedullary AVM and level of intradural AVF have been shown on MRA and correlate with catheter angiography [7 –9]. MRA is also useful for follow-up after embolization with liquid adhesive and reduces the number of catheter angiography [10,14]. Fig. 3. A 25-year-old woman with a large Type II AVM. (A, B) Arterial and venous phases of sagittal spinal MRA show a large spinal branch of the T8 posterior intercostal artery (straight arrow) supplying the enlarged anterior spinal artery. The extramedullary AVM (n) at T12 – L1 is supplied by the anterior spinal artery and drains retrograde into the dilated posterior median vein and coronal venous plexus. Numerous distended intradural veins are also demonstrated in the lumbosacral spinal canal. (C, D) Anteroposterior and lateral spinal angiogram confirms the blood supply of the AVM by the left eighth intercostal artery through anterior spinal artery (curved arrow).
References [1] Gelbert F, Guichard JP, Mourier KL, Reizine D, Aymard A, Gobin P, George B, Cophignon J, Merland JJ. Phase-contrast MR angiography of vascular malformations of the spinal cord at 0.5 T. J Magn Reson Imaging 1992;2:631 – 6. [2] Mourier KL, Gelbert F, Reizine D, Gobin PT, Bongioanni F, George
32
[3]
[4]
[5]
[6]
[7]
[8]
M.H. Pui / Journal of Clinical Imaging 28 (2004) 28–32 B, Lot G, Merland JJ. Phase contrast magnetic resonance of the spinal cord: preliminary results in spinal cord arterio- venous malformations. Acta Neurochir (Wien) 1993;123:57 – 63. Provenzale JM, Tien RD, Felsberg G, Hacien-Bey L. Spinal dural arteriovenous fistula: demonstration using phase contrast MRA. J Comput Assist Tomogr 1994;18:811 – 4. Bowen BC, Fraser K, Kochan JP, Pattany PM, Green BA, Quencer RM. Spinal dural arteriovenous fistulas: evaluation with MR angiography. AJNR Am J Neuroradiol 1995;16:2029 – 43. Mascalchi M, Bianchi MC, Quilici N, Mangiafico S, Ferrito G, Padolecchia R, Bartolozzi C. MR angiography of spinal vascular malformations. AJNR Am J Neuroradiol 1995;16:289 – 97. Mascalchi M, Quilici N, Ferrito G, Mangiafico S, Scazzeri F, Torselli P, Petruzzi P, Cosottini M, Tessa C, Bartolozzi C. Identification of the feeding arteries of spinal vascular lesions via phase-contrast MR angiography with three-dimensional acquisition and phase display. AJNR Am J Neuroradiol 1997;18:351 – 8. Binkert CA, Kollias SS, Valavanis A. Spinal cord vascular disease: characterization with fast three-dimensional contrast-enhanced MR angiography. AJNR Am J Neuroradiol 1999;20:1785 – 93. Shigematsu Y, Korogi Y, Yoshizumi K, Kitajima M, Sugahara T,
[9]
[10]
[11]
[12]
[13] [14]
Liang L, Tang D, Takahashi M. Three cases of spinal dural AVF: evaluation with first-pass, gadolinium-enhanced, three-dimensional MR angiography. J Magn Reson Imaging 2000;12:949 – 52. Mascalchi M, Cosottini M, Ferrito G, Quilici N, Bartolozzi C, Villari N. Contrast-enhanced time-resolved MR angiography of spinal vascular malformations. J Comput Assist Tomogr 1999;23:341 – 5. Mascalchi M, Ferrito G, Quilici N, Mangiafico S, Cosottini M, Cellerini M, Politi LS, Guerrini L, Bartolozzi C, Villari N. Spinal vascular malformation: MR angiography after treatment. Radiology 2001;219:346 – 53. Minami S, Sagoh T, Nishimura K, Yamashita K, Fujisawa I, Noma S, Itoh K, Togashi K, Oda Y, Matsumoto M. Spinal arteriovenous malformation: MR imaging. Radiology 1988;169:109 – 15. Bowen BC, DePrima S, Pattany PM, Marcillo A, Madsen P, Quencer RM. MR angiography of normal intradural vessels of the thoracolumbar spine. AJNR Am J Neuroradiol 1996;17:483 – 94. Bowen BC, Pattany PM. MR angiography of the spine. Magn Reson Imaging Clin N Am 1998;6:165 – 78. Thorpe JW, Kendall BE, MacManus DG, McDonald W, Miller D. Dynamic gadolinium-enhanced MRI in the detection of spinal AVM. Neuroradiology 1994;36:522 – 5.