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Advances in 3D angiography for spinal vascular malformations
Journal of Clinical Neuroscience xxx (xxxx) xxx
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Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical study
Advances in 3D angiography for spinal vascular malformations Stephanie H. Chen ⇑, Samir Sur, Marie-Christine Brunet, Jason Liounakos, David McCarthy, Dallas Sheinberg, Allan D. Levi, Robert M. Starke Department of Neurological Surgery, University of Miami Miller School of Medicine, Miami, FL, USA
a r t i c l e
i n f o
Article history: Received 10 October 2019 Accepted 5 January 2020 Available online xxxx Keywords: Spinal angiography 3D imaging Vascular malformation Endovascular Spinal fistula
a b s t r a c t Spinal vascular malformations are difficult to diagnose lesions that can be associated with significant permanent morbidity. The angioarchitecture of spinal vascular anatomy and the associated pathologies have only recently been illuminated by the advent of spinal angiography. However, conventional spinal digital subtraction angiography is often limited by significant variability, overlapping vessels, as well as an inability to understand the precise location of the nidus or fistula in relation to the spinal cord and spine. In this study, we present 4 unique cases wherein 3-dimensional rotational angiography (3DRA) with dual volume acquisition was useful in defining the anatomy of spinal fistulas as well as planning treatment. Ó 2020 Elsevier Ltd. All rights reserved.
1. Introduction The first spinal vascular malformation was described by J. Gaupp in 1888 as a ‘‘cluster of hemorrhoids” on the surface of the spinal cord [1]. However a precise understanding of the angioarchitecture of the spinal cord vasculature did not occur until the development of selective spinal angiography by Djindijan, Di Chiro, Doppman [2–4]. More recently 3D rotational angiography with dual volume acquisition has enabled reconstruction of bony/metallic structures simultaneously with macro and microvascular anatomy. This has given surgeons the unprecedented ability to visualize the precise anatomic relationships that exist between spinal vascular malformations and the bony spinal canal leading to improved preoperative planning and more efficient surgical treatment [5]. In this case series, we describe the benefit of 3-dimensional rotational angiography (3DRA) in the diagnosis and treatment of vascular malformations of the spine including spinal dural arteriovenous fistulas (SDAVF), spinal epidural fistulas (SEAVF), and perimedullary fistulas. 2. Methods 2.1. Conventional digital subtraction angiography Between 2018 and 2019, four patients underwent 3D DRA for evaluation of spinal vascular lesions at our institution. All four
patients underwent conventional selective spinal angiography under general anesthesia. The Siemens Artis Q Biplane was used for all procedures with a 512 512 pixel matrix system. Spinal segmental vessels were selected with a 5French Cobra catheter (Terumo, Somerset, NJ) and AP monoplanar digital subtraction angiography (DSA) was performed. Biplane AP and lateral biplane angiography was also performed in specific vessels of interest. 2.2. 3D rotational spinal angiography Data were acquired in a 512 512 matrix with a 20-second acquisition protocol under apnea was performed through a 200° rotation of the C-arm. A 2.5 mL/s injection of the artery of interest was performed with injection of 300 mgI/mL nonionic contrast medium at a pressure of 600 psi after an X-ray delay of 2 s. This 120 frames study was then transferred to a Siemens Syngo Workstation in native format and processed by experienced neuroradiology technicians with the assistance of the operating interventionalists (SC, MCB, RS). Reconstructed images, including maximum intensity projection images, shaded surface-rendered displays, and volumerendered displays with adjustable transparency of various structures, as well as full stereoscopic capabilities, were used to study the anatomic relationships demonstrated on these images. 3. Cases 3.1. Case 1
⇑ Corresponding author at: Department of Neurological Surgery, University of Miami Miller School of Medicine, 1095 NW Terrace, Miami, FL 33136, USA. E-mail address: [email protected] (S.H. Chen).
A 64-year-old man with history of right lumbosacral pain presented to the emergency department with a new onset of bilateral
https://doi.org/10.1016/j.jocn.2020.01.013 0967-5868/Ó 2020 Elsevier Ltd. All rights reserved.
Please cite this article as: S. H. Chen, S. Sur, M. C. Brunet et al., Advances in 3D angiography for spinal vascular malformations, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2020.01.013
2
S.H. Chen et al. / Journal of Clinical Neuroscience xxx (xxxx) xxx
leg weakness one week following a lumbar epidural steroid injection. MRI demonstrated T2 signal change representing spinal cord edema and flow voids posteriorly. DSA demonstrated a Type 4 perimedullary fistula at the T10-T11 level, which was fed by a distal branch off the L1 radiculomedullary artery. 3D rotational angiography was used to clarify intradural location of the fistulous point that was several levels above the selectively catheterized segmental vessel [Fig. 1]. The patient was brought to the operating room for a focal T10-11 partial laminectomy for surgical clipping of the fistula. DSA was performed postoperatively demonstrating complete obliteration of the fistula. Subsequent follow-up three months later revealed a marked improvement in the patient’s symptoms. 3.2. Case 2 A 56-year-old female presented with 10 days of acute onset severe lower back pain and an MRI demonstrating a ventral epidural fluid collection spanning T12 to L3 with an associated flow void at L1. The patient was neurologically intact with no evidence of myelopathy. DSA showed a hypervascular network of small tortuous vessels eccentric to the right at L1 with main feeders from T12 and L1 segmental arteries. Prominent early filling of right-sided epidural veins suggestive of arteriovenous shunting was seen. 3D rotational angiography demonstrated pure epidural fistula without intradural component. Successful embolization of this epidural spinal AVM fed by bilateral T12 and L1 segmental vessels was performed without complication [Fig. 2]. The patient was discharged in intact neurological condition and repeat DSA performed five months later demonstrated complete obliteration of the lesion. 3.3. Case 3 A 58-year-old male initially presented with severe neurogenic claudication and radiographic evidence of significant scoliosis and spinal stenosis. He underwent an L2 to S1 decompression and interbody fusion with improvement in his symptoms at three months follow up. Eight months postoperatively however he returned to clinic with progressive worsening balance, lower extremity parasthesias, frank urinary incontinence, and worsening
erectile dysfunction. The patient’s neurologic exam was significant for worsening of bilateral lower extremity weakness, a T11 sensory level, and diminished vibration and proprioception in the lower extremities without hyperreflexia. An MRI of the thoracolumbar spine demonstrated high T2 signal from T7 to the conus with numerous dorsal flow voids. DSA confirmed the presence of a dural arteriovenous fistula fed by the left L3 radicular artery with a large left-sided epidural component as well as intradural venous drainage [Fig. 3A]. The study was limited due to hardware artifact, however the location of the fistulous point at the L3 nerve root sleeve became clear upon performing 3D rotational angiography [Fig. 3]. The patient was brought to the operating room for revision of the laminectomy/facetectomy with careful and focal removal of epidural scar and abnormal fistulous vessels consisting of arterialized veins at the dorsolateral aspect of thecal sac and along the exiting left L3 nerve root. A small dural opening was utilized to cauterize and divide the intradural draining vein as well. The specific localization of the lesion in relation to the spinal titanium implants enabled minimization of epidural scar lysis and thereby reduced the risk of unintended durotomies, which can complicate such operations. At three months follow-up, he was doing well with improved bladder control and lower extremity weakness but persistent sensory and balance disturbances.
3.4. Case 4 A 46-year-old male presented with 5 months of progressively worsening numbness and parasthesias of his lower extremities, bowel and bladder incontinence and subtle lower extremity weakness bilaterally. On physical exam he had subtle 4+/5 weakness diffusely throughout the lower extremities with a T10 sensory level and hyperreflexia. MRI demonstrated prominent thoracic flow voids with abnormal spinal cord expansion and T2 hyperintensity from T6 to T11 [Fig. 4A]. DSA confirmed the presence of a Type I dural arteriovenous fistula fed by the right T8 radicular artery with significant venous congestion and prominent perimedullary veins draining both superiorly and inferiorly. A 3DRA was performed which localized the fistulous point to the T8 nerve root region
Fig. 1. (A) T2 MRI demonstrating cord edema from T8 to L1 (B) AP view of right L1 injection showing the perimedullary AV fistula with shunting point located 2 levels above the injected level and opacification of the epidural venous plexus. (C) Axial and (D) Coronal 3DRA reconstruction demonstrating location of perimedullary fistula on the posterior surface of the spinal cord located between the T10 and T11 rib articulations.
Please cite this article as: S. H. Chen, S. Sur, M. C. Brunet et al., Advances in 3D angiography for spinal vascular malformations, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2020.01.013
S.H. Chen et al. / Journal of Clinical Neuroscience xxx (xxxx) xxx
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Fig. 2. (A) Sagittal and (B) axial T2 MRI demonstrating epidural hematoma along the ventral aspect of the spinal canal from T11-L3 causing mild sac compression at L1. There is also a linear flow void demonstrating a prominent vein at the L1 level. (C) AP view of right L1 injection also contributing to this epidural fistula. (D) 3D rotational angiography with bony reconstruction clarifies relationship of ventral epidural venous drainage with bony elements. Drainage occurs ventrolateral intraosseous routes and the lateral extra-spinal plexus.
Fig. 3. (A) Oblique view of left L3 injection demonstrating vascular malformation with AV shunting and early draining vein projecting superiorly. (B) Axial and (C) lateral and (D) down-the-barrel view of 3DRA demonstrating epidural and intradural components of venous drainage of spinal fistula in relationship to the left L3 pedicle screw as well as intradural component with connection to the posterior coronal venous plexus.
below the right T8 pedicle [Fig. 4]. The patient was taken to the operating room and T7 and T8 laminectomy were performed. The draining vein was identified and ligated as it emerged from the dural root sleeve. Three months postoperatively, the patient’s bladder symptoms were significantly improved and he was intact on neurological examination.
4. Discussion Spinal arteriovenous fistulas are rare, under-diagnosed entities that can lead to substantial morbidity with progressive myelopathy. Spinal dural fistulas (SDAVF) are the most common spinal vascular malformation, with type 1 lesions typically consisting of a pathological communication between a posterior radicular branch of the segmental artery and radicular vein in the dura of the nerve root sleeve [6,7]. Arterialized pressure within the fistulous radiculomedullary vein leads to retrograde drainage into the coronal perimedullary venous plexus, a reversal of the normal centrifugal drainage leading to a congestive myelopathy, often distant from
the fistula itself. Thus, symptoms and cord edema on MRI often do not correlate with the actual location of the fistula. A conventional MRI may demonstrate dilated spinal vessels and cord edema in cases of SDAVF, but cannot clearly differentiate between arteries and veins. Spinal angiography is beneficial to localize the fistulous point, which is typically singular, despite a ‘‘nidus” like appearances with involvement of multiple feeders and the complex of numerous dilated perimedullary veins. The fistulous point is identified on spinal angiography by a caliber change between the feeding vessel and draining vein. However, unlike MRI, which can elucidate the anatomic relationships surrounding the vascular malformation, conventional angiography is limited in determining the anatomic relationships surrounding the vascular malformation due to overlapping vessels, bone, or instrumentation as in Case 3 in our series. The overlapping structures often necessitate AP and lateral biplane angiography in multiple oblique angles to visualize the fistulous point, which can be difficult to interpret. With 3DRA reconstructions, the bony anatomy or instrumentation can be rotated and used as landmarks to precisely localize the nerve root sleeve in which the fistula will be found during
Please cite this article as: S. H. Chen, S. Sur, M. C. Brunet et al., Advances in 3D angiography for spinal vascular malformations, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2020.01.013
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S.H. Chen et al. / Journal of Clinical Neuroscience xxx (xxxx) xxx
Fig. 4. (A) Sagittal T2 MRI demonstrating cord edema from T8-T12. (B) AP view of right T8 segmental artery injection with dural AV fistula and spinal venous congestion. (C) Coronal (D) axial and (E) sagittal 3DRA demonstrating the posterior radicular artery coursing underneath the right T8 pedicle with the draining vein anastomosing with the posterior coronal venous plexus. Bony anatomical reconstructions show precise location of fistula in the T8 transverse foramen.
surgical obliteration, thus increasing the efficiency and safety of the procedure by minimalizing the operative exposure necessary. Additionally, Suh et al report a series of 13 patients wherein spinal 3DRA was used to identify multiple feeders in cases of SDAVF [8]. Conventional angiography is also limited by its ability to clearly delineate the location of the pathological vessels in relation to the spinal cord and dura. While more rare, both spinal epidural fistulas and perimedullary fistulas can present with similar symptoms to spinal dural arteriovenous fistulas. In Case 1, 3DRA localized the fistula supply to a spinal pial artery on the dorsal surface of the cord between the T10 and T11 pedicles. Although most patients with perimedullary fistulas also typically present with venous congestive myelopathy, perimedullary fistulas have a higher risk for hemorrhage than the more common SDAVF [9,10]. Additionally, appropriate identification of perimedullary fistulas has important treatment implications. From an endovascular perspective, catheterization and treatment of pial arteries carries significantly higher risk as these fistulas are often fed from the anterior spinal artery [11]. From a surgical perspective, perimedullary fistulas range from slow flow shunts with single feeders to high flow shunts with multiple feeders. They are often ventral in location and require more posterolateral approaches or even corpectomy to adequately access the fistula [6,12,13]. In such cases, 3DRA is a valuable tool in localizing the fistulous point and planning the degree of bony decompression needed. Here, a focal laminectomy was performed between T10-T11 despite DSA revealing that the L1 segmental artery was supplying the fistula, thus sparing the thoracolumbar junction and providing an important minimization of bony and ligamentous disruption which can result in kyphosis and hasten the onset of degenerative disease in this region. Spinal epidural fistulas (SEAVF) are a rare entity wherein the arteriovenous shunt lies in the epidural space. In the absence of intradural drainage, SEAVF may only cause symptoms of mass effect or an acute hematoma [14]. However, SEAVF may also lead to perimedullary reflux, mimicking a SDAVF. Recognizing the distinction between these two types of fistulas is important for choos-
ing the appropriate treatment strategy. In the case of SDAVF it is sufficient to occlude the feeding artery at the fistulous point. However, in cases of SEAVF with intradural drainage, surgical disconnection of the radicular vein from the epidural plexus is recommended to prevent reflux into perimedullary veins in the case of reconstitution of the epidural fistula at a different level [15]. In Case 2, the 3DRA clarified that venous outflow was purely epidural and ventrally located, solidifying our decision to treat by endovascular embolization and aiding selection of the most optimal working views during the procedure. Disadvantages of 3DRA with respect to DSA include the higher contrast load per acquisitioned run (50 versus 6–8 mL), longer acquisition time (20 s vs 5 s), and increased patient radiation dose. 3DRA also requires increased time for post-processing review of the data at an external workstation including data transfer, reconstruction, and anatomic analysis. However, total patient contrast load, radiation dose, and treatment time can be decreased if 3DRA negates the need for multiple angles, and biplane angiography runs [5]. Spatial resolution can also be limited in 3DRA. However, 3DRA spinal images can also be reconstructed from flat panel CT angiotomography. This technology offers higher dynamic range and digital readout rates, achieving higher contrast and spatial resolutions than conventional angiography in any desired plane [16]. Another limitation of 3DRA includes the lack of temporal resolution compared to conventional DSA, particularly in the case of spinal arteriovenous malformations (AVM). However, with the increasing use of 4D DRA for cerebral AVM, this technology will likely be adaptable to spinal AVM evaluation as well [17].
5. Conclusion Conventional spinal angiography has provided a better understanding of the angioarchitecture of the spinal cord as well as the various vascular malformations associated with it, but is limited by its ability to clearly demonstrate the spatial relationships with
Please cite this article as: S. H. Chen, S. Sur, M. C. Brunet et al., Advances in 3D angiography for spinal vascular malformations, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2020.01.013
S.H. Chen et al. / Journal of Clinical Neuroscience xxx (xxxx) xxx
the surrounding anatomy. Spinal 3DRA combines high-resolution angiography with relevant 3-dimensional adjacent anatomy in a way that improves preoperative treatment planning and should be considered in all cases of complex spinal vascular malformations.
6. Disclosures None of the authors have any significant disclosures or perceived conflicts of interest with the current work. RMS research is supported by the NREF, Joe Niekro Foundation, Brain Aneurysm Foundation, Bee Foundation, and by National Institute of Health (UL1TR002736, KL2TR002737) through the Miami Clinical and Translational Science Institute, from the National Center for Advancing Translational Sciences and the National Institute on Minority Health and Health Disparities. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the NIH. RMS has consulting and teaching agreements with Penumbra, Abbott, Medtronic, InNeuroCo and Cerenovus. All authors contributed to conception and design, acquisition, analysis, interpretation of data, drafting the article, and final approval. We confirm that manuscript complies with all instructions to authors. We confirm that authorship requirements have been met and the final manuscript was approved by all authors. We confirm that this manuscript has not been published elsewhere and is not under consideration by another journal.
Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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References [1] Gaupp J. Hamorrhoiden der pia mater spinalis im gebiet des lendenmarks. Beitr Pathol 1888;2:516–8. [2] Djindjian R. Angiography of the spinal cord. University Park Press; 1970. [3] Di Chiro G, Doppman J, Ommaya AK. Selective arteriography of arteriovenous aneurysms of spinal cord. Radiology 1967;88:1065–77. [4] Doppman JL. Arteriography of the spinal cord. Semin Roentgenol 1972;7:231–9. [5] Prestigiacomo C, Niimi Y, Setton A, Berenstein A. Three-dimensional rotational spinal angiography in the evaluation and treatment of vascular malformations. Am J Neuroradiol 2003. [6] Kim LJ, Spetzler RF. Classification and surgical management of spinal arteriovenous lesions: arteriovenous fistulae and arteriovenous malformations. Neurosurgery 2006;59. S195-201; discussion S3-13. [7] Miyasaka K, Asano T, Ushikoshi S, Hida K, Koyanagi I. Vascular anatomy of the spinal cord and classification of spinal arteriovenous malformations. Interv Neuroradiol 2000;6(Suppl 1):195–8. [8] Suh DC, Kim HS, Baek H-J, Park JW, Kim KK, Rhim SC. Angioarchitecture of spinal dural arteriovenous fistula - evaluation with 3D rotational angiography. Neurointervention 2012;7:10–6. [9] Gandhi D, Chen J, Pearl M, Huang J, Gemmete JJ, Kathuria S. Intracranial dural arteriovenous fistulas: classification, imaging findings, and treatment. Am J Neuroradiol 2012;33:1007–13. [10] Barrow DL, Colohan ART, Dawson R. Intradural perimedullary arteriovenous fistulas (Type IV spinal cord arteriovenous malformations). Childs Nerv Syst 1994;81:221. [11] Gross BA, Du R. Spinal pial (type IV) arteriovenous fistulae: a systematic pooled analysis of demographics, hemorrhage risk, and treatment results. Neurosurgery 2013;73:141–51. discussion 51. [12] Hida K, Iwasaki Y, Ushikoshi S, Fujimoto S, Seki T, Miyasaka K. Corpectomy: a direct approach to perimedullary arteriovenous fistulas of the anterior cervical spinal cord. J Neurosurg 2002;96:157–61. [13] Martin NA, Khanna RK, Batzdorf U. Posterolateral cervical or thoracic approach with spinal cord rotation for vascular malformations or tumors of the ventrolateral spinal cord. J Neurosurg 1995;83:254–61. [14] Huang W, Gross BA, Du R. Spinal extradural arteriovenous fistulas. J Neurosurg Spine 2013;19:582. [15] Zozulya YP, Slin’ko EI, Al II Q. Spinal arteriovenous malformations: new classification and surgical treatment. Neurosurg Focus 2006;20:E7. [16] Chen J, Ethiati T, Gailloud P. Flat panel catheter angiotomography of the spinal venous system: an enhanced venous phase for spinal digital subtraction angiography. Am J Neuroradiol 2012;33:1875–81. [17] Sandoval-Garcia C, Royalty K, Yang P, Niemann D, Ahmed A, Aagaard-Kienitz B, et al. 4D DSA a new technique for arteriovenous malformation evaluation: a feasibility study. J Neurointerv Surg 2016;8:300–4.
Please cite this article as: S. H. Chen, S. Sur, M. C. Brunet et al., Advances in 3D angiography for spinal vascular malformations, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2020.01.013
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical study
Advances in 3D angiography for spinal vascular malformations Stephanie H. Chen ⇑, Samir Sur, Marie-Christine Brunet, Jason Liounakos, David McCarthy, Dallas Sheinberg, Allan D. Levi, Robert M. Starke Department of Neurological Surgery, University of Miami Miller School of Medicine, Miami, FL, USA
a r t i c l e
i n f o
Article history: Received 10 October 2019 Accepted 5 January 2020 Available online xxxx Keywords: Spinal angiography 3D imaging Vascular malformation Endovascular Spinal fistula
a b s t r a c t Spinal vascular malformations are difficult to diagnose lesions that can be associated with significant permanent morbidity. The angioarchitecture of spinal vascular anatomy and the associated pathologies have only recently been illuminated by the advent of spinal angiography. However, conventional spinal digital subtraction angiography is often limited by significant variability, overlapping vessels, as well as an inability to understand the precise location of the nidus or fistula in relation to the spinal cord and spine. In this study, we present 4 unique cases wherein 3-dimensional rotational angiography (3DRA) with dual volume acquisition was useful in defining the anatomy of spinal fistulas as well as planning treatment. Ó 2020 Elsevier Ltd. All rights reserved.
1. Introduction The first spinal vascular malformation was described by J. Gaupp in 1888 as a ‘‘cluster of hemorrhoids” on the surface of the spinal cord [1]. However a precise understanding of the angioarchitecture of the spinal cord vasculature did not occur until the development of selective spinal angiography by Djindijan, Di Chiro, Doppman [2–4]. More recently 3D rotational angiography with dual volume acquisition has enabled reconstruction of bony/metallic structures simultaneously with macro and microvascular anatomy. This has given surgeons the unprecedented ability to visualize the precise anatomic relationships that exist between spinal vascular malformations and the bony spinal canal leading to improved preoperative planning and more efficient surgical treatment [5]. In this case series, we describe the benefit of 3-dimensional rotational angiography (3DRA) in the diagnosis and treatment of vascular malformations of the spine including spinal dural arteriovenous fistulas (SDAVF), spinal epidural fistulas (SEAVF), and perimedullary fistulas. 2. Methods 2.1. Conventional digital subtraction angiography Between 2018 and 2019, four patients underwent 3D DRA for evaluation of spinal vascular lesions at our institution. All four
patients underwent conventional selective spinal angiography under general anesthesia. The Siemens Artis Q Biplane was used for all procedures with a 512 512 pixel matrix system. Spinal segmental vessels were selected with a 5French Cobra catheter (Terumo, Somerset, NJ) and AP monoplanar digital subtraction angiography (DSA) was performed. Biplane AP and lateral biplane angiography was also performed in specific vessels of interest. 2.2. 3D rotational spinal angiography Data were acquired in a 512 512 matrix with a 20-second acquisition protocol under apnea was performed through a 200° rotation of the C-arm. A 2.5 mL/s injection of the artery of interest was performed with injection of 300 mgI/mL nonionic contrast medium at a pressure of 600 psi after an X-ray delay of 2 s. This 120 frames study was then transferred to a Siemens Syngo Workstation in native format and processed by experienced neuroradiology technicians with the assistance of the operating interventionalists (SC, MCB, RS). Reconstructed images, including maximum intensity projection images, shaded surface-rendered displays, and volumerendered displays with adjustable transparency of various structures, as well as full stereoscopic capabilities, were used to study the anatomic relationships demonstrated on these images. 3. Cases 3.1. Case 1
⇑ Corresponding author at: Department of Neurological Surgery, University of Miami Miller School of Medicine, 1095 NW Terrace, Miami, FL 33136, USA. E-mail address: [email protected] (S.H. Chen).
A 64-year-old man with history of right lumbosacral pain presented to the emergency department with a new onset of bilateral
https://doi.org/10.1016/j.jocn.2020.01.013 0967-5868/Ó 2020 Elsevier Ltd. All rights reserved.
Please cite this article as: S. H. Chen, S. Sur, M. C. Brunet et al., Advances in 3D angiography for spinal vascular malformations, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2020.01.013
2
S.H. Chen et al. / Journal of Clinical Neuroscience xxx (xxxx) xxx
leg weakness one week following a lumbar epidural steroid injection. MRI demonstrated T2 signal change representing spinal cord edema and flow voids posteriorly. DSA demonstrated a Type 4 perimedullary fistula at the T10-T11 level, which was fed by a distal branch off the L1 radiculomedullary artery. 3D rotational angiography was used to clarify intradural location of the fistulous point that was several levels above the selectively catheterized segmental vessel [Fig. 1]. The patient was brought to the operating room for a focal T10-11 partial laminectomy for surgical clipping of the fistula. DSA was performed postoperatively demonstrating complete obliteration of the fistula. Subsequent follow-up three months later revealed a marked improvement in the patient’s symptoms. 3.2. Case 2 A 56-year-old female presented with 10 days of acute onset severe lower back pain and an MRI demonstrating a ventral epidural fluid collection spanning T12 to L3 with an associated flow void at L1. The patient was neurologically intact with no evidence of myelopathy. DSA showed a hypervascular network of small tortuous vessels eccentric to the right at L1 with main feeders from T12 and L1 segmental arteries. Prominent early filling of right-sided epidural veins suggestive of arteriovenous shunting was seen. 3D rotational angiography demonstrated pure epidural fistula without intradural component. Successful embolization of this epidural spinal AVM fed by bilateral T12 and L1 segmental vessels was performed without complication [Fig. 2]. The patient was discharged in intact neurological condition and repeat DSA performed five months later demonstrated complete obliteration of the lesion. 3.3. Case 3 A 58-year-old male initially presented with severe neurogenic claudication and radiographic evidence of significant scoliosis and spinal stenosis. He underwent an L2 to S1 decompression and interbody fusion with improvement in his symptoms at three months follow up. Eight months postoperatively however he returned to clinic with progressive worsening balance, lower extremity parasthesias, frank urinary incontinence, and worsening
erectile dysfunction. The patient’s neurologic exam was significant for worsening of bilateral lower extremity weakness, a T11 sensory level, and diminished vibration and proprioception in the lower extremities without hyperreflexia. An MRI of the thoracolumbar spine demonstrated high T2 signal from T7 to the conus with numerous dorsal flow voids. DSA confirmed the presence of a dural arteriovenous fistula fed by the left L3 radicular artery with a large left-sided epidural component as well as intradural venous drainage [Fig. 3A]. The study was limited due to hardware artifact, however the location of the fistulous point at the L3 nerve root sleeve became clear upon performing 3D rotational angiography [Fig. 3]. The patient was brought to the operating room for revision of the laminectomy/facetectomy with careful and focal removal of epidural scar and abnormal fistulous vessels consisting of arterialized veins at the dorsolateral aspect of thecal sac and along the exiting left L3 nerve root. A small dural opening was utilized to cauterize and divide the intradural draining vein as well. The specific localization of the lesion in relation to the spinal titanium implants enabled minimization of epidural scar lysis and thereby reduced the risk of unintended durotomies, which can complicate such operations. At three months follow-up, he was doing well with improved bladder control and lower extremity weakness but persistent sensory and balance disturbances.
3.4. Case 4 A 46-year-old male presented with 5 months of progressively worsening numbness and parasthesias of his lower extremities, bowel and bladder incontinence and subtle lower extremity weakness bilaterally. On physical exam he had subtle 4+/5 weakness diffusely throughout the lower extremities with a T10 sensory level and hyperreflexia. MRI demonstrated prominent thoracic flow voids with abnormal spinal cord expansion and T2 hyperintensity from T6 to T11 [Fig. 4A]. DSA confirmed the presence of a Type I dural arteriovenous fistula fed by the right T8 radicular artery with significant venous congestion and prominent perimedullary veins draining both superiorly and inferiorly. A 3DRA was performed which localized the fistulous point to the T8 nerve root region
Fig. 1. (A) T2 MRI demonstrating cord edema from T8 to L1 (B) AP view of right L1 injection showing the perimedullary AV fistula with shunting point located 2 levels above the injected level and opacification of the epidural venous plexus. (C) Axial and (D) Coronal 3DRA reconstruction demonstrating location of perimedullary fistula on the posterior surface of the spinal cord located between the T10 and T11 rib articulations.
Please cite this article as: S. H. Chen, S. Sur, M. C. Brunet et al., Advances in 3D angiography for spinal vascular malformations, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2020.01.013
S.H. Chen et al. / Journal of Clinical Neuroscience xxx (xxxx) xxx
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Fig. 2. (A) Sagittal and (B) axial T2 MRI demonstrating epidural hematoma along the ventral aspect of the spinal canal from T11-L3 causing mild sac compression at L1. There is also a linear flow void demonstrating a prominent vein at the L1 level. (C) AP view of right L1 injection also contributing to this epidural fistula. (D) 3D rotational angiography with bony reconstruction clarifies relationship of ventral epidural venous drainage with bony elements. Drainage occurs ventrolateral intraosseous routes and the lateral extra-spinal plexus.
Fig. 3. (A) Oblique view of left L3 injection demonstrating vascular malformation with AV shunting and early draining vein projecting superiorly. (B) Axial and (C) lateral and (D) down-the-barrel view of 3DRA demonstrating epidural and intradural components of venous drainage of spinal fistula in relationship to the left L3 pedicle screw as well as intradural component with connection to the posterior coronal venous plexus.
below the right T8 pedicle [Fig. 4]. The patient was taken to the operating room and T7 and T8 laminectomy were performed. The draining vein was identified and ligated as it emerged from the dural root sleeve. Three months postoperatively, the patient’s bladder symptoms were significantly improved and he was intact on neurological examination.
4. Discussion Spinal arteriovenous fistulas are rare, under-diagnosed entities that can lead to substantial morbidity with progressive myelopathy. Spinal dural fistulas (SDAVF) are the most common spinal vascular malformation, with type 1 lesions typically consisting of a pathological communication between a posterior radicular branch of the segmental artery and radicular vein in the dura of the nerve root sleeve [6,7]. Arterialized pressure within the fistulous radiculomedullary vein leads to retrograde drainage into the coronal perimedullary venous plexus, a reversal of the normal centrifugal drainage leading to a congestive myelopathy, often distant from
the fistula itself. Thus, symptoms and cord edema on MRI often do not correlate with the actual location of the fistula. A conventional MRI may demonstrate dilated spinal vessels and cord edema in cases of SDAVF, but cannot clearly differentiate between arteries and veins. Spinal angiography is beneficial to localize the fistulous point, which is typically singular, despite a ‘‘nidus” like appearances with involvement of multiple feeders and the complex of numerous dilated perimedullary veins. The fistulous point is identified on spinal angiography by a caliber change between the feeding vessel and draining vein. However, unlike MRI, which can elucidate the anatomic relationships surrounding the vascular malformation, conventional angiography is limited in determining the anatomic relationships surrounding the vascular malformation due to overlapping vessels, bone, or instrumentation as in Case 3 in our series. The overlapping structures often necessitate AP and lateral biplane angiography in multiple oblique angles to visualize the fistulous point, which can be difficult to interpret. With 3DRA reconstructions, the bony anatomy or instrumentation can be rotated and used as landmarks to precisely localize the nerve root sleeve in which the fistula will be found during
Please cite this article as: S. H. Chen, S. Sur, M. C. Brunet et al., Advances in 3D angiography for spinal vascular malformations, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2020.01.013
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Fig. 4. (A) Sagittal T2 MRI demonstrating cord edema from T8-T12. (B) AP view of right T8 segmental artery injection with dural AV fistula and spinal venous congestion. (C) Coronal (D) axial and (E) sagittal 3DRA demonstrating the posterior radicular artery coursing underneath the right T8 pedicle with the draining vein anastomosing with the posterior coronal venous plexus. Bony anatomical reconstructions show precise location of fistula in the T8 transverse foramen.
surgical obliteration, thus increasing the efficiency and safety of the procedure by minimalizing the operative exposure necessary. Additionally, Suh et al report a series of 13 patients wherein spinal 3DRA was used to identify multiple feeders in cases of SDAVF [8]. Conventional angiography is also limited by its ability to clearly delineate the location of the pathological vessels in relation to the spinal cord and dura. While more rare, both spinal epidural fistulas and perimedullary fistulas can present with similar symptoms to spinal dural arteriovenous fistulas. In Case 1, 3DRA localized the fistula supply to a spinal pial artery on the dorsal surface of the cord between the T10 and T11 pedicles. Although most patients with perimedullary fistulas also typically present with venous congestive myelopathy, perimedullary fistulas have a higher risk for hemorrhage than the more common SDAVF [9,10]. Additionally, appropriate identification of perimedullary fistulas has important treatment implications. From an endovascular perspective, catheterization and treatment of pial arteries carries significantly higher risk as these fistulas are often fed from the anterior spinal artery [11]. From a surgical perspective, perimedullary fistulas range from slow flow shunts with single feeders to high flow shunts with multiple feeders. They are often ventral in location and require more posterolateral approaches or even corpectomy to adequately access the fistula [6,12,13]. In such cases, 3DRA is a valuable tool in localizing the fistulous point and planning the degree of bony decompression needed. Here, a focal laminectomy was performed between T10-T11 despite DSA revealing that the L1 segmental artery was supplying the fistula, thus sparing the thoracolumbar junction and providing an important minimization of bony and ligamentous disruption which can result in kyphosis and hasten the onset of degenerative disease in this region. Spinal epidural fistulas (SEAVF) are a rare entity wherein the arteriovenous shunt lies in the epidural space. In the absence of intradural drainage, SEAVF may only cause symptoms of mass effect or an acute hematoma [14]. However, SEAVF may also lead to perimedullary reflux, mimicking a SDAVF. Recognizing the distinction between these two types of fistulas is important for choos-
ing the appropriate treatment strategy. In the case of SDAVF it is sufficient to occlude the feeding artery at the fistulous point. However, in cases of SEAVF with intradural drainage, surgical disconnection of the radicular vein from the epidural plexus is recommended to prevent reflux into perimedullary veins in the case of reconstitution of the epidural fistula at a different level [15]. In Case 2, the 3DRA clarified that venous outflow was purely epidural and ventrally located, solidifying our decision to treat by endovascular embolization and aiding selection of the most optimal working views during the procedure. Disadvantages of 3DRA with respect to DSA include the higher contrast load per acquisitioned run (50 versus 6–8 mL), longer acquisition time (20 s vs 5 s), and increased patient radiation dose. 3DRA also requires increased time for post-processing review of the data at an external workstation including data transfer, reconstruction, and anatomic analysis. However, total patient contrast load, radiation dose, and treatment time can be decreased if 3DRA negates the need for multiple angles, and biplane angiography runs [5]. Spatial resolution can also be limited in 3DRA. However, 3DRA spinal images can also be reconstructed from flat panel CT angiotomography. This technology offers higher dynamic range and digital readout rates, achieving higher contrast and spatial resolutions than conventional angiography in any desired plane [16]. Another limitation of 3DRA includes the lack of temporal resolution compared to conventional DSA, particularly in the case of spinal arteriovenous malformations (AVM). However, with the increasing use of 4D DRA for cerebral AVM, this technology will likely be adaptable to spinal AVM evaluation as well [17].
5. Conclusion Conventional spinal angiography has provided a better understanding of the angioarchitecture of the spinal cord as well as the various vascular malformations associated with it, but is limited by its ability to clearly demonstrate the spatial relationships with
Please cite this article as: S. H. Chen, S. Sur, M. C. Brunet et al., Advances in 3D angiography for spinal vascular malformations, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2020.01.013
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the surrounding anatomy. Spinal 3DRA combines high-resolution angiography with relevant 3-dimensional adjacent anatomy in a way that improves preoperative treatment planning and should be considered in all cases of complex spinal vascular malformations.
6. Disclosures None of the authors have any significant disclosures or perceived conflicts of interest with the current work. RMS research is supported by the NREF, Joe Niekro Foundation, Brain Aneurysm Foundation, Bee Foundation, and by National Institute of Health (UL1TR002736, KL2TR002737) through the Miami Clinical and Translational Science Institute, from the National Center for Advancing Translational Sciences and the National Institute on Minority Health and Health Disparities. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the NIH. RMS has consulting and teaching agreements with Penumbra, Abbott, Medtronic, InNeuroCo and Cerenovus. All authors contributed to conception and design, acquisition, analysis, interpretation of data, drafting the article, and final approval. We confirm that manuscript complies with all instructions to authors. We confirm that authorship requirements have been met and the final manuscript was approved by all authors. We confirm that this manuscript has not been published elsewhere and is not under consideration by another journal.
Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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Please cite this article as: S. H. Chen, S. Sur, M. C. Brunet et al., Advances in 3D angiography for spinal vascular malformations, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2020.01.013