Journal of Clinical Neuroscience 22 (2015) 180–183
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical Study
Surgical management of spinal dural arteriovenous fistulas Salvatore Chibbaro a,c, Benjamin Gory b, Marco Marsella e, Leonardo Tigan c, Anne Herbrecht a, Mikael Orabi a, Damien Bresson a, Fabian Baumann a, Jean Pierre Saint-Maurice b, Bernard George a, Pierre Kehrli c, Emmanuel Houdart b, Monica Manisor d, Raoul Pop d,⇑ a
Department of Neurosurgery, Lariboisière University Hospital, Paris, France Interventional Neuroradiology, Lariboisière University Hospital, Paris, France Department of Neurosurgery, Hautepierre University Hospital, Strasbourg, France d Interventional Neuroradiology, Hautepierre University Hospital, 1 Avenue Moliere, 67098 Strasbourg, France e Tucson Neurological Center, Tucson, AZ, USA b c
a r t i c l e
i n f o
Article history: Received 28 March 2014 Accepted 6 July 2014
Keywords: Spinal dural arteriovenous fistulas Spinal vascular malformations Spine
a b s t r a c t Spinal dural arteriovenous fistulas are the most common type of spinal arteriovenous malformations. Treatment options consist of microsurgical exclusion and/or endovascular embolization. We retrospectively identified all patients who benefited from surgical treatment at our tertiary center between January 2001 and December 2008. Clinical and imaging data were collected from patient files, including pre- and post-operative formal neurological examination, complete spine MRI and spinal digital subtraction angiography. Of our 30 patients, 25 were men and five were women with a median age of 62 years (range 24–76). The average delay between symptom onset and clinical diagnosis was 27 months (range 1–90). Complete cure of the fistula was obtained in all patients in a single surgical session with no procedural complications and no surgical morbidity. After a mean follow-up period of 32 months (range 14–128), 25 patients (83%) had improved, four were stable and one worsened. Despite recent advances in endovascular techniques and materials, there is a subgroup of patients for which surgery remains the best treatment option. Careful patient selection, a multidisciplinary approach and standardized surgical techniques can lead to excellent results with virtually no complications. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction
2. Material and methods
Spinal dural arteriovenous fistulas (SDAVF) account for approximately 70% of all vascular spinal malformations [1,2]. The diagnosis is often delayed because of the non-specific and insidious nature of the presenting symptoms. Without formal treatment, patients are at risk for paraplegia or even tetraplegia, depending on the level of the lesion [3]. Moreover, rehabilitation outcomes are significantly correlated to the delay between the onset of symptoms and treatment [4]. Recent advances in endovascular and microsurgical techniques have significantly improved operative outcomes [5–14]. We report our experience of open surgical management in a large series of consecutive patients with SDAVF.
2.1. Patient description
⇑ Corresponding author. Tel.: +33 3 6955 1273. E-mail address: [email protected] (R. Pop). http://dx.doi.org/10.1016/j.jocn.2014.07.024 0967-5868/Ó 2014 Elsevier Ltd. All rights reserved.
We retrospectively identified all patients who were diagnosed with SDAVF and who benefited from open surgical treatment at our center between January 2001 and December 2008. Patients with intracranial dural arteriovenous fistulas with peri-medullary venous drainage were excluded from the current study. The following selection criteria are used in our institution to consider patients for an open surgical approach: (1) contraindication to endovascular treatment due to the presence of an anterior spinal artery originating from the radicular artery feeding the SDAVF; (2) contraindication to endovascular treatment due to extensive atherosclerotic lesions; (3) failure of endovascular treatment due to difficulties in catheterization of the arterial feeder; and (4) fistula recurrence after embolization. According to our protocol, all patients underwent pre- and post-operative neurological examination; clinical symptoms were scored using the modified Aminoff Logue Grading Scale for
S. Chibbaro et al. / Journal of Clinical Neuroscience 22 (2015) 180–183
myelopathy (Table 1). All patients underwent spinal digital subtraction angiography (DSA) (Advantix; GE Healthcare, Little Chalfont, Buckinghamshire, UK) before and after treatment. In addition, standard pre- and post-operative MRI with and without contrast were obtained (1.5 Tesla, GE Healthcare). 2.2. Statistical analysis A statistical analysis of different pre-operative variables was conducted to determine the relationship with the final outcome in our study groups using a paired t-test for quantitative parameters. The two-sided significance level was established at 5%. 3. Surgical technique Laminectomy was performed in 10 patients (during the initial 3 years). The remaining 20 patients were treated by hemilaminectomy followed by fistula disconnection/exclusion. In selected patients, dural feeding arteries were specifically identified under microscopic magnification and coagulated with bipolar cautery. Disconnection of the draining vein just distal to the fistula was considered the definitive operative cure. Following laminectomy (or hemilaminectomy) the dura was opened in a standard longitudinal fashion and the intradural arterialized vein was identified near the nerve root where the former goes out through the dura; obviously, pre-operative DSA was often checked to match radiological and anatomical findings. Then sharp dissection of the vein was carried out. When the entire vein was mobilized, it was cauterized with bipolar forceps and, if possible, sharply divided. Next, inspection and cauterization of the inner dural layer was usually the final step. In selected patients, at the beginning of our experience, intra-operative confirmation of the fistula was obtained by perioperative injection of methylene blue dye. Intra-operative angiography was also a very useful adjunct in some cases. Somatosensory evoked potential monitoring during surgery was rarely used until 2007 due to unavailability; however, it became a routine practice afterwards. In the post-operative period, patients were treated for 3 to 6 months with oral anticoagulants. The rationale was to prevent thrombosis in the spinal venous system, occasionally seen due to the sudden reduction in flow velocities after surgical fistula exclusion. 4. Results Between January 2001 and December 2008, a total of 142 patients with SDAVF were treated at our center. Figure 1 illustrates the patient selection diagram. One hundred and twenty patients were embolized as the first treatment. The majority of these (93.4%) were cured by embolization alone. However, two patients (1.6%) had only partial success and six patients (5%) had recurrence Table 1 Modified Aminoff Logue Grading Scale for myelopathy assessment Gait 0 = Normal 1 = Leg weakness, abnormal gait or stance, but no restriction of activity 2 = Restricted activity 3 = Requiring one stick for walking 4 = Requiring two sticks, crutches, or walker 5 = Confined to wheelchair Micturition 0 = Normal 1 = Hesitancy, frequency, urgency 2 = Occasional urinary incontinence or retention 3 = Total incontinence or persistent retention
181
of fistulas on angiographic follow-up. Both non-cured groups went on to have a second intention surgery. A total of 30 patients benefited from open surgical treatment, either as first intention (n = 22) or second intention after embolization (n = 8). Among this group there were 25 men and five women, with a median age of 62 years (range 24–76). The majority of patients presented with ascending lower extremity symptoms with or without associated bowel and/or bladder dysfunction; detailed symptoms and clinical signs are summarized in Table 2. The typical evolution in the majority of patients was slow and progressive deterioration; only two patients presented with severe acute or subacute worsening. The most common initial referral diagnosis was spinal cord tumor in 18 patients, followed by transverse myelitis in eight patients. The average delay between symptom onset and clinical diagnosis was 27 months (range 1–90). The diagnosis of SDAVF was made based on the initial MRI in only 18 patients. Suggestive diagnostic features consisted of increased intramedullary T2-weighted signal changes in the lower spinal cord and conus medullaris and/or abnormal dorsal spinal cord vascularity with venous dilatation. The definitive diagnosis was achieved after spinal DSA, confirming the presence of a SDAVF in the thoracic (16 patients), lumbar (12 patients), or sacral (two patients) spine. Among the 30 patients, 22 underwent direct surgical excision without prior embolization, six had recurring lesions (they underwent prior embolization) and in the remaining two patients, embolization was only partial. In all patients (100%), the fistula was successfully obliterated at the time of the surgical procedure. There were no intra-operative complications and no post-operative morbidity was recorded. Post-operative hospitalization ranged from 4 to 11 days; often physical therapy was initiated during the hospital stay and inpatient rehabilitation was considered depending on the degree of pre-operative disability. Long term follow-up (median interval of 32 months, range 18–104), showed that 83% of patients (n = 25) clinically improved. Four of our 30 patients (13.3%) were neurologically stable when compared to the pre-operative neurological status, and one patient (3.3%) worsened. A significant change of modified Aminoff Logue Grading Scale score was observed, from a median of 5 (range 4–6) pre-operatively to a median of 2 (range 0–3) post-operatively (p < 0.001). Complete cure was confirmed in all patients with post-operative angiographic evaluations. An illustrative patient is presented in Figure 2. 5. Discussion Our results indicate that, in our series of patients, open surgical treatment was very effective in curing SDAVF. Complete disconnection of the fistula was achieved in all patients during one single operative session, with no recurrences noted on angiographic evaluation during the follow-up period. Several classifications of spinal arteriovenous malformations have been described [15,16], using various parameters, including the size and the aspect of feeding and draining vessels. All these systems are useful in clinical practice, especially with regards to risk stratification and anticipating outcome and management difficulties. On the other hand, the use of multiple categorization systems with overlapping criteria may be occasionally misleading and confusing. We believe that the unifying concept that should help in understanding and planning treatment for SDAVF is related to the exploration of the arteriovenous shunt point and the foot of the draining vein, as well as its potential effects on the global venous drainage [14,17]. Several studies have emphasized the cardinal role of venous endothelial disorders in the pathophysiology of SDAVF, and consequently identified the draining veins as
182
S. Chibbaro et al. / Journal of Clinical Neuroscience 22 (2015) 180–183
Partial embolization n=2
EMBOLIZATION n=120 Total patients treated n=142 SURGERY (first intention) n=22
Recurrence after embolization n=6
RESCUE SURGERY n=8
Cured by embolization n=112
Fig. 1. Patient selection diagram. Table 2 Presenting symptoms and clinical signs Symptoms Paraparesis Paraplegia Medullary claudication Lower extremity sensory disturbances Hypoesthesia Paresthesia Pain Radicular Back pain Acute onset of symptoms Pyramidal syndrome
Patients, n
Percentage
18 6 9 24 18 6 6 3 3 6 6
60% 20% 30% 80% 60% 20% 20% 10% 10% 20% 20%
the primary surgical target in order to obtain a definitive cure of the malformation. Clinical reports have demonstrated that in the case of persistence of the draining vein, the fistula has the propensity to recur by recruiting new arterial feeders [18]. Spinal cord venous hypertension and microcirculatory thrombotic events are considered to be the pathophysiological substrates of the clinical neurological dysfunction. None of our patients had a hemorrhagic event, and this finding is consistent with other reports [19,20]. These underlying mechanisms are also supported by the clinical findings in our series: two patients experienced their symptom onset during functions mimicking a Valsalva maneuver, three patients presented with sensory complaints during strenuous physical activity and 15 (50%) of our patients
Fig. 2. (A) Pre-treatment spinal digital subtraction angiography. Selective injection of the right first lumbar intercostal artery (L1). Radicular artery (arrow head) feeding the dural arteriovenous fistula. Tortuous draining vein projecting upwards (white arrow). Pre-treatment sagittal (B) T2-weighted and (C) T1-weighted post-gadolinium MRI, showing extensive centro-medullary edema as well as abnormal perimedullary vessels at the L1 level, corresponding to the dilated draining vein. (D) Post-treatment angiography at the same level showing complete cure of the fistula. Post-treatment sagittal (E) T2-weighted and (F) T1-weighted post-gadolinium MRI showing diminished medullary edema and disappearance of the abnormal vessels.
S. Chibbaro et al. / Journal of Clinical Neuroscience 22 (2015) 180–183
reported an increase of symptoms upon standing up as well as maintaining an upright position whereas they experienced some improvement while lying flat or in a recumbent position. This suggests that the neurological dysfunction is often exacerbated by increased venous hydrostatic forces. Controversies still exist regarding the best treatment modality for SDAVF; some authors favor surgery [16,21–23], whereas others recommend endovascular treatment [24–26]. In a single center series treating patients with endovascular techniques, neurological improvement and stabilization were reported to be 44% and 56%, respectively [27]. In a meta-analysis of 16 surgical studies, Steinmetz et al. [28] found rates of improvement and stabilization of clinical function of 55% and 34%, respectively, with a successful SDAVF occlusion rate of 98%, with 2% morbidity and no mortality. In the same meta-analysis describing 10 reports of endovascular management, the SDAVF occlusion rate was found to be 46% with an associated morbidity of 4% and no mortality. Due to too much heterogeneity and insufficient longitudinal data collection of endovascular studies, a comparison regarding the efficacy of surgery versus embolization was impossible. However, in recent papers discussing endovascular treatment, it appears that outcomes are much better; this is probably due to advances in interventional neuroradiology techniques and materials [1,2,7–9,13–16,18,22,24,25,29–36]. As a result many centers currently prefer endovascular management as the first line of treatment as long as there are no contraindications [17,31,35,37]. Our policy for managing SDAVF follows the same guidelines – endovascular therapy is considered first, with surgery reserved for the criteria previously described in the Methods section. It has been shown that in these instances, embolization is associated with higher procedural risks, especially in the presence of an anterior spinal artery originating from the arterial feeder [9,30,31,33,34,38]. In order to ensure the best standard of care for this type of lesion, patients should be evaluated with a multidisciplinary approach based on direct cooperation between endovascular specialists and neurosurgeons. This allows better patient selection in order to provide optimal treatment, which will in turn ensure better clinical outcomes [6,7,17,30]. This concept is confirmed by the excellent results obtained in our series of patients (100% cure rate with no procedural complications). 6. Conclusion Despite recent advances in endovascular techniques and materials, there is still a group of patients with SDAVF for whom surgery remains the best treatment option. Careful patient selection, a multidisciplinary approach and a standardized surgical technique can lead to excellent results with virtually no complications. Conflicts of Interest/Disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication. References [1] Kendall BE, Logue V. Spinal epidural angiomatous malformations draining into intrathecal veins. Neuroradiology 1977;13:181–9. [2] Merland JJ, Riche MC, Chiras J. Intraspinal extramedullary arteriovenous fistulae draining into the medullary veins. J Neuroradiol 1980;7:271–320. [3] Bradac GB, Daniele D, Riva A, et al. Spinal dural arteriovenous fistulas: an underestimated cause of myelopathy. Eur Neurol 1994;34:87–94. [4] Ofran Y, Yovchev I, Hiller N, et al. Correlation between time to diagnosis and rehabilitation outcomes in patients with spinal dural arteriovenous fistula. J Spinal Cord Med 2013;36:200–6. [5] Atkinson JL, Miller GM, Krauss WE, et al. Clinical and radiographic features of dural arteriovenous fistula, a treatable cause of myelopathy. Mayo Clin Proc 2001;76:1120–30. [6] Cecchi PC, Musumeci A, Rizzo P, et al. Late deterioration of neurologic function in patients surgically treated for spinal dural arteriovenous fistulas. Surg Neurol 2009;72:257–61 [discussion 261–252].
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[7] Dehdashti AR, Da Costa LB, terBrugge KG, et al. Overview of the current role of endovascular and surgical treatment in spinal dural arteriovenous fistulas. Neurosurg Focus 2009;26:E8. [8] Hessler C, Regelsberger J, Grzyska U, et al. Therapeutic clues in spinal dural arteriovenous fistulas – a 30 year experience of 156 cases. Cent Eur Neurosurg 2010;71:8–12. [9] Kim LJ, Spetzler RF. Classification and surgical management of spinal arteriovenous lesions: arteriovenous fistulae and arteriovenous malformations. Neurosurgery 2006;59:S195–201 [discussion S3–S13]. [10] Krings T, Geibprasert S. Spinal dural arteriovenous fistulas. AJNR Am J Neuroradiol 2009;30:639–48. [11] Lee TT, Gromelski EB, Bowen BC, et al. Diagnostic and surgical management of spinal dural arteriovenous fistulas. Neurosurgery 1998;43:242–6 [discussion 246–7]. [12] Lev N, Maimon S, Melamed E, et al. Spinal dural arteriovenous fistula. Harefuah 1999;137:471–4. [13] Lev N, Maimon S, Rappaport ZH, et al. Spinal dural arteriovenous fistulae – a diagnostic challenge. Isr Med Assoc J 2001;3:492–6. [14] Li M, Zhang HQ, Zhi XL, et al. Surgical interruption of spinal dural arteriovenous fistulas. Chin Med J (Engl) 2005;118:433–5. [15] Aminoff MJ, Barnard RO, Logue V. The pathophysiology of spinal vascular malformations. J Neurol Sci 1974;23:255–63. [16] Symon L, Kuyama H, Kendall B. Dural arteriovenous malformations of the spine. Clinical features and surgical results in 55 cases. J Neurosurg 1984;60:238–47. [17] Westphal M, Koch C. Management of spinal dural arteriovenous fistulae using an interdisciplinary neuroradiological/neurosurgical approach: experience with 47 cases. Neurosurgery 1999;45:451–7 [discussion 457–8]. [18] McCutcheon IE, Doppman JL, Oldfield EH. Microvascular anatomy of dural arteriovenous abnormalities of the spine: a microangiographic study. J Neurosurg 1996;84:215–20. [19] Koch C, Gottschalk S, Giese A. Dural arteriovenous fistula of the lumbar spine presenting with subarachnoid hemorrhage. Case report and review of the literature. J Neurosurg 2004;100:385–91. [20] Morimoto T, Yoshida S, Basugi N. Dural arteriovenous malformation in the cervical spine presenting with subarachnoid hemorrhage: case report. Neurosurgery 1992;31:118–20 [discussion 121]. [21] Afshar JK, Doppman JL, Oldfield EH. Surgical interruption of intradural draining vein as curative treatment of spinal dural arteriovenous fistulas. J Neurosurg 1995;82:196–200. [22] Huffmann BC, Gilsbach JM, Thron A. Spinal dural arteriovenous fistulas: a plea for neurosurgical treatment. Acta Neurochir (Wien) 1995;135:44–51. [23] Watson JC, Oldfield EH. The surgical management of spinal dural vascular malformations. Neurosurg Clin N Am 1999;10:73–87. [24] Nichols DA, Rufenacht DA, Jack CR Jr, et al. Embolization of spinal dural arteriovenous fistula with polyvinyl alcohol particles: experience in 14 patients. AJNR Am J Neuroradiol 1992;13:933–40. [25] Niimi Y, Berenstein A, Setton A, et al. Embolization of spinal dural arteriovenous fistulae: results and follow-up. Neurosurgery 1997;40:675–82 [discussion 682–3]. [26] Ushikoshi S, Hida K, Kikuchi Y, et al. Functional prognosis after treatment of spinal dural arteriovenous fistulas. Neurol Med Chir (Tokyo) 1999;39:206–12 [discussion 212–3]. [27] Song JK, Vinuela F, Gobin YP, et al. Surgical and endovascular treatment of spinal dural arteriovenous fistulas: long-term disability assessment and prognostic factors. J Neurosurg 2001;94:199–204. [28] Steinmetz MP, Chow MM, Krishnaney AA, et al. Outcome after the treatment of spinal dural arteriovenous fistulae: a contemporary single-institution series and meta-analysis. Neurosurgery 2004;55:77–87 [discussion 87–8]. [29] Guillevin R, Vallee JN, Cormier E, et al. N-butyl 2-cyanoacrylate embolization of spinal dural arteriovenous fistulae: CT evaluation, technical features, and outcome prognosis in 26 cases. AJNR Am J Neuroradiol 2005;26:929–35. [30] Marquardt G, Berkefeld J, Seifert V, et al. Preoperative coil marking to facilitate intraoperative localization of spinal dural arteriovenous fistulas. Eur Spine J 2009;18:1117–20. [31] Medel R, Crowley RW, Dumont AS. Endovascular management of spinal vascular malformations: history and literature review. Neurosurg Focus 2009;26:E7. [32] Nagata S, Morioka T, Natori Y, et al. Factors that affect the surgical outcomes of spinal dural arteriovenous fistulas. Surg Neurol 2006;65:563–8 [discussion 568]. [33] Nogueira RG, Dabus G, Rabinov JD, et al. Onyx embolization for the treatment of spinal dural arteriovenous fistulae: initial experience with long-term follow-up. Technical case report. Neurosurgery 2009;64:E197–8 [discussion E198]. [34] Park SB, Han MH, Jahng TA, et al. Spinal dural arteriovenous fistulas: clinical experience with endovascular treatment as a primary therapeutic modality. J Korean Neurosurg Soc 2008;44:364–9. [35] Schick U, Hassler W. Treatment and outcome of spinal dural arteriovenous fistulas. Eur Spine J 2003;12:350–5. [36] Sherif C, Gruber A, Bavinzski G, et al. Long-term outcome of a multidisciplinary concept of spinal dural arteriovenous fistulae treatment. Neuroradiology 2008;50:67–74. [37] Andres RH, Barth A, Guzman R, et al. Endovascular and surgical treatment of spinal dural arteriovenous fistulas. Neuroradiology 2008;50:869–76. [38] Sivakumar W, Zada G, Yashar P, et al. Endovascular management of spinal dural arteriovenous fistulas. A review. Neurosurg Focus 2009;26:E15.
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical Study
Surgical management of spinal dural arteriovenous fistulas Salvatore Chibbaro a,c, Benjamin Gory b, Marco Marsella e, Leonardo Tigan c, Anne Herbrecht a, Mikael Orabi a, Damien Bresson a, Fabian Baumann a, Jean Pierre Saint-Maurice b, Bernard George a, Pierre Kehrli c, Emmanuel Houdart b, Monica Manisor d, Raoul Pop d,⇑ a
Department of Neurosurgery, Lariboisière University Hospital, Paris, France Interventional Neuroradiology, Lariboisière University Hospital, Paris, France Department of Neurosurgery, Hautepierre University Hospital, Strasbourg, France d Interventional Neuroradiology, Hautepierre University Hospital, 1 Avenue Moliere, 67098 Strasbourg, France e Tucson Neurological Center, Tucson, AZ, USA b c
a r t i c l e
i n f o
Article history: Received 28 March 2014 Accepted 6 July 2014
Keywords: Spinal dural arteriovenous fistulas Spinal vascular malformations Spine
a b s t r a c t Spinal dural arteriovenous fistulas are the most common type of spinal arteriovenous malformations. Treatment options consist of microsurgical exclusion and/or endovascular embolization. We retrospectively identified all patients who benefited from surgical treatment at our tertiary center between January 2001 and December 2008. Clinical and imaging data were collected from patient files, including pre- and post-operative formal neurological examination, complete spine MRI and spinal digital subtraction angiography. Of our 30 patients, 25 were men and five were women with a median age of 62 years (range 24–76). The average delay between symptom onset and clinical diagnosis was 27 months (range 1–90). Complete cure of the fistula was obtained in all patients in a single surgical session with no procedural complications and no surgical morbidity. After a mean follow-up period of 32 months (range 14–128), 25 patients (83%) had improved, four were stable and one worsened. Despite recent advances in endovascular techniques and materials, there is a subgroup of patients for which surgery remains the best treatment option. Careful patient selection, a multidisciplinary approach and standardized surgical techniques can lead to excellent results with virtually no complications. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction
2. Material and methods
Spinal dural arteriovenous fistulas (SDAVF) account for approximately 70% of all vascular spinal malformations [1,2]. The diagnosis is often delayed because of the non-specific and insidious nature of the presenting symptoms. Without formal treatment, patients are at risk for paraplegia or even tetraplegia, depending on the level of the lesion [3]. Moreover, rehabilitation outcomes are significantly correlated to the delay between the onset of symptoms and treatment [4]. Recent advances in endovascular and microsurgical techniques have significantly improved operative outcomes [5–14]. We report our experience of open surgical management in a large series of consecutive patients with SDAVF.
2.1. Patient description
⇑ Corresponding author. Tel.: +33 3 6955 1273. E-mail address: [email protected] (R. Pop). http://dx.doi.org/10.1016/j.jocn.2014.07.024 0967-5868/Ó 2014 Elsevier Ltd. All rights reserved.
We retrospectively identified all patients who were diagnosed with SDAVF and who benefited from open surgical treatment at our center between January 2001 and December 2008. Patients with intracranial dural arteriovenous fistulas with peri-medullary venous drainage were excluded from the current study. The following selection criteria are used in our institution to consider patients for an open surgical approach: (1) contraindication to endovascular treatment due to the presence of an anterior spinal artery originating from the radicular artery feeding the SDAVF; (2) contraindication to endovascular treatment due to extensive atherosclerotic lesions; (3) failure of endovascular treatment due to difficulties in catheterization of the arterial feeder; and (4) fistula recurrence after embolization. According to our protocol, all patients underwent pre- and post-operative neurological examination; clinical symptoms were scored using the modified Aminoff Logue Grading Scale for
S. Chibbaro et al. / Journal of Clinical Neuroscience 22 (2015) 180–183
myelopathy (Table 1). All patients underwent spinal digital subtraction angiography (DSA) (Advantix; GE Healthcare, Little Chalfont, Buckinghamshire, UK) before and after treatment. In addition, standard pre- and post-operative MRI with and without contrast were obtained (1.5 Tesla, GE Healthcare). 2.2. Statistical analysis A statistical analysis of different pre-operative variables was conducted to determine the relationship with the final outcome in our study groups using a paired t-test for quantitative parameters. The two-sided significance level was established at 5%. 3. Surgical technique Laminectomy was performed in 10 patients (during the initial 3 years). The remaining 20 patients were treated by hemilaminectomy followed by fistula disconnection/exclusion. In selected patients, dural feeding arteries were specifically identified under microscopic magnification and coagulated with bipolar cautery. Disconnection of the draining vein just distal to the fistula was considered the definitive operative cure. Following laminectomy (or hemilaminectomy) the dura was opened in a standard longitudinal fashion and the intradural arterialized vein was identified near the nerve root where the former goes out through the dura; obviously, pre-operative DSA was often checked to match radiological and anatomical findings. Then sharp dissection of the vein was carried out. When the entire vein was mobilized, it was cauterized with bipolar forceps and, if possible, sharply divided. Next, inspection and cauterization of the inner dural layer was usually the final step. In selected patients, at the beginning of our experience, intra-operative confirmation of the fistula was obtained by perioperative injection of methylene blue dye. Intra-operative angiography was also a very useful adjunct in some cases. Somatosensory evoked potential monitoring during surgery was rarely used until 2007 due to unavailability; however, it became a routine practice afterwards. In the post-operative period, patients were treated for 3 to 6 months with oral anticoagulants. The rationale was to prevent thrombosis in the spinal venous system, occasionally seen due to the sudden reduction in flow velocities after surgical fistula exclusion. 4. Results Between January 2001 and December 2008, a total of 142 patients with SDAVF were treated at our center. Figure 1 illustrates the patient selection diagram. One hundred and twenty patients were embolized as the first treatment. The majority of these (93.4%) were cured by embolization alone. However, two patients (1.6%) had only partial success and six patients (5%) had recurrence Table 1 Modified Aminoff Logue Grading Scale for myelopathy assessment Gait 0 = Normal 1 = Leg weakness, abnormal gait or stance, but no restriction of activity 2 = Restricted activity 3 = Requiring one stick for walking 4 = Requiring two sticks, crutches, or walker 5 = Confined to wheelchair Micturition 0 = Normal 1 = Hesitancy, frequency, urgency 2 = Occasional urinary incontinence or retention 3 = Total incontinence or persistent retention
181
of fistulas on angiographic follow-up. Both non-cured groups went on to have a second intention surgery. A total of 30 patients benefited from open surgical treatment, either as first intention (n = 22) or second intention after embolization (n = 8). Among this group there were 25 men and five women, with a median age of 62 years (range 24–76). The majority of patients presented with ascending lower extremity symptoms with or without associated bowel and/or bladder dysfunction; detailed symptoms and clinical signs are summarized in Table 2. The typical evolution in the majority of patients was slow and progressive deterioration; only two patients presented with severe acute or subacute worsening. The most common initial referral diagnosis was spinal cord tumor in 18 patients, followed by transverse myelitis in eight patients. The average delay between symptom onset and clinical diagnosis was 27 months (range 1–90). The diagnosis of SDAVF was made based on the initial MRI in only 18 patients. Suggestive diagnostic features consisted of increased intramedullary T2-weighted signal changes in the lower spinal cord and conus medullaris and/or abnormal dorsal spinal cord vascularity with venous dilatation. The definitive diagnosis was achieved after spinal DSA, confirming the presence of a SDAVF in the thoracic (16 patients), lumbar (12 patients), or sacral (two patients) spine. Among the 30 patients, 22 underwent direct surgical excision without prior embolization, six had recurring lesions (they underwent prior embolization) and in the remaining two patients, embolization was only partial. In all patients (100%), the fistula was successfully obliterated at the time of the surgical procedure. There were no intra-operative complications and no post-operative morbidity was recorded. Post-operative hospitalization ranged from 4 to 11 days; often physical therapy was initiated during the hospital stay and inpatient rehabilitation was considered depending on the degree of pre-operative disability. Long term follow-up (median interval of 32 months, range 18–104), showed that 83% of patients (n = 25) clinically improved. Four of our 30 patients (13.3%) were neurologically stable when compared to the pre-operative neurological status, and one patient (3.3%) worsened. A significant change of modified Aminoff Logue Grading Scale score was observed, from a median of 5 (range 4–6) pre-operatively to a median of 2 (range 0–3) post-operatively (p < 0.001). Complete cure was confirmed in all patients with post-operative angiographic evaluations. An illustrative patient is presented in Figure 2. 5. Discussion Our results indicate that, in our series of patients, open surgical treatment was very effective in curing SDAVF. Complete disconnection of the fistula was achieved in all patients during one single operative session, with no recurrences noted on angiographic evaluation during the follow-up period. Several classifications of spinal arteriovenous malformations have been described [15,16], using various parameters, including the size and the aspect of feeding and draining vessels. All these systems are useful in clinical practice, especially with regards to risk stratification and anticipating outcome and management difficulties. On the other hand, the use of multiple categorization systems with overlapping criteria may be occasionally misleading and confusing. We believe that the unifying concept that should help in understanding and planning treatment for SDAVF is related to the exploration of the arteriovenous shunt point and the foot of the draining vein, as well as its potential effects on the global venous drainage [14,17]. Several studies have emphasized the cardinal role of venous endothelial disorders in the pathophysiology of SDAVF, and consequently identified the draining veins as
182
S. Chibbaro et al. / Journal of Clinical Neuroscience 22 (2015) 180–183
Partial embolization n=2
EMBOLIZATION n=120 Total patients treated n=142 SURGERY (first intention) n=22
Recurrence after embolization n=6
RESCUE SURGERY n=8
Cured by embolization n=112
Fig. 1. Patient selection diagram. Table 2 Presenting symptoms and clinical signs Symptoms Paraparesis Paraplegia Medullary claudication Lower extremity sensory disturbances Hypoesthesia Paresthesia Pain Radicular Back pain Acute onset of symptoms Pyramidal syndrome
Patients, n
Percentage
18 6 9 24 18 6 6 3 3 6 6
60% 20% 30% 80% 60% 20% 20% 10% 10% 20% 20%
the primary surgical target in order to obtain a definitive cure of the malformation. Clinical reports have demonstrated that in the case of persistence of the draining vein, the fistula has the propensity to recur by recruiting new arterial feeders [18]. Spinal cord venous hypertension and microcirculatory thrombotic events are considered to be the pathophysiological substrates of the clinical neurological dysfunction. None of our patients had a hemorrhagic event, and this finding is consistent with other reports [19,20]. These underlying mechanisms are also supported by the clinical findings in our series: two patients experienced their symptom onset during functions mimicking a Valsalva maneuver, three patients presented with sensory complaints during strenuous physical activity and 15 (50%) of our patients
Fig. 2. (A) Pre-treatment spinal digital subtraction angiography. Selective injection of the right first lumbar intercostal artery (L1). Radicular artery (arrow head) feeding the dural arteriovenous fistula. Tortuous draining vein projecting upwards (white arrow). Pre-treatment sagittal (B) T2-weighted and (C) T1-weighted post-gadolinium MRI, showing extensive centro-medullary edema as well as abnormal perimedullary vessels at the L1 level, corresponding to the dilated draining vein. (D) Post-treatment angiography at the same level showing complete cure of the fistula. Post-treatment sagittal (E) T2-weighted and (F) T1-weighted post-gadolinium MRI showing diminished medullary edema and disappearance of the abnormal vessels.
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reported an increase of symptoms upon standing up as well as maintaining an upright position whereas they experienced some improvement while lying flat or in a recumbent position. This suggests that the neurological dysfunction is often exacerbated by increased venous hydrostatic forces. Controversies still exist regarding the best treatment modality for SDAVF; some authors favor surgery [16,21–23], whereas others recommend endovascular treatment [24–26]. In a single center series treating patients with endovascular techniques, neurological improvement and stabilization were reported to be 44% and 56%, respectively [27]. In a meta-analysis of 16 surgical studies, Steinmetz et al. [28] found rates of improvement and stabilization of clinical function of 55% and 34%, respectively, with a successful SDAVF occlusion rate of 98%, with 2% morbidity and no mortality. In the same meta-analysis describing 10 reports of endovascular management, the SDAVF occlusion rate was found to be 46% with an associated morbidity of 4% and no mortality. Due to too much heterogeneity and insufficient longitudinal data collection of endovascular studies, a comparison regarding the efficacy of surgery versus embolization was impossible. However, in recent papers discussing endovascular treatment, it appears that outcomes are much better; this is probably due to advances in interventional neuroradiology techniques and materials [1,2,7–9,13–16,18,22,24,25,29–36]. As a result many centers currently prefer endovascular management as the first line of treatment as long as there are no contraindications [17,31,35,37]. Our policy for managing SDAVF follows the same guidelines – endovascular therapy is considered first, with surgery reserved for the criteria previously described in the Methods section. It has been shown that in these instances, embolization is associated with higher procedural risks, especially in the presence of an anterior spinal artery originating from the arterial feeder [9,30,31,33,34,38]. In order to ensure the best standard of care for this type of lesion, patients should be evaluated with a multidisciplinary approach based on direct cooperation between endovascular specialists and neurosurgeons. This allows better patient selection in order to provide optimal treatment, which will in turn ensure better clinical outcomes [6,7,17,30]. This concept is confirmed by the excellent results obtained in our series of patients (100% cure rate with no procedural complications). 6. Conclusion Despite recent advances in endovascular techniques and materials, there is still a group of patients with SDAVF for whom surgery remains the best treatment option. Careful patient selection, a multidisciplinary approach and a standardized surgical technique can lead to excellent results with virtually no complications. Conflicts of Interest/Disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication. References [1] Kendall BE, Logue V. Spinal epidural angiomatous malformations draining into intrathecal veins. Neuroradiology 1977;13:181–9. [2] Merland JJ, Riche MC, Chiras J. Intraspinal extramedullary arteriovenous fistulae draining into the medullary veins. J Neuroradiol 1980;7:271–320. [3] Bradac GB, Daniele D, Riva A, et al. Spinal dural arteriovenous fistulas: an underestimated cause of myelopathy. Eur Neurol 1994;34:87–94. [4] Ofran Y, Yovchev I, Hiller N, et al. Correlation between time to diagnosis and rehabilitation outcomes in patients with spinal dural arteriovenous fistula. J Spinal Cord Med 2013;36:200–6. [5] Atkinson JL, Miller GM, Krauss WE, et al. Clinical and radiographic features of dural arteriovenous fistula, a treatable cause of myelopathy. Mayo Clin Proc 2001;76:1120–30. [6] Cecchi PC, Musumeci A, Rizzo P, et al. Late deterioration of neurologic function in patients surgically treated for spinal dural arteriovenous fistulas. Surg Neurol 2009;72:257–61 [discussion 261–252].
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