- Email: [email protected]
Spinal Vascular Malformations: Treatment and Outcome
Original Article
Spinal Vascular Malformations: Treatment and Outcome Mehmet Yigit Akgun1, Rahsan Kemerdere1, Mustafa Onur Ulu1, Orkhan Alizada1, Cihan Isler1, Osman Kizilkilic2, Civan Islak2, Murat Hanci1
BACKGROUND: Vascular malformations of the spinal cord are a rare and complex clinical entity and can lead to severe morbidity with progressive spinal cord symptoms if not treated properly. In early stages, the disease is characterized by slowly progressive, nonspecific symptoms, such as gait disturbance, paresthesia, diffuse sensory symptoms, and radicular pain; in the late stages, bowel and bladder incontinence, erectile dysfunction, and urinary retention may develop. In recent decades, understanding and treatment of spinal vascular malformations have improved with the evolution of diagnostic tools and treatment modalities; however, it is still difficult to manage these cases because of the complexity of the pathology. The aims of this study were to present the long-term outcomes of our patients and to discuss the optimal management strategies.
-
METHODS: We reviewed the records of 78 patients with spinal vascular malformations and performed a retrospective, single-center case series evaluating initial occlusion, recanalization, retreatment, and neurologic status of patients with dural arteriovenous fistulas, perimedullary arteriovenous fistulas, arteriovenous malformations, and extradural arteriovenous fistulas who had undergone embolization and/or surgery.
-
RESULTS: No mortality was observed. Complete obliteration was achieved in 76 patients (97.4%).
-
CONCLUSIONS: Both endovascular and surgical treatment of spinal vascular malformations resulted in
-
Key words Arteriovenous fistula - Outcome - Spinal - Treatment - Vascular malformations -
Abbreviations and Acronyms ALS: Aminoff and Logue scale ASA: Anterior spinal artery AVF: Arteriovenous fistula AVM: Arteriovenous malformation DSA: Digital subtraction angiography MRI: Magnetic resonance imaging
WORLD NEUROSURGERY -: e1-e8, - 2019
significant long-term recovery from myelopathic symptoms and improvement in quality of life for most patients.
INTRODUCTION
V
ascular malformations of the spinal cord are a rare and complex clinical entity and can lead to severe morbidity with progressive spinal cord symptoms if not treated properly. Several different classifications are used to classify vascular malformations of the spinal cord, but the most widely used one was proposed by Takai.1 In Takai’s classification,1 arteriovenous malformations (AVMs) are divided into 1) dural arteriovenous fistula (AVF), 2) intramedullary glomus-type AVMs, 3) intramedullary juvenile-type AVMs, 4) perimedullary AVF, and 5) extradural/paraspinal AVM/AVF. Spinal dural arteriovenous fistulas (SDAVFs) or type 1 malformations, also classified by Spetzler as intradural dorsal AVFs, are the most common vascular malformations of the spinal cord constituting approximately 75% in this group. Perimedullary AVFs (PMAVFs) are especially rare spinal AVMs, accounting for only 15%e40% of all cases.2 In recent decades, understanding and treatment of spinal vascular malformations have improved with the evolution of diagnostic tools and treatment modalities; however, it is still difficult to manage these cases because of the complexity of the pathology. On one hand, SDAVF is a treatable cause of acquired myelopathy, resulting in severe and progressive neurologic deficits. On the other hand, PMAVFs are generally more difficult to treat because of their complicated anatomy and physiology
PMAVF: Perimedullary arteriovenous fistula SDAVF: Spinal dural arteriovenous fistula From the Departments of 1Neurosurgery and 2Radiology, Istanbul University-Cerrahpasa, Cerrahpasa Medical Faculty, Istanbul, Turkey To whom correspondence should be addressed: Mehmet Yigit Akgun, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.07.043 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
www.journals.elsevier.com/world-neurosurgery
e1
ORIGINAL ARTICLE MEHMET YIGIT AKGUN ET AL.
SPINAL VASCULAR MALFORMATIONS
compared with SDAVFs.3 Microsurgical occlusion, endovascular embolization, and the combination of both are known to be effective approaches to occlude the shunt area or fistular nidus. The choice between surgical treatment and endovascular embolization remains controversial. To our knowledge, there is no report in the literature that discusses all 4 pathologies, SDAVFs, PMAVFs, SAVMs and extradural AVFs, in the same study. We present a series of patients with these pathologies treated via surgical, endovascular, and multimodal therapies. The aim of this study is to present the long-term outcome of our patients and to discuss the optimal management strategies. MATERIALS AND METHODS
www.SCIENCEDIRECT.com
Grade
Definition
Gait 0
Normal
1
Leg weakness, abnormal gait or stance, but no restriction of activity
2
Restricted activity, but not requiring support
3
Requiring 1 cane for walking
4
Requiring 2 canes for walking
5
Confined to wheelchair
Micturition
All procedures performed in the studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. We performed a retrospective, single-center case series evaluating initial occlusion, recanalization, retreatment, and neurologic status of patients with SDAVFs, PMAVFs, SAVMs, and extradural AVFs who had undergone embolization and/or surgery. We reviewed the records of 78 patients with spinal vascular malformations between 1999 and 2018. Data were collected retrospectively using a standardized form, including age, sex, symptoms, history of spinal trauma or surgery, treatment methods, treatment results, and magnetic resonance imaging (MRI) in Digital Imaging and Communications in Medicine data format. Patients were screened based on the following inclusion criteria: 1) The diagnosis was based on spinal angiography findings, and 2) complete clinical data and images were of adequate resolution for the analysis. Patients with incomplete clinical data and/or images not of adequate resolution for the analysis were excluded from the study. All patients underwent MRI and selective spinal digital subtraction angiography (DSA). The extent of abnormal hyperintensity areas in the spinal cord and signal flow voids in the dural sac were determined from sagittal T2-weighted MRI. Fistula locations were determined by DSA, and diagnosis was established. Recanalization or recurrence was defined as the presence of persistent arteriovenous shunting or fistula at the time of the first follow-up DSA compared with the initial posttreatment DSA. Clinical outcomes consisted of the recorded historical and physical examination components of neurosurgical follow-up appointments, and examination findings were compared with symptoms at presentation. Symptoms were recorded as improved if the patient experienced improvement or resolution of the presenting symptoms. Also, pretreatment and follow-up spinal function was evaluated using the Aminoff and Logue scale (ALS) scores (Table 1).4 At the time of angiography, definitive embolization was attempted if the pathologic radicular artery did not provide anterior spinal artery (ASA) supply. If the ASA supply was noted or the embolization could not be performed for technical reasons, the patient was referred for surgical intervention. The treatment strategy was the same for all patients, such that an attempt at endovascular obliteration was the first choice of treatment. Surgery was offered whenever embolization failed or was abandoned
e2
Table 1. Aminoff-Logue Scale
0
Normal
1
Hesitancy, urgency, frequency, altered sensation, but continent
2
Occasional urinary incontinence or retention
3
Total incontinence or persistent retention
Aminoff-Logue scale scores were used to clinically assess all patients before and after treatment. Because the primary aim of treatment is symptomatic and functional improvement, in particular for gait and urinary dysfunction, the Aminoff-Logue disability scale was introduced to facilitate long-term follow-up trends.
for technical reasons. The operation was performed under general anesthesia in the prone position. The appropriate spinal level was determined using C-arm. After a midline incision, double or triple laminectomy/laminotomy was performed, the dura mater was opened, and the fistula or arteriovenous lesion was identified. The nidus was resected in intramedullary AVMs, and the shunting vein to the perimedullary coronal venous plexus or the fistula was coagulated in dural AVFs. On the first postoperative day, control selective spinal DSA was routinely performed, and if residual filling or subtotal obliteration was detected, revision surgery and/ or an endovascular approach was implemented. All patients also underwent follow-up MRI at 1 month postoperatively. Physical rehabilitation in case of neurologic impairment was routinely started from the first postoperative day. Statistical Analysis Data are reported as mean SD, median for continuous variables, or the number of patients with sample population percentages for categorical variables. Statistical analysis was performed with IBM SPSS Version 21.0 software (IBM Corporation, Armonk, New York, USA), with P < 0.05 indicating statistical significance. For quantitative data, the Kolmogorov-Smirnov test was used to test the normal distribution. Kruskal-Wallis and Wilcoxon rank sum test were used for nonenormally distributed parameters. c2 test was to assess qualitative data. RESULTS Characteristics of patients and their pathologies are summarized in Table 2. There were 60 (76.9%) male and 18 (23.1%) female patients with a mean age of 47.21 19.27 years (range, 4e84 years) at initial symptom onset. Eleven patients were 18 years
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.07.043
ORIGINAL ARTICLE MEHMET YIGIT AKGUN ET AL.
SPINAL VASCULAR MALFORMATIONS
Table 2. Summary of Patients with Spinal Vascular Malformations Total Patients (n [ 78)
Patients with SDAVFs (n [ 46)
Patients with PMAVFs (n [ 17)
Patients with SAVMs (n [ 8)
Patients with Extradural AVFs (n [ 7)
Age, years
47.21
Male/female
60/18
54.65
32.5
24.75
43.7
37/9
13/4
6/2
4/3
Cervical
4
—
2
—
2
Thoracic
51
36
9
4
2
Lumbar
21
8
6
4
3
Sacral
2
2
—
—
—
Variables
Location
Clinical manifestations (%) Pain
59 (75.6)
37 (80)
12 (70.5)
5 (62.5)
5 (71.4)
Paresis
49 (62.8)
29 (63)
10 (58.8)
6 (75)
4 (57.1)
Paresthesia
40 (51.2)
24 (52.1)
7 (41.1)
5 (62.5)
4 (57.1)
Bowel/bladder dysfunction
58 (74.3)
33 (71.7)
14 (82.3)
6 (75)
5 (71.4)
Follow-up, months (range)
89.7 (3e228)
93.2 (3e192)
76.6 (5e125)
99.4 (12e228)
85.4 (4e176)
Symptom duration, months
18.9
21.4
13.9
8.1
10.2
Endovascular
42
25
11
1
5
Surgery
21
14
5
2
0
Both
15
7
1
5
2
Improve
26 (33.3)
17 (30.4)
1 (5.8)
2 (25)
6 (85.7)
Stable
48 (61.5)
27 (65.2)
15 (88.2)
5 (62.5)
1 (14.3)
4 (5.1)
2 (4.4)
1 (5.8)
1 (12.5)
0
Pretreatment
3.57
3.63
2.23
4.37
5.57
Last follow-up
3.18
3.36
2.23
4.12
3.28
Treatment methods
Outcome at last follow-up (%)
Deteriorated Mean ALS
SDAVFs, spinal dural arteriovenous fistulas; PMAVFs, perimedullary arteriovenous fistulas; SAVMs, spinal arteriovenous malformations; AVFs, arteriovenous fistulas; ALS, Aminoff-Logue scale.
of age. Patients with AVMs were younger compared with patients with AVFs (P < 0.05). No family history of vascular malformations, spinal trauma, or surgery was noted for any patients at presentation. Among 78 patients, there were 46 (59%) SDAVFs, 17 (21.8%) PMAVFs, 8 (10.3%) SAVMs, and 7 (9%) extradural/paraspinal AVFs. The thoracic region was the most common location for SDAVFs (n ¼ 36; 78.3%), PMAVFs (n ¼ 9; 52.9%), and SAVMs (n ¼ 4; 50%); the lumbar region was the most common location for extradural AVFs (n ¼ 3; 42.9%). A single feeding artery was present in most of the SDAVF and PMAVF cases (n ¼ 39; 90.6% and n ¼ 12; 70.5%, respectively), whereas multiple feeding arteries were present in most SAVMs and extradural AVFs (n ¼ 5; 62.5% and n ¼ 4; 57.1%, respectively). Gait disturbance, sensory changes, weakness, and bowel and/or bladder dysfunction were the main symptoms in most of the
WORLD NEUROSURGERY -: e1-e8, - 2019
patients. The median interval between onset of symptoms and the date of diagnosis was 18.9 months (range, 3e185 months). The delay in diagnosis was <1 year in 21 patients (26.9%) and >3 years in 19 patients (24.3%). Median follow-up time was 93.2 months (range, 3e192 months) for SDAVFs, 76.6 months (range, 5e125 months) for PMAVFs, 99.4 months (range, 12e228 months) for SAVMs, and 85.4 months (range, 4e176 months) for extradural AVFs. No mortality was observed in the study. The mean ALS score before treatment was 3.63 for SDAVFs, 2.23 for PMAVFs, 4.37 for SAVMs, and 5.57 for extradural AVFs. The mean postoperative ALS score was 3.36 for SDAVFs, 2.23 for PMAVFs, 4.12 for SAVMs, and 3.28 for extradural AVFs. The difference between preoperative and postoperative ALS scores was found to be statistically significant (P ¼ 0.04). Neurologic status of 17 patients (36.9%) was improved after the treatment, and only 2 patients (4.3%) deteriorated in the
www.journals.elsevier.com/world-neurosurgery
e3
ORIGINAL ARTICLE MEHMET YIGIT AKGUN ET AL.
SPINAL VASCULAR MALFORMATIONS
Figure 1. Intraoperative images obtained in a patient with right T6 spinal dural arteriovenous fistula treated with microsurgical ligation. (A) The diagnosis of spinal dural arteriovenous fistula was based on the existence of a feeding osteodural artery (arrow), arteriovenous shunt located within the neural foramina, and drainage by radiculomedullary veins toward posterior spinal venous plexus. (B) After microsurgical ligation of the feeding osteodural artery, nerve roots of T6 and T7 are seen.
SDAVF group, whereas neurologic examination was unchanged in most of the patients in the PMAVF group (n ¼ 15; 88.2%) and only 1 patient (5.9%) deteriorated after the treatment. For SAVMs, 5 of 8 (62.5%) patients were the same, 2 patients (25%) improved, and 1 patient (12.5%) deteriorated after the treatment. For extradural AVFs, 6 of 7 patients (85. 7%) were improved after the treatment. The worst clinical outcomes among the groups were obtained in the SAVMs, whereas the best clinical outcomes were obtained in the extradural AVFs. Pretreatment ALS scores and long-term follow-up are summarized in Table 2. No statistically significant difference was found in postoperative ALS scores between treatment modalities (P ¼ 0.07). Of SDAVF cases, 14 patients (32.5%) were treated with microsurgical occlusion, 25 patients (54.3%) were treated with endovascular occlusion, and 7 patients (16.2%) were treated with microsurgery followed by embolization due to the failure of endovascular techniques. Complete occlusion of PMAVFs was attained by endovascular techniques only in 11 patients (64.7%), by surgery only in 5 patients (29.4%), and by both treatment modalities in 1 patient (5.8%). Among patients with SAVMs, 1 was treated with embolization that resulted in complete obliteration, 2 were treated with microsurgery that resulted in total resection, and 5 underwent embolization followed by microsurgical resection. Five patients with extradural AVFs were treated with embolization that resulted in complete obliteration, and 2 patients underwent embolization followed by microsurgical resection that resulted in complete obliteration. Overall, complete obliteration was achieved in 76 patients (97.4%). Subtotal occlusion was detected in 1 patient with SAVM who was treated with both modalities and 1 patient with PMAVF who was treated with endovascular techniques alone. Preoperative embolization did not significantly affect occlusion rates (P ¼ 0.4). The number of patients with
e4
www.SCIENCEDIRECT.com
Figure 2. A 41-year-old woman presented with progressive lower extremity weakness. (AeD) On magnetic resonance imaging, the conus level was observed to be swollen, and areas of T2 signal increase extending along the spinal cord to the lower thoracic level were observed. (A) Sagittal T2-weighted image. (B) Contrast-enhanced sagittal T1-weighted image. (C and D) Axial T2-weighted images. Tortuous vascular structures along the cord were observed in the contrast-enhanced series. (E and F) On selective spinal angiography, segmental artery injection of the left T9 level was observed with the fistula at the transverse foramina level and dilated tortuous perimedullary veins overlying the ascending radicular vein.
decreased gait and urinary scores was significantly greater after combined endovascular and surgical treatment than after singlemodality occlusion (P ¼ 0.001). Additionally, all 4 patients with deteriorated clinical findings were treated with combined modalities. Some cases in this series are illustrated in Figures 1e5.
DISCUSSION Although spinal vascular malformations constitute only 5%e9% of all vascular malformations of the central nervous system, they are a major cause of spinal cord dysfunction.5 The clinical presentation is the same, whereas the onset and sequence of neurologic findings and their progression rates are extremely variable. Pathophysiology is explained by an increase in venous pressure due to a congenital or acquired shunted blood flow
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.07.043
ORIGINAL ARTICLE MEHMET YIGIT AKGUN ET AL.
Figure 3. A 37-year-old man presented with progressive lower extremity weakness, erectile dysfunction, and urinary retention. (A and B) On magnetic resonance imaging, slight T2 signal increase along the cord and tortuous vascular structures adjacent to the cord were observed. (A) Sagittal T2-weighted image. (B) Axial T2-weighted image. (C) On selective spinal angiography, segmental artery injection performed at the left T8
reducing arteriovenous pressure gradient, which causes congestion in medullary veins and reduced intramedullary blood flow resulting in ischemic hypoxia.6 Moreover, there is general agreement concerning the acute neurologic decline for most patients with AVMs (associated with hematomyelia or subarachnoid hemorrhage) and PMAVFs, but rather a slow progression of the clinical picture for patients with dural and extradural AVFs.
Figure 4. Selective spinal angiography performed at the left L1 level by segmental artery injection showed a posterior arteriovenous malformation that was fed by the posterolateral spinal artery.
WORLD NEUROSURGERY -: e1-e8, - 2019
SPINAL VASCULAR MALFORMATIONS
level was observed with dilated tortuous perimedullary veins over the fistula and radicular vein at the level of transverse foramina. In addition, it was observed that the anterior spinal artery was fed at the same level. (D) On flat panel detector angiography, the Adamkiewicz artery, which has the characteristic hairpin appearance, feeding the anterior spinal artery is observed (arrow). Surgery was preferred in this case.
In early stages, the disease is characterized by slowly progressive, nonspecific symptoms, such as gait disturbances, paresthesia, diffuse sensory symptoms, and radicular pain; in the late stages, bowel and bladder incontinence, erectile dysfunction, and urinary retention may arise, especially for AVFs due to congestive myelopathy.7 Spinal cord AVMs that manifest with subarachnoid hemorrhage may often cause sudden and rapid development of excruciating back pain, with or without neurologic deficit. In our study, the frequency of presenting signs and symptoms was similar among the 4 groups except for a higher incidence of subarachnoid hemorrhage in spinal AVMs. MRI is key for evaluating spinal cord vascular malformations and complements the diagnosis. However, the gold standard method for definitive diagnosis is spinal angiography. Because of the nonspecific clinical presentation, a considerable number of patients with vascular malformation continue to be misdiagnosed and to receive unnecessary treatment. If the lesion is left untreated, 50% of patients will become severely disabled, and 10% will be able to walk independently after 3 years.8 By the time of diagnosis, most patients already have a certain degree of motor and sensory deficits.9 Timely and accurate diagnosis contributes greatly to the prognosis. We observed that patients benefit more from the intervention the earlier the diagnosis is made. In contrast, some studies were unable to demonstrate the influence of symptom duration on the degree of clinical improvement.10,11 In our study, treatment of patients was performed within 6 months of the first symptom in 58% of the patients with SDAVF and 66% of the patients with extradural AVF who showed clinical improvement. However, there was no correlation between the duration of treatment and clinical improvement in the other 2 groups. Besides the time interval from first symptom to treatment, the type of pathology was also associated with the results. The onset of symptoms was >3 years for all patients in our study with worsened clinical status.
www.journals.elsevier.com/world-neurosurgery
e5
ORIGINAL ARTICLE MEHMET YIGIT AKGUN ET AL.
SPINAL VASCULAR MALFORMATIONS
Figure 5. A 16-year-old boy presented with progressive lower extremity weakness. (AeC) Selective spinal angiography performed by segmental artery injection showed the filling perimedullary arteriovenous fistula at left T8 level (A and B) and right L2 level (C). A large venous aneurysm was observed in the proximal part of the drainage vein. (D) Embolization of the multiple feeders of the aneurysm sac and fistula was performed with a
In 1977, Kendall and Logue12 described SDAVFs as pathologic intrathecal veins with venous hypertension due to abnormal shunting from the arteries. SDAVFs are fed by radiculomeningeal arteries located in the dura mater of spinal nerve root sleeve and drain into the radiculomedullary veins, whereas SAVMs are generally fed by arteries that normally supply neural tissue, such as sulcocommissural branches of the ASA and perforating arteries of the posterior spinal artery. Perimedullary AVFs are arteriovenous shunts without nidus between the feeding artery and the draining vein. They are located on the surface of the spinal cord and are fed by vasocoronas originating from the ASA and/or the posterior spinal artery.13 Following the first surgical procedure by Ellsberg for spinal vascular malformation, surgical occlusion had been the mainstay treatment of these lesions.14 However, with advances in imaging modalities, technology, and embolic agents
e6
www.SCIENCEDIRECT.com
mixture of coils and glue/ethiodized oil. (E and F) On magnetic resonance imaging performed 1 week after embolization, the signal void was not observed in the aneurysm sac, which was dislocating the cord posteriorly. (E) Sagittal T2-weighted image. (F) Axial T2-weighted image. The areas of T2 signal extension extending along the compressed cord persisted.
as well as increasing popularity of endovascular techniques, endovascular embolization has become the primary treatment modality.15 In early attempts to treat these lesions endovascularly, polyvinyl alcohol particles were used with good results; however, acrylic glue (N-butyl cyanoacrylate) has become the most clearly established liquid embolic agent in the endovascular treatment.16 There are no data to support a standardized approach to the treatment of spinal vascular malformations. Although most authors consider embolization as the first-line treatment modality, additional surgical procedures for residual lesions are often required.17 In a similar vein, we offer endovascular embolization to all patients with spinal vascular malformations and reserve surgery for patients with difficult anatomy or failed embolization. Microsurgery was used as a treatment alone for the extradural AVF group only. In the present series, 53.8% of the lesions were treated endovascularly,
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.07.043
ORIGINAL ARTICLE MEHMET YIGIT AKGUN ET AL.
SPINAL VASCULAR MALFORMATIONS
and 19.2% were treated by both treatment modalities with high overall occlusion rate (97.4%) and low morbidity. Our occlusion rate is similar to the results of 100% and 94.5% for SDAVFs and PMAVFs reported in a study of mixed treatment modality approach.18 However, the occlusion rate of patients treated endovascularly was the lowest in the SAVM group. Additionally, the highest proportion of patients treated with both treatment modalities was in the SAVM group. Recurrent operations were performed in this group to achieve complete obliteration. Therefore, in contrast to the literature,19 patients with high complete obliteration (87.5%) rates were prevented from deteriorating clinically. Nevertheless, there was no significant difference in the preoperative and postoperative ALS scores in this group. We achieved complete obliteration in all patients with extradural AVFs, and our success rate was significantly higher than the current literature.20 Studies demonstrate that there are no differences in the obliteration rates between endovascular and microsurgical treatments, enabling a switch from embolization to surgery owing to either impossibility of embolization or inadequate occlusion.21 In agreement with the previous reports,22 we found no difference in outcomes and occlusion rates between the patients with AVFs and AVMs occluded endovascularly and those occluded surgically. However, the patients who underwent unsuccessful embolization attempts and required subsequent surgical occlusion (combined treatment) had significantly worse gait and urinary outcomes. Although there are limited data about this issue in the literature, we believe that better clinical results are obtained if the treatment modality is used alone, regardless of whether it is surgical or endovascular. In all our patients with clinical deterioration, we found that combined treatment was used more than once owing to structural intricacy of vascular malformations. For this reason, detailed evaluation and planning should be done in the preoperative period. Although high rates of combined treatment are seen for the SAVM group, it is possible to obtain great results in experienced centers. Clinical outcomes of patients with spinal vascular malformations are expressed in terms of ALS scores in the literature. Although pretreatment and follow-up spinal function was evaluated comparing the ALS scores in our series, we also recorded clinical results as improved or deteriorated or unchanged according to improvement or resolution of the presenting symptoms and physical examination. Preoperative and postoperative ALS scores of the patients were found to be consistent with the literature,23-25 showing better mean scores after treatment in all groups (3.36 for SDAVFs, 2.23 for PMAVFs, 4.12 for SAVMs, and 3.28 for extradural AVFs). However, physical examination revealed that the preoperative status was unchanged in most patients in the postoperative period.
REFERENCES 1. Takai K. Spinal arteriovenous shunts: angioarchitecture and historical changes in classification. Neurol Med Chir (Tokyo). 2017;57:356-365. 2. Cenzato M, Debernardi A, Stefini R, et al. Spinal dural arteriovenous fistulas: outcome and prognostic factors. Neurosurg Focus. 2012;32:E11.
Most of the published series have not directly stated functional outcomes, but modest improvements have been reported after occlusion.26 In our study, clinical worsening was observed more profoundly in the SAVM group. This result is attributed to the complexity of pathology, need for combined treatment, and severe clinical symptoms with acute onset. Although the time between the onset of symptoms and the diagnosis was shorter in this group, the decline in neurologic scores was attributed to poor neurologic presentation of the patients, as mentioned in the literature.27 Nevertheless, there was no significant difference between preoperative and postoperative ALS scores in general. Patients with spinal vascular malformations can be followed by magnetic resonance angiography and clinical evaluation in the postoperative period.27,28 However, our doctrine for the control of radiologic outcome is to perform early spinal DSA after the procedure to enable early revision surgery. In this way, we detected incomplete obliteration in 23% of the patients who underwent microsurgical occlusion and reoperated to complete the treatment before their discharge. Although there are not much data in the literature about early postoperative selective spinal angiography, we believe that it has an important role in obtaining near-perfect results. In all groups, we achieved a significant increase in the rate of total occlusion with early control as well as the absence of recurrence in the long-term follow-up. Spinal MRI is performed 1 month after the operation to observe the progression of intramedullary changes. Limitations Limitations of this study include the small cohort of patients, all of whom were treated at a single institution, and the retrospective study design.
CONCLUSIONS Both endovascular and surgical treatments of spinal vascular malformations resulted in significant long-term recovery from myelopathic symptoms and improvement in quality of life for most patients. The optimal first-line treatment strategy for each individual patient should be determined by an experienced interdisciplinary team based on the type of malformation and clinical and anatomic data. Early diagnosis and intervention are key to a positive outcome for these lesions. Treatment in symptomatic patients improves the prognosis but should be performed in specialized centers. The diagnostic difficulty resulting in tremendous delay in treatment remains the main problem in the management of this rare disease. More clinical studies with longer follow-up will enhance our experience in the treatment of spinal vascular lesions.
3. Marcus J, Schwarz J, Singh IP, et al. Spinal dural arteriovenous fistulas: a review. Curr Atheroscler Rep. 2013;15:335.
5. Jellinger K. Vascular malformations of the central nervous system: a morphological overview. Neurosurg Rev. 1986;9:177-216. 6. Aminoff MJ, Logue V. Clinical features of spinal vascular malformations. Brain. 1974;97:197-210.
4. Aminoff MJ, Logue V. The prognosis of patients with spinal vascular malformations. Brain. 1974; 97:211-218.
WORLD NEUROSURGERY -: e1-e8, - 2019
7. Schuss P, Daher FH, Greschus S, Vatter H, Guresir E. Surgical treatment of spinal dural
www.journals.elsevier.com/world-neurosurgery
e7
ORIGINAL ARTICLE MEHMET YIGIT AKGUN ET AL.
SPINAL VASCULAR MALFORMATIONS
arteriovenous fistula: management and long-term outcome in a single-center series. World Neurosurg. 2015;83:1002-1005.
16. Liu AH, Gobin P, Riina H. Endovascular surgery for vascular malformations of the spinal cord. Oper Tech Neurosurg. 2003;6:163-170.
8. da Costa L, Dehdashti AR, terBrugge KG. Spinal cord vascular shunts: spinal cord vascular malformations and dural arteriovenous fistulas. Neurosurg Focus. 2009;26:E6.
17. Hida K, Iwasaki Y, Goto K, Miyasaka K, Abe H. Results of the surgical treatment of perimedullary arteriovenous fistulas with special reference to embolization. J Neurosurg. 1999;90:198-205.
9. Sanborn MR, Crowley RW, Uschold T, Park MS, Albuquerque FC, McDougall CG. Spinal dural arteriovenous fistulas: how, when, and why. Neurosurgery. 2014;61:6-11. 10. Jellema K, Canta LR, Tijssen CC, van Rooij WJ, Koudstaal PJ, van Gijn J. Spinal dural arteriovenous fistulas: clinical features in 80 patients. J Neurol Neurosurg Psychiatr. 2003;74:1438-1440. 11. Durnford AJ, Hempenstall J, Sadek AR, et al. Degree and duration of functional improvement on long-term follow-up of spinal dural arteriovenous fistulae occluded by endovascular and surgical treatment. World Neurosurg. 2017;107:488-494. 12. Kendall BE, Logue V. Spinal epidural angiomatous malformations draining into intrathecal veins. Neuroradiology. 1977;13:181-189. 13. Cho K, Lee DY, Chung CK, et al. Treatment of spinal cord perimedullary arteriovenous fistula: embolization versus surgery. Neurosurgery. 2005;56: 232-239. 14. Bao YH, Ling F. Classification and therapeutic modalities of spinal vascular malformations in 80 patients. Neurosurgery. 1997;40:75-81. 15. Narvid J, Hetts SW, Larsen D, et al. Spinal dural arteriovenous fistulae: clinical features and longterm results. Neurosurgery. 2008;62:159-167.
e8
www.SCIENCEDIRECT.com
18. Rangel-Castilla L, Russin JJ, Zaidi HA, et al. Contemporary management of spinal AVFs and AVMs: lessons learned from 110 cases. Neurosurg Focus. 2014;37:E14. 19. Flores BC, Klinger DR, White JA, Batjer HH. Spinal vascular malformations: treatment strategies and outcome. Neurosurg Rev. 2017;40:15-28. 20. Takai K, Shojima M, Imai H, Saito N, Taniguchi M. Microsurgical and endovascular treatments of spinal extradural arteriovenous fistulas with or without intradural venous drainage. World Neurosurg. 2018;111:819-829. 21. Gross BA, Albuquerque FC, Moon K, McDougall CG. Validation of an ‘endovascularfirst’ approach to spinal dural arteriovenous fistulas: an intention-to-treat analysis. J Neurointerv Surg. 2017;9:102-105. 22. Gokhale S, Khan SA, McDonagh DL, Britz G. Comparison of surgical and endovascular approach in management of spinal dural arteriovenous fistulas: a single center experience of 27 patients. Surg Neurol Int. 2014;5:7. 23. Bretonnier M, Hénaux PL, Gaberel T, et al. Spinal dural arteriovenous fistulas: clinical outcome after surgery versus embolization: a retrospective study. World Neurosurg. 2019;127:e943-e949. 24. Kang MS, Kim KH, Park JY, et al. Comparison of endovascular embolization and surgery in the
treatment of spinal intradural dorsal arteriovenous fistulas. World Neurosurg. 2019;122:e1519-e1527. 25. Fiaschi P, Prior A, Sbaffi PF, et al. Spinal dural arteriovenous fistulas: clinical results and quality of life assessment with surgical treatment as a crucial therapy. The joint experience of two centers. World Neurosurg. 2019;122:e270-e278. 26. Gemmete JJ, Chaudhary N, Elias AE, et al. Spinal dural arteriovenous fistulas: clinical experience with endovascular treatment as a primary therapy at 2 academic referral centers. AJNR Am J Neuroradiol. 2013;34:1974-1979. 27. Park JE, Koo HW, Liu H, Jung SC, Park D, Suh DC. Clinical characteristics and treatment outcomes of spinal arteriovenous malformations. Clin Neuroradiol. 2018;28:39-46. 28. Endo T, Kajitani T, Inoue T, Sato K, Niizuma K, Endo H. Clinical characteristics of lumbosacral spinal dural arteriovenous fistula (DAVF)—comparison with thoracic DAVF. World Neurosurg. 2018; 110:383-388.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 3 May 2019; accepted 3 July 2019 Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.07.043 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.07.043
Spinal Vascular Malformations: Treatment and Outcome Mehmet Yigit Akgun1, Rahsan Kemerdere1, Mustafa Onur Ulu1, Orkhan Alizada1, Cihan Isler1, Osman Kizilkilic2, Civan Islak2, Murat Hanci1
BACKGROUND: Vascular malformations of the spinal cord are a rare and complex clinical entity and can lead to severe morbidity with progressive spinal cord symptoms if not treated properly. In early stages, the disease is characterized by slowly progressive, nonspecific symptoms, such as gait disturbance, paresthesia, diffuse sensory symptoms, and radicular pain; in the late stages, bowel and bladder incontinence, erectile dysfunction, and urinary retention may develop. In recent decades, understanding and treatment of spinal vascular malformations have improved with the evolution of diagnostic tools and treatment modalities; however, it is still difficult to manage these cases because of the complexity of the pathology. The aims of this study were to present the long-term outcomes of our patients and to discuss the optimal management strategies.
-
METHODS: We reviewed the records of 78 patients with spinal vascular malformations and performed a retrospective, single-center case series evaluating initial occlusion, recanalization, retreatment, and neurologic status of patients with dural arteriovenous fistulas, perimedullary arteriovenous fistulas, arteriovenous malformations, and extradural arteriovenous fistulas who had undergone embolization and/or surgery.
-
RESULTS: No mortality was observed. Complete obliteration was achieved in 76 patients (97.4%).
-
CONCLUSIONS: Both endovascular and surgical treatment of spinal vascular malformations resulted in
-
Key words Arteriovenous fistula - Outcome - Spinal - Treatment - Vascular malformations -
Abbreviations and Acronyms ALS: Aminoff and Logue scale ASA: Anterior spinal artery AVF: Arteriovenous fistula AVM: Arteriovenous malformation DSA: Digital subtraction angiography MRI: Magnetic resonance imaging
WORLD NEUROSURGERY -: e1-e8, - 2019
significant long-term recovery from myelopathic symptoms and improvement in quality of life for most patients.
INTRODUCTION
V
ascular malformations of the spinal cord are a rare and complex clinical entity and can lead to severe morbidity with progressive spinal cord symptoms if not treated properly. Several different classifications are used to classify vascular malformations of the spinal cord, but the most widely used one was proposed by Takai.1 In Takai’s classification,1 arteriovenous malformations (AVMs) are divided into 1) dural arteriovenous fistula (AVF), 2) intramedullary glomus-type AVMs, 3) intramedullary juvenile-type AVMs, 4) perimedullary AVF, and 5) extradural/paraspinal AVM/AVF. Spinal dural arteriovenous fistulas (SDAVFs) or type 1 malformations, also classified by Spetzler as intradural dorsal AVFs, are the most common vascular malformations of the spinal cord constituting approximately 75% in this group. Perimedullary AVFs (PMAVFs) are especially rare spinal AVMs, accounting for only 15%e40% of all cases.2 In recent decades, understanding and treatment of spinal vascular malformations have improved with the evolution of diagnostic tools and treatment modalities; however, it is still difficult to manage these cases because of the complexity of the pathology. On one hand, SDAVF is a treatable cause of acquired myelopathy, resulting in severe and progressive neurologic deficits. On the other hand, PMAVFs are generally more difficult to treat because of their complicated anatomy and physiology
PMAVF: Perimedullary arteriovenous fistula SDAVF: Spinal dural arteriovenous fistula From the Departments of 1Neurosurgery and 2Radiology, Istanbul University-Cerrahpasa, Cerrahpasa Medical Faculty, Istanbul, Turkey To whom correspondence should be addressed: Mehmet Yigit Akgun, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.07.043 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
www.journals.elsevier.com/world-neurosurgery
e1
ORIGINAL ARTICLE MEHMET YIGIT AKGUN ET AL.
SPINAL VASCULAR MALFORMATIONS
compared with SDAVFs.3 Microsurgical occlusion, endovascular embolization, and the combination of both are known to be effective approaches to occlude the shunt area or fistular nidus. The choice between surgical treatment and endovascular embolization remains controversial. To our knowledge, there is no report in the literature that discusses all 4 pathologies, SDAVFs, PMAVFs, SAVMs and extradural AVFs, in the same study. We present a series of patients with these pathologies treated via surgical, endovascular, and multimodal therapies. The aim of this study is to present the long-term outcome of our patients and to discuss the optimal management strategies. MATERIALS AND METHODS
www.SCIENCEDIRECT.com
Grade
Definition
Gait 0
Normal
1
Leg weakness, abnormal gait or stance, but no restriction of activity
2
Restricted activity, but not requiring support
3
Requiring 1 cane for walking
4
Requiring 2 canes for walking
5
Confined to wheelchair
Micturition
All procedures performed in the studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. We performed a retrospective, single-center case series evaluating initial occlusion, recanalization, retreatment, and neurologic status of patients with SDAVFs, PMAVFs, SAVMs, and extradural AVFs who had undergone embolization and/or surgery. We reviewed the records of 78 patients with spinal vascular malformations between 1999 and 2018. Data were collected retrospectively using a standardized form, including age, sex, symptoms, history of spinal trauma or surgery, treatment methods, treatment results, and magnetic resonance imaging (MRI) in Digital Imaging and Communications in Medicine data format. Patients were screened based on the following inclusion criteria: 1) The diagnosis was based on spinal angiography findings, and 2) complete clinical data and images were of adequate resolution for the analysis. Patients with incomplete clinical data and/or images not of adequate resolution for the analysis were excluded from the study. All patients underwent MRI and selective spinal digital subtraction angiography (DSA). The extent of abnormal hyperintensity areas in the spinal cord and signal flow voids in the dural sac were determined from sagittal T2-weighted MRI. Fistula locations were determined by DSA, and diagnosis was established. Recanalization or recurrence was defined as the presence of persistent arteriovenous shunting or fistula at the time of the first follow-up DSA compared with the initial posttreatment DSA. Clinical outcomes consisted of the recorded historical and physical examination components of neurosurgical follow-up appointments, and examination findings were compared with symptoms at presentation. Symptoms were recorded as improved if the patient experienced improvement or resolution of the presenting symptoms. Also, pretreatment and follow-up spinal function was evaluated using the Aminoff and Logue scale (ALS) scores (Table 1).4 At the time of angiography, definitive embolization was attempted if the pathologic radicular artery did not provide anterior spinal artery (ASA) supply. If the ASA supply was noted or the embolization could not be performed for technical reasons, the patient was referred for surgical intervention. The treatment strategy was the same for all patients, such that an attempt at endovascular obliteration was the first choice of treatment. Surgery was offered whenever embolization failed or was abandoned
e2
Table 1. Aminoff-Logue Scale
0
Normal
1
Hesitancy, urgency, frequency, altered sensation, but continent
2
Occasional urinary incontinence or retention
3
Total incontinence or persistent retention
Aminoff-Logue scale scores were used to clinically assess all patients before and after treatment. Because the primary aim of treatment is symptomatic and functional improvement, in particular for gait and urinary dysfunction, the Aminoff-Logue disability scale was introduced to facilitate long-term follow-up trends.
for technical reasons. The operation was performed under general anesthesia in the prone position. The appropriate spinal level was determined using C-arm. After a midline incision, double or triple laminectomy/laminotomy was performed, the dura mater was opened, and the fistula or arteriovenous lesion was identified. The nidus was resected in intramedullary AVMs, and the shunting vein to the perimedullary coronal venous plexus or the fistula was coagulated in dural AVFs. On the first postoperative day, control selective spinal DSA was routinely performed, and if residual filling or subtotal obliteration was detected, revision surgery and/ or an endovascular approach was implemented. All patients also underwent follow-up MRI at 1 month postoperatively. Physical rehabilitation in case of neurologic impairment was routinely started from the first postoperative day. Statistical Analysis Data are reported as mean SD, median for continuous variables, or the number of patients with sample population percentages for categorical variables. Statistical analysis was performed with IBM SPSS Version 21.0 software (IBM Corporation, Armonk, New York, USA), with P < 0.05 indicating statistical significance. For quantitative data, the Kolmogorov-Smirnov test was used to test the normal distribution. Kruskal-Wallis and Wilcoxon rank sum test were used for nonenormally distributed parameters. c2 test was to assess qualitative data. RESULTS Characteristics of patients and their pathologies are summarized in Table 2. There were 60 (76.9%) male and 18 (23.1%) female patients with a mean age of 47.21 19.27 years (range, 4e84 years) at initial symptom onset. Eleven patients were 18 years
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.07.043
ORIGINAL ARTICLE MEHMET YIGIT AKGUN ET AL.
SPINAL VASCULAR MALFORMATIONS
Table 2. Summary of Patients with Spinal Vascular Malformations Total Patients (n [ 78)
Patients with SDAVFs (n [ 46)
Patients with PMAVFs (n [ 17)
Patients with SAVMs (n [ 8)
Patients with Extradural AVFs (n [ 7)
Age, years
47.21
Male/female
60/18
54.65
32.5
24.75
43.7
37/9
13/4
6/2
4/3
Cervical
4
—
2
—
2
Thoracic
51
36
9
4
2
Lumbar
21
8
6
4
3
Sacral
2
2
—
—
—
Variables
Location
Clinical manifestations (%) Pain
59 (75.6)
37 (80)
12 (70.5)
5 (62.5)
5 (71.4)
Paresis
49 (62.8)
29 (63)
10 (58.8)
6 (75)
4 (57.1)
Paresthesia
40 (51.2)
24 (52.1)
7 (41.1)
5 (62.5)
4 (57.1)
Bowel/bladder dysfunction
58 (74.3)
33 (71.7)
14 (82.3)
6 (75)
5 (71.4)
Follow-up, months (range)
89.7 (3e228)
93.2 (3e192)
76.6 (5e125)
99.4 (12e228)
85.4 (4e176)
Symptom duration, months
18.9
21.4
13.9
8.1
10.2
Endovascular
42
25
11
1
5
Surgery
21
14
5
2
0
Both
15
7
1
5
2
Improve
26 (33.3)
17 (30.4)
1 (5.8)
2 (25)
6 (85.7)
Stable
48 (61.5)
27 (65.2)
15 (88.2)
5 (62.5)
1 (14.3)
4 (5.1)
2 (4.4)
1 (5.8)
1 (12.5)
0
Pretreatment
3.57
3.63
2.23
4.37
5.57
Last follow-up
3.18
3.36
2.23
4.12
3.28
Treatment methods
Outcome at last follow-up (%)
Deteriorated Mean ALS
SDAVFs, spinal dural arteriovenous fistulas; PMAVFs, perimedullary arteriovenous fistulas; SAVMs, spinal arteriovenous malformations; AVFs, arteriovenous fistulas; ALS, Aminoff-Logue scale.
of age. Patients with AVMs were younger compared with patients with AVFs (P < 0.05). No family history of vascular malformations, spinal trauma, or surgery was noted for any patients at presentation. Among 78 patients, there were 46 (59%) SDAVFs, 17 (21.8%) PMAVFs, 8 (10.3%) SAVMs, and 7 (9%) extradural/paraspinal AVFs. The thoracic region was the most common location for SDAVFs (n ¼ 36; 78.3%), PMAVFs (n ¼ 9; 52.9%), and SAVMs (n ¼ 4; 50%); the lumbar region was the most common location for extradural AVFs (n ¼ 3; 42.9%). A single feeding artery was present in most of the SDAVF and PMAVF cases (n ¼ 39; 90.6% and n ¼ 12; 70.5%, respectively), whereas multiple feeding arteries were present in most SAVMs and extradural AVFs (n ¼ 5; 62.5% and n ¼ 4; 57.1%, respectively). Gait disturbance, sensory changes, weakness, and bowel and/or bladder dysfunction were the main symptoms in most of the
WORLD NEUROSURGERY -: e1-e8, - 2019
patients. The median interval between onset of symptoms and the date of diagnosis was 18.9 months (range, 3e185 months). The delay in diagnosis was <1 year in 21 patients (26.9%) and >3 years in 19 patients (24.3%). Median follow-up time was 93.2 months (range, 3e192 months) for SDAVFs, 76.6 months (range, 5e125 months) for PMAVFs, 99.4 months (range, 12e228 months) for SAVMs, and 85.4 months (range, 4e176 months) for extradural AVFs. No mortality was observed in the study. The mean ALS score before treatment was 3.63 for SDAVFs, 2.23 for PMAVFs, 4.37 for SAVMs, and 5.57 for extradural AVFs. The mean postoperative ALS score was 3.36 for SDAVFs, 2.23 for PMAVFs, 4.12 for SAVMs, and 3.28 for extradural AVFs. The difference between preoperative and postoperative ALS scores was found to be statistically significant (P ¼ 0.04). Neurologic status of 17 patients (36.9%) was improved after the treatment, and only 2 patients (4.3%) deteriorated in the
www.journals.elsevier.com/world-neurosurgery
e3
ORIGINAL ARTICLE MEHMET YIGIT AKGUN ET AL.
SPINAL VASCULAR MALFORMATIONS
Figure 1. Intraoperative images obtained in a patient with right T6 spinal dural arteriovenous fistula treated with microsurgical ligation. (A) The diagnosis of spinal dural arteriovenous fistula was based on the existence of a feeding osteodural artery (arrow), arteriovenous shunt located within the neural foramina, and drainage by radiculomedullary veins toward posterior spinal venous plexus. (B) After microsurgical ligation of the feeding osteodural artery, nerve roots of T6 and T7 are seen.
SDAVF group, whereas neurologic examination was unchanged in most of the patients in the PMAVF group (n ¼ 15; 88.2%) and only 1 patient (5.9%) deteriorated after the treatment. For SAVMs, 5 of 8 (62.5%) patients were the same, 2 patients (25%) improved, and 1 patient (12.5%) deteriorated after the treatment. For extradural AVFs, 6 of 7 patients (85. 7%) were improved after the treatment. The worst clinical outcomes among the groups were obtained in the SAVMs, whereas the best clinical outcomes were obtained in the extradural AVFs. Pretreatment ALS scores and long-term follow-up are summarized in Table 2. No statistically significant difference was found in postoperative ALS scores between treatment modalities (P ¼ 0.07). Of SDAVF cases, 14 patients (32.5%) were treated with microsurgical occlusion, 25 patients (54.3%) were treated with endovascular occlusion, and 7 patients (16.2%) were treated with microsurgery followed by embolization due to the failure of endovascular techniques. Complete occlusion of PMAVFs was attained by endovascular techniques only in 11 patients (64.7%), by surgery only in 5 patients (29.4%), and by both treatment modalities in 1 patient (5.8%). Among patients with SAVMs, 1 was treated with embolization that resulted in complete obliteration, 2 were treated with microsurgery that resulted in total resection, and 5 underwent embolization followed by microsurgical resection. Five patients with extradural AVFs were treated with embolization that resulted in complete obliteration, and 2 patients underwent embolization followed by microsurgical resection that resulted in complete obliteration. Overall, complete obliteration was achieved in 76 patients (97.4%). Subtotal occlusion was detected in 1 patient with SAVM who was treated with both modalities and 1 patient with PMAVF who was treated with endovascular techniques alone. Preoperative embolization did not significantly affect occlusion rates (P ¼ 0.4). The number of patients with
e4
www.SCIENCEDIRECT.com
Figure 2. A 41-year-old woman presented with progressive lower extremity weakness. (AeD) On magnetic resonance imaging, the conus level was observed to be swollen, and areas of T2 signal increase extending along the spinal cord to the lower thoracic level were observed. (A) Sagittal T2-weighted image. (B) Contrast-enhanced sagittal T1-weighted image. (C and D) Axial T2-weighted images. Tortuous vascular structures along the cord were observed in the contrast-enhanced series. (E and F) On selective spinal angiography, segmental artery injection of the left T9 level was observed with the fistula at the transverse foramina level and dilated tortuous perimedullary veins overlying the ascending radicular vein.
decreased gait and urinary scores was significantly greater after combined endovascular and surgical treatment than after singlemodality occlusion (P ¼ 0.001). Additionally, all 4 patients with deteriorated clinical findings were treated with combined modalities. Some cases in this series are illustrated in Figures 1e5.
DISCUSSION Although spinal vascular malformations constitute only 5%e9% of all vascular malformations of the central nervous system, they are a major cause of spinal cord dysfunction.5 The clinical presentation is the same, whereas the onset and sequence of neurologic findings and their progression rates are extremely variable. Pathophysiology is explained by an increase in venous pressure due to a congenital or acquired shunted blood flow
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.07.043
ORIGINAL ARTICLE MEHMET YIGIT AKGUN ET AL.
Figure 3. A 37-year-old man presented with progressive lower extremity weakness, erectile dysfunction, and urinary retention. (A and B) On magnetic resonance imaging, slight T2 signal increase along the cord and tortuous vascular structures adjacent to the cord were observed. (A) Sagittal T2-weighted image. (B) Axial T2-weighted image. (C) On selective spinal angiography, segmental artery injection performed at the left T8
reducing arteriovenous pressure gradient, which causes congestion in medullary veins and reduced intramedullary blood flow resulting in ischemic hypoxia.6 Moreover, there is general agreement concerning the acute neurologic decline for most patients with AVMs (associated with hematomyelia or subarachnoid hemorrhage) and PMAVFs, but rather a slow progression of the clinical picture for patients with dural and extradural AVFs.
Figure 4. Selective spinal angiography performed at the left L1 level by segmental artery injection showed a posterior arteriovenous malformation that was fed by the posterolateral spinal artery.
WORLD NEUROSURGERY -: e1-e8, - 2019
SPINAL VASCULAR MALFORMATIONS
level was observed with dilated tortuous perimedullary veins over the fistula and radicular vein at the level of transverse foramina. In addition, it was observed that the anterior spinal artery was fed at the same level. (D) On flat panel detector angiography, the Adamkiewicz artery, which has the characteristic hairpin appearance, feeding the anterior spinal artery is observed (arrow). Surgery was preferred in this case.
In early stages, the disease is characterized by slowly progressive, nonspecific symptoms, such as gait disturbances, paresthesia, diffuse sensory symptoms, and radicular pain; in the late stages, bowel and bladder incontinence, erectile dysfunction, and urinary retention may arise, especially for AVFs due to congestive myelopathy.7 Spinal cord AVMs that manifest with subarachnoid hemorrhage may often cause sudden and rapid development of excruciating back pain, with or without neurologic deficit. In our study, the frequency of presenting signs and symptoms was similar among the 4 groups except for a higher incidence of subarachnoid hemorrhage in spinal AVMs. MRI is key for evaluating spinal cord vascular malformations and complements the diagnosis. However, the gold standard method for definitive diagnosis is spinal angiography. Because of the nonspecific clinical presentation, a considerable number of patients with vascular malformation continue to be misdiagnosed and to receive unnecessary treatment. If the lesion is left untreated, 50% of patients will become severely disabled, and 10% will be able to walk independently after 3 years.8 By the time of diagnosis, most patients already have a certain degree of motor and sensory deficits.9 Timely and accurate diagnosis contributes greatly to the prognosis. We observed that patients benefit more from the intervention the earlier the diagnosis is made. In contrast, some studies were unable to demonstrate the influence of symptom duration on the degree of clinical improvement.10,11 In our study, treatment of patients was performed within 6 months of the first symptom in 58% of the patients with SDAVF and 66% of the patients with extradural AVF who showed clinical improvement. However, there was no correlation between the duration of treatment and clinical improvement in the other 2 groups. Besides the time interval from first symptom to treatment, the type of pathology was also associated with the results. The onset of symptoms was >3 years for all patients in our study with worsened clinical status.
www.journals.elsevier.com/world-neurosurgery
e5
ORIGINAL ARTICLE MEHMET YIGIT AKGUN ET AL.
SPINAL VASCULAR MALFORMATIONS
Figure 5. A 16-year-old boy presented with progressive lower extremity weakness. (AeC) Selective spinal angiography performed by segmental artery injection showed the filling perimedullary arteriovenous fistula at left T8 level (A and B) and right L2 level (C). A large venous aneurysm was observed in the proximal part of the drainage vein. (D) Embolization of the multiple feeders of the aneurysm sac and fistula was performed with a
In 1977, Kendall and Logue12 described SDAVFs as pathologic intrathecal veins with venous hypertension due to abnormal shunting from the arteries. SDAVFs are fed by radiculomeningeal arteries located in the dura mater of spinal nerve root sleeve and drain into the radiculomedullary veins, whereas SAVMs are generally fed by arteries that normally supply neural tissue, such as sulcocommissural branches of the ASA and perforating arteries of the posterior spinal artery. Perimedullary AVFs are arteriovenous shunts without nidus between the feeding artery and the draining vein. They are located on the surface of the spinal cord and are fed by vasocoronas originating from the ASA and/or the posterior spinal artery.13 Following the first surgical procedure by Ellsberg for spinal vascular malformation, surgical occlusion had been the mainstay treatment of these lesions.14 However, with advances in imaging modalities, technology, and embolic agents
e6
www.SCIENCEDIRECT.com
mixture of coils and glue/ethiodized oil. (E and F) On magnetic resonance imaging performed 1 week after embolization, the signal void was not observed in the aneurysm sac, which was dislocating the cord posteriorly. (E) Sagittal T2-weighted image. (F) Axial T2-weighted image. The areas of T2 signal extension extending along the compressed cord persisted.
as well as increasing popularity of endovascular techniques, endovascular embolization has become the primary treatment modality.15 In early attempts to treat these lesions endovascularly, polyvinyl alcohol particles were used with good results; however, acrylic glue (N-butyl cyanoacrylate) has become the most clearly established liquid embolic agent in the endovascular treatment.16 There are no data to support a standardized approach to the treatment of spinal vascular malformations. Although most authors consider embolization as the first-line treatment modality, additional surgical procedures for residual lesions are often required.17 In a similar vein, we offer endovascular embolization to all patients with spinal vascular malformations and reserve surgery for patients with difficult anatomy or failed embolization. Microsurgery was used as a treatment alone for the extradural AVF group only. In the present series, 53.8% of the lesions were treated endovascularly,
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.07.043
ORIGINAL ARTICLE MEHMET YIGIT AKGUN ET AL.
SPINAL VASCULAR MALFORMATIONS
and 19.2% were treated by both treatment modalities with high overall occlusion rate (97.4%) and low morbidity. Our occlusion rate is similar to the results of 100% and 94.5% for SDAVFs and PMAVFs reported in a study of mixed treatment modality approach.18 However, the occlusion rate of patients treated endovascularly was the lowest in the SAVM group. Additionally, the highest proportion of patients treated with both treatment modalities was in the SAVM group. Recurrent operations were performed in this group to achieve complete obliteration. Therefore, in contrast to the literature,19 patients with high complete obliteration (87.5%) rates were prevented from deteriorating clinically. Nevertheless, there was no significant difference in the preoperative and postoperative ALS scores in this group. We achieved complete obliteration in all patients with extradural AVFs, and our success rate was significantly higher than the current literature.20 Studies demonstrate that there are no differences in the obliteration rates between endovascular and microsurgical treatments, enabling a switch from embolization to surgery owing to either impossibility of embolization or inadequate occlusion.21 In agreement with the previous reports,22 we found no difference in outcomes and occlusion rates between the patients with AVFs and AVMs occluded endovascularly and those occluded surgically. However, the patients who underwent unsuccessful embolization attempts and required subsequent surgical occlusion (combined treatment) had significantly worse gait and urinary outcomes. Although there are limited data about this issue in the literature, we believe that better clinical results are obtained if the treatment modality is used alone, regardless of whether it is surgical or endovascular. In all our patients with clinical deterioration, we found that combined treatment was used more than once owing to structural intricacy of vascular malformations. For this reason, detailed evaluation and planning should be done in the preoperative period. Although high rates of combined treatment are seen for the SAVM group, it is possible to obtain great results in experienced centers. Clinical outcomes of patients with spinal vascular malformations are expressed in terms of ALS scores in the literature. Although pretreatment and follow-up spinal function was evaluated comparing the ALS scores in our series, we also recorded clinical results as improved or deteriorated or unchanged according to improvement or resolution of the presenting symptoms and physical examination. Preoperative and postoperative ALS scores of the patients were found to be consistent with the literature,23-25 showing better mean scores after treatment in all groups (3.36 for SDAVFs, 2.23 for PMAVFs, 4.12 for SAVMs, and 3.28 for extradural AVFs). However, physical examination revealed that the preoperative status was unchanged in most patients in the postoperative period.
REFERENCES 1. Takai K. Spinal arteriovenous shunts: angioarchitecture and historical changes in classification. Neurol Med Chir (Tokyo). 2017;57:356-365. 2. Cenzato M, Debernardi A, Stefini R, et al. Spinal dural arteriovenous fistulas: outcome and prognostic factors. Neurosurg Focus. 2012;32:E11.
Most of the published series have not directly stated functional outcomes, but modest improvements have been reported after occlusion.26 In our study, clinical worsening was observed more profoundly in the SAVM group. This result is attributed to the complexity of pathology, need for combined treatment, and severe clinical symptoms with acute onset. Although the time between the onset of symptoms and the diagnosis was shorter in this group, the decline in neurologic scores was attributed to poor neurologic presentation of the patients, as mentioned in the literature.27 Nevertheless, there was no significant difference between preoperative and postoperative ALS scores in general. Patients with spinal vascular malformations can be followed by magnetic resonance angiography and clinical evaluation in the postoperative period.27,28 However, our doctrine for the control of radiologic outcome is to perform early spinal DSA after the procedure to enable early revision surgery. In this way, we detected incomplete obliteration in 23% of the patients who underwent microsurgical occlusion and reoperated to complete the treatment before their discharge. Although there are not much data in the literature about early postoperative selective spinal angiography, we believe that it has an important role in obtaining near-perfect results. In all groups, we achieved a significant increase in the rate of total occlusion with early control as well as the absence of recurrence in the long-term follow-up. Spinal MRI is performed 1 month after the operation to observe the progression of intramedullary changes. Limitations Limitations of this study include the small cohort of patients, all of whom were treated at a single institution, and the retrospective study design.
CONCLUSIONS Both endovascular and surgical treatments of spinal vascular malformations resulted in significant long-term recovery from myelopathic symptoms and improvement in quality of life for most patients. The optimal first-line treatment strategy for each individual patient should be determined by an experienced interdisciplinary team based on the type of malformation and clinical and anatomic data. Early diagnosis and intervention are key to a positive outcome for these lesions. Treatment in symptomatic patients improves the prognosis but should be performed in specialized centers. The diagnostic difficulty resulting in tremendous delay in treatment remains the main problem in the management of this rare disease. More clinical studies with longer follow-up will enhance our experience in the treatment of spinal vascular lesions.
3. Marcus J, Schwarz J, Singh IP, et al. Spinal dural arteriovenous fistulas: a review. Curr Atheroscler Rep. 2013;15:335.
5. Jellinger K. Vascular malformations of the central nervous system: a morphological overview. Neurosurg Rev. 1986;9:177-216. 6. Aminoff MJ, Logue V. Clinical features of spinal vascular malformations. Brain. 1974;97:197-210.
4. Aminoff MJ, Logue V. The prognosis of patients with spinal vascular malformations. Brain. 1974; 97:211-218.
WORLD NEUROSURGERY -: e1-e8, - 2019
7. Schuss P, Daher FH, Greschus S, Vatter H, Guresir E. Surgical treatment of spinal dural
www.journals.elsevier.com/world-neurosurgery
e7
ORIGINAL ARTICLE MEHMET YIGIT AKGUN ET AL.
SPINAL VASCULAR MALFORMATIONS
arteriovenous fistula: management and long-term outcome in a single-center series. World Neurosurg. 2015;83:1002-1005.
16. Liu AH, Gobin P, Riina H. Endovascular surgery for vascular malformations of the spinal cord. Oper Tech Neurosurg. 2003;6:163-170.
8. da Costa L, Dehdashti AR, terBrugge KG. Spinal cord vascular shunts: spinal cord vascular malformations and dural arteriovenous fistulas. Neurosurg Focus. 2009;26:E6.
17. Hida K, Iwasaki Y, Goto K, Miyasaka K, Abe H. Results of the surgical treatment of perimedullary arteriovenous fistulas with special reference to embolization. J Neurosurg. 1999;90:198-205.
9. Sanborn MR, Crowley RW, Uschold T, Park MS, Albuquerque FC, McDougall CG. Spinal dural arteriovenous fistulas: how, when, and why. Neurosurgery. 2014;61:6-11. 10. Jellema K, Canta LR, Tijssen CC, van Rooij WJ, Koudstaal PJ, van Gijn J. Spinal dural arteriovenous fistulas: clinical features in 80 patients. J Neurol Neurosurg Psychiatr. 2003;74:1438-1440. 11. Durnford AJ, Hempenstall J, Sadek AR, et al. Degree and duration of functional improvement on long-term follow-up of spinal dural arteriovenous fistulae occluded by endovascular and surgical treatment. World Neurosurg. 2017;107:488-494. 12. Kendall BE, Logue V. Spinal epidural angiomatous malformations draining into intrathecal veins. Neuroradiology. 1977;13:181-189. 13. Cho K, Lee DY, Chung CK, et al. Treatment of spinal cord perimedullary arteriovenous fistula: embolization versus surgery. Neurosurgery. 2005;56: 232-239. 14. Bao YH, Ling F. Classification and therapeutic modalities of spinal vascular malformations in 80 patients. Neurosurgery. 1997;40:75-81. 15. Narvid J, Hetts SW, Larsen D, et al. Spinal dural arteriovenous fistulae: clinical features and longterm results. Neurosurgery. 2008;62:159-167.
e8
www.SCIENCEDIRECT.com
18. Rangel-Castilla L, Russin JJ, Zaidi HA, et al. Contemporary management of spinal AVFs and AVMs: lessons learned from 110 cases. Neurosurg Focus. 2014;37:E14. 19. Flores BC, Klinger DR, White JA, Batjer HH. Spinal vascular malformations: treatment strategies and outcome. Neurosurg Rev. 2017;40:15-28. 20. Takai K, Shojima M, Imai H, Saito N, Taniguchi M. Microsurgical and endovascular treatments of spinal extradural arteriovenous fistulas with or without intradural venous drainage. World Neurosurg. 2018;111:819-829. 21. Gross BA, Albuquerque FC, Moon K, McDougall CG. Validation of an ‘endovascularfirst’ approach to spinal dural arteriovenous fistulas: an intention-to-treat analysis. J Neurointerv Surg. 2017;9:102-105. 22. Gokhale S, Khan SA, McDonagh DL, Britz G. Comparison of surgical and endovascular approach in management of spinal dural arteriovenous fistulas: a single center experience of 27 patients. Surg Neurol Int. 2014;5:7. 23. Bretonnier M, Hénaux PL, Gaberel T, et al. Spinal dural arteriovenous fistulas: clinical outcome after surgery versus embolization: a retrospective study. World Neurosurg. 2019;127:e943-e949. 24. Kang MS, Kim KH, Park JY, et al. Comparison of endovascular embolization and surgery in the
treatment of spinal intradural dorsal arteriovenous fistulas. World Neurosurg. 2019;122:e1519-e1527. 25. Fiaschi P, Prior A, Sbaffi PF, et al. Spinal dural arteriovenous fistulas: clinical results and quality of life assessment with surgical treatment as a crucial therapy. The joint experience of two centers. World Neurosurg. 2019;122:e270-e278. 26. Gemmete JJ, Chaudhary N, Elias AE, et al. Spinal dural arteriovenous fistulas: clinical experience with endovascular treatment as a primary therapy at 2 academic referral centers. AJNR Am J Neuroradiol. 2013;34:1974-1979. 27. Park JE, Koo HW, Liu H, Jung SC, Park D, Suh DC. Clinical characteristics and treatment outcomes of spinal arteriovenous malformations. Clin Neuroradiol. 2018;28:39-46. 28. Endo T, Kajitani T, Inoue T, Sato K, Niizuma K, Endo H. Clinical characteristics of lumbosacral spinal dural arteriovenous fistula (DAVF)—comparison with thoracic DAVF. World Neurosurg. 2018; 110:383-388.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 3 May 2019; accepted 3 July 2019 Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.07.043 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.07.043