REVIEW REVIEW
Recurrence Rates After Surgical or Endovascular Treatment of Spinal Dural Arteriovenous Fistulas: A Meta-analysis Nicolaas A. Bakker, MD, PhD* Maarten Uyttenboogaart, MD, PhD‡§ G.J. Luijckx, MD, PhD§ Omid S. Eshghi, MD‡ Aryan Mazuri, MD‡ Jan D.M. Metzemaekers, MD, PhD* Rob J.M. Groen, MD, PhD* J. Marc C. Van Dijk, MD, PhD* From the Departments of *Neurosurgery, ‡Radiology, and §Neurology, University of Groningen, University Medical Center Groningen, Groningen, the Netherlands Correspondence: Nicolaas A. Bakker, MD, PhD, Department of Neurosurgery, University Medical Center Groningen, PO Box 30.001, 9700 RB Groningen, Netherlands. E-mail: [email protected] Received, December 1, 2014. Accepted, February 3, 2015. Published Online, March 18, 2015. Copyright © 2015 by the Congress of Neurological Surgeons.
BACKGROUND: There is an increasing tendency to treat spinal dural arteriovenous fistulas (SDAVFs) endovascularly despite the lack of clear evidence favoring embolization over surgery. OBJECTIVE: To compare the initial failure and recurrence rates of primary treatment of SDAVFs by surgery and endovascular techniques. METHODS: A meta-analysis using the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) standard was performed. All the English literature from 2004 onward was evaluated. From each article that compared the 2 treatment modalities, the odds ratio (OR) was calculated. Combined ORs were calculated with Review Manager 5.3 of The Cochrane Collaboration. RESULTS: A total of 35 studies harboring 1112 patients were assessed. Initial definitive fistula occlusion was observed in 588 of 609 surgical patients (96.6%; 95% confidence interval [CI], 94.8-97.8) vs 363 of 503 endovascularly treated patients (72.2%; 95% CI, 68.1-75.9; P , .001). The combined OR from 18 studies that assessed both treatment modalities (730 patients) was 6.15 (95% CI, 3.45-11.0) in favor of surgical treatment. Late recurrence (13 studies, 480 patients) revealed an OR of 3.15 (95% CI, 1.66-5.96; P , .001) in favor of surgery. In a subgroup, recurrence was reported in 10 of 22 patients (45%) treated with Onyx vs 8 of 35 (23%) treated with n-butyle-2-cyanoacrylate (OR, 2.51; 95% CI, 0.75-8.37; P = .13). CONCLUSION: Although hampered by inclusion of poor quality studies, this metaanalysis shows a definite advantage of primary surgical treatment of SDAVF over endovascular treatment in initial failure rate and late recurrences. The often-used argument that endovascular techniques have improved and therefore outweigh surgery is not supported by this meta-analysis. KEY WORDS: Endovascular techniques, Meta-analysis, Spinal DAVF Neurosurgery 77:137–144, 2015
DOI: 10.1227/NEU.0000000000000727
S
pinal dural arteriovenous fistulas (SDAVFs), also known as type I spinal arteriovenous malformations, are the most common spinal vascular disorder. Diagnosis of an SDAVF is often challenging because of its heterogeneous presentation that can mimic other neurological disorders. A typical SDAVF is fed by a radicular
ABBREVIATIONS: CI, confidence interval; DSA, digital subtraction angiography; MeSH, Medical Subject Headings; NBCA, n-butyl 2-cyanoacrylate; OR, odds ratio; PRISMA, Preferred Reporting Items for Systematic Reviews and Meta-Analyses; SDAVF, spinal dural arteriovenous fistula
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artery and drains into a medullary vein, leading to a dilated perimedullary venous plexus and spinal cord congestion. The classic clinical picture is that of a progressive thoracic myelopathy. Surgical treatment, in which the fistula is disconnected intradurally, is associated with complete cure in the vast majority of patients.1,2 The procedure is straightforward, and complication rates are low.2 However, sometimes multilevel laminectomies are performed if the SDAVF is difficult to locate. In addition, because the dura mater has to be opened during the procedure, postoperative cerebrospinal fluid leakage can be observed after surgery. These complications may lead to a longer hospital stay. Therefore, as an alternative
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method, endovascular treatment has gained interest over the last decades.1 It is minimally invasive, and the treatment of the fistula can often be performed in combination with the diagnostic procedure. In 2004, Steinmetz et al3 reported in a meta-analysis that definitive cure rates are much lower after endovascular treatment compared with microsurgical treatment. In practice, it is observed that reaching the draining intradural vein via the endovascular route can be difficult. Over the last years, endovascular techniques and materials have generally improved. In additional, new liquid embolic agents such as Onyx, showing good results in the transarterial embolization of cranial DAVFs,4 have become available. On the other hand, surgical techniques have also improved, with better preoperative fistula localization5-7 and the application of novel minimally invasive techniques.8 In view of these recent developments, it was our aim to perform an updated meta-analysis of the literature over the past 10 years to compare the results of primary endovascular treatment with microsurgical treatment of SDAVFs.
METHODS Literature Search Three electronic databases were searched: MEDLINE (PubMed), CENTRAL (Cochrane Central Register of Controlled Trials), and EMBASE. Only the English literature was considered. Databases were scrutinized for studies published from January 2004 to September 2013. MeSH (Medical Subject Headings) terms were the following: SDAVF (all fields) or spinal dural arteriovenous (all fields) or spinal AVM and treatment (all fields). In addition, reference lists of all selected studies were scrutinized for additional studies. Studies assessing $5 patients were considered eligible. Reviews and studies included in the meta-analysis of Steinmetz et al3 from 2004 were excluded. Two reviewers (N.A.B. and J. M.C.V.D.) independently screened titles and abstracts of all retrieved articles. We obtained full-text reports of studies that were likely to report treatment outcome of SDAVFs. Studies that did not compare the 2 treatment modalities in a way to obtain 2 · 2 tables but reported outcomes of a single treatment modality (ie, surgery or endovascular treatment) were also included. In the case of multiple publications on the same data set, we used only the most recent publication to obtain unique cases. In case of disagreement between the 2 reviewers, consensus was reached by discussion. Figure 1 shows the flow chart according to the PRISMA (Preferred Reporting Items for Systematic Reviews and MetaAnalyses) statement.9 The 2 observers independently assessed the included articles.
Data Extraction All data were extracted with the use of a case-based format; patients in whom several treatments were performed were regarded as 1 single case; only the first intended treatment was registered. From all included studies, the following data were extracted and reported with the use of a predefined data extraction form (if available): (1) number of patients with an SDAVF; (2) type of treatment (surgical vs endovascular; patients initially treated with polyvinyl ethanol and surgery thereafter were regarded surgical patients); (3) rate of treatment failure, initial and late recurrence; (4) type of compound used for endovascular treatment (n-butyl 2-cyanoacrylate [NBCA] vs Onyx [Covidien, Mansfield, Massachusetts]); (5) location of fistula (craniocervical
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DAVFs were excluded); (6) time of follow-up; (7) complications related to the procedure other than recurrence of the fistula (minor [eg, wound infection, cerebrospinal fluid fistula requiring treatment] or major [leading to permanent neurological deficits]); and (8) type of study (randomized controlled trial, observational cohort, etc). No individual patient data could be derived from the majority of included studies.
Outcome Measures and Statistics Primary outcome was the failure of initial treatment or recurrence of the fistula. The latter was also assessed in a separate analysis in which late recurrence was defined as symptomatic reopening of the fistula .1 month after treatment. Initial success of treatment of the SDAVF had to be confirmed during control digital subtraction angiography (DSA) after surgery or directly after endovascular treatment. Recurrence of the fistula during follow-up was recorded either during routine follow-up imaging with magnetic resonance angiography or DSA or during clinical followup and subsequent imaging in case of clinical deterioration. In addition, the type of compound used (NBCA and derivatives vs Onyx) and its possible association with recurrence rates, as well as the number of complications from each treatment modality, were also taken into account as a secondary outcome measure. Assessment of risk of bias of the included studies was performed according to the Cochrane handbook for systematic reviews of interventions.10 Because substantial bias was potentially present in all of the included studies, funnels plots were used to estimate publication bias for all analyses (Figure 2A-2C). Continuous variables were expressed as mean with standard deviation or median and range, and categorical variables were expressed as counts and percentages with the use of SPSS software (version 20.0). Ninety-five percent confidence intervals (CIs) of the proportion were calculated by use of the Wilson procedure without continuity correction. From each article in which it was possible to compare the 2 treatment modalities (n = 18), the odds ratio (OR) was calculated from a 2 · 2 table. These were the studies included in the meta-analyses. Combined ORs and 95% CIs were calculated with RevMan (Review Manager, version 5.3. Copenhagen; The Nordic Cochrane Centre, The Cochrane Collaboration, 2014). Study heterogeneity was assessed with the I2 statistics for inconsistency. A value of .50% was considered substantial heterogeneity. In the case of statistical homogeneity, we used a fixed-effect model.
RESULTS Primary Outcome: Initial Failure or Late Recurrence Rate of SDAVFs A total of 35 studies harboring 1112 patients were included for the pooled data analysis (Table). From all surgical patients, initial treatment failure or recurrence was reported in 21 if 609 patients, leading to a successful treatment percentage of 96.6% (95% CI, 94.8-97.8). In the endovascularly treated patients, initial failure or recurrence was reported in 140 of 503 patients; thus, the successful treatment percentage was 72.2% (95% CI, 68.1-75.1; P , .001). Overall study quality was poor; only retrospective case series were available. Twenty studies directly compared endovascular and surgical treatment; 15 studies reported 1 treatment technique only (12 microsurgical and 3 endovascular). Follow-up was highly heterogeneous (Table).
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FIGURE 1. Flowchart according to the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) statement.
From all studies (n = 18730 patients) included in the metaanalysis (Figure 3), the OR was obtained, leading to a combined OR of 6.15 (95% CI, 3.45-11.0) in favor of surgical treatment. In 13 studies (480 patients; Figure 4), it was possible to extract data on the time of treatment failure (either direct or late). In terms of the risk of late recurrence, an OR of 3.15 (95% CI, 1.665.96; P , .001) in favor of surgical treatment was observed. Recurrences were observed from 1 up to 96 months after initial treatment. If initial failure of the endovascular procedure was present, this was mostly attributed to glue not reaching the draining vein. Secondary Outcome: NBCA and Derivatives vs Onyx Four studies reported on the use of both NBCA and Onyx in its patients (Figure 5). Recurrence was reported in 10 of 22 patients (45%) treated with Onyx vs 8 of 35 patients (23%) treated with NBCA (OR, 2.51; 95% CI, 0.75-8.37; P = .13).
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Secondary Outcome: Complication Rates Complications were not systematically reported (Table). Five major complications (spinal cord infarction) were reported in the endovascular group, whereas no major surgical complications (severe neurological deficit) were reported.
DISCUSSION This meta-analysis clearly shows an advantage of primary surgical treatment of SDAVFs over endovascular treatment in terms of initial fistula closure and fistula recurrence. Clinical treatment outcome was not assessed because previous studies have already shown that outcome is not dependent on the treatment modality itself but rather on definitive fistula occlusion. In 2004, Steinmetz et al3 published a meta-analysis addressing the same question and reported a success rate of 46% in the endovascular treatment group. In the present study, a success percentage of 72.2% was observed, probably reflecting the advancements in endovascular techniques that have
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FIGURE 2. A through C, funnel plots of all analyses. OR, odds ratio; RR, relative risk.
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TABLE. Study Characteristics of All Included Studiesa Complications, n Article 11
Aghakhani et al Andres et al12 Blackburn et al13 Cecchi et al14 Cenzato et al15 Cho et al16 Clark et al17 Dhandapani et al18 Gemmete et al19 Gokhale et al20 Guillevin et al21 Hanel et al6 Hessler et al22 Inagawa et al23 Jellema et al24 Kaufmann et al25 Kirsch et al26 Marquardt et al7 Nagata et al27 Narvid et al28 Park et al29 Patel et al8 Rashad et al30 Ropper et al31 Ruiz-Juretschke et al32 Saladino et al2 Schuette et al33 Sherif et al34 Shinoyama et al35 Su et al36 Takai et al37 Takami et al38 Wakao et al39 Wang et al40 Yen et al41 Total a
Year
Treatment
Study Type
Subjects
Follow-up, Median (Range), mo
Minor
Major
2008 2008 2013 2009 2012 2013 2013 2013 2013 2014 2005 2010 2010 2013 2005 2011 2013 2009 2006 2008 2008 2013 2014 2012 2011 2010 2010 2007 2010 2013 2013 2006 2012 2013 2014
MS MS 1 EV EV MS MS 1 EV MS 1 EV MS 1 EV MS MS 1 EV MS 1 EV EV MS MS 1 EV MS 1 EV MS 1 EV MS 1 EV MS 1 EV MS MS MS 1 EV MS 1 EV MS MS 1 EV MS MS 1 EV MS MS MS 1 EV MS 1 EV EV MS 1 EV MS MS 1 EV MS MS 1 EV
CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS
6 4/17 17 29 55/10 5/23 8/15 22 4/29 17/10 26 6 54/102 2/12 12/24 33/1 17/61 28 13 24/39 1/17 7 9/3 10 10/9 154 12 7/19 17/3 40 23/4 5 7/14 7 1/8 609/503
6 .12 NR .48 .36 20 (5-111) 32 (6-101) 7 NR 24 (8-60) (12-98) .12 .24 (5-97) (1-120) NR 18 (1-98) .24 .12 49 (12-160) .12 (3-24) 15 36 (4-103) .24 NR .24 57 (12-145) .12 14 (1-123) .6 .24 (1-17) 6
0/. . . 0/0 NR 1/. . . 0/0 1/5 NR/NR NR 0/1 2/0 NR NR NR/NR 1/1 NR/NR NR/NR 3/0 NR NR 0/0 0/1 0/. . . NR/NR 1/. . . 1/0 6. . . 0/. . . 0/0 NR/NR NR 2/0 NR . . ./0 0/. . . 0/0
0/. . . 0/0 NR 0/. . . 0/0 0/0 0/0 NR 0/0 0/1 NR NR NR/NR 0/1 NR/NR NR/NR 0/1 NR NR 0/0 0/0 0/. . . NR/NR 0/. . . 0/1 0/0 0/. . . 0/0 NR/NR NR 0/0 NR . . ./0 0/. . . 0/2
CS, case series; EV, endovascular treatment; MS, microsurgical treatment; NR, not reported.
been made over the last decade. Surgical success rates in this series continued to be as high, as reported by Steinmetz et al. In some series, success rates of endovascular treatment were excellent, for example, the studies of Takai et al37 and Wakao et al.39 The reasons underlying the observed differences in success rates of endovascular treatment are difficult to assess. However, one might speculate that a proper preoperative workup and patient selection are very important. In the studies mentioned, upfront decisions were made as to whether patients could be appropriately treated endovascularly. In case of a difficult angioarchitecture on diagnostic DSA, no endovascular attempt was made, and the patient was immediately referred to microsurgical treatment. Other series invariably chose to treat
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the patient endovascularly and opted for microsurgical treatment only after failure of endovascular treatment. Considering that the treatment result depends mainly on definitive fistula occlusion, in our opinion, the difference between surgical occlusion and endovascular embolization is high, with a 6fold increased risk of initial failure or recurrence of the fistula in favor of surgery. It seems that the use of Onyx over the past few years has not led to better treatment results; in contrast, nonsignificant better results with NBCA embolization compared with Onyx were observed in the present analysis.10 Considering the other second end point of the analysis, complications were not reported in a significant proportion of publications, prohibiting us from making firm conclusions. This
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FIGURE 3. Initial treatment failure and recurrence rates. CI, confidence interval; M-H, Mantel-Haenszel.
might reflect a publication bias, although previously reported complication rates of both treatment modalities were generally low.3 In this perspective, we recommend that possible complications be systematically reported in future articles, also in the absence of complications. Only then is a reliable comparison between the 2 types of treatment regarding this issue possible.
Limitations A limitation of the present meta-analysis is the poor quality of the included studies, with its associated bias in several domains (all level IV studies). Thus, one might question whether the evidence needed to reliably assess the difference in recurrence rates of both treatment modalities is unequivocally present. However, because
FIGURE 4. Late recurrence after treatment. CI, confidence interval; M-H, Mantel-Haenszel.
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FIGURE 5. Comparison of Onyx and n-butyl 2-cyanoacrylate (NCBA) in fistula recurrence. CI, confidence interval; M-H, Mantel-Haenszel.
all included studies favor a microsurgical technique over endovascular treatment and the funnel plots of the meta-analyses were reasonably distributed, it is highly unlikely that the main outcome of this analysis will change. In addition, it is highly unlikely that a higher level of evidence will be available in the near future. Another limitation is that not all studies directly compared endovascular treatment and surgical treatment. As a consequence, in these studies, especially selection bias cannot be excluded because differences in baseline characteristics could not be assessed. In addition, duration of follow-up was highly heterogeneous among the included studies (Table), possibly leading to an underestimation of the long-term recurrence rates. Because of the heterogeneity of follow-up, the risk of recurrence in relation to time after treatment also could not be reliably assessed. Considering the present results, the question arises whether patients should still be treated primarily by endovascular techniques, given the fact that functional outcome after treatment is highly dependent on the patient’s preoperative neurological status. In this analysis, some studies reported on late recurrences (.24 months after treatment) after embolization that were detected only after the clinical deterioration of the patient. This is a very important observation because patients in general regain only half of their lost neurological functions after treatment of the SDAVF.1 It is clear that endovascular techniques have improved over the last years. However, surgery has also improved with regard to minimal invasiveness of the procedure, leading to the equivalent excellent results and a quick discharge of the patient. The benefits of endovascular techniques over surgical fistula treatment regarding these factors are probably not so obvious anymore. In the past, surgery has been associated with large incisions and difficulties in finding the right level of the fistula. Today, advancements in surgical techniques allow a small incision with a tailored exposure of the fistula. Even a tubular technique has been reported, after which patients were mostly discharged home the next day.8 Therefore, endovascular techniques still have a place in the treatment of SDAVFs. Exact localization of the fistula is of utmost importance in establishing a proper minimally invasive surgical result. With the advancements in magnetic resonance angiography techniques,13,42 the fistula can already be visualized noninvasively, after which
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a DSA can be performed for definite localization of the fistula. In this respect, a selective preoperative endovascular workup may serve as an excellent adjunct.43 It has already been shown that this multimodality treatment approach is associated with high success rates in terms of minimally invasive surgery.7
CONCLUSION Although hampered by the poor quality of the included studies, this meta-analysis clearly shows an advantage of primary surgical treatment of SDAVFs over endovascular treatment in terms of initial treatment success and fistula recurrence. The often-used argument that endovascular techniques have improved over the last years and therefore outweigh surgery is not supported by this meta-analysis. Disclosure The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.
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32. Ruiz-Juretschke F, Perez-Calvo JM, Castro E, et al. A single-center, long-term study of spinal dural arteriovenous fistulas with multidisciplinary treatment. J Clin Neurosci. 2011;18(12):1662-1666. 33. Schuette AJ, Cawley CM, Barrow DL. Indocyanine green videoangiography in the management of dural arteriovenous fistulae. Neurosurgery. 2010;67(3):658-662; discussion 662. 34. Sherif C, Gruber A, Bavinzski G, et al. Long-term outcome of a multidisciplinary concept of spinal dural arteriovenous fistulae treatment. Neuroradiology. 2008;50 (1):67-74. 35. Shinoyama M, Endo T, Takahash T, et al. Long-term outcome of cervical and thoracolumbar dural arteriovenous fistulas with emphasis on sensory disturbance and neuropathic pain. World Neurosurg. 2010;73(4):401-408. 36. Su IC, terBrugge KG, Willinsky RA, Krings T. Factors determining the success of endovascular treatments among patients with spinal dural arteriovenous fistulas. Neuroradiology. 2013;55(11):1389-1395. 37. Takai K, Kin T, Oyama H, Shojima M, Saito N. Three-dimensional angioarchitecture of spinal dural arteriovenous fistulas, with special reference to the intradural retrograde venous drainage system. J Neurosurg Spine. 2013;18(4): 398-408. 38. Takami T, Ohata K, Nishio A, Hara M. Histological characteristics of arterialized medullary vein in spinal dural arteriovenous fistulas related with clinical findings: report of five cases. Neurol India. 2006;54(2):202-204. 39. Wakao N, Imagama S, Ito Z, et al. Clinical outcome of treatments for spinal dural arteriovenous fistulas: results of multivariate analysis and review of the literature. Spine (Phila Pa 1976). 2012;37(6):482-488. 40. Wang G, Ma G, Ma J, et al. Surgical treatment of spinal vascular malformations performed using intraoperative indocyanine green videoangiography. J Clin Neurosci. 2013;20(6):831-836. 41. Yen PP, Ritchie KC, Shankar JJ. Spinal dural arteriovenous fistula: correlation between radiological and clinical findings. J Neurosurg Spine. 2014;21; 837-842. 42. Lindenholz A, TerBrugge KG, van Dijk JM, Farb RI. The accuracy and utility of contrast-enhanced MR angiography for localization of spinal dural arteriovenous fistulas: the Toronto experience. Eur Radiol. 2014;24(11):2885-2894. 43. Acerbi F, Ferroli P. Surgery versus embolization in spinal dural arteriovenous fistulas: the ideal competition to improve the care of patients. World Neurosurg. 2013;80(6):e191-e193.
COMMENT
T
he authors provide an analysis of the recurrence rates of spinal dural arteriovenous fistulas (AVFs) after surgical and endovascular treatment reported since 2004. They found occlusion rates of 96.6% and 72.2% for surgically and endovascularly treated fistulas, respectively. For those fistulas treated endovascularly, they found n-butyl 2-cyanoacrylate to be more effective than Onyx. The current analysis provides a comprehensive review of the literature reporting surgical and endovascular treatment of spinal dural AVFs. As with any meta-analysis, the quality of the study is subject to that of the data evaluated. In this case, the available literature consisted only of retrospective case reviews. Furthermore, the authors encountered inconsistent follow-up and reporting of complications. However, they succeed in answering the question they set out to ask, namely, the recurrence rates of spinal dural AVFs after surgical and endovascular treatment. With continued development of endovascular technologies, improvement in the recurrence rates of endovascularly treated spinal AVFs should improve. Stephan A. Munich Elad I. Levy Buffalo, New York
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Recurrence Rates After Surgical or Endovascular Treatment of Spinal Dural Arteriovenous Fistulas: A Meta-analysis Nicolaas A. Bakker, MD, PhD* Maarten Uyttenboogaart, MD, PhD‡§ G.J. Luijckx, MD, PhD§ Omid S. Eshghi, MD‡ Aryan Mazuri, MD‡ Jan D.M. Metzemaekers, MD, PhD* Rob J.M. Groen, MD, PhD* J. Marc C. Van Dijk, MD, PhD* From the Departments of *Neurosurgery, ‡Radiology, and §Neurology, University of Groningen, University Medical Center Groningen, Groningen, the Netherlands Correspondence: Nicolaas A. Bakker, MD, PhD, Department of Neurosurgery, University Medical Center Groningen, PO Box 30.001, 9700 RB Groningen, Netherlands. E-mail: [email protected] Received, December 1, 2014. Accepted, February 3, 2015. Published Online, March 18, 2015. Copyright © 2015 by the Congress of Neurological Surgeons.
BACKGROUND: There is an increasing tendency to treat spinal dural arteriovenous fistulas (SDAVFs) endovascularly despite the lack of clear evidence favoring embolization over surgery. OBJECTIVE: To compare the initial failure and recurrence rates of primary treatment of SDAVFs by surgery and endovascular techniques. METHODS: A meta-analysis using the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) standard was performed. All the English literature from 2004 onward was evaluated. From each article that compared the 2 treatment modalities, the odds ratio (OR) was calculated. Combined ORs were calculated with Review Manager 5.3 of The Cochrane Collaboration. RESULTS: A total of 35 studies harboring 1112 patients were assessed. Initial definitive fistula occlusion was observed in 588 of 609 surgical patients (96.6%; 95% confidence interval [CI], 94.8-97.8) vs 363 of 503 endovascularly treated patients (72.2%; 95% CI, 68.1-75.9; P , .001). The combined OR from 18 studies that assessed both treatment modalities (730 patients) was 6.15 (95% CI, 3.45-11.0) in favor of surgical treatment. Late recurrence (13 studies, 480 patients) revealed an OR of 3.15 (95% CI, 1.66-5.96; P , .001) in favor of surgery. In a subgroup, recurrence was reported in 10 of 22 patients (45%) treated with Onyx vs 8 of 35 (23%) treated with n-butyle-2-cyanoacrylate (OR, 2.51; 95% CI, 0.75-8.37; P = .13). CONCLUSION: Although hampered by inclusion of poor quality studies, this metaanalysis shows a definite advantage of primary surgical treatment of SDAVF over endovascular treatment in initial failure rate and late recurrences. The often-used argument that endovascular techniques have improved and therefore outweigh surgery is not supported by this meta-analysis. KEY WORDS: Endovascular techniques, Meta-analysis, Spinal DAVF Neurosurgery 77:137–144, 2015
DOI: 10.1227/NEU.0000000000000727
S
pinal dural arteriovenous fistulas (SDAVFs), also known as type I spinal arteriovenous malformations, are the most common spinal vascular disorder. Diagnosis of an SDAVF is often challenging because of its heterogeneous presentation that can mimic other neurological disorders. A typical SDAVF is fed by a radicular
ABBREVIATIONS: CI, confidence interval; DSA, digital subtraction angiography; MeSH, Medical Subject Headings; NBCA, n-butyl 2-cyanoacrylate; OR, odds ratio; PRISMA, Preferred Reporting Items for Systematic Reviews and Meta-Analyses; SDAVF, spinal dural arteriovenous fistula
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artery and drains into a medullary vein, leading to a dilated perimedullary venous plexus and spinal cord congestion. The classic clinical picture is that of a progressive thoracic myelopathy. Surgical treatment, in which the fistula is disconnected intradurally, is associated with complete cure in the vast majority of patients.1,2 The procedure is straightforward, and complication rates are low.2 However, sometimes multilevel laminectomies are performed if the SDAVF is difficult to locate. In addition, because the dura mater has to be opened during the procedure, postoperative cerebrospinal fluid leakage can be observed after surgery. These complications may lead to a longer hospital stay. Therefore, as an alternative
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method, endovascular treatment has gained interest over the last decades.1 It is minimally invasive, and the treatment of the fistula can often be performed in combination with the diagnostic procedure. In 2004, Steinmetz et al3 reported in a meta-analysis that definitive cure rates are much lower after endovascular treatment compared with microsurgical treatment. In practice, it is observed that reaching the draining intradural vein via the endovascular route can be difficult. Over the last years, endovascular techniques and materials have generally improved. In additional, new liquid embolic agents such as Onyx, showing good results in the transarterial embolization of cranial DAVFs,4 have become available. On the other hand, surgical techniques have also improved, with better preoperative fistula localization5-7 and the application of novel minimally invasive techniques.8 In view of these recent developments, it was our aim to perform an updated meta-analysis of the literature over the past 10 years to compare the results of primary endovascular treatment with microsurgical treatment of SDAVFs.
METHODS Literature Search Three electronic databases were searched: MEDLINE (PubMed), CENTRAL (Cochrane Central Register of Controlled Trials), and EMBASE. Only the English literature was considered. Databases were scrutinized for studies published from January 2004 to September 2013. MeSH (Medical Subject Headings) terms were the following: SDAVF (all fields) or spinal dural arteriovenous (all fields) or spinal AVM and treatment (all fields). In addition, reference lists of all selected studies were scrutinized for additional studies. Studies assessing $5 patients were considered eligible. Reviews and studies included in the meta-analysis of Steinmetz et al3 from 2004 were excluded. Two reviewers (N.A.B. and J. M.C.V.D.) independently screened titles and abstracts of all retrieved articles. We obtained full-text reports of studies that were likely to report treatment outcome of SDAVFs. Studies that did not compare the 2 treatment modalities in a way to obtain 2 · 2 tables but reported outcomes of a single treatment modality (ie, surgery or endovascular treatment) were also included. In the case of multiple publications on the same data set, we used only the most recent publication to obtain unique cases. In case of disagreement between the 2 reviewers, consensus was reached by discussion. Figure 1 shows the flow chart according to the PRISMA (Preferred Reporting Items for Systematic Reviews and MetaAnalyses) statement.9 The 2 observers independently assessed the included articles.
Data Extraction All data were extracted with the use of a case-based format; patients in whom several treatments were performed were regarded as 1 single case; only the first intended treatment was registered. From all included studies, the following data were extracted and reported with the use of a predefined data extraction form (if available): (1) number of patients with an SDAVF; (2) type of treatment (surgical vs endovascular; patients initially treated with polyvinyl ethanol and surgery thereafter were regarded surgical patients); (3) rate of treatment failure, initial and late recurrence; (4) type of compound used for endovascular treatment (n-butyl 2-cyanoacrylate [NBCA] vs Onyx [Covidien, Mansfield, Massachusetts]); (5) location of fistula (craniocervical
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DAVFs were excluded); (6) time of follow-up; (7) complications related to the procedure other than recurrence of the fistula (minor [eg, wound infection, cerebrospinal fluid fistula requiring treatment] or major [leading to permanent neurological deficits]); and (8) type of study (randomized controlled trial, observational cohort, etc). No individual patient data could be derived from the majority of included studies.
Outcome Measures and Statistics Primary outcome was the failure of initial treatment or recurrence of the fistula. The latter was also assessed in a separate analysis in which late recurrence was defined as symptomatic reopening of the fistula .1 month after treatment. Initial success of treatment of the SDAVF had to be confirmed during control digital subtraction angiography (DSA) after surgery or directly after endovascular treatment. Recurrence of the fistula during follow-up was recorded either during routine follow-up imaging with magnetic resonance angiography or DSA or during clinical followup and subsequent imaging in case of clinical deterioration. In addition, the type of compound used (NBCA and derivatives vs Onyx) and its possible association with recurrence rates, as well as the number of complications from each treatment modality, were also taken into account as a secondary outcome measure. Assessment of risk of bias of the included studies was performed according to the Cochrane handbook for systematic reviews of interventions.10 Because substantial bias was potentially present in all of the included studies, funnels plots were used to estimate publication bias for all analyses (Figure 2A-2C). Continuous variables were expressed as mean with standard deviation or median and range, and categorical variables were expressed as counts and percentages with the use of SPSS software (version 20.0). Ninety-five percent confidence intervals (CIs) of the proportion were calculated by use of the Wilson procedure without continuity correction. From each article in which it was possible to compare the 2 treatment modalities (n = 18), the odds ratio (OR) was calculated from a 2 · 2 table. These were the studies included in the meta-analyses. Combined ORs and 95% CIs were calculated with RevMan (Review Manager, version 5.3. Copenhagen; The Nordic Cochrane Centre, The Cochrane Collaboration, 2014). Study heterogeneity was assessed with the I2 statistics for inconsistency. A value of .50% was considered substantial heterogeneity. In the case of statistical homogeneity, we used a fixed-effect model.
RESULTS Primary Outcome: Initial Failure or Late Recurrence Rate of SDAVFs A total of 35 studies harboring 1112 patients were included for the pooled data analysis (Table). From all surgical patients, initial treatment failure or recurrence was reported in 21 if 609 patients, leading to a successful treatment percentage of 96.6% (95% CI, 94.8-97.8). In the endovascularly treated patients, initial failure or recurrence was reported in 140 of 503 patients; thus, the successful treatment percentage was 72.2% (95% CI, 68.1-75.1; P , .001). Overall study quality was poor; only retrospective case series were available. Twenty studies directly compared endovascular and surgical treatment; 15 studies reported 1 treatment technique only (12 microsurgical and 3 endovascular). Follow-up was highly heterogeneous (Table).
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FIGURE 1. Flowchart according to the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) statement.
From all studies (n = 18730 patients) included in the metaanalysis (Figure 3), the OR was obtained, leading to a combined OR of 6.15 (95% CI, 3.45-11.0) in favor of surgical treatment. In 13 studies (480 patients; Figure 4), it was possible to extract data on the time of treatment failure (either direct or late). In terms of the risk of late recurrence, an OR of 3.15 (95% CI, 1.665.96; P , .001) in favor of surgical treatment was observed. Recurrences were observed from 1 up to 96 months after initial treatment. If initial failure of the endovascular procedure was present, this was mostly attributed to glue not reaching the draining vein. Secondary Outcome: NBCA and Derivatives vs Onyx Four studies reported on the use of both NBCA and Onyx in its patients (Figure 5). Recurrence was reported in 10 of 22 patients (45%) treated with Onyx vs 8 of 35 patients (23%) treated with NBCA (OR, 2.51; 95% CI, 0.75-8.37; P = .13).
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Secondary Outcome: Complication Rates Complications were not systematically reported (Table). Five major complications (spinal cord infarction) were reported in the endovascular group, whereas no major surgical complications (severe neurological deficit) were reported.
DISCUSSION This meta-analysis clearly shows an advantage of primary surgical treatment of SDAVFs over endovascular treatment in terms of initial fistula closure and fistula recurrence. Clinical treatment outcome was not assessed because previous studies have already shown that outcome is not dependent on the treatment modality itself but rather on definitive fistula occlusion. In 2004, Steinmetz et al3 published a meta-analysis addressing the same question and reported a success rate of 46% in the endovascular treatment group. In the present study, a success percentage of 72.2% was observed, probably reflecting the advancements in endovascular techniques that have
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FIGURE 2. A through C, funnel plots of all analyses. OR, odds ratio; RR, relative risk.
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TABLE. Study Characteristics of All Included Studiesa Complications, n Article 11
Aghakhani et al Andres et al12 Blackburn et al13 Cecchi et al14 Cenzato et al15 Cho et al16 Clark et al17 Dhandapani et al18 Gemmete et al19 Gokhale et al20 Guillevin et al21 Hanel et al6 Hessler et al22 Inagawa et al23 Jellema et al24 Kaufmann et al25 Kirsch et al26 Marquardt et al7 Nagata et al27 Narvid et al28 Park et al29 Patel et al8 Rashad et al30 Ropper et al31 Ruiz-Juretschke et al32 Saladino et al2 Schuette et al33 Sherif et al34 Shinoyama et al35 Su et al36 Takai et al37 Takami et al38 Wakao et al39 Wang et al40 Yen et al41 Total a
Year
Treatment
Study Type
Subjects
Follow-up, Median (Range), mo
Minor
Major
2008 2008 2013 2009 2012 2013 2013 2013 2013 2014 2005 2010 2010 2013 2005 2011 2013 2009 2006 2008 2008 2013 2014 2012 2011 2010 2010 2007 2010 2013 2013 2006 2012 2013 2014
MS MS 1 EV EV MS MS 1 EV MS 1 EV MS 1 EV MS MS 1 EV MS 1 EV EV MS MS 1 EV MS 1 EV MS 1 EV MS 1 EV MS 1 EV MS MS MS 1 EV MS 1 EV MS MS 1 EV MS MS 1 EV MS MS MS 1 EV MS 1 EV EV MS 1 EV MS MS 1 EV MS MS 1 EV
CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS CS
6 4/17 17 29 55/10 5/23 8/15 22 4/29 17/10 26 6 54/102 2/12 12/24 33/1 17/61 28 13 24/39 1/17 7 9/3 10 10/9 154 12 7/19 17/3 40 23/4 5 7/14 7 1/8 609/503
6 .12 NR .48 .36 20 (5-111) 32 (6-101) 7 NR 24 (8-60) (12-98) .12 .24 (5-97) (1-120) NR 18 (1-98) .24 .12 49 (12-160) .12 (3-24) 15 36 (4-103) .24 NR .24 57 (12-145) .12 14 (1-123) .6 .24 (1-17) 6
0/. . . 0/0 NR 1/. . . 0/0 1/5 NR/NR NR 0/1 2/0 NR NR NR/NR 1/1 NR/NR NR/NR 3/0 NR NR 0/0 0/1 0/. . . NR/NR 1/. . . 1/0 6. . . 0/. . . 0/0 NR/NR NR 2/0 NR . . ./0 0/. . . 0/0
0/. . . 0/0 NR 0/. . . 0/0 0/0 0/0 NR 0/0 0/1 NR NR NR/NR 0/1 NR/NR NR/NR 0/1 NR NR 0/0 0/0 0/. . . NR/NR 0/. . . 0/1 0/0 0/. . . 0/0 NR/NR NR 0/0 NR . . ./0 0/. . . 0/2
CS, case series; EV, endovascular treatment; MS, microsurgical treatment; NR, not reported.
been made over the last decade. Surgical success rates in this series continued to be as high, as reported by Steinmetz et al. In some series, success rates of endovascular treatment were excellent, for example, the studies of Takai et al37 and Wakao et al.39 The reasons underlying the observed differences in success rates of endovascular treatment are difficult to assess. However, one might speculate that a proper preoperative workup and patient selection are very important. In the studies mentioned, upfront decisions were made as to whether patients could be appropriately treated endovascularly. In case of a difficult angioarchitecture on diagnostic DSA, no endovascular attempt was made, and the patient was immediately referred to microsurgical treatment. Other series invariably chose to treat
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the patient endovascularly and opted for microsurgical treatment only after failure of endovascular treatment. Considering that the treatment result depends mainly on definitive fistula occlusion, in our opinion, the difference between surgical occlusion and endovascular embolization is high, with a 6fold increased risk of initial failure or recurrence of the fistula in favor of surgery. It seems that the use of Onyx over the past few years has not led to better treatment results; in contrast, nonsignificant better results with NBCA embolization compared with Onyx were observed in the present analysis.10 Considering the other second end point of the analysis, complications were not reported in a significant proportion of publications, prohibiting us from making firm conclusions. This
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FIGURE 3. Initial treatment failure and recurrence rates. CI, confidence interval; M-H, Mantel-Haenszel.
might reflect a publication bias, although previously reported complication rates of both treatment modalities were generally low.3 In this perspective, we recommend that possible complications be systematically reported in future articles, also in the absence of complications. Only then is a reliable comparison between the 2 types of treatment regarding this issue possible.
Limitations A limitation of the present meta-analysis is the poor quality of the included studies, with its associated bias in several domains (all level IV studies). Thus, one might question whether the evidence needed to reliably assess the difference in recurrence rates of both treatment modalities is unequivocally present. However, because
FIGURE 4. Late recurrence after treatment. CI, confidence interval; M-H, Mantel-Haenszel.
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FIGURE 5. Comparison of Onyx and n-butyl 2-cyanoacrylate (NCBA) in fistula recurrence. CI, confidence interval; M-H, Mantel-Haenszel.
all included studies favor a microsurgical technique over endovascular treatment and the funnel plots of the meta-analyses were reasonably distributed, it is highly unlikely that the main outcome of this analysis will change. In addition, it is highly unlikely that a higher level of evidence will be available in the near future. Another limitation is that not all studies directly compared endovascular treatment and surgical treatment. As a consequence, in these studies, especially selection bias cannot be excluded because differences in baseline characteristics could not be assessed. In addition, duration of follow-up was highly heterogeneous among the included studies (Table), possibly leading to an underestimation of the long-term recurrence rates. Because of the heterogeneity of follow-up, the risk of recurrence in relation to time after treatment also could not be reliably assessed. Considering the present results, the question arises whether patients should still be treated primarily by endovascular techniques, given the fact that functional outcome after treatment is highly dependent on the patient’s preoperative neurological status. In this analysis, some studies reported on late recurrences (.24 months after treatment) after embolization that were detected only after the clinical deterioration of the patient. This is a very important observation because patients in general regain only half of their lost neurological functions after treatment of the SDAVF.1 It is clear that endovascular techniques have improved over the last years. However, surgery has also improved with regard to minimal invasiveness of the procedure, leading to the equivalent excellent results and a quick discharge of the patient. The benefits of endovascular techniques over surgical fistula treatment regarding these factors are probably not so obvious anymore. In the past, surgery has been associated with large incisions and difficulties in finding the right level of the fistula. Today, advancements in surgical techniques allow a small incision with a tailored exposure of the fistula. Even a tubular technique has been reported, after which patients were mostly discharged home the next day.8 Therefore, endovascular techniques still have a place in the treatment of SDAVFs. Exact localization of the fistula is of utmost importance in establishing a proper minimally invasive surgical result. With the advancements in magnetic resonance angiography techniques,13,42 the fistula can already be visualized noninvasively, after which
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a DSA can be performed for definite localization of the fistula. In this respect, a selective preoperative endovascular workup may serve as an excellent adjunct.43 It has already been shown that this multimodality treatment approach is associated with high success rates in terms of minimally invasive surgery.7
CONCLUSION Although hampered by the poor quality of the included studies, this meta-analysis clearly shows an advantage of primary surgical treatment of SDAVFs over endovascular treatment in terms of initial treatment success and fistula recurrence. The often-used argument that endovascular techniques have improved over the last years and therefore outweigh surgery is not supported by this meta-analysis. Disclosure The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.
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32. Ruiz-Juretschke F, Perez-Calvo JM, Castro E, et al. A single-center, long-term study of spinal dural arteriovenous fistulas with multidisciplinary treatment. J Clin Neurosci. 2011;18(12):1662-1666. 33. Schuette AJ, Cawley CM, Barrow DL. Indocyanine green videoangiography in the management of dural arteriovenous fistulae. Neurosurgery. 2010;67(3):658-662; discussion 662. 34. Sherif C, Gruber A, Bavinzski G, et al. Long-term outcome of a multidisciplinary concept of spinal dural arteriovenous fistulae treatment. Neuroradiology. 2008;50 (1):67-74. 35. Shinoyama M, Endo T, Takahash T, et al. Long-term outcome of cervical and thoracolumbar dural arteriovenous fistulas with emphasis on sensory disturbance and neuropathic pain. World Neurosurg. 2010;73(4):401-408. 36. Su IC, terBrugge KG, Willinsky RA, Krings T. Factors determining the success of endovascular treatments among patients with spinal dural arteriovenous fistulas. Neuroradiology. 2013;55(11):1389-1395. 37. Takai K, Kin T, Oyama H, Shojima M, Saito N. Three-dimensional angioarchitecture of spinal dural arteriovenous fistulas, with special reference to the intradural retrograde venous drainage system. J Neurosurg Spine. 2013;18(4): 398-408. 38. Takami T, Ohata K, Nishio A, Hara M. Histological characteristics of arterialized medullary vein in spinal dural arteriovenous fistulas related with clinical findings: report of five cases. Neurol India. 2006;54(2):202-204. 39. Wakao N, Imagama S, Ito Z, et al. Clinical outcome of treatments for spinal dural arteriovenous fistulas: results of multivariate analysis and review of the literature. Spine (Phila Pa 1976). 2012;37(6):482-488. 40. Wang G, Ma G, Ma J, et al. Surgical treatment of spinal vascular malformations performed using intraoperative indocyanine green videoangiography. J Clin Neurosci. 2013;20(6):831-836. 41. Yen PP, Ritchie KC, Shankar JJ. Spinal dural arteriovenous fistula: correlation between radiological and clinical findings. J Neurosurg Spine. 2014;21; 837-842. 42. Lindenholz A, TerBrugge KG, van Dijk JM, Farb RI. The accuracy and utility of contrast-enhanced MR angiography for localization of spinal dural arteriovenous fistulas: the Toronto experience. Eur Radiol. 2014;24(11):2885-2894. 43. Acerbi F, Ferroli P. Surgery versus embolization in spinal dural arteriovenous fistulas: the ideal competition to improve the care of patients. World Neurosurg. 2013;80(6):e191-e193.
COMMENT
T
he authors provide an analysis of the recurrence rates of spinal dural arteriovenous fistulas (AVFs) after surgical and endovascular treatment reported since 2004. They found occlusion rates of 96.6% and 72.2% for surgically and endovascularly treated fistulas, respectively. For those fistulas treated endovascularly, they found n-butyl 2-cyanoacrylate to be more effective than Onyx. The current analysis provides a comprehensive review of the literature reporting surgical and endovascular treatment of spinal dural AVFs. As with any meta-analysis, the quality of the study is subject to that of the data evaluated. In this case, the available literature consisted only of retrospective case reviews. Furthermore, the authors encountered inconsistent follow-up and reporting of complications. However, they succeed in answering the question they set out to ask, namely, the recurrence rates of spinal dural AVFs after surgical and endovascular treatment. With continued development of endovascular technologies, improvement in the recurrence rates of endovascularly treated spinal AVFs should improve. Stephan A. Munich Elad I. Levy Buffalo, New York
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