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Neurosurgery
Review
Outcomes following surgical versus endovascular treatment of spinal dural arteriovenous fistula: a systematic review and meta-analysis
  1. Anshit Goyal1,
  2. Joseph Cesare1,
  3. Victor M Lu1,
  4. Mohammed Ali Alvi1,
  5. Panagiotis Kerezoudis1,
  6. Waleed Brinjikji2,
  7. Deena Nasr3,
  8. Guiseppe Lanzino1,
  9. Mohamad Bydon1
  1. 1 Neurosurgery, Mayo Clinic, Rochester, Minnesota, USA
  2. 2 Radiology, Mayo Clinic, Rochester, Minnesota, USA
  3. 3 Neurology, Mayo Clinic, Rochester, Minnesota, USA
  1. Correspondence to Dr Mohamad Bydon, Neurosurgery, Mayo Clinic, Rochester, MN 55905, USA; bydon.mohamad{at}mayo.edu

Abstract

Although surgical resection is associated with a complete cure in most cases of spinal dural arteriovenous fistulas (SDAVF), there has been an increasing trend towards embolisation. We performed a systematic review and meta-analysis comparing surgical resection with endovascular treatment in terms of success of treatment, rate of recurrence and complications. A literature search was conducted using Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines. Strength of evidence was assessed using the Grading of Recommendations Assessment, Development and Evaluation Working Group system. Surgical outcomes such as initial treatment failure, late recurrence, neurological improvement and complications were compared between the two approaches. We included 57 studies with 2029 patients, of which 32 studies with 1341 patients directly compared surgery (n=590) and embolisation (n=751). Surgery was found to be associated with significantly lower odds of initial treatment failure (OR: 0.15, 95% CI 0.09 to 0.24, I2 0%, p<0.001) and late recurrence (OR 0.18, 95% CI 0.09 to 0.39, I2 0%, p<0.001). The odds of neurological improvement following surgery were also significantly higher compared with embolisation alone (OR: 2.73, CI:1.67 to 4.48, I2 :49.5%, p<0.001). No difference in complication rates was observed between the two approaches (OR 1.78, 95% CI 0.97 to 3.26, I2 0%, p=0.063). Onyx was associated with significantly higher odds of initial failure/late recurrence as compared with n-butyl 2-cyanoacrylate (OR: 3.87, CI: 1.73 to 8.68, I2 :0%, p<0.001). Surgery may be associated with superior outcomes for SDAVFs in comparison to endovascular occlusion. Newer embolisation agents like Onyx have not conferred a significant improvement in occlusion rate.

  • spinal dural arteriovenous fistulas
  • SDAVF
  • arteriovenous malformations
  • endovascular
  • embolisation
  • surgery
  • treatment failure
  • recurrence
  • complications
  • systematic review
  • meta-analysis

https://doi.org/10.1136/jnnp-2019-320648

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    Introduction

    Spinal dural arteriovenous fistulas (SDAVFs), also known as type one spinal arteriovenous malformations (AVMs), are the most common vascular disorders of the spinal cord and constitute approximately 70% of all spinal AVMs.1–3 They are primarily located around the area of the intervertebral foramen and are fed by a branch of the segmental radicular artery that supplies the dura at every level while venous drainage is provided by the corresponding radicular vein.4 Increased pressure transmitted from the radicular artery to the draining vein causes stagnation of the venous outflow and consequent spinal cord congestion with progressive thoracic myelopathy being the predominant clinical manifestation, also known as Foix-Alajouanine Syndrome.5 Surgical treatment, which involves intradural ligation of the draining vein through a laminectomy, is associated with complete cure in the vast majority of cases.4 6 However, given the invasive nature of surgery, embolisation has increasingly gained popularity and become the first line of treatment in many cases.6 7 Previous meta-analyses by Steinmetz et al in 20048 and Bakker et al in 20136 have indicated that recurrence rates are higher with endovascular approaches. However, since 2013, several new case series have been published that have further highlighted and compared the clinical outcomes of each approach. Advances have also been made both in endovascular technology and preoperative localisation of the fistula.6 7 In addition, while previous studies have compared recurrence rates, the neurological outcomes associated with each modality have not been compared. To address this gap in knowledge, we aimed to perform an updated systematic review and meta-analysis of all available literature to elucidate the difference in clinical outcomes, such as failure rates and neurological outcomes, between the two types of treatment.

    Materials and methods

    Literature search strategy

    This systematic review was conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines.9 The literature search strategy was designed around the Patient/Population/Problem, Intervention, Comparison, Outcome (PICO) format—Is there a difference in recurrence rates and neurological outcomes (outcome) between endovascular treatment (intervention) and surgery (comparator) among patients with SDAVFs (population of interest). Electronic searches were performed using Ovid Medline/PubMed, Ovid Embase, Ovid Scopus and Cochrane Central Register of Controlled Trials, Cochrane Database of Systematic Reviews, from their dates of inception to June 2018 by a master’s level librarian with extensive meta-analytical experience. Reference lists of all articles were also screened for additional studies. The actual search strategy is available as online supplemental content 1. The PRISMA search strategy is presented in figure 1.

    Supplemental material

    Figure 1
    Figure 1

    Preferred Reporting Items for Systematic Reviews and Meta-Analyses search strategy. DAVF, dural arteriovenous fistula.

    Selection criteria

    Studies were eligible for this systematic review if they fulfilled the following eligibility criteria: (1) randomised controlled trials or observational studies reporting outcomes for surgical and/or endovascular treatment of SDAVFs; (2) studies reporting the following outcomes: initial failure, late recurrence or neurological improvement and (3) only English articles were considered. In this systematic review, we excluded studies included in the meta-analysis by Steinmetz et al in 2004.8 For multiple publications from the same institution/data, only the most recent reports were included. Cadaveric studies, abstracts, commentaries and editorials were excluded. Studies with <5 patients in both treatment arms were also excluded. All studies were screened by two independent reviewers (AG and JC) and any discrepancy was resolved by discussion.

    Data extraction

    The following data were extracted: year of study, study design, patient demographics (age, sex), duration of follow-up, type of treatment performed (surgery/endovascular), type of endovascular treatment (n-butyl 2-cyanoacrylate (NBCA)/Onyx (Covidien, Mansfield, Massachusetts), location of fistula. The outcomes of interest included (1) Initial failure, (2) late recurrence, (3) neurological improvement as measured by either Aminoff and Logue Scale (ALS) or Modified McCormick Scale and (4) complications. Data extraction from articles, tables and figures was performed by one reviewer (JC) with accuracy of data entry confirmed by a second reviewer (AG). In all studies, patients who received sequential embolisation and surgery as part of an intended preoperative multidisciplinary approach were excluded from analysis of initial failure and late recurrence. Patients receiving both endovascular and surgical treatment were excluded during analysis for odds of neurological improvement.

    Assessment of risk of bias and quality of evidence

    Each article in our meta-analysis was assessed using the Meta-analysis of Observational Studies (MOOSE) in epidemiology criteria.10 Last, confidence in effect estimates was assessed using the Grading of Recommendations Assessment, Development and Evaluation (GRADE) evidence profiling.11 Differences in quality assessment were resolved by consensus. Funnel plots were used to estimate publication bias in all analyses (online supplemental content 2, figures 1–3).

    Supplemental material

    Figure 2
    Figure 2

    Forest plots comparing rates of (A) initial failure and (B) late recurrence between surgical and endovascular treatment.

    Figure 3
    Figure 3

    Forest plot Comparing rates of (A) neurological improvement and (B) complications between surgical and endovascular treatment.

    Statistical analysis

    OR for binary outcomes was calculated to pool effect estimates. The I2 statistic was used to determine the percentage of total variation across studies secondary to heterogeneity rather than chance, with values greater than 50% representing substantial heterogeneity.12SD of change scores was calculated using the correlation coefficient methodology per the suggestion of Cochrane Review Handbook. In cases of zero events for binary outcomes in one or both treatment arms, a continuity correction of 0.1 was applied. Fixed-effects model was used when I2 <50%. All p values were two-sided. Level of statistical significance was established at <0.05. Publication bias was assessed through evaluation of asymmetry on funnel plots. Sensitivity analyses were performed by omission of each study and reevaluation of the overall trend direction. All statistical analyses were performed using STATA V.14.1 (StataCorp).

    Results

    Literature search and study characteristics

    Our search strategy identified a total of 1279 studies. After removal of duplicates, a total of 884 papers remained. Following screening of titles and abstract, 93 studies were selected for full text evaluation. Following full text evaluation, 57 articles (n=2029) were selected for qualitative and quantitative synthesis of which 32 (n=1341) directly compared surgery and endovascular treatment (surgery: n=590, endovascular: n=751). All studies were observational and median follow-up time ranged from 3 to 84 months (table 1).

    View this table:
    Table 1

    Study characteristics of included studies

    Primary outcomes

    Initial treatment failure and late recurrence

    From 32 studies (n=1341 patients) directly comparing surgery and endovascular approach, it was found that surgical ligation was associated with significantly lower odds of initial treatment failure (OR 0.15, 95% CI 0.09 to 0.24, I2 0%, p<0.001). Comparison of late recurrence from 22 studies (n=948 patients) also showed that surgery was also associated with significantly lower odds of delayed recanalisation or recurrence of the fistula (OR 0.18, 95% CI 0.09 to 0.39, I2 0%, p<0.001) (figure 2A and B).

    Neurological outcomes

    A total of 13 studies with 415 patients reported individual patient level neurological outcomes using the ALS or modified Rankin Scale. We compared odds of improvement in neurological function (yes/no) for patients receiving either endovascular treatment alone or surgery alone. Patients treated with both endovascular and surgical ligation were not included in this comparison. Surgery was associated with higher odds of neurological improvement compared with endovascular embolisation alone (OR 2.73, 95% CI 1.67 to 4.48, I2 49.5%, p<0.001) (figure 3A).

    Secondary outcomes

    Complications

    Comparison of overall complication rates from 22 studies (n=791 patients) showed a non-significant trend towards higher complication rates with surgery as compared with endovascular embolisation alone (OR 1.78, 95% CI 0.97 to 3.26, I20%, p=0.063) (figure 3B). Table 1 enlists the overall complications for the two treatment modalities reported in each study.

    Onyx versus NBCA

    A total of nine studies (n=133 patients) reported using both Onyx and NBCA in the endovascular cohort. Initial failure and late recurrence were compared across the two embolisation agents as a composite outcome. Onyx use was associated with significantly higher odds of treatment failure/late recurrence as compared with NBCA (OR 3.87, CI; 1.73 to 8.68, I20%, p<0.001) (figure 4).

    Figure 4
    Figure 4

    Forest plot comparing treatment failure rate between Onyx and n-butyl 2-cyanoacrylate (NBCA) following embolisation.

    Critical appraisal

    Study quality assessment

    Study quality was assessed using the MOOSE criteria (online supplemental content 3). There was no obvious heterogeneous bias risk implicated among all studies, with the majority lacking clarification if independent outcomes assessment was performed or not.

    Supplemental material

    Strength of evidence

    Based on the GRADE working group guidelines for strength of evidence, it was determined that the quality of outcomes ranged from very low to low. The GRADE summary of findings are detailed in table 2.

    View this table:
    Table 2

    GRADE summary of findings table

    Discussion

    The present meta-analysis showed a significantly superior outcomes profile with surgical ligation of SDAVFs compared with embolisation alone. Endovascular treatment alone was associated with significantly higher incidence of initial failure and late recurrence as compared with surgery (S: 2.8% vs E: 19.8% and S: 1.6% vs E: 11.2%, respectively).

    Previous meta-analyses by Steinmetz et al 8 and Bakker et al 6 showed treatment success rates of 46% and 72.2%, respectively, with endovascular embolisation. Compared with this, the current updated meta-analysis shows a success rate of approximately 80% with stand-alone embolisation. The higher success rate observed in our review might either be a reflection of advances in endovascular techniques or simply a more accurate reflection of actual success rate due to accrual of more evidence from a larger number of patients.

    Most series in our review involved an initial clinical review to determine feasibility of endovascular ablation. While most made the decision to embolise based on angioarchitecture,13 14 the others invariably performed a trial of embolisation with the initial spinal angiogram.15 There was significant variation observed in success rates, either due to variation in technical skill or due to a variation in definition of treatment success. Some studies considered embolisation to be definitive only when the embolic agent would successfully occlude the draining vein,16 while some relied on fistula occlusion alone.17 Occlusion of draining vein is essential for treatment success, as failure to do so is responsible for delayed recanalisation of fistula. Although the overall incidence of a successful endovascular fistula occlusion seems to have increased as per the current review, it must be noted that we also observed 6.6-fold higher odds of treatment success with surgery (1/0.15) as compared with embolisation alone, similar to Bakker et al.6 This might be because of parallel advances in microsurgical techniques that would still render more favourable odds for surgery. Advances in minimally invasive surgery have made surgical ligation more effective and feasible with a smaller incision size and shorter length of stay.18A tubular approach to surgical ligation of SDAVF has also been described.18

    We also observed higher odds of neurological improvement with surgery as compared with embolisation alone. However, we could not ascertain the neurological outcomes observed with a multimodality approach with both preoperative embolisation and surgery. Despite the failure rate with endovascular therapy, surgical morbidity remains an issue of concern during clinical decision making. In this meta-analysis, we found a marginally higher statistically significant complication rate with surgery (7.7% vs 6.9%), the complication profile must also be taken into account. Most surgical complications were wound-related complications such as surgical site infections, epidural/extradural haematomas and CSF leaks/pseudomeningoceles. On the other hand, complications with endovascular treatment were largely technique-related adverse events such as microcatheter ruptures, spinal cord infarction and other unintended ischaemic complications due to non-target embolisation. Spinal cord ischaemia might be responsible for both transient and permanent neurological deficits and the lower odds of postprocedure neurological improvement seen following embolisation alone. Neurological improvement is also suggested to be significantly dependent on successful closure of the fistula which, as observed, was lower with endovascular approaches. In many series, late recurrences were detected due to neurological deterioration of the patient.17 Due to lack of available evidence from randomised studies, it might be argued that comparable complication rates might be a consequence of selection bias. However, it does speak to the safety of surgical treatment in carefully selected patients, thereby highlighting the benefits of an individualised approach to management.

    In tandem with the results obtained by Bakker et al 6 who observed a statistically non-significant trend towards high failure rates with Onyx, our updated meta-analysis found that recently published series have failed to demonstrate any advantage of newer embolisation agents like Onyx over NBCA. In contrast, we found a significantly higher (OR: 3.87) odds of treatment failure/late recurrence associated with use of Onyx as compared with NBCA. According to Blackburn et al,19 Onyx might fail to reach the draining vein, which could be the possible reason behind this observation, since draining vein occlusion is critical for definitive treatment.17 20

    The exact role of endovascular treatment in the overall management of SDAVFs remains to be determined. More recently, studies which have focused on determining predictive clinical and imaging factors for treatment success with endovascular occlusion are welcome investigations and must be further replicated to enhance understanding its role in management.21–23 These investigations will help to determine if a primary embolisation during initial angiographic workup should be universally used (except in cases of concomitant origin of feeder artery and anterior spinal artery) or applied in a more tailored fashion, with the goal to improve the final neurological status. Factors such as the preoperative neurological status which are a direct determinant of postoperative neurological outcomes might be needed to be taken into account during workup to guide definitive management.21 24 25 The success of surgery also depends on accurate preoperative localisation of the fistula and a carefully selected endovascular workup such as coil placement might aid in a successful postoperative outcome.26 In certain cases with a complex fistular architecture, a planned preoperative embolisation might be an important adjunct to definitive surgical interruption.1 27 Future studies should also systematically report outcomes for patients who receive both endovascular and surgical treatments as part of a staged intervention.

    Strengths and limitations

    The present review has limitations which underlie the limitations of the currently available literature. All available studies were observational and were limited by selection bias, given that vascular anatomy should play an important role in guiding treatment selection. Patients with significant comorbidities might have been also less likely to receive surgery and deferred for embolisation, which could possibly confound results. A significant proportion of studies available did not directly compare surgical and endovascular approaches. Follow-up across studies was highly heterogeneous, which could have further biassed recurrence rates. Nevertheless, this represents the most updated meta-analysis comparing clinical outcomes following either approach with a large number of patients. Given that there is still significant clinical equipoise in this area, it might be justified to conduct prospective randomised studies in the future which will further elucidate the place of endovascular ablation in the context of overall management of these lesions. Randomised studies would also address the selection bias that has so far precluded an accurate characterisation of the specific role of endovascular management. An important subset of cases where the equipoise could be addressed would be patients with acceptable surgical morbidities and a favourable angioarchitecture (as determined by blinded assessment of preoperative imaging) for endovascular treatment.

    Conclusion

    In conclusion, despite advances in endovascular approaches to management of SDAVFs, the currently available literature fails to demonstrate any advantage of embolisation alone over surgery for a successful treatment outcome. Newer embolisation agents might be associated with higher failure rates. Future studies should further elucidate the role of endovascular treatment within the context of the overall management of these malformations, and determine if endovascular ablation can serve as an adjunctive treatment as part of a broader individualised multimodality approach.

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    Footnotes

    • Contributors AG Conceptualisation and design, data collection, analysis and drafting of manuscript. JC Conceptualisation and design, data collection, analysis and drafting of manuscript. VML reviewing and revising original draft. MAA reviewing and revising original draft. PK reviewing and revising original draft. WB reviewing and revising original draft. DMN reviewing and revising original draft. GL reviewing and revising original draft. MB study supervision, reviewing and revising original draft.

    • Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.

    • Competing interests None declared.

    • Patient consent for publication Not required.

    • Provenance and peer review Not commissioned; externally peer reviewed.