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Hemorrhagic Stroke
Case series
Transradial middle meningeal artery embolization for chronic subdural hematoma using Onyx: case series
  1. Gary B Rajah1,2,
  2. Muhammad Waqas1,2,
  3. Rimal H Dossani1,2,
  4. Kunal Vakharia1,2,
  5. Andrew D Gong1,2,
  6. Kyungduk Rho1,2,
  7. Steven B Housley1,2,
  8. Hamid H Rai1,2,
  9. Felix Chin1,2,
  10. Michael K Tso1,2,
  11. Kenneth V Snyder2,3,
  12. Elad I Levy2,4,
  13. Adnan H Siddiqui2,4,
  14. Jason M Davies2,5
  1. 1 Neurosurgery, University at Buffalo Jacobs School of Medicine and Biomedical Sciences, Buffalo, New York, USA
  2. 2 Neurosurgery, Gates Vascular Institute, Buffalo, New York, USA
  3. 3 Neurosurgery and Neurology and Canon Stroke and Vascular Research Center, University at Buffalo Jacobs School of Medicine and Biomedical Sciences, Buffalo, New York, USA
  4. 4 Neurosurgery and Radiology and Canon Stroke and Vascular Research Insitute, University at Buffalo, Jacobs School of Medicine, Buffalo, New York, United States
  5. 5 Neurosurgery and Bioinformatics and Canon Stroke and Vascular Research Center, University at Buffalo Jacobs School of Medicine and Biomedical Sciences, Buffalo, New York, United States
  1. Correspondence to Dr Jason M Davies, Neurosurgery and Bioinformatics and Canon Stroke and Vascular Research Center, University at Buffalo Jacobs School of Medicine and Biomedical Sciences, Buffalo, NY 14203, USA; jdavies{at}ubns.com

Abstract

Background Middle meningeal artery (MMA) embolization is an emerging therapy for the resolution of subacute or chronic subdural hematoma (CSDH). CSDH patients are often elderly and have several comorbidities. We evaluated our experience with transradial access (TRA) for MMA embolization using predominantly Onyx under conscious sedation.

Methods Data for consecutive patients who underwent transradial MMA embolization for CSDH during a 2-year period (2018–2019) were analyzed from a single-center, prospectively-maintained database. Patient demographics, comorbidities, ambulatory times, subdural hematoma resorption status, and guide catheter type were recorded. Conversion to femoral access and complication rates were also recorded. Univariate and multivariate analyses were performed.

Results Forty-six patients (mean age, 71.7±14.4 years) were included in this study. Mean CSDH size was 14±5.5 mm. Most (91.3%) TRA embolizations were performed with 6-French 0.071-inch Benchmark guide catheters (Penumbra). MMA embolization was successful in 44 patients (95.7%) (including two cases of TRA conversion). Twenty-one (48%) patients had a severe Charlson Comorbidity Index (>5). Symptomatic improvement was noted in 39 of 44 patients (88.6%). Mean length of stay was 4±3 days. Patients were ambulated immediately postprocedure. At mean follow-up (8±4 weeks), 86.4% of patients had complete or partial CSDH resolution. Persistent use of antiplatelet agents after the procedure was associated with failed or minimal CSDH resorption (5 of 6, 83.3% vs 9 of 38 23.7% with complete or near-complete resolution; P=0.009).

Conclusion Transradial Onyx MMA embolization under conscious sedation is safe and effective for CSDH treatment. TRA may be especially useful in elderly patients with numerous comorbidities.

  • artery
  • catheter
  • subdural
  • technique
  • technology

http://dx.doi.org/10.1136/neurintsurg-2020-016185

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    Introduction

    Middle meningeal artery (MMA) embolization has rapidly become a new minimally invasive endovascular strategy for the management of subacute or chronic subdural hematomas (CSDH). Although no randomized data about the efficacy of MMA embolization exists at this time, at least two trials are currently recruiting patients to assess this technique (https://clinicaltrials.gov/ct2/show/NCT04095819 and https://clinicaltrials.gov/ct2/show/NCT03307395). To date, our best data on the efficacy of this minimally invasive strategy comes in the form of meta-analytical data. Jumah et al recently reported the largest meta-analysis to date of MMA embolization for refractory CSDH.1 Those authors included 177 patients and noted a mean age of 71±19 years, with an embolization-related complication rate of 1.7%. The rate of overall treatment failure was 2.8%, and the rate of the need for rescue therapy was 2.7%. Embolized patients had a 26% lower risk of hematoma recurrence than nonembolized patients, and the need for surgical rescue was 20% lower in the embolized population.

    Several techniques for MMA embolization have been described, including the use of Onyx (Medtronic, Dublin, Ireland), polyvinyl alcohol (PVA) particles, and n-butyl cyanoacrylate (nBCA), delivered mainly via a transfemoral access (TFA) approach. The population in which MMA embolization for CSDH is most used is typically frail >70-year-old individuals. One study noted that admission frailty contributed to worse prognosis among CSDH patients.2 According to a study of surgically-treated CSDH, among CSDH patients older than 80 years of age, the Charlson Comorbidity Index (CCI) was found to be a valuable outcome predicting tool, with a longer hospital stay noted for patients in that age group who were receiving anticoagulation.3 4 Moreover, a CCI of 4–5 vs 6–8 yielded perioperative complication rates of 13% vs 27.9%, respectively. The 6-month mortality following surgery among CCI 4 to 5 patients vs 6–8 patients was 0.9% vs 11.6%, respectively. The risk of developing a recurrent CSDH among patients receiving warfarin was 42×higher than for those who were not.5 Length of hospital stay after surgical treatment of CSDH has been identified as a predictor of mortality with a HR of 2.5 in the elderly (>76 years).6

    The results from the above studies suggest that MMA embolization must be carried out with the specific intent to avoid general anesthesia, recumbency, and protracted reversal of antiplatelet and anticoagulant therapy. These goals can reduce complication rates and short hospital stays (even same-day discharge) in this frail, frequently anticoagulated population. Transradial MMA embolization has been previously described, and the purpose of this article is to present the feasibility of MMA embolization via transradial access (TRA) using predominately a Benchmark guide catheter (Penumbra Inc., Alameda, CA) with Onyx embolizate under conscious sedation and associated outcomes. We also investigated ambulation and discharge times following TRA MMA embolization.

    Methods

    Study population

    This study is a case series of consecutive patients who underwent TRA MMA embolization for the treatment of CSDH at a single institution. All patients in whom this procedure was attempted were included in this study. There were no exclusion criteria. Our institutional review board approved the study. The study period was 2018–2019. Informed consent was obtained from all patients before procedures were performed.

    Any patient with subacute/chronic SDH larger than 5 mm was included. Patients with focal neurological deficits were not candidates for upfront embolization, with the exception of mild pronator drift. SDH evacuation was emergently carried out in patients presenting in extremis. Patients could undergo embolization prior to, or within, 24 hours after SDH evacuation for those with a large amount of mass effect and midline shift >3 mm. Anticoagulation for SDH embolization alone was not a contraindication. CT scans were obtained at 24 hours and then at 2 weeks and, if improved, 30 days' later. Based on the findings of a randomized controlled trial,7 all patients were started on a statin (atorvastatin, 20 mg daily for 8 weeks) if not already prescribed for another reason. Steroids were administered to some patients at the discretion of the treating physician. Patients requiring continuation of antiplatelet agents or anticoagulation were allowed to continue these medications.

    Data analysis

    Data on demographics, clinical presentation (including CCI), neuroimaging findings before and after the embolization, and rates of retreatment were obtained. Descriptive analyses were performed using SPSS version 25 (IBM, Chicago, IL). Distribution of the data was assessed using a Shapiro–Wilk test. Data with a normal distribution were presented with means and SD. Data with a skewed distribution were presented using median and IQR. Categorical data were presented as percentages and proportions. A univariate analysis was performed to identify factors associated with failed SDH resolution. Binary logistic regression was used to identify independent predictors of failed SDH resolution.

    Technique

    A video of this technique has been published.8 The procedure was completed with mild to moderate conscious sedation and vital sign monitoring. We traditionally used the ventral radial artery for access, however, the anatomical snuff box can also be used.9 The wrist was extended on an arm board and taped in place. Ultrasound-guided micropuncture was used for difficult-to-palpate radial arteries. A 6-French (F) Glidesheath Slender catheter (Terumo Interventional, Somerset NJ) was used for access. A cocktail of verapamil (2.5 mg) and heparin (2000 units) was administered intraarterially. A 6-French, 0.071inch, 95 cm Benchmark guide catheter with either a 5F Berenstein (Merit Medical, Malvern PA) or a 5F Simmons Select diagnostic catheter (Penumbra) over a 0.035inch Glidewire (Terumo Interventional) was used to access the arch. For right-sided procedures, the right common carotid artery (CCA) was directly cannulated from the brachiocephalic trunk. Under roadmap guidance, the Benchmark guide catheter was placed into the external carotid artery. A V-18 buddy wire (Boston Scientific, Marlborough MA) was used for guide catheter stability in tortuous anatomy. A 167 cm Headway Duo microcatheter (MicroVention, Aliso Viejo CA) was then used over a 0.014inch Synchro2 microwire (Stryker Neurovascular, Fremont CA) to access the distal MMA under roadmap guidance. Selective MMA injection was performed to ensure the catheters and wires were beyond the spinosum segment and the petrosal and ophthalmic recurrent branches, as well to assess for any fistula within the sinus. In addition, it is important to correlate the location of the CSDH on a computed tomographic (CT) scan of the head with the selection of the MMA territory targeted for embolization. Lidocaine (30 mg) was injected slowly at a rate of 0.5 mL per minute to numb the dural vessels before dimethyl sulfoxide was injected at a rate of 0.1 mL/min. This maneuver is critical for patient comfort when cases are performed under conscious sedation. The practice is based on our institute’s experience and is usually effective. Theoretically, our lidocaine injection could also warn the interventionist of dangerous extracranial-to-intracranial anastomoses, especially near the orbit, as has been described previously by Chen et al.10

    Once the catheter dead space was full, Onyx 18 (Medtronic, Dublin, Ireland) was injected at a rate of approximately 0.1 mL/min to embolize the MMA and accessory MMA (if necessary) over the corresponding CSDH area on CT imaging. Reflux below the level of the orbital roof and/or sphenoid ridge was not allowed. Occasionally, we pulled the catheter back while injecting the Onyx to seal more proximal vessels. Final injections included intracranial runs. The branch (anterior vs posterior or both) targeted for embolization was selected according to the location of the maximum thickness of the SDH after we reviewed the noncontrast CT images. For example, if the frontal convexity had the maximum SDH thickness and this corresponded on angiography to the location of the frontal branch, we would embolize the frontal branch. If the anatomy was safe and allowed for reflux into the parietal branch, we would pull back the catheter while injecting and embolize that branch as well. However, the area of maximum SDH thickness was the target location. If an accessory MMA branch subserving the SDH location was seen, we would also embolize this vessel with a new microcatheter.

    Results

    We included 46 patients in the study (mean age, 71.7±14.4 years). Thirty-one patients were men (67.4%). The indications for MMA embolization were recurrent CSDH in five patients (10.9%), an adjunct procedure performed within 24 hours of burr hole evacuation in four patients (8.7%), and primary treatment in 37 patients (80.4%). Ten patients (21.7%) presented with headaches. Nine patients (19.6%) had mild hemiparesis. Twenty-one patients (45.6%) had a right-sided embolization, six patients (13.0%) had bilateral MMA embolizations. The mean size of the CSDHs was 14±5.5 mm. Demographic and baseline clinical characteristics are presented in table 1. Right-sided radial artery access was used in all patients except one. All procedures were performed under conscious sedation.

    View this table:
    Table 1

    Clinical and demographic details of study population

    MMA embolization was technically successful in 44 (95.6%) patients. This includes two cases where TRA was switched to TFA due to severe carotid tortuosity and radial artery vasospasm (figure 1). Onyx was the embolizate in 43 cases and nBCA was used in one case. One case among the initial 46 cases was aborted due to extreme tortuosity of the proximal MMA. A second case was aborted because the patient developed sudden bradycardia after lidocaine injection into the parietal branch of the MMA.

    Figure 1
    Figure 1

    Examples of two cases of transradial access failure converted to transfemoral access (TRA) for middle meningeal artery (MMA) embolization and one case of left radial artery access for MMA embolization. A, B: Anteroposterior (AP) left common carotid artery injection. Patient 1: proximal left common carotid artery (CCA) tortuosity combined with an obtuse angle between the brachiocephalic trunk and left CCA makes it very difficult for the 0.035inch wire to climb without backing out the Sim Select (Penumbra Inc., Alameda CA). The Benchmark guide catheter (Penumbra Inc., Alameda, CA) – no matter how trackable – will collapse into the arch. In such cases, a radial approach with a Sim2 Envoy guide catheter (Synthes, Kalamazoo MI) with an intermediate catheter (5-French Sofia [MicroVention, Aliso Viejo CA]) to access the external carotid artery (ECA) may be attempted (see F). B shows conversion to TFA with a VTK catheter (Cook Medical, Bloomington IN) C, D: AP left common carotid artery injection. Patient 2: in this case, the angle and length of the brachicephalic trunk combined with the left CCA proximity to the brachiocephalic trunk create a difficult access; a common origin of the brachiocephalic trunk and left CCA would aid radial access: however, instead, the Sim Select catheter must come down and take a very acute angle back up the ECA. this down vector pulls the wire and Sim Select into the arch, making navigation into the left ECA difficult. C: Depicts rescue TFA for MMA embolization. E, F: AP left common carotid artery injection. Left radial artery approach (no palpable or ultrasound evidence of pulsation of the right radial artery). The hairpin turn from the subclavian artery up the left CCA proved too much of a downward force vector for the 0.035-inch wire and Benchmark guide catheter over a Sim Select catheter (E). A Sim2 Envoy can be seen in stable position within the left CCA ostium (F). Note: this catheter is very stiff; and as such, the hairpin turn at the bottom is wider than that of the Sim Select/Benchmark set up (E). The Sim2 Envoy provided a stable launching platform for the 5F Sofia (inset) into the ECA. forming a Sim2 Envoy guide catheter in the radial artery that can be challenging, Two options exist: advancing the catheter into the ascending aorta and circling it around the valve over the wire and diagnostic catheter (to avoid step off and injury to the valve) or bouncing the wire off the arch into the brachiocephalic trunk and forming the guide catheter in the brachiocephalic trunk.

    Among the 44 patients who had successful MMA embolization, no access-site complications occurred, including in those cases in which the access approach was switched to a femoral access approach. All ambulatory patients, excluding the TFA patients, were ambulated immediately after the procedure because there was no restriction on ambulation post-TRA. The mean length of total hospital stay was 4±3 days. Seven patients received dexamethasone for 14 days. Four patients could be discharged home the same day after observation. The mean length of clinical follow-up was 8±4 weeks. Complete resolution was seen on CT imaging in 23 (52.3%) of the successfully embolized patients. Partial resolution was seen in 15 patients (34.1%). Six patients (13.6%) had minimal or no radiological reduction in hematoma size, however, no hematoma growth was seen. Symptomatic improvement was seen in 39 of the 44 (88.6%) patients (figure 2). There was no change in the size of the hematoma in five cases that had to be retreated with surgical evacuation of the CSDH. The rate of retreatment among successfully embolized patients was thus 11.4% (five of 44). One nonagenarian patient died of worsening underlying congestive heart failure and aspiration pneumonia 1 month after MMA embolization. Procedural details and outcomes are presented in table 2.

    View this table:
    Table 2

    Procedural details and outcomes

    Figure 2
    Figure 2

    CTimages without contrast pre- and post-MMA embolization. A: Pre-MMA embolization of right subdural hematoma. B: Full resolution of the right chronic subdural hematoma (CSDH) at 2 months following right MMA embolization: the sulci are now seen with no local mass effect. C: CT reveals pre-MMA embolization of a left subdural hematoma. D: CT reveals a case of a nonresponder in which the left CSDH remains the same size and density on the 2-month follow-up scan. E: CT reveals pre-MMA embolization of a left CSDH. F: CT reveal partial resolution in a patient with mild relief of mass effect from the left CSDH embolization alone.

    On univariate analysis, the use of antiplatelet agents in the postoperative period was associated with failed resorption of CSDH (83.3% vs 23.7%, P=0.009). Hematoma size, sex, age, and CCI were not associated with failed resorption of CSDH (table 3). On multivariate binary logistic regression, antiplatelet use during the postoperative period was the only significant predictor of failed CSDH resolution with an OR of 33.35 (95% CI 1.74–639.1, P=0.002). Other variables in the model included sex, CSDH size, CCI, and treatment approach (primary vs adjunct).

    View this table:
    Table 3

    Association of different variables with failed resolution of CSDH

    Discussion

    Here we report a large series of TRA MMA embolization for CSDH. We feel that TRA allows for early discharge and ambulation in this frail population. Key to our TRA is the use of the Benchmark guide catheter, which is very trackable over light 0.035inch Glidewires and Simmons diagnostic catheters. This guide catheter also provides the necessary support for distal MMA artery navigation and embolization. This guide is uniquely able to navigate radial, subclavian, and carotid loops and tortuosity, allowing for a high rate of procedural success in this population of patients who can have very tortuous anatomy. Aortic arch tortuosity increases with age and can make transfemoral procedures more time consuming, difficult, and higher embolic risk from protracted endovascular maneuvers in atherosclerotic vessels.11 The 0.071inch guide catheter provides enough support and room for a 0.018inch buddy wire when necessary for navigating difficult anatomy in addition to allowing for control injections to delineate vascular anatomy. We initially attempted to use slightly stiffer guide catheters, that is, Envoy XB DA (Stryker Neurovascular): however, although this guide catheter may provide more support, it is prone to kinking, especially when placed in tortuous right-sided vessels from a right TRA. In addition, this catheter is not as trackable from a radial approach. The Benchmark guide catheter provides the right amount of support, trackability, and length for TRA MMA embolization while still being compatible with a 6F short sheath. In our series, there were no access-site complications and a low TRA-to-TFA conversion rate. TRA allowed for early ambulation and same-day discharge in suitable patients who did not have severe medical issues requiring prolonged hospitalization.

    Assessing the cardiac literature, it is no surprise that TRA is preferred among elderly patients undergoing coronary intervention. The authors of a meta-analysis of studies comprising more than 4000 elderly patients undergoing percutaneous coronary intervention noted the noninferiority of TRA in regards to revascularization, contrast use, and procedure time: however, with respect to major bleeding, TRA had an OR of 0.49 compared with TFA.12 Those authors also noted a mean difference of 10 hours in ambulation time, favoring TRA over TFA. Jin et al showed that early ambulation following TRA vs TFA can lead to early hospital discharge and cost savings.13

    Our ideal embolic material is Onyx 18 because of its ability to seal and penetrate vessels distally in addition to its visibility, permanence, and ability for protracted injections. For these reasons, we prefer the use of Onyx over other agents. To date, no studies have shown the superiority of one embolizate over another for MMA embolization. However, most studies previously have used PVA particles.14 Our need for repeat treatment of SDH after Onyx MMA embolization in this study was 11.4%. This is higher than that in a recent meta-analysis, in which most studies used PVA particles and the retreatment rate was 3.6%.14 A reason for this may include our relatively small sample size: nevertheless, there is a need for studies to determine the best embolic agent in a head-to-head comparison.

    Lastly, we would like to draw attention to the numerous comorbidities within our patient population. Among the 44 successfully treated patients, 48% had a CCI>5. Examining our major periprocedural complication rate of 2.2%, this is incredibly low compared with the 27.9% complication rate in a series of surgical perioperative complications for patients in the CCI>5 group.4 In our series, 88% of the patients had symptomatic relief. The age and level of comorbidities in this patient population necessitates extremely low access and procedural complication rates. The comorbid conditions seen in our 46-patient study population included a 13% rate of atrial fibrillation, a 8.6% rate of congestive heart failure, and a 23.9% rate of diabetes. Antiplatelet use on univariate and multivariate analyses was the only factor in our study associated with CSDH recurrence. This may be due to failure of the SDH membranes to devascularize or embolize fully despite Onyx embolization of the more proximal vascular supply. This finding will need further study. It is interesting to note that the same is true for open cranial surgery: antiplatelets significantly increase the risk of CSDH recurrence. Wada et al noted surgical CSDH patients had a recurrence rate of 11% off antiplatelets, but if antiplatelets were held immediately before surgery, recurrence rates were 32%.15

    Limitations

    Our main limitations are the lack of comparison to TFA MMA embolization procedures and the small sample size of our series. Onyx was used for embolization in all cases but one in our series: as such, no comparisons can be made with other embolic agents. Findings in our regression analysis may be overestimated given the small numbers of patients in our series.

    Conclusion

    Transradial Onyx embolization under conscious sedation of the MMA via predominately a neurospecific 0.071inch guide catheter appears safe and useful for the treatment of CSDH in the elderly and may aid in earlier ambulation in this population of patients who are frequently prone to anticoagulation use and numerous comorbid conditions. Antiplatelet use may contribute to lack of CSDH response after MMA embolization.

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    Footnotes

    • Twitter @duktusvenosus, @Sbhousleymd, @MikeTso1

    • Contributors Conception and design: GBR, JMD, AHS, MW. Acquisition of the data: all authors. Analysis and interpretation of the data: all authors. Drafting the manuscript: GBR, MW. Critically revising the manuscript: all authors. Reviewed submitted version of manuscript: all authors.

    • 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 GBR, MW, RHD, KV, AG, KR, SBH, HHR, FC, MKT: NoneEIL: shareholder/ownership interests: NeXtGen Biologics, RAPID Medical, Claret Medical, Cognition Medical, Imperative Care (formerly the Stroke Project), Rebound Therapeutics, StimMed, Three Rivers Medical; National Principal Investigator/Steering Committees: Medtronic (merged with Covidien Neurovascular) SWIFT Prime and SWIFT Direct Trials; Honoraria: Medtronic (training and lectures); Consultant: Claret Medical, GLG Consulting, Guidepoint Global, Imperative Care, Medtronic, Rebound, StimMed; Advisory Board: Stryker (AIS Clinical Advisory Board), NeXtGen Biologics, MEDX, Cognition Medical, Endostream Medical; Site Principal Investigator: CONFIDENCE study (MicroVention), STRATIS Study—Sub I (Medtronic).AHS: financial interest/investor/stock options/ownership: Adona Medical, Inc, Amnis Therapeutics, (purchased by Boston Scientific October 2017), Blink TBI Inc., Buffalo Technology Partners Inc., Cerebrotech Medical Systems, Inc., Cognition Medical, Endostream Medical Ltd., Imperative Care, International Medical Distribution Partners, Neurovascular Diagnostics Inc., Q’Apel Medical Inc, Rebound Therapeutics Corp. (purchased 2019 by Integra Lifesciences, Corp), Rist Neurovascular Inc., Sense Diagnostics, Inc., Serenity Medical Inc., Silk Road Medical, Spinnaker Medical, Inc., StimMed, Synchron, Three Rivers Medical Inc., Vastrax, LLC, VICIS, Inc., Viseon Inc; consultant/advisory board: Amnis Therapeutics, Boston Scientific, Canon Medical Systems USA Inc., Cerebrotech Medical Systems Inc., Cerenovus, Corindus Inc., Endostream Medical Ltd., Imperative Care, Inc. Integra LifeSciences Corp., Medtronic, MicroVention, Minnetronix Neuro, Inc., Northwest University–DSMB Chair for HEAT Trial, Penumbra, Q’Apel Medical Inc., Rapid Medical, Rebound Therapeutics Corp.(purchased by Integra LifeSciences Corp.), Serenity Medical Inc., Silk Road Medical, StimMed, Stryker, Three Rivers Medical, Inc., VasSol, W.L. Gore & Associates; principal investigator/steering committee for the following trials: Cerenovus NAPA and ARISE II; Medtronic SWIFT PRIME and SWIFT DIRECT; MicroVention FRED & CONFIDENCE; MUSC POSITIVE; and Penumbra 3D Separator, COMPASS, INVEST, TIGER.KVS: consulting and teaching for Canon Medical Systems Corporation, Penumbra Inc., Medtronic, and Jacobs Institute. Co-founder: Neurovascular Diagnostics, Inc.JMD: Research grant: National Center for Advancing Translational Sciences of the National Institutes of Health under award number KL2TR001413 to the University at Buffalo. Consulting: Medtronic; Honoraria: Neurotrauma Science, LLC; shareholder/ownership interests: Cerebrotech, RIST Neurovascular. University at Buffalo Neurosurgery received an educational grant from Penumbra, Inc. However, the company had no editorial control.

    • Patient consent for publication Not required.

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