Improved results using Onyx glue for the treatment of persistent type 2 endoleak after endovascular aneurysm repair
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1 From the Eastern Vascular Society Improved results using Onyx glue for the treatment of persistent type 2 endoleak after endovascular aneurysm repair Christopher J. Abularrage, MD, a,b Virendra I. Patel, MD, a Mark F. Conrad, MD, MMSc, a Eric B. Schneider, PhD, c Richard P. Cambria, MD, a and Christopher J. Kwolek, MD, a Boston, Mass; and Baltimore, Md Objective: Persistent type 2 (PT2) endoleaks (present >6 months) after endovascular aneurysm repair are associated with adverse outcomes, and selective secondary intervention is indicated in those patients with an expanding aneurysm sac. This study evaluated the outcomes of secondary intervention for PT2. Methods: From 1999 to 2007, 136 patients who underwent endovascular aneurysm repair developed PT2 and comprised the study cohort. Primary end points included PT2 resolution (secondary interventional success) and survival, and were evaluated using multiple logistic regression and Kaplan-Meier analyses, respectively. Results: Fifty-one patients underwent a total of 68 secondary interventions for PT2 with expanding aneurysm sacs with a median postsecondary interventional follow-up of 13.7 months. Secondary interventions included 20 inferior mesenteric artery coil embolizations, 17 Onyx glue embolizations, 11 aneurysm sac coil embolizations, 10 non-onyx glue embolizations, 7 lumbar artery coil embolizations, 2 open lumbar ligations, and 1 graft explant. The overall secondary interventional success rate was 43% (29 of 68). Onyx glue embolization was associated with a greater success rate when used as the initial secondary intervention (odds ratio, 59.61; 95% confidence interval, ; P <.001). There was no difference in success between the different techniques when multiple secondary interventions were required. Five-year survival was 72% 0.08% and was unrelated to any of the secondary interventional techniques. Conclusions: Secondary intervention for PT2 is associated with success in less than half of all cases. Onyx glue embolization was associated with greater long-term success when used as the initial secondary intervention. (J Vasc Surg 2012;56:630-6.) From the Division of Vascular and Endovascular Surgery, Massachusetts General Hospital and Harvard Medical School, Boston a ; and the Division of Vascular Surgery and Endovascular Therapy, b and Center for Surgical Trials and Outcomes Research, c The Johns Hopkins Hospital, Baltimore. Author conflict of interest: none. Presented at the Twenty-fifth Annual Meeting of the Eastern Vascular Society, Washington, DC, September 22-24, Reprint requests: Christopher J. Kwolek, MD, Division of Vascular and Endovascular Surgery, Massachusetts General Hospital, Harvard Medical School, WAC440, 15 Parkman Street, Boston, MA ( ckwolek@partners.org). The editors and reviewers of this article have no relevant financial relationships to disclose per the JVS policy that requires reviewers to decline review of any manuscript for which they may have a conflict of interest /$36.00 Copyright 2012 by the Society for Vascular Surgery. doi: /j.jvs Endovascular aneurysm repair (EVAR) is an established therapy for the treatment of abdominal aortic aneurysms (AAAs) with suitable anatomy. EVAR has been associated with a 65% to 70% reduction in the 30-day mortality compared to open AAA repair. 1,2 Although the Open versus Endovascular Repair (OVER) trial demonstrated a lower aneurysm-related mortality of EVAR compared with open AAA repair at 2 years, 3 other studies have found that this early advantage in mortality is lost on long-term followup. 4-6 The equalization of mortality over time has led to a greater scrutiny of the long-term outcomes of EVAR and the need for secondary intervention. EVAR requires continued surveillance, as up to 11% of patients require secondary intervention for graft-related complications, in particular endoleaks. 7 Recent long-term follow-up of the EVAR I and EVAR II trials demonstrated a 74% freedom from secondary intervention at 8 years. 6 Although the presence of type 1 and 3 endoleaks is a clear indication for secondary intervention, the clinical significance of type 2 endoleaks has not been completely established. Type 2 endoleaks occur in 10% to 30% of patients after EVAR and may be associated with aneurysm growth and rupture. 8,9 Subdivision of type 2 endoleaks into transient (resolving within 6 months) and persistent (present beyond 6 months) has been found to predict EVAR-related complications. Persistent type 2 (PT2) endoleaks have been associated with an increased incidence of adverse outcomes, including aneurysm sac growth, secondary intervention rate, the need for conversion to open repair, and rupture. 10 In addition, long-term surveillance and secondary intervention are associated with increased costs after EVAR. 11 Accordingly, the success of secondary interventions is an important clinical goal. The purpose of this study was to evaluate the results of secondary intervention for PT2 over a 10-year period at a single academic medical center. METHODS All EVARs performed between January 1999 and December 2007 were retrospectively identified from a prospectively maintained database. The study was approved by the Institutional Review Board of the Massachusetts General
2 JOURNAL OF VASCULAR SURGERY Volume 56, Number 3 Abularrage et al 631 Hospital. Exclusion criteria included patients with thoracic aortic aneurysms, anastomotic aneurysms, isolated iliac artery aneurysms, and patients with 6 months follow-up. Preoperative data collection was obtained from the patient hospital and office charts and included demographics, medical history, and laboratory results. Estimated glomerular filtration rate was calculated according to the Modification of Diet in Renal Disease Study. 12 Chronic renal insufficiency was defined as a glomerular filtration rate 60, or chronic kidney disease stages 3 to All preoperative and postoperative computed tomography (CT) scans were reviewed by an attending radiologist, an attending vascular surgeon, and a vascular fellow. Patients underwent preoperative CT scan imaging with 2.0- to 2.5-mm cuts. Preoperative anatomic variables included maximum aneurysm diameter, maximum aneurysm luminal diameter, aneurysm sac volume, patency of the inferior mesenteric artery (IMA), number of patent lumbar arteries, occlusion of internal iliac vessels (chronic or via preoperative embolization), and percent of aneurysm sac thrombosis. The maximum aneurysm luminal diameter was defined as the shortest diagonal of the contrast opacified lumen measured on the same cross-sectional CT image with the maximum aneurysm diameter. Aneurysm sac volume was calculated based on M2S (M2S Inc, West Lebanon, NH) three-dimensional imaging total aneurysm volume to the right hypogastric artery in cubic centimeters. Thrombus load was defined as the area of the aneurysm sac measured on the same cross-sectional CT image with the maximum aneurysm diameter minus the maximum aneurysm luminal area. Percent of sac thrombosis was calculated by the method of Sampaio et al 14 and was defined as the ratio of the area of the thrombus load to that of the aneurysm sac. All patients in the study received a follow-up CT scan with intravenous contrast and thin collimation 6 months postoperatively. After a nonenhanced CT scan was performed, a bolus injection of contrast was administered at 4 ml/s with a 25-second preparation delay. Delayed phase images were then obtained, and images were reconstructed with 2.0- to 2.5-mm cuts. The presence of a type 2 endoleak was determined by the radiologist and/or surgeon and was corroborated in blind fashion by a study vascular surgeon and/or fellow. Arteriography was performed when it was not possible to differentiate between different types of endoleaks. PT2 was defined as any type 2 endoleak present 6 months postoperatively and included lateappearing type 2 endoleaks that were not present before 6 months. Further follow-up imaging with CT angiography was typically obtained at 6-month to 1-year intervals. The preferred method of treatment changed over time due to the availability of new treatment modalities. A more aggressive approach to these patients was taken as we learned of the adverse late outcomes associated with PT2 and aneurysm sac growth. Presecondary intervention anatomic variables included maximum aneurysm diameter, aneurysm sac volume, patency of the IMA, and number of patent lumbar arteries. Treatment modalities included coil embolization of the aneurysm sac, lumbar arteries, or IMA; direct sac injection of Onyx (ev3 Inc, Irvine, Calif) or non-onyx glue; open lumbar artery ligation; and graft explant. Access to the aneurysm was achieved by several methods: (1) direct translumbar puncture of the aneurysm sac with the patient in the right lateral decubitus position with placement of a 6F MAK-NV-006 mini-access trocar (Merit Medical Systems Inc, South Jordan, Utah); (2) via a retrograde brachial or femoral artery approach to the superior mesenteric artery with access to the IMA via the meandering mesenteric artery using a microcatheter; or (3) using a microcatheter via collateral vessels from the hypogastric artery. The size and number of coils used were at the attending surgeon s discretion. Direct sac puncture allowed the placement of larger fiber coils (Cook Medical Inc, Bloomington, Ind) through a 4F catheter. Both detachable and pushable coils (Cook Medical Inc) were used through the microcatheters. Non-Onyx glue treatment included Gelfoam pellets (Pfizer Inc, New York, NY) combined with Thrombin (King Pharmaceuticals Inc, Bristol, Tenn), Bioglue (Cryolife Inc, Kennesaw, Ga), and/or n-butyl-2-cyanoacrylate (Cordis Inc, Miami Lakes, Fla). Onyx is a liquid embolic agent ethylene vinyl alcohol (EVOH) copolymer dissolved in dimethyl sulfoxide (DMSO) and is approved for use in the United States with an indication for the treatment of intracranial aneurysms. It comes in two formulations: Onyx 18 (6% EVOH) and Onyx 34 (8% EVOH). Onyx 18 has a lower viscosity and, therefore, may flow farther in the endoleak cavity. Both formulas solidify within 5 minutes of injection. Onyx glue treatment required placement of an Echelon 14 microcatheter (ev3 Inc), which is compatible with the DMSO used as a component of Onyx. A failed attempt was defined as an unsuccessful endovascular attempt at accessing the endoleak cavity. Postsecondary intervention anatomic variables included maximum aneurysm diameter, aneurysm sac volume, patency of the IMA, and number of patent lumbar arteries. Secondary interventional success was defined as resolution of the PT2. Continuous variables are reported as mean SEM. Univariate comparisons of patient demographic and risk factors and anatomic variables were performed using 2 or Fisher exact test and unpaired t-tests, when appropriate. Survival analysis was performed using the Cox-Mantel test of the Kaplan-Meier survival estimates. Certain patients had more than one intervention and, thus, interventional outcomes in these patients were not independent. Therefore, the cohort was stratified into two groups: the initial secondary intervention and subsequent secondary interventions. This was performed to account for the fact that outcomes might not be independent due to either demographic factors within the patient or factors related to the nature of that patient s PT2. Logistic regression analysis was performed on the stratified groups using all variables with P.10 on univariate analysis. Procedure year was also included in the multivariable analysis because Onyx was not available
3 632 Abularrage et al JOURNAL OF VASCULAR SURGERY September 2012 Table I. Preoperative characteristics and anatomic variables Table II. Long-term secondary interventional success of endovascular interventions for PT2 endoleak Onyx Non-Onyx P value Procedures, No. Long-term success No. of patients Preoperative comorbidities Age, years a Male gender 16 (94%) 41 (84%).43 Tobacco use 13 (76%) 33 (67%).55 Hypertension 15 (88%) 43 (88%).99 Coronary artery disease 10 (59%) 12 (24%).02 Diabetes mellitus 1 (6%) 8 (16%).43 Chronic renal insufficiency 4 (24%) 22 (45%).16 COPD 2 (12%) 8 (16%).99 Atrial fibrillation 3 (18%) 16 (33%).35 Hypercholesterolemia 14 (82%) 25 (51%).04 Medications Aspirin 11 (65%) 22 (45%).26 Clopidogrel 4 (24%) 3 (6%).07 Warfarin/anticoagulation 2 (12%) 9 (18%).71 Pre-EVAR CT scan Patent IMA 17 (100%) 49 (100%) NC Patent lumbar arteries a MALD (76%) 33 (67%).99 Lumen diameter, mm a Sac diameter (mm) a Sac volume (cc) a Presecondary intervention CT scan Patent IMA 12 (71%) 43 (88%).13 Patent lumbar arteries a Sac diameter, mm a Sac volume, cc a COPD, Chronic obstructive pulmonary disease; CT, computed tomography; EVAR, endovascular abdominal aortic aneurysm repair; IMA, inferior mesenteric artery; MALD, maximum aneurysm luminal diameter; NC, not calculated. a Mean SEM. until later in the study period. All P values.05 (twotailed) were considered significant. Analyses were performed using StatView software (SAS Inc, Cary, NC). RESULTS During the study period, EVAR was performed in 832 patients. Overall results from our EVAR experience have been published previously. 15 Five hundred ninety-five of the 832 patients underwent follow-up CT scans 6 months postoperatively. PT2 was identified in 136 patients who comprised the study cohort. Fifty-one patients (38%) underwent a total of 68 secondary interventions for PT2 with expanding aneurysm sacs with a median postsecondary interventional follow-up of 13.7 months. Of the 68 secondary interventions, 3 were open surgical and 65 were endovascular procedures. Endovascular patients were divided into two cohorts depending on whether they underwent Onyx glue embolization (Onyx, n 17) or not (non-onyx, n 48). Preoperative patient characteristics and anatomic variables are summarized in Table I. The Onyx group tended to be younger ( vs years; P.004) Endovascular secondary interventions (40%) Onyx glue (76%) Lumbar coil embolization 7 3 (43%) Sac coil embolization 11 4 (36%) IMA coil embolization 20 4 (20%) Non-Onyx glue 10 2 (20%) IMA, Inferior mesenteric artery; PT2, persistent type 2. Table III. Univariate analysis of long-term interventional success of initial secondary intervention Endovascular secondary interventions Procedures, No. Long-term success P value Onyx glue (91%).001 Non-Onyx embolization 40 9 (23%) and had a higher incidence of coronary artery disease (59% vs 24%; P.02) and hypercholesterolemia (82% vs 51%; P.04). There were no statistically significant differences in the preoperative or presecondary intervention CT scan measurements between the Onyx and the non-onyx groups. Eighty percent of patients undergoing secondary intervention for PT2 had sac enlargement. The long-term success rate was 38% (29 of 77) in all secondary interventions for PT2. When excluding failed attempts at accessing the endoleak cavity (n 9), the long-term success rate of secondary intervention was 43% (29 of 68). Finally, when excluding open surgical secondary interventions, the long-term success rate of endovascular secondary intervention was 40% (26 of 65; Table II). The mean change in aneurysm sac diameter from presecondary intervention to maximum follow-up was decreased in the Onyx glue embolization group ( 2 1vs3 1mm non-onyx). Excluding failed attempts, a total of 13 patients (20%) required more than one secondary endovascular intervention, one of whom required more than two secondary interventions for persistently expanding aneurysm sac. Of the 14 subsequent secondary endovascular interventions for recurrent type 2 endoleak, only one was performed for a failure of Onyx glue embolization. Upon stratification of the cohort, there were 51 initial secondary interventions and 14 subsequent secondary interventions. On univariate analysis of the initial secondary intervention (Table III), Onyx glue embolization was associated with a greater long-term success rate (91% vs 23%; P.001). Univariate analysis of subsequent secondary interventions did not find any statistically significant differences in long-term success between those who received Onyx glue embolization and those who did not (P 1.0; Table IV). Multivariable logistic regression analysis of the
4 JOURNAL OF VASCULAR SURGERY Volume 56, Number 3 Abularrage et al 633 Table IV. Univariate analysis of long-term interventional success of subsequent secondary interventions Endovascular secondary interventions Procedures, No. Long-term success P value Onyx glue 6 3 (50%) 1 Non-Onyx embolization 8 4 (50%) Table V. Multivariable logistic regression of long-term interventional success of initial secondary intervention OR 95% CI P value Onyx glue Procedure year Coronary artery disease Age Hypercholesterolemia Clopidogrel CI, Confidence interval; OR, odds ratio. initial secondary intervention group found that Onyx glue embolization was the only examined factor associated with long-term success (odds ratio, 59.61; 95% confidence interval, ; P.001; Table V). In the entire cohort, 5-year survival was 72% 0.08% and was independent of any specific secondary interventional technique. Specifically, there were no statistically significant differences in survival between the Onyx and non-onyx groups at 4 years (92% 0.08% vs 82% 0.07%; P.84; Fig 1). No patients developed a ruptured aneurysm in the follow-up period. DISCUSSION Randomized trials have shown an early survival benefit of EVAR compared to open AAA repair, making EVAR the preferred treatment of AAAs with suitable anatomy. 2,16 However, only the OVER trial found that this early benefit in overall mortality extended beyond 2 years postoperatively. 3 Long-term costs of EVAR related to obligatory surveillance can be significant 17 and are only exacerbated by the costs of secondary interventions. 18 The need for secondary intervention after EVAR ranges from 11% to 19% and is accounted for by the presence of type 2 endoleaks in up to 40% of these cases. 7,19 Thus, type 2 endoleaks are the most common indication for secondary intervention. Type 2 endoleaks were previously believed to be of minor significance, but recent evidence suggests that this may not be the case. We have previously shown that PT2 endoleaks are associated with aneurysm sac expansion and rupture The timing of secondary intervention for type 2 endoleaks has been the subject of much debate. Some have argued that preoperative branch vessel management to prevent type 2 endoleaks can decrease the risk of adverse outcomes. 20 Results from our overall experience suggest that this is unnecessary, because only 7% of patients required secondary intervention for PT2 and 93% of patients would have undergone an unnecessary procedure. 21 We, therefore, use a strategy of selective secondary intervention for type 2 endoleaks in the presence of aneurysm sac expansion and persistence beyond 6 months postoperatively. Access to the aneurysm sac can be achieved via multiple approaches and is patient-specific. The location of the endoleak on CT scan dictates the access that is chosen. If the IMA is involved, then a superior to IMA access via the marginal artery of Drummond may be chosen. If the endoleak involves only the lumbar arteries, then a transfemoral or a hypogastric approach can be used. Translumbar access is frequently employed for all types of PT2 because it gives direct access to the aneurysm sac. The method of PT2 secondary intervention changed over the course of the 10-year study period. This was due, in part, to the commercial availability of the different techniques and our experience with endoleak management. Early on, we performed direct sac puncture with coil embolization into the aneurysm sac or the placement of other embolic materials, such as thrombin and gelfoam adjacent to the feeding vessels. Although these procedures initially seemed to decrease flow, they were often unsuccessful because we could not directly cannulate all of the feeding vessels. This led to recanalization of the endoleak cavity through the formation of new flow channels. In addition, direct coil embolization of feeding lumbar vessels is not always technically possible. This led us to seek a more reliable method to obliterate flow. Our current technique involves obtaining aneurysm sac access with subsequent placement of a DMSO-compatible microcatheter directly into the flow channel of the endoleak, which is confirmed by contrast injection. After flushing with saline to clear the catheter of all blood, the dead space of the catheter is replaced with DMSO. Onyx is then injected and allowed to fill both the flow channel within the aneurysm sac and the feeding vessels. Onyx 34 is initially injected into the endoleak cavity of the aneurysm sac and inherently propagates with the flow of blood, ultimately solidifying and plugging the endoleak channel. Once we have a cast of the feeding vessels and are comfortable with how quickly the Onyx travels, we switch to Onyx 18, which is less viscous. Thus, Onyx addresses both the aneurysm sac endoleak cavity as well as the involved aortic branch vessels. Previous studies have found improved success when the endoleak cavity is addressed in addition to the branch vessels. 22 Furthermore, aneurysm sac coil embolization may be extensive, requiring a large number of expensive coils. This may greatly increase the cost of secondary intervention with little improvement in success rates, as isolated aneurysm sac coil embolization in the current study was associated with a 36% long-term success rate. We also found that direct injection of Onyx into the aneurysm sac, without first identifying the flow channel, was not effective in treating the endoleak. Onyx is suspended in micronized tantalum powder making it radio-opaque during angiography. Thus, we
5 634 Abularrage et al JOURNAL OF VASCULAR SURGERY September 2012 Fig 1. Kaplan-Meier survival curves for the Onyx and non-onyx groups. Fig 2. Translumbar angiogram after coil and Onyx embolization demonstrating cast of feeding lumbar vessels and endoleak cavity. Fig 3. Anteroposterior radiograph demonstrating Onyx cast of endoleak cavity and feeding lumbar vessels. ideally like to see a cast of the feeding lumbar vessels on angiography to know that we have successfully treated the endoleak (Fig 2). This may result in considerable streak artifact on follow-up CT scan imaging; however, continued measurement of the aneurysm sac size is possible. One can also appreciate a cast of the endoleak cavity and feeding vessels on plain X-ray or CT reconstruction (Fig 3). Postprocedure imaging is mandatory to evaluate the success of secondary intervention. Endoleak recurrence is a common problem after secondary intervention. In the current study, this occurred in
6 JOURNAL OF VASCULAR SURGERY Volume 56, Number 3 Abularrage et al 635 Fig 4. A, Initial angiogram of inferior mesenteric-to-lumbar artery type 2 endoleak treated with Onyx via a superior mesenteric to inferior mesenteric artery approach. B, Postsecondary intervention computed tomography (CT) scan demonstrating conversion to a lumbar-to-lumbar endoleak (arrow). C, Angiogram demonstrating Onyx cast of both endoleaks. 40% of patients who initially had a successful technical result. Other series have found a 10% to 60% recurrence of type 2 endoleaks after secondary intervention. 19,23,24 This is most likely a difference in techniques because results improved throughout the course of the study. Over the study period, we also identified the ineffectiveness of isolated IMA coil embolization. Although this is a relatively easy technique, it frequently converts an IMA-to-lumbar endoleak into a lumbar-to-lumbar endoleak. 22 Other causes of embolization failure may include persistent flow through poorly packed coils, or the development of a retiform anastomosis around coiled vessels. 24 We did note recanalization of IMA vessels previously treated with coil embolization and have now changed to Onyx embolization of the IMA. This allows us to treat not only the IMA, but also a feeding lumbar vessel at the same setting. If there are multiple pairs of lumbar vessels at different levels or a patent IMA and lumbar vessels separated by a great distance, a second treatment session may be required to access another part of the sac (Fig 4). Endoleak recurrence may be difficult to identify in the presence of either coils or an Onyx cast, as both cause a great deal of scatter on follow-up CT angiography. However, we have found that accurate sac diameter measurements are not inhibited by the scatter. When combined with duplex ultrasonography scan, recurrent flow within the sac causing sac expansion can be estimated with reasonable certainty. Although the use of Onyx glue did result in the greatest success rates, one limitation of the technique is cost. Onyx is currently provided in 1-mL vials which cost approximately $2500 each. Over the study period, we changed our technique to use fewer vials at the initial secondary intervention with a focus on occluding the outflow vessels. This can often be combined with the use of large coils to partially occlude the flow channel within the aneurysm sac and decrease overall cost. We will also intentionally plan to bring patients back for repeat Onyx glue injections at a later date if feeding vessels are identified at multiple sites rather than try to fill a large aneurysm cavity with Onyx alone. It is interesting that Onyx glue embolization was associated with long-term success when used as the initial secondary intervention, but not when used in the treatment of a failed secondary intervention. No studies examining the long-term effects of Onyx exist in the literature to help explain this discrepancy. It may represent a difference in the characteristics of the PT2 itself. A prospective trial of Onyx would be necessary to tease out these details, because the analysis was limited by a small number of patients who required more than one secondary intervention. In the current study, survival did not differ among the different techniques. This likely represents the fact that the risk of rupture, which increased in the presence of PT2, is relatively low; thus, identification and treatment of PT2 with continued close follow-up results in excellent overall survival. Because Onyx was a relatively new aspect of our treatment paradigm, it remains to be seen if the increased costs justify its use. Based on the stratification of the secondary interventions, it may only be worthwhile to use Onyx at the initial secondary intervention. The current study represents one of the largest cohorts undergoing secondary intervention specifically for PT2. Our results must be viewed with caution. There were a number of diverse techniques used to treat PT2 over a long period of time. Thus, factors other than those studied may account for the results. The decision to intervene with a particular endovascular technique was surgeon-specific and driven predominantly by the experience of one senior interventionalist (C.K.) over the study period. A patient may have been a candidate for multiple techniques, but these were not randomized over the study period. Any differences seen in the current study must be confirmed in a randomized study. In conclusion, secondary intervention for PT2 is associated with success in less than half of all cases. There was an increased rate of success with the use of Onyx glue embolization at the initial secondary intervention, although survival was not predicted by any of the secondary interventional techniques. Further study of Onyx for the management of endoleak seems warranted, with the hope that a
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