CLINICAL STUDY. Since it was first described more than 20 years ago, endovascular aneurysm repair (EVAR) has become firstline
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1 CLINICAL STUDY Preoperative Inferior Mesenteric Artery before Endovascular Aneurysm Repair: Decreased Incidence of Type II Endoleak and Aneurysm Sac Enlargement with 24-month Follow-up Thomas J. Ward, MD, Stuart Cohen, MD, Aaron M. Fischman, MD, Edward Kim, MD, Francis S. Nowakowski, MD, Sharif H. Ellozy, MD, Peter L. Faries, MD, Michael L. Marin, MD, and Robert A. Lookstein, MD ABSTRACT Purpose: To review the effect of preoperative embolization of the inferior mesenteric artery (IMA) before endovascular aneurysm repair (EVAR) on subsequent endoleaks and aneurysm growth. Materials and Methods: Between August 2002 and May 2010, 108 patients underwent IMA embolization before EVAR. Coil embolization was performed in all patients in whom the IMA was successfully visualized and accessed during preoperative conventional angiography. In this cohort, the incidences of type II endoleak, aneurysm sac volume enlargement at 24 months, and repeat intervention were compared with a group of 158 consecutive patients with a patent IMA on preoperative computed tomography angiography but not on conventional angiography, who therefore did not undergo preoperative embolization. Results: The incidence of type II endoleak was significantly higher in patients not treated with embolization (49.4% [78 of 158] vs 34.3% [37 of 108]; P ¼.015). The incidence of secondary intervention for type II endoleak embolization was also significantly higher in those who did not undergo embolization (7.6% [12 of 158] vs 0.9% [one of 108]; P ¼.013). At 24 months, an increase in aneurysm sac volume was observed in 47% of patients in the nonembolized cohort (21 of 45), compared with 26% of patients in the embolized cohort (13 of 51; P ¼.03). No aneurysm ruptures or aneurysm-related deaths were observed in either group. One patient in the embolization group developed mesenteric ischemia and ultimately died. Conclusions: Preoperative embolization of the IMA was associated with reduced incidences of type II endoleak, aneurysm sac volume enlargement at 24 months, and secondary intervention. ABBREVIATIONS AAA = abdominal aortic aneurysm, EVAR = endovascular aneurysm repair, IMA = inferior mesenteric artery From the Departments of Interventional Radiology (T.J.W., S.C., A.M.F., E.K., F.S.N., R.A.L.) and Vascular Surgery (S.H.E., P.L.F., M.L.M.), Mount Sinai Medical Center, One Gustave L. Levy Pl., Box 1234, New York, NY Received May 17, 2012; final revision received and accepted September 19, Address correspondence to R.A.L.; robert.lookstein@mountsinai.org From the SIR 2012 Annual Meeting. R.A.L. is a paid consultant for Medrad (Warrendale, Pennsylvania) and Cordis Cardiac (Bridgewater, New Jersey). None of the other authors have identified a conflict of interest. & SIR, 2013 J Vasc Interv Radiol 2013; 24: Since it was first described more than 20 years ago, endovascular aneurysm repair (EVAR) has become firstline therapy for abdominal aortic aneurysms (AAA) (1,2). The EVAR 1 trial (3) produced the first data from a randomized controlled trial and demonstrated decreased 30-day mortality and aneurysm-related deaths with EVAR compared with open repair. This benefit was balanced against higher complication rates, notably endoleaks, and an increased need for secondary interventions (3). An endoleak, defined as persistent blood flow in the aneurysm sac external to the endograft, can broadly be broken down into high-pressure and low-pressure endoleaks (4). Type I and type III endoleaks are high-pressure leaks, for which secondary intervention is widely advocated. Type II and type IV endoleaks are more controversial, and the appropriate follow-up and need for secondary intervention is a topic of debate (5).
2 50 Preoperative IMA before EVAR Ward et al JVIR The principal indication for secondary intervention after EVAR is continued aneurysm sac enlargement, with intervention performed to reduce the risk of rupture. In a review of 10,228 patients by Schanzer et al (6), the presence of an endoleak on postprocedural imaging was found to be the primary predictive factor for aneurysm sac enlargement. In a review of 270 cases of AAA rupture after EVAR reported by Schlösser et al (7), the presence of an endoleak was the primary reported cause in 160 of the 235 cases in which the cause of rupture was described, with type II endoleaks responsible for 23 of the 235 ruptures. The incidence of type II endoleak after EVAR ranges from 8% to 45%, with most series reporting a high rate of spontaneous resolution: 40% 67% (8 15). Studies stratified by anatomic factors have demonstrated even higher rates of type II endoleak in certain populations, with 67% of patients with greater than six patent lumbar vessels and a patent inferior mesenteric artery (IMA) found to have a type II endoleak on follow-up (16). Preoperative embolization of aortic side branches, including patent lumbar arteries and IMAs, has been previously investigated as a method to decrease this high incidence of type II endoleak (17 19). Given the significant contribution of the IMA to the formation and maintenance of type II endoleak, as well as the relative speed and ease with which the IMA is accessed compared with other aortic side branches, the effect of preoperative embolization of the IMA in patients undergoing EVAR was investigated. MATERIALS AND METHODS All patients underwent EVAR approximately 4 8 weeks after conventional angiography, with the number and type of stent-graft detailed in Table 1. All data concerning these procedures, as well as follow-up and rates of repeat intervention, were prospectively entered into an endovascular database at the performing institution. The institutional review board approved the protocol for EVAR in all Table 1. Stent-grafts Used No Stent (n ¼ 108) (n ¼ 158) P Value Excluder 47 (44) 91 (58).024 Talent 34 (31) 46 (29).96 Zenith 1 (1) 8 (5).067 Endurant 1 (1) 6 (4).15 AneuRx 21 (19) 7 (4) o.001 Aptus 2 (2) Fortron 2 (2) Values in parentheses are percentages. Manufacturers are as follows: Excluder (W.L. Gore and Associates, Flagstaff, Arizona); Talent, Endurant, and AneuRx (Medtronic, Minneapolis, Minnesota); Zenith (Cook, Bloomington, Indiana); Aptus (Lumbard, Tempe, Arizona); and Fortron (Cordis, Bridgewater, New Jersey). patients and the retrospective review of the patient s records for the present study. Patients Over a 10-year period at a single tertiary referral center, 108 patients with AAAs and a patent IMA visualized on preprocedural computed tomographic (CT) angiography and subsequent conventional angiography underwent preoperative IMA embolization. The patients who underwent embolization were compared with 158 consecutive patients with a patent IMA visualized on preprocedural CT angiography but not on conventional angiography. It was postulated that patients with a patent IMA on CT angiography but not conventional angiography had retrograde filling of the IMA via collateral vessels and a stenotic origin that prevented visualization on conventional angiography. As a result, these patients did not have preprocedural IMA embolization. Selected images from preoperative imaging, conventional angiography with IMA coil embolization, and follow-up imaging of a patient is provided in Figure 1. Preoperative patient characteristics (Table 2) including age, sex, and maximum aneurysm diameter were not significantly different between groups. The number of patent second through fifth lumbar arteries observed on preprocedural CT angiography was significantly higher in the IMA embolization group (mean, 7.0 [range, 2 8] vs 6.3 [range 2 8]; P o.001), and mean follow-up duration was longer (mean, 985 d [range, 8 3,343 d] vs 645 d [range, 4 1,819]; P o.001). Patients with type I and type III endoleaks were excluded, as the effect of patency or embolization of the IMA with respect to type II endoleak, aneurysm sac volume, and need for secondary intervention were the clinical outcomes of interest. CT Angiography Preoperative CT angiography was performed in all patients. Helical images were obtained from the diaphragm through the femoral heads before and after intravenous bolus administration of Isovue 300 (iopamidol injection 61% [Bracco Diagnostics Inc, Princeton, New Jersey]) at a rate of 4 ml/s for a total volume of 100 ml. Diameter measurements in the axial plane were made at the level of the renal artery origins, maximum aortic diameter, and common iliac artery bifurcations. Sagittal and coronal images were reconstructed to grossly assess the feasibility of EVAR, including angulations of the aorta and patency of renal and mesenteric arteries. Diameter measurements were made by one of six board-certified radiologists with Certificates of Added Qualifications in vascular and interventional radiology. Pre- and postoperative CT angiography was performed with multislice scanners (Siemens, Erlangen, Germany), reconstructed with volume measurements on Vitrea software (Vital Images, Plymouth, Minnesota), and read by interventional radiologists (routine protocol, 2.5-mm thin axial slices with 0.6-mm spacing).
3 Volume 24 Number 1 January Figure 1. Three-dimensional reformatted image (a) from a preoperative CT angiogram. (b) Anteroposterior view from calibrated aortography in the same patient demonstrates a patent IMA (arrow). (c) Selective angiogram of the IMA with the left colic artery identified (arrow). (d) Selective angiogram of the IMA performed after coil embolization. Three-dimensional reformatted (e) image at 2-year follow-up CT angiogram. Aneurysm sac volume measurement on preoperative (f) and 2-year follow-up (g) CT angiograms, measured to be cm 3 and 92.1 cm 3, respectively. (Available in color online at Table 2. Preoperative Patient Characteristics and Follow-up Characteristic (n ¼ 108) No (n ¼ 158) P Value Age (y) Mean Range Male sex 95 (88) 133 (84).39 Aneurysm diameter (cm) Mean Range Patent lumbar arteries Mean o.001 Range Follow up (d) Mean o.001 Range 8 3, ,819 Values in parentheses are percentages. Conventional Angiography Conventional angiography of the infrarenal abdominal aorta was performed to establish longitudinal measurements before ordering and placing the aortic stent-graft. A standardized protocol was used in all patients and included conventional angiography with a calibrated flush catheter at the level of the renal arteries in the anteroposterior and lateral
4 52 Preoperative IMA before EVAR Ward et al JVIR projections, as well as pelvic angiography in the left and right anterior oblique projections. Detailed protocol has been previously described (20). Postoperative Surveillance Follow-up for all patients undergoing EVAR consisted of an office visit as scheduled by the operating surgeon after discharge, as well as CT angiography at approximately 1 month, 6 months, and then annually. Three-phase CT angiography was performed to detect the presence of endoleak. Postoperative CT angiography consisted of a noncontrast study to assess for calcium in the sac, followed by dynamic and late-phase angiographic assessment of the abdominal aorta. Presence of high-attenuation material on delayed images not corresponding to the location of calcium on the noncontrast images and at least 10 HU higher than on the noncontrast phase was diagnostic of endoleak. Aneurysm volume measurements were made by using a Vitrea three-dimensional cardiovascular imaging workstation (Vital Images) by a single experienced technologist. Enlargement of the aneurysm sac volume was defined as a volume increase of at least 2%, as previously reported surveillance protocols after EVAR have identified a 2% volume increase as a significant endpoint and the degree of volume variability is less than 2% for experienced, well trained three-dimensional technologists (21,22). The follow-up period was defined as the time from endograft implantation to the most recent follow-up CT angiogram. In the initial phase of the study, the first 10 patients were admitted after embolization and underwent sigmoidoscopy the following day to assess for bowel ischemia. All 10 of these patients were asymptomatic, with normal study results. The protocol was then changed to 6-hour observation with sigmoidoscopy to be performed in cases of abdominal pain or nausea. RESULTS All transcatheter embolization procedures of the IMA were successful at achieving stasis of flow in the proximal vessel. The incidence of type II endoleak and need for secondary intervention is provided in Figure 2. Overall, 34% of patients in the preoperatively embolized group (37 of 108) and 49% of patients in the nonembolized group (78 of 158) exhibited a type II endoleak during follow-up (P ¼.015). At 24-month ( 30 d) follow-up CT angiography, patients in the embolized group were significantly less likely to have an increasing aneurysm sac volume compared with those in the nonembolized groups (26% [13 of 51] vs 47% [21 of 45]; P ¼.03). Overall, there was no difference in 24-month volume change in the embolized group versus the nonembolized group ( 16% [range, 62% to 31%] vs 4% [range, 61% to 110%]; P ¼.058). When the volume changes of only enlarging aneurysms were examined, no significant difference was observed between the embolized and nonembolized groups (14% [range, 2% 31%] vs 23% [range, 2% 110%]; P ¼.186). Preoperative embolization of the IMA was associated with significantly fewer secondary interventions than seen in the control group (0.09% [one of 108] vs 7.6% [12 of 158]; P ¼.013; Table 3). Secondary interventions consisted of conventional angiography for transarterial embolization of a type II endoleak, with a description of secondary interventions listed in Table 4. In total, 13 secondary interventions were performed. A type II endoleak was found on conventional angiography in 11 of 13 patients, with coil embolization technically successful in 10 of 11 (91%). No direct sac punctures were performed, based on interventional radiologist preference. Kaplan Meier analysis demonstrated significantly increased freedom from secondary intervention in patients in the IMA embolization group (P o.001; Fig 3). No aneurysm ruptures or aneurysmrelated deaths were observed in either group. Study Endpoints Study endpoints included the incidence of type II endoleak, aneurysm sac volume enlargement at 24 months, and secondary interventions. Statistical Methods Statistical analysis was performed with SPSS software (SPSS, Chicago, Illinois). Preoperative and anatomic continuous variables are reported as means for patients who underwent preoperative IMA embolization and for the control cohort. Incidences of endoleak, aneurysm sac enlargement, and secondary intervention was calculated by Pearson test and Fisher exact test. Freedom from secondary intervention was assessed by using Kaplan Meier analysis, with the log-rank test used to compare subgroups. A P value of less than.05 was considered statistically significant. Figure 2. Percentage of patients in embolized and nonembolized groups with type II endoleak and need for secondary interventions.
5 Volume 24 Number 1 January Table 3. Results in IMA Embolized and Nonembolized Patients prior to EVAR Outcome (n ¼ 108) No (n ¼ 158) P Value Type II endoleak 37 (34.3) 78 (49.4).015 Enlarging sac volume at 2 y 13 of 51 (25.5) 21 of 45 (46.7).03 Volume change (%) All patients Mean Range 62.0 to to Patients with enlarging aneurysms Mean Range 2.0 to Need for secondary intervention 1 (0.9) 12 (7.6).013 Values in parentheses are percentages. Table 4. Secondary Interventions Pt. No. IMA Interval after EVAR (d) Secondary Intervention 1 No 1,021 Transarterial lumbar embolization 2 No 1,624 Diagnostic angiogram, no endoleak identified 3 No 733 Transarterial lumbar embolization 4 No 1,653 Transarterial lumbar embolization 5 No 955 Transarterial lumbar embolization 6 No 1,149 Transarterial lumbar embolization 7 No 899 Diagnostic angiogram, unable to catheterize lumbar endoleak 8 No 1,198 Transarterial IMA embolization 9 No 1,533 Transarterial lumbar embolization 10 No 807 Transarterial IMA embolization 11 No 447 Transarterial lumbar embolization 12 No 967 Transarterial IMA embolization 13 Yes 808 Diagnostic angiogram, no endoleak identified EVAR ¼ endovascular aneurysm repair, IMA ¼ inferior mesenteric artery. Complications According to Society of Interventional Radiology classification of procedural complications (23), there were 10 minor (type B) complications and one major (type F) complication related to embolization. Ten patients reported nonlocalized abdominal pain that resulted in readmission to the hospital within 24 hours after embolization. These patients were afebrile without peritoneal signs or leukocytosis. All patients underwent sigmoidoscopy during their admissions, which was negative for ischemic changes in all cases. All patients reported relief of symptoms after overnight intravenous hydration. One patient had a major complication that resulted in mortality. This patient developed severe abdominal pain and a white blood cell count of 30,000/mL within 12 hours of embolization. The patient underwent an exploratory laparotomy within 24 hours that revealed colonic infarction and a previous extended right hemicolectomy that Figure 3. Kaplan Meier analysis of freedom from secondary intervention (P o.001). Light gray ¼ embolization, black ¼ no embolization.
6 54 Preoperative IMA before EVAR Ward et al JVIR sacrificed the middle colic artery. The patient underwent a left hemicolectomy and died of multisystem organ failure within 72 hours of the index procedure. DISCUSSION Type II endoleaks continue to be a frequent complication after EVAR, with the significance and appropriate management of this finding a subject of much debate. As patency of the IMA has been described as a risk factor for type II endoleak formation after EVAR, preoperative embolization of the IMA has been reported with technical success rates as high as 100% (24,25). The safety profile of the procedure is also favorable, without complications in previously described reports (19,20,25). In our experience, the preoperative embolization of the IMA was associated with a decreased incidence of type II endoleak (34% vs 49%; P =.015). This finding is consistent with findings of Nevala et al (19) in which IMA embolization was also associated with fewer endoleaks. A decreased incidence of an enlarging aneurysm sac volume at 2-year follow-up was also noted after IMA embolization (26% vs 47%; P ¼.03), which was not unexpected given the documented association between endoleaks and aneurysm sac enlargement. The report by Nevala et al (19) found that preoperative embolization of the IMA did not result in significant reductions in aneurysm size compared with a control group. Similarly, in our experience, there was no significant difference (P ¼.058) in volume reduction in the embolized group (16%) compared with the nonembolized group (4%). However, given widespread acceptance of a conservative management approach to type II endoleak, prevention of aneurysm sac enlargement may be a more pragmatic goal than overall aneurysm volume reduction. Conservative management of type II endoleak, including close surveillance to evaluate for aneurysm sac enlargement, has been demonstrated to be safe and costeffective (26,27). Intervention transarterial, percutaneous, or open performed for an enlarging sac is done to prevent continued sac enlargement and reduce the risk of aneurysm rupture. Although the various approaches described here appear to be safe and effective, failure rates approaching 60% have been reported (28,29). The high technical success rate for transarterial embolization of type II endoleaks in the present series (91%; 10 of 11) is concordant with the 88% technical success rate reported by Funaki et al (30). One concern before implementing a widespread preoperative IMA embolization protocol at the study institution was the risk of mesenteric ischemia. Deploying embolization coils proximal to the left colic artery maintained the collateral pathways to the IMA, the arc of Riolan, and the marginal artery of Drummond, thereby minimizing the risk of mesenteric ischemia. In the present series, we saw a small number of patients who described delayed abdominal pain after the procedure. None of these cases had objective signs of mesenteric ischemia, and symptoms resolved after observation and intravenous hydration. Our current belief is that this phenomenon may be related to a transient steal-like syndrome caused by the dilation of collateral vessels to accommodate preferential circulation to the descending and sigmoid colon. Studies by Nevala et al (19) and Muthu et al (31) reported no complications with coil embolization performed at a similar anatomic location. A single patient in the present study had a major complication that resulted in mortality. The patient developed mesenteric ischemia as a result of an inability to form collateral vessels to the left colon secondary to an undisclosed, remote extended right hemicolectomy. Current institutional practice is to not attempt IMA embolization in a patient with any history of colonic resection, colonic interposition, or any procedure that may have interrupted the middle colic artery. If the history is equivocal, a selective superior mesenteric artery angiogram is obtained, with specific attention paid to the middle colic artery. The present study has many limitations; it is retrospective in nature and certain patient characteristics that could contribute to the occurrence of a type II endoleak (ie, hypertension, anticoagulation use) were not available for analysis. There were no prospective uniform criteria to decide which patients would undergo secondary intervention. A trial that randomized patients with patent IMAs on conventional angiography to attempted embolization or no embolization could be performed to address these issues. In conclusion, preoperative IMA embolization in patients with a patent IMA is a safe and technically feasible procedure. In our experience, preoperative embolization of the IMA was associated with reduced incidences of type II endoleak, aneurysm sac volume enlargement at 24 months, and secondary interventions. REFERENCES 1. 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7 Volume 24 Number 1 January White GH, Yu W, May J. Endoleak a proposed new terminology to describe incomplete aneurysm exclusion by an endoluminal graft. J Endovasc Surg 1996; 3: White GH, May J, Waugh RC, Chaufour X, Yu W. Type III and type IV endoleak: toward a complete definition of blood flow in the sac after endoluminal AAA repair. J Endovasc Surg 1998; 5: Baum R, Stavropoulos SW, Fairman RM, Carpenter JP. Endoleaks after endovascular repair of abdominal aortic aneurysms. J Vasc Interv Radiol 2003; 14: van Marrewijk C, Buth J, Harris PL, Norgren L, Nevelsteen A, Wyatt MG. Significance of endoleaks after endovascular repair of abdominal aortic aneurysms: the EUROSTAR experience. J Vasc Surg 2002; 35: Baum RA, Carpenter JP, Tuite CM, et al. Diagnosis and treatment of inferior mesenteric arterial endoleaks after endovascular repair of abdominal aortic aneurysms. Radiology 2000; 215: Gorich J, Rillinger N, Sokiranski R, et al. Leakages after endovascular repair of aortic aneurysm: classification based on findings at CT, angiography, and radiography. Radiology 1999; 213: Back MR, Bowser AN, Johnson BL, Schmacht D, Zwiebel B, Bandyk DF. Patency of infrarenal aortic side branches determines early aneurysm sac behavior after endovascular repair. Ann Vasc Surg 2003; 17: van Marrewijk C, Fransen G, Laheij R, Harris P, Buth J. Is a type II endoleak after EVAR a harbinger of risk? Causes and outcome of open conversion and aneurysm rupture during follow-up. Eur J Endovasc Surg 2004; 27: Fan CM, Rafferty EA, Geller SC, et al. Endovascular stent-graft in abdominal aortic aneurysms: the relationship between patent vessels that arise from the aneurysmal sac and early endoleak. Radiology 2001; 218: Gould DA, McWilliams R, Edwards RD, et al. Aortic side branch embolization before endovascular aneurysm repair: incidence of type II endoleak. J Vasc Interv Radiol 2002; 12: Bonvini R, Alerci M, Antonucci F, et al. Preoperative embolization of collateral side branches: a valid means to reduce type II endoleaks after endovascular AAA repair. J Endovasc Ther 2003; 10: Nevala T, Biancari F, Manninen H, et al. Inferior mesenteric artery embolization before endovascular repair of an abdominal aortic aneurysm: effect on type II endoleak and aneurysm shrinkage. J Vasc Interv Radiol 2010; 21: Axelrod DJ, Lookstein RA, Guller J, et al. Inferior mesenteric artery embolization before endovascular aneurysm repair: technique and initial results. J Vasc Interv Radiol 2004; 15: Bley TA, Chase PJ, Reeder SB, et al. Endovascular abdominal aortic aneurysm repair: nonenhanced volumetric CT for follow-up. Radiology 2009; 253: Caldwell DP, Pulfer KA, Jaggi GR, Knuteson HL, Fine JP, Pozniak MA. Aortic aneurysm volume calculation: effect of operator experience. Abdom Imaging 2005; 30: Sacks D, McClenny TE, Cardella JF, Lewis CA. Society of Interventional Radiology clinical practice guidelines. J Vasc Interv Radiol 2003; 14(suppl):S199 S Velasquez OC, Baum RA, Carpenter JP, et al. Relationship between preoperative patency of the inferior mesenteric artery and subsequent occurrence of type II endoleak in patients undergoing endovascular repair of abdominal aortic aneurysms. J Vasc Surg 2000; 32: Bonvini R, Alerci M, Antonucci F, et al. Preoperative embolization of collateral side branches: a valid means to reduce type II endoleaks after endovascular AAA repair. J Endovasc Ther 2003; 10: Steinmetz E, Rubin BG, Sanchez LA, et al. Type II endoleak after endovascular abdominal aortic aneurysm repair: a conservative approach with selective intervention is safe and cost-effective. J Vasc Surg 2004; 39: Bernhard VM, Mitchell RS, Matsumura JS, et al. Ruptured abdominal aortic aneurysm after endovascular repair. J Vasc Surg 2002; 35: Solis MM, Ayerdi J, Babcock GA, et al. Mechanism of failure in the treatment of type II endoleak with percutaneous coil embolization. J Vasc Surg 2002; 36: Ermis C, Krämer S, Tomcat R, et al. Does successful embolization of endoleaks lead to aneurysm sac shrinkage? J Endovasc Ther 2000; 7: Funaki B, Birouti N, Zangan SM, et al. Evaluation and treatment of suspected type II endoleaks in patients with enlarging abdominal aortic aneurysms. J Vasc Interv Radiol 2012; 23: Muthu C, Maani J, Plank LD, Holden A, Hill A. Strategies to reduce the rate of type II endoleaks: routine intraoperative embolization of the inferior mesenteric artery and thrombin injection into the aneurysm sac. J Endovasc Ther 2007; 14:
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