Type II endoleak in porcine model of abdominal aortic aneurysm Sergio Diaz, MD,a Matthew R. Uzieblo, MD,a Ketan M. Desai, MD,a Michael R. Talcott, DVM,b Kyongtae T. Bae, MD, PhD,c Patrick J. Geraghty, MD,a Juan C. Parodi, MD,a Gregorio A. Sicard, MD,a Luis A. Sanchez, MD,a and Eric T. Choi, MD,a St Louis, Mo Purpose: The purpose of this study was to develop a reliable in vivo porcine model of type II endoleak resulting from endovascular aortic aneurysm repair (EVAR), for the study and treatment of type II endoleak. Methods: Eight pigs underwent creation of an infrarenal aortic aneurysm, with a Dacron patch with preservation of lumbar branches. An indwelling pressure transducer was placed in the aneurysm sac. After 1 week the animals underwent EVAR with a custom-made Talent endograft. After another week the animals underwent laparoscopic lumbar artery ligation. Abdominal and pelvic computed tomography was performed after each procedure. Aneurysm sac pressure was measured in sedated and awake animals. Results: All eight animals underwent successful creation of an aortic aneurysm and EVAR resulting in exclusion of the aneurysm sac. After creation of the aneurysm the sac mean arterial pressure (MAP) was 72.5 ⴞ 6.1 mm Hg and the sac pulse pressure was 44.8 ⴞ 8.7 mm Hg. Postoperative computed tomography scans demonstrated a type II endoleak from the lumbar branches in all animals. While aneurysm sac MAP (56.5 ⴞ 7.9 mm Hg; P < .01) and pulse pressure (13.6 ⴞ 4.1 mm Hg; P < .01) decreased after EVAR, sac pulse pressure remained, with type II endoleak. All animals underwent laparoscopic lumbar artery ligation, which resulted in further reduction in the sac MAP (38.3 ⴞ 4.6 mm Hg; P < .02) and immediate absence of sac pulse pressure (0 mm Hg; P < .01). Necropsy confirmed the absence of collateral flow in the aneurysm sac, with fresh thrombus formation in all animals. Conclusion: We present a reliable and clinically relevant in vivo large animal model of type II endoleak. (J Vasc Surg 2004; 40:339-44.) Clinical Relevance: We set out to show that aortic aneurysm sac pressurization caused by lumbar arterial flow in the setting of type II endoleak can be reproduced in an in vivo porcine model of endovascular aortic aneurysm repair. Indeed, in this model the aneurysm sac pulse pressure was a sensitive indicator of type II endoleak, correlating well with findings at computed tomography, and lumbar artery ligation eliminated the endoleak, as demonstrated on computed tomography scans and sac pressure measurement. Therefore we believe this in vivo large animal model can be instrumental in the study of many aspects of the physiologic features of type II endoleak.
Since 1991 open abdominal aortic aneurysm (AAA) repair has been gradually replaced by the less invasive endovascular method of aortic aneurysm repair (EVAR).1 EVAR minimizes surgical trauma, the risk for bleeding, and the need for general anesthesia, leading to shorter hospital stay and postoperative recovery.2-4 Despite a high rate of immediate procedural success, enthusiasm for the widespread adoption of EVAR has been tempered by the persistent risk for aneurysm rupture. One of the main concerns is the presence of blood flow outside the graft, or endoleak. Endoleak occurs in a variable percentage of patients after From the Departments of Surgery,a Comparative Medicine,b and Radiology,c Washington University School of Medicine. Supported in part by an internal departmental fund and by an unrestricted research fund from Boston Scientific, Inc. Competition of interest: Dr Sanchez has been paid a consulting fee by Medtronics, Inc. Dr Parodi is a paid consultant to Boston Scientific, Inc. Dr Parodi is also a stockholder of Arteria Inc; Cardioms, Inc; Aptus, Inc; and Vascular Innovations, Inc. Reprint requests: Eric T. Choi, MD, Washington University School of Medicine, Section of Vascular Surgery, 660 S Euclid Ave, Campus Box 8109, St Louis, MO 63110 (e-mail:
[email protected]). 0741-5214/$30.00 Copyright © 2004 by The Society for Vascular Surgery. doi:10.1016/j.jvs.2004.04.003
EVAR (7%-37%).5,6 The most common type of endoleak is persistent collateral flow into the aneurysm sac (type II endoleak), primarily from the inferior mesenteric artery (IMA) or lumbar arteries.7,8 Although the incidence of spontaneous rupture with type II endoleak is rare, there are now several reports of type II endoleak leading to aneurysm expansion9 and even to spontaneous rupture.10 Some authors treat all type II endoleaks promptly,11,12 whereas others treat selectively.13 However, the consensus in the management of type II endoleak among vascular surgeons is that most cases can be observed until there is evidence of aneurysm enlargement.14-16 To address these concerns, experimental models have been developed, from latex models to ex vivo animal models.17-22 While these models have provided much information about the hemodynamics of type II endoleak, at present there is no in vivo model. In this report we introduce the first animal (porcine) model of type II endoleak via lumbar branches after EVAR. We show that all type II endoleaks are associated with pulsatile aneurysm sac pressure, and laparoscopic lumbar artery ligation results in resolution of sac pulse pressure. We believe this large animal model can be instrumental in furthering the understanding and treatment options of type II endoleak after EVAR. 339
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Fig 1. A, Infrarenal aorta exposed. B, Dacron patch is sewn after aortotomy to create an abdominal aortic aneurysm approximately 2.5 cm in diameter while preserving the lumbar branches. Indwelling pressure transducer is implanted into aneurysm sac for postoperative sac pressure measurement. C, Intraoperative angiogram reveals the aneurysm and patent lumbar branches.
METHODS Aneurysm creation. The Animal Studies Committee at Washington University School of Medicine approved all mentioned surgical procedures and experiments. Animals were cared for according to the standards set by the Guide for the Care and Use of Laboratory Animals and the Institute of Laboratory Animal Resources, National Research Council. Eight domestic female pigs (50-70 kg) were used. Three procedures were performed in each animal, with an interval of 1 week between procedures: surgical aneurysm creation, EVAR, and laparoscopic lumbar artery ligation. In addition, each pig underwent abdominal and pelvic computed tomography (CT) under general anesthesia after each procedure, to detect the presence of type II endoleak. Before each procedure the animals were fasted overnight. Intramuscular anesthesia induction consisted of ketamine (2.2 mg/kg), xylazine (2.2 mg/kg), and telazol (4.4 mg/ kg). Isofluorane was given via endotracheal tube for the duration of the procedure. Tidal volume was set at 20 mL/kg, with peak inspiratory pressure of 20 cm of water. Intraoperative monitoring included electrocardiography, pulse oximetry, and determination of end-tidal carbon monoxide. Preoperatively, cefazolin (15 mg/kg) was given. Antibiotic coverage was continued for 5 days after the operation. Postoperatively, analgesia with buprenorphine (0.05-0.1 mg/kg intramuscularly) was given as needed. After clipping the hair, the abdomen was prepared with Betadine scrub and iodine paint. With sterile technique, the peritoneal cavity was accessed via a midline abdominal incision. The abdominal aorta was clamped just below the renal arteries, and above the common iliac arteries and the middle sacral artery, with minimal dissection (Fig 1, A).
Heparin (200 U/kg) was then given intravenously. Lumbar arteries were controlled with vessel loops, with minimal trauma to the vessels, and the IMA was ligated and divided. A longitudinal incision was made on the aorta 2 cm below the renal arteries down to 2 cm below the IMA. In all animals two consecutive levels of lumbar arteries were preserved and incorporated into the aneurysm. The aortotomy was then closed with an elliptic Dacron mesh 4 cm wide, sutured to the edges of the aorta with running 4-0 Prolene, similar to the dog model of AAA previously described.23 A pressure transducer (P4.5; Konigsberg Instruments) was implanted in the aneurysm wall (Fig 1, B), passed through a subcutaneous tunnel to the dorsal surface of the animal, and accessed at the posterior neck. After abdominal and pelvic CT with intravenous contrast medium with the animal under general anesthesia, the animals were allowed to recover, and were given a regular diet the next day. Daily aneurysm sac pressure was recorded with a blood pressure recorder (5600 series; Hewlett-Packard) while the animal was completely awake. EVAR. One week after creation of the AAA the animals were anesthetized with general anesthesia, and a midline neck dissection was made with sterile technique. The left common carotid artery was controlled, and a 12F sheath was placed retrograde. A flush aortogram was obtained with a pigtail catheter to determine the aortic aneurysm anatomy (Fig 1, C). A custom-made Talent endograft (tube endograft; Medtronic) was then deployed infrarenally, excluding the aneurysm. Repeat flush aortography was performed to rule out type I and type III endoleaks. After EVAR the left common carotid artery was ligated. After abdominal and pelvic CT the animals were allowed to
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Fig 2. A, Abdominal computed tomography scan demonstrates excluded abdominal aortic aneurysm with a Talent endograft, the lumen of which contains brightly enhanced aortic blood. Inset, Perigraft pool of contrast medium along with contrast-enhanced feeding lumbar arteries, consistent with type II endoleak. Maximum aneurysm diameter, 27 ⫻ 29 mm (anteroposterior-transverse). Size of endoleak from left lumbar artery branch, 22 ⫻ 16 mm (anteroposteriortransverse). Attenuation measurement of endoleak: 130 Hounsfield units (HU). Attenuation measurement of lumen before administration of contrast medium, 43 HU. Attenuation measurement within graft, 562 HU. B, Computed tomography scan demonstrates absence of perigraft flow associated with clipped lumbar artery branch at its origin, confirming resolution of type II endoleak. C, Corresponding sac pressure tracing reveals resolution of sac pulse pressure after lumbar artery branch ligation.
recover from anesthesia, and daily aneurysm sac pressure measurement was recorded. Laparoscopic lumbar artery clipping. One week after EVAR the animals were taken to the operating room and prepared for laparoscopic surgery under general anesthesia. The retroperitoneum was accessed through a 10-mm incision in the left lateral flank; the incision was extended to the transversus abdominal muscle. A balloon obturator was advanced to the preperitoneal space, and after removal of the obturator sheath the balloon was inflated with saline solution. The preperitoneal space developed was maintained with carbon monoxide insufflation, and two additional 5-mm trocars were inserted to expose the lumbar arteries. All lumbar arteries were then ligated with stainless steel clips and divided at their exit point from the aorta. After CT, sac pressure was measured for the last time, and the animals were sacrificed. Statistical analysis. Analysis of variance and paired, two-tailed t test (Systat) were used for statistical analyses of aneurysm sac pressures, including mean arterial pressure (MAP) and pulse pressure. P ⬍ .05 was considered significant. All data are presented as mean ⫾ SEM.
RESULTS Creation of type II endoleak. Eight pigs successfully underwent creation of an AAA with preservation of lumbar branches at two consecutive levels, and underwent EVAR with a custom-made Talent endograft 1 week later. After EVAR an angiogram confirmed exclusion of the aneurysm without any evidence of types I or III endoleak in all eight animals. Post-EVAR abdominal CT scans demonstrated type II endoleak via lumbar arteries in all animals (Fig 2, A). Aneurysm sac MAP and pulse pressure were measured after each procedure and averaged for comparison. After aneurysm creation the sac MAP was 72.5 ⫾ 6.1 mm Hg and sac pulse pressure was 44.8 ⫾ 8.7 mm Hg. Aneurysm sac MAP decreased significantly (56.5 ⫾ 7.9 mm Hg; P ⬍ .01; Fig 3, A) after EVAR, even in the setting of type II endoleak. Sac pulse pressure also decreased (13.6 ⫾ 4.1 mm Hg; P ⬍ .01) after EVAR, but was persistent in all cases associated with type II endoleak (Fig 3, B). All animals had patent lumbar arteries, at both levels, at EVAR, as demonstrated at intraoperative angiography, and immediately after EVAR, as demonstrated on CT scans.
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Fig 3. A, Averaged aneurysm sac mean arterial pressure after creation of abdominal aortic aneurysm (n ⫽ 8), endovascular aneurysm repair (n ⫽ 8; *P ⬍ .01), and lumbar artery ligation (n ⫽ 8; **P ⬍ .02). B, Averaged aneurysm sac pulse pressure after creation of aneurysm (n ⫽ 8), endovascular aneurysm repair (n ⫽ 8; *P ⬍ .01), and lumbar artery ligation (n ⫽ 8; **P ⬍ .01).
Laparoscopic lumbar ligation. All animals underwent laparoscopic lumbar ligation at two levels as treatment of type II endoleak. In all cases MAP decreased (38.3 ⫾ 4.6 mm Hg; P ⬍ .02; Figs 2 and 3, A), and sac pulse pressure was absent (0 mm Hg; P ⬍ .01) after lumbar ligation (Fig 3, B). Post–lumbar ligation CT scans confirmed the absence of type II endoleak in all animals. Necropsy confirmed the CT findings and demonstrated fresh thrombus formation in the excluded sac, associated with occluded lumbar arteries. DISCUSSION Endovascular management of AAA must remain under scrutiny. While initial uncertainties about graft configuration, material, and perigraft leakage of blood have largely been resolved, type II endoleak remains a persistent problem. Therefore, a clinically applicable in vivo animal model of type II endoleak is imperative. While Sanchez et al23 created AAAs in dogs to study type III endoleak, they did not incorporate the lumbar arteries in the aneurysm creation to address the issue of type II endoleak. To our knowledge, this is the first published report of an in vivo animal model of type II endoleak after EVAR. Using this model we demonstrated that aneurysm sac pressure indeed decreases after EVAR in terms of MAP and pulse pressure (Fig 2), confirming findings in human beings.24,25 Furthermore, in the presence of type II endoleak our model demonstrated the persistence of sac pulse pressure, again
confirming findings in human beings with type II endoleak.26 While this model cannot address some issues, such as the effect of type II endoleak on aneurysm enlargement, it can address a number of important issues pertaining to treatment options when intervention is deemed necessary. In this animal model pulse pressure detection was instant with use of intraoperative sac pressure recording. For example, laparoscopic lumbar ligation resulted in the absence of aneurysm sac pulse pressure determined intraoperatively in all cases and confirmed by the absence of type II endoleak on CT scans. We further noted that there was no transmission of pulse pressure from the Talent endograft to the aneurysm sac despite thrombus in the excluded aneurysm sac. This result is in the setting of acute thrombosis, but long-term studies can be adapted to determine whether chronic thrombosis in the sac can indeed transmit systemic pressure leading to endotension (type V endoleak), as speculated by many investigators.27-29 In all of our animals aneurysm sac pulse pressure resolved with the absence of endoleak, as confirmed at postoperative CT and necropsy. When a decision is made to intervene in a patient with type II endoleak, a variety of options have been reported.14,15,30 For example, coil embolization of collateral vessels has been attempted to thrombose the collateral vessels that cause the persistent endoleak; however, the true efficacy of this approach has not been determined. In a dog model of type III endoleak, Marty et al31 demonstrated
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that coil embolization of the aneurysm sac failed to reduce sac pressure despite the absence of endoleak. Whether coil embolization of branch vessels has a different effect in the setting of type II endoleak remains to be seen. The second most commonly used treatment is injection of biologic or synthetic glue into the aneurysm sac.15 An anecdotal report demonstrated a favorable result leading to cessation of type II endoleak and reduction in aneurysm size.32 However, many surgeons believe that the only definitive therapy for type II endoleak is ligation and division of the aortic branch vessels.33 Therefore we performed laparoscopic lumbar ligation in all animals with type II endoleak. There was immediate resolution of aneurysm sac pulse pressure and absence of type II endoleak at postprocedural CT and necropsy. We believe that this technique is a reliable treatment option for type II endoleak in our animal model. With our model a randomized study can be performed to compare other techniques, including translumbar coil embolization and glue injection, with laparoscopic lumbar ligation before wider use in human beings. Furthermore, with recent complications reported34,35 in association with sac and collateral vessel coil and glue embolization, proper histologic evaluation with a reliable animal model would be prudent. Moreover, this animal model may enhance early training in these methods before use in human subjects. We set out to show that sac pressurization caused by lumbar or IMA flow, as in the setting of type II endoleak, can be reproduced in an in vivo animal model. Indeed, in this model aneurysm sac pulse pressure is a sensitive indicator of type II endoleak, correlating well with CT findings, and lumbar artery ligation eliminated the endoleak, as demonstrated on CT scans and by measurement of sac pressure. Therefore we believe this in vivo large animal model can be instrumental in the study of many aspects of type II endoleak physiology. REFERENCES 1. Parodi JC, Palmaz JC, Barone HD. Transfemoral intraluminal graft implantation for abdominal aortic aneurysms. Ann Vasc Surg 1991;5: 491-9. 2. Moore WS, Matsumura JS, Makaroun MS, Katzen BT, Deaton DH, Decker M, et al. Five-year interim comparison of the Guidant bifurcated endograft with open repair of abdominal aortic aneurysm. J Vasc Surg 2003;38:46-55. 3. Jordan WD, Alcocer F, Wirthlin DJ, Westfall AO, Whitley D. Abdominal aortic aneurysms in “high-risk” surgical patients: comparison of open and endovascular repair. Ann Surg 2003;237:623-9 ; discussion 629-30. 4. Arko FR, Hill BB, Olcott C, Harris EJ JR, Fogarty TJ, Zarins CK. Endovascular repair reduces early and late morbidity compared to open surgery for abdominal aortic aneurysm. J Endovasc Ther 2002;9:711-8. 5. Parodi JC, Ferreira LM, Beebe HG. Endovascular treatment of aneurysmal disease. Cardiol Clin 2002;20:579-88. 6. Ouriel K, Clair DG, Greenberg RK, Lyden SP, O’Hara PJ, Sarac TP, et al. Endovascular repair of abdominal aortic aneurysms: device-specific outcome. J Vasc Surg 2003;37:991-8. 7. Moore WS, Rutherford RB. Transfemoral endovascular repair of abdominal aortic aneurysm: results of the North American EVT phase 1 trial. EVT Investigators. J Vasc Surg 1996;23:543-53. 8. Murphy KD, Richter GM, Henry M, Encarnacion CE, Le VA, Palmaz JC. Aortoiliac aneurysms: management with endovascular stent-graft placement. Radiology 1996;198:473-80.
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9. White RA, Walot I, Donayre CE, Woody J, Kopchok GE. Failed AAA endograft exclusion due to type II endoleak: explant analysis. J Endovasc Ther 2001;8:254-61. 10. Hinchliffe RJ, Singh-Ranger R, Davidson IR, Hopkinson BR. Rupture of an abdominal aortic aneurysm secondary to type II endoleak. Eur J Vasc Endovasc Surg 2001;22:563-5. 11. Resch T, Ivancev K, Lindh M, Nyman U, Brunkwall J, Malina M, et al. Persistent collateral perfusion of abdominal aortic aneurysm after endovascular repair does not lead to progressive change in aneurysm diameter. J Vasc Surg 1998;28:242-9. 12. Steinmetz E, Rubin BG, Sanchez LA, Choi ET, Geraghty PJ, Baty J, 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;39:306-13. 13. Veith FJ, Baum RA, Ohki T, Amor M, Adiseshiah M, Blankensteijn JD, et al. Nature and significance of endoleaks and endotension: summary of opinions expressed at an international conference. J Vasc Surg 2002;35:1029-35. 14. Baum RA, Carpenter JP, Golden MA, Velazquez OC, Clark TW, Stavropoulos SW, et al. Treatment of type 2 endoleaks after endovascular repair of abdominal aortic aneurysms: comparison of transarterial and translumbar techniques. J Vasc Surg 2002;35:23-9. 15. Haulon S, Tyazi A, Willoteaux S, Koussa M, Lions C, Beregi JP. Embolization of type II endoleaks after aortic stent-graft implantation: technique and immediate results. J Vasc Surg 2001;34:600-5. 16. Matsumura JS, Moore WS. Clinical consequences of periprosthetic leak after endovascular repair of abdominal aortic aneurysm. Endovascular Technologies Investigators. J Vasc Surg 1998;27:606-13. 17. Parodi JC, Berguer R, Ferreira LM, La Mura R, Schermerhorn ML. Intra-aneurysmal pressure after incomplete endovascular exclusion. J Vasc Surg 2001;34:909-14. 18. Mehta M, Veith FJ, Ohki T, Lipsitz EC, Cayne NS, Darling RC III. Significance of endotension, endoleak, and aneurysm pulsatility after endovascular repair. J Vasc Surg 2003;37:842-6. 19. Skillern CS, Stevens SL, Piercy KT, Donnell RL, Freeman MB, Goldman MH. Endotension in an experimental aneurysm model. J Vasc Surg 2002;36:814-7. 20. Xenos ES, Stevens SL, Freeman MB, Pacanowski JP, Cassada DC, Goldman MH. Distribution of sac pressure in an experimental aneurysm model after endovascular repair: the effect of endoleak types I and II. J Endovasc Ther 2003;10:516-23. 21. Schurink GW, Aarts NJ, Van Baalen JM, Kool LJ, Van Bockel JH. Experimental study of the influence of endoleak size on pressure in the aneurysm sac and the consequences of thrombosis. Br J Surg 2000;87:71-8. 22. Schurink GW, Aarts NJ, Malina M, van Bockel JH. Pulsatile wall motion and blood pressure in aneurysms with open and thrombosed endoleaks: comparison of a wall track system and M-mode ultrasound scanning; an in vitro and animal study. J Vasc Surg 2000;32:795-803. 23. Sanchez LA, Faries PL, Marin ML, Ohki T, Parsons RE, Marty B, et al. Chronic intraaneurysmal pressure measurement: an experimental method for evaluating the effectiveness of endovascular aortic aneurysm exclusion. J Vasc Surg 1997;26:222-30. 24. Treharne GD, Loftus IM, Thompson MM, Lennard N, Smith J, Fishwick G, et al. Quality control during endovascular aneurysm repair: monitoring aneurysmal sac pressure and superficial femoral artery flow velocity. J Endovasc Surg 1999;6:239-45. 25. Chuter T, Ivancev K, Malina M, Resch T, Brunkwall J, Lindblad B, et al. Aneurysm pressure following endovascular exclusion. Eur J Vasc Endovasc Surg 1997;13:85-7. 26. Baum RA, Carpenter JP, Cope C, Golden MA, Velazquez OC, Neschis DG, et al. Aneurysm sac pressure measurements after endovascular repair of abdominal aortic aneurysms. J Vasc Surg 2001;33:32-41. 27. White GH, May J, Petrasek P, Waugh R, Stephen M, Harris J. Endotension: an explanation for continued AAA growth after successful endoluminal repair. J Endovasc Surg 1999;6:308-15. 28. Malina M, Lanne T, Ivancev K, Lindblad B, Brunkwall J. Reduced pulsatile wall motion of abdominal aortic aneurysms after endovascular repair. J Vasc Surg 1998;27:624-31. 29. Pacanowski JP, Stevens SL, Freeman MB, Dieter RS, Klosterman LA, Kirkpatrick SS, et al. Endotension distribution and the role of
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thrombus following endovascular AAA exclusion. J Endovasc Ther 2002;9:639-51. Conner MS III, Sternbergh WC III, Carter G, Tonnessen BH, Yoselevitz M, Money SR. Secondary procedures after endovascular aortic aneurysm repair. J Vasc Surg 2002;36:992-6. Marty B, Sanchez LA, Ohki T, Wain RA, Faries PL, Cynamon J, et al. Endoleak after endovascular graft repair of experimental aortic aneurysms: does coil embolization with angiographic “seal” lower intraaneurysmal pressure? J Vasc Surg 1998;27:454-61; discussion 462. Martin ML, Dolmatch BL, Fry PD, Machan LS. Treatment of type II endoleaks with Onyx. J Vasc Interv Radiol 2001;12:629-32. Wisselink W, Cuesta MA, Berends FJ, van den Berg FG, Rauwerda JA. Retroperitoneal endoscopic ligation of lumbar and inferior mesenteric
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arteries as a treatment of persistent endoleak after endoluminal aortic aneurysm repair. J Vasc Surg 2000;31:1240-4. 34. Elkouri S, Blair JF, Therasse E, Oliva VL, Bruneau L, Soulez G. Aortoduodenal fistula occurring after type II endoleak treatment with coil embolization of the aortic sac. J Vasc Surg 2003;37:461-4. 35. Bush RL, Lin PH, Ronson RS, Conklin BS, Martin LG, Lumsden AB. Colonic necrosis subsequent to catheter-directed thrombin embolization of the inferior mesenteric artery via the superior mesenteric artery: a complication in the management of a type II endoleak. J Vasc Surg 2001;34:1119-22. Submitted Nov 5, 2003; accepted Apr 5, 2004. Available online May 18, 2004.
