endovascular aortic aneurysm repair with stent-grafts

Endovascular Aortic Aneurysm Repair withStent-Grafts: Experimental Models CanReproduce EndoleaksSophie Lerouge, PhD, Jean Raymond, MD, Igor Salazkin, MD, Zhao Qin, MSc, Louis Gaboury, MD,

Guy Cloutier, PhD, Vincent L. Oliva, MD, and Gilles Soulez, MD, MSc

PURPOSE: To develop canine aneurysm models that can reproduce type II endoleaks after endovascular aneurysmrepair (EVAR) with stent-grafts.

MATERIALS AND METHODS: A fusiform infrarenal abdominal aortic aneurysm model (AAA) was surgicallycreated with a jugular vein patch, while preserving collateral vessels (n � 3). To allow comparative studies within thesame animal, a bilateral iliac aneurysm model was also constructed with venous patches and surgical re-implantationof the sacroiliac trunk (n � 3). Stent-grafts were implanted by femoral approach at least 2 months later in both aorticand iliac models. Follow-up imaging was performed by Doppler ultrasound (US) and angiography until animals werekilled 3 months after EVAR.

RESULTS: Angiography revealed immediate type II leaks in all cases. Leaks were still present at autopsy 3 monthsafter EVAR in all cases, and were revealed at pre-death angiography in all but one case. At autopsy, leaks werecharacterized by the presence of large endothelialized channels that formed within the thrombus between thestent-graft and the aneurysmal wall.

CONCLUSION: As shown in this pilot study, persistent type II leaks after EVAR can be reproduced in aortic and iliacanimal models. The iliac model can be created bilaterally in the same animal, thus allowing for comparativeevaluation of different therapies. These models could be used to better understand the mechanisms of endoleak, andto assess future developments aimed to improve the outcomes after EVAR.

J Vasc Interv Radiol 2004; 15:971–979

Abbreviations: AAA � aortic aneurysm model, EVAR � endovascular aneurysm repair

ENDOVASCULAR aneurysm repair(EVAR) with stent-grafts is an alterna-

tive to bypass surgery for the treat-ment of abdominal aortic aneurysm(AAA) (1). EVAR is increasingly beingused because of its less invasive natureand the growing prevalence of AAAin an aging population. One of themain drawbacks of this new techniqueis the persistence or recurrence ofblood flow into the aneurysm afterstent-graft placement, called endoleak,which occurs in 10% to 37% of patients(2–4). The most frequent are type Iendoleaks, related to an ineffectiveseal at the graft ends, and type II en-doleaks, associated with retrogradeblood flow from collateral arteries (in-ferior mesenteric or lumbar arteries).Type I and II leaks occur in up to 10%and 10% to 25% of patients treated byEVAR, respectively (5). The mecha-nisms that cause or facilitate the devel-opment of endoleaks are poorly un-derstood. Animal models are essentialto allow a better understanding of

these mechanisms, as well as to pro-vide the appropriate tools to assessnew strategies designed to decreasetheir occurrence. As such, there is aneed to create an animal model thatcan reliably reproduce endoleaks (6,7).The goal of this pilot study was todevelop two canine models that canreproduce type II endoleaks afterstent-graft repair. The first model is anaortic model of sufficient size to im-plant stent-graft devices currentlyused in human AAA. The secondmodel was developed in iliac arteriesallowing comparative studies withinthe same animal.

MATERIALS AND METHODS

Surgical Construction of Aneurysms

AAA model.—All protocols for ani-mal experimentation were approvedby the institutional Animal Commit-

From the Research Center (S.L., Z.Q., I.S., G.C.),Department of Radiology (G.S., J.R., V.O.), and De-partment of Pathology (L.G.), Centre Hospitalier del’Université de Montréal, Notre-Dame Hospital,Montreal, Quebec, Canada. Received March 1, 2004;revision requested April 21; revision received andaccepted April 23. Presented at the 2004 SIR AnnualMeeting. Address correspondence to S.L., ResearchCenter, JA de Seve Building, Notre-Dame Hospital,1560 Sherbrooke East, Montreal, Quebec H2L 4M1,Canada; E-mail: [email protected]

This project has been funded in part by the Plate-forme Technologique du CHUM, Montreal, and by astructuring group grant from Valorisation Recher-che Quebec. It now benefits from the CIRREF grantprogram.

G.S. is a consultant for Medtronic Canada Ltd. andhas identified a potential conflict of interest. None ofthe other authors have identified a potential conflictof interest.

© SIR, 2004

DOI: 10.1097/01.RVI.0000130816.33038.ED

971

tee in accordance with guidelines ofthe Canadian Council on AnimalCare. Mongrel dogs were sedatedwith subcutaneous injection ofacepromazine (0.1 mg/kg; Atravet,Ayerst Veterinary Laboratories,Guelph, ON, Canada), glycopyrrolate(0.01 mg/kg; Sabex Inc., Boucher-ville, QC, Canada), and meperidine(4 mg/kg; Sabex Inc.), and anesthe-tized with intravenous propofol (4mg/kg; Diprivan 1%, AstraZenecaCanada, Montreal, QC, Canada). Ani-mals were ventilated artificially andmaintained with surgical anesthesiaof 2% isoflurane. Postoperative anal-gesia was provided for 3 days by a75 �g Fentanyl skin patch (Durag-esic, Janssen-Ortho Inc., North York,ON, Canada).

AAAs were created in four mon-grel dogs weighing 30 to 40 kg (Fig1a–d). After the death of the first an-imal due to intra-abdominal sepsis,the protocol was changed to includethe systematic use of female dogs,dental cleaning, and preoperative an-tibiotic therapy for 1 week. An exter-nal jugular vein was surgically ex-posed through a skin incision on thelateral surface of the neck, and an 8-to 10-cm-long segment was removedand placed into heparinized salinesolution after proximal and distal li-

gation. The incision was closed inlayers with 3.0 Vicryl. A midlinelaparatomy was performed and theexposure was maintained with me-chanical retractors. Bowels were dis-placed from the abdominal cavityand protected with wet towels. Theparietal peritoneum was dissectedand the abdominal aorta was mobi-lized between renal and common il-iac arteries. Temporary occlusion wasachieved with large vascular clampsthat included the orifice of all lumbararteries. A 10-cm-long aortotomy wasperformed with scalpel and scissors.A venous patch shaped from the ex-ternal jugular vein harvested fromthe same animal was positioned overthe aortotomy and fixed with staysutures. The anastomosis was com-pleted with 4.0 Prolene running su-tures. The operative site was packed,and blood flow restored. After thor-ough check for hemostasis and ab-dominal revision, intestines were re-positioned and soft tissues closed inlayers.

Iliac Model

In this study, three iliac aneurysmswere surgically created in two mon-grel dogs weighing 20 to 25 kg (Fig2a–d). The iliac artery model was con-

structed in a similar fashion to AAA,except for the following details. A lowmidline laparatomy was performed.The peritoneum was dissected overcommon iliac arteries and the vesselswere completely mobilized includingthe sacroiliac trunk. After flow arrest,a longitudinal arteriotomy was per-formed in midsection of the iliac arter-ies. To mimick the effect of a collateral,the sacroiliac trunk was transsectedand sutured to the medial lip of thearteriotomy. A 45 mm patch fashionedfrom the external jugular vein of thesame animal was positioned over thearteriotomy and sutured with contin-uously running 7.0 Prolene. In onedog, a fusiform aneurysm of 35 mm inlength and 12 mm in diameter wascreated. In the second animal, bilateraliliac aneurysms were made shorter (17mm) and larger (17–18 mm).

Endovascular Interventions andCreation of Type II Leaks

Stent-graft implantation was per-formed 8 weeks after surgery. In theAAA model, Talent iliac stent-grafts(12 mm nominal diameter; 115–145mm long with a 13-mm proximal barestent) (Medtronic; Santa Rosa, CA)consisting of a thin Dacron monolayer

Figure 1. Abdominal aortic aneurysm model. Artistic representation showing construction of the AAA (a–c). (continues).

972 • Canine Aneurysm Models Reproducing Endoleaks after EVAR September 2004 JVIR

sutured to a NiTi support, were im-planted with fluoroscopic guidance,an 18-F catheter, and standard clinicalendovascular techniques and surgicalexposition of the femoral artery (n �

3). In the iliac aneurysm model, bal-loon expandable Jostent stent-grafts(diameter, 4–9 mm; length, 48 mm)(Jomed, Rangendingen, Germany),were implanted with fluoroscopic

guidance in the fusiform aneurysms (n� 3). The Jostent stent-graft consists ofa polytetrafluoroethylene graft sand-wiched between two stainless steelstructures. Implants were deployed

Figure 1. (continued) A peroperative photograph shows resulting fusiform aneurysm (d). Angiogra-phy 8 weeks after surgery, immediately before (e) stent-graft implantation (f), showing type II leak 3months later (g).

Lerouge et al • 973Volume 15 Number 9

and expanded at 110% of the nominaldiameter (6 mm).

Follow-up Imaging

Follow-up imaging was performedwith Doppler ultrasound (US) with a10 MHz probe (Vivid 5, GE Vingmed,Horten, Norway) 2 days after surgeryand 48 hours, 3 weeks, and 3 monthsafter stent-graft implantation. Percuta-neous transfemoral angiography wasobtained at the time of stent-graft im-plantation and before animal killing at3 months. Both imaging modalitieswere used for the detection and clas-

sification of endoleaks and for assess-ing graft patency. At angiography,type II endoleaks were defined as re-sidual opacification of aneurysms,through retrograde flow from one ofthe collateral vessels in abdominal an-eurysms (AAA model) or from thesurgically re-implanted sacroiliactrunk (iliac model). In addition to theevaluation of endoleak, Dopplersonography was used to detectchanges in aneurysm size over time,by recording diameters at the proxi-mal, medial, and distal thirds of theaneurysm.

Histopathology

Three months after stent-graft im-plantation, the dogs were killed bybarbiturate overdose immediately af-ter angiography. The aorta and iliacarteries were harvested “en bloc” andfixed in buffered formalin. The Exaktcutting-grinding system (Exakt Gmbh,Norderstedt, Germany) was used toprepare histological slides includingthe tissue/stent-graft interface. Theexplants were frozen in liquid nitro-gen and cut with the Exakt diamondsaw into transverse sections at the

Figure 2. Iliac aneurysm model. Artistic representation of the surgical constructionof bilateral iliac aneurysms (a–c). A peroperative photograph shows resulting fusi-form aneurysms (d) (continues).


proximal and distal necks and proxi-mal, medial, and distal thirds of theaneurysm, which were analyzed andphotographed. Tissues were dehy-drated and embedded in an acrylic

resin (Technovit 7200), cut and pol-ished by successive grinding papersinto 20 to 30 �m sections that werethen stained by hematoxylin and eo-sin. For better identification of cells,

the implant was carefully removedfrom a few transverse sections to pre-pare conventional 3-�m-thick, paraf-fin-embedded slides of the surround-ing thrombus that were stained by

f.e.

g. h.

Figure 2. (continued). Angiograms before (e) and after stent-graft implantation (f–h) in a left iliac aneurysm demonstrate exclusion ofthe aneurysm by the graft (g) but retrograde opacification through implanted collateral (h, arrows).


Movat pentachrome or with immuno-histochemistry. The presence of endo-thelial cells was confirmed by immu-nohistochemistry staining with factorVIII.

RESULTS

In the three animals surviving AAAsurgery, infrarenal abdominal aorticaneurysms measuring 87 mm (�12mm) in length and 20 mm (�2 mm) indiameter were created (Fig 1). Angiog-raphy and Doppler US showed thepresence of type II endoleaks in thesethree dogs immediately after stent-graft implantation. Leaks persisted at3-month angiography in two of threedogs (Fig 1). In the third dog, a leakwas detected at angiography and USat 3 weeks but not at 3 months; how-ever, evidence of a leak was found atpathology after death. In iliac aneu-rysms, type II leaks were identifiedimmediately after EVAR and persisteduntil death in all cases (Fig 2). Allgrafts remained patent. The evolutionof aneurysm diameter over time is de-tailed in the Table. Mean diameterswere obtained by averaging sono-graphic measurements obtained at theproximal, medial, and distal thirds ofthe aneurysm. Aneurysm size in-creased between surgery and stent-graft implantation (mean, 16% �7%).After EVAR, the diameter of AAAsincreased slightly or stabilized,whereas a slight decrease of the iliacaneurysms was observed (Table).Aside from endoleak pockets, tissuebetween the stent-graft and aneurys-mal wall presented heterogeneous ar-

eas of iso- and hypoechoic signal at USexamination.

Incomplete organization into con-nective tissue and presence of largeendothelialized channels were the twomain patterns observed on histologicalanalysis of the surrounding thrombus.Areas of fibrin and red blood cells al-ternated with more or less organizedconnective tissue, generally near thevessel wall, where fibroblasts, actin-positive cells and numerous smallneovessels were present. Very poorlyorganized regions were still presentnear the stent-graft 3 months afterEVAR in the AAA model, whereasbetter tissue organization was seen inthe iliac model. In all aneurysms, oneor several macroscopic “pseudovascu-lar” channels, measuring a few milli-meters in caliber and lined with endo-thelial cells, were observed betweenthe graft and the aneurysmal wall, asconfirmed by factor VIII immunohis-tochemical staining (Fig 3). In the iliacmodel, a connection with the collateralvessel could be confirmed.

Histological analysis also showedthat stent-graft incorporation into amature neointima was limited to re-gions where the implant was close tothe vessel wall (proximal and distalnecks, posterior region near the endsof the aneurysm), while only imma-ture neointima or intraluminal throm-bus were observed at other locationssuch as the middle of the aneurysm.Moreover, neointimal continuity wasnot always present at the ends ofthe stent-grafts, particularly at thetransition zone between the bare and

covered portions of the Talent(Medtronic) stent-graft.

DISCUSSION

The mechanisms leading to en-doleaks after EVAR are poorly under-stood. The development of an AAAanimal model reproducing endoleaksis an important step for the study ofmechanisms and exploration of poten-tial solutions to prevent endoleaks.Large animals are required to studyclinically applicable endovasculartools and their modifications. Aneu-rysm models created by overdilatationwith balloon inflation with/withoutelastase infusion, or by surgery withvenous/arterial patch, have alreadybeen described (6,8–14). However,these have been generally used for de-vice testing, and none have proved toreproduce endoleaks. Recently Pavc-nik et al intended to create chronictype II leaks with a patch from theinferior vena cava on the abdominalaorta with insertion of perforatedstent-graft to create an arteriovenousfistula (6). However, this model didnot reliably produce type II leaks.

This study presents two caninemodels that can reproduce chronictype II endoleaks after EVAR. Theseleaks appear immediately after EVARand depend on circulation establishedby the driving gradient created be-tween systemic and aneurysmal sacpressures, when there is a good sealbetween the stent-graft and the vesselwall at the aneurysmal necks. The au-thors believe that key factors for suc-cessful production of endoleaks here

Aneurysm Size and Changes Over Time in Both Canine Models

Dog Model SG

AngiographicEndoleaks Length of

Aneurysm(mm)

Mean Aneurysm Diameter (mm)(% diameter at surgery)

EVAR Sacrifice Surg EVAR 3 Weeks Sacrifice

1 AAA Animal sacrificed 3 days post-surgery NA NA NA NA2 AAA Talent II II 80 19.6 22.8 (116) 22.6 (115) 21.9 (112)3 AAA Talent II — 100 22.1 29.0 (131) 30.9 (140) 27.3 (123)4 AAA Talent II II 80 18.8 21.7 (116) 24.5 (131) 25.0 (133)5 Iliac LI Jostent II II 35 10.7 12.1 (110) 11.9 (108) 9.7 (88)6 Iliac LI Jostent II II 18 14.0 16.3 (116) — 10.8 (92)7 Iliac RI Jostent II II 17 11.6 12.6 (109) — 10.7 (93)

Note.—Aneurysm diameter was calculated as the average between measurements at the proximal, medial and distal thirds of theaneurysm by ultrasound imaging (in brackets, diameter at follow-up, expressed as the percentage of diameter after surgery).Depending on the model, Talent iliac SG (Medtronic, USA) or Jostent SG (Jomed, Germany) were implanted in the aneurysm.RI � right iliac; LI � left iliac; SG � stent-graft; II � type II endoleaks.


were the length of the patch in theAAA model, which allow keeping sev-eral collaterals patent and the surgicalcreation of a patent “collateral” in theiliac model. An additional consider-ation in the success of the model is thechoice of animal species: aneurysmscreated in canine models tend to per-sist, whereas aneurysms crated in por-

cine models have a propensity tothrombose and heal spontaneously(15). Dogs were also shown to moreclosely reproduce poor incorporationof human implants, whereas pigstended to heal with exuberant neoin-timal formation (7–8,15–17). Amonglarge animals, canine models presentthe best morphological and tissue

healing characteristics (7), as sug-gested by the Ad Hoc Committee ofthe Society for Vascular Surgery andfor Cardiovascular Surgery.

Angiographic endoleaks were ob-served in three of three iliac aneu-rysms and in two of three AAAs at 3months. In the third case of abdominalaneurysm, an endoleak type II was

a. b.

d.c.

Figure 3. Type II endoleaks. Type II endoleaks are structures that present residual flow as shown by color Doppler sonography in (a).They are located outside the stent-graft but within the organized aneurysmal thrombus. (b) A macrophotograph of an aortic transversesection shows a type II endoleak (arrows) as well as endoluminal thrombus (arrowhead). (c) The endoleak is generally found withinorganized connective tissue (Movat’s pentachrome stain; �50 original magnification). (d) It is lined by factor VIII positive cells (arrows)(immunostain for factor VIII; �50 original magnification).


present after implantation, but it wasno longer visible at angiography be-fore death; yet, signs of on-goingblood perfusion and the presence of a“pseudovascular” channel were ob-served at pathology. The authors be-lieve that a small leak was present at 3months but was not detected by an-giography. Computed tomography(CT) scan, which is recognized as themost efficient method (18), may haveallowed its detection. The number ofanimals in this experimentation wastoo small to draw any conclusion onthe variation of AAA diameter duringfollow-up Doppler US.

Histopathological analysis of thesemodels may be helpful to better un-derstand the mechanisms of en-doleaks. Recent studies of specimenretrieved at autopsy or late surgicalconversion after EVAR (19–21) re-ported poor tissue organizationaround the implant, even months oryears after its implantation. The lackof a mature neointima incorporatingthe stent-graft into the vessel wall, thestent-graft being easily separated fromthe aorta and the aneurysmal sac, wasobserved by several authors (19,20).They concluded that attachment ofpresently commercialized stent-graftis purely or mostly mechanical. More-over, the surrounding thrombusseems to be an immature, heteroge-neous, often semi-liquid tissue (19,21).These data suggest that healingaround the implant is insufficient toensure complete exclusion of the an-eurysm from blood flow coming fromthe aorta or collaterals. The pathologyof our animal models at 3 months re-produced some of these findings atautopsy, such as endoluminal throm-bus, poor perigraft organization, andlack of stent-graft incorporation byneointimal growth in the aneurysmalsac.

The presence of large channelslined with endothelial cells within thesurrounding thrombus of all dogs in-dicates that these could play an impor-tant role in the persistence of en-doleaks. Even when the thrombussurrounding the implant is completelyorganized into connective tissue, suchchannels allow persistence of circulat-ing blood into the aneurysm and theirspontaneous thrombosis is not to beexpected. The origin of endothelialcells (intima or vasa vasorum of theaneurysmal pouch, native or collateral

artery, and/or circulating progenitorcells (22,23), etc.) and the mechanismsof formation of these channels remainto be clarified.

Respective advantages of these aor-tic and iliac models include the abilityto test the performance of large com-mercial implants in relation to type IIendoleaks in the former, and the pos-sibility of obtaining comparative bilat-eral studies with paired data in thelatter model. The inability to identify atype II leak at angiography in one ofthe three animals with the aorticmodel represents a limitation. Givenits superior contrast resolution, CTwould be the ideal tool to identify andfollow the presence of leaks in theseanimals. These experimental modelsdiffer from conditions encountered inpatients who develop AAA, such as ir-regular aneurysm necks, calcifiedplaques, and frequent intraluminalthrombus, and their validity and repro-ducibility need to be further assessed.Yet, they are promising tools to improvethe understanding of mechanisms thatcause endoleaks and to evaluate the im-pact of future modifications of stent-graft implants or implantation tech-niques on their occurrence.

Acknowledgments: The authors thankJocelyne Lavoie (endovascular procedureand planification), Hélène Héon (veterinar-ian), and Cédric Schmitt (US image man-agement) for their participation in the ani-mal studies, Guylaine Gevry for herassistance with artwork, and Dr. Guy Allaire,Dr. Lydia Whady, and Robert Spenard, fromthe Department of pathology of CHUM, foraccess to histological equipment.

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