Prosthetic stent graft infection after endovascular abdominal aortic aneurysm repair

Prosthetic stent graft infection after endovascularabdominal aortic aneurysm repairMuhammad A. Sharif, FRCS,a Bernard Lee, FRCS,a Luk L. Lau, MD,a,b Peter K. Ellis, FRCR,b

Anton J. Collins, FRCR,b Paul H. Blair, MD,b and Chee V. Soong, MD,a Belfast, United Kingdom

Objective: The purpose of this report is to discuss the incidence, diagnosis, and management of stent graft infections afterendovascular aneurysm repair (EVAR).Methods: Data were collected from the hospital database and medical case notes for all patients with infected endograftsafter elective or emergency EVAR for abdominal aortic aneurysm (AAA) during the last 8 years in two university teachinghospitals in Northern Ireland. The data included the patient’s age, gender, presentation of sepsis, treatment offered, andthe ultimate outcome. The diagnosis of graft-related sepsis was established by a combination of investigations includinginflammatory markers, labelled white cell scan, computed tomography (CT) scan, microbiology cultures, and postmor-tem examination.Results: Graft-related septic complications occurred in six of 509 patients, including 433 elective repairs and 76emergency endografts for ruptured AAA. Two patients presented with left psoas abscess and were treated successfullywith extra-anatomic bypass and removal of the infected stent graft. Two more patients presented with infected graftwithout other evidence of intra-abdominal sepsis: one underwent successful removal of the infected prosthesis withextra-anatomical bypass, and the other was treated conservatively and died of progressively worsening sepsis. The fifthpatient presented with unexplained fever and died suddenly, with a postmortem diagnosis of aortoenteric fistula andruptured aneurysm. The last patient presented with an aortoenteric fistula, was treated conservatively in view ofconcurrent myelodysplasia, and died of possible aneurysm rupture.Conclusion: This report emphasizes the need for continued awareness of potential graft-related septic complications inpatients undergoing EVAR of AAA. Attention to detail with regard to sterility and antibiotic prophylaxis during stentgrafting and during any secondary interventions is vital in reducing the risk of infection. In addition, early recognition
and prompt treatment are essential for a successful outcome. (J Vasc Surg 2007;46:442-8.)
Prosthetic aortic graft infection after open repair ofabdominal aortic aneurysm (AAA) has been well reportedduring the last 3 decades with a range of clinical manifes-tations and therapeutic options,1 but infective complica-tions involving endografts after endovascular aneurysm re-pair (EVAR) have received little attention. Most EVARsurveillance concentrates on the technical aspects of theprocedure, including endoleaks, device migration, neckdilatation, and rupture.2-5 So far, there is limited knowl-edge on infective complications after EVAR.

Since Chalmers et al6 described the first case of aninfected stent in 1993, more centers have reported graft-related septic complications, usually in the form of singlecase reports. A recent multicenter retrospective study of 65patients with infected endografts7 failed to provide enoughdata for statistical analysis. The purpose of this short seriesis, therefore, to simply examine our experience of infectivecomplications after EVAR at two university centers ratherthan define the broad principles in the management ofinfected endovascular grafts.

From the Department of Vascular and Endovascular Surgery, Belfast CityHospitala; and the Department of Vascular Surgery, Royal Victoria Hos-pitalb.

Competition of interest: none.Reprint requests: Muhammad Anees Sharif, FRCS, Department of Vascular

and Endovascular Surgery, Belfast City Hospital, Lisburn Rd, Belfast BT97AB, UK (e-mail: [email protected]).

0741-5214/$32.00Copyright © 2007 by The Society for Vascular Surgery.
doi:10.1016/j.jvs.2007.05.027
442

PATIENTS AND METHODS

Data were collected from the hospital database for allpatients undergoing elective or emergency EVAR for AAAduring the last 8 years in the only two university teachinghospitals undertaking endovascular stenting in NorthernIreland, with a population of 1.7 million. Patients under-going EVAR were followed up in the vascular clinics at 1, 3,and 12 months and at yearly interval thereafter, unless therewas a reason for earlier follow-up. At each visit, patientsunderwent four views of plain abdominal radiographs (an-teroposterior, lateral, right anterior oblique, and left ante-rior oblique) to assess the mechanical integrity of the stent,contrast-enhanced computed tomography (CT) scan, and ablood test for levels of serum urea, creatinine, and electro-lytes.

Those patients who were reviewed in the follow-upclinic �15 months of the date of data collection wereconsidered to be compliant with the follow-up. If a patientfailed to attend follow-up, the general practitioner wascontacted. All deaths were identified through the hospitalsystem, the general practitioner, and the Registry Office forDeaths in Northern Ireland. In addition, we were notifiedof any patient who became unwell and was admitted toanother hospital for any reason.

In view of a closely linked community, all patients live�100-mile radius from the two hospitals performingEVAR. Therefore, the follow-up arrangements are ade-
quate to identify any graft-related complications in a closely

JOURNAL OF VASCULAR SURGERYVolume 46, Number 3 Sharif et al 443

monitored EVAR population. We were familiar with the sixpatients who presented with infective complications in thisseries. The data collected for these patients included age,gender, comorbidities, type of stent graft used, prophylac-tic antibiotic regimen, adjuvant endovascular interventions,presentation of sepsis, time interval between EVAR andgraft sepsis, treatment offered, and the ultimate outcome.The diagnosis of graft-related sepsis was established by acombination of investigations, including inflammatorymarkers, labelled white cell scan, CT scan, microbiologycultures, and postmortem examination.

Statistical analysis. Kaplan-Meier life-table analysiswas used for freedom from graft-related sepsis using SPSS14.0.1 (SPSS Inc, Chicago, Ill) for Windows (MicrosoftInc, Redmond, Wash). Patients were censored if they wereconverted to open repair, underwent axillofemoral graft,died during the course of follow-up, or failed to complywith the follow-up protocol.

RESULTS

From November 1998 to January 2007, 509 patientsunderwent EVAR for AAA, including 433 elective repairsand 76 emergency endografts for ruptured AAA. Duringthis period, stent graft–related sepsis was encountered in sixpatients, for a total follow-up duration of 968 person-years.The incidence of graft-related sepsis was 6.2/1000 person-years (6/968 � 1000). The average duration of follow-upwas 1.9 years (range, 0 to 8.2 years), with only 15.1%(77/509) lost to follow-up (Table I). The cause of death inpatients undergoing elective and emergency EVAR is sum-marized in Table II. Life-table analysis demonstrating free-dom from graft-related sepsis is illustrated by Kaplan-Meiercurve (Fig 1). The outcomes of the six patients who pre-sented with graft-related sepsis are summarized (Table III).

Patient 1. A 71-year-old man was admitted for elec-tive repair of aortic and bilateral common iliac artery aneu-rysms. The right internal iliac artery was already throm-bosed, but the left was aneurysmal and patent. This vesselwas coil-embolized 3 days before EVAR. The stent graftprocedure was performed uneventfully using a Zenith aor-tobiiliac stent (Cook Europe, Bjaeverskov, Denmark), anda routine follow-up CT scan 1 month after the primary

Table I. Follow-up data for endovascular aneurysmrepair of 509 patients during an 8-year period

Patient category Patients, n (%)

Confirmed deaths 146 (28.7)Continued follow-up* 275 (54)Excluded from follow-up

Converted to open repair 6 (1.2)Converted to axillofemoral bypass 2 (0.4)Unwilling patient 2 (0.4)Patient moved out of province 1 (0.2)Lost to follow-up† 77 (15.1)

*Last clinic visit �15 months.†Last clinic visit �15 months.

repair was satisfactory.

The patient was admitted 6 months later with left flankand back pain, and a pyrexia of 38°C. The leukocyte countwas 9000/mm3, C-reactive protein (CRP) level was 191mg/L, and the erythrocyte sedimentation rate (ESR) was127.0 mm/h. Propionibacterium avidum was found onblood culture, and a labelled white cell scan showed in-creased uptake in relation to the distal part of the main bodyof the stent graft (Fig 2). Intravenous piperacillin/tazobac-tam was started based on sensitivities obtained from bloodcultures. A CT scan showed an area of low density in the leftpsoas muscle with peripheral enhancement suggestive of anacute abscess (Fig 3). Under CT guidance, 250 mL of puswas aspirated from the abscess cavity and a drain was left insitu. The culture of aspirated pus failed to show any growth,however.

Bilateral axillofemoral bypasses were done before theexposure of the aneurysm through a midline approach. Asuprarenal aortic clamp was applied before the pus-filledaneurysm sac was opened (Fig 4). Because the stent graftwas barbed, the upper end was crimped down before it waspulled down. The iliac limbs of the graft were well incor-porated into the native vessel and were removed surgically.Oversewing of aorta and both iliac arteries was done usinga single layer of nonabsorbable sutures, without the needfor double rows, which could weaken the aortic stump. Adrain was left in the aneurysm sac.

Culture of the stent graft and pus did not show anygrowth. Intravenous antibiotics were continued until the

Table II. Cause of death in 146 endovascular aneurysmrepair patients during an 8-year period

Cause of death Patients, n

Elective EVAR repair 108Cardiac 22Malignancy 19Multiple organ failure 14Respiratory failure 12Renal failure 7Stroke 4Bowel ischemia 3Systemic sepsis 3Ruptured AAA after EVAR 3Endograft infection 2Bleeding diverticular disease 1No record available 18

Emergency EVAR for ruptured AAA 38Multiple organ failure 12Cardiac 7Uncontrolled rupture 4Coagulopathy 3Acute renal failure 3Respiratory tract infection 2Stroke 2Type III endoleak 1Bowel ischemia 1Malignancy 1Endograft infection 1No record available 1

EVAR, Endovascular aneurysm repair; AAA, abdominal aortic aneurysm.

patient was discharged at 3 weeks, followed by a further

JOURNAL OF VASCULAR SURGERYSeptember 2007444 Sharif et al

course of oral antibiotics as an outpatient. At 3 months, hisinflammatory markers had returned to normal and afollow-up CT scan was unremarkable. The antibiotics werestopped at this stage.

Patient 2. A 75-year-old man underwent uneventfulendovascular repair of an inflammatory AAA using an aor-tobiiliac Zenith stent graft. The follow-up CT scan at 4months showed a small, well-circumscribed collection an-terior to the left psoas muscle. This yielded thick pus ataspiration, and despite aggressive antibiotic treatment withintravenous piperacillin/tazobactam, it progressively en-larged and extended to the left limb of the stent graft. At 12months after primary repair, he became progressively moreseptic with pyrexia, a leukocyte count of 18,800/mm3,CRP level of 156.0 mg/L, and a blood culture showingStreptococcus constellatus.

At surgery, a supraceliac aortic balloon was positionedin the descending aorta through the transfemoral route.Laparotomy revealed an inflammatory mass surroundingthe neck of the aneurysm. The supraceliac balloon wasinflated before the aneurysm sac was opened and the in-fected graft was explanted. The aortic stump and bothcommon iliac arteries were oversewn. A further abscess waslocated close to the left iliac limb of the graft extending overthe left psoas. The procedure was completed by an axillo-bifemoral bypass after the abdomen was closed and re-draped. In this particular case, the operating surgeon pre-ferred to insert the axillofemoral graft after the removal ofthe infected endograft to diminish bacteremia and prevent

Fig 1. Kaplan-Meier life table analysis demonstrates freedomfrom graft-related sepsis. The number of patients at risk for eachinterval time is shown.

possible infection of the axillofemoral graft.

The periendograft pus grew coliforms and streptococci,and the patient was treated with intravenous piperacillin/tazobactam for 3 weeks postoperatively, followed by afurther course of oral ciprofloxacillin. His postoperativerecovery was complicated by dialysis-dependent renal fail-ure and atrial fibrillation requiring long-term anticoagula-tion. His inflammatory markers returned to baseline at 9months after graft removal (leukocytes 7000/mm3 andCRP �7 mg/L) at which stage his antibiotics werestopped. He remained on dialysis and died 4.5 years laterfrom a massive bowel hemorrhage secondary to diverticulardisease.

Patient 3. A 77-year-old man underwent electiveEVAR for a 6.8-cm AAA using an aortobiiliac Zenith stentgraft. Postoperatively, a type II endoleak from a lumbarartery caused slow sac expansion. By 4 years after theprimary repair, the sac had expanded to 7.9 cm, and heunderwent unsuccessful ultrasound-guided percutaneousthrombin injection into the sac in an attempt to seal theleak. Nine months later, with continued expansion of thesac to 8.1 cm, coil embolization was done for the persistenttype II endoleak. Both adjuvant procedures were done inthe interventional radiology suite without prophylactic an-tibiotic cover.

The patient was readmitted 12 days after the coil em-bolization with a 1-week history of backache and pyrexia.The leukocyte count was 9500/mm3, CRP level was 305.3mg/L, and the ESR was 127.0 mm/h. A CT scan demon-strated soft-tissue thickening and air in the right anterolat-eral aspect of the aneurysm sac suggestive of graft infection.A blood culture grew coagulase negative Staphylococcus,and he was started on intravenous piperacillin/tazobactamand teicoplanin.

He underwent right axillobifemoral bypass and exci-sion of the infected graft with oversewing of the aorticstump and both common iliac arteries. Cultures of the puscollected intraoperatively and the excised graft were nega-tive, and intravenous antibiotics were continued for 2weeks, followed by a further course of oral doxycycline andrifampicin until his CRP level returned to base line. Thepatient made a good recovery, and 12 months later, his CTscan showed no evidence of residual sepsis, with a CRP levelof 14 mg/L and functioning axillofemoral bypass.

Patient 4. A 76-year-old man was admitted 12months after a successful elective EVAR with a Talentaortobiiliac device (Medtronic, Inc, Minneapolis, Minn).He presented with lower abdominal pain, fever, leukocyto-sis (24,000/mm3), and high CRP level (240 mg/L). Threeconsecutive blood cultures grew Staphylococcus aureus, anda CT scan showed marked thickening of the aortic wall atthe neck of AAA, with adjacent lymphadenopathy andstranding of the surrounding fat planes suggestive of in-tense inflammatory response (Fig 5). He had an acutecoronary event during his hospital stay and was consideredunsuitable for graft removal in view of his deterioratinggeneral condition, impaired renal function, and poor car-diac reserve. In view of his comorbidities, he was treated
with intravenous flucloxacillin and oral rifampicin based on

BG, coronary artery bypass grafting; COAD, chronic obstructive airway disease;ccident; OR, operating room; IR, interventional radiology.


the sensitivities from blood culture. Unfortunately, he diedfrom systemic sepsis and progressively deteriorating cardiacfunction at 8 weeks from the diagnosis of his graft infection.A postmortem examination confirmed an intact stent graftwithout evidence of rupture and severe coronary arterydisease.

Patient 5. A 67-year-old man underwent successfulEVAR for a ruptured AAA using an aortouniiliac Talentdevice, an occluder in the contralateral iliac artery, and afemorofemoral bypass. Results of follow-up CT scans at 2and 6 months were unremarkable. He was admitted 10months after with profuse sweating, backache, and a feelingof malaise. The patient’s hemodynamic parameters werestable on admission, with hemoglobin level of 9.4 gm/dL,leukocyte count of 16,800/mm3, CRP level of 185 mg/L,and creatinine level of 269 �mol/L. An urgent CT scanwas arranged, but before this could take place, the patient

Table III. Variables of patients with stent graft–related se

Variable Patient 1 Patient 2

Age at graftinfection

71 75

Gender Male Male MPre-existing risks Angina, NIDDM,

smokingAngina, CABG,

COAD,smoking,hypertension

E

Immunodeficiency Nil Nil NUrgency Elective Elective EDevice Aortobiiliac Aortobiiliac AManufacturer Zenith Zenith ZProcedure setting OR OR OAntibiotic

prophylaxisCefuroxime, 1.5 g Cefuroxime,

1.5 gC

IV single dose Teicoplanin, 400mg

—

Anesthesia General General GAdjuvant

proceduresCoil embolization

of left IIANil T

Presentation Left psoas abscess Left psoasabscess

E

Interval betweenEVAR sepsisdiagnosis

6 months 12 months 6

Microbiologyculture

Propionibacteriumavidum (blood)

Streptococcusspp;coliforms(abscess)

S

Treatment EAB, removal ofinfected graft

EAB, removalof infectedgraft

E

Outcome Survived Survived S

Duration offollow-up fromgraft removal todate/death

3 months, alive 53 months,died ofdiverticularbleeding

3

NIDDM, Noninsulin dependent diabetes; EAB, extra-anatomic bypass; CAIIA, internal iliac artery; MI, myocardial infarction; CVA, cerebrovascular a

suddenly collapsed with massive hematemesis. Resuscita-
Fig 2. Labelled white cell scan shows area of increased uptake in
psis after endovascular aneurysm repair

Patient 3 Patient 4 Patient 5 Patient 6

77 76 67 70

ale Male Male Malex-smoking,prostatism

NIDDM,hypertension,chronic renalimpairment

MI, CVA,smoking,hypertension,COAD

CABG, Crohndisease

il Nil Nil Myelodysplasialective Elective Emergency Electiveortobiiliac Aortobiiliac Aortouniiliac Aortobiiliacenith Talent Talent ZenithR IR IR IRefuroxime,1.5 g

Cefuroxime,1.5 g

Cefuroxime,1.5 g

Cefuroxime,1.5 g

— Teicoplanin,400 mg

Teicoplanin,400 mg

—

eneral General Local Generalhrombininjection,coilembolization

Nil Nil Nil

ndograftinfection

Endograftinfection

AEF AEF

1 months 12 months 10 months(PM)

5 months

taphylococcusepidermidis(blood)

Staphylococcusaureus(blood)

Nil Nil

AB, removalof infectedgraft

Conservative Nil Conservative

urvived Died, systemicsepsis (8 wkspostdiagnosis)

Died,rupture

Died, possiblerupture

5 months,alive

— — —

the distal part of the stent graft (arrowhead).


tion was unsuccessful, and a postmortem examination re-vealed aortic inflammation with adhesions and a fistulouscommunication between the duodenum and anterior aorticwall.

Patient 6. This last patient, a 70-year-old man witha history of Crohn’s disease, has previously been report-ed.8 He underwent endovascular repair using a bifur-cated Zenith stent graft and presented 4 months laterwith epigastric discomfort, fever, and melena. The pres-ence of an aortoenteric fistula (AEF) was confirmed byCT scan and a barium meal. He was treated conserva-tively with intravenous antibiotics in view of his concur-rent aggressive myelodysplastic condition and poorprognosis. A repeat CT scan 8 months after the initialrepair showed complete destruction of the aneurysm sac.Two months later, he suddenly collapsed and died in thehospital. The family declined a request for postmortemexamination.

DISCUSSION

Conventional open repair of AAA has a reported graft

Fig 3. Computed tomography scan shows (arrowheadlarge area of low density anterior to left psoas muscleenhancement suggestive of acute abscess.

infection rate of 0.5% to 3%.9 In this series, the incidence of

stent graft–related sepsis was 6.2/1000 person-years. Du-casse et al7 reported a mean frequency of infection at 0.43%based on 42 cases of infected endografts within an overallexperience of 9739 endovascular procedures. This fre-quency does not represent the true incidence of stent graftinfections, however, because information on completenessof follow-up and deaths is not included. Nevertheless, theDucasse series includes a much larger database from multi-ple centers than our report and thus might be a morereliable source for patient-based incidence of EVAR infec-tion.

So far, the association between adjuvant endovascularprocedures and the risk of stent graft infection is unclear.Two patients in this series underwent an associated endolu-minal procedure. The coil embolization of the left internaliliac artery aneurysm was done 3 days before EVAR inpatient 1, and a left psoas abscess and graft infection laterdeveloped. In this case, it is difficult to ascertain whetherthe coil embolization was responsible for the subsequentevents. However, coil embolization for type II endoleak in

left limb of the aortobiiliac device and (arrowhead b) aadjacent to the left limb of the graft with peripheral

a) theand

patient 3 was clearly followed by a rapid onset of graft sepsis


during the course of the next 10 days, with no previousevidence of graft infection for �5 years.

It was interesting to note that graft sepsis was associatedwith AEF in two patients. Anecdotally, we thought that theexcessive anterior neck angulation in patient 5, with possi-ble extra pressure on the duodenum, could have contrib-uted towards the fistulization; however, the Talent stentgraft used had no intramural barbs. Although the suprare-nal component of the Zenith stent graft has barbs, it isunlikely that it contributed to the formation of an AEF inpatient 6. The AEF is more likely to be related to the

Fig 4. Intraoperative picture shows (arrowhead a) aneurysm sacopened up with pus aspirated from the sac, (arrowhead b) stentgraft inside the sac, and (arrowhead c) a back-bleeding lumbarartery controlled with a suture.

Fig 5. Computed tomography scan shows (arrowhead a) markedthickening of the aortic wall, (arrowhead b) adjacent lymphade-nopathy, and (arrowhead c) stranding of the surrounding fat planessuggestive of intense inflammatory response.

presence of small bowel Crohn’s disease. These interpreta-

tions are unsupported speculations, however, and it is stillmost likely that a primary stent graft infection led eventuallyto erosion of an adherent segment of bowel. Other causesof AEF in association with the aortic stent graft described inrecent literature include stent migration,10,11 erosion of theaorta and duodenum by embolization coils,12,13 fabricrupture,14 inflammatory nature of the aneurysm,15 andbacterial aortitis with chronic duodenal erosion.16

Reports have shown that patients with infected stentgrafts who are managed conservatively with antimicrobialtherapy and percutaneous drainage can still survive.7 In thisseries, however, two of the three patients without surgicaltreatment died of ruptured aneurysm. In patient 5, thedeath was sudden, and treatment options could not beexercised; in fact, the diagnosis of AEF was only made at thepostmortem examination. The third patient treated conser-vatively died of progressive sepsis and cardiac failure. Al-though conservative treatment of high-risk patients hasbeen proposed by some authors, most would agree that theinfected stent graft should be removed if the patient’scondition permits.17

The three patients in the current series who underwentremoval of the infected prosthesis and axillobifemoral by-pass survived. Ducasse et al7 reported 16% mortality withextra-anatomic bypass in this situation. Although the threepatients undergoing graft removal in our series had extra-anatomic reconstruction, recent studies have questionedthe choice of this approach.

The duration of the antimicrobial treatment in patientsundergoing removal of the infected prosthesis in this serieswas guided by serial estimation of CRP level. Because nocurrent guidelines exist on the exact duration of treatmentin this situation, our regimen was based on expert consen-sus involving local microbiologist, vascular surgeons, andthe interventional vascular radiologists. Another change inour protocol for antibiotic prophylaxis was made after thefinding of graft-related sepsis in patient 3, where thrombininjection without antibiotic cover was followed a week laterby graft infection. We now routinely cover all secondaryinterventions in EVAR patients by a single intravenous doseof teicoplanin and cefuroxime.

Our case series has two main limitations. First, thenumber of infected patients still remains very small, butendograft-related sepsis is an uncommon event. In view ofthe small numbers, the contribution of different risk factorstoward the etiology of graft infection is difficult to evaluate.As the duration of follow-up increases beyond the firstdecade, more cases may come to light. Second, this series isinsufficient to provide a comparative data set to allowassessment of the effectiveness of different treatment mo-dalities in endograft infections.

CONCLUSION

The incidence of stent graft–related sepsis is currentlylow. Nevertheless, as more patients are treated by endovas-cular technique, there is an increasing need to be vigilantfor the risk of graft infection. Better appreciation of the
potential risk of stent graft infection and an obsession to


detail in patient preparation and surgical technique, alongwith timely use of appropriate antibiotic regimens duringprimary and secondary interventions, may help to minimizethe risk of graft-infection. A high index of suspicion is alsorequired for diagnosis because the clinical presentationcould be varied. Removal of the infected prosthesis andrestoration of the blood flow to the lower extremities isrecommended when possible.

We offer our greatest appreciation to all the consultantvascular surgeons and interventional vascular radiologists atBelfast City Hospital and Royal Victoria Hospital for con-tributing cases, which led to the successful completion ofthis study. We also thank Patrick Comiskey, Medical Pho-tography Department, Belfast City Hospital, for providingtechnical support in production of the images shown in thisarticle.

AUTHOR CONTRIBUTIONS

Conception and design: MS, BL, CSAnalysis and interpretation: MS, LL, CSData collection: MS, PE, AC, PBWriting the article: MS, CSCritical revision of the article: MS, ML, LL, PE, AC, PB,

CSFinal approval of the article MS, BL, LL, PE, AC, PB, CSStatistical analysis: MSObtained funding: Not applicableOverall responsibility: CS

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Submitted Mar 1, 2007; accepted May 7, 2007.

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Prosthetic stent graft infection after endovascular abdominal aortic aneurysm repair