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FDG-PET in Prosthetic Graft InfectionsZohar Keidar, MD, PhD,*,‡ and Samy Nitecki, MD†,‡

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ment of Nuclel.ment of Vaculapaport Facultya, Israel.reprint requeicine, Rambaar@keidar.net

Graft infection following prosthetic vascular reconstruction is an uncommon but severecomplication. Theclinical presentation is often subtle andnonspecific andmayoccur longaftersurgery. Although defining a prosthetic vascular graft infection can be difficult, early diagnosisand treatment are essential for the correct choice of treatment to prevent further complicationsas well as the high morbidity and mortality associated with repeat surgery and removal ofinfected grafts. False-positive results may lead to unnecessary surgery while failure todiagnose graft infection may have life-threatening sequels. Scarce literature that is currentlyavailable regarding the role of 18F-labeled fluorodeoxyglucose imaging for assessment ofvascular graft infection suggests that thismodalitymay represent reliable noninvasive imagingmodality in this specific clinical setting. PET/CT increases the test specificity and thusimproves diagnostic accuracy. The precise anatomic localization of increased 18F-labeledfluorodeoxyglucose PET/CT enables accurate differentiation between graft and adjacent softtissue infection leading to more accurate diagnosis and subsequent optimized therapeuticstrategy.Semin Nucl Med 43:396-402 C 2013 Elsevier Inc. All rights reserved.

Vascular grafts replace or bypass occluded or diseasedblood vessels of small, medium, and large sizes to

maintain their function of oxygen supply to their specificterritory. Autogenous vascular grafts are taken from a patient'svessels in another region, most commonly the long saphenousvein. Artificial vascular prostheses are produced from bio-logical, synthetic, or biosynthetic materials. Biological implantsmay be either allografts, for example, human blood vesselssuch as cadaveric blood vessels and human umbilical veins, orxenografts, such as bovine carotid and mammary arteries.Synthetic grafts are made of either Dacron or polytetrafluoro-ethylene (PTFE). Dacron is mainly used in large vessels such asat aortic and aortoiliac surgery, whereas PTFE is utilized formedium-sized vessels such as femoral, popliteal, and tibialarteries. Dacron polyester grafts are very susceptible toinfections as bacteria can adhere to this material. Therefore,in recent years, Dacron grafts are coated with collagen, toreduce blood loss, and with antibiotics, to prevent infection.PTFE grafts are most commonly used for peripheral implants

$-see front matter & 2013 Elsevier Inc. All rights reserved.i.org/10.1053/j.semnuclmed.2013.04.004

ear Medicine, Rambam Health Care Campus, Haifa,

r Surgery, Rambam Health Care Campus, Haifa, Israel.of Medicine, Technion—Israel Institute of Technology,

sts to Zohar Keidar, MD, PhD, Department of Nuclearm Health Care Campus, Haifa, Israel. E-mail:

and are mainly used above the knee to avoid kinking at theknee joint. However, when dealing with critical limb ischemiawithout an autologous bypass option, a PTFE graft is fashionedbelow the knee. Occlusion of the lumen can occur because ofan ingrowth healing process (intimal hyperplasia) or progres-sion of the atherosclerotic disease. Bleeding at the suture lineduring and after implantation may cause seroma, a further sitefor potential infection. Autogenous grafts are the mainstay ofvascular surgery. Artificial grafts are inserted when autogenousvessels are unavailable or too large to be implanted in smalldiameter vessels. The most common complications associatedwith vascular graft insertions are occlusion, distal emboli,infection, and true and false aneurysms at the site of theanastomosis. Late complication in a cavity is erosion intoadjacent structures. Infection of biological or prostheticvascular grafts can have severe outcomes, ranging from lossof limb to death.1,2

Vascular Graft Infection—Frequency, Pathogenesis,Clinical Symptomatology, andDiagnosisVascular graft infection is a severe complication followingreconstructive surgery.Graft infection is rare,with an incidenceranging between 1% and 6%. Infection is caused either at the

FDG-PET in prosthetic graft infections 397

time of surgery, during procedures involving the inserted graft(such as revision or catheterization), or through involvementfrom an adjacent soft tissue focus. Late contamination in casesof bacteremia and sepsis has also been reported.3 The reasonsfor graft infection include patient-related, procedure-related,and pathogen-related factors.4-8 Patient-related factorsinclude overweight, diabetes, malignancy, immunodeficiency,a remote infective or necrotic site, renal or heart failure, and oldage. Procedure-related factors include breech in sterility,emergency “redo” surgery, prolonged procedures, recentarterial injection at the surgical field, postoperative hematoma,seroma or pseudoaneurysm, and soft tissue or wound infec-tion. The greatest risk for graft infection is an emergency redooperation on a patient with severe comorbidities. The patho-genesis of infection is by bacterial adhesion to the graft andcolonization. As the operative site heals, the graft becomes wellincorporated into the surrounding tissue and its vulnerabilityfor infection decreases.4,5,7-10

Typically, graft infection is a late complication occurringseveral months following the operation andmost infections arediagnosed after at least 4 months after surgery. Diagnosis ofgraft infection less than 4 months following surgery isconsidered an early appearance.The incidence varies with the location of the graft, lower in

the abdomen and higher for implants below the inguinalregion and into the lower extremities. Once it occurs, vasculargraft infection harbors poor prognosis. Delay in diagnosis andtreatment is deleterious and may result in limb loss or evendeath in more than 50% of patients for a morbidity andmortality ranging between 20% and 75%.6,11-15 Infection canoccur despite sterile conditions andmeticulous handling of thegraft during operation and even when prophylactic antibiotictreatment is administered. Graft infection is more common inthe inguinal region after aortobifemoral or femoropoplitealbypass. The leading cultured pathogens are Staphylococcusaureus, present in 25%-50% of the cases, and coliforms.Graft infection harbors anastomotic dehiscence and arterialrupture because of the release of destructive endotoxinssuch as proteases and elastases.5,7-9 Bacterial eradication isimpossible in the vastmajority of cases because of developmentof resistive strains and difficulty of antibiotic agents toreach and act at the infection site. The clinical presentationof vascular graft infection is variable. On one hand, presenta-tion may be subtle and difficult to diagnose especiallywith intracavitary or deeply fashioned grafts.9,13 On theother hand, it may be stormy in cases of shallow grafts suchas in the extremities or in the presence of highly virulentpathogens.4,5,7-9,11,13 Patients with aortic graft infection maypresent with unexplained low-grade fever, abdominal pain,ileus, or sepsis. The common presentation of patients withextremity bypasses includes local pain, redness, a palpablelump, and secretion in the area of the surgicalwound. Infectionshould be suspected in the presence of a draining sinus, apulsatile mass with signs of local inflammation, or alocal superficial process with poor response to antibiotics.Evidence of septic emboli or hypertrophic osteoarthropathy israre but when present, is strongly suggestive of vascular graftinfection.

When vascular graft infection is suspected, accurate andearly diagnosis is essential. This further determines the correctchoice of treatment, a decision that is of essential clinicalsignificance. A false-positive diagnosis of vascular graft infec-tion may lead to unnecessary surgery whereas failure todiagnose graft infection is associated with high morbidity.12

The most important and most challenging clinical question inthese patients is to distinguish an infected graft from aninfected wound. The differential diagnosis whether the vas-cular graft is involved within the infectious process or if thesymptoms and clinical picture are related only to an infectedwound represent the most important factor affecting manage-ment of patients with suspected vascular graft infection.Inspection of all surgical sites as well as remote infection sitessuch as venous lines, phlebitis, distal septic emboli, infectedulcer, or osteomyelitis should be performed. Pneumonia andurinary tract infections should be looked for and ruled out.Laboratory examinations for elevated white blood count,increased C-reactive protein, and sedimentation rate shouldbe carried out. In stormy cases with sepsis, wound cultures oreven blood cultures may be tested positive for infection byeither normal incubation growing or by molecular methods(polymerase chain reaction).16Next, imaging studies should beobtained. CT is the most widely used diagnostic modality inpatients with suspected vascular graft infection. Diagnosticsigns for vascular graft infection on CT include the presence oflocal fluid perigraft retention and air bubbles, but thesefindings are present in only about 50% of all cases and maybe normal in the early postoperative period. Signs suggestingan infected prosthesis include thickening of the graft wall,adjacent blurred fat, and soft tissue swelling. The sensitivity ofCT for detection of infected grafts is of 85%-100%. It decreasesin low-grade infection when the incidence of false-negative CTstudies is relatively high. CT images can be of lower quality inthe presence of artifacts caused by metallic clips. False-positiveresults can be related to postsurgical changes with ectopic airencountered for up to 6 weeks following reconstructivesurgery in noninfected cases.3 The presence of an infectedwound, a hematoma, or lymphocele in the vicinity of the graftmay also mask or mimic an infectious process involving thegraft on CT.14,17,18

The role of MRI in the diagnosis of an infected vasculargraft is not clearly defined. As for CT, changes in tissuedensity adjacent to implanted grafts can occur in infectionas well as in the presence of hematoma, lymph collection,or fibrosis and are difficult to differentiate. Infection in itsearly stages is a cause for false-negative studies.14,17 In alimited number of patients with aortic graft infection, theoverall sensitivity of MRI was 68%, associated howeverwith an overall very high specificity of 97%.19

Because morphologic abnormalities in patients with aninfected vascular graft are often nonspecific, the use offunctional or metabolic imaging approach or both hasbeen advocated, aiming to assess the clinical significanceof anatomical findings or to enable early diagnosispreceding the appearance of structural changes. Diagnosisand localization of infection using nuclear medicinetechniques have been described for nearly 3 decades.

Z. Keidar and S. Nitecki398

The most commonly performed procedures usingsingle photon emitting agents are bone scintigraphy(for osteomyelitis), Gallium-67 citrate (Ga-67), andin vitro labeled Tc-99m (Tc) or In-111 (In) leukocytewhite blood cell (WBC) scintigraphy, and studiesperformed with Tc-99m-labeled antigranulocyte mono-clonal antibody Fab' fragments. Radiotracers, regardless ofwhether they are for single photon emission computedtomography (SPECT) or FDG for PET, are primarily anexpression of function and metabolism at the tissue andcellular level.Scintigraphic images lack anatomical detail and can only

define the gross morphopathology. Integrating metabolic andanatomical information using a single hybrid imaging modal-ity, either SPECT/CT or PET/CT, has significantly improvedthe diagnostic confidence and test accuracy.20,21 The wideexperience gained from the use of PET/CT as well as SPECT/CT in the assessment of cancer and other disorders hasdemonstrated that hybrid imaging can confirm the presenceof disease and its localization to a specific organ or region of thebody. In particular, this previously gained experience is nowbeing implemented in the search for the optimal diagnosticmodality for vascular graft infection.Occasionally, exploratory surgery is required to confirm the

diagnosis of graft infection. This approach, however, should beused cautiously because in the case that there is no infection,exploration by itself may result in one. Intact grafts are wellincorporated into the surrounding tissue, covered at times byfibrotic changes. In contrast, infected grafts are free and can besurrounded by turbid fluid, air bubbles, or pus. A poorlyincorporated graft or one that is adherent to neighboringtissues are surgical findings consistent with infection involvingthe vascular implant.Once the graft is infected, bacterial eradication is rarely

possible. The optimal therapeutic option for an infectedvascular graft consists, as a rule, of its surgical removal. Atsurgery an extra-anatomical bypass is established, the graft isremoved, and debridement of the infected and necrotic tissueand reperfusion of the surrounding and distal tissue areperformed in staged procedures in a single session. Recently,in-line graft replacement was practiced with good results.22

Following surgery, antibiotic treatment is administered for aduration that depends on whether and what type of operationhas been performed and the extent of the infection. If surgerycannot be performed treatment of the infected graft requiresprolonged antibiotic coverage guided by blood cultures.12,22,23

The Role of FDG-PET/CT in theAssessment of Vascular GraftInfectionPET is a noninvasivemetabolic imagingmodality that providestomographic data and quantitative parameters of perfusion,cell viability, proliferation, andmetabolic tissue activity. FDG isat present the main PET radiopharmaceutical. FDG, a glucoseanalogue, is taken up by metabolically active cells via glucose

transporters and phosphorylated to 18F-2′-FDG-6 phosphate,but not further metabolized. While being used as themajor PET radiotracer in cancer imaging, FDG was alsoshown to accumulate in infectious processes. Neutrophils,monocytes, macrophages, and activated leukocytes in generalexpress high levels of glucose transporters, especiallyGLUT 1 and 3.24-27

In comparison with other radionuclide imaging techniquesaimed at investigating vascular graft infection, mainly labeledWBCs, FDG imaging has the advantages of having relativelyhigh target-to-background ratios, the studies being completedwithin 1-2 hours after tracer administration, and no bloodhandling being required.

Summary of FDG-PET StudiesPreliminary data on the role of FDG imaging in the diagnosisof vascular graft infection have been initially presented as casereports of single patients.28,29 A single case report hascompared results of CT angiography, FDG imaging, andTc-WBC in a patient with aortic graft infection. The onlypositive test that correctly diagnosed the presence of infectionwas FDG-PET.30 A study designed to prospectively investigatea heterogenic patient population with suspected bone or softtissue infection with FDG and to compare this modality withconventional imaging tests included 7 patients who wereassessed for suspected vascular graft infection.31 It was con-cluded that 2 of these patients had true-positive results and5 had false-negative results on FDG-PET. A single centerexperience in 5 patients with suspected prosthetic graftinfection demonstrated abnormal FDG uptake of varyingintensities. Each of the 3 patients with intense tracer uptakehad an infected implant.32

In an additional study aiming at assessing the value ofFDG-PET in the detection of aortic graft infection in 33patients, Fukuchi et al showed that although highlysensitive, the performance of FDG-PET was hamperedby a lack of specificity. In this study, FDG-PET had a highsensitivity of 91% but a specificity of only 64% ascompared with CT, which had a lower sensitivity of64% but a specificity of 86%.33 In spite of their highsensitivity, nuclear medicine procedures in general andFDG-PET in particular, are limited, as a rule, by the lack ofability to precisely define the anatomical localization ofincreased radiotracer uptake. Correlation of metabolicinformation provided by FDG-PET with anatomical dataof CT or MRI is required to accurately localize the site ofinfection, in particular in cases where the ability toprecisely define structures involved by the infectiousprocess can have critical clinical consequences. Visualside-by-side correlation or coregistration of separatelyperformed PET and CT of the lower limbs, as would bethe case in patients with suspected vascular graft infection,is not accurate enough for localizing a focus of increasedFDG uptake to the arterial prosthesis itself or to thesurrounding soft tissues. The small size and close prox-imity of anatomical structures and the effect of even slight,often involuntary, patient motion with positional changes

FDG-PET in prosthetic graft infections 399

that cause misregistration may lead to inaccurate local-ization and subsequent faulty diagnosis.34

Summary of FDG-PET/CT StudiesHybrid PET/CT imaging is performed in the same setting on asingle device, without changing the patient's position, allow-ing for correct fusion of both sets of metabolic and anatomicaldata. Localization of the lesion is facilitated by the concomitantvisualization of CT on fused PET/CT images, underscoring theability of this imaging technique to overcome the limitationsof FDG-PET for diagnosis of vascular graft infection.34 FDG-PET/CT studies define the presence, intensity, and pattern(focal or diffuse) of increased radiotracer activity on the PETcomponent and precisely determine the localization ofabnormal FDG foci to the graft or to adjacent soft tissues tothe anatomical map on the CT component.A few initial case reports have provided preliminary

evidence suggesting that FDG-PET/CT can have an incre-mental value in the assessment of infected vascular graft.35-37

In a study aimed to retrospectively assess the role of FDG-PET and PET/CT in the diagnosis of patients with fever ofunknown origin, 6 of 7 patients with suspected graft

Figure 1 A 53-year-old male who underwent stent graft insertinvestigation. The patient was admittedwith the clinical suspicioPET/CT axial slices (upper row) demonstrate an increased t(arrowheads) and involving the adjacent vertebral body (arrowFDG uptake in T5 and T6 vertebral bodies (arrow). The correspthese vertebra and a large lytic process involving both vertebraldiagnosis of discitis-osteomyelitis originating from infected stenwas removed.

infection had true-positive results whereas 1 case wasconcluded as false positive. Neither true nor false-negativestudies were found in this limited study group.38 Anothercase report has demonstrated chronic multifocal infection ofan aortoiliac vascular graft, with an infected fistula tract intothe adjacent bone causing chronic vertebral osteomyelitis.This case highlights the utility of 18F-FDG-PET/CT in theimaging of chronically infected vascular grafts and inidentifying potentially lethal complications such as fistulasinto adjacent structures.39 Figure 1 demonstrates vascularstent graft infection causing vertebral osteomyelitis.Keidar et al prospectively evaluated 39 patients with 69

vascular grafts. Forty grafts were suspected of beinginfected with the diagnosis being confirmed in 15. FDG-PET/CT results were true positive in 14, false negative in 1,and false positive in 2 cases, for sensitivity, specificity,positive predictive value (PPV), and negative predictivevalue of 93%, 91%, 88%, and 96%, respectively. Bothfalse-positive results were owing to infected hematomasadjacent to the graft and the false-negative study missedinvolvement of the graft by an infectious process in theadjacent soft tissues.34 An additional study evaluated 25patients with clinically suspected vascular prosthetic

ion for aortic arch aneurysm 2 years before the currentn of infection because of fever and upper back pain. FDG-racer uptake in aortic wall localized to the stent graft). Sagittal slices (lower row) show pathological increasedonded CT slice (lower row, left) demonstrate sclerosis ofsurfaces and the intravertebral space (dashed arrow). Thet graft was confirmed on MRI and the infected stent graft

Z. Keidar and S. Nitecki400

infection assessing the diagnostic accuracy of FDG-PET/CT, specifically the incremental value of fused images andcompared these indices with stand-alone CT. Infection ofthe vascular graft was proven in 15 patients by culture.The performance indices of FDG imaging included asensitivity of 93%, specificity 70%, PPV 82%, and negativepredictive value of 88% as compared with 56%, 57%,60%, and 58%, respectively, for stand-alone CT.40

Figure 2 demonstrates PET/CT diagnosis of vascular graftinfection. Figure 3 demonstrates PET/CT diagnosis of softtissue infection adjacent to the graft but not involving theimplant itself.A prospective study assessed a number of FDG-PET/CT

scans of 76 patientswith 96 vascular prosthetic grafts includingthe presence, intensity (graft-to-blood uptake ratio), andpattern (focal or diffuse) of FDGuptake, as well as the presenceof an anastomotic pseudoaneurysm or of irregular infiltrationboundaries on CT or both. Of all the parameters, only focalFDG uptake on the PET component and irregular graftboundary on CT were significant predictors of infection for aPPV of 97%. However, smooth lesion boundaries and no focalFDG uptake had a PPV of less than 5%. The overall diagnosticaccuracy of FDG-PET/CT for infection was above 95% in 75%of vascular grafts.41 The semiquantitative index defined as thestandardized uptake value (SUV) has not been validated ininfection and should be therefore used with caution. In a smallseries aimed at investigating the diagnostic value of FDG-PET/CT in detecting thoracic aortic prosthetic graft infection,4 patientswere diagnosedwith infected aortic grafts and 5werenot infected. Perigraft SUV(max) measurements were found tobe higher in the infected group than in the noninfected group(11.4 � 4.5 vs 6.9 � 6.4), although the difference was notstatistically significant. According to the receiver operatingcharacteristic analysis, SUV(max) greater than 8 appeared to be

Figure 2 A 54-year-old male, after right iliofemoral and femoropresulting in right above-knee amputation. The patient presentedCT sagittal slices andMIP image (right) demonstrate an increased(dashed arrow). The diagnosis of iliofemoral graft infection waremains (a rim) of the old femoropopliteal bypass were found

the cut-off value in distinguishing the 2 groups with sensitivityand specificity of 100% and 80%, respectively.42

False-Positive, False-Negative, and GraftPhysiological Uptake PatternsIncreased FDG uptake may occur at the sites of postsurgicalinflammatory changes, scar tissue, and native vessels. Based ona single case, an additional hypothesis suggests that increasedFDG uptake can be also the first and very early predictor offuture acute vascular events, specifically acute graft-relatedthrombosis.43 These potential causes for false-positive resultshave to be recognized and differentiated from abnormal FDGuptake within an infected graft. A pattern of linear FDG uptakeof mild to moderate intensity along vascular grafts with noother clinical or laboratory evidence of infection is attributed toa chronic aseptic inflammatory reaction to synthetic grafts,mediated by macrophages, fibroblasts, and foreign body giantcells.44 It was shown that FDG uptake in uninfected prostheticvascular grafts occurs frequently and the uptake can persistover time.45 It is more frequent in recently implanted grafts butcan persist for years after surgery (linear FDG uptake alongnoninfected vascular grafts can be seen in Fig. 3). IncreasedFDG uptake has been described in sites of postsurgicalinflammatory changes, in scar tissue, and native vessels.34,46

A focal pattern of intense abnormal FDG uptake indicates thepresence of a site of infection. Hyperglycemia has beenpreviously considered as one of the main reasons for false-negative FDG studies. However, a recent publication hasindicated that the false-negative rate in patients assessed forthe suspicion of an infectious or inflammatory process is notstatistically significantly different between patients with orwithout diabetes mellitus and with high or normal serumglucose levels at the time of the study.47

opliteal bypass. The femoropopliteal bypass had occludedwith nonhealing right groin wound and fever. FDG-PET/tracer uptake in right pelvis (arrows) localized to the grafts confirmed at surgery and the graft was removed. Theto be noninfected. MIP, maximum intensity projection.

Figure 3 A 56-year-old male with left femoropopliteal bypass graft performed 3 years before the current investigation. Sixmonths ago, the left femoropopliteal graft had occluded and a second vascular graft was implemented parallel to the firstone. The patient was admittedwith the clinical suspicion of infection because of fever and an infected surgical wound at themedial aspect of the left distal thigh. FDG-PET transaxial (upper row, right) andMIP (lower row, right) images show an areaof increased FDGuptake in themedial aspect of the left distal thigh (arrows) localized by PET/CT image (lower row, left) toa soft tissue swelling containing air (arrow) adjacent to the left femoropopliteal graft as seen on CT (upper row, left, dashedarrow). Based on this study, a diagnosis of large infectious process at medial aspect of the left thigh with no graftinvolvement was made. The patient underwent soft tissue debridement and responded rapidly to antibiotic therapy. Inaddition, there was diffuse increased FDG uptake of moderate intensity along both femoropopliteal bypass grafts(arrowheads), consistent with a chronic aseptic inflammatory process in the synthetic graft material. MIP, maximumintensity projection.

FDG-PET in prosthetic graft infections 401

Monitoring Response to TreatmentThere is only scarce information regarding the role of FDGimaging in the follow-up of patients with infection and formonitoring response to treatment, with some evidence sug-gesting that metabolic response to antimicrobial or anti-inflammatory therapy may indicate further clinical response.24

Treatment of an infected vascular graft consists, as a rule, in itssurgical removal. Conservative treatment consisting of inten-sive antibiotic therapy is only considered in highly compro-mised patients who cannot tolerate extensive surgery or inthose patients who have grafts in locations that are difficultto access and impossible to excise.1 Based on current datafrom peer-reviewed literature, FDG imaging cannot be recom-mended for monitoring response to antibiotic treatmentin patients with infected vascular grafts who are treatedconservatively.In summary, successful treatment of an infected vascular

graft consists of its surgical removal. This justifies the highclinical importance of accurate diagnosis of the prosthesisinvolvement by an infectious process. False-positive resultsmay lead to unnecessary major surgery whereas false-negativeresults failing to diagnose graft infection are related with high-

risk morbidity. Combining the anatomical landmarks pro-vided by CT with the presence of increased metabolism onPET has significantly improved the specificity and diagnosticaccuracy of this noninvasive imaging modality, particularly bydecreasing the rate of false-positive cases and has made precisenoninvasive diagnosis of vascular graft infection a reality.48

Well-controlled studies including large numbers of patientsneed to confirm and further validate the diagnostic perform-ance of PET/CT and its role in themanagement of patientswiththe challenging clinical dilemma of vascular graft infections.

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