Figure 88-1. Proposed mechanism of Staphylococcus epidermidis–mediated graft infection.

MICROBIOLOGY

Primary Arterial Infections

For infected aortic aneurysms, blood cultures are negative in approximately one-fourth of subjects.4

Intraoperative cultures are more reliable, although intraoperative cultures may be negative in many

cases due to improper culture techniques or preoperative antibiotic administration that precludes

isolation of organisms.4–7 In other series, up to 40% of infected aneurysms had negative blood and/or

tissue culture.5 The most frequent causative organisms vary by country. Hsu et al. found that 76% of

primary aortic infections in Taiwan were due to Salmonella strains.7 Reports from the United States

show that Staphylococcal species (S. aureus or S. epidermidis) are most prevalent, followed by Escherichia

coli, Streptococcal species, and Salmonella. Anaerobic, mycobacterial, and fungal infections represent rare

causes of arterial infections.4,6 European series are similar to the American experience, as Muller

reported that 30% of infections in his series were related to S. aureus and S. epidermidis.5 In Muller’s

series, Salmonella was the next most frequent isolate, followed by Aspergillus, Enterococcus, Streptococcus,

and E. coli.5 The causative organisms also appear to vary based on the artery involved. Infected femoral

artery aneurysms are rarely true aneurysms, but are infected pseudoaneurysms related to prior

catheterizations or intravenous drug use. Skin flora, such as S. aureus or Streptococcal species, are the

predominant organisms isolated from infected femoral artery pseudoaneurysms.27

Arterial Graft Infections

4, 6 For prosthetic graft infections of the aorta, the causal organism is frequently not identified.2 It is

believed that most aortic graft infections occur as a consequence of intraoperative contamination by

skin flora. Other sources include erosions of the graft into adequate structures and contiguous infections

that cross-contaminate the graft. The main organisms responsible for aortic graft infections are S. aureus

and S. epidermidis, accounting for 30% to 55% of the prosthetic vascular graft infections.2,10,14,15 Other

organisms include Streptococcus, gram-negative organisms, anaerobes, and fungal species.2

Polymicrobial infections are present in one-third of subjects.2 Fungal infections, particularly Candida

species, are most frequently encountered with aortoenteric fistulas (AEF).2 Anaerobic and fungal

infections are also frequently associated with polymicrobial infections and sepsis.2

Prosthetic grafts infections involving the femoral artery are most often related to Staphylococcal

species, which comprised 68% of the infections in one series.16,17 Enterococcal and polymicrobial

infections were less frequent among femoral artery grafts.16,17 Endograft infections are predominantly

caused by Staphylococcal species and other minor skin flora, such as Propionibacterium.14,15 Similarly,

Staphylococcal species predominate in peripheral arterial stent infections, with over 85% of the case

reports attributed to Staphylococcal species.20 In a report on carotid artery prosthetic patch infections,

Mann found that 58% were related to Staphylococcal infection, one-third had an unidentified source due

to negative cultures, and the remainder had gram-negative infections, with one beta-hemolytic

Streptococcal infection.18

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CLASSIFICATION OF ARTERIAL GRAFT INFECTIONS

Arterial graft infections are classified based on the time since implantation, the relationship to a surgical

site infection, and the extent of prosthetic involvement. Bunt’s classification, devised in 1983, describes

prosthetic vascular graft infections according to the anatomic segment of the graft that is infected. A P0

graft infection involves a cavitary graft, such as aortic graft or the aortic portion of an aortobifemoral

graft. P1 infections describe infections of grafts whose entire course is extracavitary, such as a lower

extremity bypass graft infection. A P2 infection occurs when the extracavitary portion of a graft with an

intracavitary origin becomes infected. Infected femoral limbs of aortobifemoral bypass graft represent a

P2 infection. P3 infections are those involving prosthetic patches, such as a carotid patch. Pertinent

descriptive qualifiers include the presence of a graft-enteric erosion, a graft-enteric fistula, or an aortic

stump infection (after removal of an infected aortic graft).28

Early graft infections are defined as those occurring less than 4 months after graft implantation. The

Szilagyi classification system classified early surgical site infections. Szilagyi I and II infections are

superficial infections. Szilagyi III surgical site infections involve either native arteries or vascular graft

material, which is most relevant to vascular surgeons.29 The Szilagyi classification system was modified

by Samson to further distinguish between different types of vascular infections.30 Samson group 1

infections involve only the dermis, whereas group 2 infections extend into the subcutaneous tissues

without graft involvement. Group 3 infections involve the graft, but not the arterial anastomosis. Group

4 infections involve an exposed anastomosis without bacteremia or anastomotic bleeding. Group 5 is the

most serious type of infection, with an exposed anastomosis and associated bacteremia or bleeding.30

Clinical management often varies significantly based on the extent of infection, according to these

classification systems.

DIAGNOSIS

The diagnosis of primary arterial infection or prosthetic graft infection may be difficult due to the

significant overlap of symptoms with other pathologies. While a thorough history and physical

examination are essential, a high index of suspicion is critical to the diagnosis. Delays in diagnosis may

have devastating consequences for the patient. Understanding some of the more common presentations

of arterial infections can facilitate a timely diagnosis.

Common Clinical Presentations

Patients with vascular infections often present with non-specific symptoms of malaise, fever, and pain in

the region of the infected artery or graft, which may be accompanied by elevations in erythrocyte

sedimentation rate (ESR) or C-reactive protein (CRP).6 These symptoms are most commonly associated

with arterial infections caused by more virulent organisms, such as S. aureus, P. aeruginosa, E. coli, or

polymicrobial infections. Arterial infections caused by lower virulence organisms, such as S. epidermidis

or Enterococcus, are often even more indolent and may not be associated with local or systemic signs

and symptoms.31 Peripheral arterial infections (primary or graft infections) may exhibit local symptoms,

such as erythema, swelling, tenderness, or a sinus tract with purulent drainage.31 In contrast, local signs

and symptoms are unlikely with infections of cavitary arteries or grafts.

If a primary arterial infection is suspected, the patient should be queried for potential sources of

infection. Many patients with arterial or graft infections have a history of an antecedent infection, such

as pneumonia or a urinary tract infection.6 A recent gastrointestinal illness may be a source of exposure

to Salmonella.7 Other potential clues include a history or clinical stigmata of intravenous drug use or a

recent invasive procedure, which could provide a mechanism for seeding of a native artery or graft.

Associated medical conditions may be cofactors in the pathogenesis of vascular infections. Any

condition that produces relative immune compromise may predispose to primary arterial or graft

infection. Examples include malignancy, human immunodeficiency virus syndrome, chronic hepatitis,

malnutrition, and conditions that require immunosuppressive medications. Predisposing conditions have

been identified in upto 70% of patients with mycotic aneurysms.4–7 Malignancy is especially relevant

due to the association between Clostridium septicum arterial infections and malignancy.32 Symptomatic

atherosclerosis is important to note since atherosclerotic plaques may become seeded by episodic

bacteremia to create a primary arterial infection.

For patients with a history of a prior bypass involving the femoral artery, occult infections frequently

present with an anastomotic pseudoaneurysm in the groin. Over 60% of femoral pseudoaneurysms are

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ultimately found to harbor an occult infection.33 Mertens found that 74% of patients with infected

infrainguinal bypass grafts presented with a draining wound or sinus.34 Infections with low virulence

organisms, such as S. epidermidis, are less likely to be present with a draining sinus because the

virulence of the organisms is insufficient to incite a vigorous inflammatory response to produce the

sinus tract.31

Graft thrombosis is another clinical presentation for an occult graft infection. Graft thrombosis is

believed to predispose to subsequent graft infection.35,36 The coagulated blood within a thrombosed

prosthetic graft provides a rich media for the microorganisms to proliferate.37 In addition, prosthetic

materials are fomites that may harbor microorganisms. Some authors advocate removing occluded

grafts when performing subsequent revascularization operations or amputations to prevent contiguous

spread from the prior occluded grafts.35,36

Gastrointestinal hemorrhage is a rare, but life-threatening presentation for graft infection that must

be diagnosed expeditiously. Any patient presenting with gastrointestinal hemorrhage that has a history

of prior aortic surgery, especially those with vascular prostheses, must have a rapid evaluation for an

AEF. AEFs often present initially with a “herald bleed,” or a relatively small amount of gastrointestinal

bleeding that temporarily abates prior to fatal exsanguination several hours or days later.37–39 The

mortality rate for AEFs is 30% to 77%. Delay in diagnosis is often a contributing factor among patients

who die from this condition. Approximately 75% of AEFs result from a communication between the

aorta and the third or fourth portion of the duodenum.37 The vast majority of AEFs occur in the setting

of prior surgical or endovascular aortic reconstruction. Rarely AEFs occur as a complication of a primary

aortic infection.40 If a portion of the graft erodes through the adjacent bowel without suture line

involvement, gastrointestinal bleeding results from intestinal mucosal irritation. This phenomenon is

termed “graft-enteric erosion.”41 Graft-enteric erosions are often discovered incidentally during surgery

to excise an infected aortic graft.

Ureteral obstruction can occur due to a mechanical complication during the tunneling of an

aortofemoral limb or as a consequence of the inflammatory reaction associated with an infected

aortofemoral limb. Ureterohydronephrosis is strongly associated with aortic graft infections. Wright et

al. found that the presence of a urologic complication after aortoiliac arterial reconstructions was

associated with a fourfold increase in the risk of graft complications, including pseudoaneurysms, limb

thrombosis, AEFs, and overt graft infections.42 Ureteral complications are typically asymptomatic, so

ureterohydronephrosis is often discovered incidentally during imaging studies for other indications and

should alert the physician to the possibility of a graft infection.

Imaging for Vascular Infection

The history, physical examination, and laboratory findings for primary arterial infection or graft

infections are often nonspecific, so imaging plays a pivotal role in establishing a diagnosis. Although

advances in imaging techniques have improved the sensitivity and specificity significantly, no single

modality is perfect. Confirming a physician’s suspicion of occult infection with a low-virulence organism

remains a challenge in many cases. Understanding the advantages and disadvantages of each imaging

modality will allow the surgeon to choose the most appropriate examination, or combination of imaging

studies, to optimize the diagnostic yield.

Computed Tomography (CT) and Computed Tomographic Angiography (CTA)

CT and CTA are the preferred imaging modalities for suspected aortic graft infections in most centers.

CT is readily available in most hospitals, and standard protocols enable most centers to duplicate the

diagnostic sensitivity achieved at centers of expertise. Contrast allergy, contrast-induced nephropathy,

metal artifact, and radiation exposure are shortcomings of CT, but the benefit outweighs the risk in

most cases. The addition of oral contrast agents can help to define the association with enteric structures

if an AEF is suspected. Findings suggestive of graft infection on CT or CTA include inflammatory

changes in the soft tissues surrounding the graft (Fig. 88-2), thickening of the bowel adjacent to

vascular structures, loss of tissue planes around the artery or graft, and perigraft or periarterial air or

fluid (Figs. 88-3 and 88-4).43,44 The sensitivity and specificity of CT for the diagnosis of aortic graft

infections may be as high as 95% and 88%, respectively,44 although the diagnostic accuracy varies

depending upon the organism and severity of the infection. The sensitivity and specificity for low-grade,

indolent infections may be as low as 55% and 100%, respectively.45,46 The presence of either fluid or air

significantly enhances both the sensitivity and specify of CT scans for detecting late graft infections (>4

months postimplantation).43,44 Early graft infections (<4 months postimplantation) present a particular

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challenge for diagnosis. Perigraft air is a normal finding in the periaortic tissues for 2 months after open

aortic reconstruction and should not be considered indicative of an aortic graft infection.47,48 Similarly,

a small amount of perigraft fluid is normal for 3 months after arterial reconstruction.43 After

endovascular aortic aneurysm repair, Sawhney found that air was visualized in the aneurysm sac,

surrounding the endograft, in 58% of patients on early postoperative CTA.49 The air is introduced

during endograft deployment and dissipates over a period of weeks after surgery.

Figure 88-2. CT scan demonstrating loss of tissue planes around the artery (A), with small foci of air (B) suggesting a mycotic

aneurysm.

Duplex Ultrasonography

Duplex ultrasound offers a relatively safe and inexpensive tool for evaluating native arteries and bypass

grafts for signs of infection. Ultrasound circumvents the risks of contrast allergy, contrast-induced

nephropathy, and radiation associated with CT. The main drawbacks of ultrasound are the lack of

availability in some centers of skilled ultrasound technicians capable of arterial imaging. Overlying

structures, particularly bowel gas and the lungs, and body habitus can also obscure visualization and

limit the efficacy of ultrasound evaluations within the chest or abdomen.43 Findings on duplex

ultrasound that are suggestive of infection include the presence of a pseudoaneurysm, hematoma, soft

tissue masses, and perigraft gas and fluid collections. A “halo sign” surrounding an infected

aortofemoral limb is a hypo-acoustic shadow surrounding the graft that is indicative of perigraft fluid

consistent with graft infection.50

Magnetic Resonance Imaging (MRI)

MRI offers some theoretical advantages over CTA for the diagnosis of vascular infections, including the

avoidance of radiation and contrast-induced nephropathy. There are also clear disadvantages to MRI

that have limited its utility in diagnosing graft infections. MRI studies for graft infection are timeconsuming, and MRI is contraindicated for patients with certain metal implants.47 The sensitivity and

specificity for graft infection is highly variable between institutions. MRI may be as useful as CT scan in

the diagnosis of arterial infections at centers with expertise with MRI for arterial infections. In a study

of 40 patients with suspected arterial graft infections, Shahidi found that the sensitivity, specificity,

positive predictive value, and negative predictive value of MRI were 68%, 97%, 95%, and 80%,

respectively.51 MRI may detect small collections of biofilms, the hallmark of S. epidermidis infections,

which are notoriously difficult to diagnose.47 MRI creates a low-intensity “halo” around infected grafts

on T1

imaging, while also creating a hyperintense signal on T2

-weighted images.47,52 Since gadolinium is

not required, MRI may be useful in patients with chronic renal insufficiency. MRI is plagued by some of

the same limitations as CT in detecting early graft infections since air and fluid are normal findings on

MRI for 2 to 3 months after graft implantation.53

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