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

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 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 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.

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 time-consuming, 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

Leukocyte Scintigraphy

Leukocyte scintigraphy may be performed using either ¹¹¹Indium- or ^99mTechnetium-labeled leukocytes to localize infection within the arterial wall or graft. A theoretical advantage of leukocyte scintigraphy is the diagnosis of indolent infections with low-virulence organisms for which the symptoms are most ambiguous. Unfortunately there are numerous pitfalls to this modality. Leukocyte scintigraphy is time-consuming, labor-intensive, and prone to false-positive results due to undesired cross-labeling of platelets that may bind to grafts.^54,55 Uptake of the radionuclide-labeled white blood cells requires intact chemotaxis and a minimum total white blood cell count of 2,000/μL.⁵⁵ The net effect of these issues is that the sensitivity and specificity for tagged white blood cell scanning is highly variable between institutions, with sensitivity and specificity both ranging between 50% and 100%.^51,54,55

Single Photon Emission Tomography (SPECT) Scanning

SPECT scanning, when combined with CT scanning, may enhance the specificity of leukocyte scintigraphy in the detection of vascular infections.^56,57 While there are limited data available at this time, the early results appear promising. Erba recently evaluated SPECT–CT in 55 subjects with suspected vascular graft infections. SPECT–CT reduced the number of false positives by 37%, compared to CT alone. The sensitivity and specificity of SPECT–CT was 100%, which was superior to SPECT or CT alone.⁵⁷

Fluorodeoxyglucose Positron Emitting Tomography (FDG-PET)

FDG-PET utilizes glucose labeled with ¹⁸fluoride, which is utilized by cells proportional to their metabolic activity. Initially, this technique was utilized to detect occult metastases in oncology patients. Recently the protocols have been adapted for the detection of occult arterial infections.^58,59 FDG-PET can be advantageous in diagnosing endograft or peripheral stent infections since the images are less prone to metal artifact. Compared with leukocyte scintigraphy, FDG-PET offers the advantages of shorter examination times, less radiation exposure, higher resolution, and improved interobserver agreement.^60,61 Unfortunately there is a high false-positive rate for diagnosing arterial graft infections because of the inflammatory response associated with prosthetic grafts.⁵⁸ Poor uptake of the FDG-glucose can also yield nonspecific results, which is a limitation of using this test in diagnosing low-virulence infections. While the sensitivity and specificity of FDG-PET alone are inferior to CT scan alone, combining FDG-PET with CT scanning markedly improves the localization of infection and the sensitivity and specificity of the examination. Using the approach, Spacek reported a diagnostic accuracy exceeding 95% in a series of 95 grafts.⁵⁹ For FDG-PET-CT, Bruggink reported a sensitivity, specificity, positive predictive value, and negative predictive value of 93%, 70%, 82%, and 88%, respectively, which was superior to FDG-PET alone. ⁶⁰ Further study is required to define the threshold for a positive FDG scan in the setting of cavitary arterial infections.^61–63 Drawbacks of the fusion technology include longer study times and increased radiation exposure. Furthermore, expertise with FDG-PET-CT techniques is not widely available. Despite these limitations, some authorities foresee the combined modality becoming the study of choice in the future.⁶¹

Adjunctive Diagnostic Modalities

Arteriography, endoscopy, and image-guided biopsy should be viewed as adjunctive diagnostic modalities that have a limited role in diagnosing graft infections. Arteriography may be useful in planning reconstruction. Rarely, an occult AEF can be discovered with angiography by filling of the enteric structure.⁶⁴ Esophagogastroduodenoscopy (EGD) is typically performed to exclude other sources of upper gastrointestinal hemorrhage in a patient with a suspected AEF. EGD was successful in diagnosing AEF in approximately 25% cases in one small series of primary AEFs.⁴⁰ In spite of the low diagnostic yield, the authors recommended endoscopy in hemodynamically stable patients with a suspected AEF because of the devastating consequences of a missed diagnosis. Image-guided biopsy of the fluid or rind surrounding the affected vascular structure has been advocated when the diagnosis of graft infection is equivocal.^65,66 This approach could potentially distinguish between patients with benign early postoperative perigraft gas versus an early graft infection. However, sufficient sampling is difficult to achieve in all cases, as the tissue is often fibrotic and in close proximity to other major vascular structures and bowel.⁶⁶ Further study will be required to clarify the role of this modality in the evaluation of arterial infections.

CONSERVATIVE MANAGEMENT

Primary Arterial Infections

Hsu et al. provided insight on the outcome of conservative management of subjects with primary aortic infections.⁶⁷ Hsu examined 22 subjects with infected aortic aneurysms with perceived contraindications to surgery. The predominant organism in the cohort was Salmonella, with two-thirds of subjects having infections of the abdominal aorta. All subjects received culture-specific intravenous antibiotics for at least 6 to 8 weeks, or until normalization of white blood cell count, daily temperatures, and C-reactive protein levels. After the acute phase treatment, oral antibiotics were continued indefinitely. In Hsu’s series, the inhospital mortality was 50% due to rupture or sepsis. The 1-year survival rate was 32%. Patients with Salmonella infections had a lower aneurysm-related mortality rate than patients with non-Salmonella infections.

Arterial Graft Infections

Calligaro advocated for complete or partial prosthetic bypass preservation in subjects with severe comorbidities precluding surgical repair.⁶⁸ Over a 20-year period, 51 extracavitary grafts (aortofemoral limbs or lower extremity bypasses) were treated with graft preservation and aggressive wound management without surgical graft resection. When wounds were present, aggressive debridement of all necrotic tissue and exudate surrounding the artery was performed. Nine cases utilized adjunctive muscle flaps to aid healing. Povidone–iodine 1% or antibiotic-soaked dressing changes were performed three times a day. With this regimen, 2 of 51 patients (4%) experienced major hemorrhage from the infected graft at 3 and 12 months after presentation. Eleven of the patients (22%) failed the treatment regimen, with nonhealing wounds or recurrent infections requiring total graft excision. Thirty-two subjects (63%) were ultimately treated successfully. Calligaro concluded that conservative management of extracavitary grafts is an acceptable option in the absence of sepsis or hemorrhage, especially when graft excision and revascularization is not feasible due to patient comorbidities. Pseudomonas infections, however, were particularly prone to failure with this regimen.

Building on the early reports of graft preservation therapy, subsequent reports have emerged utilizing vacuum-assisted negative pressure therapy with antibiotics and wound debridement to preserve extracavitary grafts with Szilagyi III wounds.^69,70 Wound healing with these regimens have ranged between 82% and 91% with excellent graft preservation rates.^69,70 Episodes of hemorrhage remain an issue with this approach,⁶⁹ and the failures have been associated with Pseudomonas.^69,70 Based on these reports, it appears that carefully selected patients with early infections involving extracavitary grafts may be treated without surgical graft excision with acceptable results.

Calligaro et al. used a nonoperative approach in six patients with intracavitary graft infections with a hostile abdomen or severe medical comorbidities.⁷¹ All subjects underwent either open or percutaneous placement of drains along the graft with instillation of 10 mL of 1% povidone–iodine in 100 mL of normal saline or antibiotics (neomycin or a cephalosporin) three times a day. All subjects were treated concurrently with culture-directed intravenous antibiotic therapy for 6 weeks, followed by 6 months of oral antibiotic therapy. Of these 6 subjects, only one died due to sepsis. One patient ultimately required total graft excision and survived. The remaining patients (66%) were alive at last follow-up. These authors showed that in highly selected patients, conservative management can have reasonable outcomes. In the absence of larger series, this approach should be reserved for patients who are not reasonable candidates for graft excision.

SURGICAL MANAGEMENT OF AORTIC ARTERIAL AND GRAFT INFECTIONS

Surgical treatment is based upon the central tenets of appropriate resuscitation, preoperative planning, resection of all infected material and tissue, and arterial revascularization. The optimal method of arterial reconstruction remains unresolved, as few direct comparisons between approaches have been published. Based on our extensive institutional experience with a variety of techniques, we have concluded that no single approach is suitable for all patients. We advocate tailoring the treatment algorithm based on each patient’s clinical presentation and the local surgical expertise.

Aortic Infections Presenting with Hemorrhage or Sepsis

A minority of patients present with septic or hemorrhagic shock. For these patients, rapid intravenous access and resuscitation are essential prior to emergent surgery. In the authors’ experience, the complexity of the operations required to manage these patients mandates a rapid CTA to obtain essential anatomic information. It is recognized that some of these patients will have either acute kidney injury or chronic kidney disease, but managing the life-threatening complications of the aortic graft infection outweighs the risk of contrast-induced nephropathy. Ideally, blood and wound cultures are obtained prior to the administration of broad-spectrum gram-positive and gram-negative antibiotic therapy. The surgical approach to managing patients presenting with hemorrhage or sepsis should be individualized based on the patient’s anatomy and the expertise of the surgeons.

Endografting as Bridge Therapy

Endografts are being used with increasing frequency as a method to temporize hemorrhage in patients with aortoenteric or aortobronchial fistulas.^38,39,72,73 When the anatomy permits, endografting may temporarily prevent exsanguination and allow time for resuscitation, medical stabilization, and further investigations to plan definitive surgery.⁷² Endografting should not be viewed as definitive therapy since recurrent hemorrhage occurs in majority of cases without further surgical treatment.^39,73 Definitive surgery should be planned within 2 weeks of endografting, since most episodes of recurrent bleeding occurred greater than 2 weeks after initial endografting.⁷³ The exception to this principle is an aortobronchial fistulae for which endografting may be viewed as definitive therapy.³⁸

Definitive Surgery for AEF

Definitive surgery for an AEF involves resection of the infected graft, repair of the enteric defect, and revascularization of the lower extremities. The most appropriate surgical approach to achieve these goals has been the focus of considerable debate. For decades, the most common approach to AEFs was total graft excision with ligation of the infrarenal aortic stump and extraanatomic bypass.^74–78 In recent years, a variety of groups have touted the merits of in situ reconstruction of the aorta after graft excision, using a variety of conduits. The advantages, disadvantages, and technical details of these approaches are discussed later in the chapter (see “Aortic Infections in the Stable Patient”).

Aortic Ligation and Extraanatomic Bypass for AEFs

In stable patients with a small herald bleed caused by an AEF, Reilly et al. at the University of California-San Francisco advocated staging of the two component operations at an interval of several days to minimize the physiologic impact on the patient.⁷⁵ The first stage of this approach consists of performing an axillobifemoral bypass or bilateral axillary–popliteal bypasses, followed several days later by resection of the infected graft with aortic stump closure. In the patient with ongoing bleeding or hemodynamic instability, a staged approach is not feasible. Reilly reported a 26% mortality rate with the staged approach, compared to 43% for the traditional, nonstaged.⁷⁵ A subsequent study by Seeger reported a 19% treatment-related mortality rate.⁷⁶ In addition to a high mortality rate, this approach is plagued by a significant risk of aortic stump blowout (9%), reinfection of the extraanatomic bypass graft (16%), and major amputation (16%).⁷⁵

In Situ Aortic Reconstruction for AEFs

In response to the sobering results associated with the traditional approach, in situ aortic reconstruction has been touted as a relatively simple and effective alternative.^80–84 Oderich et al. from the Mayo Clinic reported their results using in situ rifampin-soaked grafts in 54 patients with aortic graft-enteric erosions or fistulae.⁸⁰ In their series, operative mortality was 9%, and graft reinfection occurred in 4%. A subsequent multicenter study of 37 patients with AEFs treated with either in situ prosthetic grafts (n = 9), extraanatomic bypass (n = 25), or endografting (n = 3), reported a 30-day mortality rate of 43% for in situ reconstructions.⁸² In that series, 3 of 11 (27%) long-term survivors with in situ grafts developed reinfection of the in situ graft, which was universally fatal.

Alternative conduits for in situ reconstruction for AEFs include cryopreserved aortoiliac allograft and femoral vein. Harlander-Locke et al. published a multicenter experience with 220 patients with aortic graft infections treated with in situ cryopreserved aortoiliac allograft, which included 33 patients with AEFs.⁸³ The reinfection rate in patients presenting with AEFs was 12%. In situ repair with autogenous femoral vein is not appropriate in the unstable patient due to the time required for femoral vein harvest, but may be reasonable in the stable patient with a herald bleed due to an AEF. Valentine reported a 42% mortality rate in 24 patients treated with in situ femoral vein for AEFs and graft-enteric erosions, so femoral vein may not offer any advantage over the alternative conduits for AEFs.⁸⁴

Aortic Infection with Sepsis

Sepsis caused by an aortic infection poses a challenge because temporizing with an endograft is not an option since the septic focus is not eliminated. In unstable patients, CT-guided percutaneous drainage may be a reasonable option for source control if there is a large perigraft fluid collection. In a series of 23 patients with graft infections, Belair et al. found that percutaneous drainage was associated with improved perioperative mortality, compared to surgery alone.⁸⁵ In the absence of a large perigraft fluid collection for percutaneous drainage, graft excision with extraanatomic bypass is the most reasonable approach.

Aortic Infections in the Stable Patient

Preoperative Evaluation

The incidence of coronary artery disease is high in surgical series of arterial infections, especially in subjects with infected endografts.^2,6,14 Thus, a thorough cardiovascular history, physical examination, 12-lead electrocardiogram, and echocardiogram should be obtained to evaluate for heart failure, valvular dysfunction, and pulmonary hypertension. These investigations may reveal a history of active cardiac conditions that may modify the type of operation selected or preclude surgery. Only rarely is stress testing or coronary arteriography indicated since coronary revascularization is usually contraindicated in the context of an active infection. However, this information may alter the surgical plan, provide valuable information for the anesthesiologists, and guide discussions with the patient or family regarding the expected outcomes. Pulmonary evaluations are rarely undertaken, as this information seldom alters the management of the patient. Only those patients with the most severe pulmonary insufficiency may benefit from formal testing to guide perioperative management.⁸⁶

Operative planning is greatly facilitated by a preoperative CTA to define the arterial anatomy. Angiography of the lower extremities is reserved for cases when a concurrent infrainguinal bypass is considered likely. Noninvasive measurements of distal perfusion and lower extremity vein mapping should be performed. Ankle-brachial indices (ABIs) may forewarn the surgeon of the potential for infrainguinal revascularization after graft excision and aortoiliac reconstruction. Mapping of the bilateral greater saphenous veins and femoral–popliteal veins is essential if an autogenous conduit is contemplated. Femoral–popliteal veins with a diameter of less than 6 mm or evidence of vein wall sclerosis are inadequate for aortoiliac reconstruction.²

Anesthetic Considerations

Operations to excise infected aortic grafts are technically challenging, lengthy, and prone to a large volume of blood loss. The importance of a quality anesthesia team in managing these challenges cannot be over-stated. Hypothermia, hypovolemia, and intraoperative anemia must be assiduously avoided with the use of warming blankets, warmed resuscitative fluids, warm ambient operating room temperature, and a low threshold for blood and crystalloid replacement. The blood bank should be prepared to provide fresh-frozen plasma, cryoprecipitate, or platelets on short notice if coagulopathy develops. Culture data are often not available at the time of operation, so broad-spectrum antibiotic coverage for gram-positive, gram-negative, and anaerobic organisms should be redosed throughout the operation.

Aortic Ligation and Extraanatomic Bypass Versus In Situ Reconstruction

A major advantage of graft excision with extraanatomic bypass is the removal of all prosthetic graft material from the infected operative field. This approach also obviates the need to procure an aortoiliac allograft. Finally, use of an extraanatomic bypass circumvents any reticence a surgeon may have with harvesting femoral veins since some surgeons are not familiar with the technique. The obvious pitfalls of this approach are the risk of aortic stump blowout, reinfection of the extraanatomic bypass graft, and poor long-term patency of the extraanatomic reconstruction. In situ reconstruction is appealing because it avoids the risk of aortic stump blowout and the poor long-term patency of extraanatomic bypasses. For patients with insufficient infrarenal aorta for a secure three-layer closure, in situ may be the only reasonable option. Reinfection of new graft is the obvious risk of this approach. In the following sections, we will offer technical suggestions for performing these complex operations and summarize the published results for each approach.

Aortic Graft Excision

Common to each of the described surgical approaches to aortic graft infection is the need for complete graft excision. For graft excision, aortic exposure can be performed via a transperitoneal or retroperitoneal approach. Proximal control of the infrarenal aorta can be challenging in a redo operative field, so the surgeon should be prepared to obtain proximal control of the aorta at the suprarenal or supraceliac level. When treating an AEF, we always obtain either suprarenal or supraceliac aortic control prior to mobilizing the duodenum since there may be uncontrolled hemorrhage in the absence of proximal aortic control. Balloon control is another useful adjunct in cases of severe inflammation or scarring.⁵⁰ The left renal vein may be densely adherent to the graft or the native aorta, which may necessitate its division to gain access to the aorta near the renal arteries. Once proximal control is obtained, distal control of the bilateral common iliac arteries should ensue, unless these arteries are occluded. When excising an aortofemoral graft, the femoral limbs should be controlled in the abdomen to facilitate their removal. Removal of aortofemoral grafts requires considerable dissection in the groins for control of the prosthetic graft limbs and native common femoral, superficial femoral, and profunda femoris arteries. Femoral exposure may be performed through an incision directly over the femoral limb or incisions lateral to the sartorius muscle. The lateral incision avoids some of the prior scarring and may preserve soft tissue for arterial coverage. Systemic heparin is administered prior to cross-clamping, and the graft is removed in its entirety. Any arterial tissue that appears to be abnormally friable is probably infected and should be debrided. Remnants of graft and arterial tissue should be sent for Gram stain, culture, and sensitivity testing. A critical adjunct is wide debridement of the retroperitoneum, which is believed to decrease the residual bacterial bioburden that will predispose to recurrent infection. After completing graft excision and debridement, closure of the aortic stump or in situ aortoiliac reconstruction may ensue.

Extraanatomic Bypass

For stable patients, staging of the extraanatomic bypass and graft excision should be considered, as proposed by Reilly.⁷⁵ The first stage of this approach consists of performing an axillobifemoral bypass or bilateral axillary–popliteal bypasses, meticulously avoiding any infected or contaminated planes when tunneling the new grafts. The second stage consists of aortic graft excision, retroperitoneal debridement, and aortic stump closure. Aortic stump closure requires a meticulous three-layer closure of the aorta. The first two layers consist of two layers of nonabsorbable polypropylene suture; a vertical mattress suture, followed by running “baseball” suture. The final layer is an omental wrap secured with sutures.⁷⁵ When staging the extraanatomic bypass and graft excision, the optimal time interval between the two operations has not been defined. It has been our experience, however, that the presence of both an aortobifemoral bypass and an extraanatomic bypass creates competitive flow between the grafts that often results in thrombosis of the extraanatomic bypass graft. To minimize the risk of interval graft thrombosis, patients are anticoagulated with intravenous unfractionated heparin between operations, and a short (1 to 3 days) time interval (usually 1 to 2 days) between the two operations is planned. If the two operations are performed at the same operative setting, the clean portion of the procedure (the extraanatomic bypass) is performed prior to the infected portion of the case (graft excision) whenever feasible to minimize the risk of bacterial inoculation of the new graft.

The outcomes for graft excision with extraanatomic bypass have been sobering. In their landmark review, Yeager and Porter reported an average mortality rate of 21% with an average amputation rate of 11% and recurrent infection rate of 18%.⁷⁷ In a series of 36 patients with aortic graft infections, Seeger et al. subsequently reported a similar mortality rate (overall treatment-related mortality rate of 19%), but a lower rate of reinfection and aortic stump blowout (2.8% incidence of each complication).⁷⁶ Seeger noted that the patency of the extraanatomic bypasses was directly related to the type of graft configuration. Axillobifemoral bypasses had a primary patency of 75% at 41 months, whereas the primary patency for axillopopliteal bypasses was 0%. Similar results have been observed using this approach in treating infected abdominal aortic aneurysms. Lee reported a series of 28 patients with infected abdominal aortic aneurysms treated with aortic resection plus either in situ repair (n = 13) or extraanatomic bypass (n = 15).⁸⁷ Lee observed a 27% mortality rate for the cohort receiving extraanatomic bypass in this nonrandomized study.

In Situ Reconstruction with Cryopreserved Arterial Allografts

Experience with allograft replacement of primary or secondary arterial infections began with Alexis Carrel more than a century ago.⁸⁸ Difficulties with procurement and preservation resulted in poor quality control. Allografts were largely abandoned until their resurrection for the treatment of infectious pathologies of the ascending aorta in the 1980s.⁸⁹ Initial positive experience resulted in more widespread use, including the treatment of infected infrarenal aortic graft infections.⁹⁰ Initially, local tissue banks were responsible for procuring, preserving, and allocating allografts for clinical use. This resulted in considerable variability in the processes of preparing and storing the product, which may have impacted the quality of the product. Currently these processes have been centralized in both North America and Europe with primary suppliers of the cryopreserved allografts.

The primary advantage of cryopreserved allografts is its resistance to infection, which is substantiated by recurrent infection rates ranging between 0% and 3.6%.^83,90–94 Primary patency was 97% at 5 years in a multi-institutional registry, which is comparable to other conduits for in situ reconstruction.⁸³ The primary disadvantages of cryopreserved allograft in the early experience with this conduit were graft rupture and pseudoaneurysm formation. Newer cryopreservation techniques have improved the preservation of the arterial collagen matrix, decreasing the incidence of graft rupture and pseudoaneurysmal dilation. However, it is not clear that these issues have been fully resolved. Vogt et al. reported an allograft complication rate of 16% in a cohort of 43 implants, including one intraoperative rupture and three late ruptures (>30 days after implantation).⁹² In a multicenter registry of cryografts, 24% of patients experienced major complications, including eight ruptures and six pseudoaneurysms.⁸³ The most frequent complication, however, was persistent sepsis, occurring in 17 subjects. Other disadvantages of cryopreserved allograft include the cost of the grafts (approximately $18,000 per aortoiliac segment).⁸⁰ Moreover, these grafts are not readily available in most centers, making it less practical for infected pathologies complicated by hemorrhagic or septic shock.

In response to the early complications, Vogt recommended several techniques to prevent early adverse outcomes.⁹² These included proper timing of the allograft thawing and ligature of the allograft side branches with polypropylene suture that incorporates a portion of the allograft wall. Tension on the anastomoses must be avoided, and reinforcement of the anastomosis with circumferential allograft strips and gentamycin-impregnated fibrin glue is also recommended.

In Situ Reconstruction with Rifampin-Soaked and Silver-Impregnated Grafts

Rifampin shows unique activity against S. epidermidis biofilms, making it an excellent choice for prosthetic graft infections.⁹⁵ Rifampin-soaked Dacron grafts (600 mg rifampin in 250 mL of normal saline, soaked for 30 minutes) with omental wrapping has been shown to have variable resistance to recurrent infection, ranging between 4% and 11.5%.^80,81 Recurrent infections have been fewer when treating AEFs, compared to prosthetic graft infections. Primary patency is also excellent, ranging between 89% and 92%, with limb salvage rates of 100%.^80,81,96 Circumferential omental wrapping of the grafts is a critical technical adjunct to decrease the risk of reinfection.⁸⁰

Silver-impregnation relies upon the ability of silver to adsorb gram-positive and gram-negative bacterial membranes, resulting in disruption of the membrane and cell lysis. There has been no reported bacterial resistance to silver.⁹⁷ It is theorized that silver-impregnated grafts would have activity against E. coli and methicillin-resistant S. aureus, which would be an improvement over rifampin-soaked grafts.⁹⁸ The limited clinical data suggest that silver-impregnated grafts are not equivalent to rifampin-soaked grafts since the reinfection rate was 15.7% in a single-center series in France.^99,100

In Situ Reconstruction with Autogenous Femoral Vein

Autogenous femoral vein was proposed as an alternative conduit for in situ reconstruction for infected aortic grafts in the early 1990s.¹⁰¹ Clagett described creating a “neoaortoiliac system” using femoral veins harvested from both legs. The proposed advantages of femoral vein include an innate resistance to infection and excellent long-term patency, which is borne out by the two largest series to date using femoral vein. Ali reported 187 neoaortoiliac reconstructions using femoral vein.² The 30-day mortality for this approach (10%) was not significantly different from other in situ reconstructions for graft infection. Predictors of mortality included preoperative sepsis and infection with Candida glabrata, Klebsiella pneumonia, or Bacillus fragilis. Reinfection occurred in 5%. Primary patency was 81% at 72 months. Daenens reported similar outcomes using femoral vein, including an 8% inhospital mortality rate.¹⁰² Daenens group observed no reinfections and no cases with aneurysmal degeneration of the femoral vein graft. The 5-year primary patency was 91% with a limb salvage rate of 98%.

The major pitfall of using femoral vein for in situ reconstruction is the time required to harvest the veins. Although many surgeons have not had formal training in the technique for harvesting femoral veins, it is well within the capability of any vascular surgeon. The technique is described in detail elsewhere.¹⁰³ Briefly, femoral veins are harvested using an incision extending along the lateral edge of the sartorius muscle from the anterior superior iliac spine to the medial condyle of the femur. The sartorius muscle is reflected medially to preserve the segmental blood supply of the sartorius. Collateral vessels from the superficial femoral and popliteal arteries should be preserved during vein harvest, especially in the setting of known superficial femoral artery occlusive disease.¹⁰³ The saphenous nerve should be avoided to prevent postoperative neuralgia. The femoral vein is harvested from its confluence with the profunda vein to the knee joint to provide a length of vein required to replace an aortobifemoral bypass graft. All side branches greater than 3 mm in diameter are doubly ligated, rather than suture-ligated, since the latter may tear the wall of the vein graft. The femoral vein is divided flush with the profunda vein to avoid creating a blind stump that could serve as a nidus for thrombus formation and subsequent pulmonary embolism. The vein is then everted in its entirety, with the intimal layer on the outside, to allow excision of the venous valves. After reversion, the graft is distended and any defects are repaired with 6-0 or 7-0 polypropylene suture. The graft is used in nonreversed orientation to improve the size match at the aortic and femoral anastomoses.

Among clinicians who are not familiar with using femoral vein for aortoiliac reconstruction, there appears to be reluctance based on concerns with any venous morbidity associated with harvesting the femoral vein. Our group has extensively studied this issue.^104,105 In the early postoperative period, there is a risk of venous congestion that may produce lower leg compartment syndrome requiring fasciotomy. Early in our experience with deep vein harvest, fasciotomy was required in 17% of limbs, although many of those fasciotomies were “prophylactic.”¹⁰⁴ With additional experience, our tolerance for acute leg swelling has increased, so fasciotomy is now rarely performed. Two preoperative predictors of a higher probability of fasciotomy were identified: concurrent harvesting of the greater saphenous vein in the same limb and a low ankle–brachial index (<0.55) in the harvested limb. Prior harvest of the ipsilateral greater saphenous vein was not a risk factor for requiring a fasciotomy. Venous collaterals develop over time to normalize venous physiology in most patients, so long-term venous morbidity is minimal. One-third of patients experience mild chronic leg swelling, and the remainder are asymptomatic.¹⁰⁵ To our knowledge, no limbs have developed venous ulceration as a consequence of femoral vein harvest.

Comparisons of Arterial Reconstruction Methods for Aortic Arterial Infections

There is a dearth of direct comparisons of the various surgical options for managing graft infections in the literature. Over the past decade, there has been a trend toward various types of in situ reconstructions due to the inferior patency of extraanatomic reconstructions and the risk of aortic stump rupture.^74–78 O’Connor performed a systematic review of the literature to compare the various methods of reconstruction, comparing extraanatomic bypass, rifampin-soaked prostheses, cryopreserved allografts, and autogenous venous reconstructions.¹⁰⁶ Adverse events were more than 50% more frequent with extraanatomic bypass, compared to in situ reconstruction. The lowest event rates were noted with rifampin-soaked prosthetic bypasses. Early and late mortality was most likely after extraanatomic bypass. Autogenous venous reconstructions provided the lowest rate of reinfection, followed closely by cryopreserved allografts. Conduit failure was most likely with extraanatomic bypasses. The patient numbers were too low to compare the patency of rifampin-soaked bypasses with other reconstructions. Major amputation was most likely with either extraanatomic bypass or autogenous venous reconstructions. Table 88-1 summarizes the authors selected studies reporting the outcomes of various reconstructions in aortic infections.

NONAORTIC ARTERIAL AND GRAFT INFECTIONS

Lower Extremity Arterial Infections

Lower Extremity Graft Infections

The nonoperative management of Szilagyi III wounds was described previously. Older studies show that lower extremity bypass graft infections carry a postoperative major amputation and mortality rate of nearly 50% due to the underlying atherosclerotic disease burden.¹⁰⁷ These patients often do not have other conduit suitable for bypass, which is a major impetus for graft preservation strategies for infected extremity bypass grafts. The use of local debridement with adjunctive vacuum-assisted closure and muscle flaps has yielded promising results. Siracuse cited an estimated 1-year limb salvage rate of 71%, which was attributed to the graft preservation techniques described above.¹⁷

Cryopreserved human allograft veins have been touted as an alternative if a prosthetic bypass graft must be removed for infection. Unfortunately, human allograft veins have yielded relatively poor results. In a series of bypasses for critical limb ischemia using cryopreserved greater saphenous vein, primary patency at 1 and 3 years was 27% and 17%, respectively.¹⁰⁸ Amputation-free survival at 1 and 3 years was 43% and 23%, respectively. Cadaveric vein grafts are expensive, ranging between $7,000 and $7,500. In view of the outcomes and cost, the use of cryopreserved veins must be weighed against the outcomes of graft preservation techniques on a case-by-case basis.

Infected Common Femoral Artery Pseudoaneurysms

The management of infected common femoral artery pseudoaneurysms diverges from the management of infected pseudoaneurysms in other anatomic locations. The most frequent clinical scenarios involve infection after a history of recent arterial catheterization or intravenous drug abuse. The incidence of infection after cardiac catheterization is less than 1%, although the use of arterial closure device increases the risk due to the presence of a foreign body.¹⁰⁹ Aggressive debridement, removal of the closure device, and revascularization remains the mainstays of therapy. In situ repair with autogenous greater saphenous or femoral vein is preferred if arterial replacement is necessary.^27,110 A rotational muscle flap may be necessary for graft coverage in some cases. Occasionally, in situ repair may not be advisable due to the quality of the arteries or the surrounding tissue. Ligation of the native arteries in the groin and an extraanatomic bypass, such as an obturator bypass, may be preferable.¹¹¹ Ligation of the common femoral artery without reconstruction is utilized as a last resort and is less likely to threaten the limb if the femoral bifurcation remains intact.¹¹²

Conversely, infected common femoral artery pseudoaneurysms secondary to intravenous drug abuse should be preferentially managed with aggressive arterial and soft tissue debridement and ligation of all of the involved arteries. Immune suppression due to malnutrition and human immune deficiency virus infections, delayed presentation, and patient recidivism make arterial reconstruction hazardous in this setting. Reddy showed that ligation of the common, superficial, and profunda femoral arteries is associated with a 33% major amputation rate.¹¹³ Rates of major amputation are very low in other series, with some authors reporting zero amputations in their series.^114,115 Claudication is almost universal, however with debridement and femoral artery ligations.²⁷ Some authors recommend limiting revascularization attempts to patients with absent pedal Doppler signals after ligation of the femoral vessels, whereas others recommend amputation for all subjects with infected pseudoaneurysms due to intravenous drug abuse.¹¹⁶

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