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Current strategies for the management of infection in lower extremity revascularization
(Portuguese PDF version)

Luís Henrique Gil França¹, Henrique Jorge Stahlke Jr.²

1. Vascular Surgeon. Specialist in Vascular Surgery, SBACV. MSc in Clinical Surgery, Universidade Federal do Paraná (UFPR), Curitiba, PR, Brazil.
2. Associate Professor, Vascular Surgery, Hospital de Clínicas, Universidade Federal do Paraná (UFPR), Curitiba, PR, Brazil.

Correspondence:
Dr. Luís Henrique Gil França
Rua Coronel Dulcídio, 1189/1801
CEP 80250-100 - Curitiba - PR
Brazil
Tel.: +55 (41) 343.0963
E-mail: luishgf@hotmail.com

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ABSTRACT

Infection in the surgical management of lower extremity revascularization is a serious complication and its prevention, control and treatment may represent a clinical challenge to the vascular surgeon. Morbidity and mortality rates are high among patients who develop postoperative infection. Graft infection is difficult to eradicate and, if not adequately treated, may cause prosthesis failure, hemorrhage or sepsis. Preventive measures are fundamental to avoid postoperative infection. The use of less invasive techniques to harvest the great saphenous vein in lower extremity revascularization surgery and the use of prosthesis impregnated with silver salts and antibiotics are some examples of prophylactic measures currently employed. A successful management of the infection requires a good knowledge of the pathophysiology of this condition and the use of many therapeutic modalities like intravenous antibiotics, local wound care, surgical debridement and arterial reconstruction, when necessary. Nowadays, advances in the management of infected vascular prostheses have led to a decrease in amputations and mortality rates. The use of rifampin-bonded grafts to treat S. epidermidis infection has proved to be very effective. Early results are promising for cryopreserved allografts and autogenous femoral vein in situ grafts. The purpose of this work is to conduct an updated review of evaluation and management of infection after infrainguinal arterial bypass.

Key-words: infection, lower extremities, arteries.
Palavras-chave: infecção, membros inferiores, artérias.

J Vasc Br 2004;3(2):137-44

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Despite important therapeutic advances, prevention and treatment of postoperative infection are problems still waiting to be solved. The introduction of antibiotic therapy, in the second half of the 20th Century, increased hopes that major surgical infections would be eradicated. Unfortunately, this has not happened so far. Postoperative infections persisted and the widespread use of antibiotics made even more difficult to prevent and control surgical infections.¹

Postoperative infection in vascular surgery is a major complication that involves risk of amputation and mortality for all patients affected. Diagnostic is not always easy. In addition, the patient may present with infection many years after the surgical procedure.² Morbidity and mortality associated with infection depend on the time the bacteria takes to manifest itself, the type of graft and its location, and the kind of treatment employed.² Infrainguinal arterial bypass surgery infections, non-diagnosed or inadequately treated, present mortality rate between 0 and 22% and amputation rate between 8 and 53%.³

Traditionally, the treatment of postoperative infection in vascular surgery consists of antimicrobials, excision of the infected graft and, if necessary, an extra-anatomical revascularization.^2,4 In this article, we will discuss evaluation and diagnosis of infrainguinal arterial bypass infection as well as the currently most used preventive and therapeutic measures.

INCIDENCE

The incidence of infection after lower limb revascularization surgery ranges from 1 to 6%, occurring a few days or even a few months after the procedure. A great number of infections, however, may manifest themselves many years after the implantation.^2,4 The accurate incidence in infrainguinal bypasses is unknown, being reported as ranging from1.5 and 12% for prosthesis, and 0 to 1.7% for autologous grafts.³ Edwards et al. identified complications of the surgical wound (skin necrosis, bruises, seromas and cellulites) as primary predisposing factor in33% of cases of infection. Surgical wound complications occurred in 44% of the surgical procedures. Over a third of graft infections has previous complications of the surgical incision. These complications may occur in any kind of incision on the lower limbs. They are associated with a high rate of surgical wound infection and vascular graft infection.⁵ Calligaro et al. reported the difficulty in differentiate the infection that actually affects the graft from the surgical incision infection, since cellulite, abscesses and fistulas, although extended over the graft, do not always result in a graft infection.^6,7 Tukiainen et al. reported an incidence of surgical wound complications of 10 to 40%. They also noticed that over 15% of patients whose graft is placed under the tissue will develop infection extended to the graft.⁸ Other authors also found similar results, with incidences of 10.86% in arterial surgery infection⁹ and 12.27% in infrainguinal arterial bypasses.¹⁰

PREVENTION

Preventing the infection should be a constant concern to vascular surgeons. The employment of a prophylaxis program including pre-, intra- and postoperative measures results in small and highly acceptable infection incidence. Moreira et al. reported a 0.89% incidence of surgical wound infection and 0.97% of arterial graft infection (1.47% of synthetic grafts) after a systematic use of prophylaxis program.¹¹

Levy et al evaluated cultures of patients' skin bacterial flora on the day of admission, on the day of the surgery and 5 days after the surgical procedure. The authors concluded that patients that are, at the admission, colonized with coagulase-negative Staphylococcus, predominantly susceptible, become, during treatment, predominantly resistant strains.¹² Therefore, preoperative hospitalization should be as short as possible to avoid colonization of hospital flora.

Prophylactic antibiotics should be administered prior to the procedure, during a long surgical procedure, or when excessive changes in blood volume or fluid administration occur.² Lehnhardt et al, in 2002, experimentally showed that the association of systemic prophylactic antibiotics with local antibiotics provides the graft with higher protection against infection.¹³

The technique employed for revascularization also influences the risk of infection. In a lower limb revascularization surgery in which the great saphenous vein in situ was used as vascular graft, postoperative infections occurred mainly in the groin, however, they could also appear on the distal portions of the graft.^14,15 These infections are more likely to be serious in elderly people due to skin and subcutaneous cell tissue atrophy in the distal portion of the limb.¹⁴ A meticulous surgical technique, with closing of groin incisions by plans, avoiding bruise formation, is essential for reducing the risk of surgical wound complications, for example, necrosis of the wound edges and lymphatic fistula.¹⁶

The use of synthetic graft impregnated with bactericidal substances has been an alternative to prevent postoperative infection in vascular surgery.¹⁷ Theoretically, a vascular prosthesis that is supposed to be resistant to infection should meet some prerequisites, such as antibiotic efficacy against the bacteria involved in the infection of the prosthesis, the use of immunocompatible material with low toxicity, and the use of prosthesis with prolonged bactericidal action to allow infection-free healing.¹⁷

Firstly described by Clark & Margraff,¹⁸ in 1974, the use of vascular prosthesis impregnated with silver salts has showed efficacy in in vitro experiments, however, in vivo experiments has showed different results.¹⁷ Some aspects about silver salts should be emphasized. Silver ions are efficient against an ample spectrum of bacteria (specially Pseudomonas), and this bactericidal action is proportional to its concentration. On the other hand, silver metals have low bactericidal efficacy due to their chemical instability. Usually released from inorganic silver salts, the silver ions act by replacing essential ions like calcium and zinc. The adhesion of silver ions to the bacterial DNA interacts with cell oxidation processes and inhibit the respiratory chain. Some factors that reduce the bactericidal action of the silver ions include the deposit of plasmatic proteins on the prosthesis surface and the conversion of silver acetate into silver chloride at high concentrations of chloride ions.^17,19

A number of studies has shown that the addition of antibiotics like norfloxacin, oxacillin, amicacin and rifampin to proteins such as albumin and collagen, in vascular prosthesis, has showed to be effective in preventing vascular graft infections.^17,19-21 However, various studies have demonstrated that a complex of these antibiotics with silver ions, on the surface of the vascular prosthesis, has showed superior bactericidal action with better results when the antibiotic employed was rifampin.²¹

PATHOPHYSIOLOGY

Before and after its implantation, a vascular prosthesis may come into contact with bacteria.² This infected prosthesis should be isolated and kept away from any source of contamination, specially the skin. If the prosthesis happens to come into contact with the wound area or any others non-sterile areas it becomes susceptible to infection. When contamination of the vascular prosthesis occur, infection will probably develop only if a sufficient number of bacteria come into contact and adheres to the prosthesis, or when complications with wound healing extends towards the prosthesis² The femoral artery is one of the most employed vessels in vascular surgery. Some authors suggest that its proximity with the perineum and with the natural skin orifices (anus, uretral meatus) and the presence of germs within the skin creases make the groin area highly susceptible to infection.²¹

Bacteria can also come into direct contact with grafts through the hematogenic or the lymph passages Lower limb lymphatics are located very near to the arterial vessels and they carry limpha from the distal portion of leg and foot to the femoral region. Bacteria from the infected distal wounds travel towards the lymphonodi of the femoral area. During dissection, the lymphonodi may occasionally be damaged and, consequently, the implanted graft will be flooded with infected lymph. Moreira, in 1991, while studying the bacteriology of inguinal lymphonodi, found positive cultures in 434% of cases, being Staphylococcus epidermidis cultivated in 41% of cases. In this sudy, no correlation was observed between the cultures of lymphonodi and the culture of distal skin lesions in the same limb, and the cultures of postoperative surgical wounds or synthetic grafts.²¹

Bacteria may adhere to the atherosclerotic arterial walls and to the peri-arterial tissues from previous vascular reconstruction, behaving as reservoirs of infection. Timi, in 1992, studying the bacteriology of atherosclerotic plaques in femoral artery, observed a significant presence of positive culture, being Staphyloccoccus epidermidis the major cultivated agent. However, no relation was observed between the germs found in the atheroma plaques and in the trophic lesions of the operated limbs and the germs isolated from the infected surgical wound.²²

While studying others sources of contamination, Guimarães et al., in 1991, obtained cultures of material from the arterial wall, collected during surgical procedure. The authors noticed significant incidence of latent infection in the parietal thrombi (6% of our patients and 0.9%, respectively), that is, in the central of the atherosclerotic process. In addition, the authors observed that the majority of later infectious manifestations occurred in patients with previous subclinical contamination in the atheroma plaques.²³

The incidence of various bacterial strains isolated in the immediate postoperative (up to 30 days following the surgical procedure) differs from those isolated in the late postoperative.^2,24 For example, the coagulase-positive staphylococcus (Staphylococcus aureus) is the most frequent bacterium found in the immediate postoperative period. This bacterium produces the coagulase enzyme which inhibits phagocytosis and increases antibiotic resistance.^2,24

Infections caused by Gram-negative bacteria, including Escherichia coli, Proteus sp. e Pseudomonas aeruginosa, also often occur in the immediate postoperative. Infections caused by Pseudomonas aeruginosa are very aggressive due to the release of destructive enzymes like elastase and protease. These enzymes attack elastin and collagen that are found in the donor arterial walls and in the venous graft, compromising their structural integrity.²⁴

Late infections are frequently caused by Staphylococcus epidermidis, a coagulase-negative which lives in the skin´s normal flora of the femoral area.²⁵ This little aggressive microorganism, fond of prosthetic materials, is capable of adhere and grow on the surface of synthetic grafts, developing micro-colonies with multiple layers of bacteria adhered to one another. The majority of Staphylococcus epidermidis strains, as well as Staphylococcus aureus strains, have the capacity of releasing a exopolissacarídeo called glycocalyx, a munucious substance that coats the bacteria, similarly to a capsule. The glycocalyx eventually involves the whole colony and strongly adheres to synthetic grafts, forming a layer called biofilm.²⁵ Besides inhibiting in vitro antimicrobial action, this biofilm also difficults host response, inhibiting cell immunological response, affecting opsonization and phagocytosis of lymphocytes and damaging the tissue surrounding the prosthesis, which results in mechanical failure of anastomosis. Eradicating these bacteria from the synthetic graft becomes almost impossible, since they become nearly impermeable to host's defense.^2,25 In adittion, the biofilm favors the fixation of other bacteria, acting like a protector. This strong adherence of the bacterial biofilm to the prosthesis is the cause of high incidences of false-negative cultures, reaching up to 50% of cases. Therefore, special culture techniques are required, among them are the ultra-sonic centrifugation of the infected prosthesis in order to brake the biofilm that is adhered to the prosthesis before culture sowing.^2,22,25

CLASSIFICATION

Infections that occur after lower limb revascularization surgery are classified according to the time of manifestation, surgical wound complications and extent of graft involvement.²

The first classification for postoperative infection in vascular surgery was proposed by Szilagyi et al., in 1972. It is divided in three degrees that determine the depth of the infection and the kind of treatment to employed. When only skin and subcutaneous cell tissue are involved, the infections are classified as degree I and II type, and treatment usually requires local care of the surgical wound and antibiotic administration only. In the degree III type, the vascular graft is involved; treatment may vary from total or partial excision of the graft, revascularization with extra-anatomical graft to toamputation.²⁶

Samson et al., with the aim of better specifying graft involvement, the kind of treatment to be employed and patient prognosis, added two types: degree IV (infection with involvement of anastomosis, and degree V (infection with involvement of anastomosis sepsis or hemorrhage).²⁷

CLINICAL AND LABORATORIAL DIAGNOSIS

The majority of cases of infection occur in the immediate postoperative (up to 30 days after the surgical procedure), being the final result of surgical wound complication. Late infections manifest themselves through abscesses and skin fistulas. Although more frequent in the groin, these infections may appear in any incision or subcutaneous tissue that covers the graft. Pseudo-aneurysm is characterized by a discrete pulsatile mass and/or symptoms related to the compression of vasculonervous structures of the thigh or calf. The rupture of the arterial anastomosis, secondary to the infection, is characterized by pulsatile mass or bleeding of retroperitoneum, thigh, and calf. Septic embolus are rare. They are considered, however, as a classical sign of vascular sepsis, in the form of petechiae below the infected vascular conduit. Unspecific signs of sepsis in patients with vascular prosthesis (leukocytosis without apparent cause, fever and high hemosedimentation rate) suggest a high level of suspicion.^2-4

Color Doppler ultrasound is indicated to investigate patients with suspected infection following lower limb revascularization surgery. This noninvasive exam offers high resolution for the evaluation of potential areas of infection, below the inguinal ligament. It is also very useful to detect graft patency or thrombosis, pseudo-aneurysm, and the presence of fluid surrounding the prosthesis. Color Doppler ultrasound has the advantage of being a low cost exam of easy access that does not require contrast or radiation exposition. Among the advantages are the non-differentiation of infected from sterile fluid collections, and the characteristic of being a examiner-dependent exam.²⁸

Tomography scanning has the same structures than color Doppler, although more accurate. It is not useful, however, to detect graft patency.^2-4 The magnetic resonance has some advantages over tomography, since it allows multiple-plan images, with improved visibility. In addition, the magnetic resonance has higher detection sensitivity for small collections and soft tissue changes. The magnetic resonance has the disadvantage of not being able to detect the presence of air and calcium near the prosthesis. It is a high cost exam, available in few medical centers.^2-4

Radionuclide mapping plays an important role in vascular infection diagnosis. In some circumstances, when other complementary exams are inconclusive, the scintigraphy may be used to show areas with a great number of leukocytes or immunoglobulin on the vascular graft site. Scintilographies to detect vascular graft infection employ radioisotopes that are specially prepared for this purpose. The most used are gallium citrate, indium-111-labelled leukocytes, or technetium and polyclonal immunoglobulin G (IgG). However, this exam cannot be performed in the early postoperative period, since it may detect non-specific signs of health tissues. In a patient with clinical suspicion of late infection in the vascular prosthesis, positive scintigraphy suggests the need of surgical exploration.²⁹ Nowadays, this kind of functional imaging is better employed when coupled with anatomical images, so that it is possible to obtain the exactly location and extent of infection. The arteriography is a very important exam to define the most adequate strategy for revascularization of a ischemic limb, if necessary.^2,4,29

TREATMENT

When the general clinical condition of the patient allows, the treatment should be prepared during the preoperative period. The surgeon should require hemoculture, secretion cultures, and cultures of infected wounds. Ample spectrum antibiotic should be administered until the results are obtained, when an specific antibiotic will be prescribed.²⁴ For infections caused by Staphylococcus aureus or Staphylococcus epidermidis, first generation cephalosporin or vancomycin² should be administered. Duration of antibiotic therapy for postoperative infection has not been well defined; it may vary from two weeks to six months. Patients who receive antibiotic for a long period showed significantly better results than patients whose antibiotic therapy lasted between 10 to 14 days.² Chronic diseases related to the cardiovascular, pulmonary and renal system, as well as the nutritional status of the patient, should be evaluated and properly treated. Descriptions analysis of previous surgical procedures and exams like preoperative arteriography contributes to a better understanding of the anatomy of the graft and the location of arterial anastomosis, the indication for the first surgical treatment, the evaluation of important collateral vessels, and the adequate conditions for reimplantation of a new graft.³⁰

A suitable sequence of treatment should be individualized, according to the following priorities: (1) treatment of life risk infection; (2) prevention of infection of the new graft; (3) avoidance of prolonged ischemia.^24,30,31 Occasionally, some cases requires emergency treatment, such as patients with hemorrhage caused by rupture of an arterial anastomosis, cases of expanding pseudo-aneurysms, and even uncontrollable sepsis.^31,32

Revascularization techniques are determined by the aggressiveness of the microorganism.³³ For example, a stable pseudo-aneurysm caused by Staphylococcus epidermidis coagulase-negative may be treated with excision of the infected graft and reimplantation of a polytetrafluoroethylene (PTFE) prosthesis.²⁵ However, infections caused by different bacteria should not be treated in a similar manner, especially those infections caused by Pseudomonas sp, due to its high virulence.²⁴ Based on a retrospective study of 27 cases of infection in 220 patients who underwent to infrainguinal arterial bypasses, the author concluded that the amputation probability in patients infected by Gram-negative bacteria was approximately 26 times higher.¹⁰ Ouriel et al. reported that cases of rupture of the arterial anastomosis and graft reinfection were related to infections caused by these bacteria.³⁴ The essential components of local treatment include drainage, debridement of the infected necrotic tissue, local antibiotics, and the use of autogenous tissue for covering. These procedures are performed in a surgical room under adequate conditions.³⁵ The entire infected necrotic tissue is carefully isolated from the surgical wound and sent to culture. The arterial anastomosis, the donor artery, and the prosthesis are inspected throughout the surgical procedure. Any evidence of defect is considered a potential source of late hemorrhage. In these cases, the prosthesis is removed. Failure in controlling the infection requires additional debridement and graft excision. Total or partial graft removal is necessary when the infection results from hard control sepsis, graft thrombosis or dehiscence of anastomosis.²⁴ However, infected graft excision is usually a technically difficult procedure. It can damages a network of collateral flow that might be fundamental for limb preservation.²⁵ Calligaro et al. reported that the majority of patients who died of sepsis or hemorrhage had undergone total graft excision, with rupture of the donor artery.³⁶

Primary amputation is the most rational option for a debilitated patient with non-viable lower limb and graft infection who would not tolerate the continuous stress of multiple surgical procedures.²⁴

For patients who are able to undergo surgery, the exposed graft should be covered with muscle flap, after formation of granulation tissue. This is a good option, resulting in high rates of graft preservation and shorter hospitalization.^8,36-39 This procedure should be performed with the aim of preserving graft and limb viability. However, Calligaro et al., while comparing the use of muscle grafts and second intention healing (through local care and antibiotic therapy), did not find significant differences regarding results and costs. The authors reported that for high surgical-risk patients a second intention healing with granulation tissue formation proved to be effective in 75% of cases.³⁷ The rectus femoris muscle is largely used for this purpose. Alternative options include the rectus abdominis, the gracillis, and the sartorius muscles. The sartorius muscle has the disadvantage of having a blood segment which tends to rupture during mobilization, causing muscle ischemia and graft exposition.^38,39

Graft preservation may be performed for both venous or polytetrafluorethylene (PTFE) grafts, but it is not recommended for Dacron prosthesis, since this material present low resistance to infection.⁴⁰ During graft removal, the artery is joined or repaired (primarily or with the use of a flap) to maintain patency of important collateral vessels. Preference is giving to ligation because of the technical difficulties in reconstructing the weak walls of an infected artery. Besides, there is high probability of flap rupture in the presence of residual infection. After excision of the prosthesis and artery ligation, the revascularization will only be necessary if limb viability is threatened.^24,40 Vascularization is usually performed through arterial bypass, with graft tunnelization over sterile tissues, in an extra-anatomical plan. The use of the superficial femoral vein is a good option when an infection-resistant autologous graft is desired, with minimal morbidity of lower limb deep venous system.^41,42 The use of cryopreserved homologous artery has been proposed, however it should be carefully analyzed, since this type of graft has the tendency to be more thrombogenic and susceptible to dilation. Gabriel et al. reported the use of this type of graft in 44 patients with infected vascular prosthesis. The authors found primary and secondary patency of 63.3 and 81.8%, respectively.⁴³

Infection extension and virulence should be assessed with care when biological grafts are to be used. Due to infection, the access veins to the commonly used infrainguinal vessels are prohibitive, therefore, the surgeon should have alternative accesses available if the aim is member preservation. Access to the medial and distal portion to the deep femoral vein may be used as a origin site of a distal revascularization, when the common femoral artery has already been infected.⁴⁴ Among the various techniques described, obturator foramen bypass is an excellent option when the infection is located in the femoral area and the femoral, superficial and proximal popliteal arteries are patent.⁴⁵ The use of the external iliac artery as a donor artery is an alternative in cases of reoperations with groin preservation. This technique has some advantages since it allows proximal anastomosis in a non-treated artery, and easy and fast access to the retroperitoneum, with low risk of hemorrhage and good long term patency. The advantages include hemorrhage during tunnelization below the inguinal ligament, and ilioinguinal -iliohypogastric injury during dissection.⁴⁶

CONCLUSION

Studies with well defined and randomized protocols are still rare nowadays. This fact results in a literature that lacks a thorough definition for the treatment of vascular graft infection, since the majority of scientific works are mere reports of the experience of each service, usually with a low number of patients involved.²⁴ It has already been acknowledge that the management of infection in infrainguinal vascular procedures requires an individual and a comprehensive approach. The type and virulence of the microorganism requires a careful evaluation, specially in cases of infections caused by methicillin-resistant Staphylococcus aureus and Gram-negative bacteria.³⁵ If necessary, the revascularizations should be performed under sterile tissues through alternative accesses and extra-anatomical ways. Nowadays, new strategies employed to prevent postoperative infection in infrainguinal bypasses has reduced the rates of amputation and mortality. The use of minimally invasive techniques for the dissection of the great saphenous vein⁴⁷ and the use of grafts impregnated with silver salts and antibiotics¹⁷ has showed to be efficient as prophylactic measures against postoperative infection in vascular surgery. The replacement of the vascular graft infected by Staphylococcus epidermidis by a new prosthesis impregnated with antibiotics,²⁵ the use of the superficial femoral vein^41,42 and cryopreserved homologous grafts⁴³ are promising treatment method, however, their efficacy still requires a more comprehensive scientific investigation.

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