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T. O'Brien and J. Collin Nuffield Department of Surgery, The John Radcliffe Hospital, Oxford OX3 9DU, UK Correspondence to: Mr J. Collin

Prosthetic vascular graft infection The aetiology, diagnosis and management of prosthetic vascular graft infection are reviewed. The importance of contamination at the time of surgery as the crucial aetiological factor is highlighted. Staphylococcus epidermidis is the causative organism in over SO per cent of cases and the reasons f o r this are explored. Sound surgical technique, use of prophylactic antibiotics and the avoidance of a groin incision are emphasized as the most important factors in prevention of graft infection. Dificulties of diagnosis are highlighted and the diagnostic role of various imaging methods is assessed. Graft excision with extra-anatomic revascularization is presented as the conventional surgical solution, while the roles of less radical surgical solutions and non-operative management are discussed.

Prosthetic vascular grafts are foreign bodies and can harbour organisms within their interstices. Although infection of the prosthesis is u.nlikely to lead to disruption of the material itself, spread of infection to the native vessel produces inflammation with subsequent erosion and disruption of the artery-graft anastomosis. Haemorrhage or false aneurysm may result. The majority of graft infections are thought to arise by contamination of the graft material at the time of its insertion'.4.8. Haematogenous infection is less common than direct graft contamination', but it may explain the lag between operation and first manifestation of infection in some patients. In one series' this was over 1 year in >20 per cent of cases. Experimentally, haematogenous seeding is easy to reprodu~e~.'~. Contamination may occur because of inadequate sterilization of the graft, a breakdown in theatre sterile technique, contact with the patient's skin or an intra-abdominal organ, deposition of airborne particles, or from bacteria residing within the native artery. Contamination by organisms from the skin of the groin is the most frequent cause of graft infe~tion'.~-~. In the series of Lorentzen et aL5, no graft infections occurred in 425 patients undergoing reconstruction confined to the abdomen, whereas 62 graft infections developed in 1986 patients having a bypass involving a groin incision. Staphylococci are common skin commensals and are the most frequent isolate from infected grafts3r5.The groin is a relatively dirty area, prone to intertrigo,

and in obese patients the surgical wound lies deeply buried in folds of moist skin. The incision in the groin cuts across skin creases, tends to gape, and may disrupt lymphatic channels with subsequent development of a lymph collection. Consequently, both superficial and deep wound infections are frequent problems in this area5*6. The significance of bacteria residing within thrombus or atheroma in the native vessel is unclear"-'5. The incidence of positive cultures at the time of surgery" may be as high as 43 per cent and the organism most commonly cultured from the aortic wall is Staphylococcus epidermidis, the commonest cause of graft infection. If intra-aortic bacteria were the main source of such infection, its incidence would be similar after aortoiliac and aortofemoral bypass, but this is not the case. Durham et a1.I4, however, have estimated that, when peroperative arterial cultures are positive, the risk of developing a graft infection is around 10 per cent. Intraoperative cultures may also be made from the contents of 'bowel bags' used for the containment of small bowel during aortic surgery. In the series of Ernst et al.", cultures of the fluid transudate were positive in five of 45 patients despite systemic administration of perioperative antibiotics. Other potential sources of contamination of the graft are infected skin ulcers, gangrenous toes or an infected superficial w o ~ n d ' ~ ~ 'In ' . one series, Lorentzen et aL5 found that 55 per cent of patients who developed a graft infection had a focus of infection identified before operation. Of particular interest is that in two of the six patients identified as having a urinary tract infection before operation, cultures from urine and graft tissue were identical. Four of 22 cultures of foot lesions also yielded the organism subsequently isolated from the graft. The mechanism of transfer of infection from distal limb sepsis is unclear, but could involve direct contamination (blood-borne or lymphatic spread). Evidence for lymphatic spread is conflicting; although groin dissection inevitably cuts across lymphatics (leading to lymphatic Contamination of the operative field), cultures from the groin may not be positive4.". However, organisms injected into the ischaemic hindlimb of dogs may be cultured subsequently from ipsilateral groin wounds". Wound infection in close proximity to vascular graft material could lead to the development of graft infection by direct extension. Operation on other organs at the time of aortic surgery may contaminate the graft and most authors advise against the simultaneous performance of a second surgical procedure20.21. The importance of airborne contamination may be underestimated". Thousands of bacteria-laden skin scales are shed every minute by the operating team, and conventional theatre

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Infection of a prosthetic vascular graft is a serious complication of vascular surgery that carries high morbidity and mortality rates. Although relatively uncommon, complicating only 1-6 per cent of all operation^'-^, the cumulative incidence of such infection may be underestimated because of the long delay that often occurs between the original operation and first manifestation of infection. The number of patients at risk will continue to rise with the increasing use of prosthetic materials and the widening indications for reconstructive surgery. At current levels of activity in the UK, about 300-400 patients a year may be expected to be affected by vascular graft infection. Aortic graft infection carries a r e p ~ r t e d ' . ~mortality .~ rate of around 50 per cent and, although the mortality rate of infrainguinal graft infection3s637 is lower at around 10-25 per cent, the amputation rate consequent upon infection' approaches 80 per cent. In both situations hospital stay is invariably long, averaging 90 days in one Danish study', and may involve multiple operations. The costs of treating the small group of patients with graft infection are consequently high.

Pathogenesis

6) 1992 Butterworth-Heinemann Ltd

Prosthetic vascular graft infection: T. O‘Brien and J. Collin Antibiotic prophylaxis has been shown in randomized trials to reduce the incidence of wound and graft infection and its use is o b I ~ g a t o r y ~ . ~ ~ The - ~ ’choice . of antibiotic and length of treatment are, however, controversial. The antibiotic used should be guided by local bacterial prevalence and sensitivities, remembering that most infections are caused by S . epidermidis, S. aureus and Gram-negative organism^^*'.^^. Cephalosporins are widely used but their activity against S. epidermidis is variable. In the series of Bandyk et 19 per cent of patients were sensitive to penicillin G, 82 per cent to methicillin, 91 per cent to cephalothin, and 100per cent to both vancomycin Microbiology and gentamicin. Within 5 days of admission to hospital a Graft infection is usually bacterial, although a wide range of patient’s skin flora may be already multiresistant to micro-organisms have been implicated, including fungi24, antibiotics3’. Vancomycin offers excellent cover against mycoplasmas*’ and mycobacteria’. In early series of graft Gram-positive organisms and may be used along with S. aureus was the most frequently identified gentamicin in any patient undergoing reoperative surgery. The pathogen, being isolated in up to 50 per cent of cases. This ideal length of treatment is not known. A dose before operation pattern of infection appears to be changing: S . epidermidis, is essential, but some authors suggest discontinuing therapy Gram-negative organisms and mixed infections are increasingly 24 h after surgery while others advocate treatment until all being identified as the cause of graft i n f e c t i ~ n ~ . .~Th’ ~ ~1s ~ - ~ ’intravenous lines and catheters have been removed. A second change is similar to that observed after joint replacement and dose during the operation is wise if blood loss is heavy or if cardiac surgery. It may relate to the widespread use of surgery is prolonged. Antibiotic irrigation of wounds may prophylactic antibiotics against S. aureus and the increasing reduce colonization but has little role as an addition to prevalence of Gram-negative organisms in the hospital intravenous antibiotic therapy3’. There are no published trials environment. The rise may also relate to improved culture of the use of long-term antibiotic prophylaxis in an attempt to techniques or simply to an increase in the reporting of positive reduce the incidence of graft infection. Antibiotic-bonded grafts cultures because S. epidermidis is now regarded as a pathogen have yet to find their place in the clinical setting but show rather than a commensal. experimental p r ~ m i s e ~ ’ - ~Shue ~ . et aL3’ inoculated aortic It is known that S. epidermidis produces a slime that grafts in dogs with S. aureus; when intravenous cloxacillin was increases its adherence to biomaterials, encases the organism, used as prophylaxis the graft infection rate at 3 weeks was 80 and may thereby protect it from antibiotics3’. Bandyk et ~ 1 . per ~ cent, ~ but when the graft was impregnated with cloxacillin found 15 of 30 graft infections were caused by S. epidermidis. this dropped to 30 per cent. Antibiotic bonding to cement in This organism is of low pathogenicity, which may explain the revisional hip surgery has a well defined role, and it may be late manifestation of the majority of these infections; the mean that bonding to vascular grafts will soon play an important interval between arterial surgery and clinical manifestation of part in the prophylaxis and treatment of graft infection. infection was 41 months. These authors and other^^',^^ stressed The groin wound is the most prone to infection following the importance of fastidious microbiological techniques for the vascular surgery and, if reasonably possible, reconstructive successful isolation and culture of the causative organism. It is surgery should avoid this area. Preoperative bathing in essential to take cultures from the graft material itself and for chlorhexidine or other antiseptics has its advocate^^^.^^, but both broth and agar media to be employed. Sonication of the the evidence for any benefit is conflicting”. Shaving the skin graft material to release micro-organisms increases the increases the rate of wound infection compared with the use of proportion of positive cultures32. In only two of the 15 cases depilatory cream, but if shaving is preferred it should be in which graft material cultures proved positive were those of performed as close to the time of surgery as possible44. The perigraft fluid or tissue positive26. timing of angiography in relation to surgery has an important Two further points deserve mention. First, in all published bearing on the incidence of wound infection. Landreneau and series of graft infections there is a high incidence of negative Raju demonstrated a reduction in wound infection4’ when cultures despite convincing clinical evidence of infection. This surgery was performed within 24h of angiography or, may be due to inadequate and inappropriate samples being alternatively, when it could be delayed beyond 1 week. sent for culture, technical deficiencies in the laboratory, or Preparation of the skin before incision should be thorough, because the majority of patients are already being treated with using povidone-iodine or chlorhexidine, or both44,46.Adhesive broad-spectrum antibiotics. Specimens for microbiological skin drapes appear to increase the rate of wound infection44. culture must be handled with care and alacrity if meaningful The observation that up to 60 per cent of vascular graft results are to be obtained. Second, superficial wound cultures infections are associated with an avoidable operative may be misleading in the context of prosthetic vascular graft complication illustrates the importance of sound surgical infection. In Goldstone’s series2 there was only a 70 per cent te~hnique’.~.~’. Tissues should be handled gently, good correlation between superficial wound and graft culture results. haemostasis secured, and wound closure accurate. Haematoma, Patients with graft infection will usually have been in hospital seroma and lymphocele all provide excellent culture media and for some time and will generally be receiving antibiotics; are strongly associated with wound and graft infection’. colonization of skin and wounds by hospital commensals Routine vacuum drainage of groin wounds does not appear to becomes inevitable. Treatment of graft infection should not be prevent either lymphocele or wound infection48. Reoperation based solely on the results of superficial cultures. for early graft thrombosis or major haemorrhage significantly increases the risk of infection6. There are no trials comparing the use of a skin crease incision with vertical groin incision in Prevention an attempt to reduce local wound complications. Strategies for the prevention of infection are conveniently Vascular operations are usually performed in theatres of considered with respect to the periods before, during and after conventional design used principally for general surgery. This operation. Those who are debilitated, diabetic, uraemic, obese, practice may be inappropriate if airborne contamination is as on steroids or immunocompromised are at increased risk of important in the development of vascular prosthetic infection infection. In these high-risk patients grafting is usually best as it i s in joint replacement surgery. In orthopaedic operations, avoided other than to save life or limb. In all patients vein is provision of ultraclean air has been shown to reduce the rate the preferred conduit because of the reduced risk of infection of deep infection4’ by 78 per cent and infection rates of and the less serious consequences of any infection that may < 1 per cent are routinely achieved. The use of double gloving, develop2 3 . a no-touch technique and theatre clothing that is impermeable

clothing does not prevent all of these falling into the wound. That staphylococci resident on the skin of hospital staff may be multiresistant to antibiotics is of special concern. Whatever the mechanisms of perioperative contamination, an important risk factor in the pathogenesis of graft infection is poor surgical Up to 50 per cent of graft infections are associated with a surgical complication such as graft thrombosis, wound haematoma or lymphocele.

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to bacteria would seem wise, and does not require the large capital investment of installing ultraclean air systems”. Intravenous lines and the urinary catheter represent potential sources of bacteraemia and it seems prudent to remove these at the first opportunity. Wounds should not be tampered with unnecessarily; in this regard, transparent dressings have much to recommend them, allowing inspection of the wound while maintaining a barrier to infection. In patients in whom cultures of the aortic wall prove positive, Durham et al.I4 recommended 10 days of intravenous antibiotics followed by at least 6 months of oral therapy, but most vascular surgeons do not routinely obtain cultures from the aortic wall and question this recommendation. Haematogenous seeding of infection to a vascular graft is a continuing risk for as long as the graft remains in place. Dental work, manipulation of the genitourinary or gastrointestinal tract and, particularly, angiographic examinations all carry a risk of infection. It is sensible to cover all such procedures with antibiotics.

Clinical presentation

perigraft fluid allows microbiological culture to determine the significance of the radiological changes. This is of particular importance in patients presenting in the early period after operation, when the radiological changes of infection have to be differentiated from normal appearances after operation. The role of indium-labelled leucocyte scanning is debatable54.56.57; it has a sensitivity of 80 per cent but false A development of the technique positives are common54,56,58. using indium-labelled immunoglobulin G has shown both improved sensitivity and specificity for infection5’. Magnetic resonance imaging shows great promise and appears to be the best technique for defining the extent of graft infection60-62. Contrast sinography should be performed in all patients with an open wound or draining sinus. Angiography provides little help in confirming the presence or extent of graft infection but allows visualization of the distal vasculature before planned reconstruction. It may also demonstrate graft thrombosis or a false aneurysm. Gastroscopy is mandatory in the patient presenting with gastrointestinal bleeding. More than half the patients will prove to have reasons for bleeding other than graft-enteric fistula63.The examination must include the third and fourth parts of the duodenum and first few centimetres of the jejunum to exclude a fistula. Occasionally the graft itself will be visualized, but more commonly an ulcer, bleeding point, or merely an inflamed patch of mucosa are the only clues to the presence of a fistula. Conventional barium contrast studies have no role in the investigation of a suspected aortoduodenal fistula63.

The clinical manifestations of prosthetic vascular graft infection are protean and may be surprisingly subtle, making prompt diagnosis difficult. Early diagnosis is important in improving the prognosis5’. The majority of patients with a bypass involving the groin present with overt signs of wound sepsis such as abscess formation, development of a sinus track, cellulitis or graft exposure6. There is usually systemic upset, fever and leucocytosis. This pattern predominates in patients presenting within 1 month of surgery and diagnosis is not difficult. Less commonly, graft thrombosis, septic emboli, false Management aneurysm, or haemorrhage from the groin may indicate an The management of prosthetic vascular graft infection presents underlying graft infection. In these situations the problem may a formidable problem. Arresting haemorrhage, preservation of not be suspected until reoperation when pus is identified the limb circulation and control of sepsis are the priorities. surrounding the graft. These more insidious presentations Orthodox management involves revascularization via extraappear to be associated with infection by the low-virulence anatomic pathways and excision and debridement of infected organism S. epiderrnidi~’*’~.~ tissUe2.52,63. Recent reports have described the success of Infection of aortic prostheses is best classified into two aggressive non-operative treatment and of less radical groups, perigraft infection and graft-enteric fistula. In the series Infrainguinal and aortic graft infection are best of Goldstone and Cunningham, 38 per cent of patients with considered separately. In both situations supportive care should aortic graft infection had a graft-enteric fistula5’. Those with be intensive with high-dose antibiotic regimens and nutritional perigraft infection most commonly present with overt signs of support where appropriate. wound sepsis, but may have an indolent illness with malaise, low-grade fever, raised erythrocyte sedimentation rate and mild leucocytosis. The most common manifestation of graft-enteric Infrainguinal graft infection fistula is gastrointestinal bleeding, which occurs in about Once the diagnosis is established and the patency of the distal two-thirds of patients5’. The other third present with signs of vessels determined, standard management involves excision of sepsis without evidence of bleeding. The bleeding from a the graft and all infected tissue with vein patching of the graft-enteric fistula is usually acute and may be massive, arteriotomies. If the viability of the limb is in doubt, although chronic gastrointestinal bleeding occurs in up to revascularization is undertaken through non-infected tissue one-third of patients with a fistula. The nature of the bleeding using autogenous materials. If native vessels are patent, excision is closely related to the type of fistula: patients with acute of the graft alone may be sufficient to control sepsis while bleeding usually have an anastomotic fistula; those with a maintaining limb viability. In patients without suitable distal paraprosthetic fistula bleed chronically or not at all’. In some vessels for a bypass, amputation is usually advised7. Complete series of patients presenting with gastrointestinal bleeding who excision of the infected graft at amputation aids healing of the also had an aortic graft in situ, up to 75 per cent were found to have causes for bleeding other than graft-enteric f i s t ~ l a ~ ’ , ~ ~ .stump. The mortality rate associated with infrainguinal graft infection’ approaches 20 per cent. In the series of Kitka et al.7 In general, however, it is wise to assume that the cause of there was a particularly high mortality rate of 42 per cent in bleeding in patients with an aortic graft is a graft-enteric fistula patients undergoing attempted limb salvage. The authors until proven otherwise. advised early amputation in patients with severe sepsis and ischaemia. Less extensive surgical solutions and non-resectional Investigation treatment have been successfullye r n p l ~ y e d ~ ~ *Calligaro ~~-~’-~~. The initial investigation in patients with an infrainguinal graft et al.64 advise a graded approach to therapy. If the graft is should be ultrasonography. Perigraft fluid is suggestive of patent it is preserved; if it is occluded subtotal excision is infection and ultrasonographically guided aspiration can performed leaving a 4-mm cuff on the common femoral artery; confirm the diagnosis. The aortic segment is most effectively if there is anastomotic bleeding the whole graft is excised. In investigated using computed t ~ m o g r a p h y ~Perigraft ~ . ~ ~ . fluid, all cases infected tissue is radically debrided, intravenous gas, soft tissue swelling or false aneurysm formation are all antibiotics are given, and the wounds left open and treated with significant findings. Bowel wall thickening of > 5 mm is povidone-iodine-soaked dressings. Using this protocol they diagnostic for graft-enteric fistula55. Guided aspiration of have achieved a mortality rate of 11 per cent and an amputation

’.

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Prosthetic vascular graft infection: T. O'Brien and J. Collin

rate of 13 per cent. Non-resectional approaches t o the problem have included continuous antibiotic or antiseptic i r r i g a t i ~ n ~ and ~ . ~more ' . ~ ~recently the use of rotational muscle flaps to cover the infected groin w o ~ n d ~ ~Mixter . ~ ' . et ~ 1 . ~ ' achieved successful preservation of graft function in 20 of 21 patients using debridement, intravenous antibiotics and flap obtained healing in 13 of 14 patients coverage. Jorgensen et with groin infection with wound debridement and placement of gentamicin-impregnated collagen in the wound. The success of non-resectional therapy appears to depend on: ( 1 ) a patent graft; ( 2 ) localized infection; ( 3 ) no evidence of anastomotic disruption; and ( 4 ) surgical debridement of infected tissue.

References 1.

-

2.

3.

4. 5.

Aortic gruft infection 6. Conventional management of aortic graft infection involves extra-anatomic bypass through a non-infected clean field and 7. complete excision of the infected graft. Performing the bypass first has been shown to reduce both the mortality and amputation rates74. Nevertheless, the lowest mortality rates 8. r e ~ o r t e d ' ~ . ~are ' 10-25 per cent while rates of up to 70 per cent are not uncommon75. The operative procedures may be combined or staged. In the latter case excision is 9. performed 3-4 days after revascularization. In cases involving massive haemorrhage, however, control of bleeding must be 10. the first priority. Revascularization normally involves an axillofemoral graft with anastomosis to the common femoral artery in cases of aortoiliac infection, and to branches of the 11. superficial femoral or profunda femoris artery in cases of aortofemoral infection. A considerable technical problem surrounds management of the aortic stump. Disruption may occur in up t o 20 per cent 12. of cases5' and is almost always fatal. Thorough aortic debridement is essential and a two-layer closure using non-absorbable materials is advisable. Patching of the stump 13. using omentum7' or vascularized submucosal jejunal may help reduce the risk of disruption. Zn situ aortic replacement has also proved successful using both a u t o g e n o ~ s and ~~.~~ prosthetic' materials. Ehrenfeld et a1." reported a mortality rate of only 13 per cent in 24 patients using autogenous materials. Walker et ~ 1 . ' treated ~ 23 patients with aortoenteric fistula by excision and in situ prosthetic replacement. They achieved a perioperative mortality rate of 22 per cent and 89 per cent of survivors were alive 5 years after surgery. Jacobs et a/." recommended in situ prosthetic replacement in patients 17. with low-grade infection and negative perigraft and blood cultures. Extra-anatomic bypass is advised in patients with severe infection and positive cultures. 18. Partial excision may be appropriate in patients with localized infections confined to one limb of an aortobifemoral graft. Revascularization is then possible using femorofemoral 19. crossover, a graft through the obturator canals3 or an axillofemoral reconstruction. Non-resectional therapy, in which the infected graft is left in situ, has also proved s u c c e s s f ~ 7l 2~ ~ ~ ~ ~ 20. although its place in management is still to be defined. Localized groin infection may be treated by debridement and antibiotic i r r i g a t i ~ n ~ ~ . ~debridement '.~', and muscle flap c o ~ e r a g e ~ " ~ ' ~ , or debridement and placement of gentamicin-impregnated 21. ~ p o n g e ' ~ . ' ~Treatment . of panprosthetic infection is more problematic, although Quick et reported success in three 22. of four patients treated by continuous antibiotic irrigation.

Conclusions Prosthetic vascular graft infection presents a formidable diagnostic and therapeutic challenge, and carries a high mortality rate. Prevention remains preferable to therapy. Future developments include defining the role of antibioticbonded grafts in preventing and treating infection, and determining the place of non-resectional therapy compared with in situ graft replacement or graft excision with extra-anatomic bypass.

Br. J. Surg.. Vol. 79, No. 12, December 1992

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Paper accepted 7 June 1992

Announcement Euro pea n Su rg ica I Fel lowsh i ps Since 1990 the Council of The British Journal o f Surgery has awarded European Fellowships, each holding a value of up to E3000. Four Fellowships were awarded in 1990 and three in 1991. In 1992 the scheme was expanded to allow surgeons working in other European countries to visit the UK. Four fellowships were awarded in that year, to Mr D. C. Mitchell (London), Mr T. H. Brown (Manchester),Dr E. M. Targarona (Barcelona)and D r B. Nardo (Bologna). It is Council’s intention to offer European Fellowships once again in 1993. Applicants should submit details of their proposed itinerary and its anticipated costs, together with a curriculum vitae and two letters of support from senior colleagues. They should explain briefly how such a visit might broaden their experience and assist their career. Fellowships will not be awarded solely for the purpose of attending courses or meetings. Applications should be sent to the Company Secretary, Professor D. C. Carter, University Department ofSurgery,The Royal Infirmary, Edinburgh EH3 9YW, U K , by I February 1993.

D. C. Carter

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