Journal of Vascular Surgery
Volume 48, Issue 4 , Pages 815-820, October 2008

Aortoiliac aneurysms infected by Campylobacter fetus

  • Frédéric Cochennec, MD

      Affiliations

    • Department of Vascular Surgery, Henri Mondor Hospital, Créteil, France
    • Corresponding Author InformationReprint requests: Frédéric Cochennec, Henri Mondor Hospital, 51 av du Maréchal de Lattre de Tassigny, 94000 Créteil, France
    • ,
  • Laure Gazaigne, MD

      Affiliations

    • Department of Medical Microbiology and Infectious Diseases, Henri Mondor Hospital, Créteil, France
    • ,
  • Philippe Lesprit, MD

      Affiliations

    • Department of Medical Microbiology and Infectious Diseases, Henri Mondor Hospital, Créteil, France
    • ,
  • Pascal Desgranges, MD, PhD

      Affiliations

    • Department of Vascular Surgery, Henri Mondor Hospital, Créteil, France
    • ,
  • Eric Allaire, MD, PhD

      Affiliations

    • Department of Vascular Surgery, Henri Mondor Hospital, Créteil, France
    • ,
  • Jean-Pierre Becquemin, MD, FRCS

      Affiliations

    • Department of Vascular Surgery, Henri Mondor Hospital, Créteil, France

Received 12 March 2008; accepted 28 May 2008. published online 11 August 2008.

Article Outline

Purpose

Few reports of aortoiliac aneurysms infected by Campylobacter fetus are available. We report five cases and review previous reports, with a view to describing the clinical pattern, treatment options, and outcome of this infection.

Methods

During a 10-year period, 21 patients were diagnosed with C fetus infection in the Department of Clinical Microbiology, five of whom had an infected arterial aneurysm. We retrospectively reviewed their medical charts. Diagnosis was made on the basis of clinical presentation, computed tomography scan, perioperative findings, and identification of C fetus in at least one blood culture or culture from an aneurysm specimen. Late outcome of surviving patients was assessed by telephone interview.

Results

We identified four aortic aneurysms and one hypogastric aneurysm. All patients were seen in an emergency setting. Five had fever and abdominal pain, and three had contained rupture. Campylobacter fetus was found in blood cultures of four patients and in the aneurysm specimen of one patient. Three patients were treated by open repair and two by endovascular repair. One patient treated endovascularly died from septic shock due to C fetus at 2 weeks. One patient treated by open surgery underwent reoperation for persistent infection. The remaining patients were cured, but one died at 5 months of an unrelated cause. All surviving patients received long-term antibiotic therapy.

Conclusion

Campylobacter fetus infection of aortoiliac aneurysms is a serious condition with a high rate of rupture. However, long-term success can be obtained with prompt surgical treatment and an appropriate antibiotic regimen. The benefits of stent grafts remain debatable.

 

Infected abdominal aortic aneurysms (AAA) are rare and remain one of the most challenging issues for vascular surgeons. Traditionally, the most frequently reported organisms are Salmonella, Staphylococcus, and Streptococcus.1, 2 Recently, an increasing number of other organisms have been found that have changed the spectrum of AAA infections. During the two last decades, Campylobacter fetus has emerged as a pathogen responsible for serious systemic disease, with bacteremia and propensity to invade the vascular endothelium. Few studies on AAA infected by C fetus have been published since the first case was reported by Dolev et al.3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17 We analyzed all cases of AAA infected by C fetus diagnosed in our institution during the past 10 years and reviewed previous English-language publications to better define the epidemiologic, clinical, and bacteriologic characteristics of the disease and treatment options.

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Patients and methods 

We reviewed data from the Henri Mondor Hospital microbiology laboratory between 1997 and 2006 to identify C fetus infections and found 21 cases.

Blood cultures were grown in an automated BacT/Alert system (bioMérieux, Marcy l'Etoile, France) at the Department of Clinical Microbiology. Direct examination showed gram-negative spirally curved and actively motile rods. The organisms were grown on Columbia blood agar and chocolate agar incubated in microaerophilic conditions. Organisms were identified by an oxidase-positive reaction, with an ability to grow at 25° and 37°C but not at 42°C and by using the API Campy strip (bioMérieux). If necessary, identification was further confirmed with a molecular method: DNA extraction using the QIAamp DNA minikit (Qiagen, Hilden, Germany), polymerase chain reaction amplification and sequence analysis of an internal fragment of the 16S rDNA, as described by Bosshard et al.18

Susceptibility to antibiotics was tested using a disk diffusion method on Mueller-Hinton blood agar according to the guidelines of the Comité de l'Antibiogramme de la Société Française de Microbiologie.19 Minimum inhibitory concentrations were determined by the E-test (AB Biodisk, Solna, Sweden) according to the manufacturer's recommendations.

We retrospectively analyzed the case report forms for the 21 patients and identified four AAAs and one hypogastric aneurysm infected by C fetus. The diagnosis of aortic or hypogastric infection by C fetus was based on clinical presentation, computed tomography (CT) scan, perioperative findings, and identification of C fetus in at least one blood culture or culture from an aneurysm specimen. Late outcomes of surviving patients were assessed by telephone interview. The median follow-up was 12 months (range, 2 weeks-6 years).

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Results 

All patients were men with a mean age of 76 ± 4 years (range, 69-79 years). Detailed data concerning clinical pattern, treatment options, and outcome are presented in Table I.

Table I. Presentation, treatment, and outcome in patients with abdominal aortic aneurysm infected by Campylobacter fetus
PatientAge/sexPre-existing illnessSymptomsMaximal transverse diameter on CT scan (mm)Findings on CT scanBlood cultureSpecimen cultureTime of diagnosisOperationOutcome
169/MChronic lymphocytic leukemia, COPD, CADFever, abdominal pain, fatigue, weight loss89Contained ruptured AAAPositiveNegativePost-opDacron bifurcated graftProsthetic infection by C fetus 2 weeks post-op. Reintervention: prosthetic graft excision, aortofem and femfem bypasses with autogenous superficial fem vein. A/W at 6 months
276/MTuberculosis, alcoholismFever, back pain, fatigue, weight loss84Contained ruptured AAANegativePositivePost-opDacron tube graftDeath unrelated to infection 5 months post-op
376/MCOPD, CADFever, abdominal pain110Contained ruptured AAA, periaortic bubblesPositiveNDPost-opZenith bifurcated stent graftSeptic shock and death 2 weeks post-op
479/MLung cancer, COPD, CAD, PVD, iliac aneurysmFever, abdominal pain, diarrhea70Rapidly enlarging hypogastric aneurysmPositiveNDPre-opZenith aortomonoiliac stent graftA/W at 6 years. No recurrent infection
579/MPancreatic cancerFever, abdominal pain60Inflammatory AAAPositiveNegativePre-opAortoaortic bypass grafting with arterial cryopreserved allograftA/W at 18 months. No recurrent infection

AAA, Abdominal aortic aneurysm; A/W, alive and well; CAD, coronary artery disease; COPD, chronic obstructive pulmonary disease; CT, computed tomography; ND, not done; PVD, peripheral vascular disease.

Clinical pattern 

All patients presented with abdominal or back pain and fever. The abdominal pain was sudden in four patients, but none of them were hemodynamically unstable. Other major clinical features were asthenia and weight loss (n = 2) and gastrointestinal symptoms with diarrhea (n = 1). All patients had multiple comorbidities, including coronary artery disease (n = 3), hypertension (n = 3), peripheral vascular disease (n = 1), and chronic obstructive pulmonary disease. Four patients had immunodeficiency caused by severe alcoholism (n = 1) or malignancy (n = 3). Pre-existence of an arterial aneurysm was known before admission only for the patient with the hypogastric aneurysm. This patient had been treated by embolization 18 months before. Physical examination revealed an abdominal pulsating mass in four patients. Leukocytosis was present in all patients.

CT scan confirmed diagnosis of contained ruptured AAA in three patients. CT scan in the patient with the hypogastric aneurysm showed a rapidly enlarging aneurysm that grew from 30 to 70 mm in 8 months. Mean maximal diameter was 82.6 ± 19.1 mm (range, 60-110 mm). Aneurysms in three patients had an irregular and saccular shape, whereas fusiform aneurysms were observed in the other two patients. One patient had a thickened aortic wall, which was interpreted as an inflammatory aneurysm.

Bacteriologic findings 

Campylobacter fetus was isolated from the blood cultures of four patients. Among these patients, cultures from surgical specimens were negative (n = 2) or were not tested (n = 2). Blood cultures in one patient were negative, but C fetus was recovered from specimens of the excised aneurysm and intraluminal thrombus. All patients received antibiotics before surgery.

The primary source of infection remained unknown in all cases. Campylobacter fetus grew in blood culture in a median of 2 days. Because of the rarity of digestive symptoms, stool cultures were not tested. All C fetus isolates were susceptible to amoxicillin, amoxicillin-clavulanate, imipenem, gentamicin, and chloramphenicol. Two strains had intermediate susceptibility to cefotaxime. One isolate was resistant to ciprofloxacin, two isolates were resistant to tetracycline, and one was resistant to erythromycin. As expected, all isolates were resistant to nalidixic acid.

Treatment 

Operations were done as emergency procedures for four patients, and elective surgery was done for one. We performed open surgery in three cases and endovascular repair in two. Open surgery consisted of local débridement of the aneurysm wall and infected tissues with in situ reconstruction. In situ reconstructions included interposition of a polyester graft in two patients because the infectious process had not been recognized preoperatively and aortoaortic bypass grafting with an arterial cryopreserved allograft in one patient. Endovascular procedures were performed using a Zenith (Cook, Bloomington, Ind) bifurcated stent graft (n = 1) and a Zenith aortomonoiliac stent graft associated with a prosthetic femorofemoral bypass (n = 1). Although the diagnosis of infected aneurysm had been established preoperatively in one of those patients, we decided to treat him endovascularly because of multiple comorbidities. In the other patient who received endovascular treatment, the infectious process had not been recognized preoperatively.

Among the patients treated by open repair, no purulent material was evident at surgery. The patient with the inflammatory aneurysm detected by CT scan had a fibrous adhesion to the mesentery, retroperitoneal edema, and a thickened aneurysm wall. No aortoenteric fistula was detected.

Patients received various antibiotic regimens. Initial treatment was mostly based on intravenous amoxicillin-clavulanate (n = 3) or imipenem (n = 3), alone or combined with gentamicin. Treatment was switched to oral amoxicillin (n = 2) or amoxicillin-clavulanate (n = 3) once fever had improved and levels of inflammatory markers had decreased. At discharge, surviving patients were prescribed long-term antibiotic therapy.

Outcome 

Two patients died during the follow-up period. One, who had a contained ruptured AAA at admission, died from septic shock due to C fetus 2 weeks after the operation. This patient had received endovascular treatment because the C fetus infection was not diagnosed preoperatively. One patient who underwent interposition with a polyester tube graft died 5 months after the operation from an unrelated cause. He did not present any sign of recurrent infection on a follow-up CT scan 2 months before. Among the three remaining patients, symptoms in two cleared without clinical or radiologic evidence of recurrent infection, one at 18 months and the other at 6 years. Treatment consisted of open surgery with interpositioning of an allograft in one patient and a Zenith aortomonoiliac stent graft in the other. One patient had persistent infection. This patient had been treated by interposition of a polyester graft, and fever did not subside after surgical treatment despite appropriate antibiotic therapy. A follow-up CT scan revealed the presence of perigraft fluid (Fig). He underwent reoperation consisting of complete prosthetic graft removal and reconstruction with aortofemoral and femorofemoral bypasses using autogenous femoral superficial veins 2 weeks after the first operation. He was free of symptoms 6 months after reoperation.

  • View full-size image.
  • Fig. 

    A, This computed tomography (CT) scan was obtained in a patient with a ruptured abdominal aortic aneurysm infected by Campylobacter fetus that was treated by open surgery with interposition of a polyester graft. B, A control CT scan taken 10 days after surgery disclosed persistent infection with periprosthetic collection.

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Discussion 

In the past, Campylobacter species have been typically considered as pathogens of a wide range of domestic animals. However, they are now increasingly implicated in human disease. The Campylobacter genus contains three main pathogenic species: C jejuni, C coli, and C fetus. Campylobacter jejuni and to a lesser extent C coli are major causes of enterically transmitted bacterial syndromes, ranging from asymptomatic carriage to dysentery and inflammatory ileocolitis. They affect all ages and healthy patients. These organisms are recovered from the feces and, in rare cases, can be simultaneously grown from the blood. In contrast, C fetus is rarely isolated from stools and shows a special tropism for the human vascular endothelium. It is responsible for serious infections in elderly or immunosuppressed patients20 and has been associated with relapsing bacteremia,21 endocarditis,22 pericarditis,23 thrombophlebitis,24 meningitidis,25 arthritis,26 osteomyelitis,27 cellulitis,28 pneumonia,29 and mycotic aneurysms.30 However, involvement of C fetus in infected aortic aneurysms is rare, and to the best of our knowledge, only 15 cases have been previously published in English.3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17

Until a few years ago, C fetus infections were probably underdiagnosed. Nowadays, they seem to be recognized more frequently because of improved bacteriologic technologies, medical awareness, and a growing number of immunodeficient patients.31 The epidemiology and pathogenesis of C fetus infections are yet to be fully understood due to the rarity of the disease. Different modes of transmission have been suggested: direct contact with animals, ingestion of contaminated food or water, and spread by endogenous route.5, 20 Among our patients, the primary source of infection was unknown, and none of them reported contact with animals. The vascular tropism of C fetus has been linked to the presence of a surface receptor with high affinity to the endothelium and production of a local procoagulant that promotes thrombus formation.32 Campylobacter fetus is typically distinguished from C jejuni and C coli on the basis of its ability to grow well at 25° and 37°C, but not at 42°C, and its susceptibility to cephalothin but resistance to nalidixic acid.

Diagnosis of the disease is based on clinical presentation, CT scan, perioperative findings, and identification of C fetus in blood cultures or from specimens of the aneurysm. In our patient series, the most common symptoms were fever and abdominal or back pain. Three patients presented with a contained ruptured AAA, which is consistent with other studies: among 15 previously reported patients, 8 (53%) had a ruptured aneurysm.3, 4, 5, 7, 10, 12, 14, 15

Neither symptoms nor CT scan results are specific to AAAs infected by C fetus. Indeed, CT scans may show a saccular shape of the aneurysm, a thickened aortic wall, or periaortic ectopic gas; all these abnormalities may be present in patients with AAA infected by other organisms.33 However, of particular interest in our series, we additionally identified an inflammatory aneurysm in one patient. No previous study has demonstrated that inflammatory aneurysms are more susceptible to bacterial infection, but the ability for C fetus to infect inflammatory aortic aneurysms has already been proposed by Marty et al.7 This observation was based on the association of acute neutrophil infiltration with the chronic inflammatory infiltrate of inflammatory aneurysms. In one of our patients, the aortic aneurysm enlarged very rapidly. This characteristic has previously been reported, in some cases resulting in rupture.8, 10, 11, 13 None of our patients had periaortic collection. This is consistent with previous studies in which fibrous reaction in the retroperitoneum was far more common than periaortic collection.

Blood cultures were the only definitive diagnostic tool for four patients. One patient, who received antibiotics before blood samples were taken, remained negative, and diagnosis was made by isolation of the organism from multiple specimens of the aneurysmal wall. Some authors recommend that incubation of cultures should be extended to 2 weeks because of the rather slow growth of the organism.28

Similarly to other cases of aortic sepsis, management of AAA infected by C fetus is very challenging.34, 35 The most appropriate surgical treatment remains unclear. Conventional management of AAA sepsis involves excision of all infected tissues and ligation of the infrarenal aorta, followed by extra-anatomic arterial reconstruction. Despite its theoretic advantage of a lower risk of graft infection, this treatment strategy has been associated with a significant mortality rate and adverse outcomes such as low 5-year patency and high amputation rates, risk of dramatic aortic stump blow-out, and thrombosis ascending toward the renal arteries. Furthermore, intraoperative contamination of the graft is not rare, and secondary infections have been noted in 5% to 30% of cases in recent studies.36, 37, 38, 39, 40 None of our patients underwent this procedure. Our current practice is now to limit the indications for extra-anatomic reconstruction to infected patients in poor general condition and with a short life expectancy. Among the 15 previously published cases of AAA infected by C fetus, four were treated with axillobifemoral bypass.6, 8, 12, 13 Three were alive with no apparent sign of recurrent infection at 45, 36, and 18 months, respectively, and one died on postoperative day 7 (Table II).3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17

Table II. Treatment and outcome in published cases of abdominal aortic aneurysms infected by Campylobacter fetus
First authorAge (years)Ruptured AAAOperationPost-op antibioticsOutcome
Dolev368YesReplaced with polyester graftNDDied a few hours post-op
File463YesNDNDDied pre-op
Taylor567YesNDNDDied pre-op
Anolik673NoAneurysm excision, AXBFLong-termA/W at 45 months
Marty754YesReplaced with polyester graft7monthsA/W at 2 years
Blabey868NoAneurysm excision, AXBF7weeksA/W at 18 months
Righter956NoReplaced with polyester graft1weekA/W at 3 years
Perry1070YesReplaced with polyester graft8weeksA/W at 6 months
Rutherford1159NoReplaced with polyester graft5monthsA/W at 2 years
Jacobs1264YesAneurysm excision, AXBFNDDied 7 days post-op
Kato1361NoAneurysm excision, AXBF2weeksA/W at 36 months
Allerberger1484YesNDNDDied pre-op
Grollier1556YesReplaced with polyester graftNDND
Mii1645NoReplaced with polyester graft3monthsA/W at 1 year
Tran1778NoReplaced with polyester graftLong-termA/W at 9 months

AAA, Abdominal aortic aneurysm; A/W, alive and well; AXBF, axillofemoral bypass; ND, not done or not described.

To minimize the adverse effects of extra-anatomic reconstruction in AAA sepsis, alternative approaches have been described. Recent studies have demonstrated that in situ reconstruction with cryopreserved allografts,41, 42, 43, 44, 45 lower extremity deep veins,46 and standard,35, 47 silver-coated,48 or antibiotic-bonded38 prosthetic grafts give long-term good results. However, no randomized trials have been published, and comparisons among series are difficult due to the heterogeneity of patients and different follow-up strategies. Two of our patients and seven previously reported patients with AAA infected by C fetus underwent reconstruction with prosthetic grafts. Of these patients, one died a few hours after the operation, one died 5 months after the operation, six survived without recurrent infection with a median follow-up period of 18 months (range, 6-36 months), and one had persistent infection (Table I, Table II). Despite successful treatment of C fetus-infected AAA patients by interposition of a prosthetic graft, this approach has been associated with frequent reoperation with other gram-negative organisms. We therefore recommend the use of cryopreserved allograft or autogenous veins rather than a prosthetic graft in C fetus-infected AAAs, but further studies are necessary.

Several reports demonstrating successful endovascular repair of infected AAA associated with other organisms have been published,49, 50, 51 and this technique may provide a less invasive alternative. Endovascular treatment of infected AAA has not been widely practiced, however, and its long-term efficacy has not been established.51 Some authors have suggested that the indications for this procedure should be limited to aortic infections with low-virulence organisms and absence of gross purulence.52 A major disadvantage is the lack of débridement of infected tissues, which may result in the spread of the septic process in the retroperitoneum. Two patients in our series received endovascular treatment. One died of sepsis. We could not determine whether the septic shock was related to persistent infection of retroperitoneal tissues or infection of the stent graft. Débridement and drainage of the retroperitoneal collection after stent graft implantation should have been discussed. The other patient survived without sign of recurrent infection 6 years after operation, and to our knowledge, this is the only published case to date of C fetus–infected AAA successfully treated by endovascular repair.

Appropriate antimicrobial therapy based on susceptibility testing should be started immediately after diagnosis; however, the optimal treatment of C fetus sepsis remains poorly defined. Two in vitro studies done in Quebec found significant differences in β-lactam susceptibility31, 53: although all strains appeared susceptible to amoxicillin and imipenem, the 90% minimal inhibitory concentrations were markedly lower for imipenem (≤0.06 for imipenem; 2 μg/mL for amoxicillin). The bactericidal activity of cefotaxime has been previously found to be lower than that of amoxicillin or imipenem, and treatment failure with third-generation cephalosporins has been reported.28 Erythromycin is not recommended for the treatment of C fetus bloodstream infection, despite in vitro susceptibility to this drug, because several cases of failure have been reported.28 In our series, the three patients who were initially treated with imipenem were cured. Two patients receiving amoxicillin-clavulanate died. Although we cannot make any definite conclusions based on a small number of cases, our data suggest that imipenem should be the preferred first-line agent for the treatment of arterial aneurysms infected by C fetus. Depending on susceptibility tests, a switch to amoxicillin with or without clavulanate can be made once the situation is stabilized. In previous reports, the postoperative term for antibiotic treatment varied from 7 days9 to long-term therapy.6 The optimal duration of treatment remains uncertain, although a minimum of 3 to 4 weeks of intravenous antimicrobial therapy has been advocated.19

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Conclusions 

AAA infected by C fetus is a serious disease with a high rate of rupture. Among 20 reported cases, the 30-day mortality rate was 29%. Early diagnosis, prompt surgical treatment, and appropriate antibiotic therapy are essential. Experience with endovascular repair is limited, but this procedure may offer a benefit, especially in critically ill patients.

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Author contributions 


Conception and design: FC, JB

Analysis and interpretation: FC, JB, PL

Data collection: FC, LG, PD, EA, JB

Writing the article: FC, JB, PL

Critical revision of the article: FC, JB

Final approval of the article: FC, LG, PL, PD, EA, JB

Statistical analysis: FC

Obtained funding: FC

Overall responsibility: JB

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 Competition of interest: none.

PII: S0741-5214(08)00924-5

doi:10.1016/j.jvs.2008.05.076

Journal of Vascular Surgery
Volume 48, Issue 4 , Pages 815-820, October 2008

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