Surg Today (2007) 37:1053–1059DOI 10.1007/s00595-007-3549-x

Reprint requests to: P. BianchiReceived: October 7, 2006 / Accepted: February 8, 2007

Late Gastrointestinal Bleeding After Infrarenal Aortic Grafting: A 16-Year Experience

PAOLO BIANCHI, ILIAS DALAINAS, FABIO RAMPONI, DANIELA DELL’AGLIO, RENATO CASANA, GIOVANNI NANO, GIOVANNI MALACRIDA, and DOMENICO G. TEALDI

Department of Vascular Surgery, IRCCS Policlinico San Donato, University of Milan, Via Morandi 30, 20097 San Donato Milanese, Milano, Italy

AbstractPurpose. To review the manifestation and management of gastrointestinal (GI) bleeding caused by secondary aortoenteric fi stula (AEF) after infrarenal aortic grafting.Methods. Between 1991 and 2006, nine patients under-went emergency treatment for secondary AEF localized in the duodenum (78%), ileum (11%), or sigmoid colon (11%). Three (33%) patients suffered hypovolemic shock. There were two (22%) real fi stulas and seven (78%) paraprosthetic fi stulas. Graft infection was con-fi rmed in four (45%) patients and four (45%) had proxi-mal sterile pseudoaneurysms. Surgical management consisted of graft removal with (n = 5) or without simul-taneous extra-anatomic bypass (n = 1), in situ Dacron graft interposition (n = 3), ileo-duodenorrhaphy (n = 8), sigmoidectomy with colostomy (n = 1), and segmentary ileectomy (n = 1). Endografting was used only as a tem-porary measure to control bleeding in two patients.Results. The mortality rate was 55% (n = 5). There were no intraoperative deaths, but 75% of the septic patients, 66% of those with preoperative hemodynamic instabil-ity, 50% of those with pseudoaneurysms, and 100% of those who required bowel resection died during the early postoperative period. Moreover, all of the surviv-ing patients suffered early postoperative morbidity, resulting in prolonged intensive care unit stay and hospitalization.Conclusions. Secondary AEF is life-threatening, diffi -cult to treat, and associated with high morbidity and mortality, especially in patients with sepsis or hemody-namic instability and those requiring bowel resection.

Key words Gastrointestinal bleeding · Secondary aortoenteric fi stula · Infrarenal aortic grafting · Graft infection · Aortic pseudoaneurysm

Introduction

Gastrointestinal (GI) bleeding from a secondary aorto-enteric fi stula (AEF) is an uncommon but serious late complication of the infrarenal aortic grafting after reconstructive vascular surgery, performed years earlier for aneurysmatic or obstructive disease of the aortoiliac district.1–3 According to Vollmar and Kogel’ classifi ca-tion,4,5 secondary AEF may present as a true communi-cation between the lumen of the bowel and the lumen of the aortic graft (true AEF) or as an ulceration of the bowel wall caused by chronic decubitus on the aortic graft (paraprosthetic AEF). In true AEF, the bleeding comes from the direct passage of blood from the aorta to the bowel, whereas in paraprosthetic AEF, hemor-rhage generally comes from the bleeding vessels in the bowel after wall ulceration. The incidence of secondary AEF ranges from 0.4% to 4% in different series.5 The fi stula often develops at the level of the proximal aortic anastomosis at the site of anastomotic disruption.

Graft infection often predisposes to the formation of an AEF,4,6 representing a site for bacterial contamina-tion from the bowel to the aortic graft. On the other hand, an AEF may cause graft infection, with or without anastomotic false aneurysm formation, or it may be caused by a chronic collection of periprosthetic puru-lent fl uid or an infected anastomotic aneurysm through both erosive and infective mechanisms. It may also be associated with a sterile anastomotic false aneurysm.4,6 A proximal aortic pseudoaneurysm may rupture in the bowel with an acute true AEF formation or it may cause chronic erosion or ulceration of the bowel wall with a paraprosthetic AEF.

1054 P. Bianchi et al.: Late GI Bleeding After Infrarenal Aortic Repair

The duodenum and the ileum are the most common sites of bleeding because of their anatomical relation-ship with the proximal anastomosis of the infrarenal aortic reconstruction. For this reason, AEF generally manifests as hematemesis and melena, suggesting an upper GI tract origin.2,7 Bleeding may be acute and massive, indicating a true AEF, or it may be silent and intermittent,8,9 but severe, with progressive anemia, more suggestive of a paraprosthetic AEF, and making the diagnosis diffi cult in the non-bleeding interval. Occasionally, a colonic fi stula manifests as proctorrha-gia,10 and the GI hemorrhage may be accompanied by fever and other symptoms indicative of infection.

This single-institution retrospective study reviews the manifestations and management of GI bleeding related to secondary AEF.

Methods

Between 1991 and 2006, nine men who had undergone previous infrarenal aortic grafting were treated for GI bleeding caused by secondary AEF in our Emergency Department. The mean age of the patients was 70.6 years (range 47–83 years) and the mean interval between the primary aortic intervention and the diagnosis of sec-ondary AEF was 7.2 years (range 1–24 years). Five (55%) patients had undergone primary aortic recon-

struction at our institution. During the same period, 2194 infrarenal aortic procedures were performed in our institution, resulting in an overall incidence of 0.42%.

The indications for initial abdominal aortic grafting were aneurysmal disease in four (45%) patients and occlusive disease in fi ve (55%) patients, with corre-sponding proximal end-to-end and end-to-side aortic anastomotic reconstruction, respectively (Table 1). Seven (78%) patients with bleeding from the duodenal third portion and one (11%) with bleeding from the ileum presented with hematemesis and melena, whereas one (11%) with an AEF involving the sigmoid colon presented with proctorrhagia. Hypovolemic shock and hemodynamic instability were evident in three (33%) patients with massive hematemesis, but this allowed for a completion of the diagnostic phase before interven-tion. Three (33%) patients had a chronic percutaneous groin fi stula with bleeding or purulent secretions, or both, indicating aortofemoral graft infection.

Diagnosis was made using endoscopy and angio-computed tomography (CT). Esophagogastroduode-noscopy, which extended distally into the third and fourth duodenal portions, was performed fi rst to exclude the more common causes of bleeding and to detect the fi stula, whereas angio-CT showed evidence of graft infection, anastomotic false aneurysm, or a fi stula itself as the passage of contrast-medium from the aorta to the bowel lumen. Angiography was performed only in three

Table 1. Characteristics of the nine patients with AEF after infrarenal aortic grafting

Patient no.

Age (years) Sex Date

∆ time (years) Hospital Primary disease Anamnesis

Primary graft reconstruction

1 47 M 1991 5 Other Obstructive Hypertension, CAD Aorto-bifemoral bypass

2 73 M 1993 2 PSD Infrarenal AAA Hypertension, COPD, AF Aorto-iliac/femoral graft

3 70 M 1995 8 PSD Obstructive Hypertension, COPD, AF/ anticoagulants, femoral pseudoaneurysm

Aorto-bifemoral bypass

4 76 M 1998 1 Other Ruptured infrarenal AAA

COPD, CAD/AMI, chronic renal impairment

Aorto-bisiliac graft

5 73 M 2001 2 PSD Ruptured infrarenal AAA

Cardiomyopathy/EF35%, pace-maker

Tube graft + double stent-graft for proximal aortic pseudoaneurysm

6 57 M 2003 5 Other Obstructive Hypertension, COPD Aorto-bifemoral bypass

7 76 M 2005 24 PSD Obstructive Hypertension, gastrectomy, PAOD, femoral pseudoaneurysms

Aorto-bifemoral bypass

8 83 M 2005 12 PSD Infrarenal AAA Hypertension, ictus cerebri, COPD

Aorto-bifemoral graft

9 81 M 2006 6 Other Obstructive Hypertension, COPD, CAD Aorto-bifemoral bypass

PSD, Policlinico San Donato; CAD, coronary artery disease; COPD, chronic obstructive pulmonary disease; AF, atrial fi brillation; AMI, acute myocardial infarction; PAOD, peripheral arterial obstructive disease; M, male

P. Bianchi et al.: Late GI Bleeding After Infrarenal Aortic Repair 1055

patients, during the fi rst phase of our experience, when other diagnostic methods were not as effective as they are now for detecting AEF. There were two (22%) true AEFs caused by the rupture of a sterile pseudoaneu-rysm in the duodenum and seven (78%) paraprosthetic AEFs. Although the graft is always considered contami-nated, graft infection was confi rmed in four (45%) patients, all of whom had a paraprosthetic AEF. Four (45%) patients had a proximal aortic false aneurysm, which was sterile because it was not related or second-ary to graft infection (Table 2).

Surgery was performed using a transabdominal approach via a xipho-pubic median laparotomy in all the patients because it allowed good exposure of the entire abdominal aorta. Aortic control was safely achieved proximally below the renal arteries in seven patients. Pseudoaneurysm supra-renal aortic clamping

was required in two patients because surgical prepara-tion of the juxtarenal aorta and anastomotic aneurysm proved extremely diffi cult inside an intensely fi brotic atmosphere.

Vascular surgery consisted of graft removal with closure of the aortic stump using introverted sutures and omental wrapping to prevent infection in fi ve patients (three with graft infection), with simultaneous extra-anatomic axillo-bifemoral bypass in four, and bilateral axillo-popliteal bypass with reinforced expanded polytetrafl uoroethylene (e-PTFE) in one; removal of a double stent-graft previously delivered to exclude a proximal aortic anastomotic aneurysm, unsuc-cessfully, in one patient; graft removal without simulta-neous extra-anatomic bypass in one patient, whose old graft was infected, resulting in chronic obliteration without clinical evidence of lower limb ischemia requir-

Table 2. Clinical presentation and diagnostic work-up

Graft infectiona

Proximal aortic false aneurysm

True AEF

Paraprosthetic AEF

Hypovolemic shock Clinics Disease Diagnosis

1 ✓ ✓ Hematemesis Duodenum’s decubitus on infected graft

EGDS, aortography, angio-CT scan

2 ✓ ✓ ✓ Hematemesis, abdominal pulsation

Sterile false aneurysm ruptured in duodenum III

EGDS, aortography, angio-CT scan

3 ✓ ✓ Abdominal pain for 1 month, hematemesis, melena

Duodenum’s decubitus on sterile false aneurysm

EGDS, aortography, angio-CT scan

4 ✓ ✓ Hematemesis and melena

Duodenum’s decubitus on sterile false aneurysm

EGDS, aortography, angio-CT scan

5 ✓ ✓ ✓ Hematemesis and melena

Sterile false aneurysm ruptured in duodenum

Aortography, angio-CT scan

6 ✓ ✓ Hematemesis, cutaneous groin fi stula

Duodenum’s decubitus on infected graft

EGDS, angio-CT scan

7 ✓ Hematemesis Duodenum’s decubitus on sterile graft

EGDS, angio-CT scan

8 ✓ ✓ Abdominal pain and pulsation, proctorrhagia, bleeding groin fi stula

Sigmoid’s decubitus on infected graft

Colonoscopy, angio-CT scan

9 ✓ ✓ ✓ Hematemesis, cutaneous groin fi stula

Duodenum’s decubitus on obliterated infected graft

Angio-CT scan, EGDS

AEF, aortoenteric fi stula; EGDS, esophago-gastro-duodenoscopy; CT, computed tomographya Confi rmed graft infection on the basis of clinical history, blood examination results, and abdominal imaging (periprosthetic purulent fl uid col-lection with air content)

1056 P. Bianchi et al.: Late GI Bleeding After Infrarenal Aortic Repair

ing revascularization at the time of intervention; and in situ reconstruction with graft interposition in three patients without graft infection, two of whom under-went Dacron tube-graft interposition between the prox-imal aorta and the distal-end of the old graft and one of whom underwent new bifurcated bovine-pericardium reconstruction. Endografting with a straight PowerLink (Endologix, Irvine, CA, USA) was performed in two patients as a temporary measure to control GI bleeding and hemodynamics, followed as soon as possible by sur-gical intervention (Table 3).

Gastrointestinal surgery, which was performed by general surgeons after the vascular phase, consisted of ileo-duodenorrhaphy in eight patients, sigmoidectomy with colostomy in one, and secondary partial ileectomy during the early postoperative period for segmental mesenteric infarction at the site of previous ileorrhaphy disruption in one (Table 3).

Data were analyzed using the SPSS software package for Windows version 13.0 (SPSS, Chicago, IL, USA). The Kaplan–Meier method was used to calculate the cumulative survival.

Results

In-hospital mortality was 55% (n = 5). All fi ve deaths occurred during the early postoperative period as a result of sepsis or multiple organ failure (MOF) or both in four patients, and as a result of bowel infarction in one. Notably, the patients who died consisted of three (75%) of the four septic patients with graft infection, two (66%) of the three patients with hemodynamic instability at presentation; two (50%) of the four patients who required extensive intervention for a pseudoaneu-rysm, and the patient (100%) who required bowel resection.

Table 3. Operative details

Graft infection

Proximal aortic false aneurysm

True AEF

Paraprosthetic AEF Access to aorta

Clamping level Reconstruction Prosthesis

1 ✓ ✓ Xipho-pubic median laparotomy

Infrarenal Graft removal + axillo- bifemoral bypassDuodenorrhaphy

Reinforced e-PTFE

2 ✓ ✓ Xipho-pubic median laparotomy

Infrarenal Tube graft interpositionDuodenorrhaphy

Dacron knitted

3 ✓ ✓ Xipho-pubic median laparotomy

Infrarenal Tube graft interpositionDuodenorrhaphy

Dacron knitted

4 ✓ ✓ Xipho-pubic median laparotomy

Suprarenal Graft removal + new bifurcated graft reconstructionIleorrhaphy

Bovine pericardium

5 ✓ ✓ Xipho-pubic median laparotomy

Suprarenal Graft/stent-graft removal + axillo- bifemoral bypassDuodenorrhaphy

Reinforced e-PTFE

6 ✓ ✓ Xipho-pubic median laparotomy

Infrarenal Stent-grafta

Graft removal + axillo- bifemoral bypassDuodenorrhaphy

Reinforced e-PTFE

7 ✓ Xipho-pubic median laparotomy

Infrarenal Stent-grafta

Graft removal + axillo- bifemoral bypassDuodenorrhaphy

Reinforced e-PTFE

8 ✓ ✓ Xipho-pubic median laparotomy

Infrarenal Graft removal + bilateral axillo- popliteal bypassSigmoid-colectomy with colostomy

Reinforced e-PTFE

9 ✓ ✓ Xipho-pubic median laparotomy

Infrarenal Obliterated graft removalDuodenorrhaphy

—

AEF, aortoenteric fi stula; e-PTFE, expanded polytetrafl uoroethylenea Initial stent-grafting was performed as bridging intervention before surgical repair to achieve hemostasis

P. Bianchi et al.: Late GI Bleeding After Infrarenal Aortic Repair 1057

All the surviving patients suffered early postopera-tive major and minor morbidity and it took several days before they could tolerate their regular enteral nutrition and diet, resulting in prolonged intensive care unit stay and hospitalization. The mean hospitalization was 18.75 days (range 12–24 days).

One patient died a few years after intervention for reasons not related to AEF treatment. The other three patients have progressed well without graft infection or the need for amputation or further intervention related to previous surgery or new secondary AEFs (Table 4). Figure 1 shows the cumulative survival of the patients in this series.

Discussion

Secondary AEF is a dramatic condition, which is as dif-fi cult to diagnose as it is to treat. Although rare, its possibility should be considered in patients with severe acute or intermittent GI bleeding and a history of aortic reconstruction.2,11 Endoscopy and contrast-enhanced abdominal CT scan is the best diagnostic combination1,3,7

to exclude more common origins of GI bleeding, such as peptic ulcer or cancer, and offers the best chance of detecting a fi stula. Even then, the diagnosis is diffi -cult3,7,8,12 and AEF should still be considered if the fi nd-ings are negative, particularly in patients with intermittent GI bleeding. Thus, clinical suspicion is an important diagnostic tool.2,6,8,9,11

Long-term Survival

SurvivalCensored

0

0.0

0.2

0.4

0.6

0.8

1.0

50 100

Time in months

Cum

Sur

viva

l

150 200

Fig. 1. Kaplan–Meier cumulative survival

Table 4. Follow-up of patients after AEF repair

Graft infection

Proximal aortic false aneurysm

True AEF

Paraprosthetic AEF

Hypovolemic shock

Bowel resection Death

Early post-operative period FU

1 ✓ ✓ ✓ Sepsis, MOF —2 ✓ ✓ ✓ Ictus cerebri,

parental nutrition required. Discharged after 24 days

Ok

3 ✓ ✓ Ok Death4 ✓ ✓ ✓ Melena, parenteral

nutrition required—

5 ✓ ✓ ✓ ✓ Secondary partial ileectomy for segmentary bowel infarction

—

6 ✓ ✓ Discharged after 24 days

Ok

7 ✓ Discharged after 12 days

Ok

8 ✓ ✓ ✓ ✓ Sepsis, MOF —9 ✓ ✓ ✓ ✓ MOF —

MOF, multi-organ failure; AEF, aortoenteric fi stula

Aortoenteric fi stula is life threatening and requires aggressive surgical intervention to repair the site of bleeding, which is associated with high morbidity and mortality.1,3,11,13 The operative risk is related fi rst to the technical aspects of abdominal reopening after previous surgery, with a diffuse intense fi brotic atmosphere; and to bleeding, which creates extreme diffi culties with organ dissection, aortic clamping, and AEF repair, with a high risk of iatrogenic damage, particularly in the bowel. For proximal anastomotic aortic aneurysms,

1058 P. Bianchi et al.: Late GI Bleeding After Infrarenal Aortic Repair

extensive intervention may be required with wider exposure of the proximal abdominal aorta and suprare-nal or supraceliac clamping in the visceral ischemic phase during intervention.

Removal of the old graft with reinforced closure of the aortic stump and omental wrapping is the treatment of choice for a secondary AEF3,11,14,15 associated with graft infection, with or without an anastomotic aneu-rysm. It can be completed by simultaneous extra-anatomic bypass to prevent lower limb ischemia. Removal of the old graft with reinforced closure of the aortic stump and omental wrapping is also required for AEF unrelated to graft infection, when the proximal paraanastomotic aorta is so damaged or malacic that it does not represent a safe site for a new suture line. In situ reconstruction with a homograft is widely accepted for infected grafts,1 although we prefer not to perform re-do aorto-prosthetic anastomosis in a widely contami-nated site. In situ reconstruction with Dacron after partial or complete removal of the old graft can only be performed safely in the absence of graft infection, based on clinical history, blood examination results, and abdominal imaging confi rming the absence of peripros-thetic purulent fl uid collection with air content. Despite the absence of graft infection, secondary AEF should be suspected if there is contamination from the bowel to the prosthesis; however, acute development, interpo-sition of a sterile pseudoaneurysm, and the low bacterial count in the duodenum (which represents the most common site of AEFs) may allow for safe in situ recon-struction with Dacron.5 This is illustrated by the fact that none of the survivors in this series suffered infec-tive complications during the postoperative and follow-up periods.

Endovascular treatment is less invasive than open surgery,16 but it served only as a bridging intervention to control bleeding and normalize hemodynamics for major surgery in this series.17–19 In fact, endografts cannot work in the presence of infection18–20 and do not resolve bowel damage. Secondary AEF can only be treated defi nitively by open surgery. Two of our patients were unstable hemodynamically but as they had an acceptable proximal aortic neck, emergency stent-grafting was performed which achieved temporary hemostasis and hemodynamic stabilization.

In the present series, surgical intervention itself was successful. The in-hospital mortality rate of 55% was attributed to the consequences of sepsis and MOF and all deaths occurred during the early postoperative period. In our experience, and in accordance with other reports,13 preoperative graft infection and sepsis are the biggest risk factors for postoperative death. Moreover, the outcome after AEF repair seems favorable in the absence of preoperative hemodynamic instability,21 anastomotic aneurysms requiring extensive interven-

tions, and a need for bowel repair.13 These four aspects of the clinical presentation and management of second-ary AEF are crucial in predicting the postoperative outcome, even if surgical intervention is technically successful.

The technical strategies that could be applied at the time of primary aortic surgery to reduce the risk of secondary AEF, such as omental interposition between the duodenum and graft or an inclusion technique for aneurysms warrant investigation. Future research in this fi eld should focus on the prevention of complica-tions and the role of various prosthetic materials, espe-cially for vascular prostheses and sutures, different anastomotic techniques, and techniques to protect and cover the anastomosis site.

It is diffi cult to defi ne the clinical and imaging clues to predict secondary AEF development after aortic surgery; thus, its prevention is as challenging as its diag-nosis and treatment.2 However, it is clear that long-term follow-up is necessary after infrarenal grafting to check for signs of graft infection or anastomotic aneurysms, which often predispose to AEF formation, and which manifest a mean 5 years and 8 years after aortic surgery, respectively, as seen in the present series. Thus, all patients who undergo infrarenal aortic reconstruction should be followed up long term by abdominal aorta color-duplex ultrasound, performed yearly, and contrast-enhanced abdominal CT scan performed every 5 years, to detect signs of the development of late complications.

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