Case Reports Iliac Artery-Uretero-Colonic Fistula Presenting as Severe Gastrointestinal Hemorrhage and Hematuria: A Case Report and Review of the Literature Aleksandra Policha,1 Melissa Baldwin,2 Firas Mussa,1 and Caron Rockman,1 New York, New York
Arterioenteric fistulas represent an infrequent but potentially fatal cause of gastrointestinal hemorrhage. Patients often present in extremis from shock and sepsis. This mandates a rapid diagnosis so that prompt, potentially life-saving interventions can be performed. We report the case of a 35-year-old man who presented with hematuria and hematochezia secondary to an iliac artery-uretero-colonic fistula that developed years after open common iliac artery aneurysm repair. His condition rapidly progressed to hemorrhagic shock, and he underwent successful endovascular treatment with a covered stent graft as a bridge to definitive open surgery. Subsequently, graft explantation, extra-anatomic arterial bypass, bowel resection, and ureter ligation was undertaken. A summary of the literature on iliac artery-enteric fistulas follows.
INTRODUCTION Fistulization between the gastrointestinal tract and the abdominal aorta and its branches is a rare but potentially catastrophic cause of gastrointestinal hemorrhage. Arterioenteric fistulas (AEFs) typically occur after aortoiliac interventions for aneurysmal disease; however, primary fistula formation caused by an infectious process, malignancy, radiation exposure, and foreign body ingestion has been described in the literature.1e4 Most AEFs involve the abdominal aorta and third and fourth portions of the duodenum and occur after open and 1 Division of Vascular and Endovascular Surgery, New York University Langone Medical Center, New York, NY. 2 Department of General Surgery, New York University Langone Medical Center, New York, NY. Correspondence to: Caron Rockman, MD, Division of Vascular and Endovascular Surgery, New York University Langone Medical Center, 530 First Avenue, 6H Schwartz Health Care Center, New York, NY, 10016, USA; E-mail: [email protected]
Ann Vasc Surg 2015; 29: 1656.e1–1656.e6 http://dx.doi.org/10.1016/j.avsg.2015.07.006 Ó 2015 Elsevier Inc. All rights reserved. Manuscript received: July 12, 2015; manuscript accepted: July 30, 2015; published online: August 22, 2015.
endovascular abdominal aortic aneurysm repair.5 Iliac artery-enteric fistulas have been periodically reported in the literature, mostly in the form of small case series and reports. These AEFs typically represent a diagnostic challenge, and patients frequently undergo a complex work-up and multiple imaging studies including nuclear scanning, angiography, computed tomography, and endoscopy before the correct diagnosis are made. Such studies may be time consuming and may significantly delay treatment. Making an accurate and rapid diagnosis is of paramount importance, particularly because these patients frequently present with hemodynamic instability and sepsis requiring timesensitive intervention.2,3,6e19 Thus, a high index of suspicion for an AEF must be maintained in all patients presenting with gastrointestinal bleeding who report a history of prior aortoiliac intervention or other risk factors that predispose to this condition. Herein, we describe the operative management of a young male who presented with hematuria and hematochezia secondary to a common iliac artery (CIA)-ureteral-colonic fistula. In addition, we review the current literature on the surgical treatment of this rare condition. 1656.e1
1656.e2 Case reports
Annals of Vascular Surgery
Fig. 1. Angiography demonstrating a pseudoaneurysm at the distal suture line of the right CIA Dacron graft (A) and exclusion of flow in the pseudoaneurysm
after stent-graft placement (B). Black arrow indicates contained extravasation of contrast consistent with pseudoaneurysm.
CASE REPORT
(Atrium, Hudson, NH) was placed via an ipsilateral femoral artery approach, and completion angiography showed successful exclusion of flow in the pseudoaneurysm (Fig. 1B). Once the patient was stabilized, computed tomography was performed to facilitate definitive operative planning, which demonstrated diffuse colonic dilation with a large amount of intraluminal high-density material compatible with blood and clot (Fig. 2). In addition to a perivascular hematoma involving the right common iliac graft and right ureter was observed. The right kidney was severely atrophic, and the left kidney showed compensatory hypertrophy. The patient remained stable after endovascular intervention without any further episodes of bleeding. On return to the operating room for the second stage of treatment, he underwent an extra-anatomic left-to-right femoralefemoral arterial bypass with an 8-mm Propaten graft in preparation for iliac artery graft explantation. After this, an exploratory laparotomy was performed and identified an arteriocolonic fistula between the cecum and distal iliac graft anastomosis. The right ureter was closely associated with this inflammatory mass. An ileocecectomy was performed, and the iliac graft was explanted, and CIA oversewn proximally and distally. The right ureter was ligated, and the atrophic right kidney left in situ. The patient had an uneventful postoperative course and was discharged home on the seventh postoperative day. After consultation with the Infectious Diseases Service, the decision was made to continue intravenous broadspectrum antibiotics (Vancomycin, Cefepime, and Metronidazole) on discharge, for a total treatment duration of 6 weeks. As all infected graft material was removed intraoperatively, it was felt that additional long-term suppressive therapy was not indicated. At 1-month follow-up,
A 35-year-old human immunodeficiency virus-positive male presented to an outside emergency department with gross hematuria of several weeks duration. His medical history was significant for a 7-cm right CIA aneurysm, previously treated with interposition Dacron graft placement, also performed at another outside institution 6 years before the current presentation. The original etiology of his iliac aneurysm was unclear. On arrival at the current presentation, he was profoundly anemic with hemoglobin of 4 g/dL. Although undergoing evaluation, he developed a massive lower-gastrointestinal hemorrhage, necessitating transfusion of multiple blood products (31 units of blood, 10 units of platelets, 19 units of fresh frozen plasma, and 4 units of cryoprecipitate). He was appropriately resuscitated, broad-spectrum antibiotic therapy was initiated, and he subsequently underwent colonoscopy and upper endoscopy. On colonoscopy, a large amount of blood was observed throughout the colon, but no obvious source of hemorrhage was identified. The esophagogastroduodenoscopy revealed normal findings. After this, the patient was taken to the interventional radiology suite for a mesenteric angiogram in an attempt to identify the source of bleeding. Selective angiography revealed normal mesenteric vessels; however, a large pseudoaneurysm was noted at the distal suture line of the right iliac artery graft (Fig. 1A). The patient was then transferred to our institution for further operative management. The decision was made to proceed with endovascular treatment of the iliac pseudoaneurysm as a temporizing measure until definitive surgery could be performed for a suspected AEF. An 8 40-mm iCAST covered stent
Vol. 29, No. 8, November 2015
Case reports 1656.e3
Fig. 2. (A) Right CIA graft (arrow) in close apposition with right colon containing high-density material compatible with blood and clot. (B) Severe right
hydronephrosis (asterisk) to the level of the iliac graft (arrow) and cecum, suggestive of chronic occlusion.
he was tolerating a regular diet and reported normal bowel function and no further episodes of hematochezia or hematuria. All incisions were well-healed and pedal pulses were palpable bilaterally.
unclear etiology. The artery involved in the AEF was the CIA in 44% of subjects, the internal iliac artery in 33%, and the external iliac artery in 26%. Meanwhile, the affected-bowel segment was the colon in 51% of patients, the small bowel in 31%, and the rectum in 21%. Factors predisposing to AEF formation that were identified in these patients included prior abdominal or pelvic surgical intervention (reported in 41% of individuals), prior aortoiliac intervention (reported in 33%), pelvic malignancy (reported in 33%), and a history of intraabdominal or vascular infection (reported in 13%). Thirty-eight percent of patients were treated with endovascular intervention only (stent-graft placement or coil embolization), 8% underwent endovascular surgery as a bridge to open repair, and 54% underwent initial open intervention. The duration of follow-up ranged from 10 days to 30 months. Thirty-day mortality was 26%, with 20% of all deaths occurring intraoperatively. Causes of death included cardiac arrest, massive hemorrhage, and multiorgan failure.
LITERATURE REVIEW Methods A PubMed search was performed in March 2015 using the key terms ‘‘iliac-enteric fistula,’’ ‘‘colovascular fistula,’’ and ‘‘AEF.’’ The query was limited to English literature publications from the last 25 years (1990e2015). A manual review of the reference lists from theses articles were performed to identify additional publications. Information regarding patient demographics, risk factors for AEF formation, symptoms at presentation, operative management, and outcomes was evaluated. Results Table I summarizes the data on the 39 patients who had information available for analysis. Eighty-two percent of the patients were male, with a mean age of 69 years (range, 39e89 years). All but 1 presented with episodes of gastrointestinal bleeding, ranging from minor hematochezia to hemorrhagic shock. One patient presented with fever and bacteremia of
DISCUSSION Iliac artery-enteric fistulas represent an uncommon variant of AEFs described in the literature.
1656.e4 Case reports
Annals of Vascular Surgery
Table I. Characteristics and interventions of patients with iliac enteric fistulas Type of intervention
Patient characteristic
Demographics Mean age (years) Male gender (%) Predisposing factors (% of patients) Prior nonvascular surgical intervention Prior vascular intervention Malignancy Infection Presenting symptoms (% of patients) Gastrointestinal hemorrhage Hypotension/shock Abdominal pain Fever Vessel involved (% of patients) CIA Internal iliac artery External iliac artery Bowel segment involved (% of patients) Colon Small bowel Rectum Endovascular Intervention (% of patients) Stent graft Coil/plug Open intervention (% of patients) Explantation Extra-anatomic bypass Ligation only Primary repair
Open surgery
Endovascular intervention
Endovascular bridge to open surgery
Total
n ¼ 21
n ¼ 15
n¼3
n ¼ 39
71 21 (100)
65 9 (60)
72 2 (67)
69 32 (82)
3 9 2 3
(14) (43) (10) (14)
11 3 9 2
(73) (20) (60) (13)
2 1 2 0
(67) (33) (67) (0)
26 13 13 5
(41) (33) (33) (13)
20 6 6 5
(95) (29) (29) (24)
15 12 2 0
(100) (80) (13) (0)
3 1 1 0
(100) (33) (33) (0)
38 19 9 5
(97) (49) (23) (13)
12 (57) 8 (38) 2 (10)
4 (27) 4 (27) 7 (47)
1 (33) 1 (33) 1 (33)
17 (44) 13 (33) 10 (26)
12 (57) 6 (29) 4 (19)
6 (40) 6 (40) 3 (20)
2 (67) 0 (0) 1 (33)
20 (51) 12 (31) 8 (21)
NA NA
9 (60) 7 (47)
3 (100) 1 (33)
12 (31) 8 (21)
2 3 0 0
13 11 4 1
11 8 4 1
(52) (38) (19) (5)
Interestingly, most of these AEFs appear to be primary fistulas (not associated with prior vascular intervention).1e3,7e14,16,18e27 This is in contrast to aortoenteric fistulas, which are predominantly secondary fistulas that classically develop after abdominal aortic aneurysm repair.28,29 We identified several factors that may predispose patients to iliacenteric fistula formation. The most common factors included prior nonvascular abdominal or pelvic surgery, a history of pelvic malignancy, and prior aortic or iliac intervention.2e4,6,10,12,14e17,20,23e26,30e38 Infectious and inflammatory etiologies, such diverticulitis and typhlitis, were reported less frequently.1,2,7,25,37 Although aortoenteric fistulas most commonly involve the small bowel, iliac artery-enteric fistulas are more likely to involve the colon. Consequently, patients typically present with lowergastrointestinal hemorrhage.1e4,7e27,30e38 In addition, hypovolemic shock, abdominal pain, and
NA NA NA NA
(67) (100) (0) (0)
(33) (28) (10) (3)
sepsis are common findings associated with this type of AEF.1,3,8e20,23,24,31,32,35,38 Hematuria or hydronephrosis may also be present when the urinary system is involved,1 as was the case with our patient. Patients may present with a minor sentinel bleed before significant hemorrhage occurs, and this is the ideal time to intervene, as studies have shown that sepsis and hemodynamic instability are poor prognostic factors in AEF treatment.5 Patients who present with AEFs often undergo a plethora of diagnostic studies including upper and lower endoscopy, computed tomography (CT), angiography, and nuclear bleeding scans. Such studies, although appropriate, are sometimes nondiagnostic. Endoscopy may reveal fresh blood or clot, mucosal ulceration, or vascular graft erosion. Angiography may demonstrate an anastomotic pseudoaneurysm or contrast extravasation. On CT, the diagnosis should be suspected when a vascular structure is observed in close apposition to a
Vol. 29, No. 8, November 2015
segment of bowel, with associated inflammatory changes, extraluminal gas, and intravenous, oral, or rectal contrast extravasation. Frequently, the correct diagnosis is not made until the patient is taken to the operating room for laparotomy to control the hemorrhage.7,20,27 Initial treatment should focus on resuscitation, correction of anemia and coagulopathy, and initiation of broad spectrum antibiotics. Guidelines on the appropriate antibiotic regimen and the ideal duration of treatment are nonexistent, and most surgeons rely on parameters of infection and local infectious diseases expert opinion to guide therapy. Organisms that have been isolated in blood cultures of patients with AEF and in grafts explanted from these individuals include Staphylococcus aures, Streptococcus spp., Salmonella spp., Bacteroides fragilis, and Escherichia coli.32,34 Antibiotic selection should ensure coverage of these organisms. Endovascular treatment, with placement of a covered stent to exclude the fistula, may be used as definitive management in patients at highoperative risk for open surgery, or as a bridge to open surgery under more controlled, semielective circumstances in healthier patients. Many AEF patients are older individuals with multiple medical comorbidities, malignancy, or a short life expectancy, and endovascular therapy may represent an appropriate definitive operation for these patients. Endovascular treatment is associated with lowerperioperative morbidity and in-hospital mortality. In a study by Kakkos et al., perioperative morbidity was 25% after endovascular treatment compared with 77% after open repair. No in-hospital deaths were observed for patients who underwent endovascular treatment, whereas the in-hospital mortality rate was 35% after open repair. Although patients treated with endovascular therapy fared better in terms of perioperative morbidity and mortality, these patients had a higher rate of recurrent bleeding compared with individuals who underwent open repair (49% vs. 22%, respectively). The reintervention rate was similarly higher in the endovascular treatment group compared with the open surgical treatment group (70% vs. 36%, respectively).29 In a second study by Kakkos et al., which focused specifically on outcomes after endovascular management of AEFs, the group again demonstrated a low thirty-day mortality of 8.5% and a recurrent bleeding rate of 19%. Furthermore, they noted that patients who did not undergo intestinal repair had a high rate of combined recurrence and sepsis (48%).39 In patients who undergo endovascular treatment as the definitive operation, consideration should be given to life-long antibiotic
Case reports 1656.e5
suppression therapy, as graft material that is by definition infected is left in situ. In a younger patient, we advocate for explantation of the infected vascular segment, extra-anatomic bypass to restore perfusion, and resection or repair of the affected-bowel segment. Our patient was a previously healthy young male who presented with a severe lower-gastrointestinal hemorrhage as a result of an iliac artery-colonic fistula. Given the dramatic bleeding at the initial presentation and his good overall health, we decided that: (1) immediate endovascular treatment of the AEF was indicated to prevent any additional bleeding; and (2) given a presumed long-life expectancy, open surgery would allow for the most durable repair and for fewer long-term complications.
CONCLUSIONS Iliac artery-enteric fistulas are rare causes of gastrointestinal bleeding that occur in patients with a history of prior iliac intervention, pelvic surgery, and malignancy. The treatment algorithm should include prompt diagnosis, patient resuscitation, and definitive surgical management. Endovascular management can be used as a temporizing treatment or as definitive therapy in high-risk patients. REFERENCES 1. McFarlane M, Plummer J, Simpson L, et al. Internal iliac artery aneurysmo-colonic fistula: a rare presentation of massive lower gastrointestinal haemorrhage: report of a case. Eur Surg 2009;41:129e31. 2. Knape S, Van Nieuwenhove Y, van Tussenbroek F, et al. Endovascular techniques in the management of acute arterioenteric fistulas. J Endovasc Ther 2004;11:89e93. 3. Leonhardt H, Mellander S, Snygg J, et al. Endovascular management of acute bleeding arterioenteric fistulas. Cardiovasc Intervent Radiol 2008;31:542e9. 4. Lazaris A, Tsapralis D, Patapis P, et al. Aortoiliac endograftenteric fistula due to an ingested toothpick. J Vasc Surg 2009;50:640e3. 5. Tagowski M, Vieweg H, Wissgott C, et al. Aortoenteric Fistula as a Complication of Open Reconstruction and Endovascular Repair of Abdominal Aorta. Radiol Res Pract 2014;2014:383159. 6. Leon L, Psalms S, Ihnat D, et al. Aortofemoral graft limbe toecolon paraprosthetic fistula. J Vasc Surg 2008;47:460. 7. Mansfield L, Seymore H, Kianifard B. Arterio-enteric fistula as a result of typhlitis. Colorectal Dis 2010;12:1270e1. 8. Fumery M, Duchmann J, Andary R, et al. Lower gastrointestinal bleeding due to primary ilioenteric fistula. Abdom Imaging 2012;38:376e8. 9. Nicolaou D, Mysko W. Enteric fistulization of a common iliac artery aneurysm: An unusual cause of gastrointestinal hemorrhage and shock. Am J Emerg Med 1996;14:272e5. 10. Chin CC, Yeh CY, Kuo YH, et al. Massive lower gastrointestinal bleeding from an external iliac artery fistula in a
1656.e6 Case reports
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22.
23.
24.
patient with bladder cancer. Chang Gung Med J 2008;31: 612e5. A gao glu N, Arslan M, Dinc¸ H. A rare cause of massive rectal bleeding: internal iliac artery aneurysm. Acta Chir Belg 2006;106:104e6. Gittleman A, Glanz S, Hon M, et al. Lower gastrointestinal bleeding from the internal iliac artery: angiographic demonstration of an iliac arteriocolic fistula. Cardiovasc Intervent Radiol 2004;27:262e3. Aseem W, Schachter L, Devlin J, et al. Rupture of an internal iliac artery aneurysm into the rectum: fatal consequence of an ilioenteric fistulaea case report. Vasc Endovasc Surg 1992;26:151e4. Hirakata R, Hasuo K, Yasumori K, et al. Arterioenteric fistulae: diagnosis and treatment by angiography. Clin Radiol 1991;43:328e30. Duvnjak S, Andersen P. Life-threatening Arterioenteric fistula bleeding treated by embolization. Cardiovasc Intervent Radiol 2012;35:1535e8. Desai N, Patel S, Nwosu C, et al. Arteriojejunal Fistula Presenting with Recurrent Obscure GI Hemorrhage in a Patient with a Failed Pancreas Allograft. Case Rep Transplant 2013;2013:171807. Hicks T, Kedora J, Shutze W. Treatment of an ilioenteric fistula with an Amplatzer Vascular Plug. J Vasc Surg 2011;54: 1495e7. Wahlgren C, Wahlberg E. Rectal bleeding caused by rupture of an aneurysm of the iliac artery into the rectum. Eur J Surg 2002;168:59e60. Whittaker C, Ananthakrishnan G, DeNunzio M, et al. Endovascular repair of a primary iliac-cecal fistula presenting with gastrointestinal hemorrhage. Cardiovasc Intervent Radiol 2007;31(S2):120e3. Perhoniemi V, Tykka H, Saario I. Primary arterioenteric fistula between common iliac artery and ileum with massive bleeding. Ann Chir Gynaecol 1991;80:311e2. Katoh J, Shindo S, Kina S, et al. Rupture of an isolated internal iliac artery aneurysm into the rectum: report of a case. Surg Today 1995;25:554e6. Noh H, Fishman E, Bluemke D. Isolated common iliac artery aneurysm rupturing into small bowel: CT appearance. Abdom Imaging 1995;20:521e2. Franchin M, Tozzi M, Piffaretti G, et al. Emergency endovascular ‘‘bridge’’ treatment for iliac-enteric fistula. Cardiovasc Intervent Radiol 2011;34:1106e8. Farrell C, Bailey R, Russell E, et al. Gastrointestinal: iliacenteric fistula. J Gastroenterol Hepatol 2010;25:1015.
Annals of Vascular Surgery
25. Arthur T, Gillespie C, Butcher W, et al. Pseudoaneurysm of the internal iliac artery resulting in massive per-rectal bleeding. J Surg Case Rep 2013;2013:10e1. 26. Santos V, Razuk Filho A, Castelli Junior V, et al. Lower gastrointestinal bleeding as a result of fistula between the iliac artery and sigmoid colon in patient with advanced testicular cancer. Int Braz J Urol 2013;39:747e51. 27. Lawlor D. Primary aorto/iliac-enteric fistula: report of 6 new cases. Vasc Endovasc Surg 2004;38:281e6. 28. Bergqvist D, Bj€ orck M, Nyman R. Secondary aortoenteric fistula after endovascular aortic interventions: a systematic literature review. J Vasc Interv Radiol 2008;19:163e5. 29. Kakkos S, Antoniadis P, Klonaris C, et al. Open or endovascular repair of aortoenteric fistulas? A multicentre comparative study. Eur J Vasc Endovasc Surg 2011;41:625e34. 30. Goto A, Yu I, Naito T, et al. Fistula from an internal iliac artery aneurysm to the sigmoid colon after endovascular arterial repair. Endoscopy 2014;46(Suppl 1):E367e8. 31. Rivera R, Shah A, Ozden N. Iliac-enteric fistula diagnosed by video capsule endoscopy. Clin Gastroenterol Hepatol 2011;9:e39e40. 32. de Koning H, van Sterkenburg S, Pierie M, et al. Endovascular abdominal aortic aneurysm repair complicated by spondylodiscitis and iliaco-enteral fistula. J Vasc Surg 2008;47: 1330e2. 33. Bognar G, Sugar I, Sipos P, et al. Secondary iliac-enteric fistula to the sigmoid colon complicated with entero-graftocutaneous fistula. Case Rep Gastroenterol 2008;2:138e43. 34. Perez R, Katayama F, Bresciani C, et al. Aortoenteric fistula to the sigmoid colondcase report. Curr Surg 2005;62: 49e54. 35. Chan L, McErlean M. Secondary arterioenteric fistula involving the sigmoid colon. Am J Emerg Med 1994;12: 527e30. 36. Karkos C, Oshodi T, Vimalachandran D, et al. Internal iliac aneurysm rupture into the rectum following endovascular exclusion: an unusual cause of massive lower gastrointestinal bleeding. J Endovasc Ther 2002;9:907e11. 37. Li S, Burton F, Burton M, et al. The endoscopic diagnosis of iliac colonic fistula and review of literature. Am J Gastroenterol 1993;88:307e10. 38. Robertson G, Valente J, Hunter G, et al. Iliac-enteric fistula following Dacron patch angioplasty. Ann Vasc Surg 1991;5: 467e9. 39. Kakkos S, Papadoulas S, Tsolakis I. Endovascular management of arterioenteric fistulas: a systemic review and metaanalysis of the literature. J Endovasc Ther 2011;18:66e77.
Arterioenteric fistulas represent an infrequent but potentially fatal cause of gastrointestinal hemorrhage. Patients often present in extremis from shock and sepsis. This mandates a rapid diagnosis so that prompt, potentially life-saving interventions can be performed. We report the case of a 35-year-old man who presented with hematuria and hematochezia secondary to an iliac artery-uretero-colonic fistula that developed years after open common iliac artery aneurysm repair. His condition rapidly progressed to hemorrhagic shock, and he underwent successful endovascular treatment with a covered stent graft as a bridge to definitive open surgery. Subsequently, graft explantation, extra-anatomic arterial bypass, bowel resection, and ureter ligation was undertaken. A summary of the literature on iliac artery-enteric fistulas follows.
INTRODUCTION Fistulization between the gastrointestinal tract and the abdominal aorta and its branches is a rare but potentially catastrophic cause of gastrointestinal hemorrhage. Arterioenteric fistulas (AEFs) typically occur after aortoiliac interventions for aneurysmal disease; however, primary fistula formation caused by an infectious process, malignancy, radiation exposure, and foreign body ingestion has been described in the literature.1e4 Most AEFs involve the abdominal aorta and third and fourth portions of the duodenum and occur after open and 1 Division of Vascular and Endovascular Surgery, New York University Langone Medical Center, New York, NY. 2 Department of General Surgery, New York University Langone Medical Center, New York, NY. Correspondence to: Caron Rockman, MD, Division of Vascular and Endovascular Surgery, New York University Langone Medical Center, 530 First Avenue, 6H Schwartz Health Care Center, New York, NY, 10016, USA; E-mail: [email protected]
Ann Vasc Surg 2015; 29: 1656.e1–1656.e6 http://dx.doi.org/10.1016/j.avsg.2015.07.006 Ó 2015 Elsevier Inc. All rights reserved. Manuscript received: July 12, 2015; manuscript accepted: July 30, 2015; published online: August 22, 2015.
endovascular abdominal aortic aneurysm repair.5 Iliac artery-enteric fistulas have been periodically reported in the literature, mostly in the form of small case series and reports. These AEFs typically represent a diagnostic challenge, and patients frequently undergo a complex work-up and multiple imaging studies including nuclear scanning, angiography, computed tomography, and endoscopy before the correct diagnosis are made. Such studies may be time consuming and may significantly delay treatment. Making an accurate and rapid diagnosis is of paramount importance, particularly because these patients frequently present with hemodynamic instability and sepsis requiring timesensitive intervention.2,3,6e19 Thus, a high index of suspicion for an AEF must be maintained in all patients presenting with gastrointestinal bleeding who report a history of prior aortoiliac intervention or other risk factors that predispose to this condition. Herein, we describe the operative management of a young male who presented with hematuria and hematochezia secondary to a common iliac artery (CIA)-ureteral-colonic fistula. In addition, we review the current literature on the surgical treatment of this rare condition. 1656.e1
1656.e2 Case reports
Annals of Vascular Surgery
Fig. 1. Angiography demonstrating a pseudoaneurysm at the distal suture line of the right CIA Dacron graft (A) and exclusion of flow in the pseudoaneurysm
after stent-graft placement (B). Black arrow indicates contained extravasation of contrast consistent with pseudoaneurysm.
CASE REPORT
(Atrium, Hudson, NH) was placed via an ipsilateral femoral artery approach, and completion angiography showed successful exclusion of flow in the pseudoaneurysm (Fig. 1B). Once the patient was stabilized, computed tomography was performed to facilitate definitive operative planning, which demonstrated diffuse colonic dilation with a large amount of intraluminal high-density material compatible with blood and clot (Fig. 2). In addition to a perivascular hematoma involving the right common iliac graft and right ureter was observed. The right kidney was severely atrophic, and the left kidney showed compensatory hypertrophy. The patient remained stable after endovascular intervention without any further episodes of bleeding. On return to the operating room for the second stage of treatment, he underwent an extra-anatomic left-to-right femoralefemoral arterial bypass with an 8-mm Propaten graft in preparation for iliac artery graft explantation. After this, an exploratory laparotomy was performed and identified an arteriocolonic fistula between the cecum and distal iliac graft anastomosis. The right ureter was closely associated with this inflammatory mass. An ileocecectomy was performed, and the iliac graft was explanted, and CIA oversewn proximally and distally. The right ureter was ligated, and the atrophic right kidney left in situ. The patient had an uneventful postoperative course and was discharged home on the seventh postoperative day. After consultation with the Infectious Diseases Service, the decision was made to continue intravenous broadspectrum antibiotics (Vancomycin, Cefepime, and Metronidazole) on discharge, for a total treatment duration of 6 weeks. As all infected graft material was removed intraoperatively, it was felt that additional long-term suppressive therapy was not indicated. At 1-month follow-up,
A 35-year-old human immunodeficiency virus-positive male presented to an outside emergency department with gross hematuria of several weeks duration. His medical history was significant for a 7-cm right CIA aneurysm, previously treated with interposition Dacron graft placement, also performed at another outside institution 6 years before the current presentation. The original etiology of his iliac aneurysm was unclear. On arrival at the current presentation, he was profoundly anemic with hemoglobin of 4 g/dL. Although undergoing evaluation, he developed a massive lower-gastrointestinal hemorrhage, necessitating transfusion of multiple blood products (31 units of blood, 10 units of platelets, 19 units of fresh frozen plasma, and 4 units of cryoprecipitate). He was appropriately resuscitated, broad-spectrum antibiotic therapy was initiated, and he subsequently underwent colonoscopy and upper endoscopy. On colonoscopy, a large amount of blood was observed throughout the colon, but no obvious source of hemorrhage was identified. The esophagogastroduodenoscopy revealed normal findings. After this, the patient was taken to the interventional radiology suite for a mesenteric angiogram in an attempt to identify the source of bleeding. Selective angiography revealed normal mesenteric vessels; however, a large pseudoaneurysm was noted at the distal suture line of the right iliac artery graft (Fig. 1A). The patient was then transferred to our institution for further operative management. The decision was made to proceed with endovascular treatment of the iliac pseudoaneurysm as a temporizing measure until definitive surgery could be performed for a suspected AEF. An 8 40-mm iCAST covered stent
Vol. 29, No. 8, November 2015
Case reports 1656.e3
Fig. 2. (A) Right CIA graft (arrow) in close apposition with right colon containing high-density material compatible with blood and clot. (B) Severe right
hydronephrosis (asterisk) to the level of the iliac graft (arrow) and cecum, suggestive of chronic occlusion.
he was tolerating a regular diet and reported normal bowel function and no further episodes of hematochezia or hematuria. All incisions were well-healed and pedal pulses were palpable bilaterally.
unclear etiology. The artery involved in the AEF was the CIA in 44% of subjects, the internal iliac artery in 33%, and the external iliac artery in 26%. Meanwhile, the affected-bowel segment was the colon in 51% of patients, the small bowel in 31%, and the rectum in 21%. Factors predisposing to AEF formation that were identified in these patients included prior abdominal or pelvic surgical intervention (reported in 41% of individuals), prior aortoiliac intervention (reported in 33%), pelvic malignancy (reported in 33%), and a history of intraabdominal or vascular infection (reported in 13%). Thirty-eight percent of patients were treated with endovascular intervention only (stent-graft placement or coil embolization), 8% underwent endovascular surgery as a bridge to open repair, and 54% underwent initial open intervention. The duration of follow-up ranged from 10 days to 30 months. Thirty-day mortality was 26%, with 20% of all deaths occurring intraoperatively. Causes of death included cardiac arrest, massive hemorrhage, and multiorgan failure.
LITERATURE REVIEW Methods A PubMed search was performed in March 2015 using the key terms ‘‘iliac-enteric fistula,’’ ‘‘colovascular fistula,’’ and ‘‘AEF.’’ The query was limited to English literature publications from the last 25 years (1990e2015). A manual review of the reference lists from theses articles were performed to identify additional publications. Information regarding patient demographics, risk factors for AEF formation, symptoms at presentation, operative management, and outcomes was evaluated. Results Table I summarizes the data on the 39 patients who had information available for analysis. Eighty-two percent of the patients were male, with a mean age of 69 years (range, 39e89 years). All but 1 presented with episodes of gastrointestinal bleeding, ranging from minor hematochezia to hemorrhagic shock. One patient presented with fever and bacteremia of
DISCUSSION Iliac artery-enteric fistulas represent an uncommon variant of AEFs described in the literature.
1656.e4 Case reports
Annals of Vascular Surgery
Table I. Characteristics and interventions of patients with iliac enteric fistulas Type of intervention
Patient characteristic
Demographics Mean age (years) Male gender (%) Predisposing factors (% of patients) Prior nonvascular surgical intervention Prior vascular intervention Malignancy Infection Presenting symptoms (% of patients) Gastrointestinal hemorrhage Hypotension/shock Abdominal pain Fever Vessel involved (% of patients) CIA Internal iliac artery External iliac artery Bowel segment involved (% of patients) Colon Small bowel Rectum Endovascular Intervention (% of patients) Stent graft Coil/plug Open intervention (% of patients) Explantation Extra-anatomic bypass Ligation only Primary repair
Open surgery
Endovascular intervention
Endovascular bridge to open surgery
Total
n ¼ 21
n ¼ 15
n¼3
n ¼ 39
71 21 (100)
65 9 (60)
72 2 (67)
69 32 (82)
3 9 2 3
(14) (43) (10) (14)
11 3 9 2
(73) (20) (60) (13)
2 1 2 0
(67) (33) (67) (0)
26 13 13 5
(41) (33) (33) (13)
20 6 6 5
(95) (29) (29) (24)
15 12 2 0
(100) (80) (13) (0)
3 1 1 0
(100) (33) (33) (0)
38 19 9 5
(97) (49) (23) (13)
12 (57) 8 (38) 2 (10)
4 (27) 4 (27) 7 (47)
1 (33) 1 (33) 1 (33)
17 (44) 13 (33) 10 (26)
12 (57) 6 (29) 4 (19)
6 (40) 6 (40) 3 (20)
2 (67) 0 (0) 1 (33)
20 (51) 12 (31) 8 (21)
NA NA
9 (60) 7 (47)
3 (100) 1 (33)
12 (31) 8 (21)
2 3 0 0
13 11 4 1
11 8 4 1
(52) (38) (19) (5)
Interestingly, most of these AEFs appear to be primary fistulas (not associated with prior vascular intervention).1e3,7e14,16,18e27 This is in contrast to aortoenteric fistulas, which are predominantly secondary fistulas that classically develop after abdominal aortic aneurysm repair.28,29 We identified several factors that may predispose patients to iliacenteric fistula formation. The most common factors included prior nonvascular abdominal or pelvic surgery, a history of pelvic malignancy, and prior aortic or iliac intervention.2e4,6,10,12,14e17,20,23e26,30e38 Infectious and inflammatory etiologies, such diverticulitis and typhlitis, were reported less frequently.1,2,7,25,37 Although aortoenteric fistulas most commonly involve the small bowel, iliac artery-enteric fistulas are more likely to involve the colon. Consequently, patients typically present with lowergastrointestinal hemorrhage.1e4,7e27,30e38 In addition, hypovolemic shock, abdominal pain, and
NA NA NA NA
(67) (100) (0) (0)
(33) (28) (10) (3)
sepsis are common findings associated with this type of AEF.1,3,8e20,23,24,31,32,35,38 Hematuria or hydronephrosis may also be present when the urinary system is involved,1 as was the case with our patient. Patients may present with a minor sentinel bleed before significant hemorrhage occurs, and this is the ideal time to intervene, as studies have shown that sepsis and hemodynamic instability are poor prognostic factors in AEF treatment.5 Patients who present with AEFs often undergo a plethora of diagnostic studies including upper and lower endoscopy, computed tomography (CT), angiography, and nuclear bleeding scans. Such studies, although appropriate, are sometimes nondiagnostic. Endoscopy may reveal fresh blood or clot, mucosal ulceration, or vascular graft erosion. Angiography may demonstrate an anastomotic pseudoaneurysm or contrast extravasation. On CT, the diagnosis should be suspected when a vascular structure is observed in close apposition to a
Vol. 29, No. 8, November 2015
segment of bowel, with associated inflammatory changes, extraluminal gas, and intravenous, oral, or rectal contrast extravasation. Frequently, the correct diagnosis is not made until the patient is taken to the operating room for laparotomy to control the hemorrhage.7,20,27 Initial treatment should focus on resuscitation, correction of anemia and coagulopathy, and initiation of broad spectrum antibiotics. Guidelines on the appropriate antibiotic regimen and the ideal duration of treatment are nonexistent, and most surgeons rely on parameters of infection and local infectious diseases expert opinion to guide therapy. Organisms that have been isolated in blood cultures of patients with AEF and in grafts explanted from these individuals include Staphylococcus aures, Streptococcus spp., Salmonella spp., Bacteroides fragilis, and Escherichia coli.32,34 Antibiotic selection should ensure coverage of these organisms. Endovascular treatment, with placement of a covered stent to exclude the fistula, may be used as definitive management in patients at highoperative risk for open surgery, or as a bridge to open surgery under more controlled, semielective circumstances in healthier patients. Many AEF patients are older individuals with multiple medical comorbidities, malignancy, or a short life expectancy, and endovascular therapy may represent an appropriate definitive operation for these patients. Endovascular treatment is associated with lowerperioperative morbidity and in-hospital mortality. In a study by Kakkos et al., perioperative morbidity was 25% after endovascular treatment compared with 77% after open repair. No in-hospital deaths were observed for patients who underwent endovascular treatment, whereas the in-hospital mortality rate was 35% after open repair. Although patients treated with endovascular therapy fared better in terms of perioperative morbidity and mortality, these patients had a higher rate of recurrent bleeding compared with individuals who underwent open repair (49% vs. 22%, respectively). The reintervention rate was similarly higher in the endovascular treatment group compared with the open surgical treatment group (70% vs. 36%, respectively).29 In a second study by Kakkos et al., which focused specifically on outcomes after endovascular management of AEFs, the group again demonstrated a low thirty-day mortality of 8.5% and a recurrent bleeding rate of 19%. Furthermore, they noted that patients who did not undergo intestinal repair had a high rate of combined recurrence and sepsis (48%).39 In patients who undergo endovascular treatment as the definitive operation, consideration should be given to life-long antibiotic
Case reports 1656.e5
suppression therapy, as graft material that is by definition infected is left in situ. In a younger patient, we advocate for explantation of the infected vascular segment, extra-anatomic bypass to restore perfusion, and resection or repair of the affected-bowel segment. Our patient was a previously healthy young male who presented with a severe lower-gastrointestinal hemorrhage as a result of an iliac artery-colonic fistula. Given the dramatic bleeding at the initial presentation and his good overall health, we decided that: (1) immediate endovascular treatment of the AEF was indicated to prevent any additional bleeding; and (2) given a presumed long-life expectancy, open surgery would allow for the most durable repair and for fewer long-term complications.
CONCLUSIONS Iliac artery-enteric fistulas are rare causes of gastrointestinal bleeding that occur in patients with a history of prior iliac intervention, pelvic surgery, and malignancy. The treatment algorithm should include prompt diagnosis, patient resuscitation, and definitive surgical management. Endovascular management can be used as a temporizing treatment or as definitive therapy in high-risk patients. REFERENCES 1. McFarlane M, Plummer J, Simpson L, et al. Internal iliac artery aneurysmo-colonic fistula: a rare presentation of massive lower gastrointestinal haemorrhage: report of a case. Eur Surg 2009;41:129e31. 2. Knape S, Van Nieuwenhove Y, van Tussenbroek F, et al. Endovascular techniques in the management of acute arterioenteric fistulas. J Endovasc Ther 2004;11:89e93. 3. Leonhardt H, Mellander S, Snygg J, et al. Endovascular management of acute bleeding arterioenteric fistulas. Cardiovasc Intervent Radiol 2008;31:542e9. 4. Lazaris A, Tsapralis D, Patapis P, et al. Aortoiliac endograftenteric fistula due to an ingested toothpick. J Vasc Surg 2009;50:640e3. 5. Tagowski M, Vieweg H, Wissgott C, et al. Aortoenteric Fistula as a Complication of Open Reconstruction and Endovascular Repair of Abdominal Aorta. Radiol Res Pract 2014;2014:383159. 6. Leon L, Psalms S, Ihnat D, et al. Aortofemoral graft limbe toecolon paraprosthetic fistula. J Vasc Surg 2008;47:460. 7. Mansfield L, Seymore H, Kianifard B. Arterio-enteric fistula as a result of typhlitis. Colorectal Dis 2010;12:1270e1. 8. Fumery M, Duchmann J, Andary R, et al. Lower gastrointestinal bleeding due to primary ilioenteric fistula. Abdom Imaging 2012;38:376e8. 9. Nicolaou D, Mysko W. Enteric fistulization of a common iliac artery aneurysm: An unusual cause of gastrointestinal hemorrhage and shock. Am J Emerg Med 1996;14:272e5. 10. Chin CC, Yeh CY, Kuo YH, et al. Massive lower gastrointestinal bleeding from an external iliac artery fistula in a
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Annals of Vascular Surgery
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