From the Eastern Vascular Society
Embolization as cause of bowel ischemia after endovascular abdominal aortic aneurysm repair Wayne W. Zhang, MD,a Mahmoud N. Kulaylat, MD,b Paul M. Anain, MD,c Hasan H. Dosluoglu, MD,a Linda M. Harris, MD,a Gregory S. Cherr, MD,a Merril T. Dayton, MD,b and Maciej L. Dryjski, MD, PhD,a Buffalo, NY Objective: We investigated the incidence, cause, and outcome of large bowel and small bowel ischemia after endovascular abdominal aortic aneurysm (AAA) repair. Methods: Medical records for all patients undergoing endovascular AAA repair from December 1999 to December 2003 were reviewed. The incidence, cause, and outcome of clinically detected postoperative bowel ischemia were analyzed. Results: Seven hundred two endovascular AAA repairs were performed. In 10 patients (1.4%) acute bowel ischemia developed. Six of these patients sustained concurrent small bowel necrosis, and the remaining 4 had isolated colon ischemia. Seven patients underwent exploratory laparotomy. In 6 of these bowel resection was performed, and in 1 patient the ischemic bowel was unsalvageable. Of the 6 patients with small and large bowel ischemia, 4 had segmental or patchy necrosis, which was separated by normal-appearing intestine, and 1 had extensive ischemia that involved most of the small bowel and the entire colon, with pathologic evidence of microembolization. Three patients had preoperative occlusion of the inferior mesenteric artery. One had unilateral and 1 had bilateral hypogastric artery interruption. Five of the 6 patients with small bowel ischemia had thrombus or atheroma in the proximal aneurysmal necks. All patients with isolated colon ischemia survived. All 6 patients with concurrent small bowel ischemia died. Conclusion: The total incidence of clinically evident bowel ischemia after endovascular AAA repair is similar to that after open surgery. However, small bowel ischemia occurs more commonly in patients with endovascular repair, and is associated with extremely high mortality. The direct pathologic evidence and the patterns of segmental, skipped, or patchy ischemia in most patients imply that microembolization has an important role. ( J Vasc Surg 2004;40:867-72.)
Bowel ischemia is a devastating complication after open or endovascular abdominal aortic aneurysm (AAA) repair. Retrospective studies have documented the incidence of colonic ischemia at 1.2% to 2.0% after open procedures1-5 and 2.9% after endovascular repair,6 and prospective colonoscopic investigations have shown that bowel ischemia may occur as frequently as 6% to 30% in patients after open surgery.7-10 Severity varies from mucosal to transmural ischemia, and the mortality rate ranges from 0% to 100%.4-7,10Interruption of the inferior mesenteric artery and hypogastric artery have been presumed to be the major cause. However, in a multicenter study the incidence of postoperative colonic ischemia was 1.3% in 7 centers in which inferior mesenteric artery revascularization was routinely performed, and 1.1% in 28 centers in which inferior mesenteric artery revascularization was not performed routinely.1This suggests that other causes may be more important.
Dadian et al6 reported that colon ischemia after endovascular aneurysm repair (EVAR) occurred in 1 of 122 patients (0.8%) who required unilateral or bilateral hypogastric artery interruption and in 7 of 156 patients (4.5%) without hypogastric artery interruption. Microembolization as a cause of postoperative colon ischemia may be more important in patients who undergo EVAR than in those who undergo open repair.6Other possible causes include intraoperative hypotension, reperfusion injury, anatomic features, bowel manipulation, and iatrogenic injury, but these mechanisms are not likely to have a role in EVAR. Although EVAR has been widely used for treatment of AAA in the past several years, the incidence and cause of postoperative bowel ischemia, especially small bowel ischemia, remain unclear. The purpose of this study was to investigate the incidence, cause, and outcome of large and small bowel ischemia after endovascular AAA repair. METHODS
From the Division of Vascular Surgery, Department of Surgery, State University of New York at Buffalo,a the Department of Surgery, State University of New York at Buffalo,b and the Division of Vascular Surgery, Buffalo Catholic Health System.c Competition of interest: none. Presented at the Eighteenth Annual Meeting of the Eastern Vascular Society, Philadelphia, Pa, Apr 29 –May 2, 2004. Reprint requests: Maciej L. Dryjski, MD, PhD, Department of Surgery, State University of New York at Buffalo, Millard Fillmore Hospital, 3 Gates Circle, Buffalo, NY 14209 (e-mail:
[email protected]). 0741-5214/$30.00 Copyright © 2004 by The Society for Vascular Surgery. doi:10.1016/j.jvs.2004.08.054
This study was performed as a retrospective chart review. No attempt was made to identify subclinical cases of bowel ischemia. Medical records for all patients who underwent endovascular repair from December 1999 to December 2003 in Kaleida Health System and Buffalo Catholic Health System were reviewed. Endografts including AneuRx (Medtronic/AVE), Ancure (Guidant), Zenith (Cook), and Excluder (W. L. Gore & Associates) were used. Various sizes of standard grafts and sheaths were placed, based on the different sizes of aorta and access vessels in different patients. 867
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Table I. Demographic data for patients with colon and small bowel ischemia after endovascular AAA repair Aneurysm diameter Patient (cm)
Operating time for AAA Site of Colon (min) aneurysm ischemia
Small bowel ischemia
1
5.7
420
Infrarenal Left colon
2
6.8
360
Juxtarenal Sigmoid Distal ileum
3
8
160
Infrarenal Left colon
4
5.3
280
5
7
115
Infrarenal Sigmoid Distal and ileum rectum Infrarenal Sigmoid No
6
6.3
235
Infrarenal Entire colon
7
5.7
50
8
7.3
68
9
6
Infrarenal Left colon Infrarenal Left colon Infrarenal Entire colon
10
5.4
165
90
Previous bowel resection
Management
Other related complications
Distal No jejunum
Graft
Outcomes
Left Left “blue hemicolectomy; toes” segmental resection of distal jejunum Right Left No* hemicolectomy hemicolectomy; segmental resection of distal ileum No Subtotal Acute renal colectomy; failure segmental resection of small bowel No Extended left Acute renal hemicolectomy failure
Ancure Death (aspiration pneumonia 4 months later) Ancure Death
No
Sigmoidectomy
AneuRx Survival
Jejunum and ileum
No
No
No
Subtotal colectomy; segmental resection of small bowel; second exploration Conservative
Left trash buttock Acute renal failure
No
Ancure Survival
No
No
Conservative
No
Ancure Survival
Jejunum and ileum
Sigmoidectomy
Exploratory laparotomy (open and close) Conservative
Acute renal failure
AneuRx Death
No
AneuRx Survival
Distal ileum
Infrarenal Sigmoid No
No
AneuRx Death
AneuRx Death
AneuRx Death
AAA, Abdominal aortic aneurysm. *Patient had chronic renal failure and had been receiving hemodialysis for years.
Charts were reviewed to identify all cases of clinically documented bowel ischemia. Bowel ischemia was diagnosed on the basis of clinical findings at presentation, endoscopy, or exploratory laparotomy. In patients in whom acute ischemia developed, additional data, including initial history and physical examination, laboratory analyses (complete blood cell count; electrolytes, arterial blood gas, lactate acid levels), anesthesia records, colonoscopy descriptions, operative reports, and pathologic results were collected. Preoperative and postoperative images, including computed tomography (CT) scans and aortograms, in patients with bowel ischemia were reviewed. RESULTS Seven hundred two patients underwent EVAR during the study period. In 10 patients (1.4%) acute bowel ischemia developed. All 10 patients had colon ischemia, and 6 sustained concurrent small bowel infarction (Table I). Four
patients were men, and 6 were women; their age range was 68 to 85 years. Aneurysms were 5.3 to 8.0 cm in diameter. Nine aneurysms were infrarenal, and 1 was juxtarenal. The patient with the juxtarenal aneurysm had end-stage renal disease, and had been receiving hemodialysis for several years before EVAR. In this patient the juxtarenal aneurysm was repaired by deploying an Ancure graft above the renal arteries. The percentage of bowel ischemia was 1.4% (6 of 429) in patients who received AneuRx grafts, and 1.6% (4 of 255) in patients who received Ancure grafts. Excluder and Zenith grafts were placed in only 9 patients each with no bowel ischemia. Three patients had preexisting occlusion of the inferior mesenteric artery. One patient underwent unilateral hypogastric artery interruption with microcoils before EVAR, and 1 patient had bilateral hypogastric artery interruption from endovascular grafts without revascularization. Of the 10 patients with bowel ischemia, only 1 had mild (⬍50%)
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Fig 1. Computed tomography scans show thrombus or atheroma in proximal neck of abdominal aortic aneurysm (arrows; A), and thrombus or atheroma in bilateral iliac arteries (arrows; B). These are possible sources of microembolization during endovascular aneurysm repair.
superior mesenteric artery stenosis. The celiac arteries in all 10 patients were patent. None of the 10 patients had preexisting symptoms of mesenteric ischemia. One patient had intraoperative hypotension, with systolic blood pressure of 70 to 80 mm Hg for 15 minutes. One patient had intraoperative oliguria, and 1 patient with end-stage renal disease had been receiving hemodialysis for several years.
At presentation the 6 patients with both small and large bowel ischemia had postoperative abdominal distention, shock, and acidosis. All 6 patients, except 1 who received a nasogastric tube and sedation postoperatively, complained of abdominal pain. Two patients had bloody diarrhea. The 4 patients with isolated colon ischemia had abdominal pain, and 3 had early postoperative diarrhea.
Table II. Anatomic features of AAA and ischemic bowel
Preoperative patency of IMA
Thrombus or atheroma in aneurysm neck
Patency of hypogastric artery Bowel Patient ischemia 1 2 3 4 5 6 7 8 9 10
Preoperative
Postoperative
Thrombus or atheroma in access vessels
Type of ischemia
Direct evidence of microembolization
Colon/ small bowel Colon/ small bowel Colon/ small bowel Colon/ small bowel Sigmoid
Patent
Patent
Occluded
Yes
Bilateral iliac arteries
Transmural
Skipped, segmental ischemia
Patent
Patent
Patent
Yes
No
Transmural
Skipped, segmental ischemia
Patent
Patent
Patent
Yes
No
Transmural
Skipped, segmental ischemia
Patent
Bilaterally interrupted
Occluded
No
No
Transmural
Skipped, segmental ischemia
Patent
Occluded
Yes
None
Patent
Patent
Yes
Bilateral iliac arteries No
Transmural
Colon/ small bowel Colon Colon Colon/ small bowel Sigmoid
Right interrupted Patent
Transmural
Microscopic embolization
Patent Patent Patent
Patent Patent Patent
Patent Patent Patent
No No Yes
No No No
Mucosal Mucosal Transmural
Patchy ischemia Patchy ischemia None
Patent
Patent
Patent
No
No
Mucosal
Patchy ischemia
AAA, Abdominal aortic aneurysm; IMA, inferior mesenteric artery.
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separated by normal-appearing intestine, and 2 had extensive ischemia involving most of the small bowel and the entire colon. One of these patients demonstrated direct pathologic evidence of massive microembolization. Four patients with combined ischemia also had acute renal failure postoperatively. Microembolization resulting in trash buttock occurred in 1 of these patients, and distal embolization with “blue toes” occurred in another patient. Review of records for patients with isolated colonic ischemia revealed that 3 of 4 had mucosal ischemia only, which was managed conservatively. In the 7 patients who underwent exploratory laparotomy, 6 had bowel resection, and in 1 patient the ischemic bowel was unsalvageable. Five of the 6 patients with concurrent small bowel ischemia died early, of multiple organ failure related to acute bowel ischemia, and 1 patient died of aspiration pneumonia 4 months postoperatively. All 4 patients with isolated colon ischemia survived. They have been followed up for 18 to 41 months, with no evidence of graft infection. DISCUSSION
Fig 2. Thrombus or atheroma in aneurysm neck is dislodged while deploying the graft, and debris is flushed upstream into superior mesenteric artery by blood flow turbulence caused by guide wire manipulation, graft deployment, and balloon dilation.
Five of the 6 patients with both large and small bowel ischemia had thrombus or atheroma in the proximal neck of the aneurysm. One of the 4 patients with isolated colon ischemia had thrombus or atheroma in the proximal aneurysmal neck and bilateral common iliac arteries (Fig 1). The presence of thrombus or atheroma in proximal neck and access vessels was more frequent in patients with concurrent small bowel ischemia (5 of 6) than in the patients with isolated colon ischemia (1 of 4; Table II). CT scans were reviewed for 100 of 692 patients in whom bowel ischemia did not develop. Twenty-one patients (21%) had thrombus or atheroma in the aneurysm neck. The incidence of aneurysm neck thrombus or atheroma in patients with small bowel ischemia (5 of 6, 90%) and without bowel ischemia (21 of 100, 21%) was compared statistically with the Fisher exact test, and was significantly different (P ⫽ .003). Of the 6 patients with combined small and large bowel ischemia, 4 had segmental or patchy necrosis, which was
Colon ischemia after open AAA repair is a critical complication, and has been well addressed.11-13 However, the incidence, cause, and outcome of postoperative bowel, especially small bowel, ischemia after EVAR are poorly documented.6,14-15 Our data show that the incidence of clinically significant bowel ischemia after EVAR is 1.4%, which is approximately that after open surgery1-5; and small bowel ischemia occurred in 0.8% of patients. Sixty percent of patients with postoperative colon ischemia had concurrent small bowel ischemic infarction, which differs significantly from the ischemia noted after open repair. Prognosis with both large and small bowel ischemia is dismal, with mortality rate as high as 100% in our study. Most patients died of sepsis, shock, and multiple organ system failure. Isolated colon ischemia has a favorable outcome with conservative or surgical treatment. Interruption of the inferior mesenteric artery and hypogastric artery has been suggested as the major cause of bowel ischemia after open AAA repair.11,12,16-19 However, our data indicate that inferior mesenteric artery interruption may not be so important as was suggested previously. Although the inferior mesenteric artery is inevitably interrupted in all patients at EVAR, the incidence of postoperative bowel ischemia in our group was not increased versus that in open procedures. This could be due to the preserved collateral arteries in EVAR, which are frequently jeopardized by dissection during open surgery. Another possible cause of bowel ischemia after open and endovascular AAA repair is hypogastric artery interruption. However, previous studies have debated the necessity of hypogastric artery revascularization in the patients with bilateral hypogastric artery interruption.1,17,19-22 Eight of 10 patients with bowel ischemia in our group had patent hypogastric arteries bilaterally. Only 2 patients had interruption of the hypogastric artery: 1 patient had bilateral hypogastric artery occlusion and 1 patient had unilateral
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hypogastric artery occlusion, from endovascular grafting. Other recent studies have also documented that unilateral, and even bilateral, hypogastric artery interruption is acceptable during EVAR.6,19,20 Incidence, cause, and outcomes of small bowel ischemia after EVAR are poorly documented. In our group, small bowel ischemia occurred in 0.8% of all patients and in 60% of patients in whom postoperative colon ischemia developed after EVAR. Why is small bowel ischemia more common after EVAR versus open procedures? Interruption of the inferior mesenteric artery or hypogastric artery has not been demonstrated to impair the blood supply to the small bowel. The supraceliac aorta is not clamped during endovascular procedures, and the short period of aortic occlusion during balloon dilation does not result in ischemia and reperfusion injury. Therefore the major cause of small bowel ischemia after EVAR is different from that after open repair. In our 6 patients with concurrent small bowel ischemia, 5 patients had thrombus or atheroma in the aneurysm neck or iliac arteries. We presume that the thrombus or atheroma in the neck was dislodged while the graft was deployed and that the debris was flushed upstream into the superior mesenteric artery by blood flow turbulence caused by graft deployment or balloon dilation (Fig 2). The microemboli may be flushed into renal arteries, the inferior mesenteric artery, the hypogastric artery, and distal vessels, leading to acute renal insufficiency, colon ischemia, trash buttock, and blue toes, as well. The direct pathologic evidence and the patterns of segmental, skipped, or patchy ischemia in most of our patients support the concept that microembolization has an important role in both small and large bowel ischemia after EVAR. Although Gitlitz et al23 reported that no symptomatic embolic complications occurred in 19 patients with thrombus in the aneurysm neck, subclinical thromboembolism developed in more than 10% of their patients (2 of 19). The percentage of bowel ischemia was 1.4% in patients with AneuRx grafts (6 of 429) and 1.6% in patients with Ancure grafts (4 of 255). Excluder and Zenith grafts were placed in only 9 patients each, because of the timing of the study, and no bowel ischemia developed. Our data do not suggest that the type of graft is related to the incidence of postoperative bowel ischemia. Seven of the 10 complications of bowel ischemia occurred within the first 2 years of endovascular AAA repair in our hospitals. The lower rate of bowel ischemia may be related in part to improved technical skills, and possibly to careful patient selection. In summary, the total incidence of bowel ischemia after EVAR is approximately that after open surgery. However, small bowel ischemia occurs more commonly after EVAR, with extremely high mortality, especially in patients with full-thickness ischemia. Microembolization is a major cause of both small and large bowel ischemia after EVAR. To prevent bowel ischemia caused by microembolization, we recommend the following: (1) careful review of preoperative images to identify thrombus or atheroma in the neck of the aneurysm; (2) minimal manipulations during graft deployment; (3) direct deployment of the stent immediately
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inferior to the renal arteries, rather than dragging them down from above; and (4) open repair if a large amount of thrombus is present in the proximal aneurysm neck. Patients with thrombus or atheroma in the neck of aneurysm should be closely followed up postoperatively. Colonoscopy should be performed if there is any suspicion of microembolization, such as blue toes. Small bowel ischemia should be suspected in patients with clinical symptoms that suggest more severe ischemia than is found at colonoscopy. Because the prognosis is extremely poor, early exploratory laparotomy should be considered if small bowel ischemia cannot be ruled out. REFERENCES 1. Pittaluga P, Batt M, Hassen-Khodja R, Declemy S, Bas PL. Revascularization of internal iliac arteries during aortoiliac surgery: a multicenter study. Ann Vasc Surg 1998;12:537-43. 2. Ernst CB. Prevention of intestinal ischemia following abdominal aortic reconstruction. Surgery 1983;93:102-6. 3. Fry PD. Colonic ischemia after aortic reconstruction. Can J Surg 1988;31:162-4. 4. Brewster DC, Franklin DP, Cambria RP, Darling RC, Moncure AC, Lamuraglia GM, et al. Intestinal ischemia complicating abdominal aortic surgery. Surgery 1991;109:447-54. 5. Bjorck M, Bergquist D, Troeng T. Incidence and clinical presentation of bowel ischemia after aortoiliac surgery: 2930 operations from a population-based registry in Sweden. Eur J Vasc Endovasc Surg 1996; 12:139-44. 6. Dadian N, Ohki T, Veith FJ, Edelman M, Mehta M, Lipsitz EC, et al. Overt colon ischemia after endovascular aneurysm repair: the importance of microembolization as an etiology. J Vasc Surg 2001;34:986-96. 7. Ernst CB, Hagihara PF, Daughtery ME, Sachatello CR, Griffen WO Jr. Ischemic colitis frequency following abdominal aortic reconstruction: a prospective study. Surgery 1976;80:417-21. 8. Hagihara PF, Ernst CB, Griffen WB Jr. Frequency of ischemic colitis following abdominal aortic reconstruction. Surg Gynecol Obstet 1979; 149:571-3. 9. Ourie K, Fiore WM, Geary JE. Detection of occult colonic ischemia during aortic procedures: use of an intraoperative photoplethysmographic technique. J Vasc Surg 1988;7:5-9. 10. Welch M, Baguneid MS, McMahon RF, Dodd PD, Fulford PE, Griffiths GD, et al. Histological study of colonic ischemia after aortic surgery. Br J Surg 1998;85:1095-8. 11. Ernst CB. Colon ischemia following aortic reconstruction. In: Rutherford RB, editor. Vascular surgery. 5th ed. Philadelphia (PA): Saunders; 2000. p 1542-9. 12. Valentine RJ. Intestinal ischemia complicating abdominal aortic reconstruction. In: Ernst CB and Stanley JC, editors. Current therapy in vascular surgery. 4th ed. St Louis (MO): Mosby; 2001. p 294-8. 13. Elmarasy N, Soong CV, Walker SR, Macierewicz JA, Yusuf SW, Wenham PW, et al. Sigmoid ischemia and the inflammatory response following endovascular abdominal aortic aneurysm repair. J Endovasc Ther 2000;7:21-30. 14. Miahle C, Amicabile C, Becquemin JP. Endovascular treatment of infrarenal abdominal aneurysms by the Stentor system: preliminary results of 79 cases. J Vasc Surg 1997;25:165-72. 15. Moore WS, Kashyap VS, Vescera CL, Quinones-Baldrich WJ. Abdominal aortic aneurysm: a 6-year comparison of endovascular versus transabdominal repair. Ann Surg 1999;230:298-308. 16. Iliopoulos JI, Pierce GE, Hemreck AS, Haller CC, Thomas JH. Hemodynamics of the inferior mesenteric arterial circulation. J Vasc Surg 1990;11:120-6. 17. Seeger JM, Coe DA, Kaelin LD, Flynn TC. Routine reimplantation of patent inferior mesenteric arteries limits colon infarction after aortic reconstruction. J Vasc Surg 1992;15:635-41.
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Submitted May 17, 2004; accepted Aug 8, 2004.
