Regardless of the underlying etiology, the pathophysiology of ischemic colitis revolves around an inadequate blood supply to the colon. In patients suffering from a rAAA, there are numerous potential etiologies of this decreased blood flow including perioperative hemorrhage resulting in a loss of overall blood volume, prolonged hypotension, splanchnic vasoconstriction due to shock and vasopressors, and cross clamping or balloon occlusion of the aorta. The surgical repair itself, for both the open and endovascular (EVAR) approaches, occludes blood flow (at least temporarily) through the inferior mesenteric artery (IMA), which directly supplies the left colon. In addition, embolization of debris (thrombus and plaque) may occur from opening the aneurysmal sac or manipulation of the graft and wires inside the sac. These embolic phenomena can cause a less predictable variation of ischemic colitis, with numerous reports of right-sided colonic and even small bowel ischemia [9].

However, there is an intrinsic protective mechanism already in place. Although the colon derives its blood supply from branches of the major vessels [i.e., superior mesenteric artery (SMA) and inferior mesenteric artery (IMA)], it is the extensive collateral circulation that allows this ischemic process to be avoided in many cases. The two main collateral routes are via the marginal artery of Drummond that parallels the colon and gives rise to the vasa recta, and the meandering mesenteric artery (or arc of Riolan) which, while not always present, can represent another potential connection between the SMA and IMA systems. In addition, the IMA and internal iliac arteries communicate via the superior and middle hemorrhoidal arteries, while the left colic branch of the IMA contributes to overlap of the transverse colon that is supplied mostly by branches of the SMA. In an otherwise healthy patient, the vast vascular network would prevent any significant degree of colonic ischemia after ligation of the IMA. Yet, patients who suffer a rAAA generally have severe vascular comorbidities and are often in physiologic extremis, which explains why there is such a higher rate of colonic ischemia despite this collateral circulation. Certain parts of the colon are more prone to fluctuations in blood flow, leading to the all-too-common “rounds” question with answers consisting of the splenic flexure (i.e., Sudeck’s) and rectosigmoid junction (i.e., Griffiths). It is felt that these are the most vulnerable segments given that there is incomplete anastomosis of the marginal artery in these two locations. The next most common area affected is the cecum, likely secondary to low blood flow in the terminal branches of the ileocolic artery combined with varying presence and competency of the right colic artery [10–12].

Ischemic colitis is not an all or nothing process. The earliest manifestations are witnessed at the mucosal level, those furthest away from the vasa recta [10, 13] (Fig. 16.2). As such, there is a progression in the stages of ischemic colitis: (a) Grade I, transient mucosal ischemia; (b) Grade II, mucosal and muscularis involvement that may result in healing with fibrosis and stricture formation; and (c) Grade III, transmural ischemia and infarction which results in gangrene and perforation [14] (Fig. 16.3). Importantly, sepsis can occur in the absence of transmural ischemia, as an ischemic mucosa loses its barrier function and allows bacterial translocation to occur, which may result in sepsis.

There are certain risk factors that clearly put a patient with an AAA at higher risk of suffering ischemic colitis. The greatest risk factor is the focus of this chapter; a patient with a rAAA has a two- to fourfold increased risk for ischemic colitis. Interestingly, those underdoing surgery with a symptomatic aneurysm (even in the absence of rupture) have higher rates of ischemic colitis than elective repair based on size criteria alone in the absence of symptoms. Other independent risk factors for colonic ischemia include renal insufficiency, open versus endovascular repair, operative time >4 h, prolonged cross clamp, preoperative hypotension, aorto-bifemoral graft placement, and postoperative acidosis [15, 16].

Many of these make intuitive sense. Others have second- or third-order ramifications that promote the onset of ischemic colitis. For example, renal insufficiency itself results in a decreased ability to handle changes in volume, clear toxins, and recovery from any physiological insult. Yet, in addition, it is thought to be a marker of systemic atherosclerotic disease, which would be reflected in the mesenteric vessels that directly supply the colon, therefore decreasing the colon’s tolerance to hypotension. Worsening of renal insufficiency following repair may also represent a reflection of the severity of hypotension the patient endured perioperatively.

While the exact operative time that correlates with the onset of ischemic colitis is likely more variable, when the length of surgery is over 4 h, studies have shown a four- to sixfold increase in incidence [16]. This is likely related both to the technical difficulty of the surgery and associated hypotension and blood requirement needed during the operation. Open repair is another independent risk factor for colonic ischemia, as demonstrated in one large national database review that showed that open elective AAA repair had a rate of 2.2 % versus 0.5 % with elective EVAR repair [4]. A small randomized trial comparing open and endovascular repair in patients with rAAA found half the rate of colonic ischemia (8 % vs. 4 %) when using EVAR, but it was underpowered to reach significance [17]. However, it is remarkable to witness the drastic drop in onset with the use of endovascular approaches, even in the setting of rupture.

Some surgeons have recommended reimplanting the IMA to allow restoration of direct “forward flow” from the aorta to the left colon. While controversial, IMA reimplantation with an open repair has multiple studies, including a randomized controlled trial, that have failed to show a decreased rate of colonic ischemia with IMA reimplantation when compared with ligation of the IMA and maintenance of normothermia and normal blood pressures. On the other hand, common vascular surgery dogma is to do whatever possible to prevent pelvic ischemia because once it occurs, it is likely not reversible and is associated with high morbidity rates [18]. With this in mind, many surgeons will reimplant based on intraoperative findings such as poor backflow from the IMA (<40 mmHg) or decreased antimesenteric vasculature Doppler signals [16, 19]. An additional tool used in the past was laser Doppler flowmetry, which measures the erythrocyte flux to bowel segments and has been specifically shown to be a successful tool to determine the necessity of reimplanting the IMA [20]. More recent advances, such as the intraoperative availability of indocyanine green [21, 22] that can demonstrate real-time perfusion, may soon find its way into this intraoperative algorithm for evaluating colonic ischemia—even though it still not applicable to EVAR cases. Other more traditional operative tools such as Doppler or Wood’s lamp with fluorescent dyes can only be used in open surgery to help determine bowel viability. In contrast, there is a device available that can be used in open and endovascular aneurysm repairs that utilizes a probe placed in the rectum and measures tissue oxygen saturation. It has been shown to be sensitive in predicting colonic ischemia if the saturation drops below fifty percent of baseline. This tool can provide objective evidence to allow the opportunity to revascularize the IMA or the hypogastrics [23]. While promising, the current data is limited, and ultimately only longer-term data with a wider experience will determine its role in the evaluation and treatment of ischemic colitis.

The importance of hypogastric preservation also appears to be predicated highly on the method of repair—endovascular versus open. In open surgery, there are higher rates of colonic ischemia when hypogastric aneurysms are present or if both hypogastrics are ligated [24]. With endovascular repair, there is literature that states there are only minimal complications associated with embolization of the hypogastrics [25–27] and other series reporting increased risk of colonic ischemia if they are not preserved [28, 29]. In the setting of rAAA, there is only anecdotal evidence when discussing preserving hypogastrics, but given the extremis that patients are often in, it is likely prudent to preserve any potential collaterals to the colon, if possible. Yet, the surgeon must take into account the stability of the patient and weigh any downside that may occur with the additional operative time that another procedure would require.

Additional risk factors for the development of ischemic colitis that have no randomized data, but have been reported in small retrospective studies, include previous colonic surgery and pelvic irradiation. This should also make sense, as patients who have had previous colonic surgery have likely had the collaterals between the SMA and IMA disrupted. While there was a substantial rate of colonic ischemia in this subset of patients, these reports have been largely underpowered [16]. Yet, even a patent meandering marginal artery (arc of Riolan) has been shown to have some protective effects against ischemic colitis [30].

Finally, pelvic irradiation leads to obliteration of the microvasculature to the sigmoid and rectum, creating conditions ripe for small vessel ischemic changes. Furthermore, these radiation effects are cumulative and progressive, a fact often overlooked. Although it has not been widely studied, this appears to be a real association with patients at a higher risk of developing ischemic colitis [31]. Furthermore, this may be a precipitating factor not only in early disease but helps to explain the underlying disorder that leads to chronic changes such as colonic stricture.

The key to diagnosing ischemic colitis first and foremost involves a high degree of suspicion by the treating provider, especially given the drastic improvements in outcomes for patients that are recognized and treated promptly. Unfortunately, the signs and symptoms vary drastically and are remarkably inconsistent from patient to patient. Occasionally, ischemic colitis is recognized intraoperatively; however, that tends to be way too late. Despite a somewhat “textbook” presentation for more severe forms, the mean time to diagnosis remains ~5.5 days [14].

This delay is secondary to the wide-ranging spectrum of disease—from mild mucosal sloughing to severe (perforation and sepsis). In some cases, the majority of symptoms are often self-limited and nonspecific. The most common symptoms encountered are left lower quadrant pain, bloating, and diarrhea. The diarrhea is a consequence of mucosal sloughing which causes colonic peristalsis. Depending on the extent and severity of the ischemia, patients can present with melena, hematochezia, watery diarrhea, or even no diarrhea at all. The abdominal pain may be limited to the hypogastrium or left lower quadrant or in more severe cases present with frank peritonitis and diffuse pain. Similar to the symptomology, the imaging and laboratory studies are generally nonspecific. Plain films may show colonic dilatation and/or fluid levels. More advanced cases may have pneumatosis, portal venous gas, or pneumoperitoneum.

Historically, barium enemas were used, often showing mucosal edema suggested by thumbprinting or colonic strictures with more chronic disease. In general, barium should be avoided in this setting. Water-soluble enemas may demonstrate similar findings but are much less commonly used. The workhorse of radiology tests remains the CT scan. Although they are not initially as sensitive, later in the course, they can be more helpful showing colonic wall thickening and an inflamed edematous mesentery/fat stranding. CT also provides the ability to evaluate the bowel as well as the surrounding tissue. In this light, mucosal enhancement, intramural air, bowel dilatation, or even more ominous signs such as portal venous gas can be visualized. It can also be a very useful test in ruling out other diagnoses [32]. In general, angiography does not help in patients with acute ischemic changes and is rarely used for vessel patency (embolic/thrombotic) or to rule out other sources.

Laboratory examinations are similarly nonspecific for ischemic colitis, and no marker exists to date that is specific in identifying colonic ischemia. For more advanced cases, a leukocytosis and metabolic acidosis may be present. Occasionally, electrolyte and renal abnormalities (i.e., hypokalemia, rising BUN/Cr) may be present due to severe diarrhea combined with a lack of oral intake. Serum lactate levels may be elevated, though generalized systemic hypoperfusion or tissue hypoxia may also cause this, and is therefore not a specific marker. Unfortunately, many of these concerning lab values such as lactate, creatinine, acidosis, or leukocytosis are all commonly seen postoperatively after a rAAA. A small prospective study of 12 patients who underwent open AAA repair reported an elevated d-lactate (uncommon isomer of more common L-lactate) could be detected within 2 h postoperatively in patients with ischemic colitis compared to patients without ischemic colitis [13]. Yet, this has yet to achieve widespread clinical use.

Colonoscopy remains the most sensitive and specific study available for diagnosis of ischemic colitis (Fig. 16.4). Some suggest that any concern for colonic ischemia warrants an endoscopic evaluation and even argue routine endoscopy after rAAA using a flexible sigmoidoscopy should be performed within 24 h of the surgery. Endoscopy has a diagnostic accuracy of 78–98 % for ischemic colitis [33], in part due to the wide extent of changes and characteristics ischemia has when viewed endoscopically. In the acute phase, the bowel will demonstrate hyperemia, edema, friable mucosa, ulcerations, and petechial hemorrhages. As the ischemia progresses, evidence of submucosal edema and hemorrhage may appear as bluish-black blebs or nodules protruding into the lumen of the bowel [34]. When full-thickness transmural ischemia occurs, the mucosa typically appears gray or black, indicating gangrene. If the ischemia is more chronic, changes such as strictures and fibrosis would be endoscopy also allows the examiner to sample the colonic mucosa for pathologic assessment to help differentiate inflammatory, infectious (e.g., C. difficile), and ischemic etiologies. In reality, biopsy (Fig. 16.5) is rarely useful and is more likely to demonstrate either nonspecific ischemic or inflammatory changes and rarely shows the ghost cells that are classic for ischemia [11]. It is important to recognize that endoscopy is not without its own potential hazards. Air insufflation may result in distention of the bowel, diminishing colonic blood flow and may actually worsen the colonic ischemia [9]. In addition, the ischemic wall of the colon is fragile and at an increased risk of perforation. Chronically, endoscopy will demonstrate a smooth stricture without an associated mass, consisted with the fibrotic process that occurs over time [35].

There have been two prospective studies that have evaluated the effectiveness of routine colonoscopic screening in all patients who survive after the initial repair of a rAAA (Figs. 16.6 and 16.7). The first study by Megalopoulas et al. [36] identified preoperative risk factors (hypotension, temperature, pH, > 6 units PRBCs, fluid sequestration >5 L) that correlated with the presence of ischemic colitis. The authors concluded that when less than four were present, they were unlikely to develop colonic ischemia and therefore did not need routine endoscopic screening. One criticism of this study was that it is difficult to extrapolate to outside hospitals, as many of the parameters depend on the overall management of the patient apart from the use of endoscopy. To address this deficiency, Tottrup and colleagues prospectively screened 41 patients who survived a rAAA with colonoscopy in the first 24 h following surgery. Only nine of their patients developed colonic ischemia, and there were no perioperative or intraoperative clinical or biochemical parameters that were sufficiently reliable to distinguish patients with colonic ischemia versus those without [6]. Their conclusion was that the worse outcomes associated with a delayed diagnosis of colonic ischemia after rAAA warrant all patients to undergo routine endoscopic surveillance [37].

Conversely, routine surveillance has been questioned by those who feel colonoscopy does not necessarily change the management of patients and can even exacerbate the problem by placing a scope in a friable segment of bowel and filling it with pressurized air. They argue that if a patient has suggestive symptoms along with radiologic and examination findings concerning for severe ischemic colitis, they should undergo an exploration. On the other hand, if a patient has clinical signs of ischemic colitis but lacks peritoneal signs or sepsis, they should undergo supportive therapy alone. This argument is supported by a study that showed that clinicians are unable to differentiate mucosal versus transmural necrosis reliably with colonoscopic evaluation [38].

Once ischemic colitis is identified, treatment falls into two categories depending on the degree of injury: supportive therapy and colectomy. As most patients present with only mucosal ischemia, their clinical course is often relatively benign and warrant supportive therapy alone. Supportive therapy consists primarily of fluid resuscitation, blood pressure support, bowel rest, and antibiotics. Broad-spectrum antibiotics should typically be started due to risk for bacterial and endotoxin translocation following disruption of the mucosal membrane. Vasopressors should be used cautiously and only in septic patients. Alpha agonists are likely to worsen colonic ischemia by further reducing splanchnic blood flow. Beta-adrenergics can be considered as a first-line option if fluid therapy is inadequate to maintain blood pressure. However, pressor requirement should prompt the physician to consider if an abdominal exploration is warranted. The majority of these patients have a poor nutritional status at baseline and a high metabolic demand and will likely have a prolonged time that they will be NPO; therefore, early parenteral nutrition is often required.

Serial abdominal exams, laboratory testing, and plain film labs should be performed to monitor for worsening in their condition. Approximately 10 % of patients will fail supportive therapy and ultimately require a colectomy. Failure of supportive therapy can be obvious with signs of peritonitis, or it can be more insidious. There are patients that will continue to have persistent pain, leukocytosis, low-grade fevers, tachycardia, tender abdominal exam, but not frank peritonitis. After ruling out other sources of sepsis, abdominal exploration with colectomy is often undertaken, as the devitalized colon serves as the source for persistent problems. Decisions on when to repeat flexible endoscopy vary, but likely should be repeated if there are no resolution in symptoms, an acute change in symptoms, or prior to beginning an oral diet.

When Grade III or transmural/gangrene is identified, emergent colectomy is almost always indicated. This subset of patients, even with colectomy, have mortality rates >50 %. Patients who suffer a rAAA, compared to an elective AAA repair, and develop colonic ischemia are more likely to undergo a colectomy [4]. This is due to the larger physiologic insult that occurs with rupture. Interestingly, one study found patients undergoing colectomy for ischemic colitis after elective EVAR had significantly higher mortality than patients undergoing colectomy for rAAA or open AAA repair. This should not be misinterpreted; however, as EVAR is generally much safer and associated with lower rates of ischemic colitis. More likely, this finding reflects the delay in diagnosis, as suspicion is generally lower after elective EVAR, or the differing mechanism of the ischemic insult (i.e., cardiac) [4].

With rare exceptions, all patients with evidence of bowel infarction or perforation require surgical exploration. The greatest challenge associated with abdominal exploration is determining which portion of bowel is salvageable and which is nonviable. When evaluating the bowel intra-abdominally, it is important to remember that the serosa may appear healthy, even when there is actually full-thickness mucosal and muscularis necrosis. It is often helpful to combine an endoscopic evaluation to help determine the level of bowel viability (even despite its relative lack of accuracy). Laser Doppler flowmetry and spectrophotometry are all techniques that can assist clinical judgment in deciding bowel viability and what requires resection and what can be salvaged. Furthermore, palpation of mesenteric pulses, detecting Doppler signals on the antimesenteric portion of the bowel wall, and Wood’s lamp evaluation of the bowel wall following administration of fluorescein dye intravenously are all described techniques to help separate perfused from non-perfused bowel. Some surgeons will routinely perform a second look operation in 24–48 h, whereas others will perform it selectively when there is higher concern for intestinal viability (see Algorithm).

Operative therapy must consider both the need for bowel resection and vascular reconstruction. The surgeon must balance the need to avoid leaving behind necrotic bowel with the potential morbidity of overzealous resection leading to short bowel syndrome, although the intraoperative judgment of the well-trained surgeon remains one of the most important factors. In most cases, surgical resection involves a total abdominal colectomy with end ileostomy (Fig. 16.8). Although primary anastomosis after a subtotal or partial colectomy (Fig. 16.9) with a proximal diversion may be considered in isolated hemodynamically stable patients with healthy bowel margins, this is often a poor choice [34]. Regardless of the approach, the need for an exploration and bowel resection in the acute setting has been associated with mortality rates as high as 40 %, particularly when the patients has multiple underlying comorbidities [39].

Finally, vascular repair involves first determining the patency of the vessel supplying the at risk portion of the colon. In addition, determining whether there is antegrade flow to the iliac vessels that may provide potential pelvic collaterals is crucial. While the technical aspects of vascular reconstruction are beyond the scope of this chapter, options for dealing with the inferior mesenteric artery or other major visceral vessels include resection of the base of the vessel along with a small cuff of aortic wall (Carrel patch) and reimplanting it in the aorta or graft, patch angioplasty of the stenotic opening, bypass grafting, or endarterectomy of the atherosclerotic plaque [40–42]. In either light, embarking on a complex vascular reconstruction should not be undertaken lightly and again needs to be weighed against the potential downside of prolonged operative time, excess blood loss, and failure of the repair.

Ischemic colitis is the leading cause of death after repair of a rAAA. With few operative or clinical parameters that are sensitive or specific for colonic ischemia, suspicion must remain high in the postoperative period. Early identification and treatment of this feared complication is the only clear way to help reduce morbidity and mortality.