Lower gastrointestinal hemorrhage is typically a disorder that affects the elderly with a wide range of clinical presentations. Most bleeding stops with conservative management; thus, the vast majority of affected patients do not receive diagnostic imaging or intervention. Those with refractory bleeding are usually evaluated with nuclear scintigraphy, angiography, colonoscopy, or some combination of the three. Management options include local endovascular vasoconstrictive therapy, thermal cautery or bipolar injection delivered via an endoscope, and surgical resection. Superselective colonic embolization is rapidly gaining acceptance as a treatment option for severe colonic hemorrhage. It has many advantages as compared with more invasive procedures and is increasingly preferred to vasopressin infusion.

Etiologies of bleeding

Colonic bleeding may arise from a variety of causes, but it is most common in the elderly due to acquired conditions: diverticular disease, neoplasia, and angiodysplasia. All occur with increasing frequency with advancing age. Diverticular disease is unusual before age 40 years but is common after age 50 years and found in 66% of patients older than 80 years [1,2]. Diverticula are formed at the site where the vasa recta penetrate the muscular wall of the colon. Approximately 10% to 20% of patients with diverticula will experience bleeding [3,4], and affected patients typically have coexisting clinically active, serious medical or surgical conditions [5]. Meyers and associates [6] ascertained the etiology of bleeding in the 1970s by performing arteriography in resected colonic specimens. They found that hemorrhage begins in the dome or neck of the lesion with rupture through the media. Comparison of bleeding and nonbleeding diverticula demonstrated the role of trauma, presumably stercoral, in rupture. Diverticulitis was conspicuously absent in patients with severe bleeding. Although diverticula are usually found in the left colon, right-side diverticula appear to have a higher incidence of bleeding [1].

Angiodysplasia is a vascular abnormality that predominates in the right colon and cecum and, like diverticular disease, increases in frequency with aging. The pathophysiology of this lesion remains unproven. One proposed theory is that the anomaly begins as submucosal venous ectasia due to chronic partial obstruction that occurs during muscular contraction and distention [7]. Subsequently, the dilated veins lead to precapillary sphincter incompetence and arteriovenous communication. The preferential distribution in the cecum and right colon is explained by the law of Laplace [8]. The right colon and cecum have the highest wall tension because this portion of large bowel has the largest diameter. Bleeding from angiodysplasia usually occurs after age 60 years. Although fewer than 10% of affected patients will have hemorrhage, bleeding recurs after cessation in 85% of patients [9,10].

Benign and malignant polyps and larger tumors may cause a spectrum of bleeding. Boley et al. [11] reported that 8.3% of minor lower gastrointestinal hemorrhage and 5% of major hemorrhage are caused by colon cancer. Because neither angiography nor nuclear scintigraphy tends to definitively diagnose the etiology of hemorrhage even when patients are actively bleeding, colonoscopy should be performed in all patients with colonic hemorrhage, even those who are successfully managed with embolization.

Screening

The triage and evaluation of patients with lower gastrointestinal hemorrhage remain controversial and largely institution specific. The dynamic nature of severe bleeding leads to limitations with all techniques. To best manage bleeding, it is useful to stratify patients based on severity of hemorrhage. As a rule, more severe bleeding is best evaluated by angiography and less severe bleeding is best evaluated with colonoscopy. Recurrent minor bleeding is best evaluated and managed with colonoscopy after an aggressive bowel preparation. The strength of colonoscopy lies in its ability to provide diagnostic information in the absence of active bleeding. Its weakness is that it is relatively useless when performed without bowel preparation in patients with more significant bleeding. These latter patients are better evaluated with nuclear scintigraphy or angiography.

Hemodynamically stable patients with severe but intermittent bleeding should be evaluated with Tc-99M red blood cell scanning. This technique is advantageous as compared with angiography because scanning is performed continuously over a 2-h period. In our hospital, we consider a positive red blood cell study an urgent indication for angiography and attempt to perform the latter study within 1 h of positive scintigraphy, day or night. The rationale for this algorithm is the desire to “catch” bleeding while it remains active [12]. Scintigraphy also helps to guide angiography because the site of bleeding is often revealed, thereby enabling “targeted” angiography to be performed. Patients who are hemodynamically unstable with severe unremitting bleeding should forego nuclear scintigraphy and instead undergo resuscitation and receive angiography as soon as possible.

Helical computed tomography (CT) is emerging as a promising diagnostic option. A recent study by Kuhle and Sheiman [13] reported that bleeding rates slower than 0.4 mL/min are detectable in swine provided that peak aortic enhancement reaches 100 HU. A few clinical reports from Europe also have studied the role of CT in localizing acute lower gastrointestinal bleeding. Ernst et al. [14] noted that triple-phase CT correctly located 80% (four of five) of proven small bowel hemorrhages and 79% (11 of 14) of large bowel hemorrhages. An earlier study by Ettore et al. [15] found that 72% (13 of 18) of patients with lower gastrointestinal hemorrhage could be diagnosed using CT.

History

The concept of colonic embolization for lower gastrointestinal bleeding is not new and was attempted as early as the 1970s by Rosch and Bookstein [16,17]. By current standards, the catheters and embolic materials available then were primitive, and initial efforts led to unacceptably high rates of ischemia and infarction ranging from 13% to 33% [16,18,19]. Throughout the 1980s, colonic embolization was generally considered taboo. Instead, most interventional radiologists employed vasopressin infusion as the endovascular therapy of choice. This therapy has important limitations including a failure rate greater than 20% and a rebleeding rate greater than 15% [20]. In addition, it is very labor intensive and time consuming due to management of an indwelling arterial catheter.

Dissatisfaction with catheter-directed vasoconstriction led to renewed interest in embolization in the late 1980s and early 1990s when coaxial microcatheters became available (Fig. 1). These catheters typically range in size from 2.5 to 3 French in diameter and can be advanced through a 5-French catheter. Thus, a conventional 5-French catheter may be used to select a first-order vessel (e.g., superior or inferior mesenteric artery) and a microcatheter can be advanced through this catheter to more distal, smaller vessels. In the mesenteric circulation, the marginal artery (Fig. 2) or vasa recta (Fig. 3) can be selectively catheterized very close to the site of bleeding; this has been termed superselective catheterization. Once the bleeding vessel has been superselectively catheterized, embolic material can be deployed to arrest hemorrhage. Superselective embolization limits the segment of bowel at risk for ischemia or most often obviates the risk altogether.

Choice of embolic

Several embolic agents have been used to arrest lower gastrointestinal bleeding. Most investigators have used gel foam, polyvinyl alcohol particles, microcoils, or some combination of these. One European group reported using Ethibloc, but this agent was associated with a relatively high rate of ischemic complications and is currently considered inappropriate for bowel embolization [21].

Gel foam is a sterile gelatin sponge that may be applied to bleeding surfaces to aid in hemostasis. It is insoluble in water, porous, and malleable. It is generally considered a temporary embolic and allows vessel recanalization in several days to several weeks. Polyvinyl alcohol is a permanent embolic agent that incites an intraluminal thrombosis with an associated inflammatory reaction. It is supplied in a small vial and has a gross appearance similar to sand. Polyvinyl alcohol particles are supplied in different sizes from smaller than 100 μm to 710 μm in diameter. Microcoils are made of platinum and, when deployed, function in a similar manner to a surgical ligation. They are biocompatible but highly thrombogenic due to the addition of synthetic fibers attached to the coil. Of the three embolic agents, I favor microcoils for treating colonic hemorrhage simply because they are easy to visualize with fluoroscopy and deploy accurately. Polyvinyl alcohol particles have been used by some researchers and may have advantages, particularly for embolization of tumors, because the agent will flow to the bleeding site and occlude numerous vessels from a single injection. However, the particles cannot be directly visualized, cannot be precisely deposited (particularly if the terminal artery cannot be catheterized), and are less forgiving than microcoils if nontarget embolization occurs.

Published experience

In 1992, Guy and associates [22] reported 10 superselective embolization procedures in nine patients. All procedures were successful, and there were no cases of intestinal infarction induced by the procedure. Five years later, Gordon and colleagues [23] reported 17 cases of microcatheter embolization using microcoils, gel foam, and polyvinyl alcohol particles. Bleeding was stopped in 13 of 14 patients (93%) in whom embolization was possible and in 13 of 17 patients (76%) where there was an intention to treat. No clinically apparent bowel infarctions developed. In the ensuing 5 years, more than 100 successful cases of lower gastrointestinal embolization have been reported [22,23,24,25,26,27,28,29,30,31,32]. In these series, clinical success ranged from 44% to 91% and major ischemic complications ranged from 0% to 6%. The two largest series, by Funaki et al. [29] and Bandi et al. [30], included 27 and 48 patients, respectively. Enthusiasm for this technique continues to grow due to its inherent advantages as compared with vasopressin infusion. With embolization, bleeding is stopped at the time of the procedure without a prolonged infusion or repeat angiography. Systemic side effects of vasopressin are also avoided.

Mechanism of embolization

Ideally, embolization decreases perfusion pressure enough to arrest hemorrhage but not to the extent of total devascularization. Due to the limited collateral blood flow in the colon, overly aggressive embolization must be avoided. The mechanism of embolization depends on the embolic agent used. Microcoils decrease perfusion pressure and induce local vasospasm. This enables the patient to more effectively form clot, leading to hemostasis. Superselective embolization limits the segment of bowel at risk for ischemia. In some patients, asymptomatic submucosal ischemia develops but typically resolves over a short time [33]. Late ischemic complications such as bowel stricture [34] have been reported but appear to be quite sporadic. In our own experience, only one of 25 patients developed a stricture 1 year after embolization, and it was asymptomatic, requiring no treatment [29]

Limitations of embolization

Colonic bleeding is multifactorial. For this reason, it is likely that different disorders will vary in responsiveness to embolization. In our hospital, diverticular hemorrhage is the most common etiology of bleeding and the disorder most effectively treated by embolization [29]. Most cases of bleeding can be arrested quite easily, and we have not encountered any ischemic complications. Angiodysplasia is more difficult to treat with embolization. Peck and associates [24] noted rebleeding in 75% (three of four) cecal embolizations and attributed this observation to the preponderance of angiodysplasia in the cecum. In our experience, early rebleeding occurred in 17% (one of six) angiodysplastic lesions versus 5% (one of 19) bleeding diverticula [29].

The most important limitation of endovascular therapy is the inability to diagnose and treat patients who are not actively bleeding. It is also important to recognize that embolization is merely treating a symptom of the underlying disorder rather than the disease process itself. Thus patients with multifocal disease are at risk for repeated hemorrhage from other affected sites. Other limitations include inability to perform superselective catheterization in patients with difficult vascular anatomy or severe atherosclerotic disease.

Summary

The diagnosis and management of lower gastrointestinal hemorrhage continue to evolve and remain challenging. Minimally invasive techniques have replaced surgical resection as the initial therapies of choice. Superselective embolization and endoscopic treatment appear complementary; the strengths of one coincide with the weaknesses of the other. In general, less severe bleeding is best suited for colonoscopy, whereas more severe bleeding should be managed with embolization. Superselective embolization has been established as safe and effective and has been adopted by many interventional radiologists as the endovascular therapy of choice.

Figure 1
figure 1

Image shows 3-F microcatheter with 0.018-in. guidewire inserted coaxially through a conventional 5-F catheter.

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Figure 2
figure 2

Microcoil embolization of a marginal artery in a patient with left colonic hemorrhage. A Nuclear scintigraphy shows active bleeding from the left colon. B Superior mesenteric arteriogram shows bleeding from the distal left colon. C Angiogram of a marginal artery through a microcatheter shows focus of bleeding. D Fluoroscopic image shows microcoil embolization of a marginal artery adjacent to a bleeding site. E Follow-up angiogram shows no further bleeding, and blood flow is maintained to the colon proximal and distal to the embolized segment. F CT 6 months after embolization demonstrates coils in the marginal artery.

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Figure 3
figure 3

Microcoil embolization of distal small bowel hemorrhage. A Superior mesenteric arteriogram shows bleeding from the pelvic small bowel. B Arteriogram demonstrates cessation of hemorrhage after embolization.

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