Introduction
Background
Marston et al introduced the term ischemic colitis in their article published in 1966.1 This report was preceded by the description of reversible colonic vascular occlusion by Boley and colleagues in 1963.2 Ischemic colitis encompasses a number of clinical entities, all with an end result of insufficient blood supply to a segment or the entire colon. This disease results in ischemic necrosis of varying severities that can range from superficial mucosal involvement to full-thickness transmural necrosis.3
Bowel ischemia is mainly a disease of old age caused by atheroma of mesenteric vessels. Other causes include embolic disease, vasculitis, fibromuscular hyperplasia, aortic aneurysm, blunt abdominal trauma, disseminated intravascular coagulation, irradiation, and hypovolemic or endotoxic shock.4
Occlusive mesenteric infarction (embolus or thrombosis) has a 90% mortality rate, whereas nonocclusive disease has a 10% mortality rate.
Venous infarction occurs in young patients, usually after abdominal surgery.5 Patients may present with colicky abdominal pain, which becomes continuous. It may be associated with vomiting, diarrhea, or rectal bleeding.6,7,8,9
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Double-contrast barium enema study shows a stricture of the proximal descending colon secondary to ischemia.
Plain abdominal radiograph in a 65-year-old man presenting with acute abdominal pain and the passage of blood per rectum. Note the thumbprinting in the region of the splenic flexure and also the proximal small-bowel dilatation.
This 63-year-old man had smoked more than 30 cigarettes a day for over 40 years and gave a 3-year history of claudication. Recently, he presented with the passage of mucus and blood per rectum. Flexible sigmoidoscopy revealed a hemorrhagic edematous mucosa with superficial ulceration at the rectosigmoid junction suggestive of ischemic colitis. A flush aortogram showed only the origin of the superior mesenteric artery, but the celiac artery and the inferior artery origins were not identified. A selective superior mesenteric artery angiogram shows retrograde filling of the celiac axis and antegrade filling of the inferior mesenteric artery. Note the arch of Riolan. The image on the right is a manual subtraction image of the angiogram on the left.
Series of contrast-enhanced CT scans (see Images 17-32 in Multimedia) on a 72-year-old man presenting with acute abdominal pain. Surgery revealed mesenteric ischemia, mainly in the right and transverse colon, secondary to peripheral mesenteric thrombosis (arrow). Note the colonic edema akin to thumb printing on plain abdominal radiographs. Multiple hypoattenuating masses in the liver were due to liver abscesses. Moderate ascites is present.
Pathophysiology
The small bowel alone, the colon alone, or occasionally both may sustain a hypoxic injury from a variety of causes.10,11,12 Collectively, all these gut hypoxic injuries are designated by the term mesenteric ischemias. Ischemic colitis can be classed as an inflammatory disease of the colon caused by diminished blood flow that leads to bowel wall ischemia and a secondary inflammation.
Most of the classifications of intestinal ischemia in the literature are based on the major causative factors. Two mechanisms may cause bowel ischemia: The first and most common is diminished bowel perfusion resulting from low cardiac output; it is often seen in patients with cardiac disease or in patients with prolonged shock of any etiology. The second mechanism is occlusive disease of the vascular supply of bowel resulting from atheroma, thrombosis, or embolism in which the collateral circulation is not adequate to maintain bowel integrity.
Regardless of the mechanism, the disease follows the same course. Depending on the cause and severity of the impairment of the bowel blood supply, the morphologic pattern can be arbitrarily subdivided into 3 groups: (1) transmural infarction, (2) mural infarction in which the injury extends from the mucosa into the muscularis, and (3) mucosal infarction in which ischemic damage is confined to the mucosa.13,14
Causes of mesenteric ischemia
Causes of mesenteric ischemia include the following:
- Hypoperfusion: This may involve heart failure or prolonged shock of any etiology.
- Embolic occlusion
- Atherosclerosis
- Arterial thrombosis
- Venous thrombosis
- Vasculitis
- Large-vessel vasculitis includes Takayasu arteritis and giant cell arteritis.
- Medium-vessel vasculitis includes polyarteritis nodosa and Kawasaki syndrome.
- Small-vessel vasculitis includes microscopic polyangiitis, Wegener granulomatosis, Churg-Strauss syndrome, Henoch-Schönlein syndrome, systemic lupus erythematosus, rheumatoid vasculitis, and Behçet disease.
- Thromboangiitis obliterans
- Disseminated intravascular coagulation
- Hypercoagulable states
- Sickle cell disease
- Aortic dissection
- Aortoiliac surgery ischemia: This can develop if the inferior mesenteric artery (IMA) is sacrificed during an abdominal aortic surgery dissection.
- IMA sacrifice: This artery may be sacrificed during colonic resection, although most patients tolerate ligation of the IMA because the collateral circulation is adequate.
- Translumbar aortography
- Cardiac surgery
- Ischemic colitis in association with pheochromocytoma; this occurs from intense splanchnic vasoconstriction.
- Liver transplantation
- Bowel obstruction, particularly from an incarcerated hernia or volvulus
- Colonic carcinoma
- Trauma
- Drugs: Vasoconstrictors (eg, digitalis), norepinephrine, pseudoephedrine, ergot alkaloids, oral contraceptives, estrogens, various diuretics, antihypertensive medications, nonsteroidal anti-inflammatory drugs, chemotherapeutic agents, alosetron, paclitaxel, meloxicam, cocaine, and amphetamine abuse may be involved.
- Corrosive injury: This usually affects the proximal gut, but in rare cases, it may cause penetration injury to the transverse colon.
- Bowel infections, necrotizing enteritis
- Radiation injury
- Large-bowel ischemia: In rare cases, this may result from vascular steal syndrome. An example is occlusion of the femoral or iliac artery. The involved lower extremity is supplied by a hypertrophied IMA and hemorrhoidal arteries, with reversed flow in the internal iliac artery.
- Arteriovenous fistula between the mesenteric artery and veins: This is an unusual cause of mesenteric ischemia. Patients with this condition also have portal hypertension.
- Idiopathic
Transmural infarction
Transmural infarction is more common in the small bowel because it is entirely dependent on the mesenteric blood supply, whereas the large bowel is near the posterior abdominal wall, from where it may acquire a collateral blood supply and venous drainage. Transmural infarction usually involves a long segment of bowel, although in rare cases, skip lesions occur. Transmural infarction is usually the result of thrombosis or embolism of the superior mesenteric artery (SMA), which may affect only the small bowel (approximately one half of the mesenteric ischemias). Mesenteric venous thrombosis is another cause; this may involve both the small bowel and the large bowel. Transmural infarction of the small bowel usually involves long segments, but in rare cases, small segments may be involved.
Colonic infarction tends to occur in 2 watershed territories: (1) the splenic flexure, which is the watershed territory between the SMA and IMA blood supply, and (2) the distal sigmoid colon, which forms the watershed area between the IMA and hypogastric artery supply.
Regardless of whether the ischemia is the result of arterial or venous occlusion, the infarcted bowel always appears hemorrhagic. Early in the course of disease, the bowel appears intensely congested and dusky or purplish red in color, with foci of subserosal and submucosal ecchymoses. As the disease progresses, the bowel wall appears edematous, thickened, rubbery, and hemorrhagic. The lumen of the bowel may contain mucus or frank blood. Arterial occlusion usually results in a sharply defined border between the infarcted bowel and the normal vascularized bowel, whereas in venous thrombosis, the boundary between infarcted bowel is ill defined with no clear demarcation between viable and nonviable bowel.
Microscopy reveals suffusion of the bowel wall, which tends to mask the underlying ischemic necrosis. Later in the course of disease, inflammatory infiltration of the bowel wall and ulceration ensue. Bacterial contamination is often present, and bowel perforation may occur within 3-4 days. Arterial occlusion may be difficult to demonstrate histologically, particularly if ischemia is the result of spasm or a low-perfusion state superimposed on atheromatous disease.
Mucosal and mural infarction
Mucosal and mural infarction is an ischemic injury that is confined to the inner layers of the bowel wall. It is usually the result of hypoperfusion rather than occlusive disease. The hypoxic injury may extend deeply, but the serosa is usually spared. Shock and cardiac failure are major causative factors. Many patients with this condition have also received vasoconstrictor drugs such as digitalis or norepinephrine.
This type of injury may involve any part of the gut and is usually patchy and segmental, unlike transmural infarction, which involves long segments. In some cases, minute intramural thrombi are found; whether these are the cause or effect of the ischemic injury is not clear. The involved bowel loops may appear dark red or purple as a result of luminal hemorrhage, but serosal hemorrhage, necrosis, or inflammatory exudate is absent. The mucosa appears hemorrhagic, edematous, and thickened, with superficial ulceration.
Histologic analysis may show vascular dilatation associated with a few extravasated red cells and hemorrhagic necrosis within the superficial layers of the mucosa. However, this necrosis may extend into submucosa and the superficial layers of the muscularis. In the colon, bacterial contamination may produce superimposed pseudomembranous inflammation. The combination of necrosis and bacterial invasion develops when the mucosal barrier becomes defective. Thus, the morphologic changes seen in ischemic colitis may resemble those of pseudomembranous colitides or other inflammatory and/or infective processes.
Frequency
United States
No reliable demographic data describe the incidence of ischemic colitis in the United States. The incidence is thought to be underestimated because many mild cases may go unreported. In contrast, the incidence in patients undergoing abdominal aortic reconstructive procedures has been studied. Hunter and Guernsey reported that as many as 10% of such patients have some degree of ischemic colitis.15
With our aging population, the incidence of ischemic colitis is expected to increase. Ischemic colitis is the most common type of ischemic disease affecting the gastrointestinal tract and accounts for 50% of cases.
International
No data suggest that the worldwide incidence or prevalence of ischemic colitis differ from that in the United States.
Mortality/Morbidity
Mortality and morbidity depend on the cause and comorbidities, such as underlying cardiac disease and vasculitides, among others. The prognosis for patients with colonic ischemia is more favorable than that seen with other forms of mesenteric ischemia. A transient ischemic episode resolves usually within 1-3 months without sequelae. With significant ischemic injury, long strictures may follow and cause mechanical problems such as bowel obstruction. More severe ischemic trauma may cause bowel gangrene and perforation, but this is rare.
The mortality of patients requiring surgery for ischemic colitis remains high because most patients with bowel ischemia have significant comorbidities. Earlier diagnosis and measures to reduce blood loss may contribute to improving the overall outcome.16
In a series of 150 patients with colonic ischemia, Boley et al reported that 44.7% had reversible disease, 18.7% had persistent colitis, 12.7% had ischemic stricture, and 18.7% had gangrene or perforation. In 5.3%, follow-up was insufficient.17
Patients with isolated right colon ischemia have a poorer prognosis than those with colon ischemia involving other parts of the colon; there is also a fivefold need for surgery and 2 times greater mortality.18
Race
No racial or ethnic predilection for ischemic colitis is reported.
Sex
The male-to-female ratio in ischemic colitis is approximately 1:1.
Age
Ischemic colitis is a disease of the elderly. It is rarely seen in those younger than 60 years. The average patient age at diagnosis is 70 years.19
Younger patients can develop ischemic colitis. Most published descriptions have been case reports or small case series. Etiologies have included sickle cell disease, other vasculopathies or coagulopathies, disease induced by drugs (eg, cocaine, oral contraceptives), or long-distance running.
Anatomy
The colon derives its blood supply from both the SMA and the IMA (see Image above and Image 1 in Multimedia). The ileocolic, right colic, and middle colic arteries arising from the SMA supply the ascending and transverse colon up to the splenic flexure. The middle colic artery may occasionally arise from the celiac axis in association with the dorsal pancreatic artery. Therefore, celiac-axis angiography is sometimes necessary to evaluate the colonic blood supply.
The IMA arises from the left anterior wall of the lower abdominal aorta at variable levels from the second to the fourth lumbar vertebral bodies. The size of the IMA varies greatly in an adult. The diameter of the artery varies from 1.2-5.5 mm. The same holds true for the branches of the IMA.
No relationship exists between the size of the IMA and the degree of atheromatous disease within the aorta or IMA itself. However, a rough relationship is noted between the size of the left colic artery and the length of the colonic segment it supplies: the longer the length supplied, the greater the diameter.
The IMA courses parallel to the lower abdominal aorta and gives off its first ascending branch 3-4 cm from its origin. This left colic artery may form a single trunk in 40% of patients. More commonly (60%), the first ascending branch consists of the left colic artery, but it can also give rise to sigmoid branches. The descending branch is a continuation of the IMA, which results in further branches to the sigmoid artery and which then continues as a superior hemorrhoidal artery.
The left colic and sigmoid arteries participate via a large anastomotic arcade within the mesocolon known as the marginal artery of Drummond.20 The vasa recta supplying the bowel wall arise from the marginal artery of Drummond and other anastomotic arcades within the mesocolon. The marginal artery provides a link between the branches of the SMA and IMA. In chronic ischemia, this may be in the form of a hypertrophied vessel, the so-called wandering artery of Drummond. Further collateralization between the SMA and IMA occurs through the arch of Riolan. The arcades between the SMA and IMA are commonly seen during clinical angiography because of the frequency of IMA occlusion in the elderly population.
The inferior mesenteric vein is a continuation of the superior hemorrhoidal vein. During its upward course, it receives the sigmoid and left colonic veins. The inferior mesenteric vein drains into the splenic vein behind the pancreatic tail.
Presentation
The radiologic appearances of ischemic colitis are nonspecific and may be seen in other inflammatory disorders of the colon. A reliable diagnosis of ischemic colitis can be made only when the radiologic findings are correlated with the clinical results.
With sudden thromboembolism, patients experience abdominal pain localized to the left side of the abdomen, along with tenderness and bloody diarrhea. Severe ischemia may lead to bowel necrosis and perforation that results in an acute abdomen and shock. The patient's sign and symptoms generally resolve within several days. In some cases, a bowel stricture may develop and cause bowel obstruction. Rarely, chronic rectal ischemia may occur, causing rectal pain and incontinence.21
Preferred Examination
Abdominal plain radiography is usually an initial examination undertaken in most cases involving acute abdominal problems. Although the initial radiographic findings may be normal in colonic ischemia, it is an invaluable procedure in the differential diagnosis of an acute abdomen.22 Barium enema results are abnormal in 90% of patients with ischemic colitis.
CT is the single best test after plain radiography because it can exclude many other causes of abdominal pain and can also establish the diagnosis of intestinal ischemia. MRI is mostly useful for magnetic resonance angiography, particularly in individuals with compromised renal function. Ultrasonography is a noninvasive technique that may provide useful information, particularly in investigating chronic mesenteric ischemia. It is unlikely to be conclusive in excluding mesenteric ischemia.
Angiography has a limited role in cases of colonic ischemia, but it may be invaluable in a few specific indications, such as arteriovenous fistulas and vascular steal syndrome.
Limitations of Techniques
The radiologic features of ischemic colitis are nonspecific and may be seen in other inflammatory disorders of the colon. Results with all modalities may be normal in patients with established ischemic colitis.
Differential Diagnoses
Adrenal Adenoma
Adrenal Carcinoma
Adrenal Hemorrhage
Adrenal Metastases
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References
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Further Reading
Keywords
reversible vascular occlusion of the colon, mesenteric ischemia, intestinal necrosis, mesenteric thrombosis, mesenteric infarction, transmural infarction, mucosal infarction, mural infarction










Overview: Colitis, Ischemic