eMedicine Specialties > Radiology > Gastrointestinal

Colitis, Ischemic

Ali Nawaz Khan, MBBS, FRCS, FRCP, FRCR, Consultant Radiologist and Honorary Professor, North Manchester General Hospital Pennine Acute NHS Trust, UK
Sumaira MacDonald, MBChB, PhD, MRCP, FRCR, Lecturer, Sheffield University Medical School; Endovascular Fellow, Sheffield Vascular Institute; Muthusamy Chandramohan, MBBS, DMRD, FRCR, Consultant Radiologist, Bradford Teaching Hospitals, UK; Claire Barker, MB, ChB, FRCR, Consultant Radiologist, Christie Hospital, NHS Trust, UK

Updated: Sep 1, 2009

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

For excellent patient education resources, visit eMedicine's Esophagus, Stomach, and Intestine Center and Procedures Center. Also, see eMedicine's patient education articles Colitis, Colonoscopy, and Gastrointestinal Endoscopy.

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.^12,13,14 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.^15,16

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.¹⁷

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.¹⁸

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.¹⁹

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.²⁰

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.²¹

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

Arterial blood supply to the large bowel shows the potential site of ischemia.

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.²² 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.²³

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.²⁴ Barium enema results are abnormal in 90% of patients with ischemic colitis.^{10,23,24,25,26}

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.^{27,28,29,30,31,32,33}

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

Radiography

Findings

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.

Left: Plain abdominal radiograph in a 58-year-old man who underwent an upper GI barium study for nonspecific dyspepsia a few days earlier. The patient presented with vague abdominal discomfort and the passage of blood per rectum. Note the thumbprinting in the region of the distal transverse colon and splenic flexure. Right: Another radiograph obtained 24 hours later shows mild dilatation of the distal transverse colon with more obvious mucosal edema.

Six days later, the clinical condition of the patient seen in Image above deteriorated, with increasing abdominal pain and signs of peritonism. Note the bowel relief sign. At surgery, a perforated ischemic bowel segment at the splenic flexure was confirmed.

Left: Chest radiograph of a 45-year-old woman with mitral valve disease and atrial fibrillation who presented with acute abdominal symptoms. Note the cardiomegaly and blood diversion in the upper lobe, which is suggestive of cardiac decompensation. Right: Plain radiograph shows several dilated loops of the jejunum. Note also the stricture of the proximal transverse colon. At surgery, a gangrenous small bowel loop secondary to a mesenteric artery embolus was resected. The patient had a similar episode a year earlier, which was managed conservatively; this approach accounts for the ischemic stricture of the proximal transverse colon.

Plain supine abdominal radiograph in a 72-year-old man who presented with bloody diarrhea. Note the thumbprinting of the splenic flexure and the entire descending colon.

Postoperative abdominal radiograph in a 26-year-old patient who had stabbed himself, cutting across the jejunum. The injury was repaired on an emergency basis. After laparotomy, his recovery was slow, and he had bloody diarrhea. Colonoscopy revealed a hemorrhagic edematous mucosa of the splenic flexure suggestive of ischemic colitis. Note the thumbprinting of the distal transverse colon. See also Image 16 in Multimedia.

• Dilatation of a part of the colon may be seen early. The appearance may be not unlike that of ulcerative colitis with mucosal edema (thumbprinting) and pseudopolyp formation (see Images above and Images 5-10, 13-15 in Multimedia).
• When both the small bowel and the large bowel are affected by ischemic injury, the small bowel may also become dilated with thickening of the valvulae conniventes.
• Over time, the haustra become thickened and edematous, and it contains a large amount of secretions.
• With further edema, the haustral markings disappear completely, and the colon acquires a hoselike appearance.
• Localized pneumatosis coli may be apparent.
• Eventual tubular narrowing and stricturing appear over a long segment.

Findings on barium enema examination may include the following:

• A rapid sequence of events usually occurs over several weeks after an initial ischemic insult. The events can progress from the early stages of spasm and edema to chronic stricture formation.
• Barium enema examination during the acute stage of a vascular insult demonstrates spasm associated with thickening and blunting of the mucosal folds. Multiple mucosal scalloping or thumbprinting are seen along the contours of the bowel. Seen en face, the thumbprints appear as polypoid filling defects (see Images below and Images 2-4 in Multimedia).

Double-contrast barium enema study shows a stricture of the proximal descending colon secondary to ischemia.

Erect radiograph obtained after a double-contrast barium enema study shows a stricture at the splenic flexure.

Postevacuation image obtained after a barium enema study shows extensive thumbprinting involving the entire colon, secondary to mesenteric ischemia.

• With further progression of mucosal edema, the folds become thickened and ill defined.
• Intraluminal secretions are increased.
• Ulcerations are frequently observed in pathologic specimens of the diseased bowel segment. However, these may not be deep enough to be demonstrable radiologically. With diffuse ulceration, the mucosa may be completely effaced. Ulcers may be seen as a serrated mucosa. Deep ulcers are a late finding.
• During the healing phase, when fibrosis sets in, associated flattening and rigidity of 1 wall may be observed. The antimesenteric border of the colon becomes pleated because of scarring; this may appear as sacculations or pseudodiverticula.
• With a continuing fibrotic process, the affected segment of the large bowel acquires a tubular shape with smooth contours and a concentric lumen.
• The final outcome is usually a long stricture with proximal bowel dilatation. However, when a stricture develops, it is shorter than the original length of the ischemic bowel, as seen radiologically.
• In the stages before fibrosis develops, partial or complete recovery may occur. The ischemic process may be arrested at any of the previously described stages.

Degree of Confidence

The plain radiographic findings may be entirely normal, particularly early in the disease. However, the results of barium enema are abnormal in 90% of patients with ischemic colitis.

False Positives/Negatives

Inflammatory bowel disease, infective colitides, and carcinoma may mimic ischemic colitis. The stricture formation in ischemic colonic disease is smooth and tapering, with a concentric lumen and without shouldering or contour defects. Sacculations are common in ischemic colitis, but skip lesions are rare. In inflammatory bowel disease, cobblestoning, skip lesions, and small punched-out ulcers are common features. In colonic carcinoma, the narrowing is eccentric and associated with shouldering. In the early stages, contour defects may be observed.

In some cases of ischemic colitis, extensive mucosal ulceration may simulate a lymphosarcoma on a barium enema study.

Computed Tomography

Findings

Axial contrast-enhanced CT scans of the same patient as in Image 15 in Multimedia shows that the superior mesenteric vein is larger than the aorta. Lower CT section (left) shows a fistula between the superior mesenteric artery and the vein through a pseudoaneurysm, which was the cause of global mesenteric ischemia due to a steal phenomenon. After surgical repair of the arteriovenous communication, the patient fully recovered.

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.

Series of enhanced CT scans (see Images 17-32 in Multimedia) in the same patient.

Series of enhanced CT scans (see Images 17-32 in Multimedia) in the same patient.

Series of enhanced CT scans (see Images 17-32 in Multimedia) in the same patient.

The specific CT signs for establishing the diagnosis of bowel ischemia depend on the degree of ischemia, the length of bowel loops involved, and whether both the large bowel and small bowel are affected. Findings may include the following:

• Thromboembolism in the mesenteric vessels
• Intramural or portal venous gas
• Segmental thickening of the bowel wall
• Absence of bowel wall enhancement with contrast-enhanced CT
• Irregular narrowing of the bowel lumen as a result of mucosal edema (thumbprinting)
• Possible bowel dilatation proximal to the ischemic segment of the bowel
• Nonspecific signs of bowel ischemia, including bowel obstruction, mesenteric edema, mesenteric vascular engagement, and ascites

Degree of Confidence

CT is regarded as a valuable noninvasive tool in the diagnosis of mesenteric ischemia. Conflicting reports have appeared in the radiology literature regarding the sensitivity of CT in the diagnosis of mesenteric ischemia. Earlier reports showed a poor sensitivity of around 39%. However, more recent reports involving high-quality infusion techniques resulted in a higher sensitivity of 64-82%. This improved sensitivity is partly related to improved detection rates of more specific signs, such as direct visualization of thromboembolism in the mesenteric vessels and the lack of visualization of bowel-wall enhancement.

False Positives/Negatives

High-quality images are usually difficult to acquire because of the poor general condition of these patients. CT appears to be significantly limited in detecting small peripheral mesenteric emboli. Some of the well-known CT features of mesenteric ischemia, such as diffuse bowel dilatation, bowel wall thickening, ascites, mesenteric haziness, and vascular engorgement, are elicited in only 36% of the patients. Some of the CT findings are nonspecific and may be found in inflammatory bowel disease.

Magnetic Resonance Imaging

Findings

Ha et al showed that the sensitivity of MRI in the detection of bowel ischemia is comparable to that of CT.³¹ MRI may be useful in depicting bowel-wall changes and in demonstrating mesenteric vascular abnormalities. As with CT, the additional use of contrast enhancement allows an assessment of the dynamic changes in the bowel wall.³²

Degree of Confidence

MRI is as sensitive as CT in the diagnosis of bowel wall ischemia, and it has the added advantage of not using ionizing radiation. Some researchers have attempted cine phase-contrast MRI for the quantitation of mesenteric blood flow.³³ They measured blood flow in the SMA 30 minutes after the patient ate a meal and found promising criteria for differentiating healthy patients from those with chronic intestinal ischemia.

False Positives/Negatives

MRI has significant problems in depicting small thromboembolism in small mesenteric vessels.

Ultrasonography

Findings

Bowel gas frequently prevents the visualization of colonic changes, which are usually most marked around the splenic flexure. In the initial stages, the ischemic bowel may show increased peristalsis, which is then reduced. The bowel wall becomes thickened, and nodular and intramural hemorrhage and edema give rise to areas of reduced echogenicity. Echogenic areas may be seen in the bowel wall; these may reflect either areas of infarction infiltrate or clot. Echogenic areas with shadowing occur as a result of intramural gas. Gas may also be detected in the portal vein; this is a poor prognostic sign.

Doppler color flow imaging is performed after the patient fasts overnight to minimize bowel gas. The patient is usually scanned in a supine position with the head slightly elevated to allow the abdominal viscera to descend. To identify the celiac axis and the SMA, the aorta is scanned in the sagittal left paramedian plane, starting at the xiphisternum. The SMA is 1-2 cm distal to the celiac axis; however, the 2 may have a common origin.

Before Doppler studies of the SMA and celiac axis are performed, a Doppler velocity signal in the aorta is obtained at the level of the celiac axis and the SMA at a 60° angle. The aorta is scanned for atheroma, dissection, and aneurysm. Color flow and spectral analysis are used to detect flow disturbances. The peak systolic aortic velocity is recorded, after which velocity measurements are made at the origins of the celiac axis and the SMA.

Care should be taken when recording Doppler time-velocity waveforms at the origins of the celiac axis and the SMA because the insonation angle may be inadvertently increased beyond 60°. Both the celiac axis and the SMA should be examined during both inspiration and expiration to distinguish extrinsic disease (eg, compression of median arcuate ligament of the diaphragm on the celiac axis) from intrinsic disease (atheroma).^36,37

Evaluation of the celiac axis

Color flow Doppler sonography is effective in demonstrating flow disturbances associated with tortuosity and stenosis at the origin of the celiac axis. Doppler spectral waveforms in a normal celiac axis after fasting demonstrate a forward flow with an average peak systolic velocity of 123 cm/s ± 9 in persons aged 48-79 years. A significant increase in the systolic or diastolic flow velocity occurs after a meal.

This increase is also reflected in the hepatic and splenic arteries. The average postprandial systolic velocity 30 minutes after a meal of 355 K cal is 132 cm/s ± 7. In the presence of a 60% stenosis of the celiac axis, the peak velocity is increased to 167-208 cm/s ± 9. With this degree of stenosis, color Doppler imaging demonstrates a high-velocity jet at the stenotic site associated with poststenotic turbulent flow.

The potential for collateralization between the celiac axis, SMA, and IMA is remarkable. As a result, the peak systolic velocity in the celiac axis may be lower or much higher than expected when concomitant SMA occlusion is present. This variation may result in the overestimation or underestimation of the extent of ischemic disease.

Evaluation of the SMA

After fasting, the SMA has low diastolic flow. However, after a meal, both the peak systolic and end-diastolic velocities are significantly increased if arterial stenosis is absent. The normal fasting SMA velocities are 128 cm/s ± 16 in persons aged 23-42 years. After a meal, the peak systolic velocity increases to 162 cm/s ± 11; the end-diastolic velocity is in the range of 48 cm/s ± 7 within 15 minutes after the meal. The peak systolic velocity almost doubles within 45 minutes after a meal. With significant SMA stenosis, the peak systolic velocity exceeds 270 cm/s, with a concomitant increase in diastolic flow.

Color flow Doppler imaging shows a jet through the stenotic segment with turbulent flow downstream, which continues for some distance.

Degree of Confidence

Ultrasonography is a sensitive yet noninvasive technique that may provide useful information about mesenteric ischemia. Images may demonstrate absent or barely visible color flow, absent arterial signals, and thickened bowel-wall loops. Doppler techniques are particularly useful for investigating chronic mesenteric ischemia.

False Positives/Negatives

Limitations of Doppler analysis of celiac artery and SMA ischemia include the following: (1) there is great potential for collateralization in the splanchnic vessels, which may make an assessment of a single-vessel stenosis difficult; (2) the risk of error increases when the angle of insonation is greater than 60°; and (3) careful placement of the sample volume is crucial. The SMA must be examined throughout the visualized vessel; otherwise, a false-negative diagnosis may result.

Gas-filled dilated bowel in ileus or small bowel obstruction may prevent adequate visualization of the vasculature.

Nuclear Imaging

Findings

Stathaki et al evaluated the use of pentavalent techenetium-99m dimercaptosuccinic acid [Tc-99m (V) DMSA] in the diagnosis of ischemic colitis in 14 patients with endoscopically and histologically confirmed ischemic colitis. Tc-99m (V) DMSA scintigraphy was performed within 2 days after colonoscopy, and images were considered positive when an area of increased activity was observed in the region of interest and considered negative when no abnormal tracer uptake was detected. In 3 of the 14 patients, Tc-99m (V) DMSA images showed moderate activity in the bowel. In the other 11 patients, no abnormal tracer uptake was detected in the abdomen and, therefore, the use of Tc-99m (V) DMSA could not be considered successful in the diagnosis of ischemic colitis.¹¹

Angiography

Findings

Digital subtracted superior mesenteric angiogram in a 63-year-old woman known to have a hilar cholangiocarcinoma (note the biliary stent) who presented with a sudden onset of abdominal pain and distension. This frame from the angiogram shows a sharp cut-off of the superior mesenteric artery secondary to an acute thrombosis. This patient underwent thrombolysis, with a satisfactory outcome.

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.

Normal inferior mesenteric angiogram in a 53-year-old man.

Normal venous phase of an inferior mesenteric angiogram (same patient as in Image 11 in Multimedia).

In cases of superior or inferior mesenteric vein thrombosis, the veins may not be visualized, and collateral venous filling may be depicted. Superior or inferior mesenteric arteriovenous fistulas are readily identified with angiography. A vascular steal syndrome is usually diagnosed by means of inferior mesenteric angiography.

Degree of Confidence

Angiography has a limited role in the diagnosis of colonic ischemia; however, for a few specific indications, angiography may be invaluable (see Findings above).

False Positives/Negatives

In established colonic ischemia, no angiographic changes may be observed, or the angiographic changes may be indistinguishable from those of inflammatory bowel disease. Also, the severity of the ischemic insult and the angiographic changes appear to be poorly correlated.

Intervention

Medicolegal Pitfalls

• Ischemic colitis sometimes develops proximal to a colonic carcinoma as a result of large-bowel obstruction. It is therefore essential to rule out colonic carcinoma in the appropriate clinical setting.
• Among young adults, ischemic colitis has strong preponderance in females taking oral contraceptives. Physicians treating hemorrhagic colitis in young pregnant women or those taking oral contraceptives should consider the possibility of ischemic colitis.
• Sickle cell disease is a rare cause of ischemic colitis. It should be considered in patients with crises of abdominal sickle cell veno-occlusive pain. If not recognized, the condition can be fatal.
• Ischemic colitis caused by mesenteric hematoma as a complication of endoscopic retrograde cholangiopancreatography has been reported. Prompt evaluation and awareness of potential complications should help capture potentially life-threatening sequelae of endoscopic retrograde cholangiopancreatography.

Multimedia

Media file 1: Arterial blood supply to the large bowel shows the potential site of ischemia.

Media file 2: Double-contrast barium enema study shows a stricture of the proximal descending colon secondary to ischemia.

Media file 3: Erect radiograph obtained after a double-contrast barium enema study shows a stricture at the splenic flexure.

Media file 4: Postevacuation image obtained after a barium enema study shows extensive thumbprinting involving the entire colon, secondary to mesenteric ischemia.

Media file 5: 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.

Media file 6: Left: Plain abdominal radiograph in a 58-year-old man who underwent an upper GI barium study for nonspecific dyspepsia a few days earlier. The patient presented with vague abdominal discomfort and the passage of blood per rectum. Note the thumbprinting in the region of the distal transverse colon and splenic flexure. Right: Another radiograph obtained 24 hours later shows mild dilatation of the distal transverse colon with more obvious mucosal edema.

Media file 7: Six days later, the clinical condition of the patient seen in Image above deteriorated, with increasing abdominal pain and signs of peritonism. Note the bowel relief sign. At surgery, a perforated ischemic bowel segment at the splenic flexure was confirmed.

Media file 8: Left: Chest radiograph of a 45-year-old woman with mitral valve disease and atrial fibrillation who presented with acute abdominal symptoms. Note the cardiomegaly and blood diversion in the upper lobe, which is suggestive of cardiac decompensation. Right: Plain radiograph shows several dilated loops of the jejunum. Note also the stricture of the proximal transverse colon. At surgery, a gangrenous small bowel loop secondary to a mesenteric artery embolus was resected. The patient had a similar episode a year earlier, which was managed conservatively; this approach accounts for the ischemic stricture of the proximal transverse colon.

Media file 9: Digital subtracted superior mesenteric angiogram in a 63-year-old woman known to have a hilar cholangiocarcinoma (note the biliary stent) who presented with a sudden onset of abdominal pain and distension. This frame from the angiogram shows a sharp cut-off of the superior mesenteric artery secondary to an acute thrombosis. This patient underwent thrombolysis, with a satisfactory outcome.

Media file 10: 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.

Media file 11: Normal inferior mesenteric angiogram in a 53-year-old man.

Media file 12: Normal venous phase of an inferior mesenteric angiogram (same patient as in Image 11 in Multimedia).

Media file 13: Plain supine abdominal radiograph in a 72-year-old man who presented with bloody diarrhea. Note the thumbprinting of the splenic flexure and the entire descending colon.

Media file 14: Inferior mesenteric angiogram in the same patient as in Image 13 shows a stenosis of more than 50% at the origin of the left colic artery associated with a poststenotic dilatation. Image on the right is a manual subtraction image.

Media file 15: Postoperative abdominal radiograph in a 26-year-old patient who had stabbed himself, cutting across the jejunum. The injury was repaired on an emergency basis. After laparotomy, his recovery was slow, and he had bloody diarrhea. Colonoscopy revealed a hemorrhagic edematous mucosa of the splenic flexure suggestive of ischemic colitis. Note the thumbprinting of the distal transverse colon. See also Image 16 in Multimedia.

Media file 16: Axial contrast-enhanced CT scans of the same patient as in Image 15 in Multimedia shows that the superior mesenteric vein is larger than the aorta. Lower CT section (left) shows a fistula between the superior mesenteric artery and the vein through a pseudoaneurysm, which was the cause of global mesenteric ischemia due to a steal phenomenon. After surgical repair of the arteriovenous communication, the patient fully recovered.

Media file 17: 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.

Media file 18: Series of enhanced CT scans (see Images 17-32 in Multimedia) in the same patient.

Media file 19: Series of enhanced CT scans (see Images 17-32 in Multimedia) in the same patient.

Media file 20: Series of enhanced CT scans (Images 17-32) in the same patient.

Media file 21: Series of enhanced CT scans (Images 17-32) in the same patient.

Media file 22: Series of enhanced CT scans (Images 17-32) in the same patient.

Media file 23: Series of enhanced CT scans (Images 17-32) in the same patient.

Media file 24: Series of enhanced CT scans (Images 17-32) in the same patient.

Media file 25: Series of enhanced CT scans (Images 17-32) in the same patient.

Media file 26: Series of enhanced CT scans (Images 17-32) in the same patient.

Media file 27: Series of enhanced CT scans (Images 17-32) in the same patient.

Media file 28: Series of enhanced CT scans (Images 17-32) in the same patient.

Media file 29: Series of enhanced CT scans (Images 17-32) in the same patient.

Media file 30: Series of enhanced CT scans (Images 17-32) in the same patient.

Media file 31: Series of enhanced CT scans (Images 17-32) in the same patient.

Media file 32: Series of enhanced CT scans (see Images 17-32 in Multimedia) in the same patient.

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Keywords

colitis, ischemic colitis, reversible vascular occlusion of the colon, mesenteric ischemia, intestinal necrosis, mesenteric thrombosis, mesenteric infarction, transmural infarction, mucosal infarction, mural infarction

Contributor Information and Disclosures

Author

Ali Nawaz Khan, MBBS, FRCS, FRCP, FRCR, Consultant Radiologist and Honorary Professor, North Manchester General Hospital Pennine Acute NHS Trust, UK
Ali Nawaz Khan, MBBS, FRCS, FRCP, FRCR is a member of the following medical societies: American Association for the Advancement of Science, American Institute of Ultrasound in Medicine, British Medical Association, British Society of Interventional Radiology, Royal College of Physicians, Royal College of Physicians and Surgeons of the United States, Royal College of Radiologists, and Royal College of Surgeons of England
Disclosure: Nothing to disclose.

Coauthor(s)

Sumaira MacDonald, MBChB, PhD, MRCP, FRCR, Lecturer, Sheffield University Medical School; Endovascular Fellow, Sheffield Vascular Institute
Sumaira MacDonald, MBChB, PhD, MRCP, FRCR is a member of the following medical societies: British Medical Association, Royal College of Physicians, and Royal College of Radiologists
Disclosure: Nothing to disclose.

Muthusamy Chandramohan, MBBS, DMRD, FRCR, Consultant Radiologist, Bradford Teaching Hospitals, UK
Disclosure: Nothing to disclose.

Claire Barker, MB, ChB, FRCR, Consultant Radiologist, Christie Hospital, NHS Trust, UK
Claire Barker, MB, ChB, FRCR is a member of the following medical societies: Royal College of Radiologists
Disclosure: Nothing to disclose.

Medical Editor

Neela Lamki, MD, Professor, Department of Radiology, Sultan Qaboos University, Oman; Adjunct Professor, Department of Radiology, Baylor College of Medicine
Disclosure: Nothing to disclose.

Pharmacy Editor

Bernard D Coombs, MB, ChB, PhD, Consulting Staff, Department of Specialist Rehabilitation Services, Hutt Valley District Health Board, New Zealand
Disclosure: Nothing to disclose.

Managing Editor

Spencer B Gay, MD, Professor of Radiology, Director of Body Computed Tomography, Department of Radiology, University of Virginia Health Sciences Center
Disclosure: Nothing to disclose.

CME Editor

Robert M Krasny, MD, Resolution Imaging Medical Corporation
Robert M Krasny, MD is a member of the following medical societies: American Roentgen Ray Society and Radiological Society of North America
Disclosure: Nothing to disclose.

Chief Editor

Eugene C Lin, MD, Consulting Radiologist, Virginia Mason Medical Center; Clinical Assistant Professor of Radiology, University of Washington School of Medicine
Eugene C Lin, MD is a member of the following medical societies: American College of Nuclear Medicine, American College of Radiology, Radiological Society of North America, and Society of Nuclear Medicine
Disclosure: Nothing to disclose.

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