Patients with mesenteric ischemia have a rare, potentially life-threatening disease and may present to the primary care or emergency medicine physician. Acute and chronic forms of mesenteric ischemia share many similarities and have many differences (see images below). This article discusses mesenteric artery ischemia in general. Acute Mesenteric Ischemia, Chronic Mesenteric Ischemia, Mesenteric Artery Thrombosis, and Mesenteric Venous Thrombosis discuss the specific types of mesenteric ischemia.
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Angiogram of a patient with chronic mesenteric ischemia.
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Radiograph showing bowel spasm, an early sign of ischemia.
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Gas in the colon wall, typical of advanced ischemia.
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Ischemia stricture.
First described by Antonio Hodgson in the latter part of the 15th century, the medical profession did not become interested in this condition until the middle of the 19th century. By the turn of this century, many review articles and texts were written describing the advances in the characterization and treatment of mesenteric ischemia.
In 1901, Schnitzler described a patient with a long history of postprandial pain who was found to have an atherosclerotic plaque with overlying thrombus of the superior mesenteric artery (SMA). Schnitzler concluded that if patients could develop pain of their lower extremities secondary to atherosclerosis, patients could also develop postprandial pain as a result of atherosclerosis of the mesenteric vessels. By the middle of the 20th century, Dunphy correctly hypothesized that mesenteric ischemia was a manifestation of visceral atherosclerosis.
In 1958, Shaw and Maynard described the first thromboendarterectomy of the SMA for the treatment of acute and chronic mesenteric ischemia. Several other surgical techniques have been used to revascularize obstructed mesenteric vessels, including reimplantation of the mesenteric vessels into the adjacent aorta, transaortic visceral thromboendarterectomy first described by Stoney and Wylie in 1972, and aortovisceral bypass with vein or prosthetic grafts.
While acute mesenteric ischemia is a surgical emergency, patients with chronic mesenteric ischemia typically present with a more benign process. The specific causes of mesenteric ischemia include the following:
Acute thrombotic and acute embolic mesenteric artery ischemia
Visceral venous thrombosis
Chronic mesenteric ischemia
Nonocclusive mesenteric ischemia
Whatever the cause, the result is a decreased blood supply to the small and/or large bowel resulting in ischemia, bowel infarction, necrosis, sepsis, and, ultimately, death.
Mesenteric ischemia accounts for 0.1% of all hospital admissions. Risk factors for this disease include atherosclerosis, arrhythmias, hypovolemia, congestive heart failure, recent myocardial infarction (MI), valvular disease, advanced age, and intra-abdominal malignancy.[1, 2] Mesenteric artery stenosis is found in 17.5% of independent elderly adults.[3]
Etiology can be divided into acute and chronic obstructive and nonobstructive causes.
Acute mesenteric arterial embolism usually occurs when emboli from the heart lodge in the mesenteric arteries. The sources of such emboli can be from blood stasis secondary to atrial fibrillation or from a mural thrombus after an MI.
Valvular lesions can also result in emboli to the mesenteric system. Rarely, an embolus may be composed of atherosclerotic debris that may be dislodged during arteriography or surgery, such as aortic aneurysm resection. Most emboli lodge in the SMA, just distal to the origin of the middle colic artery.
Thrombosis typically occurs at the artery origin, resulting in more structures affected by the occlusion. Embolization, unlike thrombosis, causes less ischemic disease and is associated with better survival. Mesenteric emboli account for 50% of all cases of mesenteric ischemia.
Nonocclusive mesenteric ischemia can occur without any arterial or venous abnormalities. Typically, patients have some degree of atherosclerosis of the mesenteric vessels and report symptoms when external forces such as intra-abdominal tumors compress the vessel or when they have poor perfusion secondary to congestive heart failure, MI, or hypovolemia. It is generally a syndrome of vasospasm and constriction that typically occurs in critically ill patients who are in low-flow states (eg, from septic shock, cardiac shock, burns, or hypovolemic shock).
Low-flow states cause peripheral vasodilation and shunting of the blood from the gut to the periphery. Even treatment of mesenteric insufficiency by revascularization can result in vasospasm and an ischemic episode. Cases of patients without atherosclerotic disease of their mesenteric arteries having ischemia have been reported, but this is rare and occurs in patients with profound hypovolemic shock.
Finally, digitalis has been found to cause vasoconstriction of arterial and venous smooth muscle cells in the mesenteric vasculature. Of patients with acute mesenteric ischemia, 20-30% have nonocclusive disease.
Chronic mesenteric ischemia can be the precursor to any of the above conditions. When the arterial lumen is narrowed secondary to atherosclerosis, any increase in demand of the gut (eg, eating) or a decrease in supply (eg, hypovolemia) can result in severe abdominal pain and possibly infarction. The risk factors for atherosclerosis are therefore pertinent to the development of chronic mesenteric ischemia.
Acute insufficiency of the splanchnic blood flow can result from an arterial or venous occlusive process or a nonocclusive process such as vasospasm. The splanchnic blood flow normally ranges from 10-40% of the cardiac output depending on the state of the patient. This wide variation in flow through the mesenteric system is caused by local and regional control mechanisms. Adenosine, a metabolic byproduct of ischemia, causes dilation of the splanchnic vessels, as does nitric oxide. The sympathetic system antagonizes these vasodilatory effects and causes redirection of the blood from the gut to the more vital brain and heart during times of stress. Activation of the renin-angiotensin pathway is also known to cause vasoconstriction of the splanchnic bed. During times of hypovolemia, a patient may experience nonobstructive mesenteric ischemia because of the low-flow state. The mechanism by which a patient experiences pain because of the ischemia is poorly understood.
The consequences of vascular occlusion depend on the vessels involved. A patient with chronic mesenteric ischemia with atrial fibrillation who has an embolism to a branch of the SMA may experience mild or no symptoms because of adequate collateral flow. The patient with acute thrombosis loses perfusion from the origin of the SMA, resulting in a greater amount of dead bowel. Tissue injury can result from one of 2 mechanisms: (1) ischemic injury to the bowel or (2) reperfusion injury.
Within 4 hours after ischemia begins, the mucosal villi become necrotic. As early as 6 hours, full-thickness infarction can be observed (see the first 2 images below). Submucosal hemorrhage and edema in the colon produce a characteristic thumbprinting that is depicted in the third image below. If left untreated, patients can hemorrhage into their bowel, experience perforation, and, ultimately, become septic and die.
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Pathologic findings 2 hours after bowel ischemia starts.
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Microscopic findings 24 hours after the start of ischemia.
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Thumbprinting of the bowel, a characteristic of mesenteric artery ischemia.
Reperfusion injury occurs when ischemic bowel regains its blood flow. The result is a release of oxygen free radicals by leukocytes. Other factors, such as phospholipase A2, up-regulate prostaglandins and leukotrienes, which causes more injury.
Patients with mesenteric ischemia have a very typical presentation. However, the diagnosis may be overlooked because of the vague nature of the patients' symptoms.[4] Depending on the type of mesenteric ischemia, patients may present with a variety of signs and symptoms. Patients may present with a history of postprandial pain, typically starting 20-30 minutes after their last meal, that may last up to 60-90 minutes. Because of this, they develop food fear and experience subsequent weight loss. Patients may be severely malnourished upon presentation.
Some patients may present with an acute onset of severe abdominal pain without a history of previous postprandial pain. These patients may report blood in their stool as their bowel begins to die. The classic patient with chronic mesenteric ischemia may provide a history of postprandial pain between 10 minutes and 3 hours after a meal. The pain can become so severe that the patient may develop a fear of eating and report recent weight loss. Patients may report diarrhea or constipation, and occult testing of stool may return positive results because of the sloughing of dead ischemic bowel.
Patients with acute mesenteric ischemia provide a history of sudden onset of symptoms. Further exploration may reveal a history similar to persons with chronic ischemia. Review of the past medical history may reveal other manifestations of atherosclerotic disease such as MI, stroke, or peripheral vascular disease.
Upon physical examination, the patient is thin and writhing in pain. Palpation of the abdomen reveals no peritoneal signs (pain out of proportion to examination), and auscultation of the abdomen may reveal a bruit.
Once a diagnosis of acute mesenteric ischemia is confirmed, the patient should undergo surgery because of the risk of weight loss, pain, bowel infarction, and possible death. If chronic mesenteric ischemia is diagnosed, patients should be evaluated for cardiopulmonary and renal disease before surgery is considered.
Mastery of the anatomy of the mesenteric vessels is essential to understanding and treating patients with mesenteric artery ischemia. Unfortunately, the endless array of vascular variations can make this difficult.
The celiac axis, the SMA, and the inferior mesenteric artery supply the foregut, midgut, and hindgut, respectively.
The celiac axis arises from the ventral surface of the aorta at the T12-L1 vertebral body. It courses anteroinferior before branching into the common hepatic, splenic, and left gastric arteries. Variations to this have been observed but are too numerous to describe here.
The hepatic artery gives off the gastroduodenal artery, which branches further to the right gastroepiploic artery and the anterosuperior and posterosuperior pancreaticoduodenal arteries.
The right gastroepiploic artery has a communication with the left gastroepiploic artery, which is an immediate branch of the splenic artery.
The anterosuperior and posterosuperior pancreaticoduodenal arteries communicate with the corresponding inferior branches from the SMA.
The splenic artery gives off the left gastroepiploic artery and the dorsal pancreatic artery, which supplies the body and tail of the pancreas and communicates with the anterosuperior pancreaticoduodenal and gastroduodenal arteries and, sometimes, the middle colic artery or SMA.
The third important branch of the celiac artery is the left gastric artery, which communicates with the right gastric artery along the posterior aspect of the lesser curvature of the stomach.
The celiac artery supplies most of the blood to the lower esophagus, stomach, duodenum, liver, pancreas, and spleen.
The SMA comes off of the ventral aorta and supplies the midgut by giving off the inferior pancreaticoduodenal artery and the middle colic, right colic, and jejunal and ileal branches.
The inferior pancreaticoduodenal artery gives rise to the corresponding anteroinferior and posteroinferior branches that anastomose with the superior counterparts as described above. This communication is but one important connection that helps maintain bowel perfusion in times of ischemia of the mesenteric vessels.
The ileocolic artery supplies the ileum, cecum, and ascending colon, while the middle colic artery supplies the transverse colon and communicates with the inferior mesenteric artery.
The right colic artery typically branches at the same level as the middle colic artery.
The right and middle colic arteries are important suppliers of blood to the marginal artery of Drummond and give rise to the terminal vasa recta, which provide blood to the colon.
The inferior mesenteric artery is the smallest mesenteric vessel and comes off the anterior aorta. The inferior mesenteric artery provides blood to the distal transverse, descending, and sigmoid colon and the rectum.
Many communications exist within the mesentery to the SMA, and rectal branches offer communication of the visceral blood supply with the common blood supply.
The watershed area, near the splenic flexure, is thought to be more susceptible to ischemia secondary to poor arterial flow. Because this area is poorly developed, it has an increased propensity for ischemia.
Because of the multiple areas of potential collateral flow in the mesenteric system, at least 2 of the 3 vessels must be occluded to produce chronic ischemia.
Acute mesenteric ischemia is deemed an emergency because of the poor outcomes of untreated patients. It should be treated without reservation.
Surgical treatment may be contraindicated if the risks caused by comorbid conditions preclude surgery.
If the ischemia is thought to be caused by vasospasm, surgery is not indicated. Medical management with anticoagulants and intra-arterial vasodilators is appropriate.
The following laboratory examinations should be ordered:
Prothrombin time
Activated partial thromboplastin time
Complete blood cell count, which may reveal a leukocytosis and/or hemoconcentration
Chemistry studies that may show acidosis, increased amylase levels, or increased lactate dehydrogenase levels
If a hypercoagulable state is suggested, additional laboratory studies such as tests for protein C and S deficiencies and antithrombin III deficiency can be ordered.
Plain abdominal films can yield a presumptive diagnosis in 20-30% of patients. Late findings on plain films include intramural air and air in the portal venous system. If bowel perforation occurs, free air may be observed in the abdomen.
The computed tomography (CT) findings with specificity greater than 95% include SMA or superior mesenteric vein thrombosis, intestinal pneumatosis, portal venous gas, lack of bowel wall enhancement, and ischemia of other organs. Unlike embolic occlusions, thrombosis of the SMA generally occurs flush with the aortic origin of the vessel. Distended bowel, an absence of intestinal gas, a thickened bowel wall, and air-fluid levels are nonspecific findings.
Biplane aortography is the criterion standard for the diagnosis of mesenteric ischemia. It can be used to confirm the presence and extent of occlusive disease. Anteroposterior views demonstrate collateral pathways, while lateral projections show the origins of visceral branches.
Because arteriography can precipitate acute ischemia, ensure that the patient is well hydrated. Patients with thrombosis demonstrate complete lack of visualization of the SMA and its branches, while those with embolism to the SMA demonstrate filling of the proximal SMA only with a sharp cutoff of the artery.
If the case is not emergent, consider performing a dipyridamole-thallium scan to evaluate for coronary artery disease.
Nonocclusive mesenteric ischemia is treated medically, while acute and chronic ischemia is correctable with surgery. The first step in treating nonocclusive ischemia is identifying the underlying cause and, once found, correcting it. For instance, if a patient is found to have vasospastic disease, direct injection of papaverine into the SMA may resolve the vasospasm. If resolution with papaverine occurs, start an infusion of 30-60 mg/h.
Patients with refractory vasospasm may undergo surgery to improve flow to the ischemic bowel.
In some patients with embolic disease, intra-arterial papaverine has reversed the ischemia and averted operation.
If hypovolemia is considered likely, fluid resuscitation is required.
Start all patients with possible bowel ischemia on broad-spectrum antibiotics to cover the possibility of bowel necrosis with contamination.
In cases of acute mesenteric ischemia, the surgeon should decide the location of viable versus nonviable bowel during surgery. Laparotomy reveals that the entire small bowel and proximal colon are affected in patients with SMA thrombosis, reflecting the proximal nature of this disorder. In contrast, patients with SMA embolization have sparing of their proximal jejunum, reflecting the more distal obstruction.
In patients with extensive bowel involvement, make every effort to retain every centimeter of viable bowel. If determining bowel viability is difficult, a second look may be required 24-48 hours later. Patients with emboli are treated with an embolectomy by exposing the SMA below the mesocolon distal to the middle colic artery. A longitudinal arteriotomy is made, and a Fogarty catheter is passed distal to the embolus, is inflated, and is used to extract the embolus. If closure of the arteriotomy is difficult, a patch graft may be used or the patient may require an endarterectomy. Other methods of reperfusion involving prosthetic bypass grafting or autogenous vein grafting have also been performed, and the reader is directed to a surgical technique manual for further discussion.
Kougias et al compared the effectiveness of balloon angioplasty and/or endovascular stenting (48 patients, 58 vessels) with that of open revascularization (96 patients, 157 vessels) in the treatment of chronic mesenteric ischemia.[5] The investigators found that members of the endovascular group had a shorter hospital stay (3 days) than did patients in the open revascularization group (12 days, P < 0.03) and that the 30-day mortality rate, frequency of inhospital complications, and 3-year cumulative survival rate were the same for both groups.
Three years after the procedures, however, cumulative freedom from recurrent symptoms was found in a higher percentage of open revascularization patients than in members of the endovascular group (66% vs 27%, P < 0.02). The authors suggested that this was because the percentage of patients who underwent a 2-vessel procedure rather than a 1-vessel intervention was higher in the open group than in the endovascular one.
Another study compared the outcomes of patients with chronic mesenteric ischemia who were treated with open mesenteric revascularization before (pre-endo group) and after (post-endo group) the preferential use of endovascular revascularization. The results found that patients treated post-endo presented with higher rates of hypertension, hyperlipidemia, cardiac interventions, and dysrhythmias; higher comorbidity scores; and more extensive mesenteric artery disease. However, similar outcomes for operative mortality, morbidity, length of stay, and immediate symptom improvement were noted in both the pre-endo and post-endo groups. Primary and secondary patency rates and recurrence-free survival rates were 82%, 86%, and 84% in the pre-endo group and 81%, 82%, and 76% in the post-endo group, respectively, at 5 years.[6]
Oderich et al studied 156 patients treated for mesenteric artery complications during angioplasty and stent replacement for chronic mesenteric ischemia. They concluded that complications occurred in 7% of patients, who experienced higher mortality, higher morbidity, and longer hospital stays.[7]
Patients with chronic mesenteric ischemia may have nutritional and/or electrolyte imbalances. Correct these deficiencies to prevent intraoperative and postoperative complications.
If possible, patients undergo bowel preparation the night before surgery and take nothing by mouth after midnight the evening before surgery.
In patients with acute ischemia, immediate repletion of fluids and correction of any acid-base abnormalities is necessary, followed by operation without delay.
All patients receive broad-spectrum antibiotic therapy prior to the operation.
Type and crossmatch 4 units of packed red blood cells.
If the angiogram shows embolic disease of the SMA, start intra-arterial papaverine.
A nasogastric tube may help alleviate some of the patient's pain by reducing bowel distention.
If the surgeon thinks a patient may require extensive resection and that lifelong hyperalimentation will be the only option, this possibility should be thoughtfully discussed with the patient and his or her family to help guide the surgeon during the exploration. These types of issues are best decided beforehand, with educated input from the patient, rather than during surgery, by the surgeon.
During direct visualization of the bowel, establish viability. If the first part of the jejunum is not involved, an embolus may be present and immediate embolectomy may be indicated. Look for peristalsis, and observe the color of the bowel (pink and healthy vs red and edematous). A gross specimen is depicted in the image below. Following reconstitution of arterial flow, the viability of the bowel is reassessed. This is based on clinical findings, including the color of the bowel and the presence or absence of palpable pulses.
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Gross specimen showing hemorrhagic dead bowel.
Intraoperative Doppler scans of the bowel can provide valuable information on the patency of the vessels. One gram of intravenous fluorescein followed by bowel examination under a Wood lamp can help delineate poorly perfused bowel. Institute intraoperative anticoagulation therapy with intravenous heparin.
The most reliable method of determining bowel viability is a second-look laparotomy. The decision to perform a second look is made during the initial exploration. If a second look is deemed necessary, the surgeon should not change his or her mind, regardless of the patient's clinical progress.
Because of the high likelihood of concomitant vascular disease in the rest of the arterial tree, patients must be closely monitored.
Any laboratory or radiologic examinations not previously performed in the hospital are performed in an outpatient setting.
The patient should have frequent visits to monitor the prothrombin time, activated partial thromboplastin time, and international normalized ratio to assure proper anticoagulation.
Because of the high prevalence of atherosclerosis, one of the most common complications involves MI. Prevent postoperative MI by identifying correctable coronary artery disease before the patient enters the operating room, if possible. During the perioperative period, use a Swan-Ganz catheter to monitor fluid and cardiac function. Finally, when cross-clamping the supraceliac aorta, notify the anesthesiologist, who can use myocardial protective maneuvers and afterload reduction to maximize cardiac output.
Acute renal failure in the immediate postoperative period can be prevented by keeping the patient well hydrated and administering mannitol before the aorta is cross-clamped.
Other possible complications include bleeding, infection, bowel infarction, prolonged ileus, and graft infection.
Because of the delay in diagnosis, mesenteric artery ischemia is typically a lethal disease, with a mortality rate of 45-65%. When more than half the bowel is removed, mortality rates of up to 80% have been reported. A review of 45 studies demonstrated that the prognosis for patients with acute mesenteric ischemia differs when one looks at the etiology. Mortality rates are highest for patients with arterial thrombosis (70-87%), followed by nonocclusive mesenteric ischemia (70-80%), arterial embolism (66-71%), and venous thrombosis (44%). Mortality rates have been improving over the last 4 decades.
Over the past 20 years, diagnosis and treatment of mesenteric ischemia has advanced only minimally.
In a review of 57 cases, only 18% of patients were properly diagnosed with mesenteric ischemia before operation or death. Of the 57 patients in this review, 46 died.
Some advances in diagnosis include magnetic resonance imaging and laser Doppler flowmetry.[8] Preliminary results for these modalities are encouraging.
Percutaneous transluminal angioplasty with stenting has proven valuable as a treatment option in selected patients.[9, 10, 11, 12, 13] A study demonstrated that, at 6 months, patency was equivalent between stenting and open revascularization; however, freedom from symptoms was less in the stented group.
As previously mentioned, similar results were found in a study by Kougias et al, in which the effectiveness of balloon angioplasty and/or endovascular stenting (48 patients, 58 vessels) was compared with that of open revascularization (96 patients, 157 vessels) in the treatment of chronic mesenteric ischemia.[5] The investigators determined that members of the endovascular group had a shorter hospital stay (3 days) than did patients in the open revascularization group (12 days, P < 0.03) and that the 30-day mortality rate, frequency of inhospital complications, and 3-year cumulative survival rate were the same for both groups.
Three years after the procedures, however, cumulative freedom from recurrent symptoms was found in a higher percentage of open revascularization patients than in members of the endovascular group (66% vs 27%, P < 0.02). The authors suggested that this was because the percentage of patients who underwent a 2-vessel procedure rather than a 1-vessel intervention was higher in the open group than in the endovascular one.
Some authors recommend a trial of thrombolytic therapy if patients can be treated within 8 hours of presentation and do not have signs of bowel necrosis or peritonitis.[14] If no evidence of improvement is noted within 4 hours, patients should undergo exploration.
Local tissue plasminogen activator may reduce the amount of bowel requiring resection.
Brian James Daley, MD, MBA, FACS, FCCP, CNSC, Professor and Program Director, Department of Surgery, Chief, Division of Trauma and Critical Care, University of Tennessee Health Science Center College of Medicine
Disclosure: Nothing to disclose.
Coauthor(s)
Chandler Long, MD, Resident Physician, Department of Surgery, University of Tennessee Medical Center-Knoxville
Disclosure: Nothing to disclose.
Specialty Editors
Burt Cagir, MD, FACS, Assistant Professor of Surgery, State University of New York Upstate Medical University; Consulting Staff, Director of Surgical Research, Robert Packer Hospital; Associate Program Director, Department of Surgery, Guthrie Clinic
Disclosure: Nothing to disclose.
Francisco Talavera, PharmD, PhD, Adjunct Assistant Professor, University of Nebraska Medical Center College of Pharmacy; Editor-in-Chief, Medscape Drug Reference
Disclosure: Medscape Salary Employment
Michael A Grosso, MD, Consulting Staff, Department of Cardiothoracic Surgery, St Francis Hospital
Disclosure: Nothing to disclose.
Paolo Zamboni, MD, Professor of Surgery, Chief of Day Surgery Unit, Chair of Vascular Diseases Center, University of Ferrara, Italy
Disclosure: Nothing to disclose.
Chief Editor
John Geibel, MD, DSc, MA, Vice Chair and Professor, Department of Surgery, Section of Gastrointestinal Medicine, and Department of Cellular and Molecular Physiology, Yale University School of Medicine; Director, Surgical Research, Department of Surgery, Yale-New Haven Hospital
Sivamurthy N, Rhodes JM, Lee D. Endovascular versus open mesenteric revascularization: immediate benefits do not equate with short-term functional outcomes. J Am Coll Surg. 2006;202(6):859-67.
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