30.5.1 Superior Mesenteric Artery Embolism

SMA embolism is the most dramatic of the mesenteric vascular diseases and accounts for 33 to 50% of acute mesenteric ischemia. ^{1 , 7 , 31} Most commonly, this originates as a consequence of atrial fibrillation or acute myocardial infarction. It affords the potential for complete reversal and resolution if diagnosis and treatment are carried out promptly. ³²

The disease is characterized by a sudden onset of severe abdominal pain that generally is out of proportion to the physical examination. Associated findings include forceful gastric emptying with vomiting in approximately one-half of the patients and diarrhea in one-third. The white blood cell count usually is elevated, and frequently a history of cardiac disease and/or previous embolic phenomena is present. Plain radiography may show dilated thickened bowel loops, a ground-glass appearance due to ascites, thumbprinting, and toxic dilatation or gas in the bowel wall, portal vein, or peritoneum. All these features indicate infarction, but one-fourth of patients with infarction have a normal plain abdominal radiograph. ¹ Duplex ultrasonography of the mesenteric vessels is highly sensitive and specific; however, it is often technically limited by accompanying abdominal distention and overlying bowel gas. The historical gold standard for the diagnosis of mesenteric ischemia was selective catheterization and mesenteric angiography, but CT angiography with its better image quality, availability, and relative ease of image acquisition has challenged angiography. Conventional CT may also show ascites, intestinal wall thickening, mucosal thumbprints, pneumatosis, and portal vein gas but may be normal in 30% of patients with proven mesenteric ischemia. ¹ Diagnosis is confirmed by arteriogram. Characteristically, a sharp cutoff or meniscus sign is present at the site of the embolus several centimeters from the takeoff of the SMA. The most proximal branches supplying the proximal jejunum and the right transverse colon usually are not affected. This differentiates SMA embolism from SMA thrombosis, where the occlusion occurs at the origin of the vessel (▶ Fig. 30.2).

Some favorable early results also have been seen with thrombolytic therapy. ^{33 , 34 , 35 , 36} However, most patients with SMA embolism will need surgery, particularly when progression of the ischemic injury is suspected. The characteristic finding at surgery is a normal proximal jejunum with pulses present, reflecting the more distal placement of the embolus beyond the origin of the SMA. The ischemic changes are seen from the level of the midportion of the jejunum to the transverse colon, and no pulses are found in any of the vessels to this large section of the small and large bowels. This differs from SMA thrombosis, which is accompanied by ischemic changes involving the entire jejunum, the ileum, and the right colon.

Treatment of SMA embolism includes embolectomy or arterial reconstruction. Resection should be limited to those cases in which intestinal segments are frankly infarcted (▶ Fig. 30.3). ^{1 , 31} Early embolectomy alone usually is sufficient to restore perfusion (▶ Fig. 30.4). Care must be taken to evacuate all distally propagated thrombi, and narrowing must be avoided when closing the arteriotomy site. The need for small bowel resection often may be avoided by reevaluating the viability of the bowel 15 to 30 minutes after restoration of blood flow.

Traditional methods of determining bowel viability following reperfusion are inaccurate. Reliance on the return of normal color, the presence of mesenteric pulsations, and peristalsis promotes unnecessary bowel resection in up to 50% of cases. ³⁷ It is much more accurate to determine viability by fluorescein dye injection or by Doppler ultrasonography. Both techniques are relatively simple and allow for more precise delineation of nonperfused and nonviable bowel. ^{31 , 37 , 38} The use of surface oximetry to assess the adequacy of intestinal tissue oxygenation is especially promising. Sheridan et al ³⁹ have used a modified Clark oxygen electrode to measure tissue oxygen tension (PtO₂) and have established a reference range for intraoperative PtO₂ for the entire gastrointestinal (GI) tract. The papaverine infusion may be continued for 12 to 24 hours, and repeat angiograms may be obtained to ascertain that the vasoconstriction has been abolished. ³¹ Heparin is controversial because GI hemorrhage is a significant risk. Thrombolytic therapy with streptokinase, urokinase, or recombinant tissue plasminogen activators in cases of acute and subacute SMA embolism or thrombosis has been described. ¹

The use of second-look laparotomy may maximize intestinal salvage for those cases in which viability is uncertain. The decision to perform a second-look procedure should be made at the time of the original operation. Re-exploration has been advocated 12 to 48 hours later, regardless of apparent clinical improvement or stabilization of the patient’s overall condition. To avoid a formal second-look operation following massive resection for bowel infarction Slutzki et al ⁴⁰ used laparoscopic inspection to assess the integrity of the anastomosis and viability of the remaining bowel. At the primary operation, two 10-/12-mm laparoscopic trocars were inserted in the lower quadrants, and 48 to 72 hours later the abdominal contents were inspected laparoscopically in five consecutive patients. The authors found the technique safe and reliable in all patients. Because of concern about decreasing mesenteric blood flow, care was taken to limit the pressure to 15 mm Hg during the procedure. ⁴⁰

Anadol et al ⁴¹ compared open and laparoscopic “second-look” procedures in patients with mesenteric ischemia. In the open group (41 patients), the abdomen was closed and a second-look laparotomy was performed in 23 patients. In the laparoscopic group (36 patients), a 10-mm trocar was inserted before closing the abdomen and second-look intervention was performed by a laparoscope in 23 patients. Sixteen of the re-laparotomies in the open group (70%) revealed nothing and were unnecessary. Two patients (8%) in the laparoscopic group needed re-resection, while 20 patients (87%) were rescued from unnecessary laparotomies.

Some authors are comfortable enough with Doppler assessment of bowel viability that they no longer recommend second-look procedures. ⁴² In a review of the literature, Bergan ⁴³ demonstrated that second-look operations are useful only for select patients. Of 49 patients who had survived SMA embolectomy, a second-look operation was not performed in 42 of these survivors. Among those seven patients in whom the second-look procedure was performed, resection was necessary in only two, suggesting that the yield from this operation is modest when it is not performed on an individualized basis. The use of a second-look operation is clearly indicated whenever bowel of questionable viability has been left behind. ³¹ Sales et al ⁴⁴ reported on a series of 29 patients who underwent small bowel resection primarily for mesenteric artery occlusive disease. All patients were given an ostomy, and the authors believe that this policy decreased the mortality rate (34%) in their series. All the surviving patients had intestinal continuity restored.

Bingol et al ⁴⁵ reported 24 patients who underwent SMA embolectomy. The patients were divided into three groups according to the onset of symptoms and operation time. Group I (n = 12) patients were operated on in the first 6 hours after onset of symptoms; group II (n = 9) patients were operated on between 6 and 12 hours after onset of symptoms; and group III (n = 3) patients underwent embolectomy after 12 hours. Low-dose (5–10 mg) local tissue-type plasminogen activator (t-PA) administration directly into the SMA was an additional procedure with the embolectomy in all patients. The macroscopic view of the intestine was normal in 15 patients (12 patients in group I and 3 patients in group II) 30 minutes after the administration of local t-PA. Segmental resection was necessary in four patients in group II. Extended resection was necessary in two patients in group II and three patients in group III and all the patients died during the early postoperative period. They suggest that exploratory laparotomy should be done in patients with sudden abdominal pain, nausea, vomiting, mild leucocytosis, and metabolic acidosis who have previous valvular heart disease or atrial fibrillation. Ultimately, selective low-dose t-PA (5–10 mg) administration reduces the length of intestinal portion to be resected.

Savassi-Rocha and Veloso ⁴⁶ reported a case of SMA embolism in which arterial flow was reestablished by selective intra-arterial infusion of streptokinase. They found 18 similar cases in the literature. This procedure could be an alternative to embolectomy in selected patients, that is, patients with an early diagnosis, no evidence of intestinal necrosis, and with partial occlusion and/or occlusion of secondary branches of the SMA. Frequent arteriographies and intensive care are necessary in this approach. The patient should be continuously monitored because of the possibility of treatment failure and the need for embolectomy.

30.5.2 Superior Mesenteric Artery Thrombosis

SMA thrombosis is distinguishable from embolism because of the more insidious onset of symptoms and the prominence of hypovolemic signs initially and cardiovascular collapse later. It accounts for 5 to 50% of acute mesenteric ischemia. ^{1 , 7 , 31} The usual presentation involves the gradual onset of abdominal pain associated with progressive distention and clinical signs of dehydration. Frequently there is anorexia, nausea and vomiting, and diarrhea with occult or gross blood. Leukocytosis is usually present. Often there is a history compatible with chronic intestinal insufficiency. ^{1 , 47} Although a diagnosis can be made by arteriogram, most patients are so acutely ill at the time of presentation that surgery is inevitable, and often the definitive diagnosis is made at the time of operation. Arteriography usually shows a cutoff of SMA blood flow at its origin. When advanced disease is present, plain abdominal X-ray films may show air in the portal vein and the liver (▶ Fig. 30.5).

As with SMA embolism, initial operative management for arterial thrombosis must include revascularization of any extensive segment of ischemic bowel. Thromboendarterectomy for acute mesenteric arterial thrombosis has been associated with a high failure rate. Aortomesenteric bypass may be beneficial even if viability is not completely restored and resection becomes necessary. ³¹ The graft may salvage marginally viable proximal jejunum, which ultimately may allow the patient to be maintained on oral alimentation. In addition, the graft may lessen the risk of anastomotic leak, since healing may be impaired if an anastomosis is performed in a potentially compromised but still viable small bowel. It has been argued that emergency bypass is doomed to failure because the gut has already infarcted, early graft thrombosis is almost universal, and the patient is likely to succumb from the systemic effects of reperfusion. ¹ For these reasons, extensive resection is probably preferable to time-consuming attempts at revascularization. Johnston et al ⁴⁸ reported on nine patients who underwent a bypass graft because of acute mesenteric thrombosis with an operative mortality of 22%. Survival at 1 year was 65% and survival at 5 years was 52%.

30.5.3 Nonocclusive Mesenteric Ischemia and Infarction

Nonocclusive mesenteric infarction has been diagnosed with increasing frequency in intensive care unit settings among patients critically ill from other unrelated diseases. It accounts for 20 to 30% of cases of mesenteric ischemia. ^{1 , 7 , 31} The signs and symptoms of nonocclusive mesenteric ischemia or infarction are similar to those of thrombotic infarction, except that nonocclusive disease tends to occur in a specific group of vulnerable patients. The disease should be suspected in any patient with cardiovascular disease and abdominal pain. Although the diagnosis is difficult to make, it is important to differentiate from other causes of ischemia because therapy is primarily nonoperative. Arteriography in these patients generally does not reveal an occlusion but shows reduced blood flow secondary to severe mesenteric vasospasm. Newer studies show that the renin–angiotensin axis, not catecholamines, may be the primary mediator of the splanchnic vasoconstriction seen in response to the severe physiologic stress associated with this condition. ^{49 , 50}

Predisposing factors to nonocclusive ischemia include (1) patients with congestive heart failure who are taking digitalis and diuretics, (2) patients with valvular heart disease and low output syndromes, (3) patients with digitalis intoxication and cardiac arrhythmia, (4) patients in shock or with prolonged hypovolemia, and (5) patients experiencing postoperative hypotension. The common denominator for all these predisposing factors is the low-flow state.

Initial treatment should focus on the underlying problem contributing to the presentation. The correction of hypovolemia, treatment of arrhythmias, and relief of congestive heart failure are crucial beginnings. Antibiotics may be helpful since the ischemia may result in a loss of the mucosal barrier to bacteria. A number of vasodilator drugs have been tried, but the one most frequently used is papaverine (30–60 mg/h), usually given by angiographic catheter infusion until clinical and radiologic resolution, for up to 5 days. ^{51 , 52} Epidural block and intraoperative splanchnic block also have been used to relieve the reflex component of the vasospasm. In many patients, nonthrombotic ischemia cannot be differentiated from infarction, and laparotomy is necessary for this distinction to be made. At laparotomy, all necrotic bowels should be resected; splanchnic block or epidural block may be added at that time. The prognosis for nonocclusive mesenteric ischemia tends to be poor largely because of the severity of the underlying illness that precipitates the ischemic event.

Ward et al ⁵³ adopted an aggressive approach to the management of these patients. In a review of 34 patients with nonocclusive mesenteric ischemia, 7 patients underwent visceral arteriography, 2 of whom required operation and both died. Of the 29 patients who were explored, 21 had segmental injury and 8 had massive injury. Of the 21 with segmental injury, 12 (57%) had a primary anastomosis, 5 of whom died (42%). Nine of 21 patients (43%) underwent delayed anastomosis, and 2 of them died (22%). None with massive injury underwent primary anastomosis. A second-look operation was performed on 22 of 29 patients (76%). Eleven of the 22 (50%) underwent further bowel resection. Overall, 55% survived.

Schuler and Hudlin ⁵⁴ described the presentation and management of five cases of nonocclusive ischemic cecal necrosis. Four of the patients presented with right-sided abdominal pain, tenderness, and leucocytosis. The preoperative diagnosis was incorrect in all patients. Two patients were thought to have appendicitis, two were thought to have carcinoma, and one was thought to have a perforated viscus. Each patient underwent a right hemicolectomy and four survived. Each of the patients had ischemic necrosis without evidence of emboli or vasculitis or hypotension. Ischemic necrosis of the cecum is an infrequent variant of ischemic colitis that should be considered in the differential diagnosis of the elderly patient presenting with right lower quadrant pain.

Neri et al ⁵⁵ reviewed the diagnostic and treatment methods that emerged from their experience in 371 patients with a diagnosis of aortic dissection. Mesenteric ischemia was present in 19% of patients. In 9% of patients, bowel ischemia was not associated with a false lumen anatomy or an extension of the dissection process. The mortality rate in patients with nonocclusive mesenteric ischemia was 86%; sepsis and multiple organ failure were the cause of death in all nonsurvivors. Surgical treatment was beneficial only in the early phases of the disease. In patients who underwent operation, the significant risk factors were severe coagulation disorders, postoperative cerebral ischemia, maximal oxygen extraction rate of more than 0.40, aortic calcinosis, chronic obstructive pulmonary disease, thrombosis of the false lumen, inotropic support, and chronic renal insufficiency.

30.5.4 Mesenteric Venous Thrombosis

Mesenteric venous thrombosis accounts for 5 to 30% of all cases of gut ischemia. ^{7 , 31} Bradbury et al ¹ classified the causes of mesenteric venous thrombosis (▶ Table 30.1). To this list, Flaherty et al ⁵⁶ added a previously unrecognized cause of ischemia characterized by a vasculitis of mesenteric veins and their intramural tributaries. The authors proposed the term “mesenteric inflammatory veno-occlusive disease” to describe the entity.

Mesenteric venous thrombosis is characterized by the insidious onset of abdominal discomfort. The subacute nature of the symptoms may persist for 1 to 4 weeks. Progression of the disease is accompanied by more severe symptoms of crampy or diffuse abdominal pain, distention, or vomiting. The chief symptom of colicky pain is usually universal, nonlocalizing, and out of proportion to the meager findings of the physical examination. Mesenteric venous occlusion can often be differentiated from the previously described arterial occlusive syndromes by one of several commonly associated diseases that are present in most of the patients (▶ Table 30.1). Between 15 and 44% of patients with primary venous thrombosis will have suffered previous thromboembolic disease. ¹ The physical examination is so nonspecific that it belies the seriousness of the situation. Physical findings vary with the stage of disease and may manifest as abdominal tenderness, distention, decreased bowel sounds, guarding, rebound tenderness, a temperature greater than 38 °C, and clinical signs of shock in 25% of patients.

In general, diagnostic laboratory studies are disappointing, the exception being diagnostic peritoneal lavage, which uniformly returns serosanguineous fluid. ^{57 , 58} A leukocytosis of 10,000 to 30,000/mm³ with a leftward shift is often present. Evaluation for a hypercoagulable state should be made if the diagnosis is suspected. Radiographs, whether plain or with contrast, rarely assist in the diagnostic process. CT has established the diagnosis in 90% of cases by demonstrating thrombus directly. ¹ Small bowel follow-through findings may include marked thickening of the bowel wall and valvulae conniventes because of congestion and edema, separation of loops caused by mesenteric thickening, a long transition zone between involved and uninvolved bowel with progressive narrowing of the lumen by thickened wall, and thumbprints. Angiographic findings may include the demonstration of a thrombus in the superior mesenteric vein with partial or complete occlusion, failure to visualize the superior mesenteric or portal vein, slow or absent filling of mesenteric veins, arterial spasm, failure of arterial arcades to empty, and a prolonged blush in the involved segment. ⁷ Diagnosis frequently is made at the time of operation.

Treatment of mesenteric venous thrombosis includes fluid resuscitation, antibiotics, and prompt heparinization. ¹ The development of an acute abdomen requires operative intervention. Operative findings include the presence of congested, cyanotic, bluish-black, edematous bowel with arterial pulsations present in the mesentery. Thrombosed veins may be clearly visible, and sectioning across the mesentery shows thrombus extruding from the mesenteric veins and brisk arterial bleeding. Occasionally, a venous thrombectomy is helpful. If a long segment of bowel is involved and there is complete thrombosis of the superior mesenteric vein with possible extension to the portal vein, venous thrombectomy is indicated. A second-look operation should be performed, at which time a better assessment of the extent of nonviable bowel is made. Heparin therapy is instituted. ⁷ For short segments of bowel involvement, thrombectomy would not appear to be indicated. A wide resection of involved bowel is recommended with a primary end-to-end anastomosis. If there is doubt regarding the wisdom of restoring intestinal continuity, the bowel can be brought to the surface as a stoma or reexamined at a “second look.” Anticoagulant therapy with heparin is indicated and should be initiated during or immediately after operation, ^{1 , 59 , 60} and anticoagulation therapy should be continued for several months postoperatively unless specifically contraindicated by other associated diseases. Following resection, about half of the patients experience recurrence if anticoagulants are not administered, and of those with recurrence, approximately 50% are found to have an associated deep venous thrombosis or pulmonary embolus. ⁶¹ In the study cited, treatment with anticoagulants dramatically decreased mortality; without operation and without anticoagulant therapy, the natural history of mesenteric venous thrombosis resulted in a 95% mortality rate; with operation but without anticoagulant therapy, the mortality rate was 65%; and with operation, followed by immediate anticoagulant therapy, the mortality rate was 35%. ⁶¹

Rhee et al ⁶² evaluated the outcome of 72 patients with mesenteric venous thrombosis—53 acute and 19 chronic. A laparotomy was performed in 34 patients, 31 undergoing bowel resection and 1 an unsuccessful mesenteric venous thrombectomy. Mesenteric venous thrombosis recurred in 36%. The 30-day mortality rate was 27%. The long-term survival of patients with acute mesenteric venous thrombosis was worse than for chronic disease (36 vs. 83% at 3 years).

Divino et al ⁶³ analyzed nine patients treated surgically for mesenteric venous thrombosis. The most common presenting symptom was abdominal pain with bloody diarrhea in three patients; preoperative diagnosis of mesenteric vein thrombosis was suspected in two. Radiologic tests included plain X-rays, CT, and ultrasound. The time to operation ranged from 3 hours to 7 days after admission. All patients underwent resection of infarcted bowel with primary anastomosis and immediate postoperative anticoagulation. No patient underwent a second-look operation. The postoperative morbidity and mortality rates were 55 and 11%, respectively.

An algorithm outlining a possible approach to the management of mesenteric ischemia was published by Bradbury et al (▶ Fig. 30.6). ¹

30.5.5 Chronic Mesenteric Vascular Disease

A detailed account of chronic mesenteric vascular disease or “intestinal angina” is beyond the scope of this text, and the reader is referred to textbooks of vascular surgery. However, any discussion of acute mesenteric vascular disease would be incomplete without a brief overview of the salient points of chronic mesenteric vascular disease.

Mesenteric angina is poorly understood partly due to problems involved in diagnosing and defining the disease as a clinical syndrome. The disease is difficult to induce experimentally because the rich mesenteric collateral circulation has made it difficult to develop a satisfactory animal model. Diagnosis is further complicated by the lack of correlation between arteriographic findings and clinical symptoms. Finally, clinical studies on this disease are remarkably limited, particularly when compared with the wealth of material available on vascular disease involving other organs or organ systems.

Croft et al ⁶⁴ reviewed autopsy material on 203 patients and tried to correlate arteriographic findings with clinical symptoms and autopsy findings. Critical stenosis on two of three vessels was seen in only four of their patients, and correlation with symptoms was not found. Other researchers have reported that complaints of intestinal angina precede acute intestinal infarction in a sizable percentage of cases. Kwaan and Connolly ⁴⁷ noted that they found conspicuous warning signs present for several months in all 25 patients operated on for acute intestinal infarction.

The classic triad of symptoms is postprandial pain, fear of eating, and involuntary weight loss. The most consistent symptom complex involves the presence of postprandial pain in association with weight loss and malabsorption. The postprandial pain often is associated with “food fear,” causing the patient to refuse to eat because of the fear of subsequent pain. The pain, which is directly related to eating, is experienced soon after a meal and lasts for several hours. Because patients with chronic mesenteric vascular disease frequently are cachectic in appearance, they sometimes are evaluated for the presence of widespread malignancy rather than vascular disease. Color flow duplex scanning is increasingly used as the first-line investigation of patients suspected of having mesenteric ischemia. When an arteriogram is performed, high-grade stenosis or complete occlusion of three mesenteric vessels suggests that significant ischemic disease may be present. No relationship has been found between the loss of intestinal absorptive function and the degree of reduced flow seen on angiography. ⁶⁵ Because of the prevalence of asymptomatic arterial stenosis, the diagnosis is difficult and the indications for surgery are unclear. In general, surgery should be considered when a patient has a clinical presentation that is compatible with intestinal ischemia, arteriographic evidence of critical stenosis in two of three vessels, and no plausible explanation for the abdominal pain.

A patient with intestinal angina and weight loss, in whom other causes have been excluded, and in whom angiography shows occlusive disease of at least two of three major visceral arteries, should be considered for revascularization. Few patients meet these criteria. Surgical options for reconstruction include bypass grafting, endarterectomy, and reimplantation. Bypass grafting has been the preferred procedure, ^{48 , 66} with most authors recommending prosthetic grafts over autogenous vein grafts. Prosthetic grafts have less tendency for kinking when used between the aorta and the mobile SMA. They also are more readily available than vein grafts. Total revascularization of all affected vessels is preferred to single-vessel revascularization, since this may decrease the incidence of late recurrence. ^{48 , 67 , 68} Because of the presence of significant atherosclerotic disease in the adjacent aorta, reimplantation is seldom performed.

Illuminati et al ⁶⁹ reported on 11 patients who underwent revascularization of 11 digestive arteries for symptomatic chronic mesenteric occlusive disease. Eleven superior mesenteric arteries and 1 celiac axis were revascularized. The revascularization techniques included retrograde bypass grafting in seven cases, antegrade bypass grafting in two, percutaneous arterial angioplasty in one, and arterial reimplantation in one case. There was no operative mortality. Cumulative survival rate was 88.9% at 36 months. Primary patency rate was 90% at 36 months. The symptom-free rate was 90% at 36 months. They found that direct reimplantation and antegrade and retrograde bypass grafting all allowed good midterm results: the choice of the optimal method depends on the anatomic and general patient’s status. Angioplasty alone yields poor results and should be limited to patients at poor risk for operation.

Leke et al ⁷⁰ reported their experience with a tailored surgical approach of 16 patients operated on for chronic mesenteric ischemia. The patients ranged in age from 32 to 80 years and 75% of patients were females. The most common preoperative complaints were postprandial abdominal pain and weight loss. Revascularization was tailored to the arterial anatomy and included bypass to the SMA alone (eight), bypass to the celiac artery and SMA (six), SMA reimplantation onto the aorta (one), SMA/IMA reimplantation (one), and transaortic endarterectomy of the celiac artery/SMA (one). There was one perioperative death (mortality 5.6%). Follow-up duplex scans at a mean of 34 months showed no graft thromboses.

Some early success has been reported following angioplasty for chronic mesenteric vascular disease. ^{71 , 72 , 73} Success rates of 70 to 100% have been reported with recurrence rates of 10 to 50% within 4 to 28 months. ¹ If the patient’s symptoms later recur following angioplasty, the history of having undergone successful angioplasty suggests that the patient may expect a favorable result from surgical reconstruction.

Kasirajan et al ⁷⁴ evaluated the efficacy of percutaneous angioplasty and stenting in comparison with traditional open surgical revascularization for the treatment of chronic mesenteric ischemia. Although the results of percutaneous angioplasty and stenting and open surgery were similar with respect to morbidity, death, and recurrent stenosis, percutaneous angioplasty and stenting was associated with a significantly higher incidence of recurrent symptoms and thus their suggestion that open surgery should be preferentially offered to patients deemed fit for open revascularization.

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