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66 www.nietoeditores.com.mx ORIGINAL ARTICLE Acute mesenteric ischemia: an emergency that requires a comprehensive diagnostic approach. Abstract BACKGROUND: Acute mesenteric ischemia is a vascular emergency with mortality over 60%, which requires timely treatment. However, due to its heterogeneous pathophysiology and differences in degree and extent of ischemic damage, the clinical and radiological mani- festations are varied and often nonspecific; consequently, a thorough analysis of medical background, laboratory studies, and clinical and radiological findings is recommended in order to establish a timely diagnosis. OBJECTIVE: Identify the most common findings, direct and indirect, by computed tomography and determine low, intermediate, and high probability of a patient suffering from acute mesenteric ischemia on the basis of risk factors and clinical, biochemical, and radiological findings. MATERIAL AND METHODS: We performed a retrospective, observa- tional, cross-sectional study, with analysis of findings from computed tomography images of a series of cases of patients with diagnosis of acute mesenteric ischemia in a period of 9 years, 3 months and literature review. The purpose was to analyze the risk factors and clinical and biochemical data most commonly associated with acute mesenteric ischemia. RESULTS: Our universe included tomographic studies of 27 cases of acute mesenteric ischemia, with average age of 60.8 years. The most common clinical finding was acute abdominal pain syndrome in 19 patients (70%); the most commonly associated history was type 2 diabetes mellitus and systemic high blood pressure in 7 (26%) patients each; 13 patients (48%), according to the clinical file, had laboratory studies, of whom 11 (85%) had leukocyte values of 9,200 to 68,000; the most commonly identified findings were: arterial filling defect 48%, intestinal pneumatosis 29%, venous filling defect 22%, bowel obstruction syndrome 22%, and identification of free fluid 22%. CONCLUSION: It is advisable to conduct a quantitative analysis giving a specific value to the different findings, including risk factors, physical examination, laboratory studies, and image findings, to determine the risk of acute mesenteric ischemia in a patient with acute abdominal pain syndrome. CTA is the study with the greatest diagnostic precision. KEYWORDS: mesenteric vascular occlusion; superior mesenteric artery; emission computed tomography Moa-Ramírez GA 1 , Sánchez-García JC 2 , Onveros-Rodríguez A 3 , López- Ramírez MA 4 , Rebollo-Hurtado V 5 , García-Ruiz A 6 , Noyola-Villalobos H 7 1 Radiologist. Postgraduate course on Sectional Imaging of the Body, from the Ionizing Radiaon Department, CAT scan subsecon. 2 Medical doctor, 3 rd . year Resident of the Specialty Course and Residency in Radiology and Imaging. Escuela Militar de Graduados de Sanidad. 3 Medical doctor, 3 rd year Resident of the Specialty Course and Residency in General Surgery. Escuela Militar de Graduados de Sanidad. 4 Medical doctor 4 th year Resident of the Specialty Course and Residency in General Surgery. Escuela Militar de Graduados de Sanidad. 5 Radiologist. Postgraduate course on Seconal Imag- ing of the Body, staff doctor from the Ionizing Radia- on Department, Head of the CAT scan subsecon. 6 Medical doctor. Postgraduate course on Advanced Laparoscopic Surgery, staff doctor of the General Surgery Department. 7 Medical doctor. Postgraduate course on Advanced Transplant surgery, Head of the General Surgery Department. Hospital Central Militar, Blvd. Manuel Ávila Camacho s/n Lomas de Sotelo, Miguel Hidalgo, 11200 México, D. F. 55573100, extensiones 1406 y 1928. Correspondence Gaspar Alberto Moa-Ramírez [email protected] This paper must be quoted as Moa-Ramírez GA, Sánchez-García JC, Onveros- Rodríguez A, López-Ramírez MA, Rebollo-Hurtado V, García-Ruiz A et al. Isquemia mesentérica aguda: urgencia que exige un abordaje diagnósco integral. Anales de Radiología México 2015;14:66-88. Received: Janueary 8, 2015 Accepted: January 20, 2015 Anales de Radiología México 2015;14:66-88.
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Acute mesenteric ischemia: an emergency that requires a comprehensive diagnostic approach

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Acute mesenteric ischemia: an emergency that requires a comprehensive diagnostic approach.
Abstract
BACKGROUND: Acute mesenteric ischemia is a vascular emergency with mortality over 60%, which requires timely treatment. However, due to its heterogeneous pathophysiology and differences in degree and extent of ischemic damage, the clinical and radiological mani- festations are varied and often nonspecific; consequently, a thorough analysis of medical background, laboratory studies, and clinical and radiological findings is recommended in order to establish a timely diagnosis.
OBJECTIVE: Identify the most common findings, direct and indirect, by computed tomography and determine low, intermediate, and high probability of a patient suffering from acute mesenteric ischemia on the basis of risk factors and clinical, biochemical, and radiological findings.
MATERIAL AND METHODS: We performed a retrospective, observa- tional, cross-sectional study, with analysis of findings from computed tomography images of a series of cases of patients with diagnosis of acute mesenteric ischemia in a period of 9 years, 3 months and literature review. The purpose was to analyze the risk factors and clinical and biochemical data most commonly associated with acute mesenteric ischemia.
RESULTS: Our universe included tomographic studies of 27 cases of acute mesenteric ischemia, with average age of 60.8 years. The most common clinical finding was acute abdominal pain syndrome in 19 patients (70%); the most commonly associated history was type 2 diabetes mellitus and systemic high blood pressure in 7 (26%) patients each; 13 patients (48%), according to the clinical file, had laboratory studies, of whom 11 (85%) had leukocyte values of 9,200 to 68,000; the most commonly identified findings were: arterial filling defect 48%, intestinal pneumatosis 29%, venous filling defect 22%, bowel obstruction syndrome 22%, and identification of free fluid 22%.
CONCLUSION: It is advisable to conduct a quantitative analysis giving a specific value to the different findings, including risk factors, physical examination, laboratory studies, and image findings, to determine the risk of acute mesenteric ischemia in a patient with acute abdominal pain syndrome. CTA is the study with the greatest diagnostic precision.
KEYWORDS: mesenteric vascular occlusion; superior mesenteric artery; emission computed tomography
Motta-Ramírez GA1, Sánchez-García JC2, Ontiveros-Rodríguez A3, López- Ramírez MA4, Rebollo-Hurtado V5, García-Ruiz A6, Noyola-Villalobos H7
1 Radiologist. Postgraduate course on Sectional Imaging of the Body, from the Ionizing Radiation Department, CAT scan subsection. 2 Medical doctor, 3rd. year Resident of the Specialty Course and Residency in Radiology and Imaging. Escuela Militar de Graduados de Sanidad. 3 Medical doctor, 3rd year Resident of the Specialty Course and Residency in General Surgery. Escuela Militar de Graduados de Sanidad. 4 Medical doctor 4th year Resident of the Specialty Course and Residency in General Surgery. Escuela Militar de Graduados de Sanidad. 5 Radiologist. Postgraduate course on Sectional Imag- ing of the Body, staff doctor from the Ionizing Radia- tion Department, Head of the CAT scan subsection. 6 Medical doctor. Postgraduate course on Advanced Laparoscopic Surgery, staff doctor of the General Surgery Department. 7 Medical doctor. Postgraduate course on Advanced Transplant surgery, Head of the General Surgery Department. Hospital Central Militar, Blvd. Manuel Ávila Camacho s/n Lomas de Sotelo, Miguel Hidalgo, 11200 México, D. F. 55573100, extensiones 1406 y 1928.
Correspondence Gaspar Alberto Motta-Ramírez [email protected]
This paper must be quoted as Motta-Ramírez GA, Sánchez-García JC, Ontiveros- Rodríguez A, López-Ramírez MA, Rebollo-Hurtado V, García-Ruiz A et al. Isquemia mesentérica aguda: urgencia que exige un abordaje diagnóstico integral. Anales de Radiología México 2015;14:66-88.
Received: Janueary 8, 2015
Accepted: January 20, 2015
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INTRODUCTION
Acute mesenteric ischemia is not an isolated clinical entity but rather involves a complex group of abnormalities that include mesenteric artery embolic thrombosis, mesenteric venous thrombosis and non occlusive mesenteric isch- emia.1 Table 12 and Figures 1-2.
Acute mesenteric ischemia is a disease that mainly involves patients over 60 years of age, with a male gender predominance occurring in 1 of every 1 000 hospital admissions; some series report up to 5% hospital mortality.3 Among the multiple factors that account for an increased incidence we find a more frequent diagnosis due to the growing elderly adult population as well as an increase in the num- ber of patients in critical condition. In spite of advances of knowledge in pathophysiology, laboratory diagnosis and imaging studies, acute mesenteric ischemia is a potentially
lethal vascular emergency, associated to a mortality over 60% 1,4-6 if diagnosis takes more than 12 hours, and over 90% if it takes longer than 24 hours;7 its diagnostic approach is a clinical challenge.8
The challenge is to establish a timely and reliable diagnosis, in order to have a rapid inter- vention allowing to re-establish the mesenteric blood flow, thus preventing intestinal necrosis. Due to the heterogeneity in its pathophysiology and to the differences in grade and extension of ischemic damage, the clinical and radiological manifestations are diverse and often nonspe- cific. The key to an efficient management of this syndrome follows three principles: 1) high clini- cal suspicion; 2) proper selection of available imaging techniques to establish the diagnosis: 3) knowledge of factors that increase surgical efficacy when indicated. This approach must prevail to have a better outcome in caring for this disease. 3
Table 1. Three causes of acute mesenteric ischemia
Types of mesenteric ischemia Acute mesenteric arterial
embolism Acute mesenteric arterial
Atherosclerotic disease, trauma, infection
liver lesion Clinical findings
findings
findings
Late Increased abdominal pain, distention, absent bowel sounds, disturbances in mental status, peritoneal signs, sepsis
Diagnostic test Angiogram
Treatment
All sorts of hemodynamic sup- port, correction of acidosis, antibiotics, gastric decom- pression
Superior mesenteric embo- lectomy, chronic anticoagu-
lation
Intestinal infarction Surgery
Pathophysiology
Acute mesenteric ischemia involves an inad- equate condition of tissue perfusion that prevents from meeting the metabolic demands from one or more of the organs included in the mesenteric circulation. It is estimated that the main cause of acute mesenteric ischemia is arterial occlu- sion with a thrombus in approximately 50% of cases.1,6,8,9 Most of the thrombi originate in the atrium or left ventricle from detachment of a mural thrombus or from valvular lesions. These thrombi are often associated with cardiac ar- rhythmias such as atrial fibrillation or hypokinetic regions resulting from a previous infarction. Around 15% of embolisms lodge in the origin of the superior mesenteric artery (Figures 1 and 2, Table 210) while the rest can lodge 3 to 10 cm distal to the origin of the middle colic artery. In up to 20% of cases the embolism that originates in the superior mesenteric artery is associated with concurrent emboli in some other vascular bed.10,11 Modified Table 2.10 It is important to consider that intestinal ischemia due to an em- bolism can be found with reactive mesenteric vasoconstriction reducing the collateral flow with exacerbation of the ischemic damage.
Risk factors
The risk factors that most often have been asso- ciated, in different case series, with this disease are atherosclerosis (90%), heart disease (85%), systemic hypertension (85%), atrial fibrillation (75%), smoking (50%), digitalis use (50%) and obesity (40%).1,2,6,9
Clinical presentation
Acute mesenteric ischemia involves a complex group of abnormalities that include mesenteric arterial embolic thrombosis, mesenteric venous thrombosis and non-occlusive mesenteric ischemia.1 The clinical picture is nonspecific.
Figure 1. Vascular anatomy of acute mesenteric isch- emia. Modified from reference 36.
Figure 2. Pathophysiology of acute mesenteric isch- emia. Modified from reference 30.
The atheroma plaques are typically found in the first 2.5 from the origin of the superior mesenteric artery
Inferior pancreaticoduodenal artery
Middle colic artery
Right colic artery
Ileocolic artery
Jejunal branches
Straight vessels
Motta-Ramírez GA et al. Acute mesenteric ischemia
Tables 1 and 312 and Figures 1 and 2. Some authors have called it “acute mesentery artery syndrome”13 and in our hospital the term mes- enteric stroke is used, which we try to include and recognize as acute mesenteric ischemia in the current paper, referring to the symptoms that most frequently are associated to this disease:
1. In the initial phase, hyperperistalsis, charac- terized by rapid intestinal transit, with severe abdominal pain syndrome and no clinical correlation with other abdominal diseases, diffuse, and location can be related to the ischemic site; for example, if it is found in the anterior bowel: periumbilical; middle bowel:
Table 2. Bowel regions, irrigation and collateral connections
Region Irrigation Collateral connections
Celiac artery Pancreatoduodenal arteries and distally the arc of Buhler
Middle bowel
Duodenal region of the ampulla of Vater to the splenic flexure of colon
Superior mesenteric artery
Pancreatoduodenal arteries and proximally the arc of Buhler, marginal artery of Drummond and the arc of Riolan
Posterior bowel
Splenic flexure to the distal portion of the sigmoid colon
Inferior mesenteric artery
Marginal artery of Drummond and the proximal arc of Riolan. Distally, superior and middle hemorrhoidal arteries
Cloacal origin Branches of the infe- rior hypogastric artery
Proximally the superior and middle hemorrhoidal arteries
Table 3. Clinical features and CT findings in mesenteric ischemia
Features Arterial occlusion Venous occlusion Non occlusive
Incidence 60-70% of AMI 5-10% of AMI 20% AMI
Onset Acute Subacute Acute or subacute
Risk factors Arrythmia, myocardial infarc- tion, valvular disase, athero- sclerosis, prolonged hyper- tension
Portal hypertension, venous hypercoagulopathy, right heart failure
Hipovolemia, low heart out- put, digoxin, hypotension, alpha adrenergic agonists
Abdominal wall Thin, unchanged or thickened with reperfusion
Thickened Unchanged or thickened with perfusion
Attenuation of the abdominal wall in simple phase
Not characteristic Low with edema; high with bleeding
Not characteristic
Reduced, absent, in target or high with reperfusion
Reduced, absent, in target or increased
Reduced, absent, with heter- ogenous distribution
Intestinal dilatation Not evident Moderate to prominent Not evident
Mesenteric vessels Defect or defects in arteries, arterial occlusion, SMA diam- eter > SMV
Defect or defects in veins, congestive veins
No defects, arterial constric- tion
Mesentery Homogenous until an infarc- tion occurs
Heterogenous with ascites Homogenous until an infarc- tion occurs
SMA: superior mesenteric artery; AMI: acute mesenteric ischemia; SMV: superior mesenteric vein.
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infraumbilical; posterior bowel: pelvic; pain does not increase with palpation and is not associated with abdominal stiffness. It is accompanied by nausea, vomiting (75% and abdominal distention (25%).8,13-16
2. All this makes an early diagnosis of this condition difficult because of the similarity to other intra-abdominal processes.
Laboratory tests
They can be useful in the diagnosis of acute mesenteric ischemia, but only in its late stage. Total leukocyte count above 20 000 may be useful, with 80% sensitivity and 50% specific- ity, metabolic acidosis (38% sensitivity, 84% specificity) and high D dimer (40% sensitivity, 89% specificity).5 It has also been shown that low lactate concentrations can help to rule out the possibility of acute mesenteric ischemia and avoid unnecessary laparotomies, especially in elderly patients. Enzymes such as creatinine kinase, lactate dehydrogenase (LDH) and alka- line phosphatase may be useful in the diagnosis of a transmural infarction, but they have low sensitivity in early stages of acute mesenteric ischemia.2,5 In current times, the role of labora- tory markers in acute mesenteric ischemia is limited.5 Table 3.12 Lactate dehydrogenase has been said to be a marker that suggests acute mesenteric ischemia;17 it originates from bacteria such as Escherichia coli in the intestinal luman. The hypothesis is that concentrations are in- creased during acute mesenteric ischemia due to bacterial translocation and bacterial overgrowth after a lesion in the intestinal mucosa. However, in a recent review, sensitivity and specificity of lactate dehydrogenase proved to be only 0.82 y 0.48, respectively.17 Table 4.18
Imaging studies
A simple X-ray can be normal in up to 25% of cases5-7 with nonspecific findings in 50% and,
in the remaining 25%, it is feasible to identify, 12 hours after the initiation of acute mesenteric ischemia, mural digital impressions resulting from edema or bleeding, pneumatosis, pneu- mobilia and gas in the portal vein. Evaluation with positive oral contrast agent (barium) is contraindicated.1,2,5,9
Ultrasound plays a limited role in the evaluation of acute mesenteric ischemia due to the fact that an important number of patients have air disten- tion and dilated bowel loops making this imaging method technically difficult or impossible. It can be more useful in the on invasive evaluation can be more useful in patients with symptoms of chronic acute mesenteric ischemia.19 Dop- pler ultrasound can show the stenotic area, the occlusions in the celiac trunk or in the superior mesenteric artery with 92-100% sensitivity and 70-89% specificity. Doppler ultrasound is not a recommended study in patients with high suspi- cion of acute mesenteric ischemia.14,15
CT scan with intravenous contrast, called CT angiography (CTA), facilitates the diagnosis of primary acute mesenteric ischemia with 83.3% sensitivity and 95.5% specificity.1,4,5 It is con- sidered to be the method of choice to reach1,5,7-9
this diagnosis:1 it is a non invasive study, with 100% positive predictive value and a negative predictive value of 94%.14,20 Figure 3.11 Images are obtained from the lung base to the symphysis pubis with a collimation of 0.5 a 2.5 mm and a 1.0-2.0 pitch. For reconstruction, images should have sections of 0.7 mm thickness. The thinnest 1-2 mm sections, in arterial phase, will be used in the multiplanar reconstructions to evaluate the origin of the mesenteric arteries and their vari- ants. For the arterial phase, 100-150mL of IV non ionic contrast at a rate of 2-3.5 mL/s, scanning is started with 30 and 60 second delays. 21-23 The study must be multiphasic, since it is necessary to recognize indirect findings starting from the simple phase, such as vascular calcification sites, increased vascular density from clotting and in-
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Motta-Ramírez GA et al. Acute mesenteric ischemia
tramural bleeding, findings that are not possible to characterize in contrast phase.20-24 The vascular study includes images in the axial, sagittal and coronal planes, and it is important to examine 3D planes and to do volumetric reconstructions.3
When the cause for the clinical picture is the arterial occlusion, the initial response is the reversible vasodilation of the splacnic bed, that in CTA is shown as an increased attenuation of the bowel loop walls, visible in arterial as well as in venous phase.3 If the obstruction persists, a vasoconstriction may be originated that in CTA
will lead to a decreased loop enhancement, thickening of the intestinal wall, mural edema, diminished peristalsis and distended and dilated bowel loops. 3
If the acute mesenteric ischemia is caused by a venous obstruction, there will be greater mural thickness in the involved bowel loop2 with a target appearance due to the submucosal edema.
In the contrast phase, intraluminal filling defects are intentionally identified, characteristic for thrombi in mesenteric arteries and veins, em-
Figure 3. Flow chart for diagnosis and treatment approach in acute mesenteric ischemia.
Table 4. Sensitivity, specificity and odds ratio for findings in laboratory tests classically associated with acute mesenteric ischemia
Marker Sensitivity Specificity Possitive odds ratio (95% CI) Negative odds ratio (95% CI)
Leukocyte count 0.80 0.50 1.57 (1.97, 2.27) 0.41 (0.20, 0.83)
pH 0.38 0.84 2.49 (0.82, 7.51) 0.71 (0.45, 1.14)
D-dímer 0.89 0.40 1.48 (1.28, 1.71) 1.48 (1.28, 1.71)
Lactate 0.86 0.44 1.67 (1.37, 2.05) 0.20 (0.01, 2.86)
Suspicion of acute mesenteric ischemia
Peritonitis
Laparotomy
Central
CAT/CTA
endoprosthesis
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Anales de Radiología México 2015 January;14(1)
bolisms and infarctions in other organs, plus an abnormal enhancement of the intestinal wall, since acute mesenteric ischemia leads to diverse patterns of intestinal wall attenuation.25
Out of the acute mesenteric ischemia cases, 40 to 50% are arterial in origin and embolic in nature leading to a filling defect in the superior mesenteric artery, after detachment of a fragment of an atrial mural thrombus or a left ventricular thrombus.26 Other causes include: thrombosis within an atheroma plaque in the non occlusive mesenteric artery and mesenteric venous throm- bosis. Thrombosis of the superior mesenteric vein is the cause of the intestinal ischemia in less than 15% of cases. Finding a thrombus in the superior mesenteric vein is much less serious than arterial occlusion.26
Non surgical management of patients with acute mesenteric ischemia must be considered as the first treatment step and correction of risk factors that most often have been associated in different case series to this disease: atherosclerosis, heart disease, systemic hypertension, atrial fibrillation, smoking, digitalis use and obesity.1,2,6,9
When there are acute complications such as perforation, peritonitis and intestinal necrosis, the surgical approach is indicated.2 Splenic, liver or kidney infarction are findings for poor prognosis in patients with intestinal ischemia even without intestinal vascular involvement.26 These variations depend on the pathogenesis of the intestinal ischemia, duration, location and extension, collateral circulation, added infec- tions or whether it is perforated or not.
Acute mesenteric ischemia leads to different pat- terns of intestinal wall attenuation, besides the abnormal enhancement of the intestinal wall.25 The thickening of the intestinal wall may be due to different diseases and is not correlated with the severity of the intestinal ischemia.21-22,26-28
A very common finding of acute mesenteric ischemia is the thickened intestinal wall. 26 The intestinal wall has a normal thickness of 0.3 to 0.5 cm, depending on the degree of distention, so a thickened wall is not a specific finding. Nevertheless, in some series, it is the most fre- quently identified pattern and it is caused by the mural edema, bleeding or added infection of the ischemic intestinal wall. Initially, the intestinal wall becomes thinner instead of thicker because there is no arterial flow, no mural edema, nor bleeding.28 A thinner intestinal wall is due to a loss of volume in the intestinal wall vessels and to the loss of intestinal muscle tone. More than 0.3 cm is abnormal and must be evaluated in loops with maximal distention. Abnormal disten- tion, more than 3.0 cm, is also common in acute intestinal ischemia. However, both findings are nonspecific. 26 Ascites and mesenteric edema may be identified in acute mesenteric ischemia.26
Overall, at least one of the mesenteric signs is present in the patient with acute mesenteric ischemia. In all patients with acute mesenteric ischemia following arterial occlusion and in 68% of those that have non occlusive mesenteric isch- emia, the number of arterial vessels is reduced (p = 0.067). Pneumatosis in mesenteric vessels and reduction in the number of venous vessels is associated with higher mortality (p = 0.027 y p = 0.042, respectively). Reperfusion signs are associated with a reduced mortality (28.7 vs. 65.5%).29
In view of the characteristic findings and prognostic value, a thorough evaluation of the mesentery will provide additional information in the study and diagnosis of acute mesenteric ischemia using CAT scan.29
Portal pneumatosis or mesenteric venous gas are not always of intestinal origin. In most cases the gas comes from the intraluminal gas that crosses from the damaged mucosa to the intramural
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Motta-Ramírez GA et al. Acute mesenteric ischemia
space.27 The integrity of the mucosa, gas and the intestinal intraluminal pressure, as well as the bacterial flora, interact with each other in the formation of intestinal pneumatosis. Intestinal pneumatosis is highly suggestive of acute mes- enteric ischemia in symptomatic patients with a sensitivity ranging from 22 to 72%.26,27 Intestinal pneumatosis is not a diagnosis, it is a radiological finding that results from an underlying disease process. The importance of intestinal pneuma- tosis will depend on its nature and severity of the disease that causes it. Therefore, intestinal pneumatosis involves a very broad spectrum of diseases ranging from benign cause to abdominal sepsis and death.30
The identification of intestinal pneumatosis characterized by air bands and the combina- tion with portomesenteric venous gas in the CTA is associated with transmural intestinal infarction. On the other hand, the isolated identification of intestinal pneumatosis mainly characterized by bubbles or portomesenteric venous gas in the CTA may be related to a partial intestinal mural ischemic event, which happens in 1/3 of cases. Also, even though in acute mesenteric ischemia the identification of portomesenteric venous gas in the CTA is associated with a 56% mortality rate, this asso-…