- Email: [email protected]
Role of multidetector CT angiography in the evaluation of suspected mesenteric ischemia
European Journal of Radiology 80 (2011) e582–e587
Contents lists available at SciVerse ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Role of multidetector CT angiography in the evaluation of suspected mesenteric ischemia Meghna Barmase a , Mandeep Kang a,∗ , Jaidev Wig b , Rakesh Kochhar c , Rajesh Gupta b , Niranjan Khandelwal a a
Department of Radiodiagnosis and Imaging, Postgraduate Institute of Medical Education and Research, Chandigarh 160012, India Department of General Surgery, Postgraduate Institute of Medical Education and Research, Chandigarh 160012, India c Department of Gastro-enterology, Postgraduate Institute of Medical Education and Research, Chandigarh 160012, India b
a r t i c l e
i n f o
Article history: Received 19 May 2010 Received in revised form 11 August 2011 Accepted 19 September 2011 Keywords: Multidetector row CT Mesenteric ischemia CT angiography
a b s t r a c t Objective: To assess the role of multidetector CT angiography (MDCTA) in the diagnosis of acute mesenteric ischemia (AMI) and to compare the diagnostic utility of axial images with reconstructed images. Materials and methods: In this Institute Review Board approved prospective study, MDCTA was performed on 31 patients who presented with the clinical suspicion of AMI (25M; 6F, age range: 16–73 years). Axial and reconstructed images of each patient were evaluated independently by two radiologists for evidence of bowel wall thickening, abnormal mucosal enhancement, bowel dilatation or obstruction, mesenteric stranding, ascites, solid organ infarcts, pneumatosis intestinalis or porto-mesenteric gas, and mesenteric arterial or venous occlusion. MDCT findings were correlated with the surgical findings and clinical outcome. Patients were later divided into two groups: a study group of patients with proven AMI and a control group of patients with an alternate diagnosis, for the purpose of statistical analysis. Results: AMI was correctly diagnosed in all 16 patients on MDCTA (100% sensitivity and specificity) of whom nine patients underwent surgical exploration. Three patients expired before surgery and the remaining 5 patients were proven based on positive clinical and laboratory findings. Mesenteric arterial occlusion was seen in 7 patients while 5 patients had portomesenteric venous thrombosis. Reconstructed images using minimum intensity projection, volume rendering and multiplanar volume reconstruction were found to perform better for the detection of vascular abnormalities and improved the diagnostic confidence of both radiologists in the evaluation of bowel and mesenteric abnormalities. Conclusion: MDCTA is an effective non-invasive modality for the diagnosis of mesenteric ischemia. © 2011 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Mesenteric ischemia (MI) is a complex disorder which occurs in a variety of conditions which result in insufficient blood supply to the small or large bowel. It can cause a catastrophic fatal event with mortality rates ranging from 59% to 93% reported in literature [1]. The clinical presentation of AMI is nonspecific. Patients may complain of intense abdominal pain [2]. Blood levels of lactic acid may be elevated, as may the white blood cell count and sedimentation rate [3]. However, there are no laboratory tests that definitively diagnose acute mesenteric ischemia. The therapeutic approach to bowel infarction consists of surgical resection [4], however performing an exploratory laparotomy for any patient suspected of having AMI has its attendant
∗ Corresponding author. Tel.: +91 172 2756382; fax: +91 172 2745768. E-mail addresses: [email protected], [email protected] (M. Kang). 0720-048X/$ – see front matter © 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2011.09.015
morbidity and mortality. Catheter angiography is unequivocally the gold standard imaging modality for the evaluation of AMI. It can localize the site of occlusion and differentiate between thrombotic, embolic and non occlusive etiologies [5]. However, it is invasive, expensive and time consuming. Color doppler examination of the mesenteric circulation is helpful but may be technically difficult in imaging the mesenteric vessels in patients with AMI due to bowel gas [6]. The introduction of spiral Computed Tomography (CT) improved the ability of CT to image the mesenteric vessels and the bowel wall but it still was not sensitive (64%) for the early detection of AMI [7]. MDCT offers distinct advantages over traditional spiral CT for imaging the mesenteric vasculature. It allows acquisition of near isotropic volumetric data which allows exquisite 2 dimensional reformatted images (2D) and 3 dimensional (3D) reconstructions of the mesenteric vasculature and bowel which improve the ability to diagnose AMI [8]. This prospective study (approved by the Institute Review Board) was designed to assess the diagnostic efficacy of MDCT angiography in the evaluation of patients with the clinical suspicion of
M. Barmase et al. / European Journal of Radiology 80 (2011) e582–e587
mesenteric ischemia. The diagnostic utility of axial images vis-a-vis 3D reconstructed images including maximum intensity projections (MIP), multiplanar reconstruction (MPR) and volume rendered (VR) images were also compared. 2. Materials and methods The study group consisted of 31 consecutive patients who presented with clinical signs or symptoms suspicious for mesenteric ischemia. All patients who presented with severe abdominal pain out of proportion to clinical findings or patients with biochemical evidence of ischemia, such as elevated lactate levels or unexplained metabolic acidosis were included in the study group. Risk factors for ischemia, such as previous history of mesenteric ischemia or symptoms of chronic ischemia, severe vascular disease, atrial fibrillation without therapeutic anticoagulation, low flow (a history of hypotension or vasopressor therapy) or hypercoagulable states were also taken into consideration. Patients with clinical or laboratory suggestion of other causes of abdominal pain were not included in the study group. Patients with deranged renal parameters or a history of contrast allergy were also excluded. After informed consent was obtained, 31 patients, including 25 men (age range: 17–73 years; mean: 45 years) and 6 women (age range: 16–63 years; mean: 39 years) underwent MDCT angiography. No procedural complications were encountered. 2.1. Imaging and image evaluation All scans were performed on a multidetector CT (Sensation 16, Seimens, Erlangen, Germany) in the arterial and venous phases. Patients were kept fasting for 4–6 h before the scan. Plain water was used as negative oral contrast for distending the bowel loops (1000–1500 ml administered over 45 min). After insertion of an 18 gauge cannula into an antecubital vein, 100–120 ml of non-ionic iodinated contrast material (350 mg/ml) was injected at a rate of 4 ml/s using a pressure injector. A bolus tracking software (C.A.R.E Bolus, Siemens) was used to trigger scan initiation with the region of interest (ROI) placed over the abdominal aorta at L1 level with a threshold attenuation of 100 HU. Arterial phase images were acquired from L1 till the pubic symphysis. This was followed by the portal venous phase acquired at 60–70 s from the time of start of contrast injection from the domes of diaphragm till the pubic symphysis. Data was acquired at 5 mm scan thickness at a pitch of 0.75 which was reconstructed to overlapping sections of 1 mm. The scan voltage used was 120 kVp with a tube current of 200–250 mA. All scans were reviewed and analyzed on a separate workstation (Wizard, Siemens). 2D and 3D reconstructions including MPVR, VR and MIP images were generated. CT scans were evaluated for evidence of bowel wall thickening (>3 mm in noncollapsed small or large bowel perpendicular to the transverse plane), focal mucosal enhancement, focal lack of bowel wall enhancement, bowel dilatation (small-bowel diameter >2.5 cm or colon diameter >8 cm), bowel obstruction (bowel dilatation with evidence of a transition point and collapsed bowel distally), mesenteric stranding, ascites, solid organ infarction, free intraperitoneal air, pneumatosis intestinalis, superior mesenteric or portal venous gas, superior mesenteric or portal venous thrombosis and mesenteric arterial occlusion (thrombosis or embolus). All patients of suspected AMI who underwent MDCT angiography, were kept on close follow-up till the final diagnosis was confirmed by clinical, surgical and/or histopathological findings. The axial and reconstructed images of each patient were analyzed separately by two independent radiologists. The first radiologist reviewed the scan just after acquisition. The urgency of the clinical situation and logistic limitations made it impossible
e583
for both radiologists to review the study prior to issuing of primary report. The second radiologist reviewed the images after the patient left the department, but was blinded to the first radiologist’s interpretation. The prospective data collected at that time was used for the statistical analyses. The patients were divided into a study group composed of patients with proven AMI and a control group composed of patients with a final diagnosis that did not include AMI. 2.2. Statistical analysis The sensitivity, specificity, positive predictive values, negative predictive values and accuracy of each individual CT finding for each observer were calculated. The interobserver agreement for the detection of CT findings between the two radiologists was calculated using Kappa statistics. A Kappa statistic greater than 0.75 was considered as excellent agreement, 0.4–0.75 as fair to good agreement and less than 0.4 as poor agreement. 3. Results MDCT angiography diagnosed mesenteric ischemia in 16 patients of which nine patients underwent surgery. Three patients collapsed and expired before surgery. Mesenteric ischemia was confirmed in the remaining 5 patients by positive clinical and laboratory findings, these cases were managed conservatively and recovered. CT also provided a definitive alternate diagnosis in the 15 patients who did not have mesenteric ischemia, which was later proved on the basis of laboratory values, clinical and surgical findings (Table 1). Four patients [pancreatitis (n = 1), inflammatory colitis (n = 1) and diverticulitis (n = 2)] underwent surgery. No evidence of mesenteric ischemia was seen on CT or surgery in these patients. An ascitic tap confirmed the CT diagnosis of tubercular peritonitis and the patient recovered on anti-tubercular treatment. One patient with adenocarcinoma of colon had unresectable disease and received only palliative therapy. Thrombolytic therapy was given to the patients with aortic thrombosis (n = 1) and inferior vena cava thrombosis (n = 1). One patient with hepatic artery pseudoaneurysm was treated with percutaneous thrombin injection, following which there was no episode of malena. Two patients with ureteric calculus (n = 1) and cystic adnexal mass (n = 1) were managed conservatively. Vascular abnormalities were demonstrated in 15 patients of mesenteric ischemia. Atherosclerotic disease causing luminal compromise of the aorta/superior mesenteric artery (SMA)/celiac axis was seen in 6 of these patients. Mesenteric arterial occlusion was seen in 7 patients (43.7%). Three of these cases showed thrombotic occlusion of celiac trunk/SMA just beyond the origin from aorta Table 1 Patients with alternative diagnosis (control group). S. No.
Alternative diagnosis in patients without AMI
No. of patients [n = 15]
1 2 3 4 5 6 7 8 9 10 11 12 13
Diverticulitis Inflammatory colitis Adenocarcinoma colon Pancreatitis Portal vein/SMV thrombosis Inferior vena cava thrombosis Nephrolithiasis Tubercular peritonitis Cystic adnexal mass Perforation peritonitis Extra hepatic portal vein obstruction Hepatic artery pseudoaneurysm Aortic thrombosis
02 02 01 01 01 01 01 01 01 01 01 01 01
e584
M. Barmase et al. / European Journal of Radiology 80 (2011) e582–e587
Fig. 1. 58 year old male patient with pain abdomen and malena. MDCT angiography. (A) Coronal MPR image: the small bowel loops are dilated with thinned out walls and gross band like pneumatosis. Air is also seen in the mesenteric veins and the portal radicles in the liver. Note the irregular, non-enhancing areas in the periphery of the liver due to infarcts. (B) Sagittal MIP image shows complete occlusion of the proximal superior mesenteric artery by thrombus. This patient expired before surgery.
(Fig. 1), while three cases showed thrombosis of the horizontal part of SMA. In one case the mid SMA was completely occluded from 3.5 cm beyond its origin with extension of the thrombus into segmental branches as well (Fig. 2). One patient with mild ostial stenosis of the SMA showed an eccentric filling defect consistent with embolus at the second branching point of the SMA (Fig. 3). Another patient with no evidence of atherosclerotic disease of the aorta or mesenteric vessels showed an eccentric filling defect (embolus) in a branch vessel with an abrupt change in luminal caliber. Five patients with AMI had evidence of venous thrombosis (31%). Two of these patients had thrombosis of both the portal vein and SMV (Fig. 4). Two other patients showed thrombosis of portal vein, SMV and splenic vein with extension into small mesenteric branches (Fig. 5). One patient with midgut volvulus had secondary
compression of the mesenteric vessels leading to ischemic changes in the bowel loops. One patient of AMI showed no abnormalities in the mesenteric vasculature. The kappa statistics for the various individual CT findings of bowel ischemia showed excellent agreement between the two observers, except for the presence of mesenteric arterial stenosis (0.716) and mesenteric arterial embolus (0.652). The initial disagreements between the two radiologists were resolved by consensus review. The individual sensitivity, specificity, positive predictive value, negative predictive value and accuracy of the individual CT findings are depicted in Table 2. Mesenteric congestion, ascites, luminal dilatation and bowel wall thickening were the most common CT features noted in patients with AMI, however these were found to
Fig. 2. 40 year old male patient with two episodes of malena. MDCT angiography. (A) Sagittal MIP image shows stenosis of the proximal celiac trunk with complete occlusion of the mid SMA with nonfilling of the branches. (B) Ischemic bowel loops are thin walled and show lack of enhancement. Also note the paucity of mesenteric vessels.
M. Barmase et al. / European Journal of Radiology 80 (2011) e582–e587
e585
Fig. 3. 60 year old female patient presented with acute pain in abdomen. CT angiography. (A) Axial image: SMA shows an eccenteric filling defect suggestive of embolus. Small bowel loops show lack of mural enhancement. (B) VR image better depicts the embolus at a branch point in the SMA with distal reformation (arrow).
Fig. 4. 58 year old male patient with acute pain in abdomen. CT angiography abdomen, venous phase images. (A) There is dilatation with diffuse mural thickening of small bowel loops with a striated pattern giving a target appearance. Note the increased density with congestion of the subtending mesentery. (B) A large hypodense filling defect is seen in the superior mesenteric vein (arrow) as the cause of mesenteric ischemia.
Fig. 5. 39 year old female patient with abdominal distention and pain. MDCT angiography venous phase data. (A) Coronal MIP image shows extensive thrombosis of portal vein and SMV. Multiple collaterals are seen at the porta and in gastrohepatic ligament. Small calcific specks are seen involving the wall of SMV. Thick walled, mildly dilated jejunal loops are seen. (B) Axial image shows small foci of intramural air in the dependent part of jejunal loop suggestive of pneumatosis intestinalis.
e586
M. Barmase et al. / European Journal of Radiology 80 (2011) e582–e587
Table 2 CT findings in the two study groups. CT findings
Pts with MI (N = 16)
Control group (N = 15)
Sensitivity (%)
Specificity (%)
Positive predictive value (%)
Negative predictive value (%)
Accuracy (%)
Mortality (N = 9) (%)
Bowel wall thickening Bowel wall stratification Lack of mural enhancement Abnormal mural enhancement Mesenteric congestion/fluid Luminal dilatation Pneumatosis intestinalis Ascites Solid organ infarcts Mesenteric arterial thrombosis Mesenteric arterial stenosis Mesenteric arterial embolus Venous occlusion
9 8 7 7 12 13 5 13 4 7 5 2 5
7 3 1 2 7 2 0 8 3 1 1 0 2
56.25 50 43.75 43.75 75 81.25 31.25 81.25 25 18.75 31.25 12.5 31.25
53.33 80 93.33 80.00 53.33 86.67 100 46.67 80 93.37 93.33 100 86.67
56.35 72.73 87.5 70.00 43.16 86.67 100 61.90 57.14 18.75 83.33 100 71.43
53.33 60 60.87 57.14 66.67 81.25 57.69 70 50 51.85 56.00 51.7 54.17
54.83 64 67 61.29 64.5 83.87 64.51 64 51 54.84 61.29 54.8 58.06
55.55
Table 3 Comparison of axial and 2D/3D reconstructed images.
55.5 55.5 77.7 55.5 33.3 66
22.2
4. Discussion
CT findings
MIP/MPVR
VR
Axial
Bowel wall thickening Lack of enhancement Abnormal enhancement Mesenteric congestion/fluid Luminal dilatation Pneumatosis intestinalis Mesenteric arterial occlusion Mesenteric arterial stenosis Mesenteric arterial embolus Mesenteric venous occlusion Extent/degree of vascular abnormality
++ +++ +++ +++ +++ +++ +++ +++ +++ +++ +++
– – – – – – +++ +++ +++ ++ +++
++ ++ ++ ++ ++ +++ + + + +++ –
“–” not visualized; “+” to “+++” correspond to poor, fair, and excellent visualization.
have low specificity. The presence of solid organ infarcts, including that of liver (n = 2) and spleen (n = 2) were found to be highly specific in diagnosing AMI. The CT findings of mesenteric arterial occlusion, mesenteric venous occlusion, and lack of mural enhancement or abnormal mural enhancement and pneumatosis intestinalis were found to be most specific for bowel ischemia. Using these diagnostic criteria, AMI could be diagnosed with a sensitivity of 40.6%, specificity of 96.6%, positive predictive value of 92.85% and negative predictive value of 60.41%. The individual CT findings suggestive of bowel ischemia were compared on the axial images and 2D/3D data sets (MIP, MPVR, and VR). Mesenteric arterial occlusion (thrombotic or embolic), mesenteric arterial stenosis and venous occlusion were very well depicted on the reconstructed data set. Bowel and mesenteric abnormalities were also better seen on 3D images as compared to the axial data (Table 3). Two cases of celiac axis stenosis and one case of mesenteric arterial embolus were missed on the axial data but were diagnosed on the reformatted images (MIP and VR). Reconstructed images also improved the diagnostic confidence of both radiologists while evaluating the extent and degree of vascular involvement. 3.1. Patient outcomes In the present study mesenteric ischemia was associated with a high mortality (n = 9, 56.2%) and morbidity. Patients with arterial occlusive disease, luminal dilatation, lack of bowel wall enhancement, abnormal enhancement, pneumatosis intestinalis and solid organ infarcts were found to have a poor outcome. All patients with pneumatosis or solid organ infarcts and 5 of 7 patients with arterial occlusion (75%) had a fatal outcome.
AMI is one of the most challenging clinical conditions because of its high mortality rate (50–90%) and difficulty in diagnosis [1,9,10]. Catheter angiography was considered the gold standard but it is invasive, time consuming and difficult to perform with limited availability in select centres. Secondly, mesenteric venous ischemia is not reliably diagnosed on catheter angiography [5]. MDCT, with its wide availability and fast acquisition is a good diagnostic alternative. In the present study the mortality of patients with AMI was 56.2%. Eight of these patients had luminal dilatation (88%), six patients (66.6%) had arterial occlusive disease, and two patients had venous occlusion (22.2%), while one patient showed no evidence of any mesenteric vascular abnormality. All patients with pneumatosis intestinalis and solid organ infarcts died. Yamada et al. in their study on AMI showed that patients with presence of bowel dilatation or abnormal gas in the bowel wall or portal system were proved to have a wider extent of ischemia on surgery and hence a poorer outcome [11]. In the present study, mesenteric arterial occlusion due to thrombosis of the proximal SMA was found to be the most common cause of AMI (43.7%) while emboli in the SMA were seen in 12.4% (n = 2) of patients. Venous thrombosis is an important, but less common cause of AMI seen in 5–15% of cases of mesenteric ischemia and infarction. The majority of patients with venous occlusion show bowel wall thickening, luminal dilatation and abnormal mucosal enhancement [4,12]. Venous thrombosis was seen in four cases of AMI, none of these patients had a prior history of hypercoagulable state. All of these patients showed bowel wall thickening, mural stratification, luminal dilatation and mesenteric congestion. Conversely we also had one patient of venous occlusion who had frank bowel necrosis and pneumatosis, a rare finding in venous ischemia. Nonocclusive mesenteric ischemia usually accounts for 20–30% of cases of AMI and occurs when there is hypoperfusion from low cardiac output [4]. In the present study we had two patients in congestive cardiac failure with low cardiac output. One of these patients was a case of Ebstein’s anomaly with evidence of diffuse mesenteric ischemia, while the second patient showed evidence of inferior vena cava thrombosis with no bowel changes. Bowel wall thickening is the least specific CT finding in cases of acute bowel ischemia, as it is observed in a variety of nonischemic conditions [13]. In the present study, bowel wall thickening was seen in nine patients of mesenteric ischemia and in seven patients without ischemia. These included two patients with diverticulitis, one patient each of pancreatitis, inflammatory colitis, tubercular peritonitis, adenocarcinoma colon and a patient of extra hepatic portal vein obstruction with portal cavernoma.
M. Barmase et al. / European Journal of Radiology 80 (2011) e582–e587
Portomesenteric gas resulting from bowel ischemia has been shown to have a poor prognosis with a mortality rate of 75–90% [14]. In the present study the sensitivity and specificity of pneumatosis intestinalis for diagnosing AMI was 31.25% and 100% which is similar to the sensitivity of 36% and specificity of 100% reported by Aschoff et al. [15]. The unenhanced segments of bowel wall, a finding more commonly observed in the patients with arterial occlusion was shown to have a specificity of 100% for ischemia in the series reported by Zalcman et al. [16]. In the present study, mesenteric arterial thrombosis was seen in seven patients of AMI. Lack of bowel wall enhancement was noted in 6 of these patients (85.7%) with an overall sensitivity and specificity of 43.75% and 93.33%. The presence of mesenteric congestion, mesenteric fat stranding or fluid was found to have a very high sensitivity but a low specificity as stated by many authors in the past [7,9,15]. By using a combination of the following diagnostic criteria: mesenteric arterial thrombosis, mesenteric venous occlusion, pneumatosis intestinalis and lack of bowel wall enhancement, we could diagnose AMI with a sensitivity of 40.6% and specificity of 96.6%. The most widely used techniques of reconstruction in the diagnosis of suspected bowel ischemia are VR, MIP, and MPR. Horton and Fishman stated that when evaluating the mesenteric vessels they typically preferred using VR, although MIP was valuable for the visualization of tiny branch vessels [17]. Kirkpatrick et al. found that MIP reconstructions were easier and faster to obtain, but were subject to artefacts caused by vascular calcification. There is also potential for less accurate estimation of stenosis with increasing slab thickness. Volume rendered images, which required more time to construct gave superior three-dimensional spatial relationship of vessels [1]. We compared the axial images with the 3D reconstructed data for the assessment of vascular, bowel and mesenteric abnormalities. We encountered no vascular abnormality that could not be appreciated on 3D reconstructions. It was noted that the extent of vascular abnormalities, arterial narrowing and kinking were better seen on 3D reformatted images. The diagnostic accuracy as well as level of confidence of both observers was better when MIP and VR reconstructed images were used. The bowel changes were better seen on reconstructed images in 9 out of 16 patients of MI. It was also found that the 3D reconstructed images showed better demarcation of affected ischemic bowel from the segment of uninvolved bowel in three patients of ischemia. Mesenteric congestion and vascularity were equally well seen on both 3D reformatted and axial images.
e587
5. Conclusion Biphasic MDCT angiography is an excellent, fast and noninvasive modality for the diagnosis of bowel ischemia, as it can visualize both the bowel and mesenteric changes as well as accurately depict the mesenteric vasculature. The combination of both axial and 3D reconstructed images increases the diagnostic confidence of the interpreting radiologist. Conflict of interest None of the authors have any conflict of interest or any financial disclosures to be made. References [1] Kirkpatrick ID, Kroeker MA, Greenberg HM. Biphasic CT with mesenteric CT angiography in the evaluation of acute mesenteric ischemia: initial experience. Radiology 2003;229(1):91–8. [2] Stoney RJ, Cunningham CG. Acute mesenteric ischemia. Surgery 1993;114:489–90. [3] May LD, Berenson MM. Value of serum inorganic phosphate in the diagnosis of ischemic bowel disease. Am J Surg 1983;146:266–8. [4] Park WM, Gloviczki P, Cheny KJ, et al. Contemporary management of acute mesenteric ischemia: factors associated with survival. J Vasc Surg 2002;35(3):445–52. [5] Bakal CW, Spraygen S, Wolf EL. Radiology in intestinal ischaemia: angiographic diagnosis and management. Surg Clin North Am 1992;72(1):125–41. [6] Hermsen K, Chong WK. Ultrasound evaluation of abdominal aortic and iliac aneurysms and mesenteric ischemia. Radiol Clin North Am 2004;42(2):365–81. [7] Taourel PG, Deneuville H, Pradel JA, Regent D, Bruel JM. Acute mesenteric ischemia: diagnosis with contrast enhanced CT. Radiology 1996;199(3):632–6. [8] Horton KM, Fishman EK. Multidetector row CT of mesenteric ischemia: can it be done? Radiographics 2001;21(6):1463–73. [9] Wiesner W, Khurana B, Ji H, et al. CT of acute bowel ischemia. Radiology 2003;226(3):635–50. [10] Inderbitzi R, Wagner HE, Seiler C, et al. Acute mesenteric ischemia. Eur J Surg 2004;158:123–6. [11] Yamada K, Saeki M, Yamaguchi T, et al. Acute mesenteric ischemia, CT and plain radiographic analysis of 26 cases. Clin Imaging 1998;22(1):34–41. [12] Kim JY, Ha HK, Byun JY, et al. Intestinal infarction secondary to mesenteric venous thrombosis: CT-pathologic correlation. J Comput Assist Tomogr 1993;17(3):382–5. [13] Levy AD. Mesenteric ischaemia. Radiol Clin North Am 2007;45(3):593–9. [14] Sebastia C, Quiroga S, Espin EC, et al. Portomesenteric vein gas: pathologic mechanisms, CT findings, and prognosis. Radiographics 2000;20(5):1213–24. [15] Aschoff AJ, Stuber G, Becker BW, et al. Evaluation of acute mesenteric ischemia: accuracy of biphasic mesenteric multi-detector CT angiography. Abdom Imaging 2008;34:345–57. [16] Zalcman M, Sy M, Donckier V, et al. Helical CT signs in the diagnosis of intestinal ischemia in small-bowel obstruction. AJR Am J Roentgenol 2000;175(6):1601–7. [17] Horton KM, Fishman EK, Multidetector. CT angiography in the diagnosis of mesenteric ischemia. Radiol Clin North Am 2007;45(2):275–88.
Contents lists available at SciVerse ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Role of multidetector CT angiography in the evaluation of suspected mesenteric ischemia Meghna Barmase a , Mandeep Kang a,∗ , Jaidev Wig b , Rakesh Kochhar c , Rajesh Gupta b , Niranjan Khandelwal a a
Department of Radiodiagnosis and Imaging, Postgraduate Institute of Medical Education and Research, Chandigarh 160012, India Department of General Surgery, Postgraduate Institute of Medical Education and Research, Chandigarh 160012, India c Department of Gastro-enterology, Postgraduate Institute of Medical Education and Research, Chandigarh 160012, India b
a r t i c l e
i n f o
Article history: Received 19 May 2010 Received in revised form 11 August 2011 Accepted 19 September 2011 Keywords: Multidetector row CT Mesenteric ischemia CT angiography
a b s t r a c t Objective: To assess the role of multidetector CT angiography (MDCTA) in the diagnosis of acute mesenteric ischemia (AMI) and to compare the diagnostic utility of axial images with reconstructed images. Materials and methods: In this Institute Review Board approved prospective study, MDCTA was performed on 31 patients who presented with the clinical suspicion of AMI (25M; 6F, age range: 16–73 years). Axial and reconstructed images of each patient were evaluated independently by two radiologists for evidence of bowel wall thickening, abnormal mucosal enhancement, bowel dilatation or obstruction, mesenteric stranding, ascites, solid organ infarcts, pneumatosis intestinalis or porto-mesenteric gas, and mesenteric arterial or venous occlusion. MDCT findings were correlated with the surgical findings and clinical outcome. Patients were later divided into two groups: a study group of patients with proven AMI and a control group of patients with an alternate diagnosis, for the purpose of statistical analysis. Results: AMI was correctly diagnosed in all 16 patients on MDCTA (100% sensitivity and specificity) of whom nine patients underwent surgical exploration. Three patients expired before surgery and the remaining 5 patients were proven based on positive clinical and laboratory findings. Mesenteric arterial occlusion was seen in 7 patients while 5 patients had portomesenteric venous thrombosis. Reconstructed images using minimum intensity projection, volume rendering and multiplanar volume reconstruction were found to perform better for the detection of vascular abnormalities and improved the diagnostic confidence of both radiologists in the evaluation of bowel and mesenteric abnormalities. Conclusion: MDCTA is an effective non-invasive modality for the diagnosis of mesenteric ischemia. © 2011 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Mesenteric ischemia (MI) is a complex disorder which occurs in a variety of conditions which result in insufficient blood supply to the small or large bowel. It can cause a catastrophic fatal event with mortality rates ranging from 59% to 93% reported in literature [1]. The clinical presentation of AMI is nonspecific. Patients may complain of intense abdominal pain [2]. Blood levels of lactic acid may be elevated, as may the white blood cell count and sedimentation rate [3]. However, there are no laboratory tests that definitively diagnose acute mesenteric ischemia. The therapeutic approach to bowel infarction consists of surgical resection [4], however performing an exploratory laparotomy for any patient suspected of having AMI has its attendant
∗ Corresponding author. Tel.: +91 172 2756382; fax: +91 172 2745768. E-mail addresses: [email protected], [email protected] (M. Kang). 0720-048X/$ – see front matter © 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2011.09.015
morbidity and mortality. Catheter angiography is unequivocally the gold standard imaging modality for the evaluation of AMI. It can localize the site of occlusion and differentiate between thrombotic, embolic and non occlusive etiologies [5]. However, it is invasive, expensive and time consuming. Color doppler examination of the mesenteric circulation is helpful but may be technically difficult in imaging the mesenteric vessels in patients with AMI due to bowel gas [6]. The introduction of spiral Computed Tomography (CT) improved the ability of CT to image the mesenteric vessels and the bowel wall but it still was not sensitive (64%) for the early detection of AMI [7]. MDCT offers distinct advantages over traditional spiral CT for imaging the mesenteric vasculature. It allows acquisition of near isotropic volumetric data which allows exquisite 2 dimensional reformatted images (2D) and 3 dimensional (3D) reconstructions of the mesenteric vasculature and bowel which improve the ability to diagnose AMI [8]. This prospective study (approved by the Institute Review Board) was designed to assess the diagnostic efficacy of MDCT angiography in the evaluation of patients with the clinical suspicion of
M. Barmase et al. / European Journal of Radiology 80 (2011) e582–e587
mesenteric ischemia. The diagnostic utility of axial images vis-a-vis 3D reconstructed images including maximum intensity projections (MIP), multiplanar reconstruction (MPR) and volume rendered (VR) images were also compared. 2. Materials and methods The study group consisted of 31 consecutive patients who presented with clinical signs or symptoms suspicious for mesenteric ischemia. All patients who presented with severe abdominal pain out of proportion to clinical findings or patients with biochemical evidence of ischemia, such as elevated lactate levels or unexplained metabolic acidosis were included in the study group. Risk factors for ischemia, such as previous history of mesenteric ischemia or symptoms of chronic ischemia, severe vascular disease, atrial fibrillation without therapeutic anticoagulation, low flow (a history of hypotension or vasopressor therapy) or hypercoagulable states were also taken into consideration. Patients with clinical or laboratory suggestion of other causes of abdominal pain were not included in the study group. Patients with deranged renal parameters or a history of contrast allergy were also excluded. After informed consent was obtained, 31 patients, including 25 men (age range: 17–73 years; mean: 45 years) and 6 women (age range: 16–63 years; mean: 39 years) underwent MDCT angiography. No procedural complications were encountered. 2.1. Imaging and image evaluation All scans were performed on a multidetector CT (Sensation 16, Seimens, Erlangen, Germany) in the arterial and venous phases. Patients were kept fasting for 4–6 h before the scan. Plain water was used as negative oral contrast for distending the bowel loops (1000–1500 ml administered over 45 min). After insertion of an 18 gauge cannula into an antecubital vein, 100–120 ml of non-ionic iodinated contrast material (350 mg/ml) was injected at a rate of 4 ml/s using a pressure injector. A bolus tracking software (C.A.R.E Bolus, Siemens) was used to trigger scan initiation with the region of interest (ROI) placed over the abdominal aorta at L1 level with a threshold attenuation of 100 HU. Arterial phase images were acquired from L1 till the pubic symphysis. This was followed by the portal venous phase acquired at 60–70 s from the time of start of contrast injection from the domes of diaphragm till the pubic symphysis. Data was acquired at 5 mm scan thickness at a pitch of 0.75 which was reconstructed to overlapping sections of 1 mm. The scan voltage used was 120 kVp with a tube current of 200–250 mA. All scans were reviewed and analyzed on a separate workstation (Wizard, Siemens). 2D and 3D reconstructions including MPVR, VR and MIP images were generated. CT scans were evaluated for evidence of bowel wall thickening (>3 mm in noncollapsed small or large bowel perpendicular to the transverse plane), focal mucosal enhancement, focal lack of bowel wall enhancement, bowel dilatation (small-bowel diameter >2.5 cm or colon diameter >8 cm), bowel obstruction (bowel dilatation with evidence of a transition point and collapsed bowel distally), mesenteric stranding, ascites, solid organ infarction, free intraperitoneal air, pneumatosis intestinalis, superior mesenteric or portal venous gas, superior mesenteric or portal venous thrombosis and mesenteric arterial occlusion (thrombosis or embolus). All patients of suspected AMI who underwent MDCT angiography, were kept on close follow-up till the final diagnosis was confirmed by clinical, surgical and/or histopathological findings. The axial and reconstructed images of each patient were analyzed separately by two independent radiologists. The first radiologist reviewed the scan just after acquisition. The urgency of the clinical situation and logistic limitations made it impossible
e583
for both radiologists to review the study prior to issuing of primary report. The second radiologist reviewed the images after the patient left the department, but was blinded to the first radiologist’s interpretation. The prospective data collected at that time was used for the statistical analyses. The patients were divided into a study group composed of patients with proven AMI and a control group composed of patients with a final diagnosis that did not include AMI. 2.2. Statistical analysis The sensitivity, specificity, positive predictive values, negative predictive values and accuracy of each individual CT finding for each observer were calculated. The interobserver agreement for the detection of CT findings between the two radiologists was calculated using Kappa statistics. A Kappa statistic greater than 0.75 was considered as excellent agreement, 0.4–0.75 as fair to good agreement and less than 0.4 as poor agreement. 3. Results MDCT angiography diagnosed mesenteric ischemia in 16 patients of which nine patients underwent surgery. Three patients collapsed and expired before surgery. Mesenteric ischemia was confirmed in the remaining 5 patients by positive clinical and laboratory findings, these cases were managed conservatively and recovered. CT also provided a definitive alternate diagnosis in the 15 patients who did not have mesenteric ischemia, which was later proved on the basis of laboratory values, clinical and surgical findings (Table 1). Four patients [pancreatitis (n = 1), inflammatory colitis (n = 1) and diverticulitis (n = 2)] underwent surgery. No evidence of mesenteric ischemia was seen on CT or surgery in these patients. An ascitic tap confirmed the CT diagnosis of tubercular peritonitis and the patient recovered on anti-tubercular treatment. One patient with adenocarcinoma of colon had unresectable disease and received only palliative therapy. Thrombolytic therapy was given to the patients with aortic thrombosis (n = 1) and inferior vena cava thrombosis (n = 1). One patient with hepatic artery pseudoaneurysm was treated with percutaneous thrombin injection, following which there was no episode of malena. Two patients with ureteric calculus (n = 1) and cystic adnexal mass (n = 1) were managed conservatively. Vascular abnormalities were demonstrated in 15 patients of mesenteric ischemia. Atherosclerotic disease causing luminal compromise of the aorta/superior mesenteric artery (SMA)/celiac axis was seen in 6 of these patients. Mesenteric arterial occlusion was seen in 7 patients (43.7%). Three of these cases showed thrombotic occlusion of celiac trunk/SMA just beyond the origin from aorta Table 1 Patients with alternative diagnosis (control group). S. No.
Alternative diagnosis in patients without AMI
No. of patients [n = 15]
1 2 3 4 5 6 7 8 9 10 11 12 13
Diverticulitis Inflammatory colitis Adenocarcinoma colon Pancreatitis Portal vein/SMV thrombosis Inferior vena cava thrombosis Nephrolithiasis Tubercular peritonitis Cystic adnexal mass Perforation peritonitis Extra hepatic portal vein obstruction Hepatic artery pseudoaneurysm Aortic thrombosis
02 02 01 01 01 01 01 01 01 01 01 01 01
e584
M. Barmase et al. / European Journal of Radiology 80 (2011) e582–e587
Fig. 1. 58 year old male patient with pain abdomen and malena. MDCT angiography. (A) Coronal MPR image: the small bowel loops are dilated with thinned out walls and gross band like pneumatosis. Air is also seen in the mesenteric veins and the portal radicles in the liver. Note the irregular, non-enhancing areas in the periphery of the liver due to infarcts. (B) Sagittal MIP image shows complete occlusion of the proximal superior mesenteric artery by thrombus. This patient expired before surgery.
(Fig. 1), while three cases showed thrombosis of the horizontal part of SMA. In one case the mid SMA was completely occluded from 3.5 cm beyond its origin with extension of the thrombus into segmental branches as well (Fig. 2). One patient with mild ostial stenosis of the SMA showed an eccentric filling defect consistent with embolus at the second branching point of the SMA (Fig. 3). Another patient with no evidence of atherosclerotic disease of the aorta or mesenteric vessels showed an eccentric filling defect (embolus) in a branch vessel with an abrupt change in luminal caliber. Five patients with AMI had evidence of venous thrombosis (31%). Two of these patients had thrombosis of both the portal vein and SMV (Fig. 4). Two other patients showed thrombosis of portal vein, SMV and splenic vein with extension into small mesenteric branches (Fig. 5). One patient with midgut volvulus had secondary
compression of the mesenteric vessels leading to ischemic changes in the bowel loops. One patient of AMI showed no abnormalities in the mesenteric vasculature. The kappa statistics for the various individual CT findings of bowel ischemia showed excellent agreement between the two observers, except for the presence of mesenteric arterial stenosis (0.716) and mesenteric arterial embolus (0.652). The initial disagreements between the two radiologists were resolved by consensus review. The individual sensitivity, specificity, positive predictive value, negative predictive value and accuracy of the individual CT findings are depicted in Table 2. Mesenteric congestion, ascites, luminal dilatation and bowel wall thickening were the most common CT features noted in patients with AMI, however these were found to
Fig. 2. 40 year old male patient with two episodes of malena. MDCT angiography. (A) Sagittal MIP image shows stenosis of the proximal celiac trunk with complete occlusion of the mid SMA with nonfilling of the branches. (B) Ischemic bowel loops are thin walled and show lack of enhancement. Also note the paucity of mesenteric vessels.
M. Barmase et al. / European Journal of Radiology 80 (2011) e582–e587
e585
Fig. 3. 60 year old female patient presented with acute pain in abdomen. CT angiography. (A) Axial image: SMA shows an eccenteric filling defect suggestive of embolus. Small bowel loops show lack of mural enhancement. (B) VR image better depicts the embolus at a branch point in the SMA with distal reformation (arrow).
Fig. 4. 58 year old male patient with acute pain in abdomen. CT angiography abdomen, venous phase images. (A) There is dilatation with diffuse mural thickening of small bowel loops with a striated pattern giving a target appearance. Note the increased density with congestion of the subtending mesentery. (B) A large hypodense filling defect is seen in the superior mesenteric vein (arrow) as the cause of mesenteric ischemia.
Fig. 5. 39 year old female patient with abdominal distention and pain. MDCT angiography venous phase data. (A) Coronal MIP image shows extensive thrombosis of portal vein and SMV. Multiple collaterals are seen at the porta and in gastrohepatic ligament. Small calcific specks are seen involving the wall of SMV. Thick walled, mildly dilated jejunal loops are seen. (B) Axial image shows small foci of intramural air in the dependent part of jejunal loop suggestive of pneumatosis intestinalis.
e586
M. Barmase et al. / European Journal of Radiology 80 (2011) e582–e587
Table 2 CT findings in the two study groups. CT findings
Pts with MI (N = 16)
Control group (N = 15)
Sensitivity (%)
Specificity (%)
Positive predictive value (%)
Negative predictive value (%)
Accuracy (%)
Mortality (N = 9) (%)
Bowel wall thickening Bowel wall stratification Lack of mural enhancement Abnormal mural enhancement Mesenteric congestion/fluid Luminal dilatation Pneumatosis intestinalis Ascites Solid organ infarcts Mesenteric arterial thrombosis Mesenteric arterial stenosis Mesenteric arterial embolus Venous occlusion
9 8 7 7 12 13 5 13 4 7 5 2 5
7 3 1 2 7 2 0 8 3 1 1 0 2
56.25 50 43.75 43.75 75 81.25 31.25 81.25 25 18.75 31.25 12.5 31.25
53.33 80 93.33 80.00 53.33 86.67 100 46.67 80 93.37 93.33 100 86.67
56.35 72.73 87.5 70.00 43.16 86.67 100 61.90 57.14 18.75 83.33 100 71.43
53.33 60 60.87 57.14 66.67 81.25 57.69 70 50 51.85 56.00 51.7 54.17
54.83 64 67 61.29 64.5 83.87 64.51 64 51 54.84 61.29 54.8 58.06
55.55
Table 3 Comparison of axial and 2D/3D reconstructed images.
55.5 55.5 77.7 55.5 33.3 66
22.2
4. Discussion
CT findings
MIP/MPVR
VR
Axial
Bowel wall thickening Lack of enhancement Abnormal enhancement Mesenteric congestion/fluid Luminal dilatation Pneumatosis intestinalis Mesenteric arterial occlusion Mesenteric arterial stenosis Mesenteric arterial embolus Mesenteric venous occlusion Extent/degree of vascular abnormality
++ +++ +++ +++ +++ +++ +++ +++ +++ +++ +++
– – – – – – +++ +++ +++ ++ +++
++ ++ ++ ++ ++ +++ + + + +++ –
“–” not visualized; “+” to “+++” correspond to poor, fair, and excellent visualization.
have low specificity. The presence of solid organ infarcts, including that of liver (n = 2) and spleen (n = 2) were found to be highly specific in diagnosing AMI. The CT findings of mesenteric arterial occlusion, mesenteric venous occlusion, and lack of mural enhancement or abnormal mural enhancement and pneumatosis intestinalis were found to be most specific for bowel ischemia. Using these diagnostic criteria, AMI could be diagnosed with a sensitivity of 40.6%, specificity of 96.6%, positive predictive value of 92.85% and negative predictive value of 60.41%. The individual CT findings suggestive of bowel ischemia were compared on the axial images and 2D/3D data sets (MIP, MPVR, and VR). Mesenteric arterial occlusion (thrombotic or embolic), mesenteric arterial stenosis and venous occlusion were very well depicted on the reconstructed data set. Bowel and mesenteric abnormalities were also better seen on 3D images as compared to the axial data (Table 3). Two cases of celiac axis stenosis and one case of mesenteric arterial embolus were missed on the axial data but were diagnosed on the reformatted images (MIP and VR). Reconstructed images also improved the diagnostic confidence of both radiologists while evaluating the extent and degree of vascular involvement. 3.1. Patient outcomes In the present study mesenteric ischemia was associated with a high mortality (n = 9, 56.2%) and morbidity. Patients with arterial occlusive disease, luminal dilatation, lack of bowel wall enhancement, abnormal enhancement, pneumatosis intestinalis and solid organ infarcts were found to have a poor outcome. All patients with pneumatosis or solid organ infarcts and 5 of 7 patients with arterial occlusion (75%) had a fatal outcome.
AMI is one of the most challenging clinical conditions because of its high mortality rate (50–90%) and difficulty in diagnosis [1,9,10]. Catheter angiography was considered the gold standard but it is invasive, time consuming and difficult to perform with limited availability in select centres. Secondly, mesenteric venous ischemia is not reliably diagnosed on catheter angiography [5]. MDCT, with its wide availability and fast acquisition is a good diagnostic alternative. In the present study the mortality of patients with AMI was 56.2%. Eight of these patients had luminal dilatation (88%), six patients (66.6%) had arterial occlusive disease, and two patients had venous occlusion (22.2%), while one patient showed no evidence of any mesenteric vascular abnormality. All patients with pneumatosis intestinalis and solid organ infarcts died. Yamada et al. in their study on AMI showed that patients with presence of bowel dilatation or abnormal gas in the bowel wall or portal system were proved to have a wider extent of ischemia on surgery and hence a poorer outcome [11]. In the present study, mesenteric arterial occlusion due to thrombosis of the proximal SMA was found to be the most common cause of AMI (43.7%) while emboli in the SMA were seen in 12.4% (n = 2) of patients. Venous thrombosis is an important, but less common cause of AMI seen in 5–15% of cases of mesenteric ischemia and infarction. The majority of patients with venous occlusion show bowel wall thickening, luminal dilatation and abnormal mucosal enhancement [4,12]. Venous thrombosis was seen in four cases of AMI, none of these patients had a prior history of hypercoagulable state. All of these patients showed bowel wall thickening, mural stratification, luminal dilatation and mesenteric congestion. Conversely we also had one patient of venous occlusion who had frank bowel necrosis and pneumatosis, a rare finding in venous ischemia. Nonocclusive mesenteric ischemia usually accounts for 20–30% of cases of AMI and occurs when there is hypoperfusion from low cardiac output [4]. In the present study we had two patients in congestive cardiac failure with low cardiac output. One of these patients was a case of Ebstein’s anomaly with evidence of diffuse mesenteric ischemia, while the second patient showed evidence of inferior vena cava thrombosis with no bowel changes. Bowel wall thickening is the least specific CT finding in cases of acute bowel ischemia, as it is observed in a variety of nonischemic conditions [13]. In the present study, bowel wall thickening was seen in nine patients of mesenteric ischemia and in seven patients without ischemia. These included two patients with diverticulitis, one patient each of pancreatitis, inflammatory colitis, tubercular peritonitis, adenocarcinoma colon and a patient of extra hepatic portal vein obstruction with portal cavernoma.
M. Barmase et al. / European Journal of Radiology 80 (2011) e582–e587
Portomesenteric gas resulting from bowel ischemia has been shown to have a poor prognosis with a mortality rate of 75–90% [14]. In the present study the sensitivity and specificity of pneumatosis intestinalis for diagnosing AMI was 31.25% and 100% which is similar to the sensitivity of 36% and specificity of 100% reported by Aschoff et al. [15]. The unenhanced segments of bowel wall, a finding more commonly observed in the patients with arterial occlusion was shown to have a specificity of 100% for ischemia in the series reported by Zalcman et al. [16]. In the present study, mesenteric arterial thrombosis was seen in seven patients of AMI. Lack of bowel wall enhancement was noted in 6 of these patients (85.7%) with an overall sensitivity and specificity of 43.75% and 93.33%. The presence of mesenteric congestion, mesenteric fat stranding or fluid was found to have a very high sensitivity but a low specificity as stated by many authors in the past [7,9,15]. By using a combination of the following diagnostic criteria: mesenteric arterial thrombosis, mesenteric venous occlusion, pneumatosis intestinalis and lack of bowel wall enhancement, we could diagnose AMI with a sensitivity of 40.6% and specificity of 96.6%. The most widely used techniques of reconstruction in the diagnosis of suspected bowel ischemia are VR, MIP, and MPR. Horton and Fishman stated that when evaluating the mesenteric vessels they typically preferred using VR, although MIP was valuable for the visualization of tiny branch vessels [17]. Kirkpatrick et al. found that MIP reconstructions were easier and faster to obtain, but were subject to artefacts caused by vascular calcification. There is also potential for less accurate estimation of stenosis with increasing slab thickness. Volume rendered images, which required more time to construct gave superior three-dimensional spatial relationship of vessels [1]. We compared the axial images with the 3D reconstructed data for the assessment of vascular, bowel and mesenteric abnormalities. We encountered no vascular abnormality that could not be appreciated on 3D reconstructions. It was noted that the extent of vascular abnormalities, arterial narrowing and kinking were better seen on 3D reformatted images. The diagnostic accuracy as well as level of confidence of both observers was better when MIP and VR reconstructed images were used. The bowel changes were better seen on reconstructed images in 9 out of 16 patients of MI. It was also found that the 3D reconstructed images showed better demarcation of affected ischemic bowel from the segment of uninvolved bowel in three patients of ischemia. Mesenteric congestion and vascularity were equally well seen on both 3D reformatted and axial images.
e587
5. Conclusion Biphasic MDCT angiography is an excellent, fast and noninvasive modality for the diagnosis of bowel ischemia, as it can visualize both the bowel and mesenteric changes as well as accurately depict the mesenteric vasculature. The combination of both axial and 3D reconstructed images increases the diagnostic confidence of the interpreting radiologist. Conflict of interest None of the authors have any conflict of interest or any financial disclosures to be made. References [1] Kirkpatrick ID, Kroeker MA, Greenberg HM. Biphasic CT with mesenteric CT angiography in the evaluation of acute mesenteric ischemia: initial experience. Radiology 2003;229(1):91–8. [2] Stoney RJ, Cunningham CG. Acute mesenteric ischemia. Surgery 1993;114:489–90. [3] May LD, Berenson MM. Value of serum inorganic phosphate in the diagnosis of ischemic bowel disease. Am J Surg 1983;146:266–8. [4] Park WM, Gloviczki P, Cheny KJ, et al. Contemporary management of acute mesenteric ischemia: factors associated with survival. J Vasc Surg 2002;35(3):445–52. [5] Bakal CW, Spraygen S, Wolf EL. Radiology in intestinal ischaemia: angiographic diagnosis and management. Surg Clin North Am 1992;72(1):125–41. [6] Hermsen K, Chong WK. Ultrasound evaluation of abdominal aortic and iliac aneurysms and mesenteric ischemia. Radiol Clin North Am 2004;42(2):365–81. [7] Taourel PG, Deneuville H, Pradel JA, Regent D, Bruel JM. Acute mesenteric ischemia: diagnosis with contrast enhanced CT. Radiology 1996;199(3):632–6. [8] Horton KM, Fishman EK. Multidetector row CT of mesenteric ischemia: can it be done? Radiographics 2001;21(6):1463–73. [9] Wiesner W, Khurana B, Ji H, et al. CT of acute bowel ischemia. Radiology 2003;226(3):635–50. [10] Inderbitzi R, Wagner HE, Seiler C, et al. Acute mesenteric ischemia. Eur J Surg 2004;158:123–6. [11] Yamada K, Saeki M, Yamaguchi T, et al. Acute mesenteric ischemia, CT and plain radiographic analysis of 26 cases. Clin Imaging 1998;22(1):34–41. [12] Kim JY, Ha HK, Byun JY, et al. Intestinal infarction secondary to mesenteric venous thrombosis: CT-pathologic correlation. J Comput Assist Tomogr 1993;17(3):382–5. [13] Levy AD. Mesenteric ischaemia. Radiol Clin North Am 2007;45(3):593–9. [14] Sebastia C, Quiroga S, Espin EC, et al. Portomesenteric vein gas: pathologic mechanisms, CT findings, and prognosis. Radiographics 2000;20(5):1213–24. [15] Aschoff AJ, Stuber G, Becker BW, et al. Evaluation of acute mesenteric ischemia: accuracy of biphasic mesenteric multi-detector CT angiography. Abdom Imaging 2008;34:345–57. [16] Zalcman M, Sy M, Donckier V, et al. Helical CT signs in the diagnosis of intestinal ischemia in small-bowel obstruction. AJR Am J Roentgenol 2000;175(6):1601–7. [17] Horton KM, Fishman EK, Multidetector. CT angiography in the diagnosis of mesenteric ischemia. Radiol Clin North Am 2007;45(2):275–88.