The role of computed tomography in the diagnostic pathway of acute mesenteric ischemia: a nested case-control study

Abstract

Background

Computed tomography (CT) can be used as the primary screening modality for the evaluation of patients suspected of having acute mesenteric ischemia known to show high sensitivity and specificity rates.

Purpose

To prove the value of CT in patients with pathological abdominal findings following cardiac surgery.

Material and Methods

In a retrospective case-control study, 12 different CT scan parameters of patients with or without mesenteric ischemia following cardiac surgery were compared using univariate and logistic regression analyses.

Results

Of 14,176 patients, 133 (0.9%) received an abdominal CT scan during postoperative care due to pathological abdominal findings. Sixty-eight patients were diagnosed with acute mesenteric ischemia. In-hospital mortality was 73.5% for this group. CT parameters with the highest specificity for indicating colonic ischemia were intestinal (99%) or porto-venous (96%) pneumatosis, abnormal contrast medium enhancement (89%), and occlusion of the proximal inferior mesenteric artery (81%). All of those parameters showed low sensitivity levels in the range of 15%–23%. A statistically significant association between acute mesenteric ischemia and CT appearance was obtained for contrast medium enhancement (odds ratio [OR] 12.2, 95% confidence interval [CI] 1.5–99.2) and intestinal pneumatosis (OR 21.0, 95% CI 2.7–165.2) only.

Conclusion

The typical CT criteria indicating mesenteric ischemia lose their accuracy in patients under critical clinical conditions. As CT remains the first-line diagnostic imaging modality for abnormal abdominal findings following cardiac surgery, negative signs should not prevent early laparotomy if clinical suspicion remains high.

Keywords

Acute mesenteric ischemia cardiovascular surgery computed tomography case-control study

Introduction

Acute mesenteric ischemia (AMI) following cardiac surgery is a life-threatening condition, with reported mortality rates of 70%–90% (1,2). Early diagnosis can be seen as the key method to initiate adequate treatment and improve outcome. The typical clinical signs of AMI can hardly be obtained if the patient is on artificial ventilation or in organ failure.

Computed tomography (CT) can be used as the primary screening modality for the evaluation of patients suspected of having mesenteric ischemia. Using CT angiography, the bowel wall as well as the peri-colonic soft tissues and mesenteric perfusion can be evaluated. CT can also demonstrate alternative diagnoses and assist in managing several conditions (3). The ability of CT for diagnosing mesenteric ischemia has been reported to have sensitivity and specificity rates of approximately 90% (1,2,4,5).

However, in patients under life-threatening conditions, the key parameters of mesenteric ischemia such as bowel wall thickening or luminal dilatation of the colon can also be caused by other conditions (e.g. fluid overload, capillary leak in sepsis).

The aims of the present study were to determine whether the known CT parameters for AMI reach similar sensitivity and specificity levels even under intensive care conditions and to determine whether signs for altered mesenteric perfusion may play a greater role in the suspicion of mesenteric ischemia.

Studies focusing on CT and comparing patients with and without AMI in this setting are lacking.

Material and Methods

Patient population

In this retrospective study, all patients following cardiovascular surgery were included who have had an abdominal CT scan for various indications at our hospital within 12 years and who had been prospectively enrolled in the hospital’s database. A further 22 patients were added and later integrated into the control group, who also had an abdominal CT scan during postoperative intensive care but who had abdominal surgery as the primary operation.

The indication for performing an abdominal CT scan, as given by the intensivist, was recorded and classified into three groups: (i) (suspected) SIRS/sepsis, raised serum inflammatory parameters, organ failure but without mentioning mesenteric ischemia; (ii) the same parameters as in (i), but including mesenteric ischemia or AMI or lactatemia alone; and (iii) any other reasons.

With this model, we managed to separate patients who developed AMI after cardiac surgery from patients who showed pathological clinical abdominal symptoms but where mesenteric ischemia was excluded and other reasons for inflammation/sepsis were found. All patients with AMI had abdominal CT performed before laparotomy or further conservative therapy.

Data collection

Clinical, surgical, and laboratory data had been collected from all patients using the hospital documentary systems COPRA (Copra System GmbH, Sasbachwalden, Germany) or SAP (SAP Deutschland SE, Walldorf, Germany). General data included age, gender, length of hospital stay, mortality, ASA classification, priority, and time of the operation. Laboratory results, fluid management and administration of vasopressor therapy, and SAPSII and SOFA scores were obtained through the COPRA system on the day when the CT was performed. The Institutional Review Board of our hospital approved this retrospective study (no. 3235-08/11).

Patients

From patients undergoing cardiac surgery during this period of time, we selected only patients who had undergone: (i) coronary bypass with or without cardiopulmonary bypass (CPB); (ii) valve replacement; or (iii) ascending aortic repair with CPB (n = 14,176). In this subgroup, we first looked at patients who received an abdominal CT scan during the early postoperative course (within 35 days after cardiac surgery) for any reason (n = 111). A total of 68 patients were diagnosed with AMI and these were included into the index group. All of them underwent a laparotomy. Mesenteric ischemia was diagnosed by CT scan, endoscopic or surgical macroscopic findings of bowel ischemia, and/or was confirmed histologically. In a group of 43 post-cardiac surgery patients, no pathological findings indicating mesenteric ischemia were determined (control group), of whom 25 (58.1%) underwent a laparotomy. A further 22 patients were included into the control group after general surgical (n = 18) or vascular (n = 4) operations. These patients had abdominal CT scans due to clinical signs, but no suspicion of mesenteric ischemia occurred; 11 of them underwent a laparotomy as result.

Abdominal computed tomography

CT scanning was performed on either a 512-slice or 64-slice scanner (Revolution CT or VCT, GE Healthcare, Boston, MA, USA) using 70 mL of contrast agent (Imeron 400, Bracco Imaging, Milan, Italy) followed by 50 mL saline at 4 mL/s. Images were either carried out in the arterial phase (7%), the venous phase (2%), or both (88%). In two patients, no contrast medium was applied; two other patients were given oral contrast medium only.

For CT, we determined the date and time of CT scanning, the time to the initial operation, and the priority of the scan. The following CT criteria were obtained separately for the right and left hemicolon (middle of transverse colon as border) (6,7): bowel wall thickening (≥5 mm or thinning); contrast medium enhancement (reduced or absent); luminal dilatation (pathological if > 50 mm); intestinal or porto-mesenteric pneumatosis; mesenteric stranding; ascites; central arterial stenosis of superior mesenteric artery (SMA); peripheral arterial narrowing (SMA); arterial calcifications; arterial occlusion of inferior mesenteric artery (IMA); and the impression of the examiner on the occurrence of non-occlusive mesenteric ischemia (NOMI).

The original CT reports were not included into our study. The initial CT reports and the clinical status of patients of both groups were blinded and retrospectively analyzed again on a picture archiving workstation by two readers independently. In case of disagreement, parameters were discussed and a mutual decision was made.

All CT criteria were assessed as normal or abnormal according to the definition. In addition, the examiners were asked to rate the certainty level of their decision according to the five-staged reliability score for radiological findings (8), ranging from stage 1 (very good to assess) to stage 5 (not to assess). Only results rated as stages 1 or 2 (good to assess) were included into our data management. Results rated as stage 3 or higher were defined as “not to assess,” which is the reason for slightly differing numbers of parameters assessed.

Statistical analysis

Patients with or without mesenteric ischemia were initially compared regarding general, surgical, and other perioperative parameters using univariate analysis. Fisher’s exact or Chi-squared tests were performed for categorical variables and Mann–Whitney U-test was performed for continuous variables. Continuous data are presented as means with SD. P < 0.05 was considered significant. Odds ratio (OR), sensitivity and specificity levels, and the 95% confidence intervals (CI) of all parameters were analyzed based on the binomial distribution. Statistical analyses were performed using the Statistical Package for the Social Sciences (SPSS) software (version 25.0. SPSS Inc., Chicago, IL, USA).

Results

A total of 133 patients were included into this study, who received an abdominal CT scan within 35 days following major cardiovascular (n = 111) or abdominal (n = 22) surgery for various reasons, but mainly to exclude abdominal causes for sepsis, raised infection parameters, lactatemia, or abnormal abdominal findings. The diagnosis of AMI was made in 68 patients, who were all operated (index group). A further 43 patients after cardiac surgery and 22 patients after abdominal, general, or vascular surgery with no signs of mesenteric ischemia were seen within the period of hospitalization in the ICU, qualifying them to be included into the control group. The main clinical data did not differ between index patients and controls (Table 1). Hospital mortality rates were found to be very high in both groups.

Table 1.

Clinical features and surgical data as comparison of patients with mesenteric ischemia (n = 68) and controls (n = 65).

Parameter	Index group	Control group	P
Age (years)	67.7 (18–85)	66.9 (16–87)	0.752
Male	45 (66.2)	52 (80.0)	0.082
In-hospital mortality	50 (73.5)	43 (66.2)	0.450
ASA (day of primary operation)	3.31 ± 0.50	3.15 ± 0.59	0.073
SAPSII (day of primary operation)	50.82 ± 15.50	48.81 ± 16.81	0.072
SOFA (day of CT scan)	12.54 ± 3.07	11.67 ± 4.22	0.598
SAPSII (day of CT scan)	61.81 ± 16.28	58.78 ± 20.55	0.416
Surgical data
Occurrence of colonic ischemia	68 (100)	0
Isolated right hemicolon	19 (27.9)	0
Isolated left hemicolon	8 (11.8)	0
Bilateral	41 (60.3)	0
Kind of primary operation
Cardiovascular	68 (100)	43 (65)
General surgical / visceral	0	22 (35)
Urgency of primary operation
Emergency	19 (27.9)	22 (33.5)	0.508
Urgent	14 (20.6)	12 (18.5)
Elective	35 (51.5)	31 (47.7)
Abdominal CT scan	68 (100)	65 (100)
Time between primary operation and CT (days)	7.15 ± 6.81	7.00 ± 7.90	0.003
Laparotomy after CT scan	68 (100)	36 (55.4)
Resection of colon	59 (86.8)	15 (23.1)
Vascular (bypass, embolectomy)	2 (2.9)	3 (4.6)
Explorative laparotomy	7 (10.3)	18 (27.7)
Time between CT and re-laparotomy (hours)	29.08 ± 52.33	32.43 ± 77.22	0.457
Indication for CT scan
Sepsis, organ failure without suspicion of mesenteric ischemia	21 (30.9)	23 (35.4)	0.928
Suspicion of mesenteric ischemia, lactatemia	33 (48.5)	28 (43.1)
Any other indication	14 (20.6)	14 (21.5)

Values are given as n (%), mean ± SD, or median (range).

CT findings

Evaluation of CT criteria indicating direct abnormalities of the affected part of the colon (or not) was carried out separately for the right and left hemicolon. Sensitivity, specificity, and positive and negative predictive values for each parameter are shown in Table 2. Parameters with the highest specificity for indicating colonic ischemia of the right hemicolon were intestinal or porto-venous pneumatosis, abnormal contrast medium enhancement, absent contrast medium in the proximal IMA, >50% stenosis of the central SMA, followed by positive mesenteric fat stranding. Similar results were obtained for the left side, where, in addition, the dilated lumen of the colon was shown to be highly specific.

Table 2.

Sensitivity, specificity, PPV, and NPV of CT criteria indicating mesenteric ischemia of the right and left hemicolon (n = 133).

	Right hemicolon				Left hemicolon
Localization of affected colon	Sensitivity (%)	Specificity (%)	PPV (%)	NPV (%)	Sensitivity (%)	Specificity (%)	PPV (%)	NPV (%)
Bowel wall thickness (n = 132)	43.3 [30.6–56.8]	55.7 [43.3–67.6]	45.6 [32.3–59.3]	53.4 [41.4–65.2]	63.3 [48.3–76.6]	39.8 [29.2–51.1]	38.3 [27.7–49.7]	64.7 [50.1–77.6]
Contrast medium enhancement (n = 118)	15.0 [7.1–26.6]	88.6 [78.7–94.9]	90.0 [55.5–99.8]	62.0 [51.8–71.5]	6.1 [1.3–16.9]	89.3 [80.6–95.0]	50.0 [11.8–88.2]	67.0 [57.4–75.6]
Intestinal pneumatosis (n = 133)	23.3 [13.4–36.0]	98.6 [92.3–99.9]	93.3 [68.0–99.8]	60.0 [50.4–69.0]	10.2 [3.4–22.2]	98.8 [93.5–100]	83.3 [35.9–99.6]	65.4 [56.4–73.6]
Luminal dilatation (n = 133)	65.0 [51.6–76.9]	45.7 [33.7–8.1]	50.6 [39.0–62.2]	60.4 [46.0–73.6]	30.6 [18.2–45.4]	83.3 [73.6–90.6]	51.7 [32.5–70.6]	67.3 [57.4–76.2]
Mesenteric stranding (n = 130)	35.0 [23.1–48.4]	77.1 [65.6–86.3]	60.0 [42.1–76.1]	59.8 [49.0–69.9]	16.3 [7.3–29.7]	82.1 [72.3–89.6]	38.1 [18.1–61.6]	63.3 [53.5–72.3]
Ascites (n = 133)	70.0 [56.8–81.2]	30.0 [19.6–42.1]	46.2 [35.6–56.9]	53.8 [37.2–69.9]	69.4 [54.6–81.8]	28.6 [19.2–39.5]	36.2 [26.5–46.7]	61.5 [44.6–76.6]
Portal venous gas (n = 132)	11.7 [4.8–22.6]	95.7 [88.0–99.1]	70.0 [34.8–93.3]	56.3 [46.9–65.4]	10.2 [3.4–22.2]	94.0 [86.6–98.0]	100 [47.8–100]	64.8 [55.6–73.2]
SMA – central stenosis (n = 113)	16.7 [8.3–28.5]	78.6 [67.1–87.5]	71.4 [41.9–91.6]	57.3 [46.8–67.3]	14.3 [5.9–27.2]	75.0 [64.4–83.8]	46.7 [21.3–73.4]	64.3 [54.0–73.7]
SMA – peripheral rarefication (n = 125)	18.3 [9.5–30.4]	80.0 [68.7–88.6]	52.4 [29.8–74.3]	55.4 [45.2–65.3]	18.4 [8.8–32.0]	79.8 [69.6–87.8]	40.9 [20.7–63.6]	65.0 [55.0–74.2]
SMA – sclerosis (n = 133)	61.7 [48.2–73.9]	34.3 [23.4–46.6]	44.6 [33.7–55.9]	51.1 [36.1–65.9]	63.3 [48.3–76.6]	36.9 [26.6–48.1]	36.9 [26.6–48.1]	63.3 [48.3–76.6]
IMA – occlusion (n = 123)	3.3 [0.4–11.4]	81.4 [70.3–89.7]	25.0 [3.2–65.1]	50.9 [41.3–60.5]	4.1 [0.5–14.0]	84.5 [75.0–91.5]	25.0 [3.2–65.1]	61.7 [52.2–70.6]
CT – impression of NOMI (n = 118)	20.0 [10.6–32.3]	82.9 [72.0–90.8]	75.0 [47.6–92.7]	56.9 [46.7–66.6]	20.4 [10.2–34.3]	83.3 [73.6–90.6]	62.5 [35.4–84.8]	66.7 [56.8–75.6]

Values in brackets are 95% confidence intervals.

CT, computed tomography; IMA, inferior mesenteric artery; NOMI, non-occlusive mesenteric ischemia; NPV, negative predictive value; PPV, positive predictive value; SMA, superior mesenteric artery.

Sensitivity levels were demonstrated to be lower: the highest percentage on the right side was seen for ascites, luminal dilatation, sclerosis of the SMA, and abnormal thinning or thickening of the affected colon. Those four parameters also remained the most sensitive for the left colon (Table 2).

High positive predictive values were demonstrated for intestinal pneumatosis and abnormal contrast medium enhancement on the right side and detection of portal venous or mesenteric venous gas and intestinal pneumatosis on the left.

A quantitative comparison of sensitivity levels of both sides demonstrates that, apart from thickness, abnormal direct signs of the ischemic bowel wall (contrast medium enhancement, pneumatosis, dilatation, stranding) were seen in twice as many patients if the right colon was affected but were difficult to detect on the left side (Table 2). A statistically significant association between AMI and CT appearance was obtained for contrast medium enhancement (P = 0.001) and intestinal pneumatosis (P < 0.001) on the right side and pneumatosis alone (P = 0.025) on the left.

Grouping single parameters into direct signs of the bowel wall and indirect signs (appearance of arterial perfusion and ascites), the criteria of the latter group showed similar sensitivity and specificity levels compared with the typical features for AMI in CT.

Discussion

This retrospective analysis focused on the value of CT criteria to allow the diagnosis of AMI in patients after cardiac surgery under ICU conditions, where suspicion of bowel ischemia occurs or at least cannot be excluded. Abdominal complications following cardiothoracic surgery occur in 0.2%–2% only (9 –12), of which again a small percentage of 5%–27% is mesenteric ischemia (13 –16).

CT can be seen as one of the three columns of the diagnostic pathway beside clinical examination and colonoscopy. Multi-slice CT scan is reported to reach sensitivity and specificity levels up to 90%. It is valuable for patients after cardiac surgery under ICU conditions for two reasons: the likelihood of mesenteric ischemia is higher in this subgroup of patients; and clinical signs may be difficult to elicit and a complete colonoscopy difficult to obtain.

The key question remains whether the well-described CT criteria indicating AMI may also be imposed and interpreted as such in this subgroup of patients under ICU conditions.

We evaluated 12 criteria and compared those with the same CT findings made in patients with a similar clinical status but without ischemia. Some of those criteria, known to be highly specific for mesenteric ischemia may also appear with fluid overload, sepsis, or organ failure (5,16 –19). Despite the high specificity in patients with AMI, the occurrence of some markers may be related to the underlying cause of mesenteric ischemia (18 –21), the stage of ischemia (e.g. gangrene, reperfusion) (22,23), and the extent of mural changes (1).

Although the accuracy of CT scans indicating AMI is reported to be high, individual parameters, which form the basis of those overall studies, are reported to reach significantly lower incidence levels (24). To our knowledge, there is only one study found in the literature focusing on a post-cardiac surgery setting, where patients showed similar incidences of CT criteria (25). In the present study, sensitivity levels lay at the lowest point of the range given in the literature (24) which is difficult to explain. In contrast, reduced specificity in this particular setting may be due to a higher incidence of a changed bowel wall configuration due to fluid overload, organ failure, and capillary leak secondary to sepsis. This phenomenon regards to all signs of bowel ischemia indicating changes in the bowel wall or mesenteric tissue. To our surprise, a second group of parameters showed similar levels of accuracy, of which only a few have been mentioned in the literature as indicating mesenteric ischemia. Among those, sclerosis and proximal stenosis of the SMA, and occlusion of the IMA show the highest incidence and specificity levels. It is possible that those signs may rather indicate a potentially hindered vascular system and therefore are likely to be associated with a group of patients undergoing cardiac surgery rather than to the actual postoperative status. However, these signs should not be ignored when assessing a CT scan performed to exclude bowel ischemia in this setting.

In order to assess patients getting a CT scan in this particular setting, who were not diagnosed as having mesenteric ischemia, it was also possible to look at the non-ischemic parts of the colon. To our surprise, the incidence of altered contrast medium enhancement and mesenteric fat stranding in the non-ischemic parts of the colon was similarly high compared to the ischemic bowel. Those findings can be explained by altered cardiac output and septic capillary leak or fluid overload. However, to our knowledge, this phenomenon has never been described before and should also be taken into account when assessing an abdominal CT scan in this postoperative situation. Barrett at al. (25) also compared the CT appearance of bowel ischemia after cardiac surgery and found abnormalities in mural enhancement and mesenteric stranding in exactly 50% of control patients without bowel ischemia. Unfortunately, their control group consisted of 16 patients only. That is why those results should be interpreted with care. However, we undermined our results by adding a further 22 patients into our control group, who underwent abdominal, but not cardiac, surgery. Although this group has become more heterogenic, we see more advantages analyzing a higher number of 65 controls rather than limitations due to different causes of the altered physiological status of these patients.

As the diagnosis of colonic ischemia and its extent were determined in all index patients postoperatively, we were able to separately look at CT criteria for bowel ischemia of the right and left hemicolon. This has never been examined before. By doing this, we detected that, except eight patients, all index patients suffering from left-sided ischemia had additional ischemia of the right-sided colon. This could mean a great clinical importance. Although most right-sided CT criteria for ischemia were found negative for this small subgroup, almost all of those patients showed a dilated bowel lumen, which should not be mis-interpreted as sign of ischemia, but can be explained by dysfunction of the ischemic left-sided colon. As shown in Table 2, quantitative analysis of CT parameters demonstrates the generally low sensitivity of some of the classical criteria (mural enhancement, pneumatosis, luminal dilatation, and mesenteric fat stranding), but were found twice as high on the right side compared with the left. This is difficult to explain but reveals that negative results should be interpreted with care, especially on the left side.

Besides the retrospective design, there are a few limitations of this study. We discussed the relatively low sensitivity levels demonstrated in our study and compared the protocol of the administration of contrast medium, but no differences were found, taking into account that some patients had considerably impaired cardiac output or high doses of catecholamines. We cannot fully exclude that some of our patients, categorized into the control group, may have developed early forms of mesenteric ischemia (e.g. mucosal damage), since some of those patients were not operated after the CT scan and did not have an endoscopy to exclude ischemia.

The fact that some of our index patients also suffered from small bowel ischemia (n = 20) was documented but not taken into consideration for the analysis of our criteria. However, it is likely that some parameters (e.g. ascites) may have been influenced by this. Nevertheless, since this study focuses on the association of CT criteria and the occurrence of colonic ischemia and not on the clinical course or prognosis of the patient, this may be acceptable.

In conclusion, the CT criteria showed low sensitivity and specificity levels predicting AMI after cardiac surgery in the present study. The appearance of the parameters was different if the right or left side of the colon was affected but was even less likely to be detected on the left side. Interpretation of the CT criteria under ICU conditions is much hindered, since most signs were found positive in patients of the control group without diagnosis of mesenteric ischemia due to fluid overload, capillary leakage, or administration of catecholamines. Although CT remains the first-line diagnostic imaging modality in patients with abnormal abdominal findings after cardiac surgery, negative signs should not prevent early laparotomy if clinical suspicion remains high.

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iDs

Henning Mothes

Stefan Ludewig

References

Wiesner

Khurana

, et al. CT of acute bowel ischemia. Radiology 2003; 226:635–650.

Oldenburg

Lau

Rodenberg

, et al. Acute Mesenteric Ischemia: A Clinical Review. JAMA Internal Med 2004; 164:1054–1062.

Thoeni

Cello

JP.

CT imaging of colitis. Radiology 2006; 240:623–638.

Kirkpatrick

Kroeker

Greenberg

HM.

Biphasic CT with mesenteric CT angiography in the evaluation of acute mesenteric ischemia: initial experience. Radiology 2003; 229:91–98.

Sheedy

Earnest

IVF

Fletcher

, et al. CT of small-bowel ischemia associated with obstruction in emergency department patients: diagnostic performance evaluation. Radiology 2006; 241:729–736.

Wiesner

Mortele

Glickman

, et al. Pneumatosis intestinalis and portomesenteric venous gas in intestinal ischemia: correlation of CT findings with severity of ischemia and clinical outcome. AJR Am J Roentgenol 2001; 177:1319–1323.

Goeller

Entwicklung und Optimierung eines CT-Scores zur objektiven Diagnosestellung einer Darmischämie bei intensivmedizinisch versorgten Patienten nach einer Herzoperation [dissertation]. Leipzig: Leipzig University, 2012.

Schneider

Leinung

Kloeppel

, et al. Die präoperative Dünnschicht-Computertomografie im Management der Lungenmetastasenchirurgie. Zentralblatt Chirurgie 2008; 133:568–573.

Klotz

Vestring

Roetker

, et al. Diagnosis and treatment of nonocclusive mesenteric ischemia after open heart surgery. Ann Thorac Surg 2001; 72:1583–1586.

10.

Caleb

Acute bowel ischemia after coronary bypass surgery - a catastrophic event. Singapore Med J 2001; 42:33–37.

11.

Ghosh

Roberts

Firmin

, et al. Risk factors for intestinal ischaemia in cardiac surgical patients. Eur J Card Thorac Surg 2002; 21:411–416.

12.

Hasan

Ratnatunga

Lewis

, et al. Gut ischaemia following cardiac surgery. Interactive Cardiovascul Thorac Surg 2004; 3:475–478.

13.

Tsiotos

Mullany

Zietlow

, et al. Abdominal complications following cardiac surgery. Am J Surg 1994; 167:553–557.

14.

Niederhaeuser

Genoni

von Segesser

, et al. Mesenteric ischemia after a cardiac operation: conservative treatment with local vasodilation. Ann Thorac Surg 1996; 61:1817–1819.

15.

Khan

Lambert

Habib

, et al. Abdominal complications after heart surgery. Ann Thorac Surg 2006; 82:1796–1801.

16.

Mayo-Smith

Wittenberg

Bennett

, et al. The CT small bowel faeces sign: description and clinical significance. Clin Radiol 1995; 50:765–767.

17.

Horton

Corl

Fishman

EK.

CT evaluation of the colon: inflammatory disease. Radiographics 2000; 20:399–418.

18.

Furukawa

Kanasaki

Kono

, et al. CT diagnosis of acute mesenteric ischemia from various causes. AJR Am J Roentgenol 2009; 192:408–416.

19.

Stahl

Busch

Maschke

, et al. A retrospective analysis of nonocclusive mesenteric ischemia in medical and surgical ICU patients: Clinical data on demography, clinical signs, and survival. J Intensive Care Med 2019. Doi: 10.1188/0885066619837911.

20.

Chou

CK.

CT manifestations of bowel ischemia. AJR Am J Roentgenol 2002; 178:87–91.

21.

Copin

Ronot

Nuzzo

, et al. Inter-reader agreement of CT features of acute mesenteric ischemia. Eur J Radiol 2018; 105:87–95.

22.

Alpern

Glazer

Francis

Ischemic or infarcted bowel: CT findings.

Radiol 1988; 166:149–152.

23.

Salzano

De Rosa

Carbone

, et al. Computerized tomography features of intestinal infarction: 56 surgically treated patients of which 5 with reversible mesenteric ischemia. Radiolog Med 1999; 97:246–250.

24.

Menke

Diagnostic accuracy of multidetector CT in acute mesenteric ischemia: systematic review and meta-analysis. Radiology 2010; 256:93–101.

25.

Barrett

Upponi

Benaglia

, et al. Multidetector CT findings in patients with mesenteric ischaemia following cardiopulmonary bypass surgery. Br J Radiol 2013; 86:20130277.