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DOI: 10.1148/radiol.2413050965
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(Radiology 2006;241:729-736.)
© RSNA, 2006

Emergency Radiology

CT of Small-Bowel Ischemia Associated with Obstruction in Emergency Department Patients: Diagnostic Performance Evaluation1

Shannon P. Sheedy, MD, Frank Earnest, IV, MD, Joel G. Fletcher, MD, Jeff L. Fidler, MD and Tanya L. Hoskin, MS

1 From the Division of Abdominal Imaging, Department of Radiology (S.P.S., F.E., J.G.F., J.L.F.) and Division of Biostatistics, Department of Health Sciences Research (T.L.H.), Mayo Clinic College of Medicine, Mayo W2, 200 First St SW, Rochester, MN 55905. Received June 8, 2005; revision requested August 3; revision received October 12; accepted November 14; final version accepted February 20, 2006. Address correspondence to F.E. (e-mail: earnest{at}mayo.edu).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Purpose: To retrospectively evaluate the diagnostic performance of computed tomography (CT) for detection of small-bowel ischemia in emergency department patients with abdominal pain and to compare the prospective interpretation with a retrospective interpretation by using surgical or pathologic findings as the reference standard.

Materials and Methods: The HIPAA–compliant study was approved by the institutional review board, and patients consented to research authorization. Sixty patients (61 examinations) (25 male, 35 female patients; median age, 67 years; range, 0.9–89.7 years) with acute abdominal pain underwent immediate abdominal and pelvic CT and subsequent surgery of the small bowel within 7 days of CT. Prospective radiologic reports were reviewed for diagnosis of small-bowel obstruction and ischemia. Two gastrointestinal radiologists performed blinded, independent, retrospective review of the CT studies with no clinical data other than presence of acute abdominal pain. The reviewers categorized CT signs of obstruction and ischemia and estimated diagnostic certainty. Discordant findings were resolved by consensus review by a third gastrointestinal radiologist. CT interpretations were compared with prospective interpretations and surgical or pathologic findings. Sensitivity and specificity estimates with confidence intervals were calculated. Fisher exact and {chi}2 tests were used to assess associations between CT signs and the diagnosis of ischemia; {kappa} statistics were used to estimate agreement between readers.

Results: In 27 (44%) of 61 CT studies, small-bowel ischemia was surgically or pathologically confirmed. Sensitivity and specificity for the diagnosis of ischemia were, respectively, 14.8% and 94.1% for prospective interpretations, 29.6% and 91.2% for reader 1, 40.7% and 85.3% for reader 2, and 51.9% and 88.2% for the consensus review. Decreased segmental enhancement was the most specific sign for small-bowel ischemia (P = .001), and its recognition would have improved the diagnostic performance of all readers. There was a significant association of the small-bowel feces sign with the presence of small-bowel ischemia (P = .046).

Conclusion: Diagnostic performance assessment of CT for the diagnosis of small-bowel ischemia revealed poor prospective interpretation sensitivity.

© RSNA, 2006


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Methods for evaluating the diagnostic performance for imaging seek to improve patient care by improving diagnostic accuracy. Problems inherent in accurately assessing diagnostic performance include biases introduced by selection of a patient cohort for review; retrospective availability of other patient data (data from previous or subsequent imaging studies, clinical data including surgical and endoscopic findings and reports, laboratory values, and pathologic reports); and the interest, practice experience, and thoroughness of the reviewing radiologist. Classification and adjudication of discordant interpretations or missed findings often lack a reference standard, such as endoscopic, surgical, or pathologic findings. Reported methods for review of quality assurance of imaging studies include both random identification of missed findings or discordant interpretations found during daily practice (1,2) and systematic review of quality assurance of some proportion of imaging studies (3). Random or sequential review of images, such as that from abdominal computed tomographic (CT) examinations performed in the emergency department, may not identify poor performance for disease processes with low prevalence (4). At present, there are no ideal methods for measuring quality of diagnostic imaging, and several strategies may be necessary to evaluate and measure performance.

Performance evaluation of emergent abdominal CT interpretations is particularly important because abdominal CT is relied on for rapid triage and management of acute nontraumatic abdominal pain (5). Small-bowel obstruction is a commonly encountered finding at emergent abdominal CT, and the accuracy of CT in the diagnosis of moderate or severe bowel obstruction has been demonstrated (5–9). The diagnosis of small-bowel ischemia in the presence of obstruction, however, remains more challenging; reported sensitivities are 75%–100%, and specificities are 61%–93% (10–13). The diagnosis of small-bowel ischemia has important implications for patient care because morbidity and mortality increase with delay in diagnosis (14,15). Thus, the purpose our study was to retrospectively evaluate the diagnostic performance of CT for detection of small-bowel ischemia in patients presenting with abdominal pain to an emergency department and to compare the prospective interpretation with a retrospective interpretation by using surgical or pathologic findings as the reference standard.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Patients
The study consisted of 61 CT examinations in 60 consecutive patients who met the criteria of having acute abdominal pain, who were evaluated in the emergency department between January 2000 and October 2002, who underwent emergent CT imaging of the abdomen and pelvis at initial evaluation, and who underwent a small-bowel surgical procedure for obstruction or segmental ischemia within 7 days of initial evaluation. The patient population included 25 male and 35 female patients aged 1–89 years (median age, 67 years). One patient underwent two separate episodes of care that met criteria for inclusion in the study.

During this same period, 7306 patients underwent emergent CT examination of the abdomen and pelvis requested from the emergency department. From this cohort, 533 patients in the emergency department underwent both emergent CT examination and an abdominal surgical procedure but were excluded from the study. Reasons for exclusion were surgery on portions of the gastrointestinal tract other than the small bowel (colon, esophagus, stomach, or proximal duodenum), surgery on gynecologic organs, surgery for primary mesenteric vascular disease (arterial or venous), and trauma. No patients were excluded on the basis of the cause of obstruction found at surgery. All of the patients had consented to research authorization for record review, and the study was approved by the institutional review board and was Health Insurance Portability and Accountability Act compliant.

CT Technique
CT examinations of the abdomen and pelvis were performed with one of two multisection CT scanners (LightSpeed QXi or LightSpeed Plus; GE Medical Systems, Milwaukee, Wis) by using 5-mm reconstruction thickness and 5-mm intervals through the abdomen and pelvis or with a single section helical scanner (Hi-Speed; GE Medical Systems) by using 7-mm reconstruction thickness and 7-mm intervals. Bowel opacification was accomplished by using 50–600 mL of 2% dilute oral meglumine diatrizoate solution (MD-Gastroview; Mallinckrodt, St Louis, Mo) and intravenous contrast medium enhancement was accomplished by using 20–140 mL of iohexol (300 mg of iodine per milliliter, Omnipaque 300; Nycomed Amersham, Princeton, NJ), iopamidol (300 mg of iodine per milliliter, Isovue 300; Squibb Diagnostics, New Brunswick, NJ), or ioversol (320 mg of iodine per milliliter, Optiray 320; Mallinckrodt) injected at 3 mL/sec. Image acquisition was performed during the portal venous phase after a 70-second scan delay. Smaller doses were given to infants or patients with decreased renal function. Intravenous contrast medium was withheld at the discretion of the radiologist, often because of renal impairment or allergy to contrast medium. Five patients received no oral or intravenous contrast medium, and six patients received only oral contrast medium. Five patients received only intravenous contrast medium, and 45 received both oral and intravenous contrast medium. Exposure technique was based on patient size.

Image Review
The names and identifying patient record numbers were electronically removed from all images for each CT examination prior to loading of the cases on a workstation for review (Advantage Windows Workstation, version 4.103; GE Medical Systems). The age and sex of the patient and the date of the CT examination were not removed. Two experienced gastrointestinal radiologists (J.G.F., 5 years of experience in abdominal imaging and J.L.F., 9 years of experience in abdominal imaging) independently reviewed each CT study and were blinded to patient identification and all clinical information, including surgical or pathologic diagnosis. The radiologists knew all patients presented to the emergency department with acute abdominal pain and subsequently underwent surgery of the small bowel within the next 7 days but did not know the specific indication for the surgical procedure.

Images from each examination were specifically evaluated for CT signs of bowel obstruction and segmental ischemia or strangulation, including (a) subjective presence of circumferential bowel-wall thickening; (b) bowel-wall edema determined by the presence of submucosal edema with a visible target or halo sign; (c) presence of any intramural gas; (d) extraalimentary air; (e) portal venous or mesenteric venous gas; (f) increased attenuation of the bowel wall, compared with attenuation of adjacent bowel-wall segments in the absence of intravenous contrast enhancement; (g) subjective decreased relative enhancement of the bowel wall, compared with other bowel-wall segments after intravenous contrast enhancement; (h) presence of mesenteric fluid, defined as hazy fluid attenuation, in the mesentery adjacent to the involved segment of small bowel; (i) presence of mesenteric vascular engorgement, defined as relative dilatation of mesenteric vessels; (j) a transition point of small-bowel obstruction; (k) presence of a C- or U-shaped loop of small bowel suggesting a closed loop obstruction or volvulus; (l) presence of ascites, defined as any peritoneal fluid in men or more than a small quantity of cul-de-sac fluid in women; and (m) presence of mottled intraluminal gas and debris within the small-bowel lumen (small-bowel feces sign) (16,17).

The reviewers also had to specifically comment regarding a diagnosis of obstruction, ischemia, or both and commit to a subjective estimation of diagnostic certainty by using four categories (not present, possible, probable, or definite). A blinded consensus review of each case was conducted by a third radiologist (F.E., 10 years of experience in abdominal imaging) to resolve discrepancies, and these consensus readings were also used for analysis.

Reference Standard
The patients' charts were reviewed retrospectively (S.P.S., F.E.). Surgical or pathologic diagnosis of small-bowel obstruction, ischemia, or both was the reference standard for this study. When the presence or absence of small-bowel dilatation was not noted on surgical reports, the consensus CT interpretation of bowel obstruction was considered the reference standard for evaluation of the prospective CT interpretations. Other surgical or pathologic observations were recorded, including the presence of small-bowel obstruction, closed loop obstruction, or volvulus. The original CT reports were reviewed for specific comments regarding the presence or absence of obstruction, presence of a closed loop obstruction or volvulus, or bowel ischemia. The time between the CT examination and surgery was determined from the time recorded on the CT examination and anesthesia records. The interval between CT and abdominal surgery ranged from 1 hour 31 minutes to 175 hours 42 minutes.

Five patients underwent additional abdominal and pelvic CT examination during the 7-day interval, and only their initial CT studies from the emergency department were included in this study. Forty-three (70%) patients had undergone previous bowel surgery. Twenty-four (39%) patients were known to have enteric disease, including six with inflammatory bowel disease, seven with a personal history of colon cancer, five with diverticulosis, four with a history of small-bowel obstruction, one with a metastatic carcinoid, and one with a history of both transverse colon and sigmoid volvulus. Two patients had a personal history of prostate cancer, and three had a history of transitional cell carcinoma of the bladder.

Statistical Analysis
Statistical analyses were performed by using software (SAS, version 8.2; SAS Institute, Cary, NC,). Descriptive statistics were reported as mean and standard deviation or median and range for continuous variables. Categoric variables were reported with frequencies and percentages. A P value of less than .05 was considered to indicate a statistically significant difference for all analyses.

Sensitivity and specificity for the diagnosis of small-bowel ischemia were estimated by using surgical or pathologic findings as the reference standard. Estimates were reported with 95% exact binomial confidence intervals. The data were analyzed overall and separately for patients who underwent surgery within 24 hours of CT and those who underwent surgery more than 24 hours after CT. Results are reported both for the prospective and the retrospective interpretation.

Interobserver agreement for binary CT signs, such as presence or absence of bowel-wall thickening, was assessed with unweighted {kappa} statistics. Weighted {kappa} statistics were used to assess agreement between readers for CT variables collected by using ordinal scales. Unweighted and weighted {kappa} statistics were interpreted by using the following scale: fair agreement, 0.21–0.40; moderate agreement, 0.41–0.60; substantial agreement, 0.61–0.80; and almost perfect agreement, 0.81–1.0 (18). Ninety-five percent confidence intervals were reported for each estimated {kappa} statistic.

The association between each CT sign and small-bowel ischemia was assessed by using {chi}2 or Fisher exact tests, as appropriate. For these analyses, the response was small-bowel ischemia (yes or no) as determined with surgical or pathologic findings. The independent variables of interest were CT signs based on the consensus reading. In addition, the sensitivity and specificity of each sign, based on the consensus review, were estimated.

Although our sample size was too small to perform a complete multiple variable analysis, limited exploratory analyses were performed. Recursive partitioning with software (Splus, version 6.2; Insightful, Seattle, Wash) was performed to identify variables and interactions that might be important for classifying ischemia (yes or no) in this patient group.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Surgical Findings
Of the 61 CT imaging studies (Table 1), 27 (44%) showed segmental small-bowel ischemia. Thirty-six patients underwent abdominal surgery within 24 hours of CT examination. Twenty-one (58%) of the 36 patients had an ischemic small-bowel at surgery. The remaining patients underwent surgery more than 24 hours after CT examination, and six (24%) patients had small-bowel ischemia.


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  		Table 1. Characteristics of 60 Patients Who Underwent CT for Depiction of Small-Bowel Ischemia

 
Small-bowel obstruction was not a specific criterion for inclusion in this study, so as not to exclude patients with segmental ischemia without bowel dilatation. The presence or absence of bowel obstruction was not specifically noted in 18 of 61 surgical notes. For these studies, the consensus CT reading was used to assess the prospective interpretation. Small-bowel obstruction with bowel dilatation was confirmed at surgery or at consensus CT reading in 56 of 61 studies.

Imaging Findings
Prospective CT interpretation of small-bowel obstruction demonstrated a sensitivity of 88% (49 of 56) and specificity of 60% (three of five). There were seven studies with small-bowel obstruction and bowel dilatation not described at the prospective CT interpretation. In retrospect, four of seven studies demonstrated small-bowel obstruction at consensus reading. On three studies, small-bowel obstruction was not apparent at prospective or retrospective CT interpretation. One of these patients had a perforation with free air, and two patients had intervals of 109 hours and 139 hours between CT examination and surgery. There were two studies with small-bowel obstruction and dilatation described at prospective CT interpretation with no findings of obstruction apparent at surgery. In retrospect, one study did not demonstrate findings of small-bowel dilatation and obstruction at consensus review. In another study with a false-positive prospective interpretation of small-bowel obstruction, the patient had an interval of 175 hours between CT examination and surgery.

Table 2 shows the performance of prospective interpretation and retrospective blinded review for the study group as a whole and for the subgroups of those who underwent surgery within 24 hours of emergent CT and those who underwent surgery more than 24 hours after CT. By using the consensus data, sensitivity and specificity were calculated for each CT sign for diagnosis of small-bowel ischemia (Table 3).


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  		Table 2. Sensitivity and Specificity for Diagnosis of Small-Bowel Ischemia in 61 CT Cases of Prospective and Retrospective Review

 

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  		Table 3. Sensitivity and Specificity for CT Signs at 61 CT Examinations

 
Two CT signs had a statistically significant association with small-bowel ischemia (P < .05): decreased enhancement of the bowel wall after administration of intravenous contrast material and presence of the small-bowel feces sign (Figs 1, 2; Table 3). In the 61 studies, intravenous contrast enhancement was used in 50 and 18 of these showed an ischemic bowel at surgical findings or pathologic findings. Decreased enhancement of the bowel wall (Fig 1) was the most specific sign of an ischemic bowel, with no false-positive findings and six true-positive findings. The presence of the small-bowel feces sign was significantly associated with small-bowel ischemia (Fig 2). When comparing the <24-hour group with the >24-hour group, closed loop obstruction or volvulus approached a statistically significant association with the presence of small-bowel ischemia in the <24-hour group (P = .08) (Table 3). Ten of 27 CT studies with ischemia demonstrated CT signs of a volvulus or closed loop obstruction, and seven of 34 without ischemia had CT signs of closed loop obstruction. All other CT signs had no significant association with the diagnosis of small-bowel ischemia.


Figure 1
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  		Figure 1: Contrast-enhanced transverse CT image through lower abdomen demonstrates multiple dilated bowel loops and diminished bowel-wall enhancement (white arrowheads) in jejunal loops relative to that of adjacent contrast-enhanced loops (black arrowheads). A 30-cm segment of ischemic jejunum was resected 4 hours after CT.

 

Figure 2
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  		Figure 2: Contrast-enhanced transverse CT image through pelvis demonstrates closed loop obstruction and twisting of bowel mesentery (white arrow), diminished bowel-wall enhancement (white arrowheads), and presence of small-bowel feces sign (black arrowheads). Necrotic segment of ileum, twisted beneath an adhesive band, was resected 5 hours after CT.

 
Interobserver Agreement
There was substantial interobserver agreement (Table 4) between the individual readers for the presence of the small-bowel feces sign and ascites. There was moderate agreement for the diagnosis of small-bowel ischemia, bowel-wall edema with a target or halo sign, bowel-wall thickening, presence of mesenteric fluid, and signs of a closed loop obstruction or volvulus. There was only fair interobserver agreement between the blinded readers for mesenteric vascular engorgement and identification of a transition point. There was generally substantial or almost perfect interobserver agreement between the blinded readers and the consensus reading.


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  		Table 4. Interobserver Agreement Among Readers for Diagnosis of Small-Bowel Ischemia with CT Signs

 
Prospective and Retrospective Interpretations
Recognition of decreased bowel-wall enhancement would have substantially improved the performance for prospective interpretation of small-bowel ischemia from 14.8% to 33.3% (Table 5). Multivariate analysis of the CT signs, although somewhat limited because of sample size, was also performed by using recursive partitioning to determine the best strategy for diagnosis of small-bowel ischemia. The algorithm identified important variables of older age (≥46.4 years), presence of bowel edema, and presence of the small-bowel feces sign. The sensitivity of this algorithm was 63.0% (95% confidence interval: 42.4, 80.6), and the specificity was 79.4% (95% confidence interval: 62.1, 91.3). When compared with the consensus reading, this algorithm increased sensitivity by 11.1% and decreased specificity by 8.8%.


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  		Table 5. Improvement in Sensitivity for Diagnosis of Small-Bowel Ischemia with the Assumption of Consensus Recognition of Decreased Bowel-Wall Enhancement

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
 References
 
Previous investigations have revealed the accuracy of CT for the diagnosis of bowel ischemia among hospitalized patients suspected of having a small-bowel obstruction (10–12,19). The reported sensitivity of CT for the diagnosis of bowel ischemia ranged from 76% (10) to 100% (11), with the respective specificities of 93% and 61%. These investigations differed in inclusion criteria, proportion of patients undergoing surgery, proportion of studies without contrast enhancement, and the inclusion of nonsurgical patients for statistical analysis.

Prior investigations have revealed good sensitivity for detection of ischemia in the setting of small-bowel obstruction when using two or more CT signs as a positive indicator (10,11). In our investigation, however, if these criteria had been used, 23 of the 27 CT patient studies with ischemia would have been identified as such (sensitivity, 85%). These criteria, however, would have correctly helped identify only eight of 34 CT patient studies without ischemia (specificity, 24%).

Reduced segmental bowel-wall enhancement was 100% specific for the diagnosis of segmental small-bowel ischemia. This CT sign was present in only six of 18 studies with ischemia and contrast-enhanced CT images (sensitivity, 33.3%). If the radiologists performing prospective interpretation had recognized decreased bowel-wall enhancement as did the consensus group, they would have substantially increased sensitivity for identifying patients with segmental bowel ischemia.

On the basis of our findings, we are exploring methods for improving our diagnostic performance for detection of small-bowel ischemia and decreased bowel-wall enhancement. These methods include choosing either no oral contrast medium or neutral oral contrast medium, with emphasis on the use of intravenous contrast medium when small-bowel ischemia is suspected, and examination of the small-bowel at window settings that better depict differences in bowel-wall enhancement. With the addition of 64–detector row CT scanners in our hospital practice, we anticipate better resolution due to decreased motion and acquisition time and more advantageous depiction of bowel pathologic findings demonstrated in orthogonal planes at full resolution. The use of arterial phase imaging has been shown to be helpful in patients with arterial abnormalities associated with primary mesenteric vascular disease (20) and could improve bowel-wall enhancement (21). It may not be useful to obtain multiple acquisitions in the majority of patients being evaluated for acute abdominal pain in the emergency department because it will increase radiation dose and may not improve detection of small-bowel ischemia associated with obstruction.

An unexpected sign that proved to have a statistically significant association with small-bowel ischemia was the small-bowel feces sign. This sign, first reported by Mayo-Smith et al (16), is associated with obstruction, as well as with undigested food, secondary bacterial growth, and water absorption proximal to an obstruction. Perhaps the presence of a phytobezoar just proximal to an obstruction imparts different mechanical properties than does fluid in the distended bowel lumen and contributes to the development of ischemia.

Limitations of this study included those associated with selecting the sample, the analysis criteria, and the reference standards. Only patients who presented with abdominal symptoms to the emergency department underwent CT requested from the emergency department and underwent small-bowel surgery within the next 7 days were included. There was a large proportion of studies with small-bowel ischemia (44%). Patients who did not undergo emergent CT or surgery were excluded.

Record review of the prospective reports was performed by using specific terms for obstruction and ischemia. Even if many CT signs suggesting small-bowel ischemia were described, the report was considered to conclude a negative finding for ischemia if the possible diagnosis of small-bowel ischemia was not explicitly recorded. Criteria for CT signs were subjective, and we relied on the experience and judgment of the reviewer. This undoubtedly resulted in reduced interobserver agreement for several signs, particularly identification of mesenteric vascular engorgement or identification of a transition point in the caliber of the small bowel. There was also a difference between the readers in the identification of decreased bowel-wall enhancement that resulted in a reduced sensitivity for diagnosis of small-bowel ischemia.

For the reference standard of surgical or pathologic findings, we relied on the accuracy of observations and completeness of these records for each patient. In some cases, the surgeon resected bowel thought to be ischemic but the resected bowel had no pathologic findings of ischemia. Identification of closed loop obstruction was dependent on the surgical dissection, and extensive adhesiolysis may have complicated the identification of closed loop obstruction in some patients. From a statistical perspective, our sample size was too small to fully explore multiple variable prediction of small-bowel ischemia, and we were therefore limited primarily to univariate analysis.

In conclusion, the prospective sensitivity of CT for identifying segmental small-bowel ischemia in patients in our emergency department was much lower than that of previously published reports. Decreased segmental bowel-wall enhancement and the presence of the small-bowel feces sign were significantly associated with small-bowel ischemia in patients who were found to have small-bowel ischemia at surgery. Maximizing bowel-wall enhancement and accurately identifying decreased segmental bowel-wall enhancement, as well as explicitly communicating suspected small-bowel ischemia, should substantially improve the diagnostic performance.


   ADVANCES IN KNOWLEDGE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
References
 


   FOOTNOTES
 
Authors stated no financial relationship to disclose.

Author contributions: Guarantors of integrity of entire study, S.P.S., F.E.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, S.P.S., F.E.; clinical studies, S.P.S., F.E., J.G.F.; statistical analysis, S.P.S., F.E., T.L.H.; and manuscript editing, all authors


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 

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