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DOI: 10.1148/radiol.2362040299
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(Radiology 2005;236:712-715.)
© RSNA, 2005

Ultrasonography

Evaluation of Bowel Ischemia with Contrast-enhanced US: Initial Experience1

Jiro Hata, MD, PhD, Tomoari Kamada, MD, PhD, Ken Haruma, MD, PhD and Hiroaki Kusunoki, MD, PhD

1 From the Departments of Clinical Pathology (J.H.) and Internal Medicine, Division of Gastroenterology (T.K., K.H., H.K.), Kawasaki Medical School, 577 Matsushima, Kurasiki, Okayama 701-0192, Japan. Received February 18, 2004; revision requested April 23; final revision received October 3; accepted October 12. Address correspondence to J.H. (e-mail: ultrajiro{at}nifty.com).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To prospectively evaluate the accuracy of contrast material–enhanced ultrasonography (US) in the depiction of bowel ischemia in patients with radiographic evidence of small-bowel dilatation.

MATERIALS AND METHODS: The ethics committee approved this study, and informed consent was obtained from all patients. Fifty-one patients (34 men and 17 women; mean age, 67.1 years) with evidence of small-bowel dilatation at conventional radiography were enrolled. Twenty patients had bowel ischemia (15 cases of bowel strangulation and five of thromboembolism of the superior mesenteric artery) and 31 patients had simple obstruction. After injection of SHU-508A, the most dilated or the least peristaltic bowel segments were imaged at contrast-enhanced power Doppler US (interval, 4 seconds) for 2 minutes. Color signals obtained in the bowel wall were classified as normal, diminished, or absent. Contrast-enhanced US and classification of color signals were performed by a sonologist. The US systems were equipped with 3–12-MHz transducers. Fisher exact test was used to evaluate the significance of the differences between each group of patients, and P < .01 was considered to indicate a significant difference.

RESULTS: The color signals were absent in five patients with superior mesenteric arterial thromboembolism and in seven patients with strangulation, were diminished in five patients with strangulation, and were normal in three patients with strangulation and in 31 patients with simple obstruction. By pooling the absent and diminished color signals together as a diagnostic indicator of bowel ischemia, the sensitivity was 85% (95% confidence interval [CI]: 62.1%, 96.8%), the specificity was 100% (95% CI: 90.8%, 100%), the positive predictive value was 100% (95% CI: 83.8%, 100%), the negative predictive value was 91.2% (95% CI: 76.3%, 98.1%), the likelihood ratio for a positive test result was infinity, and the likelihood ratio for a negative test result was 0.15 (95% CI: 0.032, 0.379).

CONCLUSION: Contrast-enhanced US shows promise for the noninvasive diagnosis of bowel ischemia based on initial experience in patients with radiographic evidence of small-bowel dilatation.

© RSNA, 2005


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Bowel ischemia is a potentially fatal disorder often caused by vascular embolism and bowel strangulation. While a patient with this disorder may complain of severe abdominal pain, establishing the diagnosis is not necessarily easy owing to the lack of specific physical or laboratory findings (1). Although the definitive diagnosis is usually established at angiography, this method is not always executed easily and is not suitable for the evaluation of patients who are only suspected of having the disease. In contrast, transabdominal ultrasonography (US) is regarded as a noninvasive method for the diagnosis of gastrointestinal diseases. However, conventional Doppler US is not necessarily suitable for the evaluation of gastrointestinal microperfusion because the flow velocity and signal power are often under the rejection level of the high-pass filter (2). Within the past few years, it has become possible to evaluate transmural bowel wall perfusion at scanning after the injection of SHU-508A (3,4). Thus, the aim of this study was to prospectively investigate the accuracy of contrast material–enhanced US for the depiction of bowel ischemia in patients with radiographic evidence of small-bowel dilatation.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Patients
The ethics committee of our institution approved this study. Informed consent was obtained from all patients who participated in the study.

Among patients with evidence of small-bowel dilatation at conventional radiography who were seen at our hospital between January 2000 and March 2003, 51 patients also underwent US and were enrolled in this study. Decision to perform contrast-enhanced US was made by the attending physician (emergency department), based on the availability of US apparatus, as well as the sonologist and patient's consent. Small-bowel dilatation was defined as a distended bowel loop with air-fluid levels at conventional radiography. A radiologist with expertise in abdominal radiographic examinations interpreted the radiographs.

Twenty patients (14 men and six women; mean age, 65.3 years) had bowel ischemia, while 31 patients (20 men and 11 women; mean age, 68.2 years) had small-bowel dilatation because of obstruction caused by cancer (n = 7) or adhesions as a result of previous surgery (n = 24). There were no significant differences in sex and age distribution between patients with ischemia and patients with obstruction on the basis of the Student t test. Twenty-three patients, including seven patients with colon cancer, were treated successfully with nasointestinal drainage, while eight patients required surgery for the resection of adhesive lesions. The causes of bowel ischemia were bowel strangulation in 15 patients and thromboembolism of the superior mesenteric artery in five patients. Definitive diagnosis was established at the time of surgery (n = 18) and/or autopsy (n = 2) in patients with bowel ischemia. For patients with obstruction, computed tomography (CT) (n = 10), contrast-enhanced (Gastrografin; Nihon Schering, Osaka, Japan) studies (n = 14), or colonoscopy (n = 7), together with clinical course, established the diagnosis. Patients with disseminated intravascular coagulation (n = 1) or severe cardiac failure (n = 1) were excluded from the study since such conditions may alter tissue microcirculation. All of the patients were suitable for the adequate US studies.

US Technique and Interpretation
All patients underwent contrast-enhanced US immediately after patient history and physical findings were obtained by the attending physician (a gastroenterologist). Contrast-enhanced US was performed by a sonologist (J.H.) with 20 years of experience in gastrointestinal US. The sonologist was blinded to the results of other diagnostic tests except for the abdominal radiograph. The time between the appearance of the patient's symptoms and the hospital visit ranged from 1 to 55 hours (mean, 9.8 hours ± 9.2 [standard deviation]).

No special preparations, such as the injection of a spasmolytic or water instillation into the bowel lumen, were performed. First, US of the entire abdomen was performed for 10 minutes to detect any distended small-bowel loops. A distended small-bowel loop was defined as a segment showing more than 2 cm in diameter and a to-and-fro movement of bowel contents. In cases in which intraluminal gas interfered with imaging of the posterior wall of the bowel loop, only the anterior wall was examined. SHU-508A (1500 mg/5 mL, Levovist; Schering, Berlin, Germany) flushed with saline was injected intravenously for 10 seconds. Immediately after injection, the most dilated or the least peristaltic small-bowel segments were scanned with US for 2 minutes. The US systems (SSA-390A and 770A; Toshiba, Tokyo, Japan) were equipped with 3–12-MHz transducers. The imaging parameters were set as follows: mechanical index of 1.0–1.2, dynamic range of 50 dB, velocity range of 57.6 cm, and high-pass power Doppler filter cutoff of 130 Hz. The scanning interval was 4 seconds, and monitoring was performed with a low mechanical index to avoid destroying the microbubbles between each scanning. Contrast-enhanced US procedures were recorded on videotape and reviewed immediately after each study by the sonologist blinded to the clinical information to classify the color signals, which required approximately 3 minutes.

The color signals were classified as normal when the signals were similar to those in a normal bowel segment or in the stomach when the entire small bowel was affected, diminished when the signals were weaker than those in a normal bowel segment, or absent when no color signals were observed. Figure 1 shows the color signals. When more than one type of signal was observed, the signal with the poorest enhancement was used. We diagnosed a bowel loop as ischemic when the color signals were diminished or absent.



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  		Figure 1. US scan obtained in a 68-year-old man with bowel strangulation. Bowel segments show normal (A), diminished (B), and absent (C) color signals.

 
Statistical Analysis
We performed an accuracy assessment for the diagnosis of bowel ischemia by using KaleidaGraph software (version 3.6; Synergy Software, Reading, Pa). The reference standard was the final diagnosis. The bowel segments showing diminished and absent color signals were diagnosed as bowel ischemia at contrast-enhanced US. Fisher exact test was used to evaluate the significance of the differences between each group of patients, and P < .01 was considered to indicate a significant difference.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Results are shown in the Table. Normal color signals were observed in 34 patients, including all 31 patients with simple obstruction. Figure 2 shows representative US findings in patients with simple obstruction. In contrast, three patients with normal color signals had bowel strangulation requiring emergent surgery.


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  		TABLE 1. Classification of Color Signals for Each Disease

 


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  		Figure 2. Contrast-enhanced US findings in a 35-year-old woman with simple obstruction. Sagittal view of the middle portion of lower abdomen shows that color signals are normal in the bowel wall.

 
Five patients had diminished color signals. All of them had bowel strangulation requiring emergent surgery. Figure 3 shows examples of bowel segments with diminished or absent color signals in a patient with strangulation. Twelve patients had absent color signals. Seven patients had strangulation requiring bowel resection. Five patients had superior mesenteric arterial thromboembolism. Figure 4 shows absent color signals in the bowel wall of a patient with superior mesenteric arterial thromboembolism. The color signals seen between bowel loops are from mesenteric vessels and not the vessels in the bowel wall. Since our criteria are based on the intramural flow signals, this figure indicates the absent pattern. Two patients required bowel resection, while two patients underwent arterial thrombectomy. One patient whose onset of symptoms was 2 days before the examination died of multiple organ failure. No patient with simple obstruction had diminished or absent color signals in this study.



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  		Figure 3. Contrast-enhanced US findings of bowel segments in a 72-year-old man with bowel strangulation. Transverse view of the right portion of lower abdomen shows that the segment without strangulation has normal (A) color signal in the bowel wall, whereas the segment with ischemia has diminished (B) and absent (C) color signals.

 


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  		Figure 4. Contrast-enhanced US findings in a 78-year-old woman with superior mesenteric arterial thromboembolism. Transverse view of left upper quadrant shows that color signals are absent in all bowel segments.

 
By using diminished color signals as an independent diagnostic indicator of bowel ischemia against normal color signals, the sensitivity was 62.5% (95% confidence interval [CI]: 24.5, 94.1%), the specificity was 100% (95% CI: 90.8, 100%), the positive predictive value was 100% (95% CI: 54.9, 100%), the negative predictive value was 91.2% (95% CI: 76.3, 98.1%), the accuracy was 92.3%, the likelihood ratio for a positive test result was infinity, the likelihood ratio for a negative test result was 0.375 (95% CI: –0.085, 0.762), and the P value was less than.001. By using absent color signals as independent threshold against normal color signals, the sensitivity was 80% (95% CI: 51.9%, 95.7%), the specificity was 100% (95% CI: 90.8%, 100%), the positive predictive value was 100% (95% CI: 77.9%, 100%), the negative predictive value was 91.2% (95% CI: 76.3%, 98.1%), the accuracy was 93.5%, the likelihood ratio for a positive test result was infinity, the likelihood ratio for a negative test result was 0.2 (95% CI: 0.043, 0.481), and the P value was less than .001. By pooling the absent and diminished color signals together as a diagnostic indicator of bowel ischemia, the sensitivity was 85% (95% CI: 62.1%, 96.8%), the specificity was 100% (95% CI: 90.8%, 100%), the positive predictive value was 100% (95% CI: 83.8%, 100%), the negative predictive value was 91.2% (95% CI: 76.3%, 98.1%), the accuracy was 94.1%, the likelihood ratio for a positive test result was infinity, the likelihood ratio for a negative test result was 0.15 (95% CI: 0.032, 0.379), and the P value was less than .001.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
Findings of this study showed that contrast-enhanced US is a highly effective tool for the detection of bowel ischemia. To our knowledge, this is the first study to evaluate bowel ischemia with contrast-enhanced US.

Although early diagnosis of bowel ischemia is essential in the management of acute abdominal pain, it has been difficult to establish this diagnosis owing to the lack of typical physical, laboratory, and radiographic findings. Contrast-enhanced CT is one of the methods used for the diagnosis of this disorder (5,6). However, the contrast agents used in CT promptly move into the extravascular space, which results in difficulty differentiating between mild ischemia and congestion. In addition, radiation exposure and the potential renal toxicity of the contrast agents remain a concern. Magnetic resonance imaging has been reported to be another useful method for detecting bowel ischemia (7,8).

There have been many studies about the US assessment of bowel wall blood flow (9–12). However, most studies are conducted by using color and/or power Doppler US, which has limitations in depicting slow and small amounts of blood flow seen in the mucosal layer of the gastrointestinal wall. In contrast, contrast-enhanced US depicts microperfusion of the gastrointestinal wall as a strong signal produced by the destruction of microbubbles. The scanning method using harmonic imaging was introduced initially in liver studies and was referred to as "flash-echo imaging." With this method, microbubbles reach the target tissues without being destroyed by the ultrasound energy. Recently, US scanning with modalities such as color Doppler, power Doppler, and advanced dynamic flow (wide-band power Doppler imaging) for the visualization of microbubble destruction has become available. The strong color signals obtained with Doppler US are not dependent on blood-flow velocity because the frequency shifts are produced by bubble destruction (loss of correlation) (13). In this study, we advocated the use of the term contrast-enhanced US to include all modalities used for scanning.

There were several limitations in this study. First, the assessment of color signals was subjective. Second, interobserver agreement was not assessed. Contrast-enhanced US requires considerable experience, and thus duplication of our results may vary. Third, the exclusion of patients with disseminated intravascular coagulation and cardiac failure may have biased our results. In addition, our results may not be generalizable to patients with disseminated intravascular coagulation, acute and/or chronic cardiac failure, microcirculatory diseases, or obesity.

Further studies with a greater number of patients are needed to determine the effectiveness of contrast-enhanced US in the differentiation between early strangulation and simple obstruction. Use of a shorter scanning interval (eg, 2 seconds) and generating a time-intensity curve to detect subtle changes in blood-flow dynamics might help differentiate the two entities.

In conclusion, contrast-enhanced US is a promising tool for the assessment of bowel ischemia in patients with radiographic evidence of small-bowel dilatation. By taking the noninvasive nature of the test into account, this method has potential for application in daily practice as a diagnostic method for bowel ischemia.


   FOOTNOTES
 

Abbreviations: CI = confidence interval

Authors stated no financial relationship to disclose.

Author contributions: Guarantor of integrity of entire study, J.H.; study concepts and design, J.H.; literature research, T.K.; clinical studies, J.H.; data acquisition, H.K.; data analysis/interpretation, K.H.; statistical analysis, K.H.; manuscript preparation, definition of intellectual content, and editing, J.H.; manuscript revision/review and final version approval, K.H.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

  1. Danse EM, Van Beers BE, Jamart J, et al. Prognosis of ischemic colitis: comparison of color Doppler sonography with early clinical and laboratory findings. AJR Am J Roentgenol 2000; 175:1151–1154.[Abstract/Free Full Text]
  2. Mizushige K, Ueda T, Yuba M, et al. Dependence of power Doppler image on high pass filter instrumented in ultrasound machine. Ultrasound Med Biol 1999; 25:1389–1393.[CrossRef][Medline]
  3. Yoshida S, Hata J, Haruma K, et al. Evaluation of flash echo imaging of the canine gastrointestinal tract. J Ultrasound Med 2000; 19:751–755.[Abstract]
  4. Okanobu H, Hata J, Haruma K, et al. Preoperative assessment of gastric cancer vascularity by flash echo imaging. Scand J Gastroenterol 2002; 37:608–612.[CrossRef][Medline]
  5. Wiesner W, Khurana B, Ji H, et al. CT of acute bowel ischemia. Radiology 2003; 226:635–650.[Abstract/Free Full Text]
  6. Kim AY, Ha HK. Evaluation of suspected mesenteric ischemia: efficacy of radiologic studies. Radiol Clin North Am 2003; 41:327–342.[CrossRef][Medline]
  7. Wilkerson DK, Mezrich R, Drake C, et al. Magnetic resonance imaging of acute occlusive intestinal ischemia. J Vasc Surg 1990; 11:567–571.[CrossRef][Medline]
  8. Chan FP, Li KC, Heiss SG, et al. A comprehensive approach using MR imaging to diagnose acute segmental mesenteric ischemia in a porcine model. AJR Am J Roentgenol 1999; 173:523–529.[Abstract/Free Full Text]
  9. Okada T, Yoshida H, Iwai J, et al. Pulsed Doppler sonography for the diagnosis of strangulation in small bowel obstruction. J Pediatr Surg 2001; 36:430–435.[CrossRef][Medline]
  10. Danse EM, Laterre PF, Van Beers BE, et al. Early diagnosis of acute intestinal ischaemia: contribution of colour Doppler sonography. Acta Chir Belg 1997; 97:173–176.[Medline]
  11. Danse EM, Van Beers BE, Goffette P, et al. Acute intestinal ischemia due to occlusion of the superior mesenteric artery: detection with Doppler sonography. J Ultrasound Med 1996; 15:323–326.[Abstract]
  12. Teefey SA, Roarke MC, Brink JA, et al. Bowel wall thickening: differentiation of inflammation from ischemia with color Doppler and duplex US. Radiology 1996; 198:547–551.[Abstract/Free Full Text]
  13. Calliada F, Campani R, Bottinelli O, et al. Ultrasound contrast agents: basic principles. Eur J Radiol 1998; 27(suppl 2):S157–S160.[CrossRef]



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