Published online before print March 23, 2007, 10.1148/radiol.2432060534
(Radiology 2007;243:438-444.)
© RSNA, 2007
Multi–Detector Row CT of the Small Bowel: Peak Enhancement Temporal Window—Initial Experience1
Sebastian T. Schindera, MD,
Rendon C. Nelson, MD,
David M. DeLong, PhD,
Tracy A. Jaffe, MD,
Elmar M. Merkle, MD,
Erik K. Paulson, MD, and
John Thomas, MD
1 From the Department of Radiology, Duke University Medical Center, Box 3808, Erwin Rd, Durham, NC 27710. Received March 25, 2006; revision requested May 24; revision received June 25; accepted July 21; final version accepted September 27. Supported by a grant from E-Z-Em, Westbury, NY.
Address correspondence to R.C.N. (e-mail: rendon.nelson{at}duke.edu).
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ABSTRACT
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Purpose: To prospectively determine quantitatively and qualitatively the timing of maximal enhancement of the normal small-bowel wall by using contrast material–enhanced multi–detector row computed tomography (CT).
Materials and Methods: This HIPAA-compliant study was approved by the institutional review board. After information on radiation risk was given, written informed consent was obtained from 25 participants with no history of small-bowel disease (mean age, 58 years; 19 men) who had undergone single-level dynamic CT. Thirty seconds after the intravenous administration of contrast material, a serial dynamic acquisition, consisting of 10 images obtained 5 seconds apart, was performed. Enhancement measurements were obtained over time from the small-bowel wall and the aorta. Three independent readers qualitatively assessed small-bowel conspicuity. Quantitative and qualitative data were analyzed during the arterial phase, the enteric phase (which represented peak small-bowel mural enhancement), and the venous phase. Statistical analysis included paired Student t test and Wilcoxon signed rank test with Bonferroni correction. A P value less than .05 was used to indicate a significant difference.
Results: The mean time to peak enhancement of the small-bowel wall was 49.3 seconds ± 7.7 (standard deviation) and 13.5 seconds ± 7.6 after peak aortic enhancement. Enhancement values were highest during the enteric phase (P < .05). Regarding small-bowel conspicuity, images obtained during the enteric phase were most preferred qualitatively; there was a significant difference between the enteric and arterial phases (P < .001) but not between the enteric and venous phases (P = .18).
Conclusion: At multi–detector row CT, peak mural enhancement of the normal small bowel occurs on average about 50 seconds after intravenous administration of contrast material or 14 seconds after peak aortic enhancement.
© RSNA, 2007
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INTRODUCTION
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Until recently, fluoroscopic small-bowel follow-through and enteroclysis were considered the diagnostic imaging modalities of choice for small-bowel disorders. However, progressive advances in multi–detector row computed tomography (CT) in the past few years have led to dramatic changes in diagnostic algorithms involving the small bowel (1–7).
As the number of detector channels has increased steadily from four to 64, application of thin collimation (0.5–0.75 mm) has become a routine part of multi–detector row CT. This submillimeter configuration allows for reformation in any desired plane, with spatial resolution similar to that obtained in the transverse plane. These multiplanar reformations are particularly valuable for evaluation of the small bowel, with its long and tortuous course (5–6 m) (1). Another important advance of multi–detector row CT scanners is the substantial increase in scanning speed, which allows coverage of the entire small bowel during different enhancement phases after the bolus administration of intravenous contrast material.
Besides the technical advances of multi–detector row CT, adequate luminal distention and mural enhancement are essential for the precise diagnosis of small-bowel abnormalities, including small-bowel obstruction, Crohn disease, ischemia, and neoplasia. Small-bowel loops are distended by means of ingestion of oral contrast material, whereas the enhancement of the small-bowel wall depends on the intravenous administration of a contrast agent. To date, the timing of CT protocols for imaging the small bowel has been mainly based on experience with hepatic enhancement phases rather than on a dedicated small-bowel protocol. Although most radiologists image the small bowel with contrast material–enhanced multi–detector row CT during the arterial phase (30 seconds after infusion of contrast material), the venous phase (60–70 seconds after infusion), or both, no consensus exists about the optimal timing for small-bowel imaging (1–3,5,7). To the best of our knowledge, in no study have the small-bowel mural enhancement patterns been evaluated with contrast-enhanced multi–detector row CT.
Thus, the purpose of our study was to prospectively determine quantitatively and qualitatively the timing for maximal enhancement of the normal small-bowel wall by using contrast-enhanced multi–detector row CT.
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MATERIALS AND METHODS
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This Health Insurance Portability and Accountability Act–compliant prospective study was approved by the institutional review board, and written informed consent was obtained from each enrolled participant after information on radiation risk was given. E-Z-Em (Westbury, NY) provided financial support for a research technologist. However, only the authors of this manuscript had access to the study data and the information submitted for publication. One of the authors (R.C.N.) is a consultant for GE Healthcare (Milwaukee, Wis), the manufacturer of the scanner used to perform CT in this study.
Study Participants
Between September 1, 2005, and January 15, 2006, 25 subjects (19 men, six women; age range, 23–82 years; median age, 62 years; mean age, 58 years) were enrolled. The inclusion criteria were a minimum age of 18 years, ability to receive intravenous contrast medium, good intravenous access, and good physical health status (ie, such that the subject could hold his or her breath for at least 45 seconds). Before CT, a dedicated research nurse tested and trained each subject on holding his or her breath for 45 seconds. Study exclusion criteria were a history of inflammatory bowel diseases (eg, Crohn disease, ulcerative colitis) and abdominal trauma or acute abdominal symptoms (eg, appendicitis, small-bowel obstruction) within the past 48 hours. Potential subjects were identified by means of review of the daily institutional CT schedule for outpatients referred for clinically indicated CT of the abdomen and pelvis. Indications for abdominopelvic CT among the 25 enrolled subjects were prostate cancer (n = 5), testicular cancer (n = 4), bladder cancer (n = 3), pancreatic cancer (n = 2), lymphoma (n = 2), chondrosarcoma (n = 2), endometrial carcinoma (n = 2), evaluation for abdominal neoplasm (n = 2), uterine sarcoma (n = 1), follow-up after pancreatitis (n = 1), and hematuria (n = 1). According to medical chart review performed by a third-year radiology resident (S.T.S.), one subject had cardiac dysfunction and a reduced ejection fraction of 35%. All other subjects had normal cardiac function.
CT Scanning
All images were obtained with a 16–detector row CT scanner (LightSpeed 16; GE Healthcare) and a 0.5-second gantry rotation time. For bowel preparation, each subject ingested 900–1350 mL of 0.1% barium sulfate suspension (VoLumen; E-Z-Em), which was equally distributed over a 45-minute period. All subjects received 1 mg of intravenous glucagon (GlucaGen; Bedford Laboratories, Bedford, Ohio) 2 minutes before intravenous administration of 150 mL of iopamidol (Isovue 370; Bracco Diagnostics, Princeton, NJ), which was delivered at a rate of 5 mL/sec via a catheter (Angiocath; Infusion Therapy Systems, Sandy, Utah) inserted into an upper-arm vein.
The scanning protocol consisted of three parts: First, a single precontrast transverse image (10 mm thick) of the midabdomen was acquired. The unenhanced image, chosen from a CT scout, was deemed adequate if it depicted at least three distended small-bowel loops. Second, 30 seconds after the initiation of infusion of intravenous contrast material, ten 10-mm-thick dynamic transverse images were acquired without table movement at the location of the unenhanced image. Since these 10 single-level images were separated by 5-second intervals, the subject's single breath hold lasted 45 seconds. To reduce any additional radiation dose, the CT imaging protocol of the first and second parts was reduced from that used for standard abdominopelvic CT at our institution (from 140 kVp, 340–380 mAs to 140 kVp, 300 mAs). Third, subjects underwent clinically indicated abdominopelvic CT (detector configuration, 16 x 0.625 mm; pitch, 1.75; table speed, 17.5 mm per rotation; reconstruction, 5 x 5 mm). For the third acquisition, images were obtained during the venous phase (22 subjects), the nephrographic phase (three subjects), and the excretory phase (three subjects).
Quantitative Image Assessment and Statistical Analysis
After reconstruction of the subject's 10-mm-thick unenhanced and enhanced data sets to four 2.5-mm-thick images, quantitative analysis was performed on a separate workstation (Advantage Windows 4.2; GE Healthcare) by the radiology resident (S.T.S.). Quantitative analysis included attenuation measurements (in Hounsfield units) of the small-bowel wall and the aorta. Measurements were obtained on the unenhanced and the 10 enhanced dynamic images at 11 different time points (0 seconds, and every 5 seconds from 30 to 75 seconds). The region of interest was traced manually as a line along the course of the small bowel over a length of at least 5 cm (Profile, Advantage Windows 4.2; GE Healthcare) (Fig 1a). The mean mural attenuation values, with standard deviations (SDs), along the small-bowel wall were graphed (Fig 1b). Special care was taken to avoid inclusion of the small-bowel lumen (< +30 HU) and the perienteric fat (< –70 HU). At each of the 11 time points, three small-bowel mural measurements were obtained at three different locations. These three locations were identical for the 11 time points.
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Figure 1a: (a) Transverse contrast-enhanced CT image with small-bowel wall (arrows) manually traced to obtain mural enhancement values. (b) Graph corresponding to the manually traced line along the course of the small-bowel wall in a. The curve plots the mural attenuation values of the small bowel, in Hounsfield units (vertical axis), versus the length of the traced line, in millimeters (horizontal axis). The values on the bottom of the graph are the mean and SD (Std) of the mural enhancement, in Hounsfield units, along the trace. pos. = Position.
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Figure 1b: (a) Transverse contrast-enhanced CT image with small-bowel wall (arrows) manually traced to obtain mural enhancement values. (b) Graph corresponding to the manually traced line along the course of the small-bowel wall in a. The curve plots the mural attenuation values of the small bowel, in Hounsfield units (vertical axis), versus the length of the traced line, in millimeters (horizontal axis). The values on the bottom of the graph are the mean and SD (Std) of the mural enhancement, in Hounsfield units, along the trace. pos. = Position.
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Aortic attenuation measurements were obtained by manually placing a circular region of interest (150–350 mm2) in the center of the abdominal aorta. Three aortic attenuation measurements at three different locations were acquired for each time point. These three aortic locations were identical for the 11 time points.
Contrast enhancement of the small-bowel wall and the abdominal aorta was defined as the absolute difference between the average precontrast attenuation values and postcontrast attenuation values. Time-enhancement curves (expressed as attenuation vs time) were generated.
To measure intraobserver variation in the three small-bowel mural and the three aortic attenuation measurements for the 11 time points, we calculated the overall mean SD and the overall mean SD as a percentage of the mean level. For the small-bowel wall and the aorta, spline-smoothed curves were calculated to estimate the time points (seconds) of the peak and the intervals achieved within 95% of peak enhancement. To summarize the time points, descriptive statistics were obtained. Descriptive data were also calculated for the small-bowel mural enhancement values (in Hounsfield units) during three different phases: (a) the arterial phase, representing actual aortic peak enhancement; (b) the enteric phase, representing peak small-bowel mural enhancement; and (c) the venous phase after a fixed delay of 70 seconds. The time points of phases 1 and 2 differed for each subject. Paired Student t tests for differences in contrast enhancement of the small-bowel wall were computed as measured during these three phases. A Bonferroni adjusted P value less than .05 was considered to indicate a significant difference. All statistical analyses were performed with SAS, version 9.1.3 (SAS, Cary, NC), software.
Qualitative Image Assessment and Statistical Analysis
Three board-certified abdominal radiologists (E.M.M., T.A.J., J.T.) with 7, 6, and 5 years of experience, respectively, independently evaluated the CT images for small-bowel wall conspicuity. The radiology resident (S.T.S.) selected three 10-mm-thick images for each subject to represent the three different (arterial, enteric, and venous) enhancement phases. The level of the three images for each subject was the same. Because the time point of peak aortic and small-bowel mural enhancement differed for each subject, the time points of the selected images for the arterial and enteric phases were different for each subject. The abdominal aorta and mesenteric arteries were removed manually on the workstation by the resident (S.T.S.) to minimize the reader's ability to identify the enhancement phase according to opacification of the abdominal vessels (Fig 2). Before the start of qualitative image assessment, each reader was instructed in the criteria for image grading. The three images for each subject were presented in random order in a blinded fashion. Images were printed on film hard copies by using a soft-tissue window (width, 400 HU; level, +40 HU).
For the assessment of small-bowel wall conspicuity, readers were asked to subjectively rate the images on a continuous five-point scale (1 = none, 2 = poor, 3 = moderate, 4 = good, 5 = excellent). For the grading of small-bowel conspicuity, the reader selected the two most adequately distended bowel loops.
Statistical analysis for small-bowel conspicuity was performed with the Wilcoxon signed rank test by averaging the readers' numeric scores between the three enhancement phases. A Bonferroni adjusted P value less than .05 was considered to indicate a significant difference. Agreement between the readers for rating the small-bowel conspicuity during the three enhancement phases was determined with weighted 
statistics.
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RESULTS
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Quantitative Assessment
The overall mean SD and the overall mean SD as a percentage for the three small-bowel wall attenuation measurements for the 11 time points were 7.8 HU and 12.0%, respectively; for the aorta, these values were 4.5 HU and 2.7%, respectively. Peak enhancement of the small-bowel wall occurred a mean of 49.3 seconds ± 7.7 (SD) after the initiation of infusion of the intravenous contrast material, whereas aortic peak enhancement occurred after a mean of 35.8 seconds ± 6.4 (Table 1). The time of peak aortic enhancement ranged from 30.0 to 61.7 seconds after the initiation of infusion of the intravenous contrast material, and the peak small-bowel enhancement occurred between 36.6 and 70.0 seconds. The peak contrast enhancement of the small-bowel wall occurred a mean of 13.5 seconds ± 7.6 after the peak contrast enhancement of the abdominal aorta (Fig 3). The 95% interval for peak enhancement of the small-bowel wall started at 45.1 seconds after the infusion initiation and lasted until 54.6 seconds after the infusion initiation.
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Figure 3: Time-enhancement curve for the small-bowel (SB) and the aorta. At the mean time of peak aortic enhancement (approximately 35 seconds), the enhancement of the small bowel is still increasing. At approximately 45 seconds, a 10-second plateau of small-bowel wall enhancement begins. At approximately 70 seconds (venous phase), small-bowel wall enhancement decreases steadily.
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Mean enhancement of the small bowel (Table 2) was significantly higher during the enteric phase (47.5 HU) than during the arterial phase (33.6 HU) (mean delay, 35.8 seconds) or venous phase (38.3 HU) (P < .001). The difference in enhancement, although higher during the venous phase than during the arterial phase, was not significant (P = .15).
Qualitative Assessment
With respect to conspicuity of the small-bowel wall, all three readers scored the enteric-phase images highest and the arterial-phase images lowest (Table 3). Images obtained during the venous phase and the enteric phase were rated significantly higher than those obtained during the arterial phase (P < .001). Although the difference in mean rated conspicuity between the enteric phase and the venous phase protocols was not significant (P = .18), the sample size was small and an interesting difference cannot be ruled out. For the three enhancement phases, there was modest agreement (mean range, 0.15–0.31) among all three readers for rating small-bowel wall conspicuity (Table 4).
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DISCUSSION
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While broad knowledge exists on the individual enhancement patterns of the liver and the pancreas, to the best of our knowledge, similar data are not yet available for the small bowel (8–10). This knowledge gap led us to evaluate quantitatively and qualitatively the mural enhancement characteristics of the normal small bowel to determine the temporal window of peak enhancement at CT.
Our quantitative data indicate peak mural enhancement of the small bowel at an average of about 50 seconds after the initiation of contrast material infusion. As proposed recently by Bodily et al (7), we termed the temporal window covering the peak mural enhancement of the small bowel the enteric phase. The duration of the 95% interval was nearly 10 seconds (starting at 45.1 seconds and ending at 54.6 seconds after initiation of the contrast material infusion) and represented a plateau. This plateau provided a wide imaging window for CT of the small bowel during maximal enhancement. Toward the end of the 10-second plateau, the mural enhancement of the small bowel decreased steadily over time, indicating a gradual washout of contrast material. At 70 seconds (venous phase), the enhancement values of the small-bowel wall were significantly lower than they were during the enteric phase. Additionally, the enteric phase also offered significantly superior mural enhancement compared with the arterial phase. Hence, our quantitative assessment revealed the enteric phase to be the temporal window for peak enhancement during CT of the small bowel.
In a previous study, Horton et al (11) obtained contrast enhancement measurements of the normal small bowel on abdominal CT scans. Instead of a 45-second dynamic single-level CT examination, as used by our group, these investigators limited their evaluation to the arterial phase (30-second scanning delay) and the venous phase (60-second scanning delay). The arterial phase revealed slightly higher mural enhancement compared with the venous phase (11). The higher enhancement values during the arterial phase differed from our findings, and we were unable to determine the actual cause of the discrepancy. Furthermore, Horton et al (11) proposed that the mural enhancement differences between the arterial and the venous phases, which were small (eg, 8 HU in the jejunum), might not have been clinically important. Regarding small-bowel conspicuity, however, our qualitative results demonstrated a preference for the images obtained during the enteric phase. The modest agreement among the three readers for small-bowel conspicuity might be explained by the purely subjective assessment used, with no prior calibration on a continuous five-point scale. Although it is unclear whether the use of enteric-phase images translates into improved detection and characterization of small-bowel disorders, we recommend, on the basis of our findings, that CT be performed during maximum mural enhancement.
As recently reported by Bodily et al (7), quantitative measurements of small-bowel wall hyperenhancement on CT images have correlated closely with endoscopic and histologic findings of inflammatory Crohn disease. In the future, quantitative measurement of small-bowel perfusion with CT may become an accurate and useful method for determining objectively the presence and the severity of small-bowel disorders, such as Crohn disease and intestinal ischemia (7,12). Functional data could thereby be added to the morphologic information provided by CT scanning (11). In the case of inflammatory bowel disease, two measurement techniques for objective prediction of the disease activity with regard to mural enhancement have been described (7): (a) A standardized enhancement value for the small bowel is used as a threshold for delineating active Crohn disease, or (b) an interindividual comparison of mural enhancement between inflamed and normal-appearing segments is performed (7). The fixed threshold method has one major drawback: the wide variation in enhancement values of the small-bowel wall, which was confirmed by our quantitative data (7). The variance in mural enhancement may be caused by the subject's cardiac output and weight and by the protocol for injection of contrast agent (eg, injection rate, scanning delay, total amount of iodine, or concentration) (7). The range of the cardiac output in our study was reflected by the range of peak aortic enhancement times (30.0–61.7 seconds). In contrast, the described method of interindividual comparison of mural enhancement with CT imaging seems to be more precise for predicting the activity of small-bowel diseases, since both the proximal small bowel and the distal small bowel seem to enhance in a uniform fashion (11).
For the attenuation measurement of the small bowel, a line region of interest was applied. In our opinion, this technique is quite reliable and robust, as indicated by the mean SD as a percentage for the three small-bowel wall attenuation measurements for the 11 time points. A mean variation of 12.0% is acceptable, given the fact that the small-bowel wall is a thin anatomic structure with a variation of enhancement among the different layers of the wall (13).
Different practical approaches to coordinating the timing of the CT acquisition during the enteric phase exist. Given the 10-second plateau during the intervals achieved within 95% of peak enhancement, a fixed scanning delay of about 50 seconds would achieve peak mural enhancement of the small bowel in most patients at an injection rate of 5 mL/sec. An additional time delay of up to 5 seconds for peak enhancement of the small-bowel wall has to be considered when injection rates lower than 5 mL/sec are used. In patients with extremely low or high cardiac outputs, we also suggest tailored scanning delays (up to ±20 seconds). For instance, in one of our subjects with mild heart failure and a reduced ejection fraction of 35%, peak mural enhancement of the small bowel was substantially delayed to around 70 seconds. Besides the fixed time delay, a more precise timing of the enteric phase can be achieved with bolus triggering from peak aortic enhancement. Since, in our study, peak mural enhancement of the small bowel occurred an average of 14 seconds after peak aortic enhancement, we recommend a 14-second delay after peak aortic enhancement.
There were limitations to our study. First, the sample size of 25 subjects was small. Since the small cohort included subjects with a wide age range (23–82 years), we were able to obtain images in subjects with different cardiac outputs. Cardiac output substantially influences the time to peak mural enhancement. Another potential limitation was that our study did not include patients with small-bowel disease. However, the objective of our investigation was to evaluate the enhancement pattern of the normal small bowel. To date, we are uncertain whether the described enteric phase improves the sensitivity and specificity of detection of small-bowel lesions. Additional studies will be needed to address this issue. A minor limitation was that film hard-copy images instead of digital images (on a workstation) were used for qualitative image assessment. Another potential minor limitation was that it was not practicable to remove all mesentery vessels with a diameter smaller than 3 mm. However, there is only a small possibility that vessels this thin will influence a reader's ability to identify precisely the enhancement phase.
In summary, we have demonstrated the enhancement pattern and the peak enhancement temporal window for the normal small bowel with contrast-enhanced multi–detector row CT. As a result of these findings, we have modified the small-bowel protocol in our practice to imaging during the enteric phase with automated triggering and a 14-second scanning delay after peak aortic enhancement.
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ADVANCES IN KNOWLEDGE
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- Peak mural enhancement of the small bowel occurs on average 50 seconds after initiation of intravenous administration of contrast material.
- Peak mural enhancement of the small bowel occurs an average of 14 seconds after the peak aortic enhancement.
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FOOTNOTES
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Abbreviations: SD = standard deviation
See Materials and Methods for pertinent disclosures.
Author contributions: Guarantors of integrity of entire study, S.T.S., R.C.N.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, S.T.S.; clinical studies, S.T.S., R.C.N.; statistical analysis, D.M.D.; and manuscript editing, all authors
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ABSTRACT
INTRODUCTION
