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Technical Developments |
1 From the Department of Diagnostic Radiology (P.B.W., J.G.F., C.D.J.) and Division of Gastroenterology, Department of Internal Medicine (W.J.S.), Mayo Clinic, 200 First St SW, Rochester, MN 55905. From the 2001 RSNA scientific assembly. Received July 19, 2002; revision requested August 29; revision received December 24; accepted January 15, 2003. Address correspondence to J.G.F. (e-mail: fletcher.joel@mayo.edu).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDiscussionREFERENCES |
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© RSNA, 2003
Index terms: Contrast media, comparative studies • Crohn disease, 74.262 • Enteritis, 742.26 • Ileum, 742.262 • Intestines, CT, 742.1211
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDiscussionREFERENCES |
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Numerous CT enterography techniques have been designed to optimize visualization of the small bowel (9,13–21). The majority of these studies have employed fluoroscopic placement of a nasojejunal tube to infuse oral contrast material; this is also referred to as CT enteroclysis. Most patients find placement of this nasojejunal tube onerous. Our goal was to (a) examine the feasibility of predicting active small bowel Crohn disease with use of a noninvasive peroral CT enterography protocol versus a conventional CT enterography protocol with a nasojejunal tube and then (b) compare each with fluoroscopic small bowel examination and endoscopy with biopsy.
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MATERIALS AND METHODS |
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Patients were alternately assigned by our study coordinator to undergo either a noninvasive peroral CT enterography protocol or CT enterography with a nasojejunal tube. Twelve patients were originally assigned to undergo noninvasive peroral CT enterography, and 11 patients were assigned to undergo CT enterography with a nasojejunal tube. If a patient refused the assigned CT enterography protocol, the patient was given the option of choosing the alternate CT enterography protocol. Three patients refused the CT enterography with nasojejunal tube placement; as a result, 15 patients underwent noninvasive peroral contrast material–enhanced CT enterography, whereas only eight patients underwent the conventional CT enterography protocol with a nasojejunal tube.
Each patient also underwent traditional fluoroscopic small bowel examination with use of thin barium (Barosperse, 50% wt/vol suspension; Lafayette Pharmaceutical, Lafayette, Ind). Patients drank 225-mL aliquots at intervals and volumes chosen at the discretion of the attending radiologist. An experienced gastrointestinal radiologist in our department performed frequent, intermittent palpation and fluoroscopic observation (approximately every 15–20 minutes) until the terminal ileum was adequately assessed. A routine overhead radiograph was obtained after each intermittent fluoroscopic assessment. At the conclusion of the examination, three overhead radiographs (one posteroanterior and two oblique images) were obtained. The mean time between CT and fluoroscopic small bowel examination was 0.8 day with a median and mode of 1 day (range, 0–5 days). Based on an assumption of 5 minutes of fluoroscopy time, six overhead posteroanterior radiographs, and two overhead oblique radiographs, an estimated average effective dose equivalent (for men and women) is 1.21 mSv.
All 23 patients underwent endoscopy with intubation of the terminal ileum or neoterminal ileum (ie, the most distal portion of a surgically altered ileum). The mean time between CT and ileoscopy was 5.3 days with a median and mode of 1 day (range, 0–34 days). Twenty patients underwent biopsy of the terminal ileum or neoterminal ileum. In patients undergoing ileal biopsy, the standard of reference for active small bowel inflammation compatible with Crohn disease was pathologic confirmation. Three patients had negative endoscopic examination results and subsequently did not undergo biopsy. In these three patients, endoscopic assessment of the terminal ileum was used as the reference standard for the presence of active small bowel inflammation. Seven patients subsequently underwent surgery with a mean time between CT and surgery of 21.3 days and a median of 27 days.
CT Enterography
Both groups were administered one 10-mg dose of oral metoclopramide (Pharmaceutical Associates, Greenville, SC) 75 minutes prior to CT enterography in order to increase gastric and small bowel peristalsis. Patients enrolled in the noninvasive CT enterography protocol drank four 450-mL aliquots of water in 75 minutes, for a total of 1,800 mL. The first aliquot was given immediately after the metoclopramide, and subsequent aliquots were given at 25, 50, and 65 minutes after the ingestion of the peristaltic agent. CT scanning was performed at 75 minutes after metoclopramide ingestion. Patients enrolled in the conventional invasive CT enterography protocol underwent nasojejunal intubation with a 13-F 155-cm nasojejunal tube (Maglinte enteroclysis catheter; Lafayette Pharmaceutical), which was followed by hand injection of 1,800 mL of methylcellulose injected at approximately 60 mL/min prior to CT examination. For both CT enterography regimens, patients were intravenously administered 1 mg of glucagon prior to scanning. Contrast-enhanced biphasic CT images were acquired at 40 and 70 seconds (GE LightSpeed or LightSpeed Plus; GE Medical Systems, Milwaukee, Wis) by using 2.5-mm section thickness, 270 mA, 120 kVp, and 150 mL of contrast material (iopamidol [Isovue 300]; Bracco Diagnostics, Princeton, NJ) intravenously injected at a rate of 3 mL/sec. Images were reconstructed every 2.5 mm. The mean effective dose equivalent (for men and women) for each CT phase was 9.58 mSv, with an additional 1.13 mSv for the placement of the nasojejunal tube (when required).
Image Evaluation
Two gastrointestinal radiologists (J.G.F. and C.D.J.) reviewed all images in consensus and were blinded to endoscopic assessment and the results of all other imaging examinations. CT images were interpreted first, in random order; fluoroscopic images were interpreted next, also in random order. The interpretation of fluoroscopic small bowel examination images was augmented by unblinding of the examination report written by the gastrointestinal fluoroscopist at the time the examination was performed.
Each CT enterography examination image was assessed for adequacy of luminal distention. Adequate luminal distention was defined as separation of the lumen by enteric contrast material without collapse. Reviewers assigned a distention score based on an estimate of the percentage of small bowel with adequate distention. If greater than 90% of the small bowel was adequately distended, the CT enterography examination received a distention score of 4 (optimal); if 70%–90% of the small bowel was adequately distended, the examination received a distention score of 3 (good); if 40%–69% was adequately distended, the examination received a score of 2 (moderate); and if there was less than 40% adequate distention, the examination received a distention score of 1 (mild).
CT enterography criteria used to determine the presence of active Crohn disease included mucosal hyperenhancement, mural stratification, and mesenteric fat stranding. Mucosal hyperenhancement was defined as hyperattenuation of the bowel wall (when mural stratification was absent) or of the inner aspect of the bowel wall (when mural stratification was present), as compared with the mural attenuation of adjacent ileal loops. Fluoroscopic small bowel examination criteria used to determine the presence of active Crohn disease included aphthous ulcers, fold thickening or obliteration, linear ulcers and cobblestone pattern, and luminal stenosis with ulceration. For both types of examination, radiologists also noted the presence of fistulas, sinus tracts, abscesses, phlegmons, and extraenteric manifestations of Crohn disease (including cholelithiasis, nephrolithiasis, and sacroiliitis). Fistulas were defined as hyperenhancing (at CT) or barium-filled tracts (at fluoroscopic examination) extending from the bowel to other structures. Sinus tracts had a similar appearance but did not extend to other structures. Abscesses were defined as circumscribed extraluminal fluid collections (at both examinations) with enhancing, well-defined walls (at CT only). Phlegmons were defined as extraenteric masses of fluid and soft-tissue attenuation (at CT only). The presence of fistulas/sinus tracts and abscesses/phlegmons at fluoroscopic small bowel follow-through and CT enterography were compared with each other and with surgical findings (when available), or with sinograms and findings at clinical examinations in cases of enterocutaneous fistulas.
Radiologists also assessed the need for a biphasic examination by rating the contribution of the early (40-second) phase compared with that of the portal venous (70-second) phase. The contribution of the early phase was rated as "potential contribution" if CT findings were demonstrated on only the early phase images or if findings were more conspicuous on the early phase images. The early phase was rated to have "no contribution" if portal venous phase images demonstrated all findings at least as well as the early phase images.
Statistical Analysis
Adequacy of luminal distention was compared between the two CT enterography protocols by using the Wilcoxon rank sum test (P 
.05 considered to show significance). The sensitivity, specificity, positive predictive value, negative predictive value, and accuracy were determined for each type of CT enterography technique and fluoroscopic small bowel examination, and these were compared to our reference standard (histologic or endoscopic assessment).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDiscussionREFERENCES |
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There was no significant difference in the adequacy of luminal distention between the noninvasive, peroral water CT enterography technique and CT enteroclysis with use of the nasojejunal tube (P = .16, Fig 1). Both protocols had a median distention score of 2 (moderate). CT enterography performed with a nasojejunal tube had a mean distention score of 2.75, while peroral noninvasive CT enterography had a mean distention score of 2.10.
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The performance of CT enterography in depicting Crohn disease in patients with endoscopic and pathologic evidence of active terminal ileal disease is shown in Table 1. CT enterography (combined results of both techniques) correctly demonstrated active ileal Crohn disease in 10 of 13 patients. Active disease was demonstrated by mucosal hyperenhancement (n = 9), mural stratification (n = 5), or mesenteric fat stranding (n = 4). CT enterography enabled correct identification of normal terminal ileum in nine of 10 patients (Fig 2). Active terminal ileal Crohn disease was correctly detected in eight of 13 patients at fluoroscopic small bowel examination (Fig 3). The performance of fluoroscopic small bowel examination is also shown in Table 1.
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Discussion |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDiscussionREFERENCES |
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CT enterography outperformed the fluoroscopic small bowel examination in the detection of fistulas and sinus tracts, in addition to abscesses or phlegmons. Results of previous studies have found CT superior in the detection of enterocutaneous and enterovesical fistulas but barium examinations superior in the detection of enteroenteric and enterocolic fistulas and sinus tracts (6). CT also depicted other important extracolonic findings such as sacroiliitis, cholelithiasis, and nephrolithiasis. The detection of sacroiliitis is important, as it may support the diagnosis of Crohn disease or predate the development of small bowel disease (8).
There was no difference in luminal distention between the two tested CT enterography techniques (P = .16), and 80% of patients had moderate to optimal distention of small bowel loops at CT with the peroral technique. Given these findings, there appears to be no significant advantage to using the invasive CT enterography technique in place of the noninvasive peroral water CT enterography protocol. Similarly, Mazzeo et al (21) concluded that CT enterography performed using 2 L of iso-osmotic solution was an effective alternative to nasojejunal tube placement in patients suspected of having small bowel Crohn disease.
We had hypothesized that early, mucosal phase images might demonstrate subtle mucosal hyperenhancement not seen on portal venous phase imaging, as the bowel mucosa optimally enhances during this phase (22). We found, however, that the acquisition and review of early phase images provides no contribution to the assessment of Crohn disease activity. Eliminating the acquisition of these early phase images eliminates half the radiation dose of the CT examination. Mucosal hyperenhancement and mural stratification are depicted equally well during both vascular phases.
Direct comparison of our study to the work of others is difficult, as to our knowledge there are no other studies that specifically compare the use of CT enterography with negative oral contrast material with the use of fluoroscopic small bowel examination in the detection of endoscopically proved active small bowel Crohn disease. Several investigators (9,18,21) have demonstrated the utility of contrast-enhanced CT after placement of a nasojejunal tube and the infusion of methylcellulose in the detection of active Crohn disease and its complications. Our noninvasive peroral protocol eliminates use of the nasojejunal tube, the placement of which many patients find onerous (eg, three of 11 [27%] patients assigned to undergo CT enterography with nasojejunal tube refused tube placement and instead underwent the noninvasive examination). Both Raptopoulos et al (19) and Mazzeo et al (21) have previously described peroral, noninvasive CT enterography protocols with negative (polyethylene glycol) and positive oral contrast material (Readicat; E-Z-Em, Westbury, Conn), respectively. Their results were compared largely with the results of barium examinations, which can underrepresent small bowel inflammation and disease (23,24). In contrast, our study employed water as an oral contrast agent and used an endoscopic and histologic reference standard. Nevertheless, both studies demonstrated promising performance in detecting active disease and its complications. Our protocol used a volume of water (as oral contrast agent) that was similar to the volumes of contrast agent used in these other noninvasive protocols. By employing water as the contrast agent (as opposed to barium), we believe we can better see mucosal hyperenhancment and mural stratification because of differences in attenuation between enteric contents, mucosa, and submucosa.
Our choice to compare CT enterography with fluoroscopic small bowel examination rather than enteroclysis could be criticized. At our institution, fluoroscopic examination of the small bowel is used solely for the assessment of small bowel Crohn disease. Small bowel enteroclysis is highly sensitive and specific in the detection of small bowel Crohn disease (25) and is considered by many to be the barium examination of choice in the assessment of small bowel Crohn disease. However, a properly performed fluoroscopic examination of the small bowel with "repeated, frequent fluoroscopic evaluation with vigorous manual palpation and appropriate patient positioning" has been shown to equal the accuracy of enteroclysis (26,27). Additionally, widespread use, ease of performance, and greater patient acceptance are compelling reasons to compare the fluoroscopic small bowel examination with CT in the detection of active small bowel Crohn disease.
One limitation of the CT enterography technique is that it may fail to depict very mild inflammation. All three false-negative examinations in our study had only a few aphthous ulcers at ileoscopy, while all other positive CT examinations correlated to more severe disease at ileoscopy. Conversely, however, CT enterography and fluoroscopic small bowel follow-through display the entire small bowel, while ileoscopy evaluates only the most distal ileum. Our evaluation of CT enterography is limited in that we evaluated the performance of imaging examinations only in the terminal ileum, where endoscopic correlation was available. Our evaluation is also limited because of the high percentage of patients with Crohn disease: The underlying small bowel inflammation in our patients may have resulted in improved luminal distention, and these results may not translate to other patient populations (eg, patients without small bowel disease). We examined only patients known or suspected to have Crohn disease because we sought to examine the utility of this test in a particular patient population, and we used patients without active terminal ileal inflammation in our cohort as controls. We routinely administered oral metoclopramide as part of our CT enterography protocol; however, radiologists may prefer to not administer this drug in patients with obstructive symptoms because of the possibility of an exacerbation of symptoms. These patients can likely undergo successful noninvasive peroral CT enterography without degradation of luminal distention because their obstructive disease will improve luminal distention proximally. Finally, while both CT enterography protocols performed equally well, we note that the majority of patients had only "adequate" luminal distention. Other oral contrast agents or different regimens for administering oral contrast agents may improve the technique by further optimizing luminal distention.
In conclusion, in the assessment of patients known or suspected to have Crohn disease, both nasojejunal tube and peroral CT enterography techniques performed at least as well as fluoroscopic small bowel examination in the detection of active small bowel disease. The use of a conventional, invasive CT enterography protocol with a nasojejunal tube may not be justified when a noninvasive peroral water CT protocol appears to be equally effective. Additionally, the acquisition and review of early phase images appears to be unjustified when portal phase scanning is performed. The presence of the employed CT criteria for active disease (ie, mucosal hyperenhancement, mural stratification, or mesenteric fat stranding) were good predictors of active small bowel disease at ileoscopy. Additionally, CT enterography is more sensitive than fluoroscopic examination in the detection of extraenteric findings such as abscesses and fistulas. We conclude that noninvasive peroral CT enterography performed with water as oral contrast material is a promising method for evaluating patients with known Crohn disease, and the evaluation of this technique in a larger group of patients suspected of Crohn disease is warranted.
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FOOTNOTES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDiscussionREFERENCES |
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