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1 Department of Radiology, Children's Hospital of British Columbia, 4480 Oak
St., Vancouver, B. C. V6H 3V4, Canada.
2 Department of Pediatrics, Division of Gastroenterology, Children's Hospital of
British Columbia, Vancouver, B. C. V6H 3V4, Canada.
Received July 5, 2002;
accepted after revision October 14, 2002.
Address correspondence to D. H. Jamieson.
Abstract
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SUBJECTS AND METHODS. This was a prospective study. Eighteen children undergoing workup for inflammatory bowel disease underwent MDCT, colonoscopy, and barium studies of the small bowel before commencement of therapy. Examinations were independently reviewed. The patients and their guardians completed a questionnaire assessing the acceptability of each study.
RESULTS. In 13 of 18 children, the findings of MDCT and barium studies of the small bowel concurred in the evaluation of terminal ileum disease. In three of these children, MDCT detected skip segments of small-bowel disease not detected on barium studies of the small bowel. In two of 18 children, the terminal ileum was not visualized on barium studies of the small bowel, whereas MDCT showed substantial terminal ileum disease in both children. In three of 18 children, there was discordance between the two tests regarding terminal ileum disease. However, these discordant imaging findings were all subtle. In addition, MDCT revealed extraenteric abnormalities, clinically relevant in two children (ureteric obstruction and perirectal abscess), and showed the colon in all children, seven of whom had incomplete colonoscopy. The questionnaire revealed that 16 of 18 patients preferred MDCT to small-bowel barium studies. The reasons given were poor tolerance of oral barium and the long duration of barium studies of the small bowel.
CONCLUSION. MDCT can be an alternative to barium studies of the small bowel for evaluation of the small bowel in patients with inflammatory bowel disease. MDCT also offers additional, clinically relevant information not obtained by small-bowel barium studies.
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In our pediatric gastroenterology service, this disease map is currently achieved by a combination of upper gastrointestinal endoscopy, upper gastrointestinal and small-bowel barium studies, and colonoscopy. It is our experience that the barium studies of the small bowel can be poorly tolerated, particularly by ill children. In addition, the current standard protocol may fail to image the entire bowel because of inadequate small-bowel barium studies or incomplete colonoscopy.
CT has an accepted role in imaging the complications of inflammatory bowel disease [1, 2, 3, 4]. In this setting, we noted that using a multidetector CT (MDCT) scanner with the capability of multiplanar reconstruction, we could delineate the extent of bowel disease in addition to the specific complication. In our experience, MDCT is well tolerated. Hence we believe that MDCT has the potential to replace small-bowel barium studies for evaluation of the small bowel and to provide additional clinically relevant information about colonic disease and extraenteric complications. The CT findings of inflammatory bowel disease in adults have been well described in the medical literature [1, 2, 5, 6].
Studies of adults comparing single-detector helical CT with enteroclysis have shown that CT can be more sensitive and can show additional disease segments [7, 8]. Studies using single-detector helical CT also showed that multiplanar reconstructions increase the confidence of diagnosis without necessarily affecting the frequency or sensitivity of abnormalities detected [9].
We established a prospective study with the aim of comparing MDCT with barium studies of the small bowel in the evaluation of small-bowel involvement in pediatric patients who were evaluated by our gastroenterology service at their initial presentation for inflammatory bowel disease.
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Children eligible for inclusion in the study were those with clinically suspected but untreated inflammatory bowel disease at the initial presentation. Those who had commenced medical therapy were excluded because it was believed that medication, particularly steroids, might alter the radiographic findings.
Institutional ethics board approval was obtained for the study. Guardians of the children signed an informed consent that detailed the study protocol, potential risks of the added radiation, and the IV administration of iodinated contrast material.
Within 1 week of clinical diagnosis and before commencement of medical therapy, patients underwent abdominal and pelvic MDCT, upper gastrointestinal and small-bowel barium studies, and endoscopy. Tests were undertaken on three consecutive days. MDCT was performed before the other examinations to avoid artifacts from barium or gas introduced at endoscopy.
CT was performed with a four-channel multidetector scanner (MX 8000; Phillips Medical Systems, Best, The Netherlands). The protocol used was as follows: slice thickness, 2.5 mm; pitch, 1.25; 120 kVp; 80–150 mAs; and rotation time, 0.5–0.75 sec. IV iohexol 65% (Omnipaque 300 mg I/mL; Nycomed, Brampton, Canada) at a dose of 2 mL/kg was administered over 50 sec, with scanning commencing in the portal venous phase of enhancement (55 sec). Topical tetracaine 4% weight-for-weight (Ametop gel; Smith and Nephew, Lachine, Canada) was applied before insertion of the peripheral IV cannula. Positive oral contrast medium was not used. We do not believe that bowel luminal opacity is required to delineate the bowel, and we think that positive bowel contrast medium may obscure mucosal enhancement [10]. Instead, bowel distention was achieved by giving 200–500 mL of water or clear juice over the 30 min before scanning. The scan data were reviewed at a workstation (Magicview 1000; Siemens, Erlangan, Germany) using multiplanar reconstructions.
The signs considered suggestive of inflammatory bowel disease were bowel wall thickening (>2.5 mm), mucosal or transmural enhancement, fibrofatty proliferation, mesenteric hyperemia, and lymphadenopathy (Figs. 1, 2, 3, 4 and 5). These signs were taken from studies of adults published in the medical literature [1, 2, 5, 6], and the presence of at least two signs was considered necessary to diagnose a segment of bowel as abnormal.
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Endoscopy was performed in the gastroenterology suite in patients who were under conscious sedation with upper gastrointestinal endoscopy preceding colonoscopy. Biopsies were routinely performed for histologic examination.
Barium studies of the small bowel were performed after a single-contrast upper gastrointestinal study using 30% weight-for-volume barium (Polibar Plus; Therapex Division of E-Z-EM Canada, Montreal, Canada). The patient was offered an additional 2–3 cups (0.4–0.6 L) of barium, and overhead radiographs were obtained at 30 min 1 hr and as necessary thereafter. Spot fluoroscopy or compression was intermittently performed as necessary, and specific images of the terminal ileum were always obtained.
All investigations were independently reported without knowledge of the results of the other tests. MDCT examinations were reported by one of two pediatric radiologists. Barium studies of the small bowel were performed and reported by one of five additional pediatric radiologists. The endoscopy report was submitted by one of three staff pediatric gastroenterologists and included the results of histology on the biopsy specimens.
The reports issued by the attending radiologist or gastroenterologist were then evaluated and compared. We conducted a second, retrospective review of all MDCT and small-bowel barium examinations and found no significant disagreement with the issued reports. In the instances of minor disagreement, the initially reported findings were used to preserve the prospective methodology of the study.
On completion of the examinations, the children and their guardians were interviewed, and a questionnaire assessing their acceptance of the two imaging studies was completed. The perceived duration of each of the two examinations was recorded. A rating scale assessing the amount of discomfort caused by each examination was also recorded (0–10, with 0 being no discomfort and 10, maximal discomfort). Finally, the children and their guardians were asked for an overall assessment of which imaging study they would prefer if given a choice to undergo only one.
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The terminal ileum was visualized on all 18 MDCT studies and on 16 of 18 small-bowel barium studies. The two children in whom the small-bowel barium studies failed to reveal the terminal ileum were shown to have marked terminal ileum disease on MDCT. Of the 16 children in whom the terminal ileum was visualized on both tests, 13 showed concordance as to the presence or absence of terminal ileum disease (11 had the disease, and two had normal findings). The remaining three children had discordant findings. Two patients underwent barium studies of the small bowel that revealed subtle terminal ileum disease not revealed on MDCT (Figs. 6A, 6B), and one patient underwent MDCT that showed subtle terminal ileum disease not seen on small-bowel barium studies. In no child was marked disease of the terminal ileum observed in one test and not also recorded in the other.
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Correlation of the imaging studies with colonoscopy and histology reports pertaining to the terminal ileum revealed that the terminal ileum was accessed in 11 of 18 colonoscopy examinations. Of the 11 children with concordant terminal ileum disease (reported on barium studies of the small bowel and MDCT), colonoscopic findings confirmed the presence of disease in five, failed to access the terminal ileum in four, and reported the terminal ileum as normal in two. In the two children with concordant findings of a normal terminal ileum on MDCT and small-bowel barium studies, both had normal colonoscopy correlation. Of the three children with discordant terminal ileum imaging findings, in only one was the terminal ileum accessed on colonoscopy. This was the child in whom MDCT showed subtle disease not reported on barium studies of the small bowel and in whom the colonoscopy reported a normal terminal ileum.
Small-bowel disease proximal to the terminal ileum was assessed separately. MDCT showed skip segments of small-bowel disease outside the terminal ileum in three of 18 children. In all three of these children, terminal ileum disease was also present. Barium studies of the small bowel did not identify skip segments of small-bowel disease in any of the studies.
In addition, we noted that MDCT revealed the entire small and large bowel in all 18 examinations, whereas the current standard of combined small-bowel barium studies and endoscopy failed to reveal the entire small and large bowel in eight of the 18 children. This was as a result of inadequate barium studies of the small bowel in two children and incomplete colonoscopy in seven (one case overlapped with both inadequate small-bowel barium studies and incomplete colonoscopy).
Clinically significant extraenteric abnormalities, not visible on small-bowel barium studies, were recorded on two MDCT examinations. These abnormalities comprised an obstructed right ureter due to an inflammatory mass in the right iliac fossa (Fig. 7) and a perirectal abscess. Renal cysts were noted on two other examinations but recorded as incidental observations.
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The patient questionnaire revealed that 16 of 18 children preferred MDCT to barium studies of the small bowel. The median score on the 1–10 rating scale for discomfort was 3 for MDCT and 7 for small-bowel barium studies. The main reasons given for dissatisfaction with barium studies of the small bowel were intolerance of oral barium and the long duration of the follow-through examination. The two children who preferred the small-bowel barium examination to MDCT each expressed discomfort related to the IV insertion line. In one of these children, topical anesthetic was not used, and in the other child, difficulty was encountered inserting the IV line, requiring two attempts.
The average perceived duration of each examination, from the time the child entered the department to undergo preparation for the study to the time he or she left the department, was 50 min (range, 10–90 min) for MDCT and 235 min (range, 180–480 min) for small-bowel barium studies.
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Our study involved a small number of patients. The strengths of the study were that it was prospective, and MDCT, endoscopy, and small-bowel barium studies were all completed within a week and before commencement of therapy, allowing valid comparison of disease status.
Barium studies of the small bowel and MDCT performed equally in the evaluation of the terminal ileum in 13 of 18 children. These 13 children included three in whom MDCT showed additional proximal small-bowel skip lesions not seen on barium studies of the small bowel. This finding suggests increased sensitivity for disease detection on MDCT. In two of 18 children, barium studies of the small bowel failed to show the terminal ileum, whereas MDCT showed marked terminal ileum disease; hence, MDCT was considered the better test. In three of 18 patients, there was discordance between MDCT and small-bowel barium studies regarding terminal ileum disease. In all three, subtle or equivocal findings on either test led to discordance, and neither study was clearly superior.
An additional advantage of MDCT over barium studies of the small bowel is that MDCT can show extraenteric abnormalities. In two of our patients, extraenteric abnormalities were unsuspected and influenced clinical treatment of the patient.
Perhaps most significantly, we found that MDCT consistently imaged the entire small and large bowel, which was not achieved by the current investigational protocol in eight of 18 children. Often, it is the most ill children or children with severe diseases who have incomplete studies because of their poor tolerance for oral barium and the greater challenge in performing complete colonoscopy.
The radiology to colonoscopy correlation, as it pertains to the terminal ileum, did raise some interesting issues. The terminal ileum was accessed in only 11 of 18 colonoscopies. Although many reasons may be postulated to explain this low rate of complete colonoscopy, it does correlate with our observation that children at initial presentation with inflammatory bowel disease often had severe and extensive disease (Figs. 7 and 8). In the two children in whom MDCT and barium studies of the small bowel concurred that terminal ileum disease was absent, this finding was confirmed on colonoscopy. In the 11 children in whom MDCT and barium studies of the small bowel concurred that terminal ileum disease was present, the terminal ileum was accessed only in seven. In five of these children, colonoscopy and histology confirmed the presence of terminal ileum disease. In two, colonoscopy showed a normal terminal ileum, which could be interpreted as indicating that both MDCT and barium studies of the small bowel have a high false-positive rate when assessing terminal ileum disease. In each of these children, however, clear radiologic disease was revealed on both imaging studies (Figs. 9A, 9B). Another possible explanation is that endoscopy results in the underdiagnosis of terminal ileum disease. Endoscopic evaluation may have been limited to the most distal portion of the terminal ileum, hence missing more proximal disease. Alternatively endoscopy may detect mucosal disease but fail to depict transmural changes.
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Our patient preference questionnaire revealed that most children prefer MDCT to barium studies of the small bowel because of intolerance to oral barium and the longer duration of the follow-through examination. The questionnaire also confirmed that MDCT is a much quicker examination, requiring the patient and parents or guardians to spend less time in the hospital and reducing the use of radiology staff resources.
Previous studies have shown a cost savings by using CT rather than combined barium studies of the small bowel and barium enema to evaluate inflammatory bowel disease in adults [3]. In our institution, the cost of the MDCT examination is CAD$230, whereas the cost of small-bowel barium studies is CAD$150, representing a CAD$80 cost differential. Given the potential advantages of MDCT, both diagnostically and from a patient viewpoint, we believe this added cost is justified. Potential cost-savings because of less prolonged use of radiology staff resources and the possibility of more limited colonoscopic studies if MDCT is proven useful in evaluating the colon also need to be considered.
Further work remains to be done comparing MDCT with colonoscopy in the evaluation of large-bowel involvement in children with inflammatory bowel disease. In the medical literature, CT has been shown to be accurate at assessing large-and small-bowel disease in adults [8, 9]. If this is also found to be true in the pediatric population, then MDCT has the potential to become a single, well-tolerated test that could accurately and reliably map disease involvement throughout the entire large and small bowel. In this way, gastroenterologists could restrict colonoscopy to achieve the single aim of providing a colonoscopic and a histologic diagnosis. They could then pass an endoscope to the level of the first diseased segment of bowel and decrease the risk of complications that might ensue passing the scope through severely diseased bowel.
The disadvantages of MDCT over barium studies of the small bowel are the increased radiation exposure and the necessity for administration of IV contrast material. The estimated effective dose of an MDCT study of the abdomen and pelvis is 15 mSv [11]. An upper gastrointestinal study and small-bowel barium study have an estimated effective dose of 6–8 mSv [12]. The extra radiation burden imposed by performing MDCT instead of barium studies of the small bowel would be 7–9 mSv. The average annual background radiation exposure in Canada is 2 mSv [13]. Denver, however, has 12.4 mSv annual background radiation [14]. The risk of radiation in CT is the induction of leukemia and solid tumors. Mature data from Japanese populations exposed to less than 20 mSv in the 1945 atomic bomb explosions have indicated a small but statistically significant increase in cancers [15]. Nevertheless, we believe that the information gained from MDCT justifies the increased radiation burden compared with barium studies of the small bowel in appropriately selected patients.
In conclusion, in a pediatric population, MDCT can be a rapid, reliable, well-tolerated, and accurate alternative to barium studies for the initial evaluation of the small bowel in inflammatory bowel disease. MDCT has the ability to reveal extraenteric abnormalities and colonic disease, which are potential advantages requiring further evaluation.
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