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Original Research |
1 Department of Diagnostic Radiology, Mayo Clinic, 13400 E Shea Blvd.,
Scottsdale, AZ 85259.
2 Department of Internal Medicine, Mayo Clinic, Scottsdale, AZ.
3 Division of Gastroenterology and Hepatology, Mayo Clinic, Scottsdale,
AZ.
4 Division of Biostatistics, Mayo Clinic, Scottsdale, AZ.
Received July 16, 2007;
accepted after revision December 8, 2007.
Address correspondence to A. K. Hara
(hara.amy{at}mayo.edu).
Abstract
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MATERIALS AND METHODS. Forty CT enterography examinations in 20 patients (12 women, eight men; mean age, 55.5 years) with known Crohn's disease were retrospectively evaluated by a radiologist who was blinded to the clinical history. One radiologist determined whether imaging findings of Crohn's disease were present and, if so, whether the findings progressed, regressed, or remained stable between examinations. CT enterography findings were then compared with disease progression or regression based on symptoms and clinical follow-up. Direct comparison of CT enterography and endoscopy was also performed when available.
RESULTS. Disease progression or regression by CT enterography correlated with symptoms in 16 of 20 (80%) patients. Specifically, CT enterography and symptoms agreed in 12 patients with clinical disease progression, two patients with clinical regression, and two with clinically stable disease. In four of 20 (20%) patients, symptoms progressed although CT enterography findings were negative (n = 2) or improved (n = 2). No treatment change was initiated; and at follow-up, three of four patients were improved and the remaining patient was stable symptomatically. Sixteen ileoscopies were attempted in 12 patients; however, four examinations did not reach the ileum. In the remaining examinations, endoscopy correlated with CT enterography in all cases (12/12, 100%) and with symptoms in nine of 12 (75%) cases. The weighted kappa statistic, which measures the chance-adjusted agreement between CT enterography and symptoms, was 0.57 (95% CI, 0.20-0.94).
CONCLUSION. This preliminary study indicates that imaging changes between CT enterography examinations have excellent potential for reliably monitoring Crohn's disease progression or regression.
Keywords: Crohn's disease • CT enterography
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Most patients receive the initial diagnosis of Crohn's disease based on a combination of clinical, endoscopic, biochemical, and radiologic data [5, 6]. At our institution, CT enterography using neutral oral contrast material and thin-slice imaging is quickly replacing barium examination as the imaging technique of choice to evaluate Crohn's disease. CT enterography can show subtle changes in bowel wall thickening or enhancement that are often missed by barium examinations. In addition, unlike barium examinations, overlapping bowel loops are not obscured and abscesses are clearly identified.
Although several studies have shown the ability of CT enterography to aid in the diagnosis of Crohn's disease [1, 7-11], to our knowledge no study has yet shown whether changes on sequential CT enterography examinations in the same patient correlate to clinical changes. The purpose of this study was to determine whether imaging changes of Crohn's disease on sequential CT enterography examinations correlate with clinical disease progression or regression.
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Twenty patients (12 women, eight men) with a mean age of 55.5 years (range, 22-88 years) met the study criteria. All 20 patients underwent two CT enterography examinations, for a total of 20 imaging comparisons.
CT Enterography Technique
All patients undergoing CT enterography ingested a total of 1,350 mL of
neutral oral contrast material (0.1% weight/volume [w/v] barium sulfate
suspension, VoLumen, E-Z-EM) over a 45-minute period, drinking 450 mL of oral
contrast material at 15-minute intervals. Patients were scanned on a 4- or
16-MDCT scanner (Volume Zoom or Sensation 16, Siemens Medical Solutions).
Glucagon (0.5 mg) was given IV immediately before scanning, and 150 mL of IV
contrast material (iohexol; Omni paque, GE Healthcare) was given at a rate of
4 mL/s. Single-phase scanning during the enteric phase
[12] was performed after a
45-second delay. Images were acquired with a section thickness of 3 mm and a
reconstruction interval of 1.5 mm. Coronal reconstructions were performed at
3-mm-thick sections every 3 mm.
One radiologist with expertise in abdominal imaging, who was blinded to presenting symptoms and endoscopic results, reviewed all CT enterography examinations and recorded any imaging findings of Crohn's disease that were present in the small bowel or colon. Findings consistent with Crohn's disease included mucosal hyperenhancement, bowel wall thickening > 3 mm, bowel strictures, fistula, or abscess. While still blinded to clinical history and endoscopy results, the same radiologist then compared CT enterography examinations for each patient to determine whether imaging findings progressed, regressed, or remained stable between examinations. The location of disease was also recorded (colon, small bowel, or both).
Clinical Symptoms and Follow-Up
We used an electronic clinical database to record the presenting symptoms
at the office visit before each CT enterography. Symptoms included abdominal
pain, diarrhea, rectal bleeding, weight loss, nausea, and fever. A
gastroenterologist with expertise in inflammatory bowel disease, who was
blinded to CT enterography results, reviewed the clinical notes to determine
whether symptoms had progressed, regressed, or remained stable between
examinations.
Clinical follow-up after the second CT enterography examination was also performed using the electronic clinical note database. Interval changes in Crohn's disease treatment, symptoms, and length of follow-up were recorded.
Endoscopy
Although comparison with endoscopy was not a primary focus of this study,
any small-bowel endoscopic examinations performed within 6 months of CT
enterography were included for comparison, including colonoscopy with
ileoscopy and capsule endoscopy. A gastroenterologist with expertise in
inflammatory bowel disease reviewed all endoscopic examination reports and
images to identify findings consistent with Crohn's disease. These included
erythema, edema, erosions, ulcers, and strictures in the small bowel or
colon.
Data Analysis
The changes in symptoms and CT enterography findings were quantified using
three ordered categories: progression, stability, or regression. The agreement
of the change in CT enterography findings versus symptoms was measured using
the weighted kappa coefficient. The weighted kappa is the proportion of
agreement beyond that expected by chance, expressed relative to the maximum
possible agreement beyond that expected by chance. A high kappa value implies
a high degree of correlation between CT enterography and symptoms. The
percentage of CT enterography findings that agreed with symptoms overall and
for each category (progression, regression, stable) was reported. The
percentage of CT enterography findings that agreed with endoscopic findings
was also reported. The statistical uncertainty of the percentages was
quantified using the exact binomial method.
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Concordant Symptoms and CT Enterography
Disease progression or regression by CT enterography correlated with
symptoms in 16 of 20 (80%) patients. The weighted kappa statistic, which
measures the chance-adjusted agreement, was 0.57 (95% CI, 0.20-0.94). This
kappa value indicates that the correlation is higher than expected due to
chance, but not very high in practical terms.
Of the 16 patients with concordant symptoms and CT enterography, most had evidence of worsening disease (12/16, 75%) (Figs. 1A, 1B, 2A and 2B). Imaging findings at CT enterography included bowel wall thickening with mucosal hyperenhancement (n = 29 examinations), fistula (n = 2), abscess (n = 1), and small-bowel obstruction (n = 1). For patient symptoms, abdominal pain was the most common complaint (n = 26), followed by diarrhea (n = 11), rectal bleeding (n = 5), nausea (n = 5), weight loss (n = 3), and fever (n = 1). Several patients had more than one complaint. Most (11/12) patients with worsening findings on CT enterography received additional treatment for Crohn's disease. These patients showed symptomatic improvement at follow-up with changes in Crohn's disease medical therapy (n = 9), surgery (n = 1), and bowel rest (n = 1). One patient was not treated and had no change in symptoms.
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Two patients with concordant symptoms and CT enterography had evidence of disease regression. The two patients with improving symptoms (resolution of gastrointestinal bleeding) were imaged to exclude a mass lesion as a cause of nausea and to follow-up a known abdominal aortic aneurysm. CT enterography in these patients showed resolution or decrease in colonic wall thickening and enhancement. One patient underwent initial endoscopy confirming disease in the colon, but had neither follow-up endoscopy to confirm resolution nor a decrease in colonic disease. At follow-up, however, both patients were asymptomatic.
Two patients with concordant symptoms and CT enterography showed no change in either symptoms or imaging findings. These patients were imaged because of continued diarrhea despite treatment and to follow-up suspected colon strictures in the absence of symptoms. At CT enterography, one patient had stable mild thickening of the terminal ileum and the other remained negative. Neither of the patients underwent endoscopy. None of the patients with stable CT enterography findings received additional treatment for Crohn's disease, and both were asymptomatic at follow-up.
Discordant Symptoms and CT Enterography
Discordant CT enterography findings and symptoms were present in four of 20
(20%) patients. Two patients had worsening symptoms of pain but by CT
enterography were improved. One patient with improved CT enterography had
undergone interval resection of diseased small bowel, and the other had
decreased wall thickening and enhancement of the ileum. One endoscopy was
performed at the time of the second CT enterography in the patient with ileal
disease, which showed ileal erosions only. No initial endoscopy had been
performed for comparison to determine whether disease had improved on
endoscopy. At follow-up, both patients were asymptomatic without any change in
Crohn's disease therapy.
The two patients with negative CT enterography underwent a total of two ileoscopies and one capsule endoscopy, all of which were negative. At follow-up, one patient was asymptomatic after starting antidepressants and the other had stable pain. Therefore, in these four patients with symptoms of pain but no correlative change at CT enterography, all but one had resolution of symptoms without any change in Crohn's disease treatment.
Endoscopy
A total of 12 patients underwent 16 endoscopic examinations, including 15
attempted colonoscopies with ileoscopy and one capsule endoscopy. The mean
time between CT enterography and endoscopy was 18.3 ± 28 days (range,
0-100 days). Three patients underwent a total of four incomplete
colonoscopies, which were excluded from analysis.
Overall, 12 of 12 (100%) endoscopies correlated with CT enterography findings (i.e., positive endoscopy findings of Crohn's disease and positive CT enterography findings of Crohn's disease). Endoscopic findings correlated with symptoms in nine of 12 (75%) cases. The discrepant cases included three cases with symptoms of pain but negative ileoscopy (n = 2) and capsule endoscopy (n = 1). The most common findings at endoscopy were erosions (n = 6), ulcers (n = 5), and pseudopolyps (n = 1).
On the basis of endoscopy, there were two false-positive CT enterography examinations (suspected disease in the terminal ileum in one patient, the colon in another) and four false-negative CT enterography studies for colon disease found at endoscopy.
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CT enterography is a relatively new imaging technique that combines the improved spatial and temporal resolution of MDCT with large amounts of ingested neutral contrast material. Unlike routine CT, which uses high-density oral contrast material, CT enterography uses a low-density or neutral oral contrast material, allowing the detection of the abnormal mucosal enhancement that is common in Crohn's disease [1, 7, 11]. CT enterography also uses approximately three times more oral contrast material than routine CT examinations to optimize bowel distention. Advantages of CT enterography for the evaluation of Crohn's disease include its noninvasive nature, fast examination time (scanning time < 1 minute), and multiplanar projections. The multiplanar projections of CT enterography improve anatomic presentation of the bowel and can help clarify the presence of extramural complications [9, 11, 16].
In clinical practice, most patients will undergo a single initial evaluation with CT enterography to diagnose or exclude Crohn's disease, stage the disease, or help determine whether surgical intervention is necessary. Repeated CT enterography is typically not performed but may be when the clinical data are equivocal, conventional therapy has failed, the extent of disease needs to be established before starting more aggressive medical therapy, a complication is suspected, or development of functional symptoms (i.e., symptoms not related to Crohn's disease) is suspected. Although CT enterography is often used clinically in these situations, no study has previously been done to determine whether this method is accurate in assessing changes in Crohn's disease activity.
In our study, most patients (16/20) were reimaged because of progressive symptoms of Crohn's disease. In these patients, CT enterography confirmed progression of known disease in 12 of 16 patients (including enlargement of a known abscess) and detected a new small-bowel obstruction in one patient. All but one of these patients were subsequently treated medically or surgically for Crohn's disease with an improvement in symptoms, indicating that the worsening symptoms were due to Crohn's disease and not to a functional or non-Crohn's disease cause. Equally important, however, was the ability of CT enterography to exclude the presence of active Crohn's disease in four patients with worsening symptoms. Clinical follow-up confirmed that CT enterography was accurate in predicting that the worsening symptoms were not due to active Crohn's disease because three of four patients showed symptomatic improvement without any change in Crohn's disease therapy and the remaining patient had stable symptoms. In these patients, CT enterography was a useful tool to confirm the clinical suspicion that their symptoms were functional in cause. Therefore, in our small study, it appears that CT enterography is an accurate test to determine whether worsening symptoms are due to Crohn's disease.
Similar results have also been shown in a recent study assessing the ability of MR enterography to evaluate therapeutic response after Crohn's disease relapse [17]. In that study, 20 patients underwent MR enterography twice, once during clinically active Crohn's disease and another during clinical remission. As in our study, they found changes in bowel wall thickening and enhancement that correlated to clinically active disease or remission.
Whether to use MR enterography or CT enterography for assessing Crohn's disease activity requires consideration of several differences. MR enterography has several advantages, including the lack of ionizing radiation and the ability to give gadolinium contrast material in patients with iodinated contrast allergies. The main limitations of MR enterography are its high cost and that it is less available. CT enterography is more widely available, cheaper, and faster (20-seconds scanning time vs 30 minutes with MR enterography) than MR enterography. Overall, MR enterography is likely the best test for young patients because of the radiation dose saving. In older patients at decreased risk from radiation exposure, the benefit of MR enterography is debatable.
Comparison with endoscopy was not a primary focus of our study, but our findings suggest that CT enterography findings may provide better correlation with endoscopically active disease than patient symptoms provide. In a subgroup of patients, endoscopy correlated better with CT enterography findings (12/12, 100%) than did symptoms (9/12, 75%). Larger studies have also shown that findings of Crohn's disease at CT enterography correlate highly with endoscopy. For example, in a study of 96 patients who underwent CT enterography and ileoscopy, bowel wall thickening and enhancement on CT enterography correlated significantly (p < 0.001) with ileoscopic and histologic findings of active Crohn's disease [1]. In our study, CT enterography was less accurate in predicting the presence of colonic Crohn's disease. This is not surprising because CT enterography is not optimized for colonic distention; and with bowel underdistention, disease can be obscured or simulate abnormal wall thickening.
The main limitations of this study are the small sample size and its retrospective nature. This study is also at risk for selection bias because patients with worsening symptoms would be more likely to have repeated CT enterography examinations than patients who improved or remained stable [18]. Another limitation is that not all patients had endoscopic or histologic data available for comparison. Although endoscopy is the reference standard for diagnosing Crohn's disease, it is not always used to monitor disease activity and was used in a typically limited fashion in these patients. In addition, ileal intubation can be difficult in patients with scarring and strictures due to colonic Crohn's disease.
In conclusion, this preliminary study is the first to our knowledge to show that imaging changes between sequential CT enterography examinations may be useful for monitoring Crohn's disease progression or regression. In addition, small-bowel CT enterography findings correlated well with endoscopy in a subset of patients. Although CT enterography should not be used to routinely monitor disease because of the radiation exposure, it may be particularly useful when attempting to differentiate symptoms of Crohn's disease from functional symptoms or to assess for complications of Crohn's disease. In the future, larger prospective studies are needed to confirm these results.
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  S. A. Taylor, S. Punwani, M. Rodriguez-Justo, A. Bainbridge, R. Greenhalgh, E. De Vita, A. Forbes, R. Cohen, A. Windsor, A. Obichere, et al. Mural Crohn Disease: Correlation of Dynamic Contrast-enhanced MR Imaging Findings with Angiogenesis and Inflammation at Histologic Examination--Pilot Study Radiology, May 1, 2009; 251(2): 369 - 379. [Abstract] [Full Text] [PDF]
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