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MR Imaging in Patients with Crohn Disease: Value of T2- versus T1-weighted Gadolinium-enhanced MR Sequences with Use of an Oral Superparamagnetic Contrast Agent¹

¹ From the Departments of Radiological Sciences (F.M., A.B., M.C.C., M.M.), Clinical Sciences, Gastroenterology Unit (A.V., A.C., R.C.), and Surgical Sciences (C.M.), University of Rome La Sapienza, Via Regina Elena 324, 00161 Rome, Italy. Received February 8, 2004; revision requested April 15; final revision received March 18, 2005; accepted April 19. Address correspondence to F.M. (e-mail: francesca.maccioni{at}uniroma1.it).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Purpose: To prospectively compare oral contrast-enhanced T2-weighted half-Fourier rapid acquisition with relaxation enhancement (RARE) magnetic resonance (MR) imaging with T1-weighted gadolinium-enhanced fast low-angle shot (FLASH) MR and standard examinations in the evaluation of Crohn disease.

Materials and Methods: Institutional review board approval and informed consent were obtained. Fifty-nine patients with Crohn disease underwent MR imaging after oral administration of a superparamagnetic contrast agent; RARE plain and fat-suppressed sequences and FLASH sequences were performed before and after intravenous injection of gadolinium chelate. References were endoscopic, small-bowel barium, computed tomographic, ultrasonographic, and clinical-biochemical scoring of disease activity. Two radiologists analyzed MR images for presence and extent of Crohn disease lesions, presence of strictures or other complications, and degree of local inflammation. MR findings were correlated with endoscopic, radiologic, and clinical data ( statistic and Spearman rank correlation test).

Results: T2-weighted MR was 95% accurate, 98% sensitive, and 78% specific for detection of ileal lesions. Agreement between T1- and T2-weighted images ranged from 0.77 for ileal lesions to 1.00 for colic lesions. T2-weighted MR enabled detection of 26 of 29 severe strictures, 17 of 24 enteroenteric fistulas, and all adhesions and abscesses; T1-weighted MR enabled detection of 20 of 29 severe strictures, 16 of 24 enteroenteric fistulas, and all adhesions and abscesses. Complications leading to surgery were found in 12 (20%) patients; these were assessed correctly with either T1- or T2-weighted images. T2-weighted signal intensities of the wall and mesentery correlated with biologic activity (P < .001, r of 0.774 and 0.712, respectively). Interobserver agreement was 0.642–1.00 for T2-weighted and 0.711–1.00 for T1-weighted images.

Conclusion: T2-weighted MR can depict Crohn disease lesions and help assess mural and transmural inflammation with the same accuracy as gadolinium-enhanced T1-weighted MR. Combination of gadolinium-enhanced T1- and T2-weighted sequences is useful in the assessment of Crohn disease.

© RSNA, 2005

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Crohn disease is a chronic disorder of the entire alimentary tract that is characterized by an inflammatory process that extends through all the layers of the bowel wall and frequently leads to strictures, fistulas, and/or abscesses. Because this condition is treated with antiinflammatory drugs for long periods of time, a routine assessment of the inflammatory activity (ie, Crohn disease activity) is required to monitor the effects of medical therapy (1–4). At the same time, periodic evaluation of disease extent throughout the small and large bowels and detection of possible complications, such as strictures or fistulas, are also needed to determine the course and severity of the disease or to plan any changes in therapy (5).

According to several reports, magnetic resonance (MR) imaging is a valuable tool in the detection of main intestinal abnormalities in patients with Crohn disease and in the evaluation of disease activity (6–14). In addiction, MR imaging has several advantages compared with other imaging modalities, particularly computed tomography (CT), which plays a major role in the evaluation of patients with Crohn disease. First, MR imaging lacks ionizing radiation, which is extremely important, considering these patients are frequently young and will require numerous imaging studies during their lives to enable assessment of the evolution of their chronic disease. Second, it is widely accepted that the higher intrinsic contrast of MR imaging allows easier detection of inflammatory changes in human tissues. Third, since different MR imaging parameters can be used to evaluate any disease, MR imaging could offer additional information on Crohn disease with respect to CT. For example, T1- and T2-weighted MR sequences can be used, or the signal intensity can be modulated by selectively suppressing the fat signal intensity on T1- and T2-weighted images.

To our knowledge, there is still no agreement, however, regarding the MR imaging technique to be used, the choice of intestinal contrast agent (ie, positive, biphasic, or negative contrast agents) (15–24), or the type of contrast agent administration (ie, oral administration, administration through a nasojejunal tube, or MR enteroclysis) (9,18,19,22,25,26). Several studies on the detection of Crohn disease lesions have shown a higher diagnostic value of T1-weighted gadolinium-enhanced images compared with that of T2-weighted images (11,12). All of these studies were, however, based on the use of biphasic oral contrast agents (producing a dark lumen on T1-weighted images and a bright lumen on T2-weighted images), which are more valuable for T1-weighted sequences than for T2-weighted sequences.

T2-weighted sequences are widely considered to be extremely sensitive in the study of inflammatory human tissues (eg, musculoskeletal or nervous tissues), but their value is likely underestimated in inflammatory bowel diseases. Superparamagnetic agents (ie, iron oxide particles) reduce the high signal intensity of intestinal fluids on both T2- and T1-weighted MR images, thus producing a homogeneous negative contrast effect (10,17,20,23,24,26). To increase the depiction of the intestinal wall on T2-weighted images, fat-suppressed sequences can be used, as shown in previous studies (10,19).

Thus, the purpose of our study was to prospectively determine the accuracy of T2-weighted half-Fourier rapid acquisition with relaxation enhancement (RARE) sequences after oral administration of a negative oral contrast agent in the evaluation of Crohn disease lesions compared with the accuracies of T1-weighted gadolinium-enhanced fast low-angle shot (FLASH) sequences and reference-standard examinations, which included clinical and laboratory tests, ileocolic endoscopic examination, radiologic barium study of the small and large bowel, and surgical assessment.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Patient Population
The study protocol was approved by our institutional review board, and written informed consent was obtained from all the patients.

Between January and December 2002, 70 consecutive patients with a proved diagnosis of Crohn disease were prospectively selected for MR imaging studies during a periodic clinical and diagnostic assessment. All patients who had already undergone radiographic examination of the bowel in the previous 12 months were previously excluded from the study for radiation protection reasons. Two patients refused to undergo the examination because they were claustrophobic, while nine were excluded because they had already undergone MR imaging.

A total of 59 patients (30 men, 29 women) with a mean age of 46.3 years (age range, 18–76 years) were included in this study. The mean age of women was 46.7 years (age range, 18–70 years), and the mean age of men was 46.0 years (age range, 23–76 years). No statistical differences in age were found between women and men (P > .05). Researchers periodically followed up patients in the gastroenterology unit of our hospital (University of Rome La Sapienza, Rome, Italy), whereas imaging examinations were performed in the department of radiology at the same institution. MR imaging was included in the follow up of patients with Crohn disease, in association with ultrasonography (US), ileocolic endoscopic examination, barium enema study, clinical evaluation, and laboratory testing. The diagnosis of Crohn disease was always based on standard criteria (27) by associating findings of radiologic barium studies, endoscopies, and histologic evaluations of biopsy specimens. All patients were undergoing pharmacologic treatment with oral corticosteroids or other drugs (ie, azathioprine, infliximab, mesalazine, or antibiotics).

Patient Examination
Examination of patients included clinical evaluations, laboratory tests, ileocolic endoscopic examinations, and barium studies, all of which were performed either before or after MR imaging and within a maximum interval of 15 days.

Barium studies of the small bowel were performed in all the patients as a follow-through procedure or with enteroclysis, in accordance with standard techniques, by five experienced gastrointestinal radiologists (all of whom had more than 10 years of experience and were blinded to the results of MR imaging). The enteroclysis technique was based on the association of methylcellulose and barium sulfate as intestinal contrast agents, which were administered through a nasojejunal tube. Barium enema study of the colon was also performed whenever colonoscopy was not feasible or findings were incomplete, with use of the double-contrast technique.

Endoscopy of the colon and terminal ileum was planned for all patients within 15 days of MR imaging and was always performed by endoscopists with more than 8 years of experience who were blinded to the results of MR imaging and worked in the gastroenterology unit of our university hospital.

Location and length of the disease at the level of the small and large bowels (from jejunum to rectum), number and degree of strictures, and presence of fistulas were documented at ileocolic endoscopic examination and barium study; these tests were considered the reference examinations (5,28).

To assess other Crohn disease complications, such as abscesses, phlegmons and nonenteroenteric fistulas, each patient also underwent abdominal and pelvic US, which was performed by three experienced radiologists within 15 days of MR imaging. These radiologists were blinded to the results of MR imaging, and they used both 3.5- and 7.5-MHz probes. If a severe complication was found at US or strongly suspected at clinical examination, CT examination of the abdomen and pelvis was performed with a multi–detector row CT scanner (Somatom Plus 4 Volume Zoom; Siemens, Erlangen, Germany) and a standard technique for examination of the abdomen and pelvis.

Patients with severe complications of Crohn disease underwent surgery, which was considered to be the reference standard whenever it was performed.

The Crohn disease activity index (CDAI), according to the criteria proposed by Best et al (29,30), was evaluated in all patients within 1 week of MR imaging by an experienced gastroenterologist (A.V., with 10 years of experience) and a gastroenterology resident (A.C.). This index was used to assign a specific score to the different clinical signs and symptoms (eg, duration of symptoms, diarrhea, body temperature, abdominal pain). A CDAI score lower than 150 was considered inactive (scored as 0), a score between 150 and 350 was considered mildly to moderately active (scored as 1), and a score higher than 350 was considered severe (scored as 2).

Laboratory tests were performed within 1 week before or after MR imaging; white blood cell (WBC) count, erythrocyte sedimentation rate (ESR), C-reactive protein (CRP) level, orosomucoids level, and 1-acid-glycoprotein level were assessed. ESR was considered negative if it was less than or equal to 7 mm per minute (score of 0), positive and moderate if it was between 8 and 15 mm per minute (score of 1), and positive and high if it was greater than 15 mm per minute (score of 2). CRP was considered positive (score of 1) if CRP levels were higher than 5 mg/L and negative if CRP levels were lower than 5 mg/L (score of 0). A positive result from three of five laboratory tests indicated the presence of sustained inflammatory events or biologic activity, which was then scored as 1. If results of four or five tests were positive, biologic activity was considered high (scored as 2), whereas it was considered absent or not relevant (scored as 0) if results of two or fewer tests were positive.

In our study, the positivity of acute-phase reactants was considered the main index of biologic activity and served as the reference standard in the assessment of intestinal inflammatory activity. CDAI scores were compared with MR imaging findings but were not considered as a reference standard.

Patients underwent laboratory evaluation in different clinics; we excluded data based on reference values that were different from those used by us, as well as biochemical examinations dated 10 days before or after the date of the MR examination.

MR Imaging Technique
All patients were examined 1 hour after oral administration of 600–900 mL of the superparamagnetic contrast agent ferumoxsil (Lumirem; Laboratoires Guerbet, Paris, France), which is a suspension of silicone-coated iron oxide particles. The total volume of oral contrast material administered varied according to patient acceptance and intestinal length (in patients who had undergone previous surgical resection). Approximately 1 hour was needed for homogeneous distribution of the contrast material through the small and large bowel.

MR imaging examinations were performed with a 1.5-T system (Magnetom Vision Plus; Siemens) equipped with a phased-array coil. A standard MR imaging study for assessment of Crohn disease included T2-weighted RARE sequences, which were performed in the transverse and coronal planes to cover the entire upper and lower abdomen, with the following parameters: repetition time msec/echo time msec, 4.4/90; 150° flip angle; 160 x 256 matrix; 20-second breath hold; 20 sections acquired; 7-mm section thickness; 15% gap for transverse acquisitions; and no gap for coronal acquisitions. T2-weighted RARE sequences were performed after fat-suppression with a presaturation technique in only the transverse plane. Usually, two or three breath holds were required for imaging of the abdomen and pelvis, whereas one breath hold was sufficient for imaging of the coronal plane.

T1-weighted FLASH sequences were performed with the following parameters: 160/5.7, 20-second breath hold for 20 sections, 70°–90° flip angle, 160 x 256 matrix, 6-mm section thickness, 15% gap for the transverse plane, and no gap for the coronal plane. T1-weighted FLASH sequences were performed only in the transverse plane and without fat suppression before injection of gadolinium-based contrast material, whereas they were performed in the transverse and coronal planes after injection of gadolinium-based contrast material, with the addition of fat suppression. Intravenous injection of gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany) was performed with a power injector at a flow rate of 2 mL/sec and with a mean dose of 15 mL per patient (with a concentration of 0.18 mmol per kilogram of body weight) and followed by injection of 20 mL of saline; image acquisition was started 60 seconds after the beginning of the injection. After injection, transverse sequences through the abdomen and pelvis were performed first and followed by coronal sequences; all gadolinium-enhanced sequences required three or four breath holds. The median examination time was 30 minutes (range, 20–40 minutes).

Analysis of MR Images
Images were evaluated on film hard copies by an experienced gastrointestinal radiologist (F.M., with 8 years of experience in MR imaging of the gastrointestinal tract) and a diagnostic radiology resident (M.C.C.). Reviewers worked independently and were blinded to the results of clinical and endoscopic examinations and barium studies.

For each patient, T2- and T1-weighted images (groups A and B, respectively) were evaluated and scored in a randomized fashion in different sessions. In additional sessions, T1- and T2-weighted images were analyzed and scored together (group C).

The bowel was divided into seven different intestinal segments, as follows: jejunum, ileum, ascending colon, transverse colon, descending colon, sigmoid colon, and rectum, for a total of 413 segments.

Once the Crohn disease lesions were identified in one or more intestinal segments, the following parameters were assessed quantitatively or qualitatively:

In group A (ie, T2-weighted images obtained with and without fat suppression), we assessed the following parameters: (a) lesion site, (b) lesion extent (measured in centimeters), (c) number of strictures and their degree (based on the degree of prestenotic dilatation), (d) maximum bowel wall thickness (measured in millimeters), (e) bowel wall signal intensity, (f) signal intensity of fibrofatty proliferation on fat-suppressed images, and (g) local complications (eg, local free fluid, phlegmons, abscesses, or fistulas).

In group B (ie, T1-weighted images obtained before and after administration of gadolinium-based contrast agents), we assessed the following parameters: (a) lesion site, (b) lesion extent (measured in centimeters), (c) number of strictures and their degree (based on the degree of prestenotic dilatation), (d) maximum bowel wall thickness (measured in millimeters), (e) gadolinium enhancement of the bowel wall, (f) enhancement of fibrofatty proliferation, and (g) local complications (eg, local free fluid, phlegmons, abscesses, or fistulas).

In group C (ie, T1- and T2-weighted images together), we assessed the following parameters: (a) lesion site, (b) lesion extent (measured in centimeters), (c) number of strictures and their degree (based on the degree of prestenotic dilatation), (d) maximum bowel wall thickness (measured in millimeters), (e) degree of bowel wall inflammation (gadolinium enhancement and T2-weighted signal intensity) (f) signs of mesenteric inflammation, and (g) local complications (eg, local free fluid, phlegmons, abscesses, or fistulas).

Lesion site (parameter a) was classified with letters indicating one or more of the seven different previously mentioned intestinal segments. Lesion extent (parameter b) was measured in centimeters. Number of strictures (parameter c) was quantified as a given number or as zero. The degree of the strictures was considered mild when the lumen diameter above the stricture was slightly higher than the normal value, and it was considered moderate to severe when it was at least more than twice the normal value. Bowel wall thickness (parameter d) was qualitatively evaluated and considered normal (score of 0) when thickness was 4 mm or less, moderate (score of 1) when thickness was 4–7 mm, and marked (score of 2) when thickness was more than 7 mm.

In group A, signal intensity of the bowel wall on T2-weighted fat-suppressed images (parameter e) was considered abnormal if it was greater than that of the liver or spleen, absent or minimal (score of 0) if it was lower than that of the liver or spleen, mild (score of 1) if it was greater than that of the spleen but lower than that of the renal cortex, and marked (score of 2) if it was equal to that of the renal cortex or cerebrospinal fluid.

In group B, gadolinum enhancement of the bowel wall (parameter e) was considered abnormal if the degree of enhancement at visual inspection was greater than that of the splenic parenchyma. Gadolinum enhancement of the bowel wall was absent (score of 0) if no enhancement was observed, mild (score of 1) if enhancement of the bowel wall was greater than enhancement of the spleen but lower than enhancement of the renal cortex, and marked (score of 2) if enhancement of the bowel wall was equal to enhancement of the renal cortex or the intravascular signal, according to previous studies (11,12). In group C, both criteria were considered.

Increased perivisceral fat signal intensity on gadolinium-enhanced or T2-weighted fat-suppressed MR images (parameter f) was considered a sign of transmural inflammation and scored as 0 if it was absent (ie, normal fat tissue), as 1 if it was lower than that of the inflamed bowel wall, and as 2 if it was similar to hyperintensity of the bowel wall.

Morphologic and Activity-related MR Imaging Parameters
All MR imaging parameters of groups A, B, and C were divided into morphologic and activity-related groups. In groups A, B, and C, parameters a, b, c, and g (ie, lesion site, lesion extent, number of strictures and their degree, and local complications, respectively) were considered morphologic parameters and evaluated quantitatively, whereas parameters related to mural and extramural inflammation (activity-related parameters) were assessed qualitatively. The images were analyzed quantitatively and qualitatively on film hard copies for groups A, B, C.

The reference standards for morphologic parameters were endoscopy and barium study. Reference standards for parameter g (ie, local complications) were CT, US, and surgery for abscesses and phlegmons that were treated surgically; CT for phlegmons that were treated conservatively; and barium enema for fistulas.

The reference standard for parameters d, e, and f of all activity-related groups was the biologic activity considered on a per-patient basis. The results were also compared with biologic tests and with the CDAI. If more than one bowel segment was involved, only the site of maximum MR activity was considered for statistical correlation with the reference examination.

Statistical Analysis
Statistical differences in age between men and women were calculated with the Kolmogorov-Smirnov test. A P value of less than .05 indicated a statistically significant difference. Interobserver agreement on MR imaging parameters was calculated with the statistic. The general linear model test has been used to compare lengths of diseased segments (pairwise comparison).

MR imaging parameters of groups A, B, and C were compared with the reference biologic activity by using nonparametric statistical analysis (Spearman rank correlation); P values less than .05 were considered to indicate a statistically significant difference. Correlation between different T1- and T2-weighted parameters was performed by using the statistic. The statistical software used was SPSS for Windows (release 10.0.0; SPSS, Chicago, Ill).

Sensitivity, specificity, positive and negative predictive values, and accuracy were assessed with standard formulas. Although we report the interobserver agreement between an experienced gastrointestinal radiologist and a 4th-year resident for lesion detection at any level of the gastrointestinal tract, we considered only those results that were obtained from the experienced radiologist (reader 1) for analysis of sensitivity and specificity.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Patient Evaluation
Small-bowel barium studies were performed in all patients (ie, small-bowel follow-through studies in 30 patients and enteroclyses in 29) (Tables 1 –3). Colonoscopy was considered complete in 45 of 59 patients, with the last 10 cm of the ileum also assessed. In 11 patients, colonoscopy was incomplete or could not be performed because of the severity of the disease, and three patients refused the examination. In these 14 patients, the colon was evaluated with a barium enema study.

A total of 47 strictures were found at the level of the small and large bowel in 22 patients who underwent barium studies or ileocolic endoscopic examinations. On the basis of the degree of prestenotic dilation, 29 strictures were judged to be severe or moderate and 18 were judged to be mild; three strictures required surgery.

Enteroenteric fistulas were found in nine patients; one patient with complex enteroenteric and cutaneous fistulas underwent surgery.

Results of radiologic barium studies and endoscopy regarding location and length of the disease at the level of the small and large bowel (from the jejunum to the rectum), number and degree of the strictures, and presence of fistulas are reported in Tables 1–3.

Clinical activity was evaluated with the CDAI, which showed that Crohn disease was active in 50 patients (CDAI score > 150) and in clinical remission in nine. Among the 50 patients with active Crohn disease, 32 had a CDAI value of 150–350, whereas 18 had more severe symptoms and a CDAI of more than 350.

Laboratory tests showed that 45 of 59 patients had a positive CRP level and 56 of 59 patients had an ESR higher than 7 mm per minute; ESR ranged from 8 to 15 mm per minute in 26 of 59 patients and was higher than 15 mm per minute in 30 patients. By considering all the positive acute-phase reactants, the biologic activity was found to be very high (four or five positive reactants) in 27 patients, moderate (three positive reactants) in 22 patients, and absent (only two or fewer positive reactants) in 10 patients.

Eight patients underwent surgery to treat an abscess or phlegmon (n = 5) or a complex fistulous tract involving the psoas muscle (n = 1), the urinary bladder (n = 1), or the ovaries (n = 1). Three patients underwent surgery to treat severe intestinal strictures, and one patient underwent surgery to treat complex enteroenteric cutaneous fistulas.

In total, 12 (20%) of 59 patients underwent surgery to treat complicated Crohn disease 5–30 days after MR examination.

Morphologic Assessment of Crohn Disease with MR Imaging
Identification of lesion site.—In the detection and localization of Crohn disease lesions from the jejunum to the rectum (Figs 1, 2), T2-weighted RARE images showed an accuracy of 93%–95%, with a mean value of 95% (Tables 4–6). In the depiction of ileal lesions, they showed 98% sensitivity, 78% specificity, 96% positive predictive value, and 88% negative predictive value (Figs 1a, 1b, 2a, 2c–2e).

View larger version (107K): [in this window] [in a new window]   Figure 1a: MR images in a 28-year-old man with known Crohn disease and high biologic activity (positive ESR, CRP level, and WBC count) and positive clinical indexes of activity (CDAI > 150). (a, b) T2-weighted RARE transverse images obtained (a) without and (b) with fat suppression after oral administration of a negative contrast agent show marked diffuse wall thickening (arrow) at level of the terminal ileum, with minimal perivisceral free fluid; this can be seen better on b (arrowhead). After suppression, T2-weighted signal intensity of the wall is extremely high, suggesting diffuse wall edema and active disease. Adjacent bowel loops do not show wall or luminal abnormalities; they are clearly depicted because of low signal intensity of intestinal contrast agent. (c) Gadolinium-enhanced FLASH T1-weighted transverse MR image obtained with fat suppression show marked diffuse wall thickening and marked wall enhancement at level of the distal ileum (arrow) and dilatation of local mesenteric vessels (ie, "comb sign") (arrowheads) (31). These findings are concordant with those observed on T2-weighted images and are suggestive of active Crohn disease.

View larger version (111K): [in this window] [in a new window]   Figure 1b: MR images in a 28-year-old man with known Crohn disease and high biologic activity (positive ESR, CRP level, and WBC count) and positive clinical indexes of activity (CDAI > 150). (a, b) T2-weighted RARE transverse images obtained (a) without and (b) with fat suppression after oral administration of a negative contrast agent show marked diffuse wall thickening (arrow) at level of the terminal ileum, with minimal perivisceral free fluid; this can be seen better on b (arrowhead). After suppression, T2-weighted signal intensity of the wall is extremely high, suggesting diffuse wall edema and active disease. Adjacent bowel loops do not show wall or luminal abnormalities; they are clearly depicted because of low signal intensity of intestinal contrast agent. (c) Gadolinium-enhanced FLASH T1-weighted transverse MR image obtained with fat suppression show marked diffuse wall thickening and marked wall enhancement at level of the distal ileum (arrow) and dilatation of local mesenteric vessels (ie, "comb sign") (arrowheads) (31). These findings are concordant with those observed on T2-weighted images and are suggestive of active Crohn disease.

View larger version (112K): [in this window] [in a new window]   Figure 1c: MR images in a 28-year-old man with known Crohn disease and high biologic activity (positive ESR, CRP level, and WBC count) and positive clinical indexes of activity (CDAI > 150). (a, b) T2-weighted RARE transverse images obtained (a) without and (b) with fat suppression after oral administration of a negative contrast agent show marked diffuse wall thickening (arrow) at level of the terminal ileum, with minimal perivisceral free fluid; this can be seen better on b (arrowhead). After suppression, T2-weighted signal intensity of the wall is extremely high, suggesting diffuse wall edema and active disease. Adjacent bowel loops do not show wall or luminal abnormalities; they are clearly depicted because of low signal intensity of intestinal contrast agent. (c) Gadolinium-enhanced FLASH T1-weighted transverse MR image obtained with fat suppression show marked diffuse wall thickening and marked wall enhancement at level of the distal ileum (arrow) and dilatation of local mesenteric vessels (ie, "comb sign") (arrowheads) (31). These findings are concordant with those observed on T2-weighted images and are suggestive of active Crohn disease.

View larger version (172K): [in this window] [in a new window]   Figure 2a: MR images show recurrence of Crohn disease in a 52-year-old man who underwent resection of the terminal ileum and descending colon 12 years earlier; this patient had a low level of biologic disease activity (negative ESR, CRP level, and WBC count) but positive clinical indexes of activity (ie, CDAI > 150). (a) Coronal T2-weighted RARE image obtained after oral administration of a negative contrast agent. Recurrent Crohn disease at the level of the anastomotic ileal loop is clearly evident (arrows); the affected bowel loop shows thickened walls, reduced and irregular lumen over approximately 20 cm, and mild bowel dilatation above the stricture. Marked mesenteric fibrofatty proliferation (*) is also evident, separating the affected bowel segment from the adjacent normal ileal and jejunal loops. (b) Coronal FLASH T1-weighted MR image obtained after intravenous injection of gadolinium-based contrast material. Diffuse wall thickening, increased wall enhancement, and lumen stenosis were observed at the level of the ileal anastomotic loop, suggesting recurrent Crohn disease (arrows). Bowel dilatation above the stricture is, however, less evident on this image than on the corresponding T2-weighted image. (c) Image obtained at follow-through barium examination shows a long inflammatory stricture (arrows) at the level of the anastomotic ileal loop. Marked fibrofatty proliferation is possible owing to separation of the affected bowel segment from the normal ileal and jejunal loops. (d) Transverse T2-weighted RARE image shows wall thickening at the level of the anastomotic loop (arrow) and inhomogeneity and increased volume of the perivisceral fat tissue, which separates the affected loop from the other ileal loops. (e) Transverse fat-suppressed T2-weighted fast spin-echo image obtained at the same level. The T2-weighted signal intensity of the wall (arrow) is moderate; no signal intensity is evident at the level of the fibrofatty proliferation; this finding suggests the presence of chronic moderately active disease. (f) Transverse fat-suppressed T1-weighted FLASH image obtained at the same level. Layered wall enhancement (arrow) is evident, as is dilatation of the mesenteric vessels. These findings are suggestive of chronic moderately active disease.

View larger version (191K): [in this window] [in a new window]   Figure 2b: MR images show recurrence of Crohn disease in a 52-year-old man who underwent resection of the terminal ileum and descending colon 12 years earlier; this patient had a low level of biologic disease activity (negative ESR, CRP level, and WBC count) but positive clinical indexes of activity (ie, CDAI > 150). (a) Coronal T2-weighted RARE image obtained after oral administration of a negative contrast agent. Recurrent Crohn disease at the level of the anastomotic ileal loop is clearly evident (arrows); the affected bowel loop shows thickened walls, reduced and irregular lumen over approximately 20 cm, and mild bowel dilatation above the stricture. Marked mesenteric fibrofatty proliferation (*) is also evident, separating the affected bowel segment from the adjacent normal ileal and jejunal loops. (b) Coronal FLASH T1-weighted MR image obtained after intravenous injection of gadolinium-based contrast material. Diffuse wall thickening, increased wall enhancement, and lumen stenosis were observed at the level of the ileal anastomotic loop, suggesting recurrent Crohn disease (arrows). Bowel dilatation above the stricture is, however, less evident on this image than on the corresponding T2-weighted image. (c) Image obtained at follow-through barium examination shows a long inflammatory stricture (arrows) at the level of the anastomotic ileal loop. Marked fibrofatty proliferation is possible owing to separation of the affected bowel segment from the normal ileal and jejunal loops. (d) Transverse T2-weighted RARE image shows wall thickening at the level of the anastomotic loop (arrow) and inhomogeneity and increased volume of the perivisceral fat tissue, which separates the affected loop from the other ileal loops. (e) Transverse fat-suppressed T2-weighted fast spin-echo image obtained at the same level. The T2-weighted signal intensity of the wall (arrow) is moderate; no signal intensity is evident at the level of the fibrofatty proliferation; this finding suggests the presence of chronic moderately active disease. (f) Transverse fat-suppressed T1-weighted FLASH image obtained at the same level. Layered wall enhancement (arrow) is evident, as is dilatation of the mesenteric vessels. These findings are suggestive of chronic moderately active disease.

View larger version (116K): [in this window] [in a new window]   Figure 2c: MR images show recurrence of Crohn disease in a 52-year-old man who underwent resection of the terminal ileum and descending colon 12 years earlier; this patient had a low level of biologic disease activity (negative ESR, CRP level, and WBC count) but positive clinical indexes of activity (ie, CDAI > 150). (a) Coronal T2-weighted RARE image obtained after oral administration of a negative contrast agent. Recurrent Crohn disease at the level of the anastomotic ileal loop is clearly evident (arrows); the affected bowel loop shows thickened walls, reduced and irregular lumen over approximately 20 cm, and mild bowel dilatation above the stricture. Marked mesenteric fibrofatty proliferation (*) is also evident, separating the affected bowel segment from the adjacent normal ileal and jejunal loops. (b) Coronal FLASH T1-weighted MR image obtained after intravenous injection of gadolinium-based contrast material. Diffuse wall thickening, increased wall enhancement, and lumen stenosis were observed at the level of the ileal anastomotic loop, suggesting recurrent Crohn disease (arrows). Bowel dilatation above the stricture is, however, less evident on this image than on the corresponding T2-weighted image. (c) Image obtained at follow-through barium examination shows a long inflammatory stricture (arrows) at the level of the anastomotic ileal loop. Marked fibrofatty proliferation is possible owing to separation of the affected bowel segment from the normal ileal and jejunal loops. (d) Transverse T2-weighted RARE image shows wall thickening at the level of the anastomotic loop (arrow) and inhomogeneity and increased volume of the perivisceral fat tissue, which separates the affected loop from the other ileal loops. (e) Transverse fat-suppressed T2-weighted fast spin-echo image obtained at the same level. The T2-weighted signal intensity of the wall (arrow) is moderate; no signal intensity is evident at the level of the fibrofatty proliferation; this finding suggests the presence of chronic moderately active disease. (f) Transverse fat-suppressed T1-weighted FLASH image obtained at the same level. Layered wall enhancement (arrow) is evident, as is dilatation of the mesenteric vessels. These findings are suggestive of chronic moderately active disease.

View larger version (98K): [in this window] [in a new window]   Figure 2d: MR images show recurrence of Crohn disease in a 52-year-old man who underwent resection of the terminal ileum and descending colon 12 years earlier; this patient had a low level of biologic disease activity (negative ESR, CRP level, and WBC count) but positive clinical indexes of activity (ie, CDAI > 150). (a) Coronal T2-weighted RARE image obtained after oral administration of a negative contrast agent. Recurrent Crohn disease at the level of the anastomotic ileal loop is clearly evident (arrows); the affected bowel loop shows thickened walls, reduced and irregular lumen over approximately 20 cm, and mild bowel dilatation above the stricture. Marked mesenteric fibrofatty proliferation (*) is also evident, separating the affected bowel segment from the adjacent normal ileal and jejunal loops. (b) Coronal FLASH T1-weighted MR image obtained after intravenous injection of gadolinium-based contrast material. Diffuse wall thickening, increased wall enhancement, and lumen stenosis were observed at the level of the ileal anastomotic loop, suggesting recurrent Crohn disease (arrows). Bowel dilatation above the stricture is, however, less evident on this image than on the corresponding T2-weighted image. (c) Image obtained at follow-through barium examination shows a long inflammatory stricture (arrows) at the level of the anastomotic ileal loop. Marked fibrofatty proliferation is possible owing to separation of the affected bowel segment from the normal ileal and jejunal loops. (d) Transverse T2-weighted RARE image shows wall thickening at the level of the anastomotic loop (arrow) and inhomogeneity and increased volume of the perivisceral fat tissue, which separates the affected loop from the other ileal loops. (e) Transverse fat-suppressed T2-weighted fast spin-echo image obtained at the same level. The T2-weighted signal intensity of the wall (arrow) is moderate; no signal intensity is evident at the level of the fibrofatty proliferation; this finding suggests the presence of chronic moderately active disease. (f) Transverse fat-suppressed T1-weighted FLASH image obtained at the same level. Layered wall enhancement (arrow) is evident, as is dilatation of the mesenteric vessels. These findings are suggestive of chronic moderately active disease.

View larger version (114K): [in this window] [in a new window]   Figure 2e: MR images show recurrence of Crohn disease in a 52-year-old man who underwent resection of the terminal ileum and descending colon 12 years earlier; this patient had a low level of biologic disease activity (negative ESR, CRP level, and WBC count) but positive clinical indexes of activity (ie, CDAI > 150). (a) Coronal T2-weighted RARE image obtained after oral administration of a negative contrast agent. Recurrent Crohn disease at the level of the anastomotic ileal loop is clearly evident (arrows); the affected bowel loop shows thickened walls, reduced and irregular lumen over approximately 20 cm, and mild bowel dilatation above the stricture. Marked mesenteric fibrofatty proliferation (*) is also evident, separating the affected bowel segment from the adjacent normal ileal and jejunal loops. (b) Coronal FLASH T1-weighted MR image obtained after intravenous injection of gadolinium-based contrast material. Diffuse wall thickening, increased wall enhancement, and lumen stenosis were observed at the level of the ileal anastomotic loop, suggesting recurrent Crohn disease (arrows). Bowel dilatation above the stricture is, however, less evident on this image than on the corresponding T2-weighted image. (c) Image obtained at follow-through barium examination shows a long inflammatory stricture (arrows) at the level of the anastomotic ileal loop. Marked fibrofatty proliferation is possible owing to separation of the affected bowel segment from the normal ileal and jejunal loops. (d) Transverse T2-weighted RARE image shows wall thickening at the level of the anastomotic loop (arrow) and inhomogeneity and increased volume of the perivisceral fat tissue, which separates the affected loop from the other ileal loops. (e) Transverse fat-suppressed T2-weighted fast spin-echo image obtained at the same level. The T2-weighted signal intensity of the wall (arrow) is moderate; no signal intensity is evident at the level of the fibrofatty proliferation; this finding suggests the presence of chronic moderately active disease. (f) Transverse fat-suppressed T1-weighted FLASH image obtained at the same level. Layered wall enhancement (arrow) is evident, as is dilatation of the mesenteric vessels. These findings are suggestive of chronic moderately active disease.

View larger version (117K): [in this window] [in a new window]   Figure 2f: MR images show recurrence of Crohn disease in a 52-year-old man who underwent resection of the terminal ileum and descending colon 12 years earlier; this patient had a low level of biologic disease activity (negative ESR, CRP level, and WBC count) but positive clinical indexes of activity (ie, CDAI > 150). (a) Coronal T2-weighted RARE image obtained after oral administration of a negative contrast agent. Recurrent Crohn disease at the level of the anastomotic ileal loop is clearly evident (arrows); the affected bowel loop shows thickened walls, reduced and irregular lumen over approximately 20 cm, and mild bowel dilatation above the stricture. Marked mesenteric fibrofatty proliferation (*) is also evident, separating the affected bowel segment from the adjacent normal ileal and jejunal loops. (b) Coronal FLASH T1-weighted MR image obtained after intravenous injection of gadolinium-based contrast material. Diffuse wall thickening, increased wall enhancement, and lumen stenosis were observed at the level of the ileal anastomotic loop, suggesting recurrent Crohn disease (arrows). Bowel dilatation above the stricture is, however, less evident on this image than on the corresponding T2-weighted image. (c) Image obtained at follow-through barium examination shows a long inflammatory stricture (arrows) at the level of the anastomotic ileal loop. Marked fibrofatty proliferation is possible owing to separation of the affected bowel segment from the normal ileal and jejunal loops. (d) Transverse T2-weighted RARE image shows wall thickening at the level of the anastomotic loop (arrow) and inhomogeneity and increased volume of the perivisceral fat tissue, which separates the affected loop from the other ileal loops. (e) Transverse fat-suppressed T2-weighted fast spin-echo image obtained at the same level. The T2-weighted signal intensity of the wall (arrow) is moderate; no signal intensity is evident at the level of the fibrofatty proliferation; this finding suggests the presence of chronic moderately active disease. (f) Transverse fat-suppressed T1-weighted FLASH image obtained at the same level. Layered wall enhancement (arrow) is evident, as is dilatation of the mesenteric vessels. These findings are suggestive of chronic moderately active disease.

For the detection of Crohn disease lesions at any level of the gastrointestinal tract, good statistical agreement was present between T1-weighted gadolinium-enhanced and T2-weighted MR images (Figs 1b, 1c), with values of 0.77 for ileal lesions and 1.00 for colic lesions (Table 6).

Detection of disease extent.—In the assessment of disease extent, a statistical difference between T2-weighted sequences and the reference standard was not found (P > .05) (Table 1). The mean disease length was 35.5 cm (median length, 35 cm; standard deviation, 21.2 cm) for MR imaging examinations and 36.3 cm (median length, 36 cm; standard deviation, 19.2 cm) for reference examinations (Fig 2a–2c).

Detection of strictures and other complications.—MR imaging enabled detection of 39 (83%) of 47 strictures in 20 patients, with underestimation of low-grade (13 of 18 were detected) rather than high-grade strictures (26 of 29 were detected) (Table 3).

T2-weighted RARE sequences were used to detect 39 of 47 strictures in 20 patients. The accuracy of T1-weighted gadolinium-enhanced sequences was slightly lower, enabling detection of 31 of 47 strictures in 16 patients (Fig 2a–2c). The overall sensitivity, specificity, and accuracy of T2-weighted sequences in the detection of strictures were 83%, 100%, and 91%, respectively, whereas the overall sensitivity, specificity, and accuracy of T1-weighted gadolinium-enhanced sequences were 66%, 100%, and 81%, respectively.

At reference examinations, 24 enteroenteric fistulas were found in nine patients. T2- and T1-weighted sequences enabled detection of 17 (71%) of 24 and 16 (66%) of 24 enteroenteric fistulas, respectively (Fig 3); the association of T1- with T2-weighted images increased the overall detection rate to 75% (18 of 24 enteroenteric fistulas); in two (22%) of nine patients, fistulas were misinterpreted as tight adhesions. The overall sensitivity, specificity, and accuracy of T2-weighted sequences in the detection of enteric fistulas were 71%, 100%, and 91%, respectively, whereas overall sensitivity, specificity, and accuracy of T1-weighted gadolinium-enhanced sequences were 67%, 100%, and 89%, respectively.

View larger version (144K): [in this window] [in a new window]   Figure 3a: MR images obtained in a 41-year-old man with a 20-year history of Crohn disease. (a) T2-weighted RARE coronal image obtained after oral administration of a negative contrast agent. In the pelvis, slightly to the right of the midline, an ileal loop is angulated, and it converges (arrow) with other ileal loops; this suggests the presence of enteroenteric fistulas. (b) T1-weighted FLASH coronal image, obtained after intravenous injection of gadolinium-based contrast material. In the pelvis, slightly to the right of the midline, an ileal loop sharply converges (arrow) with other ileal loops; this finding is suggestive of enteroenteric fistulas. All the involved bowel loops show increased bowel wall enhancement.

View larger version (147K): [in this window] [in a new window]   Figure 3b: MR images obtained in a 41-year-old man with a 20-year history of Crohn disease. (a) T2-weighted RARE coronal image obtained after oral administration of a negative contrast agent. In the pelvis, slightly to the right of the midline, an ileal loop is angulated, and it converges (arrow) with other ileal loops; this suggests the presence of enteroenteric fistulas. (b) T1-weighted FLASH coronal image, obtained after intravenous injection of gadolinium-based contrast material. In the pelvis, slightly to the right of the midline, an ileal loop sharply converges (arrow) with other ileal loops; this finding is suggestive of enteroenteric fistulas. All the involved bowel loops show increased bowel wall enhancement.

Enteric fistulas were missed at MR imaging in two patients, but complex nonenteroenteric fistulous tracts were diagnosed with MR imaging in three patients. A large number of adhesions (48 adhesions in 20 patients), all of which were underestimated with reference examinations, were detected with MR imaging.

MR imaging revealed four abscesses in four patients (Fig 4); all abscesses were confirmed at surgery but were undetected at barium study or colonoscopy. MR imaging also depicted three phlegmons. One phlegmon was treated with surgical resection, and the other two were treated with pharmacologic therapy and confirmed with other imaging modalities (US and CT). All abscesses and phlegmons were diagnosed with both T1- and T2-weighted images (Fig 4a, 4b).

View larger version (134K): [in this window] [in a new window]   Figure 4a: MR images obtained in a 21-year-old man with known Crohn disease of the distal ileum that was treated with corticosteroids. Patient history included recent mild worsening of symptoms and lower abdominal pain in association with increased ESR, CRP level, and WBC count without fever. Patient underwent MR imaging and, 24 hours later, surgery. At surgery, a large abscess arising from the distal ileum that required ileocecal resection was found; no resection of the descending colon was needed. (a) Transverse fat-suppressed T1-weighted FLASH image obtained after injection of gadolinium chelates. A large fluid collection surrounded by contrast-enhanced inflammatory tissue (black arrows) anteriorly displaces the distal ileum (white arrows) adjacent to the descending colon. Both the wall of the distal ileum (white arrows) and the descending colon (white arrowhead) are characterized by marked gadolinium enhancement. (b) T2-weighted RARE transverse image. Note the descending colon (white arrowhead), the distal ileal loop (black arrows), and the large fluid collection (white arrows), which is characterized by high signal intensity and likely arises from the posterior mesenteric border of the ileal loop. (c) T2-weighted RARE coronal image. Note the large fluid collection (white arrows) between the distal ileal loop (black arrows) and the descending colon (white arrowhead). The high-signal-intensity fluid collection can be easily distinguished from the adjacent normal bowel loops, all of which have a low-signal-intensity lumen after the administration of a negative oral contrast agent.

View larger version (125K): [in this window] [in a new window]   Figure 4b: MR images obtained in a 21-year-old man with known Crohn disease of the distal ileum that was treated with corticosteroids. Patient history included recent mild worsening of symptoms and lower abdominal pain in association with increased ESR, CRP level, and WBC count without fever. Patient underwent MR imaging and, 24 hours later, surgery. At surgery, a large abscess arising from the distal ileum that required ileocecal resection was found; no resection of the descending colon was needed. (a) Transverse fat-suppressed T1-weighted FLASH image obtained after injection of gadolinium chelates. A large fluid collection surrounded by contrast-enhanced inflammatory tissue (black arrows) anteriorly displaces the distal ileum (white arrows) adjacent to the descending colon. Both the wall of the distal ileum (white arrows) and the descending colon (white arrowhead) are characterized by marked gadolinium enhancement. (b) T2-weighted RARE transverse image. Note the descending colon (white arrowhead), the distal ileal loop (black arrows), and the large fluid collection (white arrows), which is characterized by high signal intensity and likely arises from the posterior mesenteric border of the ileal loop. (c) T2-weighted RARE coronal image. Note the large fluid collection (white arrows) between the distal ileal loop (black arrows) and the descending colon (white arrowhead). The high-signal-intensity fluid collection can be easily distinguished from the adjacent normal bowel loops, all of which have a low-signal-intensity lumen after the administration of a negative oral contrast agent.

View larger version (170K): [in this window] [in a new window]   Figure 4c: MR images obtained in a 21-year-old man with known Crohn disease of the distal ileum that was treated with corticosteroids. Patient history included recent mild worsening of symptoms and lower abdominal pain in association with increased ESR, CRP level, and WBC count without fever. Patient underwent MR imaging and, 24 hours later, surgery. At surgery, a large abscess arising from the distal ileum that required ileocecal resection was found; no resection of the descending colon was needed. (a) Transverse fat-suppressed T1-weighted FLASH image obtained after injection of gadolinium chelates. A large fluid collection surrounded by contrast-enhanced inflammatory tissue (black arrows) anteriorly displaces the distal ileum (white arrows) adjacent to the descending colon. Both the wall of the distal ileum (white arrows) and the descending colon (white arrowhead) are characterized by marked gadolinium enhancement. (b) T2-weighted RARE transverse image. Note the descending colon (white arrowhead), the distal ileal loop (black arrows), and the large fluid collection (white arrows), which is characterized by high signal intensity and likely arises from the posterior mesenteric border of the ileal loop. (c) T2-weighted RARE coronal image. Note the large fluid collection (white arrows) between the distal ileal loop (black arrows) and the descending colon (white arrowhead). The high-signal-intensity fluid collection can be easily distinguished from the adjacent normal bowel loops, all of which have a low-signal-intensity lumen after the administration of a negative oral contrast agent.

T2-related parameters (parameters e and f, group A) were related to T1-weighted bowel wall gadolinium enhancement (parameter e, group B): T2-weighted bowel wall and fat signal intensities showed correlation values of 0.919 and 0.852, respectively, with wall gadolinium enhancement (P < .001) (Fig 1).

Weak correlations were obtained by correlating the CDAI with the MR imaging parameters (Table 7).

Interobserver Agreement
Interobserver agreement was considered statistically significant for all parameters evaluated (Tables 8, 9). In the detection of lesions located between the jejunum and the rectum, a high level of agreement was observed on T1- and T2-weighted images (Table 7), with coefficient values ranging from 0.642 to more than 0.999. The highest agreement was obtained in the evaluation of lesions located in the right side of the body and the descending colon on T2-weighted images ( = 0.924 and 0.914, respectively). In the assessment of activity-related MR parameters, the overall agreement was very good, with values ranging from 0.797 to 0.865 (Table 8). The Spearman rank correlation overall results are reported in Table 6.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

On the other hand, the value of T2-weighted sequences in the evaluation of Crohn disease is still controversial, although the T2-weighted signal intensity is expected to be increased at the level of the inflamed bowel wall (10,13,14,16,21,32). Preliminary studies found an increase in T2-weighted signal intensity at the level of the inflamed wall and perivisceral fat tissue in patients with active Crohn disease (10,19), whereas other studies (11,12) found an overall lower diagnostic value of T2-weighted sequences in comparison with T1-weighted sequences, either in the evaluation of morphologic changes of Crohn disease or in the assessment of disease activity.

To highlight the T2-weighted signal intensity of the inflamed bowel wall, we chose a negative superparamagnetic oral contrast agent (ie, iron oxide particles) rather than a positive or biphasic one for several reasons: The diagnostic value of T2-weighted MR images significantly improves after administration of a negative contrast agent (20,23). On T2-weighted images, in fact, the signal intensity of the bowel content is markedly inhomogeneous, owing to the brightness of intestinal fluids, the darkness of air, and the intermediate signal intensity of stool. After administration of the negative intestinal contrast agent, a homogeneous low signal intensity, similar to that of intestinal air, is obtained throughout the bowel. Such homogeneous signal intensity cannot be obtained with an intestinal contrast agent producing high signal intensity on T2-weighted images because of the residual low signal intensity of air. Furthermore, if combined with fat suppression, the low signal intensity of the lumen allows the T2-weighted signal intensity of the inflamed wall and minimal amounts of perivisceral fluid or edema of the mesenteric fat to be seen; these are hardly ever seen, otherwise (Fig 1a, 1b). The superparamagnetic intestinal contrast agent also improves the quality of T1-weighted gadolinium-enhanced images by homogeneously decreasing the signal intensity of the lumen, thus highlighting wall enhancement (Fig 1c) (10–16).

Moreover, we chose oral administration of contrast material instead of enteroclysis for specific reasons. First, patient acceptance of oral contrast material is better, and the examination is relatively simple, lasting a total of 30–40 minutes. The placement of a nasojejunal tube requires more time and radiation exposure, and it causes patient discomfort. Second, oral administration allows evaluation of the entire small and large bowel, from the duodenum to the sigmoid colon. With enteroclysis, disease confined to the duodenum or proximal jejunum can be missed. Moreover, distending the small bowel to its maximum can reduce the evidence of large-bowel disease because the colon is compressed by the distended small-bowel loops. Similarly, mesenteric or peritoneal disease (ie, adhesions) can be underestimated with marked bowel dilatation. Finally, assessment of bowel wall and mesenteric signal intensity, which is crucial in the evaluation of transmural inflammatory bowel disease, is better performed with moderate rather than marked lumen dilatation.

A possible disadvantage of oral contrast agent administration is the possibility of suboptimal intestinal filling in case of low patient compliance; however, this was rarely observed in our series. Poor intestinal distention may cause underestimation of low-grade strictures.

To validate this MR imaging technique and to assess the accuracy of T2-weighted MR sequences in patients with Crohn disease, we considered several MR imaging parameters related to the disease. We assessed T1- and T2-weighted images, both separately and together; 413 intestinal segments were evaluated in 59 patients, and we adopted a per-segment rather than a per-patient approach. This can be considered a limitation of our study because we have performed multiple observations in each patient, with potential interdependency. In a disease that affects multiple bowel segments, however, the per-segment analysis allowed us to consider several different parameters.

Some parameters were classified as "morphologic" (ie, lesion site and length and presence of strictures, fistulas, and other complications) and compared with endoscopic and radiologic results. Others were related to disease activity and classified as "activity-related" parameters and compared with clinical-biochemical data.

In the detection and localization of Crohn disease in both the small and the large bowel, accuracy of T2-weighted images was high, ranging from 93% to 95% from the jejunum to the rectum; this was comparable with the accuracy of T1-weighted gadolinium-enhanced MR imaging.

In the assessment of disease length, no significant difference was found between T2- and T1-weighted MR sequences and the reference standard.

In the diagnosis of strictures, T2-weighted MR sequences showed higher sensitivity and accuracy than did T1-weighted MR sequences (sensitivity, 83% vs 66%; accuracy, 91% vs 81%). This can be explained by the poor wall enhancement that is frequently observed in patients with fibrostenosing disease and can produce an unclear bowel profile on coronal T1-weighted contrast material–enhanced images. Conversely, if intestinal contrast material filling is adequate, coronal T2-weighted MR images always offer an excellent anatomic display in patients with either inflammatory or fibrostenosing disease (Fig 2a).

Regarding the diagnosis of enteroenteric fistulas, no differences were found between T1- and T2-weighted sequences (89% vs 91% respectively), although their association moderately increased the overall detection rate from between 66% and 71% to 75%. The diagnosis of fistulas remains one of the major limitations of MR imaging in the assessment of Crohn disease, in part because it is difficult to obtain direct evidence of the fistulous enteroenteric tract; however, several indirect signs, such as marked adhesions of different bowel loops or marked and sharp angulations and convergence of several loops toward a central point (Figs 3a, 3b), indicate the presence of fistulas. In our experience, approximately 25% of fistulas were missed when compared with findings of barium enema studies. However, complex nonenteroenteric fistulas, such as enterourinary fistulas or fistulas into retroperitoneal structures (ie, in the psoas muscle), were easily diagnosed with MR imaging but underestimated with barium studies. Such complex fistulas, more so than enteroenteric fistulas, represent severe complications of Crohn disease and usually require surgical treatment. Moreover, MR imaging showed high sensitivity in the detection of enteroenteric adhesions, which are widely considered to be precursors of fistula lesions.

Other severe complications that require surgery, such as abscesses or phlegmons, were found in 20% of patients, and all complications were assessed correctly either on T1- or T2-weighted images. These results confirm the clinical value of MR imaging, which could potentially replace CT in the diagnosis of all severe complications of Crohn disease. Thus, in our experience, MR imaging was used to correctly assess most of the main morphologic abnormalities of Crohn disease, with the performance of T2-weighted imaging being slightly better.

Regarding MR imaging parameters related to local inflammation, both T1- and T2-weighted imaging parameters were correlated with biologic signs of inflammation or biologic activity (P < .001), whereas a lower correlation (P = .02) was found with the CDAI. When active intestinal inflammation develops in patients with Crohn disease, large amounts of cytokines and other proinflammatory mediators are produced. This induces an increased serum concentration of acute phase reactants (or biologic activity) that is in correlation to the severity of intestinal lesions (1,5,27). On the other hand, the CDAI has a lower specificity since it is based on subjective symptoms, such as abdominal pain and severity of diarrhea (29,30). Presently, to our knowledge, no absolute clinical criteria are available to define and quantify inflammatory activity of Crohn disease lesions.

A significant correlation between T2-weighted wall hyperintensity, gadolinium-enhanced bowel wall enhancement, and biologic activity has been demonstrated in previous studies (10). Our study results confirm these findings and show an intercorrelation between T2-weighted wall signal intensity and gadolinium enhancement at the level of the affected bowel (r = 0.919).

However, despite such a strong correlation between the T2-weighted wall signal intensity and T1-weighted wall enhancement obtained after gadolinium-based contrast material intravenous injection, some intrinsic differences should be noted. The increased gadolinium enhancement observed at the level of the inflamed wall is, in fact, likely related to wall hypervascularity and/or increased vascular permeability, whereas the T2-weighted wall hyperintensity is determined on the basis of an increased amount of edema and fluid components within the inflamed wall. Hypervascularity and edema represent different features of inflammation, and they frequently, but not necessarily, overlap.

The T2-weighted hyperintensity of the mesenteric fat tissue, which was frequently observed on fat-suppressed images outside the affected bowel wall, is another characteristic finding of active Crohn disease. It is an expression of the typical Crohn disease transmural and extramural inflammatory processes and likely related to mesenteric edema or minimal amounts of perivisceral free fluid, which cannot be detected on gadolinium-enhanced images (Fig 1b, 1c).

Therefore, T2-weighted fat-suppressed images offer additional information on mural and transmural Crohn disease inflammation. These images are either complementary or dissimilar to gadolinium-enhanced images.

An intrinsic limitation of T2-weighted fat-suppressed images is the poor anatomic detail (Figs 1b, 2e), which is due to the diffuse low signal intensity of suppressed images. For this reason, these images should always be acquired in association with and related to T2-weighted unsuppressed images.

Other limitations of this study included the relatively small sample size and, above all, the heterogeneity of tests used as reference standards. Such heterogeneity is, however, necessarily related to the complexity of Crohn disease. Complete examination of patients with Crohn disease requires the association of several different imaging, clinical, and instrumental examinations. The disease, in fact, discontinuously affects the small and large bowel, thus requiring both endoscopic and radiologic examinations to diagnose lesion site and extent. At the same time, it produces transmural inflammation and complications that are undetectable at endoscopy or conventional radiography but can be detected easily with cross-sectional imaging. Moreover, to our knowledge, a reference examination to assess disease activity does not exist, although laboratory and clinical tests are widely used for this purpose.

Results of our study differ from those of previous studies (11,12), where T2-weighted sequences showed a lower accuracy than gadolinium-enhanced sequences, both in the depiction of pathologic segments (sensitivity, 51% vs 85%) and in the evaluation of disease severity (sensitivity, 43% vs 93%). A