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Keywords:

  • Crohn's disease;
  • MRI;
  • pathology;
  • inflammation

Abstract

  1. Top of page
  2. Abstract
  3. PATIENTS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

Background:

The aim was to evaluate the value of magnetic resonance imaging (MRI) findings in Crohn's disease (CD) in correlation with pathological inflammatory score using surgical pathology analysis as a reference method.

Methods:

CD patients who were to undergo bowel resection surgery underwent MR enterography before surgery. The CD pathological inflammatory score of the surgical specimens was classified into three grades: mild or nonactive CD, moderately active CD, and severely active CD; fibrosis was also classified into three grades: mild, moderate, and severe. Mural and extramural MRI findings were correlated with pathological inflammatory and fibrosis grades.

Results:

Fifty-three consecutive patients were included retrospectively. The mean delay between MRI and surgery was 24 days (range 1–90, median 14). The CD pathological inflammatory score was graded as follows: grade 0 (11 patients, 21%), grade 1 (15 patients, 28%), and grade 2 (27 patients, 51%). MRI findings significantly associated with pathological inflammatory grading were wall thickness (P < 0.0001), degree of wall enhancement on delayed phase (P < 0.0001), pattern of enhancement on both parenchymatous (P = 0.02), and delayed phase, (P = 0.008), T2 relative hypersignal wall (P < 0.0001), blurred wall enhancement (P = 0.018), comb sign (P = 0.004), fistula (P < 0.0001), and abscess (P = 0.049). The inflammation score correlated with the fibrosis score (r = 0.63, P = 0.0001).

Conclusions:

Our study identified MRI findings significantly associated with surgical pathological inflammation. These lesions are considered potentially reversible and may be efficiently treated medically. We also showed that fibrosis was closely and positively related to inflammation. Inflamm Bowel Dis 2011

Crohn's disease (CD) is a chronic inflammatory bowel disorder characterized by remittent and relapsing episodes.1 Assessment of inflammatory activity is crucial to decide optimal treatment: patients with severe inflammatory lesions receive medical therapy, while patients without or with moderate inflammatory lesions associated with obstructive symptoms undergo surgery.2, 3

Numerous criteria are used to assess disease activity including clinical symptoms, physical findings, laboratory parameters, and endoscopic results.4 However, clinical and biological criteria must be supported by results of other diagnostic techniques because these scores are unreliable4, 5; moreover, clinical activity seems to be independent of the severity of mucosal lesions and biological activity.5, 6

Conventional and/or wireless capsule endoscopies only provide information about the intestinal mucosa, while conventional small bowel contrast studies only provide indirect information about the intestinal wall. These limitations are important because inflammation in CD is commonly transmural.1, 7

New imaging tools such as computed tomography (CT) and magnetic resonance imaging (MRI) provide information about the mucosa, the intestinal wall, and adjacent structure abnormalities, including complications such as fistula or abscesses.8, 9

The accuracy of CT enteroclysis seems to be good for evaluating CD. Chiorean et al10 correlated CT findings with surgical pathology to assess the accuracy of CT enteroclysis in differentiating inflammatory from fibrostenotic lesions. A scoring system was defined to reliably differentiate these lesions. However, because of the radiation doses of CT scan and the increased risk of radiation-induced cancers,11, 12 especially in young people, reliable nonradiation diagnostic techniques must be developed to follow these patients who require regular evaluations.13

Because of its excellent soft-tissue contrast, multiplanar images, the absence of exposure to radiation, safe contrast agents, and ability to show mural and extramural abnormalities,14 MRI is becoming the standard imaging technique for CD.3 Several studies have shown that MRI plays a role in the assessment of CD activity, using different variables.9, 15–17 These variables have only been correlated with clinical and biological scores (e.g., the Crohn's Disease Activity Index [CDAI]) or with endoscopic findings, which all have certain limits because CD is a mural and transmural disease.

To our knowledge, only one study has compared MRI findings with the pathological analysis of surgical specimens, but with a small number of patients.18 The aim of our study was to determine the diagnostic value of MRI findings in CD in correlation with inflammatory activity with surgical pathological analysis as a reference method.

PATIENTS AND METHODS

  1. Top of page
  2. Abstract
  3. PATIENTS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

Patients

Eligibility criteria for this retrospective monocentric cohort study in Beaujon Hospital (Clichy, France) were: consecutive adult patients with documented CD who were to undergo bowel resection for small bowel CD; small bowel MRI within 3 months prior to surgery; and stable medical treatment from MRI until surgery. All consecutive patients seen from June 2006 to February 2009 were included.

Surgical treatment of patients was decided during our weekly medical and surgical rounds, where all patients potentially requiring surgery for CD are discussed. Moreover, our policy has been to systematically perform MRI before any surgical procedure in CD patients.

Patients receiving tumor necrosis factor antibody (anti-TNF) treatment within 2 months before MRI or between MRI and surgery were excluded because this treatment can induce mucosal healing in CD.19

The following information was collected for all patients: gender, age at surgery, duration of disease at surgery, disease activity at surgery estimated by the Harvey–Bradshaw index (HBI),20 and biological parameters (C-reactive protein [CRP], leukocyte count), surgical indication, previous bowel surgeries, and type of surgery. The study was approved by our Institutional Review Board.

Methods

MRI Technique

After oral administration of 1000 mL of hyperosmotic water solution (mannitol 5%), MRI was performed with a 1.5 T system (Intera, Philips Medical Systems, Best, The Netherlands) using a body coil. Breath-hold imaging was first performed in the coronal plane using a T2-weighted single shot turbo spin echo sequence with fat suppression (TR/TE 20,364/100, matrix 243 × 512, turbo factor 71, slice thickness 5 mm, 25 slices per image set, 20-second breath-hold duration), and in the coronal and axial planes using a true Fast Imaging with Balanced Steady-state (true FISP) sequence (TR/TE 3/1.5, matrix 256 × 256, flip 60°, slice thickness 5–8 mm, 25–40 slices per image set, 21-second breath-hold duration). After intravenous administration of 1 mg of glucagon (GlucaGen, Novo Nordisk, Bagsvaerd, Denmark), a 3D FLASH T1-weighted sequence was performed before and 90 seconds (coronal plane) and 8 minutes (axial and coronal plane) after an intravenous injection of gadolinium chelates (Dotarem, Guerbet, France) at a dose of 0.2 mL/kg of body weight, with fat suppression (TR/TE 3.7/1.3, matrix 269 × 236, flip 10°, slice thickness 8 mm, 40 slices, 20-second breath-hold duration). Ninety seconds was considered the parenchymatous time and 8 minutes the delayed time.16

MRI Data Analysis

All MRI studies were reviewed by two experienced radiologists (M.Z., V.V.), who were unaware of clinical, surgical, or laboratory data for the patients, and a consensus was reached.

The following imaging findings were evaluated:

  • Degree of wall enhancement on both parenchymatous (90 seconds) and delayed (8 minutes) T1-weighted images, scored as moderate or marked, compared with enhancement of adjacent normal bowel.16

  • Pattern of enhancement: homogeneous or layered (i.e., visualization of two or three layers of the bowel wall) on parenchymatous and on delayed T1-weighted images.5

  • Well-defined or blurred wall enhancement on delayed T1-weighted images.

  • Wall signal intensity on T2-weighted images,17 evaluated as mild or high.

  • Wall thickness in both T2 (true FISP) and T1-weighted images.

  • The presence of upstream intestinal loop dilatation (at least 1.5 × normal loop).

  • Extramural findings: the presence or absence of fatty proliferation (i.e., space-occupying lesion, separating and/or displacing adjacent small bowel loops),16 comb sign (i.e., segmental dilatation or engorgement of the vasa recta),10 lymph nodes (i.e., presence of any lymph nodes in the mesentery), fistula, and/or abscesses.

The length and location of abnormal segments were also recorded.

Pathological Analysis

All surgical small-bowel specimens showed CD lesions and were analyzed prospectively by macroscopic examination of unfixed specimens and microscopic examination after fixation with formalin and standard hematoxylin-eosin safran stain. One expert gastrointestinal pathologist (D.C.H.) who was unaware of the clinical, biological, and radiological findings examined all specimens and stained histological sections. Two main features were evaluated during the macroscopic examination: total length (centimeters) of the resected specimens and the presence of significant luminal strictures; the specimen was then carefully examined to identify any fistula or abscesses as described by Borley et al.21 The thickness of the intestinal wall was measured in millimeters on whole-mount slides of transverse sections of the most severely involved intestinal segment.

At least 10 samples (blocks) were prepared for each surgical specimen to include all lesions observed macroscopically (strictures, ulcerations, fissures, and fistula) and make sure that there was a representative evaluation of all pathological changes. The most severe abnormalities observed microscopically were selected to score inflammation and fibrosis.

The CD pathological inflammatory score routinely used at Beaujon's university hospital was graded into three categories (grades 0-1-2) as follows: grade 0 (mild or nonactive CD): minimal neutrophil infiltrate limited to mucosae; grade 1 (moderately active CD): neutrophil infiltrate limited to the mucosa and submucosa without muscular involvement; grade 2 (severely active CD): transmural neutrophil infiltrate through the muscularis propria and/or fistula and/or abscesses in the subserosa (Fig. 1A–C).

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Figure 1. Whole-mount slides from transversal sections of affected small bowels illustrating inflammatory grades (hematoxylin-eosin safran stain). (A) Grade 0: no active inflammation was observed (no neutrophil infiltrate); marked transmural fibrosis with obliteration of normal layers causing severe stricture. (B) Grade 1: neutrophil infiltrate limited to the mucosa and submucosa creating fissures, without alteration of the muscularis. (C) Grade 2: massive neutrophil infiltrate and with transmural penetration creating fistula and abscesses into the serosa and the extramural fat.

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We also graded inflammation in all patients using the score described by Chiorean et al,10 which includes both acute and chronic inflammation.

Fibrosis was then graded into three categories (grade 0-1-2) as follows: grade 0: minimal fibrosis limited to submucosa; grade 1: massive submucosal fibrosis with preserved layers; grade 2: massive transmural fibrosis with effacement of normal layers. We were unable to use Chiorean et al's fibrosis score because of difficulties to grade some items such as mild versus severe strictures or level of muscular hyperplasia.

Statistical Analysis

Surgical pathology was the reference method for assessing the accuracy of MRI for the diagnosis of CD inflammation and fibrosis.

The correlations between the two inflammation scores (CD pathological inflammatory score and the one used by Chiorean et al10) and between CD pathological inflammatory score and fibrosis score (as defined by the scoring system above), were estimated using the Mantel–Haenszel χ2, Spearman rank correlation coefficient.

The CD pathological inflammatory score was correlated with thickness of the bowel wall. Sensitivity and specificity were calculated for different wall thicknesses to differentiate inflammation grade 0 patients and upper grades, and grade 2 patients and lower grades. Sensitivity, specificity, and accuracy were calculated for the detection of fistula and/or abscesses by MRI and pathology.

The CD pathological inflammatory score was correlated with MRI variables for mural findings (degree of enhancement in parenchymatous phase and delayed phase, pattern of enhancement in parenchymatous phase and delayed phase, T2 wall hypersignal, blurred wall enhancement, upstream dilatation, wall thickness) and extramural findings (Comb sign, fistula and abscesses, lymph nodes, fatty proliferation) using the χ2 Fisher exact test and Kruskal–Wallis test.

The sign-by-sign correlation between MRI and pathological variables was performed for wall thickness, length of affected segments, and presence of fistula and/or abscesses using χ2 Fisher exact test, Spearman rank correlation coefficient, and Kruskal–Wallis test.

The CD pathological inflammatory score was correlated with the HBI, CRP, and white cell count using Kruskal–Wallis test. No specific hypothesis was performed for missing data.

RESULTS

  1. Top of page
  2. Abstract
  3. PATIENTS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

Demographic and Clinical Data

Fifty-three patients were included. The demographic and clinical features are presented in Table 1. Eleven patients who had received anti-TNF treatment within 2 months before surgery were excluded. Fourteen patients who had previously been treated with an anti-TNF but the last infusion was administered more than 2 months before surgery were included. The mean delay between small bowel MRI and surgery was 24 days (range 1–90, median 14). MRI was not performed or was performed more than 3 months before surgery in 9 and 11 patients, respectively, who were excluded. Figure 2 shows a flowchart of patients.3

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Figure 2. Flowchart of patient inclusion in the study.

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thumbnail image

Figure 3. MRI findings: delayed T1-weighted images illustrating CD inflammatory grades. (A) Grade 0: coronal image in a 24-year-old male; the pathological wall is 5 mm thick, with mild and homogeneous enhancement; there is no comb sign. (B) Grade 1: coronal image in a 59-year-old female; the pathological wall is 9 mm thick, with marked and layered enhancement. Note the presence of fatty proliferation with displaced adjacent loops. (C) Grade 2: axial image in a 20-year-old female; the pathological wall is 11 mm thick, with marked, homogeneous, and blurred enhancement. Note the presence of a cutaneous fistula.

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Table 1. Demographic Characteristics of 53 Patients Operated on for Small Bowel Crohn's Disease
FactorNumber of Patients (%)
  1. a

    More than 1 cigarette/day.

AgeMean yrs35 (15–74)
SexMen28 (53%)
Women25 (47%)
Duration of diseaseMean yrs10 (0–34)
Location of disease at entrySmall bowel6 (11%)
Ileocolonic47 (89%)
Disease behavior for small bowel according to Montreal classificationB1 inflammatory6 (11%)
B2 stenotic32 (61%)
B3 penetrating15 (28%)
Pharmacotherapy at the time of surgeryNo treatment18 (34%)
Steroids6 (11%)
Immunosuppressant11 (21%)
 Steroids and immunosuppressant4 (8 %)
History of surgery before inclusionSegmental small bowel resection7 (13%)
Ileocecal resection17 (32%)
Colonic resection6 (11%)
Smoking historyNever26 (49%)
Current*a10 (19%)
Previous17 (32%)

Indications for surgery in our 53 patients were bowel obstruction in 23 (43%) patients, refractory nonobstructive disease in three (6%), and perforating disease (refractory fistula or abscess) in 15 (28%); 12 (23%) patients had more than one indication for surgery.

Evaluation of clinical activity by the HBI was assessed in 49 patients and showed that 40 (82%) patients had active disease (HBI ≥4) and 9 (18%) had mild or nonactive disease. Disease activity could not be assessed in four patients because of the presence of stoma. The inflammatory syndrome was evaluated by the level of CRP (available at the time of MRI in 39 (74%) patients) and the white cell count in all patients. The association between these parameters and CD pathological inflammatory score is summarized in Table 2.

Table 2. Association Between CD Pathological Inflammatory Score in Surgical Specimens, Clinical Crohn's Disease Activity (HBI), and Biologic Inflammation in 53 Patients Operated on for Crohn's Disease (CD)
CD Pathological Inflammatory Score*Harvey-Bradshaw Index (n = 49) Mean ± SE (n)C-reactive Protein mg/L (n = 39) Mean ± SE (n)White Cell Count G/L (n = 53) Mean ± SE (n)
  • *

    Grade 0: mild or nonactive CD; grade 1: moderately active CD; grade 2: severely active CD.

Grade 05.8 ± 2.3 (9)4.2 ± 3.2 (9)7.6 ± 3.9 (11)
Grade 17.1 ± 3.3 (5)12.0 ± 16.1 (8)8 ± 4.8(15)
Grade 26.3 ± 2.9 (25)39.5 ± 48.0 (22)10 ± 4.3 (27)
P0.710.00140.051

Pathological Features

All intestinal resection specimens showed the fibro-inflammatory changes of CD with a uniform pattern in samples (blocks) from the same patient. The distribution of the 53 patients into the three grades according to the CD pathological inflammatory score was as follows: grade 0 (11 patients, 21%), grade 1 (15 patients, 28%), and grade 2 (27 patients, 51%). Their distribution into the three grades according to the fibrosis score was as follows: grade 0 (two patients, 4%), grade 1 (15 patients, 28%), and grade 2 (36 patients, 68%). This is summarized in Table 3.

Table 3. Distribution of the 53 Surgical Specimens of Patients Operated on for Crohn's Disease According to the CD Pathological Inflammatory and the Fibrosis Scores
  Fibrosis Scorea
 Grade012Total
  • a

    Grade 0: no or minimal fibrosis limited to submucosa; grade 1: massive submucosal fibrosis with preserved layers; grade 3: massive transmural fibrosis with effacement of normal layers.

  • b

    Grade 0: mild or nonactive CD; grade 1: moderately active CD; grade 2: severely active CD.

CD pathological inflammatory scoreb024511
1011415
2002727
Total2153653

CD pathological inflammatory score was correlated with the fibrosis score (r = 0.63, P = 0.0001) and with the inflammatory score used by Chiorean et al10 (r = 0.80, P = 0.0001).

There was no significant difference in the length of the specimens according to CD pathological inflammatory score; the length was 21.5 ± 25 cm in grade 0 patients, 35.3 ± 40 in grade 1 patients, and 24.8 ± 9.6 cm in grade 2 patients.

Macroscopic examination showed 44/53 (83%) patients with strictures and 25/53 (47%) patients with fistula or abscesses. Among them, 20/25 (80%) had concomitant strictures.

The thickness of the bowel wall on whole-mount slides was strongly correlated with the CD pathological inflammatory score (6.7 ± 1.4 mm for grade 0, 11.2 ± 3 mm for grade 1, and 17.3 ± 3.8 mm for grade 2, P < 0.0001).

Correlations Between MRI and Pathological Characteristics

The location of abnormal intestinal segments was the same for resected surgical specimens and MRI findings. The mean length of surgical specimens was 271 ± 252 mm, the mean length of involved bowel measured by MRI was 228 ± 164 mm (r = 0.52, P = 0.0002). The mean wall thickness measured by the pathologist on slide sections was 13.4 ± 5.4 mm.

The mean wall thickness measured by MRI was 8.9 ± 2.6 mm and 9.3 ± 2.6 mm on T2- and T1-weighted images, respectively, and was significantly correlated in each patient (r = 0.9, P < 0.0001). The correlation with pathological wall thickness measurements was also significant (r = 0.68, P < 0.0001 for T2 measurements, r = 0.70, P < 0.0001 for T1 measurements). To differentiate patients with grade 0 from others (grade 1 or 2), a threshold of 6 mm had a sensitivity and specificity of 63.6% and 92.9%, and a threshold of 7 mm had a sensitivity and specificity of 90.9% and 78.6%, respectively (on T2 sequences). To differentiate patients with grade 2 from the others (grade 0 or 1), a threshold of 10 mm had a sensitivity and specificity of 55.6% and 84.6%, respectively, and a threshold of 11 mm had a sensitivity and specificity of 40.7% and 92.3%, respectively.

Detection of fistula and/or abscesses by MRI had a sensitivity, specificity, and accuracy of 88%, 93%, and 91%, respectively (P < 0.0001).

Upstream dilatation of intestinal loops on MRI was not significantly associated (P = 0.71) with the pathological finding of stenosis.

Association Between MRI signs, CD Pathological Inflammatory, and Fibrosis Scores

Table 4 shows the results of associations for each imaging sign within the three groups according to CD pathological inflammatory score (Figures 3A-C). When comparing the association between MRI signs and CD pathological inflammatory score or between MRI signs and the inflammatory score described by Chiorean et al, we found three signs significantly associated with our score but not with the one of Chiorean et al: Pattern of enhancement delayed phase (P = 0.008 versus 0.5), blurred wall enhancement (P < 0.001 versus 0.14), and abscess (P = 0.049 versus 0.59).

Table 4. MRI Findings and CD Pathological Inflammatory Score in 53 Surgical Specimens of Patients Operated on for Crohn's Disease
 CD Pathological Inflammatory Score
 Grade 0* (n = 11) % (n)Grade 1* (n = 15) % (n)Grade 2* (n = 27) % (n)P
  • *

    Grade 0: mild or non active CD; grade 1: moderately active CD; grade 2: severely active CD.

Wall thickness (mm; m±SD)    
 T2 sequences6.1 ± 18.4 ± 1.810.3 ± 2.4<0.0001
 T1 sequences6.2 ± 1.39.2 ± 1.810.6 ± 2.2<0.0001
Mural findings    
Degree of enhancement    
 Parenchymatous phase   0.57
   Mild55% (6)33% (5)37% (10) 
  Marked45% (5)67% (10)63% (17) 
 Delayed phase   <0.0001
 emsp;Mild64% (7)47% (7)7% (2) 
   Marked36% (4)53% (8)93% (25) 
Pattern of enhancement    
 Parenchymatous phase   0.02
  Layered36% (4)80% (12)81% (22) 
  Homogeneous64% (7)20% (3)19% (5) 
 Delayed phase   0.008
  Layered18% (2)73% (11)30% (8) 
  Homogeneous82% (9)27 (4)70% (19) 
T2 wall hypersignal0% (0)0% (0)56% (15)<0.0001
Blurred wall enhancement0% (0)0% (0)37% (10)0.018
Upstream dilatation38% (4)47% (7)44% (12)0.87
Extramural findings    
 Comb sign36% (4)67% (10)89% (24)0.004
 Fistula0% (0)13% (2)81% (22)<0.0001
 Abscess0% (0)7% (1)30% (8)0.049
 Lymph nodes36% (4)73% (11)56% (15)0.19
 Fatty proliferation64% (7)47% (7)70% (19)0.48

Table 5 shows the results of associations for each imaging sign within the three groups according to fibrosis score.

Table 5. MRI Findings and Fibrosis Score in 53 Surgical Specimens of Patients Operated on for Crohn's Disease
 Fibrosis Score
 Grade 0* (n = 2) % (n)Grade 1* (n = 15) % (n)Grade 2* (n = 36) % (n)P
  • *

    Grade 0: no or minimal fibrosis limited to submucosa; grade 1: massive submucosal fibrosis with preserved layers; grade 3: massive transmural fibrosis with effacement of normal layers.

Wall thickness (mm; m±SD)    
 T2 sequences5 ± 07.5 ± 1.69.7 ± 2.60.0018
 T1 sequences5 ± 108.3 ± 1.89.9 ± 2.50.0039
Mural findings    
Degree of enhancement    
 Parenchymatous phase   0.33
  Mild0% (0)53% (8)36% (13) 
  Marked100% (2)47% (7)64% (23) 
 Delayed phase   0.15
  Mild50% (1)47% (7)22% (8) 
  Marked50% (1)53% (8)78% (28) 
Pattern of enhancement    
 Parenchymatous phase   0.45
  Layered50%(1)80% (12)69% (25) 
  Homogeneous50% (1)20% (3)31% (11) 
 Delayed phase   0.1
  Layered0% (0)60% (9)33% (12) 
  Homogeneous100% (2)40 (6)67% (24) 
T2 wall hypersignal0% (0)0% (0)42% (15)0.026
Blurred wall enhancement0% (0)0% (0)28% (10)0.062
Upstream dilatation50% (1)40% (6)44% (16)1
Extramural findings    
 Comb sign100% (2)47% (7)81% (29)0.03
 Fistula0% (0)13% (2)61% (22)0.0011
 Abscess0% (0)7% (1)22% (8)0.49
 Lymph nodes100% (2)73% (11)47% (17)0.11
 Fatty proliferation50% (1)53% (8)67% (24)0.68

DISCUSSION

  1. Top of page
  2. Abstract
  3. PATIENTS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

Our study permitted us to identify MRI signs significantly associated with pathological inflammation. The ability to recognize inflammation is of major interest in the management of patients in the clinical setting, as this condition is potentially reversible using medical therapy, and its absence usually leads to surgical therapy. Two analytical methods (MRI and pathological analysis of resected specimens) were selected that evaluate both mural and extramural components. Indeed, histological analysis of intestinal resection is essential to determine CD activity because active lesions are often transmural, enclosing fissures or fistula mixed with edema and neutrophil infiltration if the disease is still active.

Certain mural MRI findings were found to be associated with our CD pathological inflammatory score of the disease. Wall thickness on either T1- or T2-weighted sequences as well as wall thickness on whole-mount slides were shown to be significantly increased with disease activity. Our results show that a threshold of 6 mm can be used to distinguish between patients with inactive disease (grade 0) and active disease (grade 1 or 2) (sensitivity and specificity, 63.6% and 92.9%, respectively). This value agrees with other studies which suggest that a normal bowel wall is between 1 and 3 mm thick, and the minimal value for wall thickness in CD is 4 mm22 or 5 mm.16, 23 Furthermore, a threshold of 11 mm provides a distinction between severe active CD patients (grade 2) and others (grade 0 or 1) (sensitivity and specificity, 40.7% and 92.3%, respectively). Although this measurement may be obtained on T1- or T2-weighted sequences, it was easier on T2 sequences. This finding was found to be significantly associated in most CT or MRI studies.10, 15–17, 24

Bowel wall enhancement has also been extensively investigated in CD patients. However, results from the literature are confusing because various acquisition times, different enhancement patterns (homogeneous, layered, mucosal), and various estimations of the degree of wall enhancement10, 15–17 have been used. Interestingly, all the enhancement criteria evaluated in this study were significantly related to the CD pathological inflammatory score in the different grades, except the degree of wall enhancement at the parenchymatous phase. The most striking finding to differentiate inactive CD (grade 0) from moderately active (grade 1) and severely active (grade 2) CD patients was the degree of wall enhancement on delayed T1-weighted sequences. Therefore, delayed T1-weighted sequences seem to play an important role in assessing disease activity.

As reported by others,17 wall signal intensity in T2-weighted sequences was associated with disease activity in this series. We also found that a blurred enhancement pattern in delayed phase imaging was well correlated with activity grading, and was essentially observed in severely active CD patients. This probably corresponds to transmural inflammation extending to adjacent mesentery fat, described by Colombel et al5 as perienteric inflammation, which correlated well with increased CRP, as in our study.

Certain extramural MRI findings were significantly associated with disease activity: the presence of the comb sign, fistula, and abscesses, findings which were mostly observed in active CD patients. Despite one negative study,16 the comb sign has mostly been reported in active CD patients.10, 15, 17 Diagnosis of abscesses is a major issue in clinical practice because it changes the course and management of the disease and usually requires interventional treatment.17

Conversely, no relationship was found between the presence of lymph nodes or fatty proliferation and disease activity. Chiorean et al and Gourtsoyiannis et al observed a significant number of lymph nodes in active CD patients.10, 15–17, 24 This discrepancy could be explained because we considered all lymph nodes whatever the size, number, or enhancement.

To our knowledge, only two studies compared MRI and surgical pathological findings, including 18 and 17 patients, respectively.18, 25 One of these studies did not mention pathological classification reference and used MRI-determined categories.25

Most of the findings that were significant in our study were also described in the study of Punwani et al.18 Wall thickness, T2 hypersignal, and pattern of enhancement are associated with histologic markers of acute inflammation, whereas degree of enhancement at parenchymatous time (70 seconds for this study) and lymph nodes are not associated.18 Moreover, we think our study brings additional information. We used a pathological score for acute inflammation and fibrosis which was, as in their study, adapted from the classification of Borley et al.21 However, we simplified this score, which makes it easier for daily practice. Our data were qualitative and not quantitative, contrary to their study, as it has been suggested that quantitative measurements are less reliable than visual estimates for identifying active CD.5 Last, we also studied all the findings at a very delayed time (8 minutes), and we have shown that this timing is very important in distinguishing moderately active CD patients (grade 1) from severely active CD patients (grade 2).

Compared with the study which evaluated CT scan imaging and surgical pathological findings,10 our pathological score has the two major advantages of not mixing chronic (lymphoid infiltrates) and acute (neutrophil infiltrates) inflammation and distinguishing perforating and nonperforating phenotypes.

In our study, fibrosis was evaluated and found to be well correlated with inflammation. The relationship between transmural fibrosis and the severity of acute inflammation (deep fissures and fistula) is consistent with previous pathological studies, showing the correlation between fistula formation and strictures with massive mural fibrosis.26, 27 This correlation between acute inflammation and fibrosis is an important and innovative point, suggesting that it may not be relevant to make an exclusive distinction, as is usually done, between inflammatory patients and fibrotic patients. Moreover, we did not find any correlation between the fibrosis score and MRI pattern or degree of enhancement wall.

The present study has certain limitations. First, it is a retrospective study. Second, we deliberately chose oral administration of contrast medium and therefore did not investigate certain mural criteria such as superficial ulcers, fold thickening, and nodularity. As shown previously by Gourtsoyiannis et al,16 MRI enteroclysis provides better results for these subtle abnormalities than MRI without enteroclysis. Nevertheless, although these are early CD findings, the relationship between their presence and disease activity is questionable.16 Moreover, naso-jejunal tube placement is uncomfortable, making movement artifacts more frequent, and it has clearly been shown that small bowel MRI with oral administration is much more acceptable to patients than MRI enteroclysis.28

In conclusion, this study identified several MRI findings that were significantly associated with inflammatory activity in CD using surgical pathological examination as the reference method. Demonstration of the high accuracy of MRI for detecting the presence of inflammatory activity is of significant clinical relevance because of its therapeutic implications as patients with severe inflammatory lesions will receive medical therapy, while those without or with only moderate inflammatory lesions will preferably undergo surgery. Altogether, these results could help us to select patients for medical or surgical therapy and also be used to monitor responses to therapeutic interventions both in the clinical setting and in therapeutic trials.

REFERENCES

  1. Top of page
  2. Abstract
  3. PATIENTS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES