Dynamic contrast-enhanced magnetic resonance imaging and diffusion-weighted imaging in the activity staging of terminal ileum Crohn's disease

Abstract

Background: The activity staging of Crohn's disease (CD) in the terminal ileum is critical in developing an accurate clinical treatment plan. The activity of terminal ileum CD is associated with the microcirculation of involved bowel walls. Dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) and diffusion-weighted imaging (DWI) can reflect perfusion and permeability of bowel walls by providing microcirculation information. As such, we hypothesize that DCE-MRI and DWI parameters can assess terminal ileum CD, thereby providing an opportunity to stage CD activity.

Aim: To evaluate the value of DCE-MRI and DWI in assessing activity of terminal ileum CD.

Methods: Forty-eight patients with CD who underwent DCE-MRI and DWI were enrolled. The patients' activity was graded as remission, mild and moderate-severe. The transfer constant (K^trans), wash-out constant (K_ep), and extravascular extracellular volume fraction (V_e) were calculated from DCE-MRI and the apparent diffusion coefficient (ADC) was obtained from DWI. Magnetic Resonance Index of Activity (MaRIA) was calculated from magnetic resonance enterography. Differences in these quantitative parameters were compared between normal ileal loop (NIL) and inflamed terminal ileum (ITI) and among different activity grades. The correlations between these parameters, MaRIA, the Crohn's Disease Activity Index (CDAI), and Crohn's Disease Endoscopic Index of Severity (CDEIS) were examined. Receiver operating characteristic curve analyses were used to determine the diagnostic performance of these parameters in differentiating between CD activity levels.

Results: Higher K^trans (0.07 ± 0.04 vs 0.01 ± 0.01), K_ep (0.24 ± 0.11 vs 0.15 ± 0.05) and V_e (0.27 ± 0.07 vs 0.08 ± 0.03), but lower ADC (1.41 ± 0.26 vs 2.41 ± 0.30) values were found in ITI than in NIL (all P < 0.001). The K^trans, K_ep, V_e and MaRIA increased with disease activity, whereas the ADC decreased (all P < 0.001). The K^trans, K_ep, V_e and MaRIA showed positive correlations with the CDAI (r = 0.866 for K^trans, 0.870 for K_ep, 0.858 for V_e, 0.890 for MaRIA, all P < 0.001) and CDEIS (r = 0.563 for K^trans, 0.567 for K_ep, 0.571 for V_e, 0.842 for MaRIA, all P < 0.001), while the ADC showed negative correlations with the CDAI (r = -0.857, P < 0.001) and CDEIS (r = -0.536, P < 0.001). The areas under the curve (AUC) for the K^trans, K_ep, V_e, ADC and MaRIA values ranged from 0.68 to 0.91 for differentiating inactive CD (CD remission) from active CD (mild to severe CD). The AUC when combining the K^trans, K_ep and V_e was 0.80, while combining DCE-MRI parameters and ADC values yielded the highest AUC of 0.95.

Conclusion: DCE-MRI and DWI parameters all serve as measures to stage CD activity. When they are combined, the assessment performance is improved and better than MaRIA.

Keywords: Crohn’s disease; Diffusion-weighted imaging; Ileum; Magnetic resonance imaging; Perfusion imaging.

Figure 1

A 41-year-old male with moderate active Crohn’s disease in the terminal ileum and a Crohn’s Disease Activity Index of 267 and Crohn’s Disease Endoscopic Index of Severity of 12. A: Terminal ileum demonstrates wall thickening and increased signal on axial T2-weighted image; B: Terminal ileum wall has a high signal. Axial diffusion-weighted imaging image (b = 800 s/mm²) demonstrates high signal (arrow) in the same bowel segment. Region of interest (ROI) for the inflammatory bowel wall shows that apparent diffusion coefficient = 1.11×10^-3 mm²/s; C: ROI for the inflammatory bowel wall shows that K^trans = 0.10 min^-1 (K_ep = 0.87 min^-1, V_e = 0.11); D: In contrast, ROI of the normal appearing ileal loop shows that K^trans = 0.01 min^-1 (K_ep = 0.80 min^-1, V_e = 0.02); E: The contrast concentration curve of inflammatory bowel is plotted as ROI (line with circle) and fitted with the model (line); F: The contrast concentration curve of normal loop is plotted as ROI (line with circle) and fitted with the model (line). ROI: Region of interest.

Figure 2

A 42-year-old male with remission of Crohn’s disease in the terminal ileum and a Crohn’s Disease Activity Index of 108 and Crohn’s Disease Endoscopic Index of Severity of 2. A: Axial T2-weighted image shows mural thickening and hyperintensity in the terminal ileum (arrow); B: Axial diffusion-weighted imaging image (b = 800 s/mm²) demonstrates high signal (arrow) in the same bowel segment. Regions of interest (ROI) for the inflammatory bowel wall shows that apparent diffusion coefficient = 1.89×10^-3 mm²/s; C: K^trans map is obtained through the relevant phase. The perfusion parameters of the ROI placed in the terminal ileum is calculated by TCM (K^trans = 0.18 min^-1); D: K_ep map is obtained through the relevant phase. The K_ep of the ROI placed is 0.98 min^-1; E: V_e map is obtained through the relevant phase. The V_e of the ROI placed is 0.19; F: The contrast concentration curve is plotted as ROI (line with circle) and fitted with the model (line). ROI: Region of interest.

Figure 3

The K^trans, K_ep, V_e and apparent diffusion coefficient among the three groups. A: Bar charts show increasing K^trans, between the normal ileal loop (NIL) and the inflamed terminal ileum (ITI) and pairwise comparisons of them is different (all P < 0.001); B: K_ep between the NIL and the ITI is different (all P < 0.001); C: V_e between the NIL and the ITI is different (all P < 0.001); D: Apparent diffusion coefficient between the NIL and the ITI is different (all P < 0.001). Furthermore, increasing K^trans, K_ep and V_e are shown with activity of CD in remission, mild and moderate-severe CD while decreasing apparent diffusion coefficients are shown (all P < 0.001). ^aP indicate difference with P < 0.001. NIL: Normal ileal loop; ITI: Inflamed terminal ileum.

Figure 4

Correlations of inflamed terminal ileum with Crohn’s Disease Activity Index and Crohn’s Disease Endoscopic Index of Severity in Crohn’s disease. A and C: Scatterplots show positive correlation of K^trans, K_ep and V_e and negative correlation of apparent diffusion coefficient in inflamed terminal ileum of Crohn’s disease patients with Crohn’s Disease Activity Index score; B and D: Positive correlation of K^trans, K_ep and V_e and negative correlation of apparent diffusion coefficient in inflamed terminal ileum of Crohn’s disease patients with Crohn’s Disease Endoscopic Index of Severity score. CDAI: Crohn’s Disease Activity Index; CDEIS: Crohn’s Disease Endoscopic Index of Severity; ADC: Apparent diffusion coefficient.

Figure 5

Receiver operating characteristic curve analysis. Receiver operating characteristic curve analysis shows high accuracy of K^trans (areas under the curve [AUC] = 0.76), V_e (AUC = 0.78), K_ep (AUC = 0.68), apparent diffusion coefficient (AUC = 0.89) and Magnetic Resonance Index of Activity (AUC = 0.91) for differentiating inactive from active Crohn’s disease. Accuracy of combining the K^trans, K_ep and V_e (AUC = 0.80) is higher than the individual dynamic contrast-enhanced magnetic resonance imaging parameters. The highest AUC is observed when combining dynamic contrast-enhanced magnetic resonance imaging and diffusion-weighted imaging parameters (AUC = 0.95). ROC: Receiver operating characteristic; ADC: Apparent diffusion coefficient; DCE-MRI: Dynamic contrast-enhanced magnetic resonance imaging; MaRIA: Magnetic Resonance Index of Activity.

Figure 6

Bland-Altman analysis for the intraclass and interclass coefficients. A: Bland-Altman analysis of the difference between the two observers’ average results for K^trans; B: Bland-Altman analysis of the difference between the two observers’ average results for apparent diffusion coefficient; C: Bland-Altman analysis of the difference between the two observers’ average results for K_ep. ADC: Apparent diffusion coefficient; SD: Standard deviation.