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Computed Tomography and Magnetic Resonance Enterography Findings in Crohn’s Disease: What Does the Clinician Need to Know From the Radiologist?
Canadian Association of Radiologists Journal xx (2013) 1e10 www.carjonline.org
Abdominal Imaging / Imagerie abdominale
Computed Tomography and Magnetic Resonance Enterography Findings in Crohn’s Disease: What Does the Clinician Need to Know From the Radiologist? Carolina Pesce Lamas Constantino, MDa,b,*, Rosana Souza Rodrigues, MD, PhDa,c, Jaime Araujo Oliveira Neto, MDc, Edson Marchiori, MD, PhDa, Antonio Luis Eiras Araujo, MDa,c, Renata de Mello Perez, MD, PhDd, Daniella Braz Parente, MD, PhDa,c a Department of Radiology, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil Department of Abdominal Imaging, Dimagem diagnostico por imagem, Rio de Janeiro, Brazil c Department of Radiology, D’Or Institute for Research and Education, Rio de Janeiro, Brazil d Department of Clinic and Hepatology, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil b
Abstract The purpose of this pictorial essay was to discuss and illustrate computed tomography and magnetic resonance enterography findings in patients with Crohn’s disease. These noninvasive and easily performed methods for the evaluation of Crohn’s disease are useful for differentiating between active and fibrotic bowel disease, and can help to guide treatment (medical vs surgical). Although inflammatory and fibrostenotic findings of Crohn’s disease may overlap, computed tomography and magnetic resonance enterography can help to identify the presence, extent, and severity of active inflammation that may respond to medical therapy, and the existence of fistulas and fibrostenosis that may benefit from surgical management. Resume Cette presentation vise a explorer et illustrer les resultats de l’enterographie par tomodensitometrie et resonance magnetique chez des patients atteints de la maladie de Crohn. Ces modalites d’evaluation de la maladie de Crohn, non effractives et facilement realisables, permettent de differencier le stade actif du stade fibreux de la maladie intestinale inflammatoire et peuvent aider a orienter vers un traitement medical ou chirurgical. Les composantes inflammatoires et fibreuses de la maladie de Crohn ont parfois des apparences comparables. Dans ce contexte, l’enterographie par TDM ou resonance magnetique est utile pour la detection des lesions et l’evaluation de l’etendue et de la gravite durant la phase active, susceptible d’^etre traitee medicalement, ainsi que pour la detection des fistules et des stenoses fibreuses, dont le traitement sera de preference chirurgical. Ó 2013 Canadian Association of Radiologists. All rights reserved. Key Words: Crohn’s; Enterography; Computed tomography; Magnetic resonance; Inflammation; Fibrostenosis
Computed tomography enterography (CTE) and magnetic resonance enterography (MRE) are the main imaging methods used to diagnose, stage, and monitor small bowel Crohn’s disease. These methods are used to evaluate transmural pathologic changes and extraluminal * Address for correspondence: Carolina Pesce Lamas Constantino, MD, Rua Mario Covas Junior, 190, Apto 1301, Barra da Tijuca 22631-030, Rio de Janeiro, Rio de Janeiro, Brazil. E-mail address: [email protected] (C. Pesce Lamas Constantino).
complications [1e3]. Crohn’s disease has a wide spectrum of presentation and is often associated with active inflammation and fibrosis [4e6]. Imaging findings that indicate active inflammation include mural thickening, submucosal oedema, contrast enhancement, prominent vasa recta, mesenteric oedema, and reactive lymphadenopathy. Other findings suggest fibrostenotic disease, such as wall thickening, with hypointense T1 and T2 signal intensity with no or slight inhomogeneous enhancement that becomes more prominent in a delayed phase [1,3,7]. Fistulous tracts and
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Figure 1. A 37-year-old man with fibrostenotic-predominant Crohn’s disease coexisting with active inflammation. Coronal (A) and axial (B) computed tomography enterographic images, showing marked wall thickening associated with mural stratification (A, B, arrows). Note also the significant upstream dilatation (A, arrowhead).
abscess characterize the penetrating form of the disease [1,3,8]. This pictorial essay reviews the CTE and MRE findings of patients with Crohn’s disease by highlighting patterns that
aid in the characterization of active inflammation, fistulas, and fibrostenosis. The proper identification of these patterns will enable the clinician to select the most appropriate treatment (clinical or surgical).
Figure 2. A 33-year-old man with Crohn’s disease. Axial T2 half-Fourier acquisition single-shot turbo spin-echo (HASTE) images without (A) and with (B) fat suppression, showing wall thickening with submucosal oedema characterized by high signal intensity on the T2 image (A, arrow) that persists on the T2 fat-suppressed image (B, arrow). Note also a small mural ulceration (A, B, arrowhead).
Figure 3. A 55-year-old woman with mural fat deposition in long-standing Crohn’s disease. Axial computed tomography enterographic section, showing abnormally low attenuation of the bowel wall, a finding consistent with fat deposition (arrows). Note the mucosal and serosal hyperenhancement (arrowheads), which indicate a pattern of chronic disease with activity.
CT and MRE findings in Crohn’s disease / Canadian Association of Radiologists Journal xx (2013) 1e10
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performed from the diaphragm to the pubic symphysis during the enteric phase, 45 seconds after the beginning of intravenous contrast material injection (100-150 mL) at a rate of 3-4 mL/s. Images are acquired with a section thickness of 2.0-2.5 mm and a reconstruction interval of 1.0-1.5 mm. Multiplanar reformatting helps the characterization of enteric and extraenteric abnormalities [3,9]. MRE
Figure 4. A 65-year-old woman with mural fat deposition in long-standing Crohn’s disease. Axial T2 half-Fourier acquisition single-shot turbo spinecho (HASTE) image (A), showing wall thickening of a small bowel segment with high signal intensity within the submucosa that loses signal intensity on an axial T2 fat-suppressed image (B), consistent with fat deposition (arrows).
Techniques CTE and MRE are performed after the distention of the small bowel with a large volume of neutral contrast agent (1500-2000 mL) given orally 40-60 minutes before the examination [1e3]. Polyethylene glycol electrolyte solution, 3% mannitol, and 0.1% wt/vol low-concentration barium with sorbitol (Volumen; E-Z-EM, Westbury, NY) are available as oral contrast agents. Patients undergoing CTE or MRE are requested to abstain from all food and drink for 4 hours before scanning [9]. CTE Neutral CTE oral contrast allows proper evaluation of small bowel mural enhancement. Single-phase scanning is
The most commonly used MRE enteric contrasts are the biphasic agents, which have low signal intensity on T1-weighted images (T1WI) and high signal intensity on T2-weighted images (T2WI). The low signal intensity of these agents on T1WI improves the contrast between bowel lumen and the inflamed hyperenhancing bowel wall after intravenous contrast material administration. The use of spasmolytics agents, such as hyoscine butylbromide and glucagon, are useful for reducing bowel peristalsis and motion artifacts [1,10]. The MRE protocol includes a combination of axial and coronal T2 half-Fourier acquisition single-shot turbo spinecho (HASTE) (single-shot fast spin-echo [SSFSE]) with and without fat suppression, balanced steady-state free precession (SSFP)(True fast imaging with steady-state precession [TrueFISP]) images, and pree and postecontrast-enhanced gradient-echo T1 3-dimensional sequences. T2 HASTE (SSFSE) sequences best demonstrate focal wall thickening, fold pattern changes, and ulceration but are susceptible to intraluminal motion and are often associated with intraluminal low-signal-intensity artifacts. Balanced SSFP (TrueFISP) images best depict mesenteric adenopathy and prominent vasa recta in active Crohn’s disease (‘‘comb sign’’) but are prone to susceptibility artifacts when air is present within the bowel lumen. Fat suppression may be added for better detection of wall and mesenteric oedema as well as for differentiation of focal submucosal fatty infiltration from oedema. Postcontrast imaging is a very important part of the examination, performed 30, 70, and 90 seconds after gadolinium intravenous injection (2 mL/s) and allows the assessment of bowel wall, nodal, and fistulas enhancement [1,10,11]. MRE and CTE have comparable accuracy in the evaluation of Crohn’s disease [1]. The lack of ionizing radiation is a major advantage of MRE over CTE, especially when considering the young age of patients with Crohn’s disease, who will require multiple examinations during their lifetimes [7,11]. The superior tissue contrast of MRE may also allow differentiation among various pathologic changes in the bowel wall that may show nonspecific low attenuation on CTE images. In addition, MRE uses a safer venous contrast agent. However, CTE has higher temporal and spatial resolution, a shorter imaging time, less variability in examination quality, and easy availability and lower cost [1,3,10,11].
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Figure 5. A 45-year-old woman with fibrostenotic-predominant Crohn’s disease and skip lesions. Axial T2 magnetic resonance (MR) image (A) and axial fat-saturation T1 MR image obtained after contrast injection (B), showing a bowel-wall stricture with low T2 signal intensity (A, B, arrow), transmural homogeneous enhancement (B, black arrowhead), and upstream dilatation (A, white arrowhead). Axial T2 MR image (C) and axial fatsaturation T1 MR postcontrast image (D) of the same patient at another level, showing a bowel-wall stricture (C, D, large arrow) with submucosal oedema (C, thin arrow), stratified enhancement (D, black arrowheads), and upstream dilatation (C, white arrowhead), which favor the diagnosis of active disease.
Imaging Findings Bowel-Wall Abnormalities Bowel-wall thickening Both active inflammatory and fibrostenotic Crohn’s disease usually present with bowel-wall thickening (>3 mm), a finding with high sensitivity and specificity for this disease (83%-91% and 86%-100%, respectively) (Figure 1) [2,8,10,12,13] . Submucosal oedema Submucosal oedema usually represents active inflammatory Crohn’s disease and manifests as nonspecific low attenuation on CTE images and high T2 signal intensity on MRE images. Oedema is more conspicuous on fatsuppressed images (Figure 2) [3,4,8,12]. Fat wall infiltration (fat halo sign) The presence of submucosal fat deposition in the bowel wall is a sign of chronic Crohn’s disease. On CTE images,
such infiltration appears as very low attenuation (fat density) (Figure 3). On MRE, it is seen as high T2 signal intensity on nonefat-suppressed images that loses signal intensity on fatsuppressed images (Figure 4) [3,8,14]. Fibrosis Fibrotic wall thickening appears as nonspecific low attenuation on CTE images and has low T1 and T2 signal intensity on MRE images. Both imaging methods show no enhancement or slight progressive enhancement that becomes more prominent in a very delayed phase (8 minutes) (Figure 5) [3,7,8,15]. Patients who present with this feature in addition to clinically significant stenosis are candidates for surgical intervention [16]. Contrast enhancement Mural enhancement is the most-sensitive indicator of active Crohn’s disease [1e3]. Three different enhancement patterns have been described in Crohn’s disease: homogeneous, layered (stratified), and mucosal enhancement. The homogeneous pattern is characterized by
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Figure 7. A 36-year-old woman with skip lesions in Crohn’s disease. Axial computed tomography enterographic section, demonstrating 2 inflammatory small bowel loops (arrows) separated by a normal segment, which is a characteristic finding of Crohn’s disease.
appearance in cross-sectional imaging. In the mucosal pattern, enhancement of the innermost layer of the bowel wall is observed (Figure 6). In Crohn’s disease, all contrast-enhancement patterns are associated with active inflammation when compared with histopathologic findings and may be associated with fibrotic changes. Patients with fibrotic changes in the bowel wall often have coexistent active inflammation [4e7,13]. Although stratified enhancement has been reported to show a higher correlation with active inflammation than other enhancement patterns [6,8], the clinical significance of each enhancement pattern has not been well established in the literature [13]. The absence of enhancement is useful for the exclusion of disease activity [15]. Skip Lesions Patients with Crohn’s disease frequently have multiple involved small bowel segments separated by healthy bowel, which are referred to as skip lesions (Figure 7) [1,3,10,14].
Figure 6. Three enhancement patterns in Crohn’s disease. Axial fatsaturation T1 magnetic resonance images obtained after contrast injection, demonstrating (A) homogeneous enhancement of the entire wall thickness (arrow), (B) layered (stratified) enhancement, characterized by mucosal (arrowhead) and serosal (arrow) enhancement, and (C) mucosal enhancement (arrow).
diffuse enhancement of the entire wall thickness. Stratified enhancement shows mucosal, relatively poor submucosal, and serosal enhancement, which creates a target-like
Figure 8. A 28-year-old man with fibrostenotic-predominant Crohn’s disease and coexisting active inflammation. Axial computed tomography enterographic image, showing a very significant stricture with upstream dilatation (arrowhead) and mucosal hyperenhancement (arrows).
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Figure 9. A 21-year-old woman with Crohn’s disease. A coronal True fast imaging with steady-state precession (TrueFISP) image (A) and a coronal T1 postcontrast image (B), showing wall thickening of the distal ileum (A, white arrowhead) located a few centimetres from an ileocolic anastomosis (black arrowheads), with homogeneous enhancement (B, white arrowhead). Note also the prominent vasa recta characterized by short low-signal-intensity parallel lines on the T2 TrueFISP image (A), oriented perpendicular to the longitudinal axis (A, arrow), and high-signal-intensity parallel lines (B, arrow) due to contrast enhancement of the vasculature (B).
Bowel-Wall Stenosis and Bowel Obstruction
Ulcerations
Bowel-wall stenosis in Crohn’s disease is invariably associated with a segment of thickened bowel wall, whereas adhesive strictures do not demonstrate this finding [10] and can be due to active inflammation (Figure 8). This differentiation is crucial to the choice of therapy. Disease activity can be suggested by oedema, mucosal ulceration, and contrast enhancement. Although this distinction is very important, it is not always clear on imaging studies [16]. When a prestenotic dilatation of >3 cm is present, the disease is probably chronic and clinically significant [4e6].
Moderate and deep ulcerations appear as areas of mural irregularity on postcontrast CTE or MRE, and on T2-weighted images (Figure 11) [1,8,10,14]. The reported sensitivity of MRE for the diagnosis of ulcers is 56%-90% [8,13].
Prominent Vasa Recta (Comb Sign) Prominent vasa recta are caused by increased mesenteric vascularity during active inflammation. The vessels penetrate the bowel wall perpendicular to the affected bowel lumen and are seen as parallel lines that enhance after contrast administration (Figure 9) [1e3,10].
Mesenteric Oedema Mesenteric oedema is seen as increased attenuation of the mesenteric fat on CTE images and high T2 signal intensity on fat-suppressed MRE images, which corresponds to active disease in the bowel wall (Figure 10) [3,7,10].
Figure 10. A 55-year-old man with Crohn’s disease. Axial fat-saturated T2 magnetic resonance enterographic image, showing high signal intensity in mesentery adjacent to the involved ileal segment (arrow). This finding is best observed with fat suppression.
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Figure 11. A 65-year-old woman with Crohn’s disease. A coronal T2 half-Fourier acquisition single-shot turbo spin-echo (HASTE) image (A) and a coronal True fast imaging with steady-state precession [TrueFISP] image (B), showing wall thickening with deep ulceration (A, B, arrow) of the distal ileum. (C) Note the wall ulceration (arrow), and also mucosal hyperenhancement (arrowhead) on a coronal T1 postcontrast image.
Sinuses and Fistulas Sinuses (Figure 12) and fistulas indicate active disease and are seen as high-attenuation lines on CTE images and T2 hyperintense lines that enhance after contrast administration,
Figure 12. A 36-year-old woman with penetrating Crohn’s disease. Coronal volume-rendered computed tomography enterographic section, depicting a sinus tract (arrowhead) that originated from the terminal ileum. Note other signs of active inflammation (wall thickening and mucosal hyperenhancement) in the ileocecal valve and terminal ileum (arrow).
which reflect their higher vascular flow and hyperemia [8]. Complex internal fistulas usually have a stellate appearance, with multiple tracts and bowel loops that radiate from the
Figure 13. A 42-year-old man with fibrostenotic-predominant Crohn’s disease. A complex fistula with transmural inflammation and marked upstream dilatation is evident. A coronal fat-suppressed T1 magnetic resonance image obtained after intravenous contrast administration, showing complex ileoileal (arrow) and ileocolonic (arrowhead) fistulas with diffuse enhancement of the entire wall thickness (transmural inflammation), and marked upstream dilatation.
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Figure 14. A 37-year-old man with an enterovesical fistula in Crohn’s disease. Sagittal (A) and coronal (B) computed tomography enterographic images, depicting an ileovesical fistula (white arrows) with thickening and enhancement of the bladder dome (black arrowheads). A small amount of gas is visible inside the bladder (A, white arrowhead). An ileoileal fistula with bowel-wall thickening and mural hyperenhancement is also visible (B, black arrow).
central portion that are associated with desmoplastic and fibrotic reactions in the surrounding mesentery. Fistulas in Crohn’s disease can be enteroenteric and enterocolonic (Figure 13), enterovesical (Figure 14), enterocutaneous (Figure 15), and perianal [1,4,10]. The reported sensitivity of MRE and CTE for the detection of internal fistulas is 83% and the specificity is 100% [8]. Abscesses Abscesses are seen as hyperintense on T2W MRE imaging, with a corresponding hypodense appearance on CT,
with a capsule that enhances after contrast administration (Figure 16) [1,8,10]. These features are a sign of active disease [4].
Pseudodiverticulum Formation Pseudodiverticulum is the apparent dilatation of the antimesenteric border of the bowel wall. This condition occurs as a consequence of fibrosis of the diseased mesenteric side and is usually associated with other signs of chronic disease (Figure 17) [8,10].
Fibrofatty Proliferation Fibrofatty proliferation occurs as increased mesenteric fat surrounding chronically inflamed bowel loops and is a sign of chronic disease (Figure 18) [1,2,8].
Reactive Lymphadenopathy Reactive lymphadenopathy commonly occurs in association with active inflamed bowel loops [1,5,8].
Pitfalls Figure 15. A 59-year-old man with Crohn’s disease. Axial computed tomography enterographic image, depicting a complex enterocutaneous fistula with a track from the rectum to the skin (arrows) and multiple foci of cutaneous drainage (arrowheads). This patient also had ileocutaneous fistulous tracks (not shown).
Fat wall infiltration, oedema, and fibrosis Abnormalities such as fatty wall infiltration, oedema, and fibrosis appear as nonspecific low attenuation on CTE and are more readily characterized by MRE because of its higher tissue contrast differentiation [3,7,10].
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Figure 16. A 59-year-old man with known Crohn’s disease. Coronal (A) and axial (B) T2 magnetic resonance (MR) images and an axial gadolinium-enhanced fat-saturated T1 MR image (C), showing a small fluid collection with a thick, irregular, and contrast-enhanced wall, within the lower abdomen, in the mesentery adjacent to the cecum and terminal ileum, without communication with the bowel lumen (arrow). These findings are consistent with an abscess.
Inadequate bowel distention Inadequate bowel distention is an important problem that can affect the assessment of wall thickness and enhancement. Nondistended loops can simulate or mask disease [3,10,11,14]. Conclusion CTE and MRE are powerful tools in the management of Crohn’s disease that can demonstrate small bowel mucosal
Figure 17. A 56-year-old man with multiple pseudodiverticula in Crohn’s disease. Coronal computed tomography enterographic image, showing pseudosacculations (arrowheads) produced by asymmetric thickening of the terminal ileal mesenteric border. Also note the prominence of the vasa recta (comb sign, arrows).
and mural inflammation as well as diagnose extraluminal complications. Mural thickening, submucosal oedema, wall enhancement, fat stranding, reactive lymphadenopathy, and engorgement of the vasa recta characterize active disease. Fibrostenotic disease is seen as nonspecific wall hypodensity on CTE and as mural hypointense signaling on T1- and T2-weighted images, with a lack of enhancement or progressive delayed enhancement. Findings that indicate long-standing Crohn’s disease include submucosal fat deposition, pseudodiverticula, fibrofatty proliferation, and fibrotic strictures. CTE and MRE can also help to identify the predominant disease type (active inflammatory or fibrostenotic) and to guide and monitor treatment (medical vs surgical).
Figure 18. A 46-year-old woman with long-standing Crohn’s disease. Axial computed tomography enterographic image, showing fibrofatty proliferation encircling the involved bowel loops (arrows). Note also ileal segments that display wall thickening and mural hyperenhancement, mainly in the mucosa (arrowheads). A complex ileocolonic fistula was also noted in this patient (not shown).
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References [1] Fidler JL, Guimaraes L, Einstein DM. MR imaging of the small bowel. Radiographics 2009;29:1811e25. [2] Huprich JE, Fletcher JG. CT enterography: principles, technique and utility in Crohn’s disease. Eur J Radiol 2009;69:393e7. [3] Elsayes KM, Al-Hawary MM, Jagdish J, et al. CT enterography: principles, trends, and interpretation of findings. Radiographics 2010; 30:1955e70. [4] Zappa M, Stefanescu C, Cazals-Hatem D, et al. Which magnetic resonance imaging findings accurately evaluate inflammation in small bowel Crohn’s disease? A retrospective comparison with surgical pathologic analysis. Inflamm Bowel Dis 2011;17:984e93. [5] Chiorean MV, Sandrasegaran K, Saxena R, et al. Correlation of CT enteroclysis with surgical pathology in Crohn’s disease. Am J Gastroenterol 2007;102:2541e50. [6] Punwani S, Rodriguez-Justo M, Bainbridge A, et al. Mural inflammation in Crohn disease: location-matched histologic validation of MR imaging features. Radiology 2009;252:712e20. [7] Siddiki H, Fidler J. MR imaging of the small bowel in Crohn’s disease. Eur J Radiol 2009;69:409e17. [8] Sinha R, Verma R, Verma S, et al. MR enterography of Crohn disease: part 2, imaging and pathologic findings. AJR Am J Roentgenol 2011; 197:80e5.
[9] Paulsen SR, Huprich JE, Fletcher JG, et al. CT enterography as a diagnostic tool in evaluating small bowel disorders: review of clinical experience with over 700 cases. Radiographics 2006;26:641e57; discussion 57e62. [10] Tolan DJ, Greenhalgh R, Zealley IA, et al. MR enterographic manifestations of small bowel Crohn disease. Radiographics 2010;30: 367e84. [11] Sinha R, Verma R, Verma S, et al. MR enterography of Crohn disease: part 1, rationale, technique, and pitfalls. AJR Am J Roentgenol 2011;197:76e9. [12] Steward MJ, Punwani S, Proctor I, et al. Non-perforating small bowel Crohn’s disease assessed by MRI enterography: derivation and histopathological validation of an MR-based activity index. Eur J Radiol 2012;81:2080e8. [13] Ziech ML, Bipat S, Roelofs JJ, et al. Retrospective comparison of magnetic resonance imaging features and histopathology in Crohn’s disease patients. Eur J Radiol 2011;80:299e305. [14] Lee-Elliott C, Ayer R. Small bowel MRI imaging in the DGH: are you doing it yet? Clin Radiol 2012;67:605e12. [15] Lawrance IC, Welman CJ, Shipman P, et al. Correlation of MRIdetermined small bowel Crohn’s disease categories with medical response and surgical pathology. World J Gastroenterol 2009;15:3367e75. [16] Van Assche G, Dignass A, Panes J, et al. The second European Evidencebased Consensus on the Diagnosis and Management of Crohn’s Disease: definitions and diagnosis. J Crohns Colitis 2010;4:7e27.
Abdominal Imaging / Imagerie abdominale
Computed Tomography and Magnetic Resonance Enterography Findings in Crohn’s Disease: What Does the Clinician Need to Know From the Radiologist? Carolina Pesce Lamas Constantino, MDa,b,*, Rosana Souza Rodrigues, MD, PhDa,c, Jaime Araujo Oliveira Neto, MDc, Edson Marchiori, MD, PhDa, Antonio Luis Eiras Araujo, MDa,c, Renata de Mello Perez, MD, PhDd, Daniella Braz Parente, MD, PhDa,c a Department of Radiology, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil Department of Abdominal Imaging, Dimagem diagnostico por imagem, Rio de Janeiro, Brazil c Department of Radiology, D’Or Institute for Research and Education, Rio de Janeiro, Brazil d Department of Clinic and Hepatology, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil b
Abstract The purpose of this pictorial essay was to discuss and illustrate computed tomography and magnetic resonance enterography findings in patients with Crohn’s disease. These noninvasive and easily performed methods for the evaluation of Crohn’s disease are useful for differentiating between active and fibrotic bowel disease, and can help to guide treatment (medical vs surgical). Although inflammatory and fibrostenotic findings of Crohn’s disease may overlap, computed tomography and magnetic resonance enterography can help to identify the presence, extent, and severity of active inflammation that may respond to medical therapy, and the existence of fistulas and fibrostenosis that may benefit from surgical management. Resume Cette presentation vise a explorer et illustrer les resultats de l’enterographie par tomodensitometrie et resonance magnetique chez des patients atteints de la maladie de Crohn. Ces modalites d’evaluation de la maladie de Crohn, non effractives et facilement realisables, permettent de differencier le stade actif du stade fibreux de la maladie intestinale inflammatoire et peuvent aider a orienter vers un traitement medical ou chirurgical. Les composantes inflammatoires et fibreuses de la maladie de Crohn ont parfois des apparences comparables. Dans ce contexte, l’enterographie par TDM ou resonance magnetique est utile pour la detection des lesions et l’evaluation de l’etendue et de la gravite durant la phase active, susceptible d’^etre traitee medicalement, ainsi que pour la detection des fistules et des stenoses fibreuses, dont le traitement sera de preference chirurgical. Ó 2013 Canadian Association of Radiologists. All rights reserved. Key Words: Crohn’s; Enterography; Computed tomography; Magnetic resonance; Inflammation; Fibrostenosis
Computed tomography enterography (CTE) and magnetic resonance enterography (MRE) are the main imaging methods used to diagnose, stage, and monitor small bowel Crohn’s disease. These methods are used to evaluate transmural pathologic changes and extraluminal * Address for correspondence: Carolina Pesce Lamas Constantino, MD, Rua Mario Covas Junior, 190, Apto 1301, Barra da Tijuca 22631-030, Rio de Janeiro, Rio de Janeiro, Brazil. E-mail address: [email protected] (C. Pesce Lamas Constantino).
complications [1e3]. Crohn’s disease has a wide spectrum of presentation and is often associated with active inflammation and fibrosis [4e6]. Imaging findings that indicate active inflammation include mural thickening, submucosal oedema, contrast enhancement, prominent vasa recta, mesenteric oedema, and reactive lymphadenopathy. Other findings suggest fibrostenotic disease, such as wall thickening, with hypointense T1 and T2 signal intensity with no or slight inhomogeneous enhancement that becomes more prominent in a delayed phase [1,3,7]. Fistulous tracts and
0846-5371/$ - see front matter Ó 2013 Canadian Association of Radiologists. All rights reserved. http://dx.doi.org/10.1016/j.carj.2012.11.004
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C. Pesce Lamas Constantino et al. / Canadian Association of Radiologists Journal xx (2013) 1e10
Figure 1. A 37-year-old man with fibrostenotic-predominant Crohn’s disease coexisting with active inflammation. Coronal (A) and axial (B) computed tomography enterographic images, showing marked wall thickening associated with mural stratification (A, B, arrows). Note also the significant upstream dilatation (A, arrowhead).
abscess characterize the penetrating form of the disease [1,3,8]. This pictorial essay reviews the CTE and MRE findings of patients with Crohn’s disease by highlighting patterns that
aid in the characterization of active inflammation, fistulas, and fibrostenosis. The proper identification of these patterns will enable the clinician to select the most appropriate treatment (clinical or surgical).
Figure 2. A 33-year-old man with Crohn’s disease. Axial T2 half-Fourier acquisition single-shot turbo spin-echo (HASTE) images without (A) and with (B) fat suppression, showing wall thickening with submucosal oedema characterized by high signal intensity on the T2 image (A, arrow) that persists on the T2 fat-suppressed image (B, arrow). Note also a small mural ulceration (A, B, arrowhead).
Figure 3. A 55-year-old woman with mural fat deposition in long-standing Crohn’s disease. Axial computed tomography enterographic section, showing abnormally low attenuation of the bowel wall, a finding consistent with fat deposition (arrows). Note the mucosal and serosal hyperenhancement (arrowheads), which indicate a pattern of chronic disease with activity.
CT and MRE findings in Crohn’s disease / Canadian Association of Radiologists Journal xx (2013) 1e10
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performed from the diaphragm to the pubic symphysis during the enteric phase, 45 seconds after the beginning of intravenous contrast material injection (100-150 mL) at a rate of 3-4 mL/s. Images are acquired with a section thickness of 2.0-2.5 mm and a reconstruction interval of 1.0-1.5 mm. Multiplanar reformatting helps the characterization of enteric and extraenteric abnormalities [3,9]. MRE
Figure 4. A 65-year-old woman with mural fat deposition in long-standing Crohn’s disease. Axial T2 half-Fourier acquisition single-shot turbo spinecho (HASTE) image (A), showing wall thickening of a small bowel segment with high signal intensity within the submucosa that loses signal intensity on an axial T2 fat-suppressed image (B), consistent with fat deposition (arrows).
Techniques CTE and MRE are performed after the distention of the small bowel with a large volume of neutral contrast agent (1500-2000 mL) given orally 40-60 minutes before the examination [1e3]. Polyethylene glycol electrolyte solution, 3% mannitol, and 0.1% wt/vol low-concentration barium with sorbitol (Volumen; E-Z-EM, Westbury, NY) are available as oral contrast agents. Patients undergoing CTE or MRE are requested to abstain from all food and drink for 4 hours before scanning [9]. CTE Neutral CTE oral contrast allows proper evaluation of small bowel mural enhancement. Single-phase scanning is
The most commonly used MRE enteric contrasts are the biphasic agents, which have low signal intensity on T1-weighted images (T1WI) and high signal intensity on T2-weighted images (T2WI). The low signal intensity of these agents on T1WI improves the contrast between bowel lumen and the inflamed hyperenhancing bowel wall after intravenous contrast material administration. The use of spasmolytics agents, such as hyoscine butylbromide and glucagon, are useful for reducing bowel peristalsis and motion artifacts [1,10]. The MRE protocol includes a combination of axial and coronal T2 half-Fourier acquisition single-shot turbo spinecho (HASTE) (single-shot fast spin-echo [SSFSE]) with and without fat suppression, balanced steady-state free precession (SSFP)(True fast imaging with steady-state precession [TrueFISP]) images, and pree and postecontrast-enhanced gradient-echo T1 3-dimensional sequences. T2 HASTE (SSFSE) sequences best demonstrate focal wall thickening, fold pattern changes, and ulceration but are susceptible to intraluminal motion and are often associated with intraluminal low-signal-intensity artifacts. Balanced SSFP (TrueFISP) images best depict mesenteric adenopathy and prominent vasa recta in active Crohn’s disease (‘‘comb sign’’) but are prone to susceptibility artifacts when air is present within the bowel lumen. Fat suppression may be added for better detection of wall and mesenteric oedema as well as for differentiation of focal submucosal fatty infiltration from oedema. Postcontrast imaging is a very important part of the examination, performed 30, 70, and 90 seconds after gadolinium intravenous injection (2 mL/s) and allows the assessment of bowel wall, nodal, and fistulas enhancement [1,10,11]. MRE and CTE have comparable accuracy in the evaluation of Crohn’s disease [1]. The lack of ionizing radiation is a major advantage of MRE over CTE, especially when considering the young age of patients with Crohn’s disease, who will require multiple examinations during their lifetimes [7,11]. The superior tissue contrast of MRE may also allow differentiation among various pathologic changes in the bowel wall that may show nonspecific low attenuation on CTE images. In addition, MRE uses a safer venous contrast agent. However, CTE has higher temporal and spatial resolution, a shorter imaging time, less variability in examination quality, and easy availability and lower cost [1,3,10,11].
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Figure 5. A 45-year-old woman with fibrostenotic-predominant Crohn’s disease and skip lesions. Axial T2 magnetic resonance (MR) image (A) and axial fat-saturation T1 MR image obtained after contrast injection (B), showing a bowel-wall stricture with low T2 signal intensity (A, B, arrow), transmural homogeneous enhancement (B, black arrowhead), and upstream dilatation (A, white arrowhead). Axial T2 MR image (C) and axial fatsaturation T1 MR postcontrast image (D) of the same patient at another level, showing a bowel-wall stricture (C, D, large arrow) with submucosal oedema (C, thin arrow), stratified enhancement (D, black arrowheads), and upstream dilatation (C, white arrowhead), which favor the diagnosis of active disease.
Imaging Findings Bowel-Wall Abnormalities Bowel-wall thickening Both active inflammatory and fibrostenotic Crohn’s disease usually present with bowel-wall thickening (>3 mm), a finding with high sensitivity and specificity for this disease (83%-91% and 86%-100%, respectively) (Figure 1) [2,8,10,12,13] . Submucosal oedema Submucosal oedema usually represents active inflammatory Crohn’s disease and manifests as nonspecific low attenuation on CTE images and high T2 signal intensity on MRE images. Oedema is more conspicuous on fatsuppressed images (Figure 2) [3,4,8,12]. Fat wall infiltration (fat halo sign) The presence of submucosal fat deposition in the bowel wall is a sign of chronic Crohn’s disease. On CTE images,
such infiltration appears as very low attenuation (fat density) (Figure 3). On MRE, it is seen as high T2 signal intensity on nonefat-suppressed images that loses signal intensity on fatsuppressed images (Figure 4) [3,8,14]. Fibrosis Fibrotic wall thickening appears as nonspecific low attenuation on CTE images and has low T1 and T2 signal intensity on MRE images. Both imaging methods show no enhancement or slight progressive enhancement that becomes more prominent in a very delayed phase (8 minutes) (Figure 5) [3,7,8,15]. Patients who present with this feature in addition to clinically significant stenosis are candidates for surgical intervention [16]. Contrast enhancement Mural enhancement is the most-sensitive indicator of active Crohn’s disease [1e3]. Three different enhancement patterns have been described in Crohn’s disease: homogeneous, layered (stratified), and mucosal enhancement. The homogeneous pattern is characterized by
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Figure 7. A 36-year-old woman with skip lesions in Crohn’s disease. Axial computed tomography enterographic section, demonstrating 2 inflammatory small bowel loops (arrows) separated by a normal segment, which is a characteristic finding of Crohn’s disease.
appearance in cross-sectional imaging. In the mucosal pattern, enhancement of the innermost layer of the bowel wall is observed (Figure 6). In Crohn’s disease, all contrast-enhancement patterns are associated with active inflammation when compared with histopathologic findings and may be associated with fibrotic changes. Patients with fibrotic changes in the bowel wall often have coexistent active inflammation [4e7,13]. Although stratified enhancement has been reported to show a higher correlation with active inflammation than other enhancement patterns [6,8], the clinical significance of each enhancement pattern has not been well established in the literature [13]. The absence of enhancement is useful for the exclusion of disease activity [15]. Skip Lesions Patients with Crohn’s disease frequently have multiple involved small bowel segments separated by healthy bowel, which are referred to as skip lesions (Figure 7) [1,3,10,14].
Figure 6. Three enhancement patterns in Crohn’s disease. Axial fatsaturation T1 magnetic resonance images obtained after contrast injection, demonstrating (A) homogeneous enhancement of the entire wall thickness (arrow), (B) layered (stratified) enhancement, characterized by mucosal (arrowhead) and serosal (arrow) enhancement, and (C) mucosal enhancement (arrow).
diffuse enhancement of the entire wall thickness. Stratified enhancement shows mucosal, relatively poor submucosal, and serosal enhancement, which creates a target-like
Figure 8. A 28-year-old man with fibrostenotic-predominant Crohn’s disease and coexisting active inflammation. Axial computed tomography enterographic image, showing a very significant stricture with upstream dilatation (arrowhead) and mucosal hyperenhancement (arrows).
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Figure 9. A 21-year-old woman with Crohn’s disease. A coronal True fast imaging with steady-state precession (TrueFISP) image (A) and a coronal T1 postcontrast image (B), showing wall thickening of the distal ileum (A, white arrowhead) located a few centimetres from an ileocolic anastomosis (black arrowheads), with homogeneous enhancement (B, white arrowhead). Note also the prominent vasa recta characterized by short low-signal-intensity parallel lines on the T2 TrueFISP image (A), oriented perpendicular to the longitudinal axis (A, arrow), and high-signal-intensity parallel lines (B, arrow) due to contrast enhancement of the vasculature (B).
Bowel-Wall Stenosis and Bowel Obstruction
Ulcerations
Bowel-wall stenosis in Crohn’s disease is invariably associated with a segment of thickened bowel wall, whereas adhesive strictures do not demonstrate this finding [10] and can be due to active inflammation (Figure 8). This differentiation is crucial to the choice of therapy. Disease activity can be suggested by oedema, mucosal ulceration, and contrast enhancement. Although this distinction is very important, it is not always clear on imaging studies [16]. When a prestenotic dilatation of >3 cm is present, the disease is probably chronic and clinically significant [4e6].
Moderate and deep ulcerations appear as areas of mural irregularity on postcontrast CTE or MRE, and on T2-weighted images (Figure 11) [1,8,10,14]. The reported sensitivity of MRE for the diagnosis of ulcers is 56%-90% [8,13].
Prominent Vasa Recta (Comb Sign) Prominent vasa recta are caused by increased mesenteric vascularity during active inflammation. The vessels penetrate the bowel wall perpendicular to the affected bowel lumen and are seen as parallel lines that enhance after contrast administration (Figure 9) [1e3,10].
Mesenteric Oedema Mesenteric oedema is seen as increased attenuation of the mesenteric fat on CTE images and high T2 signal intensity on fat-suppressed MRE images, which corresponds to active disease in the bowel wall (Figure 10) [3,7,10].
Figure 10. A 55-year-old man with Crohn’s disease. Axial fat-saturated T2 magnetic resonance enterographic image, showing high signal intensity in mesentery adjacent to the involved ileal segment (arrow). This finding is best observed with fat suppression.
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Figure 11. A 65-year-old woman with Crohn’s disease. A coronal T2 half-Fourier acquisition single-shot turbo spin-echo (HASTE) image (A) and a coronal True fast imaging with steady-state precession [TrueFISP] image (B), showing wall thickening with deep ulceration (A, B, arrow) of the distal ileum. (C) Note the wall ulceration (arrow), and also mucosal hyperenhancement (arrowhead) on a coronal T1 postcontrast image.
Sinuses and Fistulas Sinuses (Figure 12) and fistulas indicate active disease and are seen as high-attenuation lines on CTE images and T2 hyperintense lines that enhance after contrast administration,
Figure 12. A 36-year-old woman with penetrating Crohn’s disease. Coronal volume-rendered computed tomography enterographic section, depicting a sinus tract (arrowhead) that originated from the terminal ileum. Note other signs of active inflammation (wall thickening and mucosal hyperenhancement) in the ileocecal valve and terminal ileum (arrow).
which reflect their higher vascular flow and hyperemia [8]. Complex internal fistulas usually have a stellate appearance, with multiple tracts and bowel loops that radiate from the
Figure 13. A 42-year-old man with fibrostenotic-predominant Crohn’s disease. A complex fistula with transmural inflammation and marked upstream dilatation is evident. A coronal fat-suppressed T1 magnetic resonance image obtained after intravenous contrast administration, showing complex ileoileal (arrow) and ileocolonic (arrowhead) fistulas with diffuse enhancement of the entire wall thickness (transmural inflammation), and marked upstream dilatation.
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Figure 14. A 37-year-old man with an enterovesical fistula in Crohn’s disease. Sagittal (A) and coronal (B) computed tomography enterographic images, depicting an ileovesical fistula (white arrows) with thickening and enhancement of the bladder dome (black arrowheads). A small amount of gas is visible inside the bladder (A, white arrowhead). An ileoileal fistula with bowel-wall thickening and mural hyperenhancement is also visible (B, black arrow).
central portion that are associated with desmoplastic and fibrotic reactions in the surrounding mesentery. Fistulas in Crohn’s disease can be enteroenteric and enterocolonic (Figure 13), enterovesical (Figure 14), enterocutaneous (Figure 15), and perianal [1,4,10]. The reported sensitivity of MRE and CTE for the detection of internal fistulas is 83% and the specificity is 100% [8]. Abscesses Abscesses are seen as hyperintense on T2W MRE imaging, with a corresponding hypodense appearance on CT,
with a capsule that enhances after contrast administration (Figure 16) [1,8,10]. These features are a sign of active disease [4].
Pseudodiverticulum Formation Pseudodiverticulum is the apparent dilatation of the antimesenteric border of the bowel wall. This condition occurs as a consequence of fibrosis of the diseased mesenteric side and is usually associated with other signs of chronic disease (Figure 17) [8,10].
Fibrofatty Proliferation Fibrofatty proliferation occurs as increased mesenteric fat surrounding chronically inflamed bowel loops and is a sign of chronic disease (Figure 18) [1,2,8].
Reactive Lymphadenopathy Reactive lymphadenopathy commonly occurs in association with active inflamed bowel loops [1,5,8].
Pitfalls Figure 15. A 59-year-old man with Crohn’s disease. Axial computed tomography enterographic image, depicting a complex enterocutaneous fistula with a track from the rectum to the skin (arrows) and multiple foci of cutaneous drainage (arrowheads). This patient also had ileocutaneous fistulous tracks (not shown).
Fat wall infiltration, oedema, and fibrosis Abnormalities such as fatty wall infiltration, oedema, and fibrosis appear as nonspecific low attenuation on CTE and are more readily characterized by MRE because of its higher tissue contrast differentiation [3,7,10].
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Figure 16. A 59-year-old man with known Crohn’s disease. Coronal (A) and axial (B) T2 magnetic resonance (MR) images and an axial gadolinium-enhanced fat-saturated T1 MR image (C), showing a small fluid collection with a thick, irregular, and contrast-enhanced wall, within the lower abdomen, in the mesentery adjacent to the cecum and terminal ileum, without communication with the bowel lumen (arrow). These findings are consistent with an abscess.
Inadequate bowel distention Inadequate bowel distention is an important problem that can affect the assessment of wall thickness and enhancement. Nondistended loops can simulate or mask disease [3,10,11,14]. Conclusion CTE and MRE are powerful tools in the management of Crohn’s disease that can demonstrate small bowel mucosal
Figure 17. A 56-year-old man with multiple pseudodiverticula in Crohn’s disease. Coronal computed tomography enterographic image, showing pseudosacculations (arrowheads) produced by asymmetric thickening of the terminal ileal mesenteric border. Also note the prominence of the vasa recta (comb sign, arrows).
and mural inflammation as well as diagnose extraluminal complications. Mural thickening, submucosal oedema, wall enhancement, fat stranding, reactive lymphadenopathy, and engorgement of the vasa recta characterize active disease. Fibrostenotic disease is seen as nonspecific wall hypodensity on CTE and as mural hypointense signaling on T1- and T2-weighted images, with a lack of enhancement or progressive delayed enhancement. Findings that indicate long-standing Crohn’s disease include submucosal fat deposition, pseudodiverticula, fibrofatty proliferation, and fibrotic strictures. CTE and MRE can also help to identify the predominant disease type (active inflammatory or fibrostenotic) and to guide and monitor treatment (medical vs surgical).
Figure 18. A 46-year-old woman with long-standing Crohn’s disease. Axial computed tomography enterographic image, showing fibrofatty proliferation encircling the involved bowel loops (arrows). Note also ileal segments that display wall thickening and mural hyperenhancement, mainly in the mucosa (arrowheads). A complex ileocolonic fistula was also noted in this patient (not shown).
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