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Magnetic Resonance Enterography in the Evaluation of the Small Bowel
Magnetic Resonance Enterography in the Evaluation of the Small Bowel Carmel G. Cronin, MRCPI, FFR(RCSI), Derek G. Lohan, FFR(RCSI), Ann M. Browne, MRCPI, Clare Roche, MRCPI, FFR(RCSI), FRCR, and Joseph M. Murphy, MRCPI, FFR(RSCI), FRCR
A
dvances in magnetic resonance imaging (MRI) technology and the introduction of fast MRI sequences have evoked increasing interest in the use of MRI for small bowel evaluation and as a potential successor to conventional enteroclysis (CE), or small bowel series and/or small bowel follow through (SBFT) and computed tomography enteroclysis or enterography. MR enteroclysis/enterography small bowel follow-through (MRSBFT) techniques have been described, each with different advantages and disadvantages. However, both techniques provide excellent soft-tissue contrast resolution, superb luminal, mural, and extramural enteric detail, and direct multiplanar imaging capabilities that enhance the diagnostic value of MRI for small bowel diseases. The attraction of MRI is further augmented by the absence of ionizing radiation exposure, facilitating sequential imaging and the derivation of vital information regarding small bowel function and the effect of disease thereon.1,2 MRI of the small bowel is an evolving diagnostic tool with many aspects of the technique yet to be optimized, from patient preparation and imaging protocols to new radiological and clinical indications and uses.
Clinical Indications To date, the main clinical indications include assessment and diagnosis of Crohn’s disease (CD) (Fig. 1) and to a lesser extent, evaluation of celiac disease, small bowel tumors, lymphoma, and small bowel obstruction.3-5 Other scientific and educational reviews have demonstrated isolated cases of small bowel pathology at MR enterography as outlined in Table 1.4-14
Technique Patient Preparation In general, patients fast from midnight the preceding night, which allows time for small bowel emptying. Lin and Narral15 demonstrated success with a preprocedural fasting time of 4 hours. This shorter fasting period allows imaging to be performed at more flexible times throughout the day.
Oral Contrast A high volume is required to distend the bowel for circumferential mural evaluation. Patient tolerance is the current limitation. As yet, there is no consensus on the optimal volume of oral contrast medium needed for an enterographic examination. Ajaj et al16 reported no significant differences in bowel distension with 1000, 1200, or 1500 mL of mannitol solution. Kuehle et al17 studied the effect of different types and volumes of oral contrast on bowel distension and timing of image acquisition and found that good distension of the bowel was achieved with 1350-mL contrast medium (1.2%-2% sorbitol solution and 0.2% locust bean gum), with no additional distension achieved by increasing the contrast medium volume to 1800 mL. Thus, a volume between 1000 and 1350 mL seems adequate. There are several oral contrast agents that have been used in MRI, each with different advantages and disadvantages. Numerous contrast agents have been evaluated. Limitations of their use predominantly relate to unpalatable taste, cost, and availability of the agent and associated side effects, including nausea, vomiting, and diarrhea. Oral contrast agents include biphasic, negative, and positive contrasts.
Biphasic Contrast Agents Department of Radiology, University College Hospital, Galway, Ireland. Address reprint requests to Carmel G. Cronin, MRCPI, FFR(RCSI), Department of Radiology, University College Hospital, Galway, Ireland. E-mail: [email protected]
0037-198X/09/$-see front matter © 2009 Elsevier Inc. All rights reserved. doi:10.1053/j.ro.2009.05.006
There are two enhancement patterns seen with the biphasic contrast agents in use. Low signal on T1- and high signal on T2-weighted images is the most common. The other pattern is high signal on T1- and low signal on T2-weighted images. 237
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Figure 1 (A-C) MR enterography images of a 30 year old patient with Crohn’s disease. Images demonstrate mural thickening (white arrow), high signal within the mural thickening (black arrow), mesenteric vessel (vasa recta) engorgement (white arrowhead), mesenteric adenopathy (black arrow head) consistent with active disease.
Low Signal on T1- and High Signal on T2-Weighted Images These contrast agents have been widely evaluated and are most commonly used. The biphasic oral contrast agents commercially available include water, polyethylene glycol, VoLumen (Bracco, Lake Success, NY), nonosmotic agents, such as locust bean gum and methylcellulose, metamucil, diatrizoate meglumine, diatrizoate sodium, and low Hounsfield value or molecular weight barium. Water is widely available, cheap, and acceptable. As a contrast agent, however, water is undesirable because of its absorption in the distal small bowel resulting in suboptimal distension17-19 of the site most commonly affected by CD. Polyethylene glycol is a high-osmolarity, nonabsorbed, non-
fermented contrast medium, which has been shown to provide excellent intraluminal contrast and luminal distension.1,20-22 VoLumen, a contrast agent containing sorbitol whose osmotic properties cause it to retain water, has also been shown to be effective.15 High Signal on T1 and Low Signal on T2 Concentrated gadolinium chelates mixed with barium provide the opposite signal intensity to the biphasic agents mentioned previously; they have high signal intensity on T1weighted images and low signal on T2-weighted images.23 These agents, similar to negative contrast agents, can increase the conspicuity of abscesses adjacent to small bowel loops on T2-weighted imaging, as this agent decreases the signal in-
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Table 1 Pathologic Findings at MR Enterography
Positive Contrast Agents
Inflammatory bowel disease CD, celiac disease Radiation enteritis Scleroderma Small bowel tumors Benign Small bowel polyposis Duodenal Diffuse small bowel polyposis Adenoma of the ampulla Duodenal leiomyoma Lipoma Malignant Duodenal adenocarcinoma Melanoma, plasmacytoma, carcinoid, GIST Infiltrative obstructing peritoneal colon cancer metastasis Small bowel lymphoma Congenital anomalies Small bowel malrotation Duodenal diverticula Small bowel obstruction or dilation Other Duodenitis Duodenal intusseseption
Positive contrast agents show high signal on T1- and T2weighted images secondary to paramagnetic substances. These substances include gadolinium chelates,24 manganese ions,30 ferrous ions,31 and foods such as blueberry juice.32 Positive contrast agents demonstrate wall thickening well on T1-weighted images. Positive contrast agents can also increase the conspicuity of bowel interloop abscesses on T1weighted imaging, in which the bowel lumen will have high signal intensity because of the positive contrast agent and the interloop abscesses will have low signal intensity fluid on T1 with rim enhancement if intravenous contrast in used.24 Contrast agents used to date have different qualities and the choice of contrast agent used is largely influenced by the radiologist’s choice and experience at evaluating the bowel. Knowledge of the properties of each contrast is important for their optimal use and for problem solving. For example, if the use of positive T2 contrast makes it difficult to differentiate a diseased small bowel loop from an interloop abscess, using a negative contrast agent might solve the problem on a study with positive T2 contrast.
tensity in the bowel lumen but does not affect the high signal in the adjacent abscess. However, low intraluminal signal on T2 can decrease the conspicuity of mural pathology as there is less difference in signal intensity between moderate signal wall thickening and low signal intraluminal contrast, and low signal intraluminal pathology against low signal intraluminal contrast.
Negative Contrast Agents Negative oral contrast agents show low signal on T1- and T2-weighted imaging secondary to superparamagnetic particles. Negative contrast agents include perfluorooctyl bromide, ferumoxide oral suspension, and oral magnetic particles.24-29 The main advantage of negative contrasts is that, similar to biphasic agents negative on T2, they can improve the conspicuity of abscesses adjacent to small bowel loops, as negative contrast agents decrease the signal intensity in the bowel lumen but not the high signal in the adjacent abscess on T2-weighted imaging. A limitation of negative contrast is that the moderate signal of inflamed bowel wall may be less conspicuous on T2weighted images using a negative intraluminal contrast agent, with less difference in signal intensity between moderate signal of the diseased bowel wall and low signal of the intraluminal contrast than moderate signal of diseased bowel wall and high signal of positive T2 intraluminal contrasts. Furthermore, the low signal intensity of intraluminal contrast on T2-weighted images may decrease the conspicuity of the normal small bowel wall and of low signal intensities lesions on T2-weighted images, such as carcinoid tumors or CD.
Intravenous Contrast The normal bowel wall on contrast-enhanced 3D FLASH images with fat saturation exhibits high signal intensity because of gadolinium uptake, and is well delineated between the low signal intensity of the mesenteric fat and the negative intraluminal contrast agent. A scanning delay of 60-80 seconds after IV contrast allows for demonstration of the bowel wall, mesenteric vessels, and inflammatory lymph nodes. The 3D FLASH sequence is sensitive to motion; consequently, antiperistaltic drug administration should precede the application of the sequence. The use of intravenous contrast in the assessment of CD has been investigated in many studies. Gourtsoyiannis et al1 ranked the product of bowel wall thickness, lymph node enhancement, and intestinal ulcers as having the strongest correlation with active CD. The degree of bowel wall thickening and enhancement also has high degree of correlation with the Crohn’s disease activity index (CDAI) and histologic grading. Sempere et al33 compared MRI findings of bowel wall thickening and enhancement in patients with active and quiescent CD, and found significant correlation between the degree of enhancement and thickening in comparison with CDAI. Koh et al34 reported a sensitivity of 91% and a specificity of 71% for active CD, whereas using the CDAI the sensitivity was 92% and specificity 28% in the same study. Assessment of inflammatory activity is required to monitor the effects of medical therapy and immune-modulating agents.
Image Timing In our institute we image at approximately 20 minutes after contrast ingestion to maximize visualization of the proximal small bowel. Delayed repeat imaging is performed as needed until the contrast bolus has passed to the colon (Fig. 2). Examination completion is defined as the presence of con-
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Figure 2 A and B are normal MR small bowel follow through in a 60 year old patient. On the initial image (A) at 20 minutes the jejunum and proximal ileum are well distended with the distal ileum poorly distended. On the delayed imaging at approximately 50 minutes (B) the proximal and distal ileum are well distended with contrast.
trast in the cecum or distal, with diagnostic-quality distension of the small bowel throughout its length. Some investigators advocate repeated imaging immediately after ingestion until the contrast reaches the terminal ileum, before formal imaging sequences are performed.21,35 This approach seems less practical as it increases the examination time required using valuable MR table time36 and results in poor patient tolerance. Other studies have advocated a longer duration of contrast ingestion of 45 minutes before imaging. Figure 2 shows a normal MRSBFT in a 60-year-old patient. On the initial image (Fig. 2A) at 20 minutes, the jejunum and proximal ileum are well distended, whereas the distal ileum is poorly distended. On the delayed image at approximately 50 minutes (Fig. 2B), the proximal and distal ileum are well distended with contrast.
Patient Position Until recently it was felt that the prone position was ideal for patient imaging as it helps to separate bowel loops, provide maximal bowel coverage on coronal images, and decrease scanning volume. However, for patient comfort and other practical considerations, the supine position may be preferred. The importance of optimal small bowel distension at MRSBFT has been repeatedly emphasized in the published data. We demonstrated that although the prone position offers better distention, it did not translate to better lesion detection.37
Patient Motion The effect of motion during the acquisition of data is one of the main causes of image degradation in MRI of the small bowel. Sequences used for MRI of the bowel should be fast
and insensitive to motion artifacts.38 For imaging sequences sensitive to motion artifact, such as single-shot sequences (half-acquisition single-shot turbo spin-echo [HASTE], single-shot fast spin-echo [SSFSE], single-shot turbo spinecho), an antispasmodic agent may be given intramuscularly or intravenously before imaging to decrease bowel peristalsis.
Magnetic Resonance Imaging An MRI system with a magnetic field strength of at least 1.5 T should be used for small bowel imaging. MR enterography at 3 T has yet not been reported.
MRI Planes Usually each phase of imaging involves a combination of coronal and axial two-dimensional acquisitions from the diaphragm to the symphysis pubis in craniocaudal extent and the entire abdominal cavity in the transverse plane. The acquisition of multiple imaging planes is critical to avoid problems with partial volume effects. Additional sagittal planes are sometimes required for precise small bowel and pathology localization and evaluation.
MRSBFT Sequences The introduction of fast spin-echo sequences, otherwise known as turbo spin-echo, depending on manufacturer, has been a major advancement in MR technique. This technique reduces image acquisition time to the order of seconds, and brings the small bowel within purview of MRI. There is no consensus on the most appropriate protocol, but most studies have used T2-weighted sequences (balanced gradient echo and/or single shot technique) and contrast-enhanced
MR enterography in the evaluation of the small bowel gradient echo sequences for disease activity assessment. The main diagnostic T2-weighted sequences can be divided into the balanced gradient echo (true fast imaging with steadystate precession [TruFISP], fast imaging employing steadystate acquisition, balanced fast field echo (FFE)) sequences and the single-shot technique (HASTE, SSFSE, single-shot turbo spin-echo). Fast T1-weighted gradient echo sequences without fat suppression or T1-weighted fast spin-echo sequences can also be performed before and after intravenous contrast injection to aid in detecting and characterizing disease activity.
TruFISP Sequences TruFISP (steady-state free precession) is a fast MR technique with the highest signal-to-noise ratio per unit time of all imaging sequences. With the short repetition time now possible, it can produce an image with acceptable resolution in ⬎1 second. It has both T1 and T2 contrast weighting, which produces strong contrast between tissues with different ratios of T1 and T2. Tissue contrast largely reflects the T2 differences in different structures, as T1 is held constant by the extremely short repetition time and echo time. Tissues with a high ratio, such as bile, blood, and fat, appear bright. TruFISP was described by Prassopoulos et al39 as the cardinal sequence for MR small bowel imaging. Because of high contrast between the hypointense bowel wall and hyperintense lumen (assuming use of a positive or biphasic oral contrast agent), bowel wall abnormalities are well highlighted on this sequence. It provides motion-free, high-resolution, “T2-like” images of the small intestine, mesentery, and vessels in seconds.40 Ulcerations, cobblestoning, wall thickening, and luminal narrowing are well visualized and demonstrated in detail on TruFISP images. The high intraluminal signal seen on these T2-weighted images is highly advantageous for detecting fistulas and sinus tracts, which may otherwise be missed on the T1 sequence because of limited contrast with the surround tissues.39 Motion-related artifacts are minimal on TruFISP images because of the short acquisition time.24,41 TruFISP sequences are also insensitive to intraluminal flow voids—an artifact seen in HASTE imaging because of balanced and symmetric gradient of TruFISP design. Consequently, the use of antiperistaltic drugs to reduce bowel motion can be avoided, giving a major advantage to TruFISP over the other sequences.4
TruFISP Artifacts The most common artifact observed in TruFISP imaging is the black boundary artifact, which appears in voxels in which both fat and water protons are present. This artifact can be easily recognized as a thin “black” line along the outer border of the bowel wall. Black-boundary artifacts can be clearly differentiated from normal small bowel wall and folds and from abnormal bowel wall thickening by its low signal intensity as opposed to the moderate signal intensity of the normal and thickened small bowel wall. It generally does not interfere with the diagnosis of small bowel wall abnormalities and has not been found to cause any significant limitations.42
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HASTE Sequences The T2-weighted sequences are generated by rapid acquisition and relaxation enhancement, with ultrafast acquisition time, usually in the order of seconds. The names of these sequences are manufacturer-dependent, including the HASTE and the SSFSE sequences. On heavily T2-weighted images, actively inflamed bowel wall is edematous and seen as high T2 signal. In the quiescent stage of the disease, the wall signal intensity decreases to reflect underlying fibrosis. Fat-suppression techniques can be helpful in T2-weighted images by increasing the conspicuity of high signal intensity in the bowel wall against adjacent fat saturated mesenteric fat in areas of active inflammation.43 Excellent correlation between biological activity and T2-weighted wall signal intensity has been found.44 The images produced by this technique are highly resistant to magnetic susceptibility and chemical shift artifact.
HASTE Artifacts The long TE in combination with the single-slice acquisition makes the HASTE sequence sensitive to motion artifact and flow artifact. Flow artifact is caused by intestinal peristalsis. Intraluminal flow void can be seen as areas of low signal intensity within the bowel lumen. This appearance can be problematic in the evaluation of potential intraluminal masses. The administration of glucagon reduces bowel peristalsis and can reduce or eliminate flow artifact and provides homogeneous luminal opacification.39 The HASTE sequence has poor soft-tissue contrast45 and does not provide sufficient information regarding the mesentery39 because of k-space filtering effects.46 Mesenteric structures are better visualized on the TruFISP sequence than on the single-shot HASTE sequence.
Advantages, Disadvantages, and Importance of Each Technique Conventional Imaging Versus MR Enteroclysis Until recently conventional imaging was considered the gold standard for small bowel investigation against which all new modes of investigation were assessed. Several studies have found MR enteroclysis to be superior to CE.4,47-49 In a study by Ochsenkuhn et al48 comparing CE and MR enteroclysis assessment of Crohn’s terminal ileitis, with endoscopy and histology as baseline criteria, MR enteroclysis had superior sensitivity to CE (89% vs 72%). Furthermore, MRI detected proximal lesions in 9 cases missed by CE. In a trial by Rieber et al49 comparing MR enteroclysis with CE in 84 patients with histologic and endoscopic correlation, the sensitivity for diagnosing inflammatory bowel disease was 85.4% for CE vs 95.2% for MR enteroclysis, and the specificity was 76.9% for CE vs 92.6% for MR enteroclysis. MR enteroclysis was found to have the added advantage of better depicting extramural detail. In this study, because none of the abscesses was diagnosed with CE; the sensitivity was 0% for CE, but 77.8% for
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242 MR enteroclysis. Sensitivity for diagnosing fistulae was 17.7% for CE and 70.6% for MR enteroclysis.49
ography had the potential to be used as a radiation-free alternative for the evaluation of patients with CD.54
MR Enteroclysis vs MR Enterography
Limitations of MRI
Enteroclysis can result in a very stressful patient experience. It requires duodenal and/or jejunal intubation and radiation exposure when performed with conventional fluoroscopic guidance. The enterography technique obviates the need for nasoenteric intubation resulting in better patient acceptance. Ideally the use of an adequate volume of oral contrast, consumed in a constant manner in enterography should provide adequate small bowel luminal distension and obviate the need for enteroclysis and the invasive component of the enteroclysis technique. In a study by Masselli et al50 comparing MR enteroclysis and MR enterography (MR per OS), enteroclysis offered statistically significantly superior small bowel distension only in the jejunum. MR enteroclysis was superior to MR enterography at visualizing superficial abnormalities (P ⬍ 0.01), however all pathologic findings were reliably detected by both techniques. These findings were similar to those in studies by Negaard et al and Schreyer et al. In a study of 40 patients, Negaard et al51 found that bowel distension was inferior with MR enterography (MRI per OS) as compared with MR enteroclysis. However, both methods diagnosed CD with equal sensitivity and a high diagnostic accuracy (sensitivity, specificity, positive predictive values, and negative predictive values: MRI per OS 88%, 89%, 89%, 89%, respectively; MRE 88%, 84%, 82%, 89%) and interobserver agreement (MRI per OS, k ⫽ 0.95; MRE, k ⫽ 1). In a study of 21 patients, Schreyer et al52 found that all pathologic findings seen on CE were seen on MR enterography and MR enteroclysis, with MRI detecting additional information in 6 of 21 patients. Thus, the improved distension at enteroclysis over enterography may not necessarily translate into improved sensitivity and specificity for disease diagnosis. In our institution, we use the enterography technique for all cases, reserving enteroclysis for those not able to tolerate oral contrast, nondiagnostic enterography examinations, problem solving, and further evaluation of those with normal examinations but a high clinical suspicion for small bowel disease.
One of the main limitations of MRI is the inferior spatial and temporal resolution in comparison with CT. Using multidetector CT scanners, 2-3-mm images can be obtained throughout the abdomen in seconds in a single breath-hold. With this improved spatial resolution, multiplanar reformatted images can be generated in various planes. In comparison, the slice thickness for MRI is usually 4-6 mm. However, the improved spatial and temporal resolution of CT over MRI does not necessarily translate into improved sensitivity and specificity. It is not possible to establish the relative diagnostic performances of MRE and CTE from existing published data. The radiologist must determine which imaging modality to use, whether the functional information, soft-tissue contrast, and absence of ionizing radiation that can be obtained with MRI outweigh its inferior spatial and temporal resolution.
Computed Tomography vs MRI Only a few published studies have compared CT and MRI. In a study by Low et al53 comparing contrast-enhanced MRI and single-phase helical CT scanning in 26 patients with CD, MRI depicted 80%-85% of abnormal segments, as compared with 60%-65% by CT. Moderate and marked disease was shown equally well on CT and MRI, but for mild disease MRI detected 68%-79% of the abnormal segments, as compared with 32%-46% by CT. There was no significant difference in complication detection (fistulas, phlegmon, or abscess) between MR and CT.53 In a recent study comparing CT enterography, MR enterography, and SBFT in the assessment of CD of the small bowel, MR enterography had a diagnostic effectiveness comparable with of CT enterography, and both were superior to SBFT. This study concluded that MR enter-
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243 36. Patak MA, Froehlich JM, von Weymarn C, et al: Non-invasive distension of the small bowel for magnetic-resonance imaging. Lancet 358: 987-988, 2001 37. Cronin CG, Lohan DG, Mhuircheartaigh JN, et al: MRI small-bowel follow-through: prone versus supine patient positioning for best smallbowel distention and lesion detection. AJR Am J Roentgenol 191:502506, 2008 38. Umschaden HW, Gasser J: MR enteroclysis. Radiol Clin North Am 41:231-248, 2003 39. Prassopoulos P, Papanikolaou N, Grammatikakis J, et al: MR enteroclysis imaging of Crohn’s disease. Radiographics 201:S161-S172, 2001 40. Papanikolaou N, Prassopoulos P, Grammatikakis I, et al: Technical challenges and clinical applications of magnetic resonance enteroclysis. Top Magn Reson Imaging 13:397-408, 2002 41. Lauenstein TC, Schneemann H, Vogt FM, et al: Optimization of oral contrast agents for MR imaging of the small bowel. Radiology 228:279283, 2003 42. Gourtsoyiannis N, Papanikolaou N, Grammatikakis J, et al: MR enteroclysis: technical considerations and clinical applications. Eur Radiol 12:2651-2658, 2002 43. Horton KM, Eng J, Fishman EK: Normal enhancement of the small bowel: evaluation with spiral CT. J Comput Assist Tomogr 24:67-71, 2000 44. Madsen SM, Thomsen HS, Schlichting P, et al: Evaluation of treatment response in active Crohn’s disease by low-field magnetic resonance imaging. Abdom Imaging 24:232-239, 1999 45. Coates GG, Borrello JA, McFarland EG, et al: Hepatic T2-weighted MRI: a prospective comparison of sequences, including breath-hold, half-Fourier turbo spin echo (haste). J Magn Reson Imaging 8:642-649, 1998 46. Gourtsoyiannis NC, Papanikolaou N, Karantanas A: Magnetic resonance imaging evaluation of small intestinal Crohn’s disease. Best Pract Res Clin Gastroenterol 20:137-156, 2006 47. Albert JG, Martiny F, Krummenerl A, et al: Diagnosis of small bowel Crohn’s disease: a prospective comparison of capsule endoscopy with magnetic resonance imaging and fluoroscopic enteroclysis. Gut 54: 1721-1727, 2005 48. Ochsenkuhn T, Herrmann K, Schoenberg SO, et al: Crohn’s disease of the small bowel proximal to the terminal ileum: detection by MR enteroclysis. Scand J Gastroenterol 39:953-960, 2004 49. Rieber A, Wruk D, Potthast S, et al: Diagnostic imaging in Crohn’s disease: comparison of magnetic resonance imaging and conventional imaging methods. Int J Colorectal Dis 15:176-181, 2000 50. Masselli G, Casciani E, Polettini E, et al: Comparison of MR enteroclysis with MR enterography and conventional enteroclysis in patients with Crohn’s disease. Eur Radiol 18:438-447, 2008 51. Negaard A, Paulsen V, Sandvik L, et al: A prospective randomized comparison between two MRI studies of the small bowel in Crohn’s disease, the oral contrast method and MR enteroclysis. Eur Radiol 17: 2294-2301, 2007 52. Schreyer AG, Geissler A, Albrich H, et al: Abdominal MRI after enteroclysis or with oral contrast in patients with suspected or proven Crohn’s disease. Clin Gastroenterol Hepatol 2:491-497, 2004 53. Low RN, Francis IR, Politoske D, et al: Crohn’s disease evaluation: comparison of contrast enhanced MR imaging and single-phase helical CT scanning. J Magn Reson Imaging 11:127-135, 2000 54. Lee SS, Kim AY, Yang SK, et al: Crohn’s disease of the small bowel: comparison of CT enterography, MR enterography, and small-bowel Follow-Through as diagnostic techniques. Radiology 251:751751, 2009
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dvances in magnetic resonance imaging (MRI) technology and the introduction of fast MRI sequences have evoked increasing interest in the use of MRI for small bowel evaluation and as a potential successor to conventional enteroclysis (CE), or small bowel series and/or small bowel follow through (SBFT) and computed tomography enteroclysis or enterography. MR enteroclysis/enterography small bowel follow-through (MRSBFT) techniques have been described, each with different advantages and disadvantages. However, both techniques provide excellent soft-tissue contrast resolution, superb luminal, mural, and extramural enteric detail, and direct multiplanar imaging capabilities that enhance the diagnostic value of MRI for small bowel diseases. The attraction of MRI is further augmented by the absence of ionizing radiation exposure, facilitating sequential imaging and the derivation of vital information regarding small bowel function and the effect of disease thereon.1,2 MRI of the small bowel is an evolving diagnostic tool with many aspects of the technique yet to be optimized, from patient preparation and imaging protocols to new radiological and clinical indications and uses.
Clinical Indications To date, the main clinical indications include assessment and diagnosis of Crohn’s disease (CD) (Fig. 1) and to a lesser extent, evaluation of celiac disease, small bowel tumors, lymphoma, and small bowel obstruction.3-5 Other scientific and educational reviews have demonstrated isolated cases of small bowel pathology at MR enterography as outlined in Table 1.4-14
Technique Patient Preparation In general, patients fast from midnight the preceding night, which allows time for small bowel emptying. Lin and Narral15 demonstrated success with a preprocedural fasting time of 4 hours. This shorter fasting period allows imaging to be performed at more flexible times throughout the day.
Oral Contrast A high volume is required to distend the bowel for circumferential mural evaluation. Patient tolerance is the current limitation. As yet, there is no consensus on the optimal volume of oral contrast medium needed for an enterographic examination. Ajaj et al16 reported no significant differences in bowel distension with 1000, 1200, or 1500 mL of mannitol solution. Kuehle et al17 studied the effect of different types and volumes of oral contrast on bowel distension and timing of image acquisition and found that good distension of the bowel was achieved with 1350-mL contrast medium (1.2%-2% sorbitol solution and 0.2% locust bean gum), with no additional distension achieved by increasing the contrast medium volume to 1800 mL. Thus, a volume between 1000 and 1350 mL seems adequate. There are several oral contrast agents that have been used in MRI, each with different advantages and disadvantages. Numerous contrast agents have been evaluated. Limitations of their use predominantly relate to unpalatable taste, cost, and availability of the agent and associated side effects, including nausea, vomiting, and diarrhea. Oral contrast agents include biphasic, negative, and positive contrasts.
Biphasic Contrast Agents Department of Radiology, University College Hospital, Galway, Ireland. Address reprint requests to Carmel G. Cronin, MRCPI, FFR(RCSI), Department of Radiology, University College Hospital, Galway, Ireland. E-mail: [email protected]
0037-198X/09/$-see front matter © 2009 Elsevier Inc. All rights reserved. doi:10.1053/j.ro.2009.05.006
There are two enhancement patterns seen with the biphasic contrast agents in use. Low signal on T1- and high signal on T2-weighted images is the most common. The other pattern is high signal on T1- and low signal on T2-weighted images. 237
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Figure 1 (A-C) MR enterography images of a 30 year old patient with Crohn’s disease. Images demonstrate mural thickening (white arrow), high signal within the mural thickening (black arrow), mesenteric vessel (vasa recta) engorgement (white arrowhead), mesenteric adenopathy (black arrow head) consistent with active disease.
Low Signal on T1- and High Signal on T2-Weighted Images These contrast agents have been widely evaluated and are most commonly used. The biphasic oral contrast agents commercially available include water, polyethylene glycol, VoLumen (Bracco, Lake Success, NY), nonosmotic agents, such as locust bean gum and methylcellulose, metamucil, diatrizoate meglumine, diatrizoate sodium, and low Hounsfield value or molecular weight barium. Water is widely available, cheap, and acceptable. As a contrast agent, however, water is undesirable because of its absorption in the distal small bowel resulting in suboptimal distension17-19 of the site most commonly affected by CD. Polyethylene glycol is a high-osmolarity, nonabsorbed, non-
fermented contrast medium, which has been shown to provide excellent intraluminal contrast and luminal distension.1,20-22 VoLumen, a contrast agent containing sorbitol whose osmotic properties cause it to retain water, has also been shown to be effective.15 High Signal on T1 and Low Signal on T2 Concentrated gadolinium chelates mixed with barium provide the opposite signal intensity to the biphasic agents mentioned previously; they have high signal intensity on T1weighted images and low signal on T2-weighted images.23 These agents, similar to negative contrast agents, can increase the conspicuity of abscesses adjacent to small bowel loops on T2-weighted imaging, as this agent decreases the signal in-
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Table 1 Pathologic Findings at MR Enterography
Positive Contrast Agents
Inflammatory bowel disease CD, celiac disease Radiation enteritis Scleroderma Small bowel tumors Benign Small bowel polyposis Duodenal Diffuse small bowel polyposis Adenoma of the ampulla Duodenal leiomyoma Lipoma Malignant Duodenal adenocarcinoma Melanoma, plasmacytoma, carcinoid, GIST Infiltrative obstructing peritoneal colon cancer metastasis Small bowel lymphoma Congenital anomalies Small bowel malrotation Duodenal diverticula Small bowel obstruction or dilation Other Duodenitis Duodenal intusseseption
Positive contrast agents show high signal on T1- and T2weighted images secondary to paramagnetic substances. These substances include gadolinium chelates,24 manganese ions,30 ferrous ions,31 and foods such as blueberry juice.32 Positive contrast agents demonstrate wall thickening well on T1-weighted images. Positive contrast agents can also increase the conspicuity of bowel interloop abscesses on T1weighted imaging, in which the bowel lumen will have high signal intensity because of the positive contrast agent and the interloop abscesses will have low signal intensity fluid on T1 with rim enhancement if intravenous contrast in used.24 Contrast agents used to date have different qualities and the choice of contrast agent used is largely influenced by the radiologist’s choice and experience at evaluating the bowel. Knowledge of the properties of each contrast is important for their optimal use and for problem solving. For example, if the use of positive T2 contrast makes it difficult to differentiate a diseased small bowel loop from an interloop abscess, using a negative contrast agent might solve the problem on a study with positive T2 contrast.
tensity in the bowel lumen but does not affect the high signal in the adjacent abscess. However, low intraluminal signal on T2 can decrease the conspicuity of mural pathology as there is less difference in signal intensity between moderate signal wall thickening and low signal intraluminal contrast, and low signal intraluminal pathology against low signal intraluminal contrast.
Negative Contrast Agents Negative oral contrast agents show low signal on T1- and T2-weighted imaging secondary to superparamagnetic particles. Negative contrast agents include perfluorooctyl bromide, ferumoxide oral suspension, and oral magnetic particles.24-29 The main advantage of negative contrasts is that, similar to biphasic agents negative on T2, they can improve the conspicuity of abscesses adjacent to small bowel loops, as negative contrast agents decrease the signal intensity in the bowel lumen but not the high signal in the adjacent abscess on T2-weighted imaging. A limitation of negative contrast is that the moderate signal of inflamed bowel wall may be less conspicuous on T2weighted images using a negative intraluminal contrast agent, with less difference in signal intensity between moderate signal of the diseased bowel wall and low signal of the intraluminal contrast than moderate signal of diseased bowel wall and high signal of positive T2 intraluminal contrasts. Furthermore, the low signal intensity of intraluminal contrast on T2-weighted images may decrease the conspicuity of the normal small bowel wall and of low signal intensities lesions on T2-weighted images, such as carcinoid tumors or CD.
Intravenous Contrast The normal bowel wall on contrast-enhanced 3D FLASH images with fat saturation exhibits high signal intensity because of gadolinium uptake, and is well delineated between the low signal intensity of the mesenteric fat and the negative intraluminal contrast agent. A scanning delay of 60-80 seconds after IV contrast allows for demonstration of the bowel wall, mesenteric vessels, and inflammatory lymph nodes. The 3D FLASH sequence is sensitive to motion; consequently, antiperistaltic drug administration should precede the application of the sequence. The use of intravenous contrast in the assessment of CD has been investigated in many studies. Gourtsoyiannis et al1 ranked the product of bowel wall thickness, lymph node enhancement, and intestinal ulcers as having the strongest correlation with active CD. The degree of bowel wall thickening and enhancement also has high degree of correlation with the Crohn’s disease activity index (CDAI) and histologic grading. Sempere et al33 compared MRI findings of bowel wall thickening and enhancement in patients with active and quiescent CD, and found significant correlation between the degree of enhancement and thickening in comparison with CDAI. Koh et al34 reported a sensitivity of 91% and a specificity of 71% for active CD, whereas using the CDAI the sensitivity was 92% and specificity 28% in the same study. Assessment of inflammatory activity is required to monitor the effects of medical therapy and immune-modulating agents.
Image Timing In our institute we image at approximately 20 minutes after contrast ingestion to maximize visualization of the proximal small bowel. Delayed repeat imaging is performed as needed until the contrast bolus has passed to the colon (Fig. 2). Examination completion is defined as the presence of con-
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Figure 2 A and B are normal MR small bowel follow through in a 60 year old patient. On the initial image (A) at 20 minutes the jejunum and proximal ileum are well distended with the distal ileum poorly distended. On the delayed imaging at approximately 50 minutes (B) the proximal and distal ileum are well distended with contrast.
trast in the cecum or distal, with diagnostic-quality distension of the small bowel throughout its length. Some investigators advocate repeated imaging immediately after ingestion until the contrast reaches the terminal ileum, before formal imaging sequences are performed.21,35 This approach seems less practical as it increases the examination time required using valuable MR table time36 and results in poor patient tolerance. Other studies have advocated a longer duration of contrast ingestion of 45 minutes before imaging. Figure 2 shows a normal MRSBFT in a 60-year-old patient. On the initial image (Fig. 2A) at 20 minutes, the jejunum and proximal ileum are well distended, whereas the distal ileum is poorly distended. On the delayed image at approximately 50 minutes (Fig. 2B), the proximal and distal ileum are well distended with contrast.
Patient Position Until recently it was felt that the prone position was ideal for patient imaging as it helps to separate bowel loops, provide maximal bowel coverage on coronal images, and decrease scanning volume. However, for patient comfort and other practical considerations, the supine position may be preferred. The importance of optimal small bowel distension at MRSBFT has been repeatedly emphasized in the published data. We demonstrated that although the prone position offers better distention, it did not translate to better lesion detection.37
Patient Motion The effect of motion during the acquisition of data is one of the main causes of image degradation in MRI of the small bowel. Sequences used for MRI of the bowel should be fast
and insensitive to motion artifacts.38 For imaging sequences sensitive to motion artifact, such as single-shot sequences (half-acquisition single-shot turbo spin-echo [HASTE], single-shot fast spin-echo [SSFSE], single-shot turbo spinecho), an antispasmodic agent may be given intramuscularly or intravenously before imaging to decrease bowel peristalsis.
Magnetic Resonance Imaging An MRI system with a magnetic field strength of at least 1.5 T should be used for small bowel imaging. MR enterography at 3 T has yet not been reported.
MRI Planes Usually each phase of imaging involves a combination of coronal and axial two-dimensional acquisitions from the diaphragm to the symphysis pubis in craniocaudal extent and the entire abdominal cavity in the transverse plane. The acquisition of multiple imaging planes is critical to avoid problems with partial volume effects. Additional sagittal planes are sometimes required for precise small bowel and pathology localization and evaluation.
MRSBFT Sequences The introduction of fast spin-echo sequences, otherwise known as turbo spin-echo, depending on manufacturer, has been a major advancement in MR technique. This technique reduces image acquisition time to the order of seconds, and brings the small bowel within purview of MRI. There is no consensus on the most appropriate protocol, but most studies have used T2-weighted sequences (balanced gradient echo and/or single shot technique) and contrast-enhanced
MR enterography in the evaluation of the small bowel gradient echo sequences for disease activity assessment. The main diagnostic T2-weighted sequences can be divided into the balanced gradient echo (true fast imaging with steadystate precession [TruFISP], fast imaging employing steadystate acquisition, balanced fast field echo (FFE)) sequences and the single-shot technique (HASTE, SSFSE, single-shot turbo spin-echo). Fast T1-weighted gradient echo sequences without fat suppression or T1-weighted fast spin-echo sequences can also be performed before and after intravenous contrast injection to aid in detecting and characterizing disease activity.
TruFISP Sequences TruFISP (steady-state free precession) is a fast MR technique with the highest signal-to-noise ratio per unit time of all imaging sequences. With the short repetition time now possible, it can produce an image with acceptable resolution in ⬎1 second. It has both T1 and T2 contrast weighting, which produces strong contrast between tissues with different ratios of T1 and T2. Tissue contrast largely reflects the T2 differences in different structures, as T1 is held constant by the extremely short repetition time and echo time. Tissues with a high ratio, such as bile, blood, and fat, appear bright. TruFISP was described by Prassopoulos et al39 as the cardinal sequence for MR small bowel imaging. Because of high contrast between the hypointense bowel wall and hyperintense lumen (assuming use of a positive or biphasic oral contrast agent), bowel wall abnormalities are well highlighted on this sequence. It provides motion-free, high-resolution, “T2-like” images of the small intestine, mesentery, and vessels in seconds.40 Ulcerations, cobblestoning, wall thickening, and luminal narrowing are well visualized and demonstrated in detail on TruFISP images. The high intraluminal signal seen on these T2-weighted images is highly advantageous for detecting fistulas and sinus tracts, which may otherwise be missed on the T1 sequence because of limited contrast with the surround tissues.39 Motion-related artifacts are minimal on TruFISP images because of the short acquisition time.24,41 TruFISP sequences are also insensitive to intraluminal flow voids—an artifact seen in HASTE imaging because of balanced and symmetric gradient of TruFISP design. Consequently, the use of antiperistaltic drugs to reduce bowel motion can be avoided, giving a major advantage to TruFISP over the other sequences.4
TruFISP Artifacts The most common artifact observed in TruFISP imaging is the black boundary artifact, which appears in voxels in which both fat and water protons are present. This artifact can be easily recognized as a thin “black” line along the outer border of the bowel wall. Black-boundary artifacts can be clearly differentiated from normal small bowel wall and folds and from abnormal bowel wall thickening by its low signal intensity as opposed to the moderate signal intensity of the normal and thickened small bowel wall. It generally does not interfere with the diagnosis of small bowel wall abnormalities and has not been found to cause any significant limitations.42
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HASTE Sequences The T2-weighted sequences are generated by rapid acquisition and relaxation enhancement, with ultrafast acquisition time, usually in the order of seconds. The names of these sequences are manufacturer-dependent, including the HASTE and the SSFSE sequences. On heavily T2-weighted images, actively inflamed bowel wall is edematous and seen as high T2 signal. In the quiescent stage of the disease, the wall signal intensity decreases to reflect underlying fibrosis. Fat-suppression techniques can be helpful in T2-weighted images by increasing the conspicuity of high signal intensity in the bowel wall against adjacent fat saturated mesenteric fat in areas of active inflammation.43 Excellent correlation between biological activity and T2-weighted wall signal intensity has been found.44 The images produced by this technique are highly resistant to magnetic susceptibility and chemical shift artifact.
HASTE Artifacts The long TE in combination with the single-slice acquisition makes the HASTE sequence sensitive to motion artifact and flow artifact. Flow artifact is caused by intestinal peristalsis. Intraluminal flow void can be seen as areas of low signal intensity within the bowel lumen. This appearance can be problematic in the evaluation of potential intraluminal masses. The administration of glucagon reduces bowel peristalsis and can reduce or eliminate flow artifact and provides homogeneous luminal opacification.39 The HASTE sequence has poor soft-tissue contrast45 and does not provide sufficient information regarding the mesentery39 because of k-space filtering effects.46 Mesenteric structures are better visualized on the TruFISP sequence than on the single-shot HASTE sequence.
Advantages, Disadvantages, and Importance of Each Technique Conventional Imaging Versus MR Enteroclysis Until recently conventional imaging was considered the gold standard for small bowel investigation against which all new modes of investigation were assessed. Several studies have found MR enteroclysis to be superior to CE.4,47-49 In a study by Ochsenkuhn et al48 comparing CE and MR enteroclysis assessment of Crohn’s terminal ileitis, with endoscopy and histology as baseline criteria, MR enteroclysis had superior sensitivity to CE (89% vs 72%). Furthermore, MRI detected proximal lesions in 9 cases missed by CE. In a trial by Rieber et al49 comparing MR enteroclysis with CE in 84 patients with histologic and endoscopic correlation, the sensitivity for diagnosing inflammatory bowel disease was 85.4% for CE vs 95.2% for MR enteroclysis, and the specificity was 76.9% for CE vs 92.6% for MR enteroclysis. MR enteroclysis was found to have the added advantage of better depicting extramural detail. In this study, because none of the abscesses was diagnosed with CE; the sensitivity was 0% for CE, but 77.8% for
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242 MR enteroclysis. Sensitivity for diagnosing fistulae was 17.7% for CE and 70.6% for MR enteroclysis.49
ography had the potential to be used as a radiation-free alternative for the evaluation of patients with CD.54
MR Enteroclysis vs MR Enterography
Limitations of MRI
Enteroclysis can result in a very stressful patient experience. It requires duodenal and/or jejunal intubation and radiation exposure when performed with conventional fluoroscopic guidance. The enterography technique obviates the need for nasoenteric intubation resulting in better patient acceptance. Ideally the use of an adequate volume of oral contrast, consumed in a constant manner in enterography should provide adequate small bowel luminal distension and obviate the need for enteroclysis and the invasive component of the enteroclysis technique. In a study by Masselli et al50 comparing MR enteroclysis and MR enterography (MR per OS), enteroclysis offered statistically significantly superior small bowel distension only in the jejunum. MR enteroclysis was superior to MR enterography at visualizing superficial abnormalities (P ⬍ 0.01), however all pathologic findings were reliably detected by both techniques. These findings were similar to those in studies by Negaard et al and Schreyer et al. In a study of 40 patients, Negaard et al51 found that bowel distension was inferior with MR enterography (MRI per OS) as compared with MR enteroclysis. However, both methods diagnosed CD with equal sensitivity and a high diagnostic accuracy (sensitivity, specificity, positive predictive values, and negative predictive values: MRI per OS 88%, 89%, 89%, 89%, respectively; MRE 88%, 84%, 82%, 89%) and interobserver agreement (MRI per OS, k ⫽ 0.95; MRE, k ⫽ 1). In a study of 21 patients, Schreyer et al52 found that all pathologic findings seen on CE were seen on MR enterography and MR enteroclysis, with MRI detecting additional information in 6 of 21 patients. Thus, the improved distension at enteroclysis over enterography may not necessarily translate into improved sensitivity and specificity for disease diagnosis. In our institution, we use the enterography technique for all cases, reserving enteroclysis for those not able to tolerate oral contrast, nondiagnostic enterography examinations, problem solving, and further evaluation of those with normal examinations but a high clinical suspicion for small bowel disease.
One of the main limitations of MRI is the inferior spatial and temporal resolution in comparison with CT. Using multidetector CT scanners, 2-3-mm images can be obtained throughout the abdomen in seconds in a single breath-hold. With this improved spatial resolution, multiplanar reformatted images can be generated in various planes. In comparison, the slice thickness for MRI is usually 4-6 mm. However, the improved spatial and temporal resolution of CT over MRI does not necessarily translate into improved sensitivity and specificity. It is not possible to establish the relative diagnostic performances of MRE and CTE from existing published data. The radiologist must determine which imaging modality to use, whether the functional information, soft-tissue contrast, and absence of ionizing radiation that can be obtained with MRI outweigh its inferior spatial and temporal resolution.
Computed Tomography vs MRI Only a few published studies have compared CT and MRI. In a study by Low et al53 comparing contrast-enhanced MRI and single-phase helical CT scanning in 26 patients with CD, MRI depicted 80%-85% of abnormal segments, as compared with 60%-65% by CT. Moderate and marked disease was shown equally well on CT and MRI, but for mild disease MRI detected 68%-79% of the abnormal segments, as compared with 32%-46% by CT. There was no significant difference in complication detection (fistulas, phlegmon, or abscess) between MR and CT.53 In a recent study comparing CT enterography, MR enterography, and SBFT in the assessment of CD of the small bowel, MR enterography had a diagnostic effectiveness comparable with of CT enterography, and both were superior to SBFT. This study concluded that MR enter-
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