Chapter Outline
Small bowel radiology has undergone dramatic changes in the past 2 decades. Despite recent advances in small bowel endoscopy and video capsule technology, radiologic imaging remains an important means of evaluating patients with suspected or established small bowel disease. Cross-sectional imaging techniques are used to investigate extraluminal abnormalities and intraluminal changes and have gradually replaced barium contrast examinations for many indications.
Magnetic resonance imaging (MRI) has many properties that make it well suited to imaging of the small bowel, such as the lack of ionizing radiation, improved tissue contrast that can be achieved by using a variety of pulse sequences, and the ability to perform real-time functional imaging. Moreover, MR modalities allow visualization of the entire bowel without overlapping bowel loops as well as the detection of intra- and extraluminal abnormalities. These morphologic MR findings, combined with contrast enhancement features and functional information, help make an accurate diagnosis and consequently characterize small bowel diseases. These features dramatically change the image interpretation process. Radiologists must focus on morphologic findings and functional data of small bowel motility to exploit MR capabilities fully. Optimal distention of the small bowel loops is crucial for the correct evaluation of the bowel wall because collapsed bowel loops may hide lesions or mimic disease by mistakenly suggesting that the collapsed segments are actually an abnormality-related thickened bowel wall.
Two main techniques have been used to achieve small bowel distention, MR enteroclysis with infusion of the contrast material through a nasojejunal tube and MR enterography with oral administration of contrast material. There is a general preference among radiologists for performing enterography over enteroclysis; however, this preference is controversial. MR enteroclysis is known to provide better depiction of endoluminal lesions in the small intestine than that achieved at MR enterography performed with an oral contrast agent. It is also generally acknowledged that MR enteroclysis provides optimal small bowel distention and allows more accurate detection of strictures. However, nasoenteric intubation for MR enteroclysis may cause patient discomfort, and it involves various technical and logistical difficulties, as well as exposure to radiation. MR enteroclysis performed with the continuous administration of an enteric contrast agent is not possible at all facilities.
Although Crohn’s disease is the primary indication for MR enterography because many patients require multiple follow-up imaging examinations, MR enterography is performed with increasing frequency for the evaluation of other small bowel diseases. MR imaging offers detailed morphologic information and functional data of small bowel disease, thereby allowing the diagnosis of early or subtle structural abnormalities and guiding patient therapy.
Technical Considerations
Enteral Contrast Agents for Magnetic Resonance Imaging
A number of enteral agents have been proposed for use in small bowel MR imaging. The most important features of enteral contrast agents include uniform and homogeneous opacification, adequate distention of the small bowel lumen, high contrast between the lumen and small bowel, low cost, and absence of serious adverse side-effects.
There are three main groups of enteral agents. The signal intensity that results from their use varies according to the pulse sequence used. Positive contrast enteral agents, which yield high signal intensity on T1-weighted images, include gadolinium chelates, manganese ions, ferrous ions, and foods such as blueberry juice. Although these enteral agents can show mural thickening on T1-weighted images, they inevitably are limited regarding the detection of more subtle mucosal or wall hyperenhancement after the intravenous injection of gadolinium-based contrast material. Consequently, their routine use is not recommended.
Negative contrast enteral agents, which yield low signal intensity on T2-weighted and especially T2*-weighted images, constitute solutions with superparamagnetic iron oxides (SPIOs), including nanoparticles of maghemite in bentonite matrix, and ultrasmall SPIOs (USPIOs). Currently, the only negative contrast agent commercially available in the United States is ferumoxsil oral suspension, which is used in MR cholangiopancreatography to reduce the signal from surrounding bowel. The high signal intensity of inflammation in the bowel wall and in the surrounding fat may be more conspicuous on T2-weighted images obtained with a negative contrast agent because of the greater contrast achieved between the high signal intensity of inflammation and the low signal intensity of the lumen. Side effects (observed in 5% to 15% of cases) associated with these enteral agents include poor palatability of the agent, nausea, vomiting, and rectal leakage. Moreover, the low signal intensity of intraluminal contrast on T2-weighted images and associated susceptibility effects may reduce the conspicuity of the normal small bowel wall, low signal intensity lesions, such as carcinoid tumors, and intraluminal abnormalities.
The third group of agents are biphasic enteral contrast agents, which have been most widely tested and are most commonly used for MR enteroclysis and MR enterography. They produce low signal intensity on T1-weighted images and high signal intensity on T2-weighted images. The low signal intensity of these agents on T1-weighted images improves the contrast between the bowel lumen and hyperenhancing mural inflammation or masses after intravenous administration of contrast material ( Fig. 40-1 ). The marked contrast between the lumen and dark bowel wall on T2-weighted images improves the detection of endoluminal abnormalities and more effectively highlights transmural ulcers. Commercially available biphasic enteral agents include water, polyethylene glycol, barium sulfate (VoLumen; E-Z-Em/Bracco, Lake Success, NY), and nonosmotic agents such as locust bean gum and methylcellulose. Polyethylene glycol is a high-osmolar, nonabsorbed, nonfermented contrast medium that has been shown to provide excellent intraluminal contrast and luminal distention, although this enteral agent may cause mild diarrhea. Barium sulfate, an enteral contrast agent that contains sorbitol, whose osmotic properties cause it to retain water, has also proved to be effective. Barium sulfate and water–polyethylene glycol solution are both superior to plain water and water-methylcellulose solution for achieving optimal small bowel distention.
Technique
Optimal distention of the small bowel loops is crucial for the correct evaluation of the bowel wall. This is because collapsed bowel loops may obscure lesions or mimic disease by mistakenly suggesting that the collapsed segments are actually an abnormality-related thickened bowel wall.
MR enteroclysis has been shown to depict early disease and the number of involved segments more accurately, whereas enterography is more time-efficient for radiologists and other staff because nasojejunal tube placement is not required. Although jejunal distention is frequently suboptimal, the ileum, which is the most common site of small bowel involvement in Crohn’s disease and the region of most interest to clinicians, is usually well depicted. Enterography also eliminates radiation exposure and the technical and logistical difficulties of nasojejunal tube insertion, and it removes a potential barrier to patient compliance with future examinations.
Enterography techniques require the ingestion of a large amount of fluid that fills the stomach and small bowel. 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 ; a volume of 1350 to 1500 mL is adequate in most cases.
Although rapid transit (<20 minutes) to the right colon has been observed, there is a delay of at least 40 to 60 minutes from contrast material ingestion to imaging in most patients. Although some authors advocate imaging the patient twice (e.g., after 20 minutes for optimal visualization of the distended jejunum and after 45 minutes for the ileum), a single acquisition performed 40 minutes after the ingestion of oral contrast material is effective and practical in terms of patient compliance and efficient time use of the MR imager.
Magnetic Resonance Imaging Protocol and Pulse Sequences
A preprocedural fast of 4 hours is recommended because fasting reduces the amount of food residue and debris in the intestinal lumen, which may mimic mass lesions or polyps. Patients are imaged in the supine or prone position. The prone position helps separate bowel loops, provide maximal bowel coverage on coronal images, and decrease the imaging volume. Although the prone position does offer better distention, it does not translate to better lesion detection. The supine position affords greater patient comfort and is indicated for patients with abdominal pain, stomas, and/or abdominal wall fistulas.
For the MR enterography protocol, an initial thick slab T2-weighted MR cholangiopancreatographic study helps assess small bowel distention. If there is inadequate distention of the ileum, the patient can return to the waiting room to drink more oral contrast material. The MR technical protocol is shown in Table 40-1 .
| Parameter | True FISP | T2-Weighted Half-Fourier RARE | T1-Weighted 3D Vibe | 2D True FISP | ||
|---|---|---|---|---|---|---|
| Axial | Coronal | Axial/Axial Fat-Saturated | Coronal | Coronal/Axial | Coronal and Axial | |
| Repetition time/echo time (msec) | 4.3/2.2 | 4.3/2.2 | 1000/90 | 1000/90 | 4.1/1.1 | 500/75 |
| Flip angle (degrees) | 50 | 50 | 150 | 150 | 10 | 50 |
| Field of view (mm) | 320-400 | 320-400 | 320-400 | 320-400 | 320-400 | 400 |
| Matrix | 256 × 224 | 256 × 224 | 256 × 224 | 256 × 224 | 256 × 224 | 256 × 256 |
| Parallel imaging factor | 2 | 2 | 2 | 2 | 3 | 2 |
| Section thickness (mm) * | 5 | 3 | 4 | 3 | 2.5 | 10 |
| No. of signals acquired | 1 | 1 | 1 | 1 | 1 | 6 |
| Receiver bandwidth (Hz) | 125 | 125 | 62.5 | 62.5 | 62.50 | 1930 |
| Acquisition time (sec) | 19 | 21 | 15-20 | 15-20 | 15-20 | 25 |
Antiperistaltic agents such as hyoscine butylbromide (Buscopan; Boehringer Ingelheim, Ingelheim, Germany) or glucagon (Glucagen; Novo Nordisk, Bagsvaerd, Denmark) are used intravenously to eliminate peristalsis and reduce motion artifact. Achieving reduced peristalsis is of considerable importance for the T1-weighted 3D sequences performed after the administration of intravenous contrast material and may help limit intraluminal flow artifacts on images obtained with the half-Fourier acquisition. I administer an initial 10 mg of hyoscine butylbromide or 0.2 mg of glucagon immediately before the examination starts to reduce intraluminal flow voids. The patient receives an additional dose of the same strength prior to gadolinium-based contrast material injection.
The T2-weighted sequence based on the half-Fourier reconstruction technique, termed half-Fourier RARE (rapid acquisition and relaxation enhancement) or single-shot fast spin-echo , allows each image to be obtained in less than 1 second, minimizing artifacts caused by small bowel peristalsis. They produce high contrast between the lumen and bowel wall, providing excellent depiction of wall thickening and changes in the fold pattern.
Limitations of half-Fourier RARE include its sensitivity to intraluminal flow voids and the fact that it poorly depicts the mesentery because of k space filtering effects, which are related to the combination of a single-shot acquisition and partial Fourier technique. The latter results in selective spatial filtering, leading to the loss of fine details of tissues that exhibit low to moderate T2 relaxation times. The coronal and axial balanced gradient-echo MR images that are obtained yield contrast that is intermediate relative to contrast on T1- and T2-weighted images.
Various acronyms are used to describe the balanced gradient-echo sequences, including fast imaging employing steady-state acquisition (FIESTA), true fast imaging with steady-state precession (FISP), and balanced steady-state free precession, depending on the manufacturer. These pulse sequences are particularly effective as a means of obtaining information about mural and extraintestinal abnormalities. The black boundary artifact encountered at fat-water interfaces with the balanced gradient-echo sequence can be clearly differentiated from abnormal bowel wall thickening because the fat-water interface is of low signal intensity, which contrasts with the moderate signal intensity of the thickened small bowel wall.
Two- or three-dimensional spoiled gradient-echo fat-saturated T1-weighted sequences can be used to acquire contrast-enhanced images. Because contrast-enhanced images acquired with 3D volumetric sequences provide better spatial resolution and allow multiplanar reconstruction, they are preferred with fully cooperative patients. When patients have difficulty in breath holding and remaining still, a 2D T1-weighted sequence, which is less susceptible to motion artifacts but has reduced spatial resolution, may be used instead of the 3D volumetric sequences. Gadolinium-based contrast material is administered by injecting 0.2 mmol/kg of body weight at a rate of 2 mL/sec, followed by a bolus injection of 20 mL of isotonic saline. Coronal gradient-echo fat-saturated T1-weighted sequences are obtained before and 30 and 70 seconds after the injection, followed by an axial sequence beginning 90 seconds after the injection, which covers the entire abdomen. The entire protocol for MR enterography takes 20 to 25 minutes.
Few studies have investigated the role of diffusion-weighted imaging for the detection of bowel inflammation in Crohn’s disease. The apparent diffusion coefficient may facilitate quantitative analysis of disease activity. Visual assessment of diffusion-weighted images may provide greater accuracy, whereas calculation of the apparent diffusion coefficient may facilitate a quantitative analysis of disease activity.
Some authors have demonstrated that inflamed bowel segments have more restricted diffusion compared with normal bowel segments, and have further shown that diffusion-weighted imaging (DWI) is more sensitive than dynamic contrast-enhanced (DCE) MRI for actively inflamed terminal ileum; combining both techniques can potentially improve diagnostic specificity. Other authors have reported a sensitivity, specificity, and accuracy of 86.0%, 81.4%, and 82.4%, respectively, for the detection of disease-active segments. Another study demonstrated restricted diffusion in inflamed portions of the colon in patients with ulcerative colitis, one of which also showed that DWI had similar accuracy to contrast-enhanced sequences for detecting inflamed bowel. The outcomes of these studies suggest an evolving role for DWI in inflammatory bowel disease.
The ultrafast acquisition of the balanced steady-state free precession (SSFP) technique described earlier allows high temporal resolution imaging of the whole length and width of the abdomen in a coronal slice with subsecond repetition times during a single breath-hold. The resulting cine sequence can be used to evaluate small bowel peristalsis visually, and identify areas of altered motility, specifically focal areas of paralysis or hypomotility. Cine MR sequences have been found to detect more specific findings for Crohn’s disease than standard MR enterography and identified significantly more patients with Crohn’s disease than those identified on MR enterography alone. Moreover, cine MRI was a feasible approach for detecting a longitudinal ulcer in small bowel Crohn’s disease, which appeared as asymmetric involvement or mesenteric rigidity with antimesenteric flexibility. More recently, software methods have been developed to assess small bowel motility in an automated manner as well as analyzing the motility quantitatively, suggesting a role for quantified motility in assessing disease activity.
MRI of the small bowel can be performed with a 3-T system, but the higher field strength requires modifications of the pulse sequences that are used at 1.5 T. Higher specific absorption rates because of the long acquisition time needed to obtain axial sections of the entire abdomen with a half-Fourier RARE sequence at 3 T are often a limiting factor. The use of parallel imaging techniques may help reduce the acquisition time and decrease the specific absorption rate, but such reductions are achieved at the expense of the signal-to-noise ratio. The use of FISP sequences is not always feasible at 3 T because of distortion artifacts. However, it is possible to obtain dynamic T1-weighted images at 3 T that have spatial resolution commensurate with that of T1-weighted images obtained at 1.5 T.
Image Interpretation
Initially, MR fluoroscopic sequences are used to assess the grade of distention of the small bowel and provide a panoramic view of the caliber and location of the jejunal and ileal loops. The images are displayed in the cine loop mode to visualize small bowel mobility.
The transit of the polyethylene glycol solution through the small bowel is considered normal when unimpeded flow of intraluminal solution from the duodenojejunal junction to the ascending colon is observed, with no evidence of transit delay or stenosis. Low-grade stenosis is diagnosed when contrast material reaches the site of obstruction without any delay and flows into the loop below the obstruction. In patients with a high-grade partial small bowel obstruction, the arrival of contrast material at the site of obstruction is delayed, and only a minimal amount flows into the collapsed loop beyond the obstruction, thus making it difficult to define the fold pattern. A transition zone between the dilated bowel above and the narrowed bowel below marks the site of any obstruction. MR fluoroscopic pulse sequences yield useful information concerning the distensibility of narrowed areas, facilitate the differentiation of contractions from strictures in the evaluation of prestenotic dilation, evaluate small bowel mobility, and demonstrate findings similar to those seen at barium enema examinations, such as the morphology of the stenosis, which help differentiate among mucosal, submucosal, and extraparietal origins of disease.
Balanced gradient-echo and T2-weighted images are examined to detect the presence of bowel wall thickening. Multiplanar projections can be obtained by alternating between axial and coronal acquisitions.
The main challenge in MR image interpretation is bowel underdistention, which may mimic or mask disease. When mural thickening is consistently observed on images from different sequences and planes, the likelihood of a correct diagnosis increases. A wall thickness more than 3 mm in a properly distended small bowel loop should be regarded as abnormal. The presence of perienteric or mesenteric abnormalities is evaluated; a fat-saturated T2-weighted study can help detect perienteric inflammation and penetration. Gadolinium-enhanced images are obtained to enable detection of any hyperenhancement of the bowel wall. In a narrowed segment, hyperenhancement can be used to differentiate contraction from mural disease. If the enhancement is identical to that of adjacent bowel loops in the same segment, it most likely represents underdistended contracted normal bowel. If there is more mucosal enhancement (mucosal hyperemia) or notably less submucosal enhancement (bowel wall edema), true disease should be suspected. Delayed images may also help distinguish transient contractions from wall thickening.
If hyperenhancement is seen in a bowel wall of normal thickness, it is necessary to differentiate between true disease and artifact. In these cases, it is important to compare the enhancement with that of other loops that are similarly distended, and with that of bowel loops within the same segment, because normal jejunum enhances more robustly than normal ileum.
The enhancement pattern of bowel loops can help differentiate between small bowel diseases. Homogeneous hyperenhancement (white) can be seen in ischemia, inflammatory bowel disease, adhesions, and occasionally in tumors. A hypoenhancing (gray) wall may be seen in inflammatory bowel disease and tumors. Mural stratification (the target pattern) is typically seen in active Crohn’s disease.
Clinical Applications
Crohn’s Disease
The evaluation of chronic inflammatory bowel disease presents several problems. First, it is important to identify the presence of Crohn’s disease and differentiate it from other small bowel diseases. Second, the number, length, and locations of the segments involved in each patient need to be determined. Third, if a stenosis is present, it needs to be classified as inflammatory or fibrous so that the patient can receive appropriate medical or surgical therapy.
Furthermore, if inflammatory activity is present, it is important to distinguish among mild, moderate, and severe disease because medical management differs depending on the disease stage. Fourth, the presence of mesenteric complications, such as abscesses and fistulas, need to be assessed because their presence influences the choice of therapy.
The visualization of early changes of Crohn’s disease, such as ulcerations and subtle wall thickening, is highly dependent on the quality of luminal distention. High-resolution (thin section) true FISP and half-Fourier RARE images can depict early Crohn’s disease changes; for example, an aphthous ulcer appears as a nidus of high signal intensity surrounded by a halo of moderate signal intensity ( Fig. 40-2 ).
Barium contrast enteroclysis and capsule endoscopy are more accurate than MRI as a means of detecting subtle mucosal abnormalities. However, the clinical importance of a mucosal break or a few superficial aphthous lesions is not clear. There is evidence that suggests that up to 13% of healthy asymptomatic individuals may have mucosal breaks and other minor lesions of the small bowel at capsule endoscopy.
Two types of ulcers are seen in Crohn’s disease, superficial aphthoid ulcers and deep fissuring ulcers. Deep fissuring ulcers are more clinically significant. They penetrate the mucosa into the deeper layers of the bowel wall, resulting in submucosal inflammation and edema. On MRI, they appear as thin lines of high signal intensity oriented longitudinally or transversally (fissure ulcers) within a thickened bowel wall ( Fig. 40-3 ).
Sensitivity values for the detection of bowel ulceration in the literature range from 75% to 90%. MRI can also be used to detect minimal disease on the basis of mucosal enhancement of the bowel wall after intravenous injection of contrast medium ( Fig. 40-4 ).
Related posts:
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Perfusion Computed Tomography and Magnetic Resonance Imaging in the Abdomen and Pelvis
Ulcerative and Granulomatous Colitis: Idiopathic Inflammatory Bowel Disease
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