This article addresses the current technique and protocols for magnetic resonance (MR) enterography, with a primary focus on inflammatory bowel disease (IBD) and a secondary detailed discussion of other diseases of the small bowel beyond IBD. A brief discussion of MR imaging for appendicitis is included, but the evaluation of appendicitis does not require an enterographic protocol. The focused key points and approach presented in this article are intended to enhance the reader’s understanding to help improve patient compliance with the MR enterographic studies, overcome challenges, and improve interpretation.
Key points
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Magnetic resonance (MR) enterography is the preferred imaging examination for the evaluation of inflammatory bowel disease (IBD) in children and adolescents, as it provides a comprehensive look at intraluminal and extraluminal pathology without the use of ionizing radiation.
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Bowel distention is one of the important challenges in achieving diagnostic imaging; however, postcontrast imaging, diffusion-weighted imaging (DWI) and cine imaging also play significant roles and provide complementary information, making them important parts of the MR enterography protocol.
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Attempts should be made to identify and subjectively quantify active bowel wall inflammation; active inflammation and fibrosis can coexist in the same narrowed bowel segment.
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MR enterography is useful to evaluate for diagnoses outside of IBD including infections, polyps, tumors, and vascular lesions in the setting of occult gastrointestinal (GI) bleeding.
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It is critical to interpret MR enterographic studies systematically, including evaluation of both normal and abnormal bowel segments. This evaluation is especially important when assessing jejunal disease, as this is an area of many pitfalls and false-positive results.
Introduction
MR enterography has gained momentum during the last decade and has become a standard imaging technique in the evaluation of children with IBD. The sensitivity and specificity of MR enterography have been validated in both adults and children. There has been an emphasis on advancing MR enterography because of the concerns of the effects of cumulative ionizing radiation exposure in this population due to repeated imaging, especially in children. The risks of irradiation and importance of radiation safety in children are well recognized and extensively addressed in the medical literature, Web sites ( www.imagegently.org , www.imagewisely.org ), and other media available to the general public. In many places in North America, MR enterography has replaced conventional GI fluoroscopy and computed tomographic (CT) enterography and has become the first-line imaging test for known or suspected IBD. With the advent of faster MR imaging sequences, improvement in oral contrast agents and patient compliance, and optimization of DWI and functional cine sequences, radiologists are able to provide valuable, accurate information about disease activity and progression to guide medical versus surgical treatment in children with IBD.
Several years ago, authors first described using MR enterography for applications beyond IBD ; however, there are limited data in the literature on the use of MR enterography for non-IBD diseases. One factor driving the expansion of the role of MR enterography among pediatric imagers is the use of MR imaging for appendicitis in children. However, ultrasonography (US) is still the first-line of imaging for assessing appendicitis, and MR imaging protocols for evaluation of appendicitis commonly do not warrant oral or intravenous contrast. In the setting of acute or chronic abdominal pain, US is often the initial examination ordered and may be followed by CT if the clinical question has not been answered. Yet, the multiplanar capability, lack of ionizing radiation, inherent high soft-tissue contrast, and capacity to examine extramural findings make MR enterography an excellent tool for assessing causes of generalized abdominal pain, particularly if thought to relate to the bowel. MR enterography is at present used to assess gastrointestinal tract diagnoses including infections, polyps, masses (tumors), sources of occult GI bleeding such as vascular lesions, and graft-versus-host disease.
In this article, the authors (1) describe the latest techniques, challenges, and tips for performing high-quality MR enterographic examinations; (2) describe the spectrum of findings in IBD, including Crohn disease (CD) and ulcerative colitis (UC); and (3) discuss techniques and applications of MR enterography for non-IBD entities.
Introduction
MR enterography has gained momentum during the last decade and has become a standard imaging technique in the evaluation of children with IBD. The sensitivity and specificity of MR enterography have been validated in both adults and children. There has been an emphasis on advancing MR enterography because of the concerns of the effects of cumulative ionizing radiation exposure in this population due to repeated imaging, especially in children. The risks of irradiation and importance of radiation safety in children are well recognized and extensively addressed in the medical literature, Web sites ( www.imagegently.org , www.imagewisely.org ), and other media available to the general public. In many places in North America, MR enterography has replaced conventional GI fluoroscopy and computed tomographic (CT) enterography and has become the first-line imaging test for known or suspected IBD. With the advent of faster MR imaging sequences, improvement in oral contrast agents and patient compliance, and optimization of DWI and functional cine sequences, radiologists are able to provide valuable, accurate information about disease activity and progression to guide medical versus surgical treatment in children with IBD.
Several years ago, authors first described using MR enterography for applications beyond IBD ; however, there are limited data in the literature on the use of MR enterography for non-IBD diseases. One factor driving the expansion of the role of MR enterography among pediatric imagers is the use of MR imaging for appendicitis in children. However, ultrasonography (US) is still the first-line of imaging for assessing appendicitis, and MR imaging protocols for evaluation of appendicitis commonly do not warrant oral or intravenous contrast. In the setting of acute or chronic abdominal pain, US is often the initial examination ordered and may be followed by CT if the clinical question has not been answered. Yet, the multiplanar capability, lack of ionizing radiation, inherent high soft-tissue contrast, and capacity to examine extramural findings make MR enterography an excellent tool for assessing causes of generalized abdominal pain, particularly if thought to relate to the bowel. MR enterography is at present used to assess gastrointestinal tract diagnoses including infections, polyps, masses (tumors), sources of occult GI bleeding such as vascular lesions, and graft-versus-host disease.
In this article, the authors (1) describe the latest techniques, challenges, and tips for performing high-quality MR enterographic examinations; (2) describe the spectrum of findings in IBD, including Crohn disease (CD) and ulcerative colitis (UC); and (3) discuss techniques and applications of MR enterography for non-IBD entities.
Nomenclature of MR bowel imaging
There are several MR imaging techniques for the bowel: MR enterography (MR imaging after oral contrast ingestion), MR enteroclysis (MR imaging after instilling a large volume of enteric contrast via a nasojejunal tube), and MR colonography (MR imaging performed after rectal and colonic administration of contrast or saline enema). Of these, MR enterography is the most common, practical, and acceptable imaging examination performed in pediatric patients.
Patient preparation
All patients should be given nothing by mouth between 4 and 6 hours before the study. Adequate hydration up to 4 hours before the MR imaging study is recommended to reduce vasovagal reactions, reduce side effects of administered medications and contrast agents (both oral and intravenous [IV]), and facilitate IV line placement. Most patients having an MR enterography examination are adolescents; therefore, sedation is not usually required. However, use of sedation for MR enterography depends on institutional sedation policies, and alternatives to sedation may need to be considered ( Box 1 ).
These are important points to address in conjunction with nursing, technologists, and clinicians
Bowel preparation: No routine bowel cleansing protocol is needed, except in cases for evaluation of colonic polyps
Sedation: Most cases (especially adolescents) do not require sedation. Follow sedation guidelines per institution. Consider (1) patients alternative examination, (2) MR enterography under general anesthesia with airway protection because oral contrast is required, (3) child life involvement, and (4) use of video goggles
Oral contrast type and delivery: Biphasic contrast is ideal and recommended. Continuous drinking during a 45-minute period. Can be given through G-tube if required or nasogastric tube if patient refuses by mouth
Antispasmolytics: Helps improve image quality. May still perform MR enterography without but recommended.
Options outside of the United States: Buscopan (butylscopolamine)
Options in the United States: Glucagon (IV or intramuscular) or hyoscyamine (Levsin) IV or sublingual
For IV glucagon: Slowly inject with adequate saline flush to reduce side effects
Intravenous contrast: Recommended for all MR enterographic examinations. If IV contrast is contraindicated, DWI and fat-saturated T2-weighted imaging can provide valuable information about disease activity
If MR imaging is contraindicated: Alternative examinations such as bowel US or CT enterography should be considered (the former is preferred by the authors)
Contrast: oral, rectal, and intravenous
Although there is no consensus on the optimal oral contrast regimen, the most favorable contrast agents used for MR enterography are biphasic agents (hypointense on T1-weighted and hyperintense on T2-weighted sequences). The literature on pediatric MR enterographic imaging describes use of mannitol, polyethylene glycol, low-concentration barium solution (0.1% weight/volume) with sorbitol (VoLumen [Bracco Diagnostics, Inc.]), and sorbitol alone with flavoring ( Box 2 ). In general, these agents prevent the absorption of water and allow for bowel distention. Patients are encouraged to drink continuously and steadily during a period of 45 to 60 min, with total oral contrast volumes varying from 600 to 1000 mL. Some institutional protocols also include 200 to 240 mL of water in the last 10 to 15 minutes before placing patient on the scanner. One way to improve duodenal and jejunal distention is to ask the patient to lay right side down the last 10 to 15 min before scanning. A study in adult patients performed a head-to-head comparison of oral contrast agents and reported that volumes greater than 1000 mL led to increased cathartic side effects. MR imaging scanning ideally begins within 1 hour from the beginning of contrast ingestion. Rectal contrast in the form of saline enema could be considered in certain cases, including (1) concern of a rectal or colonic stricture and (2) incomplete or inadequate colonic endoscopy. IV contrast is also given for every MR enterography, unless there is a contraindication.
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Provide patient and family education
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Have nursing staff supervise and encourage oral contrast ingestion
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Chill and flavor contrast
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Offer a nasogastric tube for contrast administration early on in a child who is reluctant to drink
VoLumen (Bracco Diagnostics, Inc.), alone or mixed with ferumoxsil iron oxide suspension
Mannitol
Polyethylene glycol (mixed with juice, flavoring)
Sorbitol (mixed with flavoring)
Antiperistaltics and other medications
Antiperistaltics have the advantage of improving the quality of MR enterography examinations by reducing motion from bowel peristalsis. These agents do have significant side effects, most notably nausea and vomiting. These side effects can be limited by slow administration, hydration, and administration of antiemetics. Butylscopamine (Buscopan) is approved for use outside the United States. In the United States, glucagon and hyoscyamine are approved for use. Glucagon, the more common of the 2 medications used in pediatrics, can be given IV or intramuscular, 0.5 to 1.0 mg total. Glucagon can be given in a split dose, half at the beginning of the MR enterographic study and half just before the contrast-enhanced images are acquired. Patients should be thoroughly screened for glucagon by the nursing staff as outlined in the article by Darge and colleagues. Other medications advocated by some anecdotally in adults include metoclopramide and erythromycin, which accelerate gastric emptying, promoting adequate proximal small-bowel filling in the early part of the examination. These are not used in children for MR enterography. Some centers chose not to give antiperistaltic agents, and researchers have described that in these situations the MR enterographic studies can still be diagnostic. However, a recent pediatric study has shown benefits in using IV glucagon, as there was significant improvement in visualization of the bowel wall after IV glucagon was administered in comparison to the same sequence without glucagon.
Technique: positioning, coils, and sequences
Patients can be scanned in the prone or supine position using a multichannel torso or body phased array coil on a 1.5- or 3-Tesla (T) magnet. Anatomic coverage should always include the pelvis but need not include the lung bases or top of the liver. Although not always possible, prone imaging may be useful to separate the bowel loops and help reduce bowel motion. Exceptions to the prone position include presence of an ostomy, recent abdominal surgery, abdominal wall fistula, severe nausea, or if the study is being done under anesthesia. In these exceptional cases and in general, supine imaging with other strategies to reduce motion will yield diagnostic studies and has been shown to have no impact on lesion detection or characterization.
The main sequences of the MR enterographic examination include axial and coronal T2-weighted single-shot fast spin echo (SSFSE) sequences with and without fat suppression, axial and coronal balanced steady state free precession (SSFP) sequences, axial T2-weighted FSE with fat suppression, axial diffusion-weighted echoplanar imaging, and coronal three-dimensional (3D) T1-weighted gradient recalled echo (GRE) imaging with fat suppression ( Box 3 ). After administration of IV gadolinium-containing contrast material (0.1–0.2 mmol/kg), dynamic coronal 3D T1-weighted GRE sequences with fat suppression are obtained in time intervals of 45 to 55, 70, and 180 seconds. These intervals are not standard but are institutional specific. Delayed axial and coronal postcontrast 2D or 3D T1-weighted sequences with fat suppression are acquired following dynamic imaging. Dynamic postcontrast imaging is considered critical by many as it provides temporal information and has been shown to help differentiate active from fibrotic disease. The postcontrast dynamic acquisition also enables better visualization of progressive transmural bowel wall enhancement and bowel stratification seen with active inflammation in IBD. Regarding motion suppression, there are 2 main strategies in addition to using antiperistaltic agents: (1) breath hold techniques when the patient is cooperative and (2) respiratory triggering or navigator gating technique.
Sequences | Advantages & Pathology Depicted | Artifacts |
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Single-shot fast spin-echo (SSFSE/HASTE) |
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Balanced gradient echo (FIESTA/TRUFISP/BTFE) |
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Diffusion-weighted imaging (DWI) |
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Dynamic contrast enhanced 3D T1-SPGR (VIBE/LAVA/eTHRIVE) |
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Cine
Cine sequences are now commonly included in MR enterography protocols. They are acquired as coronal thick slab steady state precession images repeated sequentially from front to back during a period of 2 minutes. The slice thickness can be between 8 and 10 mm, and on average about 18 to 20 images are acquired in each location and can be stacked together to be viewed as 1 acquisition. Cine sequences can be obtained before the first dose of glucagon is given (for single-dose glucagon or split dose protocols), or it can be performed before and after glucagon is given to assess functionality. As this is a fast sequence, there is relative flexibility in its application. The rationale for using cine imaging is to identify abnormal segments of bowel motility. As shown on fluoroscopic barium studies of the small bowel, segments infiltrated by disease, whether infection, inflammation, or tumor, are commonly fixed in place and separated from adjacent bowel loops, and generally do not peristalse normally. Cine can provide added information, especially for equivocal bowel segments, and also aid in the confirmation of true strictures. One study compared cine MR enterographic sequences with conventional sequences in patients with CD and found more abnormal bowel segments with cine than with the standard sequences, but these were not confirmed with histology. The data in this publication are limited, and further studies are needed to validate the utility of this sequence.
Diffusion-weighted imaging
DWI also is becoming a standard part of MR enterography protocols in the pediatric population. DWI is an echoplanar sequence obtained in the axial plane with free breathing or respiratory triggering using anywhere between 3 and 5 b -values. There is no consensus on the ideal b -values to use in clinical practice; however, any combination between 0 and 1000 will yield adequate imaging (the authors use b- values of 0, 200, 500, 800, and 1000). The goal of DWI sequences is to help identify actively inflamed segments of bowel. Active disease demonstrates restricted diffusion (mural areas bright on DWI sequence and low or dark signal on the automatically generated apparent diffusion coefficient [ADC] maps). Early investigation into further refinement of diffusion processing techniques is underway, with the incorporation of intravoxel incoherent motion (IVIM) diffusion procession. By using numerous b -values from low (10–50 mm/s 2 ) to high (800–1000 mm/s 2 ), this processing aims to separate the “background noise” of Brownian motion from true perfusional changes to better detect inflammation. Further work is needed, however, to refine IVIM and bring it into routine clinical practice. Practically, DWI is most useful when there is a questionable area of bowel abnormality; seeing restricted diffusion can increase reader confidence that the bowel segment is truly abnormal. Anecdotally, the authors have found that in rare cases when IV contrast cannot be given to a patient or if there are areas of suboptimal bowel distention, DWI can be helpful. Some investigators have advocated that there is potential for DWI to replace contrast-enhanced sequences.
DWI is a helpful tool when there is less-than-optimal bowel distention or if IV contrast cannot be given to detect areas of active disease.
3-T versus 1.5-T
Imaging with 3-T scanners is advantageous over imaging with 1.5-T magnets because of the increased signal-to-noise ratio; however, the trade-off for the increased signal-to-noise ratio is a concomitant increase in image artifacts. There are limited published data regarding MR enterographic imaging at 3-T. As described by Dagia and colleagues, single-shot fast spin-echo sequences perform well at 3-T. Although the single-shot sequences still demonstrate flow artifacts within the bowel lumen, intramural and extramural pathology is still clearly depicted ( Fig. 1 A ). In the authors’ experience, performing single-shot sequences without fat suppression also helps decrease the artifacts encountered. The balanced SSFP sequences are prone to increased susceptibility artifacts, particularly from air in the bowel, especially the colon (see Fig. 1 B). The pronounced chemical shift artifact at 3-T that occurs at the fat–water interfaces can adversely affect interpretation of bowel-wall pathology either leading to false-negative or false-positive results (see Fig. 1 C–E). There are a few ways to overcome these challenges at 3-T; one is to remove the sequence that is the most problematic (balanced SSFP) as the other sequences can identify the same abnormalities. The second is to optimize the sequences that withstand 3-T and do better at higher field strengths such as DWI and postcontrast imaging. In the authors’ experience, when performing balanced SSFP sequences, increasing the field of view, increasing the number of slices above and below the area of coverage, and maintaining repetition time less than 4.0 ms improve image quality. High-quality cine sequences are feasible at 3-T.
Performance of MR enterography
The conventional gold standard imaging test for small-bowel mucosal involvement in CD is the double-contrast small-bowel barium fluoroscopic enteroclysis with a sensitivity of 93% to 95% and specificity of 92% to 96.5%. The invasiveness of this test, lack of extraluminal information, and use of ionizing radiation, however, make this examination impractical, particularly in pediatric patients. In contrast, MR assessment of IBD has been shown to have a sensitivity of 93.0% and specificity of 92.8%, with MR enteroclysis performing slightly better than MR enterography. A review of the literature shows MR enterography (with no contribution from MR enteroclysis studies) having a sensitivity ranging between 81% and 91% and a specificity between 67% and 89% for diagnosis of IBD.
Normal findings on MR enterography
With optimal distention, normal bowel loops should be closely opposed to each other, not separated or fixed, with normal brisk peristalsis on cine images ( Fig. 2 A ). Abnormal bowel wall thickening (BWT) is generally considered greater than 3 mm; in children, abnormal measurements of bowel wall are defined as BWT greater than 2.5 mm for small bowel and greater than 2 mm for the colon. The jejunum is an area of potential pitfall because the valvulae conniventes are normally more prominent than in other sections of the small bowel and may simulate BWT ( Fig. 2 B). The enhancement of the normal jejunum is greater than that of the normal ileum ( Fig. 2 C). In addition, when underdistended, the normal jejunum may have an apparent wall thickness of up to 7 mm. Another normal finding is the presence of high signal content within the colon on T1-weighted images related to colonic fecal material ( Fig. 2 D). The cause of this high T1 signal in the colon is unclear.
Prominent mesenteric lymph nodes are commonly seen in normal children on CT and MR imaging. Normal lymph nodes have a central fatty hilum, tend to be fewer in number, are localized primarily to the right lower quadrant, and only mildly enhance.
Inflammatory bowel disease
IBD has been reported to affect approximately 16.6 in 100,000 children and 5.3 in 100,000 children younger than 16 years. Studies have demonstrated an increasing incidence of IBD within the United States, Europe, and Asia. UC and CD together encompass most IBD; however, in around 10% of patients, it is categorized as indeterminate.
CD is characterized by asymmetric, granulomatous, and transmural inflammation of the GI tract with periods of remission and relapse. The cause is multifactorial, and evidence suggests that environmental factors may play a significant role. Any portion of the GI tract may be affected, resulting in discontinuous involvement or skip lesions. Onset of the disease is typically in late adolescence or early adulthood. A combination of clinical examination, radiological findings, biochemical investigations, and endoscopic and histologic features is utilized to confirm the diagnosis of CD. Different classification systems of CD have been proposed in an attempt to prognosticate, follow disease status, and facilitate implementation of different treatment strategies. Imaging classification systems have been proposed as well. The following is one such classification system proposed by Maglinte and colleagues, in which CD is divided into 4 subtypes ( Box 4 ).