Pediatric Imaging Pictorial Essay
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1 Pediatric Imaging Pictorial Essay Chalian et al. MR Enterography of IBD in Pediatric Patients Pediatric Imaging Pictorial Essay Majid Chalian 1 Arzu Ozturk 1 Maria Oliva-Hemker 2 Scott Pryde 1 Thierry A. G. M. Huisman 1 Chalian M, Ozturk A, Oliva-Hemker M, Pryde S, Huisman TAGM Keywords: Crohn disease, inflammatory bowel disease, MR enterography, pediatric imaging, ulcerative colitis DOI: /AJR Received August 11, 2010; accepted after revision November 13, Department of Radiology, Division of Pediatric Radiology, Russell H. Morgan Department of Radiology and Radiological Science, Johns Hopkins Hospital, 600 N Wolfe St, Nelson, B-173, Baltimore, MD Address correspondence to T. A. G. M. Huisman (thuisma1@jhmi.edu). 2 Division of Pediatric Gastroenterology and Nutrition, Johns Hopkins Hospital, Baltimore, MD. WEB This is a Web exclusive article. AJR 2011; 196:W810 W X/11/1966 W810 American Roentgen Ray Society MR Enterography Findings of Inflammatory Bowel Disease in Pediatric Patients OBJECTIVE. The purpose of this article is to illustrate and describe the characteristic MR enterography findings in children with inflammatory bowel disease (IBD) and to present MR enterography as the first-choice imaging modality in this setting. CONCLUSION. Given its high sensitivity and specificity for IBD and lack of ionizing radiation, MR enterography is a valuable technique for examining children with IBD. I nflammatory bowel diseases (IBDs) including Crohn disease and ulcerative colitis are chronic inflammatory diseases of the gastrointestinal tract with extraintestinal manifestations. IBD has been reported to have an overall prevalence of 16.6 cases per 100,000 children and 5.3 cases per 100,000 children younger than 16 years old. Crohn disease is twice as common in children as ulcerative colitis [1 3]. Endoscopy has been considered the gold standard for diagnosing IBD; however, endoscopy provides little access to the small bowel, is limited for identifying extraluminal lesions, and has low patient compliance especially in the pediatric population [4]. CT has proven its value for the evaluation of IBD especially because this cross-sectional imaging technique allows identification of both intra- and extraluminal lesions and complications. The high radiation dose limits its use in the pediatric population. It is well known that children are more vulnerable to the effects of ionizing radiation than adults [5] and are more at risk to experience the late effects of ionizing radiation because of their longer life expectancy, especially because IBD is a chronic disease that may require multiple follow-up examinations. Consequently, MRI seems to be exquisitely well suited for the diagnostic workup of children with IBD because of its complete lack of ionizing radiation. In addition, the various anatomic (T1- and T2-weighted sequences) and functional (diffusion-weighted sequences) image contrasts that can be generated by MRI may give additional valuable information. Until recently, MRI was limited by long acquisition times and a lack of oral contrast agents that could adequately distend the bowel. Water may be used as a cheap and safe biphasic (T1 hypointense, T2 hyperintense) endoluminal contrast material; however, the progressive resorption of water results in inadequate distention of the frequently affected distal ileum. With the development of fast T1- and T2-weighted MRI sequences and hyperosmolar biphasic (i.e., T1 hypointense, T2 hyperintense) oral contrast agents (e.g., barium preparation [VoLumen, Bracco Diagnostics] or polyethylene glycol), high-resolution images of the bowel can now be acquired. The simultaneous IV injection of glucagon further enhances image quality because bowel motion is suppressed. Consequently, MR enterography is the imaging modality of choice for the initial and follow-up evaluation of children with IBD [6]. MR enterography provides superior soft-tissue contrast, renders multiple imaging contrasts, can be acquired in multiple planes, gives an excellent depiction of fluid and edema, allows accurate differentiation of inflammatory strictures from fibrostenotic strictures [7], and has a high sensitivity for detecting mucosal changes [8]. Preliminary studies have shown that MR enterography has a sensitivity and specificity for IBD similar to CT enterography and is more sensitive for IBD than small-bowel follow-through studies [6]. In addition, MR enterography is preferred by patients because it causes less abdominal discomfort and nausea [9, 10]. The aim of this article is to show the characteristic MR enterography findings of IBD and to highlight the role of MR enterography W810 AJR:196, June 2011
2 MR Enterography of IBD in Pediatric Patients for detecting gastrointestinal IBD findings in children. MR Enterography Technique Biphasic hyperosmolar endoluminal contrast agents such as VoLumen (10 ml/kg of body weight) are used for optimal bowel distention. Although studies have reported even better controlled bowel distention by administering the oral contrast agent through a nasogastric or nasojejunal tube, oral application should be favored in children to optimize patient compliance [9, 10]. Adequate filling of the bowel by oral contrast material also reduces bowel motion and endoluminal air and gas. No special dietary preparation is necessary. Patients are imaged in the prone position because the bowel loops are closer to the imaging coil, air moves to a more posterior location, small-bowel loops are better separated from each other, and motion artifact including respiratory-related motion is reduced. A combination of fast axial and coronal T1- and T2-weighted sequences should be used to cover the entire gastrointestinal tract. Typically fat-saturated thin-sliced T2-weighted true fast imaging with steady-state precession (FISP) sequences (slice, 3 4 mm; interslice gap, 10%; field of view [FOV], mm; matrix, ; TR range, ms; TE, shortest) and 3D T1-weighted fatsaturated unenhanced and contrast-enhanced gradient-echo sequences (slice, mm; interslice gap, 10%; FOV, mm; matrix, ) are acquired. The FOV and matrix were optimized for each individual patient on the basis of body size. Ultrafast true FISP sequences reduce motion artifacts because of the short acquisition times. The fat-saturation technique increases contrast resolution by reducing the chemical shift induced black boundary artifacts along the bowel wall. Injection of IV gadolinium based contrast agents further increases detection of active inflammation. IV glucagon improves image quality because bowel motion is suppressed. No parasympatholytic agent was administered to further decrease bowel motion. Normal Appearance of the Bowel on MR Enterography A normal bowel wall is uniformly thin and exhibits moderate T1 and T2 signal intensity on true FISP images (Fig. 1). The cutoff value for differentiating between a normal and a thickened bowel wall is 3 mm [6]. True FISP sequences display mesenteric lymph nodes and vessels with low signal intensity surrounded by hyperintense mesenteric fat. Mesenteric nodes smaller than 5 mm measured along their short axis are considered physiologic [7]. On contrast-enhanced sequences, normal mucosa shows mild to moderate enhancement with intact layering and stratification of the mucosa, submucosa, and muscularis propria. The mesenteric fat is hypointense on fat-saturated sequences and outlines the bowel sharply. Features of IBD on MR Enterography Bowel Wall Thickening A bowel wall thickness of greater than 3 mm is considered pathologic [6]. Affected inflamed bowel segments typically show T1 hypointense and T2 hyperintense mucosalsubmucosal edema with matching contrast enhancement (Figs. 2 5). In patients with Crohn disease, skip lesions may be observed; skip lesions are characterized by multiple simultaneously occurring separate lesions (Fig. 5). In patients with ulcerative colitis, the wall thickening extends retrograde from the anus to the rectum, colon, or small bowel. This pattern of retrograde extension is specific for ulcerative colitis (Figs. 3 and 4). Mural Stratification Mural stratification relates to the differential or layered enhancement pattern of the various bowel wall layers that may be interrupted depending on the degree and kind of inflammation and fibrosis. In Crohn disease, inflammation extends across all bowel layers, resulting in the loss of bowel layering, whereas in ulcerative colitis the inflammation is limited to the mucosa (Figs. 2 5). Cobblestones Typically in ulcerative colitis and less frequently in Crohn disease, aphthous ulcers may be seen along the inflamed mucosa. In advanced cases of IBD, lesions enlarge and become confluent to form deep linear or stellate ulcerations with bulging of the edematous residual mucosa. Comb Sign Extension of inflammation beyond the serosa of the bowel, typical of Crohn disease, and the resulting increased mesenteric vascularity result in the typical comblike signal alteration. This comb sign is well seen on fatsaturated sequences (Fig. 5). Fibrofatty Proliferation Fibrofatty proliferation, also known as creeping, refers to fatty deposition along the mesenteric border of inflamed bowel segments. It appears as blank space separating adjacent bowel loops (Fig. 5). Especially in children this finding might be particularly striking [11]. Fibrofatty proliferation is highly suggestive of Crohn disease [12]. Strictures and Stenosis Chronic IBD affected bowel segments may become stenotic. Stenosis may be anatomic or functional because of hypoperistalsis. The affected bowel segment does not extend adequately despite the presence of endoluminal contrast material, and mild to moderate dilatation of more proximal bowel loops is frequently noted (Figs. 2, 3, and 5). Stenosis is also suggested if the degree of distention of an affected bowel segment remains unchanged during the examination. Mesenteric Lymph Nodes Reactive mesenteric lymph nodes are easily depicted on T1- and T2-weighted sequences as grapelike nodular soft-tissue lesions surrounded by mesenteric fat (Fig. 6). Mesenteric nodes larger than 5 mm in diameter, especially if clustered and enhancing, indicate active inflammation [13]. Fistula Patients with Crohn disease and those with ulcerative colitis may have a simple or complex perianal fistula that may extend through the various layers of the internal and external sphincter complex. In addition, enteroenteric, enterocolic, enterocutaneous, or enterovesical fistulas may be seen in Crohn disease (Figs. 7 and 8). Fistulas are typically seen where two inflamed bowel segments are in close proximity to each other or in regions of high-grade stenosis. Typically the fistulous tract will show strong enhancement and may be filled with oral contrast material. Incidental Findings The major advantage of MR enterography is that not only the bowel lumen, bowel wall, and immediate paraintestinal structures are visualized, but also the entire abdomen is displayed. Extraintestinal findings may include a psoas abscess (Fig. 9), sacroiliitis, or vasculitis with aneurysm formation. In addition, various incidental findings may be seen that mimic IBD disease such as appendicitis (Fig. 10), spondylitis, or even pregnancy (Fig. 11). Conclusion MR enterography provides excellent bowel detail without the need for ionizing radia- AJR:196, June 2011 W811
3 Chalian et al. tion. MR enterography allows study of acute or chronic bowel wall inflammation, its early and late complications, extraintestinal disease, and possible incidental findings that may mimic IBD. MR enterography is especially valuable in children who may undergo multiple imaging studies during the course of their life-long disease and are highly sensitive to the deleterious effects of radiation. MR enterography should be the primary cross-sectional imaging modality in children evaluated for IBD. CT should be considered only if there are absolute contraindications for an MRI examination (e.g., pacemaker). A References 1. Cosgrove M, Al-Atia RF, Jenkins HR. The epidemiology of paediatric inflammatory bowel disease. Arch Dis Child 1996; 74: Hyams JS. Inflammatory bowel disease. Pediatr Rev 2000; 21: Sawczenko A, Sandhu BK, Logan RF, et al. Prospective survey of childhood inflammatory bowel disease in the British Isles. Lancet 2001; 357: Horsthuis K, Bipat S, Stokkers PC, Stoker J. Magnetic resonance imaging for evaluation of disease activity in Crohn s disease: a systematic review. Eur Radiol 2009; 19: Palmer L, Herfarth H, Porter CQ, Fordham LA, Sandler RS, Kappelman MD. Diagnostic ionizing radiation exposure in a population-based sample of children with inflammatory bowel diseases. Am J Gastroenterol 2009; 104: Leyendecker JR, Bloomfeld RS, DiSantis DJ, Waters GS, Mott R, Bechtold RE. MR enterography in the management of patients with Crohn disease. RadioGraphics 2009; 29: Lawrance IC, Welman CJ, Shipman P, Murray K. Correlation of MRI-determined small bowel Crohn s disease categories with medical response and surgical pathology. World J Gastroenterol 2009; 15: Rimola J, Rodriguez S, García-Bosch O, et al. B Magnetic resonance for assessment of disease activity and severity in ileocolonic Crohn s disease. Gut 2009; 58: 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 2007; 17: Negaard A, Sandvik L, Berstad AE, et al. MRI of the small bowel with oral contrast or nasojejunal intubation in Crohn s disease: randomized comparison of patient acceptance. Scand J Gastroenterol 2008; 43: Sheehan AL, Warren BF, Gear MW, Shepherd NA. Fat-wrapping in Crohn s disease: pathological basis and relevance to surgical practice. Br J Surg 1992; 79: Hara AK, Swartz PG. CT enterography of Crohn s disease. Abdom Imaging 2009; 34: Koh DM, Miao Y, Chinn RJ, et al. MR imaging evaluation of the activity of Crohn s disease. AJR 2001; 177: Fig. 1 Crohn disease. A and B, Coronal T2-weighted MR image of 12-yearold boy (A) and contrast-enhanced T1-weighted MR image of 14-year-old girl (B) with confirmed Crohn disease. Oral biphasic contrast material (T2 hyperintense, T1 hypointense) is seen within distended bowel loops. On T2-weighted image, bowel loops are evenly distributed throughout abdomen; are adjacent to each other; and are not abnormally separated by, for example, increased amount of fat. T2 hypointense bowel wall can easily be seen and measures 1 2 mm in thickness. On T1-weighted image, endoluminal contrast material is T1 hypointense and bowel wall is T1 hyperintense because of contrast enhancement. In right lower abdomen, terminal ileum shows mild wall thickening with increased contrast enhancement of bowel wall; these findings are consistent with terminal ileitis. Colon is filled with moderately intense mixture of stool and fluid. Stomach is filled with hypointense fluid. Liver is without focal lesions. W812 AJR:196, June 2011
4 MR Enterography of IBD in Pediatric Patients Fig. 3 Axial fat-saturated T2-weighted image (top), T1-weighted image (middle), and contrast-enhanced fat-saturated T1-weighted MR image (bottom) of 17-year-old girl with confirmed ulcerative colitis. Wall of sigmoid colon is mildly thickened, with increased T2 hyperintensity and contrast enhancement of inflamed mucosa. Adjacent fat is unremarkable; inflammatory process is limited to mucosa. Fig. 4 Coronal fat-saturated T2-weighted image (top), T1-weighted image (middle), and contrastenhanced T1-weighted image (bottom) of rectum of 17-year-old girl with confirmed ulcerative colitis. Affected rectal wall is thickened and T2 hyperintense with significant wall enhancement. Biphasic endoluminal contrast material distends lumen, thereby facilitating diagnosis. No signs of stranding of adjacent fat are seen. Fig. 2 Axial contrast-enhanced CT image (top left), axial contrast-enhanced T2-weighted MR image (top right), unenhanced fat-saturated T1-weighted MR image (bottom left), and contrast-enhanced fatsaturated T1-weighted MR image (bottom right) of 11-year-old boy with confirmed Crohn disease. CT image reveals long ileal segment with moderate wall thickening and narrowed lumen within small pelvis. On T2-weighted image and especially on contrastenhanced T1-weighted images, various layers of bowel wall can be differentiated from one another in better detail than on CT study. Mucosa is significantly thickened (edematous) and T2 hyperintense, with increased contrast enhancement compatible with active inflammation. In more proximal segment, transmural extension of inflammation obscures various layers of bowel wall. Transmural extension is characteristic of Crohn disease. Bowel lumen is moderately narrowed and can easily be identified by endoluminal biphasic T1 hypointense and T2 hyperintense oral contrast material. AJR:196, June 2011 W813
5 Chalian et al. Fig. 5 Axial fat-saturated contrast-enhanced T1- weighted MR images (top and middle) and subtraction image (bottom) of 17-year-old girl with confirmed Crohn disease. Prominent wall thickening and increased contrast enhancement of multiple segments of distal ileum are seen; these findings are best seen on subtraction images and are consistent with Crohn disease. Bowel lumen is mildly narrowed. Increased amount of fat that is seen along and between inflamed bowel segments is known as fibrofatty proliferation. Multiple mildly dilated mesenteric vessels due to reactive hyperemia are noted. Vessels are orientated in plane perpendicular to bowel wall resembling teeth of comb (comb sign). Fig. 6 Coronal fat-saturated T2-weighted MR images of 14-year-old girl with active Crohn disease affecting terminal ileum. Multiple subcentimeter T2 hyperintense mesenteric lymph nodes (arrowheads) are seen along mesenteric vascular pedicle. Lymph nodes are outlined by hypointense mesenteric fat. Mild thickening of bowel wall (arrows) is noted in region of terminal ileum. W814 AJR:196, June 2011
6 MR Enterography of IBD in Pediatric Patients A Fig year-old boy with confirmed Crohn disease. A, Axial T2-weighted (top) and contrast-enhanced fat-saturated T1-weighted (middle and bottom) MR images show conglomerate of distal ileal loops within right lower abdomen. Significant wall thickening is noted with loss of bowel wall stratification and intense contrast enhancement. Lumen is highly stenotic; minimal amount of T1 hypointense oral contrast material is seen within bowel lumen. Affected bowel loops appear to be adherent to each other and reach adjacent bladder. Stranding of adjacent mesenteric fat and comb sign indicate transmural extension of inflammatory process. B, Coronal oblique fat-saturated T2-weighted MR image reveals fistulous tract (arrows) connecting inflamed distal ileal loop with urinary bladder. T2 hyperintense oral contrast material is noted within fistulous tract; urinary bladder wall is focally thickened. Extension of fistulous tract into bladder was confirmed by endoscopy. Fig. 8 Axial fat-saturated contrast-enhanced T1-weighted MR image of 11-year-old boy with confirmed Crohn disease. Comma-shaped, peripherally enhancing perianal abscess related to transsphincteric fistula is noted. Mild stranding of adjacent perianal fat is also noted. B AJR:196, June 2011 W815
7 Chalian et al. Fig. 10 Axial fat-saturated contrast-enhanced T1- weighted MR images of 16-year-old boy with confirmed Crohn disease show mildly thickened appendix with T1-hypointense fluid within lumen of appendix suggestive of appendicitis (arrows). No focal abscess is seen. In addition, contrast-enhancing, thickened, and mildly stenotic distal ileal bowel loops are noted. Mild fibrofatty proliferation is seen along inflamed bowel loops. Fig. 11 Axial fat-saturated contrast-enhanced T1- weighted (top) and fat-saturated T2-weighted (bottom) MR images of 17-year-old girl with confirmed Crohn disease and increasing symptoms of nausea and vomiting. MR findings exclude active inflammation; however, unexpected 2- to 4-week-old intrauterine pregnancy (arrows) is noted. A B Fig year-old girl with confirmed Crohn disease. A, Axial fat-saturated contrast-enhanced T1- weighted MR image shows conglomerate of strongly enhancing, stenotic distal ileal loops in right abdomen with complete loss of wall stratification. Bowel loops in left abdomen appear unremarkable. B, Coronal fat-saturated T2-weighted image (left) and coronal contrast-enhanced fat-saturated T1-weighted images (middle and right) show classical rightsided psoas muscle abscess. Abscess is centrally filled with T2 hyperintense, T1 hypointense pus surrounded by contrast material enhancing thick pseudocapsule (short arrow). In addition, edematous T2 hyperintense swelling of psoas muscle (arrowheads) is seen. Conglomerate of contrast material (long arrows) enhancing inflamed mesenteric lymph nodes and bowel loops is seen in region of terminal ileum. Right kidney is mildly obstructed, likely because of inflammatory reaction or involvement of right ureter. W816 AJR:196, June 2011
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