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DOI:10.2214/AJR.05.0511
AJR 2006; 187:522-531
© American Roentgen Ray Society


Pictorial Essay

MR Enteroclysis of Inflammatory Small-Bowel Diseases

Bart M. Wiarda1, Ernst J. Kuipers2, Martin A. Heitbrink1, Arnoud van Oijen3 and Jaap Stoker4

1 Department of Radiology, Medical Center Alkmaar, Wilhelminalaan 12, 1815 JD Alkmaar, The Netherlands.
2 Department of Gastroenterology and Hepatology, Erasmus University Medical Center, Rotterdam, The Netherlands.
3 Department of Gastroenterology, Medical Center Alkmaar, Alkmaar, The Netherlands.
4 Department of Radiology, Amsterdam Medical Center, University of Amsterdam, Amsterdam, The Netherlands.

Received March 23, 2005; accepted after revision May 29, 2005.

 
Address correspondence to B. M. Wiarda.


Abstract
Top
Abstract
Introduction
MRI Technique
Normal Appearance
Crohn's Disease
Other Inflammatory Small-Bowel...
References
 
OBJECTIVE. MR enteroclysis has been introduced in the workup of small-bowel diseases. The major advantage of this technique over others is the combined visualization of luminal, mural, and extramural abnormalities. In this article we propose an MR enteroclysis protocol, present a stepwise approach for evaluation of these examinations, and discuss the different inflammatory conditions that can be detected.

CONCLUSION. MR enteroclysis can be considered the current first-line imaging technique for inflammatory small-bowel disorders.

Keywords: enteroclysis • gastrointestinal radiology • inflammatory bowel disease • MRI • small bowel


Introduction
Top
Abstract
Introduction
MRI Technique
Normal Appearance
Crohn's Disease
Other Inflammatory Small-Bowel...
References
 
MRI with enteroclysis can be used as the initial imaging method for small-bowel diseases. The enteroclysis technique enables optimal distention of the small bowel, which results in accurate visualization of stenoses and obstructions [1]. The high-volume-induced reflex atony leads to well-defined visualization of the bowel wall almost without peristalsis-induced artifacts. MR enteroclysis has shown excellent correlation with conventional enteroclysis in grading small-bowel obstruction and functional information while also providing transmural and extramural visualization [2].


MRI Technique
Top
Abstract
Introduction
MRI Technique
Normal Appearance
Crohn's Disease
Other Inflammatory Small-Bowel...
References
 
After placement of a nasoduodenal catheter under fluoroscopy, the small-bowel is distended with 1,000-3,000 mL of methylcellulose (0.5%) and water solution using an electric infusion pump (Roentgen Contrast Mittel Pumpe, Nicholas), located outside the scanner room, at an infusion rate of 80-200 mL/min. The MR protocol (Table 1) consists of MR fluoroscopy using a thick-slab 50-mm coronal HASTE sequence with fat saturation, starting at the beginning of the infusion and repeated every 8 seconds during normal breathing. This allows for the study contrast passage speed, luminal distention, peristalsis, and retrograde filling of the stomach. Subsequently, every 5 minutes, depending on the degree of distention observed from the HASTE images, coronal and axial true fast imaging with steady-state precession (FISP) sequences with fat saturation are performed with a slice thickness of 5 mm to study morphologic changes. Finally, with maximal distention, multislice HASTE images with fat saturation and unenhanced and enhanced (0.1 mmol/kg gadolinium) coronal and axial fast low-angle shot (FLASH) 2D images with fat saturation are obtained 60 seconds after contrast injections are made.


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TABLE 1: MR Protocol of MR Enteroclysis

 


Normal Appearance
Top
Abstract
Introduction
MRI Technique
Normal Appearance
Crohn's Disease
Other Inflammatory Small-Bowel...
References
 
The coronal thick-slab HASTE images give valuable information, both for identifying fixed bowel loops and luminal stenosis and for timing of morphologic sequences with optimally distended bowel loops (Figs. 1A, 1B, 1C, and 1D). The higher spatial and contrast resolution of the morphologic series facilitates evaluation of surface structures (e.g., folds, ulcerations), bowel wall morphology, and thickness and extramural abnormalities (e.g., lymphadenopathy, increased mesenteric vascularization, and abscess) (Fig. 2). Bowel wall thickness larger than 3 mm must be considered abnormal [3]. We used morphologic sequences to identify and localize abnormalities. Enhanced T1-weighted fat-saturation series are used to establish enhancement of the abnormalities and evaluate disease activity, especially in Crohn's disease.


Figure 1
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Fig. 1A 63-year-old woman with suspected Crohn's disease. Coronal thick-slab HASTE fat-saturation image shows adequate distention of jejunal loops (arrowheads) but collapsed or stenotic terminal ileum (arrow).

 

Figure 2
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Fig. 1B 63-year-old woman with suspected Crohn's disease. Coronal true fast imaging with steady-state precession (FISP) fat-saturation image obtained at same time as A shows wall thickening of terminal ileum (arrows) with collapsed or stenotic lumen. Note normal folds without wall thickening of jejunal loops (arrowheads).

 

Figure 3
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Fig. 1C 63-year-old woman with suspected Crohn's disease. Coronal thick-slab HASTE fat-saturation image obtained a few minutes later than A shows distention of terminal ileum (arrows).

 

Figure 4
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Fig. 1D 63-year-old woman with suspected Crohn's disease. Coronal true FISP fat saturation image obtained at same time as C shows distended terminal ileum with wall thickening without stenosis (arrow). Thick-slab HASTE imaging facilitates optimal timing of true FISP fat-saturation sequences with maximal distention. This increases certainty of grading small-bowel stenosis.

 

Figure 5
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Fig. 2 35-year-old woman with healthy-appearing small-bowel. During optimal distention, coronal true fast imaging with steady-state precession fat-saturation image shows normal folds in jejunum (arrowheads) and no stenosis or bowel wall thickening in terminal ileum (arrows).

 

Crohn's Disease
Top
Abstract
Introduction
MRI Technique
Normal Appearance
Crohn's Disease
Other Inflammatory Small-Bowel...
References
 
Crohn's disease can be localized in every segment of the small bowel, with a predilection for the terminal ileum. The major advantage of MR enteroclysis over other techniques for detection of small-bowel abnormalities is visualization of the complete small bowel and extramural disease manifestations without the use of ionizing radiation. The imaging protocol enables identification of both the diagnosis and the extent of the disease. Functional information can be used to differentiate between collapsed normal bowel wall, active disease, inactive disease, and bowel wall stenosis (Figs. 3A and 3B). Within the morphologic series, the most important characteristics for disease activity (i.e., bowel wall edema, ulcerations, and increased mesenteric vascularization [comb sign]) are contained (Figs. 4A and 4B). The contrast-enhanced series contributes to the differentiation between active and chronic disease. Specific characteristics for Crohn's disease—that is, creeping fat (increased mesenteric fat), skip lesions, and fistulas—can be identified on both the morphologic and contrast-enhanced series. Characteristics of active inflammation of the small bowel are bowel wall edema, ulcerations, increased mesenteric vascularization, increased enhancement of the bowel wall, and mesenteric lymph nodes [4] (Figs. 5A, 5B, and 5C). In acute inflammation, the bowel wall can have a layered pattern. A double-halo sign is related to submucosal edema (Figs. 6A, 6B, and 6C). Inactive disease is characterized by no abnormalities (i.e., optimal distention of bowel loops, healthy peristalsis, and no stenosis) or bowel wall thickening with relative low signal intensity representing fibrosis with limited, homogeneous contrast enhancement (Fig. 7). Fat accumulation in the submucosa can be found in the subacute or chronic stage (Fig. 8). MRI can show infiltration of mesenteric fat that may evolve into a fistula (Fig. 9). Intraluminal fluid and the use of an IV contrast medium can improve the detection of fistulas. Abscesses are more readily identified on the sequences performed after the injection of IV contrast medium (Fig. 10). MRI also allows the evaluation of complications associated with Crohn's disease, including intussusception, stricture formation, and carcinoma.


Figure 6
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Fig. 3A 31-year-old man with known Crohn's disease. Coronal true fast imaging with steady-state precession (FISP) and fat saturation shows almost no distention of jejunum (arrowheads) and suggesting a wide-open terminal ileum (arrows).

 

Figure 7
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Fig. 3B 31-year-old man with known Crohn's disease. Coronal true FISP image obtained with fat saturation during optimal distention shows normal jejunal loops (arrowheads) and short segment of bowel wall thickening of terminal ileum with high-grade stenosis (arrows). Optimal distention contributes to differentiation between stenosis and collapsed bowel loops.

 

Figure 8
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Fig. 4A 38-year-old woman with suspected Crohn's disease. Coronal true fast imaging with steady-state precession (FISP) and fat saturation without optimal distention of small-bowel loops shows wall thickening of ileum (arrows), with increased mesenteric vascularization (comb sign, arrowheads) and creeping fat (dot).

 

Figure 9
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Fig. 4B 38-year-old woman with suspected Crohn's disease. Coronal true FISP fat-saturation image obtained during optimal distention shows that thickened ileum loop has intermediate- to high-grade stenosis (arrows). In accordance with A, comb sign (arrowheads) and creeping fat (dot) are visualized.

 

Figure 10
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Fig. 5A 21-year-old man with proven Crohn's disease. Coronal true fast imaging with steady-state precession (FISP) and fat saturation shows two segments of bowel wall thickening, mucosal ulcerations (arrowhead), and stenosis with prestenotic dilatation (thick solid arrow) of ileum. This figure also shows fibrofatty proliferation (creeping fat, dot), mesenteric lymph nodes (thin arrow), and increased mesenteric vascularity (comb sign, open arrow). Distal from diseased proximal segment is second segment of thickened ileum loop (asterisk): skip lesion.

 

Figure 11
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Fig. 5B 21-year-old man with proven Crohn's disease. Coronal fast low-angle shot (FLASH) 2D fat-saturation image obtained after contrast injection shows increased contrast enhancement of two thickened segments of small-bowel loops (skip lesions, arrows) and increased mesenteric vascularity (comb sign, open arrow).

 

Figure 12
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Fig. 5C 21-year-old man with proven Crohn's disease. Endoscopy shows ulcerations (arrows) and loss of ileal folds.

 

Figure 13
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Fig. 6A 42-year-old man with known Crohn's disease. Axial true fast imaging with steady-state precession (FISP) and fat saturation shows diffuse thickening, edema (arrow), and irregular mucosa of mainly mucosa of bowel wall of ileum. Small amount of ascites (asterisk) was found in this region.

 

Figure 14
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Fig. 6B 42-year-old man with known Crohn's disease. Axial enhanced fast low-angle shot (FLASH) 2D fat-saturation image shows diffuse thickening, irregular mucosa (arrowhead), and intense contrast enhancement of mainly mucosa of bowel wall of ileum (arrow). This implies active disease. Active disease is also visible in sigmoid and rectum (open arrows).

 

Figure 15
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Fig. 6C 42-year-old man with known Crohn's disease. Endoscopy of terminal ileum shows ulcu (arrow) with wall of edema (arrowhead).

 

Figure 16
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Fig. 7 46-year-old woman with midgut malrotation type 1 and suspected Crohn's disease. Coronal true fast imaging with steady-state precession (FISP) and fat saturation shows thickening of terminal ileum (arrow), without increased contrast enhancement (not shown). Wall thickness of cecum (arrowhead) is normal. Absence of ulcerations, bowel wall edema, and increased contrast enhancement are features of inactive Crohn's disease.

 

Figure 17
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Fig. 8 60-year-old man with proven Crohn's disease. Coronal true fast imaging with steady-state precession (FISP) and fat saturation shows fat accumulation in submucosa (arrowhead), which implies subacute or chronic disease stage. Fistula between two ileum loops (arrow) is also visualized.

 

Figure 18
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Fig. 9 45-year-old woman with proven Crohn's disease. Axial true fast imaging with steady-state precession (FISP) and fat saturation shows fistula between small bowel and soft-tissue layers of abdominal wall (arrow).

 

Figure 19
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Fig. 10 37-year-old woman with known Crohn's disease. Axial fast low-angle shot (FLASH) 2D fat-saturation image obtained after contrast injection shows thickened ileum loop with intense contrast enhancement (arrow). On left side of this loop is small abscess (arrowhead).

 


Figure 20
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Fig. 11 75-year-old woman with recently proven celiac disease. Coronal true fast imaging with steady-state precession (FISP) and fat saturation shows decrease in jejunal folds (arrowheads) and increase in ileal folds ("ileal jejunization," arrows), which are characteristic features of celiac disease.

 


Figure 21
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Fig. 12 31-year-old woman with abdominal pain and diarrhea. Axial true fast imaging with steady-state precession (FISP) and fat saturation shows diffuse thickened jejunum loop (arrow) with edema of all wall layers, especially serosa. Without proven cause, her complaints resolved spontaneously. In follow-up, no relapse of complaints is established. This case is example of jejunitis without proven cause.

 


Figure 22
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Fig. 13 65-year-old man with left flank pain and infectious jejunitis. Axial true fast imaging with steady-state precession (FISP) and fat saturation shows thickened jejunal folds (arrows). Normal folds in distal jejunum (arrowhead) are shown. Parapelvic cyst can be seen in right kidney. Stool of this patient was giardiasis-positive.

 

Other Inflammatory Small-Bowel Diseases
Top
Abstract
Introduction
MRI Technique
Normal Appearance
Crohn's Disease
Other Inflammatory Small-Bowel...
References
 
Other inflammatory small-bowel diseases can have features that resemble Crohn's disease, such as wall thickening, loss of folds, ulcerations, stenosis, and increased mesenteric vascularization (comb sign). Identification of disease-specific features is therefore important in the diagnosis of Crohn's disease and includes creeping fat, skip lesions, and fistulas.

Celiac disease is a gluten-sensitive malabsorption syndrome, characterized by villous atrophy and crypt hyperplasia of the small intestinal mucosa, occurring at any age. Imaging features of celiac disease are small-bowel atonia, mucosal fold thickening, increased fold separation, and increased ileal folds ("ileal jejunization") [5] (Fig. 11). In a quarter of the patients with proven celiac disease, no macroscopic abnormalities can be found.

Jejunitis can be described as a most likely inflammatory entity of only the jejunum without a proven cause. It is characterized by a thickening of all jejunal wall layers with serosal edema (Fig. 12). The findings can resolve completely and should be differentiated from jejunitis in Crohn's disease using specific Crohn's disease features.

Inflammation related to bacteria or parasites causes diffuse wall and fold thickening and resolves completely after therapy (Fig. 13). Intestinal tuberculosis is a rare manifestation in which the ileocecal region is commonly involved. In the acute stage, ulcerations can be seen; in the subacute stage, scarring effects on the bowel wall can be identified.

Eosinophilic gastroenteropathy is a rare disorder characterized by peripheral and tissue eosinophilia infiltrating all three layers of the bowel wall and can involve any segment of the gastrointestinal tract, especially the stomach and small bowel. It is characterized by a loss of all mucosal folds in the small bowel, bowel wall thickening, and atonia [6] (Figs. 14A and 14B).


Figure 23
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Fig. 14A 66-year-old woman with proven eosinophilic gastroenteropathy. Coronal true fast imaging with steady-state precession (FISP) shows diffuse loss of mucosal folds and diffuse thickened wall of all small-bowel loops (arrows). Lack of motility on thick-slab HASTE sequence with fat saturation (not shown) is also characteristic of this disease.

 

Figure 24
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Fig. 14B 66-year-old woman with proven eosinophilic gastroenteropathy. Endoscopy shows loss of ileum folds with nodularity (arrows) of mucosa.

 
Sclerosing encapsulating peritonitis is a rare disorder, occurring in patients undergoing peritoneal dialysis. Lack of peristalsis at MR fluoroscopy and diffuse bowel wall thickening in the appropriate clinical setting provide the diagnosis. Peritoneal calcifications are conspicuous at CT [7] (Figs. 15A, 15B, and 15C).


Figure 25
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Fig. 15A 44-year-old woman with peritoneal dialysis and sclerosing encapsulating peritonitis. Coronal true fast imaging with steady-state precession (FISP) and fat saturation shows diffuse pronounced small-bowel wall thickening (arrows) and central localization. Thick-slab HASTE fat-saturation images reveal lack of motility (not shown).

 

Figure 26
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Fig. 15B 44-year-old woman with peritoneal dialysis and sclerosing encapsulating peritonitis. Coronal fast low-angle shot (FLASH) 2D fat-saturation image obtained after contrast injection shows increased diffuse enhancement of small-bowel wall (arrows).

 

Figure 27
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Fig. 15C 44-year-old woman with peritoneal dialysis and sclerosing encapsulating peritonitis. C, Axial CT after contrast injection shows diffuse peritoneal calcifications (arrows).

 
Radiation enteritis is a complication after radiation therapy that occurs often within 2 years, sometimes as long as 10-20 years, after radiation therapy. The disease is characterized by diffuse mild thickening, intense contrast enhancement, loss of folds, and lack of peristalsis of the small-bowel loops in the area of previous radiation therapy [8] (Figs. 16A and 16B).


Figure 28
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Fig. 16A 75-year-old woman with radiation enteritis, 20 years after abdominal hysterectomy and radiation therapy for endometrial carcinoma. Axial true fast imaging with steady-state precession (FISP) and fat saturation shows diffuse mild thickened distended ileum loops (arrows), without peristalsis (not shown). Note colostomy bag ventral of right abdominal wall after resection of colon carcinoma 2 years ago.

 

Figure 29
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Fig. 16B 75-year-old woman with radiation enteritis, 20 years after abdominal hysterectomy and radiation therapy for endometrial carcinoma. Coronal fast low-angle shot (FLASH) 2D image shows increased contrast enhancement of thickened ileum loops (arrows) in contrast with normal enhancement of colon (arrowhead).

 


References
Top
Abstract
Introduction
MRI Technique
Normal Appearance
Crohn's Disease
Other Inflammatory Small-Bowel...
References
 

  1. Beall DP, Regan F. MRI of bowel obstruction using the HASTE sequence. J Comput Assist Tomogr 1996;20 : 823-825[CrossRef][Medline]
  2. Umschaden HW, Szolar D, Gasser J, Umschaden M, Haselbach H. Small-bowel disease: comparison of MR enteroclysis images with conventional enteroclysis and surgical findings. Radiology2000; 215:717 -725[Abstract/Free Full Text]
  3. Schunk K. Small bowel magnetic resonance imaging for inflammatory bowel disease. Top Magn Reson Imaging2002; 13:409 -425[CrossRef][Medline]
  4. Gourtsoyiannis N, Papanikolaou N, Grammatikakis J, Papamastorakis G, Prassopoulos P, Roussomoustakaki M. Assessment of Crohn's disease activity in the small bowel with MR and conventional enteroclysis: preliminary results. Eur Radiol 2004;14 : 1017-1024[CrossRef][Medline]
  5. Laghi A, Paolantonio P, Catalano C, et al. MR imaging of the small bowel using polyethylene glycol solution as an oral contrast agent in adults and children with celiac disease: preliminary observations. AJR 2003; 180:191 -194[Abstract/Free Full Text]
  6. Horton KM, Fishman EK. Uncommon inflammatory diseases of the small bowel: CT findings. AJR 1998;170 : 385-388[Free Full Text]
  7. Cancarini GC, Sandrini M, Vizzardi V, et al. Clinical aspects of peritoneal sclerosis. J Nephrol 2001;14 : 39-47
  8. Nguygen NP, Antoine JE, Dutta S, Karlsson U, Sallah S. Current concepts in radiation enteritis and implications for future clinical trials. Cancer 2002; 95:1151 -1163[CrossRef][Medline]

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