REVIEW ARTICLE
Imaging Crohn Disease: MR Enterography Pablo Rodriguez, MD,* Ramiro Mendez, MD,* Fatima Matute, MD,* Paula Hernandez, MD,* and Juan Luis Mendoza, MD, PhD† Abstract: Magnetic resonance enterography in Crohn disease management has been rapidly growing in importance during recent years. Being familiar to this technique is essential for radiologists and also, to some extent, for gastroenterologists. Our aim is to study and describe the imaging findings in magnetic resonance enterography in Crohn disease to develop a comprehensive and useful review article and imaging atlas. Key Words: Crohn disease, inflammatory bowel disease, magnetic resonance enterography, magnetic resonance imaging (J Comput Assist Tomogr 2014;38: 219–227)
C
rohn disease (CD) is a chronic inflammatory condition that belongs to the so-called inflammatory bowel diseases, together with ulcerative colitis and indeterminate colitis. The exact cause of the disease is not known, although several factors have been found to be related to its pathophysiology, such as genetic, immunological, and environmental factors. Crohn disease can affect any segment of the digestive tract from mouth to anus, but it most frequently affects the small and large bowel. Terminal ileum is the most common site of onset.1 Crohn disease typically shows a segmental affection of the bowel, combining affected gut segments separated by spared ones. There can also be extraintestinal affections, including osteoarticular, dermatological, or hepatobiliary. The onset of the disease usually occurs in the second and third decades of life.2 Crohn disease is characterized by full-thickness bowel wall inflammation, with formation of nonnecrotizing granulomata (Fig. 1). Penetrating wall ulcers may develop and end up in bowel perforation and fistulas. Intestinal fibrosis can develop in chronic stages of the disease. Crohn disease is usually a long-term condition with acute relapses. Acute and chronic lesions can coincide in time. Patients can present with a wide range of symptoms, including abdominal pain and cramps and diarrhea (with or without blood). The course of the disease may be complicated with intestinal fistulas (sometimes developed after surgical interventions), abdominal abscesses, or by bowel obstruction. Management of CD is based on long-term maintenance and treatment of acute recurrences. Treatment is mainly pharmacologic, consisting in aminosalicylates, corticosteroids, and immunosuppressive and immunomodulatory drugs. Surgical resection of the affected bowel segment is considered when there are acute complications and medical treatment fails to control symptoms or there is a fibrotic intestinal stenosis and should always be restricted to short damaged areas. From the *Departments of Radiology and †Gastroenterology, Hospital Clínico San Carlos, Madrid, Spain. Received for publication August 7, 2013; accepted September 25, 2013. Reprints: Pablo Rodriguez, MD, Department of Radiology, Hospital Clinico San Carlos, Prof. Martin Lagos s/n 28040 Madrid, Spain (e‐mail: [email protected]). The authors declare no conflict of interest. No funding was received from any institution or organization to elaborate this work. Copyright © 2014 by Lippincott Williams & Wilkins
J Comput Assist Tomogr • Volume 38, Number 2, March/April 2014
It is important to assess CD inflammatory activity. Predominance of acute inflammatory changes or intestinal fibrosis in an acute relapse of the disease or in the setting of an intestinal obstruction will determine the initial medical and/or surgical approach. Physical examination, acute-phase reactants, endoscopy and biopsy, imaging tests, and clinical indexes such as Crohn’s Disease Activity Index and Harvey-Bradshaw Index are among the tools used to appraise CD activity. Traditionally, barium contrast radiological studies and computed tomography (CT) have been the imaging studies of choice when evaluating the diagnosis and complications in patients with CD. However, repetition of x-ray studies could lead to an important accumulated radiation dose. This is of special importance in children and patients starting at a young age and suffering repeated outbreaks.3–6 Magnetic resonance enterography (MR-E) is an imaging technique whose utilization in CD management has been increasing in recent years. Its accuracy is similar to that of the CT enterography (CT-E) in overall diagnostic efficacy in CD, assessing the extension of the process and depicting active inflammatory changes. Magnetic resonance enterography however does not use any ionizing radiation and has several other advantages when compared with its CT counterpart. Magnetic resonance enterography is superior to CT-E in the detection of bowel fibrosis, subtle endoluminal and mucosal changes, showing submucosal edema, and also in depicting bowel strictures mainly because MR has a better soft tissue contrast and provides a wide range of diagnostic tools in the form of different imaging sequences such as diffusion-weighted imaging (DWI), fat saturation techniques, dynamic contrast enhancement, and real-time functional imaging among others.4,7–12 These advantages award MR-E a prevailing role in CD imaging as it is a technique that not only helps in diagnosing the disease but provides information about the extent and the degree of inflammation and fibrosis, detects possible complications, helps in the subtype classification of patients with CD, aids to decide and plan the surgical and/or medical management, and is also an important tool in monitoring therapeutic response.3,7,8,13–19 Computed tomography is however more available, less time consuming, and less technically complex than MR. Computed tomography also has a higher sensitivity to detect free air in the abdominal cavity, and abscesses between bowel loops could be easier to diagnose if a positive (iodinated or barium) oral contrast is used. Hence, CT keeps a role in the acute or emergency setting as well as in older patients or patients with difficulties to tolerate an MR-E examination.8,12,18,20 Pelvic magnetic resonance is a different magnetic resonance (MR) examination also important in CD patients, mainly in those with perianal fistulizing disease.21,22 Endoscopy is still the gold standard imaging technique for the assessment of the condition of the gastrointestinal tract. Colonoscopy provides essential information about the mucosa of the colon and the terminal ileum and allows biopsies to be performed. However, there are some technical limitations because most of the small bowel cannot be assessed by colonoscopy, transmural and extraintestinal disease cannot be evaluated by endoscopy, www.jcat.org
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
219
J Comput Assist Tomogr • Volume 38, Number 2, March/April 2014
Rodriguez et al
FIGURE 1. Noncaseating granuloma. Photomicrograph from large bowel (hematoxylin-eosin stain, original magnification, 100×). There is a noncaseating granuloma (arrows) in the bowel mucosa of a patient with Crohn’s disease. Figure 1 can be viewed online in color at www.jcat.org.
and sometimes retrograde ileoscopy is not technically possible. Magnetic resonance enterography (MR-E) is therefore an important diagnostic technique that can help and supplement endoscopy. The advantages of MR-E are of key importance, especially in situations such as the suspicion of extraintestinal complications or when assessing postsurgical recurrence of CD.23–27 Ultrasound examination of the bowel has also been used in CD. Although it is a noninvasive technique that does not use ionizing radiation, it has proven to be less precise when defining CD extension in comparison with MR-E and other pathological findings such as fistulas.28 As the importance of MR-E in CD is increasingly growing, it is important for clinicians, especially gastroenterologists, and not only for radiologists to be familiar with the findings of CD in MR-E.
MATERIALS, METHODS, AND MR-E TECHNIQUE We reviewed 120 consecutive MR-E studies practiced between 2010 and 2011 in patients with CD in our hospital. We studied frequent and infrequent imaging findings of CD such as the affected intestinal segments, presence of bowel stenosis and/or intestinal obstruction, mural thickening of intestinal loops, signs of active inflammation of the bowel, different patterns of intestine wall enhancement, presence of enlarged mesenteric lymph nodes, intestinal wall ulcerations, signs of long-term CD, as well as the presence of secondary complications. We collected the more representative examples of those findings to provide a comprehensive imaging atlas of radiological signs of CD in MR-E. The indications for prescribing an MR-E study in a patient with CD in our center are summarized in Table 1. We follow a standard examination protocol when performing MR-E in CD outpatients in our institution. In these cases, MR-E is performed after 5 days of low-residue diet and 4 to 6 hours of fasting because of the volume of liquid that they are going to ingest for the imaging study. We regularly use a 3% mannitol solution as oral contrast media for distending the small bowel. It is a slightly hypo-osmolar solution, almost isotonic, but we have also used isosmolar solution of polyethyleneglycol in some cases. Patients should drink 1.5 L of this mannitol solution in 30 to 40 minutes, and we begin MR examination after waiting for another 15 minutes. If the patient experiences vomiting or nausea that prevents swallowing or does not tolerate the oral consumption of the contrast media
220
www.jcat.org
solution, we consider postponing the examination or using a lesser amount of oral contrast that sometimes is good enough for a diagnostic MR-E study especially in subocclusive cases. Most patients are young and do not experience cardiac or renal conditions that may advise against the intake of large amounts of liquid. There are, however, some conditions that may be found in CD and can complicate the intake of that volume, such as short-bowel syndrome or acute bowel obstructions. Shortbowel syndrome is a disorder caused by the removal of large parts of small bowel in which patients cannot drink large volumes and their rapid bowel transit causes a higher frequency of defecation that can complicate the MR-E study. In the setting of an acute bowel obstruction, we do not administer any oral solution. In MR enteroclysis, bowel contrast is administered through a jejunal tube, consistently providing a better distension of the small bowel, particularly the jejunum, as well as a better depiction of superficial wall abnormalities in comparison with MR-E.9,29 However, routinely, we do prefer performing MR enterography rather than MR enteroclysis because MR enteroclysis studies are technically more complex than enterographies (oral administration of bowel contrast), there is a need for x-ray control of correct tube placing, and they are unpleasant for patients because administration of large volumes of contrast liquids can be better tolerated per os. Furthermore, the differences between MR-E and MR enteroclysis in distal small-bowel distension are less significant, and both techniques have shown good accuracy when assessing the bowel in CD.30–32 We performed MR-E studies in two 1.5T machines (Signa HDx and Excite HDx; GE Healthcare, Milwaukee, Wis) using an 8-channel phased-array surface coil, field of view covering from diaphragm to pelvis when possible (at least from midliver to urinary bladder). Patients lay in supine position, holding their arms above their head, and feet pointing to the scanner. In a 3-plane localizer series, we checked that the oral solution had reached the right colon at least. If not, we waited for another 10 to 20 minutes before starting the examination. Some claustrophobic patients were able to withstand the MR exploration in prone position. If a claustrophobic patient cannot stand the MR examination, we have to move that patient to the CT room and practice a CT enterography instead using the previously administered neutral (water density) contrast agent. We do use glucagon (1 mg subcutaneous or intravenous) as spasmolytic drug to reduce intestinal mobility and to achieve a better dilatation of bowel loops. The 1-mg dose was divided in 2 injections of 0.5 mg each, one at the beginning of the study and the other one just before the administration of intravenous gadolinium-based contrast (Gd-DOTA, DOTAREM; Guerbet, France). In diabetic patients, we use hyoscine butylbromide instead of glucagon (20–40 mg, intravenous). Patients with glaucoma or prostatic symptoms could have a contraindication to hyoscine butylbromide.
TABLE 1. MR-Enterography Indications in CD in Our Institution Abscence of definitive diagnosis after colono-ileoscopy with intestinal biopsy Acute outbreak with intestinal obstruction Postsurgical relapse Treatment failure Evaluating response to treatment Suspicion of complications Study of extension
© 2014 Lippincott Williams & Wilkins
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
J Comput Assist Tomogr • Volume 38, Number 2, March/April 2014
Imaging Crohn Disease: MR Enterography
TABLE 2. Montreal Classification of Crohn Disease Age at diagnosis (A)
Localization (L)
Behavior (B)
A1 ≤16 years
L1 Terminal ileum
A2 17–40 years A3 >40 years
L2 Colonic L3 Ileo-colonic L4 Upper digestive tract
B1 Nonstricturing, nonpenetrating B2 Stricturing B3 Penetrating p: perianal disease modifier
Our MR-E scan protocol usually includes the following sequences: Single-shot fast spin-echo (SSFSE) T2-weighted images (GE Healthcare), acquired in both coronal and axial planes (slice thickness, ≤5 mm), with and without fat suppression. Fast imaging employing steady-state acquisition (FIESTA) images (GE Healthcare) in coronal and axial planes (slice thickness, ≤5 mm). Gradient-echo T1 in-phase and out-of-phase images in coronal plane. Diffusion-weighted images of the region of interest. Axial plane, b = 600 s/mm2, 8 NEX (number of excitations). Three-dimensional gradient-echo T1 images with fat suppression, in coronal plane (slice thickness of 3 mm). This includes a baseline acquisition and 3 dynamic sequences performed 30, 60, and 120 seconds after intravenous administration of gadoliniumbased contrast (0.1 mmol/kg; Gd-DOTA, DOTAREM). Another delayed sequence 5 to 7 minutes after contrast injection was performed. Usually, an axial acquisition was also performed between 2 and 5 minutes after contrast injection. All sequences are acquired with the patient in apnea except in DWI, which is acquired with free-synchronized breathing. The whole scanning time ranges between 30 and 35 minutes. We do not usually perform dynamic cine studies unless we want to accurately assess intestinal mobility.
FIGURE 2. Intestinal obstruction secondary to inflammatory bowel stenosis. A, Coronal SSFSE T2WI fatsat. Small-bowel obstruction secondary to a stenotic ileum loop with thickened wall (arrows). Small amount of free fluid in pelvis. B, Coronal 3-dimensional GRE T1 fatsat (60 seconds after intravenous contrast injection). The stenotic ileum loop shows enhancement of the mucosa, transmural ulcers, and a mural abscess (small arrows).
RESULTS AND DISCUSSION: IMAGING FINDINGS Crohn disease has a variable clinical course, and there are different clinical classifications. Montreal Classification of 2005 (Table 2) classifies CD patients on the basis of the age at diagnosis, the main disease's localizations, and its pattern of behavior.33 Magnetic resonance enterography has been proven to have a good correlation with surgical findings when assessing Montreal Classification behavior of CD.19 Maglintie et al34 described a widely used classification of CD in 4 subtypes more focused on imaging aspects. These subtypes are the active inflammatory disease, the perforating-fistulizing disease, the fibrostenotic disease, and the reparative-regenerative disease.
TABLE 3. Signs of Acute Inflammation in MR-Enterography Bowel wall thickening High signal intensity in bowel wall in DWI Mesenteric prominent vascularity (comb sign) Hyperintense signal of peri-intestinal fat in T2WI
Hyperintense wall signal in fatsat T2WI Increased enhancement in bowel wall (especially if stratified) Enlarged, increased in number, or enhancing lymph nodes Ascites
© 2014 Lippincott Williams & Wilkins
FIGURE 3. Acute inflammatory changes in the bowel wall. Detail of axial SSFE T2WI with (A) and without (B) fatsat. There is a distal ileum loop with wall thickening (arrow) in A, and B displays better the hyperintensity of the wall compatible with edema (arrow). C, Detail of axial 3-dimensional GRE T1WI fatsat (60 seconds after intravenous contrast injection). The affected loop shows increased mucosal enhancement (arrow). D, Detail of DWI (b = 600). The ileum loop has a high signal intensity (arrow), especially in the mucosa-submucosa. www.jcat.org
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
221
J Comput Assist Tomogr • Volume 38, Number 2, March/April 2014
Rodriguez et al
FIGURE 4. Bowel loop with acute inflammatory changes (thick arrow) and other loop with chronic CD changes (thin arrow). A, Axial SSFSE T2WI. Two ileum loops (arrows) show thickening and high signal intensity of their walls. B, Axial GRE T1WI. The more anterior ileum loop show wall thickening with a low signal (thick arrow), whereas the other one (thin arrow) has wall thickening and a high signal in T1WI compatible with fatty submucosa infiltration, typical in chronic CD. C, Axial SSFSE T2WI fatsat. The more anterior ileum loop shows increased signal within its wall compatible with edema (thick arrow), whereas the other loop has less increased wall signal (thin arrow). D, DWI (b = 600). The more anteriorly located affected loop shows clearly increased signal intensity compatible with acute inflammation (thick arrow), whereas the other does not (thin arrow). Note the diffuse mesenteric fat hypertrophy in all sequences, a typical finding of CD.
Probably, these CD subtypes are actually different stages or patterns of behavior rather than different varieties of the disease.
Active Inflammatory Disease The affected bowel loops seem to have a thickened wall, with radiological signs of acute inflammatory changes. In Table 3, the main acute inflammatory findings in bowel loops and in other tissues are summarized. Bowel wall thickening is associated with active inflammation.35,36 The degree of thickening has been proven to be correlated with Crohn’s Disease Activity Index.37 Thickening of intestinal wall can lead to luminal stenosis and secondary intestinal obstruction (Fig. 2). Magnetic resonance
FIGURE 5. Stratified type of enhancement and comb sign. A, Coronal FIESTA (steady state GRE). An ileal loop near an ileocolostomy (arrows) is dilated, and it shows wall thickening and prominent mesenteric vasculature. B, Coronal 3-dimensional GRE T1WI fatsat (120 seconds after intravenous contrast injection). The affected ileal loop (arrows) has an increased mucosal enhancement (stratified type of enhancement) and prominence of mesenteric vasculature (comb sign), reflecting acute inflammatory changes. Note the marked irregularity of the mucosa in relation to superficial ulcerations.
222
www.jcat.org
enterography can detect stenosis with a 96% sensitivity.19 In cases of intestinal obstruction, it is important to differentiate whether the wall thickening seems to be mainly caused by acute inflammation or it is caused by fibrosis because this distinction could help decide the patient’s treatment—either medical or surgical. Signal hyperintensity in the bowel wall in T2-weighted images (T2WIs), especially in fat-suppressed sequences, indicates wall edema, thus being a sign of acute inflammation (Figs. 3, 4).35,36,38 A high signal intensity in DWI and restricted diffusion of the bowel wall have also been related to acute inflammation (Figs. 3, 4).39–44 The histopathological basis of these imaging findings remains unclear; however, Oto et al39 suggest that the dense lymphoid infiltrates and granulomata present in bowel wall in CD may restrict the diffusion of water molecules in the extracellular space and therefore provoking a high signal intensity in DWI and restricted diffusion. Maccioni et al43 have also proposed that the restricted diffusion observed in active
FIGURE 6. Nonstratified type of enhancement (transmural). A, Axial FIESTA (steady state GRE). Ileum loop with thickened wall (arrows). B, Axial 3-dimensional GRE T1WI fatsat (120 seconds after intravenous contrast injection). The affected bowel loop (arrows) shows increased full-thickness wall enhancement, with subtle prominence of mesenteric vasculature, compatible with transmural acute inflammation. © 2014 Lippincott Williams & Wilkins
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
J Comput Assist Tomogr • Volume 38, Number 2, March/April 2014
Imaging Crohn Disease: MR Enterography
FIGURE 9. Reactive mesenteric lymph nodes in CD. A, Axial precontrast 3-dimensional GRE T1WI fatsat showing multiple mesenteric enlarged lymph nodes with a reactive aspect (arrows). B, Axial 3-dimensional GRE T1WI fatsat (60 seconds after intravenous contrast injection). The lymph nodes are enhanced, supporting acute inflammation (arrows).
FIGURE 7. Inflammatory pseudopolyps. Axial 3-dimensional GRE T1WI fatsat images (120 seconds after intravenous contrast injection) from two different patients showing inflammatory pseudopolyps (arrows). In A, the small bowel loop has a thickened wall and full-thickness increased enhancement; whereas in B, the bowel loop also shows wall thickening but with mucosal hyperenhancement and prominence of the mesenteric vasculature.
wall inflammation might be related to some extent to the presence of fibrosis in the affected wall. Diffusion-weighted imaging sequences are performed quickly and sometimes are the most sensitive in detecting inflammation (edema) in the intestinal wall, with a sensitivity value of 100%, specificity of 92.9%, and a negative predictive value of 100%.44 Increased intravenous contrast enhancement of the bowel wall indicates inflammation.7,35 The so-called stratified type of bowel enhancement (mucosal increased enhancement with submucosal edema) has been related to acute inflammation (Figs. 3C, 5).36,45 Full-thickness nonstratified enhancement of intestinal wall can represent transmural acute inflammation as well (Figs. 6, 7A),46 although fibrotic bowel segments can also
show full-thickness enhancement, especially in delayed phases of the dynamic gadolinium enhanced series (Fig. 8). The so-called comb sign represents ingurgitation and prominence of vessels in the mesenteric side of a bowel loop. It favors the diagnosis of acute bowel wall inflammation (Figs. 5, 7B).35 Crohn disease affects more often the mesenteric side of the bowel loop. Reactive mesenteric enlarged lymph nodes are suggestive of the active inflammatory process.47 Local lymph nodes that are increased in number may also indicate local inflammation. Their degree of contrast enhancement has also been related to acute inflammation (Fig. 9).48 A high signal in fat-suppressed T2-weighted images in the intra-abdominal fat surrounding the bowel loops is an indicator of acute inflammation46 (especially if neighboring loops also show signs of acute inflammation). The presence of ascites in an adequate context of acute bowel inflammation is a nonspecific sign that supports mesenteric and/or peritoneal secondary irritation (Fig. 2A). Nevertheless, ascitic fluid in a moderately important amount is not a frequent finding in CD; thus, its presence might raise the possibility of an alternative diagnosis, as it happened in this patient with CD and a large amount of intraperitoneal fluid (Fig. 10).
FIGURE 8. Fibrotic changes in bowel loops. A, Coronal SSFSE T2WI. There are several jejunal loops in LUQ that show wall thickening with a low signal intensity (arrows). B, Coronal SSFSE T2WI fatsat. The aforementioned bowel loops do not have increased signal after fat saturation, meaning that there is no significant wall edema (arrows). C, Coronal 3-dimensional GRE T1WI fatsat (delayed acquisition after intravenous contrast injection). The small bowel loops show a full-thickness faint enhancement (arrows). These findings are related to bowel wall fibrosis. © 2014 Lippincott Williams & Wilkins
www.jcat.org
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
223
J Comput Assist Tomogr • Volume 38, Number 2, March/April 2014
Rodriguez et al
FIGURE 10. Crohn disease patient with a large amount of ascites. A, Coronal SSFSE T2 fatsat and (B) coronal 3-dimensional GRE T1 fatsat (late acquisition after intravenous contrast injection). The volume of ascitic fluid is much larger than the expected for an acute outbreak of CD. There is also peritoneal enhancement (arrows). These MR findings raised the suspicion of peritoneal carcinomatosis, but final diagnosis was peritoneal mesothelioma. Note left colon “C,” which is deformed by long-term evolution of CD and there is also pericolonic fat proliferation “F.”
The presence of intestinal ulcerations (superficial, longitudinal, or transverse ulcers), especially when they are transmural, supports the diagnosis of CD.49 Although very superficial ulcers are difficult to detect with MR-E, some irregularities of the mucosa can be assessed (Fig. 5). Linear or longitudinal ulcers are almost pathognomonic of CD50 and form the characteristic cobblestone-like pattern, more typically described in barium x-ray studies.
FIGURE 12. Enteric fistulas. Axial 3-dimensional GRE T1WI fatsat (delayed acquisition after intravenous contrast injection) from 2 different patients. A, Multiple entero-enteric fistulas between ileal loops in the pelvic region. The stratified type of enhancement indicates that these fistulas have active inflammation. B, Short entero-enteric fistula between 2 small-bowel loops showing enhancement indicating activity. C, Active entero-cutaneous fistula and inflammatory changes in the abdominal wall (arrows).
Transverse ulcers can be found in bowel loops of CD patients, and they can progress toward the serosa, ending up in a transmural ulcer, bowel perforation, or even fistula formation (Fig. 11). When bowel wall becomes ulcerated in CD, areas of remaining and relatively spared mucosa can be left isolated surrounded by the ulcers, forming the so-called pseudopolyps or inflammatory polyps (Figs. 7, 11). Mural abscesses can also be found in the intestine of patients with CD, especially in those with acute inflammation (Fig. 2).
Perforating and Fistulating Disease
FIGURE 11. Inflammatory pseudopolyps and transmural ulcer. Detail from coronal 3-dimensional GRE T1WI fatsat (late acquisition after intravenous contrast injection). There is a small bowel loop showing wall thickening, stratified-pattern of enhancement, and prominence of mesenteric vasculature. Multiple inflammatory pseudopolyps can be appreciated (one of them is pointed with a “P”). There is also a transmural ulceration with increased enhancement, indicating activity (arrow). Urinary bladder (“B”).
224
www.jcat.org
It is characterized by developing deep wall or transmural ulcers that might progress into fistulizing tracts. The frequency of presentation of fistulas in CD patients through life can be up to 35%. Most of these fistulas develop in the perianal region,51 and when imaging is needed, they are usually evaluated by a specific pelvic MR study. When fistulas arise in small bowel loops, they can be diagnosed and assessed by MR-E. Magnetic resonance enterography detection of fistulas has a good correlation with surgical findings.19 Small bowel fistulas can be blind-ended, entero-enteric, entero-colonic, entero-vesical, entero-vaginal, or entero-cutaneous among others. Associated inflammatory signs (high signal on T2 or DWI and increased gadolinium enhancement) indicate activity of the fistula (Fig. 12) and sometimes fluid or even gas can be found inside the fistulous tract. Fistulas can lead to the formation of abdominal inflammatory masses and abscesses (Fig. 13). The presence of abscesses is a relative contraindication for anti–TNF-alpha therapy. Transmural inflammation and ulcers can cause adhesions between bowel loops or between the loops and the mesentery. These adhesions can be either inflammatory active or fibroticchronic (Fig. 14).
Fibrostenotic Disease It is a long-term evolution subtype of CD in which intestine loops have experienced chronic inflammation and develop fibrosis. © 2014 Lippincott Williams & Wilkins
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
J Comput Assist Tomogr • Volume 38, Number 2, March/April 2014
Imaging Crohn Disease: MR Enterography
FIGURE 13. Intra-abdominal abscess. A, Coronal SSFSE T2WI and (B) Coronal 3-dimensional GRE T1WI fatsat (delayed acquisition after intravenous contrast injection). There is a large intra-abdominal fluid collection (big arrows) with enhancing wall and located next to the sigmoid colon, compatible with abscess. There is an inflammatory tract from affected sigmoid colon to the uterus (small arrows).
Imaging findings of intestinal fibrosis are summarized in Table 4. Low to moderate wall signal in T2WI and absence of inflammatory findings in a bowel loop showing a thickened wall favor the diagnosis of fibrosis. Faint and especially nonstratified and inhomogeneous wall enhancement has been related to fibrosis as well (Figs. 4, 8).46,48,52,53 Abnormal pseudosacculations of intestinal loops indicate chronic damage and fibrosis of the loop.46 Fibrostenotic disease is described as a relative contraindication for infliximab therapy; thus, it is important to detect fibrostenosing changes without evidence of CD inflammatory activity.54
Mesenteric fat hypertrophy is a typical finding in CD (Figs. 4, 8, 10).46,55
CONCLUSIONS The role of MR-E in the management of CD is rapidly increasing in importance because it can help in the diagnosis and evaluation of the extent of the disease. Information about the location of the disease, the degree of inflammation, and the presence of complications can influence medical treatment and guide
TABLE 4. Signs of Intestinal Fibrosis
Reparative and Regenerative Disease It is distinguished by mucosal atrophy, regenerative polyps (not to be confused with inflammatory pseudopolyps), and absence of acute active inflammation. Fatty infiltration of the submucosa is a characteristic sign of chronic CD (Figs. 4A–B, 15).49
FIGURE 14. Fibrotic adhesions. A, Coronal FIESTA and (B) coronal precontrast 3-dimensional GRE T1WI fatsat. There is a thin tract (arrow) from the right colon to the surrounding intra-abdominal fat. Note the tentlike effect on colon wall. C, Coronal 3-dimensional GRE T1WI fatsat (delayed acquisition after intravenous contrast injection), there is faint enhancement of the tract (arrow), meaning that it is probably a fibrotic adhesion. In the 3 images, hypertrophy of surrounding intra-abdominal fat can be seen. © 2014 Lippincott Williams & Wilkins
Bowel wall thickening without acute inflammatory changes Faint and inhomogeneous wall enhancement
Hypointensity of signal of the bowel wall in T2WI fat suppressed Intestinal pseudosacculations
FIGURE 15. Fatty infiltration of submucosa. A, Close-up from an axial SSFSE T2W image. Bowel loop with a high signal intensity in submucosa (arrows). B, Same sequence with fatsat (selective suppression of fat signal). The hyperintense submucosa loses its signal (arrows), indicating the fatty infiltration, a typical finding of chronic CD. www.jcat.org
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
225
J Comput Assist Tomogr • Volume 38, Number 2, March/April 2014
Rodriguez et al
surgery when needed, thus affecting the patient’s outcome. Consequently, it is important for physicians attending patients with CD, and not only for radiologists, to be familiar with its MR imaging findings. REFERENCES 1. Baumgart DC, Sandborn WJ. Inflammatory bowel disease: clinical aspects and established and evolving therapies. Lancet. 2007;369:1641–1657. 2. Karlinger K, Györke T, Makö E, et al. The epidemiology and the pathogenesis of inflammatory bowel disease. Eur J Radiol. 2000;35:154–167. 3. Jaffe TA, Gaca AM, Delaney S, et al. Radiation doses from small-bowel follow-through and abdominopelvic MDCT in Crohn’s disease. AJR Am J Roentgenol. 2007;189:1015–1022. 4. Quencer KB, Nimkin K, Mino-Kenudson M, et al. Detecting active inflammation and fibrosis in pediatric Crohn’s disease: prospective evaluation of MR-E and CT-E. Abdom Imaging. 2013;38:705–713. 5. Alliet P, Desimpelaere J, Hauser B, et al. MR enterography in children with Crohn disease: results from the Belgian pediatric Crohn registry (Belcro). Acta Gastroenterol Belg. 2013;76:45–48. 6. Silverstein J, Grand D, Kawatu D, et al. Feasibility of using MR enterography for the assessment of terminal ileitis and inflammatory activity in children with Crohn disease. J Pediatr Gastroenterol Nutr. 2012;55:173–177. 7. Grand DJ, Beland M, Harris A. Magnetic resonance enterography. Radiol Clin North Am. 2013;51:99–112. 8. Masselli G, Gualdi G. CT and MR enterography in evaluating small bowel diseases: when to use which modality? Abdom Imaging. 2013;38:249–259. 9. Masselli G, Gualdi G. MR imaging of the small bowel. Radiology. 2012;264:333–348.
ESGAR evidence-based consensus guidelines. J Crohns Colitis. 2013;7:556–585 19. Schill G, Iesalnieks I, Haimerl M, et al. Assessment of disease behavior in patients with Crohn’s disease by MR enterography. Inflamm Bowel Dis. 2013;19:983–990. 20. Al-Hawary MM, Kaza RK, Platt JF. CT enterography: concepts and advances in Crohn’s disease imaging. Radiol Clin North Am. 2013;51:1–16. 21. De Miguel Criado J, del Salto LG, Rivas PF, et al. MR imaging evaluation of perianal fistulas: spectrum of imaging features. Radiographics. 2012;32:175–194. 22. Sahni VA, Ahmad R, Burling D. Which method is best for imaging of perianal fistula?. Abdom Imaging. 2008;33:26–30. 23. Paparo F, Denegri A, Revelli M, et al. Crohn’s disease: value of diagnostic imaging in the evaluation of anastomotic recurrence. Ann Ital Chir. 2013;5:84. In Press. 24. Mazziotti S, Ascenti G, Scribano E, et al. Guide to magnetic resonance in Crohn’s disease: from common findings to the more rare complicances. Inflamm Bowel Dis. 2011;17:1209–1222. 25. Mazziotti S, Blandino A, Scribano E, et al. MR enterography findings in abdominopelvic extraintestinal complications of Crohn’s disease. J Magn Reson Imaging. 2013;37:1055–1063. 26. Patil SA, Cross RK. Update in the management of extraintestinal manifestations of inflammatory bowel disease. Curr Gastroenterol Rep. 2013;15:314. 27. Gallego Ojea JC, Echarri Piudo AI, Porta Vila A. Crohn’s disease: the usefulness of MR enterography in the detection of recurrence after surgery. Radiologia. 2011;53:552–559. 28. Castiglione F, Mainenti PP, De Palma GD, et al. Noninvasive diagnosis of small bowel Crohn’s disease: direct comparison of bowel sonography and magnetic resonance enterography. Inflamm Bowel Dis. 2013;19:991–998.
10. Siddiki HA, Fidler JL, Fletcher JG, et al. Prospective comparison of state-of-the-art MR enterography and CT enterography in small-bowel Crohn’s disease. AJR Am J Roentgenol. 2009;193:113–121.
29. 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. 2008;18:438–447.
11. Fiorino G, Bonifacio C, Peyrin-Biroulet L, et al. Prospective comparison of computed tomography enterography and magnetic resonance enterography for assessment of disease activity and complications in ileocolonic Crohn’s disease. Inflamm Bowel Dis. 2011;17:1073–1780.
30. Arrivé L, El Mouhadi S. MR enterography versus MR enteroclysis. Radiology. 2013;266:688.
12. Panés J, Bouzas R, Chaparro M, et al. Systematic review: the use of ultrasonography, computed tomography and magnetic resonance imaging for the diagnosis, assessment of activity and abdominal complications of Crohn’s disease. Aliment Pharmacol Ther. 2011;34:125–145. 13. Rimola J, Rodríguez S, Cabanas ML, et al. MRI of Crohn’s disease: from imaging to pathology. Abdom Imaging. 2012;37:387–396. 14. Sinha R, Verma R, Verma S, et al. MR enterography of Crohn disease: part 1, rationale, technique, and pitfalls. AJR Am J Roentgenol. 2011;197:76–79. 15. Mendoza JL, González-Lama Y, Taxonera C, et al. Using of magnetic resonance enterography in the management of Crohn’s disease of the small intestine: first year of experience. Rev Esp Enferm Dig. 2012;104:578–583. 16. Cheriyan DG, Slattery E, McDermott S, et al. Impact of magnetic resonance enterography in the management of small bowel Crohn’s disease. Eur J Gastroenterol Hepatol. 2013;25:550–555. 17. Rimola J, Ordás I, Rodriguez S, et al. Magnetic resonance imaging for evaluation of Crohn’s disease: validation of parameters of severity and quantitative index of activity. Inflamm Bowel Dis. 2011;17:1759–1768. 18. Panes J, Bouhnik Y, Reinisch W, et al. Imaging techniques for assessment of inflammatory bowel disease: Joint ECCO and
226
www.jcat.org
31. 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;17:2294–2301. 32. 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. 2004;2:491–497. 33. Silverberg MS, Satsangi J, Ahmad T, et al. Toward an integrated clinical, molecular and serological classification of inflammatory bowel disease: Report of a Working Party of the 2005 Montreal World Congress of Gastroenterology. Can J Gastroenterol. 2005;19 (suppl A):5–36. 34. Maglinte DD, Gourtsoyiannis N, Rex D, et al. Classification of small bowel. Crohn’s subtypes based on multimodality imaging. RadiolClin North Am. 2003;41:285–303. 35. Zappa M, Stefanescu C, Cazals-Hatem D, et al. Which magnetic resonance imaging findings accurately evaluate inflammation in small bowel Crohn’s disease? A retrospective comparison with surgical pathologic analysis. Inflamm Bowel Dis. 2011;17:984–993. 36. Punwani S, Rodriguez-Justo M, Bainbridge A, et al. Mural inflammation in Crohn disease: location-matched histologic validation of MR imaging features. Radiology. 2009;252:712–720. 37. Sempere GA, MartinezSanjuan V, Medina Chulia E, et al. MRI evaluation of inflammatory activity in Crohn’s disease. AJR Am J Roentgenol. 2005;184:1829–1835.
© 2014 Lippincott Williams & Wilkins
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
J Comput Assist Tomogr • Volume 38, Number 2, March/April 2014
38. Maccioni F, Staltari I, Pino AR, et al. Value of T2-weighted magnetic resonance imaging in the assessment of wall inflammation and fibrosis in Crohn’s disease. Abdom Imaging. 2012; 37:944–957. 39. Oto A, Zhu F, Kulkarni K, et al. Evaluation of diffusion-weighted MR imaging for detection of bowel inflammation in patients with Crohn’s disease. AcadRadiol. 2009;16:597–603. 40. Kilickesmez O, Atilla S, Soylu A, et al. Diffusion-weighted imaging of the rectosigmoid colon: preliminary findings. J Comput Assist Tomogr. 2009;33:863–866. 41. Kiryu S, Dodanuki K, Takao H, et al. Free-breathing diffusion-weighted imaging for the assessment of inflammatory activity in Crohn’s disease. J Magn Reson Imaging. 2009;29:880–886. 42. Oto A, Kayhan A, Williams JT, et al. Active Crohn’s disease in the small bowel: evaluation by diffusion weighted imaging and quantitative dynamic contrast enhanced MR imaging. J Magn Reson Imaging. 2011;33:615–624. 43. Maccioni F, Patak MA, Signore A, et al. New frontiers of MRI in Crohn’s disease: motility imaging, diffusion-weighted imaging, perfusion MRI, MR spectroscopy, molecular imaging, and hybrid imaging (PET/MRI). Abdom Imaging. 2012; 37:974–982. 44. Buisson A, Joubert A, Montoriol P-F, et al. Diffusion-weighted magnetic resonance imaging for detecting and assessing ileal inflammation in Crohn’s disease. Aliment Pharmacol Ther. 2013;37:537–545. 45. Maccioni F, Bruni A, Viscido A, et al. MR imaging in patients with Crohn disease: value of T2- versus T1-weighted gadolinium-enhanced MR sequences with use of an oral superparamagnetic contrast agent. Radiology. 2006;238:517–530.
© 2014 Lippincott Williams & Wilkins
Imaging Crohn Disease: MR Enterography
46. Tolan DJ, Greenhalgh R, Zealley IA, et al. MR enterographic manifestations of small bowel Crohn disease. Radiographics. 2010;30:367–384. 47. Leyendecker JR, Bloomfeld RS, DiSantis DJ, et al. MR enterography in the management of patients with Crohn disease. Radiographics. 2009;29:1827–1846. 48. Maccioni F, Viscido A, Marini M, et al. MRI evaluation of Crohn’s disease of the small and large bowel with the use of negative superparamagnetic oral contrast agents. Abdom Imaging. 2002;27:384–393. 49. Sinha R, Rajiah P, Murphy P, et al. Utility of high-resolution MR imaging in demonstrating transmural pathologic changes in Crohn disease. Radiographics. 2009;29:1847–1867. 50. Kelvin FM, Herlinger H. Crohn’s disease. In: Herlinger H, Maglinte DD, Birnbaum BA, eds. Clinical Imaging of Small Intestine. 2nd ed. New York, NY: Springer; 2001:259–289. 51. Hvas CL, Dahlerup JF, Jacobsen BA, et al. Diagnosis and treatment of fistulising Crohn’s disease. Dan Med Bull. 2011;58:C4338. 52. Fiorino G, Cesarini M, Malesci A, et al. The role of magnetic resonance imaging in detecting intestinal fibrosis in Crohn’s disease. Curr Drug Targets. 2012;13:1273–1279. 53. Fornasa F, Benassuti C, Benazzato L. Role of magnetic resonance enterography in differentiating between fibrotic and active inflammatory small bowel stenosis in patients with Crohn’s disease. J Clin Imaging Sci. 2011;1:35. 54. Poggioli G, Laureti S, Campieri M, et al. Infliximab in the treatment of Crohn’s disease. Ther Clin Risk Manag. 2007;3:301–308. 55. Stange EF, Travis SP, Vermeire S, et al. European evidence based consensus on the diagnosis and management of Crohn’s disease: definitions and diagnosis. Gut. 2006;55(suppl 1):i1–i15.
www.jcat.org
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
227
Imaging Crohn Disease: MR Enterography Pablo Rodriguez, MD,* Ramiro Mendez, MD,* Fatima Matute, MD,* Paula Hernandez, MD,* and Juan Luis Mendoza, MD, PhD† Abstract: Magnetic resonance enterography in Crohn disease management has been rapidly growing in importance during recent years. Being familiar to this technique is essential for radiologists and also, to some extent, for gastroenterologists. Our aim is to study and describe the imaging findings in magnetic resonance enterography in Crohn disease to develop a comprehensive and useful review article and imaging atlas. Key Words: Crohn disease, inflammatory bowel disease, magnetic resonance enterography, magnetic resonance imaging (J Comput Assist Tomogr 2014;38: 219–227)
C
rohn disease (CD) is a chronic inflammatory condition that belongs to the so-called inflammatory bowel diseases, together with ulcerative colitis and indeterminate colitis. The exact cause of the disease is not known, although several factors have been found to be related to its pathophysiology, such as genetic, immunological, and environmental factors. Crohn disease can affect any segment of the digestive tract from mouth to anus, but it most frequently affects the small and large bowel. Terminal ileum is the most common site of onset.1 Crohn disease typically shows a segmental affection of the bowel, combining affected gut segments separated by spared ones. There can also be extraintestinal affections, including osteoarticular, dermatological, or hepatobiliary. The onset of the disease usually occurs in the second and third decades of life.2 Crohn disease is characterized by full-thickness bowel wall inflammation, with formation of nonnecrotizing granulomata (Fig. 1). Penetrating wall ulcers may develop and end up in bowel perforation and fistulas. Intestinal fibrosis can develop in chronic stages of the disease. Crohn disease is usually a long-term condition with acute relapses. Acute and chronic lesions can coincide in time. Patients can present with a wide range of symptoms, including abdominal pain and cramps and diarrhea (with or without blood). The course of the disease may be complicated with intestinal fistulas (sometimes developed after surgical interventions), abdominal abscesses, or by bowel obstruction. Management of CD is based on long-term maintenance and treatment of acute recurrences. Treatment is mainly pharmacologic, consisting in aminosalicylates, corticosteroids, and immunosuppressive and immunomodulatory drugs. Surgical resection of the affected bowel segment is considered when there are acute complications and medical treatment fails to control symptoms or there is a fibrotic intestinal stenosis and should always be restricted to short damaged areas. From the *Departments of Radiology and †Gastroenterology, Hospital Clínico San Carlos, Madrid, Spain. Received for publication August 7, 2013; accepted September 25, 2013. Reprints: Pablo Rodriguez, MD, Department of Radiology, Hospital Clinico San Carlos, Prof. Martin Lagos s/n 28040 Madrid, Spain (e‐mail: [email protected]). The authors declare no conflict of interest. No funding was received from any institution or organization to elaborate this work. Copyright © 2014 by Lippincott Williams & Wilkins
J Comput Assist Tomogr • Volume 38, Number 2, March/April 2014
It is important to assess CD inflammatory activity. Predominance of acute inflammatory changes or intestinal fibrosis in an acute relapse of the disease or in the setting of an intestinal obstruction will determine the initial medical and/or surgical approach. Physical examination, acute-phase reactants, endoscopy and biopsy, imaging tests, and clinical indexes such as Crohn’s Disease Activity Index and Harvey-Bradshaw Index are among the tools used to appraise CD activity. Traditionally, barium contrast radiological studies and computed tomography (CT) have been the imaging studies of choice when evaluating the diagnosis and complications in patients with CD. However, repetition of x-ray studies could lead to an important accumulated radiation dose. This is of special importance in children and patients starting at a young age and suffering repeated outbreaks.3–6 Magnetic resonance enterography (MR-E) is an imaging technique whose utilization in CD management has been increasing in recent years. Its accuracy is similar to that of the CT enterography (CT-E) in overall diagnostic efficacy in CD, assessing the extension of the process and depicting active inflammatory changes. Magnetic resonance enterography however does not use any ionizing radiation and has several other advantages when compared with its CT counterpart. Magnetic resonance enterography is superior to CT-E in the detection of bowel fibrosis, subtle endoluminal and mucosal changes, showing submucosal edema, and also in depicting bowel strictures mainly because MR has a better soft tissue contrast and provides a wide range of diagnostic tools in the form of different imaging sequences such as diffusion-weighted imaging (DWI), fat saturation techniques, dynamic contrast enhancement, and real-time functional imaging among others.4,7–12 These advantages award MR-E a prevailing role in CD imaging as it is a technique that not only helps in diagnosing the disease but provides information about the extent and the degree of inflammation and fibrosis, detects possible complications, helps in the subtype classification of patients with CD, aids to decide and plan the surgical and/or medical management, and is also an important tool in monitoring therapeutic response.3,7,8,13–19 Computed tomography is however more available, less time consuming, and less technically complex than MR. Computed tomography also has a higher sensitivity to detect free air in the abdominal cavity, and abscesses between bowel loops could be easier to diagnose if a positive (iodinated or barium) oral contrast is used. Hence, CT keeps a role in the acute or emergency setting as well as in older patients or patients with difficulties to tolerate an MR-E examination.8,12,18,20 Pelvic magnetic resonance is a different magnetic resonance (MR) examination also important in CD patients, mainly in those with perianal fistulizing disease.21,22 Endoscopy is still the gold standard imaging technique for the assessment of the condition of the gastrointestinal tract. Colonoscopy provides essential information about the mucosa of the colon and the terminal ileum and allows biopsies to be performed. However, there are some technical limitations because most of the small bowel cannot be assessed by colonoscopy, transmural and extraintestinal disease cannot be evaluated by endoscopy, www.jcat.org
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
219
J Comput Assist Tomogr • Volume 38, Number 2, March/April 2014
Rodriguez et al
FIGURE 1. Noncaseating granuloma. Photomicrograph from large bowel (hematoxylin-eosin stain, original magnification, 100×). There is a noncaseating granuloma (arrows) in the bowel mucosa of a patient with Crohn’s disease. Figure 1 can be viewed online in color at www.jcat.org.
and sometimes retrograde ileoscopy is not technically possible. Magnetic resonance enterography (MR-E) is therefore an important diagnostic technique that can help and supplement endoscopy. The advantages of MR-E are of key importance, especially in situations such as the suspicion of extraintestinal complications or when assessing postsurgical recurrence of CD.23–27 Ultrasound examination of the bowel has also been used in CD. Although it is a noninvasive technique that does not use ionizing radiation, it has proven to be less precise when defining CD extension in comparison with MR-E and other pathological findings such as fistulas.28 As the importance of MR-E in CD is increasingly growing, it is important for clinicians, especially gastroenterologists, and not only for radiologists to be familiar with the findings of CD in MR-E.
MATERIALS, METHODS, AND MR-E TECHNIQUE We reviewed 120 consecutive MR-E studies practiced between 2010 and 2011 in patients with CD in our hospital. We studied frequent and infrequent imaging findings of CD such as the affected intestinal segments, presence of bowel stenosis and/or intestinal obstruction, mural thickening of intestinal loops, signs of active inflammation of the bowel, different patterns of intestine wall enhancement, presence of enlarged mesenteric lymph nodes, intestinal wall ulcerations, signs of long-term CD, as well as the presence of secondary complications. We collected the more representative examples of those findings to provide a comprehensive imaging atlas of radiological signs of CD in MR-E. The indications for prescribing an MR-E study in a patient with CD in our center are summarized in Table 1. We follow a standard examination protocol when performing MR-E in CD outpatients in our institution. In these cases, MR-E is performed after 5 days of low-residue diet and 4 to 6 hours of fasting because of the volume of liquid that they are going to ingest for the imaging study. We regularly use a 3% mannitol solution as oral contrast media for distending the small bowel. It is a slightly hypo-osmolar solution, almost isotonic, but we have also used isosmolar solution of polyethyleneglycol in some cases. Patients should drink 1.5 L of this mannitol solution in 30 to 40 minutes, and we begin MR examination after waiting for another 15 minutes. If the patient experiences vomiting or nausea that prevents swallowing or does not tolerate the oral consumption of the contrast media
220
www.jcat.org
solution, we consider postponing the examination or using a lesser amount of oral contrast that sometimes is good enough for a diagnostic MR-E study especially in subocclusive cases. Most patients are young and do not experience cardiac or renal conditions that may advise against the intake of large amounts of liquid. There are, however, some conditions that may be found in CD and can complicate the intake of that volume, such as short-bowel syndrome or acute bowel obstructions. Shortbowel syndrome is a disorder caused by the removal of large parts of small bowel in which patients cannot drink large volumes and their rapid bowel transit causes a higher frequency of defecation that can complicate the MR-E study. In the setting of an acute bowel obstruction, we do not administer any oral solution. In MR enteroclysis, bowel contrast is administered through a jejunal tube, consistently providing a better distension of the small bowel, particularly the jejunum, as well as a better depiction of superficial wall abnormalities in comparison with MR-E.9,29 However, routinely, we do prefer performing MR enterography rather than MR enteroclysis because MR enteroclysis studies are technically more complex than enterographies (oral administration of bowel contrast), there is a need for x-ray control of correct tube placing, and they are unpleasant for patients because administration of large volumes of contrast liquids can be better tolerated per os. Furthermore, the differences between MR-E and MR enteroclysis in distal small-bowel distension are less significant, and both techniques have shown good accuracy when assessing the bowel in CD.30–32 We performed MR-E studies in two 1.5T machines (Signa HDx and Excite HDx; GE Healthcare, Milwaukee, Wis) using an 8-channel phased-array surface coil, field of view covering from diaphragm to pelvis when possible (at least from midliver to urinary bladder). Patients lay in supine position, holding their arms above their head, and feet pointing to the scanner. In a 3-plane localizer series, we checked that the oral solution had reached the right colon at least. If not, we waited for another 10 to 20 minutes before starting the examination. Some claustrophobic patients were able to withstand the MR exploration in prone position. If a claustrophobic patient cannot stand the MR examination, we have to move that patient to the CT room and practice a CT enterography instead using the previously administered neutral (water density) contrast agent. We do use glucagon (1 mg subcutaneous or intravenous) as spasmolytic drug to reduce intestinal mobility and to achieve a better dilatation of bowel loops. The 1-mg dose was divided in 2 injections of 0.5 mg each, one at the beginning of the study and the other one just before the administration of intravenous gadolinium-based contrast (Gd-DOTA, DOTAREM; Guerbet, France). In diabetic patients, we use hyoscine butylbromide instead of glucagon (20–40 mg, intravenous). Patients with glaucoma or prostatic symptoms could have a contraindication to hyoscine butylbromide.
TABLE 1. MR-Enterography Indications in CD in Our Institution Abscence of definitive diagnosis after colono-ileoscopy with intestinal biopsy Acute outbreak with intestinal obstruction Postsurgical relapse Treatment failure Evaluating response to treatment Suspicion of complications Study of extension
© 2014 Lippincott Williams & Wilkins
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
J Comput Assist Tomogr • Volume 38, Number 2, March/April 2014
Imaging Crohn Disease: MR Enterography
TABLE 2. Montreal Classification of Crohn Disease Age at diagnosis (A)
Localization (L)
Behavior (B)
A1 ≤16 years
L1 Terminal ileum
A2 17–40 years A3 >40 years
L2 Colonic L3 Ileo-colonic L4 Upper digestive tract
B1 Nonstricturing, nonpenetrating B2 Stricturing B3 Penetrating p: perianal disease modifier
Our MR-E scan protocol usually includes the following sequences: Single-shot fast spin-echo (SSFSE) T2-weighted images (GE Healthcare), acquired in both coronal and axial planes (slice thickness, ≤5 mm), with and without fat suppression. Fast imaging employing steady-state acquisition (FIESTA) images (GE Healthcare) in coronal and axial planes (slice thickness, ≤5 mm). Gradient-echo T1 in-phase and out-of-phase images in coronal plane. Diffusion-weighted images of the region of interest. Axial plane, b = 600 s/mm2, 8 NEX (number of excitations). Three-dimensional gradient-echo T1 images with fat suppression, in coronal plane (slice thickness of 3 mm). This includes a baseline acquisition and 3 dynamic sequences performed 30, 60, and 120 seconds after intravenous administration of gadoliniumbased contrast (0.1 mmol/kg; Gd-DOTA, DOTAREM). Another delayed sequence 5 to 7 minutes after contrast injection was performed. Usually, an axial acquisition was also performed between 2 and 5 minutes after contrast injection. All sequences are acquired with the patient in apnea except in DWI, which is acquired with free-synchronized breathing. The whole scanning time ranges between 30 and 35 minutes. We do not usually perform dynamic cine studies unless we want to accurately assess intestinal mobility.
FIGURE 2. Intestinal obstruction secondary to inflammatory bowel stenosis. A, Coronal SSFSE T2WI fatsat. Small-bowel obstruction secondary to a stenotic ileum loop with thickened wall (arrows). Small amount of free fluid in pelvis. B, Coronal 3-dimensional GRE T1 fatsat (60 seconds after intravenous contrast injection). The stenotic ileum loop shows enhancement of the mucosa, transmural ulcers, and a mural abscess (small arrows).
RESULTS AND DISCUSSION: IMAGING FINDINGS Crohn disease has a variable clinical course, and there are different clinical classifications. Montreal Classification of 2005 (Table 2) classifies CD patients on the basis of the age at diagnosis, the main disease's localizations, and its pattern of behavior.33 Magnetic resonance enterography has been proven to have a good correlation with surgical findings when assessing Montreal Classification behavior of CD.19 Maglintie et al34 described a widely used classification of CD in 4 subtypes more focused on imaging aspects. These subtypes are the active inflammatory disease, the perforating-fistulizing disease, the fibrostenotic disease, and the reparative-regenerative disease.
TABLE 3. Signs of Acute Inflammation in MR-Enterography Bowel wall thickening High signal intensity in bowel wall in DWI Mesenteric prominent vascularity (comb sign) Hyperintense signal of peri-intestinal fat in T2WI
Hyperintense wall signal in fatsat T2WI Increased enhancement in bowel wall (especially if stratified) Enlarged, increased in number, or enhancing lymph nodes Ascites
© 2014 Lippincott Williams & Wilkins
FIGURE 3. Acute inflammatory changes in the bowel wall. Detail of axial SSFE T2WI with (A) and without (B) fatsat. There is a distal ileum loop with wall thickening (arrow) in A, and B displays better the hyperintensity of the wall compatible with edema (arrow). C, Detail of axial 3-dimensional GRE T1WI fatsat (60 seconds after intravenous contrast injection). The affected loop shows increased mucosal enhancement (arrow). D, Detail of DWI (b = 600). The ileum loop has a high signal intensity (arrow), especially in the mucosa-submucosa. www.jcat.org
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
221
J Comput Assist Tomogr • Volume 38, Number 2, March/April 2014
Rodriguez et al
FIGURE 4. Bowel loop with acute inflammatory changes (thick arrow) and other loop with chronic CD changes (thin arrow). A, Axial SSFSE T2WI. Two ileum loops (arrows) show thickening and high signal intensity of their walls. B, Axial GRE T1WI. The more anterior ileum loop show wall thickening with a low signal (thick arrow), whereas the other one (thin arrow) has wall thickening and a high signal in T1WI compatible with fatty submucosa infiltration, typical in chronic CD. C, Axial SSFSE T2WI fatsat. The more anterior ileum loop shows increased signal within its wall compatible with edema (thick arrow), whereas the other loop has less increased wall signal (thin arrow). D, DWI (b = 600). The more anteriorly located affected loop shows clearly increased signal intensity compatible with acute inflammation (thick arrow), whereas the other does not (thin arrow). Note the diffuse mesenteric fat hypertrophy in all sequences, a typical finding of CD.
Probably, these CD subtypes are actually different stages or patterns of behavior rather than different varieties of the disease.
Active Inflammatory Disease The affected bowel loops seem to have a thickened wall, with radiological signs of acute inflammatory changes. In Table 3, the main acute inflammatory findings in bowel loops and in other tissues are summarized. Bowel wall thickening is associated with active inflammation.35,36 The degree of thickening has been proven to be correlated with Crohn’s Disease Activity Index.37 Thickening of intestinal wall can lead to luminal stenosis and secondary intestinal obstruction (Fig. 2). Magnetic resonance
FIGURE 5. Stratified type of enhancement and comb sign. A, Coronal FIESTA (steady state GRE). An ileal loop near an ileocolostomy (arrows) is dilated, and it shows wall thickening and prominent mesenteric vasculature. B, Coronal 3-dimensional GRE T1WI fatsat (120 seconds after intravenous contrast injection). The affected ileal loop (arrows) has an increased mucosal enhancement (stratified type of enhancement) and prominence of mesenteric vasculature (comb sign), reflecting acute inflammatory changes. Note the marked irregularity of the mucosa in relation to superficial ulcerations.
222
www.jcat.org
enterography can detect stenosis with a 96% sensitivity.19 In cases of intestinal obstruction, it is important to differentiate whether the wall thickening seems to be mainly caused by acute inflammation or it is caused by fibrosis because this distinction could help decide the patient’s treatment—either medical or surgical. Signal hyperintensity in the bowel wall in T2-weighted images (T2WIs), especially in fat-suppressed sequences, indicates wall edema, thus being a sign of acute inflammation (Figs. 3, 4).35,36,38 A high signal intensity in DWI and restricted diffusion of the bowel wall have also been related to acute inflammation (Figs. 3, 4).39–44 The histopathological basis of these imaging findings remains unclear; however, Oto et al39 suggest that the dense lymphoid infiltrates and granulomata present in bowel wall in CD may restrict the diffusion of water molecules in the extracellular space and therefore provoking a high signal intensity in DWI and restricted diffusion. Maccioni et al43 have also proposed that the restricted diffusion observed in active
FIGURE 6. Nonstratified type of enhancement (transmural). A, Axial FIESTA (steady state GRE). Ileum loop with thickened wall (arrows). B, Axial 3-dimensional GRE T1WI fatsat (120 seconds after intravenous contrast injection). The affected bowel loop (arrows) shows increased full-thickness wall enhancement, with subtle prominence of mesenteric vasculature, compatible with transmural acute inflammation. © 2014 Lippincott Williams & Wilkins
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
J Comput Assist Tomogr • Volume 38, Number 2, March/April 2014
Imaging Crohn Disease: MR Enterography
FIGURE 9. Reactive mesenteric lymph nodes in CD. A, Axial precontrast 3-dimensional GRE T1WI fatsat showing multiple mesenteric enlarged lymph nodes with a reactive aspect (arrows). B, Axial 3-dimensional GRE T1WI fatsat (60 seconds after intravenous contrast injection). The lymph nodes are enhanced, supporting acute inflammation (arrows).
FIGURE 7. Inflammatory pseudopolyps. Axial 3-dimensional GRE T1WI fatsat images (120 seconds after intravenous contrast injection) from two different patients showing inflammatory pseudopolyps (arrows). In A, the small bowel loop has a thickened wall and full-thickness increased enhancement; whereas in B, the bowel loop also shows wall thickening but with mucosal hyperenhancement and prominence of the mesenteric vasculature.
wall inflammation might be related to some extent to the presence of fibrosis in the affected wall. Diffusion-weighted imaging sequences are performed quickly and sometimes are the most sensitive in detecting inflammation (edema) in the intestinal wall, with a sensitivity value of 100%, specificity of 92.9%, and a negative predictive value of 100%.44 Increased intravenous contrast enhancement of the bowel wall indicates inflammation.7,35 The so-called stratified type of bowel enhancement (mucosal increased enhancement with submucosal edema) has been related to acute inflammation (Figs. 3C, 5).36,45 Full-thickness nonstratified enhancement of intestinal wall can represent transmural acute inflammation as well (Figs. 6, 7A),46 although fibrotic bowel segments can also
show full-thickness enhancement, especially in delayed phases of the dynamic gadolinium enhanced series (Fig. 8). The so-called comb sign represents ingurgitation and prominence of vessels in the mesenteric side of a bowel loop. It favors the diagnosis of acute bowel wall inflammation (Figs. 5, 7B).35 Crohn disease affects more often the mesenteric side of the bowel loop. Reactive mesenteric enlarged lymph nodes are suggestive of the active inflammatory process.47 Local lymph nodes that are increased in number may also indicate local inflammation. Their degree of contrast enhancement has also been related to acute inflammation (Fig. 9).48 A high signal in fat-suppressed T2-weighted images in the intra-abdominal fat surrounding the bowel loops is an indicator of acute inflammation46 (especially if neighboring loops also show signs of acute inflammation). The presence of ascites in an adequate context of acute bowel inflammation is a nonspecific sign that supports mesenteric and/or peritoneal secondary irritation (Fig. 2A). Nevertheless, ascitic fluid in a moderately important amount is not a frequent finding in CD; thus, its presence might raise the possibility of an alternative diagnosis, as it happened in this patient with CD and a large amount of intraperitoneal fluid (Fig. 10).
FIGURE 8. Fibrotic changes in bowel loops. A, Coronal SSFSE T2WI. There are several jejunal loops in LUQ that show wall thickening with a low signal intensity (arrows). B, Coronal SSFSE T2WI fatsat. The aforementioned bowel loops do not have increased signal after fat saturation, meaning that there is no significant wall edema (arrows). C, Coronal 3-dimensional GRE T1WI fatsat (delayed acquisition after intravenous contrast injection). The small bowel loops show a full-thickness faint enhancement (arrows). These findings are related to bowel wall fibrosis. © 2014 Lippincott Williams & Wilkins
www.jcat.org
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
223
J Comput Assist Tomogr • Volume 38, Number 2, March/April 2014
Rodriguez et al
FIGURE 10. Crohn disease patient with a large amount of ascites. A, Coronal SSFSE T2 fatsat and (B) coronal 3-dimensional GRE T1 fatsat (late acquisition after intravenous contrast injection). The volume of ascitic fluid is much larger than the expected for an acute outbreak of CD. There is also peritoneal enhancement (arrows). These MR findings raised the suspicion of peritoneal carcinomatosis, but final diagnosis was peritoneal mesothelioma. Note left colon “C,” which is deformed by long-term evolution of CD and there is also pericolonic fat proliferation “F.”
The presence of intestinal ulcerations (superficial, longitudinal, or transverse ulcers), especially when they are transmural, supports the diagnosis of CD.49 Although very superficial ulcers are difficult to detect with MR-E, some irregularities of the mucosa can be assessed (Fig. 5). Linear or longitudinal ulcers are almost pathognomonic of CD50 and form the characteristic cobblestone-like pattern, more typically described in barium x-ray studies.
FIGURE 12. Enteric fistulas. Axial 3-dimensional GRE T1WI fatsat (delayed acquisition after intravenous contrast injection) from 2 different patients. A, Multiple entero-enteric fistulas between ileal loops in the pelvic region. The stratified type of enhancement indicates that these fistulas have active inflammation. B, Short entero-enteric fistula between 2 small-bowel loops showing enhancement indicating activity. C, Active entero-cutaneous fistula and inflammatory changes in the abdominal wall (arrows).
Transverse ulcers can be found in bowel loops of CD patients, and they can progress toward the serosa, ending up in a transmural ulcer, bowel perforation, or even fistula formation (Fig. 11). When bowel wall becomes ulcerated in CD, areas of remaining and relatively spared mucosa can be left isolated surrounded by the ulcers, forming the so-called pseudopolyps or inflammatory polyps (Figs. 7, 11). Mural abscesses can also be found in the intestine of patients with CD, especially in those with acute inflammation (Fig. 2).
Perforating and Fistulating Disease
FIGURE 11. Inflammatory pseudopolyps and transmural ulcer. Detail from coronal 3-dimensional GRE T1WI fatsat (late acquisition after intravenous contrast injection). There is a small bowel loop showing wall thickening, stratified-pattern of enhancement, and prominence of mesenteric vasculature. Multiple inflammatory pseudopolyps can be appreciated (one of them is pointed with a “P”). There is also a transmural ulceration with increased enhancement, indicating activity (arrow). Urinary bladder (“B”).
224
www.jcat.org
It is characterized by developing deep wall or transmural ulcers that might progress into fistulizing tracts. The frequency of presentation of fistulas in CD patients through life can be up to 35%. Most of these fistulas develop in the perianal region,51 and when imaging is needed, they are usually evaluated by a specific pelvic MR study. When fistulas arise in small bowel loops, they can be diagnosed and assessed by MR-E. Magnetic resonance enterography detection of fistulas has a good correlation with surgical findings.19 Small bowel fistulas can be blind-ended, entero-enteric, entero-colonic, entero-vesical, entero-vaginal, or entero-cutaneous among others. Associated inflammatory signs (high signal on T2 or DWI and increased gadolinium enhancement) indicate activity of the fistula (Fig. 12) and sometimes fluid or even gas can be found inside the fistulous tract. Fistulas can lead to the formation of abdominal inflammatory masses and abscesses (Fig. 13). The presence of abscesses is a relative contraindication for anti–TNF-alpha therapy. Transmural inflammation and ulcers can cause adhesions between bowel loops or between the loops and the mesentery. These adhesions can be either inflammatory active or fibroticchronic (Fig. 14).
Fibrostenotic Disease It is a long-term evolution subtype of CD in which intestine loops have experienced chronic inflammation and develop fibrosis. © 2014 Lippincott Williams & Wilkins
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
J Comput Assist Tomogr • Volume 38, Number 2, March/April 2014
Imaging Crohn Disease: MR Enterography
FIGURE 13. Intra-abdominal abscess. A, Coronal SSFSE T2WI and (B) Coronal 3-dimensional GRE T1WI fatsat (delayed acquisition after intravenous contrast injection). There is a large intra-abdominal fluid collection (big arrows) with enhancing wall and located next to the sigmoid colon, compatible with abscess. There is an inflammatory tract from affected sigmoid colon to the uterus (small arrows).
Imaging findings of intestinal fibrosis are summarized in Table 4. Low to moderate wall signal in T2WI and absence of inflammatory findings in a bowel loop showing a thickened wall favor the diagnosis of fibrosis. Faint and especially nonstratified and inhomogeneous wall enhancement has been related to fibrosis as well (Figs. 4, 8).46,48,52,53 Abnormal pseudosacculations of intestinal loops indicate chronic damage and fibrosis of the loop.46 Fibrostenotic disease is described as a relative contraindication for infliximab therapy; thus, it is important to detect fibrostenosing changes without evidence of CD inflammatory activity.54
Mesenteric fat hypertrophy is a typical finding in CD (Figs. 4, 8, 10).46,55
CONCLUSIONS The role of MR-E in the management of CD is rapidly increasing in importance because it can help in the diagnosis and evaluation of the extent of the disease. Information about the location of the disease, the degree of inflammation, and the presence of complications can influence medical treatment and guide
TABLE 4. Signs of Intestinal Fibrosis
Reparative and Regenerative Disease It is distinguished by mucosal atrophy, regenerative polyps (not to be confused with inflammatory pseudopolyps), and absence of acute active inflammation. Fatty infiltration of the submucosa is a characteristic sign of chronic CD (Figs. 4A–B, 15).49
FIGURE 14. Fibrotic adhesions. A, Coronal FIESTA and (B) coronal precontrast 3-dimensional GRE T1WI fatsat. There is a thin tract (arrow) from the right colon to the surrounding intra-abdominal fat. Note the tentlike effect on colon wall. C, Coronal 3-dimensional GRE T1WI fatsat (delayed acquisition after intravenous contrast injection), there is faint enhancement of the tract (arrow), meaning that it is probably a fibrotic adhesion. In the 3 images, hypertrophy of surrounding intra-abdominal fat can be seen. © 2014 Lippincott Williams & Wilkins
Bowel wall thickening without acute inflammatory changes Faint and inhomogeneous wall enhancement
Hypointensity of signal of the bowel wall in T2WI fat suppressed Intestinal pseudosacculations
FIGURE 15. Fatty infiltration of submucosa. A, Close-up from an axial SSFSE T2W image. Bowel loop with a high signal intensity in submucosa (arrows). B, Same sequence with fatsat (selective suppression of fat signal). The hyperintense submucosa loses its signal (arrows), indicating the fatty infiltration, a typical finding of chronic CD. www.jcat.org
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
225
J Comput Assist Tomogr • Volume 38, Number 2, March/April 2014
Rodriguez et al
surgery when needed, thus affecting the patient’s outcome. Consequently, it is important for physicians attending patients with CD, and not only for radiologists, to be familiar with its MR imaging findings. REFERENCES 1. Baumgart DC, Sandborn WJ. Inflammatory bowel disease: clinical aspects and established and evolving therapies. Lancet. 2007;369:1641–1657. 2. Karlinger K, Györke T, Makö E, et al. The epidemiology and the pathogenesis of inflammatory bowel disease. Eur J Radiol. 2000;35:154–167. 3. Jaffe TA, Gaca AM, Delaney S, et al. Radiation doses from small-bowel follow-through and abdominopelvic MDCT in Crohn’s disease. AJR Am J Roentgenol. 2007;189:1015–1022. 4. Quencer KB, Nimkin K, Mino-Kenudson M, et al. Detecting active inflammation and fibrosis in pediatric Crohn’s disease: prospective evaluation of MR-E and CT-E. Abdom Imaging. 2013;38:705–713. 5. Alliet P, Desimpelaere J, Hauser B, et al. MR enterography in children with Crohn disease: results from the Belgian pediatric Crohn registry (Belcro). Acta Gastroenterol Belg. 2013;76:45–48. 6. Silverstein J, Grand D, Kawatu D, et al. Feasibility of using MR enterography for the assessment of terminal ileitis and inflammatory activity in children with Crohn disease. J Pediatr Gastroenterol Nutr. 2012;55:173–177. 7. Grand DJ, Beland M, Harris A. Magnetic resonance enterography. Radiol Clin North Am. 2013;51:99–112. 8. Masselli G, Gualdi G. CT and MR enterography in evaluating small bowel diseases: when to use which modality? Abdom Imaging. 2013;38:249–259. 9. Masselli G, Gualdi G. MR imaging of the small bowel. Radiology. 2012;264:333–348.
ESGAR evidence-based consensus guidelines. J Crohns Colitis. 2013;7:556–585 19. Schill G, Iesalnieks I, Haimerl M, et al. Assessment of disease behavior in patients with Crohn’s disease by MR enterography. Inflamm Bowel Dis. 2013;19:983–990. 20. Al-Hawary MM, Kaza RK, Platt JF. CT enterography: concepts and advances in Crohn’s disease imaging. Radiol Clin North Am. 2013;51:1–16. 21. De Miguel Criado J, del Salto LG, Rivas PF, et al. MR imaging evaluation of perianal fistulas: spectrum of imaging features. Radiographics. 2012;32:175–194. 22. Sahni VA, Ahmad R, Burling D. Which method is best for imaging of perianal fistula?. Abdom Imaging. 2008;33:26–30. 23. Paparo F, Denegri A, Revelli M, et al. Crohn’s disease: value of diagnostic imaging in the evaluation of anastomotic recurrence. Ann Ital Chir. 2013;5:84. In Press. 24. Mazziotti S, Ascenti G, Scribano E, et al. Guide to magnetic resonance in Crohn’s disease: from common findings to the more rare complicances. Inflamm Bowel Dis. 2011;17:1209–1222. 25. Mazziotti S, Blandino A, Scribano E, et al. MR enterography findings in abdominopelvic extraintestinal complications of Crohn’s disease. J Magn Reson Imaging. 2013;37:1055–1063. 26. Patil SA, Cross RK. Update in the management of extraintestinal manifestations of inflammatory bowel disease. Curr Gastroenterol Rep. 2013;15:314. 27. Gallego Ojea JC, Echarri Piudo AI, Porta Vila A. Crohn’s disease: the usefulness of MR enterography in the detection of recurrence after surgery. Radiologia. 2011;53:552–559. 28. Castiglione F, Mainenti PP, De Palma GD, et al. Noninvasive diagnosis of small bowel Crohn’s disease: direct comparison of bowel sonography and magnetic resonance enterography. Inflamm Bowel Dis. 2013;19:991–998.
10. Siddiki HA, Fidler JL, Fletcher JG, et al. Prospective comparison of state-of-the-art MR enterography and CT enterography in small-bowel Crohn’s disease. AJR Am J Roentgenol. 2009;193:113–121.
29. 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. 2008;18:438–447.
11. Fiorino G, Bonifacio C, Peyrin-Biroulet L, et al. Prospective comparison of computed tomography enterography and magnetic resonance enterography for assessment of disease activity and complications in ileocolonic Crohn’s disease. Inflamm Bowel Dis. 2011;17:1073–1780.
30. Arrivé L, El Mouhadi S. MR enterography versus MR enteroclysis. Radiology. 2013;266:688.
12. Panés J, Bouzas R, Chaparro M, et al. Systematic review: the use of ultrasonography, computed tomography and magnetic resonance imaging for the diagnosis, assessment of activity and abdominal complications of Crohn’s disease. Aliment Pharmacol Ther. 2011;34:125–145. 13. Rimola J, Rodríguez S, Cabanas ML, et al. MRI of Crohn’s disease: from imaging to pathology. Abdom Imaging. 2012;37:387–396. 14. Sinha R, Verma R, Verma S, et al. MR enterography of Crohn disease: part 1, rationale, technique, and pitfalls. AJR Am J Roentgenol. 2011;197:76–79. 15. Mendoza JL, González-Lama Y, Taxonera C, et al. Using of magnetic resonance enterography in the management of Crohn’s disease of the small intestine: first year of experience. Rev Esp Enferm Dig. 2012;104:578–583. 16. Cheriyan DG, Slattery E, McDermott S, et al. Impact of magnetic resonance enterography in the management of small bowel Crohn’s disease. Eur J Gastroenterol Hepatol. 2013;25:550–555. 17. Rimola J, Ordás I, Rodriguez S, et al. Magnetic resonance imaging for evaluation of Crohn’s disease: validation of parameters of severity and quantitative index of activity. Inflamm Bowel Dis. 2011;17:1759–1768. 18. Panes J, Bouhnik Y, Reinisch W, et al. Imaging techniques for assessment of inflammatory bowel disease: Joint ECCO and
226
www.jcat.org
31. 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;17:2294–2301. 32. 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. 2004;2:491–497. 33. Silverberg MS, Satsangi J, Ahmad T, et al. Toward an integrated clinical, molecular and serological classification of inflammatory bowel disease: Report of a Working Party of the 2005 Montreal World Congress of Gastroenterology. Can J Gastroenterol. 2005;19 (suppl A):5–36. 34. Maglinte DD, Gourtsoyiannis N, Rex D, et al. Classification of small bowel. Crohn’s subtypes based on multimodality imaging. RadiolClin North Am. 2003;41:285–303. 35. Zappa M, Stefanescu C, Cazals-Hatem D, et al. Which magnetic resonance imaging findings accurately evaluate inflammation in small bowel Crohn’s disease? A retrospective comparison with surgical pathologic analysis. Inflamm Bowel Dis. 2011;17:984–993. 36. Punwani S, Rodriguez-Justo M, Bainbridge A, et al. Mural inflammation in Crohn disease: location-matched histologic validation of MR imaging features. Radiology. 2009;252:712–720. 37. Sempere GA, MartinezSanjuan V, Medina Chulia E, et al. MRI evaluation of inflammatory activity in Crohn’s disease. AJR Am J Roentgenol. 2005;184:1829–1835.
© 2014 Lippincott Williams & Wilkins
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
J Comput Assist Tomogr • Volume 38, Number 2, March/April 2014
38. Maccioni F, Staltari I, Pino AR, et al. Value of T2-weighted magnetic resonance imaging in the assessment of wall inflammation and fibrosis in Crohn’s disease. Abdom Imaging. 2012; 37:944–957. 39. Oto A, Zhu F, Kulkarni K, et al. Evaluation of diffusion-weighted MR imaging for detection of bowel inflammation in patients with Crohn’s disease. AcadRadiol. 2009;16:597–603. 40. Kilickesmez O, Atilla S, Soylu A, et al. Diffusion-weighted imaging of the rectosigmoid colon: preliminary findings. J Comput Assist Tomogr. 2009;33:863–866. 41. Kiryu S, Dodanuki K, Takao H, et al. Free-breathing diffusion-weighted imaging for the assessment of inflammatory activity in Crohn’s disease. J Magn Reson Imaging. 2009;29:880–886. 42. Oto A, Kayhan A, Williams JT, et al. Active Crohn’s disease in the small bowel: evaluation by diffusion weighted imaging and quantitative dynamic contrast enhanced MR imaging. J Magn Reson Imaging. 2011;33:615–624. 43. Maccioni F, Patak MA, Signore A, et al. New frontiers of MRI in Crohn’s disease: motility imaging, diffusion-weighted imaging, perfusion MRI, MR spectroscopy, molecular imaging, and hybrid imaging (PET/MRI). Abdom Imaging. 2012; 37:974–982. 44. Buisson A, Joubert A, Montoriol P-F, et al. Diffusion-weighted magnetic resonance imaging for detecting and assessing ileal inflammation in Crohn’s disease. Aliment Pharmacol Ther. 2013;37:537–545. 45. Maccioni F, Bruni A, Viscido A, et al. MR imaging in patients with Crohn disease: value of T2- versus T1-weighted gadolinium-enhanced MR sequences with use of an oral superparamagnetic contrast agent. Radiology. 2006;238:517–530.
© 2014 Lippincott Williams & Wilkins
Imaging Crohn Disease: MR Enterography
46. Tolan DJ, Greenhalgh R, Zealley IA, et al. MR enterographic manifestations of small bowel Crohn disease. Radiographics. 2010;30:367–384. 47. Leyendecker JR, Bloomfeld RS, DiSantis DJ, et al. MR enterography in the management of patients with Crohn disease. Radiographics. 2009;29:1827–1846. 48. Maccioni F, Viscido A, Marini M, et al. MRI evaluation of Crohn’s disease of the small and large bowel with the use of negative superparamagnetic oral contrast agents. Abdom Imaging. 2002;27:384–393. 49. Sinha R, Rajiah P, Murphy P, et al. Utility of high-resolution MR imaging in demonstrating transmural pathologic changes in Crohn disease. Radiographics. 2009;29:1847–1867. 50. Kelvin FM, Herlinger H. Crohn’s disease. In: Herlinger H, Maglinte DD, Birnbaum BA, eds. Clinical Imaging of Small Intestine. 2nd ed. New York, NY: Springer; 2001:259–289. 51. Hvas CL, Dahlerup JF, Jacobsen BA, et al. Diagnosis and treatment of fistulising Crohn’s disease. Dan Med Bull. 2011;58:C4338. 52. Fiorino G, Cesarini M, Malesci A, et al. The role of magnetic resonance imaging in detecting intestinal fibrosis in Crohn’s disease. Curr Drug Targets. 2012;13:1273–1279. 53. Fornasa F, Benassuti C, Benazzato L. Role of magnetic resonance enterography in differentiating between fibrotic and active inflammatory small bowel stenosis in patients with Crohn’s disease. J Clin Imaging Sci. 2011;1:35. 54. Poggioli G, Laureti S, Campieri M, et al. Infliximab in the treatment of Crohn’s disease. Ther Clin Risk Manag. 2007;3:301–308. 55. Stange EF, Travis SP, Vermeire S, et al. European evidence based consensus on the diagnosis and management of Crohn’s disease: definitions and diagnosis. Gut. 2006;55(suppl 1):i1–i15.
www.jcat.org
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
227
