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Radiología. 2011;53(5):421---433

www.elsevier.es/rx

UPDATE IN RADIOLOGY

Magnetic resonance enterography: Review of the techniquefor the study of Crohn’s disease�

L. Herraiz Hidalgo ∗, E. Alvarez Moreno, J. Carrascoso Arranz, R. Cano Alonso,V. Martínez de Vega Fernández

Departamento de Diagnóstico por la Imagen, Hospital Universitario Quirón, Pozuelo de Alarcón, Madrid, Spain

Received 14 September 2010; accepted 10 March 2011

KEYWORDSCrohn’s disease(D003424);Magnetic resonanceimaging (D008279);Cine MRI (D019028);Gadolinium(D005682)

Abstract Crohn’s disease is a chronic disease with an unpredictable course. Patients withCrohn’s disease will have to undergo numerous imaging tests. Crohn’s disease often affectsyoung people, who are more vulnerable to the harmful effects of repeated exposure to ionizingradiation. The high resolution of tissues on MR enterography gives it a diagnostic accuracy similarto that of CT; however, MR enterography does not have the drawback of ionizing radiation.The clinical indices used to assess Crohn’s disease are subjective and not very accurate; thus,enterographic techniques are becoming more common in clinical practice as a means to followup patients objectively. In this article, we describe the MR enterography technique we use toevaluate Crohn’s disease. We illustrate the most relevant imaging findings, and we review thesubtypes of the disease, the related scientific literature, and the MR indices used to assessthe severity of Crohn’s disease.© 2010 SERAM. Published by Elsevier España, S.L. All rights reserved.

PALABRAS CLAVEEnfermedad de Crohn(D003424);Resonanciamagnética (D008279);Cine-RM (D019028);

Entero-resonancia magnética: revisión de la técnica para el estudio de la enfermedadde Crohn

Resumen La enfermedad de Crohn es una enfermedad crónica de curso imprevisible querequiere numerosos estudios radiológicos durante la vida. Afecta frecuentemente a pacientesjóvenes, más vulnerables a los efectos nocivos de las exploraciones repetidas con radiaciones

loaded from http://http://zl.elsevier.es, day 29/07/2013. This copy is for personal use. Any transmission of this document by any media or format is strictly prohibited.

Gadolinio (D005682) ionizantes. La precisión diagnóstica de la enterografía por RM es similar a la de la tomografíacomputarizada por su alta resolución tisular, sin el inconveniente de la radiación. Los índices
clínicos de valoración de la enfermedad son poco precisos y subjetivos por lo que las técnicasenterográficas de imagen se están incorporando cada vez más a la práctica clínica como mediosobjetivos de control de la gravedad de la enfermedad. En este artículo, describimos nuestratécnica enterográfica en RM para la valoración de la enfermedad de Crohn. Revisaremos los
� Please cite this article as: Herraiz Hidalgo L, et al. Entero-resonancia magnética: revisión de la técnica para el estudio de laenfermedad de Crohn. Radiología. 2011; 53:421---33.

∗ Corresponding author.E-mail address: [email protected] (L. Herraiz Hidalgo).

2173-5107/$ – see front matter © 2010 SERAM. Published by Elsevier España, S.L. All rights reserved.

dx.doi.org/10.1016/j.rxeng.2011.03.002

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mailto:[email protected]

422 L. Herraiz Hidalgo et al.

hallazgos más relevantes por imagen y los subtipos de la enfermedad, la literatura científicarelacionada y los índices por RM en la valoración de la gravedad de la enfermedad.© 2010 SERAM. Publicado por Elsevier España, S.L. Todos los derechos reservados.

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TahdT1- and T2-weighted images), positive (high signal intensityon both T1 and T2), and biphasic (high signal intensity onT2 and low signal on T1 images). The biphasic category con-tains the largest number of agents (including osmotic agents

Table 1 Enteric contrast agents for MR imaging.

Limitations

PositiveGadolinium chelatesa CostsManganesea Low availabilityFood (milk, juice) Storage, expiration

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distentionPolyethylene glycol Rapid transit, diarrheaMannitol Osmotic effect, third spaceMethylcellulose AvailabilityBarium sulfate TasteLow density barium DiarrheaGadolinium chelatesa Costs

Document downloaded from http://http://zl.elsevier.es, day 29/07/2013. This copy is for personal use. Any transmission of this document by any media or format is strictly prohibited.

ntroduction

rohn’s disease (CD) is a chronic disease with annpredictable course characterized by frequent flare-upsnterspersed with periods of remission of varying length.atients with CD are subjected to multiple endoscopic andadiologic examinations throughout their lives.

CD is most often diagnosed in young patients (peak agef onset between the 2nd and 4th decades of life), who areore vulnerable to the hazards of repeated exposure to ion-

zing radiation associated with the chronic-recurrent coursef the disease.1,2

Certain subgroups of patients with CD are at greater riskf high lifetime doses of radiation including those with earlynset of the disease, with proximal gastrointestinal tractnvolvement, patients with penetrating---fistulizing diseasend those who require medical treatment with intravenousIV) steroids or TNF inhibitors or multiple surgeries.3

CT and MR enterography have proven superior to con-entional barium examinations since they provide essentialnformation about transmural and extramural involvements,nd about the complications that may determine surgicalreatment (obstruction, fistulas, abscesses).4

In recent years, MR enterographic techniques haveemonstrated a diagnostic accuracy similar to that of CThanks to the high resolution of tissues on MR enterography,o the development of new ultrafast sequences and the usef different types of oral contrast agents,5---7 in addition tohe benefits of avoiding the use of ionizing radiation.

The clinical indexes for the assessment of CD lack accu-acy, are subject to subjective interpretation1 and do notake into account the presence of extramural complications,hich may alter the optimal management of the patient.herefore, imaging techniques8 are increasingly being incor-orated into the clinical practice as objective methods tovaluate the activity and severity of the disease, and sci-ntific societies are starting to include them as first-lineechniques in their recommendations.9

agnetic resonance enterography protocol

agnetic resonance enterography versus magneticesonance enteroclysis

nteroclysis provides better depiction of mucosal abnormal-ties than enterography, but both techniques have a similarerformance in the detection of transmural involvementnd extramural complications. Although loop distensionchieved with enteroclysis generally is superior to thatchieved with enterography, this may not translate into an
mprovement in diagnostic accuracy.10
Patient acceptance favors MR enterography over MR ente-oclysis, and this acceptance is thus supported by recentiterature.

atient preparation

atients are instructed to avoid solid food at least 4 hefore the examination to achieve uniform peristalsis andmprove tolerance for ingestion of oral contrast agent. These of cathartics is not required. In the absence of bowelreparation, the presence of stools precludes an adequatentraluminal evaluation in less than 10% of colonic segments,hich is an acceptable outcome.11 A warm saline enema

s administered when simultaneous colonic assessment isequired.

Fluoroscopic or multiphase SSFSE (cine mode) MR imag-ng allows for the dynamic evaluation of the bowel loopsy monitoring the contrast column, reducing the number ofon-assessable segments and false positives.1,12---14

dministration of oral contrast agent

he literature describes three groups of enteric contrastgents that may be used for MR enterography to obtain aomogeneous contrast column and achieve uniform bowelistension (Table 1): negative (low signal intensity on both

Manganesea Availability

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Magnetic resonance enterography: Review of the technique

such as mannitol and non-osmotic such as polyethylenegly-col [PEG] and methylcellulose) and is the most used typeof enteric contrast (more availability, better depiction andlower cost). The ‘‘dark lumen’’ on T1-weighted images isessential for the assessment of the bowel mucosa and forthe detection of mural enhancement after IV contrast (IVC)administration.

Mannitol and PEG are the oral contrast agents most com-monly used and described in the literature.

Other important issues regarding oral contrast admin-istration are the volume of contrast and the timing ofadministration, which are determined by the agent used.There is a high interpersonal variability in transit times,even higher than the variability between healthy subjectsand patients with CD (with the exception of patients withobstruction). Using PEG, the average time the column ofcontrast takes to reach the cecum varies from 20 to 240 min,with an average time of 55---65 min.15,16

We use PEG solution (45 mg reconstituted in 1 l) ofwhich the patient takes 1.5---2 l (depending on the patienttolerance) commencing approximately 45---60 min beforeimaging. The patient takes 1---1.5 l in the first 30 min andthen 250 ml every 15 min. Immediately before imaging, thepatient drinks approximately 500 ml of water. This regimenpermits the evaluation of the entire small bowel in slowintestinal transits, and the water administered on the MRtable allows for the scanning of the jejunal loops in rapidintestinal transits, where the passage to the colon may resultin poor small bowel distension.

In patients with obstruction, the use of oral contrastagents may be obviated, but this requires individual eval-uation based on the symptoms.17

This regimen is quite well tolerated. According to ourexperience, there are virtually no adverse effects andless than 5% of our patients had intestinal discomfort ormoderate-severe diarrhea for several hours after the exam-ination. We could complete the imaging studies in allpatients. These results agree with the results reported inprevious papers.5,16,18

Rectal contrast administration

Some authors have advocated concomitant administrationof a warm rectal enema to improve the depiction of theentire colon and the distension of the terminal ileum.19 Wedo not routinely perform enemas, but when required, weadminister 1---1.5 l of warm saline via the rectum, dependingon the patient tolerance.

Antegrade colonic filling is also possible and well tol-erated, although it does not provide an optimal colonicdistension. Two-step techniques have also been describedin which the patients drink 2 l of PEG solution 2---4 h beforethe examination, and then 1.2---2 l of solution, dependingon the patient tolerance, 45 min before the examination.11

Spasmolytics and gastric emptying

The literature describes a wide variability of spas-molytics and modes of administration. Most authors useN-butilscopolamine or glucagon IV or intramuscularly. Weuse 20 mg of IV N-butilscopolamine (Buscopan® Boehringer,

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he study of Crohn’s disease 423

ngelheim, Germany) immediately before the procedure, asuggested by some authors.4,5,10,20---23 The literature reportsoses varying from 10 mg24 to 40 mg administered at theeginning of the examination.19,25 According to our expe-ience, this regimen does not interfere significantly withhe dynamic assessment of the bowel and improves thevaluation of the dynamic contrast-enhanced MR imaging,ore sensitive to artifacts related to bowel motility. It is

lso possible to divide the dose or administer a doubleose,26,27 one immediately before the examination and aecond one before the dynamic contrast-enhanced imaging,lthough this modality increases the room utilization time.lucagon (0.2---1 mg) is also widely used because it acts fastnd has a shorter half-life. Glucagon is administered at theeginning23,24 or during the course of the examination, afterine imaging and before the IV administration of the con-rast agent.1 Another option is dividing the dose into twooses, following the regimen previously described,2 to notnterfere in the evaluation of the distension and peristalsis.

The additional administration of IV erythromycin haseen recommended28 to achieve a homogeneous gastricmptying, and prone imaging has been recommendedo improve bowel loop separation and reduce motionrtifacts.10

According to our experience, prone imaging in combina-ion with spasmolytics may result in excessive reduction oferistalsis, limiting the assessment of loop motility. Also itust be considered that prone imaging can be uncomfort-

ble for the patient.

agnetic resonance protocol: sequences

e use a 1.5 T system (Signa HD; GE Medical Systems, Mil-aukee, WI) with an 8-channel abdominal phased-array coil

hat allows evaluation of the entire abdominal and pelvicegion in a single examination. When necessary, the ano-ectal imaging was completed with high-resolution protocoln a further examination. The average duration of the exam-nation was approximately 35 min (range 20---55 min).

After the initial sequences applied for localization, wecquire coronal and axial fat-suppressed FIESTA (fast imag-ng employing steady state acquisition) images (TR 3.7/TE.7; TI 200; flip angle of 70◦; variable FOV of 28---45 cmepending on the patient; 5---8 mm thickness/1.0 gap; matrixf 224 × 320; 1 NEX). Next, we apply an axial FRFSE sequencehat covers the region(s) of interest (TR 6000/TE 90; Echorain 20; variable FOV; 5---8 mm thickness/1.0 gap; matrix of20 × 224; 2 NEX). We continue with axial and coronal SSFSEequences (TR 850-1200/TE 80-90; variable FOV; 3---4 mmhickness/0.3 gap; matrix of 224 × 192; 0.55 NEX). Subse-uently, cine or multiphase imaging is performed selectinghe region and plane of interest. We use multiphase coro-al and axial FIESTA sequences (TR 3.7/TE 1.7; TI 200; flipngle of 70◦; variable FOV of 28---45 cm depending on theatient; 5---8 mm thickness/1.0 gap; matrix of 224 × 320;

NEX), performing sets of 15 acquisitions over the regionf interest per slice plane.

We finish the dynamic study M3D LAVA (TR 3.9/TE 1,8;I 7,0; variable FOV; 3---4 mm thickness/2.3 ov; flip anglef 12◦; matrix of 288 × 192; 0.7 NEX) after IVC administra-ion in the best plane (axial or coronal) for evaluating the

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ffected loops, acquiring 5 sets. Finally, we apply a coronalSPGR sequence (TR 230/TE 1.6; 4---6 mm thickness/0.6 gap;84 × 192; 1 NEX).

R imaging findings for the evaluationf Crohn’s disease activity

he assessment of active CD with MR imaging may deter-ine the management of the patient. Next, we describe

he MR findings associated with CD divided into mural andxtramural.

owel wall assessment

ural thickeningural thickening is one of the signs that better correlatesith CD. Several studies have reported that mural thickening4 mm in a plane perpendicular to the loop is a reliable pre-ictor of the disease (with a sensitivity of 88% and specificityf 75%),29 and that there is a significant reduction in muralhickening in response to the treatment.30,31 However, theegments that respond to the treatment remain pathologi-ally thickened in comparison with the normal bowel loopsf control subjects; in addition, there is low correlationetween wall thickening and disease activity.32 Moreover,he assessment of wall thickening could be limited by theegree of bowel distension33; optimal bowel distension ishus required to establish the limits of normal mural thick-ning. Nonetheless, Punwani et al. have recently reported arecise correlation between mural thickness on MR imagesnd surgical specimen.21

nhancement ratio of the bowel wall

ural enhancement in segments with active inflammation isignificantly higher than in normal segments, and is highlypecific for the detection of segmental involvement.29 Stud-es comparing segments with active inflammation before andfter treatment have proven that the peak of signal intensityecreases significantly after medical treatment.30,31 Cor-elation between mural enhancement and clinical activityndexes varies among studies but it is, in general, consideredood.20,26,29,34---37

There is clear evidence suggesting that bowel wallnhancement is the parameter that best correlates with theegree of inflammation.31

atterns of enhancement

everal mural enhancement patterns have been described:

-- Layered, laminated or stratified pattern (‘‘target’’ sign)is secondary to the edema of the submucosa and mus-cularis propria that appears in the early stages of thedisease in bowel loops with active inflammation resultingin increased mucosal and serosal enhancement. This isuseful to differentiate between loops with active inflam-
mation and loops with homogeneous enhancement, thatis, without active disease.10,20,24,29
-- Mucosal-only enhancement, which may be the only signof early active inflammation.

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-- Homogeneous mural enhancement characteristic ofchronic disease and quiescent or inactive disease.

-- Absence of mucosal enhancement and weak and homoge-neous enhancement of the rest of the layers. It also is anindicator of active disease.

he layered enhancement has a high sensitivity (of approx-mately 100%), specificity (87%) and diagnostic accuracy93.75%) in the detection of active inflammation.20

Punwani et al. reported statistically significant differ-nces between the layered, mucosal-only and homogeneousural enhancement patterns and the histologic indexes of

cute inflammation. Segments with layered enhancementave a major inflammatory component in the histologic anal-sis, while those with homogeneous enhancement lack acutenflammatory component.21 Del Vescovo et al. reported sim-lar results.20

yperintensity on T2 weighted images

ubmucosal edema in inflamed loops produces increasedignal intensity (Fig. 1). Several articles have reportedood correlation between signal hyperintensity on T2-eighted images of the affected loops and the presencef active inflammation,1,21,38,39 as well as significant dif-erences between healthy individuals and patients withesponse to treatment.30

ucosal abnormalities

ucosal abnormalities are typical findings of MR entero-lysis. A recent study reported that mucosal abnormalitiesre the most sensitive sign in patients with active CD.23

everal types of ulcerations may also be identified. Earlyucosal inflammation is characterized by aphthous or super-cial ulcers. These early manifestations are usually notisualized on MR,24,40 although sometimes appear as subtlebnormal imaging findings23 (Fig. 2). In this respect, conven-ional endoscopy, capsule endoscopy and barium imaging areuperior to MR imaging for their detection.41

As inflammation penetrates the wall, longitudinal andross-sectional fissures form the characteristic cobbleston-ng appearance. The visualization of deep fissures on MRmaging correlates with more severe lesions in the affectedegments on endoscopic Images.19

istension and peristalsisynamic cine mode imaging allows for the evaluationf the peristaltic activity of the bowel loops, of non-istended segments, especially the jejunal segments,42 anday help differentiate between inflammatory and fibrotic

trictures.23

MR enterography is useful for determining the possi-le causes of bowel obstruction, including CD.17,43 Dynamicmaging and the pattern of enhancement also help in theifferentiation between chronic strictures and transientpasms, between stricture caused by inflammation and
brotic stricture, and between severe bowel obstructionnd reversible obstruction.1
Cine imaging provides better depiction of the lesions thanonventional MR enterography.12,14

Magnetic resonance enterography: Review of the technique for the study of Crohn’s disease 425

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Figure 1 T2 signal hyperintensity of the bowel wall. Coronalileum with thickened and hyperintense wall on T2-weighted ima

Extramural findings

Abnormalities of the mesenteric fibrofatty tissueSome authors consider that there is an increase in T2 signalintensity in the fibrofatty tissue in virtually all patients withbiologically active inflammation, which may be related tomesenteritis, with edema and hyperemia of local vessels.32

On the other hand, fibrofatty proliferation, which sur-rounds and produces separation of the affected loops, mayappear in both active and inactive disease. A considerableamount of fibrofatty tissue may be seen in inactive dis-ease, but the signal appears increasingly hypointense onT2-weighted fat-suppressed images due to a higher fibrouscontent.32

Mesenteric vascularityThe increased mesenteric vascularity of the mesenteric bor-
der of the affected loop is known as the ‘‘comb sign’’. Thissign has a high sensitivity for the detection of active diseasebut low specificity, not reaching statistical significance.29
It has been suggested that increased vascular engorgement

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Figure 2 Mucosal abnormalities: superficial ulcers. (A) and (B) Axwith submucosal edema and irregular mucosal surface with some

terminal ileum shows multiple superficial ulcers (black arrows).

TA (A) and axial SSFSE (B) images show a loop of the terminalwhite arrows), and associated deep ulcers (yellow arrow in B).

ay persist for long periods in patients with inactive or qui-scent disease due to chronic mesenteric fibrosis.44

nhancement of local lymph nodesomogeneous enhancement of mesenteric lymph nodes,oderate or intense, is highly suggestive of active CD; how-

ver, moderate lymph node enhancement can also be seen in0% of cases with inactive disease.44 On the other hand, theize of the regional lymph nodes shows a weak correlationith the degree of inflammatory activity.45

dditional extramural findingshe presence of abscesses or active fistulas, found in 35% ofatients at some point during the course of the disease, isery specific in the diagnosis of inflammatory activity.23,46,47

lassification of Crohn’s disease: subtypes

D has been classified into several subgroups, and patientsay exhibit characteristics of more than one disease

ial FIESTA images show mural thickening of the terminal ileumfocal ulcerations (white arrows). (C) Endoscopic view of the


Figure 3 Distortion or blunting of the mucosal folds and thickening of the valvulae conniventes. (A) Coronal SSFSE image showst al ile( rows)

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hickening and blunting of valvulae conniventes of the terminB) Endoscopic view shows mucosal ulcers and edema (black ar

ubtype.1 There is a wide interpatient variability in the ten-ency to develop one subtype of another.

The subtypes are the active inflammatory sub-ype (described also as non-fistulizing non-stenotic),erforating-fistulizing, stenotic or fibrostenotic, andeparative---regenerative subtype.

This subtype classification is useful to determine if theatient may benefit from medical or surgical treatment.n this respect, understanding of the imaging findings andorrect classification are essential.

ctive inflammatory disease subtype

arly manifestations of CD include edema and aphthouslcerations, which are readily detected by endoscopyhereas MR imaging is less effective.40 The initial mucosal

nflammation may progressively develop into deep ulcers,ransmural inflammation, and granuloma formation withubsequent wall thickening, hyperemia, submucosal edemand hypertrophy of mesenteric fat.

Minimal active inflammatory signs are characterized asphthous or superficial ulcers on endoscopic images. Endo-copic and barium examinations are clearly superior inhe detection of these superficial mucosal abnormalities,41

hich may not be identified on MR imaging even with opti-al luminal distension.24,40 However, sometimes even subtle

bnormalities may be seen with MR imaging, including super-cial ulcerations (Fig. 2) that in combination with distortion,lunting, and a polypoid appearance of the valvulae con-iventes (Fig. 3) has high specificity for CD.23

Mucosal hyperemia is seen as an area of intense enhance-ent after contrast agent administration. Occasionally, this

nhancement may be the only imaging finding. The earlyeak of signal intensity after contrast administration corre-
ates well with the CD activity index (CDAI).23
As previously mentioned, the stratified pattern (layeredattern or ‘‘target’’ sign) of contrast enhancement has alsoeen correlated with active inflammation20,21 (Fig. 4).

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um with a pseudopolypoid appearance (white arrows in (A). in the terminal ileum.

Additional extramural findings in the setting of inflamma-ory subtype include mesenteric hyperemia with engorgedessels corresponding to hypervascularity of the affectedegment (‘‘comb’’ sign) usually accompanied by edema andesenteric fat proliferation around the affected loop. This

atty hypertrophy produces increased signal intensity on T2mages that correlates with active inflammation, but doesot correlate with the amount of fibrofatty proliferation, ashis can be present in inactive or quiescent disease.32

As mentioned before, regional lymphadenopathy is fre-uently seen in patients with inflammatory changes.44

-- Severe inflammation: signs of severe inflammatoryactivity include deep mucosal ulcerations and a‘‘cobblestone’’ appearance of the bowel mucosa (Fig. 5),very characteristic of CD.

Deep transmural ulcers are easily detected on FIESTA,SFSE and T1-weighted fat-suppressed images after contrastdministration.

The serrated lumen sign is secondary to the presencef multiple transverse ulcerations that result in an irreg-lar appearance and it correlates with severe inflammatoryisease activity.

In some individuals, these deep transmural ulcersrogress with resultant early fistula formation, being thusncluded in the penetrating---fistulizing disease subtype.

enetrating---fistulizing subtype

his subtype is characterized by severe inflammation thatrogresses to transmural ulceration with fistula formationr intestinal perforation. Prior to fistulization, large pene-
rating ulcers may be identified.
Differentiation between deep transmural ulcerationsfissures) and well-established fistulas is crucial as fis-ures may respond to more aggressive immunomodulatory


Figure 4 Stratified pattern. (A) Coronal T1-weighted fat-suppressed image and IV contrast. (B) Axial LAVA image with IV contrastshows the characteristic layered stratification with mucosal (blue arrows) and serosal (white arrow) enhancement and submucosal

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hypointensity (curved yellow arrows) secondary to edema. (B) C

treatments (TNF inhibitors), whereas established fistulascan act as potential infectious reservoirs that may lead tosepsis.

Active fistulas show intense contrast enhancement, whilechronic fistulas are seen as low-signal serpiginous tractswith no enhancement after contrast administration. Fis-tulous communications may occur between several bowelloops (internal fistula) or between loops and the skin or other
adjacent organs (external fistula) (Fig. 6).
The perianal region is the most common site affectedby fistulas. For this reason, complementary high resolution

oor

Figure 5 Inflammatory pseudopolyps: cobblestone sign. (A) and (B)multiple pseudopolyps (small white arrows) that correlate with the

appearance of the bowel mucosa (black arrows). The extensive inflaorifices, clearly visible on the MR image with colocolic fistulous tratracts with an abscess demonstrated in the left lateral abdominal w

-sectional image shows the target-like appearance of the loop.

maging of this region is sometimes required. According toome authors, fistula formation occurs at some point duringhe course of the disease in up to 35% of patients, and up to0% of patients develop perianal fistulas.47

Extramural complications such as abscesses (Fig. 7),nflammatory masses or adjacent organ involvement can beasily seen at MR enteroclysis.

Immunomodulatory therapy must be discontinued in case
f mural abscesses or fistulas because of the risk of devel-ping sepsis and their presence should be mentioned in theadiological report.
Coronal FIESTA images of left colon show mural thickening andcolonoscopic view (C) and (D) showing the typical cobblestonemmation precluded the detection with colonoscopy of fistulouscts (curved arrow in A) and external tracts (enterocutaneousall-curved arrow in B).


Figure 6 External fistulas. (A) and (B) Coronal T2-weighted fat-suppressed images show several fistulous colocolic tracts (yellowarrows) between the colonic splenic flexure and descending colon, and external subsplenic tracts to the abdominal wall (whitea st wi s) an

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rrow), where there is a large abscess that extends to the chemages show enhancement of the fistulous tracts (yellow arrow

ibrostenotic-stenotic subtype

mall bowel obstruction is the characteristic manifesta-ion of this disease subtype. The imaging examination
hows the fixed segment of stenosis, wall thickening orevere inflammatory changes are not necessarily present,nd homogeneous enhancement may be seen after contrastdministration. The persistence of mural thickening varies
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igure 7 Examples of abscesses in two different patients. (A) Axiayellow arrows) adjacent to the inflammatory ileal loops with thicbdominal wall abscess (white arrows).

all (white arrowhead). (C) and (D) Axial IV contrast-enhancedd peripheral enhancement of the abscess (white arrows).

nd it can persist over time irrespective of the inflammatoryisease activity (Fig. 8).

Cine imaging shows absence of distensibility and peristal-is. Bowel obstruction is usually accompanied by a greaterr lesser degree of prestenotic dilatation.

Differentiation between fibrotic and edematous steno-is is useful for selecting patients for surgical versusedical treatment. Chronic fibrotic stenoses are typically

l LAVA image with contrast shows several mesenteric abscesseskened wall. (B) Image of the same patient as in Fig. 6 shows


Figure 8 Fibrotic stenosis. (A) and (B) Coronal FIESTA images of a patient with a history of terminal ileum resection for Crohn’sdisease and episodes of partial bowel obstruction show fibrotic stenosis (white arrows in A and B) not distensible at dynamiccine imaging. (C) Axial contrast-enhanced T1-weighted fat-suppressed image and (D) Coronal contrast-enhanced T1-weighted fat-

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suppressed image of a patient with no history of surgery, but wileum with homogeneous contrast enhancement (arrows), comp

hypointense on both T1 and T2 sequences, whereas inflam-matory stenoses with transmural edema are hyperintense onT2 fat-suppressed sequences.

Pseudosacculation (omega sign) is usually caused byasymmetric fibrosis involving the mesenteric margin of theloop that results in pseudosaccule formation on the antime-senteric side (Fig. 9).

Reparative---regenerative subtype

Mucosal atrophy (absence of valvulae conniventes) andregenerative polyps characterize this phase.

The ‘‘halo’’ sign is caused by submucosal fibrosis and fathypertrophy, characteristic of the chronic reparative sub-type (Fig. 10).

Mucosal atrophy with focal areas of sparing is seen as
pseudopolyps that demonstrate no significant enhancementor edema.
Sometimes, extensive filiform polyposis with no edema-tous component may be seen. Regenerative pseudopolyps

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imilar symptoms, show thickening and stenosis of the terminale with chronic stenosis.

re not to be confused with those appearing among theeep ulcerations that develop in the advanced inflammatoryisease (cobblestone sign).

RI evaluation of activity in Crohn’s disease

he clinical indexes for the assessment of CD lack accu-acy, are subject to subjective interpretation and do notake into account the presence of extramural complications.herefore, CT and MR enterography are being increasingly

ncorporated into clinical practice as objective methods toontrol the severity of the disease.

The clinical index most widely accepted and most fre-uently used by gastroenterologists is the CDAI, whichvaluates during one week eight clinical variables. Thisndex is subject to wide variability of interpretations and to
he subjectivity of both the patient and gastroenterologist.ther simpler indexes (Harvey-Bradshaw index), or thosesed in combination with laboratory (Dutch or Van Heesndex), histopathologic (acute inflammatory score [AIS]) or


Figure 9 Pseudosacculation caused by asymmetric bowel fibrosis: omega sign. (A) Coronal FIESTA. (B) Axial SSFSE. (C) Axial FIESTA.( icatefi e no

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D) Axial T2-weighted fat-suppressed images. Yellow arrows indbrotic changes of the ileal loop forming a pseudosaccule on th

ndoscopic parameters (Crohn’s disease endoscopic indexf severity [CDEIS]) are not satisfactory either and do notnclude information on extramural complications.

Novel imaging techniques, specifically MR enterography,
lay an important role in the follow-up of inflammatoryowel disease.
Gourtsoyiannis et al. propose a magnetic resonance indexf activity (MaRIA) based on the presence of deep ulcers and

C

ae

Table 2 MRI index of severity for the evaluation of the inflamma

MRI quantitative findings

Wall thickness (mm)

Wall enhancementa (%)

Luminal stenosis (%)

MRI qualitative findings

Mucosal abnormalities (ulcers, cobblestoning. . .)

Layered pattern of enhancement

Mesenteric abnormalities (hyperemia, comb sign)

Pathologic lymphadenopathy (>10 mm, intense enhancement)

Fistulas

Inflammatory enteric masses-abscesses

Dynamic cine imaging

Normal peristalsis

Distensibility

MRI activity index

From Girometti et al.13 Diagnostic accuracy 91.1%, sensitivity 93.1%, sa Equation: signal intensity post-Gd − signal intensity pre-Gd/signal i

shortening of the mesenteric side of the bowel caused by then-fibrotic antimesenteric side (white arrows).

ymph node enhancement to discriminate between activend inactive disease.44

Rimola et al19,25 propose a simplified MaRIA to mea-ure disease activity, reporting good correlation with the
DEIS.
We use the MRI scoring system proposed by Girometi etl13,48 that includes mural, extramural and dynamic param-ters and has showed higher diagnostic accuracy than the

tory disease activity.

Scoring

0 1 2<3 3---4 >4<70 70---100 100<50 50---80 > 800 1--- +--- +--- +--- +--- +--- +0 1+ ---+ ---0---1 2---6 >7No activity Mild Moderate to severe

pecificity 87.5%.ntensity pre-Gd × 100.

Magnetic resonance enterography: Review of the technique for t

Figure 10 Wall thickening mainly at the expense of the sub-mucosa (white curved arrow), which appears hypointense onthe axial T2 fat-suppressed image, reflecting fat hypertrophyand fibrosis in the setting of the regenerative---reparative sub-type. The serosa (blue arrow) and mucosa appear hyperintense

A

-

---

-

--

--

-

C

T

A

Dhsatcta

R

5. Ippolito D, Invernizzi F, Galimberti S, Panelli MR, Sironi S. MR


producing the halo sign.

assessment of single parameters such as the enhancementpattern, enhancement curve or wall thickening49 (Table 2).

Conclusion

MR enterography is easy to perform and causes few adverseeffects. This technique is very useful in the evaluation ofparameters of importance for the gastroenterologist andthat may dictate a change in patient management.

We intend to achieve an optimal and uniform bowel dis-tension to obtain images with high resolution of contrastbetween the bowel wall and lumen, to assess the wallthickening, the distribution of wall abnormalities and bowelmotility with dynamic cine imaging.

The radiological report should include the location andextent of the affected segments, the patchy or continuousdistribution, and the presence of extramural complicationsthat may alter the treatment.

Inflammatory stenosis has to be differentiated fromfibrotic stenosis by assessing the distensibility and peristalsisof the affected segment.

The determination of the subtype or subtypes (in caseof manifestations of more than one subtype) of the dis-ease based on the previous definitions is essential to providepatients with the appropriate treatment and follow-up.

Young patients can especially benefit from MR enterog-raphy as they may require multiple follow-up examinationsfor disease relapse and monitoring of the disease progres-sion considering the mentioned parameters, such as lengthand number of segments, wall thickening, signal intensity,wall enhancement, etc.

Lastly, using the Crohn’s disease MRI index of severity we
can quantify the degree of inflammation in a more objectiveand reproducible manner than using clinical indexes.

uthorship

-- Responsible for the integrity of the study: L. HerraizHidalgo.

-- Conception of the study: L. Herraiz Hidalgo.-- Design: L. Herraiz Hidalgo.-- Acquisition of data: (considering that data are the data

collection of the patients studied with MR enterographyduring the above mentioned period, the correlation withthe clinical data obtained from the medical records inelectronic format, the correlation with surgical proto-cols, primary care reports, etc., and the classificationof the disease into the subtypes described in the mainmanuscript): J. Carrascoso Arranz, R. Alonso Cano andL. Herraiz Hidalgo.

-- Analysis and interpretation of data: J. Carrascoso Arranz,R. Alonso Cano and L. Herraiz Hidalgo.

-- Statistical analysis: not applicable.-- Bibliographic search: E. Álvarez Moreno and L. Herraiz

Hidalgo.-- Drafting of the manuscript: L. Herraiz Hidalgo.-- Critical review with intellectually relevant contributions:

V. Martínez de Vega.-- Approval of the final version: all the authors have

reviewed the manuscript and are aware of the modifica-tions made to it, giving their approval of the final version.

onflict of interest

he authors declare no conflict of interests.

cknowledgements

r Manuel Recio Rodríguez and Dr Mar Jiménez de la Penaave contributed to the review and drafting of this paper,haring their experience with relevant advices, and havelso contributed to the review of the relevant images andheir captions. We would thus like to thank them for theirontributions, although it is not possible to include them inhe author list because of the limitations to the number ofuthors.

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