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ORIGINAL ARTICLE: GASTROENTEROLOGY

Magnetic Resonance Enterography Healing and


Magnetic Resonance Enterography Remission Predicts
Improved Outcome in Pediatric Crohn Disease
y
Cary G. Sauer, zJeremy P. Middleton, §Courtney McCracken, yjjJonathan Loewen,
yjj
Kiery Braithwaite, yjjAdina Alazraki, ôDiego R. Martin, and ySubra Kugathasan

ABSTRACT

Background: Mucosal healing predicts clinical remission and improved What Is Known
outcomes in patients with Crohn disease (CD). Magnetic resonance enter-
ography (MRE) is a noninvasive imaging modality that can assess small and  Crohn disease affects the small bowel, often beyond
large bowel wall inflammation. Evidence suggests that MRE may be an
the reach of endoscopy.
acceptable alternative to evaluate mucosal healing over endoscopy. Our  Mucosal healing results in improved outcome in
objective is to determine whether MRE remission predicts clinical remission
Crohn disease.
at follow-up in children with CD.  Magnetic resonance enterography detects active
Methods: We performed an institutional review board–approved
inflammation in Crohn disease.
retrospecitve chart review using our prospectively maintained MRE CD  Magnetic resonance enterography correlates with
database. Inclusion criteria were all children who underwent an MRE more
endoscopy and histopathology.
than 6 months after diagnosis with CD who had follow-up of at least 1 year
from imaging.
Results: A total of 101 children with CD underwent MRE, a median of 1.3 What Is New
years from diagnosis with a median follow-up of 2.8 years after MRE.
 Magnetic resonance enterography remission and
Active inflammation was detected in 65 MRE studies, whereas 36 MRE
studies demonstrated MRE remission. A total of 88.9% of children resolution of active inflammation is associated with
demonstrating MRE remission were in clinical remission at follow-up, fewer surgeries for Crohn disease.
 Magnetic resonance enterography remission is
whereas only 44.6% of those demonstrating MRE active inflammation
achieved clinical remission. Children demonstrating MRE-active associated with fewer medication changes.
 Magnetic resonance enterography may be a surro-
inflammation were more likely to have a change in medication (44.6%
vs 8.3%) and more likely to undergo surgery (18.5% vs 2.8%). gate for mucosal healing, especially when not acces-
Conclusions: MRE remission is associated with clinical remission at sible by standard endoscopy.
follow-up at least 1 year after MRE. MRE remission was associated with
fewer medication changes and fewer surgeries suggesting that, similar to
endoscopic remission, MRE remission demonstrates improved outcome.
Key Words: Crohn disease, magnetic resonance enterography, pediatric
Additional research is needed to confirm that MRE can be used as a surrogate
for mucosal healing.
(JPGN 2016;62: 378–383)

Received January 30, 2015; accepted August 31, 2015.


From the Emory University School of Medicine Department of Pediatrics,
the yChildren’s Healthcare of Atlanta, the zDepartment of Pediatrics,
C rohn disease (CD) is a chronic inflammatory bowel disease
that can affect all portions of the gastrointestinal tract. CD
diagnosed in childhood has a poor prognosis with up to 59% of
children displaying complicated disease at long-term follow-up (1,2).
University of Virginia Health System, the §Division of Bioinformatics,
Emory and Children’s Research Center, Atlanta, GA, the jjDivision of Despite medical management, the risk of surgery 3 years after
Pediatric Radiology, Emory University Department of Pediatrics, and the diagnosis is 20%, and 5 years after diagnosis is 34% (1). Improving
ôDivision of Radiology, Arizona University School of Medicine, the outcome of pediatric CD is essential in this lifelong disease.
Tucson. Improved outcome and sustained clinical remission has been
Address correspondence and reprint requests to Cary G. Sauer, MD, Emory reported in patients who demonstrated endoscopic remission
University School of Medicine, Division of Pediatric Gastroenterology, and mucosal healing, regardless of treatment (3–7). The use of
Emory Children’s Center, 2015 Uppergate Dr, Atlanta, GA 30322 regular endoscopic surveillance to adjust treatment results in higher
(e-mail: csauer@emory.edu). likelihood of obtaining mucosal healing (8). In addition, a recent
This research was supported by the Crohn’s and Colitis Foundation of evaluation of the Study of Biologic and Immunomodulator Naive
America through a Career Development Award (C.G.S.) and by the
Emory and Children’s Research Institute for Statistical Analysis (C.M.).
Patients in Crohn’s Disease (SONIC) trial suggests that clinical
The authors report no conflicts of interest. symptoms are not a reliable measure of mucosal healing (9). Mucosal
Copyright # 2016 by European Society for Pediatric Gastroenterology, healing as an endpoint of therapy has become the preferred target as a
Hepatology, and Nutrition and North American Society for Pediatric result of mounting data demonstrating improved outcome.
Gastroenterology, Hepatology, and Nutrition Endoscopy can be used to detect mucosal healing in the
DOI: 10.1097/MPG.0000000000000976 colon and terminal ileum; however, when small bowel or ileal

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JPGN  Volume 62, Number 3, March 2016 MRE Healing and Remission Predicts Improved Outcome in Pediatric CD

predominant CD is present, endoscopy may not fully evaluate the through the abdomen and pelvis, including the perineum, including
disease burden. The use of magnetic resonance imaging and other sequences to detect perianal CD. Sedation was not used for any of
cross-sectional imaging techniques to evaluate for mucosal healing the children younger than 6 years (2 patients in this study). All of the
is necessary in many patients. In addition, these techniques do not patients were scanned on a 3T (Magnetom Trio Tim; Siemens
require sedation/anesthesia and can detect additional findings such Healthcare, Erlangen, Germany) or 1.5T (Magnetom Aera; Siemens
as intraabdominal complications that endoscopy cannot evaluate. Healthcare) scanner. The protocol is designed such that there
The utility of small bowel imaging for CD with magnetic is redundancy among the sequences to allow several opportunities
resonance enterography (MRE) has been well established. In to assess the same anatomy in multiple planes. T2-weighted images
pediatric CD, MRE has been shown to be feasible (10–13), useful were acquired in both the axial and coronal planes with a single-shot
for diagnosis (14,15), and to correlate with endoscopy and histo- fast spin echo (ssT2) sequence (380 mm2 field of view [FOV],
pathology (16–18). MRE can detect response to treatment in as 320  224 matrix, 5-mm slice thickness, TR/TE/flip angle ¼ 1500/
little as 2 weeks (19,20). Meanwhile, small bowel imaging with 70/150, acceleration factor of 2.0) both without fat saturation, and
MRE or CT enterography has been shown to be useful in medical with fat saturation using spectral adiabatic inversion recovery
management of CD, and accurate in assessing mucosal healing in technique (27). Axial and coronal 3D T1-weighted gradient echo
patients with CD when compared with ileocolonoscopy (21–25). (T1W GRE) images were obtained in the precontrast phase, and
Recently, a comparison of MRE to balloon enteroscopy of the small then subsequently in the arterial, venous, and delayed phases with
bowel demonstrated similar sensitivities for active inflammation the following parameters: 380 mm2 FOV, 288 matrix (80% phase
(26). resolution), partial Fourier imaging 6/8, TR/TE/flip angle ¼ 3.44/
No studies have evaluated outcome with mucosal healing as 1.25/10o, 104 slices at 2.8-mm slice thickness, and bandwidth at 450
detected by MRE. We sought to evaluate outcome in children with hertz/pixel and 2 times acceleration. Each patient’s weight was
small bowel CD who underwent MRE and determine whether recorded and gadopentetate dimeglumine (Magnevist; Bayer Scher-
healing on MRE resulted in improved outcome. ing Pharma, Berlin, Germany) was administered at a dose of
0.1 mmol/kg and a rate of 2 mL/s, followed by a 20-mL saline
METHODS flush at 2 mL/s using a dual chamber power injector (Spectris;
Medrad, Warrendale, PA). Acquisition time for 3D GRE images
Study Population was 15 to 17 seconds and performed in a single breath hold. Our
A prospectively maintained MRE database for children with protocol does not use antimotility agents. Patients were imaged in
CD at Emory University and Children’s Healthcare of Atlanta was the supine position. Nonsedated patients also received oral contrast
queried retrospectively. All of the children who underwent MRE (450–900 mL Volumen, 60 minutes before imaging), as tolerated.
evaluation greater than 180 days after diagnosis and with at least 1 Additional sequences include diffusion-weighted images, and an
year of follow-up after MRE were included in the study. Each axial steady state free precession sequence was also obtained with a
patient only contributed 1 MRE study for this analysis. All studies single-shot technique (380 mm2 FOV, 320  256 matrix, TR/TE/flip
were ordered by the primary gastroenterologist for clinical reasons, angle ¼ 3.51/1.55/508, 50 slices at 5 mm thickness [no gap], and
and no MRE studies were performed for research purposes. The bandwidth of 1040 hertz/pixel). A coronal, thick section heavily
indication for each MRE was most frequently listed as Crohn T2-weighted sequence (380 mm2 FOV, 384  307 matrix, 60 mm
disease, and therefore specific symptoms could not be evaluated. slice thickness, TR/TE/flip angle ¼ 2000–5000/709/180, accelera-
The study was institutional review board approved for the use of tion factor of 2.0) is then acquired 15 times (each slab acquisition
private health information. between 2 and 5 seconds) to assess the dynamic properties of bowel
motility. Additional T2-weighted sequences were also acquired
Chart Review through the pelvis with ssT2 sequence in the sagittal plane and a
high-resolution, 3-dimensional (3D) turbo spin echo sequence using
A comprehensive chart review was performed to obtain variable flip angles in the axial plane (250 mm2 FOV, 256  257
updated data on physician global assessment (PGA), current medi- matrix, 1-mm slice thickness, TR/TE/flip angle ¼ 1300/97/variable,
cations, and complications. Patients taking mercaptopurine, approximately 5 to 6 minutes acquisition time). When patients were
azathioprine, or methotrexate were considered to be on immuno- unable to breath hold or were sedated, an additional motion-
modulator therapy whereas those on infliximab or adalimumab insensitive pre- and postcontrast T1 fast low-angle shot sequence
were considered to be on biologic therapy. was added for further review.
All of the MRE studies were evaluated by radiologists with
advanced training in MRE interpretation. One of 3 radiologists MRE Interpretation
independently reviewed the study and determined whether it fits
into 1 of 2 categories: MRE Remission and MRE-Active Inflam- One of 3 pediatric radiologists (A.A., K.B., J.L.) with
mation. Chronic disease changes without active inflammation were advanced training in MRE interpretation reviewed each MRE
considered remission. MRE remission defined as lack of active studies and was blinded to the history and clinical symptoms.
inflammation was considered complete MRE healing. MRE studies were reviewed separate from the original clinical
Our primary outcome measure was set before data collection reading. Comparison between the original reading and the reading
as PGA at last follow-up. In addition, we collected data on for the present study was not made because the reading for the
medications, medication changes, and surgery but chose before present study focused only on the presence or absence of
collection of data to not to include more subjective measures of active inflammation.
disease outcome such as hospitalization or symptom index. Active inflammation was defined as abnormal bowel wall
thickening with corresponding increased enhancement on postga-
MRE Protocol dolinium T1W images along with high signal intensity on T2W-
spectral adiabatic inversion recovery technique fat-suppressed
Our MRE protocol consists of a combination of T2-weighted, images. Residual abnormal enhancement with improvement
and dynamic, multiphase contrast-enhanced T1-weighted images in bowel wall thickening and simultaneous recovery of normal

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Sauer et al JPGN  Volume 62, Number 3, March 2016

TABLE 1. Population characteristics

MRE remission MRE active inflammation P

No. patients 36 65
Sex (%)
Male 20 (55.6) 39 (60.0) NS
Female 16 (44.4) 26 (40.0) NS
Age classification (Paris classification)
A1a (<10 y old) 7 15 NS
A1b (10–17 y old) 29 47 NS
A2 (17–40 y old) 0 3 NS

Disease location (Paris classification) (%)
L1 9 (25.0) 13 (20.0) NS
L2 12 (33.3) 12 (18.5) NS
L3 15 (41.7) 40 (61.5) NS
L4a 7 (19.4) 11 (16.9) NS
L4b 5 (13.9) 20 (30.8) NS
Disease behavior (Paris classification)
B1 (nonstricturing, nonpenetrating) 31 46 NS
B2 (stricturing) 5 13 NS
B3 (penetrating) 0 2 NS
B2B3 (penetrating and stricturing) 0 4 NS
P (perianal modifier) 6 8 NS
Median interval in years from diagnosis to MRE (range) 1.5 (0.5–7.6) 1.3 (0.5–8.4) NS
Median disease duration, y (range) 4.5 (1.7–10.3) 4.9 (1.6–12.0) NS
Median follow-up after MRE, y (range) 2.4 (1.1–5.1) 3.2 (1.0–5.5) NS

MRE ¼ magnetic resonance enterography. L1, distal 1/3 ileum  limited cecal disease; L2, colonic; L3, ileocolonic; L4a, upper disease proximal to
Ligament of Treitz; L4b, upper disease distal to ligament of Treitz and proximal to distal 1/3 ileum.

Percentages do not add to 100% because patients can have multiple locations.

T2 signal was determined to be resolution of the active inflam- only CD. CD diagnosis was confirmed based on the presence of a
mation but with underlying fibrosis, and thus would be classified as granuloma, presence of gross endoscopic small bowel disease, and
no active inflammation. Lymph node enlargement, comb sign, and in the case of colonic only CD by expert review (S.K.). Patient
free fluid were not included in the analysis but may have contributed characteristics including disease location, disease duration, and
to the final interpretation. MRE studies were classified as MRE duration of follow-up after MRE were no different between
remission and MRE active inflammation based on the criteria MRE remission and MRE active inflammation groups. Median
above. Active inflammation was classified in an all-or-none interval from diagnosis until the first MRE was 1.3 years and
approach and degree of inflammation was not considered. median follow-up was 2.8 years for our population (Table 1).

Statistical Analysis MRE Results


Statistical analyses were conducted using SAS 9.3 for Win- MRE studies demonstrated 36 children with CD in MRE
dows (SAS Institute, Cary, NC). Statistical significance was remission and 65 children with CD demonstrated MRE active
assessed at the 0.05 level. MRE status was defined as a binary inflammation. Figures 1 and 2 illustrate MRE studies classified
variable (remission, active inflammation). Chi-square tests were as MRE remission and MRE-active inflammation.
used to compare sex, race, treatment, and PGA at follow-up among
the MRE remission group and the MRE active inflammation group. Treatment
For some comparisons, exact chi-square tests were used if the cell
counts were less than 5. In addition, the exact chi-square test was At the time of MRE study, there were no differences in
used to compare treatment among the levels of PGA at follow-up. medications used (immunomodulators vs biologics) between the
The Wilcoxon rank-sum test was used to compare the duration of active inflammation and remission groups. Of those taking immu-
disease among the MRE groups. nomodulator medications as primary therapy, 10 of 33 (30.3%)
patients demonstrated MRE remission. Of those on biologic medi-
RESULTS cations as primary therapy, 26 of 68 (38.2%) patients demonstrated
MRE remission (Table 2).
Demographics and Clinical Characteristics At the time of last follow-up, 3 (8.3%) patients in the MRE
A total of 101 children underwent MRE evaluation greater remission group changed medications, whereas 29 (44.6%) children
than 180 days after diagnosis with at least 1 year of follow-up after in the MRE active inflammation group changed medications.
MRE. Most children in the study demonstrated small bowel disease Medication changes included switching from an immunomodulator
on initial diagnostic staging of CD location based on the Paris to a biologic medication and changing the type of biologic
classification; however, 24 of 101 (23.8%) demonstrated colonic medication used (Table 2).

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JPGN  Volume 62, Number 3, March 2016 MRE Healing and Remission Predicts Improved Outcome in Pediatric CD

A B

FIGURE 1. Remission. A, Coronal T2 spectral adiabatic inversion recovery technique (SPAIR) and (B) T1 postcontrast images at the level of the
pelvis show no abnormal within the bowel walls, but with corresponding thin enhancement (arrows) suggesting chronic, fibrous change.

A B

FIGURE 2. Active inflammation. A, Axial T2 spectral adiabatic inversion recovery technique (SPAIR) and (B) T1 postcontrast images at the level of
the pelvis show abnormal bright signal in a thick-walled segment of distal ileum (arrows) with corresponding enhancement.

Clinical Outcome at Follow-up patients, 17 achieved clinical remission by PGA at follow-up,


5 demonstrated mild disease on PGA at follow-up, 5 demonstrated
In children who demonstrated MRE remission (n ¼ 36), moderate disease on PGA at follow-up, and 2 demonstrated severe
88.9% were in clinical remission at follow-up, with the median disease on PGA at follow-up. In children demonstrating MRE
follow-up of 2.4 years. In patients who demonstrated MRE-active remission, only 1 (2.8%) underwent surgery during the follow-up
inflammation (n ¼ 65), only 29 (44.6%) were in clinical remis- time period, whereas in the MRE active inflammation
sion. Of those patients with active inflammation on MRE, 29 group 12 children (18.5%) underwent surgery during the
(44.6%) underwent a change of medication and of those 29 follow-up period (Table 3).

TABLE 2. Treatment at MRE and long-term follow-up

MRE remission (n ¼ 36) MRE active inflammation (n ¼ 65) P

Treatment at time of MRE (%)


Immunomodulator 10 (27.8) 23 (35.4) 0.435
Biologic 26 (72.2) 42 (64.6)
Treatment at follow-up visit (%)
Immunomodulator 9 (25.0) 7 (10.8) 0.061
Biologic 27 (75.0) 58 (90.9)
Change in medication (%)
Immunomodulator to biologic 1 (2.8) 17 (26.2) 0.003
Biologic change within class 2 (5.6) 12 (18.5) 0.072

MRE ¼ magnetic resonance enterography.

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TABLE 3. Long-term follow-up outcome

PGA at long-term follow-up MRE remission (n ¼ 36) MRE active inflammation (n ¼ 65) P

Clinical remission (%) 32 (88.9) 29 (44.6) <0.001


Mild disease (%) 3 (8.3) 20 (30.8)
Moderate disease (%) 1 (2.8) 11 (16.9)
Severe disease (%) 0 (0) 5 (7.7)
Surgery (%) 1 (2.8) 12 (18.5) 0.024
Any change in medication (%) 3 (8.3) 29 (44.6) <0.001

MRE ¼ magnetic resonance enterography; PGA ¼ physician global assessment.

DISCUSSION continued symptoms and those not responding to their current


Mucosal healing as evaluated by endoscopy is associated treatment, evident by a high percentage with active inflammation.
with improved outcome in multiple studies (3,6,7). Conventional The present use of cross-sectional imaging, however, provides a
endoscopy, however, is invasive, is limited to the distal ileum, and window into its use in clinical practice. Indication for MRE was
requires sedation or anesthesia in children. Data suggest that MRE available but in a vast majority the indication was Crohn disease
can be used to monitor response to treatment, detect active disease and therefore was not useful to analysis regarding symptoms or no
not evident on endoscopy, and demonstrates high correlation with symptoms. We did not use a standardized MRE scoring system for
mucosal healing on endoscopy (20,24). These data suggest that our studies but instead deployed an ‘‘all or none’’ approach as did
MRE may be act as a substitute to endoscopy when evaluating for previous studies evaluating endoscopic healing. We believed this
mucosal healing. manner of grading MRE studies was more akin to grading
There is a paucity of data regarding outcome after demon- endoscopic remission where a Simple Endoscopic Score for
strating healing on cross-sectional imaging. Our study demonstrates CD must be 0 to be considered mucosal healing. Because most
improved outcome in children with MRE remission as compared to MRE scoring systems are difficult to use a recent study demon-
those with active inflammation on MRE. Children achieving MRE strates that T2 hyperintensity was the best marker for active
remission were less likely to have a change in medication or need disease (28). We also chose not to include less objective measures
for surgery and more likely to be in clinical remission at long-term of outcome such as hospitalization or flares as criteria for
follow-up. There was 1 patient in the MRE remission who went on hospitalization and definition of flares can differ greatly. Finally,
to require surgery after developed a small bowel obstruction we did not perform repeat MRE studies or endoscopy at the end of
because of a stricture after he lost response to his primary medi- follow-up because performing these studies on asymptomatic
cation. MRE remission was defined as absence of active inflam- children can be difficult to justify.
mation on MRE and can be considered similar to mucosal healing In summary, we demonstrate superior outcome in children
on endoscopy. The present study further supports emerging data with CD who demonstrate MRE remission. Children with CD who
that objective findings of remission by endoscopy or imaging are demonstrate MRE remission were less likely to change medi-
associated with improved outcome (6,8). cations, less likely to require surgery, and were more likely to
One of the advantages of MRE is evaluating proximal small be in clinical remission at follow-up. The present data suggest that
bowel CD. In our study, more than 40% of our patients had Paris demonstrating healing with MRE may be an effective alternative to
classification L4a or L4b. Because demonstrating mucosal healing endoscopy, and should be considered when lesions are beyond the
in these patients would require small bowel enteroscopy, the use of reach of standard endoscopy. More prospective studies in children
serial imaging in lieu of endoscopy would be preferable as this is an are necessary to determine whether MRE can be used as a surrogate
advanced endoscopic procedure not available at all pediatric cen- to endoscopy in evaluating mucosal healing.
ters. Knowing that MRE can demonstrate mucosal healing is critical
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