Magnetic Resonance Imaging of the Gut: A Primer for the ... computed tomography (CT) and magnetic ... increased susceptibility to motion artifact and local fi eld ... manganese ions

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© 2014 by the American College of Gastroenterology The American Journal of GASTROENTEROLOGY

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CLINICAL AND SYSTEMATIC REVIEWS

INTRODUCTION Fluoroscopy of the alimentary tract is not obsolete, but it has

moved from being the fi rst-line study for evaluation of the patient

presenting with gastrointestinal (GI) symptoms to a problem-

solving tool. Both computed tomography (CT) and magnetic

resonance imaging (MRI) off er advantages over traditional fl uor-

oscopic techniques, especially for evaluation of extraluminal com-

plications of GI disease. CT is the most utilized imaging modality

for patients with nonbiliary symptoms, and nonspecifi c and acute

abdominal pain. However, MRI evaluation of the solid organs of

the abdomen is well established and it has an increasing role in the

evaluation of bowel disease.

Th e physics of MRI is complex and will be addressed only briefl y

( 1 ). Clinical MRI is based on the interaction of protons and radi-

ofrequency waves in the presence of a strong external magnetic

fi eld. Unlike CT imaging, MRI does not use potentially harm-

ful ionizing radiation. Magnet strength is measured in Tesla (T)

and ranges from 0.1 to 3 T for clinical body imaging. Higher fi eld

strength can result in the higher spatial and temporal resolution

needed for imaging the bowel; currently, imaging the GI tract is

optimal at high fi eld strength (1.5 and 3 T). Ultrahigh fi eld MRI

scanning can go as high as 15 T, but such high fi elds are restricted

to preclinical research.

Images of the patient are obtained through a multistep process of

energy transfer and signal transmission. When the patient is placed

in the magnet, mobile protons associated with fat and water align

parallel to the external magnetic fi eld. A radiofrequency pulse is

then applied, causing the protons to move from their lower, stable

energy state to a higher, unstable energy state (excitation). When

the radiofrequency pulse is removed, the protons “ relax ” and emit

a radio signal that is captured by a receiving coil and reconstructed

into images through a complex mathematical algorithm: the Fou-

rier transform. Diff erent tissues have diff erent relaxation rates that

lead to diff erent levels of signal intensity (SI) on the reconstructed

image. Tissue with a high SI (e.g., fat) is brighter than a tissue with

low SI (e.g., cortical bone). Th e diff erence in SI is called tissue con-

trast.

T1 and T2 are parameters of relaxation that vary by tissue type

and the acquisition program. Multiple pulse sequences are acquired

for MRI imaging. A pulse sequence is a set of defi ned radiofre-

quency pulses and timing parameters used to acquire image data.

Th e data are acquired in volumes (voxels), reconstructed as two-

dimensional pixels and displayed relative to tissue SI variations

(tissue contrast). At diff erent points in the examination, acquisi-

tion is programmed to accentuate T1 and T2 contrast weighting.

In T1-weighted sequences, fl uid appears black (low SI) and in T2-

weighted sequences fl uid appears white (high SI). With the addi-

tion of functional imaging sequences, such as diff usion-weighted

imaging (DWI), areas of active infl ammation, fi brosis, and highly

cellular neoplasm become more conspicuous.

Th e absence of ionizing radiation, superior tissue contrast, and

dynamic abilities of MRI are particularly well suited for address-

ing the clinical questions commonly encountered in luminal

gastroenterology practice. Compared with CT, the weaknesses

of MRI include lower spatial resolution, longer acquisition

times, increased susceptibility to motion artifact and local fi eld

Magnetic Resonance Imaging of the Gut: A Primer for the Luminal Gastroenterologist Miriam Romero , MD 1 , James L. Buxbaum , MD 2 and Suzanne L. Palmer, MD 1

Magnetic resonance imaging (MRI) is well established for imaging the solid organs of the abdomen and pelvis. In recent years it has been having an increasingly important role in the evaluation of the gastrointestinal (GI) tract. Fluoroscopy and abdominal computed tomography, the traditional mainstays of bowel imaging, remain valuable; however, the contemporary emphasis on decreasing patient radiation exposure is driving practice toward non-ionizing modalities such as MRI. The inherent dynamic properties of MRI, its superior tissue contrast, and cross-sectional capabilities offer additional advantages. Here we review, from esophagus to anus, techniques and indications for MRI of the GI lumen with an emphasis on the normal MRI appearance of the GI tract and commonly encountered pathology. Am J Gastroenterol 2014; 109:497–509; doi: 10.1038/ajg.2013.452; published online 7 January 2014

1 Department of Radiology, Keck School of Medicine, University of Southern California , Los Angeles , California , USA ; 2 Department of Internal Medicine, Gastroenterology, Keck School of Medicine, University of Southern California , Los Angeles , California , USA . Correspondence: Suzanne L. Palmer, MD , Department of Radiology, Keck School of Medicine, University of Southern California , 1500 San Pablo Street , 2nd Floor Imaging, Los Angeles , California 90033 , USA . E-mail: [email protected] Received 4 July 2013; accepted 24 November 2013

The American Journal of GASTROENTEROLOGY VOLUME 109 | APRIL 2014 www.amjgastro.com

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Romero et al .

inhomogeneity, more limited scanner access, and higher cost. In

addition, the longer required imaging time may not be suitable in

critically ill patients. Morbidly obese patients may not fi t into many

scanners and claustrophobic patients may require sedation or anx-

iolytic medication. However, if properly used , MRI can serve as an

excellent problem-solving tool.

IMAGING TECHNIQUES Patient preparation for routine abdominal pelvic MRI is straightfor-

ward. Fasting for 4 – 6 h before the study is recommended to reduce

bowel peristalsis, minimize intraluminal residue, and optimize vis-

ualization of the biliary system, which is part of the diff erential in

most patients presenting with abdominal symptoms. Unlike solid

organs, the bowel can be easily displaced and distended. Collapsed

loops can both simulate and obscure pathology; therefore, if enteric

imaging is desired, attention to good bowel distension is mandatory.

Th ere are several specialized protocols that require specifi c prepara-

tion. MR enterography (MRE) techniques require a large volume of

oral contrast. MR colonography (MRC) techniques require bowel

cleansing preparation, similar to that used for CT colonography

(CTC) and optical colonoscopy, as well as colonic contrast.

Luminal contrast agents are categorized based on their T1 and

T2 SI ( Figure 1 ). Positive agents have high SI on both T1- and

T2-weighted sequences. Examples include dilute gadolinium

chelates (Gd-C), manganese ions (some fruit juices contain high

levels), high-fat milk, and ferrous ions. As positive agents may

mask mural enhancement on post-contrast sequences, they are

not recommended. Negative agents have low SI on both T1- and

T2-weighted sequences. Perfl uorooctyl bromide, ferumoxide, and

room air are among the available options ( 2 ). Inner loop abscess

visualization is improved with such agents, but susceptibility arti-

fact from these agents may be accentuated. Th e most commonly

used agents are biphasic, low SI on T1-weighted sequences, and

high SI on T2-weighted sequences. Th ese agents off er high con-

trast between the high SI lumen and low SI bowel wall on T2-

weighed sequences without masking abnormal enhancement on

T1-weighted sequences. Water, methycellulose, mannitol, sorbitol,

polyethylene glycol, pineapple juice, blueberry juice, low-fat milk,

and dilute barium are biphasic agents ( 3,4 ).

An optimal oral contrast agent is reasonably palatable, optimizes

luminal distension, has minimal side eff ects, is readily available,

and is inexpensive. Water satisfi es four of the fi ve criteria, but is

absorbed across the intestinal mucosa, limiting distension. Poly-

ethylene glycol and mannitol have limited absorption by the bowel;

however, their cathartic eff ects oft en cause diarrhea ( 5 ). Dilute

barium sulfate (98 – 99 % water) provides good bowel distension,

is well-tolerated, and relatively inexpensive ( Figure 2a ). Low-fat

milk may be used with good results as well.

Patients may drink up to 1,200 – 1,500 cc of oral contrast, espe-

cially if the distal small bowel is the area of interest. Th e optimal

volume of contrast, the speed of contrast ingestion, and time to

imaging can vary greatly in patients with diff erent pathologic

processes and disease activity. Incomplete luminal distention is a

common problem, particularly in the jejunum. As collapsed bowel

loops can both obscure and mimic disease, some tailoring may have

to be done on an individual basis. For foregut imaging, up to 1 liter

of water is given within 15 min of imaging; for small bowel imag-

ing to the level of the cecum, the patient typically begins ingesting

dilute barium sulfate 90 min before imaging ( 6 ); if small and large

bowel contrast is desired, ingestion of dilute barium sulfate may be

started 3 – 4 h before the examination.

Rectal contrast is not generally used; however, rectal contrast

may be helpful for evaluating anorectal pathology. Luminal

Contrast T2 T1

Positive

Negative

Biphasic

Figure 1 . Positive agents produce high signal intensity (SI) on both T1-weighted (T1W) and T2-weighted (T2W) sequences. Negative agents pro-duce low SI on both T1W and T2W sequences. Biphasic agents produce high SI on T2W and low SI on T1W sequences.

La b c

*

L L

* *

Figure 2 . Biphasic contrast agent appearance: 2 % barium sulfate on coronal T2-weighted (T2W) image ( a ) and coronal T1-weighted (T1W) post contrast with antiperistaltic agent image ( b ). Coronal T1W image without anti peristaltic agent ( c ). * Normal stomach with adequate contrast distension; arrows, normal jejunum; L, liver.


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Magnetic Resonance Imaging of the Gut

MRI may be performed in all trimesters. Many institutions,

including ours, require patients to sign informed consent before

the examination. Protocols for pregnant patients rely on unen-

hanced imaging. Gadolinium crosses the placental barrier, and

fetal risk associated with gadolinium exposure remains unknown;

thus, these agents should not be routinely used in pregnancy.

IMAGING FINDINGS Esophagus and stomach Fluoroscopic esophagography remains the mainstay of nonopti-

cal imaging for evaluation of the esophagus. Motility studies are

readily performed with fl uoroscopy, and post-operative perfora-

tions are easily demonstrated. However, MRI has potential value

in the assessment of gastroesophageal junction anatomy and refl ux

( 14,15 ), including elucidating the structures at the gastroesophageal

junction and proximal stomach that constitute the refl ux barrier.

MRI has potential use in dynamic swallow studies, but further cor-

relation with manometry and video fl uoroscopy is needed ( 16 ).

For esophageal carcinoma staging, CT remains the accepted

imaging modality, but MRI can potentially provide detailed ana-

tomic information ( 17 ), and sequences coned down to the poste-

rior mediastinum may be helpful for problem solving in diffi cult

cases or when iodinated contrast is contraindicated ( Figures 3a

and b ). MRI can aid in the evaluation of both congenital lesions and

post-operative changes ( Figures 4a and b ). Hiatal hernia is a com-

mon incidental fi nding easily recognized on MRI ( Figure 5 ). MR

esophagography has also been favorably compared with conven-

tional MRI in tumor localization, tumor length, and staging ( 18 ).

Normally, the gastric wall should appear as a thin, uniform, low

SI line on T2-weighted imaging, measuring 2 – 3 mm in thickness

( Figure 2a ). Gastric rugae may increase the apparent thickness of

the gastric wall when prominent, but may be diff erentiated from

pathology, as normal rugae will enhance homogeneously with the

rest of the stomach wall ( Figure 2b ). Mural thickening secondary

to gastritis is typically diff use and SI is brighter on T2-weighted

images due to edema ( Figure 6 ). In contrast, gastric cancer results

in focal wall thickening that appears slightly higher in SI on T2-

weighted images, intermediate SI on T1-weighted images, and with

heterogeneous enhancement on post contrast images ( Figures 7a,b

and 8 ) ( 19,20 ). Linitis plastica will have lower T2-weighted signal

than other gastric cancers because of its desmoplastic nature and

does not enhance as brightly with contrast ( 20 ). Lymphadenopathy

and hepatic metastases are well demonstrated on MRI; however,

additional work is needed to establish its effi cacy in staging gastric

cancer ( 21 – 23 ) .

Over the course of the last decade, the applicability of MRI for

the evaluation of gastric emptying and gastric motility has been

examined and preliminary results are favorable ( 24 ). However,

fl uoroscopic swallowing studies and nuclear medicine gastric

studies are less costly and less time intensive.

Small bowel Historically, the small bowel has presented the greatest imaging

challenge because of its relative inaccessibility and long length.

contrast distends the rectal lumen and can increase the con-

spicuity of the abnormal wall SI, thickening, and enhance-

ment. Either aqueous gel or water may be used. Approximately

60 – 120 cc of gel are administered before the beginning of the

examination or water may be instilled via Foley under gravity

during the study. Either a surface coil or an endorectal coil may

be used; although an endorectal coil may provide better spa-

tial resolution, its narrow fi eld of view and associated patient

discomfort are signifi cant drawbacks. Endorectal coils may also

distort adjacent structures.

Bowel motion can degrade a study; therefore, administration

of an antiperistaltic agent is recommended for enteric imaging

( Figures 2b and c ). Th e antiperistaltic is administered at the begin-

ning of the examination, when the patient is placed on the MRI

table. Th e choice of antiperistaltic is based on familiarity with and

access to the agent. Frequently used agents include glucagon and

butylscopolamine, although the latter is not FDA approved for use

in the United States. Glucagon may be administered intravenously

(IV) or intramuscularly. A tuberculin syringe is used for intramus-

cular injection and its small gauge causes relatively little discomfort

during injection. However, IV injection may have faster onset and

longer duration of anti-peristaltic eff ects than intramuscular injec-

tion ( 7 ). Sublingual or IV Levsin may also be administered ( 8 ). IV

injection of glucagon may be associated with increased nausea and

vomiting. At our institution, patients undergoing routine abdominal

MRI are positioned supine on the table, whereas patients undergoing

MRE and MRC examinations may be positioned prone to maximize

abdominal compression, provide maximal bowel coverage on coro-

nal images, and separate bowel loops. However, for patient comfort

reasons, patients may be imaged the supine position ( 9 ).

MRI imaging should be performed on a high fi eld magnet (1.5 –

3 T). Evaluation of the GI tract relies on rapid acquisition sequences

while the patient holds their breath, although free breathing

sequences may be used. Approximately 30 – 40 min are allotted for

each examination. IV contrast is routinely used in enteric imaging,

and Gd-C are the contrast agents of choice. Administration of Gd-

C should be avoided in patients with acute kidney injury, end-stage

or severe chronic kidney disease, as these patients are at higher risk

of nephrogenic systemic fi brosis, a potentially life-threatening con-

dition. Th ere is no absolute estimated glomerular fi ltration rate cut-

off below which Gd-C cannot be administered; however, the use

of Gd-C should be avoided when the estimated glomerular fi ltra-

tion rate is < 30 ml / min per 1.73 m 2 ( 10,11 ). Th is is not an absolute

contraindication; the use of Gd-C should be at the discretion and

judgment of the ordering physician. If possible, alternative imaging

should be considered. If contrast-enhanced MRI is necessary this

should be documented in the patient ’ s record, and if the patient is

on hemodialysis the MRI should be scheduled immediately before

dialysis. Although Gd-C agents are eff ectively removed with hemo-

dialysis, no published report has proved that early dialysis prevents

the development of nephrogenic systemic fi brosis ( 10 – 13 ). Specifi c

agents are contraindicated in patients with estimated glomeru-

lar fi ltration rate < 30 ml / min per 1.73 m 2 , including nonionic

linear Gadodiamide and Gadoverssetamide, and Gadopentetate

dimeglumine; hence, alternative Gd-C agents should be used ( 10 ).


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Romero et al .

Th e traditional small-bowel series does not distend the small

bowel reliably, and enteroclysis requires uncomfortable nasojeju-

nal intubation ( 25 ). Neither modality gives direct visualization of

extraluminal pathology. CT enterography and MRE have high res-

olution for evaluating enteric and nonenteric changes of the small

bowel. Crohn ’ s disease is the leading indication for cross-sectional

small bowel imaging. In addition to the morbidity associated with

infl ammation, Crohn ’ s disease is complicated by fi stulas, stric-

tures, obstruction, abscesses, and cancer. CT enterography and

MRE have been found to be equally accurate in detecting active

small bowel infl ammation and the extra-enteric complications of

Crohn ’ s disease, despite increased motion artifact on MRE ( 26 ).

Consensus guidelines endorse both MRE and CT enterography

( 27 ). However, CT exposes patients to ionizing radiation and

should be used judiciously in patients who may be imaged multi-

ple times, such as those with infl ammatory bowel disease, as these

patients are typically young and may require multiple studies over

the course of their lifetimes ( 28,29 ).

Capsule endoscopy allows direct mucosal evaluation of the small

bowel while minimizing patient discomfort ( 30 ). However, the

capsule cannot be maneuvered, and luminal narrowing may result

in a mechanical obstruction ( 30 ). Although we do not routinely

perform small bowel follow-through before capsule endoscopy,

given the low likelihood of retention, clinical history suggestive

of obstruction mandates a fl uoroscopic study to exclude strictures

( 31 ). Albert et al. ( 32 ) have shown MRI to have comparable sensi-

tivity to capsule endoscopy in the detection of small bowel Crohn ’ s

disease, while simultaneously allowing evaluation of extra-intesti-

nal disease.

Th e diff erent segments of small bowel have a very characteris-

tic normal MRI appearance. Normally, the small bowel measures

no more than 3 cm in diameter and the wall measures no more

than 3 – 4 mm in thickness. Th e jejunum should have no fewer

than threefolds per inch; the ileum may have up to fi vefolds per

inch. Findings associated with Crohn ’ s disease include wall thick-

ening and increased enhancement, both of which vary depend-

ing on disease activity. In the setting of acute infl ammation, the

thickened bowel wall will have higher SI on T2-weighted images,

and intense enhancement on post-contrast sequences ( Figures 9a

and b ). Chronically aff ected bowel loops are of lower SI on

Ha

b

Figure 3 . Appearance of the normal esophagus on sagittal T1-weighted (T1W) ( a ) and axial T2-weighted (T2W) ( b ) images (arrows). The esopha-gus is typically intermediate in signal intensity.

a

b

a

b

Figure 4 . Sixty-one-year-old male status post esophagectomy for esopha-geal cancer. Coronal T2-weighted (T2W) ( a ) and axial post contrast T1-weighted (T1W) ( b ) images demonstrate a normal, posterior mediastinal gastric pull-up with normal gastric wall enhancement (arrows).


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as linear bowel wall protrusions. Avidly enhancing lymph nodes,

mesenteric edema, and engorged vasa recta have been associated

with active disease. Mesenteric fi bro-fatty proliferation around

infl amed bowel supports a diagnosis of Crohn ’ s disease ( 37 ).

Acute complications of Crohn ’ s disease such as small bowel

obstruction, ileus, and bowel leak, may be seen on MRI ( Figures 11

and 12a, b ), but the availability in the acute care setting allows CT

to remain the imaging modality of choice for the patient present-

ing with acute abdominal symptoms. More chronic complications,

T2-weighted images, with delayed rather than early enhance-

ment on post-contrast sequences. Mildly increased enhancement

in non-thickened bowel should be approached cautiously, as it

can lead to false positives. Th e multiphasic capabilities of MRE

allow diff erentiation of strictures from areas of non-distension, as

strictures will persist over time ( 33 ). At our institution, we obtain

ultrafast single shot T2-weighted spin echo imaging in the coro-

nal plane at the beginning and at the end of the examination to

help diff erentiate fi xed lesions from areas of narrowing due to

peristalsis. Coronal plane single shot T2-weighted spin echo cine

imaging, before antiperistaltic medication onset of action, can

also be used to evaluate for persistent stricture and dysmotility

( 34 ). Areas of stenosis may be associated with prestenotic dilata-

tion ( Figures 10a and b ) ( 35 ).

MRI does not demonstrate early and superfi cial ulceration rou-

tinely due to limited spatial resolution ( 36 ). In these patients, cap-

sule endoscopy should be considered. Deep ulcerations of Crohn ’ s

disease may be identifi ed on both T1- and T2-weighted sequences

L

*

S

K

K

Figure 5 . Coronal T2-weighted (T2W) image of incidentally identifi ed, moderate-sized hiatal hernia (arrow). L, liver; S, spleen; K, kidney; * adrenal gland.

LS

*

Figure 6 . Firty-seven-year-old male with abdominal pain. Axial T2-weighted (T2W) image demonstrates diffuse gastric wall thickening (}) and increased signal (arrow). Acute gastritis was demonstrated on upper endoscopy . L, liver; S, spleen; * ascites.

G

L

a

b

K

P

S

K

G

L P

S

KK

Figure 7 . Foty-fi ve-year-old female presenting with vague abdominal pain. Axial T2-weighted (T2W) ( a ) and T1-weighted (T1W) with fat suppression ( b ) images demonstrate gastric wall thickening with intermediate signal intensity (SI). Biopsy revealed gastric carcinoma. L, liver; P, pancreas; K, kidney; G, gallbladder; S, spleen.

L

*

*

Figure 8 . Thirty-seven-year-old female with gastric cancer. Coronal T1-weighted (T1W) post-contrast image demonstrates irregularly thickened, enhancing gastric wall (large arrowhead) consistent with gastric carcinoma. A stent (arrow) was placed to relieve obstructive symptoms. Small bowel (small arrowheads) is thickened due to peritoneal disease. L, liver; * ascites.


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Romero et al .

including fi stulas, sinus tracts, and adhesions are well characterized

on MRI ( Figure 13 ). Fistulas appear high in signal on T2-weighted

imaging and the walls avidly enhance following the administration

of IV contrast.

Bowel wall thickening, fold density, and increased enhancement

are not specifi c to Crohn ’ s disease. For example, both increased

and decreased numbers of jejunal folds may be seen in celiac dis-

ease ( 38 ). Other forms of enteritis can also present with similar

MRI fi ndings; therefore, the distribution of enteric pathology and

the presence or absence of nonenteric fi ndings should be corre-

lated with the clinical presentation and history in order to increase

accuracy of the diagnosis ( Figure 10a ).

Small bowel tumors, although uncommon, may be encountered

( Figures 14 and 15 ). Malignant lesions include adenocarcinomas

( Figure 15 ), lymphomas, GI stromal tumors, and carcinoids. Both

Van Weyenberg et al. ( 39 ) and Masselli et al. ( 40 ) have demon-

strated a high accuracy of MR enteroclysis for diagnosis of small

bowel neoplasms in patients suspected of having a small bowel

malignancy, although it remains an emerging technique, and MRI

may have a role in the surveillance of polyposis syndromes. MRI

may not be as sensitive in the detection of smaller polyps as capsule

endoscopy ( 41 ). However, for polyps > 15 mm, MRI has a detection

rate similar to capsule endoscopy, and MRI also localizes polyps

more accurately ( Figure 16 ) ( 42 ). Although small bowel assess-

ment is critical for Peutz Jeghers, the role for surveillance beyond

the duodenum in other polyposis syndromes, whether by imaging,

capsule, or deep enteroscopy, has not been validated ( 43,44 ).

Appendix Well-established and readily available, CT is ideal for the diagnosis

of appendicitis and its complications in adults. MRI provides an

alternative in children and pregnant patients, for whom ionizing

radiation is particularly undesirable ( 45,46 ). MRI has demonstrated

high specifi city and sensitivity for appendicitis in pediatric and

pregnant patients, with 100 % sensitivities reported for both popu-

lations. Negative laparotomy rates in pregnant women can also be

decreased without increasing the perforation rate ( 47 ). MRI has

also been shown to be cost eff ective in pregnant women with sus-

pected appendicitis following indeterminate ultrasound (US) ( 48 ).

Leeuwenburgh et al. ( 49 ) demonstrated similar accuracy between

MRI and CT for the detection of MRI in adult patients ( 50,51 ).

No deleterious eff ects of MRI on the fetus have been documented

and MRI can be performed at any stage of pregnancy. However,

B

a

b

B

Figure 9 . Fifty-eight-year-old male with Crohn ’ s disease. Coronal T2-weighted (T2W) ( a ) and T1-weighted (T1W) post-contrast ( b ) images demonstrate changes at the level of the terminal ileum and ileocecal valve, including wall thickening and edema, increased wall enhancement, and a pseudopolyp (white arrow). The remainder of the ilium (dashed oval) and jejunum (oval) are normal. B, bladder.

a

b

Figure 10 . Seventy-one-year-old female status post external beam radia-tion therapy for cervical cancer. Coronal T1-weighted (T1W) post-contrast image ( a ) reveals abnormally increased ileal wall enhancement consist-ent with radiation ileitis (arrow). This is associated with dilatation of the proximal small bowel. Spot image from an X-ray small bowel follow-through confi rms the fi ndings ( b ). Direct compression accentuates the persistent narrowing and abnormal separation of the involved loops of ileum.


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Pediatrics, and General Surgery departments. Th e fi rst examina-

tion performed is a targeted right-lower quadrant US to identify

the appendix. If the study is equivocal MRI is then performed,

and if positive the patient is sent for surgery. Conversely, a normal

appendix excludes the diagnosis of appendicitis, and other poten-

tial causes of abdominal pain should be sought ( 51 ).

Neither IV nor oral contrast is required for MRI evaluation

of acute appendicitis. MR contrast agents pass through the pla-

centa and enter the fetal circulation; the risk to the fetus remains

unknown ( 50 ). A gravid uterus will displace the appendix from its

usual location, requiring a thorough inspection to correctly iden-

tify it. As on both CT and US, the appendix can be recognized

as a blind-ending tubular structure originating from the cecum.

A thickened ( > 6 mm) and edematous appendiceal wall and adja-

cent infl ammatory changes support the diagnosis of acute appen-

dicitis. Abscesses that may develop in cases of perforation are well

demonstrated on MRI. DWI sequences may be useful in making a

subtle case of appendicitis more conspicuous ( Figures 17a and b ).

Colon Most colonic MRI is performed to evaluate known infl ammatory

or neoplastic disease. CTC has been more extensively validated

we routinely consent pregnant patients before imaging ( 52,53 ). At

our institution, we have developed an imaging algorithm for these

patient populations in conjunction with the Emergency Medicine,

L

G

B*

Figure 11 . Sixty-year-old male presenting with renal failure and abdominal distention. Coronal T2-weighted (T2W) image demonstrates diffusely dilated, fl uid fi lled loops of small bowel and diffuse ileal wall edema. No point of obstruction was found and distention resolved with dialysis, consistent with ileus. L, liver; G, gallbladder; B, bladder; * ascites.

a

b

Figure 12 . Thirty-nine-year-old male presenting with diffuse abdominal pain. Axial T1-weighted (T1W) image ( a ) demonstrates a crescentic region of low signal (extraluminal gas, arrow) with fl uid adjacent to a short seg-ment of small bowel with mild wall irregularity (dashed oval). Computed tomography (CT) confi rms the presence of extraluminal gas and fl uid, consistent with small bowel perforation ( b ).

Figure 13 . Fifty-nine-year-old male with Crohn ’ s disease and a history of multiple surgeries presenting with abdominal pain. Axial T2-weighted (T2W) image demonstrates an adhesion (arrow) extending from the sig-moid colon (large arrowhead) to a loop of small bowel (small arrowhead). Whether this adhesion resulted from healing of an ileocolonic fi stula to the sigmoid or prior surgery could not determined, but fi stula was favored given the location.

Figure 14 . Sixty-fi ve-year-old woman with abdominal pain. Coronal T2-weighted (T2W) image demonstrates an exophytic, subserosal mass involving the second portion of the duodenum (arrow), consistent with gastrointestinal stromal tumor (GIST).


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Romero et al .

and is currently favored over MRC outside of research protocols,

especially in patients who cannot undergo optical colonoscopy.

Kuehle et al. ( 54 ) showed a sensitivity and specifi city of 83 % and

90 % , respectively, for MRC in detecting polyps ≥ 5 mm; the ACRIN

study showed a sensitivity for CTC of 90 % for detecting polyps

≥ 10 mm with a sensitivity for polyps ≥ 5 mm of 65 % ( 55 ). Although

MRC compares favorably with CTC, work in this area remains in

earlier stages with overall polyp sensitivities ranging from 28.5 %

to 100 % reported ( 56 ). Th e challenges of MRC are similar to those

of CTC and most are related to bowel preparation. Fecal tagging

may reduce the amount of bowel preparation needed or elimi-

nate it altogether, but this technique is not fully optimized and

sensitivity remains poor ( 57,58 ). Dark lumen and bright lumen

MRC are the two major techniques. Insuffl ated room air, CO 2 ,

and warm tap water are the most frequently used types of dark

lumen contrast. However, gas can cause artifacts, although there

remains debate on the severity of the induced artifacts ( 59 ). Both

barium and Ferumoxsil can be used as dark lumen tagging agents.

For dark lumen MRC, IV Gd is used; carcinoma will enhance,

whereas polyps will not ( 59 ). Dilute Gd-C enema may be used in

bright lumen techniques or T2 imaging may be performed with

water enemas. As more Gd is needed for an enema than for an

IV injection, bright lumen MRC will be more expensive. Air may

also simulate a fi lling defect on bright lumen MRC and the ben-

efi ts of contrast enhancement for evaluating both colonic lesions

and extraluminal disease is lost ( 59 ). As in CTC, most imaging is

performed in both supine and prone positions ( 56 ).

MRC has demonstrated high sensitivity for polyps > 1 cm,

although it does not reliably identify polyps < 5 mm ( 60 ). How-

ever, as small polyps tend to remain stable for 3 – 5 years without

undergoing malignant degeneration, this limitation may not be

clinically signifi cant. In addition, polyps < 6 mm found on CTC

are not reported. Graser et al. ( 61 ) recently compared the diagnos-

tic accuracy of optical colonoscopy, MRC, and fecal occult blood

testing for the detection of colonic neoplasia in asymptomatic

patients. MRC detected adenomas ≥ 6 mm with high sensitivity

and specifi city, although levels of sensitivity remained lower than

optical colonoscopy ( 61,62 ).

CT also remains the recommended modality of choice for stag-

ing colon carcinoma; however, because of MRI ’ s superior tissue

contrast, staging of known colon carcinoma is recommended

when contrast-enhanced CT is contraindicated ( 63 ). Tumor exten-

sion into the adjacent fat, lymph nodes, and the presence of perito-

neal disease and distant metastatic disease may be evaluated using

MRI.

MRE is the preferred technique for evaluating both small bowel

and colonic involvement by infl ammatory bowel disease; how-

ever, recent studies have suggested that MRC with DWI can detect

infl ammation related to infl ammatory bowel disease, particularly

ulcerative colitis (UC), without the need for bowel preparation or

oral contrast ( 64 ). UC changes extend proximally from the rectum

without the skip lesions typically seen in Crohn ’ s disease ( Figure 18 ).

Mucosal erosions develop in active UC with adjacent “ pseudopol-

yps ” composed of edematous, heaped mucosa. Pseudopolyps,

representing areas of residual mucosa between areas of ulceration

and denuded mucosa, are also well characterized on MRI. Chronic

UC will lead to shortening of the colon and loss of normal haus-

tral folds, creating a “ lead pipe ” appearance ( Figure 19 ). As it is

not a transmural process, UC is not associated with fi stula and

abscess formation. Complications of UC such as toxic megacolon

can be readily imaged. Th e MRI appearance of UC is similar to

Crohn ’ s disease: thickened bowel with abnormal enhancement.

Isolated colonic involvement may be seen in Crohn ’ s disease, and

when limited to the anorectal region and distal colon, may not be

Figure 15 . Eighty-one-year-old female with abdominal pain. Coronal T2-weighted (T2W) image demonstrates abnormal wall thickening of the second portion of the duodenum (arrow). Although nonspecifi c, the length of involvement (short) and the intermediate signal intensity favor neoplasm over infl ammation / infection. Pathology revealed a poorly differentiated adenocarcinoma.

a

b

Figure 16 . Sixty-seven-year-old female with an ileal polyp found by wire-less capsule video endoscopy, located 10 min from the ileocecal (IC) valve. Axial T2-weighted (T2W) ( a ) and coronal T1-weighted (T1W) post-contrast ( b ) images from magnetic imaging enterography (MRE) show a low T2 signal intensity (SI) polyp with enhancement located ~ 15 cm from the IC valve (arrow). The polyp and location were confi rmed with biopsy via colonoscopic approach.


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T2 and T3 tumors because of the same desmoplastic reaction that

is problematic for EUS.

High resolution (3 mm) T2-weighted sequences can diff erenti-

ate the layers of the rectal wall allowing for T staging within the

TMO staging system ( Figure 22b ). Tumor appears slightly hyper-

intense relative to muscle on T2 imaging and hypointense relative

to the submucosal and mesorectal fat. IV contrast is not necessary

as it has not been shown to increase staging accuracy ( 70 ), and

although the use of endoluminal contrast is controversial aque-

ous gel may help defi ne the endoluminal component of the tumor.

An endoluminal coil is not necessary for imaging rectal cancer;

although it may improve resolution, increased patient discomfort

limits its use. As with EUS, high rectal tumors and lesions causing

stenosis are inadequately evaluated by endoluminal MRI.

Stage T2 tumors invade but do not penetrate the muscularis pro-

pria, whereas T3 tumors invade through the muscularis propria

and into the subserosa ( Figure 22 ). However, diff erentiating T2 and

T3 tumors may be diffi cult. T2 lesions may be overstaged because

of the diffi culty in distinguishing whether an irregular outer rectal

wall border represents infl ammation from desmoplastic reaction

or tumor and fi brosis together ( 70 ). Extramural vascular invasion,

a predictor of local and distant recurrence, can be identifi ed on

MRI as intermediate SI material expanding the vessel ( 70 ). Th is

represents at least T3. Stage 4 tumors invade adjacent organs and

structures, or have perforated the peritoneum.

Neoadjuvant chemoradiation therapy is oft en used in cases of

extramural spread in T3 – T4 tumors. By downstaging and down-

sizing locally advanced cancers, pre-operative chemoradiation ide-

ally improves resectability, decreases local recurrence, preserves

sphincter function in low tumors, and improves survival ( 71 ).

Restaging MRI can demonstrate a reduction in tumor volume,

decrease in size and number of lymph nodes ( 71 ), as well as help

decide surgical approach. If the residual tumor is confi ned to the

distinguishable from UC. MRE may be helpful in clarifying a

patient ’ s diagnosis by identifying skip lesions that are characteristic

for Crohn ’ s disease versus the contiguous disease characteristic of

UC ( Figure 20 ). Bowel wall thickening is a nonspecifi c fi nding, and

its distribution, the clinical setting, and additional radiological fi nd-

ings should be correlated in arriving at a diagnosis ( Figure 21 ).

Rectum Th e prognosis of rectal cancer depends largely on the degree of

rectal wall tumor infi ltration and regional lymph node involve-

ment. Both endoscopic US (EUS) and MRI have been used for

staging the primary cancer, and although some studies have sug-

gested that EUS is more accurate ( 65,66 ), others have demon-

strated comparable results for MRI ( 67 ). Accuracies for T staging

ranging from 63 to 97 % have been reported for EUS and between

65 and 86 % for MRI ( 68,69 ). Unlike EUS, MRI is able to evalu-

ate stenosing and high rectal tumors, and simultaneously image

the entire pelvis to evaluate for adjacent organ invasion and lym-

phadenopathy ( Figure 22a ). MRI is also less operator-dependent.

Outside of high volume centers, EUS has shown decreased accu-

racies and sensitivities, primarily because of operator variability

( 68,69 ). EUS is very accurate for discriminating between T1 and

T2 tumors, and Puli et al. ( 69 ) demonstrated sensitivities and spe-

cifi cities of 96 % and 91 % , respectively, for T3 lesions and of 95 %

and 98 % , respectively, for T4 lesions. Most MRI staging failures

occur in diff erentiating T1 and T2 lesions because the submucosal

layer is not visualized on phased array MRI and in diff erentiating

a

b

Figure 17 . Sixteen-year-old male with right lower quadrant pain. Axial steady state free precession (SSFP) image ( a ) demonstrates multiple loops of fl uid fi lled bowel. Axial diffusion-weighted imaging (DWI; b = 800) image ( b ) demonstrates restricted diffusion involving the appendix. The fl uid in the adjacent small bowel drops in signal intensity (SI) making the appendix more conspicuous (arrows).

U

Figure 18 . Forty-one-year-old female with an 8-year history of ulcerative colitis. Coronal T1-weighted (T1W) post-contrast image demonstrates increased signal intensity (SI) in the thickened wall of the sigmoid colon and avid contrast enhancement (oval). This is consistent with moderate to severe disease. Arrow, engorged vasa recta; arrowhead, normal colonic haustra; U, uterus.


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Romero et al .

rectal wall, trans-anal local excision can be performed, with lower

morbidity and mortality when compared with transabdominal

excision ( 72 ). Patients with more advanced tumors can be treated

with total mesorectal excision, an en bloc resection of the primary

tumor and mesorectum performed by dissecting along the mes-

orectal fascial plane. Th is procedure has dramatically decreased

the rates of local recurrence ( 73 ). Th e mesorectal fascia appears as

a thin hypointense line surrounding the mesorectal fat and repre-

sents the circumferential resection margin when total mesorectal

excision surgical approach is used. A distance ≥ 5 mm between the

tumor and mesorectal fascia predicts an uninvolved circumfer-

ential resection margin of at least 1 mm. Th e presence of tumor

or a malignant node within 1 mm of the surgical bed predisposes

patients to local recurrence ( 70 ).

MRI following either surgery or chemoradiation can be used

to determine treatment response and evaluate for residual or

recurrent disease as a problem-solving modality when CT fi nd-

ings are equivocal, or when carcinoembryonic antigen is rising

despite negative CT fi ndings. However, tumor may be diffi cult to

distinguish from active fi brosis following chemoradiation, lead-

ing to both overstaging and understaging ( 73,74 ). Both tumor

and active fi brosis may appear as hypointense tissue invading the

Figure 19 . Twenty-fi ve-year-old male with history of colitis. Coronal T2-weighted (T2W) image demonstrates a smooth appearance of the transverse colon wall due to the loss of haustral folds. This patient was diagnosed with ulcerative colitis.

Figure 20 . Twenty-six-year-old male presenting with a history of ulcerative colitis. Magnetic resonance enterography (MRE) demonstrated asymmetric and noncontiguous areas of active colonic and terminal ilium disease with the magnetic resonance imaging (MRI) appearance of “ thumb-printing ” in the transverse colon (arrow). Colonoscopy confi rmed discontinuous colon and terminal ilium fi ndings, and this patient ’ s diagnosis was changed to Crohn ’ s disease. Terminal ilium disease not included in this image.

**

*

Figure 21 . Sixty-fi ve-year-old male with cirrhosis and portal hypertension. Coronal T2-weighted (T2W) images reveal a diffusely edematous trans-verse colon (arrows). Although the most common location for bowel edema associated with portal hypertension is in the cecum and ascending colon, the stomach (arrowhead) and small bowel ( * ) walls were also thickened and edematous.

*

T

a

b

Figure 22 . Forty-fi ve-year-old male with mass seen on colonoscopy. Water-soluble gel was inserted into the rectum to accentuate rectal pathology. Sagittal T2-weighted (T2W) image ( a ) shows irregular wall thickening at the level of the recto-sigmoid junction (arrows). Axial T2W image ( b ) shows tumor and normal wall. Normal mucosa is typically a low signal intensity (SI) line (black arrow), submucosa is normally high SI (white arrow), musclaris propria is a low SI line (arrowhead). Tumor SI (T) is slightly higher than muscularis propria SI. There is extension of tumor into the mesorectal fat ( * ).


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ing all tracts can help prevent a simple fi stula from becoming com-

plex and avoid post-operative fi stula recurrence ( 86 ).

Th e major anal structures can be identifi ed on CT, but MRI has

far superior contrast resolution and better depicts the anatomy

( 87 ). Endoanal US has high resolution but a smaller fi eld of view

that may limit evaluation of tracts extending into the perianal

space and beyond the levator ani complex ( 88 ). Studies compar-

ing the accuracy of endoanal US with MRI have yielded a wide

variety of results ( 89,90 ). Th e modalities are complimentary and

choice of imaging modality should take into account the specifi c

patient ’ s clinical picture, surgeon preference, modality availability,

and expertise and cost ( 91 ).

At our institution we perform imaging with a phase array sur-

face coil; although an endorectal coil may maximize resolution,

patient discomfort is signifi cant in these patients and distension

associated with the coil itself can distort measurements ( 87 ). No

special patient preparation is required. We perform T1- and T2-

weighted imaging without fat saturation to delineate the muscles

and fat planes, and identify the fi stula tract. Fibrotic fi stula tracts

will be T1 and T2 hypointense and demonstrate delayed enhance-

ment on post-contrast images. Active tracts containing fl uid, pus,

or granulation tissue will be T2 hyperintense and enhance on T1

post-contrast sequences. T2-weighted imaging with fat suppres-

sion helps identify areas of edema, as well as tracts and abscesses

fi lled with fl uid. Pre- and post-contrast T1-weighted imaging

with fat suppression reveals areas of enhancement and infl am-

mation. Abscesses will appear T2 hyperintense, without internal

enhancement, and typically with peripheral enhancement. Gas

within an abscess may appear as susceptibility artifact. DWI

sequences are routinely performed and can be particularly help-

ful in patients that cannot receive IV contrast. Imaging should be

aligned with respect to the anal canal to depict the anal sphincter

complex in a surgically relevant plane; oblique axial and coronal

and axial images should therefore be obtained ( 92 ).

CONCLUSION Th e absence of ionizing radiation, superior tissue contrast, and

dynamic abilities of MRI are particularly well suited for addressing

the clinical questions commonly encountered in the practice of the

mesorectal fascia and pelvic sidewall. DWI may help in determin-

ing treatment response following therapy ( 75 ).

Nodal staging may be performed with CT, positron emission

tomography-CT, MRI, and locally with EUS. Nodal staging is lim-

ited, on both MRI and CT, as benign and malignant nodes overlap

signifi cantly in size, although the addition of signal heterogeneity

and border irregularity can increase sensitivity and specifi city ( 76 ).

However, it is diffi cult to diff erentiate an irradiated lymph node

from a metastatic node following treatment. Th e use of ultrasmall

superparamagnetic iron oxide contrast agents may help distinguish

benign and malignant lymph nodes ( 77 ). Macrophages in normal

nodes will take up ultrasmall superparamagnetic iron oxide agents

and appear low in signal on T2- “ star ” images. Nodes involved with

metastases will not take up the agents and reveal persistent areas of

high SI on T2 “ star ” . MRI restaging aft er chemoradiation therapy

could identify patients without nodal disease, who could be can-

didates for local excision. However, work in this area remains pre-

liminary, and although specifi city may be increased sensitivity is

similar to that when using morphologic features ( 78 ). Th e addition

of DWI sequences to conventional MRI can increase the sensitiv-

ity of detecting lymph node metastases over that of CT ( 78 ). DWI

may also help identify complete responders following chemoradia-

tion and allow for more conservative management of these patients

( 79 – 81 ). In some cases, biopsy is required to provide the diagnosis.

Anus MRI is a valuable tool in evaluation of anorectal disease. Perianal

fi stulas ( Figure 23 ) are frequently encountered complications of

Crohn ’ s disease and MRI can accurately depict the fi stula course,

its relationship with the sphincter, and associated abscesses. MRI

has been shown to provide important information that may alter

surgical approach, particularly in patients with complex and recur-

rent infl ammatory and infectious disease ( 82,83 ). Deep-tissue fi s-

tula healing may lag substantially behind more superfi cial healing,

making MRI a valuable tool for monitoring medical therapy ( 84 )

and also potentially disease activity ( 85 ). Infl ammatory activity

persists on MRI aft er clinical symptoms and drainage have resolved

( 86 ). Recent European Crohn ’ s and Colitis Organization guidelines

for the management of Crohn ’ s disease recommend MRI or EUS

for all fi stula cases where treatment is planned. Correctly identify-

a b c

Figure 23 . Thirty-fi ve-year-old female with history of anal fi stula for evaluation of residual tract. Coronal T1-weighted (T1W) post-contrast image dem-onstrates an intersphincteric fi stula extending along the right lateral aspect of the external sphincter from the right deep gluteal fold (white arrows) ( a ). Fluid within the fi stula (white arrow), asymmetry of the puborectalis muscle (arrowheads), and relationship of the fi stula to the muscles are best seen on T2-weighted (T2W) image ( b ). T1W post-contrast image status post placement of a “ mushroom ” catheter (arrows) and a Seton in a trans-sphincteric com-ponent of the fi stula, not defi nitely identifi ed on the earlier study (black arrows) ( c ).


508R

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Romero et al .

luminal gastroenterologist. With careful enteric contrast selection

and antiperistaltic agents, MRI can serve as an excellent problem-

solving tool, providing a comprehensive picture of infl ammatory

bowel disease and its complications, particularly in cases of small

bowel Crohn ’ s disease. It achieves these aims without exposing

young patients to unnecessary radiation. Th e strength of MRI for

staging rectal cancer and evaluating the extent of anorectal fi stula

involvement has been confi rmed in the literature and MRI can be

used to optimize surgical planning. Recent work with DWI and

ultrasmall ferromagnetic particles is also promising in helping to

make the important distinction between benign and malignant

disease. As MRI ’ s capabilities evolve, it will develop into a key

component of the clinician ’ s diagnostic toolkit.

CONFLICT OF INTEREST Guarantor of the article: Suzanne L. Palmer, MD.

Specifi c author contributions: Miriam Romero: conceiving, initiat-

ing, writing, and editing the manuscript; fi nal review and approval

of the submitted manuscript. James Buxbaum: writing and editing

the manuscript, and fi nal review and approval of the submitted

manuscript. Suzanne L. Palmer: conceiving, initiating, writing, and

editing the manuscript, fi nal review and approval of the submitted

manuscript, and submission of the manuscript.

Financial support: None.

Potential competing interests: None.

Study Highlights

WHAT IS CURRENT KNOWLEDGE 3 Magnetic resonance imaging (MRI) is appropriate for evalu-

ating hepatobiliary pathology.

3 MRI lacks ionizing radiation.

3 MRI has superior tissue contrast and dynamic imaging abilities.

WHAT IS NEW HERE 3 MRI is a problem-solving tool for luminal gastroenterologists.

3 MRI is appropriate for evaluation of infl ammatory bowel disease.

3 MRI is appropriate for staging rectal cancer.

3 MRI is appropriate for evaluating anorectal fi stulas.

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GASTROENTEROLOGY ARTICLE OF THE WEEK February 12, 2015

Romero M, Buxbaum JL, Palmer SL. Magnetic resonance imaging of the gut: a primer for the luminal gastroenterologist. Am J Gastroenterol 2014;109:497-509. 1. The normal thickness of the small bowel wall on MRI is a. 1-2 mm b. 3-4 mm c. 5-6 mm d. 10-12mm True or False 2. Enhancement of normal-thickness small bowel wall may be false positives and should not be interpreted as indicative of inflammation 3. Avidly enhancing mesenteric lymph nodes in a patient with suspected IBD raises the possibility of lymphoma 4. MRI can be performed in all trimesters of pregnancy 5. EUS examination of rectal cancer obviates the need for MRI staging 6. In T1-weighted sequences, fluid appears black, in T2 weighted sequences, it appears white 7. MRI IV contrast is safe during pregnancy 8. MRE uses dilute barium as the contrast media, no IV contrast is used 9. In rectal cancer, MRI is inferior to EUS for differentiating T1 and T2 stages. 10. The appendix can be examined by MRI without having to use oral or IV contrast 11. To evaluate the anus for fistula, an endorectal coil must be used

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