Applied Radiology

Upper and lower endoscopy, which enable direct visualization and biopsy of diseased GI tissue, represent the gold standard for the evaluation of Crohn's disease. Radiology plays a significant role as well, one that traditionally has centered on the use of barium studies, including the barium enema and upper GI study with small bowel follow-through. It is important to realize, however, that barium studies show only the GI lumen and not the diseased intestinal wall.

Helical CT holds the predominant role in cross-sectional imaging of Crohn's disease and the evaluation of its complications. Magnetic resonance imaging (MRI), however, has many advantages for the evaluation of the GI tract in general, and Crohn's disease in particular.

We first described the double-contrast technique--combining intraluminal contrast agents and intravenous gadolinium--for MR evaluation of gastrointestinal disease in 1997. ² This MR technique takes advantage of the high contrast resolution of MR imaging to depict enhancement of the inflamed bowel wall. We subsequently performed a study comparing helical CT and MRI in Crohn's disease, using double-contrast techniques. ³ Among our conclusions were that MRI is superior for depicting both normal and inflamed bowel wall; shows more marked enhancement of inflamed areas; is superior to CT for the depiction of subtle bowel disease; and is equivalent for depicting such complications as fistula, abscess, or phlegmon.

Some of the challenges that arise in MRI of the GI tract include peristaltic motion, respiratory motion, and variability in the position of the small intestine and colon. In addition, it is necessary to distend the bowel during imaging, and, until recently, inexpensive intraluminal contrast agents have not been widely available. It is also necessary to distinguish subtle changes in the bowel wall from artifact that may be related to the MR acquisition or from collapsed bowel. Faster pulse sequences and improved hardware have overcome many of these challenges, enabling MR to move to the forefront of GI imaging.

Double-Contrast Protocol

We use a double-contrast protocol for MR of the GI tract (Table 1). ⁴ First, the patient drinks two to three bottles of ReadiCat 2 (E-Z-Em, Westbury, NY) or an equal amount of water to provide intraluminal contrast. Water is effective if scanning is accomplished very quickly. The disadvantage, however, is that it is reabsorbed by the colon. If the patient drinks slowly, water may not be effective in distending the bowel.

Next, we administer 500 to 1000 mL of rectal water through a balloon-tipped enema. We fill the balloon with water to decrease susceptibility to artifact from the balloon.

We use single-shot spin-echo sequences to obtain very rapid, heavily T2-weighted images in both the axial and coronal planes. It takes approximately 19 seconds on our scanner to acquire a set of 12 images. Multiple breathholds are performed to image the abdomen and pelvis in the axial and coronal planes.

One mg of glucagon is injected intravenously to decrease peristalsis. This is followed immediately with a double dose of gadolinium contrast media (0.2 mmol/kg). We then acquire two-dimensional images using a breathhold fast spoiled gradient-echo (SGE) sequence with fat suppression. We typically image at high resolution, using a matrix of 512 * 192. The bandwidth is about +20 kHz, and we use a three-quarter field of view to shorten the time of acquisition. It takes 20 to 24 seconds to acquire 12 images. We set up two passes in the axial plane, each of which requires 4 breathholds, and then acquire 1 set of coronal images. The study is performed very rapidly and takes about 15 minutes from start to finish.

Another technique we often apply is MR enteroclysis. Using the same bowel preparation and single-shot spin-echo sequence, we acquire a 10-cm thick section using a very long TE (600 msec), similar to that used in magnetic resonance cholangiopancreatography (MRCP). This acquisition takes only 2 sec to obtain, and the resulting image looks very much like a barium study. This technique may be used to perform dynamic MR imaging of the GI tract by obtaining multiple sequential 2-second images following the administration of oral contrast material. By placing these images in a cine loop, one can review gastric and small intestinal motility.

Among the advantages of the double-contrast approach are the low cost and ready availability of intraluminal agents, and the effectiveness of these agents in distending and separating the bowel. In addition, very rapid breathhold imaging sequences reduce motion artifact, particularly when glucagon is administered to reduce peristalsis.

Perhaps most important, the double-contrast technique creates a set of biphasic images that facilitate depiction of both the bowel lumen and the bowel wall (Figure 1). On the T2-weighted single shot fast spin echo images, for example, the water or ReadiCat 2 is bright, thereby functioning as a positive agent that shows the lumen of the bowel and intestines. This is useful for demonstrating changes in the caliber of the lumen and in looking for stricture. In the same patient, the same intraluminal contrast functions as a negative agent on T1-weighted fat-suppressed gradient echo imaging. This enables visualization of the wall of the bowel, which normally appears as multiple thin lines or rings.

In interpreting MR images, it is important to look at the thickness of the bowel wall and at its enhancement. The normal bowel wall should measure 3 mm or less; anything more is considered thickened. For defining mural enhancement, we use a non-fatty liver as our standard. If mural enhancement is the same or less than that of the liver, we consider it normal. Enhancement that exceeds that of the liver is considered mildly abnormal, and enhancement equal to that of the intravascular gadolinium is considered markedly abnormal.

MR versus Helical CT

Most radiologists use helical CT to evaluate patients with Crohn's disease. Nonetheless, the ability to image the bowel wall is essential for defining pathology in Crohn's disease and other intestinal disorders, and represents a critical advantage of MRI over CT or barium studies.

Figure 2 offers a good example. In this patient, helical CT demonstrates some mural thickening in the wall of the ileum. With the MRI double-contrast technique, however, the lumen is distended nicely, and the thickened wall of the ileum shows intense enhancement. Superior conspicuity of enhancement in the inflamed wall is a consistent advantage of MRI, one that accounts for its having become the exam of choice for the evaluation of Crohn's disease at our center.

Clear differences in the sensitivity of MRI and helical CT become even more evident in subtle cases of Crohn's disease, as depicted in Figure 3. Much of the bowel appears normal on CT. On MRI, however, the entire bowel wall is distinctly abnormal, a conclusion that was confirmed by endoscopic findings of pancolitis and ileitis. We consistently find that the distribution of disease is much better visualized on MRI than on helical CT.

Correlations with Endoscopy

Because of its close correlation with endoscopy, MRI is able to guide clinical decision-making. We have discovered that the activity of Crohn's disease correlates with the degree of gadolinium enhancement, so that a thickened bowel wall that doesn't enhance signifies inactive disease. This is an important finding, as a patient who has chronic inactive disease will receive different treatment than a patient with acute, actively inflamed Crohn's disease.

Figure 4 demonstrates the ability of MRI to distinguish active from inactive Crohn's disease. Barium enema shows a stricture, but it is impossible to determine whether the Crohn's disease is acute or chronic. On MRI, the degree of enhancement is minimal and the T2-weighted image is very dark. In our experience, this pattern correlates with inactive disease. Endoscopy confirmed this impression, demonstrating a perfectly smooth mucosa. Biopsy found some chronic inflammation but no active disease.

By comparison, in patients with active disease, marked thickening and enhancement of the bowel wall correlate well with endoscopic findings of erythema, ulceration, pseudopolyps, and a cobblestone-like mucosa, an appearance that signifies very severe Crohn's disease (Figure 5). Similarly, MRI is a valuable tool for the assessment of complications of Crohn's disease. Figure 6 shows a patient with an enterovesicle fistula. On MRI, the inflammatory mass in the terminal ileum is well visualized, as is an eccentric thickening of the wall of the bladder near the fistula.

MRI is able to detect very focal disease as well, even though it can be subtle. An example of this would be a patient who returns with abdominal pain after surgical resection. In such a case, focal, localized recurrent disease at the site of bowel anastomosis may be seen on gadolinium-enhanced MR images with good bowel distension.

Beyond Crohn's Disease

The same double-contrast MRI techniques that work in Crohn's disease are equally well suited to other types of GI disease. We use this approach not only in inflammatory bowel disease, but also to evaluate patients with infectious enteritis and colitis, mesenteric ischemia, and cancer. We use MRI fairly regularly to stage colon cancer, for example, looking at the depth of penetration of the tumor through the wall. It works well for evaluating gastric and small bowel malignancies, and serosal metastases from ovarian cancer and other primary tumors.

Figure 7 serves as another example of the range of applications of double-contrast MRI. This patient had a 1-month history of diarrhea. The helical CT was unremarkable. MRI showed that the terminal ileum demonstrated marked thickening and enhancement, which was not depicted on the helical CT scan. On endoscopy, there were ulcerations at the ileocecal valve and in the distal ileum, as well as ulcerated plaques in the right colon. This case of probable infectious colitis again demonstrates the superior depiction of relatively subtle changes by MRI when compared with helical CT.

Conclusion

Superior conspicuity of enhancement gives double-contrast MRI a clear advantage over helical CT in the imaging of patients with Crohn's disease. This approach is effective for imaging not only inflammatory bowel disease, but other forms of GI disease, including such conditions as infectious colitis, mesenteric ischemia, and cancer. *

Discussion

TG: Thank you very much, Dr. Low. We have some time for discussion of this very interesting topic.

RS: I have a couple of questions. The first one relates to early and later enhancement. I guess the early enhancement I like to think of as perfusional, and later as sort of interstitial space. Do you find that it's very important to keep those two data sets separate? How do you treat them when you evaluate the bowel?

RL: Particularly, when you are trying to distinguish or determine the degree of activity, you need to look at the perfusional information from the first pass. We look at that and then try to distinguish if it is enhancing a lot or a little. The second set, everything tends to enhance on those. We do not use those in terms of determining the activity. That's a good point.

RS: The other question is if you have also used that to distinguish between Crohn's disease and ulcerative colitis? I noticed in your cases the same thing we've found in our studies, and that is that with Crohn's you get transmural enhancement, whereas in ulcerative colitis, we've seen submucosal sparing consistently.

RL: Right. I think because of the incidence of the disease, our experience with ulcerative colitis is clearly less. But I think our experience tends to be less intramural thickening. Although at end-stage ulcerative colitis, we do tend to see more significant enhancement.

MP: Russell, I noticed in some of your 2D gradient-echo gadolinium-enhanced images, that you were getting some dropout where surgical clips were evident. Have you tried the 3D to minimize this?

RL: We played around with the 3D pulse sequence. But as Richard said, we tend to like the appearance of the 2D better. There are certainly some advantages of the 3D in terms of the thickness of the sections. At this point, we haven't used that significantly. The single-shot image is probably in that saline one, you have a lot of bowel gas or something, and with artifact, tend to work pretty well too.

LK: Russell, you said you used double dose for these studies, why? Did you try single dose and it didn't work?

RL: It would work with single dose. It's based on our experience looking at a lot of extrahepatic disease, particularly peritoneal tumor. We did a lot of comparisons of single versus high dose for peritoneal tumor. We found that for particularly things outside the liver, they enhance more, anything that you are waiting for awhile to enhance. So it's a logical next step to assume that it would also work in Crohn's disease. I think clearly that does show us more. Any time you are looking at subtle enhancement, with the degree of enhancement of something relatively thin, it's important and more is logically better.