Dr. Low is the Medical Director of Sharp and Children's MRI Center, San Diego, CA.

The early focus of body magnetic resonance (MR) imaging was for the evaluation of solid visceral organs, such as the liver, and kidneys. MR imaging of nonsolid organs, including the gastrointestinal (GI) tract and the peritoneum, posed significant challenges related to motion artifact and long examination times. However, new advances in MR imaging hardware and software have overcome all of these challenges, and MR imaging of the extrahepatic abdomen has evolved to become a powerful and robust imaging technique. Once motion artifact is eliminated, the superior contrast conspicuity of MRI allows for the depiction of subtle enhancing diseases that are not visible on other routine cross-sectional studies. In particular, MR imaging excels at depicting diseases of the GI tract and the peritoneum, making MRI of these organs a routine part of our clinical practice. This article will review clinical applications, MR protocols, and techniques for MR imaging of inflammatory, infectious, and ischemic intestinal diseases, as well as benign and malignant diseases of the peritoneum.

Gastrointestinal MR imaging

The unique ability of MR imaging to visualize the bowel wall directly is the foundation of its power for evaluating inflammatory, infectious, ischemic, and malignant GI tract diseases. Mural involvement of the GI tract is the common denominator for all of these varied diseases. By combining breath-hold MR imaging with intravenous (IV) gadolinium and readily available intraluminal agents, MR imaging can consistently depict subtle mural diseases of the GI tract as areas of bowel-wall thickening and enhancement.

Techniques and protocols:
GI tract MR imaging

Intraluminal contrast agents

Adequate distension of the stomach, small intestine, and colon is essential for MR imaging of the GI tract. Incomplete intestinal distention may mask important findings or may mimic an inflammatory or neoplastic mass. Fortunately, there are many different intraluminal contrast agents available. Our experience has shown the benefits of a biphasic intraluminal agent that is bright on T2-weighted images and dark on T1-weighted images (Figure 1). ^1-3 A dark or low-signal intraluminal agent on the gadolinium-enhanced spoiled gradient-echo (SGE) T1 images is very useful, as it helps to accentuate enhancement of the adjacent diseased bowel wall. A high-signal intraluminal agent on T1 images could obscure subtle mural enhancement.

At our institution, we use either water or dilute barium sulfate, which is 98% water. Each agent demonstrates a biphasic appearance on T2- and T1-weighted images. Both are well-tolerated and readily available. Dilute barium sulfate is iso-osmolar, so it will stay in the GI tract and not be reabsorbed. On the other hand, water is reabsorbed, making adequate distension of the distal small bowel unpredictable. Agents such as manitol can be added to the water to increase its osmolarity and reduce intestinal reabsortion. At our institution, we have patients ingest 1400 mL of oral contrast material beginning 30 to 45 minutes before the examination. Rectal water can be administered through a balloon-tipped barium enema catheter. The balloon should be filled with water to avoid the susceptibility artifact generated by the air in the balloon. Alternative routes of administration have been suggested, including MR enteroclysis via a nasojejunal tube.

Other intraluminal contrast agents include water mixed with gadolinium chelate, which is high signal intensity on T1- and T2-weighted images; and iron-oxide­containing agents, which are low signal intensity on both types of MR images.

Intravenous contrast agents

Intravenous gadolinium (0.2 mmol/kg) is administered for the gadolinium-enhanced SGE images. Although it is not essential to the technique, we use a power injector with a bolus injection at a rate of 2 mL/sec. The nonspecific extracellular gadolinium chelates will enhance inflammatory, infectious, and malignant disease of the GI tract and peritoneum, markedly increasing their conspicuity. One mg of IV glucagon is preloaded into the IV tubing and is administered at the time of gadolinium injection to decrease bowel peristalsis.

Pulse sequences

MR imaging of the gastrointestinal tract requires rapid imaging to minimize the effects of respiratory motion and peristalsis. ^1-7 Gastrointestinal tract disease can be subtle so that normal physiologic motion can obscure important findings. Rapid, breath-hold MR imaging is clearly essential for effective GI tract imaging. At our center we use breath-hold single-shot fast spin-echo (SSFSE), and breath-hold fat-suppressed SGE imaging after IV gadolinium administration. ¹ This combination of images produces rapid T2-weighted, gadolinium-enhanced SGE T1-weighted images that are relatively insensitive to motion artifact. Administering 1 mg IV glucagon at the time of IV gadolinium injection reduces bowel peristalsis.

Specific imaging parameters will depend upon the particular MR imager and software being used. On our current scanner, Echo Speed 1.5T LX Signa MR Scanner (General Electric Medical Systems, Waukesha, WI), we use the following imaging parameters:

SSFSE-- Repetition time (TR) infinite, echo time (TE) 90, matrix 256 * 192, flip angle 90š, 0.5 number of excitations (NEX), bandwidth (BW) 62 kHz, slice thickness 8 mm, 2-mm gap, echo-train length (ETL) >100.

Gadolinium-enhanced SGE T1-- TR 160, TE 2.1, 256 * 192, 512 zero order filling (ZIP), flip angle 70š, 1 NEX, BW 20 kHz, slice thickness 8 mm, fat suppression, field of view ( ³ /4 FOV).

The entire abdomen and pelvis are imaged in the axial plane and coronal planes. For the gadolinium-enhanced images, we obtain two sets of axial images. This will require multiple breath-holds to cover the abdomen and pelvis. We typically obtain 12 slices per breath-hold, so the abdomen and pelvis can be covered with 4 breath-holds per acquisition.

Alternative imaging sequences include true fast imaging with steady-state free precession (FISP) for the T2-weighted images. On these images, there is excellent contrast between the high-signal lumen distended with water or dilute barium sulfate and the adjacent bowel wall. For the gadolinium-enhanced images, one may alternatively perform volumetric imaging with a three-dimensional (3D) gradient-echo pulse sequence. The 3D acquisition rapidly obtains multiple thin sections during one breath-hold. Inversion recovery fat-suppression is added to the 3D acquisition to improve the conspicuity of enhancing mural disease. Imaging parameters are highly variable depending upon the MR imager used. Typical acquisitions will acquire 56 to 100 sections in one breath-hold. The slice thickness will be chosen to optimize anatomic coverage during the period of suspended respiration. Typical slice thickness might be 4 mm, which can be interpolated down to a thickness of 2 mm. As the efficiency and image quality of these 3D images improves, they will likely replace two-dimensional (2D) SGE imaging for gadolinium-enhanced MR imaging.

Coils

Most of our GI tract and peritoneal MR imaging is performed with the body coil. The excellent image homogeneity and extended coverage of the body coil are important for GI tract and peritoneal imaging. While phased-array surface coils will improve image signal-to-noise ratio, the images are often less homogeneous. High signal near the coil when using phased-array coils can mask or mimic important subtle findings on MR images of the GI tract and peritoneum.

Clinical applications for gastrointestinal MRI

Inflammatory bowel disease

Crohn's disease is a chronic inflammatory disease of the GI tract that is characterized by apthous ulceration, cobblestoning, strictures, and fistula formation. Changes in the bowel wall are typically discontinuous and asymmetrical and can be depicted on cross-sectional imaging studies. Helical computed tomography (CT) and MR imaging can be used to assess the mural changes of Crohn's disease and to depict extraintestinal complications, including fistula formation, abscesses, and phlegmons (Figure 2).

Inflammatory diseases of the GI tract such as Crohn's disease or ulcerative colitis are exquisitely depicted with MR imaging. ^1-5 By combining a negative oral contrast agent with fat-suppressed, gadolinium-enhanced MR imaging, one may show bowel wall thickening and enhancement (Figure 3). In our experience, compared with helical CT, MR imaging is much more sensitive to earlier or milder forms of inflammatory bowel disease. In a study of 26 patients with Crohn's disease, ² depiction of mural thickening and/or enhancement was superior on the MR images, which showed 55 (85%) and 52 (80%) of 65 abnormal bowel segments for the 2 observers, compared with helical CT, which showed 39 (60%) and 42 (65%) ( P <0.001, P < 0.05) of bowel segments affected by Crohn's disease.

Both the T2-weighted SSFSE images and the gadolinium-enhanced SGE images are useful for depicting mural thickening (Figure 4). ¹ Gadolinium enhancement of the inflamed bowel segments facilitates detection of diseased bowel. In addition, the degree of bowel wall enhancement correlates with the activity of the inflammatory process. The enhancement of the normal bowel wall is equal to or less than that of the liver parenchyma. Bowel wall enhancement that is more than the liver indicates mild inflammation, and enhancement that is equal to intravascular gadolinium represents inflammation marked in intensity. Bowel that is actively inflamed from Crohn's disease will show a gadolinium enhancement more than that of the liver parenchyma. ¹ On the other hand, thickened bowel that does not enhance correlates with non-acute disease. In a study of 28 patients with Crohn's disease, gadolinium-enhanced SGE MR images correctly predicted the severity of Crohn's disease in 93% of patients compared with 43% for the SSFSE images. ¹

It is equally important to be able to accurately depict complications of Crohn's disease. In our experience, MR imaging and helical CT are equivalent for depicting fistulas, abscesses, and phlegmons. ² Gadolinium enhancement of extraintestinal abscesses and phlegmons facilitates their detection on MR imaging. Fistulas will be depicted directly as fluid- or air-filled tracts between adjacent bowel loops, viscera, and/or the abdominal wall. More commonly, one may see distortion and tethering of bowel loops at the site of fistulous connection.

The MR depiction of mural changes of Crohn's disease and other inflammatory intestinal diseases requires adequate distension of the bowel. Collapsed bowel may enhance and mimic abnormal bowel. In addition, subtle bowel wall changes may be hidden by inadequately distended bowel. Optimal intestinal distension can be achieved by combining oral and rectally administered water-
soluble contrast material.

Mesenteric ischemia

Diagnosing intestinal ischemia can be a clinical and imaging challenge. The presenting symptoms of cramping abdominal pain, leukocytosis, diarrhea, and hematochezia are not specific and can be seen with inflammatory or infectious intestinal diseases. Mesenteric ischemia is caused by inadequate arterial supply or insufficient venous drainage of the involved segment of bowel. ^8-13 Arterial insufficiency is much more common and may be due to occlusive or nonocclusive causes. Nonocclusive causes are much less common and are related to low flow states and hypoperfusion. Occlusive mesenteric ischemia may be due to atheromatous plagues, embolic disease, and abdominal aortic aneurysms with a dissection involving the superior mesenteric artery (SMA). Less common mechanical causes of intestinal ischemia include adhesions, small bowel herniation, intussusception, or a volvulus. Hypercoaguable states, such as antiphospholipid syndrome, can also predispose patients to thrombotic occlusion of mesenteric vessels.

By combining gadolinium-enhanced MR angiography and anatomic MR imaging of the abdomen and pelvis, a comprehensive examination can be performed in the patient with suspected intestinal ischemia. The MR angiography will evaluate possible occlusive disease of the SMA and the inferior mesenteric artery (IMA), while the anatomic images will show mural thickening of the involved bowel segments. Our current approach involves administering the intraluminal contrast agents described above, followed by a gadolinium-enhanced MR angiograms of the abdominal aorta and mesenteric vessels. This is followed by the breath-hold SSFSE and gadolinium-enhanced fat-suppressed SGE images of the abdomen and pelvis.

Findings of mesenteric ischemia include occlusion of the SMA, IMA, or, rarely, of the celiac artery branches. Due to collateral circulation, typically two of the three mesenteric vessels must be involved to produce symptoms of mesenteric ischemia. It is important to realize that distal small vessel occlusion may produce focal ischemia. Such distal occlusions are beyond the resolution of current MR angiography techniques. For this reason we always assess the bowel wall for secondary changes of mural thickening.

On the anatomic SSFSE or true FISP images and the gadolinium-enhanced SGE images, focal mural thickening in a vascular distribution can be seen (Figure 5). In patients with acute arterial insufficiency, there will be diminished or absent enhancement within the thickened segments of ischemic bowel. A target appearance with enhancement of the mucosal and serosal layers surrounding a nonenhancing muscularis layer can be seen. This assessment of lack of enhancement should be made on the initial gadolinium-enhanced images. On delayed images, bowel wall enhancement may be evident from leakage of the contrast from the capillaries into the damaged bowel wall. In the nonacute setting, the pattern of enhancement will be variable depending upon the degree of revascularization, fibrosis, or tissue necrosis. In our experience, findings on MR imaging can resolve very rapidly following spontaneous revascularization of the ischemic segment of bowel.

Infectious intestinal diseases

Infectious gastroenteritis or colitis may be imaged using identical MR techniques. As with Crohn's disease, infectious diseases of the small bowel or colon will present as segments of bowel with mural thickening and abnormal enhancement. In our experience, it is not possible to distinguish infectious from inflammatory bowel disease. Follow-up MR imaging after a course of antibiotic therapy will show improvement or resolution of mural thickening and enhancement. As with other types of intestinal disease, the excellent contrast conspicuity of MR imaging makes it more sensitive than helical CT for depicting infectious GI disease.

Peritoneal MR imaging

The depiction of small peritoneal implants and carcinomatosis is a challenge for cross-sectional imaging studies, including CT scanning and unenhanced MR imaging. However, with gadolinium-enhanced MR imaging, small peritoneal tumors are
routinely depicted with a level of conspicuity that is unmatched by other imaging studies. Marked enhancement of small peritoneal implants with IV gadolinium on MR images facilitates detection of metastases to free peritoneal surfaces and bowel serosa. ^14-16 Following the injection of gadolinium, peritoneal implants slowly accumulate the contrast material and are, therefore, most conspicuous on images obtained 5 to 10 minutes following the IV injection of the gadolinium chelate. The addition of fat suppression reduces the competing high signal of the adjacent fat and is an important element in this technique.

Several studies have shown that gadolinium-enhanced, fat-suppressed MR imaging is superior to CT scanning in depicting peritoneal tumor (Figure 6). ^14,15 The superior performance of enhanced MR imagining compared with CT scanning is most noticeable in the depiction of small (<1 cm) tumor implants and carcinomatosis. In a recent study, ¹⁴ gadolinium-enhanced MR imaging detected 75% to 80% of small tumor implants (<1 cm) compared with 22% to 33% for CT scans ( P <0.0001).

Techniques and protocols:
Peritoneal MR imaging

The MR protocol and techniques we use for evaluating peritoneal disease are very similar to those that we use for MRI of the GI tract. We again use entirely breath-hold acquisitions to reduce motion artifact. The abdomen and pelvis are covered in the axial and coronal planes with a breath-hold, fat-suppressed T2-weighted FSE acquisition and then with the same gadolinium-enhanced, fat-suppressed SFE acquisition described for GI tract imaging.

Pulse sequences

Breath-hold T2-weighted FSE-- TR 2500, TE 77, 256 * 192, ETL 17, flip angle 90š, 1 NEX, BW ±32 kHz, slice thickness 7 mm, interslice gap 3 mm, ³ /4 FOV, fat suppression, flow compensation, 512 ZIP, time 25 sec for 12 slices.

Gadolinium-enhanced SGE T1-- TR 160, TE 2.1, 256 * 192, 512 ZIP, flip angle 70š, 1 NEX, BW 20 kHz, slice thickness 8 mm, fat suppression, ³ /4 FOV, scan time 25 sec for 12 slices.

Intraluminal contrast

We use the same intraluminal contrast agents to distend the stomach, small intestine, and colon for patients with suspected peritoneal tumor. As with GI tract disease, inadequate bowel distension can significantly limit image interpretation. To distend the bowel, we use 1400 mL of dilute barium sulfate or water starting 30 minutes before the examination. Rectal water, 500 to 1000 mL, can also be administered for distention of the colon. Distension of the pelvic bowel is especially important in patients with treated gynecologic malignancy, in whom subtle tumor recurrence often occurs near the rectosigmoid colon.

Intravenous contrast agents

We use the same double dose (0.2 mmol/kg) of IV gadolinium chelate administered as a bolus at 2 mL/sec. One mg IV glucagon is preloaded in the IV tubing to decrease peristalsis on the gadolinium-enhanced SGE MR images.

Clinical applications for MRI
of peritoneal disease

Ovarian cancer

Gadolinium-enhanced MR imaging is useful in women with ovarian cancer to monitor response to therapy by depicting residual peritoneal tumor and to detect recurrence in patients with a rising serum CA-125 level (Figure 7). Detecting clinically occult tumor is critical in determining appropriate patient management. After chemotherapy, declining serum CA-125 values indicated tumor response to treatment. Unfortunately, a normal CA-125 value does not exclude residual tumor, as up to 50% of women with a normal CA-125 value after chemotherapy still have residual tumor. ^17-19

As fewer second-look surgeries are being performed, ^20,21 our oncologists now use the results of gadolinium-enhanced MR imaging to determine response to chemotherapy. In order to establish the accuracy of MR imaging in depicting tumor in women with treated ovarian cancer, we performed a 5-year longitudinal study in which we compared the results of MR imaging with serum CA-125 level and physical examination in 69 women with treated ovarian cancer. ¹⁶ MR findings were compared with the clinical impression of tumor presence or absence, based upon CA-125 values and physical examination. Our experience confirmed that gadolinium-enhanced MR imaging detects clinically occult tumors in women with treated ovarian cancer. Thirty-nine of the 69 patients were in clinical remission with a normal CA-125 level and physical examination. In our study, 23 of 39 (59%) of patients in clinical remission had residual subclinical tumor proven by laparotomy or clinical follow-up. Gadolinium-enhanced MR imaging correctly showed residual tumor in 20 of 23 patients. ¹⁶

For all 69 patients, MR images had a 91% sensitivity, 87% specificity, 90% accuracy, and 72% negative predictive value, and were superior to serum CA-125 level (53%, 94%, 63%, and 38%) ( P <0.0001), and physical examination (26%, 94%, 43%, and 29%) ( P <0.0001) for depicting residual or recurrent tumor.

Second-look laparotomy (SLL) was performed in 34 patients. There was no significant difference between SLL and MR imaging, each of which had an 87% sensitivity, 75% specificity, and 85% accuracy. In this subset of patients, SLL and MR imaging were superior to serum CA-125 level ( P <0.05) (60%, 100%, and 65%). ¹⁶

The improved sensitivity of gadolinium-enhanced MR imaging in depicting small volume tumors, compared with CA-125 levels alone, provides our oncologists with information critical to patient management ^15,22-26 ; providing a more accurate means of monitoring response to adjuvant chemotherapy and detecting recurrence after initial response. In our experience, gadolinium-enhanced MR imaging often shows residual tumor in patients after adjuvant chemotherapy, indicating a need for additional treatment. ^15,16

Peritoneal metastases
from other abdominal tumors

Gadolinium-enhanced, fat suppressed, SGE MR imaging is equally effective for evaluating peritoneal metastases from other primary tumors of the pancreas and GI tract. Primary tumors of the stomach, pancreas, colon, and appendix often spread by intraperitoneal tumor cell exfoliation and subsequent peritoneal carcinomatosis. At our institution, the information from MR imaging is used to determine the appropriate course of therapy. Accurate depiction of subtle peritoneal tumor can completely alter patient management. For instance, in a patient with pancreatic cancer, surgical resection is not indicated if metastatic peritoneal tumor is confirmed on preoperative MR imaging. Similarly, in the patient with colon cancer metastatic to the liver, possible hepatic resection of isolated liver metastases may prolong survival. However, with concurrent peritoneal metastases, hepatic tumor resection is obviously contraindicated. In patients with gastric cancer, we are all familiar with the drop metastases to the pelvis producing large complex Krukenberg tumors. However, it is more common to find subtle peritoneal metastases elsewhere in abdomen on MR images. The ability of gadolinium-enhanced MR imaging to depict subtle peritoneal tumor and carcinomatosis makes it a valuable study in the oncology patient. ²⁷ At our institution, we use MR imaging as the primary imaging study in these patients. This approach becomes especially important when peritoneal tumor is of immediate clinical concern.

Spread of abdominal tumors
along peritoneal reflections

The peritoneal reflections also form the ligaments that connect the abdominal organs and viscera to one another and to the retroperitoneum and abdominal wall. ^28,29 In the upper abdomen, a complex network of peritoneal reflections surround and connect the liver, stomach, spleen, kidneys, and duodenum. These peritoneal reflections thus serve as important potential pathways for spread of abdominal malignancies. ^28,29

The gastrohepatic ligament is also known as the lesser omentum and extends from the lesser curvature of the stomach to the left lobe of the liver. On the liver surface the gastrohepatic ligament extends into the fissure for the ligamentum venousum that separates the caudate lobe from the left hepatic lobe. The hepatoduodenal ligament is located along the free margin of the lesser omentum or gastrohepatic ligament. It extends from the porta hepatis to the duodenal sweep and contains the components of the portal triad; the portal vein, hepatic artery, and bile ducts. The hepatoduodenal ligament is an important pathway of spread of inflammation or tumor from the retroperitoneum to the liver or from the liver to the retroperitoneum.

Once tumor gains access to the liver, it can spread along the periportal space that then communicates with the left intersegmental fissure and the falciform ligament. The falciform ligament connects the liver with the anterior abdominal wall. Using these peritoneal reflections, a continuous pathway is thus established from the retroperitoneum through the liver to the abdominal wall. For example, a pancreatic cancer can spread along the hepatoduodenal ligament from the retroperitoneum to the liver, then along the periportal tissues to the falciform ligament, and, finally, to the anterior abdominal wall.

The gastrohepatic, gastrosplenic, splenorenal ligaments, greater omentum, and transverse mesocolon are additional peritoneal reflections that serve as potential pathways of spread for tumors of the liver, stomach, spleen, kidneys, and colon. A thorough understanding of the interconnected peritoneal reflections will improve our interpretation of imaging studies in patients with metastatic abdominal tumor.

Pseudomyxoma peritonei

Pseudomyxoma peritonei is a rare condition characterized by the accumulation of copious gelatinous masses throughout the peritoneal cavity. Pseudomyxoma peritonei may be associated with appendiceal mucin-producing tumors or may occur as a complication of ovarian mucinous cystadenoma. This is typically a slowly progressive disease in which patients present with increasing abdominal girth, an inguinal hernia, or a palpable ovarian mass. While pseudomyxoma does not metastasize via the lymphatics or blood stream, it is a progressive disease, which if untreated eventually leads to death by replacement of the peritoneal cavity by mucinous tumor.

The primary tumor of the appendix or ovary is typically inconspicuous at the time of diagnosis. Mucin-producing tumor cells escape from the appendix or ovary and distribute throughout the peritoneal cavity. The eventual deposition of the tumor cells is determined by pathways of flow of peritoneal fluid and by gravity. Bulky tumor deposits in the omentum and right and left subphrenic spaces is most common. Deposition of tumor cells on bowel surfaces is uncommon except at the ileocecal region, the rectosigmoid regions, and the gastric antrum.

On gadolinium-enhanced MR imaging, pseudomyxoma peritonei is depicted as thick and heterogeneously enhancing peritoneal tumor masses (Figure 8). The peritoneal implants are typically less homogeneous in appearance than in ovarian cancer. This more heterogeneous appearance may reflect various amounts of nonenhancing mucinous material versus enhancing cellular tumor in the pseudomyxoma peritoneal implants. As in ovarian cancer, eventually all of the peritoneal surfaces become encased in tumor.

Conclusion

MR imaging of the GI tract and the peritoneum is a powerful clinical and imaging tool that can provide essential information to your patients and clinicians. By combining breath-hold MR imaging with intravenous and intraluminal contrast agents, images can be generated that capitalize on the superior contrast conspicuity of MRI to depict subtle diseases of the GI tract and the peritoneum. AR