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DOI: 10.1148/radiol.2281020728
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(Radiology 2003;228:157-165.)
© RSNA, 2003


Gastrointestinal Imaging

Distinguishing Benign from Malignant Bowel Obstruction in Patients with Malignancy: Findings at MR Imaging1

Russell N. Low, MD, Sloane C. Chen, MD and Robert Barone, MD

1 From the Sharp Memorial Hospital and Sharp Departments of Radiology (R.N.L., S.C.C.) and Surgical Oncology (R.B.), and Sharp and Children’s MRI Center (R.N.L., S.C.C.), 7901 Frost St, San Diego, CA 92123. Received June 19, 2002; revision requested August 9; revision received September 27; accepted November 22. Address correspondence to R.N.L.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To retrospectively evaluate the features of benign versus malignant bowel obstruction on unenhanced and gadolinium-enhanced spoiled gradient-echo magnetic resonance (MR) images in patients with malignancy.

MATERIALS AND METHODS: Forty-eight patients with malignancy and bowel obstruction underwent abdominal and pelvic MR imaging. Two blinded radiologists independently evaluated each study for dilated bowel, transition point, level of obstruction, obstructing mass, mural thickening and enhancement, and peritoneal disease. Benign obstruction was recorded if no mass was present and if mural thickening (when present) was segmental or diffuse. Malignant bowel obstruction was recorded if there was a mass, a disseminated abdominal tumor, or focal mural thickening. MR images were compared with surgical findings, follow-up imaging studies, and clinical outcome. {chi}2 test and Fisher exact test were used to assess the relationship between the MR features and benign versus malignant obstruction.

RESULTS: Bowel obstruction had a benign cause in 19 patients and a malignant cause in 29 patients. Observer 1 correctly characterized benign bowel obstruction in 17 of 19 patients and malignant bowel obstruction in 27 of 29 patients. The sensitivity of observer 1 for characterizing malignant obstruction was 93%, specificity was 89%, and accuracy was 92%. Observer 2 correctly characterized benign bowel obstruction in 18 of 19 patients and malignant bowel obstruction in 26 of 29 patients. The sensitivity of observer 2 for characterizing malignant obstruction was 90%, specificity was 95%, and accuracy was 92%. Malignant bowel obstruction was present in 24 of 25 patients with an obstructing mass (P < .001). All 16 patients with focal mural thickening had malignant obstruction. Benign obstruction was present in four of five patients with diffuse mural thickening. Segmental mural thickening occurred in four patients with serosal metastases and in 11 patients with benign bowel obstruction. More extensive peritoneal thickening and enhancement correlated with malignant obstruction.

CONCLUSION: In patients with malignancy who have symptoms indicative of bowel obstruction, gadolinium-enhanced MR imaging can help distinguish benign from malignant causes of bowel obstruction.

© RSNA, 2003

Index terms: Intestinal neoplasms, 74.31, 74.32 • Intestines, MR, 74.121412 • Intestines, stenosis or obstruction, 74.143


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Distinguishing benign from malignant bowel obstruction in a patient with malignancy is a critical diagnostic and imaging challenge that confronts radiologists and clinicians daily. Diagnosing benign or malignant bowel obstruction profoundly affects management decisions and has important prognostic implications (15). Benign bowel obstruction may be caused by postsurgical adhesions, radiation enteritis, abscess, phlegmon, or other infectious or inflammatory gastrointestinal diseases. Malignant bowel obstruction may be caused by an obstructing primary tumor, local tumor recurrence, or metastases involving the bowel and adjacent mesentery (615). While the list of benign and malignant causes is clear, the clinical manifestations of obstructions are often similar, and the results of diagnostic imaging examinations may be inconclusive.

Magnetic resonance (MR) imaging of the gastrointestinal tract has been proposed for patients with Crohn disease and some gastrointestinal malignancies (1623). The high contrast resolution of MR images, combined with gadolinium enhancement, allows one to depict subtle enhancing inflammatory or malignant processes involving the bowel (1618). There is clearly a wide spectrum of MR findings in patients with bowel obstruction. To our knowledge, no previous study has been performed to distinguish benign from malignant bowel obstruction on the basis of MR imaging. The purpose of our study was to retrospectively evaluate features of benign and malignant bowel obstruction at unenhanced and gadolinium-enhanced spoiled gradient-echo MR imaging in patients with malignancy.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Patients
A review of a computerized database of all MR examinations performed at our institution revealed a total of 48 consecutive patients with bowel obstruction who were referred for MR imaging of the abdomen and pelvis between 1996 and 2002. This study group represents a subset of all patients with bowel obstruction at our institution and is the result of clinician-based selection. At our institution, many oncology patients undergo MR imaging as the primary diagnostic imaging test. Patients were not recruited for this study. MR imaging was used for cross-sectional imaging on the basis of clinician preferences. In 10 patients, there were additional clinical contraindications to administration of iodinated contrast material, which prompted selection of MR imaging for patient evaluation. Our Institutional Review Board approved this retrospective review of MR images and patient records. Following the study, all identifiers were removed from the records to protect patient privacy. Informed consent was not required.

The diagnosis of bowel obstruction was confirmed on the basis of a review of each patient’s medical records and discharge summaries by one author (R.N.L.), a clinical presentation with nausea and vomiting, and radiographs of the abdomen demonstrating a dilated small bowel, colon, or both. The radiographic findings supportive of small-bowel obstruction included the presence of gas and fluid-filled small-bowel loops greater than 2.5 cm, which showed air-fluid levels and a degree of distention disproportionate compared with distal small bowel and the colon. Radiographic findings supportive of a diagnosis of colonic obstruction included the presence of colonic and small-bowel distention with a transition zone to collapsed distal colon. In 21 patients, 15 small-bowel oral barium examinations and six barium enema examinations were also used to confirm the presence of bowel obstruction. On the basis of all of the above information, one observer graded the degree of bowel obstruction as mild to moderate in 28 patients and high in 20 patients. Bowel obstruction was graded as mild to moderate if the bowel dilatation was less than 4 cm in diameter and if barium examinations (when performed) showed some delayed passage of barium beyond the point of obstruction. Bowel obstruction was graded as high if the bowel dilatation was greater than or equal to 4 cm in diameter and if barium examinations (when performed) showed no passage of barium distal to the point of obstruction. At the time of MR imaging, there were either clinical or radiographic findings suggestive of bowel obstruction.

Our study included 14 men and 34 women with a mean age of 62 years (range, 32–89 years). At the time of MR imaging, 44 patients had a known diagnosis of malignancy, while the remaining four patients had malignancy proven after the MR examination was performed. Twenty-three patients had colon cancer, 14 had ovarian cancer, four had endometrial cancer, three had cervical cancer, two had non-Hodgkin lymphoma, one had gastric cancer, and one had a leiomyosarcoma. Of the two patients with non-Hodgkin lymphoma, one had bulky abdominal tumor proven at surgery, and the other had benign obstruction due to pseudomembranous colitis proven at colonoscopy and biopsy.

MR Imaging
All MR examinations were performed with a 1.5-T imager (Signa; GE Medical Systems, Milwaukee, Wis) with high-performance gradients (23 mT/m, 120 mT · m-1 · sec-1) by using the body coil. Contrast material is routinely administered orally at our institution to patients in whom there is an interest in depicting gastrointestinal or peritoneal disease or disseminated abdominal tumor. In our study, 37 patients ingested oral contrast material, as determined according to the patient’s ability to tolerate ingestion. Starting 1 hour prior to imaging, patients were given 900 mL of 2% dilute barium oral contrast material (Readi-Cat 2; E-Z-Em, Westbury, NY) and were instructed to drink one bottle (450 mL) of dilute barium every 30 minutes. The volume that was tolerable varied from less than 100 mL in patients with high-grade bowel obstruction to 900 mL in patients with mild bowel obstruction. In 16 patients, water (500–1,000 mL) was administered into the rectum for colonic distention just prior to imaging. The decision to use water was based on a suspicion of a left-sided colonic obstruction as determined with conventional radiographs, clinical history, or both. The MR examination time for all pulse sequences was 30 minutes with breath-hold acquisitions, including T1-weighted, T2-weighted, and dynamic gadolinium-enhanced MR imaging of the abdomen and pelvis. The dilute barium sulfate and water provided negative intraluminal contrast on the T1-weighted and gadolinium-enhanced spoiled gradient-echo MR images and positive intraluminal contrast on the T2-weighted MR images.

A single-shot fast spin-echo coronal localizer image was obtained. Imaging parameters included repetition time of infinity, echo time of 94 msec (infinity/94), 256 x 256 matrix, one-half signal acquired, 7-mm section thickness, 3-mm section gap, echo train length of 94, and receiver bandwidth of ±62 kHz. Twelve sections were obtained during a 19-second breath hold. Transverse breath-hold, non–fat-suppressed, spoiled gradient-echo T1-weighted images were obtained with 160/4.4, 256 x 192 matrix, 1 signal acquired, 10-mm section thickness, 0-mm section gap, and receiver bandwidth of ±62 kHz. Transverse fat-suppressed T2-weighted images were obtained with either breath-hold fast-recovery fast spin-echo technique (2,500/77, 256 x 192 matrix, 1 signal acquired, 7-mm section thickness, 3-mm section gap, echo train length of 17, and receiver bandwidth of ±32 kHz) or respiratory-triggered, breathing-averaged, fast spin-echo technique (4,600/90, 256 x 224 matrix, two signals acquired, 7-mm section thickness, 3-mm section gap, echo train length of 11, and receiver bandwidth of ±32 kHz).

Gadolinium-enhanced spoiled gradient-echo breath-hold images with fat saturation were obtained in the transverse plane through the entire abdomen and pelvis immediately after the intravenous administration of 0.1 mmol/kg gadolinium chelate (gadopentetate dimeglumine, Magnevist, Berlex Laboratories, Wayne, NJ; Gadoversetamide, Optimark, Mallinckrodt Medical, St Louis, Mo; Gadodiamide, Omniscan, Amersham Health, Princeton, NJ). To cover the abdomen and pelvis in the transverse plane, four 24-second breath holds were required, and each produced 12 noncontiguous sections. Coronal and delayed transverse spoiled gradient-echo images were obtained 5 minutes after injection of contrast material. Imaging parameters included 141–165/2.1, 512–256 x 192 matrix with a three-quarter field of view for the transverse acquisition, one signal acquired, 8–10-mm-thick sections with no intersection gap, ±16–20-kHz receiver bandwidth, and 70° flip angle.

Proof of Disease
Medical, surgical, and histopathologic records were reviewed. The patient’s surgeon, oncologist, or both were interviewed by one author (R.N.L.) at the time of initial presentation and during clinical follow-up of patients. The cause of bowel obstruction was proved with surgical exploration in 30 patients, biopsy in eight, and clinical follow-up and review of imaging studies in the remaining 10. Among the 29 patients with malignant obstruction, disease was proved with surgery in 21 (72%) patients, biopsy in six (21%), and clinical and imaging follow-up in two (7%). Among the 19 patients with benign obstruction, disease was proved with surgery in nine (47%) patients, biopsy in two (11%), and clinical and imaging follow-up in eight (42%). Surgical biopsies and histopathologic evaluation were performed in the 30 patients who had surgical proof of disease. Percutaneous core biopsy was performed in five patients, and endoscopic biopsy was performed in one patient with pseudomembranous colitis, one patient with radiation enteritis, and one patient with a nonresectable primary colon cancer.

Specific causes of benign obstruction were established when possible. Radiation enteritis was established with a correlative history of radiation therapy in the involved area in patients with bowel obstruction. Ischemic bowel disease was established with endoscopic findings. Infectious or inflammatory bowel disease was established with endoscopic findings, a positive cytotoxicity test for toxin B, or both. Benign bowel obstruction due to adhesions was established with surgery in eight patients and was presumed to exist in three patients with bowel obstruction and a history of abdominal surgery. These patients did not previously undergo radiation therapy or have clinical evidence of infectious bowel disease. In these same patients, clinical follow-up showed no evidence of recurrent tumor for 8 months in one patient, 3 years in the second patient, and 5 years in the third patient.

For all patients, the time of clinical and imaging follow-up varied from 6 months to 5 years (mean, 14 months). Of the six patients with relatively short follow-up of 6–8 months, five had surgical proof of disease. One patient with ovarian cancer has been followed up for 5 years without evidence of recurrent tumor. Follow-up imaging included MR examinations in 15 patients, computed tomographic (CT) scanning in six patients, and both CT and MR in eight patients.

Clinical and imaging follow-up were accepted as evidence of malignant bowel obstruction if there was evidence of progressive tumor. A tumor was defined as progressive if a subsequent imaging study showed increasing size or number of abdominal and/or pelvic tumors, or a physical examination revealed palpable tumors and levels of serum tumor markers were elevated. Two patients with ovarian cancer and bowel obstruction had a disseminated abdominal tumor; one patient died 8 months and the other died 16 months (mean, 12 months) after the MR examination. Serial cross-sectional examinations showed progressive abdominal tumor in both patients.

Clinical and imaging follow-up were accepted as evidence of benign bowel obstruction in eight patients who were observed for 8–60 months (mean, 22 months). In these patients, symptoms of bowel obstruction resolved, and there was no clinical or imaging evidence of tumor at follow-up examinations. Six of the eight patients underwent follow-up cross-sectional examinations, the results of which confirmed absence of tumor. At this writing, the final two patients have been followed up clinically for 16 months (one patient) and 26 months (one patient) without any evidence of residual or recurrent tumor.

Cause and Location of Bowel Obstruction
Benign bowel obstruction was present in 19 patients and was caused by adhesions in 11 patients, radiation enteritis in five patients, infectious or inflammatory intestinal disease in two patients, and ischemic bowel disease in one patient. Malignant bowel obstruction was present in the remaining 29 patients and was caused by primary intestinal cancer in seven patients, serosal metastases in 16 patients, and an adjacent mass in six patients. Among all 48 patients, the level of bowel obstruction was localized to the middle small bowel in five patients, distal small bowel in 23 patients, ascending colon in one patient, descending colon in three patients, and rectosigmoid colon in 16 patients.

Review of MR Images
Two radiologists (R.N.L., S.C.C.) with 12 years and 6 years of experience, respectively, in interpreting abdominal MR images were blinded to patient diagnosis and identifying data, results of biopsy, and other imaging studies. These physicians independently reviewed all MR images of each patient. Observers evaluated images from the entire examination, including images obtained with all imaging sequences. For each patient, the observers evaluated the MR images for the presence of dilated bowel, a transition point, the level of bowel obstruction, masses producing the bowel obstruction, mural thickening and enhancement, and peritoneal enhancement. Mural thickening was described as mild (>3 mm, <5 mm), moderate (≥5 mm, ≤15 mm), or marked (>15 mm). The distribution of mural thickening was described as focal if the segment of bowel was less than or equal to 10 cm, segmental if the segment of the bowel was greater than 10 cm, or diffuse if at least 50% of the bowel was involved. Peritoneal disease was described as mild if the peritoneum showed minimal or no thickening (≤3 mm) with abnormal enhancement greater than liver parenchyma. Moderate peritoneal disease was recorded if the thickness was greater than 3 mm but less than 10 mm. Marked peritoneal disease was recorded if the thickness was greater than or equal to 10 mm. Mild mural enhancement was described if the bowel wall enhanced more than the liver parenchyma and marked if the degree of enhancement equaled that of adjacent vessels.

On the basis of these independent observations, both observers also categorized each case as benign or malignant bowel obstruction. The criteria for selecting benign or malignant cause of bowel obstruction included the presence or absence of an obstructing mass and the distribution of mural thickening. Benign bowel obstruction was recorded for patients with no obstructing mass present and if mural thickening (when present) was either segmental or diffuse. Malignant bowel obstruction was recorded for patients with an obstructing mass, focal mural thickening, or evidence of disseminated abdominal tumor. The presence of relevant concomitant findings of malignancy such as liver metastases, which were depicted in two patients, was not used to determine a benign or malignant cause of bowel obstruction. The categories of and classification as benign and malignant was based on published CT findings (2430) and on our known clinical and MR imaging experience. Prior CT reports have established that the presence of a neoplasm or space-occupying lesion at the point of obstruction indicates malignant bowel obstruction, while the absence of a mass at the transition site indirectly suggests a benign obstruction due to adhesions (2430). For each observer, the sensitivity, specificity, and accuracy of predicting benign or malignant bowel obstruction were recorded.

Both observers then reviewed the MR images jointly. Differences regarding the presence or degree of specific features of bowel obstruction were resolved by consensus. The information from the consensus review of the MR images was not used to change either observer’s initial interpretation of benign or malignant bowel obstruction.

After this blinded review of the MR images, one author (R.N.L.) reviewed proof of disease. Each MR feature of bowel obstruction was correlated with either benign or malignant obstruction. Also, combinations of MR findings were noted for the 29 patients with malignant bowel obstruction. Complications from the MR examinations were noted and recorded in written reports or nursing notes.

The initial prospective interpretations of the MR examinations as recorded in the written MR reports were also evaluated. The criteria used to establish benign or malignant bowel obstruction in the prospective reports were less defined than in the retrospective review of the MR images, but the reports do reflect the radiologist’s initial interpretation. The ability to distinguish malignant from benign bowel obstruction in the prospective interpretations was assessed, and the corresponding prospective sensitivity, specificity, and accuracy were calculated.

Statistical Analysis
The {kappa} coefficient of interobserver agreement was calculated for the depiction of the specific features of benign versus malignant bowel obstruction. Fisher exact test and {chi}2 test were used to assess the relationship between the MR features and the presence of benign versus malignant bowel obstruction and to investigate and test for significant differences between the groups. Two-by-two or two-by-three contingency tables were constructed. The null hypothesis was rejected if P values were less than or equal to .05.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Retrospective Independent Review of MR Images
On the basis of the findings established at independent retrospective review of the MR examinations, observers 1 and 2 correctly predicted benign obstruction in 17 and 18 of the 19 patients, respectively (Fig 1) and malignant obstruction in 27 and 26 of the 29 patients, respectively. For characterizing malignant obstruction, observer 1 had a sensitivity of 93%, a specificity of 89%, and an accuracy of 92%. The corresponding values for observer 2 were 90%, 95%, and 92%.



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Figure 1. MR image of a patient with colon cancer who previously underwent radiation therapy and who now has bowel obstruction. Transverse gadolinium-enhanced spoiled gradient-echo MR image (165/2.1; flip angle, 70°) shows segmental mural thickening (arrows) measuring approximately 1 cm and enhancement of all visualized pelvic bowel. No obstructing mass was present. Findings correlate with radiation enteritis. Both observers correctly predicted benign bowel obstruction.

 
Observer 1 made false-positive interpretations of malignant obstruction in two patients and observer 2 made a false-positive interpretation in one patient. In one of the two patients, a small, nonenhancing fibrotic pelvic mass occurred at the point of obstruction due to adhesions. In the second patient, there were discontinuous areas of mild segmental mural thickening without an obstructing mass. One observer misinterpreted the findings as multifocal serosal tumor. Benign obstruction due to adhesions was found at surgery.

False-negative interpretations occurred in two patients for observer 1 and in three patients for observer 2. In one patient, serosal metastasis produced segmental mural thickening that extended over a 15-cm segment of the distal ileum. This length was longer than the 10-cm definition we used for focal mural thickening. In review of our cases of benign segmental thickening, all but one case showed much longer segments of thickened bowel, while the segmental mural thickening in malignant obstruction typically involved shorter segments of bowel. The second false-negative interpretation occurred in a patient with a 2-cm obstructing pelvic mass that was not depicted on MR images. Observer 2 also did not identify a small obstructing nodal mass in a patient with high-grade small-bowel obstruction. In this patient, an associated finding of moderate peritoneal tumor was noted but not used to distinguish benign from malignant bowel obstruction.

Features of Malignant and of Benign Bowel Obstruction: Consensus Review of MR Images
Table 1 lists the specific features of benign and malignant bowel obstruction, as established by means of a consensus reading by the two observers. Salient features are summarized below.


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TABLE 1. Features of Benign Bowel Obstruction and Malignant Bowel Obstruction

 
An obstructing mass correlated with malignant bowel obstruction in 24 of 25 patients and was the most reliable indicator of malignant bowel obstruction (P < .001; {chi}2 = 24.605) (Figs 2 and 3). One patient with a small fibrotic pelvic mass from benign adhesions was incorrectly believed to have malignant obstruction.



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Figure 2a. MR images of a patient with treated ovarian cancer. (a) Coronal gadolinium-enhanced spoiled gradient-echo MR image (140/2.1; flip angle, 70°) shows a bulky abdominal mass (arrows) producing bowel obstruction. The confluent abdominal mass involves the peripancreatic and portal regions superiorly and the small-bowel mesentery inferiorly. (b) Transverse gadolinium-enhanced spoiled gradient-echo MR image (140/2.1; flip angle, 70°) depicts a tumor mass (arrows) at the point of bowel obstruction. Other images (not shown) depicted bulky peritoneal tumor and a transition point in bowel dilatation. Both observers correctly predicted malignant bowel obstruction. Findings were confirmed at surgery.

 


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Figure 2b. MR images of a patient with treated ovarian cancer. (a) Coronal gadolinium-enhanced spoiled gradient-echo MR image (140/2.1; flip angle, 70°) shows a bulky abdominal mass (arrows) producing bowel obstruction. The confluent abdominal mass involves the peripancreatic and portal regions superiorly and the small-bowel mesentery inferiorly. (b) Transverse gadolinium-enhanced spoiled gradient-echo MR image (140/2.1; flip angle, 70°) depicts a tumor mass (arrows) at the point of bowel obstruction. Other images (not shown) depicted bulky peritoneal tumor and a transition point in bowel dilatation. Both observers correctly predicted malignant bowel obstruction. Findings were confirmed at surgery.

 


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Figure 3. MR image of a patient with treated cervical cancer and high-grade bowel obstruction. Transverse gadolinium-enhanced spoiled gradient-echo MR image (140/2.1; flip angle, 70°) shows marked bowel distention and an obstructing 3-cm mass (arrows) in the right lower quadrant. Gadolinium enhancement improves the conspicuity of the obstructing tumor. Focal mural thickening was better depicted on adjacent images (not shown). Enhancing peritoneal tumor (arrowheads) is present in the lower abdomen and pelvis. Metastatic cervical cancer producing bowel obstruction was confirmed at surgery. Both observers correctly predicted malignant bowel obstruction.

 
The distribution of mural thickening was also useful. Focal mural thickening correlated with malignant obstruction (P < .001; {chi}2 = 17.601) (Fig 4) and diffuse mural thickening was benign in four of five patients. One patient with diffuse mural thickening also had a small obstructing mass, which was found at surgery. The mass was not depicted on MR images, and led to a false-negative interpretation of malignant bowel obstruction. Segmental mural thickening occurred in malignant and benign bowel obstruction (Fig 1). Malignant segmental mural thickening occurred in four patients with serosal metastases (Fig 5) and was more localized than the segmental mural thickening that occurred in 11 patients with benign bowel obstruction (Fig 1), which involved longer segments of bowel, was often bilateral, and was sometimes in the distribution of a radiation port.



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Figure 4a. MR images of a patient with a history of rectal cancer and who now has abdominal pain and bowel obstruction. (a) Transverse gadolinium-enhanced spoiled gradient-echo MR image (165/2.1; flip angle, 70°) through the middle of the abdomen depicts focal mural thickening (arrows) involving an 8-cm segment of the transverse colon. No obstructing mass was present. (b) Coronal gadolinium-enhanced spoiled gradient-echo MR image (160/2.1; flip angle, 70°) depicts mural thickening of the transverse colon (white arrows). Additionally, note the focal mural thickening (black arrow) of the gastric antrum. Findings correlate with surgically proven serosal metastases from the patient’s rectal cancer. Both observers correctly predicted malignant bowel obstruction.

 


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Figure 4b. MR images of a patient with a history of rectal cancer and who now has abdominal pain and bowel obstruction. (a) Transverse gadolinium-enhanced spoiled gradient-echo MR image (165/2.1; flip angle, 70°) through the middle of the abdomen depicts focal mural thickening (arrows) involving an 8-cm segment of the transverse colon. No obstructing mass was present. (b) Coronal gadolinium-enhanced spoiled gradient-echo MR image (160/2.1; flip angle, 70°) depicts mural thickening of the transverse colon (white arrows). Additionally, note the focal mural thickening (black arrow) of the gastric antrum. Findings correlate with surgically proven serosal metastases from the patient’s rectal cancer. Both observers correctly predicted malignant bowel obstruction.

 


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Figure 5. MR image of a patient with treated colon cancer and partial bowel obstruction. Transverse gadolinium-enhanced spoiled gradient-echo MR image (165/2.1; flip angle, 70°) shows segmental mural thickening (arrows), which involved a 15-cm segment of the distal ileum without an obstructing mass. Both observers incorrectly predicted benign obstruction on the basis of the segmental (>10 cm) length of bowel wall thickening and absence of an obstructing mass.

 
Peritoneal disease occurred in both patients with benign obstruction and patients with malignant obstruction but was typically mild in benign obstruction and moderate or marked in malignant obstruction (P < .001; {chi}2 = 17.355) (Fig 3).

Other MR features of bowel obstruction, such as the degree of bowel dilatation, the degree of mural thickening, and the presence of mural enhancement, showed no correlation with benign or malignant intestinal obstruction (Table 1).

Of the 29 patients with malignant bowel obstruction, 24 had an obstructing mass at MR imaging (Figs 2 and 3). Twenty-one patients demonstrated mural thickening, which was focal in 16 patients, segmental in four patients with serosal metastases, and diffuse in one patient. The degree of mural thickening in patients with serosal metastases producing bowel obstruction was either moderate or marked. Mild mural thickening without an obstructing mass was never a feature of malignant bowel obstruction. Peritoneal thickening and enhancement were present in 16 patients and were mild in one patient, moderate in five, and marked in 10. Table 2 describes the combined MR features of malignant bowel obstruction. The most common combination of findings, seen in 11 of 29 patients, was the presence of an obstructing mass, focal mural thickening, and moderate to marked peritoneal disease (Fig 3). An isolated obstructing mass without additional findings was the next most common pattern and was seen in seven patients. Four patients with malignant obstruction did not have an obstructing mass. Two patients had focal mural thickening, one patient had localized segmental thickening (15 cm) that was incorrectly categorized as benign obstruction, and the final patient had more extensive serosal metastases combined with disseminated abdominal tumor.


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TABLE 2. Combined MR Features of Malignant Bowel Obstruction

 
Of the 19 patients with benign bowel obstruction, MR findings were characterized by the absence of a mass in 18 of 19 patients (Fig 6). Mural thickening was present in 15 of 19 patients. Mural thickening was characterized as segmental in 11 patients with radiation enteritis (n = 3), infectious enteritis (n = 2) (Fig 7), postoperative adhesions (n = 5), or ischemic enteritis (n = 1) and as diffuse in four patients with radiation enteritis (n = 1) or postoperative adhesions (n = 3). Peritoneal enhancement was present in 11 of 19 patients and was characterized as mild in nine and moderate in two.



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Figure 6. MR image of a woman with a 3-year history of ovarian cancer and who now has bowel obstruction. Transverse gadolinium-enhanced spoiled gradient-echo MR image (165/2.1; flip angle, 70°) shows enhancing dilated small bowel (arrows) with mild mural thickening but no obstructing mass. Both observers correctly predicted benign bowel obstruction. The patient’s bowel obstruction resolved, and she has remained tumor free for 5 years without additional treatment. Bowel wall enhancement is a nonspecific finding seen in both malignant and benign bowel obstruction.

 


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Figure 7. MR image of a patient with a history of lymphoma who now has abdominal pain and bowel obstruction. Coronal fat-suppressed gadolinium-enhanced spoiled gradient-echo MR image (140/2; flip angle, 70°) shows marked segmental mural thickening (arrows) and enhancement of the descending colon. No obstructing mass was present. Pseudomembranous colitis was confirmed with endoscopy and clinical evaluation, with a positive cytotoxicity test for toxin B. Both observers correctly predicted benign bowel obstruction.

 
Table 1 represents a consensus reading by the two observers for discordant findings. There was good agreement regarding the bowel dilatation, peritoneal disease, presence or absence of a mass, and the presence and distribution of mural thickening. Discrepancies of interpretation tended to center around the degree of mural thickening, peritoneal enhancement, and bowel dilatation.

Prospective Review of MR Images
The initial prospective interpretations of the MR images resulted in correct predictions of malignant bowel obstruction in 27 patients with two false-negative interpretations, 12 true-negative interpretations (Fig 8), and seven false-positive interpretations, yielding a corresponding sensitivity of 93%, specificity of 63%, and accuracy of 81%.



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Figure 8a. MR images of a patient with colon cancer who previously underwent colectomy and who now has acute small-bowel obstruction. (a) Coronal and (b) transverse gadolinium-enhanced spoiled gradient-echo MR images (165/2.1; flip angle, 70°) show markedly dilated small bowel (long arrows in a and white arrows in b) with mild diffuse mural thickening (short arrows in a) and mural enhancement. In the pelvis, the transverse image (b) shows mesenteric infiltration and tethering (black arrow) of the dilated small bowel, without evidence of an obstructing mass. Mild peritoneal enhancement was noted on other images (not shown). Findings at surgery confirmed small-bowel obstruction due to adhesions. Both observers correctly predicted benign bowel obstruction.

 


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Figure 8b. MR images of a patient with colon cancer who previously underwent colectomy and who now has acute small-bowel obstruction. (a) Coronal and (b) transverse gadolinium-enhanced spoiled gradient-echo MR images (165/2.1; flip angle, 70°) show markedly dilated small bowel (long arrows in a and white arrows in b) with mild diffuse mural thickening (short arrows in a) and mural enhancement. In the pelvis, the transverse image (b) shows mesenteric infiltration and tethering (black arrow) of the dilated small bowel, without evidence of an obstructing mass. Mild peritoneal enhancement was noted on other images (not shown). Findings at surgery confirmed small-bowel obstruction due to adhesions. Both observers correctly predicted benign bowel obstruction.

 
Among the original written reports, there were seven false-positive interpretations of malignant obstruction. Six of the seven patients demonstrated mild segmental or diffuse mural thickening and enhancement that was often associated with mild peritoneal enhancement but no evidence of an obstructing mass. The more rigorously applied definition of malignant bowel obstruction used in our study leads us to conclude that these six cases should be classified as benign bowel obstruction.

{kappa} analysis showed good interobserver agreement. For evaluating the level of obstruction, presence of a transition point, dilated bowel, an obstructing mass (Fig 9), the intestinal or extraintestinal location of the mass, mural enhancement, peritoneal enhancement, the presence and distribution of mural thickening, and the characterization of benign or malignant obstruction, the two observers agreed on 446 of 480 observations, {kappa} = 0.80. The range of {kappa} values for the different features of bowel obstruction varied from 0.56 for determining the degree of bowel dilatation to 0.91 for characterizing the bowel obstruction as benign or malignant.



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Figure 9. MR image of patient with treated ovarian cancer and bowel obstruction. Transverse gadolinium-enhanced spoiled gradient-echo MR image (165/2.1; flip angle, 70°) shows pelvic ascites (A) and an enhancing mass (arrows) invading a 10-cm segment of the sigmoid colon. The presence of the mass confirms malignant obstruction. Both observers correctly predicted malignant bowel obstruction.

 
Two patients experienced emesis at the time of the MR examination. All other patients tolerated the MR examination without reported complications.


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Bowel obstruction is a common complication in patients with advanced stage cancer; it occurs in 5%–42% of patients with advanced ovarian cancer (611) and 4%–24% of patients with advanced colorectal cancer (1215). Both benign and malignant causes of bowel obstruction must be considered, however, as the distinction between nonmalignant and malignant causes of intestinal obstruction can be critical to patient care (15). Primary and recurrent tumor must be distinguished from a host of benign causes of bowel obstruction, including adhesions, inflammatory bowel disease, hernias, and postirradiation enteritis. After abdominal surgery for cancer, nonmalignant adhesions account for 21%–38% of intestinal obstructions, while malignant obstruction accounts for the remaining 62%–79% (3,4). It has been reported that in patients with colorectal cancer, nearly half of the cases of bowel obstruction are caused by benign conditions (14).

The diagnostic value of cross-sectional imaging is most obvious in patients in whom the findings at CT or MR imaging can assist the clinician in choosing surgical or conservative medical management (2428). Cross-sectional studies may depict an obstructing mass, peritoneal carcinomatosis, or nodal metastases. In the patient with benign obstruction, CT or MR imaging may show findings of radiation enteritis, infectious or inflammatory intestinal disease, or indirect evidence of adhesions. Adhesions may be diagnosed indirectly by means of the notable absence of a mass at the transition point. The sensitivity of CT for correctly predicting the cause of bowel obstruction was 73% in a study evaluating 64 patients with bowel obstruction (25). The value of CT in the setting of bowel obstruction was demonstrated by Taourel et al (28), who showed that the findings at CT modified the decision to pursue surgical versus nonsurgical treatment of bowel obstruction in 21% of patients.

The clinical decision to pursue surgical versus conservative medical management of bowel obstruction will depend on multiple factors, including the cause, level, and degree of bowel obstruction, the patient’s clinical condition, and the presence of advanced metastatic tumor in the abdomen and pelvis (15). Management of primary obstructing gastrointestinal cancers may include resection or bypass of the obstructing mass, radiation or chemotherapy, and stent placement in patients who are poor surgical candidates (15,15). Bowel obstruction in a patient with recurrent tumor may be caused by local tumor recurrence or distant peritoneal and serosal metastases. Localized metastatic disease producing intestinal obstruction may be managed surgically with resection and primary anastamosis with multiple side-to-side enterostomies in a patient with obstructing carcinomatosis. On the other hand, patients with incomplete bowel obstruction due to benign conditions such as adhesions, radiation enteritis, or other inflammatory conditions may benefit from a trial of conservative medical management. Medical management may also be indicated in the patient with advanced cancer and bowel obstruction in the setting of diffuse metastatic cancer, intraabdominal carcinomatosis, or rapidly recurring massive ascites (5). These contraindications to surgery reflect the overall poor prognosis of these patients and the high perioperative mortality in patients with advanced cancer after laparotomy for bowel obstruction.

The decision to use MR imaging or helical CT in oncology patients with bowel obstruction will be based on many factors, including cost, availability, radiologist expertise, and clinician preference. At most institutions, helical CT is the cross-sectional imaging examination used in patients with bowel obstruction (2429). Compared with MR imaging, helical CT scanning is clearly performed more quickly, and the equipment is typically more readily available. Multidetector helical CT with reconstruction further accentuates many of the advantages of abdominal CT scanning. With the increasing use of MR imaging in oncology patients, however, an understanding of the capabilities of MR imaging in patients with bowel obstruction is essential for correct image interpretation and patient care. Certainly the patient with allergy to contrast material or renal insufficiency may be evaluated with MR imaging. While our experience is atypical for most institutions, our oncologists often use MR imaging as the primary cross-sectional imaging test in many of their patients. This reflects, in part, the proven ability of MR imaging to depict hepatic and extrahepatic tumor and the charge of the MR examination, which at our institution is less than the charge of a corresponding helical CT examination.

To our knowledge, the role of MR imaging in the oncology patient with bowel obstruction has not been previously explored. The adoption of faster MR imaging techniques, combined with intraluminal contrast materials, has facilitated MR imaging of the gastrointestinal tract (16,17,23,31,32). Potential advantages of MR imaging include its excellent soft-tissue contrast, which facilitates depiction of enhancing tumors and peritoneal carcinomatosis. Mural thickening of the bowel wall is also well depicted on gadolinium-enhanced MR images (1618). Overall, in our study MR imaging distinguished benign from malignant intestinal obstruction well, with sensitivity and accuracy greater than 90% for both observers.

The important differentiation between benign adhesions and malignant obstruction due to carcinomatosis can be problematic. Bowel obstruction due to adhesions may show mild peritoneal enhancement and mesenteric infiltration, often with segmental or diffuse mural thickening but without an obstructing mass. In our study, this pattern correlated with benign obstruction and was not seen in patients with malignant bowel obstruction. Carcinomatosis that causes bowel obstruction produces moderate or bulky peritoneal thickening and tumor masses, indicating malignant obstruction. These patients often show findings of disseminated abdominal tumor. The distribution of mural thickening can also provide important clues in distinguishing benign from malignant obstruction. Focal mural thickening indicates malignant obstruction, most commonly from serosal metastases. Diffuse mural thickening without an obstructing mass indicates benign obstruction, and segmental mural thickening can occur in either benign or malignant bowel obstruction.

The ability of MR imaging to depict peritoneal tumor and hepatic and extrahepatic tumor also assists clinicians in determining the extent of abdominal tumor and in selecting appropriate medical or surgical treatment options. While we did not evaluate the different sequences and imaging planes, it is our experience that fat-suppressed gadolinium-enhanced spoiled gradient-echo MR imaging in the transverse plane is most useful for depicting mural thickening, peritoneal tumor, and an enhancing obstructing bowel mass. In practice, we rely heavily on these images in patients with bowel obstruction.

The use of dilute barium sulfate as an oral contrast material has been described to achieve bowel distention and separation. While the use of this agent for MR imaging is an off-label application, dilute barium sulfate has a relatively long history of use and is well tolerated by patients. In patients with bowel obstruction, oral contrast material can precipitate nausea and vomiting and can potentially lead to complications such as bowel perforation. The 2% barium sulfate used in our study is much less concentrated than the barium that is often used for small-bowel gastrointestinal series in patients with bowel obstruction. In addition, prior to MR imaging, each patient is instructed to drink the dilute barium sulfate as tolerated, which allows the patient to titrate the amount of oral contrast material that he or she ingests. Typically, patients with high-grade bowel obstruction require less oral contrast material for bowel distention and are able to ingest less oral contrast material.

Limitations of this study include the lack of pathologic proof in all patients. Since more of the patients with malignant obstruction had surgical proof of disease than the patients with benign obstruction, this may have introduced bias into the study. Clinical and imaging follow-up, combined with consultation with the patient’s oncologist, however, provided clear evidence of either progressive tumor in patients with malignant bowel obstruction or resolution of symptoms and no evidence of tumor at follow-up in patients with benign obstruction. Because our patient population represents a subset of all patients with bowel obstruction at our institution, the effects of selection bias must be considered. A direct comparison of the results of MR imaging and helical CT in the oncology patient with bowel obstruction will be essential but was beyond the scope and design of the current retrospective study. Finally, the population described in this article was highly selected, including only patients with mechanical bowel obstruction and a history of malignancy. The application of these MR imaging techniques to a less selected patient population is not addressed by our study.

While our MR imaging protocol is a comprehensive screen of the abdomen and pelvis, including unenhanced T1-weighted, T2-weighted, and dynamic gadolinium-enhanced imaging of the abdomen and pelvis, more tailored examinations of the liver with three phases could also be performed. Liver-specific contrast agents may also play a role in this evaluation in the future. Our MR protocol provides an excellent screening examination of the abdomen and pelvis and is especially effective for evaluating patients with bowel obstruction. As with all MR examinations, this protocol can be tailored to answer specific clinical questions.

In conclusion, by using currently available techniques, MR imaging is effective in distinguishing benign from malignant bowel obstruction in patients with cancer. Features that indicate malignant bowel obstruction include the presence of an obstructing mass, focal or localized segmental mural thickening, and moderate or marked peritoneal thickening and enhancement. Benign intestinal obstruction is indicated by the absence of an obstructing mass and more generalized segmental or diffuse mural thickening. Careful attention to these features of bowel obstruction will allow the radiologist to provide valuable information that may assist oncologic diagnosis and treatment planning.


    FOOTNOTES
 
Author contributions: Guarantor of integrity of entire study, R.N.L.; study concepts, R.N.L., S.C.C.; study design, R.N.L.; literature research, R.N.L.; clinical studies, R.B; data acquisition, R.N.L., S.C.C., R.B.; data analysis/interpretation, R.N.L., S.C.C.; statistical analysis, R.N.L.; manuscript preparation, R.N.L., S.C.C.; manuscript definition of intellectual content, R.N.L.; manuscript editing, R.N.L., S.C.C., R.B.; manuscript revision/review and final version approval, R.N.L., S.C.C., R.B.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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