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1
Department of Diagnostic Radiology, University Hospital Essen, Hufelandstr.
55, D-45122 Essen, Germany.
2
Department of Gastroenterology and Hepatology, University Hospital Essen,
D-45122 Essen, Germany.
Received January 31, 2001;
accepted after revision April 3, 2001.
Address correspondence to J. F. Debatin.
Abstract
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SUBJECTS AND METHODS. Six healthy volunteers and six patients with suspected colorectal tumors, undergoing conventional colonoscopy within 1 week of MR imaging, were included in this study. For fecal tagging, 200 mL of a barium-containing contrast agent was ingested with each of four principal meals preceding the examination. For MR colonography, the colon was filled with a barium and water mixture while gadobenate dimeglumine (0.2 mmol/kg) was injected IV.
RESULTS. The combination of fecal tagging and colonic filling with barium resulted in a homogeneously low signal throughout the colonic lumen in all 12 subjects. IV injection of gadolinium caused avid enhancement of the colonic wall. Similarly, lesions arising from the colonic wall enhanced avidly. In the six evaluated patients, MR colonography correctly identified two colonic carcinomas in two patients and one polyp in each of another two patients.
CONCLUSION. Fecal tagging obviates bowel cleansing and should, therefore, enhance patient acceptance for MR colonoscopy. Barium used as the tagging agent is promising because it is inexpensive, commercially available, and characterized by an excellent safety profile.
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Recent studies have shown virtual colonography based on either CT or MR three-dimensional (3D) data sets to be effective in the detection of clinically relevant polyps exceeding 10 mm [6,7,8,9]. Both CT and MR colonography are considerably less painful than colonoscopy. Because colonic polyps are difficult to differentiate from residual stool, both CT and MR colonography continue to require a cleansed colon. Hence, patient acceptance for screening purposes continues to be limited [10]. Cleansing protocols could be eliminated if the signal intensity of fecal material was rendered similar to that of the contrast agent used to distend the colon. This concept of fecal tagging has been proposed in conjunction with MR colonography with gadolinium-based agents for rectal filling and oral tagging [11]. High contrast-agent costs have limited the clinical impact of that technique, however.
The objective of this study was to evaluate the feasibility of fecal tagging in conjunction with MR colonography with an inexpensive contrast agent, barium sulfate.
Prior concepts of MR colonography have been based on a bright colonic lumen induced by the administration of a rectal enema spiked with gadopentetate dimeglumine in which polyps are visualized as dark filling defects. The proposed strategy is based on rendering the colonic lumen dark by means of a rectal enema of barium sulfate and visualization of colonic polyps by virtue of their enhancement after the IV injection of a paramagnetic gadolinium-based contrast agent. The contrast-enhanced colonic wall is imaged with an ultrafast heavily T1-weighted 3D gradient-echo sequence. Beyond the rectal enema, the colonic lumen contains air and stool. Whereas air exhibits no signal, stool can be signal-rich on T1-weighted images, reflecting the presence of manganese or iron in various foodstuffs. To assimilate the signal of stool to the dark barium sulfate enema filling the colonic lumen, the stool signal must be reduced. To this end, barium sulfate was used as the oral fecal tagging agent.
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MR colonography was performed on a 1.5-T MR system (Magnetom Sonata; Siemens Medical Systems, Erlangen, Germany). To permit coverage of the entire colon, an overlap of body array and large flex coil was used for signal reception. No sedative or analgesic agents were used. To reduce bowel motion and alleviate colonic spasm, 20 mg of scopolamine (Buscopan; Boehringer Ingelheim, Germany) was administered IV before filling the colon by rectal enema with 2000-2500 mL of a 1:4 mixture of barium (5 g/100 mL) and water while the patient was lying prone on the scanning table. To ensure safe and optimal filling of the colon, the filling process was monitored with a non-slice-select acquisition (TR/TE, 1.3/4.2; flip angle, 25°; matrix, 128 x128), collecting one image every 3 sec. Once the enema reached the cecum, gadobenate dimeglumine (Multihance; Bracco, Milan, Italy) was injected IV in a dose of 0.2 mmol/kg at a flow rate of 3 mL/sec followed by rapid injection of 20 mL of normal saline at the same rate. A 3D data set was acquired in the coronal plane 75 sec after completion of the gadobenate dimeglumine administration with a T1-weighted 3D gradient-echo sequence (1.64/0.6). Other sequence parameters included a flip angle of 15°, a field of view of 45 cm, and a matrix of 230 x 256. Sixty-four contiguous slices with a thickness of 3.14 mm were collected as part of each 3D data set. Using zero interpolation in the slice direction, we reduced the effective slice thickness by 1.57 mm. The data were collected over 22 sec in end inspiration during a single breath-hold. After the acquisition of this sequence, the enema bag was placed on the floor for facilitated emptying of the colon, and the patient was removed from the scanner.
The first part of the study was conducted on six healthy volunteers without
any history of gastrointestinal symptoms or surgery (mean age, 32 years; age
range, 28-37 years). One volunteer serving as an internal control did not
ingest the barium sulfate tagging agent, whereas the other five volunteers
underwent the fecal tagging protocol, as outlined previously. MR colonography
was performed on all volunteers. Signal characteristics of the colonic wall
were evaluated relative to the tagged (n = 5) and untagged fecal
material. To this end, regions of interest (ROI) were placed in the lumen and
wall of the ascending, transverse, and descending colon. Furthermore, image
noise, defined as the standard deviation of signal intensities measured in a
ROI placed outside the body, was determined. On the basis of these
signal-intensity (SI) measurements, contrast-to-noise ratios (CNR) were
calculated in the usual manner:
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After successful completion of the volunteer studies, six patients with
suspected colorectal tumors also underwent MR colonography after fecal
tagging. All patients underwent conventional colonoscopy within 1 week of MR
imaging. Three-dimensional MR data sets were analyzed interactively on a
workstation (Virtuoso, Siemens Medical Systems) in the multiplanar reformation
mode and on the basis of virtual endoscopic renderings by an observer unaware
of the findings of conventional colonoscopy. ROI measurements were performed
in detected lesions and in the adjacent lumen. On the basis of these
measurements, CNRs were calculated in the usual fashion:
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The study was conducted in accordance with all guidelines set forth by the approving institutional review board. Informed consent was obtained before each imaging from each subject.
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After fecal tagging, the signal in the colonic lumen was homogeneously dark, permitting the selective depiction of the contrast-enhancing colonic wall (Fig. 1). Signal differences between luminal stool and colonic walls were high throughout the colon as evidenced by a mean CNR of 24.65 ± 3.7 (range, 18.7-29.0) (Table 1). There were no statistically significant differences (p > 0.05) between the various colonic regions with a mean CNR of 24.3 ± 4.0 (range, 18.7-27.7) in the ascending colon, of 24.2 ± 2.9 (range, 20.3-28.0) in the transverse colon, and of 25.5 ± 3.5 (range, 21.0-29.0) in the descending colon. CNRs were sufficiently high to permit virtual endoscopic viewing of the entire colon with visualization of colonic haustra (Fig. 2A,2B). The tagged stool was virtually indistinguishable from the administered enema.
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MR colonography performed on the control volunteer who had not ingested the tagging agent revealed signal-rich stool that could not readily be differentiated from the brightly enhancing colonic wall (Fig. 1). CNRs in this volunteer were significantly lower (p < 0.01) with measurements ranging from 6.0 in the ascending, to -5.1 in the transverse, and 2.4 in the descending colon. This difference in volunteer data solely reflected the higher signal of the stool in the untagged subject and documented the signal-reducing effects on stool of the proposed fecal tagging strategy.
Conventional colonoscopy performed in six patients revealed a single 10-mm polyp located in the sigmoid colon in one patient, a single 6-mm polyp located in the descending colon in one patient, a carcinoma located in the rectum in one patient, and another colonic carcinoma presumably located in the right colonic flexure in one patient. No masses were identified in the remaining two patients. MR colonography in conjunction with fecal tagging correlated well with conventional colonoscopy. The colonic lumen containing the barium enema, air, and tagged stool was characterized by homogeneously low signal, permitting virtual endoscopic renderings similar to those achieved in the volunteer examinations. Fully correlating with conventional colonoscopy, the blinded analysis of MR colonography failed to reveal any disease in two patients. Because of easily delineated enhancement of lesions, blinded analysis identified both polyps in the sigmoid (Fig. 3A,3B,3C) and descending colon. Furthermore, both colonic carcinomas (Fig. 4) were also detected on the basis of their avid enhancement after the IV administration of a paramagnetic contrast agent. In contrast to conventional colonoscopy, however, MR colonography located one carcinoma in the transverse colon just proximal to the splenic flexure—a location subsequently confirmed at surgery. All four lesions were easily recognized as such on multiplanar reformats and on virtual endoscopic images (Fig. 3A,3B,3C).
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In most centers, colonoscopy has emerged as the principal means of examining the colon. It offers the convenience of examination and biopsy or polyp removal but has multiple disadvantages, including procedural discomfort resulting in the need for patient sedation, a small but defined risk for perforation, and the inability to reach the cecum in up to 5% of patients [12]. Moreover, colonoscopy is limited by poor patient acceptance, which is a most important variable for a screening test [4, 5, 13]. Thus Rex et al. [14] have shown that even when it is offered free of charge, most patients refused to undergo the test for primary colorectal cancer screening.
Virtual colonography combines the breath-hold acquisition of 3D CT or MR data sets with advanced data postprocessing to provide computer-simulated multiplanar exoscopic and virtual endoscopic views of the colon [7, 9, 15]. On the basis of cross-sectional images, this type of examination offers several advantages over conventional colonoscopy, the most significant of which relates to the lack of procedural pain and discomfort. Recent studies have revealed excellent results regarding the detection of polyps exceeding 10 mm for both CT and MR colonography [6, 9, 16, 17]. In contrast to conventional colonoscopy, analysis is not limited to endoscopic viewing. Rather the 3D data sets can be scrolled in a traditional two-dimensional mode on a workstation in any desired plane. This type of multiplanar reformation analysis depicts the colon relative to the surrounding abdominal morphology, thereby facilitating the exact location of abnormalities. Lesions can be more accurately located as shown in this study in one patient suffering from a colonic carcinoma in the transverse colon near the splenic flexure.
Similar to colonoscopy, both MR and CT colonography do require prior bowel cleansing, necessitating the ingestion of large amounts of gastrointestinal lavage solutions [13, 17, 18]. Although different solutions with a variety of tastes are available, colonic cleansing is disliked by most patients and limits patient acceptance [10, 18]. In a randomized trial comparing flexible sigmoidoscopy and colonoscopy, 75% of subjects who underwent colonoscopy complained of symptoms related to bowel preparation ranging from "feeling unwell" to "inability to sleep" [19].
Fecal tagging obviates bowel cleansing. Reflecting the vast soft-tissue potential inherent to the MR experiment, the implementation of fecal tagging favors MR imaging over CT. Efforts concerning fecal tagging have also been undertaken in conjunction with CT colonography. The focus of this work has been to use barium to tag the stool, which otherwise can mask or simulate polyps. In contrast to MR colonography, the contrast medium is administered with the standard bowel preparation [20].
The principle of fecal tagging for MR colonography has been shown on the basis of a bright rectal enema distending the colonic lumen containing brightly tagged stool [11]. This effect was accomplished by administering a gadolinium-based enema and tagging the stool by means of an orally administered paramagnetic contrast agent. Cost considerations have limited the widespread clinical implementation of gadolinium-based fecal tagging. The amount required for oral tagging exceeds the amount generally administered IV. In addition to the gadolinium required to spike the rectal enema, more than 160 mL of a standard 0.5-mol/L preparation of a gadolinium-based agent is required.
The strategy presented in this study is based on a dark colonic lumen with darkened stool in conjunction with the enhancement of the colonic wall. The amount of gadolinium administered IV ranged between 26 and 36 mL (0.2 mmol/kg of body weight). Beyond the reduced cost, several advantages are inherent in the dark-lumen strategy. Pockets of residual air, which can be indistinguishable from polyps on bright-lumen MR colonography, blend into the darkened colonic lumen, thereby obviating collection of a second data set in the supine patient position. This advantage considerably reduces the data-acquisition time and halves the data interpretation efforts. Although the approach based on a bright colonic lumen only indirectly assesses the colonic wall, the proposed strategy is based on analysis of the colonic wall itself. Enhancement of colonic polyps has been described in conjunction with both CT and MR colonography [7, 21]. In this study, enhancement after the IV administration of an extracellular gadolinium-based contrast agent proved sufficient for complete analysis of the wall and easy detection of even small masses arising from the colonic wall. Thus, the colonic carcinomas were identified with the same ease as the 10- and 6-mm polyps. This form of direct colonic wall imaging promises also to be helpful in assessing other abnormal conditions affecting the bowel wall, such as inflammatory diseases. Furthermore, parenchymal organs contained in the field of view, such as the liver, are easily assessed for the presence of concomitant disease on the basis of the collected contrast-enhanced T1-weighted image sets.
For maximal enhancement of the colonic wall, gadobenate dimeglumine, a weakly albumin-binding agent that is known to result in augmented enhancement compared with other agents [22], was chosen. For optimal results, the agent was administered at a higher dose, usually used for MR angiography [23]. Furthermore, the 3D data acquisition was timed to coincide with the maximal contrast concentration in the interstitium of the colonic wall occurring at 75 sec after completion of the IV contrast administration.
The recommended low-fiber diet, the oral ingestion of barium sulfate, and the placement of the rectal tube did not adversely affect patient comfort. Similarly, the single-contrast enema is well tolerated if administered in conjunction with a spasmolytic agent. Beyond improving patient acceptance by obviating bowel cleansing, fecal tagging may actually enhance the diagnostic accuracy of colonography. Current CT and MR techniques have been shown to be limited by residual stool, which can simulate the presence of polyps [7, 24, 25]. By equilibrating the signal characteristics of stool with those of the enema, fecal material no longer appears as a filling defect in the colonic lumen and cannot be confused with a polyp.
Barium sulfate, the orally administered fecal tagging agent, is a well-known diagnostic contrast agent still in widespread use as the oral contrast agent for esophageal, gastric, and small-bowel radiography. Compared with gadolinium-based agents, it is far less expensive, is provided in various flavors, and has a most favorable safety profile. Anaphylactoid reactions or other adverse side effects are rare. The agent is not absorbed and mixes well with stool. Similarly, as long as contraindications to the rectal administration of barium sulfate, including the presence of toxic megacolon or colonic perforation, are observed [26], there are virtually no risks associated with the administration of barium sulfate as an enema. In fact, barium remains the agent of choice for both single- and double-contrast radiography of the colon. Thus, barium does appear to be the ideal oral-tagging and rectal-filling agent for examining the colon.
Clearly, the described strategy for colonic imaging without prior bowel cleansing will need to be validated in large patient cohorts before any clinical use. In particular, the fact that all polyps enhance after the IV administration of contrast agents in a manner similar to the colonic wall as in CT colonography [21] needs to be verified for MR colonography. Although the presented technique will require some refinements, barium-based MR colonography with fecal tagging fulfills most requirements to be established as a screening method for colorectal cancer. We are hopeful that the potential associated with this strategy will motivate others to join us in the quest to further develop and evaluate this technique.
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