First published online February 28, 2007
British Journal of Radiology (2007) 80, 235-241
© 2007 British Institute of Radiology
doi: 10.1259/bjr/83959666
Prospective study on bright lumen magnetic resonance colonography in comparison with conventional colonoscopy
B Saar, MD
1
A Meining, MD
2
A Beer, MD
3
M Settles, SC, PhD
3
H Helmberger, MD
4
E Frimberger, MD
2
E J Rummeny, MD
3 and
T Rösch, MD
5
1 Department of Diagnostic, Interventional and Pediatric Radiology, University Hospital of Berne, Inselspital, Switzerland, 2 Department of Internal Medicine II, Technische Universitaet of Munich, Germany, 3 Department of Radiology, Technische Universitaet of Munich, Germany, 4 Department of Radiology and Nuclear Medicine, Hospital Dritter Orden, Munich, Germany, 5 Department of Medicine, Division of Hepatology and Gastroenterology, Charité Medical Center, Virchow Hospital, Medical School of Berlin, Berlin, Germany
Correspondence: Dr Bettina Saar, Department of Diagnostic, Interventional and Pediatric Radiology, University Hospital of Berne, Inselspital, CH-3010 Berne, Switzerland. E-mail: bettina.saar{at}insel.ch
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Abstract
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The aim of this prospective trial was to evaluate sensitivity and specificity of bright lumen magnetic resonance colonography (MRC) in comparison with conventional colonoscopy (CC). A total of 120 consecutive patients with clinical indications for CC were prospectively examined using MRC (1.5 Tesla) which was then followed by CC. Prior to MRC, the cleansed colon was filled with a gadolinium–water solution. A 3D GRE sequence was performed with the patient in the prone and supine position, each acquired during one breathhold period. After division of the colon into five segments, interactive data analysis was carried out using three-dimensional post-processing, including a virtual intraluminal view. The results of CC served as a reference standard. In all patients MRC was performed successfully and no complications occurred. Image quality was diagnostic in 92% (574/620 colonic segments). On a per-patient basis, the results of MRC were as follows: sensitivity 84% (95% CI 71.7–92.3%), specificity 97% (95% CI 89.0–99.6%). Five flat adenomas and 6/16 small polyps (
5 mm) were not identified by MRC. MRC offers high sensitivity and excellent specificity rates in patients with clinical indications for CC. Improved MRC techniques are needed to detect small polyps and flat adenomas.
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Introduction
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Colorectal neoplasia is the third most commonly diagnosed cancer and the second leading cause of death due to malignancies in western industrial countries [1]. The high incidence – and the high mortality rates despite the availability of curative treatment when the disease is detected early – have led to recommendations to implement screening programmes, including faecal occult blood testing (FOBT), or sigmoidoscopy together with FOBT, and, in some countries as well as with barium enema or colonoscopy [2–6].
Despite its many advantages – including the opportunity to carry out biopsy and polypectomy during the same examination session – colonoscopy still has a low level of acceptance, with colon cleansing preparation and pain during the examination being the main factors leading to non-compliance among patients. The search for alternative methods has led to the development of advanced cross-sectional imaging modalities using CT scanning and MRI. These rapidly evolving techniques are also summarized as "virtual colonography" [7, 8]. So far, the method of magnetic resonance colonography (MRC) has shown high accuracy, but mostly in small patient groups [9–11].
The aim of this prospective trial was to evaluate the sensitivity and specificity of bright lumen MRC in comparison with conventional colonoscopy (CC) in consecutive patients with clinical indications for CC.
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Patients and methods
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Patients
The prospective study received trial protocol approval from the institutional ethics committee. Within a 24 month period a total of 126 consecutive patients scheduled for colonoscopy were prospectively asked whether they would be willing to undergo MRC on the same day as CC was planned. Inclusion criteria for MRC were indications for a CC (non-specific abdominal complaints a positive FOBT, follow up after polypectomy) and an age of over 18 years. Exclusion criteria were contraindications for MRI and pregnancy. From 126 patients asked for participation, six were excluded due to MRI contraindications [pacemaker (n = 4), history of cerebral aneurysm clipping (n = 1), severe claustrophobia (n = 1)]. If more than one patient was scheduled for a CC on the same day the first patient who agreed was "the study patient" on a "first to consent basis". After written informed consent had been obtained, all of the patients underwent standard lavage preparation for CC with a polyethylene electrolyte solution (Oralav®, Braun, Germany, 4–6 l per os). MRC was performed 1–3 h prior to CC.
Bright lumen magnetic resonance colonography
The patients were placed in the left lateral decubitus position on the MR table for insertion of a routine flexible enema catheter. The colon was filled via a routine enema bag (Guerbet Enema Bag, Guerbet, Germany) under MRI guidance in the prone position. The enema, with a volume of 1.5–2.5 l, consisted of a water–gadolinium diethylenetriamine pentaacetic acid solution (Gd-DTPA) (Magnevist®, Schering, Germany) at a concentration of 1:100. Peristalsis was reduced using butylscopolamine (Buscopan®). In patients with a body weight of 60 kg or lower 20 mg of butylscopolamine was administered (> 60 kg body weight 40 mg of butylscopolamine). The MR table was protected by absorbent pads. For MRC a 1.5 Tesla system (ACS NT, Intera; Philips, Germany) was used. To cover the whole abdominal volume, a phased-array body coil oriented in the craniocaudal direction was used (maximum field of view 500 mmx500 mm). The filling phase was observed using a single thick-slice radiofrequency (RF) spoiled gradient echo sequence at a rate of one image per second. After the contrast enema had distended the whole colon, a three-dimensional RF spoiled gradient echo sequence was acquired to delineate the entire colon in the coronal direction (Table 1
). With these parameters, it was possible to obtain a package of 120–130 contiguous sections to image the entire colon during one single breathhold period (20–23 s). After data acquisition in the prone position, a second data set was sampled in the supine position to delineate regions of residually trapped air. Additional enema material was administered (to avoid partial colon collapse) until the patient started to complain about the inconvenience of abdominal pressure. For analysis and lesion matching, the colon was divided into five segments in both MRC and colonoscopy (caecum and ascending colon; transverse colon; descending colon; sigmoid colon; rectum).
Conventional colonoscopy (CC)
CC was conducted in the standard mode with conventional video colonoscopes (Olympus CF-130 L and CF-140 L; Olympus Europe, Hamburg, Germany). When necessary, sedation was administered by intravenous application of midazolam (Dormicum®; Roche, Basel, Switzerland) and/or propofol (Propofol®; Fresenius, Germany). During withdrawal of the instrument after the caecum had been reached, careful inspection of the entire circumference of the various colonic segments was carried out to ensure that small and flat polyps were not missed. Findings were localized in relation to the instrument's length on withdrawal (with the colonoscope in a straightened position), in the right colon according to the distance from the ileocaecal valve; and, whenever possible, with transillumination. Polyps and masses were measured on the basis of histopathological analysis of the polypectomy specimens, or during endoscopy if polypectomy was not performed, with a biopsy forceps being used for reference. The withdrawal time was between 10 min and 15 min (not including biopsy or polypectomy procedures). All polyps were either removed by conventional polypectomy or biopsied. Only experienced colonoscopists (> 1000 colonoscopies) performed the colonoscopies during the study period.
Post-processing/MRI data analysis
First, image quality of the source images was analysed and scored from 1 to 5 (1 excellent, 2 good, 3 fair, 4 poor, 5 not diagnostic). The score involved colon distension, homogeneity of the enema as well as motion or faecal artefacts. MR data analysis was performed in consensus reading for lesion detection as well as for quality scoring by two experienced board-certified radiologists. The radiologists had performed more than 50 MRCs prior to this study. The observers were blinded to the patient's history, clinical data and symptoms.
The obtained images were transferred to a workstation (Ultrasparc 30/60; Sun, Palo Alto, CA). The source images, the multiplanar reconstructions (MPR), the maximum intensity projections (MIP), as well as the virtual views with a supplementary cine mode were all reviewed to find a diagnosis. Post-processing was carried out interactively using a commercially available software package (EasyVision version 4.3; Philips, Hamburg, Germany). Subsequently, three-dimensional imaging was performed by using perspective volume rendering, with a translucency of 0% and a viewing angle of 120° to compromise between image distortion and surface visibility. After manual definition of a path through the bowel (from rectum to caecum) the flythrough was computed. The colon was examined in both antegrade and retrograde directions by using 5 mm increments. On the background screen, reformatted two-dimensional images in three planes were displayed so that whenever necessary, two- and three-dimensional images could be compared. The data set acquired in the prone position was most important for analysis, but in areas with trapped air not covered by the enema, the supine position was essential. Polyps or masses were classified as wall adherent filling defects with low signal intensity (Figure 1). The lesion size was measured by an integrated software tool. Distances during instrument withdrawal of CC were used to estimate the lesion location in the corresponding colon segment of MRC. Lesion matching of MRC and CC was performed by using the reports of CC as a standard of reference. For a true positive result, the lesion identified at MRC had to have been matched according to location, size and morphologic features to a lesion found at CC. In the per-patient evaluation, a result was considered to be a true positive finding only when at least one polyp identified at MRC was matched to a lesion seen at CC. All other results were considered to be false positive findings.
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Figure 1. (a) Source image of MRC with a pedunculated polyp of the sigmoid colon (white arrow). (b) Displays the same polyp of 8 mm in size in the virtual endoluminal view (black arrow), polyp and size confirmed at CC.
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Statistical analysis was performed using a contingency table and the Fischer's exact test (GraphPad InStat, version 3.01, GraphPad Software, San Diego, CA). Sensitivity, specificity, positive and negative predictive values (PPV, NPV) were calculated with corresponding 95% confidence intervals (95% CI). We did not address per polyp specificity because of uncertainty regarding the denominator for this group [12].
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Results
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Feasibility and complications
120 patients (56 men, 64 women; median age 69 years, range 22–87 years) underwent MRC successfully. The procedure was well tolerated by all patients and no complications occurred. No relevant spillage contaminated the MRI scanner. Sedatives or analgesics were not necessary for MRC. Patient room time in the MR suite was 15–35 min, mean time was 21.5 min.
Image quality
All acquired data sets were reviewed for diagnostic purposes. In three cases the prone and in two cases the supine data set was acquired twice due to initial misunderstanding of the breathhold request. The analysis in these cases was performed using the second data set, since the first was inadequate due to severe motion artefacts. Image quality was scored and listed in Table 2. An excellent or at least fair image quality was found in 92% (574/620) of the colon segments. Images from the right colon were more often found to be of reduced quality than those from the left colon. The time required to analyse the MRC data ranged from 13.5 min to 48 min, with a mean of 23.5 min.
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Table 2. Quality ranking of the different colon segments. Score: 1 excellent, 2 good, 3 fair, 4 poor, 5 not diagnostic
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Sensitivity and specificity of MRC
The mean numbers of polyps per patient was 2 (range 0–14). The polyp size ranged from 0.2 cm to 3 cm. Additionally, in eight patients stenosing masses were found [seven colon carcinoma (Figure 2), one severe ulcerative colitis].
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Figure 2. High grade stenosis due to colon cancer of the left flexure in the MIP. The entire colon was delineated including some diverticula of the descending and sigmoid colon.
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On a per-patient basis, the results of MRC were as follows: sensitivity 84 % (n = 47/56; 95% CI 71.7–92.3%), specificity 97% (n = 62/64; 95% CI 89.0–99.6%); positive predictive value 96% (95% CI 86.04–99.5%); negative predictive value 87% (95% CI 77.3–94.0%). In two patients MRC revealed two polyps each ranked false positive for MRC. These two findings appeared as wall adjacent filling defects in the source images and in the MPR. One was delineated in the transverse colon (6 mm in diameter), the other in the descending colon (7 mm in diameter). In the virtual endoluminal view both lesions showed a polyp like configurated shape. Although the lesions fulfilled the criteria of a positive finding at MRC, they were not confirmed by CC. Thus, they were ranked as false positives for MRC. However, no false positive polyps were identified due to mismatching.
On a per-polyp basis, MRC showed a sensitivity of 81% (n = 83 of 103 polyps; 95% CI 70.2–91.4%). Regarding only lesions of more than 5 mm in diameter, MRC visualized 72 of the 82 polyps (sensitivity 88%; 95% CI 77.1–94.7%).
The polyp detection rate depending on polyp size is shown in Figure 3. Five flat adenomas, found by CC, were missed by MRC. Even in retrospect these flat lesions were not found. MRC found 10 of 16 (63%) polyps with a diameter of 5 mm or less, 44 of 51 (86%) polyps 5–10 mm in size, and 29 of 31 (94%) polyps more than 10 mm in size (Figure 4). Additionally MRC correctly identified tumour stenosis in all eight patients.
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Figure 4. Comparison of the conventional colonoscopic view(a) and the virtual view of a MRC data set (b) showing a sessile adenoma of 12 mm in size, polyp and size confirmed at CC.
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Results of conventional colonoscopy
In 114 of the 120 patients (95%), conventional colonoscopy visualized the entire colon. In four of the eight patients with stenoses, the obstruction could not be traversed endoscopically. In one patient with long-standing ulcerative colitis, the sigmoid colon showed a high grade stenosis, which was not traversable even with a paediatric colonoscope. After resection only inflammation was found on histopathology. No malignancy was detected. The other three patients had occlusive carcinomas. One had a synchronous carcinoma in the descending colon. The other two patients were suffering from occlusive carcinomas of the sigmoid or descending colon, respectively. One also had multiple polyps of different sizes. The results of virtual colonoscopy were confirmed by surgery in these four cases.
In two of the 120 patients (1.7%) a colon perforation occurred during CC. One patient with an infiltrating ovarian cancer experienced perforation during passage through an angulated and fixed sigmoid (the patient underwent surgery). The other patient with arterial bleeding after polypectomy (of a 3 cm sessile adenoma) was endoscopically coagulated. The subsequent minor perforation (free air) was managed conservatively. For CC, sedation was administered in 93 of the 120 patients (78%). In 64 patients CC showed no pathological findings.
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Discussion
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Colorectal cancer represents a major public health problem, especially in developed countries. MRC is a rapidly evolving technique with the potential to improve early diagnosis of colon cancer and its precursors. The purpose of this prospective study was to assess the value of MRC to detect colorectal polyps and masses in routine clinical practice. Therefore 120 consecutive patients with clinical indications for CC were prospectively enrolled and investigated with MRC and CC. Conventional colonoscopy served as a reference standard. The main goal of this study was to determine the sensitivity and specificity rates of MRC in daily routine use, e.g. none of the consecutive patients was excluded from data analysis for any reason. Although CC is not considered as a perfect test for detection of colorectal lesions, as reported in a study of a back-to-back colonoscopy showing a high miss rate of adenomas, it must be considered as the standard of reference [13].
A major advantage of MRC is its minimal invasiveness and its safety. In our study no severe complications were observed and none of the patients needed supporting drugs. In contrast, in 78% of the patients undergoing CC analgetics, sedatives or both were administered. This is supported by the study of Taylor et al, which included 186 patients. The authors found that although patients were most satisfied with colonoscopy, they reported more pain during both colonoscopy and sigmoidoscopy than during CT colonography, and they also found CT more acceptable. In patients expressing a preference, CT colonography was the preferred follow up investigation [14].
Although the procedure of MRC is minimally invasive, currently, a cleansed colon is a prerequisite for the procedure. In studies dealing with patient acceptance of virtual colonoscopy, the most inconvenient part is colon cleansing [15]. A procedure without the need for strong bowel preparation would be desirable. First feasibility studies showed that only mild preparation is possible for MRC [16, 17]. Recently published results underscore the necessity of further efforts focusing on this topic [18].
In our patient group CC failed in 5% and perforations were observed in 1.7%. In a large, population-based study the incidence of perforation from colonoscopy was 0.19% and from sigmoidoscopy was 0.09% [19]. A recently published study by Ajaj and colleagues focused on the indication of incomplete colonoscopy and reported that MRC was diagnostic in 35 of 37 patients [20]. This is supported by our data since bright lumen MRC delineated the entire colon in all patients with high grade stenosis as well as with incomplete colonoscopies. All those patients underwent surgery revealing three carcinoma and one stenosis due to chronic ulcerative colitis.
In a recent study Luboldt et al investigated 132 patients with MRC and reported high sensitivity (93%) and specificity (99%) rates for large lesions [21]. In contrast to our study, patients with small lesions (5 mm), flat adenomas and poor image quality due to motion artefacts were excluded from data analysis. The study design with inclusion of consecutive patients without exclusion of difficult diagnostic conditions (small polyps, flat adenomas, artefacts) may explain why a reduced overall sensitivity of 84% was found in the current study. When only large lesions with a size of 10 mm or more were analysed, our per-polyp sensitivity increased to 94%. It is important to note that even in this demanding patient group our overall specificity was 97%. In addition, the availability of the MR scanner in our clinical setting did not allow for repeat MR examination after bowel cleansing in those patients who were found to have multiple artefacts due to retained faecal material.
The current study clearly indicates that MRC has limitations in the detection of flat adenomas and small polyps (diameter 5 mm) with the latter showing a sensitivity of 62%. Additionally, air bubbles or residual stool adjacent to the colon wall may mimic polyps, being a reason for false positive results. Although small lesions are still a matter of debate, this limitation affects the procedure's usability [22, 23]. However, this may be overcome by new MRC techniques. The recently introduced technique of dark lumen MRC utilizes tap water for colon distension and intravenous contrast media for direct visualization of the colon wall [24]. A direct assessment on the assumed colonic lesions may improve differentiation of artefacts from solid lesions, but even with this technique small and particuliary flat lesions were often overlooked [25].
The bright lumen technique requires a gadolinium-enhanced fluid enema to provide a sufficient contrast between colonic lumen, colon wall and adjacent lesions. The high contrast is a prerequisite for computing the virtual endoluminal view. Albeit in the study group the enema was well tolerated and no severe complications occurred, the fluid enema requires a normal sphincter control. This might be a limitation of the procedure for patients with any problems of incontinence or mental limitations. Although similar to water regarding MR signal properties on T1 weighted (T1W) images, the fear of susceptibility artefacts rendered the use of air or other gases less applicable for MRC. The practicability of administering room air for bowel distension in MRC was first evaluated by Morrin et al [26]. Seven patients underwent MRC after the insufflation of air. T2-weighted half-Fourier single-shot turbo spin echo (HASTE) images were acquired. Due to susceptibility artefacts image quality was suboptimal in five of seven examinations, a 15 mm polyp was correctly detected, but a 6 mm polyp was missed. Even more promising results were found by Ajaj et al [27]. They compared air with water for colon distension in MRC in 50 patients. Separately, air and water in 25 patients each was used for colon distension. After administering intravenous contrast media a three-dimensional T1W sequence with high spatial resolution in all three planes was acquired (dark lumen MRC). In this study MRC using room air for bowel distension was considered feasible. Comparable results in the air-distended and the water-distended group were observed in detection of colorectal lesions. The assessment of the colonic wall in an air-distended colon on 3D T1W GRE images was not corrupted by susceptibility artefacts. Air and water were similarly well tolerated as colonic distending agents. In this context, the authors pointed out that the use of ultrashort submillisecond echo times is predicated upon the availability of a scanner with high performance gradient systems.
Further technical developments are under investigation and may improve image quality. A main requirement of MRC is an adequate signal-to-noise-ratio in very short acquisition times. Further developments like parallel acquisition techniques (PAT) or higher field strength may solve this issue and minimize the reported limitations. In a recently published study, the authors found that even with a PAT factor up to six, 2D PAT leads to a moderate contrast-to-noise-ratio loss [28]. For MRC, distinct shorter acquisition times can be achieved with identical resolution.
In conclusion MRC can be considered a minimally invasive and safe procedure. This prospective trial showed the high potential of MRC in detecting colorectal lesions in patients with clinical indications for CC that can be compared with the results of CC. However, improved MRC techniques are needed to detect small polyps and flat adenomas.
Received for publication May 31, 2006.
Revision received August 2, 2006.
Accepted for publication August 15, 2006.
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Abstract
Introduction
