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MR colonography: current status

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Page 1: MR colonography: current status

Eur Radiol (2006) 16: 1519–1526DOI 10.1007/s00330-006-0260-z GASTROINTESTINAL

Thomas C. Lauenstein

Received: 24 February 2006Revised: 14 March 2006Accepted: 16 March 2006Published online: 20 April 2006# Springer-Verlag 2006

MR colonography: current status

Abstract Magnetic resonance colo-nography (MRC) has gained accessinto clinical routine as a means for theassessment of the large bowel. Thereare widely accepted indications forMRC, especially in patients withincomplete conventional colonoscopy.Furthermore, virtual MRC is more andmore propagated as a screening tool,with advantages especially inherent tothe non-invasive character of thisprocedure and the lack of ionizingradiation exposition. Beyond a suffi-

ciently high diagnostic accuracy, out-standing patient acceptance is a majoradvantage of MRC as a diagnosticmodality. This review article describesindications, techniques and clinicaloutcome of current MRC approaches.Furthermore, the impact of fecal tag-ging concepts is discussed.

Keywords MR colonography .Colorectal cancer screening .Inflammatory bowel disease .Patient acceptance

Introduction

Colorectal cancer continues to be the third leading cause ofcancer-related mortality in industrialized countries, withover 50,000 deaths in 2005 [1]. The majority of colorectalcancers develop from benign lesions over a relatively longtime range of up to 10 years [2]. Due to the adenomatouspathogenesis of most colorectal cancers [3], screening forcolorectal polyps and subsequent polypectomy is a veryeffective approach for reducing the incidence of thismalignant tumor [4].

Dedicated screening guidelines have been establishedencompassing different diagnostic tools, such as fecaloccult blood testing, flexible sigmoidoscopy, colonoscopyand double barium enema examination. Among theseprocedures, optical colonoscopy is the most accuratemeans for examining the colon with high sensitivity andspecificity regarding the detection of precancerous polyps[5]. However, only moderate patient participation isobserved in screening programs, even if access tocolonoscopy was free [6, 7]. This is mainly related toprocedural pain coupled with the rigors of preparatorybowel cleansing [8–11]. Virtual colonography (VC) hasevolved during the last decade as a promising alternative to

optical endoscopy. This technique is based on the acqui-sition of either computed tomography (CT) or magneticresonance imaging (MRI) data sets. Due to the non-invasive character and the lack of procedural pain anddiscomfort, VC offers an imminent advantage overconventional colonoscopy. Furthermore, analysis is notlimited to the bowel itself. Rather, all surrounding abdom-inal structures can be assessed as well and lesions can bemore accurately located [12]. Eventually, the entire coloncan be depicted even in the presence of stenotic lesions orelongated bowel segments. In contrast, conventional colo-noscopy is incomplete in up to 26% of the cases [13, 14].

Virtual colonography is proven to be effective regardingthe detection of polyps exceeding 7 mm in size [15–22].Because of economical rationale and higher clinicalavailability of scanners, most approaches so far havefocused on CT colonoscopy (CTC). Despite promisingdiagnostic results in terms of diagnostic accuracy, thefuture of CTC as a screening method remains uncertain,because associated ionizing radiation raises the possibilityof even a public health concern [23–25]. Lifetimeattributable risk estimates for developing a radiation-induced malignant cancer in a screening population usingCT have been as high as one in 50 patients [25]. Thus, a

T. C. Lauenstein (*)Department of Radiology,The Emory Clinic,1365 Clifton Road, Building A,Suite AT-627,Atlanta, GA 30322, USAe-mail: [email protected].: +1-404-7783800Fax: +1-404-7783880

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compelling rationalization for pursuing MR colonography(MRC) is avoidance of risks associated with ionizingradiation exposure. In addition, intravenous MR contrastagents are coupled with a more favorable safety design thanCT contrast compounds since they are associated with farfewer anaphylactoid reactions and lack any nephrotoxicity[26, 27]. Current techniques of MRC, indications andclinical outcome are described in this article.

Indications of MRC

Screening programs have been shown to reduce theincidence of colorectal cancer by more than 80% [28, 29].MRI actually provides all properties necessary for asuccessful screening tool, including high patient acceptanceand good accuracy. Preliminary results of MRC as ascreening method are encouraging [30, 31]. One mayorproblem may relate to the inability of MR colonography todetect colorectal polyps <5 mm. On the one hand, thesignificance of this limitation is equivocal: these lesions arenot prone to malignant degeneration and remain stable overa time range of 3–5 years [32]. On the other hand, thesesmall polyps might become detectable with further techni-cal development: the implementation of parallel acquisitiontechniques (PAT) will help to increase spatial resolution andconsequently the detection rate of small lesions. However,flat adenomas are likely to remain elusive.

A proven indication for MRC is incomplete endoscopy(i.e., due to stenoses or elongated bowel segments).Hereby, virtual endoscopy can provide helpful additionalinformation [33–35]. Distending media used for MRC,namely water or gasiform substances, will pass the stenoticsegments and will allow for a sufficiently high conspicuityof the prestenotic structures. Thus, virtual colonography is

associated with significantly higher completion rates: onlya high-grade stenosis will prohibit the passage of water orair required for distending pre-stenotic segments (Fig. 1).Hartmann et al. [33] have assessed the concept of MRC in32 patients with incomplete previous optical colonoscopydue to high-grade stenoses (n=26), bowel elongation (n=5)and patient intolerance (n=1). All stenoses were correctlyidentified on the MR data sets. A total number of ninepolyps located in prestenotic bowel segments weredepicted. These findings were confirmed by subsequentsurgery and/or postoperative endoscopy. Only two smallpolyps (5 and 8 mm in size) were missed by MRC. Thisconcept was evaluated in another trial as well [35]. In 37patients presence of colorectal pathologies was assessed ona segmental basis. Conventional colonoscopy could notreach almost 50% of the potentially visible segments. Incontrast, only 4% of the bowel segments were notassessable on MRI data sets. All stenotic and post-stenoticlesions were correctly diagnosed by means of MRC.Furthermore, MR-based assessment of pre-stenotic seg-ments additionally revealed several pathologies notdepicted by conventional endoscopy. Five polyps, twomalignant tumors and inflammatory chances in fourpatients were depicted.

MRC also has been successfully applied in patients withinflammatory bowel disease [36–38; Fig. 2]. As for thedepiction of colorectal masses, endoscopy in conjunctionwith biopsy has been considered the “gold standard” for theassessment of inflammatory bowel diseases [39, 40]. Theability of MRI to detect and quantify inflammatory boweldisease has been assessed in several studies [41–43]. In atrial by Schreyer et al. [41] severe colonic inflammationwas depicted by MRC with high accuracy. However, subtleinflammatory changes mainly in patients with Crohn’sdisease were misdiagnosed in some cases. In another study,23 patients with suspected inflammatory bowel disease ofthe large bowel were examined by means of MRI and

Fig. 1 Contrast-enhanced T1-weighted image of a patient with highgrade inflammatory stenosis in the transverse colon (arrows). Pre-stenotic bowel segments were not assessable by optical colonoscopy.The rectal enema administered for MR imaging, however, passed thestenosis and enables an assessment of the right colonic flexure as wellas the ascending colon

Fig. 2 Contrast-enhanced T1-weighted data of a patient withCrohn’s disease. An active inflammatory process was seen in thetransverse colon with increased contrast enhancement of the bowelwall and lumen narrowing

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subsequent optical colonoscopy [43]. Inflammatory chang-es were quantified according to several criteria, includingbowel wall thickness, bowel wall contrast enhancement,loss of haustral folds and presence of perifocal lymphnodes. More than 90% of the colonic segments withinflammatory bowel disease changes were correctlyidentified on the MR images. Again, some mildly inflamedsegments were not described as such. Finally, MRI has alsobeen proposed for the assessment of diverticulitis [44, 45].

The depiction of inflammatory processes is not limited tothe bowel wall itself. Moreover, the presence of extramuralchanges, including fistulae, conglomerate tumors andabscesses can often be found, while these extra-intestinalfindings are not even suspected by endoscopy [38].

Data acquisition and interpretation

Prior to the MR examination a bowel preparation has to beperformed. Different strategies can be pursued: eitherpatients have to undergo bowel cleansing in an identicalway to that required for conventional colonoscopy or so-called “fecal tagging” approaches can be applied. The latterwill be described and discussed later on. When a bowelpurgation protocol has been used, MRC should beperformed in the morning to avoid unnecessary patientdiscomfort. General contraindications for MRI, such aspresence of metallic implants or severe claustrophobia,should be excluded. Hip prostheses may lead to significantartifacts in the pelvis, thereby impeding a reliable analysisof the rectum and sigmoid colon. These patients should beexcluded as well. The administration of sedative oranalgesics, which is often performed at optical colonosco-py, is usually not required. Another prerequisite for MRC isrelated to sufficient bowel distension. Most colonicsegments are physiologically collapsed and may mimicbowel wall thickening. Thus, they cannot be assessedproperly. The administration of distending media (usuallywater solutions) via a rectal catheter allows for a reliabledistension of all colonic segments. To permit a gooddepiction of the bowel wall, a high contrast between the

Fig. 3 For MRC the patient is scanned in prone position. Acombination of two flex surface array coils is placed on the patient’sback. The rectal enema consisting of warm water is administered viaan enema bag using hydrostatic pressure

Fig. 4 Bright-lumen contrast mechanism using water as a rectalenema in conjunction with TrueFISP data collection. The bowel wallimpresses as dark filling defects within the bright colonic lumen.This type of imaging has been proven helpful in patients withinflammatory bowel disease

Fig. 5 Dark-lumen contrast mechanism of MRC. T1-weighted datacollection after the i.v. administration of gadolinium results in anenhancing bright bowel wall, which can be easily distinguished fromthe dark colonic lumen

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bowel lumen and wall is necessary. Contrast mechanismshereby depend on the MR sequences in question and theadministration of (intravenous and/or rectal) contrastagents.

Since MR data acquisition is mainly performed underbreath-hold conditions, the use of an appropriate hardwaresystem (i.e., the use of a 1.5-T scanner equipped withstrong gradient systems) is necessary. Initial results haveshown MRC to also be feasible at 3 T [46]. The patient

should be examined in the prone position. To ensure ahomogenous and complete signal reception, the use of twosurface array coils is recommended (Fig. 3). The admin-istration of spasmolytic agents (e.g., scopolamine orglucagon), which is controversially discussed for CTcolonoscopy, has a proven benefit for MR colonography:bowel spasms can be obviated and motion artifacts aresignificantly reduced. Furthermore, the administration ofsmasmolytic agents will ensure an optimal bowel disten-sion. The colon can be filled with approximately 2,500 mlof warm tap water via a rectal tube or a thin flexiblecatheter. The filling process can be monitored by anacquisition of non-slice select sequences providing anupdate image every 2–3 s.

Different sequence types should be acquired. After thecollection of a localizer sequence, we propose the acqui-sition of T2-weighted single-shot sequences (e.g., HASTE)with fat suppression and/or fast imaging with steady stateprecession sequences (TrueFISP, Balanced Fast Field Echoor FIESTA) in axial and/or coronal plane. The coloniclumen filled with water shows a high signal on theseimages, whereas the colonic wall and lesions arising from itimpress as dark filling defects (Fig. 4). Subsequently, T1-weighted MRI should be performed in conjunction withand without intravenous administration of gadolinium. Afirst pre-contrast T1-weighted 3D gradient-echo data set inthe coronal plane should be repeated approximately 75 safter i.v. injection of paramagnetic contrast (Fig. 5). Dataacquisition can be completed with a T1-weighted 2DFLASH sequence in the axial plane allowing for theassessment of the adjacent abdominal organs in high imagequality (Fig. 6). Eventually, the enema bag is placed on thefloor for draining the water and the patient is removed fromthe scanner.

For interpretation purposes, all data sets should betransferred to a post-processing workstation. Three-dimen-sional data sets should be evaluated using a multiplanarreformation (MPR) mode. Thus, the colonic wall can beassessed in all three orthogonal planes. As for the diagnosisof colorectal masses, a careful comparison between pre-and post-contrast T1-weighted scans is mandatory. Contrastenhancement value should be determined by measuringsignal intensities of lesions in both scans. This allows for an

Fig. 6 The post-contrast T1-weighted images allow for an accuratesimultaneous assessment of extraintestinal organs, including liver,spleen (a), kidneys and pancreas (b)

Fig. 7a–c Patient with a 1-cmsessile colonic polyp. Compar-ing the pre- (a) and post-contrast(b) T1-weighted images, a con-siderable enhancement can bedetermined. c The lesion im-presses as a dark filling defecton T2-weighted imaging

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excellent differentiation between true colorectal masses andresidual stool particles. While colorectal lesions alwaysstrongly enhance (Fig. 7), residual stool never shows anycontrast enhancement (Fig. 8). The analysis of the T2-weighted scans will provide helpful information regardinginflammation processes shown as edema on fat suppressedimages or pericolic stranding on non-suppressed images.Steady state precession sequences can be especially usefuldue to their relative motion insensitivity. Furthermore, thissequence type may be superior in certain cases because ofhigh contrast-to-noise ratios between the bowel wall andlumen. However, it may be difficult to distinguish betweenpolyps and residual feces without T1-weighted data.

Different software tools are commercially availablewhich display 3D source data as a virtual endoscopic fly-through (Fig. 9). If possible, 3D data should be additionallyassessed based on these virtual endoscopic renderings,which has been shown to improve the depiction of small

lesions in particular. Besides, the 3D depth perceptionenables the radiologist to assess haustral fold morphologymore reliably and haustra can be differentiated fromcolorectal masses more exactly. It is important to performa fly-through both in an antegrade as well as retrogradedirection. This reduces the risk of missing relevant lesions,since both sides of haustral folds are depicted. Automaticpathfinders, which are already widely used for CTcolonoscopy, might be implemented in the future, therebyfacilitating the diagnostic analysis. Another substantialhelp may be the usage of color-encoding software for thedetection of colorectal masses or inflammatory lesions, aspropagated by Schreyer et al. [41].

VC studies are not limited to endoscopic viewing.Simultaneous information is collected for all abdominalorgans within the field of view. Especially in patients withcolorectal malignancy, imaging of the liver to excludehepatic metastases is of major interest. The combination ofpre- and post-contrast T1-weighted as well as T2-weightedimages has been shown to be most accurate for thedepiction and characterization of hepatic lesions [47]. Inaddition, further unsuspected illness can be detected,including other malignant tumours, e.g., prostate or renalcell cancer, bone or lymph node metastases or vasculardisease [48].

Diagnostic accuracy of MRC

In a recent trial, MRC has been evaluated regarding thedetection rate of colorectal masses [22]. One hundredpatients scheduled for optical colonoscopy because ofvarious clinical indications were studied. A standard bowelcleansing protocol was performed before the examination.MR imaging was mainly based on the acquisition of pre-and post-gadolinium T1-weighted data and was followedby optical colonoscopy on the same day. In six patientsoptical endoscopy was incomplete and two patients

Fig. 8 Residual stool particles may mimic colorectal lesions oncontrast-enhanced T1-weighted imaging (a) and T2-weightedimaging (b). However, the evaluation of pre-contrast T1-weighteddata reveals a high signal intensity of that area before contrastadministration (arrow) and no subsequent contrast enhancement canbe found. Thus, a colorectal polyp can be definitely excluded

Fig. 9 The application of dedicated software systems allows for thedisplay of 3D data as virtual endoscopic views, which has beenshown to be helpful for a more accurate depiction of colorectallesions

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abandoned MRC because of claustrophobia. A totalnumber of 107 colorectal masses were depicted by meansof endoscopy. On a per patient analysis, all-over sensitivityof MRC for the detection of colorectal masses was 90%and specificity amounted to 96%. On a per polyp analysis,sensitivity of MRC amounted to 100% for polyps largerthan 10 mm and 84% for polyps between 6 and 9 mm indiameter. Similar findings were reported by Ajaj et al. [48].One hundred and twenty-two subjects of a high riskpopulation underwent both MRC and subsequent conven-tional endoscopy. While none of the lesions smaller than5 mm in size could be detected by MRC, all polyps>10 mm, as well as nine carcinomas, were correctlydiagnosed. Sixteen of 18 lesions between 5 and 10 mmwere found. On a per polyp basis, sensitivity and speci-ficity for the detection of lesions >5 mm was determined tobe 93% and 100%, respectively.

Most studies evaluating MRC were performed so farwithin high-risk cohorts. There is only a small amount ofdata about accuracy of MRC as a screening tool. Kuehle etal. [31] reported about a trial encompassing over 300screening patients older than 50 years without any historyof previous bowel disturbances. They underwent MRC andconventional colonoscopy within 4 weeks. MR data wereanalysed concerning the presence of colorectal masses andwere compared with endoscopy serving as the goldstandard. The overall detection rate for adenomatouspolyps >5 mm only amounted to 74%, while polyps>10 mm were depicted with a sensitivity of 93%. Overallspecificity of MRC for the detection of colorectal lesionswas 93% in this trial. Again, the discussion remains aboutthe impact and importance of the diagnosis of small polyps.

Patient acceptance

Virtual MRC has still required bowel cleansing in a mannersimilar to colonoscopy, because stool can mimic colonic

masses. However, 75% of patients undergoing bowelpreparation complain about symptoms ranging from“feeling unwell” to “inability to sleep” [49]. Thus, patientacceptance is negatively impacted [10, 11]. If bowelcleansing was eliminated, an even higher patient accep-tance of MRC could be assured. “Fecal tagging” is such aconcept to avoid bowel cleansing. Based on the ingestionof contrast compounds to regular meals prior to theexamination, signal intensity of fecal material is modifiedand adapted to the signal properties of the rectal enema.Hence, fecal material becomes “virtually invisible”(Fig. 10).

Highly concentrated barium sulfate has been used forfecal tagging in several volunteers and patient studiesproviding diagnostic image quality [50–52]. In a recenttrial, however, it could be demonstrated that ingestion of(100%) barium was regarded almost as unpleasant asbowel purgation due to viscosity and taste [53]. Thus, othertagging substances should be taken into account [31, 54].These compounds need to fulfil several requirements: theyshould not be reabsorbed in the GI tract, should mix wellwith foodstuff and stool, must alter signal characteristicsadequately and—last but not least—must be easy to beingested for the patient. A new tagging method is based ona solution containing 5% gastrografin, 1% barium and0.2% locust bean gum. Two hundred and eighty-fourasymptomatic patients have been evaluated with thisapproach (own unpublished data). The tagging solutionwas ingested with every main meal starting 2 days beforethe MR examination. MRC was performed on a 1.5-T MRsystem (Magnetom Sonata, Siemens Medical Solutions,Erlangen, Germany) in conjunction with a rectal enemaconsisting of warm tap water. Optical colonoscopy (OC)was performed within the following 4 weeks after MRcolonography. For colonoscopy patients underwent bowelpurgation with a polyethylene glycol solution and receivedboth sedatives and analgetics prior to the examination.Each 24 h following both examinations, patient acceptance

Fig. 10a, b Patient undergoingMRC with fecal tagging/withoutbowel cleansing. a TrueFISPimaging reveals presence of re-sidual stool in the transversecolon (arrows). b Due to theprevious administration of tag-ging agents, the signal intensityof fecal material is low on T1-weighted imaging and the stoolbecomes virtual invisible

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was assessed based on a standardized questionnaire.Specific aspects of each modality were evaluated using aten-point scale. In addition, patients were asked whichexaminations they would choose for future screeningprocedures. Patients rated the ingestion of the polyethyleneglycol electrolyte solution significantly more unpleasant(mean value: 4.8) compared with the ingestion of thetagging agent for MRC (mean value: 3.4). The mostunpleasant part of the MRC was the placement of the rectaltube and administration of water enema. Slightly morepatients preferred MRC as a future examination (46% vs

43%). Independently from the procedure itself, there wasanother aspect in favour of MRC: time-consumption willalso have a direct influence on patient preferences forscreening tools. After optical endoscopy, patients oftenneed to be monitored for a certain period, whichconsiderably extends the overall examination time. Dueto the high diagnostic accuracy and the possibility ofsimultaneous polypectomy, OC will certainly keep onplaying an important role as a diagnostic tool for the largebowel, anyway. For patients unwilling to undergo endos-copy, however, MRC can be a well accepted alternative.

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