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Eur Radiol (2008) 18: 429–437 DOI 10.1007/s00330-007-0764-1 Andrik J. Aschoff Andrea S. Ernst Hans-Juergen Brambs Markus S. Juchems Received: 8 February 2007 Revised: 25 July 2007 Accepted: 24 August 2007 Published online: 25 September 2007 # European Society of Radiology 2007 A. J. Aschoff (*) . A. S. Ernst . H.-J. Brambs . M. S. Juchems Diagnostic and Interventional Radiology, University Hospitals of Ulm, Steinhoevelstr. 9, 89070 Ulm, Germany e-mail: [email protected] Tel.: +40-731-50061003 Fax: +40-731-50061005 GASTRO INTESTINAL CT colonography: an update Abstract Computed tomographic (CT) colonography (CTC)—also known as “virtual colonoscopy”—was first described more than a decade ago. As advancements in scanner technology and three-dimensional (3D) postprocessing helped develop this method to mature into a potential option in screening for colorectal cancer, the fundamentals of the examination remained the same. It is a minimally invasive, CT-based procedure that simulates conventional colonoscopy using 2D and 3D com- Introduction “Virtual colonoscopy” was first described by David Vining more than a decade ago [1]. Its potential was quickly evident and it developed from a research tool to a potential screening method for colorectal cancer. The basic approach of acquiring a three-dimensional (3D) dataset after colon distension in combination with 2D/3D postprocessing has not changed, though. The preferred terminology for this method should be computed tomographic colonography (CTC) [2]. Epidemiology Colorectal cancer is one of the most common causes for cancer deaths. With an estimated number of 106,680 new cases in 2006 and 55,170 estimated deaths in the same year, it is the third most frequent cancer found among men and women in the United States and the third most common cause of death among cancers [3]. A variety of predisposing factors for developing colorectal cancer are known. These include: a first-degree puterized reconstructions. The primary aim of CTC is the detection of colorectal polyps and carcinomas. However, studies reveal a wide performance variety in regard to polyp detection, especially for smaller polyps. This article reviews the available literature, discusses established indications as well as open issues and highlights potential future developments of CTC. Keywords CT colonography . Screening . Colon cancer relative in whom colon cancer or a large adenomatous polyp was diagnosed before the age of 60 years; inflammatory bowel disease; a history of familial adenomatous polyposis or hereditary nonpolyposis; colorectal cancer syndromes and prior adenomatous polyps or colon cancers. In developing colorectal cancer, the colonic polyps—in particular the adenomatous polyps—play a key role. Through a genetic mutation, normal colon cells may transform into hyperproliverative epithelium, adenomas and finally into colorectal cancer [4]. Colorectal polyps can be removed endoscopically (polypectomy), and colonoscopic polypectomy results in a lower than expected incidence of colorectal cancer [5] (Fig. 1). The symptoms of colorectal cancer are often uncharacteristic (obstipation, diffuse pain, loss of weight) and may delay the final diagnosis. Therefore tests are desired to detect colon cancer in its early stages or—even better—its precursors, the adenomatous polyps. Various screening tests for colorectal cancer are available—fecal occult blood test (FOBT), sigmoidoscopy and colonoscopy are the most important ones. Each of these methods has its limitations. FOBT is a very specific but not sensitive test [6] and sigmoidoscopy does not assess the 430 single breath hold without respiration artifacts is an advantage that is particularly beneficial for CTC. Patient preparation Fig. 1 a Normal colon as seen in optical colonoscopy and b corresponding endoluminal CTC reconstruction whole colon. Nevertheless, even sigmoidoscopy leads to a decrease of mortality [7], although up to 52% of the colorectal polyps are located proximal to the rectosigmoid [8] and significant polyps can be overseen if located proximal to the rectosigmoid [9]. Colonoscopy is considered the “gold standard” of screening for colorectal polyps and endoscopy incorporates the possibility to perform a biopsy or excision of a polyp [10, 11]. It offers high sensitivity and specificity, but some limitations apply to this method as well, including the invasiveness with a low but existent complication rate and the inconvenience patients have to suffer [12–14]. The rate of serious complications during or immediately after colonoscopy has been reported to be below 0.1% [15]. CTC Indications Besides the potential of a screening option for colorectal polyps and cancer, which is still controversial, CTC has increasingly established clinical indications, including incomplete colonoscopy, evaluation of the colon proximal to a stenosing lesion, and investigation of patients that are not in a suitable condition for undergoing a conventional colonoscopy (e.g., patients with bleeding disorders), or for patients refusing conventional colonoscopy [16–19]. CT equipment CTC has benefited greatly from developments in computed tomography (CT) scanner technology and new methods of 3D image processing. The introduction of spiral CT in the early 1990s culminated in the development of multidetector (MD) CT systems that allow scanning of greater volumes with thinner slices in less time. The possibility to perform an examination of the whole abdomen within a Various studies have been published on how to prepare patients prior to the examination. A well-distended, virtually stool- and fluid-free colon is the traditional way to perform a CTC [20, 21]. The cathartic cleansing keeps the reader from misinterpreting residual feces and helps to investigate as much colonic surface as possible. Unfortunately, this is highly dependent on patient compliance. Other publications emphasize that it is possible to perform a CTC without cathartic cleansing by using stooland fluid-tagging [22, 23]. Fecal- and fluid-tagging is achieved by fractionated oral administration of contrast agent (barium, sodium/meglumine diatrizoate). This helps to improve discrimination between stool residues and genuine polyps, and thus potentially improves the specificity of CTC [23, 24]. Different regimes and medications to perform a cathartic bowel cleansing are in use. A lot of experience with these medications exists because most of them are also used prior to optical colonoscopy. In addition to home-made cleansing solutions that some favor, most institutions rely on one of three commercially available groups of cleansing solutions: polyethylene glycol [PEG; e.g., GoLytely preparations (Delcoprep) and NuLytely preparations (Endofalk)]-based, phospho-soda-based solutions (e.g., Fleet Phospho-soda) and magnesium citrate (e.g., LoSoPrep). Although some studies show an advantage for phospho-soda, we favor a NuLytely PEG-based cleansing protocol as we are constantly able to achieve sufficient cleansing with this preparation regime [25]. Macari et al. [20] compared phospho-soda-based (‘dry’) cathartic preparation with PEG-electrolyte-based solutions (‘wet’) for CTC and found significantly less residual fluid and a drier mucosal surface using phospho-soda. Although preparations from both groups have been demonstrated safe for use in healthy individuals, caution should be taken in selecting a bowel preparation for individuals with significant comorbid conditions [26]. Sodium phosphate is contraindicated in patients with serum electrolyte imbalances, advanced hepatic dysfunction, acute and chronic renal failure, recent myocardial infarction, unstable angina, congestive heart failure, ileus, malabsorption, and ascites [26]. As mentioned above, it is possible to perform CTC without cathartic cleansing (“dry” preparation) [22, 27]. Bielen et al. [24] reported high patient compliance and acceptance using a “dry” bowel preparation. Especially noncompliant, elderly patients could benefit from a dry preparation. Combined with fecal tagging the use of automated cleansing techniques [28, 29] seems to be very promising. 431 After colonic cleansing, good bowel distension during scanning is required to further enhance visualization of the colonic surface. The easiest and most inexpensive way of achieving a pneumocolon is insufflating room air through a rectal enema tube into the colon using a manual balloon pump. This can be performed physician or patient controlled. We routinely achieve satisfactory results using the later approach [25]. CO2 administration instead of room air can be done automatically and patient controlled as well [30]. Some favor CO2 over room air as it is supposed to be better tolerated by means of patient comfort and potentially provides better colonic distension [31]. Several studies showed that it is imperative to perform the CT scan in the prone and supine patient positions [32– 35]. This helps to reallocate fluid to reveal previously hidden colonic surface, and insufflated air is redistributed during patient repositioning to further improve sensitivity and specificity in detecting colorectal polyps. Another controversially discussed issue is the use of spasmolytics (glucagon, N-butylscopolamin) prior to the scan to improve colonic distension. While some studies clearly show beneficial results in regard to bowel distension and patient comfort when using spasmolytics [36, 37], others failed to do so [35, 38]. Nevertheless, we routinely use spasmolytics. 2D and 3D data work-up The most important 2D procedures are the evaluation of the axial images and multiplanar reconstructions (MPR) that can be used to reconstruct any required scan orientation. In early studies on CTC, the complementary use of 2D and 3D images together was assumed to provide the highest sensitivity [45, 46]. Although some of the newer studies still favor a solitary 2D interpretation over 3D viewing [47, 48], some studies yielded low sensitivities for large polyps, ranging from 55% to 64% [49–51] using a primary 2D approach. On the other hand, some authors prefer primary 3D work-up [52, 53]. The impressive results (sensitivity 93.8% for lesions >10 mm) achieved in the latter study all go along with further improved CTC software as well as in CT scanner hardware. A major disadvantage of a primary 3D endoluminal approach—similar to conventional colonoscopy—is the lack of ability to look behind haustral folds. Ante- and retrograde fly-throughs are therefore mandatory, resulting in increased interpretation time. New visualization methods like an unfolded cube projection [54] and virtual dissection displays (e.g., Philips Filet view, Fig. 2, [47, 55, 56]) have the potential to overcome this limitation. Significant decrease of evaluation time down to 10 min per case could be observed with these techniques. Although it is our personal experience that lesion detection is best performed using a 3D approach, it is CTC scanning protocols necessary to further evaluate detected lesions in a 2D or MPR work-up to avoid pitfalls caused by misinterpreting Both collimation and pitch may influence the sensitivity for stool residuals, inverted diverticula, etc. as genuine colopolyp detection [39]. rectal polyps (Fig. 3). In the recent literature a clear trend for recommending Much emphasis has been put into CTC research, but there lower collimations can be recognized [18, 47, 48]. has been much unsteadiness in the results obtained with According to the “Consensus statement on CT colonography” regard to sensitivity and specificity, as outlined below. It of the European society of gastrointestinal and abdominal seems clear that reader performance increases with experadiology ESGAR [40], a collimation of less than 3 mm is rience [57, 58], and physicians who do CTC should receive currently recommended. appropriate training to perform and evaluate CTC datasets. The downside of acquiring thinner slices may be A lot of research [59–63] has been performed on increased radiation dose. As radiation is of serious concern automated polyp detection [computer-aided detection when performing CTC, exposure has to be kept as low as (CAD), Fig. 4], using different approaches: CAD as a “first possible. Consequently many studies investigated so-called reader”, as a “concurrent reader,” or as a “second reader.” As low-dose protocols [41–44]. In a study that was published a “first reader”, CAD separates out negative cases before by Macari et al. in 2002 [44], 50 mAs tube current, 120 kV physicians read the cases. However, this paradigm bears the voltage and a collimation of 4×1 mm were used. Large risk of missing colorectal lesions. CAD as a “concurrent polyps (>10 mm) were detected with a sensitivity of 93%, reader” presents suspect lesions to the physician, who can whereas the detection of intermediate size polyps (6–9 mm) then further evaluate the presented lesion and decide whether was compromised totaling in a sensitivity of 70%. Even it is a genuine polyp or not. It is unclear whether this type of more encouraging results were published by Iannacone et evaluation biases the reader by drawing attention to CAD al. in 2003 [43]. With a current of 10 mAs and a voltage of findings. Finally CAD as “second reader” re-reviews CTC 140 kVp, 100% sensitivity was reached for large polyps cases. Thus, CAD findings can be used to alter a report if (>10 mm) as well as for intermediate sized ones (6–9 mm). lesions have been missed in first place. Using CAD as a The “Consensus statement” mentioned above [44] “second reader” in this specific setting may lead to an currently recommends for supine and prone non-IV contrast increase in reading time, though [64]. enhanced acquisition with a tube current of 100 mAs or less Recently published data showed encouraging results (50 mAs or less), dependent on available CT technology. using CAD. In a study performed by Taylor et al. [62], 432 Fig. 2 Principle of a colon dissection display. The colon, previously reconstructed as a tube, is cut at one side (a), unrolled (b) and presented similar to a pathological specimen (c) CAD reached a sensitivity of 92% for polyps >10 mm. Overall the CAD performance was comparable and in some parts even better than that of expert readers. If a robust CAD algorithm can be found, a further decrease in interpretation time may be on the horizon, and inexperienced readers might miss less polyps. Although so-called “flat” adenomas are not considered to have a markedly increased risk of developing into invasive cancer compared with sessile or pedunculated polyps by some researchers [65], they still remain problematic to be detected in CTC [66, 67]. Since up to 27% of all baseline adenomas may be flat [65], this remains a problem that needs researchers’ attention in the future. One possible Fig. 3 Pitfall in CTC. a Polypoid lesion as seen in endoluminal and dissection 3D reconstructions. b The corresponding MPR discriminates residual feces (arrow) containing air from a genuine polyp approach is using a “translucency view” (Fig. 5). This postprocessing algorithm assigns colors to the mucosa based on HU values. Besides ruling out false positives by helping to differentiate between stool residuals and colorectal polyps, this might (especially if used in conjunction with IV contrast media) help to reveal flat adenomas. CTC performance Pickhardt and coworkers published in 2003 the first large prospective study in an average-risk screening population, comparing more than 1,200 CT colonographies with 433 Fig. 4 CAD marked 8-mm polyp (blue) in endoluminal (a) and dissection (b) display mode optical colonography performed on the same day [53]. Their sensitivity of CTC in the detection of adenomatous polyps was 93.8% for polyps at least 10 mm in diameter, 93.9% for polyps at least 8 mm in diameter, and 88.7% for polyps at least 6 mm in diameter. The sensitivity of optical colonoscopy for adenomatous polyps was 87.5%, 91.5%, and 92.3% for the three sizes of polyps, respectively. They concluded that CTC is an accurate screening method for the detection of colorectal neoplasia in asymptomatic Fig. 5 “Tranclucency view” (shown in the middle of the upper row). 1 untagged stool is represented in green; 2 pedunculated polyp is shown in red average-risk adults and compares favorably with optical colonography (Fig. 6). Not quite 2 years later, Rockey and coworkers published their prospective results of more than 600 CTCs in comparison with optical colonoscopy and air contrast barium enema [51], using a similar study design to the one used by Pickhardt et al. [53]. When analyzed on a perpatient basis, for lesions 10 mm or larger in size, the sensitivity of CTC was 59% (compared with 93.8% reported by Pickhardt and coworkers), and of colonoscopy 98%. For lesions 6–9 mm in size, sensitivity was 51% for CTC and 99% for colonoscopy. The exact reason for this striking difference in reported performance of CTC is yet unclear, although both papers were extensively discussed and commented in the scientific community. Three recent major meta-analysis publications tried to systematically approach the CTC performance in the light of the reported variability [68–70] (Table 1). In the largest meta-analysis published up to now, Mulhall et al. [69] systematically reviewed the test performance of CTC, selecting prospective studies published before February 2005 from 33 studies (CTC after full bowel preparation and insufflation of the colon, with colonoscopy or surgery as the gold standard, collimation smaller than 5 mm, both 2D and 3D for scan interpretation) providing data on 6,393 patients. The sensitivity of CTC 434 account for this variability. Collimation, type of scanner, and mode of imaging explain some of the discrepancy, but not all of it. Patients’ perception and tolerance of CTC compared with conventional colonoscopy Many comparisons of patients’ acceptance and tolerance have been published, and researchers were able to show that either CTC is better tolerated than colonoscopy [13, 14] or vice versa [71, 72]. The discussion is not very useful because most colonoscopies are performed using sedatives, which makes a direct comparison impossible. Nevertheless, bowel preparation seems to be the most uncomfortable issue for both CTC and colonoscopy from the patients’ point of view [14]. CTC in incomplete colonoscopy CTC after incomplete colonoscopy may be especially helpful for evaluation of the nonvisualized part of the colon after incomplete colonoscopy, and it can increase the diagnostic yield of masses and clinically important polyps in this context [17, 19, 73]. The rate of incomplete colonoscopies varies between 4% [74] and 19% [75–77]. This frequency serves as an important indication for performing immediate CTC in order to avoid repeat bowel preparation when possible. Fig. 6 Colonic polyp. a Dissection view, b endoluminal view, c endoscopic view. Note also diverticulae, especially apparent in a was heterogeneous but improved as polyp size increased [48% (95% CI, 25–70%) for detection of polyps <6 mm, 70% (95% CI, 55–84%) for polyps 6–9 mm, and 85% (95% CI, 79–91%) for polyps >9 mm]. In contrast, specificity was homogenous [92% (95% CI, 89–96%) for detection of polyps <6 mm, 93% (95% CI, 91–95%) for polyps 6–9 mm, and 97% (95% CI, 96–97%) for polyps >9 mm]. They came to the conclusion that, although CTC is highly specific, the range of reported sensitivities is wide, and patient or scanner characteristics do not fully CTC open issues As discussed above and outlined in the meta-analysis by Mulhall et al. [69], the wide range of reported sensitivities that can not be completely explained must be resolved before CTC can be advocated for generalized screening for colorectal cancer. CTC has not yet been officially accepted as a screening procedure in any country, mainly because of the lack of reliable evidence resulting from large trials. Another important open issue concerns the relevance of small polyps. The overall prevalence of colorectal polyps independent of size and histology in an average risk screening population is estimated to be in the range of 25– Table 1 CTC performance as calculated in meta-analyses Authors Year Number of studies included Number of patients included Per patient sensitivity; polyps >9 mm (95% CI) Per patient sensitivity; polyps 6–9 mm (95% CI) Per patient sensitivity; polyps <6 mm (95% CI) Sosna et al. [68] Mulhall et al. [69] 2003 2005 14 33 1,324 6,393 88% (84–93%) 85% (79–91%) 84% (80–89%) 70% (55–84%) 65% (57–73%) 48% (25–70%) 435 30% [78–80]. The current concept of polypectomy is to remove all polyps detected during optical colonoscopy (independent of size and histology). This results in a significant decrease in mortality from colorectal cancer, as shown by the National Polyp Study Workgroup [5]. Although some authors argue that polyps of less than 5 mm [81] or 10 mm [82] in size may not need immediate polypectomy, the majority of gastroenterologists disagree [83], and no prospective study has shown a decrease in the mortality of colorectal cancer using any threshold size for polypectomy. This has several implications for CTC. Even if CTC would be capable of detecting all or at least the majority of the polyps smaller than 10 mm and no falsepositive findings would occur, approximately every third or fourth patient would still have to undergo interventional optical colonoscopy with polypectomy after CTC. Since this seems to be an unacceptably high rate of follow-up endoscopies and the known lower sensitivity of CTC in the detection of smaller polyps, a threshold size for “relevant” polyps would have to be defined before CTC could be used in large screening settings. The other major implication relates to the fact that CTC performs poorer in the detection of smaller polyps and relates to the clinical value of a “negative” CTC in terms of need for follow-up exams, and the definition of a reasonable time interval to do so. Addressing the significance of missed or found small polyps on CTC, Macari et al. [84] recommend a CTC follow-up after 3 years for lesions smaller than 6 mm. The ESGAR consensus statement recommends that polyps less than 5 mm in size should not even be reported, providing that agreement for such a reporting policy has been made with those referring patients [40], but no general recommendation regarding follow-up intervals was made. In a consensus proposal, the Working Group on Virtual Colonoscopy discusses the so called “clinically important polyp and the rationale for surveillance” and discriminates between “diminuitive”, “intermediate”, “multiple intermediate” and “lesions that are 1 cm in size or larger” [85]. In their opinion, “diminuitive” lesions (smaller than 5 mm) should not be reported, similar to the approach suggested by the ESGAR consensus [40]. Patients with one or two “intermediate” lesions (6–9 mm) should be recommended interval surveillance after up to three years depending on several factors, including patient age, sex, comorbidities, and preference and local practice. More than three lesions of 6–9 mm or one lesion of at least 10 mm require immediate colonoscopy. Although aspects of this proposal may be discussed controversially, the proposed framework addresses the definite need to have a reference guide for interpretation of CTC results. Conclusion CTC offers high sensitivity and specificity for the detection of colon cancer and polyps larger than 10 mm in size, given suitable equipment and experienced investigators. It is the method of choice for incomplete colonoscopies and for patients that to some reason can not undergo optical colonoscopy. Nevertheless, its use in routine screening should be subject to the introduction of quality controls with prescribed examination standards. For screening purposes, the wide range of reported sensitivities that can not be completely explained must be resolved and a threshold size for clinically relevant polyps has to be defined, and its application backed by prospective studies. In particular, multicenter trials are necessary to achieve this goal. Computer-assisted evaluation has the potential to shorten the examination time and may further increase sensitivity in the near future. References 1. Vining D, Shifrin R, Grishaw E (1994) Virtual colonoscopy. Radiology 193:446 2. 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