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Incidental lesions found on CT colonography: their nature and frequency

¹ Department of Public Health and Epidemiology, Public Health Building, The University of Birmingham, Edgbaston, Birmingham B15 2TT, ² Department of Intestinal Imaging, St. Mark's Hospital, Watford Road, Northwick Park, London HA1 3UJ and ³ Department of Surgery, The University of Birmingham, Edgbaston, Birmingham B15 2TT, UK

	Abstract

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CT colonography has been used to detect colonic polyps and cancers, but its effect in practice will also be influenced by the frequency with which extracolonic lesions of various types are detected. We performed a systematic review of the types of incidental lesions found on CT colonography. This is necessary to model the benefits and harms of detecting extracolonic lesions. Primary clinical studies of extracolonic findings on CT colonography were identified from electronic databases, scanning reference lists and hand searches of relevant journals and conference proceedings. A data collection proforma was used to collect information on extracolonic findings. 17 discreet studies were identified, involving 3488 patients. In total 40% of patients were recorded to have abnormalities and many had more than one abnormality. Nearly 14% of patients had further investigations and 0.8% were given immediate treatment. Extracolonic cancers were detected in 2.7% (0.9% had N0M0 cancers) and 0.9% had an aortic aneurysm. The number of extracolonic findings was high in all studies. While only a small population were judged "important", the prevalence of serious lesions outside the colon was nevertheless higher than in many other screening programs.

	Introduction

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CT colonography uses a combination of helical CT scanning and complex image rendering to image the large bowel and is able to produce images that simulate those seen on conventional video-endoscopy; hence the alternative term "virtual colonoscopy" [1, 2]. The sensitivity and specificity of this new health technology for neoplasia (i.e. cancers and polyps) is likely to be superior to the established imaging test, barium enema, and similar to video colonoscopy [2]. The results of studies, which have measured the accuracy of colonography by conducting both this test and colonoscopy sequentially on the same patients, have been reviewed elsewhere [1].

One of the intriguing features of colonography, however, is its ability to detect extracolonic lesions – sometimes referred to as "incidental findings", because the whole abdomen, pelvis and lower lung fields are imaged, as opposed to just the colorectum. These incidental findings have been classified according to their importance: i.e. highly important, possibly important and unimportant. An holistic assessment of the benefits and drawbacks of colonography as compared with other diagnostic and screening methods, must include an assessment of the benefits and harms which result from the detection of these lesions. In some cases, lives may be saved by detecting disease at a stage when it is still curable. In others, unnecessary procedures may be performed, with resultant complications, anxiety and use of resources.

A rational assessment of the "balance sheet", contingent on finding these incidental lesions, must begin with careful enumeration of the frequency and nature of such lesions. We therefore performed a systematic review of studies of incidental lesions found in the course of colonography carried out for the purposes of screening or diagnosis.

	Methods

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Identification of studies
We included primary clinical studies of extracolonic and incidental findings on CT colonography. According to the guidance from the NHS Centre for Reviews and Dissemination [3], we identified studies by searching electronic databases, scanning reference list of papers and consulting experts in the specialty. No date or language limits were placed on the searches. We also hand searched selected journals. We found no other systematic reviews focusing on extracolonic lesions (see Appendix 1 for full search strategies).

One reviewer (TX) examined titles, abstracts and keywords of citations, as given on electronic databases, and selected those which mentioned the concept of extracolonic lesions. Where possible the full text of all of potentially relevant citations was then obtained. All retrieved references were exported to Reference Manager v 10.0 (Thompson ResearchSoft, Thompson Corp., Berkley, CA).

Data extraction and synthesis
One reviewer (TX) decided whether studies met the inclusion criteria and this was checked by a second reviewer (MR). Using a standardized, piloted, data collection proforma, these two reviewers independently extracted data from papers on extracolonic findings from CT colonography.

We first collected methodological information: i.e. whether or not the population was clearly described; whether the author stated that consecutive cases were studied; whether the data collection was prospective or retrospective; and whether the investigations were carried out for diagnostic or screening purposes (Table 1). This process was carried out independently by two investigators (TX and MR) and any differences resolved in a three way meeting (TX, MR and RL).

We assembled data in three separate tables. First, data from full papers published in peer-reviewed articles dealing with patients given a bowel preparation were included in Table 2 (series 1). We assembled data collected from conference proceedings in Table 3 (series 2), on the grounds that these are generally less comprehensive and had been subject to less stringent quality control than the full articles. In some papers, although the focus was on primary CT diagnosis of colorectal cancers, full bowel preparation was not used since the population investigated was the frail elderly, in whom CT was being requested as an alternative to either barium enema (which has a high technical failure rate in this group) [16, 17] or video colonoscopy (which suffers from an increased rate of adverse events in this group) [6, 16, 17]. This might be expected to decrease sensitivity for colonic neoplasia. However, the incidence of extracolonic findings, might be expected to be increased in this group since they are older and clinical presentation is frequently non-specific. We therefore assembled data from these papers in Table 4 (series 3).

	Results

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We describe the features of the 18 studies on which reports could be retrieved in Table 1. Only six of the reports clearly stated that consecutive cases were studied. 14 were clearly prospective studies. Three of the studies dealt with colonography as a screening test, while 14 studied diagnostic colonographies. It was not possible to be clear on this issue in the remaining paper. Most of the studies were rather small: only three included more than 200 patients and one included as few as 37 patients.

We discerned that two full papers [5, 11] emanated from the same centre – the Mayo clinic. The most recent paper [5] did not make it clear whether or not the two series overlapped. We therefore contacted two of the authors, who confirmed that the first paper did indeed contaminate the second (we would like to thank Amy Hara and Joel Fletcher from the Mayo for their help in elucidating this issue). We excluded the earlier paper and did not include it in Table 2.

Findings from full papers, excluding papers dealing specifically with the frail elderly, are given in Table 2. The mean age of patients included was the mid 60s in five studies, with slightly older and younger patients in the remaining studies. As expected, the mean age in papers dealing with the frail elderly (Table 4) was considerably higher. Contrast was used in five of all studies.

The number of abnormalities was high in all three series. In total 40% (1314/3280) of patients were recorded to have abnormalities. The percentage of people with an abnormality was 36% (930/2565), 65% (316/483) and 29% (68/232) in the three series, respectively. The total number of abnormalities was even greater, since many patients had more than one abnormality. The total number of abnormalities as a proportion of people screened was 58% (1483/2565), 66% (190/290) and 26% (90/350), respectively, in the three series. These calculations are based on those authors who provided both the relevant numerator and denominator information (some studies did not record the total number of abnormalities – only the number of patients with at least one abnormality). In addition some other papers did not give the number of patients with a diagnosis – only the total number of incidental lesions found (see Tables 2–4). To sum up, extracolonic abnormalities are common, even when the frail elderly are excluded. Indeed, in six of the studies the total number of abnormalities found was greater than the number of patients entered.

In a number of studies, authors graded the lesions according to their "importance". The total number of "important findings" among 2787 patients was 292 (10.5%). As previously stated, they use different criteria to classify lesions as important and in all cases "importance" was based on clinical relevance in terms of the need for further investigations. For this reason, we also separately abstracted cases with relatively common serious diseases – cancers and abdominal aortic aneurysms. When we did this, the proportion of lesions of confirmed importance was much smaller; a total of 2.7% (81/3005) had cancers and 0.9% (30/3305) had aortic aneurysms. Six studies recorded the size of aortic aneurysms. 16 aneurysms were detected in these studies; 3 (19%) were over 5.5 cm in size and the remainder were between 3 cm and 5.5 cm. A total of 0.9% (24/2549) patients had N0M0 cancers. Again, these calculations are based on those authors who provided both the relevant numerator and denominator information (see Tables 2–4).

The number of further investigations carried out was also quite large – in some case it even exceeded the number of lesions regarded as important by the author. A total of 13.8% (188/1362) of patients had further investigation.

The incidence of immediate treatment was only given in six studies and averaged 0.8% (17/2237).

Two studies gave the incidence of lesions found during long-term follow-up. Among these two studies the probability of finding yet a further lesion on long-term follow-up was 2.7% (3/110).

Eight studies explicitly record the nature of early stage (N0M0) primary extracolonic cancers; Table 5 lists these cancers by their primary organ. Among a total of 2549 patients, 6 kidney cancers (0.24%), 5 ovarian cancers (0.20%), 5 lung cancers (0.20%), 4 pancreatic cancers (0.16%) and 1 liver cancer (0.04%) were found. These prevalence figures are all higher than the 25-year incidence figures recorded, for example, in the Surveillance, Epidemiology and End Results (SEER) database [25].

	Discussion

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However, a detection rate for "early" cancer of about 6 per 1000 is significant in both clinical and epidemiological terms. For example, the prevalence of breast cancer in breast screening programmes is similar (range from 5.6 to 8.5 per 1000 women) [22], and the prevalence of ovarian cancer in ovarian cancer screening programmes is very much lower (about 1 per 2000 women) [23]. Indeed, the prevalence of "early" colorectal cancer detected by this modality in screening studies is of similar magnitude (0.7% had N0M0 bowel cancer) [24]. It therefore transpires that colonography may be an important method for the detection of early cancers other than colon cancers, although we recognize that this modality also detects colonic lesions in their pre-malignant phase (i.e. colonic adenomas).

Nearly half (42%) of cancers detected were of an early stage N0M0. Detection of lesions at this stage is, of course, most likely to result in health gains. From these data we therefore tentatively suggest that CT colonography, even without the use of contrast, may be an important potential modality, net of its effect on detecting colonic lesions. That said, it is important not to extrapolate the potential benefits of detecting early lesions uncritically from the prognoses of such lesions detected in normal clinical practice. This is because the prognoses of lesions detected in early stage may differ systematically according to method of detection. A crucial concept that relates to the effects of detecting early lesions is sojourn time. The fact that the prevalence was higher than the 25-year incidence implies quite long sojourn times and suggests that only once or infrequent screening may be effective in reducing eventual mortality. However, very long sojourn times suggest that the number of years of life gained might be quite modest and some lesions may never progress; at the limit, this must be the case where prevalence exceeds lifetime incidence. Future modelling will have to make assumptions about these variables and incorporate further information that will eventually be obtained, for example from the US Prostate, Lung, Colorectal and Ovarian (PLCO) screening study [26].

We also observe that this is "early" days for this form of diagnosis or screening. The publications which we cite are often based on incomplete data sets. For example, in many cases they do not clearly indicate that consecutive cases were studied. Nevertheless, some of the papers (such as that of Gluecker and colleagues) are of high quality [5]. The data from Gluecker study are very much in line with those from the other studies in Table 2. However, we will be the first to argue that bigger and more comprehensive datasets are required. Lastly, practically all of the studies used symptomatic patients rather than those with a population risk for colorectal cancer. It is therefore possible that the condition that prompted the investigation, was extracolonic (especially in the frail elderly group). If so, the common finding of such lesions would add further weight to arguments for the use of this method for diagnosis, but it would also suggest that lower utility would result from detection of extracolonic lesions in a screening program. However, we think that the incidental lesions revealed by this modality would generally have been "silent", i.e. they are truly incidental, except for the frail elderly and we analysed this group separately for this reason. If we are right, the possibility of finding serious lesions outside the colon should be added to the colon related benefits of this screening modality, although the model would need to include the "costs" of investigations and interventions prompted by the method. These costs would have to be broadly defined to include the anxiety and other morbidity associated with investigation of incidental lesions.

	Appendix 1: Search strategy for electronic databases and hand search run in March 2004

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Pubmed
• Text terms used and the corresponding number of papers retrieved:

Other electronic databases searched
• We also repeated the searches in the following databases:

Hand searched following relevant journals
Gastroenterology. Diseases of the Colon and Rectum. The American Journal of Gastroenterology. Radiology. British Journal of Radiology. European Journal of Radiology. European Radiology. (from January 2003 to February 2004).

Conference proceedings handsearched
• Boston Medical Center. Proceedings of the Fourth International Symposium of Virtual Colonoscopy, Boston, USA. 13–15 October 2003.

• American College of Gastroenterology. Proceedings of the 68th Annual Scientific Meeting of the American College of Gastroenterology, Baltimore, USA. 13–15 October 2003.

• American College of Gastroenterology. Proceedings of the 67th Annual Scientific Meeting of the American College of Gastroenterology, Washington, USA. 20–23 October 2002.

• ASCRS. Proceedings of the meeting of the American-Society-of-Colon-and-Rectal-Surgeons, New Orleans, LO, USA. 21–26 June 2003.

• ASCRS. Proceedings of the meeting of the American-Society-of-Colon-and-Rectal-Surgeons, Chicago, IL, USA. 03–09 June 2002.

• AGA. Digestive Disease Week 2003 Meeting. Proceedings of the 104th Annual Meeting of the American-Gastroenterological-Association. Orlando, FL, USA. 17–22 May 2003.

• AGA. Proceedings of the Annual Meeting of the American-Gastroenterological-Association. San Francisco, CA, USA. 19–22 May 2002.

• AGA. Digestive Disease Week 2001 Meeting. Proceedings of the 102nd Annual Meeting of the American-Gastroenterological-Association. Atlanta, GA, USA. 20–23 May 2001.

• RSNA. Proceedings of the 89th Scientific Assembly and Annual Meeting of the Radiological-Society-of-North-America. Chicago, IL, USA. 30 November – 05 December 2003.

• RSNA. Proceedings of the 88th Scientific Assembly and Annual Meeting of the Radiological-Society-of-North-America. Chicago, IL, USA. 01–06 December 2002.

• RSNA. Proceedings of the 87th Scientific Assembly and Annual Meeting of the Radiological-Society-of-North-America. Chicago, IL, USA. 25–30 November 2001.

• RSNA. Proceedings of the 86th Scientific Assembly and Annual Meeting of the Radiological-Society-of-North-America. Chicago, IL, USA. 26 November–01 December 2000.

• European Congress of Radiology. ECR 2003 Conference, Vienna, Austria, 07–11 Mar 2003.

• ECR. Proceedings of the 14th Annual Meeting of the European Congress of Radiology. Vienna, Austria. 01–04 March 2002.

• ECR. Proceedings of the 13th Annual Meeting of the European Congress of Radiology. Vienna, Austria. 02–06 March 2001.

	Footnotes

 
This study was sponsored by the Health Technology Assessment Programme of the Department of Health in England. The views are those of the authors.

Received for publication April 21, 2004. Accepted for publication August 19, 2004.

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