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British Journal of Radiology 74 (2001),4-14 © 2001 The British Institute of Radiology

Review article

CT and bowel disease

A H Freeman, MB, FRCR

Department of Radiology, Addenbrooke's Hospital, Hills Road, Cambridge, CB2 2QQ UK


   Abstract
Top
 Abstract
Introduction
 The large bowel
 The small bowel
 References
 
CT has now come of age in the detection and demonstration of bowel pathology and is likely to supplant traditional imaging techniques further in the future. Its role here has been greatly aided by the advent of fast spiral CT sequences and, with the development of even faster multidetector CT systems, this can only increase.


   Introduction
Top
 Abstract
 Introduction
The large bowel
 The small bowel
 References
 
The introduction of CT in the 1970s heralded a new era in radiology, initially with applications to the head and later to the chest and abdomen. Abdominal studies were originally confined to the solid organs and the retroperitoneum, extending eventually into the peritoneal cavity. Bowel detail itself was not referred to owing to slow data acquisition times and lack of definition.

Major improvements in computing science as well as the development of spiral techniques have now led to large volume data acquisition and ultimately three-dimensional (3D) CT. Even before these improvements, there was recognition of the potential role that CT might play in evaluating bowel disorders both by the demonstration of secondary signs of bowel disease, i.e. abnormal fat [1] or hypervascularity [2], as well as by direct imaging of the bowel wall. Greater emphasis has been placed on imaging the colon rather than the small bowel, and CT in relation to the colon will be discussed first.


   The large bowel
Top
 Abstract
 Introduction
 The large bowel
The small bowel
 References
 
The colon is subject to four common conditions: (1) tumour; (2) diverticular disease; (3) inflammatory bowel disease; and (4) appendicitis.

Tumour
Rectal carcinoma initially aroused CT interest [3, 4] and its role in staging is now well accepted. The ability of CT to detect liver metastases (Dukes' D), lymph node involvement (Dukes' C) and local infiltration into the adjacent perirectal fat (Dukes' B2) was a revelation. However, the distinction between Dukes' B1 with tumour limited to the muscularis and Dukes' A with tumour limited to the submucosa remains impossible with CT but can be made with endoscopic ultrasound [5]. Even here, spiral CT may be useful if a biphasic contrast examination is performed so that both arterial and venous phases are recorded, as T1 tumours can be distinguished from T2 tumours by the absence of enhancement in the venous phase [6]. CT remains a general staging tool for those lesions considered appropriate for pre-operative radiotherapy, particularly squamous tumours arising from the anorectal margin.

CT is on stronger ground in the assessment of recurrent tumour as there is often an extramucosal mass at the anastomosis, which may not be appreciated by either barium studies or colonoscopy. Allowance has to be made for soft tissue abnormalities in the early post-operative phase, which often form a perirectal halo, and also for post-radiation change if radiation has been used as adjuvant therapy [7].

The post-rectal space after either low anterior resection or abdomen/perineal resection is a difficult area. Is the mass due to fibrosis or to recurrence? This presents a problem for both CT and MRI, neither of which can give a definite answer [8] (Figure 1Go). An enhancing mass is strongly suggestive of recurrent tumour and perfusion studies are currently under scrutiny with CT [9] and MRI [10]; but only biopsy will give a definitive result. It will be interesting to see whether positron emission tomography (PET) will provide useful data in this clinical setting.



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  		Figure 1. Pelvic CT following abdominal perineal resection, showing slight enhancement of the pre-sacral mass, which also contains a centre of lower attenuation. This was owing to recurrent disease, but the distinction is difficult by imaging criteria alone.

 
Tumours are visible in other areas of the colon, particularly if they demonstrate a large mass, butconventional non-spiral CT has not been routinely used so far for their detection in a symptomatic population.

An exception to this has been the role of CT in demonstrating colon cancer in frail elderly patients who have suggestive symptoms. Given that these patients are likely to find the preparation and performance of a barium enema distressing, and that it may prove incomplete in these patients, a pilot study was performed to assess the performance of CT against barium enema in this patient group [11]. Encouraging results from this study led to the implementation of a protocol involving oral preparation as the sole means for opacifying the colon and all patients were then examined using 1.0 cm thick slices at 1.5 cm intervals [12]. The typical signs of bowel cancer were looked for, i.e. localized bowel wall thickening particularly if asymmetrical, local fat invasion and/or polypoid mass formation (Figures 2a,bGo). It is difficult to detect masses much smaller than 1.5 cm with this technique, but in the age group concerned the detection of small mucosal polyps is not considered of major clinical importance. Furthermore, the procedure is being performed for prognostic information only in many of these patients. A further advantage of this technique is that other pathology outside of the colon is routinely demonstrated, including liver metastases, involvement of the abdominal wall and ascites.



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  		Figure 2. (a) CT in a patient with anaemia. The thickening on the medial wall of the caecum was overlooked, with the carcinoma being demonstrated on a contrast enema 10 months later (b). This case illustrates the point of paying attention to any area of abnormal bowel wall thickening.

 
The concept and usefulness of this minimal preparation examination has recently been validated by two further publications [13, 14], but the next logical step was to examine the colon following full bowel preparation and air/gas distension. A preliminary report showed that utilizing this protocol together with spiral CT was highly effective in the demonstration of colonic tumours [15], and this was confirmed by a larger series from the same authors in which 38 carcinomas were correctly identified in 47 patients with an overall staging accuracy of 75% [16] (Figure 3Go). Both of these studies utilized two-dimensional (2D) CT, but one of the major advantages of spiral CT is its ability to examine the whole abdomen in one breath-hold, thus introducing the prospect of 3D CT. This technique, originally described by Vining [17], utilizes two computed techniques to enhance the data gleaned from 2D imaging. These include perspective projection and real-time rendering, whereby 3D images are generated at 15–30 frames per s. This can be combined with either surface rendering or volume rendering, so that in the former the impression is given of the outside of the bowel loop (as viewed at laparotomy) whereas the latter can give rise to images from inside the bowel thus creating the illusion that the operator is flying through the lumen of the colon (virtual endoscopy).



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  		Figure 3. Image taken during colography after full bowel preparation and air insufflation demonstrates an annular carcinoma of the caecum (arrows).

 
At least three large trials [18–20] have shown a high degree of accuracy in the detection of tumours and large polyps by these techniques when assessed against standard colonoscopy, although demonstration of small polyps remains difficult. Obviously, maximal bowel distension has to be obtained and this can be difficult to assess, as one has to rely on the patient's comments and judge the results from the subsequent scanogram. Air is preferred to carbon dioxide because the rapid resorption of the latter can lead to a collapsed colon at the time of scanning. A spasmolytic drug is usually used but there is no overall agreement as to whether or not intravenous contrast medium is essential. Reconstruction times are falling but still add considerably to the overall time of the examination, which is short, as it should involve a single spiral run through the abdomen once gas has been administered. A second run is occasionally required, usually with the patient in the prone position to overcome the problem of fluid layering on the posterior wall of the colon, which may obscure lesions. This will double the radiation burden, the absorbed dose from a single spiral CT run through the abdomen being equivalent to that of a barium enema.

Interest in this development has been heightened by the proposal for a national screening programme to detect colorectal cancer. It is accepted that, in the UK, introduction of such a national programme could result in the prevention of approximately 1200 deaths from colorectal cancer each year [21] and two pilot schemes have been set up to cover populations of approximately one million each. Both these pilot schemes use conventional colonoscopy as the diagnostic tool to evaluate positive faecal occult blood. However, colonoscopy has a significant complication rate and if introduced on a national screening scale, it could result in up to 12 deaths per annum. For this reason, virtual colonoscopy has been advanced as a diagnostic test [22], although to date there has been no trial between this and the only other non-invasive test, the tried and tested double contrast barium enema. There is probably little difference in the sensitivity of the two techniques in the detection of large polyps or tumours, but virtual colonoscopy would have the advantage of more rapid patient throughput and probably better patient compliance. It also offers the potential to proceed to a therapeutic colonoscopy if this is indicated. Finally, as it is viewed as a new and exciting development by both radiologists and radiographers, it might help to train and recruit staff for screening programmes [23], which has been notoriously difficult in other screening areas, such as mammography.

Is virtual colonoscopy necessary or is 2D imaging enough? It is imperative that all images are viewed at different window settings if 2D only is used, including those at lung settings. This can be done quickly whilst the patient is on the table, whereas virtual colonoscopy at present requires the use of a separate work station and considerable computing time. The advantage of virtual colonoscopy is that both antegrade and retrograde virtual images are stored in a cine loop and can therefore be viewed in an interactive fashion, so that polyps may be seen at different angles and tumours looked at from entirely different perspectives [19]. It seems likely to become widely available in the next few years and will thus require much more CT capacity.

Diverticular disease
Diverticular disease and its complications remain a major source of morbidity. Assessment of the extent of diverticular change in the colon is best shown by barium enema, but demonstrating its complications is increasingly in the realm of CT [24, 25]. This particularly applies to the evaluation of either local or remote diverticular abscess. Whilst there may be characteristic signs of a pericolic abscess at barium enema, its size and extent is much better appreciated during CT, which may also be used for drainage guidance [26]. One of the characteristics of diverticular disease in the sigmoid is thickening of the bowel wall, which may be confused with malignancy (Figure 4aGo). The thickening is partly due to collagenous change, but in many cases it is secondary to an inflammatory process associated with diverticular disease, which in turn may give rise to mesenteric inflammation. The presence of fluid at the root of the mesentery together with vascular engorgement in the mesentery has been reported as a useful sign in distinguishing sigmoid diverticulitis from carcinoma [27] (Figure 4bGo). However, a recent prospective review showed that distinction is often still difficult, considerable overlap of the signs allowing unequivocal distinction between diverticulitis and carcinoma in only about 50% of cases [28].



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  		Figure 4. Two examples of diverticular disease of the sigmoid and its complications. (a) Marked soft tissue thickening of the sigmoid within which there are diverticula. At this stage much of the change is likely to be collagenous. (b) Low attenuation element indicates a more fluid component due to a pericolic abscess. Note in both examples the prominent vascularity around the lesion and the changes in the pericolic fat.

 
Inflammatory bowel disease
Inflammatory bowel disease is a less common colonic problem but the various forms of colitis (for example, idiopathic, ischaemic, pseudomembranous) can still present a diagnostic challenge, particularly if only the right side of the colon is involved. Although HMPAO-labelled white cell scintigraphy retains centre stage in the assessment of idiopathic colitides, both the primary and secondary changes caused by colitis are well appreciated with CT and may often be the first clue in an abdominal complaint of unknown cause [29]. As with diverticulitis, these changes include increased vascularity at the mesentery [2, 30] together with inflammatory infiltration in the pericolic fat [31] (Figure 5Go). The demonstration of abscess and fistula formation in Crohn's disease is well appreciated on both CT and MRI. The primary sign of inflammatory bowel disease is bowel wall thickening, caused mainly by submucosal oedema, and results in the so-called halo sign. Attempts have been made to assess the nature of colitis from the diameter of the colonic wall and, as would be expected, Crohn's disease and pseudomembranous colitis give more marked thickening (of the order of 10 to 11 mm) than that found in ulcerative colitis (7–8 mm) [32–34] (Figure 6Go). The bowel wall thickening may give rise to confusion with malignancy, but the distinction is helped by the presence of the halo sign, which is rarely if ever seen in malignancy. The presence of a symmetrical distribution in the colon together with inflammatory change in the mesentery also help in making the distinction. With long-standing chronic ulcerative colitis there is a true permanent deposition of submucosal fat together with increased perirectal fat [35].



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  		Figure 5. Crohn's colitis demonstrating marked inflammatory changes in the perirectal fat together with considerable bowel wall thickening of both the rectum and sigmoid.

 


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  		Figure 6. Prominent thickening of the bowel wall in the ascending colon completely obliterates the lumen in a case of pseudomembranous colitis. Note that the left colon is not so severely involved. There is also hyperaemia of the mucosa.

 
Appendicitis
Until relatively recently there was no radiological input into the diagnosis of appendicitis other than occasional plain abdominal radiographs, which would show an appendicolith in approximately 10% of cases.

Ultrasound was the initial cross-sectional imaging tool to be used [36] and subsequent studies confirmed the sensitivity of this method both in the detection of appendicitis as well as in the demonstration of the normal appendix [37]. The key to the examination obviously lies with the utilization of high frequency probes, together with graded compression of the right iliac fossa. This technique also allows the operator to interact with the patient, a point emphasized by Puylaert, and of course this test has particular relevance in the paediatric population [38]. In addition, alternative right iliac fossa lesions could be evaluated [39].

At about the same time there were also initial reports of the value of CT in diagnosing acute appendicitis [40, 41] as well as in demonstrating the normal appendix [42]. Again, the advent of spiral CT has considerably simplified its diagnostic potential so that it is now possible to perform a short spiral run at the level of the appendix leading to the term "FACT" (focused appendix CT) [43]. A large number of studies have confirmed its accuracy, many quoting a sensitivity and specificity of around 96%. The CT signs of appendicitis include a distended fluid-filled tubular structure with a thickened and enhancing wall (Figure 7aGo). In 20–40% there will be an intraluminal calcified appendicolith. Outside the appendix, the expected signs of inflammation are stranding and abnormal fat planes, plus a frank abscess. Pericaecal changes are often present (Figure 7bGo). In addition, other non-appendiceal abnormalities, such as mesenteric adenopathy, are well demonstrated by this technique [44].



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  		Figure 7. Two examples of acute appendicitis with (a) distended fluid-filled lumen of the appendix together with some enhancement of its wall, and (b) more prominent inflammatory change extending into the pericaecal area.

 
There is no consensus about preparation for this procedure. Initial studies utilized intraluminal and intravenous contrast media, but equally good results may be obtained without the use of any contrast medium. The current view suggests that colonic opacification with only dilute contrast material is all that is required [45]. How necessary is this imaging when compared with traditional clinical examination? Balthazar and colleagues [46] have shown a considerable drop in appendicectomies yielding a normal appendix, from 20% to 4%. Apart from the patient avoiding unnecessary operation, the actual cost savings and facility savings to the hospital have also been well documented [47].


   The small bowel
Top
 Abstract
 Introduction
 The large bowel
 The small bowel
References
 
Tumour
The role of CT in small bowel disease has developed relatively recently, partly owing to the fact that the small intestine is a less common source of pathology. Two roles for CT have emerged; first, in the investigation of small bowel tumours, and second in the evaluation of small bowel obstruction. Enteroclysis or a dedicated barium follow-through examination have been the mainstay of small bowel investigation for many years. Properly conducted, these procedures give excellent mucosal detail but lesions are occasionally missed because of overlapping bowel loops or poor contrast. In a recent series of enterocylses performed for the investigation of obscure gastrointestinal bleeding, the yield was approximately 20% in identifying a small bowel cause [48]. Many of these are of course tiny mucosal lesions, but some are larger tumours and CT has been advocated for their detection [49]. In these situations, CT may demonstrate a tumour, either as an area of focal bowel wall thickening or by the presence of an actual mass [50]. As in the colon, CT has the advantage of demonstrating extramucosal disease as well as evidence of distant spread. Leiomyomas, the commonest benign small bowel tumour, often demonstrate the typical "iceberg" phenomenon of a relatively small submucosal mass together with a much larger serosal component, the extent of which is best appreciated on CT. Malignant tumours of the small bowel include adenocarcinomas, lymphoma, carcinoid, leiomyosarcomas and metastases, many of which exhibit typical CT appearances [51]. Adenocarcinomas are most commonly found in the distal duodenum and proximal jejunum, with a favourite site at the duodenal/jejunal flexure. They are the commonest malignant small bowel tumours and usually involve a relatively short segment of the bowel either as a circumferential irregular thickening of the bowel wall or an eccentric mass with or without ulceration [52]. By comparison, primary non-Hodgkin's lymphoma (NHL) of the bowel usually involves the distal ileum, although it may be multifocal.

NHL presents a range of CT appearances, including localized bowel wall thickening, which tends to be concentric, with involvement of long segments or multiple luminal masses, again usually in the ileum [53] (Figure 8Go). The stomach is another recognized source with characteristic appearances of rugal thickening [54]. The stomach also attracts considerable interest because of the association between the presence of Helicobacter pylori and mucosa associated lymphoid tumour (MALT). The diagnosis of lymphoma is often helped by the presence of associated lymphadenopathy and/or splenomegaly. An interesting manifestation of lymphoma in the small bowel is aneurysmal dilatation, which, as its name suggest, results from a dilated single segment of small bowel without any obstructive element. This is due to destruction of the muscularis propria by the lymphoma.



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  		Figure 8. Lymphoma of the small bowel showing the typical thickened concentric ring appearance.

 
An understanding of the changes induced by carcinoid tumours helps with the CT diagnosis [55]. These typically arise in the ileum but it is their secondary changes involving the mesentery that are often characteristic. These usually take the form of a mass towards the root of the mesentery with extensive stranding caused by the intense desmoplastic reaction induced by a carcinoid tumour. Liver metastases complete the picture in a patient with the carcinoid syndrome. Leiomyosarcomas and other connective tissue tumours are less common and, like leiomyomas, they usually have a significant extraluminal mass, which in many cases undergoes ischaemia and necrosis, resulting in large cavities that may connect with the bowel lumen. The small bowel is commonly involved by metastatic disease either from within the abdomen (Figures 9a,bGo), such as from a pancreatic or ovarian tumour, or by haematogenous spread from breast tumour and melanoma. Melanoma deposits usually give rise to intraluminal masses with a characteristic bulls eye appearance [56], whereas breast metastases to both the small bowel and the colon tend to cause a scirrhous reaction (Figures 10a,bGo).



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  		Figure 9. Carcinoma of the rectum, which has disseminated within the abdominal cavity. Contrast study of the small bowel (a) demonstrates angulation and narrowing of a number of jejunal loops, an appearance confirmed by the CT image (b), which also shows the loculated ascites surrounding these loops.

 


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  		Figure 10. Haematogeneous spread of breast carcinoma to the colon causing the typical crenated appearance along the superior margin of the transverse colon as shown on the barium enema (a). The CT image (b) clearly shows the submucosal mass in this region (arrows).

 
CT requires optimal patient preparation with both oral and intravenous contrast agents to succeed in these situations. CT technique is important: standard 7–10 mm contiguous images through the abdomen with, as necessary, the use of further thin section collimation through regions of interest. Ideally, the bowel should be distended because partially collapsed bowel may be confused with bowel wall thickening, thus simulating a tumour. This has naturally led to the concept of combining enteroclysis with CT, as the former gives maximal small bowel distension and the latter better extramucosal anatomical information. Initially described in Germany, it attracted the title of CT Sellink in honour of one of the originators of enteroclysis [57]. Dilute contrast medium was used to distend and opacify the bowel, but a variation has been to use methylcellulose as the distending agent. A spiral run CT study after intravenous contrast medium is then able to give exquisite detail of the small intestinal wall, and encouraging results have been reported in the investigation of Crohn's disease [58]. Adding these protocols makes for a much longer procedure for operator and patient, and many patients find the passage of the tube distressing. Is it worth it? There is little doubt that performance of CT enterography without a tube is better than conventional barium studies in assessing the complications of Crohn's disease [59]. Whether more practical information is obtained by formal CT enteroclysis is not clear, but Bender et al [60] suggest that it may well have a useful role in the detailed assessment of small bowel obstruction (vide infra). The same authors note that it may be useful in detecting causes of occult blood loss from the small bowel, including the demonstration of small bowel tumours, but note that to date there has not been any study reviewing its efficacy in this respect. Logically, CT enteroclysis should be more effective but has not yet gained widespread acceptance, which may reflect the relative rarity of these particular problems.

Obstruction
The diagnosis of small bowel obstruction is often straightforward, relying on clinical history and plain radiography. The latter, however, may be inconclusive or misleading in up to 50% of cases, necessitating contrast studies to distinguish between ileus and obstruction. CT has now assumed a pivotal role in the diagnosis of small bowel obstruction as it is simple to perform and does not usually require the use of contrast agents. It relies on the demonstration of dilated air- and fluid-filled small bowel loops, together with the presence of collapsed loops distal to the site of obstruction [61]. In addition, CT is also of value in diagnosing the potential cause of obstruction, such as tumour or internal hernia, e.g. paraduodenal or obturator, the latter being only appreciated on CT [62] (Figures 11a,bGo). The commonest cause for small bowel obstruction is adhesive disease and although adhesions themselves are not usually demonstrated on CT, they can occasionally appear as bands crossing the mesentery. In addition, small bowel tethering, usually to the anterior abdominal wall, provides a further clue to the presence of adhesion [63]. Intraabdominal abscesses may also cause obstruction by involving and tethering small bowel loops (Figures 12a,bGo). Hernias, internal as well as external, account for approximately 15% of small bowel obstructions and CT is ideally placed to demonstrate these. It is thus vitally important that CT images are obtained down to the level of the symphysis pubis, so that the inguinal canal is included. Inguinal and, classically, femoral hernias may be overlooked at clinical examination, particularly in fat patients.



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  		Figure 11. Small bowel obstruction in an elderly female. The more cranial image (a) demonstrates multiple dilated loops of small bowel with characteristic air–fluid levels. The image through the lower pelvis (b) demonstrates the obturator hernia on the right, which was the cause of the obstruction. Further questioning revealed a history of pain passing down the inside of the right leg.

 


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  		Figure 12. Partial small bowel obstruction with prominent dilatation of a mid abdominal small bowel loop, but also fluid in the caecum and descending colon (a). The more caudal image through the pelvis (b) demonstrates the obstruction as being due to diverticular disease of the sigmoid (arrowheads) causing a pelvic abscess (arrows) within which the small bowel had become entangled.

 
In addition to demonstrating the site and nature of obstruction, CT has been used to assess the viability of obstructed loops, particularly in the scenario of closed loop obstruction where mortality rates can rise to 20–30% [64]. It is hoped that CT would be able to assess the need for urgent surgery as opposed to conservative treatment in some of these patients. Good results in this respect have been reported by Balthazar in his series of 100 patients. Utilizing CT signs of strangulation, which include dilated loops with thick bowel walls, a radial distribution with stretching of attached mesenteric folds and mesenteric haemorrhage, the detection rate of bowel ischaemia was 73%. The authors recommended caution in placing too much emphasis on the CT signs alone and considered that the appearances must be taken in conjunction with the clinical signs.

Trauma
Blunt abdominal trauma is a situation where CT is frequently the first imaging technique [65]. CT provides excellent evidence of small bowel perforation, and bleeding from the bowel may be demonstrated by the presence of blood in the peritoneal cavity or haematoma formation in both the wall of the bowel and the mesentery. Some of these signs may be very subtle and review of the images at different window settings is mandatory [66].

Further evidence of the sensitivity of CT in assessing visceral injuries is provided by Becker et al [67], who quote a sensitivity of 93% in the detection of these injuries, but noted that many of the quoted figures are based on relatively small series and often retrospective analysis.


   Acknowledgments
 
The author wishes to express particular thanks to Professor Adrian Dixon for all his helpful advice in the preparation of this article and for reviewing the manuscript.

Received for publication January 17, 2000. Revision received September 4, 2000. Accepted for publication September 25, 2000.


   References
Top
 Abstract
 Introduction
 The large bowel
 The small bowel
 References
 

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