the future of colorectal imaging: computed tomographic colonography

The future of colorectal imaging:computed tomographic colonography

Amy K. Hara, MDDepartment of Radiology, Mayo Clinic, 13400 East Shea Blvd.,

Scottsdale, AZ, 85259, USA

Since the introduction of ‘‘virtual colonoscopy’’ or computed tomog-

raphic colonography (CTC) in 1994, much progress in the development and

clinical testing of this technique has been performed. It is now a clinically

feasible technique, allowing the examination to be completed and inter-

preted in less than an hour. Commercial software is widely available and

it is being performed electively at many sites. Despite the increasing clinicaluse, the exact role of CTC has yet to be defined, specifically in a screening

population. This article summarizes the technique, study results, limitations,

and future issues of this evolving colon examination.

Definitions

The term two-dimensional (2D) images (multiplanar images) refers to 2Dimages that are oriented in an axial, coronal, sagittal, or oblique direction in

relation to the body or colon.

The term three-dimensional (3D) images (virtual colonoscopy) refers to

computer-rendered 3D images of the colon lumen that simulate a colono-

scopy image.

CTC [computed tomographic (CT) colography] refers to a combination

display technique utilizing 2D multiplanar and 3D endoluminal CT images

to screen for colorectal lesions (Fig. 1).

Gastroenterol Clin N Am

31 (2002) 1045–1060

E-mail address: [email protected]

0889-8553/02/$ – see front matter � 2002, Elsevier Science (USA). All rights reserved.

PII: S 0 8 8 9 - 8 5 5 3 ( 0 2 ) 0 0 0 6 0 - 2

Fig. 1. CTC: 2D multiplanar images oriented in (A) coronal, (B) sagittal, and (C) axial planes

to the colon lumen demonstrate the 9 mm polyp (arrows). (D) 3D images simulate a

colonoscopy-like view of the polyp (arrow). (E) Endoscopic image of the polyp, which was a

submucosal leiomyome (arrow).

1046 A.K. Hara / Gastroenterol Clin N Am 31 (2002) 1045–1060

Image acquisition

Patient preparation

Colon preparation

Currently, a CTC examination requires a bowel preparation, most

commonly the identical preparation as colonoscopy. The most common

preparation consists of 4 L of polyethylene glycol electrolyte solution

and two 5 mg bisacodyl tablets. Other preparations that have been usedinclude phospho-soda and magnesium citrate with cleansing enemas or

suppositories.

One small study evaluating CTC with different bowel preparations dem-

onstrated significantly less residual colonic fluid with a phospho-soda prep-

aration than a polyethylene glycol preparation [1]. Larger randomized

studies of different colon preparations, however, are needed for further eval-

uation.

An attractive possibility with CTC is a ‘‘virtual bowel preparation’’ usingoral contrast agents. See the Clinical Performance/With oral contrast (fecal

tagging) section of this article for more details.

Spasmolytic agents

Spasmolytic agents are not routinely administered for CTC mainly due to

the high cost of glucagon and its questionable benefits. One study demon-

strated no significant improvement in colon distention during CTC from

routine administration of glucagon [2]. Scopolaminebuytylbromide (Busco-

pan; Boehringer Ingelheim, Ingelheim, Germany) is another spasmolytic

drug used in Europe that is not Food and Drug Administration–approved

for use in the United States. It is much less expensive than glucagon(<$1) and, therefore, more widely used in European studies to improve

colonic distention.

Colon insufflation

The patient is typically placed in a lateral decubitus position and an

enema tip is inserted into the rectum. A retention cuff is minimally inflated

in most patients. The colon is insufflated with carbon dioxide gas or room

air. The end point of insufflation is usually approximately 1.5 L to 2.0 L

of gas or to maximal patient tolerance.

CT scanning parameters

Multidetector scanners are preferred because the entire abdomen and pel-

vis can be scanned in a single 20-second breathhold instead of multiple

breathholds needed with a single detector scanner. Although studies have

demonstrated improved colon distention and less respiratory artifacts withmultidetector scanners, no differences in lesion detection have yet been dem-

onstrated [3].

1047A.K. Hara / Gastroenterol Clin N Am 31 (2002) 1045–1060

Scanning parameters are variable between different CT scanners and

institutions. Scanning techniques have included a collimation of 3 mm or

5 mm, reconstruction intervals of 1 mm to 3 mm, and a helical pitch of 2or less. Studies have demonstrated that various combinations of these

parameters provide detection of lesions 5 mm or larger [4]. Patients are

scanned in both the supine and prone positions routinely (Fig. 2) because

it has been found that this provides better colon visualization and improved

polyp detection than supine images alone [5,6].

The radiation dose varies between studies, with milliampere levels rang-

ing from 50 mA to 250 mA. Due to the high contrast between intraluminal

colonic air and the colon wall, the milliamperes can be substantially reduced

Fig. 2. CTC is performed with prone and supine image acquisitions in order to maximize lesion

detection. (A) Supine image demonstrates a collapsed sigmoid colon. No lesions are visible. (B)

Prone image demonstrates the same region of sigmoid colon that is now air distended. The

cancer is now easily detected (arrow). (C) Endoscopic view of the cancer (arrows).


(thereby lowering the radiation dose) when evaluating exclusively for colon

lesions [7]. If using a 5 mm collimation, 3 mm reconstruction interval, and a

milliampere level of 70, the dose for supine and prone CTC is 20% lowerthan the standard dose from a double-contrast barium enema (4.53 mGy for

men and 7.45 mGy for women) [4]. It has not yet been determined, how-

ever, how much the milliampere level can be lowered when also evaluating

extracolonic structures such as the liver or when performing exams with

intravenous (IV) contrast.

Image evaluation

Hardware/software

After the patient is scanned, the images are transferred from the CT scan-

ner to an off-line computer workstation containing software for CTC. The

CTC software varies between manufacturers and no studies have yet com-

pared software performance. Generally, the software incorporates both

2D and 3D image displays of the colon. The 2D display format can include

synchronized or unsynchronized prone and supine images, as well as multi-

planar images oriented either along the colon lumen or the long axis of thepatient. Although many different 3D rendering approaches have been dis-

cussed, volume rendering is most commonly used for CTC. With the most

advanced imaging software and CT platforms, no post-processing time is

required to produce 2D and 3D images, and these images are fully interac-

tive in real time.

General approach

A combined 2D and 3D imaging approach is used for CTC. The most

common approach uses the 2D axial images displayed at lung window set-

tings for initial colon screening. Screening begins at the rectum and the

colon is followed on axial images to the cecum. An abnormality on these

images can be identified with a mouse click, and fully interactive multiplanar

2D and 3D endoluminal images are then available for further evaluation.

The 3D endoluminal images are mainly used for problem solving and notfor routine evaluation because they are more time-consuming to evaluate

and produce. Multiple studies have demonstrated that this approach detects

polyps faster and as accurately as a complete 3D endoluminal evaluation

[8,9]. In the future, with improved automation of 3D ‘‘fly-throughs’’ of the

colon, all the 3D images may be routinely evaluated during a CTC exami-

nation.

It is important to evaluate the colon at both wide and narrow window/

level settings. The lung (wide) window setting is best for polyp detection andevaluating haustral folds. The soft tissue (narrow) window setting is best for

evaluating colon wall thickness, stool and extracolonic structures (Fig. 3).


Clinical performance

Without IV contrast

The majority of studies have been performed without IV contrast (Fig. 4)

in high-risk patient populations (previous polyp, symptoms). The studies are

summarized in Table 1. The largest study (300 patients) found a sensitivityof 94% for adenomas �1 cm and 82% for adenomas between 0.5 cm and 0.9

cm. There were only 2 of 300 patients with false positive polyps �1 cm by

CTC in this study [10]. Another study of 100 patients published in the New

England Journal of Medicine demonstrated sensitivities of 100% for colorec-

tal carcinomas, 91% for polyps �1 cm, and 82% for polyps 6 mm to 9 mm

[11]. Previous studies also demonstrated similar excellent results with sensi-

tivities ranging from 83% to 100% and specificities ranging from 82% to

100% for polyps �1 cm [6,8,12–14]. Early studies without a prone acquisi-tion demonstrated a lower sensitivity (75%) and specificity (90%) for polyps

�1 cm [15].

CTC is also useful for patients with incomplete colonoscopy. The advan-

tages of CTC performed immediately after an incomplete colonoscopy are

(1) the need for only a single bowel cleansing and (2) less air insufflation

because the colon is usually already well distended. In fact, CTC may be pre-

ferred over barium enema to evaluate the proximal colon in these situations

because barium could preclude immediate surgery. In a study of CTC inpatients with obstructing carcinomas, CTC correctly identified 29 of 29

occlusive carcinomas, two of two proximal synchronous carcinomas, and

23 of 23 proximal polyps [16]. In patients with an incomplete colonoscopy,

CTC correctly identified the cause of the incomplete colonoscopy in 74% of

Fig. 3. Wide window settings are optimal for polyp detection but will underestimate cir-

cumferential tumors. (A) Wide window setting: colon wall thickness is not well appreciated.

(B) Narrow window setting: abnormal circumferential wall thickening (arrow) is now easily seen

in a patient with an ascending colon carcinoma. In addition, note the invasion of the right renal

capsule.


patients and visualized 96% of colon segments compared with 41% at colo-

noscopy [17]. This study also found that CTC detected more polyps and was

better tolerated than barium enema in the same patients [17].

All of the currently published data has been from single institutions in

high-risk populations. A multicenter trial in a screening population has been

recently completed with pending results.

With IV contrast

Recent studies have demonstrated that CTC examinations with IV con-

trast may have distinct advantages over noncontrast examinations. For

example, CTC examinations with IV contrast will enhance polyps, thereby

differentiating polyps from nonenhancing stool and polyps submerged in

Fig. 4. Infiltrating adenocarcinoma presenting as a thickened fold. (A) 2D axial image:

thickened fold in the transverse colon (arrows). (B) 3D endoluminal image: irregularly thickened

fold with abnormal surface contour is identified. (From Johnson CD, Dachman AH. CT

colonography: the next colon screening examination? Radiology 2000;216:331–341; with

permission.)

Table 1

CTC performance data for polyps �1 cm

Study

Total no.

Total no.

of polyps Sensitivity (%)Specificity

of pts �1 cm By polyp By pt by pt (%)

Yee 300 68 94 100 2 FP

Fletcher 180 121 75 85 93

Laghi 165 42 92 92 97

Fenlon 100 22 91 96 96

Royster 20 22 100 100 NA

Kay 38 11 90 82 Not reported

Dachman 44 6 83 83 100


fluid (Fig. 5). In addition, a contrast-enhanced examination allows detection

of hepatic metastases that could otherwise be missed on a noncontrast

examination. The disadvantages of IV contrast administration are risk ofa contrast reaction (0.3%) and the need for a routine CT radiation dose

instead of the lower dose used on some noncontrast CTC examinations.

Only two studies of CTC with IV contrast have been reported, but the

results are very promising. In a study of 81 patients with colonoscopic cor-

relation, IV contrast significantly increased reader confidence and the sensi-

tivity of medium-sized polyp detection (0.5–0.9 cm). Although the detection

of large polyps and masses was not statistically different, two large polyps

submerged in fluid were detected only with IV contrast administration [18].In another study of 50 patients with resected colorectal carcinoma, CTC

with IV contrast detected local recurrences with an accuracy of 94% and

identified 5 patients with metastatic disease. The only metachronous lesion,

a 4 cm tubulovillous adenoma in the cecum, was successfully identified at

CTC despite being missed on the initial colonoscopy [19].

With oral contrast (fecal tagging)

CTC examinations are not routinely done with oral contrast. The interestin developing an oral contrast regimen is to perfect fecal tagging. Fecal tag-

ging not only differentiates stool and polyps but could allow computerized

bowel cleansing, potentially eliminating the bowel preparation. With this

technique, stool appears higher attenuation (white) compared with polyps

Fig. 5. Enhanced polyp with IV contrast. (A) 2D axial image: this polyp (arrow) submerged in

fluid would have been missed without IV contrast. (B) Endoscopy image of the 4.0 cm

tubulovillous adenoma.


(gray). This is the opposite appearance when using IV contrast to differen-

tiate stool (gray) from polyps (white).

The largest study involving 56 patients found that dilute barium sulfatedrinks given in multiple doses 48 hours prior to CTC can label 75% to

98% of the colon and allow detection of 80% to 100% of polyps �1 cm

(Fig. 6) [20]. Other studies of digital subtraction bowel cleansing have been

successfully demonstrated in an animal model and in a small study of five

patients [21,22]. This method of fecal tagging with oral contrast, however,

is highly variable and not currently optimized for clinical use. In addition,

patient compliance may also be a detrimental factor.

Limitations

Stool / fluid

One of the main potential causes of both false negatives and false posi-

tives in CTC is retained stool or fluid. In examinations without IV or oral

contrast, polyps adjacent to or submerged within stool or fluid cannot be

seen. As mentioned previously, the administration of IV or oral contrastcan differentiate polyps from stool. Other features that can distinguish

stool from polyps are the presence of air within stool (Fig. 7) and move-

ment of stool/fluid to the dependent colon wall on prone and supine

imaging. Although the morphology of stool can sometimes be used to dis-

tinguish it from polyps, this is not always reliable, especially with tubulo-

villous neoplasms that often have a multilobulated and irregular contour

(Fig. 8).

Fig. 6. Oral contrast/fecal tagging: oral barium ingested before a CTC examination without IV

contrast can differentiate polyps and stool. Stool is electronically labeled purple; polyp (arrow)

remains white. (From Callstrom MR et al. CT colonography study without carthartic

preparation: feasibility study. Radiology 2001;219:693–698; with permission.)


Flat polyps

Flat polyps are more difficult to detect than sessile or pedunculated pol-

yps and have been reported numerous times as CTC false negatives [16,23].

With multidetector scanners and thinner slice collimation, however, these

lesions can now be detected. The administration of IV contrast can also

Fig. 7. Typical appearance of stool. (A) 2D image: air mixed with soft tissue attenuation

material is typical for stool (arrows). (B) 3D image: stool will simulate a pylyp/cancer on 3D

images (arrows).

Fig. 8. Villous adenoma simulating stool. (A) 2D image: irregular morphology simulates stool

(arrows). (B) 3D image: irregular morphology simulates stool (arrows). (From Johnson CD,

Dachman AH. CT colonography: the next colon screening examination? Radiology 2000;

216:331–341; with permission.)


improve detection [19] (see Fig. 5). Due to the low prevalence of these types

of lesions, however, no studies of flat lesions have yet been performed.

Collapsed colon

Any area of the colon that is collapsed can obscure lesions. With the use

of prone repositioning, adequate air distention, and a multidetector scanner,

this is a relatively infrequent cause of missed lesions. Intravenous and sub-

cutaneous glucagon has been used to improve colon distention, although

one study demonstrated no significant improvement [2].

Interpretation time

The time to interpret CTC has rapidly and steadily improved since it

was first introduced in 1994. Currently, reported times for interpretation

of a supine and prone examination range from 10 to 35 minutes [9–11,14].

It is clear that increased experience improves interpretation time. Image

processing time is now negligible using the combined 2D and 3D evalua-tion approach described previously and commercially available software.

Interpretation time may be further reduced in the future with the devel-

opment of computerized polyp detection software programs (ie, artificial

intelligence).

Extracolonic findings

Unlike the other radiologic screening test of the colon (the barium

enema), CTC has the ability to detect extracolonic disease. In a study of264 patients undergoing CTC without IV contrast, extracolonic findings

rated as high clinical importance were reported in 11% of patients [24].

Many of these findings required surgical intervention, including two previ-

ously unsuspected abdominal aortic aneuryms measuring >4 cm, two

asymptomatic renal cell adenocarcinomas (Fig. 9), a pneumothorax, and

an inguinal hernia containing bowel. This study found that extracolonic

findings of low clinical importance rarely induced further work-up,

whereas the work-up for findings of high clinical importance was oftenbeneficial and added little to the overall cost of the examination. It was also

demonstrated, however, that significant lesions in solid organs can be

missed without IV contrast. As expected, subsequent CTC studies using

IV contrast were successful in detecting solid organ masses such as hepatic

metastases [19,25].

At this time, CTC is generally offered only as a colon examination,

although the majority of radiologists routinely evaluate the extracolonic

organs. Patients should be informed that without IV contrast and at areduced radiation dose, CTC is a suboptimal screening examination of the

abdomen and pelvis.


Patient survey results

Patient preference and compliance are important factors for the success

of any screening examination. In general, CTC examinations are perceived

to be more uncomfortable by patients because they are performed without

conscious sedation, unlike colonoscopy. Studies using patient question-

naires to compare CTC and conventional colonoscopy have had varying

results, with some showing a preference for CTC [26] and others for colonos-

copy [27]. Although the final preferences of these studies differ, both dem-

onstrate that the majority of CTC examinations cause minimal to nodiscomfort. Other factors than discomfort that can influence patient prefer-

ence include examination cost, convenience, risks of radiation, sedation or

colon perforation, and the ability to be treated and diagnosed with a single

test. Another study based on questionnaires sent to 323 potential patients

found that potential patients preferred CTC over colonoscopy (60% to

26%) and 82% would comply more with colon cancer screening recommen-

dations if CTC were available [28].

Computer-aided diagnosis

Computer-aided diagnosis for CTC could potentially decrease radiologist

interpretation time and increase diagnostic accuracy. The research in this

area is preliminary but promising. One automated detection program basedon volumetric features demonstrated 100% (18/18) sensitivity for polyps �5

mm using supine and prone images with 2.5 false positives per patient [29].

Using supine images only and a shape-based detection algorithm, another

study found a 64% (18/28) sensitivity for polyps �1 cm with six false posi-

tives per patient (Fig. 10). Sensitivity would likely be higher if prone images

were also evaluated [30].

Fig. 9. Extracolonic findings: asymptomatic left renal cell carcinoma (arrow) incidentally

discovered at noncontrast low-dose CTC.


Comparison with other imaging techniques

No direct comparative studies between barium enema and CTC have yet

been performed; however, CTC has some definite advantages. These advan-

tages include the absence of overlapping structures on the image (a source of

perceptive errors), a more uniform image acquisition technique, the ability

to evaluate extracolonic structures, a faster imaging time, no need to coat

the colon for adequate evaluation, and elimination of a second colon cleans-

ing prior to surgery. In addition, the examination is better tolerated by some

patients because they do not have to retain barium or be placed in multiplepositions during the examination.

Magnetic resonance colonography (MRC) is similar in many ways to

CTC. It can evaluate extracolonic tissues and depict the colon in a multipla-

nar technique. The main advantage of MRC is the lack of ionizing radia-

tion; however, this is of limited value in the older screening population

for colorectal cancer. MRC requires a liquid (gadolinium or water) instead

of air enema, similar to the barium enema. In addition, MRC gives IV con-

trast as do some CTC examinations. The largest study of 132 patients with27 lesions �1 cm demonstrated a sensitivity of 93%, a specificity of 99%, a

positive predictive value of 92%, and a negative predictive value of 98% for

these large lesions [31]. A more recent study demonstrated the feasibility of

fecal tagging (eliminating the bowel cleansing) with MRC in a small number

of patients [32]. MRC and CTC use similar techniques for fecal tagging,

which require a lengthy preparation period of 36 to 48 hours.

MRC is still in the early stages of evaluation and may be a useful alter-

native when concerns for radiation exposure are present. In general, how-ever, CTC is currently more widely available and less expensive to perform.

Fig. 10. Automated polyp dectection. (A) CTC with computer algorithm for automated polyp

detection: polyp labeled red (arrows). (B) Endoscopic image: 1.5 cm pedunculated polyp

(arrows). (From Summers RM et al. Automated polyp detection at CT colonography: feasibility

assessment in a human population. Radiology 2001;219:51–9; with permission.)


Other considerations

Cost of CTC

The cost of CTC and coverage by third-party payers remain undecided

and could have an enormous impact on usage rates. Based on economic

modeling, some have concluded that to become cost effective and competi-

tive with colonoscopy for colorectal cancer screening, CTC must be associ-

ated with a compliance rate 15% to 20% better than or procedure costsroughly 50% less than colonoscopy [33].

CTC as part of total body CT scanning

Although controversial at present [34], total body CT scanning is widely

available to screen for cancers in multiple organ systems and health-threat-

ening but nonmalignant disease such as osteoporosis, coronary artery calci-

fication, or vascular aneurysms. Outcome studies are needed to establish thevalue of screening in the asymptomatic population and the effect on health

costs. If total body CT scanning is incorporated into the periodic health

examination in the future, then CTC would become an especially rational

and patient-friendly strategy for colorectal cancer screening. This ‘‘one-stop

shop’’ would allow screening of the lung, heart, colon, and abdomen with

one CT scan. If a polyp is found at CTC, then the patient could have

same-day colonoscopy; therefore, patients would only require one colon

preparation. Also, if a lesion suspicious for colon cancer is identified, thenthe patient could immediately be given IV contrast to evaluate for hepatic

metastases.

Summary

The development of colorectal cancer screening alternatives that are

attractive to patients and effective for screening is critical for reducing this

too-common and deadly disease. CTC is an exciting technique that is the

only imaging alternative developed since the barium enema for colon screen-

ing. In the past few years, many obstacles to clinical implementation of CTChave been eliminated. For example, there is no longer any post-processing

time, which was previously as long as 8 to 10 hours, and the interpretation

time has been drastically reduced from 4 hours to 15 to 20 minutes. The

majority of studies have demonstrated excellent results for detection of

lesions �1 cm, with few false positives. This examination will continue to

improve with the development of automated (computer) detection programs

and automated 3D rendering algorithms. In addition, cathartic bowel prep-

aration, one of the biggest obstacles to patient compliance with colorec-tal cancer screening, may be eliminated if successful fecal tagging can be

developed. The most important issue that remains is its performance in a


screening population, and studies are currently underway to answer that

important question.

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the future of colorectal imaging: computed tomographic colonography

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