DOI:10.2214/AJR.07.2099
AJR 2008; 190:374-385
© American Roentgen Ray Society
Critical Analysis of the Performance of Double-Contrast Barium Enema for Detecting Colorectal Polyps
6 mm in the Era of CT Colonography
Jacob Sosna1,2,
Tamar Sella1,
Oumar Sy3,
Philip T. Lavin3,
Ruth Eliahou1,
Shifra Fraifeld1 and
Eugene Libson1
1 Department of Radiology, Hadassah Hebrew University Medical Center, POB 12000,
Jerusalem, Israel.
2 Department of Radiology, Beth Israel Deaconess Medical Center, Boston,
MA.
3 Boston Biostatistics Research Foundation, Framingham, MA.
Received February 21, 2007;
accepted after revision September 9, 2007.
Address correspondence to J. Sosna
(jacobs{at}hadassah.org.il).
Abstract
OBJECTIVE. The purpose of our study was to perform a meta-analysis
comparing the performance of double-contrast barium enema (DCBE) with CT
colonography (CTC) for the detection of colorectal polyps
6 mm using
endoscopy as the gold standard.
MATERIALS AND METHODS. Prospective DCBE and CTC studies were
identified. Percentages of polyps and of patients with polyps
10 mm and
6–9 mm were abstracted. The performance of DCBE versus CTC was
determined by separately evaluating each technique's performance versus that
of endoscopy, and contrasting the techniques. The I-squared statistic and
Fisher's exact test were used for heterogeneity, the Cochran-Mantel-Haenszel
and the Kruskal-Wallis tests for correlation, and the Az
test for comparing pooled weighted estimates of performance.
RESULTS. Eleven studies of DCBE (5,995 patients, 1,548 polyps) and
30 studies of CTC (6,573 patients, 2,348 polyps) fulfilled inclusion criteria.
For polyps
10 mm, a 0.121-perpatient sensitivity difference favored CTC
(p < 0.0001; DCBE, 0.702 [95% CI, 0.687–0.715]; CTC, 0.823
[0.809–0.836]). For polyps
10 mm, a 0.031-per-polyp sensitivity
difference favored CTC (p < 0.0001; DCBE, 0.715
[0.703–0.726]; CTC, 0.746 [0.735–0.757]). For polyps
10 mm, a
specificity difference of 0.104 favored CTC (p = 0.001; DCBE, 0.850
[0.847–0.855]; CTC, 0.954 [0.952–0.955]). DCBE was also
significantly less sensitive for 6- to 9-mm polyps (p <
0.001).
CONCLUSION. DCBE has statistically lower sensitivity and specificity
than CTC for detecting colorectal polyps
6 mm.
Keywords: barium enema colonoscopy CT colonography double-contrast barium enema meta-analysis virtual colonoscopy
Introduction
Colorectal cancer is the second leading cause of death from cancer in the
United States, with a 6% lifetime risk of disease
[1]. Routine screening for
malignancies and adenomatous polyps is recommended to begin at the age of 50
years, or at a younger age for those at higher risk
[2–5].
Effective screening can greatly reduce colorectal cancer morbidity and
mortality
[6–8];
however, only 30–45% of those for whom screening is recommended comply
with guidelines [9].
Potential screening options for colorectal cancer include fecal occult
blood testing, flexible sigmoidoscopy, conventional colonoscopy, and
double-contrast barium enema (DCBE). Although DCBE is an accepted and
reimbursed screening method for colorectal cancer, published evidence from
controlled studies examining the accuracy of this method is limited.
CT colonography (CTC), or virtual colonoscopy, was introduced in 1994
[10]. CTC has the potential to
increase compliance because it is perceived to be more tolerable for patients
and may have fewer associated complications than conventional colonoscopy
[11–13].
However, the U.S. Preventive Services Task Force found insufficient evidence
to conclude that CTC improves health outcomes and determined that rigorous
studies must precede the acceptance of CTC as a routine screening tool
[5]. The recent American
Gastroenterological Association position paper stated that CTC is indicated
only for incomplete colonoscopy but in the future may become an accepted
screening technique [14].
Thus, CTC is considered an evolving technique pending results from multicenter
trials.
DCBE needs to be reevaluated with comparable rigor because previous studies
have questioned its performance
[15]. Although several CTC
meta-analyses have been published, to our knowledge no meta-analysis addresses
DCBE performance. The purpose of this study was to perform a meta-analysis of
the sensitivity and specificity of DCBE for the detection of colorectal polyps
6 mm in comparison with CTC, using endoscopy as the gold standard.
Materials and Methods
This study did not involve human subjects directly and was exempt from
institutional review board approval.
Data Sources and Literature Search
A comprehensive literature search of English-language studies was performed
using the PubMed, MEDLINE, and EMBRACE databases, and the Cochrane Controlled
Trials registry. DCBE keywords were double-contrast barium enema, barium
enema, and pneumocolon. CTC articles were identified using the keywords CT
colonography, CT colonoscopy, virtual colonoscopy, and CT pneumocolon.
Searches included peer-reviewed DCBE studies published from January 1960
through December 2006, and CTC studies published from January 1994 through
December 2006. Review articles, letters, comments, articles without original
data, conference abstracts, and secondary presentations were excluded.
Study Eligibility
All DCBE and CTC studies included in the analysis were prospective.
Additional DCBE study inclusion criteria were full colorectal preparation when
air and barium were used to reveal colon segments, both spot and overhead
films, evaluation of the entire colon, full conventional colonoscopy or
sigmoidoscopy as the reference standard, DCBE reader blinding to the results
of conventional colonoscopy or sigmoidoscopy, and reports of performance in
absolute numbers and in percentages for polyps or masses of different sizes.
Comparisons between flexible sigmoidoscopy and DCBE were made only in the
rectum and sigmoid colon.
CTC study inclusion criteria were based on the CTC consensus document
[16]. Additional CTC inclusion
criteria were full colorectal preparation when the entire colon was evaluated,
full conventional colonoscopy as the reference standard (with or without
segmental unblinding), CTC reader blinding to the results of conventional
colonoscopy, CTC performed with the patient in both the prone and supine
positions after the insufflation of air or CO2, at least a
single-detector CT scanner, slice thickness
5 mm, both 2D and 3D (full or
partial) readings, and reports of performance in absolute numbers and in
percentages for polyps or masses of different sizes. In some studies, these
criteria were fulfilled with only a subgroup of patients, and findings for
other groups were excluded from the analysis.
Studies in which IV iodinated contrast material was routinely administered
to all patients were excluded because contrast material is not used
consistently in colorectal cancer screening programs. We also excluded studies
of which the primary aim was evaluating ultralow radiation dose, those with no
or minimal colonic preparation, and studies evaluating computer-aided
detection because these techniques are still experimental. When adenomas or
the total amount of polyps were presented, the larger number was used. When
two or more readers assessed the same study population, the average of their
findings was used (Table
1).
View this table:
[in this window]
[in a new window]
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TABLE 1: Studies Comparing Performance of Double-Contrast Barium Enema with
Colonoscopy or Sigmoidoscopy and CT Colonography (CTC) with Colonoscopy, for
Diagnosis of Polyps 6 mm
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Data Extraction
The meta-analysis was performed in compliance with QUORUM (Quality of
Reporting of Meta-Analyses) guidelines
[17]. Two investigators
extracted the data from each article separately, with disagreements resolved
by consensus. Included studies were randomly sorted for data extraction, and
only the first author, year of publication, sample size, and patient risk were
recorded in the data sheet. Patients with symptoms or a history of colorectal
neoplasia, those under surveillance, and those with positive findings on a
previous screening test were considered high risk. DCBE and CTC technique, the
experience of radiologists and the protocol for interpreting imaging studies,
the number of patients per study, number of lesions detected by diameter (
10 mm, 6–9 mm), number of patients in whom lesions of these size
categories were detected, and specificity for detection of polyps
10 mm
were recorded for each study. End points were per-polyp and per-patient
sensitivity for DCBE or CTC, and specificity for polyps
10 mm.
Statistical Analysis
The relative performance of DCBE and CTC was determined by separately
evaluating each technique's sensitivity and specificity in comparison with
endoscopy on the basis of the pooled weighted results of the relevant series
of studies, and then contrasting DCBE and CTC outcomes.
To determine whether data could be pooled across studies, the I-squared
statistic and Fisher's exact test were used to assess heterogeneity within the
DCBE and CTC series at each study end point. I-squared statistic values range
from 0% to 100%, with smaller values indicating higher homogeneity and larger
values indicating greater heterogeneity.
For each diagnostic technique, pooled specificity and sensitivity were
estimated, weighted and unweighted by study size, and 95% CIs were computed.
The relationship between polyp size and sensitivity was assessed for each
technique using the Cochran-Mantel-Haenszel and the Kruskal-Wallis tests.
Analyses comparing pooled weighted estimates of DCBE and CTC outcomes were
generated. The Az test comparing two independent population
proportions was used because the specificity and sensitivity end points were
both proportions, and the DCBE and CTC samples of articles were independent. A
p value of < 0.05 was considered significant.
Results
Literature Search
We retrieved 662 original articles addressing all aspects of DCBE from the
databases; 11 fulfilled inclusion criteria
[15,
18–27]
(Table 1). Thirty studies were
excluded because they were retrospective (n = 23)
[28–50],
compared techniques for a portion of patients rather than providing separate
results for all parts (n = 5)
[26,
51–54],
did not mention absolute numbers (n = 1)
[55], or involved children
(n = 1) [56].
We retrieved 636 original articles addressing all aspects of CTC; 30
fulfilled inclusion criteria
[11,
20,
57–82]
(Table 1). Thirty-three studies
were excluded because of overlap of published results (n = 3)
[83–85],
frequent IV contrast use (n = 6)
[71,
86–90],
single scanning position (n = 7)
[91–97],
minimal or no preparation (n = 6)
[98–103],
computer-aided detection (n = 4)
[96,
104–106],
ultralow radiation dose (n = 5)
[107–111],
or a small patient series (n = 2)
[112,
113].
Two articles comparing DCBE and CTC in the same population of patients were
included [20,
77]. In these studies,
findings for each imaging method were analyzed separately and thus could be
added to the cumulative experience for each technique.
No DCBE study involved 50 or fewer subjects, six (55%) had 51–500
patients, and five (45%) had more than 500. Six studies (55%) involved only
high-risk patients, one study (9%) included a mixture of average- and
high-risk patients, one study (9%) included average-risk patients, and three
(27%) studies provided no information regarding patient selection.
Conventional colonoscopy was the reference standard in five studies (46%),
sigmoidoscopy in four (36%), and both conventional colonoscopy and
sigmoidoscopy in two studies (18%).
Six of 30 CTC studies (20%) had 50 subjects or fewer, 19 (63.3%) had
51–500 patients, and five (17%) had more than 500. Six studies (20%)
included only average-risk patients or a combination of high- and
average-risk, and 24 (80%) included only high-risk patients. In 14 studies
(53.3%), some or all patients were evaluated with MDCT scanners.
Data Synthesis
DCBE—A total of 5,995 patients were included in the 11
articles analyzed. In this population, 970 polyps were detected by
conventional colonoscopy, including 549 polyps
10 mm in diameter and 421
polyps of 6–9 mm. Specific data for each article are given in
Table 2.
Pooling appropriateness tests for sensitivity and specificity analysis of
DCBE studies yielded p < 0.001 for the Fisher's exact test on all
end points except per-patient sensitivity for polyps 6–9 mm, for which
the p value was 0.268. I-squared values ranged from 81.46% for
per-patient sensitivity for polyps 6–9 mm to 96.01% for specificity.
I-squared values could not be calculated for per-patient sensitivity for
polyps
5 mm. Pooled study results, both unweighted and weighted by study
size, are provided in Table
3.
Data analysis of trend using the Cochran-Mantel-Haenszel test showed
increasing per-patient (p < 0.0001) and per-polyp (p =
0.0048) sensitivity for polyp detection with increasing polyp size. The
Kruskal-Wallis tests for per-patient and per-polyp sensitivity trends as polyp
size increased were not significant, with p values of 0.2765 and
0.2291, respectively.
CTC—A total of 6,673 patients were included in the 30 CTC
articles analyzed. At conventional colonoscopy, 2,348 polyps were detected,
including 925 polyps with diameters
10 mm and 1,423 polyps of 6–9
mm. Specific data for each article are given in
Table 2. Tests for pooling
appropriateness yielded p < 0.001 using the Fisher's exact test.
I-squared values varied from 47.6% for per-polyp specificity for polyps
10 mm to 81.13% per-polyp sensitivity for polyps
10 mm, and 74.91%
per-patient sensitivity for polyps
10 mm. Pooled CTC study results, both
unweighted and weighted by study size, are provided in
Table 3.
Data analysis of trend using the Cochran-Mantel-Haenszel test showed
increasing perpatient and per-polyp sensitivity with increasing polyp size
(p < 0.0001). The Kruskal-Wallis test confirmed these
findings.
Comparison of CTC and DCBE—Estimates comparing pooled DCBE
performance with pooled CTC performance showed significant differences in
favor of CTC for specificity and per-polyp sensitivity in polyps
6 mm
(Table 4).
Discussion
Although DCBE is an accepted and widely used technique, we could retrieve
only 11 prospective studies comparing DCBE with conventional colonoscopy or
sigmoidoscopy, even when the search was extended back to 1960. Of interest is
the relatively small number of prospective studies addressing DCBE
performance. In fact, studies that used sigmoidoscopy as the reference
standard were included to increase the number of studies analyzed. We
attributed the relatively small number of prospective DCBE studies in
comparison with CTC to rising methodologic standards in recent years. The
routine use of less demanding methods in previous years resulted in 24
retrospective DCBE studies. No DCBE study published before 1982 was
prospective. We decided not to use retrospective studies even though their use
would have increased considerably the number of studies analyzed. Data
gathering and analysis vary greatly in retrospective and prospective studies,
and including retrospective studies could increase heterogeneity of the pooled
data. Indeed, tighter acceptance criteria for CTC studies in our analysis led
to greater homogeneity in our data compared with other meta-analyses, as
pointed out later. DCBE was assessed rather than single-contrast barium enema
because DCBE is the more widely accepted technique for radiologic imaging of
the large bowel.
The 30 CTC articles analyzed in this study emanate from a variety of groups
that have used CTC over the past 13 years. Acceptance criteria for CTC studies
included dual positioning,
5-mm slice thickness, 2D and 3D reading, and
use of a single-detector or preferably MDCT scanner. Techniques in the studies
differ for technical factors such as section width and reconstruction
interval. We decided to include only studies with section width
5 mm,
which provides acceptable thickness
[114], although thinner
collimation is optimal and has been shown to improve performance. Tube current
was also variable. Although ultralow tube currents have been shown to have
good diagnostic yield, they were excluded from the analysis because they are
not yet used routinely for CTC studies
[107–110].
Although IV contrast material may increase CTC sensitivity for medium-sized
polyps [115], we also
excluded articles in which contrast material was administered because it would
not be routinely used for screening.
This analysis showed more heterogeneity in sensitivity and specificity
measures among DCBE studies and more homogeneity among CTC studies. Whereas
DCBE heterogeneity was greater than 80% for all end points, heterogeneity was
47% for CTC specificity and 74% for CTC per-patient sensitivity to polyps
10 mm in diameter. Although heterogeneity is higher for DCBE, we did not
specifically aim to determine the sources of heterogeneity in the relatively
small number of DCBE studies. For CTC, the most important parameters for
population-based decisions—for example, test specificity and perpatient
sensitivity of the clinically important finding (polyps
10 mm)—are
at lower but potentially acceptable levels compared with conventional
colonoscopy.
DCBE had lower performance levels, with specificity of 0.850 and
per-patient sensitivity for larger polyps of 0.702. On the other hand, the
meta-analysis showed that CTC has a very good specificity for polyps
10
mm (0.954) and good per-patient sensitivity (0.823). The difference was
statistically significant.
On the basis of our results, CTC has a very good record for specificity.
Extrapolation of our findings to a population of 1,000 patients, including 50
patients with polyps
10 mm (5% prevalence), would result in six more
underdiagnosed cases on DCBE (35 true-positive polyps of 50 patients with
polyps) than on CTC (41 true-positive polyps). Although some of these polyps
could be diagnosed in subsequent screening studies, it seems likely that some
of these missed polyps might be diagnosed as malignancies at a later stage
when interventions are less effective. We believe that the primary end point
in screening is indeed detection of patients with polyps and that sensitivity
should be as high as possible. According to our findings, DCBE would also
result in 90 more overdiagnosed cases (138 false-positive cases on DCBE
compared with 48 at CTC), leading to unnecessary biopsies, higher costs, and
greater uncertainty for patients and their families.
The true goal in screening is to reduce the morbidity and mortality rates
of colorectal cancer. As always, this goal is balanced against financial
requirements and potential harm to the patient. Nevertheless, high-risk
adenomas, and even some early cancers, are surrogate end points that may have
no influence on true patient outcome. Most high-risk adenomas will never
progress to cancer. Thus, the statistical differences found in our study need
ultimate verification in long-term studies addressing the end point of
mortality associated with colorectal cancer.
Pooled CTC sensitivity and specificity in this analysis are comparable to
those in previously published CTC meta-analyses
[114,
116,
117], with less
heterogeneity. This may be partially explained by stricter inclusion criteria
in this study, which resulted in a smaller number of included articles (e.g.,
30 studies in this analysis vs 33 in the metaanalysis by Mulhall et al.
[114]).
The reports we analyzed included mostly high-risk patients. There were more
polyps per patient in the CTC than the DCBE studies, which may partly explain
improved CTC performance because higher prevalence affects and increases
positive predictive value. However, this is unlikely to be the sole
explanation for the better performance of CTC because high-risk patients
represented the majority in both groups.
Although DCBE is widely considered an acceptable screening method for
colorectal cancer, our findings indicate that it may be less specific and less
sensitive than CTC for detection of polyps
6 mm. Although meta-analysis
does not replace large prospective clinical trials, reports have shown that
findings based on analysis of pooled data of a series of smaller studies do
not differ significantly from outcomes of large trials
[118,
119]. And although CTC is not
recommended for screening, the results of this analysis suggest that CTC may
be considered at least as effective as DCBE. Although short-term results of
CTC used in a screening population with third-party coverage were recently
published [120], further
studies should be performed to address the economic aspects and radiation
considerations of the widespread use of CTC as a reimbursable screening tool.
CTC has the added benefit of evaluating extracolonic organs
[121,
122].
Conventional colonoscopy performed with video endoscopy, as in recent
years, may be more sensitive than it was in the 1980s, when fiberoptic viewing
was standard. Thus, the relative performance of DCBE compared with
conventional colonoscopy in earlier studies may not accurately represent the
relative performance today, given the recent improvement in conventional
colonoscopy sensitivity. More than half of the DCBE studies focused on the
rectum and sigmoid because flexible sigmoidoscopy was the standard of
reference. DCBE is known to be least accurate in these colon segments,
possibly skewing data downward. However, prevalence of polyps in these regions
is also higher, which may limit a possible reduction in patient sensitivity
and specificity.
Limitations of our study may include an inherent publication bias, because
studies that show positive effect tend to be published more often than those
that do not [123]. There is
also a possible tendency to publish studies with positive results of newer
technologies (e.g., CTC) compared with older techniques (DCBE), which are
considered less attractive for research. In addition, several weakly positive
studies may add to a strong positive result when pooled. A rich delineation of
possible sources of heterogeneity requires a more sensitive technique than
meta-analysis. We included information on study characteristics, but our
ability to discriminate sources of heterogeneity was limited. We also could
not evaluate other factors, such as the impact of varying expertise among
radiologists reading CTC studies and the notion that younger radiologists are
less trained in the performance and interpretation of DCBE. We think that the
main reason for the slow demise of DCBE is low reimbursement and the lack of
radiologists who are adequately trained in this technique. When properly
performed, DCBE remains a cost-effective clinical tool. Even though DCBE is
performed with deceasing frequency, it is still a reimbursable technique that
is used in common practice by radiologists worldwide and by technologists in
some countries such as the United Kingdom.
In conclusion, despite its widespread use, scientific data on the overall
performance of DCBE compared with CTC are limited. Our study suggests that
DCBE has lower sensitivity and specificity than CTC for detecting polyps
6 mm, with the difference being statistically significant.
References
- Cancer facts and figures 2006. American Cancer Society Website.
Available at
www.cancer.org.
Updated 2007. Accessed July 2, 2007
- Rex DK, Johnson DA, Lieberman DA, Burt RW, Sonnenberg A. Colorectal
cancer prevention 2000: screening recommendations of the American College of
Gastroenterology. American College of Gastroenterology. Am J
Gastroenterol 2000; 95:868
–877[Medline]
- Smith RA, Cokkinides V, Eyre HJ. American Cancer Society guidelines
for the early detection of cancer, 2004. CA Cancer J
Clin 2004; 54:41
–52[Abstract/Free Full Text]
- Winawer SJ, Fletcher RH, Miller L, et al. Colorectal cancer
screening: clinical guidelines and rationale.
Gastroenterology 1997;112
: 594–642[CrossRef][Medline]
- Pignone M, Rich M, Teutsch SM, Berg AO, Lohr KN. Screening for
colorectal cancer in adults at average risk: a summary of the evidence for the
U.S. Preventive Services Task Force. Ann Intern Med2002; 137:132
–141[Abstract/Free Full Text]
- Wagner J, Tunis S, Brown M, Ching A, Almeda R. The
cost-effectiveness of colorectal cancer screening in average risk adults. In:
Young G, Levin B, eds. Prevention and early detection of colorectal
cancer. Philadelphia, PA: Saunders, 1996:321
–356
- Winawer SJ, Flehinger BJ, Schottenfeld D, Miller DG. Screening for
colorectal cancer with fecal occult blood testing and sigmoidoscopy.
J Natl Cancer Inst 1993;85
:1311
–1318[Abstract/Free Full Text]
- Winawer SJ, Zauber AG, Ho MN, et al. Prevention of colorectal
cancer by colonoscopic polypectomy. The National Polyp Study Workgroup.
N Engl J Med 1993;329
:1977
–1981[Abstract/Free Full Text]
- Ioannou GN, Chapko MK, Dominitz JA. Predictors of colorectal cancer
screening participation in the United States. Am J
Gastroenterol 2003; 98:2082
–2091[CrossRef][Medline]
- Vining DJ, Gelfand DW, Bechtold RE, Scharling ES, Grishaw EK,
Shifrin RY. Technical feasibility of colon imaging with helical CT and virtual
reality. (abstr) AJR 1994;162
[American Roentgen Ray Society 94th Annual
Meeting Program Book suppl]: 104
- Van Gelder RE, Nio CY, Florie J, et al. Computed tomographic
colonography compared with colonoscopy in patients at increased risk for
colorectal cancer. Gastroenterology 2004;127
: 41–48[CrossRef][Medline]
- Burling D, Halligan S, Slater A, Noakes MJ, Taylor SA. Potentially
serious adverse events at CT colonography in symptomatic patients: national
survey of the United Kingdom. Radiology2006; 239:464
–471[Abstract/Free Full Text]
- Sosna J, Sella T, Bar-Ziv J, Libson E. Perforation of the colon and
rectum: a newly recognized complication of CT colonography. Semin
Ultrasound CT MR 2006; 27:161
–165[CrossRef][Medline]
- AGA Clinical Pratice and Economics Committee. Position of the
American Gastroenterological Association (AGA) Institute on computed
tomographic colonography. Gastroenterology2006; 131:1627
–1628[CrossRef][Medline]
- Winawer SJ, Stewart ET, Zauber AG, et al. A comparison of
colonoscopy and double-contrast barium enema for surveillance after
polypectomy. National Polyp Study Work Group. N Engl J
Med 2000; 342:1766
–1772[Abstract/Free Full Text]
- Zalis ME, Barish MA, Choi JR, et al. CT colonography reporting and
data system: a consensus proposal. Radiology2005; 236:3
–9[Free Full Text]
- Moher D, Cook DJ, Eastwood S, Olkin I, Rennie D, Stroup DF.
Improving the quality of reports of meta-analyses of randomised controlled
trials: the QUOROM statement. Quality of Reporting of Meta-analyses.
Lancet 1999; 354:1896
–1900[CrossRef][Medline]
- Farrands PA, Vellacott KD, Amar SS, Balfour TW, Hardcastle JD.
Flexible fiberoptic sigmoidoscopy and double-contrast barium-enema examination
in the identification of adenomas and carcinoma of the colon. Dis
Colon Rectum 1983; 26:725
–727[CrossRef][Medline]
- Jensen J, Kewenter J, Haglind E, Lycke G, Svensson C, Ahren C.
Diagnostic accuracy of double-contrast enema and rectosigmoidoscopy in
connection with faecal occult blood testing for the detection of rectosigmoid
neoplasms. Br J Surg 1986;73
: 961–964[Medline]
- Johnson CD, MacCarty RL, Welch TJ, et al. Comparison of the
relative sensitivity of CT colonography and double-contrast barium enema for
screen detection of colorectal polyps. Clin Gastroenterol
Hepatol 2004; 2:314
–321[CrossRef][Medline]
- Kewenter J, Brevinge H, Engaras B, Haglind E. The yield of flexible
sigmoidoscopy and double-contrast barium enema in the diagnosis of neoplasms
in the large bowel in patients with a positive Hemoccult test.
Endoscopy 1995;27
: 159–163[Medline]
- Rex DK, Lehman GA, Lappas JC, Miller RE. Sensitivity of
double-contrast barium study for left-colon polyps.
Radiology 1986;158
: 69–72[Abstract/Free Full Text]
- Rockey DC, Koch J, Yee J, McQuaid KR, Halvorsen RA. Prospective
comparison of air-contrast barium enema and colonoscopy in patients with fecal
occult blood: a pilot study. Gastrointest Endosc2004; 60:953
–958[CrossRef][Medline]
- Saito Y, Slezak P, Rubio C. The diagnostic value of combining
flexible sigmoidoscopy and double-contrast barium enema as a one-stage
procedure. Gastrointest Radiol 1989;14
: 357–359[CrossRef][Medline]
- Steine S, Stordahl A, Lunde OC, Loken K, Laerum E. Double-contrast
barium enema versus colonoscopy in the diagnosis of neoplastic disorders:
aspects of decision-making in general practice. Fam
Pract 1993; 10:288
–291[Abstract/Free Full Text]
- Thoeni RF, Petras A. Double-contrast bariumenema examination and
endoscopy in the detection of polypoid lesions in the cecum and ascending
colon. Radiology 1982;144
: 257–260[Abstract/Free Full Text]
- Williams CB, Macrae FA, Bartram CI. A prospective study of
diagnostic methods in adenoma follow-up. Endoscopy1982; 14:74
–78[Medline]
- Anderson N, Cook HB, Coates R. Colonoscopically detected colorectal
cancer missed on barium enema. Gastrointest Radiol1991; 16:123
–127[CrossRef][Medline]
- Bloomfield JA. Reliability of barium enema in detecting colonic
neoplasia. Med J Aust 1981;1
: 631–633[Medline]
- Brewster NT, Grieve DC, Saunders JH. Double-contrast barium enema
and flexible sigmoidoscopy for routine colonic investigation. Br J
Surg 1994; 81:445
–447[Medline]
- Connolly DJ, Traill ZC, Reid HS, Copley SJ, Nolan DJ. The double
contrast barium enema: a retrospective single centre audit of the detection of
colorectal carcinomas. Clin Radiol 2002;57
: 29–32[CrossRef][Medline]
- Culpan DG, Mitchell AJ, Hughes S, Nutman M, Chapman AH. Double
contrast barium enema sensitivity: a comparison of studies by radiographers
and radiologists. Clin Radiol 2002;57
: 604–607[CrossRef][Medline]
- Gillespie JS, Kelly BE. Double contrast barium enema and colorectal
carcinoma: sensitivity and potential role in screening. Ulster Med
J 2001; 70:15
–18[Medline]
- Johnson CD, Carlson HC, Taylor WF, Weiland LP. Barium enemas of
carcinoma of the colon: sensitivity of double- and single-contrast studies.
AJR 1983; 140:1143
–1149[Abstract/Free Full Text]
- Law RL, Longstaff AJ, Slack N. A retrospective 5-year study on the
accuracy of the barium enema examination performed by radiographers.
Clin Radiol 1999;54
: 80–83; discussion
83–84[CrossRef][Medline]
- Morosi C, Ballardini G, Pisani P, et al. Diagnostic accuracy of the
double-contrast enema for colonic polyps in patients with or without
diverticular disease. Gastrointest Radiol1991; 16:345
–347[CrossRef][Medline]
- Myllylä V, Päivänsalo M, Laitinen S. Sensitivity of
single and double contrast barium enema in the detection of colorectal
carcinoma. Rofo 1984;140
: 393–397[Medline]
- Ott DJ, Gelfand DW, Wu WC, Kerr RM. Sensitivity of double-contrast
barium enema: emphasis on polyp detection. AJR1980; 135:327
–330[Abstract]
- Ott DJ, Gelfand DW, Wu WC, Munitz HA, Chen YM. How important is
radiographic detection of diminutive polyps of the colon?
AJR 1986; 146:875
–878[Free Full Text]
- Ott DJ, Scharling ES, Chen YM, Gelfand DW, Wu WC. Positive
predictive value and posttest probability of diagnosis of colonic polyp on
single- and double-contrast barium enema. AJR1989; 153:735
–739[Abstract/Free Full Text]
- Ott DJ, Scharling ES, Chen YM, Wu WC, Gelfand DW. Barium enema
examination: sensitivity in detecting colonic polyps and carcinomas.
South Med J 1989;82
: 197–200[Medline]
- Ferrucci JT. Double-contrast barium enema: use in practice and
implications for CT colonography. AJR 2006;187
: 170–173[Abstract/Free Full Text]
- Kung JW, Levine MS, Glick SN, Lakhani P, Rubesin SE, Laufer I.
Colorectal cancer: screening double-contrast barium enema examination in
average-risk adults older than 50 years. Radiology2006; 240:725
–735[Abstract/Free Full Text]
- Rex DK, Cutler CS, Lemmel GT, et al. Colonoscopic miss rates of
adenomas determined by back-to-back colonoscopies.
Gastroenterology 1997;112
: 24–28[CrossRef][Medline]
- Smith GA, O'Dwyer PJ. Sensitivity of double contrast barium enema
and colonoscopy for the detection of colorectal neoplasms. Surg
Endosc 2001; 15:649
–652[CrossRef][Medline]
- Stefansson T, Bergman A, Ekbom A, Nyman R, Pahlman L. Accuracy of
double contrast barium enema and sigmoidoscopy in the detection of polyps in
patients with diverticulosis. Acta Radiol1994; 35:442
–446[Medline]
- Tawn DJ, Squire CJ, Mohammed MA, Adam EJ. National audit of the
sensitivity of double-contrast barium enema for colorectal carcinoma, using
control charts. For the Royal College of Radiologists Clinical Radiology Audit
Sub-Committee. Clin Radiol 2005;60
: 558–564[CrossRef][Medline]
- Wafula JM. Diagnostic yield from barium enemas: a study among
patients referred by general practitioners and hospital outpatient
departments. Br J Gen Pract 1992;42
: 330–332[Medline]
- Warden MJ, Petrelli NJ, Herrera L, Mittelman A. Endoscopy versus
double-contrast barium enema in the evaluation of patients with symptoms
suggestive of colorectal carcinoma. Am J Surg1988; 155:224
–226[CrossRef][Medline]
- Cheong Y, Farrow R, Frank CS, Stevenson GW. Utility of flexible
sigmoidoscopy as an adjunct to double-contrast barium enema examination.
Abdom Imaging 1998;23
: 138–140[CrossRef][Medline]
- Irvine EJ, O'Connor J, Frost RA, et al. Prospective comparison of
double contrast barium enema plus flexible sigmoidoscopy v colonoscopy in
rectal bleeding: barium enema v colonoscopy in rectal bleeding.
Gut 1988; 29:1188
–1193[Abstract/Free Full Text]
- Jensen J, Kewenter J, Asztely M, Lycke G, Wojciechowski J. Double
contrast barium enema and flexible rectosigmoidoscopy: a reliable diagnostic
combination for detection of colorectal neoplasm. Br J
Surg 1990; 77:270
–272[Medline]
- Norfleet RG, Ryan ME, Wyman JB, et al. Barium enema versus
colonoscopy for patients with polyps found during flexible sigmoidoscopy.
Gastrointest Endosc 1991;37
: 531–534[Medline]
- Thoeni RF, Menuck L. Comparison of barium enema and colonoscopy in
the detection of small colonic polyps. Radiology1977; 124:631
–635[Abstract]
- Durdey P, Weston PM, Williams NS. Colonoscopy or barium enema as
initial investigation of colonic disease. Lancet1987; 2:549
–551[CrossRef][Medline]
- Aggarwal V, Mittal SK, Kumar N, Chowdhury V. A comparative study of
double contrast barium enema and colonoscopy for evaluation of rectal bleeding
in children. Trop Gastroenterol 1995;16
: 132–137[Medline]
- Cotton PB, Durkalski VL, Pineau BC, et al. Computed tomographic
colonography (virtual colonoscopy): a multicenter comparison with standard
colonoscopy for detection of colorectal neoplasia.
JAMA 2004; 291:1713
–1719[Abstract/Free Full Text]
- Dachman AH, Kuniyoshi JK, Boyle CM, et al. CT colonography with
three-dimensional problem solving for detection of colonic polyps.
AJR 1998; 171:989
–995[Abstract/Free Full Text]
- Fenlon HM, Nunes DP, Schroy PC 3rd, Barish MA, Clarke PD, Ferrucci
JT. A comparison of virtual and conventional colonoscopy for the detection of
colorectal polyps. N Engl J Med 1999;341
:1496
–1503[Abstract/Free Full Text]
- Fletcher JG, Johnson CD, Welch TJ, et al. Optimization of CT
colonography technique: prospective trial in 180 patients.
Radiology 2000;216
: 704–711[Abstract/Free Full Text]
- Gluecker T, Dorta G, Keller W, Jornod P, Meuli R, Schnyder P.
Performance of multidetector computed tomography colonography compared with
conventional colonoscopy. Gut 2002;51
: 207–211[Abstract/Free Full Text]
- Hara AK, Johnson CD, MacCarty RL, Welch TJ, McCollough CH, Harmsen
WS. CT colonography: single-versus multi-detector row imaging.
Radiology 2001;219
: 461–465[Abstract/Free Full Text]
- Johnson CD, Harmsen WS, Wilson LA, et al. Prospective blinded
evaluation of computed tomographic colonography for screen detection of
colorectal polyps. Gastroenterology 2003;125
: 311–319[CrossRef][Medline]
- Lefere PA, Gryspeerdt SS, Dewyspelaere J, Baekelandt M, Van
Holsbeeck BG. Dietary fecal tagging as a cleansing method before CT
colonography: initial results polyp detection and patient acceptance.
Radiology 2002;224
: 393–403[Abstract/Free Full Text]
- Macari M, Bini EJ, Jacobs SL, et al. Significance of missed polyps
at CT colonography. AJR 2004;183
: 127–134[Abstract/Free Full Text]
- Macari M, Bini EJ, Jacobs SL, et al. Colorectal polyps and cancers
in asymptomatic average-risk patients: evaluation with CT colonography.
Radiology 2004;230
: 629–636[Abstract/Free Full Text]
- Macari M, Bini EJ, Xue X, et al. Colorectal neoplasms: prospective
comparison of thin-section low-dose multi-detector row CT colonography and
conventional colonoscopy for detection. Radiology2002; 224:383
–392[Abstract/Free Full Text]
- Macari M, Milano A, Lavelle M, Berman P, Megibow AJ. Comparison of
time-efficient CT colonography with two- and three-dimensional colonic
evaluation for detecting colorectal polyps. AJR2000; 174:1543
–1549[Abstract/Free Full Text]
- McFarland EG, Pilgram TK, Brink JA, et al. CT colonography:
multiobserver diagnostic performance. Radiology2002; 225:380
–390[Abstract/Free Full Text]
- Mendelson RM, Foster NM, Edwards JT, Wood CJ, Rosenberg MS, Forbes
GM. Virtual colonoscopy compared with conventional colonoscopy: a developing
technology. Med J Aust 2000;173
: 472–475[Medline]
- Morrin MM, Farrell RJ, Raptopoulos V, McGee JB, Bleday R, Kruskal
JB. Role of virtual computed tomographic colonography in patients with
colorectal cancers and obstructing colorectal lesions. Dis Colon
Rectum 2000; 43:303
–311[CrossRef][Medline]
- Ginnerup Pedersen GB, Christiansen TE, Bjerregaard NC, Ljungmann K,
Laurberg S. Colonoscopy and multidetector-array computed-tomographic
colonography: detection rates and feasibility.
Endoscopy 2003;35
: 736–742[CrossRef][Medline]
- Pescatore P, Glucker T, Delarive J, et al. Diagnostic accuracy and
interobserver agreement of CT colonography (virtual colonoscopy).Gut
2000; 47:126
–130[Abstract/Free Full Text]
- Pickhardt PJ, Choi JR, Hwang I, et al. Computed tomographic virtual
colonoscopy to screen for colorectal neoplasia in asymptomatic adults.
N Engl J Med 2003;349
:2191
–2200[Abstract/Free Full Text]
- Pineau BC, Paskett ED, Chen GJ, et al. Virtual colonoscopy using
oral contrast compared with colonoscopy for the detection of patients with
colorectal polyps. Gastroenterology 2003;125
: 304–310[CrossRef][Medline]
- Rex DK, Vining D, Kopecky KK. An initial experience with screening
for colon polyps using spiral CT with and without CT colography (virtual
colonoscopy). Gastrointest Endosc 1999;50
: 309–313[CrossRef][Medline]
- Rockey DC, Paulson E, Niedzwiecki D, et al. Analysis of air
contrast barium enema, computed tomographic colonography, and colonoscopy:
prospective comparison. Lancet 2005;365
: 305–311[Medline]
- Royster AP, Fenlon HM, Clarke PD, Nunes DP, Ferrucci JT. CT
colonoscopy of colorectal neoplasms: two-dimensional and three-dimensional
virtual-reality techniques with colonoscopic correlation.
AJR 1997; 169:1237
–1242[Abstract/Free Full Text]
- Spinzi G, Belloni G, Martegani A, Sangiovanni A, Del Favero C,
Minoli G. Computed tomographic colonography and conventional colonoscopy for
colon diseases: a prospective, blinded study. Am J
Gastroenterol 2001; 96:394
–400[CrossRef][Medline]
- Taylor SA, Halligan S, Saunders BP, et al. Use of multidetector-row
CT colonography for detection of colorectal neoplasia in patients referred via
the Department of Health "2-week-wait" initiative. Clin
Radiol 2003; 58:855
–861[CrossRef][Medline]
- Yee J, Akerkar GA, Hung RK, Steinauer-Gebauer AM, Wall SD, McQuaid
KR. Colorectal neoplasia: performance characteristics of CT colonography for
detection in 300 patients. Radiology2001; 219:685
–692[Abstract/Free Full Text]
- Yee J, Kumar NN, Hung RK, Akerkar GA, Kumar PR, Wall SD. Comparison
of supine and prone scanning separately and in combination at CT colonography.
Radiology 2003;226
: 653–661[Abstract/Free Full Text]
- Fenlon HM, Nunes DP, Clarke PD, Ferrucci JT. Colorectal neoplasm
detection using virtual colonoscopy: a feasibility study. Gut1998; 43:806
–811[Abstract/Free Full Text]
- Laghi A, Iannaccone R, Carbone I, et al. Computed tomographic
colonography (virtual colonoscopy): blinded prospective comparison with
conventional colonoscopy for the detection of colorectal neoplasia.
Endoscopy 2002;34
: 441–446[CrossRef][Medline]
- Vos FM, van Gelder RE, Serlie IW, et al. Three-dimensional display
modes for CT colonography: conventional 3D virtual colonoscopy versus unfolded
cube projection. Radiology 2003;228
: 878–885[Abstract/Free Full Text]
- Harvey CJ, Amin Z, Hare CM, et al. Helical CT pneumocolon to assess
colonic tumors: radiologic–pathologic correlation.
AJR 1998; 170:1439
–1443[Abstract/Free Full Text]
- Laghi A, Iannaccone R, Bria E, et al. Contrast-enhanced computed
tomographic colonography in the follow-up of colorectal cancer patients: a
feasibility study. Eur Radiol 2003;13
: 883–889[Medline]
- Miao YM, Amin Z, Healy J, et al. A prospective single centre study
comparing computed tomography pneumocolon against colonoscopy in the detection
of colorectal neoplasms. Gut 2000;47
: 832–837[Abstract/Free Full Text]
- Munikrishnan V, Gillams AR, Lees WR, Vaizey CJ, Boulos PB.
Prospective study comparing multislice CT colonography with colonoscopy in the
detection of colorectal cancer and polyps. Dis Colon
Rectum 2003; 46:1384
–1390[CrossRef][Medline]
- Neri E, Giusti P, Battolla L, et al. Colorectal cancer: role of CT
colonography in preoperative evaluation after incomplete colonoscopy.
Radiology 2002;223
: 615–619[Abstract/Free Full Text]
- Cohnen M, Vogt C, Aurich V, Beck A, Haussinger D, Modder U.
Multi-slice CT-colonography in low-dose technique: preliminary results.
Rofo 2002; 174:835
–838[Medline]
- Gluecker T, Meuwly JY, Pescatore P, et al. Effect of investigator
experience in CT colonography. Eur Radiol2002; 12:1405
–1409[CrossRef][Medline]
- Hara AK, Johnson CD, Reed JE, et al. Detection of colorectal polyps
with CT colography: initial assessment of sensitivity and specificity.
Radiology 1997;205
: 59–65[Abstract/Free Full Text]
- Kay CL, Kulling D, Hawes RH, Young JW, Cotton PB. Virtual
endoscopy: comparison with colonoscopy in the detection of space-occupying
lesions of the colon. Endoscopy 2000;32
: 226–232[CrossRef][Medline]
- Luo M, Shan H, Zhou K. CT virtual colonoscopy in patients with
incomplete conventional colonoscopy. Chin Med J (Engl)2002; 115:1023
–1026[Medline]
- Summers RM, Jerebko AK, Franaszek M, Malley JD, Johnson CD. Colonic
polyps: complementary role of computer-aided detection in CT colonography.
Radiology 2002;225
: 391–399[Abstract/Free Full Text]
- Wong BC, Wong WM, Chan JK, et al. Virtual colonoscopy for the
detection of colorectal polyps and cancers in a Chinese population.
J Gastroenterol Hepatol 2002;17
:1323
–1327[CrossRef][Medline]
- Gryspeerdt S, Lefere P, Herman M, et al. CT colonography with fecal
tagging after incomplete colonoscopy. Eur Radiol2005; 15:1192
–1202[CrossRef][Medline]
- Iannaccone R, Laghi A, Catalano C, et al. Computed tomographic
colonography without cathartic preparation for the detection of colorectal
polyps. Gastroenterology 2004;127
:1300
–1311[CrossRef][Medline]
- Kealey SM, Dodd JD, MacEneaney PM, Gibney RG, Malone DE. Minimal
preparation computed tomography instead of barium enema/colonoscopy for
suspected colon cancer in frail elderly patients: an outcome analysis study.
Clin Radiol 2004;59
: 44–52[CrossRef][Medline]
- Lefere P, Gryspeerdt S, Marrannes J, Baekelandt M, Van Holsbeeck B.
CT colonography after fecal tagging with a reduced cathartic cleansing and a
reduced volume of barium. AJR 2005;184
:1836
–1842[Abstract/Free Full Text]
- Lipscomb G, Loughrey G, Thakker M, Rees W, Nicholson D. A
prospective study of abdominal computerized tomography and colonoscopy in the
diagnosis of colonic disease in an elderly population. Eur J
Gastroenterol Hepatol 1996;8
: 887–891[Medline]
- Thomeer M, Carbone I, Bosmans H, et al. Stool tagging applied in
thin-slice multidetector computed tomography colonography. J Comput
Assist Tomogr 2003; 27:132
–139[CrossRef][Medline]
- Luboldt W, Mann C, Tryon CL, et al. Computer-aided diagnosis in
contrast-enhanced CT colonography: an approach based on contrast.
Eur Radiol 2002;12
:2236
–2241[Medline]
- Yoshida H, Masutani Y, MacEneaney P, Rubin DT, Dachman AH.
Computerized detection of colonic polyps at CT colonography on the basis of
volumetric features: pilot study. Radiology 2002;222
: 327–336[Abstract/Free Full Text]
- Yoshida H, Nappi J, MacEneaney P, Rubin DT, Dachman AH.
Computer-aided diagnosis scheme for detection of polyps at CT colonography.
RadioGraphics 2002;22
: 963–979[Abstract/Free Full Text]
- Cohnen M, Vogt C, Beck A, et al. Feasibility of MDCT colonography
in ultra-low-dose technique in the detection of colorectal lesions: comparison
with high-resolution video colonoscopy. AJR2004; 183:1355
–1359[Abstract/Free Full Text]
- Iannaccone R, Laghi A, Catalano C, et al. Detection of colorectal
lesions: lower-dose multi-detector row helical CT colonography compared with
conventional colonoscopy. Radiology 2003;229
: 775–781[Abstract/Free Full Text]
- Iannaccone R, Laghi A, Catalano C, Mangiapane F, Piacentini F,
Passariello R. Feasibility of ultra-low-dose multislice CT colonography for
the detection of colorectal lesions: preliminary experience. Eur
Radiol 2003; 13:1297
–1302[Medline]
- Vogt C, Cohnen M, Beck A, et al. Detection of colorectal polyps by
multislice CT colonography with ultra-low-dose technique: comparison with
high-resolution videocolonoscopy. Gastrointest Endosc2004; 60:201
–209[CrossRef][Medline]
- Iannaccone R, Catalano C, Mangiapane F, et al. Colorectal polyps:
detection with low-dose multi-detector row helical CT colonography versus two
sequential colonoscopies. Radiology 2005;237
: 927–937[Abstract/Free Full Text]
- Abdel Razek AA, Abu Zeid MM, Bilal M, Abdel Wahab NM. Virtual CT
colonoscopy versus conventional colonoscopy: a prospective study.
Hepatogastroenterology 2005;52
:1698
–1702[Medline]
- Kalra N, Suri S, Bhasin DK, et al. Comparison of multidetector
computed tomographic colonography and conventional colonoscopy for detection
of colorectal polyps and cancer. Indian J
Gastroenterol 2006; 25:229
–232[Medline]
- Mulhall BP, Veerappan GR, Jackson JL. Metaanalysis: computed
tomographic colonography. Ann Intern Med2005; 142:635
–650[Abstract/Free Full Text]
- Morrin MM, Farrell RJ, Kruskal JB, Reynolds K, McGee JB,
Raptopoulos V. Utility of intravenously administered contrast material at CT
colonography. Radiology 2000;217
: 765–771[Abstract/Free Full Text]
- Halligan S, Altman DG, Taylor SA, et al. CT colonography in the
detection of colorectal polyps and cancer: systematic review, meta-analysis,
and proposed minimum data set for study level reporting.
Radiology 2005;237
: 893–904[Abstract/Free Full Text]
- Sosna J, Morrin MM, Kruskal JB, Lavin PT, Rosen MP, Raptopoulos V.
CT colonography of colorectal polyps: a metaanalysis.
AJR 2003; 181:1593
–1598[Abstract/Free Full Text]
- Cappelleri JC, Ioannidis JP, Schmid CH, et al. Large trials vs
meta-analysis of smaller trials: how do their results compare?
JAMA 1996; 276:1332
–1338[Abstract/Free Full Text]
- LeLorier J, Gregoire G, Benhaddad A, Lapierre J, Derderian F.
Discrepancies between meta-analyses and subsequent large randomized,
controlled trials. N Engl J Med 1997;337
: 536–542[Abstract/Free Full Text]
- Pickhardt PJ, Taylor AJ, Kim DH, Reichelderfer M, Gopal DV, Pfau
PR. Screening for colorectal neoplasia with CT colonography: initial
experience from the 1st year of coverage by third-party payers.
Radiology 2006;241
: 417–425[Abstract/Free Full Text]
- Gluecker TM, Johnson CD, Wilson LA, et al. Extracolonic findings at
CT colonography: evaluation of prevalence and cost in a screening population.
Gastroenterology 2003;124
: 911–916[CrossRef][Medline]
- Sosna J, Kruskal JB, Bar-Ziv J, Copel L, Sella T. Extracolonic
findings at CT colonography. Abdom Imaging2005; 30:709
–713[CrossRef][Medline]
- Irwig L, Macaskill P, Glasziou P, Fahey M. Metaanalytic methods for
diagnostic test accuracy. J Clin Epidemiol1995; 48:119
–130; discussion 131–132[CrossRef][Medline]
- Thoeni RF, Petras A. Detection of rectal and rectosigmoid lesions
by double-contrast barium enema examination and sigmoidoscopy: accuracy of
technique and efficacy of standard overhead views.Radiology
1982;142
: 59–62[Abstract/Free Full Text]
- Arnesen RB, Adamsen S, Svendsen LB, Raaschou HO, von Benzon E,
Hansen OH. Missed lesions and false-positive findings on computed-tomographic
colonography: a controlled prospective analysis.
Endoscopy 2005;37
: 937–944[Medline]
- Reuterskiold MH, Lasson A, Svensson E, Kilander A, Stotzer PO,
Hellstrom M. Diagnostic performance of computed tomography colonography in
symptomatic patients and in patients with increased risk for colorectal
disease. Acta Radiol 2006;47
: 888–898[CrossRef][Medline]

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