Critical Analysis of the Performance of Double-Contrast Barium Enema for Detecting Colorectal Polyps ≥ 6 mm in the Era of CT Colonography

374 AJR:190, February 2008

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]. How-ever, the U.S. Preventive Services Task Force found insufficient evidence to conclude that CTC improves health outcomes and deter-mined 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 con-sidered an evolving technique pending results from multicenter trials.

DCBE needs to be reevaluated with com-parable rigor because previous studies have questioned its performance [15]. Although several CTC meta-analyses have been pub-lished, to our knowledge no meta-analysis addresses DCBE performance. The purpose of this study was to perform a meta-analysis

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 Eugene Libson1

Sosna J, Sella T, Sy O, et al.

1Department of Radiology, Hadassah Hebrew University Medical Center, POB 12000, Jerusalem, Israel. Address correspondence to J. Sosna ([email protected]).

2Department of Radiology, Beth Israel Deaconess Medical Center, Boston, MA.

3Boston Biostatistics Research Foundation, Framingham, MA.

Gastrointest ina l Imaging • Or ig ina l Research

AJR 2008; 190:374–385

0361–803X/08/1902–374

© American Roentgen Ray Society

Colorectal cancer is the second leading cause of death from can-cer in the United States, with a 6% lifetime risk of disease [1].

Routine screening for malignancies and ad-enomatous polyps is recommended to begin at the age of 50 years, or at a younger age for those at higher risk [2–5]. Effective screen-ing 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 colorec-tal cancer include fecal occult blood test-ing, flexible sigmoidoscopy, conventional colonoscopy, and double-contrast barium enema (DCBE). Although DCBE is an ac-cepted 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 colonos-copy, was introduced in 1994 [10]. CTC has

Keywords: barium enema, colonoscopy, CT colonography, double-contrast barium enema, meta-analysis, virtual colonoscopy

DOI:10.2214/AJR.07.2099

Received February 21, 2007; accepted after revision September 9, 2007.

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-per-patient 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.

Sosna et al.Double-Contrast Barium Enema for Detecting Polyps

Gastrointestinal ImagingOriginal Research

Dow

nloa

ded

from

ww

w.a

jron

line.

org

by U

CSF

LIB

& C

KM

/RSC

S M

GM

T o

n 12

/04/

14 f

rom

IP

addr

ess

169.

230.

243.

252.

Cop

yrig

ht A

RR

S. F

or p

erso

nal u

se o

nly;

all

righ

ts r

eser

ved

AJR:190, February 2008 375

Double-Contrast Barium Enema for Detecting Polyps

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 MethodsThis study did not involve human subjects

directly and was exempt from institutional review board approval.

Data Sources and Literature SearchA 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 EligibilityAll 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).

Data ExtractionThe 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 AnalysisThe 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.

ResultsLiterature Search

We retrieved 662 original articles address-ing all aspects of DCBE from the databases; 11 fulfilled inclusion criteria [15, 18–27] (Ta-ble 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 address-ing 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 scan-ning position (n = 7) [91–97], minimal or no preparation (n = 6) [98–103], computer-aided detection (n = 4) [96, 104–106], ultralow radi-ation 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 in-cluded [20, 77]. In these studies, findings for each imaging method were analyzed sepa-rately and thus could be added to the cumu-lative experience for each technique.

No DCBE study involved 50 or fewer sub-jects, 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%) stud-ies provided no information regarding patient selection. Conventional colonoscopy was the reference standard in five studies (46%), sigmoidoscopy in four (36%), and both con-ventional colonoscopy and sigmoidoscopy in two studies (18%).

Six of 30 CTC studies (20%) had 50 sub-jects 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.

Dow

nloa

ded

from

ww

w.a

jron

line.

org

by U

CSF

LIB

& C

KM

/RSC

S M

GM

T o

n 12

/04/

14 f

rom

IP

addr

ess

169.

230.

243.

252.

Cop

yrig

ht A

RR

S. F

or p

erso

nal u

se o

nly;

all

righ

ts r

eser

ved


Sosna et al.

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

Authors Journal Year CTC Radiologic InterpretationNo. of

PatientsComparison

Study Population

Double-contrast barium enema

Williams et al. [27] Endoscopy 1982 NA 330 CC High risk

Thoeni and Petras [124] Radiology 1982 NA 53 CC High risk

Farrands et al. [18]a Dis Col Rectum 1983 NA 227 FS Mixed

Rex et al. [22] Radiology 1986 NA 65 FS NA

Jensen et al. [19] Br J Surg 1986 NA 458 FS High risk

Saito et al. [24] Gastrointest Radiol 1989 NA 675 FS NA

Steine et al. [25] Fam Practice 1993 NA 189 CC NA

Kewenter et al. [21] Endoscopy 1995 NA 1,831 FS + CC High risk

Winawer et al. [15] N Engl J Med 2000 NA 862 CC High risk

Johnson et al. [20] Clin Gastroenterol Hepatol

2004 NA 691 CC + FS Average risk

Rockey et al. [77] Lancet 2005 NA 614 CC High risk

Virtual colonoscopy

Royster et al. [78] AJR 1997 2 readers in consensus, experienced radiologists, CTC experience not stated; 2D and 3D; blinding to CTC findings

20 CC High risk

Dachman et al. [58] AJR 1998 2 readers, independent review, experience not described; primarily 2D with 3D confirmation; blinding to CTC findings

44 CC High risk

Fenlon et al. [59] N Engl J Med 1999 2 readers in consensus, experienced radiologists, CTC experience not stated; 2D and 3D; blinding to CTC findings

100 CC High risk

Rex et al. [76] Gastrointest Endosc 1999 2 radiologists in consensus, experience not described; 2D and 3D; blinding to CTC findings

46 CC Average risk

Morrin et al. [115] Radiology 2000 2 readers, independent review, 18 mo of CTC experience; primarily 2D with 3D confirmation; segmental unblinding

33 CC High risk

Mendelson et al. [70] Med J Aust 2000 1 reader, new to reading CTC at study inception; 2D and 3D; blinding to CTC findings

53 CC High risk

Pescatore et al. [73] Gut 2000 2 radiologist–gastroenterologist teams read independently, CTC experience not described; 2D and 3D; blinding to CTC findings

50 CC High risk

Fletcher et al. [60] Radiology 2000 Multiple readers, independent review and later consensus review, CTC experience not described; primarily 2D with 3D confirmation; blinding to CTC findings

180 CC High risk

Macari et al. [68] AJR 2000 2 CTC-trained radiologists, independent review; 2D and 3D; blinding to CTC findings

42 CC Average risk

Hara et al. [62] Radiology 2001 2 radiologists, independent review, CTC experience not described; 2D and 3D; blinding to CTC findings

237 CC High risk

Yee et al. [81] Radiology 2001 2 readers independently and in consensus, CTC experience not described; 2D and 3D; blinding to CTC findings

300 CC High risk

Spinzi et al. [79] Am J Gastroenterol 2001 1 reader with later supervisor review of detected lesions, limited CTC experience; primarily 2D with 3D confirmation; blinding to CTC findings

99 CC High risk

Table 1 continues on next page

Dow

nloa

ded

from

ww

w.a

jron

line.

org

by U

CSF

LIB

& C

KM

/RSC

S M

GM

T o

n 12

/04/

14 f

rom

IP

addr

ess

169.

230.

243.

252.

Cop

yrig

ht A

RR

S. F

or p

erso

nal u

se o

nly;

all

righ

ts r

eser

ved



Authors Journal Year CTC Radiologic InterpretationNo. of

PatientsComparison

Study Population

Gluecker et al. [61] Gut 2002 Radiologist and CTC-experienced gastroenterologist in consensus; 2D and 3D; blinding to CTC findings

50 CC High risk

Lefere et al. [64] Radiology 2002 2 readers in consensus, CTC experience not stated; 2D and 3D; segmental unblinding

100 CC High risk

Macari et al. [67] Radiology 2002 1 radiologist with 4 y of CTC experience; primarily 2D with 3D confirmation; blinding to CTC findings

105 CC High risk

McFarland et al. [69] Radiology 2002 4 experienced readers, limited CTC experience; primarily 2D with 3D confirmation; blinding to CTC findings

70 CC High risk

Pickhardt et al. [74] N Engl J Med 2003 1 of 6 experienced readers, range of CTC experience; fly-through and 2D; segmental unblinding

1,233 CC Average risk

Ginnerup Pedersen et al. [72] Endoscopy 2003 1 research fellow reader with good CTC experience; primarily 2D with 3D confirmation; segmental unblinding

148 CC High risk

Johnson et al. [63] Gastroenterology 2003 2 readers, prior experience with 150 CTC examinations; primarily 2D with 3D confirmation; blinding to DCBE and endoscopy

703 CC High risk

Pineau et al. [75] Gastroenterology 2003 1 experienced reader, CTC experience not stated; 2D and 3D; segmental unblinding

205 CC Mixed

Taylor et al. [80] Clin Radiol 2003 1 of several readers, experience not described; primarily 2D with 3D confirmation; segmental unblinding

54 CC High risk

Yee et al. [82] Radiology 2003 2 readers, experience not described; fly-through and 2D; blinding to CTC findings

182 CC Mixed

Johnson et al. [20] Clin Gastroenterol Hepatol

2004 2 readers, prior experience with 150 CTC cases; primarily 2D with 3D confirmation; blinding to DCBE and endoscopy

691 CC High risk

Van Gelder et al. [11] Gastroenterology 2004 1 experienced reader and 1 fellow, both with good CTC experience; primarily 2D with 3D confirmation; blinding to CTC findings; second-look colonoscopy as needed

249 CC High risk

Macari et al. [66] Radiology 2004 1 radiologist with 5 y of CTC experience; primarily 2D with 3D confirmation; blinding to CTC findings

68 CC Average risk

Cotton et al. [57] JAMA 2004 1 reader, limited CTC experience; primarily 2D with 3D confirmation; segmental unblinding

600 CC High risk

Macari et al. [65] AJR 2004 1 radiologist with 5 y of CTC experience; blinding to CTC findings

186 CC High risk

Rockey et al. [77] Lancet 2005 Unknown number of radiologists, limited CTC experience; primarily 2D with 3D confirmation; segmental unblinding

614 CC High risk

Arnesen et al. [125] Endoscopy 2005 1 reader, limited CTC experience; 2D and 3D; blinding to CTC findings

100 CC High risk

Reuterskiold et al. [126] Acta Radiol 2006 2 readers, CTC experience not described; primarily 2D with 3D confirmation; blinding to CTC findings with retrospective matching

111 CC High risk

Note—NA = not applicable, CC = conventional colonoscopy, FS = flexible sigmoidoscopy, DCBE = double-contrast barium enema. aFocused solely on sensitivity and specificity to adenomas and neoplastic lesions.

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 (continued)

Dow

nloa

ded

from

ww

w.a

jron

line.

org

by U

CSF

LIB

& C

KM

/RSC

S M

GM

T o

n 12

/04/

14 f

rom

IP

addr

ess

169.

230.

243.

252.

Cop

yrig

ht A

RR

S. F

or p

erso

nal u

se o

nly;

all

righ

ts r

eser

ved


Sosna et al.

Data SynthesisDCBE—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 sensitiv-ity and specificity analysis of DCBE studies yielded p < 0.001 for the Fisher’s exact test on all end points except per-patient sensitiv-ity 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 sensitiv-ity 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 in-cluded 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 sensitiv-ity 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 per- patient and per-polyp sensitivity with increas-ing polyp size (p < 0.0001). The Kruskal- Wallis test confirmed these findings.

Comparison of CTC and DCBE—Esti-mates comparing pooled DCBE performance with pooled CTC performance showed sig-nificant differences in favor of CTC for speci-ficity and per-polyp sensitivity in polyps ≥ 6 mm (Table 4).

DiscussionAlthough DCBE is an accepted and widely

used technique, we could retrieve only 11 pro-

spective studies comparing DCBE with con-ventional colonoscopy or sigmoidoscopy, even when the search was extended back to 1960. Of interest is the relatively small number of prospective studies addressing DCBE perfor-mance. In fact, studies that used sigmoidos-copy 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 de-manding 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 in-cluding 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. Ac-ceptance 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 sec-tion width ≤ 5 mm, which provides accept-able thickness [114], although thinner col-limation 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 con-trast material may increase CTC sensitiv-ity 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 heterogene-ity 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 het-erogeneity 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 impor-tant parameters for population-based deci-sions—for example, test specificity and per-patient 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. Extrapola-tion 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 pol-yps). Although some of these polyps could be diagnosed in subsequent screening stud-ies, it seems likely that some of these missed polyps might be diagnosed as malignan-cies 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 pa-tients and their families.

The true goal in screening is to reduce the morbidity and mortality rates of colorec-tal 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 influ-ence 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

Dow

nloa

ded

from

ww

w.a

jron

line.

org

by U

CSF

LIB

& C

KM

/RSC

S M

GM

T o

n 12

/04/

14 f

rom

IP

addr

ess

169.

230.

243.

252.

Cop

yrig

ht A

RR

S. F

or p

erso

nal u

se o

nly;

all

righ

ts r

eser

ved



TABLE 2: Summary of Statistics for Double-Contrast Barium Enema and CT Colonography

Author YearSize (mm)

Total No. of Polyps

Detected by Endoscopy

No. of True-Positive

PolypsPer-Polyp Sensitivity

Total No. of Cases



CasesPer-Patient Sensitivity

Specificity for Polyps ≥ 10 mm


Williams [27]a,b 1982 ≥ 10 63 41 0.71 0.98

Thoeni and Petras [124] 1982 ≥ 10 21 17 0.81

Farrands et al. [18] 1983 ≥ 10 50 38 0.76

Rex et al. [22] 1986 ≥ 10 17 17 1.00 0.96

Jensen et al. [19] 1986 ≥ 10 56 43 0.77

Saito et al. [24] 1989 ≥ 10 16 14 0.88

Steine et al. [25] 1993 ≥ 10 21 17 0.81 0.97

Kewenter et al. [21] 1995 ≥ 10 235 180 0.77 211 156 0.74

Winawer et al. [15] 2000 ≥ 10 23 11 0.48 23 11 0.48 0.74

Johnson et al. [20] 2004 ≥ 10 21 9 0.43 19 9 0.47 0.99

Rockey et al. [77] 2005 ≥ 10 76 34 0.45 63 30 0.48 0.90

Williams et al. [27] 1982 6–9 NA

Thoeni and Petras [124] 1982 6–9 12 12 1.00

Farrands et al. [18] 1983 6–9 NA

Rex et al. [22] 1986 6–9 23 19 0.83

Jensen et al. [19] 1986 6–9 33 20 0.61

Saito et al. [24] 1989 6–9 49 35 0.71

Steine et al. [25] 1993 6–9 12 6 0.50

Kewenter et al. [21] 1995 6–9 NA

Winawer et al. [15] 2000 6–9 82 35 0.43 64 34 0.53

Johnson et al. [20] 2004 6–9 27 11 0.41 20 12 0.60

Rockey et al. [77] 2005 6–9 158 47 0.30 116 41 0.35

CT colonography

Royster et al. [78] 1997 ≥ 10 22 22 1.00 20 20 1

Dachman et al. [58] 1998 ≥ 10 6 5 0.83 6 5 0.83 1.00

Fenlon et al. [59] 1999 ≥ 10 22 20 0.91 0.93

Rex et al. [76] 1999 ≥ 10 14 7 0.50 10 8 0.80 0.89

Morrin et al. [71] 2000 ≥ 10 12 11 0.92 6 5 0.83 1.00

Mendelson et al. [70] 2000 ≥ 10 11 8 0.73

Pescatore et al. [73] 2000 ≥ 10 11 8 0.73

Fletcher et al. [60] 2000 ≥ 10 121 91 0.75 96 82 0.85 0.93

Macari et al. [68] 2000 ≥ 10 1 1 1.00 0.96

Hara et al. [62] 2001 ≥ 10 19 16 0.84 14 12 0.86 0.91

Yee et al. [81] 2001 ≥ 10 82 74 0.90 49 49 1.00 0.99

Spinzi et al. [79] 2001 ≥ 10 13 8 0.62

Gluecker et al. [61] 2002 ≥ 10 11 9 0.82

McFarland et al. [69] 2002 ≥ 10 40 27 0.68 28 25 0.89

Macari et al. [67] 2002 ≥ 10 14 13 0.93

Lefere et al. [64] 2002 ≥ 10 25 25 1.00 25 25 1.00 1.00

Pickhardt et al. [74] 2003 ≥ 10 51 47 0.92 48 45 0.94 0.96

Ginnerup Pedersen et al. [72] 2003 ≥ 10 38 34 0.89 25 21 0.84

Johnson et al. [63] 2003 ≥ 10 59 27 0.46 47 23 0.49 0.98

Pineau et al. [75] 2003 ≥ 10 27 21 0.78 20 18 0.90 0.95

Table 2 continues on next page

Dow

nloa

ded

from

ww

w.a

jron

line.

org

by U

CSF

LIB

& C

KM

/RSC

S M

GM

T o

n 12

/04/

14 f

rom

IP

addr

ess

169.

230.

243.

252.

Cop

yrig

ht A

RR

S. F

or p

erso

nal u

se o

nly;

all

righ

ts r

eser

ved


Sosna et al.

Author YearSize (mm)

Total No. of Polyps



PolypsPer-Polyp Sensitivity

Total No. of Cases



CasesPer-Patient Sensitivity

Specificity for Polyps ≥ 10 mm

Taylor et al. [80] 2003 ≥ 10 10 9 0.90 1.00

Yee et al. [82] 2003 ≥ 10 41 38 0.93

Johnson et al. [20]c 2004 ≥ 10 NA 25 0.81 NA 23 0.79 0.95

Van Gelder et al. [11] 2004 ≥ 10 48 37 0.77 31 26 0.84 0.92

Macari et al. [66] 2004 ≥ 10 3 3 1.00 3 3 1.00 0.99

Cotton et al. [57] 2004 ≥ 10 54 28 0.52 42 23 0.55 0.96

Macari et al. [65] 2004 ≥ 10 22 20 0.91

Rockey et al. [77] 2005 ≥ 10 76 40 0.53 0.96

Arneson et al. [125] 2005 ≥ 10 18 12 0.67 12 9 0.75 0.95

Reuterskiold et al. [126] 2006 ≥ 10 23 21 0.91 19 18 0.95 0.92

Royster et al. [78] 1997 6–9 10 9 0.90

Dachman et al. [58] 1998 6–9 3 1 0.33

Fenlon et al. [59] 1999 6–9 40 33 0.83

Rex et al. [76] 1999 6–9 14 6 0.43 7 3 0.43

Morrin et al. [115] 2000 6–9 11 4 0.36 12 7 0.58

Mendelson et al. [70] 2000 6–9 18 4 0.22

Pescatore et al. [73] 2000 6–9

Fletcher et al. [60] 2000 6–9 142 67 0.47 130 114 0.88

Macari et al. [68] 2000 6–9 5 3 0.60

Hara et al. [62] 2001 6–9 NA

Yee et al. [81] 2001 6–9 141 113 0.80 54 50 0.93

Spinzi et al. [79] 2001 6–9 32 18 0.56

Gluecker et al. [61] 2002 6–9 15 5 0.33

McFarland et al. [69] 2002 6–9 45 16 0.36 20 14 0.70

Macari et al. [67] 2002 6–9 27 19 0.70

Lefere et al. [64] 2002 6–9 31 28 0.90 23 21 0.91

Pickhardt et al. [74] 2003 6–9 159 133 0.84

Ginnerup Pedersen et al. [72] 2003 6–9 31 22 0.71 19 19 1.00

Johnson et al. [63] 2003 6–9 94 38 0.40 69 36 0.52

Pineau et al. [75] 2003 6–9 48 36 0.75 25 20 0.80

Taylor et al. [80] 2003 6–9 4 3 0.75

Yee et al. [82] 2003 6–9 89 71 0.80

Johnson et al. [20]c 2004 6–9 NA 28 0.72 95 25 0.83 0.86

Van Gelder et al. [11] 2004 6–9 36 25 0.69 14 9 0.64

Macari et al. [66] 2004 6–9 17 9 0.53

Cotton et al. [57] 2004 6–9 119 27 0.23 76 23 0.30

Macari et al. [65] 2004 6–9 26 26 1.00

Rockey et al. [77] 2005 6–9 158 75 0.47

Arnesen et al. [125] 2005 6–9 46 27 0.60 27 18 0.67

Reuterskiold et al. [126] 2006 6–9 24 19 0.75 9 5 0.56

Note—NA = not applicable. aReports sensitivity and specificity for adenomas and neoplastic lesions only. bReports findings of lesions ≥ 7. cOur meta-analysis used overall sensitivity and specificity based on double reading for CTC data.

TABLE 2: Summary of Statistics for Double-Contrast Barium Enema and CT Colonography (continued)

Dow

nloa

ded

from

ww

w.a

jron

line.

org

by U

CSF

LIB

& C

KM

/RSC

S M

GM

T o

n 12

/04/

14 f

rom

IP

addr

ess

169.

230.

243.

252.

Cop

yrig

ht A

RR

S. F

or p

erso

nal u

se o

nly;

all

righ

ts r

eser

ved



previously published CTC meta-analyses [114, 116, 117], with less heterogeneity. This may be partially explained by stricter inclu-sion criteria in this study, which resulted in a smaller number of included articles (e.g., 30 studies in this analysis vs 33 in the meta-analysis 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 stud-ies, which may partly explain improved CTC performance because higher prevalence af-fects and increases positive predictive value. However, this is unlikely to be the sole ex-planation 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 me-ta-analysis does not replace large prospec-tive clinical trials, reports have shown that findings based on analysis of pooled data of a series of smaller studies do not differ sig-nificantly from outcomes of large trials [118, 119]. And although CTC is not recommend-ed 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 popula-tion with third-party coverage were recently published [120], further studies should be performed to address the economic aspects and radiation considerations of the wide-spread use of CTC as a reimbursable screen-ing tool. CTC has the added benefit of evalu-ating 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 rela-tive performance today, given the recent im-provement in conventional colonoscopy sen-sitivity. 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 accu-rate in these colon segments, possibly skew-ing data downward. However, prevalence of polyps in these regions is also higher, which may limit a possible reduction in patient sen-sitivity 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 tech-nologies (e.g., CTC) compared with older techniques (DCBE), which are considered less attractive for research. In addition, sev-eral weakly positive studies may add to a strong positive result when pooled. A rich delineation of possible sources of hetero-geneity requires a more sensitive technique than meta-analysis. We included informa-tion on study characteristics, but our ability to discriminate sources of heterogeneity was limited. We also could not evaluate other fac-tors, 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 reimburse-ment 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

TABLE 3: Pooling of Double-Contrast Barium Enema and CT Colonography Studies

Study End Point

Unweighted Pooled

Measure

95% CI for Unweighted

Pooled Measure

Sample-Size

Weighted Pooled

Measure

95% CI for Sample-Size

Weighted Pooled

Measure


Per-patient specificity, polyps ≥ 10 mm 0.856 0.841–0.876 0.851 0.847–0.855

Per-polyp sensitivity, polyps ≥ 10 mm 0.698 0.657–0.734 0.714 0.703–0.726

Per-polyp sensitivity, polyps 6–9 mm 0.456 0.405–0.504 0.404 0.388–0.420

Per-patient sensitivity, polyps ≥ 10 mm 0.678 0.628–0.726 0.701 0.687–0.715

Per-patient sensitivity, polyps 6–9 mm 0.419 0.345–0.489 0.405 0.382–0.428

CT colonography

Per-patient specificity, polyps ≥ 10 mm 0.940 0.930–0.950 0.954 0.952–0.955

Per-polyp sensitivity, polyps ≥ 10 mm 0.762 0.734–0.790 0.746 0.735–0.757

Per-polyp sensitivity, polyps 6–9 mm 0.602 0.576–0.628 0.598 0.589–0.606

Per-patient sensitivity, polyps ≥ 10 mm 0.828 0.794–0.862 0.823 0.809–0.836

Per-patient sensitivity, polyps 6–9 mm 0.703 0.661–0.744 0.707 0.692–0.721

TABLE 4: Comparison of Performance of Double-Contrast Barium Enema (DCBE) and CT Colonography (CTC)

End PointCTC Pooled

Point EstimateDCBE Pooled

Point Estimate DifferenceaStandard Error of Difference

Test Statisticb p

Per-patient specificity, polyps ≥ 10 mm 0.954 0.850 0.103 0.002 54.371 0.0001

Per-polyp sensitivity, polyps ≥ 10 mm 0.746 0.715 0.031 0.008 3.883 0.0001

Per-polyp sensitivity, polyps 6–9 mm 0.598 0.405 0.193 0.009 20.645 0.0001

Per-patient sensitivity, polyps ≥ 10 mm 0.823 0.702 0.120 0.010 11.765 0.0001

Per-patient sensitivity, polyps 6–9 mm 0.707 0.406 0.301 0.014 21.384 0.0001

aCTC pooled point estimate – DCBE pooled point estimate. bAz test.

Dow

nloa

ded

from

ww

w.a

jron

line.

org

by U

CSF

LIB

& C

KM

/RSC

S M

GM

T o

n 12

/04/

14 f

rom

IP

addr

ess

169.

230.

243.

252.

Cop

yrig

ht A

RR

S. F

or p

erso

nal u

se o

nly;

all

righ

ts r

eser

ved


Sosna et al.

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 sensi-tivity and specificity than CTC for detecting polyps ≥  6 mm, with the difference being statistically significant.

References 1. Cancer facts and figures 2006. American Cancer

Society Website. Available at www.cancer.org.

Updated 2007. Accessed July 2, 2007

2. Rex DK, Johnson DA, Lieberman DA, Burt RW,

Sonnenberg A. Colorectal cancer prevention

2000: screening recommendations of the Ameri-

can College of Gastroenterology. American Col-

lege of Gastroenterology. Am J Gastroenterol

2000; 95:868–877

3. Smith RA, Cokkinides V, Eyre HJ. American Can-

cer Society guidelines for the early detection of

cancer, 2004. CA Cancer J Clin 2004; 54:41–52

4. Winawer SJ, Fletcher RH, Miller L, et al. Col-

orectal cancer screening: clinical guidelines and

rationale. Gastroenterology 1997; 112:594–642

5. 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

Med 2002; 137:132–141

6. 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

7. 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

8. Winawer SJ, Zauber AG, Ho MN, et al. Preven-

tion of colorectal cancer by colonoscopic polypec-

tomy. The National Polyp Study Workgroup.

N Engl J Med 1993; 329:1977–1981

9. Ioannou GN, Chapko MK, Dominitz JA. Predic-

tors of colorectal cancer screening participation

in the United States. Am J Gastroenterol 2003;

98:2082–2091

10. Vining DJ, Gelfand DW, Bechtold RE, Scharling

ES, Grishaw EK, Shifrin RY. Technical feasibil-

ity of colon imaging with helical CT and virtual

reality. (abstr) AJR 1994; 162 [American Roent-

gen Ray Society 94th Annual Meeting Program

Book suppl]:104

11. Van Gelder RE, Nio CY, Florie J, et al. Computed

tomographic colonography compared with colono-

scopy in patients at increased risk for colorectal

cancer. Gastroenterology 2004; 127: 41–48

12. Burling D, Halligan S, Slater A, Noakes MJ, Tay-

lor SA. Potentially serious adverse events at CT

colonography in symptomatic patients: national

survey of the United Kingdom. Radiology 2006;

239:464–471

13. Sosna J, Sella T, Bar-Ziv J, Libson E. Perforation

of the colon and rectum: a newly recognized

complication of CT colonography. Semin Ultra-

sound CT MR 2006; 27:161–165

14. AGA Clinical Pratice and Economics Committee.

Position of the American Gastroenterological

Association (AGA) Institute on computed tomo-

graphic colonography. Gastroenterology 2006;

131:1627–1628

15. Winawer SJ, Stewart ET, Zauber AG, et al. A

comparison of colonoscopy and double-contrast

barium enema for surveillance after polypecto-

my. National Polyp Study Work Group. N Engl J

Med 2000; 342:1766–1772

16. Zalis ME, Barish MA, Choi JR, et al. CT

colonography reporting and data system: a con-

sensus proposal. Radiology 2005; 236:3–9

17. 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

18. Farrands PA, Vellacott KD, Amar SS, Balfour

TW, Hardcastle JD. Flexible fiberoptic sigmoi-

doscopy and double-contrast barium-enema ex-

amination in the identification of adenomas and

carcinoma of the colon. Dis Colon Rectum 1983;

26:725–727

19. Jensen J, Kewenter J, Haglind E, Lycke G, Svens-

son C, Ahren C. Diagnostic accuracy of double-

contrast enema and rectosigmoidoscopy in con-

nection with faecal occult blood testing for the

detection of rectosigmoid neoplasms. Br J Surg

1986; 73:961–964

20. 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

21. Kewenter J, Brevinge H, Engaras B, Haglind E.

The yield of flexible sigmoidoscopy and double-

contrast barium enema in the diagnosis of neo-

plasms in the large bowel in patients with a positive

Hemoccult test. Endoscopy 1995; 27: 159–163

22. Rex DK, Lehman GA, Lappas JC, Miller RE.

Sensitivity of double-contrast barium study for

left-colon polyps. Radiology 1986; 158:69–72

23. Rockey DC, Koch J, Yee J, McQuaid KR, Halvors-

en RA. Prospective comparison of air-contrast

barium enema and colonoscopy in patients with

fecal occult blood: a pilot study. Gastrointest

Endosc 2004; 60:953–958

24. 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

25. Steine S, Stordahl A, Lunde OC, Loken K,

Laerum E. Double-contrast barium enema versus

colonoscopy in the diagnosis of neoplastic disor-

ders: aspects of decision-making in general prac-

tice. Fam Pract 1993; 10:288–291

26. Thoeni RF, Petras A. Double-contrast barium-

enema examination and endoscopy in the detec-

tion of polypoid lesions in the cecum and ascend-

ing colon. Radiology 1982; 144:257–260

27. Williams CB, Macrae FA, Bartram CI. A pro-

spective study of diagnostic methods in adenoma

follow-up. Endoscopy 1982; 14:74–78

28. Anderson N, Cook HB, Coates R. Colonoscopi-

cally detected colorectal cancer missed on barium

enema. Gastrointest Radiol 1991; 16:123–127

29. Bloomfield JA. Reliability of barium enema in

detecting colonic neoplasia. Med J Aust 1981;

1:631–633

30. Brewster NT, Grieve DC, Saunders JH. Double-

contrast barium enema and flexible sigmoidos-

copy for routine colonic investigation. Br J Surg

1994; 81:445–447

31. Connolly DJ, Traill ZC, Reid HS, Copley SJ, Nolan

DJ. The double contrast barium enema: a retro-

spective single centre audit of the detection of col-

orectal carcinomas. Clin Radiol 2002; 57:29–32

32. Culpan DG, Mitchell AJ, Hughes S, Nutman M,

Chapman AH. Double contrast barium enema sen-

sitivity: a comparison of studies by radiographers

and radiologists. Clin Radiol 2002; 57:604–607

33. Gillespie JS, Kelly BE. Double contrast barium

enema and colorectal carcinoma: sensitivity and

potential role in screening. Ulster Med J 2001;

70:15–18

34. 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

35. 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

36. 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 Radiol 1991; 16:345–347

37. 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

38. Ott DJ, Gelfand DW, Wu WC, Kerr RM. Sensi-

tivity of double-contrast barium enema: empha-

sis on polyp detection. AJR 1980; 135:327–330

39. Ott DJ, Gelfand DW, Wu WC, Munitz HA, Chen

Dow

nloa

ded

from

ww

w.a

jron

line.

org

by U

CSF

LIB

& C

KM

/RSC

S M

GM

T o

n 12

/04/

14 f

rom

IP

addr

ess

169.

230.

243.

252.

Cop

yrig

ht A

RR

S. F

or p

erso

nal u

se o

nly;

all

righ

ts r

eser

ved



YM. How important is radiographic detection of

diminutive polyps of the colon? AJR 1986;

146:875–878

40. Ott DJ, Scharling ES, Chen YM, Gelfand DW,

Wu WC. Positive predictive value and posttest

probability of diagnosis of colonic polyp on sin-

gle- and double-contrast barium enema. AJR

1989; 153:735–739

41. Ott DJ, Scharling ES, Chen YM, Wu WC, Gel-

fand DW. Barium enema examination: sensitivity

in detecting colonic polyps and carcinomas. South

Med J 1989; 82:197–200

42. Ferrucci JT. Double-contrast barium enema: use

in practice and implications for CT colonogra-

phy. AJR 2006; 187:170–173

43. Kung JW, Levine MS, Glick SN, Lakhani P,

Rubesin SE, Laufer I. Colorectal cancer: screen-

ing double-contrast barium enema examination

in average-risk adults older than 50 years. Radi-

ology 2006; 240:725–735

44. Rex DK, Cutler CS, Lemmel GT, et al. Colono-

scopic miss rates of adenomas determined by

back-to-back colonoscopies. Gastroenterology

1997; 112:24–28

45. 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

46. Stefansson T, Bergman A, Ekbom A, Nyman R,

Pahlman L. Accuracy of double contrast barium

enema and sigmoidoscopy in the detection of pol-

yps in patients with diverticulosis. Acta Radiol

1994; 35:442–446

47. Tawn DJ, Squire CJ, Mohammed MA, Adam EJ.

National audit of the sensitivity of double-con-

trast barium enema for colorectal carcinoma, using

control charts. For the Royal College of Radiolo-

gists Clinical Radiology Audit Sub-Committee.

Clin Radiol 2005; 60:558–564

48. Wafula JM. Diagnostic yield from barium ene-

mas: a study among patients referred by general

practitioners and hospital outpatient departments.

Br J Gen Pract 1992; 42:330–332

49. Warden MJ, Petrelli NJ, Herrera L, Mittelman A.

Endoscopy versus double-contrast barium enema

in the evaluation of patients with symptoms sug-

gestive of colorectal carcinoma. Am J Surg 1988;

155:224–226

50. 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

51. Irvine EJ, O’Connor J, Frost RA, et al. Prospec-

tive 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

52. Jensen J, Kewenter J, Asztely M, Lycke G,

Wojciechowski J. Double contrast barium enema

and flexible rectosigmoidoscopy: a reliable diag-

nostic combination for detection of colorectal

neoplasm. Br J Surg 1990; 77:270–272

53. Norfleet RG, Ryan ME, Wyman JB, et al. Barium

enema versus colonoscopy for patients with pol-

yps found during flexible sigmoidoscopy. Gastro-

intest Endosc 1991; 37:531–534

54. Thoeni RF, Menuck L. Comparison of barium

enema and colonoscopy in the detection of small

colonic polyps. Radiology 1977; 124:631–635

55. Durdey P, Weston PM, Williams NS. Colonos-

copy or barium enema as initial investigation of

colonic disease. Lancet 1987; 2:549–551

56. 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

57. Cotton PB, Durkalski VL, Pineau BC, et al. Com-

puted tomographic colonography (virtual colonos-

copy): a multicenter comparison with standard

colonoscopy for detection of colorectal neoplasia.

JAMA 2004; 291:1713–1719

58. Dachman AH, Kuniyoshi JK, Boyle CM, et al.

CT colonography with three-dimensional prob-

lem solving for detection of colonic polyps. AJR

1998; 171:989–995

59. Fenlon HM, Nunes DP, Schroy PC 3rd, Barish

MA, Clarke PD, Ferrucci JT. A comparison of

virtual and conventional colonoscopy for the de-

tection of colorectal polyps. N Engl J Med 1999;

341:1496–1503

60. Fletcher JG, Johnson CD, Welch TJ, et al. Opti-

mization of CT colonography technique: pro-

spective trial in 180 patients. Radiology 2000;

216:704–711

61. Gluecker T, Dorta G, Keller W, Jornod P, Meuli R,

Schnyder P. Performance of multidetector com-

puted tomography colonography compared with

conventional colonoscopy. Gut 2002; 51:207–211

62. Hara AK, Johnson CD, MacCarty RL, Welch TJ,

McCollough CH, Harmsen WS. CT colonogra-

phy: single- versus multi-detector row imaging.

Radiology 2001; 219:461–465

63. 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

64. Lefere PA, Gryspeerdt SS, Dewyspelaere J,

Baekelandt M, Van Holsbeeck BG. Dietary fecal

tagging as a cleansing method before CT colonog-

raphy: initial results polyp detection and patient

acceptance. Radiology 2002; 224:393–403

65. Macari M, Bini EJ, Jacobs SL, et al. Significance

of missed polyps at CT colonography. AJR 2004;

183:127–134

66. Macari M, Bini EJ, Jacobs SL, et al. Colorectal

polyps and cancers in asymptomatic average-risk

patients: evaluation with CT colonography. Radi-

ology 2004; 230:629–636

67. Macari M, Bini EJ, Xue X, et al. Colorectal neo-

plasms: prospective comparison of thin-section

low-dose multi-detector row CT colonography and

conventional colonoscopy for detection. Radiology

2002; 224:383–392

68. 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 pol-

yps. AJR 2000; 174:1543–1549

69. McFarland EG, Pilgram TK, Brink JA, et al. CT

colonography: multiobserver diagnostic perfor-

mance. Radiology 2002; 225:380–390

70. Mendelson RM, Foster NM, Edwards JT, Wood

CJ, Rosenberg MS, Forbes GM. Virtual colonos-

copy compared with conventional colonoscopy:

a developing technology. Med J Aust 2000;

173:472–475

71. Morrin MM, Farrell RJ, Raptopoulos V, McGee

JB, Bleday R, Kruskal JB. Role of virtual com-

puted tomographic colonography in patients with

colorectal cancers and obstructing colorectal le-

sions. Dis Colon Rectum 2000; 43:303–311

72. Ginnerup Pedersen GB, Christiansen TE, Bjerre-

gaard NC, Ljungmann K, Laurberg S. Colonosco-

py and multidetector-array computed-tomographic

colonography: detection rates and feasibility.

Endoscopy 2003; 35:736–742

73. Pescatore P, Glucker T, Delarive J, et al. Diagnos-

tic accuracy and interobserver agreement of CT

colonography (virtual colonoscopy). Gut 2000;

47:126–130

74. 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

75. 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

76. Rex DK, Vining D, Kopecky KK. An initial ex-

perience with screening for colon polyps using

spiral CT with and without CT colography (vir-

tual colonoscopy). Gastrointest Endosc 1999;

50:309–313

77. Rockey DC, Paulson E, Niedzwiecki D, et al. Anal-

ysis of air contrast barium enema, computed tomo-

graphic colonography, and colonoscopy: prospec-

tive comparison. Lancet 2005; 365:305–311

78. Royster AP, Fenlon HM, Clarke PD, Nunes DP,

Ferrucci JT. CT colonoscopy of colorectal neo-

plasms: two-dimensional and three-dimensional

virtual-reality techniques with colonoscopic

Dow

nloa

ded

from

ww

w.a

jron

line.

org

by U

CSF

LIB

& C

KM

/RSC

S M

GM

T o

n 12

/04/

14 f

rom

IP

addr

ess

169.

230.

243.

252.

Cop

yrig

ht A

RR

S. F

or p

erso

nal u

se o

nly;

all

righ

ts r

eser

ved


Sosna et al.

correlation. AJR 1997; 169:1237–1242

79. Spinzi G, Belloni G, Martegani A, Sangiovanni

A, Del Favero C, Minoli G. Computed tomo-

graphic colonography and conventional colonos-

copy for colon diseases: a prospective, blinded

study. Am J Gastroenterol 2001; 96:394–400

80. 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

81. Yee J, Akerkar GA, Hung RK, Steinauer-

Gebauer AM, Wall SD, McQuaid KR. Colorec-

tal neoplasia: performance characteristics of

CT colonography for detection in 300 patients.

Radiology 2001; 219:685–692

82. 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

83. Fenlon HM, Nunes DP, Clarke PD, Ferrucci JT.

Colorectal neoplasm detection using virtual

colonoscopy: a feasibility study. Gut 1998;

43:806–811

84. Laghi A, Iannaccone R, Carbone I, et al. Com-

puted tomographic colonography (virtual

colonoscopy): blinded prospective comparison

with conventional colonoscopy for the detection

of colorectal neoplasia. Endoscopy 2002; 34:

441–446

85. Vos FM, van Gelder RE, Serlie IW, et al. Three-

dimensional display modes for CT colonogra-

phy: conventional 3D virtual colonoscopy versus

unfolded cube projection. Radiology 2003;

228:878–885

86. Harvey CJ, Amin Z, Hare CM, et al. Helical CT

pneumocolon to assess colonic tumors: radiologic–

pathologic correlation. AJR 1998; 170: 1439–1443

87. 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

88. Miao YM, Amin Z, Healy J, et al. A prospective

single centre study comparing computed tomog-

raphy pneumocolon against colonoscopy in the

detection of colorectal neoplasms. Gut 2000;

47:832–837

89. 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

90. Neri E, Giusti P, Battolla L, et al. Colorectal

cancer: role of CT colonography in preoperative

evaluation after incomplete colonoscopy. Radiol-

ogy 2002; 223:615–619

91. Cohnen M, Vogt C, Aurich V, Beck A, Hauss-

inger D, Modder U. Multi-slice CT-colonography

in low-dose technique: preliminary results. Rofo

2002; 174:835–838

92. Gluecker T, Meuwly JY, Pescatore P, et al. Effect

of investigator experience in CT colonography.

Eur Radiol 2002; 12:1405–1409

93. Hara AK, Johnson CD, Reed JE, et al. Detection

of colorectal polyps with CT colography: initial

assessment of sensitivity and specificity. Radiol-

ogy 1997; 205:59–65

94. Kay CL, Kulling D, Hawes RH, Young JW, Cotton

PB. Virtual endoscopy: comparison with colonos-

copy in the detection of space-occupying lesions of

the colon. Endoscopy 2000; 32:226–232

95. Luo M, Shan H, Zhou K. CT virtual colonoscopy

in patients with incomplete conventional colonos-

copy. Chin Med J (Engl) 2002; 115:1023–1026

96. Summers RM, Jerebko AK, Franaszek M, Mal-

ley JD, Johnson CD. Colonic polyps: comple-

mentary role of computer-aided detection in CT

colonography. Radiology 2002; 225:391–399

97. Wong BC, Wong WM, Chan JK, et al. Virtual

colonoscopy for the detection of colorectal polyps

and cancers in a Chinese population. J Gastroen-

terol Hepatol 2002; 17:1323–1327

98. Gryspeerdt S, Lefere P, Herman M, et al. CT

colonography with fecal tagging after incomplete

colonoscopy. Eur Radiol 2005; 15:1192–1202

99. Iannaccone R, Laghi A, Catalano C, et al. Com-

puted tomographic colonography without cathar-

tic preparation for the detection of colorectal

polyps. Gastroenterology 2004; 127:1300–1311

100. Kealey SM, Dodd JD, MacEneaney PM, Gibney

RG, Malone DE. Minimal preparation computed

tomography instead of barium enema/colonos-

copy for suspected colon cancer in frail elderly

patients: an outcome analysis study. Clin Radiol

2004; 59:44–52

101. Lefere P, Gryspeerdt S, Marrannes J, Baekelandt

M, Van Holsbeeck B. CT colonography after fe-

cal tagging with a reduced cathartic cleansing

and a reduced volume of barium. AJR 2005;

184:1836–1842

102. 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

103. Thomeer M, Carbone I, Bosmans H, et al. Stool

tagging applied in thin-slice multidetector com-

puted tomography colonography. J Comput Assist

Tomogr 2003; 27:132–139

104. Luboldt W, Mann C, Tryon CL, et al. Computer-

aided diagnosis in contrast-enhanced CT colonog-

raphy: an approach based on contrast. Eur Radiol

2002; 12:2236–2241

105. 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

106. Yoshida H, Nappi J, MacEneaney P, Rubin DT,

Dachman AH. Computer-aided diagnosis scheme

for detection of polyps at CT colonography. Ra-

dioGraphics 2002; 22:963–979

107. 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. AJR

2004; 183:1355–1359

108. Iannaccone R, Laghi A, Catalano C, et al. Detection

of colorectal lesions: lower-dose multi-detector row

helical CT colonography compared with conven-

tional colonoscopy. Radiology 2003; 229:775–781

109. 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 expe-

rience. Eur Radiol 2003; 13:1297–1302

110. 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

Endosc 2004; 60:201–209

111. Iannaccone R, Catalano C, Mangiapane F, et al.

Colorectal polyps: detection with low-dose

multi-detector row helical CT colonography ver-

sus two sequential colonoscopies. Radiology

2005; 237:927–937

112. 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

113. Kalra N, Suri S, Bhasin DK, et al. Comparison of

multidetector computed tomographic colonogra-

phy and conventional colonoscopy for detection

of colorectal polyps and cancer. Indian J Gastro-

enterol 2006; 25:229–232

114. Mulhall BP, Veerappan GR, Jackson JL. Meta-

analysis: computed tomographic colonography.

Ann Intern Med 2005; 142:635–650

115. Morrin MM, Farrell RJ, Kruskal JB, Reynolds K,

McGee JB, Raptopoulos V. Utility of intrave-

nously administered contrast material at CT

colonography. Radiology 2000; 217:765–771

116. Halligan S, Altman DG, Taylor SA, et al. CT

colonography in the detection of colorectal pol-

yps and cancer: systematic review, meta-analysis,

and proposed minimum data set for study level

reporting. Radiology 2005; 237:893–904

117. Sosna J, Morrin MM, Kruskal JB, Lavin PT,

Rosen MP, Raptopoulos V. CT colonography of

colorectal polyps: a metaanalysis. AJR 2003;

181:1593–1598

118. Cappelleri JC, Ioannidis JP, Schmid CH, et al.

Large trials vs meta-analysis of smaller trials:

how do their results compare? JAMA 1996;

Dow

nloa

ded

from

ww

w.a

jron

line.

org

by U

CSF

LIB

& C

KM

/RSC

S M

GM

T o

n 12

/04/

14 f

rom

IP

addr

ess

169.

230.

243.

252.

Cop

yrig

ht A

RR

S. F

or p

erso

nal u

se o

nly;

all

righ

ts r

eser

ved



276:1332–1338

119. LeLorier J, Gregoire G, Benhaddad A, Lapierre J,

Derderian F. Discrepancies between meta-analy-

ses and subsequent large randomized, controlled

trials. N Engl J Med 1997; 337:536–542

120. Pickhardt PJ, Taylor AJ, Kim DH, Reichelderfer M,

Gopal DV, Pfau PR. Screening for colorectal neo-

plasia with CT colonography: initial experience

from the 1st year of coverage by third-party pay-

ers. Radiology 2006; 241:417–425

121. Gluecker TM, Johnson CD, Wilson LA, et al.

Extracolonic findings at CT colonography: evalu-

ation of prevalence and cost in a screening popula-

tion. Gastroenterology 2003; 124:911–916

122. Sosna J, Kruskal JB, Bar-Ziv J, Copel L, Sella T.

Extracolonic findings at CT colonography. Ab-

dom Imaging 2005; 30:709–713

123. Irwig L, Macaskill P, Glasziou P, Fahey M. Meta-

analytic methods for diagnostic test accuracy. J Clin

Epidemiol 1995; 48:119–130; discussion 131–132

124. Thoeni RF, Petras A. Detection of rectal and

rectosigmoid lesions by double-contrast barium

enema examination and sigmoidoscopy: accura-

cy of technique and efficacy of standard over-

head views. Radiology 1982; 142:59–62

125. Arnesen RB, Adamsen S, Svendsen LB, Ra-

aschou HO, von Benzon E, Hansen OH. Missed

lesions and false-positive findings on computed-

tomographic colonography: a controlled pro-

spective analysis. Endoscopy 2005; 37:937–944

126. Reuterskiold MH, Lasson A, Svensson E, Ki-

lander A, Stotzer PO, Hellstrom M. Diagnostic

performance of computed tomography colonog-

raphy in symptomatic patients and in patients

with increased risk for colorectal disease. Acta

Radiol 2006; 47:888–898

F O R Y O U R I N F O R M A T I O N

Unique new customized medical search engine service from ARRS! ARRS GoldMiner™ is a new keyword- and concept-driven search engine that provides instant access to radiologic images published in peer-reviewed journals. For more information, visit http://goldminer.arrs.org.

Dow

nloa

ded

from

ww

w.a

jron

line.

org

by U

CSF

LIB

& C

KM

/RSC

S M

GM

T o

n 12

/04/

14 f

rom

IP

addr

ess

169.

230.

243.

252.

Cop

yrig

ht A

RR

S. F

or p

erso

nal u

se o

nly;

all

righ

ts r

eser

ved

Documents

Critical Analysis of the Performance of Double-Contrast Barium Enema for Detecting Colorectal Polyps ≥ 6 mm in the Era of CT Colonography