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DOI:10.2214/AJR.07.2099
AJR 2008; 190:374-385
© American Roentgen Ray Society

Original Research

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
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
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
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
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
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 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
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).


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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

 

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
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
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.


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

 

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.


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

 

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).


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

 


Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
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
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 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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