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DOI: 10.1148/radiol.2361040799
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(Radiology 2005;236:95-101.)
© RSNA, 2005

Evidence-based Practice

Role of US in Detection of Crohn Disease: Meta-Analysis1

Mirella Fraquelli, MD, PhD, Agostino Colli, MD, Giovanni Casazza, PhD, Silvia Paggi, MD, Alice Colucci, MD, Sara Massironi, MD, Piergiorgio Duca, MD and Dario Conte, MD

1 From the Postgraduate School of Gastroenterology, IRCCS Ospedale Maggiore, Via F. Sforza 35, 20122 Milan, Italy (M.F., S.P., A. Colucci, D.C.); Department of Internal Medicine, Ospedale A. Manzoni, Lecco, Italy (A. Colli, S.M.); and Department of Clinical Sciences, Ospedale L. Sacco, Milan, Italy (G.C., P.D.). Received May 3, 2004; revision requested July 20; revision received August 2; accepted August 26. Supported by the Associazione Amici della Gastroenterologia del Granelli and a special grant from the CARIPLO Foundation. Address correspondence to M.F. (e-mail: mfraquelli{at}yahoo.it).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To evaluate the accuracy of ultrasonography (US) in the detection of Crohn disease in adults by systematically reviewing both cohort studies (those including patients whose clinical characteristics were consistent with those caused by an inflammatory bowel disease) and case-control studies (those in which patients with Crohn disease were compared with patients with other bowel diseases or healthy control subjects).

MATERIALS AND METHODS: The MEDLINE, EMBASE, and Cochrane Library databases were used to retrieve all the cross-sectional studies that assessed the diagnostic accuracy of US against that of one of several predefined reference standards (ie, radiologic, endoscopic, or histologic findings). The studies that fulfilled the inclusion criteria were identified, and their methodological quality was evaluated. Of the 2860 primary studies identified, two case-control and five cohort series fulfilled the inclusion criteria. Statistical analysis was performed by using the summary receiver operating characteristic (SROC) model.

RESULTS: The ranges of US sensitivity and specificity for the diagnosis of Crohn disease reported for the included series were 75%–94% and 67%–100%, respectively; the heterogeneity of these values prevented the calculation of a cumulative value. The SROC curve revealed a clear cutoff effect that depended on the chosen bowel wall thickness threshold. Sensitivity and specificity of 88% and 93%, respectively, were achieved when a bowel wall thickness threshold greater than 3 mm was used, and sensitivity and specificity of 75% and 97%, respectively, were achieved when a threshold greater than 4 mm was used.

CONCLUSION: US examination seems appropriate for confirming or excluding Crohn disease as a diagnosis in a clinical context characterized by a pretest probability of Crohn disease that ranges from 12% to about 60%. In particular, for Crohn disease limited to the ileum, US may represent a valid alternative to the small-bowel series, while for colonic involvement US may be useful in ruling out the diagnosis.

© RSNA, 2005


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Crohn disease is an inflammatory bowel disease that may involve various portions of the gastrointestinal tract, although ileal and/or colonic involvement is most frequent. In addition to relying on clinical findings, the diagnosis of Crohn disease relies on information yielded by a combination of various imaging and endoscopic techniques and/or histologic examination (1). In particular, ultrasonography (US) of the bowel loops is a noninvasive procedure whose ability to depict bowel wall abnormalities has recently been improved by the availability of high-frequency transducers.

The role of US in the diagnosis of Crohn disease has been investigated extensively (2–47), but the estimates of its diagnostic accuracy have been based on the results of studies that differed in terms of design, population characteristics, and reference standards. Furthermore, most of the currently available data have been obtained from studies that included patients with a previous diagnosis of Crohn disease but lacked an appropriate control population, thus making it possible to calculate only the positive predictive value of US examination.

The purpose of our meta-analysis was to evaluate the accuracy of US in detection of Crohn disease in adults by systematically reviewing both cohort studies (those including patients whose clinical characteristics were consistent with those of an inflammatory bowel disease) and case-control studies (those in which patients with Crohn disease were compared with patients with other bowel diseases or healthy control subjects).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Data Sources
The primary study retrieval sources were MEDLINE (which, at the time we performed our literature search, included articles published from January 1966 through the 1st week of April 2004); EMBASE (which included articles published from January 1988 through the 1st week of April 2004); the Cochrane Library database (which included systematic reviews published from January 1988 through the 1st issue of 2004); and reference lists from all available review articles, primary studies, and proceedings of major meetings published between January 1995 and the 1st week of April 2004. The search was not restricted to articles published in a certain language or languages. In cases of incomplete data, the original material was directly requested from the study authors.

The search strategy, which included the use of both Medical Subject Headings, or MeSH, and free terms, is detailed in Figure 1.



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  		Figure 1. MEDLINE search strategy used in the study.

 
Study Selection Criteria
The aim of our search was to identify cross-sectional studies that met the following two criteria: First, the study had been performed with patients who had clinical (eg, chronic diarrhea, abdominal pain) and/or laboratory data (increased levels of acute phase reactants) that were suggestive of an inflammatory bowel disease. Second, the study examined compared the accuracy of US in the diagnosis of Crohn disease with the accuracy of one of the following reference standards: (a) radiologic evidence, at small-bowel series, of a peculiar ileal pattern whose severity increased with the stage of the disease, with a characteristic cobblestone appearance of the mucosa, luminal narrowing with retrodilation, and possible coexistence of fistulas and/or sinus tracts in the more advanced stages of disease (1); (b) a pattern macroscopically consistent with that of Crohn disease at endoscopy (1); and/or (c) appropriately classified histologic findings obtained after colonic or ileal surgery or endoscopic procedures (1).

Consideration was given to both cohort studies aimed at detecting Crohn disease among patients whose clinical characteristics were consistent with those of inflammatory bowel disease and case-control studies aimed at assessing the accuracy of US in discriminating patients with Crohn disease from patients with other bowel diseases or healthy individuals or in enabling exclusion of an underlying disease.

Types of Participants and Interventions
The cohort studies included patients with clinical (eg, chronic diarrhea, abdominal pain) and laboratory features that were possibly related to an underlying inflammatory bowel disease, whereas the case-control studies included patients known to have Crohn disease as well as either patients with other organic or functional bowel diseases or healthy control subjects. Both study types assessed the diagnostic accuracy of US against at least one of the reference standards defined above.

Inclusion and Exclusion Criteria
In this systematic review, we included studies with the following features: (a) involvement of either a population representative of the spectrum of the disease or a population of patients with Crohn disease and either patients with other bowel diseases or healthy control subjects; (b) use of an appropriate reference standard; and (c) presence of data regarding sensitivity and specificity values or the possibility of deriving such values from the results analysis. Reports of studies involving children and duplicate reports were not included.

Quality Assessment of Primary Studies
The included studies were assessed in terms of their methodologic quality to explain the possible sources of heterogeneity. In agreement with previously defined standards (48,49), the criteria we used to rate the quality of the studies were as follows: spectrum composition (whether the sample composition [ie, clinical population or case control] was properly described); verification (whether exhaustive details concerning the method of applying the reference standard were given; verification was considered complete when all patients were examined by using the same reference standard and partial when all patients were not thus examined); interpretation of test results (whether blinded or not); method of patient selection (whether consecutive or not); methods of data collection and reporting (whether data collection was prospective, retrospective, or "unknown" [in case of doubt]); and whether details concerning the test, reference standard, or population were provided (sufficiently or insufficiently). In addition, data concerning intra- and interobserver variability, when detailed in the studies, were considered as quality parameters.

Outcome Measures
The outcome measures for diagnostic accuracy were sensitivity and specificity.

Review Methods
The search was independently performed by two reviewers (M.F. and S.P.). The review included all of the studies that were initially identified in the manner described above, and the results of the review were analyzed by five reviewers (M.F., S.P., A. Colli, S.M., and A. Colucci). In addition, each of the five reviewers reexamined the selected studies to identify those that fulfilled the inclusion criteria and then evaluated the methodologic quality of the studies by using reported parameters, as defined above (49). The data concerning the types of participants, the interventions, and the outcome measures were independently extracted by each reviewer. Any discrepancy was openly discussed by the reviewers, and, in cases of further disagreement, the judgment of an independent gastroenterologist with 30 years of clinical experience (D.C.) was considered final.

Statistical Analysis
The sensitivity (true-positive rate) and specificity (true-negative rate) of each study was recorded, and exact 95% confidence intervals based on a binomial distribution were calculated. The homogeneity of the true-positive and the true-negative rates was evaluated by using the {chi}2 or exact test (50) and a significance level of .1 (51). In cases of heterogeneity, the relationship between sensitivity and specificity was evaluated by using the Spearman correlation coefficient, {rho} (52), and assuming a between-study variation in cutoff points when {rho} was less than –0.3 (53).

When a between-study variation in cutoff points was observed, the summary receiver operating characteristic (SROC) curve was calculated (52). Maximum joint sensitivity and specificity was defined as the point on the SROC curve that intersected a diagonal line running from the top left corner to the bottom right corner of the diagram and represented the point at which sensitivity and specificity had the same value. A perfect test has a maximum joint sensitivity and specificity score of 1.0, whereas a nondiagnostic test has a score of 0.5 or less.

A subgroup analysis was predefined to explain the possible sources of clinical heterogeneity between studies on the basis of the study design, the percentage prevalence of Crohn disease (ie, the pretest probability) (<10%, 10%–40%, or >40%), the reference standard used, the percentage prevalence of irritable bowel syndrome (<10%, 10%–40%, or >40%), the bowel wall thickness cutoff (>3 vs >4 mm [a value of ≤ 3 mm is considered normal]) used, the disease location (ileal, ileocolonic, or colonic), the percentage frequency of ulcerative colitis (<10%, 10%–40%, or >40%), the frequency of the US transducer used (≤5 vs >5 MHz), and the year of study publication (before or during 1990 vs after 1990).

So that we could analyze the presence of a publication bias, we constructed a funnel plot of the individual studies, with log diagnostic odds ratios plotted against sample size. An asymmetric funnel plot would suggest that other small studies may have been conducted but not published because of unfavorable results (54).

The data were analyzed by using SAS, version 8.2 (SAS Institute, Cary, NC).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Included Studies
Of the 2860 primary study reports identified, 2147 represented nonduplicated study reports and were retrieved in abstract form because of a 25% overlap between the MEDLINE and EMBASE databases. Because 2103 of these abstracts were considered not pertinent, only 44 of the studies were retrieved as full texts. Of these 44 studies, 27 were excluded because of the inappropriateness of the population studied (eg, there was a lack of control subjects) (n = 12) (6,11,14,15,18,22,25–28,35,40), a lack of or use of an inappropriate reference standard (n = 6) (10,12,16,21,34,36), the unavailability of sensitivity or specificity values (n = 4) (23,24,32,47), data duplication (n = 1) (20), or the involvement of a pediatric population (n = 4) (9,17,31,33). So that we could obtain a pooled value, we excluded an additional 11 studies (2,5,7,13,19,29,30,37–39,41) in which the US sign of bowel wall thickness was not considered as a single variable and/or a precise bowel wall thickness threshold level was not provided. Thus, at the end of the process, the final analysis included five cohort (3,4,42–44) and two case-control studies (45,46) whose main characteristics are detailed in Table 1. In detail, the prevalence of Crohn disease (ie, the pretest probability of the disease) in the five cohort studies ranged between 12% and 64%.


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  		TABLE 1. Characteristics of Seven Studies of Diagnostic Performance of US in Crohn Disease

 
Sensitivity and Specificity
The sensitivity and specificity values of US for the diagnosis of Crohn disease in the seven studies, together with their 95% confidence intervals, are detailed in Figure 2. Because of the heterogeneity of the values, we could not calculate a pooled value; however, the presence of an inverse correlation between the sensitivity and specificity values ({rho} = –0.43) allowed us to construct an SROC curve of summary data (Fig 3) that revealed overall sensitivity and specificity ranges of 75%–94% and 67%–100%, respectively. More specifically, for a bowel wall thickness cutoff value of greater than 3 mm, sensitivity and specificity, respectively, were 88% and 93% (positive likelihood ratio, 12.5; negative likelihood ratio, 0.12), whereas for a thickness greater than 4 mm, the values were 75% and 97% (positive likelihood ratio, 25; negative likelihood ratio, 0.25). In addition, the maximum joint sensitivity and specificity of the SROC curve was 0.882. Furthermore, analysis of the data according to study design (Fig 2) revealed that the degree of variability between values was even greater for the case-control studies. The presence of a clear cutoff effect related to the chosen bowel wall thickness threshold was more evident when only the cohort studies, which better fit the curve, were taken into account.



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  		Figure 2. Graph shows the sensitivity and specificity of US in the detection of Crohn disease reported for the seven studies. Reimund et al (46) and Sonnenberg et al (45) were case-control studies; the other five studies were prospective cohort studies. Mean values ({blacksquare}) and 95% confidence intervals (error bars) are indicated; the heterogeneity of the results prevented the calculation of a cumulative value.

 


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  		Figure 3. SROC curve for detection of Crohn disease with US according to both study design and bowel wall thickness (BWT) cutoff level. Black circles = prospective cohort studies with a bowel wall thickness cutoff of greater than 3 mm, black triangles = case-control study with a bowel wall thickness cutoff of greater than 3 mm. The gray circles indicate prospective cohort studies with a bowel wall thickness cutoff of greater than 4 mm, and the gray triangle indicates a case-control study with a bowel wall thickness cutoff of greater than 4 mm. Overall, data revealed a clear cutoff effect that depended on the chosen bowel wall thickness threshold. Sensitivity decreased and specificity increased when the bowel wall thickness threshold changed from greater than 3 to greater than 4 mm.

 
Bias and Observer Variability
Furthermore, so that we could assess a possible publication bias, we designed an inverted funnel plot (Fig 4). As is evident from the figure, the lack of studies with a limited number of patients (ie, <100) and a log diagnostic odds ratio of less than 4 accounted for the asymmetry of the curve.



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  		Figure 4. Inverted funnel plot of individual studies with log diagnostic odds ratio, or log(DOR), plotted against sample size (ie, number of patients in study). The lack of studies with a limited number of patients (ie, <100) and log diagnostic odds ratios of less than 4 accounts for the evident asymmetry of the funnel plot and suggests that other small studies may have been conducted but not published because of unfavorable results.

 
Results of the quality assessment (Table 2) revealed that the same reference standard was used with all patients in three studies (3,42,45), thus leading to complete verification corresponding to a lack of bias; in the remaining four studies (4,43,44,46), the verification was partial in that different reference standards had been used for different subsets of patients. Blinding was practiced in all but one study (43), and patient recruitment was consecutive in five studies (3,4,42,44,46). All study reports detailed the characteristics of both the equipment and the procedures used for US, whereas the characteristics of the reference standard examination were properly described in only one report (42).


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  		TABLE 2. Results of Assessment of Methodological Quality of Seven Studies of Diagnostic Performance of US in Crohn Disease

 
Finally, all but one study lacked details concerning intra- and interobserver variability; when these variables were reported, they had been calculated only for a subset of patients (45).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
Data from primary studies that assessed the accuracy of US in the detection of Crohn disease in adults were summarized in the present review.

Different findings at US—for example, bowel wall thickness, the pattern of vascularization, the presence of abdominal fluid, and/or the presence of enlarged mesenteric lymph nodes—have been used for the diagnosis of Crohn disease. However, because not all such findings were reported for all of the included studies, we considered only the accuracy of bowel wall thickness and decided to include only those studies that involved use of a precise bowel wall thickness cutoff level so that we could obtain a pooled value of the operative characteristics of the test itself.

The significant heterogeneity of the estimates of sensitivity (75%–94%) and specificity (67%–100%) precluded the possibility of obtaining a cumulative value of diagnostic accuracy. The SROC analysis revealed the presence of a clear cutoff effect based on the different bowel wall thickness thresholds (>3, >4, >5, and ≥7 mm, respectively) used in different studies (3,4,42–46). This threshold effect became even more evident in the predefined subgroup analysis of the cohort studies. When a bowel thickness cutoff value of greater than 3 mm was used, the sensitivity of the test increased to 88%–89% (negative likelihood ratio, 0.1), supporting the use of this cutoff value in a diagnostic strategy of exclusion; conversely, the use of a cutoff value of greater than 4 mm led to a high specificity value (97%–100%) (positive likelihood ratio, 25), making the use of this value highly appropriate for a confirmatory strategy.

On the basis of the above findings, the actual role of US in the diagnosis of Crohn disease depends on the prevalence of the disease (ie, the pretest probability); in the five cohort studies included in the present review, the pretest probability ranged from 12% to 64%, mainly as a consequence of differences in both the selection criteria and the characteristics of the referral center. For example, if a pretest probability of the disease of 12% is assumed—that is, if a hypothetical patient with low risk is considered—US evidence of a bowel wall thickness of 3 mm or less could enable one to rule out the disease because the posttest probability of the disease would decrease to about 1%. Conversely, US evidence of a bowel wall thickness of greater than 4 mm in a high-risk population with a pretest probability of 64% would increase the posttest probability of Crohn disease to up to 97%.

As far as the relevance of the study design to the study results is concerned, our SROC curve analysis revealed that the variability of the estimates was related mainly to the case-control studies (45,46), whose position was more distant from the curve. In fact, case-control studies lead to less reproducible estimates and usually result in overestimation of the accuracy of a diagnostic test (49).

We performed an ad hoc subgroup analysis to consider the possible relationships between clinical heterogeneity and differences in population characteristics, US features or technical characteristics, and type of reference standard used. Differences in Crohn disease prevalence can unpredictably affect US sensitivity and specificity values owing to the variability of prevalence across settings (55). The disease location could also have influenced the diagnostic estimates, as suggested by the results of three series (6,40,47). Another factor with a possible effect on US sensitivity and specificity could be the use of a recently introduced high-frequency probe responsible for a time-related technical improvement. A high-frequency transducer was used in two of the included series (44,46), but comparison of these series with the other series was precluded by different study designs and thresholds of normal bowel thickness.

In cases of colonic Crohn disease, another factor that is potentially relevant in modifying US operative characteristics could be the prevalence of ulcerative colitis, which is the most frequent cause of chronic colonic inflammation and is often characterized by the presence of bowel wall thickening, in the evaluated population; this prevalence could possibly account for confusing results. However, in the cohort studies included in the present review, the actual prevalence of ulcerative colitis (<10%) was lower than would be expected in an unselected population. Because most of the included studies were conducted at tertiary referral centers, it is highly probable that patients presenting with chronic bloody diarrhea would have been immediately examined and given a diagnosis with endoscopy. A low sensitivity value (38%) and a high specificity value (98%) were reported for the single study (to our knowledge) that evaluated the operative characteristics of US in the detection of ulcerative colitis (44). At present, however, data in a population that reflects a more realistic clinical scenario—that is, a population with a higher prevalence of ulcerative colitis—are lacking.

Overall, the lack or paucity of data for all of the predefined variables considered in our study made it impossible to evaluate their possible influence on study outcome.

Furthermore, our present study had possible limitations that should be considered. First, this study lacked an adequate reference standard for the confirmation of Crohn disease. For example, in case of ileal Crohn disease, even when results of small-bowel series (currently considered the reference standard for Crohn disease with ileal involvement) are consistent, the diagnosis must eventually rely on histologic findings if false-positive results are to be avoided. In addition, the sensitivity and specificity estimates derived from our systematic review were limited to the diagnostic role of US, and no inferences were made concerning disease staging. A second limitation of this review was the lack of data on the performance of US in differentiating Crohn disease from other organic bowel diseases (eg, intestinal tuberculosis, ulcerative colitis, indeterminate colitis) that are also characterized by increased bowel wall thickness (41,56). As an example, if we consider a different clinical context, such as that in an area with a high prevalence of intestinal tuberculosis, the accuracy of US in the diagnosis of Crohn disease will obviously be reduced as a consequence of a reduction in the specificity of the technique that is related to the increase in the frequency of false-positive results. Properly designed primary studies (57) should be performed to overcome this limitation.

Finally, the asymmetry of the funnel plot, which was consistent with the lack of studies that both had a small sample size and revealed a low diagnostic accuracy of US, suggests the presence of a possible publication bias in that it is highly probable that such series are less likely to be published than are small studies with more appealing results.

In conclusion, in the presence of both clinical and laboratory findings leading to a pretest probability of Crohn disease that ranges from 12% to about 60%, as in the series analyzed in our systematic review (3,4,42–46), the operative characteristics of US bowel examination, especially in the presence of two different bowel wall thickening thresholds, seem appropriate for confirming or ruling out the diagnosis. In particular, in cases of ileal Crohn disease, US could represent a valid alternative to small-bowel series, not only in predicting the presence of ileal Crohn disease but also in revealing the extent of the disease (a strong correlation between US and radiographic findings of extent of disease has recently been demonstrated [47]). Furthermore, compared with small-bowel series, US has the advantage of being noninvasive, less costly, and easily repeatable and thus can be very useful in following up patients, especially in monitoring the response to treatment. Additionally, in the setting of colonic Crohn disease, US examination may be useful in ruling out the disease, even if the final diagnosis still must rely on endoscopic findings.


   FOOTNOTES
 

Abbreviations: SROC = summary receiver operating characteristic

Authors stated no financial relationship to disclose.

Author contributions: Guarantors of integrity of entire study, M.F., D.C.; study concepts, M.F., A. Colli, G.C., S.P., D.C.; study design, M.F., D.C., A. Colli; literature research, S.P., M.F., A. Colli; data acquisition, S.P., A. Colucci; S.M., P.D.; data analysis/interpretation, M.F., A. Colli, D.C., S.P.; statistical analysis, G.C., P.D.; manuscript preparation, M.F., S.P., A. Colli, S.M., D.C.; manuscript definition of intellectual content, M.F., A. Colli, D.C.; manuscript editing, M.F., S.P., A. Colucci, A. Colli, S.M.; manuscript revision/review, M.F., D.C., A. Colli, P.D.; manuscript final version approval, all authors


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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