Diagnostic accuracy of bowel ultrasonography in patients with inflammatory bowel disease: a systematic review and meta-analysis

Sheza Malika, Sruthi Venugopalanb, Bettina Gabrielle Tenorioc, Shahab R. Khand, Priyadarshini Loganathane, Udayakumar Navaneethanf, Babu P. Mohang

Rochester General Hospital, NY, USA; Duke University School of Medicine, Durham, NC, USA; Ateneo School of Medicine and Public Health, Pasig, Philippines; Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, USA; UT Health, San Antonio, TX, USA; Orlando Digestive Institute, Orlando Health, Orlando, FL, USA; Orlando Gastroenterology PA, Orlando, FL, USA

aInternal Medicine, Rochester General Hospital, NY, USA (Sheza Malik); bDivision of Infectious Diseases and International Health, Duke University School of Medicine, Durham, NC, USA (Sruthi Venugopalan); cAteneo School of Medicine and Public Health, Pasig, Philippines (Bettina Gabrielle Tenorio); dBrigham and Women’s Hospital, Harvard Medical School, Boston, MA, USA (Shahab R. Khan); eInternal Medicine, UT Health, San Antonio, TX, USA (Priyadarshini Loganathan); fOrlando Digestive Institute, Orlando Health, Orlando, FL, USA (Udayakumar Navaneethan); gGastroenterology and Hepatology, Orlando Gastroenterology PA, Orlando, FL, USA (Babu P. Mohan)

Correspondence to: Babu P. Mohan MD, Orlando Gastroenterology PA, 1507 S Hiawassee Rd, STE 105, Orlando, FL, USA 32835, e-mail: dr.babu.pm@gmail.com
Received 28 January 2023; accepted 28 September 2023; published online 20 December 2023
DOI: https://doi.org/10.20524/aog.2024.0842
© 2024 Hellenic Society of Gastroenterology

Abstract

Background Bowel ultrasonography (BUS) is emerging as a promising noninvasive tool for assessing disease activity in inflammatory bowel disease (IBD) patients. We evaluated the diagnostic accuracy of BUS in IBD patients against the gold standard diagnostic method, standard colonoscopy.

Methods Major databases were searched from inception to May 2023 for studies on BUS diagnostic accuracy in IBD. Outcomes of interest were pooled sensitivity, specificity, positive (PPV), and negative (NPV) predictive values. Endoscopic confirmation served as ground truth. Standard meta-analysis methods with a random-effects model and I2 statistics were applied. Risk of bias was assessed using the Quality Assessment of Diagnostic Accuracy Studies-2 tool.

Results Twenty studies (1094 patients) were included in the final analysis. The majority (75%) of studies considered bowel wall thickness >3 mm as abnormal. Endoscopic evaluation was performed between days 3 and 180. The pooled diagnostic accuracy of BUS in IBD was 66% (95% confidence interval [CI] 58-72%; I2=78%), sensitivity was 88.6% (95%CI 85-91%; I2=77%), and specificity 86% (95%CI 81-90%; I2=95%). PPV and NPV were 94% (95%CI 93-96%; I2=25%) and 74% (95%CI 66-80%; I2=95%), respectively. On subgroup analysis, small-intestine contrast-enhanced ultrasonography (SICUS) demonstrated high sensitivity (97%, 95%CI 91-99%; I2=83%), whereas BUS exhibited high specificity (94%, 95%CI 92-96%; I2=0%) and NPV (76%, 95%CI 68-83%; I2=80.9%). Meta-regression revealed a significant relation between side-to-side anastomosis and BUS specificity (P=0.02) and NPV (P=0.004).

Conclusion The high diagnostic accuracy of BUS in detecting bowel wall inflammation suggests utilizing regular BUS as the primary modality, with subsequent consideration of SICUS if clinically warranted.

Keywords Bowel ultrasound, inflammatory bowel disease, meta-analysis

Ann Gastroenterol 2024; 37 (1): 54-63

Introduction

Inflammatory bowel disease (IBD), including ulcerative colitis (UC), and Crohn’s disease (CD), is known to cause recurring episodes of inflammation in the gastrointestinal tract, significantly impacting the quality of life of affected individuals [1]. Along with endoscopic and histological healing, achieving and maintaining clinical remission is critical for the effective management of IBD [2].

Regular monitoring of IBD patients is necessary to maintain symptom stability and proactively prevent disease flares. This involves a combination of clinical symptom assessment, measurement of fecal calprotectin and/or high-sensitivity C-reactive protein levels, and periodic colonoscopy exams [3]. In recent years, we have seen emerging data on the use of bedside bowel ultrasound (BUS) in assessing disease activity in patients with IBD. Office-based BUS seems to hold promise as a noninvasive, convenient, and cost-effective method of monitoring disease activity [4,5].

Changes in bowel wall thickness are used as a marker of inflammation in BUS, and complications such as abscesses or strictures can also be identified [6]. Furthermore, BUS allows for real-time evaluation, making it a useful tool for guiding treatment decisions and monitoring responses to therapy [7,8]. However, despite its potential as a noninvasive tool for evaluating inflammation in patients with IBD, the diagnostic accuracy of BUS has not been extensively validated by meta-analysis. In this study, we aimed to evaluate the pooled diagnostic accuracy of BUS in patients with IBD.

Materials and methods

This study adhered to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines (PRISMA checklist provided in the supplementary material: Appendix 1) [9].

Search strategy

We conducted a comprehensive search of several databases and conference proceedings, including the PubMed, Ovid, Cochrane and CINHAL databases (earliest inception to May 2023). An experienced medical librarian using inputs from the study authors helped with the literature search to identify studies reporting BUS in patients with IBD. The detailed literature search strategy is provided in Appendix 2. Two authors (SM, SV) independently reviewed the titles and abstracts of studies identified in the primary search and excluded studies that did not address the research question, based on prespecified exclusion and inclusion criteria. The full text of the remaining articles was reviewed to determine whether it contained relevant information. Any discrepancy in article selection was resolved by consensus, and in discussion with a co-author (BPM). The bibliographic section of the selected articles, as well as the systematic and narrative articles on the topic, were manually searched for additional relevant articles.

Study selection

In this meta-analysis, we included studies that reported on the clinical and technical outcomes of BUS in patients with IBD and met the following criteria: 1) evaluation of BUS in patients with IBD; and 2) specific information provided on diagnostic accuracy parameters of BUS in assessing IBD disease activity, including IBD flare and postoperative CD recurrence. Studies were included irrespectively of the geography and abstract/manuscript status, as long as they provided the data needed for our analysis. We excluded studies that did not provide sufficient data to allow estimation of outcomes of interest. The standard procedure used as a control was colonoscopy/ileocolonoscopy. Details are provided in Supplementary Table 1. In the case of multiple publications from the same cohort, data from the most recent comprehensive report were included.

Table 1 Study and population characteristics

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Data abstraction and quality assessment

Data on study-related outcomes in the individual studies were abstracted into a standardized form by 2 authors (SV, BT) independently. Assessment of risk of bias in the included studies was carried out using the Quality Assessment of Diagnostic Accuracy Studies - 2 (QUADAS-2) tool, and 2 authors (SM, SRK) did the quality scoring independently [10]. The details of the study quality assessment are summarized in Supplementary Table 2.

Table 2 Cumulative diagnostic accuracy parameters of bowel US in IBD and based on US subtypes

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Outcomes assessed

The primary analysis of this study focused on calculating the pooled rate of diagnostic accuracy parameters of BUS in IBD, such as accuracy, sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV). Subgroup analysis was planned to study the pooled diagnostic accuracy outcomes with standard BUS and small-intestine contrast-enhanced US (SICUS), for CD and UC.

Statistical analysis

We used meta-analysis techniques to calculate the pooled estimate in each case, following the methods suggested by DerSimonian and Laird [11] and using the random-effects model, and our application can be seen to fit within their general approach (where the effect is measured by probability of risk). When the incidence of an outcome was 0 in a study, a correction of 0.01 was added to the number of incident cases before statistical analysis [12]. We assessed heterogeneity between study-specific estimates using 2 methods: Cochrane Q statistics and I2 statistics. [13,14] Values of <30%, 30-60%, 61-75%, and >75% were suggestive of low, moderate, substantial and considerable heterogeneity, respectively [15]. Publication bias was ascertained qualitatively, by visual inspection of the funnel plot, and quantitatively, by the Egger test [16]. All analyses were performed using Comprehensive Meta-Analysis (CMA) software, version 4 (BioStat, Englewood, NJ).

Results

Search results and population characteristics

From a total of 487 citations identified by our literature search, 427 titles were screened and 45 full-length articles were assessed for eligibility. Of these, 20 studies were included in the final meta-analysis [17-36]. The schematic diagram of the study selection is illustrated in Fig. 1.

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Figure 1 PRISMA study selection flow chart

Table 1 describes the population characteristics. A total of 1094 patients were studied. The majority of the patient population were male (66.67%), and the mean age was 40.17 (14-54) years.

Characteristics and quality of included studies

Table 1 describes the characteristics of the included studies. The meta-analysis included 20 independent cohort studies, with a total of 1094 patients: 5 studies (n=291) assessed UC patients, while 15 studies (n=803) assessed the use of BUS in patients with CD, 10 studies in postoperative recurrence of CD (n=436), 2 CD in general (n=181) and 3 in both CD and postoperative CD combined (n=186).

The sonographic examinations were carried out using a convex or linear 2-16 MHz probe. The number of operators varied from 1-6. For the majority (75%) of the studies, a bowel wall thickness >3 mm was considered abnormal. The other parameters assessed for activity on intestinal ultrasound are summarized in Supplementary Table 3. The lag time (time interval between US and endoscopy) was reported in 17 studies. The mean lag time was 22 (range: 3-180) days.

None of the studies were population-based. Only 1 study (Ripolles et al, 2021) was multicenter-based, whereas the rest were single-center. All studies reported clear information regarding the diagnostic accuracy parameters of BUS in IBD: accuracy, sensitivity, specificity, PPV, and NPV. All the studies included were original manuscripts. Supplementary Table 1 provides details of the study quality assessment.

Meta-analysis outcomes

Cumulative pooled rates

The cumulative pooled rate for the diagnostic accuracy of BUS in IBD was 66% (95% confidence interval [CI] 58-72%; I2=78%). The cumulative pooled rate of sensitivity was 88.6% (95%CI 85-91%; I2=77%) (Forest plot, Fig. 2), while the specificity was 86% (95%CI 81-90%; I2=95%) (Forest plot, Fig. 3). The pooled rates of PPV and NPV were 94% (95%CI 93-96%; I2=25%), and 74% (95%CI 66-80%; I2=95%), respectively.

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Figure 2 Forest plot, sensitivity of BUS in IBD: overall and by BUS subtypes

BUS, bowel ultrasound; IBD, inflammatory bowel disease; CI, confidence interval

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Figure 3 Forest plot, specificity of BUS in IBD: overall and by BUS subtypes

BUS, bowel ultrasound; IBD, inflammatory bowel disease; CI, confidence interval

Pooled rates based on BUS, BUS with color Doppler, and SICUS

A subgroup analysis was performed to study the accuracy outcomes of standard BUS, SICUS, and color Doppler BUS in IBD. SICUS demonstrated high sensitivity (97%, 95%CI 91-99%; I2=83%), whereas BUS exhibited high specificity (94%, 95%CI 92-96%; I2=0%), and NPV (76%, 95%CI 68-83%; I2=80.9%).

Pooled rates in CD, postoperative CD recurrence, and UC

A subgroup analysis was conducted based on IBD subtypes to study the outcomes of BUS in CD, postoperative CD recurrence, and UC. The pooled NPV for postoperative CD recurrence was noted to be low at 53% (95%CI 32-72%; I2=95%).

Pooled rates of BS, BS with color Doppler and SICUS in CD

We additionally performed a subgroup analysis to study the pooled diagnostic accuracy of various BUS subtypes exclusively in CD, which included CD and postoperative recurrence of CD. BUS, BUS with color Doppler and SICUS demonstrated excellent sensitivity and PPV. The NPV for SICUS was noted to be low at 50% (95%CI 20-80%; I2=96%).

Meta-regression analysis by anastomosis types in postoperative CD recurrence

A meta-regression analysis was conducted to ascertain if the type of anastomosis in postoperative CD affected the pooled outcomes. In particular, end-to-side anastomosis demonstrated a significant correlation with PPV (P=0.04), while side-to-side anastomosis seemed to demonstrate a significant correlation with specificity (P=0.02) and NPV (P=0.004).

All pooled rates with corresponding I2 heterogeneity are summarized in Table 2. Forest plots are illustrated in Supplementary Fig. 1-12.

Validation of meta-analysis results

Sensitivity analysis

To assess the possible dominant effect of individual studies on the meta-analysis, we excluded one study at a time and analyzed its effect on the main summary estimate. We did not find any single study that significantly affected the outcomes of interest or the heterogeneity.

Heterogeneity

Since pooled diagnostic accuracy parameters were evaluated in this study, the statistical concept of heterogeneity does not apply here. Nevertheless, we have reported the I2 values for all pooled outcomes studied in Table 2, alongside the pooled rates. A high heterogeneity was expected because of variability in BUS technique, BUS subtypes, and IBD subtypes.

Publication bias

A publication bias assessment was deferred in this study as the concept of “sample size” to “effects size” does not apply to diagnostic accuracy studies.

Discussion

Our study, in contrast to those of Rispo et al and Shintaro Sagami et al [37,38], assessed BUS in a broader context, including CD, postoperative CD recurrence, and UC. We also analyzed various BUS subtypes for CD, and our meta-regression explored the impact of different anastomotic surgeries on postoperative CD. This meta-analysis of 20 studies evaluating BUS in patients with IBD demonstrated excellent pooled rates of diagnostic accuracy.

The overall cumulative sensitivity was 88.6%, specificity was 86%, PPV was 94% and NPV was 74%. Additionally, we performed an analysis based on BUS subtypes (such as BUS, BUS with color Doppler, SICUS) and IBD subtypes (CD, postoperative CD, UC). Excellent sensitivity and PPV were demonstrated with each BUS subtype, especially with SICUS. Similarly, excellent sensitivity and PPV were noted with each IBD subtype. To the best of our knowledge, this is the largest pooled quantitative synthesis of diagnostic parameters of BUS in patients with IBD.

BUS is a cost-effective and easy-to-use bedside modality that can provide immediate outpatient clinical data to the gastroenterologist if an IBD flare is suspected in an office-based setting. Furthermore, inpatient resources and time could be potentially saved. Although excellent diagnostic accuracy parameters are demonstrated in this study, the most appropriate BUS tool is currently unknown. We observed a sensitivity of 97% and a PPV of 96% with SICUS; however, the NPV was only 50%. On the other hand, regular BUS demonstrated a sensitivity of 87%, a PPV of 87%, a specificity of 87% and an NPV of 74%. The reported values seem to suggest that regular BUS could be the first-line ultrasound modality in patients with IBD, and SICUS could be a second-line modality for further detailed examinations if clinically warranted. Previous studies have shown a correlation between the qualitative evaluation of SICUS and IBD clinical activity [39-42].

In terms of IBD subtypes, the sensitivity of BUS in CD and postoperative CD combined was 92%, PPV was 94%, specificity was 87% and NPV was 81%. For UC, BUS demonstrated a sensitivity of 89%, a PPV of 94%, a specificity of 77% and an NPV of 80%. These values suggest that BUS demonstrated good diagnostic accuracy values in both CD and UC. However, the UC findings were limited to fewer studies. In patients with CD and postoperative recurrence of CD, SICUS demonstrated a sensitivity and PPV of 96%, though with an NPV of only 50%. Therefore, as stated above, regular BUS could be an appropriate first-line modality, followed by intestinal contrast enhancement if clinically warranted. Data categorized by BUS subtypes were not available for patients with UC. It is worth noting that the existing literature on BUS primarily focuses on its use in CD rather than UC, underscoring the need for more studies in UC patients. Regardless of the type of IBD, a wall thickness of >3 mm was used as the cutoff in the majority of the studies to diagnose a potential inflammation of the bowel wall.

Our meta-regression analysis of various types of anastomotic surgeries in the context of BUS in postoperative CD yielded interesting results. End-to-end, side-to-end, end-to-side and side-to-side anastomoses were assessed for any potential effects on diagnostic accuracy results with BUS in postoperative CD. Although the majority of the parameters were not affected by the type of anastomoses, PPV seemed to have significant association with end-to-side anastomosis, while side-to-side anastomosis seemed to have a significant association with BUS specificity and NPV. Theoretically, one could hypothesize that a side-to-side anastomosis would display a much thicker bowel wall in the presence of inflammation; conversely, a higher NPV could be anticipated in the absence of inflammation. This is a unique finding of this study. However, previous studies have reported variability in this regard, with some reporting no influence of the type of surgical anastomosis on bowel sonography outcomes [22,24]. On the same note, it is important to state that meta-regression analysis is a weak statistical tool and further studies are warranted to establish this finding.

The strengths of this review lie in the systematic literature search with well-defined inclusion criteria, careful exclusion of irrelevant and redundant studies, the inclusion of high-quality studies with detailed extraction of data, and statistics to establish and/or refute the validity of the results of our meta-analysis. Our study is applicable to a broad and diverse clinical setting, with important findings that suggest the utilization of BUS in IBD. This study also had limitations. There was inherent heterogeneity between the different studies in our analysis, owing to the various BUS modalities studied, IBD subtypes and technical differences. Many patient characteristics and clinical symptoms were unaccounted for and might have contributed to the observed heterogeneity. The lag time between BUS exam and confirmatory endoscopy varied widely. While a separate postoperative CD analysis would have been beneficial, it was unfeasible in view of the unsegregated data in the original studies. Our primary aim was to assess the diagnostic accuracy of ultrasound in IBD, leaving real-life studies to address the clinical implications of these findings. Despite these limitations, our study provides valuable information on the pooled diagnostic accuracy of BUS in IBD. The pooled parameters classified by BUS and IBD subtypes are key findings of this study. Furthermore, the meta-regression analysis demonstrating an excellent NPV of BUS in side-to-side anastomosis is a unique finding.

In conclusion, based on this meta-analysis, excellent pooled diagnostic parameters were demonstrated with BUS in patients with IBD. Regular office-based BUS could be the first-line modality, followed by SICUS if clinically warranted. The majority of current data relate to patients with CD and postoperative recurrence of CD, warranting future studies in patients with UC. BUS seemed to yield a good NPV in postoperative CD patients with side-side anastomosis. Future prospective studies are warranted to establish the role of BUS in patients with IBD.

Summary Box

What is already known:

  • Regular monitoring of patients with inflammatory bowel disease (IBD) is vital for maintaining symptom stability and preventing disease flares

  • Bowel ultrasound (BUS) is a real-time evaluation tool used for treatment guidance and therapy monitoring in IBD patients

What the new findings are:

  • Excellent diagnostic accuracy was observed with BUS in patients with IBD, particularly when a cutoff of 3 mm or greater was used to diagnose bowel wall inflammation

  • Small intestine contrast-enhanced ultrasonography (SICUS) exhibited high sensitivity, while BUS demonstrated remarkable specificity and negative predictive value

  • Regular monitoring of IBD patients can be efficiently achieved through office-based BUS, serving as a primary diagnostic modality

  • When necessary, clinicians can consider using SICUS as a follow-up diagnostic tool to complement BUS, ensuring comprehensive disease assessment and personalized care

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Notes

Conflict of Interest: Udayakumar Navaneethan: Consultant to AbbVie, Takeda, Jenssen, BMS, and Pfizer. All other authors declare no conflicts of interest and no financial disclosures