# Understanding the learning curve of intestinal ultrasound in inflammatory bowel disease: A comparative study between novice, regular and expert

Léo Bove, Jérémy Meyer, Michael Collins, Eric Frampas, Arnaud Bourreille, Catherine Le Berre

► To cite this version:

Léo Bove, Jérémy Meyer, Michael Collins, Eric Frampas, Arnaud Bourreille, et al. Understanding the learning curve of intestinal ultrasound in inflammatory bowel disease: A comparative study between novice, regular and expert. Clinics and Research in Hepatology and Gastroenterology, 2025, 49 (3), pp.102548. 10.1016/j.clinre.2025.102548. hal-05075005

HAL Id: hal-05075005

https://hal.science/hal-05075005v1

Submitted on 20 May 2025

HAL is a multi-disciplinary open access
archive for the deposit and dissemination of sci-
entific research documents, whether they are pub-
lished or not. The documents may come from
teaching and research institutions in France or
abroad, or from public or private research centers.

L'archive ouverte pluridisciplinaire HAL, est
destinée au dépôt et à la diffusion de documents
scientifiques de niveau recherche, publiés ou non,
émanant des établissements d'enseignement et de
recherche français ou étrangers, des laboratoires
publics ou privés.

<figure><img src="image_1.png" /></figure>

Distributed under a Creative Commons Attribution 4.0 International License
Original article

# Understanding the learning curve of intestinal ultrasound in inflammatory bowel disease: A comparative study between novice, regular and expert

<figure><img src="image_2.png" /></figure>

Léo Bove<sup>a</sup>, Jérémy Meyer<sup>b</sup>, Michael Collins<sup>a</sup>, Eric Frampas<sup>b</sup>, Arnaud Bourreille<sup>a,c</sup>, Catherine Le Berre<sup>a,c, e</sup>

## ARTICLE INFO

### Keywords:

- Crohn's disease
- Ulcerative colitis

- IBUS-SAS

- MUC score

## ABSTRACT

**Background:** Intestinal ultrasound (IUS) has emerged as a valuable tool for monitoring inflammatory bowel disease (IBD), but its reliability depends on the technical skills of the operator.

**Aims:** This study aimed to assess the IUS learning curve of a novice briefly trained to get him familiarized with the ultrasound machine and normal/abnormal IUS images, and a gastroenterologist with formal general ultrasound training and regular IUS experience (> 200 exams), using an expert radiologist as the gold standard.

**Methods:** The ULTRA-IBD study was a single-center, prospective study involving 50 consecutive IBD patients. Three successive IUS examinations were performed on each patient by the 3 operators. Inter-rater agreement on IUS disease activity was calculated using the intraclass correlation coefficient.

**Results:** The experienced gastroenterologist demonstrated consistently good agreement with the radiologist throughout the study, while the novice failed to go beyond poor agreement after 50 examinations, although a faster learning curve was observed in patients without history of IBD surgery.

**Conclusion:** These findings highlight the difficulty of the technical performance of IUS rather than its interpretation. Comprehensive ultrasound training beforehand and between 50 and 200 examinations of experience are necessary before embarking on IUS.

## Introduction

Current management of inflammatory bowel diseases (IBD) implies regular and objective assessment of disease activity [1]. This tight monitoring with unappealing and/or time-consuming procedures such as conventional endoscopy or magnetic resonance enterography (MRE) [2] may reinforce the negative impact of the disease on the daily life of patients with IBD. Repeated expensive examinations also take part in the economic burden on health care systems through direct and indirect costs [3,4]. Thus, there is a need for the development of non-invasive and affordable monitoring tools.

In the era of shared medical decision-making and patient-centered management, intestinal ultrasound (IUS) appears to be the ideal tool. IUS may serve for IBD diagnosis [5-8], detection of post-operative

recurrence [9], and detection of early treatment response in both ulcerative colitis (UC) [10-12] and Crohn's disease (CD) [13-15]. The combination of IUS and fecal calprotectin is effective in identifying mucosal healing in UC [16]. Conversely, clinical relapse could be predicted using IUS in patients with clinically inactive UC [17].

However, to date, the required experience to be able to reliably perform IUS has not been studied extensively. Most published studies focused on the inter-rater agreement of IUS being performed by well-experienced ultrasonographists [18,19]. The inter-rater agreement of IUS with ultrasonographists of varying experience has been studied more recently, but again the novice operators already had > 200 examinations of experience [20] or attended an 8-hour theoretical course and conducted 50 IUS together with an expert ultrasonographist [21].

The objective of the ULTrasound inter-Reader Agreement in IBD

https://doi.org/10.1016/j.clinre.2025.102548

<footnote><sup>a</sup> Institut des Maladies de l'Appareil Digestif (IMAD), Hépato-Gastro-Entérologie et Assistance Nutritionnelle, Inserm CIC 1413, Nantes Université, CHU Nantes, F-44000 Nantes, France</footnote>

<footnote><sup>b</sup> Central Department of Radiology and Medical Imaging, Nantes Université, CHU Nantes, F-44000 Nantes, Nantes, France</footnote>

<footnote><sup>c</sup> Institut des Maladies de l'Appareil Digestif (IMAD), Inserm UMR 1235, Nantes Université, CHU Nantes, F-44000 Nantes, France</footnote>

<footnote>* Corresponding author at: Catherine Le Berre, Institut des Maladies de l'Appareil Digestif (IMAD), Hépato-Gastro-Entérologie et Assistance Nutritionnelle, Inserm CIC 1413, Inserm UMR 1235, Nantes Université, CHU Nantes, 1 place Alexis Ricordeau, F-44000 Nantes, France.</footnote>

<footnote>E-mail addresses: leo-bove@hotmail.fr (L. Bove), jeremy.meyer@chu-nantes.fr (J. Meyer), michael.collins@chu-nantes.fr (M. Collins), eric.frampas@chu-nantes.fr (E. Frampas), arnaud.bourreille@chu-nantes.fr (A. Bourreille), catherine.leberre@chu-nantes.fr, catherine@leberre.org (C. Le Berre).</footnote>
(ULTRA-IBD) study was to assess, in a real-life setting among patients with IBD, the inter-rater agreement over time on IUS disease activity between three operators of varying experience.

## Methods

### Study design and setting

The ULTRA-IBD study was a single-center, prospective study led in the Nantes University Hospital from April 2023 to January 2024. Patients were recruited consecutively in the outpatient department.

### Ethics

Eligible patients were informed during the visit with their IBD specialist that they could participate in the study. Patient's oral non-opposition was collected and notified in the visit's report. This was a non-interventional study approved by the local research ethics committee (Groupe Nantais d'Éthique dans le Domaine de la Santé [GNEDS]) on January 30th, 2023 (23-11-01-190).

### Study population

Outpatients aged over 18, with an established diagnosis of IBD (CD or UC), coming in for their scheduled visit with their referent IBD specialist, could be included regardless of disease activity. Non-inclusion criteria included ongoing pregnancy, IBD-unclassified, pouchitis, or disease limited to the perineum or to the upper gastrointestinal (GI) tract.

The number of 50 patients to be included was chosen, due to the lack of data about IUS learning curve at the time of study design, based on the cut-off of 20 exams to be qualified being evidenced in studies studying the learning curve for residents in appendicitis or biliary ultrasound [22, 23].

### Clinical data collection

Upon inclusion, immediately after their consultation with the patient, the IBD specialist reported his own assessment of disease activity (physician global assessment) on a VAS between 0 and 10, and on a semi-quantitative 4-item ordinal scale (inactive, mildly active, moderately active, and severely active), having access to all available data in the patient's medical record, including biomarker levels and endoscopy data.

Clinical data were collected at baseline, including age, body mass index (BMI), type of IBD (CD or UC), disease duration, disease location and behavior according to the Montreal classification, history of intestinal resection, presence of stoma, patient-reported outcomes (PRO)-2, ongoing disease-related treatments, history of biologic therapy failure, endoscopic disease activity scores and level of biomarkers (C-reactive protein [CRP] and/or fecal calprotectin [FC]) in the last 3 months if available.

The disease was considered as active based on the PRO-2 (abdominal pain > 1 and/or stool frequency > 3/day in CD; rectal bleeding > 0 and/or stool frequency > 0 in UC) and/or CRP level (> 5 mg/L) and/or FC level (> 250 mg/kg) and/or endoscopically active disease and/or physician global assessment using the semi-quantitative ordinal scale rated as moderately or severely active.

### IUS protocol

Each patient had 3 successive IUS examinations by 3 different operators always performing the IUS in the same order. First, a resident specializing in gastroenterology, hereafter named "GI Trainee", had a 2h-theoretical training to IUS and a 1h-hands-on supervised workshop on healthy volunteers before the beginning of the study. He had no

formal practical training to general ultrasound on patients, and low IUS experience (< 10 exams). These few IUS exams were performed under the supervision of the senior gastroenterologist described below, before the start of the study, to familiarize himself with the ultrasound machine. Half of these IUS exams were performed in active IBD patients, half of them in patients without IBD, to give him an overview of what a normal intestine and an active IBD look like in ultrasound. Second, a senior gastroenterologist specialized in IBD, hereafter named "IBD Specialist", had formal training to general ultrasound (6 months including 1 month of totally supervised examinations) and showed good IUS experience in IBD ('on-the-job' training, > 200 exams). Third, an expert GI senior radiologist, hereafter named "Radiologist" and considered as the 'gold standard', had extensive general abdominal ultrasound experience (12 years) including IUS in IBD (> 500 exams).

Each IUS was performed in the same conditions with the same US machine (LOGIQ™ P9, GE Healthcare) equipped with two probes (abdominal convex, 1-6 MHz and linear, 5-10 MHz), in the supine position without any preparation (no fasting required, no intravenous contrast agents administered). The choice of the most appropriate probe was left to the operator's discretion, depending on the patient's morphology.

All operators were blinded to the physician global assessment of disease activity. Patients were asked not to give any information regarding their disease to the operators during the entire examination period. The only clinical information provided to the operators was the type of IBD and disease location in case of CD (ileal, colonic or ileocolonic). The second and third operators were also blinded to the previous operators' IUS findings for a given patient.

After having performed the 3 successive IUS to each patient, the 3 operators debriefed together in the patient's presence. Continuous feedback with supporting images and/or cineloops was provided to the GI Trainee and/or the IBD Specialist by the Radiologist notably in case of discordance with the 'gold standard'; if no agreement was achieved, the Radiologist could perform the IUS again in presence of the 2 other operators.

### IUS findings

IUS findings were reported by each operator on a case report form including the following criteria: disease activity as assessed by IUS on a VAS between 0 and 10 and on a semi-quantitative 4-item ordinal scale (inactive, mildly active, moderately active, severely active); maximal BWT (mm), CDS with pulse repetition frequency (PRF) around 5-7 m/s (none=0, short signals=1, long signals inside the bowel=2, long signals inside and outside the bowel=3 as in the modified Limberg score [24]), inflammatory mesenteric fat (i-fat) (absent, uncertain, present), BWS (normal, uncertain, focal < 3 cm, extensive ≥ 3 cm), presence of an abscess (no/yes). When several segments were inflamed, these criteria were scored based on the most inflamed one.

Based on these criteria, the validated IBUS-SAS [25] and MUC score [26] were calculated for patients with CD and UC, respectively (see Supplementary data). The cut-offs for defining endoscopic disease activity were > 25.2 using the IBUS-SAS for patients with CD [27] and > 6.2 using the MUC score for patients with UC [28].

Operators also reported the most inflamed segment (ileum, right colon, transverse colon, left colon/sigmoid, not applicable), the duration of IUS examination, and assessed the patient's echogenicity (good, moderate, bad).

### Outcomes

The primary outcome was the inter-rater agreement over time as measured by the VAS of disease activity as scored by the ultrasonographists. Secondary outcomes were the inter-rater agreements over time as measured by (i) the ordinal scale of disease activity, (ii) the IBUS-SAS or MUC score, and (iii) each item composing the scores. The
impact of clinical characteristics on the inter-rater agreement between ultrasonographers was also analyzed for the variables of interest that might impact IUS technical features (type of IBD, disease location and behavior in CD, history of intestinal resection, disease activity and BMI). The correlation between IUS disease activity and other markers of activity was also assessed (PRO-2, biomarkers, physician global assessment).

## Statistics

Continuous variables are described using means and standard deviations (SD) and were compared using the Student t-test when comparing 2 variables, or ANOVA one-way test when comparing 3 variables. Categorical variables are described as headcounts and percentages and were compared using Chi-squared test (or Fisher's exact test if statistically inappropriate).

The inter-rater agreement was assessed through the two-way random, single measure model of intra-class correlation coefficient (ICC(2,1)) for continuous variables, and through weighted kappa coefficient for categorical variables. All analyses were done with the expert Radiologist considered as the gold standard. ICC and kappa values are interpreted according to Cicchetti's values [29]: < 0.4 is poor agreement, 0.4 to 0.6 is moderate agreement, 0.6 to 0.75 is good agreement, > 0.75 is excellent agreement.

The impact of variables of interest on the inter-rater agreement on IUS disease activity (VAS) was analyzed through the comparison of ICCs in the presence and absence of these criteria. ICCs were compared by calculation of the Z-statistic and then of the right-tailed Student's distribution for that Z-statistic. The correlation between IUS disease activity (VAS) and other markers of disease activity (PRO-2, biomarkers [CRP and FC levels], physician global assessment) was assessed using the Spearman's correlation test.

Analyses were performed using Microsoft Excel 2023 (Microsoft Corporation, Redmond, USA) for descriptive statistics, and MedCalc® Statistical Software version 22.023 (MedCalc Software Ltd, Ostend, Belgium) for analytical statistics. For all statistical analyses, α = 0.05 was considered as an acceptable threshold for type I error. Figures were done using GraphPad Prism version 10.0.0 for Windows (GraphPad Software, Boston, Massachusetts, USA).

## Results

### Study population

In total, 150 IUS exams were performed on 47 patients – three patients participated in the study twice. Clinical characteristics are described in Table 1; more details are available in Supplementary data. In total, 15 patients (31.9 %) had an active disease (3 UC, 12 CD), including one patient who participated twice and had an active disease at both time points.

IUS findings by the expert Radiologist and differences in IUS technical features between the 3 operators are described in Supplementary data.

### Inter-rater agreement on IUS disease activity

#### Visual analog scale

The inter-rater agreement over time between IBD Specialist and the gold standard (Radiologist) was good to excellent throughout the study without any “learning curve” effect, with an ICC ranging from 0.61 to 0.79 during the whole study (Fig. 1A). The overall agreement after 50 patients was good with an ICC at 0.71 (95 % CI 0.54–0.83).

By contrast, the inter-rater agreement between GI Trainee and Radiologist was poor with an overall ICC after 50 patients at 0.33 (95 % CI 0.05–0.55). There was no “learning curve” effect (Fig. 1B).

<table><caption>**Table 1**
Clinical characteristics of the study population at baseline (n = 47 patients).</caption><thead><tr><th>Clinical characteristic</th><th>Value</th></tr></thead><tbody><tr><td>Type of IBD, n (%)</td><td></td></tr><tr><td>CD</td><td>36 (76.6)</td></tr><tr><td>UC</td><td>11 (23.4)</td></tr><tr><td>Gender, n (%)</td><td></td></tr><tr><td>Female</td><td>24 (51.0)</td></tr><tr><td>Male</td><td>23 (49.0)</td></tr><tr><td>Disease duration [years], mean (SD)</td><td>15.3 (8.4)</td></tr><tr><td>Age at baseline [years], mean (SD)</td><td>44.5 (15.8)</td></tr><tr><td>BMI<sup>a</sup> [kg/m<sup>2</sup>], mean (SD)</td><td>24.2 (4.2)</td></tr><tr><td>Disease location in patients with CD, n (%)</td><td></td></tr><tr><td>L1 (ileal)</td><td>10 (27.8)</td></tr><tr><td>L2 (colonic)</td><td>10 (27.8)</td></tr><tr><td>L3 (ileocolonic)</td><td>16 (44.4)</td></tr><tr><td>L4 (upper digestive tract)</td><td>3 (8.3)</td></tr><tr><td>Perineal location</td><td>13 (36.1)</td></tr><tr><td>Disease location in patients with UC, n (%)</td><td></td></tr><tr><td>E1 (proctitis)</td><td>1 (9.1)</td></tr><tr><td>E2 (left-sided colitis)</td><td>4 (36.4)</td></tr><tr><td>E3 (extensive colitis)</td><td>6 (54.5)</td></tr><tr><td>History of biologic therapy, n (%)</td><td></td></tr><tr><td>1 biologic</td><td>19 (40.4)</td></tr><tr><td>2 biologics</td><td>9 (19.1)</td></tr><tr><td>≥3 biologics</td><td>11 (23.4)</td></tr><tr><td>Disease behavior in patients with CD, n (%)</td><td></td></tr><tr><td>B1 (inflammatory)</td><td>26 (72.2)</td></tr><tr><td>B2 (stricturing)</td><td>8 (22.2)</td></tr><tr><td>B3 (penetrating)</td><td>2 (5.6)</td></tr><tr><td>History of intestinal resection, n (%)</td><td>11 (23.4)</td></tr><tr><td>Presence of stoma, n (%)</td><td>2 (4.3)</td></tr><tr><td>PRO-2 in patients with CD<sup>b</sup>, mean (SD)</td><td></td></tr><tr><td>Stool frequency</td><td>1.1 (0.7)</td></tr><tr><td>Abdominal pain</td><td>0.3 (0.6)</td></tr><tr><td>PRO-2 in patients with UC<sup>b</sup>, mean (SD)</td><td></td></tr><tr><td>Stool frequency</td><td>0.3 (0.8)</td></tr><tr><td>Rectal bleeding</td><td>0.1 (0.3)</td></tr><tr><td>CRP<sup>b, c</sup> [mg/L], mean (SD)</td><td>3.1 (2.6)</td></tr><tr><td>Fecal calprotectin<sup>b, d</sup>, mean (SD)</td><td>569.2</td></tr><tr><td></td><td>(1170.8)</td></tr><tr><td>Physician global assessment<sup>b</sup></td><td></td></tr><tr><td>VAS [0–10], mean (SD)</td><td>1.0 (1.6)</td></tr><tr><td>Semi-quantitative scale, n (%)</td><td></td></tr><tr><td>Inactive</td><td>29 (58.0)</td></tr><tr><td>Mildly active</td><td>15 (30.0)</td></tr><tr><td>Moderately active</td><td>6 (12.0)</td></tr><tr><td>Severely active</td><td>0 (0.0)</td></tr><tr><td>Treatment modification or optimization in the last 3 months<sup>b, n (%)</sup></td><td>7 (14.0)</td></tr><tr><td>Ongoing IBD-related treatments<sup>b</sup>, n (%)</td><td></td></tr><tr><td>No treatment or exclusive 5-ASA</td><td>9 (18.0)</td></tr><tr><td>azathioprine or methotrexate</td><td>6 (12.0)</td></tr><tr><td>Anti-TNF agents</td><td>25 (50.0)</td></tr><tr><td>Other biologics</td><td>13 (26.0)</td></tr><tr><td>Jak inhibitor</td><td>3 (6.0)</td></tr></tbody></table>

Abbreviations: ASA, Aminosalicylates; BMI, Body mass index; CD, Crohn's disease; CRP, C-reactive protein; IBD, Inflammatory bowel disease; SD, Standard deviation; TNF, Tumor necrosis factor; UC, Ulcerative colitis; VAS, Visual analog scale.

#### Semi-quantitative ordinal scale

Similar results were achieved when using a semi-quantitative 4-item ordinal scale for assessing IUS disease activity. The overall weighted Cohen's kappa for agreement between IBD Specialist and Radiologist after 50 patients was 0.68 (95 % CI 0.55–0.80) (good agreement) (Fig. 1C), while the overall weighted Cohen's kappa for agreement between GI Trainee and Radiologist after 50 patients was 0.23 (95 % CI -0.10–0.40) (poor agreement) (Fig. 1D).

<footnote>a three missing data;</footnote>

<footnote>b calculations made on fifty patients as three patients participated twice in the study;</footnote>

<footnote>c seven missing data;</footnote>

<footnote>d twenty missing data.</footnote>
<figure><img src="image_3.png" /><figcaption>**Fig. 1.** Evolution of inter-rater agreement over time on IUS disease activity: (A) between IBD Specialist and Radiologist using VAS; (B) between GI Trainee and Radiologist using VAS; (C) between IBD Specialist and Radiologist using a semi-quantitative ordinal scale; (D) between GI Trainee and Radiologist using a semi-quantitative ordinal scale.</figcaption></figure>

Abbreviations: GI, Gastrointestinal; IBD, Inflammatory bowel disease; ICC, Intraclass correlation coefficient; IUS, Intestinal ultrasound; VAS, Visual analog scale.

### Disease activity scores

In patients with CD (n = 38), the IBUS-SAS showed almost-excellent agreement between IBD Specialist and Radiologist, whether using the score as a continuous variable (ICC = 0.74 [95 % CI 0.56–0.85]) or considering the cut-off > 25.2 indicating an active disease (kappa = 0.74 [95 % CI 0.53–0.94]). By contrast, the agreement between GI Trainee and Radiologist was poor in both cases (ICC = 0.23 [95 % CI –0.10–0.51] and kappa = 0.17 [95 % CI –0.14–0.48]) (Fig. 2A).

Similarly, in patients with UC (n = 12), the MUC score showed good-to-excellent agreement between IBD Specialist and Radiologist, whether using the score as a continuous variable (ICC = 0.80 [95 % CI 0.20–0.94]) or considering the cut-off > 6.2 (kappa = 0.62 [95 % CI 0.21–1.00]). The agreement between GI Trainee and Radiologist was poor in both cases (ICC = 0.36 [95 % CI –0.24–0.76] and kappa = 0.27 [95 % CI –0.26–0.80]) (Fig. 2A).

### IUS parameters

Out of all four IUS parameters scored, BWT and BWS had the best agreement between IBD Specialist and Radiologist. The inter-rater agreement on BWT stayed in a narrow range of good agreement throughout the study (range of ICC 0.66–0.74) and the overall ICC after 50 patients was at 0.74 (95 % CI 0.59–0.85). The inter-rater agreement on BWS trended towards a “learning curve” effect, with a kappa coefficient steadily rising from 0.48 after 5 patients to 0.83 after 40 patients. The overall kappa coefficient after 50 patients was at 0.74 (95 % CI 0.57–0.91) (good agreement). The other parameters showed poor-to-moderate agreement, with overall kappa values for CDS and i-fat at 0.39 (95 % CI 0.21–0.58) and 0.53 (95 % CI 0.23–0.82), respectively, without any “learning curve” effect (Fig. 2B).

The inter-rater agreement between GI Trainee and Radiologist was poor on all four IUS parameters (ICC for BWT = 0.20 [95 % CI –0.06–0.46]; kappa for CDS = 0.28 [95 % CI 0.04–0.52]; kappa for i-fat

= 0.06 [95 % CI –0.21–0.32]; kappa for BWS = 0.11 [95 % CI –0.13–0.34]), without any “learning curve” effect (Fig. 2C).

### Impact of clinical characteristics on the inter-rater agreement

Among the variables of interest that might impact IUS technical features, the inter-rater agreement significantly differed between operators depending on the type of IBD, CD location and a history of IBD-related surgery; CD behavior, disease activity and the BMI did not significantly impact the inter-rater agreement between the 3 operators, although there was a tendency for better agreement between GI Trainee and Radiologist in case of active disease (versus inactive disease), and in patients with normal BMI (versus patients with overweight) (Fig. 3, details in Supplementary data).

Given the high impact of a history of surgery on the novice performance, the assessment of inter-rater agreement over time was repeated in the overall population after exclusion of patients with a history of surgery (n = 38). Agreement between GI Trainee and Radiologist yielded a clear “learning curve” effect, with an ICC going from 0.21 (poor agreement) to 0.59 (almost-good agreement) with a steady increase throughout the study (Fig. 4). The same learning curve was achieved for ordinal activity scale agreement, although both the nadir kappa (k=-0.07) and the end kappa (k = 0.46) were lower.

### Correlation between IUS disease activity and other markers of disease activity

#### PRO-2

In patients with CD, there was a slight correlation between PRO-2 and Radiologist’s assessment of disease activity through VAS, with Spearman’s ρ = 0.36 (95 % CI 0.05–0.61, p = 0.02). Such correlation was not found for IBD Specialist and GI Trainee, with respective ρ values
<figure><img src="image_4.png" /><figcaption>**Fig. 2.** Inter-rater agreement: (A) between the three operators on IBUS-SAS in CD patients and MUC score in UC patients; (B) between IBD Specialist and Radiologist on each IUS parameter; (C) between GI Trainee and Radiologist on each IUS parameter.</figcaption></figure>

Abbreviations: BWT, Bowel Wall Thickness; BWS, Bowel Wall Stratification; CD, Crohn's disease; GI, Gastrointestinal; IBD, Inflammatory bowel disease; IBUS-SAS, International Bowel Ultrasound Segmental Activity Score; ICC, Intraclass correlation coefficient; IUS, Intestinal ultrasound; MUC, Milan ultrasound criteria; UC, Ulcerative colitis.

<figure><img src="image_5.png" /><figcaption>**Fig. 3.** Variations of inter-rater agreement on IUS disease activity assessed by VAS according to IBD type, CD location, history of surgery, CD behavior, disease activity and BMI.</figcaption></figure>

Abbreviations: BMI, Body mass index; CD, Crohn's disease; IBD, Inflammatory bowel disease; UC, Ulcerative Colitis; ICC, Intraclass correlation coefficient.

<caption>**Fig. 4.** Evolution of inter-rater agreement over time on IUS disease activity assessed by VAS between GI Trainee and Radiologist after exclusion of patients with history of IBD-related surgery.</caption>

Abbreviations: GI, Gastrointestinal; IBD, Inflammatory bowel disease; ICC, Intraclass correlation coefficient; IUS, Intestinal ultrasound; VAS, Visual analog scale.

of 0.15 (95 % CI -0.17-0.45, *p* = 0.35) and 0.29 (95 % CI -0.03-0.56, *p* = 0.07).

In patients with UC, there was a good correlation between PRO-2 and Radiologist's and IBD Specialist's assessments of disease activity through VAS, with Spearman's *ρ* = 0.77 (95 % CI 0.34-0.93, *p* = 0.004) and 0.60 (95 % CI 0.39-0.87, *p* = 0.04), respectively. Such a correlation was not found for GI Trainee, with a *ρ* value of 0.34 (95 % CI -0.29-0.76, *p* = 0.27).
## Biomarkers

For all three operators, Spearman's ρ showed a poor correlation between IUS disease activity assessment and biomarkers. For CRP (43 available data), ρ values were at 0.20 (95% CI -0.10-0.48, *p* = 0.19), 0.14 (95% CI -0.16-0.43, *p* = 0.35) and 0.09 (95% CI -0.22-0.38, *p* = 0.58) for Radiologist, IBD Specialist and GI Trainee, respectively. For FC (30 available data), ρ values were at 0.12 (95% CI -0.25-0.46, *p* = 0.52), 0.20 (95% CI -0.17-0.52, *p* = 0.29), and -0.27 (95% CI -0.57-0.10, *p* = 0.15) for Radiologist, IBD Specialist and GI Trainee, respectively.

## Physician global assessment

There was a significant positive correlation between all three operators and the physician global assessment using the VAS, with the correlation being highest for Radiologist with ρ at 0.60 (95% CI 0.40-0.76, *p* < 0.0001), moderate for IBD Specialist with ρ at 0.40 (95% CI 0.14-0.61, *p* = 0.004), and weakest for GI Trainee with ρ at 0.32 (95% CI 0.05-0.55, *p* = 0.02).

## Discussion

The ULTRA-IBD study analyzed the inter-rater agreement on 50 IUS performed in IBD patients between three operators of varying experience, including an expert gastrointestinal radiologist, an IBD specialist and a resident specializing in gastroenterology starting almost from scratch. The IBD specialist with formal general ultrasound training and already experienced in IUS ('on-the-job' training) showed continuously good agreement with the expert radiologist throughout the study, while the novice resident failed to go beyond poor agreement, although a faster learning curve was observed in patients without history of IBD surgery.

This primarily highlights that being an expert radiologist is not needed to have satisfying performance in point-of-care IUS for assessing disease activity in IBD, and gastroenterologists with sufficient experience can be confident in their results. This is consistent with other studies in which an experience of 200 examinations allowed a gastroenterologist to get accurate IUS results for the assessment of IBD activity as compared to MRE and ileocolonoscopy [30] or to experts with > 1000 IUS examinations of experience [20]. The other key point is the importance of a formal training in general ultrasound with supervised examinations before beginning IUS training. Indeed, for a complete beginner without proper ultrasound training, a total of 50 IUS examinations is not enough to achieve acceptable performance on IBD patients.

This study is the first one to analyze the “learning curve” almost from scratch in IUS performance in a specific population of IBD patients, and most importantly, in a real-life setting. Indeed, a very recent study analyzed the learning curve for interpreting inflammation parameters on IUS using images and cineloops [31], therefore ignoring the technical part of IUS performance.

Our study has limitations, mainly the fact that only one novice trainee and one experienced IUS operator were evaluated against the gold standard in a single center. Thus, we cannot rule out the individual operators' innate capabilities limiting the generalization of results to a wider population of gastroenterologists. Another weakness is the low number of active patients included in the study – less than one third, although it does reflect the reality of IBD outpatients in a tertiary expert center, and makes our results maybe more significant as more active patients would have likely be easier to assess (the novice trainee and the radiologist had a non-significant trend of better agreement in active versus inactive patients). However, another larger study would be required, with more patients, more evenly distributed between active and inactive disease, as well as more trainees, in order to avoid any selection and assessment bias. Finally, few of the included patients had recent endoscopy, which remains the gold standard in IBD activity assessment, to compare our IUS results with.

The important impact of surgery on novice performance is interesting. Overall performance of GI Trainee after excluding the patients with history of surgery increased from poor to moderate-to-good with a clear “learning curve” effect, hinting that performing the examination and working around non-modal anatomy is a more advanced IUS skill than seeing and interpreting standard “cuts” found in the same location in modal anatomy. In other words, performing the IUS examination is harder than interpreting it.

This echoes the recent study by Bezzio et al. in which there was an early gap in performance between trainees who were already well-experienced in general ultrasound and complete ultrasound novices. This reinforces the hypothesis that the key early-level ultrasound skill is technically performing the ultrasound examination itself and understanding the relationship between probe positioning and angulation and internal anatomy, rather than the interpretation of the examination and recognizing normal or pathological characteristics. [21]

Not all the IUS parameters analyzed in our study showed good agreement between IBD Specialist and Radiologist, and our results differ from the literature. While we confirm that BWT is a consistently reliable indicator, BWS was surprisingly the parameter with the best agreement, while CDS scored according to the modified Limberg scale had poor agreement and the aspect of mesenteric fat (i-fat) had moderate agreement.

Apart from BWT which is always evaluated as reproducible and reliable in studies, our other results are in contrast with most of the literature. In the development study of the IBUS-SAS [25], it was the BWS that had poor agreement with *k* = 0.39 while CDS had moderate-to-good agreement with *k* = 0.60. In Fraquelli et al.'s study [18], poor agreement was found for BWS while CDS had good agreement in CD patients. Calabrese et al.'s [19] also found higher reliability for CDS than for BWS, although the difference was less pronounced. Smith et al.'s [20] found higher agreement for i-fat than for other parameters, while BWS and CDS were at similar agreement. One explanation may be the low number of patients with active disease in our study, because CDS and i-fat have been reported as good signs of current inflammation and good predictors of future flare-ups [11,13,15,17,26,32], while BWT and BWS can also be altered in case of inactive disease (sequelae).

In our study, no strong correlation was found between IUS disease activity assessment and common markers of disease activity (PRO-2, CRP, FC) each taken in isolation. However, we showed a good correlation between IUS activity and the physician global assessment of disease activity which is obviously based in part on PRO-2, CRP and FC. Keeping in mind that the IUS were performed in full blindness of current or past biomarkers, symptoms, and clinician assessment, this hints at blinded IUS examination being a good overall assessment tool and not just a surrogate for other individual markers of activity. For FC in particular, as this result differs from previous studies [33-35], this might also be the result of FC measurements being taken at various intervals before the IUS examination, going from the day of the IUS up to 3 months before. Moreover, other studies have suggested that FC and IUS do not provide the same information [36,37], especially in patients with CD involving the small bowel – representing the vast majority of our sample, in whom FC is less sensitive for detecting active disease [38].

With the growing number of IBD patients and the need for accurate evaluation of disease activity, IUS is of the utmost interest both for its reliability, ease of access, time-efficiency, patient tolerability, and low cost. However, our study along with others outlines the need for proper training and experience before getting reliable results in IUS. But what is proper training, and its modalities, is today not well defined.

No formal consensus by a scientific society currently exists on IBD IUS training. The European Federation of Societies for Ultrasound in Medicine and Biology (EFSUMB) guidelines for IUS [39] only mention that “dedicated training is necessary”, with a low quality of evidence. An international consensus using Delphi method was recently published about the objectives to attain in training for achieving competency [40], in which several gastroenterologists and only one radiologist
participated. It is interesting to note that, contrary to what our results tend to show as being harder for novices, this consensus has more statements about *interpretation* skills than about *technical* skills, and no mention is made of being able to successfully identify post-surgical anatomical modifications. The number of examinations necessary to acquire proper experience is also voluntarily not defined, on the argument that this figure will differ from trainee to trainee.

Thus, a formal consensus by a scientific society, addressing these points, should be developed and published to streamline IUS training and ensure that all IBD patients get accurate assessment. A possible model could be the European Society of Gastrointestinal Endoscopy (ESGE) statement for endoscopic ultrasound training [41], which not only defines skills to acquire but actual training modalities, as well as measurable accuracy success and minimum number of procedures to complete. Formal theoretical knowledge (2–3 days intensive hands-on supervised workshop), and proper supervision with on-the-go corrections and suggestions for how to improve – as is the standard by the international bowel ultrasound group training curriculum – should also be recommended. Finally, such a consensus would need to address the points raised earlier about the factors making the examination more difficult for novices, e.g. post-surgery patients.

## Conclusion

In this study comparing the inter-rater agreement of IUS findings in IBD patients between a novice, an experienced gastroenterologist, and an expert radiologist, all blinded to disease activity and history, the experienced gastroenterologist (> 200 exams) demonstrated consistently good agreement with the radiologist throughout the study, while the novice failed to go beyond poor agreement after 50 examinations, although a faster learning curve was observed in patients without history of IBD surgery. These findings highlight the difficulty of the technical performance of IUS rather than its interpretation.

## Glossary

**BMI:** Body Mass Index
**BWS:** Bowel Wall Stratification
**BWT:** Bowel Wall Thickness
**CD:** Crohn's Disease
**CDS:** Color Doppler Signal
**CI:** Confidence Interval
**CRP:** C-reactive protein
**FC:** Fecal Calprotectin
**GI:** Gastrointestinal
**IBD:** Inflammatory Bowel Disease
**IBUS-SAS:** International Bowel Ultrasound Segmental Activity Score
**ICC:** Intraclass Correlation Coefficient i-fat: Inflammatory mesenteric fat
**IUS:** Intestinal Ultrasound
**MUC:** Milan Ultrasound Criteria
**MRE:** Magnetic Resonance Enterography
**PRF:** Pulse Repetition Frequency
**PRO:** Patient-Reported Outcomes
**SD:** Standard Deviation
**UC:** Ulcerative Colitis
**VAS:** Visual Analog Scale

## Author contributions

**LB, CLB:** conceptualization, data curation, formal analysis, investigation, methodology, validation, writing – original draft.

**JM:** conceptualization, investigation, writing – review and editing.

**MC, AB:** investigation, writing – review and editing.

**EF:** writing – review and editing.

All the authors read and approved the final version of the

manuscript.

## Data availability

The data that support the findings of this study are available on request from the corresponding author.

## CRediT authorship contribution statement

**Léo Bove:** Writing – original draft, Validation, Methodology, Investigation, Formal analysis, Data curation, Conceptualization.

**Jérémy Meyer:** Writing – review & editing, Investigation, Conceptualization.

**Michael Collins:** Writing – review & editing, Investigation.

**Eric Frampas:** Writing – review & editing.

**Arnaud Bourreille:** Writing – review & editing, Investigation.

**Catherine Le Berre:** Writing – original draft, Validation, Methodology, Investigation, Formal analysis, Data curation, Conceptualization.

## Declaration of competing interest

Dr. Collins declares lecture or consulting fees from Abbvie, Celltrion, Janssen, and Takeda.

Prof. Bourreille declares lecture or consulting fees from Abbvie, Amgen, Celltrion, Ferring, Fresenius Kabi, Galapagos, Gilead, Janssen, MSD, OSE Immunotherapeutics, Pfizer, Roche, Takeda, and Tillotts.

Dr. Le Berre has served as a consultant for Abbvie, Celltrion, Janssen, Gilead and Takeda; has received payment for lectures from Abbvie, Amgen, Celltrion, Ferring, Fresenius Kabi, Galapagos, Janssen, Lilly, MSD, Nordic Pharma, Pfizer, and Takeda; reports grant support from Abbvie and Takeda; has received meeting support fees from Abbvie, Celltrion, Ferring, Fresenius Kabi, Galapagos, Janssen, Lilly, MSD, Pfizer, Sandoz, and Takeda.

The other authors have nothing to disclose.

## Funding sources

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

## Acknowledgements

We thank all the patients who participated in the study, as well as Bastien Perrot, methodologist and biostatistician at Nantes University for his practical advice during the conception of the study and the data analysis.

## Supplementary materials

Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.clinre.2025.102548.

## References

[1] Turner D, Ricciuto A, Lewis A, D'Amico F, Dhaliwal J, Griffiths AM, et al. STRIDE-II: an update on the selecting therapeutic targets in Inflammatory Bowel Disease (STRIDE) Initiative of the International Organization for the Study of IBD (IOIBD): determining therapeutic goals for treat-to-target strategies in IBD. Gastroenterology 2021;160:1570-83. https://doi.org/10.1053/j.gastro.2020.12.031.

[2] Buisson A, Gonzalez F, Poullenot F, Nancey S, Sollellis E, Fumery M, et al. Comparative acceptability and perceived clinical utility of monitoring tools: a nationwide survey of patients with inflammatory bowel disease. Inflamm. Bowel Dis. 2017;23:1425-33. https://doi.org/10.1097/MIB.00000000000001140.

[3] Burisch J, Vardi H, Schwartz D, Friger M, Kiudelis G, Kupčinskas J, et al. Healthcare costs of inflammatory bowel disease in a pan-European, community-based, inception cohort during 5 years of follow-up: a population-based study. Lancet Gastroenterol Hepatol 2020;5:454-64. https://doi.org/10.1016/S2468-1253(20)30012-1.

[4] Burisch J, Zhao M, Odes S, De Cruz P, Vermeire S, Bernstein CN, et al. The cost of inflammatory bowel disease in high-income settings: a Lancet Gastroenterology &
Hepatology Commission. Lancet Gastroenterol Hepatol 2023;8:458-92. https://doi.org/10.1016/S2468-1253(23)00003-1.

[5] Rispo A, de Sire R, Mainenti PP, Imperatore N, Testa A, Maurea S, et al. David against Goliath: direct comparison of handheld bowel sonography and magnetic resonance enterography for diagnosis of Crohn's Disease. Inflamm Bowel Dis 2023; 29:563-9. https://doi.org/10.1093/ibd/izac116.

[6] Brodersen JB, Jensen MD, Juel MA, Kjeldsen J, Knudsen T, Rafaelsen SR. Intestinal ultrasound in patients with suspected Crohn's disease - results of a prospective evaluation by trainees. Scand J Gastroenterol 2023;58:1405-11. https://doi.org/10.1080/00365521.2023.2234538.

[7] Taylor SA, Mallett S, Bhatnagar G, Morris S, Quinn L, Tomini F, et al. Magnetic resonance enterography compared with ultrasonography in newly diagnosed and relapsing Crohn's disease patients: the METRIC diagnostic accuracy study. Health Technol Assess 2019;23:1-162. https://doi.org/10.3310/hta23420.

[8] Xu C, Li L, Zhang Y, Wang R, Zhang H. Diagnostic accuracy of different cross-sectional imaging techniques for disease location and activity in Crohn's disease and external validation and comparison of MARIAs and IBUS-SAS. Abdom Radiol 2023;48:821-32. https://doi.org/10.1007/s00261-022-03751-7.

[9] Rispo A, Imperatore N, Testa A, Nardone OM, Luglio G, Caporaso N, et al. Diagnostic accuracy of ultrasonography in the detection of postsurgical recurrence in Crohn's Disease: a systematic review with meta-analysis. Inflamm Bowel Dis 2018;24:977-88. https://doi.org/10.1093/ibd/izy012.

[10] Maaser C, Petersen F, Helwig U, Fischer I, Roessler A, Rath S, et al. Intestinal ultrasound for monitoring therapeutic response in patients with ulcerative colitis: results from the TRUST&UC study. Gut 2020;69:1629-36. https://doi.org/10.1136/gutjnl-2019-319451.

[11] de Voogd FA, Bots SJ, van Wassenaer EA, de Jong M, Pruijt MJ, D'Haes GR, et al. Early intestinal ultrasound predicts clinical and endoscopic treatment response and demonstrates drug-specific kinetics in moderate-to-severe ulcerative colitis. Inflamm Bowel Dis 2023;izad274. https://doi.org/10.1093/ibd/izad274.

[12] Allocca M, Dell'Avalle C, Furfaro F, Zilli A, D'Amico F, Peyrin-Biroulet L, et al. Early intestinal ultrasound predicts long-term endoscopic response to biologics in ulcerative colitis. J Crohn's Colitis 2023;17:1579-86. https://doi.org/10.1093/ecco-jcc/ijjad071.

[13] de Voogd F, Bots S, Gecse K, Gilja OH, D'Haes G, Nylund K. Intestinal ultrasound early on in treatment follow-up predicts endoscopic response to anti-tnfα treatment in Crohn's disease. J Crohn's Colitis 2022;16:1598-608. https://doi.org/10.1093/ecco-jcc/ijjad072.

[14] Kucharzik T, Wittig BM, Helwig U, Börner N, Rössler A, Rath S, et al. Use of intestinal ultrasound to monitor Crohn's Disease activity. Clin Gastroenterol Hepatol 2017;15:535-42. https://doi.org/10.1016/j.cgh.2016.10.040. e2.

[15] Kucharzik T, Wilkens R, D'Agostino M-A, Maconi G, Le Bars M, Lahaye M, et al. Early ultrasound response and progressive transmural remission after treatment with Ustekinumab in Crohn's disease. Clin Gastroenterol Hepatol 2023;21:153-63. https://doi.org/10.1016/j.cgh.2022.05.055. e12.

[16] Yzet C, Meudjo E, Brazier F, Hautefeuille V, Moreau C, Robert C, et al. Intestinal ultrasound, fecal calprotectin, and their combination to predict endoscopic mucosal healing in ulcerative colitis: a real-life cross-sectional study. Inflamm Bowel Dis 2024;izae145. https://doi.org/10.1093/ibd/izae145.

[17] Maeda M, Sagami S, Tashima M, Yamana Y, Karashima R, Miyatani Y, et al. Milan ultrasound criteria predict relapse of ulcerative colitis in remission. Inflam Intest Dis 2023;8:95-104. https://doi.org/10.1159/000532052.

[18] Fraquelli M, Sarno A, Girelli C, Laudi C, Buscarini E, Villa C, et al. Reproducibility of bowel ultrasonography in the evaluation of Crohn's disease. Dig Liver Dis 2008; 40:860-6. https://doi.org/10.1016/j.dld.2008.04.006.

[19] Calabrese E, Kucharzik T, Maaser C, Maconi G, Strobel D, Wilson SR, et al. Real-time interobserver agreement in bowel ultrasonography for diagnostic assessment in patients with Crohn's Disease: an international multicenter study. Inflamm Bowel Dis 2018;24:2001-6. https://doi.org/10.1093/ibd/izy091.

[20] Smith RL, Taylor KM, Friedman AB, Su HY, Con D, Gibson PR. Interrater reliability of the assessment of disease activity by gastrointestinal ultrasound in a prospective cohort of patients with inflammatory bowel disease. Eur J Gastroenterol Hepatol 2021;33:1280-7. https://doi.org/10.1097/MEG.00000000000002253.

[21] Bezzio C, Saibeni S, Vernero M, Furfaro F, Monteleone M, Ribaldone D, et al. The learning curve for using intestinal ultrasonography. Dig Liver Dis 2024. https://doi.org/10.1016/j.dld.2024.01.192. 0.

[22] Kim J, Kim K, Kim J, Yoo J, Jeong W, Cho S, et al. The learning curve in diagnosing acute appendicitis with emergency sonography among novice emergency medicine residents. J Clin Ultrasound 2018;46:305-10. https://doi.org/10.1002/jcu.22577.

[23] Seyedhoseini J, Nasrelari A, Mohammadrezaei N, Karimialavijeh E. Inter-rater agreement between trained emergency medicine residents and radiologists in the

examination of gallbladder and common bile duct by ultrasonography. Emerg Radiol 2017;24:171-6. https://doi.org/10.1007/s10140-016-1468-0.

[24] Limberg B. Diagnosis of chronic inflammatory bowel disease by ultrasonography. J Gastroenterol 1999;37:495-508.

[25] Novak KL, Nylund K, Maaser C, Petersen F, Kucharzik T, Lu C, et al. Expert consensus on optimal acquisition and development of the International Bowel ultrasound segmental activity score [IBUS-SAS]: a reliability and inter-rater variability study on intestinal ultrasonography in Crohn's disease. J Crohns Colitis 2021;15:609-16. https://doi.org/10.1093/ecco-jcc/jjaa216.

[26] Allocca M, Fiorino G, Bonovas S, Furfaro F, Gilardi D, Argollo M, et al. Accuracy of Humanitas ultrasound criteria in assessing disease activity and severity in ulcerative colitis: a prospective study. J Crohns Colitis 2018;12:1385-91. https://doi.org/10.1093/ecco-jcc/jjy107.

[27] Dragoni G, Gottin M, Innocenti T, Lynch EN, Bagnoli S, Macri G, et al. Correlation of ultrasound scores with endoscopic activity in Crohn's Disease: a prospective exploratory study. J Crohns Colitis 2023;17:1387-94. https://doi.org/10.1093/ecco-jcc/ijjad068.

[28] Allocca M, Filippi E, Costantino A, Bonovas S, Fiorino G, Furfaro F, et al. Milan ultrasound criteria are accurate in assessing disease activity in ulcerative colitis: external validation. United Eur Gastroenterol J 2021;9:438-42. https://doi.org/10.1177/2050640620980203.

[29] Cicchetti DV. The precision of reliability and validity estimates re-visited: distinguishing between clinical and statistical significance of sample size requirements. J Clin Exp Neuropsychol 2001;23:695-700. https://doi.org/10.1076/jcen.23.5.695.1249.

[30] Wright EK, Wang I, Wong D, Bell SJ, Connell WR, Thompson AJ, et al. Accuracy of point-of-care intestinal ultrasound for Crohn's disease. Australas J Ultrasound Med 2020;23:176-82. https://doi.org/10.1002/ajum.12218.

[31] Madsen GR, Tolsgaard MG, Gecse K, Novak K, Boscardin C, Attauabi M, et al. Classifying inflammation on intestinal ultrasound images and cineloops - A learning curve study. J Crohn's Colitis 2024;ijjae112. https://doi.org/10.1093/ecco-jcc/ijjae112.

[32] Allocca M, Dal Buono A, D'Alessio S, Spaggiari P, Garlatti V, Spinelli A, et al. Relationships between intestinal ultrasound parameters and histopathologic findings in a prospective cohort of patients with Crohn's disease undergoing surgery. J Ultrasound Med 2023. https://doi.org/10.1002/jum.16191.

[33] St-Pierre J, Delisle M, Kheirkhahrahimabadi H, Goodall TM, Bryant RV, Christensen B, et al. Bedside intestinal ultrasound performed in an inflammatory bowel disease urgent assessment clinic improves clinical decision-making and resource utilization. Crohns Colitis 2023;36:5. https://doi.org/10.1093/crocol/otad050. otad050.

[34] You M-W, Moon SK, Lee YD, Oh SJ, Park SJ, Lee CK. Assessing active bowel inflammation in Crohn's disease using intestinal ultrasound: correlation with fecal calprotectin. J Ultrasound Med 2023;42:2791-802. https://doi.org/10.1002/jum.16317.

[35] Yzet C, Brazier F, Hautefeuille V, Richard N, Decrombecque C, Sarba R, et al. Non-invasive evaluation of mucosal healing by intestinal ultrasound or fecal calprotectin is efficient in Crohn's disease: a cross-sectional study. Clin Res Hepatol Gastroenterol 2024;48:102387. https://doi.org/10.1016/j.clinre.2024.102387.

[36] Allocca M, Dell'Avalle C, Zilli A, Furfaro F, D'Amico F, Jairath V, et al. Ultrasound remission after biologic induction and long-term endoscopic remission in Crohn's disease: a prospective cohort study. ECLInicalMedicine 2024;71:102559. https://doi.org/10.1016/j.eclinm.2024.102559.

[37] Mathieu K, Junda J, Minet-Quinard R, Coban D, Dodel M, Pereira B, et al. Intestinal ultrasonography as an alternative to Fecal Calprotectin to monitor patients with Crohn's Disease: experience from a novice sonographer. Dig Dis Sci 2024;69: 3402-12. https://doi.org/10.1007/s10620-024-08548-w.

[38] D'Arcangelo G, Imondi C, Terrin G, Catassi G, Aloi M. Is fecal calprotectin a useful marker for small bowel Crohn Disease? J Pediatr Gastroenterol Nutr 2021;73: 242-6. https://doi.org/10.1097/MPG.00000000000003151.

[39] Nylund K, Maconi G, Hollerweger A, Ripolles T, Pallotta N, Higginson A, et al. EFSUMB recommendations and guidelines for gastrointestinal ultrasound. Ultraschall Med 2017;38:e1-15. https://doi.org/10.1055/s-0042-115853.

[40] Madsen GR, Wilkens R, Boysen T, Burisch J, Bryant R, Carter D, et al. The knowledge and skills needed to perform intestinal ultrasound for inflammatory bowel diseases-an international Delphi consensus survey. Aliment Pharmacol Ther 2022;56:263-70. https://doi.org/10.1111/apt.16950.

[41] Badaoui A, Teles De Campos S, Fusaroli P, Gincul R, Kahaleh M, Poley J-W, et al. Curriculum for diagnostic endoscopic ultrasound training in Europe: european Society of Gastrointestinal Endoscopy (ESGE) Position Statement. Endoscopy 2024; 56:222-40. https://doi.org/10.1055/a-2224-8704.