Introduction

Endoscopic postoperative recurrence (POR) of Crohn's disease (CD) occurs in up to 70% of patients within the first 12 months after ileocecal resection (ICR) with anastomosis if no prophylactic therapy is started. Early postoperative prophylaxis with thiopurines or anti-TNF agents may lower this number to 30-50%. However, scarce data on POR are available in the long-term.

Aims & Methods

To evaluate the long-term outcomes of patients without endoscopic POR at the first endoscopic assessment.
We performed a retrospective, observational study including consecutive CD patients undergoing ICR with anastomosis at four European referral centres since 1998. All patients underwent a first endoscopic assessment within 18 months from ICR demonstrating no endoscopic POR (Rutgeerts score i0-i1), and had a clinical follow-up ³24 months including at least one further endoscopic assessment. Main outcomes were endoscopic (Rutgeerts >i1), clinical (development of digestive symptoms together with a disease recurrence seen at endoscopic or radiological examination that prompted changes in the treatment) and surgical (new intestinal resection) POR, need for rescue therapy and “delayed POR” (any need for rescue therapy or clinical or surgical POR) during follow-up.

Results

One-hundred eighty-five patients were included (133 Rutgeerts i0, 52 Rutgeerts i1), of whom 88 (48%) started thiopurines or 17 anti-TNF (9%) early after surgery and 80 (43%) patients did not start any prophylactic therapy. No clinical risk factors for POR were present in 38%, whereas 27% met ³1 (active smoking, penetrating disease, perianal disease and/or previous ICR). By the last endoscopic assessment that was performed a median (IQR) of 58 (24-133) months after the first one, endoscopic POR was observed in 39% (17% i3-i4). Cumulative probability of remaining free of endoscopic POR in the total cohort was 97% at 1 year, 68% at 5 years and 61% at 10 years, from the index colonoscopy. During a median follow-up of 104 (IQR, 55-196) months, 30% of the patients developed clinical POR and 31% required rescue treatment (thiopurines in 14 patients, biological therapies in 43 and dose-escalation in 1). Cumulative probability of remaining free of clinical POR for the total cohort was 97.5% at one year, 81.8% at 5 years and 72.1% at 10 years. Finally, 5% of the patients had surgical POR at the end of follow-up.
In multivariate analysis, no risk factors were observed for endoscopic, severe endoscopic and surgical POR. However, early prophylactic treatment was protective for clinical POR (OR 0.54 [95%CI 0.32-0.96]; p=0.026) and need for rescue therapy (OR 0.43 [95%CI 0.23-0.79]; p=0.007), whereas a Rutgeerts score i0 at index ileocolonoscopy was the only factor that prevented from “delayed POR” (OR 2.00 [95%CI 1.18-3.31]; p=0.009).

Conclusion

Most patients without endoscopic POR after ICR will remain free of endoscopic and clinical POR in the long-term, although the risk steadily increases over time. Moreover, early postoperative prophylactic therapy seems to prevent the long-term risk of clinical POR and reduces the need for rescue therapies. Therefore, periodical non-invasive monitoring seems a suitable strategy for patients without endoscopic POR at the first postoperative endoscopic assessment, particularly if early prophylaxis was started or no endoscopic lesions (i0) were observed at index ileocolonoscopy.

Introduction

The Rutgeerts score, developed three decades ago, is used to assess postoperative endoscopic recurrence in patients with Crohn’s disease (CD) following ileocolonic resection with an end-to-end anastomosis.¹ However, contemporary surgical techniques have introduced new anatomical locations – the ileal body and ileal inlet – which were not accounted for in the original Rutgeerts score.² Additionally, the original Rutgeerts score has demonstrated limited inter-observer reliability.³ To address these limitations, an updated Rutgeerts score, incorporating new anatomical sites, has been proposed. According to the updated Rutgeerts score lesions restricted to the ileal inlet, or the ileal body can no longer be scored as i2a.² While the updated Rutgeerts score offers improved assessment of inflammation after an ileocolonic resection, its reproducibility has not yet been validated.

Aims & Methods

The aim of our study was to evaluate the inter- and intra-observer reliability of the updated Rutgeerts score.
We conducted a retrospective analysis of 183 patients with CD (48% male, median age 36.8 years) who underwent video-recorded ileocolonoscopy within 14 months of resection with ileocolonic anastomosis. An expert reader MF selected and scored videos of ileocolonoscopies, which were then used as the gold standard. After receiving a two-hour training with a set of ten videos eight expert gastroenterologists reviewed and scored the videos. Each reader assessed 92 videos, including 23 videos that were re-scored after at least one month. Based on the gold standard, inter- and intra-rater agreement was calculated across all score levels and for each score level. Inter-rater reliability was assessed using Fleiss' kappa, and intra-rater reliability using Cohen’s kappa, both with and without application of linear weights.

Results

The probability of perfect agreement between two readers across all scores was 0.604 (95% CI: 0.559-0.649). The chance-corrected inter-observer agreement based on Fleiss’ kappa with linear weights across all scores was 0.619 (95% CI: 0.562-0.676). The strongest inter-observer agreement was observed for the i2a score, with a value of 0.736 (95% CI: 0.647-0.826), while the weakest was seen for the i1 score (0.357, 95%CI: 0.225-0.489).
Intra-rater reliability with a Cohen’s kappa was 0.688 (0.609-0.767), and with weighted kappa was 0.831 (0.758-0.868). The overall agreement rate was 76.0% (69.1%-82.0%).

	Categorical		Ordinal
	Estimate	95%CI	Estimate	95%CI
All levels	0.604	(0.559;0.649)	0.882	(0.866;0.897)
i0	0.633	(0.467;0.800)	0.884	(0.824;0.945)
i1	0.357	(0.225;0.489)	0.829	(0.758;0.899)
i2a	0.736	(0.647;0.826)	0.925	(0.896;0.954)
i2b	0.502	(0.439;0.566)	0.856	(0.834;0.877)
i3	0.487	(0.351;0.623)	0.859	(0.798;0.920)
i4	0.715	(0.606;0.824)	0.894	(0.854;0.934)

Table 1. Summary of agreement across score levels: Agreement for all scores and by individual score levels, based on the gold standard (defined as the scores given by an expert reader MF). Categorical agreement reflects only perfect agreement. Ordinal agreement applies linear weights, assigning less weight to minor disagreements and more to larger ones.

Conclusion

The updated Rutgeerts score demonstrates good agreement and substantial inter- and intra-rater reliability in assessing postoperative endoscopic recurrence in CD, supporting its potential for broader adaptation in both clinical practice and research settings.

References

1. Rutgeerts P, Geboes K, Vantrappen G, Beyls J, Kerremans R, Hiele M. Predictability of the postoperative course of Crohn’s disease. Gastroenterology. 1990;99(4):956-963. doi:10.1016/0016-5085(90)90613-6
2. Rivière P, Bislenghi G, Vermeire S, et al. Postoperative Crohn’s Disease Recurrence: Time to Adapt Endoscopic Recurrence Scores to the Leading Surgical Techniques. Clin Gastroenterol Hepatol. 2022;20(6):1201-1204. doi:10.1016/j.cgh.2022.02.025
3. Marteau P, Laharie D, Colombel JF, et al. Interobserver Variation Study of the Rutgeerts Score to Assess Endoscopic Recurrence after Surgery for Crohn’s Disease. Journal of Crohn’s and Colitis. 2016;10(9):1001-1005. doi:10.1093/ecco-jcc/jjw082

Introduction

Postoperative recurrence (POR) in patients with Crohn’s disease (CD) occurs mostly within the first year after ileocolic resection. POR can be prevented efficiently with early postoperative use of thiopurines or anti-TNF agents. Recently, it has been reported that medical prevention for POR might also reduce the risk of delayed POR.

Aims & Methods

Aims: To assess the long-term risk of a second intestinal resection for CD according to the use of early medical prevention of POR.
Methods: Adult patients with CD who underwent a first ileocolic resection with ileocolic anastomosis between 1990 and 2020 and at least one year of clinical follow-up were identified from the Spanish ENEIDA registry. Patients in whom ileocolic resection was due to cancer were excluded. Medical prevention of POR was defined as any immunomodulator or biological agent started within the first 6 months after the ileocolic resection and maintained for at least 3 months. Medical treatment of POR was defined as any immunomodulator or biological agent started at least 6 months after the index surgery. Surgical POR was defined as the need for a second intestinal resection at least 6 months after the first ileocolic resection.

Results

A total of 5,084 patients were included. Main characteristics of the whole cohort were as follows: 51% men, 39% active smokers at the first surgery, 40% penetrating and 40% stricturing behaviour, 25% perianal disease. 34% exposed to immunomodulators and 25% to biologicals before the first surgery. Median disease duration at first surgery of 3 years (range, 0-46), median age at index surgery was 35 years (range, 9-89), median follow-up until second resection or last visit of 125 months (range 6-408). 55% followed medical prophylaxis (33% thiopurines, 10% biological monotherapy, 12% combotherapy). Surgical POR occurred in 17% of the whole cohort. Kaplan-Meier survival curves showed a significantly higher risk of surgical POR among patients who did not follow medical prevention (P<0.0001), whether with thiopurines (P<0.0001) or biologicals (P<0.0001). No differences in surgical POR were observed between medical prevention with biologicals in monotherapy or combotherapy (P=0.588) nor between thiopurines and biologicals (P=0.114). In the Cox regression analysis, medical prevention with thiopurines (HR 0.65, 95%CI 0.56-0.76; P<0.0001) and medical treatment with biologicals (HR 0.87, 95%CI 0.80-0.94; P<0.0001) or thiopurines (HR 0.88, 95%CI 0.78-0.99; P<0.032) were independent protective factors of surgical POR.

Conclusion

Early medical prevention (particularly with thiopurines) seems to have a long-term beneficial effect on preventing surgical POR. Our findings support the systematic use of early medical prevention instead of endoscopy-driven strategies in the postoperative setting of CD.

Introduction

Accurate and timely endoscopic evaluation is critical for the management of postoperative Crohn’s disease (CD). Although numerous established and novel indices exist, their relative operating properties and the optimal instrument for routine use in clinical and research settings are unknown.

Aims & Methods

We characterised the reliability and responsiveness of both historical and novel endoscopic indices using centrally assessed ileocolonoscopy videos from a randomised controlled trial comparing infliximab versus placebo for preventing postoperative CD (PREVENT; NCT01190839). Three blinded central readers independently assessed 70 videos from the PREVENT trial using the Rutgeerts and modified Rutgeerts scores, POCER index, REMIND score, Simple Endoscopic Score for CD (SES-CD), and the CD Endoscopic Index of Severity (CDEIS). Indices were scored separately for the neoterminal ileum, the anastomosis (including the blind loop of a side-to-side anastomosis), and the distal colonic segment. Intra- and inter-rater reliability was quantified using the intraclass correlation coefficient (ICC) and was interpreted using the Landis and Koch benchmarks.¹ Responsiveness was quantified using the win probability (WinP), defined as the probability of a patient receiving infliximab having a better endoscopic score than a patient receiving placebo, and interpreted using Cohen’s benchmarks.²

Results

Inter-rater reliability was substantial for the Rutgeerts (ICC 0.74 [95% CI: 0.62-0.83]) and modified Rutgeerts scores (0.79 [0.68-0.86]), ileal REMIND score (0.79 [0.67-0.87]), SES‑CD (0.79 [0.70-0.86]), and CDEIS (0.80 [0.72-0.86]). Inter-rater reliability was moderate for the POCER index (ICC 0.49 [0.26-0.64]) and fair for the anastomotic REMIND score (0.30 [0.14-0.47]). Intra-rater reliability was almost perfect for all indices (ICC≥0.81) (Table 1). The Rutgeerts (WinP 0.77 [95% CI: 0.65-0.86]) and modified Rutgeerts scores (WinP 0.81 [0.69-0.89]), ileal REMIND score (WinP 0.83 [0.72-0.91]), SES-CD (WinP 0.80 [0.66-0.89]), and CDEIS (WinP 0.75 [0.61-0.86]) demonstrated a large degree of responsiveness when treatment assignment was the criterion for change. The POCER index (WinP 0.54 [0.43-0.65]) and the anastomotic REMIND score (WinP 0.53 [0.42-0.64]) had a small degree of responsiveness. The reliability and responsiveness of all indices were consistently lower when assessed at the anastomosis or distal colon compared to the neoterminal ileum.

Table 1. Reliability and responsiveness of endoscopic scores

Index	Inter-rater ICC (95% CI)a	Intra-rater ICC (95% CI)a	WinP (95% CI)b,c	WinP (95% CI)b,d
Rutgeerts score	0.74 (0.62, 0.83)	0.90 (0.85, 0.94)	0.77 (0.65, 0.86)	0.72 (0.57, 0.83)
Modified Rutgeerts score	0.79 (0.68, 0.86)	0.92 (0.88, 0.96)	0.81 (0.69, 0.89)	0.68 (0.52, 0.81)
POCER index	0.49 (0.26, 0.64)	0.89 (0.78, 0.95)	0.54 (0.43, 0.65)	0.61 (0.46, 0.74)
REMIND - Ileal	0.79 (0.67, 0.87)	0.91 (0.85, 0.96)	0.83 (0.72, 0.91)	0.71 (0.55, 0.83)
REMIND - Anastomotic	0.30 (0.14, 0.47)	0.81 (0.71, 0.89)	0.53 (0.42, 0.64)	0.62 (0.47, 0.75)
SES-CD	0.79 (0.70, 0.86)	0.93 (0.87, 0.96)	0.80 (0.66, 0.89)	0.70 (0.54, 0.82)
CDEIS	0.80 (0.72, 0.86)	0.91 (0.86, 0.95)	0.75 (0.61, 0.86)	0.70 (0.56, 0.81)
Overall VAS	0.81 (0.72, 0.87)	0.90 (0.84, 0.94)	0.80 (0.67, 0.88)	0.71 (0.55, 0.83)
a Interpreted according to the Landis and Koch benchmarks1: poor = <0; slight = 0.0–0.20; fair = 0.21–0.40; moderate = 0.41–0.60; substantial = 0.61–0.80; and almost perfect = 0.81–1.00. b WinPs of 0.56, 0.64, and 0.71 correspond to Cohen’s effect sizes of 0.2, 0.5, and 0.8, which are the benchmarks for “small”, “moderate”, and “large” effects, respectively.2 c Using treatment assignment as the criterion for change. d Using clinical recurrence as the criterion for change. Abbreviations: WinP, Win probability; CDEIS, Crohn’s Disease Endoscopic Index of Severity; CI, confidence interval; ICC, intraclass correlation coefficient; POCER, Postoperative Crohn's endoscopic recurrence; SES-CD, Simple Endoscopic Score for Crohn’s Disease; VAS, visual analogue scale.

Conclusion

Existing endoscopic indices are reliable and responsive for assessing postoperative CD activity in the neoterminal ileum but are suboptimal for assessing the anastomosis or distal colon.

References

1. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977; 33 (1):159-174.
2. Zou G, Zou L, Qiu SF. Parametric and nonparametric methods for confidence intervals and sample size planning for win probability in parallel-group randomized trials with Likert item and Likert scale data. Pharm Stat 2023; 22 (3):418-439.

Disclosure

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