Key points

Introduction

Approximately 70% of patients with CD undergo surgical resection for the treatment of medically refractory disease or its complications during their lifetime. The sickest cohort of CD patients experiences rapid postoperative relapse at the anastomotic site, which can lead to repeated surgeries. A majority of CD patients have a reconstruction of the intestine after surgery, where a surgical anastomosis connects the upstream and downstream segments of bowel, whereas other patients require an ostomy. Over the past 2 decades, the types of surgical anastomoses used in CD reconstruction have changed, where end-to-side and end-to-end anastomoses have been surpassed by the more rapidly created side-to-side anastomoses (antiperistaltic orientation and isoperistaltic orientation). Although high-definition white light endoscopes have allowed for enhanced assessment of the postoperative mucosal surface, there is limited information at this time that helps inform and guide gastroenterologists regarding endoscopic assessment of surgically altered anatomy, particularly in regard to the different types of anastomoses. This article provides a comprehensive review of the timing and purpose of endoscopic evaluation in postoperative CD patients and provides pragmatic information regarding interpretation of endoscopic findings at the different types of surgical anastomoses after ileocecal resection.

Introduction

Approximately 70% of patients with CD undergo surgical resection for the treatment of medically refractory disease or its complications during their lifetime. The sickest cohort of CD patients experiences rapid postoperative relapse at the anastomotic site, which can lead to repeated surgeries. A majority of CD patients have a reconstruction of the intestine after surgery, where a surgical anastomosis connects the upstream and downstream segments of bowel, whereas other patients require an ostomy. Over the past 2 decades, the types of surgical anastomoses used in CD reconstruction have changed, where end-to-side and end-to-end anastomoses have been surpassed by the more rapidly created side-to-side anastomoses (antiperistaltic orientation and isoperistaltic orientation). Although high-definition white light endoscopes have allowed for enhanced assessment of the postoperative mucosal surface, there is limited information at this time that helps inform and guide gastroenterologists regarding endoscopic assessment of surgically altered anatomy, particularly in regard to the different types of anastomoses. This article provides a comprehensive review of the timing and purpose of endoscopic evaluation in postoperative CD patients and provides pragmatic information regarding interpretation of endoscopic findings at the different types of surgical anastomoses after ileocecal resection.

Surgery and Crohn’s disease: assessing postoperative Crohn’s disease recurrence

Ileocecal resection is the hallmark operation for CD, dating back to the original description of the disease in 1932, where 14 patients with terminal ileal strictures underwent resection after radiographic characterization. This historical perspective is relevant today, because a majority of CD patients require surgery, but radiographic studies have now been complemented with colonoscopy and direct mucosal assessment of the preoperative and postoperative mucosa. The importance of endoscopic assessment of postoperative CD patients stems directly from the fact that there are different patterns of CD recurrence and this heterogeneous natural history may be linked to personalized approaches tailored to maintain the surgically induced clinical remission. Endoscopy offers an opportunity to not only visualize the site of surgery but also allow for characterization of the early return of mucosal ulceration, not yet radiographically apparent, which carries important prognostic significance. Furthermore, mucosal pinch biopsies at the level of the anastomosis give additional information that can help personalize therapeutic intervention. Lastly, in certain situations, an anastomotic stricture may form and endoscopically guided pneumatic balloon dilatation with or without intralesional steroid injection can be attempted to re-establish luminal patency. The ability to endoscopically assess the surgical anastomosis and the neoterminal ileum in the postoperative time period for diagnostic, prognostic, and therapeutic purposes is essential for improving CD clinical outcomes.

Endoscopic assessment of the Crohn’s disease anastomosis: gauging postoperative recurrence and tailoring therapy

The ability to effectively gauge CD activity at the postoperative neoterminal ileum is dependent on a structured assessment where objective endoscopic features are linked to a predictable natural history over the ensuing years. The postoperative CD patient provides the best opportunity to standardize an endoscopic assessment score, because the neoterminal ileum is essentially free of disease after surgical reconstruction, and the return of CD lesions over a known time (eg, the date of surgery) offers an opportunity to characterize disease trajectories. The development of a postoperative neoterminal ileal score, which was associated with clinical CD recurrence, was achieved by Rutgeerts and colleagues in Leuven, Belgium, in the early 1990s. Using a cohort of 89 postoperative CD patients, these investigators developed an endoscopic scoring system to grade the severity of mucosal ulceration at the neoterminal ileum 1 year after resection and were able to associate patterns of ulceration with subsequent clinical recurrence over the next 6 years. The Rutgeerts endoscopic scoring system grades the severity of recurrent CD in the postoperative patient by focusing on the mucosa of the ileocolonic anastomosis and the neoterminal ileum, just proximal to the anastomosis. Scores range from an ileal endoscopic score of i0 to i4, the latter score indicative of more severe endoscopic recurrence (the majority of neoterminal ileal mucosa is ulcerated). The score i0 indicates an endoscopically normal neoterminal ileum, whereas the emergence of scattered aphthous ulcers (<5 ulcers) is classified as a Rutgeerts i1 score. More than 5 aphthous ulcers in the neoterminal ileum is defined as a Rutgeerts i2 score. Deeper, discrete stellate ulcers constitute a Rutgeerts i3 score (ulcers involve <50% of the lumen), and the most severe recurrence, Rutgeerts i4 score, demonstrates linear ulcers encompassing more than 50% of the lumen, representing the most significant recurrence. Table 1 defines the different endoscopic scores of the Rutgeerts score and Fig. 1 displays the corresponding endoscopic images of different recurrence scores at the neoterminal ileum.

Rutgeerts postoperative endoscopic ileal scores; classic endoscopic features of the i0, i1, i2, i3, and i4 scores are demonstrated.

Patients with an ileal Rutgeerts score of i0 or i1 are considered in endoscopic remission in the postoperative time period. The prognostic component of the score suggests that a majority of these individuals do not require medical therapy, because they have a low probability of developing clinical recurrence of their CD over the ensuing years. One of the most important insights that arose from the development of the Rutgeerts score was the understanding that a majority of postoperative CD patients remain asymptomatic for up to 3 years after their surgery/reanastomosis, which is irrespective of early endoscopic features seen at the anastomosis 1 year after surgery. Although demonstrating objective evidence of CD recurrence at the anastomosis, a majority of postoperative CD patients with more severe endoscopic recurrence (i4) 1 year after surgery experience clinical relapse (70% by 1 year after surgery). CD patients with i3 recurrence 1 year after surgery have a 1-year clinical recurrence rate of 30% and a 50% recurrence rate by year 4. This identification of silent endoscopic recurrence that portends a clinical relapse in the ensuing years highlighted the importance of assessing and documenting objective evidence of recurrence in the year after surgery. Patients with aggressive return of mucosal lesions seen on endoscopy essentially declared themselves appropriate candidates for postoperative treatment, with immunomodulator and/or biologic agents, prior to the return of significant damaging disease, which might otherwise be less responsive to therapy.

Although the Rutgeerts score was never validated for postoperative CD treatment trials, the score has been used to define endoscopic recurrence and has been used in several studies assessing the efficacy of preventing CD recurrence in the postoperative time period. In a majority of studies, clinical recurrence remained the primary endpoint whereas patterns of endoscopic recurrence were designated secondary endpoints. In a recent study by De Cruz et al., the authors developed and prospectively validated a new postoperative endoscopic index of severity (POCER Index) by assessing number (0, ≤2, >2), size (1-5mm vs ≥6mm), depth (superficial vs deep), and circumferential extent (<25% vs ≥25%) of anastomotic ulcers. Detection of deep ulcers and more extensive anastomotic ulceration (≥25%) at a 6 month post-operative time period were highly associated with significant endoscopic recurrence (Rutgeerts ileal score i≥2) at an 18 month post-operative time period. This simplified endoscopic staging may ultimately prove useful in stratifying post-operative CD patients to receive immunomodulator and/or biologic therapy following surgery.

Early attempts to delay postoperative recurrence of CD demonstrated marginal benefit of 5 aminosalicylic agents, antibiotics, and purine analog agents. More significant results were demonstrated with the use of postoperative biologic agents, which showed significant benefit regarding the prevention of CD endoscopic recurrence.

In 2015 and 2016, 2 multicenter clinical trials were published, which used the Rutgeerts score as a key component in a step-up approach for managing postoperative CD as well as assessing the efficacy of postoperative biologic therapy. In the POCER (Post-Operative Crohn’s Endoscopic Recurrence) trial, postoperative CD patients underwent endoscopic assessment and, based on the patterns of recurrence, were stratified to receive immunomodulators and/or biologic agents. In the PREVENT (Infliximab for Prevention of Recurrence of Post-Surgical Crohn’s Disease Following Ileocolonic Resection: a Randomized, Placebo-Controlled Study) trial, which randomized patients to receive infliximab versus placebo infusions in the postoperative time period, there was a significant decrease in patterns of endoscopic recurrence at 18 months. Unfortunately, the primary end point of the trial was a composite score composed of both clinical symptoms and endoscopic recurrence, which was not met in interim analysis. As a result, the trial was halted prematurely due to the failure to achieve a predesignated clinical recurrence prevention endpoint. The rates of endoscopic recurrence of CD were cut in half, however, in the patients who received active therapy.

Practical guidance: endoscopic evaluation guides management of postoperative Crohn’s disease

The growing consensus from published evidence suggests that endoscopic evaluation of the colonic and ileal mucosa helps guide CD medical therapy in the postoperative setting. Although there are no official guidelines, the authors recommend that postoperative CD patients undergo an ileocolonoscopy 6 to 12 months after their intestinal resection to evaluate the anastomosis and the neoterminal ileum just proximal to the anastomosis. The reproducible patterns of CD recurrence make this targeted assessment very high yield in terms of prognostication and stratification for further medical therapy, because the intestine just proximal to the anastomosis has the highest likelihood for CD recurrence.

Currently there are 2 strategies for approaching postoperative CD; the first is watchful waiting and only starting patients with high risk for recurrence on a prophylactic medication, whereas the other strategy (and the authors’ preference) is to start high-risk and moderate-risk patients on a prophylactic medication. At 6 to 12 months postoperatively, patients undergo a colonoscopy to evaluate for postoperative CD recurrence, and, depending on the presence of endoscopic lesions (Rutgeerts ileal score > i2), medical management is modified, either medication escalated or changed.

Given the emergence of data suggesting benefit of immunosuppressive and/or biologic therapy when used in the early postoperative time period, it is recommended that patients who undergo ileocecectomy with an anastomosis have an ileocolonoscopy as early as 6 to 12 months postoperatively. The purpose of this early and typically asymptomatic endoscopic assessment is to evaluate for early postoperative recurrence of CD to optimize medical therapy in a timely fashion, prior to the recurrence of significant inflammation and irreversible damage and tissue remodeling. This is particularly true for CD patients who choose to go on no form of postoperative medical therapy after resection and reanastomosis.

Postoperative surgical anatomy in Crohn’s disease: pragmatic approach to endoscopic assessment of the anastomotic configuration

As discussed previously, the most common CD surgery is an ileocecal resection with ileocolonic anastomosis. The type of reconstruction after ileocecal resection varies, however, with essentially 4 different configurations comprising the majority of anastomoses. At present, the American Society of Colon and Rectal Surgeons does not recommend one type of surgical anastomosis over another, because the best prospective multicenter trial data assessing end-to-end versus side-to-side anastomoses did not demonstrate superior or inferior outcomes, which included operative complications, leaks, and patterns of CD recurrence at 1 year. Thus, society recommendations have left the choice of anastomotic configuration to the discretion of the treating surgeon. More recent prospective, observational data generated by the Inflammatory Bowel Disease Center at the University of Pittsburgh Medical Center (UPMC) suggest, however, that not all anastomotic configurations are equal when considering long-term outcomes in postoperative CD patients. The authors have found that the type of anastomosis has a significant impact on the long-term quality of life of patients, irrespective of recurrence of CD inflammation, with end-to-end anastomoses functioning better than side-to-side anastomoses (antiperistaltic orientation). In addition, the different types of anastomoses need to be accurately interpreted when assessing postoperative CD patients endoscopically. The underappreciation of different anastomotic configurations is apparent when considering that one of the major endoscopic reporting programs, ProVation (Minneapolis, Minnesota), offers only 1 diagram ( Fig. 2 P ) for describing endoscopic findings in postoperative CD patients (although there are text dropdown menus to accurately describe anastomotic type and also a separate drop down menu to annotate the Rutgeerts ileal recurrence score). For gastroenterologists to take full advantage of endoscopic assessment of the surgery site, comprehensive understanding and command of the endoscopic appearance of the surgical anatomy after reconstruction are required. The 4 most common types of surgical reconstruction and endoscopic features are outlined and guidance provided on their clinical strengths and limitations from the perspective of the endoscopist.

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