Crohn disease is a chronic inflammatory condition, affecting the entire gastrointestinal tract, that follows a relapsing and remitting course. Approximately two-thirds of patients with Crohn disease undergo a resective surgery during their lifetime, often because of complications associated with the disease, including fistula, abscess, fibrostenotic stricture. Once patients undergo a surgical resection, they are at an increased risk for future reoperation, and 30% to 70% of patients with Crohn disease require reoperation within 10 years of their initial surgery. Although some risk factors have been associated with need for reoperation, the complexities of the timing and severity of disease recurrence are not well-understood.
Currently, the gold standard for postoperative Crohn disease evaluation is performing an ileocolonoscopy within 1 year of a resective surgery. During this evaluation, the severity of endoscopic recurrence in the neoterminal ileum can be determined (Rutgeerts score), providing prognostic information regarding the risk of future symptomatic recurrence, as well as the development of complications, and the need for reoperation. Recently, noninvasive strategies to assess for early disease recurrence have been described, including wireless capsule endoscopy (WCE), small intestinal contrast ultrasonography (SICUS), and magnetic resonance enterography (MRE). However, ileocolonoscopy remains the procedure of choice because of its well-described prognostic score.
Recent reviews have focused on stratifying patients based on their risk factors for postoperative recurrence, and considering prophylactic therapy for those patients who are at higher risk for disease progression. The timing of treatment initiation in the postoperative period remains controversial, although an ileocolonoscopy should be performed within12 months postoperatively regardless of a patient’s treatment regimen. Several classes of medications have been evaluated in the postoperative setting, with the strongest data supporting the use of nitroimidazole antibiotics, immunomodulators (azathioprine [AZA]/6-mercaptopurine [6-MP]), and antitumor necrosis factor (anti-TNF) medications.
This article discusses the evaluation of postoperative Crohn disease, focusing on endoscopic evaluation with ileocolonoscopy and WCE. Risk factors for recurrence are reviewed, as well as recommendations for risk stratification. Finally, an algorithm for the evaluation and treatment of postoperative Crohn disease is presented.
Definition and Patterns of Recurrence
Postoperative Crohn disease recurrence has been defined in several different manners, including endoscopic, histologic, symptomatic (clinical), radiographic, and surgical. Early studies demonstrated that reconstitution of the fecal stream is critical for the development of postoperative recurrence, and evidence of histopathologic Crohn disease has been described as soon as 7 days following resective surgery. The timing of recurrence follows a well-described pattern, with endoscopic recurrence always a precursor to symptomatic recurrence. Endoscopic recurrence rates are 73% to 95% at 1 year, and 83% to 100% at 3 years, with symptomatic recurrence rates being only 20% to 37% and 34% to 86% at these respective time points. This clinically silent disease has been best described in the postoperative Crohn disease setting, but elucidates the natural history of Crohn disease; most disease is asymptomatic until intestinal inflammation is severe, often corresponding with the development of complications requiring surgery. Endoscopic recurrence follows a predictable pattern, with the initial postoperative ulcers presenting in the neoterminal ileum, proximal to the ileocolonic anastomosis. The postoperative disease pattern tends to mimic that of the preoperative period, meaning that patients who undergo resective surgery for a stricturing or penetrating complication are likely to have those respective disease behaviors recur postoperatively.
Risk Factors for Recurrence
Multiple studies have attempted to describe patient and disease characteristics that are associated with a higher risk for disease recurrence. Data concerning many of these risk factors are conflicting, although several risk factors have consistently been shown to be associated with early and severe disease recurrence ( Box 1 ). Cigarette smoking, a penetrating disease phenotype, and a history of prior surgical resections are the strongest risk factors for postoperative disease recurrence. In addition, short disease duration prior to initial surgery may be a risk factor for postoperative recurrence. Several other risk factors have been studied, with conflicting results, including gender, indication for surgery, length of resected segment, presence of granulomas in resected segment, involvement of resected margin with active disease, genetic factors (NOD2/CARD15), serologic profile anti-saccharomyces cerevisiae antibodies, corticosteroid treatment at time of surgery, and a perioperative blood transfusion requirement. Although not yet described, it is the authors’ opinion that patients failing to respond to immunomodulators/biologics who progress to surgery are also at high risk for postoperative recurrence.
High Quality Evidence:
• Smoking
• Penetrating disease
• Prior Crohn disease resection
• Short duration of disease
Conflicting Evidence:
• Perioperative complications
• Young age at disease onset
• Family history of IBD
• Anatomical site of disease (ileal vs colonic vs ileocolonic)
• Disease extent (>100 cm)
• Disease activity at time of resection
• Type of anastomosis
Risk Factors for Recurrence
Multiple studies have attempted to describe patient and disease characteristics that are associated with a higher risk for disease recurrence. Data concerning many of these risk factors are conflicting, although several risk factors have consistently been shown to be associated with early and severe disease recurrence ( Box 1 ). Cigarette smoking, a penetrating disease phenotype, and a history of prior surgical resections are the strongest risk factors for postoperative disease recurrence. In addition, short disease duration prior to initial surgery may be a risk factor for postoperative recurrence. Several other risk factors have been studied, with conflicting results, including gender, indication for surgery, length of resected segment, presence of granulomas in resected segment, involvement of resected margin with active disease, genetic factors (NOD2/CARD15), serologic profile anti-saccharomyces cerevisiae antibodies, corticosteroid treatment at time of surgery, and a perioperative blood transfusion requirement. Although not yet described, it is the authors’ opinion that patients failing to respond to immunomodulators/biologics who progress to surgery are also at high risk for postoperative recurrence.
High Quality Evidence:
• Smoking
• Penetrating disease
• Prior Crohn disease resection
• Short duration of disease
Conflicting Evidence:
• Perioperative complications
• Young age at disease onset
• Family history of IBD
• Anatomical site of disease (ileal vs colonic vs ileocolonic)
• Disease extent (>100 cm)
• Disease activity at time of resection
• Type of anastomosis
Endoscopic Evaluation of Postoperative Crohn Disease
Ileocolonoscopy
Rutgeerts and colleagues initially described a scoring system for the endoscopic evaluation of postoperative Crohn disease in 1984. The Rutgeerts score, grading the severity of endoscopic lesions 1 year postoperatively, is currently the best predictor of postoperative Crohn disease course ( Table 1 and Fig. 1 ). Mild endoscopic recurrence includes patients with no evidence of aphthous ulcerations (i0), and patients with less than 5 aphthous ulcerations in the neoterminal ileum (i1). Patients with i2 disease had a postoperative clinical behavior between those with mild disease and those with more severe lesions, and had an endoscopic appearance of greater than 5 aphthous ulcerations, with normal intervening mucosa, or skip areas of larger lesions, or lesions confined to the ileocolonic anastomosis. Finally, patients with i3 or i4 endoscopic scores had a more severe appearance. Patients with diffuse aphthous ileitis with diffusely inflamed mucosa were categorized as i3, whereas the presence of diffuse inflammation with larger ulcers, nodules, and/or narrowing were categorized as i4.
| Endoscopic Score | Endoscopic Findings |
|---|---|
| i0 | No lesions |
| i1 | ≤5 aphthous lesions |
| i2 | >5 aphthous lesions with normal mucosa between the lesions, or skip areas of larger lesions or lesions confined to the ileocolonic anastomosis (ie, <1 cm in length) |
| i3 | Diffuse aphthous ileitis with diffusely inflamed mucosa |
| i4 | Diffuse inflammation with already larger ulcers, nodules, and/or narrowing |
In 1990, the same group reported on a cohort of 122 patients who had been prospectively followed after undergoing bowel resection for Crohn disease. The aims of this study were to describe the evolution of endoscopic lesions found during postoperative ileocolonoscopy and to determine if these lesions were left behind at surgery, or represented de novo lesions. At 1 year postoperatively, 73% of patients had evidence of endoscopic recurrence, whereas only 20% had symptoms suggestive of recurrence. Multivariate analysis, stratified for the preoperative disease activity score, found that the only factor significantly associated with symptomatic recurrence was the endoscopic index.
Clinical outcome was then analyzed based on endoscopy score, with i0 and i1 patients grouped together. The 39% of the cohort who were included in the mild endoscopic activity (i0/i1) group did very well, with 80% of these patients having no endoscopic lesions after 3 years of follow-up. There were also few cases of clinical recurrence in this group during follow-up. Conversely, patients with evidence of more significant endoscopic recurrence (i3–i4) tended to have a more severe disease course, developing early symptoms and progressing to complications. At 12 months postoperatively, 70% of patients with i4 disease had already experienced symptomatic recurrence, and all but one patient had experienced symptomatic recurrence by 3 years. Whereas 80% of patients with mild endoscopic lesions had unchanged lesions at 3 years, 92% of those with severe lesions at initial ileocolonoscopy had progression or very severe evolution at 3 years.
These investigators and others have been able to describe a biphasic pattern to postoperative recurrence, which can be explained by the findings of this study. Patients with severe disease (i3/i4) tend to have early symptomatic recurrence and experience complications, including penetrating disease, which require early reoperation. Another group of patients experiences slower disease progression, ultimately leading to fibrostenotic stricturing, and often requires reoperation 5 to 7 years later.
The Crohn disease activity index (CDAI) is often used in clinical trials in order to assess for disease activity and to monitor for disease recurrence. However, in the postoperative setting, the usefulness of the CDAI has been questioned, and the Rutgeerts score has proved to be a better predictor of disease evolution.
Regueiro and colleagues studied the correlation between CDAI and endoscopic recurrence as part of their postoperative infliximab study. Endoscopic recurrence was defined as a score of i2 to i4, clinical recurrence was CDAI greater than 200, and clinical remission was CDAI greater than 150. At 1-year postoperatively, 50% of the 24 patients were in endoscopic remission, with 50% showing evidence of endoscopic recurrence. There was no relationship found between mean CDAI score and endoscopy score at 1 year. In fact, mean CDAI scores at 1 year were identical (134) in both groups, and the agreement between CDAI scores and endoscopy was poor (Pearson R = 0.07). When a CDAI greater than 200 was used as a cutoff for clinical recurrence, sensitivity and specificity with endoscopy was 33% and 91%, respectively. Therefore, most endoscopic recurrences did not meet criteria for clinical recurrence using the CDAI score, which had a 67% false-negative rate. Interestingly, neither C-reactive protein nor erythrocyte sedimentation rate was associated with endoscopic recurrence in this study, although histologic scores were found to correlate with endoscopic recurrence.
This study demonstrates that the CDAI score is not an effective measure of postoperative disease recurrence, and, although CDAI is not routinely used clinically, these results support the observations that patients do not experience symptomatic recurrence until later in their postoperative course.
Wireless Capsule Endoscopy
Although ileocolonoscopy remains the recommend modality for the assessment of postoperative disease recurrence, several studies have begun to evaluate a possible role for WCE in this setting ( Fig. 2 ). The advantages of noninvasive tests to evaluate for postoperative recurrence include greater patient acceptance, lack of sedation, less bowel preparation, and a decreased risk (perforation, bleeding) than with colonoscopy. In addition, there may be technically difficult anatomy encountered during postoperative ileocolonoscopy, and the neoterminal ileum cannot always be accessed. Finally, WCE allows examination of a greater area of small bowel mucosa.
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