Endoscopic dilation is an efficacious and safe treatment of intestinal strictures in Crohn s disease

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1 Alimentary Pharmacology and Therapeutics Endoscopic dilation is an efficacious and safe treatment of intestinal strictures in Crohn s disease A. Gustavsson*,, A. Magnuson, B. Blomberg*, M. Andersson, J. Halfvarson*, & C. Tysk*, *Department of Medicine, Division of Gastroenterology, Örebro University Hospital, Örebro, Sweden. School of Health and Medical Sciences, Örebro University, Örebro, Sweden. Unit of Statistics and Epidemiology, Centre for Clinical Research, Örebro University Hospital, Örebro, Sweden. Department of Surgery, Örebro University Hospital, Örebro, Sweden. Correspondence to: Prof. C. Tysk, Department of Medicine, Division of Gastroenterology, Örebro University Hospital, Örebro, Sweden. curt.tysk@orebroll.se Publication data Submitted 13 January 2012 First decision 21 March 2012 Resubmitted 12 April 2012 Accepted 2 May 2012 EV Pub Online 22 May 2012 SUMMARY Background Bowel strictures are a major cause of morbidity, hospitalisation and surgery in Crohn s disease. Aim We report short- and long-term efficacy and safety of endoscopic balloon dilation of strictures due to Crohn s disease. Methods Retrospective study of patients who underwent endoscopic balloon dilation between 1987 and Results We performed 776 dilations, of which 621 (80%) were on anastomotic strictures, in 178 patients (94 women) with Crohn s disease. At first dilation, median (IQR) age of patients was 45 (37 56) years and disease duration 16 (8 22) years. Technical success rate was 689/776 (89%). A subset of 75 patients from the primary catchment area, with >5-year follow-up, underwent a total of 246 dilations. At 1-year follow-up, 60/75 (80%) patients had undergone no further intervention or one additional dilation only. At 3 and 5 years, corresponding figures were 43/75 (57%) and 39/75 (52%). Cumulative proportions of patients undergoing surgery at 1, 3 and 5 years were 13%, 28% and 36%. Complication rate per procedure for all 178 patients was 41/776 (5.3%), bowel perforation (n = 11, 1.4%), major bleeding requiring blood transfusion (n = 8, 1.0%), minor bleeding (n = 10, 1.3%) and abdominal pain or fever (n = 12, 1.5%). Ten patients underwent surgery due to complications (perforation n = 8, bleeding n = 2). There was no procedure-related mortality. Conclusions Endoscopic balloon dilation is an efficacious and safe alternative to surgical resection of intestinal strictures in Crohn s disease. At 5-year follow-up, 52% of patients required no further or one additional dilation only, whereas 36% had undergone surgical resection. Complication frequency was low. Aliment Pharmacol Ther 2012; 36: doi: /j x

2 A. Gustavsson et al. INTRODUCTION Bowel strictures are a major cause of morbidity, hospitalisation and surgery in Crohn s disease (CD). Strictures are caused by transmural inflammation leading to tissue remodelling, mesenchymal cell proliferation and fibrosis, but the underlying cellular and molecular mediators have not yet been elucidated. 1 3 Any segment of the gastrointestinal tract can be affected, but most commonly the terminal ileum, ileocolonic anastomosis or colon is involved. Traditionally, fibrotic strictures have been treated by surgical resection, as medical treatment is ineffective. The cumulative risk for surgery 10 years after diagnosis of CD is approximately 40 55%. 4 The recurrence risk after resection is high. New endoscopic lesions will be found in a large majority of patients as early as after 1 year, 5, 6 which may in due course cause recurrent clinical symptoms requiring a second surgical procedure in 20 44% of patients after 10 years. 4, 7 In the long-term perspective, multiple resections may be associated with a risk for short-bowel syndrome. Strictureplasty has therefore evolved as a surgical bowel-preserving alternative and has been shown to be as safe and efficient as bowel resection in treating fibrotic strictures in CD Endoscopic balloon dilation is a nonsurgical alternative in treatment of fibrotic strictures in CD. It was first described in and has generally been accepted as an effective and safe treatment for short anastomotic strictures, although the evidence is limited Most previous studies are retrospective uncontrolled, observational studies with small numbers of patients and short follow-up time. In general, the immediate technical success is high, but the clinical efficacy is variable. A review of 23 publications including between 5 and 59 patients reported a technical success rate of 90%, a rate of major complications like bowel perforation or severe bleeding of 3%, and a surgical recurrence rate of 27.6% after a median follow-up of 21 months. 16 However, the evidence for long-term efficacy is sparse. The aim of this study is to report a single referral centre experience of short-term and long-term efficacy and safety of endoscopic balloon dilation in treatment of intestinal strictures in CD. MATERIAL AND METHODS Patients The study comprised 178 patients, including both patients from the primary catchment area of the hospital (n = 125) and referred patients (n = 53). Patients were retrospectively identified by running the register of surgical procedures against the diagnosis register at the Departments of Medicine and Surgery at Örebro University Hospital during the period 1987, when the first dilation was performed, to Search items were endoscopic balloon dilation (4488 and 4886 according to the Classification of Surgical Procedures version 6 and JDA 55, JDH 32, JFA 38, JFA 58 and JGA 58 according to Classification of Surgical Procedures version 7) and Crohn s disease (555A, 555B, 555C and 555X according to International Classification of Diseases version 9 and K.50.0, K.50.1, K.50.8 and K.50.9 according to International Classification of Diseases version 10). Demographic data, clinical characteristics and endoscopic and surgical procedures were searched for in the medical records at the Departments of Medicine and Surgery. Diagnosis of CD was based on Lennard-Jones criteria. 17 Disease location and behaviour were classified according to Montreal classification. 18 All patients were included in the calculations on technical success and complications. To reduce the risk of referral bias, analyses of clinical efficacy were restricted to patients from our primary catchment area. These patients had a regular follow-up at our outpatient colitis clinic. Patients from the primary catchment area were separated into two groups. One group consisted of patients who, after the index dilation, underwent further endoscopic dilations due to recurrent symptomatic bowel strictures only (n = 83). The other group consisted of patients who anytime had further stricture dilations performed without associated clinical symptoms of bowel obstruction (n = 42). Stricture and endoscopic dilation A bowel stricture was considered to exist when passage of a standard colonoscope was not possible. A symptomatic stricture refers to a stricture associated with clinical symptoms of bowel obstruction such as postprandial abdominal pain, vomiting and nausea. Anastomotic strictures have been considered most appropriate for endoscopic dilation, and the authors have generally been restrictive in treating de novo strictures, especially colonic strictures. Concomitant fistula or abscesses have been exclusion criteria. In most cases, the stricture was documented by a small bowel follow-through or enteroclysis, or in recent years a magnetic resonance tomography of the small bowel. In patients with symptoms of bowel obstruction and a previous history of stricturing CD, colonoscopy was performed without prior radiological investigation. In the early study period, repeated 152 Aliment Pharmacol Ther 2012; 36:

3 Endoscopic dilation in Crohn s disease dilations 1 4 times/year were performed in some patients without any clinical symptoms of bowel obstruction, as this practice might reduce the risk of surgery. During the latter study period, dilation was performed principally only in patients with strictures causing recurrent clinical symptoms of bowel obstruction. Analyses of long-term outcome will be restricted to the latter group of patients. Endoscopic dilation was generally done as an outpatient procedure using conscious sedation with midazolam and/or alfentanil or diazepam and/or pethidine. A few procedures were done under general anaesthesia. Several different physicians with variable endoscopic skill performed the dilation procedure. Standard colonoscope (Olympus, Hamburg, Germany; Pentax Europe GmbH, Hamburg, Germany) and through-the-scope dilation balloons with a maximal diameter of 12 to 25 mm (Boston Scientific, Cork, Ireland; Cook Medical Europe Ltd, Limerick, Ireland) were used. The balloon was positioned under visual control in the stricture and inflated with water stepwise with a gradually increasing diameter. Inflation time varied between 1 and 3 min. The procedure was repeated until the colonoscope could pass through the stricture. Fluoroscopy was not used. After the procedure, patients were observed for at least 2 h in a recovery room. Outcome Outcome measures were technical and clinical efficacy and complication rates. Technical success was defined as being able to pass the endoscope through the stricture after the procedure. Short-term clinical success was defined as relief of clinical symptoms of bowel obstruction during the following month after the endoscopic procedure. Long-term efficacy was assessed on proportion of patients undergoing no further procedure, one dilation, two dilations, three dilations, >3 dilations or surgery for each year during the first 5 years after index dilation. Evaluation of clinical efficacy was made in patients from the primary catchment area only, whereas technical success was assessed in all patients, including referred patients. Surgery refers to any operation leading to intestinal resection or strictureplasty. Complications such as bowel perforation, bleeding, abdominal pain, fever or death following the procedure and requiring hospital stay or prolonged hospital stay were assessed in all patients. Major bleeding was defined as any bleeding requiring blood transfusion. Statistics Data are presented as median and interquartile range (IQR). Differences between groups were tested with Chi-squared test, or when appropriate Fisher s exact test and a P-value <0.05 was statistically significant. Time to first surgical procedure after index dilation was illustrated with Kaplan Meier plot and differences between groups were tested with log-rank test. Ethics This study was approved by the Regional Ethics Review Board in Uppsala. RESULTS Demographics of all patients During , 178 patients (94 women) underwent endoscopic balloon dilation due to bowel strictures causing obstructive symptoms. The median (IQR) age at diagnosis of CD was 29 (20 39) and at first dilation 45 (37 56) years. Demographics and clinical characteristics of the patients are shown in Table 1. Demographics of patients from the primary catchment area In total, 125 (70%) patients resided in the primary catchment area of the hospital. The median age at diagnosis of CD was 31 (22 42) years and at first dilation 46 (38 57) years. Demographics and clinical characteristics of the patients are shown in Table 1. Endoscopic dilation in all patients In 178 patients, a total of 776 dilations were made; 155 (20%) were performed on de novo strictures and 621 (80%) on anastomotic strictures. Six hundred twenty-five (81%) procedures were performed in patients with symptomatic strictures, and 151 (19%) dilations in patients with strictures causing no clinical symptoms. Details of strictures and dilation procedures are shown in Table 2. Data on length of stricture were not accessible retrospectively. In a few dilations, local corticosteroid injection (n = 9) or incision with a papillotome (n = 7) was used as a complement. The dilation procedure was done with sedation with benzodiazepines and/or opioid analgesics in 726 (94%) procedures, general anaesthesia in 11 (1%) and in 37 (5%) procedures no sedation was given (data missing in two patients). Endoscopic dilation in patients from primary catchment area In 125 patients, a total of 594 dilations were made; 107 (18%) were performed on de novo strictures and 487 (82%) on anastomotic strictures. Four hundred Aliment Pharmacol Ther 2012; 36:

4 A. Gustavsson et al. Table 1 Demographic and clinical characteristics of all patients and patients from primary catchment area All patients N = 178 Patients from primary catchment area N = 125 Gender: male/female 84/94 66/59 Age at diagnosis, median (IQR) 29 (20 39) years 31 (22 42) years Age at first dilation, median (IQR) 45 (37 56) years 46 (38 57) years Disease duration at first dilation, median (IQR) 16 (8 22) years 16 (8 22) years Disease location at diagnosis Ileal (L1) 84 (55%) 66 (54%) Colonic (L2) 20 (13%) 17 (14%) Ileocolonic (L3) 49 (32%) 40 (33%) Data missing 25 2 Behaviour at diagnosis Nonstricturing, nonpenetrating (B1) 77 (52%) 60 (50%) Stricturing (B2) 60 (41%) 53 (44%) Fistulating (B3) 10 (7%) 8 (7%) Data missing 31 4 Previous surgery 146 (82%) 105 (84%) Follow-up time, median (IQR) * 12 (7 20) years* IQR, interquartile range. * Available only in patients from the primary catchment area. Table 2 Data on stricture characteristics and dilation procedures All patients N = 178 Patients from primary catchment area N = 125 Number of dilations De novo strictures 155 (20%) 107 (18%) Anastomotic strictures 621 (80%) 487 (82%) Location of stricture Upper GI 14 (2%) 9 (2%) Ileum 105 (14%) 74 (12%) Ileo-ileal anastomosis 18 (2%) 7 (1%) Ileo-colonic anastomosis 601 (77%) 479 (81%) Colon 21 (3%) 14 (2%) Ileo-rectal anastomosis 2 (0.1%) 2 (0.3%) Rectum 15 (2%) 9 (2%) Stricture width 5 mm 63 (11%) 50 (12%) >5 mm 489 (89%) 365 (88%) Data missing Diameter of dilation balloon mm 19 (3%) 17 (3%) 18 mm 274 (39%) 200 (37%) 20 mm 196 (28%) 158 (29%) 25 mm 216 (31%) 167 (31%) Data missing seventy-nine (81%) of procedures were performed in patients with symptomatic strictures and 115 (19%) dilations in patients with strictures causing no obstructive symptoms. Details of strictures and dilation procedures are shown in Table 2. Outcome of endoscopic dilation in all patients Technical success was achieved in 689/776 dilations (89%). Complication rate per procedure was 41/776 (5.3%), which includes bowel perforation (n = 11, 1.4%), major bleeding (n = 8, 1.0%), minor bleeding (n = 10, 1.3%) and abdominal pain or fever (n = 12, 1.5%) (Table 3). Ten patients underwent surgery due to complications (perforation n = 8, bleeding n = 2). Significantly more complications (20/216, 9.3%) occurred with use of the largest balloon (diameter of 25 mm) compared with use of smaller balloons (diameter of 20 mm) (17/489, 3.5%) (P < 0.01). In four complications, the size of the balloon was not known. No difference was found between the two groups with respect to complications requiring surgery [4/216 (1.9%) vs. 4/489 (0.8%) (P = 0.23)]. In two complications requiring surgery, the size of the balloon was not known. Complications did not differ between patients dilated due to de novo (5/155, 3.2%) or anastomotic strictures (36/621, 5.8%) (P = 0.20). There was no procedure-related mortality. Outcome of endoscopic dilation in patients from primary catchment area Technical success, analysed in all 125 patients, was achieved in 533/594 dilations (90%) and clinical success in 370 (77%) of 479 dilations performed on strictures causing clinical obstructive symptoms. Of 125 patients, 83 patients underwent repeated dilations due to recurrent symptomatic strictures only. A 154 Aliment Pharmacol Ther 2012; 36:

5 Endoscopic dilation in Crohn s disease Table 3 Complications requiring hospitalisation in 178 patients with Crohn s disease undergoing 776 endoscopic dilations Bowel perforation Major bleeding Minor bleeding Abdominal pain/fever Total Requiring surgery Not requiring surgery Total 11 (1.4%) 8 (1.0%) 10 (1.3%) 12 (1.5%) 41 (5.3%) subset of 75 patients, with a follow-up of 5 years, underwent 246 dilations. The cumulative proportion of patients undergoing no further invention, repeated dilations, or surgery each year during 5-year follow-up after index dilation is shown in Figure 1. No further intervention or one additional dilation only was needed in 60/75 (80%) patients during the first year after the index dilation, and at 3 and 5 years corresponding figures were 43/75 (57%) and 39/75 (52%) (Figure 1). Cumulative proportions of patients undergoing surgery at 1, 3 and 5 years were 13%, 28% and 36%. Time to surgery is shown in Figure 2. Probability of surgery-free survival did not differ between dilations of de novo strictures compared with anastomotic strictures (P = 0,86) (Figure 2). There was no bowel malignancy diagnosed in any patient during follow-up. Among the 83 patients undergoing dilations due to symptomatic stricture only, the indication for surgery was technical failure at the dilation procedure (n = 7), patient s request or doctor s advice due to need of frequent dilations (n = 11), proximal stricture not identified at time of dilation (n = 10), active inflammation (n = 5), complication related to dilation procedure (n = 2) and miscellaneous (n = 8). Of 125 patients from the primary catchment area, 42 patients had during follow-up repeated dilations of bowel stricture that was clinically asymptomatic. These patients underwent a total of 342 procedures, of which 113 (33%) were performed due to an asymptomatic stricture. This group is very heterogeneous, and analyses of clinical outcome will thus not be possible, except for time to subsequent surgical procedure. During follow-up, 22/42 (52%) patients were operated after 6 (2 10) years. DISCUSSION This is one of the largest studies evaluating endoscopic balloon dilation of fibrostenotic strictures in Crohn s disease. The data, strengthened by the long follow-up period of a median 12 years and the large number of patients and procedures, emphasise that endoscopic dilation is an effective and safe method of treating anastomotic strictures, which constituted the majority of strictures. At index dilation, all patients suffered from obstructive bowel symptoms that likely would have required surgery if endoscopic dilation had not been accessible. During 5-year follow-up, 52% of the patients required no further intervention or just one additional dilation, and only 36% of patients underwent another % Year 1 Year 2 Year 3 Year 4 Year 5 Surgery >3 Dilations 3 Dilations 2 Dilations 1 Dilation No further intervention Figure 1 Cumulative proportions of patients undergoing no further invention, repeated dilations or surgery during 5- year follow-up following index dilation. This analysis is restricted to 75 patients having repeated dilations only of strictures causing symptoms of bowel obstruction, and with a follow-up of 5 years or more. Aliment Pharmacol Ther 2012; 36:

6 A. Gustavsson et al. Probability not undergoing surgery Anastomosis De novo Years At risk anastomotic stricture de novo stricture 1 1 Figure 2 Kaplan Meier plot showing probability of surgery-free survival in relation to time after index dilation in patients with anastomotic or de novo strictures (P = 0.86). This analysis is restricted to 83 patients having repeated dilations only of strictures causing symptoms of bowel obstruction. surgical resection. Technical success was achieved in 89% of all dilations, which is similar or slightly inferior compared with other studies. 13, 19 The immediate clinical success rate, defined as relief of clinical symptoms during the following month after the procedure, was 77% in patients from the primary catchment area of the hospital. Of greater importance is the long-term efficacy. This analysis was based on a subset of 75 patients from the primary catchment area to reduce selection bias of referral cases, and excluding cases having repeated dilations owing to asymptomatic recurrence of strictures, as the latter would not reflect the true long-term efficacy of the procedure. During the first year, 80% of the patients required no further intervention or one additional dilation only, and at 3 and 5 years corresponding figures were 57% and 52% (Figure 1). At 5-year follow-up, 4/75 (5%) patients required 3 dilations, which illustrates that the patients can be well managed in the long-term perspective, as well, with repeated endoscopic dilations. The length of symptom-free interval, the technical feasibility and the patient s preference will aid in the clinical choice between surgery and repeated dilation. The recurrence of stricture does not reflect a failure of the method but rather the natural history of stricturing CD. 20 In their large study of 237 dilations performed in 138 patients, Thienpont et al. reported the need of repeated dilation in 46% or surgery in 24% of patients during a follow-up of 5.8 years. 19 Similarly, in a systematic review of 13 studies enrolling 347 cases, 58% of patients avoided surgery during a mean follow-up of 33 months (range: months) and 22% required two dilation procedures, while 19% required more than two dilations, ranging from 3 to Surgery was ultimately required in 42% of patients after a mean period of 15 (range 1 70) months. Our results are quite consistent with those data but have the advantage of presenting cumulative proportion of patients undergoing no further invention, repeated dilations or surgery for each year during 5 years following index dilation (Figure 1). This gives a more detailed view of long-term outcome and underscores the value of endoscopic dilation in the treatment of strictures in CD. In our study, complication rates per procedure were similar to other studies, 16, 19 with a frequency of 5.3% for any complication requiring hospital stay and of 1.3% for a complication requiring surgery. Considering that a symptomatic stricture is an indication of surgery, this complication risk is acceptable. We found that the largest balloon (25 mm) was associated with significantly greater risk of any complication compared to smaller balloons. This has previously been observed but not confirmed. 21 In previous studies, the procedure was performed under general anaesthesia 19, 22 or conscious sedation In this study, only 11/776 (1.4%) required general anaesthesia and a large majority of procedures were done during conscious sedation using benzodiazepines and/or opioids. A minority of dilation procedures (37/776, 4.8%) was performed without any sedative at all. Theoretically, conscious sedation or no sedation has the advantage of allowing the patient s discomfort to be monitored as an indicator of impending perforation during the procedure. In this study, 1/11 (9%) patient under general anaesthesia suffered from a complication, but the figures are too small to assess whether general anaesthesia carries a higher risk than conscious sedation. 156 Aliment Pharmacol Ther 2012; 36:

7 Endoscopic dilation in Crohn s disease The limitation of this study, consistent with previous reports, is the retrospective, observational study design without a control group. The study period is very long with a median follow-up time of 12 years. This is strength of the study, but it also makes the data more heterogeneous. The first dilation in our hospital was done in In the early period, repeated dilations were performed in patients with recurrent strictures but without clinical symptoms of bowel obstructions out of a belief that this might reduce the risk of surgery. Today, only patients with obstructive symptoms are referred for dilation. During the years, the indication for referral to surgery may have changed, albeit treatment in general was discussed in a medico-surgical team. Comparing outcome of two time periods, vs , showed no significant differences with respect to repeated dilation or surgery within the first year (data not shown). This supports that changes in the medical or surgical treatment have not significantly influenced our data. At index dilation, only 20% of patients were treated with thiopurines, and biologics have not been used at all in this cohort. Another potential limitation is that several different physicians with variable endoscopic skill performed the procedures. This, however, reflects a day-to-day clinical situation, which makes the results even more relevant. Factors influencing outcome after endoscopic balloon dilation in fibrostenotic Crohn s disease are largely unknown. Technically successful dilation, 28, 29 a stricture length <4 cm 13 and absence of ulcer in the stricture 30 were found to be good prognostic factors. Data on influence of smoking after dilation are sparse and inconsistent. An increased risk for surgery 22 or recurrent dilation 30 was reported in smokers, whereas others found no significant association. 24, 31 Thienpont et al. reported that neither disease activity, assessed by CRP levels or endoscopic disease activity score, nor medical treatment after index dilation influenced subsequent disease course. 19 We are currently analysing these factors in our material. Fibrotic complications are one of the less understood manifestations of CD, and there is a need for further research to improve therapy and reduce hospitalisation and surgery. Intralesional steroid injections have been attempted to prolong the results of endoscopic dilation with various results In a small series of three patients, dilation of colonic strictures was achieved by intralesional injection of infliximab. 36 Metallic stent insertion has been tried in a few patients but was limited by stent migration. 37 Whether a biodegradable stent can be an alternative remains to be studied. 38 Whether drugs like azatioprine or anti-tnf therapy can change the natural history of CD in general and the risk of recurrent fibrostenotic stricture in particular is not yet known. In contrast to other reports, 25, 26 this study may suggest that dilation of de novo strictures is as efficient and safe as dilation of anastomotic strictures (Figure 2). However, we do not put too much emphasis on this observation, as the number of such dilations is small compared with the number of anastomotic stricture dilations. Furthermore, we had restricted indication for dilation of de novo strictures, and there is obviously potential selection bias in this group of patients. In conclusion, this study demonstrates that endoscopic balloon dilation of intestinal strictures in CD is an effective and safe alternative to surgical resection. At 5-year follow-up, 52% of the patients had undergone no further intervention or one additional dilation only, and 36% had undergone surgical resection. Complication rate per procedure was low. ACKNOWLEDGEMENTS Declaration of personal interests: Anders Gustavsson has served as a speaker for MSD. Jonas Halfvarson has served as a speaker for MSD, Abbott and Renapharma Vifor. Curt Tysk has served as a speaker for Tillotts Pharma, Falk Pharma, Ferring, MSD and AstraZeneca. Declaration of funding interests: This study was funded in part by The Foundation for Clinical Research in Inflammatory Bowel Disease, United States and Uppsala-Örebro Regional Research Council, Sweden. 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