- Research
- Open access
- Published:
Evaluation of symptomatic small bowel stricture in Crohn’s disease by double-balloon endoscopy
BMC Gastroenterology volume 23, Article number: 247 (2023)
Abstract
Purpose
To assess the efficacy of double-balloon endoscopy (DBE) for the detection of small-bowel strictures in Crohn’s disease (CD).
Methods
This tertiary-referral hospital cohort study was conducted between January 2018 and May 2022. CD patients with symptoms of small-bowel stricture were enrolled sequentially. All of the patients were subjected to both computed tomography enterography (CTE) and DBE, and their symptoms of stricture were assessed using the Crohn’s Disease Obstructive Score (CDOS). The diagnostic yield of DBE was compared to that of CTE, and the relationship between the DBE findings and CDOS was investigated. The factors influencing the DBE diagnosis were examined using Cox regression analysis.
Results
This study included 165 CD patients. The CDOS scores were higher in 95 patients and lower in 70 patients. DBE detected 92.7% (153/165) and CTE detected 85.5% (141/165) of the strictures. The DBE diagnostic yields were 94.7% (90/95) in the high CDOS patients and 91.4% (64/70) in the low CDOS patients (P = 0.13). Patients with a history of abdominal surgery and abscess had a lower diagnosis rate in the multivariate analysis.
Conclusion
DBE has been demonstrated to be an efficient diagnostic method for detecting small bowel strictures in CD patients. Additionally, there was no difference in the diagnostic yields between patients with low and high obstructive scores.
Introduction
Crohn’s disease (CD) is a chronic inflammatory gastrointestinal disease that can lead to a variety of complications. Intestinal strictures are common CD complications, occurring in 15–30% of patients within the first 10 years after diagnosis [1, 2]. Strictures are frequently associated with obstructive symptoms, necessitating endoscopic and surgical intervention [3, 4]. Therefore, it is critical to accurately diagnose and evaluate CD stenosis.
Approximately 70–80% of CD lesions involve the small intestine, with 30% of the lesions being isolated small-bowel lesions [5,6,7]. Small-bowel CD has a more complicated pathology and is more likely to develop stricture complications than colonic CD [8,9,10].
Because of the unique anatomy and technical limitations, diagnosing and evaluating isolated small-bowel CD is difficult for gastroenterologists. Transabdominal ultrasonography (TUS), computed tomography enterography (CTE), magnetic resonance enterography (MRE), small-bowel capsule endoscopy (CE), and double-balloon enteroscopy (DBE) are some of the new endoscopic and radiologic techniques for evaluating small intestinal stenosis that have been developed in recent years (DBE).
TUS is a useful tool for the diagnosis and monitoring of small-bowel strictures [11]. However, accurate and dependable results in US depend on having seasoned operators. Numerous studies have reported on the detection efficiency and ability of MRE predict surgical outcomes [12, 13]. This method, however, is time-consuming and costly. Furthermore, the interobserver consistency of MRE has been variable [14]. CTE is extremely effective at detecting small-bowel CD, with a sensitivity of 83% and a specificity of 88% [15]. Additionally, the rapid collection and image reconstruction of CTE allows for visualization of the entire small bowel and extraintestinal lesions [16]. Although CE is a very useful noninvasive tool for evaluating intestinal mucosal lesions in CD patients with small-bowel involvement, capsule retention has been reported in up to 5–13% of patients with known Crohn’s disease [17,18,19]. The risk of capsule retention is much higher in patients with small-bowel obstruction [20]. Furthermore, tissue diagnosis and endoscopic treatment cannot be performed when necessary [21].
DBE has been developed in recent decades for treating small-bowel diseases [22, 23]. The benefits of this deep enteroscopy technique include more direct visualization of the small intestine, the ability to obtain tissue biopsies for histopathology, and the ability to treat strictures [24,25,26]. Hence, DBE has become a widely accepted modality for assessing small-bowel CD [27]. Previous studies assessed the efficacy of DBE for the diagnosis and treatment of CD, and the majority of these studies involved patients with isolated CD of the small bowel [28,29,30,31].
The relationship between CD small-bowel strictures detected by DBE and the severity of stenosis symptoms, however, remains unknown. In addition, the factors influencing the diagnosis of DBE in patients with small bowel CD are still unknown. Hence, we conducted a prospective cohort study to evaluate the diagnostic yield of DBE in small-bowel CD patients with a symptomatic stricture.
Patients and methods
Patients and data collection
From January 2018 to May 2022, 165 CD patients with symptomatic small bowel strictures were enrolled at Anhui Medical University’s First Affiliated Hospital. This facility is a tertiary care facility for inflammatory bowel disease (IBD). All of the included patients met the following inclusion criteria: (1) a defined diagnosis of CD; (2) small bowel stricture symptoms; and (3) isolated small bowel strictures. Patients with an intra-abdominal abscess, suspected perforation, acute strangulated intestinal obstruction, contrast media allergies, or contraindications to DBE or CTE were excluded. All of these patients underwent CTE and DBE and were preoperatively followed up (Fig. 1). The time between CTE and DBE was reduced to less than one month. For the DBE procedures, all patients provided informed consent.
The prospectively obtained demographic and clinical data included sex, age, time from CD diagnosis to DBE, location of CD, previous surgery, laboratory values (complete blood cell count, albumin, C-reactive protein), and CD activity index [32].
The severity of stenosis symptoms
The Crohn’s Disease Obstructive Score (CDOS) was used to assess and quantify obstructive symptoms. The score was developed based on four core items (obstructive pain feature, signs of nausea, vomiting, dietary restriction, and hospitalization) and was tested in a recent clinical study [33]. In the CDOS, the severity of stenosis symptoms is graded from 1 to 6. The patients were divided into low- (1–3) and high-score (4–6) groups to compare the relationship between the DBE findings and obstructive severity.
DBE procedure and evaluation
All patients who underwent DBE procedures were sedated with a combination of intravenous and inhalation anesthesia. DBE was performed with an EN-580T enteroscope (FUJIFILM, Tokyo, Japan) and an overture, which was performed by three IBD endoscopists with at least 200 cases of experience. The insertion route was chosen according to the estimated location of the suspected lesion, mainly based on the results of CE or radiological findings (i.e., enteroclysis, CTE or MRE ). If the location of the small-bowel lesion is unknown or uncertain, clinical presentation of small bowel stricture was the basis for starting DBE from antegrade or retrograde approach. Oral administration of 2000 ml polyethylene glycol-electrolyte lavage solution (Beaufour Ipsen Industrie, Dreux, France) 4 h before the retrograde DBE examination was used for bowel preparation. Antegrade DBE was performed after an 8-hour fast and before processing.
The depth of DBE insertion was calculated using a method described in the previous literature [34]. CD-associated DBE stricture was defined as failure to pass the endoscope or an internal diameter of the small-bowel lumen of less than 10 mm [35]. During the DBE examination, the small-bowel stricture site was described as either the jejunum, terminal ileum, or proximal ileum [36]. The jejunum was defined as the section of the small bowel from the proximal part of the small bowel to the proximal part of the ileum. The terminal ileum was defined as a 10 cm section from the ileocecal valve. The proximal part of the ileum was defined as the section of the bowel between the proximal end of the terminal part and the terminal ileum.
CT enterography procedure and evaluation
Four hours before CTE examinations, all patients underwent intestinal preparation with 2000 ml polyethylene glycol-electrolyte lavage solution (Beaufour Ipsen Industrie, Dreux, France). Before scanning, 1500 ml of mannitol solution was taken orally, eventually reaching the small bowel for evaluation. A 128-slice MDCT scanner was used to perform CTE (GE Medical System, Chicago, IL, USA). The scan parameters were as follows: 5 mm layer thickness and spacing; 1.375:1 pitch; kV 120; and mAs 300. After injecting 100 ml of contrast agent (320 mgI/mL) into the elbow vein, the entire abdomen was scanned with delays of 45 and 90 s. An experienced gastrointestinal radiologist who was blinded to the clinical and endoscopic information analyzed the CTE images.
On CTE imaging, intestinal strictures were defined as follows: a localized thickened bowel wall and constriction of the intestinal lumen, enhanced bowel wall thickness ≥ 25%, reduction in luminal diameter ≥ 50%, and dilation of the small intestine proximal to the stricture ≥ 3 cm [37].
Statistics
Means ± SDs or medians and range are used to describe quantitative variables. The DBE and CTE diagnostic yields were expressed as percentages and compared using the chi-square test. The factors influencing the DBE diagnosis were examined using Cox regression analysis. Variables with P < 0.05 in the univariate analysis were tested further in a multivariate analysis. SPSS 21.0 was used for all statistical analyses (IBM Corporation, Armonk, NY, USA). P < 0.05 was regarded as statistically significant.
Results
Patient characteristics and severity of stricture symptoms at baseline
A total of 174 patients with symptomatic small intestinal strictures were enrolled in the study from January 2018 to May 2022. Nine patients were excluded due to intra-abdominal abscess (n = 5), acute severe intestinal obstruction (n = 2), or contraindications to DBE or CTE (n = 2). Hence, this study included 165 CD patients with small-bowel strictures (Fig. 1). Table 1 shows the baseline patient characteristics. According to the Montreal classification [38], all patients had a stricture phenotype. Previous small intestinal surgery was linked with CD in 41 (24.8%) patients. Forty-two (25.5%) of the patients had a previous intra-abdominal abscess or an intestinal fistula but not at the time of enrollment. The patients were divided into two groups based on the severity of their stricture symptoms. The low-score group was comprised of 70 (42.4%) patients with CDOS = 1–3 (16 patients, CDOS = 1; 18 patients, CDOS = 2; 36 patients, CDOS = 3), while the high-score group was comprised of 95 (57.5%) patients with CDOS = 4–6 (45 patients, CDOS = 4; 36 patients, CDOS = 5; 14 patients, CDOS = 6).
Results of DBE and CTE
In our study, 165 CD patients with symptomatic small intestinal strictures underwent 179 DBEs. The antegrade route was used for 14 procedures, while the retrograde route was used for 137 procedures. DBE was performed via both routes on 14 patients. In the DBE procedures, no patient experienced adverse events (such as anesthesia accident, gastrointestinal perforation or hemorrhage, or pancreatitis).
In the antegrade DBE examinations, the mean length of insertion was 237.14 ± 88.61 cm, and in the retrograde procedure, it was 99.83 ± 60.13 cm. DBE detected 168 strictures. In 136 patients, there was a single stricture. DBE detected small-bowel strictures in the jejunum (23, 13.7%), proximal ileum (131, 78.0%), and terminal ileum (14, 8.3%).
The overall diagnostic yield of DBE in CD patients with small-bowel strictures was 92.7% (153/165 patients), while with CTE, it was 85.5% (141/165 patients). DBE and CTE both detected strictures in 137 patients. Sixteen patients had DBE-positive strictures but negative CTE results. Of these, 15 had disease restricted to the ileum, and 1 had disease in the jejunum. Strictures were not accessible at DBE in 4 cases, which resulted from adhesions because of previous intra-abdominal abscess/intestinal fistula and history of CD-associated abdominal surgery, but were all detected by CTE.
We then associated the DBE or CTE findings with the severity of stricture symptoms. Based on the CDOS, the patients were divided into the low-score and high-score groups. The DBE diagnostic yields were 91.4% and 94.7% in the low-score and high-score groups, respectively (P = 0.13). Intriguingly, patients in the high-score group had a significantly higher CTE diagnostic yield than those in the low-score group (90.1% vs. 75.9%, P = 0.01).
Over the course of DBEs, 10 strictures in 6 patients were dilated. Obstructive symptoms were relieved after balloon dilatation in all patients. Within the study period, 5 of 6 patients remained surgery-free. In terms of surgery, stricturoplasty and bowel resection were performed in 3 and 5 patients, respectively.
Factors associated with successful detection of DBE
Univariate analysis was used to examine the factors associated with successful detection using DBE (gender, age of diagnosis, disease duration, history of CD-associated abdominal surgery, previous intra-abdominal abscess/intestinal fistula, levels of CRP, CDAI, location of disease, perianal disease, severity of stricture symptoms). Variables with P < 0.05 in the univariate analysis were tested further in a multivariate analysis. In the multivariate analysis, previous intra-abdominal abscess/intestinal fistula (hazard ratio = 2.021, 95% confidence interval (CI): 1.075–3.826, P = 0.021) and history of CD-associated abdominal surgery (hazard ratio = 2.852, 95% CI: 1.146–3.467, P = 0.017) were considered independent prognostic factors (Table 2).
Discussion
In this study, we evaluated the efficacy and safety of DBE for detecting small-bowel strictures in CD patients. Our study’s main findings were as follows: (1) DBE was an effective method for diagnosing strictures in CD patients with obstructive symptoms. (2) The severity of stricture symptoms did not affect the diagnostic yield of DBE. (3) A history of abdominal surgery and abscess was linked to the failure to detect DBE.
Up to 67% of CD cases involve the small bowel [39], with 10–30% of cases involving solitary lesions in the small bowel [40]. Small-bowel strictures in CD patients can be difficult to diagnose, particularly in patients with extensive small-bowel involvement. The DBE technique has made examination of the entire small-bowel feasible [41], let alone the investigation of the deep small bowel [22].
DBE is an efficacious tool for evaluating small-bowel strictures linked with CD, according to our findings. The diagnostic yield of DBE procedures performed by experienced IBD endoscopists was 92.7%. Several studies found that the diagnostic yield of DBE in CD patients ranged from 22 to 70% [26, 42,43,44]. However, in a study comparing the diagnostic yields of DBE and fluoroscopic enterolysis, Naoki Ohmiya et al. found that DBE had a diagnostic yield of up to 95% for small-bowel obstruction [45]. A comparison study compared MR and balloon enteroscopy for small-bowel strictures in CD [13]. All strictures in 57 patients that were detected by balloon enteroscopy were MR-positive. Furthermore, 37 patients had endoscopic strictures that could not be detected using MR imaging. The following are some possible explanations for our study’s high diagnostic yield: (1) All DBE procedures were performed by IBD endoscopists with at least 200 cases of experience. (2) Based on previous medical history, either antegrade or retrograde DBE was chosen. The patients in this study had symptomatic small-bowel strictures and did not have early-stage disease.
DBE complications have been reported in determining the safety of this technique for assessing the small bowel in CD patients. According to these findings, the rate of complications (e.g., bleeding, perforation, and pancreatitis) ranged between 1.2% and 1.6% [46, 47]. Nonetheless, no DBE-related adverse events were observed during our diagnostic process, confirming the safety of DBE even in CD patients with small bowel strictures.
Previous research has shown that CTE and MRE are both valuable diagnostic techniques for investigating small-bowel lesions in CD patients [48, 49]. MRE has the benefits of no requirement for radiation exposure and includes high temporal and spatial resolution. However, CTE outperforms MRE in terms of scan time, lack of artifacts, and availability in most hospitals [50]. Consequently, CTE has been recommended as a useful tool for assessing disease activity and complications in CD involving the small bowel [51, 52]. Abnormal CTE results in the small bowel normally indicate the need for DBE, so it is critical to compare DBE and CTE findings. In our study, we compared the diagnostic yields of DBE and CTE in patients with small-bowel obstructive symptoms, and DBE correctly detected more strictures than CTE. An early study looked at the role of CT in the diagnosis of small intestine obstruction. CT results were used to correctly identify 63% (29 of 46) of those with small-bowel obstruction [53]. CTE outperforms conventional CT in detecting small-bowel strictures. When different criteria and gold standards are used in different studies, the sensitivity of CTE for the detection of small-bowel stenosis ranges from 85 to 93% [28, 54,55,56]. In this study, we found that the overall diagnostic yield of CTE for establishing a diagnosis of small bowel obstruction was 85.5%, which is consistent with previous findings. Although CTE’s diagnostic ability was found to be equivalent to DBE’s, we discovered that the diagnostic efficacy varied according to the severity of symptoms. Maglinte et al. classified patients with small intestine obstruction into low-grade and high-grade partial obstructions, with CT detecting 81% of the high-grade obstructions and 48% of the low-grade obstructions [53]. These findings could be attributed to DBE’s ability to directly visualize mucosal lesions.
Our study examined not only the diagnostic ability of DBE in CD patients with small-bowel strictures but also the factors associated with DBE efficacy in these patients. Previous intra-abdominal abscess/intestinal fistula and history of CD-associated abdominal surgery were considered independent prognostic factors of DBE detection failure. Adhesions from previous surgeries and a complicated phenotype (such as intra-abdominal abscess or fistula) of CD may make DBE insertion difficult. In a multicenter retrospective study investigating DBE results and the influence on CD management, the target area of 17% of patients could not be reached due to adhesions from previous surgeries, which limited deep penetration [27]. Kohei Matsushita et al. investigated the efficacy and safety of DBE in pediatric patients after surgery. In four postoperative patients and 2 nonoperative patients, there was difficultly in transanal pleating due to adhesions or thickening of the intestinal wall caused by inflammation (P = 0.02) [57]. These findings are consistent with our conclusion that DBE has limitations due to strongly adhered adhesions in CD patients.
There were several potential limitations to this study. First, this was a single-center study. The patients in the study were all enrolled at a tertiary care facility. Second, all DBE procedures were conducted by three experienced IBD endoscopists, which may result in a higher diagnosis rate and better outcomes. Finally, further clinical outcome analysis in CD patients with small bowel strictures should be conducted.
Our study concludes that DBE is an effective and safe method for assessing CD patients with small-bowel strictures. Furthermore, the benefit of DBE was demonstrated in low-grade obstructions. Previous intra-abdominal abscess/intestinal fistula and history of CD-associated abdominal surgery were considered independent prognostic factors of DBE detection failure.
Data Availability
Available data are all presents in the paper.
References
Cosnes J, Gower-Rousseau C, Seksik P, Cortot A. Epidemiology and natural history of inflammatory bowel diseases. Gastroenterology. 2011;140(6):1785–94. https://doi.org/10.1053/j.gastro.2011.01.055.
Kelvin T, Thia,William J, Sandborn,William S, Harmsen AR, Zinsmeister EV, Loftus Jr. Risk factors associated with progression to intestinal complications of Crohn’s disease in a population-based cohort. Gastroenterology. 2010;139(4):1147–55. https://doi.org/10.1053/j.gastro.2010.06.070.
Futami K, Arima S. Role of strictureplasty in surgical treatment of Crohn’s disease. J Gastroenterol. 2005;40(Suppl 16):35–9. https://doi.org/10.1007/BF02990577.
Bettenworth D, Gustavsson A, Atreja A, Lopez R, Tysk C, Assche G, Rieder F. A pooled analysis of efficacy, safety, and long-term outcome of endoscopic balloon dilation therapy for patients with stricturing crohn’s disease. Inflamm Bowel Dis. 2017;23(1):133–42. https://doi.org/10.1097/MIB.0000000000000988.
Steinhardt HJ, Loeschke K, Kasper H, Holtermüller KH, Schäfer H. European Cooperative Crohn’s Disease Study (ECCDS): clinical features and natural history. Digestion. 1985;31(2–3):97–108. https://doi.org/10.1159/000199186.
Farmer RG, Hawk WA, Turnbull RB Jr. Clinical patterns in Crohn’s disease: a statistical study of 615 cases. Gastroenterology. 1975;68(4):627–35. https://doi.org/10.1016/s0016-5085(75)80270-8.
Freeman HJ. Natural history and long-term clinical course of Crohn’s disease. World J Gastroenterol. 2014;20(1):31–6. https://doi.org/10.3748/wjg.v20.i1.31.
Louis E, Collard A, Oger AF, Degroote E, Aboul Nasr El Yafi FA, Belaiche J. Behaviour of Crohn’s disease according to the Vienna classification: changing pattern over the course of disease. Gut. 2001;49(6):777–82. https://doi.org/10.1136/gut.49.6.777.
Louis E, Michel V, Hugot JP, Reenaers C, Fontaine F, Delforge M, El Yafi F, Colombel JF, Belaiche J. Early development of stricturing or penetrating pattern in Crohn’s disease is influenced by disease location, number of flares, and smoking but not by NOD2/CARD15 genotype. Gut. 2003;52(4):552–7. https://doi.org/10.1136/gut.52.4.552.
Oostenbrug LE, van Dullemen HM, te Meerman GJ, Jansen PL, Kleibeuker JH. Clinical outcome of Crohn’s disease according to the Vienna classification: Disease location is a useful predictor of disease course. Eur J Gastroenterol Hepatol. 2006;18(3):255–61. https://doi.org/10.1097/00042737-200603000-00005.
Nakano M, Oka S, Tanaka S, Aoyama T, Watari I, Hayashi R, Miyaki R, Nagai K, Sanomura Y, Yoshida S, Ueno Y, Chayama K. Clinical usefulness of classification by transabdominal ultrasonography for detection of small-bowel stricture. Scand J Gastroenterol. 2013;48(9):1041–7. https://doi.org/10.3109/00365521.2013.822546.
Abreu MT, Taylor KD, Lin YC, Hang T, Gaiennie J, Landers CJ, Vasiliauskas EA, Kam LY, Rojany M, Papadakis KA, Rotter JI, Targan SR, Yang H. Mutation in NOD2 are associated with fibrostenosing disease in patients with Crohn’s disease. Gastroenterology. 2002;123(3):679–88. https://doi.org/10.1053/gast.2002.35393.
Takenaka K, Ohtsuka K, Kitazume Y, Matsuoka K, Fujii T, Nagahori M, Kimura M, Fujioka T, Araki A, Watanabe M. Magnetic resonance evaluation for small bowel strictures in Crohn’s disease: comparison with balloon enteroscopy. J Gastroenterol. 2017;52(8):879–88. https://doi.org/10.1007/s00535-016-1284-z.
Tielbeek JA, Makanyanga JC, Bipat S, Pendsé DA, Nio CY, Vos FM, Taylor SA, Stoker J. Grading Crohn disease activity with MRI: interobserver variability of MRI features, MRI scoring of severity, and correlation with Crohn Disease Endoscopic Index of Severity. AJR Am J Roentgenol. 2013;201(6):1220–8. https://doi.org/10.2214/ajr.12.10341.
Liu W, Liu J, Xiao W, Luo G. A diagnostic accuracy meta-analysis of CT and MRI for the evaluation of small bowel Crohn disease. Acad Radiol. 2017;24(10):1216–25. https://doi.org/10.1016/j.acra.2017.04.013.
Wang JJ, Guo QZ, Zhao JP, Liu M, Liao GQ, Chen NJ, Tian D, Wu XL. Multidetector CT enterography versus double-balloon enteroscopy: comparison of the diagnostic value for patients with suspected small bowel diseases. Gastroenterol Res Pract. 2016;5172873. https://doi.org/10.1155/2016/5172873.
Iddan G, Meron G, Glukhovsky A, Swain P. Wireless capsule endoscopy. Nature. 2000;405(6785):417. https://doi.org/10.1038/35013140.
Barkin J, Friedman S. Wireless capsule endoscopy requiring surgical intervention: the world’s experience. Am J Gastroenterol. 2002;97(9):298. https://doi.org/10.1016/s0002-9270(02)05390-x.
Cave D, Legnani P, de Franchis R, Lewis BS. ICCE consensus for capsule retention. Endoscopy. 2005;37(10):1065–7. https://doi.org/10.1055/s-2005-870264.
Cheifetz AS, Kornbluth AA, Legnani P, Schmelkin I, Brown A, Lichtiger S, Lewis BS. The risk of retention of the capsule endoscope in patients with known or suspected Crohn’s disease. Am J Gastroenterol. 2006;101(10):2218–22. https://doi.org/10.1111/j.1572-0241.2006.00761.x.
Mow WS, Lo SK, Targan SR, Dubinsky MC, Treyzon L, Abreu-martin MT, Papadakis KA, Vasiliauskas EA. Initial experience with wireless capsule enteroscopy in the diagnosis and management of inflammatory bowel disease. Clin Gastroenterol Hepatol. 2004;2(1):31–40. https://doi.org/10.1016/s1542-3565(03)00289-1.
Yamamoto H, Sekine Y, Sato Y, Higashizawa T, Miyata T, Iino S, Ido K, Sugano K. Total enteroscopy with a nonsurgical steerable double-balloon method. Gastrointest Endosc. 2001;53(2):216–20. https://doi.org/10.1067/mge.2001.112181.
Yamamoto H, Sugano K. A new method of enteroscopy: the double-balloon method. Can J Gastroenterol. 2003;17(4):273–4. https://doi.org/10.1155/2003/309532.
Yamamoto H, Yano T, Kita H, Sunada K, Ido K, Sugano K. New system of double-balloon enteroscopy for diagnosis and treatment of small intestinal disorders. Gastroenterology. 2003;125(5):1556. https://doi.org/10.1016/j.gastro.2003.03.004.
Di Caro S, May A, Heine DG, et al. The european experience with double-balloon enteroscopy: indications, methodology, safety, and clinical impact. Gastrointest Endosc. 2005;62(4):545–50. https://doi.org/10.1016/j.gie.2005.04.029.
Heine GD, Hadithi M, Groenen MJ, Kuipers EJ, Jacobs MA, Mulder CJ. Double-balloon enteroscopy: indications, diagnostic yield, and complications in a series of 275 patients with suspected small-bowel disease. Endoscopy. 2006;38(1):42–8. https://doi.org/10.1055/s-2005-921188.
Rahman A, Ross A, Leighton JA, Schembre D, Gerson L, Simon K, Lo, Waxman I, Dye C, Semrad C. Double-balloon enteroscopy in Crohn’s disease: findings and impact on management in a multicenter retrospective study. Gastrointest Endosc. 2015;82(1):102–7. https://doi.org/10.1016/j.gie.2014.12.039.
Voderholzer WA, Beinhoelzl J, Rogalla P, Murrer S, Schachschal G, Lochs H, Ortner MA. Small bowel involvement in Crohn’s disease: a prospective comparison of wireless capsule endoscopy and computed tomography enteroclysis. Gut. 2005;54(3):369–73. https://doi.org/10.1136/gut.2004.040055.
Oshitani N, Yukawa T, Yamagami H, et al. Evaluation of deep small bowel involvement by double-balloon enteroscopy in Crohn’s disease. Am J Gastroenterol. 2006;101(7):1484–9. https://doi.org/10.1111/j.1572-0241.2006.00648.x.
Mensink PB, Groenen MJ, van Buuren HR, Kuipers EJ, van der Woude CJ. Double-balloon enteroscopy in Crohn’s disease patients suspected of small bowel activity: findings and clinical impact. J Gastroenterol. 2009;44(4):271–6. https://doi.org/10.1007/s00535-009-0011-4.
Kondo J, Iijima H, Abe T, et al. Roles of double-balloon endoscopy in the diagnosis and treatment of Crohn’s disease: a multicenter experience. J Gastroenterol. 2010;45(7):713–20. https://doi.org/10.1007/s00535-010-0216-6.
Yoshida EM. The Crohn’s Disease Activity Index, its derivatives and the inflammatory bowel Disease Questionnaire: a review of Instruments to assess in Crohn’s Disease. Can J Gastroenterol. 1999;13(1):65–73. https://doi.org/10.1155/1999/506915.
Yoram Bouhnik F, Carbonnel D, Laharie, et al. Efficacy of adalimumab in patients with Crohn’s disease and symptomatic small bowel stricture:a multicentre, prospective, observational cohort (CREOLE) study. Gut. 2017;67(1):53–60. https://doi.org/10.1136/gutjnl-2016-312581.
May A, Nachbar L, Schneider M, Ell C. Push-and-pull enteroscopy using the double-balloon technique: method of assessing depth of insertion and training of the enteroscopy technique using the Erlangen Endo-Trainer. Endoscopy. 2005;37(1):66–70. https://doi.org/10.1055/s-2004-826177.
Navaneethan U, Vargo JJ, Narayanan Menon KV, Sanaka MR, Tsai CJ. Impact of balloon-assisted enteroscopy on the diagnosis and management of suspected and established small-bowel Crohn’s disease. Endoscopy Int Open. 2014;2(4):E201–6. https://doi.org/10.1055/s-0034-1377522.
Takenaka K, Ohtsuka K, Kitazume Y, et al. Comparison of magnetic resonance and balloon enteroscopic examination of deep small intestine in patients with Crohn’s disease. Gastroenterology. 2014;147(2):334–42. https://doi.org/10.1053/j.gastro.2014.04.008.
Rieder F, Bettenworth D, Ma C, et al. An expert consensus to standardise definitions, diagnosis and treatment targets for anti-fibrotic stricture therapies in Crohn’s disease. Aliment Pharmacol Ther. 2018;48(3):347–57. https://doi.org/10.1111/apt.14853.
Silverberg MS, Satsangi J, Ahmad T, et al. Toward an integrated clinical, molecular and serological classification of inflammatory bowel disease: report of a working party of the 2005 Montreal World Congress of Gastroenterology. Can J Gastroenterol. 2005;19(Suppl A):5A–36A. https://doi.org/10.1155/2005/269076. . .
Yang SK, Yun S, Kim JH, et al. Epidemiology of inflammatory bowel disease in the Songpa-Kangdong district, Seoul, Korea, 1986–2005: a KASID study. Inflamm Bowel Dis. 2008;14(4):542–9. https://doi.org/10.1002/ibd.20310.
Van Assche G, Dignass A, Panes J, et al. The second european evidence-based consensus on the diagnosis and management of Crohn’s disease: definitions and diagnosis. J Crohns Colitis. 2010;4(1):7–27. https://doi.org/10.1016/j.crohns.2009.12.003.
Yamamoto H, Kita H, Sunada K, et al. Clinical outcomes of double-balloon endoscopy for the diagnosis and treatment of small-intestinal diseases. Clin Gastroenterol Hepatol. 2004;2(11):1010–6. https://doi.org/10.1016/s1542-3565(04)00453-7.
Manes G, Imbesi V, Ardizzone S, Cassinotti A, Pallotta S, Porro GB. Use of double-balloon enteroscopy in the management of patients with Crohn’s disease: feasibility and diagnostic yield in a high-volume centre for inflammatory bowel disease. Surg Endosc. 2009;23(12):2790–5. https://doi.org/10.1007/s00464-009-0518-z.
Gay G, Delvaux M. Double balloon enteroscopy in Crohn’s disease and related disorders: our experience. Gastrointest Endosc. 2007;66(3):82–S90. https://doi.org/10.1016/j.gie.2007.06.036.
Jang HJ, Eun CS, Choi HW, et al. Double balloon enteroscopy in suspected Crohn’s Disease: the KASID Multi-Center Trial. Gastrointest Endosc. 2008;67(5):AB273. https://doi.org/10.1016/j.gie.2008.03.760.
Ohmiya N, Arakawa D, Nakamura M, Honda W, Shirai O, Taguchi A, Itoh A, Hirooka Y, Niwa Y, Maeda O, Ando T, Goto H. Small-bowel obstruction: diagnostic comparison between double-balloon endoscopy and fluoroscopic enteroclysis, and the outcome of enteroscopic treatment. Gastrointest Endosc. 2009;69(1):84–93. https://doi.org/10.1016/j.gie.2008.04.067.
Mensink P, Haringsma J, Kucharzik T, et al. Complications of double balloon enteroscopy: a multicenter survey. Endoscopy. 2007;39(7):613–15. https://doi.org/10.1055/s-2007-966444.
Möschler O, May AD, Müller MK, Ell C. Complications in double-balloon-enteroscopy (DBE): results of the german DBE register. Gastrointest Endosc. 2007;65(5):AB158. https://doi.org/10.1016/j.gie.2007.03.238.
Ochsenkühn T, Herrmann K, Schoenberg SO, Reiser MF, Göke B, Sackmann M. Crohn’s disease of the small bowel proximal to the terminal ileum: detection by MR enteroclysis. Scand J Gastroenterol. 2004;39(10):953–60. https://doi.org/10.1080/00365520410003218.
Chiorean MV, Sandrasegaran K, Saxena R, Maglinte DD, Nakeeb A, Johnson CS. Correlation of CT enteroclysis with surgical pathology in Crohn’s disease. Am J Gastroenterol. 2007;102(11):2541–50. https://doi.org/10.1111/j.1572-0241.2007.01537.x.
Hara AK, Swartz PG. CT enterography of Crohn’s disease. Abdom Imaging. 2009;34(3):289–95. https://doi.org/10.1007/s00261-008-9443-1.
Panes J, Bouhnik Y, Reinisch W, Stoker J, Taylor SA, Baumgart DC, Danese S, Halligan S, Marincek B, Matos C, et al. Imaging techniques for assessment of inflammatory bowel disease: Joint ECCO and ESGAR evidence-based consensus guidelines. J Crohns Colitis. 2013;7(7):556–85. https://doi.org/10.1016/j.crohns.2013.02.020.
Bruining DH, Siddiki HA, Fletcher JG, Sandborn WJ, Fidler JL, Huprich JE, Mandrekar JN, Harmsen WS, Evans PE, Faubion WA, et al. Benefit of computed tomography enterography in Crohn’s disease: effects on patient management and physician level of confidence. Inflamm Bowel Dis. 2012;18(2):219–25. https://doi.org/10.1002/ibd.21683.
Maglinte DD, Gage SN, Harmon BH, et al. Obstruction of the small intestine: accuracy and role of CT in diagnosis. Radiology. 1993;188(1):61–4. https://doi.org/10.1148/radiology.188.1.8511318.
Fiorino G, Bonifacio C, Peyrin-Biroulet L, et al. Prospective comparison of computed tomography enterography and magnetic resonance enterography for assessment of disease activity and complications in ileocolonic Crohn’s disease. Inflamm Bowel Dis. 2011;17(5):1073–80. https://doi.org/10.1002/ibd.21533.
Solem CA, Loftus EV, Fletcher JG, et al. Small-bowel imaging in Crohn’s disease: a prospective, blinded, 4-way comparison trial. Gastrointest Endosc. 2008;68(2):255–66. https://doi.org/10.1016/j.gie.2008.02.017.
Turetschek K, Schober E, Wunderbaldinger P, et al. Findings at helical CT-enteroclysis in symptomatic patients with crohn disease: correlation with endoscopic and surgical findings. J Comput Assist Tomogr. 2002;26(4):488–92. https://doi.org/10.1097/00004728-200207000-00002.
Matsushita K, Inoue M, Nagano Y, Koike Y, Otake K, Okita Y, Uchida K, Kusunoki M. Safety of double-balloon enteroscopy in postoperative pediatric patients. Pediatr Int. 2020;62(9):1073–6. https://doi.org/10.1111/ped.14249.
Acknowledgements
Not applicable.
Funding
This study was funded by the National Natural Science Foundation of China (82170564).
Author information
Authors and Affiliations
Contributions
Study conception and design: Jing Hu, Juan Wu; methodology: Jing Hu, NaiZhong Hu, Wei Han; Data collection: Jing Hu, Juan Wu, PeiPei Zhang, XingWang Wu; formal analysis: Jing Hu, PeiPei Zhang, Qiao Mei; funding acquisition:Qiao Mei; Writing original draft: Jing Hu; review and editing: Qiao Mei, Wei Han; visualization: Wei Han, Juan Wu, PeiPei Zhang; project administration: Wei Han.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
All methods in our study were carried out in accordance with the Declaration of Helsinki. Anhui Medical University’s Research Ethics Committee approved this study (protocol number: ETIC 5101116), and written informed consent was obtained from all patients. One participant in the study was under the age of 16, written informed consent was obtained from his guardian.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
About this article
Cite this article
Hu, J., Wu, J., Zhang, P. et al. Evaluation of symptomatic small bowel stricture in Crohn’s disease by double-balloon endoscopy. BMC Gastroenterol 23, 247 (2023). https://doi.org/10.1186/s12876-023-02839-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1186/s12876-023-02839-8