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Urs: Double-balloon enteroscopy in children

The pursuit to visualize the entire small intestine has not been satisfactory until a decade ago. Despite improvements in skills, knowledge and technique of paediatric endoscopy, it lags behind in adopting new developments. The development of double-balloon enteroscopy (DBE), originally described in 2001 by Yamamoto et al.,1 is an endoscopic technique that allows a specially trained endoscopist to navigate the entire small bowel from the oral or rectal end, or using both routes. DBE allows both diagnostic and therapeutic techniques to be performed within the small bowel, avoiding the need of an open surgical procedure.

The DBE system (Fujinon; Fujinon Inc., Japan) consists of high-resolution video endoscopes, employing a flexible over-tube, as described elsewhere.24 Two sizes of DBEs are used (EN-450T5 and EN-450P5/20). The EN-450T5 has a working length of 200 cm, an outer diameter of 9.4 mm and a 2.8-mm forceps channel, allowing therapeutic intervention. The EN-450P5/20 has a working length of 200 cm, an outer diameter of 8.5 mm and a 2.2-mm forceps channel. The endoscopes and over-tube have balloons fitted at the distal tip of each, which are sequentially inflated and deflated with air from a pressure-controlled pump system with a maximum inflatable pressure of 45 mmHg. When inflated with air, the balloons can grip sections of small intestine and ‘shorten’ the small intestine by pleating it over the endoscope. Sequential shortening of the small intestine over the endoscope and advancement of the endoscope enables a comprehensive examination of the small intestine.

The approach (oral, anal or both) is determined by a paediatric gastroenterologist based on clinical judgement or by the findings of wireless capsule endoscopy (WCE). The insertion of the endoscope is continued until target lesions are reached, total enteroscopy achieved or no further progress possible. Both approaches are used if inspection of the whole intestine is needed. In these cases, the most distal part of the small bowel negotiated by the trans-oral approach is ‘tattooed’ in the submucosal plane with an endoneedle, and submucosal injection of methylene blue. DBE is then performed via the trans-anal approach to attain the marked area. The progression is assessed on the assumption that each set of manoeuvres to advance the endoscopes traverses around 30 cm of bowel for the trans-oral and 20 cm for the trans-anal approach, with a diminishing distance when more attempts at advancement are made.

Initial reports of use in children were documented,5 with most studies in abstract form.69 The first report in the paediatric population was published in 2007 by Leung10 in a small number of children, and since this there has emerged a body of literature of DBE in children documenting the safety, feasibility and diagnostic usefulness of the technique.24,1113 The series by Nishimura et al.2 is to date the largest paediatric patient group to undergo DBE.

We published the largest case series to date of the experience of DBE in children and prospectively evaluated the diagnostic and therapeutic utility of DBE, compared with WCE, in a setting of a single tertiary care paediatric referral centre.14 A total of 113 DBE procedures in 58 consecutive children aged < 18 years (36 boys, 22 girls; median age 12.7 years, range 1–18 years) were performed for a variety of suspected small bowel disorders between December 2008 and March 2012. A prior evaluation with upper gastrointestinal (GI) endoscopy and ileo-colonoscopy was performed in all children. A further 19 children had undergone radiological investigations of the small bowel (magnetic resonance imaging, n = 11; barium, n = 5; computerized tomography, n = 3), with 54 children receiving WCE. The overall median (range) examination time was 92.5 (45–275) minutes with median (range) estimated insertion length of small bowel distal to pylorus of 230 cm (80–450 cm), and proximal to ileocaecal valve was 80 cm (5–275 cm). The common indications resembled adult studies with polyposis syndromes (n = 21) and obscure GI bleeding (n = 16). The various findings noticed were polyps (n = 19), mucosal ulcers and erosions (n = 8), submucosal elevations with white nodules (n = 4) and angioma/angiodysplasia (n = 2). There was improved diagnostic yield for small bowel lesions at 77.7% (42/54) with prior WCE. In around 47% of children, endotherapeutics were attempted and in about 73% it led to a change in management (42/58). Minor complications in three children (5.2%) were noted with an uneventful recovery.14

A summary of large, published reports is shown in Table 1. The safety profile of DBE in children has shown to be similar to adult studies. There are no major complications – only minor complications have so far been reported. We also highlighted that children with surgically altered anatomy and poor general condition are at a higher risk of complications, irrespective of the therapeutic nature of the procedure. In the adult literature, acute pancreatitis, perforation and bleeding are known significant complications. In pooled data from the German Multicentre Survey, involving 2245 procedures, an overall complication rate of 1.2% was reported.15 In a multicentre survey conducted by Mensink et al.,16 the complication rate for diagnostic procedures was 0.8%, and for therapeutic procedures this increased to 4%.

TABLE 1

A summary of published paediatric reports

Study details Leung (2007)10 Liu et al. (2009)4 Lin and Erdman (2010)3 Nishimura et al. (2010)2 Shen et al. (2012)13 Urs et al. (2014)14
Country Hong Kong China USA Japan China UK
Number of patients 26 31 11 48 30 58
Examination time, oral/anal (minutes) 90/120 40/70 132/130 103/76 77/95 80/40
Diagnostic yield (%) 88 81 46 65 97 70.7
Depth of insertion, oral/anal (cm) 200–300/– 265/65 250/300 230/80
Therapeutic yield (%) 20 40 10 46.5
Complications Sore throat (n = 1) None Abdominal pain (n = 5) Bleeding (n = 1) Sore throat (n = 6); abdominal pain (n = 8) Perforation (n = 1)
Number of procedures 30 33 13 92 35 113
Age range (years) 4–29 3–14 8–20 4–18 5–18 1–18
Full enteroscopy, n/N (%) 2/2 5/9 (56) 12/40 (30)

A lower percentage of full enteroscopy is documented in the paediatric population than in the adult population, although the reason for this has not been identified. It has been suggested that children’s smaller abdominal cavity produces sharper angles during enteroscopy. The rate of complete enteroscopy in our study population was 30% (resembling Western success rates),14 compared with 56% reported by the Nishimura group (resembling higher Eastern success rates).2 The overall median examination time was also slightly longer than in adult studies and may reflect the technical difficulty, expertise and experience, lack of paediatric-sized endoscopes, younger patients and use of general anaesthesia.

The indications in the paediatric population include obscure GI bleeding, investigation of abdominal pain, inflammatory bowel disease, chronic diarrhoea, surveillance and treatment of polyposis syndrome, and assessment of biliary strictures after Roux-en-Y hepaticojejunostomy (Table 2).17 The most common indication in our group was polyposis syndrome followed by obscure GI bleeding. In Nishimura et al.2 the main indication was represented by a highly selected group of patients, such as those affected by biliary stenosis after living donor liver transplantation.

Our study was unique, combining the evaluation using WCE before DBE in all patients with suspected small bowel disorders and comparing the diagnostic yield. The overall diagnostic yield was significantly higher with positive WCE at 75% compared to 27.5% after a negative WCE. Earlier studies in both adult and paediatric settings reported DBE diagnostic yields ranging from 48% to 86% as a result of differing relative indications.1,2,1822 Our study also could contribute significantly to the diagnostic and therapeutic algorithm for the management of small bowel diseases in children. However, little was reported about the therapeutic benefits of DBE in the paediatric population, but our cohort suggested comparable results to adult studies and closely resembles other paediatric data (see Table 1).

TABLE 2

A summary of indications for DBE

Diagnostic Therapeutic
Obscure GI bleeding Haemostasis
Evaluation of coeliac disease Polypectomy
Malabsorption Treatment of stenosis
Crohn’s disease Retrieval of foreign bodies
Hereditary polyposis syndromes ERCP in patients with Billroth type II stomach or Roux-en-Y anastomosis
ERCP in patients with altered surgical anatomy Gastrostomy placement in abnormal anatomy
Suspected tumours Treatment of early postoperative small bowel obstruction

ERCP, endoscopic retrograde cholangiopancreatography.

The results from various paediatric studies suggest that DBE is a safe, efficacious and useful tool in the diagnosis and treatment of small bowel disease in children. In addition, in our series the diagnostic yield of DBE was comparable to that of WCE, with considerable therapeutic implications, and with its minimal complication rate should serve as a valuable addition to endoscopic techniques. Nevertheless, the two techniques should be considered not competing, but complementary. DBE offers a less invasive approach that may reduce the need for surgery and associated morbidity, particularly in selected indications such as polyposis syndrome, obscure GI bleeding and Crohn’s disease. When small bowel disease is suspected, we would suggest that less invasive WCE is carried out initially, followed by DBE, as indicated. Such a strategy will maximize the diagnostic and therapeutic potential of DBE, and the two techniques should be the mainstay of any paediatric GI unit that aspires to provide a full small bowel diagnostic and minimally invasive endotherapeutic service.

References

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Yamamoto H, Sekine Y, Sato Y, et al. Total enteroscopy with a nonsurgical steerable double-balloon method. Gastrointest Endosc 2001; 53:216–20. http://dx.doi.org/10.1067/mge.2001.112181

2. 

Nishimura N, Yamamoto H, Yano T, et al. Safety and efficacy of double-balloon enteroscopy in pediatric patients. Gastrointest Endosc 2010; 71:287–94. http://dx.doi.org/10.1016/j.gie.2009.08.010

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Lin TK, Erdman SH. Double-balloon enteroscopy: pediatric experience. J Pediatr Gastroenterol Nutr 2010; 51:429–32. http://dx.doi.org/10.1097/MPG.0b013e3181d2979c

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Moreels TG, Mensink P, Kuipers EJ, et al. Small bowel evaluation by double-balloon enteroscopy in pediatric patients: results of two university hospital endoscopy units. Gastrointest Endosc 2009; 69:AB172. http://dx.doi.org/10.1016/j.gie.2009.03.328

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Xu CD, Deng CH, Zhong J, et al. Application of double-balloon push enteroscopy in diagnosis of small bowel disease in children. Zhonghua Er Ke Za Zhi 2006; 44:90–2.

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Urs AN, Martinelli M, Rao P, Thomson MA. Diagnostic and therapeutic utility of double-balloon enteroscopy in children. J Pediatr Gastroenterol Nutr 2014; 58:204–12. http://dx.doi.org/10.1097/MPG.0000000000000192

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