Introduction

The advent of flexible fiberoptic endoscopes transformed the diagnosis and management of gastrointestinal disorders in adults and children, allowing direct visualization with targeted mucosal biopsies. Furthermore, endotherapeutic procedures are now possible throughout the upper GI tract and ileocolon. However, the small bowel, distal to the ligament of Trietz and proximal to the terminal ileum, has to date been inaccessible to conventional GI endoscopes.

The Sonde type enteroscope, developed in the 1970s, involved the introduction of a long thin fiberoscope, with an inflatable balloon attached to its distal tip, through the nose into the stomach. The fiberoscope was guided into the duodenum by a gastroscope and the balloon attached to the tip of the fiberoscope was inflated. Normal peristalsis ensured the movement of the fiberoscope down the small bowel and theoretical visualization of the entire small bowel. However, the procedure itself was cumbersome and limited by lack of therapeutic potential.

Push enteroscopy, introduced in the 1990s, allowed access to the proximal small bowel beyond the ligament of Trietz. This was improvised by the addition of a semirigid overtube which made it possible to reach up to 70–100 cm of small bowel beyond the pylorus. In addition to diagnosis, endotherapy became achievable with push enteroscopy, although limited to the jejunum. The indications in adults for push enteroscopy included overt and occult GI bleeding, iron deficiency anemia abdominal pain, Crohn’s disease, percutaneous endoscopic jejunostomy (PEJ) placement, and ERCP (Billroth type II). Push enteroscopy has been evaluated extensively in adults with a diagnostic yield of 41–75%. There is one report of its use in children.

Nevertheless, the diagnosis of small bowel disease beyond the proximal jejunum still remained a challenge, never mind proximal to the distal ileum. Intraoperative enteroscopy technique was developed needing an operative colotomy or enterotomy through which the endoscope was passed to visualize the small bowel. This had a very good diagnostic yield but carried a high complication rate. This technique was further refined by performing an initial upper GI endoscopy and a subsequent colonoscopy, and the surgeon manually threaded the small bowel over the tip of the endoscope, thus avoiding an enterotomy, with the advent of laparoscopic assistance. Intraoperative laparoscopy‐assisted push enteroscopy offers an advantage in that the whole of the small bowel may be examined endoluminally. However, of course, this involves handling of the bowel, and the need for both a surgeon and an endoscopist.

Wireless capsule endoscopy (WCE) was the next major advance in the diagnostic assessment of the mid‐small bowel. WCE made it possible to visualize the entire small bowel. The main advantage has been the relative noninvasiveness of this procedure with good diagnostic yield. WCE has been found to be superior to push enteroscopy in the diagnosis of obscure GI bleeding in adults. However, the major limitations of WCE have been the inability to perform air insufflations, rinsing of tissue, taking biopsies or undertaking endotherapeutic procedures, and thus its major utility is limited to diagnostic input alone, at least so far. Complications, although rare, do exist and are mainly in the form of capsule retention that requires surgical intervention; however, the need for removal is extraordinarily rare.

In 2001, Yamamoto et al. reported a new method where two balloons were used, one at the tip and the other at the distal end of an overtube, to perform total enteroscopy without the need for laparotomy. Double‐balloon enteroscopy (DBE) was thus born. DBE enables high‐resolution endoscopic imaging of the entire small bowel, with the advantage over WCE of potential for mucosal biopsies and interventional endotherapy (e.g., nonvariceal hemostasis, snare polypectomy, and pneumatic balloon stricture dilation).

Double‐balloon enteroscopy technique

The pediatric DBE system (Fujinon Inc., Japan) (Figure 14.1) consists of a high‐resolution video enteroscope (EN‐450P5/20) with a flexible overtube (TS‐12140). The video enteroscope has a working length of 200 cm and an outer diameter of 8.5 mm while the flexible overtube has a length of 140 cm and outer diameter of 12 mm. The enteroscopes either have a 2.2 mm (“P” scope) or a 2.8 mm (“T” scope) forceps channel that enables routine biopsy, and the latter allows other common therapeutic interventions. The enteroscope and the overtube are fitted with a balloon each at the tip. The overtube and balloons are disposable. The balloons can be inflated and deflated with air from a pressure‐controlled pump system with maximum inflatable pressure of 60 mmHg. Since the inflation of balloons is pressure‐controlled, they can be used safely, regardless of the diameter of the small bowel. The balloons help to anchor the scope and/or the overtube and stabilize the intestinal wall. This enables the further advance of the scope. The overtube prevents bending or looping of the intestine.

Both balloons are deflated at the start of the procedure. On reaching the distal duodenum or preferably jejunum, the overtube balloon is inflated to fix and stabilize the overtube within the lumen. Subsequently, the enteroscope is advanced as far as possible. Then the enteroscope tip balloon is inflated and the overtube balloon is deflated. The overtube is now advanced to reach the enteroscope tip. The overtube is again inflated and both enteroscope and overtube are gently withdrawn together in order to “concertina” the small bowel over both. The whole procedure is repeated and each set of maneuvers (or “passes”) can allow up to 40–60 cm of small bowel to be examined, until the terminal ileum (TI) is reached (Figure 14.2). If the TI is not reached then the most distal region reached is “tattooed” in the submucosal plane with an endo‐needle, using a bleb of normal saline then injected with methylene blue or indigo carmine (Figure 14.3). Alternatively 1 in 10 dyes in saline can be injected directly into the bowel wall, but there is a theoretical risk of intraperitoneal leak with this one‐step technique.

An approximate distance of postpylorus small bowel negotiation can be calculated if one assumes that 5 cm of overtube insertion equates to approximately 40 cm of small bowel. The DBE can then be repeated via the transanal route and retrograde movement from the TI proximally up the ileum, allowing full examination of the whole small bowel. Colon negotiation can be facilitated with the overtube balloon in the colon itself. Simultaneous fluoroscopy has not been found to allow further advancement of the DBE in recent studies.

On withdrawal in either procedure, close examination of the mucosal surface occurs as with standard endoscopy, but lesions are dealt with as soon as they are found, whether this is on intubation or withdrawal. Bowel preparation is as for standard ileocolonoscopy. The procedure is carried out under general anesthetic in children.

As noted above, there are two other Fujinon double‐balloon enteroscopes used in adults: the EN450T5, with a diameter of 9.4 mm and a larger accessory channel of 2.8 mm allowing for therapeutic enteroscopy, and the EN450B15 with a working length of 152 cm useful in difficult colonoscopies and ERCP in patients with Roux‐en‐Y anastomosis. These scopes allow endotherapy as opposed to the smaller pediatric endodiagnostic scope which we previously reserved for children under 3 years or 15 kg in weight. However, as experience has been gained it is clear that the more flexible smaller enteroscope has a greater chance of full small bowel examination than the stiffer “adult” enteroscope. We have attained full small bowel examination with the smaller scope. A newer smaller diameter enteroscope with a larger 2.8 mm working channel allowing more therapeutic procedures has been produced and is promising.

Pediatric experience

Limited DBE experience exists in the pediatric literature. Nishimura et al. performed 92 procedures in 48 patients using four different double‐balloon enteroscopes including a prototype. The mean duration of procedures was 96 minutes (range 30–220 minutes). The most common indication was stricture of biliary anastomosis following living donor liver transplantation (23 patients). Other indications included obscure GI bleeding (10 patients), surveillance and treatment of hereditary polyposis syndromes (five patients), abdominal pain (four patients), and inflammatory bowel disease (two patients). The overall diagnostic yield was 65%. Therapeutic interventions were performed in 40% of patients including balloon dilation, biliary stenting, or removal of stones in 13 patients, polypectomy in five patients and argon plasma coagulation in one patient. Complications reported included self‐limiting abdominal pain in 10 patients, mucosal injury of the small bowel in one patient, and postpolypectomy bleeding in one patient.

Diagnostic	Therapeutic
Obscure GI bleeding	Hemostasis
Evaluation of celiac disease	Polypectomy
Malabsorption	Treatment of stenoses
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 bowel anatomy
Suspected tumors	Treatment of early postoperative small bowel obstruction

Liu et al. reported a retrospective case series of 31 patients. Oral approach was used in 18 patients and anal approach in 11 patients. Two patients underwent both oral and anal approaches and the entire small bowel was visualized. The procedure time ranged from 40 to 70 minutes. Twenty seven of these patients were investigated for obscure GI bleeding. A source for the bleeding was found in 21 patients, giving a diagnostic yield of 77%. Angiomata and Crohn’s disease were the most common causes for bleeding. Four patients were investigated for chronic diarrhea; two were found to have lymphangiectasia, and one each had a diagnosis of IBD and celiac disease. The overall diagnostic yield was 80%.

In our own experience, initial description n = 14 (now n = 40), we have examined 40 patients: eight for Peutz–Jeghers syndrome (PJS), 24 for obscure or occult GI bleeding, two for recurrent abdominal pain, one patient with Cowden’s syndrome and persistent GI bleeding, and five for suspected but unproven (by conventional endoscopy) Crohn’s disease. The median time was 118 minutes (range 95–195 minutes) for the whole procedure. The entire small bowel was examined in six patients and a length of 200–320 cm distal to pylorus in the remaining. Sixteen patients had only an oral approach; the remainder had oral and anal approaches. Polyps were detected and successfully removed (Figure 14.4) in all eight patients with PJS, in one patient with tubulovillous adenoma of the duodenum, in one patient with significant anemia and occult bleeding, and in a patient with Cowden’s syndrome. A diagnosis was made in a patient with multiple angiomata (Figure 14.5) not amenable to endotherapy, and in one with a discrete angioma which was treated with argon plasma coagulation. The source of bleeding was identified in a further patient with varices. DBE was normal or revealed minor mucosal friability in the remaining patients. Hence, a diagnostic yield in the majority was achieved with therapeutic success in all but one in whom lesions required intervention. Incidentally, a Meckel’s diverticulum was found in one patient (Figure 14.6). Two patients with blue rubber bleb nevus syndrome had successful ablation of the lesions with argon plasma coagulation with no complications (Figure 14.7).

No complications were encountered. All patients underwent general anesthesia and were allowed home on the same day. Part of the ability to perform the procedure as a day case was due to the use of carbon dioxide insufflation – a much more rapid absorption led to a greater depth of intubation as the peritoneal cavity was thus less encumbered by gas‐filled small bowel loops preventing advancement, and once woken the patients experienced minimal or no abdominal distension‐related pain. Interestingly, the end expired CO₂ recorded during anesthesia rose, but not to any level that was considered compromising, nor higher than observed during CO₂‐assisted laparoscopy. ERCP via a balloon enteroscope is now well established in adult endoscopy, and is particularly useful when a Roux‐en‐Y loop is present.

Complications

From the three pediatric case series reported involving 107 children undergoing 186 procedures when oral and anal approaches are included, no major complications have been reported. Minor complications included abdominal pain, sore throat, minor aspiration, and bleeding following polypectomy. The lack of any significant complications reported reflects the small number of patients involved and the different indications for DBE in comparison to adults. In the adult literature, acute pancreatitis, perforation, and bleeding are known significant complications. Minor complications include pain, fever, and vomiting. Single case reports of intraperitoneal bleeding and paralytic ileus have also been published.

Several mechanisms have been proposed for the occurrence of acute pancreatitis. These include sphincter injury from direct compression by the balloons, duodenal pancreatic reflex, and direct pancreatic injury secondary to endoscopic compression of the pancreas against the spine.

In one large international survey, 40 complications occurred from 2362 procedures (1.7%). The incidences of acute pancreatitis and perforations were similar at 0.3% each. Twelve bleeding complications were reported from 364 polypectomies, none of which were a major bleed. In another large pooled data study from the German national register involving 3894 procedures, a complication rate of 1.2% was reported. Rates of acute pancreatitis were similar while perforations were higher at 3.4%. There were also six major bleeding episodes. Similar complication rates were reported in data from nine US centers.

Single‐balloon enteroscopy

Using an Olympus platform and standard push enteroscope or pediatric‐size colonoscope, this technique has its followers (Figure 14.8). It has the advantage of using existing equipment, but suffers from certain disadvantages that preclude deep small bowel intubation – this is identifed by most users. Hence, it is useful for proximal small bowel lesions, but rarely is full small bowel traverse acquired. As there is only one balloon, it relies (during withdrawal to concertina the bowel over the scope, once the balloon has been deflated to facilitate this part of the enteroscopy) on the operator trying to hook the tip of the scope over one of the valvulae coneventes in the small bowel. However, inevitably during withdrawal, there is retrograde slippage, and a seesaw motion occurs during intubation and withdrawal, after only a few “passes.” For deep small bowel intubation it is therefore not the procedure of choice, although it seems to be safe. Only one small series of seven patients exists in the pediatric literature to date. It has been used successfully in case reports in children, for example, for the treatment of small bowel varices with a child having a hepaticojejunostomy.

Spiral enteroscopy

This is an exciting recent development which arose from the application of novel thinking to an enduring problem – how to insert a flexible tube through a flexible tube. Thus, instead of pushing, this principle is the screw and advance concept, thus pulling the enteroscope through the small bowel. A mathematical relationship exists between the rotational force/movement, the acuteness of the spiral, and the resultant forward progression of the tip of the scope.

A disposable overtube with an outer spiral is placed transorally over an endoscope (Figure 14.9) – typically, a Fujinon enteroscope at present – and after the pylorus is negotiated, the operator simply rotates the handles of the overtube which remain outside the patient in a clockwise direction to produce forward movement (Figure 14.10). Remarkable forward movement with simultaneous “concertina”‐ing of the small bowel over the instrument occurs. When this motion is stopped, then stable nonmovement of the tip of the scope can be observed. Simple reversal (counterclockwise) results in removal of the tip of the scope through the small bowel. With this degree of control, lesions can be targeted accurately for endotherapy without the distraction of intestinal peristalsis. Recent large adult studies have been published, although some groups identify that the diagnostic yield may be less than that of DBE, although insertion depth seems to be greater than SBE.

Intraoperative or laparoscopy‐assisted enteroscopy

It has to be said that this is an inferior technique to nonoperative enteroscopy. Intraoperative or laparoscope‐assisted enteroscopy starts with conventional enteroscopic jejunal intubation followed by surgical assistance. The endoscopist’s role is relatively passive, deflecting the tip of the instrument while the surgeon, either with hands or laparoscopic instruments, concertinas examined parts of the small bowel over the enteroscope. Both the mucosal and serosal surfaces can be examined. Very little air is insufflated into the bowel to avoid hindering the surgeon. Dimmed lights in the operating field also help to identify the position of the tip of the instrument. In experienced hands, all the small bowel is examined in 60% of cases, taking up to 2–3 hours (Figure 14.11). An enterotomy may be used to insert a sterilized enteroscope in some situations. Lesions can be marked by injection of ink or placement of a suture.

Intraoperative or laparoscopy‐assisted enteroscopy is the most successful technique for identifying sites of obscure gastrointestinal bleeding with diagnostic yields of between 83% and 100%. Laser or bipolar coagulation can be used, and resection of lesions is recommended if intraoperative. This technique has demonstrable advantages in assessment of the extent of polyposis syndromes. “On‐table” enteroscopy has a better pick‐up rate for polyps at laparotomy than external transillumination and palpation. It can be helpful to view both serosal and mucosal surfaces simultaneously, especially with transillumination, when trying to identify small isolated lesions such as isolated pockets of intestinal lymphangiectasia (Figure 14.12). When attempted in Crohn’s disease, up to 65% of patients have had lesions not previously identified in the small bowel by other investigations, including direct vision of the serosal surface of the bowel. As previously mentioned, occult Crohn’s disease can be identified in children using enteroscopy. Partial intestinal obstruction and Meckel’s diverticulum have also been identified at intraoperative enteroscopy. Small bowel neoplasia must not be forgotten as the second most common cause of obscure gastrointestinal bleeding in younger patients, accounting for 5–10% of cases in young adults. Exploratory laparoscopy and enteroscopy are important in preventing missed diagnoses.

In essence, intraoperative enteroscopy is likely to give way to DBE in the very near future.

General complications

Complications are not often encountered with simple push enteroscopy, but when the overtube is employed, significant patient discomfort has been described. Other, rare complications of the overtube include pharyngeal tear, Mallory–Weiss tear, gastric mucosal stripping, pancreatitis, and duodenal perforation. DBE may be associated with pancreatitis in some cases, especially if the overtube balloon is first inflated too proximally, i.e., this needs to occur past the ligament of Treitz. Intraoperative enteroscopy has a 5% incidence of perforation and, in one series, a 50% incidence of mucosal laceration. Prolonged ileus has been occasionally described.

None of these rare complications have been reported in the limited studies investigating children.

Conclusion

Flexible GI endoscopy is sufficient for diagnostic and therapeutic procedures in the vast majority of pediatric cases, and in adult patients with obscure gastrointestinal bleeding is known to determine the source in up to 90%. However, in the small number of cases when the pathology is confined to the small bowel beyond the reach of conventional endoscopy, WCE and DBE have a role. DBE allows examination of the entire small bowel, making it possible to diagnose small bowel Crohn’s disease, obscure GI bleeding and tumors otherwise not attainable by conventional GI endoscopy, and also to perform endotherapeutic procedures such as hemostasis, polypectomy, balloon dilation of strictures, and retrieval of foreign bodies. DBE has a high diagnostic and therapeutic yield and a low risk of complications in 1–2% of cases. DBE is feasible and safe in children.