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Small bowel enteroscopy: territory conquered, future horizons

Semrad, Carol E

Current Opinion in Gastroenterology: March 2009 - Volume 25 - Issue 2 - p 110–115
doi: 10.1097/MOG.0b013e3283260916
Small intestine: Edited by David H. Alpers and William F. Stenson

Purpose of review To review recent advances in small bowel enteroscopy, focusing on indications, modifications to improve imaging and techniques, pitfalls, and clinical applications.

Recent findings The need for endoscopic access to improve diagnosis and treatment of small bowel disease has led to the development of novel technologies, video capsule, and double balloon endoscopy. Newer devices, single balloon and spiral endoscopy, are just entering clinical use. With new technologies come the trials and tribulations of learning new endoscopic skills and determining their role in the diagnosis and treatment of small bowel disease. Identification of small bowel lesions has dramatically improved. However, small bowel angulations, peristalsis, and bilious fluid in the lumen can result in false readings or missed lesions. Studies are underway to determine the best strategy to apply new enteroscopy technologies for the diagnosis and management of small bowel disease, particularly bleeding.

Summary Complete enteroscopy of the small bowel is now possible. However, because of the length of the small bowel, endoscopic examination and therapeutic maneuvers require patience and significant skill. Prospective randomized studies are needed to guide diagnostic testing and therapy with these new endoscopic techniques.

The University of Chicago, Chicago, Illinois, USA

Correspondence to Carol E. Semrad, MD, University of Chicago, 5841 South Maryland Avenue, MC 4080, S401, Chicago, IL 60637, USA Tel: +1 773 702 6921; fax: +1 773 702 5790; e-mail:

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The small bowel has been a relatively unexplored area of the gastrointestinal tract due to limited endoscopic access. The main limitations to examination are its length (360–600 cm in the adult) and tortuous anatomy in the abdominal cavity. Although sonde [1] and push [2] enteroscopy have been utilized to diagnose and treat small bowel disease, the former is time-consuming and uncomfortable and the latter limits examination to proximal jejunum. Intraoperative enteroscopy was the only treatment option for lesions deep in the small bowel. Recently, video capsule endoscopy and double balloon endoscopy (DBE) have been developed for complete examination of the small bowel and therapeutic interventions without surgery. These milestone technologies have led to new cataloguing of small bowel lesions and have altered management of small bowel bleeding [3••]. This article reviews recent advances in small bowel enteroscopy to include indications, improvements in methods, applications, limitations, and outcomes.

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The most common indication for small bowel enteroscopy is obscure gastrointestinal tract bleeding. In about 5% of individuals with gastrointestinal tract bleeding, no cause can be found at upper or lower endoscopy [4•]. Small bowel bleeding is the most common cause; however, missed lesions at upper or lower endoscopy have been reported in 26–75% of cases [4•,5]. The overall rate of gastrointestinal tract bleeding is expected to increase due to the widespread use of double and triple anticoagulation for vascular stents and concomitant heart or cerebrovascular disease [6••]. Other indications include suspected or known Crohn's disease, polyposis syndrome, chronic diarrhea, malabsorption, and refractory celiac disease. Diagnostic yield is low when enteroscopy is performed for abdominal pain without additional signs or symptoms [7]. Therapeutic indications include treatment of bleeding lesions (thermal, injection, clips), polypectomy, stricture dilation, stenting, direct percutaneous jejunostomy tube placement and endoscopic retrograde cholangiopancreatography (ERCP) in individuals with altered small bowel anatomy.

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Video capsule endoscopy

In 2000, Iddan et al. [8] reported on a wireless capsule endoscope for examination of the small bowel. The first prototype conveyed surprisingly vivid small bowel images, much like the Mars rover. In clinical trials, capsule endoscopy was found to be safe, relatively noninvasive, with excellent patient acceptance [9]. Interestingly, 13.8% of healthy individuals were found to have small bowel lesions [10]. In a meta-analysis study [11], capsule endoscopy was superior to push enteroscopy (63 versus 28%) in detecting small bowel bleeding lesions.

Capsule endoscopy was also superior to barium studies (42 versus 6%) in detecting all clinically significant small bowel lesions [11]. In the only randomized trial of first-line testing for obscure gastrointestinal tract bleeding, capsule endoscopy had a significantly higher diagnostic yield than push enteroscopy (50 versus 24%; see Table 1) [12••].

Table 1

Table 1

Major limitations of capsule endoscopy remain the inability to obtain tissue samples and the lack of therapeutic capability. Progress is being made to improve visualization, reading accuracy, and limit capsule retention in the small bowel.

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Improving visualization and image quality

Newer generation capsules have an increased field of view from 140 to 156° and soon will have increased capture rates from 2 to 4 frames per second to improve mucosal visualization and image quality. The capsule endoscope travels naturally through the small intestine propelled by peristalsis. Foamy bile and dark green fluid, particularly in the ileum, continue to limit visualization of small bowel mucosa. There have been a number of studies comparing bowel preparations and prokinetics to overnight fasting alone with conflicting results [13•]. In a recent prospective, randomized controlled trial comparing clear liquids and 8 h fast to oral sodium phosphate the night before and morning of the procedure [14•], no significant difference was found in bowel cleanliness.

Study comparisons are difficult due to differing preparations and lack of a standardized cleanliness score. A validated 3 grading systems to evaluate small bowel cleanliness [15] may help resolve whether bowel preparation improves mucosal visualization.

Simethicone, taken 20 min before capsule endoscopy, decreases small bowel air bubbles [16]. Most capsules, over 80%, reach the cecum within the 8 h battery life [13•]. Factors associated with incomplete small bowel examinations are delayed gastric transit, previous small bowel surgery, hospitalization, and poor bowel cleansing [17•].

The availability of real-time viewing will allow endoscopic placement into the duodenum in cases of unexpected delayed gastric emptying.

A second capsule endoscope is now available that has a high-resolution charge-coupled device and a real-time image viewer monitor [18]. A comparison of the two capsules available shows similar diagnostic yields. There was subjective improvement in image quality with the capsule containing the high-resolution device [19•].

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Improving reading time and accuracy

Over 50 000 images are obtained during capsule endoscopy. Over the years, software has been developed to decrease reading time. However, this may be at a cost. Reducing the number of images examined, increases the diagnostic miss rate by 2–8% when compared with standard viewing, particularly with solitary lesions [20•]. Software that automatically compresses identical small bowel images makes it difficult to detect segments of prolonged transit delays that may be clinically relevant. Reading accuracy is crucial as it guides recommendations for management. Interpretation variability is most common with angioectasias and red spots [19•]. Adherent mucous can resemble a small bowel ulcer. Air bubbles or debris can be misinterpreted as a polyp or mass lesion. There are no uniform training guidelines for reading capsule endoscopy. Diagnostic yield and reading accuracy improved in nurse-interpreted studies when a structured capsule endoscopy training program was utilized [21].

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Patency capsule to predict retention

Capsule retention in the small bowel is the main complication of capsule endoscopy. Although the overall risk is low (<1%), individuals with suspected or known Crohn's disease have a higher risk of 1.6 and 21%, respectively [22]. Other risk factors for capsule retention include chronic use of NSAIDs, previous abdominal surgery, radiation therapy, and obstructive symptoms. Small bowel barium studies are of limited value in predicting risk of capsule retention. Computed tomography (CT) and magnetic resonance (MR) enterography may be more helpful due to improved detection of small bowel wall thickening [23•]. Although capsule retention may be valuable in identifying the site of an obstructing tumor that requires surgical resection, it is a major problem in Crohn's disease. It is not always possible to extract retained capsules using DBE or other therapeutic enteroscopes. Although capsule-related intestinal obstruction is rare and capsule materials are inert, most patients prefer removal if possible.

A dissolvable capsule endoscope (patency capsule) the same size of a capsule endoscope (26 mm × 10 mm) has been developed and tested to screen patients at high risk for capsule retention in the small bowel [24]. Its lactose outer shell dissolves when retained in the intestine for more than 30 h and a hand-held scanner can track location of the thin radiofrequency identification tag in the body. Patency is determined by passage of an intact capsule or the absence of signal detection in the body after 30 h. In patients with known strictures who successfully passed the patency capsule (about 56% patients studied), there were no subsequent capsule endoscope retentions [24].

In those who retained the patency capsule, abdominal pain was common. One patient had bowel obstruction. In the everyday clinical setting, determining capsule patency in high-risk patients has proved challenging due to poor capsule salvage from the stool and difficulty in distinguishing capsule retention in the small bowel versus colon [25•].

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Double balloon endoscopy

In 2001, Yamamoto et al. [26] reported on DBE, the first enteroscope that allowed deep access into the small bowel and therapeutic capacity. The double balloon or push-and-pull technique utilizes a 145 cm overtube backloaded on a 200 cm enteroscope and a latex balloon attached to each end. Once the system is passed into the proximal small bowel, serial inflation and deflation of balloons allow pleating of bowel on the back of the overtube and forward advancement of the enteroscope into a new segment of bowel. In a prospective, controlled study in patients evaluated with both DBE and push enteroscopy [27••], depth of insertion and diagnostic yield were significantly higher with DBE (see Table 2). Push enteroscopy was associated with lower examination time, sedation, and radiograph exposure. A number of studies [28,29,30,31,32••] have reported on the methodology and diagnostic and therapeutic yields of DBE (see Table 3). In the USA, procedure time significantly decreased after the first 10 DBE cases [31]. Success of total enteroscopy (4–86%) and diagnostic yield (43–80%) using DBE varied and may reflect the learning curve or technical limitations related to previous abdominal surgery or perhaps body size.

Table 2

Table 2

Table 3

Table 3

Although gastrointestinal tract bleeding is the main indication for DBE, it is also of value in the diagnosis of small bowel Crohn's disease and lymphoma or ulcerative jejunitis in refractory celiac disease [33]. In two retrospective studies of gastrointestinal tract bleeding outcomes [34,35], 69–89% of patients with DBE-guided therapy had no further bleeding. Identification of definitive bleeding lesions had the best outcomes. A recent prospective study [36] suggests a less favorable gastrointestinal tract bleeding outcome following DBE. Rebleeding rates were similar in patients who received DBE with therapy (20%) and DBE without therapy (18%).

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Improving depth of insertion

The main limitation of DBE is failure to advance deep into the small bowel. Beyond the ligament of Treitz, the small bowel is attached on a fan-shaped mesenteric stalk of variable length, configuration, and laxity. Total small bowel enteroscopy is possible but requires significant experience (over 150 cases) to improve completion rates from 8 to 63% [32••]. The postsurgical abdomen, altered small bowel anatomy, and large body size may limit complete enteroscopy in the best of hands. Stable advancement of the enteroscope into the ileum from the anal approach is particularly challenging and failures occur in about 20% of patients [37]. There are no studies on optimal body position, abdominal pressure, or the use of an endoscope stiffener to improve depth of insertion from the oral or anal approach. Type of sedation has no effect on depth of insertion [31].

Carbon dioxide insufflation improves depth of insertion particularly from the upper approach [38••]. India ink tattooing is helpful to mark the deepest site of insertion when complete enteroscopy is desired and to mark lesions for minimally invasive surgical resection. Laparoscopic-assisted DBE can be useful for polyp removal in Peutz-Jeghers syndrome [39] and when DBE alone cannot reach small bowel bleeding lesions for technical reasons (personal experience).

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Improving therapeutics

Availability of tools that fit both the pediatric (2.2 mm) and therapeutic (2.8 mm) double balloon enteroscope channel is improving. More needs to be known about optimal settings for thermal therapy in the small bowel. Therapeutic capacity has increased particularly in the use of the double balloon technique to allow ERCP in individuals with Roux-en-Y anastomoses. In such cases, the overtube acts as a pliable, straightening device around tight bowel angulations allowing advancement into fairly long limbs.

Dilation of small bowel strictures in Crohn's disease is possible [40•] but long-term benefit is not yet known and perforation remains a risk.

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Limiting complications

Abdominal pain is common following DBE and can be lessened by the use of carbon dioxide insufflation. Diagnostic DBE has an overall complication rate of 1.7% (perforation 0.3%, bleeding 0.8%, pancreatitis 0.3%) [41•]. The cause of pancreatitis is uncertain. Advancing the overtube and enteroscope into the jejunum before inflating balloons and avoiding excessive tension on the mesentery during push–pull cycles may limit this risk. Therapeutic DBE has a relatively high complication rate of 4.3% (polypectomy bleeding 3.3%, argon plasma coagulation perforation 1.2%, dilation perforation 2.9%) [41•].

Endoscope positioning and optimal visualization for polyp removal deep in the small bowel is challenging, particularly with large Peutz-Jeghers polyps. Careful selection of nonulcerated, short strictures for dilation may limit perforations. In our experience in the USA [42], complication rates were similar to those previously reported. However, 50% of the perforations reported occurred during diagnostic procedures in patients with ileoanal or ileocolonic anastomoses.

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New enteroscopy technologies with therapeutic capacity

Single balloon enteroscopy (SBE) is similar to DBE except for the fact that the former utilizes a single balloon on the overtube and a hyper flexible endoscope tip. This decreases set-up time. The single balloon enteroscope is also stiffer that may facilitate one-to-one advancement in the small bowel and improve success rates for ileal intubation from the anal approach. In the initial clinical experience using SBE, average depth of insertion (270 cm) and diagnostic yield (54%) were similar to those with DBE [43]. Procedure time was somewhat shorter. There are no comparison studies between DBE and SBE with regard to complete enteroscopy rates.

Spiral enteroscopy is a completely new technology that consists of a 48 French rotating overtube with spiral threads. The spiral overtube can be backloaded on a double or single balloon enteroscope. After intubation of the stomach with the enteroscope, the overtube is rotated clockwise through the upper gastrointestinal tract until the spiral threads engage in the jejunum beyond the ligament of Treitz. Once free in the abdominal cavity, clockwise spinning of the overtube results in rapid pleating of small bowel onto the overtube. In a preliminary report [44], average procedure time for spiral enteroscopy was significantly shorter (32 min) than times reported for DBE (see Table 3) and SBE. However, the diagnostic yield was also lower (32%), suggesting decreased time spent performing therapeutics [44]. At present, spiral enteroscopy is limited to the oral approach.

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Comparing capsule endoscopy with double balloon endoscopy: a marriage proposal

There are a number of small studies comparing the diagnostic yield of capsule endoscopy with DBE. In a meta-analysis that included 11 studies, the overall diagnostic yield for capsule endoscopy (60%, n = 397) was similar to that for DBE (57%, n = 360) [45]. There was no significant difference in the diagnostic yields for bleeding, inflammatory findings, or tumor detection. A cost-effectiveness analysis for diagnosis of gastrointestinal tract bleeding favors capsule endoscopy over push enteroscopy and radiologic studies [46]. A cost-effectiveness analysis for management of bleeding favors DBE over all other therapeutic modalities [47]. Capsule endoscopy is patient friendly, guides DBE approach in positive studies, and predicts a low rebleeding rate in negative studies [48•]. DBE is invasive and requires significant resources and time. One approach to the management of gastrointestinal tract bleeding is to combine capsule endoscopy and DBE, reserving DBE for treatment of positive findings on capsule endoscopy or active bleeding when there is high suspicion the source is the small bowel. However, no test substitutes for good clinical judgment. Missed lesions on capsule endoscopy, most commonly tumors, have been subsequently detected by DBE [49] and radiologic studies (CT and MR enterography) [50]. All small bowel diagnostic studies must be considered in difficult cases of obscure gastrointestinal tract bleeding, particularly in the young age group.

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The golden age of complete small bowel enteroscopy has arrived. This has resulted in improved diagnosis of small bowel lesions and altered management. It has facilitated earlier diagnosis of lesions difficult to detect such as Meckel's diverticulum and Crohn's ulcerations when presenting deep in the small bowel. The highest therapeutic impact has been on the management of small bowel bleeding lesions, familial polyposis syndromes, and biliary disease in those with altered small bowel anatomy. However, there is a long and winding road ahead and much work needs to be done. Advances need to continue to improve visualization, reading and procedure times, and therapeutics.

Gastroenterologists and other healthcare providers need to be trained. What is most desired is the need for randomized, prospective studies to compare technologies and long-term outcomes, particularly in small bowel bleeding. Certainly, the past 8 years have been a remarkable start.

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References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

• of special interest

•• of outstanding interest

Additional references related to this topic can also be found in the Current World Literature section in this issue (pp. 165–166).

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bleeding; capsule; enteroscopy; overtube; small bowel

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