Small bowel capsule endoscopy (CE) was introduced in 2001 as a noninvasive means of obtaining high-quality, color endoscopic images from the duodenum to the cecum. Soon thereafter, CE challenged traditional studies as the preferred method of examining the small bowel mucosa in adults. Early studies suggested superior lesion detection when compared to push enteroscopy and small bowel follow-through or enteroclysis in the evaluation of obscure gastrointestinal bleeding (GIB) and small bowel involvement of Crohn’s disease. Since those initial reports, CE has become a widely used tool in both adult and pediatric-aged patients for a number of indications including inflammatory disorders of the small bowel such as Crohn’s disease and celiac disease, obscure GIB, polyposis syndromes, unexplained growth failure, abdominal pain, and vascular anomalies. Diagnostic yield has been found to be superior to both small bowel follow-through and standard endoscopic investigation in the evaluation of children with suspected small bowel disease. As of January 2014, CE had been approved by the U.S. Food and Drug Administration (FDA) for use in children 2 years of age and older.
Equipment
The history of the development of the small bowel capsule is fascinating and has been well documented. Although several companies now produce CE equipment, most clinical and research experience involves the PillCam SB by Given Imaging (Yoqneam, Israel). This system uses a 26-mm by 11-mm capsule containing, among other things, a transmitter, battery, light source, and camera, which takes two pictures per second over a span of up to 12 hours. The images are transmitted by radiotelemetry to a recording device worn by the patient ( Figure 63-1 ). A computer workstation is then used by the provider to download and review images and to create a report. A similar system called Endocapsule is produced by Olympus using a capsule of identical size (Olympus America Inc). More recently, Intromedic Co Ltd (Seoul, Korea) introduced the MiroCam, which is a slightly smaller (24 × 11 mm) system. All three devices are FDA approved and available for purchase in the United States.
Performance of CE Study
Compared with other methods of small bowel examination including radiographic evaluation, push enteroscopy, and overtube or balloon-assisted enteroscopy, CE is easily performed. At UT Southwestern Medical Center in Dallas, it has been our institution’s experience, the capsule can be swallowed by children as young as 6 years of age. However, success of voluntary ingestion may depend more on maturity level and confidence of the child than chronologic age, as many older children and teenagers fail or refuse to swallow the capsule. In patients who are unable to swallow the capsule, endoscopic placement across the pylorus is fairly routine.
Patient Preparation
Debate continues over what type of preparation is superior before CE study. Standard instructions often include nothing by mouth for 12 hours before capsule ingestion. Then, 2 hours after capsule ingestion, the patient may take clear liquids. Four hours after ingestion, the patient may have a light meal. The use of a bowel prep the night before the study with polyethylene glycol has recently been recommended, because a meta-analysis of adult studies has shown improvement in both visualization and diagnostic yield with this regimen when compared to fasting alone. Polyethylene glycol preparation was superior to sodium phosphate–based regimens as well. The addition of simethicone just prior to capsule ingestion has also been shown to improve visualization. In the only prospective randomized controlled trial (RCT) evaluating this question in pediatric patients, a regimen of 25 mL/kg (max 1 L) of polyethylene glycol with 20 mL (376 mg) of simethicone produced significantly better visualization scores, but similar diagnostic yield, to no bowel prep, either agent alone, or to higher volumes of polyethylene glycol alone, suggesting that this may be the optimal regimen in pediatric patients.
Ingestion Versus Endoscopic Placement
Before performing CE studies in children, a fundamental question that must be answered is whether the patient will be able to voluntarily ingest the capsule. A swallowed capsule is preferable and tends to provide cleaner images, as capsule placement in small patients frequently causes mucosal trauma and self-limited bleeding that can confound the study interpretation. As mentioned previously, patients as young as 6 years of age have successfully swallowed the capsule, but children older than age 8 will more reliably succeed. Seidman et al. have proposed a trial with candy such as large jellybeans before the study date to predict success.
If a capsule cannot be swallowed, endoscopic placement across the pylorus is usually not a difficult procedure. This has been reported in children using polypectomy snares and Roth Net (US Endoscopy, Mentor, OH, U.S.A.) to advance the capsule, and a simple capsule delivery device for use with standard gastroscopes (AdvanCE, US Endoscopy) is commercially available. Successful use of this device has been reported in a series of nine children from 4- to 8-years-old.
Endoscopic capsule placement can be performed with patients in the supine position, but passage through the posterior pharynx may be facilitated by a left lateral decubitus position. Following esophageal intubation, the next difficulty may be encountered when advancing the capsule through the pylorus. If significant resistance is encountered, careful balloon dilation of the pylorus to a diameter of 11 mm or greater is possible, or a small dose of glucagon will likely lead to pyloric relaxation, permitting passage. Another option is to gently pass a pediatric colonoscope or therapeutic endoscope across the pylorus just before passing the capsule to achieve dilation of the entire upper gastrointestinal (GI) tract. In cases where the capsule cannot pass the pylorus, deposition in the stomach is not optimal, because the chances of it entering the duodenum without assistance are low. After the release of the capsule in the duodenum, it may be helpful to push the capsule as far distally as possible using the endoscope to prevent retrograde migration into the stomach. Prokinetic agents such as erythromycin or metoclopramide may be beneficial as well in preventing retrograde migration after endoscopic placement.
Image Review
Diagnostic review of capsule endoscopy studies is technically uncomplicated. The North American Society of Pediatric Gastroenterology, Hepatology and Nutrition (NASPGHAN) recently recommended that trainees should interpret 20 CE under supervision before being considered competent. Although not formally evaluated in pediatrics, this recommendation parallels the American Society for Gastrointestinal Endoscopy (ASGE) recommendations, which include completion of a gastrointestinal endoscopy training program, competence in upper gastrointestinal endoscopy and colonoscopy, and either formal training in capsule endoscopy during gastroenterology fellowship or completion of a hands-on CE course with review of the first 20 capsule studies by an experienced capsule endoscopist.
Physician review of CE studies can be time consuming, and the question has been raised whether the time required makes economic or practical sense. Viewing practices certainly vary among physicians, but early studies reported small bowel viewing times of 34 to 120 minutes for adult procedures. It has been recommended that novice viewers read studies at an image rate of no higher than 12 to 15 frames per second, with experts reading at rates of up to 20 frames per second.
Indications
There are a number of indications for small bowel CE in children. These include evaluation of small bowel mucosa for evidence of Crohn’s disease, obscure GIB, celiac disease, polyps and tumors, and graft-versus-host disease (GVHD). Other indications include evaluation of unexplained growth failure, abdominal pain, and protein-losing enteropathy or intestinal lymphangiectasia ( Figure 63-2 ). These indications have been described primarily in retrospective case series and will be discussed individually.
Crohn’s Disease
Capsule endoscopy is frequently used in the evaluation of suspected Crohn’s disease and has been shown to detect small bowel inflammation in patients with otherwise normal evaluations ( Figure 63-3 ). In adult patients, CE has been compared to enteroclysis, small bowel follow-through, and computerized tomography (CT) scan, and found to be superior in establishing the presence and extent of small bowel inflammation in patients with known or suspected Crohn’s disease. Based on prospective and retrospective data, CE has been effective in the evaluation of suspected Crohn’s disease in children as well, and been shown to influence management decisions and outcomes. CE has been prospectively and retrospectively compared to magnetic resonance enterography (MRE) in pediatric Crohn’s, showing similar sensitivity and specificity with the added advantage of picking up subtle lesions missed by MRE, but the disadvantage of missing extraintestinal disease. It has been recommended by NASPGHAN as an appropriate procedure when Crohn’s disease of the small bowel is strongly suspected but cannot be detected by other modalities.
Differentiation of Crohn’s disease from ulcerative colitis remains clinically challenging at times, but one finding that is useful in this differentiation is significant small bowel mucosal inflammation. Several pediatric studies have concluded that CE leads to reclassification of inflammatory bowel disease (IBD) from ulcerative colitis or IBD unclassified to definitive Crohn’s disease. CE may also prove useful as a noninvasive way to document mucosal healing in Crohn’s disease and to monitor for postoperative recurrence proximal to surgical anastomoses. The use of CE as first-line evaluation of the small bowel in patients with suspected Crohn’s disease has been discussed but remains controversial; however, it is clear that CE in children can be useful in the diagnosis and classification of IBD and may help to improve outcomes by facilitating appropriate choices of therapy.
Obscure Gastrointestinal Bleeding
Obscure GIB is typically defined as gastrointestinal bleeding with a source not identified by traditional upper and lower endoscopy and typically requires investigation of the small bowel. Soon after the introduction of small bowel CE, it became clear that the color images it provided were superior to radiographic evaluation in cases of suspected small bowel bleeding. Subsequently, it was determined that CE had higher diagnostic yield when compared to push enteroscopy, likely due to its ability to view a greater length of small bowel mucosa. Based on these results, CE is currently recommended as the first-line investigation for adult patients with obscure gastrointestinal bleeding. No prospective studies have been performed in children, but case reports and small retrospective series support the use of CE in pediatric populations for this indication, reporting diagnostic yields of 62% to 100%.
Celiac Disease
Traditional upper gastrointestinal endoscopy with multiple duodenal biopsies, in conjunction with serologic evaluation, remains the standard approach for the diagnosis of celiac disease in children. However, it has been suggested that the use of small bowel biopsy as a gold standard for diagnosis of celiac disease has significant limitations such as poor acceptance of endoscopy in asymptomatic patients, patchy mucosal changes that could lead to false negative results, and the possibility of more severe villous atrophy in the proximal jejunum, not reachable by standard upper gastrointestinal endoscopy. Studies have not been performed in children, but a meta-analysis of six adult studies involving 166 patients revealed a pooled sensitivity of 89% and specificity of 95% when CE was used to evaluate the proximal small bowel in patients with suspected celiac disease. Based on these results, CE appears to be a reasonable alternative to biopsy, particularly in cases where standard endoscopy is refused or not possible, diagnosis is especially challenging, or patients are not responding to appropriate therapy.
Polyposis
Children with polyposis syndromes such as Peutz-Jeghers syndrome, juvenile polyposis syndrome, and familial adenomatous polyposis are at risk of developing polyps in the small bowel. These polyps can predispose patients to complications ranging from bleeding to bowel obstruction to neoplastic transformation. Several studies have demonstrated the utility of CE in identifying polyps in the small bowel, and small blinded comparisons to barium follow-through have favored CE for this indication. When prospectively compared to MR enterography in adults, CE was found to be better tolerated while having statistically similar polyp detection rates. One small pediatric trial showed that 90% of polyposis patients preferred CE to barium follow-through. In summary, CE shows promise as a method of evaluating the small bowel in children with polyposis syndromes while avoiding exposure to radiation.
Graft-Versus-Host Disease
GVHD causes significant morbidity and mortality in patients undergoing stem cell transplantation, and the small intestine is a common site that requires investigation. Standard evaluation when gastrointestinal symptoms are present includes endoscopy with biopsy, but several groups have found CE to be useful as a low-risk, noninvasive alternative that allows visualization of a greater portion of the small bowel. In fact, Neumann et al. found that CE detected three cases of GVHD that would have been missed by standard endoscopy alone. However, three cases of GVHD were diagnosed on biopsy alone after normal-appearing upper endoscopy. Several weaknesses associated with this approach include the high prevalence of vomiting in patients with GVHD, making CE less likely to be successful, and the inability of CE to take biopsies. The lack of histologic specimens could result in failure to diagnose opportunistic infections or the misattribution of ulcerations found at CE as being due to GVHD rather than other causes such as nonsteroidal anti-inflammatory medication use.
Unexplained Growth Failure
Moy and Levine reported a series of seven patients who underwent CE following grossly and histologically normal upper gastrointestinal endoscopy and colonoscopy in the evaluation of unexplained growth failure. Four of these patients were found to have jejunal erosions or ulcerations, leading to diagnosis of and therapy for Crohn’s disease with subsequent weight gain.
Recurrent Abdominal Pain
The role of endoscopic evaluation in children with recurrent abdominal pain (RAP) is controversial. Shamir et al. performed CE in 10 children with RAP, hypothesizing those intestinal lesions beyond the reach of an endoscope may be responsible for patient symptoms. All patients subsequently underwent standard upper gastrointestinal endoscopy with biopsies. Capsule endoscopy in three patients revealed gross evidence of gastritis not seen by esophagogastroduodenoscopy, but detected on biopsy. All three subsequently responded to proton pump inhibitor therapy. In addition, evidence of ileocecal Crohn’s disease was found in a fourth patient by CE. Several months later, this patient developed classic clinical signs of Crohn’s disease. Arguelles-Arias et al. performed CE in 16 children with chronic abdominal pain. Significant findings were seen in the ileum of one patient suggestive of small bowel Crohn’s disease. Although CE is possibly helpful in rare, isolated cases, routine use of CE in children with recurrent abdominal pain without other symptoms cannot be supported based on these findings.
Protein-Losing Enteropathy/Intestinal Lymphangiectasia
Gastrointestinal protein loss can be a challenging clinical problem. CE has been used to diagnose and determine the extent of lymphangiectasia, yielding positive results in patients following normal upper gastrointestinal endoscopy due to the potentially patchy distribution of the disease or more distal location of the disease.
Limitations
The limitations of small bowel CE are apparent, and the true sensitivity of CE studies remains unknown. The greatest limitation is the inability to obtain tissue samples for histologic evaluation. In addition, the clinician reading the CE images is at the mercy of variations in gastrointestinal motility that can greatly affect the amount of mucosa that is actually seen. Other limitations include incomplete small bowel transit, luminal debris impairing visualization, inadequate bowel distention, rapid transit through portions of the bowel, and inability to steer or deflect the field of view.
Another significant limitation of CE in a pediatric population is the large size of the capsule. Although inability to swallow the capsule can easily be overcome by endoscopic placement, the ability of the capsule to traverse a child’s gastrointestinal tract can be limited by the size of the upper esophagus, pylorus, bowel lumen, and ileocecal valve. That being said, Oikawa-Kawamoto et al. recently showed that capsule endoscopy can be safely performed in young infants, reporting successful endoscopic placement in infants as young as 10 months of age and as small as 7.9 kg.
Contraindications and Complications
There are few absolute contraindications to performing CE in pediatric or adult-sized patients. In 2013, the ASGE Technology Committee listed the presence of known or suspected gastrointestinal obstructions, strictures or fistulas, cardiac pacemakers or other electromedical devices, swallowing disorders, and pregnancy as relative contraindications. In patients with known strictures when surgery is planned, CE could help surgeons identify clinically significant lesions. Safe and effective CE has been reported in patients with pacemakers as well, including one child, although telemetry should be considered for the duration of the study.
The primary complication associated with CE in children is capsule retention, or failure to naturally excrete the capsule. Atay et al. reported a series of 207 pediatric patients undergoing CE study for various indications. The capsule retention rate was 1.4%, which is similar to rates reported in larger adult series. All three patients in this series who had capsule retention had known Crohn’s disease, and all had a body mass index (BMI) below the fifth percentile for age. Thus, known Crohn’s disease and BMI less than the fifth percentile should be considered red flags for potential CE retention.
There is no recommendation as to how long a retained capsule may safely remain in the gastrointestinal tract, and the longest reported period a capsule has been retained in an adult is 6 years. However, complications such as perforation, impaction, and fracture of the capsule requiring laparotomy have been reported. Prevention of capsule retention is difficult, if not impossible. In addition, with the exception of known Crohn’s disease, in the majority of patients, small bowel contrast series has been shown repeatedly to be ineffective in identifying lesions predisposing to capsule retention. The Patency System, or Agile Capsule (Given Imaging), is a biodegradable capsule of identical size to the video capsule that may be useful in determining the safety of performing CE in adults and children. Cohen et al. recently prospectively studied patency capsules in a group of 18 patients with suspected or confirmed pediatric Crohn’s disease and found that all patients who successfully passed intact patency capsules (83%) also had uneventful CE. Indeed, at the time of this writing, only one reported patient (a 17-year-old with known Crohn’s disease) has experienced CE retention after passing an intact patency capsule (1 week prior). In summary, the literature currently suggests that passage of an intact patency capsule reduces, but does not eliminate, the risk of CE retention, and failure of the patency capsule to traverse the gastrointestinal tract should be considered a relative contraindication to capsule endoscopy.
Other potential complications include emesis related to capsule ingestion, aspiration of the video capsule, and equipment failure, which may not be evident until review of the images is attempted.
Enteroscopy
Introduction
Although capsule endoscopy has revolutionized diagnostic examination of the entire length of the small bowel, its inability to biopsy or perform therapeutic interventions when lesions are detected remains a significant limitation. However, new techniques such as balloon and spiral enteroscopy now allow fairly low-risk and reliable access to the jejunum and ileum where biopsies and standard endoscopic therapies such as polypectomy, foreign body or retained video capsule removal, stricture dilation, and hemostasis can be performed. These innovative techniques often allow deep intubation of the small intestine without the need for surgical assistance and can be performed safely in an outpatient setting.
Push Enteroscopy
Historically the most popular type of small bowel endoscopic examination, push enteroscopy, involves the gradual advancement of a specially designed, long enteroscope with a standard working channel as deeply as possible into the small intestine. Alternatively, a pediatric colonoscope is often used. The primary limitation of push enteroscopy is that sharp angulation of the duodenum dissipates the propelling force transmitted to the endoscope, resulting in loop formation in the upper gastrointestinal tract. Reducing these loops is difficult, and they significantly affect depth of intubation. True depth of insertion is difficult to measure and varies greatly among patients and examiners, but 120 to 180 cm beyond the ligament of Treitz is possible using standard push enteroscopy. Push enteroscopy has been utilized in pediatric patients to demonstrate the patchiness of celiac mucosal involvement, and has been suggested to be a useful second-step for reevaluating suspected celiac with normal duodenal histology. In adults, push enteroscopy is commonly utilized for placement of percutaneous endoscopic jejunostomy tubes in a procedure analogous to percutaneous endoscopic gastrostomy (PEG) placement. Currently there are no reports of push enteroscopy being utilized for this application in children.
Balloon Enteroscopy (Push and Pull Enteroscopy)
Double-Balloon Enteroscopy
First described in 2001, and commercially available since 2003, double-balloon enteroscopy (DBE) (Fujinon Inc, Saitama, Japan) allows evaluation and therapy of the jejunum and ileum in adults and children. The principle involved is that an overtube with an inflated balloon can anchor and shorten the intestine when retracted, while straightening the bowel yet to be examined, thereby allowing deep advancement of the enteroscope, and preventing undesired looping ( Figure 63-4 ). Thus, the force of insertion is transmitted to the tip of the enteroscope. The bowel that has already been viewed is “telescoped” on the overtube so no further stretching occurs. The “second” balloon is located at the tip of the enteroscope and is intermittently inflated to anchor the scope and prevent slippage while the overtube is gradually advanced. Well-organized, concentric rings should be created as the endoscope traverses the small bowel, signifying successful deep enteroscopy ( Figure 63-5 ). Using this technique, complete small bowel viewing from duodenum to cecum, or by a combined antegrade and retrograde approach can at times be achieved, although the rate of complete examination varies by reporting author and geographic origin of the series. The overtubes used for diagnostic and therapeutic DBE have outer diameters of 12.2 and 13.2 mm, respectively.
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