REVIEW
Endoscopic and Radiographic Evaluation of the Small Bowel in 2012 Charles E. Dye, MD,a Ryan R. Gaffney, DO,b Thomas M. Dykes, MD, FACR,c Matthew T. Moyer, MD, MSa a Division of Gastroenterology/Hepatology; bDepartment of Internal Medicine; cDepartment of Radiology, Penn State College of Medicine and Milton S. Hershey Medical Center, Hershey, Pa.
ABSTRACT Traditionally, the diagnosis of small bowel disorders has been challenging secondary to the small intestine’s length, tortuosity, and anatomic location. Recent technologic advancements in the field of enteroscopy and radiographic imaging have facilitated a more thorough endoscopic evaluation of patients with small bowel disease ranging from obscure gastrointestinal bleeding to inflammatory bowel disease and small bowel tumors. Such developments have made it possible to avoid invasive surgical procedures in certain clinical scenarios where they were previously the gold standard. In this review, we report an update on the diagnostic and management approach to patients with small bowel disease, emphasizing the advantages and limitations of the latest modalities now available to primary care physicians and gastroenterologists for evaluating patients with presumed disease of the small intestine. © 2012 Elsevier Inc. All rights reserved. • The American Journal of Medicine (2012) 125, 1228.e1-1228.e12 KEYWORDS: Balloon-assisted enteroscopy; Capsule endoscopy; Computed tomography enterography; Endoscopy; Obscure gastrointestinal bleeding; Push enteroscopy; Small bowel disease
The small intestine ranges from 4 to 7 m in length, extending from the pylorus to the ileocecal valve, and is divided into 3 regions (duodenum, jejunum, ileum) based on structural and functional considerations. The organ is tasked with a complex array of functions, including nutrient, electrolyte, and water absorption, and is richly innervated with both extrinsic and intrinsic neurons that manage its motor physiology. The small bowel receives its vascular supply via the superior mesenteric artery with the jejunum and ileum suspended by a thin, broad-based mesentery attached to the posterior abdominal wall, allowing free movement within the abdomen.1 Historically, despite its anatomic simplicity, accurate medical evaluation of the small bowel has proved to be more elusive. The organ is located deep within the abdo-
Funding: None. Conflict of Interest: None. Authorship: All authors had access to the data and played a role in writing this manuscript. Requests for reprints should be addressed to Ryan R. Gaffney, DO, Department of Internal Medicine, Penn State Hershey Medical Center, 500 University Drive, PO Box 850, Mail Code H039, Hershey, PA 17033. E-mail address:
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0002-9343/$ -see front matter © 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.amjmed.2012.06.017
men, where its length, mobility, and tortuosity present significant challenges to effective radiographic and endoscopic evaluation. Consequently, small bowel disease often has been difficult to diagnose, resulting in repetitive testing and poor clinical outcomes.2 The standard evaluation traditionally consisted of a mixed combination of push enteroscopy, barium small-bowel follow-through, and computed tomography (CT). Recent innovations in medical technology have resulted in significantly more effective small bowel imaging, including capsule endoscopy, deep enteroscopy, computed tomography enterography (CTE), and magnetic resonance enterography (MRE). We review these increasingly available transformative technologies and some of their most common clinical applications.
A NEW STANDARD IN SMALL BOWEL EVALUATION AND TREATMENT: WIRELESS CAPSULE ENDOSCOPY The widespread use of capsule endoscopy during the last several years has revolutionized small bowel imaging by providing a consistent and noninvasive method for complete visualization and assessment of the mucosa. Trials have repeatedly shown that capsule endoscopy is more sensitive
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than standard endoscopic and radiographic techniques and riority of capsule endoscopy over these conventional proidentifies lesions throughout the small bowel.3,4 The Pillcedures.5,6 Capsule endoscopy also is effective in the diagCam SB (Given Imaging, Yokneam, Israel) consists of 3 nosis and evaluation of small bowel mucosal disease, most main components: an ingestible disposable capsule, a data commonly illustrated by Crohn’s disease. A recent metarecorder worn by the patient, and a dedicated computer analysis of prospective studies in nonstricturing Crohn’s workstation (Figure 1). The capdisease showed the diagnostic sule is 26 ⫻ 11 mm with 4 lightyield of capsule endoscopy to be emitting diodes for illumination, a superior to small-bowel followCLINICAL SIGNIFICANCE 156-degree field of view, and a through, push enteroscopy, and battery life of approximately 8 CTE; however, the role of CTE is ● Innovations in the fields of enteroshours. Once swallowed, images evolving.2,7,8 In addition to obcopy, radiographic imaging, and wireare captured at a rate of 2 per scure gastrointestinal bleeding and less capsule endoscopy have facilitated second and transmitted to the data Crohn’s disease, capsule endosa more complete evaluation of the small recorder by radiofrequency. After copy also has proved useful in debowel in recent years, minimizing the return of the data recorder, images tecting small bowel tumors. need for intraoperative endoscopy when are processed for review using a The American Society of Gasit was previously the gold standard. sophisticated software system altrointestinal Endoscopy has publowing capture of significant palished guidelines for the clinical ● When assessing patients with small bowel thology as thumbnails for incluuse of capsule endoscopy, and aldisease, targeted evaluations should be sion into a final report. A similar though it is safe, there are some guided by clinical parameters and pasystem, the EndoCapsule (Olymimportant caveats and contrainditient-specific factors incorporating the pus Corporation, Tokyo, Japan), cations.9 One concern is diagnosadvantages, disadvantages, and availabilwas recently introduced and is tic specificity, with Crohn’s disity of each investigative modality. thought to be safe with a similar ease and inflammatory lesions diagnostic yield.5 such as nonsteroidal anti-inflamCapsule endoscopy was first matory drug enteropathy being approved for the evaluation of obscure gastrointestinal representative confounders. Furthermore, 13% of normal, bleeding. Large, well-designed, meta-analyses comparing asymptomatic persons may have mucosal breaks and minor the diagnostic yield of capsule endoscopy with small-bowel lesions detected by capsule endoscopy.3,10 Cited contrainfollow-through, push enteroscopy, and CT in patients with dications include swallowing disorders, known or suspected obscure gastrointestinal bleeding have confirmed the supeobstruction of the small bowel including strictures, im-
Figure 1 Components of capsule endoscopy system. Large image illustrates computer workstation for downloading data, as well as data interpretation and report generation. Inset from left to right: capsule model (which is swallowed), data recorder, and close-up of the data recording system.
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Figure 2 Deep enteroscopy devices: (Top) Example of a single balloon endoscopy system demonstrating the overtube fitted with an inflatable and deflatable balloon with a 200-cm enteroscope protruding from the end of the overtube. (Bottom) Example of a double-balloon endoscopy system demonstrating the overtube and its protruding enteroscope both fitted with balloons.
planted cardiac electromedical devices, and pregnancy. Patients who cannot swallow the capsule can have it placed endoscopically. In patients likely to have obstructive lesions, patency can be assessed before capsule ingestion with the self-dissolving Agile Patency Capsule system (Given Imaging, Yokneam, Israel), which is identical in size to an imaging capsule but with a soluble lactose body and a radiofrequency tag. If excretion of the intact capsule is witnessed by the patient or a scanner does not detect the tag at 30 hours, it is safe to proceed with capsule endoscopy.11 Finally, the radiofrequency signal of capsule endoscopy has a theoretic potential for electromagnetic interference with cardiac pacemakers and defibrillators. Several studies have demonstrated that is safe to perform capsule endoscopy in patients with these cardiac devices without any significant harm or interference.9,12-14
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ment of the scope and pleating of the bowel over the overtube. With proper training and experience, small bowel intubation of 240 to 360 cm can be expected, compared with traditional push enteroscopy and ileoscopy (90-150 cm and 50-80 cm, respectively).17,18 The ability to view the entire small bowel with balloon-assisted enteroscopy varies and seems to depend on factors including operator experience and patient characteristics such as prior bowel surgery, with rates of complete enteroscopy from 12% to 80%.19,20 Spiral enteroscopy is a novel endoscopic technique for deep small bowel visualization that has recently become available for clinical use. This method uses a specialized spiral-shaped overtube called the Endo-Ease Discovery Small Bowel (Spirus Medical Inc, Stoughton, Mass) that is approximately 118 cm long with raised, 5.5-mm, hollow high spirals at the distal end (Figure 3). The device has 2 handles for manual rotation with a locking mechanism on the proximal end allowing for attachment to the enteroscope. Spiral enteroscopy allows for evaluation of the small bowel by way of rotate-to-advance technology. Here, rotatory clockwise and counterclockwise movements permit pleating of the small bowel over the overtube, thereby allowing advancement and withdrawal of the enteroscope while preventing twisting of the small intestine.21 Preliminary data from a case series of 27 patients with obscure gastrointestinal bleeding demonstrated that spiral enteroscopy, by using an overtube over a pediatric colonoscope, was safe and had a diagnostic yield of 33% with an average depth of small bowel insertion to 176 cm from the ligament of Treitz.22 A recent retrospective analysis comparing single-balloon enteroscopy and spiral enteroscopy showed that a greater depth of maximal insertion was achieved with spiral enteroscopy than the single-balloon technique.23 Although the diagnostic yield of both methods were similar, spiral enteroscopy appeared to achieve a faster small-bowel evaluation with shorter procedure times. Sim-
DEEP ENTEROSCOPY With the increased detection rate by capsule endoscopy of potential pathology in the mid-small bowel, innovations in overtube-assisted deep enteroscopy have been critical to diagnose and treat pathology previously accessible only through surgical interventions. The best studied of these modalities is the double-balloon endoscopy system (Fujinon Inc, Saitama, Japan), which has a balloon on the distal end of both the endoscope and the specialized overtube, whereas the more recently introduced single-balloon endoscopy system (Olympus Corporation, Tokyo, Japan) has a balloon only on the overtube (Figure 2).15,16 The technique of balloon-assisted enteroscopy involves a series of push and pull steps, known as advancement cycles, which allow straightening of angles and more effective forward move-
Figure 3 The spiral overtube shown without its associated enteroscope. Note the characteristic raised, hollow spirals at its distal end.
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ilar data from a prospective crossover study of patients with small bowel bleeding from vascular malformations confirmed reduced examination time with spiral enteroscopy as compared to double-balloon enteroscopy, although the double-balloon technique was superior for achieving a deeper insertion depth into the small intestine.24 The potential for complications with spiral enteroscopy should not be overlooked, however, because reports of small bowel perforation and pneumoperitoneum have been described in patients with altered small bowel anatomy, including strictures and anastomoses.25 Common indications for deep enteroscopy include tissue biopsy, hemostasis, tattoo placement for surgical identification, polypectomy, balloon dilation, and foreign body retrieval (eg, retained capsules).26,27 It appears that double balloon enteroscopy has a diagnostic yield similar to capsule endoscopy in the evaluation of small bowel disease, in addition to providing biopsy and therapeutic options.27-29 Limitations of deep enteroscopy include invasiveness and complexity, often mandating additional endoscopic personnel and anesthesia support. In addition, the entire small bowel is not typically visualized in a single procedure, current reimbursement may not be commensurate with endoscopic resource use, and there is the rare possibility of serious complications, including aspiration pneumonia, pancreatic trauma, and perforation.18,29,30 A useful clinical strategy seems to be the use of capsule endoscopy or other small bowel imaging as screening and targeting tools to optimize efficient use of deep enteroscopy.31 Made possible by the high negative predicative value of capsule endoscopy, the approach of targeted deep
enteroscopy has been shown to increase both the diagnostic (73%-93%) and therapeutic (57%-73%) yields of the procedure and can select the more productive route (antegrade vs retrograde).17,27,31,32 Reserving deep enteroscopy for positive findings on less-invasive procedures seems reasonable. However, if clinical suspicion remains high for pathology, such as persistent occult bleeding and iron-deficiency anemia suggesting malignancy, then other radiographic procedures and pursuing deep enteroscopy may be appropriate.
COMPUTED TOMOGRAPHY AND MAGNETIC RESONANCE ENTEROGRAPHY Advances in multidetector CT and the introduction of neutral density, enteric contrast have made CTE an effective imaging modality for evaluating the small bowel.30,31 Conventional CT uses high-density enteric contrast. CTE uses larger volumes of neutral density contrast (1350 mL 0.1% w/v barium with sorbitol), thinner CT slice thickness, and isotropic multiplanar reformats.33-35 The neutral density enteric contrast provides improved luminal distension compared with other enteric contrast agents and combined with intravenous (IV) contrast enhancement offers more reliable assessment of bowel wall thickness and enhancement characteristics that correlate with inflammation or hypervascular lesions.33,36 Similar imaging characteristics of the small bowel may be obtained with MRE. MRE protocols commonly use T2-weighted and IV-enhanced gradient-echo T1 weight sequences in combination with biphasic (low signal
Figure 4 Coronal reformat of CTE examination showing mural thickening and hyper-enhancement of a segment of distal ileum (black arrow) and engorged vasa recta (yellow arrow), both highly suggestive of active inflammation.
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on T1 weight sequences and high signal on T2 weight sequences) orally ingested contrast.37,38 CTE and MRE are particularly useful in the detection and evaluation of small bowel Crohn’s disease.33-36,39 Findings of active bowel inflammation include bowel wall thickening greater than 3 mm, mural hyperenhancement, and stratification (Figures 4 and 5). Extra-enteric findings of active inflammation include vasa recta congestion, mesenteric stranding/edema, fibrofatty proliferation of the mesentery, and fistula formation.33-36 Studies suggest that CTE and capsule endoscopy have equal sensitivity for Crohn’s disease (82% and 83%, respectively), and CTE may have higher specificity than capsule endoscopy (83% and 53%, respectively).34,35 The diagnostic yield of MRE and CTE for Crohn’s disease appears similar, and both modalities are better predictors of extra-intestinal disease manifestations than traditional small-bowel follow-through.37 One advantage of MRE is the lack of radiation exposure for young patients. Both modalities can detect stenosis, where capsule endoscopy would be contraindicated, and can help predict fibrostenotic versus acute inflammatory strictures.33,35,36,39 Another indication for CTE and MRE is the diagnosis of small bowel masses. The neutral density enteric contrast combined with IV enhancement facilitates detection of hypervascular small bowel masses, such as carcinoid tumors and small gastrointestinal stromal tumors (Figure 6).33,36 In
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Figure 6 Coronal reformat of CTE examination showing a small hypervascular neoplasm in the proximal small bowel (black arrow). Positive enteric contrast used in conventional CT would obscure this hyperenhancing lesion.
Figure 7 Capsule endoscopy image of a large arteriovenous malformation.
Figure 5 Coronal MRE examination showing mural thickening and hyper-enhancement of a segment of distal ileum (black arrow) and engorged vasa recta (yellow arrow), both highly suggestive of active inflammation. Although this is a different patient, note the similarity in findings with the respective CTE in Figure 4.
addition, there may be an evolving role of CTE and MRE in the assessment of obscure gastrointestinal bleeding in selected patients. One recent study yielded positive findings for bleeding sources in 10 of 22 patients with obscure gastrointestinal bleeding. Eight of those 10 positive CTE findings also were positive at capsule endoscopy or by subsequent clinical diagnosis. CTE also helped to correctly identify 3 lesions undetected at capsule endoscopy.40 Limitations of CTE include the use of ionizing radiation, nondiagnostic examinations in patients unable to tolerate a large volume of oral contrast (ie, patients
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with nausea and vomiting or anatomic alterations after bariatric surgery), and severe IV contrast allergy or significant renal disease.41
COMMON CLINICAL APPLICATIONS Obscure Gastrointestinal Bleeding Gastrointestinal bleeding is classified as overt or occult.42 Overt bleeding is present if visible blood is seen in the stool as melena or hematochezia or in the emesis as hematemesis or coffee-ground emesis. Occult bleeding is characterized by fecal occult positivity or iron-deficiency anemia without any visible blood loss to the patient or clinician. Obscure gastrointestinal bleeding has been defined as bleeding of unknown origin that persists after an initial negative evaluation by upper and lower endoscopy and radiographic evaluation of the small bowel, typically by small-bowel follow-through.43 Although representing only 5% of gastrointestinal bleeding cases, identification and treatment have historically proved difficult, with some cases ultimately
requiring invasive procedures, such as intraoperative enteroscopy after exploratory laparotomy.27,43,44,45 After the establishment of capsule endoscopy, deep enteroscopy, and CTE/MRE, however, surgery is increasingly reserved for failed resolution after deep enteroscopy.28 The first approach to obscure gastrointestinal bleeding should typically include repeat upper and lower endoscopy given the high number of missed lesions detectable by second-look endoscopy, because of slow, intermittent bleeding, compromised endoscopic visualization, or delay in the performance of endoscopy greater than 48 hours after the patient’s initial presentation.43-47 The importance of second-look endoscopy cannot be overstated, because the yields of repeat upper endoscopy and colonoscopy have been reported up to 29% and 6%, respectively, by the American Society of Gastrointestinal Endoscopy.47 If second-look endoscopy is negative, attention is turned to the small bowel, where capsule endoscopy allows a noninvasive evaluation of the entire small bowel in 79% to 90% of patients with a diagnostic yield of 38% to 83%.48,49 One of
Figure 8 Suggested approach to the evaluation and management of patients with obscure gastrointestinal bleeding. CTE ⫽ computed tomography enterography; GI ⫽ gastrointestinal; MRE ⫽ magnetic resonance enterography.
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the strengths of capsule endoscopy lies in its high positive (94%-97%) and negative (83%-100%) predictive value in the evaluation of obscure gastrointestinal bleeding.50,51 Positive findings lead to specific management in 37% to 87% of patients, with 50% to 66% of patients event-free at followup27,50,52 (Figure 7). A recent, large meta-analysis has shown that capsule endoscopy and double-balloon enteroscopy have similar diagnostic yield in small bowel evaluation and suggested that capsule endoscopy should be used first because it is less invasive, more readily available, better tolerated, and useful in guiding subsequent therapy.52 Technetium 99m–labeled red blood cell scanning can be useful in recurrent overt bleeding requiring transfusions, and the technetium 99m pertechnetate (Meckel Scan) can be useful in the diagnosis of Meckel diverticulum in younger patients with unclear sources for hematochezia.47,53 Angiography remains useful for localization of active bleeding and the diagnosis of nonbleeding vascular lesions, and has the potential to detect bleeding if the rate approaches 1.0 mL/min. The main value of angiography is its ability to perform therapeutic embolization of bleeding, albeit with a small risk of pseudoaneurysm, thrombosis, dissection, or bowel infarction.20 Advances in CT imaging will potentially prove useful in obscure gastrointestinal bleeding, such as combining CT angiography protocol IV infusion with CTE protocol oral contrast. A generalized patient care approach for obscure gastrointestinal bleeding would be to first consider repeat upper endoscopy and colonoscopy because of the significant rate of missed lesions (Figure 8). Clinical signs, such as the color of nasogastric tube aspirate or the presence of hematemesis or melena, may help determine which endoscopic method to proceed with first. Patients with fecal occult positivity should be managed on the basis of the presence or absence of iron-deficiency anemia, keeping in mind that a major problem with guaiac-based fecal occult blood testing is a high rate of false-positive results. If no iron deficiency is present, further testing after upper endoscopy and colonoscopy is typically not warranted unless the patient has recurrent bleeding or a precipitous decline in hemoglobin and hematocrit data.47 For those patients with overt, visible bleeding or occult bleeding with associated iron deficiency and lack of significant findings on repeat endoscopy and colonoscopy, wireless capsule endoscopy should be considered with possible intervention (push enteroscopy, deep enteroscopy, surgical referral) as appropriate according to the type of lesion and its location. In patients with potential contraindications to capsule endoscopy, such as suspected stricture or partial obstruction, CTE or MRE may be considered as an initial test. In patients with active, overt bleeding, management must be adjusted according to the situation. Therapy initially begins with resuscitation efforts to stabilize the patient. If the patient is hemodynamically stable, choices include capsule-guided deep enteroscopy or proceeding directly to deep enteroscopy after a negative bidirectional
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endoscopy. In the setting of rapid bleeding with instability, it may be prudent to perform a radioisotope bleeding scan or immediate angiography to treat the bleeding source. Intraoperative enteroscopy should be reserved for patients with severe, recalcitrant bleeding and those in whom a small bowel lesion is not accessible to deep enteroscopy.27,43,47
Inflammatory Disease of the Small Bowel Inflammatory and ulcerative disease of the small bowel typically presents with painful symptoms and may be associated with overt or occult gastrointestinal bleeding. Crohn’s disease is a common example, and colonoscopy with examination of the terminal ileum often provides the initial clinical diagnosis. Other common causes are aspirin and nonsteroidal anti-inflammatory medications, where upper endoscopy may first be informative. When inflammatory, ulcerative disease is located in the mid-bowel, diagnosis and evaluation are more challenging, requiring one of the newer small bowel imaging modalities discussed earlier. Capsule endoscopy can be useful for diagnosing Crohn’s disease in patients with symptoms suggestive of inflammatory bowel disease or in patients with indeterminate colitis.9 A recent meta-analysis of patients with clinical signs and symptoms of small bowel disease demonstrated a detection rate of 55.3% when capsule endoscopy was being used in a patient population with suspected or known Crohn’s disease.54 By facilitating effective imaging of the entire small bowel, capsule endoscopy can detect even subtle flat lesions, thereby enabling assessment of disease activity in patients with established Crohn’s disease (Figure 9). In a large retrospective study of 134 symptomatic patients with
Figure 9 Capsule endoscopy image of diffuse small superficial mid-bowel ulcers consistent with Crohn’s enteritis in a patient with previous biopsy-proved Crohn’s ileocolitis.
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Figure 10 Evaluation of suspected Crohn’s disease involving the small bowel. Adapted from Mergener K, Ponchon T, Gralnek I, et al. Literature review and recommendations for clinical application of small-bowel capsule endoscopy, based on a panel discussion by international experts. Endoscopy. 2007;39:895-909.48 CTE ⫽ computed tomography enterography; MRE ⫽ magnetic resonance enterography.
Crohn’s disease, a diagnostic yield comparable to ileoscopy and superior to small-bowel follow-through was reported for capsule endoscopy when both diagnostic and suspicious findings were considered. Of note, this study showed that capsule endoscopy yielded negative findings in 48% of symptomatic patients, suggesting the presence of other disease processes and avoiding unnecessary therapeutic modification and further invasive testing.55 Despite a comparable detection rate and high sensitivity for patients with small intestinal inflammatory bowel disease, capsule endoscopy should not be used in patients with known or suspected stricturing type disease given the risk for capsule retention. A preprocedural small-bowel followthrough does not exclude the presence of a stricture, because retention rates were reported in up to 5% of patients who underwent a small-bowel follow-through before the deployment of a capsule.56 Therefore, capsule endoscopy should be performed only after a reassuring patency capsule examination or CTE or MRE result, because the typical capsule retention rates of 1.5% to 5% will be higher in this setting.8,9 As such, there is growing support for CTE as the
initial imaging modality in ulcerative disease with suspected stenosis.8,33-36 In the assessment of patients with presumed or known small bowel inflammatory bowel disease, a generalized clinical approach would first begin with colonoscopy with examination and biopsy of the ileum for the initial diagnosis (Figure 10). If this is nondiagnostic or proves to be a difficult examination, small bowel evaluation is then essential, with the test of choice being capsule endoscopy with its high sensitivity after giving consideration to stricturing disease. In clinical scenarios where the risk of stricturing is high, as in the patient who presents with recurrent small bowel obstructions, we recommend evaluation with CTE, MRE, or a patency capsule first. The results of capsule endoscopy or CTE/MRE can then guide the use of enteroscopy for definitive histopathologic diagnosis by biopsy in the appropriate clinical situation.
Small Bowel Tumors Both malignant (adenocarcinoma, carcinoid, lymphoma, and sarcoma) and benign (adenoma, leiomyoma, fibroma,
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Figure 11 Diagnostic and management algorithm for a patient with a suspected small bowel tumor detected on capsule endoscopy. Adapted from Mergener K, Ponchon T, Gralnek I, et al. Literature review and recommendations for clinical application of small-bowel capsule endoscopy, based on a panel discussion by international experts. Endoscopy. 2007;39:895-909.48 CTE ⫽ computed tomography enterography; MRE ⫽ magnetic resonance enterography.
Figure 12 Image from CT examination without the use of enteric contrast demonstrates dilated, fluid-filled small bowel consistent with obstruction. The wall of the obstructed small bowel has decreased enhancement (black arrow) compared with a normally enhancing adjacent small bowel loop (yellow arrow), suggesting the obstructed bowel also is ischemic.
and lipoma) tumors can arise in the small bowel. The frequency of these lesions is reported to be 6% to 12% in patients undergoing capsule endoscopy, most commonly for obscure gastrointestinal bleeding.57 These less common entities traditionally are diagnosed late because of the vague nature of their presenting symptoms, often with poor treatment outcomes. Although radiographic and endoscopic tools are available, there is no established consensus recommending the best, single method for evaluating patients with suspected small bowel tumors. New imaging modalities may facilitate earlier detection; however, limitations with bowel distention and missed lesions may translate to a role for deep enteroscopy when suspicion is high, even with negative capsule endoscopy and CTE findings.40,58,59 In the evaluation of a patient with a possible small bowel tumor, no specific endoscopic or radiographic test is recommended as the initial imaging study of choice. However, current literature does not seem to suggest the use of an upper gastrointestinal series with small-bowel followthrough as the first test to be performed primarily because of its limited sensitivity.57 Large meta-analyses have compared capsule endoscopy with other diagnostic modalities,
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such as small-bowel follow-through, push enteroscopy, and CT imaging in patients with obscure gastrointestinal bleeding, and have confirmed the superiority of capsule endoscopy over these conventional procedures for the detection of small bowel tumors.4,6-7 A recent single-center retrospective study compared the performance of CTE and capsule endoscopy in identifying small bowel tumors. In a subgroup of 17 patients who underwent both CTE and capsule endoscopy for full evaluation, CTE was found to be more sensitive than capsule endoscopy (94.1% vs 35.3%) in detecting small bowel neoplasms.60 One significant limitation to capsule endoscopy that bears mention is the possibility of false-positive data, particularly if transient bulges into the small bowel lumen seemingly appear as a submucosal mass.58,61 False-negative results also need to be considered, especially for those patients with a high clinical suspicion of Table 1
a solitary lesion such as adenocarcinoma. In these cases, deep enteroscopy or even intra-operative enteroscopy may be necessary for complete reassurance. In addition, capsule endoscopy cannot distinguish benign from malignant lesions, and it is particularly limited for visualization of periampullary duodenal polyps in patients with hereditary polyposis syndromes.62 If a small bowel mass is detected on capsule endoscopy, further evaluation and management are determined by the probability of the lesion being malignant (Figure 11). All patients should first undergo cross-sectional CT or magnetic resonance imaging (MRI) to assess for extraluminal disease and potential metastatic spread.52 Lesions with an intermediate to high probability of malignancy warrant deep enteroscopy or surgery for histologic diagnosis pending the results of cross-sectional imaging. Patients with small
Small Bowel Imaging Modalities Indications
Strengths
Weaknesses
Cost*
Capsule endoscopy
Obscure GI bleeding Small bowel inflammatory disease and tumors
Small bowel hemorrhage Biopsy and tattoo Foreign body retrieval Dilation and stenting Crohn’s disease Small bowel tumor Obstructive pathology
Miss rate for isolated lesions Risk of capsule retention with obstructive disease Difficult to distinguish cause of inflammatory lesions Requires deeper sedation Invasive with complications Time and staff intensive
$756
Deep enteroscopy
Direct visualization of entire small bowel High yield for mucosal lesions Detects small amounts of blood Less invasive mucosal views Provides definitive histopathology Therapeutic capabilities Entire small bowel imaged Widely available and noninvasive Provides extraluminal information Entire small bowel imaged Provides extraluminal data Noninvasive Lack of radiation exposure for younger patients Readily available Low cost Reasonable yield in ileus/obstruction Readily available Low risk of complications
Limited utility for flat lesions Radiation dose Large amount of oral contrast IV contrast: allergy/renal disease
$689
Limited utility for flat lesions Large amount of oral contrast Time and staff intensive Limited availability
$1248
Poor utility for mucosal disease and isolated lesions
$88
Limited utility for mucosal disease and isolated lesions Radiation dose Limited resolution Imprecise for bleeding site localization Time and staff intensive
$107
CTE
MRE
Crohn’s disease Small bowel polyp/tumor
Plain films
Obstruction and ileus Foreign body Free air
Small-bowel followthrough GI bleeding scan
Crohn’s disease Small bowel tumor Obstructive pathology Obscure GI bleeding
Angiography
Obscure GI bleeding
Noninvasive Good sensitivity for bleeding rates of 0.1-0.4 cm3 blood/ min Helpful for timing angiography Rapid and noninvasive Sensitive for bleeding rates of 0.5-1.0 cm3 blood/min Allows for therapeutic embolization if feasible
Less sensitive if performed during period of inactive bleeding Requires additional radiation and contrast exposure
CTE ⫽ computed tomography enterography; GI ⫽ gastrointestinal; IV ⫽ intravenous; MRE ⫽ magnetic resonance enterography. *Cost is defined as the total of technical and professional reimbursement from Medicare. †Cost for deep enteroscopy includes reimbursement for general anesthesia services from Medicare.
$1871†
$402
$521
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bowel tumors that have a low probability for malignancy are managed on the basis of the results of CT or MRI; repeat capsule endoscopy is recommended if CT or MRI shows normal results and not accompanied by high-risk clinical features suggestive of malignancy.
Intestinal Obstruction and Ileus The diagnostic imaging approach in the evaluation of small bowel obstruction depends on the clinical presentation. Acute, high-grade small bowel obstruction is well evaluated by standard CT, with reported diagnostic accuracy of more than 90%.60,63 Enteric contrast is not needed in the evaluation of high-grade small bowel obstruction because the distended, fluid-filled bowel loops provide excellent inherent contrast. CT is now considered the best imaging modality for determining which patients would benefit from conservative management versus those who require surgical intervention (Figure 12).63 Evaluation of low-grade or intermittent small bowel obstruction is a challenge for standard CT, with sensitivity reported as low as 50%.59 CTE is not yet established as having a role in evaluation of intermittent or low-grade small bowel obstruction, possibly because small bowel distension at CTE is not completely reliable. CT enteroclysis with nasojejunal tube intubation and mechanical contrast infusion is more difficult and invasive; however, it combines the advantages of controlled small bowel distension with cross-sectional CT imaging. The greater and more reliable distension of the small bowel with CT enteroclysis offer improved sensitivity and specificity (89% and 100%, respectively) in the evaluation of low-grade small bowel obstruction.60
CONCLUSIONS Although evaluation of the small bowel is still challenging, it has been dramatically enhanced by the development of capsule endoscopy, deep enteroscopy, and CTE/MRE. At present, targeted evaluations should be guided by clinical parameters (Table 1), particularly until further direction is available from prospective outcomes data incorporating cost-efficacy. Capsule endoscopy seems to be effective in patients without painful or obstructive symptoms. When a mass or obstructive type lesion is suspected, CTE/MRE and deep enteroscopy are reasonable modalities, each with unique strengths and weaknesses. When therapy is indicated, deep enteroscopy is the logical choice, whereas CTE or MRE may be chosen first when it is important to clarify potential extraluminal disease associations.
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