DOI: 10.1148/radiol.2453060798
(Radiology 2007;245:661-671.)
© RSNA, 2007
CT Enteroclysis1
Dean D. T. Maglinte, MD,
Kumaresan Sandrasegaran, MD,
John C. Lappas, MD, and
Michael Chiorean, MD
1 From the Department of Radiology (D.D.T.M., K.S., J.C.L.) and Department of Medicine, Division of Gastroenterology (M.C.), Indiana University School of Medicine, 550 N University Blvd, OU 15, Indianapolis, IN 46202-5253. Received May 7, 2006; revision requested July 6; revision received August 17; accepted September 18; final version accepted December 4; final review by D.D.T.M. June 11, 2007.
Address correspondence to D.D.T.M. (e-mail: dmaglint{at}iupui.edu).
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ABSTRACT
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Computed tomographic (CT) enteroclysis is a hybrid technique that combines the methods of fluoroscopic intubation-infusion small-bowel examinations with that of abdominal CT. The use of multidetector CT technology has made this a versatile examination that has evolved into two distinct technical modifications. CT enteroclysis can be performed by using positive enteral contrast material without intravenous contrast material and neutral enteral contrast material with intravenous contrast material. CT enteroclysis has been shown to be superior to other imaging tests such as peroral small-bowel examinations, conventional CT, and barium enteroclysis, except in the demonstration of early apthous ulcers of Crohn disease. CT enteroclysis is complementary to capsule endoscopy in the elective investigation of small-bowel disease, with a specific role in the investigation of Crohn disease, small-bowel obstruction, and unexplained gastrointestinal bleeding.
© RSNA, 2007
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INTRODUCTION
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Imaging investigations have dominated the evaluation of small-bowel disease for more than 100 years, until the advent of capsule endoscopy. Small-bowel follow-through has been the most commonly performed examination because of its simplicity, availability, and low cost. Barium enteroclysis has been shown to have overall higher accuracy and reliability at the expense of increased invasiveness and decreased patient tolerance without the use of conscious sedation (1). The disadvantage of all fluoroscopic oral small-bowel examinations is the inability to provide any extraluminal information. Computed tomography (CT) performed with oral and intravenous contrast material has a proven track record of depicting bowel wall and mesenteric abnormalities (2,3). A comparison of barium enteroclysis and abdominal CT performed in the same patients with small-bowel Crohn disease has demonstrated a much higher yield of CT in revealing mural and extraluminal manifestations of disease, including abscesses, while enteroclysis was superior for luminal abnormalities including low-grade bowel obstruction from stenosis, ulcerations, and demonstration of fistulae mainly as a result of the enteral volume challenge generated by the controlled infusion of the contrast agent (4). It was only a matter of time until CT enteroclysis was developed to overcome the individual deficiencies and to combine the advantages of both barium enteroclysis and conventional abdominal CT examinations into one technique. As reported by Kloppel et al in 1992 (5), CT enteroclysis was shown to be useful in depicting mucosal abnormalities, as well as bowel thickening, fistulae, and other extraintestinal complications of Crohn disease. In patients suspected of having small-bowel obstruction, Bender et al (6) showed that CT enteroclysis was superior to conventional CT for the diagnosis of lower grades of bowel obstruction and was also able to reveal the nature of the obstructive lesion, including adhesions.
The introduction of multidetector CT technology has allowed the evaluation of organs, such as the small intestine, that have a tortuous course. It is possible to obtain isotropic or near-isotropic resolution voxels of the abdomen and pelvis with 16-section or higher CT scanners in a reasonable breath hold. This allows the creation of coronal and sagittal reformations of similar resolution as transverse images. Modern scanners have the ability to automatically produce off-axial reformations in any desired plane, either from raw data or from isotropic resolution transverse source images. Multiplanar cross-referenced viewing of the small bowel is essential to detect sites of bowel obstruction and small-bowel masses and in planning surgical intervention (7,8).
At the same time, progress in endoscopy has been remarkable. Capsule endoscopy and double-balloon enteroscopy have allowed full exploration of the small bowel, the latter with interventional capabilities previously only available through intraoperative enteroscopy (9,10). This article examines the modifications of CT enteroclysis that have evolved since the original description more than 10 years ago and its clinical applications.
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CT ENTEROCLYSIS TECHNIQUES
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CT enteroclysis initially used positive enteral contrast material without intravenous contrast material and was mainly used to detect lower grades of small-bowel obstruction and fistulae. In the mid 1990s, water and other neutral gastrointestinal contrast agents (attenuation similar to that of water) were used for detection of gastric and small-bowel disease (11,12). These agents allowed better assessment of mucosal enhancement and mural thickness, as well as global assessment of solid organs and mesenteric vasculature. They allowed multiplanar reformations without artifacts. Thus, CT enteroclysis can be performed by using positive enteral contrast material without intravenous contrast material or neutral enteral contrast material with intravenous contrast material. With either technique, bowel preparation includes a low-residue diet, ample fluids, laxative on the day prior to the examination, and nothing by mouth on the day of the examination. As with barium enteroclysis, when a 13-F enteroclysis catheter (MEC; Cook, Bloomington, Ind) is used, patients are given the option to have conscious sedation. In our practice, most (over 90%) patients are given conscious sedation. To adequately perform CT enteroclysis, the logistics of nursing care and continuous monitoring need to be established. We charge separate Current Procedural Terminology codes for sedation, fluoroscopy, and CT examinations. In other practices, CT enteroclysis is performed without sedation or with minimal sedation such as with orally administered diazepam.
CT Enteroclysis with Neutral Enteral and Intravenous Contrast Material
Neutral contrast agents include water, methyl cellulose, and dilute 0.1% barium sulfate (Volumen; EZ-Em, Lake Success, NY) (Fig 1). The dilute barium sulfate suspension has a flavoring agent. It contains sorbitol to reduce water absorption and gum to increase viscosity. These ingredients theoretically result in better bowel distention. We prefer water as the enteral agent in enteroclysis since neither taste nor absorption of the enteral agent is an issue with this technique. The rapid pressurized infusion of enteral contrast material and the use of an antiperistaltic agent allow optimal small- and large-bowel distention. There is a slight attenuation difference between water and barium sulfate, which has an attenuation of 30–50 HU (Fig 2). Advantages of water include lower cost and reduced viscosity, which allows a smaller nasoenteral tube or faster infusion rates. In our practice, we use a standard 13-F enteroclysis catheter for all diagnostic enteroclysis. Other sizes of catheters, such as 12-F (E-Z-Em) are also available. All these agents have also been tried in the alternative technique of CT enterography where small-bowel filling is achieved with oral hyperhydration with at least 1.5 L of oral contrast material. Because of its taste and slower absorption, barium sulfate may be preferred for CT enterography. CT enterography studies have shown better detection of mucosal enhancement and bowel distention with barium sulfate than with water (13–15).
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Figure 2a: (a) Coronal reformation of CT enteroclysis image in 45-year-old patient with water as neutral enteral contrast material shows hyperenhancement of terminal ileal mucosa (arrowhead) and mural thickening. Retrograde ileoscopy with biopsy revealed mild recurrent Crohn disease. (b) Coronal reformation of CT enteroclysis image obtained with dilute 0.1% barium sulfate in 50-year-old patient with mild active Crohn disease shows similar findings. The barium sulfate has slightly higher attenuation (30–50 HU) than water (0–20 HU) and a barely visible speckled appearance, probably since it is a suspension of several ingredients, including gum, sorbitol, and barium sulfate.
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Figure 2b: (a) Coronal reformation of CT enteroclysis image in 45-year-old patient with water as neutral enteral contrast material shows hyperenhancement of terminal ileal mucosa (arrowhead) and mural thickening. Retrograde ileoscopy with biopsy revealed mild recurrent Crohn disease. (b) Coronal reformation of CT enteroclysis image obtained with dilute 0.1% barium sulfate in 50-year-old patient with mild active Crohn disease shows similar findings. The barium sulfate has slightly higher attenuation (30–50 HU) than water (0–20 HU) and a barely visible speckled appearance, probably since it is a suspension of several ingredients, including gum, sorbitol, and barium sulfate.
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The amount and rate of administration of intravenous contrast material will depend on the radiologist's individual preference. We prefer CT acquisition during the late arterial or early portal venous phase, when maximum intestinal mucosal enhancement occurs (16). The balloon tip is ideally positioned in the horizontal duodenum to the left of midline, and the balloon is inflated with 30 mL of air. We routinely inject 60 mL of air through the catheter at fluoroscopy after balloon inflation to determine that air does not reflux into the proximal duodenum and to ensure that the catheter tip is not in a diverticulum. If reflux is seen, the catheter tip is placed more distally in the duodenum and/or the balloon is further inflated. After the CT examination, we withdraw the tube into the stomach to aspirate excess fluid.
CT Enteroclysis with Positive Enteral Contrast Material
Positive enteral contrast agents include 4%–15% water-soluble contrast agent solution and dilute barium solutions (Fig 3). The concentration used is mostly based on the radiologist's preference. We prefer 12% iodinated water-soluble contrast medium to less concentrated water-soluble enteral contrast agents because of the added value of fluoroscopic observations and diagnostic quality of the radiographs obtained.
Since the infusion of enteral contrast material is performed with fluoroscopic control, the balloon and catheter tip can be positioned initially in the descending duodenum to decrease the fluoroscopic time of intubation. We have performed more than 7000 CT enteroclysis examinations in this manner, with placement of the catheter tip in the descending duodenum rather than in the proximal jejunum, and have not found reflux of enteral contrast material to be an important issue. However, if the small bowel is distended on the scout image, the catheter tip is positioned in the proximal jejunum. Because of the viscosity of the positive enteral contrast material, a 13- or a 14-F decompression catheter (MDEC; Cook) is used. Figure 4 gives the CT parameters for CT enteroclysis.
CT Enteroclysis versus CT Enterography
Intravenous contrast material–enhanced abdominopelvic CT following ingestion of a large volume of neutral oral contrast agent, typically 1.5–2 L, is termed CT enterography. CT enterography may be a suitable alternative to CT enteroclysis, where expertise for the latter is not available. A recent study (17) of 95 patients who underwent CT enterography with water as oral contrast agent demonstrated that mural attenuation and wall thickness corresponded with activity of Crohn disease measured at ileoscopy. However, distention of the small bowel at CT enterography may not be as guaranteed as that at enteroclysis. In a European series (18) on CT enterography, 20 (19%) of 106 study patients were removed from the analysis because of poor or absent small-bowel distention. A feasibility study comparing CT enteroclysis and enterography (19) looked at a small number of patients. In the study, peroral CT enterography (n = 15) was compared with nasojejunal CT enterography (n = 8), which was equated with CT enteroclysis. The nasojejunal infusion of enteral contrast material was performed with hand injection of enteral contrast material over 30 minutes. The essential enteroclysis requirement of a hydraulic pump to maintain and alter the rate of infusion was not used in this small study. No substantial differences in bowel distensibility were found in the small group of patients. Further studies are needed to determine if CT enterography can replace or complement CT enteroclysis, especially in answering questions following capsule endoscopy.
CT Enteroclysis versus MR Enteroclysis
Magnetic resonance (MR) enteroclysis has the advantage of a lack of radiation exposure and safe contrast agents but appears less accurate than CT enteroclysis. In a prospective comparison between MR enteroclysis and CT enteroclysis, the latter showed higher sensitivity and interobserver agreement for imaging signs of small-bowel disease (20). The sensitivity of CT enteroclysis for bowel wall thickening, abnormal bowel wall enhancement, and adenopathy was 89%, 79%, and 64%, respectively. For the same signs, the sensitivity of MR enteroclysis was 60%, 56%, and 14%, respectively. The interobserver agreement for these signs varied between 0.52 and 0.65 for CT enteroclysis and between 0.15 and 0.48 for MR enteroclysis.
CT Enteroclysis versus Capsule Endoscopy
The details of capsule endoscopy are beyond the scope of this review and have been discussed elsewhere (21–24). There is no doubt that capsule endoscopy affords superior mucosal evaluation compared with any imaging examination. However, disadvantages of this technique include retention of capsule, poor localization of lesion site, and equivocal evaluation in the presence of excess luminal fluid or rapid transit. Precapsule studies have been performed in patients who are at relatively high risk of capsule retention. Such patients include those with known Crohn disease, nonsteroidal anti-inflammatory drug use, small-bowel obstruction, and prior major abdominal surgery or radiation therapy. Four studies reported 20 cases of capsule retention (in 1119 patients having capsule examination), all of which followed normal small-bowel barium studies (25–28). We are not aware of published evidence of the value of CT enterography in this respect. CT enteroclysis, to our knowledge, is the only study that has been found to reliably help exclude small-bowel strictures prior to capsule study. Of 56 patients with Crohn disease who underwent CT enteroclysis, 15 were found to have strictures and did not undergo capsule endoscopy. The remaining 41 patients had undergone successful capsule endoscopy without permanent retention of the capsule (one patient had painful temporary jejunal retention of the capsule) (29). In these 41 patients, CT enteroclysis and capsule endoscopy both depicted a substantial number of terminal ileal Crohn lesions (24 with capsule endoscopy vs 21 with CT enteroclysis), unlike for jejunal lesions (25 with capsule endoscopy vs 12 with CT enteroclysis) (29).
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CLINICAL INDICATIONS
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Since the introduction of multidetector CT technology, we use CT enteroclysis with neutral enteral and intravenous contrast material as our primary method of investigation, except for detection of low-grade small-bowel obstruction or enteric leak for which CT enteroclysis with positive enteral contrast material is preferable. Positive enteral contrast material is also used if there is a contraindication to intravenous contrast material. CT enteroclysis with neutral enteral and intravenous contrast material requires less radiation (less fluoroscopy) and allows a more detailed evaluation not only of the small intestine but also of the colon and the entire abdomen (Fig 5).
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Figure 5: Coronal reformation of CT enteroclysis image obtained with water as enteral contrast agent in 59-year-old patient with diarrhea and wheezing shows 3-cm hypervascular mass (arrowhead) in ileum that proved to be a carcinoid. Intravenous contrast material with neutral enteral contrast material (water in this case) allowed global assessment of bowel wall, mesentery, and liver (hypervascular metastasis, arrow).
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Small-Bowel Obstruction
A CT examination is often performed in patients with acute abdominal symptoms, including those with small-bowel obstruction. Routine CT is very useful in diagnosing high-grade small-bowel obstruction, with quoted accuracies in excess of 90% (30,31). However, in low-grade small-bowel obstruction, conventional CT is less accurate, with sensitivity and specificity of 50% and 94%, respectively (Fig 6) (32,33). In comparison, performance of CT enteroclysis with positive enteral contrast material is better, with sensitivity and specificity of 89 and 100%, respectively (33). The preference for positive enteral contrast material is that it allows performance of fluoroscopy during infusion. Subtle delays in the passage of contrast material are thus detected. In patients with symptoms of proximal jejunal obstruction, findings of conventional CT may be negative particularly if a nasogastric tube was used to decompress the stomach or if the patient vomited prior to the scan. CT enteroclysis with the catheter tip in the descending duodenum results in a more precise diagnosis (Fig 7).
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Figure 6a: CT enteroclysis for low-grade small-bowel obstruction in 38-year-old man with recurrent abdominal pain after remote appendectomy. (a) Transverse conventional CT image shows no evidence of distended small bowel and was interpreted as unremarkable. (b) Transverse CT enteroclysis image with positive enteral contrast material obtained 3 days later shows distended proximal bowel loop with abrupt tapering (arrowhead) of caliber adjacent to anterior parietal peritoneum. Distal small bowel contains enteral contrast material (arrow) but is nondistended. Low-grade obstruction secondary to anterior enteroparietal peritoneal and enteroenteric (interloop) adhesions was diagnosed and proved at subsequent laparoscopy.
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Figure 6b: CT enteroclysis for low-grade small-bowel obstruction in 38-year-old man with recurrent abdominal pain after remote appendectomy. (a) Transverse conventional CT image shows no evidence of distended small bowel and was interpreted as unremarkable. (b) Transverse CT enteroclysis image with positive enteral contrast material obtained 3 days later shows distended proximal bowel loop with abrupt tapering (arrowhead) of caliber adjacent to anterior parietal peritoneum. Distal small bowel contains enteral contrast material (arrow) but is nondistended. Low-grade obstruction secondary to anterior enteroparietal peritoneal and enteroenteric (interloop) adhesions was diagnosed and proved at subsequent laparoscopy.
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Figure 7a: CT enteroclysis in 48-year-old patient with anemia, intermittent vomiting, and negative findings of upper gastrointestinal endoscopy and colonoscopy. (a) Transverse CT image of upper abdomen prior to capsule endoscopy. The patient vomited barium sulfate and could only tolerate two cups of water (400 mL) slowly. Except for an enlarged spleen, findings of the examination were interpreted as unremarkable for obstruction or mass. CT enteroclysis was performed to localize and characterize cause of lesion after capsule was retained. (b) Fluoroscopic radiograph at initial infusion of positive enteral contrast material shows the capsule (arrowhead) obstructed by an infiltrating mass (arrow) in proximal jejunum. (c) Transverse CT enteroclysis image shows proximal jejunal mass (arrow) and adjacent soft-tissue mass (arrowhead) that was suspected to be an enlarged node. Surgical findings revealed adenocarcinoma of proximal jejunum and non-Hodgkin lymphoma in mesenteric nodes.
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Figure 7b: CT enteroclysis in 48-year-old patient with anemia, intermittent vomiting, and negative findings of upper gastrointestinal endoscopy and colonoscopy. (a) Transverse CT image of upper abdomen prior to capsule endoscopy. The patient vomited barium sulfate and could only tolerate two cups of water (400 mL) slowly. Except for an enlarged spleen, findings of the examination were interpreted as unremarkable for obstruction or mass. CT enteroclysis was performed to localize and characterize cause of lesion after capsule was retained. (b) Fluoroscopic radiograph at initial infusion of positive enteral contrast material shows the capsule (arrowhead) obstructed by an infiltrating mass (arrow) in proximal jejunum. (c) Transverse CT enteroclysis image shows proximal jejunal mass (arrow) and adjacent soft-tissue mass (arrowhead) that was suspected to be an enlarged node. Surgical findings revealed adenocarcinoma of proximal jejunum and non-Hodgkin lymphoma in mesenteric nodes.
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Figure 7c: CT enteroclysis in 48-year-old patient with anemia, intermittent vomiting, and negative findings of upper gastrointestinal endoscopy and colonoscopy. (a) Transverse CT image of upper abdomen prior to capsule endoscopy. The patient vomited barium sulfate and could only tolerate two cups of water (400 mL) slowly. Except for an enlarged spleen, findings of the examination were interpreted as unremarkable for obstruction or mass. CT enteroclysis was performed to localize and characterize cause of lesion after capsule was retained. (b) Fluoroscopic radiograph at initial infusion of positive enteral contrast material shows the capsule (arrowhead) obstructed by an infiltrating mass (arrow) in proximal jejunum. (c) Transverse CT enteroclysis image shows proximal jejunal mass (arrow) and adjacent soft-tissue mass (arrowhead) that was suspected to be an enlarged node. Surgical findings revealed adenocarcinoma of proximal jejunum and non-Hodgkin lymphoma in mesenteric nodes.
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Adhesions account for 60%–80% of small-bowel obstructions and are classified as parietal or visceral. The former extend from the bowel to the peritoneal surface, usually to anterior parietal peritoneum. The latter extend from the small bowel to other small-bowel loops (interloop) or to adjacent organs such as the colon and uterus. This distinction is useful. Dense anterior parietal adhesions increase the risk of bowel injury during laparoscopy and may require alternative trocar insertion techniques (34,35). It is generally thought that parietal adhesions cause abdominal pain and interloop adhesions are associated with bowel obstruction (36). CT enteroclysis depicts adhesions even in the absence of small-bowel obstruction (37). Findings that indicate the presence of adhesions include deformity and fixation of the small bowel to the peritoneal lining, with obliteration of the fat plane, kinking, or sharp angulation of bowel loops and asymmetric wall thickening (Fig 8). Unlike in adhesive obstruction, nonobstructive adhesions do not show an abrupt transition point. Nonobstructive adhesions are known to cause chronic abdominal pain in postoperative patients. There is debate in the surgical literature whether adhesiolysis is justified in the absence of bowel obstruction.
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Figure 8a: CT enteroclysis with positive enteral contrast material demonstrates adhesions. (a) Parietal adhesions. Transverse image in 50-year-old patient with anemia and recurrent abdominal pain who was allergic to iodinated contrast material shows flattening (black arrowheads) of the anterior wall of small bowel and loss of fat plane between the posterior wall of rectus sheath and bowel wall. Anterior parietal peritoneum was thickened (arrow). Appearances suggested nonobstructing anterior enteroparietal peritoneal adhesions. Note presence of fat plane and normal convexity (white arrowhead) of small bowel on left side. (b) Visceral adhesions. Transverse image in 35-year-old patient with recurrent abdominal pain and vomiting with unremarkable prior CT examination findings shows dilated loops of small bowel in left hemiabdomen. On the right side, small-bowel loop showed variable caliber (arrow), sharp angulations (white arrowhead), and asymmetric wall thickening (black arrowhead) suggestive of enteroenteric (interloop) adhesions, which were confirmed at surgery.
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Figure 8b: CT enteroclysis with positive enteral contrast material demonstrates adhesions. (a) Parietal adhesions. Transverse image in 50-year-old patient with anemia and recurrent abdominal pain who was allergic to iodinated contrast material shows flattening (black arrowheads) of the anterior wall of small bowel and loss of fat plane between the posterior wall of rectus sheath and bowel wall. Anterior parietal peritoneum was thickened (arrow). Appearances suggested nonobstructing anterior enteroparietal peritoneal adhesions. Note presence of fat plane and normal convexity (white arrowhead) of small bowel on left side. (b) Visceral adhesions. Transverse image in 35-year-old patient with recurrent abdominal pain and vomiting with unremarkable prior CT examination findings shows dilated loops of small bowel in left hemiabdomen. On the right side, small-bowel loop showed variable caliber (arrow), sharp angulations (white arrowhead), and asymmetric wall thickening (black arrowhead) suggestive of enteroenteric (interloop) adhesions, which were confirmed at surgery.
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There is a subset of patients with small-bowel obstruction in whom conservative treatment is preferred (38). This subset includes patients with early (< 7 days) postoperative obstruction, Crohn disease, or carcinomatosis and patients with a history of radiation therapy or multiple surgeries without clinical or biochemical evidence for strangulation. CT enteroclysis techniques in these patients allow the radiologist to undertake a therapeutic, as well as diagnostic, role. A 14-F multipurpose decompression/enteroclysis catheter (MDEC; Cook) inserted into the proximal jejunum is used to decompress small bowel over several hours, usually overnight. Such a tube is preferable to a nasogastric tube, which usually only decompresses the stomach and cannot be used for CT enteroclysis. The effectiveness of decompression is improved if the decompression tube tip is closer to the point of obstruction. Once decompressed, the severity of bowel obstruction could be discerned by infusion of iodinated enteral contrast material at a slower rate. The infusion is stopped if the patient complains of abdominal pain or if there is back flow of contrast material into the duodenum. Delayed acquisition of the CT images may be required in some instances. If a CT examination performed 3 hours later shows that the enteral contrast material has passed beyond the site of obstruction, treatment remains as conservative bowel decompression, and in most cases the obstruction resolves without surgery (38). On the other hand, if no enteral contrast material is seen in the colon at a second CT examination performed 12 hours after infusion, the obstruction is deemed high grade or possibly complete and surgery is indicated. If there is clinical or CT evidence of closed loop obstruction or strangulation, immediate surgery is indicated. In patients with altered gastroduodenal anatomy, such as with the Whipple procedure, the catheter tip is positioned in the gastric remnant, with the balloon retracted to occlude the gastroesophageal junction to prevent esophageal reflux. This positioning allows assessment of the gastric outlet, the biliopancreatic limb, and the efferent loop of jejunum (39).
Crohn Disease
In patients suspected of having (and previously undiagnosed) Crohn disease, capsule endoscopy has a low retention rate of 1%–2% (40) and higher diagnostic yield than small-bowel barium study, conventional CT, CT enteroclysis, or CT enterography (29,41–44). After negative colonoscopy and ileoscopy findings, capsule endoscopy is considered to be the first-line examination in the investigation of suspected nonstricturing Crohn disease (21,45). Imaging tests are performed if capsule use is contraindicated or findings are equivocal. CT enteroclysis is accurate in depicting mucosal abnormalities, bowel thickening, fistulae, and extraintestinal manifestations (Figs 2, 9). In established Crohn disease, the capsule has a retention rate of up to 8% (40). In patients presenting with complications that include bowel obstruction, refractoriness to medical therapy, and fistulous disease, imaging tests are usually considered first. Bowel obstruction may be caused by fibrostenotic Crohn disease or by active inflammation. If there is a history of abdominal surgery, adhesions are also a possible cause. Differentiation is important since therapy differs for these causes. The luminal stenosis caused by active inflammation responds well to anti-inflammatory agents, including tumor necrosis factor inhibitors, such as infliximab (Remicade; Centocor, Horsham, Pa). However, infliximab is contraindicated in fibrostenotic obstruction (46). The distinction may be made by using CT enteroclysis with neutral enteral and intravenous contrast material (Fig 10) (17,41). Although the diagnosis of fistulae can be made with neutral enteral contrast media, especially with dilute barium sulfate, the demonstration of small enteral fistulae is best made with positive enteral contrast material (Fig 11).
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Figure 9: Transverse CT enteroclysis image in 51-year-old man with worsening symptoms shows thickened small bowel with mucosal and mural hyperenhancement (black arrow) adherent to thickened lateral peritoneal lining (black arrowheads). There is a small gas-containing abscess (white arrowhead) posteriorly and fistulous communication along thickened peritoneum to a larger abscess (white arrow) anteriorly. There is also evidence of moderate inflammatory activity indicated by mucosal enhancement and comb sign (dashed arrow) of mesenteric vessels.
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Figure 10a: Active inflammatory stenotic and fibrostenotic subtypes of Crohn disease. (a) Coronal reformation of CT enteroclysis image obtained with neutral enteral contrast material in 59-year-old woman shows mucosal hyperenhancement (black arrow), thickened wall (*), luminal narrowing of terminal ileum, and prominent vasa recta (black arrowhead), the comb sign. Proximal small bowel is distended (white arrow). Appearances indicated active inflammatory subtype of Crohn disease with secondary obstruction. Note mild, irregular bile duct dilatation (white arrowheads) indicating associated sclerosing cholangitis. Patient was treated with immunomodulatory therapy. (b) Coronal reformation of CT enteroclysis image in 49-year-old woman with Crohn disease with chronic abdominal pain and vomiting shows stricture (arrowhead) of terminal ileum. The mildly thickened wall did not markedly enhance and there was no engorgement of vasa recta. Mild mucosal hyperenhancement may be seen in patients with fibrostenosis. Colonoscopic dilation was performed. Biopsies did not show active inflammation.
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Figure 10b: Active inflammatory stenotic and fibrostenotic subtypes of Crohn disease. (a) Coronal reformation of CT enteroclysis image obtained with neutral enteral contrast material in 59-year-old woman shows mucosal hyperenhancement (black arrow), thickened wall (*), luminal narrowing of terminal ileum, and prominent vasa recta (black arrowhead), the comb sign. Proximal small bowel is distended (white arrow). Appearances indicated active inflammatory subtype of Crohn disease with secondary obstruction. Note mild, irregular bile duct dilatation (white arrowheads) indicating associated sclerosing cholangitis. Patient was treated with immunomodulatory therapy. (b) Coronal reformation of CT enteroclysis image in 49-year-old woman with Crohn disease with chronic abdominal pain and vomiting shows stricture (arrowhead) of terminal ileum. The mildly thickened wall did not markedly enhance and there was no engorgement of vasa recta. Mild mucosal hyperenhancement may be seen in patients with fibrostenosis. Colonoscopic dilation was performed. Biopsies did not show active inflammation.
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Figure 11: Sagittal reformation of CT enteroclysis image obtained with positive enteral contrast material in 34-year-old woman with known Crohn disease with pneumaturia and pelvic pain shows stenosed loop (black arrowhead) of ileum adherent to the dome of urinary bladder with enteral contrast material (black arrow) in urinary bladder indicating ileovesical fistula. Another fistulous tract was seen (dashed arrow) entering the sigmoid colon (white arrow).
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Small-Bowel Neoplasms
Reports have confirmed the effectiveness of CT enteroclysis in the diagnosis of small-bowel neoplasms (47,48). Because of its ability to characterize the small-bowel wall, its mesentery, and the liver, CT enteroclysis with neutral enteral and intravenous contrast material is the preferred technique when the patient has no evidence of small-bowel obstruction (Fig 2). More accurate determination of primary or metastatic lesions involving the small bowel is possible with CT enteroclysis compared with conventional (nonenteroclysis) CT (Fig 12) (33,49,50).
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Figure 12a: Small-bowel metastases in 80-year-old man with history of colon cancer and symptoms of small-bowel obstruction. (a) Transverse conventional CT image with oral and intravenous contrast material shows distended small-bowel loops (arrow), but no bowel mass is seen. (b) Transverse CT enteroclysis image with positive contrast material obtained 2 weeks later shows multiple masses (arrowheads) in small-bowel wall consistent with serosal metastases and distended small-bowel loop (arrow). Metastases were proved to be cause of bowel obstruction at surgery.
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Figure 12b: Small-bowel metastases in 80-year-old man with history of colon cancer and symptoms of small-bowel obstruction. (a) Transverse conventional CT image with oral and intravenous contrast material shows distended small-bowel loops (arrow), but no bowel mass is seen. (b) Transverse CT enteroclysis image with positive contrast material obtained 2 weeks later shows multiple masses (arrowheads) in small-bowel wall consistent with serosal metastases and distended small-bowel loop (arrow). Metastases were proved to be cause of bowel obstruction at surgery.
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The first-line examination of small-bowel tumors depends on the presentation. If the presentation is with obscure gastrointestinal bleeding, capsule endoscopy is likely to be performed (see below). However, if the indication is pain or small-bowel obstruction, CT will usually be the first-line examination. Although the accuracy of multidetector CT with neutral oral and intravenous contrast material has improved (51), the detection of small nonobstructive primary tumors requires optimal bowel distention that is achievable with CT enteroclysis (Fig 2). CT enteroclysis has a complementary role to capsule endoscopy and push enteroscopy in screening for small polyps in familial polyposis and Peutz-Jeghers syndromes (Fig 13).
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Figure 13a: CT enteroclysis in hereditary polyposis. (a) Image in 53-year-old patient with history of Peutz-Jeghers syndrome referred for evaluation of small-bowel polyps. Transverse CT enteroclysis image with neutral enteral and intravenous contrast material shows small intraluminal polyps (arrowheads) in jejunum. (b) Coronal reformation shows small polyps (arrowheads) in anterior loops. Hamartomatous polyps were removed at double balloon enteroscopy.
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Figure 13b: CT enteroclysis in hereditary polyposis. (a) Image in 53-year-old patient with history of Peutz-Jeghers syndrome referred for evaluation of small-bowel polyps. Transverse CT enteroclysis image with neutral enteral and intravenous contrast material shows small intraluminal polyps (arrowheads) in jejunum. (b) Coronal reformation shows small polyps (arrowheads) in anterior loops. Hamartomatous polyps were removed at double balloon enteroscopy.
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Obscure Gastrointestinal Bleeding
No identifiable cause for gastrointestinal blood loss is found in 30%–50% of patients after standard endoscopy and conventional radiologic studies. Radiologic tests such as small-bowel follow-through and barium enteroclysis with methylcellulose have poor sensitivities of less than 5% and 10%–20%, respectively, in this situation (52–55). Vascular malformations such as angioectasia are seen in 50%–70% of patients with obscure gastrointestinal bleeding, substantially higher than possible with routine imaging studies. Comparative studies reported in the gastroenterology endoscopic literature have shown that capsule endoscopy is the test with the highest yield in assessing a small-bowel source of bleeding and is superior to small-bowel barium studies, conventional CT, and CT enterography (56–58). We are not aware of literature in which CT enteroclysis was directly compared with capsule endoscopy in obscure gastrointestinal bleeding. In our experience, CT enteroclysis may be of use in identifying the cause of obscure gastrointestinal bleeding if findings of capsule studies are equivocal or negative (Fig 14). CT enteroclysis may help identify submucosal tumors or Meckel diverticulitis. We believe that CT enteroclysis (or CT enterography) has a second-line role in the investigation of the probable source of bleeding from the small bowel.
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Figure 14: CT enteroclysis image with neutral enteral contrast material in 63-year-old woman with unexplained gastrointestinal bleeding shows 3-cm hypervascular submucosal mass (arrow) arising from mid small bowel, which was proved at surgery to be gastrointestinal stromal tumor. Capsule endoscopy revealed jejunal angioectasia (not shown) but no mass.
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Miscellaneous Application
CT enteroclysis has been of value in resolving the false-positive and false-negative interpretations from nonenteral volume-challenged small-bowel studies that arise from the difficulties associated with poor distention or peristalsis, simulating wall thickening (59).
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DISADVANTAGES OF CT ENTEROCLYSIS
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The discomfort associated with nasoenteric tube placement may be alleviated with the use of conscious sedation and smaller tubes (60). Conscious sedation requires dedicated personnel and makes the procedure longer and more expensive. In smaller institutions, this may not be practical. The logistics of performing CT when the fluoroscopic suite is far from the CT area is a deterrent. The use of CT units with fluoroscopic capabilities may help circumvent this issue when neutral enteral contrast material is used for enteroclysis. Although CT enteroclysis requires additional radiologist time for catheter placement, the time for interpretation of this examination is less than that required for other complex CT studies, such as renal donor imaging or CT colonography.
The addition of CT to enteroclysis increases the cost of the procedure, and exposure of patients and staff to radiation remains an important issue even if newer multidetector CT technology has improved dose efficiency (61). The invasiveness of the procedure raises concern for complications such as bowel perforation, enteral contrast material aspiration, or respiratory depression from sedation. In some cases, the procedure cannot be performed because of inability to place the enteroclysis tube in an adequate position. However, in our experience, such events are rare.
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CONCLUSION
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CT enteroclysis combines the advantages of CT and barium enteroclysis. Although it has disadvantages, experience has shown its value in the investigation of small-bowel diseases. The use of multidetector technology and two-dimensional reformatting has improved sensitivity of detection and confidence in diagnosing small-bowel lesions.
Capsule endoscopy gives unparalleled depiction of the mucosal surface of the small bowel. Imaging tests of the small bowel should evolve to answer questions that capsule endoscopy cannot answer satisfactorily. In this respect, CT enteroclysis is generally superior to conventional CT and small-bowel follow-through. The role of CT enterography versus CT enteroclysis needs to be clarified with future studies.
We believe CT enteroclysis is complementary to capsule endoscopy in the investigation of unexplained gastrointestinal bleeding and the diagnosis of small-bowel tumors. It has specific roles in the staging of established small-bowel Crohn disease. CT enteroclysis techniques could be used not only to diagnose low-grade small-bowel obstruction but also as a therapeutic option in selected cases with small-bowel obstruction.
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ESSENTIALS
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- CT enteroclysis overcomes the individual deficiencies of barium enteroclysis and abdominal CT.
- CT enteroclysis can be performed by using positive enteral contrast material without intravenous contrast material or neutral enteral contrast material (attenuation similar to that of water) with intravenous contrast material.
- CT enteroclysis with neutral enteral and intravenous contrast material is our primary method of investigation except for detection of low-grade small-bowel obstruction or enteric leak, for which CT enteroclysis with positive enteral contrast material is preferable.
- We prefer water as the neutral enteral agent in enteroclysis over methylcellulose and dilute bar-ium (0.1%).
- Imaging tests of the small bowel should evolve to answer questions that capsule endoscopy cannot answer satisfactorily; in this respect, CT enteroclysis is generally superior to conventional CT and small-bowel follow-through.
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FOOTNOTES
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D.D.T.M. is a consultant to EZ-Em (Lake Success, NY) and Cook (Bloomington, Ind).
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ABSTRACT
INTRODUCTION
