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Published online before print November 14, 2003, 10.1148/radiol.2301021535
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(Radiology 2004;230:260-265.)
© RSNA, 2004


Gastrointestinal Imaging

Small Bowel: Preliminary Comparison of Capsule Endoscopy with Barium Study and CT1

Amy K. Hara, MD, Jonathan A. Leighton, MD, Virender K. Sharma, MD and David E. Fleischer, MD

1 From the Mayo Clinic, 13400 E Shea Blvd, Scottsdale, AZ 85259. From the 2002 RSNA scientific assembly. Received November 21, 2002; revision requested January 22, 2003; final revision received June 19; accepted August 6. Address correspondence to A.K.H. (e-mail: hara.amy@mayo.edu).


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To retrospectively compare capsule endoscopic (CE) findings with findings at barium studies or computed tomography (CT) in patients without evidence of small-bowel stricture at barium examination.

MATERIALS AND METHODS: Fifty-two patients underwent CE, and the majority (43 of 52) did so for obscure gastrointestinal bleeding. Forty-two (81%) of 52 patients underwent 36 small-bowel follow-through examinations; four, enteroclysis; and 19, contrast material–enhanced CT of the abdomen and pelvis within 6 months of CE (either before or after CE). Imaging results were retrospectively reviewed and compared with CE, standard endoscopic, and surgical results. Findings of any examinations between CE and imaging that were discrepant were retrospectively reviewed by a radiologist not blinded to CE results. Proportion of positive findings at CE was compared with proportion of positive findings at barium studies and CT in the same patients. Statistical significance was calculated with McNemar {chi}2 statistic.

RESULTS: Barium examination findings were positive in one (3%) of 40 patients; CE findings were positive in 22 (55%) (P < .001). CT demonstrated small-bowel findings in four (21%) of 19 patients, but CE demonstrated findings in 12 (63%) of 19 patients (P = .02). The most common CE finding, angioectasia (n = 11), was not detected at any imaging study. More ulcers (n = 8) were detected with CE than with barium study (one of eight) and CT (three of six). At CE, three of five surgically confirmed masses (carcinoid, intussusception, lymphangioma) were identified, but two jejunal tumors were not detected in a patient with poor bowel preparation. At barium study, no masses (zero of five) were detected; at CT, one of four masses was detected.

CONCLUSION: In patients without a small-bowel stricture at barium study, more small-bowel disease was found at CE when findings were retrospectively compared with barium examination and CT findings.

© RSNA, 2003

Index terms: Intestines, CT, 74.12112 • Intestines, endoscopy, 74.1279 • Intestines, radiography, 74.1271


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Fluoroscopic small-bowel imaging is challenging because of the complex and lengthy small-bowel anatomy. Until recently, the small bowel was the only part of the alimentary tract not completely accessible with endoscopy, and only indirect evaluation was possible by using small-bowel follow-through (SBFT) barium examination or enteroclysis. Both of these radiologic techniques, however, are suboptimal: Varying examination techniques hamper the SBFT examination (1,2), and patient discomfort and high radiation dose limit enteroclysis (3,4).

For the first time, direct visualization of the entire small bowel is possible with wireless capsule endoscopy (CE), a new Food and Drug Administration–approved technology. Patients ingest a small capsule that is propelled by peristalsis through the small bowel and transmits endoluminal images to an external recorder. The images are subsequently downloaded from the recorder to a dedicated computer workstation and evaluated by a gastroenterologist. Early reports are very promising for this technique, which has the ability to aid in the detection of cases of angioectasia, tumors, ulcers, and inflammatory changes (59).

The purpose of this study was to retrospectively compare CE findings with findings at any barium or computed tomographic (CT) study in patients who had no evidence of a small-bowel stricture at barium examination.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Clinical Data
Between September 2001 and April 2002, 52 patients underwent CE for the following indications: obscure gastrointestinal bleeding (ie, bleeding of unknown origin that persisted or recurred after endoscopic examination, including colonoscopy and/or upper endoscopy, with negative findings [n = 43]), inflammatory bowel disease (n = 8), or chronic abdominal pain (n = 1). The patients included 31 men (mean age, 64 years; age range, 21–92 years) and 21 women (mean age, 63 years; age range, 28–82 years). Only those patients without a history of small-bowel stricture or with a barium study negative for a stricture underwent CE.

A clinical note database was used to retrospectively identify those patients who underwent barium study and/or CT within 6 months of CE (either before or after CE). Imaging results both within and outside of our institution were included. When available, imaging tests and CE results were also compared with endoscopic, surgical, and biopsy results. For patients with discrepant CE and imaging results (ie, a positive CE finding but a negative barium examination or CT finding), any available findings from imaging tests were reviewed to determine whether the CE findings could be identified in retrospect. If the imaging and CE findings matched (ie, both demonstrated a jejunal mass), the images were not reviewed. All second reviews were performed by a board-certified radiologist (A.K.H.) with 7 years of experience with CT and barium studies who was not blinded to the CE results. All primary imaging studies from our institution were conducted by board-certified radiologists with 7–25 years of experience. Approval for this retrospective review was given by the Mayo Foundation Institutional Review Board, and informed consent was waived.

The number of patients and the types of examinations included in this study are summarized in Table 1. Forty-two (81%) of 52 patients who fit the study criteria underwent 36 SBFT, four enteroclysis, and 19 CT examinations. No patients underwent both SBFT and enteroclysis examinations, and each patient underwent only one CT examination. Only four SBFT and two CT examinations were performed more than 3 months from CE (either before or after CE). Most patients (33 [79%] of 42) underwent examinations at our institution. The remaining nine patients underwent 10 examinations at outside institutions.


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TABLE 1. Summary of Patient Examinations

 
Small-Bowel Examination
All small-bowel examinations except one performed at our institution were single-contrast barium examinations, with 50% wt/vol barium sulfate suspension (Entrobar; Lafayette Pharmaceuticals, Lafayette, Ind). Intermittent fluoroscopic evaluation was performed at 30-minute intervals until the terminal ileum was visualized. Patients received 400–600 mL of barium. All fluoroscopy was performed by a radiologist, and all images were digital. Overhead images were not obtained routinely. One enteroclysis examination was performed by using a combined single- and double-contrast technique. Five hundred milliliters of barium as 50% wt/vol barium sulfate suspension and 2,000 mL of methylcellulose (Entrocel; Lafayette Pharmaceuticals), which was composed of 500 mL of concentrated methylcellulose and 1,500 mL of water, were used.

CT Technique
All CT examinations performed at our institution (n = 16) were performed with a multi–detector row CT scanner (Somaton Plus 4 Volume Zoom; Siemens, Erlangen, Germany). All examinations were performed with contrast material (Omnipaque; Nycomed, Princeton, NJ), 300 mg administered intravenously at 0.45 mL per kilogram of body weight. The majority of scans (12 of 16) were obtained with our routine protocol at 5-mm section thickness, with scanning beginning at 70 seconds at 2–4 mL/sec. Four scans were obtained by using a specialized small-bowel protocol with a 3-mm section thickness, 1.5-mm reconstructions, and 2,000 mL of water as the oral contrast agent. Scanning began at 40 seconds (to optimize mucosal enhancement). Oral contrast agents were administered as follows: Nine patients received 30 oz (890 mL) of a 2.2% wt/vol barium sulfate suspension (Medescan; Lafayette Pharmaceuticals), and three received 30 oz (890 mL) of water. All examinations were performed from the diaphragm to the symphysis pubis. In no examination at our institution were motion artifacts present, and in 12 of 16 examinations, 50%–75% small-bowel opacification was achieved with oral contrast material. On three scans, 25%–50% opacification was achieved; and on one, less than 25% opacification was achieved.

CE Technique
The Food and Drug Administration–approved diagnostic imaging capsule (M2A Diagnostic Imaging System; Given, Yoqneam, Israel) was used for small–bowel imaging. Patients fasted 8 hours prior to the examination and ingested a 2.6 x 1.1-cm capsule that contained a miniature video camera, a light source, batteries, and a radio transmitter. The capsule was propelled by peristalsis through the small bowel, and video images were recorded for 8 hours. By using leads (Sensor Arrays; Given Imaging) taped to the body, images were transmitted from the capsule by means of radio telemetry to a portable recorder (Given data recorder; Given Imaging), which the patient wore on a belt. The capsule was eventually expelled and discarded. The images were subsequently downloaded from the recorder to a dedicated computer workstation (Rapid Workstation; Given Imaging) and evaluated by one of three gastroenterologists (J.A.L., V.K.S., D.E.F.) with 10–15 years of endoscopic experience. The gastroenterologists evaluated all the endoscopic images obtained with the capsule in a sequential video format. The locations of the small-bowel abnormalities were determined by estimating their relationship to anatomic landmarks (eg, pylorus, ileocecal valve) and the time at which they were depicted.

Statistical Analysis
The proportion of positive findings at CE was compared with the proportion of positive findings at barium study and CT. The comparisons were limited to only those patients who underwent imaging with both methods. For example, when CE and barium examination were compared, the patients who underwent CE were exactly the same as those who underwent barium examination. The statistical significance was calculated with the McNemar {chi}2 statistic. A difference with a P value of less than .05 was considered significant.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
CE results are summarized in Tables 25. CE depicted 11 cases of angioectasia (Fig 1), eight ulcers, and three masses. Barium examination results are summarized in Tables 2 and 3. Forty (95%) of 42 patients underwent a small-bowel barium examination. Findings were positive in only one (3%) of 40 barium studies (Fig 2); by comparison, they were positive in 19 (48%) of 40 CE examinations (P < .001). Four patients had more than one finding at CE. The single positive finding at SBFT examination was ulceration of the terminal ileum, which was also identified at CE. The same patient who underwent this SBFT examination also had an enterocolic fistula, which was not identified at CE. Four patients underwent enteroclysis, and findings for all were negative. CE in these four patients demonstrated two cases of angioectasia and one ulcer.


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TABLE 2. CE versus Barium Study: Results per Patient in 40 Patients

 

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TABLE 3. CE versus Barium Examination: Comparison of Findings in 40 Patients

 

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TABLE 4. CE versus CT: Results per Patient in 19 Patients

 

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TABLE 5. CE versus CT: Comparison of Findings in 19 Patients

 


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Figure 1. CE Image in 72-year-old woman with obscure gastrointestinal bleeding. Ileal angioectasia (arrow) was demonstrated at CE but not depicted at SBFT examination or CT. Patient underwent ileal resection and has had no recurrent symptoms.

 


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Figure 2a. Images in 28-year-old woman suspected of having recurrent Crohn disease. Crohn disease was detected at CE, SBFT examination, and CT. (a) CE image shows one of multiple small ulcers (circle) in the terminal ileum. (b) Transverse CT scan shows thickening and enhancement (arrows) of the terminal ileum. (c) SBFT image reveals featureless terminal ileum with "rose-thorn" ulcerations (arrows).

 


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Figure 2b. Images in 28-year-old woman suspected of having recurrent Crohn disease. Crohn disease was detected at CE, SBFT examination, and CT. (a) CE image shows one of multiple small ulcers (circle) in the terminal ileum. (b) Transverse CT scan shows thickening and enhancement (arrows) of the terminal ileum. (c) SBFT image reveals featureless terminal ileum with "rose-thorn" ulcerations (arrows).

 


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Figure 2c. Images in 28-year-old woman suspected of having recurrent Crohn disease. Crohn disease was detected at CE, SBFT examination, and CT. (a) CE image shows one of multiple small ulcers (circle) in the terminal ileum. (b) Transverse CT scan shows thickening and enhancement (arrows) of the terminal ileum. (c) SBFT image reveals featureless terminal ileum with "rose-thorn" ulcerations (arrows).

 
CT results are summarized in Tables 4 and 5. Nineteen (45%) of 42 patients underwent abdominopelvic CT. CT demonstrated small-bowel findings in four (21%) of 19 patients, and CE demonstrated them in 12 (63%) of 19 patients (P = .02). CE showed 14 findings in 12 patients, whereas CT showed five findings in four patients. Findings at CT were positive and those at CE were negative in one patient with a small-bowel mass (Fig 3). Three patients with inflammatory small-bowel disease were correctly identified at CT and CE by using the specialized small-bowel imaging protocol. CT findings in these patients included thickening and arterial enhancement of the terminal ileum (Fig 1), perianal and coloenteric fistulas, mild diffuse colitis, and mesenteric lymphadenopathy.



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Figure 3. Coronal CT scan in 75-year-old man with obscure gastrointestinal bleeding shows stromal tumor (arrow). This tumor was not detected at CE because of retained food.

 
Four patients had a total of five surgically confirmed small-bowel masses (Table 6). Three masses were identified at CE, and these included a 1.7-cm ileal carcinoid tumor (Fig 4), an intussuscepted small-bowel loop without an associated lesion, and a 1.5-cm lymphangioma. All three patients had negative findings at SBFT examination, and two of three patients had CT findings that were also negative. One patient with a nondiagnostic CE examination because of retained food had two small-bowel masses that were identified at surgery as a gastrointestinal stromal tumor and a carcinoid tumor. One of the masses was detected at CT; neither was detected at SBFT examination. The mass identified at CT had previously been identified by using angiography and was known by the dictating radiologist.


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TABLE 6. Summary of Small-Bowel Masses

 


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Figure 4. CE image in 69-year-old man with obscure gastrointestinal bleeding shows carcinoid tumor (arrows). Tumor was not detected at SBFT examination or CT.

 
CE helped to identify eight patients with ulcers (Fig 1). In two of these patients, ulcers were confirmed at surgery (n = 1) or colonoscopy (n = 1). Four other patients had a history of inflammatory bowel disease, and in three of these patients recent colonic inflammatory bowel disease was demonstrated at colonoscopy. The remaining two patients did not undergo further work-up. All eight patients with ulcers underwent a barium examination (seven SBFT, one enteroclysis); in only one of the SBFT examinations were findings positive. Six of eight patients with ulcers underwent CT; findings from three of six CT examinations were positive. One patient with an incomplete CE examination in which the colon was not visualized had an anastomotic ulcer that was identified at colonoscopy.

False-negative CE findings included two small-bowel masses that were confirmed surgically; an ulcer confirmed with biopsy; and a coloenteric fistula detected at SBFT examination, CT, and double-contrast barium enema study. Other bowel-associated findings identified at CT included severe superior mesenteric artery stenosis, mesenteric lymphadenopathy, and diffuse mild colitis secondary to inflammatory bowel disease that was confirmed at colonoscopy.

All false-negative findings from imaging examinations performed at our institution were reviewed (A.K.H.), and none of the CE findings could be identified retrospectively.


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Until the introduction of CE, imaging studies offered the only complete small-bowel examination. The most common radiologic imaging test of the small bowel is the barium SBFT examination because of its relative ease of administration and less patient discomfort compared with enteroclysis. The accuracy of the SBFT examination, however, varies widely among radiologists and institutions, depending on technique. In some studies, researchers have demonstrated that by using a careful SBFT examination, with frequent fluoroscopy and compression radiography, performance is as good as that of enteroclysis (4,10). When the SBFT examination includes mainly overhead radiographs and infrequent fluoroscopy, however, the performance is poor (1,2).

Barium examinations, most consisting of careful SBFT examinations, showed poor performance in this study and demonstrated disease in only one patient compared with results at CE, which helped to find disease in 19 patients. Barium examinations compared poorly with CE for many reasons. First, in 10 of 19 patients, cases of angioectasia were detected at CE but were not detectable at barium examination. In addition, enteroclysis was rarely performed in these patients, although it is often the recommended examination when small-bowel bleeding is suspected (11,12). While it is possible that more findings would have been discovered with this technique, CE still demonstrated an ulcer in patients with negative findings at enteroclysis. A suboptimal technique may also have contributed to the poor performance. For example, the double-contrast upper gastrointestinal and SBFT examinations were often performed sequentially for patient convenience, although this is not recommended since the more opaque contrast medium used for an upper gastrointestinal examination can compromise the SBFT examination (13). In addition, up to eight SBFT examinations may be performed simultaneously by one radiologist, and this workload invariably leads to lengthy intervals between fluoroscopic examinations. Finally, CE was not performed in patients with a stricture found at SBFT examination, thus biasing the study against patients with advanced small-bowel disease. If these patients with more severe small-bowel disease were included, it is likely that more findings would have been demonstrated with the SBFT examination.

CT performed better than barium examination for detection of small-bowel disease, although fewer ulcers and masses were detected than at CE. CT is being used more frequently for small-bowel evaluation, particularly in advanced Crohn disease and for evaluation of small-bowel obstruction (1416). In this study, a specialized CT protocol for the small bowel (with 3-mm section thickness and water as the oral contrast agent) successfully helped to identify more Crohn disease (n = 3) in the terminal ileum compared with that identified at SBFT examination (n = 1). Detection of intraluminal small-bowel masses by using a conventional CT protocol was less successful, however, with only one of the four surgically proved masses detected. Although detection of small-bowel masses may be improved with a dedicated CT protocol for the small bowel, nonuniform small-bowel distention due to peristaltic contractions or collapsed loops makes detection of intraluminal lesions difficult. The advantage of CT includes evaluation of disease outside the small bowel, which can complement intraluminal CE findings. In this study, CT depicted several extraenteric abnormalities, which included a perianal fistula, coloenteric fistula, mesenteric lymphadenopathy, severe superior mesenteric artery stenosis, and diffuse mild colitis from inflammatory bowel disease.

CE, while demonstrating many findings not seen with imaging, is not a perfect technique. In this study, two jejunal tumors and a coloenteric fistula were not depicted by using CE. Lesion localization and evaluation can be difficult with CE, with no current ability to measure an abnormality or control the camera when an abnormality is recognized. The inability to accurately localize CE-detected abnormalities makes it difficult to confirm or determine the clinical importance of findings not detected with standard techniques. This pitfall of CE further underscores the need to perfect complementary imaging techniques, such as CT enterography or enteroclysis, to confirm and localize small-bowel lesions. Other disadvantages of CE include an 8-hour pretest fast, an 8-hour recording time, a 2-hour image download time, and up to a 1-hour interpretation time. The cost of the examination is also not fully reimbursed at this time. Another disadvantage of CE is that it is contraindicated in patients with known obstruction or stricture, since the device could become lodged in the narrowed segment. In patients with high-grade obstruction, CT would appear to be the next best test to evaluate the cause and location of the obstruction (14,17). SBFT examination can also be used in these patients but can be time-consuming and cause more patient discomfort compared with CT.

The main advantage of CE is the ability to provide a more complete endoscopic evaluation of the small bowel than has previously been available. Other advantages include relatively low risk for the patient, absence of radiation, and minimal patient discomfort. It is also likely less operator dependent compared with the SBFT examination. Vascular abnormalities, such as cases of angioectasia, are a common cause of gastrointestinal bleeding and are also detected most reliably with direct visualization.

Although comparisons were only performed for patients who had undergone the same studies (ie, CE and SBFT examination or CE and CT), there are obviously several confounding factors within this analysis that could affect the results. For example, the radiologic studies were performed at several institutions with varying techniques and by several radiologists. Any of these factors clearly could affect the results. In addition, the conclusions concerning CE can be extrapolated only to those patients with negative findings at barium examination and not to all patients undergoing a barium study, since patients with strictures identified at barium examination were excluded from undergoing CE. Finally, verification bias favoring CE also exists because in most cases of angioectasia and ulcers there was no pathologic proof. Studies in which researchers evaluate CE are difficult because pathologic proof of many CE findings would require intraoperative endoscopy, which is not the standard of care for most common small-bowel CE findings. Another relative study limitation is the 0–6-month interval between endoscopy and radiologic examination, and this interval could allow abnormalities to become more or less conspicuous at a subsequent examination.

The results of this retrospective review mainly serve as a preliminary comparison of small-bowel imaging techniques that included SBFT examination, enteroclysis, CT, and CE. In patients without evidence of small-bowel stricture at barium studies, CE helped to find more small-bowel disease compared with barium examinations and CT. While radiologic imaging examinations were expectedly negative for findings such as angioectasia, other abnormalities such as ulcers or masses were also unexpectedly not detected. Current CE technology, however, cannot measure ulcers or polyps, so the size of these lesions not detected by using barium examination or CT is not known. Surprisingly, CT depicted more small-bowel findings than did barium studies, and specialized CT protocols for small-bowel imaging may further improve performance. In the future, CE is likely to play an important role in small-bowel imaging, but further prospective comparative studies with barium examinations and CT are needed.


    ACKNOWLEDGMENTS
 
We gratefully acknowledge the statistical assistance of Joseph G. Hentz, MS.


    FOOTNOTES
 
Abbreviations: CE = capsule endoscopy, SBFT = small-bowel follow through

Author contributions: Guarantor of integrity of entire study, A.K.H.; study concepts, A.K.H.; study design, A.K.H., J.A.L.; literature research, A.K.H.; clinical studies, all authors; data acquisition, all authors; data analysis/interpretation, J.A.L., V.K.S., D.E.F.; statistical analysis, A.K.H.; manuscript preparation, definition of intellectual content, and final version approval, A.K.H.; manuscript editing and revision/review, A.K.H., J.A.L., D.E.F.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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A. K. Hara, J. A. Leighton, R. I. Heigh, V. K. Sharma, A. C. Silva, G. De Petris, J. G. Hentz, and D. E. Fleischer
Crohn Disease of the Small Bowel: Preliminary Comparison among CT Enterography, Capsule Endoscopy, Small-Bowel Follow-through, and Ileoscopy
Radiology, January 1, 2006; 238(1): 128 - 134.
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D. D. T. Maglinte
Capsule Imaging and the Role of Radiology in the Investigation of Diseases of the Small Bowel
Radiology, September 1, 2005; 236(3): 763 - 767.
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A. K. Hara, J. A. Leighton, V. K. Sharma, R. I. Heigh, and D. E. Fleischer
Imaging of Small Bowel Disease: Comparison of Capsule Endoscopy, Standard Endoscopy, Barium Examination, and CT
RadioGraphics, May 1, 2005; 25(3): 697 - 711.
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D. D. T. Maglinte
Invited Commentary
RadioGraphics, May 1, 2005; 25(3): 711 - 718.
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More Data on Capsule Endoscopy of the Small Bowel
Journal Watch (General), January 27, 2004; 2004(127): 2 - 2.
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