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DOI: 10.1148/radiol.2363041868
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(Radiology 2005;236:763-767.)
© RSNA, 2005

Editorial

Capsule Imaging and the Role of Radiology in the Investigation of Diseases of the Small Bowel1

Dean D. T. Maglinte, MD

1 From the Department of Radiology, Indiana University Hospital, Indiana University School of Medicine, 550 N University Blvd, Room UH0279, Indianapolis, IN 46202-5253. Received November 2, 2004; accepted November 5. Address correspondence to the author (e-mail: dmaglint{at}iupui.edu).

The mesenteric small intestine is the last frontier of the alimentary tube that has not been conquered by fiberoptic endoscopy. In the late 1980s and early 1990s, proponents of enteroclysis were predicting the eventual decline in the use of the small bowel follow-through (SBFT) examination in the investigation of small bowel diseases (1). This prediction was based not only on the reported superiority of enteroclysis over the SBFT examination but also on the diagnostic potential of the flexible endoscope (2). Progress in enteroscopy was small and slow, however, and enteroclysis has not become as widespread as initially expected. The SBFT examination remains the most commonly performed radiologic examination of the small bowel (3,4).

In an article published in 2004 by Iddan and Swain (5), information pertinent to the history of capsule endoscopy is included. They reported that, in 1981, Iddan, an engineer with expertise in electro-optics, conceptualized the science fiction–like idea of remote imaging by using the combination of miniaturization of electronic components and advanced telemetry. He discussed his idea with a gastroenterologist, and, by 1994, they had applied for patents, and feasibility studies and studies in volunteers began. Working separately and not knowing the ongoing research by Iddan, Swain, a gastroenterologist from England, and colleagues (6) showed the first live transmission of images of the pig intestinal mucosa by using commonly available electronic components in 1996. The two investigators collaborated in their research efforts, and, by 2000, human studies began. In August 2001, the Food and Drug Administration approved the capsule endoscope (M2A Capsule Endoscope; Given Imaging, Yoqneam, Israel) for clinical use. The American Medical Association recently assigned a permanent Current Procedural Terminology code for insurance reimbursement for capsule endoscopy that became effective on January 1, 2004 (7).

This editorial is intended to acquaint radiologists with wireless capsule endoscopy and clinical results of comparative studies of wireless capsule endoscopy and radiologic methods of investigation of the small intestine. The potential effect of capsule imaging and the recent introduction of the patency capsule (M2A Patency Capsule; Given) into the use of radiologic methods of investigation are discussed. Suggestions are made to keep radiologic investigations clinically relevant in the current investigation of small bowel diseases.

Wireless Capsule Endoscope
The capsule endoscope is 11 mm in diameter and 26 mm in length. It weighs 3.7 g and is contained in a plastic capsule that is resistant to the action of digestive juices. The three major components of capsule imaging are (a) the camera and transmitter, (b) the receiver and recorder, and (c) the workstation. The battery life of the capsule is 7–8 hours. Two images are transmitted per second. Approximately 55 000 images are transmitted to six electrocardiogram-like receiving sensors that are applied to the abdominal wall and are recorded with hardware worn on a belt powered with two 5D cell silver oxide batteries. The recorded images are downloaded into a workstation with localizing software that approximates the segment of the small bowel recorded. The time for this process was 2–3 hours in the past but has been decreased with software updates. The time for workstation review (interpretation) is 45–90 minutes. The image viewed has a 140° field of view and a 1:8 magnification from a depth of 1–30 mm (8).

The capsule is swallowed with a glass of water after the patient has fasted for 12 hours. The patient can drink water after 2 hours and have a meal after 4 hours. Oroanal transit time is 4–48 hours. Transgastric transit time is 8–184 minutes (average, 61 minutes). Small bowel transit time is 183–393 minutes (average, 251 minutes) (8).

Comparison of Wireless Capsule Endoscopy with Push Enteroscopy
The standard flexible 215-cm enteroscope can be advanced 50–100 cm. Results of animal studies with pellets that have a 3–6-mm circumference have indicated a higher sensitivity of push enteroscopy when compared with capsule enteroscopy in regard to the visualized length of the pellets. With inclusion of the entire length of the small bowel, however, capsule enteroscopy had a higher sensitivity than did push enteroscopy. Evaluation of the esophagus and stomach by using the capsule endoscope is limited (9–11).

Comparison of Wireless Capsule Endoscopy with Radiologic Examinations
The limitations of indirect imaging of the mucosa of the small intestine are starting to become apparent as more studies about the comparison of wireless capsule endoscopy and radiologic investigations are reported (12–18). Notwithstanding selection bias and the difficulty in evaluating the false-positive and false-negative rates of wireless capsule endoscopy, it appears that, on the basis of results of recent comparative clinical studies, capsule imaging depicts more lesions in the mesenteric small intestine than does any other method of radiologic investigation of this segment of the gastrointestinal tract. The conclusions in earlier reports suggested the need for radiologic investigations to exclude potentially obstructive abnormalities of the small bowel—a major risk of wireless capsule endoscopy (12–18). These reports predated the introduction of the patency capsule.

The Patency Capsule
As experience has been accumulated, it has become apparent that the most commonly used radiologic method of investigation, the SBFT examination, has poor sensitivity in the diagnosis of lower grades of partial mechanical obstruction of the small bowel or in the demonstration of small mucosal or submucosal lesions. The wireless capsule was obstructed in reports about patients with normal results of an SBFT examination. The limitations involved in the evaluation of a long, nondistended, overlapping, and tortuous organ such as the small bowel have long been recognized by proponents of enteral volume-challenged (intubation infusion) examinations of the small bowel (enteroclysis with barium and its current modifications, such as computed tomographic [CT] enteroclysis and magnetic resonance [MR] enteroclysis) (19–29). The patency capsule, also known as the obstruction pill, was conceived because of the shortcomings of conventional radiologic examinations in the diagnosis of lower grades of partial obstruction of the small bowel. Early experience with this biodegradable capsule, with dimensions similar to those of the capsule endoscope, indicates that it is an accurate and objective method for the evaluation of potentially obstructive lesions of the small bowel prior to wireless capsule endoscopy (30–32). Investigators in one report suggested that the patency capsule should be used in the early investigation of obstruction of the small bowel, an indication of the potential for bypassing radiologic investigation in the future (31). The patency capsule has just been introduced in the United States and is undergoing clinical trials.

Current Status of Barium Examination of Small Bowel
Enteroclysis has been documented in the literature as the most accurate radiologic method for the diagnosis of obstruction of the small bowel, Crohn disease, unexplained gastrointestinal bleeding, and neoplasms of the small bowel (2). Because of the ease of performance and convenience to radiologists and because of the disadvantages of enteroclysis, which include the discomfort to patients caused by intubation and the need for hands-on involvement by the radiologists in performing the procedure, the SBFT examination has remained the most commonly performed method for the investigation of diseases of the small bowel (3,4).

Accumulated experience with wireless capsule endoscopy has uniformly shown the poor performance of the SBFT examination compared with that of capsule imaging (12–18). Ulcers, erosions, and polyps that are shown by using capsule imaging are reported to be frequently missed by using the SBFT examination. The SBFT examination often was ordered prior to wireless capsule endoscopy to exclude potential causes of obstruction of the small bowel, a major contraindication to wireless capsule endoscopy prior to the introduction of the patency capsule. Although large diverticula and dysmotility of the small bowel can be diagnosed by using the SBFT examination, comparative study results have shown significant limitations of the SBFT examination for the evaluation of other potentially obstructive abnormalities of the small bowel (11–18). The success of the patency capsule may potentially eliminate the need for the SBFT examination prior to capsule imaging. As the use of wireless capsule endoscopy becomes increasingly widespread, the role of the SBFT examination in the investigation of unexplained anemia or gastrointestinal bleeding in a patient without a clinical background of possible obstruction of the small bowel will follow the same route as the Billroth I procedure after the introduction of the histamine 2 receptor antagonists and the proton pump inhibitors.

The biphasic enteroclysis examination, with methylcellulose as the double-contrast agent, has been the most commonly performed enteroclysis method in many countries (19). Recently, we noted that methylcellulose as a double-contrast agent produced a washout effect in the demonstration of superficial mucosal features (13). The more methylcellulose is infused to achieve a good double-contrast effect, the more subtle surface features were effaced, an effect that diminishes lesion conspicuity. Because of this experience in which superficial ulcers of early Crohn disease and small submucosal masses shown by using wireless capsule endoscopy were not diagnosed even when the lesions were pointed out prior to the enteroclysis examination with methylcellulose, a review of the radiologic literature was performed to see which method of radiologic investigation demonstrated superficial mucosal lesions of the small bowel. In 1977, Ekberg (33) reported the results of a comparison of the SBFT examination and double-contrast enteroclysis with air (CO2) in patients with Crohn disease of the small bowel. Aphthoid lesions of the small bowel, which were not shown by using the SBFT examination, were diagnosed by using double-contrast enteroclysis with air. In an article, one researcher correlated findings at double-contrast enteroclysis with air with findings at analysis of surgical and histologic specimens in patients with Crohn disease who underwent surgery (34). Enteroclysis with air showed good correlation in the demonstration of aphthae and small scars. Since adoption of double-contrast enteroclysis with barium and air as the radiologic method of examination in patients with unexplained gastrointestinal bleeding, I have diagnosed superficial ulcers secondary to the administration of medications (nonsteroidal antiinflammatory drugs or potassium) and early Crohn disease with aphthae as the only manifestation in patients. It appears that, with the current experience with double-contrast enteroclysis with barium and air, medication-related small ulcerations may be more common in the small bowel than was previously realized. Unfortunately, double-contrast enteroclysis with barium and air is a technically more demanding examination and is more uncomfortable for the patient than is double-contrast enteroclysis with methylcellulose (35). We offer optional conscious sedation that includes analgesia to our patients who undergo enteroclysis, particularly that with air (35). This has made the procedure more tolerable for both the patient and the operator.

CT Enteroclysis
After an endoscopic examination of the upper and lower gastrointestinal tracts with negative findings, abdominal and pelvic CT frequently is requested prior to an SBFT examination. Large tumors that involve the small bowel, which manifest clinically as gastrointestinal bleeding or anemia, can be diagnosed (17). Small masses, ulcers, and erosions, however, are not diagnosed. Current experience with capsule enteroscopy also has shown this limitation.

A recently described modification of enteroclysis, first reported by Kloppel et al (24) in 1992, was introduced to overcome the individual deficiencies of CT and of enteroclysis with barium and to combine the advantages of both into one technique. The capability of multi–detector row helical CT scanners of increased anatomic coverage with fewer motion artifacts and of production of images with thinner collimation and increased temporal and spatial resolution has led to improved imaging of organs that are longer than they are wide, such as the mesenteric small intestine, by using CT enteroclysis (26). Experience has shown that it is reliable for the diagnosis of diseases of the small bowel (26–29). Initially described as a method used with positive enteral (water-soluble) contrast agents, it has been further refined for use with neutral enteral contrast agents, with intravenous contrast enhancement to address the indication of unexplained gastrointestinal bleeding, anemia, or Crohn disease (28,35). The distention of the small bowel achieved with infusion of neutral enteral contrast agents (such as water, methylcellulose, and others [Volumen; E-Z-Em, Westbury, NY]) and the depiction of the wall of the small bowel with intravenous contrast agents have shown great promise in the demonstration of mucosal hyperemia and edema of the bowel wall caused by inflammatory bowel disease. Findings in recent reports about a large group of patients have shown the reliability of this method for the diagnosis of tumors of the small bowel (36,37). Further clinical experience will define the use of either method of CT enteroclysis for different clinical indications. Personal experience with both methods of CT enteroclysis indicates that the use of neutral enteral and intravenous contrast agents is technically a simpler method than are all the other modifications of enteroclysis, and this experience suggests that CT enteroclysis is better tolerated by patients and allows a more global look, not only of the small bowel but also of the stomach and colon, as well as of the solid abdominal organs (35,37). In addition, the ability to infuse water or other neutral enteral contrast agents through smaller catheters may decrease the need for conscious sedation and may improve patient acceptance of CT enteroclysis.

Radiologic Investigations in the Era of Wireless Capsule Endoscopy
Before capsule endoscopy.—Except for the emergent clinical investigation for possible diseases of the small bowel, in which abdominal CT will remain the primary method of investigation, the role of imaging is likely to undergo reassessment on the basis of current results of wire-less capsule endoscopy in the elective work-up of patients. In the patient who does not have a risk factor that precludes the performance of wireless capsule endoscopy, such as a potentially obstructive lesion of the small bowel, radiology may be left only a limited role. Where the indication raises the possibility of early Crohn disease or enteropathy caused by nonsteroidal antiinflammatory drugs, double-contrast enteroclysis with air is the most reliable method of radiologic investigation in the patient who can tolerate the examination. CT enteroclysis with neutral enteral and intravenous contrast enhancement should otherwise suffice for all before-capsule radiologic investigations when there is a possibility of a potentially obstructive abnormality of the small bowel. How the introduc-tion of the patency capsule will affect the use of radiologic investigations remains to be seen. In the investigation of unexplained gastrointestinal bleeding, in which there is no clinical history to suggest possible obstruction of the small bowel, the SBFT examination will likely be an examination of the past. Where the possibility of a neoplasm of the small bowel exists, CT enteroclysis is a reliable imaging method for this indication (36,37). In my experience, there is no radiologic method of investigation to show angioectasia, the most common wireless capsule endoscopic finding in the evaluation of unexplained gastrointestinal bleeding. Perhaps dual-phase abdominal and pelvic CT with neutral (enteral contrast with intravenous contrast enhancement, so-called CT enterography) may demonstrate this abnormality in the emergent investigation when the patient is actively bleeding (38). With this method, moderate active inflammatory disease abnormalities of the small bowel, such as those in Crohn disease, and larger polypoid masses of the small bowel that may manifest with unexplained bleeding or anemia also can be demonstrated (39,40).

After capsule endoscopy.—As more reports appear in the literature and adoption of wireless capsule endoscopy becomes universal, limitations of wireless capsule endoscopy will become more apparent. Questions about the specificity of wireless capsule endoscopy in the clinical setting will be answered with further experience. Lesions that are missed at wireless capsule endoscopy because of poor bowel preparation, rapid transit of the small bowel, delayed transit of the small bowel, camera orientation away from a lesion, and fistula detection have been reported (39). A stricture that causes a downstream lesion to be missed at wireless capsule endoscopy may not be clinically relevant if the stricture requires surgery. Otherwise, accurate radiologic investigation will be required to characterize areas of narrowing seen at wireless capsule endoscopy (Fig 1).



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  		Figure 1a. Images in 69-year-old man referred for wireless capsule endoscopy because of unexplained gastrointestinal bleeding with negative findings at barium and CT examinations and no abnormalities at endoscopy of upper and lower gastrointestinal tracts. (a) Wireless capsule endoscopic image obtained at level of distal small bowel shows a circumferential linear ulcer (arrow) and mild narrowing of lumen. (b) Image obtained at double-contrast enteroclysis with barium and air for characterization of ulcerations and extent of possible stenotic Crohn disease, which obstructed passage of wireless capsule. Image shows focal circumferential fold thickening (arrow) that obstructed passage of capsule. Multiple areas of proximal narrowing, which did not obstruct the passage of the capsule, also were seen in the middle of the ileum (not shown). At surgery, radiographic diagnosis of obstructive diaphragm disease from long-term use of baby aspirin (81 mg acetylsalicylic acid) was confirmed.

 


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  		Figure 1b. Images in 69-year-old man referred for wireless capsule endoscopy because of unexplained gastrointestinal bleeding with negative findings at barium and CT examinations and no abnormalities at endoscopy of upper and lower gastrointestinal tracts. (a) Wireless capsule endoscopic image obtained at level of distal small bowel shows a circumferential linear ulcer (arrow) and mild narrowing of lumen. (b) Image obtained at double-contrast enteroclysis with barium and air for characterization of ulcerations and extent of possible stenotic Crohn disease, which obstructed passage of wireless capsule. Image shows focal circumferential fold thickening (arrow) that obstructed passage of capsule. Multiple areas of proximal narrowing, which did not obstruct the passage of the capsule, also were seen in the middle of the ileum (not shown). At surgery, radiographic diagnosis of obstructive diaphragm disease from long-term use of baby aspirin (81 mg acetylsalicylic acid) was confirmed.

 
As with all examinations in which the human factor is involved, perceptive errors are inevitable. Already, the clinical importance of the small arteriovenous malformations without positive evidence of bleeding and the superficial mucosal "scratches" shown with wireless capsule endoscopy are increasingly being questioned. A mucosal scratch is a nonspecific finding and will need further characterization for a precise diagnosis in many instances. Personal experience with double-contrast enteroclysis with air and barium that is performed after wireless capsule endoscopy and for which the findings are interpreted by experienced endoscopists to assess disease extent or to characterize Crohn disease has shown the limitations of wireless capsule endoscopy in regard to the characterization of superficial ulcers and their precise location. In one instance, radiologic examination showed a giant Meckel diverticulum with ulcerations in the junction of the diverticulum to the ileum, a finding that was confirmed at surgery. There was no evidence of Crohn disease (Fig 2). In another patient, diaphragm disease was shown at enteroclysis with air, a finding that was ascribed to Crohn disease at wireless capsule endoscopy. This was also confirmed at surgery (Fig 1). There was no evidence of Crohn disease. The patient who has persistent symptoms or bleeding with negative findings at wireless capsule endoscopy will require accurate radiologic investigation. I have diagnosed Meckel diverticulum that was confirmed at surgery in a patient who had negative findings at prior wireless capsule endoscopy. Ulcers caused by nonsteroidal antiinflammatory drugs were shown with double-contrast enteroclysis with air and barium that was performed after wireless capsule endoscopy with negative findings in a teenager who was suspected of having Crohn disease. The localization of lesions and the subtyping of different manifestations of Crohn disease that are necessary to triage patients to medical or surgical treatment will require accurate radiologic investigation. Enteroclysis with barium and air and CT enteroclysis will provide accurate information in most instances.



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  		Figure 2a. Images in 21-year-old man referred for wireless capsule endoscopy because of chronic abdominal pain and anemia. SBFT examination, radionuclide examination, and endoscopy of upper and lower gastrointestinal tracts disclosed no abnormalities. (a) Wireless capsule endoscopic image shows shallow ulcer (arrow) in one segment of ileum. Other images showed ulcers in the adjacent segment and possibly in the colon (not shown). (b) Image obtained at double-contrast enteroclysis with barium and air, performed after wireless capsule endoscopy for characterization of extent of Crohn disease, shows a large saccular dilatation (arrowheads) in a pelvic segment of ileum. Scattered ulcerations (arrow) in one dilated sac are seen adjacent to its attachment to a normal-appearing loop of ileum. At surgery, presence of a giant Meckel diverticulum with ulcerations was confirmed. There was no evidence of Crohn disease.

 


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  		Figure 2b. Images in 21-year-old man referred for wireless capsule endoscopy because of chronic abdominal pain and anemia. SBFT examination, radionuclide examination, and endoscopy of upper and lower gastrointestinal tracts disclosed no abnormalities. (a) Wireless capsule endoscopic image shows shallow ulcer (arrow) in one segment of ileum. Other images showed ulcers in the adjacent segment and possibly in the colon (not shown). (b) Image obtained at double-contrast enteroclysis with barium and air, performed after wireless capsule endoscopy for characterization of extent of Crohn disease, shows a large saccular dilatation (arrowheads) in a pelvic segment of ileum. Scattered ulcerations (arrow) in one dilated sac are seen adjacent to its attachment to a normal-appearing loop of ileum. At surgery, presence of a giant Meckel diverticulum with ulcerations was confirmed. There was no evidence of Crohn disease.

 
Summary
The current clinical indications for wireless capsule endoscopy have been expanded to include almost any symptom of disease of the small bowel. The SBFT examination previously was a prerequisite for wireless capsule endoscopic protocols before capsule administration to exclude potentially obstructive lesions of the small bowel. Commonly, patients also underwent abdominal CT with positive oral contrast and intravenous contrast enhancement. False-negative results and low sensitivity with these methods of investigation to rule out potentially obstructive abnormalities of the small bowel led to the development of the patency capsule. The superior results with wireless capsule endoscopy, compared with these radiologic methods of investigation, has again exposed the limitations of nonenteral volume–challenged examinations known to proponents of enteroclysis but infrequently used because of convenience and patient discomfort.

As more experience with wireless capsule endoscopy and the recently introduced patency capsule is reported, the role of radiologic investigations in the elective clinical investigation of diseases of the small bowel will need to undergo reevaluation. The appropriate use of double-contrast enteroclysis with barium and air and CT enteroclysis will keep radiologic investigations important and in the forefront of imaging of the small bowel in the elective investigation of diseases of the small bowel. In a market-driven health care environment, with current reported results of wireless capsule endoscopy, the convenience and ease of performance of radiologic methods of investigation that have low sensitivity and poor negative predictive value will no longer justify the relevance of the SBFT examination in the elective investigation of diseases of the small bowel. With the availability of more reliable and refined methods of radiologic investigation, the SBFT examination may likely become a historical vignette in the era of capsule imaging.

FOOTNOTES

Author stated no financial relationship to disclose.

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Am. J. Roentgenol., May 1, 2007; 188(5): 1344 - 1355.
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D. D. T. Maglinte and J. E. Huprich
Invited Commentary * Author's Response.
RadioGraphics, May 1, 2006; 26(3): 657 - 662.
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