RadioGraphics 2006;26:657-662
Invited Commentary
Dean D. T. Maglinte, MD
Department of Radiology, Indiana University Hospital Indianapolis, Indiana
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Introduction
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Despite advances in endoscopy, the mesenteric small intestine remains the most challenging segment of the alimentary canal to examine owing to its length, caliber, and location within the peritoneal cavity. Since its introduction into clinical use in the late 1970s, CT has improved the diagnosis of a wide variety of intestinal disorders. The introduction of helical technology in 1989 and the subsequent development of multi–detector row CT will further change how organs that are longer than they are wide and that have an unpredictable orientation (eg, the small bowel) will be evaluated (1,2). Because multi–detector row CT allows acquisition of isotropic or near isotropic voxels, multiplanar imaging of the small bowel is now a daily clinical tool used to improve CT diagnosis (2–4).
The article by Paulsen et al (5) provides insights into how multi–detector row CT will continue to change how we investigate small bowel disorders. The authors’ clinical experience shows us that CT enterography can be used routinely in the diagnosis of small bowel diseases. Currently, the small bowel follow-through examination is the most commonly performed radiologic examination when small bowel disease is suspected (6). The question remains whether CT enterography will replace the small bowel follow-through examination, with its known inherent limitations (7–9), in the routine radiologic investigation of small bowel disorders. Furthermore, are there additional clinical applications of CT enterography other than those mentioned in the article?
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Historical and Technical Considerations
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The term CT enterography was introduced by Raptopoulos et al in 1997 in reference to a modified abdominal CT technique tailored to address small bowel Crohn disease (10,11). With this technique, approximately 1000–1500 mL of a 2% barium-based or 2%–2.5% water-soluble iodine-based oral contrast material was administered 1–2 hours before scanning. A high dose of intravenous contrast material and a biphasic injection rate regimen were used. This method resulted in vascular opacification, parenchymal enhancement, and combined renal parenchymal and excretory phase scanning (10). Another small bowel–focused CT method was subsequently described in which a neutral enteric contrast material (PEG electrolyte solution and whole milk) and an isotonic oral solution were used (12,13).
In the article by Paulsen et al (5), water and water-methylcellulose solution were initially used, then were replaced by PEG electrolyte solution and subsequently by low-concentration barium (0.1% w/v ultra-low-dose barium with sorbitol) as the authors’ technique evolved. A total volume of 1350 mL of oral contrast material was used and was administered according to the schedule described in the article (5).
In the subset of patients mentioned in the article in whom different methods of CT enterography were used, moderate to severe active inflammation of Crohn disease, medium-sized tumors, and greater degrees of small bowel obstruction were diagnosed. However, the question arises whether the volumes of oral contrast material used are adequate in patients without active inflammation, with a possible subcentimeter mass, or with low-grade obstruction. In my experience with CT enteroclysis performed with either (a) neutral enteric contrast material with intravenous contrast material or (b) positive enteric contrast material, the total volume of oral contrast material given will be inadequate to maintain optimum filling of a nonobstructed small intestine and the proximal colon. In our practice, we perform CT enterography with a maximum of 2250 mL of oral contrast material—less if the patient experiences nausea, which is why we give patients the choice of water or the blackberry-flavored low-concentration barium as the enteric oral contrast material. In my experience, it is the total volume of contrast material ingested and the use of a promotility agent with subsequent administration of a hypotonic agent that ensure optimum filling of the entire small intestine. The schedule for the use of oral contrast material in CT enterography at my institution is shown in the Figure.
Unless enteroclysis (enteric infusion) is performed, there is no oral contrast material that adequately distends the small intestine if the small bowel has not already been distended by an inflammatory process or other obstructing abnormality. I would question the statement by Paulsen et al (5) that no difference in the adequacy of small bowel distention was noted between patients who underwent nasojejunal intubation and those who ingested a large volume of oral contrast material in a feasibility study by Wold et al (14). A review of that article seems to indicate that its authors were comparing CT enterography performed with a high dose of orally ingested contrast material with CT enterography performed with a similar amount of contrast material injected manually through a nasojejunal tube. The latter procedure, which was called CT enteroclysis by the authors, was not really enteroclysis as it should be performed. First, infusion of contrast material at a high speed should be continuous and cannot be achieved with manual syringe injection, as was performed in their study. Second, the infusion should be continued during CT acquisition, not discontinued as in their study. Injecting a hypotonic agent does not distend the small bowel or colon, although this is a frequent misconception; it simply abolishes or diminishes peristalsis. The reason (as is well shown in the article by Paulsen et al [5]) that patients with active inflammation have distended small bowel is that inflamed segments undergo spasm and proximal segments are distended and lesion conspicuity improved because of the use of neutral enteric contrast and the mucosal or mural enhancement produced by intravenous contrast material. A similar phenomenon occurs when a medium-sized intraluminal or mural mass or partial obstruction is present. In patients without small bowel inflammation or a medium-sized mass, the difficulty of maintaining filling of the entire length of a nonobstructing small bowel may be a limitation of studies performed with a smaller volume of oral contrast material. More time may be allowed for ingestion to prevent nausea when a large volume is used. Excluding significant small bowel abnormalities in a nondistended or collapsed segment is difficult. Confident exclusion of a small bowel lesion is unlikely to be achieved with less than 1.5 L of a neutral oral contrast agent.
Although I would agree that water is absorbed faster than the other oral agents described, in my experience, it is not absorbed fast enough to produce clinical problems when rapidly infused. We routinely use at least 3 L of water for CT enteroclysis and have had no complications with this regime in a tertiary care facility where 1200–1300 enteroclysis examinations are performed annually. The enteric contrast agent is eliminated rectally before significant absorption ensues (15). However, when water is ingested, its slower transit may result in its being absorbed faster; hence, the commercially prepared low-concentration barium contains additives that decrease absorption and result in better filling of a noninflamed or nonobstructed small bowel. The administration of (a) a promotility agent after ingestion of the first 400-mL aliquot of neutral oral contrast material and (b) a hypotonic agent just before CT acquisition will improve filling of the entire small bowel. The use of a larger volume of oral contrast material allows evaluation of both the small bowel and the colon, an important consideration in the assessment of inflammatory bowel disease.
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Clinical Considerations
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Crohn Disease
It is my opinion that CT enterography with neutral enteric and intravenous contrast material will eventually replace the barium small bowel follow-though examination as the routine initial radiologic method of investigation for small bowel Crohn disease. This trend is well documented in the article by Paulsen et al (5), particularly in the evaluation of patients with known small bowel or colonic Crohn disease. CT enterography may not be as accurate in the classification of small bowel Crohn disease into subtypes as enteric volume-challenged small bowel examinations such as CT enteroclysis. Nevertheless, because CT enterography is easy to perform, it will replace traditional low-yield diagnostic procedures such as the follow-through examination and conventional abdominal CT with positive oral contrast material for this indication (16). The capacity of CT enterography to help objectively quantify mural inflammation will aid in solving part of the conundrum in the clinical management of Crohn disease (17). The capacity of CT enterography to depict segments with mild stenotic involvement and to demonstrate the full extent of disease prior to surgery has yet to be determined (18). It has been shown that even CT enteroclysis with neutral enteric and intravenous contrast material may not demonstrate the apthae of early Crohn disease if they represent the only manifestation of the disease and can be visualized only at double-contrast barium-air enteroclysis (19); however, this is most likely an uncommon situation. Although double-contrast barium-air enteroclysis excels in demonstrating the superficial lesions of early Crohn disease (20,21), it is uncomfortable for the patient (requiring conscious sedation) and technically difficult and will most likely be used to characterize nonspecific ulcers or stenosis seen at capsule endoscopy in practices where the relevant expertise is available (22).
Small Bowel Tumors
A method of small bowel examination with a high negative predictive value and high sensitivity is needed to evaluate for small bowel tumors owing to the nonspecificity of the presenting symptoms. Capsule endoscopy does not appear to be accurate in the evaluation of submucosal masses (19). CT enteroclysis has been shown to be accurate for this indication (23,24) and more accurate than capsule endoscopy (23). Larger masses, especially those with obstructive symptoms, can be visualized at CT enterography; however, visualization of subcentimeter polypoid masses that do not produce obstruction will most likely be difficult.
Miscellaneous Clinical Applications
As stated in the article by Paulsen et al (5), other diseases can be diagnosed and significant incidental nonintestinal abnormalities depicted with CT enterography, which, like CT enteroclysis, does indeed allow global abdominal evaluation. Thanks to (a) the neutral contrast material seen in the alimentary canal, (b) the enhancement pattern produced by intravenous contrast material, and (c) the use of multiplanar reformation, we have diagnosed pancreas divisum and small solid organ tumors in our practice. Perhaps the term CT enterography is a misnomer, since this modality is in reality a form of abdominopelvic CT that makes use of a larger volume of neutral oral contrast agent and intravenous contrast enhancement. Conventional CT is performed with a smaller volume of positive oral contrast agent, which decreases the conspicuity of mucosal enhancement at multisection CT when intravenous contrast material is administered.
CT enterography may have value in the investigation of acute abdominal pain (11). The large volume of neutral oral contrast material required may not be feasible in a nauseated patient, and the length of time needed to ingest the recommended volume may be impractical in a busy emergency department, where speed and efficiency are required. CT enterography may be feasible in the emergency setting if the patient has a nasogastric tube. The required volume can be administered through the tube. This procedure can be of value in patients suspected of having intestinal ischemia or active bleeding (25). An added advantage of CT enterography with neutral oral and intravenous contrast material that was not mentioned in the article by Paulsen et al (5) is that, in addition to allowing improved depiction of mucosal and mural enhancement, the use of neutral oral contrast material prevents misinterpretation of small bowel abnormalities from admixture defects and pseudomasses seen when using positive oral contrast material in patients with small bowel stasis from any cause (25).
Further experience will help define the role of CT enterography in the investigation of other diseases.
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Summary
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The article by Paulsen et al (5) describes an extended application of multisection CT technology in the evaluation of the abdomen and pelvis, particularly in patients with small bowel Crohn disease. The use of this technology in other indications remains to be determined. It will most likely replace the traditional small bowel follow-through examination as the initial radiologic method of investigation for small bowel Crohn disease. Enteroclysis with its various modifications will remain the most accurate method of small bowel investigation and a tool for answering relevant questions that cannot be answered with nonenteric volume-challenged examinations. The technique of CT enterography will continue to evolve with experience and with the development of other oral contrast agents. All factors considered, with intestinal CT, the more neutral or negative the enteric contrast material used, the better the mucosal or mural enhancement; thus, improved lesion conspicuity results when intravenous contrast material is administered.
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References
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- Horton KM, Fishman EK. The current status of multidetector row CT and three-dimensional imaging of the small bowel. Radiol Clin North Am 2003;41:199–212.[CrossRef][Medline]
- Maglinte DD, Bender GN, Heitkamp DE, Lappas JC, Kelvin FM. Multidetector-row helical CT enteroclysis. Radiol Clin North Am 2003;41:249–262.[CrossRef][Medline]
- Paulson EK, Jaffe TA, Thomas J, Harris JP, Nelson RC. MDCT of patients with acute abdominal pain: a new perspective using coronal reformations from submillimeter isotropic voxels. AJR Am J Roentgenol 2004;183:899–906.[Free Full Text]
- Yaghmai V, Nikolaidis P, Hammond N, et al. CT diagnosis of small bowel obstruction using coronal reformations without the aid of axial images: accuracy and practical implications—Abdominal Radiology Course 2005. San Antonio, Tex: Society of Gastrointestinal Radiologists, 2005.
- Paulsen SR, Huprich JE, Fletcher JG, et al. CT enterography as a diagnostic tool in evaluating small bowel disorders: review of clinical experience with over 700 cases. RadioGraphics 2006;26:641–662.[Abstract/Free Full Text]
- Ha AS, Levine MS, Rubesin SE, Laufer I, Herlinger H. Radiographic examination of the small bowel: survey of practice patterns in the United States. Radiology 2004;231:407–412.[Abstract/Free Full Text]
- Maglinte DD, Burney BT, Miller RE. Lesions missed on small bowel follow-through: analysis and recommendations. Radiology 1982;144:737–739.[Abstract/Free Full Text]
- Maglinte DD, O’Connor K, Bessette J, Chernish SM, Kelvin FM. The role of the physician in the late diagnosis of primary malignant tumors of the small intestine. Am J Gastroenterol 1991;86:304–308.[Medline]
- Maglinte DD, Kelvin FM, O’Connor K, Lappas JC, Chernish SM. Review: current status of small bowel radiography. Abdom Imaging 1996;21:247–257.[CrossRef][Medline]
- Raptopoulos V, Schwartz RK, McNicholas MM, Movson J, Pearlman J, Joffe N. Multiplanar helical CT enterography in patients with Crohn’s disease. AJR Am J Roentgenol 1997;169:1545–1550.[Abstract/Free Full Text]
- Rosen MP, Siewart B, Sands DZ, Bromberg R, Edlow J, Raptopoulos V. Value of abdominal CT in the emergency department for patients with abdominal pain. Eur Radiol 2003;13:418–424.[Medline]
- Thompson SE, Raptopoulos V, Sheiman RL, McNicholas MM, Prassopoulos P. Abdominal helical CT: milk as low-attenuation oral contrast agent. Radiology 1999;211:870–875.[Abstract/Free Full Text]
- Mazzeo S, Caramella D, Battola L, et al. Crohn disease of the small bowel: spiral CT evaluation after oral hyperhydration with isotonic solution. J Comput Assist Tomogr 2001;25:612–616.[CrossRef][Medline]
- Wold PB, Fletcher JG, Johnson CD, Sandborn WJ. Assessment of small bowel Crohn disease: noninvasive peroral CT enterography compared with other imaging methods and endoscopy—feasibility study. Radiology 2003;229:275–281.[Abstract/Free Full Text]
- Maglinte DD, Lappas JC, Heitkamp D, et al. Technical refinements in enteroclysis: advances in intestinal imaging. Radiol Clin North Am 2003; 41:213–229.[CrossRef][Medline]
- Maglinte DD, Gourtsoyiannis, Rex D, et al. Classifications of small bowel Crohn’s subtypes based on multimodality imaging. Radiol Clin North Am 2003;41:285–303.[CrossRef][Medline]
- Bodily KD, Fletcher JG, Solem CA, et al. Crohn disease: mural attenuation and thickness at contrast-enhanced CT enterography—correlation with endoscopic and histologic findings of inflammation. Radiology 2006;238:505–516.[Abstract/Free Full Text]
- Maglinte DD. Science to practice: do mural attenuation and thickness at contrast-enhanced CT enterography correlate with endoscopic and histologic inflammation in Crohn disease? Radiology 2006;238:381–382.[Abstract/Free Full Text]
- Maglinte DD. Capsule imaging and the role of radiology in the investigation of diseases of the small bowel. Radiology 2005;236:763–767.[Free Full Text]
- Ekberg O. Crohn’s disease of the small bowel examined by double contrast technique. Gastrointest Radiol 1977;1(4):355–359.[Medline]
- Tanaka K. Double contrast study of the minute lesions of Crohn’s disease of the small intestine. Stom Intest 1982;17:871–882.
- Maglinte DD. Small bowel imaging: a rapidly changing field and a challenge to radiology. Eur Radiol (in press).
- Boudiaf M, Jaff A, Soyer P, Bouchnik Y, Hamzi L, Rymer R. Small-bowel diseases: prospective evaluation of multi–detector row helical CT enteroclysis in 107 consecutive patients. Radiology 2004; 233:338–344.[Abstract/Free Full Text]
- Romano S, De Lutio E, Rollandi GA, Romano L, Grassi R, Maglinte DD. Multidetector computed tomography enteroclysis (MDCT-E) with neutral enteral and IV contrast enhancement in tumor detection. Eur Radiol 2005;15:1178–1183.[CrossRef][Medline]
- Maglinte DDT, Rhea JT, Ledbetter MS. The role of CT in acute abdominal disease: pitfalls and their lessons. In: Mann FA, et al. Syllabus: emergency radiology—categorical course in diagnostic radiology. Oak Brook, Ill: Radiological Society of North America, 2004; 119–131.
Author’s Response
James E. Huprich, MD
Department of Diagnostic Radiology, Mayo Clinic Rochester, Minnesota
We thank Dr Maglinte for his comments. We share his enthusiasm for this new technique (CT enterography) and believe it will play a significant role in evaluating patients with suspected small bowel disease.
We would like to respond briefly to some of his questions and comments. We believe that CT enterography will indeed replace small bowel follow-through examinations in the routine investigation of many small bowel disorders. Our experience and that of others demonstrates the usefulness of CT enterography in the evaluation of patients with Crohn disease. We believe that CT enterography will also prove to be the best modality for suspected submucosal small bowel tumors, which appear to be a "blind spot" for capsule endoscopy. Whether small bowel polyps can be accurately detected remains to be seen. Preliminary studies in which we used a modified version of the technique described in our article (1) suggest that multiphase CT enterography can help accurately detect abnormalities responsible for obscure gastrointestinal bleeding and can complement capsule endoscopy in these patients (2).
We believe that, in most cases, the volumes of oral contrast material we suggest will produce distention that is adequate to separate the walls of the small bowel and allow detection of bowel wall abnormalities. We are not attempting to "volume challenge" the small bowel so as to detect low-grade obstruction—only to produce good separation of opposing luminal surfaces. During our early experience with CT enterography, we administered 2000 mL of PEG electrolyte solution orally. As low-concentration barium solution entered our practice, we felt that 1350–1800 mL of this agent provided small bowel distention equivalent to that achievable with earlier techniques. Whether the administration of greater volumes of low-concentration barium results in an improved diagnostic yield (as Dr Maglinte suggests) is a question we are currently evaluating. However, one disadvantage of this contrast agent is that 1350 mL can cause mild, self-limited diarrhea, and greater volumes may exacerbate this side effect.
We share Dr Maglinte’s opinion that low-grade or intermittent small bowel obstructions are unlikely to be detectable with peroral techniques of luminal distention and probably require volume challenging the small bowel by means of enteric intubation. In patients who do not have Crohn disease in whom low-grade obstruction is suspected, we prefer to perform CT enteroclysis through an enteric tube.
As Dr Maglinte pointed out, adequate bowel distention by means of oral contrast material administration is easier to achieve in patients with Crohn disease owing to the altered compliance of diseased bowel wall. This phenomenon aids in the diagnosis of areas of significant stenosis. In our experience, persistent areas of narrowing seen on scans obtained a few minutes apart correlate well with strictures demonstrated at conventional small bowel follow-through examination, especially when accompanied by proximal bowel dilatation and mucosal hyperenhancement. We have also been able to detect fistulas with this technique, which appear as extraenteric enhancing tracts. The versatility of CT enterography should allow classification of cases into subtypes of Crohn disease and help guide therapy. Further investigation in this area seems warranted.
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References
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- Huprich JE, Fletcher JG, Alexander JA, et al. Obscure GI bleeding: 64-channel multi-phase, multi-planar CT enterography has a role (abstr). In: Radiological Society of North America scientific assembly and annual meeting program [book online]. Oak Brook, Ill: Radiological Society of North America, 2005. http://rsna2005.rsna.org/rsna2005/V2005.
- Paulson EK, Jaffe TA, Thomas J, Harris JP, Nelson RC. MDCT of patients with acute abdominal pain: a new perspective using coronal reformations from submillimeter isotropic voxels. AJR Am J Roentgenol 2004;183:899–906.
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Introduction
Historical and Technical...
