Applied Radiology

 Dr. Fletcher is a Professor of Radiology, Dr. Fidler is an Associate Professor of Radiology, Dr. Huprich is an Associate Professor of Radiology, Mr. Llano is a Research Fellow, Mr. Spencer is a Research Fellow, Department of Radiology, and Dr. Bruining is an Assistant Professor of Medicine, Division of Gastroenterology and Hepatology, at the Mayo Clinic, Rochester, MN.

Recent advances in computed tomography (CT) and magnetic resonance (MR) technology permit excellent visualization of the small-bowel wall and lumen with enteric contrast when the organ is appropriately distended.^1,2 These techniques can accurately detect small-bowel inflammation,^3-6 tumors,^7,8 and even vascular lesions.^8,9 These imaging advances directly impact patient care and are changing diagnostic approaches to patients with inflammatory bowel disease and small-bowel tumors.^10,11

Overview of techniques: Acquisition and indication

Multiple variations exist for CT and MR imaging of the small bowel. Table 1 summarizes the clinical indications for different types of dedicated small-bowel imaging exams with CT or MR. Table 2 summarizes the most salient features of image acquisition for each of these imaging alternatives.

CT enterography

CT enterography is a global exam to assess for suspected small-bowel disease. Predominant indications include Crohn’s disease (diagnosis and staging), abdominal pain, diarrhea, diffuse small-bowel diseases, and low-grade obstruction. It is performed with large volumes of neutral enteric contrast, along with iodinated intravenous contrast, to maximize the visualization of enhancing small-bowel wall and inflammation. Multiplanar images are reconstructed with high spatial resolution (slice thickness ≤3 mm) in multiple planes. While water can be used for enteric contrast, agents that prohibit resorption of water along the small-bowel lumen,such as polyethylene glycol and low-contrast barium solution (Volumen), are preferred, as they improve small-bowel distention and lengthen the period in which optimal imaging is possible.¹² Our institution typically gives patients 3 bottles (1350 cc) of low-contrast barium solution (Volumen) over 30 to 60 min prior to a CT or MR enterography examination, with an additional 500 cc of water 15 min prior to imaging. Because of the large volume of ingested enteric contrast, radiologists and clinicians should recognize that other imaging alternatives should be contemplated for hospitalized patients. Contrast-enhanced CT is typically performed 50 sec after the injection of enteric contrast during the enteric phase, when peak small-bowel enhancement is achieved.¹³ However, it should be recognized that imaging in the portal phase of enhancement is also acceptable and does not decrease the performance of the exam in identifying active Crohn’s disease (Figure 1).¹⁴ Ideally, minimal detector configurations of < 1 mm are selected to obtain crisp coronal images that maximize z-axis spatial resolution. Radiologic technologists should be taught that CT enterography exams must obtain images through the entire perineum in order to detect perianal fistulizing disease, which is the sole finding of active disease in some patients. CT enterography exams should be performed with CTDI_vol less than routine abdominal CT, despite the decreased slice thickness, which is possible because of the high contrast of the small-bowel wall and Crohn’s-related enteric inflammation. Automatic exposure control should be utilized to minimize and individualize radiation dose. Recent studies have shown that automatic exposure control can be used to substantially decrease radiation dose at CT enterography, while maintaining diagnostic performance (Figure 1).^15-17 Lower tube voltages can be used to increase iodine signal to compensate for suboptimal intravenous contrast or to reduce radiation dose (Figure 2).

Because segmental mural hyperenhancement is associated with histologic inflammation,⁴ CT enterography can be used to detect small-bowel, Crohn’s-related inflammation. CT enterography has a sensitivity of approximately 80% to 90% for detecting active small-bowel inflammation from Crohn’s disease, when CT enterography is performed as described above and using ileocolonoscopy with biopsy as a reference standard.^{3-5, 18-22} However, a recent comparison of CT and MR enterography demonstrated that active small-bowel inflammation can be present when a normal-appearing ileal mucosa is identified at ileocolonoscopy.⁶ The potential systematic error in using ileocolonoscopy alone as a reference standard for detecting small-bowel Crohn’s disease likely results in an 8% to 9% underestimate of sensitivity in theafore mentioned studies.²³ Radiologists should use a combination of mural thickness and hyperenhancement when identifying active small-bowel inflammation.^{3, 23} Similar findings can be used to identify colonic inflammation.²⁴

MR enterography

MR enterography can be performed with standard 1.5 tesla (T) magnets employing an 8-channel phased array coil to image the abdomen and pelvis. The timing of enteric contrast ingestion is similar to CT enterography. Precontrast images generally consist of axial and coronal single-shot, fast-spin echo, and TrueFISP imaging. Single-shot, fast-spin echo images permit clear depiction of the gut wall and have few artifacts other than flow voids within the intestinal lumen from peristalsis. TrueFISP imaging also clearly depicts the small-bowel wall and is particularly useful for examining the small-bowel mesentery. We employ a double-dose of gadolinium contrast for MR enterography, with the 3D VIBE sequences being started at 45 sec after the beginning of gadolinium injection. Dynamic coronal images are acquired in 3 sequential volumes,with 10 sec between scans to allow for breath holding. Postcontrast VIBE and 2D SPGR images with saturation are also obtained. 0.5 mg ofGlucagon is given subcutaneously at the beginning of the MR examination and another 0.5 mg is given intravenously immediately prior to gadolinium enhancement to alleviate motion artifact from bowel peristalsis.

For the detection of Crohn’s disease, several prospective small studies and a large review have shown that the sensitivity of MR enterography is similar to CT enterography.^{6, 25-27}

Triple-phase CT enterography

Multiphase CT enterography is performed similarly to single-phase CT enterography, except that multiple acquisitions are obtained. Arterial-phase imaging is performed to demonstrate angiodysplasias and arterial venous shunting, with enteric-phase images acquired to display a majority of small-bowel tumors and inflammation, with delayed-phase images increasing diagnostic confidence and potentially demonstrating active bleeding. Axial and coronal images are reconstructed at 2-mm slice width and 1-mm reconstruction interval with coronal maximum intensity projection (MIP) images often being used to highlight enhancing pathology on coronal reconstruction.²⁸ Radiation dose can be minimized with automatic exposure control and kV selection, but most importantly, with appropriate patient selection.¹¹

Triple-phase CT enterography is reserved for patients with obscure GI bleeding and in whom a suspected bleeding source is not found after initial primary upper and lower endoscopy. It is a complementary test to capsule endoscopy.^{8, 11} We recently performed a prospective study in 58 adult patients with obscure GI bleeding, with all patients undergoing capsule endoscopy and multiphase CT enterography within one month. ²⁹ Multiphase CT enterography and capsule endoscopy exams were positive in 14 of 16 and 6 of 16 patients, respectively,yielding sensitivities of 88% vs 38%, with multiphase CT enterography being significantly more sensitive. This improved sensitivity was predominantly due to the improved identification of small-bowel tumors with 6 of 9 being missed by capsule endoscopy, but not multiphaseCT enterography (Figure 3).

MR enteroclysis

Cross-sectional enteroclysis provides superior bowel distention compared to enterography at the expense of decreased patient acceptance. Therefore, at our institution, enteroclysis is reserved for those cases with negative conventional imaging or enterography and the need for excellent small-bowel distention to detect subtle abnormalities. MR enteroclysis is performed for suspected low-grade small-bowel obstruction when routine imaging fails to demonstrate a partial small-bowel obstruction (Figure 4). Following fluoroscopic placement of a nasojejunal tube, precontrast monitoring scans are performed during the rapid infusion of bi-phasic, enteric contrast agents (typically between 80 cc/min and 120 cc/min, depending upon patient symptoms). Precontrast radiologist monitoring is required to assess for distention of the small bowel and stomach. Once distention of the terminal ileum is achieved or when patient symptoms develop or when a persistent transition zone is identified, high-resolution axial and coronal images are acquired before and after intravenous contrast administration.Multiphase imaging can be helpful over suspected points of obstruction to demonstrate a typical to-and-fro peristalsis seen at fluoroscopy proximal to points of obstruction.

MR enteroclysis is predominantly used at our institution for the diagnosis of low-grade partial small-bowel obstruction.³⁰ It is being increasingly employed to evaluate for suspected small-bowel tumors at other sites.^31,32 Some have recently shown that MR enterography without placement of the nasojejunal tube may also be useful in identifying small-bowel polyps.⁷

CT enteroclysis

CT enteroclysis is performed similarly to MR enteroclysis. Positive enteric contrast is generally utilized for suspected small-bowel neoplasms or partial obstructions. Neutral enteric contrast is generally employed when differential possibilities, such as radiation enteritis or Crohn’s disease, are more likely. Low-dose monitoring scans are performed after infusion of every 500-1000 cc of enteric contrast, with rates of infusion being increased or decreased depending upon patient symptomatology. During such monitoring scans, we increase the rate when the bowel distention is < 2 cm and decrease the rate of infusion when bowel diameter is > 3 cm. CT enteroclysis with neutral contrast is performed at the same dose settings as routine CT enterography. With the use of positive enteric contrast, high spatial resolution images can be obtained at lower doses because of the large contrast differences between the bright, contrast-filled enteric lumen and surrounding soft tissue of the bowel wall. We typically perform low-dose CT enteroclysis for patients with polyposis, employing dose settings one-half those of routine CT enterography and obtaining excellent visualization of the bowel.

Imaging findings

Crohn’s disease

Small-bowel inflammation is best diagnosed using a combination of segmental mural hyper-enhancement and small-bowel wall thickening.^3,23 Segmental hyperenhancement without wall thickening is a more sensitive marker of small-bowel inflammation, but is less specific.Other findings, such as the Comb sign (engorgement of the vasa recta), fibrofatty proliferation, and stranding in the perienteric fat also indicate active inflammation.^2,33 Asymmetric and patchy hyperenhancement of the bowel wall is specific for Crohn’s disease. Fistulas appear as extra-enteric enhancing tracts, which may or may not contain fluid (Figure 5).³⁴

Obscure GI bleeding (OGIB)

Small-bowel masses and vascular lesions account for the majority of abnormalities causing OGIB. In most cases, their appearance on multiphase CTE is characteristic and allows differentiation of masses from vascular lesions. The appearance of small-bowel neoplasms is discussed below.

Angioectasias

The most common small-bowel vascular lesions causing OGIB are angioectasias—endoscopically visible lesions up to several millimeters in size consisting of dilated capillaries in the lamina propria.³⁵ The most common appearance on multiphase CTE is a round or plaque-like focal area of enhancement, brightest on the enteric phase, which fades slightly during the delayed phase. These lesions are frequently multiple and commonly occur in patients without signs of OGIB. Therefore, correlation with endoscopic findings is sometimes problematic (Figure 6).Enhancement characteristics are similar to carcinoid tumors; however, lesion size and shape will usually allow differentiation. In some cases, angioectasias may be visible during the arterial phase and can be accompanied by an early draining vein.

Small-bowel masses

The appearance of small-bowel neoplasms has been described, with each neoplasm having a spectrum of appearances.² Carcinoid tumors are typically hyperenhancing luminal polyps and masses, with characteristic mesenteric metastases (when present). GIST tumors frequently have an exoenteric component. Small-bowel lymphoma often is polypoid and may be associated with lumen dilatation with nearby lymphadenopathy, often affecting multiple points along the GI tract. Small-bowel polyps can originate from a variety of histologies and enhance variably, and can appear indistinguishable from other small-bowel filling defects, such as ectopic pancreas.

CT vs. MRI vs. other small-bowel exams

While CT and MR enterography perform similarly in identifying active Crohn’s disease and its complications, a number of variables should beconsidered when selecting the most appropriate test for any patient. Because of the improved temporal and spatial resolution of CT, we generally select CT enterography as a desired examination when there is a concern for sepsis. CT enterography is generally the first examination performed for suspected Crohn’s disease in adult patients, while MR enterography may be the first exam performed in younger patients. We prefer MR enterography when there is the question of low-grade obstruction or when the clinician desires to assess response to immunomodulator therapy in the absence of patient symptomatology.³⁶ CT is, of course, performed in patients with implantable devices or claustrophobia. MR is a feasible alternative in patients with contraindications to CT, such as renal impairment, contrast allergy, or pregnancy.

Much has been made in the popular press regarding the radiation risks of CT; however, it should be remembered that the risks of radiation forCT examination are too low to be accurately estimated.^37,38 CT enterography can detect known causes of morbidity and mortality in Crohn’s disease patients and change management decisions in approximately 50%, often because protean symptoms are usually unrelated to biologic activity. Furthermore, immunomodulator drugs are very expensive and have significant risk,³⁹ but the benefits of these drugs outweigh the risks.⁴⁰ Finally, CT enterography has been selected and judged by a panel of experts to be the most appropriate imaging test in patients with suspected Crohn’s disease.⁴¹ We generally perform MR enterography in younger patients and as a follow-up examination in asymptomatic adult patients.

The urgency for enterography examination, as well as its costs and local expertise, also affect these imaging decisions. CT is readily available in most practices, but due to the growing use of MR in small-bowel assessment, radiology practices should be encouraged to expand their MR enterography access. At our institution CT enterography costs about one-third that of MR enterography.

Small-bowel follow-through and capsule endoscopy are also important small-bowel diagnostic tests that may be more appropriate than cross-sectional enterography, depending on the clinical situation. We often perform small-bowel follow through in complex post-surgical cases, or suspected pseudo-obstruction, scleroderma, or small-bowel diverticulosis. Capsule endoscopy is a complementary test to multiphase CT enterography in patients with obscure GI bleeding, owing to its exquisite mucosal assessment. It is also useful in identifying erosions and other signs of mild Crohn’s disease after a negative CT or MR enterography, when clinical symptoms persist. Performing cross-sectional enterography prior to capsule endoscopy decreases the risk of capsule retention.^19,20

Impact on patient care

Crohn’s disease

CT and MR enterography are dramatically altering Crohn’s disease diagnostic and management algorithms. At our institution, 273 patients with suspected or established Crohn’s disease recently underwent a prospective study, in which referring gastroenterologists completed a pre-CT enterography questionnaire regarding their postmanagement plans.⁴² After reviewing imaging results, clinicians reported that CT enterography altered their management plans in 51% (54% of these were those with suspected Crohn’s disease and 48% with established Crohn’s disease). Similar findings were noted by Higgins et al, where CTE data changed the perception for the likelihood of steroid benefit in 41 of 67 Crohn’s disease cases.⁴³ These results likely reflect the uncertainty that exists, as symptoms and clinical indices, such as the Crohn’s Disease Activity Index (CDAI), have a poor correlation with endoscopic disease activity.^{44, 45} Cross-sectional imaging can provide objective measures of disease activity while also detecting occult penetrating disease and extra-luminal disease manifestations.⁴⁶ In addition, intestinal response to therapy (remodeling) can be followed on CTE or MRE,⁴⁷ suggesting the possibility of using imaging indices or end-points to tailor therapy. CT and MR enterography are becoming vital components of global disease activity and intestinal damage assessments.

Obscure GI bleeding

Capsule endoscopy has been widely accepted as the diagnostic tool of choice for the evaluation ofOGIB. However our experience, along with others, suggests a significant false-negative rate for the diagnosis of small-bowel tumors.⁴⁸ Multiphase CTE has proven to be sensitive in the detection of small-bowel masses. We believe the addition of multiphase CTE to the routine diagnostic work-up of patients with obscure GI bleeding is warranted, particularly in patients with a prior negative capsule endoscopy.

Polyposis

Many patients with polyposis syndromes develop small-bowel polyps at an early age, and patients are at risk for developing complications, such as bleeding, intussusceptions, and gastrointestinal and extraluminal malignancies. Therefore, routine surveillance of these patients is usually performed. Endoscopy is performed to detect and treat gastric, duodenal, proximal jejunal, and colonic polyps. Several techniques are available to detect small-bowel polyps, including wireless capsule endoscopy, cross-sectional enterography/enteroclysis, and balloon-assisted endoscopy. Wireless capsule endoscopy and enterography are well tolerated and can be used to detect larger polyps (1.0-1.5 cm) that may be more clinically significant and require either balloon-assisted endoscopic removal or surgery. Studies have shown that while wireless capsule endoscopy may detect smaller polyps than MR enterography, there is no significant difference in detection of larger, more clinically significant polyps. MR enterography more accurately localizes these polyps, is more reliable in size estimation, and can be used as a guide for subsequent treatment approaches.^7,49 An additional advantage of cross-sectional imaging is the ability to screen for extraluminal malignancies that can arise in Peutz-Jeghers syndrome.

Conclusion

Cross-sectional imaging is transforming the radiologic and clinical assessment of the small bowel and care of patients with small-bowel diseases. Techniques should be selected based on clinical suspicion and adapted to individual patients.

RefeRences

1. Fidler JL, Guimaraes L, Einstein DM. MR imaging of the small bowel. Radiographics. 2009;29: 1811-1825.
2. 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;26:641-657; discussion 657-662.
3. Baker ME, Walter J, Obuchowski NA, et al. Mural attenuation in normal small bowel and active inflammatory Crohn’s disease on CT enterography: Location, absolute attenuation, relative attenuation, and the effect of wall thickness. AJR Am J Roentgenol. 2009;192:417-423.
4. 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.
5. Booya F, Fletcher JG, Huprich JE, et al. Active Crohn disease: CT findings and interobserver agreement for enteric phase CT enterography. Radiology. 2006;241:787-795.
6. Siddiki HA, Fidler JL, Fletcher JG, et al. Prospective comparison of state-of-the-art MR enterography and CT enterography in small-bowel Crohn’s disease. AJR Am J Roentgenol. 2009;193:113-121.
7. Gupta A, Postgate AJ, Burling D, et al. A prospective study of MR enterography versus capsule endoscopy for the surveillance of adult patients with Peutz-Jeghers syndrome. AJR Am J Roentgenol. 2010;195:108-116.
8. Huprich JE, Fletcher JG, Alexander JA, et al. Obscure gastrointestinal bleeding: Evaluation with 64-section multiphase CT enterography--initial experience. Radiology. 2008;246:562-571.
9. Graca BM, Freire PA, Brito JB, et al. Gastroenterologic and radiologic approach to obscure gastrointestinal bleeding: How, why, and when? Radiographics. 2010;30:235-252.
10. D’Haens GR, Fedorak R, Lemann M, et al. Endpoints for clinical trials evaluating disease modification and structural damage in adults with Crohn’s disease. Inflamm Bowel Dis. 2009;15:1599-1604.
11. Singh V, Alexander JA. The evaluation and management of obscure and occult gastrointestinal bleeding. Abdom Imaging. 2009;34:311-319.
12. Young BM, Fletcher JG, Booya F, et al. Head-to-head comparison of oral contrast agents for cross-sectional enterography: Small bowel distention, timing, and side effects. J Comput Assist Tomogr. 2008;32:32-38.
13. Schindera ST, Nelson RC, DeLong DM, et al. Multi-detector row CT of the small bowel: Peak enhancement temporal window—initial experience. Radiology.2007;243:438-444.
14. Vandenbroucke F, Mortele KJ, Tatli S, et al. Noninvasive Multidetector Computed Tomography Enterography in Patients with Small-Bowel Crohn’s Disease: Is a 40-Second Delay Better than 70 Seconds? Acta Radiol. 23 2007:1-9.
15. Kambadakone AR, Prakash P, Hahn PF, Sahani DV. Low-dose CT examinations in Crohn’s disease: Impact on image quality, diagnostic performance, and radiation dose. AJR Am J Roentgenol. 2010;195:78-88.
16. Allen BC, Baker ME, Einstein DM, et al. Effect of altering automatic exposure control settings and quality reference mAs on radiation dose, image quality, and diagnostic efficacy in MDCT enterography of active inflammatory Crohn‘s disease. AJR Am J Roentgenol. 2010;195:89-100.
17. Leng S, Yu L, McCollough CH. Radiation dose reduction at CT enterography: How low can we go while preserving diagnostic accuracy? AJR Am J Roentgenol. 2010;195:76-77.
18. Hassan C, Cerro P, Zullo A, et al. Computed tomography enteroclysis in comparison with ileoscopy in patients with Crohn’s disease. Int J Colorectal Dis. 2003;18:121-125.
19. Solem CA, Loftus EV, Jr., Fletcher JG, et al. Small-bowel imaging in Crohn’s disease: A prospective, blinded, 4-way comparison trial. Gastrointest Endosc. 29 2008;68:255-266.
20. Voderholzer WA, Beinhoelzl J, Rogalla P, et al. Small bowel involvement in Crohn’s disease: A prospective comparison of wireless capsule endoscopy and computed tomography enteroclysis. Gut.2005;54:369-373.
21. Hara A, Leighton J, Sharma V, Fleischer DE. Small bowel: Preliminary comparison of capsule endoscopy with barium study and CT. Radiology. 2004;230:260-265.
22. Hara AK, Leighton JA, Heigh RI, et al. Crohn disease of the small bowel: Preliminary comparison among CT enterography, capsule endoscopy, small-bowel follow-through, and ileoscopy. Radiology. 2006;238:128-134.
23. Siddiki H, Fletcher J, Hara A, et al. Validation of a lower radiation computed tomography enterography imaging protocol to detect Crohn’s disease in the small bowel. Inflamm Bowel Dis. 2010.
24. Johnson KT, Hara AK, Johnson CD. Evaluation of colitis: Usefulness of CT enterography technique. Emerg Radiol. 2009;16:277-282.
25. Lee SS, Kim AY, Yang SK, et al. Crohn disease of the small bowel: Comparison of CT enterography, MR enterography, and small-bowel follow-through as diagnostic techniques. Radiology. 2009;251:751-761.
26. Schmidt S, Guibal A, Meuwly JY, et al. Acute Complications of Crohn’s Disease: Comparison of Multidetector-Row Computed Tomographic Enterography with Magnetic Resonance Enterography. Digestion. 2010;82:229-238.
27. Horsthuis K, Bipat S, Bennink RJ, Stoker J. Inflammatory bowel disease diagnosed with US, MR, scintigraphy, and CT: Meta-analysis of prospective studies. Radiology. 2008;247:64-79.
28. Huprich JE. Multi-phase CT enterography in obscure GI bleeding. Abdom Imaging. 2009;34: 303-309.
29. Huprich J, Fletcher J, Alexander J, et al. Obscure GI bleeding: 64 Channel Multi-phase, Multiplanar CT Enterography Has a Role (Abstract No. SSM09-06). Paper presented at: Annual Meeting of the Radiological Society of North America, 2005; Chicago, IL.
30. Gourtsoyiannis N, Papanikolaou N, Grammatikakis J, Prassopoulos P. MR enteroclysis: Technical considerations and clinical applications. Eur Radiol. 2002;12:2651-2658.
31. Masselli G, Polettini E, Casciani E, et al. Small-bowel neoplasms: Prospective evaluation of MR enteroclysis. Radiology. 2009;251:743-750.
32. Van Weyenberg SJ, Meijerink MR, Jacobs MA, et al. MR enteroclysis in the diagnosis of small-bowel neoplasms. Radiology. 2010;254:765-773.
33. Lee S, Ha H, Yang S, et al. CT of prominent pericolic or perienteric vasculature in patients with Crohn’s disease: Correlation with clinical disease activity and findings on barium studies. AJR. 2002;179:1029-1036.
34. Booya F, Akram S, Fletcher J, et al. CT enterography and fistulizing Crohn’s disease: Clinical benefit and radiographic findings. Abdom Imaging. 2009;34:467-475.
35. Yano T, Yamamoto H. Vascular, polypoid, and other lesions of the small bowel. Best Pract Res Clin Gastroenterol. 2009;23:61-74.
36. Guimaraes L, Fidler JL, Fletcher JG, et al. Assessment of appropriateness of indications for CT enterography in younger patients. Inflamm Bowel Dis. 2010;16:226-232.
37. Committee to Assess Health Risks from Exposure to Low Levels of Ionizing Radiation, National Research Council. Health Risks from Exposure to Low Levels of Ionizing Radiation: BEIR VII Phase 2. Washington, D.C.: National Academies Press; 2006.
38. McCollough CH, Guimaraes L, Fletcher JG. In defense of body CT. AJR Am J Roentgenol. 2009;193:29-39.
39. Toruner M, Loftus EV, Jr., Harmsen WS, et al. Risk factors for opportunistic infections in patients with inflammatory bowel disease. Gastroenterology. 2008;134:929-936.
40. Siegel CA, Hur C, Korzenik JR, et al. Risks and benefits of infliximab for the treatment of Crohn’s disease. Clin Gastroenterol Hepatol.2006;4:1017-1024.
41. American College of Radiology. ACR Appropriateness Criteria^®. Available at: http://www.acr.org/secondarymainmenucategories/quality_safety/app_criteria.aspx. Accessed August 11, 2010.
42. Bruining D, Siddiki H, Fletcher J, et al. Clinical benefit of CT enterography in suspected or established Crohn’s disease: Impact on patient management and physician level of confidence. Paper presented at: 109th Annual Meeting of the American Gastroenterological Association Institute, 2008; San Diego, CA.
43. Higgins PD, Caoili E, Zimmermann M, et al. Computed tomographic enterography adds information to clinical management in small bowel Crohn‘s disease. Inflamm Bowel Dis. 2007;13:262-268.
44. Jones J, Loftus EV, Jr., Panaccione R, et al. Relationships between disease activity and serum and fecal biomarkers in patients with Crohn’s disease. Clin Gastroenterol Hepatol.2008;6:1218-1224.
45. Modigliani R. Endoscopic severity index for Crohn’s disease. Gastrointest Endosc. 1990;36:637.
46. Bruining DH, Siddiki HA, Fletcher JG, et al. Prevalence of penetrating disease and extraintestinal manifestations of Crohn’s disease detected with CT enterography. Inflamm Bowel Dis. 2008;14: 1701-1706.
47. Bruining DH, Loftus E. V. J, Ehman E, et al. Intestinal wall remodeling measured with serial CT enterography in patients with Crohn’s Disease treated with infliximab. Digestive Disease Week; New Orleans, LA; 2010; Abstract 543.
48. Postgate A, Despott E, Burling D, et al. Significant small-bowel lesions detected by alternative diagnostic modalities after negative capsule endoscopy. Gastrointest Endosc. 2008;68:1209-1214.
49. Caspari R, von Falkenhausen M, Krautmacher C, et al. Comparison of capsule endoscopy and magnetic resonance imaging for the detection of polyps of the small intestine in patients with familial adenomatous polyposis or with Peutz-Jeghers‘ syndrome. Endoscopy. 2004;36:1054-1059.