The 2 main ways to avoid radiation exposure in IBD are to (1) determine if a radiographic study is necessary and (2) choose an imaging study that limits radiation exposure when possible. The most obvious way to limit radiation exposure is to limit unnecessary CT scans. The most common location for patients, including those with IBD, to get a CT scan is in the ER.45,46 The number of CT scans performed in the ER has markedly increased in the last several decades. For example, a recent study in patients with IBD found a 165% increase in CT scans in the ER over a roughly 10-year period.47 Several studies have found that patients receive repeated CT scans during their repeated ER visits with no objective benefit from these repeated exposures to ionizing radiation. A recent study in 648 patients with CD assessed in the ER showed that despite an almost doubling of CT scan use from 47% in 2001 to 78% in 2009, the rate of management altering findings (perforation, obstruction, abscess) did not differ between the 2 time periods, at 29.0% and 34.9%, respectively, nor did the rate of hospital admission.48 Another study focusing on the outcome of CT scans for abdominal pain in the ER showed a very low yield of 8.4% and 4.9% for the second and the third repeat CT scans, respectively, in a non-IBD cohort49 compared with the first CT, which had a diagnostic yield of 22.5%. These studies point to the potential overuse of CT scans in the ER and low increase in yield of CT scan findings despite a rapid increase in the number of CT scan being preformed. Indeed, a recent interesting prospective study from the University of Pennsylvania showed that by creating a simple “reminder tool” in the electronic medical record that mentioned the adverse effects of cumulative radiation from CT scanning and the low yield from repeat CT scans for abdominal pain, investigators were able to decrease the number of CT scans in the ER by 10%.50 These studies also highlighted an urgent need to establish a validated pathway to narrow the use of CT scanning in IBD during ER visits and hospital admissions.
The second way to limit DMR exposure in IBD is to choose a different radiographic examination than CT scans—magnetic resonance imaging (MRI) of abdomen, magnetic resonance enterography (MRE), or abdominal US; all of which do not expose patients with IBD to ionizing radiation. The pros and cons of these alternative radiographic imaging modalities to CT are listed in Table 3 and discussed below.
CTE has become the test of choice for accurate assessment of the small bowel in patients with CD because it not only can detect severe complications like an abscess or a fistula but it can also detect subtle mucosal lesions or a mild intestinal stricture. However, CTE exposes patients to considerable ionizing radiation. To avoid radiation exposure, similar protocols using magnetic resonance technology have been developed. MRE like CTE allows for a combination of high-resolution imaging with high-volume oral contrast agent. Cross-sectional imaging modalities available in CT and MRI have become increasingly important in diagnosing complications of IBD that often require acute intervention, such as abscesses, fistulas, or bowel perforation.51 The most significant advantage in MRI over CT is the lack of radiation exposure in MRI. Historically, MRI of the abdomen was limited by extensive motion artifact from respiration and long acquisition times.52 Consequently, the role of MRI in IBD was limited mainly to the evaluation of perianal disease in Crohn’s with a pelvic MRI as the pelvis is not subject to breathing aperistaltic motion. However, over the past decade, MRI sequencing has been dramatically improved, providing high-resolution motion-free images to better evaluate the entire bowel.53
Indeed, recent advances in magnetic resonance technology have increased its image resolution that is now comparable with CT imaging. Multiple prospective studies have demonstrated MRE to be better or at least comparable with other imaging modalities in evaluation of small bowel disease in patients with CD. Berstein et al54 compared MRE with fluoroscopic barium small bowel series in 30 subjects and found that 10 studies were normal by both modalities and 8 studies showed similar extent of CD by both tests. SBFT revealed additional information in 4, whereas MRI provided clinically relevant added information in 8, including identifying active inflammation in structured areas based on the wall enhancement patterns, lymphadenopathy, and vasa recta changes. MRE also allows dynamic evaluations of small bowel peristalsis and dispensability of areas of luminal narrowing and intraluminal masses to better assess the severity and characteristics of intestinal strictures.55 Comparison of MRI and single-phase helical CT scanning demonstrated MRI to be superior for detection of subtle bowel inflammatory changes.56 In another study, a prospective comparison of MRE and CTE showed MRE to be equally as sensitive as CTE in detecting mucosal abnormalities in CD, but MRE was even more sensitive than CTE in detecting strictures or ileal inflammation (mucosal enhancement).57 Therefore, GI imaging with MRE in IBD has significant advantage not only for assessing treatment response by the presence and severity of mucosal inflammation through abnormal enhancement patterns but also for assessing the ileum and cecum in patients difficult to reach by colonoscopy.58 Unfortunately, limitations of MRE in comparison with CT include higher cost, potentially less radiologist experience with the MRE protocols, and less geographic availability of high resolution required to do these procedures. Furthermore, long examination times and residual intraluminal air may limit the use of MRI in patients who are critically ill or those with acute and severe exacerbations of their disease.59 However, the use of MRE when it is feasible would significantly decrease the number of CT examinations and thus decrease radiation exposure in patients with IBD.
US provides another alternative modality to CT to evaluate the GI tract in IBD. Dedicated US examination of GI tract in patients with IBD is capable of identifying extraintestinal complications of IBD and assessing the extent and severity of mucosal abnormalities including the depth of mucosal involvement that could be highly useful to differentiate Crohn's colitis with transmural involvement from UC with superficial mucosal involvement.60 One study conducted by highly experience GI ultrasonographers reported that US can detect small or large bowel inflammation in patients with suspected or proven IBD in the range of 78% to 96% and 89% to 100%, respectively.61 Unfortunately, abdominal US may also provide false-negative results when the mucosal lesions are superficial or in obese patients, even in the hands of an experienced radiologist.62 The use of oral contrast agents such as iso-osmolar polyethylene glycol solution may increase sensitivity in defining disease extent, lesion site, and bowel complications of CD,63 but concerns over false negatives, operator expertise, lack of protocols in most medical centers has limited its widespread use.
Traditional SBFT with oral barium contrast historically has been the modality of choice to assess inflammatory or structural lesions in patients with suspected or documented CD. Evaluation of small bowel by barium follow-through in conjunction with fluoroscopy and manual palpation to compress the individual loops properly has been clinically accepted for patients with suspected or proven diagnosis of IBD.59 SBFT also has the benefit of being associated with small effective radiation exposure of 3 mSv.64 In Europe, small bowel enteroclysis (SBE), rather than SBFT, has been the preferred mode of evaluation of the small bowel in IBD since 1980s. SBE relies primarily on abnormalities in bowel mucosal pattern and intestinal caliber.65 It poses an advantage of detecting early mucosal pathologies of CD including aphthous ulcerations or mucosal granularity and short strictures in small bowel. However, these techniques are insensitive for detecting transmural inflammation or extraluminal complications in IBD.66 In addition, SBE in particular requires placement of a nasogastric tube, which is invasive and uncomfortable and thus highly unpopular with patients. Also, because it requires extensive fluoroscopic time, radiation exposure can be significantly higher than SBFT, and the utility of SBE is limited in centers where MRE is easily available.
Finally, capsule endoscopy (CE) has also emerged as an adjunctive tool in evaluating the small bowel and may aid in providing useful knowledge in patients with suspected CD or for assessing the extent and severity of disease.67 Evidence has suggested that findings of CE may impact the management of patients with CD. For example, normal small bowel in CE in symptomatic patients with documented CD would spare these patients from unnecessary change in their anti-inflammatory medication. Indeed, 48% of 134 symptomatic patients previously diagnosed with CD by SBFT or ileocolonoscopy had normal small bowel in CE.68 In contrast, 52% of the patients with CD were found to have significant small bowel ulcerations in their CE that led to a change in treatment. Furthermore, a meta-analysis found that CE had higher sensitivity for detecting small bowel lesions than small bowel radiography, CTE, or colonoscopy with ileoscopy when it was used in the evaluation of suspected or established patients with CD.69 A recent study found that CE detected small bowel lesions in 24% of the patients with CD with perianal disease (e.g., abscesses, fistulas, recurrent fissures) who had normal SBFT on ileoscopy, SBFT, or CTE/MRE.70 There are several important limitations for the use of CE. These include a lack of accessibility and the risk of capsule retention in a stricture, a risk that is increased in patients with IBD.71
The risk of DMR brings several challenging ethical issues regarding informed consent. Patients should be informed of risks and benefits of all the tests they receive including a CT scan. First, the risks of DMR should be discussed with the patient. Second, clinicians should include the patient in the decision making regarding the choice of radiological imaging when appropriate. Although this is a controversial issue due to a concern that patients will misinterpret the actual risk and refuse needed imaging, a recent editorial in JAMA has highlighted several key points in regards to this issue.72 The intent of informed consent is clear that adequate information about any test that a reasonable person would want to know should be provided to the patient before it being performed. This requires that all risks and benefits of diagnostic medical imaging are outlined and alternatives are discussed. The lack of informed consent in diagnostic imaging is highlighted by the findings of a recent cross-sectional study in patients in the ER for abdominal pain that found that 70% of patients underestimated the radiation exposure delivered by one CT scan, and 39% of the patients who reported having no previous CT imaging had had a CT examination in the past when their medical records were reviewed.73 Currently, informed consent is not necessary to obtain a CT scan, but informing patients about the risks of DMR is important for clinicians to consider in the future.
Patients with IBD, particularly CD, are at increased risk of high cumulative doses of DMR. Young age is the greatest risk factor for the development of a malignancy from ionizing radiation; therefore, patients diagnosed at a young age with IBD, who often have a more aggressive disease course, are at the greatest risk of a future malignancy from radiation exposure. Other identifiable risk factors for high radiation exposure in IBD include the use of immunomodulators, use of biologics, or a history of multiple surgeries. The exact risk of malignancy from high exposure to DMR remains controversial, based on the available data ranges from very high to very low. However, some increased risk of malignancy is present, and given this risk, alternative forms of imaging such as MRE, US, or CE should be considered in patients with IBD. Establishing a validated pathway to narrow the use of CT scanning during hospitalization or visits to the ER is needed in patients with IBD. In the meantime, physicians need to carefully consider the risks and benefits of a CT scan, particularly when evaluating a young patient with CD who has identifiable risk factors for an aggressive disease course.
1. van Assche G, Vermeire S, Rutgeerts P. Mucosal healing and anti TNFs in IBD. Curr Drug Targets. 2010;11:227–233.
2. Reinisch W, Wang Y, Oddens BJ, et al.. C-reactive protein, an indicator for maintained response or remission to infliximab in patients with Crohn's disease: a post-hoc analysis from ACCENT I. Aliment Pharmacol Ther. 2012;35:568–576.
3. D'Inca R, Dal Pont E, Di Leo V, et al.. Can calprotectin predict relapse risk in inflammatory bowel disease? Am J Gastroenterol. 2008;103:2007–2014.
4. Modigliani R, Mary JY, Simon JF, et al.. Clinical, biological, and endoscopic picture of attacks of crohn's disease. Evolution on prednisolone. groupe d'etude therapeutique des affections inflammatoires digestives. Gastroenterology. 1990;98:811–818.
5. Brenner D, Hall E. Computed tomography—an increasing source of radiation exposure. New Engl J Med. 2007;357:2227–2283.
6. Jess T, Frisch M, Simonsen J. Trends in overall and cause-specific mortality among patients with inflammatory bowel disease from 1982 to 2010. Clin Gastroenterol Hepatol. 2013;11:43–48.
7. Jess T, Gamborg M, Matzen P, et al.. Increased risk of intestinal cancer in Crohn's disease: a meta-analysis of population-based cohort studies. Am J Gastroenterol. 2005;100:2724–2729.
8. Kleinerman RA. Cancer risks following diagnostic and therapeutic radiation exposure in children. Pediatr Radiol. 2006;36(suppl 2):121–125.
9. Berrington de Gonzalez A, Mahesh M, Kim KP, et al.. Projected cancer risks from computed tomographic scans performed in the united states in 2007. Arch Intern Med. 2009;169:2071–2077.
10. Newnham E, Hawkes E, Surender A, et al.. Quantifying exposure to diagnostic medical radiation in patients with inflammatory bowel disease: are we contributing to malignancy? Aliment Pharmacol Ther. 2007;26:1019–1024.
11. Martin CJ. Effective dose: how should it be applied to medical exposures? Br J Radiol. 2007;80:639–647.
12. Mettler FA Jr, Bhargavan M, Faulkner K, et al.. Radiologic and nuclear medicine studies in the united states and worldwide: frequency, radiation dose, and comparison with other radiation sources–1950-2007. Radiology. 2009;253:520–531.
13. Smith-Bindman R, Lipson J, Marcus R, et al.. Radiation dose associated with common computed tomography examinations and the associated lifetime attributable risk of cancer. Arch Intern Med. 2009;169:2078–2086.
14. Kalra MK, Maher MM, Toth TL, et al.. Strategies for CT radiation dose optimization. Radiology. 2004;230:619–628.
15. Prakash P, Kalra MK, Kambadakone AK, et al.. Reducing abdominal CT radiation dose with adaptive statistical iterative reconstruction technique. Invest Radiol. 2010;45:202–210.
16. Mettler FA Jr, Huda W, Yoshizumi TT, et al.. Effective doses in radiology and diagnostic nuclear medicine: a catalog. Radiology. 2008;248:254–263.
17. Ohana M, Mima A, Sonoyama H, et al.. CT enterography with polyethylene glycol electrolyte solution for diagnosis of crohn's disease. Nihon Shokakibyo Gakkai Zasshi. 2012;109:910–920.
18. Jensen MD, Kjeldsen J, Rafaelsen SR, et al.. Diagnostic accuracies of MR enterography and CT enterography in symptomatic Crohn's disease. Scand J Gastroenterol. 2011;46:1449–1457.
19. Bruining DH, Loftus EV Jr, Ehman EC, et al.. Computed tomography enterography detects intestinal wall changes and effects of treatment in patients with crohn's disease. Clin Gastroenterol Hepatol. 2011;9:679–683.e1.
20. Kambadakone AR, Prakash P, Hahn PF, et al.. 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.
21. 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.
22. Brenner DJ, Doll R, Goodhead DT, et al.. Cancer risks attributable to low doses of ionizing radiation: assessing what we really know. Proc Natl Acad Sci U S A. 2003;100:13761–13766.
23. Hall EJ, Brenner DJ. Cancer risks from diagnostic radiology: the impact of new epidemiological data. Br J Radiol. 2012;85:e1316–1317.
24. Koenig TR, Wolff D, Mettler FA, et al.. Skin injuries from fluoroscopically guided procedures: part 1, characteristics of radiation injury. AJR Am J Roentgenol. 2001;177:3–11.
25. O'Neill SB, O'Connor OJ, McWilliams SR, et al.. Minimization of radiation exposure due to computed tomography in inflammatory bowel disease. Clin Res Hepatol Gastroenterol. 2011;35:105–110.
26. Cardis E, Vrijheid M, Blettner M, et al.. The 15-country collaborative study of cancer risk among radiation workers in the nuclear industry: estimates of radiation-related cancer risks. Radiat Res. 2007;167:396–416.
27. Preston DL, Pierce DA, Shimizu Y, et al.. Effect of recent changes in atomic bomb survivor dosimetry on cancer mortality risk estimates. Radiat Res. 2004;162:377–389.
28. van Gent DC, Hoeijmakers JH, Kanaar R. Chromosomal stability and the DNA double-stranded break connection. Nat Rev Genet. 2001;2:196–206.
29. Pearce MS, Salotti JA, Little MP, et al.. Radiation exposure from CT scans in childhood and subsequent risk of leukaemia and brain tumours: a retrospective cohort study. Lancet. 2012;380:499–505.
30. Loftus EV Jr, Silverstein MD, Sandborn WJ, et al.. Crohn's disease in Olmsted County, Minnesota, 1940-1993: incidence, prevalence, and survival. Gastroenterology. 1998;114:1161–1168.
31. Loftus EV Jr. Clinical epidemiology of inflammatory bowel disease: incidence, prevalence, and environmental influences. Gastroenterology. 2004;126:1504–1517.
32. Kandiel A, Fraser AG, Korelitz BI, et al.. Increased risk of lymphoma among inflammatory bowel disease patients treated with azathioprine and 6-mercaptopurine. Gut. 2005;54:1121–1125.
33. Bongartz T, Sutton AJ, Sweeting MJ, et al.. Anti-TNF antibody therapy in rheumatoid arthritis and the risk of serious infections and malignancies: systematic review and meta-analysis of rare harmful effects in randomized controlled trials. JAMA. 2006;295:2275–2285.
34. Desmond AN, O'Regan K, Curran C, et al.. Crohn's disease: factors associated with exposure to high levels of diagnostic radiation. Gut. 2008;57:1524–1529.
35. Peloquin JM, Pardi DS, Sandborn WJ, et al.. Diagnostic ionizing radiation exposure in a population-based cohort of patients with inflammatory bowel disease. Am J Gastroenterol. 2008;103:2015–2022.
36. Levi Z, Fraser E, Krongrad R, et al.. Factors associated with radiation exposure in patients with inflammatory bowel disease. Aliment Pharmacol Ther. 2009;30:1128–1136.
37. Palmer L, Herfarth H, Porter CQ, et al.. Diagnostic ionizing radiation exposure in a population-based sample of children with inflammatory bowel diseases. Am J Gastroenterol. 2009;104:2816–2823.
38. Kroeker KI, Lam S, Birchall I, et al.. Patients with IBD are exposed to high levels of ionizing radiation through CT scan diagnostic imaging: a five-year study. J Clin Gastroenterol. 2011;45:34–39.
39. Fuchs Y, Markowitz J, Weinstein T, et al.. Pediatric inflammatory bowel disease and imaging-related radiation: are we increasing the likelihood of malignancy? J Pediatr Gastroenterol Nutr. 2011;52:280–285.
40. Sauer CG, Kugathasan S, Martin DR, et al.. Medical radiation exposure in children with inflammatory bowel disease estimates high cumulative doses. Inflamm Bowel Dis. 2011;17:2326–2332.
41. Aithal GP, Mansfield JC. Review article: the risk of lymphoma associated with inflammatory bowel disease and immunosuppressive treatment. Aliment Pharmacol Ther. 2001;15:1101–1108.
42. Bebb JR, Aithal GP, Logan RP. Immunosuppression, IBD, and risk of lymphoma. Gut. 2002;51:296.
43. Krewski D, Zielinski JM, Hazelton WD, et al.. The use of biologically based cancer risk models in radiation epidemiology. Radiat Prot Dosimetry. 2003;104:367–376.
44. Chatu S, Subramanian V, Pollok RC. Meta-analysis: diagnostic medical radiation exposure in inflammatory bowel disease. Aliment Pharmacol Ther. 2012;35:529–539.
45. Pines JM. Trends in the rates of radiography use and important diagnoses in emergency department patients with abdominal pain. Med Care. 2009;47:782–786.
46. Kocher KE, Meurer WJ, Fazel R, et al.. National trends in use of computed tomography in the emergency department. Ann Emerg Med. 2011;58:452–462.e3.
47. Ananthakrishnan AN, McGinley EL, Saeian K, et al.. Trends in ambulatory and emergency room visits for inflammatory bowel diseases in the United States: 1994-2005. Am J Gastroenterol. 2010;105:363–370.
48. Kerner C, Carey K, Mills AM, et al.. Use of abdominopelvic computed tomography in emergency departments and rates of urgent diagnoses in Crohn's disease. Clin Gastroenterol Hepatol. 2012;10:52–57.
49. Nojkov B, Duffy MC, Cappell MS. Utility of repeated abdominal CT scans after prior negative CT scans in patients presenting to ER with nontraumatic abdominal pain. Dig Dis Sci. 2013;58:1074–1083.
50. Mills AM, Holena DN, Kerner C, et al.. Electronic accountability tools reduce CT overutilization in ED patients with abdominal pain. Acad Emerg Med. 2012;19:S205.
51. Baumgart DC, Sandborn WJ. Inflammatory bowel disease: clinical aspects and established and evolving therapies. Lancet. 2007;369:1641–1657.
52. Gee MS, Harisinghani MG. MRI in patients with inflammatory bowel disease. J Magn Reson Imaging. 2011;33:527–534.
53. Furukawa A, Saotome T, Yamasaki M, et al.. Cross-sectional imaging in Crohn disease. Radiographics. 2004;24:689–702.
54. Bernstein CN, Greenberg H, Boult I, et al.. A prospective comparison study of MRI versus small bowel follow-through in recurrent Crohn's disease. Am J Gastroenterol. 2005;100:2493–2502.
55. Amzallag-Bellenger E, Oudjit A, Ruiz A, et al.. Effectiveness of MR enterography for the assessment of small-bowel diseases beyond Crohn disease. Radiographics. 2012;32:1423–1444.
56. Low RN, Francis IR, Politoske D, et al.. Crohn's disease evaluation: comparison of contrast-enhanced MR imaging and single-phase helical CT scanning. J Magn Reson Imaging. 2000;11:127–135.
57. Fiorino G, Bonifacio C, Peyrin-Biroulet L, et al.. Prospective comparison of computed tomography enterography and magnetic resonance enterography for assessment of disease activity and complications in ileocolonic Crohn's disease. Inflamm Bowel Dis. 2011;17:1073–1080.
58. Mc Laughlin PD, O'Connor OJ, O'Neill SB, et al.. Minimization of radiation exposure due to computed tomography in inflammatory bowel disease. ISRN Gastroenterol. 2012;2012:790279.
59. Herfarth H, Palmer L. Risk of radiation and choice of imaging. Dig Dis. 2009;27:278–284.
60. Strobel D, Goertz RS, Bernatik T. Diagnostics in inflammatory bowel disease: ultrasound. World J Gastroenterol. 2011;17:3192–3197.
61. Horsthuis K, Bipat S, Bennink RJ, et al.. Inflammatory bowel disease diagnosed with US, MR, scintigraphy, and CT: meta-analysis of prospective studies. Radiology. 2008;247:64–79.
62. Maconi G, Parente F, Bollani S, et al.. Abdominal ultrasound in the assessment of extent and activity of Crohn's disease: clinical significance and implication of bowel wall thickening. Am J Gastroenterol. 1996;91:1604–1609.
63. Calabrese E, Zorzi F, Pallone F. Ultrasound of the small bowel in Crohn's disease. Int J Inflam. 2012;2012:964720.
64. Giles E, Hanci O, McLean A, et al.. Optimal assessment of paediatric IBD with MRI and barium follow-through. J Pediatr Gastroenterol Nutr. 2012;54:758–762.
65. Carucci LR, Levine MS. Radiographic imaging of inflammatory bowel disease. Gastroenterol Clin North Am. 2002;31:93–117, ix.
66. Holzknecht N, Helmberger T, von Ritter C, et al.. MRI of the small intestine with rapid MRI sequences in Crohn disease after enteroclysis with oral iron particles. Radiologe. 1998;38:29–36.
67. Lewis BS. Expanding role of capsule endoscopy in inflammatory bowel disease. World J Gastroenterol. 2008;14:4137–4141.
68. Mehdizadeh S, Chen GC, Barkodar L, et al.. Capsule endoscopy in patients with Crohn's disease: diagnostic yield and safety. Gastrointest Endosc. 2010;71:121–127.
69. Dionisio PM, Gurudu SR, Leighton JA, et al.. Capsule endoscopy has a significantly higher diagnostic yield in patients with suspected and established small-bowel Crohn's disease: a meta-analysis. Am J Gastroenterol. 2010;105:1240–1248; quiz 1249.
70. Adler SN, Yoav M, Eitan S, et al.. Does capsule endoscopy have an added value in patients with perianal disease and a negative work up for Crohn's disease? World J Gastrointest Endosc. 2012;4:185–188.
71. Triester SL, Leighton JA, Leontiadis GI, et al.. A meta-analysis of the yield of capsule endoscopy compared to other diagnostic modalities in patients with non-stricturing small bowel Crohn's disease. Am J Gastroenterol. 2006;101:954–964.
72. Baerlocher MO, Detsky AS. Discussing radiation risks associated with CT scans with patients. JAMA. 2010;304:2170–2171.
73. Baumann BM, Chen EH, Mills AM, et al.. Patient perceptions of computed tomographic imaging and their understanding of radiation risk and exposure. Ann Emerg Med. 2011;58:1–7.e2.