Radiation Exposure From Diagnostic Imaging Among Patients With Gastrointestinal Disorders

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1 CLINICAL GASTROENTEROLOGY AND HEPATOLOGY 2012;10: Radiation Exposure From Diagnostic Imaging Among Patients With Gastrointestinal Disorders ALAN N. DESMOND, SEBASTIAN MCWILLIAMS, MICHAEL M. MAHER, FERGUS SHANAHAN, and EAMONN M. QUIGLEY Departments of Gastroenterology and Radiology, Cork University Hospital, Cork; Alimentary Pharmabiotic Centre, University College Cork, National University of Ireland, Cork, Ireland This article has an accompanying continuing medical education activity on page e30. Learning Objectives At the end of this activity, the learner should cite the types of gastrointestinal disorders that are associated with high levels of diagnostic radiation exposure. See editorial on page 216. BACKGROUND & AIMS: There are concerns about levels of radiation exposure among patients who undergo diagnostic imaging for inflammatory bowel disease (IBD), compared with other gastrointestinal (GI) disorders. We quantified imaging studies and estimated the cumulative effective dose (CED) of radiation received by patients with organic and functional GI disorders. We also identified factors and diagnoses associated with high CEDs. METHODS: We analyzed data from 2590 patients who were diagnosed with GI disorders at a tertiary gastroenterology center from January 1999 January 2009 on the basis of International Statistical Classification of Diseases and Health-related Problems, 10th revision and Rome III criteria. High annual CED and high total CED were defined as figures exceeding the 90th percentile for the population. RE- SULTS: Diagnostic imaging was performed on 57% of the patients (1429 of 2509). High annual CEDs ( 9.6 millisieverts/ annum) were independently associated with Crohn s disease (odds ratio [OR], 5.3; P.0001), organic small bowel disease (OR, 2.6; P.005), and functional disorders of childhood and adolescence (OR, 9.8; P.005). High total CEDs ( 30.8 millisieverts) were independently associated with Crohn s disease (OR, 81.9; P.0001), ulcerative colitis (OR, 19.0; P.0001), indeterminate colitis (OR, 7.5; P.0005), and the following non-ibd diagnoses: organic small bowel disorders (OR, 12.5; P.0001), organic hepatic disorders (OR, 3.6; P.01), and functional disorders of childhood and adolescence (OR, 13.8; P.02). CONCLUSIONS: Higher levels of annual and total diagnostic radiation exposure are associated with IBD and with other organic and functional GI disorders. Evidence-based guidelines for image analysis of patients with organic and functional gastrointestinal disorders, especially those that reduce radiation exposure, are needed. Keywords: Cancer Risk; Test; Abdominal; Computed Tomography; CT Scan; Diagnosis. Access to high-quality imaging facilities and the advent of rapid-acquisition computed tomography (CT) have made CT imaging of the gastrointestinal (GI) tract a valuable and widely used clinical investigation. However, because CT uses higher levels of ionizing radiation than other imaging modalities, 1 more widespread use has led to increases in the amount of diagnostic radiation to which patients are exposed. 2 This is a cause for concern, because protracted exposure to low levels of ionizing radiation might be associated with increased lifetime risk of malignancy Several groups, including ours, have identified risk factors for increased diagnostic radiation exposure in patients with inflammatory bowel disease (IBD) However, the use of diagnostic radiation across a broad range of organic and functional GI disorders has not been subjected to rigorous study. Therefore, the aims of this study were (1) to examine the use of diagnostic imaging in a large cohort of patients referred to a tertiary gastroenterology center with special interests in IBD and functional GI disorders between January 1, 1999, and January 1, 2009; (2) to estimate the cumulative effective dose (CED) of diagnostic radiation received by patients with IBD, other organic GI disorders, and functional GI disorders; and (3) to identify risk factors that place patients with GI disorders at risk of increased total CED. Methods Patient Population All patients who attended gastroenterology clinics at a tertiary center with special interests in IBD and functional GI disorders from January 1, 1999 January 1, 2009 were identified from the center s prospectively maintained electronic patient database. Patients with at least 4 weeks of follow-up were included. Clinical and demographic data were obtained by retrospective chart review. Patients diagnosed with a malignancy were excluded. All IBD diagnoses and organic GI diagnoses were coded according to International Statistical Classification of Diseases and Health-related Problems, 10th revision. 14 All functional GI diagnoses were classified according to the Rome III criteria. 15 In total, 38.1% of the study cohort (957 of 2509) had IBD, 40.6% (1019 of 2509) had non-ibd organic GI disorders, 25.1% (629 of 2509) had functional GI disorders, and 6.5% (163 Abbreviations used in this paper: CED, cumulative effective dose; CI, confidence interval; CT, computed tomography; GI, gastrointestinal; IBD, inflammatory bowel disease; msv, millisievert; OR, odds ratio by the AGA Institute /$36.00 doi: /j.cgh

2 260 DESMOND ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 10, No. 3 Table 1. Radiation Dose for Common Imaging Studies Imaging study Effective dose of radiation (msv) Equivalent no. of chest radiographs (n) Equivalent years of background radiation (n) Chest radiograph Abdominal radiograph Barium swallow Barium follow-through Barium enema Endoscopic retrograde cholangiopancreatogram CT, head CT, abdomen CT, pelvis CT, virtual colonoscopy CT, pulmonary angiogram of 2509) were not diagnosed with a GI disorder. More than one GI diagnosis was made in 10.3% of patients (259 of 2509). Diagnostic Imaging and Radiation Exposure The patient database was cross-referenced with the centralized electronic archive of the department of radiology to identify all imaging studies performed during January 1, 1999 January 1, Each imaging study was assigned an effective dose based on the average effective doses for diagnostic imaging studies published by the Radiological Society of North America 1 (Table 1) and classified by modality as CT, barium, ultrasound, plain radiograph, or other (nuclear imaging, angiography, interventional procedures, etc). CED was calculated for each patient on the basis of diagnostic imaging performed within 6 months before referral, during clinical follow-up, and within 6 months subsequent to most recent review. All imaging studies performed were included, both abdominal and nonabdominal. Data Compilation and Statistical Analysis Data compilation was performed by using Microsoft Access 2007 (Microsoft Corporation, Redmond, WA). Statistical analyses were performed by using GraphPad Prism version 5.01, GraphPad Stata version 3.1 (GraphPad Software Incorporated, San Diego, CA) and SPSS version 15 (SPSS Inc, Chicago, IL). The difference in mean number of imaging studies and diagnostic radiation exposure between patient groups was analyzed by using the Mann Whitney U test and Kruskal Wallis test, as appropriate. Univariate linear regression was used to examine the correlation between patient age at referral and duration of follow-up with number of imaging studies performed, annual CED, and total CED. High total CED and high annual CED were defined as values exceeding the 90th percentile for the entire patient population. The likelihoods of undergoing diagnostic imaging and of receiving high annual or high total CED according to patient characteristics were calculated by multivariate binary logistic regression analyses that included the following variables for each patient: gender, age at referral, duration of follow-up, and GI diagnoses. Likelihoods were expressed as odds ratios (ORs), with P values of less than.05 deemed to be significant. Results Patient Population A total of 2840 patients attended between January 1, 1999, and January 1, Patients with follow-up of less than 4 weeks duration (n 305) and patients with a malignancy (n 26) were excluded. The remaining 2509 patients comprised the study cohort (1066 men and 1443 women; mean age at referral, 39.8 years; age range, years; mean follow-up, 2.6 years; range, 4 weeks 10 years). Pediatric patients (aged less than 16 years at referral) accounted for 4.7% (118 of 2509) of the study cohort. Patients with attendance of less than 6 months and of 6- to 12-month duration accounted for 31.6% (793 of 2509) and 14.9% (375 of 2509) of the study cohort, respectively. Complete clinical and radiologic data were available in all cases. Sources of referral were as follows: primary care, 73.9% (1855 of 2509); hospital-based physician, 16.8% (422 of 2509); hospital-based surgeon, 8.3% (208 of 2509); and other, 1% (24 of 2509). At the conclusion of the study period, 881 patients (35.1%) remained under active follow-up, 1625 patients (64.8%) had been discharged, and 3 patients (0.1%) were deceased. Overall, 57% (1429 of 2509) of patients underwent diagnostic imaging. A total of 10,038 imaging studies were performed. The mean number of imaging studies performed per patient was 4 (range, 0 115). Abdominal imaging accounted for 48.3% (4848 of 10,038) of all studies performed. The number of imaging studies performed did not vary with gender (P.54) or correlate with age at referral (r 0.03, P.16) but did show a positive correlation with duration of follow-up (r 0.38, P.0001). Factors independently associated with the likelihood of undergoing diagnostic imaging are shown in Table 2. Diagnostic imaging was more likely in patients who were older at referral (OR, 1.1 per 10 years increased age; P.001) and patients with longer duration of follow-up (OR, 1.1 per year of follow-up; P.0005). All IBD diagnoses were independently associated with an increased likelihood of undergoing imaging, as were hepatic disorders (OR, 2.3; P.0005), functional gastroduodenal disorders (OR, 1.8; P.02), functional bowel disorders (OR, 1.2; P.04), and functional disorders of childhood and adolescence (OR, 10.2; P.03). Increased Use of Imaging During the study period, there was increased use of imaging studies in all modalities (Figure 1A). The number of CTs scans performed per 100 patients increased significantly from 10 studies in to 18.6 studies in (P.005, Mann Whitney U test). Patients who attended in the final year of the study period were significantly more likely to undergo diagnostic imaging than patients who attended in the

3 March 2012 RADIATION EXPOSURE FROM DIAGNOSTIC IMAGING 261 Table 2. Multivariate Analysis: OR of Undergoing Diagnostic Imaging According to Patient Age, Gender, Duration of Follow-up, and GI Diagnosis OR 95% CI P value Age at referral a Male gender Duration of follow-up b IBD Crohn s disease Ulcerative colitis Indeterminate colitis Organic GI disorders Esophageal Gastroduodenal Small bowel Pancreatobiliary Colorectal Hepatic GI infection Miscellaneous organic disorders Functional GI disorders Functional esophageal Functional gastroduodenal Functional bowel disorder Functional disorders of childhood and adolescence Miscellaneous functional disorders NOTE. N 2509 patients (259 patients 1 diagnosis, 163 patients with no diagnosis). a OR per 10 years increased age. b OR per year of follow-up. first year of the study period (OR, 2.2; 95% confidence interval [CI], ; P.0001). Annual Radiation Exposure Between 1999 and 2009, there were significant increases in the amount of diagnostic radiation received by patients annually (Figure 1B). Mean annual radiation exposure increased from 2.2 millisieverts (msv)/annum in , to 3.1 msv/ annum in (P.0005). The greatest increase was seen in exposure from CT imaging, from 0.9 msv/annum to 1.8 msv/annum. Annual diagnostic radiation exposure exceeded likely background radiation exposure from natural sources in 54.5% of patients (779 of 1429) who underwent imaging (background radiation exposure is approximately 2.9 msv/annum in the United States and Europe 3 ). Mean annual CED was significantly higher in patients with IBD than in patients with organic GI disorders or functional GI disorders (mean annual CED, 4.9 msv/annum, 3.1 msv/annum, and 3.1 msv/annum, respectively; P.0001; Table 3). The 90th percentile for annual CED was 9.6 msv/annum. On multivariate analysis (Table 4), annual CED exceeding this figure was independently associated with the following diagnoses: Crohn s disease (OR, 5.3; P.0001), organic small bowel disease (OR, 2.6; P.005), functional GI disorders of childhood and adolescence (OR, 9.8; P.04), and miscellaneous functional GI disorders (OR, 2.5; P.05). The 251 patients with high annual exposure comprised patients with the following diagnoses: Crohn s disease, n 107 (42.6%); ulcerative colitis, n 34 (13.5%); indeterminate colitis, n 5 (2.0%); organic GI disorders, n 46 (18.3%); functional GI disorders, n 17 (6.8%); coexisting organic and functional GI disorders, n 28 (11.2%); and no GI disorders, n 14 (5.6%). The male-to-female ratio in this high annual exposure group was 107:144, and the mean age at conclusion of follow-up was 43.5 years (range, years). High annual exposure occurred in 13.4% of patients (45 of 335) with functional GI disorders who underwent imaging. Cumulative Radiation Exposure Mean cumulative radiation exposure per patient was 10.4 msv (95% CI, msv; range, msv). Cumulative exposures exceeding 50 msv occurred in 9.7% of patients (138 of 1429) who underwent diagnostic imaging and exceeded 100 msv in 25.4% of these cases (35 of 138) (Figure 2). Abdominal imaging accounted for 48.3% of studies (4844 of 10,038) Figure 1. (A) Annual number of imaging studies performed per 100 patients; (B) annual diagnostic radiation exposure per patient, N 2509 patients.

4 262 DESMOND ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 10, No. 3 Table 3. Annual and Total CED of Diagnostic Radiation According to GI Diagnosis Annual CED (msv/annum) Total CED (msv) GI diagnosis Patients (n) Mean 95% CI Mean 95% CI IBD Crohn s disease Ulcerative colitis Indeterminate colitis Organic GI disorders Esophageal Gastroduodenal Small bowel Pancreatobiliary Colorectal Hepatic GI infection Miscellaneous organic disorders Functional GI disorders Functional esophageal Functional gastroduodenal Functional bowel disorder Functional disorders of childhood and adolescence Miscellaneous functional disorders No GI diagnosis All patients 2509 a NOTE. Total of 10,038 imaging studies performed during study period (January 1999 January 2009). a 259 patients with 1 diagnosis. and 84.1% of radiation (21,884 of 26,027 msv). Abdominal CT alone accounted for 11.5% of studies (1157 of 10,038) and 50.6% of radiation (13,178 of 26,027 msv). Total CED was higher in patients with IBD (mean total CED, 20.5 msv) than in all other diagnostic groups (P.0001). Total CED was significantly higher in patients with Crohn s disease than in patients with ulcerative colitis or indeterminate colitis (mean total CED, 30.1 msv vs 11.7 msv and 10.7 msv, respectively; P.0001; Table 3). The 90th percentile for total radiation exposure was 30.8 msv. Exposure exceeding this figure was associated with increased age at referral (OR, 1.1 per 10 years; P.02) and increased duration of follow-up (OR, 1.1 per year; P.0001). High total CED was also independently associated with a diagnosis of Crohn s disease (OR, 81.9; P.0001), ulcerative colitis (OR, 19.0; P.0001), or indeterminate colitis (OR, 7.5; P.0005), and with the following non-ibd diagnoses: organic small bowel disorders (OR, 12.5; P.0001), hepatic disorders (OR, 3.6; P.01), miscellaneous organic disorders (OR, 2.7; P.01), and functional GI disorders of childhood and adolescence (OR, 13.8; P.02). The majority of patients with CED exceeding the 90th percentile consisted of patients with IBD: Crohn s disease (63.7%, 160 of 251), ulcerative colitis (21.5%, 54 of 251), and indeterminate colitis (2.0%, 5 of 251), but this group also included patients from all other diagnostic groups: organic GI disorders (7.2%, 18 of 251), functional GI disorders (0.8%, 2 of 251), coexisting organic and functional GI disorders (4.4%, 11 of 251), and no GI disorders (0.4%, 1 of 251). Patients in this high total exposure group had a mean age of 44.0 years at conclusion of follow-up (range, years) and a male-to-female ratio of 109:142. More than half of patients in this group were younger than 35 years of age at last clinical contact (51.4%, 129 of 251; 55 men and 75 women). High total CED occurred in 3.9% of patients (13 of 335) with functional GI disorders who underwent imaging. Of the 251 patients with high total exposure, 135 were also in the high annual exposure group. There was a positive correlation between duration of follow-up and cumulative radiation exposure (r %, P.0001). Mean cumulative exposures in patients who attended for less than 6 months (mean CED, 2.3 msv; range, 0 67 msv) and patients who attended for 6 12 months (mean CED, 4.6 msv; range, msv) were significantly lower than in patients with attendance exceeding 1 year (mean CED, 16.8 msv; range, msv) (P.0001). Patients who attended for less than 1 year accounted for 6.4% of patients (16 of 251) in the high total exposure group. Discussion This study quantifies the use of diagnostic imaging in a large patient cohort encompassing a broad range of organic and functional gastrointestinal disorders. The results show that significant increases in radiation exposure in the last decade have paralleled the increased use of CT imaging. While cumulative exposure is highest in patients with Crohn s disease, high cumulative exposure may also occur in patients with other organic and functional gastrointestinal disorders. Large epidemiologic studies of populations of atomic bomb survivors and workers in the nuclear industry indicate that radiation exposure might be associated with increased incidence of solid cancers and leukemias, and that the risk increases with cumulative exposure in a linear fashion. 4 6 Most subjects in the study population received cumulative exposures of less than 30 msv. The health risks posed by exposures at this low level remain a subject of debate. However, many experts agree

5 March 2012 RADIATION EXPOSURE FROM DIAGNOSTIC IMAGING 263 Table 4. Multivariate Analysis: OR of High Annual CED and High Total CED According to Patient Age, Gender, Duration of Follow-up, and GI Diagnosis High annual CED ( 9.6 msv/annum) High total CED ( 30.8 msv) OR 95% CI P value OR 95% CI P value Age at referral a Male gender Duration of follow-up b IBD Crohn s disease Ulcerative colitis Indeterminate colitis Organic GI disorders Esophageal Gastroduodenal Small bowel Pancreatobiliary Colorectal Hepatic GI infection Miscellaneous organic disorders Functional GI disorders Functional esophageal Functional gastroduodenal Functional bowel disorder Functional disorders of childhood and adolescence Miscellaneous functional disorders NOTE. N 2509 patients (259 patients 1 diagnosis). a OR per 10 years increased age. b OR per year of follow-up. that cumulative radiation exposures exceeding msv might have the potential to result in harm. Cumulative exposures of this magnitude were not uncommon in the study cohort, occurring in almost 10% of subjects who underwent imaging. The most concerning finding might be that more than half of patients with cumulative exposure exceeding the 90th percentile were younger than 35 years old at last clinical contact. On the basis of US National Academy of Science estimates 3 and individual patient cumulative exposures, the lifetime excess relative risk of developing malignancy in the subgroup of patients with cumulative exposures exceeding the 90th percentile Figure 2. CED of diagnostic radiation received by patients. would be between 1% and 8.6% for the men and between 1.8% and 14.8% for the women. It is also noteworthy that the majority of patients in the high cumulative exposure group had IBD, a condition that is known to confer an increased lifetime risk of developing GI malignancy. 16,17 The clinical benefits of widely available diagnostic imaging of the GI tract are not in doubt. This is particularly true for patients with disorders such as Crohn s disease, who often require abdominal imaging to establish the extent of their disease and to detect extramural complications. The use of diagnostic imaging in functional GI disorders has not been subjected to rigorous study, and the benefits in this population are not as immediately evident. The functional GI disorders are clearly defined by clinical criteria, but diagnostic uncertainty and the associated fear of missing something might tempt gastroenterologists to perform imaging in patients with symptoms entirely consistent with a functional diagnosis. Although systematic reviews have emphasized the low diagnostic yield of this practice, there are few data on the frequency with which this approach is implemented or on the radiation exposure that it incurs. The results of this study show that almost half of patients with functional disorders alone underwent diagnostic imaging, and a minority had annual exposures exceeding the 90th percentile for the entire study population. Although this study confirms increased use of diagnostic imaging in the last decade, the findings also demonstrate that more than 40% of patients attending a tertiary gastroenterology center did not undergo diagnostic imaging. In the majority of patients (1730 of 2509, 66.9%) annual CED

6 264 DESMOND ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 10, No. 3 because of diagnostic imaging did not exceed annual background radiation exposure from natural sources. Although clinicians have a poor knowledge of the radiation doses associated with common imaging studies, 21,22 the concept of keeping diagnostic radiation exposure to a minimum is a well-established principle of medical radiography. 23,24 This is particularly true when dealing with younger patients, whose longer life expectancy magnifies the potentially deleterious effects of radiation exposure, and when dealing with female patients, whose reproductive organs and breast tissue are likely to be particularly radiosensitive. Despite this, we found no correlation between annual diagnostic radiation exposure and age or gender. Radiation protection is especially pertinent to patients with functional GI disorders, who are typically female and of reproductive age. Therefore, it is reassuring that patients with functional disorders alone were exposed to significantly less diagnostic radiation than patients with IBD and other organic disorders. Although patients with functional disorders of childhood and adolescence were at increased risk of high annual and high total diagnostic radiation exposure, it is likely that these patients represented cases at the more complex or severe end of this diagnostic group, who required referral to a specialist clinic that generally deals with adults. Given the global prevalence of functional GI disorders and the potential for large volumes of negative studies, there is a clear need for evidence-based guidance on the use of diagnostic imaging in this population. Alternative, radiation-free imaging modalities including ultrasound, capsule endoscopy, and magnetic resonance imaging (MRI) are available. Ultrasound has proven diagnostic utility in GI disorders, especially in the pediatric population, but can be time-consuming and operator-dependent. 25 Although indications for capsule endoscopy are increasing, 26 it remains a second-line modality and is not universally available. Although abdominal MRI and MRI enterography have proven utility in the diagnosis of GI disease, issues surrounding cost and availability of MRI mean that CT is likely to remain the modality of choice for cross-sectional abdominal imaging in most centers for the foreseeable future. There are numerous strategies available to reduce the radiation dose associated with CT imaging. 27 New technologies that allow abdominal CT imaging at doses reduced by up to 60% are emerging 28 and are under prospective study at many centers, including ours. This study is subject to limitations. The population was based in a tertiary gastroenterology center specializing in IBD and functional GI disorders. The findings are therefore relevant to patients with more severe or complicated disease courses, particularly those who attend specialist centers for periods exceeding 1 year, and should not be extrapolated to patients managed exclusively at primary or secondary care level. The radiologic data compiled for this study did not include MRI studies because MRI services are not centralized at our center, and we could not ensure accurate imaging statistics for such a large population. In addition, local MRI services are prioritized for specialties other than gastroenterology (eg, rheumatology, orthopedics, and neurology), and therefore, MRI was not readily available to our patients during the entire study period. Finally, the actual dose of radiation received by a patient undergoing imaging might vary appreciably according to equipment, imaging technique, patient body habitus, and other technical factors. Using published average effective doses for diagnostic imaging studies might have resulted in overestimates or underestimates of cumulative radiation exposure in individual cases. Conclusions The last decade has seen significant increases in the amount of diagnostic radiation to which patients with GI disorders attending specialist centers are exposed. The majority of this exposure is due to abdominal CT. Higher levels of exposure are more likely in patients with IBD and organic small bowel disorders but are also associated with other organic and functional diagnoses. Given the likely deleterious effects of exposure to ionizing radiation and the age and gender profile of patients in these disease categories, there is a clear need for evidence-based guidelines on the use of diagnostic imaging in patients with organic and functional GI disorders. References 1. Mettler FA Jr, Huda W, Yoshizumi TT, et al. Effective doses in radiology and diagnostic nuclear medicine: a catalog. Radiology 2008;248: Brenner DJ, Hall EJ. Computed tomography: an increasing source of radiation exposure. N Engl J Med 2007;357: Committee on Biological Effects of Ionizing Radiation (BEIR). Health risks from exposure to low levels of ionizing radiation: BEIR VII phase 2. Washington, DC: National Academies Press, Available at: Accessed January 5, Little MP. Cancer and non-cancer effects in Japanese atomic bomb survivors. J Radiol Protect 2009;29:A43 A 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: Brenner DJ, Elliston CD, Hall EJ, et al. Estimates of the cancer risks from pediatric CT are not merely theoretical: comment: on Point/counterpoint: in x-ray computed tomography, technique factors should be selected according to patient size. Against the proposition. Med Phys 2001;28: Brenner D, Elliston C, Hall E, et al. Estimated risks of radiationinduced fatal cancer from pediatric CT. AJR Am J Roentgenol 2001;176: Martin DR, Semelka RC. Health effects of ionising radiation from diagnostic CT. Lancet 2006;367: Berrington de Gonzales A, Darby S. Risk of cancer from diagnostic x-rays: estimates for the UK and 14 other countries. Lancet 2004;363: Hall EJ, Brenner DJ. Cancer risks from diagnostic radiology. Br J Radiol 2008;81: 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: 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: 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: World Health Organization International Classification of Diseases-10. Geneva, Switzerland: World Health Organization, Available at: icd10online. Accessed June 6, 2009.

7 March 2012 RADIATION EXPOSURE FROM DIAGNOSTIC IMAGING Rome III diagnostic criteria for functional GI disorders. Raleigh, NC: The Rome Foundation, Available at: romecriteria.org/rome_iii_gastro. Accessed June 6, Bernstein CN, Blanchard JF, Kliewer E, et al. Cancer risk in patients with inflammatory bowel disease: a population-based study. Cancer 2001;91: Jess T, Loftus EV Jr, Velayos FS, et al. Risk of intestinal cancer in inflammatory bowel disease: a population-based study from Olmsted County, Minnesota. Gastroenterology 2006;130: Cash BD, Schoenfeld P, Chey WD. The utility of diagnostic tests in irritable bowel syndrome patients: a systematic review. Am J Gastroenterol 2002;97: Brandt LJ, Bjorkman D, Fennerty MB, et al. Systematic review on the management of irritable bowel syndrome in North America. Am J Gastroenterol 2002;97(Suppl):S7 S American College of Gastroenterology Task Force on Irritable Bowel Syndrome, Brandt LJ, Chey WD, et al. An evidencebased position statement on the management of irritable bowel syndrome. Am J Gastroenterol 2009;104(Suppl 1):S1 S Arslanoğlu A, Bilgin S, Kubal Z, et al. Doctors and intern doctors knowledge about patients ionizing radiation exposure doses during common radiological examinations. Diagn Interv Radiol 2007;13: Soye JA, Paterson A. A survey of radiation dose among health professionals in Northern Ireland. Br J Radiol 2008;81: Winkler NT. ALARA concept: now a requirement. Radiol Technol 1980;51: Bevelacqua JJ. Practical and effective ALARA. Health Phys 2010; 98(Suppl 2):S39 S Saibeni S, Rondonotti E, Iozzelli A, et al. Imaging of the small bowel in Crohn s disease: a review of the old and new techniques. World J Gastroenterol 2007;13: Liao Z, Gao R, Xu C, et al. Indications and detection, completion, and retention rates of small-bowel capsule endoscopy: a systematic review. Gastrointest Endosc 2010;71: Kalra MK, Maher MM, Rizzo S, et al. Radiation exposure and projected risks with multidetector-row computed tomography scanning: clinical strategies and technologic developments for dose reduction. J Comput Assist Tomogr 2004;28(Suppl 1): S46 S 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: Reprint requests Address requests for reprints to: Alan N. Desmond, MB, BMedSc, MRCPI, Department of Gastroenterology, Clinical Sciences Building, Cork University Hospital, Cork, Ireland. alanndesmond@ gmail.com; fax: 353 (0) Conflicts of interest The authors disclose no conflicts. Funding Supported in part by Science Foundation, Ireland, by the Health Research Board of Ireland, and by an unrestricted research grant from Abbott Pharmaceuticals.

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