Diagnostic imaging and radiation exposure in inflammatory bowel disease

Table 1 Radiation doses from gastrointestinal imaging studies in comparison to background radiation, condensed from RadiologyInfo.org[9] and Mettler et al[10]

Imaging procedure	Average effective dose (mSv)	Time period for equivalent effective dose from natural background radiation1
Multiphase CT abdomen and pelvis	31	10.3 yr
PET/CT	25	8.3 yr
CT Abdomen and Pelvis	10	3.3 yr
CT Colonography	10	3.3 yr
CT Abdomen	8	2.7 yr
Barium Enema	8	2.7 yr
Small bowel follow-through	5	1.7 yr
X-ray abdomen	0.7	2.8 mo

¹Based on the assumption of an average effective dose of 3 mSv per year from natural background radiation. CT: Computed tomography; PET: Positron emission tomography.

Table 2 Quantification of the cumulative effective dose of diagnostic radiation received by IBD patients, and factors associated with high cumulative radiation exposure (cumulative effective dose > 50 mSv); adapted from Chatu et al[12] with permission

Study	Number of patients (n)	Country	Design	Patient population	Outcome CED≥50 mSv	Mean/Median CED (mSv)	Factors associated with high radiation exposure
Newnham et al[59], 2007	100 (62 CD, 37 UC, 1 indeterminate colitis)	Australia	Retrospective study, single tertiary centre, patients recruited consecutively from clinic	Adult (16-84 yr)	11/100 (11%) 9 CD, 2 UC	Median CED 10 mSv	Assessed: age, gender, disease, disease duration, previous surgery, immunomodulator use, referral source Significant: none
Desmond et al[11], 2008	354 CD	Ireland	Retrospective study, single tertiary centre, patients recruited from IBD database July 1992-June 2007	Adult and paediatric (8.6-78.3 yr)	CED ≥ 75 mSv in 55/354 patients (15.5%)	Mean CED 36.1 mSv	Assessed: age, gender, smoking, FH, disease distribution, disease behaviour, medication, surgical history Significant: age < 17 at diagnosis, upper GI tract disease, penetrating disease, requirement for IV steroids, infliximab use, multiple surgeries
Peloquin et al[18], 2008	215 (103 CD, 112 UC)	United States	Retrospective study, population based inception cohort diagnosed between 1991 to 2001 from Olmsted County	Adult and paediatric (1.2-91.4 yr)	N/A	Median CED CD: 26.6 mSv UC: 10.5 mSv	N/A
Levi et al[60], 2009	324 (199 CD, 125 UC)	Israel	Retrospective study, single tertiary centre, patients diagnosed Jan 1999-Dec 2006, recruited from IBD database	Adult and paediatric ≤ 17 yr (18) > 18 yr (306)	23/324 (7.1%)	Mean CED CD: 21.1mSv UC: 15.1mSv	Assessed: age, surgery, diagnosis, medical therapy, disease duration, gender Significant: CD, surgery, prednisolone use, disease duration, first year of disease, age
Palmer et al[61], 2009	1593 (965 CD, 628 UC)	United States	Retrospective study, population based cohort recruited from insurance claims database Jan 2003-December 2004	Paediatric (2-18 yr)	N/A (34% CD, 23% UC exposed to moderate radiation - at least 1 CT or 3 fluoroscopic procedures)	N/A	Assessed: age, gender, region, hospitalisation, surgery, ED encounter, medication Significant: hospitalisation, inpatient GI surgery, ED encounter, use of steroids
Kroeker et al[62], 2011	553 (371 CD, 182 UC)	Canada	Retrospective study, single tertiary centre, patients diagnosed 2003-2008, recruited from IBD database	Adult and paediatric (15-84 yr)	28/553 (5%) 27 CD, 1 UC	Mean CED CD: 14.3 mSv UC: 5.9 mSv	Assessed: age at diagnosis, gender, disease distribution, previous surgery Significant: previous surgery
Fuchs et al[63], 2011	257 (171 CD, 86 UC)	United States	Retrospective study single tertiary centre, patients reviewed Jan-May 2008	Paediatric (< 18 yr)	15/257 (5.8%) 14 CD, 1UC	Mean CED CD: 20.5 mSv UC: 11.7 mSv	Assessed in CD cohort: gender, disease behaviour, previous surgery, disease duration, elevated platelet count at diagnosis Significant: previous surgery, elevated platelet count at diagnosis
Sauer et al[64], 2011	117 (86 CD, 31 UC)	United States	Retrospective study, single tertiary centre, patients diagnosed 2002-2008	Paediatric (2-18 yr)	6/117 (5%) 6 CD	Median CED CD: 15.6 mSv UC: 7.2 mSv	N/A
Huang et al[65], 2011	105 (61 CD, 32 UC, 12 indeterminate colitis)	United States	Single tertiary paediatric centre, patients identified from medical records	Paediatric cohort (11 mo-18 yr)	6/105 (6%)	Mean CED 15 mSv	Assessed: surgery, disease type, disease location, racioethnic background, anti TNF agents, use of immunomodulators, hospital admissions, age at diagnosis Significant: CD, small bowel involvement, black ethnicity, number of hospital admissions, previous surgery, anti TNF alpha use
Butcher et al[17], 2012	280	United Kingdom	Retrospective study, single tertiary centre, consecutive patients attending IBD clinic	Adult cohort	6.3% CD	Mean CED 10.17 mSv Median CED 4.12 mSv	Significant: smoking status, disease duration, previous surgery
Jung et al[15], 2013	2199 (777 CD, 1422 UC)	South Korea	Retrospective study, multicentre conducted at 13 university hospitals in South Korea, patients diagnosed July 1987-Jan 2012 included	Adult cohort (Mean age: CD 29.2 yr; UC 42.2 yr)	34.7% CD, 8.4% UC	Mean CED CD: 53.6 mSv UC: 16.4 mSv	Assessed: gender, age at diagnosis, disease duration, disease extent, surgery, hospitalisation, 5-ASA use, steroids, immunomodulator use Significant: For CD - longer disease duration, ileocolonic disease, upper GI tract involvement, surgery, hospitalisation, steroids For UC - surgery, hospitalisation, infliximab use
Chatu et al[14], 2013	415 (217 CD, 198 UC)	United Kingdom	Retrospective study, single tertiary centre, patients consecutively recruited from clinic Jan 2011- June 2011	Adult cohort (Mean age: CD 30.8 yr; UC 36.9 yr)	32/415 (8%) 29 CD, 3 UC	Median CED CD: 7.2 mSv UC: 2.8 mSv	Assessed: gender, age at diagnosis, disease type, steroid use within 3 mo diagnosis, use of immunomodulators or biologics, extraintestinal features, IBD related surgery Significant: males, IBD related surgery
Estay et al[13], 2015	325 (82 CD, 243 UC)	Chile	Retrospective study, patients recruited from IBD Registry 2011-2013	Adult cohort (16-86 yr)	22/325 (6.8%): CD 16 (19.5%); UC 6 (2.5%)	Mean CED 11.97 mSv CD: 29.9 mSv UC: 5.92 mSv	Assessed in CD cohort only: age at diagnosis, disease duration, disease location, disease behaviour, perianal disease, surgery, hospitalisation, medications Significant: longer disease duration, ileal involvement, stricturing disease, treatment with steroids and biological agents, CD related hospitalisation or surgery

UC: Ulcerative colitis; CD: Crohn’s disease; IBD: Inflammatory bowel disease; CED: Cumulative effective dose; mSv: Millisieverts of radiation; ED: Emergency department; FH: Family history.

Table 3 Comparison of diagnostic accuracies of radiation-free imaging (ultrasonography/magnetic resonance imaging) vs conventional ionising radiation imaging for the evaluation of small bowel Crohn’s disease

Study	Country	Number of patients (n)	Design	Imaging compared	Study findings
Low et al[66], 2000	United States	26 CD	Prospective study, single centre	Contrast enhanced MR with single phase CT using findings from surgery, barium studies, endoscopy and histology as reference standard	Side-by-side comparison: MR imaging superior than helical CT in depiction of normal bowel wall, mural thickening or enhancement and overall GI tract evaluation MR images showed 55 (85%) and 52 (80%) of 65 abnormal bowel segments for the two observers, compared with helical CT which showed 39 (60%) and 43 (65%) of bowel segments affected by CD (P < 0.001, P < 0.05)
Maconi et al[67], 2003	Italy	128 CD	Prospective study, consecutive CD patients who underwent surgery immediately after diagnostic work-up	US, barium studies, CT to detect internal fistulae and intra-abdominal abscesses compared to intraoperative findings	Detecting internal fistula: comparable diagnostic accuracy of US (85.2%) and barium X-ray (84.8%) studies Sensitivity US (71.4%), X-ray (69.6%), Specificity US (95.8%), X-ray (95.8%) Detection of abscesses: US (90.9%), CT (86.4%) Overall diagnostic accuracy higher with CT than US (91.8% vs 86.9%) due to false positives with US
Parente et al[49], 2004	Italy	102 CD	Prospective study, consecutive patients with proven CD by BE and ileocolonoscopy enrolled from IBD clinic Dec 2002-July 2003 Adult cohort (≥ 18 yr)	Conventional US vs oral contrast enhanced US, compared to BE and ileocolonoscopy as gold standard	Per segment analysis: Superior diagnostic accuracy of contrast US in detecting small bowel CD. Sensitivity: conventional US 91.4%, contrast US 96.1% Good correlation of disease extent measurements with BE: US (r = 0.83), contrast US (r = 0.94) Higher sensitivity and specificity with contrast US in detecting ≥ 1 small bowel strictures: Sensitivity: US (74%), contrast US (88.8%) Specificity: US (93.3%), contrast Us (97.3%) US and contrast US more accurate in detecting internal fistulas than BE, but no significant difference in diagnostic accuracy between US and contrast US. US (80%), contrast US (86%), BE (67%) Significantly improved interobserver variability between sonographers with contrast US for detecting bowel wall thickness and disease location
Calabrese et al[55], 2005	Italy	28 CD	Prospective study, consecutive patients recruited from IBD clinic Adult cohort (age range 21-60 yr)	SICUS (performed by a sonologist of 1 yr experience) vs TUS (performed by an experienced sonologist of 10 yr experience), compared to SBE as gold standard	Sensitivity for detection of small bowel lesions: 96% TUS, 100% SICUS Greater correlation of extension of lesions between SICUS and SBE (r = 0.88) vs TUS and SBE (r = 0.64) Sensitivity for detection of ≥ 1 stricture: 76% TUS, 94% SICUS Sensitivity and specificity for assessing prestenotic dilatation: 50% and 100% for TUS, vs 100% and 90% for SICUS
Horsthuis et al[40], 2007	Amsterdam	1735 (sample size 15-440)	Meta-analysis of 33 prospective studies published between Jan 1993- Feb 2006 Adult and paediatric cohort (age range 2-86 yr)	US, MRI, scintigraphy, CT US evaluated in 11 studies, MRI in 11, scintigraphy in 9 and CT in 7 studies	Per-patient analysis: Significantly lower specificity for scintigraphy vs US. No significant difference between mean sensitivities for diagnosis of IBD Sensitivities: 89.7% US, 93% MRI, 87.8% scintigraphy, 84.3% CT Specificities: 95.6% US, 92.8% MR, 84.5% scintigraphy, 95.1% CT Per bowel segment analysis: Significantly lower sensitivity and specificity for CT compared to scintigraphy and MRI. Sensitivities: 73.5% US, 70.4% MRI, 77.3% scintigraphy, 67.4% CT. Specificities: 92.9% US, 94% MRI, 90.3% scintigraphy, 90.2% CT
Lee et al[22], 2009	South Korea	30 CD	Prospective study, single centre, consecutive patients with known or suspected CD enrolled Adult cohort (age range 18-44 yr)	MRE, CT, SBFT for detection of active small bowel inflammation and extra enteric complications with ileocolonoscopy as reference standard	No significant difference between CTE, MRE and SBFT for the detection of active terminal ileitis. Sensitivity CTE (89%), MRE (83%), SBFT (67%-72%) Significantly higher sensitivity for MRE (100%) and CTE (100%) compared to SBFT (32% reader 1, 37% reader 2) for the detection of extra enteric complications
Siddiki et al[68], 2009	United States	33 CD	Prospective blinded study, single centre, consecutive patients with suspected active small bowel CD April 2005-May 2008 Adult cohort (age range 20-63 yr)	MRE, CTE compared with ileocolonoscopy	No significant difference between sensitivity of MRE (90.5%) and CTE (95.2%) in detecting active small bowel CD In 8 cases (24%) MRE and CTE identified active small bowel inflammation not detected at ileocolonoscopy MRE significantly lower image quality score than CTE
Ippolito et al[69], 2009	Italy	29 CD	Prospective study, Single centre, symptomatic patients with proven CD and suspected relapse, recruited from outpatient clinic Adult and paediatric cohort (age range 14-70 yr) Mean age 43.8 yr	Contrast MRE and contrast multi-detector CTE	Complete agreement between MRE and CTE in classification of disease activity (k = 1) Good level of agreement between MRE and CTE for wall thickening and mucosal hyperenhancement (k = 1), comb (k = 0.9) and halo signs (k = 0.86) CTE superior to MRE in detecting fibrofatty proliferation (P = 0.045) MRE depicted higher number of fistulas than CTE but non-significant (P = 0.083)
Schreyer et al[70], 2010	Germany	53 CD	Retrospective study, Single centre, Patients with advanced CD and acute abdominal pain attending the emergency department Adult cohort	Conventional CT, MRE	No significant difference in image quality between CT and MRE No significant difference in diagnosis of small bowel inflammation between CT (69.4%) and MRE (71.4%) CT detection of lymph nodes significantly higher than MRE No significant difference in detection of fistulae (CT n = 25, MRE n = 27) or abscesses (CT n = 32, MRE n = 32)
Panés et al[41], 2011	Spain	N/A	Systematic review of 68 prospective studies, minimum 15 patients per study	US, CT, MRI for diagnosis of CD, assessment of disease extent and activity, detection of complications	Sensitivity for diagnosis of suspected CD and evaluation of disease activity: US 84%, MRI 93% Specificity for diagnosis of suspected CD and evaluation of disease activity: US 92%, MRI 90% CT similar accuracy to MRI for assessment of disease activity and extension. US accuracy lower for disease proximal to terminal ileum US, CT, MRI all high accuracy for detection of fistulas, abscesses, stenosis. US higher false positive for abscesses
Fiorino et al[43], 2011	Italy	44 CD	Prospective study, Single centre, consecutive patients with ileocolonic CD requiring endoscopic or radiological evaluation Enrolled 2006-2009 Adult cohort (> 18 yr) Mean age 44 yr	CTE and MRE to assess disease activity and complications in ileocolonic CD, using ileocolonoscopy as reference standard	MRE significantly superior to CTE in detecting internal strictures: sensitivity (92% vs 85%), accuracy (95% vs 91%), specificity (90% vs 51%) Overall no significant difference in sensitivity and specificity of MRE and CTE in localising CD, bowel wall thickening, bowel wall enhancement, enteroenteric fistulas, detection of abdominal nodes, perivisceral fat enhancement Per segment analysis, MRE significantly superior to CTE in detecting ileal wall enhancement, with higher sensitivity (93% vs 81%) and accuracy (88% vs 81%), but lower specificity (72% vs 81%). MRE significantly superior in localising rectal disease, with higher accuracy (93% vs 85%), specificity (100% vs 50,9%) but lower sensitivity (72% vs 81%)
Jensen et al[71], 2011	Denmark	50 CD	Prospective, multicentre study, patients with symptomatic pre-existing CD requiring small bowel imaging for treatment decisions	MRE and CTE compared with gold standard of ileoscopy or surgery	No significant difference between MRE and CTE for detection of small bowel CD MRE: sensitivity 74%, specificity 80% CTE: sensitivity 83%, specificity 70% No significant difference for detection of small bowel stenosis. MRE: sensitivity 55%, specificity 92%. CTE: sensitivity 70%, specificity 92%
Chatu et al[50], 2012	United Kingdom	143 CD	Retrospective study, single tertiary centre, all symptomatic patients with known or suspected CD who underwent SICUS retrospectively were reviewed June 2007-Dec 2010 Adult cohort Mean age 36 yr	SICUS compared with SBFT, CT, histological findings from ileocolonoscopy or surgery, and CRP, using final diagnosis as the reference standard	Sensitivity of SICUS in detecting active small bowel CD in known or suspected cases 93%, specificity 99%, positive predictive value 98%, negative predictive value 95% Agreement between SICUS with SBFT (k = 0.88), CT (k = 0.91), histological findings (k = 0.62), CRP (k = 0.07)
Pallotta et al[51], 2012	Italy	49 CD	Prospective study, consecutive patients, adult and paediatric CD who underwent resective bowel surgery Jan 2000-Oct 2010 Mean age 37.7 yr (Age range 12-78 yr)	Conventional transabdominal US and SICUS compared to intraoperative and histological findings to assess CD complications	SICUS ability to: Detect at least one stricture: Sensitivity 97.5%, specificity 100%, k = 0.93 Detect two or more strictures: Sensitivity 75%, specificity 100%, k = 0.78 Detect fistulas: Sensitivity 96%, specificity 90.5%, k = 0.88 Detect intra-abdominal abscesses: Sensitivity 100%, specificity 95%, k = 0.89
Qiu et al[44], 2014	China	290 CD	Systematic review with meta-analysis including six studies, all prospective with enrollment of consecutive CD patients	MRE and CTE in detecting active small bowel CD and complications	Pooled sensitivity MRE in detecting active small bowel CD: 87.9%, specificity 81.2% Pooled sensitivity CTE in detecting active small bowel CD 85.8%, specificity 83.6% No significant difference between MRE and CTE in detecting fistula, stenosis and abscesses.
Kumar et al[52], 2015	United Kingdom	67 CD	Retrospective study, Single tertiary centre. Adult cohort (age 18.8-68.9 yr) CD patients requiring resective bowel surgery within 6 mo of SICUS/MRE investigation being performed June 2007-December 2012	SICUS and MRE compared to intraoperative findings	Sensitivity of SICUS and MRE in detecting: Strictures: 87.5%, 100% Fistulae: 87.7%, 66.7 Abscesses: 100%, 100% Bowel dilatation: 100%, 66.7% Bowel wall thickening: 94.7% and 81.8% Compared with surgery, high level of agreement of SICUS, MRE in: Localising strictures: k = 0.75, 0.88 Fistulae: k = 0.82, 0.79 Abscesses k = 0.87, 0.77 High level of agreement between SICUS and MRE in identifying stricturing disease (k = 0.84), number and location of strictures (k = 0.85), fistulae (k = 0.65), mucosal thickening (k = 0.61)
Aloi et al[53], 2015	Italy	25 CD	Single tertiary centre for paediatric IBD Paediatric cohort with known or suspected small bowel CD	MRE, SICUS, CE for diagnosis of small bowel CD	Jejunum: Specificity CE significantly lower (61%) than MRE. No significant difference in sensitivity: SICUS 92%, CE 92%, MRE (75%) Proximal and mid-ileum: Specificity CE significantly lower. No significant difference in sensitivity: MRE 100%, CE 100%, SICUS 80% Terminal ileum: Sensitivity of SICUS and MRE (94%, 94%) higher than CE (81%), CE more specific

CD: Crohn’s disease; MRE: Magnetic resonance enterography; CT: Computed tomography; CTE: Computerised tomography enterography; SICUS: Small intestine contrast-enhanced ultrasonography; CE: Capsule endoscopy; BE: Barium enteroclysis; SBFT: Small bowel follow-through; US: Ultrasonography; MRI: Magnetic resonance imaging.