Accepted Manuscript

Accuracy of Small Intestine Contrast Ultrasonography, Compared to

Computed Tomography Enteroclysis, in Characterizing Lesions in
Patients with Crohn’s Disease

E. Calabrese, F. Zorzi, S. Onali, E. Stasi, R. Fiori, S. Prencipe, A.

Bella, C. Petruzziello, G. Condino, E. Lolli, G. Simonetti, L.
Biancone, F. Pallone

PII: S1542-3565(13)00123-7
DOI: 10.1016/j.cgh.2013.01.015
Reference: YJCGH 53181

To appear in: Clinical Gastroenterology and Hepatology

Accepted date: 11 January 2013

Please cite this article as: Calabrese, E., Zorzi, F., Onali, S., Stasi, E., Fiori, R., Prencipe,
S., Bella, A., Petruzziello, C., Condino, G., Lolli, E., Simonetti, G., Biancone, L.,
Pallone, F., Accuracy of Small Intestine Contrast Ultrasonography, Compared to
Computed Tomography Enteroclysis, in Characterizing Lesions in Patients with Crohn’s
Disease, Clinical Gastroenterology and Hepatology (2013), doi:
10.1016/j.cgh.2013.01.015.

This is a PDF file of an unedited manuscript that has been accepted for publication. As a
service to our customers we are providing this early version of the manuscript. The
manuscript will undergo copyediting, typesetting, and review of the resulting proof
before it is published in its final form. Please note that during the production process
errors may be discovered which could affect the content, and all legal disclaimers that
apply to the journal pertain.

All studies published in Clinical Gastroenterology and Hepatology are embargoed until
3PM ET of the day they are published as corrected proofs on-line. Studies cannot be
publicized as accepted manuscripts or uncorrected proofs.
Accuracy of Small Intestine Contrast Ultrasonography, Compared to Computed
Tomography Enteroclysis, in Characterizing Lesions in Patients with Crohn’s Disease

Calabrese E, Zorzi F, Onali S, Stasi E, Fiori R*, Prencipe S, Bella A^, Petruzziello C, Condino G,
Lolli E, Simonetti G*, Biancone L, Pallone F.

Gastroenterology Unit, Department of Systems Medicine; *Department of Diagnostic Imaging

and Molecular Imaging, Interventional Radiology, Nuclear Medicine and Radiotherapy;
University of Rome “Tor Vergata”, Italy; ^National Centre for Epidemiology, Surveillance and
Health Promotion, Istituto Superiore di Sanita’, Rome, Italy.

Short title: SICUS vs CT-Enteroclysis for CD

Word count: 3300

Key words: Crohn’s disease, small intestine contrast ultrasonography, CT-Enteroclysis.

Author contributions: EC conceived the study. EC, FZ, ES, GS and RF produced and interpreted
sonographic and radiologic data. EC, FZ, AB and FP analyzed and interpreted the data. EC and
FP drafted the manuscript. EC, OS, SP, CP, GC, EL, and LB enrolled and followed up the
patients.

Conflict of interest: none.

Address for the correspondence:

Emma Calabrese, M.D., Ph.D
Gastrointestinal Unit, Department of Systems Medicine
University of Rome “Tor Vergata”
Viale Oxford, 81
00133 Rome, Italy
Tel. +39.06.20900969
Fax +39.06.20904437
e-mail: emma.calabrese@uniroma2.it
Abstract:
Background & Aims: Small intestine contrast ultrasonography (SICUS) is a radiation-free
technique that can detect intestinal damage in patients with Crohn’s disease (CD). We evaluated
the diagnostic accuracy of SICUS in determining the site, extent, and complications of CD,
compared with computed tomography (CT)-enteroclysis as the standard.

Methods: We performed a retrospective analysis of data from 59 patients with CD evaluated by

SICUS and CT-enteroclysis 3 months apart, between January 2007 and April 2012. We
evaluated disease site (based on bowel wall thickness), extent of lesions, and presence of
complications (stenosis, prestenotic dilation, abscess, or fistulas) using CT-enteroclysis as the
standard. Sensitivity, specificity, and diagnostic accuracy were calculated. We determined the
correlations in maximum wall thickness and disease extent in the small bowel between results
from SICUS and CT-enteroclysis.

Results: SICUS identified the site of small bowel CD with 98% sensitivity, 67% specificity, and
95% diagnostic accuracy; it identified the site of colon CD with 83% sensitivity, 97.5%
specificity, and 93% diagnostic accuracy. Results from SICUS and CT-enteroclysis correlated in
determination of bowel wall thickness (Rho=0.79) and disease extent (Rho=0.89; P<.0001 for
both). SICUS detected ileal stenosis with 95.5% sensitivity, 80% specificity, and 91.5%
diagnostic accuracy, and pre-stenotic dilation with 87% sensitivity, 67% specificity, and 75%
diagnostic accuracy. SICUS detected abscesses with 78% sensitivity, 100% specificity, and 97%
diagnostic accuracy, and fistulas with 78.5% sensitivity, 95.5% specificity, and 91.5% diagnostic
accuracy.

Conclusions: SICUS identified lesions and complications in patients with CD with high levels
of sensitivity, specificity, and accuracy compared to CT-enteroclysis. SICUS might be used as an
imaging tool as part of a focused diagnostic examination of patients with CD.

KEY WORDS: IBD, inflammatory bowel disease, detection, cross-sectional imaging technique

2
Background

Crohn’s disease (CD) is an inflammatory bowel disease (IBD) that may involve various
portions of the gastrointestinal tract, although ileal and colonic involvement is most frequent. CD
is a transmural progressive and destructive disease leading to irreversible bowel damage
characterized by stenosis of the intestinal lumen and penetrating lesions such as fistulas and
abscesses. Assessment of intestinal inflammatory lesions by imaging techniques is essential for
diagnosis and for management of CD patients requiring a proper management plan.
Ileocolonoscopy is the first line investigation in the diagnosis, management, and
monitoring of CD (1); however ileocolonoscopy cannot always be completed and there are
several drawbacks related to invasiveness, discomfort and poor patient acceptance.
Ileocolonoscopy also does not evaluate ileal disease extent and transmural damage.
Looking beyond the mucosa surface, over the last few years, several cross-sectional
imaging techniques have been increasingly used for evaluation of patients with CD, including
bowel ultrasound (US), computed tomography (CT) and magnetic resonance imaging (MRI).
The ECCO and the ACG guidelines (1-2) considered CT or MR enterography/enteroclysis as the
cross sectional imaging techniques with the highest diagnostic accuracy for the detection of
intestinal involvement of CD including extramural complications. Transabdominal
Ultrasonography (US) is considered a useful additional technique for assessing bowel
inflammation (1). In a recent systematic review conducted by Panes and colleagues, no
significant differences in diagnostic accuracy among the imaging techniques (bowel US, CT,
MR) were observed and concluded that because patients with IBD often needed frequent re-
evaluations of the disease status, use of a diagnostic modality that does not involve the use of
ionizing radiation is preferable (3).
Small Intestine Contrast Ultrasonography (SICUS) has emerged as a valuable and
radiation-free technique in the detection of intestinal damage in CD (4). When compared with
conventional bowel US, the use of an oral contrast agent (polyethilen glycol, PEG) improved the
overall sensitivity in the detection of small bowel lesions in CD patients (5-8).
The aim of our study was to evaluate the diagnostic accuracy of SICUS for CD site,
disease extent and complications using CT-Enteroclysis as gold standard.

3
Methods

Study design and population

We retrospectively identified 59 patients with established CD who underwent SICUS and

CT-Enteroclysis between January 2007 and April 2012. To be included in the study CT-
Enteroclysis and SICUS were performed within 3 months. This retrospective study was
conducted with the approval of the ethical committee.

Definitions and procedures

Diagnosis, CD site and patient’s management were made according generally accepted
recommendations (1, 9). Clinical characteristics of the 59 patients enrolled in the study are
shown in Table 1.

SICUS was performed in all patients by one independent experienced operator. The
patients were examined in the fasting state without any preparation. SICUS was performed as
previously described (6, 10), after the ingestion of 375 mL (range 250-500 mL) of polyethylene
glycol (PEG) using a convex transducer (1-8 MHz) and a high frequency linear-array transducer
for details (3-11 MHz) (Esaote, My Lab Twice, Genoa, Italy). Median SICUS duration was 40
minutes (range 35-90 minutes). No patient was obese and technically adequate scans were
obtained in all patients.

CT-Enteroclysis was performed in all patients by one independent experienced operator.

Colonic cleansing the day before the examination was accomplished with PEG solution. A 20G
needle was placed in an antecubital vein and 8-F nasojejunal catheter with a Teflon-covered
guide wire was positioned under fluoroscopic guidance (Guerbet, Guebert GmbH D65838,
Sulzbach/Ts) with the distal extremely located in the distal duodenal tract. Afterward the patient
was taken into the CT room where hypodense contrast material (1500 mL of PEG) was
administered manually with 60-mL syringes, with a constant and continuous injection rate of 150
mL/min followed by a flow rate of 200 mL/min until the maximum tolerance of the patient. Just
before the examination patients received a smooth muscle relaxant (N butylscopolamine) to
prevent spasms, achieve uniform small bowel distension, and reduce abdominal discomfort. The

4
study was performed by a 64-slice multidetector (LightSpeed VCT, General Electric Medical
System, Milwaukee, WI, USA) with the following scan parameters: collimation 1.25 mm, table
feed 39.37 mm/rot, 120 kV, 300 mAs, pitch 0.984:1, rotation time 0.5 s, time of acquisition 12.5
s, FOV 50 cm, matrix 512x512. After the infusion of PEG, CT scan was performed before and
after the administration of intravenous iodinated contrast material. The contrast-enhanced study
was acquired 70s after the administration of contrast material (Ultravist 370, Schering AG,
Berlin, Germany). Median CT-Enteroclysis duration was 20 minutes (range 15-25 minutes). The
radiation dose for each patient was 8 mSV (ASIR protocol).

Forty one out of 59 patients underwent also ileocolonoscopy within 3 months from
sonographic and radiologic assessments and twenty one out of fifty nine patients underwent ileo-
colonic resection for complications (abscess, obstruction or refractory disease) during the follow
up.

Data collection

Information for each patient was obtained by review of medical record, including
endoscopy and surgical reports. The sonographer was not blinded to the clinical characteristics of
patients but SICUS was performed before CT-Enteroclysis in all cases. Small bowel contrast
ultrasonography and CT-Enteroclysis criteria for the presence of CD lesions and complications
were: bowel wall thickness (>3 mm) and disease extent (cm), presence of stricturing (stenosis
with or without pre-stenotic dilation) and penetrating complications (fistulas, abscess) (6, 11).

Statistical analysis

Statistical analysis was performed using STATA 11.2 (Stata Corporation, College
Station, Texas, USA). CT-Enteroclysis was considered the gold standard test for assessing the
accuracy of SICUS for CD lesions. Sensitivity, specificity, positive and negative predictive value
(PPV and NPV), diagnostic accuracy of SICUS was calculated. Correlations between SICUS and
CT-Enteroclysis parameters in terms of maximum bowel wall thickness and disease extent were
estimated using Spearman’s rank correlation (rho). Additionally SICUS and CT-Enteroclysis
agreement for maximum bowel wall thickness and disease extent were calculated using the
Bland-Altman method (12).

5
Results

CD site

The sensitivity, specificity, PPV, NPV, and diagnostic accuracy of SICUS for disease site
of small bowel CD was 98%, 67%, 96%, 80%, and 95%, respectively. Figure 1 illustrates how
SICUS provides imaging as accurate as CT-Enteroclysis for detecting bowel involvement
(Figure 1). A similar level of sensitivity, specificity, PPV, NPV, and diagnostic accuracy was
found for colonic site (83%, 97.5%, 94%, 93%, and 93%, respectively). SICUS correctly
identified the 3 patients with CD jejunal lesions.

A significant correlation was observed between SICUS data and CT-Enteroclysis in

terms of maximum bowel wall thickness (rho=0.79, p<0.0001). In addition the Bland-Altman
plot confirmed the agreement between the two techniques with 5.88% for maximum bowel wall
thickness outside the limits of agreement (Figure 2, panel A-B). Similarly a high correlation was
found between SICUS and CT-Enteroclysis when disease extent was taken into account
(rho=0.89, p<0.0001). The Bland-Altman plot confirmed the agreement between the two
techniques with 3.52% for disease extent outside the limits of agreement (Figure 2, panel C-D).
As shown in Figure 3 SICUS appeared to provide clear enough images for establishing disease
extent with a definition comparable to that provided by CT imaging (Figure 3).

During the follow up 21 out of 59 patients underwent surgery for complications, and
disease extent was measured by surgical pathologist on the resected specimen. There was a good
correlation between disease extent at SICUS and surgery (rho=0.83, p<0.0001). The Bland-
Altman plot confirmed the agreement between SICUS and surgery with 4.76% for disease extent
outside the limits of agreement (Figure 2, panel E-F). Similarly, correlation between disease
extent at CT-Enteroclysis and at pathology was significant (rho=0.68, p<0.0001).

Using colonoscopy as the gold standard for colonic lesions, SICUS and CT-Enteroclysis
showed the same values of sensitivity (71%), specificity (100%) and accuracy (89%).
Colonoscopy was incomplete in 4 out of 41 of patients (10%) and ileoscopy was unsuccessful in
18 out of 41 patients (44%) due to ileocecal valve stenosis.

6
CD complications

Sensitivity, specificity, PPV, NPV, and diagnostic accuracy of SICUS in detecting ileal
stenosis and pre-stenotic dilation was 95.5%, 80%, 93%, 86%, 91.5% and 87%, 67%, 62.5%,
89%, 75% respectively. Figure 4 shows how SICUS provides imaging of a typical sonographic
picture of stenosis with prestenotic dilation as accurate as CT-Enteroclysis imaging (Figure 4).
Using colonoscopy as the gold standard for colonic stenosis, CT-Enteroclysis detected only one
out of 3 stenosis (1 TP, 2 FN, 33 TN), while SICUS detected no stenoses (3 FN, 33 TN).

Abscesses were detected by CT-Enteroclysis in 9 patients; SICUS detected 7 out of 9

showing 78% of sensitivity, 100% of specificity, 100% of PPV, 96% of NPV, and 97% of
diagnostic accuracy in detecting abscesses (Figure 5). Fistulas were detected by CT-Enteroclysis
in 14 patients thus SICUS showed 78.5% of sensitivity, 95.5% of specificity, 85% of PPV, 93%
of NPV, and 91.5% of diagnostic accuracy in detecting overall fistulas.

Discussion

CD is a chronic, relapsing condition characterized by trans-mural inflammation of the

intestine. Hence, there is an urgent need to develop non-invasive imaging methods capable of
assessing disease activity and severity. CT and MR-Enterography/Enteroclysis were shown to be
accurate in evaluating disease activity and complications, such as fistulas and strictures (11).
Both techniques allow visualizing the small bowel above the ileocecal valve and the colon,
adding information about bowel wall involvement of the disease and extra-luminal signs of CD
to endoscopic findings. However, radiation exposure of CD patients undergoing repeated CT
examination should be carefully considered. Peloquin and colleagues analyzed the diagnostic
ionizing radiation exposure in a large IBD patient cohort, showing that CD patients were
exposed to 2.46 times more diagnostic ionizing radiation than patients with ulcerative colitis
(UC), potentially increasing the risk of developing cancer (13). The choice between CT and MR-
Enterography/Enteroclysis is often determined by local availability and expertise, and in some
countries also differences in the cost between CT and MRE (14). There is strong evidence that
all the available techniques to visualize the small bowel, such as US, CT, MR or position
emission tomography are perform equally in CD (15). Due to the need of frequent disease re-
evaluation, these observations add support to the view that the use of radiation free imaging

7
modality is preferable (15). US is a low cost, non invasive, radiation free imaging modality that
is gaining wider acceptance in gastroenterology and it is chosen as the first-line imaging
procedure for diagnosis of CD more frequently in Europe than in United States (16). Studies, in
unselected groups of patients, have shown that US may diagnose CD with a sensitivity of 67–
96% and specificity of 79–100% and that degree and extent of bowel wall thickening on US
correlate with clinical and biochemical parameters in children and young adults in comparison
with traditional radiologic techniques (17-18). Sensitivity of US in detecting CD lesions in the
ileum has been reported as high as 90% while US accuracy for upper small bowel and rectum
appeared to be lower (19). The use of oral contrast agents such as iso-osmolar polyethylene
glycol (PEG) has been shown to increase sensitivity in defining disease site (5-6), extent (5, 7)
and bowel complications in small bowel CD (20) and to reduce inter- and intra-observer
variability (5). Thus, Small Intestine Contrast Ultrasonography (SICUS) has been proposed to
accurately define CD intestinal damage for either initial assessment or monitoring progression
over time (5-7, 21-23).

Results from our head to head comparison study between SICUS and CT-Enteroclysis
confirmed the relevance of this sonographic technique as a valuable diagnostic tool for CD. In
this population, we found that SICUS is highly effective in localization of the disease, which is
the first goal of disease evaluation when patients first present with the disease and physicians
monitor it overtime. Furthermore, SICUS and CT-Enteroclysis gave similar results for the
detection of bowel wall thickening which is one of the most common pathological findings in
patients with CD. Similarly SICUS and CT-Enteroclysis showed a high correlation in terms of
lesion extent. Unexpectedly in a subgroup of patients, correlation between lesion extent at
SICUS and surgery was higher than at CT-Enteroclysis and surgery.

Regarding stricturing and penetrating complications SICUS showed a high sensitivity,

specificity and diagnostic accuracy in detecting ileal stenosis and pre-stenotic dilation as well as
fistulas and abscesses. SICUS and CT-Enteroclysis showed a lower accuracy in detecting
stenoses of colon but a head to head comparison is not possible due to low numbers of patients.

This study had two main limits. Because of the retrospective characteristic of the study,
bias in assessment was a possibility. Prospective studies are needed to assess if SICUS results
truly alters management plans and physician level of confidence in CD. The second one was that

8
SICUS was performed by a single expert operator. Operator-dependence is the most important
limit reported for US. However experience is direct connected with diffusion of this technique
that up to day is widespread in Germany, Italy and Spain and is starting to diffuse in Canada. In
addition interobserver agreement between sonographers with variable experience in US has been
reported as good in a few preliminary studies showing satisfactory results, but a learning curve
for this technique is still lacking (24).
In conclusion compared to CT-Enteroclysis, our retrospective study indicates that SICUS
showed a high diagnostic accuracy for detecting CD lesions in the ileum and in the colon, high
correlations in terms of bowel wall thickness and disease extent, high diagnostic accuracy for
detecting stricturing and penetrating complications. SICUS is a non-invasive imaging technique
that appears to be accurate in detecting CD lesions and complications. Due to its radiation free
nature, SICUS is easily repeatable if the patients’ condition changes and may be used as an
imaging tool performed as part of a focused diagnostic examination in CD.

9
Acknowledgments

Ethics approval: this study was conducted with the approval of the local Ethical committee of the
University of Rome “Tor Vergata”.

This study was accepted and presented as oral communication at DDW 2012, May 19-22, San
Diego, CA.

This manuscript was supported by “Fondazione Umberto di Mario Onlus.”

10
Table 1. Clinical characteristics of patients at inclusion in the study

Total number of patients 59

Male, n 29 M
Age (median/range, years) 41 (20-78)
Duration of disease (median/range, months) 96 (12-456)
Disease location
- Ileal, n (%) 32 (55)
- Ileocolonic, n (%) 22 (37)
- Jejuno-ileal, n (%) 3 (5)
- Colonic, n (%) 2 (3)
Disease behaviour
- Non stricturing non penetrating, n (%) 10 (17)
- Stricturing, n (%) 30 (51)
- Penetrating, n (%) 19 (32)
Previous surgery, n (%) 18 (30)
Indications of evaluation
- Assessment of disease, n (%) 43 (73)
- Obstructive symptoms, n (%) 12 (20)
- Pre-surgical evaluation, n (%) 3 (5)
- Control after therapy, n (%) 1 (2)
Therapy
- None, n (%)
- 5-ASA, n (%) 6 (10)
- Antibiotics, n (%) 25 (42)
- Corticosteroids, n (%) 16 (27)
- Azathioprine, n (%) 28 (47)
- Anti-TNFs, n (%) 6 (10)
9 (15)

11
Figures legend

Figure 1

Comparison between SICUS (panel A) and CT-Enteroclysis (panel B) images of a CD patient.

The white arrows indicate bowel wall thickness and the arrowheads lumen diameter of terminal
ileum as assessed by SICUS (panel A). The white circle on panel B encloses the same segment
of the terminal ileum presenting thickening and contrast enhancement as assessed by CT-
Enteroclysis.

Figure 2

Correlation between SICUS data and CT-Enteroclysis in terms of maximum bowel wall
thickness (mm, panel A) did reach statistical significance (rho=0.79, p<0.0001). The Bland-
Altman plot confirmed the agreement between the two techniques with 5.88% outside the limits
of agreement (mean difference -1.088, 95% limits of agreement -5.084, 2.908) (panel B).

Correlation between SICUS and CT-Enteroclysis when disease extent (cm, panel C) was taken
into account (rho=0.89, p<0.0001). The Bland-Altman plot confirmed the agreement between the
two techniques with 3.52% outside the limits of agreement (mean difference -0.433, 95% limits
of agreement -13.840, 12.975) (panel D).

Correlation between disease extent at SICUS and surgery (cm, panel E) did reach statistical
significance (rho=0.83, p<0.0001). The Bland-Altman plot confirmed the agreement between
SICUS and surgery with 4.76% outside the limits of agreement (mean difference -0.810, 95%
limits of agreement -12.770, 11.151) (panel F).

Figure 3

A second example of SICUS (panels A-C) and CT-Enteroclysis (panels D, E) images of a CD

patient. SICUS (white arrows, panels A-C) allowed the exact location and extent definition in
this 45-year-old CD patient, with a long lesion in the neo-terminal ileum characterized by bowel
wall thickness and lumen narrowing comparing CT-Enteroclysis (white circles, panels D, E).

Figure 4

Comparison between SICUS (panels A, B) and CT-Enteroclysis (panel C) images of a CD

patient. In panel A the white arrows indicate bowel wall thickness and stenosis of the terminal
ileum and in panel B the arrowheads indicate pre stenotic dilation as assessed by SICUS. The
white circle encloses the same patient’ segment of the stenosis with prestenotic dilation as
assessed by CT-Enteroclysis (panel C).

Figure 5

In panel A SICUS showed a pelvic abscess (white arrows) in a 40-year-old CD patient, which
was confirmed by CT-Enteroclysis in panel B (white circle).
12
References

1. Van Assche G, Dignass A, Panes J, et al. The second European evidence-based

Consensus on the diagnosis and management of Crohn's disease: Definitions and diagnosis. J
Crohns Colitis. 2010;4:7-27
2. Lichtenstein GR, Hanauer SB, Sandborn WJ. Management of Crohn's disease in adults.
Am J Gastroenterol. 2009;104:465-483; quiz 464, 484
3. Panes J, Bouzas R, Chaparro M, et al. Systematic review: the use of ultrasonography,
computed tomography and magnetic resonance imaging for the diagnosis, assessment of activity
and abdominal complications of Crohn's disease. Aliment Pharmacol Ther. 2011;34:125-145
4. Pallotta N, Baccini F, Corazziari E. Small intestine contrast ultrasonography (SICUS) in
the diagnosis of small intestine lesions. Ultrasound Med Biol. 2001;27:335-341
5. Parente F, Greco S, Molteni M, et al. Oral contrast enhanced bowel ultrasonography in
the assessment of small intestine Crohn's disease. A prospective comparison with conventional
ultrasound, x ray studies, and ileocolonoscopy. Gut. 2004;53:1652-1657
6. Calabrese E, La Seta F, Buccellato A, et al. Crohn's disease: a comparative prospective
study of transabdominal ultrasonography, small intestine contrast ultrasonography, and small
bowel enema. Inflamm Bowel Dis. 2005;11:139-145
7. Pallotta N, Tomei E, Viscido A, et al. Small intestine contrast ultrasonography: an
alternative to radiology in the assessment of small bowel disease. Inflamm Bowel Dis.
2005;11:146-153
8. Calabrese E, Zorzi F, Pallone F. Ultrasound of the small bowel in Crohn's disease. Int J
Inflam. 2012;2012:964720
9. Dignass A, Van Assche G, Lindsay JO, et al. The second European evidence-based
Consensus on the diagnosis and management of Crohn's disease: Current management. J Crohns
Colitis. 2010;4:28-62
10. Calabrese E, Petruzziello C, Onali S, et al. Severity of postoperative recurrence in
Crohn's disease: correlation between endoscopic and sonographic findings. Inflamm Bowel Dis.
2009;15:1635-1642
11. 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
12. Bland JM, Altman DG. Statistical methods for assessing agreement between two methods
of clinical measurement. Lancet. 1986;1:307-310
13. 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
14. Rimola J, Panes J. New Imaging Standards for Evaluation of Inflammatory Bowel
Disease? Gastroenterology. 2012
15. 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
16. Nikolaus S, Schreiber S. Diagnostics of inflammatory bowel disease. Gastroenterology.
2007;133:1670-1689
17. 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
18. Haber HP, Busch A, Ziebach R, et al. Bowel wall thickness measured by ultrasound as a
13
marker of Crohn's disease activity in children. Lancet. 2000;355:1239-1240
19. Parente F, Greco S, Molteni M, et al. Role of early ultrasound in detecting inflammatory
intestinal disorders and identifying their anatomical location within the bowel. Aliment
Pharmacol Ther. 2003;18:1009-1016
20. Pallotta N, Vincoli G, Montesani C, et al. Small intestine contrast ultrasonography
(SICUS) for the detection of small bowel complications in crohn's disease: a prospective
comparative study versus intraoperative findings. Inflamm Bowel Dis. 2012;18:74-84
21. Parente F, Maconi G, Bollani S, et al. Bowel ultrasound in assessment of Crohn's disease
and detection of related small bowel strictures: a prospective comparative study versus x ray and
intraoperative findings. Gut. 2002;50:490-495
22. Pallotta N, Baccini F, Corazziari E. Ultrasonography of the small bowel after oral
administration of anechoic contrast solution. Lancet. 1999;353:985-986
23. Calabrese E, Zorzi F, Zuzzi S, et al. Development of a numerical index quantitating small
bowel damage as detected by ultrasonography in Crohn's disease. J Crohns Colitis. 2012;6:852-
860
24. Fraquelli M, Sarno A, Girelli C, et al. Reproducibility of bowel ultrasonography in the
evaluation of Crohn's disease. Dig Liver Dis. 2008;40:860-866

14
Figure
Click here to download high resolution image
Figure
Click here to download high resolution image
Figure
Click here to download high resolution image
Figure
Click here to download high resolution image
Figure
Click here to download high resolution image