Journal of Crohn's and Colitis (2012) 6, 852–860

Available online at www.sciencedirect.com

Development of a numerical index quantitating small

bowel damage as detected by ultrasonography in

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Crohn's disease
Emma Calabrese a,⁎, Francesca Zorzi a,1 , Sara Zuzzi b,1 , Shinya Ooka a ,
Sara Onali a , Carmelina Petruzziello a , Giovanna Jona Lasinio c ,
Livia Biancone a , Carla Rossi b , Francesco Pallone a
a
Cattedra di Gastroenterologia, Universita` di Roma “Tor Vergata”, Italy
b
Centro Interdipartimentale di Biostatistica e Bioinformatica, Università di Roma “Tor Vergata”, Italy
c
Dipartimento di Statistica, Probabilità e Statistiche Applicate, Sapienza Università di Roma, Italy

Received 19 October 2011; received in revised form 23 December 2011; accepted 19 January 2012

KEYWORDS Abstract
Ultrasonography;
Small bowel Crohn's Small intestine contrast ultrasonography (SICUS) has emerged as a valuable tool in the detection of
disease; intestinal damage in Crohn's disease (CD). Our aim was to develop a numerical index quantitating
Structural damage; small bowel damage as detected by SICUS in patients with an established diagnosis of CD. One
Imaging hundred and ten patients with ileal or ileocolonic CD were prospectively enrolled and followed
up for one year. Disease activity was assessed by CDAI and CRP levels. Study variables included
bowel wall thickness, lumen diameter, lesion length and number of lesion site. Fistula, mesenteric
adipose tissue alteration, abscess and lymphnodes were also considered. Bowel segments were con-
sidered as a hollow cylinder. Standardized variations of variables were combined into a statistical
and mathematical model to create an algorithm scoring an index value ranging from 0 to 200.
Index was subdivided into a severity scale with 5 classes from the lower (A) to the higher score
(E). Median lesion index value was significantly higher (p b 0.005) in patients with a CDAI N 150
and in patients with CRP N 5 mg/l (p = 0.003). Patients classified in class E and D at SICUS underwent
surgery within one year follow up more frequently than those in class C, B and A (p b 0.0001). We
propose a new index for assessment of small bowel lesions in CD (SLIC: sonographic lesion index
for CD) developed by using SICUS. This index may turn ultrasonography in CD from a descriptive
qualitative assessment to a quantitative numerical index suitable for comparison studies.
© 2012 European Crohn's and Colitis Organisation. Published by Elsevier B.V. All rights reserved.

⁎ Corresponding author at: Cattedra di Gastroenterologia, Dipartimento di Medicina, Universita` di Roma Tor Vergata, Via Montpellier 1,
00133, Rome, Italy. Tel.: + 39 0620900969; fax: +39 0620904437.
E-mail addresses: [email protected], [email protected] (E. Calabrese).
1
FZ and SZ equally contributed to this study.

1873-9946/$ - see front matter © 2012 European Crohn's and Colitis Organisation. Published by Elsevier B.V. All rights reserved.
doi:10.1016/j.crohns.2012.01.015
Development of a numerical index quantitating small bowel damage in Crohn' disease 853

1. Background, working hypothesis and aims It is conceivable that if sonographic evaluation could be
expressed by a numerical reproducible index, SICUS would be
more easily incorporated into the overall assessment of CD
Symptoms in Crohn's Disease (CD) do not necessarily reflect patients. Hence the aim of our prospective study was to
type and severity of intestinal changes, often leading to mul- develop a quantitative sonographic index for ileal lesions in CD.
tiple imaging procedures mostly involving cross sectional ra-
diation based techniques. 1 Data have been provided to show
that age less than seventeen at diagnosis and severity of dis-
ease were associated with higher radiation doses 2 and that
2. Study population
CD patients were exposed to 2.46 times more diagnostic ion-
izing radiation than patients with ulcerative colitis (UC). 3 The study was conducted over a two years period including
Ultrasonography (US) and magnetic resonance imaging one year clinical follow-up. One hundred and ten patients
(MRI) have emerged as valuable tools in detecting intestinal with ileal or ileocolonic CD were enrolled [n = 65 male (59%);
lesions and in evaluating disease activity in CD. 4–12 Both median age: 42 yrs (range: 14–79 yrs); disease duration: medi-

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methods do not use radiation, the former ensuring a real- an 108 mos, (range: 12–528)]. Diagnosis, CD location and pa-
time point of care assessment and the latter a high quality tients' assessment were made according generally accepted
contrast resolution of soft tissue. A meta-analysis of pro- recommendations. 1,19,26,27 Seventy eight patients (70.9%)
spective studies showed variable diagnostic accuracy had pure ileal disease, 32 (29.1%) had ileal disease with
among US, MRI, Scintigraphy, Computed Tomography (CT), cecal involvement were classified as ilecolonic according to
and positron emission tomography in inflammatory bowel the Montreal criteria. 28 In 11 pts there were additional sites
disease (IBD). 11 Due to the need of frequent disease re- of involvement in the upper GI tract. Among enrolled patients,
evaluation, these observations add support to the view 52 (47.3%) had a primary CD, 58 (52.7%) had post-operative
that the use of radiation free imaging modality is recurrence after at least one ileocolonic resection [median
preferable. 11 interval between ileocolonic resection and sonographic
US is a low cost, non invasive, radiation free imaging mo- assessment 48 mos (range 6–420 mos)]. Since our aim was to
dality that is gaining wider acceptance in gastroenterology develop numerical index quantitating ileal damage in CD, we
and it is chosen as the first-line imaging procedure for diag- amplified our study population with those patients who were
nosis of CD more frequently in Europe than in United likely to have a pure ileal diasease. Among these those with
States. 13 Studies, in unselected groups of patients, have postoperative recurrence that is in the vast majority of
shown that US may diagnose CD with a sensitivity of patients initially ileal (neo terminal ileum) were included. 22
67–96% and specificity of 79–100% and that degree and ex- Median CDAI was 106, range 6–462. Median CRP was 2.35
tent of bowel wall thickening on US correlate with clinical (range 0.1–43 mg/L). Clinical characteristics of patients
and biochemical parameters in children and young enrolled in the study are shown in Table 1.
adults. 14,15 Sensitivity of US in detecting CD lesions in the
ileum has been reported as high as 90% while US accuracy 3. Ultrasonographic assessment
for upper small bowel and rectum appeared to be lower. 17
The use of oral contrast agents such as iso-osmolar polyeth- SICUS was performed in all patients by one experienced op-
ylene glycol (PEG) has been shown to increase sensitivity in erator. The patients were examined in the fasting state
defining disease site, 7,8 extent 4,8 and bowel complications without any preparation. SICUS was performed as previously
in small bowel CD 16 and to reduce inter- and intra-observer described, 7,18,28 after the ingestion of 375 mL (range
variability. 8 Thus, Small Intestine Contrast Ultrasonography 250–500 mL) of PEG using a convex transducer (3.5–5 MHz)
(SICUS) has been proposed to accurately define CD intestinal and a high frequency linear-array transducer for details
damage for either initial assessment or monitoring progres- (5–12 MHz) (Hitachi, EUB 6500, Japan). Median SICUS dura-
sion over time. 4,7,8,17,18 tion was 40 min (range 35–90 min). No patient was obese
Drawbacks in the routine use of SICUS in CD include the as to prevent appropriate sonographic assessment and tech-
lack of precise criteria to define bowel involvement and nically adequate scans were obtained in all patients. Sono-
quantify ileal lesions severity. Numerical indices of what graphic findings included: increased bowel wall thickening
has been called clinical activity have been developed and (W N 3 mm) for at least 4 cm 7,10; small bowel dilation (DD),
the Crohn's disease activity index (CDAI) is now widely used defined as a lumen diameter ≥ 25 mm; small bowel stricture
in the everyday practice of most IBD centers and in clinical (DN) defined as lumen diameter b 10 mm, measured at the
research. 19 Indices and scores have been developed for level of maximally distended loop, independently on preste-
assessing degree and severity of luminal inflammation in notic dilation; fistulas, defined as hypoechoic tract with or
those areas that can be reached by an endoscope, namely without hyperechoic content; mesenteric adipose tissue al-
the Crohn's disease Endoscopic Index of severity (CDEIS), teration 29 and lymphnodes 30; abscess identified as roundish
the Simplified Endoscopy Score (SES-CD) and, in the postop- anechoic lesions, with an irregular wall, often presenting in-
erative setting, the Rutgeerts' score. 20–22 These instruments ternal echoes and posterior echo enhancement. 7
are currently the standard by which the efficacy of drugs and
products is assessed in clinical trials.
While the problem of quantitating clinical judgment and 4. Index construction
endoscopic appearance has been solved, the issue of quanti-
tating sonographic images is still open. Different studies The construction of the lesion index was based on continu-
have been published in this area with no conclusive data 23–25 ous, discrete and dichotomous variables used for describing
854 E. Calabrese et al.

Table 1 Clinical and biological characteristics of 110 to develop lesion index. A wide variability of these variables
patients at inclusion in the study. was observed in a continuous and segmented damaged bowel
tract and different values of W, DN (narrowing diameter) and
Male, n (%) 65 M
DD (dilation diameter) were observed in each patient (Fig. 2,
Age, median (range) 42 yrs
panel A to H). At this purpose damaged bowel lesions were
Duration of disease (median, mos) 108
divided on segments (small hollow cylinders) named as i,
Disease location
ranged from 1 to n (n ≥ sites number). Wij, DNij, DDij, LWij (le-
– Ileal, n (%) 78 (70.3%)
sion length of hollow wall thickening) LDNij (lesion length of
– Ileocolonic, n (%) 32 (28.8%)
the lumen narrowing) and LDDij (lesion length of lumen
– Associated upper GI lesions n (%) 11 (9.9%)
dilation) were identified. Therefore the following areas
Disease behavior
(for patient j and segment i) were calculated (Eq. (1)):
– Penetrating 22 (20%)
– Stricturing 65 (59%) AW ij ¼ W ij ⋅Lij ; ADNij ¼ DNij ⋅Lij ; ADDij ¼ DDij ⋅Lij ð1Þ
– Non penetrating non stricturing 23 (2 1%)

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CDAI, median (range) 106 (6–462)
Normal bowel parameters defined as W0 = 3 mm,
Previous surgery, n (%) 58 (52.3%)
DN0 = 10 mm and DD0 = 25 mm 7,10,28,32 were used to calculate
CRP (mg/L), median (range) 2.4 mg/dL (0.1–43)
the benchmark areas (Eq. (2)) and were compared with a
Yrs, years; CRP, C-Reactive Protein; GI, gastrointestinal. damaged bowel area in each patient j (Eq. (3))

AW i0 ¼ 3 mm⋅Lij ; ADNi0 ¼ 10 mm⋅Lij ; ADDi0 ¼ 25 mm⋅Lij

lesions in each patient. Bowel wall thickening (W), lumen (D) ð2Þ
and length of the lesion (L) were considered as continuous
variables; number of lesion sites (sites number) was



ΔAW ij ¼ W ij −3 ⋅Lij ; ΔADNij ¼ DNij −10 ⋅Lij ; ΔADDij ¼ DDij −25 ⋅Lij
considered as discrete variable while abscesses, fistulas,
mesentery adipose tissue alteration and lymphnodes were ð3Þ
considered as dichotomous variables. This process scoring
Every damaged bowel tracts i, for each patient j, were
was conducted in several steps. All variables that influenced
summed to determine the total area variations ΔAWj,
disease severity were weighted according to a consensus by
ΔADNj, ΔADDj (Eq. (4)). These variations added to lesions
using a Delphic approach. 31
sites number matched as measures of the disease lesion
Bowel segments were considered as a hollow cylinder
magnitude for each patient j.
(Fig. 1, panel A), where W represented difference in terms
of bowel wall thickening between internal diameter and ex-
X
n X
n X
n
ternal cylinder, D was considered as the internal diameter ΔAW j ¼ ΔAW ij ; ΔADNj ¼ ΔADNij ; ΔADDj ¼ ΔADDij
cylinder and L was considered as length (Fig. 1, panel B). i¼1 i¼1 i¼1
Uninvolved and damaged bowel segments were differentiat- ð4Þ
ed on the basis of W and D values. Hollow cylinder is a three-
dimensional figure whereas US is a bi-dimensional image ΔAWj, ΔADNj, ΔADDj quantities and site numbers had dif-
technique that analyzes longitudinal area of the bowel wall ferent nature, magnitude and scales. Therefore a standardi-
(AW) and longitudinal area of the bowel lumen (AD). Hence zation procedure in order to delete possible confounding
AW given by W and L and AD, given by D and L were included factors due to these aspects was considered and applied.

Figure 1 Schematic representation of the intestine as a hollow cylinder. Panel A: W: bowel wall thickening; D: bowel lumen; L:
lesion length. Panel B: Longitudinal section of lumen (AD); longitudinal section of bowel wall thickening (AW).
Development of a numerical index quantitating small bowel damage in Crohn' disease 855

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Figure 2 Drawing shows bowel wall thickening, lumen diameter and lesion extent variations of CD patient. Lesion is subdivided in
eight hollow cylinders as visualized and measured by SICUS. Every cylinder corresponds to a sonographic picture showing defined pa-
rameters (Panel A to H). SLIC was 103.6, class and I.dicho were respectively D and D0.

More precisely, all continuous variables (ΔAW, ΔADN, ΔADD) o The variability intervals of ΔADD were selected fixing the variability
were associated to severity classes as followed: interval of DD and varying the range of LDD, since DD and LDD had
not the same degree of relevance. Severity classes were assigned
to ΔADD.
• Variability range of W, DN, DD, LW, LDN, LDD and sites number
were subdivided into intervals and proper thresholds according
to current sonographic data available in published stud- In a continuous scale, the standardized transformation was
ies7,10,28,32 and weighted by consensus.31 assessed by using the segmented linear function proposed by
• ΔAW, ΔADN, ΔADD thresholds were taken into account for deter- Ott and Hunt. 33 Regarding the discrete variable, sites number,
mining different classes of disease lesions for each variable. a different standardization procedure was evaluated and a
• A final common scale for the standardized values was assessed. common scale value was assigned according to the increasing
number of sites. Four standardized variables as specific con-
In a decreasing order of severity, the following ranking tinuous indices (from 0 to 200) of bowel wall thickening
was obtained by consensus: 1) DD, 2) DN, 3) W and L and (I.W), lumen narrowing (I.DN), lumen dilation (I.DD) and num-
was included into the standardization procedure of ΔAW, ber of sites (I. sites number) were developed. On the basis of
ΔADN, ΔADD. Classes of severity were defined by a numerical the international experts' opinion 31 different weights (normal-
and arbitrary common scale ranged from 0 to 200. ized at 1) of all variables were added to develop final synthetic
The introduction of the ranking into standardization pro- index. Hence a quantitative sonographic lesion index,
tocol led to choices to associate the variability ranges of I = (0,200] (Eq. (5)) was derived by weighted average (Fig. 3).
ΔAW, ΔADN, ΔADD to severity classes: " # " #
Xn Xn
Ij ¼ α ΔW ij ⋅LWij þβ ΔDNij ⋅LDNij
o The variability intervals of ΔAW were selected following the area
magnitude natural order, since W and L had the same degree of
"
i¼1 #
STAND i¼1 STAND
Xn
relevance. Hence the severity classes were assigned to ΔAW; þγ ΔDDij ⋅LDDij þ λ½n:sitesSTAND ð5Þ
o The variability intervals of ΔADN were selected fixing the vari- i¼1 STAND
ability interval of DN and varying the range of LDN, since DN and
LDN had not the same degree of relevance. Severity classes Using R software platform a packed script for calculating
were assigned to ΔADN; lesion index was developed. The Sonographic Lesion Index
856 E. Calabrese et al.

for CD (SLIC) was obtained from all 110 patients (Fig. 4). SLIC
values ranged from 1.4 to 200 in these patients with a medi-
an value of 39.6. Fig. 2 shows how small bowel sonographic
imaging in a CD patient was subdivided in eight hollow cylin-
ders as visualized and measured by SICUS (pictures A to H)
giving in this patient a SLIC measurement of 103.6.
Thus, the SLIC index was developed comprehensively includ-
ing all parameters that can be evaluated by US and representing
a measurement of structural small bowel damage as expressed
in terms of bowel wall thickening, lesion length, strictures.

5. Clinical activity and short term outcome

according to SLIC

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Figure 4 Values distribution of SLIC obtained from 110 CD
patients.
While SLIC per se offers a quantitative approach to the use of
SICUS in CD, we also explored whether and how SLIC might be
best suited for clinical assessing and monitoring CD patients. A median CDAI of 86 (range: 41–249) and 22 out of 29 had a re-
severity scale with 5 classes was therefore derived based on current disease after surgery.
different grouping of the SLIC index (I) values from the lowest Median SLIC index value was 48.3 (range 5–200) in pa-
to the highest: class A, I ∈ (0,20]; class B, I ∈ (20,40]; class C, I tients with clinically active disease as defined by a CDAI
∈ (40,60]; class D, I ∈ (60,120]; class E, I ∈ (120,200]. above 150 and 32.4 (2.8–200) in patients with a CDAI less
Characteristics and differences of the five classes' pa- than 150 (p = 0.005) (Fig. 5, panel A). Likewise in patients
tients are shown in Table 2. The 5 patients classified in with CRP N 5 mg/L median SLIC value was significantly higher
class E had a median CDAI of 253 (range: 63–291). Two out than that of patients with CRP b 5 mg/L [54.4 (range 5.5–
of 5 had a recurrent disease after surgery (time from surger- 200) vs 33.8 (1.4–110.4), p = 0.003) (Fig. 5, panel B).
y N 2 years). Twenty-four patients were included in class D Twelve of the 110 enrolled patients underwent urgent or
with a median CDAI of 111 (range: 12–409). Six out of 24 elective surgical bowel resection within one year follow up.
had a recurrent disease after surgery. The 26 patients in Among these, there were 4 out of the 5 patients classified in
class C had a median CDAI of 109.5 (range: 7–462). In class class E and 7 out of the 24 classified in class D. In contrast,
C 12 out of 26 had a recurrent disease after surgery. surgery was required only in one patient out of 26 in class
Twenty-six patients were in class B with a median CDAI of C and none in classes B and A (p b 0.0001) (Fig. 6). Median
104.5 (range: 11–379) and 13 out of 26 had a recurrent dis- SLIC was 88 (range 25.4–200) in those patients undergoing
ease after surgery. In class A there were 29 patients with a surgery within one year. Five patients required full dose

Figure 3 Algorithm of SLIC development.

Development of a numerical index quantitating small bowel damage in Crohn' disease 857

Table 2 Characteristics and differences of the five classes' patients.

Pts Median age Disease duration Number of patients with time Median CDAI Median SLIC
(range) (mos) interval between SICUS and (range) (range)
ileocolonic resection N 2 yrs
Class E 5 37(37–50) 180(144–324) 2 253 (63–291) 128.2 (119–200)
Class 24 35(18–69) 108(12–408) 6 (3 pts less than 2 yrs) 111 (12–409) 72.4 (64.8–110.4)
D
Class 26 46(21–75) 144(12–528) 12 (2 pts less than 2 yrs) 109.5 (7–462) 46.3 (40.8–59.8)
C
Class B 26 45(18–79) 36(12–456) 13 (l0 pts less than 2 yrs) 104.5 (11– 379) 29.6 (21.2–38.8)
Class A 29 41(18–72) 96(12–492) 22 (l3pts less than 2 yrs) 86 (41–249) 10.3 (1.4–18.3)

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corticosteroid treatment during one year follow up. Among variables reflecting extraparietal damage could be incorporat-
these five, there were 2 out of the 5 patients classified in ed to potentially correct class allocation based on SLIC.
class E and 2 of the 24 classified in class D, while steroids Dichotomous variables (abscess, fistula, mesenteric
were required only in one out of 26 in class C and none in adipose tissue alteration, lymphnodes) were then added to
classes B and A. Five patients were lost at follow up, 2 in the index on the basis of weights of the international experts'
class D, 1 in class C, 1 in class B and 1 in class A respectively. opinion as well, 31 hence a dichotomous index was developed
(I.dicho). In a decreasing order of severity, the following
ranking was obtained: 1) abscess, 2) fistula, 3) mesenteric
6. Additional variables that may affect severity
adipose tissue alteration, 4) lymphnodes. The following scale
scale allocation defined the dichotomous index:

SLIC and consequent severity scale class allocation were based • I.dicho = 0 if all dichotomous variables were absent.
on discrete and continuous variables reflecting parietal intes- • I.dicho = 1 if mesenteric adipose tissue alteration and/or lymph-
tinal damage. We have also explored whether dichotomous nodes were present and other dichotomous variables were absent.

Figure 5 Relation of median SLIC with CDAI and CRP. Panel A: Median lesion index value was significantly different in patients with
CDAI b 150 vs patients with CDAI N 150 (p = 0.005). Panel B: Median lesion index was significantly different in patients with CRP N 5 mg/L
vs patients with CRP b 5 mg/L (p = 0.003).
858 E. Calabrese et al.

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Figure 6 Patients' outcome during one year clinical follow-up. Patients classified in class E and D at SICUS underwent surgery within
one year more frequently than those in class C, B and A (p b 0.0001).

• I.dicho = 2 if fistula was present, abscesses was absent and other and is simple to calculate using a dedicated software program.
dichotomous variables (mesenteric adipose tissue alteration, The mathematical algorithm can be easily adjusted based on
lymphnodes) were either absent or present. new technical development e.g. oral and intravenous contrast
• I.dicho = 3 if abscess was present and other dichotomous vari-
(data unpublished). SLIC entirely relies on precise and specific
ables (fistula, mesenteric adipose tissue alteration, lymphnodes)
data recording. We here reported the construction of the
were either absent or present.
index and showed that SLIC depicts SICUS detected changes
providing suggestion that SLIC may reflect disease severity.
The following scale described the combination of the SLIC Inter-observer agreement between sonographers with vari-
index classes I (A, B, C, D, E) and the dichotomous index able experience in US has been reported as good in a few pre-
I.dicho: liminary studies showing satisfactory results, but a learning
curve for this technique is still lacking. 34 Agreement between
• A0, A1, A2, A3 paired evaluations in the same patients and between opera-
• B0, B1, B2, B3
tors will be the next step. A limit of our calculated index is
• C0, C1, C2, C3
in further differentiating patients that have values higher
• D0, D1, D2, D3
• E0, E1, E2, E3 than W N 15 mm or L N 400 mm or DD N 75 mm because they
will be scored as maximum value. In our preliminary results
all these patients that had these values were those that devel-
Taking as an example the small bowel changes shown in
oped severe disease and achieving surgery or major therapeu-
Fig. 2 class allocation in the severity scale would be D and
tic options for CD (4 out of 5 class E patients undergone
I.dicho would be D0.
surgery).
While this manuscript was in preparation, the process of
7. Comment developing a new scoring system, the Crohn's Disease
Digestive Damage Score (the Lémann score) was
The present study describes the methodology for developing a introduced. 35 Such a score should take into account damage
suitable instrument for assessing small bowel CD and creating location, severity, extent, progression and reversibility as
a quantitative lesion index using SICUS. SLIC takes into ac- measured by diagnostic imaging modalities, portraying
count both the extent and severity of the small bowel damage, patients' disease course and progression. We here report
including stricturing and penetrating lesions as assessed by how we have developed and constructed a new instrument
SICUS. SLIC also offers the potential for evaluating the pro- for quantitating small bowel damage as detected by SICUS.
gression of the small bowel disease over a period of time We have here also shown that this instrument can be
through serial assessment and possible changes after treat- incorporated into the overall clinical assessment of CD pa-
ments. SLIC meets the goal of incorporating items intuitively tients, expectedly offering a novel tool for comparison
considered as important by experienced gastroenterologists studies in CD.
Development of a numerical index quantitating small bowel damage in Crohn' disease 859

Conflict of interest 10. Fraquelli M, Colli A, Casazza G, Paggi S, Colucci A, Massironi S,

et al. Role of US in detection of Crohn disease: meta-analysis.
Radiology 2005;236(1):95–101.
None. 11. Horsthuis K, Bipat S, Bennink RJ, Stoker J. Inflammatory bowel
disease diagnosed with US, MR, scintigraphy, and CT: meta-analysis
of prospective studies. Radiology 2008;247(1):64–79.
Acknowledgments 12. Schreyer AG, Menzel C, Friedrich C, Poschenrieder F, Egger L,
Dornia C, et al. Comparison of high-resolution ultrasound and
MR-enterography in patients with inflammatory bowel disease.
The authors thank the participation of C. Bernstein, Y. World J Gastroenterol 2011;17(8):1018–25.
Chowers, JF Colombel, M. Cottone, I. Dotan, R. Eliakim, R. 13. Nikolaus S, Schreiber S. Diagnostics of inflammatory bowel disease.
Fedorak, A. Forbes, M. Gassull, P. Gibson, S.B. Hanauer, H. Gastroenterology 2007;133(5):1670–89.
Lochs, D. Jewell, P. Michetti, P. Munkholm, C. Prantera, P. 14. Maconi G, Parente F, Bollani S, Cesana B, Bianchi Porro G.
Rutgeerts, J. Schoelmerich, D. Strobel, S. Travis and M. Abdominal ultrasound in the assessment of extent and activity
Vecchi. of Crohn's disease: clinical significance and implication of bowel

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The authors thank the useful discussion and software as- wall thickening. Am J Gastroenterol 1996;91(8):1604–9.
sistance of Dr. Mario Santoro, Department of Mathematics, 15. Haber HP, Busch A, Ziebach R, Stern M. Bowel wall thickness
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Università of Rome “Tor Vergata”; Dr. Emanuela Visconti
in children. Lancet 2000;355(9211):1239–40.
for the management of patients during ultrasonography; Dr 16. Pallotta N, Vincoli G, Montesani C, Chirletti P, Pronio A,
Christian Rosati for the technical support. Caronna R, et al. Small intestine contrast ultrasonography
Ethics approval: this study was conducted with the ap- (SICUS) for the detection of small bowel complications in crohn's
proval of the University of Rome “Tor Vergata”. disease: A prospective comparative study versus intraoperative
This manuscript was supported by “Fondazione Umberto findings. Inflamm Bowel Dis 2012;18(1):74–84.
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