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Ileocolic versus Small-Bowel

Intussusception in Children: Can
US Enable Reliable Differentiation?1
Original Research

Natali Lioubashevsky, MD
Purpose: To assess clinical and ultrasonographic (US) criteria that
Nurith Hiller, MD
can be used to confidently differentiate ileocolic from
Katya Rozovsky, MD
small-bowel intussusception.
Lee Segev, MD
Natalia Simanovsky, MD Materials and Institutional review board approval was obtained for this
Methods: retrospective study, and the need to obtain informed con-
sent was waived. US and clinical data for children given
a diagnosis of intussusception in the years 2007 through
2011 were evaluated. The diameters of the intussusception
and the inner fat core, the outer bowel wall thickness,
and the presence or absence of lymph nodes inside the
intussusception and mesentery were noted. The Student
t test, the Mann-Whitney test, and the Levene test were
used for comparison of parametric variables, while the
x2 and Fisher exact tests were used for comparison of
categoric data.

Results: There were 200 cases of intussusception in 174 patients

(126 boys, 48 girls; mean age, 17.2 months (range, 0
years to 7 years 1 month); 57 (28.5%) were small-bowel
and 143 (71.5%) were ileocolic intussusceptions. Mean
lesion diameter was 2.63 cm (range, 1.3–4.0 cm) for ileo-
colic versus 1.42 cm (range, 0.8–3.0 cm) for small-bowel
intussusception (P , .0001). Mean fat core diameter was
1.32 cm (range, 0.6–2.2 cm) for ileocolic versus 0.1 cm
(range, 0–0.75 cm) for small-bowel intussusception (P ,
.0001). The ratio of inner fat core diameter to outer wall
thickness was greater than 1.0 in all ileocolic intussuscep-
tions and was less than 1.0 in all small-bowel intussuscep-
tions (P , .0001). Lymph nodes inside the lesion were
seen in 128 (89.5%) of the 143 ileocolic intussusceptions
versus in eight (14.0%) of the 57 small-bowel intussuscep-
tions (P , .0001). Children with ileocolic intussusception
had more severe clinical symptoms and signs, with more
vomiting (P = .003), leukocytosis (P = .003), and blood in
the stool (P = .00005).

Conclusion: The presence of an inner fatty core in the intussuscep-

tion, lesion diameter, wall thickness, the ratio of fatty core
thickness to outer wall thickness, and the presence of
lymph nodes in the lesion may enable reliable differenti-
ation between ileocolic and small-bowel intussusceptions.
1
From the Department of Medical Imaging, Hadassah–He-
brew University Medical Center, POB 24035, Jerusalem, q
RSNA, 2013
Israel 91120. Received November 28, 2012; revision
requested January 4, 2013; revision received March 2;
accepted March 11; final version accepted April 4. Address
correspondence to N.S. (e-mail: natalias@hadassah.org.il).

q
RSNA, 2013

266 radiology.rsna.org n Radiology: Volume 269: Number 1—October 2013

PEDIATRIC IMAGING: Can US Help Differentiate between Ileocolic and Small-Bowel Intussusception?
I
ntussusception is one of the most
common pediatric abdominal emer-
gencies, with 80% of cases occur-
ring in patients younger than 2 years
(1). The diagnosis is usually achieved
with ultrasonography (US), which has
a sensitivity and a specificity of close
to 100% in experienced hands (2). The
classic US appearance of intussuscep-
tion has been described as a pseudokid-
ney or doughnut sign (3,4).
The choice of treatment depends
on the type of intussusception. Ileoco-
lic intussusception without evidence of
necrosis requires reduction by enema,
with 24-hour follow-up owing to the
possibility of recurrence, and surgical
reduction in cases where enema is un-
successful (5). Reduction is achieved by
means of enema alone in 80%–95% of
cases (5,6). Immediate surgery is indi-
cated when there are signs of necrosis
(5). The relative frequency of small-
bowel intussusception varies in the lit-
erature between 1.6% and 25% of all
cases of intussusception (6,7). Most in-
vestigators have found that small-bowel
intussusception can be safely moni-
tored and will reduce spontaneously
without surgical intervention (8–10),
although Ko et al (11) and Munden et al
(12) found that persistent small-bowel
intussusception often has an associated
lead point or bowel necrosis and neces-
sitates surgery.
Advances in Knowledge
nn The ratio of hyperechoic inner fat
core diameter to wall thickness is
a useful parameter enabling con-
fident differentiation between
ileocolic intussusception (ratio,
.1.0) and small-bowel intussus-
ception (ratio, ,1.0) at US in
children (P , .0001).
nn The presence of lymph nodes
inside the intussusception and
larger lesion diameter also con-
tribute to a definitive diagnosis;
lymph nodes inside the lesion
were seen in 128 (89.5%) of 143
ileocolic intussusceptions versus
in eight (14.0%) of 57 small-
bowel intussusceptions
(P , .0001).
Radiology: Volume 269: Number 1—October 2013
US findings for both types of in-
tussusception are often similar, and
the decision regarding appropriate
intervention may thus be complex.
The presence of lymph nodes inside
the intussusception and its diame-
ter have been described as helpful
(6,10,12,13). In the works of Park
et al (13) and Tiao et al (9), diame-
ter was significantly larger in ileocolic
intussusception; however, reported
measurements of lesion diameter and
length in ileocolic and small-bowel in-
tussusception have overlapped. Other
features that might increase diagnostic
specificity have been reported in small
series of patients, but no reliable crite-
ria have been found to safely differen-
tiate between ileocolic and small-bowel
intussusception.
We aimed to determine whether
there are clinical and US parameters
that will enable reliable differentiation
between ileocolic and small-bowel in-
tussusception, thus allowing optimal
clinical management and preventing un-
necessary enema intervention.
Materials and Methods
Patients
Institutional review board approval was
obtained for this retrospective study,
and the need to obtain informed con-
sent was waived. The study included
all consecutive pediatric patients who
were given a diagnosis of intussus-
ception and who were registered with
an appropriate diagnosis code for in-
tussusception in our hospital during
a 5-year period beginning in January
2007. Repeat intussusception episodes
during the same hospital admission
or occurring within 1 week from the
first admission were excluded from the
study. Intussusception events in the
same child more than 1 week after the
Implication for Patient Care
nn A definitive diagnosis of ileocolic
versus small-bowel intussuscep-
tion enables a confident choice
between urgent reduction and
conservative management.
n radiology.rsna.org
Lioubashevsky et al
first episode were considered as sepa-
rate illnesses and were included in the
study as independent cases. All the ex-
aminations at admission to the emer-
gency department were performed by
residents or senior radiologists (in-
cluding N.L., K.R., and N.S.) with or
without pediatric radiology training.
Multiple transverse and longitudinal
images of the lesion are routinely ob-
tained in our department as part of
our standard protocol.
Demographic and clinical parame-
ters—including sex; age; and presence
of fever, abdominal pain, vomiting, and/
or blood in the stool—as well as physi-
cal examination and laboratory findings
(eg, abdominal distention, presence of
palpable mass, leukocytosis) and the
outcome after enema or surgery were
retrospectively obtained from clinical
records.
US studies of all patients in the
study were performed with either ATL
HDI 5000 or HD 11 machines (Phil-
ips Healthcare, Eindhoven, the Neth-
erlands) by using small convex 5- to
8-MHz and linear 7- to 12-MHz trans-
ducers appropriate to the child’s size
and body habitus.
US images were retrospectively re-
evaluated in consensus on the hospital’s
picture archiving and communication
system (Centricity PACS; GE Health-
care, Milwaukee, Wis) by two radiolo-
gists (N.S., with 20 years of experience
performing and interpreting pediatric
US studies, and N.L., with 14 years of
experience). The reference standard
diagnosis was obtained from surgical
records in cases where surgery was
Published online before print
10.1148/radiol.13122639 Content codes:
Radiology 2013; 269:266–271
Author contributions:
Guarantors of integrity of entire study, N.L., N.H., N.S.;
study concepts/study design or data acquisition or data
analysis/interpretation, all authors; manuscript drafting
or manuscript revision for important intellectual content,
all authors; manuscript final version approval, all authors;
literature research, all authors; clinical studies, N.L., N.H.,
K.R., N.S.; statistical analysis, N.L., L.S.; and manuscript
editing, N.H., K.R., N.S.
Conflicts of interest are listed at the end of this article.
267
PEDIATRIC IMAGING: Can US Help Differentiate between Ileocolic and Small-Bowel Intussusception?
performed (22 ileocolic intussuscep-
tions and one small-bowel intussuscep-
tion [three of these 23 intussusceptions
were later excluded from analysis be-
cause of the presence of mass lesions]),
from the results of enema examinations
(121 ileocolic and three small-bowel in-
tussusceptions), or on the basis of clin-
ical outcome (observation for at least
24 hours, until spontaneous reduction
occurred, as confirmed at follow-up US)
in cases of small-bowel intussusception
(56 small-bowel intussusceptions, in-
cluding the three treated with enema
examination).
The presence of free peritoneal
fluid or enlarged mesenteric lymph
nodes outside the lesion was recorded.
The anteroposterior diameter of the
lesion, the diameter of the inner fat
core, and the thickness of the outer
wall were measured (Fig 1). In cases
when the inner fat core was too thin to
be reliably measured, it was assigned a
thickness of 0.01 mm. The core-to-wall
index was calculated as the ratio of the
fat core diameter to the wall thickness
on the transverse image that showed
the maximal thickness of central hyper-
echoic fat tissue. The presence or ab-
sence of lymph nodes inside the lesion
was noted. Measuring the true length
of the intussusception retrospectively
on images was difficult and unreliable;
therefore, we abandoned the attempt
to analyze this parameter.
In one case of small-bowel intussus-
ception in a 6-year-old boy, US revealed
the lead point. The patient underwent
surgery, and histopathologic examina-
tion revealed Hodgkin lymphoma. In
two patients with ileocolic intussuscep-
tion, the lead point was seen at US. At
surgery, a hamartomatous polyp was
seen in one patient, and Meckel diver-
ticulum was found in the second child.
We believed that an obvious mass lesion
inside the intussusceptum in these three
cases had caused displacement and
compression of the fat component, pre-
cluding reliable measurement of the fat
core. These three cases were included
in comparisons of clinical findings and
general US presentations, but they were
excluded from measurements such as
lesion diameter and core-to-wall index.
268
Lioubashevsky et al
Statistical Analysis Figure 1
Statistical analysis was performed for
parametric variables such as intussus-
ception diameter, wall thickness, and
fat core thickness by using the Stu-
dent t test, the Mann-Whitney test,
and the Levene test; for categoric data
such as the presence of lymph nodes
or free abdominal fluid the x2 test and
the Fisher exact test were used (P ,
.05 was considered to indicate a signif-
icant difference). Multiple comparisons
with use of the Bonferroni adjustment
were performed to confirm the uni-
variate analysis results (P , .0001).
Multiple logistic regression analysis
was performed to adjust for potential
confounding. The data analysis was
performed by using statistical software
(SAS, version 9.1e; SAS Institute, Cary,
NC).
Results
A total of 200 cases of intussusception
in 174 patients (126 boys and 48 girls;
mean age, 17.2 months; range, 0 years
to 7 years 1 month) were included in
the study, including 143 cases (71.5%)
of ileocolic intussusception and 57 cases
(28.5%) of small-bowel intussuscep- Figure 1: (a) Schematic demonstration of
tion. A total of 197 cases (141 ileoco- measurement technique in ileocolic intussusception.
lic intussusceptions and 56 small-bowel Solid line = lesion diameter, dashed line = inner fat
intussusceptions) were included in the core, dotted line = outer wall thickness. (b) Typical
statistical analysis of lesion parameters. US appearance of 26-mm ileocolic intussusception
Seventeen patients had two intussus- in an 11-month-old boy. Of note are the large
ception events during the study period, diameter (solid arrow), thick (3.5 mm) outer wall
and five patients had three events each (dotted arrow), and obvious 5.7-mm internal fat
(26 cases of intussusception). Seven core (dashed arrow). The core-to-wall index is 1.63
patients had episodes of different types (5.7/3.5). LN = lymph node.
of intussusception, nine patients had
repeated ileocolic intussusception, and
five had multiple episodes of small-bow- 143 ileocolic intussusceptions and 38
el intussusception. (66.7%) of the 57 small-bowel intussus-
Mean age was 14.2 months 6 9 ceptions occurred in boys (P = .29). Re-
(standard deviation) (range, 0 years to sults of statistical analysis of the clinical
5 years 6 months) for the patients with symptoms at admission are summarized
ileocolic intussusception and was 25.3 in Table 1. Blood in the stool, vomiting,
months 6 20 (range, 3 months to 7 and leukocytosis were significantly
years 1 month) for patients with small- more common in patients with ileoco-
bowel intussusception. The difference lic intussusception (P = .0005, .03, and
was statistically significant according .03, respectively).
to both the Student t test (P = .0001) Presence of lymph nodes inside the
and the Levene test (P = .0002). There lesion (Table 2) and presence of free peri-
was no difference in sex distribution be- toneal fluid were significantly more likely
tween the groups; 100 (69.9%) of the to occur in ileocolic intussusceptions.
radiology.rsna.org n Radiology: Volume 269: Number 1—October 2013
PEDIATRIC IMAGING: Can US Help Differentiate between Ileocolic and Small-Bowel Intussusception? Lioubashevsky et al

The typical US appearance of ileocolic Table 1

intussusception is demonstrated in Fig-
ure 1. The presence of echogenic fatty Results of Statistical Analysis of Clinical Symptoms at Admission in Cases of Ileocolic
tissue in the center of the intussuscep- and Those of Small-Bowel Intussusception
tion was noted in all patients in the ileo- Parameter Ileocolic Intussusception (n = 143) Small-Bowel Intussusception (n = 57) P Value
colic intussusception group. Conversely,
small-bowel intussusceptions typically Blood in stool 57 (39.9) 3 (5.3) .00005
Vomiting 108 (75.5) 22 (38.6) .003
had a multilayered “double ring” appear-
Leukocytosis 29 (20.3) 1 (1.8) .003
ance and demonstrated no or minimal
Fever  38°C 16 (11.2) 7 (12.3) .606
linear echogenic fat tissue in the center
Abdominal distention 13 (9) 0 .075
(Figs 2, 3). The presence of mesenteric
Palpable mass 13 (9) 1 (1.8) .159
lymph nodes outside the lesion did not
differ in ileocolic (95 of 143 lesions) ver- Note.—Data are numbers of cases of intussusception, with percentages in parentheses.
sus small-bowel (43 of 57 lesions) intus-
susception (P = .092).
For all ileocolic intussusceptions, Table 2
the fat core–to-wall index was greater
than 1.0. In comparison, the inner fat US Parameters and Measurements in Ileocolic and Small-Bowel Intussusceptions
core–to-wall index was less than 1.0 in Ileocolic Intussusception Small-Bowel Intussusception
35 of 56 small-bowel intussusceptions Parameter (n = 143) (n = 57) P Value
(Table 2). The inner fat core was not
identifiable or was too thin for reliable Lymph nodes inside the 128 (89.5) 8 (14.0) ,.0001
measurement in the remaining 21 pa- intussusception
tients. This is helpful in cases of edem- Mesenteric lymph nodes 95 (66.4) 43 (75.4) .092
Free peritoneal fluid 42 (29.4) 6 (10.5) .007
atous bowel wall resulting in increased
Diameter (cm)* 2.63 6 0.4 (1.4–4.0) 1.42 6 0.39 (0.8–3.0) ,.0001
small-bowel intussusception diameter,
Diameter of fat core (cm)* 1.32 6 0.36 (0.6–2.2) 0.1 6 0.26 (0–0.75) ,.0001
as seen in a patient with edematous
Outer wall thickness (cm)* 0.6 6 0.13 (0.3–1.0) 0.42 6 0.12 (0.3–0.9) ,.0001
bowel wall caused by Henoch-Schönlein
Core-to-wall index* 2.28 6 0.57 (1.3–3.2) 0.16 6 0.17 (0.1–0.88) ,.0001
purpura (Fig 4). Diameter alone may
also be confusing in small infants, whose Note.—Unless otherwise specified, data are numbers of cases of intussusception, with percentages in parentheses.
small-bowel diameter naturally results in * Data are means 6 standard deviations, with ranges in parentheses.
small-diameter intussusceptions (Fig 5).
Univariate analyses with Bonferroni
adjustments were performed for sex,
Discussion
fever higher than 38°C, vomiting, pres- specifically, they are due to the ana-
ence of lymph nodes inside the lesion, We have shown that the index of the tomic characteristics of the mesentery
and outer rim thickness. Presence of diameter of the hyperechoic inner fat that is pulled into the central part of
lymph nodes inside the lesion and vom- core to wall thickness may be a useful the intussusception together with the
iting remained significantly associated parameter enabling confident differ- telescoping bowel. We hypothesize that
with ileocolic intussusception when all entiation between ileocolic and small- most important feature of the ileocolic
tests were considered simultaneously bowel intussusception in children; intussusception is an echogenic fat core
(P , .0001 and P = .0093, respectively). an index of inner fat core diameter that represents mesenteric fat.
Multiple logistic regression model to wall thickness greater than 1.0 is At the jejunal end of the mesen-
analysis with adjustment for sex, age, characteristic of ileocolic intussuscep- tery, fat is deposited near the root and
fever higher than 38°C, vomiting, pres- tion, while an index of less than 1.0 is is scanty near the intestinal wall. In
ence of lymph nodes inside the lesion, characteristic of small-bowel intussus- contrast, at the ileal end of the mesen-
and outer rim thickness showed that ception. The presence of lymph nodes tery, fat extends from the root to the
lymph nodes inside the lesion and outer inside the intussusception and larger intestinal wall (14,15). Ileocolic intus-
rim thickness were significantly associ- lesion diameter were also characteris- susception always contains ileal mesen-
ated with type of intussusception (P , tic of ileocolic intussusception in our tery, which explains the marked central
.0001 and P = .014, respectively). Core- patients. echogenic fat core in these lesions.
to-wall index at a threshold of 1.0 and The differences between the appear- Small-bowel intussusception shows no
fat core diameter of 0.1 cm were not ance at US of ileocolic intussusception or a minimal flat fatty component. In-
included in the model because both had and that of small-bowel intussuscep- creased mesenteric fat in the distal il-
100% positive predictive value for ileo- tion originate from anatomic elements eum also explains the uneven diameter
colic intussusception. of these two forms of intussusception; of the hyperechoic inner fat core on

Radiology: Volume 269: Number 1—October 2013 n radiology.rsna.org 269

PEDIATRIC IMAGING: Can US Help Differentiate between Ileocolic and Small-Bowel Intussusception?
Figure 2
Figure 2: US image of 12-mm small-bowel intus-
susception in 9-month-old girl. Note the absence of
a central fat core. The lesion reduced spontaneously.
Figure 4
Figure 4: US image of large (25-mm-diameter)
small-bowel intussusception in 7-year-old boy
with Henoch-Schönlein purpura. The outer wall is
thickened, but no fat tissue is seen in the central
part of the lesion.
different images of the same study. It
is thus important to perform the mea-
surements for the fat core–to-wall in-
dex calculation on images that show the
maximum fat core diameter. This index
is derived from the diameter of the fat
core versus the thickness of the outer
wall. An index greater than 1.0 is asso-
ciated with 100% sensitivity and speci-
ficity for ileocolic intussusception in our
experience. This index appears to en-
able reliable differentiation of ileocolic
from small-bowel intussusception. The
presence of fat in ileocolic intussuscep-
tion also attenuates mesenteric lymph
nodes included in the intussusception,
making them easily identifiable.
270
Figure 3
Figure 3: US image of 18-mm small-bowel
intussusception in 8-month-old boy shows that the
intussusception has a small (0.3 mm) and flat inner
fat core (arrows). The outer wall diameter is 0.5
mm, and the core-to-wall index is 0.6 (0.3/0.5). The
lesion reduced spontaneously.
Figure 5
Figure 5: US image of small (17-mm-diameter) il-
eocolic intussusception in 3-month-old boy. Note the
inner fat core (7.0 mm) (arrows) and the outer wall
(5.0 mm). The core-to-wall index is 1.4 (7.0/5.0).
Doi et al (8) consider small-bowel
intussusception to be a precursor of
ileocolic intussusception and suggest
that it should be followed up closely un-
til spontaneous reduction occurs. In pa-
tients with small-bowel intussusception
that did not reduce spontaneously and
who underwent surgery, lead points or
necrotic small bowel have been found
at surgery by other authors, who there-
fore do not recommended enema as the
treatment of choice for these lesions
(9,16). On the contrary, Saxena et al
(17) reported a high incidence of small-
bowel intussusception that did not re-
duce spontaneously, and they achieved
radiology.rsna.org
Lioubashevsky et al
successful enema reduction in six of
seven cases where it was attempted.
We are in agreement with other authors
(9,16), who have suggested that enema
reduction should not be routinely used
in the management of small-bowel in-
tussusception. In our series, 56 cases of
small-bowel intussusception were seen
to have reduced spontaneously at fol-
low-up US. One child with small-bowel
intussusception had a lead point lesion,
which was diagnosed at US. Pathologic
examination of the resected bowel re-
vealed Hodgkin lymphoma.
Our work is in agreement with that
of authors who reported older ages in
the population of patients with small-
bowel intussusception (10,13). In our
study, the mean age was 14.2 months
6 9 for the ileocolic group and 25.3
months 6 20 for the small-bowel intus-
susception group (P = .0001). We were
able to demonstrate a significantly high-
er incidence of blood in stool, vomiting,
and leukocytosis in patients with ileo-
colic intussusception. Owing to the ret-
rospective nature of this study, we had
to rely on clinical notes, which could
provide incomplete details on the clin-
ical presentation regarding such symp-
toms and signs as vomiting and blood
in stool, thus limiting the value of this
analysis. None of the clinical signs al-
lowed confident differentiation between
the types of intussusception in an indi-
vidual case.
As the accuracy and safety of US in
the diagnosis of intussusception have
increased, enemas are no longer used
routinely for diagnosis and are mostly
reserved for therapeutic purposes
(3,8,16). US characteristics such as le-
sion diameter, lesion length, outer wall
thickness, and the presence of lymph
nodes are known to differ between
types of intussusception (6,9,10,13).
Our measurements of the diameter and
outer wall thickness are very similar to
those obtained by Park et al (13). Our
data regarding the multilayered appear-
ance and measurements of small-bowel
intussusception are also very similar to
those of Kim (18).
However, there is overlap in mea-
surements relating to ileocolic and those
relating to small-bowel intussusception
n Radiology: Volume 269: Number 1—October 2013
PEDIATRIC IMAGING: Can US Help Differentiate between Ileocolic and Small-Bowel Intussusception?
that have been reported by various
authors, and most reports have been
based on relatively small patient series
(10,13); thus, no single parameter has
been identified that enables unequivo-
cal differentiation between these two
types of intussusception.
In the past, when a lesion that we
had diagnosed as a small-bowel intus-
susception did not reduce spontane-
ously during the initial or follow-up
US examination, surgeons in our insti-
tution requested an enema on several
occasions to ensure that we had not
misdiagnosed an ileocolic intussuscep-
tion. On the basis of our findings in this
study, we now routinely calculate the
core-to-wall index, which has proved to
be reliable.
The major limitation of this study
was its retrospective character. Addi-
tional limitations were a lack of a refer-
ence standard for cases without enema
or surgery, with only empiric confir-
mation of the appropriateness of con-
servative management, and repeated
episodes in patients with potentially
similar appearances being counted
more than once. Further prospective
studies are warranted to validate our
conclusions.
In conclusion, clinical findings and
measurements of lesion diameter alone
cannot enable reliable differentiation
between ileocolic and small-bowel in-
tussusception; however, in our expe-
rience, the presence of a fatty core in
the lesion in combination with lesion
diameter and wall thickness and espe-
cially the ratio between the diameter of
the fatty core to the thickness of the
outer wall, as well as the presence of
internal lymph nodes, can be used to
differentiate between the types of in-
tussusception. Validation of our find-
ings in a larger patient population is
Radiology: Volume 269: Number 1—October 2013
warranted, with the goal of defining a
reliable means for definitive differentia-
tion between these two common forms
of intussusception.
Disclosures of Conflicts of Interest: N.L. No
relevant conflicts of interest to disclose. N.H. No
relevant conflicts of interest to disclose. K.R. No
relevant conflicts of interest to disclose. L.S. No
relevant conflicts of interest to disclose. N.S. No
relevant conflicts of interest to disclose.
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