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Subtypes of Irritable Bowel Syndrome in Children: Prevalence

at Diagnosis and at Follow-Up


Eleonora Giannetti, MD1, Gianluigi deAngelis, MD2, Rossella Turco, MD1, Angelo Campanozzi, MD3, Licia Pensabene, MD4,
Silvia Salvatore, MD5, Federica de Seta, MD1, and Annamaria Staiano, MD1
Objectives To assess the prevalence of irritable bowel syndrome (IBS) subtypes in childhood at diagnosis and
their changes over 1 year.

Study design This is an observational, prospective, multicenter study. Consecutive pediatric patients with IBS,
according to Rome III criteria, were enrolled over a 1-year period. Parents recorded weekly stool frequency and
consistency and gastrointestinal and extraintestinal symptoms in a diary. Stool consistency was scored according
to the Bristol Stool Form Scale. Children were evaluated after 2, 3, 6, and 12 months.
Results We enrolled 100 children with IBS (median age 9.9 years, range 4.2-16.7 years, 52 girls and 48 boys). At
time of enrollment, constipation-IBS was the prevalent subtype (45%), with a prevalence of girls at 62% (P < .005);
diarrhea-IBS was reported in 26% of children, with a prevalence of boys at 69% (P < .005); and alternating-IBS was
described in 29% of children, without a difference between sexes. During the follow-up, 10% of patients changed
their IBS subtypes at 2 months, 9% at 3 months, 7% at 6 months, and 6.3% at 12 months. Twenty-four percent of
patients changed IBS subtype between the time of enrollment and 12 months.
Conclusions Constipation-IBS is the prevalent subtype in children, with a higher frequency in girls. In boys, diarrheaIBS is the most common subtype. It is important to acquire knowledge about IBS subtypes to design clinical trials that
may eventually shed new light on suptype-specific approaches to this condition. (J Pediatr 2014;164:1099-103).

rritable bowel syndrome (IBS), as described by using the Rome criteria, includes symptoms of abdominal pain or discomfort
accompanied by changes in bowel patterns.1,2 Studies have estimated the prevalence of IBS to range between 6% and 14% in
children and between 22.0% and 35.5% in adolescents.3,4 A confident diagnosis, confirmation, and explanation of pain experience and reassurance can by itself be therapeutic.5 Specific goals of therapy include modifying severity and developing strategies
for dealing with symptoms.1 In adults, the Rome III committee recommends a subclassification into different subtypes based on
the predominant bowel habit (constipation-IBS [C-IBS] or diarrhea-IBS [D-IBS]).6 Different authors7 consider that patients
with symptoms of both constipation and diarrhea should constitute an alternating-IBS (A-IBS) or a mixed-IBS subtype.
A systematic review showed that the clinical course of IBS is highly heterogeneous because IBS clinical subtype distribution
differs depending on the population evaluated, the geographical location, and the criteria used to define IBS and bowel habit
subtypes. In most cases, clinical course is characterized by the presence of mild-to-moderate symptoms appearing sequentially.8
A recent study in adults showed that the distribution of IBS subtypes is stable over time in most of the patients, although
30%-40% of patients with IBS changed intestinal pattern at least once during a 2-week period.9
As reported in guidelines and review articles, drug therapy in IBS should be chosen on the basis of the predominant bowel
symptom.10-13 Only 1 study performed in pediatric patients in Sri Lanka showed an equal distribution of IBS subtypes.14
The aims of the present study were to establish the predominant IBS subtypes in children at diagnosis and to observe the
changes over time of IBS subtypes.

Methods
Patients eligible for the study were children aged 5-17 years who were referred for abdominal pain and subsequently received a
diagnosis of IBS at 1 of 5 different Italian pediatric clinicsUniversity of Naples Federico II, University of Foggia, HospitalUniversity of Parma, University Magna Graecia of Catanzaro, and University
of Insubria, Varesebetween January 2010 and January 2012. IBS was diagnosed

5-HT
A-IBS
C-IBS
D-IBS
FGID
IBS

5-hydroxytryptamine
Alternating-irritable bowel syndrome
Constipation-irritable bowel syndrome
Diarrhea-irritable bowel syndrome
Functional gastrointestinal disorder
Irritable bowel syndrome

From the 1Department of Translational Medical Science,


Section of Pediatrics, University of Naples Federico II,
Naples, Italy; 2Gastroenterology Unit, Hospital-University
of Parma, Parma, Italy; 3Department of Pediatrics,
University of Foggia, Foggia, Italy; 4Department of
Pediatrics, University Magna Graecia of Catanzaro,
Catanzaro, Italy; and 5Department of Pediatrics,
University of Insubria, Varese, Italy
The authors declare no conflicts of interest.
0022-3476/$ - see front matter. Copyright 2014 Elsevier Inc.
All rights reserved. http://dx.doi.org/10.1016/j.jpeds.2013.12.043

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using the Rome III criteria for pediatric functional gastrointestinal disorders (FGIDs).1 Exclusion criteria were: (1)
FGIDs other than IBS; (2) any underlying chronic disorders;
(3) cerebral palsy; (4) delayed psychomotor development;
and (5) children who had received drugs that modify bowel
habits, such as probiotics, laxatives, and antidiarrheals, during the previous month.
An informed consent was obtained at enrollment from
parents of all children younger than 10 years and from
both parents and children if older than 10 years. The study
was approved by the independent ethics committees of all
participant centers.
The study had a multicenter, observational, prospective
design. At the first visit (T0 [enrollment]), a medical history
was collected and all patients underwent clinical evaluation,
laboratory tests (full blood cell count, inflammatory markers,
antitransglutaminase and antiendomysial antibodies, fecal
calprotectin), and a trial with a lactose-free diet for 2 weeks,
to exclude lactose intolerance. Information regarding
abdominal pain characteristics, bowel habits, and associated
symptoms were recorded using a previously validated selfadministered questionnaire. The questionnaire was developed according to the Rome III diagnostic questionnaire
for pediatric FGIDs.15 Parents received a diary in which to
record weekly stool frequency and consistency, the presence
of specific behaviors during the evacuation such as retentive
posturing or excessive volitional stool retention, and the
presence of gastrointestinal symptoms. A score of the stool
consistency was subsequently attributed according to the
Bristol Stool Form Scale.16 Patients were subclassified in
different subtypes of IBS based on the adult Rome III classification, due to the lack of a classification in the pediatric
age.6 Children were prospectively evaluated at 2 (T1), 3
(T2), 6 (T3), and 12 (T4) months after enrollment. At each
visit, the interim history was assessed, weekly diaries were
reviewed and discussed, a physical evaluation was performed,
and the children and/or their parents were asked to again
complete the IBS symptoms questionnaire. If a child did
not return for a planned follow-up visit, follow-up data
were obtained through a telephone call by the authors.
After inclusion in the study, all children were treated with
reassurance and with lifestyle changes provided by means of
oral and written instructions; in particular, families were explained that IBS is a functional bowel disorder in the absence
of any organic cause and were educated to face episodes of
abdominal pain by attempting to reduce the patients anxiety
and worries. Furthermore, children were invited to play sports
and encouraged to practice outdoor activities,17 they were recommended to eliminate excess of fructose and spices from the
diet,18-20 and they were encouraged to consume a regular fiber
diet (age in years plus 5 g/day)21,22 by means of written recommendations (Appendix; available at www.jpeds.com). No
drug treatment was started during the follow-up period.
Compliance with these recommendations and failure to
take other forms of therapy were assessed at each follow-up
visit by examination of the diary completed by patients
and/or their parents.
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Statistical Analysis
Statistical analysis was carried out using SPSS statistical
software package for Windows (13.0; SPSS Inc, Chicago,
Illinois). A value of P < .05 was considered as significant.
Fisher exact test was used to assess the prevalence of symptoms in the 3 groups.

Results
Of 113 patients eligible for the study, 11 (9.7%) declined
participation. Two children (1.8%) were excluded from the
study because they improved after the 2-week lactose-free
diet trial. In all subjects, laboratory findings were unremarkable. No children changed from IBS to another FGID during
the study period.
We enrolled 100 children with diagnosis of IBS (48 boys
and 52 girls, median age 9.9 years, range 4.2-16.7 years).
Median time between onset of symptoms and diagnosis
was 6.2 months (range 2-10 months).
At the time of enrollment (T0), C-IBS was the prevalent
subtype, present in 45 of 100 children (45%), with a prevalence of 62% in girls (28/45; P < .05); D-IBS was reported
in 26 of 100 (26%) children, with a prevalence of 69% in
boys (18/26; P < .05); and A-IBS was described in 29 of 100
children (29%), with no significant difference in prevalence
between sexes. The prevalence of the different subtypes at
diagnosis is shown in Figure 1.
At diagnosis, 41% of patients had difficulty falling asleep,
53% of patients reported recurrent absences from school
and/or interruption of their activities, 32% of patients had
joint pain, and 43% had headache. Difficulty falling asleep,
absences from school and/or interruption of activities, and
the other reported extraintestinal symptoms were not significantly related to IBS subtype (Table I).
At 2-month follow-up (T1), 10 of 100 (10%) patients presented changes in IBS subtypes: 3 from C-IBS to D-IBS, 3
from A-IBS to C-IBS, and 4 from A-IBS to D-IBS. At
3-month follow-up (T2), 9 of 100 (9%) patients presented

Figure 1. Prevalence of the different IBS subtypes and distribution according to sex at diagnosis.
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Table I. Correlation between IBS subtypes and


extraintestinal symptoms
IBS subtypes, n (%)

Difficulty falling asleep,


No. (%)
Absences from
school/interruption
of activities, No. (%)
Joint pain, No. (%)
Headache, No. (%)

C-IBS,
45 (45)

D-IBS,
26 (26)

A-IBS,
29 (29)

Total,
100

19 (42.2)

8 (30.7)

14 (48.3)

41 (41)

.41

25 (55.5)

12 (46.1)

16 (55.2)

53 (53)

.72

14 (31.1)
22 (48.9)

5 (19.2)
9 (34.6)

13 (44.8)
12 (41.4)

32 (32)
42 (42)

.12
.49

changes in IBS subtypes: 1 from A-IBS to C-IBS, 1 from


D-IBS to A-IBS, 1 from D-IBS to C-IBS, 2 from C-IBS to
D-IBS, 2 from C-IBS to A-IBS, and 2 from A-IBS to D-IBS.
At 6-month follow-up (T3), 7 of 100 patients (7%) presented
changes in IBS subtypes: 3 from C-IBS to A-IBS, 2 from
A-IBS to D-IBS, 1 C-IBS to D-IBS, and 1 from D-IBS to
A-IBS.
After 1 year, in 53 of 95 children (55.7%), change in bowel
habit and abdominal pain disappeared, and 5 children were
lost at follow-up3 dropped out because drug prescriptions
were requested, whereas 2 discontinued the follow-up visits.
In the remaining 42 children, C-IBS was still the most frequent
subtype, detected in 21 of 42 children (50%; P = .01); C-IBS was
present in 12 of 21 girls and 9 of 21 boys (57% and 43%, respectively; P = .35). D-IBS was present in 12 of 42 patients (29%)
and it was still more frequent in boys, with a prevalence of 2
of 12 girls and of 10 of 12 boys (17% and 83%, respectively;
P = .02). A-IBS was present in 9 of 42 (21%) patients with
no difference between sexes (P = .4).
From T3 to T4, changes of subtypes were observed in 6 of
95 children (6.3%): 3 from A-IBS to C-IBS and 3 from A-IBS

to D-IBS. Figure 2 shows the distribution of subtypes during


the 1-year study period.
Overall, 23 of 95 patients (24.2%) changed IBS subtype
only once between T0 and T4, and the most frequent changes
were observed from A-IBS to C-IBS or D-IBS. Nine patients
changed IBS subtype more than once during the study
period. Changes of IBS subtypes throughout the study are
shown in Table II (available at www.jpeds.com).

Discussion
The major findings of our study were that: (1) C-IBS was the
prevalent subtype, with a significantly higher frequency in
girls, and D-IBS was more frequent in boys; (2) the prevalent
subtype did not change during the 12-month follow-up
period; (3) there was a variation in bowel pattern in 24%
of children during the follow-up period; and (4) among the
intestinal and extraintestinal symptoms considered, none
was related to IBS subtypes.
In our study, distribution of IBS subtypes showed that CIBS was the most frequent subtype. A previous pediatric
study assessing IBS subtypes in Sri Lankan children and adolescents, reported that C-IBS, D-IBS, and A-IBS were almost
equally distributed.14 In a systematic review, Guilera et al8
found that, in adults, US studies showed a similar distribution between C-IBS, D-IBS, and A-IBS and that European
studies reported that both C-IBS and D-IBS subtypes were
the most commonly detected. Similarly, Engsbro et al9 found
a tendency toward C-IBS and D-IBS being the most stable
subtypes. This pattern was also found by Dorn et al,23
whereas Penny et al24 and Halder et al25 described C-IBS as
the least stable subtype. Most of the available studies reported
A-IBS to be the most common subgroup,26 especially when
the investigation is primary care office based.8 Ersryd and

Figure 2. Distribution of IBS subtypes at diagnosis and at the 4 timepoints during follow-up.
Subtypes of Irritable Bowel Syndrome in Children: Prevalence at Diagnosis and at Follow-Up

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others have demonstrated that the presence of diarrhea is an


explanation for referral from primary care to gastroenterologists,27-29 which might explain a higher proportion of D-IBS
in some studies from gastroenterology outpatient clinics.30,31
According to most of the authors, A-IBS was the most common Rome II subtype, whereas according to Rome III
criteria, C-IBS and D-IBS were the most common subtypes.
In our population, female sex was more frequently associated with constipation and male sex with diarrhea, similar to
what was previously reported by Rajindrajith and Devanarayana in a pediatric cohort14 and by other authors in adult
populations31-34 but not with the findings from another adult
study that, using Rome III criteria, found no sex difference in
the prevalence of subtypes.27
Identification of IBS subtypes would be important in both
clinical practice and research, because pharmacological management of IBS is becoming more specific and new therapies
are being developed that target specific IBS subtypes. Our
findings showed that the point prevalence of subtypes is fairly
stable over time, although 24% of patients changed subtype
during a 1-year period. Our stability rate (76%) is higher
than that found in some adult studies. Engsbro et al9 found
that, in a 10-week follow-up, about 60% of patients remained
within the same subtype from one period to the next, whereas
30%-40% of patients changed subtype. Dorn et al23 found a
stability rate of Rome II subtypes of 15% and of Rome III
subtypes of 23% based on six 2-week periods over a total of
15 months, and Drossman et al35 found 24% to be stable,
when evaluating Rome II subtypes 6 times for 2 weeks during
15 months. In contrast, Williams et al36 showed that among
the whole survey sample, 30% of subjects remained in the
same IBS subtype in the 2001 and 2004 surveys and 18%
changed IBS subtype, and the remaining 52% of subjects
no longer met the criteria for IBS during the follow-up.
Mearin et al37 found that 61% of their patients were stable
when evaluating them twice during 4 weeks with an interval
of 1 month.
The discrepancy among these results could be related to
the different population and criteria used to define the subtypes of IBS and to a shorter follow-up compared with our
study. At present, there are no pediatric data on the variability of IBS subtypes over time.
It is interesting to note that in our population, similarly to
Garrigues et al,7 most changes occurred from A-IBS to C-IBS
or D-IBS (21%); changes from C-IBS to D-IBS, or vice versa,
occurred in a minority of patients (8%), and it was not common to change from C-IBS or D-IBS to A-IBSdirect shifts
between these subtypes were rarely seen.
Changes in symptoms and in bowel habit subtype may
depend on different factors besides the natural history of
the disease, such as the effect of treatment or of the reassurance derived by a physician visit. In the present study, all children received the same behavioral and dietary advice to avoid
a treatment bias in the assessment of subtype changes.
The interest in subtyping patients with IBS has grown
stronger as new drugs have been introduced on the market.
As reported in several guidelines and review articles,10-13
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drug therapy in IBS should be aimed at the primary bowel
symptom. Furthermore, new investigational drugs, such as
5-hydroxytryptamine (5-HT)3 antagonists and 5-HT4
agonists, have been developed to treat specific bowel habit
disordersdiarrhea and constipation, respectively.10,11
Pharmaceutical agents acting on 5-HT receptors have the
potential to ameliorate the smooth muscle spasm, abdominal pain, and change in bowel habit that patients with IBS
experience. A recent review by Camilleri and Di Lorenzo38
showed that the treatment of constipation or diarrhea also
improves abdominal pain, which is the most important
symptom in IBS. In particular, treatment with lubiprostone
was associated with significant improvement in bowel
movement frequency as well as symptoms of abdominal
discomfort/pain and bloating.39 A systematic review and
meta-analysis found that 5-HT3 antagonists improve
abdominal pain and discomfort and global IBS symptoms
in men and women with nonconstipated and diarrheapredominant IBS.40
Our study has some limitations. First, as the study was
conducted at a tertiary care center, our population was
selected and patients had no comorbidities and no other
FGIDs and, during the follow-up period considered, did
not receive any pharmacological treatment. We cannot
exclude that all these potentially confounding factors may
affect the changes in IBS subtypes in a less pure population.
Furthermore, we cannot rule out that the recommendation
for all children to follow the same diet plan, despite being established to not influence the course of the syndrome, could
have minimally affected the evolution of IBS subtypes. On the
other hand, dietary recommendations were provided to the
whole population and represented an intervention that likely
determined a trivial effect on the natural history of IBS.
Finally, another potential drawback of our analysis is that
we did not assess the impact of pharmacological therapy on
IBS symptoms. However, this was beyond the aims of our
research and should be investigated in further studies.
In conclusion, in our population, C-IBS is the most prevalent subtype overall at the timepoints considered, with a significant higher frequency in girls. A variation of bowel
pattern is reported during the follow-up in 25% of children
with IBS. It is important to acquire knowledge about IBS subtypes to design clinical trials that may eventually shed new
light on subtype-specific approaches to this condition. n
Submitted for publication Aug 6, 2013; last revision received Dec 11, 2013;
accepted Dec 19, 2013.
Reprint requests: Annamaria Staiano, MD, Department of Translational
Medical Science, Section of Pediatrics, University Federico II, Via S. Pansini,
5, 80131 Naples, Italy. E-mail: staiano@unina.it

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Appendix. Irritable Bowl Syndrome Informative Sheet for Parents.

Table II. Changes in IBS subtype throughout the study


Type of changes

n (%)

No changes
C-IBS
D-IBS
A-IBS
C-IBS / A-IBS or D-IBS
C-IBS / A-IBS
C-IBS / D-IBS
D-IBS / A-IBS or C-IBS
D-IBS / A-IBS
D-IBS / C-IBS
A-IBS / C-IBS or D-IBS
A-IBS / C-IBS
A-IBS / D-IBS

63 (66.3)
34 (36.9)
23 (24.2)
11 (11.6)
11 (11.6)
5 (5.2)
6 (6.3)
3 (3.1)
2 (2.1)
1 (1)
18 (18.9)
7 (7.4)
11 (11.6)

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