Bacterial Overgrowth and Methane Production in Children with Encopresis
Alycia Leiby, MD, Devendra Mehta, MD, Vani Gopalareddy, MD, Susan Jackson-Walker, PhD, and Karoly Horvath, MD, PhD
Objectives To assess the prevalence of small intestinal bacterial overgrowth (SIBO) and methane production in
children with encopresis.
Study design Radiographic fecal impaction (FI) scores were assessed in children with secondary, retentive en-
copresis and compared with the breath test results. Breath tests with hypoosmotic lactulose solution were per-
formed in both the study patients (n = 50) and gastrointestinal control subjects (n = 39) groups.
Results The FI scores were significantly higher in the patients with encopresis who were methane producers
(P < .01). SIBO was diagnosed in 21 of 50 (42%) patients with encopresis and 9 of 39 (23%) of control subjects
(P = .06). Methane was produced in 56% of the patients with encopresis versus 23.1% of the control subjects in
Conclusions Children with FI and encopresis had a higher prevalence of SIBO, elevated basal methane levels,
and higher methane production. Methane production was associated with more severe colonic impaction. Further
study is needed to determine whether methane production is a primary or secondary factor in the pathogenesis of
SIBO and encopresis. (J Pediatr 2010;156:766-70).
symptom (84%) in children presenting with constipation to pediatric gastroenterologists.2
Encopresis is frustrating for patients and families and often requires a significant period of time for treatment and bowel
retraining. The recovery rates vary from 30% to 50% after 1 year and from 48% to 75% after 5 years of treatment.3
Orocecal transit time is prolonged in children with constipation.4,5Animal studies have shown that methane, a product of
colonic bacterial fermentation in human beings, prolongs intestinal transit.6Methane production on breath tests has been as-
longed colonic transit time in children with constipation. It was also reported that methane production is more common in
children with encopresis when compared with children with constipation only and in control subjects.8,9
Anaerobic bacteria in the terminal ileum and colon are responsible for the production of methane gas. Elevated pH and in-
over 1 ppm, and there was a negative correlation between frequency of bowel movements and breath methane concentration.
Increased breath methane level has been reported in many disorders, including cystic fibrosis, diverticulosis, constipation-pre-
dominant irritable bowel syndrome, and colon cancer.12-15
In healthy subjects, bacterial proliferation in the upper gastrointestinal tract is controlled by gastric acid secretion, intestinal
motility,andthe mucosal immune system.Prolonged intestinaltransittime representsa risk factor for small intestinalbacterial
overgrowth (SIBO). SIBO is defined by an excessive amount of bacteria, particularly anaerobes, in the upper gastrointestinal
examiningtheprevalenceof SIBOinchildrenwithencopresis.Theaim ofthisstudywastoassessSIBOprevalencemeasured by
the lactulose breath test in children with secondary, retentive encopresis with and without methane-producing flora and to
compare the results with control subjects.
t has been shown that the onset of constipation may be associated with a diet change early in life, toilet training during the
toddler years, orapainful defecation episodeassociatedwitheither analfissuresoraninfectious colitis, leadingtowithhold-
ing.1Untreated chronic constipation may result in fecal incontinence. Encopresis was the most frequent accompanying
The study was conducted at the Gastroenterology and Nutrition Outpatient
Clinic of the Alfred I. duPont Hospital for Children in Wilmington, DE, from
January 2005 to June 2008. The study enrolled otherwise healthy school age chil-
dren (6 to 12 years) with normal general intellectual functioning who had a his-
From the Division of Pediatric Gastroenterology and
Nutrition (A.L., D.M., V.G., K.H.) and Division of
Behavioral Health (S.J.), Alfred I. duPont Hospital for
Children, Wilmington, DE, and the Thomas Jefferson
University (A.L., D.M., V.G., S.J., K.H.), Philadelphia, PA
Funding for the project was obtained through the Nem-
ours Foundation. The authors declare no conflicts of in-
0022-3476/$ - see front matter. Copyright ? 2010 Mosby Inc.
All rights reserved. 10.1016/j.jpeds.2009.10.043
Lactulose breath test
Small intestinal bacterial overgrowth
patients had daily or weekly episodes of fecal soiling for
a minimum of 2 months before evaluation. Patients were
not excluded if they had previously been treated for encopre-
sis, because all were still symptomatic and non-adherent to
the prescribed therapies. Children with a history of gastroin-
Fifty children with encopresis were included in the study,
and 68% (34 of 50) were male patients. Mean duration of
constipation was 3.47 ? 2.56 years. The control group con-
sisted of 39 children of whom 61% were male. Control pa-
tients had various gastrointestinal problems but had no
signs or symptoms of constipation or encopresis. The indica-
tions for the test included abdominal pain, flatulence, vomit-
ing, and diarrhea. Although there was no significant age
difference between the groups, the body mass index (BMI),
weight, and height percentiles were significantly higher in
the encopresis group (data not shown).
Fecal Impaction Scores
An abdominal flat-plate radiograph was obtained for all the
patients with encopresis before the start of therapy. The de-
gree of fecalimpaction wasassessed bya scoring system rang-
ing from 0 to 3.17A grade of ‘‘0’’ was designated for feces in
tum, cecum, and discontinuous elsewhere; a grade of ‘‘2’’ for
and affecting all segments; and a grade of ‘‘3’’ for feces in the
rectum, cecum, continuous elsewhere, and a dilated colon
and impacted rectum. Figure 1 (available at www.jpeds.
com) shows examples of impaction scores. The radiographs
were reviewed at the first office visit and independently by
2 investigators. In cases of discrepancy the score that was in
agreement between 2 of the 3 physicians was used.
Lactulose Breath Test
The lactulose breath test (LBT) was performed at the first
visit before starting the therapy. To reduce osmotic effect,
the test solution consisted of lactulose 10 g in water 240
mL. This solution had an osmolality of 121 mosmol/L.
All patients completed the lactulose breath test after an
overnight fast of 10 hours. Patients were given a list of foods
high in carbohydrates to avoid the afternoon and evening be-
fore the day oftestingand were advised to avoid smoke expo-
sure and vigorous exercise on the testing day. Testing was
rescheduled if the patient had been on an antibiotic within
the previous 2 weeks or had significant carbohydrate con-
sumption the night before.
An initial baseline breath sample was collected. Additional
180 minutes after the ingestion of test solution. End-expira-
tory breath samples were collected with the GaSampler sys-
tem (QuinTron Instrument
The second sample was used if the level of carbon dioxide in
the first sample was too low.
Samples were measured with the Microlyzer model SC
analyzer (QuinTron Instrument Company). Hydrogen
and methane concentrations were expressed in ppm. The
machine was calibrated with the QuinGas-3 (QuinTron
Instrument Company) standard gas mixture containing
100 ppm hydrogen, 50 ppm methane, and 5% carbon di-
Criteria for Methane Production and SIBO
Patients were considered methane producers if their level
was more than 3 ppm at any point in the study (based
on ambient air containing about 1.8 ppm).18High basal
methane was diagnosed if the baseline sample was >10
ppm. SIBO was diagnosed if the hydrogen level was $20
ppm or the methane level was $10 ppm above baseline at
The Nemours Clinical Research Review Committee and In-
stitutional Review Board approved the protocol. Permission
for participation was obtained from the guardian and assent
for participation from children ages 7 to 12 years.
The c2test for a 2-tailed P value was used for comparing fre-
quencies between 2 groups. Odds ratios and 95% confidence
intervals were calculated. For comparing means between the
2 groups, the 2-tailed t test was used. P < .05 was considered
as statistically significant.
The mean fecal impaction (FI) radiographic score was 1.9 ?
0.65 for the entire encopretic group. There was a significant
difference (P < .01) in the mean FI score between methane
producers (2.03 ? 0.32; n = 24) and non-methane–produc-
ing patients (1.72 ? 0.44; n = 26). The mean FI scores of
the SIBO-positive patients (1.9 ? 0.49) and the SIBO-nega-
tive patients (1.89 ? 0.39) were not different (P = .06).
SIBO was found in 21 of the 50 (42%) children with en-
copresis. The prevalence of SIBO was lower (23.1%) in the
gastrointestinal control group. The difference did not reach
statistical significance (P = .06). Of the patients with encop-
resis and SIBO, the diagnosis was made on the basis of ele-
vated methane levels in 8 patients, elevated hydrogen levels
in 11 patients, and both elevated methane and hydrogen
levels in 2 patients. The diagnosis of SIBOis sometimes based
on a ‘‘double peak,’’ which is defined as an early peak of 2
consecutive hydrogen values more than 10 ppm above the
baseline value that is clearly distinguishable from a colonic
peak of >20 ppm above baseline20or a rise of 20 ppm occur-
ring more than 15 minutes before a colonic peak.19In our
group, a double peak was found in 10 patients with encopre-
sis and 2 gastrointestinal control subjects. There was no dif-
ference between groups in sex or existence of SIBO.
High basal methane concentration was measured in 24 of
50 (48%) patients with encopresis versus 4 of 39 (10.3%)
control subjects (P < .001). Methane production ($3 ppm)
Vol. 156, No. 5 ?
at any time during the LBT was present in 28 of 50 (56%) pa-
tients with encopresis and 9 of 39 (23.1%) controls (P < .01).
Figure 2 illustrates the average methane and hydrogen pro-
ductions in the SIBO-positive and SIBO-negative patients
in the 2 study groups. It clearly shows the higher methane
levels in the encopretic group.
We were able to retest 6 of the 21 patients with encopresis
who had SIBO. The other 15 patients refused retesting or
were lost to follow-up. Of these 6 patients, 3 had responded
to therapy as defined by daily, soft stools and no soiling dur-
ing the 4 weeks before the repeat LBT. Two of the 6 patients
(33%) still had SIBO; both were nonresponders and were
nonadherent to therapy. Four of the 6 retested patients
were methane producers according to the initial LBT and re-
mained so on the repeat LBT.
Because the bacterial flora in the small intestine is controlled
motility, patients with encopresis and methane production
are at risk for SIBO. We hypothesized that methane produc-
tion increases the risk for SIBO by slowing small intestinal
transit time. SIBO was diagnosed more frequently in our pa-
tients with encopresis compared with the children with other
gastrointestinal disorders, but this did not reach significance
(P = .06). However, we did not use healthy control subjects;
our control group consisted of gastroenterology patients
without constipation. In a study by Rhodes et al,19all 37
healthy control subjects had negative lactulose breath test re-
Methane in the gut is the sole result of anaerobic bacterial
production predominantly from the organism Methanobre-
vibacter smithii.12Lactulose does not influence methane-pro-
ducing flora; therefore it can be used as substrate for the
LBT.18Bond et al18showed that newborns and children
younger than 2 years do not excrete methane. Levels then
slowly rise until the age of 10 years, when adult values are
reached. There seem to be many factors influencing the pro-
duction of methane in the gut.11A significant concentration
of methanogenic bacteria must be reached to produce a rise
of 1 ppm above atmospheric level.12Bacterial culture in
adults revealed that an average concentration of 9.45 log10
methanogenic organisms per gram dry weight of stool was
needed to produce methane. Peoplewho had an average con-
centration of 4.9 log10methanogenic organisms per gram dry
weight ofstool orless didnot produce detectable methane on
In animal experiments, Pimentel et al6demonstrated that
methane infusions slowed small intestinal transit and altered
contractile activity. They hypothesized that methane may ac-
tivate a reflex pathway similar to the way fat stimulates the
‘‘ileal brake,’’ triggering nonpropulsive contractions.
It can be hypothesized that a methane-overgrowth cycle
exists by methane slowing the small intestinal transit, result-
ing in SIBO and subsequent increase of the anaerobic bacte-
rial load producing more methane and perpetuating
prolonged transit time and constipation. In this study, 56%
of the patients with encopresis produced methane, and
48% had high basal methane levels. These values are higher
than those found in our control group consisting of children
methane and 10% had high baseline values. These results are
in accordance with the previously published reports describ-
ing that higher percentage of children with encopresis and
constipation produced methane.8,9Fiedorek et al9found
that 65% of the patients with encopresis were methane pro-
ducers compared with the control group without constipa-
tion or encopresis, for whom 15% of patients had
Figure 2. Average methane and hydrogen productions in the
SIBO-positive and SIBO-negative patients in the encopretic
and control groups (Mean ? SEM).
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Vol. 156, No. 5
Leiby et al
a methane level >3 ppm. Similar results were also found in
a study of 40 children in which 75% with soiling had in-
creased breath methane, compared with 16% of children in
a group with constipation and no soiling.8
Both pediatric and adult studies reported a negative corre-
lation between frequency of bowel movements and breath
methane concentration in methane producers.9,11There are
reports showing that successful management of constipation
may eliminate methane production after 6 to 8 weeks of di-
etary and laxative therapy.9
Methane has consistently been associated with constipa-
tion-predominant irritable bowel syndrome in adults under-
going lactulose breath testing.11,21Older studies of healthy
adults also have shown longer transit time in methane pro-
ducers.7,22Methane producers had significantly higher co-
lonic fecal load (FI score) as was shown in our study. Our
study also suggests that methane not only increases fecal
load but also provides a favorable environment for increased
growth of methanogenic bacteria and SIBO. High intestinal
bacterial load might also exacerbate the symptoms of consti-
pation, flatulence, and encopresis.
The effect of rectal distension on the upper gastrointestinal
motility has been documented in both animal and human
studies. The effect of continuous isobaric rectal distension
on gastric emptying and orocecal transit was evaluated in
young females. The rectal distension significantly prolonged
the gastric half-emptying time; however, the mean orocecal
ferent.23In a study on 77 patients with slow transit constipa-
tion, 43% exhibited altered motor function in the esophagus
or small bowel.24Thefrequency of bowelmovementsin those
with upper gastrointestinal dysmotility was less (0.5 ? 0.1 vs
1.3 ? 0.3 bowel movements/per week, P = .04).24The preva-
lence of altered motility (43%) is similar to the percentage of
our study group (42%) with SIBO. It is likely that small intes-
tinal dysmotility can be an additional important factor in the
increased prevalence of SIBO in patients with encopresis.
Our study has some limitations. The gold standard test for
SIBO is the direct culture. The breath hydrogen/methane test
is an indirect test for SIBO. The lactulose breath test was cho-
sen to prove it because it is easy to perform and noninvasive.
The lactulose used without dilution is a hypertonic sub-
strate25that will likely alter transit time; therefore we used
a hypoosmolar solution. We were not able to retest all of
the patients with encopresis and SIBO because many either
refused retesting or were lost to follow-up. Our control sub-
jects were patients seen in the outpatient gastroenterology
clinic for symptoms other than constipation or encopresis
and were therefore not ‘‘healthy’’ volunteers.
There is no clear agreement in the literature regarding the
optimal substrate, cut-off values for hydrogen and methane
and the time of their elevation for bacterial overgrowth. Lac-
tulose and glucose are the most commonly used substrates.
sult. Some advocate the use of the ‘‘double peak’’ method,
which has been defined as an early peak of 2 consecutive hy-
drogen values >10 ppm above the baseline value that is
clearly distinguishable fromacolonicpeakof >20ppmabove
baseline20or a rise of 20 ppm occurring more than 15 min-
utes before a colonic peak.19Although this double peak is
rarely seen in clinical practice,26in our study we found that
greater than one third of patients with SIBO had a double
There is no optimal noninvasive study for the diagnosis of
SIBO. In a review of published papers regarding SIBO,
Khoshini et al27concluded that the intestinal culture studies,
which are considered the gold standard, did not meet the
quality standards. Their analysis suggests that glucose breath
tests had somewhat better specificity and sensitivity then
those studies that used lactulose as substrate.
We conclude that children with fecal impaction and en-
evated basal methane levels and higher methane production.
Methaneproductionwasassociatedwithmore severe colonic
sit time but is strongly associated with constipation. This rai-
ses an interesting question; do factors (diet, antibiotic use,
etc) that influence colonic flora and increase methane pro-
duction contribute to the development of constipation and
fecal impaction or is methane production just the conse-
quence of fecal impaction? A larger study looking at changes
in motility, methane production, and symptoms after antibi-
otic treatment in constipated patients with encopresis with
documented SIBO would provide important information. n
The authors thank Jerrianne Kuntz, RN, for her assistance with breath
Submitted for publication Jun 22, 2009; last revision received Sep 14, 2009;
accepted Oct 30, 2009.
Reprint requests: Karoly Horvath, MD, PhD, Alfred I. duPont Hospital for
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Figure 1. Abdominal radiograph-based scoring system for FI. Download full-text
Bacterial Overgrowth and Methane Production in Children with Encopresis