Neurogastroenterology & Motility

Neurogastroenterol Motil (2014) 26, 779785 doi: 10.1111/nmo.12324

Effect of a low-flatulogenic diet in patients with

flatulence and functional digestive symptoms

F. AZPIROZ ,* C. HERNANDEZ ,* D. GUYONNET , A. ACCARINO ,* J. SANTOS ,* J.-R. MALAGELADA * & F. GUARNER *

*Digestive System Research Unit, University Hospital Vall dHebron, Centro de Investigaci
on Biomedica en Red de Enfermedades
Hepaticas y Digestivas (Ciberehd), Departament de Medicina, Universitat Aut
onoma de Barcelona, Bellaterra (Cerdanyola del
Valles), Spain
Digestive Health Department, Danone Research, Palaiseau, France

Key Message

A diet low in fermentable residues reduced subjective perception of functional digestive symptoms and the
objective number of anal gas evacuations, which served as a marker of the response to treatment.
Our aim was to demonstrate the potential effects of diet on gas-related symptoms.
In 30 patients complaining of flatulence and other abdominal symptoms the effect of a low-flatulogenic diet on
gas evacuation, abdominal symptoms and well-being was tested using a controlled randomized parallel design.
The test diet significantly reduced the number of anal gas evacuations, the sensations of flatulence and
abdominal distension, and enhanced digestive well.

Abstract reduced the number of gas evacuations (by 54  10%;

Background Diets rich in fermentable residues
increase intestinal gas production. Our aim was to
demonstrate the potential effects of diet on gas-related
symptoms. Methods The effect of a low-flatulogenic
test diet (restricted to foodstuffs low in fermentable
residues; n = 15) was compared to that of a balanced
control diet (Mediterranean type; n = 15) in 30
patients complaining of flatulence and other abdom-
inal symptoms using a randomized parallel design.
The following outcomes were measured daily: number
of anal gas evacuations by an event marker, severity of
gas-related symptoms by 010 scales, and sensation of
digestive comfort by a 5 (unpleasant) to +5 (pleasant)
scale. Measurements were taken pretreatment for
3 days on their habitual diet and for 7 days during
the treatment phase. Key Results No pretreatment
differences were detected between patients allocated
to the control or test diets. The test diet significantly
p = 0.002 vs basal diet) whereas the control diet had a
lesser effect (reduction by 28  9%; p = 0.059 vs basal
diet; p = 0.089 vs test diet). Compared to the control
diet, the test diet significantly reduced flatulence (by
48  7% vs 27  8%, respectively; p = 0.018), abdom-
inal distension (by 48  4% vs 22  12%, respec-
tively; p = 0.038), and enhanced digestive well-being
(by 149  18% vs 58  22%, respectively; p = 0.006).
Conclusions & Inferences In patients with gas-related
symptoms, a low-flatulogenic diet produces immedi-
ate beneficial effects with digestive, cognitive, and
emotive dimensions. The number of gas evacuations is
an objective biological marker of response to dietary
treatment.
Keywords clinical intestinal disorders, colonic motil-
ity and disorders, functional disorders.

Address for Correspondence
Fernando Azpiroz, MD, Digestive System Research Unit,
Hospital General Vall dHebron, Barcelona 08035, Spain.
Tel: (34) 93 274 62 22; fax: (34) 93 489 44 56;
e-mail: azpiroz.fernando@gmail.com
Received: 22 November 2013
Accepted for publication: 30 January 2014
INTRODUCTION
Many patients with functional gut disorders attribute
their symptoms to excessive intestinal gas. Among gas-
related symptoms, the predominant complaint is flat-
ulence, defined as an increase in the number of anal gas
evacuations. Flatulence is frequently associated with

2014 John Wiley & Sons Ltd 779

F. Azpiroz et al.
other symptoms that patients may relate to the
accumulation of intestinal gas, such as abdominal
bloating defined as a subjective sensation of increased
abdominal pressure, and abdominal distension defined
as an increase in girth.1,2
Intestinal gas is produced by and large in the colon
where unabsorbed dietary components are fermented
by colonic bacteria.35 The composition and metabolic
activity of colonic microbiota exhibit very wide inter-
individual variations.68 Hence, the amount of gas
produced by each subject depends not only on the
fermentable substrates reaching the colon, but also on
the individuals composition of microbiota. Gas-
related symptoms may respond to diets low in non-
absorbable fermentable substrates; however, despite its
clinical significances, experimental evidence in sup-
port of this treatment option is scant.2,913 Our aim
was to test the efficacy of a low-residue diet on
flatulence and other gas-related symptoms. To this
end, we selected a series of patients primarily com-
plaining of flatulence, and compared the effect of the
low-flatulogenic test diet to that of a balanced control
diet using a randomized parallel design. The charac-
terization of these patients compared to healthy sub-
jects has been previously reported.1 To rule out basal
differences between treatment groups, patients were
evaluated prior to treatment, first during a period on
their habitual diet and thereafter during a period on a
diet rich in fermentable residues (Fig. 1).
MATERIAL AND METHODS
Participants
Patients who consulted for excessive passage of gas through the
anus were instructed to complete a pre-entry questionnaire (see
Figure 1 Study procedure and design. The effect of a low-flatulogenic
test diet (n = 15) was compared to that of a balanced control diet (n = 15)
using a randomized parallel design. Both groups were characterized
pretreatment on their habitual diet and on a high-residue diet.
780
Neurogastroenterology and Motility
details in Clinical questionnaire below); only those scoring anal
gas evacuation 5 on a 10-point scale were invited to participate in
the study. Other eligibility criteria were: age between 18 and
70 years, bodyweight between 18 and 30 Kg/m2, and willingness
to follow dietary instructions. Thirty patients were included in
the study (Table 1), which was conducted at the University
Hospital Vall dHebron between April 2010 and November 2011.
All patients gave their written informed consent to participate in
the study. The study protocol had been previously approved by the
Institutional Review Board of the University Hospital Vall
dHebron. The procedures followed were in accordance with the
World Medical Associations Declaration of Helsinki (1964, and
its later amendments).
Measurements
Number of anal gas evacuations The number of anal gas
evacuations was measured using an event marker (DT2000
Memory Stopwatch; Digi Sport Instruments, Shanggiu, China),
which records the timing over 24 h when a button is pressed.
Participants were instructed to carry the event marker during the
day and register every passage of anal gas. On each study day, the
recording time was divided into three thirds, and the number of
evacuations during each third was counted. Previous studies
measuring the number of gas evacuations simultaneously by an
event marker and the continuous recording of anal gas evacuation
showed a very good correlation.1417
Clinical questionnaire Participants were instructed to complete a
daily questionnaire evaluating the following parameters: (a)
number of bowel movements and stool form using the Bristol
scale18; (b) subjective sensations (overall rating integrating fre-
quency and intensity) of flatulence (anal gas evacuation), abdom-
inal bloating (pressure/fullness), abdominal distension (girth
increment), borborygmi, and abdominal discomfort/pain, by
corresponding 010 analog scales; and (c) digestive/abdominal
sensation of well-being (feeling good or not) using a 10-point scale
graded from 5 (dissatisfaction/unpleasantness) to +5 (satisfac-
tion/pleasantness). Participants were instructed to keep a diary
specifying the foods consumed to confirm compliance with the
diet.
Segmental gas distribution in the gut Abdominal CT scans were
obtained with a helical multislice CT scanner (Mx8000; Philips
Medical Systems, Best, The Netherlands) with the following
specifications: exposure of 120 kV and 50 mAs, 2.5-mm section
thickness, reconstruction at 1.6-mm intervals, 1.5 pitch ratio, and
512 9 512 acquisition matrix.19 With these characteristics, the
total effective dose was 2.4 mSv, similar to the dose of a CT
Table 1 Demographic and clinical characteristics pretreatment
Study groups
Control diet Test diet
Age (mean  SE, years) 50  3 55  3
BMI (mean  SE, Kg/m2) 26  1 26  1
Sex (women/men, n) 7/8 11/4
Clinical syndrome
Postprandial distress syndrome (n) 7 8
IBS (n) 7 4
Functional abdominal pain (n) 1 3
2014 John Wiley & Sons Ltd
Volume 26, Number 6, June 2014
colograph and ~ of the dose of a standard CT scan.20 Abdominal
CT image analysis was performed using a software program
developed in our laboratory.19 The program permits fully auto-
mated measurement of total gas volume within the abdominal
cavity, and the measurement of segmental volumes in selected
regions of the gut using a three-dimensional reconstruction
program specifically developed for that purpose.
Study procedure and design
Patients were randomly allocated (using a computer-generated
sequence) into control and test groups (n = 15 each). One
researcher (JS) generated the random allocation sequence, enrolled
participants, and assigned participants to treatment groups.
Patients were blinded to the assigned intervention. Prior to
treatment, each study group was characterized as follows: firstly,
patients were instructed to continue on their habitual diet for
3 days, and were then placed on a diet rich in fermentable residues
for a further 3 days (Fig. 1). Each meal of the high-residue diet
(breakfast, lunch, dinner) included at least one portion of the
following: (a) bread, cereals, pastries made of whole wheat or corn;
(b) beans, soya beans, corn, broad beans, peas; (c) Brussels sprouts,
cauliflower, broccoli, cabbage, celery, onions, leeks, garlic, arti-
chokes; (d) bananas, figs, peaches, grapes, prunes. The patients
then entered the 7-day treatment phase during which they
consumed either the test diet (low in fermentable residues) or
the control diet (balanced Mediterranean type), as described below
(Fig. 1). On the low-flatulogenic test diet, patients were instructed
to eat as much as they liked but were restricted to the following
foodstuffs: (a) meat, fish, fowl, eggs; (b) lettuce, tomatoes, avocado,
olives; (c) rice, gluten-free bread, rice bread; (d) dairy products; (e)
strained orange juice, berries; (f) sugar, chocolate, coffee, wine,
vinegar, oil. On the balanced control diet patients were instructed
to eat each day: (a) 23 portions of meat, fowl, fish, or eggs; (b) two
portions of vegetables, salad or legumes; (c) four portions of bread,
rice, pasta, potatoes, or cereals; (d) two portions of dairy products;
(e) two portions of fruit; and (f) three portions of oil or butter
(15 mL or 10 g/portion, respectively). A specifically trained nurse
provided detailed instructions on the foods to be consumed and
avoided on each diet and encouraged patient compliance by
regular phone calls. Patients were instructed to complete the daily
clinical questionnaires during the 3 days on the habitual diet, the
last day on the high-residue diet, and during the 7-day treatment
phase. Daytime anal gas evacuations were registered for 3 days on
the habitual diet, the last day on the high-residue diet, and the last
day of the treatment phase (Fig. 1). Intestinal gas distribution was
measured on the high-residue diet. Weight and girth (measured by
tape measure) were registered on the last day of the habitual diet
and treatment phase (Fig. 1).
Data analysis and statistical analysis
No formal calculation of sample size was made in this pilot study.
The primary outcome was the number of gas evacuations and the
secondary outcomes were the intensity of abdominal sensations
and digestive well-being. In each group of patients, the effect of
diet was calculated as the difference of basal (mean of 3 days)
minus the 7th treatment day. Mean or grand mean values (SE) of
all parameters measured were calculated. The KolmogorovSmir-
nov test was used to check data distribution normality. Compar-
isons of parametric normally distributed data were made by
Students t-test, paired tests for intragroup comparisons, and
unpaired tests for intergroup comparisons; otherwise, the Wilco-
xon signed-rank test was used for paired data and the Mann
2014 John Wiley & Sons Ltd
Diet for gas-related symptoms
Whitney U-test for unpaired data. Correlations of paired data were
analyzed by linear regression analysis. Prevalence of specific
features among individuals was compared by the chi-square test.
A p < 0.05 was considered significant for all statistical analyses.
RESULTS
Characterization of study groups pretreatment
Demographics Demographic data of patients allocated
to the control diet and the test diet are shown in
Table 1. All patients reported associated symptoms
and fulfilled Rome III criteria for specific functional
gut disorders,21,22 with a similar distribution of
postprandial distress syndrome, irritable bowel syn-
drome (IBS), and functional abdominal pain in both
groups (Table 1). All randomized patients completed
the trial and were analyzed.
Habitual diet The daily calorie and fiber intake, while
patients remained on their habitual diet during the
pretreatment phase, was similar in those allocated to
the control diet group (1475  51 kcal, 17.2  0.8 g
fiber) and the test diet group (1692  99 kcal,
16.9  1.3 g fiber). Patients reported subjective percep-
tion of flatulence, abdominal symptoms and digestive
discomfort, and the intensity of these sensations was
similar in both groups (Fig. 2 and Table 2). Scores on
the pre-entry questionnaires were remarkably similar
to those obtained during the pretreatment phase (on
habitual diet), and day-to-day variability in the sensa-
tions was low (Fig. 2 and Table 2). No differences in
stool form and frequency were detected between the
control diet (4.0  0.3 Bristol score; 1.3  0.1
daily stools) and test diet (4.5  0.3 Bristol score;
1.5  0.2 daily stools) groups. On their habitual diet,
the number of gas evacuations was similar in both
groups (22  3 and 22  5 daily evacuations, respec-
tively; Fig. 3).
High-residue diet On the high-residue diet, subjective
symptom scores and the number of gas evacuations
increased to a similar level in the groups of patients
allocated to the control and test diets (up to 42  6 and
47  10 daily evacuations, respectively; Table 2).
Abdominal gas content and distribution, measured
while on the high-residue diet, was similar in the
control diet group (159  24 mL total volume;
32  10 mL in the stomach, 26  11 mL in the small
bowel, and 101  15 mL in the colon) and in the test
diet group (175  33 mL total volume; 26  6 mL in
the stomach, 23  9 mL in the small bowel, and
127  33 mL in the colon).
781
F. Azpiroz et al. Neurogastroenterology and Motility

lower than on the habitual diet pretreatment

(p < 0.001); fiber intake on the control diet
(15.4  1.2 g) did not differ from the habitual or test
diets. Neither the test nor control diets significantly
influenced stool frequency or consistency. The test
diet reduced girth (by 0.7  0.2 cm; p = 0.002 vs basal)
and weight (by 0.6  0.1 Kg; p < 0.001 vs basal); the
control diet had inconsistent effects which overall did
not differ statistically from those observed on the test
diet.

Subjective sensations All digestive/abdominal sensa-

tions, including digestive well-being, significantly
improved on the test diet (p < 0.014 by ANOVA for all).
The improvement started early and increased over the
initial days on the diet (Fig. 2). The net effect of the test
diet on sensations (change from basal to the 7th day)
was more pronounced than that of the control diet: a
significant difference was observed in flatulence
(p = 0.018), abdominal distension (p = 0.038), and
digestive well-being (p = 0.006); a trend was also
observed in bloating sensation (p = 0.062; Fig. 2). Thus,
in the majority of patients on the test diet (12 of 15)
symptoms became relatively mild (4 score), a propor-
tion higher than that observed on the control diet (4 of
15; p = 0.009 vs test diet by chi-square test). The effect
of the control and test diets on sensation rates was not
related to the pretreatment level of these parameters on
the habitual or high-residue diets.

Number of anal gas evacuations The test diet signif-

Figure 2 Effect of diet on abdominal sensations (scored from 0 to 10)
and digestive well-being (scored from +5, i.e. pleasant, to 5, i.e.
unpleasant) measured daily during the basal period on the habitual diet
(3 days; black) and during the treatment period (7 days; gray). Data are
means  SE.
Response to treatment
Girth and weight Daily fiber intake on the low-
flatulogenic test diet (13.6  0.8 g) was significantly
icantly reduced the number of gas evacuations (down
to 7  1 per day; p = 0.002 vs basal diet), whereas the
control diet had a lesser effect (14  2 daily evacua-
tions; p = 0.059 vs basal diet; p = 0.012 vs test diet;
Fig. 3). The net effect of the test diet (reduction by
54  10% from basal to the 7th day) was greater than
the effect of the control diet (by 28  9%); however,
the difference did not reach statistical significance. On
the test diet, the proportion of subjects with fewer than

Table 2 Digestive sensations pretreatment

Control group Test group

Perception score Pre-entry Habitual diet High-residue diet Pre-entry Habitual diet High-residue diet

Flatulence* 8.0  0.3 7.4  0.3 8.6  0.3 8.0  0.4 7.3  0.4 8.8  0.4
Bloating* 5.9  0.7 5.5  0.6 7.1  0.5 6.7  0.6 6.5  0.3 7.9  0.4
Distension* 6.3  0.6 5,5  0.6 6.9  0.5 6.9  0.7 6.3  0.5 8.3  0.3
Discomfort/pain* 5.7  0.6 5.4  0.5 7.5  0.4 6.9  0.5 6.3  0.4 8.4  0.4
Borborygmi* 4.4  0.7 3.9  0.7 4.3  0.6 4.5  0.6 4.0  0.5 5.7  0.6
Well-being 3.3  0.2 2.9  0.2 4.1  0.2 3.9  0.0 3.3  0.2 4.4  0.2

*Abdominal sensations scored from 0 to 10.

Digestive well-being scored from 5 (dissatisfaction/unpleasantness) to +5 (satisfaction/pleasantness). Data are mean  SE.

782 2014 John Wiley & Sons Ltd

Volume 26, Number 6, June 2014
Figure 3 Effect of test (T) and control (C) diets on the number of
daytime anal gas evacuations with respect to pretreatment on the
habitual diet (H). The reduction from pretreatment was significant
with the test diet (p = 0.002), but not with the control diet (p = 0.059;
p = 0.089 vs test diet). Data are individual values ( women, men) on
the habitual diet pretreatment (average of 3 days) and at the 7th day of
treatment.
12 evacuations per day (14 of 15) was significantly
higher than on the control diet (7 of 15; p = 0.005 by
chi-square test). The effect of control and test diets on
the number of gas evacuations was not related to the
pretreatment number of evacuations (Fig. 2). Further-
more, the relationship between the effect of the diets
on the number of gas evacuations and on abdominal
symptoms was poor (R < 0.5 for all).
Influence of sex Overall, no sex differences were
observed in the number of gas evacuations and sensa-
tion scores during the pretreatment period. Similarly,
no sex differences were found in the response to
treatment within each study group.
DISCUSSION
Our data provide experimental evidence in support of
dietary manipulations for the treatment of flatulence
and other abdominal symptoms. Indeed, a diet low in
fermentable residues reduced the subjective perception
of functional digestive symptoms and the objective
number of anal gas evacuations, which served as a
marker of the response to treatment.
Various mechanisms may be involved in the devel-
opment of gas-related symptoms. Diet influences the
volume of gas produced by colonic fermentation,
the volume evacuated, the number of evacuations, and
the sensation of flatulence, as experimentally demon-
strated in the laboratory.1,23,24 However, gas volume is
2014 John Wiley & Sons Ltd
Diet for gas-related symptoms
not the sole cause of flatulence, as some patients
complaining of flatulence do have an increased number
of gas evacuations, but do not expel higher volumes of
gas than healthy subjects on the same diet.1 Conceiv-
ably, in these flatulent patients, a hypersensitive
rectum may impel them to frequently pass gas.
Furthermore, another subset of patients complain of
flatulence but, when objectively measured, the actual
number of evacuations is within normal range.1 In these
patients, the subjective sensation of flatulence may be
related to an increased awareness of gas evacuation
owing to central hypervigilance and/or peripheral
hypersensitivity with a sensation of rectal gas.25,26
In this study, we assessed digestive well-being and
gut comfort by measuring the emotive, i.e. hedonic,
dimension of sensations using a specific scale. In
flatulent patients, gas-related symptoms were associ-
ated with a negative sensation of digestive well-being,
and both the cognitive (symptoms) and affective
dimension (well-being) improved with dietary manip-
ulations. A placebo effect may be involved and con-
tribute to the subjective symptom improvement, as
observed in the group on the control diet. Neverthe-
less, the low-flatulogenic diet produced an objective
reduction in the number of gas evacuations.
The improved symptom scores observed on the low-
flatulogenic diet may have been due to diminished
colonic gas production, but a reduction in a fecal bulk,
as suggested by the reduction in bodyweight, may also
have contributed.27 The effect of the diet on the
number of gas evacuations and sensation of flatulence
was clearer than that on abdominal bloating and
distension. It could be speculated that the improve-
ment in different symptoms is mechanism-dependent:
the effect on gas evacuation and flatulence may be
related to diminished gas production, and the effect on
bloating and distension to bulk reduction.
The clinical applicability of our observations
remains speculative. The low-flatulogenic test diet
showed remarkable short-term efficacy although it had
been designed rather intuitively given the scant infor-
mation available in the literature.2 Our study does not
provide indications on predictors of response; indeed,
the diet was equally effective regardless of the clinical
categories. Furthermore, as the balanced control diet
also worked, at least in some patients, the question is
what degree of dietary restriction should be recom-
mended. We wish to acknowledge the limited sample
size of this proof-of-concept study, the wide age, and
BMI ranges of the patients included and that the
control and test groups were not sex-matched; just how
these factors might influence study outcomes remain
unknown.
783
F. Azpiroz et al. Neurogastroenterology and Motility

Our data indicate that dietary restriction of non-
absorbable, fermentable residues reduces the substrates
available for gas production by colonic microbiota,
with rapid symptomatic benefit. Other types of restric-
tive diets low in fermentable oligosaccharides, disac-
charides, monosaccharides, and polyols (FODMAPs)
have also proven effective in the management of IBS-
type symptoms.28 These interventions may also affect
the composition of microbiota by the negative selec-
tion of species dependent on the missing substrates. To
some extent, this effect is comparable to that obtained
with antibiotics, which have also been proposed for the
treatment of IBS symptoms.29
Recently, the concept of microbiota as a super organ
has been proposed, envisioning the various beneficial
influences of robust and diverse microbiota on the
host, including digestive, metabolic, immune, and
cognitiveemotive effects. The microbiota profile rap-
idly adapts to the type of substrates delivered with the
diet.8,30. For instance, the chronic ingestion of non-
absorbable carbohydrates initially causes gas-related
symptoms which later subside, an adaptive change
attributed to the proliferation of bacteria that metab-
olize the carbohydrates by a non-fermentative pathway
and/or proliferation of microorganisms that consume
the excess gas released by fermentation.31,32 It has been
shown that microbiota in patients with flatulence have
low robustness.1 Thus, the indiscriminate restriction
of non-absorbable substrates in their diet may further
impoverish microbiota, which in turn may worsen
their symptoms in the long term. Hence, the direct and
immediate symptomatic benefit of restrictive diets
must be balanced against their potentially harmful
effects on colonic microbiota. Hopefully, in the future,
deeper understanding of microbiota regulatory mecha-
nisms will permit the design of individually tailored
diets that selectively restrict offending foodstuffs, but
contain the essential substrates for harboring healthy
microbiota.
ACKNOWLEDGMENTS
The authors thank Maite Casaus and Anna Aparici for technical
support, Gloria Santaliestra for secretarial assistance, and
Christine OHara for English editing of the manuscript.
FUNDING
This work was supported by a grant from Danone Research
(France), a grant from the Spanish Ministry of Education (Direc-
ci
on General de Investigaci
on, SAF 2009-07416), Ciberehd, which
is funded by the Instituto de Salud Carlos III, and a Career
Development Award to Carlos Hernandez from the Rome
Foundation.
DISCLOSURE
Dr. Guyonnet is an employee of Danone Research and remaining
authors have no competing interests.
AUTHOR CONTRIBUTION
FA study design, data interpretation, manuscript preparation; CH
data analysis; DG study design, data interpretation; AA study
supervision; JS patient recruitment; J-RM study design, manu-
script revision, and FG study design.

REFERENCES
1 Manichanh C, Eck A, Varela E, Roca J,
Clemente JC, Gonzalez A, Knights D,
Knight R et al. Anal gas evacuation
and colonic microbiota in patients
with flatulence: effect of diet. Gut
2014; 63: 4018.
2 Azpiroz F, Levitt MD. Intestinal gas.
In: Feldman M, Friedman LS, Brandt
LJ, eds. Sleisenger and Fordtrans.
Gastrointestinal and Liver Disease:
Pathophysiology, Diagnosis, Manage-
ment, 9th edn. Canada: Saunders,
Elsevier, 2010: 23340.
3 Anderson IH, Levine AS, Levitt MD.
Incomplete absorption of the carbo-
hydrate in all-purpose wheat flour. N
Engl J Med 1981; 304: 8912.
4 Levitt MD, Hirsh P, Fetzer CA,
Sheahan M, Levine AS. H2 excretion
after ingestion of complex carbohy-
drates. Gastroenterology 1987; 92:
3839.
5 Flourie B, Leblond A, Florent C, Rau-
tureau M, Bisalli A, Rambaud JC.
Starch malabsorption and breath gas
excretion in healthy humans consum-
ing low- and high-starch diets. Gas-
troenterology 1988; 95: 35663.
6 Eckburg PB, Bik EM, Bernstein CN,
Purdom E, Dethlefsen L, Sargent M,
Gill SR, Nelson KE et al. Diversity of
the human intestinal microbial flora.
Science 2005; 308: 16358.
7 Qin J, Li R, Raes J, Arumugam M,
Burgdorf KS, Manichanh C, Nielsen
T, Pons N et al. A human gut micro-
bial gene catalogue established by
metagenomic sequencing. Nature
2010; 464: 5965.
8 Wu GD, Chen J, Hoffmann C, Bittin-
ger K, Chen YY, Keilbaugh SA, Bewtra
M, Knights D et al. Linking long-term
dietary patterns with gut microbial
enterotypes. Science 2011; 334: 1058.
9 Azpiroz F, Malagelada J-R. Abdominal
bloating. Gastroenterology 2005; 129:
106078.
10 Sutalf LO, Levitt MD. Follow-up of a
flatulent patient. Dig Dis Sci 1979;
24: 6524.
11 Wolever TM, Robb PA. Effect of guar,
pectin, psyllium, soy polysaccharide,
and cellulose on breath hydrogen and
methane in healthy subjects. Am
J Gastroenterol 1992; 87: 30510.
12 Wagner JR, Carson JF, Becker R,
Gumbmann MR, Danhof IE. Compar-
ative flatulence activity of beans and
bean fractions for man and the rat. J
Nutr 1977; 107: 6809.
13 Hickey C, Calloway D, Murphy E.
Intestinal gas production following
ingestion of fruits and fruit juice.
Am J Dig Dis 1972; 17: 3839.

784 2014 John Wiley & Sons Ltd

Volume 26, Number 6, June 2014
14 Serra J, Azpiroz F, Malagelada J-R.
Gastric distension and duodenal lipid
infusion modulate intestinal gas
transit and tolerance in humans.
Am J Gastroenterol 2002; 97: 2225
30.
15 Serra J, Azpiroz F, Malagelada J-R.
Mechanisms of intestinal gas reten-
tion in humans: impaired propulsion
versus obstructed evacuation. Am J
Physiol 2001; 281: G13843.
16 Serra J, Azpiroz F, Malagelada J-R.
Intestinal gas dynamics and tolerance
in humans. Gastroenterology 1998;
115: 54250.
17 Serra J, Azpiroz F, Malagelada J-R.
Impaired transit and tolerance of
intestinal gas in the irritable bowel
syndrome. Gut 2001; 48: 149.
18 Heaton KW, ODonnell LJ. An office
guide to whole-gut transit time.
Patients recollection of their stool
form. J Clin Gastroenterol 1994; 19:
2830.
19 Perez F, Accarino A, Azpiroz F, Ma-
lagelada J-R. Gas distribution within
the human gut: effect of meals. Am J
Gastroenterol 2007; 102: 8429.
20 Accarino A, Perez F, Azpiroz F, Qui-
roga S, Malagelada JR. Abdominal
distension results from caudo-ventral
redistribution of contents. Gastroen-
terology 2009; 136: 154451.
2014 John Wiley & Sons Ltd
21 Longstreth GF, Thompson WG, Chey
WD, Houghton LA, Mearin F, Spiller
RC. Functional bowel disorders. Gas-
troenterology 2006; 130: 148091.
22 Tack J, Talley NJ, Camilleri M, Holt-
mann G, Hu P, Malagelada JR, Stang-
hellini V. Functional gastroduodenal
disorders. Gastroenterology 2006;
130: 146679.
23 Tomlin J, Lowis C, Read NW. Inves-
tigation of normal flatus production
in healthy volunteers. Gut 1991; 32:
6659.
24 Steggerda FR. Gastrointestinal gas
following food consumption. Ann N
Y Acad Sci 1968; 150: 5766.
25 Kellow JE, Azpiroz F, Delvaux M,
Gebhart GF, Mertz H, Quigley EM,
Smout AJPM. Applied principles of
neurogastroenterology: physiology/
motility sensation. Gastroenterology
2006; 130: 141220.
26 Azpiroz F, Bouin M, Camilleri M,
Mayer EA, Poitras P, Serra J, Spiller
RC. Mechanisms of hypersensitivity
in IBS and functional disorders.
Neurogastroenterol Mot 2007; 19:
6288.
27 Francis CY, Whorwell PJ. Bran and
irritable bowel syndrome: time for
reappraisal. Lancet 1994; 344: 3940.
28 Halmos EP, Power VA, Shepherd SJ,
Gibson PR, Muir JG. A diet low in
785
Diet for gas-related symptoms
FODMAPs reduces symptoms of irri-
table bowel syndrome. Gastroenter-
ology 2014; 146: 6775.
29 Pimentel M, Lembo A, Chey WD,
Zakko S, Ringel Y, Yu J, Mareya SM,
Shaw AL et al. Rifaximin therapy for
patients with irritable bowel
syndrome without constipation. N
Engl J Med 2011; 364: 2232.
30 Claesson MJ, Jeffery IB, Conde S,
Power SE, OConnor EM, Harris
HM, Coakley M, Lakshminarayanan
B et al. Gut microbiota composition
correlates with diet and health in the
elderly. Nature 2013; 488: 17884.
31 Hertzler SR, Savaiano DA, Levitt
MD. Fecal hydrogen production and
consumption measurements.
Response to daily lactose ingestion
by lactose maldigesters. Dig Dis Sci
1997; 42: 34853.
32 Silk DB, Davis A, Vulevic J, Tzortzis
G, Gibson GR. Clinical trial: the
effects of a trans-galactooligosaccha-
ride prebiotic on faecal microbiota
and symptoms in irritable bowel syn-
drome. Aliment Pharmacol Ther
2009; 29: 50818.