Content uploaded by Santiago Aguadé-Bruix
Author content
All content in this area was uploaded by Santiago Aguadé-Bruix on Jun 17, 2019
Content may be subject to copyright.
Impaired Viscerosomatic Reflexes and Abdominal-Wall Dystony
Associated With Bloating
FABRIZIO TREMOLATERRA,* ALBERT VILLORIA,* FERNANDO AZPIROZ,* JORDI SERRA,*
SANTIAGO AGUADÉ,
‡
and JUAN–R. MALAGELADA*
*Digestive System Research Unit,
‡
Department of Nuclear Medicine, University Hospital Vall d’Hebron, Autonomous University of Barcelona,
Barcelona, Spain
Background & Aims: Abdominal bloating is a frequent
complaint in irritable bowel syndrome (IBS), but its un-
derlying mechanism remains uncertain. Our aim was to
determine whether the abdominal wall, specifically its
adaptation to intra-abdominal volumes, plays a role.
Methods: In 12 patients complaining of abdominal
bloating (8 IBS and 4 functional bloating) and in 12
healthy controls, the effect of colonic gas load (24 mL/
min rectal gas infusion for 1 hour) on perception (mea-
sured by a 0 – 6 scale), abdominal girth, and muscular
activity was tested. With the participants sitting on an
ergonomic chair and the trunk erect, multichannel elec-
tromyography was measured via bipolar surface elec-
trodes located over the upper and lower rectus abdomi-
nis, and the external and internal oblique bilaterally.
Results: In healthy controls, colonic gas loads produced
subjective symptoms (score, 3.0 ⴞ0.3), objective ab-
dominal distention (girth increment, 6 ⴞ1 mm), and
increased the activity of the abdominal muscles (exter-
nal oblique activity, 11% ⴞ3% in; P<.05 vs basal). At
the same infused gas volumes, the patients developed
significantly more symptoms (score, 4.5 ⴞ0.4) and
abdominal distention (11 ⴞ1 mm; P<.05 vs healthy
for both). These abnormal responses were associated
with failed tonic contraction of the abdominal wall (ex-
ternal oblique activity change, ⴚ1% ⴞ4%; Pvalue not
significant vs basal) and paradoxic relaxation of the
internal oblique (activity reduction, 26% ⴞ7%; P<.01
vs basal). Conclusions: In patients with bloating, abdom-
inal perception and distention in response to intra-ab-
dominal volume increments are exaggerated markedly
and associated with muscular dystony of the abdominal
wall.
Patients with irritable bowel syndrome (IBS) fre-
quently report a sensation of bloating associated
with other abdominal symptoms and believe that at
times their girth becomes abnormally enlarged. Intesti-
nal hypersensitivity and impaired handling of gut con-
tents have been proposed as mechanisms of their subjec-
tive symptoms, but the reason for actual abdominal
distention is more uncertain.
1
Several studies have shown
that patients complaining of bloating have impaired
clearance and tolerance of intestinal gas.
2– 6
Furthermore,
some studies reported increased abdominal gas in IBS:
the gas surface in plain abdominal radiographs was 28%–
118% larger in IBS patients than in controls.
7–9
Consid-
ering that the normal volume of intestinal gas is about
200 mL,
2,4,6,10,11
the extra volume in patients could elicit
discomfort, but hardly would account for objective ab-
dominal distention. Other studies failed to show in-
creased volumes of intestinal gas in these pa-
tients.
2,4,6,10,12
In this context, we developed an
alternative hypothesis that would explain the mechanism
of abdominal distention in the absence of a net increment
in intra-abdominal volume. We postulated that disten-
tion represents an abnormal response of the abdominal
wall to its content with intra-abdominal redistribution
and anterior displacement.
Hence, we designed an experimental study with 2
aims: (1) to determine whether patients complaining of
bloating develop abnormal abdominal distention in re-
sponse to a standard volume load, and (2) to show a
potential mechanism for this abnormal response, specif-
ically, abnormal activity of the abdominal muscles. To
these aims, we used a previously validated experimental
model of intestinal gas retention
13
to compare girth and
electromyographic responses of the abdominal muscles in
patients with bloating and healthy controls. In this ar-
ticle the term bloating is used for the patient’s belief that
abdominal girth has increased, and abdominal distention is
used to describe an actual change in girth.
Abbreviations used in this paper: EMG, electromyography; IBS, irri-
table bowel syndrome.
©2006 by the American Gastroenterological Association Institute
0016-5085/06/$32.00
doi:10.1053/j.gastro.2005.12.036
GASTROENTEROLOGY 2006;130:1062–1068
Materials and Methods
Participants
Sixteen patients predominantly complaining of ab-
dominal bloating (12 women, 4 men; age range, 18 –74 years)
and 24 healthy individuals without gastrointestinal com-
plaints (9 women, 7 men; age range, 21– 40 years) were
studied; of these 40 participants, 12 patients and 12 healthy
controls participated in the main study, and the other 16
participated in ancillary studies (see Experimental Design sec-
tion). On a scale from 0 (none) to 4 (incapacitating), the mean
score of bloating in patients was 2.7 ⫾0.1. By using Rome II
criteria, 10 patients were classified as IBS and 6 were classified
as functional bloating.
14
The study protocol had been approved
by the Institutional Review Board of the University Hospital
Vall d’Hebron, and all participants gave written informed
consent to participate in the study.
Abdominal Electromyography
Electromyographic (EMG) activity was recorded at 8
different sites corresponding to the upper rectus, external
oblique, lower rectus, and internal oblique at both sides of the
abdomen (Figure 1).
15
At each site, EMG activity was recorded
by means of bipolar Ag-AgCl surface electrodes with a diam-
eter of 1 cm (Kendall Arbo Kiddy H207PG/F; Tyco Health-
care, Barcelona, Spain) placed 4 cm apart. An abrasive paste
(Everi; Spes Medica, Battipaglia, Italy) was used to reduce skin
impedance. The electrodes were connected to an EMG record-
ing system (Electromyographic System ASE 16; Prima Bio-
medical & Sport, Mareno di Piave, Italy). EMG activity was
recorded at 1024 Hz, amplified 20,000 times, and filtered with
a high-pass filter at 30 Hz and a low-pass filter at 500 Hz.
16
The appropriate location of the electrodes was checked by
recording EMG responses to maximal voluntary abdominal
contractions (global activation of all muscular components;
Figure 2), responses to sit-ups (preferential activation of upper
and lower rectus abdominis), and responses to rotation of the
trunk at both sides in the erect position (activation of ipsilat-
eral internal and contralateral external oblique).
Colonic Gas Load
Colonic gaseous filling was performed by a 60-minute
continuous gas infusion at 24 mL/min (1440 mL final volume)
via a balloon catheter (Foley catheter 20 F; Bard, Barcelona,
Spain) introduced into the rectum and hermetically connected
to a modified volumetric pump (Asid Bonz PP 50-300; Lubra-
tronics, Unterschleissheim, Germany). To prevent rectal gas
leaks, the intrarectal balloon was inflated with 5 mL of water.
The gas mixture infused (88% nitrogen, 6.5% carbon dioxide,
and 5.5% oxygen, bubbled into water for saturation) mim-
icked the partial pressures of venous blood gases to minimize
diffusion across the intestinal-blood barrier.
17,18
Measurement of Abdominal Girth Changes
At the beginning of the experiments, a nonstretch belt
was placed over the umbilicus. The overlapping ends of the
belt were adjusted carefully by means of 2 elastic bands so that
the belt constantly adapted to the abdominal wall. Girth
measurements during the study were performed directly by
means of a metric tape fixed to the belt. All measurements
were performed while participants were breathing quietly and
Figure 2. Example of abdominal EMG activity. A voluntary abdominal
contraction induced a marked increment in the activity of all muscular
components of the abdominal wall.
Figure 1. Abdominal EMG recording. The EMG activities of various
components of the abdominal wall were measured by means of
bipolar surface electrodes at both sides of the abdomen.
April 2006 BLOATING AND ABDOMINAL–WALL DYSTONY 1063
were referenced to the midpoint of respiratory displacements
and by averaging inspiratory and respiratory determinations
over 3 consecutive respiratory excursions. Measurements were
taken at 10-minute intervals without manipulation of the
belt-tape assembly. Previous studies have validated the repro-
ducibility of the measurements
19
and the sensitivity of this
method to detect consistently the small variations in girth
induced by various experimental conditions.
2–5,13
Perception Measurements
Conscious perception was measured at 10-minute in-
tervals by means of 4 graphic rating scales, each graded from
0 (no perception) to 6 (painful sensation), specifically for
scoring 4 possible abdominal sensations: (1) pressure/bloating,
(2) borborigmi/colicky sensation, (3) stingy sensation, and (4)
other type of sensation (to be specified), respectively. The
questionnaire included an additional scale to score rectal per-
ception, and the one presented to patients also had a tick box
(yes/no) to signal the replicability of customary symptoms. The
location of the perceived sensations was marked on an abdom-
inal diagram divided into 9 regions corresponding to the
epigastrium, periumbilical area, hypogastrium, both hypo-
chondria, flanks, and iliac fossae. Participants were instructed
to report the sensations perceived over the preceding 10-
minute period in the scales.
2,3,20–22
Procedure
Participants (both patients and healthy controls) were
instructed to eat a low-flatulogenic diet for the 2 preceding
days. After an 8-hour fast the rectal catheter and the abdominal
EMG surface electrodes were positioned (Figure 1). First,
postural changes of the abdominal muscles were studied by
comparing the EMG activity recorded for 20-second periods in
duplicate at 2-minute intervals in supine rest and in the erect
position with the participants relaxed and sitting on an ergo-
nomic chair. Thereafter, the responses to colonic gas loads were
studied with the participants sitting on the ergonomic chair
with the trunk erect, EMG activity was continuously recorded,
first, during a 30-minute basal period, and subsequently,
during 60-minute colonic gas filling.
Ancillary studies. Studies without colonic gas load. To
rule out potential time effects of prolonged erect position on
abdominal-wall activity, abdominal EMG activity was re-
corded continuously for 90 minutes with the participants
sitting on the ergonomic chair without colonic gas infusion.
Scintigraphic study. To map the intraluminal distribu-
tion of the colonic gas load, the gas infused was labeled with
2mL133Xe (74 MBq). During the 60-minute gas-infusion
period, anterior and posterior abdominal scans were obtained
simultaneously at 60-second intervals using a dual-head, large
field of view gamma camera with high-energy collimators
(Helix; General Electric-Elscint, Haifa, Israel).
Experimental Design
Twelve patients (9 women, 3 men) and 12 healthy
controls (8 women, 4 men) participated in the main studies
(postural activity and responses to gut distention). Eight ad-
ditional healthy controls (4 women, 4 men) were studied
without colonic gas infusion. Another 4 patients (3 women, 1
man) and 4 healthy controls (1 woman, 3 men) participated in
the ancillary scintigraphic study.
Data Analysis
Girth changes were referred to girth measurements at
the start of the basal period. The intensity of abdominal
perception was measured by the scores rated in the scales at
each time interval during the study (using the highest score
when more than 1 sensation was rated simultaneously). In each
participant we also counted the number of times each abdom-
inal sensation was scored to calculate the frequency of each
specific sensation.
EMG activity was measured at 10-minute intervals as the
average root mean square voltage
23
recorded at each specific
muscle over 2-minute periods and was expressed as the percent
change from basal activity.
Scintigraphic images were analyzed by a region-of-interest
program.
22
In each study, 5 regions of interest were defined as
the largest region excluding areas of overlap that encompassed,
respectively, the small bowel, cecum, hepatic flexure, splenic
flexure, and rectosigma. Depth corrections were performed by
calculating the geometric mean of anterior and posterior scans.
The activity measured in each region was divided by its surface
for normalization. The activity in each region was expressed as
the percent of total activity (sum in all 5 regions).
Statistical Analysis
In each group of participants we calculated the mean
values (⫾SE) of the parameters measured. The Kolmogorov–
Smirnov test was used to check the normality of data distri-
bution. Comparisons of parametric, normally distributed data
were performed by the Student ttest, paired tests for intra-
group comparisons, and unpaired tests for intergroup compar-
isons; otherwise the Wilcoxon signed-rank test was used for
paired data and the Mann–Whitney Utest was used for
unpaired data. The Bonferroni correction was applied for mul-
tiple comparisons (right vs left). Correlations of various pa-
rameters were performed by linear regression analysis. The
location of sensations over the abdomen and symptom distri-
bution were compared by the 2test. Differences in regional
radioactivity distribution in the scintigraphic images were
compared by the Wilcoxon signed-rank test.
Results
No differences in body weight or height were
found between patients and healthy controls, and ab-
dominal circumference before the start of the study was
similar in both groups (843 ⫾43 mm vs 795 ⫾20 mm,
respectively; Pvalue not significant). Because no lateral
predominance in abdominal EMG activity was observed,
the right and left activity recorded at each muscular site
was averaged and pooled data are reported. During vol-
1064 TREMOLATERRA ET AL GASTROENTEROLOGY Vol. 130, No. 4
untary abdominal contractions the EMG activity in-
creased to a level somewhat lower in patients than in
healthy controls, but this difference was statistically sig-
nificant only for the internal oblique during ipsilateral
rotation of the trunk (55 ⫾10 vvs97⫾17 vin
healthy controls; P⬍.05).
Postural Activity
In the supine position, no differences in basal
activity were observed between patients and healthy
controls (Figure 3). The activity of the internal oblique
significantly increased when the participant adopted the
erect position, and this increment was similar in patients
and healthy controls (Figure 3).
Responses to Gut Distention
Abdominal distention and symptoms. Compared
with healthy controls, standard colonic loads in pa-
tients produced significantly more perception (score,
4.5 ⫾0.4vs3.0⫾0.3; P⬍.05) and objective
abdominal distention (11 ⫾1mmvs6⫾1 mm; P⬍
.05). In 53% ⫾6% of the occasions during colonic gas
infusion the participants reported more than 1 sensa-
tion perceived simultaneously; pressure/bloating, bor-
borigmi/colicky sensation, and stingy sensation were
reported similarly by patients in 89% ⫾5%, 54% ⫾
7%, and 20% ⫾8% of the occasions, respectively, and
by healthy controls in 90% ⫾4%, 54% ⫾12%, and
20% ⫾8%, respectively. Symptoms were localized in
the abdominal midline over the hypogastrium, peri-
umbilical region, and the epigastrium both in patients
(75% ⫾8%, 67% ⫾10%, and 41% ⫾8%, respec-
tively) and controls (60% ⫾10%, 62% ⫾10%, and
28% ⫾11%, respectively). The extension of the re-
ferral area was larger in patients than in healthy
controls, but the differences did not reach statistical
significance (74% ⫾7% and 53% ⫾2% of symptoms
were referred over more than 2 areas, respectively). In
81% ⫾10% of the occasions, sensations were recog-
nized by the patients as their customary complaints.
Muscular activity of the abdominal wall. In
healthy controls the colonic gas load was associated with
a significant increment in EMG activity of all abdominal
muscles but the internal oblique (Figure 4). These EMG
changes were not attributable to time effects of pro-
longed erect position because no significant increment
was observed in the studies without gas infusion (3% ⫾
4% activity change in the superior rectus, ⫺4% ⫾10%
in the inferior rectus, 19% ⫾23% in the external
oblique, and ⫺27% ⫾9% in the internal oblique). The
response to colonic gas load was impaired markedly in
patients who failed to develop significant increments in
the lower rectus and external oblique and who further-
more showed a significant inhibition of the internal
oblique during colonic gas infusion (Figure 4). Patients
were older than healthy controls, but age did not explain
the differences found because the muscular responses in
the younger half of the patients (ⱕ45 y) were not sig-
nificantly different than in the older half (⬎45 y). In
patients, the degree of inhibition of the internal oblique
correlated with the increment of abdominal girth (Figure
5), but not with the increment in perception score (r ⫽
0.002; P⫽.9).
Colonic gas distribution. The intracolonic gas
distribution through the rectosigma, splenic flexure, he-
patic flexure, and cecum was similar in patients (45% ⫾
11%, 18% ⫾3%, 24% ⫾8%, and 13% ⫾8%,
respectively) and healthy controls (50% ⫾8%, 17% ⫾
2%, 19% ⫾7%, and 14% ⫾7%, respectively; Pvalue
was not significant vs patients), without detectable gas
reflux into the small bowel.
Figure 3. Postural adaptation. The erect position increased the basal
activity of the internal oblique to a similar level in patients and healthy
controls. □, Patients; ●, healthy controls; *, P⬍.05 vs supine.
April 2006 BLOATING AND ABDOMINAL–WALL DYSTONY 1065
Discussion
We have shown that the activity of the abdominal
musculature adapted to intra-abdominal content, that
this modulatory mechanism fails in patients complaining
of bloating, and that the faulty muscular response is
associated with exaggerated abdominal distention in re-
sponse to intra-abdominal volume loads. These data pro-
vide experimental evidence in support of the patients’
claims by showing that they are prone to abdominal
distention caused by abdominal-wall dystony.
We used an experimental model that incorporates a
standard intra-abdominal volume load to determine
whether the girth increment was similar in patients and
healthy controls. Interestingly, the same volume load
produced significantly more abdominal distention in pa-
tients with bloating. In the short term, the configuration
of the anterior abdominal wall is determined by the
balance between intra-abdominal forces and the activity
of the various muscular components of the wall.
1
Hence,
further testing our working hypothesis, we also investi-
gated the response of the abdominal muscles to intra-
abdominal volume increments. First, we were able to
show that healthy controls adapt to intra-abdominal
volume loads by increasing the muscular activity of the
abdominal wall. The EMG response detected probably
reflects a tone increment in the abdominal muscles that
control expansion. This adaptive response likely is me-
diated by viscerosomatic reflexes, which have been char-
acterized in experimental animal models.
24
Interestingly,
we found that patients complaining of bloating show
impaired abdominal contraction in response to colonic
gas loads and even a paradoxic relaxation of the internal
oblique. Our data further show that the decrease in
activity of the internal oblique correlated with incre-
ments in girth, suggesting that the faulty response
would favor an exaggerated protrusion of the anterior
abdominal wall in response to standard volume loads.
Previous studies have suggested that patients with
abdominal distention may have weak abdominal mus-
Figure 4. Responses of abdominal muscles to standard intra-abdom-
inal volume load. In healthy controls the volume load induced signif-
icant contraction of all abdominal muscles, except the internal
oblique. Patients showed an abnormal adaptive response with im-
paired contraction of the lower rectus and external oblique, and
paradoxic relaxation of the internal oblique. □, Patients; , healthy
controls; *, P⬍.05 vs basal.
Figure 5. Relationship between relaxation of the internal oblique and
abdominal distention in response to colonic gas load.
1066 TREMOLATERRA ET AL GASTROENTEROLOGY Vol. 130, No. 4
cles.
25
A later study using an EMG recording of the
abdominal wall
26
showed no differences in basal activity
either in the erect or supine positions between bloating
patients and healthy controls,
26
and the present study
confirms these data. We have shown that the adaptation
of the abdominal wall to posture is similar in patients
and controls, and this change primarily affects the inter-
nal oblique, whose function is to counterbalance gravi-
tational forces and provide support for abdominal con-
tents.
27
However, when a much more potent contraction
of the internal oblique is elicited by ipsilateral rotation of
the trunk, EMG activity is lower in patients than in
healthy controls. The significance of these data cannot be
ascertained because the maneuvers to activate abdominal
muscles cannot be standardized reliably.
Patients not only showed a faulty adaptation of the
abdominal wall and excessive abdominal distention in
response to the intra-abdominal volume load, but also
reported significantly more abdominal complaints. Of
note, the perceived sensations replicated their customary
symptoms, and most patients described them as abdom-
inal fullness/bloating. The question is: where do these
sensations originate from? The distribution of the gas-
eous load in the colon was similar in patients and con-
trols. Abdominal perception did not correlate with
changes in abdominal-wall activity. Hence, increased
perception probably was related to the gut hypersensi-
tivity that is characteristic of IBS.
21
However, we cannot
rule out that in cases of pronounced distention, the
abdominal wall may contribute to the bloating sensation.
The changes in girth induced by the colonic gas load
in patients (⯝1 cm) were similar to those previously
observed under other experimental conditions
2–5,28
but
were relatively small, equivalent to a clinically mild or
even subclinical episode of abdominal distention. Indeed,
the severity of clinical bloating is variable, and our
patients were not at the top of the scale (they scored their
customary bloating as 2.7 on a scale of 0 – 4). The precise
circumstances that trigger the clinically severe episodes
of visible distention have not been well characterized
29
and have not been reproduced experimentally in the
laboratory to date.
Several abnormalities have been detected that may
play a role in the development of abdominal distention.
Gas transit studies have shown nicely that patients com-
plaining of bloating have impaired clearance and reduced
tolerance of intraluminal gas loads.
2,3
This dysfunction
predominantly affects the small bowel,
5
and is related to
abnormal reflex control of gas propulsion.
3
Impaired
handling of gut contents may result in segmental pool-
ing and focal gut distention, which may induce abnormal
viscerosomatic reflexes, leading to abdominal distention.
On the other hand, subjective symptoms in these pa-
tients may originate from the intraluminal stimulus in a
hypersensitive gut and/or from the distended abdominal
wall itself, as discussed earlier. Conscious sensations aris-
ing from the gut also could induce abdominal distention
via abnormal behavioral responses. Gas was used in the
present and in previous studies to investigate the patho-
physiology of abdominal bloating and distention, but
this does not imply that gas is the offending element;
indeed, other intraluminal components, including chyme
and endogenous secretions, also may induce abnormal
responses and symptoms.
Abdominal bloating probably represents a heteroge-
neous condition produced by a combination of patho-
physiologic mechanisms that may differ among individ-
ual patients. The present data add a new perspective to
this puzzle by showing that abnormal viscerosomatic
responses are an important component of the disease
mechanism of distention.
References
1. Azpiroz F, Malagelada J-R. Abdominal bloating. Gastroenterology
2005;129:1060–1078.
2. Caldarella MP, Serra J, Azpiroz F, Malagelada J-R. Prokinetic
effects of neostigmine in patients with intestinal gas retention.
Gastroenterology 2002;122:1748–1755.
3. Serra J, Salvioli B, Azpiroz F, Malagelada J-R. Lipid-induced intes-
tinal gas retention in the irritable bowel syndrome. Gastroenter-
ology 2002;123:700–706.
4. Serra J, Azpiroz F, Malagelada J-R. Impaired transit and tolerance
of intestinal gas in the irritable bowel syndrome. Gut 2001;48:
14–19.
5. Salvioli B, Serra J, Azpiroz F, Lorenzo C, Aguade S, Castell J,
Malagelada J-R. Origin of gas retention and symptoms in patients
with bloating. Gastroenterology 2005;128:574–579.
6. Lasser RB, Bond JH, Levitt MD. The role of intestinal gas in
functional abdominal pain. N Engl J Med 1975;293:524–526.
7. Poynard T, Hernandez M, Xu P, Couturier D, Frexinos J, Bom-
melaer G, Benand-Agostini H, Chaput JC, Rheims N. Visible ab-
dominal distention and gas surface: description of an automatic
method of evaluation and application to patients with irritable
bowel syndrome and dyspepsia. Eur J Gastroenterol Hepatol
1992;4:831–836.
8. Chami TN, Schuster MM, Bohlman ME, Pulliam TJ, Kamal N,
Whitehead WE. A simple radiologic method to estimate the quan-
tity of bowel gas. Am J Gastroenterol 1991;86:599–602.
9. Koide A, Yamaguchi T, Odaka T, Koyama H, Tsuyuguchi T, Ki-
tahara H, Ohto M, Saisho H. Quantitative analysis of bowel gas
using plain abdominal radiograph in patients with irritable bowel
syndrome. Am J Gastroenterol 2000;95:1735–1741.
10. Lasser RB, Levitt MD, Bond JH. Studies of intestinal gas after
ingestion of a standard meal. Gastroenterology 1976;70:A906.
11. Accarino AM, Quiroga S, Azpiroz F, Perez F, Alvarez-Castells A,
Malagelada JR. Changes in intestinal gas during early digestion
evidenced by a new CT analysis program. Gastroenterology
2005;128:A672.
12. Maxton DG, Martin DF, Whorwell P, Godfrey M. Abdominal dis-
tention in female patients with irritable bowel syndrome: explo-
ration of possible mechanisms. Gut 1991;32:662–664.
April 2006 BLOATING AND ABDOMINAL–WALL DYSTONY 1067
13. Harder H, Serra J, Azpiroz F, Passos MC, Aguadé S, Malagelada
J-R. Intestinal gas distribution determines abdominal symptoms.
Gut 2003;52:1708–1713.
14. Thompson WG, Longstreth G, Drossman DA, Heaton K, Irvine EJ,
Muller-Lissner SC. Functional bowel disorders and D. Functional
abdominal pain. In: Drossman DA, Corazziari E, Talley NJ, Thomp-
son WG, Whitehead WE, eds. The functional gastrointestinal
disorders. 2nd ed. McLean, VA: Degnon Associates, 2000:351–
432.
15. Ng JK, Kippers V, Richardson CA. Muscle fibre orientation of
abdominal muscles and suggested surface EMG electrode posi-
tions. Electromyogr Clin Neurophysiol 1998;38:51–58.
16. Redfern MS, Hughes RE, Chaffin DB. High-pass filtering to re-
move electrocardiographic interference from torso EMG record-
ings. Clin Biomed 1993;8:44–48.
17. Foster RE. Physiological basis of gas exchange in the gut. Ann N
Y Acad Sci 1968;150:4–12.
18. Pogrund RS, Steggerda FR. Influence of gaseous transfer be-
tween the colon and blood stream on percentage gas composi-
tions of intestinal flatus in man. Am J Physiol 1948;153:475–
482.
19. Serra J, Azpiroz F, Malagelada J-R. Intestinal gas dynamics and
tolerance in humans. Gastroenterology 1998;115:542–550.
20. Gracely R. Studies of pain in normal man. In: Wall PMR, ed.
Textbook of pain. Edinburgh: Churchill Livingstone, 1994:315–
336.
21. Azpiroz F. Gastrointestinal perception: pathophysiological impli-
cations. Neurogastroenterol Motil 2002;14:229–239.
22. Harder H, Serra J, Azpiroz F, Malagelada J-R. Reflex control of
intestinal gas dynamics and tolerance in humans. Am J Physiol
2004;286:G89–G94.
23. Hägg GM, Melin B, Kadefors R. Applications in ergonomics. In:
Merletti RPP, ed. Electromyography, physiology, engineering, and
noninvasive applications. Hoboken, NJ: John Wiley & Sons, Inc,
2004:343–363.
24. Martinez V, Thakur S, Mogil J. Differential effects of chemical and
mechanical colonic irritation on behavioral pain response to in-
traperitoneal acetic acid in mice. Pain 1999;81:179–186.
25. Sullivan SN. A prospective study of unexplained visible abdomi-
nal bloating. N Z Med J 1994;1:428–430.
26. McManis PG, Newall D, Talley NJ. Abdominal wall muscle activity
in irritable bowel syndrome with bloating. Am J Gastroenterol
2001;96:1139–1142.
27. De Troyer A. Mechanical role of the abdominal muscles in relation
to posture. Respir Physiol 1983;53:341–353.
28. Passos MC, Tremolaterra F, Serra J, Azpiroz F, Malagelada J-R.
Impaired reflex control of intestinal gas transit in patients with
abdominal bloating. Gut 2005;54:344–348.
29. Alvarez W. Hysterical type of nongaseous abdominal bloating.
Arch Intern Med 1949;84:217–245.
Received May 19, 2005. Accepted December 14, 2005.
Address requests for reprints to: Fernando Azpiroz, MD, Digestive
System Research Unit, Hospital General Vall d’Hebron, 08035 Barce-
lona, Spain. e-mail: fernando.azpiroz@telefonica.net; fax: (34) 93-489-
44-56.
Present affiliation of F.T.: Gastroenterology Department, Azienda
Ospedaliera Policlinico, Universita Federico II, Naples, Italy.
Supported in part by the Spanish Ministry of Education (Dirección
General de Enseñanza Superior del Ministerio de Educación y Cultura,
BFI 2002-03413), Instituto de Salud Carlos III (grants 02/3036 and
CO3/02), Generalitat de Catalunya (Direcció General de Recerca
1998SGR-00113), and National Institutes of Health (grant DK 57064).
Also supported by a scholarship from the Spanish Ministry of Health
(ISC III 02/3036 to J.S.) and by a scholarship from the Spanish Ministry
of Health (Ayuda para contratos post Formación Sanitaria Especial-
izada, ISC III 300051 to A.V.).
The authors thank Anna Aparici and Maite Casaus for technical
support, and Gloria Santaliestra for secretarial assistance.
1068 TREMOLATERRA ET AL GASTROENTEROLOGY Vol. 130, No. 4
