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Neurogastroenterology
Original article
Mechanisms of postprandial abdominal bloating and distension in functional dyspepsia
  1. Emanuel Burri1,2,3,4,
  2. Elizabeth Barba1,2,3,
  3. Jose Walter Huaman5,
  4. Daniel Cisternas1,2,3,6,
  5. Anna Accarino1,2,3,
  6. Alfredo Soldevilla7,
  7. Juan-R Malagelada1,2,3,
  8. Fernando Azpiroz1,2,3
  1. 1Digestive System Research Unit, University Hospital Vall d'Hebron, Barcelona, Catalunya, Spain
  2. 2Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (Ciberehd), Barcelona, Catalunya, Spain
  3. 3Department of Medicine, Universitat Autònoma de Barcelona, Barcelona, Catalunya, Spain
  4. 4Department of Internal Medicine, Stadtspital Triemli, Zürich, Switzerland
  5. 5Digestive Department, Hospital General de Catalunya, Barcelona, Spain
  6. 6Departamento de Gastroenterología, Facultad de Medicina, Pontificia Universidad Católica de Chile, Santiago, Chile
  7. 7Department of Physics, Polytechnic University of Catalonia, Barcelona, Spain
  1. Correspondence to Fernando Azpiroz, Digestive System Research Unit, University Hospital Vall d'Hebron 08035 Barcelona, Catalunya, Spain; azpiroz.fernando{at}gmail.com

Abstract

Objective Patients with irritable bowel syndrome and abdominal bloating exhibit abnormal responses of the abdominal wall to colonic gas loads. We hypothesised that in patients with postprandial bloating, ingestion of a meal triggers comparable abdominal wall dyssynergia. Our aim was to characterise abdominal accommodation to a meal in patients with postprandial bloating.

Design A test meal (0.8 kcal/ml nutrients plus 27 g/litre polyethylenglycol 4000) was administered at 50 ml/min as long as tolerated in 10 patients with postprandial bloating (fulfilling Rome III criteria for postprandial distress syndrome) and 12 healthy subjects, while electromyographic (EMG) responses of the anterior wall (upper and lower rectus, external and internal oblique via bipolar surface electrodes) and the diaphragm (via six ring electrodes over an oesophageal tube in the hiatus) were measured. Means +/− SD were calculated.

Results Healthy subjects tolerated a meal volume of 913±308 ml; normal abdominal wall accommodation to the meal consisted of diaphragmatic relaxation (EMG activity decreased by 15±6%) and a compensatory contraction (25±9% increase) of the upper abdominal wall muscles (upper rectus and external oblique), with no changes in the lower anterior muscles (lower rectus and internal oblique). Patients tolerated lower volume loads (604±310 ml; p=0.030 vs healthy subjects) and developed a paradoxical response, that is, diaphragmatic contraction (14±3% EMG increment; p<0.01 vs healthy subjects) and upper anterior wall relaxation (9±4% inhibition; p<0.01 vs healthy subjects).

Conclusions In functional dyspepsia, postprandial abdominal distension is produced by an abnormal viscerosomatic response to meal ingestion that alters normal abdominal accommodation.

  • FUNCTIONAL DYSPEPSIA
  • GASTRIC MOTILITY
  • GASTROINTESTINAL FUNCTION
  • VISCERAL SENSITIVITY
  • FUNCTIONAL BOWEL DISORDER

https://doi.org/10.1136/gutjnl-2013-304574

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    Significance of this study

    What is already known about this subject?

    • In response to bowel distension by gas, in healthy individuals, a reflex mechanism causes the anterior abdominal wall to contract and the diaphragm to relax to accommodate the intra-abdominal gas load.

    • Patients with IBS-related or functional bloating exhibit abnormal abdominal accommodation to colonic gas loads.

    • In healthy subjects, ingestion of a meal elicits a similar process of abdominal accommodation, which suggests that this is a physiological phenomenon.

    What are the new findings?

    • Postprandial bloating in patients with functional dyspepsia has a dual component: a subjective bloating sensation attributable to gastric dysfunction (impaired accommodation and hypersensitivity); objective abdominal distension due to abnormal abdominal accommodation (paradoxical diaphragmatic contraction and anterior wall relaxation).

    How might it impact on clinical practice in the foreseeable future?

    • Thorough evaluation and potential management of postprandial bloating in functional dyspepsia should consider abdominal wall motion in addition to gastric dysfunction.

    Introduction

    By means of an experimental model of colonic gas infusion in healthy individuals, we demonstrated that the abdominal walls actively accommodate changes in intra-abdominal content.1 ,2 This process involves metered diaphragmatic relaxation coupled with a compensatory anterior wall contraction that prevents excessive abdominal distension. In subsequent studies, we further proved abdominal accommodation to be a physiological phenomenon also triggered by meal ingestion.3

    Abdominal bloating is a frequent complaint in patients with irritable bowel syndrome.4 Using the provocative colonic gas infusion test, we showed that patients with bloating exhibit abnormal abdominal accommodation in response to intraluminal gas loads.5 Patients with dyspepsia and postprandial distress syndrome are characterised by abdominal bloating after meal ingestion.6 ,7 We hypothesised that, in analogy to irritable bowel syndrome (IBS), dyspeptic bloating is related to abnormal abdominal accommodation to meal loads. Hence, our aim was to characterise the muscular response of the anterior abdominal wall and diaphragm to a test meal in patients with dyspepsia complaining of postprandial bloating, and relate the bloating sensation to objective abdominal distension.

    Material and methods

    Participants

    Patients whose major complaint was postprandial abdominal bloating, that is, who believed that their abdomen distended after meals, and with organic diseases ruled out by a clinical workup, were prospectively recruited from the gastroenterology outpatient clinic. Based on sample size calculations (see statistical analysis below), 10 patients (all women; age range: 29–65 years; mean body mass index (BMI±SD 24.6±5.6 kg/m2) were included the study. Using a standard abdominal symptoms questionnaire8–12 all patients were found to fulfil Rome III criteria for postprandial distress syndrome.7 Twelve healthy subjects (10 women, 2 men; age range: 20–37 years; BMI 22.8±1.7 kg/m2) without gastrointestinal symptoms (verified by the standard symptom questionnaire) were recruited by public advertising to serve as controls. The study protocol was approved by the Institutional Review Board of the University Hospital Vall d'Hebron, and all subjects gave their written informed consent to participate in the study.

    Intra-abdominal volume load

    A liquid test meal was administered orally as long as tolerated at a fixed rate of 50 ml/min. The test meal consisted of a water mixture of nutrients (833 ml/litre Edanec, Abbott, Madrid, Spain (0.8 kcal/ml)) to delay gastric emptying and non-absorbable polyethylenglycol 4000 (27 g/litre) to prevent water absorption.

    Electromyography of the abdominal walls

    Muscular activity of the abdominal walls, that is, the diaphragm and anterior wall, was recorded by electromyography (Electromyographic System ASE 16, PRIMA Biomedical and Sport, Mareno di Piave, Italy) 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.13

    Diaphragmatic electromyographic (EMG) activity was measured via intraoesophageal electrodes mounted over a probe. The probe consisted of a polyvinyl tube with six ring electrodes, 5 mm wide, at 15 mm intervals. The electrodes were made using a pen dispenser for drawing highly conductive silver traces (Conductive Pen, Chemtronics, Leeds, UK). The electrodes were connected by insulated copper wires (200 µm in diameter) running through the lumen of the tube to external plugs. After nasal intubation, the radio-opaque electrodes were positioned across the diaphragmatic hiatus under fluoroscopic control with the trunk erect (as during the subsequent test period). Bipolar EMG activity was recorded from contiguous electrodes. The position of the electrodes was rechecked (and adjusted if necessary) by recording the responses to a Valsalva manoeuvre. Cardiac activity was superimposed on the diaphragmatic EMG signal: to prevent electrocardiographic artefacts, 0.2 s intervals were removed from the diaphragmatic EMG signal around each QRS peak using a specifically developed digital filter. This method, previously described in detail, has been validated by showing reproducible and selective responses to various conditions1 ,2; specifically, it was shown that EMG activity increased in response to Valsalva manoeuvres (figure 1) and to abdominal inspiration (diaphragmatic contraction), but not to thoracic inspiration (intercostal contraction), whereas EMG activity decreased in response to intra-abdominal loads, which were shown by ultrasonography and CT scanning to be associated with diaphragmatic ascent.1 ,2

    Figure 1
    Figure 1

    Example of diaphragmatic electromyographic (EMG) recording. (A) Raw signal; (B) filtered signal; (C) integrated tracing (root mean square of the 10 previous samples). Note increase in EMG activity during Valsalva manoeuvre compared with baseline rest.

    Anterior abdominal wall activity was recorded via bipolar electrodes (Kendall Arbo Kiddy H207PG/F, Tyco Healthcare, Barcelona, Spain) at four different sites: upper rectus, external oblique, lower rectus and internal oblique on the right side of the abdomen.8 ,14 The appropriate location of anterior wall electrodes was verified by recording EMG responses to sit ups (preferential activation of upper and lower rectus) and responses to trunk rotation (activation of ipsilateral internal and contralateral external oblique).

    Girth measurement

    The method has been previously described in detail.8 Briefly, a non-stretch belt (48 mm wide) was placed over the umbilicus and fixed to the skin on the back to prevent slipping. The overlapping ends of the belt were adjusted carefully by two elastic bands to maintain the belt constantly adapted to the abdominal wall. Girth measurements during the study were taken directly with a metric tape measure fixed to the belt. Measurements were obtained at 5 min intervals. Previous studies validated the reproducibility of the measurements and sensitivity of this method to consistently detect the small variations in girth induced by various experimental conditions.8 ,10 ,11 ,15–17

    Perception measurement

    Abdominal perception was measured by graphic rating scales graded from 0 (no perception) to 6 (painful sensation). Independent scales were used for scoring pressure/bloating, cramp/rumbling sensation, puncture/stinging sensation, and nausea. The location of the sensations (epigastrium, periumbilical area, hypogastrium, both hypochondria, flanks and iliac fossae) was marked on an abdominal diagram. During the study, participants, previously instructed, were asked to score the sensations perceived during the preceding 5 min period (one or more sensations simultaneously) on the scales. This method has been extensively used and previously validated in detail.8 ,12 ,15 ,17 ,18

    Procedure and experimental design

    Participants were instructed to fast for 8 h prior to the study. A 10 min equilibration period was allowed after the preparatory procedures. Studies were conducted with participants sitting erect on an ergonomic chair.8 ,19 ,20 The back of the chair was adjusted to the lumbar area to fix the curvature of the spine. Valsalva manoeuvres were performed at the beginning of each experiment. Perception, girth and EMG activity were measured at 5 min intervals during a 15 min basal period and during ingestion of the test meal. Each participant was studied once.

    Data analysis

    Abdominal perception intensity was measured by the scores rated on the scales at each time interval during the study (using the highest score when more than one sensation was simultaneously rated). EMG activity was measured (at 5 min intervals) as the root mean square voltage8 ,21 averaged over 1 min periods. Responses to different volumes of the test meal were expressed as a percentage of change from basal. Diaphragmatic activity was measured at each recording lead, and the activity recorded by the best two channels was averaged. The maximum volume tolerated by each subject was determined, and responses to 25%, 50%, 75% and 100% of the maximum tolerated load were measured (mean of two measurements taken at 5 min intervals). Unless otherwise stated, values corresponding to 100% of the maximum load tolerated (as defined above) are provided (mean values of measurements during the last min of ingestion and 5 min before). Measurements at other time points were taken as the mean of the two closest measurements.

    Statistical analysis

    Sample size was calculated based on previous data.5 With a 15% EMG activity change with a power of 80% and a significance level of 5% (two sided) being anticipated, at least six participants were required in each group. Volume–response curves were constructed by averaging (±SD) the responses to 25%, 50%, 75% and 100% of the volume ingested.

    The Kolmogorov–Smirnov test was used to check the normality of data distribution. Intragroup comparisons were made by paired analysis using Student t test for parametric normally distributed data and the Wilcoxon signed rank test otherwise. Intergroup comparisons were performed by one-way analysis of variance (ANOVA) and Mann–Whitney U test if applicable. The association of parameters was analysed using Pearson's correlation and linear regression analysis. Perception of the different types of symptoms and their distribution over the abdomen was compared by the χ2 test. A p value<0.05 was considered significant for all statistical analyses.

    Results

    Abdominal perception and tolerance to the test meal

    Prior to meal ingestion, 7 of the 10 patients with dyspepsia reported a mild sensation of abdominal pressure/bloating (overall 1.7±1.4 score), whereas healthy subjects reported no perception. Patients perceived significantly lower meal loads than healthy subjects: perception thresholds (minimal volume that induced a change in perception) were 246±13 ml versus 458±279 ml, respectively (p=0.026). Similarly, patients tolerated smaller meal volumes than healthy subjects: 604±310 ml (12±6 min ingestion time) versus 913±308 ml (18±3 min ingestion), respectively (p=0.030). In healthy subjects, a meal volume of 600 ml (equivalent to the mean volume tolerated in patients) induced relatively mild perception (2.4±0.9 score). Likewise, at the common maximum volume tolerated by all subjects (210 ml), perception scored 0.5±0.1 in healthy subjects versus 2.7±0.3 in patients (p<0.001).

    The type of sensations described by patients and healthy subjects in response to the test meal was similar (no differences by ANOVA): pressure/bloating (90±32% and 70±38%, respectively), cramp/rumbling sensation (7±21% and 10±25%, respectively), puncture/stinging sensation (20±42% and 12±30%, respectively) and nausea (28±42% and 7±17%, respectively). In both groups, the type of sensation did not change throughout the meal ingestion period. In patients, the types of sensation were also similar regardless of tolerance; that is, they were the same in the half of patients with lower tolerance as in the half of patients with higher tolerance.

    Sensations were perceived predominantly over the abdominal midline. However, extension of the referral area on the abdominal surface manifested by patients was greater than in healthy subjects (36±17 vs 14±6, respectively, p=0.005) and more frequently included the periumbilical area (92±15% vs 26±23%; p<0.001). In patients, the referral pattern of the sensations did not depend on the volume tolerated and was similar in the half of patients with higher tolerance versus the half with lower tolerance.

    Abdominal wall responses to the test meal

    Ingestion of the test meal produced a relatively small but significant increment in girth (figure 2). With the same meal volume, distension was greater in patients than in healthy subjects: at the highest tolerated volume, distension in patients was 6.4±6.1 mm vs 2.4±2.3 mm at an equivalent meal volume (600 ml) in healthy subjects (p=0.045). Interestingly, even relatively small meal volumes elicited significant girth increments, which were larger in patients than in healthy subjects: 210 ml (common maximum tolerated) induced a girth increment of 1.7±2.1 mm in patients (p=0.016 vs basal) vs 0.7±0.8 mm in healthy subjects (p=0.010 vs basal; p=0.153 vs patients).

    Figure 2
    Figure 2

    Abdominal distension in response to test meal. In each subject girth increment at 25%, 50%, 75% and 100% of the maximum tolerated volume was measured; data are mean±SD in patients and healthy subjects. Meal ingestion induced a consistent increment in girth, which was significantly larger in patients than in healthy subjects (p<0.045).

    At baseline, EMG activity in the upright position was similar in patients and healthy subjects in all abdominal wall muscles except the internal oblique, which showed lower activity in patients (table 1). In healthy subjects, meal ingestion induced significant changes in muscular activity of the abdominal walls: progressive relaxation of the diaphragm coupled with contraction of the muscles in the upper anterior abdominal wall (upper rectus and external oblique) and no change in the lower abdominal muscles (lower rectus and internal oblique; figure 3). In contrast to healthy subjects, patients developed a paradoxical response, with contraction of the diaphragm and relaxation of the upper anterior wall (figure 3). No significant changes in the lower abdominal wall (lower rectus and internal oblique) were detected in either group (p=0.486 vs basal in patients, p=0.223 in healthy subjects). The changes in EMG activity occurred progressively during the ingestion period.

    Figure 3
    Figure 3

    Abdominal wall responses to test meal. Note that in healthy subjects diaphragmatic relaxation was associated with upper anterior wall contraction (upper rectum and external oblique), and paradoxical response in patients, that is, diaphragmatic contraction and upper anterior wall relaxation; no significant changes in the lower anterior wall (lower rectus and internal oblique) were detected. In each subject measurements at the end of ingestion and 5 min before were averaged. Data are mean ± SD. *p < 0.01 versus basal; #p < 0.001 versus healthy subjects.

    View this table:
    Table 1

    Basal activity of the diaphragm and anterior abdominal muscles

    At a volume equivalent to the mean volume tolerated by patients (600 ml), healthy subjects exhibited 9±4% diaphragmatic relaxation and 15±7% upper abdominal wall contraction (pooled data for upper rectus and external oblique; p<0.001 vs patients at mean volume tolerated for both). At the maximum meal volume tolerated by all subjects (210 ml), differences between patients and healthy subjects were already detected: 7±7% diaphragmatic contraction versus 4±2% relaxation, respectively (p<0.001) and 3±4% upper anterior muscle relaxation versus 8±7% contraction, respectively (p<0.001).

    Discussion

    This study suggests that postprandial bloating in patients with functional dyspepsia has a dual mechanism. The uncomfortable bloating feeling that patients experience may reflect poor tolerance of the stomach to the meal. However, our results showed the objective concomitant distension to be due to abnormal accommodation of the muscular walls of the abdomen to the intragastric load.

    As previously reported, patients with dyspepsia perceived and tolerated smaller meal volumes than healthy subjects.22 ,23 Perception of intragastric content depends on stimulation of tension receptors in the gastric wall.20 Using different paradigms of gastric distension, it has been consistently shown that distending levels, unperceived or well tolerated by healthy subjects, induce symptoms and even discomfort in patients.7 ,19 ,24–27 The difference between patients and healthy subjects is more pronounced in the postprandial period because the presence of nutrients increases visceral sensitivity in healthy subjects,28–31 but this effect is exaggerated in patients with dyspepsia.19 ,32

    Gastric hypersensitivity is not the sole mechanism of postprandial symptoms in dyspepsia. During fasting, the stomach normally exerts a tonic contraction due to sustained vagal cholinergic input,33 and ingestion of a meal normally produces metered gastric relaxation to accommodate the volume load without a further increase in wall tension.28 ,34 ,35 In patients with functional dyspepsia, gastric capacity and compliance during fasting are similar to those in healthy subjects.19 ,24 ,25 However, these patients show a defective relaxatory response to ingestion of a meal that increases gastric wall tension. This increase in gastric wall tension induces a bloating sensation, which is further augmented by concomitant gastric hypersensitivity.7 ,19 Hence, poor meal tolerance and postprandial symptoms characteristic of the dyspeptic postprandial distress syndrome are related to a combined and synergistic dysfunction involving impaired accommodation of the stomach and increased conscious perception of gastric wall tension.

    In this study meal ingestion produced a minimal girth increment in healthy subjects owing to the efficacy of the normal abdominal accommodation mechanism that activated diaphragmatic relaxation, providing extra space in the upper abdominal cavity, and a compensatory contraction of the anterior wall muscles preventing distension in the upright position. By contrast, patients with dyspepsia experienced a significantly larger increment in girth owing to aberrant abdominal accommodation, featuring paradoxical contraction of the diaphragm and relaxation of the anterior wall.

    Abdominal wall responses to the intragastric volume load in dyspepsia bear a remarkable analogy to those observed in patients with functional or IBS-related bloating in response to colonic gas infusion.1 ,8 On the one hand, patients with IBS and bloating had reduced tolerance to colonic gas infusion and reported significantly more severe symptoms than healthy subjects; this is conceivably related to intestinal hypersensitivity with increased perception of mechanical stimuli characteristic of these patients.36–40 On the other hand, colonic gas infusion induced exaggerated abdominal distension in patients with IBS-related bloating due to distorted abdominal accommodation. The contraction of the diaphragm induced by meal loads in dyspepsia was comparable to that observed in IBS during colonic gas infusion. Furthermore, abdominal CT imaging showed that real-life episodes of abdominal distension in IBS are associated with diaphragmatic descent.41 However, the response of the anterior wall in dyspepsia and IBS was site specific. Patients with dyspepsia reacted to meal ingestion with relaxation of the upper anterior wall, that is, the upper rectus and external oblique, as opposed to contraction in healthy subjects. No changes in the lower muscles, that is, the lower rectus and internal oblique, were observed either in patients with dyspepsia or in healthy subjects. By contrast the internal oblique was relaxed in response to colonic gas in patients with IBS.

    The degree of experimentally induced abdominal distension by the test meal in patients with dyspepsia and by the colonic gas load in patients with IBS was similar but relatively small compared with real-life episodes of abdominal distension recorded by an ambulatory technique in patients with IBS,42–44 possibly because other precipitating/triggering factors, such as stress or fatigue, contribute to the final effect. The degree of abdominal distension associated with postprandial bloating in real life has not been objectively documented.

    Normal gastric accommodation is accomplished by a network of interacting reflexes released by mechanical and chemical stimuli, predominantly nutrient specific, in the stomach and intestine. Failure of such normal control mechanisms in patients with functional dyspepsia may explain the pathophysiology of the postprandial bloating sensation.6 ,7 ,19 ,39 Our data expand on previous observations by showing that patients with dyspepsia and postprandial bloating have impaired gastric responses and distorted abdominal accommodation. Physiological, abdominal accommodation is conceivably regulated by reflex mechanisms arising from the gut or from the abdominal wall itself.45 The cause of the aberrant response in patients with dyspepsia is not clear. It could be related to an impaired reflex or to a behavioural response triggered by perception of gastric sensation. The latter explanation seems plausible considering that in patients with IBS, disturbed abdominal accommodation, that is, the paradoxical activity of the diaphragm and anterior wall, can be corrected by EMG-based biofeedback techniques.46

    Acknowledgments

    The authors thank Professor R Merletti and Dr A Bottin for help in setting up the electromyography system; Maite Casaus, Purificación Rodriguez and Anna Aparici for technical support; Christine O'Hara for English editing of the manuscript; and Gloria Santaliestra for secretarial assistance.

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    Footnotes

    • Contributors EmB: study management, conduction of experiments, and data analysis; JWH: conduction of experiments; ElB: conduction of experiments and data analysis; DC: conduction of experiments; AA: supervision of studies; AS: adaptation of the EMG system; J-RM: study design, data interpretation, and manuscript revision; and FA: study design, data interpretation, and manuscript preparation.

    • Funding Supported in part by the Spanish Ministry of Education (Dirección General de Investigación, SAF 2009-07416), and European Community (project OASIS, QLRT-2001-00218); Ciberehd is funded by the Instituto de Salud Carlos III. EmB was supported by grants from the Freiwillige Akademische Gesellschaft (Basel, Switzerland) and the Gottfried und Julia Bangerter-Rhyner-Stiftung (Bern, Switzerland). DC was supported by grants from Comisión Nacional de Investigación Científica y Tecnológica-Gobierno de Chile and from Pontificia Universidad Católica de Chile.

    • Competing interests None.

    • Patient consent Obtained.

    • Provenance and peer review Not commissioned; externally peer reviewed.