SEARCH

SEARCH BY CITATION

Keywords:

  • exercise;
  • non-invasive;
  • oesophagus;
  • small intestine;
  • stomach

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. References

Exercise decreases splanchnic bloodflow. Therefore exercise may induce alterations in gastrointestinal (GI) function. In the present study we investigated the effect of high-intensity exercise on oesophageal motility, gastro-oesophageal reflux, gastric pH, gastric emptying, orocaecal transit time (OCTT), intestinal permeability and glucose absorption simultaneously, using an ambulatory protocol.

Ten healthy well-trained male subjects underwent a rest–cycling–rest, and a rest–rest–rest protocol (60–90–210 min). Oesophageal motility, gastro-oesophageal reflux and intragastric pH was measured using a trans-nasal catheter. OCTT was measured via breath H2 measurement. A sugar absorption test was applied to determine intestinal permeability and glucose absorption. Gastric emptying was measured using the 13C-acetate breath test.

Peristaltic velocity was increased during cycling, compared to rest (4.92 (2.86) vs. 4.03 (1.48) cm s–1, P = 0.015). Peristaltic contraction pressure at the mid-oesophagus and the duration of the peristaltic contractions at the mid- and distal oesophagus was lower during cycling. There were no differences between the pre-exercise, the exercise and the post-exercise episodes for gastric pH or for both the number and duration of reflux episodes, in both the rest and cycling trials. Neither gastric emptying nor OCTT showed differences between rest and cycling. The lactulose/rhamnose ratio and intestinal glucose absorption were significantly decreased in the cycling trial.

Our model enables multiple GI-measurements during exercise. Cycling at 70% Wmax does not lead to differences in reflux, gastric pH or gastrointestinal transit in healthy trained individuals. The distal oesophageal pressure decreases and peristaltic velocity increases. The lactulose/rhamnose ratio and jejunal glucose absorption are decreased during exercise.


INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. References

Strenuous exercise is able to alter parameters of gastrointestinal function. A number of studies have reported an increase of gastro-oesophageal reflux during exercise.1[2][3]–4

The effect of exercise on oesophageal motility has been studied by Soffer et al.2, 3 They reported an intensity-dependent decline in duration, amplitude and number of oesophageal contractions, which reached significance at near-maximal exercise intensities.

The effect of exercise on gastric pH is as yet unknown. Feldman et al.5 studied the effect of exercise on postprandial gastric secretion, and reported little effect on postprandial gastric secretory function. Zach et al.6 found that in healthy subjects a one-hour exercise period at a constant load of 50% VO2max (maximal oxygen uptake) significantly decreased the volume of gastric juice and the concentration of hydrochloric acid, leading to a higher pH and decreased basal acid output (BAO).

Gastric emptying may also be altered as a result of physical exercise, but is also dependent upon factors such as composition and volume of the meal. During exercise, predominantly liquids are consumed. From studies performed at rest and during exercise it appears that up to exercise intensity levels of 70–80% VO2max, there is no difference between both conditions in the regulation of gastric emptying. At higher intensities, which cannot be maintained for very long periods, the gastric emptying rate (GER) has been found to be retarded. In relation to exercise, the GER of liquids mainly depends on: exercise intensity, volume of the drink, and energy density of the drink.7

There is no consensus about the effect of exercise on the orocaecal transit time (OCTT). This is the time which elapses between oral ingestion and the arrival of the non-absorbed fraction of the meal in the proximal colon.8 Intense exercise reduces intestinal blood flow9 and leads to elevated plasma concentrations of catecholamines, endorphins,10 and all types of GI-hormones,11 each of which may affect intestinal motility. However, the few reports concerning the effect of exercise on intestinal transit time show conflicting results.12[13][14]–15

There are few data available concerning the effect of exercise on intestinal permeability. Øktedalen et al.16 and Moses et al.17 reported an increased permeability after running. In contrast, Ryan et al.18 evaluated the effect of running and aspirin intake on intestinal permeability, and observed no change in permeability in relation to exercise.

It has been suggested that a reduction of mesenteric blood flow by more than 50% causes a linear fall in the rate of glucose absorption.19 In contrast, Fordtran et al.20 reported that severe exercise did not influence the intestinal glucose uptake, as measured with a triple lumen perfusion technique.

All the studies which have been published so far, concerning the effect of physical exercise on gastrointestinal function, focus on one or two parameters of GI-function. Therefore the aim of the present study was to investigate the effect of high-intensity exercise on oesophageal motility, GI-reflux, gastric acid, gastric emptying, orocaecal transit time, intestinal permeability and intestinal glucose absorption simultaneously, using a maximally non-invasive rest-exercise-rest protocol in a controlled laboratory setting.

METHODS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. References

Subjects

10 healthy well-trained male subjects (age 18–21 years), who have not suffered from exercise-induced GI-symptoms, were studied on three different days. Their diet was standardized during the 24 hours preceding the test days. The subjects were not allowed to consume fibre-rich or spicy food products, alcohol, caffeine-containing products, drugs, or to perform physical exercise the day preceding the test days.

Design of the study

Firstly the subjects underwent a stationary slow pull-through manometry in order to locate the lower oesophageal sphincter (LES) and to exclude gross manometric abnormalities. Subsequently the subjects underwent a cycling test21 in order to determine their Wmax (maximal power output). On the two actual testing days the subjects underwent in random order either a rest-cycling-rest protocol, or a protocol in which the cycling period was replaced by rest.

Investigation protocol

A scheme of the investigation protocol is provided in Fig. 1. After an overnight fast, the subjects arrived at the laboratory at 08.00. A thin catheter allowing the registration of oesophageal motility, gastro-oesophageal reflux and intragastric pH (Konigsberg, Pasadena, CA, USA) was inserted transnasally.

image

Figure 1.  An overview of the investigation protocol.

Download figure to PowerPoint

Subsequently the subjects received a standard liquid breakfast (4 mL kg–1 bodyweight, pH=5.8), and remained seated in a chair for 60 min. During this period resting values for oesophageal motility, gastric pH and gastro-oesophageal reflux were obtained. Subsequently the subjects emptied their bladders, mounted a stationary bicycle ergometer (Lode, Groningen, The Netherlands) in the cycling trial, or remained seated in the resting trial. In the cycling trial a warming-up was performed for 10 min at 100 W. During the final minute of this warming-up a carbohydrate-electrolyte solution (CES) (2mL kg–1 body weight), was ingested. The composition of the CES and the used liquid meal is displayed in Table 1.

Table 1.   Composition of the carbohydrate-electrolyte solution and the liquid meal. Thumbnail image of

At t=0 of the subsequent exercise period, the cycling intensity was increased to a load of 70% of the previously determined individual maximal power output (Wmax 70%, which is equivalent to> 80% VO2max), which was maintained for 90 min. If the subjects were not able to maintain the cycling load, it was lowered by 5%. If necessary, this was repeated, until the subject had completed the 90 min cycling period. During this period, the subject received CES (2 mL kg–1 body weight) at t=20, and CES (5 mL kg–1 body weight) at t=40, in order to compensate for sweat losses and to minimize dehydration. All drinks were at room temperature (19 °C). At time=90 min the subject dismounted the cycle ergometer after which they remained normally seated in a comfortable chair for 210 min to obtain post-exercise resting values. At t=150 the subjects received a standard liquid lunch (4 mL kg–1 body weight). For each breath sample the subjects breathed for 2 min through a mouthpiece, which was connected to a mixing chamber. Breath samples for 13CO2 and H2 analysis were collected from the mixing chamber at 5-min and 15-min intervals, respectively. From t=0 to t=300 the total urine production was collected.

Testing procedures

Oesophageal parameters

Two solid-state pressure sensors measured oesophageal pressure at 13 cm (P1) and 3 cm (P3) above the LES, respectively. The catheter was connected to an ambulatory data-recorder (MMS, Enschede, The Netherlands), thus allowing continuous registration of pH and pressure. The stored data were transferred from the ambulatory data-logger to a personal computer system, and edited using specialized manometry software (MMS, Enschede, The Netherlands).

In each episode of the trials the following parameters were evaluated: the number of peristaltic contractions, the mean peristaltic pressure at P1 and P3, the mean duration of peristaltic pressure events at P1 and P3, and the peristaltic velocity.

Gastro-oesophageal reflux

A reflux episode was defined as a period in which the pH in the oesophagus, at 5 cm above the LES, was lower than 4. The following parameters were determined:

1 The number of reflux episodes

2 The duration of the reflux episodes as a percentage of time.

3 Gastric pH – The intraluminal pH was measured 5 cm above the LES, and in the fundus of the stomach at 10 cm below the LES, simultaneously.

The following parameters were determined during each episode of the experiments: (1) Median pH in the fundus, which was determined during the pre-exercise episode, the exercise episode, and the post-exercise episode. No corrections were made for pH-changes due to the ingested drinks and liquid meals as they were similar in the cycling and rest protocol. (2) Percentage of time in which the pH in the fundus was lower than 4.

Gastric emptying

The assessment and mathematical evaluation of 13C-enrichment was carried out as follows: The drink administered at t=40 during the exercise episode contained 150 mg sodium [1–13C]-acetate (99%; Cambridge Isotope Laboratories, Andover, MA, USA) in order to determine the gastric emptying rate using the 13C-acetate breath test. Breath samples for 13CO2-enrichment analysis were drawn from the mixing chamber at five-minute intervals from t=40 to t=90, using Vacutainer tubes. One breath sample was taken before administration of the drink at t < 40, in order to determine background enrichment. The collected breath samples were analysed for 13C isotopic enrichment of the expired CO2 using Isotope Ratio Mass Spectrometry (Finnigan MAT 252, USA). The 13C-enrichment of CO2 was expressed as the delta (δ) per millilitre difference between the 13C/12C-ratio of the breath sample and a known laboratory reference standard according to the formula:

inline image

The δ-value was then related to an international standard, Pee Dee Belemnite (PDB).

The data from the breath enrichment were fitted by non-linear regression analysis according to a dual exponential function with the following features:

inline image

A dual compartment description of 13CO2-production (atb and ftg) is applied because acetate is oxidized both in the splanchnic area and in the working muscles. The decrease in 13CO2 enrichment is also described in two factors; the first factor (ce(–td)) describes washout of 13CO2 through the body bicarbonate pool via the breath, and the second factor (he(–ti)) describes other processes of 13CO2 removal; sequestration of 13CO2 in bone, excretion via urine and incorporation into glucose.26 In this equation a, b, c, d, f, g, h and i are constants, t is the time and j is the background enrichment.

In the present study the results are based on the time to peak 13C-enrichment in the breath samples (13C-TTP) derived from the dual exponential function. The 13C-TTP was considered as the parameter of gastric emptying.22 A correction factor of 5.9 min was added to the 13C-TTP derived from the exercise experiments. This was done to correct for the increased rate of oxidation of the [13C]-acetate, and exhalation of the 13CO2 during exercise conditions.23

OCTT

The drink administered at t=0 of the exercise episode contained a nondigestible soluble carbohydrate (5 g lactulose, Centrafarm syrup, 670 mg mL–1, Etten-Leur, The Netherlands) allowing the measurement of OCTT via H2 measurement in breath. As soon as the lactulose enters the colon, bacterial fermentation will take place, and H2 gas will be produced.24 Breath samples for H2 analysis were collected from the mixing chamber at 15 min intervals, starting at t=0, using a 140 mL syringe, and were analysed for H2 enrichment using a sensitive electrochemical exhaled hydrogen monitor (GMI Medical Ltd, Renfrew, UK). The OCTT was determined using the time of onset of a sustained increase in breath H2, which is the first breath sample that shows a higher breath H2 than the preceding one, followed by two or more breath samples that show a further increase.

Intestinal permeability and glucose absorption

The drink administered at t=0 of the exercise episode contained 5 g lactulose (Centrafarm syrup, 670 mg mL–1, Etten-Leur, The Netherlands), 0.5 g rhamnose and 0.35 g 3-O- D-methyl M-glucose (3-OMG) (Sigma Chemical Co., St. Louis, MO, USA), allowing the measurement of intestinal permeability and intestinal glucose absorption.25 At the end of the experiment, at t=300, total urine was collected, its volume was determined, and a small portion was stored at –80 °C for lactulose, rhamnose and 3-OMG determination. The urinary lactulose, rhamnose and 3-OMG-excretion was determined by a validated, sensitive, newly developed fluorescent detection HPLC system.25 Subsequently the lactulose and rhamnose recoveries, and the lactulose/rhamnose and 3-OMG/rhamnose ratios were calculated.

Statistics

Differences between the respective episodes of the two trials were analysed using Wilcoxon’s non-parametric tests. Data are presented as median (range). The level of confidence was set at P < 0.05. All statistical analyses were performed using SPSS 7.5 for Windows statistical package.

RESULTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. References

All the subjects were able to complete the 90-min cycling episode. It was, however, frequently necessary to decrease the cycling load in 5% steps. The progress of the relative median cycling loads was: at t=0: 70% Wmax (70–70), at t=30: 65% Wmax (65–70), at t=60: 60% Wmax (60–65) and at t=90: 60% Wmax (55–65) The median initial load (70% Wmax) was 243.5 (217–350) W, and the median load at the end of the 90-min cycling period was 215.5 (185-325) W. Bodyweight in the rest experiment decreased 0.3 kg. It was 71.3 (56.4–89.1) kg at the start, and 71.0 (55.8–88.7) kg at the end of the testing day. The bodyweight in the exercise experiment decreased 0.8 kg, from 72.3 (55.7–88.7) kg at the start to 71.5 (54.5–87.8) kg at the end of the testing day.

Oesophageal motility

The data from the oesophageal motility measurements are displayed in Table 2. The peristaltic velocity appeared to be increased during cycling, compared to rest. The number of peristaltic contractions, the peristaltic pressure at P1 and the duration of the peristaltic contractions at P1 and P3 were lower during cycling.

Table 2.   Result of the manometric measurements in median (range) of the oesophagus during the exercise and post-exercise episodes of the rest and the cycling trial (= 10) Thumbnail image of

Gastric pH

The results of the gastric pH measurements are displayed in Table 3. There were no significant differences between the pre-exercise, the exercise and the post-exercise episodes in both median gastric pH (P=0.767, 0.208 and 0.933, respectively), and the percentage of time in which the gastric pH was lower than 4 (P= 0.314, 0.889 and 0.612, respectively).

Table 3.   Results of the gastric pH measurements in median (range) in the pre-exercise, exercise and post-exercise episodes of the rest and the cycling trial (= 10) Thumbnail image of

Gastro-oesophageal reflux

The results of the gastro-oesophageal reflux measurements are displayed in Fig. 2. There were no significant differences between the pre-exercise, the exercise and the post-exercise episodes in both the number of reflux episodes (P= 0.129, 0.610 and 0.786, respectively) and the duration of reflux as a percentage of time (P=0.237, 0.612, and 0.463, respectively).

image

Figure 2.  Number and duration of gastro-oesophageal reflux episodes (median, upper range) in both the rest and the cycling trial, during the pre-exercise, exercise and post-exercise episodes, respectively. No significant differences could be observed (n=10).

Download figure to PowerPoint

Gastric emptying and OCTT

Neither gastric emptying nor the OCTT show differences between the rest and the cycling trials. 13C-TTP in the rest trial was 29.3 min (17.4–42.2) and in the cycling trial it was 28.7 min (21.6–34.2) (P= 0.33). OCTT in the rest trial was 117.5 min (105.0–165.0), and in the cycling trial it was 140.0 min (105.0–195.0) (P= 0.17).

Intestinal permeability and glucose absorption

The results of the intestinal permeability and the 3-OMG absorption measurements are displayed in Fig. 3. The lactulose/rhamnose ratio was significantly higher in the rest trial, compared to the cycling trial (0.015 (0.0076–0.027) and 0.0067 (0.0017–0.0141), respectively, P=0.009). The changes in individual values between rest and cycling are displayed in Fig. 4. Nine out of 10 subjects showed a decrease in the lactulose/rhamnose ratio in the cycling trial, compared to the rest trial. The 3-OMG/rhamnose ratio was also significantly higher in the rest trial compared to the cycling trial (3.51 (2.63–4.77) and 2.64 (2.03–3.91), respectively, P= 0.007).

image

Figure 3.  The lactulose/rhamnose (n=10, P=0.009) and the 3-OMG/rhamnose ratio in the rest and in the cycling trial (n=10, P=0.007).

Download figure to PowerPoint

image

Figure 4.  The individual change in the lactulose/rhamnose ratio as a result of cycling.

Download figure to PowerPoint

The urinary recoveries of 3-OMG, rhamnose and lactulose are displayed in Fig. 5. Lactulose and 3-OMG recoveries were significantly lower in the cycling trial, compared to the rest trial. Rhamnose recovery showed no difference between the trials (lactulose: cycling: 0.09% (0.038%–0.173%), rest: 0.22% (0.078%–0.394%), P=0.009, rhamnose: cycling: 15.0% (8.54%–23.99%), rest: 14.0% (9.64%–22.37%), P=0.65, respectively, 3-OMG: cycling: 35.15% (21.06%–62.12%), rest: 46.67% (38.35%–58.83%), P=0.028).

image

Figure 5.  Urinary recoveries of 3-OMG, rhamnose and lactulose in the rest and the cycling trials (n=10, P=0028 (*), P=0.65, and P=0.009 (*), respectively).

Download figure to PowerPoint

DISCUSSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. References

Our study demonstrates that physical exercise has an effect on oesophageal function. Oesophageal function was measured at 3 cm (P3) and 13 cm (P1) above the LES. At 3 cm above the LES the oesophagus is entirely composed of smooth muscle tissue. At 13 cm above the LES, however, the oesophagus also contains striated muscle tissue. It is known that the peristaltic velocity wave is slower in striated muscle (3 cm sec–1) than in smooth muscle (5 cm sec–1), and that the amplitude of the peristaltic waves in the lower part of the oesophagus are higher than in the upper part, and the duration of smooth muscle waves are longer than in striated muscle.26 The difference in control and innervation and the difference in motility characteristics of striated and smooth oesophageal muscle might explain some of the observed differences between rest and cycling. Exercise leads to an increase in sympathetic, and a decrease in parasympathetic activity. This may lead to a decreased vagal stimulation which is restricted to the striated muscle component of the muscle tissue in the both the P1 region (mixed striated and smooth muscle tissue) of the oesophagus, thus explaining the decreased pressure at P1 of the peristaltic waves during exercise. It may also explain why the pressure at P3 is not changed during exercise, since this region is entirely composed of smooth muscle. Nitric oxide synthase inhibition leads to decreased swallow-induced contraction amplitude in the distal oesophagus, and also diminishes swallow-induced contraction latencies, predominantly in the distal oesophagus, thereby decreasing the latency gradient and increasing the peristaltic velocity.27 We observed a similar pattern during exercise, which might be explained by an exercise-induced increased activity of the enteral nerve system (ENS), due to a decreased ENS inhibition via nitric oxide.

Exercise may lead to a substantial decrease in GI blood flow of more than 50%.28, 29 Rowell et al.30 demonstrated a 60–70% reduction in splanchnic blood flow in subjects exercising at an intensity of 70% VO2max, and Clausen9 reported a reduction in splanchnic blood flow of 80% of the resting level during maximal exercise. Therefore exercise may induce alterations in GI-function. This might be a factor in the pathophysiology of exercise-induced GI-symptoms. These symptoms point to changes concerning both the upper and the lower GI-tract. Training status, exercise intensity, hydration state and nutrition seem to play an important role. GI-symptoms during strenuous physical activity occur more frequently in untrained people compared to trained people, and more in females than in males. In ‘gliding’ sports like cycling, skating and swimming the prevalence of GI-symptoms is lower compared to running.8

The results of the present study indicate that there are no differences in gastro-oesophageal reflux, gastrointestinal transit time or gastric pH between a resting and a cycling trial. This is the case during both the exercise episode, and the post-exercise episode.

It has been hypothesized that intense exercise may provoke gastro-oesophageal reflux. Earlier studies in our department, however, showed that exercise at 70% Wmax on a stationary bicycle does not itself increase either the number of gastro-oesophageal reflux episodes or the percentage of time of reflux, if the experiments are conducted in a well-controlled laboratory setting.31 These observations are confirmed by the results of the present study. This, however, does not rule out the possibility that reflux may occur more often at near-maximal exercise intensities, or during different types of exercise, such as running. In this respect, Soffer et al.2, 3 demonstrated that a significant increase in reflux occurred only at the highest intensity (90% VO2max for 10 min) in a graded cycling exercise protocol, and Kraus et al.1 demonstrated an increase in reflux in runners. Peters et al.32 studied the LES pressure in healthy volunteers before and immediately after 30 min of cycling at an increasing intensity. They observed a decreased LES pressure during severe exercise. Schoeman et al.33 studied reflux and LES pressure in ambulatory subjects who performed a standardized exercise program consisting of three 10-min periods of exercise. They observed an increase in gastro-oesophageal reflux during exercise and a decrease in basal LES pressure during exercise, which was however, unrelated to the occurrence of reflux. The majority of the reflux episodes were associated with transient LES relaxations (TLESR). The number of TLESRs was not increased during exercise.

Reflux has also been suggested to be associated with increased gastric acid production. The present study demonstrates that the gastric pH does not change as a result of exercise. However, the possibility that the basal acid output was altered during exercise cannot be excluded.

During an exercise/rest investigation, significant differences were observed between the percentages of time in which the gastric pH was lower than 4. This can, however, be explained by the pH of the ingested drinks, and by the effect of the ingested pre– and post-exercise liquid meals on the gastric pH.

Our results demonstrated that the gastric emptying rate was not affected by exercise at a cycling load of 70% Wmax, which corresponds with approximately 80% VO2max. This observation is in accordance with other studies, which showed that exercise intensities up to 70–80% VO2max do not affect gastric emptying.7 The relation between the gastric emptying rate, gastric acid production and reflux at high intensity exercise, which may lead to an increase in gastro-oesophageal reflux, should be clarified in the future.

The liquid OCTT was also unchanged in our experiments. This is in accordance with the observations of Soffer et al.,34 who measured the effect of cycling at different intensities on duodeno-jejunal motor activity and OCTT in cyclists. They observed an unchanged OCTT and an increase in intestinal postprandial motor activity (phase III) during exercise at higher intensities. This effect was intensity-dependent and not related to gastrointestinal symptoms. The latter observation was confirmed by Peters et al.,35 who observed an unexpected early reappearance of phase III motor activity during exercise, especially if a carbohydrate liquid was consumed. These results suggest that exercise-induced phase III activity of the small bowel is not related to the OCTT. The possible relationship between an exercise-induced alteration in the gastric emptying rate and the OCTT requires further investigation.

The intestinal permeability can be measured using the lactulose/rhamnose test. This test is based on the comparison of intestinal permeation of lactulose, which follows a paracellular permeation route, with that of rhamnose, which follows a transcellular permeation route, by measuring the ratio of urinary excretion of these molecules.36 An exercise-induced reduction of splanchnic blood flow might be expected to lead to an impairment of intestinal blood supply, resulting in an increased intestinal permeability, reflected by an increased lactulose/rhamnose ratio. In this respect, the observed effect of cycling on the lactulose/rhamnose ratio is surprising, and in contrast to the findings of Pals et al.37 They studied athletes who ran on a treadmill for 1 h at an intensity of 80% VO2max, which is a comparable intensity to our experiments, and observed an increased lactulose/rhamnose ratio, due to increased lactulose absorption. Lower intensities did not result in a change of permeability. They administered the lactulose/rhamnose solution after 30 min of running, which meant that the solution, after emptying from the stomach, was predominantly exposed to the intestinal lumen in the post-exercise period. It cannot, however, be excluded that the difference in results between our experiments and those of Pals et al.,37 may also be explained by the different types of exercise; running vs. cycling. The lactulose/rhamnose permeability test is based on the assumption that both pre- and post-absorptive factors do not influence the outcome of the test, since rhamnose, which is passively absorbed via the transcellular route, serves as a control probe for lactulose, which is absorbed via the paracellular route.36 It can be debated whether these assumptions are valid under exercise conditions, since our results show no difference in rhamnose recoveries between the rest and exercise experiments, but show a significant decrease in lactulose recovery in the exercise experiment. Since pre-absorptive factors such as gastric emptying and OCTT appeared not to be influenced by exercise as indicated by our experiments, the results might suggest a possible impairment in renal lactulose clearance in the exercise experiment, rather than a change in intestinal permeability.

Intestinal glucose uptake is a carrier-mediated transport process. Our results demonstrated a decreased absorptive capacity for glucose uptake in the cycling trial, as reflected by a decreased 3-OMG/rhamnose ratio. This decrease in absorptive capacity may be explained by the decreased splanchnic blood flow, leading to a lower activity of the jejunal Na+/K+-ATPase, necessary for glucose absorption.

In summary, it can be concluded that cycling at 70% Wmax does not lead to differences in gastro-oesophageal reflux, gastric pH or gastrointestinal transit in healthy trained individuals in a controlled experimental setting. However, oesophageal motility is affected by cycling. The distal oesophageal pressure is decreased and the peristaltic velocity is increased. The lactulose/rhamnose ratio is decreased, due to decreased lactulose absorption. Jejunal glucose absorption is also decreased during cycling. The pathophysiological mechanisms of the exercise-induced changes in gastrointestinal parameters are hypothetical, and require further investigation.

ACKNOWLEDGMENTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. References

This study was supported with grants from Novartis Nutrition Ltd, and the Dutch Olympic Committee.

References

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. References
  • 1
    Kraus BB, Sinclair JW, Castell DO. Gastroesophageal reflux in runners: characteristics and treatment. Ann Int Med 1990; 112: 429 33.
  • 2
    Soffer EE, Merchant RK, Duethman G, Launspach J, Gisolfi C, Adrian TE. Effect of graded exercise on esophageal motility and gastroesophageal reflux in trained athletes. Dig Dis Sci 1993; 38(2): 220 4.
  • 3
    Soffer EE, Wilson J, Duethman G, Launspach J, Adrian TE. Effect of graded exercise on esophageal motility and gastroesophageal reflux in nontrained subjects. Dig Dis Sci 1994; 39(1): 193 8.
  • 4
    Clark CS, Kraus BB, Sinclair J, Castell, DO. Gastroesophageal reflux induced by exercise in healthy volunteers. J Am Med Ass 1989; 261: 3599 601.
  • 5
    Feldman M & Nixon JV. Effect of exercise on postprandial gastric secretion and emptying in humans. J Appl Physiol 1982; 53(4): 851 4.
  • 6
    Zach E, Markiewicz K, Lukin M, Cholewa M. The behaviour of basal gastric secretion during exercise and restitution in chronic gastric and duodenal ulcer patients. Dtsch Z Fur Verdauungs-Stoffwechselkr 1982; 42(2–3): 53 63.
  • 7
    Brouns F. Gastric emptying as a regulatory factor in fluid uptake. Int J Sports Med 1998; 19 (Suppl. 2): S125 8.
  • 8
    Brouns F & Beckers EJ. Is the gut an athletic organ? Digestion, absorption and exercise. Sports Med 1993; 15(4): 242 57.
  • 9
    Clausen JP. Effect of physical training on cardiovascular adjustments to exercise in man. Physiol Rev 1977; 57: 779 815.
  • 10
    McMurray RG, Forsythe WA, Mar MH, Hardy CJ. Exercise intensity-related responses of beta-endorphin and catecholamines. Med Sci Sports Exerc 1987; 19(6): 570 4.
  • 11
    O’Connor AM, Johnston CF, Buchanan KD, Boreham C, Trinick TR, Riddoch CJ. Circulating gastrointestinal hormone changes in marathon running. Int J Sports Med 1995; 16(5): 283 7.
  • 12
    Cammack JN, Read W, Cann A et al. Effect of prolonged exercise on the passage of a solid meal through the stomach and the small intestine. Gut 1982; 23: 957 62.
  • 13
    Keeling WF & Martin BJ. Gastrointestinal transit during mild exercise. J Appl Physiol 1987; 63(3): 978 81.
  • 14
    Keeling WF, Harris A, Martin BJ. Orocecal transit during mild exercise in women. J Appl Physiol 1990; 68(4): 1350 3.
  • 15
    Meshkinpour H, Kemp C, Fairshter R. Effect of aerobic exercise on mouth-to-cecum transit time. Gastroenterology 1989; 96: 938 41.
  • 16
    Øktedalen O, Lunde OC, Opstad PK, Aabakken L, Kvernebo K. Changes in the gastrointestinal mucosa after long-distance running. Scand J Gastroenterol 1992; 27: 270 4.
  • 17
    Moses F, Singh A, Smoak B et al. Alterations in intestinal permeability during prolonged high-intensity running. Gastroenterology 1991; 100: A472A472.
  • 18
    Ryan AJ, Chang R-T, Gisolfi CV. Gastrointestinal permeability following aspirin intake and prolonged running. Med Sci Sports Exerc 1996; 28(6): 698 705.
  • 19
    Winne D. Models of the relationship between drug absorption and the intestinal blood flow. In: Shepherd AP, Granger DN, eds. Physiology of Intestinal Circulation. New York, NY: Raven Press 1984: 289.
  • 20
    Fordtran JS & Saltin B. Gastric emptying and intestinal absorption during prolonged severe exercise. J Appl Physiol 1967; 23(3): 331 5.
  • 21
    Kuipers H, Verstappen FTJ, Keizer HA, Geurten P, Van Kranenburg G. Variability of aerobic performance in the laboratory and its physiologic correlates. Int J Sports Med 1985; 6: 197 201.
  • 22
    Van Nieuwenhoven MA, Wagenmakers AJM, Senden JMG, Brouns F, Brummer R-JM. The assessment of gastric emptying of liquids during exercise using a [13C]-acetate breath test . Eur J Physiol 1997; 434: R39 R46, A12A12.
  • 23
    Van Nieuwenhoven MA, Wagenmakers AJM, Brouns F, Brummer R-JM. Effect of mode of administration of [13C]-acetate on [13C]-appearance in breath: implications for the gastric emptying breath test . Gastroenterology 1997; 112(4): A843A843.
  • 24
    Levitt MD. Production and excretion of hydrogen gas in man. N Engl J Med 1969; 281(3): 122 7.
  • 25
    Rooyakkers DR, Van Eijk HM, Deutz NEP. Simple and sensitive multi-sugar-probe gut permeability test by high-performance liquid chromatography with fluorescence labelling. J Chromatogr A 1996; 730(1–2): 99 105.
  • 26
    Yamada T. Textbook of Gastroenterology, Vol 1. Philadelphia, USA: J.B. Lippincott Company, 1991: 157–188
  • 27
    Anand N & Paterson WG. Role of nitric oxide in esophageal peristalsis. Am J Physiol 1994; 266: G123 31.
  • 28
    Konturek S, Falser J, Obtulowicz W. Effect of exercise on gastrointestinal secretions. J Appl Physiol 1973; 34: 324 8.
  • 29
    Wade OL, Combes B, Chilos AW et al. The effect of exercise on the splanchnic blood flow and splanchnic blood Volume in normal men. Clin Sci 1956; 15: 457 63.
  • 30
    Rowell LR, Blackmon JR, Bruce RA. Indocyanin green clearance and estimated blood flow during mild to maximal exercise in upright man. J Clin Invest 1964; 43: 1677 90.
  • 31
    Van Nieuwenhoven MA, Brouns F, Brummer R-JM. Ambulatory measurement of esophageal motility, LES pressure and gastroesophageal reflux during exercise. Gastroenterology 1996; 110: A704A704.
  • 32
    Peters O, Peters P, Clarys JP, De Meirleir K, Devis G. Esophageal motility and exercise. Gastroenterology 1988; 94: A351A351.
  • 33
    Schoeman MN, Tippett MD, Akkermans LMA, Dent J, Holloway RH. Mechanisms of gastroesophageal reflux in ambulant healthy human subjects. Gastroenterology 1995; 108: 83 91.
  • 34
    Soffer EE, Summers RW, Gisolfi C. Effect of exercise on intestinal motility and transit time in athletes. Am J Physiol 1991; 260: G698 702.
  • 35
    Peters HPF. Gastrointestinal symptoms and dysfunction during prolonged exercise. Thesis, Utrecht University, 1995.
  • 36
    Bjarnason I, MacPherson A, Hollander D. Intestinal permeability, an overview. Gastroenterology 1995; 108: 1566 81.
  • 37
    Pals KL, Chang R-T, Ryan AJ, Gisolfi CV. Effect of running on intestinal permeability. J Appl Physiol 1997; 82(2): 571 6.