Secondary Logo

Journal Logo

Esophageal Reflux in Conditioned Runners, Cyclists, and Weightlifters

COLLINGS, KIMBERLY L.1; PRATT, PIERCE F.2; RODRIGUEZ-STANLEY, SHEILA1; BEMBEN, MICHAEL3; MINER, PHILIP B.1

Medicine & Science in Sports & Exercise: May 2003 - Volume 35 - Issue 5 - p 730–735
CLINICAL SCIENCES: Clinical Investigations
Free

ABSTRACT COLLINGS, K. L., F. P. PRATT, S. RODRIGUEZ-STANLEY, M. BEMBEN, and P. B. MINER. Esophageal Reflux in Conditioned Runners, Cyclists, and Weightlifters. Med. Sci. Sports Exerc., Vol. 35, No. 5, pp. 730–735, 2003.

Introduction: Gastroesophageal reflux disease is a disorder in which gastric contents move from stomach to esophagus. Exercise is a recognized contributing factor to reflux in healthy volunteers and is reported to be proportional to exercise intensity and the type of exercise. Our aim was to explore changes in physiology occurring in conditioned runners, cyclists, and weightlifters.

Methods: Ten subjects from each sport with >3-month history of exercise-induced heartburn were enrolled. Subjects underwent evaluation of fasting and fed esophageal pH, heart rate, GI symptom, and perceived exertion during standardized exercise routines at 65% (60 min) and 85% (20 min) of their maximal capabilities.

Results: Weightlifters experienced the most heartburn and reflux: 18.51 ± 17.34% time esophageal pH <= 4.0 fasted and 35.81 ± 34.33% time pH <= 4.0 fed. Runners developed mild symptoms and moderate reflux: 4.90 ± 3.96% time pH <= 4.0 (fasted) and 17.16 ± 7.90% time (fed). Cyclists exhibited mild symptoms and reflux: 3.97 ± 5.44% time pH <= 4.0 fasting and 6.49 ± 6.22% time fed.

Conclusion: Our study demonstrates that strenuous exercise induces significant reflux and related symptoms in conditioned athletes.

1Oklahoma Foundation for Digestive Research, University of Oklahoma Health Sciences Center, Oklahoma City, OK;

2PPD Pharmaco, Wilmington, NC; and

3Health and Sport Sciences Department, University of Oklahoma, Norman, OK

Address for correspondence: Philip B. Miner, Jr., M.D., President and Medical Director, Oklahoma Foundation for Digestive Research, 711 Stanton L. Young Blvd., Ste. 619, Oklahoma City, OK 73104; E-mail: kimberly-collings@ouhsc.edu.

Submitted for publication June 2000.

Accepted for publication November 2002.

Gastroesophageal reflux disease (GERD) is a common disorder in which gastric contents move from the stomach into the esophagus. Numerous provocative physiologic events can exacerbate gastroesophageal reflux by increasing gastric acid secretion, impairing gastric emptying, inducing transient lower esophageal sphincter relaxations (tLESr), increasing the pressure gradient between the stomach and esophagus, or decreasing esophageal clearance. Exercise may contribute to GERD in asymptomatic healthy volunteers, inducing reflux proportional to the intensity and type of exercise (4,7,16,21).

The relationship of exercise and GERD is supported by published epidemiological data indicating that upper gastrointestinal symptoms occur in as many as 58% of surveyed athletes, seemingly related to exercise intensity (17,19,20). A number of testable hypotheses could explain exercise-induced gastroesophageal reflux. Changes in body position necessary during competitive cycling and weightlifting regimens decrease the beneficial effects of gravity on esophageal clearance as subjects shift away from an upright position. Increased intra-abdominal pressure induced by the Valsalva maneuver performed by weightlifters or the bent-over racing position maintained by cyclists both can increase the abdominal component of the vectorial force pushing gastric contents up against the lower esophageal sphincter. It is also possible that exertion may lead to modified gastrointestinal motor activity including decrements in esophageal peristaltic activity, lower esophageal sphincter tone, and delayed gastric emptying. These and other physiologic changes could occur secondary to diversion of mesenteric blood flow during exercise.

The aim of our study was to explore the changes in gastrointestinal physiology that occur during exercise in conditioned runners, cyclists, and weightlifters. We sought to 1) quantitate the effects of graded endurance exercise on measurable reflux (% time esophageal pH <= 4 and <= 5); 2) compare the effects of a typical precompetition meal on specific reflux parameters; 3) correlate symptom severity with exercise intensity, duration, and esophageal acid exposure; and 4) determine if reflux and/or symptoms persist after the cessation of athletic activity during a “cool-down” period.

Back to Top | Article Outline

METHODS

Subjects.

Healthy subjects who typically engaged in weightlifting, bicycling, or running at least 4× wk-1 were sought for a five-phase exercise protocol. Subjects selection was directed toward proficiency and fitness within the athletes’ chosen sport as opposed to body type or body mass index matching between sports as the activities chosen shape the physique of the individual. Subjects related a minimum 3-month history of heartburn occurring during exercise at least 2× wk-1. This guideline for minimal heartburn is equivocated with the threshold of justifiable prescriptive medication among the general population.

The Institutional Review Board of the University of Oklahoma and the Western Institutional Review Board approved all aspects of the study, including the protocol and informed consent form. Written informed consent was obtained from each study subject before the performance of any study procedures per good clinical practices and the standard operating procedures of the Oklahoma Foundation for Digestive Research. This study was funded by an unrestricted grant from the Procter and Gamble Company.

Back to Top | Article Outline

Screening and manometry assessment.

Detailed medical history, physical exam, ECG, and screening laboratory studies (blood chemistry and UA) were conducted on eligible subjects. Standard esophageal manometry was performed to document potential motility disorders using a solid state Konigsberg catheter (Konigsberg Instruments, Inc., Pasadena, CA). The distance of the lower esophageal sphincter (LES) from the nares was recorded to assure proper placement of the pH catheter at subsequent visits. Position of the upper esophageal sphincter, LES pressure (LESP), percent relaxation of the lower esophageal sphincter, and peristaltic amplitudes within the distal esophagus were assessed using dry and wet swallows.

Back to Top | Article Outline

Fitness assessment.

A standard treadmill stress test by Bruce protocol for volume of oxygen ([latin capital V with dot above]O2) maximum (3) was performed to verify that each individual could safely attain maximum heart rates expected for running and cycling exercise visits. Weightlifting subjects also underwent Bruce protocol, but as weightlifters, conditioning is centered on muscle mass rather than cardiovascular fitness, Weightlifters’ workloads for subsequent exercise visits were determined by a 1-repetition maximum (1-RM) for each of eight different weightlifting exercises. After each individual lifted what they considered to be their maximum weight on each exercise, 65% and 85% of that 1-RM was calculated to be used for exercise routines done during the next two visits to capture the most similar training scenario to the cardiovascular athletes.

Back to Top | Article Outline

Esophageal pH monitoring.

Subjects were intubated transnasally with a dual electrode pH catheter (15-cm spacing) with an internal reference electrode (Medtronics Synectics). The catheter was positioned with the proximal electrode 5 cm above the upper margin of the manometrically identified LES (esophagus) and the distal electrode 10 cm below the LES (stomach). Continuous electronic recording of the esophageal pH profile was accomplished with a Mk III Digitrapper. Esophageal pH parameters (percent time pH <= 4, percent time pH <= 5) were then processed and calculated with a Medtronics Synectics pH profile program. All data analyses were performed on the numeric output of this software program.

Back to Top | Article Outline

Exercise evaluation.

To determine effects of exercise alone on reflux and heartburn, subjects performed their first exercise session in a fasting state. Fasted subjects underwent a 1-h baseline esophageal pH assessment while at rest in an upright position. During exercise, cyclists rode (in the bent-over racing cycling position) on an indoor stationary bicycle trainer with their own road racing bicycle attached. Runners utilized a motorized treadmill. The regimen consisted of 60 min of exertion at 65% maximal heart rate and 20 min at 85% maximal heart rate. Changes in speed and elevation of treadmill of individual runners and changes in rpm of individual cyclists were used to keep heart rate at the predetermined level. Weightlifters performed a series of weightlifting exercises at 65% of their 1-RM (three sets) and 85% of their 1-RM (one set). Heart rate, level of perceived exertion (1), and heartburn or heartburn-related symptoms were recorded at 5-min intervals for the runners and cyclists, and immediately after each exercise for weightlifters. Due to the intensity of exercise with its risk of dehydration, subjects were allowed up to 6 ounces of water (up to 24 ounces total) at 0, 30, and 60 min after beginning the exercise routine and after the exercise period. Subjects were monitored for 2 h after exercise (“cool-down” period) during which they were required to maintain an upright position. Subjects were then extubated and dismissed.

The fed phase of the study was conducted in the same manner as the fasting session with the addition of a “typical” precompetition nonprovocative breakfast meal [1 cup of Cornflakes, 6 ounces of 2% milk, 14 ounces of Welch’s grape juice, and a banana (560 kcal, 757 mL, pH = 4.2)] (4) 1 h after initiation of baseline, before exercise. All subjects were required to consume the same amount regardless of body size to standardize the volume and pH of intake for consistent reflux stimulus. Subjects were allowed 15 min to eat and began exercise 45 min after the end of the meal. The exercise protocol was repeated as previously outlined.

Back to Top | Article Outline

Statistical analysis.

ANOVA single-factor and two-factor tests were utilized as appropriate to compare changes in percent time esophageal pH <= 4 (acidic reflux) and 5 (gastroesophageal reflux). All values are expressed as the mean plus or minus standard deviation.

Back to Top | Article Outline

RESULTS

Due to the low prevalence of heartburn in distance runners, a cohort of three symptomatic runners was supplemented with seven asymptomatic conditioned distance runners who met all other inclusion/exclusion criteria.

A total of 33 subjects were enrolled. Three subjects were unable to complete all phases of the study, and one subject with previously undiagnosed achlorhydria was excluded from final data analysis post hoc. One subject’s data included only the fasting state; data from the fed state of that subject were excluded due to equipment failure. These exclusions resulted in 29 evaluative fasting pH records and 28 evaluative fed pH records.

Seven of the 10 weightlifters demonstrated nonspecific esophageal motor abnormalities such as those often seen in patients with a history of gastroesophageal reflux. Four of the 10 cyclists displayed various esophageal motility disorders, possibly indicative of less prominent gastroesophageal reflux than the weightlifter population. Similarly, 3 of the 10 runners displayed esophageal motility abnormalities (Table 1). Mean lower esophageal sphincter pressure was within normal limits for all groups evaluated (Table 2).

TABLE 1

TABLE 1

TABLE 2

TABLE 2

Aerobic fitness was measured by performance time associated with the Bruce protocol treadmill test (5,10). In addition, performance on the Bruce protocol substantiated that each aerobic athlete should be capable of enduring sustained exercise (Table 2). The results confirmed the experience and conditioning of all of the athletes with [latin capital V with dot above]O2max of the cyclists’ and runners’ averaging above 55 mL O2·kg-1·min-1—representing results typical in aerobically trained athletes (14). Cyclists and runners both proved to be aerobically fit, with cyclists’ mean estimated [latin capital V with dot above]O2max achieving 66.1 ± 5.9 mL O2·kg-1·min-1, whereas runners’ mean estimated [latin capital V with dot above]O2max was 61.7 ± 12.3 mL O2·kg-1·min-1. Weightlifters’ mean estimated [latin capital V with dot above]O2max was 48.9 ± 10.5—a lower mean value consistent with the fact that much of weightlifters’ principal exercise is anaerobic. Mean 1-RM data from all weightlifters confirmed participants’ ability and proficiency with the selected weightlifting routine (Table 3).

TABLE 3

TABLE 3

All athletes demonstrated normal esophageal acid exposure during the baseline period. Substantial acid reflux was observed during weightlifting compared with running and cycling (Fig. 1). Fasting weightlifters exhibited extremely high levels of acidic gastroesophageal reflux during exercise (18.51% ± 17.34 of the 80-min exercise period), exceeding the levels of exercise-induced reflux in fasting cyclists (P <= 0.03) and runners (P <= 0.04). Cyclists experienced the lowest levels of gastroesophageal reflux of the three groups evaluated. During fasted exercise, cyclists had esophageal acid reflux during 3.97 ± 5.44% of the total exercise time (Fig. 1). Fasted runners also had relatively low acid reflux with 4.90 ± 3.96% of the time pH <= 4.0 (Fig. 1). The precompetitive meal increased esophageal acid exposure during exercise in weightlifters from 18.51 ± 17.34% in the fasted state to 35.18 ± 34.33% in the fed state. Fed cyclists experienced significantly less reflux levels than weightlifters (P <= 0.02) with reflux increasing from 3.97 ± 5.44% (fasting) to 6.49 ± 6.22% (fed). Runners more than tripled their acid reflux with the addition of the precompetitive meal from 4.90 ± 3.96% (fasted) to 17.16 ± 7.90%.

FIGURE 1--Baseline reflux in the fasting and fed state is illustrated as percent time pH ≤ 4.0 □ and as percent time pH ≤ 5.0 ▪. The reflux during the entire exercise period (65% effort plus 85% effort) is shown as percent time pH ≤ 4.0 B and as percent time pH ≤ 5.0 0. Weight-lifters displayed the most reflux of all athletes with all groups’ reflux time increasing in the fed state. Percent time pH ≤ 5.0 increases evaluative reflux proportionally for all groups assessed.

FIGURE 1--Baseline reflux in the fasting and fed state is illustrated as percent time pH ≤ 4.0 □ and as percent time pH ≤ 5.0 ▪. The reflux during the entire exercise period (65% effort plus 85% effort) is shown as percent time pH ≤ 4.0 B and as percent time pH ≤ 5.0 0. Weight-lifters displayed the most reflux of all athletes with all groups’ reflux time increasing in the fed state. Percent time pH ≤ 5.0 increases evaluative reflux proportionally for all groups assessed.

Gastroesophageal reflux (an attempt to quantitate both acidic and nonacidic reflux components), determined by percent of time with esophageal pH <= 5, was also assessed in all athletes (Fig. 1). The amount of gastroesophageal reflux was quite high during exercise in the fasting and fed states for weightlifters (32.52 ± 26.89% and 49.26 ± 37.95%, respectively). Compared with cyclists, weightlifters had significantly more gastroesophageal reflux in both fasting and fed states (P <= 0.04 and P <= 0.01, respectively). Gastroesophageal reflux (percent time pH <= 5.0) increased minimally from 10.44 ± 14.63% in the fasted state to 11.45 ± 8.76% in the fed state for cyclists (Fig. 1). Fasting runners had slightly less gastroesophageal reflux than cyclists did. However, as with acid reflux gastroesophageal reflux in runners was tripled in the fed state from 8.40 ± 5.75% to 26.76 ± 13.08%.

Members of all sporting groups reported at least minimal heartburn in association with exercise. Weightlifters commonly reported moderate symptoms during both fasted and fed workouts. Cyclists reported mild symptoms during exercise, certainly less prominent than symptoms in weightlifters. Although 7 of the 10 runners reported no prior history of exercise-induced heartburn, 6 of the 10 reported at least mild symptoms during the exercise routine.

Weightlifters frequently change body position to work different muscle groups during exercise. Body position (upright vs reclined) and exercise type (upper vs lower body exercises) did not influence subjective symptoms or objective reflux measurements (Fig. 2). Each of the eight different exercises produced equivalent high levels of reflux with no distinguishing characteristics. Body position did not worsen reflux. Fed cyclists with their horizontal body position had significantly less acid reflux (6.49% time pH <= 4.0) as compared with upright runners (17.17%). This trend is also present when examining gastroesophageal reflux.

FIGURE 2--Reflux during the weightlifters’ fasting session □ and fed session ▪ at 65% and 85% effort and in the upright and reclined positions illustrated as percent time pH ≤ 4.0. “Upright” and “reclined” weightlifting exercises elicited equal amounts of reflux. Feeding increased the amount of reflux for both body positions and effort levels.

FIGURE 2--Reflux during the weightlifters’ fasting session □ and fed session ▪ at 65% and 85% effort and in the upright and reclined positions illustrated as percent time pH ≤ 4.0. “Upright” and “reclined” weightlifting exercises elicited equal amounts of reflux. Feeding increased the amount of reflux for both body positions and effort levels.

No statistically significant changes in reflux occurred in any group when increasing effort from 65% to 85% of maximum effort. Runners were the only athletes who experienced a statistically significant drop in reflux when exertion decreased from 85% to the nonexercise “cool-down” period.

Due to protocol restraints, cyclists were the only athletes whose water intake could be evaluated for the effect of sipping fluids during exercise. Although cyclists did not experience any noticeable increase in heartburn symptoms with the ingestion of water, their mean esophageal pH over the 5-min period before sipping compared with the 5-min period after sipping decreased from 6.27 ± 0.54 to 5.80 ± 0.73, whereas their mean gastric pH increased from 1.25 ± 0.30 to 1.55 ± 0.27 (P <= 0.03).

Back to Top | Article Outline

DISCUSSION

Building on the knowledge that upper gastrointestinal symptoms are common in association with exercise, we examined esophageal parameters that could be the basis for understanding the numerous possible pathophysiologic events responsible for these symptoms. We hypothesized that changes in body position and the Valsalva maneuver performed during strenuous exercise would counter beneficial effects of gravity and would thus lead to increased reflux by increasing the upward vectorial force on gastric contents against the protective lower esophageal sphincter. Reflux results when the summation of these vectorial forces on gastric contents exceeds the resistance of the LES. In addition to esophageal physiology, gastric physiology may be altered with strenuous exercise resulting in decreased gastric blood flow, motility, and gastric acid secretion.

We studied three types of athletic pursuits chosen because we anticipated each to result in different physiologic effects on the upper gastrointestinal tract. We expected distance runners to have the least reflux and symptoms because of their upright posture and rhythmic breathing patterns. Weightlifters were expected to manifest high levels of reflux due to the profound increase in intra-abdominal pressure during lifting. Weightlifters also frequently exercise in a horizontal body position, thus eliminating the beneficial effect of gravity on control of reflux. We expected that cyclists would experience an intermediate level of reflux as they exert similar effort to the runners in a stable but bent-over racing position.

As anticipated, weightlifters followed our predicted reflux patterns with the most of all athletes, but unlike our hypothesis suggested, runners were found to demonstrate more reflux than cyclists. The enormous increase in reflux during exercise in the weightlifters supports the theory that changes in intra-abdominal pressure may constitute one of the critical elements in gastroesophageal reflux as opposed to body position alone. Body position was further examined by comparing the reflux of cyclists with runners. The less important role of body position is illustrated by measured reflux in cyclists and runners where exercise level is similar but body position changes. The upright runners have less reflux than the bent-over cyclists do. This is consistent with Peters’ observation that reflux lasts longer in monitored runners than cyclists (9). The reflux of gastric contents secondary to undiagnosed impaired gastric emptying or poor esophageal clearance in these individuals may explain these and similar results (2,18). Alternatively, cyclists may be protected from position-induced reflux by physical mechanisms such as altered pressure of the diaphragmatic crura while in their racing position. During the “cool-down” period after exercise, in which the athletes were 1) restricted to the exercise room, 2) not permitted food, and 3) not permitted to recline, acid reflux was greater than baseline for the cyclists. This period of reflux in cyclists cannot be explained by exercise-induced changes in intra-abdominal pressure or positional changes. Weightlifters and runners experienced an expected decrease in reflux during “cool-down,” but only the runners’ decrease was statistically significant.

Feeding a precompetitive meal should influence reflux by increasing the volume of intragastric contents available for reflux, increasing tLESr, decreasing gastric emptying, and inducing acid secretion. As predicted, the amount of reflux increases in each of the exercise groups studied in the fed state although statistical significance could only be demonstrated in runners.

Although acid reflux and control of hydrogen ion secretion have become synonymous with gastroesophageal reflux disease and its contemporary treatment, it must be remembered that GERD may more accurately be described as the inappropriate presence of gastric contents in the esophagus regardless of the pH of those contents. This more complete picture of gastroesophageal reflux is captured by extending the pH range of analyzed refluxate from pH <= 4.0 to a pH threshold in the range mimicking the pH of most meals–generally around pH 5.0 (11–13). Gastroesophageal reflux, defined in this way, includes refluxate with a pH below 4.0 as well as gastric contents with pH values falling between 4.0 and 5.0 that move into the esophagus. Reflux of gastric contents may provoke esophageal symptoms independent of acid or synergistically with acid. Contributing factors include volume of the meal, pepsin, bile, and specific meal constituents such as capsaicin (11,12). Based on our experience with assessing total reflux (13), we examined this problem by capturing gastroesophageal reflux with a pH <= 5.0 used for a cutoff in addition to the traditional pH <= 4.

The relative rates of gastroesophageal reflux between athletic groups mirrored those of acid reflux. The most remarkable observation of gastroesophageal reflux demonstrates that weightlifters, whose brief bursts of intense physical effort last only seconds, had reflux throughout one third of the total 80-min exercise period when fasting and half of the time when fed. This finding in weightlifters cannot be explained by mere changes in intra-abdominal pressure during exercise, nor is it due to compromised basal lower esophageal sphincter tone as the mean LESP of the study group was 18 mm Hg (Table 2).

Despite significant reflux during exercise, symptoms were relatively mild. It is possible that esophageal symptoms are altered by the psychological or physiologic suppression of visceral sensation (e.g., endorphin secretion, particularly in these elite athletes). This theory is supported by our observation that during bursts of effort by the weightlifters, mild symptoms were reported, but in the intervals after lifting effort, the athletes complained vigorously of heartburn. The impact of heartburn symptoms on athletic performance seems minimal; however, it is likely that other physiologic changes such as increased airway resistance that occur with acid reflux (6,15) may lead to subtle, unrecognized compromise of maximal competitive performance.

Common lifestyle modifications encouraged to control heartburn acknowledge the importance of body position as a risk factor for reflux during a routine workday and during sleep. Lifestyle modifications emphasize the use of gravity to help diminish reflux. The weightlifting routine was analyzed by body position to focus attention on position and its resulting relative risk of reflux. No differences were found in the amount of reflux regardless of whether weightlifters were upright or reclined. In addition, no differences were detected in the amount of reflux in relation to exercise involving the upper versus lower body—the reflux was high in each of these groups. This is consistent with the observation that no differences in reflux were seen between runners and cyclists in whom the major exercise differentiation was position and not effort. The differences observed during exercise as opposed to recognized symptoms of reflux during ordinary daily activities are difficult to explain. Compensatory physiologic mechanisms during exercise are likely.

Increasing exercise effort has been reported to amplify changes in reflux (16). Our data for the runners, cyclists, and weightlifters, whether fasted or fed, did not statistically support this hypothesis. Differences between the findings in our subjects and those of Soffer et al. (16) may be explained by protocol design differences. We measured reflux during continuous exercise with 85% maximal effort immediately after 60 min of sustained effort at 65% maximal effort. Soffer et al. (16) evaluated graded exercise effort in time blocks of varying length with intervening rest periods. Even with this difference in protocol design, the acid exposure during 90% effort was 13% in Soffer et al.’s study (16) whereas our subjects had 6.9% exposure. Quite possibly, the carefully regimented performance conditions we imposed more accurately reflect a typical exercise program and the physiologic changes due to exercise.

The “siphon effect” of sipping fluid, which draws intragastric contents into the esophagus, was described by Linsman (8) in 1965 as a radiographic test for reflux. This interesting event is complex and partially related to the increased negative intrathoracic pressure during sipping combined with reflex LES relaxation in response to a swallow. This literally suctions fluid from the gastric reservoir into the esophagus. Observations of cyclists drinking fluid while cycling raised the possibility that the siphon effect plays a role in reflux during competitive cycling. The increase in the mean gastric pH is consistent with the dilution of the intragastric contents by water, whereas the simultaneous fall in mean esophageal pH supports the hypothesis that the siphon effect increases refluxate into the esophagus in cyclists.

Physiologic studies of athletes are an area of concern because of the number of changes that can occur during exercise that may influence performance. Conditioned athletes may or may not exhibit changes in gastrointestinal physiology identical to those seen in unconditioned participants. Competitive athletes may select sports in which their somatic/visceral symptoms are minimal or activities in which they can develop compensatory mechanisms. These issues are important areas of exploration in seeking answers to pathophysiologic questions and providing opportunities to utilize pharmacology to influence exercise-induced symptoms.

The authors wish to acknowledge and thank Tim Balm (Procter and Gamble) for his input and review of the manuscript.

This study was funded by an unrestricted grant from the Procter and Gamble Company.

Back to Top | Article Outline

REFERENCES

1. Borg, G. A. Psychophysical bases of perceived exertion. Med. Sci. Sports Exerc. 14: 377-381, 1982.
2. Brouns, F. Gastric emptying as a regulatory factor in fluid uptake. Int. J. Sports Med. 19 (Suppl. 2): S125-S128, 1998.
3. Bruce, R. A. Exercise testing of patients with coronary artery disease. Ann. Clin. Res. 3: 323-332, 1971.
4. Clark, C. S., B. B. Kraus, J. Sinclair, and D. O. Castell. Gastroesophageal reflux induced by exercise in healthy volunteers. JAMA 261: 3599-3601, 1989.
5. Foster, C., A. S. Jackson, M. L. Pollock, et al. Generalized equations for predicting functional capacity from treadmill performance. Am. Heart J. 107: 1229-1234, 1984.
6. Harding, S. M., C. A. Schan, M. R. Guzzo, R. W. Alexander, L. A. Bradley, and J. E. Richter. Gastroesophageal reflux-induced bronchoconstriction: is micro-aspiration a factor? Chest 108: 1220-1227, 1995.
7. Kraus, B. B., J. W. Sinclair, and D. O. Castell. Gastroesophageal reflux in runners. Ann. Intern. Med. 112: 429-433, 1990.
8. Linsman, J. F. Gastroesophageal reflux elicited while drinking water (water siphonage test): its clinical correlation with pyrosis. Am. J. Roentgenol. 94: 325-332, 1965.
9. Peters, H. P. F., J. W. C. Wiersma, J. Koerselman, et al. The effect of a sports drink on gastroesophageal reflux during a run-bike-run test. Int. J. Sports Med. 21: 65-70, 2000.
10. Pollock, M. L., J. Broida, and Z. Kendrick. Validity of the palpation technique of heart rate determination and its estimation of training heart rate. Res. Q. 43: 77-81, 1972.
11. Rodriguez-Stanley, S., K. L. Collings, M. Robinson, J. Filinto, S. Zubaidi, and P. B. Miner. Capsaicin: effects on symptoms, reflux and gastric emptying. Aliment. Pharmacol. Ther. 14: 129-134, 2000.
12. Rodriguez-Stanley, S., M. Robinson, D. L. Earnest, B. Greenwood-Van Meerveld, and P. B. Miner. Esophageal hypersensitivity may be a major cause of heartburn. Am. J. Gastroenterol. 94: 628-631, 1999.
13. Rodriguez-Stanley, S., K. L. Collings, J. Filinto, S. Zubaidi, M. Robinson, and P. B. Miner. A pH threshold of 4.0 underestimates gastroesophageal reflux (Abstract). Gastroenterology 116:G1287, A293, 1999.
14. Saltin, B., and P. O. Astran. Maximal oxygen uptake in athletes. J. Appl. Physiol. 23: 353-358, 1967.
15. Schan, C. A., S. M. Harding, J. M. Haile, L. A. Bradley, and J. E. Richter. Gastroesophageal reflux-induced bronchoconstriction: an intra-esophageal acid infusion study using state-of-the-art technology. Chest 106: 731-737, 1994.
16. Soffer, E. E., J. Wilson, G. Duethman, J. Launspach, and T. E. Adrian. Effect of graded exercise on esophageal motility and gastroesophageal reflux in non-trained subjects. Dig. Dis. Sci. 39: 193-198, 1994.
17. Strauss, R. H., R. R. Lanese, and D. J. Leizman. Illness and absence among wrestlers, swimmers and gymnasts at a large university. Am. J. Sports Med. 16: 653-655, 1988.
18. Van Nieuwenhoven, M. A., R. J. M. Brummer, and F. Brouns. Gastrointestinal function during exercise: comparison of water, sports drink, and sports drink with caffeine. J. Appl. Physiol. 89: 1079-1085, 2000.
19. Worme, J. D., T. J. Doubt, A. Singh, C. J. Ryan, F. M. Moses, and P. A. Deuster. Dietary patterns, gastrointestinal complaints, and nutrition knowledge of recreational triathletes. Am. J. Clin. Nutr. 51: 690-697, 1990.
20. Worobetz, L. J., and D. F. Gerrard. Gastrointestinal symptoms during exercise in enduro athletes: prevalence and speculations on aetiology. N. Z. Med. J. 98: 644-646, 1985.
21. Yazaki, E., A. Shawdon, I. Beasley, and D. F. Evans. The effect of different types of exercise on gastro-oesophageal reflux. Aust. J. Sci. Med. Sport. 28: 93-96, 1996.
Keywords:

GASTROESOPHAGEAL REFLUX; HEARTBURN; GASTROINTESTINAL MOTILITY; EXERCISE; ESOPHAGEAL PH; ATHLETES

© 2003 American College of Sports Medicine