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).
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%.
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.
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).
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.
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Keywords:© 2003 American College of Sports Medicine
GASTROESOPHAGEAL REFLUX; HEARTBURN; GASTROINTESTINAL MOTILITY; EXERCISE; ESOPHAGEAL PH; ATHLETES