Digestive Diseases and Sciences, Vol. 35, No, 4 (April 1990), pp. 428--432
Exercise Increases Solid Meal Gastric Emptying Rates in Men J.G. M O O R E , MD, F.L. D A T Z , MD, and P.E. C H R I S T I A N , BS
Gastric emptying rates o f radiolabeled b e e f stew meals were measured in 10 healthy, young (median age = 27 years) male subjects on each o f three randomly chosen study days. The subjects either (1) stood at rest, (2) walked on an exercise treadmill at 3.2 km/hr, or (3) at 6.4 km/hr during the study while gastric emptying was being monitored by externally positioned g a m m a cameras. Compared to the standing at rest study, exercise significantly increased gastric emptying (at rest emptying half-time (tl/2) = 72.6 + 7.6 (SEM) min; 3.2 km/hr tl/2 = 44.5 +- 3.9 min, P = 0.0051; 6.4 km/hr tl/2 = 32.9 +- 1.9 min, P = 0,0051). The 6.4 km/hr emptying time was significantly (P = O.0249)faster than the 3.2 km/hr e m p t y i n g time. Thus, the amount o f exercise is a physiological factor that alters solid meal gastric emptying rates. KEY WORDS: gastric emptying; exercise; radionuclide solid meals; human.
Exercise has been reported to accelerate, delay, or not influence liquid meal gastric emptying rates and to accelerate solid meal gastric emptying rates (15). All of these studies have been difficult to interpret b e c a u s e o f the different methods e m p l o y e d to study gastric emptying during exercise, the degree of exercise, the small numbers of subjects studied, and the inclusion of both males and females in the healthy study populations. The p u r p o s e of this investigation was to study the effect of light and m o d e r a t e exercise on solid food emptying rates in a group of young, healthy male subjects. M A T E R I A L S AND M E T H O D S Subjects. Ten healthy male volunteer subjects [median age = 27 (22-44) years; median weight = 79.5 (68.2Manuscript received July 25, 1989; accepted December 7, 1989. From the University of Utah, Division of Nuclear Medicine and Department of Medicine, Veterans Affairs Medical Center, Salt Lake City, Utah. Support for this paper was provided by the Veterans Affairs Medical Center, Salt Lake City, Utah 84148. Address for reprint requests: Dr. John G. Moore, VA Medical Center ( l l 1G), 500 Foothill Blvd., Salt Lake City, Utah 84148.
428
102.2) kg] were studied. All denied any previous history of chronic upper gastrointestinal disease or recent use of medications known to alter gastrointestinal function. The subjects were prohibited from smoking, alcohol, or medication use during and for three days prior to performance of each emptying study. Each subject had three emptying studies administered in random design over eight months. Four of the 10 subjects participated in an earlier study of the effect of posture on gastric emptying (6). Informed consent was obtained following approval by the Institutional Review Board of the University of Utah. Meals and Solid-Phase Radioisotope Marker. For each emptying study, subjects were given a 300-g standardized test meal consisting of 150 g of beef stew and 150 g of orange juice. The total caloric value of this meal was 208 kcal. The preparation of each solid meal included the radiolabeling by injection of 5-7 mCi of technetium-99m sulfur colloid into commercial pork liver pat6 (Sells) followed by frying until crisp. The labeled liver pat6 was then mixed evenly into the beef stew prior to ingestion. The validation of this method of preparation has been reported (7). The estimated radiation with the administered dose (600 p~Ci) of 99mTc is 11 mrad for total body and 144 mrad for stomach (8). Meal consumption time was less than 5 min. Radioisotopic Counting Standing at Rest. Imaging techniques and validation studies for studies performed in the standing position have been described (9). Images were obtained with a scintillation camera equipped with a Digestive Diseases and Sciences, Vol. 35, No. 4 (April 1990)
0163-2116/90/0400-0428506.00/09 1990PlenumPublishingCorporation
EXERCISE AND GASTRIC EMPTYING low-energy parallel hole collimator. The solid-phase counts were recorded by setting the pulse-height analyzer on the 140 keV photopeak of 99mTCwith a 15% window. The subjects ingested the meal in the standing position and stood in front of the gamma camera for abdominal imaging and counting. Counting acquisition time was 60 sec for each position (anterior and posterior) at each time interval. In between imaging intervals, the subjects stood at rest. External 99mTC point sources were taped to the abdomen to allow for more accurate horizontal and vertical repositioning of the subject. At every timing interval, images were acquired in both the anterior and posterior projections by having the subject rotate 180 degrees in front of the camera. The geometric mean of the anterior and posterior counts obtained for the gastric region of interest was calculated to correct for the effect of depth and radiation attenuation within the body (10). The counts observed at each imaging interval were normalized to a percentage of the count obtained at meal conclusion (zero time), which was assigned a 100% value. Images and counts were obtained at zero time, and every 15 min thereafter for 2 hr. Radioisotopie Counting Walking at 3.2 kin/hr. The images, counts, and correction factors were obtained and applied in an identical manner to the standing study except that subjects began walking at the rate of 3.2 km/hr on an exercise treadmill (Quinton, Seattle, Washington) immediately following the first image (zero time). Approximately 13 min of each 15-min counting interval was spent in exercise. Radioisotopie Counting Walking at 6.4 kin/hr. This study was identical to the walking at 3.2 km/hr study except that the subject began fast walking at the rate of 6.4 km/hr on the exercise treadmill immediately following the first image (zero time). The three studies were done on all subjects on separate study days by random selection. Resting and exercise pulse rates at 1 and 2 hr after beginning exercise were obtained on all subjects. Statistical Analysis. Means and standard errors of the normalized counts were computed at each imaging interval. Tests for linearity revealed that, for the group of studies, the data conformed most closely to a linear fit (standing at rest: R 2 = 0.817 (linear), 0.75 (exponential); walking at 3.2 km/hr: R E = 0.846 (linear), 0.697 (exponential); walking at 6.4 km/hr: R 2 = 0.862 (linear), 0.878 (exponential). Linear regression slopes were computed and compared for all studies. The emptying half-times (tlAs)--the time taken after meal ingestion for 50% of the radionuclide marker to empty from the gastric region of interest--were computed from the linear regression slopes. Two-tailed paired t tests for significant differences were applied at all counting intervals and for tlA. RESULTS Standing at Rest. The standing only study (Figure 1) produced the slowest gastric emptying rates when compared to the exercise studies. The mean percent retention values in the standing only study when c o m p a r e d to the 3.2 km/hr walking study Digestive Diseases and Sciences, Vol. 35, No. 4 (April 1990)
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were significantly higher at all eight 15-min counting intervals following the zero time image (15 min, P = 0.013; 30 min, P = 0.004; 45 min, P = 0.005; 60 min, P < 0.001; 75 min, P < 0.001; 90 min, P < 0.001; 105 min, P = 0.006; 120 min, P = 0.022). The mean tl/2 values were also significantly different [standing tl/2 = 72.6 --- 7.6 (SEM) min; 3.2 km/hr walking tVz = 44.5 --- 3.9 min; P = 0.0051] as were the regression slopes (standing slope = - 0 . 6 3 4 ; 3.2 km/hr; walking slope = - 0 . 7 6 0 ; P < 0.05). The mean percent retention values in the standing only study, when c o m p a r e d to the 6.4 km/hr walking study, were also significantly higher at all eight 15-min counting intervals following the zero time image (15 min, P = 0.028; 30 min, P = 0.002; 45 rain, P < 0.001; 60 min, P < 0.001; 75 min, P < 0.001; 90 min, P < 0.001; 105 min, P = 0.001; 120 min, P = 0.001). The mean tl/2 values were also significantly different (standing t1/2 = 72.6 --- 7.6 min; 6.4 km/hr walking tV2 = 32.9 --- 1.9 min; P = 0.0051) as were the regression slopes (standing slope = - 0 . 6 3 4 ; 6.4 km/hr walking slope = - 0 . 7 9 0 ; P < 0.05) (Figures 1 and 2). Walking at 3.2 kin/hr. Walking at 3.2 km/hr, c o m p a r e d to the standing at rest study, resulted in significantly more rapid gastric emptying rates. The 3.2 km/hr study, when c o m p a r e d to the 6.4 km/hr study, produced significantly higher mean percent retention values at four counting intervals (30 min, P = 0.049; 90 min, P = 0.029; 105 min, P = 0.030; 120 min, P = 0.049). The mean tl/2 values were also significantly different (3.2 km/hr tVz = 44.5 -+ 3.9
429
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min; 6.4 km/hr tl/2 = 32.9 -+ 1.9 min; P = 0.0249). The regression slopes were not significantly different (3.2 km/hr slope = -0.760; 6.4 km/hr slope = -0.790; P = NS) (Figures 1 and 2). Walking at 6.4 km/hr. Walking at 6.4 km/hr, compared to the standing only and 3.2 km/hr walking studies, produced the most rapid gastric emptying rates (Figures I and 2). Effects of Exercise. Pulse rates (PR) rose at 1 and 2 hr after beginning exercise when compared to the standing at rest pulse rate [standing at rest mean PR = 71.4 -+ 3.0; 3.2 km/hr PR = 79.3 -+ 4.2 (1 hr, P = 0.144), 83.4 -+ 4.4 (2 hr, P = 0.041); 6.4 km/hr PR = 101.4 _+ 4.4 (1 hr, P < 0.001), 110.8 _+ 3.5 (2 hr, P < 0.001)]. DISCUSSION This study demonstrated that exercise significantly enhanced solid-meal gastric emptying rates. When compared to standing only, walking at 3.2 km/hr and 6.4 km/hr enhanced gastric emptying rates by 39% and 55%, respectively. When compared to the lying at rest position in a previous study, in which 4 of the 10 subjects participated, the enhancement in gastric emptying was even more pronounced (6). Compared to the lying position, walking at 3.2 km/hr and 6.4 km/hr increased gastric emptying rates by 62% and 72%, respectively. Thus, exercise and body posture, in addition to a host of other variables such as marker species, marker stability, meal weight, meal caloric content, meal composition, the use of geometric mean cor-
430
rection, sex, age, and time of day when measurements are obtained have all been shown to significantly influence the measurement and interpretation of radionuclide-based tests of gastric emptying (6, 9-18). These factors must be taken into account when establishing a standardized gastric emptying method, a point repeatedly emphasized in the literature (12-14, 20-23). Exercise is another variable in this measurement that must be controlled within each laboratory. These results are in agreement with those of Cammack et al who, employing a radionuclidebased method similar to ours, demonstrated that prolonged exercise (bicycle riding) significantly increased gastric emptying rates in a group (N = 7; six males, one female) of healthy volunteers (5). However, Feldman and Nixon, employing an intestinal tube-dye recovery technique, demonstrated that exercise (bicycle riding) had no significant effect on gastric emptying rates in a group (N = 5; two males, three females) of healthy volunteers (4). Both studies included small numbers of subjects, and both studies included males and females in their study populations. It has been demonstrated that sex markedly influences gastric emptying rates. Premenopausal females have markedly slower gastric emptying rates when compared to age matched males (6, 7). Thus, it is not appropriate to mix sexes when evaluating any variable that may influence gastric emptying. In addition, the dye-recovery technique for measuring gastric emptying employed in the latter study permitted measurement of only Digestive Diseases and Sciences, Vol. 35, No. 4 (April 1990)
EXERCISE AND GASTRIC EMPTYING
the liquid phase of the meal. Furthermore, intestinal intubation itself alters upper gastrointestinal tract transit (23). Carrio et al reported that exercise did not significantly alter gastric emptying of a radiolabeled egg omelet meal in a group of trained male marathon runners, when compared to resting studies in the same subjects (24). However, their resting meal gastric emptying rates were significantly faster than those of a sedentary group, matched for age and sex. These findings suggested to the authors that adaptation in gastric emptying occurs in trained athletes, possibly related to functional changes in sympathetic and parasympathetic neurohumoral influences on gastric emptying. In a recent report, walking at 4.5 km/hr was shown to increase mouth-to-cecum transit time in a group (N = 2 3 : 9 males. 14 females) of healthy adults (25). Hydrogen breath concentration determinations following an oral load of 10 g of lactulose was used to measure total mouth-to-cecum transit time. and no attempt was made to study gastric transit time separately. However. these results may be reconciled with the findings of decreased gastric transit times with exercise reported herein. Disparate gastric and small bowel emptying and transit patterns were reported as an effect of upper gastrointestinal tract intubation (23). Intestinal intubation slowed gastric emptying while increasing small bowel transit. Thus, changes in gastric emptying may occur independent of changes small bowel transit, a previously noted observation (26). It is possible that the observation of enhanced gastric emptying rates for meals with exercise has clinical application. Patients with complaints of postprandial fullness and epigastric discomfort may benefit by walking following their meals. Patients with demonstrated delayed gastric emptying patterns, eg, diabetics with gastropathy, may also benefit, although their gastric emptying responses to changes in body posture and exercise has yet to be demonstrated.
REFERENCES I. Campbell JMH, Mitchell MB, Powell ATW: The influence of exercise on digestion. Guy's Hosp Rep 78:279-293, 1928 2. Hellenbrandt FA, Tepper RH: Studies on the influence of exercise on the digestive work of the stomach. II. Its effect on emptying time. Am J Physiol 107:355-363, 1934 3. Fordtran JS, Saltin B: Gastric emptying and intestinal absorption during prolonged severe exercise. J Apply Physiol 23:331-335, 1965 Digestive Diseases and Sciences, Vol. 35, No. 4 (April 1990)
4. Feldman M, Nixon JV: Effect of exercise on postprandial gastric secretion and emptying in humans. J Appl Physiol 53(4):851-854, 1982 5. Cammack J, Read NW, Cann PA, Greenwood B, Holgate AM: Effect of prolonged exercise on the passage of a solid meal through the stomach and small intestine. Gut 23:957961, 1982 6. Moore JG, Datz FL, Christian PE, Greenberg E, Alazraki N: Effect of body posture on radionuclide measurements of gastric emptying. Dig Dis Sci 33(12):1592-1595, 1988 7. Christian PE, Moore JG, Datz FL: Comparisons of Tc99m-labelled liver and liver pat6 as markers for solid phase gastric emptying. J Nucl Med 25:364-366, 1984 8. Siegel JA, Wu RK, Knight LC, Zelec RE, Stern HS, Malmud LS: Radiation dose estimates for oral agents used in gastrointestinal disease. J Nucl Med 24:835-837, 1983 9. Moore JG, Christian PE, Coleman RE: Gastric emptying of varying meal weight and composition in man. Evaluation by dual liquid- and solid-phase isotopic method. Dig Dis Sci 26(1):16-22, 1981 10. Moore JG, Christian PE, Taylor AT, Alazraki N: Gastric emptying measurements: Delayed and complex patterns without appropriate corrections. J Nucl Med 26:1206-1210, 1985 11. Datz FL, Christian PE, Moore JG: Gender-related differences in gastric emptying. J Nucl Med 28:1204-1207, 1987 12. Hutson WR, Roehrkasse RL, Wald A: Influence of gender and menopause on gastric emptying and motility. Gastroenterology 96:11-17, 1989 13. Heading RC, Tothill P, McGloughlin GP, Sherman DJC: Gastric emptying rate measurement in man. A double isotope scanning technique for simultaneous study of liquid and solid components at a meal. Gastroenterology 71:45-50, 1976 14. Meyer JH, MacGregor IL, Guellar R, Martin P, Cavalieri R: 99mTc-Tagged chicken liver as a marker of solid food in the human subject. Am J Dig Dis 21:296-304, 1976 15. Moore JG, Christian PE, Brown JA, Brophy C, Datz FL, Taylor AT, Alazraki N: Influence of meal weight and caloric content on gastric emptying of meals in man. Dig Dis Sci 29(6):513-519, 1984 16. Dugas MC, Schade RR, Lhotsky D, Van Theil D: Comparison of methods for gastric isotope emptying. Am J Physiol 243(3):6237-6242, 1982 17. Moore JG, Tweedy C, Christian PE, Datz FL: Effect of age on gastric emptying of liquid-solid meals in man. Dig Dis Sci 28(4):340-343, 1983 18. Goo RH, Moore JG, Greenberg E, Alazraki N: Circadian variation in gastric emptying of meals in man. Gastroenterology 993:515-518, 1987 19. Loo FD, Palmer DW, Soergel KH, Kalbfleisch JH, Wood CN: Gastric emptying in patients with diabetes mellitus. Gastroenterology 86:485-494, 1984 20. Meyer JH, Van Deventer G, Graham LS: Error and corrections with scintigraphic measurements of gastric emptying. J Nucl Med 24:197-203, 1983 21. Tothill P, McGloughlin GP, Heading RC: Technique and errors in scintigraphic measurements of gastric emptying. J Nucl Med 19:256-261, 1978 22. Malmud LS, Fisher RS, Knight LC, Rock E: Scintigraphic evaluation of gastric emptying. Semin Nucl Med 12:116-125, 1982
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MOORE ET AL 23. Read NW, A1 Janabi MN, Bates TE, Barber DC: Effect of gastrointestinal intubation on the passage of a solid meal through the stomach and small intestine in humans. Gastroenterology 84:1568-1572, 1983 24. Carrio I, Estorch M, Serra-Grima R, Ginjaume M, Notivol R, Calabuig R, Vilardell F: Gastric emptying in marathon runners. Gut 30:152-155, 1989
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25. Meshkinpour H, Kemp C, Fairshter R: Effect of aerobic exercise on mouth-to-cecum transit time. Gastroenterology 96(3):938-941, 1989 26. Read NW, Cammack J, Edwards C, Holgate AM, Cann PA, Brown C: Is the transit time of a meal through the small intestine related tO the rate at which it leaves the stomach? Gut 23:824-828, 1982
Digestive Diseases and Sciences, Vol. 35, No. 4 (April 1990)
Exercise Increases Solid Meal Gastric Emptying Rates in Men J.G. M O O R E , MD, F.L. D A T Z , MD, and P.E. C H R I S T I A N , BS
Gastric emptying rates o f radiolabeled b e e f stew meals were measured in 10 healthy, young (median age = 27 years) male subjects on each o f three randomly chosen study days. The subjects either (1) stood at rest, (2) walked on an exercise treadmill at 3.2 km/hr, or (3) at 6.4 km/hr during the study while gastric emptying was being monitored by externally positioned g a m m a cameras. Compared to the standing at rest study, exercise significantly increased gastric emptying (at rest emptying half-time (tl/2) = 72.6 + 7.6 (SEM) min; 3.2 km/hr tl/2 = 44.5 +- 3.9 min, P = 0.0051; 6.4 km/hr tl/2 = 32.9 +- 1.9 min, P = 0,0051). The 6.4 km/hr emptying time was significantly (P = O.0249)faster than the 3.2 km/hr e m p t y i n g time. Thus, the amount o f exercise is a physiological factor that alters solid meal gastric emptying rates. KEY WORDS: gastric emptying; exercise; radionuclide solid meals; human.
Exercise has been reported to accelerate, delay, or not influence liquid meal gastric emptying rates and to accelerate solid meal gastric emptying rates (15). All of these studies have been difficult to interpret b e c a u s e o f the different methods e m p l o y e d to study gastric emptying during exercise, the degree of exercise, the small numbers of subjects studied, and the inclusion of both males and females in the healthy study populations. The p u r p o s e of this investigation was to study the effect of light and m o d e r a t e exercise on solid food emptying rates in a group of young, healthy male subjects. M A T E R I A L S AND M E T H O D S Subjects. Ten healthy male volunteer subjects [median age = 27 (22-44) years; median weight = 79.5 (68.2Manuscript received July 25, 1989; accepted December 7, 1989. From the University of Utah, Division of Nuclear Medicine and Department of Medicine, Veterans Affairs Medical Center, Salt Lake City, Utah. Support for this paper was provided by the Veterans Affairs Medical Center, Salt Lake City, Utah 84148. Address for reprint requests: Dr. John G. Moore, VA Medical Center ( l l 1G), 500 Foothill Blvd., Salt Lake City, Utah 84148.
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102.2) kg] were studied. All denied any previous history of chronic upper gastrointestinal disease or recent use of medications known to alter gastrointestinal function. The subjects were prohibited from smoking, alcohol, or medication use during and for three days prior to performance of each emptying study. Each subject had three emptying studies administered in random design over eight months. Four of the 10 subjects participated in an earlier study of the effect of posture on gastric emptying (6). Informed consent was obtained following approval by the Institutional Review Board of the University of Utah. Meals and Solid-Phase Radioisotope Marker. For each emptying study, subjects were given a 300-g standardized test meal consisting of 150 g of beef stew and 150 g of orange juice. The total caloric value of this meal was 208 kcal. The preparation of each solid meal included the radiolabeling by injection of 5-7 mCi of technetium-99m sulfur colloid into commercial pork liver pat6 (Sells) followed by frying until crisp. The labeled liver pat6 was then mixed evenly into the beef stew prior to ingestion. The validation of this method of preparation has been reported (7). The estimated radiation with the administered dose (600 p~Ci) of 99mTc is 11 mrad for total body and 144 mrad for stomach (8). Meal consumption time was less than 5 min. Radioisotopic Counting Standing at Rest. Imaging techniques and validation studies for studies performed in the standing position have been described (9). Images were obtained with a scintillation camera equipped with a Digestive Diseases and Sciences, Vol. 35, No. 4 (April 1990)
0163-2116/90/0400-0428506.00/09 1990PlenumPublishingCorporation
EXERCISE AND GASTRIC EMPTYING low-energy parallel hole collimator. The solid-phase counts were recorded by setting the pulse-height analyzer on the 140 keV photopeak of 99mTCwith a 15% window. The subjects ingested the meal in the standing position and stood in front of the gamma camera for abdominal imaging and counting. Counting acquisition time was 60 sec for each position (anterior and posterior) at each time interval. In between imaging intervals, the subjects stood at rest. External 99mTC point sources were taped to the abdomen to allow for more accurate horizontal and vertical repositioning of the subject. At every timing interval, images were acquired in both the anterior and posterior projections by having the subject rotate 180 degrees in front of the camera. The geometric mean of the anterior and posterior counts obtained for the gastric region of interest was calculated to correct for the effect of depth and radiation attenuation within the body (10). The counts observed at each imaging interval were normalized to a percentage of the count obtained at meal conclusion (zero time), which was assigned a 100% value. Images and counts were obtained at zero time, and every 15 min thereafter for 2 hr. Radioisotopie Counting Walking at 3.2 kin/hr. The images, counts, and correction factors were obtained and applied in an identical manner to the standing study except that subjects began walking at the rate of 3.2 km/hr on an exercise treadmill (Quinton, Seattle, Washington) immediately following the first image (zero time). Approximately 13 min of each 15-min counting interval was spent in exercise. Radioisotopie Counting Walking at 6.4 kin/hr. This study was identical to the walking at 3.2 km/hr study except that the subject began fast walking at the rate of 6.4 km/hr on the exercise treadmill immediately following the first image (zero time). The three studies were done on all subjects on separate study days by random selection. Resting and exercise pulse rates at 1 and 2 hr after beginning exercise were obtained on all subjects. Statistical Analysis. Means and standard errors of the normalized counts were computed at each imaging interval. Tests for linearity revealed that, for the group of studies, the data conformed most closely to a linear fit (standing at rest: R 2 = 0.817 (linear), 0.75 (exponential); walking at 3.2 km/hr: R E = 0.846 (linear), 0.697 (exponential); walking at 6.4 km/hr: R 2 = 0.862 (linear), 0.878 (exponential). Linear regression slopes were computed and compared for all studies. The emptying half-times (tlAs)--the time taken after meal ingestion for 50% of the radionuclide marker to empty from the gastric region of interest--were computed from the linear regression slopes. Two-tailed paired t tests for significant differences were applied at all counting intervals and for tlA. RESULTS Standing at Rest. The standing only study (Figure 1) produced the slowest gastric emptying rates when compared to the exercise studies. The mean percent retention values in the standing only study when c o m p a r e d to the 3.2 km/hr walking study Digestive Diseases and Sciences, Vol. 35, No. 4 (April 1990)
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were significantly higher at all eight 15-min counting intervals following the zero time image (15 min, P = 0.013; 30 min, P = 0.004; 45 min, P = 0.005; 60 min, P < 0.001; 75 min, P < 0.001; 90 min, P < 0.001; 105 min, P = 0.006; 120 min, P = 0.022). The mean tl/2 values were also significantly different [standing tl/2 = 72.6 --- 7.6 (SEM) min; 3.2 km/hr walking tVz = 44.5 --- 3.9 min; P = 0.0051] as were the regression slopes (standing slope = - 0 . 6 3 4 ; 3.2 km/hr; walking slope = - 0 . 7 6 0 ; P < 0.05). The mean percent retention values in the standing only study, when c o m p a r e d to the 6.4 km/hr walking study, were also significantly higher at all eight 15-min counting intervals following the zero time image (15 min, P = 0.028; 30 min, P = 0.002; 45 rain, P < 0.001; 60 min, P < 0.001; 75 min, P < 0.001; 90 min, P < 0.001; 105 min, P = 0.001; 120 min, P = 0.001). The mean tl/2 values were also significantly different (standing t1/2 = 72.6 --- 7.6 min; 6.4 km/hr walking tV2 = 32.9 --- 1.9 min; P = 0.0051) as were the regression slopes (standing slope = - 0 . 6 3 4 ; 6.4 km/hr walking slope = - 0 . 7 9 0 ; P < 0.05) (Figures 1 and 2). Walking at 3.2 kin/hr. Walking at 3.2 km/hr, c o m p a r e d to the standing at rest study, resulted in significantly more rapid gastric emptying rates. The 3.2 km/hr study, when c o m p a r e d to the 6.4 km/hr study, produced significantly higher mean percent retention values at four counting intervals (30 min, P = 0.049; 90 min, P = 0.029; 105 min, P = 0.030; 120 min, P = 0.049). The mean tl/2 values were also significantly different (3.2 km/hr tVz = 44.5 -+ 3.9
429
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min; 6.4 km/hr tl/2 = 32.9 -+ 1.9 min; P = 0.0249). The regression slopes were not significantly different (3.2 km/hr slope = -0.760; 6.4 km/hr slope = -0.790; P = NS) (Figures 1 and 2). Walking at 6.4 km/hr. Walking at 6.4 km/hr, compared to the standing only and 3.2 km/hr walking studies, produced the most rapid gastric emptying rates (Figures I and 2). Effects of Exercise. Pulse rates (PR) rose at 1 and 2 hr after beginning exercise when compared to the standing at rest pulse rate [standing at rest mean PR = 71.4 -+ 3.0; 3.2 km/hr PR = 79.3 -+ 4.2 (1 hr, P = 0.144), 83.4 -+ 4.4 (2 hr, P = 0.041); 6.4 km/hr PR = 101.4 _+ 4.4 (1 hr, P < 0.001), 110.8 _+ 3.5 (2 hr, P < 0.001)]. DISCUSSION This study demonstrated that exercise significantly enhanced solid-meal gastric emptying rates. When compared to standing only, walking at 3.2 km/hr and 6.4 km/hr enhanced gastric emptying rates by 39% and 55%, respectively. When compared to the lying at rest position in a previous study, in which 4 of the 10 subjects participated, the enhancement in gastric emptying was even more pronounced (6). Compared to the lying position, walking at 3.2 km/hr and 6.4 km/hr increased gastric emptying rates by 62% and 72%, respectively. Thus, exercise and body posture, in addition to a host of other variables such as marker species, marker stability, meal weight, meal caloric content, meal composition, the use of geometric mean cor-
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rection, sex, age, and time of day when measurements are obtained have all been shown to significantly influence the measurement and interpretation of radionuclide-based tests of gastric emptying (6, 9-18). These factors must be taken into account when establishing a standardized gastric emptying method, a point repeatedly emphasized in the literature (12-14, 20-23). Exercise is another variable in this measurement that must be controlled within each laboratory. These results are in agreement with those of Cammack et al who, employing a radionuclidebased method similar to ours, demonstrated that prolonged exercise (bicycle riding) significantly increased gastric emptying rates in a group (N = 7; six males, one female) of healthy volunteers (5). However, Feldman and Nixon, employing an intestinal tube-dye recovery technique, demonstrated that exercise (bicycle riding) had no significant effect on gastric emptying rates in a group (N = 5; two males, three females) of healthy volunteers (4). Both studies included small numbers of subjects, and both studies included males and females in their study populations. It has been demonstrated that sex markedly influences gastric emptying rates. Premenopausal females have markedly slower gastric emptying rates when compared to age matched males (6, 7). Thus, it is not appropriate to mix sexes when evaluating any variable that may influence gastric emptying. In addition, the dye-recovery technique for measuring gastric emptying employed in the latter study permitted measurement of only Digestive Diseases and Sciences, Vol. 35, No. 4 (April 1990)
EXERCISE AND GASTRIC EMPTYING
the liquid phase of the meal. Furthermore, intestinal intubation itself alters upper gastrointestinal tract transit (23). Carrio et al reported that exercise did not significantly alter gastric emptying of a radiolabeled egg omelet meal in a group of trained male marathon runners, when compared to resting studies in the same subjects (24). However, their resting meal gastric emptying rates were significantly faster than those of a sedentary group, matched for age and sex. These findings suggested to the authors that adaptation in gastric emptying occurs in trained athletes, possibly related to functional changes in sympathetic and parasympathetic neurohumoral influences on gastric emptying. In a recent report, walking at 4.5 km/hr was shown to increase mouth-to-cecum transit time in a group (N = 2 3 : 9 males. 14 females) of healthy adults (25). Hydrogen breath concentration determinations following an oral load of 10 g of lactulose was used to measure total mouth-to-cecum transit time. and no attempt was made to study gastric transit time separately. However. these results may be reconciled with the findings of decreased gastric transit times with exercise reported herein. Disparate gastric and small bowel emptying and transit patterns were reported as an effect of upper gastrointestinal tract intubation (23). Intestinal intubation slowed gastric emptying while increasing small bowel transit. Thus, changes in gastric emptying may occur independent of changes small bowel transit, a previously noted observation (26). It is possible that the observation of enhanced gastric emptying rates for meals with exercise has clinical application. Patients with complaints of postprandial fullness and epigastric discomfort may benefit by walking following their meals. Patients with demonstrated delayed gastric emptying patterns, eg, diabetics with gastropathy, may also benefit, although their gastric emptying responses to changes in body posture and exercise has yet to be demonstrated.
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4. Feldman M, Nixon JV: Effect of exercise on postprandial gastric secretion and emptying in humans. J Appl Physiol 53(4):851-854, 1982 5. Cammack J, Read NW, Cann PA, Greenwood B, Holgate AM: Effect of prolonged exercise on the passage of a solid meal through the stomach and small intestine. Gut 23:957961, 1982 6. Moore JG, Datz FL, Christian PE, Greenberg E, Alazraki N: Effect of body posture on radionuclide measurements of gastric emptying. Dig Dis Sci 33(12):1592-1595, 1988 7. Christian PE, Moore JG, Datz FL: Comparisons of Tc99m-labelled liver and liver pat6 as markers for solid phase gastric emptying. J Nucl Med 25:364-366, 1984 8. Siegel JA, Wu RK, Knight LC, Zelec RE, Stern HS, Malmud LS: Radiation dose estimates for oral agents used in gastrointestinal disease. J Nucl Med 24:835-837, 1983 9. Moore JG, Christian PE, Coleman RE: Gastric emptying of varying meal weight and composition in man. Evaluation by dual liquid- and solid-phase isotopic method. Dig Dis Sci 26(1):16-22, 1981 10. Moore JG, Christian PE, Taylor AT, Alazraki N: Gastric emptying measurements: Delayed and complex patterns without appropriate corrections. J Nucl Med 26:1206-1210, 1985 11. Datz FL, Christian PE, Moore JG: Gender-related differences in gastric emptying. J Nucl Med 28:1204-1207, 1987 12. Hutson WR, Roehrkasse RL, Wald A: Influence of gender and menopause on gastric emptying and motility. Gastroenterology 96:11-17, 1989 13. Heading RC, Tothill P, McGloughlin GP, Sherman DJC: Gastric emptying rate measurement in man. A double isotope scanning technique for simultaneous study of liquid and solid components at a meal. Gastroenterology 71:45-50, 1976 14. Meyer JH, MacGregor IL, Guellar R, Martin P, Cavalieri R: 99mTc-Tagged chicken liver as a marker of solid food in the human subject. Am J Dig Dis 21:296-304, 1976 15. Moore JG, Christian PE, Brown JA, Brophy C, Datz FL, Taylor AT, Alazraki N: Influence of meal weight and caloric content on gastric emptying of meals in man. Dig Dis Sci 29(6):513-519, 1984 16. Dugas MC, Schade RR, Lhotsky D, Van Theil D: Comparison of methods for gastric isotope emptying. Am J Physiol 243(3):6237-6242, 1982 17. Moore JG, Tweedy C, Christian PE, Datz FL: Effect of age on gastric emptying of liquid-solid meals in man. Dig Dis Sci 28(4):340-343, 1983 18. Goo RH, Moore JG, Greenberg E, Alazraki N: Circadian variation in gastric emptying of meals in man. Gastroenterology 993:515-518, 1987 19. Loo FD, Palmer DW, Soergel KH, Kalbfleisch JH, Wood CN: Gastric emptying in patients with diabetes mellitus. Gastroenterology 86:485-494, 1984 20. Meyer JH, Van Deventer G, Graham LS: Error and corrections with scintigraphic measurements of gastric emptying. J Nucl Med 24:197-203, 1983 21. Tothill P, McGloughlin GP, Heading RC: Technique and errors in scintigraphic measurements of gastric emptying. J Nucl Med 19:256-261, 1978 22. Malmud LS, Fisher RS, Knight LC, Rock E: Scintigraphic evaluation of gastric emptying. Semin Nucl Med 12:116-125, 1982
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MOORE ET AL 23. Read NW, A1 Janabi MN, Bates TE, Barber DC: Effect of gastrointestinal intubation on the passage of a solid meal through the stomach and small intestine in humans. Gastroenterology 84:1568-1572, 1983 24. Carrio I, Estorch M, Serra-Grima R, Ginjaume M, Notivol R, Calabuig R, Vilardell F: Gastric emptying in marathon runners. Gut 30:152-155, 1989
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25. Meshkinpour H, Kemp C, Fairshter R: Effect of aerobic exercise on mouth-to-cecum transit time. Gastroenterology 96(3):938-941, 1989 26. Read NW, Cammack J, Edwards C, Holgate AM, Cann PA, Brown C: Is the transit time of a meal through the small intestine related tO the rate at which it leaves the stomach? Gut 23:824-828, 1982
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