intragastric pressure, and gastric emptying rate. ALLAN GELIEBTER, SANDRA WESTREICH, RICHARD N. PIERSON, JR., AND. THEODORE B. VAN ITALLIE.
Extra-abdominal pressure alters food intake, intragastric pressure, and gastric emptying rate ALLAN GELIEBTER, THEODORE B. VAN
SANDRA ITALLIE
WESTREICH,
RICHARD
N. PIERSON,
JR., AND
Obesity Research Center, Department of Medicine, College of Physicians and Surgeons, Columbia University at St. Luke’s-Roosevelt Hospital Center, New York 10025; and Department of Psychology, Tour0 College, New York, New York 10036
GELIEBTER, ALLAN, SANDRA WESTREICH, RICHARD N. PIERSON, JR., AND THEODORE B. VAN ITALLIE. Extru-abdominal pressure alters food intake, intragastric pressure, and gastric emptying rate. Am. J. Physiol. 250 (Regulatory Integrative
Comp. Physiol. 19): R549-R552, 1986.-Compression of the animal stomach gives rise to vagal discharges that could signal satiety. To test a noninvasive method of inducing compression of the human stomach, we first employed extra-abdominal pressure levels of 0, 10, and 20 Torr, counterbalanced for sequence, in six lean and obese subjects. A large blood pressure cuff was wrapped around the abdomen of the subject with the air bladder over the epigastrium. The bladder was inflated before ingestion of a liquid meal by the subject until satiated. Relative to 0 Torr, pressures of 10 and 20 Torr significantly reduced spontaneous food intake (P c 0.03) without producing discomfort. In a second study, extra-abdominal pressure of 20 Torr also raised intragastric pressure by a mean of 5.5 Torr (P < 0.03). In a third study, extra-abdominal pressure of 20 Torr did not alter gastric emptying rate during meal ingestion but ultimately enhanced emptying rate when this pressure was maintained for >lOO min after meal completion (P < 0.01). externally applied pressure; stomach; lean and obese subjects SATIETY IS SIGNALLED in part by the mechanical state of the stomach (5). Compression and distension of the animal stomach excite gastric receptors that result in increased vagal activity (2, 14, 22), which can activate neurons in the ventromedial nucleus of the hypothalamus (1,23, 24). Compression of the animal stomach also raises intragastric pressure (14, 22) associated with increased tension of the stomach wall (11). Indirect compression of the stomach by injecting air into the abdominal cavity of the dog induces a proportional rise in intragastric pressure (26). Raising intragastric pressure in the dog by increasing intragastric volume accelerates gastric emptying (25), which has been implicated as a satiety factor (12,19). Applying external pressure to the abdomen can raise intragastric pressure in humans (4, 6), but the effect on gastric emptying is not known. Surgery to reduce stomach capacity leads to decreased food intake and body weight in obese patients (17) but with significant risk of morbidity and mortality (7). A less invasive method to limit gastric capacity involves indirect compression of the stomach with extra-abdominal pressure. We applied extra-abdominal pressure to
determine the effects on spontaneous food intake, intragastric pressure, and gastric emptying rate in humans. GENERAL
METHODS
Subjects. Subjects were healthy without symptoms of gastrointestinal disease and not dieting. Each experiment involved six subjects, age 20-53 yr, equally represented by sex, half of whom were lean and half obese, 20% above desirable weight (3). Subjects were paid for each session. The study protocols and consent forms were approved by the Institutional Review Board of St. Luke’s-Roosevelt Hospital Center. Procedure. Subjects did not eat before breakfast or between breakfast and the test meal. They ate a standard breakfast (250 g of apple juice and a buttered English muffin) in our appetitive behavior laboratory. A comparable breakfast left almost no residue in the stomach 23 h later, as after an overnight fast (20). Our subjects returned 3.5 h later to consume the test meal, a liquid lunch consisting of Sustacal (Mead Johnson), a nutritionally complete food (5.6% protein, 2.1% fat, 13% carbohydrate, 78% water, and 0.9% ash by weight) with a density of 1.07 g/ml and an energy value of 1 kcal/ml. This meal was ingested through a straw from a concealed reservoir (8a). All subjects had originally rated the food as at least 6 out of 10 on a scale of l-10 where 1 is extremely bad, 10 is extremely good, and 5 is fair. Subjects were asked not to wear any restrictive clothing and to remove belts before ingestion of the meal. Then a large (20 x 152 cm) specially modified thigh blood pressure cuff (Baum) linked to a mercury manometer was wrapped around the abdomen with the air bladder (19 X 38 cm) on the epigastrium extending from the left midaxillary line laterally to the midsternal line medially and from the xiphisternum down to the umbilicus. The air bladder position and dimensions were chosen to cover completely the region over the stomach. A specific level of pressure, 0, 10, or 20 Torr (1 Torr = 1 mmHg), was then applied throughout the period of meal ingestion. The food was served at a temperature of 6”C, and the reservoir was weighed before and after food consumption. The subject maintained a seated position with minimal movement during meal ingestion. Pressure measurements and meal duration were recorded by the experimenter, who sat behind the subject and out of view. The
0363-6119/86 $1.50 Copyright 0 1986 the American Physiological
Society
R549
R550
EXTRA-ABDOMINAL
PRESSURE
AND FOOD INTAKE
passed orally into the stomach and inflated with 100 ml of air. The tube was retracted until the balloon met resistance at the cardia and was passed down 2 cm to allow slack. The tube was then taped to the cheek and shoulder of the subject to secure its position. The distal end of the tube was attached to a Statham transducer linked to a Sanborn dual-channel carrier-amplifier recorder. Subjects participated in two sessions that were counterbalanced for sequence. In one, extra-abdominal pressure (20 Torr) was applied, in the other it was not. EXPERIMENT 1. SPONTANEOUS FOOD INTAKE During each session the subject ingested 500 ml of SusProcedure. Extra-abdominal pressure levels of 0, 10, tacal at a steady rate of 100 ml/min as directed by the experimenter, who monitored the disappearance of liquid and 20 Torr were applied in a repeated randomized food from a concealed graduated container. sequence on different days for each subject. Subjects Results. When extra-abdominal pressure of 20 Torr were told that the main purpose- of the study was to was applied, intragastric pressure increased significantly detect expansion of the abdomen during meal ingestion by monitoring air bladder pressure, with several pressure by a mean of 5.5 Torr [F (1,4) = 11.0,P < 0.031 relative to the condition of 0 Torr pressure (see Fig. 2). Ingestion levels used to determine the one most sensitive to abdomof the liquid meal itself did not significantly [F (1, 4) = inal expansion. They were asked to ingest each lunch 0.3, NS] alter intragastric pressure when extra-abdomimeal from the reservoir until they felt full. The subjects nal pressure was applied or when it was not. food intake was measured. None rema ined unaware that spontaneously reported discomfort at any pressure level 3. GASTRIC EMPTYING RATE during experimental sessions and when questioned at the EXPERIMENT end of the study. Procedure. Subjects participated in two sessions counResults. As shown in Fig. 1, spontaneous food intake terbalanced for sequence. During one session extra-abwas inversely related to external pressure. Analysis of dominal pressure was applied (20 Torr); during the other variance for different pressure levels indicated signifino pressure was applied. In each session the subject cant differences [F (2, 8) = 6.0, P < 0.031between food consumed 500 ml of Sustacal over 5 min at a rate of 100 intake volumes. The pressures of 10 and 20 Torr each ml/min. The meal contained a tracer dose (150 mCi) of significantly (P < 0.05) reduced food intake by 14.6 and ggmTc-labeled sulfur colloid. The subject was seated in 18.4%, respectively, relative to base-line intake after 0 precisely the same position in both sessions next to a Torr pressure. These reductive effects were not statistiscintillation gamma camera (Siemens Mobile using a cally different from each other. Neither duration of meal, diverging collimator at a setting of 140 keV with a 15% 5.3 t 1.2 (SD) min [F (2,8) = 2.7, NS], nor ingestion window) positioned posteriorly to image the stomach for rate, 159 t 91.5 (SD) ml/min, [F (23) = 0.1, NS], was measuring gastric emptying (10). Cumulative radioactive significantly altered by application of pressure. counts were recorded by computer (DEC Gamma 11) every 2 min for 110 min, beginning 1 min before ingesEXPERIMENT 2. INTRAGASTRIC PRESSURE tion. A region of interest, region A, was determined Procedure. A small latex balloon (medium finger cot) during the fifth 2-min period, when counts were generally attached to a polyethylene tube (Salem Sump, 8 Fr) was subject was requested not to eat for 2 h after the test meal. Statistical art&&. Analysis of variance for repeated measures was used with post hoc analysis by the method of Newman-Keuls (27). The principal effect studied was within individuals, since subjects served as their own controls. When differences occurred between weight or sex groups they are noted. All P values are two tailed, with P < 0.05 for a considered significant.
850 750 n
F
E 650 z! 550 :0 P F -*v
250 1
0 Extra-obdominol
I
I
IO
20
Pressure ( mm Hg )
1. Test meal intake was signifcantly reduced when 10 and 20 Torr of extra-abdominal pressure (p < 0.03) were applied relative to 0 Torr. Closed ci&.es, lean subjects; open circles, obese subjects; X, mean values.
Extra-obdominol
FIG.
Pressure ( mm Hg )
2. Intragastric pressure was significantly (P c 0.03) increased when 20 Torr of extra-abdominal pressure was applied relative to 0 Torr, after ingestion of meal. Symbols are as in Fig. 1. FIG.
EXTRA-ABDOMINAL
PRESSURE
maximal, by programming the computer to include all pixels (each 0.9 x 0.9 cm in a 64 X 64 pixel matrix) ranging from 20 to 100% of the pixel with the highest counts. The air bladder completely covered the epigastric area corresponding to region A, which resembled the shape of the stomach. Region B, corresponding to the intestines, was chosen as a horizontal area below region A. To determine percent emptying that occurred during meal ingestion, counts from region B after meal ingestion were used as a proportion of the sum of region B and region A during the fifth period. To determine percent emptying after the meal, diminution of counts in region A from the fifth period were used. After correcting for isotope decay, half time for gastric emptying was obtained by determining the first period during which the number of counts from region A was less than half those of the fifth period. Results. During meal ingestion, application of external pressure did not significantly alter gastric emptying rate: 8.6 + 2.2% (SE) emptied when the pressure was 0 Torr andi2.4 t 3.1% emptied when pressure was 20 Torr [F (1, 4) = 2.8, NS]. Application of 20 Torr pressure after ingestion significantly accelerated emptying rate. As shown in Fig. 3, the mean half time beginning after ingestion was 78.3 min without pressure applied and 66.0 min with pressure applied [F (1, 5) = 19.8,P c 0.011. DISCUSSION
Application of two levels of moderate pressure to the epigastrium reduced spontaneous food intake. Garrow and Gardiner (8) observed that a nylon cord tied around the abdomen can prevent weight regain in patients after weight loss because the cord tightens when weight is gained. The cord may also reduce intake during individual meals by exerting extra-abdominal pressure as the stomach fills. Externally applied pressure significantly raised intragastric pressure. This rise corresponds to an increase in
0 Extra-obdominol
20
Pressure hn
Hg )
3. Half time for gastric emptying after meal ingestion was significantly (P c 0.01) reduced when 20 Torr of extra-abdominal pressure was applied relative to 0 Torr. Symbols are as in Fig. 1. FIG.
AND FOOD INTAKE
FE51
stomach wall tension, estimated to be proportional to the product of intragastric pressure and the square root of volume (11). Intragastric pressure did not rise significantly during meal consumption in experiment 2 because the meal was easily accommodated by the stomach. Lorber and Shay (16) observed a mean rise of only 0.4 Torr after subjects swallowed 250 ml of a water-barium emulsion. With ingestion of larger volumes of liquid food, we have observed progressive rises in intragastric pressure: for 1,000 ml, 1.5 Torr, and for 1,500 ml, 3 Torr. These increases remain small because the gastric musculature relaxes as more material enters the stomach (9,15). Thus a rise in intragastric pressure may, act as a satiety signal only after large intakes or after compression of the stomach. The mean rate of caloric emptying after ingestion with no external pressure applied was 3 kcal/min, close to what Hunt et al. (12) found, 5 kcal/min, for a liquid meal with the same caloric density of 1 kcal/ml. During meal ingestion the emptying rate averaged 8.6 kcal/ml, reflecting the more rapid early phase of emptying (18,21). Hunt et al. (12) and McHugh and Moran (19) proposed that gastric emptying rate plays a role in satiety. Meals that empty slowly from the stomach may induce earlier and longer lasting satiety than those that empty quickly. In our study there was no significant change in gastric emptying rate during the meal itself when extra-abdominal pressure was applied, suggesting that emptying rate during ingestion was not involved in altering satiety. However, with continued application of extra-abdominal pressure, gastric emptying rate was accelerated after meal ingestion. Previously, Strunz and Grossman (25) showed that gastric emptying rate in the dog could be enhanced after raising intragastric pressure by increasing intragastric volume. Hunt and MacDonald (13) demonstrated in humans that increasing meal volume enhanced emptying rate but did not measure intragastric pressure. Our results show that inducing a rise in intragastric pressure is sufficient to enhance emptying rate even when volume is not manipulated. By raising intragastric pressure the propulsive force promoting emptying is increased (25). Although extra-abdominal pressure reduced meal intake, long-term use of extra-abdominal pressure, as with an abdominal binder, may not reduce total daily food intake, since gastric emptying rate might be increased after individual meals, with earlier resumption of hunger triggering further ingestion (12). In summary, we found that extra-abdominal pressure significantly decreased test meal intake, increased intragastric pressure, and when maintained after meal ingestion enhanced gastric emptying rate. We thank Dr. Marvin Friedman, Division of Nuclear Medicine, for assistance in the gastric emptying studies and Dr. Donald P. Kotler, Division of Gastroenterology, for consultations. This research was supported in part by National Institute of Arthritis, Diabetes, and Digestive and Kidney Diseases Grant AM-2668702. Some of these data were presented at a meeting of the Eastern Psychological Association in April 1983. Address for reprint requests: A. Geliebter, St. Luke’s-Roosevelt
R552 Hospital, WH-1030, Amsterdam 10025.
EXTRA-ABDOMINAL
PRESSURE
Ave. and 114th St., New York, NY
Received 16 April 1985; accepted in final form 24 October 1985. REFERENCES B. K., AND R. V. PILLAI. Activity of single neurones in the hypothalamic feeding centres: effect of gastric distension. J. Physiol. Lond. 192: 63-77, 1967. 2. ANDREWS, P. L. R., D. GRUNDY, AND T. SCRATCHERD. Vagal afferent discharge from mechanoreceptors in different regions of the ferret stomach J. Physiol. Land. 298: 513-524, 1980. 3. BRAY, GEORGE 0. (Editor). Obesity in Perspective. Washington, DC: US Govt. Printing Office, 1975, vol. 2, part 1, p. 70-83. (Fogarty Int. Ser. Prevent. Med.) [DHEW Publ. (NIH) 75-7081 4. COHEN, S., AND L. D. HARRIS. Does hiatus hernia affect competence of the gastroesophageal sphincter? N. Ertgl. J. Med. 284: 1053-1056,197l. 5. DEUTSCH, J. A., M. F. GONZALEZ, AND W. G. YOUNG. Two factors control meal size. Bruin Res. Bull. 5, Suppl. 4: 55-57, 1980. 6. FISHER, R. S., L. S. MALMUD, G. S. ROBERTS, AND I. F. LOBIS. Gastroesophageal (GE) scintiscanning to detect and quantitate GE reflux. Gastroenterology 70: 301-308, 1976. 7. FREEMAN, J. B., AND H. BURCHETT. Failure rate with gastric partitioning for morbid obesity. Am. J. Surg. 145: 113-119, 1983. 8. GARROW, J. S., AND G. T. GARDINER. Maintenance of weight loss in obese patients after jaw wiring. Br. Med. J. 282: 858-860, 1981. 8&GELIEBTER, A. Effects of equicaloric loads of protein, fat, and carbohydrate on food intake in the rat and man. Physiol. Behau. 22: 267-273,1979. 9. GIANTURCO, C. Some mechanical factors of gastric physiology. Am. J. Roentgenol. 31: 735-744,1934. 10. HARVEY, R. F., D. G. MACKIE, N. J. G. BROWN, D. H. KEELING, AND W. T. DAVIES. Measurement of gastric emptying time with a gamma camera. Lzncet 1: 16-18, 1970. 11. HOPKINS, A. Relation between pressure and volume in hollow viscera. Gut 7: 521-524, 1966. 12. HUNT, J. N., R. CASH, AND P. NEWLAND. Energy density of food, gastric emptying, and obesity. Am. J. Clin. Nutr. 31: 5259-5260, 1978. 13. HUNT, J. N., AND I. MACDONALD. The influence of volume on gastric emptying. J. Physiol. Land. 126: 459-474, 1954. 1. ANAND,
AND FOOD INTAKE
14. IGGO, A. Tension receptors in the stomach and the urinary bladder. J. Physiol. Lond. 128: 593-607,1955. 15. KELLING, G. Untersuchungen uber die Spannungszustande der Bauchwand, der Magenund der Darmwand. 2. Biol. 44: 161-258, 1903. 16. LORBER, S. H., AND H. SHAY. Technical and physiological considerations in measuring gastrointestinal pressures in man. Gastroenterology 27: 478-487,1954. 17. MASON, E. E., K. J. PRINTEN, T. J. BLOMMERS, AND D. H. SCOTT. Gastric bypass for obesity after ten years experience. Int. J. Obesity 2: 197-206,1978. 18. MCHUGH, P. R. The control of gastric emptying. J. Auton. New. Syst. 9: 221-231, 1983. 19. MCHUGH, P. R., AND T. H. MORAN. Calories and gastric emptying: a regulatory capacity with implications for feeding. Am. J. Physiol. 236 (Regulatory Integrative Comp. Physiol. 5): R254-R260, 1979. 20. MILLER, M., H. Y. WISHART, AND W. S. NIMMO. Gastric contents at induction of anaesthesia. Is a 4-hour fast necessary? Br. J. Anuesth. 55: 1185-1187, 1983. 21. MOBERG, S., AND G. CARLBERG. Gastric emptying in healthy subjects and in patients with various malabsorption states. Scund. J. Gastroenterol. 9: 7-21, 1974. 22. PAINTAL, A. S. A study of gastric stretch receptors. Their role in the peripheral mechanism of satiation of hunger and thirst. J. Physiol. Lond. 126: 255-270, 1954. 23. SHARMA, K. N., B. K. ANAND, S. DUA, AND B. SINGH. Role of stomach in regulation of activities of hypothalamic feeding centers. Am. J. Physiol. 201: 593-598, 1961. 24. SHARMA, K. N., S. DUA-SHARMA, AND H. L. JACOBS. Electrophysiological monitoring of multi-level signals related to food intake. In: Neural Integration of Physiological Mechanisms and Behavior, edited by G. J. Mogenson and F. R. Calaresu. Toronto: Univ. of Toronto, 1975. 25. STRUNZ, U. T., AND M. I. GROSSMAN. Effect of intragastric pressure on gastric emptying and secretion. Am. J. Physiol. 235 (Endocrinol. Metab. Gastrointest. Physiol. 4): E552-E555, 1978. 26. WESLEY, J. R., R. DRONGOWSDI, AND A. G. CORAN. Intragastric pressure measurement: a guide for reduction and closure of the silastic chimney in omphalocele and gastroschisis. J. Pediutr. Surg. 16: 264-270,1981. 27. WINER, B. J. Statistical Principles in Experimental Design (2nd ed.). New York: McGraw-Hill, 1971.