Gastric distension and gastric capacity in relation to food intake in humans

Physiology&Behavior, Vol. 44, pp. 665-668. Copyright©PergamonPress pie, 1988.Printedin the U.S.A.

0031-9384/88$3.00 + .00

Gastric Distension and Gastric Capacity in Relation to Food Intake in Humans ALLAN GELIEBTER 3

Obesity Research Center, Department o f Medicine and Psychiatry St. Luke's-Roosevelt Hospital, New York, N Y 10025 and Department o f Psychology, Touro College, New York, N Y 10036

GELIEBTER, A. Gastric distension and gastric capacity in relation to food intake in humans. PHYSIOL BEHAV 44(4/5) 665-668, 1988.--Two studies were performed in the same subjects to explore the relationship between stomach capacity and food intake. In the first study, a balloon was passed orally into the stomach of four lean and four obese subjects before they ingested a liquid lunch meal. The balloon was filled with 0, 200, 400, 600, and 800 ml of water in a random sequence on different days. The balloon was kept inflated during ingestion then deflated and removed. Food intake was significantly reduced (p<0.01) by a balloon volume of ~>400ml. In the second study, another balloon was inserted into the stomach of these subjects to estimate stomach capacity. The balloon was gradually filled at the rate of 100 ml/min with 30 sec pauses. The subjects rated their discomfort as 1 to 10, from no discomfort to extreme discomfort. A rating of 10 was the main index for stomach capacity. Mean capacity (ml) for the lean subjects was 1100+185 (SE) and for the obese 1925_+175 (SE), t=3.24, p<0.02. When stomach capacity from the second study was correlated to spontaneous food intake at 0 balloon volume from the first study, r=.44, n.s. However, the relationship between stomach capacity and the balloon volume needed to suppress 50% of spontaneous intake was significant, r= .66, p<0.05. This may have implications for treatment of obesity with a gastric balloon. Obesity

Stomach distension

Stomach capacity

Food intake

SOME subjects report feeling full when their stomach is distended with a balloon (2,7). However, the volume required to induce fullness has not been measured, and the direct effect on food intake has not been assessed (1,11). Therefore, in the first study, the effect of gastric distension on spontaneous food ingestion in both lean and obese subjects was determined. In the second study, the capacity of the stomach in these subjects was estimated.

Appetite

Obesity treatment

Satiety

troesophageal junction by filling it with 100 ml of water and withdrawing until resistance was felt. The balloon was then emptied, passed down another 2 cm, and fixed in place by taping the exterior tubing to the cheek and shoulder of the subject. The tube led behind the subject's back to two 60 ml syringes in series. This tube was also connected in parallel with a pressure transducer, linked to a recorder. The balloon was filled with 0, 200, 400, 600, or 800 ml, in a random sequence on alternate days. The rate off'filing was 100 ml/min with 30 sec pauses for measuring intragastric pressure. The balloon remained at the designated volume during subsequent meal consumption and was then deflated and withdrawn after the subject finished the meal. On another day at the end of the study, the balloon was f'flled with 800 ml and then deflated before the meal was ingested. In two lean subjects it was filled with 600 ml because 800 ml had previously caused them discomfort. Subjects were unaware of the balloon volumes used. The subjects ingested a nutritionally complete liquid meal (Sustacal, 1 kcal/ml) by straw from a concealed container.

STUDY 1 METHOD Four normal weight and four overweight subjects equally distributed by sex participated in the study. The characteristics of the subjects are shown in Table 1. Subjects fasted from 9 p.m. the previous evening and had a small standard breakfast in our laboratory the next morning. After 3 hours, a latex gastric balloon (4 in. section of Trojan condom) attached to a tube was inserted orally into the stomach. The balloon was retracted to the gas-

1The author is indebted to Sandra Westreich for technical ass/stance. ~Fhe study was sup'ported in part by The St. Luke's-Roosevelt Institute for Health Sciences. aRequests for reprints should be addressed to Dr. Allan Geliebter, St. Luke's-Roosevelt Hospital, WH-10, Amsterdam Ave. and 114th St., New York, NY 10025.

665

666

GELIEBTER TABLE1 SUBJECT CHARACTERISTICS Subject

Weight Type

Sex

Age

Height (m)

Weight (kg)

Deviation* (%)

1 2 3 4 5 6 7 8

obese obese obese obese lean lean lean lean

M M F F M M F F

30 21 34 20 26 18 27 23

1.79 1.73 1.64 1.60 1.68 1.78 1.60 1.66

91.8 95.9 94.1 77.7 65.5 77.7 53.2 56.8

28 45 68 47 6 11 0 -2

*Deviation from expected average weight for a given sex, age, and height (8). IOOO

2400

800

2000 J

600

E

400

"U

2

1600

,,=

m

0

1200

200

0

I I 0

, 200

, 400

, OOO

' 800

-:'

* Inflate/ Deflate

Balloon Volume (ml) FIG. 1. Mean intakes in obese and lean subjects were significantly reduced (p<0.01) by a balloon volume of 400 ml or more. Differences between obese and lean subjects were not significant. Inflation to maximal volume followed by deflation resulted in intakes no different than 0 balloon volume.

They received their preferred flavor, vanilla or chocolate, throughout the study. They were asked to ingest the liquid meal until satiated and not ot eat anything for 3 hours afterwards. They remained unaware that food intake was measured.

Statistics Data were treated with analysis of variance for repeated measures with post hoe tests by Newman Keuls (12).

"-

800

-~u" 03

~

400

Lean

Obese

FIG. 2. Obese subjects had a significantly larger stomach capacity than lean subjects (p<0.02) using a criterion of a discomfort level of 10.

food intake after inflation to maximum volume and deflation was comparable to that after 0 volume. Excluding the inflate-deflate condition, a line of regression was calculated for the mean values of the obese and lean subjects, which showed that for each ml of balloon distension, 0.4 ml of food intake was reduced. STUDY 2 METHOD

RESULTS The greater the balloon volume the smaller the food intake (see Fig. 1) with a volume of 400 ml or more producing a significant decrease in food intake, F(5,20)=4.5, p<0.01. There were no significant differences between lean and obese subjects, F(1,4)=0.04, n.s., nor between the males and the females, F(1,4) = 2.2, n.s. None of these interactions was significant, F(5,20)= 1.3, n.s. There was also no significant difference in meal duration, F(5,20)=0.7, n.s., which averaged 3.3 min. There was an insignificant rise of intragastric pressure during balloon inflation (1 cm H20/300 ml) and during subsequent meal consumption (1 cm H20/420 ml). Mean

The same subjects participated in a separate study to measure gastric capacity. They reported to the lab between 12 and 2 p.m. after not having eaten since 9 p.m. the previous evening. The same balloon was then inserted into the stomach and inflated at the rate of 100 ml/min with 30 sec pauses for measuring intragastric pressure. Before and after each 100 ml of inflation, the subjects rated their hunger, satiety, nausea, and discomfort on scales ranging from l - - n o t at all, to 10---extreme. Balloon inflation ended when the subject rated discomfort as 10. After 2 minutes, balloon deflation began and proceeded at the same rate. The balloon was then withdrawn.

GASTRIC D I S T E N S I O N A N D GASTRIC C A P A C I T Y

667

2000

2000-

"E

1600

1600-

E =

1200

A

> u

"E

o

E

.:.:.:.:.:.:.:.:.:.:-:.:-

!!!!!!!!!!!!

800

4) v. 0 ,..... e-

12000

800-

iiiiiiiiiiiiiiiiiililili !:i!i:!i:!i:!i:!i:!i:!i:!i:!i:!i:!ii!i

400

400 -

••...........:....

0

Obese

Lean

FIG. 3. Obese subjects had a significantly larger stomach capacity than lean subjects (p<0.05), using an intragastric pressure rise of 5 cm H20 as a criterion.

1U .E

I~ltl~ I.l.101m I I~'iolL,*. l

l

8

t~

: : Obese ~----OLean

.....'""

°°.°''""~f'°'"*'"*"""°*"°"°""'"'*'*"

............

[]

•

•

D

r • .44

I

I

I

I

I

I

400

800

1200

1600

2000

2400

Gastric

Capacity (ml)

FIG. 4. Relationship between spontaneous food intake at 0 balloon volume and gastric capacity in the same subjects. The correlation did not reach statistical significance. It can be seen that the obese subjects overall have a larger gastric capcity than the lean subjects (p
6 ¢ 0

~E 0 U

4 0 -'''''~

2

0

I

t

I

I

I

0

200

400

600

800

Balloon Volume (ml) FIG. 5. Mean discomfort ratings in obese and lean subjects as a function of balloon volume from 0 to 800 ml. The mean changes in ratings were not significant. The main index for stomach capacity was the volume reached when the subject rated discomfort as 10. Another index was the volume reached for a given pressure rise, such as 5 cm H20. Statistics

Groups were compared with analysis of variance. Correlations were done with Pearson's r.

extended to 11 subjects, five lean and six obese: mean gastric capacity (ml) for o b e s e = 1 9 2 0 - 1 3 6 (SE), and for lean= 1017_+ 154 (SE), F(1,9)= 19.4, p<0.002. Satiety ratings generally tracked the discomfort ratings and reached the maximum of 10 at a lower volume than the volume producing maximal discomfort. This suggests that satiety is related to gastric capacity. When we compare the intake from the first study at 0 balloon volume with gastric capacity from the second study, r=.44, n.s. (Fig. 4). F o r each subject, the balloon volume needed by linear regression to suppress 50% of the intake after 0 balloon volume, correlated with gastric capcity, r= .66, p<0.05. To determine the possible role of discomfort in producing food-intake suppression in the first study, I examined the discomfort ratings in the second study for the same balloon volumes of 0, 200, 400, 600, and 800 ml (Fig. 5). The mean rise in discomfort was from 1.8 at 0 balloon volume to 3.1 at 800 ml volume, a small nonsignificant rise (t =2.1, n.s.). At a balloon volume of 400 ml when food intake was already significantly lower than at 0 balloon volume, the mean discomfort rating was only 2.2, as compared to 1.8 at 0 balloon volume (t= 1.6, n.s.). The overall correlation coefficient between discomfort rating and food intake was not significant (r=.4, n.s.).

RESULTS

The mean volume needed to reach subjective capacity was significantly larger for the obese than for the lean subjects, F(1,6)=10.2, p<0.02, as shown in Fig. 2. The mean change in intragastric pressure at this volume was not significantly different between lean and obese subjects, 7.2 cm H20, F(1,6)=2.8, n.s. When a 5 cm rise in intragastric pressure is used as a criterion for capacity, the mean volume required to produce this pressure was also significantly greater for the obese, F(1,6)=6.0, p<0.05, Fig. 3. Although capacity was larger for the men than for the women, it was not significant, F(1,6)=0.7, n.s. The results have now been

DISCUSSION

In Study 1, gastric distension reduced subsequent food intake with an efficiency of about 40%. Thus distension may contribute partly to satiety. Discomfort was apparently not a factor in food-intake suppression because the discomfort ratings neither increased significantly nor correlated significantly with food intake as determined from Study 2. Gastric emptying rate was not a major factor because even an 800 ml balloon volume did not significantly slow emptying during a meal ingestion period (3). The most likely mechanism for suppression of food intake involved stimulation of gastric

668

GELIEBTER

stretch receptors which transmit signals via the vagus to the hypothalamus (9,10). The failure of maximal distension and deflation before the meal to suppress subsequent intake suggests a fast-acting neural signal. In Study 2, obese subjects had a much larger gastric capacity than lean subjects. It is unlikely that this was due to greater pain tolerance by the obese since measures based on the rise of intragastric pressure, which is not subjective, also showed a larger gastric capacity in the obese. Similar findings showing a larger capacity in extremely obese patients have been reported in Sweden (6). Although the obese had a larger capacity, they did not ingest more liquid lunch than the lean in the first study when balloon volume was 0. This is consistent with the nonsignificant correlation observed between capacity and intake.

The correlation between gastric capacity and the balloon volume needed to suppress 50% of spontaneous intake was significant. A larger balloon volume was therefore needed to reduce intake by a certain percent in subjects with a large capacity. This suggests that in treatment of obesity with chronic gastric balloons, larger balloon volumes may be required for subjects with a bigger stomach capacity (4,5). CONCLUSION Gastric distension by balloon significantly reduced food intake in both lean and obese subjects. The obese subjects had a significantly larger stomach capacity than the lean subjects. Suppression of food intake in the obese with a gastric balloon, taking into account gastric capacity, deserves further investigation.

REFERENCES 1. Aune, S. Intragastric pressure after vagotomy in man. Scand. J. Gastroenterol. 4:447--452; 1969. 2. Boring, E. G. The sensations of the alimentary canal. Am. J. Psychol. 26:1-57; 1915. 3. Geliebter, A.; Westreich, S.; Hashim, S. A. Intragastric balloon induced reduction of test meal intake. Fed. Proc. 44:1502; 1985. 4. Geliebter, A.; Gage, D.; Westreich, S.; McCray, R.; Hashim, S. A. Effects of intragastric balloon on body weight, food intake, and gastric emptying rate. Ann. NY Acad. Sci. 499:324-326; 1987. 5. Geliebter, A.; Westreich, S.; Hashim, S. A.; Gage, D. Gastric balloon reduces food intake and body weight in obese rats. Physiol. Behav. 39:399-402; 1987. 6. Granstrom, L. ; Backman, L. Stomach distension in extremely obese and in normal subjects. Acta Chir. Scand. 151:367-370; 1985.

7. Hertz, A. F. The alimentary canal in health and disease. Lancet i: I051-1056; 1911. 8. Metropolitan Life Insurance Company. Metropolitan life insurance height and weight tables. Statist. Bull. 64:2-9; 1983. 9. Paintal, A. S. A study of gastric stretch receptors. Their role in the peripheral mechanism of satiation of hunger and thirst. J. Physiol. 126:255--270; 1954. 10. Sharma, K. N.; Anand, B. K.; Dua, S.; Singh, B. Role of stomach in regulation of activities of hypothalamic feeding centers. Am. J. Physiol. 201:593-598; 1961. 11. Villar, H. V.; Wangenteen, M. D.; Burks, T. F.; Patton, D. D. Mechanisms of satiety and gastric emptying after gastric partioning and bypass. Surgery 90:229-236; 1981. 12. Winer, B. J. Statistical principles in experimental design. New York: McGraw-Hill; 1971.