The Effect of Sham Feeding on the Secretion and Motility of Canine Duodenal Pouches

The Effect of Sham Feeding on the Secretion and Motility of Canine Duodenal Pouches

G.-\Sl'ROENTEROLOGY Copyright Vol. 51, No.2 Printed in U.S.A. © 1966 by The Williams & Wilkins Co. THE EFFECT OF SHAM FEEDING ON THE SECRETION AND...

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G.-\Sl'ROENTEROLOGY

Copyright

Vol. 51, No.2 Printed in U.S.A.

© 1966 by The Williams & Wilkins Co.

THE EFFECT OF SHAM FEEDING ON THE SECRETION AND MOTILITY OF CANINE DUODENAL POUCHES R . M. PRESHAW, M.D.,

AND

R . SELLE

KNAUF,

M.D.

Department of Experimental Surgery, McGill University, Montreal, Canada

In decerebrate or decapitate cats prolonged excitation of the vagus nerve above the diaphragm causes a secretion from the duodenum, principally from that area containing the Brunner's glands. 1 • 2 Florey and Harding-a were unable to obtain an increase in secretion when food was offered to a hungry cat equipped with a duodenal fistula, and this appears to be the only recorded attempt to demonstrate a psychic phase of duodenal secretion. Experiments are described in this report in which the effect of sham feeding was observed on the secretion and motility of vagally innervated pouches of the first part of the duodenum in dogs, and compared 1rith the responses obtained after simple feeding of a meat meal.

Methods Three mongrel dogs, weighing from 14 to 17.5 kg, were provided with an esophagostomy by the method of Olbe. 4 At the same operation a pouch was made of the first portion of the duodenum in the manner described by Wright et al. 2 A double mucosal diaphragm was constructed exactly at the pylorus through an incision on the greater curvature border of the pyloric gland area of the stomach : the duodenum was transected 1 em above the entrance of the common bile duct into the duodenal wall, and closed distally. The small duodenal pouch was drained to the exterior by a mucocutaneous fistula, and intestinal continuity was restored by gastroReceived January 3, 1966. Accepted March 14, 1966. Address requests for reprints to: Dr. R . M. Preshaw, Department of Experimental Surgery, Donner Building, McGill University, Montreal 2, Quebec, Canada. This study was supported by Grant M.B.T. 775 from the Medical Research Council, Ottawa. The authors thank Miss Daphne Lan g for expert technical assistance.

jejunostomy. At a second operation a metal cannula (internal diameter, 2.0 em) was placed in the most dependent portion of the stomach to form a gastric fistula (fig. 1). Three weeks were allowed for recovery from these procedures before experiments were started. After an overnight fast of 18 hr, gastric and duodenal juices were collected by gravity drainage for 60 min to confirm basal levels of secretion. Sham feeding was perfonned with 200 g of homogenized cooked meat; this was repeatedly consumed over a period of exactly 20 min. The secretion from the duodenal pouches was also measured after feeding a standard meal of 600 g of proprietary tinned dog food (Dr. Ballard's Animal Foods, Ltd., :i'viontreal); in these eJqJeriments the gastric and esophageal cannulas were closed throughout. The responses to feeding and sham feeding were followed for 150 min. A control experiment was performed in which gastric and duodenal juices were collected for 210 min without stimulation. The volume of gastric and duodenal juice was measured at 15-min intervals. The concentration of acid in gastric juice was determined by titrating 1.0-ml samples with 0.1 N sodium hydroxide, using phenolphthalein as an indicator (end point pH 8.2 to 10.0). The output of acid is given in milliequivalents secreted per 15 min. Samples of both gastric and duodenal juice were deep-frozen within 1 hr after collection for estimation of pepsin-like activity by the method of Hunt. • The juice collected from the duodenal pouches has a constant concentration of bicarbonate at about 20 to 40 mEq per liter, 6 and it was found that the addition of 0.1 N hydrochloric acid to the duodenal juice in the ratio 1 : 1 would result in a mixture of pH 2.0 to 2.2; this was then used to determine pepsin-like activity exactly as described by Hunt for pure gastric juice. In 10 pairs of duplicate samples of duodenal juice, the standard deviation of the difference between paired samples was 0.7 pepsin units per ml. The output of pepsin is given in units secreted per 15 min. · The motility of the duodenal pouch was recorded after sham feeding and simple feeding, 193

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PRESHAW AND SELLE KNAUF

sham feeding and the means of the corresponding control collections were compared by the 1\'IannWhitney U-test. 8 Results Gastric

L ~i
Duodenal pouch

FIG. 1. Diagram of surgical preparation. The animals also had an esophagostomy.

using a small latex balloon (8 by 4 mm) filled with saline; the balloon was maintained within the lumen of the pouch by hand. This was connected to a pressure transducer (Sanborn no. 267B) by a saline-filled polyethylene tube with an internal diameter of 2.2 mm. Pressure changes were recorded by a Sanborn amplifier-recorder (model 321). Recordings were made for a basal period of 20 min, and then simple feeding or sham feeding was carried out exactly as described above: the response was followed throughout the period of feeding and for at least 20 min after feeding was completed. In these experiments sham feeding was performed with the gastric cannula draining freely, but no attempt was made to collect either gastric or duodenal juices; during the response to simple feeding the gastric cannula was closed. The pressure recordings were divided into 5-min periods and analyzed by a method similar to that described by Hightower and Code.7 It was found that apparent small increases in pressure were caused by movements of the animal, and these could not be distinguished from true changes in pressure within the pouch. To obviate this difficulty, pressure waves with an amplitude below 15 mm of mercury were ignored, and flu ctuations in the base line were also disregarded. The percentage of time occupied during each 5-min period by pressure waves greater than 15 mm of mercury was calculated, and the sum of the amplitudes (millimeters of mercury) of complexes higher than 15 mm of mercury was measured for each 5-min period. The results of the studies on secretion from the gastric fistula and the duodenal pouch have been presented in the form of graphs of the mean values obtained in all e},:periments. The differences between the means of the volume and pepsinlike activity of duodenal juice secreted after

Sham feeding. Sham feeding caused a marked increase in the output of acid and pepsin by the stomach (fig. 2), which " ·as still greater than control levels 150 min after feeding. The volume and the output of pepsin-like activity from the duodenal pouch \Yere transiently increased by sham feeding, but returned to control levels within 30 min (fig. 2). The difference between the means of the first collection after sham feeding and the corresponding control collection \YaS significant for volume (difference, 0.61 ml ; U = 6; P < 0.01), but hardly significant for pepsin output (difference, 2.0 units; U = 15; 0.1 > P > 0.05). The concentration of pepsin-like activity in duodenal juice \YUS not appreciably altered by sham feeding. The effect of sham feeding on the motility of the duodenal pouch was more complex. In 7 out of 12 experiments sham feeding caused an immediate rise in duodenal motor activity, which was still evident as long as 90 min after feeding (fig. 3). In four experiments (in two dogs) no increase in activity was apparent during the actual period of sham feeding, but motility increased shortly after sham feeding was completed : an example of this type of response is shown in figure 4. In one experiment sham feeding was without any obvious effect on duodenal motility. Table 1 gives a summary of the observed changes in pouch motility after sham feeding. Simple feeding . A meat meal caused an increase in the rate of secretion of duodenal juice and an increase in the output of pepsin-like activity (fig. 5) . The rate of secretion reached a peak of 1.8 ml per 15 min (sEM, 0.4 ml). The peak rate after sham feeding was 1.0 ml per 15 min (SEM, 0.1 ml). Simple feeding caused an increase in motor activity of the duodenal pouch in each of six experiments (table 1 and fig. 6). Discussion

Savitch and Sochestvensky1 recorded that electrical vagal stimulation caused a secre-

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DUODENAL MOTILITY AFTER SHAM FEEDING

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tion from the upper small intestine in cats. This was confi1~med by Wright et al.,2 who showed that the secretion came mainly from that area of duodenum containing the Brunner's glands. These workers also found histological evidence of depletion of the mucous content of · Brunner's glands after vagal stimulation: · In the present study we have shown that sham feeding causes a small but definite secretion from vagally innervated pouches of the first part of the duodenum in dogs; this is perhaps the first demonstration of a cephalic phase of duodenal secretion. Our results do not allow any conclusions about the mechanism of the increase in secretion after sham feeding, but it would appear likely to be caused by vagal impulses. The secretory response of the duodenal pouches to simple feeding of a meat meal was considerably greater than the response to sham feeding and lasted for more than 15

min. This is similar to the responses described by others for duodenal pouches in dogs. 6 Although traces of various enzymatic activities were found in duodenal juice by several earlier workers, ·wright et al. 2 could not demonstrate any activity when precautions were taken to collect pure duodenal secretion. However, Cooke and Grossman (unpublished data) have shown that small amounts of pepsin-like activity can be detected in duodenal juice, and the output of this substance is increased after feeding. We have confirmed these findings, and have shown further that there is a small, barely significant rise in the output of pepsin-like activity after sham feeding. This contrasts with the large increase in the output of pepsin by the stomach after sham feeding in the same animals (fig. 2), and suggests that the output of pepsin-like substances from

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PRESHA.TF A.ND SELLE KNA.UF

Vol. 51, So. ?.

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SHAM FEEDING

SHAM

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TIME IN MINUTES

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the duodenum is not under the control of the parasympathetic nervous system to the same extent as the pepsin secretion from the gastric glands. The effect of sham feeding on duodenal motility has not been previously recorded. Electrical vagal stimulation generally causes

an increase in upper small intestinal mo· tility. 9 -i.l In some experiments Bayliss and Starling12 noted inhibition of duodenal motility during the period of vagal stimula· tion in anesthetized dogs, followed by aug· mentation of activity when the stimulus was removed. This is similar to the response

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DUODENAL MOTILITY AFTER SHAM FEEDING 1. lvfean duodenal pressure wave activity per 5-min period (wave complexes greater than 15 mm of mercury only)

TABLE

Standard meal c

Sham feeding" 5-min period b % of time

Sum of amplitudes

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Sum of amplitudes

mm;Hg

8.1 10.7 6.8 7. 3

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17.6 16 .8 13 .5 15.1 15 .5

470 260 300 345

(235) (80) (110) (155)

830 860 665 620 825 510 800

(205) (225) (150) (140) (220) (125) (180)

mmHg

1 2 3 4 Feeding started 5 6 7 8 9 10

12.1 10.5 8.2 7.4

(3.2) (1. 1) (2.2) (2. 3)

760 540 410 350

(170) (160) (150) (145)

21. 1 20.3 19.5 24.1 22.1 20.6

(4.7) (3 .6) (3.7) (4.6) (4.8) (2.8)

1560 1325 1575 1310 750 1240

(570) (340) (510) (315) (145) (280)

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Vol. 51, No. 2

PRESHAW AND SELLE KNAUF

DOG ~95

FED 600 g MEAT

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+12

+13 TIME

+35 IN

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MINUTES

FIG. 6. Tracing from duodenal pressure recording after a meat meal.

observed occasionally in the present study after sham feeding (fig. 4). It is of interest that sham feeding has been shown to cause inhibition of motility in both the body of the stomach and the pyloric gland area in dogs.I3, I4 Fogelson and Bachrach15 have suggested that the juice secreted from duodenal pouches might be secondary to increased motility. This difficulty has been fully discussed elsewhere. 6 In the present study sham feeding generally caused an increase in duodenal motility, and it is therefore not possible to exclude that the brief secretory response to sham feeding might be entirely secondary to the increase in motility of the pouch. Summary

The effect of sham feeding has been observed in dogs with a vagally innervated pouch of the first part of the duodenum and a gastric fistula. Sham feeding caused a small and transient increase in secretion from the duodenal pouch, and also an increase in the motor activity of the pouch. The secretory response of the duodenal pouch to a meat meal was greater than the response to sham feeding, and was also

associated with an increase m motor activity. REFERENCES 1. Savitch, V. Y ., and N . A. Sochestvensky . 1917. L 'influence du nerf vague sur Ia secretion d 'intestine. C. R . Soc. Bioi. (Paris) 80: 508509. 2. Wright, R. D., M.A. Jennings , H. W . Florey, a nd R. Lium. 1940. The influence of nerves and drugs on secretion from the small intestine and a n investigation of the enzymes in intestinal juice. Quart. J. Exp. Physiol. 30: 73-120. 3. Florey, H. W., and H. E. Harding. 1935. The nature of the hormone controlling Brunner 's glands. Quart . J. Exp. Physiol. 25: 329-339. 4. Olbe , L. 1959. Esophageal cannula dog, a simple mode of preparation for sham feeding experiments. Gastroenterology 37: 460--462. 5. Hunt, J. N . 1948. A method for estimating pepsin activity in gastric contents. Biochem. J . 42: 104-109. 6. Grossman, M. I. 1958. The glands of Brunner. Physiol. R ev. 38: 675-690. 7.- Hightower, N.C ., and C . F. Code. 1950. The qu antitative analysis of antral gastric motility records in normal human beings, with a study of the effects of neostigmine. Proc. Mayo Clin. 25: 697-704. 8. Siegel S. 1956. N onparametric statistics for

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9.

10.

11.

12.

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DUODENAL MOTILITY AFTER SHAM FEEDING

the behavioural sciences. McGraw-Hill Book Co. ; Inc. , New York. Harper, A. A., C. Kidd, and T. Scratcherd. 1959. Vagovagal reflex effects on gastric and pancreatic secretion and gastrointestinal motility. J. Physiol. (London) 148: 417-436. van Harn, G. L. 1963. Responses of muscles of cat small intestine to autonomic nerve stimulation. Amer. J. Physiol. 204: 352-358. Kewenter, J. 1965. The vagal control of the jejuna! and ileal motility and blood flow. Acta Physiol. Scand. 65: Suppl. 251. Bayliss, W. M., and E. H. Starling, 1899. The

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movements and innervation of the small intestine. J. Physiol. (London) 24:99- 143. 13. Lorber, S. H., S. A. Koma rov, and H. Shay. 1950. Effect of sham feeding on gastric motor activity of the dog . Amer. J. Physiol. 162 : 447-451. 14. Olbe, L., and B. J acobson. 1963. Intraluminal pressure waves of the stomach in dogs studied by endoradiosondes. Gastroenterology 44: 787- 796. 15. Fogelson, S. J., and W. H. Bachrach. 1939. Response of Brunner's glands to secretin. Amer. J. Physiol. 128: 121-123.