Studies of Paralytic lleus Effects of lntraperitoneal

Injury on Motility of the Canine Small Intestine

Nand K. Mishra, MD, Toledo, Ohio Hubert E. Appert, PhD, Toledo, Ohio John M. Howard, MD, Toledo, Ohio

Although paralytic ileus is a major complication of injury, either traumatic or operative, and also results from other diseases, the actual conditions leading to ileus have not been studied systematically. The concept of ileus dates back to antiquity; however, its meaning has changed considerably over the years. Nearly all abdominal distention with vomiting was regarded by Hippocrates as ileus. Celcus, a distinguished Roman physician (14-37 AD), wrote, “in ileus from excess of pain patients earnestly desire death.” He thought ileus was a very painful condition associated with inflammation of the bowel. The modern concept of paralytic ileus differs from that of small bowel obstruction etiologically, clinically, and therapeutically. Paralytic ileus, as encountered in daily surgical practice, almost always occurs in association with other diseases or injuries; therefore, it is nearly impossible to recognize any single specific pathophysiologic cause of pure paralytic ileus in patients. For this reason the present investigation was undertaken to determine the specific conditions leading to ileus in dogs. Material and Methods Healthy dogs of either sex, weighing from 20 to 25 kg, were fasted for twenty-four hours before and after the

operative procedures but were allowed free access to water. In addition, the dogs received 1,500 ml of saline intravenously per day. Initially, the peritoneal cavity From the Departments of Surgery and Physiology, Medical College of Ohio at Toledo, Toledo, Ohio. This work was supported by a grant from the John A. Hartford Foundation, Inc. Reprint requests should be addressed to John M. Howard, MD, Medical College of Ohio at Toledo, PO Box 6190, Toledo, Ohio 43614.

~O~UTN128, May1875

was opened under aseptic conditions using intravenous sodium pentobarbital anesthesia. A fistula, extending from the intestinal lumen through the body wall, was created in the upper jejunum. A Thomas cannula was secured into the wall of the jejunum about 10 cm below the ligament of Treitz. The cannula was brought through the abdominal wall in a manner similar to that used in preparing dogs with duodenal fistulas [I]. The dogs were either allowed to recover for two weeks or used immediately. The fistula in the jejunum permitted introduction of a catheter into the small intestine. The catheter had a balloon and electrode attached to permit the simultaneous monitoring of mechanical and electrical activity of the intestine. The inside diameter of the catheter (Figure 1) measured 4 mm; the balloon had a capacity of 15 ml. The electrode consisted of silver-plated wire in strands with the insulation removed at a point in the middle of the balloon. The balloon was inflated with 5 to 10 ml of air. The distended intestine consistently showed mechanical activity and “slow” electrical waves having spike potentials during the control periods. Air was used to transmit the pressure from the balloon to a Statham pressure gauge. Electrical and mechanical recordings were made using a Grass polygraph recorder. Eight different procedures were employed to inhibit intestinal motility. Zntraperitoneal Gastric Juice. After cannulation, gastric juice was collected from dogs that had been fasted for twenty-four hours. Histamine (0.1 mg/kg of body weight) was administered subcutaneously at hourly intervals to stimulate gastric secretion. The four dogs receiving the intraperitoneal gastric juice were not anesthetized and had a jejunal fistula prepared as described previously. Gastric juice, 5 ml/kg, was administered intraperitoneally, and its effects on mechanical and electrical activity of the intestine were monitored. The dogs appeared to tolerate injection of the gastric juice with only moderate discomfort. The procedure was repeated on four consecutive days.

559

Mishra, Appert, and Howard

ity was monitored as described, immediately procedure and on four subsequent days. Partial Occlusion of the Superior

Figure 1. Balloon catheter and electrode assembly used to measure lntestlnal pressure and electrical actiwity. The TefIor@ insulation was removed from the wire at the point lndkated by the arrow. Gastric Perforation. A stab wound was made in the anterior wall of the stomach in six dogs anesthetized with sodium pentobarbital. A polyethylene tube, measuring 0.25 inches in inside diameter and 1.5 inches in length, was sutured into the gastric incision to prevent the omentum from sealing the perforation., While the gastroperitoneal fistula was created, a’Thomas cannula was placed in the upper jejunum, as in the previous series, to permit monitoring of electrical and mechanical activity of the intestine. Penicillin (1.0 million units) and streptomycin (1.0 gm) were administered intraperitoneally to reduce peritoneal sepsis. Intestinal motility was monitored as described previously. Appendiceal Ligation. The blood supply and base of the appendix were ligated in four dogs. At the time of ligation, a jejunal fistula was made for recording intestinal motility as in the previous experiments. The abdomen was closed and antibiotics were administered intraperitoneally as previously described. Intestinal motility was recorded immediately after the procedure and on each subsequent day. Zntraperitoneal Chemical Irritation. A fistula in the upper jejunum was prepared as described. The six dogs were allowed to recover for two weeks before further experimentation. Intraperitoneal irritation was produced by injecting 2 per cent iodine in 2 per cent potassium iodide solution, 1 ml/kg of body weight, according to the method of Douglas and Mann [z]. Electrical and mechanical activities of the intestine were monitored four hours subsequently as described previously. Intestinal motility was also studied on.the following day. Retroperitoneal Blood. Dogs were prepared with a Thomas cannula in the jejunum and allowed to recover for two weeks as before. The effects of retroperitoneal blood were studied in two dogs. The abdominal cavity was opened under aseptic conditions using sodium pentobarbital anesthesia, and 50 ml of blood was injected into the retroperitoneal area near the twelfth thoracic and first and second lumbar segments. Intestinal motil-

560

Mesenteric

after the Artery.

The peritoneal cavity was opened under aseptic conditions in four dogs. The lumen of the superior mesenteric artery was occluded to approximately half its diameter by a continuous suture extending over a 2 cm distance. At that time, a cannula was placed in the jejunum and intestinal motility was monitored immediately and on four subsequent days, as described previously. Mechanical and Thermal Peritoneal Irritation. Six dogs were prepared with a Thomas cannula in the jejunum as described. At the same time the dogs were subjected to intraperitoneal irritation. An area of parieta1 peritoneum, measuring 2 by 4 inches, ventral to each of the kidneys, was burned with a Boviee electrocautery. In addition, the intestinal wall and parietal peritoneum were abraded with dry gauze. Intestinal motility was monitored on the same day and five subsequent days. The dogs were sacrificed on the fifth day. At that time the small intestine was divided into three parts by placing ligatures at the beginning and end of the duodenum, midway between the ligament of Treitz and the ileocecal valve, and at the ileocecal valve. The fluid in each part of the intestine was collected and measured. Results Intraperitoneal Gastric Juice. In this series of experiments temporary inhibition of intestinal motility was noted when the gastric juice was injected intraperitoneally. As shown in Figure 2, immediately after the injection of gastric juice, mechanical activity of the intestine ceased. The amplitude of the electrical “slow” waves diminished slightly, and spike potentials were no longer associated with the “slow” waves. The period of inhibition lasted several hours. Intestinal motility was nearly normal the day after injection of gastric juice in all four dogs. Repetition of this procedure for four consecutive days did not appear to cause progressive deterioration in the condition of the dogs. When the dogs were sacrificed on the fourth day, there was little evidence of peritonitis or other abnormalities of the abdominal organs. Gastric Perforation. As a result of gastric perforation two dogs survived less than twenty-four hours and four dogs died between twenty-four and forty-eight hours. A typical record of electrical and mechanical activity of the intestine in a dog shortly before death is shown in Figure 3. There was almost complete inhibition of mechanical activity of the intestine. The “slow” electrical waves persisted until the animal died. The spike potentials, however, were absent at that time. No fluid or air had accumulated within the lumen of the small intes-

The American Journal of Surgery

Paralytic lleus

tine, but there was an accumulation of 500 to 1,000 ml of peritoneal fluid. Appendiceal Ligation. Two of four dogs exhibited moderate inhibition of intestinal motility as long as forty-eight hours. In two dogs intestinal motility was essentially normal after twenty-four hours. (Figure 4.) In these two with normal intestinal motility after twenty-four hours, autopsy revealed omentum completely surrounding and encapsulating the necrotic appendix. Intraperitoneal Chemical Irritation. Iodine administered intraperitoneally slightly inhibited electrical and mechanical activity of the intestine at the time of injection. (Figure 5.) Within twentyfour hours the recordings appeared to be normal. The condition of the dogs appeared normal and they had no obvious signs of peritonitis or ileus. At autopsy, five days after the procedure, the abdominal organs appeared normal. Retroperitoneal Blood. No obvious changes in intestinal motility resulted from retroperitoneal injection of 50 ml of blood in each of two dogs. Partial Occlusion of the Superior Mesenteric Artery. Intestinal motility appeared normal within

twenty-four hours after partial occlusion of the superior mesenteric artery in all four dogs. No fluid accumulation was observed in either the intestinal lumen or the peritoneal cavity. Mechanical

and Thermal Peritoneal

Irritation.

Electrical and mechanical activity of the intestine appeared only slightly inhibited for several hours after the abdominal cavity was opened and the peritoneum irritated. Each day, until the fifth day when the abdomen was re-explored before sacrifice, normal peristalsis was observed throughout the entire intestine in each dog. Each part of the small bowel contracted vigorously when pinched. The dogs were sacrificed on the fifth day. The volume and composition of the fluid taken from the various parts of the intestine, as well as the characteristics of the peritoneal fluid, are shown in Tables I and IT, respectively. The bacterial culture of the peritoneal fluid demonstrated no growth. In only three of six dogs could peritoneal fluid be obtained. Intestinal fluid was obtained in four of six dogs.

-

,__“_..__““%.ll_

.___”

..,.

__..“.._“...”

.

.-.,_^

AFTER 24 HOURS

AFTEfl SO CC GASTRffi JUICE

CoNTm.

Figure 2. The effect of intraperitoneal gastric juice. The upper part of the tracing shows mechanical activity that was completely Inhibited by the intraperltoneal injection of 50 ml of gastric juice. Motility returned after twentyfour hours. The lower part of the tracing shows the concomitant changes in electrkal activity. Spike potentials disappeared after the injection of gastric juice but returned within twenty-four hours. “Slow” wave activity was not abolished.

PL._‘.“_...._

__._“__”

I_.

nwms*pltlr

B.

_-

--.

tl “4.-1

.,.-..a

AFTa? lEll!cwis

Figure 3. The effect of gas&k perforation. Within twentyfour hours after gastric perforatkn, intestinal motlltty, shown in the upper part of tfw tracing, was completely Inhlbited. ‘slow” wave electrical actlvlty was retained until the dog died, but spike activity disamared within twenty-four hours after gastric perforation.

Figure 4. After appendkeal ligatkn electrical and mechanical activities of the intestine were only slight& Inhlblted.

Comments

There have been relatively few investigations of the conditions leading to paralytic ileus in experimental animals. In this series of experiments various types of abdominal injury were used in an effort to inhibit intestinal motility. The effects of in-

Volume129,May1975

Figure 5. lntraperftoneal kdlne caused an inhlbitkn of intestinal m0ttnty immedlatety after ns Injection, but motil/ty returned wtthin twenty-four hours.

561

Mishra, Appert, and Howard

TABLE

I

Fluid and Electrolyte

Dog Numberand Intestinal Segment

1 Duodenum

2

3

4

5

6

Jejunum Ileum Duodenum Jejunum Ileum Duodenum Jejunum Ileum Duodenum Jejunum Ileum Duodenum Jejunum Ileum Duodenum Jejunum Ileum

Composition

of Intestinal

Weight of Intestinal Segment

Fluid in Intestinal Segment

(gm)

(ml)

(mOsm/L)

72 211 150 70 210 195 90 143 225 56 196 107 64 208 189 50 193 204

10 140 150 0 0 0 50 55 0 10 5 75 0 0 0 5 10 15

296 305 316

gastric juice were similar to those observed by Smith, Jepson, and Catchpole [3] who found that ninety minutes after the injection of 20 ml of 0.1 hydrochloric acid into cats intestinal motility was still inhibited. Their observations were not continued beyond that period of time. In our investigation, intestinal motility returned to almost normal after twenty-four hours. Similarly, Douglas and Mann [2] found that intraperitoneal irritation caused by the injection of Lugol’s iodine solution in dogs and rabbits caused an inhibition of intestinal motility that lasted as long as four hours. Motility returned after this period of inhibition. Lindqvist [4] found that the retroperitoneal injection of blood and turpentine reduced but did not eliminate the transit of material through the gastrointestinal tract of rats. Williams [5] has reviewed the effects of vascular insufficiency of the intestine in humans and experimental animals. Passi and Lansing [6] investigated the effects of complete and partial occlusion of the superior mesenteric artery. Dogs subjected to complete mesenteric arterial occlusion died traperitoneal

TABLE

II

Accumulation

1 4 5

562

of Peritoneal

Fluid

(ml)

Osmotic Pressure (mOsm/L)

Sodium (mEq/L)

Potassium (mEq/L)

Total Protein (gm/l@J ml)

150 34 250

290 286 240

150 154.5 140

4.75 6.45 5.02

20.57 28.57 20.5

Dog Number

Fluid

Segments

of Dogs Subjected

306 326 ... 379 382 302

... ... ... 370 350 302

Irritation

Sodium

Potassium

(mEq/L)

(mEq/L)

140 150 154

... ... ...

to Peritoneal

... 180 170

... 178 125.5 90.5

... ... 175 130 120

Total Protein

(gm/lOOml)

7.75 8.8 8.1

11.02 10.50 10.44

...

...

.., 8.3 13.2

.. . 10.52 10.82

... 16.0 15.0 15.0

... ... 14.0 15.0 16.0

39.36 16.88 16.88 ...

... 30.50 16.0 10.0

within twenty-four hours. In a few of the dogs subjected to partial mesenteric arterial occlusion, thrombosis developed and they died in the immediate postoperative period. The dogs without mesenteric arterial thrombosis appeared to be similar to the control animals in the immediate postoperative period. Zuidema et al [7] studied the effects of occlusion for two hours of the superior mesenteric artery. For several days after the procedure they found a striking increase of intravenously administered 1311polyvinylpyrrolidine in the stool. The dogs appeared to be in good health a few days later. The findings in the current investigation appear to agree with those of Rothnie, Harper, and Catchpole [8]. Those investigators found that in humans after abdominal operation the small intestine remains capable of normal motility and propulsion. They believed that reduction of intestinal motility during the postoperative period was due to an absence of intestinal contents resulting from impaired gastric emptying. Noer [9] similarly showed that intestinal motility persisted in humans after abdominal operation, although the intestinal transit times of radiopaque media were prolonged. Tinckler (101 similarly found that anesthesia and manipulation of the intestine in dogs inhibited but did not eliminate intestinal motility. In the present investigation, little accumulation of intraluminal fluid was observed in the small intestine despite rather severe intraperitoneal irritation. This observation is consistent with the find-

lho American Journal ol Surgery

Paralytic

ings of other investigators. Glucksman, Kalser, and Warren [II] found that the absorption of glucose and Na22C1 was not inhibited in dogs after intestinal transection and reanastomosis. The importance of intestinal decompression during the postoperative period was emphasized by Moss [12] and is well known. Moss found that when air swallowing is prevented, there is early postoperative restoration of intestinal function, and rates of feeding as high as 100 ml/hour are tolerated in many patients within twenty-four hours after operation. In the current investigation, repeated chemical and mechanical irritation of the peritoneal surface of the abdominal cavity caused only a slight increase in the amount of fluid found in the intestinal lumen. Other forms of intraperitoneal injury did not lead to any noticeable excess accumulation of fluid within the small intestine. From this study it is concluded that, in dogs at least, intraperitoneal irritation is of little importance in causing accumulation of fluid within the small intestine during nonobstructive ileus. Summary This study is significant in demonstrating that the small intestine of the dog is extremely resistant to paralytic ileus. The various types of intraabdominal irritation studied were quite severe. After a transient period of inhibition, however, in most instances motility of the small intestine returned and continued until near the time of death. Various types of intra-abdominal irritation were used to study paralytic ileus in dogs, including intraperitoneal injection of gastric juice, gastroperitoneal fistula, appendiceal ligation, intraperitoneal injection of Lugol’s iodine solution, retroperitoneal injection of blood, and mechanical and thermal irritation of the intestine and peritoneum. The electrical and mechanical activity of the small intestine was observed by means of a Thomas cannula implanted in the jejunum. The presence or absence of fluid accu&lation within the intestinal lumen or peritoneal cavity was noted at autopsy.

Vohme 129, May 1975

lleus

Intra-abdominal chemical irritation caused a transient inhibition of intestinal motility, which was reversed when the irritation was stopped. Repeated irritation did not appear to cause progressive, irreversible inhibition of intestinal motility. When intestinal motility was depressed, spike potentials were absent in the recordings of electrical activity of the intestine. The “slow” electrical waves were distinguishable at all times. With the exception of the gastroperitoneal fistulas, the procedures were tolerated with only transient inhibition of intestinal motility. Accumulation of intraperitoneal fluid occurred in dogs subjected to gastroperitoneal fistulas. A small amount of intraluminal fluid accumulated in dogs subjected to repeated thermal and mechanical irritation of the intestines and peritoneum. In the other groups of dogs no significant increase in intestinal or intraperitoneal fluid was observed. References 1. Thomas JE: Methods for study of external secretory function of the pancreas. Methods Med Res 4: 149, 1951. 2. Douglas DM, Mann FC: The effect of peritoneal irritation on the activity of me intestine. Br Med J 1: 227, 1941. 3. Smith MK, Jepson RP, Catchpole BN: Ileus: an experimental study. Br J Surg 52: 361, 1965. 4. Lindqvist B: Propulsive gastrointestinal motility related to retroperitoneal irritation. Acta Chir Stand (Suppl) 365, 1966. 5. Williams LF: Vascular insufficiency of the intestines. Gesfrcenterology61: 757, 1971. 6. Passi BB, Lansing AM: Experimental intestinal malabsorption produced by vascular insufficiency. Can J Surg 7: 332, 1964. 7. Zuidema GD. Turcotte, JC, Wolfman EL, Child CG: Metabolic studies in acute small-bowel ischemia. Arch Surg 65: 130, 1962. 6. Rothnie NG, Harper RAK, Catchpole BN: Early postoperative gastrointestinal activity. Lancet 2: 64, 1963. 9. Noer T: Roentgenological transit time through the small intestine in the immediate postoperative period. Acta Chir Stand 134: 577. 1968. 10. Tinckler LT: Surgery and intestinal motility. Br J Surg 52: 140. 1965. 11. Glucksman DL, Kalser MH, Warren WD: Small intestinal absorption in the immediate postoperative period. Surgery 60: 1020, 1966. 12. Moss G: Postoperative decompression and feeding. Surg Gynecol Obstet 122: 550, 1966.

563

Studies of paralytic ileus. Effects of intraperitoneal injury on motility of the canine small intestine.

This study is significant in demonstrating that the small intestine of the dog is extremely resistant to paralytic ileus. The various types of intra-a...
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