Original Papers Digestion 14: 293-303 ( 1976)
Gastrointestinal Myoelectrical Activity during the Postoperative Period in Man J. Dauchel, J.C. Schang, J. Kachelhoffer, R. Eloy and J.F. Grenier' Service d'investigations chirurgicales. Pavillon chirurgical I). Hospices civils, Strasbourg
Key Words. Cholecystectomy • Klcctromyography • Gastrointestinal motility • Ileum • Intestinal obstruction • Jejunum • Stomach • Surgery operative Abstract. Myoelectrical activity of the gastrointestinal tract has been studied in the postoperative period of 13 patients who underwent cholecystectomy. The recordings have been performed by means of extracellular electrodes which were implanted at the levels of stomach, jejunum, ileum and colon during the surgical procedure. The records showed that fast activity is always persistent while the basic electrical rhythm is greatly disorganized during the immediate postoperative period. Such a characteristic pattern of the electrical activity suggested that the lack of peristaltic and propulsive movements, always noted during this period, is not correlated with a disappearance of gastrointestinal contractions, but only with a disturbance in their coordination.
Electrical potentials recorded from intestinal smooth muscles can be divided into two types: spike activity and slow waves. Spike activity is concomitant with intestinal muscle contractions (4, 28, 35). In contrast, the slow waves are omnipresent and constitute the basic electrical rhythm (BER). They demon strate a gradient of rate which decreases along the intestine in a caudad direction (27). Slow waves coordinate muscle contractions and seem to organize peristaltic movements (22, 29). The well-known concept of postoperative 'physiological’ ileus was deduced from the observation that abdominal surgery is followed by bowel distension, disappearance of intestinal sounds and delay in passage of stools for several days. These observations led to the belief that the gastrointestinal tract is paralyzed after abdominal surgery. Now, numerous studies using conventional techniques, 1 The expert technical assistance of M. Claude Mendel is gratefully acknowledged.
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Received: November 13, 1975; accepted: March 11, 1976.
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such as radiology or audiometrical methods (2, 23, 30), have demonstrated that the intestinal contractions are rapidly occurring after abdominal surgery. Never theless, these studies failed to provide precise information concerning the ‘physi ological’ ileus. Therefore, a further investigation into this problem appears to be of great interest. The purpose of the present work was to study tire electrical activity of the gastrointestinal tract after abdominal surgery for assessing the recovery of its motility.
Recordings were obtained from a group of 13 patients who underwent cholecystec tomy. The nature and extent of the investigations were explained to these subjects who have previously given informed consent. Thus, the trial was always restricted to volunteers. Silver-silver chloride electrodes were implanted on stomach, jejunum, ileum and colon during the surgical procedure. The recording surface of the electrodes consisted of a straight segment of wire approximately 3 mm long which was inserted into the muscular coat by serosal way and fixed with a suture of catgut. The lead wires from the electrodes to the recorder passed through the abdominal wall in the same orifice as that performed for drainage of the abdominal cavity. The electrodes were withdrawn on the 7th postoperative day by pulling out the lead wires. A common indifferent electrode was placed on the abdominal wall of the patients. In order to prevent the influences of pharmacological therapy on gastrointestinal motility (23), drugs and anesthetics were strictly managed. Thus, each patient received only diazepam (10 mg) as preoperative medication. Anesthetics were sodium pentobarbital (500 mg) and suxamethonium (80 mg). A nasogastric tube was passed and constant suction was instituted for the first 3 postoperative days. During this period, the patients received only saline solutions (mainly 3 liters of saline with 5 % of glucose per day) by intravenous perfusions. The recorder was an Accutrace (Beckman) polygraph with low-level preamplifiers. Two values of time constants were used to record the potentials occurring at each electrode: 0.03 and 1 sec for the recording of fast activity and slow waves, respectively. A continuous recording of 60 min duration was performed immediately after the operation, and then every 12 h during the first 7 postoperative days. The analysis of the tracings was carried out by dividing the 60-min recordings into 12 consecutive segments of 5 min each. Their interpretation considered both fast activity and slow waves. (1) Configuration of slow waves was studied because postoperative tracings demon strated that regular BER alternated with irregular potential variations which could not be considered as normal slow waves. Thus, a ‘normal slow wave’ had to be characterized, referring to its period, amplitude and configuration, in order to measure the time during which a normal BER was observed. The period of the slow waves is known to present little variations in time (4, 6, 22). Studies in man have demonstrated that these variations never exeed 10 % of the value of the mean slow wave period (12, 13). Thus, we have considered that each potential variation which ranged within these limits could account for a slow wave. Anatomical location of the electrodes allowed to know the approximative value of the BER frequency at the recording site. Precise determination of the mean slow wave period was performed when BER presented a regular pattern for at least 30 sec. Amplitude of the potential variations had to reach more than 0.1 mV. Finally, the configuration of the normal slow waves had to correspond to those which were described by Basset al. (3) and Prosser and Bortoff (37). In fact, the most typical characteristic was the depolarization
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Methods
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Fig. 1. Tracing illustrating determination of the index of regularity of the RER: normal slow waves are recorded during n time intervals: (A ,), (A,), (A3) , ... (An). Index of regularity (%):
(A,) + (A2) + (A3) + - ( A „ ) V/ 100 R (= S min)
phase which punctuated precisely the limits of the slow waves. Thus, number of normal slow waves could be counted as well as the mean period. The ratio between the number of normal slow waves and the theoretical total number of slow waves during 1 h of recording expressed a percent of normal BER duration which was called ‘index of regularity of the BER' (fig. 1). (2) Spiking activity of the bowel was measured on the tracings which were performed with a time constant of 0.03 sec. Electric signals reaching less than 10 jiV in amplitude were detected. Only 'bursts of spikes' have been considered since their occurrence corresponds to that of intestinal contractions, whereas ‘spikes’ by themselves arc only representative of the strength of a contraction (4, 7, 8). The duration of spiking activity was calculated in attributing at each burst of spikes the mean duration of a slow wave. Mean period of slow waves was measured during time intervals in which BER exhibited a regular configuration. Thus, the theoretical number of slow waves which were superimposed by bursts of spikes could be determined, as well as the theoretical total number of slow waves occurring during the whole recording time. Then, it was possible to calculate the percentage of ‘superim posed’ slow waves which represents the duration of fast activity, according to the method of measurement of McCoy and Baker (29) and Weisbrodt and Christensen (42). In order to present these data more clearly, the numbers obtained have been given as a ‘percentage of fast activity’. When several bursts occurred within the duration of one slow wave (fig. 2, arrows), they were considered to account for only one burst. (3) in addition, the time at which each patient passed flatus was noted. This clinical data enabled us to determine the mean value and SEM of the duration of the ‘physiological’ ileus, as far as the 13 patients of the study are concerned.
Results
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Electrical Activity Jejunum. The immediate postoperative tracings were highly disorganized at the level of the jejunum. During this period, the BER was constituted most of
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Fig. 2. Postoperative tracings recorded in jejunum on the 1st (top record), 24th (middle record) and 36th postoperative hour (bottom record). The recordings were per formed with a time constant of 1 sec (upper tracings) and 0.03 sec (lower tracings).
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Fig. 3. Postoperative tracings recorded in colon on the 1st (top record), 36th (middle record) and 72nd postoperative hour (bottom record). The recordings were performed with a time constant of 1 sec (upper tracings) and 0.03 sec (lower tracings).
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the time, by irregular slow waves with an abnormal aspect, and a low and variable amplitude (0.35 ± 0.20 mV). Only a few normal slow waves were present, so that the index of regularity of the BER was found to be low (about 25 %). The later tracings showed a progressive normalization of the slow waves associated with an increase in their amplitude. Finally, a normal BER was re corded on the 36th postoperative hour. Then, the index of regularity was about 80 %, while the amplitude of the slow waves reached 0.85 ± 0.08 mV and their frequency about 15 cpm. A great number of bursts of spikes occurred in the early postoperative period. Thus, the percentage of fast activity reached 44 ± 18 % immediately after the operation. This value is greater than the percentage usually observed in the jejunum under resting conditions (about 30 %). On the 12th postoperative hour, the percentage of fast activity decreased to 19 ± 7 %. Then, a progressive increase occurred and a normal percentage was observed on the 36th postoperative hour (fig. 2; table I). Ileum. The pattern of the electrical activity at the level of the ileum was similar, but slower than that observed at the level of the jejunum: the BER was greatly disturbed immediately after the operation and it normalized pro gressively within 48 h. On the 48th hour, the index of regularity was found to be about 80%, the amplitude of the slow waves, 0.75 ± 0.10 mV, and their fre quency, about 10 cpm. Similarly, a high percentage of fast activity was noted immediately after the operation, as was the case at the level of the jejunum. After a decrease on the 12th postoperative hour, the percentage of fast activity increased progressively and normalized about 48 h after the operation (table I). Colon. A completely disorganized BER was observed in the colon during the first 24 postoperative hours. During this time, the index of regularity was less than 5 %. The normalization of the BER occurred within 72 h. Then, the index o f regularity was about 90 %, the amplitude of the slow waves 2.10 ± 0.30 mV and their frequency about 6 cpm. No fast activity was observed before the 36th postoperative hour. Later, some bursts of spikes occurred. Nevertheless, the percentage of fast activity remained low and it reached normal values as from the 72nd postoperative hour only (fig. 3; table 1). Stomach. The tracings were also disturbed immediately after the operation at the level of the stomach. Nevertheless, a relatively great number of slow waves with a normal aspect occurred immediately after the surgical procedure, so that the index of regularity was relatively high (about 45 %). Progressively, all the slow waves became regular and a normal BER was observed on about the 24th postoperative hour. At this time, the value of the index of regularity was about 98 %, the amplitude of the slow waves 0.80 ± 0.02 mV and their frequency about 4.5 cpm. The percentage of fast activity was very low during the early postoperative period: thus, it was less than 5 % during the 1st postoperative hour. Later tracings showed a progressive increase of this percentage. Finally, it normalized within about 24 h after tire operation (table I).
Jejunum
1 12 24 36 48 60 72
24.2 t 7.3 44 ± 18 37.4 ± 9.4 19 t 7 56.0 ± 11.3 82.4 i 9.7 37 ± 9 81.0 ± 12.4 41 ± 7 24 t 8 78.2 ± 8.5 84.2 ± 6.3 29 ± 10
index of regularity of the BER %
percentage of fast activity
Stomach
Colon
Ileum
00 ♦1 m
index of regularity of the BER %
percentage of fast activity
index of regularity of the BER %
20.1 25.2 45.0 68.1 80.4 80.0 85.6
34 ± 15 12 t 7 25 ± 6 31 ± 9 39 ± 12 37 ± 10 32 ± 12
less than 5 less than 5 less than 5 less than 5 less than 5 12.4 ± 7.1 37.2 ± 8.4 less than 5 12 ± 8 65.3 ± 6.2 76.4 ± 17.5 30 ± 12 18 ± 9 90.3 ± 9.9
± 5.4 ± 8.1 ± 11.0 ± 10.3 t 8.5 ± 9.4 ± 8.5
percentage of fast activity
index of regularity of the BER %
percentage of fast activity
45.8 69.4 98.0 98.0 93.2 97.1 98.6
less than 5 less than 5 9±5 12 ± 7 8±5 7*4 11 ± 5
± 2.6 ± 2.3 ± 1.0 ± 1.1 ± 1.0 ± 1.2 ± 1.0
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Post operative time, h
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Table I. Index of regularity of the BF.R and percentage of fast activity at the levels of jejunum, ileum, colon and stomach in each stage of the study (mean values ± SEM)
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Duration o f 'Physiological'Ileus The patients have passed flatus on about the 70th postoperative hour (mean duration of the ‘physiological’ ileus ± SEM: 70 ± 8 h).
Analysis of the results presented in this study requires that normal electro myographic state is known in man. Numerous works have been carried out in this field by use of intraluminal devices. Such techniques were extensively employed to study the electrical activity of stomach and colon in normal sub jects (13 15, 20, 21, 24, 32, 40). Small bowel electromyography is less well known because intraluminal techniques cannot be used in normal subjects for studying this part of the gastrointestinal tract. Nevertheless, some authors have obtained tracings by placing electrodes in exteriorized segments of bowel (17) or during surgery (16, 36). These studies demonstrate that intestinal electrical activity recorded in man can be compared to that obtained in other mammals, such as dog and cat. Especially BER has always been noted to exhibit little variations in frequency and amplitude. Thus, it seems that tracings obtained in our work can be considered as normal when the different parameters of slow waves (index of regularity, amplitude, configuration) have reached a steady state. Possible artefacts resulting from the medications which were given to the patients may be excluded since it is well known that BER is little or not affected by pharmacological substances. Most workers have reported that general anaes thesia (27), cholinergic and adrenergic blocking or mimicking agents (5, 9, 10, 18, 31, 38), ganglion-blocking drugs (31, 20), morphine (27) or pentobarbital (27) only slightly change BER frequency, but do not disturb BER amplitude or configuration. Numerous studies of gastrointestinal motility after abdominal surgery have been carried out by several authors in the last decades. All the reports have been in agreement about the fact that intestinal motility is not abolished during the early postoperative period. Farrar and Ingelfinger (23), using audiometrical techniques, have noted that some gastrointestinal contractions are present im mediately after an abdominal operation. Nachlas et al. (33) reported that barium instilled into the bowel during the operation progressed slowly through the gastrointestinal tract in the early postoperative period. Our observations are in agreement with these findings because of the persistence of electrical fast activity observed during the whole postoperative period. Moreover, immediately after the operation, fast activity was more marked than under the resting con ditions. These observations suggest that intestinal motor activity can be in creased in the early postoperative period. In fact, this phenomenon has been previously noted by Baker and Dudley (2) who carried out studies of abdominal
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Comments
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sounds in surgical patients. Today, the cause of this increased motor activity is not clearly established, but it can be thought that handling of the bowel during the operation may play a role. Although intestinal contractions are present during the immediate postoperative period, it appears that they produce only a few propulsive movements. Nachtas et al. (33) have noted that the transit time of a barium bolus through all intestinal segments is considerably longer during the first 24 hours after abdominal surgery than under resting conditions. This phenomenon might be correlated with a disturbance in coordination of intestinal motility. This hypothesis is supported by our observation that, during the im mediate postoperative period, the BER was always abnormal. Indeed, it is well established that the BER has a preponderant role in the occurrence and the propagation of muscular contractions, and it can be suggested that the distur bances of the BER are responsible for the lack of large propulsive movements during the early postoperative period. In the present study some differences have been noted in the delay of the normalization of the electrical activity after surgery between the various seg ments of the digestive tract. Almost similar data have been previously reported as far as the gastrointestinal motility is concerned (25, 26, 39, 43). All these authors have outlined that the recovery of the normal motility occurs in the small intestine within 36 h, in the stomach within 48 h and in the colon within more than 48 h. Thus, our findings concerning the small bowel and the colon are in agreement with the results of these investigators since the normalization of the BER has been noted in our patients within 36 h in the jejunum, 48 h in the ileum and 72 h in the colon. The good correlation between the time of normal ization of the BER in the colon and the time at which the patients have passed flatus gives further evidence of the role of this organ in the duration of postoper ative ‘physiological’ ileus. Only for the stomach, our results are not entirely in agreement with the data provided by the conventional investigations, in partic ular with radiological methods. Indeed, radiological studies indicate that the gastric motor activity does not return to the normal pattern before the 48th postoperative hour. However, in all our patients, a normal BER has been observed at the level of the stomach as early as 24 h after the operation. It must be noted that, when radiological methods are used, gastric motility is considered as normal when barium passed through the gastroduodenal junction (33). Now, some authors have reported that a noticeable increase of the pyloric tone usually occurred after abdominal surgical procedures (29). Thus, it can be thought that the long delay observed for the recovery of a normal gastric motility with radiological methods is related to the hypertony of the gastroduodenal junction, and does not reflect the real time of the normalization of the motor activity of the stomach. Based on our electrical activity study, the gastric motility seems to be normalized within about 24 h after the operation. These findings are in agreement with the data reported by Sarna et al. (41).
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It is well established in animals that postoperative ileus results from sympathetic inhibition mediated by a spinal reflex and this is generally accepted as being also true for man (1, 11, 19, 34, 44). The present study brings further indications about the mechanisms of paralytic ileus. It demonstrates that post operative motility is not abolished but only disorganized, and that failure of propulsive movements results from the loss of their coordination by BER. Precise relationships between disturbances of electrical activity of smooth muscle cells and sympathetic inhibition remain to be established. Nevertheless, some cellular mechanisms may be suggested hypothetically. One of these mechanisms could be an alteration of nexuses which are actually thought to constitute the anatomical support of intracellular coupling. Thus, smooth muscle cells may depolarize in an uncoordinated manner as evoked by BER irregu larities. Another mechanism may be that there are disturbances of the rela tionships between circular and longitudinal muscle layers, so that synchroniza tion of the movements of each layer is transiently abolished, resulting in the absence of organized peristaltic movements. A third mechanism may be that stimulation of inhibitory neurons of the enteric plexuses is involved in sympa thetic inhibition, resulting in an interruption of the neuronal modulation of intestinal motility.
References
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1 Abe, li: Apperi, H E ., and Howard, J.M.: Hemodynamic observations of adynamic ileus in the conscious dog. Ann. Surg. 179: 332 - 338 (1974). 2 Baker, /.. W. and Dudley, H.A.: Ascultation of the abdomen in surgical patients. Lancet «.517-519(1961). 3 Bass. P.: Code, C.F., and l.ambert, E.H.: Motor and electric activity of the duodenum. Am. J. Physiol. 201: 287-291 (1961). 4 Bass, P.: In vivo electrical activity of the small bowel; in Code Handbook of physiol ogy, vol. 4, sect. 6, pp. 2051 2074 (Williams & Wilkins, Baltimore 1968). 5 Berkson, J.: Electromyographic studies of the gastrointestinal tract. V. Further inquiries into the origin of potential variations of the small intestine by means of several drugs. Am. J. Physiol. 105: 450 453 (1933). 6 Bortoff, A.: Slow potential variations of small intestine. Am. J. Physiol. 201: 203-208 (1961). 7 Bozler, E.: Electrophysiological studies on the motility of the gastrointestinal tract. Am. J. Physiol. 127: 301-307 (1939). 8 Bozler, E.: Reflex peristalsis of the intestine. Am. J. Physiol. 157: 338-342 (1949). 9 Bunker, C.E. and Nelsen, T.S.: Use of the electroenterogram to determine pacemaker activity of the small intestine. Surg. Forum 15: 293 (1964). 10 Castleton, K.B.: An experimental study of the movements of the small intestine. Am. J. Physiol. 107: 641-646 (1934). 11 Catchpole, B.N.: Ileus; use of sympathetic blocking agents in its treatment. Surgery, St Louis 66: 811-820 ( 1969).
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Christensen, J.: Schedl, H.P., and Clifton, J.A.: The basic electrical rhythm of the duodenum in normal human subjects and in patients with thyroid disease. J. clin. Invest. 43: 1659-1667 (1964). Christensen, J. : The small intestinal basic electrical rhythm (slow wave) frequency gradient in normal men and in patients with a variety of diseases. Gastroenterology 50: 309-315 (1966). Couturier, D.: Roze, C, and Couturier-Turpin, M.H.: Electromyography of the colon in situ: an experimental study in man and in the rabbit. Gastroenterology 56: 317— 322 (1969). Couturier, D. et Roze. C: Mesure des paramètres caractéristiques de l’électromyogramme gastrique human normal. Biol. Gastro-Enterol. 60: 11-22 (1971). Daniel, E.E.: Carlow, D.R.: Wächter, B.T.: Sutherland, W.H., and Bogoch, A.: Electrical activity of the small intestine. Gastroenterology 37: 268-281 (1959). Daniel, E.E.: Honour, A.J., and Bogoch, A.: Antagonism of serotonin-induced contrac tion and electrical activity in the ileum. Gastroenterology 39: 62-73 (1960). Daniel, E.E.: Wächter, B.T.: Honour, A.J., and Bogoch, A.: The relationship between electrical and mechanical activity of the small intestine of dog and man. Can. J. Biochem. Physiol. 38: 777-801 (1960). Dubois, A.; Kopin, J.J.; Pettigrew, K.D., and Jacobowitz, D.M.: Chemical and histochemical studies of postoperative sympathetic activity in the digestive tract in rats. Gastroenterology 66: 403-407 (1974). Duthie, H.L.; Brown, B.H.: Robertson-Dunn, B K w o n g , K.K.; Wittaker, G.E., and Waterfall, W.: Electrical activity in the gastroduodenal area. Slow waves in the proximal duodenum. A comparison of man and dog. Am. J. dig. Dis. 17: 344 (1972). Duthie, H.L.: Waterfall, W., and Brown, B.H.: The electrical and motor actions of gastrointestinal hormones on the duodenum in man. Gut 14: 689-696 (1973). Duthie, H.L.: Electrical activity of the gastrointestinal smooth muscle. Gut 15: 669-681 (1974). Farrar, J.J. and Inge¡finger, F.J.: Gastrointestinal motility as revealed by study of abdominal sounds. Gastroenterology 29: 789-799 (1955). Forster, F.M.: Helm, J.D., and Ingelfinger, F.J.: The electrical potentials of the human small intestine. Am. J. Physiol. 139: 433-437 (1943). Glucksman, D.L.: Kaiser, H.. and Warren, W.D.: Small intestine absorption in the immediate postoperative period. Surgery, St Louis 60: 1020-1027 (1966). Harrower, L.W.: Postoperative ileus. Am. J. Surg. 116: 369 374 (1968). Holaday, D.A.; Volk, H.. and Mandell, J.: Electrical activity of the small intestine with special reference to origin of rhythmicity. Am. J. Physiol. 195: 505-515 (1958). McCoy, E.J. and Bass. P.: Chronic electrical activity of gastroduodenal area: effects of food and certain catecholamines. Am. J. Physiol. 205: 439-445 (1963). McCoy, E.J. and Baker, R.D.: Effect of feeding on electrical activity of dog’s small intestine. Am. J. Physiol. 214: 1291-1295 (1968). McPhail, J.L: Hardy. J.D.: Conn, J.H.; Shor, J., and Robinson, S.: Studies in postoper ative ileus: intestinal motility as reflected in the propulsion of radioopaque materials. Surg. Forum 2: 471-473 (1958). Milton, G. W.; Smith, A. W., and Armstrong, H.I.O.: The origin of the rhythmic electropotential changes in the duodenum. Q. J! exp. Physiol. 40: 79-88 (1955). Monges, H. et Salducci, J.: Etude clectromyographique de la motricité gastrique chez l’homme normal. Archs Mal. Appar. dig. 58: 517-530 (1969). Nachlas, M.M.: Younis, M.T.: Roda, C.P.. and Wityk, J.J.: Gastrointestinal motility studies as a guide of postoperative management. Ann. Surg. 175: 510 522 (1972). Downloaded by: Univ. of California Santa Barbara 128.111.121.42 - 3/8/2018 2:14:17 PM
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Neely, J.: The effects of analgesic drugs on gastrointestinal motility in man. Br. J. Surg. 56: 925-929 (1969). 35 Nelsen, T.S. and Baker. J.C.: Simulation of the electrical and mechanical gradient of the small intestine. Am. J. Physiol. 214: 749-757 (1968). 36 Nielubowicz, J.: Folga, J., and Wiekowska, W.: Electroenterolography. Archs Surg., Chicago 90: 698-707 (1965). 37 Prosser, C.L. and Borloff, A.: Electrical activity of intestinal muscle under in vitro conditions; in Code Handbook of physiology, vol. 4, sect. 6, pp. 2025—2050 (Williams & Wilkins, Baltimore 1968). 38 Puestow, C.B.: Studies on the origin of automaticity of the intestine: the action of certain drugs on isolated intestinal transplants. Am. J. Physiol. 106: 682-688 (1933). 39 Bothnie, N.G.: Harper, N.A.K., and Catchpole, B.N.: Early postoperative intestinal motility. Lancet ii: 64-67 (1963). 40 Salducci, J. et Monges, H.: Etude électromyographique du duodénum chez l’homme normal. Archs Mal. Appar. dig. 59: 19-28 (1970). 41 Sarna, S.K.; Bowes, K.L., and Daniel, E.E.: Postoperative gastric electrical control activity (E.C.A.) in man; in Daniel Proc. 4th Int. Symp. on Gastrointestinal Motility, Banff 1973, pp. 73-83 (Mitchell, Vancouver 1974). 42 Weisbrodt, JV. W. and Christensen, J.: Electrical activity on the cat duodenum in fasting and vomiting. Gastroenterology 63: 1004-1010 (1972). 43 Wells, C; Rawlinson, K.: Tinckler, /.., Jones, //.. and Saunders, J.: Ileus and postoper ative intestinal motility. Lancet ii: 136-137 (1961). 44 Wilson, J.P.: Postoperative motility of the large intestine in man. Gut 16: 689-692 (1975). 34
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J.F. Grenier, Pavillon chirurgical B, Hospices civils, F 67005 Strasbourg Cedex (France)
Gastrointestinal Myoelectrical Activity during the Postoperative Period in Man J. Dauchel, J.C. Schang, J. Kachelhoffer, R. Eloy and J.F. Grenier' Service d'investigations chirurgicales. Pavillon chirurgical I). Hospices civils, Strasbourg
Key Words. Cholecystectomy • Klcctromyography • Gastrointestinal motility • Ileum • Intestinal obstruction • Jejunum • Stomach • Surgery operative Abstract. Myoelectrical activity of the gastrointestinal tract has been studied in the postoperative period of 13 patients who underwent cholecystectomy. The recordings have been performed by means of extracellular electrodes which were implanted at the levels of stomach, jejunum, ileum and colon during the surgical procedure. The records showed that fast activity is always persistent while the basic electrical rhythm is greatly disorganized during the immediate postoperative period. Such a characteristic pattern of the electrical activity suggested that the lack of peristaltic and propulsive movements, always noted during this period, is not correlated with a disappearance of gastrointestinal contractions, but only with a disturbance in their coordination.
Electrical potentials recorded from intestinal smooth muscles can be divided into two types: spike activity and slow waves. Spike activity is concomitant with intestinal muscle contractions (4, 28, 35). In contrast, the slow waves are omnipresent and constitute the basic electrical rhythm (BER). They demon strate a gradient of rate which decreases along the intestine in a caudad direction (27). Slow waves coordinate muscle contractions and seem to organize peristaltic movements (22, 29). The well-known concept of postoperative 'physiological’ ileus was deduced from the observation that abdominal surgery is followed by bowel distension, disappearance of intestinal sounds and delay in passage of stools for several days. These observations led to the belief that the gastrointestinal tract is paralyzed after abdominal surgery. Now, numerous studies using conventional techniques, 1 The expert technical assistance of M. Claude Mendel is gratefully acknowledged.
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Received: November 13, 1975; accepted: March 11, 1976.
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such as radiology or audiometrical methods (2, 23, 30), have demonstrated that the intestinal contractions are rapidly occurring after abdominal surgery. Never theless, these studies failed to provide precise information concerning the ‘physi ological’ ileus. Therefore, a further investigation into this problem appears to be of great interest. The purpose of the present work was to study tire electrical activity of the gastrointestinal tract after abdominal surgery for assessing the recovery of its motility.
Recordings were obtained from a group of 13 patients who underwent cholecystec tomy. The nature and extent of the investigations were explained to these subjects who have previously given informed consent. Thus, the trial was always restricted to volunteers. Silver-silver chloride electrodes were implanted on stomach, jejunum, ileum and colon during the surgical procedure. The recording surface of the electrodes consisted of a straight segment of wire approximately 3 mm long which was inserted into the muscular coat by serosal way and fixed with a suture of catgut. The lead wires from the electrodes to the recorder passed through the abdominal wall in the same orifice as that performed for drainage of the abdominal cavity. The electrodes were withdrawn on the 7th postoperative day by pulling out the lead wires. A common indifferent electrode was placed on the abdominal wall of the patients. In order to prevent the influences of pharmacological therapy on gastrointestinal motility (23), drugs and anesthetics were strictly managed. Thus, each patient received only diazepam (10 mg) as preoperative medication. Anesthetics were sodium pentobarbital (500 mg) and suxamethonium (80 mg). A nasogastric tube was passed and constant suction was instituted for the first 3 postoperative days. During this period, the patients received only saline solutions (mainly 3 liters of saline with 5 % of glucose per day) by intravenous perfusions. The recorder was an Accutrace (Beckman) polygraph with low-level preamplifiers. Two values of time constants were used to record the potentials occurring at each electrode: 0.03 and 1 sec for the recording of fast activity and slow waves, respectively. A continuous recording of 60 min duration was performed immediately after the operation, and then every 12 h during the first 7 postoperative days. The analysis of the tracings was carried out by dividing the 60-min recordings into 12 consecutive segments of 5 min each. Their interpretation considered both fast activity and slow waves. (1) Configuration of slow waves was studied because postoperative tracings demon strated that regular BER alternated with irregular potential variations which could not be considered as normal slow waves. Thus, a ‘normal slow wave’ had to be characterized, referring to its period, amplitude and configuration, in order to measure the time during which a normal BER was observed. The period of the slow waves is known to present little variations in time (4, 6, 22). Studies in man have demonstrated that these variations never exeed 10 % of the value of the mean slow wave period (12, 13). Thus, we have considered that each potential variation which ranged within these limits could account for a slow wave. Anatomical location of the electrodes allowed to know the approximative value of the BER frequency at the recording site. Precise determination of the mean slow wave period was performed when BER presented a regular pattern for at least 30 sec. Amplitude of the potential variations had to reach more than 0.1 mV. Finally, the configuration of the normal slow waves had to correspond to those which were described by Basset al. (3) and Prosser and Bortoff (37). In fact, the most typical characteristic was the depolarization
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Methods
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Fig. 1. Tracing illustrating determination of the index of regularity of the RER: normal slow waves are recorded during n time intervals: (A ,), (A,), (A3) , ... (An). Index of regularity (%):
(A,) + (A2) + (A3) + - ( A „ ) V/ 100 R (= S min)
phase which punctuated precisely the limits of the slow waves. Thus, number of normal slow waves could be counted as well as the mean period. The ratio between the number of normal slow waves and the theoretical total number of slow waves during 1 h of recording expressed a percent of normal BER duration which was called ‘index of regularity of the BER' (fig. 1). (2) Spiking activity of the bowel was measured on the tracings which were performed with a time constant of 0.03 sec. Electric signals reaching less than 10 jiV in amplitude were detected. Only 'bursts of spikes' have been considered since their occurrence corresponds to that of intestinal contractions, whereas ‘spikes’ by themselves arc only representative of the strength of a contraction (4, 7, 8). The duration of spiking activity was calculated in attributing at each burst of spikes the mean duration of a slow wave. Mean period of slow waves was measured during time intervals in which BER exhibited a regular configuration. Thus, the theoretical number of slow waves which were superimposed by bursts of spikes could be determined, as well as the theoretical total number of slow waves occurring during the whole recording time. Then, it was possible to calculate the percentage of ‘superim posed’ slow waves which represents the duration of fast activity, according to the method of measurement of McCoy and Baker (29) and Weisbrodt and Christensen (42). In order to present these data more clearly, the numbers obtained have been given as a ‘percentage of fast activity’. When several bursts occurred within the duration of one slow wave (fig. 2, arrows), they were considered to account for only one burst. (3) in addition, the time at which each patient passed flatus was noted. This clinical data enabled us to determine the mean value and SEM of the duration of the ‘physiological’ ileus, as far as the 13 patients of the study are concerned.
Results
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Electrical Activity Jejunum. The immediate postoperative tracings were highly disorganized at the level of the jejunum. During this period, the BER was constituted most of
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Fig. 2. Postoperative tracings recorded in jejunum on the 1st (top record), 24th (middle record) and 36th postoperative hour (bottom record). The recordings were per formed with a time constant of 1 sec (upper tracings) and 0.03 sec (lower tracings).
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Fig. 3. Postoperative tracings recorded in colon on the 1st (top record), 36th (middle record) and 72nd postoperative hour (bottom record). The recordings were performed with a time constant of 1 sec (upper tracings) and 0.03 sec (lower tracings).
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the time, by irregular slow waves with an abnormal aspect, and a low and variable amplitude (0.35 ± 0.20 mV). Only a few normal slow waves were present, so that the index of regularity of the BER was found to be low (about 25 %). The later tracings showed a progressive normalization of the slow waves associated with an increase in their amplitude. Finally, a normal BER was re corded on the 36th postoperative hour. Then, the index of regularity was about 80 %, while the amplitude of the slow waves reached 0.85 ± 0.08 mV and their frequency about 15 cpm. A great number of bursts of spikes occurred in the early postoperative period. Thus, the percentage of fast activity reached 44 ± 18 % immediately after the operation. This value is greater than the percentage usually observed in the jejunum under resting conditions (about 30 %). On the 12th postoperative hour, the percentage of fast activity decreased to 19 ± 7 %. Then, a progressive increase occurred and a normal percentage was observed on the 36th postoperative hour (fig. 2; table I). Ileum. The pattern of the electrical activity at the level of the ileum was similar, but slower than that observed at the level of the jejunum: the BER was greatly disturbed immediately after the operation and it normalized pro gressively within 48 h. On the 48th hour, the index of regularity was found to be about 80%, the amplitude of the slow waves, 0.75 ± 0.10 mV, and their fre quency, about 10 cpm. Similarly, a high percentage of fast activity was noted immediately after the operation, as was the case at the level of the jejunum. After a decrease on the 12th postoperative hour, the percentage of fast activity increased progressively and normalized about 48 h after the operation (table I). Colon. A completely disorganized BER was observed in the colon during the first 24 postoperative hours. During this time, the index of regularity was less than 5 %. The normalization of the BER occurred within 72 h. Then, the index o f regularity was about 90 %, the amplitude of the slow waves 2.10 ± 0.30 mV and their frequency about 6 cpm. No fast activity was observed before the 36th postoperative hour. Later, some bursts of spikes occurred. Nevertheless, the percentage of fast activity remained low and it reached normal values as from the 72nd postoperative hour only (fig. 3; table 1). Stomach. The tracings were also disturbed immediately after the operation at the level of the stomach. Nevertheless, a relatively great number of slow waves with a normal aspect occurred immediately after the surgical procedure, so that the index of regularity was relatively high (about 45 %). Progressively, all the slow waves became regular and a normal BER was observed on about the 24th postoperative hour. At this time, the value of the index of regularity was about 98 %, the amplitude of the slow waves 0.80 ± 0.02 mV and their frequency about 4.5 cpm. The percentage of fast activity was very low during the early postoperative period: thus, it was less than 5 % during the 1st postoperative hour. Later tracings showed a progressive increase of this percentage. Finally, it normalized within about 24 h after tire operation (table I).
Jejunum
1 12 24 36 48 60 72
24.2 t 7.3 44 ± 18 37.4 ± 9.4 19 t 7 56.0 ± 11.3 82.4 i 9.7 37 ± 9 81.0 ± 12.4 41 ± 7 24 t 8 78.2 ± 8.5 84.2 ± 6.3 29 ± 10
index of regularity of the BER %
percentage of fast activity
Stomach
Colon
Ileum
00 ♦1 m
index of regularity of the BER %
percentage of fast activity
index of regularity of the BER %
20.1 25.2 45.0 68.1 80.4 80.0 85.6
34 ± 15 12 t 7 25 ± 6 31 ± 9 39 ± 12 37 ± 10 32 ± 12
less than 5 less than 5 less than 5 less than 5 less than 5 12.4 ± 7.1 37.2 ± 8.4 less than 5 12 ± 8 65.3 ± 6.2 76.4 ± 17.5 30 ± 12 18 ± 9 90.3 ± 9.9
± 5.4 ± 8.1 ± 11.0 ± 10.3 t 8.5 ± 9.4 ± 8.5
percentage of fast activity
index of regularity of the BER %
percentage of fast activity
45.8 69.4 98.0 98.0 93.2 97.1 98.6
less than 5 less than 5 9±5 12 ± 7 8±5 7*4 11 ± 5
± 2.6 ± 2.3 ± 1.0 ± 1.1 ± 1.0 ± 1.2 ± 1.0
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Post operative time, h
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Table I. Index of regularity of the BF.R and percentage of fast activity at the levels of jejunum, ileum, colon and stomach in each stage of the study (mean values ± SEM)
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Duration o f 'Physiological'Ileus The patients have passed flatus on about the 70th postoperative hour (mean duration of the ‘physiological’ ileus ± SEM: 70 ± 8 h).
Analysis of the results presented in this study requires that normal electro myographic state is known in man. Numerous works have been carried out in this field by use of intraluminal devices. Such techniques were extensively employed to study the electrical activity of stomach and colon in normal sub jects (13 15, 20, 21, 24, 32, 40). Small bowel electromyography is less well known because intraluminal techniques cannot be used in normal subjects for studying this part of the gastrointestinal tract. Nevertheless, some authors have obtained tracings by placing electrodes in exteriorized segments of bowel (17) or during surgery (16, 36). These studies demonstrate that intestinal electrical activity recorded in man can be compared to that obtained in other mammals, such as dog and cat. Especially BER has always been noted to exhibit little variations in frequency and amplitude. Thus, it seems that tracings obtained in our work can be considered as normal when the different parameters of slow waves (index of regularity, amplitude, configuration) have reached a steady state. Possible artefacts resulting from the medications which were given to the patients may be excluded since it is well known that BER is little or not affected by pharmacological substances. Most workers have reported that general anaes thesia (27), cholinergic and adrenergic blocking or mimicking agents (5, 9, 10, 18, 31, 38), ganglion-blocking drugs (31, 20), morphine (27) or pentobarbital (27) only slightly change BER frequency, but do not disturb BER amplitude or configuration. Numerous studies of gastrointestinal motility after abdominal surgery have been carried out by several authors in the last decades. All the reports have been in agreement about the fact that intestinal motility is not abolished during the early postoperative period. Farrar and Ingelfinger (23), using audiometrical techniques, have noted that some gastrointestinal contractions are present im mediately after an abdominal operation. Nachlas et al. (33) reported that barium instilled into the bowel during the operation progressed slowly through the gastrointestinal tract in the early postoperative period. Our observations are in agreement with these findings because of the persistence of electrical fast activity observed during the whole postoperative period. Moreover, immediately after the operation, fast activity was more marked than under the resting con ditions. These observations suggest that intestinal motor activity can be in creased in the early postoperative period. In fact, this phenomenon has been previously noted by Baker and Dudley (2) who carried out studies of abdominal
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Comments
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sounds in surgical patients. Today, the cause of this increased motor activity is not clearly established, but it can be thought that handling of the bowel during the operation may play a role. Although intestinal contractions are present during the immediate postoperative period, it appears that they produce only a few propulsive movements. Nachtas et al. (33) have noted that the transit time of a barium bolus through all intestinal segments is considerably longer during the first 24 hours after abdominal surgery than under resting conditions. This phenomenon might be correlated with a disturbance in coordination of intestinal motility. This hypothesis is supported by our observation that, during the im mediate postoperative period, the BER was always abnormal. Indeed, it is well established that the BER has a preponderant role in the occurrence and the propagation of muscular contractions, and it can be suggested that the distur bances of the BER are responsible for the lack of large propulsive movements during the early postoperative period. In the present study some differences have been noted in the delay of the normalization of the electrical activity after surgery between the various seg ments of the digestive tract. Almost similar data have been previously reported as far as the gastrointestinal motility is concerned (25, 26, 39, 43). All these authors have outlined that the recovery of the normal motility occurs in the small intestine within 36 h, in the stomach within 48 h and in the colon within more than 48 h. Thus, our findings concerning the small bowel and the colon are in agreement with the results of these investigators since the normalization of the BER has been noted in our patients within 36 h in the jejunum, 48 h in the ileum and 72 h in the colon. The good correlation between the time of normal ization of the BER in the colon and the time at which the patients have passed flatus gives further evidence of the role of this organ in the duration of postoper ative ‘physiological’ ileus. Only for the stomach, our results are not entirely in agreement with the data provided by the conventional investigations, in partic ular with radiological methods. Indeed, radiological studies indicate that the gastric motor activity does not return to the normal pattern before the 48th postoperative hour. However, in all our patients, a normal BER has been observed at the level of the stomach as early as 24 h after the operation. It must be noted that, when radiological methods are used, gastric motility is considered as normal when barium passed through the gastroduodenal junction (33). Now, some authors have reported that a noticeable increase of the pyloric tone usually occurred after abdominal surgical procedures (29). Thus, it can be thought that the long delay observed for the recovery of a normal gastric motility with radiological methods is related to the hypertony of the gastroduodenal junction, and does not reflect the real time of the normalization of the motor activity of the stomach. Based on our electrical activity study, the gastric motility seems to be normalized within about 24 h after the operation. These findings are in agreement with the data reported by Sarna et al. (41).
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It is well established in animals that postoperative ileus results from sympathetic inhibition mediated by a spinal reflex and this is generally accepted as being also true for man (1, 11, 19, 34, 44). The present study brings further indications about the mechanisms of paralytic ileus. It demonstrates that post operative motility is not abolished but only disorganized, and that failure of propulsive movements results from the loss of their coordination by BER. Precise relationships between disturbances of electrical activity of smooth muscle cells and sympathetic inhibition remain to be established. Nevertheless, some cellular mechanisms may be suggested hypothetically. One of these mechanisms could be an alteration of nexuses which are actually thought to constitute the anatomical support of intracellular coupling. Thus, smooth muscle cells may depolarize in an uncoordinated manner as evoked by BER irregu larities. Another mechanism may be that there are disturbances of the rela tionships between circular and longitudinal muscle layers, so that synchroniza tion of the movements of each layer is transiently abolished, resulting in the absence of organized peristaltic movements. A third mechanism may be that stimulation of inhibitory neurons of the enteric plexuses is involved in sympa thetic inhibition, resulting in an interruption of the neuronal modulation of intestinal motility.
References
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1 Abe, li: Apperi, H E ., and Howard, J.M.: Hemodynamic observations of adynamic ileus in the conscious dog. Ann. Surg. 179: 332 - 338 (1974). 2 Baker, /.. W. and Dudley, H.A.: Ascultation of the abdomen in surgical patients. Lancet «.517-519(1961). 3 Bass. P.: Code, C.F., and l.ambert, E.H.: Motor and electric activity of the duodenum. Am. J. Physiol. 201: 287-291 (1961). 4 Bass, P.: In vivo electrical activity of the small bowel; in Code Handbook of physiol ogy, vol. 4, sect. 6, pp. 2051 2074 (Williams & Wilkins, Baltimore 1968). 5 Berkson, J.: Electromyographic studies of the gastrointestinal tract. V. Further inquiries into the origin of potential variations of the small intestine by means of several drugs. Am. J. Physiol. 105: 450 453 (1933). 6 Bortoff, A.: Slow potential variations of small intestine. Am. J. Physiol. 201: 203-208 (1961). 7 Bozler, E.: Electrophysiological studies on the motility of the gastrointestinal tract. Am. J. Physiol. 127: 301-307 (1939). 8 Bozler, E.: Reflex peristalsis of the intestine. Am. J. Physiol. 157: 338-342 (1949). 9 Bunker, C.E. and Nelsen, T.S.: Use of the electroenterogram to determine pacemaker activity of the small intestine. Surg. Forum 15: 293 (1964). 10 Castleton, K.B.: An experimental study of the movements of the small intestine. Am. J. Physiol. 107: 641-646 (1934). 11 Catchpole, B.N.: Ileus; use of sympathetic blocking agents in its treatment. Surgery, St Louis 66: 811-820 ( 1969).
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Neely, J.: The effects of analgesic drugs on gastrointestinal motility in man. Br. J. Surg. 56: 925-929 (1969). 35 Nelsen, T.S. and Baker. J.C.: Simulation of the electrical and mechanical gradient of the small intestine. Am. J. Physiol. 214: 749-757 (1968). 36 Nielubowicz, J.: Folga, J., and Wiekowska, W.: Electroenterolography. Archs Surg., Chicago 90: 698-707 (1965). 37 Prosser, C.L. and Borloff, A.: Electrical activity of intestinal muscle under in vitro conditions; in Code Handbook of physiology, vol. 4, sect. 6, pp. 2025—2050 (Williams & Wilkins, Baltimore 1968). 38 Puestow, C.B.: Studies on the origin of automaticity of the intestine: the action of certain drugs on isolated intestinal transplants. Am. J. Physiol. 106: 682-688 (1933). 39 Bothnie, N.G.: Harper, N.A.K., and Catchpole, B.N.: Early postoperative intestinal motility. Lancet ii: 64-67 (1963). 40 Salducci, J. et Monges, H.: Etude électromyographique du duodénum chez l’homme normal. Archs Mal. Appar. dig. 59: 19-28 (1970). 41 Sarna, S.K.; Bowes, K.L., and Daniel, E.E.: Postoperative gastric electrical control activity (E.C.A.) in man; in Daniel Proc. 4th Int. Symp. on Gastrointestinal Motility, Banff 1973, pp. 73-83 (Mitchell, Vancouver 1974). 42 Weisbrodt, JV. W. and Christensen, J.: Electrical activity on the cat duodenum in fasting and vomiting. Gastroenterology 63: 1004-1010 (1972). 43 Wells, C; Rawlinson, K.: Tinckler, /.., Jones, //.. and Saunders, J.: Ileus and postoper ative intestinal motility. Lancet ii: 136-137 (1961). 44 Wilson, J.P.: Postoperative motility of the large intestine in man. Gut 16: 689-692 (1975). 34
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J.F. Grenier, Pavillon chirurgical B, Hospices civils, F 67005 Strasbourg Cedex (France)
