Postoperative Electromyographic
Profile
in Human Jejunum
CHRISTIAN DUCERF, M.D., CLAUDE DUCHAMP, M.D., and MICHEL POUYET, M.D.
The postoperative electromyographic profile of the proximal je-
junum and its evolution during recovery from surgery were defined in fasted humans after cholecystectomy. An intraluminal probe supporting four groups of bipolar electrodes was transnasally inserted at the end of surgery to allow continuous recording of jejunal electrical activity over 4 consecutive days. Electromyographic activity was characterized by an early reappearance of phase 3 of migrating myoelectric complexes (MMC) lasting 5.2 ± 0.6 minutes and occurring at 38.1 ± 3.1-minute intervals at day 1 after surgery. During the 4 days after surgery, there was an increased duration of MMC, mainly consisting of phase 2 occurrence with an increased duration and lengthening of the MMC cycle. The amplitude of spikes during phase 3 increased. During the postoperative period, characterized by an inversion of the circadian rhythm, the velocity of propagation was higher (p < 0.05) between 18:00 and 06:00 (4.0 ± 0.5 cm/minute) than between 06:00 and 18:00 (3.1 ± 0.3 cm/minute). In contrast, the duration of phase 2 was lower during nighttime (18:00 to 06:00) than during daytime. The authors conclude that during the early (1 to 2 days) period after cholecystectomy, the jejunal electromyographic activity is limited to phase 3 activity, but that a normal fasted pattern is recovered after 4 days. A progressive reorganization and coordination of the intestinal tract may account for this delay.
P5 OSTOPERATIVE ILEUS IS characterized by tempo-
rarily impaired gastrointestinal motility causing discomfort, increased morbidity rate, and prolonged hospitalization. After operation, the slowed transit ofsolids is subsequent to the suppression of the migrating burst of action potentials and contractions,' which are observed throughout the gut during fasting in humans.2-5 The interdigestive electromyographic (EMG) activity of the small bowel of humans displays a cyclic pattern, characterized by the interdigestive migrating myoelectric complex (MMC). This complex consists of three succesAddress reprint requests to C. Ducerf, M.D., H6pital de la CroixRousse, Clinique Chirurgicale A, 93, Grande-Rue de la Croix-Rousse, F-69004, Lyon, France. Accepted for publication July 1, 1991.
237
From the Clinique Chirurgicale A, H6pital de /a Croix-Rousse, Lyon, France
sive phases4: a quiescent phase 1 with slow waves only; a phase 2 with increasing action potential activity superimposed on some slow waves; and a phase 3 of maximal activity with action potentials on every slow wave, lasting several minutes. A phase 4 of rapid return to phase 1 is sometimes described. Correspondingly, the cyclic motor activity of the small intestine has little or no contractile activity in phase 1, intermittent and irregular contractions during phase 2, and a maximal rate of contraction during phase 3.4967 Inhibition of intestinal EMG activity is considered to be transient in gastric antrum and of short duration in the small bowel, suggesting that the postoperative ileus is only a colonic problem.8 The radiographic characterization of early motility of the gastrointestinal tract after surgery was recognized many years ago.9 Several observations report that MMC are present in the upper intestine during the early postoperative period,'0'2 whereas others indicate a late recovery after surgery.'3'4 All these studies focused on the early restoration of MMC in the upper intestine, or on the characterization of this activity at a given time after surgery, but only two of them"1,12 described the evolution of intestinal EMG activity during the first days of surgical recovery. The main result of the previous report" was the early reappearance ofphase 3 activity in the small bowel, in addition to a recovery of normal activity after gas expulsion, which was marked by an EMG disorganization. The aim of this study was to verify this pattern of recovery but also to go into the temporal evolution of the phenomenon in the course of the first 4 postoperative days. In particular we wanted to reexamine the question of the EMG disorganization before the normal transit recovery. Therefore, the present study was designed to pro-
DUCERF, DUCHAMP, AND POUYET
238
vide more information on the different patterns of the jejunal electromyographic activity after abdominal surgery and on the continuous evolution of this pattern after a single type of surgery, cholecystectomy, using an intraluminal probe introduced by nasal route.
Patients and Methods Patients The protocol was approved by the ethical committee Claude Bernard University Review Board for Human Studies). Between 1989 and 1990, the EMG activity of the upper intestine was investigated in 10 patients aged 50 to 80 years, seven women and three men, after abdominal surgery consisting of cholecystectomy. All patients underwent surgery at approximately the same time of day. Recordings were performed immediately after abdominal closure and continuously over 4 days after surgery. Anesthesia was realized with phenoperidine (R1406, Janssen LeBrun, Paris, France) as morphinomimetic, at a dose of 2 to 6 mg according to the duration of operation, but always administered more than 30 minutes before the end of operation. Postoperative treatment consisted of rehydration, antibiotics, and preventive heparin therapy. Opiate analgesics were excluded in all cases. All patients had normal recovery from abdominal surgery. Informed consent was obtained from each patient, and the probe was withdrawn for patients presenting any sign of discomfort or gastric pain. None of them resorted to this possibility.
Recordings Continuous recordings of the first 60 cm of the upper intestine were obtained by an intraluminal probe derived from that of Fleckenstein6 and the one previously described by Pouyet et al. " The intraluminal probe consisted of a sterilizable polyvinyl tube (150 cm in length and 8 mm in diameter) supporting four groups of two electrodes placed at 5-mm intervals, the groups being 7 cm apart, and one ground electrode. The first group was located 7 cm from the tip. Each electrode (0.1 1 mm in diameter) consisted of a ring of nickel-chrome wire (80% to 20%; Johnston Matthey Metals Ltd, London, UK) fixed around the probe. The sensor consisted of three separated tubes: a large one, ending at the top of the sensor for parenteral nutrition; a smaller one, ending at 100 cm of the distal end for gastric emptying; and the smallest, in the lumen of which the wires leading from the electrodes to the recorder were inserted to exit at the distal end. The probe was introduced transnasally at the end of surgery before abdominal closure, with manual guidance to pass over the pylorus, and positioned so that the gastric aperture was at the level of the pyloric antrum and the
Ann. Surg. * March 1992
four groups of electrodes were in the jejunum. During postoperative recovery, the position of the probe was ascertained by x-ray radiography, showing the probe with a radiopaque signal at the top ofthe probe and the ground electrode located 25 cm from the top. The probe was localized in relation to its position from the ligament of Treitz. The free ends of the wires were connected to an eightchannel polygraph (Reega VIII, Alvar, Paris, France), and bipolar recordings were performed with a short time constant (0.01 second) at a paper speed of 1.2 cm/minute, or at a larger time constant (0.8 second) and paper speed (2.4 cm/second) for slow wave recording. The parameters studied were the duration of MMC, the respective durations of each phase of MMC, and the duration, amplitude, and migrating velocity of phase 3. The MMC was divided into three sequential phases: phase 1 was characterized by the absence of activity or the presence of some occasional spike potentials; the criteria of phase 2 was the appearance of irregular activity that increases in intensity throughout the phase, until the phase 3 occurrence. Phase 1 duration was obtained by subtracting the duration of phase 2 from the total duration of MMC. Phase 4 was not considered. We did not measure the amplitude of every spike burst because it would have represented a considerable number of measurements and it was difficult to distinguish every spike burst of one phase 3 episode at the paper speed used. The mean amplitude of the spike bursts was obtained by a planimetric method, allowing the measurement of the envelope area around each phase 3 complex, and thereby the mean amplitude of phase 3. This enabled a consistent decrease of the number of measurements.
Statistical Analysis Results are expressed as mean ± standard error of the mean (SEM). The values were pooled and averaged in each patient per periods of 6 hours per day through the 4 days of the study. The means ± SEM values were calculated from the mean values of each parameter on each period of time per subject. Statistical significance of parameter evolution through surgical recovery was assessed by one-way analysis of variance followed by paired Student's t test. Results
Clinical Observations All patients had normal postsurgical recovery as evidenced by the absence of abnormal clinical signs and the presence of gas expulsion between the second and third day after surgery. The mean hospitalization duration was 7 days.
VOl. 215.- NO. 3
239
POSTOPERATIVE ELECTROMYOGRAPHIC PROFILE min a
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Jejunal EMG Profile After Surgery Electromyographic recordings 3 hours after surgery demonstrated the presence of phase 3 lasting 5.2 ± 0.6 minutes and occurring at 38.1 ± 3.1-minute intervals during the first 6 hours of recording in jejunum, as shown in Figure 1. These "ectopic" complexes were characterized by the absence of phase 2, however, and were composed only of the quiescent phase 1 and repetitive bursts ofspikes similar to the phase of regular spiking activity or phase 3 of the MMC. These peculiar complexes are called postoperative migrating myoelectric complexes. During the quiescent period, the slow waves appeared regularly at a rhythm of 12.2 ± 0.2 per minute.
Jejunal EMG Recovery After Surgery The duration of postoperative MMC increased progressively (F = 2.1; p < 0.05) from 38.1 ± 3.1 minutes at day 1 (just after operation) to 67.8 ± 10.2 minutes at day 4 of surgical recovery (Fig. 2). Concomitantly, the duration of phase 2 progressively increased from 2.1 ± 0.9 minutes (day 1, 12:00 to 18:00) to 42.2 ± 6.8 min (F = 11.7; p < 0.001), until a normal pattern and characteristics of MMC were reached (phase 1: 31%; phase 2: 62%; phase 3: 7%) corresponding to those reported in the literature.4 A significant variation (F = 2.2; p < 0.01) was observed in phase 3 duration through the 4 days of recovery, mainly because of a small increased duration at day 2 (Fig. 2, Table 1). In parallel, the mean amplitude of spike bursts during phase 3 progressively increased from 0.39 ± 0.01 mV at day 1 to 0.52 ± 0.01 mV at day 4 (F = 2.6; p < 0.01) (Table 1). The velocity of phase 3 (Fig. 3) decreased progressively from day 1 to day 4 of recovery, but not regularly (F = 4.4; p < 0.001). Indeed, a circadian variation of the migrating velocity was observed: during day 2, the velocity of propagation was lower (3.1 ± 0.2 versus 4.0 ± 0.3 cm/minutes; p < 0.01) during daytime (06:00 to 18:00) than during nighttime (18:00 to 06:00). No significant nyctohemeral variation was detected at day 3, whereas lower velocity (p < 0.05) was recorded during
nighttime (18:00 to 06:00) at day 4 (3.0 ± 0.2 versus 3.6 ± 0.2 cm/minute, p < 0.01) than during daytime (Fig. 4). A nyctohemeral variation also appeared in the duration of phase 2, as reported in Figure 3, with maximal values during day time, but not in duration of phase 1, phase 2, and MMC, nor in amplitude of phases 2 and 3. In contrast, the rhythm of slow waves appeared unchanged over the 4 days of surgical recovery, as could be observed from partial recordings at longer time constants performed at different days after surgery. Further, because the tube did not incorporate suction to keep the electrodes applied to the mucosa, it could have induced an intermittent identification of slow waves. Therefore, the evolution of slow waves was not monitored during the time course of surgical recovery. Discussion
Our study confirms that MMC are present in humans in early surgical recovery, thereby confirming earlier observations. '02 It also describes for the first time the pattern of total recovery as well as the nyctohemeral variations up to the fourth day in fasted state. Other studies have reported the first postoperative occurrence of MMC between the second and fifth days after surgery'3 or between the sixth and ninth days.'4 In contrast, Dauchel et al.'" did not find MMC after cholecystectomy, but only disorganized slow waves during the first 36 hours. In a previous study, we showed that the common feature of intestinal electrical recovery"1 may be divided into three phases: a first one of early reappearance of postoperative myoelectric complexes lasting about 90 hours, a very short second phase of EMG disorganization just after gas expulsion, and then, a third phase of normalized MMC. The present study confirms the first part of this pattern, but failed to indicate an EMG disorganization. The profile of recovery after cholecystectomy was characterized by an early electric spiking activity of the small bowel, which resulted atjejunal level, in a higher frequency and lower duration of isolated and ectopic phase 3 com-
Ann. Surg. * March 1992
DUCERF, DUCHAMP, AND POUYET
240
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MG. 2. Four-day postoperative electromyographic profile of the jejunum in one patient 3 hours after cholecystectomy. Diagrammatic representation of the electromyogram for the four groups of electrodes at, respectively, 10, 17, 24, and 31 cm from the ligament of Treitz. Black columns show the phases of regular spiking activity (phase 3). Open areas show irregular spiking activity (phase 2). Note that phase 3 is present at the beginning of the night time. first recording session. -,
pared with values of MMC in normal subjects reported elsewhere.23'5'7 The values we report here in human jejunum are in agreement with those previously reported" I during the first 24 postoperative hours. In the present study, the higher velocity of propagation (3.9 ± 0.2 cm/ minute) compared with the previously referred works may be explained by a more proximal position of the jejunal electrodes, because the migration velocity gradually decreases along the small bowel.2'4 5 These results also may be compared with values reported in human duodenum,'3 either for total duration of complexes (41.9 ± 3.4 minutes), or of phase 2 (5.7 ± 1.0 minutes) and phase 3 (4.7 ± 0.3 minutes) between the second and fifth postoperative
days.'3 They are also in agreement with some early postoperative duodenal values,'0 but at variance with others.'2 Indeed, in the latter study also performed on cholecystectomized patients but with serosal electrodes implanted in the duodenum, the frequency of occurrence of phase 3 was very low at day 1 after surgery, and increased thereafter,'2 contrary to the results of the present study. After surgery, the early appearance and permanence of electrical activity limited to phase 3 episodes suggest that they play an important role in maintaining a functional small intestine. This early high frequency of phase 3 is probably not related to the presence of the sensor because no significant mechanical effect of intraluminal probe was
TABLE 1. Postoperative Characteristics ofPhase 3 of Migrating Myoelectric Complexes in 10 Patients at Different Days (D) After Cholecystectomy
Duration (min)
Amplitude (mV) Di
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D3
D4
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D2
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0.54 ±0.01
0.52 ±0.01
5.2 ±0.6
+0.5
Mean ± SEM.
5.9
D3
D4
5.7 ±0.5
5.4 ±0.4
Vol. 215 . No. 3
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POSTOPERATIVE ELECTROMYOGRAPHIC PROFILE
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found in comparison with muscular implanted electrodes.'6 According to their role of "housekeeper,"'7 phase 3 episodes ensure the homeostasis of the bacterial content of the small bowel in preventing bacterial overgrowth.7"8 Therefore, they might be useful in repelling the colonic flora after surgery. The frequent occurrence of phase 3
5.0
FIG. 4. Postoperative nyctohemeral variations in the propagation velocity (cm/min) of phase 3 over 4 days (D1-D4) after cholecystectomy (mean + SEM, n = 10 patients). Each day is divided into periods of 6 hours. **p < 0.01 vs. the pre-
persisted until the recovery of phase 2, whereas the propagation velocity decreased. The reappearance of phase 2 episodes induced an increased duration of postoperative complexes. In contrast, no significant increase in duration of the complexes was found between the second and fifth postoperative days by Stoddard et al., 13 but these authors
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242
DUCERF, DUCHAMP, AND POUYET
did not continuously monitor the EMG activity during this period. It is generally accepted that MMCs originate in the gastroduodenal area and mainly (50% to 60%) in the duodenum.4'5 In patients, the removal of the gastric antrum after the Billroth II procedure is associated with a striking increase in the frequency of the phase 3 activity fronts recorded by a manometric probe,'9 as observed either after truncal vagotomy with splanchnicectomy" and after complete denervation of an autotransplanted intestinal loop.2' Therefore, it may be assumed that the gastric antrum continuously reduces the intestine's own frequency of MMC occurrence.22 After surgery, duodenal motor activity usually returns well before gastric contractions appear.9"'0 In this case, the absence of inhibitory influences related to gastric motor activity on the duodenum may explain the observed increased number of jejunal phase 3 activity fronts. It has been shown that the delay in the return ofgastric motility after abdominal surgery was the consequence of disordered electrical control activity of the stomach.23 The progressive (2 to 3 days) reappearance of normal MMC ofthe jejunum would seem to be related to an improvement of gastroduodenal coordination, but further experimental investigation is required to confirm this hypothesis. Conversely, our results show a circadian variation in the durations of phase 2, and of migration velocity in the postoperative period. Some circadian variations in MMC propagation velocity have been reported in upper intestine of healthy humans,24 with a higher propagation velocity during daytime than during the night. In the present study, phase 3 propagated at a higher velocity between 18 and 6 hours than between 6 and 18 hours during the second day, whereas normal circadian variations appeared on the fourth postoperative day. This suggests that the disruption of the circadian modulation system, induced by surgery or anesthesia, takes at least 3 days to return to normal. It is generally accepted that the enteric nervous system is able to program and integrate enteric motor activity,4,25 and it was suggested that the variation in propagation of the MMC reflected the speed of transmission within the enteric nervous system.24 In cholecystectomy, the integrity of the small bowel is preserved. Therefore, the disruption of the enteric nervous system could be attributed rather to the effect of anesthesia, or laparotomy, because it was shown in dogs and sheep that laparotomy induced a complete inhibition of electrical spiking activity26 and thus would be liable to disorganize such a system. Laparotomy rather than anesthesia may be the important variable. The observed enteric oscillation, however, also could be a consequence of circadian modulation by the central nersuggested by the nocturnal reduction of phase 2 reported here. This phenomenon is to be compared with the known reduction of the irregular contractions of phase II during sleep,27'28 suggesting that the sleepvous system, as
Ann. Surg. * March 1992
waking pattern can modulate enteric activity. It has to be noted that in humans there is a similar period for both MMC and sleep cycles.29 The question arises whether a profound disruption of the sleep-waking pattern after surgery might account for the observed postoperative changes, as well the absence of phase 2s as the inversion of the nyctohemeral cycle. Indeed, during the first day after operation, the patients were rather somnolent most of the time (as we could judge), but they did not appear to be continuously asleep. Thereafter, the 18:00 to 06:00. period included most of the sleep hours. Therefore, the reorganization of the enteric activity seemed to parallel the recovery of a normal sleep-waking pattern. If a reduction of the number of contractions in phase II was found during sleep,27'28 however, no complete disappearance was observed. Thus, this could not be, in our opinion, the simple explanation of the phenomenon. Further, in the absence of electroencephalographic activity recordings in the present study, the nyctohemeral repartition of sleep, as well as the quality of the sleep episodes and the connection with EMG activity, can hardly be appreciated and remain to be determined. The present results failed to indicate a marked EMG disorganization at the time of gas expulsion and just before the normal transit recovery, as was previously found.1' The return to normality was principally achieved by a reorganization of the nyctohemeral variations in the phase 3 propagation velocity at the fourth day after surgery, at a time when the disorganized EMG was reported. This difference with the previous report could result from the different populations studied. The abdominal surgery of the present subjects consisted only of cholecystectomy, whereas in the previous study, only 2 of 20 subjects were cholecystectomized. This suggests that the postoperative recovery pattern may depend on the type of surgery, but further studies are required to clarify this point. In conclusion, the recovery ofjejunal electrical activity after surgery described in this study emphasizes the early presence of phase 3, but the persistence of motor alteration until the fourth day. This delay, accounted for by a progressive reorganization and coordination of the intestinal tract, should be taken into account in postsurgical care. Acknowledgments The authors thank Dr. Bueno and Dr. Fioramonti (Department of Pharmacology, INRA, Toulouse, France) for helpful criticisms of the manuscript, and M. Caussette for technical assistance in constructing the probes.
References 1. Smith J, Kelly KA, Weinshilboum RM. Pathophysiology of postoperativeleus. Arch Surg 1977; 112:203-209. 2. Fleckenstein P, Krogh F, Oigaard A. The interdigestive myoelectrical complex and other migrating electrical phenomena in the human
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13. 14.
15. 16.
POSTOPERATIVE ELECTROMYOGRAPHIC PROFILE
small intestine. In Duthie HL, ed. Gastrointestinal Motility in Health and Diseases. Lancaster: MTP Press, 1978, pp 33-41. Thompson DG, Wingate DL, Archer L, et al. Normal patterns of upper human small bowel motor activity recorded by prolonged radiotelemetry. Gut 1980; 21:500-506. Sarna SK. Cyclic motor activity: migrating motor complex: 1985. Gastroenterology 1985; 89:894-913. Kellow JE, Borody TJ, Phillips SF, et al. Human interdigestive motility: variations in patterns from esophagus to colon. Gastroenterology 1986; 91:386-395. Fleckenstein P. Migrating electrical spike activity in the fasting human small intestine. Am J Dig Dis 1979; 23:769-775. Vantrappen G, Janssens J, Hellemans J, Ghoos Y. The interdigestive motor complex of normal subjects and patients with bacterial overgrowth of the small intestine. J Clin Invest 1977; 59:11581166. Woods J, Erikson L, Condon R, et al. Postoperative ileus: a colonic problem? Surgery 1978; 84:527-533. Rothnie NG, Kemp Harper RA, Catchpole BN. Early postoperative gastrointestinal activity. Lancet 1963; 2:64-67. Catchpole B, Duthie H. Postoperative gastrointestinal complexes. In Duthie HL, ed. Gastrointestinal Motility in Health and Diseases. Lancaster: MTP Press, 1978, pp 33-41. Pouyet M, Denavit M, Roche M, Achard F. Profil electromyographique du jejunum humain apres chirurgie abdominale. Gastroenterol Clin Biol 1985; 9:412-416. Soper NJ, Sarr MG, Kelly KA. Human duodenum myoelectric activity after operation and with pacing. Surgery 1990; 107:63-68. Stoddard CS, Swallwood RH, Duthie HL. Migrating myoelectrical complexes in man. In Duthie HL, ed. Gastrointestinal Motility in Health and Diseases. Lancaster: MTP Press, 1978, pp 9-15. Waterfall W. Electrical patterns in the human jejunum with and without vagotomy. Surgery 1983; 94:186-190. Dauchel J, Schang JC, Kachelhoffer J, et al. Gastrointestinal myoelectrical activity during the postoperative period in man. Digestion 1976; 14:293-303. Fleckenstein P, Oigaard A. Electrical spike potentials of the small bowel: a comparative study of recordings obtained from muscular implanted and intraluminal suction electrodes. Dig Dis Sci 1976; 21:996-999.
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17. Code CF, Schlegel JF. The gastrointestinal interdigestive housekeeper motor correlates ofthe interdigestive myoelectric complex of the dog. In Daniel EE, Gilbert JAL, Schofield B, et al., ed. Proceedings of the Fourth International Symposium on Gastrointestinal Motility. Vancouver: Mitchell Press Ltd, 1974, pp 631-634. 18. Caenepeel P, Janssens J, Vantrappen G, et al. Interdigestive myoelectric complex in germ-free rats. Dig Dis Sci 1989; 34:11801184. 19. Bortolotti M, Bersani G, longanesi A, et al. Modification of the interdigestive migrating motor complex (IMMC) in patients with partial gastrectomy and gastrojejunostomy [abstr]. Gastroenterol Clin Biol 1983; 7:722. 20. Ruckebusch Y, Bueno L. Migrating myoelectric complex of the small intestine: an intrinsic activity mediated by the vagus. Gastroenterology 1977; 73:1309-1314. 21. Sarr MG, Kelly KA. Myoelectric activity of the autotransplanted canine jejuno ileum. Gastroenterology 1980; 78:1251. 22. Laplace JP. Motricite de l'intestin grele: organisation, regulations et fonctions. -Quinze ans de recherches sur les complexes migrants. Reprod Nutr Develop 1984; 24:707-765. 23. Sarna SK, Bowes KL, Daniel EE. Postoperative gastric electrical control activity (ECA) in man. Proceedings of the 4th International Symposium on Gastrointestinal Motility. Vancouver: Mitchell Press, 1973, p 73. 24. Kumar D, Wingate DL, Ruckebusch Y. Circadian variation in the propagation velocity of the migrating motor complex. Gastroenterology 1986; 91:926-930. 25. Wood JD. Enteric neurophysiology. Am J Physiol 1984; 247:G585G598. 26. Bueno L, Fioramonti J, Ruckebusch Y. Postoperative intestinal motility in dogs and sheep. Am J Dig Dis 1978; 23:682-689. 27. Thompson DG, Laidlaw JM, Wingate DL. Abnormal small bowel motility demonstrated by radio-telemetry in a patient with irritable colon. Lancet 1979; ii: 1321-1323. 28. Ritchie HD, Thompson DG, Wingate DL. Diurnal variation in human jejunal fasting motor activity. J Physiol Lond 1980; 305: 54P-55P. 29. Ruckebusch Y, Bueno L. Electrical spiking activity of the small intestine as an ultradian rhythm. Proc Int Union Physiol Sci 1977; 12:787.
Profile
in Human Jejunum
CHRISTIAN DUCERF, M.D., CLAUDE DUCHAMP, M.D., and MICHEL POUYET, M.D.
The postoperative electromyographic profile of the proximal je-
junum and its evolution during recovery from surgery were defined in fasted humans after cholecystectomy. An intraluminal probe supporting four groups of bipolar electrodes was transnasally inserted at the end of surgery to allow continuous recording of jejunal electrical activity over 4 consecutive days. Electromyographic activity was characterized by an early reappearance of phase 3 of migrating myoelectric complexes (MMC) lasting 5.2 ± 0.6 minutes and occurring at 38.1 ± 3.1-minute intervals at day 1 after surgery. During the 4 days after surgery, there was an increased duration of MMC, mainly consisting of phase 2 occurrence with an increased duration and lengthening of the MMC cycle. The amplitude of spikes during phase 3 increased. During the postoperative period, characterized by an inversion of the circadian rhythm, the velocity of propagation was higher (p < 0.05) between 18:00 and 06:00 (4.0 ± 0.5 cm/minute) than between 06:00 and 18:00 (3.1 ± 0.3 cm/minute). In contrast, the duration of phase 2 was lower during nighttime (18:00 to 06:00) than during daytime. The authors conclude that during the early (1 to 2 days) period after cholecystectomy, the jejunal electromyographic activity is limited to phase 3 activity, but that a normal fasted pattern is recovered after 4 days. A progressive reorganization and coordination of the intestinal tract may account for this delay.
P5 OSTOPERATIVE ILEUS IS characterized by tempo-
rarily impaired gastrointestinal motility causing discomfort, increased morbidity rate, and prolonged hospitalization. After operation, the slowed transit ofsolids is subsequent to the suppression of the migrating burst of action potentials and contractions,' which are observed throughout the gut during fasting in humans.2-5 The interdigestive electromyographic (EMG) activity of the small bowel of humans displays a cyclic pattern, characterized by the interdigestive migrating myoelectric complex (MMC). This complex consists of three succesAddress reprint requests to C. Ducerf, M.D., H6pital de la CroixRousse, Clinique Chirurgicale A, 93, Grande-Rue de la Croix-Rousse, F-69004, Lyon, France. Accepted for publication July 1, 1991.
237
From the Clinique Chirurgicale A, H6pital de /a Croix-Rousse, Lyon, France
sive phases4: a quiescent phase 1 with slow waves only; a phase 2 with increasing action potential activity superimposed on some slow waves; and a phase 3 of maximal activity with action potentials on every slow wave, lasting several minutes. A phase 4 of rapid return to phase 1 is sometimes described. Correspondingly, the cyclic motor activity of the small intestine has little or no contractile activity in phase 1, intermittent and irregular contractions during phase 2, and a maximal rate of contraction during phase 3.4967 Inhibition of intestinal EMG activity is considered to be transient in gastric antrum and of short duration in the small bowel, suggesting that the postoperative ileus is only a colonic problem.8 The radiographic characterization of early motility of the gastrointestinal tract after surgery was recognized many years ago.9 Several observations report that MMC are present in the upper intestine during the early postoperative period,'0'2 whereas others indicate a late recovery after surgery.'3'4 All these studies focused on the early restoration of MMC in the upper intestine, or on the characterization of this activity at a given time after surgery, but only two of them"1,12 described the evolution of intestinal EMG activity during the first days of surgical recovery. The main result of the previous report" was the early reappearance ofphase 3 activity in the small bowel, in addition to a recovery of normal activity after gas expulsion, which was marked by an EMG disorganization. The aim of this study was to verify this pattern of recovery but also to go into the temporal evolution of the phenomenon in the course of the first 4 postoperative days. In particular we wanted to reexamine the question of the EMG disorganization before the normal transit recovery. Therefore, the present study was designed to pro-
DUCERF, DUCHAMP, AND POUYET
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vide more information on the different patterns of the jejunal electromyographic activity after abdominal surgery and on the continuous evolution of this pattern after a single type of surgery, cholecystectomy, using an intraluminal probe introduced by nasal route.
Patients and Methods Patients The protocol was approved by the ethical committee Claude Bernard University Review Board for Human Studies). Between 1989 and 1990, the EMG activity of the upper intestine was investigated in 10 patients aged 50 to 80 years, seven women and three men, after abdominal surgery consisting of cholecystectomy. All patients underwent surgery at approximately the same time of day. Recordings were performed immediately after abdominal closure and continuously over 4 days after surgery. Anesthesia was realized with phenoperidine (R1406, Janssen LeBrun, Paris, France) as morphinomimetic, at a dose of 2 to 6 mg according to the duration of operation, but always administered more than 30 minutes before the end of operation. Postoperative treatment consisted of rehydration, antibiotics, and preventive heparin therapy. Opiate analgesics were excluded in all cases. All patients had normal recovery from abdominal surgery. Informed consent was obtained from each patient, and the probe was withdrawn for patients presenting any sign of discomfort or gastric pain. None of them resorted to this possibility.
Recordings Continuous recordings of the first 60 cm of the upper intestine were obtained by an intraluminal probe derived from that of Fleckenstein6 and the one previously described by Pouyet et al. " The intraluminal probe consisted of a sterilizable polyvinyl tube (150 cm in length and 8 mm in diameter) supporting four groups of two electrodes placed at 5-mm intervals, the groups being 7 cm apart, and one ground electrode. The first group was located 7 cm from the tip. Each electrode (0.1 1 mm in diameter) consisted of a ring of nickel-chrome wire (80% to 20%; Johnston Matthey Metals Ltd, London, UK) fixed around the probe. The sensor consisted of three separated tubes: a large one, ending at the top of the sensor for parenteral nutrition; a smaller one, ending at 100 cm of the distal end for gastric emptying; and the smallest, in the lumen of which the wires leading from the electrodes to the recorder were inserted to exit at the distal end. The probe was introduced transnasally at the end of surgery before abdominal closure, with manual guidance to pass over the pylorus, and positioned so that the gastric aperture was at the level of the pyloric antrum and the
Ann. Surg. * March 1992
four groups of electrodes were in the jejunum. During postoperative recovery, the position of the probe was ascertained by x-ray radiography, showing the probe with a radiopaque signal at the top ofthe probe and the ground electrode located 25 cm from the top. The probe was localized in relation to its position from the ligament of Treitz. The free ends of the wires were connected to an eightchannel polygraph (Reega VIII, Alvar, Paris, France), and bipolar recordings were performed with a short time constant (0.01 second) at a paper speed of 1.2 cm/minute, or at a larger time constant (0.8 second) and paper speed (2.4 cm/second) for slow wave recording. The parameters studied were the duration of MMC, the respective durations of each phase of MMC, and the duration, amplitude, and migrating velocity of phase 3. The MMC was divided into three sequential phases: phase 1 was characterized by the absence of activity or the presence of some occasional spike potentials; the criteria of phase 2 was the appearance of irregular activity that increases in intensity throughout the phase, until the phase 3 occurrence. Phase 1 duration was obtained by subtracting the duration of phase 2 from the total duration of MMC. Phase 4 was not considered. We did not measure the amplitude of every spike burst because it would have represented a considerable number of measurements and it was difficult to distinguish every spike burst of one phase 3 episode at the paper speed used. The mean amplitude of the spike bursts was obtained by a planimetric method, allowing the measurement of the envelope area around each phase 3 complex, and thereby the mean amplitude of phase 3. This enabled a consistent decrease of the number of measurements.
Statistical Analysis Results are expressed as mean ± standard error of the mean (SEM). The values were pooled and averaged in each patient per periods of 6 hours per day through the 4 days of the study. The means ± SEM values were calculated from the mean values of each parameter on each period of time per subject. Statistical significance of parameter evolution through surgical recovery was assessed by one-way analysis of variance followed by paired Student's t test. Results
Clinical Observations All patients had normal postsurgical recovery as evidenced by the absence of abnormal clinical signs and the presence of gas expulsion between the second and third day after surgery. The mean hospitalization duration was 7 days.
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POSTOPERATIVE ELECTROMYOGRAPHIC PROFILE min a
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FIG. 1. Electromyographic recording of human jejunum with a short time constant (0.01 sec) showing only spiking activity and with a high time constant (0.8 sec) displaying slow waves and spiking activity obtained during the first day after cholecystectomy. The samples shown here are different events on the same subject.
Jejunal EMG Profile After Surgery Electromyographic recordings 3 hours after surgery demonstrated the presence of phase 3 lasting 5.2 ± 0.6 minutes and occurring at 38.1 ± 3.1-minute intervals during the first 6 hours of recording in jejunum, as shown in Figure 1. These "ectopic" complexes were characterized by the absence of phase 2, however, and were composed only of the quiescent phase 1 and repetitive bursts ofspikes similar to the phase of regular spiking activity or phase 3 of the MMC. These peculiar complexes are called postoperative migrating myoelectric complexes. During the quiescent period, the slow waves appeared regularly at a rhythm of 12.2 ± 0.2 per minute.
Jejunal EMG Recovery After Surgery The duration of postoperative MMC increased progressively (F = 2.1; p < 0.05) from 38.1 ± 3.1 minutes at day 1 (just after operation) to 67.8 ± 10.2 minutes at day 4 of surgical recovery (Fig. 2). Concomitantly, the duration of phase 2 progressively increased from 2.1 ± 0.9 minutes (day 1, 12:00 to 18:00) to 42.2 ± 6.8 min (F = 11.7; p < 0.001), until a normal pattern and characteristics of MMC were reached (phase 1: 31%; phase 2: 62%; phase 3: 7%) corresponding to those reported in the literature.4 A significant variation (F = 2.2; p < 0.01) was observed in phase 3 duration through the 4 days of recovery, mainly because of a small increased duration at day 2 (Fig. 2, Table 1). In parallel, the mean amplitude of spike bursts during phase 3 progressively increased from 0.39 ± 0.01 mV at day 1 to 0.52 ± 0.01 mV at day 4 (F = 2.6; p < 0.01) (Table 1). The velocity of phase 3 (Fig. 3) decreased progressively from day 1 to day 4 of recovery, but not regularly (F = 4.4; p < 0.001). Indeed, a circadian variation of the migrating velocity was observed: during day 2, the velocity of propagation was lower (3.1 ± 0.2 versus 4.0 ± 0.3 cm/minutes; p < 0.01) during daytime (06:00 to 18:00) than during nighttime (18:00 to 06:00). No significant nyctohemeral variation was detected at day 3, whereas lower velocity (p < 0.05) was recorded during
nighttime (18:00 to 06:00) at day 4 (3.0 ± 0.2 versus 3.6 ± 0.2 cm/minute, p < 0.01) than during daytime (Fig. 4). A nyctohemeral variation also appeared in the duration of phase 2, as reported in Figure 3, with maximal values during day time, but not in duration of phase 1, phase 2, and MMC, nor in amplitude of phases 2 and 3. In contrast, the rhythm of slow waves appeared unchanged over the 4 days of surgical recovery, as could be observed from partial recordings at longer time constants performed at different days after surgery. Further, because the tube did not incorporate suction to keep the electrodes applied to the mucosa, it could have induced an intermittent identification of slow waves. Therefore, the evolution of slow waves was not monitored during the time course of surgical recovery. Discussion
Our study confirms that MMC are present in humans in early surgical recovery, thereby confirming earlier observations. '02 It also describes for the first time the pattern of total recovery as well as the nyctohemeral variations up to the fourth day in fasted state. Other studies have reported the first postoperative occurrence of MMC between the second and fifth days after surgery'3 or between the sixth and ninth days.'4 In contrast, Dauchel et al.'" did not find MMC after cholecystectomy, but only disorganized slow waves during the first 36 hours. In a previous study, we showed that the common feature of intestinal electrical recovery"1 may be divided into three phases: a first one of early reappearance of postoperative myoelectric complexes lasting about 90 hours, a very short second phase of EMG disorganization just after gas expulsion, and then, a third phase of normalized MMC. The present study confirms the first part of this pattern, but failed to indicate an EMG disorganization. The profile of recovery after cholecystectomy was characterized by an early electric spiking activity of the small bowel, which resulted atjejunal level, in a higher frequency and lower duration of isolated and ectopic phase 3 com-
Ann. Surg. * March 1992
DUCERF, DUCHAMP, AND POUYET
240
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MG. 2. Four-day postoperative electromyographic profile of the jejunum in one patient 3 hours after cholecystectomy. Diagrammatic representation of the electromyogram for the four groups of electrodes at, respectively, 10, 17, 24, and 31 cm from the ligament of Treitz. Black columns show the phases of regular spiking activity (phase 3). Open areas show irregular spiking activity (phase 2). Note that phase 3 is present at the beginning of the night time. first recording session. -,
pared with values of MMC in normal subjects reported elsewhere.23'5'7 The values we report here in human jejunum are in agreement with those previously reported" I during the first 24 postoperative hours. In the present study, the higher velocity of propagation (3.9 ± 0.2 cm/ minute) compared with the previously referred works may be explained by a more proximal position of the jejunal electrodes, because the migration velocity gradually decreases along the small bowel.2'4 5 These results also may be compared with values reported in human duodenum,'3 either for total duration of complexes (41.9 ± 3.4 minutes), or of phase 2 (5.7 ± 1.0 minutes) and phase 3 (4.7 ± 0.3 minutes) between the second and fifth postoperative
days.'3 They are also in agreement with some early postoperative duodenal values,'0 but at variance with others.'2 Indeed, in the latter study also performed on cholecystectomized patients but with serosal electrodes implanted in the duodenum, the frequency of occurrence of phase 3 was very low at day 1 after surgery, and increased thereafter,'2 contrary to the results of the present study. After surgery, the early appearance and permanence of electrical activity limited to phase 3 episodes suggest that they play an important role in maintaining a functional small intestine. This early high frequency of phase 3 is probably not related to the presence of the sensor because no significant mechanical effect of intraluminal probe was
TABLE 1. Postoperative Characteristics ofPhase 3 of Migrating Myoelectric Complexes in 10 Patients at Different Days (D) After Cholecystectomy
Duration (min)
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D4
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0.52 ±0.01
5.2 ±0.6
+0.5
Mean ± SEM.
5.9
D3
D4
5.7 ±0.5
5.4 ±0.4
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found in comparison with muscular implanted electrodes.'6 According to their role of "housekeeper,"'7 phase 3 episodes ensure the homeostasis of the bacterial content of the small bowel in preventing bacterial overgrowth.7"8 Therefore, they might be useful in repelling the colonic flora after surgery. The frequent occurrence of phase 3
5.0
FIG. 4. Postoperative nyctohemeral variations in the propagation velocity (cm/min) of phase 3 over 4 days (D1-D4) after cholecystectomy (mean + SEM, n = 10 patients). Each day is divided into periods of 6 hours. **p < 0.01 vs. the pre-
persisted until the recovery of phase 2, whereas the propagation velocity decreased. The reappearance of phase 2 episodes induced an increased duration of postoperative complexes. In contrast, no significant increase in duration of the complexes was found between the second and fifth postoperative days by Stoddard et al., 13 but these authors
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DUCERF, DUCHAMP, AND POUYET
did not continuously monitor the EMG activity during this period. It is generally accepted that MMCs originate in the gastroduodenal area and mainly (50% to 60%) in the duodenum.4'5 In patients, the removal of the gastric antrum after the Billroth II procedure is associated with a striking increase in the frequency of the phase 3 activity fronts recorded by a manometric probe,'9 as observed either after truncal vagotomy with splanchnicectomy" and after complete denervation of an autotransplanted intestinal loop.2' Therefore, it may be assumed that the gastric antrum continuously reduces the intestine's own frequency of MMC occurrence.22 After surgery, duodenal motor activity usually returns well before gastric contractions appear.9"'0 In this case, the absence of inhibitory influences related to gastric motor activity on the duodenum may explain the observed increased number of jejunal phase 3 activity fronts. It has been shown that the delay in the return ofgastric motility after abdominal surgery was the consequence of disordered electrical control activity of the stomach.23 The progressive (2 to 3 days) reappearance of normal MMC ofthe jejunum would seem to be related to an improvement of gastroduodenal coordination, but further experimental investigation is required to confirm this hypothesis. Conversely, our results show a circadian variation in the durations of phase 2, and of migration velocity in the postoperative period. Some circadian variations in MMC propagation velocity have been reported in upper intestine of healthy humans,24 with a higher propagation velocity during daytime than during the night. In the present study, phase 3 propagated at a higher velocity between 18 and 6 hours than between 6 and 18 hours during the second day, whereas normal circadian variations appeared on the fourth postoperative day. This suggests that the disruption of the circadian modulation system, induced by surgery or anesthesia, takes at least 3 days to return to normal. It is generally accepted that the enteric nervous system is able to program and integrate enteric motor activity,4,25 and it was suggested that the variation in propagation of the MMC reflected the speed of transmission within the enteric nervous system.24 In cholecystectomy, the integrity of the small bowel is preserved. Therefore, the disruption of the enteric nervous system could be attributed rather to the effect of anesthesia, or laparotomy, because it was shown in dogs and sheep that laparotomy induced a complete inhibition of electrical spiking activity26 and thus would be liable to disorganize such a system. Laparotomy rather than anesthesia may be the important variable. The observed enteric oscillation, however, also could be a consequence of circadian modulation by the central nersuggested by the nocturnal reduction of phase 2 reported here. This phenomenon is to be compared with the known reduction of the irregular contractions of phase II during sleep,27'28 suggesting that the sleepvous system, as
Ann. Surg. * March 1992
waking pattern can modulate enteric activity. It has to be noted that in humans there is a similar period for both MMC and sleep cycles.29 The question arises whether a profound disruption of the sleep-waking pattern after surgery might account for the observed postoperative changes, as well the absence of phase 2s as the inversion of the nyctohemeral cycle. Indeed, during the first day after operation, the patients were rather somnolent most of the time (as we could judge), but they did not appear to be continuously asleep. Thereafter, the 18:00 to 06:00. period included most of the sleep hours. Therefore, the reorganization of the enteric activity seemed to parallel the recovery of a normal sleep-waking pattern. If a reduction of the number of contractions in phase II was found during sleep,27'28 however, no complete disappearance was observed. Thus, this could not be, in our opinion, the simple explanation of the phenomenon. Further, in the absence of electroencephalographic activity recordings in the present study, the nyctohemeral repartition of sleep, as well as the quality of the sleep episodes and the connection with EMG activity, can hardly be appreciated and remain to be determined. The present results failed to indicate a marked EMG disorganization at the time of gas expulsion and just before the normal transit recovery, as was previously found.1' The return to normality was principally achieved by a reorganization of the nyctohemeral variations in the phase 3 propagation velocity at the fourth day after surgery, at a time when the disorganized EMG was reported. This difference with the previous report could result from the different populations studied. The abdominal surgery of the present subjects consisted only of cholecystectomy, whereas in the previous study, only 2 of 20 subjects were cholecystectomized. This suggests that the postoperative recovery pattern may depend on the type of surgery, but further studies are required to clarify this point. In conclusion, the recovery ofjejunal electrical activity after surgery described in this study emphasizes the early presence of phase 3, but the persistence of motor alteration until the fourth day. This delay, accounted for by a progressive reorganization and coordination of the intestinal tract, should be taken into account in postsurgical care. Acknowledgments The authors thank Dr. Bueno and Dr. Fioramonti (Department of Pharmacology, INRA, Toulouse, France) for helpful criticisms of the manuscript, and M. Caussette for technical assistance in constructing the probes.
References 1. Smith J, Kelly KA, Weinshilboum RM. Pathophysiology of postoperativeleus. Arch Surg 1977; 112:203-209. 2. Fleckenstein P, Krogh F, Oigaard A. The interdigestive myoelectrical complex and other migrating electrical phenomena in the human
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small intestine. In Duthie HL, ed. Gastrointestinal Motility in Health and Diseases. Lancaster: MTP Press, 1978, pp 33-41. Thompson DG, Wingate DL, Archer L, et al. Normal patterns of upper human small bowel motor activity recorded by prolonged radiotelemetry. Gut 1980; 21:500-506. Sarna SK. Cyclic motor activity: migrating motor complex: 1985. Gastroenterology 1985; 89:894-913. Kellow JE, Borody TJ, Phillips SF, et al. Human interdigestive motility: variations in patterns from esophagus to colon. Gastroenterology 1986; 91:386-395. Fleckenstein P. Migrating electrical spike activity in the fasting human small intestine. Am J Dig Dis 1979; 23:769-775. Vantrappen G, Janssens J, Hellemans J, Ghoos Y. The interdigestive motor complex of normal subjects and patients with bacterial overgrowth of the small intestine. J Clin Invest 1977; 59:11581166. Woods J, Erikson L, Condon R, et al. Postoperative ileus: a colonic problem? Surgery 1978; 84:527-533. Rothnie NG, Kemp Harper RA, Catchpole BN. Early postoperative gastrointestinal activity. Lancet 1963; 2:64-67. Catchpole B, Duthie H. Postoperative gastrointestinal complexes. In Duthie HL, ed. Gastrointestinal Motility in Health and Diseases. Lancaster: MTP Press, 1978, pp 33-41. Pouyet M, Denavit M, Roche M, Achard F. Profil electromyographique du jejunum humain apres chirurgie abdominale. Gastroenterol Clin Biol 1985; 9:412-416. Soper NJ, Sarr MG, Kelly KA. Human duodenum myoelectric activity after operation and with pacing. Surgery 1990; 107:63-68. Stoddard CS, Swallwood RH, Duthie HL. Migrating myoelectrical complexes in man. In Duthie HL, ed. Gastrointestinal Motility in Health and Diseases. Lancaster: MTP Press, 1978, pp 9-15. Waterfall W. Electrical patterns in the human jejunum with and without vagotomy. Surgery 1983; 94:186-190. Dauchel J, Schang JC, Kachelhoffer J, et al. Gastrointestinal myoelectrical activity during the postoperative period in man. Digestion 1976; 14:293-303. Fleckenstein P, Oigaard A. Electrical spike potentials of the small bowel: a comparative study of recordings obtained from muscular implanted and intraluminal suction electrodes. Dig Dis Sci 1976; 21:996-999.
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17. Code CF, Schlegel JF. The gastrointestinal interdigestive housekeeper motor correlates ofthe interdigestive myoelectric complex of the dog. In Daniel EE, Gilbert JAL, Schofield B, et al., ed. Proceedings of the Fourth International Symposium on Gastrointestinal Motility. Vancouver: Mitchell Press Ltd, 1974, pp 631-634. 18. Caenepeel P, Janssens J, Vantrappen G, et al. Interdigestive myoelectric complex in germ-free rats. Dig Dis Sci 1989; 34:11801184. 19. Bortolotti M, Bersani G, longanesi A, et al. Modification of the interdigestive migrating motor complex (IMMC) in patients with partial gastrectomy and gastrojejunostomy [abstr]. Gastroenterol Clin Biol 1983; 7:722. 20. Ruckebusch Y, Bueno L. Migrating myoelectric complex of the small intestine: an intrinsic activity mediated by the vagus. Gastroenterology 1977; 73:1309-1314. 21. Sarr MG, Kelly KA. Myoelectric activity of the autotransplanted canine jejuno ileum. Gastroenterology 1980; 78:1251. 22. Laplace JP. Motricite de l'intestin grele: organisation, regulations et fonctions. -Quinze ans de recherches sur les complexes migrants. Reprod Nutr Develop 1984; 24:707-765. 23. Sarna SK, Bowes KL, Daniel EE. Postoperative gastric electrical control activity (ECA) in man. Proceedings of the 4th International Symposium on Gastrointestinal Motility. Vancouver: Mitchell Press, 1973, p 73. 24. Kumar D, Wingate DL, Ruckebusch Y. Circadian variation in the propagation velocity of the migrating motor complex. Gastroenterology 1986; 91:926-930. 25. Wood JD. Enteric neurophysiology. Am J Physiol 1984; 247:G585G598. 26. Bueno L, Fioramonti J, Ruckebusch Y. Postoperative intestinal motility in dogs and sheep. Am J Dig Dis 1978; 23:682-689. 27. Thompson DG, Laidlaw JM, Wingate DL. Abnormal small bowel motility demonstrated by radio-telemetry in a patient with irritable colon. Lancet 1979; ii: 1321-1323. 28. Ritchie HD, Thompson DG, Wingate DL. Diurnal variation in human jejunal fasting motor activity. J Physiol Lond 1980; 305: 54P-55P. 29. Ruckebusch Y, Bueno L. Electrical spiking activity of the small intestine as an ultradian rhythm. Proc Int Union Physiol Sci 1977; 12:787.
