Quantitative effect of oral feeding on gastrointestinal myoelectric activity in the conscious dog

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Gastrointestinal myoelectric activity was recorded in seven studies in five dogs during two hours of fasting immediately followed by feeding and subsequent recording for four hours. In four studies serial plasma samples were taken for
  Quantitative Effect of Oral Feeding on Gastrointestinal Myoelectric Activity in the Conscious Dog DAVID WINGATE, FRCP, ELIZABETH PEARCE, MA, ANNE LING, MIScT, BARBARA BOUCHER, FRCP, HILARY THOMPSON, FRCS, and MICHAEL HUTTON, BA Gastrointestinal myoelectric activity was recorded in seven studies in five dogs during two hours of asting immediately followed by feeding and subsequent recording for four hours. In four studies serial plasma samples were taken for radioimmunoassay of insulin and gastrin. In all animals there was a significant reduction P < 0.01) in gastric basic electri- cal rhythm BER) frequency on feeding which was sustained throughout the postprandial period. There was no change in the duodenal BER. Feeding induced a significant P < 0.01) increase in overall jejunal and ileal but not duodenal) spike activity. Ileal but not jejunal) spike activity again increased significantly P < 0.05) after the first two post- prandial hours. The changes in serum gastrin or in serum insulin did not appear to ac- count for most of the observed changes in myoelectric activity, suggesting that other humoral and~or neural factors mediate the response to food. The discovery of the migrating myoelectric com- plex of the fasting dog (1) less than a decade ago has transformed the study of myoelectric activity. Since that time it has been shown that the fasting myo- electric complex is common to several (if not all) mammalian species. In carnivores (2) the sequence of migrating complexes is interrupted on feeding at all levels of the intestine and replaced by inter- mittent spike activity (3). The cause of this change is not known, but changes of patterns of myo- electric activity similar to those found on feeding have been induced in the dog with pentagastrin (4, 5) and with insulin (6). The aim of this study was to measure the canine myoelectric response to feeding and to compare it with the changes in serum concentrations of insulin From the Department of Gastrointestinal Science, London Hospital Medical College, London, England. This project was carried out under the grants from the Well- come Trust, the University of London Central Research Fund, and the Medical Research Council of Great Britain. Address for reprint requests: Dr. David Wingate, London Hospital, Whitechapel Road, London E1 IBB, England. and gastrin, previously implicated as mediators of the myoelectric response to food. The design of the experiments, which each included an initial 2-hr fasting period allowed each animal to act as its own fasting control. Replicate studies of myoelectric ac- tivity were carried out on two of the animals. It should be emphasized that the choice of the peptides for assay was prompted by data reported by other workers (4-6), although it is now clear that feeding induces the release of a number of intestinal peptides. In particular, cholecystokinin has close affinities to gastrin in its effects on myoelectric ac- tivity (8, 9); unfortunately, no reliable assay for this peptide was available. MATERIALS AND METHODS Animals Five adult Labrador dogs (weight range 25-27 kg) with 12 implanted monopolar silver-silver chloride electrodes equispaced on the serosa of the digestive tract between the gastric antrum and the ileocecal valve, were used in this study. The electrodes had been inserted during asep- tic surgery up to six months before the time of study. Digestive Diseases and Sciences, Vol. 24, No. 6 June 1979) 0163-2116/79/0600-0417503.00/1 9 1979 Digestive Disease Systems, nc. 417  Wires from the electrodes terminated in a steel cannula implanted in the dog's abdominal wall to which an ex- ternal connector could be attached, and which also served as the remote indifferent electrode. Placement of the cannula in this site, and its use as the indifferent elec- trode greatly diminished disturbance of the electrical re- cord due to movement. Prior to surgery the animals had been trained to stand for several hours at a time support- ed by a sling, without apparent distress or discomfort. At all times an investigator was with the animals during study. Recording Techniques For the analysis of spike activity, myoelectric activity was recorded at three sites--duodenum, mid-jejunum, and distal ileum--on C120 1/s-in. magnetic tape cassettes with the Medilog 4-24 tape recorder (Oxford Electronic Instruments, Abingdon, Oxon). The fourth channel on the recording system was used for marking events during the study and also for marking the passage of time by means of a quartz oscillator built into the tape recorder. During the recording, signals monitored at the tape re- cording head were continuously displayed on an os- cilloscope. For the measurement of the basic electrical rhythm (BER), samples of direct tape recording from the gastric antrum and from the duodenum were recorded on ul- traviolet-sensitive chart paper using a fiber-optic record- ing oscilloscope, and intervals between slow waves were measured from the record. Experimental Design Study Protocol. During the study, which was preceded by 18 hr of fasting, the dogs remained at rest, supported by slings. The experimental design was arranged so that each animal acted as its own control. Each study lasted 6 hr during which recording was continuous. The first 2 hr were a record of fasting activity and plasma hormone lev- els, and during this time the presence of fasting myo- electric activity was verified. At the end of 2 hr, the ani- mal was fed its normal daily meal. This consisted of 400 g canned meat and 200 g biscuits (Pal meat and Mick bis- cuits, Pedigree Petfoods Ltd., Melton Mowbray, Eng- land). The nutrient load was 114.4 g protein, 26.2 g fat, and 151 carbohydrate. The energy value of the meal is 1040 kcal. The meal was invariably consumed within 2 rain. Recording continued for 4 hr from the start of feed- ing. Time signals were added to the recording tape at the beginning of the study, after 2 hr, and then at 30-rain in- tervals after feeding. Blood sampling. Prior to each study, an indwelling in- travenous cannula, length 28 in., ID 0.44 in., (Drum Car- tridge Catheter, Abbot Laboratories, N. Chicago, Illi- nois) was inserted into the cephalic or saphenous vein of the animal through a 14G 2-in. Thinwall needle. Coagu- lation between sampling was prevented by a slow infusion of physiological saline. 5-ml samples of venous blood for radioimmunoassay were collected in plain glass tubes via the cannula at the beginning of the study, after one hour, just before feeding and then 5, 10, 30, 45, 60, 90, 120,150, 180,210, and 240 min after food. Seven studies were car- WINGATE ET AL TABLE 1. MEAN SPIKE/30 MIN VALUES DURING THE POSTPRANDIAL PERIOD* Exp. No. t Dog Duodenum Jejunum Ileum 1 C 209• 41 496 • 80 264 • 170 2 A 331 • 107 777 • 156 994 • 163 3 H 453 • 64 457 • 43 535 • 170 4 L 241 • 67 579• 157 268 • 102 5 N 497 • 134 1175 • 88 557 • 134 6 A 689 • 62 824 • 127 1175 • 174 7 C 170• 43 257• 49 560• 185 *Spike values are mean values of eight 30-min totals --- 1 stan- dard deviation. tSerial assays of gastrin and insulin were incorporated in Exp. 1- 4 inclusive. ried out on the five animals but, for technical reasons, samples of hormone assay were only taken in four of these studies; each of these four studies was carried out in a different animal (see Table 1). Hormone Assays. Serum samples were rapidly sepa- rated and stored at -20 ~ C until assay. Radioimmunoas- says for insulin and gastrin were carried out by the meth- ods of Morgan and Lazarow (10) and Kaess and Meriadec (11), respectively, using synthetic human gastrin (I.C.I.) and bovine canine insulin as standards, with a reproduc- ibility of within 7%. Data Analysis Analysis of Tape Recorded Data. The system of analysis has been previously described in full (7). Taped data is replayed at high speed (replay speed-record speed = 60:1). During replay, slow-wave activity is re- moved by a bandpass filter, and spike activity (recorded at about 10-30 Hz) is amplified as required and passed to Schmitt triggers set so that each spike will trigger a pulse, which is delivered as a 5 V TTL logic pulse. Mains inter- ference, which is minimal in a system isolated from ac supply, is removed during replay by a notch filter set at approximately 3 kHz (= 50 Hz x 60). The TTL pulses are accumulated in digital counters which are latched and reset by the prerecorded time signals; thus the total num- ber of spikes at the end of the control (fasting) period is displayed as are the spike totals at 30-rain intervals there- after. At the same time, during replay, pulses are passed to an integrator which is sampled and reset every second; the output of this integrator is passed to a Y/t plotter to give a histogram of recorded spike activity per minute. Analysis of Spike Activity. In the system employed here each spike potential corresponds to a single event, de- noted by a logic pulse; thus a spike burst registers as sev- eral pulses (7). Spike activity in this system refers to the number of spikes--not the number of spike bursts, or, as in another technique (6), to the integrated signal after bandpass filtering. Spike activity was analyzed in three ways. The total spike activity for the 2 hr before feeding at each of the three levels in the small intestine was com- pared with the total spike activity for the two subsequent 2 hr periods after feeding. Variations in spike activity fol- lowing feeding were also measured, as total spikes for 418 Digestive Diseases and Sciences, Vol. 24, No. 6 June 1979)  FOOD AND CANINE MYOELECTRIC ACTIVITY BER 5 5 4 5 3 5 S TOMA CH 5 PRE 5 POST 60' POST BER 20 19.5 19 18.5 18 17 5 Cycles/ p~O.01 N.S. Cycles/ min. ~ p~O.O 1 = min. DUODENUM 5 PRE 5 POST 60 POST N. 5. N.S. Fig 1. Gastric (left) and duodenal (right) basic electrical rhythm changes in re sponse to feeding. Points from the same study are joined by solid lines. The values for 5 min before feeding were representative of fasting values in all studies; there were no significant variations during the fasting period in any of the studies. The statistical significance of the changes was calculated using a paired t test (NS = not significant). each 30-min period. The incidence of migrating myo- electric complexes (MMC) was judged from the histo- gram of spike activity in which MMCs register as a peak of intense activity, usually reaching 100 spikes/min fol- lowed by a period of absent spike activity. Basic Electrical Rhythm (BER). The frequency of the BER for the gastric antrum and the duodenum was calcu- lated from 5-rain samples of continuous chart record by visual inspection. Comparisons were made of the BER frequency 1 hr before feeding, 5 min before feeding, 5 min after feeding, and 60 min after feeding. RESULTS Basic Electrical Rhythm The effect of feeding on the frequency of the BER basic electrical rhythm is illustrated in Figure 1. On feeding there was a rapid and significant reduction in gastric BER frequency (P < 0.01) which re- mained depressed for the remainder of the study. Although there seemed to be a tendency for the fre- quency of the BER to return towards fasting level, this was not statistically significant. By contrast (Figure 1), there was no significant effect on the duodenal BER which did not change on feeding or subsequently during the postprandial period. Plasma Gastrin and Insulin Changes The range and mean values of serum levels of in- sulin and gastrin in four animals are illustrated in Figure 2; unfortunately adequate serum samples could not be obtained from the fifth animal. In spite of variations between animals, a clear pattern of changes emerged, with obvious differentiation be- tween fasting and fed levels. There was an early gastrin peak after feeding, followed by a gradual de- cline, with a secondary minor elevation after 2 hr. Insulin, which was low during fasting, rose on feed- ing, but the rise was slow in comparison with gas- trin and there was considerable postprandial varia- tion. There was no correlation between changes in plasma insulin and changes in spike activity at any level of the small intestine. There was no correla- tion between changes in plasma gastrin and ileal or jejunal spike activity, but in 2 out of 4 studies, there was a significant (P < 0.05) correlation between postprandial variation in duodenal spike activity and changes in plasma gastrin. When the same data from all 4 studies were grouped, the correlation was not significant. Correlations were not improved by comparing changes in spike activity with integrated plasma peptide values, obtained by calculating the area under the plasma peptide curves. Effect on Intestinal Spike Activity The effect of feeding (illustrated in Figure 3) was the replacement in all studies of fasting activity by Digestive Diseases and Sciences, Vol. 24, No. 6 June 1979) 419  WINGATE ET AL IR GASTRIN pg/ml 120 80 40 Range 9 mean (n=4J g 9 N I meal 1 0 2 4 6 R INSUL N .,uU/ml 120- 80 ~0 I I 2 4 HOURS Fig 2. Change in serum immunoreactive gastrin (above) and in- sulin (below) on feeding. Each point is the mean of four duplicate estimations; the shaded area indicates the range. There appears, in spite of wide variation, to be an insulin peak at 45 min after feeding, with a subsequent trough and secondary peaks in the 3rd and 4th hours after the meal. continuous intermittent spike activity at all three levels of the small intestine. Effect on Migrating Myoelcctric Complexes. In all studies the effect of feeding at all levels of the in- testine was the substitution of intermittent spiking activity for the fasting sequence of MMCs. This change occurred within 5 min in all studies in the jejunum, and in 5/7 studies in the ileum; it was ob- served at all levels in all studies within 20 min of feeding. In one study, a change resembling an MMC was seen in the jejunum 2 hr after feeding, con- sisting of phase-locked bursts of intense spike activ- ity followed by absence of spikes for 15 min, before resumption of the feeding pattern. There was no ex- planation for this phenomenon, and since there was no disruption of the feeding pattern in the duode- num or ileum, this may not have been a true migrat- ing complex, but merely a local event. Total Spike Activity: Fasting vs Fed. There was no significant increase in duodenal spike activity in spite of the change in pattern illustrated in Figure 3. Comparison of total spike activity (Figure 4) at the three levels of the small intestine in the 2 hr before and after feeding showed a significant (P < 0.01) in- crease in overall jejunal and ileal spike activity; ileal (but not jejunal) spike activity increased again (P < 0.05) in the second postprandial 2-hr period. Postprandial Variation of Spike Activity. Varia- tions were observed in postprandial spike activity at all levels of the intestine (Figure 5). The problem in analyzing these results arises from the considerable variation in the average spike activity recorded at different electrode sites, and in different animals. Table 1 shows the mean and standard deviation of total spike activity/30 min recorded following feed- ing at each electrode in each animal. Inspection of the data shows that the rate of postprandial spike incidence at each site in each experiment was rea- sonably uniform. Because of the range of absolute values, grouped means (Figure 5) show a large stan- dard deviation, and although some of the post- prandial changes in Figure 5 are statistically signifi- cant at the 5% level, the data are presented as being of interest in relation to changing plasma peptide levels rather than as evidence of significant change. The significant (P < 0.05) decline in duodenal spike activity is of possible interest in relation to changes in plasma gastrin but cannot be regarded as conclu- sive. Replicate Studies. Although the pattern of spike response to feeding was consistent, there was wide variation in total spike activity in numerical terms. Replicate studies were carried out on two animals (Table 1) to assess the consistency of response in one animal on different days. From these studies, it became clear that the intrasubject variation was as great as the intersubject variation, and there would be no validity in attempting to establish a "mean spike response" for each animal on the basis of rep- licate studies. DISCUSSION These studies have defined, in quantitative terms, the changes in intestinal spike activity on feeding which were first reported by Code and Marlett (3). The attempt to relate spike activity, expressed nu- merically, to serum peptide levels raises the prob- lem of correlating disparate phenomena. Whereas a single plasma sample may be taken as an "average" value, reference to the histogram of spike activity 420 Digestive Diseases and Sciences, Vol. 24, No. 6 June 1979)  FOOD AND CANINE MYOELECTRIC ACTIVITY DOG A DUODENUM 1'4EA L r- I00 1 I s,,IKE : i I ~176 JEJUNUM ~ 0 t i i oo l 0 z 6 HR Fig 3. Histogram of myoelectnc spike activity in one study. An MMC preceding the meal is starred; it can be seen that the meal virtually coincided with the MMC peak in the ileum, and the absent spike activity which followed an earlier MMC was abol- ished by feeding. It can also be seen that the peak spike activity during an MMC exceeds the maximum rate of postprandial spike activity. (Figure 3) shows that there may be a tenfold--or greater--variation in spike activity from minute to minute. It is obvious that the relationship, if any, between spike activity and hormone levels is not close. Since it is possible that there is a correlation between blood peptides and the trend of spike activ- ity, we have used cumulative totals of spike activity over longer periods of time in order to obtain aver- age values. During fasting, as we have found in a previous study (9), the cyclical change in spike ac- tivity dictates an average value based on cumulative incidence over a long period (2 hr): after feeding, a shorter period (30 min) seems adequate to indicated changing trends of spike activity. The attempt to correlate these arbitrary values to plasma values obtained from serial discrete (and virtually instanta- neous) samples is open to question, but the trends revealed by analysis of the data bear examination. Feeding induces a change in the pattern of spiking activity at all levels of the small intestine (3). Even in the distal intestine, this change is rapid, and thus may be presumed to be a neural or humoral effect, rather than due to stimulation by chyme. In the proximal intestine, the change in spiking activity is a redistribution of spikes in relation to time; in the jejunum and ileum feeding involves an increase in activity as well as an altered pattern. When the postprandial pattern is considered in more detail (Figure 5), it can be seen that post- prandial spiking is most intense in the duodenum soon after feeding, whereas the jejunal peak activity is delayed, and the ileal peak activity still further delayed. Only in the duodenum is the trend of post- prandial spike activity parallel with the trend of change in serum gastrin; distally the peak activity is delayed. At no level does the trend of postprandial spike activity follow the changes in serum insulin. Moreover, postprandial spiking activity does not bear the relationship to serum gastrin which might be predicted from the effects of exogenous gastrin (9), viz, no increase in duodenal or jejunal spike ac- tivity, and persistent fasting activity in the ileum. The caudad propagation of peak postprandial spik- ing activity over a period of 3 hr (Figure 5) suggests that it may be dictated by the transit of the nutrient load, rather than by humoral factors. The effect of feeding on BER frequency is equally inexplicable in terms of the effects of gastrin. Kelly (12) was the first to describe the accelerating effect of gastrin on BER frequency; the effect is dose de- pendent (9, 13) and there is a similar dose depen- dent increase in duodenal BER frequency (9). The effect of feeding on the gastric BER resembles the effect of simple distention (14), both in the slowing of the BER frequency and the rapidity of the change. We have not been able to reproduce the BER changes on feeding in our laboratories with exoge- Digestive Diseases and Sciences, Vol. 24, No. 6 June 1979) 421
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