Results

SUBJECTS

All subjects consumed both meals within 20 minutes. Owing to probe migration, data from one subject were omitted; the results from 18 subjects were analysed. Immediately after ingestion of a meal, there was a prompt increase in colonic pressure activity in all subjects (fig2). Randomisation of meals ensured that the order in which the meals were given did not affect the gastrocolonic response. We found that the two meals induced differential effects on colonic motor response.

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Figure 2

Typical changes in colonic motor activity in the same individual, before and after ingestion of: (A) a predominantly fat meal; and (B) a predominantly carbohydrate meal. P1, transverse colon; P2, splenic flexure; P3 and P4, descending colon; P5, sigmoid colon; P6, rectum. After the fat meal, pressure waves persisted for over three hours. After the carbohydrate meal, pressure activity decreased after 2.5 hours. The proximal colonic segments (P1–P3) showed greater activity than the distal (P4–P6) colonic segments.

EFFECTS OF A FATTY MEAL

Pressure activity

When compared with the control period, the number of pressure waves, the area under the curve, and the percentage of recording time when pressure activity occurred were higher (p<0.05) during the first hour following the meal (table 1). The area under the curve was also higher during the second and third hours (fig3).

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Figure 3

Effects of each meal on the area under the curve (AUC) of pressure waves. Results expressed as mean (95% confidence interval). * p<0.05 Meal versus control, † p<0.05 fat versus carbohydrate.

Wave patterns

Isolated, simultaneous or propagating pressure waves were seen throughout the four hour period and in each subject (table 2). When compared with the control period, a greater (p<0.05) number of propagating waves and simultaneous waves was seen during all three hours following the meal (table 2). Also, there was a higher (p<0.05) number of retrograde waves in the first hour following the meal compared with the control period (table 2). The mean amplitude of propagating pressure waves did not change significantly (table 2). Periodic rectal motor activity (PRMA) was observed during the preprandial and postprandial hours, but its incidence was not affected by meals (table 2). When compared with the control period, during the first postprandial hour, more subjects exhibited specialised propagating waves (table 3). Although higher, the number of waves was not significant. Seven (39%) subjects did not show specialised propagating waves postprandially. The amplitude, duration, and velocity of propagation of these pressure waves were not affected by the meal.

Regional differences

When compared with the control period, the area under the curve of pressure activity was significantly higher (p<0.05) in the transverse/descending colon than in the rectosigmoid colon, during the first postprandial hour (table 1). Also, the area under the curve in the transverse/descending colon was higher during all three hours compared with the control period, but not in the rectosigmoid colon (table 1).

EFFECTS OF A CARBOHYDRATE MEAL

Pressure activity

The number of pressure waves, the percentage activity (table 1) and the area under the curve of pressure waves (fig 3) increased (p<0.05) significantly during the first postprandial hour. During the second and third postprandial hours, the pressure activity decreased to control values (table 1).

Wave patterns

During the first postprandial hour there was a higher (p<0.05) incidence of propagating waves, but not simultaneous or retrograde waves (table 2). The number of simultaneous waves actually decreased (p<0.05) in the third postprandial hour compared with the preprandial period (fig 3). Postprandially, the mean amplitude of pressure waves did not change significantly (table 2). When compared with the control period, during the first hour more subjects showed specialised propagating waves with a higher incidence (table 3). The difference was not significant. The amplitude, duration, and velocity of propagation of these waves were not affected by the meal. PRMA was observed and its incidence was unchanged during the first two hours, but there was a higher incidence during the third postprandial hour (table2).

Regional differences

When compared with the control period, the area under the curve of pressure waves was greater (p<0.05) in the transverse/descending colon than in the rectosigmoid colon during the first postprandial hour, but not during the next two hours (table 1).

COMPARISON OF HIGH FAT AND HIGH CARBOHYDRATE MEALS

The onset of pressure activity or cyclical activity was quicker (p<0.001) after the carbohydrate meal when compared with the fat meal. After ingestion of the carbohydrate meal, the colonic motor activity and cyclical activity were induced at 41.3 (18.8) and 62.1 (18.5) seconds, respectively, whereas after ingestion of the fat meal they were induced at 162 (21.3) and 356 (52) seconds, respectively. Unlike the carbohydrate meal, the fat induced pressure activity persisted well into the second and third postprandial hours (p<0.05) when compared with the control period (fig 3). Both meals induced a greater (p<0.001) number of propagating waves during the first hour (table 2). Only the fat meal, however, induced a greater (p<0.05) number of simultaneous waves during the three hours and retrograde pressure waves during the first hour (table 2). Furthermore, the fat meal induced a significantly higher (p<0.05) number of simultaneous waves than the carbohydrate meal (table 2).

Discussion

Although the colonic motor response which occurs after a fat meal has been described previously,14 16 27 31 this is the first study that has examined colonic manometry after ingestion of a predominantly fat or carbohydrate meal within the same individual. Unlike a previous report,16 we found that a carbohydrate meal not only induced a colonic motor response, but the magnitude of response during the first hour was comparable to that of an isoenergy fat meal.

In the previous study,16 glucose or olive oil were used as opposed to a whole meal, the energy content of the two meals was lower, and the electrical spike activity was recorded from a limited segment (rectosigmoid region only). In this context, our finding that both meals induced greater motor activity in the transverse/descending colon than the rectosigmoid colon is important. This observation not only confirms previous studies,12 27 32 but underscores the fact that colonic motor changes can be missed or misinterpreted if motor activity is recorded from a limited segment. In addition to the examination of a longer segment, we also sought to minimise the effects of colon cleansing,11 13 the effects of infusing fluid into the colon, and the effects of meal consistency, by assessing the colonic motor responses at 10 and 27 hours after probe placement, by using solid state technology, and by giving whole meals rather than liquid meals.12 The smell, sight, and taste of food may each influence colonic motor activity.33 We sought to minimise these influences by presenting meals that looked similar in volume, colour, smell, and appearance. Thus, our study was performed under more physiological conditions.

We cannot exclude the possibility that the small amount of fat which was present in the carbohydrate meal may have exerted some effect on the colonic motor response. The fat component of the carbohydrate meal, however, accounted for only 0.8 MJ, an energy load that does not induce a colonic motor response.15 Furthermore, the differential effects on motor activity and on motor patterns would argue in favour of a direct effect of the carbohydrate component.

Unlike observations in the canine colon,6 we did not observe an early and late colonic response in humans. In one human study a possible bimodal response has been described.12The duration of recording in this study, however, was only 90 minutes, and therefore was insufficient to provide information regarding the late response. Also, a liquid meal was given.12 In contrast, we found that the colonic motor response reverted to the preprandial state within three to four hours, and thereafter no further increase was seen. The late colonic response has been ascribed to the motor activity induced by the arrival of meal residues into the caecum.5 We did not find evidence to support this concept. Instead, our findings suggest that ingestion of a meal seems to be a more important stimulus for colonic motor activity. Whether more frequent ingestion of meals stimulates a greater response merits further study.

After a carbohydrate meal, the onset of motor activity was quicker, albeit small, but the duration of motor response was clearly shorter when compared with the fat meal. Because the colonic motor response may be induced by stimulation of mechanoreceptors in the upper gut2 and possibly mediated by neurohormonal mechanisms,2 31 34 the differential effects of the two meals may be due to either the rate of transit of each meal through the upper gut or the stimulation of different neurohormones or receptors. Previously, it has been shown that meals containing fat delay gastric and small bowel transit.19 35 The infusion of fat into the duodenum also induces a duodenal brake.18 These effects are probably due to the stimulation of specialised mucosal cells such as I cells of the duodenojejunum that secrete cholecystokinin,2 31 34 or due to the release of peptide YY,36 both of which can delay gastric emptying. Thus, the prolonged colonic motor response that is induced by a fat meal may in part be due to the slower transit of this meal through the upper gut and the release of cholecystokinin.31 34 In contrast, the shorter duration and the more rapid onset of the colonic motor response after a carbohydrate meal may be due to the more rapid transit of this meal through the stomach and small bowel.

In order to obviate any bias, the motor patterns were analysed by one investigator who was unaware of the meal composition or the results of other motor parameters. We found that 50% of subjects exhibited high amplitude, prolonged duration, specialised propagating waves after either meal. In those subjects who exhibited this phenomenon, on average one or two specialised propagating sequences were seen. This incidence was much higher than that reported previously11 12 34 and could be due to the more physiological conditions of our study. This finding not only confirms previous observations,37 but suggests that strong propagating waves may shift a larger volume of stool postprandially, particularly when there are no opposing simultaneous or retrograde pressure waves. Similar patterns described previously have been termed high amplitude propagating contractions11 28 in humans and giant migrating contractions5 6 in dogs. Because these waves are not only of a high amplitude but also of prolonged duration (more than 13 seconds), we felt that specialised propagating pressure waves may be a more appropriate term for describing these waves.

We also found that both meals induced a greater number of propagating pressure waves when compared with the preprandial hour. The incidence of simultaneous and retrograde pressure waves showed a differential response, however. After a carbohydrate meal there was a distinct drop off in their incidence, but after a fat meal this pattern persisted for three hours. Because diarrhoea is associated with decreased phasic activity38 39 and constipation with excessive phasic pressure activity,38 40 it is possible that the aforementioned effects of a fat meal on colonic motility may delay stool transport. In contrast, the increased number of propagating and specialised propagating pressure waves that were induced by a carbohydrate meal without an associated increase in the simultaneous or retrograde pressure waves (particularly in the second and third postprandial hours) is less likely to impede stool transport.35 As colon transit was not assessed in this study, however, our statement(s) should be interpreted with caution.

Our investigation reveals that both fat and carbohydrate meals induce a colonic motor response with 50% of subjects exhibiting high amplitude, prolonged duration, propagating pressure waves. The duration of phasic activity appears to depend on nutrient composition: a higher fat content is associated with a more prolonged colonic motor response. Thus, nutrient composition of a whole meal appears to influence the colonic motor response.