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Keywords:

  • ambulatory manometry;
  • duodenum;
  • gastroduodenal motility;
  • migrating motor complex;
  • physiology;
  • stomach

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. References

Circadian antroduodenal motor activity was studied in 40 normal subjects by means of a portable recording system consisting of a computerized data logger and a probe with microtransducers. The quantitative and qualitative characteristics of contraction events during the interdigestive and digestive periods, as well as during the awake and asleep periods, were analysed. The composition and timing of meals and night recumbence were standardized. In spite of the high interindividual variability in motor parameters, significant differences in the characteristics of interdigestive and digestive periods between waking and sleep states were found. This paper confirms the existence of a circadian variation in antroduodenal motor activity and provides reference values from a large series of normal subjects that can be used for statistical comparisons with those obtained from patients recorded with the same method.


INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. References

Twenty four-hour ambulatory manometry with microtransducers and portable recording apparatus is becoming widely available for the study of gastrointestinal motility. Not only the oesophagus and small intestine, but also the antroduodenal tract can be investigated with this technique. However, very few studies have been performed on this region,1[2]–3 compared to the small intestine,4[5][6][7][8][9][10][11][12][13][14]–15 probably because there are more technical difficulties in keeping the probe in the correct position across the pylorus.1,16,17 However, the main problem is the high interindividual variability of the gut motor parameters. If the control group is small, it may be difficult to reach a statistical significance comparison with the data recorded from patients. Furthermore, there are marked differences in the values of some parameters in published studies, especially with respect to the interdigestive period. We believe that the interindividual variation, and also the differences between studies, could be due, at least in part, to differences in meal composition and timing of eating and sleeping. Consequently we standardized the meal composition and timing of the meals and night recumbence, as we did previously for the study of the circadian motor activity of the oesophagus.18 In addition, in order to reduce the influence exerted on statistical comparisons by the interindividual variability, we collected a large number of subjects by an ad hoc multicentre study group, established under the aegis of GISMAD (Italian Group for Study of Gut Motility). The aim of this study is to establish the normal 24 h characteristics of the interdigestive, diurnal and nocturnal, and digestive motor activity of the antroduodenal tract using a commercially available apparatus for ambulatory manometry.

MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. References

Subjects

The study was carried out on 40 normal subjects (19 males and 21 females, mean age 32.5 years, range 18–49 years; ten from the centre of Bologna, 24 from S. Giovanni Rotondo and six from Genova). As the local research ethics committee for one of the centres forbids the payment of volunteers (and it is not easy to recruit unpaid volunteers), not all the subjects were healthy volunteers. Some were recruited from patients attending internal medicine and gastroenterology outpatient clinics, who did not have severe disease and were healthy with regard to the digestive system. Particular care was used to exclude patients with symptoms of functional gut disorders. The following disorders were contra-indications for inclusion in the study: organic lesions of the gut, such as hiatal hernia, ulcers, stenosis, etc.; previous surgery of the digestive tract (excluding appendectomy); symptoms of gastro-oesophageal reflux disease and of oesophageal, gastroduodenal, colonic and biliary motility disorders; and hepatic, cardiac, renal, neurologic and systemic diseases in which an involvement of the digestive tract is possible (diabetes, scleroderma, etc.).

The total number of clinic patients was 14 and their diagnoses were: mild arterial hypertension (two cases); benign cardiac dysrhythmia, chronic bronchitis (three cases); nontoxic thyroid adenoma, uncomplicated cystitis; nephrolithiasis; haemorrhoids; anal fissure; benign colonic and rectal polyps; Gilbert’s syndrome. All patients were asked to discontinue medication likely to alter gut function for 5 days prior to the study.

Additional exclusion criteria valid for all subjects were: alcohol consumption >20 g per day; smoking >10 cigarettes per day and inability of the smoker to reduce the number of cigarettes to less than three per day for the day of study; drug abuse; age >70 years.

Informed consent was obtained from all subjects.

Recording apparatus

The manometry system used by each centre for recording oesophageal motility consisted of the following devices: a six-channel portable solid-state digital data-logger (Microdigitrapper 4 Mb, Synectics Med Inc) with current sampling frequency of 4 Hz, A-D conversion, temporary storage up to 4 Mb and event markers; a probe with 5–6 miniaturized electronic pressure transducers 5 cm apart (Koenigsberg Instruments); and an IBM-compatible personal computer with data display and printer, permanent data storage and software for the analysis of data and generation of reports (Gastrosoft version 6.2, Multigram, Synectics Medical Inc.).

Study procedure

The recording started in the morning and stopped after 23–24 h. Calibration of the manometric probe was performed just before the study with external application of atmospheric zero and 50 mHg pressure by means of a water column. The probe was passed transnasally and, with the aid of fluoroscopy, was positioned with three sensors in the duodenum and the remainder in the distal gastric antrum. This probe configuration and positioning allowed us to detect both the interdigestive and digestive motor activity of the distal half of the antrum. If one sensor is in the duodenal bulb, the proximal sensor is 5 cm orad, that is, about 3 cm from the pylorus. If the latter, as frequently happens after a meal, retracts to 6 cm proximal to the pylorus, the sensor within the duodenal bulb will retract into the antrum. Thus, one of the sensors is always present in the distal half of the antrum and is able to record both the digestive and interdigestive motility, including the antral phase III. For a gastric phase III to be effective in clearing gastric solids, there must be powerful occlusive contractions in the distal corpus and the antrum. Phase III episodes, which do not give rise to powerful pressure increases at 4 cm from the pylorus, or that involve only the distal 2-3 cm of the antrum, cannot be considered normal, because their effectiveness on antral clearing is almost completely abolished.

In order to avoid a migration of the antral sensors, when the three distal sensors were positioned in the duodenum, catheter slack in the corpus and fundus was taken up by withdrawing the probe under fluoroscopic control until the antral sensors were applied to the lesser curvature of the stomach. The probe was then securely taped to the nose and the recording unit was attached to a waist belt on the subject. Individuals were allowed to return home and were encouraged to perform normal daily activities and their normal work, when possible. They were instructed to record on a diary the start and the end of the meals and night recumbence and to use the event buttons. A diet sheet was given for standardization of meals; snacks and alcoholic, carbonated and acidic beverages were forbidden. The required timing for starting the meals was 1200–1300 h and 1800–1900 h, and 2200–2300 h till 700–800 h for bed rest. Each meal consisted of: 60 g bread, 60 g pasta with tomato sauce, 100 g hamburger, 150 g vegetables, 10 g oil and 150 g fruit for a total of 830 kcal. For future studies on persons who are not familiar with, or do not appreciate the advantages of a Mediterranean diet, minor variations are possible. Pasta might be replaced by an equicaloric quantity of cereals in the morning, or of fried potatoes for dinner, while tomato sauce could be added to the hamburger or fried potatoes. In addition, the meals could be brought forward slightly to 1000–1100 h (brunch) and dinner to 1700–1800 h.

After the completion of the recording, the data was unloaded from the recorder onto the computer for the analysis.

Analysis of recordings

The pressure tracing was reviewed on the computer screen and a print-out of the entire recording or of selected intervals obtained. A dedicated software programme described in detail in a previous study on ambulatory oesophageal manometry was used.18 The software was able to recognize as artefacts the simultaneous pressure rises occurring with similar amplitude and duration at all the sensors and due to gross body movements, straining, etc. The resting pressure is represented by a baseline that was the reference for all calculations: it was defined automatically through the most frequent level of the smaller pressure variations at each site. The baseline was automatically updated every 10 s. A contraction was considered ‘valid’ and included in the calculations if it exceeded a pressure threshold of 10 mmHg and had a minimum duration of 1 s. The total period of recording was divided into two periods; the digestive period, from the start of the meal to the first duodenal phase III, and the interdigestive period, which was subdivided into sleeping and waking periods. Phase III was visually identified in the stomach by a sequence of 2–3 waves per min for at least 2 min, followed by a phase of motor silence and in temporal relationship with a duodenal phase III. The latter was identified as a propagated burst of pressure waves with a frequency of 10–12 per min for at least 2 min, followed by a phase of motor quiescence. Phase I was defined as a period of at least 10 min during which there were ≤3 contractions 10 min−1. Cluster activity was recognized visually and defined as a sequence of bursts of at least three phasic contractions, separated by a quiescent period of at least 15 s and observed in at least two sensors.16 The following parameters were calculated during the sleeping and waking periods: MMC cycle length, percentage duration of MMC phases, number, duration, wave frequency, wave amplitude, wave duration and propagation velocity of phase III, wave frequency, wave amplitude, wave duration and motility index of both phase II and the digestive period. Phase III propagation velocity between the antrum and the duodenum, and along the duodenum, were calculated by the onset of phase III. In addition, the percentage of duodenal phases III associated with antral phases III was calculated during the sleeping and waking periods.

Statistical study

The mean values of the sleeping period were compared with those of the waking period by means of the Wilcoxon matched-pairs test and chi square test whenever indicated. The mean values of antral and duodenal wave frequency and amplitude, and motility index of the first 3 h of the digestive period after lunch, were compared with those after dinner. In addition we calculated the temporal relationship between the first postprandial antral and duodenal phases III which occurred after dinner.

RESULTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. References

The length of the total recording period was 1344 min ± 91 (mean ± SD), 465 min ± 53 of which are represented by the sleeping period.

Interdigestive period

The whole duration of the interdigestive period was 632 min ± 164 and its characteristics are summarized in Tables 1 and 2. At least one cycle of the migrating motor complex (MMC) with phases I, II and III (Fig. 1a) was recorded in all subjects. The most remarkable findings of this period are the following:

Table 1.   Characteristics of MMC cycle and phases III of the antrum and duodenum during the awake and asleep periods of the interdigestive period Thumbnail image of
Table 2.   Characteristics of the antral and duodenal phases II during the awake and asleep periods of the interdigestive period Thumbnail image of
image

Figure 1.  (a) Phase III of the migrating motor complex recorded in a normal subject from the antrum (first two traces) and the duodenum (last three traces); (b) postprandial motor activity recorded in the same subject as part (a). The first two sensors that in part (a) were positioned in the antrum migrated proximally into the corpus, probably because of the postprandial antral distension, and did not record any more phasic waves. Contemporaneously the third sensor that in part (a) was positioned in the proximal duodenum, migrated into the antrum, were it recorded the phasic waves of the digestive period.

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the number of phases III recorded during the sleeping period was higher than that of the waking period, while the number of phases III starting from the duodenum was higher than that from the stomach. 24% of duodenal phases III are associated with antral phases III during the waking period and 30% during the sleeping period, without a significant difference;

the antro-duodenal propagation velocity of phase III of the waking period was not significantly different from that of the sleeping period;

the propagation velocity of the duodenal phase III was faster during the waking period compared with the sleeping period; during the latter a stationary phase III was recorded in two subjects;

the mean MMC cycle was longer during the waking period mainly because of a more prolonged phase II compared with the sleeping period;

the phase II motor activity during the waking period was significantly higher than during the sleeping period, with the presence of cluster activity in 65% of cases; clusters were absent during the sleeping period.

Digestive period

The whole duration of the fed activity was 632 ± 164 min. However, the duration of the antral fed activity was significantly longer than the duodenal one: in fact phase III activity reappeared after dinner significantly (P < 0.005) later in the antrum (386 ± 120 min) than in the duodenum (316 ± 82 min). The evidence that the particular spacing configuration of the probe pressure sensors allows us to record easily the postprandial antral activity is given by Fig. 1(b). The mean values of the motility index, amplitude, duration and frequency of pressure waves of digestive motor activity of the antrum and duodenum are summarized in Table 3. A cluster activity was frequently observed in the duodenal recordings of 87.5% of the subjects, but it never exceeded a duration of 10 min. The antroduodenal motor activity of the first three hours after dinner was lower than that after lunch (Table 3).

Table 3.   Characteristics of the antral and duodenal motor activity observed during the whole digestive period Thumbnail image of

DISCUSSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. References

The results of this study confirm the opinion of other investigators1[2]–3,19 that the 24-h ambulatory manometry is a simple technique, easy to perform, well tolerated by the patient and able to provide reliable information on the circadian antroduodenal motor activity. The main limitation of the ambulatory manometry lies in the fact that the number of sensors that can be currently utilized does not exceed six, which is a number clearly insufficient for a satisfactory study of the antrum, duodenum and jejunum. So, we preferred to dedicate all the sensors to study the motor activity of the antrum and the proximal half of the duodenum, rather than to use one or two sensors to record the distal duodenum or the jejunum. The motor activity of the proximal duodenum is strictly correlated with that of the antrum, while that of the distal duodenum–jejunum is under a different physiological control. However, one potential drawback of ambulatory antroduodenal study is the difficulty in maintaining an adequate contact between the proximal recording points and the antrum, especially in the postprandial state, when a relevant widening of the antral cavity takes place. Some investigators, who used three antral sensors, 1–2 cm apart, failed to monitor continuously the antral motor activity for the entire period of the study in nearly half of the subjects3 or did not record any antral activity during the postprandial period in all the subjects.1 As explained in the results section, we solved this problem with a catheter design and positioning which means there is always at least one sensor in the distal half of the antrum, even during the digestive period. We are aware that this solution does not allow a detailed study of the antropyloric contractions especially after meals, when the contractions are more variable and may be lumen occlusive for a shorter length of the antrum than during phase III. Nevertheless, it allowed us to record the antral waves over a 24-h period giving few but essential parameters, that characterize the waking and sleeping periods, such as the number of effective antral phases III, which is lower during the night, and the digestive period, which is characterized by antral motor activity, such as the frequency and amplitude of occlusive waves of the distal half of the antrum, which are lower after dinner than after lunch.

Our study confirms the presence of a rather high interindividual variability, although lower than that observed in other studies, as can be inferred from the standard errors. This result might be due, not only to the high number of subjects, but also to the standardization of meals and periods of night recumbence. We believe that these data may well allow valuable comparisons with that of patients investigated with the same methodology, facilitating the achievement of a statistical significance.

The comparison of our results with previous studies is difficult, not only because those concerning antroduodenal recordings are very few, but also because the values of some parameters showed marked differences among the various studies. For example, the duration of the postprandial period ranged from 199 min1 to 424 min,3 the MMC cycle duration during the waking period from 81 min8 to 238 min,6 the percentage duration of phase I during the waking period from 0.8%6 to 34%3 of the entire MMC cycle, and the propagation velocity from 25.2 cm min−11 to 6.4 cm min−1.10 Although these values concern principally the duodeno–jejunal motor activity, the differences are strikingly high and require an explanation. One of the possible causes of these differences could be found in the diversity in meal composition and the timing of meals and night recumbence. In fact, for example, the duration of the fed pattern is significantly longer after a high caloric11 or a high-fat meal20 in comparison with a low caloric or low-fat meal, respectively, with consequent decreases of the total number of phases III. However, our results confirm in general the circadian behaviour of the gastroduodenal motility that emerged from the analysis of the above-mentioned studies. The phases III during sleep are more numerous and propagate at lower velocity than during the waking period. The higher number of phases III during sleep is due not only to a longer period of fasting, but also to a shorter interval between phases III, being the phase II of shorter duration. Only a portion (24–30%) of the duodenal phases III that resulted were associated with antral phases III, without significant difference between the waking and sleeping periods. One of the reasons for this phenomenon may lie in the fact that the postprandial reappearance of phase III in the antrum is delayed with respect to that of the duodenum. The reason why the antroduodenal motor activity after dinner was lower than after lunch, although the composition of the meals was the same, is unknown. Another study7 compared the motor activity after breakfast and dinner, but the results cannot be comparable to ours, because the meals were completely different between the studies. A duodenal cluster activity is rather a common finding during the waking period especially after meals, while it is completely absent during the sleeping period.

The physiopathological and clinical relevance of these findings should be validated by comparison studies in patients with well-established gastroduodenal motor disorders. We believe that this technique should be especially helpful in the investigation of patients with dyspepsia, because it gives sufficient evaluation of the antral motor function during the interdigestive and digestive periods, which is altered in a portion of this type of patients.2, 21,22 The prolonged assessment of the antroduodenal motor activity permits study, in a more physiological manner and without the stress connected with the hospital environment, of the relationship between the symptoms arising during the usual conditions of life and the antroduodenal motor abnormalities. We believe that ambulatory manometry should not replace, but be integrated with, stationary manometry, because the current technology does not yet allow accurate study of the antropyloric region. However, when the technology has resolved this limitation, then this technique will become a very useful clinical and research tool.

References

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. References
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