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Keywords:

  • migrating motor complex;
  • migrating motor complex phase III;
  • sonography.

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Funding
  8. Disclosures
  9. Author Contributions
  10. References
  11. Supporting Information

Background  Migrating motor complex phase III (MMC phase III) of intestine is an important physiological mechanism traditionally recognized by myoelectric recordings or pressure tracings. Direct imaging is difficult and sonographic visualization in human has not been reported.

Methods  We have demonstrated this unique phenomenon in three patients who underwent abdominal sonographic examinations. Characteristic images were recorded by videotape and both spatial and temporal features were analyzed.

Key Results  Occurrences of multiple equally spaced, rhythmic intestinal contractions were observed. Parameters including wave frequency, propagation velocity, and duration of the events agreed with those of the well-known phase III. The presence of distinct cyclic patterns observed in two and abolition by meal in the other patient further support our conclusion.

Conclusions & Inferences  We conclude that the migrating waves observed in our study represent the human MMC phase III. This unique finding in human subjects merits further investigation.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Funding
  8. Disclosures
  9. Author Contributions
  10. References
  11. Supporting Information

The fasting human small intestine displays cyclic appearance of clusters of characteristic contractions called migrating motor complex (MMC). Four stages can be identified: phase I of quiescence activity, phase II of irregular and sporadic contractility, phase III presenting successive bouts of regularly peristaltic contractions, followed by a transient and irregular phase IV. Migrating motor complex phase III (phase III) has been regarded as the housekeeper that cleans the intestines periodically from the gastric antrum to the ileum.1 Phase III has been traditionally recognized by myoelectric recordings, pressure, or strain gauge tracings. Novel techniques have been introduced lately, but they have not gained wide application yet.2,3 Videofluoroscopy has the advantage of direct visualization of the intestinal motions while carries a risk of radiation exposure.4,5 Trans-abdominal real-time sonography is a non-invasive and versatile tool for imaging the intestines and has gained substantial progress in the last decade when newer techniques were introduced.6,7 In this study, we report the use of sonography in demonstrating the characteristic images of phase III in three fasting patients.

Materials and Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Funding
  8. Disclosures
  9. Author Contributions
  10. References
  11. Supporting Information

In our previous study elucidating the mechanisms of bowel sounds,8 we have performed sonographic examination in about 200 patients, among which, three were found to present phase III-like activities. Case A was a 69-year-old male with acute abdominal pain, who finally recovered after conservative management and came out with the diagnosis of pseudo-obstruction. Case B, a 65-year-old male presenting with fever and abdominal pain, was diagnosed to have a ruptured splenic lymphoma. Case C was a 47-year-old male alcoholic with liver cirrhosis, complaining of abdominal pain; a final diagnosis of acute pancreatitis was made.

The sonographic procedures have been described previously.8 Briefly, a curvilinear 3.5 MHz or a linear 7.5 MHz transducers (M2410A Ultrasound System, Hewlett-Packard, Andover, MA, USA) were used. After an initial survey over the entire abdomen, a specific location was chosen where the scanning probe was held fixed for at least 20 min (according to Tomomasa et al.9). The selection of probes was highly individualized, depending on the patient’s habitus and depth of the target intestinal loops, etc. Video clips recorded at a rate of 30 frames-per-second were used for calculation of the speed and contraction frequency. Inter- (CJL and CYL) and intra-observer (CJL) variability was evaluated according to Filippi et al.10 Quantitative data were expressed as means ± SEM unless stated otherwise.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Funding
  8. Disclosures
  9. Author Contributions
  10. References
  11. Supporting Information

The total durations of recording in Case A, B, and C were 29.9, 33.4, and 27.1 min, respectively. Featured parameters of the migrating waves (MWs) were summarized in Table 1.

Table 1.   Featured parameters of the migrating waves (MWs)
CaseNo. of sampled wavesDuration of MWs (min)Frequency in cpm (Duration in s)Propagation velocity (cm min−1)Supplementary findings
  1. cpm, cycles per minute.

  2. Values are means ± SEM.

  3. * P-value > 0.1 between the 1st and the 2nd MWs of Case A.

A1st MWs, N = 95.711.1 (5.4 ± 0.1)*25.6 ± 0.4*Cyclic pattern
2nd MWs, N = 9≥4.510.9 (5.5 ± 0.1)24.2 ± 0.9Cyclic pattern
B N = 10≥2.511.3 (5.3 ± 0.2)22.0 ± 0.8Followed by quiescence
C = 10≥25.09.7 (6.2 ± 0.1)25.3 ± 1.6Aboral migration & abolition by meal

Case A

Under sonography, sporadic contractions were initially observed at the right lower quadrant of the abdomen. Later, the sporadic background was replaced by a regular motility pattern. The bowel motions consisted of a row of equally spaced MWs with rhythmic contractions alternating with dilatations, while maintaining their relative position during migration (Video S1).

The first MWs had lasted for 5.7 min before entering another irregular phase with asynchronous waves (Video S2). Four minutes and 40 s later, the bowel turned silent gradually and stayed quiescent for a period of 2 min. It was at this point the examination was interrupted for a recess of 6.4 min, which accounted for the gap appeared on the timeline. On returning back to the examination, another irregular phase was already underway and, before long, transformed into the second regular phase of MWs that was almost indistinguishable from the first in all aspects (Table 1). The recording ended at about 30 min when the MWs were still ongoing. Sequential images acquired at 1 s interval were presented in Fig. 1A showing the steady migration of the contractions rightward. The time course and the cycling pattern were summarized in Fig. 2.

image

Figure 1.  The video frames from Case A, B, and C were acquired at 1 s interval revealing rhythmic and continuous contractile activities. The broken arrows indicate propagation of the contraction rings showing fewer zigzags in Case A because breath-holding was undertaken. The values of maximal diameter in Case A, B, and C were 2.1, 1.6, and 1.9 cm, respectively. The data for minimal diameters in three cases were 1.4, 0.9, and 0.9 cm. The interwave distances were 2.2, 1.8, and 2.5 cm. The bars represent 1 cm.

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image

Figure 2.  Schematic illustration of the temporal sequences in Case A. Upper panel shows the proposed staging as equivalent to those of MMC. Time axis was labeled as minute, and time elapsed as min-and-sec (e.g. 5 m 44 s). Lower panel shows the representative images captured 2 s apart from the respective phases. Note the presence of a gap of 6 min 26 s which masked the putative transition from phase I to phase II.

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Case B

Successive waves in row were detected over the left upper quadrant. The clustered MWs were moving steadily rightward (Fig. 1B, Video S3). About 2.5 min later, the MWs were succeeded by a transient stage of decreased motility (putative phase IV), lasting for 15 s, then replaced by total akinesia. The presence of this transition of phases was reminiscent of the well-known phase III.

Case C

The familiar images of MWs caught our sight again (Fig. 1C, Video S4). The MWs moved smoothly from the left upper quadrant downward. As phase III was suspected, a test meal (Osmolite 237 mL, 250 Kcal, Abott Lab. Ltd. QC, Canada) was given orally within 2 min. Eight minutes and 8 s after the meal, the regular sequence was brought to an abrupt end. In addition, inflow of chyme distending the lumen sequentially in the same direction as that of MWs’ was witnessed (Video S5), confirming the aboral migration of MWs.

Inter- and intra-observer data were analyzed. The median inter-observer agreements were 87.4% (CI, 85.3–89.5%) for the duration and 90.3% (CI, 88.5–92.1%) for propagation velocity. The intra-observer agreements were 93.0% (CI, 90.0–96.0%) for duration and 93.8% (CI, 90.8–96.8%) for propagation velocity.

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Funding
  8. Disclosures
  9. Author Contributions
  10. References
  11. Supporting Information

Migrating motor complex phase III has been defined as an uninterrupted presence of phasic contractions that fulfill the following criteria: (i) duration more than 2 min; (ii) recurrence at a frequency of 10–12 min−1; (iii) aboral propagation; and (iv) followed by a period of complete quiescence (phase I).11 Detailed comparison between MWs and phase III regarding these criteria were made.

Although the generally accepted range of duration of phase III in normal subjects is 5–10 min, the variability is wide12 and values up to 13.5 ± 3.5 min (mean ± SD) were recorded.11 The durations of our MWs were 5.7 and ≥4.5 min in Case A, ≥2.5 min in Case B, and ≥25.0 min in Case C. Therefore, all except Case C were expected to fall within this range. In cirrhotic patients with portal hypertension, as in our Case C, the duration of jejunal phase III was found to be significantly increased.13 Moreover, regarding normal variations, a meta-analysis study of jejunal MMC by prolonged ambulatory manometry on healthy adults yielded a range from 0 to around 23 min.14 In fact, an uninterrupted occurrence of ≥2 min has been proposed as the only criterion required for the duration of phase III11 and a consensus report suggested no upper limit needed for the phase III duration.15

The migration velocity of a normal phase III (the ‘activity front’) was generally around 2–10 cm min−1.15,16 However, a much wider range up to 2.5–26.5 cm min−1 was obtained in proximal jejunum by ambulatory manometry.12,17 Our MWs yielded values from 22.0 to 25.6 cm min−1 and is thus within this range. Previous fluoroscopic studies generated even more diversified results, i.e. 150 and 240 cm min−1, separately.4,18 The cause for this diversification was unknown, although difference between the velocities of the activity front itself and the individual contractions within it does exist.16 In general, propagation velocity has not been proposed as a manometric criterion for identification of human phase III in previous studies.19

Major evidence indicating the phase III nature of our MWs resides in the frequency study. There is great variability in almost all phase III parameters except frequency,5 which is known to derive from the slow wave frequency, i.e. 11–12 cycles per minute (cpm) in duodenum and 7–8 cpm in ileum.12 In our study, the contraction frequencies were narrowly confined between 9.7 and 11.1 cpm, which are in good agreement with a feature of phase III.

Multiphasic phase IIIs are not considered unusual, as they have been detected in both normal subjects and patients with functional abdominal pain.5 Hence, the presence of biphasic occurrence of MWs, 15 min apart as appeared in Case A, does not preclude their roles as true phase IIIs.

In conclusion, considering the parameters discussed above, MWs may be regarded as the sonographic manifestation of phase III, which has not been reported previously. The recognition of MMC phase III by trans-abdominal sonography is difficult, but obviously feasible. Further studies, such as simultaneous manometry and sonographic recordings are needed to confirm our findings. If established, the sonographic measurement of human MMC phase III may greatly supplement our knowledge in this important topic.

Funding

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Funding
  8. Disclosures
  9. Author Contributions
  10. References
  11. Supporting Information

The study was supported in part by a grant from the National Science Council (NSC-99-2320-B-320-010-MY3).

Author Contributions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Funding
  8. Disclosures
  9. Author Contributions
  10. References
  11. Supporting Information

CJL conducted the sonographic examinations and wrote the manuscript; SCH was responsible for scientific advice and revision of the manuscript. YCH was in charge of the patient recruitment; CYL performed data collection and statistical analysis; HIC is the principal investigator who contributed to the study supervision and critical revision of the manuscript. All authors have read the manuscript and approved the submission to Neurogastroenterol & Motility.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Funding
  8. Disclosures
  9. Author Contributions
  10. References
  11. Supporting Information

Supporting Information

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Funding
  8. Disclosures
  9. Author Contributions
  10. References
  11. Supporting Information

Video S1. The first phase III in Case A. The bowel motions consisted of a row of equally-spaced, wave-like configurations with rhythmic contractions, migrated rightward at a rate of 25.6 cm min-1 and a frequency of 11 cpm.

Video S2. The putative phase IV in Case A. This phase is characterized by the presence of sporadic contractions and asynchronous waves that followed immediately after phase III.

Video S3. The clustered MWs in Case B were moving steadily rightward at a rate of 22 cm min-1 and a frequency of 11 cpm.

Video S4. The MWs in Case C moved smoothly leftward at a rate of 25.3 cm min-1 and a frequency of 9.7 cycles per minute. Moderate amount of ascites was noted.

Video S5. In Case C, about 8 minutes after a test meal, inflow of chyme distending the lumen sequentially toward the left was observed, which coincided with the direction of the pre-existing MWs. Note that, The MWs turned adynamic (serpent-like) long before the chyme arrived, i.e. the abolishment of the MWs is not caused by mechanical distension but rather something happened earlier. This feature agrees with the neurohumoral nature of phase III.

FilenameFormatSizeDescription
NMO_12023_sm_Legends-Revised.doc26KSupporting info item
NMO_12023_sm_VideoS1.mov6238KSupporting info item
NMO_12023_sm_VideoS2.mov6516KSupporting info item
NMO_12023_sm_VideoS3.mov8697KSupporting info item
NMO_12023_sm_VideoS4.mov8769KSupporting info item
NMO_12023_sm_VideoS5.mov8058KSupporting info item

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