Associations Between Colonic Motor Patterns and Autonomic Nervous System Activity Assessed by High-Resolution Manometry and Concurrent Heart Rate Variability

Yuhong Yuan, M Khawar Ali, Karen J Mathewson, Kartik Sharma, Mahi Faiyaz, Wei Tan, Sean P Parsons, Kailai K Zhang, Natalija Milkova, Lijun Liu, Elyanne Ratcliffe, David Armstrong, Louis A Schmidt, Ji-Hong Chen, Jan D Huizinga, Yuhong Yuan, M Khawar Ali, Karen J Mathewson, Kartik Sharma, Mahi Faiyaz, Wei Tan, Sean P Parsons, Kailai K Zhang, Natalija Milkova, Lijun Liu, Elyanne Ratcliffe, David Armstrong, Louis A Schmidt, Ji-Hong Chen, Jan D Huizinga

Abstract

Abnormal colonic motility may be associated with dysfunction of the autonomic nervous system (ANS). Our aim was to evaluate if associations between colonic motor patterns and autonomic neural activity could be demonstrated by assessing changes in heart rate variability (HRV) in healthy volunteers. A total of 145 colonic motor patterns were assessed in 11 healthy volunteers by High-Resolution Colonic Manometry (HRCM) using an 84-channel water-perfused catheter. Motor patterns were evoked by balloon distention, a meal and luminal bisacodyl. The electrocardiogram (ECG) and cardiac impedance were assessed during colonic manometry. Respiratory sinus arrhythmia (RSA) and root mean square of successive differences of beat-to-beat intervals (RMSSD) served as measures of parasympathetic reactivity while the Baevsky's Stress Index (SI) and the pre-ejection period (PEP) were used as measures of sympathetic reactivity. Taking all motor patterns into account, our data show that colonic motor patterns are accompanied by increased parasympathetic activity and decreased sympathetic activity that may occur without eliciting a significant change in heart rate. Motor Complexes (more than one motor pattern occurring in close proximity), High-Amplitude Propagating Pressure Waves followed by Simultaneous Pressure Waves (HAPW-SPWs) and HAPWs without SPWs are all associated with an increase in RSA and a decrease in SI. Hence RSA and SI may best reflect autonomic activity in the colon during these motor patterns as compared to RMSSD and PEP. SI and PEP do not measure identical sympathetic reactivity. The SPW, which is a very low amplitude pressure wave, did not significantly change the autonomic measures employed here. In conclusion, colonic motor patterns are associated with activity in the ANS which is reflected in autonomic measures of heart rate variability. These autonomic measures may serve as proxies for autonomic neural dysfunction in patients with colonic dysmotility.

Keywords: PEP; RSA; autonomic nervous system; baevsky stress index; colonic motility; high-amplitude pressure waves; parasympathetic; sympathetic.

Copyright © 2020 Yuan, Ali, Mathewson, Sharma, Faiyaz, Tan, Parsons, Zhang, Milkova, Liu, Ratcliffe, Armstrong, Schmidt, Chen and Huizinga.

Figures

FIGURE 1
FIGURE 1
Motor patterns. (A) High-Amplitude Propagating Pressure Waves (HAPWs) occurring as a single isolated event. White line indicates the presence of a 10 cm long balloon in the catheter where no data could be collected. The anal sphincter pressure is seen at 86 cm. 0 cm is in the proximal colon. (B) A HAPW followed by a simultaneous pressure wave (SPW) referred to as HAPW-SPW. White line indicates the presence of a 10 cm long balloon in the catheter where no data could be collected. The catheter was fully inside the colon such that the anal sphincter activity was not recorded. The HAPW started distal to the balloon. (C) Motor Complexes, defined as two or more distinct propulsive motor patterns that followed each other closely so that HRV changes could not be assessed for the individual patterns. In this catheter, two balloons were present at the white lines so that two sections of 10 cm did not have pressure sensors. No anal activity was recorded.
FIGURE 2
FIGURE 2
Changes in autonomic activity in response to posture changes (n = 11), Significance was assessed by one-way ANOVA with repeated measures and Bonferroni correction for (A,B,D,E). Friedman test followed by Dunn’s multiple comparison tests was used to assess significance for (C). (A) RSA declined upon standing and walking compared to the supine baseline position. (B) RMSSD declined upon standing and walking compared to the supine baseline position. (C) SI increased upon standing and walking compared to baseline position. (D) PEP decreased significantly only during walking. (E) Heart rate increases upon standing and walking compared to the supine baseline position.
FIGURE 3
FIGURE 3
Changes in autonomic activity in response to all motor patterns. Data sets are derived by averaging all 145 motor patterns within subjects, hence n = 11. The Friedman test was applied for assessment of significance, followed by the Dunn’s multiple comparisons test. (A) RSA increased significantly during the motor activity and recovered within 2 min. (B) RMSSD increased significantly during the motor activity and recovered. (C) SI decreased significantly during the motor activity. (D) PEP decreased significantly after motor activity. (E) Heart rate remained unchanged.
FIGURE 4
FIGURE 4
Overall changes in autonomic activity in response to Motor Complexes (N = 42; n = 9). The following HRV parameters were assessed: RSA (A), RMSSD (B), the Baevsky’s Stress Index (SI) (C), PEP (D), and heart rate (E). Data sets were derived by averaging all motor patterns within subjects, hence n = 9). The Friedman test was applied for assessment of significance followed by Dunn’s multiple comparisons test (F-M).
FIGURE 5
FIGURE 5
Changes in autonomic activity in response to all individual Motor Complexes (N = 42). Data are shown as% change. The Friedman test was applied for assessment of significance followed by Dunn’s multiple comparisons test. RSA: before to during p = 0.0007; during to recovery, p < 0.0001. SI: before to during p = 0.0104; during to recovery, p ≤ 0.0001 (F-D).
FIGURE 6
FIGURE 6
Overall changes in autonomic activity in response to HAPW-SPW’s. Data sets are derived by averaging all 45 motor patterns within 7 subjects, hence n = 7. The following HRV parameters were assessed: RSA (A), RMSSD (B), the Baevsky’s Stress Index (SI) (C), PEP (D), and heart rate (E). The Friedman test was applied for assessment of significance followed by Dunn’s multiple comparisons test (F-D-M).
FIGURE 7
FIGURE 7
Changes in autonomic activity in response to all HAPW-SPW’s N = 45. Data are shown as % change. The Friedman test was applied for assessment of significance followed by Dunn’s multiple comparisons test. RSA: before to during p = 0.0018; during to recovery, p ≤ 0.0001. SI: before to during p = 0.0022; during to recovery, p < 0.0001 (F-D).
FIGURE 8
FIGURE 8
Overall changes in autonomic activity in response to HAPW’s. Data sets are derived by averaging all motor patterns within subjects, hence n = 6). The following HRV parameters were assessed: RSA (A), RMSSD (B), the Baevsky’s Stress Index (SI) (C), PEP (D), and heart rate (E). The Friedman test was applied for assessment of significance followed by Dunn’s multiple comparisons test (F-D-M).
FIGURE 9
FIGURE 9
Changes in autonomic activity in response to all HAPW’s (N = 28). Data are shown as % change. The Friedman test was applied for assessment of significance followed by Dunn’s multiple comparisons test. RSA: before to during, not significant; during to recovery, not significant. SI: before to during p = 0.0389; during to recovery, p = 0.004 (F-D).
FIGURE 10
FIGURE 10
Overall Changes in autonomic activity in response to 30 SPW’s. Data sets were derived by averaging all motor patterns within subjects, hence n = 6. The following HRV parameters were assessed: RSA (A), RMSSD (B), the Baevsky’s Stress Index (SI) (C), PEP (D), and heart rate (E). The Friedman test was applied for assessment of significance followed by Dunn’s multiple comparisons test (F-D-M).
FIGURE 11
FIGURE 11
Changes in autonomic activity in response to all SPW’s (N = 30). Data are shown as % change. The Friedman test was applied for assessment of significance followed by Dunn’s multiple comparisons test. RSA: before to during, ns; during to recovery, p = 0.0142. SI: before to during: ns.; during to recovery, p = 0.0021 (F-D).
FIGURE 12
FIGURE 12
Correlations between supine HRV parameters and changes in HRV parameters due to posture changes compared to the changes in those measures due to motor activity. (A) Correlation between RSA during supine rest and change in RSA during HAPW. (B) Correlation between RMSSD during supine rest and change in RSA during HAPW. (C) Correlation between change in RMSSD from supine to standing and change in RSA during HAPW. (D) Correlation between PEP during supine rest and change in PEP during HAPW-SPW.

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