The cyclic motor patterns in the human colon.
colonic motility
cyclic motor pattern
high-resolution colonic manometry
interstitial cells of Cajal
rectal pressure waves
Journal
Neurogastroenterology and motility
ISSN: 1365-2982
Titre abrégé: Neurogastroenterol Motil
Pays: England
ID NLM: 9432572
Informations de publication
Date de publication:
05 2020
05 2020
Historique:
received:
20
12
2018
revised:
31
12
2019
accepted:
03
01
2020
pubmed:
4
3
2020
medline:
20
4
2021
entrez:
4
3
2020
Statut:
ppublish
Résumé
High-resolution colonic manometry gives an unprecedented window into motor patterns of the human colon. Our objective was to characterize motor activities throughout the entire colon that possessed persistent rhythmicity and spanning at least 5 cm. High-resolution colonic manometry using an 84-channel water-perfused catheter was performed in 19 healthy volunteers. Rhythmic activity was assessed during baseline, proximal balloon distention, meal, and bisacodyl administration. Throughout the entire colon, a cyclic motor pattern occurred either in isolation or following a high-amplitude propagating pressure wave (HAPW), consisting of clusters of pressure waves at a frequency centered on 11-13 cycles/min, unrelated to breathing. The cluster duration was 1-6 minutes; the pressure waves traveled for 8-27 cm, lasting 5-8 seconds. The clusters itself could be rhythmic at 0.5-2 cpm. The propagation direction of the individual pressure waves was mixed with >50% occurring simultaneous. This high-frequency cyclic motor pattern co-existed with the well-known low-frequency cyclic motor pattern centered on 3-4 cpm. In the rectum, the low-frequency cyclic motor pattern dominated, propagating predominantly in retrograde direction. Proximal balloon distention, a meal and bisacodyl administration induced HAPWs followed by cyclic motor patterns. Within cyclic motor patterns, retrograde propagating, low-frequency pressure waves dominate in the rectum, likely keeping the rectum empty; and mixed propagation, high-frequency pressure waves dominate in the colon, likely promoting absorption and storage, hence contributing to continence. Propagation and frequency characteristics are likely determined by network properties of the interstitial cells of Cajal.
Sections du résumé
BACKGROUND
High-resolution colonic manometry gives an unprecedented window into motor patterns of the human colon. Our objective was to characterize motor activities throughout the entire colon that possessed persistent rhythmicity and spanning at least 5 cm.
METHODS
High-resolution colonic manometry using an 84-channel water-perfused catheter was performed in 19 healthy volunteers. Rhythmic activity was assessed during baseline, proximal balloon distention, meal, and bisacodyl administration.
KEY RESULTS
Throughout the entire colon, a cyclic motor pattern occurred either in isolation or following a high-amplitude propagating pressure wave (HAPW), consisting of clusters of pressure waves at a frequency centered on 11-13 cycles/min, unrelated to breathing. The cluster duration was 1-6 minutes; the pressure waves traveled for 8-27 cm, lasting 5-8 seconds. The clusters itself could be rhythmic at 0.5-2 cpm. The propagation direction of the individual pressure waves was mixed with >50% occurring simultaneous. This high-frequency cyclic motor pattern co-existed with the well-known low-frequency cyclic motor pattern centered on 3-4 cpm. In the rectum, the low-frequency cyclic motor pattern dominated, propagating predominantly in retrograde direction. Proximal balloon distention, a meal and bisacodyl administration induced HAPWs followed by cyclic motor patterns.
CONCLUSIONS AND INFERENCES
Within cyclic motor patterns, retrograde propagating, low-frequency pressure waves dominate in the rectum, likely keeping the rectum empty; and mixed propagation, high-frequency pressure waves dominate in the colon, likely promoting absorption and storage, hence contributing to continence. Propagation and frequency characteristics are likely determined by network properties of the interstitial cells of Cajal.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13807Subventions
Organisme : CIHR
Pays : Canada
Informations de copyright
© 2020 John Wiley & Sons Ltd.
Références
Rodriguez L, Sood M, Di Lorenzo C, Saps M. An ANMS-NASPGHAN consensus document on anorectal and colonic manometry in children. Neurogastroenterol Motil. 29(1):e12944.
Camilleri M, Bharucha AE, Di Lorenzo C, et al. American Neurogastroenterology and Motility Society consensus statement on intraluminal measurement of gastrointestinal and colonic motility in clinical practice. Neurogastroenterol Motil. 2008;20(12):1269-1282.
Giorgio V, Borrelli O, Smith VV, et al. High-resolution colonic manometry accurately predicts colonic neuromuscular pathological phenotype in pediatric slow transit constipation. Neurogastroenterol Motil. 2013;25(1):70-e9.
Dinning PG, Wiklendt L, Maslen L, et al. Colonic motor abnormalities in slow transit constipation defined by high resolution, fibre-optic manometry. Neurogastroenterol Motil. 2015;27:379-388.
Rao SSC, Sadeghi P, Beaty J, Kavlock R, Ackerson K. Ambulatory 24-h colonic manometry in healthy humans. Am J Physiol Gastrointest Liver Physiol. 2001;280(4):G629-G639.
Chen J-H, Parsons SP, Shokrollahi M, et al. Characterization of simultaneous pressure waves as biomarkers for colonic motility assessed by high-resolution colonic manometry. Front Physiol Gastrointestinal Sci. 2018;9:1248.
Corsetti M, Pagliaro G, Demedts I, et al. Pan-colonic pressurizations associated with relaxation of the anal sphincter in health and disease: a new colonic motor pattern identified using high-resolution manometry. Am J Gastroenterol. 2017;112:479-489.
Lin AY, Du P, Dinning PG, et al. High-resolution anatomic correlation of cyclic motor patterns in the human colon: evidence of a rectosigmoid brake. Am J Physiol Gastrointest Liver Physiol. 2017;312(5):G508-G515.
Rao SS, Sadeghi P, Batterson K, et al. Altered periodic rectal motor activity: a mechanism for slow transit constipation. Neurogastroenterol Motil. 2001;13(6):591-598.
Snape WJ Jr, Carlson GM, Matarazzo SA, et al. Evidence that abnormal myoelectrical activity produces colonic motor dysfunction in the irritable bowel syndrome. Gastroenterology. 1977;72(3):383-387.
Narducci F, Bassotti G, Gaburri M, Morelli A. Twenty four hour manometric recording of colonic motor activity in healthy man. Gut. 1987;28(1):17-25.
Rao SS, Welcher K. Periodic rectal motor activity: the intrinsic colonic gatekeeper. Am J Gastroenterol. 1996;91(5):890-897.
Dinning PG, Wiklendt L, Maslen L, et al. Quantification of in vivo colonic motor patterns in healthy humans before and after a meal revealed by high-resolution fiber-optic manometry. Neurogastroenterol Motil. 2014;26(10):1443-1457.
Sarna SK, Waterfall WE, Bardakjian BL, Lind JF. Types of human colonic electrical activities recorded postoperatively. Gastroenterology. 1981;81(1):61-70.
Bueno L, Fioramonti J, Ruckebusch Y, Frexinos J, Coulom P. Evaluation of colonic myoelectrical activity in health and functional disorders. Gut. 1980;21(6):480-485.
Huizinga JD, Waterfall WE. Electrical correlate of circumferential contractions in human colonic circular muscle. Gut. 1988;29(1):10-16.
Huizinga, JD. The physiology and pathophysiology of interstitial cells of Cajal: pacemaking, innervation, and stretch sensation. In Said H, Kaunitz JK, Ghishan F, Merchant J, Wood J (Eds.), Physiology of the Gastrointestinal Tract. Elsevier; 2018: 305-336.
Blair PJ, Rhee P-L, Sanders KM, Ward SM. The significance of interstitial cells in neurogastroenterology. J Neurogastroenterol Motil. 2014;20(3):294-317.
Huizinga JD, Lammers WJ. Gut peristalsis is governed by a multitude of cooperating mechanisms. Am J Physiol Gastrointest Liver Physiol. 2009;296(1):G1-G8.
Knowles CH, Farrugia G. Gastrointestinal neuromuscular pathology in chronic constipation. Best Pract Res Clin Gastroenterol. 2011;25(1):43-57.
Hasler WL. Is constipation caused by a loss of colonic interstitial cells of Cajal? Gastroenterology. 2003;125(1):264-265.
Der-Silaphet T, Malysz J, Hagel S, Arsenault AL, Huizinga JD. Interstitial cells of Cajal direct normal propulsive contractile activity in the mouse small intestine. Gastroenterology. 1998;114(4):724-736.
Farrugia G. Reply to: Hasler, WL. Is constipation caused by a loss of colonic interstitial cells of Cajal? Gastroenterology 125 (2003) 264-265. Gastroenterology. 2003;125:265-266.
Cipriani G, Gibbons SJ, Verhulst PJ, et al. Diabetic Csf1 op/opmice lacking macrophages are protected against the development of delayed gastric emptying. Cell Mol Gastroenterol Hepatol. 2016;2(1):40-47.
Coss-Adame E, Rao SSC, Valestin J, Ali-Azamar A, Remes-Troche JM. Accuracy and reproducibility of high-definition anorectal manometry and pressure topography analyses in healthy subjects. Clin Gastroenterol Hepatol. 2015;13(6):1143-1150. e1.
Liem O, Burgers RE, Connor FL, et al. Solid-state vs water-perfused catheters to measure colonic high-amplitude propagating contractions. Neurogastroenterol Motil. 2012;24(4):345-e167. https://doi.org/10.1111/j.1365.
Koppen IJN, Wiklendt L, Yacob D, Di Lorenzo C, Benninga MA, Dinning PG. Motility of the left colon in children and adolescents with functional constpation; a retrospective comparison between solid-state and water-perfused colonic manometry. Neurogastroenterol Motil. 2018;30(9):e13401.
Chen J-H, Yu Y, Yang Z, et al. Intraluminal pressure patterns in the human colon assessed by high-resolution manometry. Sci Rep. 2017;7:41436.
Rao SSC, Sadeghi P, Beaty J, Kavlock R. Ambulatory 24-hour colonic manometry in slow-transit constipation. Am J Gastroenterol. 2004;99(12):2405-2416.
Vather R, O'Grady G, Lin AY, et al. Hyperactive cyclic motor activity in the distal colon after colonic surgery as defined by high-resolution colonic manometry. Br J Surg. 2018;105(7):907-917.
Wiklendt L, Mohammed SD, Scott SM, Dinning PG. Classification of normal and abnormal colonic motility based on cross-correlations of pancolonic manometry data. Neurogastroenterol Motil. 2013;25(3):e215-e223.
Huizinga JD, Chen J-H, Fang Zhu Y, et al.: The origin of segmentation motor activity in the intestine. Nat Commun. 2014;5:3326.
Code CF, Hightower NC Jr, Morlock CG. Motility of the alimentary canal in man; review of recent studies. Am J Med. 1952;13(3):328-351.
Kerlin P, Zinsmeister A, Phillips S. Motor responses to food of the ileum, proximal colon, and distal colon of healthy humans. Gastroenterology. 1983;84(4):762-770.
Bampton PA, Dinning PG, Kennedy ML, Lubowski DZ, Cook IJ. The proximal colonic motor response to rectal mechanical and chemical stimulation. Am J Physiol Gastrointest Liver Physiol. 2002;282(3):G443-G449.
Bampton PA, Dinning PG, Kennedy ML, Lubowski DZ, deCarle D, Cook IJ. Spatial and temporal organization of pressure patterns throughout the unprepared colon during spontaneous defecation. Am J Gastroenterol. 2000;95(4):1027-1035.
Cook IJ, Furukawa Y, Panagopoulos V, Collins PJ, Dent J. Relationships between spatial patterns of colonic pressure and individual movements of content. Am J Physiol Gastrointest Liver Physiol. 2000;278(2):G329-G341.
Vather R, O'Grady G, Arkwright JW, et al. Restoration of normal colonic motor patterns and meal responses after distal colorectal resection. Br J Surg. 2016;103(4):451-461.
Couturier D, Roze C, Couturier-Turpin MH, Debray C.: Electromyography of the colon in situ. An experimental study in man and in the rabbit. Gastroenterology. 1969;56(2):317-322.
Schang JC, Devroede G. Fasting and postprandial myoelectric spiking activity in the human sigmoid colon. Gastroenterology. 1983;85(5):1048-1053.
Huizinga JD, Stern HS, Chow E, Diamant NE, El-Sharkawy TY. Electrophysiologic control of motility in the human colon. Gastroenterology. 1985;88(2):500-511.
Huizinga JD, Stern HS, Chow E, Diamant NE, El-Sharkawy TY. Electrical basis of excitation and inhibition of human colonic smooth muscle. Gastroenterology. 1986;90(5 Pt 1):1197-1204.
Rumessen JJ, Vanderwinden J-M, Rasmussen H, Hansen A, Horn T. Ultrastructure of interstitial cells of Cajal in myenteric plexus of human colon. Cell Tissue Res. 2009;337(2):197-212.
Rumessen JJ, Thuneberg L. Pacemaker cells in the gastrointestinal tract: interstitial cells of Cajal. Scand J Gastroenterol Suppl. 1996;216:82-94.
Christensen J. Myoelectric control of the colon. Gastroenterology. 1975;68(3):601-609.
Huizinga JD, Parsons SP. Pacemaker network properties determine intestinal motor pattern behaviour. Exp Physiol. 2019;104:623-624.
Parsons SP, Huizinga JD. Phase waves and trigger waves: emergent properties of oscillating and excitable networks in the gut. J Physiol. 2018;596:4819-4829.
Parsons SP, Huizinga JD. The phase response and state space of slow wave contractions in the small intestine. Exp Physiol. 2017;102(9):1118-1132.
Wei R, Parsons SP, Huizinga JD. Network properties of ICC affect intestinal pacemaker activities and motor patterns, according to a mathematical model of weakly coupled oscillators. Exp Physiol. 2017;102:329-346.
Quan X, Yang Z, Xue M, Chen J-H, Huizinga JD. Relationships between motor patterns and intraluminal pressure in the 3-taeniated proximal colon of the rabbit. Sci Rep. 2017;7:42293.
Picon L, Lémann M, Flourié B, Rambaud J-C, Rain J-D, Jian R. Right and left colonic transit after eating assessed by a dual isotopic technique in healthy humans. Gastroenterology. 1992;103(1):80-85.
Ritchie JA. Colonic motor activity and bowel function. I. Normal movement of contents. Gut. 1968;9(4):442-456.
Dinning PG, Sia TC, Kumar R, et al. High-resolution colonic motility recordings in vivo compared with ex vivo recordings after colectomy, in patients with slow transit constipation. Neurogastroenterol Motil. 2016;28:1824-1835.
Bassotti G, Chiarioni G, Germani U, Battaglia E, Vantini I, Morelli A. Endoluminal instillation of bisacodyl in patients with severe (slow transit type) constipation is useful to test residual colonic propulsive activity. Digestion. 1999;60(1):69-73.
Bassotti G, Battaglia E, de Roberto G, Morelli A, Tonini M, Villanacci V. Alterations in colonic motility and relationship to pain in colonic diverticulosis. Clin Gastroenterol Hepatol. 2005;3:248-253.
Moreno-Osset E, Bazzocchi G, Lo S, et al. Association between postprandial changes in colonic intraluminal pressure and transit. Gastroenterology. 1989;96(5 Pt 1):1265-1273.
Bampton PA, Dinning PG, Kennedy ML, et al. Prolonged multi-point recording of colonic manometry in the unprepared human colon: providing insight into potentially relevant pressure wave parameters. Am J Gastroenterol. 2001;96(6):1838-1848.
Dinning PG, Benninga MA, Southwell BR, et al. Paediatric and adult colonic manometry: a tool to help unravel the pathophysiology of constipation. World J Gastroenterol. 2010;16(41):5162-5172.
Bassotti G, Chistolini F, Battaglia E, et al. Are colonic regular contractile frequency patterns in slow transit constipation a relevant pathophysiological phenomenon. Dig Liver Dis. 2003;35(8):552-556.
Parsons SP, Huizinga JD. Spatial noise in coupling strength and natural frequency within a pacemaker network: consequences for development of intestinal motor patterns according to a weakly coupled oscillator model. Front Neurosci. 2016;10:19.