First translational consensus on terminology and definitions of colonic motility in animals and humans studied by manometric and other techniques

Abstract

Alterations in colonic motility are implicated in the pathophysiology of bowel disorders, but high-resolution manometry of human colonic motor function has revealed that our knowledge of normal motor patterns is limited. Furthermore, various terminologies and definitions have been used to describe colonic motor patterns in children, adults and animals. An example is the distinction between the high-amplitude propagating contractions in humans and giant contractions in animals. Harmonized terminology and definitions are required that are applicable to the study of colonic motility performed by basic scientists and clinicians, as well as adult and paediatric gastroenterologists. As clinical studies increasingly require adequate animal models to develop and test new therapies, there is a need for rational use of terminology to describe those motor patterns that are equivalent between animals and humans. This Consensus Statement provides the first harmonized interpretation of commonly used terminology to describe colonic motor function and delineates possible similarities between motor patterns observed in animal models and humans in vitro (ex vivo) and in vivo. The consolidated terminology can be an impetus for new research that will considerably improve our understanding of colonic motor function and will facilitate the development and testing of new therapies for colonic motility disorders.

Fig. 1. Myogenic motor patterns in animals.

The images show graphical representations of wall motion captured by video recordings of a colon segment in an organ bath. Each frame of the video is converted to a greyscale image that maps changes in colon diameter. In these diameter maps (DMaps), darker shading represents an increased diameter (dilation) and lighter regions represent a reduced diameter (contraction). The three DMaps show the three main myogenic (non-neurogenic) patterns of motor activity in the colon of different animal species (in vitro isolated preparations). a | In the colon of most experimental animals, chaotic shallow contractions, termed ripples, are generated by a network of pacemaker cells at the submucous border (interstitial cells of Cajal (ICC) submucosal) acting on the circular muscle to elicit slow waves. In this example from a rabbit distal colon, these ripples become prominent once the neural activity is blocked by tetrodotoxin. b | In some species, faster ripples have been recorded, which seem to be generated by a net of pacemaker cells located at the myenteric plexus level (ICC myenteric). In this example from the rabbit proximal colon, fast phasic contractions appear following application of hexamethonium, which blocks nicotinic receptors. c | Slow phasic contractions have been recorded, for example in the rat colon after blocking neural activity with lidocaine and then applying the cholinergic agonist carbachol; whether these slow myogenic contractions exist in all species remains to be determined. Part a adapted with permission from ref., The American Physiological Society. Part b adapted from ref., Springer Nature Limited. Part c adapted from ref., CC-BY-4.0 https://creativecommons.org/licenses/by/4.0/.

Fig. 2. Neurogenic motor patterns in animals.

Images a–c show examples of neurogenic motor patterns expressed as spatiotemporal maps showing changes in diameter (DMaps) of the excised colon of different animal species in vitro. Two main neurogenic motor patterns have been recognized. The first is neural peristalsis (consensus term) triggered by distension, which was described as propulsive contractions in the guinea pig distal colon (part a) and subsequently as long-distance contractions in the rabbit colon (part b). The second motor pattern present in the rabbit proximal colon consists of very slowly propagating contractions, representing the neural colonic motor complex (part c) and subsequently as haustral boundary contractions or progression (part b). In the complete mouse colon (part d) and in the guinea pig distal colon (part e) colonic motor complexes occur in distended segments. Neurogenic peristalsis is triggered and sustained by content, whereas the colonic motor complexes are generated as regular motor activity slowly traversing long segments of colon or appearing even in the absence of any propulsion of contents. Part a adapted with permission from ref., The American Physiological Society. Part b adapted with permission from ref., The American Physiological Society. Part c adapted with permission from ref., The American Physiological Society. Part d adapted with permission from ref., Wiley-VCH. Part e adapted with permission from ref., Wiley-VCH.

Fig. 3. Motor patterns in isolated strips of the human colon.

a | Low-frequency contractions superimposed with intermediate-frequency motor events or ripples. b | Intermediate-frequency motor events or ripples. c | High-frequency contractions. Different time and amplitude scales were used to optimally visualise each type of contractile activity.

Fig. 4. Colonic motor patterns of an excised section of human sigmoid colon.

a | The excised sigmoid colon is placed into an organ bath filled with an oxygenated Krebs solution maintained at 37°C. Motor patterns are recorded by a high-resolution manometric catheter attached to a rod at the base of the preparation. b | A series of propagating pressure waves recorded from the section of the colon. Three large propagating contractions start at the oral end and move towards the anal end of the segment.

Fig. 5. Colonic motor patterns frequently identified by HRM in adults.

The introduction of high-resolution manometry (HRM) increased the accuracy of the detection of colonic motor patterns. The most frequently detected patterns in adults are simultaneous pressure increases, cyclic propagating motor patterns and haustral activity. a | Examples of simultaneous pressure increases (pan-colonic pressurizations). These are characterized by simultaneous pressure increases recorded across all recording sensors and are associated with relaxation of the anal sphincter. b | The cyclic propagating motor pattern, shown as a spatiotemporal colour plot, recorded in a healthy adult colon. This activity increases after a meal, originates at the rectosigmoid junction and propagates primarily in a retrograde direction (anal to oral). c | Cyclic propagating motor patterns can also occur in clusters spaced at 1–4-min intervals. These clusters appear after the consumption of a high-calorie meal. d | Intrahaustral activity often has a frequency of ~3 cpm in ≤5 consecutive sensors and, therefore, seems to be activity within a haustrum. Part d adapted from ref., CC-BY-4.0 https://creativecommons.org/licenses/by/4.0/.

Fig. 6. HAPCs in children.

Normally and abnormally propagating high-amplitude propagating contractions (HAPCs) have been identified by high-resolution manometry in children. a | In normal HAPCs, the amplitude is >75 mmHg and the contractions propagate distally to the rectosigmoid junction. The anal sphincter relaxes concurrently to the HAPC. b | In abnormally propagating HAPCs, the contractions do not propagate beyond the transverse colon. c | An abnormal configuration of HAPCs with multipeaked waveforms and prolonged duration. This configuration has been associated with histological evidence of colonic neuropathy.

Fig. 7. Scintigraphic assessment of gastrointestinal transit.

a | Gastric emptying and small intestinal transit are assessed with ^99mTc-labelled polystyrene pellets, whereas colonic transit is measured with ¹¹¹In-labelled charcoal in delayed-release capsules. b | Proportion of ¹¹¹In counts in each of four colonic regions of interest and stool is multiplied by the appropriate weighting factor, ranging from 1 to 5.

Fig. 8. Assessment of colonic motility using a barostat.

The barostat–manometric assembly is positioned in the descending colon with a polyethylene balloon in apposition to the colonic mucosa. The device maintains the balloon at a pressure that ensures that the colonic wall is not distended. Contractions of the colonic wall induce a decrease in the baseline balloon volume, which is recorded by the barostat.

Fig. 9. MRI assessment of colonic wall movement.

MRI enables the measurement of various characteristics of the gastrointestinal tract, such as organ volumes, transit rate and motility. In this MRI of a sagittal section of the ascending colon, the horizontal lines define the colonic lumen. During cine MRI, changes in the lengths of the lines provide a measure of transverse wall velocity, which enables the calculation of a motility index (the percentage of data points at which the wall velocity is >0.5 mm/s).