Skip to main content
SpringerLink
Log in

A review of mixing and propulsion of chyme in the small intestine: fresh insights from new methods

  • Review
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

The small intestine is a convoluted flexible tube of inconstant form and capacity through which chyme is propelled and mixed by varying patterns of contraction. These inconstancies have prevented quantitative comparisons of the manner in which contractile activity engenders mixing of contained chyme. Recent quantitative work based on spatiotemporal mapping of intestinal contractions, macro- and micro-rheology, particle image velocimetry and real-time modelling has provided new insights into this process. Evidence indicates that the speeds and patterns of the various types of small intestinal contraction are insufficient to secure optimal mixing and enzymatic digestion over a minimal length of intestine. Hence particulate substrates and soluble nutrients become dispersed along the length of the lumen. Mixing within the lumen is not turbulent but results from localised folding and kneading of the contents by contractions but is augmented by the inconstant spatial disposition of the contractions and their component contractile processes. The latter include inconstancies in the sites of commencement and the directions of propagation of contraction in component groups of smooth muscle cells and in the coordination of the radial and circular components of smooth muscle contraction. Evidence suggests there is ongoing augmentation of mixing at the periphery of the lumen, during both the post-prandial and inter-meal periods, to promote flow around and between adjacent villi. This results largely from folding of the relatively inelastic mucosa during repeated radial and longitudinal muscular contraction, causing chyme to be displaced by periodic crowding and separation of the tips of the relatively rigid villi. Further, micro-rheological studies indicate that such peripheral mixing may extend to the apices of enterocytes owing to discontinuities in the mobile mucus layer that covers the ileal mucosa.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

Annealing of mucins:

Process of union of individual masses of mucin secreted from individual goblet cells by inter-diffusion of their respective carbohydrate side chains

Apical crowding of villi:

Gathering together of the tips of villi in the region between adjacent mucosal microfolds that leads to expulsion of fluid from the spaces between the tips

Continuously stirred tank reactor (CSTR):

A theoretical ideal chemical reactor that runs at a steady rate with continuous flow of reactants and product with complete, i.e. perfect mixing, so that the concentration of reactants is uniform within

Mucosal microfolds:

Inwardly projecting folds of mucosa that develop spontaneously as a result of relative differences in the mechanical properties and in the axial lengths of the mucosal and muscular components of the small intestine

Newtonian fluid:

A fluid in which the shear rates that develop during flow are always proportional to the shear stress applied, so that viscosity remains constant

Phasic contraction:

Concerted or coordinated short-lived contraction of groups of smooth muscle following neural or myogenic stimulation, e.g. peristalsis

Pseudoplasticity:

The property of a non-Newtonian fluid in which its apparent viscosity decreases with increase in shear rate

Reynolds number:

The ratio of the inertial forces within a moving fluid (that generally cause motion to continue) to viscous forces (that can be viewed as frictional and generally cause motion to slow). For flow within a simple tube Reynolds numbers of less than 2,300 are considered to describe a condition in which viscous forces predominate so that flow is laminar, i.e. occurs in an orderly fashion that can be viewed as a series of concentric tubes within the pipe. Conversely, Reynolds numbers >2,300 describe a condition in which inertial forces predominate so that flow in elements of the liquid become unstable and turbulent

Rheometry:

Techniques that determine the relationship between the forces that stress materials, or mixtures of materials, and the elastic and fluid deformations that they produce

Shear:

Deformation induced in a material when its layers are shifted laterally in relation to each other

Shear rate:

In a fluid is given by the rate of change in velocity (velocity gradient) with which one fluid layer passes over an adjacent layer

Strain:

Degree of deformation by stretch or compression. Generally determined as a percentage increase or decrease of original length

Strain rate:

The rate at which a component is deformed by stretching (positive strain rate) or compression for example during contraction (negative strain rate)

Stress:

Force per unit area either parallel or perpendicular to the area to which it is applied

Tonic contraction:

Longer lasting contraction resulting from sustained contraction of groups of component smooth muscle cells, chiefly through inhibition of actin–myosin ATPase, that generates ongoing tension (tone) within the wall of the structure in which it operates

Turbulent mixing:

A condition in which widespread mixing results from the ongoing appearance of unsteady vortices and areas of folding and kneading on many length scales that interact with one another other

Viscosity:

The ratio of the force that is applied to a liquid to the longitudinal movement of the fluid, i.e. shear, that it generates

Viscoelasticity:

Time-dependent property of materials that exhibit the characteristics of solid behaviour, i.e. elasticity and of liquid flow, i.e. viscosity when undergoing deformation. The elastic component of digesta is thought to result from interaction of the contained particles

References

  • Ahluwalia N, Thompson D, Barlow J, Heggie L (1994) Human small intestinal contractions and aboral traction forces during fasting and after feeding. Gut 35:625–630

    PubMed Central  CAS  PubMed  Google Scholar 

  • Angeli TR, O’Grady G, Du P, Paskaranandavadivel N, Pullan AJ, Bissett IP, Cheng LK (2013) Circumferential and functional re-entry of in vivo slow-wave activity in the porcine small intestine. Neurogastroenterol Mot 25:e304–e314

    CAS  Google Scholar 

  • Arkwright J, Blenman N, Underhill I, Maunder S, Szczesniak M, Dinning P, Cook I (2009) In-vivo demonstration of a high resolution optical fiber manometry catheter for diagnosis of gastrointestinal motility disorders. Opt Express 17:4500–4508

    CAS  PubMed  Google Scholar 

  • Arun CP (2004) The importance of being asymmetric: the physiology of digesta propulsion on earth and in space. Ann N Y Acad Sci 1027:74–84

    CAS  PubMed  Google Scholar 

  • Atuma C, Strugala V, Allen A, Holm L (2001) The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo. Am J Physiol 280:G922–G929

    CAS  Google Scholar 

  • Azpiroz F, Malagelada JR (1985) Physiological variations in canine gastric tone measured by an electronic barostat. Am J Physiol 248:G229–G237

    CAS  PubMed  Google Scholar 

  • Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI (2004) The gut microbiota as an environmental factor that regulates fat storage. Sci Signal 101:15718

    Google Scholar 

  • Bampton P, Dinning P, Kennedy M, Lubowski D, Cook I (2001) Prolonged multi-point recording of colonic manometry in the unprepared human colon: providing insight into potentially relevant pressure wave parameters. Am J Gastroenterol 96:1838–1848

    CAS  PubMed  Google Scholar 

  • Barry PH, Diamond J (1984) Effects of unstirred layers on membrane phenomena. Physiol Rev 64:763–872

    CAS  PubMed  Google Scholar 

  • Bates JM, Akerlund J, Mittge E, Guillemin K (2007) Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in zebrafish in response to the gut microbiota. Cell Host Microbe 2:371–382

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bayliss WM, Starling EH (1899) The movements and innervation of the small intestine. J Physiol 24:99–143

    PubMed Central  CAS  PubMed  Google Scholar 

  • Benard T, Bouchoucha M, Dupres M, Cugnenc PH (1997) In vitro analysis of rat intestinal wall movements at rest and during propagated contraction: a new method. Am J Physiol 273:G776–G784

    CAS  PubMed  Google Scholar 

  • Björnsson E, Abrahamsson H (1995) Interdigestive gastroduodenal manometry in humans. Indication of duodenal phase III as a retroperistaltic pump. Acta Physiol Scand 153:221–230

    PubMed  Google Scholar 

  • Bongaerts JHH, Rossetti D, Stokes JR (2007) The lubricating properties of human whole saliva. Trib Lett 27:277–287

    CAS  Google Scholar 

  • Bornhorst GM, Ströbinger N, Rutherfurd SM, Singh RP, Moughan PJ (2013) Properties of gastric chyme from pigs fed cooked brown or white rice. Food Biophys 8:12–23

    Google Scholar 

  • Bornstein JC, Furness JB, Kunze WAA, Bertrand PP (2002) Enteric reflexes that influence motility. In: Brookes SJH, Costa M (eds) Innervation of the Gastrointestinal Tract. Taylor & Francis, London, pp 1–55

    Google Scholar 

  • Brookes S, Costa M (2002) Innervation of the gastrointestinal tract. Taylor & Francis, London

    Google Scholar 

  • Bueno L, Fioramonti J, Ruckebusch Y (1975) Rate of flow of digesta and electrical activity of the small intestine in dogs and sheep. J Physiol 249:69–85

    PubMed Central  CAS  PubMed  Google Scholar 

  • Burns JC, Parkes T (1967) Peristaltic motion. J Fluid Mech 29:731–743

    Google Scholar 

  • Cannon WB (1898) The movements of the stomach studied by means of the Röntgen rays. Am J Physiol 1:359–382

    Google Scholar 

  • Cannon WB (1902) The movements of the intestines studied by means of the Röntgen rays. Am J Physiol 6:251–277

    Google Scholar 

  • Cannon WB (1912) Peristalsis, segmentation, and the myenteric reflex. Am J Physiol 30:114–128

    Google Scholar 

  • Castedal M, Björnsson E, Abrahamsson H (1998) Postprandial peristalsis in the human duodenum. Neurogastroenterol Mot 10:227–233

    CAS  Google Scholar 

  • Costa M, Furness J (1982) Nervous control of intestinal motility. Mediators and Drugs in Gastrointestinal Motility I. Springer, pp 279–382

  • Cserni T, Szekeres JP, Furka I, Németh N, Józsa T, Mikó I (2005) Hydrostatic characteristics of the ileocolic valve and intussuscepted nipple valves: an animal model. Investigative Surgery 18:185–191

    Google Scholar 

  • de Gennes PG (1971) Reptation of a polymer chain in the presence of fixed obstacles. J Chem Phys 55:572–579

    Google Scholar 

  • de Loubens C, Lentle RG, Love RJ, Hulls C, Janssen PWM (2013) Fluid mechanical consequences of pendular activity, segmentation, and pyloric outflow in the proximal duodenum of the rat and the guinea pig. J R Soc Interface 10:20130027

    PubMed Central  PubMed  Google Scholar 

  • de Loubens C, Lentle RG, Hulls C, Janssen PW, Love RJ, Chambers JP (2014) Characterisation of mixing in the proximal duodenum of the rat during longitudinal contractions and comparison with a fluid mechanical model based on spatiotemporal motility data. PLoS One 9:e95000

    PubMed Central  PubMed  Google Scholar 

  • Dikeman CL, Barry KA, Murphy MR, Fahey JGC (2007a) Diet and measurement techniques affect small intestinal digesta viscosity among dogs. Nut Res 27:56–65

    CAS  Google Scholar 

  • Dikeman CL, Murphy MR, Fahey GC (2007b) Diet type affects viscosity of ileal digesta of dogs and simulated gastric and small intestinal digesta. J Anim Physiol Anim Nutr 91:139–147

    CAS  Google Scholar 

  • Dillard S, Krishnan S, Udaykumar H (2007) Mechanics of flow and mixing at antroduodenal junction. World J Gastroenterol 13:1365

    PubMed Central  PubMed  Google Scholar 

  • Dinning PG, Arkwright JW, Costa M, Wiklendt L, Hennig G, Brookes SJ, Spencer NJ (2011a) Temporal relationships between wall motion, intraluminal pressure, and flow in the isolated rabbit small intestine. Am J Physiol Gastrointest LiverPhysiol 300:G577–G585

    CAS  Google Scholar 

  • Dinning PG, Arkwright JW, Costa M, Wiklendt L, Hennig G, Brookes SJH, Spencer NJ (2011b) Temporal relationships between wall motion, intraluminal pressure, and flow in the isolated rabbit small intestine. Am J Physiol 300:G577–G585

    CAS  Google Scholar 

  • Dinning P, Wiklendt L, Gibbins I, Patton V, Bampton P, Lubowski D, Cook I, Arkwright J (2013) Low-resolution colonic manometry leads to a gross misinterpretation of the frequency and polarity of propagating sequences: initial results from fiber-optic high-resolution manometry studies. Neurogastroenterol Mot 25:e640–e649

    CAS  Google Scholar 

  • Donnelly G, Jackson TD, Ambrous K, Ye J, Safdar A, Farraway L, Huizinga JD (2001) The myogenic component in distention-induced peristalsis in the guinea pig small intestine. Am J Physiol 280:G491–G500

    CAS  Google Scholar 

  • Egorov VI, Schastlivtsev IV, Prut EV, Baranov AO, Turusov RA (2002) Mechanical properties of the human gastrointestinal tract. J Biomech 35:1417–1425

    PubMed  Google Scholar 

  • Ensign-Hodges L, Henning A, Schneider C, Maisel K, Wang Y-Y, Porosoff M, Cone R, Hanes J (2013) Ex vivo characterization of particle transport in mucus secretions coating freshly excised mucosal tissues. Mol Pharmaceut 10(6):2176–2182

    Google Scholar 

  • Ermund A, Schütte A, Johansson ME, Gustafsson JK, Hansson GC (2013) Studies of mucus in mouse stomach, small intestine, and colon. I. Gastrointestinal mucus layers have different properties depending on location as well as over the Peyer’s patches. Am J Physiol Gastrointest LiverPhysiol 305:G341–G347

    CAS  Google Scholar 

  • France J, Thornley JHM, Siddons RC, Dhanoa MS (1993) On incorporating diffusion and viscosity concepts into compartmental models for analysing faecal marker excretion patterns in ruminants. Br J Nutr 70:369–378

    CAS  PubMed  Google Scholar 

  • Fullard L, Lammers W, Wake GC, Ferrua MJ (2014) Propagating longitudinal contractions in the ileum of the rabbit–efficiency of advective mixing. Food function 5(11):2731–2742

    CAS  PubMed  Google Scholar 

  • Galligan JJ, Vanner S (2005) Basic and clinical pharmacology of new motility promoting agents. Neurogastroenterol Mot 17:643–653

    CAS  Google Scholar 

  • Gordon AR, Siegman MJ (1971) Mechanical properties of smooth muscle. I. Length-tension and force-velocity relations. Am J Physiol Leg Content 221:1243–1249

    CAS  Google Scholar 

  • Gregersen H, Jorgensen C, Dall F, Jensen S (1992) Characteristics of spontaneous and evoked motility in the isolated perfused porcine duodenum. J Appl Physiol 73:9–19

    CAS  PubMed  Google Scholar 

  • Gregersen H, Hausken T, Yang J, Odegaard S, Gilja OH (2006) Mechanosensory properties in the human gastric antrum evaluated using B-mode ultrasonography during volume-controlled antral distension. Am J Physiol 290:G876–G882

    CAS  Google Scholar 

  • Grivel ML, Ruckebusch Y (1972) The propagation of segmental contractions along the small intestine. J Physiol 227:611–625

    PubMed Central  CAS  PubMed  Google Scholar 

  • Grovum WL, Williams VJ (1973) Rate of passage of digesta in sheep. 1. The effect of level of food intake on marker retention times along the small intestine and on apparent water absorption in the small and large intestines. Br J Nutr 29:13–21

    CAS  PubMed  Google Scholar 

  • Gwynne RM, Thomas EA, Goh SM, Sjovall H, Bornstein JC (2004) Segmentation induced by intraluminal fatty acid in isolated guinea-pig duodenum and jejunum. J Physiol 556:557–569

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hambleton BF (1914) Note upon the movements of the intestinal villi. Am J Physiol 34:446–447

    Google Scholar 

  • He B, Xu W, Santini PA, Polydorides AD, Chiu A, Estrella J, Shan M, Chadburn A, Villanacci V, Plebani A (2007) Intestinal Bacteria Trigger T Cell-Independent Immunoglobulin A2 Class Switching by Inducing Epithelial-Cell Secretion of the Cytokine APRIL. Immunity 26:812–826

    CAS  PubMed  Google Scholar 

  • Hennig GW, Costa M, Chen BN, Brookes SJH (1999) Quantitative analysis of peristalsis in the guinea-pig small intestine using spatio-temporal maps. J Physiol 517:575–590

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hosoyamada Y, Sakai T (2005) Structural and mechanical architecture of the intestinal villi and crypts in the rat intestine: integrative reevaluation from ultrastructural analysis. Anat Embryol (Berl) 210:1–12

    Google Scholar 

  • Hosoyamada Y, Sakai T (2007) Mechanical components of rat intestinal villi as revealed by ultrastructural analysis with special reference to the axial smooth muscle cells in the villi. Arch Histol Cytol 70:107–116

    PubMed  Google Scholar 

  • Huizinga JD, Lammers WJEP (2009) Gut peristalsis is governed by a multitude of cooperating mechanisms. Am J Physiol 296:G1–G8

    CAS  Google Scholar 

  • Huizinga J, McKay C, White E (2006) The many facets of intestinal peristalsis. Am J Physiol Gastrointest Liver Physiol 290:G1347–G1349

    CAS  PubMed  Google Scholar 

  • Huizinga JD, Chen J-H, Zhu YF, Pawelka A, McGinn RJ, Bardakjian BL, Parsons SP, Kunze WA, Wu RY, Bercik P (2014) The origin of segmentation motor activity in the intestine. Nat Commun 5:3326

    PubMed  Google Scholar 

  • Hurst AF (1931) Discussion on the function of the sympathetic nervous system. Proc R Soc Med 25:1597–1599

    Google Scholar 

  • Husebye E (1999) The patterns of small bowel motility: physiology and implications in organic disease and functional disorders. Neurogastroenterol Mot 11:141–162

    CAS  Google Scholar 

  • Janssen PWM, Lentle RG (2013) Spatiotemporal mapping techniques for quantifying gut motility. In: Cheng LK, Farrugia G (eds) New Advances in Gastrointestinal Motility Research. Springer, New York, pp 219–241

    Google Scholar 

  • Janssen PWM, Lentle RG, Asvarujanon P, Chambers P, Stafford KJ, Hemar Y (2007) Characterisation of flow and mixing regimes within the ileum of the brushtail possum using residence time distribution analysis with simultaneous spatio-temporal mapping. J Physiol 582:1239–1248

    PubMed Central  CAS  PubMed  Google Scholar 

  • Janssen P, Lentle R, Chambers P, Reynolds G, De Loubens C, Hulls C (2014) Spatiotemporal organization of standing postprandial contractions in the distal ileum of the anesthetized pig. Neurogastroenterol Mot 26(11):1651–1662

    CAS  Google Scholar 

  • Jeffrey B, Udaykumar HS, Schulze KS (2003) Flow fields generated by peristaltic reflex in isolated guinea pig ileum: impact of contraction depth and shoulders. Am J Physiol 285:G907–G918

    CAS  Google Scholar 

  • Johansson ME, Phillipson M, Petersson J, Velcich A, Holm L, Hansson GC (2008) The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci 105:15064–15069

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jumars PA (2000) Animal guts as ideal chemical reactors: maximizing absorption rates. Am Nat 155:527–543

    PubMed  Google Scholar 

  • Junqueira LC, Carneiro J (2005) Small intestine. Basic histology: text and atlas, 11th edn. McGraw-Hill, p 144

  • Kellow JE, Borody TJ, Phillips SF, Tucker RL, Haddad AC (1986) Human interdigestive motility: variations in patterns from esophagus to colon. Gastroenterology 91:386–395

    CAS  PubMed  Google Scholar 

  • Kerrigan D, Read N, Houghton L, Taylor M, Johnson A (1991) Disturbed gastroduodenal motility in patients with active and healed duodenal ulceration. Gastroenterology 100:892–900

    CAS  PubMed  Google Scholar 

  • Khosla R, Feely LC, Davis SS (1989) Gastrointestinal transit of non-disintegrating tablets in fed subjects. Int J Pharm 53:107–117

    CAS  Google Scholar 

  • King CE, Arnold L (1922) The activities of the intestinal mucosal motor mechanism. Am J Physiol 59:23

    Google Scholar 

  • Kong F, Singh RP (2009a) Digestion of raw and roasted almonds in simulated gastric environment. Food Biophys 4:365–377

    PubMed Central  Google Scholar 

  • Kong F, Singh RP (2009b) Modes of disintegration of solid foods in simulated gastric environment. Food Biophys 4:180–190

    PubMed Central  PubMed  Google Scholar 

  • Lammers WJEP (2000) Propagation of individual spikes as “patches” of activation in isolated feline duodenum. Am J Physiol 278:G297–G307

    CAS  Google Scholar 

  • Lammers WJEP (2005) Spatial and temporal coupling between slow waves and pendular contractions. Am J Physiol 289:G898–G903

    CAS  Google Scholar 

  • Lammers WJEP, Slack JR (2001) Of slow waves and spike patches. News Physiol Sci 16:138–144

    CAS  PubMed  Google Scholar 

  • Lammers WJEP, Stephen B, Slack JR (2002) Similarities and differences in the propagation of slow waves and peristaltic waves. Am J Physiol 283:G778–G786

    CAS  Google Scholar 

  • Larson M, Schulze K (2002) Appearance of peristaltic reflex in isolated guinea pig ileum in response to boluses of air, water, oil, and cellulose. Dig Dis Sci 47:2644–2650

    CAS  PubMed  Google Scholar 

  • Latham TW (1966) Fluid motions in a peristaltic pump. MS Thesis, Massachusetts Institute of Technology, Cambridge

  • Lentle RG, Janssen PWM (2008) Physical characteristics of digesta and their influence on flow and mixing in the mammalian intestine: a review. J Comp Physiol B 178:673–690

    CAS  PubMed  Google Scholar 

  • Lentle RG, Stafford KJ, Kennedy MS, Haslett SJ (2002) Rheological properties of digesta suggest little radial or axial mixing in the forestomach of the tammar (Macropus eugenii) and the parma (Macropus parma) wallaby. Physiol Biochem Zool 75:572–582

    PubMed  Google Scholar 

  • Lentle RG, Hemar Y, Hall CE, Stafford KJ (2005) Periodic fluid extrusion and models of digesta mixing in the intestine of a herbivore, the common brushtail possum (Trichosurus vulpecula). J Comp Physiol B 175:337–347

    PubMed  Google Scholar 

  • Lentle RG, Hemar Y, Hall CE (2006) Viscoelastic behaviour aids extrusion from and reabsorption of the liquid phase into the digesta plug: creep rheometry of hindgut digesta in the common brushtail possum Trichosurus vulpecula. J Comp Physiol B 176:469–475

    PubMed  Google Scholar 

  • Lentle RG, Janssen PWM, Asvarujanon P, Chambers P, Stafford KJ, Hemar Y (2007) High definition mapping of circular and longitudinal motility in the terminal ileum of the brushtail possum Trichosurus vulpecula with watery and viscous perfusates. J Comp Physiol B 177:543–556

    PubMed  Google Scholar 

  • Lentle RG, Janssen PWM, Asvarujanon P, Chambers P, Stafford KJ, Hemar Y (2008) High definition spatiotemporal mapping of contractile activity in the isolated proximal colon of the rabbit. J Comp Physiol B 178:257–268

    PubMed  Google Scholar 

  • Lentle RG, De Loubens C, Hulls C, Janssen PWM, Golding MD, Chambers JP (2012) A comparison of the organization of longitudinal and circular contractions during pendular and segmental activity in the duodenum of the rat and guinea pig. Neurogastroenterol Mot 24:686–e298

  • Lentle R, Janssen P, DeLoubens C, Lim Y, Hulls C, Chambers P (2013a) Mucosal microfolds augment mixing at the wall of the distal ileum of the brushtail possum. Neurogastroenterol Mot 25:881–e700

  • Lentle R, Reynolds G, Janssen P (2013b) Gastrointestinal tone; its genesis and contribution to the physical processes of digestion. Neurogastroenterol Mot 25(12):931–942

    CAS  Google Scholar 

  • Levenspiel O (1999) Chemical reaction engineering. Wiley, New York

    Google Scholar 

  • Levitt MD, Kneip JM, Levitt DG (1988) Use of laminar flow and unstirred layer models to predict intestinal absorption in the rat. J Clin Invest 81:1365–1369

    PubMed Central  CAS  PubMed  Google Scholar 

  • Levitt MD, Strocchi A, Levitt DG (1992) Human jejunal unstirred layer: evidence for extremely efficient luminal stirring. Am J Physiol 262:G593–G596

    CAS  PubMed  Google Scholar 

  • Lim YF (2014) Factors influencing mass transfer in the small intestine. IFNHH. Massey University, Palmerston North

    Google Scholar 

  • Lim Y, Williams M, Lentle R, Janssen P, Mansel B, Keen S, Chambers P (2013a) An exploration of the microrheological environment around the distal ileal villi and proximal colonic mucosa of the possum (Trichosurus vulpecula). J R Soc Interface 10

  • Lim YF, Williams MAK, Lentle RG, Janssen PWM, Mansel BW, Keen SAJ, Chambers P (2013b) An exploration of the microrheological environment around the distal ileal villi and proximal colonic mucosa of the possum (Trichosurus vulpecula). J R Soc Interface 10:20121008

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lim YF, Lentle RG, Janssen PW, Williams MA, de Loubens C, Mansel BW, Chambers P (2014) Determination of Villous Rigidity in the Distal Ileum of the Possum (Trichosurus vulpecula). PLoS One 9:e100140

    PubMed Central  PubMed  Google Scholar 

  • Lin HC (2006) Ileal brake: neuropeptidergic control of intestinal transit. Curr Gastroenterol Rep 8:367–373

    PubMed  Google Scholar 

  • Lin CC, Metters AT (2006) Hydrogels in controlled release formulations: network design and mathematical modeling. Adv Drug Deliv Rev 58:1379–1408

    CAS  PubMed  Google Scholar 

  • Lin HC, Wang L (1996) Jejunal brake. Dig Dis Sci 41:326–329

    CAS  PubMed  Google Scholar 

  • Love RJ, Lentle RG, Asvarujanon P, Hemar Y, Stafford KJ (2012) An expanded finite element model of the intestinal mixing of digesta. Food Digestion 4:26–35

    Google Scholar 

  • Macagno EO, Christensen JM (1981) Fluid mechanics of gastrointestinal flow. In: Johnson LR (ed) Physiology of the gastrointestinal tract. Raven, New York, pp 335–358

    Google Scholar 

  • Makhlouf GM, Murthy KS (2006) Cellular physiology of gastrointestinal smooth muscle. In: Johnson LR (ed) Physiology of the gastrointestinal tract. Raven Press, New York

    Google Scholar 

  • Malbert CH (2005) The ileocolonic sphincter. Neurogastroenterol Mot 17:41–49

    Google Scholar 

  • Mandalari G, Faulks RM, Rich GT, Lo Turco V, Picout DR, Lo Curto RB, Bisignano G, Dugo P, Dugo G, Waldron KW (2008) Release of protein, lipid, and vitamin E from almond seeds during digestion. J Agric Food Chem 56:3409–3416

    CAS  PubMed  Google Scholar 

  • McDonald D, Pethick D, Mullan B, Hampson D (2001) Increasing viscosity of the intestinal contents alters small intestinal structure and intestinal growth, and stimulates proliferation of enterotoxigenic Escherichia coli in newly-weaned pigs. Br J Nutr 86:487–498

    CAS  PubMed  Google Scholar 

  • McRorie J, Brown S, Cooper R, Givaruangsawat S, Scruggs D, Boring G (2000) Effects of dietary fibre and olestra on regional apparent viscosity and water content of digesta residue in porcine large intestine. Aliment Pharmacol Ther 14:471–477

    CAS  PubMed  Google Scholar 

  • Melville J, Macagno E, Christensen J (1975) Longitudinal contractions in the duodenum: their fluid-mechanical function. Am J Physiol 228:1887–1892

    CAS  PubMed  Google Scholar 

  • Meyer J, Gu Y, Elashoff J, Reedy T, Dressman J, Amidon G (1986) Effects of viscosity and fluid outflow on postcibal gastric emptying of solids. Tc 1:001

    Google Scholar 

  • Moulton DE, Goriely A (2011) Circumferential buckling instability of a growing cylindrical tube. J Mech Phys Solids 59:525–537

    Google Scholar 

  • Pallotta N, Cicala M, Frandina C, Corazziari E (1998) Antro-pyloric contractile patterns and transpyloric flow after meal ingestion in humans. Am J Gastroenterol 93:2513–2522

    CAS  PubMed  Google Scholar 

  • Pappenheimer JR (2001) Role of pre-epithelial ‘unstirred’ layers in absorption of nutrients from the human jejunum. J Membr Biol 179:185–204

    CAS  PubMed  Google Scholar 

  • Penry DL, Jumars PA (1987) Modeling animal guts as chemical reactors. Am Nat 129:69–96

    CAS  Google Scholar 

  • Pescatori M, Marsicano B, Mancinelli R, Salinari S, Bertuzzi A (1980) Control of peristalsis in the isolated rabbit colon. In: Christensen J (ed) Gastrointestinal motility. Raven Press, New York, pp 479–486

    Google Scholar 

  • Pohl P, Saparov SM, Antonenko YN (1998) The size of the unstirred layer as a function of the solute diffusion coefficient. Biophys J 75:1403–1409

    PubMed Central  CAS  PubMed  Google Scholar 

  • Puchelle E, Zahm J, Quemada D (1986) Rheological properties controlling mucociliary frequency and respiratory mucus transport. Biorheology 24:557–563

    Google Scholar 

  • Rao SS, Lu C, Schulze-Delrieu K (1996) Duodenum as a immediate brake to gastric outflow: a videofluoroscopic and manometric assessment. Gastroenterology 110:740–747

    CAS  PubMed  Google Scholar 

  • Robbe C, Capon C, Maes E, Rousset M, Zweibaum A, Zanetta JP, Michalski JC (2003) Evidence of regio-specific glycosylation in human intestinal mucins. J Biol Chem 278:46337–46348

    CAS  PubMed  Google Scholar 

  • Sarna S (1985) Cyclic motor activity; migrating motor complex: 1985. Gastroenterology 89:894

    CAS  PubMed  Google Scholar 

  • Sarna SK (2008) Are interstitial cells of Cajal plurifunction cells in the gut? Am J Physiol 294:G372–G390

    CAS  Google Scholar 

  • Sarna S, Condon RE, Cowles V (1983) Enteric mechanisms of initiation of migrating myoelectric complexes in dogs. Gastroenterology 84:814–822

    CAS  PubMed  Google Scholar 

  • Schemann M, Ehrlein HJ (1986) Postprandial patterns of canine jejunal motility and transit of luminal content. Gastroenterology 90:991–1000

    CAS  PubMed  Google Scholar 

  • Schulze KS, Clark E (2008) Ink dispersion by sequential contractions in isolated segments of guinea pig ileum and duodenum. Neurogastroenterol Mot 20:1317–1327

    CAS  Google Scholar 

  • Schulze-Delrieu K (1999) Visual parameters define the phase and the load of contractions in isolated guinea pig ileum. Am J Physiol 276:G1417–G1424

    CAS  PubMed  Google Scholar 

  • Seerden TC, Lammers W, De Winter BY, De Man JG, Pelckmans PA (2005) Spatiotemporal electrical and motility mapping of distension-induced propagating oscillations in the murine small intestine. Am J Physiol 289:G1043–G1951

    CAS  Google Scholar 

  • Shelat KJ, Nicholson T, Flanagan BM, Zhang D, Williams BA, Gidley MJ (2015) Rheology and microstructure characterisation of small intestinal digesta from pigs fed a red meat-containing Western-style diet. Food Hydrocolloids 44:300–308

    CAS  Google Scholar 

  • Sibley RM, Calow P (1986) Physiological ecology of animals: an evolutionary approach. Blackwell, Oxford

    Google Scholar 

  • Siegle ML, Ehrlein HJ (1988) Digestive motor patterns and transit of luminal contents in canine ileum. Am J Physiol 254:G552–G559

    CAS  PubMed  Google Scholar 

  • Slater PJB, Lester NP (1982) Minimising errors in splitting behaviour into bouts. Behaviour 79:153–161

    Google Scholar 

  • Spencer NJ, Hennig GW, Smith TK (2002) A rhythmic motor pattern activated by circumferential stretch in guinea-pig distal colon. J Physiol 545:629–648

    PubMed Central  CAS  PubMed  Google Scholar 

  • Spencer NJ, Hennig GW, Smith TK (2003) Stretch-activated neuronal pathways to longitudinal and circular muscle in guinea pig distal colon. Am J Physiol 284:G231–G241

    CAS  Google Scholar 

  • Spiller RC, Brown ML, Phillips SF (1987) Emptying of the terminal ileum in intact humans. Influence of meal residue and ileal motility. Gastroenterology 92:724–729

    CAS  PubMed  Google Scholar 

  • Steffe JF (1996) Rheological methods in food process engineering. Freeman Press, East Lancing

    Google Scholar 

  • Stevens C, Hume I (2004) Comparative physiology of the vertebrate digestive system. Cambridge University Press

  • Stevens RJ, Publicover NG, Smith TK (2000) Propagation and neural regulation of calcium waves in longitudinal and circular muscle layers of guinea pig small intestine. Gastroenterology 118:892–904

    CAS  PubMed  Google Scholar 

  • Takahashi T (2011) Flow behavior of digesta and the absorption of nutrients in the gastrointestine. J Nutr Sci Vitaminol (Tokyo) 57:265–273

    CAS  Google Scholar 

  • Takahashi T, Sakata T (2004) Viscous properties of pig cecal contents and the contribution of solid particles to viscosity. Nutrition 20:377–382

    PubMed  Google Scholar 

  • Tanaka S, Podolsky DK, Engel E, Guth PH, Kaunitz JD (1997) Human spasmolytic polypeptide decreases proton permeation through gastric mucus in vivo and in vitro. Am J Physiol Gastrointest Liver Physiol 272:G1473–G1480

    CAS  Google Scholar 

  • Thomson ABR, Dietschy JM (1984) The role of the unstirred water layer in intestinal permeation. In: Csaky TZ (ed) Pharmacology of intestinal permeation. Springer, New York, pp 165–269

    Google Scholar 

  • Thuneberg L, Peters S (2001) Toward a concept of stretch-coupling in smooth muscle. I. Anatomy of intestinal segmentation and sleeve contractions. Anat Rec 262:110–124

    CAS  PubMed  Google Scholar 

  • Tonini M, De Ponti F, Frigo G, Crema F (2002) Pharmacology of the enteric nervous system. Innervation of the gastrointestinal tract. Taylor & Francis, London, pp. 213–294

  • Trendelenburg P (1917) Physiologische und pharmakologische Versuche über die Dünndarmperistaltik. Naunyn-Schmiedeberg’s Arch Pharmacol 81:55–129

    Google Scholar 

  • Verdugo P (1990) Goblet cells secretion and mucogenesis. Annu Rev Physiol 52:157–176

    CAS  PubMed  Google Scholar 

  • Wang Y, Brasseur J, Banco G (2007) A multiscale lattice-Boltzmann model of macro-to-micro scale transport relevant to gut function. Am Phys Soc, 60th Meeting Div Fluid Dynamics, Salt Lake City

  • Wang Y, Brasseur J, Banco G (2009) Enhancement of absorption by micro-mixing induced by villi motion. Bull Am Phys Soc 54

  • Wang Y, Brasseur JG, Banco GG, Webb AG, Ailiani AC, Neuberger T (2010) Development of a lattice-Boltzmann method for multiscale transport and absorption with application to intestinal function. In: De S, Guilak G, Mofrad MRK (eds) Computational modeling in biomechanics. Springer, New York, pp 69–96

    Google Scholar 

  • Wilding IR, Hardy JG, Maccari M, Ravelli V, Davis SS (1991) Scintigraphic and pharmacokinetic assessment of a multiparticulate sustained release formulation of diltiazem. Int J Pharm 76:133–143

    CAS  Google Scholar 

  • Womack WA, Barrowman JA, Graham WH, Benoit JN, Kvietys PR, Granger DN (1987) Quantitative assessment of villous motility. Am J Physiol Gastrointest Liver Physiol 252:G250–G256

    CAS  Google Scholar 

  • Won KJ, Sanders KM, Ward SM (2005) Interstitial cells of Cajal mediate mechanosensitive responses in the stomach. Proc Natl Acad Sci USA 102:14913–14918

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wood JD, Perkins WE (1970) Mechanical interaction between longitudinal and circular axes of the small intestine. Am J Physiol 218:762–768

    CAS  PubMed  Google Scholar 

  • Yang W, Fung TC, Chian KS, Chong CK (2007) Instability of the two-layered thick-walled esophageal model under the external pressure and circular outer boundary condition. J Biomech 40:481–490

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Food, Nutrition and Human Health, Massey University, Private Bag 11222, Palmerston North, New Zealand

    R. G. Lentle

  2. UMR 782 Génie et Microbiologie des Procédés Alimentaires, INRA, AgroParisTech, CBAI, 78850, Thiverval-Grignon, France

    C. de Loubens

Authors
  1. R. G. Lentle
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. de Loubens
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to R. G. Lentle.

Additional information

Communicated by I. D. Hume.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lentle, R.G., de Loubens, C. A review of mixing and propulsion of chyme in the small intestine: fresh insights from new methods. J Comp Physiol B 185, 369–387 (2015). https://doi.org/10.1007/s00360-015-0889-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-015-0889-5

Keywords

Search

Navigation