Abstract
Eructation is composed of three independent phases: gas escape, upper barrier elimination, and gas transport phases. The gas escape phase is the gastro-LES inhibitory reflex that causes transient relaxation of the lower esophageal sphincter, which is activated by distension of stretch receptors of the proximal stomach. The upper barrier elimination phase is the transient relaxation of the upper esophageal sphincter along with airway protection. This phase is activated by stimulation of rapidly adapting mechanoreceptors of the esophageal mucosa. The gas transport phase is esophageal reverse peristalsis mediated by elementary reflexes, and it is theorized that this phase is activated by serosal rapidly adapting tension receptors. Alteration of the receptors which activate the upper barrier elimination phase of eructation by gastro-esophageal reflux of acid may in part contribute to the development of supra-esophageal reflux disease.
Similar content being viewed by others
References
Lang IM, Medda BK, Shaker R. Digestive and respiratory tract motor responses associated with eructation. Am J Physiol. 2013;304:G1044–53.
Patrikios J, Martin CJ, Dent J. Relationship of transient lower esophageal sphincter relaxation to postprandial gastroesophageal reflux and belching in dogs. Gastroenterology. 1986;90:545–51.
McNally EF, Kelly JE Jr, Ingelfinger FJ. Mechanism of belching: effects of gastric distension with air. Gastroenterology. 1964;46:254–9.
Strombeck DR, Griffen DW, Harold D. Eructation of gas through the gastroesophageal sphincter before and after limiting distension of the gastric cardias or infusion of beta-adrenergic amine in dogs. Am J Vet Res. 1989;50:751–3.
Franzi SJ, Martin CJ, Cox MR, Dent J. Response of canine lower esophageal sphincter to gastric distension. Am J Physiol. 1990;259:G380–5.
Penagini R, Carmagnola S, Cantu P, Alloca M, Bianchi PA. Mechanoreceptors of the proximal stomach: role in triggering transient lower esophageal sphincter relaxation. Gastroenterology. 2004;126:49–56.
Straathof JW, Ringers J, Lamers CB, Masclee AA. Provocation of transient lower esophageal sphincter relaxation by gastric distension with air. Am J. Gastreoenterol. 2001;96:2317–23.
Wyman JB, Dent J, Heddle R, Dodds WJ, Toouli J, Downton J. Control of belching by the lower esophageal sphincter. Gut. 1990;31:639–46.
Dougherty RW, Habel RE, Bond HE. Esophageal innervation and the eructation reflex in sleep. Am J Vet Res. 1958;19:115–28.
Kahrilas PJ, Dodds WJ, Dent J, Wyman JB, Hogan WJ, Arndorfer RC. Upper esophageal sphincter function during belching. Gastroenterology. 1986;91:133–40.
Daintree-Johnson H, Laws JW. The cardia in swallowing, eructation, and swallowing. Lancet. 1966;2:1268–73.
Monges H, Salducci J, Naudy B. Dissociation between the electrical activity of the diaphragmatic dome and crura muscular fibers during esophageal distension, vomiting and eructation. J Physiol. 1978;74:541–54.
Boyle JT, Altschuler SM, Nixon TE, Tuchman DN, Pack AI, Cohen S. Role of diaphragm in the genesis of lower esophageal pressure in the cat. Gastroenterololgy. 1985;88:723–30.
Mittal RK, Rochester DF, McCallum RW. Electrical and mechanical activity in the human lower esophageal sphincter during diaphragmatic contraction. J Clin Invest. 1988;81:1182–9.
Lang IM, Medda BK, Shaker R. Mechanisms of UES relaxation initiated by gastric air distension. Am J Physiol. 2014;307:G452–8.
Babaei A, Bhargava V, Korsapaai H, Zheng WH, Mittal RK. A unique longitudinal muscle contraction pattern associated with transient lower esophageal sphincter relaxation. Gastroenterology. 2008;134:1322–31.
Jiang Y, Bhargava V, Mittal RK. Mechanism of stretch-activated excitatory and inhibitory responses in the lower esophageal sphincter. Am J Physiol. 2009;297:G397–405.
Mittal RK, Karstens A, Leslie E, Babaaei A, Bhargava V. Ambulatory high-resolution manometry, lower esophageal sphincter lift, and transient lower esophageal sphincter relaxation. Neurogastroenterol Motil. 2012;24:40-e2.
Dogan I, Bhargava V, Liu J, Mittal RK. Axial stretch: a novel mechanism of the lower esophageal sphincter relaxation. Am J Physiol. 2007;292:G329–3344.
Jiang Y, Bhargava V, Lal HA, Mittal RK. Variability in the muscle composition of rat esophagus and neural pathway of lower esophageal sphincter relaxation. Am J Physiol. 2011;301:G1014–9.
Staunton E, Smid SD, Dent J, Blackshaw LA. Triggering of transient LES relaxation in ferrets: role of sympathetic pathways and effects of baclofen. Am J Physiol. 2000;279:G157–62.
Frisby CL, Mattson JP, Jensen JM, Lehmann A, Dent J, Blackshaw LA. Inhibition of transient lower esophageal sphincter relaxation and gastroesophageal reflux by metabotropic glutamate receptor ligands. Gastroenterology. 2005;129:995–1004.
Paterson WG, Rattan S, Goyal RK. Experimental induction of isolated lower esophageal sphincter relaxation in anesthetized opossums. J Clin Invest. 1986;77:1187–93.
Pandolfino JE, Zhang Q, Ghosh SK, Han A, Boniquit C, Kahrilas PJ. Transient lower esophageal sphincter relaxations and reflux: mechanistic analysis using concurrent fluoroscopy and high-resolution manometry. Gastroenterology. 2006;131:1725–33.
Martin CJ, Patrikios J, Dent J. Abolition of gas reflux and transient lower esophageal sphincter relaxation by vagal blockade in the dog. Gastroenterology. 1986;91:890–6.
Reynolds RPE. T Y El-Sharkawy, Diament NE. Lower esophageal sphincter function in the cats: role of central innervation assesses by transient vagal blockade. Am J Physiol. 1984;246:G666–74.
Young RL, Page AJ, Cooper NJ, Frisby CL, Blackshaw LA. Sensory and motor innervation of the crural diaphragm by the vagus nerves. Gastroenterology. 2010;138:1091–101.
Liu J, Yamamoto Y, Schirmer BD, Ross RA, Mittal RK. Evidence for a peripheral mechanism of esophagocrural diaphragm inhibitory reflex in cats. Am J Physiol. 2000;278:G281–8.
Dong H, Jiang Y, Dong J, Mittal RK. Inhibitory motor neurons of the myenteric plexus are mechanosensitive. Am J Physiol. 2015;308:C405–13.
Sang Q, Goyal RK. Lower esophageal sphincter relaxation and activation of medullary neurons by subdiaphragmatic vagal stimulation in the mouse. Gastroenterology. 2000;119:1600–9.
Niedringhaus M, Jackson PG, Pearson R, Shi M, Dretchen K, Gillis RA, Sahibzada N. Brainstem sites controlling the lower esophageal sphincter and crural diaphragm in the ferret: a neuroanatomical study. Autonom Neurosci: Basic and Clin. 2008;144:50–60.
Collman PI, Trembly L, Diamant NE. The central vagal efferent supply to the esophagus and lower esophageal sphincter. Gastroenterology. 1993;104:1430–8.
Bieger D, Hopkins DA. Viscerotropic representation of the upper alimentary tract in the medulla oblongata in the rate: the nucleus ambiguus. J Comp Neurol. 1987;262:546–62.
Altschuler SM, Bao X, Bieger D, Hopkins DA, Miselis RR. Viscerotropic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts. J Comp Neurol. 1989;283:248–68.
Niedringhaus M, Jackson PG, Evans SRT, Verbalis JG, Gillis RA. Dorsal motor nucleus of the vagus: a site for evoking simultaneous changes in crural diaphragm, lower esophageal sphincter pressure and fundus tone. Am J Physiol. 2008;294:R121–31.
Rossiter CD, Norman WP, Jain M, Hornby PM, Benjamin S, Gillis RA. Control of the lower esophageal sphincter pressure from two sites in dorsal motor nucleus of the vagus. Am J Physiol. 1990;259:G899–906.
Kalia M, Mesulum M-M. Brain stem projections of sensory and motor components of the vagus comoplex in the cat: I. The cervical vagus and nodose ganglion. J Comp Neurol. 1980;193:435–65.
Lehmann A, Antonsson M, Bremmer-Danilesen M, Flardh M, Hansson-Branden L, Karrberg L. Activation of GABAb receptor inhibits transient lower esophageal sphincter relaxations in dogs. Gastroenterology. 1999;117:1147–54.
Blackshaw LA, Smid SD, O’Donnell TA, Dent J. GABA(B) receptor-mediated effects on vagal pathways to the lower esophageal sphincter and heart. Br J Pharmacol. 2000;130:279–88.
Blackshaw LA, Staunton E, Lehmann A, Dent J. Inhibition of transient LES relaxations and reflux in ferrets by GABA receptor agonist. Am J Physiol. 1999;277:G867–74.
Lidums I, Lehmann A, Checklin H, Dent J, Holloway RH. Control of transient lower esophageal sphincter relaxations and reflux by the GABA(B) agonist baclofen in normal subjects. Gastroenterology. 2000;118:7–13.
Smid SD, Young RL, Cooper NJ, Blackshaw LA. GABABR expressed on vagal afferent neurons inhibit gastric mechanosensitivity in ferret proximal stomach. Am J Physiol. 2001;281:G1494–501.
Liu J, Pehlivanov N, Mittal RK. Baclofen blocks LES relaxation and crural diaphragm inhibition by esophageal and gastric distension in cats. Am J Physiol. 2002;283:G1276–81.
Jensen J, Lehmann A, Uverbant A, Carlsson A, Jerndal G, Nilsson K, Frisby C, Blackshaw LA, Mattson JP. Transient lower esophageal sphincter relaxations in dogs are inhibited by metabotropic glutamate receptor 5 antagonist. Eur J Pharmacol. 2005;519:154–7.
Brooks PA, Glaum SR, Miller RJ, Spyer KM. The actions of baclofen on neurons and synaptic transmission in the nucleus tractus solitarii of the rat in vitro. J Physiol. 1992;457:115–29.
Margeta-Mitrovic M, Mitrovic I, Riley RC, Jan LY, Basbaum AI. Immunohistochemical localization of GABA(B) receptors in the rat central nervous system. J Comp Neurol. 1999;405:299–321.
Smid SD, Blackshaw LA. Vagal neurotransmission to the ferret lower esophageal sphincter: inhibition via GABA(B) receptors. Br J Pharmacol. 2000;131:624–30.
Page AJ, Blackshaw LA. GABA(9B) receptors inhibit mechanosensitivity of primary afferent endings. J Neurosci. 1999;19:8597–602.
Partosoedarso ER, Young RL, Blackshaw LA. GABA(B) receptors on vagal afferent pathways: peripheral and central inhibition. Am J Physiol. 2001;280:G658–68.
Lehmann A, Blackshaw LA, Branen L, Carlsson A, Jensen J, Nygen E, Smid SD. Cannabinoid receptor agonism inhibits lower esophageal sphincter relaxation and reflux in dogs. Gastroenterology. 2002;123:1129–34.
Lehmann A, Branden L. Effects of antagonism of NMDA receptors on transient lower esophageal sphincter relaxation in the dog. Eur J Pharmacol. 2001;431:253–8.
Lang IM, Medda BK, Jadcherla S, Shaker R. The role of the superior laryngeal nerve in esophageal reflexes. Am J Physiol. 2012;302:G1445–57.
Pandolfino JE, Ghosh SK, Zhang Q, Han A, Kahrilas PJ. Upper esophageal function during transient lower oesophageal sphincter relaxation (tLOSR); it is mainly about microburps. Neurogastroenterol Motil. 2007;19:202–10.
Babaei A, Bhargava V, Mittal MK. Upper esophageal sphincter during transient lower esophageal sphincter relaxation: effects of reflux content and posture. Am J Physiol. 2010;298:G601–7.
Shaker R, Ren J, Kern M, Dodds WJ, Hogan WJ, Li Q. Mechanisms of airway protection and upper esophageal sphincter opening during belching. Am J Physiol. 1992;262:G621–8.
Szczesniak MM, Williams RBH, Brake HM, Maclean JC, Cole IE, Cook IJ. Upregulation of the esophago-UES relaxation response: a possible pathophysiological mechanisms in suspected reflux laryngitis. Neurogastroenterol Motil. 2010;22(381–386):e89.
Lang IM, Medda BK, Shaker R. Mechanisms of reflexes induced by esophageal distension. Am J Physiol. 2001;281:G1246–63.
Lang IM. Upper esophageal sphincter. In: Goyal RK, Shaker R, editors. Goyal and Shaker’s GI online. New York: Nature Publishing Group; 2006. doi:10.1038/gimo12.
Mu L, Sanders I. Neuromuscular organization of the human upper esophageal sphincter. Ann Otol Rhinol Laryngol. 2001;107:370–7.
Szczesniak MM, Williams RB, Cook IJ. Mechanisms of esophago-pharyngeal acid regurgitation in human subjects. PLoS ONE. 2011;6:e22630.
Harding R, Titchen DA. Chemosensitive vagal endings in the esophagus of the cat. J Physiol. 1975;247:52P–3P.
Clerc N, Mei N. Vagal mechanoreceptors located in the lower oesophageal sphincter of the cat. J Physiol. 1983;336:487–98.
Zagorodnyuk VP, Brookes SJH. Transduction sites of vagal mechanoreceptors in the guinea pig esophagus. J Neurosci. 2000;20:6249–55.
Page AJ, Blackshaw LA. An in vitro study of the properties of vagal afferent fibers innervating the ferret oesophagus and stomach. J Physiol. 1998;512:907–16.
Hwang K, Grossman MI, Ivy AC. Nervous control of the cervical portion of the esophagus. Am J Physiol. 1948;154:343–57.
Brok HAJ, Copper MP, Stroeve RJ, Ongerboer BW, Venker-van Haagen AJ, Schouwenburg PF. Evidence for recurrent laryngeal nerve contribution in motor innervation of the human cricopharyngeal muscle. Laryngoscope. 1999;109:705–8.
Lang IM, Medda BK, Shaker R. Differential activation of medullary vagal nuclei caused by stimulation of different esophageal mechanoreceptors. Brain Res. 2011;1368:119–33.
Kalia M, Mesulum M-M. Brain stem projections of sensory and motor components of the vagus complex in the cat: II. Laryngeal, trachea-bronchial, pulmonary, cardiac, and gastrointestinal branches. J Comp Neurol. 1980;193:467–508.
Holstege G, Graveland G, Bijker-Biemond C, Scuddeboom I. Location of motoneurons innervating soft palate, pharynx, and upper esophagus. Anatomical evidence for a possible swallowing center in the pontine reticular fomation. Brain Behav Evol. 1983;23:47–62.
Van Loveren H, Saunders MC, Casini P, Keller JT. Localization of motoneurons of the stylopharyngeus muscle in the cat. Neurosci Lett. 1985;58:251–5.
Yoshida T, Miyazaki T, Hirano M, Shin T, Totoki T, Kanaseki T. An investigation of the location of the motoneurons innervating the pharyngeal constrictors and the cervical esophagus muscles of cats using horderadish peroxidase method. J Otorhinolaryngol Soc Jpn. 1981;84:758–61.
Pasaro R, Lobera B, Gonzolez-Baron S, Delgado-Garcia JM. Cytoarchitectonic organization of laryngeal motoneurons within the nucleus ambiguous of the cat. Exp Neurol. 1983;82:623–34.
Borison HL. Area postrema: chemoreceptor circumventricular organ of the medulla oblongata. Prog Neurobiol. 1989;32:351–90.
Blondeau K, Boecxstaens V, Rommel N, Farre R, Depeyer S, Holvoet L, Boeckxstaens G, Tack JF. Baclofen improves symptoms and reduces postprandial flow events in patients with rumination and supragastric belching. Clin Gastroenterol Hepatol. 2012;10:379–84.
Cossentino MJ, Mann K, Armbruster SP, Lake JM, Maydonovitch C, Wong RK. Randomized clinical trial: the effects of baclofen in patients with gastro-esophageal reflux- a randomized perspective. Aliment Pharmacol Ther. 2012;35:1036–44.
Carr DH, Scott PC, Titchen DA. Manometric and electromyographic observations of the esophagus of sheep in eructation, regurgitation and swallowing. J Exp Physiol. 1983;68:661–74.
Laskiewitcz A. Vomiting and eructation with regard to the upper respiratory organs. Acta Oto-Laryngol. 1956;3:27–34.
Heywood LH, Wood AKW. Thoracic oesophageal motor activity during eructation in sheep. J Exp Phsyiol. 1985;70:603–13.
Stevens CE, Sellers AF. Pressure events in bovine esophagus and reticulum associated with eructation, deglutition and regurgitation. Am J Physiol. 1960;199:598–602.
Winship DH, Zboralske F, Weber WN, Soergel KH. Esophagus in rumination. Am J Physiol. 1964;207:1189–94.
Duncan DL. The effects of vagotomy and splanchnectomy on gastric motility is sheep. J Physiol. 1953;119:156–69.
Clerc N. Afferent innervation of the lower esophageal sphincter of the cat. J ANS. 1984;10:213–6.
Clerc N, Mei N. Thoracic esophageal mechanoreceptors connected with fibers following sympathetic pathways. Brain Res Bull. 1983;10:1–7.
Nichols TR, Cope TC, Abelow TA. Rapid spinal mechanisms of motor coordination. Exerc Sport Sci Rev. 1999;27:255–84.
Heywood LY, Wood AK. Retrograde oesophageal contractions in the dog. Quart J Exp Physiol. 1988;73:87–94.
Szczesniak MM, Fuentealba SE, Burnett A, Cook IJ. Differential relaxation and contractile responses of the human upper esophageal sphincter mediated by interplay of mucosal and deep mechanoreceptor activation. Am J Physiol. 2008;294:G982–8.
Kessing BF, Bredenoord AJ, Smout AJPM. Mechanism of gastric and supragastric belching: a study using concurrent high-resolution manometry and impedance monitoring. Neurogastroenterol Motil. 2012;24:e573–9.
Hemmink GJM, Bredenoord AJ, Weusten BLAM, Timmer R, Smout AJPM. Supragastric belching in patients with reflex symptoms. Am J Gastroenterol. 2009;104:1992–7.
Kessing BF, Govaert F, Masclee ADAM, Conchillo JM. Impedance measurements and high-resolution manometry help to better define rumination episodes. Scan J Gastroentrol. 2011;46:1310–5.
Bredenoord AJ, Weusten BLAM, Sifrim D, Timmer R, Smout AJPM. Aerophagia, gastric, and supragastric belching: a study using intraluminal electrical impedance monitoring. Gut. 2004;53:1561–5165.
Bredenoord AJ, Weusten BLAM, Timmer R, Smout AJPM. Air swallowing, belching, and reflux in patients with gastroesophageal reflux disease. Gastroenterology. 2006;101:1721–6.
Doty RW, Bosma JF. An electromyographic analysis of reflex deglutition. J Neurophysiol. 1956;19:44–60.
Lang IM, Dana N, Medda BK, Shaker R. Mechanism of airway protection during retching, vomiting, and swallowing. Am J Physiol. 2002;283:G529–36.
Hardemark Cedborg AI, Sundman E, Boden K, Hedstrom HW, Kuylenstierna R, Ekberg O, Erikson KI. Co-ordination of spontaneous swallowing with respiratory airflow and diaphragmatic and abdominal muscle activity in healthy adult humans. Exp Physiol. 2009;94:459–68.
Uysal H, Kizilay F, Unal A, Gungor HA, Ertekin C. The interaction between breathing and swallowing in healthy individuals. J Electromyogr Kinesiol. 2013;23:659–63.
Fernandez S, Aspirot A, Kerzner B, Froedlandaer J, Di Lorenzo C. Do some adolescents with rumination syndrome have “supragastric vomiting”? J Pediat Gastroenterol Hepatol Nutrition. 2010;50:103–5.
Titchen DA. Diaphragmatic and oesophageal activity in regurgitation in sheep: an electromyographic study. J Physiol. 1979;292:381–90.
Hopman WP, van Kouwen MC, Smout AJ. Does (supra)gastric belching trigger recurrent hiccups? W J Gastroenterol. 2010;16:1795–9.
Shaker R, Babaei A, Naini S. Prevention of esophagopharyngeal reflux by augmenting the upper esophageal sphincter pressure barrier. Laryngoscope. 2014;2014(124):2268–74.
Acknowledgments
This project was supported by NIH P01DK068051; Mechanisms of Upper Gut and Airway Interaction; Project 3: The Physiology of the Pharyngo-Esophageal Junction
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest
Dr. Lang has no conflicts of interest.
Rights and permissions
About this article
Cite this article
Lang, I.M. The Physiology of Eructation. Dysphagia 31, 121–133 (2016). https://doi.org/10.1007/s00455-015-9674-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00455-015-9674-6