Advertisement

Dysphagia

, Volume 31, Issue 2, pp 121–133 | Cite as

The Physiology of Eructation

  • Ivan M. Lang
Review Paper

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.

Keywords

Eructation Belching Esophago-pharyngeal reflux (EPR) Esophageal reverse peristalsis Transient relaxation of the lower esophageal sphincter (TLESR) Transient relaxation of the upper esophageal sphincter (TUESR) Supra-esophageal reflux disease (SERD) 

Notes

Acknowledgments

This project was supported by NIH P01DK068051; Mechanisms of Upper Gut and Airway Interaction; Project 3: The Physiology of the Pharyngo-Esophageal Junction

Compliance with Ethical Standard

Conflicts of interest

Dr. Lang has no conflicts of interest.

References

  1. 1.
    Lang IM, Medda BK, Shaker R. Digestive and respiratory tract motor responses associated with eructation. Am J Physiol. 2013;304:G1044–53.Google Scholar
  2. 2.
    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.PubMedGoogle Scholar
  3. 3.
    McNally EF, Kelly JE Jr, Ingelfinger FJ. Mechanism of belching: effects of gastric distension with air. Gastroenterology. 1964;46:254–9.PubMedGoogle Scholar
  4. 4.
    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.PubMedGoogle Scholar
  5. 5.
    Franzi SJ, Martin CJ, Cox MR, Dent J. Response of canine lower esophageal sphincter to gastric distension. Am J Physiol. 1990;259:G380–5.PubMedGoogle Scholar
  6. 6.
    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.CrossRefPubMedGoogle Scholar
  7. 7.
    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.CrossRefGoogle Scholar
  8. 8.
    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.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Dougherty RW, Habel RE, Bond HE. Esophageal innervation and the eructation reflex in sleep. Am J Vet Res. 1958;19:115–28.PubMedGoogle Scholar
  10. 10.
    Kahrilas PJ, Dodds WJ, Dent J, Wyman JB, Hogan WJ, Arndorfer RC. Upper esophageal sphincter function during belching. Gastroenterology. 1986;91:133–40.PubMedGoogle Scholar
  11. 11.
    Daintree-Johnson H, Laws JW. The cardia in swallowing, eructation, and swallowing. Lancet. 1966;2:1268–73.CrossRefGoogle Scholar
  12. 12.
    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.Google Scholar
  13. 13.
    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.Google Scholar
  14. 14.
    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.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Lang IM, Medda BK, Shaker R. Mechanisms of UES relaxation initiated by gastric air distension. Am J Physiol. 2014;307:G452–8.Google Scholar
  16. 16.
    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.CrossRefPubMedGoogle Scholar
  17. 17.
    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.CrossRefGoogle Scholar
  18. 18.
    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.CrossRefPubMedCentralGoogle Scholar
  19. 19.
    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.Google Scholar
  20. 20.
    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.Google Scholar
  21. 21.
    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.Google Scholar
  22. 22.
    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.CrossRefPubMedGoogle Scholar
  23. 23.
    Paterson WG, Rattan S, Goyal RK. Experimental induction of isolated lower esophageal sphincter relaxation in anesthetized opossums. J Clin Invest. 1986;77:1187–93.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    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.CrossRefPubMedGoogle Scholar
  25. 25.
    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.PubMedGoogle Scholar
  26. 26.
    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.PubMedGoogle Scholar
  27. 27.
    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.CrossRefPubMedGoogle Scholar
  28. 28.
    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.Google Scholar
  29. 29.
    Dong H, Jiang Y, Dong J, Mittal RK. Inhibitory motor neurons of the myenteric plexus are mechanosensitive. Am J Physiol. 2015;308:C405–13.CrossRefGoogle Scholar
  30. 30.
    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.CrossRefPubMedGoogle Scholar
  31. 31.
    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.CrossRefGoogle Scholar
  32. 32.
    Collman PI, Trembly L, Diamant NE. The central vagal efferent supply to the esophagus and lower esophageal sphincter. Gastroenterology. 1993;104:1430–8.PubMedGoogle Scholar
  33. 33.
    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.CrossRefPubMedGoogle Scholar
  34. 34.
    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.CrossRefPubMedGoogle Scholar
  35. 35.
    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.Google Scholar
  36. 36.
    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.PubMedGoogle Scholar
  37. 37.
    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.CrossRefPubMedGoogle Scholar
  38. 38.
    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.CrossRefPubMedGoogle Scholar
  39. 39.
    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.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    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.PubMedGoogle Scholar
  41. 41.
    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.CrossRefPubMedGoogle Scholar
  42. 42.
    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.Google Scholar
  43. 43.
    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.Google Scholar
  44. 44.
    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.CrossRefPubMedGoogle Scholar
  45. 45.
    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.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    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.CrossRefPubMedGoogle Scholar
  47. 47.
    Smid SD, Blackshaw LA. Vagal neurotransmission to the ferret lower esophageal sphincter: inhibition via GABA(B) receptors. Br J Pharmacol. 2000;131:624–30.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Page AJ, Blackshaw LA. GABA(9B) receptors inhibit mechanosensitivity of primary afferent endings. J Neurosci. 1999;19:8597–602.PubMedGoogle Scholar
  49. 49.
    Partosoedarso ER, Young RL, Blackshaw LA. GABA(B) receptors on vagal afferent pathways: peripheral and central inhibition. Am J Physiol. 2001;280:G658–68.Google Scholar
  50. 50.
    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.CrossRefPubMedGoogle Scholar
  51. 51.
    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.CrossRefPubMedGoogle Scholar
  52. 52.
    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.Google Scholar
  53. 53.
    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.CrossRefGoogle Scholar
  54. 54.
    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.Google Scholar
  55. 55.
    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.PubMedGoogle Scholar
  56. 56.
    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.Google Scholar
  57. 57.
    Lang IM, Medda BK, Shaker R. Mechanisms of reflexes induced by esophageal distension. Am J Physiol. 2001;281:G1246–63.Google Scholar
  58. 58.
    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.Google Scholar
  59. 59.
    Mu L, Sanders I. Neuromuscular organization of the human upper esophageal sphincter. Ann Otol Rhinol Laryngol. 2001;107:370–7.CrossRefGoogle Scholar
  60. 60.
    Szczesniak MM, Williams RB, Cook IJ. Mechanisms of esophago-pharyngeal acid regurgitation in human subjects. PLoS ONE. 2011;6:e22630.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Harding R, Titchen DA. Chemosensitive vagal endings in the esophagus of the cat. J Physiol. 1975;247:52P–3P.PubMedGoogle Scholar
  62. 62.
    Clerc N, Mei N. Vagal mechanoreceptors located in the lower oesophageal sphincter of the cat. J Physiol. 1983;336:487–98.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Zagorodnyuk VP, Brookes SJH. Transduction sites of vagal mechanoreceptors in the guinea pig esophagus. J Neurosci. 2000;20:6249–55.PubMedGoogle Scholar
  64. 64.
    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.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Hwang K, Grossman MI, Ivy AC. Nervous control of the cervical portion of the esophagus. Am J Physiol. 1948;154:343–57.PubMedGoogle Scholar
  66. 66.
    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.CrossRefPubMedGoogle Scholar
  67. 67.
    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.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    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.CrossRefPubMedGoogle Scholar
  69. 69.
    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.CrossRefPubMedGoogle Scholar
  70. 70.
    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.CrossRefPubMedGoogle Scholar
  71. 71.
    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.Google Scholar
  72. 72.
    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.CrossRefPubMedGoogle Scholar
  73. 73.
    Borison HL. Area postrema: chemoreceptor circumventricular organ of the medulla oblongata. Prog Neurobiol. 1989;32:351–90.CrossRefPubMedGoogle Scholar
  74. 74.
    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.CrossRefPubMedGoogle Scholar
  75. 75.
    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.PubMedGoogle Scholar
  76. 76.
    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.CrossRefGoogle Scholar
  77. 77.
    Laskiewitcz A. Vomiting and eructation with regard to the upper respiratory organs. Acta Oto-Laryngol. 1956;3:27–34.CrossRefGoogle Scholar
  78. 78.
    Heywood LH, Wood AKW. Thoracic oesophageal motor activity during eructation in sheep. J Exp Phsyiol. 1985;70:603–13.CrossRefGoogle Scholar
  79. 79.
    Stevens CE, Sellers AF. Pressure events in bovine esophagus and reticulum associated with eructation, deglutition and regurgitation. Am J Physiol. 1960;199:598–602.Google Scholar
  80. 80.
    Winship DH, Zboralske F, Weber WN, Soergel KH. Esophagus in rumination. Am J Physiol. 1964;207:1189–94.PubMedGoogle Scholar
  81. 81.
    Duncan DL. The effects of vagotomy and splanchnectomy on gastric motility is sheep. J Physiol. 1953;119:156–69.CrossRefGoogle Scholar
  82. 82.
    Clerc N. Afferent innervation of the lower esophageal sphincter of the cat. J ANS. 1984;10:213–6.Google Scholar
  83. 83.
    Clerc N, Mei N. Thoracic esophageal mechanoreceptors connected with fibers following sympathetic pathways. Brain Res Bull. 1983;10:1–7.CrossRefPubMedGoogle Scholar
  84. 84.
    Nichols TR, Cope TC, Abelow TA. Rapid spinal mechanisms of motor coordination. Exerc Sport Sci Rev. 1999;27:255–84.CrossRefPubMedGoogle Scholar
  85. 85.
    Heywood LY, Wood AK. Retrograde oesophageal contractions in the dog. Quart J Exp Physiol. 1988;73:87–94.CrossRefGoogle Scholar
  86. 86.
    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.Google Scholar
  87. 87.
    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.CrossRefPubMedGoogle Scholar
  88. 88.
    Hemmink GJM, Bredenoord AJ, Weusten BLAM, Timmer R, Smout AJPM. Supragastric belching in patients with reflex symptoms. Am J Gastroenterol. 2009;104:1992–7.CrossRefPubMedGoogle Scholar
  89. 89.
    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.CrossRefGoogle Scholar
  90. 90.
    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.CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Bredenoord AJ, Weusten BLAM, Timmer R, Smout AJPM. Air swallowing, belching, and reflux in patients with gastroesophageal reflux disease. Gastroenterology. 2006;101:1721–6.Google Scholar
  92. 92.
    Doty RW, Bosma JF. An electromyographic analysis of reflex deglutition. J Neurophysiol. 1956;19:44–60.PubMedGoogle Scholar
  93. 93.
    Lang IM, Dana N, Medda BK, Shaker R. Mechanism of airway protection during retching, vomiting, and swallowing. Am J Physiol. 2002;283:G529–36.Google Scholar
  94. 94.
    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.CrossRefPubMedGoogle Scholar
  95. 95.
    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.CrossRefPubMedGoogle Scholar
  96. 96.
    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.CrossRefGoogle Scholar
  97. 97.
    Titchen DA. Diaphragmatic and oesophageal activity in regurgitation in sheep: an electromyographic study. J Physiol. 1979;292:381–90.CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Hopman WP, van Kouwen MC, Smout AJ. Does (supra)gastric belching trigger recurrent hiccups? W J Gastroenterol. 2010;16:1795–9.CrossRefGoogle Scholar
  99. 99.
    Shaker R, Babaei A, Naini S. Prevention of esophagopharyngeal reflux by augmenting the upper esophageal sphincter pressure barrier. Laryngoscope. 2014;2014(124):2268–74.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Division of Gastroenterology and Hepatology, Department of MedicineMedical College of WisconsinMilwaukeeUSA
  2. 2.Dysphagia Institute Animal Research Laboratory, MACC Fund Research CenterMedical College of WisconsinMilwaukeeUSA

Personalised recommendations