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Published in: Dysphagia 4/2020

01-08-2020 | Original Article

Elicitation of the Swallowing Reflex by Esophageal Stimulation in Healthy Subjects: An Evaluation Using High-Resolution Manometry

Authors: Hiroshige Taniguchi, Yoichiro Aoyagi, Koichiro Matsuo, Sayuri Imaeda, Makoto Hirumuta, Eiichi Saitoh

Published in: Dysphagia | Issue 4/2020

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Abstract

The purposes of this human study using high-resolution manometry were to verify whether the swallowing reflex can be evoked by intra-esophageal fluid injection and whether the reflex latency and manometric variables differ depending on the injected location, amount, or speed. Ten healthy individuals participated in this study. The tip of the intranasal catheter for injection was placed at 5 cm (upper), 10 cm (upper-middle), 15 cm (lower-middle), or 20 cm (lower) from the distal end of the upper esophageal sphincter (UES). An intra-esophageal injection of 3 mL or 10 mL of thickened water was administered and controlled at 3 mL/s or 10 mL/s. Latencies from the start of the injection to the onset of UES relaxation were compared regarding injection locations, amounts, and rates. Manometric variables of intra-esophageal injection and voluntary swallowing were compared. The latency became shorter when the upper region was injected. Latency after the 10-mL injection was shorter than that after the 3-mL injection (p < 0.01) when faster injection (10 mL/s) was used. Faster injection induced shorter latency (p < 0.01) when a larger volume (10 mL) was injected. Pre-maximum and post-maximum UES pressures during voluntary swallowing or during spontaneous swallowing when injecting the upper esophageal region were significantly higher than spontaneous swallowing at other regions (p < 0.01). Intra-esophageal fluid injection induces the swallowing reflex in humans. The most effective condition for inducing the swallowing reflex involved a larger fluid amount with a faster injection rate in the upper esophagus.
Literature
1.
go back to reference Enzmann DR, Harell GS, Zboralske FF. Upper esophageal responses to intraluminal distention in man. Gastroenterology. 1977;72:1292–8.CrossRef Enzmann DR, Harell GS, Zboralske FF. Upper esophageal responses to intraluminal distention in man. Gastroenterology. 1977;72:1292–8.CrossRef
2.
go back to reference Torrico S, Kern M, Aslam M, Narayanan S, Kannappan A, Ren J, Sui Z, Hofmann C, Shaker R. Upper esophageal sphincter function during gastroesophageal reflux events revisited. Am J Physiol Gastrointest Liver Physiol. 2000;279:G262–267.CrossRef Torrico S, Kern M, Aslam M, Narayanan S, Kannappan A, Ren J, Sui Z, Hofmann C, Shaker R. Upper esophageal sphincter function during gastroesophageal reflux events revisited. Am J Physiol Gastrointest Liver Physiol. 2000;279:G262–267.CrossRef
3.
go back to reference Gerhardt DC, Shuck TJ, Bordeaux RA, Winship DH (1978) Human upper esophageal sphincter. Response to volume, osmotic, and acid stimuli. Gastroenterology 75(2), 268–274.CrossRef Gerhardt DC, Shuck TJ, Bordeaux RA, Winship DH (1978) Human upper esophageal sphincter. Response to volume, osmotic, and acid stimuli. Gastroenterology 75(2), 268–274.CrossRef
4.
go back to reference Aslam M, Kern M, Shaker R. Modulation of oesophago-UOS contractile reflex: effect of proximal and distal esophageal distention and swallowing. Neurogastroenterol Motil. 2003;15:323–9.CrossRef Aslam M, Kern M, Shaker R. Modulation of oesophago-UOS contractile reflex: effect of proximal and distal esophageal distention and swallowing. Neurogastroenterol Motil. 2003;15:323–9.CrossRef
5.
go back to reference Babaei A, Dua K, Naini SR, Lee J, Katib O, Yan K, Hoffmann R, Shaker R. Response of the upper esophageal sphincter to esophageal distension is affected by posture, velocity, volume, and composition of the infusate. Gastroenterology. 2012;142(4):734–43.CrossRef Babaei A, Dua K, Naini SR, Lee J, Katib O, Yan K, Hoffmann R, Shaker R. Response of the upper esophageal sphincter to esophageal distension is affected by posture, velocity, volume, and composition of the infusate. Gastroenterology. 2012;142(4):734–43.CrossRef
6.
go back to reference Lang IM, Medda BK, Jadcherla SR, Shaker R. Characterization and mechanisms of the pharyngeal swallow activated by stimulation of the esophagus. Am J Physiol Gastrointest Liver Physiol. 2016;311(5):G827–G837837.CrossRef Lang IM, Medda BK, Jadcherla SR, Shaker R. Characterization and mechanisms of the pharyngeal swallow activated by stimulation of the esophagus. Am J Physiol Gastrointest Liver Physiol. 2016;311(5):G827–G837837.CrossRef
7.
go back to reference Taniguchi H, Aoyagi Y, Matsuo K, Nakagawa K, Saitoh E. Development of an esophageal stimulation method to elicit swallowing reflex in humans. J Oral Rehabil. 2017;45(3):211–5.CrossRef Taniguchi H, Aoyagi Y, Matsuo K, Nakagawa K, Saitoh E. Development of an esophageal stimulation method to elicit swallowing reflex in humans. J Oral Rehabil. 2017;45(3):211–5.CrossRef
8.
go back to reference Hoffman MR, Ciucci MR, Mielens JD, Jiang JJ, McCulloch TM. Pharyngeal swallow adaptations to bolus volume measured with high-resolution manometry. Laryngoscope. 2010;120:2367–73.CrossRef Hoffman MR, Ciucci MR, Mielens JD, Jiang JJ, McCulloch TM. Pharyngeal swallow adaptations to bolus volume measured with high-resolution manometry. Laryngoscope. 2010;120:2367–73.CrossRef
9.
go back to reference Lin T, Xu G, Dou Z, Lan Y, Yu F, Jiang L. Effect of bolus volume on pharyngeal swallowing assessed by high-resolution manometry. Physiol Behav. 2014;128:46–51.CrossRef Lin T, Xu G, Dou Z, Lan Y, Yu F, Jiang L. Effect of bolus volume on pharyngeal swallowing assessed by high-resolution manometry. Physiol Behav. 2014;128:46–51.CrossRef
10.
go back to reference Matsubara K, Kumai Y, Samejima Y, Yumoto E. Swallowing pressure and pressure profiles in young healthy adults. Laryngoscope. 2014;124:711–7.CrossRef Matsubara K, Kumai Y, Samejima Y, Yumoto E. Swallowing pressure and pressure profiles in young healthy adults. Laryngoscope. 2014;124:711–7.CrossRef
11.
go back to reference Hashmi S, Rao SS, Summers RW, Schulze K. Esophageal pressure topography, body position, and hiatal hernia. J Clin Gastroenterol. 2014;48:224–30.CrossRef Hashmi S, Rao SS, Summers RW, Schulze K. Esophageal pressure topography, body position, and hiatal hernia. J Clin Gastroenterol. 2014;48:224–30.CrossRef
12.
go back to reference Hasan Y, Go J, Hashmi SM, Valestin J, Schey R. Influence of everyday bolus consistencies in different body positions on high-resolution esophageal pressure topography (HREPT) parameters. Dis Esophagus. 2015;28:246–52.CrossRef Hasan Y, Go J, Hashmi SM, Valestin J, Schey R. Influence of everyday bolus consistencies in different body positions on high-resolution esophageal pressure topography (HREPT) parameters. Dis Esophagus. 2015;28:246–52.CrossRef
13.
go back to reference Babaei A, Bhargava V, Mittal RK. Upper esophageal sphincter during transient lower esophageal sphincter relaxation: effects of reflux content and posture. Am J Physiol Gastrointest Liver Physiol. 2010;298:G601–607.CrossRef Babaei A, Bhargava V, Mittal RK. Upper esophageal sphincter during transient lower esophageal sphincter relaxation: effects of reflux content and posture. Am J Physiol Gastrointest Liver Physiol. 2010;298:G601–607.CrossRef
14.
go back to reference Zhang XJ, Xiang XL, Tu L, Xie XP, Hou XH. The effect of position on esophageal structure and function determined with solid-state high-resolution manometry. J Dig Dis. 2015;16:350–6.CrossRef Zhang XJ, Xiang XL, Tu L, Xie XP, Hou XH. The effect of position on esophageal structure and function determined with solid-state high-resolution manometry. J Dig Dis. 2015;16:350–6.CrossRef
15.
go back to reference Bredenoord AJ, Fox M, Kahrilas PJ, Pandolfino JE, Schwizer W, Smout AJ. Chicago classification criteria of esophageal motility disorders defined in high resolution esophageal pressure topography. Neurogastroenterol Motil. 2012;24(Suppl 1):57–655.CrossRef Bredenoord AJ, Fox M, Kahrilas PJ, Pandolfino JE, Schwizer W, Smout AJ. Chicago classification criteria of esophageal motility disorders defined in high resolution esophageal pressure topography. Neurogastroenterol Motil. 2012;24(Suppl 1):57–655.CrossRef
16.
go back to reference McCulloch TM, Hoffman MR, Ciucci MR. High-resolution manometry of pharyngeal swallow pressure events associated with head turn and chin tuck. Ann Otol Rhinol Laryngol. 2010;119:369–76.CrossRef McCulloch TM, Hoffman MR, Ciucci MR. High-resolution manometry of pharyngeal swallow pressure events associated with head turn and chin tuck. Ann Otol Rhinol Laryngol. 2010;119:369–76.CrossRef
17.
go back to reference Hoffman MR, Mielens JD, Ciucci MR, Jones CA, Jiang JJ, McCulloch TM. High-resolution manometry of pharyngeal swallow pressure events associated with effortful swallow and the Mendelsohn maneuver. Dysphagia. 2012;27:418–26.CrossRef Hoffman MR, Mielens JD, Ciucci MR, Jones CA, Jiang JJ, McCulloch TM. High-resolution manometry of pharyngeal swallow pressure events associated with effortful swallow and the Mendelsohn maneuver. Dysphagia. 2012;27:418–26.CrossRef
18.
go back to reference Ghosh SK, Pandolfino JE, Rice J, Clarke JO, Kwiatek M, Kahrilas PJ. Impaired deglutitive EGJ relaxation in clinical esophageal manometry: a quantitative analysis of 400 patients and 75 controls. Am J Physiol Gastrointest Liver Physiol. 2007;293:G878–885.CrossRef Ghosh SK, Pandolfino JE, Rice J, Clarke JO, Kwiatek M, Kahrilas PJ. Impaired deglutitive EGJ relaxation in clinical esophageal manometry: a quantitative analysis of 400 patients and 75 controls. Am J Physiol Gastrointest Liver Physiol. 2007;293:G878–885.CrossRef
19.
go back to reference Pandolfino JE, Ghosh SK, Zhang Q, Jarosz A, Shah N, Kahrilas PJ. Quantifying EGJ morphology and relaxation with high-resolution manometry: a study of 75 asymptomatic volunteers. Am J Physiol Gastrointest Liver Physiol. 2006;290:G1033–1040.CrossRef Pandolfino JE, Ghosh SK, Zhang Q, Jarosz A, Shah N, Kahrilas PJ. Quantifying EGJ morphology and relaxation with high-resolution manometry: a study of 75 asymptomatic volunteers. Am J Physiol Gastrointest Liver Physiol. 2006;290:G1033–1040.CrossRef
20.
go back to reference Ghosh SK, Pandolfino JE, Zhang Q, Jarosz A, Shah N, Kahrilas PJ. Quantifying esophageal peristalsis with high-resolution manometry: a study of 75 asymptomatic volunteers. Am J Physiol Gastrointest Liver Physiol. 2006;290:G988–997.CrossRef Ghosh SK, Pandolfino JE, Zhang Q, Jarosz A, Shah N, Kahrilas PJ. Quantifying esophageal peristalsis with high-resolution manometry: a study of 75 asymptomatic volunteers. Am J Physiol Gastrointest Liver Physiol. 2006;290:G988–997.CrossRef
22.
go back to reference Kahrilas PJ, Bredenoord AJ, Fox M, Gyawali CP, Roman S, Smout AJ, Pandolfino JE. The Chicago Classification of esophageal motility disorders. Neurogastroenterol Motil. 2015;27:160–74.CrossRef Kahrilas PJ, Bredenoord AJ, Fox M, Gyawali CP, Roman S, Smout AJ, Pandolfino JE. The Chicago Classification of esophageal motility disorders. Neurogastroenterol Motil. 2015;27:160–74.CrossRef
23.
go back to reference Yahagi R, Okuda-Akabane K, Fukami H, Matsumoto N, Kitada Y. Facilitation of voluntary swallowing by chemical stimulation of the posterior tongue and pharyngeal region in humans. Neurosci Lett. 2008;448:139–42.CrossRef Yahagi R, Okuda-Akabane K, Fukami H, Matsumoto N, Kitada Y. Facilitation of voluntary swallowing by chemical stimulation of the posterior tongue and pharyngeal region in humans. Neurosci Lett. 2008;448:139–42.CrossRef
24.
go back to reference Kijima M, Isono S, Nishino T. Coordination of swallowing and phases of respiration during added respiratory loads in awake subjects. Am J Respir Crit Care Med. 1999;159:1898–902.CrossRef Kijima M, Isono S, Nishino T. Coordination of swallowing and phases of respiration during added respiratory loads in awake subjects. Am J Respir Crit Care Med. 1999;159:1898–902.CrossRef
25.
go back to reference Jung KW, Jung HY, Myung SJ, Kim SO, Lee J, Yoon IJ, Seo SY, Lee JH, Kim DH, Choi KD, Song HJ, Lee GH, Murray JA, Romero Y, Kim JH. The effect of age on the key parameters in the Chicago classification: a study using high-resolution esophageal manometry in asymptomatic normal individuals. Neurogastroenterol Motil. 2015;27:246–57.CrossRef Jung KW, Jung HY, Myung SJ, Kim SO, Lee J, Yoon IJ, Seo SY, Lee JH, Kim DH, Choi KD, Song HJ, Lee GH, Murray JA, Romero Y, Kim JH. The effect of age on the key parameters in the Chicago classification: a study using high-resolution esophageal manometry in asymptomatic normal individuals. Neurogastroenterol Motil. 2015;27:246–57.CrossRef
26.
go back to reference Creamer B, Schlegel J. Motor responses of the esophagus to distention. J Appl Physiol. 1957;10:498–504.CrossRef Creamer B, Schlegel J. Motor responses of the esophagus to distention. J Appl Physiol. 1957;10:498–504.CrossRef
27.
go back to reference Woodland P, Aktar R, Mthunzi E, Lee C, Peiris M, Preston SL, Blackshaw LA, Sifrim D. Distinct afferent innervation patterns within the human proximal and distal esophageal mucosa. Am J Physiol Gastrointest Liver Physiol. 2015;308:G525–531.CrossRef Woodland P, Aktar R, Mthunzi E, Lee C, Peiris M, Preston SL, Blackshaw LA, Sifrim D. Distinct afferent innervation patterns within the human proximal and distal esophageal mucosa. Am J Physiol Gastrointest Liver Physiol. 2015;308:G525–531.CrossRef
28.
go back to reference Tsujimura T, Udemgba C, Inoue M, Canning BJ. Laryngeal and tracheal afferent nerve stimulation evokes swallowing in anaesthetized guinea pigs. J Physiol. 2013;591:4667–799.CrossRef Tsujimura T, Udemgba C, Inoue M, Canning BJ. Laryngeal and tracheal afferent nerve stimulation evokes swallowing in anaesthetized guinea pigs. J Physiol. 2013;591:4667–799.CrossRef
29.
go back to reference 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 Gastrointest Liver Physiol. 2008;294:G982–988.CrossRef 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 Gastrointest Liver Physiol. 2008;294:G982–988.CrossRef
30.
go back to reference Sengupta JN, Kauvar D, Goyal RK. Characteristics of vagal esophageal tension-sensitive afferent fibers in the opossum. J Neurophysiol. 1989;61:1001–100.CrossRef Sengupta JN, Kauvar D, Goyal RK. Characteristics of vagal esophageal tension-sensitive afferent fibers in the opossum. J Neurophysiol. 1989;61:1001–100.CrossRef
31.
go back to reference Lang IM, Medda BK, Shaker R. Mechanisms of reflexes induced by esophageal distension. Am J Physiol Gastrointest Liver Physiol. 2001;281:G1246–1263.CrossRef Lang IM, Medda BK, Shaker R. Mechanisms of reflexes induced by esophageal distension. Am J Physiol Gastrointest Liver Physiol. 2001;281:G1246–1263.CrossRef
32.
go back to reference Lang IM, Shaker R. Anatomy and physiology of the upper esophageal sphincter. Am J Med. 1997;103:50S–5S.CrossRef Lang IM, Shaker R. Anatomy and physiology of the upper esophageal sphincter. Am J Med. 1997;103:50S–5S.CrossRef
33.
go back to reference Lang IM, Medda BK, Jadcherla S, Shaker R. The role of the superior laryngeal nerve in esophageal reflexes. Am J Physiol Gastrointest Liver Physiol. 2012;302:G1445–1457.CrossRef Lang IM, Medda BK, Jadcherla S, Shaker R. The role of the superior laryngeal nerve in esophageal reflexes. Am J Physiol Gastrointest Liver Physiol. 2012;302:G1445–1457.CrossRef
34.
go back to reference Steele CM, Miller AJ. Sensory input pathways and mechanisms in swallowing: a review. Dysphagia. 2010;25:323–33.CrossRef Steele CM, Miller AJ. Sensory input pathways and mechanisms in swallowing: a review. Dysphagia. 2010;25:323–33.CrossRef
35.
36.
go back to reference Hwang K. Mechanism of transportation of the content of the esophagus. J Appl Physiol. 1954;6:781–96.CrossRef Hwang K. Mechanism of transportation of the content of the esophagus. J Appl Physiol. 1954;6:781–96.CrossRef
37.
go back to reference He M, Ohrui T, Azumi M, Ida S, Sasaki H. Depressed involuntary swallowing and risk of pneumonia. J Am Geriatr Soc. 2004;52:1032–3.CrossRef He M, Ohrui T, Azumi M, Ida S, Sasaki H. Depressed involuntary swallowing and risk of pneumonia. J Am Geriatr Soc. 2004;52:1032–3.CrossRef
Metadata
Title
Elicitation of the Swallowing Reflex by Esophageal Stimulation in Healthy Subjects: An Evaluation Using High-Resolution Manometry
Authors
Hiroshige Taniguchi
Yoichiro Aoyagi
Koichiro Matsuo
Sayuri Imaeda
Makoto Hirumuta
Eiichi Saitoh
Publication date
01-08-2020
Publisher
Springer US
Published in
Dysphagia / Issue 4/2020
Print ISSN: 0179-051X
Electronic ISSN: 1432-0460
DOI
https://doi.org/10.1007/s00455-019-10068-z

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