Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Article
  • Published:
Dysphagia Aims and scope Submit manuscript

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.

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
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Enzmann DR, Harell GS, Zboralske FF. Upper esophageal responses to intraluminal distention in man. Gastroenterology. 1977;72:1292–8.

    Article  CAS  Google Scholar 

  2. 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.

    Article  CAS  Google Scholar 

  3. 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.

    Article  CAS  Google Scholar 

  4. 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.

    Article  CAS  Google Scholar 

  5. 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.

    Article  Google Scholar 

  6. 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.

    Article  Google Scholar 

  7. 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.

    Article  Google Scholar 

  8. 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.

    Article  Google Scholar 

  9. 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.

    Article  CAS  Google Scholar 

  10. Matsubara K, Kumai Y, Samejima Y, Yumoto E. Swallowing pressure and pressure profiles in young healthy adults. Laryngoscope. 2014;124:711–7.

    Article  Google Scholar 

  11. Hashmi S, Rao SS, Summers RW, Schulze K. Esophageal pressure topography, body position, and hiatal hernia. J Clin Gastroenterol. 2014;48:224–30.

    Article  Google Scholar 

  12. 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.

    Article  CAS  Google Scholar 

  13. 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.

    Article  CAS  Google Scholar 

  14. 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.

    Article  Google Scholar 

  15. 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.

    Article  Google Scholar 

  16. 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.

    Article  Google Scholar 

  17. 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.

    Article  Google Scholar 

  18. 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.

    Article  CAS  Google Scholar 

  19. 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.

    Article  CAS  Google Scholar 

  20. 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.

    Article  CAS  Google Scholar 

  21. Paterson WG. Esophageal peristalsis. GI Motil Online. 2006. https://doi.org/10.1038/gimo13.

    Article  Google Scholar 

  22. 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.

    Article  CAS  Google Scholar 

  23. 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.

    Article  CAS  Google Scholar 

  24. 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.

    Article  CAS  Google Scholar 

  25. 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.

    Article  CAS  Google Scholar 

  26. Creamer B, Schlegel J. Motor responses of the esophagus to distention. J Appl Physiol. 1957;10:498–504.

    Article  CAS  Google Scholar 

  27. 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.

    Article  CAS  Google Scholar 

  28. 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.

    Article  CAS  Google Scholar 

  29. 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.

    Article  CAS  Google Scholar 

  30. Sengupta JN, Kauvar D, Goyal RK. Characteristics of vagal esophageal tension-sensitive afferent fibers in the opossum. J Neurophysiol. 1989;61:1001–100.

    Article  CAS  Google Scholar 

  31. Lang IM, Medda BK, Shaker R. Mechanisms of reflexes induced by esophageal distension. Am J Physiol Gastrointest Liver Physiol. 2001;281:G1246–1263.

    Article  CAS  Google Scholar 

  32. Lang IM, Shaker R. Anatomy and physiology of the upper esophageal sphincter. Am J Med. 1997;103:50S–5S.

    Article  CAS  Google Scholar 

  33. 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.

    Article  CAS  Google Scholar 

  34. Steele CM, Miller AJ. Sensory input pathways and mechanisms in swallowing: a review. Dysphagia. 2010;25:323–33.

    Article  Google Scholar 

  35. Lang IM. The physiology of eructation. Dysphagia. 2016;31:121–33.

    Article  Google Scholar 

  36. Hwang K. Mechanism of transportation of the content of the esophagus. J Appl Physiol. 1954;6:781–96.

    Article  CAS  Google Scholar 

  37. 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.

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank Drs. Takanori Tsujimura and Makoto Inoue of the Division of Dysphagia Rehabilitation at Niigata University Graduate School of Medical and Dental Sciences for their valuable advice regarding this research.

Funding

This research was supported by a research grant-in-aid for Scientific Research C (no. 25862078 and 16K01477) from the Japanese Ministry of Education, Science, Culture, Sports, Science, and Technology.

Author information

Authors and Affiliations

  1. Department of Dentistry & Oral-Maxillofacial Surgery, School of Medicine, Fujita Health University, Toyoake, Japan

    Hiroshige Taniguchi & Koichiro Matsuo

  2. Department of Dentistry for the Disability and Oral Health, School of Dentistry, Asahi University, Mizuho, Japan

    Hiroshige Taniguchi

  3. Department of Rehabilitation Medicine I, School of Medicine, Fujita Health University, Toyoake, Japan

    Yoichiro Aoyagi & Eiichi Saitoh

  4. Faculty of Rehabilitation, Fujita Health University Hospital, Toyoake, Japan

    Sayuri Imaeda

  5. Faculty of Rehabilitation, Fujita Health University Bantane Hospital, Nagoya, Japan

    Makoto Hirumuta

Authors
  1. Hiroshige Taniguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yoichiro Aoyagi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Koichiro Matsuo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sayuri Imaeda
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Makoto Hirumuta
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Eiichi Saitoh
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Hiroshige Taniguchi, Yoichiro Aoyagi, Sayuri Imaeda, and Makoto Hirumuta made substantial contributions to the conception, design, acquisition, analysis, and interpretation of data. Hiroshige Taniguchi and Yoichiro Aoyagi participated in drafting the paper or revising it critically for important intellectual content. Yoichiro Aoyagi, Koichiro Matsuo, and Eiichi Saitoh provided final approval of the version to be submitted and any revised version.

Corresponding author

Correspondence to Yoichiro Aoyagi.

Ethics declarations

Conflict of interest

None.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Taniguchi, H., Aoyagi, Y., Matsuo, K. et al. Elicitation of the Swallowing Reflex by Esophageal Stimulation in Healthy Subjects: An Evaluation Using High-Resolution Manometry. Dysphagia 35, 657–666 (2020). https://doi.org/10.1007/s00455-019-10068-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00455-019-10068-z

Keywords

Search

Navigation