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Disruption of the Obligatory Swallowing Sequence in Patients with Wallenberg Syndrome

  • Mari NakaoEmail author
  • Fumiko Oshima
  • Yutaka Maeno
  • Shinich Izumi
Original Article


Although the sequence of events involved in swallowing varies among healthy adults, healthy adults demonstrate some consistent patterns, including opening of the upper esophageal sphincter (UES) prior to maximum laryngeal elevation (LE). Previous animal studies suggested that swallowing is regulated by a neuronal network in the medulla, and lateral medullary infarction, or Wallenberg syndrome, frequently causes dysphagia. This retrospective, observational, multicenter study aimed to determine if the sequence of swallowing events was disturbed in patients with Wallenberg syndrome compared with previously published reference data for healthy adults. The study subjects included 35 patients with Wallenberg syndrome admitted to three hospitals in Japan from 1/4/2009 to 31/3/2017. Sixteen timing events, including maximum LE and UES opening, and the intervals between events were measured. If the sequence of events was the same as in healthy adults, the interval value was positive, and if the sequence of events was opposite to that in healthy adults, the value was negative. The median interval from UES opening to maximum LE was − 0.02 s (range − 0.80 to 0.89, 95% CI − 0.14 to 0.10). About half of the Wallenberg cases showed negative values indicating that the sequence was reversed. These results suggest that lateral medullary infarction impairs the sequence of swallowing events.


Stroke Dysphagia Deglutition Videofluorography Sequence Deglutition disorders Wallenberg syndrome Swallowing disorder 



The authors would like to thank Prof. Masako Kurachi for advice on defining timing-related events, and Prof. Yoshimi Suzukamo for advice on methods related to statistical analysis. Part of this work was presented as a poster at the 2018 Dysphagia Research Society Conference (DRS), Baltimore, USA. We also thank Prof. Catriona M. Steele and Susan Furness, PhD, from Edanz Group ( for editing a draft of this manuscript.

Compliance with Ethical Standards

Conflict of interest

Mari Nakao declares that she has no conflict of interest. Fumiko Oshima declares that she has no conflict of interest. Yutaka Maeno declares that he has no conflict of interest. Shinichi Izumi declares that he has no conflict of interest.

Ethical Approval

This study was approved by the Institutional Review Board of Tohoku University School of Medicine (ID 2016-1-857) with the 1964 Helsinki Declaration and its later amendments. This article does not contain any studies with human participants, materials acquired from human body parts, or animals performed by any of the authors. Information including ethical standards and contact information on this study was disclosed on the web site of each facility that participated in this study.

Supplementary material

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Supplementary material 1 (DOCX 24 kb)
455_2018_9970_MOESM2_ESM.docx (20 kb)
Supplementary material 2 (DOCX 20 kb)


  1. 1.
    Jean A. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev. 2001;81:929–69.CrossRefGoogle Scholar
  2. 2.
    Umezaki T. Enge no Shinkei Kikou (Neural system of swallowing). Koujinou kinou kennkyu. 2007;27:215–21.Google Scholar
  3. 3.
    Sugimoto T, Umezaki T, Takagi S, Narikawa K, Shin T. Crossing inputs of the superior laryngeal nerve afferents to medullary swallowing-related neurons in the cat. Neurosci Res. 1998;30:235–45.CrossRefGoogle Scholar
  4. 4.
    Mendell DA, Logemann JA. Temporal sequence of swallow events during the oropharyngeal swallow. J Speech Lang Hear Res. 2007;50:1256–71.CrossRefGoogle Scholar
  5. 5.
    Kendall KA, Leonard RJ, McKenzie SW. Sequence variability during hypopharyngeal bolus transit. Dysphagia. 2003;18:85–91.CrossRefGoogle Scholar
  6. 6.
    Molfenter SM, Leigh C, Steele CM. Event sequence variability in healthy swallowing: building on previous findings. Dysphagia. 2014;29:234–42.CrossRefGoogle Scholar
  7. 7.
    Herzberg EG, Lazarus CL, Steele CM, Molfenter SM. Swallow event sequencing: comparing healthy older and younger adults. Dysphagia. 2018 (in print).Google Scholar
  8. 8.
    Miller AJ. Deglutition. Physiol Rev. 1982;62:129–84.CrossRefGoogle Scholar
  9. 9.
    Umezaki T, Matsuse T, Shin T. Medullary swallowing-related neurons in the anesthetized cat. Neuro Rep. 1998;9:1793–8.Google Scholar
  10. 10.
    Katz PS. Evolution of central pattern generators and rhythmic behaviours. Philos Trans R Soc Lond B. 2016;371:20150057.CrossRefGoogle Scholar
  11. 11.
    Ishibashi A, Fujishima I. Lesion of the nucleus solitarius leads to impaired laryngeal sensation in bulbar palsy patients. J Stroke Cerebrovasc Dis. 2012;21:174–80.CrossRefGoogle Scholar
  12. 12.
    Aydogdu I, Ertekin C, Tarlaci S, Turman B, Kiylioglu N, Secil Y. Dysphagia in lateral medullary infarction (Wallenberg’s syndrome): an acute disconnection syndrome in premotor neurons related to swallowing activity? Stroke. 2001;32:2081–7.CrossRefGoogle Scholar
  13. 13.
    Norrving B, Cronqvist S. Lateral medullary infarction: prognosis in an unselected series. Neurology. 1991;41:244–8.CrossRefGoogle Scholar
  14. 14.
    Sacco RL, Freddo L, Bello JA, Odel JG, Onesti ST, Mohr JP. Wallenberg’s lateral medullary syndrome. Clinical-magnetic resonance imaging correlations. Arch Neurol. 1993;50:609–14.CrossRefGoogle Scholar
  15. 15.
    Palmer JB. Bolus aggregation in the oropharynx does not depend on gravity. Arch Phys Med Rehabil. 1998;79:691–6.CrossRefGoogle Scholar
  16. 16.
    Palmer JB, Hiimae KM, Matsuo K, Hashima H. Volitional control of food transport and bolus formation during feeding. Physiol Behav. 2007;91:66–70.CrossRefGoogle Scholar
  17. 17.
    Toogood JA, Barr AM, Stevens TL, Gati JS, Menon RS, Martin RE. Discrete functional contribution of cerebral cortical foci in voluntary swallowing: a functional magnetic resonance imaging (fMRI) “Go, No-Go” study. Exp Brain Res. 2005;161(1):81–90.CrossRefGoogle Scholar
  18. 18.
    Kendall KA. Oropharyngeal swallowing variability. Laryngoscope. 2002;112:547–51.CrossRefGoogle Scholar
  19. 19.
    Belafsky PC, Kuhn MA. The clinician’s guide to swallowing fluoroscopy. Berlin: Springer; 2014.Google Scholar
  20. 20.
    Logemann JA, Pauloski BR, Rademaker AW, Colangelo LA, Kahrilas PJ, Smith CH. Temporal and biomechanical characteristics of oropharyngeal swallow in younger and older men. J Speech Lang Hear Re. 2000; s 43:1264–1274.Google Scholar
  21. 21.
    Molfenter SM, Steele CM. Temporal variability in the deglutition literature. Dysphagia. 2012;27:162–77.CrossRefGoogle Scholar
  22. 22.
    Nam HS, Oh BM, Han TR. Temporal characteristics of hyolaryngeal structural movements in normal swallowing. Laryngoscope. 2015;125:2129–33.CrossRefGoogle Scholar
  23. 23.
    Pearson WG Jr, Taylor BK, Blair J, Martin-Harris B. Computational analysis of swallowing mechanics underlying impaired epiglottic inversion. Laryngoscope. 2016;126:1854–8.CrossRefGoogle Scholar
  24. 24.
    Kendall KA, McKenzie S, Leonard RJ, Goncalves MI, Walker A. Timing of events in normal swallowing: a videofluoroscopic study. Dysphagia. 2000;15:74–83.CrossRefGoogle Scholar
  25. 25.
    Oshima F, Yokozeki M, Hamanaka M, Imai K, Makino M, Kimura M, Fujimoto Y, Fujiu-Kurachi M. Prediction of dysphagia severity: an investigation of the dysphagia patterns in patients with lateral medullary infarction. Intern Med. 2013;52:1325–31.CrossRefGoogle Scholar
  26. 26.
    Olzewski J, Baxter D. Cytoarchitecture of the human brain stem. 2nd ed. Basel: Kargor; 1982.Google Scholar
  27. 27.
    Kim JS. Pure lateral medullary infarction: clinical-radiological correlation of 130 acute, consecutive patients. Brain. 2003;126:1864–72.CrossRefGoogle Scholar
  28. 28.
    Crary MA, Mann GDC, Groher ME. Initial psychometric assessment of a functional oral intake scale for dysphagia in stroke patients. Arch Phys Med Rehabil. 2005;86:1516–20.CrossRefGoogle Scholar
  29. 29.
    Rosenbeck JC, Robbins JA, Roecker EB, Coyle JL, Wood JL. A penetration-aspiraiton scale. Dysphagia. 1996;11(2):93–8.CrossRefGoogle Scholar
  30. 30.
    Pearson WG Jr, Molfenter SM, Smith ZM, Steele CM. Image-based management of post-swallow residue: the normalized residue ratio scale. Dysphagia. 2013;28:167–77.CrossRefGoogle Scholar
  31. 31.
    Huckabee M-L, Lamvik K, Jones R. Pharyngeal mis-sequencing in dysphagia: characteristics, rehabilitative response, and etiological speculation. J Neurol Sci. 2014;343:153–8.CrossRefGoogle Scholar
  32. 32.
    Rofes L, Vilardell N, Clave P. Post-stroke dysphagia: progress at last. Neurogastroenterol Motil. 2013;25:278–82.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Physical Medicine and RehabilitationTohoku University Graduate School of MedicineSendaiJapan
  2. 2.Rehabilitation DepartmentYokohama Brain and Spine CenterYokohamaJapan
  3. 3.Rehabilitation DepartmentSuwa Redcross HospitalSuwaJapan
  4. 4.Kyoto Redcross HospitalKyotoJapan

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