Skip to main content
SpringerLink
Log in

Electrophysiological Evaluation of Dysphagia in the Mild or Moderate Patients with Multiple Sclerosis: A Concept of Subclinical Dysphagia

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

Abstract

Swallowing mechanism and neurogenic dysphagia in MS have been rarely studied by electromyographical (EMG) methods. This study aims to evaluate the presence of subclinical dysphagia in patients with mild multiple sclerosis (MS) using electrophysiological methods. A prospective study of 51 patients with relapsing remitting multiple sclerosis and 18 age-matched healthy adults was investigated. We used electromyography to measure the activity of the submental muscles during swallowing. Electrophysiological recordings of patients were obtained during relapse, after relapse, and at any time in remission period. Clinical dysphagia was found in 12 % of MS patients, while electrophysiological swallowing abnormalities were encountered in 33 % of patients. Subclinical dysphagia was determined in 35 % of patients during an MS relapse, in 20 % of patients after a relapse, and in 25 % of all 51 patients in the remission period based on EMG findings. Duration of swallowing signal of submental muscles in all MS patients was found to be longer than in normal subjects (p = 0.001). During swallowing of 50 ml of sequential water, the compensatory respiratory cycles occurred more often in MS patients than normal subjects, especially during a relapse (p = 0.005). This is the first study investigating swallowing abnormalities and subclinical dysphagia from the electrophysiological aspect in MS patients with mild disability. The electrophysiological tests described in this study are useful to uncover subclinical dysphagia since they have the advantage of being rapid, easy to apply, non-invasive, and without risk for the patients.

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

Similar content being viewed by others

References

  1. Ertekin C, Aydoğdu I. Neurophysiology of swallowing. Clin Neurophysiol. 2003;114:2226–44.

    Article  PubMed  Google Scholar 

  2. Ertekin C. Voluntary versus spontaneous swallowing in man. Dysphagia. 2011;26:183–92.

    Article  PubMed  Google Scholar 

  3. 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(9):2081–7.

    Article  CAS  PubMed  Google Scholar 

  4. Jean A. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev. 2001;81:929–69.

    CAS  PubMed  Google Scholar 

  5. Aviv JE. Effects of aging on sensitivity of the pharyngeal and supraglottic areas. Am J Med. 1997;103:74s–6s.

    Article  CAS  PubMed  Google Scholar 

  6. Chi-Fishman G, Stone M, McCall GN. Lingual action in normal sequential swallowing. J Speech Lang Hear Res. 1998;41:771–85.

    Article  CAS  PubMed  Google Scholar 

  7. Ertekin C, Kiylioglu N, Tarlaci S, Keskin A, Aydogdu I. Effect of mucosal anesthesia on oropharyngeal swallowing. Neurogastroenterol Motil. 2000;12:567–72.

    Article  CAS  PubMed  Google Scholar 

  8. Theurer JA, Bihari F, Barr AB, Martin RE. Oropharyngeal stimulation with air-pulse trains increases swallowing frequency in healthy adults. Dysphagia. 2005;20:254–60.

    Article  PubMed  Google Scholar 

  9. Bergamaschi R, Crivelli P, Rezzani C, Patti F, Solaro C, Rossi P, et al. The DYMUS questionnaire for the assessment of dysphagia in multiple sclerosis. J Neurol Sci. 2008;269:49–53.

    Article  CAS  PubMed  Google Scholar 

  10. Poorjavad M, Derakhshandeh F, Etemadifar M, Soleymani B, Minagar A, Maghzi AH. Oropharyngeal dysphagia in multiple sclerosis. Mult Scler. 2010;16(3):362–5.

    Article  PubMed  Google Scholar 

  11. Calcagno P, Ruoppolo G, Grasso MG, De Vincentiis M, Paolucci S. Dysphagia in multiple sclerosis—prevalence and prognostic factors. Acta Neurol Scand. 2002;105:40–3.

    Article  CAS  PubMed  Google Scholar 

  12. De Pauw A, Dejaeger E, D’hooghe B, Carton H. Dysphagia in multiple sclerosis. Clin Neurol Neurosurg. 2002;104(4):345–51.

    Article  PubMed  Google Scholar 

  13. Tassorelli C, Bergamaschi R, Buscone S, Bartolo M, Furnari A, Crivelli P, et al. Dysphagia in multiple sclerosis: from pathogenesis to diagnosis. Neurol Sci. 2008;29:360.

    Article  Google Scholar 

  14. Prosiegel M, Schelling A, Wagner-Sonntag E. Dysphagia and multiple sclerosis. Int MS J. 2004;11:22–31.

    CAS  PubMed  Google Scholar 

  15. Abraham S, Scheinberg LC, Smith CR, LaRocca NG. Neurologic impairment and disability status in outpatients with multiple sclerosis reporting dysphagia symptomatology. J Neurol Rehabil. 1997;11:7–13.

    Google Scholar 

  16. Wiesner W, Wetzel SG, Kappos L, Hoshi MM, Witte U, Radue EW, Steinbrich W. Swallowing abnormalities in multiple sclerosis: correlation between videofluoroscopy and subjective symptoms. Eur Radiol. 2002;12(4):789–92.

    Article  CAS  PubMed  Google Scholar 

  17. Thomas FJ, Wiles CM. Dysphagia and nutritional status in multiple sclerosis. J Neurol. 1999;246:677–82.

    Article  CAS  PubMed  Google Scholar 

  18. Logeman JA. Evaluation and treatment of swallowing disorders. 2nd ed. Austin: Pro-ed Inc; 1998.

    Google Scholar 

  19. Ertekin C, Pehlivan M, Aydoğdu I, Ertaş M, Uludağ B, Celebi G, et al. An electrophysiological investigation of deglutition in man. Muscle Nerve. 1995;18:1177–86.

    Article  CAS  PubMed  Google Scholar 

  20. Ertekin C, Aydogdu I, Yüceyar N, Tarlaci S, Kiylioglu N, Pehlivan M, Celebi G. Electrodiagnostic methods for neurogenic dysphagia. Electroencephalogr Clin Neurophysiol. 1998;109(4):331–40.

    Article  CAS  PubMed  Google Scholar 

  21. Aydogdu I, Kiylioglu N, Tarlaci S, Tanriverdi Z, Alpaydin S, Acarer A, Baysal L, Arpaci E, et al. Diagnostic value of “dysphagia limit” for neurogenic dysphagia: 17 years of experience in 1278 adults. Clin Neurophysiol. 2014. doi:10.1016/j.clinph.2014,06.035.

    PubMed  Google Scholar 

  22. Ertekin C, Aydogdu I, Yüceyar N. Piecemeal deglutition and dysphagia limit in normal subjects and in patients with swallowing disorders. JNNP. 1996;61:491–6.

    CAS  Google Scholar 

  23. Ertekin C, Aydogdu I, Yüceyar N, et al. Pathophysiological mechanisms of oropharyngeal dysphagia in amyotrophic lateral sclerosis. Brain. 2000;123:125–40.

    Article  PubMed  Google Scholar 

  24. Aydogdu I, Tanriverdi Z, Ertekin C. Dysfunction of bulbar central pattern generator in ALS patients with dysphagia during sequential swallowing. Clin Neurophysiol. 2011;122:1219–28.

    Article  PubMed  Google Scholar 

  25. Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M. Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol. 2011;69(292):302.

    Google Scholar 

  26. Kurzke JF. Rating neurologist impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology. 1983;33:1444–52.

    Article  Google Scholar 

  27. Gurgor N, Arici S, Kurt-Incesu T, Secil Y, Tokucoglu F, Ertekin C. An electrophysiological study of the sequential water swallowing. J Electromyogr Kinesiol. 2013;23:619–26.

    Article  CAS  PubMed  Google Scholar 

  28. Ertekin C, Aydogdu I, Tarlaci S, Turman AB, Kiylioglu N. Mechanisms of dysphagia in suprabulbar palsy with lacunar infarct. Stroke. 2000;31(6):1370–6.

    Article  CAS  PubMed  Google Scholar 

  29. Daniels SK, Foundas AL. Swallowing physiology of sequential straw drinking. Dysphagia. 2001;16(3):176–82.

    Article  CAS  PubMed  Google Scholar 

  30. Lederle A, Hoit JD, Barkmeier-Kraemer J. Effects of sequential swallowing on drive to breathe in young, healthy adults. Dysphagia. 2012;27(2):221–7.

    Article  PubMed  Google Scholar 

  31. Dozier TS, Brodsky MB, Michel Y, Walters BC Jr, Martin-Harris B. Coordination of swallowing and respiration in normal sequential cup swallows. Laryngoscope. 2006;116(8):1489–93.

    Article  PubMed  Google Scholar 

  32. Miller AJ. The neuroscientific principles of swallowing and dysphagia. San Diego: Singular Publishing Group; 1999.

    Google Scholar 

  33. Watanabe Y, Abe S, Ishikawa T, Yamada Y, Yamane GY. Cortical regulation during the early stage of initiation of voluntary swallowing in humans. Dysphagia. 2004;19(2):100–8.

    Article  PubMed  Google Scholar 

Download references

Conflict of interest

None.

Author information

Authors and Affiliations

  1. Department of Neurology, Faculty of Medicine, Atatürk Training and Research Hospital, Izmir Katip Celebi University, Izmir, Turkey

    Yesim Beckmann, Nevin Gürgör, Ahmet Çakır, Şehnaz Arıcı, Tülay Kurt İncesu & Yaprak Seçil

  2. Department of Neurology, Ege University Medical School, Izmir, Turkey

    Cumhur Ertekin

Authors
  1. Yesim Beckmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nevin Gürgör
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ahmet Çakır
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Şehnaz Arıcı
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tülay Kurt İncesu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yaprak Seçil
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Cumhur Ertekin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yesim Beckmann.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Beckmann, Y., Gürgör, N., Çakır, A. et al. Electrophysiological Evaluation of Dysphagia in the Mild or Moderate Patients with Multiple Sclerosis: A Concept of Subclinical Dysphagia. Dysphagia 30, 296–303 (2015). https://doi.org/10.1007/s00455-015-9598-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00455-015-9598-1

Keywords

Search

Navigation