, Volume 30, Issue 5, pp 540–550 | Cite as

Electrophysiological Investigations of Shape and Reproducibility of Oropharyngeal Swallowing: Interaction with Bolus Volume and Age

  • Enrico AlfonsiEmail author
  • Giuseppe Cosentino
  • Luca Mainardi
  • Antonio Schindler
  • Mauro Fresia
  • Filippo Brighina
  • Marco Benazzo
  • Arrigo Moglia
  • Elena Alvisi
  • Brigida Fierro
  • Giorgio Sandrini
Original Article


Electrophysiological assessment provides valuable information on physiological and pathophysiological characteristics of human swallowing. Here, new electrophysiological measures for the evaluation of oropharyngeal swallowing were assessed: (1) the activation pattern of the submental/suprahyoid EMG activity (SHEMG); (2) the reproducibility of the oral and pharyngeal phases of swallowing, by calculating the similarity index (SI) of the SHEMG (SI-SHEMG) and of the laryngeal–pharyngeal mechanogram (SI-LPM) during repeated swallows; and (3) kinesiological measures related to the LPM. An electrophysiological–mechanical method for measuring the activation pattern of the SHEMG, the SI-SHEMG, and the SI-LPM, and maximal LPM velocity and acceleration during swallowing was applied in 65 healthy subjects divided into three age groups (18–39, 40–59, 60 years or over). All the measures were assessed during three trials of eight consecutive swallows of different liquid bolus volumes (3, 12, and 20 ml). A high overall reproducibility of oropharyngeal swallowing in healthy humans was recorded. However, while values of SI-SHEMG were similar in all the age groups, the SI-LPM was found to fall significantly in the older age group. Both the SI-SHEMG and the SI-LPM were found to fall with increasing bolus volumes. The activation pattern of the SHEMG and the LPM kinesiological measures were differently modified by bolus volume and age in the older subjects with respect to the others. We describe a new approach to the electrophysiological study of swallowing based on computed semi-automatic analyses. Our findings provide insight into some previously uninvestigated aspects of oropharyngeal swallowing physiology, considered in relation to bolus volume and age. The new electrophysiological measures here described could prove useful in the clinical setting, as it is likely that they could be differently affected in patients with different kinds of dysphagia.


Swallowing Dysphagia Electromyography Age Bolus volume Reproducibility 



EMG activity of the submental/suprahyoid muscles


Envelope of the submental/suprahyoid EMG activity


Triangular ‘theoretical’ reference shape


Analytical comparison between SHEMG-E and T-shape


Similarity index


Laryngeal–pharyngeal mechanogram


Similarity index of the SHEMG-E


Similarity index of the LPM


Maximal velocity of the LPM


Maximal acceleration of the LPM


Motor units



The authors wish to thank Ms. Catherine Wrenn for the linguistic revision of the manuscript. This study was supported by a Grant from the Italian Ministry of Health related to the Project “Presbyphagia: analysis of diagnostic criteria and identification of potential innovative treatments” RF-2010-231945.

Compliance with Ethical Standards

Conflict of interest

The authors report no conflicts of interest.


  1. 1.
    Ertekin C, Aydoğdu I, Yüceyar N, Pehlivan M, Ertaş M, Uludağ B, Celebi G. Effects of bolus volumes on the oropharyngeal swallowing: an electrophysiological study in man. Am J Gastroenterol. 1997;11:2049–53.Google Scholar
  2. 2.
    Perlman AL, Palmer PM, McCulloch TM, Van Daele JD. Electromyographic activity from human laryngeal, pharyngeal, and submental muscles during swallowing. J Appl Physiol. 1999;86:1663–9.PubMedGoogle Scholar
  3. 3.
    Dind R, Logemann JA, Larson CR, Rademaker AW. The effects of taste and consistency on swallow physiology in younger and older healthy individuals: a surface electromyographic study. J Speech Lang Hear Res. 2003;46:977–89.CrossRefGoogle Scholar
  4. 4.
    Vaiman M, Eviatar E, Segal S. Evaluation of normal deglutition with the help of rectified surface electromyography. Dysphagia. 2004;19:125–32.CrossRefPubMedGoogle Scholar
  5. 5.
    Miyaoka Y, Ashida I, Kawakami S, Tamaki Y, Miyaoka S. Activity patterns of the suprahyoid muscles during swallowing of different fluid volumes. J Oral Rehabil. 2010;37:575–82.PubMedGoogle Scholar
  6. 6.
    Nilsson H, Ekberg O, Olsson R, Hindfelt B. Quantitative aspects of swallowing in an elderly nondysphagic population. Dysphagia. 1996;11:180–4.CrossRefPubMedGoogle Scholar
  7. 7.
    Ertekin C, Keskin A, Kiylioglu N, Kirazli Y, On AY, Tarlaci S, Aydoğdu I. The effect of head and neck positions on oropharyngeal swallowing: a clinical and electrophysiological study. Arch Phys Med Rehabil. 2001;82:1255–60.CrossRefPubMedGoogle Scholar
  8. 8.
    Cichero J. Swallowing from infancy to old age. In: Cichero JAY, Murdoch BE, editors. Dysphagia. Foundation, theory and practice, vol. 6. Chichester: Wiley; 2006. p. 26–46.Google Scholar
  9. 9.
    Sahin Sağlam AM, Uydas NE. Relationship between head posture and hyoid position in adult females and males. J Craniomaxillofac Surg. 2006;34:85–92.CrossRefPubMedGoogle Scholar
  10. 10.
    Inagaki D, Miyaoka Y, Ashida I, Ueda K, Yamada Y. Influences of body posture on duration of oral swallowing in normal young adults. J Oral Rehabil. 2007;34:414–21.CrossRefPubMedGoogle Scholar
  11. 11.
    Sakuma T, Kida I. Relationship between ease of swallowing and deglutition-related muscle activity in various postures. J Oral Rehabil. 2010;37:583–9.PubMedGoogle Scholar
  12. 12.
    Logemann JA. Evaluation and treatment of swallowing disorders. Austin: ProED; 1983.Google Scholar
  13. 13.
    Ertekin C, Pehlivan M, Aydoğdu I, Ertaş M, Uludağ B, Celebi G, Colakoğlu Z, Sağduyu A, Yüceyar N. An electrophysiological investigation of deglutition in man. Muscle Nerve. 1995;18:1177–86.CrossRefPubMedGoogle Scholar
  14. 14.
    Alfonsi E, Versino M, Merlo IM, Pacchetti C, Martignoni E, Bertino G, Moglia A, Tassorelli C, Nappi G. Electrophysiologic patterns of oral-pharyngeal swallowing in parkinsonian syndromes. Neurology. 2007;68:583–9.CrossRefPubMedGoogle Scholar
  15. 15.
    Kahrilas PJ, Logemann JA. Volume accommodation during swallowing. Dysphagia. 1993;8:259–65.CrossRefPubMedGoogle Scholar
  16. 16.
    Crary MA, Carnaby Mann GD, Groher ME. Biomechanical correlates of surface electromyography signals obtained during swallowing by healthy adults. J Speech Lang Hear Res. 2006;49(1):186–93.CrossRefPubMedGoogle Scholar
  17. 17.
    Inman VT, Ralston HJ, Sauders JB, Feinstein B, Wright EW Jr. Relation of human electromyogram to muscular tension. Electroencephalogr Clin Neurophysiol. 1952;4:187–94.CrossRefPubMedGoogle Scholar
  18. 18.
    Jean A. Brainstem control of swallowing: neural network and cellular mechanisms. Physiol Rev. 2001;81:929–69.PubMedGoogle Scholar
  19. 19.
    Takahashi K, Groher M, Michi K. Symmetry and reproducibility of swallowing sounds. Dysphagia. 1994;9:168–73.CrossRefPubMedGoogle Scholar
  20. 20.
    Pinnington LL, Ellis RE. Reproducibility of swallowing over time in healthy elderly adults. Dysphagia. 2006;2006:1–6.CrossRefGoogle Scholar
  21. 21.
    Faes L, Nollo G, Antolini R, Gaita F, Ravelli F. A method for quantifying atrial fibrillation organization based on wave-morphology similarity. IEEE Trans Biomed Eng. 2002;49:1504–13.CrossRefPubMedGoogle Scholar
  22. 22.
    Mainardi L, Sornmo L, Cerutti S. Understanding atrial fibrillation: the signal processing contribution. San Francisco: Morgan & Claypool Publishers; 2008.Google Scholar
  23. 23.
    Babaei A, Ward BD, Siwiec RM, Ahmad S, Kern M, Nencka A, Li SJ, Shaker R. Functional connectivity of the cortical swallowing network in humans. Neuroimage. 2013;76:33–44.PubMedCentralCrossRefPubMedGoogle Scholar
  24. 24.
    Michou E, Hamdy S. Cortical input in control of swallowing. Curr Opin Otolaryngol Head Neck Surg. 2009;17(3):166–71.CrossRefPubMedGoogle Scholar
  25. 25.
    Sörös P, Inamoto Y, Martin RE. Functional brain imaging of swallowing: an activation likelihood estimation meta-analysis. Hum Brain Mapp. 2009;30:2426–39.CrossRefPubMedGoogle Scholar
  26. 26.
    Ertekin C, Aydoğdu I, Yűceyar N. Piecemeal deglutition and dysphagia limit in normal subjects and in patients with swallowing disorders. J Neurol Neurosurg Psychiatry. 1996;61:491–6.PubMedCentralCrossRefPubMedGoogle Scholar
  27. 27.
    Dantas RO, Kern MK, Massey BT, Dodds WJ, Kahrilas PJ, Brasseur JG, Cook IJ, Lang IM. Effect of swallowed bolus variables on oral and pharyngeal phases of swallowing. Am J Physiol. 1990;258:G675–81.PubMedGoogle Scholar
  28. 28.
    Aviv JE, Martin JH, Jones ME, Wee TA, Diamond B, Keen MS, Blitzer A. Age-related changes in pharyngeal and supraglottic sensation. Ann Otol Rhinol Laryngol. 1994;103:749–52.CrossRefPubMedGoogle Scholar
  29. 29.
    Takamori M, Gutmann L, Shane SR, Morgantown WV. Contractile properties of human skeletal muscle. Normal and thyroid disease. Arch Neurol. 1971;25:535–46.CrossRefPubMedGoogle Scholar
  30. 30.
    Buchthal F, Schmalbruch H. Motor unit of mammalian muscle. Physiol Rev. 1980;60(1):90–142.PubMedGoogle Scholar
  31. 31.
    Yao W, Fuglevand RJ, Enoka RM. Motor-unit synchronization increases EMG amplitude and decreases force steadiness of simulated contractions. J Neurophysiol. 2000;83(1):441–52.PubMedGoogle Scholar
  32. 32.
    Semmler JG. Motor unit synchronization and neuromuscular performance. Exerc Sport Sci Rev. 2002;30(1):8–14.CrossRefPubMedGoogle Scholar
  33. 33.
    Bagust J, Lewis DM, Westerman RA. The properties of motor units in a fast and slow twitch muscle during post-natal development in the kitten. J Physiol. 1974;237:75–90.PubMedCentralCrossRefPubMedGoogle Scholar
  34. 34.
    De Luca CJ, Erim Z. Common drive of motor units in regulation of muscle force. Trends Neurosci. 1994;17:229–305.Google Scholar
  35. 35.
    De Luca CJ, Adam A, Wotiz R, Gilmore LD, Nawab SH. Decomposition of surface EMG signals. J Neurophysiol. 2006;96:1646–57.CrossRefPubMedGoogle Scholar
  36. 36.
    Howard JE, McGill KC, Dorfman LJ. Age effects on properties of motor unit action potentials: ADEMG analysis. Ann Neurol. 1988;24:207–13.CrossRefPubMedGoogle Scholar
  37. 37.
    Donner M, Jones B. Ageing and neurological disease. In: Jones B, Donner MW, editors. Normal and abnormal swallowing: imaging in diagnosis and therapy. New York: Springer; 1991.Google Scholar
  38. 38.
    Robbins J, Hamilton JW, Lof GL, Kempster GB. Oropharyngeal swallowing in normal adults of different ages. Gastroenterology. 1992;103:823–9.PubMedGoogle Scholar
  39. 39.
    Martin R, Barr A, MacIntosh B, Smith R, Stevens T, Taves D, Gati J, Menon R, Hachinski V. Cerebral cortical processing of swallowing in older adults. Exp Brain Res. 2007;176:12–22.CrossRefPubMedGoogle Scholar
  40. 40.
    Malandraki GA, Bradley PS, Perlmann A, Karampinos DC. Age-related differences in laterality of cortical activations in swallowing. Dysphagia. 2010;25:238–49.CrossRefPubMedGoogle Scholar
  41. 41.
    Humbert IA, Fitzgerald ME, McLaren DG, Johnson S, Porcaro E, Kosmatka K, Hind J, Robbins J. Neurophysiology of swallowing: effects of age and bolus type. Neuroimage. 2009;4:982–91.CrossRefGoogle Scholar
  42. 42.
    Freund HJ, Büdingen HJ, Dietz V. Activity of single motor units from human forearm muscles during voluntary isometric contractions. J Neurophysiol. 1975;38(4):933–46.PubMedGoogle Scholar
  43. 43.
    Alfonsi E, Merlo IM, Ponzio M, Montomoli C, Tassorelli C, Biancardi C, Lozza A, Martignoni E. An electrophysiological approach to the diagnosis of neurogenic dysphagia: implications for botulinum toxin treatment. J Neurol Neurosurg Psychiatry. 2010;81:54–60.CrossRefPubMedGoogle Scholar
  44. 44.
    Alfonsi E, Bergamaschi R, Cosentino G, Ponzio M, Montomoli C, Restivo DA, Brighina F, Ravaglia S, Prunetti P, Bertino G, Benazzo M, Fontana D, Moglia A. Electrophysiological patterns of oropharyngeal swallowing in multiple sclerosis. Clin Neurophysiol. 2013;124:1638–45.CrossRefPubMedGoogle Scholar
  45. 45.
    Taniguchi H, Tsukada T, Ootaki S, Yamada Y, Inoue M. Correspondence between food consistency and suprahyoid muscle activity, tongue pressure, and bolus transit times during the oropharyngeal phase of swallowing. J Appl Physiol. 2008;105:791–9.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Enrico Alfonsi
    • 1
    Email author
  • Giuseppe Cosentino
    • 2
  • Luca Mainardi
    • 3
  • Antonio Schindler
    • 4
  • Mauro Fresia
    • 1
  • Filippo Brighina
    • 2
  • Marco Benazzo
    • 5
  • Arrigo Moglia
    • 1
  • Elena Alvisi
    • 1
  • Brigida Fierro
    • 2
  • Giorgio Sandrini
    • 1
  1. 1.Department of Neurophysiopathology and Neurorehabilitation, National Institute of Neurology, “C. Mondino” Foundation IRCCSUniversity of PaviaPaviaItaly
  2. 2.Department of Experimental Biomedicine and Clinical Neurosciences (BioNeC)University of PalermoPalermoItaly
  3. 3.Department of Electronics, Information and BioengineeringPolitecnico di MilanoMilanItaly
  4. 4.Department of Otorhinolaryngology, “L. Sacco” HospitalUniversity of MilanMilanItaly
  5. 5.Department of Otorhinolaryngology, “San Matteo” HospitalUniversity of PaviaPaviaItaly

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