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27-07-2021 | Electromyographic | Review

Electrokinesiographic Study of Oropharyngeal Swallowing in Neurogenic Dysphagia

Authors: Enrico Alfonsi, Massimiliano Todisco, Mauro Fresia, Cristina Tassorelli, Giuseppe Cosentino

Published in: Dysphagia | Issue 2/2023

Abstract

Electrokinesiographic study of swallowing (EKSS) can be useful for the assessment of patients with suspected or overt neurogenic dysphagia. EKSS consists of multichannel recording of the electromyographic (EMG) activity of the suprahyoid/submental muscle complex (SHEMG), the EMG activity of the cricopharyngeal muscle (CPEMG), and the laryngopharyngeal mechanogram (LPM). The LPM is an expression of the mechanical changes that the laryngopharyngeal structures undergo during the pharyngeal phase of swallowing. This method allows detailed evaluation of the magnitude, duration and temporal relations of the different events that characterize oropharyngeal swallowing, and thus in-depth exploration both of physiological deglutition mechanisms and of pathophysiological features of swallowing in neurogenic dysphagia. Furthermore, EKSS can guide dysphagia treatment strategies, allowing identification of optimal solutions for single patients. For instance, CPEMG recording can identify incomplete or absent relaxation of the upper esophageal sphincter during the pharyngeal phase of swallowing, thus suggesting a therapeutic approach based on botulinum toxin injection into the cricopharyngeal muscle. More recently, the ‘shape’ of SHEMG and the reproducibility of both SHEMG and LPM over repeated swallowing acts have been implemented as novel electrokinesiographic parameters. These measures could be valuable for straightforward non-invasive investigation of dysphagia severity and response to dysphagia treatment in clinical practice.

Bass NH, Morrell RM. The neurology of swallowing. In: Groher ME, editor. Dysphagia, diagnosis and management. 2nd ed. Boston, Massachusetts: Butterworth-Heinemann; 1992. p. 1–30.

Jean A. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev. 2001;81:929–69. https://doi.org/10.1152/physrev.2001.81.2.929.CrossRefPubMed

Martin-Harris B. Coordination of respiration and swallowing. GI Motility online. 2006. https://doi.org/10.1038/gimo10.CrossRef

Zito A, Bini P, Todisco M, Cosentino G, Mauramati S, Paoletti M, Marasco V, Marchioni E, Alfonsi E. A rare syndrome causing neurogenic dysphagia. Dysphagia. 2020. https://doi.org/10.1007/s00455-020-10208-w.CrossRefPubMedPubMedCentral

Zald DH, Pardo JV. The functional neuroanatomy of voluntary swallowing. Ann Neurol. 1999;46:281–6. https://doi.org/10.1002/1531-8249(199909)46:3%3c281::AID-ANA2%3e3.0.CO;2-L.CrossRefPubMed

Martin RE, MacIntosh BJ, Smith RC, Barr AM, Stevens TK, Gati JS, Menon RS. Cerebral areas processing swallowing and tongue movement are overlapping but distinct: a functional magnetic resonance imaging study. J Neurophysiol. 2004;92:2428–43. https://doi.org/10.1152/jn.01144.2003.CrossRefPubMed

Mosier K, Patel R, Liu WC, Kalnin A, Maldjian J, Baredes S. Cortical representation of swallowing in normal adults: functional implications. Laryngoscope. 1999;109:1417–23. https://doi.org/10.1097/00005537-199909000-00011.CrossRefPubMed

Kern MK, Jaradeh S, Arndorfer RC, Shaker R. Cerebral cortical representation of reflexive and volitional swallowing in humans. Am J Physiol Gastrointest Liver Physiol. 2001;280:G354-360. https://doi.org/10.1152/ajpgi.2001.280.3.G354.CrossRefPubMed

Hamdy S, Aziz Q, Rothwell JC, Singh KD, Barlow J, Hughes DG, Tallis RC, Thompson DG. The cortical topography of human swallowing musculature in health and disease. Nat Med. 1996;2:1217–24. https://doi.org/10.1038/nm1196-1217.CrossRefPubMed

10.

Hamdy S, Rothwell JC, Brooks DJ, Bailey D, Aziz Q, Thompson DG. Identification of the cerebral loci processing human swallowing with H2(15)O PET activation. J Neurophysiol. 1999;81:1917–26. https://doi.org/10.1152/jn.1999.81.4.1917.CrossRefPubMed

11.

Abe S, Wantanabe Y, Shintani M, Tazaki M, Takahashi M, Yamane GY, Ide Y, Yamada Y, Shimono M, Ishikawa T. Magnetoencephalographic study of the starting point of voluntary swallowing. Cranio. 2003;21:46–9. https://doi.org/10.1080/08869634.2003.11746231.CrossRefPubMed

12.

Penfield W, Boldrey E. Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain. 1937;60:389–443. https://doi.org/10.1093/brain/60.4.389.CrossRef

13.

Barker AT, Jalinous R, Freeston IL. Non-invasive magnetic stimulation of human motor cortex. Lancet. 1985;1:1106–7. https://doi.org/10.1016/s0140-6736(85)92413-4.CrossRefPubMed

14.

Jestrović I, Coyle JL, Sejdić E. Decoding human swallowing via electroencephalography: a state-of-the-art review. J Neural Eng. 2015;12: 051001. https://doi.org/10.1088/1741-2560/12/5/051001.CrossRefPubMedPubMedCentral

15.

Hamdy S, Mikulis DJ, Crawley A, Xue S, Lau H, Henry S, Diamant NE. Cortical activation during human volitional swallowing: an event-related fMRI study. Am J Physiol. 1999;277:G219-225. https://doi.org/10.1152/ajpgi.1999.277.1.G219.CrossRefPubMed

16.

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. https://doi.org/10.1212/01.wnl.0000254478.46278.67.CrossRefPubMed

17.

Miller AJ. The neuroscientific principles of swallowing and dysphagia. San Diego, California: Singular Publishing Group; 1999. p. 100–1.

18.

Mosier K, Bereznaya I. Parallel cortical networks for volitional control of swallowing in humans. Exp Brain Res. 2001;140:280–9. https://doi.org/10.1007/s002210100813.CrossRefPubMed

19.

Martin RE, Goodyear BG, Gati JS, Menon RS. Cerebral cortical representation of automatic and volitional swallowing in humans. J Neurophysiol. 2001;85:938–50. https://doi.org/10.1152/jn.2001.85.2.938.CrossRefPubMed

20.

McCullough GH, Wertz RT, Rosenbek JC, Mills RH, Webb WG, Ross KB. Inter- and intrajudge reliability for videofluoroscopic swallowing evaluation measures. Dysphagia. 2001;16:110–8. https://doi.org/10.1007/PL00021291.CrossRefPubMed

21.

Roman S, Huot L, Zerbib F, Bruley des Varannes S, Gourcerol G, Coffin B, Ropert A, Roux A, Mion F. High-resolution manometry improves the diagnosis of esophageal motility disorders in patients with dysphagia: a randomized multicenter study. Am J Gastroenterol. 2016;111:372–80. https://doi.org/10.1038/ajg.2016.1.CrossRefPubMed

22.

Sundaram PS, Subramanyam P. Scintigraphic evaluation of swallowing. In: Thankappan K, Iyer S, Menon JR (eds) Dysphagia management in head and neck cancers. Springer; 2018, p. 89–100

23.

Rosenbek JC, Robbins JA, Roecker EB, Coyle JL, Wood JL. A penetration-aspiration scale. Dysphagia. 1996;11:93–8. https://doi.org/10.1007/BF00417897.CrossRefPubMed

24.

Langmore SE, Schatz K, Olsen N. Fiberoptic endoscopic examination of swallowing safety: a new procedure. Dysphagia. 1988;2:216–9. https://doi.org/10.1007/BF02414429.CrossRefPubMed

25.

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. https://doi.org/10.1002/mus.880181014.CrossRefPubMed

26.

Logemann JA. Evaluation and treatment of swallowing disorders, 2nd edn. Pro-Ed, Austin, Texas; 1998.

27.

Goyal RK, Paterson WG. Esophageal motility. In: Wood JD (ed) Handbook of physiology, the gastrointestinal system. Bethesda, Maryland; 1989, section 6, volume I (pt 2), chapter 22, p. 865–908.

28.

Lang IM. Upper esophageal sphincter. GI Motility online. 2006. https://doi.org/10.1038/gimo12.CrossRef

29.

Lang IM, Shaker R. An overview of the upper esophageal sphincter. Curr Gastroenterol Rep. 2000;2:185–90. https://doi.org/10.1007/s11894-000-0059-z.CrossRefPubMed

30.

Sivarao DV, Goyal RK. Functional anatomy and physiology of the upper esophageal sphincter. Am J Med. 2000;108:27S-37S. https://doi.org/10.1016/s0002-9343(99)00337-x.CrossRefPubMed

31.

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. https://doi.org/10.1016/j.clinph.2013.03.003.CrossRefPubMed

32.

Alfonsi E, Cosentino G, Mainardi L, Schindler A, Fresia M, Brighina F, Benazzo M, Moglia A, Alvisi E, Fierro B, Sandrini G. Electrophysiological investigations of shape and reproducibility of oropharyngeal swallowing: interaction with bolus volume and age. Dysphagia. 2015;30:540–50. https://doi.org/10.1007/s00455-015-9634-1.CrossRefPubMed

33.

Ertekin C, Aydoğdu I, Yüceyar N. Piecemeal deglutition and dysphagia limit in normal subjects and in patients with swallowing disorders. J Neurol Neurosurg Psychiatry. 1996;61:491–6. https://doi.org/10.1136/jnnp.61.5.491.CrossRefPubMedPubMedCentral

34.

Gokyigit MC, Pazarci NK, Ercan I, Seker S, Turgut S, Ertekin C. Identification of distinct swallowing patterns for different bolus volumes. Clin Neurophysiol. 2009;120:1750–4. https://doi.org/10.1016/j.clinph.2009.07.039.CrossRefPubMed

35.

Bülow M. Psychogenic dysphagia. In: Shaker R, Belafsky PC, Postma GN, Easterling C, editors. Principles of deglutition. A multidisciplinary text for swallowing and its disorders: Springer; 2013. p. 771–6.CrossRef

36.

DeLong MR, Wichmann T. Circuits and circuit disorders of the basal ganglia. Arch Neurol. 2007;64:20–4. https://doi.org/10.1001/archneur.64.1.20.CrossRefPubMed

37.

Hallett M. Parkinson revisited: pathophysiology of motor signs. Adv Neurol. 2003;91:19–28.PubMed

38.

Tsujimura T, Suzuki T, Yoshihara M, Sakai S, Koshi N, Ashiga H, Shiraishi N, Tsuji K, Magara J, Inoue M. Involvement of hypoglossal and recurrent laryngeal nerves on swallowing pressure. J Appl Physiol. 2018;124:1148–54. https://doi.org/10.1152/japplphysiol.00944.2017.CrossRefPubMed

39.

McCulloch TM, Jaffe D. Head and neck disorders affecting swallowing. GI Motility online. 2006. https://doi.org/10.1038/gimo36.CrossRef

40.

Cowan AJ, Skinner M, Berk JL, Sloan JM, O’hara C, Seldin DC, Sanchorawala V. Macroglossia - not always AL amyloidosis. Amyloid. 2011;18:83–6. https://doi.org/10.3109/13506129.2011.560217.CrossRefPubMed

41.

Jones HN, Muller CW, Lin M, Banugaria SG, Case LE, Li JS, O’Grady G, Heller JH, Kishnani PS. Oropharyngeal dysphagia in infants and children with infantile Pompe disease. Dysphagia. 2010;25:277–83. https://doi.org/10.1007/s00455-009-9252-x.CrossRefPubMed

42.

Wittmann AL. Macroglossia in acromegaly and hypothyroidism. Virchows Arch A Pathol Anat Histol. 1977;373:353–60. https://doi.org/10.1007/BF00432533.CrossRefPubMed

43.

Ertekin C, Aydogdu I, Yüceyar N, Kiylioglu N, Tarlaci S, Uludag B. Pathophysiological mechanisms of oropharyngeal dysphagia in amyotrophic lateral sclerosis. Brain. 2000;123:125–40. https://doi.org/10.1093/brain/123.1.125.CrossRefPubMed

44.

Barbiera F, Condello S, De Palo A, Todaro D, Mandracchia C, De Cicco D. Role of videofluorography swallow study in management of dysphagia in neurologically compromised patients. Radiol Med. 2006;111:818–27. https://doi.org/10.1007/s11547-006-0075-7.CrossRefPubMed

45.

Briani C, Marcon M, Ermani M, Costantini M, Bottin R, Iurilli V, Zaninotto G, Primon D, Feltrin G, Angelini C. Radiological evidence of subclinical dysphagia in motor neuron disease. J Neurol. 1998;245:211–6. https://doi.org/10.1007/s004150050207.CrossRefPubMed

46.

Cosentino G, Alfonsi E, Mainardi L, Alvisi E, Brighina F, Valentino F, Fierro B, Sandrini G, Bertino G, Berlangieri M, De Icco R, Fresia M, Moglia A. The importance of the reproducibility of oropharyngeal swallowing in amyotrophic lateral sclerosis. An electrophysiological study. Clin Neurophysiol. 2017;128:792–8. https://doi.org/10.1016/j.clinph.2017.02.006.CrossRefPubMed

47.

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. https://doi.org/10.1161/hs0901.094278.CrossRefPubMed

48.

Umay EK, Unlu E, Saylam GK, Cakci A, Korkmaz H. Evaluation of dysphagia in early stroke patients by bedside, endoscopic, and electrophysiological methods. Dysphagia. 2013;28:395–403. https://doi.org/10.1007/s00455-013-9447-z.CrossRefPubMed

49.

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. https://doi.org/10.1136/jnnp.2009.174698.CrossRefPubMed

50.

Alfonsi E, Restivo DA, Cosentino G, De Icco R, Bertino G, Schindler A, Todisco M, Fresia M, Cortese A, Prunetti P, Ramusino MC, Moglia A, Sandrini G, Tassorelli C. Botulinum toxin is effective in the management of neurogenic dysphagia. Clinical-electrophysiological findings and tips on safety in different neurological disorders. Front Pharmacol. 2017;8:80. https://doi.org/10.3389/fphar.2017.00080.CrossRefPubMedPubMedCentral

51.

Baijens LW, Speyer R. Effects of therapy for dysphagia in Parkinson’s disease: systematic review. Dysphagia. 2009;24:91–102. https://doi.org/10.1007/s00455-008-9180-1.CrossRefPubMed

52.

McFarland NR, Hess CW. Recognizing atypical parkinsonisms: “red flags” and therapeutic approaches. Semin Neurol. 2017;37:215–27. https://doi.org/10.1055/s-0037-1602422.CrossRefPubMedPubMedCentral

53.

Jaradeh S. Muscle disorders affecting oral and pharyngeal swallowing. GI Motility online. 2006. https://doi.org/10.1038/gimo35.CrossRef

54.

Daniels SK. Neurological disorders affecting oral, pharyngeal swallowing. GI Motility online. 2006. https://doi.org/10.1038/gimo34.CrossRef

55.

Ertekin C, Tarlaci S, Aydogdu I, Kiylioglu N, Yuceyar N, Turman AB, Secil Y, Esmeli F. Electrophysiological evaluation of pharyngeal phase of swallowing in patients with Parkinson’s disease. Mov Disord. 2002;17:942–9. https://doi.org/10.1002/mds.10240.CrossRefPubMed

56.

Seçil Y, Arıcı Ş, İncesu TK, Gürgör N, Beckmann Y, Ertekin C. Dysphagia in Alzheimer’s disease. Neurophysiol Clin. 2016;46:171–8. https://doi.org/10.1016/j.neucli.2015.12.007.CrossRefPubMed

57.

Jones CA, Hammer MJ, Hoffman MR, McCulloch TM. Quantifying contributions of the cricopharyngeus to upper esophageal sphincter pressure changes by means of intramuscular electromyography and high-resolution manometry. Ann Otol Rhinol Laryngol. 2014;123:174–82. https://doi.org/10.1177/0003489414522975.CrossRefPubMedPubMedCentral

58.

Müller J, Wenning GK, Verny M, McKee A, Chaudhuri KR, Jellinger K, Poewe W, Litvan I. Progression of dysarthria and dysphagia in postmortem-confirmed parkinsonian disorders. Arch Neurol. 2001;58:259–64. https://doi.org/10.1001/archneur.58.2.259.CrossRefPubMed

59.

Ertekin C (2014) Electrophysiological evaluation of oropharyngeal dysphagia in Parkinson's disease. J Mov Disord.2014;7:31–56. https://doi.org/10.14802/jmd.14008

60.

Litvan I, Sastry N, Sonies BC. Characterizing swallowing abnormalities in progressive supranuclear palsy. Neurology. 1997;48:1654–62. https://doi.org/10.1212/wnl.48.6.1654.CrossRefPubMed

61.

Shaker R. Reflex interaction of pharynx, esophagus, and airways. GI Motility Online. 2006. https://doi.org/10.1038/gimo11.CrossRef

62.

Elidan J, Shochina M, Gonen B, Gay I. Electromyography of the inferior constrictor and cricopharyngeal muscles during swallowing. Ann Otol Rhinol Laryngol. 1990;99:466–9. https://doi.org/10.1177/000348949009900610.CrossRefPubMed

63.

Restivo DA, Palmeri A, Marchese-Ragona R. Botulinum toxin for cricopharyngeal dysfunction in Parkinson’s disease. N Engl J Med. 2002;346:1174–5. https://doi.org/10.1056/NEJM200204113461517.CrossRefPubMed

64.

Restivo DA, Casabona A, Nicotra A, Zappia M, Elia M, Romano MC, Alfonsi E, Marchese-Ragona R. ALS dysphagia pathophysiology: differential botulinum toxin response. Neurology. 2013;80:616–20. https://doi.org/10.1212/WNL.0b013e318281cc1b.CrossRefPubMed

65.

Vaiman M, Eviatar E, Segal S. Evaluation of normal deglutition with the help of rectified surface electromyography records. Dysphagia. 2004;19:125–32. https://doi.org/10.1007/s00455-003-0504-x.CrossRefPubMed

66.

Kahrilas PJ, Logemann JA. Volume accommodation during swallowing. Dysphagia. 1993;8:259–265. https://doi.org/10.1007/BF01354548

67.

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;49:186–93. https://doi.org/10.1044/1092-4388(2006/015).CrossRefPubMed

68.

Weber EH. De pulsu, resorpitione, auditu et tactu. Annotationes anatomicae et physiologicae. Lipsiae, Prostat apud C.F. Koehler; 1834.

69.

Gale MR. Lucretius: De Rerum Natura. Book V: Oxford University Press; 2009.

70.

Cosentino G, Tassorelli C, Prunetti P, Todisco M, De Icco R, Avenali M, Minafra B, Zangaglia R, Valentino F, Pacchetti C, Bertino G, Mauramati S, Fresia M, Alfonsi E. Reproducibility and reaction time of swallowing as markers of dysphagia in parkinsonian syndromes. Clin Neurophysiol. 2020;131:2200–8. https://doi.org/10.1016/j.clinph.2020.06.018.CrossRefPubMed

71.

Cichero J. Swallowing from infancy to old age. In: Cichero JAY, Murdoch BE (eds) Dysphagia. Foundation, theory and practice, vol. 6. Wiley, Chichester; 2006, pp 26–46.

72.

Teismann IK, Warnecke T, Suntrup S, Steinsträter O, Kronenberg L, Ringelstein EB, Dengler R, Petri S, Pantev C, Dziewas R. Cortical processing of swallowing in ALS patients with progressive dysphagia–a magnetoencephalographic study. PLoS One. 2011;6:e19987. https://doi.org/10.1371/journal.pone.0019987.CrossRefPubMedPubMedCentral

73.

Ertekin C. Voluntary versus spontaneous swallowing in man. Dysphagia. 2011;26:183–92. https://doi.org/10.1007/s00455-010-9319-8.CrossRefPubMed

74.

Uludag IF, Tiftikcioglu BI, Ertekin C. Spontaneous swallowing during all-night sleep in patients with Parkinson disease in comparison with healthy control subjects. Sleep. 2016;39:847–54. https://doi.org/10.5665/sleep.5640.CrossRefPubMedPubMedCentral

75.

Cosentino G, Tassorelli C, Prunetti P, Bertino G, De Icco R, Todisco M, Di Marco S, Brighina F, Schindler A, Rondanelli M, Fresia M, Mainardi L, Restivo DA, Priori A, Sandrini G, Alfonsi E. Anodal transcranial direct current stimulation and intermittent theta-burst stimulation improve deglutition and swallowing reproducibility in elderly patients with dysphagia. Neurogastroenterol Motil. 2020;32:e13791. https://doi.org/10.1111/nmo.13791.CrossRefPubMed

76.

Aydogdu I, Tanriverdi Z, Ertekin C. Dysfunction of bulbar central pattern generator in ALS patients with dysphagia during sequential deglutition. Clin Neurophysiol. 2011;122:1219–28. https://doi.org/10.1016/j.clinph.2010.11.002.CrossRefPubMed

Title: Electrokinesiographic Study of Oropharyngeal Swallowing in Neurogenic Dysphagia
Authors: Enrico Alfonsi
Massimiliano Todisco
Mauro Fresia
Cristina Tassorelli
Giuseppe Cosentino
Publication date: 27-07-2021
Publisher: Springer US
Keywords: Electromyographic
Dysphagia
Dysphagia
Dysphagia
Published in: Dysphagia / Issue 2/2023
Print ISSN: 0179-051X
Electronic ISSN: 1432-0460
DOI: https://doi.org/10.1007/s00455-021-10336-x

At a glance: The STEP trials

Springer Medicine

Electrokinesiographic Study of Oropharyngeal Swallowing in Neurogenic Dysphagia

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

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