Introducing a Virtual Lesion Model of Dysphagia Resulting from Pharyngeal Sensory Impairment

NeuroSignals

Volumn 26, Issue 1, 2019, Pages 1-10

  Muhle, Paul ^a   Claus, Inga ^a   Marian, Thomas ^a   Schröder, Jens B ^a   Wollbrink, Andreas ^a   Pantev, Christo ^a   Warnecke, Tobias ^a   Dziewas, Rainer ^a   Suntrup Krueger, Sonja ^a  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

Author keywords

Magnetoencephalography; Neurogenic dysphagia; Pharyngeal hypesthesia; Pneumatic stimulation; Swallowing; Virtual lesion model

Indexed keywords

ADULT; ARTICLE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DYSPHAGIA; EVOKED RESPONSE; FEMALE; HUMAN; HUMAN EXPERIMENT; MAGNETOENCEPHALOGRAPHY; MALE; MOTOR CORTEX; NORMAL HUMAN; PHARYNX; RANDOMIZED CONTROLLED TRIAL; SENSORIMOTOR CORTEX; SENSORY CORTEX; SENSORY STIMULATION; TOPICAL ANESTHESIA; VISCERAL AFFERENT NERVE;

EID: 85063791492     PISSN: 1424862X     EISSN: 14248638     Source Type: Journal    
DOI: 10.1159/000487037     Document Type: Article

References (50)

1. Michou E, Hamdy S: Cortical input in control of swallowing. Curr Opin Otolaryngol Head Neck Surg 2009;17:166-171.
2. Arnold M, Liesirova K, Broeg-Morvay A, Meisterernst J, Schlager M, Mono ML, El-Koussy M, Kagi G, Jung S, Sarikaya H: Dysphagia in Acute Stroke: Incidence, Burden and Impact on Clinical Outcome. PLoS One 2016;11:e0148424.
3. Cabre M, Serra-Prat M, Palomera E, Almirall J, Pallares R, Clave P: Prevalence and prognostic implications of dysphagia in elderly patients with pneumonia. Age Ageing 2010;39:39-45.
4. Geeganage C, Beavan J, Ellender S, Bath PM: Interventions for dysphagia and nutritional support in acute and subacute stroke. Cochrane Database Syst Rev 2012;10:CD000323.
5. Pisegna JM, Kaneoka A, Pearson WG, Jr., Kumar S, Langmore SE: Effects of non-invasive brain stimulation on post-stroke dysphagia: A systematic review and meta-analysis of randomized controlled trials. Clin Neurophysiol 2016;127:956-968.
6. Scutt P, Lee HS, Hamdy S, Bath PM: Pharyngeal Electrical Stimulation for Treatment of Poststroke Dysphagia: Individual Patient Data Meta-Analysis of Randomised Controlled Trials. Stroke Res Treat 2015;2015:429053.
7. Teismann IK, Steinstraeter O, Stoeckigt K, Suntrup S, Wollbrink A, Pantev C, Dziewas R: Functional oropharyngeal sensory disruption interferes with the cortical control of swallowing. BMC Neurosci 2007;8:62.
8. Chee C, Arshad S, Singh S, Mistry S, Hamdy S: The influence of chemical gustatory stimuli and oral anaesthesia on healthy human pharyngeal swallowing. Chem Senses 2005;30:393-400.
9. Mansson I, Sandberg N: Effects of surface anesthesia on deglutition in man. Laryngoscope 1974;84:427-437.
10. Ertekin C, Kiylioglu N, Tarlaci S, Keskin A, Aydogdu I: Effect of mucosal anaesthesia on oropharyngeal swallowing. Neurogastroenterol Motil 2000;12:567-572.
11. Suntrup S, Kemmling A, Warnecke T, Hamacher C, Oelenberg S, Niederstadt T, Heindel W, Wiendl H, Dziewas R: The impact of lesion location on dysphagia incidence, pattern and complications in acute stroke. Part 1: dysphagia incidence, severity and aspiration. Eur J Neurol 2015;22:832-838.
12. Macht M, Wimbish T, Bodine C, Moss M: ICU-acquired swallowing disorders. Crit Care Med 2013;41:2396-2405.
13. Mistry S, Verin E, Singh S, Jefferson S, Rothwell JC, Thompson DG, Hamdy S: Unilateral suppression of pharyngeal motor cortex to repetitive transcranial magnetic stimulation reveals functional asymmetry in the hemispheric projections to human swallowing. J Physiol 2007;585:525-538.
14. Jayasekeran V, Singh S, Tyrrell P, Michou E, Jefferson S, Mistry S, Gamble E, Rothwell J, Thompson D, Hamdy S: Adjunctive functional pharyngeal electrical stimulation reverses swallowing disability after brain lesions. Gastroenterology 2010;138:1737-1746.
15. Teismann IK, Steinstraeter O, Warnecke T, Ringelstein EB, Pantev C, Dziewas R: Measurement of pharyngeal sensory cortical processing: Technique and physiologic implications. BMC Neurosci 2009;10:76.
16. Voss RF, Clarke J: 1/f noise' in music and speech. Nature 1975;258:317-318.
17. Suntrup S, Teismann I, Wollbrink A, Winkels M, Warnecke T, Pantev C, Dziewas R: Pharyngeal electrical stimulation can modulate swallowing in cortical processing and behavior-magnetoencephalographic evidence. Neuroimage 2015;104:117-124.
18. Dziewas R, Teismann IK, Suntrup S, Schiffbauer H, Steinstraeter O, Warnecke T, Ringelstein EB, Pantev C: Cortical compensation associated with dysphagia caused by selective degeneration of bulbar motor neurons. Hum Brain Mapp 2009;30:1352-1360.
19. Suntrup S, Teismann I, Bejer J, Suttrup I, Winkels M, Mehler D, Pantev C, Dziewas R, Warnecke T: Evidence for adaptive cortical changes in swallowing in Parkinson's disease. Brain 2013;136:726-738.
20. Teismann IK, Warnecke T, Suntrup S, Steinstrater 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.
21. Oostenveld R, Fries P, Maris E, Schoffelen JM: FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011;2011:156869.
22. Pfurtscheller G: Functional brain imaging based on ERD/ERS. Vision Res 2001;41:1257-1260.
23. Nolte G: The magnetic lead field theorem in the quasi-static approximation and its use for magnetoencephalography forward calculation in realistic volume conductors. Phys Med Biol 2003;48:3637-3652.
24. Suntrup S, Teismann I, Wollbrink A, Winkels M, Warnecke T, Floel A, Pantev C, Dziewas R: Magnetoencephalographic evidence for the modulation of cortical swallowing processing by transcranial direct current stimulation. Neuroimage 2013;83:346-354.
25. Maris E, Oostenveld R: Nonparametric statistical testing of EEG-and MEG-data. J Neurosci Methods 2007;164:177-190.
26. Teismann IK, Dziewas R, Steinstraeter O, Pantev C: Time-dependent hemispheric shift of the cortical control of volitional swallowing. Hum Brain Mapp 2009;30:92-100.
27. Lowell SY, Poletto CJ, Knorr-Chung BR, Reynolds RC, Simonyan K, Ludlow CL: Sensory stimulation activates both motor and sensory components of the swallowing system. Neuroimage 2008;42:285-295.
28. Small DM: Taste representation in the human insula. Brain Struct Funct 2010;214:551-561.
29. Hagen MC, Zald DH, Thornton TA, Pardo JV: Somatosensory processing in the human inferior prefrontal cortex. J Neurophysiol 2002;88:1400-1406.
30. Furlong PL, Hobson AR, Aziz Q, Barnes GR, Singh KD, Hillebrand A, Thompson DG, Hamdy S: Dissociating the spatio-temporal characteristics of cortical neuronal activity associated with human volitional swallowing in the healthy adult brain. Neuroimage 2004;22:1447-1455.
31. Rolls ET: The functions of the orbitofrontal cortex. Brain Cogn 2004;55:11-29.
32. Yoshida Y, Tanaka Y, Hirano M, Nakashima T: Sensory innervation of the pharynx and larynx. Am J Med 2000;108:51S-61S.
33. Szurhaj W, Bourriez JL, Kahane P, Chauvel P, Mauguiere F, Derambure P: Intracerebral study of gamma rhythm reactivity in the sensorimotor cortex. Eur J Neurosci 2005;21:1223-1235.
34. Jafari S, Prince RA, Kim DY, Paydarfar D: Sensory regulation of swallowing and airway protection: A role for the internal superior laryngeal nerve in humans. J Physiol 2003;550:287-304.
35. Aviv JE: Clinical assessment of pharyngolaryngeal sensitivity. Am J Med 2000;108:68S-72S.
36. Gross J, Schnitzler A, Timmermann L, Ploner M: Gamma oscillations in human primary somatosensory cortex reflect pain perception. PLoS Biol 2007;5:e133.
37. Sulica L, Hembree A, Blitzer A: Swallowing and sensation: evaluation of deglutition in the anesthetized larynx. Ann Otol Rhinol Laryngol 2002;111:291-294.
38. Aviv JE, Martin JH, Sacco RL, Zagar D, Diamond B, Keen MS, Blitzer A: Supraglottic and pharyngeal sensory abnormalities in stroke patients with dysphagia. Ann Otol Rhinol Laryngol 1996;105:92-97.
39. 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;103:749-752.
40. Mortelliti AJ, Malmgren LT, Gacek RR: Ultrastructural changes with age in the human superior laryngeal nerve. Arch Otolaryngol Head Neck Surg 1990;116:1062-1069.
41. Wirth R, Dziewas R, Beck AM, Clave P, Hamdy S, Heppner HJ, Langmore S, Leischker AH, Martino R, Pluschinski P, Rosler A, Shaker R, Warnecke T, Sieber CC, Volkert D: Oropharyngeal dysphagia in older persons-from pathophysiology to adequate intervention: A review and summary of an international expert meeting. Clin Interv Aging 2016;11:189-208.
42. Onofri SM, Cola PC, Berti LC, da Silva RG, Dantas RO: Correlation between laryngeal sensitivity and penetration/aspiration after stroke. Dysphagia 2014;29:256-261.
43. Marian T, Schroder JB, Muhle P, Claus I, Riecker A, Warnecke T, Suntrup-Krueger S, Dziewas R: Pharyngolaryngeal Sensory Deficits in Patients with Middle Cerebral Artery Infarction: Lateralization and Relation to Overall Dysphagia Severity. Cerebrovasc Dis Extra 2017;7:130-139.
44. Muhle P, Suntrup-Krueger S, Bittner S, Ruck T, Claus I, Marian T, Schroder JB, Minnerup J, Warnecke T, Meuth SG, Dziewas R: Increase of Substance P Concentration in Saliva after Pharyngeal Electrical Stimulation in Severely Dysphagic Stroke Patients-an Indicator of Decannulation Success Neurosignals 2017;25:74-87.
45. Ebihara T, Sekizawa K, Nakazawa H, Sasaki H: Capsaicin and swallowing reflex. Lancet 1993;341:432.
46. Ebihara T, Takahashi H, Ebihara S, Okazaki T, Sasaki T, Watando A, Nemoto M, Sasaki H: Capsaicin troche for swallowing dysfunction in older people. Journal of the American Geriatrics Society 2005;53:824-828.
47. Ebihara S, Kohzuki M, Sumi Y, Ebihara T: Sensory stimulation to improve swallowing reflex and prevent aspiration pneumonia in elderly dysphagic people. Journal of pharmacological sciences 2011;115:99-104.
48. Rofes L, Arreola V, Martin A, Clave P: Natural capsaicinoids improve swallow response in older patients with oropharyngeal dysphagia. Gut 2013;62:1280-1287.
49. Ortega O, Rofes L, Martin A, Arreola V, Lopez I, Clave P: A Comparative Study Between Two Sensory Stimulation Strategies After Two Weeks Treatment on Older Patients with Oropharyngeal Dysphagia. Dysphagia 2016;31:706-716.
50. Fraser C, Rothwell J, Power M, Hobson A, Thompson D, Hamdy S: Differential changes in human pharyngoesophageal motor excitability induced by swallowing, pharyngeal stimulation, and anesthesia. Am J Physiol Gastrointest Liver Physiol 2003;285:G137-144.