Neurogenic Dysphagia in Brainstem Disorders and EMG Evaluation

Neurogenic dysphagia is a prevalent condition that may result in serious complications. Screening and follow up are critical for early diagnosis, prognosis and management which can mitigate its complications and be cost-saving. Several Neurophysiological methods are described to evaluate the Neurogenic Dysphagia including Single Bolus Analysis, Dysphagia Limit, Cricopharyngeal sphinter electromyogram EMG , Continuous water swallowing with respiratory recording, Polygraphic recording for spontaneous swallows in awake and sleeping states. All techniques mentioned above were developed in our laboratory. Brain stem disorders are particularly important to investigate the presence of dysphagia due to its high incidence and also its severity. These swallowing methods presented and discussed in this review are reliable, cheap and easy applicable quantitative tests to detect and to follow up both subclinical and clinical dysphagia

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  • Ertekin C, Aydogdu I. Neurophysiology of swallowing. Clin Neuro- physiol 2003; 114:2226-2244. [CrossRef]
  • Ertekin C. Electrophysiological evaluation of oropharyngeal dys- phagia in Parkinson’s disease. J Mov Disord 2014; 7:31-56. [CrossRef]
  • Jean A. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev 2001; 81:929-969.
  • Ertekin C. Electrophysiological techniques to evaluate swallowing in central and peripheral nervous system disorders. J Clin Neuro- physiol 2015; 32:314-323. [CrossRef]
  • Hughes TA, Wiles CM. Neurogenic dysphagia: the role of the neu- rologist. J Neurol Neurosurg Psychiatry 1998; 64: 569-572. [CrossRef]
  • Logemann JA. Evaluation and treatment of swallowing disorders. 2nd ed. Austin, TX: Pro-ed publishers, 1998.
  • Aydogdu I, Kiylioglu N, Tarlaci S, et al. Diagnostic value of “dyspha- gia limit” for neurogenic dysphagia: 17 years of experience in 1278 adults. Clin Neurophysiol 2015; 126:634-643. [CrossRef]
  • Humbert IA, Robbins J. Normal swallowing and functional magnetic resonance imaging: a systematic review. Dysphagia 2007; 22:266- 275. [CrossRef]
  • Ertekin C, Aydogdu I, Yüceyar N, et al. Electrodiagnostic methods for neurogenic dysphagia. Electroencephalogr Clin Neurophysiol 1998; 109:331-340. [CrossRef]
  • Pena MJ, Ravasco P, Machado M, et al. What is relevance of percu- taneous endoscopic gastrostomy on the survival of patients with amyotrophic lateral sclerosis. Amyotroph Lateral Scler 2012; 13: 550- 554. [CrossRef]
  • Logemann JA. Evaluation and treatment of swallowing disorders. San Diego: College Hill Press, 1983.
  • Ramsey D, Smithard D, Kalra L. Silent aspiration: what do we know? Dysphagia 2005; 20:218-225. [CrossRef]
  • Stoeckli SJ, Huisman TA, Seifert B, Martin-Harris BJ. Interrater re- liability of videofluoroscopic swallow evaluation. Dysphagia 2003; 18:53-57. [CrossRef]
  • Ertekin C, Pehlivan M, Aydoğdu I, et al. An electrophysiological in- vestigation of deglutition in man. Muscle Nerve 1995; 18:1177-1186. [CrossRef]
  • Ertekin C, Aydoğdu I, Yüceyar N. Piecemeal deglutition and dyspha- gia limit in normal subjects and in patients with swallowing disor- der. J Neurol Neurosurg Psychiatry 1996; 61:491-496. [CrossRef]
  • Aydogdu I, Tanriverdi Z, Ertekin C. Dysfunction of bulbar central pat- tern generator in ALS patients with dysphagia during sequential deglutition. Clin Neurophysiol 2011; 122:1219-1228. [CrossRef]
  • Jean A. Brainstem organization of the swallowing network. Brain Behav Evol 1984; 25:109-16. [CrossRef]
  • Jean A. Control of the central swallowing program by inputs from the principal receptors. A review. J Auton Nerv Syst 1984; 10:225-233. [CrossRef]
  • Bieger D. Rhomboncephalic pathways and neurotransmitters con- trolling deglutition. Am J Med 2001; 111:85S-89S. [CrossRef]
  • Kessler JP, Jean A. Identification of the medullary swallowing re- gions in the rat. Exp Brain Res 1985; 57:256-263.
  • Jean A, Car A, Roman C. Comparison of activity in pontine versus medullary neurons during swallowing. Exp Brain Res 1975; 22:211-220. [CrossRef]
  • Jean A, Dallaporta M. Electrophysiologic characterization of the swal- lowing pattern generator in the brainstem. GI Motility 2006; 9:1-37.
  • Umezaki T, Matsuse T, Shin T. Medullary swallowing-related neurons in the anesthetized cat. Neuroreport 1998; 9:1793-1798. [CrossRef]
  • Aydogdu I, Ertekin C, Tarlaci S, Turman B, Kiylioglu N, Secil Y. Dys- phagia in lateral medullary infarction (Wallenberg’s syndrome): an acute disconnection syndrome in premotor neurons related to swallowing activity? Stroke 2001; 32:2081-2087. [CrossRef]
  • Miller AJ. The neuroscientific principles of swallowing and dyspha- gia. San Diego: Singular Publishing Group, 1999.
  • Jean A, Car A. Inputs to swallowing medullary neurons from the peripheral afferent fibers and swallowing cortical area. Brain Res 1979; 178: 567-572. [CrossRef]
  • Ertekin C. Voluntary versus spontaneous swallowing in man. Dys- phagia 2011; 26:183-192. [CrossRef]
  • Thexton AJ, Crompton AW, German RZ. Electromyographic activity during the reflex pharyngeal swallow in the pig: Doty and Bosma (1956) revisited. J Appl Physiol 2007; 102:587-600. [CrossRef]
  • Nishino T. Physiological and pathophysiological implications of upper airway reflexes in humans. Jpn J Physiol 2000; 50:3-14. [CrossRef]
  • Lang IM. Brain stem control of the phases of swallowing. Dysphagia 2009; 24:333-348. [CrossRef]
  • Pehlivan M, Yüceyar N, Ertekin C, et al. An electronic device measur- ing the frequency of spontaneous swallowing: digital phagometer. Dysphagia 1996; 11:259-264. [CrossRef]
  • Ertekin C, Eryasar G, Gürgör N, Arıcı S, Secil Y, Kurt T. Orbicularis oculi muscle activation during swallowing in humans. Exp Brain Res 2013; 224:79-91. [CrossRef]
  • 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; 49:186-193. [CrossRef]
  • Crary MA, Sura L, Carnaby G. Validation and demonstration of an isolated acoustic recording technique to estimate spontaneous swallow frequency. Dysphagia 2013; 28:86-94. [CrossRef]
  • Dua K, Surapaneni SN, Kuribayashi S, Hafeezullah M, Shaker R. Pro- tective role of aerodigestive reflexes against aspiration: study on subjects with impaired and preserved reflexes. Gastroenterology 2011; 140:1927-1933. [CrossRef]
  • Lund JP. Mastication and its control by the brain stem. Crit Rev Oral Biol Med 1991; 2: 33-64. [CrossRef]
  • Tsuboi A, Kolta A, Chen CC, Lund JP. Neurons of the trigeminal main sensory nucleus participate in the generation of rhythmic motor patterns. Eur J Neurosci 2003; 17: 229-238. [CrossRef]
  • Ertekin C, Aydogdu I, Yüceyar N, et al. Effects of bolus volumes on the oropharyngeal swallowing: an electrophysiological study in man. Am J Gastroenterol 1997; 92:2049-2053.
  • Perlman AL. Electromyography and the study of oropharyngeal swallowing. Dysphagia 1993; 8:351-355. [CrossRef]
  • Chi-Fishman G, Stone M, McCall GN. Lingual action in normal sequen- tial swallowing. J Speech Lang Hear Res 1998; 41:771-785. [CrossRef]
  • Steele CM, Van Lieshout P. Tongue movements during water swal- lowing in healthy young and older adults. J Speech Lang Hear Res 2009; 52:1255-1267. [CrossRef]
  • Ertekin C, Aydogdu I. Electromyography of the cricopharyngeal muscle of the upper esophageal sphincter. Muscle Nerve 2002; 26:729-739. [CrossRef]
  • Ertekin C, Celik M, Secil Y, Tarlaci S, Kiylioğlu N, Aydoğdu I. The elec- tromyographic behaviour of the thyroarytenoid muscle during swallowing. J Clin Gastroenterol 2000; 30:274-280. [CrossRef]
  • Kruger E, Teasell R, Salter K, Foley N, Hellings C. The rehabilitation of patients recovering from brainstem strokes: case studies and clini- cal considerations. Top Stroke Rehabil 2007; 14: 56-64. [CrossRef]
  • Aydogdu I, Yuceyar N, Kiylioglu N, et al. Physiological changes in oropharyngeal swallowing with age: an electrophysiological study. J Neurol Sci Turk 2007; 24:144-155.
  • Teasell RW, Bach D, McRae M. Prevalence and recovery of aspira- tion poststroke: a retrospective analysis. Dysphagia 1994; 9:35-39. [CrossRef]
  • Finestone HM, Teasel RW, Heitzner J. Case study of dysphagia and aspiration following a brainstem stroke. Topics in stroke rehabilita- tion 1999; 6:41-45. [CrossRef]
  • Oshima F, Yokozeki M, Hamanaka M, et al. Predilection of dyspha- gia severity: An investigation of the dysphagia patterns in pa- tients with lateral medullary infarction. Intern Med 2013; 52:1325- 1331. [CrossRef]
  • Kwon M, Lee JH, Kim JS. Dysphagia in unilateral medullary in- farction: lateral vs medial lesions. Neurology 2005; 65:714-718. [CrossRef]
  • Kim JS. Pure lateral medullary infarction: clinical-radiological cor- relation of 130 acute, consecutive patients. Brain 2003; 126:1864-1872. [CrossRef]
  • Beckmann Y et al: Acute transient dysphagia in brain stem infarc- tion 2016(Unpublished)
  • Huckabee ML, Prosiegel M. Wallenberg syndrome (WS). In: Jones HN, Rosenbek JC, eds. Dysphagia in rare conditions. An Encyclope- dia. 1st ed. San Diego: Plural Publishing; 2010: 639-646.
  • Paliwal VK, Kalita J, Misra UK. Dysphagia in a patient with bilateral medial medullary infarcts. Dysphagia 2009; 24:349-353. [CrossRef]
  • Kim SJ, Lee JH, Im JH, Lee MC. Syndromes of pontine base infarc- tion. A clinical-radiological correlation study. Stroke 1995; 26:950-955. [CrossRef]
  • Aviv JE, Sacco RL, Thomson J, et al. Silent laryngopharyngeal sen- sory deficits after stroke. Ann Otol Rhinol Laryngol 1997; 106:87-93. [CrossRef]
  • Seçil Y, Aydogdu I, Ertekin C. Peripheral facial palsy and dysfunction of the oropharynx. J Neurol Neurosurg Psychiatry 2002; 72:391-393. [CrossRef]
  • Daniels SK, Foundas AL. Swallowing physiology of sequential straw drinking. Dysphagia 2001; 16:176-182. [CrossRef]
  • Lederle A, Hoit J, Barkmeier-Kraemer J. Effect of sequential swal- lowing on drive to breathe in young, healthy adults. Dysphagia 2012; 27:221-227. [CrossRef]
  • Chi-Fishman G, Sonies BC. Motor strategy in rapid sequential swal- lowing: new insights. J Speech Lang Hear Res 2000; 43:1481-1492. [CrossRef]
  • Hughes TA, Wiles CM. Clinical measurement of swallowıing in health and in neurogenic dysphagia. QJM 1996; 89: 109-116. [CrossRef]
  • Suiter DM, Leder SB. Clinical utility of the 3-ounce water swallowing test. Dysphagia 2008; 23:244-250. [CrossRef]
  • Daniels SK, Corey DM, Hadskey LD, Legendre C, Priestly DH, Rosen- bek JC, et al. Mechanism of sequential swallowing during straw drinking in healthy young and older adults. J Speech Lang Hear Res 2004; 47:33-45. [CrossRef]
  • Gürgör N, Arıcı Ş, Kurt Incesu T, Seçil Y, Tokuçoğlu F, Ertekin C. An electrophysiological study of the sequential water swallowing. J Electromyogr Kinesiol 2013; 23:619-626. [CrossRef]
  • Beckmann Y, Gürgör N, Çakır A, et al. Electrophysiological eval- uation of dysphagia in the mild or moderate patients with multi- ple sclerosis: a concept of subclinical dysphagia. Dysphagia 2015; 30:296-303. [CrossRef]
  • Dozier TS, Brodsky MB, Michel Y, Walters BC Jr, Martin-Harris B. Co- ordination of swallowing and respiration in normal sequential cup swallowing. Laryngoscope 2006; 116:1489-1493.
  • Umemoto G, Tsuboi Y, Kitashima A, Furuya H, Kikuta T. Impaired food transportation in Parkinson’s disease related to lingual bradykine- sia. Dysphagia 2011; 26:250-255. [CrossRef]
  • Donovan NJ, Daniels SK, Edmiaston J, et al. Dysphagia screening: state of the art: invitational conference proceeding from the State- of-the-Art Nursing Symposium, International Stroke Conference 2012. Stroke 2013; 44:e24-31. [CrossRef]
  • Ince PG, Wharton SB. Cytopathology of the motor neuron. In: Eisen A, editor. Clinical neurophyisology of motor neuron disease. Am- sterdam: Elsevier; 2004. p.149-168. [CrossRef]
  • Eisen A, Krieger C. Classic charcot amyotrophic lateral sclerosis. In: Eisen A, editor. Clinical neurophysiology of motor neuron disease. Amsterdam: Elsevier; 2004. p.469-488. [CrossRef]
  • Zang DW, Yang Q, Wang HX, Egan G, Lopes EC, Cheema SS. Mag- netic resonance imaging reveals neuronal degeneration in the brainstem of the superoxide dismutase 1 transgenic mouse model of amyotrophic lateral sclerosis. Eur J Neurosci 2004; 20:1745-1751. [CrossRef]
  • Angenstein F, Niessen HG, Goldschmidt J, Vielhaber S, Ludolph AC, Scheich H. Age-dependent changes in MRI of motor brain stem nuclei in a mouse model of ALS. Neuroreport 2004; 15:2271-2274. [CrossRef]
  • Le Forestier N, Maisonobe T, Piquard A, et al. Does primary lateral sclerosis exist? A study of 20 patients and a review of literature. Brain 2001; 124:1989-1999. [CrossRef]
  • German RZ, Crompton AW, Thexton AJ. Integration of the reflex pharyngeal swallow into rhythmic oral activity in a neurologically intact pig model. J Neurophysiol 2009; 102:1017-1025. [CrossRef]
  • Ertekin C, Aydogdu I, Yüceyar N, Kiylioglu N, Tarlaci S, Uludag B. Pathophysiological mechanism of oropharyngeal dysphagia in amyotrophic lateral sclerosis. Brain 2000; 123:125-140. [CrossRef]
  • Afkari S. Measuring frequency of spontaneous swallowing. Aus- tralas Phys Eng Sci Med 2007; 30:313-317.
  • Uludag IF, Tiftikcioglu BI, Ertekin C. Spontaneous swallowing during all night sleep in patients with Parkinson disease in comparison to healthy control subjects. Sleep 2016; 39:847-854. [CrossRef]
  • Dergachyov O, Guttermann LA, Mareev DV, Burikov AA Swallowing motions in man during sleep. Sleep Res 1997; 26:195.
  • Sato K, Nakashima T. Human adult deglutition during sleep. Ann Otol Rhinol Laryngol 2006; 115:334-339. [CrossRef]
  • Thach BT. Can we breathe and swallow at the same time? J Appl Physiol (1985) 2005; 99:1633.
  • Zerari-Mailly F, Buisseret P, Buisseret-Delmas C, Nosjean A. Trigem- ino-solitarii-facial pathways in rat. J Comp Neurol 2005; 487:176-189 [CrossRef]