Motorkortikale Reorganisation bei Dysphagie nach Schlaganfall

Zusammenfassung

Das Schlucken ist eine lebenswichtige motorische Funktion, dessen zentralnervöse Steuerung in den letzten beiden Jahrzehnten zunehmend aufgeklärt wurde. Neben der lange bekannten Bedeutung medullärer Strukturen konnte die Beteiligung eines ausgedehnten bilateralen, kortikalen und subkortikalen Netzwerkes nachgewiesen und die Funktion einzelner Hirnareale definierten Teilaspekten des Schluckaktes zugeordnet werden.

Häufigste Ursache einer gestörten Schluckfunk­tion ist der Schlaganfall. Die Dysphagie tritt mit einer Inzidenz von etwa 50% auf und geht infolge von Aspirationspneumonien mit einer erhöhten Mortalität einher. Während etwa 15% der Patienten an einer persistierenden Dysphagie leiden, weist die Mehrzahl der Betroffenen einen günstigen Spontanverlauf mit einer Erholung der Schluckfunktion binnen weniger Tage bis Wochen auf. Der Hirninfarkt stellt somit ein geeignetes Läsions-Studienmodell zur Beobachtung funktioneller Restitution infolge neuronaler Plastizität im Spontanverlauf sowie als Folge therapeutischer Interventionen dar. So basiert die bemerkenswerte Funktionserholung überwiegend auf einer adaptiven Reorganisation in schluckrelevanten Arealen der gesunden Hemisphäre. In den Fokus therapeutischer Studien treten daher anstelle herkömmlicher Praktiken zur Beeinflussung der Biomechanik zunehmend Verfahren, welche eine Modulation der zugrunde liegenden neuronalen Netzwerke zum Ziel haben. Über eine Beeinflussung des kortikalen Erregbarkeits- und Aktivitätsniveaus sollen sie eine strukturelle und funktionelle Reorganisation forcieren, die klinisch als Funktionsverbesserung sichtbar ist. Von Interesse sind kortikale Stimulationsverfahren wie die transkranielle Magnet- oder Gleichstromstimulation, aber auch peripher ansetzende Methoden wie die elektrische Pharynxstimulation. Einige dieser Verfahren haben einen methodischen Entwicklungsstand erreicht, der ihre Anwendung im klinischen Kontext zunehmend denkbar erscheinen lässt. Entscheidend hierfür wird eine Verbesserung von Effektstärke und Wirkdauer durch weitere Optimierung der Stimulationsprotokolle sein.

Abstract

Swallowing is an essential part of life, whose central neural processing has increasingly been explored over the last 2 decades. Besides the well-known significance of medullary structures, involvement of a bilateral, widely distributed cortical and subcortical network has been shown. Moreover, the role of distinct brain areas could be related to specific aspects of swallowing control.

Stroke is the most frequent reason for swallowing dysfunction. Dysphagia in stroke has a reported incidence of approximately 50% and is associated with increased mortality due to aspiration pneumonia. While 15% of patients suffer from persistent dysphagia, the majority shows fast recovery of swallow function within days to weeks. Thus, stroke constitutes a convenient lesion model to evaluate functional recovery due to spontaneous neuronal plasticity and following therapeutic interventions. The remarkable recovery of stroke-related dysphagia depends on compensatory reorganization in the undamaged hemisphere. The focus of treatment studies is therefore shifting from exercise-based manipulation of swallowing biomechanics towards approaches that modulate the underlying neural systems. By influencing cortical excitability and activity levels these methods are said to promote structural and functional reorganization resulting in clinical improvement. Techniques include those applied to the cortex like transcranial magnetic or direct current stimulation, but also those applied to the periphery, such as pharyngeal electrical stimulation. Some of these techniques have reached a stage of development that makes future use in clinical practice conceivable. Increasing the effect size and duration by further optimizing stimulation protocols will be a crucial issue.

Schlüsselwörter

Schlaganfall - Dysphagie - neuronale Plastizität - Neuromodulation

Key words

stroke - dysphagia - neuronal plasticity - neuromodulation

• Literatur

• 1 Dodds WJ, Stewart ET, Logemann JA. Physiology and radiology of the normal oral and pharyngeal phases of swallowing. AJR Am J Roentgenol 1990; 154: 953-963
• 2 Donner MW, Bosma JF, Robertson DL. Anatomy and physiology of the pharynx. Gastrointest Radiol 1985; 10: 196-212
• 3 Jean A. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev 200; 81: 929-969
• 4 Hamdy S, Aziz Q, Rothwell JC et al. The cortical topography of human swallowing musculature in health and disease. Nature Medicine 1996; 2: 1217-1224
• 5 Hamdy S, Mikulis DJ, Crawley A et al. Cortical activation during human volitional swallowing: an event-related fMRI study. Am J Physiol 1999; 277 ((1 Pt1) G219-G225
• 6 Hamdy S, Rothwell JC, Brooks DJ et al. Identification of the cerebral loci processing human swallowing with H2(15)O PET activation. J Neurophysiol 1999; 81: 1917-1926
• 7 Zald DH, Pardo JV. The functional neuroanatomy of voluntary swallowing. Ann Neurol 1999; 46: 281-286
• 8 Martin RE, Goodyear BG, Gati JS et al. Cerebral cortical representation of automatic and volitional swallowing in humans. J Neurophysiol 2001; 85: 938-950
• 9 Dziewas R, Soros P, Ishii R et al. Neuroimaging evidence for cortical involvement in the preparation and in the act of swallowing. Neuro­image 2003; 20: 135-144
• 10 Furlong PL, Hobson AR, Aziz Q et al. Dissociating the spatio-temporal characteristics of cortical neuronal activity associated with human volitional swallowing in the healthy adult brain. Neuroimage 2004; 22: 1447-1455
• 11 Teismann IK, Dziewas R, Steinstraeter O et al. Time-dependent hemispheric shift of the cortical control of volitional swallowing. Hum Brain Mapp 2009; 30: 92-100
• 12 Teismann IK, Steinstraeter O, Schwindt W et al. Age-related changes in cortical swallowing processing. Neurobiol Aging 2010; 31: 1044-1050
• 13 Leopold NA, Daniels SK. Supranuclear control of swallowing. Dysphagia 2010; 25: 250-257
• 14 Martin R, Barr A, MacIntosh B et al. Cerebral cortical processing of swallowing in older adults. Exp Brain Res 2007; 176: 12-22
• 15 Mistry S, Verin E, Singh S et al. 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 ((Pt 2) 525-538
• 16 Mistry S, Michou E, Rothwell J et al. Remote effects of intermittent theta burst stimulation of the human pharyngeal motor system. Eur J Neurosci 2012; 36: 2493-2499
• 17 Malandraki GA, Sutton BP, Perlman AL et al. Age-related differences in laterality of cortical activations in swallowing. Dysphagia 2010; 25: 238-249
• 18 Martino R, Foley N, Bhogal S et al. Dysphagia after stroke: incidence, diagnosis, and pulmonary complications. Stroke 2005; 36: 2756-2763
• 19 Davalos A, Ricart W, Gonzalez-Huix F et al. Effect of malnutrition after acute stroke on clinical outcome. Stroke 1996; 27: 1028-1032
• 20 Ickenstein GW, Stein J, Ambrosi D et al. Predictors of survival after severe dysphagic stroke. J Neurol 2005; 252: 1510-1516
• 21 Smithard DG, Smeeton NC, Wolfe CD. Long-term outcome after stroke: does dysphagia matter?. Age Ageing 2007; 36: 90-94
• 22 Warnecke T, Teismann I, Meimann W et al. Assessment of aspiration risk in acute ischaemic stroke – evaluation of the simple swallowing provocation test. J Neurol Neurosurg Psychiatry 2008; 79: 312-314
• 23 Riecker A, Gastl R, Kuhnlein P et al. Dysphagia due to unilateral infarction in the vascular territory of the anterior insula. Dysphagia 2009; 24: 114-118
• 24 Suntrup S, Warnecke T, Kemmling A et al. Dysphagia in patients with acute striatocapsular hemorrhage. J Neurol 2012; 259: 93-99
• 25 Weller M. Anterior opercular cortex lesions cause dissociated lower cranial nerve palsies and anarthria but no aphasia: Foix-Chavany-Marie syndrome and “automatic voluntary dissociation” revisited. J Neurol 1993; 240: 199-208
• 26 Steinhagen V, Grossmann A, Benecke R et al. Swallowing disturbance pattern relates to brain lesion location in acute stroke patients. Stroke 2009; 40: 1903-1906
• 27 Daniels SK, Foundas AL, Iglesia GC et al. Lesion site in unilateral stroke patients with dysphagia. J Stroke Cerebrovasc Dis 1996; 6: 30-34
• 28 Daniels SK, Corey DM, Fraychinaud A et al. Swallowing lateralization: the effects of modified dual-task interference. Dysphagia 2006; 21: 21-27
• 29 Robbins J, Levine RL, Maser A et al. Swallowing after unilateral stroke of the cerebral cortex. Arch Phys Med Rehabil 1993; 74: 1295-1300
• 30 Mann G, Hankey GJ, Cameron D. Swallowing function after stroke: prognosis and prognostic factors at 6 months. Stroke 1999; 30: 744-748
• 31 Smithard DG, O’Neill PA, Parks C et al. Complications and outcome after acute stroke. Does dysphagia matter?. Stroke 1996; 27: 1200-1204
• 32 Smithard DG, O’Neill PA, England RE et al. The natural history of dysphagia following a stroke. Dysphagia 1997; 12: 188-193
• 33 Prosiegel M, Holing R, Heintze M et al. Swallowing therapy – a prospective study on patients with neurogenic dysphagia due to unilateral paresis of the vagal nerve, Avellis’ syndrome, Wallenberg’s syndrome, posterior fossa tumours and cerebellar hemorrhage. Acta Neurochir Suppl 2005; 93: 35-37
• 34 Teismann IK, Suntrup S, Warnecke T et al. Cortical swallowing processing in early subacute stroke. BMC Neurol 2011; 11: 34
• 35 Saur D, Lange R, Baumgaertner A et al. Dynamics of language reorganization after stroke. Brain 2006; 129 ((Pt 6) 1371-1384
• 36 Nelles G. Cortical reorganization – effects of intensive therapy. Restor Neurol Neurosci 2004; 22: 239-244
• 37 Hamdy S, Aziz Q, Rothwell JC et al. Explaining oropharyngeal dysphagia after unilateral hemispheric stroke. Lancet 1997; 350: 686-692
• 38 Hamdy S, Aziz Q, Rothwell JC et al. Recovery of swallowing after dysphagic stroke relates to functional reorganization in the intact motor cortex. Gastroenterology 1998; 115: 1104-1112
• 39 Muellbacher W, Artner C, Mamoli B. The role of the intact hemisphere in recovery of midline muscles after recent monohemispheric stroke. J Neurol 1999; 246: 250-256
• 40 Li S, Luo C, Yu B et al. Functional magnetic resonance imaging study on dysphagia after unilateral hemispheric stroke: a preliminary study. J Neurol Neurosurg Psychiatry 2009; 80: 1320-1329
• 41 Foltys H, Krings T, Meister IG et al. Motor representation in patients rapidly recovering after stroke: a functional magnetic resonance imaging and transcranial magnetic stimulation study. Clin Neurophysiol 2003; 114: 2404-2415
• 42 Suntrup S, Meisel A, Dziewas R et al. Dysphagia diagnostics and therapy of acute stroke: Federal survey of certified stroke units. Nervenarzt 2012; 83: 1619-1624
• 43 Carnaby G, Hankey GJ, Pizzi J. Behavioural intervention for dysphagia in acute stroke: a randomised controlled trial. Lancet Neurol 2006; 5: 31-37
• 44 Ertekin C, Kiylioglu N, Tarlaci S et al. Effect of mucosal anaesthesia on oropharyngeal swallowing. Neurogastroenterol Motil 2000; 12: 567-572
• 45 Chee C, Arshad S, Singh S et al. The influence of chemical gustatory stimuli and oral anaesthesia on healthy human pharyngeal swallowing. Chem Senses 2005; 30: 393-400
• 46 Teismann IK, Steinstraeter O, Stoeckigt K et al. Functional oropharyngeal sensory disruption interferes with the cortical control of swallowing. BMC Neurosci 2007; 8: 62
• 47 Fraser C, Rothwell J, Power M et al. Differential changes in human pharyngoesophageal motor excitability induced by swallowing, pharyngeal stimulation, and anesthesia. Am J Physiol Gastrointest Liver Physiol 2003; 285: G137-G144
• 48 Lowell SY, Poletto CJ, Knorr-Chung BR et al. Sensory stimulation activates both motor and sensory components of the swallowing system. Neuroimage 2008; 42: 285-295
• 49 Pommerenke W. A study of the sensory areas eliciting the swallowing reflex. Am J Physiol 1927; 84: 36-41
• 50 Rosenbek JC, Roecker EB, Wood JL et al. Thermal application reduces the duration of stage transition in dysphagia after stroke. Dysphagia 1996; 11: 225-233
• 51 Hamdy S, Jilani S, Price V et al. Modulation of human swallowing behaviour by thermal and chemical stimulation in health and after brain injury. Neurogastroenterol Motil 2003; 15: 69-77
• 52 Kaatzke-McDonald MN, Post E, Davis PJ. The effects of cold, touch, and chemical stimulation of the anterior faucial pillar on human swallowing. Dysphagia 1996; 11: 198-206
• 53 Sciortino K, Liss JM, Case JL et al. Effects of mechanical, cold, gustatory, and combined stimulation to the human anterior faucial pillars. Dysphagia 2003; 18: 16-26
• 54 Teismann IK, Steinstrater O, Warnecke T et al. Tactile thermal oral stimulation increases the cortical representation of swallowing. BMC Neurosci 2009; 10: 71
• 55 Logemann JA, Pauloski BR, Colangelo L et al. Effects of a sour bolus on oropharyngeal swallowing measures in patients with neurogenic dysphagia. J Speech Hear Res 1995; 38: 556-563
• 56 Pelletier CA, Lawless HT. Effect of citric acid and citric acid-sucrose mixtures on swallowing in neurogenic oropharyngeal dysphagia. Dysphagia 2003; 18: 231-241
• 57 Mistry S, Rothwell JC, Thompson DG et al. Modulation of human cortical swallowing motor pathways after pleasant and aversive taste stimuli. Am J Physiol Gastrointest Liver Physiol 2006; 291: G666-G671
• 58 Babaei A, Kern M, Antonik S et al. Enhancing effects of flavored nutritive stimuli on cortical swallowing network activity. Am J Physiol Gastrointest Liver Physiol 2010; 299: G422-G429
• 59 Abdul Wahab N, Jones RD, Huckabee ML. Effects of olfactory and gustatory stimuli on neural excitability for swallowing. Physiol Behav 2010; 101: 568-575
• 60 Wahab NA, Jones RD, Huckabee ML. Effects of olfactory and gustatory stimuli on the biomechanics of swallowing. Physiol Behav 2011; 102: 485-490
• 61 Ludlow CL, Humbert I, Saxon K et al. Effects of surface electrical stimulation both at rest and during swallowing in chronic pharyngeal Dysphagia. Dysphagia 2007; 22: 1-10
• 62 Rosenbek JC, Robbins J, Fishback B et al. Effects of thermal application on dysphagia after stroke. J Speech Hear Res 1991; 34: 1257-1268
• 63 Rosenbek JC, Roecker EB, Wood JL et al. Thermal application reduces the duration of stage transition in dysphagia after stroke. Dysphagia 1996; 11: 225-233
• 64 Rosenbek JC, Robbins J, Willford WO et al. Comparing treatment intensities of tactile-thermal application. Dysphagia 1998; 13: 1-9
• 65 Park CL, O’Neill PA, Martin DF. A pilot exploratory study of oral electrical stimulation on swallow function following stroke: an innovative technique. Dysphagia 1997; 12: 161-166
• 66 Power M, Fraser C, Hobson A et al. Changes in pharyngeal corticobulbar excitability and swallowing behavior after oral stimulation. Am J Physiol Gastrointest Liver Physiol 2004; 286: G45-G50
• 67 Power ML, Fraser CH, Hobson A et al. Evaluating oral stimulation as a treatment for dysphagia after stroke. Dysphagia 2006; 21: 49-55
• 68 Hamdy S, Rothwell JC, Aziz Q et al. Long-term reorganization of human motor cortex driven by short-term sensory stimulation. Nat Neurosci 1998; 1: 64-68
• 69 Fraser C, Power M, Hamdy S et al. Driving plasticity in human adult motor cortex is associated with improved motor function after brain injury. Neuron 2002; 34: 831-840
• 70 Jayasekeran V, Singh S, Tyrrell P et al. Adjunctive functional pharyngeal electrical stimulation reverses swallowing disability after brain lesions. Gastroenterology 2010; 138: 1737-1746
• 71 Freed ML, Freed L, Chatburn RL et al. Electrical stimulation for swallowing disorders caused by stroke. Respir Care 2001; 46: 466-474
• 72 Lim KB, Lee HJ, Lim SS et al. Neuromuscular electrical and thermal-tactile stimulation for dysphagia caused by stroke: a randomized controlled trial. J Rehabil Med 2009; 41: 174-178
• 73 Bulow M, Speyer R, Baijens L et al. Neuromuscular electrical stimulation (NMES) in stroke patients with oral and pharyngeal dysfunction. Dysphagia 2008; 23: 302-309
• 74 Permsirivanich W, Tipchatyotin S, Wongchai M et al. Comparing the effects of rehabilitation swallowing therapy vs. neuromuscular electrical stimulation therapy among stroke patients with persistent pharyngeal dysphagia: a randomized controlled study. J Med Assoc Thai 2009; 92: 259-265
• 75 Xia W, Zheng C, Lei Q et al. Treatment of post-stroke dysphagia by vitalstim therapy coupled with conventional swallowing training. J Huazhong Univ Sci Technolog Med Sci 2011; 31: 73-76
• 76 Seidl RO, Nahrstaedt H, Schauer T. Electric stimulation in dysphagia therapy – a review. Laryngorhinootologie 2009; 88: 768-774
• 77 Clark H, Lazarus C, Arvedson J et al. Evidence-based systematic review. effects of neuromuscular electrical stimulation on swallowing and neural activation. Am J Speech Lang Pathol 2009; 18: 361-375
• 78 Gow D, Rothwell J, Hobson A et al. Induction of long-term plasticity in human swallowing motor cortex following repetitive cortical stimulation. Clin Neurophysiol 2004; 115: 1044-1051
• 79 Jefferson S, Mistry S, Michou E et al. Reversal of a virtual lesion in human pharyngeal motor cortex by high frequency contralesional brain stimulation. Gastroenterology 2009; 137: 841-849 849.e1
• 80 ONeil KH, Purdy M, Falk J et al. The Dysphagia Outcome and Severity Scale. Dysphagia 1999; 14: 139-145
• 81 Khedr EM, Abo-Elfetoh N, Rothwell JC. Treatment of post-stroke dysphagia with repetitive transcranial magnetic stimulation. Acta Neurol Scand 2009; 119: 155-161
• 82 Khedr EM, Abo-Elfetoh N. Therapeutic role of rTMS on recovery of dysphagia in patients with lateral medullary syndrome and brainstem infarction. J Neurol Neurosurg Psychiatry 2010; 81: 495-499
• 83 Park JW, Oh JC, Lee JW et al. The effect of 5Hz high-frequency rTMS over contralesional pharyngeal motor cortex in post-stroke oropharyngeal dysphagia. a randomized controlled study. Neurogastroenterol Motil 2013; 25: e324-e250
• 84 Michou E, Mistry S, Jefferson S et al. Targeting unlesioned pharyngeal motor cortex improves swallowing in healthy individuals and after dysphagic stroke. Gastroenterology 2012; 142: 29-38
• 85 Monte-Silva K, Kuo MF, Liebetanz D et al. Shaping the optimal repeti­tion interval for cathodal transcranial direct current stimulation (tDCS). J Neurophysiol 2010; 103: 1735-1740
• 86 Edwards DJ, Krebs HI, Rykman A et al. Raised corticomotor excitability of M1 forearm area following anodal tDCS is sustained during robotic wrist therapy in chronic stroke. Restor Neurol Neurosci 2009; 27: 199-207
• 87 Celnik P, Paik NJ, Vandermeeren Y et al. Effects of combined peripheral nerve stimulation and brain polarization on performance of a motor sequence task after chronic stroke. Stroke 2009; 40: 1764-1771
• 88 Uy J, Ridding MC. Increased cortical excitability induced by transcranial DC and peripheral nerve stimulation. J Neurosci Methods 2003; 127: 193-197
• 89 Jefferson S, Mistry S, Singh S et al. Characterizing the application of transcranial direct current stimulation in human pharyngeal motor cortex. Am J Physiol Gastrointest Liver Physiol 2009; 297: G1035-G1040
• 90 Suntrup S, Teismann I, Wollbrink A et al. Magnetoencephalographic evidence for the modulation of cortical swallowing processing by transcranial direct current stimulation. Neuroimage 2013; 83: 346-354
• 91 Kumar S, Wagner CW, Frayne C et al. Noninvasive brain stimulation may improve stroke-related dysphagia: a pilot study. Stroke 2011; 42: 1035-1040
• 92 Yang EJ, Baek SR, Shin J et al. Effects of transcranial direct current stimulation (tDCS) on post-stroke dysphagia. Restor Neurol Neurosci 2012; 30: 303-311
• 93 Shigematsu T, Fujishima I, Ohno K. Transcranial direct current stimulation improves swallowing function in stroke patients. Neurorehabil Neural Repair 2013; 27: 363-369
• 94 Warnecke T, Dziewas R. Neurogene Dysphagien – Diagnostik und Therapie. 1. Aufl. Stuttgart: W. Kohlhammer GmbH; 2013