Pharyngeal electrical stimulation in amyotrophic lateral sclerosis: a pilot study

Christine Herrmann, Falk Schradt, Beate Lindner-Pfleghar, Joachim Schuster, Albert C Ludolph, Johannes Dorst, Christine Herrmann, Falk Schradt, Beate Lindner-Pfleghar, Joachim Schuster, Albert C Ludolph, Johannes Dorst

Abstract

Background: Patients with amyotrophic lateral sclerosis (ALS) suffer from dysphagia that increases the risk for aspiration, pneumonia and weight loss. Pharyngeal electrical stimulation (PES) is a therapeutic technique that applies electric stimuli to the patient's pharynx in order to improve swallowing based on the principle of cortical plasticity and reorganization. Previous studies have demonstrated positive effects in patients with various neurological diseases.

Objective: This study was initiated to investigate the effect of PES on swallowing function in patients with ALS.

Methods: In all, 20 ALS patients with severe dysphagia [characterized by a Penetration Aspiration Scale (PAS) of at least 4 in thin liquid] were randomized to receive either PES for 10 min at 3 consecutive days in addition to Standard Logopaedic Therapy (SLT) or SLT alone. Swallowing function was evaluated by Fiberoptic Endoscopic Evaluation of Swallowing (FEES) at five timepoints: at baseline, 1 day, 4 days, 3 weeks and 3 months after treatment. Primary endpoint was the severity of penetrations or aspirations as classified by PAS. Secondary endpoints were adverse events, dysphagia-related quality of life, Swallowing Quality of Life (SWAL-QOL), Dysphagia Severity Rating Scale (DSRS), residues, leaking, ALS Functional Rating Scale Revised (ALSFRS-R), and the performance in Clinical Evaluation of Swallowing (CES). The trial is registered under the name of 'Pharyngeal Electrical Stimulation in Amyotrophic Lateral Sclerosis' with ClinialTrials.gov, number NCT03481348 (https://ichgcp.net/clinical-trials-registry/NCT03481348).

Results: Both groups combined showed a significant improvement (p = 0.003) of median Total-PAS from 3.6 [interquartile range (IQR) = 2.9-5.0] at baseline to 2.3 (IQR = 1.8-4.0) 1 day after treatment. During subsequent study visits, PAS increased again but remained below baseline. PES and control group did not differ significantly 1 day after intervention (p = 0.32). Similar effects were found in the majority of secondary endpoints.

Interpretation: The findings suggest that PES may not provide an additional positive effect on swallowing function in ALS. SLT seems to yield at least short-term positive effects on swallowing function and swallowing-specific life quality in ALS.Registration: ClinialTrials.gov: NCT03481348.

Keywords: Fiberoptic Endoscopic Evaluation of Swallowing; amyotrophic lateral sclerosis; logopaedic therapy; pharyngeal electrical stimulation.

Conflict of interest statement

Conflict of interest statement: The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

© The Author(s), 2022.

Figures

Figure 1.
Figure 1.
Total-PAS in whole study population. BL, baseline; d1, 1 day after treatment; d4, 4 days after treatment; m3, 3 months after treatment; PAS, Penetration Aspiration Scale; w3, 3 weeks after treatment.
Figure 2.
Figure 2.
Total-PAS in PES and control group. BL, baseline; d1, 1 day after treatment; d4, 4 days after treatment; m3, 3 months after treatment; PAS, Penetration Aspiration Scale; PES, pharyngeal electrical stimulation; w3, 3 weeks after treatment.
Figure 3.
Figure 3.
Swallowing function (blue-coloured water) before (BL) and after treatment (d1). The figure shows the penetration and aspiration findings evaluated by FEES in a patient receiving PES before and 1 day after completed treatment (=3 sessions of PES) during a swallowing test with a teaspoon of blue-coloured water. Above: silent aspiration (*) in the trachea (1) without ejection from the airway (PAS = 8) at baseline. Below: penetration of water (*) into the airways but remaining above the vocal folds (2) (PAS = 3) 1 day after completed treatment (=3 sessions of PES). BL, baseline; d1, 1 day after treatment; FEES, Fiberoptic Endoscopic Evaluation of Swallowing; PAS, Penetration Aspiration Scale.
Figure 4.
Figure 4.
Erythema at the pharyngeal wall after PES. The figure shows an erythema after PES in FEES 1 day after treatment that diminished 5 days after treatment. Left: erythema (*) 1 day after intervention. Right: diminishing erythema 5 days after intervention. FEES, Fiberoptic Endoscopic Evaluation of Swallowing; PES, pharyngeal electrical stimulation.

References

    1. Couratier P, Corcia P, Lautrette G, et al. Epidemiology of amyotrophic lateral sclerosis: a review of literature. Rev Neurol 2016; 172: 37–45.
    1. Onesti E, Schettino I, Gori MC, et al. Dysphagia in amyotrophic lateral sclerosis: impact on patient behavior, diet adaptation, and riluzole management. Front Neurol 2017; 8: 94.
    1. Kasarskis EJ, Berryman S, Vanderleest JG, et al. Nutritional status of patients with amyotrophic lateral sclerosis: relation to the proximity of death. Am J Clin Nutr 1996; 63: 130–137.
    1. Carrion S, Cabre M, Monteis R, et al. Oropharyngeal dysphagia is a prevalent risk factor for malnutrition in a cohort of older patients admitted with an acute disease to a general hospital. Clin Nutr 2015; 34: 436–442.
    1. Jesus P, Fayemendy P, Nicol M, et al. Hypermetabolism is a deleterious prognostic factor in patients with amyotrophic lateral sclerosis. Eur J Neurol 2018; 25: 97–104.
    1. Peter RS, Rosenbohm A, Dupuis L, et al. Life course body mass index and risk and prognosis of amyotrophic lateral sclerosis: results from the ALS registry Swabia. Eur J Epidemiol 2017; 32: 901–908.
    1. Paganoni S, Deng J, Jaffa M, et al. Body mass index, not dyslipidemia, is an independent predictor of survival in amyotrophic lateral sclerosis. Muscle Nerve 2011; 44: 20–24.
    1. Dupuis L, Corcia P, Fergani A, et al. Dyslipidemia is a protective factor in amyotrophic lateral sclerosis. Neurology 2008; 70: 1004–1009.
    1. Dorst J, Kuhnlein P, Hendrich C, et al. Patients with elevated triglyceride and cholesterol serum levels have a prolonged survival in amyotrophic lateral sclerosis. J Neurol 2011; 258: 613–617.
    1. Murono S, Hamaguchi T, Yoshida H, et al. Evaluation of dysphagia at the initial diagnosis of amyotrophic lateral sclerosis. Auris Nasus Larynx 2015; 42: 213–217.
    1. Solazzo A, Monaco L, Vecchio LD, et al. Earliest videofluoromanometric pharyngeal signs of dysphagia in ALS patients. Dysphagia 2014; 29: 539–544.
    1. Waito AA, Tabor-Gray LC, Steele CM, et al. Reduced pharyngeal constriction is associated with impaired swallowing efficiency in amyotrophic lateral sclerosis (ALS). Neurogastroenterol Motil 2018; 30: e13450.
    1. Eisenhuber E, Schima W, Schober E, et al. Videofluoroscopic assessment of patients with dysphagia: pharyngeal retention is a predictive factor for aspiration. Am J Roentgenol 2002; 178: 393–398.
    1. 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.
    1. 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.
    1. Teismann IK, Warnecke T, Suntrup S, et al. Cortical processing of swallowing in ALS patients with progressive dysphagia – a magnetoencephalographic study. PLoS ONE 2011; 6: 20.
    1. Dalakas MC, Hatazawa J, Brooks RA, et al. Lowered cerebral glucose utilization in amyotrophic lateral sclerosis. Ann Neurol 1987; 22: 580–586.
    1. 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.
    1. 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.
    1. Muhle P, Suntrup-Krueger S, Bittner S, et al. 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.
    1. Restivo DA, Casabona A, Centonze D, et al. Pharyngeal electrical stimulation for dysphagia associated with multiple sclerosis: a pilot study. Brain Stimul 2013; 6: 418–423.
    1. Suntrup S, Marian T, Schroder JB, et al. Electrical pharyngeal stimulation for dysphagia treatment in tracheotomized stroke patients: a randomized controlled trial. Intensive Care Med 2015; 41: 1629–1637.
    1. Dziewas R, Stellato R, van der Tweel I, et al. Pharyngeal electrical stimulation for early decannulation in tracheotomised patients with neurogenic dysphagia after stroke (PHAST-TRAC): a prospective, single-blinded, randomised trial. Lancet Neurol 2018; 17: 849–859.
    1. Ravits J. Focality, stochasticity and neuroanatomic propagation in ALS pathogenesis. Exp Neurol 2014; 262: 121–126.
    1. Brooks BR, Miller RG, Swash M, et al. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 2000; 1: 293–299.
    1. Rosenbek JC, Robbins JA, Roecker EB, et al. A penetration-aspiration scale. Dysphagia 1996; 11: 93–98.
    1. 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.
    1. Lindner-Pfleghar B, Schradt F, Weydt P. ALS Praxisbuch: Möglichkeiten logopädischer Therapie bei Amyotropher Lateralsklerose. 1st ed. Idstein: Schulz-Kirchner, 2018, pp. 64–73.
    1. Türk C, Söhlemann S, Rummel H. Das Castillo Morales-Konzept. 2nd ed. Stuttgart: Thieme, 2020.
    1. Nusser-Müller-Busch R. Die Therapie des Facio-Oralen Trakts: F.O.T.T. nach Kay Coombes. 1st ed. Berlin: Springer, 2004, pp. 3–118.
    1. Shanahan TK, Logemann JA, Rademaker AW, et al. Chin-down posture effect on aspiration in dysphagic patients. Arch Phys Med Rehabil 1993; 74: 736–739.
    1. Ohmae Y, Logemann JA, Kaiser P, et al. Effects of two breath-holding maneuvers on oropharyngeal swallow. Ann Otol Rhinol Laryngol 1996; 105: 123–131.
    1. Prosiegel M. Neurogene dysphagien – Leitlinien für Diagnostik und Therapie in der Neurologie (AWMF-Registernummer: 030/111). Berlin: Deutschen Gesellschaft für Neurologie, 2015.
    1. Hey C, Pluschinski P, Zaretsky Y, et al. [Penetration-Aspiration Scale according to Rosenbek. Validation of the German version for endoscopic dysphagia diagnostics]. HNO 2014; 62: 276–281.
    1. McHorney CA, Robbins J, Lomax K, et al. The SWAL-QOL and SWAL-CARE outcomes tool for oropharyngeal dysphagia in adults: III. Dysphagia 2002; 17: 97–114.
    1. Gabriel V. Lebensqualität bei Schluckstörungen. Validierung eines Fragebogens zur Untersuchung der spezifischen Lebensqualität bei Schluckstörungen. Magisterarbeit, München, 2004.
    1. Waxman MJ, Durfee D, Moore M, et al. Nutritional aspects and swallowing function of patients with Parkinson’s disease. Nutr Clin Pract 1990; 5: 196–199.
    1. Ickenstein GW, Prosiegel M, Höhlig C, et al. Standardisierung des Untersuchungsablaufs bei neurogener oropharyngealer Dysphagie (NOD) – Evaluation des NOD-Stufenkonzeptes. Akt Neurol 2009; 36: P496.
    1. Cedarbaum JM, Stambler N, Malta E, et al. The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J Neurol Sci 1999; 169: 13–21.
    1. Abdulla S, Vielhaber S, Körner S, et al. Validation of the German version of the extended ALS functional rating scale as a patient-reported outcome measure. J Neurol 2013; 260: 2242–2255.
    1. Jayasekeran V, Singh S, Tyrrell P, et al. Adjunctive functional pharyngeal electrical stimulation reverses swallowing disability after brain lesions. Gastroenterology 2010; 138: 1737–1746.
    1. Scutt P, Lee HS, Hamdy S, et al. Pharyngeal electrical stimulation for treatment of poststroke dysphagia: individual patient data meta-analysis of randomised controlled trials. Stroke Res Treat 2015; 2015: 429053.
    1. Brettschneider J, Del Tredici K, Toledo JB, et al. Stages of pTDP-43 pathology in amyotrophic lateral sclerosis. Ann Neurol 2013; 74: 20–38.
    1. Braak H, Brettschneider J, Ludolph AC, et al. Amyotrophic lateral sclerosis – a model of corticofugal axonal spread. Nat Rev Neurol 2013; 9: 708–714.
    1. Restivo DA, Alfonsi E, Casabona A, et al. A pilot study on the efficacy of transcranial direct current stimulation applied to the pharyngeal motor cortex for dysphagia associated with brainstem involvement in multiple sclerosis. Clin Neurophysiol 2019; 130: 1017–1024.
    1. Munneke MA, Stegeman DF, Hengeveld YA, et al. Transcranial direct current stimulation does not modulate motor cortex excitability in patients with amyotrophic lateral sclerosis. Muscle Nerve 2011; 44: 109–114.
    1. Quartarone A, Lang N, Rizzo V, et al. Motor cortex abnormalities in amyotrophic lateral sclerosis with transcranial direct-current stimulation. Muscle Nerve 2007; 35: 620–624.
    1. Sivaramakrishnan A, Datta A, Bikson M, et al. Remotely supervised transcranial direct current stimulation: a feasibility study for amyotrophic lateral sclerosis. NeuroRehabilitation 2019; 45: 369–378.
    1. Kawai S, Tsukuda M, Mochimatsu I, et al. A study of the early stage of dysphagia in amyotrophic lateral sclerosis. Dysphagia 2003; 18: 1–8.
    1. Bath PM, Scutt P, Love J, et al. Pharyngeal electrical stimulation for treatment of dysphagia in subacute stroke: a randomized controlled trial. Stroke 2016; 47: 1562–1570.
    1. Nardone R, Golaszewski S, Thomschewski A, et al. Disinhibition of sensory cortex in patients with amyotrophic lateral sclerosis. Neurosci Lett 2020; 722: 22.
    1. Höffken O, Schmelz A, Lenz M, et al. Excitability in somatosensory cortex correlates with motoric impairment in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Frontotemporal Degener 2019; 20: 192–198.
    1. da Costa Franceschini A, Mourao LF. Dysarthria and dysphagia in amyotrophic lateral sclerosis with spinal onset: a study of quality of life related to swallowing. NeuroRehabilitation 2015; 36: 127–134.
    1. Tabor L, Gaziano J, Watts S, et al. Defining swallowing-related quality of life profiles in individuals with amyotrophic lateral sclerosis. Dysphagia 2016; 31: 376–382.
    1. Farri A, Accornero A, Burdese C. Social importance of dysphagia: its impact on diagnosis and therapy. Acta Otorhinolaryngol Ital 2007; 27: 83–86.
    1. Paris G, Martinaud O, Petit A, et al. Oropharyngeal dysphagia in amyotrophic lateral sclerosis alters quality of life. J Oral Rehabil 2013; 40: 199–204.

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