The importance of the reproducibility of oropharyngeal swallowing in amyotrophic lateral sclerosis. An electrophysiological study
Introduction
Oropharyngeal dysphagia is one of the most frequent and critical clinical symptoms of amyotrophic lateral sclerosis (ALS). It has a severe impact on the patient’s quality of life and invariably leads to malnutrition, dehydration and a high risk of aspiration pneumonia (Kasarskis et al., 1996, Kühnlein et al., 2008). Swallowing difficulties may appear at any stage of the disease, and typically have a progressive course, albeit with unpredictable changes over time. Not uncommonly, dysphagia is diagnosed only when swallowing function is already significantly impaired; this diagnostic delay can be attributed, in part, to the fact that adaptation mechanisms initially compensate for the relatively slow deterioration of bulbar function.
On these bases, it seems reasonable to argue that swallowing function should be routinely evaluated in all patients with ALS, whether or not they have clear symptoms of dysphagia. Indeed, early recognition of swallowing dysfunctions, and identification of the underlying pathophysiological mechanisms, are fundamental to ensure early and targeted treatment strategies that could prevent severe complications and delay the need for percutaneous endoscopic gastrostomy (Barbiera et al., 2006, Kühnlein et al., 2008, Andersen et al., 2012).
As reported in the literature, there exist several procedures for assessing swallowing function in ALS; these include videofluoroscopy (VF), used alone or in conjunction with manometry (Briani et al., 1998, Higo et al., 2002, Higo et al., 2004, Kawai et al., 2003, Goeleven et al., 2006), fiberoptic endoscopic evaluation of swallowing (FEES) (Leder et al., 2004, Ruoppolo et al., 2013), and oropharyngoesophageal scintigraphy (Fattori et al., 2006). Videofluoroscopic swallow evaluation is considered the most sensitive technique for detecting dysphagia, and it has also been shown to be capable of detecting preclinical abnormalities in non-dysphagic ALS patients who later develop swallowing problems (Briani et al., 1998, Kawai et al., 2003, Goeleven et al., 2006). However, VF is not always available, involves irradiation exposure, and adds to the evaluation costs and personnel requirements of the evaluation; these drawbacks make it unsuitable for use in regular follow-up assessments.
Electrophysiological assessment, on the other hand, is a non-invasive method that allows reliable and easily repeatable investigation of the physiological and pathological aspects of oropharyngeal swallowing (Ertekin et al., 1995, Perlman et al., 1999, Vaiman et al., 2004). In a recent study, we described a new electrophysiological approach for non-invasive evaluation of oropharyngeal swallowing (Alfonsi et al., 2015). In particular, we evaluated, in normal subjects, the reproducibility of the electrophysiological signals related to the oral and pharyngeal phases of swallowing by calculating a similarity index (SI) across repeated swallowing acts. In accordance with the concept that the act of swallowing is characterized by stereotyped motor behaviors modulated by different bolus properties (Jean, 2001), we recorded a high overall reproducibility of both the oral phase and the pharyngeal phase of swallowing in physiological conditions.
In the present study we evaluated the SI in ALS patients with and without clear symptoms of dysphagia as assessed by clinical examination and FEES. Our first aim was to investigate whether evaluation of the reproducibility of oropharyngeal swallowing, along with other classical electrophysiological measures such as the oropharyngeal interval and the duration of the electromyographic activity of the submental/suprahyoid muscles, might provide useful information on functional aspects of swallowing in ALS. Our second aim was to evaluate whether electrophysiological assessment could reveal swallowing abnormalities in non-dysphagic ALS patients when compared to age- and sex-matched healthy controls. Were this found to be the case, electrophysiological assessment might become a useful tool in the routine evaluation of oropharyngeal swallowing in patients with ALS, even at the initial stage of the disease.
Section snippets
Subjects
Twenty-six patients (11 female, 15 male; mean age = 61 ± 12 years, ranging from 32 to 80 years) with a diagnosis of definite or probable ALS according to the El Escorial criteria (Brooks et al., 2000), and 30 age- and sex-matched healthy controls (15 female, 15 male; mean age = 60 ± 9 years, ranging from 39 to 74 years) were enrolled in the study. The patients were consecutively recruited at first presentation or in the course of routine, three-monthly check-ups at the neurology clinic of the C. Mondino
Results
The electrophysiological assessment was completed in all the subjects and the experimental procedures were well tolerated both by the healthy volunteers and by the patients. t-test showed no statistically significant difference for age between patients and controls (p = 0.68). On the basis of the DOSS scores, which summarized the results of the clinical and FEES evaluations, the patients were divided into two groups: those with (16 patients) and those without (10 patients) signs and symptoms of
Discussion
The reproducibility of oropharyngeal swallowing may be a useful new parameter for the evaluation of physiological and pathological aspects of deglutition. This topic was recently investigated using a non-invasive electrophysiological assessment, which provides objective and reliable measures of swallowing function (Alfonsi et al., 2015).
The act of swallowing involves multiple areas of the central nervous system. It is initiated voluntarily but continues through a precisely orchestrated sequence
Acknowledgments
We wish to thank Ms Catherine Wrenn for the linguistic revision of the manuscript.
Conflict of interest statement: None of the authors have potential conflicts of interest to be disclosed.
References (34)
- et al.
Electrophysiological patterns of oropharyngeal swallowing in multiple sclerosis
Clin Neurophysiol
(2013) - 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) - et al.
Transcranial direct current stimulation enhances sucking of a liquid bolus in healthy humans
Brain Stimul
(2014) - et al.
Longitudinal analysis of progression of dysphagia in amyotrophic lateral sclerosis
Auris Nasus Larynx
(2004) - et al.
Nutritional status of patients with amyotrophic lateral sclerosis: relation to the proximity of death
Am J Clin Nutr
(1996) - et al.
Swallowing function following hypopharyngeal reconstruction with the pectoralis major musculocutaneous flap
Auris Nasus Larynx
(1991) Swallowing in ALS and motor neuron disorders
Neurol Clin
(1987)- et al.
Electrophysiologic patterns of oral-pharyngeal swallowing in parkinsonian syndromes
Neurology
(2007) - et al.
Electrophysiological investigations of shape and reproducibility of oropharyngeal swallowing: interaction with bolus volume and age
Dysphagia
(2015) - et al.
EFNS guidelines on the clinical management of amyotrophic lateral sclerosis (MALS)–revised report of an EFNS task force
Eur J Neurol
(2012)
Role of videofluorography swallow study in management of dysphagia in neurologically compromised patients
Radiol Med
Radiological evidence of subclinical dysphagia in motor neuron disease
J Neurol
World Federation of Neurology Research Group on Motor Neuron Diseases. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis
Amyotroph Lateral Scler Other Motor Neuron Disord
An electrophysiological investigation of deglutition in man
Muscle Nerve
Pathophysiological mechanisms of oropharyngeal dysphagia in amyotrophic lateral sclerosis
Brain
Assessment of swallowing by oropharyngoesophageal scintigraphy in patients with amyotrophic lateral sclerosis
Dysphagia
Manofluorographic evaluation of swallowing in amyotrophic lateral sclerosis and its relationship with clinical evaluation of swallowing
Amyotroph Lateral Scler
Cited by (12)
Reproducibility and reaction time of swallowing as markers of dysphagia in parkinsonian syndromes
2020, Clinical NeurophysiologyCitation Excerpt :It is also worth mentioning that reproducibility of the oral and pharyngeal phases of swallowing in non-dysphagic patients was not decreased with respect to controls. This differs from what we observed in patients with amyotrophic lateral sclerosis, presenting a significant reduction of both SI-SHEMG and SI-LPM also before the onset of dysphagia (Cosentino et al., 2017). Therefore, a reduced reproducibility of the oral phase of swallowing seems to represent an electrophysiological marker of dysphagia onset in parkinsonian syndromes.
Subclinical dysphagia in task-specific mouth tremor triggered by drinking
2019, Clinical NeurophysiologyInvestigation of variation factors in EMG measurement of swallowing: instruction can improve EMG reproducibility
2022, Medical and Biological Engineering and Computing