Skill versus Strength in Swallowing Training: Neurophysiological, Biomechanical, and Structural Assessments
Thesis DisciplineSpeech and Language Sciences
Degree GrantorUniversity of Canterbury
Degree NameDoctor of Philosophy
Swallowing is a complex sensorimotor behaviour that includes precisely-timed bilateral activation and relaxation of muscles of the face, lips, tongue, cheeks, palate, larynx, pharynx and oesophagus. These events of activation and inhibition are controlled by many structures of the brain and are executed by cranial nerves that carry motor and sensory information to and from the swallowing muscles. Swallowing disorders are common sequelae of many neurological and structural disorders, including stroke, Parkinson’s disease, and head and neck cancer. Changes to swallowing physiology are also prevalent in older individuals, but these changes do not necessarily translate to dysphagia. Decreased muscle strength, changes to motor unit properties, and hypotrophic changes in skeletal muscles can result in age-related changes in swallowing physiology. In addition to muscular changes, neural changes might also change swallowing function in older subjects. The motor-learning literature presents a clear distinction between the differential applications and effects of skill- and strength-training approaches for rehabilitation of limb movement. In contrast to limb-movement rehabilitation, swallowing rehabilitation approaches consist mainly of strength training, although the pathophysiological basis for dysphagia is not always weakness. Therefore, this Phase I clinical-trial critically evaluated a unique swallowing skill training protocol in which the goal of intervention is to increase precision of motor control during swallowing. A Phase I clinical-trial was necessary to identify the appropriate protocol for inducing neurophysiological, biomechanical, and structural adaptations, to estimate effect sizes, and to identify adverse effects. The first and primary question addressed in this thesis was whether swallowing skill training would produce greater physiological effects in healthy subjects than a traditional swallowing strength training approach. In order to answer this question, three levels of assessment were included. Neurophysiological assessment consisted of delivering single-pulse transcranial magnetic stimulation (TMS) over the M1 area that sends efferent projections to the submental muscle group during a functional task of volitional saliva swallowing, and during a non-functional task of submental muscle group contraction. Biomechanical assessments consisted of pharyngeal and upper esophageal sphincter (UES) pressure measurements using pharyngeal manometry during effortful and non-effortful swallowing tasks, submental muscle activation measurements using surface electromyography (sEMG) during effortful and non-effortful swallowing tasks, and hyoid displacement using ultrasonography. Structural assessment consisted of measuring the cross sectional area of the submental muscle group. Finally, motor performance during training, and subjective ratings of the training protocols were assessed. Two skill training protocols were developed to assess the use of immediate versus delayed visual feedback in swallowing skill training. In addition, a pilot study aimed at examining the effects of increased dosage of training sessions was conducted. Forty healthy subjects (20 young, and 20 old; 20 females and 20 males) were allocated to skill and strength training groups in a counterbalanced manner. Strength training consisted of execution of the effortful swallowing technique targeting increased demand for strength. Skill training targeted precise timing and force execution during swallowing execution. Several motor-learning principles were considered in devising the training protocols, including the principles of task specificity and high intensity of training. Biofeedback was included to promote motor learning. Since the submental muscle group plays an important role in hyolaryngeal excursion, the current study utilized submental sEMG biofeedback using custom-made training software. The training protocols consisted of 1000 repetition of swallowing over a 2-week period. Subjects trained for an hour, five days a week, for 2 weeks (i.e., 10 training sessions). The extended dosage protocol included 10 subjects and comprised an additional eight sessions. The results indicated that there was a significant difference in submental activation following training, with strength training having an increase in sEMG peak amplitude in comparison to skill training. There were no other differences between groups at the 5% error level. Patterns of change were revealed when marginally significant results (0.05 < p ≤ 0.10) were investigated as well. Strength training resulted in a trend towards increased neural drive for volitional effortful-type tasks (i.e., effortful saliva swallowing, effortful water swallowing, and submental muscle contraction) as indicated by increased MEP magnitude (p = 0.07) which was consistent with significantly increased peak amplitude of submental activity measures (p < 0.001). This finding supports the task specificity principle of motor learning. Skill training resulted in no changes in MEP magnitude. There was a trend (p = 0.06) towards increased submental muscles activity during functional swallowing tasks (i.e., non-effortful swallowing) in young subjects,. Males in skill training had decreased duration of UES opening in 10 mL water effortful swallowing task (p = 0.02), a trend towards increased UES pressure in non-effortful saliva swallowing task (p = 0.07), and reduced hyoid displacement following training (p < 0.001). Changes in pharyngeal pressures were detected for skill training with delayed visual feedback that resulted in decreased pressure at mid-pharynx in effortful and non-effortful tasks (p < 0.05). No difference in submental CSA changes was detected in either training group. Both groups improved motor performance measured by data collected during the session (target hit-rate and muscle activity). The results of the pilot study that examined the effects of an extended dosage of training were difficult to interpret due to the small sample size. However, there were significant and marginally significant effects of skill training on mid-pharyngeal and UES pressure duration events. Dysphagia is common in patients with Parkinson’s disease, but no specific training programme exists for these patients, leading to the second question addressed through this research. Since movement planning is compromised due to dysfunction of the basal ganglia, providing external information for planning and executing swallowing was hypothesized to alleviate dysphagic symptoms. Ten subjects were recruited. Swallowing skill training with immediate feedback was administered for one hour every day, five days a week, for 2 weeks, similar to the training dosage and frequency in the healthy group. Biomechanical and structural changes were assessed. Swallowing skill training with immediate feedback led to an increase in submental activity in effortful swallowing tasks but not non-effortful tasks. In addition, it was found that individuals with dysphagia secondary to Parkinson’s disease have deceased submental muscle reserve relative to healthy subjects. Preliminary analysis of MEP data led to exploration of submental MEP measures between younger and older subjects. This ‘discovery’ research shed light on the third topic addressed in this thesis. There are contradicting results in the literature regarding age-related brain activity during swallowing. Since submental MEPs were included as an outcome measure in the main study, it was important to evaluate them at baseline in order to understand and interpret changes in this measure. Unlike other measures, such as pharyngeal pressure and hyoid displacement that have been documented in the literature to change with age, no similar study has been conducted to assess for differences in swallowing-related MEPs. Baseline data from the main study were analysed. Older subjects produced larger MEP magnitude in comparison to young in volitional saliva swallowing and volitional submental contraction. This finding raised some questions regarding the use of MEPs as an outcome measure, since it is not clear what constitutes a ‘positive’ change. This study documented, for the first time, the application of skill training in swallowing in a healthy and dysphagic population. Positive effects of treatment were found in the dysphagic group; an indication of negative effects was identified in the healthy group. In addition, this is the first study to compare skill to strength training in swallowing. The only significant difference between the two was significantly greater submental activation in effortful swallowing tasks following strength training in comparison to skill training; although there were some significant interactions between age and training type and gender and training type. This project represents the first Phase I clinical-trial of an innovative approach for addressing swallowing impairments. Achieving the ultimate aim of finding the most appropriate training protocol for treating individuals with a specific pathophysiological basis of dysphagia, requires the implementation of a long-term on-going research programme characterized by a staged process. This research programme sets an initial reference framework from which further projects can estimate the sample size required to answer specific questions, control for effects of age and gender and their interaction with training, increase precision in choosing assessment tools, and test new specific questions.