Abstract
A neurogenic dysphagia is dysphagia caused by problems with the central and peripheral nervous systems, is particularly prevalent in conditions such as Parkinson’s disease and stroke. It significantly impacts the quality of life for affected individuals and causes additional burdens, such as malnutrition, aspiration pneumonia, asphyxia, or even death from choking due to improper eating. Physical therapy offers a non-invasive treatment with high efficacy and low cost. Evidence supporting the use of physical therapy in dysphagia treatment is increasing, including techniques such as neuromuscular electrical stimulation, sensory stimulation, transcranial direct current stimulation, and repetitive transcranial magnetic stimulation. While initial studies have shown promising results, the effectiveness of specific treatment regimens still requires further validation. At present, there is a lack of scientific evidence to guide patient selection, develop appropriate treatment regimens, and accurately evaluate treatment outcomes. Therefore, the primary objectives of this review are to review the results of existing research, summarize the application of physical therapy in dysphagia management, we also discussed the mechanisms and treatments of physical therapy for neurogenic dysphagia.
1 Introduction
There are several complex physiological movements involved in swallowing, including movements of the mouth, pharynx, larynx, and esophagus (Shaw and Martino, 2013). Dysphagia refers to the disruption of the normal swallowing process (Rofes et al., 2011), which poses severe risks including malnutrition, aspiration pneumonia, asphyxia, etc (). The causes of dysphagia can be divided into neurogenic, structural, and mental dysphagia (Medicine DRCO, 2023). A neurogenic dysphagia results from problems with the central and peripheral nervous systems (). The number of people suffering from neurogenic dysphagia each year worldwide is estimated at 400000 to 800,000 (Panebianco et al., 2020). Among the diseases that predispose to neurogenic dysphagia are stroke, Parkinson’s disease, amyotrophic lateral sclerosis, multiple sclerosis, and other forms of neurodegeneration (). It is a common complication of stroke to experience dysphagia afterward, it is estimated that 20–43% of patients have persistent dysphagia after 3 months, which can lead to aspiration pneumonia, malnutrition, water and electrolyte disorders, and other complications (). There is a prevalence of 18–100% of Parkinson’s disease with dysphagia, it can lead to dehydration, malnutrition, aspiration pneumonia, depression, and social isolation, and it can also affect the quality of life and even cause death (). Dehydration, malnutrition, asphyxia, and death are all risks associated with neurogenic dysphagia, which severely reduces the quality of life for the patient (Xia et al., 2023; Kocica et al., 2024).
Physical therapy, as a new treatment method, directly targets the swallowing nerve circuit to enhance swallowing function (Li et al., 2023). Common clinical treatments for dysphagia include neuromuscular electrical stimulation (NMES), sensory stimulation, repetitive transcranial magnetic stimulation (rTMS), and transcranial direct current stimulation (tDCS) (; Miller et al., 2022; Li et al., 2023). However, there remains paucity of discourse on the application of physical therapy in dysphagia management in different diseases. The purpose of this review article is to provide more theoretical support for the application of physical therapy in neurogenic dysphagia, and to describe treatment principles and treatment programs of several commonly used physical therapy programs.
2 Mechanisms associated with dysphagia
Swallowing is a complex process, it involves the coordination of more than 30 muscles in the mouth, pharynx, larynx, and esophagus, encompassing four distinct stages: oral preparation, oral transit, pharynx, and esophageal phase (). It involves various levels of the central nervous system, from the cortex to the medulla, as well as multiple cranial and peripheral nerves (). It is well recognized that pharyngeal movements are strongly related to the innervation of sensory branches of the cranial nerves (Nascimento et al., 2021). Usually, swallowing is controlled by four types of components: (1) afferent motor fibers in cranial nerves and ansa cervicalis; (2) afferent sensory fibers in cranial nerves; (3) fibers lining the cerebral, cerebellar, and cerebellar hemispheres that synapse in the swallowing centers; (4) paired swallowing centers in the brainstem that synapse with each other (). In the swallowing process, fiber transmitters transmit signals from peripheral nerves and the cerebral cortex to the swallowing centers in the brain stem (). There is a complex unit called the swallowing central pattern generator that is composed of motor neurons and interneurons located in the brainstem’s medulla oblongata, a region that contains swallowing neurons (Sasegbon et al., 2024). Two parts make up the pattern generator of the swallowing center: (1) the dorsal region consisting of the nucleus tractus solitarius and peripheral neurons; (2) the nucleus and reticular formation surrounding the nucleus are located in the ventral region (). Nucleus ambiguous innervates the muscles of the oral cavity, larynx, and pharynx through the trigeminal, facial, glossopharyngeal, vagus, and accessory nerves (Petko and Tadi, 2023; ), The nucleus tractus solitary can receive incoming information from the nucleus doubtful and then send efferent fibers to the corresponding muscles, but mainly integrates information from higher cortical centers and peripheral sensory afferents and regulates swallowing according to the nature of the food bolus (; Ye et al., 2024). Overall (see Figure 1), the swallowing central pattern generator is responsible for the formation and regulation of swallowing motor sequences, processing incoming information, generating preprogrammed swallowing responses, and distributing appropriate signals to the motor nuclei of cranial nerves and their axons, which are ultimately transmitted to the many muscles involved in swallowing (Yamamoto et al., 2022).
Figure 1
A trigeminal and facial nerve innervate the muscles of the mouth, masticatory muscles are innervated by the trigeminal nerve, while the glossopharyngeal nerve and the vagus nerve innervate the muscles of the pharynx (). In addition, the contraction of the esophageal sphincter affects the operation of swallowing, it contains the cricopharyngeal and hypopharyngeal constrictors and is innervated by the vagus nerve, while the muscularis that promote the contraction of the esophageal sphincter during swallowing, such as the suprahyoid muscles (stylohyoid, digastric, and mylohyoid muscles) and thyrohyoid muscles, are innervated by the trigeminal, facial, and hypoglossal nerves (McCarty and Chao, 2021). The recruitment of muscles necessary for the swallowing sequence is directed by the swallowing network, and integration between descending signals and afferent inputs may occur in the cortex and cerebellum, where there are multiple synaptic connections for different functions, the cerebral cortex may be responsible for the initiation of motor commands, and some cortical areas may be responsible for the integration of chewing and swallowing information, other regions, however, feed the descending signal back to the brain stem with the sensation of the bolus moving along the swallowing channel (). Although movement is directed by the cortex, the cerebellum is also associated with movement and plays a key role in the balanced coordination of muscle movements (Roostaei et al., 2014). Influences the cortical swallowing module consisting of primary motor, auxiliary motor, primary sensory cortical areas, and cingulate gyrus (Sasegbon and Hamdy, 2023).
The term “neurogenic dysphagia” refers to dysphagia, or dysfunction of swallowing mechanisms, in patients who have suffered a neurologic insult or disease (Teismann et al., 2007). Such diseases include stroke, Parkinson’s disease, and multiple sclerosis, among other neurodegenerative disease processes (). Dysphagia following stroke primarily stems from cerebral cortex and subcortical structures damage, affecting areas like the motor cortex, cerebellum, thalamus, and other parts, as well as sensory defects of the pharyngeal mucosa (Teismann et al., 2007; Qin et al., 2023). It is characterized by a delayed or absent swallowing reflex and a premature overflow of bolus (Labeit et al., 2023), pharyngeal food residues and pharyngeal motility disorders (Warnecke et al., 2021). A dysphagia caused by Parkinson’s disease is different from dysphagia caused by stroke because it is primarily caused by problems with the brainstem, muscle atrophy, and dopaminergic and non-dopaminergic mechanisms (Patel et al., 2020). The patient presented with hypoesthesia of the pharynx, food residue, and bradykinesia of the oropharynx (Labeit et al., 2020a), the swallowing reflex was impaired, and the bolus overflowed prematurely (Labeit et al., 2020b). The pathological mechanisms of dysphagia in multiple sclerosis include damage of cortical bulbar fibers alone or in combination, damage of the brainstem swallowing center, abnormalities of the cerebellum affecting the accuracy of sequential planning and coordination of swallowing, failure of the afferent nerve central sensory pathway and abnormal impairment of the central motor pathway (). Its dysfunction may occur at any stage of swallowing and cause various complications such as aspiration pneumonia, malnutrition and airway obstruction ().
3 Physical therapy
3.1 Neuromuscular electrical stimulation
The purpose of NMES is to stimulate peripheral nerves associated with paralyzed pharyngeal muscles with low-frequency electrical stimulation, aiming to enhance their functionality (). In simpler terms, the effects of NMES on swallowing are improved through the contraction of pharyngeal muscles (). Laryngeal elevation and reduction resulting from pharyngeal muscle defects are the primary causes of dysphagia in stroke patients, leading to potential issues such as aspiration and pharyngeal residue (). Therefore, the NMES therapy is considered one of the most effective treatments for dysphagia caused by stroke (). Moreover, patients with Parkinson’s disease often use NMES as a form of physical therapy to improve tongue muscle weakness (Park et al., 2018).
Preliminary studies indicated that increased tongue power results in greater activation of the suprahyoid muscle during swallowing (Oh, 2016). This goal can be achieved by NMES, by depolarizing motor axons and activation of type II fast-twitch muscle fibers in neuromuscular tissues, either through peripheral nerves or muscle belly (; ). In patients with brain injury-related dysphagia, the NMES strengthens both suprahyoid and infrahyoid muscles, along with the muscles that assist in swallowing (Seo et al., 2021). Moreover, the long-term application of NMES benefits the recovery of swallowing-related cortical neuroplasticity in stroke patients (Zhang et al., 2022). Given the loss of swallowing motor control in stroke patients, functional muscle contraction patterns are primarily re-educated during NMES (Miller et al., 2022). This entails triggering the peripheral neuromuscular system via external electrical stimulus, depolarizing cervical muscle nerve fibers, and initiating oropharyngeal muscle contraction to improve swallowing function (Wang et al., 2023). In addition, it shows promise in improving dysphagia associated with other diseases such as Parkinson’s disease and head and neck cancer, in similar ways to how NMES improves dysphagia associated with strokes, it stimulates the nerve and motor endplates of the nerve (Tan et al., 2013).
In the application of NMES, electrodes are typically positioned on the hyoid muscles or adjacent areas, utilizing a frequency range of 25 to 120 Hz (Miller et al., 2022). Recent research findings, as summarized in Table S1, suggest the optimal treatment duration for NMES is generally between 20 to 30 min, with an application frequency of 80 Hz, and electrodes placed on the hyoid muscles (Miller et al., 2022). At present, studies consistently demonstrate that NMES improves swallowing function in patients suffering from neurogenic dysphagia, attributed to the following factors: (1) stimulation of the tongue, orbicular oris muscles, and other related muscles to promote the development of normal movement patterns and enhance organ and muscle functions; (2) alteration in the excitability of the pharyngeal cortex to promote normal swallowing mode operation; (3) activation of the swallowing center, facilitating the functional reconstruction of the nervous system (Konecny and Elfmark, 2018; Meng et al., 2018; Zeng et al., 2018; Oh et al., 2020).
In summary (see Figure 2), the NMES stimulates the depolarization of the axons below the electrode, and the depolarization signal of motor axons propagates from the stimulation site to the muscle (peripheral pathway) to produce contraction, which can induce the neural plasticity of the central nervous system and enhance the neuromuscular function after nervous system injury (). A NMES consists of muscle reeducation primarily focused on improving swallowing function by facilitating normal swallowing mode operation ().
Figure 2
3.2 Sensory stimulation
Sensory stimulation plays a crucial role in promoting the rehabilitation of swallowing function (
Ice stimulation therapy uses repetitive mechanical, pressure, and temperature stimulation to enhance the sensitivity of the soft palate and pharynx. By increasing the sensory sensitivity of local nerves, ice stimulation prompts local muscles contraction and triggers the swallowing reflex (Li et al., 2017). Consequently, ice stimulation mobilizes resting neuron excitability, reconstructs the neural network to achieve functional reorganization, promotes the normal swallowing reflex, and restores the function of swallowing organs (
The improvement of dysphagia through acid stimulation may be attributed to sensory feedback information (Logemann et al., 1995). Previous studies investigating neurogenic swallowing dysfunction found that subjects consuming water with a citric acid concentration of 2.7%, compared to plain water, exhibited increased spontaneous swallowing and reduced aspirations, leading to an improvement in swallowing function (Pelletier and Lawless, 2003). Wang et al. (2022) reported an effective acid stimulation medium for treating dysphagia in stroke patients. This method entailed applying vitamin C tablet powder (0.2 g/day) to the patient’s bilateral tongue using a cotton swab, followed by swallowing practice instructions. Additionally, tongue massage with the cotton swab and guidance for tongue and masticatory muscle exercises were included (5–6 times per day, 15 min each time for 2 weeks). Acid stimulation promotes saliva secretion by stimulating the tongue, thereby accelerating the swallowing process and relieving swallowing disorders (Wang et al., 2022). Acid stimulation effectively improves stroke dysphagia based on two fundamental principles. Furthermore, acid stimulation increases the activity intensity of swallowing-related muscles such as the mylohyoid and front belly of the digastric muscles, triggering stronger contractions during swallowing and consequently improving dysphagia (Palmer et al., 2005).
Carbonation stimulation is also considered to be a beneficial sensory stimulation technique for improving dysphagia, primarily by enhancing the contractility of the velum and oropharynx (Omari et al., 2020) as well as prolonging the opening duration of the upper esophageal sphincter (Miura et al., 2009). A recent study conducted by Morishita et al. (2023) has suggested that carbonation may induce changes in brain excitability, resulting in shorter swallowing times in healthy individuals consuming carbonated beverages. Additionally
In summary (see Figure 2), the intensity and duration of the swallowing response can be triggered or regulated by a complex biofeedback mechanism, sensory stimulation transmit signals mainly through the trigeminal, facial, glossopharyngeal and vagus nerves, which on the one hand directly reach the swallowing central pattern generator, and on the other hand, transmit signals to the cerebral cortex, which outputs information to the swallowing central pattern generator for integration and tissue, the swallowing response is facilitated (
3.3 Repetitive transcranial magnetic stimulation
The technique of rTMS involves placing a coil to the head to generate a magnetic field when an electric current passes through it, this magnetic field induces current flows within brain tissue perpendicular to its direction, which are of strong strength to induce modifications in both cortical and subcortical white matter axons (Ridding and Rothwell, 2007). The rTMS can either suppress or excite neuronal activity depending on the frequency used: frequencies at or below 1 Hz suppress neuronal activity, while those above 5 Hz elicit neuronal excitation (
There is evidence that rTMS alters cortical excitability, regulates neurotransmitter release, and promotes neuroplasticity in the brain (
In summary (see Figure 2), the cerebral cortex and cerebellum are the primary stimulation targets for rTMS in dysphagia, it uses electromagnetic induction to depolarization synapses and accelerate the operation of swallowing circuit through changes in neuroplasticity, so as to improve swallowing function (Speyer et al., 2022; Labeit et al., 2024).
3.4 Transcranial direct current stimulation
The tDCS technique is a groundbreaking method of non-invasive brain stimulation (Pisegna et al., 2016) that involves applying small electrical currents (1–2 mA) through two surface electrodes, the anode electrode and cathode electrode, to targeted brain regions, thereby triggering and modulating brain activity (
Neuroplasticity is the concept behind tDCS, which is a form of noninvasive brain stimulation (
In general (see Figure 2), the treatment principle of tDCS can improve dysphagia in a variety of diseases (Lefaucheur, 2016). Its current directly stimulates the brain or cerebellum and changes the polarity of nerve cells, aiming to trigger and promote neuroplasticity and improve dysphagia (Speyer et al., 2022; Labeit et al., 2024).
4 Summary and prospect
Neurogenic dysphagia is currently managed with motor training, oral medications, and surgery (
Considering the increasing public interest in neurogenic dysphagia, it is crucial to also address its effects on individuals with schizophrenia. Future research should prioritize investigating the pathogenesis of dysphagia in schizophrenia, exploring the effectiveness of physical therapy interventions, and identifying the most suitable therapy targets for this specific population.
Statements
Author contributions
KL: Conceptualization, Writing – review & editing, Funding acquisition, Supervision. CF: Writing – review & editing, Conceptualization, Writing – original draft. ZX: Writing – review & editing. JZ: Writing – original draft. CZ: Investigation, Writing – original draft. RL: Investigation, Writing – original draft. CG: Supervision, Writing – review & editing. JW: Writing – original draft. CX: Writing – review & editing, Investigation. YZ: Writing – review & editing. WD: Writing – review & editing.
Funding
The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This study was supported by Medical and Health Science and Technology Development Plan of Shandong Province (No. 202303090378); Key Research Plan of Jining City (No. 2023YXNS006).
Acknowledgments
We appreciate the help of the Home for Researchers website in drawing, writing, etc.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Supplementary material
The Supplementary material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fnhum.2024.1404398/full#supplementary-material
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Summary
Keywords
Parkinson’s disease, stroke, schizophrenia, dysphagia, neuromuscular electrical stimulation, repetitive transcranial magnetic stimulation, sensory stimulation, transcranial direct current stimulation
Citation
Li K, Fu C, Xie Z, Zhang J, Zhang C, Li R, Gao C, Wang J, Xue C, Zhang Y and Deng W (2024) The impact of physical therapy on dysphagia in neurological diseases: a review. Front. Hum. Neurosci. 18:1404398. doi: 10.3389/fnhum.2024.1404398
Received
28 March 2024
Accepted
28 May 2024
Published
06 June 2024
Volume
18 - 2024
Edited by
Elisa Kallioniemi, New Jersey Institute of Technology, United States
Reviewed by
Maja Rogić Vidaković, University of Split, Croatia
Anna-Lisa Schuler, Max Planck Institute for Human Cognitive and Brain Sciences, Germany
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© 2024 Li, Fu, Xie, Zhang, Zhang, Li, Gao, Wang, Xue, Zhang and Deng.
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*Correspondence: Kun Li, likunyjs@163.com; Wei Deng, dengw@zju.edu.cn
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