The impact of physical therapy on dysphagia in neurological diseases: a review

Frontiers in Human Neuroscience 01 frontiersin.org

The impact of physical therapy on

dysphagia in neurological

diseases: a review

KunLi

*, CuiyuanFu

, ZhenXie

, JiajiaZhang

ChenchenZhang

, RuiLi

, CaifengGao

, JiahuiWang

ChuangXue

, YuebingZhang

and WeiDeng

3,4

Shandong Daizhuang Hospital, Jining, China,

Department of Psychology, Xinxiang Medical

University, Xinxiang, China,

Aliated Mental Health Center and Hangzhou Seventh People’s Hospital,

Zhejiang University School of Medicine, Hangzhou, China,

Liangzhu Laboratory, MOE Frontier

Science Center for Brain Science and Brain-machine Integration, State Key Laboratory of Brain-

Machine Intelligence, Zhejiang University, Hangzhou, China

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 aected individuals and causes additional burdens, such as malnutrition,

aspiration pneumonia, asphyxia, or even death from choking due to improper

eating. Physical therapy oers a non-invasive treatment with high ecacy

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 eectiveness 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.

KEYWORDS

Parkinson’s disease, stroke, schizophrenia, dysphagia, neuromuscular electrical

stimulation, repetitive transcranial magnetic stimulation, sensory stimulation,

transcranial direct current stimulation

1 Introduction

ere 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 (Hurtte etal.,

2023). e 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 (El Halabi etal., 2023). e number of people suering

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,

OPEN ACCESS

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

*CORRESPONDENCE

Kun Li

[email protected]

Wei Deng

[email protected]

RECEIVED 28 March 2024

ACCEPTED 28 May 2024

PUBLISHED 06 June 2024

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

Wang, Xue, Zhang and Deng. This is an

open-access article distributed under the

terms of the Creative Commons Attribution

License (CC BY). The use, distribution or

reproduction in other forums is permitted,

provided the original author(s) and the

original publication in this journal is cited, in

accordance with accepted academic

practice. No use, distribution or reproduction

is permitted which does not comply with

these terms.

TYPE Review

PUBLISHED 06 June 2024

DOI 10.3389/fnhum.2024.1404398

Li et al. 10.3389/fnhum.2024.1404398

Frontiers in Human Neuroscience 02 frontiersin.org

Parkinson’s disease, amyotrophic lateral sclerosis, multiple sclerosis,

and other forms of neurodegeneration (Chandran and Doucet, 2024).

It is a common complication of stroke to experience dysphagia

aerward, it is estimated that 20–43% of patients have persistent

dysphagia aer 3 months, which can lead to aspiration pneumonia,

malnutrition, water and electrolyte disorders, and other complications

(Chen etal., 2024). ere 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

aect the quality of life and even cause death (Dashtelei etal., 2024).

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) (Alvarez-Berdugo et al., 2016;

Miller etal., 2022; Li etal., 2023). However, there remains paucity of

discourse on the application of physical therapy in dysphagia

management in dierent diseases. e 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 (Dodds etal., 1990). It involves various

levels of the central nervous system, from the cortex to the medulla, as

well as multiple cranial and peripheral nerves (El Halabi etal., 2023).

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) aerent motor bers in cranial nerves and ansa

cervicalis; (2) aerent sensory bers in cranial nerves; (3) bers 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 (Dodds et al., 1990). In the swallowing

process, ber transmitters transmit signals from peripheral nerves and

the cerebral cortex to the swallowing centers in the brain stem

(Hashimoto etal., 2019). ere 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 (Jang and Kim, 2021). 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; Chandran and Doucet, 2024),

e nucleus tractus solitary can receive incoming information from

the nucleus doubtful and then send eerent bers to the corresponding

muscles, but mainly integrates information from higher cortical

centers and peripheral sensory aerents and regulates swallowing

according to the nature of the food bolus (Chandran and Doucet, 2024;

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).

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 (Costa, 2018). In addition, the contraction of the esophageal

sphincter aects 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). e recruitment of muscles necessary for

the swallowing sequence is directed by the swallowing network, and

integration between descending signals and aerent inputs may occur

in the cortex and cerebellum, where there are multiple synaptic

connections for dierent 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 (Cheng etal., 2022). 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). Inuences the cortical swallowing module consisting of

primary motor, auxiliary motor, primary sensory cortical areas, and

cingulate gyrus (Sasegbon and Hamdy, 2023).

e term “neurogenic dysphagia” refers to dysphagia, or

dysfunction of swallowing mechanisms, in patients who have suered

a neurologic insult or disease (Teismann etal., 2007). Such diseases

include stroke, Parkinson’s disease, and multiple sclerosis, among

other neurodegenerative disease processes (Chandran and Doucet,

2024). Dysphagia following stroke primarily stems from cerebral

cortex and subcortical structures damage, aecting 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 reex and

a premature overow 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 dierent 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). e patient presented with

hypoesthesia of the pharynx, food residue, and bradykinesia of the

oropharynx (Labeit etal., 2020a), the swallowing reex was impaired,

and the bolus overowed prematurely (Labeit et al., 2020b). e

pathological mechanisms of dysphagia in multiple sclerosis include

damage of cortical bulbar bers alone or in combination, damage of

Li et al. 10.3389/fnhum.2024.1404398

Frontiers in Human Neuroscience 03 frontiersin.org

the brainstem swallowing center, abnormalities of the cerebellum

aecting the accuracy of sequential planning and coordination of

swallowing, failure of the aerent nerve central sensory pathway and

abnormal impairment of the central motor pathway (Alfonsi etal.,

2013). Its dysfunction may occur at any stage of swallowing and cause

various complications such as aspiration pneumonia, malnutrition

and airway obstruction (Ansari etal., 2020).

3 Physical therapy

3.1 Neuromuscular electrical stimulation

e purpose of NMES is to stimulate peripheral nerves associated

with paralyzed pharyngeal muscles with low-frequency electrical

stimulation, aiming to enhance their functionality (Doucet et al.,

2012). In simpler terms, the eects of NMES on swallowing are

improved through the contraction of pharyngeal muscles (Carnaby

et al., 2020). 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 (Bath etal., 2018). erefore, the NMES therapy

is considered one of the most eective treatments for dysphagia

caused by stroke (Beom et al., 2011). Moreover, patients with

Parkinson’s disease oen 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). is goal can beachieved by NMES, by depolarizing motor axons

and activation of type II fast-twitch muscle bers in neuromuscular

tissues, either through peripheral nerves or muscle belly (Carnaby etal.,

2020; Carson and Buick, 2021). 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 benets 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). is entails triggering

the peripheral neuromuscular system via external electrical stimulus,

depolarizing cervical muscle nerve bers, 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 ndings, 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 suering 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).

FIGURE1

The mechanism of swallowing. As part of the swallowing central program generator, the nucleus ambiguous receives relevant cranial nerve stimulation

and the nucleus tractus solitarius receives cortical and peripheral sensory input, after receiving the signal, the swallowing-related muscles are

stimulated to promote the normal swallowing process (Yamamoto etal., 2022). (A) The swallowing center’s operation. (B) Swallowing muscles. (C) A

normal swallowing process; NTS, Nucleus tractus solitarius; CPG, Central program generator; NA, Nucleus ambiguous; V, Trigeminal nerve; VII, Facial

nerve; IX, Glossopharyngeal nerve; X, Vagus nerve; XI, Accessory nerve.

Li et al. 10.3389/fnhum.2024.1404398

Frontiers in Human Neuroscience 04 frontiersin.org

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

aer nervous system injury (Bergquist etal., 2011). A NMES consists of

muscle reeducation primarily focused on improving swallowing function

by facilitating normal swallowing mode operation (Jeon etal., 2020).

3.2 Sensory stimulation

Sensory stimulation plays a crucial role in promoting the

rehabilitation of swallowing function (Cola et al., 2012). Normal

swallowing relies on somatosensory inputs associated with trigeminal,

glossopharyngeal, and vagus nerves (Jean, 2001). When the sensory

information pathway is impaired, reduced sensory input can slow

down the swallowing-cortical pathway, resulting in dysphagia

(Teismann etal., 2007). Sensory stimulation of the cranial nerves

enhances the transmission of information to the solitary tract nucleus

in the brainstem (Alvarez-Berdugo etal., 2016). is, in turn, increases

the sensory input to the nucleus tract solitary in the brainstem through

cranial nerves, promoting the operation of normal swallowing pattern,

and ultimately improving swallowing function (Jean, 2001). Common

sensory stimulation methods include ice, acid, and carbonation

stimulation (Regan, 2020).

Ice stimulation therapy uses repetitive mechanical, pressure, and

temperature stimulation to enhance the sensitivity of the so palate

and pharynx. By increasing the sensory sensitivity of local nerves, ice

stimulation prompts local muscles contraction and triggers the

swallowing reex (Li et al., 2017). Consequently, ice stimulation

mobilizes resting neuron excitability, reconstructs the neural network

to achieve functional reorganization, promotes the normal swallowing

reex, and restores the function of swallowing organs (Ilott etal.,

2016). In the application of ice stimulation therapy Nakamura and

Fujishima (2013) dipped a cotton stick about 10 cm long and 1.27 cm

in diameter into the water until it froze into a frozen sucker, then

lightly rubbed and pressed it against the posterior tongue, bottom of

the tongue, and posterior pharyngeal wall of stroke patients with

dysphagia for 10 s, results revealed that ice stick massage could shorten

the threshold of the swallowing response phase. Kawakami et al.

(2019) demonstrated that placing an ice stick in the mouth is superior

to placing it on the neck. Intraoral ice stimulation signicantly can

increase the excitability of the swallowing pathway in the cortex,

trigger swallowing initiation, and shorten the duration of the

pharyngeal phase. Early rehabilitation of stroke patients with dysphagia

is closely related to the central nervous system’s ability to compensate

and reconstruct injured areas, thereby increasing the excitability of the

nervous system and facilitating swallowing by activating the central

nervous system to form new sensory and motor projections (Qin etal.,

2019). At this point, when applied to stroke-related dysphagia, ice

stimulation’s eects primarily manifest in two ways. Firstly, it activates

sensory nerve bers, boosts sensory recovery, and restores the neural

network (Ferrara etal., 2018). Secondly, it enhances sensory sensitivity.

By increasing the sensitivity of the swallowing reex area, it amplies

sensory inputs before swallowing, induces the generation of swallowing

reex, and nally improves swallowing function (Cui etal., 2020).

e 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 eective acid stimulation medium for treating dysphagia

in stroke patients. is method entailed applying vitamin C tablet

FIGURE2

Improvement of dysphagia by physical therapy. Depolarization of axons is induced by NMES, which induces swallowing muscle contraction and

improves swallowing (Bergquist etal., 2011). On the other hand, it can stimulate the excitability of the pharyngeal cortex, induce the operation of the

central pattern generator, and improve swallowing (Zeng etal., 2018). Sensory stimulation transmits signals through the cranial nerves, on the one hand,

directly to the central pattern generator, and on the other hand, it transmits signals to the cerebral cortex, where it is integrated and organized, and ﬁnally

promotes the swallowing response (Alvarez-Berdugo etal., 2016). A change in neural plasticity is used to accelerate the operation of swallowing circuits

through rTMS, which uses electromagnetic induction to depolarize synapses, ultimately improving swallowing (Labeit etal., 2024). Dysphagia can

beimproved by tDCS because it alters nerve cell polarity and triggers neuroplasticity (Speyer etal., 2022). NMES: Neuromuscular electrical stimulation;

tDCS, Transcranial direct current stimulation; rTMS, Repetitive transcranial magnetic stimulation, CPG, Central pattern generator; C, Carbonation.

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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 eectively

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 benecial

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

Bülow et al. (2003) demonstrated that carbonation stimulation

eectively reduces airway aspiration and pharyngeal retention, and

shortens the duration of the pharyngeal phase duration. Sdravou etal.

(2012) conducted an experiment involving carbonation stimulation in

17 patients with neurogenic dysphagia, conrming that drinking

carbonated water can reduce aspiration. e eectiveness of

carbonation in improving swallowing function can beattributed to

two main factors. On the one hand, it is related to the activation of

swallowing pathways. Stimulation of peripheral sensory receptors and

sensory bers in the nucleus tractus solitarius in the brainstem

activates the pattern generator of the swallowing center (Nagano etal.,

2022). On the other hand, carbonation aects numerous receptors in

the larynx, namely mechanoreceptors, chemoreceptors, pain receptors,

and thermoreceptors, which respond to carbonation stimulation by

triggering protective reexes to prevent aspiration (Bradley, 2000).

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 (Alvarez-Berdugo etal., 2016).

3.3 Repetitive transcranial magnetic

stimulation

e technique of rTMS involves placing a coil to the head to

generate a magnetic eld when an electric current passes through it, this

magnetic eld induces current ows within brain tissue perpendicular

to its direction, which are of strong strength to induce modications in

both cortical and subcortical white matter axons (Ridding and Rothwell,

2007). e 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

(Honda etal., 2021). Studies on healthy participants have investigated

the eects of rTMS on the pharyngeal motor cortex (Yamamura etal.,

2018). Findings indicate that rTMS at 1 Hz inhibits the excitability of

the pharyngeal motor cortex, whereas high-frequency stimulation, such

as 10 Hz stimulation of the cerebellar hemisphere increases the

amplitude of pharynx cortical motor evoked potentials (Vasant etal.,

2015; Sasegbon et al., 2020b). Due to its potential neural repair

mechanisms, dysphagia has been treated extensively with rTMS

(Sasegbon et al., 2020a). Recent schemes for rTMS treatment of

dysphagia are summarized in Table S2. According to Table S2, treatment

with rTMS focuses primarily on the cerebellum and pharyngeal motor

cortex. High frequencies are predominantly used for treatment

frequency, and the treatment time is mostly selected daily, 5 days a week,

for a total of 2 weeks, and the swallowing function test results are

improved (Dong etal., 2022; Rao etal., 2022; Zhong etal., 2023).

ere is evidence that rTMS alters cortical excitability, regulates

neurotransmitter release, and promotes neuroplasticity in the brain

(Kesikburun, 2022). e increase in cortical activity in the cerebral

hemispheres is associated with functional recovery in stroke patients

with dysphagia, and the reorganization of neural networks plays a

signicant role in the recovery of swallowing function (Hoogendam

etal., 2010). e changes in neuroplasticity are closely related to rTMS

induced synaptic connections in the process of regulating the

functional state of the cerebral cortex (Li etal., 2022). ere is no

single target for rTMS treatment of stroke dysphagia; rather, it involves

the regeneration of swallowing function in stroke patients through the

cooperative action of multiple brain areas (Dong etal., 2022). Aer

virtual lesion simulation in stroke patients with dysphagia, cerebellar

high frequency rTMS not only improves the excitability of the

pharyngeal motor cortex in healthy volunteers (Sasegbon etal., 2019,

2020b) but also improves swallowing function among stroke patients

with dysphagia (Zhong etal., 2023). is may beexplained by the fact

that the cerebellum is connected to the brainstem by three cerebellar

peduncles, which directly communicate with the various motor nuclei

of the brainstem (Roostaei etal., 2014). Based on the evidence that

rTMS could improve not only swallowing disorder but also motor

function, Khedr etal. applied rTMS to Parkinson’s disease patients

with dysphagia and achieved the envisaged results: Parkinson’s disease

patients could benet from rTMS for dysphagia (Khedr etal., 2019).

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

e 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 (He etal., 2022). In

recent years, there has been strong interest in tDCS as an eective,

noninvasive method to treat dysphagia (Cheng etal., 2021). Table S3

shows the application of tDCS in dysphagia treatment in recent years.

It can beseen from the table that tDCS is mostly used for stroke-

related dysphagia. e location of the anode is related to the area

involved in the pharyngeal motor cortex. e cathodes are mostly

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placed in the contralateral supraorbital region and the opposite

shoulder, most single intervention sessions last 20 min, the treatment

eect can generally achieve the improvement of swallowing function

(Farpour etal., 2023; El Nahas etal., 2024).

Neuroplasticity is the concept behind tDCS, which is a form of

noninvasive brain stimulation (Kesikburun, 2022). e swallowing

motor task-related activities of the brain are enhanced through

glutamatergic and calcium-dependent processes, including

synaptogenesis, reorganization, strengthening, and inhibition of brain

networks (Pisegna etal., 2016; Tedesco Triccas etal., 2016). Anodal

tDCS can improve swallowing function by stimulating the pharyngeal

motor cortex in patients with Parkinson’s disease, which is associated

with an increase in the strength of synaptic connections related to

deglutition in the cerebral cortex (Tedesco Triccas et al., 2016).

Dysphagia can also beameliorated by tDCS in older adults with and

without neurological conditions, which is associated with the induction

of a polar-dependent shi in underlying cortical excitability, as well as

a broad activation of pharyngeal motor cortex in both brain hemispheres

(Cosentino etal., 2020). Furthermore, stroke patients oen choose

tDCS as a treatment for dysphagia, with numerous therapeutic targets

(Gómez-García et al., 2023), related to the regions involved in the

swallowing network and the fact that tDCS promotes neuroplasticity

(Ahn et al., 2017). For example, enhancing the excitability of the

uninjured side of the swallowing cortex, the injured side of the

swallowing cortex, the bilateral swallowing cortex, and the superior

limbic gyrus can be benecial for enhancing swallowing function

(Wang etal., 2020; Mao etal., 2022; Farpour etal., 2023). Dysphagia in

stroke patients can be eectively improved by tDCS, and anodal

stimulation of the right swallowing cortex in patients with multiple

sclerosis dysphagia can also improve swallowing function, as anodal

stimulation of the swallowing motor cortex of the right also activates an

extensive network involving the contralateral hemisphere to compensate

for the damage caused by focal brain injury (Cosentino etal., 2018).

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 (El Halabi et al., 2023). Clinical

evidence supports the use of movement training for mild-to-

moderate dysphagia (Saconato et al., 2016), with strong

recommendations from intermediate and high-level evidence

sources (Medicine DRCO, 2023; Yang etal., 2023). Patients with

severe dysphagia typically undergo medical or surgical interventions,

especially at intermediate and advanced disease stages (Cotaoco

etal., 2024). While conventional treatments may take longer to reach

full ecacy, physical therapy has emerged as a non-invasive and

practical approach to shorten treatment duration for dysphagia

patients (Frost et al., 2018; Bengisu et al., 2024). is review

elucidates the physiological function of the swallowing system, the

pathological mechanisms of neurogenic dysphagia, and the

principles and application of physical therapy. Overall, physical

therapy oers benets to individuals with neurogenic dysphagia by

enhancing swallowing recovery, improving treatment outcomes, and

enhancing quality of life (Banda etal., 2023; Bengisu etal., 2024).

Considering the increasing public interest in neurogenic

dysphagia, it is crucial to also address its eects on individuals with

schizophrenia. Future research should prioritize investigating the

pathogenesis of dysphagia in schizophrenia, exploring the eectiveness

of physical therapy interventions, and identifying the most suitable

therapy targets for this specic population.

Author contributions

KL: Conceptualization, Writing – review & editing, Funding

acquisition, Supervision. CF: Writing – review & editing,

Conceptualization, Writing – original dra. ZX: Writing – review &

editing. JZ: Writing – original dra. CZ: Investigation, Writing –

original dra. RL: Investigation, Writing – original dra. CG:

Supervision, Writing – review & editing. JW: Writing – original dra.

CX: Writing – review & editing, Investigation. YZ: Writing – review

& editing. WD: Writing – review & editing.

Funding

e author(s) declare that nancial support was received for the

research, authorship, and/or publication of this article. is 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

e authors declare that the research was conducted in the

absence of any commercial or nancial relationships that could

beconstrued as a potential conict 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 aliated 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

e Supplementary material for this article can befound online

at: https://www.frontiersin.org/articles/10.3389/fnhum.2024.1404398/

full#supplementary-material

Li et al. 10.3389/fnhum.2024.1404398

Frontiers in Human Neuroscience 07 frontiersin.org

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