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DYSPHAGIA ASSESSMENT AND TREATMENT PLANNING: A TEAM APPROACH
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DYSPHAGIA ASSESSMENT AND TREATMENT PLANNING: A TEAM APPROACH
ADDENDUM 10–2
New Applications for Old Technology in Dysphagia
Rehabilitation:
Madeline Mills and Maggie-Lee Huckabee
sEMG Biofeedback
Surface electromyography (sEMG) has
been used as an adjunct to dysphagia
rehabilitation for decades. Reports of
sEMG in the literature have historically focused on its application as a
biofeedback modality during execution
of strengthening exercises for swallowing (Bogaardt et al., 2009; Bryant, 1991;
Crary, 1995; Crary et al., 2004; Huckabee & Cannito, 1999). In this approach,
surface electrodes are placed on the skin
overlying targeted muscles and provide a visual representation of degree
of muscle activation. Swallowing with
greater effort produces a higher-amplitude sEMG waveform, allowing the
patient clear feedback regarding the
relative strength of muscle contraction
(Bogaardt et al., 2009; Bryant, 1991;
Crary, 1995; Crary et al., 2004; Huckabee & Cannito, 1999).
A shift in understanding of swallowing from a brainstem-driven reflex to a
cortically modulated skill has prompted
a more recent and alternative approach
to rehabilitation. Swallowing skill training (Huckabee & Burnip, 2018; Huckabee & Lamvik-Gozdzikowska, 2019)
proposes to acquire (or reacquire) skill
in swallowing through functional repetition and refinement of motor task
execution, enlisting cortical modulation and adaptive practice (Huckabee
& Macrae, 2014). Three key factors provide a foundation to optimize motor
relearning, including (a) specificity of
practice, (b) task challenge, and (c)feedback (Zimmerman et al., 2020). Several
diverse approaches to skill training that
incorporate these factors have been
described in the literature. MartinHarris et al. (2015) used respiratoryrelated feedback and a systematic
protocol to train improvements in
respiratory-swallowing coordination
in patients with head and neck cancer. Huckabee et al. (2014) successfully
used pharyngeal manometry as a biofeedback tool to rehabilitate pharyngeal
sequencing in patients who presented
with this skill-based deficit. Key features in skill-based training are the use
of impairment specific feedback and
protocols that are designed with principles of neuroplasticity in mind.
This skill-training approach has
also provided a new purpose for the
old technology of sEMG biofeedback.
Whereas previously the time by amplitude waveform available through
sEMG biofeedback was used to maximize force generation during swallowing, swallowing skill training uses this
information to refine precision in motor
control. The Biofeedback in Strength
and Skill Training (BiSSkiT) software
and treatment protocol was initially
developed as a research tool to explore
sEMG biofeedback approaches for
swallowing skill training. Although the
software contains treatment protocols
for both strength- and skill-based train-
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ing, the more novel approach addresses
skill training.
Prior to beginning a skill-training
session, patients complete a series of
calibration swallows, allowing the
software to identify a relatively moderate range of sEMG muscle activation
between 30% and 70% of maximal force
generation. During skill-training exercise, a visual target is placed randomly
on the screen, but within this calibrated range. This ensures that the targets are high enough from baseline to
register swallowing behavior but also
not within the “effortful swallowing”
range of muscle contraction. Patients
then execute a series of swallowing
trials, which are displayed as a time-byamplitude sEMG waveform and given
the instructions to perform swallows
such that “the peak of the waveform
falls within the target” (Athukorala
etal., 2014, p. 1376). Using the waveform and additional visual feedback
regarding error in both amplitude
and temporal aspects of swallowing,
patients modulate behavior to increase
precision in motor control. The size of
the target adapts over trials depending
on patient performance, either decreasing in size to require increased precision
(after three consecutive “hits” of the
target) or increasing in size (after three
consecutive “misses”) to provide more
positive feedback. Approaches to sEMG
biofeedback in skill-based dysphagia
therapy have been the focus of earlier
studies, including work by Stepp et al.
(2011). Similar to BiSSkiT skill training,
participants were required to modulate
muscle activation in their anterior neck
to manipulate a simple video game on
a computer screen. However, this task
did not require physiologic swallowing, omitting an opportunity to opti-
mize the specificity of the skill-training
task, which is known to promote neural plasticity (Kleim & Jones, 2008).
In requiring the patient to swallow,
BiSSkiT incorporates this task-specific
principle of neural plasticity and promotes the goal of acquiring swallowing
as a skill.
Specific BiSSkiT treatment protocols
are yet to be formally established across
etiologies and impairment levels, but
the automatic adaptation of task difficulty relative to real-time patient performance promotes a task challenge
that is individualized to each patient.
Frequency of sessions and number of
swallowing repetitions to maximize
recovery vary in the reported literature, are yet to be empirically defined,
and, indeed, may ultimately need to
be adapted for the individual needs
of the patient. Indications for the use
of BiSSkiT coincide with indications
for strength- or skill-training therapeutic approaches, that is, in the presence of suspected muscle weakness or
impaired motor planning, respectively.
Due to its integral role in this technology, the limitations of sEMG extend to
BiSSkiT. sEMG displays a measure of
muscle activation, not swallowing specifically. As such, care is required to
appropriately differentiate swallows
from other submental muscle activity
such as tongue movement or hyoid stabilization when supporting patients in
completing the therapy.
Athukorala et al. (2014) investigated
the effects of BiSSkiT skill training for
individuals with dysphagia secondary
to Parkinson’s disease. These patients
(n = 10) underwent ten 1-hour BiSSkiT
skill-training sessions (once per day for
10 days over a 2-week period), completing 100 swallowing trials in each
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DYSPHAGIA ASSESSMENT AND TREATMENT PLANNING: A TEAM APPROACH
session. These 100 swallows were partitioned into five 20-swallow blocks, with
a brief break between each. Patients
demonstrated improvements in functional, biomechanical, and swallowing-related quality of life measures
posttreatment and when reassessed
after 2 weeks. An exploratory study by
Perry et al. (2018) also reported subjective and physiological improvements
in dysphagic symptoms for a patient
(n= 1) with multiple system atrophy
(cerebellar subtype) following six
1-hour BiSSkiT skill-training sessions
over a period of 6 weeks.
Though small, the evidence base for
dysphagia therapies targeting swallowing skill shows promise (Athukorala et
al., 2014; Huckabee et al., 2014; MartinHarris et al., 2015; Perry et al., 2018).
Importantly, the BiSSkiT skill-training
protocols are merely a means to an
end of targeted swallowing skill training; for this technology, supportive
research is also still early and emerging. Future studies exploring application in dysphagia secondary to other
etiologies and with larger sample sizes
will continue to support growth of this
evidence.
Readers wishing to pursue a more
in-depth study of BiSSkiT and swallowing skill training are directed to the
following papers:
n
Athukorala, R. P., Jones, R. D.,
Sella, O., & Huckabee, M. L.
(2014). Skill training for swallowing rehabilitation in patients with
Parkinson’s disease. Archives of
Physical Medicine and Rehabilitation, 95(7), 1374–1382. https://doi
.org/10.1016/j.apmr.2014.03.001
n
Huckabee, M.-L., & Macrae, P.
(2014). Rethinking rehab: Skill-
based training for swallowing
impairment. Perspectives on Swal-
lowing and Swallowing Disorders
(Dysphagia), 23(1), 46–53. https://
doi.org/doi:10.1044/sasd23.1.46
n
Huckabee, M.-L., & Burnip, E.
(2018). Still rethinking rehab: Motor learning treatment approaches
for dysphagia. Perspectives of the
ASHA Special Interest Groups, 3(13),
146–156. https://doi.org/10.1044/
2018_PERS-SIG13-2018-0006
REFERENCES
Athukorala, R. P., Jones, R. D., Sella, O., &
Huckabee, M. L. (2014). Skill training
for swallowing rehabilitation in patients
with Parkinson’s disease. Archives of
Physical Medicine and Rehabilitation, 95(7),
1374–1382. https://doi.org/10.1016/j.ap
mr.2014.03.001
Bogaardt, H. C. A., Grolman, W., & Fok-
kens, W. J. (2009). The use of biofeedback in the treatment of chronic dysphagia in stroke patients. Folia Phoniatrica et
Logopaedica, 61(4), 200–205. https://doi
.org/10.1159/000227997
Bryant, M. (1991). Biofeedback in the treat-
ment of a selected dysphagic patient.
Dysphagia, 6(3), 140–144. https://doi
.org/10.1007/BF02493516
Crary, M. A. (1995). A direct intervention
program for chronic neurogenic dysphagia secondary to brainstem stroke. Dys-
phagia, 10(1), 6–18. https://doi.org/10
.1007/bf00261273
Crary, M. A., Carnaby, G. D., Groher, M. E.,
& Helseth, E. (2004). Functional benefits
of dysphagia therapy using adjunctive
sEMG biofeedback. Dysphagia, 19(3),
160–164. https://doi.org/10.1007/s004
55-004-0003-8
Huckabee, M.-L., & Burnip, E. (2018). Still
rethinking rehab: Motor learning treatment approaches for dysphagia. Perspec-
10. THE TREATMENT PLAN: BEHAVIORAL APPROACHES
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tives of the ASHA Special Interest Groups,
3(13), 146–156. https://doi.org/10.1044/
2018_PERS-SIG13-2018-0006
Huckabee, M.-L., & Cannito, M. P. (1999).
Outcomes of swallowing rehabilita-
tion in chronic brainstem dysphagia:
A retrospective evaluation. Dysphagia,
14(2), 93–109. https://doi.org/10.1007/
PL00009593
Huckabee, M.-L., Lamvik, K., & Jones, R.
(2014). Pharyngeal mis-sequencing in
dysphagia: Characteristics, rehabilitative
response, and etiological speculation.
Journal of the Neurological Sciences, 343(1),
153–158. https://doi.org/10.1016/j.jns
.2014.05.064
Huckabee, M.-L., & Lamvik-Gozdzikowska,
K. (2018). Reconsidering rehabilitation
for neurogenic dysphagia: Strengthen-
ing skill in swallowing. Current Physi-
cal Medicine and Rehabilitation Reports,
6(3), 186–191. https://doi.org/10.1007/
s40141-018-0193-x
Huckabee, M.-L., & Macrae, P. (2014).
Rethinking rehab: Skill-based training
for swallowing impairment. Perspectives
on Swallowing and Swallowing Disorders
(Dysphagia), 23(1), 46–53. https://doi
.org/ doi:10.1044/sasd23.1.46
Kleim, J. A., & Jones, T. A. (2008). Principles
of experience-dependent neural plastic-
ity: implications for rehabilitation after
brain damage. Journal of Speech, Lan-
guage, and Hearing Research, 51(1), S225–
S239. https://doi.org/10.1044/1092-43
(2008/018)
Martin-Harris, B., McFarland, D., Hill, E. G.,
Strange, C. B., Focht, K. L., Wan, Z., Blair,
J., & McGrattan, K. (2015). Respiratoryswallow training in patients with head and
neck cancer. Archives of Physical Medicine
and Rehabilitation, 96(5), 885–893. https://
doi.org/10.1016/j.apmr .2014.11.022
Perry, S. E., Sevitz, J. S., Curtis, J. A., Kuo,
S. H., & Troche, M. S. (2018). Skill training resulted in improved swallowing in
a person with multiple system atrophy:
An endoscopy study. Movement Disorders
Clinical Practice, 5(4), 451–452. https://
doi.org/10.1002/mdc3.12628
Stepp, C. E., Britton, D., Chang, C., Merati,
A. L., & Matsuoka, Y. (2011). Feasibility
of game-based electromyographic biofeedback for dysphagia rehabilitation. In
2011 5th International IEEE/EMBS Conference on Neural Engineering (pp. 233–236).
Institute of Electrical and Electronics
Engineers. https://doi.org/10.1109/NER
.2011.5910530
Zimmerman, E., Carnaby, G., Lazarus, C. L.,
& Malandraki, G. A. (2020). Motor learning, neuroplasticity, and strength and
skill training: Moving from compensation to retraining in behavioral management of dysphagia. American Journal of
Speech-Language Pathology, 29(2S), 1065–
1077. https://doi.org/10.1044/2019_
AJSLP-19-00088
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DYSPHAGIA ASSESSMENT AND TREATMENT PLANNING: A TEAM APPROACH
ADDENDUM 10–3
Neuromodulation Treatments: Repetitive
Transcranial Magnetic Stimulation (rTMS),
Transcranial Direct Current Stimulation (tDCS),
and Pharyngeal Electrical Stimulation (PES)
Ivy Cheng and Shaheen Hamdy
BACKGROUND/INTRODUCTION
Neuroplasticity, which is the ability
of the nervous system to change in
response to intrinsic or extrinsic stimuli, is crucial for functional recovery
of swallowing following neurological
diseases. Early studies found that unilateral hemispheric stroke patients who
recovered from dysphagia showed an
expansion in the brain areas that represent the pharynx in the unaffected
hemisphere, but such change was
absent in those with persistent dysphagia (Hamdy, Aziz, et al., 1998; Hamdy
et al., 1996). These findings indicate
that the recovery of swallowing function may depend on the compensatory reorganization of intact neural
circuitry. Adaptations in brain activation patterns were also evident in
patients with Parkinson’s disease (PD)
(Suntrup, Teismann, Bejer, et al., 2013)
or motor neuron disease (Dziewas et
al., 2009) with functional swallowing,
suggesting the importance of neuroplasticity in dysphagia rehabilitation.
Recently, repetitive transcranial magnetic stimulation (rTMS), transcranial direct current stimulation (tDCS),
and pharyngeal electrical stimulation
(PES), the three major neuromodula-
tion techniques applied to dysphagia,
have been studied extensively in their
capacity to promote neuroplasticity in
the human swallowing network. Notwithstanding, some practical issues
need to be addressed before these techniques can be widely adopted for clinical use. This review will examine their
mechanisms of action in neurogenic
dysphagia and explore the evidence
for efficacy.
TECHNOLOGY/MECHANISM
rTMS
Transcranial magnetic stimulation
(TMS) is a type of noninvasive brain
stimulation (NIBS) that was first introduced as a neurophysiological technique to evaluate brain function (Barker
et al., 1985). TMS is based on the principle of electromagnetic induction. When
an electric current passes through the
TMS coil, a magnetic field perpendicular to the current direction is generated,
which, when placed over the scalp, can
induce a secondary current onto the
brain tissue (Barker & Shields, 2017;
Berardelli et al., 1998; Terao & Ugawa,
2002). Repetitive trains of TMS pulses
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(repetitive TMS [rTMS]) can strengthen
(long-term potentiation [LTP]) or weaken
(long-term depression [LTD]) synaptic
connections (Hoogendam et al., 2010;
Pascual-Leone et al., 1998). These neuroplasticity changes are likely mediated by N-methyl-D-aspartate (NMDA)
receptors (Huang et al., 2007; Stefan
et al., 2002).
In healthy volunteers, 5 Hz rTMS
increases the excitability of the swallowing (pharyngeal) motor cortex (Gow
et al., 2004), whereas 1 Hz rTMS reduces
it and disrupts swallowing behavior
(Mistry et al., 2007). This suppression
of the swallowing system is referred to
as a “virtual lesion.” In a further study,
Jefferson et al. demonstrated that 5 Hz
rTMS applied over the unaffected hemisphere reversed the neurophysiologic
and behavioral disruptions induced by
the “virtual lesion” (Jefferson, Mistry,
Michou, et al., 2009). Apart from cortical stimulation, rTMS applied over
the cerebellum, which is involved in
swallowing control (Cheng, Takahashi,
et al., 2022), can also modulate the
swallowing system (Jayasekeran et al.,
2011). Studies have shown that 10Hz
cerebellar rTMS induced excitation in
the pharyngeal motor cortex (Vasant
et al., 2015) and reversed disruptions
induced by the “virtual lesion” (Sasegbon et al., 2019). Taken together, these
findings indicate that the human swallowing motor cortex is highly plastic
and susceptible to rTMS.
tDCS
tDCS is another form of NIBS that
delivers electric current onto the brain
through surface electrodes, includ-
ing one or more positive (anode) and
negative (cathode) electrodes. During
tDCS, the “active” electrode is placed
over the target area while the “return”
electrode is placed over another cranial region or body part. Unlike rTMS,
which directly depolarizes neurons,
tDCS produces weak internal electric
fields that change the threshold for
discharge of stimulated neurons and
modulate the firing rate of individual
neurons (Nitsche & Paulus, 2000, 2001;
Radman et al., 2009). When applied for
a sufficient duration, tDCS can induce
changes in cortical excitability that last
longer than the stimulation duration
(Priori, 2003), and such changes are
likely mediated by NMDA receptors
(Liebetanz et al., 2002).
Jefferson et al. first found that 10 minutes of 1.5 mA and 20 minutes of 1mA
anodal tDCS enhanced pharyngeal cortical excitability, whereas 10 minutes of
1.5 mA cathodal tDCS suppressed it
(Jefferson, Mistry, Singh, et al., 2009).
Further studies suggested that anodal
tDCS can enhance the excitability of
suprahyoid motor cortex (Doeltgen
et al., 2018; Zhao et al., 2015), cortical
(swallowing) activation in both hemispheres (Suntrup, Teismann, Wollbrink,
et al., 2013), and swallowing behavior
(Cosentino et al., 2018; Doeltgen et al.,
2018; Suntrup, Teismann, Wollbrink,
et al., 2013). Finally, anodal tDCS can
reverse the physiological effects caused
by the “virtual lesion” to the pharyngeal (Vasant et al., 2014) and mylohyoid motor cortex (Hwang et al., 2022).
These studies demonstrated the ability of tDCS to modulate the swallowing motor system, making it a potentially viable treatment for dysphagia
rehabilitation.
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DYSPHAGIA ASSESSMENT AND TREATMENT PLANNING: A TEAM APPROACH
PES
PES is a peripherally applied neuromodulation technique that electrically
stimulates the pharyngeal mucosa
through bipolar ring electrodes housed
in a catheter that is inserted transnasally or orally and positioned in the
mid-pharynx (Hamdy, Aziz, et al.,
1998). The ability of PES to modulate
the swallowing neural network has
been demonstrated in several neurophysiological and neuroimaging studies. Using TMS, Hamdy, Aziz, et al. first
discovered that sensory input to the
pharynx by PES increased both pharyngeal cortical excitability and the representational map (Hamdy, Aziz, et al.,
1998). Importantly, such neuroplasticity
changes lasted longer than the stimulation duration. Other studies supported
this finding in which they showed that
the optimal frequency for PES was
5Hz and that this could increase pharyngeal cortical excitability for up to
60 minutes, which is more sustainable
than that induced by water drinking
(Fraser et al., 2002, 2003; Magara et al.,
2016). Functional neuroimaging studies reported following PES a bilateral
increase in sensorimotor cortical activation during swallowing (Fraser et al.,
2002; Suntrup, Teismann, et al., 2015),
which was associated with behavioral
gains (Suntrup, Teismann, et al., 2015).
Moreover, saliva substance P level,
which is related to swallowing reflex, in
healthy adults (Suntrup‐Krueger et al.,
2016) and patients with poststroke dysphagia increases after PES (Muhle et al.,
2017). Finally, PES can reverse the neurophysiological disruptions caused by
the “virtual lesion” to the pharyngeal
motor cortex (Jayasekeran et al., 2010).
APPLICATION
rTMS
The most severe acute adverse effect
of rTMS is induced seizures due to the
spread of excitation across the brain.
However, the risk is extremely low
(less than 0.03%) when safety guidelines are followed and no permanent
damage has been reported (Rossi et al.,
2020). The latest safety guideline suggests that TMS using a figure-of-8 coil is
considered safe in patients with cardiac
pacemakers, vagal nerve stimulation
systems, and spinal cord stimulators
and in patients who are taking medications known to lower seizure threshold
(Rossi et al., 2020).
A number of experimental rTMS
protocols have been proposed for
patients with poststroke dysphagia
(Cheng et al., 2021). The stimulation
target (esophageal, pharyngeal, mylohyoid and tongue motor cortex, and
pharyngeal sensory cortex), frequency,
and intensity vary across studies. The
stimulation frequency and intensity are
interrelated and determined based on
the safety guidelines. In general, rTMS
protocols can be classified into two categories: cortical rTMS, in which rTMS
is applied over the cerebral cortex of
one (unilateral rTMS) or both (bilateral
rTMS) hemispheres, and cerebellar
rTMS, in which rTMS is applied over
the cerebellum. Unilateral rTMS can be
further divided into three main types
based on the stimulation frequency
and hemisphere: high-frequency rTMS
applied over the unaffected hemisphere
(excitatory contralesional rTMS), highfrequency rTMS applied over the affected hemisphere (excitatory ipsilesional
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rTMS), and low frequency applied over
the unaffected hemisphere (inhibitory
contralesional rTMS).
tDCS
tDCS is considered safe because of the
weak current used to modulate neural
activity (Antal et al., 2017). No serious adverse effects have been reported
among more than 10,000 patients (Fregni et al., 2015). Other adverse effects
such as itchiness at the scalp, burning
sensation, and headache have been reported, but they are transient and typically resolved once stimulation ceased
(Russo et al., 2017).
The majority of published protocols
used tDCS as an adjunct to conventional dysphagia treatments (Cheng et
al., 2021). All studies employed anodal
tDCS, but the stimulation duration
ranged from 20 to 30 minutes for 4 to
48 days. Like rTMS, contralesional,
ipsilesional, bilateral, and cerebellar
tDCS have been studied. The stimulation targets include pharyngeal and
esophageal motor cortices and inferior sensorimotor cortex. It should be
noted that the brain stimulation targeting by tDCS, which is determined by
electrode area (24–100 cm
2
), is less focal
than rTMS.
PES
PES is considered a safe technique
with no serious device-related adverse
events reported in healthy or patient
studies (Dziewas et al., 2018). It has
been approved by the Food and Drug
Administration (FDA) and the Euro-
pean Commission (EC) as a dysphagia
treatment. In 2002, Fraser et al. identified PES delivered at 5 Hz and 75% of
the maximum intensity tolerated by
the recipient as the optimal protocol
in enhancing pharyngeal cortical excitability (Fraser et al., 2002). A further
dose-response study found that 10 minutes of PES per day for 3 days resulted
in the greatest reduction in the dysphagia severity in patients with poststroke
dysphagia among the five regimens
studied (Jayasekeran et al., 2010). Most
published randomized controlled trials
(RCTs) in dysphagic patients employed
the 3-day treatment regimen and used
PES as a standalone treatment (Cheng
et al., 2021).
RESULTS/EVIDENCE
rTMS
To date, there is no consensus on the
optimal protocol in facilitating dysphagia recovery. In patients with poststroke dysphagia, studies have shown
that rTMS increases cortical representation and excitability (Khedr et al., 2009;
Zhang et al., 2019) and enhances pharyngeal sensory conduction (Cabib et
al., 2020b). Functionally, reduced dysphagia severity and risks of penetration
and aspiration have been reported with
1 Hz rTMS (Lim et al., 2014; Tarameshlu et al., 2019) and 5 Hz rTMS (Park
et al., 2013). However, some studies
also reported no treatment effects on
swallowing safety (Cabib et al., 2020a;
Michou et al., 2014; Park et al., 2013;
Unluer et al., 2019) or biomechanics
(Cheng et al., 2017). By contrast, only
a few studies have explored the effects
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