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Clinical Decision Making in Patients with

Stroke-Related Dysphagia
Cecilia C. Felix, M.A., CCC-SLP,1
Megan E. Joseph, M.Ed., CCC-SLP,1,2 and
Stephanie K. Daniels, Ph.D., CCC-SLP2

ABSTRACT

This article aims to highlight stroke considerations in the

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evaluation and management of dysphagia. Although dysphagia was
previously thought to occur only following brainstem or bilateral cortical
strokes, the development of brain imaging and dynamic swallowing
studies has revealed small, unilateral supratentorial strokes can produce
dysphagia. In this article, screening, evaluation, and management of
dysphagia are outlined, as well as the clinical decision making that
occurs when taking into account cognitive and communication deficits
that may be present. For the clinical swallow examination, chart review,
interview, informal evaluation of cognition and communication, obser-
vation of posture, oral cavity inspection, cranial nerve examination, and
the direct swallowing assessment are reviewed along with tailoring of
each according to the deficits observed. Specific compensation and
rehabilitation strategies are discussed along with how cognitive and
communication deficits can guide the clinician’s decision-making
process to select an appropriate plan of care. A case study is provided
to synthesize the process into a real-world scenario.

KEYWORDS: dysphagia, stroke, rehabilitation, assessment/


evaluation

Learning Outcomes: As a result of this activity, the reader will be able to (1) discuss the various levels of
swallowing evaluation and identify the information obtained with each; (2) implement knowledge of the clinical
swallowing examination to increase the extent of information obtained in the evaluation; and (3) summarize
the factors to consider when implementing management strategies in patients with stroke-related dysphagia.

1
Department of Speech Pathology, Memorial Hermann Clinical Decision Making in Dysphagia; Guest Editors,
Health System, Houston, Texas; 2Department of Commu- Gary H. McCullough, Ph.D., CCC-SLP and Balaji Ran-
nication Sciences and Disorders, University of Houston, garathnam, Ph.D., CCC-SLP.
Houston, Texas. Semin Speech Lang 2019;40:188–202. Copyright
Address for correspondence: Stephanie K. Daniels, # 2019 by Thieme Medical Publishers, Inc., 333 Seventh
Ph.D., CCC-SLP, Department of Communication Avenue, New York, NY 10001, USA. Tel: +1(212) 584-
Sciences and Disorders, University of Houston, 4455 4662.
Cullen Blvd., Houston, TX 77204-6018 DOI: https://doi.org/10.1055/s-0039-1688815.
(e-mail: skdaniels@uh.edu). ISSN 0734-0478.
188
CLINICAL DECISION MAKING IN PATIENTS WITH STROKE-RELATED DYSPHAGIA/FELIX ET AL 189

A wide discrepancy in the incidence of American Stroke Association (AHA/ASA),


dysphagia in adults following stroke, ranging all individuals presenting with suspected stroke,
from 25 to 81%, has been reported.1 This regardless of severity or symptoms, should be
variability is, in part, the result of discrepancies maintained nil per os (NPO), or nothing by
in evaluation procedures, as well as various mouth including oral medications, until scree-
definitions and classifications for determining ning is completed.10 If the screening proves
dysphagia. When utilizing a comprehensive negative, that is, the person passes, oral intake
swallowing evaluation, such as the videofluo- can begin. If the screening is positive, that is,
roscopic swallowing study (VFSS), the inci- the individual fails, nonoral intake is main-
dence of dysphagia following acute stroke is tained and speech–language pathology consult
approximately 50%,2 with the incidence of is expedited. The screening does not provide
aspiration occurring in about one-half of those information that contributes to the hypothesis
individuals with dysphagia.3 of underlying swallowing impairment and
Prior to the advent of in vivo brain imaging development of a management plan.
studies and dynamic swallowing studies such as A swallowing screening is designed to be

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VFSS, it was generally posited that dysphagia quick and rapidly administered, typically by nur-
could only occur following a brainstem or ses, either in the emergency department or once
bilateral cortical stroke. Imaging studies, howe- the patient is admitted to the hospital. Training of
ver, have allowed us to correlate structure and nurses or any group of health care providers is
function leading to knowledge that a single essential for accurate implementation and inter-
cortical or subcortical stroke in either the right pretation of the swallowing screening tool (SST),
or left hemisphere can produce dysphagia.4,5 as they do not have the training or day-to-day
While diffusion-weighted acquisition comple- experience in identifying signs associated with
ted during magnetic resonance imaging (MRI) dysphagia. It is important to also remember that
brain scans allows immediate identification of nurses have many responsibilities other than
small, acute infarcts, other acquisition methods swallowing screening, so the time commitment
of MRI, as well as computed tomography scans, to education and maintenance of skills must also
can also provide insight into structure–function be feasible. Review of available SSTs suggests
relationships in swallowing. It is a common variable times necessary for education including
assumption that stroke volume must be large 10 minutes for the Barnes Jewish-Hospital-Stroke
with a corroborating high National Institute of Dysphagia Screen (BJH-SDS),11 1 hour for the
Health Stroke Scale Score to produce dyspha- Rapid Aspiration Screening for Suspected Stroke
gia. Research, however, has demonstrated that (RAS3),12 and 4 hours for the Toronto Bedside
mild stroke and small lesion volume can pro- Swallowing Screening Test (Tor-BSST).13
duce dysphagia.4,6–9 Regardless of the initial training time, one must
consider the best way to deliver the education so
that it is feasible for speech–language pathologists
SWALLOWING SCREENING (SLPs) given nurses’ rotating schedules and the
There are three levels in the evaluation of frequent addition of new nurses. In this regard,
swallowing: screening, clinical swallowing exa- some form of web-based training may be best;
mination (CSE), and instrumental assessment. however, this should be followed by hands-on
The purpose of swallowing screening is to practice with a standardized patient actor or with
determine who is at risk of dysphagia and/or actual patients.14 Moreover, booster sessions in
aspiration. As screenings are designed to be the form of web-based models may be required to
completed on everyone in a population in which facilitate initial education to sustain high adhe-
there is a high risk of the problem, in the case of rence and reliability.
stroke, the swallowing screening should be There are currently five available SSTs that
completed on all individuals admitted to hos- have been validated for patients for stroke, tested
pital with suspected stroke including those against instrumental assessment, and designed
patients with mild stroke. Per recommenda- for nurses or other frontline health care providers
tions of the American Heart Association/ to administer. These screening tools are the
190 SEMINARS IN SPEECH AND LANGUAGE/VOLUME 40, NUMBER 3 2019

BJH-SDS,11,15 Gugging Swallowing Screen,16 to any CSE. A thorough chart review should
RAS3,12,17 TOR-BSST,13 and the 3-oz Water include neurological damage, structural chan-
Swallow Challenge/Yale Swallow Protocol.18–20 ges, diagnostic imaging, relevant consultations,
While there is currently no consensus on a single current medications, appropriate laboratory
best SST for patients with suspected stroke, this results, and history of dysphagia with any
does not mean that screening should not be previous evaluations and/or treatment.
completed. Rather it suggests that the stakehol- The interview portion can fill in any mis-
ders in the stroke SST should carefully review sing information not available during the chart
the strengths and limitations of the research for review; although the amount of information
each available screening and then select the one gathered can vary widely based on the setting in
that most meets their needs. which it is completed and the patient’s ability.
Various models in which an SST can be At the inpatient level, the SLP may be consul-
implemented are available.21 Many hospitals ted for a failed swallowing screen, reduced oral
may follow a model in which the stroke SST is intake, or signs of dysphagia during oral intake.
completed by a frontline health care provider The patient may not realize that there is a

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such as a nurse, and only patients who fail the concern for swallowing as he/she has had no
screening receive a speech–language pathology opportunity to eat or drink since admission or
consult for a CSE. This model, however, may the patient may be unaware of deficits. Com-
not be the best process for stroke. Patients pleteness and accuracy of the interview may be
frequently present with cognitive deficits such affected by level of alertness, cognitive, and
as decreased attention, neglect, or impulsive- language deficits. Conversely, some patients
ness, which may affect swallowing,22–24 and with acute stroke may be very aware of their
may be missed by a routine SST. It is, thus, swallowing problems and contribute important
suggested that SLPs be consulted to complete a information during the interview. At the out-
CSE on all individuals admitted with stroke. patient level, the patient may be coming in for a
For patients who pass the swallowing screening, specific complaint related to his/her swallowing
oral intake can be initiated, and the consult to and provide great detail. In either location, it is
the SLP need not be expedited. Moreover, in important to start with an open-ended request,
this day of rapid discharge, it would allow the “Tell me about your swallowing,” and then
SLP the opportunity to screen for cognitive and determine the need for further questions based
language deficits that may be missed during the on the response. If family is available in either
neurological workup. setting, questions can also be directed to them if
warranted to provide more detailed informa-
tion; however, lack of family availability should
CLINICAL SWALLOW not delay completion of the CSE. The SLP
EXAMINATION should attempt to gather details concerning any
The CSE is designed to determine the need for history of dysphagia and interventions, baseline
instrumental assessment, guide decision diet, type of difficulty (coughing, food feels
making regarding oral diet initiation/continua- stuck, painful swallow, etc.), onset and duration
tion and identify critical information to help of dysphagia, progression of the swallowing
guide any potential management plan. This is problem (worsening, improving, static), textu-
accomplished by completing a chart review and res with which difficulty occurs, anything that
patient interview, cognitive and communica- facilitates swallowing, and level of indepen-
tion informal assessment, observation of gross dence for oral intake and hygiene.
motor skills and oral cavity inspection, cranial
nerve assessment, and evaluation of swallowing.
Cognition and Communication
Informal Assessment
Chart Review and Patient Interview As many patients with stroke have deficits
Gathering information regarding the patient’s in cognition and communication that can
prior and current level of function is imperative affect swallowing, it is important that SLPs
CLINICAL DECISION MAKING IN PATIENTS WITH STROKE-RELATED DYSPHAGIA/FELIX ET AL 191

informally evaluate cognition and communica- rule out possibility of aspiration.26 Further-
tion throughout the CSE. The SLP should more, the number of decayed teeth is associated
determine if the patient can comprehend and with development of pneumonia.25
respond to open-ended questions about swal-
lowing, if yes/no questions are required, or if
history needs to be obtained from family due to Cranial Nerve Examination
decreased comprehension or expression. Like- The cranial nerve examination can highlight
wise, during the cranial nerve examination, the decreased sensation, range of motion (ROM),
SLP should determine if the patient follows symmetry, and strength of orofacial muscula-
commands without demonstration or if a model ture that may result in deficits during the oral
of the movement is required to facilitate com- phase of swallowing as well as provide the SLP
prehension. As the patient is talking, in addi- with a unique opportunity to infer potential
tion to focusing on content and language changes to the otherwise unobservable muscu-
abilities, the clinician should assess the patient’s lature of the pharynx. Typically subjective
vocal quality paying particular attention to binary judgement (weak, strong) is used during

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breathy or wet vocal quality as these may cranial nerve examination; however, objective
indicate reduced true vocal fold (TVF) adduc- measures such as the Iowa Oral Pressure Instru-
tion or pooling of material on the TVFs, ment (IOPI) for tongue strength and an analog
respectively. Lastly, motor speech disorders peak flow meter to measure volitional cough
such as dysarthria and apraxia of speech should flow rate are available with normative data for
be identified. As with communication, the SLP tongue strength27 and volitional cough
will want to informally assess cognition in terms strength.28 Rather than performing cranial
of alertness, memory, attention, neglect, and nerve assessment without thought or inference,
impulsiveness throughout the CSE. the SLP is encouraged to always consider the
nerve which innervates the muscle and what
other muscles, especially pharyngeal, the nerve
Observation of Physical Presentation innervates. This adds greater strength to the
and Oral Cavity Inspections examination. See Table 1 for information con-
Throughout the CSE, the SLP should observe cerning cranial nerves assessment.
the overall presentation of the patient making
note of the patient’s posture (e.g., sitting
upright or leaning to one side), decreased or Swallowing Assessment
unilateral movements of the extremities, which Presentation of swallowing trials during a CSE
could be related to hemiparesis or neglect, allows the SLP the opportunity to observe signs
contractures, and overall appearance. This of oral and pharyngeal dysphagia in direct
information helps determine the level of inde- relation to oral intake. The primary reasons to
pendence for self-feeding and oral hygiene as not directly assess swallowing would be decrea-
dependence in these areas is associated with the sed alertness of the patient or poor secretion
development of pneumonia.25 management. Multiple trials of each consis-
Inspection of the oral cavity should be tency and volume are ideal to obtain a consistent
completed to assess the integrity of all oral measure of a patient’s swallowing. The follo-
structures (lips, gums, tissues, dentition, hard wing textures are typically assessed: thin liquids,
palate, velum, and tongue) as well as the quality semisolids, and solids. As semisolids and solids
of the structures and overall hygiene. The SLP can result in pharyngeal residue, which can alter
should observe salivary production and contain- bolus flow on subsequent trials, it is ideal to
ment, color differences, injury, presence and fit begin the assessment with small volumes of thin
of dental prosthesis, food/debris in the oral liquid. The amount of aspiration, should it
cavity, and odor. Poor oral hygiene has high occur, will be limited if starting with a small
specificity in detecting aspiration in the post- thin liquid volume (e.g., 5 mL). The typical
stroke population; however, it has poor sensi- protocol should test gradual increases of thin
tivity, so absence of poor oral hygiene does not liquids for SLP-regulated volumes (5 and
192 SEMINARS IN SPEECH AND LANGUAGE/VOLUME 40, NUMBER 3 2019

Table 1 Cranial Nerve Assessment


Cranial nerve Muscles Assessment examples Potential effects

V: Trigeminal - Temporalis - Open and close jaw - Reduced mastication


- Masseter against resistance - Reduced sensation of
- Medial and lateral pte- - Jaw lateralization oral residue
rygoids - Sensation to the lower - Decreased superior
- Anterior digastric face, palate, and oral hyolaryngeal
- Mylohyoid tongue movement
- Tensor veli palatini - Palpate larynx during
swallowing
VII: Facial - Facial muscles (e.g., - Retract, protrude, late- - Poor labial seal
buccinators, orbicula- ralize lips - Lateral sulcus residue
ris oris) - Labial closure against - Decreased superior
- Posterior digastric resistance hyoid movement

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- Stylohyoid - Close eyes; raise eye- - Decreased salivation
- Submandibular and brows
sublingual glands - Palpate larynx during
swallowing
IX: Glossopharyngeal - Stylopharyngeus - Sensation bilateral fau- - Delayed pharyngeal
- Parotid glands cial arches, palatine swallow
tonsils, or PPW - Reduced sensation of
BOT residue
- Reduced pharyngeal
shortening with dif-
fuse residue
- Decreased salivation
X: Vagus - Intrinsic laryngeal - Phonation - Breathy voice
muscles - Volitional cough - Reduced glottis clo-
- Sensation of larynx sure with aspiration
and inferior pharynx during the swallow
- Weak cough
- Increased risk for
silent aspiration
IX and X: Pharyngeal plexus - Palatoglossus - Palatal symmetry - Hyper-/hyponasality
- Palatopharyngeus - Nasal resonance - Nasal regurgitation
- Pharyngeal constrictors - Reduced pharyngeal
- Cricopharyngeus shortening with dif-
- Salpingopharyngeus fuse residue
- Levator veli palatini - Reduced UES opening
with pyriform sinus
residue
XII: Hypoglossal - Intrinsic and extrinsic - Retract, protrude, ele- - Reduced mastication
lingual muscles vate, depress, latera- - Reduced bolus control
lize tongue - Reduced oral transfer
- Protrude tongue - Oral residue
against resistance - Decreased BOT
retraction with
valleculae residue
CLINICAL DECISION MAKING IN PATIENTS WITH STROKE-RELATED DYSPHAGIA/FELIX ET AL 193

Table 1 (Continued)
Cranial nerve Muscles Assessment examples Potential effects
Cervical nerve 1 - Geniohyoid - Palpate larynx during - Decreased UES open-
- Thyrohyoid swallowing ing due to decreased
anterior laryngeal
movement with pyri-
form sinus residue
- Decreased laryngeal
elevation

Abbreviations: BOT, base of tongue; PPW, posterior pharyngeal wall; UES, upper esophageal sphincter.

10 mL) along with patient-regulated volumes assessment and initiating, continuing, or hal-
(e.g., putting 30 mL in a cup and having a ting oral intake. Rather than integrating the
patient take a “normal” size swallow). Depen- components of a comprehensive CSE, the SLP

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ding on a patient’s response to small volumes, may opt to use the Mann Assessment of Swallo-
testing sequential swallowing of a larger volume wing Ability31 as a standardized CSE for stroke.
(e.g., 90 mL) should be completed as most
individuals drink via self-regulated sequential
swallows. For semisolids, the volume should INSTRUMENTAL EVALUATION
initially be one teaspoon (5 mL); this can be The goals of the instrumental evaluation in the
increased to a heaping teaspoon on a subsequent diagnosis of stroke-related dysphagia are (1)
trial. The oral cavity should be inspected for evaluation of biomechanical and physiologic
residue following ingestion of semisolids and function and dysfunction, (2) determination
solids. The larynx should be palpated during all of swallowing safety and efficiency, (3) identi-
swallows.29,30 While laryngeal palpation will fication of effective compensatory management,
assist in determining onset of the pharyngeal (4) determination of appropriate diet, and (5)
swallow and the number of swallows, which determination of rehabilitation approaches.
may be indicative of oropharyngeal residue, the While there are various types of instrumental
SLP is unable to determine bolus location in evaluations available with each having strengths
relationship with the onset of hyolaryngeal and limitations, the VFSS is the preferred
movement nor is he/she able to determine the initial evaluation for individuals with stroke-
extent of laryngeal elevation. related dysphagia, as it allows for direct assess-
Signs of oral dysphagia, which can be ment of oral, pharyngeal, and esophageal stages
observed, include anterior loss, bolus holding, with the ability to identify underlying swallo-
multiple lingual gestures, oral residue, and wing impairments during the oral and pharyn-
decreased mastication. Signs of pharyngeal geal phases of swallowing. This information is
dysphagia can include throat clearing, coug- required to determine the rehabilitation plan.
hing, wet vocal quality, and multiple swallows. Various commercially available VFSS measure-
While overt signs of throat clearing, coughing, ment tools such as the MBSImP32 and Swal-
and wet vocal quality can be an indication of lowtail (Belldev Medical, Arlington Heights,
airway invasion, the absence of these signs IL) with corresponding normative data33 are
cannot always be associated with no airway available. The videoendoscopic evaluation of
invasion as many patients with stroke silently swallowing (VEES) may be preferred, however,
aspirate. It is, therefore, important to not for individuals who are medically fragile, ven-
depend solely on the patient’s response during tilator dependent, or have contractures in which
oral intake to determine the presence or absence positioning would be problematic, as the testing
of dysphagia, but rather, the SLP synthesizes all equipment is portable, and the evaluation can be
information gathered during the comprehen- completed bedside. Moreover, VEES is an
sive CSE to generate appropriate recommenda- excellent follow-up assessment to document
tions concerning the need for further improvement in swallowing signs during
194 SEMINARS IN SPEECH AND LANGUAGE/VOLUME 40, NUMBER 3 2019

rehabilitation, for example, no aspiration, redu- bolus hold to determine if larger volumes of thin
ced valleculae residue, without exposing the liquid can be safely swallowed for pleasure with
patient to further radiation. Manometry, both supervision or to implement as a compensatory
low resolution and high resolution, may be a strategy during mealtime as the patient’s
good adjunctive evaluation if abnormalities in memory improves. Conversely, the SLP can
pharyngeal or upper esophageal sphincter follow up with VEES to test these other
pressure and/or mistiming of muscular contrac- compensatory strategies as cognition improves.
tion are suspected.34 Some compensatory strategies such as the
The protocol for the swallowing tasks in Mendelsohn maneuver can be difficult to learn
VFSS should be similar to the protocol used in even in individuals with intact comprehension
the CSE in which various volumes, consisten- and cognition. If findings from the CSE sug-
cies, and trials are tested. Unlike the CSE, the gest that the Mendelsohn maneuver may be
duration of the VFSS is restricted due to indicated, ideally the SLP can attempt to teach
radiation exposure. Like the CSE, the SLP it prior to the VFSS. If this cannot be achieved,
starts with small thin liquid volumes (5 mL) of a the SLP can address teaching the maneuver in

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contrast agent and gradually increases the volu- therapy and then follow up with a repeat VFSS
mes depending on a patient’s performance. This to determine if the maneuver is performed
is of particular importance when evaluating correctly and achieving desired results. As
individuals with frontal lobe or right hemi- some compensatory strategies may have nega-
sphere damage (RHD), as they can exhibit tive effects, for example, effortful swallow
reduced inhibition, judgment, and impulse which can result in nasal redirection37 and
control. Ideally, two to three trials of each decreased pharyngeal shortening and increased
volume and/or consistency are evaluated35; hypopharyngeal residue,38 the SLP must test all
swallowing on command is omitted as it can strategies in VFSS prior to recommendation.
affect bolus positioning and timing,36 and
patients should self-administer all volumes
and consistencies. As individuals with stroke MANAGEMENT
may have paralysis, some assistance in feeding In determining the appropriate treatments for
may be required. Likewise, if a person demonst- individuals with dysphagia following stroke, a
rates poor attention and/or poor awareness clinician must consider several factors in
which are not uncommon following RHD, management, specifically in regard to compen-
the SLP may need to verbally “command” the sation and rehabilitation. Frequently, both are
patient to swallow. recommended for patients and are addressed
If a patient demonstrates consistent airway simultaneously. That is, if required for a safe
invasion or post-swallow residual, then the SLP and efficient swallow, a compensatory strategy
must test effects of compensatory strategies. is recommended during intake and rehabilita-
Knowledge about cognition and comprehen- tive strategies are targeted during swallowing
sion obtained from the CSE is critical to therapy to address the underlying impairment.
determine which strategies should be evaluated. In determining the best recommendations for
The SLP may opt to not evaluate strategies such compensation and rehabilitation, the SLP must
as 3-second bolus hold or chin tuck, as these consider both external and internal evidence.
require memory and attention as well as strict External evidence is the quality of the research
supervision if cognition is compromised and to support the treatment, and internal evidence
may instead trial nectar thick liquids which do pertains to patient, family, and environmental
not rely on a patient’s cognition. If this consis- factors, including patient goals.
tency proves to prevent aspiration, the SLP can For individuals with stroke, considerations
continue the liquid protocol with nectar thick need to be made for deficits in cognition or
liquids. However, depending on the length of comprehension that may serve as a barrier for
the VFSS and the internal evidence from the participation in therapy. For these patients,
client, the SLP may also choose to evaluate rehabilitation may need to be postponed until
strategies such as chin tuck and/or 3-second improvement occurs and direct supervision will
CLINICAL DECISION MAKING IN PATIENTS WITH STROKE-RELATED DYSPHAGIA/FELIX ET AL 195

likely be required for implementation of com- ments describe a specific regimen (e.g., expira-
pensatory techniques. For individuals who are tory muscle strength training [EMST],50
weak or deconditioned, rehabilitation can still Shaker exercise,51 lingual resistance),52 the
be targeted, although at a reduced intensity. majority of exercises do not, which makes it
difficult for the clinician to prescribe an effec-
tive dose.
Compensation As with compensation, the quality of the
Compensatory strategies are designed to allow a evidence varies across each rehabilitation tech-
person to achieve a safe and efficient oral diet by nique. Many studies target sign (residue, aspi-
eliminating signs of dysphagia, for example, ration) as the outcome and not the underlying
aspiration, residue. Even though some research impairment (e.g., increased BOT to PPW
has suggested correlation between the CSE and contact); both should be evaluated. For some
VFSS in broad diet recommendations,39 nume- treatments, only immediate effects following
rous studies support the need for instrumental rehabilitation are reported (e.g., thermal-tactile
evaluation to determine the need for and effec- application)53 or investigators have studied only

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tiveness of any recommended compensa- immediate effects (e.g., Masako maneuver),54
tion40–42 and ensure no negative effects as or results following short-term intervention
discussed previously. However, if only oral stage duration (e.g., effortful swallow55 and Mendel-
dysphagia is suspected in the CSE, compensa- sohn maneuver).56 While initially testing in
tions such as solid bolus alteration to minced healthy adults is beneficial to identify any
and moist or cyclic ingestion to clear oral positive or negative effects (e.g., chin tuck
residue can be evaluated without instrumental against resistance57 or recline exercise58), fol-
assessment. low-up studies in patient populations are criti-
Some compensatory strategies are intuitive cal. Three rehabilitative treatments (Shaker
but have no empiric evidence such as volume exercise,51 lingual resistance exercise,59 and
regulation, dry swallow, or sequential swallo- EMST50,60) have been studied in disordered
wing for swallowing apraxia. Other strategies populations with reported positive long-term
have only indirect evidence such as 3-second biomechanical and clinical effects. Even though
bolus hold.1 Finally, other compensations have lingual resistance is suggested to improve oral
direct evidence with some strategies having and pharyngeal tongue movement and strength,
stronger empiric findings (e.g., chin tuck for only oral tongue pressures have been evaluated.
airway invasion before and during the swal- See Table 3 for a list of rehabilitative strategies.
low43,44 when the pooled material is in the
valleculae45 and effortful swallow for valleculae
residue due to reduced base of tongue (BOT) to Oral Hygiene
posterior pharyngeal wall [PPW] contact),46,47 Oral hygiene should be part of the management
while the evidence for other strategies is less plan in all patients with stroke-related dyspha-
strong (e.g., chin tuck for valleculae residue48 gia. It is well known that factors common in
and carbonation).49 See Table 2 for a list of patients following stroke such as decreased
compensatory strategies. mobility and dependence in eating and dental
hygiene are related to the development of
pneumonia.25 Systematic reviews concerning
Rehabilitation the implementation of oral hygiene interven-
Rehabilitative treatment is completed outside tions in nursing home facilities have identified
of mealtime. While foods may be used during positive results in reducing morbidity and mor-
rehabilitation exercises, they are not used for tality.61,62 Based on these reviews, brushing
nutritional purposes. Traditionally, rehabilita- teeth following meals, daily denture cleaning,
tion has focused on strength training. Other and weekly professional oral health care are
types of rehabilitation, such as skill training and suggested; however, the optimal regime of oral
central and peripheral modulation, are being care is unclear as frequency and duration of
investigated. While some rehabilitation treat- tooth brushing varied across studies.
196
Table 2 Compensatory Strategies
Compensation Swallowing sign Stroke-related considerations

Self-regulated or sequential - Swallowing apraxia - Volume size with patients who are impulsive
swallowing - Ensure no aspiration with increased volume
Volume regulation - Pharyngeal pooling with/without airway invasion before or - Can be implemented with individuals with cognitive and/or
during the swallow comprehension impairment with commercially available
devices
- If devices are unavailable, these individuals will require direct
supervision
3-s bolus hold - Discoordinated oral transfer - Individuals with cognitive and/or comprehension impairment
- Pharyngeal pooling with/without airway invasion before or will require direct supervision
during the swallow
Chin tuck - Pharyngeal pooling with airway invasion before or during the - Individuals with cognitive and/or comprehension impairment
swallow will require direct supervision
- Airway invasion during the swallow due to reduced supra-
glottic closure
- Valleculae residue with/without airway invasion after the
swallow
SEMINARS IN SPEECH AND LANGUAGE/VOLUME 40, NUMBER 3

Carbonation - Pharyngeal pooling with/without airway invasion before or - Individuals with cognitive and/or comprehension impairment
during the swallow will require direct supervision
2019

- Pharyngeal residue with/without airway invasion after the


swallow
Thickened liquids - Airway invasion before or during the swallow - Monitor hydration status
- Consider small volumes of water for pleasure; volume
regulation devices or direct supervision may be required
Breath hold maneuvers - Airway invasion before and during the swallow - Complex strategy; must have good comprehension and
memory to complete
- Consider potential for fatigue in elderly or deconditioned
patients

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Table 2 (Continued)
Compensation Swallowing sign Stroke-related considerations
- Consider duration of pooling prior to airway invasion before
implementing
- Risk of cardiac arrhythmias in stroke patients64
Dry swallow - Pharyngeal residue - Easy to train and implement
- Individuals with cognitive and/or comprehension impairment
will require direct supervision to complete
Cyclic ingestion - Pharyngeal residue - Easy to train and implement
- Individuals with cognitive and/or comprehension impairment
will require direct supervision to complete
Head turn
To weaker side Unilateral pyriform sinus residue - Individuals with cognitive and/or comprehension impairment
To either side Bilateral pyriform sinus residue will require direct supervision to complete
Effortful swallow - Vallecular residue - Individuals with cognitive and/or comprehension impairment
will require direct supervision to complete
- Consider potential for fatigue in elderly or deconditioned
patients
Mendelsohn maneuver - Pyriform sinus residue - Complex maneuver to train, even for individuals with good
comprehension and cognition
- Individuals with cognitive and/or comprehension impairment
will require direct supervision to complete
- Consider potential for fatigue in elderly or deconditioned
patients
CLINICAL DECISION MAKING IN PATIENTS WITH STROKE-RELATED DYSPHAGIA/FELIX ET AL
197

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198 SEMINARS IN SPEECH AND LANGUAGE/VOLUME 40, NUMBER 3 2019

Table 3 Rehabilitation Strategies


Exercise Underlying impairment Stroke-related considerations

Thermal-tactile application - Delayed initiation of pharyngeal - As multiple sessions are required, care-
swallow giver will need to be trained to facilitate
completion in individuals with cognitive or
comprehension impairment or individuals
with dominant side hemiparesis
Lingual resistance exercises - Reduced orolingual control and - Visual feedback with external device such
strength as the IOPI may increase participation in
- Reduced BOT-PPW contact individuals with cognitive or comprehen-
sion deficits
Masako maneuver - Reduced BOT-PPW contact - Individuals who are edentulous and
without dentures will have increased diffi-
culty completing exercise

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- SLP may need to hold patient’s tongue
for those with cognitive or comprehension
deficits
Effortful swallow - Reduced base of tongue - Using sEMG visual feedback may facili-
retraction tate implementation in patients with com-
prehension or cognitive impairment
EMST - Reduced laryngeal elevation - As multiple sessions are required, care-
- Reduced volitional cough giver will need to be trained to facilitate
strength completion in individuals with cognitive or
comprehension impairment
Mendelsohn maneuver - Reduced UES opening - Complex exercise and difficult to teach for
individuals with comprehension or cogni-
tive impairment even when using sEMG
visual feedback
Shaker exercise - Reduced UES opening - Easy to demonstrate, for patient to
imitate, and for clinician to manipulate the
body for individuals with comprehension
or cognitive deficits
- As multiple sessions are required, care-
giver will need to be trained to facilitate
completion in individuals with cognitive or
comprehension impairment
- Most individuals, especially those who are
deconditioned, will not be able to com-
plete maximum duration or repetitions
initially, so will extend past recommended
6 wk
- For patients on tube feeding, ensure that
exercise is not completed within 1 h
following feeding
CTAR - Reduced UES opening - Easy to demonstrate, for patient to
imitate, and for clinician to manipulate the
body for individuals with comprehension
or cognitive deficits
CLINICAL DECISION MAKING IN PATIENTS WITH STROKE-RELATED DYSPHAGIA/FELIX ET AL 199

Table 3 (Continued)
Exercise Underlying impairment Stroke-related considerations
Recline exercise - Reduced UES opening - Easy to demonstrate, for patient to
imitate, and for clinician to manipulate the
body for individuals with comprehension
or cognitive deficits
Wada exercise - Reduced UES opening - Easy to demonstrate, for patient to
imitate, and for clinician to manipulate the
body for individuals with comprehension
or cognitive deficits
- Avoid in individuals with TMJ issues pain
with jaw opening

Abbreviations: BOT, base of tongue; CTAR, chin tuck against resistance; EMST, expiratory muscle strength training;
IOPI, Iowa Oral Performance Instrument; PPW, posterior pharyngeal wall; sEMG, surface electromyography; SLP,

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speech–language pathologist; TMJ, temporomandibular joint; UES, upper esophageal sphincter.

Implementation of an oral hygiene pro- along with left lingual asymmetry on protru-
gram to reduce risk of pneumonia is suggested sion with decreased ROM and strength
in the AHA/ASA guidelines for management (hypoglossal cranial nerve). The swallowing
of acute ischemic stroke.63 While nursing staff portion of the CSE was completed with trials
frequently assumes the burden of completing of water (5 mL, 10 mL, self-regulated cup
dental care, multidisciplinary collaboration bet- sip), applesauce, and cheese crackers. LB
ween nursing, speech pathology, occupational exhibited impulsivity with oral trials charac-
therapy, and dental hygiene would appear to be terized by not waiting for prompts, eating
most appropriate to develop and implement quickly, and poor control of volume. Oral
effective training and adherence to an oral phase dysphagia was evident characterized
care program for patients following stroke. by impaired bolus preparation with prolonged
and inefficient mastication of solids, reduced
bolus cohesion with oral residue present on
CASE SCENARIO left lingual/dental surface and buccal space,
LB, a 54-year-old male patient with history of and prolonged oral transit time with solids.
obesity and insulin-dependent diabetes mellitus Coughing was evident in both trials of self-
type 2, was admitted to general hospital with regulated cup sip; however, LB appeared
complaint of left-sided weakness and slurred unconcerned as he attempted to continue
speech for 1 day. His MRI scan revealed a right drinking the water. Larger liquid volumes
middle cerebral artery ischemic stroke. Speech– were not administered.
language pathology was consulted for dysphagia A VFSS was completed later that day with
evaluation as the patient was NPO following a the following trials tested: thin liquid Varibar
positive nursing-administered swallowing barium (5 mL, 10 mL, self-regulated cup sip),
screen. Prior to the stroke, LB consumed nectar thick Varibar barium (self-regulated cup
regular solids with thin liquids at home with sip, sequential swallowing), Varibar barium
no history of dysphagia. pudding, and a barium pudding-coated cracker.
The informal cognitive screen during the The oral phase was noted to be the same as
CSE revealed disorientation, impaired short- during the CSE with the addition of reduced
term memory, impulsivity, reduced insight orolingual control for thin liquids resulting in
into deficits, and left neglect. Cranial nerve pyriform sinus pooling and aspiration before
assessment revealed reduced left labial asym- the swallow (weak cough but no clearing) with
metry at rest and with extension as well as the self-regulated cup sip trials. Given cognitive
decreased ROM and strength (facial cranial deficits, 3-second bolus hold, and chin tuck
nerve). Weak volitional cough was identified, were not attempted as compensatory strategies.
200 SEMINARS IN SPEECH AND LANGUAGE/VOLUME 40, NUMBER 3 2019

Nectar thick liquid, however, was attempted M.E.J. receives salary support from the Uni-
and proved successful in preventing airway versity of Houston and Memorial Hermann
invasion during self-regulated cup sip and Health System.
sequential swallowing. During the pharyngeal S.K.D. receives salary support from the Uni-
phase, LB exhibited decreased BOT retraction versity of Houston, and royalties from Plural
yielding moderate valleculae residue and redu- Publishing and MedBridge.
ced UES opening due to decreased anterior
hyolaryngeal elevation yielding moderate bila-
teral pyriform sinus residue with semisolids and REFERENCES
the masticated solid. The residue did not build
up with subsequent swallows. 1. Daniels SK, Huckabee ML, Gozdzikowska K.
Dysphagia Following Stroke, 3rd ed. San Diego,
The SLP recommended nectar thick liquids
CA: Plural Publishing; 2019
(International Dysphagia Diet Standardization 2. Martino R, Foley N, Bhogal S, Diamant N,
Initiative [IDDSI] level 2; www.iddsi.org) and Speechley M, Teasell R. Dysphagia after stroke:
minced and moist solids (IDDSI level 5). Super- incidence, diagnosis, and pulmonary complications.

Downloaded by: Universidad de Barcelona. Copyrighted material.


vision during meals to regulate rate of ingestion Stroke 2005;36(12):2756–2763
was recommended as well as supervised 10 mL 3. Mann G, Hankey GJ, Cameron D. Swallowing
water volumes using a commercially available function after stroke: prognosis and prognostic
factors at 6 months. Stroke 1999;30(04):744–748
cup for pleasure. LB participated in the occupa-
4. Daniels SK, Foundas AL. Lesion localization in
tional therapy feeding program during lunch, acute stroke patients with risk of aspiration.
and nursing support staff or family members J Neuroimaging 1999;9(02):91–98
were available to supervise breakfast and dinner. 5. Robbins J, Levine RL, Maser A, Rosenbek JC,
Rehabilitation recommendations included lin- Kempster GB. Swallowing after unilateral stroke of
gual resistance exercises using the IOPI to the cerebral cortex. Arch Phys Med Rehabil 1993;
provide visual feedback to improve oral tongue 74(12):1295–1300
6. Cola MG, Daniels SK, Corey DM, Lemen LC,
strength, the Masako maneuver and effortful
Romero M, Foundas AL. Relevance of subcortical
swallowing to also increase BOT to PPW stroke in dysphagia. Stroke 2010;41(03):482–486
contact, EMST to facilitate cough strength, 7. Daniels SK, Pathak S, Mukhi SV, Stach CB,
and the Shaker exercises to facilitate anterior Morgan RO, Anderson JA. The relationship bet-
hyolaryngeal elevation. LB’s family was taught ween lesion localization and dysphagia in acute
the exercises, so they could complete the neces- stroke. Dysphagia 2017;32(06):777–784
sary trials outside of his twice-daily therapy 8. Joundi RA, Martino R, Saposnik G, Giannakeas V,
Fang J, Kapral MK. Predictors and outcomes of
sessions.
dysphagia screening after acute ischemic stroke.
LB was transferred to acute rehab on day 4 Stroke 2017;48(04):900–906
and continued to receive twice daily swallowing 9. Steinhagen V, Grossmann A, Benecke R, Walter
and cognitive therapy. Therapy staff and family U. Swallowing disturbance pattern relates to brain
provided oral hygiene after every meal. A repeat lesion location in acute stroke patients. Stroke
VFSS was completed during week 3 and revea- 2009;40(05):1903–1906
led improvement in mastication, orolingual 10. Jauch EC, Saver JL, Adams HP Jr, et al; American
Heart Association Stroke Council; Council on
control, BOT to PPW contact, and UES open-
Cardiovascular Nursing; Council on Peripheral
ing. No aspiration of liquids was noted, and Vascular Disease; Council on Clinical Cardiology.
pharyngeal residue was minimal. Soft and bite- Guidelines for the early management of patients
sized solids (IDDSI level 6) and thin liquids with acute ischemic stroke: a guideline for health-
(IDDSI level 0) were recommended along with care professionals from the American Heart Asso-
continued supervision to monitor impulsive ciation/American Stroke Association. Stroke 2013;
behavior during mealtime. 44(03):870–947
11. Edmiaston J, Connor LT, Loehr L, Nassief A.
Validation of a dysphagia screening tool in acute
stroke patients. Am J Crit Care 2010;19(04):
FINANCIAL DISCLOSURES 357–364
C.C.F. receives salary support from Memorial 12. Anderson JA, Pathak S, Rosenbek JC, Morgan
Hermann Health System. RO, Daniels SK. Rapid aspiration screening for
CLINICAL DECISION MAKING IN PATIENTS WITH STROKE-RELATED DYSPHAGIA/FELIX ET AL 201

suspected stroke: Part 2: Initial and sustained nurse tors of swallowing recovery in stroke. J Rehabil Res
accuracy and reliability. Arch Phys Med Rehabil Dev 2006;43(03):301–310
2016;97(09):1449–1455 25. Langmore SE, Terpenning MS, Schork A, et al.
13. Martino R, Silver F, Teasell R, et al. The Toronto Predictors of aspiration pneumonia: how important
Bedside Swallowing Screening Test (TOR-BSST): is dysphagia? Dysphagia 1998;13(02):69–81
development and validation of a dysphagia scree- 26. McCullough GH, Rosenbek JC, Wertz RT,
ning tool for patients with stroke. Stroke 2009;40 McCoy S, Mann G, McCullough K. Utility of
(02):555–561 clinical swallowing examination measures for
14. Freeland TR, Pathak S, Garrett RR, Anderson JA, detecting aspiration post-stroke. J Speech Lang
Daniels SK. Using medical mannequins to train Hear Res 2005;48(06):1280–1293
nurses in stroke swallowing screening. Dysphagia 27. Vanderwegen J, Guns C, Van Nuffelen G, Elen R,
2016;31(01):104–110 De Bodt M. The influence of age, sex, bulb
15. Edmiaston J, Connor LT, Steger-May K, Ford position, visual feedback, and the order of testing
AL. A simple bedside stroke dysphagia screen, on maximum anterior and posterior tongue
validated against videofluoroscopy, detects dyspha- strength and endurance in healthy Belgian adults.
gia and aspiration with high sensitivity. J Stroke Dysphagia 2013;28(02):159–166
Cerebrovasc Dis 2014;23(04):712–716 28. Smith Hammond CA, Goldstein LB, Horner RD,

Downloaded by: Universidad de Barcelona. Copyrighted material.


16. Trapl M, Enderle P, Nowotny M, et al. Dysphagia et al. Predicting aspiration in patients with ischemic
bedside screening for acute-stroke patients: the stroke: comparison of clinical signs and aerodyna-
Gugging Swallowing Screen. Stroke 2007;38(11): mic measures of voluntary cough. Chest 2009;135
2948–2952 (03):769–777
17. Daniels SK, Pathak S, Rosenbek JC, Morgan RO, 29. Murray J. Manual of Dysphagia Assessment in
Anderson JA. Rapid aspiration screening for Adults. San Diego, CA: Singular; 1999
suspected stroke: part 1: development and valida- 30. Logemann JA. Evaluation and Treatment of Swal-
tion. Arch Phys Med Rehabil 2016;97(09): lowing Disorders. 2nd ed. Austin, TX: Pro-Ed;
1440–1448 1998
18. Suiter DM, Leder SB. Clinical utility of the 3- 31. Mann G. MASA: The Mann Assessment of Swal-
ounce water swallow test. Dysphagia 2008;23(03): lowing Ability. Clifton Park, NY: Thomson Del-
244–250 mar Learning; 2002
19. Warner HL, Suiter DM, Nystrom KV, Poskus K, 32. Martin-Harris B, Brodsky MB, Michel Y, et al.
Leder SB. Comparing accuracy of the Yale swallow MBS measurement tool for swallow impairment–
protocol when administered by registered nurses MBSImp: establishing a standard. Dysphagia
and speech-language pathologists. J Clin Nurs 2008;23(04):392–405
2014;23(13-14):1908–1915 33. Leonard R, Kendall KA. Dysphagia Assessment
20. Suiter DM, Sloggy J, Leder SB. Validation of the and Treatment Planning. 4th ed. San Diego, CA:
Yale Swallow Protocol: a prospective double- Plural Publishing; 2019
blinded videofluoroscopic study. Dysphagia 2014; 34. Huckabee ML, Macrae P, Lamvik K. Expanding
29(02):199–203 instrumental options for dysphagia diagnosis and
21. American Speech-Language-Hearing Association research: ultrasound and manometry. Folia Pho-
Steering Committee of Special Interest Division niatr Logop 2015;67(06):269–284
13. Frequently asked questions (FAQ) on swallo- 35. Molfenter SM, Steele CM. Physiological variabi-
wing screening: special emphasis on patients with lity in the deglutition literature: hyoid and laryngeal
acute stroke. 2009. Available at: http://www.asha. kinematics. Dysphagia 2011;26(01):67–74
org/uploadedFiles/FAQs-on-Swallowing-Scree- 36. Daniels SK, Schroeder MF, DeGeorge PC, Corey
ning.pdf. Accessed April 24, 2019 DM, Rosenbek JC. Effects of verbal cue on bolus
22. Ebrahimian Dehaghani S, Yadegari F, Asgari A, flow during swallowing. Am J Speech Lang Pathol
Bagheri Z. The mediator effect of cognition on the 2007;16(02):140–147
relationship between brain lesion location and 37. Garcia JM, Hakel M, Lazarus C. Unexpected
dysphagia in patients with stroke: applying a struc- consequence of effortful swallowing: case study
tural equation model. J Oral Rehabil 2019;46(01): report. J Med Speech-Lang Pathol 2004;12(02):
33–39 59–67
23. Parker C, Power M, Hamdy S, Bowen A, Tyrrell P, 38. Molfenter SM, Hsu CY, Lu Y, Lazarus CL.
Thompson DG. Awareness of dysphagia by Alterations to swallowing physiology as the result
patients following stroke predicts swallowing per- of effortful swallowing in healthy seniors. Dysp-
formance. Dysphagia 2004;19(01):28–35 hagia 2018;33(03):380–388
24. Schroeder MF, Daniels SK, McClain M, Corey 39. Rangarathnam B, McCullough GH. Utility of the
DM, Foundas AL. Clinical and cognitive predic- clinical swallowing exam for understanding
202 SEMINARS IN SPEECH AND LANGUAGE/VOLUME 40, NUMBER 3 2019

swallowing physiology. Dysphagia 2016;31(04): 53. Rosenbek JC, Robbins J, Willford WO, et al.
491–497 Comparing treatment intensities of tactile-thermal
40. Baylow HE, Goldfarb R, Taveira CH, Steinberg application. Dysphagia 1998;13(01):1–9
RS. Accuracy of clinical judgment of the chin- 54. Fujiu M, Logemann JA. Effect of a tongue-holding
down posture for dysphagia during the clinical/ maneuver on posterior pharyngeal wall movement
bedside assessment as corroborated by videofluo- during deglutition. Am J Speech Lang Pathol 1996;
roscopy in adults with acute stroke. Dysphagia 5(01):23–30
2009;24(04):423–433 55. Felix VN, Corrêa SM, Soares RJ. A therapeutic
41. Fraser S, Steele CM. The effect of chin down maneuver for oropharyngeal dysphagia in patients
position on penetration-aspiration in adults with with Parkinson’s disease. Clinics (São Paulo) 2008;
dysphagia. Can J Speech-Lang Pathol Audiol 63(05):661–666
2012;36(02):142–148 56. McCullough GH, Kamarunas E, Mann GC,
42. Miles A, McFarlane M, Scott S, Hunting A. Schmidley JW, Robbins JA, Crary MA. Effects
Cough response to aspiration in thin and thick of Mendelsohn maneuver on measures of swallo-
fluids during FEES in hospitalized inpatients. Int J wing duration post stroke. Top Stroke Rehabil
Lang Commun Disord 2018;53(05):909–918 2012;19(03):234–243
43. Bülow M, Olsson R, Ekberg O. Videomanometric 57. Yoon WL, Khoo JK, Rickard Liow SJ. Chin tuck

Downloaded by: Universidad de Barcelona. Copyrighted material.


analysis of supraglottic swallow, effortful swallow, against resistance (CTAR): new method for enhan-
and chin tuck in patients with pharyngeal dysfunc- cing suprahyoid muscle activity using a Shaker-type
tion. Dysphagia 2001;16(03):190–195 exercise. Dysphagia 2014;29(02):243–248
44. Macrae P, Anderson C, Humbert I. Mechanisms 58. Mishra A, Rajappa A, Tipton E, Malandraki GA.
of airway protection during chin-down swallo- The recline exercise: comparisons with the head lift
wing. J Speech Lang Hear Res 2014;57(04): exercise in healthy adults. Dysphagia 2015;30(06):
1251–1258 730–737
45. Shanahan TK, Logemann JA, Rademaker AW, 59. Robbins J, Kays SA, Gangnon RE, et al. The
Pauloski BR, Kahrilas PJ. Chin-down posture effects of lingual exercise in stroke patients with
effect on aspiration in dysphagic patients. Arch dysphagia. Arch Phys Med Rehabil 2007;88(02):
Phys Med Rehabil 1993;74(07):736–739 150–158
46. Huckabee ML, Steele CM. An analysis of lingual 60. Hegland KW, Davenport PW, Brandimore AE,
contribution to submental surface electromyogra- Singletary FF, Troche MS. Rehabilitation of swal-
phic measures and pharyngeal pressure during lowing and cough functions following stroke: an
effortful swallow. Arch Phys Med Rehabil 2006; expiratory muscle strength training trial. Arch Phys
87(08):1067–1072 Med Rehabil 2016;97(08):1345–1351
47. Steele CM, Huckabee ML. The influence of 61. Sjögren P, Nilsson E, Forsell M, Johansson O,
orolingual pressure on the timing of pharyngeal Hoogstraate J. A systematic review of the preven-
pressure events. Dysphagia 2007;22(01):30–36 tive effect of oral hygiene on pneumonia and
48. Knigge MA, Thibeault S. Relationship between respiratory tract infection in elderly people in
tongue base region pressures and vallecular clea- hospitals and nursing homes: effect estimates and
rance. Dysphagia 2016;31(03):391–397 methodological quality of randomized controlled
49. Turkington LG, Ward EC, Farrell AM. Carbo- trials. J Am Geriatr Soc 2008;56(11):2124–2130
nation as a sensory enhancement strategy: a narra- 62. van der Maarel-Wierink CD, Vanobbergen JN,
tive synthesis of existing evidence. Disabil Rehabil Bronkhorst EM, Schols JM, de Baat C. Oral health
2017;39(19):1958–1967 care and aspiration pneumonia in frail older people:
50. Troche MS, Okun MS, Rosenbek JC, et al. Aspi- a systematic literature review. Gerodontology 2013;
ration and swallowing in Parkinson disease and 30(01):3–9
rehabilitation with EMST: a randomized trial. 63. Powers WJ, Rabinstein AA, Ackerson T, et al;
Neurology 2010;75(21):1912–1919 American Heart Association Stroke Council. 2018
51. Shaker R, Easterling C, Kern M, et al. Rehabili- guidelines for the early management of patients
tation of swallowing by exercise in tube-fed patients with acute ischemic stroke: a guideline for health-
with pharyngeal dysphagia secondary to abnormal care professionals from the American Heart Asso-
UES opening. Gastroenterology 2002;122(05): ciation/American Stroke Association. Stroke 2018;
1314–1321 49(03):e46–e110
52. Rogus-Pulia N, Rusche N, Hind JA, et al. Effects 64. Chaudhuri G, Hildner CD, Brady S, Hutchins B,
of device-facilitated isometric progressive resis- Aliga N, Abadilla E. Cardiovascular effects of the
tance oropharyngeal therapy on swallowing and supraglottic and super-supraglottic swallowing
health-related outcomes in older adults with dysp- maneuvers in stroke patients with dysphagia. Dysp-
hagia. J Am Geriatr Soc 2016;64(02):417–424 hagia 2002;17(01):19–23

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