Miami Speech & Swallowing Center

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ORIGINAL RESEARCH ARTICLE

Neuromuscular Electrical Stimulation Efficacy in Acute Stroke Feeding Tube Dependent Dysphagia During 

Inpatient Rehabilitation


ABSTRACT

Kushner DS, Peters K, Eroglu ST, Perless-Carroll M, Johnson-Greene D:  Neuromuscular electrical stimulation efficacy in acute stroke feeding tube dependent dysphagia during inpatient rehabilitation. Am J Phys Med Rehabilitation 2013;92:486495.


Objective: The aim of this study was to compare the efficacy of neuromuscular electrical stimulation (NMES) in addition to traditional dysphagia therapy (TDT) including progressive resistance training (PRT) with that of TDT/PRT alone during inpatient rehabilitation for treatment of feeding tube dependent dysphagia in patients who have had an acute stroke.


Design: This study is an inpatient rehabilitation case-control study involving 92 patients who have had an acute stroke with initial Functional Oral Intake Scale (FOIS) scores of 3 or lower and profound to severe feeding tube dependent dysphagia.  Sixty-five patients, the NMES group, received NMES with TDT/PRT, and 27 patients, the case-control group, received only TDT/PRT. Treatment occurred in hourly sessions daily for a mean T SD of 18 T 3 days. W2 Analyses/t tests revealed no significant statistical differences between the groups for age (t=j0.85; P = 0.40), sex (W2 = 0.05; P = 0.94), and stroke location (W2 = 4.2; P = 0.24). A Mann-Whitney U

test revealed a statistically significant difference between the groups for the initial FOIS score (z = j2.4; P = 0.015), with the NMES group having worse initial scores with a mean rank of 42.64 and the case-control TDT/PRTgroup having a mean rank of 55.8.  The main outcome measure was the comparison of the FOIS scores after treatment.


Results: The mean T SD FOIS score after NMES with TDT/PRT treatment was 5.1 T 1.8 compared with 3.3 T 2.2 in the case-control TDT/PRTgroup. The mean gain for the NMES group was 4.4 points; and for the case-control group, 2.4 points.  Significant improvement in swallowing performance was found for the NMES group

compared with the TDT/PRT group (z = 3.64; P G 0.001). Within the NMES group, 46% (30 of 65) of the patients had minimal or no swallowing restrictions (FOIS score of 57) after treatment, whereas 26% (7 of 27) of those in the case-control group improved to FOIS scores of 57, a statistically significant difference (W2 = 6.0; P = 0.01).

Conclusions: This study suggests that NMES with TDT/PRT is significantly more effective than TDT / PRT alone during inpatient rehabilitation in reducing feeding tube dependent dysphagia in patients who have had an acute stroke.  Key Words: Stroke, Dysphagia, Deglutition Disorders, Rehabilitation, Electric Stimulation Therapy


Authors:

David S. Kushner, MD

Kenneth Peters, MS, CCC-SLP

Stacy Thomashaw Eroglu, MA, CCC-SLP

Melissa Perless-Carroll, MS, CCC-SLP

Douglas Johnson-Greene, PhD


Affiliations:

From the Department of Rehabilitation Medicine, University of Miami Miller School of Medicine, Miami, Florida (DSK, DJ-G); Department of Speech-Language Pathology, HealthSouth Rehabilitation Hospital,

Miami, Florida (KP); and Department of Speech-Language Pathology, HealthSouth Rehabilitation Hospital,

Sunrise, Florida (STE, MP-C).


Correspondence:

All correspondence and requests for reprints should be addressed to: David S. Kushner, MD, Department of

Rehabilitation Medicine, University of Miami Miller School of Medicine, 20601 Old Cutler Rd, Miami FL 33189.


Disclosures:

Supported, in part, by the United States Department of Education, National Institute of Disability Research and Rehabilitation grant H133A12009(to D.J-G.) Presented at the American Congress oRehabilitation Medicine annual conference in Atlanta in October 2011, and the abstract was published in

Archives of Physical Medicine and Rehabilitation October 2011;92(10):16912.

Financial disclosure statements have

been obtained, and no conflicts of

interest have been reported by the

authors or by any individuals in control

of the content of this article.

0894-9115/13/9206-0486/0

American Journal of Physical

Medicine & Rehabilitation

Copyright * 2013 by Lippincott

Williams & Wilkins

DOI: 10.1097/PHM.0b013e31828762ec

486 Am. J. Phys. Med. Rehabil. & Vol. 92, No. 6, June 2013

Copyright © 2013 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.


Approximately 800,000 acute strokes occur annually

in the United States,1,2 of which 45%-70% of

cases have dysphagia.  Dysphagia increases the risk

for aspiration pneumonia,malnutrition/dehydration,

depression, and premature death. Dysphagia complications

impair recovery and lead to prolonged

hospitalizations; rehospitalizations; and the need

for respiratory support, tracheotomy, tube feedings,

and related nutritional supplements and equipment,

resulting in increased healthcare costs. The average

cost per patient associated with percutaneous tube

feedings is estimated to exceed $30,000 per year.7 In

patients who have had an acute stroke having dysphagia,

it is estimated that more than 11% require

placement of percutaneous gastrostomy tubes annually,

and at least 50% of those individuals will require

it long-term.6,8 Aspiration pneumonia is the

most common cause of death in individuals having

untreated dysphagia after stroke,9 accounting for at

least 10% of deaths occurring within 30 days of the

initial hospital admission.4 The mortality rate for

feeding tube dependent patients may be as high as

36% during the 2 yrs after the acute stroke.6

Dysphagia in stroke results from impairments

of the oral and pharyngeal stages of swallowing.10,11

During the oral-pharyngeal stages of swallowing, the

contraction and inhibition of approximately 50 pairs

of muscles are coordinated in the propulsion of a

food bolus, solid or liquid, to the esophagus while

protecting the airway to the larynx.10,11 Ascending

sensory input from the oropharynx and descending

motor input from the cortical/subcortical brain swallowing

centers are integrated in the lower brainstem

in a network of neurons known as the central

pattern generator (CPG).10 12 The swallowing process

is mediated via the CPG and the cranial nerve

nuclei of V, VII, IX, X, and XII.10 12 Treatments of

dysphagia in stroke may target the enhancement of

sensory feedback from the oropharynx to the CPG

and/or target strengthening of the oropharyngeal

musculature that is in disuse atrophy secondary to

reduced motor output from the CPG.

Traditional dysphagia therapy (TDT) involves

oral motor exercises, including progressive resistance

training (PRT), to strengthen the oropharyngeal musculature

that is in disuse atrophy13; biofeedback

techniques and sensory stimulation to target the

CPG5,1417; and compensatory swallowing strategies

including various modifications of head, neck, and

body postures.13,18 Adjustment of food/liquid temperature,

viscosity, and volume18,19 and the use of

tube feedings for severe dysphagia are also included.

TDT strategies have limited success in severe

dysphagia, require prolonged durations of treatment

of up to 52 wks,5 and have therapeutic benefits that

may be short lasting.20,21 Transcutaneous neuromuscular

electrical stimulation (NMES) was approved by

the Food and Drug Administration in 2001 as a treatment

of dysphagia22 and is hypothesized to target

strengthening of the oropharyngeal musculature in

disuse atrophy while also providing sensory feedback

to the CPG and the cortical/subcortical swallowing

centers.20,23 The use of NMES in dysphagia treatment

was identified in a 2005 national survey by speechlanguage

pathologists (SLPs) as an area of interest

needing further evidence-based research.24 However,

6 yrs since that survey, the use of NMES in clinical

practice still remains controversial. Efficacy studies

that have been published since the Food and Drug

Administration approval have had mixed results for

patients having mostly chronic mild, moderate, and

severe dysphagia of various etiologies.20,25,29 Only

two published randomized NMES studies thus far

have been limited to only patients who have had a

stroke having dysphagia,26,30 of which one demonstrated

efficacy,30 whereas one did not.26 Both of

these studies included patients who have had subacute

and chronic stroke with mild to severe dysphagia

but excluded patients who have had brainstem

strokes.26,30 There has not yet been a study to evaluate

NMES efficacy when added to TDT in comparison

with TDT alone limited to only patients who have

had acute ischemic or hemorrhagic hemisphere and

brainstem stroke having severe to profound feeding

tube dependent dysphagia during inpatient rehabilitation;

thus, the purpose of this study was to fill that

gap in clinical knowledge.


METHODS:

Participants

This study included 92 patients admitted at

two HealthSouth Rehabilitation Hospital inpatient

facilities (HealthSouth, Miami, FL, and HealthSouth,

Sunrise, FL), from 2005 through 2011, who have

had acute stroke with initial Functional Oral Intake

Scale (FOIS)31 scores of 3 or lower and severe to

profound feeding tube dependent dysphagia. The

severe to profound dysphagia was defined in this

study as a high risk for aspiration of all solids and/or

liquids to aspiration of all consistencies including

saliva on the initial SLP swallowing assessment, with

nothing-by-mouth recommendation and tube feeding

required for maintaining the patients’ nutritional

needs. Inclusion criteria for this study were adult patients

having percutaneous gastrostomy feeding tubes

with profound to severe oropharyngeal dysphagia,

www.ajpmr.com NMES in Dysphagia 48

having the ability to follow a minimum of one-step

simple commands consistently, and having had new on set

hemorrhagic or ischemic stroke. Participants

were excluded from this study if they had esophageal phase

swallowing disorders, structural swallowing

disorders, or co_morbid neurologic degenerative disorders

or if there was documentation of any behavioral

disorder or other issues that interfered with a patient’s

ability to consistently participate in dysphagia treatment.

In addition, any patient who has had a stroke

admitted with a feeding tube who did not have clinical

signs of profound to severe dysphagia per the initial

SLP evaluation was excluded from this study, unless a

high risk for silent aspiration was subsequently documented

by a modified barium swallow (MBS)32 test.

Thus, pre treatment feeding tube dependent dysphagia

was confirmed for all patients included in this

study. An exclusion criterion for the NMES group was

inability to tolerate the electrical stimulation treatment.

Medical contraindications for the NMES group,

at the discretion of attending physicians, included

having cardiac pacemakers or a history of seizures or

epilepsy. Consent for inpatient rehabilitation treatment

was obtained for all patients directly or from their

healthcare proxies/surrogates on admission per the

standard HealthSouth corporate policy/protocol. Further

consent was obtained from the attending physicians

before administration of NMES to any patient.

NMES was prescribed by approximately half of the

attending physicians for all patients having feeding

tube dependency, whereas about one-fourth prescribed

NMES only to those patients having no

history of seizures or cardiac pacemakers, and the

remaining one-fourth did not prescribe NMES to

any patient because of lack of published evidence

supporting NMES efficacy, which is one of the main

reasons for this study. Thus, of the 92 patients who

have had an acute stroke, 65 received NMES/TDT

and 27 received only TDT. The patients who received

NMES/TDT were started on treatment at a mean of

15.7 days after the acute stroke, whereas the patients

in the TDT group initiated treatment at a mean of

15.4 days after the stroke. Demographics of both the

NMES and TDT cohorts are given (Table 1). Participant

data were obtained and maintained by the SLP

investigators, such that the patients cannot be identified

directly or indirectly in any manner. This study

was approved by the HealthSouth Corporate Clinical

Research Review Committee.


Procedure:

All patients in this study were evaluated within

24 hrs of admission by the SLPs who have a mean of

7 yrs of licensed clinical experience and a certificate

of clinical competency. The initial FOIS31 scores were

determined for each patient at risk for pharyngeal

aspiration/penetration by solid and/or liquid boluses

on the basis of the admission SLP clinical assessment

and the preadmission MBS test results, if available.

The SLP swallowing evaluations have been shown

to have good sensitivity, specificity, and interrater

reliability.33 Clinical evaluations by the experienced

SLPs, including testing for voluntary cough, dysphonia,

dysarthria, impaired gag reflex, postswallow

cough, and voice change,34 are effective in diagnosing

patients who have had a stroke at risk for pharyngeal

penetration/aspiration, whereas MBS studies have

been shown to be more sensitive to the diagnosis of

silent aspiration.34,35 Thus, any patient who has had a

stroke admitted with a feeding tube who did not have

clinical signs of profound to severe dysphagia per the

initial SLP evaluation was referred for an MBS study.

In this manner, feeding tube dependency was confirmed

at the time of admission, before treatment and

inclusion in this study. All patients, including those

in the NMES group, received TDT on the basis of

each patient’s initial SLP clinical assessment. Therapeutic

exercises were provided as needed to increase

strength, endurance, range of motion, and mobility

of the oral-facial, lingual, and laryngeal musculature.

All patients received PRT13 including any combination

of lingual-strengthening exercises,13,36,37 laryngeal

adduction-elevation exercises,13 effortful swallow maneuver,

13,38 Mendelsohn maneuver,13,39 Masako maneuver,

13,40 and Shaker exercises.13,37,41 The patients

also received sensory biofeedback treatments including

thermal stimulation.5,1417 Compensatory

swallowing strategies,13,18 including modifications of

TABLE 1 The case-control and NMES group

demographics

Case-control group demographics

Patients, N 27

Left hemisphere stroke 9

Right hemisphere stroke 10

Intracerebral hemorrhage 7

Brainstem stroke 1

Age range, yrs 49Y91

Men, n 16

Women, n 11

NMES group demographics

Patients, N 65

Left hemisphere stroke 36

Right hemisphere stroke 14

Intracerebral hemorrhage 12

Brainstem stroke 3

Age range, yrs 19Y89

Men, n 38

Women, n 27

488 Kushner et al. Am. J. Phys. Med. Rehabil. & Vol. 92, No. 6, June 2013

Copyright © 2013 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

head, neck, and body postures, were used as needed

on the basis of any anatomic or postural deficits. The

patients received therapeutic or trial feedings as tolerated,

with one-to-one supervision by the SLP either

in private treatment sessions or in the therapeutic

dining area/dysphagia group at breakfast, lunchtime,

and dinner. TDT was administered in hourly formal

sessions and at meal times, 56 days per week,

for a minimum of 5 hrs per week, for a mean T SD

of 18 T 3 days during the course of inpatient rehabilitation.

Of the 92 patients who received TDT,

65 were provided with NMES treatment, described

below in the BInstrumentation[ section. The casecontrol

group for this study comprised the remaining

27 patients receiving only TDT. Both the

NMES and TDT treatment groups received, on average,

the same amount of SLP therapy sessions. The

patients demonstrating consistent safe swallowing

without any signs of aspiration on the SLP evaluations

and/or on the MBS study were then referred for

percutaneous gastrostomy feeding tube removal.

Instrumentation/NMES

Sixty-five patients received NMES with TDT,

including PRT. NMES treatment was provided by

NMES-certified/VitalStim-certified SLPs per the treatment

protocol described in the proprietary VitalStim

certification course and training manual.42 NMES

was provided in hourly sessions with a dual-channel

electrotherapy system (VitalStim Experia; Empi Inc,

St Paul, MN) with pulsed current at a fixed pulse rate

 mean, 80 Hz and with a pulse duration

of 100-300 microseconds. The SLPs adjusted the phase duration

of the current as low as 100 microseconds for some

patients to improve tolerance, whereas some patients

received a pulse rate of less than 80 Hz (80 Hz)

minimize fatigue. High volt treatment was used in

the patients having excessive adipose tissue, with the

phase duration fixed at 100 secs, the frequency set at

up to 120 Hz, and with a maximum intensity of 500 .

Before electrode placement, the face and/or the anterior

neck region of each patient was prepared with

an alcohol swab to remove any substance that might

interfere with electrode contact. Several standard

electrode placement configurations were used at the

discretion of the treating SLPs on the basis of each

patient’s initial clinical assessment (Fig. 1). NMES

was introduced with a gradual increase in the current

of up to a maximum of 25 mA/500 V as tolerated

and as necessary to evoke a submaximal muscle contraction.

Motor responses in the oropharyngeal muscles

were identified by the SLPs when (1) a grabbing

sensation was reported by the patient or (2) a submaximal

muscle contraction was palpated by the

SLP. Submaximal NMES stimulation was used in this

study because maximal stimulation may have negative

physiologic effects on swallowing function such as

laryngeal depression in patients with chronic dysphagia.

43 NMES was administered in conjunction with

PRT exercises13,3,641 which have been postulated to

maximize the efficacy of NMES treatment in dysphagia.

23,44 Therapeutic/trial feedings were introduced

as tolerated during NMES, with gradual adjustments

to bolus volume/consistencies, swallow strategies, and

the rate of oral intake. All patients were monitored

during NMES administration for any possible adverse

outcomes/side effects of the treatment including

acute cardiac arrhythmias, palpitations, chest pain,

hypotension, dizziness, interference with pacemaker

function, laryngospasm, glottis closure, burns, and

seizures. Standard electrode placements shown in

Figure 1 purposefully avoid the area of the carotid

body to minimize cardiovascular risks.

Outcome Measures

The primary outcome goal of this study was patient

improvement in swallowing status to feeding

tube independence. The functional swallowing ability

of each patient in this study was scored on admission

and at discharge using the FOIS,31 an objective

7-point ordinal dietary scale reflecting an individual’s

ability to safely swallow solids and liquids (Table 2).

The FOIS has been demonstrated to have strong reliability

and validity specific to populations of patients

who have had a stroke having dysphagia.31 The

interrater reliability of the HealthSouth SLPs was

not specifically assessed; however, each SLP involved

in this study had a mean of 5 yrs of clinical experience

in using the FOIS scale. The initial FOIS scores for all

patients ranged from 1 to 3, consistent with profound

to severe feeding tube dependent dysphagia verified

by the admission SLP clinical evaluations and the

preadmissionMBS studies, if available. The discharge

FOIS scores were not scored higher than 3 for any

patient who still required tube feedings as a result of

persistent signs of dysphagia on the basis of clinical

examination and/or a follow-up MBS study. The main

outcome measure of this study was the comparison

of the FOIS scores obtained for each group after

treatment.


Statistical Analyses:

Statistical Package for the Social Sciences version

19 was used for all analyses; P G 0.05 was

the level of significance for the comparisons. Means/

standard deviations/percentages were computed for

the demographic/clinical data. To compare the NMES

and case-control groups on variables of interest,

www.ajpmr.com NMES in Dysphagia 489

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FIGURE 1 VitalStim placement (adapted with permission by Empi, Inc).

490 Kushner et al. Am. J. Phys. Med. Rehabil. & Vol. 92, No. 6, June 2013

Copyright © 2013 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

independent-samples t tests were used for parametric

data, and W2 analyses and Mann-Whitney U test were

computed for categorical data. A logistic regression

was computed to predict FOIS independence

 using group membership as the independent

variable and age, sex , and stroke location

as covariates.


RESULTS:

The W2 and t test analyses revealed no significant

differences between the NMES and casecontrol

groups for demographic variables including

age (t =j0.85; P = 0.40) and sex (W2=0.05; P=0.94).

The Mann-Whitney U test revealed a statistically significant

difference between the groups for the initial

FOIS score (z = j2.4; P = 0.015), with the

NMES group having a mean rank of 42.64 and the

case-control TDT/PRT group having a mean rank of

55.8. Stroke location did not differ significantly between

the two groups (W2 = 4.2; P = 0.24). Thus, the

NMES and case-control groups were similar for all

demographic variables and stroke location, but the

NMES experimental group had statistically worse

initial FOIS scores.

The mean T SD FOIS score after NMES treatment

was 5.1 T 1.8 compared with the case-control

group, which had amean T SD FOIS score of 3.3 T 2.2.

The mean gain for the NMES group was 4.4 points;

and for case-control group, 2.4 points. Examination

of between-group differences showed significant improvement

in swallowing performance in the NMES

group compared with the case-control group (z=3.6;

P G 0.001; Fig. 2).

Thirty (46%) of 65 patients in the NMES group

had minimal or no swallowing restrictions after treatment, whereas only 7 (26%)

of 27 patients in the case-control group improved to

a significant difference (W2 = 6.0)

P = 0.01). A logistic regression computed to determine

the relationship between group membership

(NMES vs. case-control) and FOIS independence

controlling for age, sex , and stroke

location found no significant covariates, but FOIS

independence was significantly related to group

membership (W2 = 6.3; P = 0.01), with NMES treatment

predictive of better swallowing outcomes. No

adverse outcomes/side effects occurred in any of the

65 patients who received NMES in this study.

TABLE 2 Functional Oral Intake Scale31

Score Performance Implication Deficit

1 Aspirates saliva Nothing by mouth Profound

2 Tube dependent Nothing by mouth/minimal trials Profound

3 Tube dependent Full trials by mouth Severe

4 Total oral Single texture trials Moderate

5 Total oral Multiple texture trials Mild

6 Total oral By mouth/restrictions Minimal

7 Regular diet By mouth/no restrictions Normal

FIGURE 2 The mean FOIS scores for the NMES and case-control groups.

www.ajpmr.com NES in Dysphagia 491

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DISCUSSION

The results of this pilot study suggest the efficacy

of NMES when added to TDT, including PRT

exercises,13,3641 in comparison with TDT/PRT alone

during inpatient rehabilitation in reducing profound

to severe feeding tube dependent dysphagia

in patients who have had an acute stroke. A possible

explanation for NMES efficacy observed in

this study may be its theoretical dual mode of action

in potentiating standard TDT strategies that

target the oropharyngeal muscles in disuse atrophy

for strengthening while simultaneously stimulating

feedback to the cortical/subcortical swallowing areas

via the CPG to enhance brain plasticity/recovery of

swallowing control. It is known that impairment

of the cortical/subcortical pathway stimulation to the

muscles of swallowing after a stroke results in rapid

onset of disuse atrophy.5 Even a few days without

the estimated 600-2400 normal daily swallows could

result in disuse atrophy of the oropharyngeal muscles

after a stroke.5,45,46 Type 2 muscle fibers are the first

to undergo disuse atrophy,22,47 and these type 2

muscle fibers predominate in high speed contractions

of certain oropharygeal muscles important to normal

swallowing.22,47,48 TDT exercises predominantly target

type 1 muscle fibers, which typically activate with

less strenuous force than do type 2 muscle fibers.22,44

NMES stimulates forceful muscle contractions especially

in type 2 muscle fibers.5,22,27,30 Thus, NMES

with TDT, including PRT,13,3641 theoretically targets

both type 1 and type 2 muscles of swallowing for

strengthening.5,22,28,30

Enhancement of sensory feedback to the cortical/

subcortical swallowing centers is another mode of

action by which NMES may promote swallowing recovery.

Normal motor function, as well as motor

skills acquisition, is dependent on somatosensory input

to the cortical and subcortical brain structures.49,52

Somatosensory stimulation feedback can induce plastic

brain changes resulting in heightened corticomotor

excitability in brain areas corresponding to the

stimulated body part, which may outlast the stimulation

period.49,5356 Brain activation in both the

sensory and motor regions has been documented

by functional magnetic resonance imaging after peripheral

NMES in human subjects.57,.59 Pharyngeal

NMES has been shown to increase corticobulbar

excitability,53,60 increase brain functional magnetic

resonance imaging responses,59 and improve dysphagia

after a stroke.5,30,59 Safe swallowing is a complex

process that is initiated voluntarily but completed

as a reflex process involving the cranial nerves, the

CPG, and the cortical/subcortical brain swallowing

centers.10,12 Thus, the efficacy of NMES observed in

this study may also be explained by its theoretical

effects on stimulating brain plasticity/recovery in

swallowing control.

The rapid improvement in swallowing function

observed in the NMES group in this study is in contrast

to the findings of other studies that suggest that

most cases of severe to profound post-stroke dysphagia

have feeding tube dependence that continues from

15 wks to longer than 60 wks after stroke.6,8,61,65

There seems to be a therapeutic window for neural

repair/recovery that may be time sensitive after a

stroke because most functional recovery occurs within

3 mos of acute stroke onset.66 It is possible that NMES

with TDT and, particularly, PRT during inpatient rehabilitation

maximize the use of this potential therapeutic

window in stimulating plasticity/recovery in

the brain swallowing control centers. NMES with PRT

during inpatient rehabilitation may also promote early

recovery in type 2 oropharyngeal muscles in disuse

atrophy before the atrophy becomes too severe to respond

to short-term exercise therapy. This pilot study

further emphasizes the observation that NMES administration

with PRT13,36,41 may maximize recovery

of the oropharyngeal muscles in disuse atrophy.23,44 In

addition, sensory feedback to the brain swallowing

centers from NMES may be further enhanced when

the electrical stimulation feedback is used in combination

with active strength training.49 In this study,

as in others,5,22,26,28,30 no adverse outcomes or side

effects occurred with the administration of NMES.

The administration protocol of NMES in this pilot

study, including electrode placement and electrical

current settings, seems to be safe and well tolerated.


Study Limitations:

Most importantly, this was not a randomized

controlled study but, instead, a case-control study.

The comparison groups in this study were statistically

similar before treatment in the clinical and

demographic variables; however, they differed in

numbers because there were more than twice as

many patients in the NMES group. It is possible that

this difference in patient numbers could have biased

statistical power in favor of the NMES group by reducing

variability in the one group but not in the

other. In addition, because this was a clinical study,

there is a possibility that selection bias may have

unintentionally occurred. Furthermore, this study

did not involve a blinded design because the SLPs

who administered the swallowing therapy were also

the same clinicians who performed the pretreatment/

posttreatment swallow evaluations and scored the

FOIS. This could have resulted in bias based on the

expectations of the unblinded SLP. Furthermore,

the interrater reliability of the SLPs involved in this

492 Kushner et al. Am. J. Phys. Med. Rehabil. & Vol. 92, No. 6, June 2013

Copyright © 2013 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

study was not specifically assessed, although all had at

least 5 yrs’ clinical experience in using the FOIS scale.

In addition, not all patients in this study underwent

objective pretreatment/posttreatment MBS tests. In

addition, small-sample group comparisons are not

without limitations. Trends may be observed in a

larger sample study in which differences in treatment

efficacy may become apparent in comparison subgroups

affected by demographic or clinical factors.

CONCLUSIONS

The results of this study help to fill a gap in

clinical knowledge and suggest an efficacy of NMES

treatm13,36Y41 in patients who have had an acute

ent when added to TDT, including PRT exercises,

stroke having feeding tube dependent dysphagia

during inpatient rehabilitation. Randomized studies

will be necessary to validate this intervention. Given

the paucity of published studies on this important

clinical problem, NMES certainly deserves further

research in patients who have had an acute stroke

having profound to severe feeding tubeYdependent

dysphagia because it is safe when administered according

to the protocol/parameters used in this study,

it seems to be efficacious, and it is easy to implement

through trained SLPs.

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ORIGINAL RESEARCH ARTICLE

Neuromuscular Electrical Stimulation

Efficacy in Acute Stroke Feeding

TubeYDependent Dysphagia During

Inpatient Rehabilitation

ABSTRACT

Kushner DS, Peters K, Eroglu ST, Perless-Carroll M, Johnson-Greene D:

Neuromuscular electrical stimulation efficacy in acute stroke feeding

tubeYdependent dysphagia during inpatient rehabilitation. Am J Phys Med Rehabil

2013;92:486Y495.

Objective: The aim of this study was to compare the efficacy of neuromuscular

electrical stimulation (NMES) in addition to traditional dysphagia therapy (TDT) including

progressive resistance training (PRT) with that of TDT/PRT alone during inpatient

rehabilitation for treatment of feeding tubeYdependent dysphagia in patients who

have had an acute stroke.

Design: This study is an inpatient rehabilitation case-control study involving

92 patients who have had an acute stroke with initial Functional Oral Intake Scale

(FOIS) scores of 3 or lower and profound to severe feeding tubeYdependent dysphagia.

Sixty-five patients, the NMES group, received NMES with TDT/PRT, and

27 patients, the case-control group, received only TDT/PRT. Treatment occurred in

hourly sessions daily for a mean T SD of 18 T 3 days. W2 Analyses/t tests revealed no

significant statistical differences between the groups for age (t=j0.85; P = 0.40), sex

(W2 = 0.05; P = 0.94), and stroke location (W2 = 4.2; P = 0.24). A Mann-Whitney U

test revealed a statistically significant difference between the groups for the initial FOIS

score (z = j2.4; P = 0.015), with the NMES group having worse initial scores with a

mean rank of 42.64 and the case-control TDT/PRTgroup having a mean rank of 55.8.

The main outcome measure was the comparison of the FOIS scores after treatment.

Results: The mean T SD FOIS score after NMES with TDT/PRT treatment

was 5.1 T 1.8 compared with 3.3 T 2.2 in the case-control TDT/PRTgroup. The mean

gain for the NMES group was 4.4 points; and for the case-control group, 2.4 points.

Significant improvement in swallowing performance was found for the NMES group

compared with the TDT/PRT group (z = 3.64; P G 0.001). Within the NMES group,

46% (30 of 65) of the patients had minimal or no swallowing restrictions (FOIS score

of 5Y7) after treatment, whereas 26% (7 of 27) of those in the case-control group

improved to FOIS scores of 5Y7, a statistically significant difference (W2 = 6.0;

P = 0.01).

Conclusions: This study suggests that NMES with TDT/PRT is significantly

more effective than TDT/PRTalone during inpatient rehabilitation in reducing feeding

tubeYdependent dysphagia in patients who have had an acute stroke.

Key Words: Stroke, Dysphagia, Deglutition Disorders, Rehabilitation, Electric

Stimulation Therapy

Authors:

David S. Kushner, MD

Kenneth Peters, MS, CCC-SLP

Stacy Thomashaw Eroglu, MA, CCC-SLP

Melissa Perless-Carroll, MS, CCC-SLP

Douglas Johnson-Greene, PhD

Affiliations:

From the Department of Rehabilitation

Medicine, University of Miami Miller

School of Medicine, Miami, Florida

(DSK, DJ-G); Department of

Speech-Language Pathology,

HealthSouth Rehabilitation Hospital,

Miami, Florida (KP); and Department

of Speech-Language Pathology,

HealthSouth Rehabilitation Hospital,

Sunrise, Florida (STE, MP-C).

Correspondence:

All correspondence and requests for

reprints should be addressed to: David

S. Kushner, MD, Department of

Rehabilitation Medicine, University of

Miami Miller School of Medicine,

20601 Old Cutler Rd, Miami FL 3318.

Disclosures:

Supported, in part, by the United States

Department of Education, National

Institute of Disability Research and

Rehabilitation grant H133A120099

(to D.J-G.)

Presented at the American Congress of

Rehabilitation Medicine annual

conference in Atlanta in October 2011,

and the abstract was published in

Archives of Physical Medicine and

Rehabilitation October

2011;92(10):1691Y2.

Financial disclosure statements have

been obtained, and no conflicts of

interest have been reported by the

authors or by any individuals in control

of the content of this article.

0894-9115/13/9206-0486/0

American Journal of Physical

Medicine & Rehabilitation

Copyright * 2013 by Lippincott

Williams & Wilkins

DOI: 10.1097/PHM.0b013e31828762ec

486 Am. J. Phys. Med. Rehabil. & Vol. 92, No. 6, June 2013

Copyright © 2013 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

Approximately 800,000 acute strokes occur annually

in the United States,1,2 of which 45%Y70% of

cases have dysphagia.1Y6 Dysphagia increases the risk

for aspiration pneumonia,malnutrition/dehydration,

depression, and premature death. Dysphagia complications

impair recovery and lead to prolonged

hospitalizations; rehospitalizations; and the need

for respiratory support, tracheotomy, tube feedings,

and related nutritional supplements and equipment,

resulting in increased healthcare costs. The average

cost per patient associated with percutaneous tube

feedings is estimated to exceed $30,000 per year.7 In

patients who have had an acute stroke having dysphagia,

it is estimated that more than 11% require

placement of percutaneous gastrostomy tubes annually,

and at least 50% of those individuals will require

it long-term.6,8 Aspiration pneumonia is the

most common cause of death in individuals having

untreated dysphagia after stroke,9 accounting for at

least 10% of deaths occurring within 30 days of the

initial hospital admission.4 The mortality rate for

feeding tubeYdependent patients may be as high as

36% during the 2 yrs after the acute stroke.6

Dysphagia in stroke results from impairments

of the oral and pharyngeal stages of swallowing.10,11

During the oral-pharyngeal stages of swallowing, the

contraction and inhibition of approximately 50 pairs

of muscles are coordinated in the propulsion of a

food bolus, solid or liquid, to the esophagus while

protecting the airway to the larynx.10,11 Ascending

sensory input from the oropharynx and descending

motor input from the cortical/subcortical brain swallowing

centers are integrated in the lower brainstem

in a network of neurons known as the central

pattern generator (CPG).10Y12 The swallowing process

is mediated via the CPG and the cranial nerve

nuclei of V, VII, IX, X, and XII.10Y12 Treatments of

dysphagia in stroke may target the enhancement of

sensory feedback from the oropharynx to the CPG

and/or target strengthening of the oropharyngeal

musculature that is in disuse atrophy secondary to

reduced motor output from the CPG.

Traditional dysphagia therapy (TDT) involves

oral motor exercises, including progressive resistance

training (PRT), to strengthen the oropharyngeal musculature

that is in disuse atrophy13; biofeedback

techniques and sensory stimulation to target the

CPG5,14Y17; and compensatory swallowing strategies

including various modifications of head, neck, and

body postures.13,18 Adjustment of food/liquid temperature,

viscosity, and volume18,19 and the use of

tube feedings for severe dysphagia are also included.

TDT strategies have limited success in severe

dysphagia, require prolonged durations of treatment

of up to 52 wks,5 and have therapeutic benefits that

may be short lasting.20,21 Transcutaneous neuromuscular

electrical stimulation (NMES) was approved by

the Food and Drug Administration in 2001 as a treatment

of dysphagia22 and is hypothesized to target

strengthening of the oropharyngeal musculature in

disuse atrophy while also providing sensory feedback

to the CPG and the cortical/subcortical swallowing

centers.20,23 The use ofNMES in dysphagia treatment

was identified in a 2005 national survey by speechlanguage

pathologists (SLPs) as an area of interest

needing further evidence-based research.24 However,

6 yrs since that survey, the use of NMES in clinical

practice still remains controversial. Efficacy studies

that have been published since the Food and Drug

Administration approval have had mixed results for

patients having mostly chronic mild, moderate, and

severe dysphagia of various etiologies.20,25Y29 Only

two published randomized NMES studies thus far

have been limited to only patients who have had a

stroke having dysphagia,26,30 of which one demonstrated

efficacy,30 whereas one did not.26 Both of

these studies included patients who have had subacute

and chronic stroke with mild to severe dysphagia

but excluded patients who have had brainstem

strokes.26,30 There has not yet been a study to evaluate

NMES efficacy when added to TDT in comparison

with TDT alone limited to only patients who have

had acute ischemic or hemorrhagic hemisphere and

brainstem stroke having severe to profound feeding

tubeYdependent dysphagia during inpatient rehabilitation;

thus, the purpose of this study was to fill that

gap in clinical knowledge.

METHODS

Participants

This study included 92 patients admitted at

two HealthSouth Rehabilitation Hospital inpatient

facilities (HealthSouth, Miami, FL, and HealthSouth,

Sunrise, FL), from 2005 through 2011, who have

had acute stroke with initial Functional Oral Intake

Scale (FOIS)31 scores of 3 or lower and severe to

profound feeding tubeYdependent dysphagia. The

severe to profound dysphagia was defined in this

study as a high risk for aspiration of all solids and/or

liquids to aspiration of all consistencies including

saliva on the initial SLP swallowing assessment, with

nothing-by-mouth recommendation and tube feeding

required for maintaining the patients’ nutritional

needs. Inclusion criteria for this study were adult patients

having percutaneous gastrostomy feeding tubes

with profound to severe oropharyngeal dysphagia,

www.ajpmr.com NES in Dysphagia 487

Copyright © 2013 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

having the ability to follow a minimum of one-step

simple commands consistently, and having had newonset

hemorrhagic or ischemic stroke. Participants

were excluded from this study if they had esophagealphase

swallowing disorders, structural swallowing

disorders, or comorbid neurologic degenerative disorders

or if there was documentation of any behavioral

disorder or other issues that interfered with a patient’s

ability to consistently participate in dysphagia treatment.

In addition, any patient who has had a stroke

admitted with a feeding tube who did not have clinical

signs of profound to severe dysphagia per the initial

SLP evaluation was excluded from this study, unless a

high risk for silent aspiration was subsequently documented

by amodified barium swallow (MBS)32 test.

Thus, pretreatment feeding tubeYdependent dysphagia

was confirmed for all patients included in this

study. An exclusion criterion for the NMES group was

inability to tolerate the electrical stimulation treatment.

Medical contraindications for the NMES group,

at the discretion of attending physicians, included

having cardiac pacemakers or a history of seizures or

epilepsy. Consent for inpatient rehabilitation treatment

was obtained for all patients directly or from their

healthcare proxies/surrogates on admission per the

standard HealthSouth corporate policy/protocol. Further

consent was obtained from the attending physicians

before administration of NMES to any patient.

NMES was prescribed by approximately half of the

attending physicians for all patients having feeding

tube dependency, whereas about one-fourth prescribed

NMES only to those patients having no

history of seizures or cardiac pacemakers, and the

remaining one-fourth did not prescribe NMES to

any patient because of lack of published evidence

supporting NMES efficacy, which is one of the main

reasons for this study. Thus, of the 92 patients who

have had an acute stroke, 65 received NMES/TDT

and 27 received only TDT. The patients who received

NMES/TDT were started on treatment at a mean of

15.7 days after the acute stroke, whereas the patients

in the TDT group initiated treatment at a mean of

15.4 days after the stroke. Demographics of both the

NMES and TDT cohorts are given (Table 1). Participant

data were obtained and maintained by the SLP

investigators, such that the patients cannot be identified

directly or indirectly in any manner. This study

was approved by the HealthSouth Corporate Clinical

Research Review Committee.

Procedure

All patients in this study were evaluated within

24 hrs of admission by the SLPs who have a mean of

7 yrs of licensed clinical experience and a certificate

of clinical competency. The initial FOIS31 scores were

determined for each patient at risk for pharyngeal

aspiration/penetration by solid and/or liquid boluses

on the basis of the admission SLP clinical assessment

and the preadmission MBS test results, if available.

The SLP swallowing evaluations have been shown

to have good sensitivity, specificity, and interrater

reliability.33 Clinical evaluations by the experienced

SLPs, including testing for voluntary cough, dysphonia,

dysarthria, impaired gag reflex, postswallow

cough, and voice change,34 are effective in diagnosing

patients who have had a stroke at risk for pharyngeal

penetration/aspiration, whereas MBS studies have

been shown to be more sensitive to the diagnosis of

silent aspiration.34,35 Thus, any patient who has had a

stroke admitted with a feeding tube who did not have

clinical signs of profound to severe dysphagia per the

initial SLP evaluation was referred for an MBS study.

In this manner, feeding tube dependency was confirmed

at the time of admission, before treatment and

inclusion in this study. All patients, including those

in the NMES group, received TDT on the basis of

each patient’s initial SLP clinical assessment. Therapeutic

exercises were provided as needed to increase

strength, endurance, range of motion, and mobility

of the oral-facial, lingual, and laryngeal musculature.

All patients received PRT13 including any combination

of lingual-strengthening exercises,13,36,37 laryngeal

adduction-elevation exercises,13 effortful swallow maneuver,

13,38 Mendelsohn maneuver,13,39 Masako maneuver,

13,40 and Shaker exercises.13,37,41 The patients

also received sensory biofeedback treatments including

thermal stimulation.5,14Y17 Compensatory

swallowing strategies,13,18 includingmodifications of

TABLE 1 The case-control and NMES group

demographics

Case-control group demographics

Patients, N 27

Left hemisphere stroke 9

Right hemisphere stroke 10

Intracerebral hemorrhage 7

Brainstem stroke 1

Age range, yrs 49Y91

Men, n 16

Women, n 11

NMES group demographics

Patients, N 65

Left hemisphere stroke 36

Right hemisphere stroke 14

Intracerebral hemorrhage 12

Brainstem stroke 3

Age range, yrs 19Y89

Men, n 38

Women, n 27

488 Kushner et al. Am. J. Phys. Med. Rehabil. & Vol. 92, No. 6, June 2013

Copyright © 2013 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

head, neck, and body postures, were used as needed

on the basis of any anatomic or postural deficits. The

patients received therapeutic or trial feedings as tolerated,

with one-to-one supervision by the SLP either

in private treatment sessions or in the therapeutic

dining area/dysphagia group at breakfast, lunchtime,

and dinner. TDT was administered in hourly formal

sessions and at meal times, 5Y6 days per week,

for a minimum of 5 hrs per week, for a mean T SD

of 18 T 3 days during the course of inpatient rehabilitation.

Of the 92 patients who received TDT,

65 were provided with NMES treatment, described

below in the BInstrumentation[ section. The casecontrol

group for this study comprised the remaining

27 patients receiving only TDT. Both the

NMES and TDT treatment groups received, on average,

the same amount of SLP therapy sessions. The

patients demonstrating consistent safe swallowing

without any signs of aspiration on the SLP evaluations

and/or on the MBS study were then referred for

percutaneous gastrostomy feeding tube removal.

Instrumentation/NMES

Sixty-five patients received NMES with TDT,

including PRT. NMES treatment was provided by

NMES-certified/VitalStim-certified SLPs per the treatment

protocol described in the proprietary VitalStim

certification course and training manual.42 NMES

was provided in hourly sessions with a dual-channel

electrotherapy system (VitalStim Experia; Empi Inc,

St Paul, MN) with pulsed current at a fixed pulse rate

of 5Y120 Hz (mean, 80 Hz) and with a pulse duration

of 100Y300 Ksecs. The SLPs adjusted the phase duration

of the current as low as 100 Ksecs for some

patients to improve tolerance, whereas some patients

received a pulse rate of less than 80 Hz (5Y80 Hz) to

minimize fatigue. High volt treatment was used in

the patients having excessive adipose tissue, with the

phase duration fixed at 100Ksecs, the frequency set at

up to 120 Hz, and with a maximumintensity of 500 V.

Before electrode placement, the face and/or the anterior

neck region of each patient was prepared with

an alcohol swab to remove any substance that might

interfere with electrode contact. Several standard

electrode placement configurations were used at the

discretion of the treating SLPs on the basis of each

patient’s initial clinical assessment (Fig. 1). NMES

was introduced with a gradual increase in the current

of up to a maximum of 25 mA/500 V as tolerated

and as necessary to evoke a submaximal muscle contraction.

Motor responses in the oropharyngeal muscles

were identified by the SLPs when (1) a grabbing

sensation was reported by the patient or (2) a submaximal

muscle contraction was palpated by the

SLP. Submaximal NMES stimulation was used in this

study because maximal stimulation may have negative

physiologic effects on swallowing function such as

laryngeal depression in patients with chronic dysphagia.

43 NMES was administered in conjunction with

PRT exercises13,36Y41 which have been postulated to

maximize the efficacy of NMES treatment in dysphagia.

23,44 Therapeutic/trial feedings were introduced

as tolerated during NMES, with gradual adjustments

to bolus volume/consistencies, swallow strategies, and

the rate of oral intake. All patients were monitored

during NMES administration for any possible adverse

outcomes/side effects of the treatment including

acute cardiac arrhythmias, palpitations, chest pain,

hypotension, dizziness, interference with pacemaker

function, laryngospasm, glottis closure, burns, and

seizures. Standard electrode placements shown in

Figure 1 purposefully avoid the area of the carotid

body to minimize cardiovascular risks.

Outcome Measures

The primary outcome goal of this study was patient

improvement in swallowing status to feeding

tube independence. The functional swallowing ability

of each patient in this study was scored on admission

and at discharge using the FOIS,31 an objective

7-point ordinal dietary scale reflecting an individual’s

ability to safely swallow solids and liquids (Table 2).

The FOIS has been demonstrated to have strong reliability

and validity specific to populations of patients

who have had a stroke having dysphagia.31 The

interrater reliability of the HealthSouth SLPs was

not specifically assessed; however, each SLP involved

in this study had a mean of 5 yrs of clinical experience

in using the FOIS scale. The initial FOIS scores for all

patients ranged from 1 to 3, consistent with profound

to severe feeding tubeYdependent dysphagia verified

by the admission SLP clinical evaluations and the

preadmissionMBS studies, if available. The discharge

FOIS scores were not scored higher than 3 for any

patient who still required tube feedings as a result of

persistent signs of dysphagia on the basis of clinical

examination and/or a follow-up MBS study. The main

outcome measure of this study was the comparison

of the FOIS scores obtained for each group after

treatment.

Statistical Analyses

Statistical Package for the Social Sciences version

19 was used for all analyses; P G 0.05 was

the level of significance for the comparisons. Means/

standard deviations/percentages were computed for

the demographic/clinical data. To compare theNMES

and case-control groups on variables of interest,

www.ajpmr.com NES in Dysphagia 489

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FIGURE 1 VitalStim placement (adapted with permission by Empi, Inc).

490 Kushner et al. Am. J. Phys. Med. Rehabil. & Vol. 92, No. 6, June 2013

Copyright © 2013 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

independent-samples t tests were used for parametric

data, and W2 analyses and Mann-Whitney U test were

computed for categorical data. A logistic regression

was computed to predict FOIS independence

(scores of 5Y7), using group membership as the independent

variable and age, sex , and stroke location

as covariates.

RESULTS

The W2 and t test analyses revealed no significant

differences between the NMES and casecontrol

groups for demographic variables including

age (t =j0.85; P = 0.40) and sex (W2=0.05; P=0.94).

The Mann-Whitney U test revealed a statistically significant

difference between the groups for the initial

FOIS score (z = j2.4; P = 0.015), with the

NMES group having a mean rank of 42.64 and the

case-control TDT/PRT group having a mean rank of

55.8. Stroke location did not differ significantly between

the two groups (W2 = 4.2; P = 0.24). Thus, the

NMES and case-control groups were similar for all

demographic variables and stroke location, but the

NMES experimental group had statistically worse

initial FOIS scores.

The mean T SD FOIS score after NMES treatment

was 5.1 T 1.8 compared with the case-control

group, which had amean T SD FOIS score of 3.3 T 2.2.

The mean gain for the NMES group was 4.4 points;

and for case-control group, 2.4 points. Examination

of between-group differences showed significant improvement

in swallowing performance in the NMES

group compared with the case-control group (z=3.6;

P G 0.001; Fig. 2).

Thirty (46%) of 65 patients in the NMES group

had minimal or no swallowing restrictions (FOIS

scores of 5Y7) after treatment, whereas only 7 (26%)

of 27 patients in the case-control group improved to

FOIS scores of 5Y7, a significant difference (W2 = 6.0;

P = 0.01). A logistic regression computed to determine

the relationship between group membership

(NMES vs. case-control) and FOIS independence

(scores of 5Y7) controlling for age, sex , and stroke

location found no significant covariates, but FOIS

independence was significantly related to group

membership (W2 = 6.3; P = 0.01), with NMES treatment

predictive of better swallowing outcomes. No

adverse outcomes/side effects occurred in any of the

65 patients who received NMES in this study.

TABLE 2 Functional Oral Intake Scale31

Score Performance Implication Deficit

1 Aspirates saliva Nothing by mouth Profound

2 Tube dependent Nothing by mouth/minimal trials Profound

3 Tube dependent Full trials by mouth Severe

4 Total oral Single texture trials Moderate

5 Total oral Multiple texture trials Mild

6 Total oral By mouth/restrictions Minimal

7 Regular diet By mouth/no restrictions Normal

FIGURE 2 The mean FOIS scores for the NMES and case-control groups.

www.ajpmr.com NES in Dysphagia 491

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DISCUSSION

The results of this pilot study suggest the efficacy

of NMES when added to TDT, including PRT

exercises,13,36Y41 in comparison with TDT/PRT alone

during inpatient rehabilitation in reducing profound

to severe feeding tubeYdependent dysphagia

in patients who have had an acute stroke. A possible

explanation for NMES efficacy observed in

this study may be its theoretical dual mode of action

in potentiating standard TDT strategies that

target the oropharyngeal muscles in disuse atrophy

for strengthening while simultaneously stimulating

feedback to the cortical/subcortical swallowing areas

via the CPG to enhance brain plasticity/recovery of

swallowing control. It is known that impairment

of the cortical/subcortical pathway stimulation to the

muscles of swallowing after a stroke results in rapid

onset of disuse atrophy.5 Even a few days without

the estimated 600Y2400 normal daily swallows could

result in disuse atrophy of the oropharyngeal muscles

after a stroke.5,45,46 Type 2 muscle fibers are the first

to undergo disuse atrophy,22,47 and these type 2

muscle fibers predominate in high speed contractions

of certain oropharygeal muscles important to normal

swallowing.22,47,48 TDT exercises predominantly target

type 1 muscle fibers, which typically activate with

less strenuous force than do type 2 muscle fibers.22,44

NMES stimulates forceful muscle contractions especially

in type 2 muscle fibers.5,22,27,30 Thus, NMES

with TDT, including PRT,13,36Y41 theoretically targets

both type 1 and type 2 muscles of swallowing for

strengthening.5,22,28,30

Enhancement of sensory feedback to the cortical/

subcortical swallowing centers is another mode of

action by which NMES may promote swallowing recovery.

Normal motor function, as well as motor

skills acquisition, is dependent on somatosensory input

to the cortical and subcortical brain structures.49Y52

Somatosensory stimulation feedback can induce plastic

brain changes resulting in heightened corticomotor

excitability in brain areas corresponding to the

stimulated body part, which may outlast the stimulation

period.49,53Y56 Brain activation in both the

sensory and motor regions has been documented

by functional magnetic resonance imaging after peripheral

NMES in human subjects.57Y59 Pharyngeal

NMES has been shown to increase corticobulbar

excitability,53,60 increase brain functional magnetic

resonance imaging responses,59 and improve dysphagia

after a stroke.5,30,59 Safe swallowing is a complex

process that is initiated voluntarily but completed

as a reflex process involving the cranial nerves, the

CPG, and the cortical/subcortical brain swallowing

centers.10Y12 Thus, the efficacy of NMES observed in

this study may also be explained by its theoretical

effects on stimulating brain plasticity/recovery in

swallowing control.

The rapid improvement in swallowing function

observed in the NMES group in this study is in contrast

to the findings of other studies that suggest that

most cases of severe to profound post-stroke dysphagia

have feeding tube dependence that continues from

15 wks to longer than 60 wks after stroke.6,8,61Y65

There seems to be a therapeutic window for neural

repair/recovery that may be time sensitive after a

stroke becausemost functional recovery occurswithin

3mos of acute stroke onset.66 It is possible that NMES

with TDT and, particularly, PRT during inpatient rehabilitation

maximize the use of this potential therapeutic

window in stimulating plasticity/recovery in

the brain swallowing control centers. NMES with PRT

during inpatient rehabilitationmay also promote early

recovery in type 2 oropharyngeal muscles in disuse

atrophy before the atrophy becomes too severe to respond

to short-term exercise therapy. This pilot study

further emphasizes the observation that NMES administration

with PRT13,36Y41 may maximize recovery

of the oropharyngeal muscles in disuse atrophy.23,44 In

addition, sensory feedback to the brain swallowing

centers from NMES may be further enhanced when

the electrical stimulation feedback is used in combination

with active strength training.49 In this study,

as in others,5,22,26,28,30 no adverse outcomes or side

effects occurred with the administration of NMES.

The administration protocol of NMES in this pilot

study, including electrode placement and electrical

current settings, seems to be safe and well tolerated.

Study Limitations

Most importantly, this was not a randomized

controlled study but, instead, a case-control study.

The comparison groups in this study were statistically

similar before treatment in the clinical and

demographic variables; however, they differed in

numbers because there were more than twice as

many patients in the NMES group. It is possible that

this difference in patient numbers could have biased

statistical power in favor of the NMES group by reducing

variability in the one group but not in the

other. In addition, because this was a clinical study,

there is a possibility that selection bias may have

unintentionally occurred. Furthermore, this study

did not involve a blinded design because the SLPs

who administered the swallowing therapy were also

the same clinicians who performed the pretreatment/

posttreatment swallow evaluations and scored the

FOIS. This could have resulted in bias based on the

expectations of the unblinded SLP. Furthermore,

the interrater reliability of the SLPs involved in this

492 Kushner et al. Am. J. Phys. Med. Rehabil. & Vol. 92, No. 6, June 2013

Copyright © 2013 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

study was not specifically assessed, although all had at

least 5 yrs’ clinical experience in using the FOIS scale.

In addition, not all patients in this study underwent

objective pretreatment/posttreatment MBS tests. In

addition, small-sample group comparisons are not

without limitations. Trends may be observed in a

larger sample study in which differences in treatment

efficacy may become apparent in comparison subgroups

affected by demographic or clinical factors.

CONCLUSIONS

The results of this study help to fill a gap in

clinical knowledge and suggest an efficacy of NMES

treatment when added to TDT, including PRT exercises,

13,36Y41 in patients who have had an acute

stroke having feeding tubeYdependent dysphagia

during inpatient rehabilitation. Randomized studies

will be necessary to validate this intervention. Given

the paucity of published studies on this important

clinical problem, NMES certainly deserves further

research in patients who have had an acute stroke

having profound to severe feeding tubeYdependent

dysphagia because it is safe when administered according

to the protocol/parameters used in this study,

it seems to be efficacious, and it is easy to implement

through trained SLPs.

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