Dysphagia
DOI 10.1007/s00455-016-9736-4
ORIGINAL ARTICLE
A Comparative Study Between Two Sensory Stimulation
Strategies After Two Weeks Treatment on Older Patients
with Oropharyngeal Dysphagia
Omar Ortega1 • Laia Rofes1 • Alberto Martin2 • Viridiana Arreola2
Irene López2 • Pere Clavé1,2,3
Received: 17 March 2016 / Accepted: 21 July 2016
 Springer Science+Business Media New York 2016
Abstract Oropharyngeal dysphagia (OD) is a prevalent
geriatric syndrome. Treatment is based on compensatory
strategies to avoid complications. New treatments based on
sensory stimulation to promote the recovery of the swal-
lowing function have proved effective in acute studies but
prolonged treatment needs further research. Our aim was to
evaluate and compare the effect of two, longer-term sen-
sory treatment strategies on older patients with OD. 38
older patients (C70 years) were studied with videofluo-
roscopy (pre/posttreatment) and randomized into two
10-day treatment groups: Group A—transient receptor
potential vanilloid 1 (TRPV1) agonist (capsaicin
1 9 10-5 M) and Group B—transcutaneous sensory elec-
trical stimulation (TSES) (Intelect VitalStim, biphasic
pulses, 300 ls, 80 Hz). Patients were analyzed for treat-
ment response. Patients were old (80.47 ± 5.2 years), with
comorbidities (3.11 ± 1.59 Charlson Index), polymedica-
tion (8.92 ± 3.31 drugs/patient), and mild functional
impairment (86.84 ± 17.84 Barthel Index), and 28.9 %
were at risk of malnutrition (MNA-sf). Overall, all patients
Electronic supplementary material The online version of this
article (doi:10.1007/s00455-016-9736-4) contains supplementary
material, which is available to authorized users.
& Omar Ortega
oortega@csdm.cat
1
Centro de Investigación Biomédica en Red de enfermedades
hepáticas y digestivas (CIBERehd), Instituto de Salud Carlos
III, Barcelona, Spain
2 cacy of swallow (oropharyngeal residue), which can lead to
Unitat d’Exploracions Funcionals Digestives, Laboratori de
Fisiologia Digestiva CIBERehd CSdM-UAB, Hospital de
Mataró, Barcelona, Spain
3
Fundació Institut d’Investigació Germans Trias i Pujol,
Badalona, Spain
•
had videofluoroscopic signs of impaired safety of swallow
(ISS) with delayed oropharyngeal swallow response
(OSR). After sensory stimulation, prevalence of ISS
decreased to 68.42 % in both groups (P = 0.019). There
were 68.42 % responders in Group A (TRPV1) and
42.11 % in Group B (TSES). Group A responders showed
an improvement in the penetration–aspiration scale (PAS,
5.23 ± 2.04 to 3 ± 1.47; P = 0.002), and the same was
true for those of Group B (4.63 ± 1.41 to 2.13 ± 0.64;
P = 0.007). 10-day sensory stimulation with either therapy
improved safety of swallow and OSR in older patients with
OD, reducing the severity of OD in a significant subgroup
of these patients.
Keywords Deglutition
Deglutition disorders

Swallowing disorders
Therapeutics
Electric stimulation
therapy
TRPV1 agonist
Older patients
Introduction
Oropharyngeal dysphagia (OD) is a common geriatric
syndrome, with prevalence rates according to patients’
phenotype: 23 % for independently living older people [1];
47 % for patients in acute geriatric units; 55 % for hospi-
talized older patients with community-acquired pneumonia
(CAP), and 56–78 % for institutionalized older residents
[1–3].
Patients with OD may present impaired safety of swal-
low (penetrations and/or aspirations) and/or impaired effi-
several serious complications like malnutrition, dehydra-
tion, lower respiratory tract infections, aspiration pneu-
monia (AP), and readmissions and increase in morbi-
mortality [1, 3–6]. Impaired safety of swallow is
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 O. Ortega et al.: A Comparative Study Between Two Sensory Stimulation Strategies After…
characterized by delayed laryngeal vestibule closure (LVC)
and impaired efficacy by impaired tongue propulsion and
delayed maximal vertical hyoid motion [7].
OD in the older population is related to motor and
sensory impairments. Motor impairments are mainly
caused by the loss of muscular force and bolus propulsion
strength with aging, associated with malnutrition and sar-
copenia [8–10]. Sensory impairments of the pharyngeal
and supraglottic areas have been related to a reduction of
myelinated nerve fibers of the superior laryngeal nerve
[11–14]. These deficits have been related to OD and
impaired safety of swallow [15, 16]. In healthy persons, the
swallowing center receives high afferent input, suggesting
the involvement of sensory feedback during swallowing,
and that input is of key importance to trigger and modulate
the oropharyngeal swallow response (OSR). However, in
older persons, sensory input of the pharynx and larynx is
impaired, and this alteration is very prevalent and strongly
associated with the presence of aspirations [11, 12].
Nowadays, the majority of older patients with OD are
managed with compensatory strategies such as fluid and
diet adaptation with changes in bolus volume and viscosity,
and swallowing maneuvers and head postures [17–19].
These strategies, although effective in compensating
swallowing impairments, do not improve the OSR [7, 20].
A systematic review on the effects of OD therapy con-
cluded that ‘‘although some significant positive outcome
studies have been published, there is a need for further
research using randomized controlled trials’’ [21].
Innovative treatments are being tested to improve OSR
and avoid OD complications. One of these treatments is
based on increasing the oropharyngeal sensory input
through the afferent pathways using chemical, physical, or
electrical stimuli [22]. The rise of sensory stimuli may
increase sensory input to the swallowing center of the brain
stem, leading to earlier initiation of deglutition and timely
protection of the respiratory airway. Moreover, periodical
sensory stimulation may reorganize the motor cortex and
induce cortical neuroplasticity facilitating deglutition [22].
Transcutaneous sensory electrical stimulation (TSES) or
chemical stimulation (such as transient receptor potential
cation channel subfamily V member 1 (TRPV1) agonists)
are two sensory stimulation strategies that can be used to
that purpose.
Two studies from our group on older patients with OD
showed that the supplementation of the bolus with TRPV1
and transient receptor potential cation channel subfamily
A member 1 (TRPA1) agonists significantly improved
impaired safety [23, 24] and efficacy of swallow [24].
Other publications showed that acute administration of
capsaicin (10-11 to 10-9 M) reduced the latency of
swallow reflex (LSR) [25], and that daily administration
of the same compound during 4 weeks (10-6 M) also
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shortened the LSR, protecting the airway in older patients
with OD, particularly those with risk of aspiration [26]. A
recent publication also showed a reduction in the LSR
after the ingestion of capsaicin-supplemented food during
20 days [27]. The few studies using transcutaneous sen-
sory electrical stimulation (TSES) have shown contro-
versial results. Two acute studies using TSES showed an
increase in base of tongue pressures in older adults
[28, 29]. One study in patients with neurogenic OD,
which consisted of 6 weeks treatment with TSES, showed
an improvement of the swallow reaction time, a reduction
in the aspiration scores, and an improvement in quality of
life of the participants [30]. Another pair of studies
comparing 15 days traditional logopedic dysphagia treat-
ment (TLDT) versus TLDT ? TSES with patients with
Parkinson’s disease showed no significant improvement
between groups, suggesting a therapy effect of TLDT
without any additional influence of TSES [31, 32].
Finally, two more publications showed significant
improvements in the OSR and prevalence of aspirations in
poststroke patients [33, 34]. Although the articles pub-
lished on this topic are increasing, the mid-term effect of
these therapies on older patients with OD is fairly
unknown.
The aim of this study was to evaluate and compare with
videofluoroscopy (VFS) the therapeutic effect of two dif-
ferent two-week interventions based on sensory stimulation
of the afferent deglutition pathways (TRPV1 agonist and
TSES) on older patients with OD.
Patients and Methods
Study Population
We studied 38 older patients (70 years or older) with OD
that were prospectively recruited from the Gastrointestinal
Physiology Unit of the Hospital de Mataró (Spain) between
November 2012 and June 2016 (Fig. 1). Inclusion criteria
were to be 70-year old or older and have confirmed diag-
nosis of OD with VFS signs of impaired safety of swallow
(Penetration–Aspiration Scale [ 2) [35]. Exclusion criteria
were active neoplasm or infectious process, epilepsy or
convulsive disorders, gastroesophageal reflux disease,
implanted electrodes or pacemakers, severe dementia, and
to be currently participating in another clinical trial. All
participants were informed about the study and signed the
informed consent form. Study protocol was approved by
the Ethics Committee of the Hospital de Mataró (CEIC
04/12) and was conducted according to the principles and
rules laid down in the Declaration of Helsinki and its
subsequent amendments and following the EU rules for
clinical trials on humans (EU Clinical Trial Regulation
O. Ortega et al.: A Comparative Study Between Two Sensory Stimulation Strategies After…
Fig. 1 Study flow chart. TRPV1
transient receptor potential
vanilloid 1, TSES
transcutaneous sensory
electrical stimulation
(EU-CTR, EU No 536/2014)). ClinicalTrials.gov registra-
tion code: NCT01762228.
Swallowing Evaluation Measurements
Clinical Symptoms of OD
The Eating Assessment Tool (EAT-10), a screening ques-
tionnaire to assess the risk of OD, was administered to the
patients before and after the two-week treatment [32, 33].
Clinical Signs of OD
The V-VST was used in order to clinically screen patients
for dysphagia and specifically for impaired safety of
swallow before the treatment. This test uses three volumes
and three viscosities together with a pulse oximeter to
assess clinical signs of OD. The characteristics of this tool
have been described elsewhere [7, 20].
Videofluoroscopic Study
VFS was performed before and 5 days after the treatment to
assess its effect objectively by measuring and quantifying the
severity of OD and the OSR, including hyoid motion. Patients
were studied seated, in a lateral projection which included the
oral cavity, pharynx, larynx, and cervical esophagus. Vide-
ofluoroscopic recordings were obtained with a Super XT-20
Toshiba Intensifier (Toshiba Medical Systems Europe,
Zoetermeer, The Netherlands) and recorded at 25 frames/s
using a Panasonic AG DVX-100B video camera (Matsushita
Electric Industrial Co, Osaka, Japan). Patients were studied
during the deglutition of series of 5, 10, and 20 mL nectar
(274.42 ± 13.14 mPa s), liquid (20.40 ± 0.23 mPa s), and
pudding boluses (3931.23 ± 166.15 mPa s). Nectar and
pudding viscosity were obtained by adding 3.5 g and 8.5 g,
respectively, of thickener Resource ThickenUp (Nestlé
Nutrition, Barcelona, Spain) to 100 mL of liquid composed
by 1:1 mineral water and the X-ray contrast Gastrografin
(Bayer Hispania SL, Sant Joan Despı́, Spain). Boluses were
carefully offered to patients with a syringe. Videofluoro-
scopic signs of impaired safety and efficacy of deglutition
were identified accordingly to previously accepted definitions
[7]. Impaired safety signs were laryngeal vestibule penetra-
tions and tracheobronchial aspirations, classified according to
the PAS, assessed in each deglutition. Unsafe swallow was
considered when the PAS score was higher than 2 (PAS
categories: 1–2 safe swallow; 3–5 penetrations; 6–8 aspira-
tions) [24, 35]. VFS measurements were considered to be the
main outcome variables of the study.
VFS signs of impaired efficacy and safety of swallow
were measured as the ratio between the number of patients
presenting signs divided by the total number of patients per
group. Prevalence of patients presenting a VFS signs of
impaired efficacy and safety of swallow at each specific
bolus volume and viscosity was divided by the number of
patients that performed that bolus type.
Oropharyngeal swallow response OSR was measured
with the 5 mL nectar bolus because all patients performed
this swallow. OSR measurements have been described
previously by our group [7]. To describe the biomechanics
of OSR, we used the time to LVC, to upper esophageal
sphincter opening (UESO), final kinetic energy (KE) of the
bolus, bolus propulsion force, and mean bolus velocity. In
addition, we quantitatively determined the hyoid motion
(vertical and anterior movement) in an X–Y coordinate
system using specialized software (Swallowing Observer;
Image & Physiology SL, Barcelona, Spain) [42].
Response to the Treatment
After the two-week treatment, patients were divided into
responders (R) and nonresponders (NR) to identify which
factors make patients respond better to each treatment.
Responders were defined as those patients who, after
treatment, achieved safe swallow at a lower level of
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viscosity or, at the same viscosity level, improved at least
one point in the PAS [35].
Safety of the Treatment
During the study, any adverse events (AE) or serious
adverse events (SAE) were recorded and reported to the
Ethics Committee of the Hospital de Mataró and assessed
for relationship to the study procedures with the Karch–
Lasagna algorithm [43].
Experimental Design
A prospective randomized clinical trial was designed to
evaluate and compare, with VFS, the effect on signs of
impaired efficacy and safety of swallow as well as OSR of
two treatments based on sensory stimulation during
2 weeks in older patients with OD (Supplementary Fig. 1).
These treatments have been previously studied separately
by our group [24, 26]. During the pretreatment visit, we
collected the following data: sociodemographic character-
istics of the population, functional capacity according to
the Barthel Index [36], frailty status according to the L.
Fried criteria [37], comorbidities with the Charlson
Comorbidity Index [38], and nutritional status according to
the short form of the Mini Nutritional Assessment (MNA-
sf) [39]. Clinical symptoms of OD were measured using the
Spanish version of the EAT-10 [40, 41]. In addition, the
volume-viscosity swallowing test (V-VST) was used as a
clinical tool to screen patients for clinical signs of impaired
safety of swallow [20]. If the clinical evaluation revealed a
sign of impaired safety of swallow, then a VFS was per-
formed in order to confirm the previous clinical findings.
Patients with a score higher than 2 on the penetration–
aspiration scale (PAS) [35] were included in the study and
randomized into one of the two treatment arms using a
specialized software (GraphPad QuickCalcs 2012):
(a) TRPV1 agonist 10 treatment days of chemical sensory
stimulation with a natural TRPV1 agonist solution (natural
capsaicinoids 1 9 10-5 M). Capsaicin solution was
obtained from an alimentary capsaicinoid sauce (McIl-
henny Co, Avery Island, Louisiana, USA) containing
185.5 lg/g of capsaicinoid. This concentration was previ-
ously determined using liquid chromatography (AOAC
995.03 method) [24]. Final concentration was obtained by
dissolution of the capsaicinoid sauce in 10 mL tomato juice
to obtain a nectar-like solution. Treatment was taken by
patients three times per day before each meal and five days
per week (Monday to Friday) for 2 weeks. The study
product was prepared once a week, collected by patients
every Monday, and preserved refrigerated (4 C). (b) TSES
10 treatment days of electrical stimulation using the thy-
rohyoid position and applying an intensity of 75 % of the
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motor threshold previously determined [34]. Treatment
consisted of the application, at rest, of 80 Hz of transcu-
taneous electrical stimulus (biphasic, 700 ls) using the
Intelect VitalStim device (Chattanooga Group, Hixson,
TN, USA). Patients with e-stim came to the hospital to
perform the therapy 1 h per day, 5 days a week (Monday to
Friday) for 2 weeks [34] (Supplementary Fig. 1).
Statistical Analysis
Qualitative data are presented as relative and absolute
frequencies and analyzed by the Fisher’s exact test (sex,
VFS signs of impaired efficacy and safety of swallow) or
the Chi-square test (Fried criteria and MNA-sf categories,
dysphagia cause, PAS scores categories). Continuous data
are presented as mean ± standard deviation (SD) and
compared with the T-test (intergroup comparisons) or
Paired T-test (intragroup comparisons); for those variables
that did not follow a normal distribution, we used the
nonparametric Mann–Whitney U-test (intergroup compar-
isons) or the Wilcoxon-paired test (intragroup compar-
isons). To assess normality, we used the D’Agostino and
Pearson omnibus normality test. Results were interpreted
according to the obtained P value, the magnitude of the
observed effect, and their clinical and biological plausi-
bility. Statistical significance was accepted if P values were
less than 0.05. Statistical analysis was performed using
GRAPHPAD PRISM 6 (San Diego, CA, USA).
Results
Patient Demographics
Both groups of patients with OD showed similar demo-
graphic, phenotypic, and clinical characteristics: mean age
was 80.5 ± 5.2 years, and patients presented high number of
comorbidities (Charlson = 3.1 ± 1.59), mildly impaired
functional status (Barthel = 86.8 ± 17.8), polymedication
(8.9 ± 3.3 drugs/patient), and the majority of them belonged
to the prefrail phenotype according to the L. Fried Frailty
Classification [37]. In addition, 63.16 % were well-nour-
ished according to the MNA-sf. The causes of OD in the
whole population were the aging process (39.5 %), or a
combination of aging with previous stroke (42.1 %), or
neurodegenerative diseases (15.8 %) (Table 1).
Baseline Assessment of OD
Clinical Symptoms and Signs of OD
Both groups of older patients presented similar results on
the EAT-10 score ([8 points), showing a population at
O. Ortega et al.: A Comparative Study Between Two Sensory Stimulation Strategies After…

Table 1 Health status

G. A TRPV1 G. B TSES P value

n 19 19
Age 81.2 ± 5.6 79.8 ± 4.84 0.409
Sex ($) 57.9 % (11) 52.6 % (10) 1
Charlson 2.94 ± 1.6 3.26 ± 1.6 0.851
0 5.26 (1) 10.53 (2) 0.747
1–2 31.58 (6) 15.79 (3)
3–4 52.63 (10) 57.89 (11)
C5 10.53 (2) 15.79 (3)
Barthel 86.05 ± 13.9 87.10 ± 21.6 0.560
Optimum (100) (%) 36.84 (7) 47.37 (9) 0.743
Suboptimum (\100) (%) 63.16 (12) 52.63 (10)
Fried 1.53 ± 1.12 1.63 ± 1.21 0.782
Robust (%) 21.1 (4) 21.1 (4) 0.711
Prefrail (%) 63.16 (12) 52.63 (10)
Frail (%) 15.8 (3) 26.32 (5)
MNA-sf 11.74 ± 2.1 11.84 ± 2.36 0.446
Well-nourished (%) 63.16 (12) 63.16 (12) 0.808
At risk (%) 31.57 (6) 26.32 (5)
Malnourished (%) 5.26 (1) 10.53 (2)
2
BMI (kg/m ) 27.28 ± 3.9 26.07 ± 3.2 0.307
Dysphagia causea
Elderly (%) 42.1 (8) 36.8 (7) 0.980785
Stroke (%) 42.1 (8) 42.1 (8)
NDD (%) 15.8 (3) 15.8 (3)
Medication 9.42 ± 3.7 8.42 ± 2.9 0.358
Demographical, clinical, and nutritional data of the population P value corresponds to the comparison between GA and GB
MNA-sf mini nutritional assessment-short form, BMI body mass index, NDD neurodegenerative disease, RX-CH therapy radio or chemotherapy,
TRPV1 transient receptor potential vanilloid 1, TSES transcutaneous sensory electrical stimulation
a
Dysphagia cause from 1/19 patients from group B was radiotherapy (not shown in table)

high risk of OD. The V-VST further confirmed these OSR

results showing that both groups presented similar high
prevalence of clinical signs of impaired efficacy (Group A:
78.95 %, Group B: 89.47 %; P = 0.659) and safety of
swallow (Group A: 68.42 %; Group B: 84.21 %;
P = 0.447).
VFS Signs of OD
Table 2 also shows the results of the impaired physiology
of the swallow response of the study population at base-
line. Both groups presented severe and similar delays in
timing of LVC and UESO, and similar severe impair-
ments in bolus KE, and reduced tongue thrust and bolus
velocity.

VFS results showed that all patients from both groups
presented VFS signs of impaired safety with a prevalence
of aspirations of 21–26 % and that of silent aspirations of
15.8 %. In addition, both groups had similar maximum
PAS scores (Table 2). During baseline VFS, increasing
bolus viscosity not only improved patients’ safety of
swallow but also increased residue. Pudding viscosity
significantly achieved the highest safety among the three
tested viscosities in both groups of patients (Fig. 2).
Hyoid Movement
We have also found that both groups of patients presented
impairments in time and extent of baseline hyoid move-
ment. However, patients from Group B (TSES) had even
shorter baseline maximal vertical hyoid extension
(P = 0.032) and maximal anterior extension (P = 0.062)
compared to patients from Group A (TRPV1 agonist)
(Table 2).

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Table 2 Effect of the treatment

G. A TRPV1 P value G. B TSES P value
VFS 1 VFS 2 VFS 1 VFS 2

n 19 19 19 19
Clinical questionnaire
EAT-10 8.78 ± 8.8 6.11 ± 7.19 0.016 10.94 ± 9.71 8.47 ± 9.99 0.075
VFS
Impaired efficacy (OR ? PR) (%) 100 (19) 94.71(18) 1 84.21 (16) 100 (19) 0.603
Oral residue (%) 89.5 (17) 89.5 (17) 1 78.9 (15) 89.5 (17) 0.659
Pharyngeal residue (%) 78.9 (15) 78.9 (15) 1 63.2 (9) 56.2 (10) 1
Impaired safety (%) 100 (19) 68.48 (13) 0.019 100 (19) 68.42 (13) 0.019
Penetrations (%) 73.68 (14) 57.89 (11) 0.495 78.95 (15) 42.11 (8) 0.044
Aspirations (%) 26.32 (5) 10.53 (2) 0.404 21.05 (4) 26.32 (5) 1
Silent aspirations (PAS = 8) (%) 15.8 (3) 5.26 (1) 0.603 15.8 (3) 21.05 (4) 1
Higher PAS 4.84 ± 1.77 3.73 ± 1.88 0.075 5 ± 1.53 4.26 ± 2.43 0.151
OSR
LVC (ms) 395.8 ± 113.1 389.5 ± 94.13 0.856 440 ± 134 381.1 ± 182.2 0.158
UESO (ms) 294.7 ± 101.7 308.4 ± 114.6 0.780 328.42 ± 100.3 328.42 ± 154.4 0.670
KE (mJ) 0.62 ± 0.51 0.86 ± 0.89 0.463 0.61 ± 0.45 0.62 ± 0.41 0.978
Force (mJ) 9.32 ± 6.94 12.91 ± 13.11 0.433 9.38 ± 6.25 10.1 ± 6.19 0.618
Mean Bolus velocity (m/s) 0.22 ± 0.12 0.24 ± 0.12 0.389 0.21 ± 0.1 0.22 ± 0.1 0.717
Hyoid movement (n = 14/group)
Maximal vertical extension (mm) 26.82 ± 5.58 22.80 ± 10.71 0.345 20.3 ± 8.31 18.97 ± 9.72 0.303
Maximal anterior extension (mm) 41.9 ± 6.13 38.92 ± 12.51 0.989 37.24 ± 5.37 37.59 ± 5.06 0.765
Maximal vertical extension time (s) 0.53 ± 0.27 0.57 ± 0.26 0.909 0.45 ± 0.17 0.41 ± 0.17 0.294
Maximal anterior extension time (s) 0.5 ± 0.23 0.69 ± 0.28 0.058 0.54 ± 0.23 0.51 ± 0.21 0.619
Bold values are considered statistically significant (P value \ 0.05)
Underlined values are close to statistical significance (P value between 0.05–0.075)
Clinical and instrumental evaluation of oropharyngeal dysphagia. P value corresponds to the comparison between VFS 1 and VFS 2
EAT-10 eating assessment tool, V-VST volume-viscosity swallowing test, OR oral residue, PR pharyngeal residue, PAS Penetration–aspiration
scale, OSR oropharyngeal swallow response, LVC laryngeal vestibule closure, UESO upper esophageal sphincter opening, KE kinetic energy,
TRPV1 transient receptor potential vanilloid 1, and TSES transcutaneous sensory electrical stimulation

Posttreatment Assessment of OD B: 5 ± 1.52 vs. 4.26 ± 2.43; P = 0.151). Nevertheless,

Clinical Symptoms of OD
Treatment with TRPV1 agonists induced a significant
reduction of more than two points in the EAT-10 score,
whereas treatment with TSES did not reduce the EAT-10
score significantly (Table 2).
VFS Signs of OD
Prevalence of VFS signs of impaired safety of swallow were
significantly and similarly reduced in both treatment groups
(100–68.42 %; P = 0.019, Table 2). In addition, severity of
OD measured with the PAS score was also reduced in both
treatment groups without reaching statistical significance
(Group A: 4.84 ± 1.77 vs. 3.73 ± 1.88; P = 0.075. Group
statistical significance was observed when we analyzed
distribution of patients from both treatment groups according
to PAS scores categories between VFS1 and VFS2 (Fig. 3).
OSR
No differences were found regarding OSR parameters
(LVC, UESO, KE, force, and mean bolus velocity)
between baseline and posttreatment in both groups
(Table 2).
Hyoid Movement
Posttreatment hyoid maximal vertical and anterior exten-
sion and time was very similar to baseline and not affected
by the treatment (Table 2).

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Fig. 2 Baseline VFS signs of

OD. Impaired efficacy was
determined by the presence of
oral and/or pharyngeal residue.
Impaired safety of swallow was
expressed as percentage of
patients who presented
penetration and/or aspirations
during VFS. *P \ 0.05;
**P \ 0.01; ***P \ 0.001;
****P \ 0.0001 vs. thin liquid.
TRPV1 transient receptor
potential vanilloid 1, TSES
transcutaneous sensory
electrical stimulation

Fig. 3 Baseline and

Posttreatment Penetration–
Aspiration Scale Score.
Distribution of patients at each
level of the PAS during the first
VFS. 1–2 safe swallow; 3–5
penetrations; 6–8 aspirations (8:
silent aspirations). *P \ 0.05
(PAS scores categories between
baseline and posttreatment).
TRPV1 transient receptor
potential vanilloid 1, TSES
transcutaneous sensory
electrical stimulation

Therapeutic Effect of the Treatment
Response to the Treatment
According to our previous definition, we found a response
rate of 68.42 % (13/19) in the capsaicin group
(1 9 10-5 M) and 42.1 % (8/19) in the TSES group.
Responder Phenotype
No significant differences were found between responders
and nonresponders from both groups regarding the ana-
lyzed demographical and clinical characteristics (sex, age,
comorbidities, functional status, frailty, nutritional status,
OD etiology, medication, and OD status). We only found a
slight difference between functional status of patients from
Group A (TRPV1) (83.1 ± 14.8 vs. 94.2 ± 6.65;
P = 0.09).
VFS Signs of OD in Responders
We observed a reduction in the prevalence of impaired
safety of swallow in both groups of responders (Group A:
100 vs. 53.81 %, P = 0.014; Group B: 100 vs. 25 %,
P = 0.007). Furthermore, prevalence of aspirations was
also significantly reduced in Group A (38.46 vs. 0 %,
P = 0.039) and the prevalence of penetrations in Group B
(87.5 vs. 25 %, P = 0.040). Severity of OD according to
the PAS score was significantly reduced in both groups of
responders (Group A: 5.23 ± 2.04 vs. 3 ± 1.47,
P = 0.002; Group B: 4.63 ± 1.41 vs. 2.13 ± 0.64,
P = 0.007) (Fig. 4).

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Fig. 4 Effect of the treatment in responder patients. PAS penetra-
tion–aspiration scale, LVC laryngeal vestibule closure, VFS videoflu-
oroscopy, TRPV1 transient receptor potential vanilloid 1, TSES
Oropharyngeal Swallow Response in Responders
Regarding OSR, we did not find significant differences in
UESO time, KE, propulsion force, or mean bolus velocity.
However, LVC time significantly improved in responder
patients from Group B (TSES) (480 ± 167 ms vs.
295 ± 189.9, P = 0.02) (Fig. 4).
Hyoid Movement
Hyoid movement was not affected by either treatment.
Safety of the Treatment
During the study, we had five serious adverse events
(SAEs), two in the capsaicin group, and three in TSES
group, involving hospitalization for various reasons such as
respiratory infection, pneumonia, and stroke, and all
patients recovered. None of the SAE’s was related to the
study treatments. We concluded that our treatments were
safe for our older patients with OD.
Discussion
In this proof of concept study, we found that 10 days
treatment with sensory stimulation strategies reduced the
prevalence of VFS signs of impaired safety of swallow in
older patients with OD. Furthermore, capsaicin
1 9 10-5 M and TSES were effective in 68.42 and 42.1 %
123
transcutaneous sensory electrical stimulation. *P \ 0.05; **P \ 0.01;
***P \ 0.001 (VFS1 vs. VFS2)
of patients, respectively, significantly improving impaired
safety of swallow according to PAS. In addition, both
treatments were found to be safe according to our results as
no AE/SAE presented by patients was related to the study
treatments. Our results suggest that chronic sensory stim-
ulation might promote the recovery of swallow function in
a significant subgroup of older patients with OD, even
though we were not able to identify any phenotypic char-
acteristic linked to the response to treatment.
As far as we know, this is the first study to compare the
effect of two chronic sensory treatments to improve swal-
lowing physiology in older patients with OD. Conventional
treatment, based on compensation, is not able to improve
patient’s swallow physiology and so patients are con-
demned to use thickeners, postures, and/or manoeuvers
[21]. This compensatory effect was significantly confirmed
in our study, as it has been in previous ones
[19, 20, 44, 45], as our population, who presented impaired
safety when swallowing thin liquid, avoided 100 and
89.47 % of unsafe swallows in groups TRPV1 and TSES,
respectively, when using pudding viscosity.
Our study population was old, had a high number of
comorbidities, mildly impaired functionality, took a large
number of drugs and most had an appropriate nutritional
status. In addition, 78.9 % of them were prefrail or frail
according to L. Fried criteria. Swallowing function was
strongly impaired in both groups of patients as all of them
had impaired safety of swallow, with 15.8 % presenting
silent aspirations, and with a high prevalence of impaired
efficacy of swallow with oropharyngeal residue (100 and
O. Ortega et al.: A Comparative Study Between Two Sensory Stimulation Strategies After…
84.21 % in TRPV1 and TSES, respectively). OSR was also
severely impaired in both groups of patients with a delayed
LVC and weak bolus propulsion forces leading to a slow
mean bolus velocity and delayed hyoid elevation and
movement. This is a very similar result to a previous study
with frail older patients with OD that we performed,
indicating a population at high risk of nutritional and res-
piratory complications [7]. Baseline maximal vertical and
anterior hyoid extension was low in our population as in
that one [7], indicating low elevation of the larynx and
therefore reduced airway protection. In addition, maximal
vertical extension time was delayed. The delay in hyoid
elevation and movement is a strong predictor of aspiration
as it contributes to delayed LVC [45]. Hence, these patients
are at high risk of suffering from respiratory infections and
aspiration pneumonia.
After the treatment and second VFS, we achieved a
significant reduction in the VFS signs of impaired safety of
swallow in both treatment groups. However, this reduction
in the VFS signs of impaired safety of swallow was not
accompanied by a significant improvement of the OSR.
Even so, the severity of impaired safety alterations (PAS)
was diminished (Table 2). After the analysis, patients were
divided according to their response to therapy based on
physiological (PAS improvement) and/or clinical
improvements (viscosity improvement). One of the main
reasons to split both groups according to response to the
treatment was to find out which clinical characteristics
made a difference to whether a patient responded or not.
This is very important in order to be able to select the best
therapy for each phenotype of older patient with OD.
Unfortunately, in our study, we did not find conclusive
differences between phenotypes of responders and nonre-
sponders; we only found a slight difference between
functional status of patients from Group A (TRPV1)
between responders and nonresponders (83.1 ± 14.8 vs.
94.2 ± 6.65; P = 0.09). This might be due to the fact that
the response to the treatment is related to different
parameters than the ones that we analyzed (such as dif-
ferences in cortical capacity to respond to a stimulus) or to
the small sample size. Further studies including a larger
sample size and analyzing neurophysiological parameters
are needed in order to determine and define the responder
phenotype for each of the tested treatments.
Our treatments aimed to stimulate the main afferent/
sensory deglutition pathways (maxillary branch of the
trigeminal nerve, the glossopharyngeal nerve, and the
superior laryngeal nerve) that project to the supra-medul-
lary structures and to the nucleus tractus solitarius in the
brainstem [46] to promote cortical plasticity and improve
OSR. It has been reported that 10 days treatment with
motor transcutaneous electrical stimulation on poststroke
patients with OD improved the efficacy and safety of
swallow and OSR while transcutaneous electrical stimu-
lation at sensory level (using the same parameters as our
study), improved only the safety of swallow and OSR [34].
In that earlier study, patients responded better to sensory
stimulation than in our present study. This might be due to
the brains of poststroke patients having greater neuroplas-
ticity and being able to reorganize themselves to move
functions to undamaged areas and thus respond better to
the different treatments than the brains of a mixed popu-
lation of older patients.
An earlier study also evaluated the effect of chronic
treatment with TRPV1 agonists (10-6 M) on older patients
and reported a significant improvement in the latency of
swallow clinically evaluated, after one month supplemen-
tation with oral capsaicin before every meal [26]. However,
the improvements were not verified with instrumental
assessment such as videofluoroscopy or fiberoptic
endoscopy.
Over the whole sample, even when patients were divi-
ded according to response to treatment, no improvement in
efficacy of swallow was found in any group of patients.
That finding is logical as impaired efficacy is mainly
related to low bolus propulsion force and impaired pha-
ryngeal clearance caused by muscular weakness of the
tongue and pharyngeal muscles, due mainly to age-related
sarcopenia [6, 9]. However, our therapeutic approach was
not directed to improving muscle function like motor
rehabilitation, but primarily focused on promoting cortical
plasticity to improve swallow safety.
The effect of the treatment was shown to last for at least
5 days after the last treatment session as the second VFS
was performed in that period of time. However, further
studies are also needed to measure the duration of the
treatment over longer periods of time and to adjust treat-
ment session frequency if needed.
The main limitation of the study, although it was a
proof of concept, was the small sample size, the vari-
ability of cause of dysphagia between patients and the
absence of a control group to discard placebo effect.
Large-controlled randomized clinical trials should be
performed to assess the effect of these two therapeutic
approaches on older patients with OD and to assess the
duration of the effect of the treatment. Furthermore, it
would be interesting to use neurophysiologic techniques
in order to know the mechanism of action of these
treatments on our target population and the potential role
of cortical plasticity.
In the statistical analysis of our results, we did not
correct the level of significance with a Bonferroni adjust-
ment. While this might have resulted in an overestimation
of our results, we believe each comparison in our study was
independent from the others so the probability of a Type 1
error was also independent in each comparison. For this
123
 O. Ortega et al.: A Comparative Study Between Two Sensory Stimulation Strategies After…
reason, the results obtained in our study must be interpreted
according to the probability of a Type 1 error (P value).
In conclusion, both sensory stimulation treatments
induced objective improvements in the prevalence of VFS
signs of impaired safety of swallow in older patients with
OD. In addition, the treatments are easy to learn and to use,
with no safety concerns. These novel therapeutic strategies
open a new treatment paradigm for geriatric patients
affected with OD as they have the potential to improve
swallowing physiology rather than compensating it.
Acknowledgments We would like to thank Mrs. Jane Lewis and
Ailish Maher for reviewing the manuscript and to Mrs. Natàlia
Vilardell for her help during the study.
Funding This work has been supported by Fundació Agrupació
Mútua, Barcelona; and Ciberehd, Instituto de Salud Carlos III, Bar-
celona, Spain.
Compliance with Ethical Standards
Conflict of Interest We declare no conflicts of interest.
Ethical Approval All participants were informed about the study
and signed the informed consent form. Study was approved by the
Ethics Committee of the Hospital de Mataró (CEIC 04/12).
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Omar Ortega PhD
Laia Rofes PhD
Alberto Martin MSc
Viridiana Arreola MSc
Irene López MSc
Pere Clavé MD, PhD
123