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Usefulness of Ice Massage in Triggering the Swallow Reflex

Tomoyuki Nakamura, MD,* and Ichiro Fujishima, MD

In Japan, ice massage is widely used as the prefeeding technique to facilitate dry
swallowing, to improve swallowing apraxia for initiating the swallowing action,
and in daily swallowing training. In a crossover study, we evaluated the usefulness
of ice massage for eliciting the swallowing response. The subjects were 24 dysphagic
patients with stroke and cerebrovascular disease. We measured the latency between
the command of dry swallowing and the triggering of the swallow reflex by videofluoroscopic examination of swallowing, with and without ice massage. When a subject could not swallow all the 4 trials we recorded whether he or she could swallow
or not. And we counted how many times he or she could swallow with and without
ice massage. Our results suggest that ice massage significantly shortened the latency
to triggering of the swallow reflex and often initiated swallowing even in those subjects who could not swallow without the massage. These results demonstrate that ice
massage has an immediate effect on triggering of the swallow reflex. The effect of ice
massage was especially remarkable in the 15 subjects who had supranuclear lesions
compared with the subjects with nuclear lesions. Thus, ice massage could activate
the damaged supranuclear tract and/or the normal nucleus and subnuclear tract
for swallowing. Ice massage has proven useful in many clinical dysphagia training
sessions. Key Words: Ice massagetriggering the swallow reflex.
2013 by National Stroke Association

Stroke and cerebrovascular diseases are known to cause


dysphagia. The swallow reflex is a basic reflex, and a loss
or delay in triggering of the swallow response causes
aspiration and retention of food in the pharyngeal stage.
Several therapeutic procedures that trigger the swallow
reflex have been investigated. Pommerenke1 identified
the anterior faucial pillars as one of the sensitive oral
areas for initiation of the swallow reflex. The stimulation
of the anterior faucial pillars succeeded in a reduced

From the *Department of Rehabilitation, Seirei Mikatahara General


Hospital, Shizuoka, Japan; Graduate School of Neurosurgery, Tokyo
Medical and Dental University, Tokyo, Japan; and Hamamatsu City
Rehabilitation Hospital, Hamamatsu, Japan.
Received August 14, 2011; revision received September 20, 2011;
accepted September 27, 2011.
Address correspondence to Tomoyuki Nakamura, MD, Department of Rehabilitation, Seirei Mikatahara General Hospital, 3453
Mikatahara-cho, Kita-ku, Hamamatsu, Shizuoka 433-8558, Japan.
E-mail: ntomoyuki@sis.seirei.or.jp.
1052-3057/$ - see front matter
2013 by National Stroke Association
doi:10.1016/j.jstrokecerebrovasdis.2011.09.016

378

delay in initiation of the swallowing response, primarily


in the pharyngeal phase. Kojima et al2 reported on Kpoint stimulation for pseudobulbar palsy. The physiological mechanism behind K-point stimulation is not clear,
but this technique is widely applied to treat patients
with pseudobulbar palsy in Japan.
Ice massage with an ice stick applied to the throat, base
of the anterior faucial arches, base of the tongue, and
posterior pharyngeal wall is widely used in Japan as a prefeeding technique to induce dry swallowing, to stimulate
swallowing apraxia for initiating the swallow action, and
in daily swallowing training. Although ice massage and
its effects are widely recognized in Japan, this technique
has never been studied in controlled conditions. Anecdotal data suggest that ice massage shortens the latent
period of triggering of the swallow reflex and helps elicit
the swallowing response even in those patients who cannot initiate the swallow reflex voluntarily. In the present
study, we evaluated the usefulness of ice massage in
eliciting the swallow response in 24 dysphagic patients
with stroke and cerebrovascular disease and examined
the utility of this technique in the Japanese clinical setting.

Journal of Stroke and Cerebrovascular Diseases, Vol. 22, No. 4 (May), 2013: pp 378-382

UTILITY OF ICE MASSAGE ON SWALLOW REFLEX

379

Table 1. Delay in the swallow reflex based on the VFES


guideline of the Japanese Society of Dysphagia
Rehabilitation
Rank
3, no delay
2, mild delay
1, severe delay

Time of initiation of swallow reflex


Swallowing occurs before or at the
time food reaches the piriform fossa
Swallowing within 3 seconds after
food reaches the piriform fossa
Swallowing occurs more than
3 seconds after food reaches the
piriform fossa
Figure 1. The ice stick consists of a 4-inch-long, 0.5-inch-diameter wooden
stick with a frozen water-impregnated cotton tip.

Subjects and Methods


The study subjects were 24 dysphagic patients with
stroke and cerebrovascular disease, all of whom were
enrolled between October and November 2010. Before
the study, the 3-mL water-swallowing test3 was performed
to screen the subjects and videofluoroscopic examination
of swallowing (VFES) was used to identify dysphagia in
the pharyngeal stage. The delay in initiation of the swallow
reflex was estimated based on the guideline for VFES of the
Japanese Society of Dysphagia Rehabilitation4 (Table 1).
We excluded subjects who could not cooperate with the
procedure and those with severely altered consciousness,
but included those with mildly altered consciousness
(Glasgow Coma Scale E4 V4-5 M6) and those who could
follow commands. We obtained written consent from all
subjects or families, and performed all tests in accordance
with prescribed ethical standards.
We performed ice massage using a 4-inch-long, 0.5-inchdiameter frozen water-impregnated cotton-tipped stick
(ice stick; Fig 1). Each patient received an ice massage for
10 seconds with rubbing and light compression to the
posterior tongue and tongue base, velum, and posterior
pharyngeal wall.
We measured the latency between the command to dry
swallow and the triggering of the swallow reflex, and
recorded the results of all trials on VFES. Rapid elevation
of the thyroid cartilage was considered to indicate triggering of the swallow reflex. We measured the latency when
the larynx was in the highest position. To avoid excessive
radiation exposure, if a subject could not swallow for
10 seconds, the video recording was stopped and the subject was deemed to not demonstrate a swallow response.
We evaluated the latency with ice massage followed by
the dry swallowing command (A) and with the dry swallowing command without ice massage (B). For each subject, we measured latency 4 times under 2 conditions:
A-B-A-B and B-A-B-A. The interval between conditions
was more than 10 seconds, to prevent any influence of
the effect of the preceding condition. Each subject was
randomly assigned 1 of the 2 conditions. When a subject
could not swallow all the 4 times, we recorded whether

he or she could swallow within 10 seconds or not. And


we counted how many times he or she could swallow
with and without ice massage. We reviewed all of the
data compiled by 2 researchers and checked that each
measurement was the same. We analyzed the significance
of latency with or without ice massage using the paired
t test and the significance of the number of swallowing responses with or without ice massage using the Wilcoxon
rank sum test, with the significance level set at P 5 .05.

Results
A total of 24 subjects (19 men and 5 women; mean age,
71.5 6 10.3 years) were recruited into this study and examined. The cause of dysphagia was cerebral infarction (CI)
involving the lateral medulla in 9 subjects, CI without lateral medulla involvement in 10 subjects, intracerebral
hemorrhage (ICH) in 3 subjects, and subarachnoid hemorrhage (SAH) in 2 subjects. Fifteen subjects had 1 supranuclear lesion, 13 had a mildly delayed swallow reflex, and
4 demonstrated severely delayed swallowing (Table 2).
Fourteen subjects were able to initiate the swallowing
response in all 4 trials (Tables 3 and 4). In this group, the
average latency after ice massage was 1.55 6 0.42
seconds, significantly shorter than the latency without ice
massage (2.17 6 1.53 seconds; t 5 2.16; P 5 .00366). In 10
subjects, swallowing could not be triggered in all trials
Table 2. Baseline characteristics of the study subjects
Characteristic

Value

Number of subjects
Age, years, mean 6 SD
Sex, male/female, n
Delay in swallowing reflex in VFES,
no/mild/severe, n
Diagnosis, n (%)
CI with lateral medulla
CI without lateral medulla
ICH
SAH
Lesions, supranuclear/nuclear, n

24
71.5 6 10.3
19/5
7/13/4

9 (37.5)
10 (41.7)
3 (12.5)
2 (8.33)
15/9

T. NAKAMURA AND I. FUJISHIMA

380

Table 3. Characteristics and latencies with ice massage (A) and without ice massage (B) in subjects who could initiate the swallow
reflex in all 4 trials
Age, years

Sex

Diagnosis

Lesion

Pattern

A, seconds

B, seconds

85
61
84
36
68
73
83
68
75
83
84
73
75
51

F
M
F
M
M
M
M
M
M
M
M
M
F
M

CI
SAH
CI
SAH
CI
CI
CI
CI
CI
CI
CI
CI
CI
CI

Left basal ganglia


Left cerebral hemisphere
Right pons
Bilateral cerebral hemisphere
Right lateral medulla
Left lateral medulla
Bilateral cerebellar hemisphere
Left pons
Bilateral cerebellar hemisphere
Bilateral cerebellar hemisphere
Bilateral basal ganglia
Left lateral medulla
Right pons and lateral medulla
Right cerebral hemisphere

ABAB
ABAB
ABAB
ABAB
ABAB
ABAB
ABAB
ABAB
ABAB
BABA
BABA
BABA
BABA
BABA

1.61
0.96
2.64
2.29
0.78
1.22
1.18
1.47
1.83
2.39
1.90
1.82
1.34
0.30

4.64
1.55
2.43
4.56
1.01
1.24
2.66
2.48
1.71
2.59
2.06
2.17
0.91
0.43

(Tables 5 and 6). A significantly higher average number of


swallow responses were triggered after ice massage than
without ice massage (1.30 6 0.70 vs 0.50 6 0.50; P 5 .0267).
In particular, the 15 subjects with supranuclear lesion
demonstrated a remarkable swallowing tendency, and
10 subjects were able to initiate the swallowing response
in all 4 trials (Tables 3 and 4). The average latency was
significantly shorter after ice massage than without ice
massage (1.66 6 0.509 seconds vs 2.51 6 1.65 seconds;
t 5 2.26; P 5 .00354). In 5 subjects, swallowing could not
be triggered in all trials (Tables 5 and 6). The average
number of swallow responses triggered was higher with
ice massage than without ice massage (1.40 6 0.72 vs
0.20 6 0.32; P 5 .0413). In the 9 subjects with nuclear
lesions, no significant findings were noted; 4 of these
subjects were able to initiate the swallowing response
in all 4 trials (Tables 3 and 4). The average latency was
slightly shorter after ice massage than without ice
massage (1.29 6 0.183 seconds vs 1.33 6 0.331 seconds;

t 5 3.18; P 5 .820). In 5 subjects, the swallowing


response could not be triggered in all trials (Tables 5 and
6). A slightly higher average number of swallow
responses could be triggered with ice massage than
without ice massage (1.20 6 0.64 vs 0.80 6 0.32; P 5 .343).

Discussion
In subjects who were able to initiate swallowing reflex
in all 4 trials, ice massage shortened the latency of triggering the swallowing reflex after the command, and the
massage had an immediate effect on triggering a swallow
response. In addition, the findings in subjects who could
not initiate the swallow reflex in any trial suggest that ice
massage may be useful for patients who cannot swallow
voluntarily. In Japan, ice massage is widely used not
only as a swallowing training technique and a prefeeding
technique, but also to promote swallowing in individuals
who tend to stop swallowing during meals. We attempted

Table 4. Characteristics and latencies with ice massage (A) and without ice massage (B) in subjects who could initiate the swallow
reflex in all 4 trials
Characteristic

Value

Number of subjects (%)


Age, years, mean 6 SD
Sex, male/female, n
Condition, ABAB/BABA, n
Lesion, supranuclear/nuclear, n

14 (58.3)
71.4 6 10.4
11/3
9/5
10/4
Latency, seconds, mean 6 SD

All
With supranuclear lesions
With nuclear lesions

With ice massage (A)

Without ice massage (B)

P value

1.55 6 0.420
1.66 6 0.509
1.29 6 0.183

2.17 6 1.53
2.51 6 1.65
1.33 6 0.331

.00366
.00354
.820

UTILITY OF ICE MASSAGE ON SWALLOW REFLEX

381

Table 5. Characteristics of the swallow reflex triggered with ice massage (A) and without ice massage (B) in subjects in whom the
swallow reflex was not triggered in every trial
Age, years

Sex

Diagnosis

Lesion

Pattern

A, times

B, times

59
63
73
88
79
82
79
80
45
69

M
M
M
M
M
F
M
M
M
F

CI
CI
CI
CI
ICH
CI
CI
CI
ICH
CI

Right lateral medulla


Left pons
Left lateral medulla
Left lateral medulla
Right putamen
Left lateral medulla
Right lateral medulla
Bilateral basal ganglia
Bilateral pons
Right thalamus

ABAB
ABAB
ABAB
BABA
BABA
BABA
BABA
BABA
BABA
BABA

2
2
2
1
1
0
1
2
0
2

1
0
0
1
0
1
1
1
0
0

to orally feed such subjects and provided swallowing


training for them for specified periods. The effect of ice
massage was more significant in subjects with supranuclear lesions than in those with nuclear lesions. Thus,
ice massage could activate a damaged supranuclear tract
of swallowing and/or a normal nucleus and subnuclear
tract.
The importance of the cerebrocortical and corticobulbar
tracts has been recognized recently. Martin et al5 identified cerebrocortical area that represents the function of
swallowing in humans with functional magnetic resonance imaging. Daniels et al6 proposed a role of the insular cortex in dysphagia. Power et al7 reported that
electrical faucial pillar stimulation alters corticobulbar excitability, suggesting that ice massage can activate the
supranuclear tract.
The aforementioned findings suggest that ice massage
can activate normal nucleus and subnuclear tract in the
following way. When the larynx and pharynx are stimulated, pharyngeal and laryngeal sensory receptors
transform the cool/warm, pain, tactile, and pressure sensations into signals to initiate the swallowing response.

The base of the tongue, posterior pharyngeal wall,


anterior faucial arches, epiglottis, and arytenoids appear
to be especially sensitive in the swallow reflex. The signals are transmitted through the superior laryngeal nerve
and the pharyngeal branch of the glossopharyngeal
nerve. The superior laryngeal nerve, a branch of the vagus
nerve, is the main laryngeal afferent peripheral nerve,8
and the pharyngeal branch of the glossopharyngeal nerve
is the main pharyngeal afferent peripheral nerve. The signals are transmitted to the nucleus of the solitary tract and
then to the swallow center in the medullary reticular formation.9 Ice massage provides cold, tactile, and pressure
sensations to the base of the tongue, posterior pharyngeal
wall, and anterior faucial arches, apparently resulting in
transmission of strong signals to the swallow center to
elicit the swallow reflex.
Increasing the sensory input is one ways to restore
swallowing. Air pulses, chemical transmitters, and other
methods have been used in attempts to improve swallowing.10,11 Thermomechanical facilitation also has been used
to effectively induce swallowing.12 Extending the work
of Pommerenke,1 Logemann13 studied tactile-thermal

Table 6. Characteristics of the swallow reflex triggered with ice massage (A) and without ice massage (B) in subjects in whom the
swallow reflex was not triggered in every trial
Characteristic

Value

Number of subjects (%)


Age in years, mean 6 SD
Sex, male/female
Condition, ABAB/BABA
Lesion, supranuclear/nuclear

10 (41.7)
71.7 6 10.2
8/2
3/7
5/5
Swallow time, seconds, mean 6 SD

All
With supranuclear lesions
With nuclear lesions

With ice massage (A)

Without ice massage (B)

P value

1.30 6 0.70
1.40 6 0.72
1.20 6 0.64

0.50 6 0.50
0.20 6 0.32
0.80 6 0.32

.0267
.0413
.343

T. NAKAMURA AND I. FUJISHIMA

382

application as a technique to stimulate the swallow reflex.


One of the earliest techniques developed for swallowing
training, this involves applying cold (thermal) contact to
the base of the anterior faucial arches using a laryngeal
mirror.
Lazzara et al14 reported that thermal sensitization
shortened the duration of oral and pharyngeal transit in
23 of 25 neurologically impaired patients, and concluded
that this technique enhanced the triggering of the swallow reflex. They hypothesized that touch and cold stimulation to the anterior faucial pillars increased oral
awareness and provided an alerting sensory stimulus to
the cortex and brainstem. Rosenbek et al15 showed that
thermal application decreased the duration of stage transition in the absence of any change in the occurrence of
aspiration or penetration in 7 male subjects. Thermal
application also reportedly reduced the duration of stage
transition and total swallow duration in 22 dysphagic
stroke survivors.16 Consequently, tactile-thermal application has been widely using in dysphagic patients as
a form of swallowing training, but its use is limited to
those who can voluntarily open the mouth and swallow.17
In the present study, the effect of ice massage was
similar to that of previously described methods. However, ice massage is more useful and effective than other
methods, for several reasons:
1. Ice massage is a very simple and cheap method.
Only a frozen water-impregated cotton-tipped stick
is used; no special and expensive instruments, such
as the cooled laryngeal mirror required in tactilethermal application and air pulses or chemical
transmitter, are required.
2. Ice massage is a very easy and safe method. Any
therapist can easily perform this technique on any
patient.
3. Ice massage is widely adaptable. It can be applied
regardless of whether swallowing is voluntary,
compared with tactile-thermal application, which
is followed by voluntary swallowing.
Acknowledgement: We thank M. Groher, PhD, and
G. Mann, PhD, for their helpful comments on the manuscript.

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