TITLE: The effect of olfactory stimuli on the balance ability of stroke
patients

  ABSTRACT:
[Purpose] The present study attempted to identify the effect of olfactory stimulation on
the balance ability of stroke patients. [Subjects] Thirty-three (33 males) stroke patients
participated in the study. The stroke patients were divided into three groups: a black
pepper oil (BPO) group (n=11), lavender oil (LVO) group (n=11), and distilled water (DW)
group (n=11). [Methods] Two sessions (control trial/stimulus trial) of Romberg's test
(eyes open 1 min/eyes closed 1 min) were conducted on a force platform to measure the data
for the COP (center of pressure). Olfactory stimulation was provided at as a stimulus.
[Results] With the eyes open, a statistically significant difference was found in average
anterior posterior displacement (Ymean) and average medial lateral displacement (Xmean)
among the three groups when comparing the groups before and after stimulation. The
comparison between the eyes open and eyes closed conditions in each group showed a
significant difference in the area of the 95% confidence ellipse (area) and Xmean of the
BPO group and in the area of the LVO group (area, Xmean). [Conclusion] The findings
indicate that the interaction of brain areas activated by the olfactory stimulation exerts
an influence on the balance ability of stroke patients.

BODY.INTRODUCTION:
A stroke is an acute onset of neurological dysfunction resulting from an abnormality of
cerebral circulation1) and is one of the
major causes of long-term disability2).
Stroke patients' sensory, motor, cognitive, and emotional disabilities impose restrictions
on their basic activities of daily living3). Disabilities in the form of reduced postural balance, postural
control, and functional movement are general problems of stroke patients4). Impairment of balance control is a main
problem in these patients, since it may greatly affect their mobility and independence and
often increases the risk of falls5, 6).  Balance deficits can be identified from observing increased postural sway in stroke
patients during quiet standing7, 8). Many studies on quiet standing in stroke patients have
utilized force platform technology to evaluate weight bearing and body sway; based on the
location and movement of the COP of the ground reaction force9). Analysis of the movement of the COP obtained from data collected
using a force platform is a general method to measure postural sway with quiet standing10).  Most of the research on quiet standing makes use of a kinetic measurement method in which
the anterior-posterior and medial-lateral displacements of the COP are calculated on a force
platform11). In general, evaluation of
balance ability of stroke patients depends on the following four indices: mean COP velocity
(velocity), area of the 95% confidence ellipse (area), average anterior-posterior
displacement (Ymean), and average medial-lateral displacement (Xmean)12,13,14,15).  An individual's postural control is a complex motor task that is controlled by hierarchical
neural systems including the spinal cord, brainstem, cerebellum, basal ganglia, and the
cerebral cortex16). Standing balance
control, in turn, is a complex sensorimotor action based on automated and reflexive spinal
programs under the influence of the brainstem, cerebellum, cortex, and several distinct and
separate supraspinal centers17). In order
to maintain postural control a series of processes are required that involve various
systems, including sensory information for visual sense, vestibular sense, proprioception,
cognitive integration, cerebellum function, and the sensory-motor feedback system18, 19).  It has been reported that odor provides a strong stimulation to a wide area of the cerebral
cortex20) and that olfactory stimulation
activates various regions of the brain as well as the orbitofrontal cortex21). Other research has suggested that the
cerebellum is involved in odor information processing22, 23). It has also been found
that patients with localized cerebellar atrophies and focal cerebellar lesions showed
olfactory impairment24). All these
findings may lead us to assume that olfactory stimulation is closely related to various
regions of the brain.  Some recent research has suggested that olfactory stimulation may increase the postural
stability of the elderly25). It has also
been reported that olfactory stimulation increased the gait ability of the elderly26) and that it decreased their risk of
falls27). Many studies have been carried
out to identify the relationship between olfactory stimulation and postural control, but not
much has been reported on stroke patients. This study attempted to identify the effect of
olfactory stimulation on the balance ability of stroke patients having balance problems.

BODY.SUBJECTS AND METHODS:
Table 1Table 1.Subject characteristicsBPOmean±SDLVOmean±SDDWmean±SDGender (male/female)11/011/011/0Age (years)58.7±15.162.6±10.757.5±10.1Height (cm)170.4±4.4169.8±5.3167.3±7.2Weight (kg)67.4±8.063.9±6.864.7±6.8Stroke type (number)Ischemic/hemorrhagic6/55/67/4Affected side (number)Left/Right8/310/18/3Time since stroke (month)25.4±12.422.4±16.130.4±16.5MMSE (score)28.2±2.227.55±2.725.73±2.2Brunnstrom (stage)4.36±0.84.00±0.84.18±0.8BPO, black pepper oil; LVO, lavender oil; DW, distilled water; MMSE, mini-mental shows the general physical characteristics of the group of chronic stroke
patients used as subjects, who met the following criteria: they were chronic stroke patients
who had hemiplegia from strokes for at least 6 months; had normal olfactory function
diagnosed with an olfactory identification test; scored greater than 24 points on the
mini-mental state examination (MMSE) test and showed no problem in communication, could walk
10 m by themselves did not have any disease in musculoskeletal, cardiovascular, or endocrine
system, who did not take any medicine that a could influence posture and balance passed the
third stage of the Brunnstrom recovery scale; and agreed to voluntarily participate in the
present research. Written informed consent has been obtained from each subject or patient.
The Ethics Committee of Namseoul University, South Korea, also approved the study. The IRB
approval number is Research-140421-3.  The 33 subjects were randomly assigned to one of three subgroups: the black pepper,
lavender, and distilled water. Black pepper, lavender oil (Absoulte aromas Ltd. Alton,
England), and distilled water were used as olfactory stimuli for the subjects. The
experiment was conducted for all three groups between 10 to 11 in the morning. Measurement
of COP values with quiet standing was carried out with a BT4 force platform (Hur Laps Oy,
Tampere, Finland). The participants did performed two sessions (control trial/stimulus
trial) of Romberg's test (eyes open 1 min/eyes closed 1 min) on the force platform (BT4, Hur
Laps Oy, Tampere, Finland).  First, a Romberg's test (for COP measurement) was conducted before olfactory stimuli for
one minute with the eyes open, and this was followed by two minutes of rest and then
performance of the test again for one minute with the eyes closed. After a four minute of
rest, the olfactory stimulus was given, and the COP was measured for one minute with the
eyes open; this was followed by two minutes of rest and then measurement of the COP again
for one minute with the eyes closed. The olfactory stimulus was given to the patients via an
aroma necklace that they did not wear during rest periods. The subjects sat in a chair
comfortably while resting25).  COP excursion was tested using a four-channel portable force platform (Hur Labs BT4) that
was calibrated prior to testing; the channels were checked before every test. The Patients
were instructed to look straight ahead and stand as still as possible with their arms
hanging down. The foot position was standardized: patients stood with a 2 cm heel-to-heel
distance and an angle of 30° between the feet. The test was carried out with the eyes opens,
focusing on a point 2 m ahead, and with the eyes closed. The participants stood still for at
least 5 s (pre-phase) before measurement. After the pre-phase, the COP was measured for the
next 60 seconds. Signals were sampled at 200 Hz and filtered with a digital low-pass filter
at a 7.8 Hz cutoff frequency prior to sampling; signals were filtered with two low-pass
filters, with the first-stage filter being a is sinc3 type and the second-stage filter being
a 22-tap filter.  In the current research, the area of the 95% confidence ellipse (area), average
anterior-posterior displacement (Ymean), and average medial-lateral displacement (Xmean)
were selected as the COP values.  SPSS Statistics 18.0 program for Windows was used in this research to carry out all
statistical analyses. The general characteristics of the subjects were analyzed with the
Kolmogorov-Smirnov test. Multivariate analysis of variance was to analyze variable effects
based on the three balance ability factors, area, Xmean, and Ymean, of the three groups. A
paired t-test was also conducted to compare presence and absence of sight: the eyes open and
eyes closed conditions. The level of significance was set at 0.05.

BODY.RESULTS:
The three groups showed changes in area, Xmean, and Ymean before and after olfactory
stimuli with the eyes open and eyes closed, as shown in Table 2Table 2.Differences among the three groups in area, Xmean and Ymean before and after
olfactory stimuli with eyes open and closedConditionVariableGroupPre mean±SDPost mean±SDEOArea (mm2)BPO521.3±397.6394.6±249.1LVO602.5±594.1500.2±401.2DW570.0±346.5458.8±290.1Xmean (mm)BPO*22.8±16.316.2±11.9LVO*21.0±14.814.3±11.5DW20.8±20.816.9±11.7Ymean (mm)BPO*−15.7±12.8−25.5±12.7LVO−17.7±15.9−21.1±15.9DW−14.4±14.7−17.3±17.8ECArea (mm2)BPO528.1±497.4563.3±364.7LVO580.4±510.3602.7±487.1DW758.1±635.9632.8±489.4Xmean (mm)BPO21.5±13.918.2±11.8LVO22.6±13.915.0±12.5DW21.3±21.817.8±15.0Ymean (mm)BPO−14.0±12.6−23.9±13.3LVO−18.3±14.8−19.1±15.9DW−9.3±25.7−15.0±19.7*Expressed as p<0.05. BPO, black pepper oil; LVO, lavender oil; DW, distilled
water; area, area of the 95% confidence ellipse; Ymean, average anterior-posterior
displacement; Xmean, average medial-lateral displacement; EO, eyes open; EC, eyes
closed. With the eyes open, a statistically significant difference was not found
(p<0.05) among the three groups in area, but significant differences were found in Xmean
and Ymean in comparisons of the values before and after olfactory stimulus. With the eyes
closed, on the other hand, no significant difference was found in area, Xmean, and Ymean
among the three groups (p>0.05).  There were also changes in area, Xmean, and Ymean within each group with the eyes open and
eyes closed (Table 3Table 3.Eyes open vs. eyes closed: differences in area, Xmean, and Ymean of each group
before and after olfactory stimulationGroupVariableEO mean±SDEC mean±SDBPOArea* (mm2)126.7±213.9−35.2±290.1Xmean* (mm)6.6±12.23.2±10.9Ymean (mm)9.8±11.09.9±8.3LVOArea* (mm2)602.5±594.1−102.5±170.0Xmean (mm)−1.6±13.3−0.6±5.4Ymean0.6±6.1−1.9±8.1DWArea (mm2)−188.1±463.8−173.9±270.2Xmean (mm)−0.5±18.4−0.9±6.6Ymean (mm)−5.0±15.1−2.2±8.0*Expressed as p<0.05. BPO, black pepper oil; LVO, lavender oil; DW, distilled
water; area, area of the 95% confidence ellipse; Ymean, average anterior-posterior
displacement; Xmean, average medial-lateral displacement; EO, eyes open; EC, eyes
closed). In the comparison of the eyes open and eyes open conditions for each group,
it was found that the area and Xmean of the BPO group and the area of the LVO group showed
significant differences (p<0.05). However, no significant difference was found in
comparison of the eyes open and eyes closed conditions in terms of the comparison in Ymean
of the BPO group, Xmean and Ymean of the LVO group and all three indices in the DW
group.

BODY.DISCUSSION:
The present research attempted to identify the impact of olfactory stimuli on the balance
ability of stroke patients. It was found that olfactory stimuli decreased the Xmean (BPO,
LVO) and Ymean (BPO) values with the eyes open.  Similar results were reported in previous research. Freeman S et al.25), for instance, found in their test of balance ability with
black pepper oil and lavender oil as olfactory stimuli that the COP values (RMS velocity and
trajectory length in the medial-lateral and anterior-posterior directions) decreased
significantly. Ebihara et al.26) also
reported that the TUG (Timed Up and Go) test score of the elderly significantly decreased
after being given olfactory stimuli of lavender oil and grapefruit oil. Sakamoto et al.27) also found an interesting result: seniors
showed significantly lowered risk of falls after being given olfactory stimuli consisting of
a lavender scent for 12 months. Thus, it can be concluded that olfactory stimuli enhance
balance ability, which supports previous research.  Miyanari et al.21) have reported that
many areas of the brain can be activated by olfactory stimuli: the subthalamic nucleus in
the left hemisphere and precentral gyrus, insula right hemisphere, and right superior
frontal gyrus, as well as the orbitofrontal cortex. Also, cerebellar activity was
consistently observed in functional imaging studies of olfaction22, 23). Thus, it was
found that olfactory stimuli can activate other areas of the brain as well as olfactory
function.  Previous research has found that performance of balance tasks may activate many regions of
the brain: the parietal lobe, prefrontal cortex, sensorimotor regions, precuneus, cingulate
cortex, thalamus, frontal gyri, temporal gyri, cerebellum, vermis, basal ganglia,
supplementary motor area, insula, supramarginal gyrus, precentral gyrus, corpus callosum,
and caudate nucleus28,29,30). Thus, it might be
possible to conclude in general that performing balance tasks would lead to activation of
various regions of the brain.  Of the abovementioned activated regions, the insula is considered one of the most activated
regions in functional neuroimaging research31, 32). It is known that it is involved in the
input of visceral motor/sensory, gustatory, olfactory, vestibular/auditory, visual, verbal,
pain, and sensory/motor information; auditory processing with respect to music; eating; and
processing of attention and emotion33,34,35,36). Craig37) argued that the insula integrates and processes various types of
stimuli.  Ng38) suggested that maintenance of
balance must involve simultaneous and continuous data processing of multiple systems
including sensory information; visual, vestibular, and proprioceptive senses; cognitive
integration; attention and executive function; cerebellar function; and sensory and motor
feedback. The insula contains the vestibular system39). It has been reported that vestibular stimulation leads to
activation of the brain40), specifically,
the right posterior insula41). Also, many
functional neuroimaging studies of olfaction have continuously observed cerebellar
activities22, 23).  Together, the abovementioned studies suggest that olfactory stimuli can activate the insula
and cerebellum and that performing balance tasks can activate the insula, cerebellum, and
vestibular system. Thus, the combination and interaction of olfactory stimuli and performing
balance tasks can activate various regions of the brain, and help enhance the balance
ability of stroke patients. The COP values showed significant differences when black pepper
and lavender scents were used as olfactory stimuli, but no difference was found with
distilled water. The COP values increased with the eyes closed. Such a result can be
explained by a previous study, which found that balance control needs visual, vestibular,
and proprioceptive senses35), and another
study, which found that postural control was dependent on visual information in stroke
patients when standing42). Different COP
values depending on the presence/absence of sight might be a natural result, since blockage
of sight results in increased body sway, as sight is one of the important elements for
postural control. Visual dependence of stroke patients also contributed to the difference in
COP values in the present study. The finding of significant differences in COP values in the
black pepper and lavender scent groups might lead us to conclude that olfactory stimuli
affect balance ability.  Freeman S et al.25) found that the COP
values of the elderly decreased with the eyes closed, but it was found in this research that
the COP values of stroke patients decreased with the eyes open. This finding explains why we
could not greatly lower the COP values of stroke patients by providing olfactory stimulus
with the eyes closed, since they show visual dependence behavior42).  It was found that an olfactory stimulus led to improvement of balance ability in the stroke
patients. This result might be attributable to strong activation and interaction of various
areas of the brain as result of the olfactory stimulus and their performance of balance
tasks. Further research should be carried before making any generalizations, since not much
research has been carried out on the relationship between an olfactory stimulus and
balance.

Question: Compared to Distilled water what was the result of Black pepper oil on Area of the 95% confidence ellipse with the eyes closed?
Evidence: With the eyes open, a statistically significant difference was not found
(p<0.05) among the three groups in area
Answer: no significant difference