The effect of olfactory stimuli on the balance ability of strokepatients

Mi-Na Gim

Sang-bin Lee

Kyung-Tae Yoo

Ji-Young Bae

Mi-Kyoung Kim

Jung-Hyun Choi

Abstract

INTRODUCTION

A stroke is an acute onset of neurological dysfunction resulting from an abnormality ofcerebral circulation1⁾ and is one of themajor causes of long-term disability2⁾.Stroke patients’ sensory, motor, cognitive, and emotional disabilities impose restrictionson their basic activities of daily living3⁾. Disabilities in the form of reduced postural balance, posturalcontrol, and functional movement are general problems of stroke patients4⁾. Impairment of balance control is a mainproblem in these patients, since it may greatly affect their mobility and independence andoften increases the risk of falls5, 6⁾.

Balance deficits can be identified from observing increased postural sway in strokepatients during quiet standing7, 8⁾. Many studies on quiet standing in stroke patients haveutilized force platform technology to evaluate weight bearing and body sway; based on thelocation and movement of the COP of the ground reaction force9⁾. Analysis of the movement of the COP obtained from data collectedusing 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 whichthe anterior-posterior and medial-lateral displacements of the COP are calculated on a forceplatform11⁾. In general, evaluation ofbalance ability of stroke patients depends on the following four indices: mean COP velocity(velocity), area of the 95% confidence ellipse (area), average anterior-posteriordisplacement (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 hierarchicalneural systems including the spinal cord, brainstem, cerebellum, basal ganglia, and thecerebral cortex16⁾. Standing balancecontrol, in turn, is a complex sensorimotor action based on automated and reflexive spinalprograms under the influence of the brainstem, cerebellum, cortex, and several distinct andseparate supraspinal centers17⁾. In orderto maintain postural control a series of processes are required that involve varioussystems, 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 cerebralcortex20⁾ and that olfactory stimulationactivates various regions of the brain as well as the orbitofrontal cortex21⁾. Other research has suggested that thecerebellum is involved in odor information processing22, 23⁾. It has also been foundthat patients with localized cerebellar atrophies and focal cerebellar lesions showedolfactory impairment24⁾. All thesefindings may lead us to assume that olfactory stimulation is closely related to variousregions of the brain.

Some recent research has suggested that olfactory stimulation may increase the posturalstability of the elderly25⁾. It has alsobeen reported that olfactory stimulation increased the gait ability of the elderly26⁾ and that it decreased their risk offalls27⁾. Many studies have been carriedout to identify the relationship between olfactory stimulation and postural control, but notmuch has been reported on stroke patients. This study attempted to identify the effect ofolfactory stimulation on the balance ability of stroke patients having balance problems.

SUBJECTS AND METHODS

Table 1

Table 1.

Subject characteristics

	BPO mean±SD	LVO mean±SD	DW mean±SD
Gender (male/female)	11/0	11/0	11/0
Age (years)	58.7±15.1	62.6±10.7	57.5±10.1
Height (cm)	170.4±4.4	169.8±5.3	167.3±7.2
Weight (kg)	67.4±8.0	63.9±6.8	64.7±6.8
Stroke type (number)
Ischemic/hemorrhagic	6/5	5/6	7/4
Affected side (number)
Left/Right	8/3	10/1	8/3
Time since stroke (month)	25.4±12.4	22.4±16.1	30.4±16.5
MMSE (score)	28.2±2.2	27.55±2.7	25.73±2.2
Brunnstrom (stage)	4.36±0.8	4.00±0.8	4.18±0.8

BPO, black pepper oil; LVO, lavender oil; DW, distilled water; MMSE, mini-mental

shows the general physical characteristics of the group of chronic strokepatients used as subjects, who met the following criteria: they were chronic stroke patientswho had hemiplegia from strokes for at least 6 months; had normal olfactory functiondiagnosed with an olfactory identification test; scored greater than 24 points on themini-mental state examination (MMSE) test and showed no problem in communication, could walk10 m by themselves did not have any disease in musculoskeletal, cardiovascular, or endocrinesystem, who did not take any medicine that a could influence posture and balance passed thethird stage of the Brunnstrom recovery scale; and agreed to voluntarily participate in thepresent 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 IRBapproval 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. Theexperiment was conducted for all three groups between 10 to 11 in the morning. Measurementof 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/stimulustrial) of Romberg’s test (eyes open 1 min/eyes closed 1 min) on the force platform (BT4, HurLaps Oy, Tampere, Finland).

First, a Romberg’s test (for COP measurement) was conducted before olfactory stimuli forone minute with the eyes open, and this was followed by two minutes of rest and thenperformance of the test again for one minute with the eyes closed. After a four minute ofrest, the olfactory stimulus was given, and the COP was measured for one minute with theeyes open; this was followed by two minutes of rest and then measurement of the COP againfor one minute with the eyes closed. The olfactory stimulus was given to the patients via anaroma necklace that they did not wear during rest periods. The subjects sat in a chaircomfortably while resting25⁾.

COP excursion was tested using a four-channel portable force platform (Hur Labs BT4) thatwas calibrated prior to testing; the channels were checked before every test. The Patientswere instructed to look straight ahead and stand as still as possible with their armshanging down. The foot position was standardized: patients stood with a 2 cm heel-to-heeldistance 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 atleast 5 s (pre-phase) before measurement. After the pre-phase, the COP was measured for thenext 60 seconds. Signals were sampled at 200 Hz and filtered with a digital low-pass filterat a 7.8 Hz cutoff frequency prior to sampling; signals were filtered with two low-passfilters, with the first-stage filter being a is sinc3 type and the second-stage filter beinga 22-tap filter.

In the current research, the area of the 95% confidence ellipse (area), averageanterior-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 allstatistical analyses. The general characteristics of the subjects were analyzed with theKolmogorov-Smirnov test. Multivariate analysis of variance was to analyze variable effectsbased on the three balance ability factors, area, Xmean, and Ymean, of the three groups. Apaired t-test was also conducted to compare presence and absence of sight: the eyes open andeyes closed conditions. The level of significance was set at 0.05.

RESULTS

The three groups showed changes in area, Xmean, and Ymean before and after olfactorystimuli with the eyes open and eyes closed, as shown in Table 2

Table 2.

Differences among the three groups in area, Xmean and Ymean before and afterolfactory stimuli with eyes open and closed

Condition	Variable	Group	Pre mean±SD	Post mean±SD
EO	Area (mm²)	BPO	521.3±397.6	394.6±249.1
		LVO	602.5±594.1	500.2±401.2
		DW	570.0±346.5	458.8±290.1
	Xmean (mm)	BPO*	22.8±16.3	16.2±11.9
		LVO*	21.0±14.8	14.3±11.5
		DW	20.8±20.8	16.9±11.7
	Ymean (mm)	BPO*	−15.7±12.8	−25.5±12.7
		LVO	−17.7±15.9	−21.1±15.9
		DW	−14.4±14.7	−17.3±17.8
EC	Area (mm²)	BPO	528.1±497.4	563.3±364.7
		LVO	580.4±510.3	602.7±487.1
		DW	758.1±635.9	632.8±489.4
	Xmean (mm)	BPO	21.5±13.9	18.2±11.8
		LVO	22.6±13.9	15.0±12.5
		DW	21.3±21.8	17.8±15.0
	Ymean (mm)	BPO	−14.0±12.6	−23.9±13.3
		LVO	−18.3±14.8	−19.1±15.9
		DW	−9.3±25.7	−15.0±19.7

*Expressed as p<0.05. BPO, black pepper oil; LVO, lavender oil; DW, distilledwater; area, area of the 95% confidence ellipse; Ymean, average anterior-posteriordisplacement; Xmean, average medial-lateral displacement; EO, eyes open; EC, eyesclosed

. 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 Xmeanand Ymean in comparisons of the values before and after olfactory stimulus. With the eyesclosed, on the other hand, no significant difference was found in area, Xmean, and Ymeanamong the three groups (p>0.05).

There were also changes in area, Xmean, and Ymean within each group with the eyes open andeyes closed (Table 3

Table 3.

Eyes open vs. eyes closed: differences in area, Xmean, and Ymean of each groupbefore and after olfactory stimulation

Group	Variable	EO mean±SD	EC mean±SD
BPO	Area* (mm²)	126.7±213.9	−35.2±290.1
	Xmean* (mm)	6.6±12.2	3.2±10.9
	Ymean (mm)	9.8±11.0	9.9±8.3
LVO	Area* (mm²)	602.5±594.1	−102.5±170.0
	Xmean (mm)	−1.6±13.3	−0.6±5.4
	Ymean	0.6±6.1	−1.9±8.1
DW	Area (mm²)	−188.1±463.8	−173.9±270.2
	Xmean (mm)	−0.5±18.4	−0.9±6.6
	Ymean (mm)	−5.0±15.1	−2.2±8.0

). 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 showedsignificant differences (p<0.05). However, no significant difference was found incomparison of the eyes open and eyes closed conditions in terms of the comparison in Ymeanof the BPO group, Xmean and Ymean of the LVO group and all three indices in the DWgroup.

DISCUSSION

The present research attempted to identify the impact of olfactory stimuli on the balanceability 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 withblack pepper oil and lavender oil as olfactory stimuli that the COP values (RMS velocity andtrajectory length in the medial-lateral and anterior-posterior directions) decreasedsignificantly. Ebihara et al.26⁾ alsoreported that the TUG (Timed Up and Go) test score of the elderly significantly decreasedafter being given olfactory stimuli of lavender oil and grapefruit oil. Sakamoto et al.27⁾ also found an interesting result: seniorsshowed significantly lowered risk of falls after being given olfactory stimuli consisting ofa lavender scent for 12 months. Thus, it can be concluded that olfactory stimuli enhancebalance ability, which supports previous research.

Miyanari et al.21⁾ have reported thatmany areas of the brain can be activated by olfactory stimuli: the subthalamic nucleus inthe left hemisphere and precentral gyrus, insula right hemisphere, and right superiorfrontal gyrus, as well as the orbitofrontal cortex. Also, cerebellar activity wasconsistently observed in functional imaging studies of olfaction22, 23⁾. Thus, it wasfound that olfactory stimuli can activate other areas of the brain as well as olfactoryfunction.

Previous research has found that performance of balance tasks may activate many regions ofthe brain: the parietal lobe, prefrontal cortex, sensorimotor regions, precuneus, cingulatecortex, 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 bepossible to conclude in general that performing balance tasks would lead to activation ofvarious regions of the brain.

Of the abovementioned activated regions, the insula is considered one of the most activatedregions in functional neuroimaging research31, 32⁾. It is known that it is involved in theinput of visceral motor/sensory, gustatory, olfactory, vestibular/auditory, visual, verbal,pain, and sensory/motor information; auditory processing with respect to music; eating; andprocessing of attention and emotion33,34,35,36⁾. Craig37⁾ argued that the insula integrates and processes various types ofstimuli.

Ng38⁾ suggested that maintenance ofbalance must involve simultaneous and continuous data processing of multiple systemsincluding sensory information; visual, vestibular, and proprioceptive senses; cognitiveintegration; attention and executive function; cerebellar function; and sensory and motorfeedback. The insula contains the vestibular system39⁾. It has been reported that vestibular stimulation leads toactivation of the brain40⁾, specifically,the right posterior insula41⁾. Also, manyfunctional neuroimaging studies of olfaction have continuously observed cerebellaractivities22, 23⁾.

Together, the abovementioned studies suggest that olfactory stimuli can activate the insulaand cerebellum and that performing balance tasks can activate the insula, cerebellum, andvestibular system. Thus, the combination and interaction of olfactory stimuli and performingbalance tasks can activate various regions of the brain, and help enhance the balanceability of stroke patients. The COP values showed significant differences when black pepperand lavender scents were used as olfactory stimuli, but no difference was found withdistilled water. The COP values increased with the eyes closed. Such a result can beexplained by a previous study, which found that balance control needs visual, vestibular,and proprioceptive senses35⁾, and anotherstudy, which found that postural control was dependent on visual information in strokepatients when standing42⁾. Different COPvalues depending on the presence/absence of sight might be a natural result, since blockageof sight results in increased body sway, as sight is one of the important elements forpostural control. Visual dependence of stroke patients also contributed to the difference inCOP values in the present study. The finding of significant differences in COP values in theblack pepper and lavender scent groups might lead us to conclude that olfactory stimuliaffect balance ability.

Freeman S et al.25⁾ found that the COPvalues of the elderly decreased with the eyes closed, but it was found in this research thatthe COP values of stroke patients decreased with the eyes open. This finding explains why wecould not greatly lower the COP values of stroke patients by providing olfactory stimuluswith the eyes closed, since they show visual dependence behavior42⁾.

It was found that an olfactory stimulus led to improvement of balance ability in the strokepatients. This result might be attributable to strong activation and interaction of variousareas of the brain as result of the olfactory stimulus and their performance of balancetasks. Further research should be carried before making any generalizations, since not muchresearch has been carried out on the relationship between an olfactory stimulus andbalance.

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