1.      Introduction

Since its proposition by Skill, [1]in 1989, Vibroacoustic Therapy (VAT) has gained prominence owing to its therapeutic effects, most of which have been identified in the octave range between 40 and 80 Hz, which is the range at the center of the VAT area. VAT is a process in which vibrations are directly applied to the body in the form of low-frequency sinusoid tones in combination with selected musicStandly[2]demonstrated that VAT, which combines “listening to music” with vibrotactile stimulation, resulted in substantial relaxation effects when compared with “listening to music” alone. In addition, Lundqvist et al. [3] demonstrated the efficacy of VAT in reducing self-injurious, stereotypic, and destructive behaviors among patients with developmental disabilities.

Our previous study [4] suggested that VAT mitigates the depressive symptoms in elderly Nursing Home (NH) residents. However, no improvement effect on the cognitive function was reported in that study.

In this study, the device used is a mattress-type vibroacoustic device, its low-frequency (20-150Hz) components produce vibration through six vibration transducers placed near the shoulders, waist, and femur. Our pilot study [5] suggests that steam foot spas mitigate cognitive impairment, primarily attentional disturbance, potentially improving the cardiac function in geriatric impairments. The cholinergic nervous sural region, which projects from the Nucleus Basalis of　Meynert(NBM)in the basal forebrain to the cerebral cortex and from the septal region to the hippocampus, dilates the blood vessels in the cerebral cortex and hippocampus [6]. The activation of the nicotinic acetylcholine nervous system enhances the neuroprotective effect to increase the secretion of the nerve growth factor [7].  Piché et al. [8] investigated the NBM nerve activity with somatosensory stimulation (brushing to the peripheral limbs of rats) and determined the release of acetylcholine and increased blood flow in the cerebral cortex. Improvement in the attentional disturbance of hospitalized elderly patients by steam foot spas could be attributed to the activity of the NBM because of the thermal stimulation of lower limbs.

Thus, it can be hypothesized that steam foot spas improve attentional disturbance in the elderly. However, because this device uses steam (42^°C), it cannot be used in the summer in Japan. Hence, we developed extremity stimulation via the vibroacoustic device, which, in this study, is a vibration transducer that transforms low-frequency components of 20-150 Hz, which is almost the same frequency band we used in our previous experiments, into vibrations. This device is anticipated to best reflect the efficacy and safety of our previous studies.

In this study, we aimed to investigate whether VAT improved attentional disturbance symptoms in elderly NH residents.

2.                  Subjects and Method

4.1.  Stimuli

We enrolled 10 elderly NH residents (3 males, 7 females; age: 80.38 ± 3.68 years) who presented with surface attentional disturbance (sub-items of the MMSE: attention and calculation, 1.5 ± 1.72/5) (Table 1). We performed extremity stimulation of VAT on all participants for 30 minutes every day for 2 consecutive weeks, except for Saturdays and Sundays. The objectives and procedures of the study were explained to all subjects as well as to their families. This project was approved by the Geriatric Health Service Facility Kiryuuen, and all subjects provided their informed consent.

This vibroacoustic device comprised four manchettes (transducer is embedded) and a headphone to separate audio signals from music into two lines. While auditory music from one of the lines was entirely available for the headphone, the other line isolated low-frequency components (20-150 Hz) and reproduced them as vibrational stimuli through four vibration transducers (a device converting electrical signals into mechanical vibrations) embedded in the manchette to the bilateral upper arm and bilateral lower leg.

Herein, we performed VAT from 15:30 to 16:00 every day based on data by Smallwood et al. [9], which proved that aromatherapy and massage given during that time of the day were most effective for patients with dementia. Similarly, our previous study also indicated that 40Hz vibratory sound for 30-minute period was most effective for PC12m3 cells [10]. All subjects in this study selected the music as per their preference.

4.2.              Outcome Measure

4.2.1.         Rating scale

We examined sadness and depression using DMAS, [11] a 24-item (score, 0-144) observational scale that is used to rate mood and functional abilities. In this scale, the first 17 items were designed to measure mood in cognitively impaired subjects and last seven to assess the cognitive and functional impairment. The mood subscale has a maximum score of 102 with a higher score representing greater dysphoria.

Furthermore, we assessed cognitive performance using the Mini-Mental State Examination (MMSE; score: 0-30)[12]. Behavioral disturbances were assessed using the Dementia Behavior Disturbance (DBD; score: 0-68) scale. [13]. In addition, we developed a 28-item DBD scale to avoid certain challenges encountered while using older instruments. Each of the 28 items was designed to be used in an interview format, with patients’ primary caregivers as respondents. Each behavior was rated on a Likert-type scale with five possible responses corresponding to the frequency of the behavior in the preceding week (0, never; 4, all the time). Thus, higher scores indicated more disturbances. Notably, the reliability and validity of the Japanese version of the DBD scale has been previously established [14].

For each patient, we recorded DMAS, MMSE, and DBD at the same time before and after 2 weeks of VAT.

4.2.2.         Examination of physical responses

Physiological responses including the tympanic temperature, percutaneous oxygen saturation (SpO₂), blood pressure, and pulse rate were assessed. Tympanic temperature was recorded using a TERUMO ear-type thermometer (EM-30 CPL; TERUMO Co., Ltd., Tokyo, Japan). All measurements were recorded on weekdays over 2 consecutive weeks (a total of 10 times). In addition, we performed each measurement in triplicates after 5 minutes of bed rest immediately after VAT, and the highest value was used for analysis. SpO₂levels were evaluated with a finger pulse oximeter (EPOCH 30; Ubi-X Co., Ltd., Tokyo, Japan) on weekdays over 2 consecutive weeks (a total of 10 times). Furthermore, the BP and pulse were measured using an OMRON digital automatic wrist-type sphygmomanometer (HEM-632; OMRON Co., Ltd., Kyoto, Japan).

4.2.3.         Sleeping hours and sleep efficiency

We measured sleeping hours using a wristwatch-type actigraphy (Micromini RC; Ambulatory Monitoring Inc., Ardsley, NY), which reportedly exhibits 90% or more agreement with sleep polygraphy [15], records gravitational acceleration as little as 0.01 G with pressure sensors in three directions along the X-, Y-, and Z-axes, and discriminates between sleep and wake phases from the amount of activities during gravitational acceleration. Moreover, it uses sleep-wake distinction software approved by the American Academy of Sleep Medicine [16]. We used the Sadeh algorithm as a discriminant [17,18]. We recorded measurements for 16 days, except during bathing, from 1 day before VAT until 1 day after VAT concluded. This aimed to determine each patient’s circaseptan rhythm, which is a cycle comprising 7 days in which several biological processes of life resolve, for example, blood pressure and heart rate [19-21].

4.2.4.         Data analysis

In this study, data were statistically analyzed using SPSS software (version 16.0, SPSS, Chicago, IL). The Wilcoxon signed-ranks test was used to determine significant differences in physiological responses (tympanic temperature, SpO₂, BP, and pulse) before and after VAT, and sleep-wake time (total sleep time, wake time, and nighttime sleep) of the first and second week. We considered the significance level at 0.05.

3.                  Result

Table 2 summarizes the changes in the DMAS, DBD, and MMSE scores before and after VAT. A significant improvement in depression as assessed using DMAS was noted (P< 0.05). In addition, a significant improvement was observed in depression and sadness, as assessed using items 1-17 of DMAS (P< 0.05). However, no significant improvement was observed in the overall dementia severity (items 18-24). Moreover, a significant improvement in the behavioral problems of dementia assessed using the DBD was noted (P< 0.05).  Even though no significant improvement was observed on the MMSE, attention and calculation item (one of the sub-items of MMSE) exhibited a significant difference (P< 0.05). Regarding physiological responses, a significant increase in the tympanic temperature was noted (P< 0.001) after VAT. In addition, a significant decrease in the systolic blood pressure was noted (P< 0.01) after VAT. No significant change was noted in the diastolic blood pressure, pulse, and SpO₂(Table 3). Lastly, no significant change was observed in the sleep-wake rhythm (Table 3).

4.      Discussion

Falempinet al. [22] suggested that the tendon vibration (120 Hz) on the rat soleus muscle can be used as a paradigm to counteract the atrophic process observed after hindlimb unloading. When tendon vibration was applied, the soleus muscle stretched. Hence, they concluded that the protocol used this exercise is eccentric contraction exercise training. The vibration region of VAT in the present study was 20-120 Hz, which suggested that the soleus muscle demonstrates eccentric contraction exercise because it directly stimulates the lower leg triceps on both sides. These findings indicate that although VAT is a passive music therapy, it leads to strength training without putting a burden on the cardiopulmonary function. Blumenthal et al. [23] demonstrated that aerobic exercise is an effective treatment for depression in the elderly compared with antidepressant drugs. Singh et al. [24] reported that not only aerobic exercise but also resident exercise exerts an antidepressant effect. The improvement effect on depression witnessed in 10 elderly NH residents (P< 0.05) in this study could be attributed to eccentric contraction exercise of the soleus muscle by the VAT stimulation. Furthermore, the improvement effect on depression seems to alleviate elderly NH patients’ behavioral problems (P< 0.05). Furthermore, Sunderland et al. [11] reported that scores significantly correlated with the global measures of depression (r = 0.73) and sadness (r = 0.65), with highly satisfactory inter-rater reliability.

Haffeman et al. [25] reported that the resistance exercise training may reduce the central blood pressure in older adults with hypertension and prehypertension. In this study, a significant reduction in the systolic blood pressure could be attributed to the effect of eccentric contraction exercise of the soleus muscle induced by VAT stimulation.

The cholinergic nervous system, which projects from the NBM in the basal forebrain to the cerebral cortex and from the septal region to the hippocampus, dilates the blood vessels in the cerebral cortex and hippocampus. During the flow, nitric oxide is produced by vascular endothelial cells, located on the inner wall of the components of the cardiovascular system, which induces relaxation of vascular smooth muscle cells. Furthermore, it increases the cerebral blood flow, which, in turn, is induced by cerebral microvascular extensions [26]. Piché[8] reported an increase in the NBM nerve activity with somatosensory stimulation and established the release of acetylcholine and increase of the blood flow within the cerebral cortex.

In this study, the temperature inside the tympanic chamber of elderly NH residents significantly increased (P< 0.01) after VAT stimulation, which is presumed to be because of the NBM activity promoting the blood flow in the brain and causing an increase in the internal carotid artery temperature.

This is presumed to be due to the activity of NBM promoting blood flow in the brain, resulting in an increase in internal carotid artery temperature, which was reflected in the significant increase in the temperature inside tympanic chamber [27]. Furthermore, cholinergic neurons are involved in improving cognitive function because these neurons are involved in memory and attention [28].

These neurons activate vasodilators [29]. Vascular endothelial cells are located on the inner wall of the components of the cardiovascular system, and nitric oxide is produced by vascular endothelial cells, which induces the relaxation of vascular smooth muscle cells [26]. It increases cerebral blood flow, which in turn is induced by cerebral microvascular extensions. Cholinergic neurons are activated by somatosensory stimuli, [8,29] suggesting their activation by somatosensory stimulation, improving attention and memory. Apparently, cerebral blood flow temperature are physiological indicators that confirm this effect. Overall, the improvement of attentional disturbance in this study could be attributed to the induction and activation of the NBM by low-frequency VAT stimulation.

5.      Conclusion

The extremity stimulation of VAT may potentially decrease depression and attentional disturbance in elderly NH residents. Nevertheless, further well-controlled, extensive studies are warranted to confirm these findings. In a nutshell, the presence of music is indispensable in promoting the effect of VAT.

6.      Acknowledgments

This study was supported, in part, by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (Grant No.23500625).

Table 1: Characteristics of study participants (n=10). 

Table 2:  Effect of VAT treatments on cognitive function, behavioral symptoms, and psychological symptoms.

Table 3: Effect of VAT treatments on physiological responses and on sleep-wake rhythm.

1.       Skill O (1989)VibroAcoustic therapy. Music therapy8: 61-77.

2.       Standly JM (1991) The effect of vibrotactail and auditory stimuli on perception of comfort, heat reat, and peripheral finger temperature. Journal of music Therapy 28:120-134.

3.       Lundquist LO, Anderson G, Viding J (2009) Effect of vibroacoustic music on challenging haviors in individual with autism and developmental disabilities. Res Autism SpectrDisord 3:390-400.

4.       Koike Y, Hoshitani M, Tabata M, Seki K, Nishimura R, et al. (2012) Effect of vibroacoustic therapy om elderly nursing home residents with depression. JPhysTherSci 24:291-294.

5.       Koike Y, Kondo H, Kondo S, Takagi M, Kano Y (2013) Effect of a steam foot spa on geriatric inpatients with cognitive impairment: a pilot study. Clinical Interventions in Aging 8: 543-548.

6.       Sato A, Sato Y, Uchida S (1992) Regulation of regional cerebral blood flow by cholinergic fibers originating in the basal forebrain. Int J Dev Neurosci14: 327-337.

7.       Hotta H, Kagitani F, Kondo M, Uchida S (2009) Basal forebrain stimulation induces NGF secretion in ipsilateral parietal cortex via nicotinic receptor activation in adult, but not aged rats. Neurosci Res63: 122-128.

8.       Piché M, Uchida S, Hara S, Aikawa Y, Hotta H (2010) Modulation of somatosensory-evoked cortical blood flow changes by GABAergic inhibition of the nucleus basalis of Meynert in urethane-anaesthetized rats. J Physiol588: 2163-2171.

9.       Smallwood J, Brown R, Coulter F, Irvine E, Copland C (2001) Aromatherapy and behaviour disturbances in dementia: a randomized controlled trial. Int J Geriatr Psychiatry16:1010-1013.

10.    Koike Y, Iwamoto S, Kimata Y, Nohno T, Hiragami F, et al. (2004) Low-frequency vibratory sound induces neurite outgrowth in PC12m3 cells in which nerve growth factor-induced neurite outgrowth is impaired. TissCult ResCommun23:81-90.

11.    Sunderland T, Hill JL, Lawlor BA, Molchan SE (1988)NIMH Dementia Mood Assessment Scale (DMAS). Psychopharmacol Bull 24: 747-53.

12.    Folstein MF, Folstein SE, McHugh PR (1975) "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiat Res 12: 189-198.

13.    Baumgarten M, Becker R, Gauthier S (1990) Validity and reliability of the dementia behavior　disturbance scale.JAmGeriatrSoci38:221-226.

14.    Mizoguchi T, Iijima S, Eto F, Ishizuka A, Orimo H (1993) [Reliability and validity of a Japanese version of the Dementia Behavior Disturbance Scale]. Jpn J Geriat [Nihon Ronen IgakkaiZasshi]. 30: 835-840.

15.    Ancoli-Israel S, Cole R, Alessi C, Chambers M, Moorcroft W, et al.(2003) The role of actigraphy in the study of sleep and circadian Rhythms. Sleep 26: 342-392.

16.    Cole RJ, Kripke DF, Gruen W, Mullaney DJ, Gillin JC (1992) Automaticsleep/wakeidentificationfromwristactivity. Sleep 15:461-469.

17.    Sadeh A, Sharkey KM, Carskadon MA (1994) Activity-based sleep-wake identification: an empirical test of methodological issues. Sleep17: 201-207.

18.    Sadeh A, Hauri PJ, Kripke DF, Lavie P (1995) The role of actigraphy in the evaluation of sleep disorders. Sleep 18: 288-302.

19.    Lee MS, Lee JS, Lee JY, Cornélissen G, Otsuka K, et al. (2003) About 7-day (circaseptan) and circadian changes in cold pressor test (CPT).Biomed Pharmacother 57: 39s-44s.

20.    Otsuka K, Yamanaka G, Shinagawa M, Murakami S, Yamanaka T, et al. (2004)Chronomic community screening reveals about 31% depression, elevated blood pressure and infradian vascular rhythm alteration. Biomed Pharmacother.58: S48-55.

21.    Shinagawa M, Otsuka K, Murakami S, Kubo Y, Cornelissen G, et al. (2002) Seven-day (24-h) ambulatory blood pressure monitoring, self-reported depression and quality of life scores.Blood Press Monit 7: 69-76.

22.    Falempin M, In-Albon SF (1999) Influence of brief daily tendon vibration on rat soleus muscle in non-weight-bearing situation. J ApplPhysiol87: 3-9.

23.    Blumenthal JA, Babyak MA, Moore KA, Craighead WE, Herman S, et al. (1999) Effects of exercise training on older patients with major depression. Arch Intern Med 159: 2349-2356.

24.    Singh NA, Clements KM, Singh MA(2001) The efficacy of exercise as a long-term antidepressant in elderly subjects: a randomized, controlled trial. J GerontolABiol Sci Med Sci 56: M497-504.

25.    Heffernan KS, Yoon ES, Sharman JE, Davies JE, Shih YT, et al. (2013) Resistance exercise training reduces arterial reservoir pressure in older adults with prehypertension and hypertension. Hypertens Res 36: 422-427.

26.    Hotta H, Uchida S, Kagitani F (2002) Effects of stimulating the nucleus basalis of Meynert on blood flow and delayed neuronal death following transient ischemia in the rat cerebral cortex. Jpn J Physiol 52: 383-93.

27.    Moriya K, Sekitani T, Yamashita H, Mizokami H (1993) Tympanic membrane temperature in a patient with vertigo. Acta OtolaryngolSuppl506:24-25.

28.    Piri M, Zarrindast MR (2011) Nitric oxide in the ventral tegmental area is involved in retrieval of inhibitory avoidance memory by nicotine. Neuroscience175:154-161.

Uchida S, Hotta H, Misawa H, Kawashima K (2013) The missing link between long-term stimulation of nicotinic receptors and the increases of acetylcholine release and vasodilation in the cerebral cortex of aged rats.J Physiol Sci 63: 95-101.