Article

Impaired Autonomic Nervous System Activity During Sleep in Family Caregivers of Ambulatory Dementia Patients in Japan

Biological Research for Nursing 2015, Vol. 17(1) 21-28 ª The Author(s) 2014 Reprints and permission: sagepub.com/journalsPermissions.nav DOI: 10.1177/1099800414524050 brn.sagepub.com

Shihomi Sakurai, PHN, MSN1,2, Joji Onishi, MD, PhD, MPH3, and Makoto Hirai, MD, PhD1

Abstract The number of dementia patients requiring care is rapidly increasing in Japan. Consequently, a large percentage of family members, including spouses and children of those with dementia, are assuming the role of primary caregiver. Many caregivers develop health problems including sleep disorders. Some report poor quality of sleep even when sleep duration is normal. In the present study, we used actigraphy and heart rate variability spectral analysis to assess autonomic nervous system activity and quality of sleep in family caregivers of people with ambulatory dementia. The 20 caregivers who participated in our study exhibited significantly higher levels of sympathetic nervous system activity during sleep than noncaregivers. This abnormal activity was most prominent during the first half of the sleep period and was not related to overall sleep duration. We propose that relaxation is inhibited during the first half of the sleep period in this caregiver population. This may be due to increased stress, as caregivers of people with ambulatory dementia may worry about their patients waking and wandering at night, potentially injuring themselves. Our findings indicate a need for increased support for caregivers of people with dementia, including the assessment and treatment of sleep disorders. Keywords actigraphy, autonomic nervous system activity, caregiver, dementia, sleep

The population of people with dementia is expected to exceed 65.7 million worldwide by 2030 (World Health Organization, 2012). In Japan, it is estimated that the number of patients with dementia requiring care will reach 3.23 million by 2025. It is customary for people in Japan to care for their aging parents; accordingly, 60% of caregivers of frail, elderly individuals are family members (Ministry of Health, Labour and Welfare, 2008). Many of these caregivers develop health problems related to the stress of caregiving to the extent that family caregiving of patients with dementia is becoming a social problem. Two thirds of family caregivers of people with dementia have experienced sleep disorders (McCurry, Pike, Vitiello, Logsdon, & Teri, 2008). Furthermore, a number of reports on the health and sleeping habits of family caregivers of people with dementia have suggested that these sleep disorders are associated with an increased risk of cardiovascular disease (Mausbach et al., 2006; Mills et al., 2009; von Ka¨nel et al., 2006). Therefore, the development of support systems for caregivers who are suffering from sleep disorders may have a protective effect against cardiovascular disease. The characteristics of sleep disorders that affect family caregivers of people with dementia include reduced sleep time, lowered sleep efficiency, extended sleep latency, and frequently interrupted sleep (McCurry, Logsdon, Teri, & Vitiello, 2007;

von Ka¨nel et al., 2006). Increased waking time after sleep onset has been positively correlated with increased sympathetic nervous system activity (Mausbach et al., 2006). Reduced sleep time has also been correlated with increased sympathetic nervous system activity (Tochikubo, Ikeda, Miyajima, & Ishii, 1996). Thus, increased autonomic nervous activity seems to be clearly related to reduced sleep in this population. Some caregivers report sleep problems even when the amount of sleep they receive each night is within the average range. For instance, researchers have found that caregivers of people with dementia suffer from poor quality sleep due to the psychological impact of the burden of caregiving or related

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Department of Nursing, Nagoya University Graduate School of Medicine, Nagoya, Japan 2 Department of Community Nursing, Kanazawa Medical University School of Nursing, Kanazawa, Japan 3 Department of Community Medicine, Nara Medical University, Kashihara, Japan Corresponding Author: Shihomi Sakurai, PHN, MSN, Nagoya University Graduate School of Medicine, 1-1, Daikominami, Higasi-ku, Nagoya 461-8673, Japan. Email: [email protected]

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instances of depression (McCurry et al., 2007; Rowe, McCrae, Campbell, Benito, & Cheng, 2008). We have not, however, encountered any studies that have examined sleep quality in dementia caregivers who report sleep problems but receive a normal amount of sleep. Sleep quality can be measured using both subjective and objective indices. Objective measures include actigraphy to measure sleep efficiency and heart rate variability (HRV) for the assessment of autonomic nervous system activity (McCurry, Gibbons, Logsdon, Vitiello, & Teri, 2009; Takahara et al., 2008). In the present study, we investigated whether the sleep of family caregivers of people with dementia is disturbed in terms of autonomic nervous system activity, irrespective of the amount of sleep they receive. We used HRV to evaluate autonomic nervous system activity during sleep. We quantified the power spectra on the basis of standardized frequency domain measurements (Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology, 1996), using low frequency (LF) power (0.04–0.15 Hz) and high frequency (HF) power (0.15–0.40 Hz) as indices of HRV. While HF is vagally mediated, LF originates from a variety of both sympathetic and vagal mechanisms. Otzenberger et al. (1998) reported that HRV was closely correlated with a well-documented marker of sympathovagal balance, that is, the ratio of LF to HF power in the frequency spectrum analysis of R-R intervals on the electrocardiogram (ECG). We focused on the burden of caregiving, which previous authors have proposed as a factor in poor sleep quality (McCurry et al., 2007). Some investigators have reported that self-reported sleep quality of caregivers was related to the daytime and nighttime behaviors of patients for whom they cared (Naruse, Nagata, Taguchi, Kuwahara, & Murashima, 2012; Simpson & Carter, 2013), but others have found no such relationship (Beaudreau et al., 2008; McCurry et al., 2008). Naruse, Nagata, Taguchi, Kuwahara, and Murashima (2012) found that the sleep issues that caregivers of physically independent people with dementia reported were related to the severity of the dementia symptoms of the person for whom they were caring. However, among caregivers of physically dependent people with dementia, the severity of dementia did not contribute to self-reported caregiver sleep issues. McCurry, Logsdon, Teri, and Vitiello (2007) and Beaudreau et al. (2008), who found no relationship between severity of dementia symptoms and self-reported caregiver sleep quality, evaluated caregivers’ sleep without regard to the physical abilities of the patients with dementia for whom they cared. One explanation for these contradictory results thus may be that the physical abilities of the patients with dementia are related to the quality of sleep of their caregivers. We hypothesized that, within the total population of caregivers of people with dementia, caregivers of more physically able people with dementia would report a heavier psychological burden of caregiving and more severe sleep disturbances, irrespective of their actual amount of sleep and wake time after sleep onset. Because of the good physical condition of the patients, their caregivers may be more concerned about the possibility that they will get out of bed and wander, a concern that

could result in decreased sleep time and quality. More specifically, our primary hypothesis for the present study was that family caregivers of people with ambulatory dementia experience increased sympathetic nervous system activity at night, even if they receive an average amount of sleep.

Materials and Methods Participants We recruited 20 family caregivers (caregiver group) of people with dementia and 20 noncaregivers (noncaregiver group). The inclusion criteria for caregivers were as follows: (1) age  75 years; (2) for women, more than 2 years after menopause; (3) not receiving treatment for sleep disorders; and (4) caring for patients with little or no gait disturbances who had been diagnosed with dementia by a physician or by a care certification committee. The inclusion criteria for noncaregivers (control participants) included the first three of the four criteria for caregivers. We limited the age of the participants to reduce the impact of aging on sleep and autonomic nervous system activity. We limited participants to men and postmenopausal women to reduce the effects of female hormones on sleep and autonomic nervous system activity. We recruited caregivers with the assistance of the staff of 17 home care support centers in the Tokai and Hokuriku regions of Japan. Staff members of the home care support centers distributed written information about the protocol of the study to caregivers. We then telephoned the caregivers whom the staff had contacted and explained the study. We obtained written informed consent from all caregivers before participation. We recruited noncaregivers for the study by placing fliers at community centers in the Tokai and Hokuriku regions. People who submitted applications to participate in the study were included as control participants if they satisfied the inclusion criteria and gave written informed consent.

Ethical Considerations This study conformed to the provisions of the 1995 Declaration of Helsinki (as revised in Edinburgh in 2000). The Ethics Review Committee of the Nagoya University School of Medicine, Nagoya, Japan (Ref: 8-110) approved the protocol for this study. All participants gave written informed consent before participating in this study, and their anonymity was preserved.

Outcome Measures Sleep/waking. We recorded muscular activity level during sleep using an actigraph. During recording, zero crossings were set to occur at 1-min intervals, and an evaluation was made every minute. The AW2 software package (Ambulatory Monitoring, Inc., Ardsley, NY), which incorporates Cole’s sleep scoring algorithm (Cole, Kripke, Gruen, Mullany, & Gillin, 1992), was used to score sleep/wake states. The sleep variables were defined as follows:

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1. Sleep time: Total duration of sleep in minutes (i.e., time spent in a sleep state between sleep onset and wake time). 2. Sleep efficiency: (total sleep/time in bed)  100. 3. Sleep latency: Time in minutes between bedtime and sleep onset. 4. Wake after sleep onset (WASO): Amount of time scored as awake between sleep onset and wake time. The nighttime sleep period was divided into a first half and a second half based on the midpoint of total sleep time. Participants complete sleep diaries in which they recorded time in bed, wake time and reasons for WASO, which we used in conjunction with the actigraphy data to generate in-bed and out-of-bed periods for analysis using the AW2 software package.

Autonomic Nervous System Activity The R-R (R wave to R wave) interval of heart activity was recorded during sleep using an Activtracer AC301 and evaluated using a Mem-Calc calculator (GMS Inc., Tokyo). After arrhythmia analysis, HRV was measured. We then calculated the HF amplitude, as (2  HF power)1/2, and the LF/HF ratio. HRV was assessed every 5 min. We used the LF/HF ratio as a relative index of sympathetic activity and HF amplitude as an index of parasympathetic activity. Higher HF amplitudes indicate higher levels of parasympathetic nervous system activity, and higher LF/HF ratios indicate higher levels of sympathetic nervous system activity.

Questionnaires Questionnaires focused on the sleep and stress status of the family member acting as the caregiver and the health status of the person receiving care. We used an original questionnaire developed for the study to gather data about caregivers, including lifestyle behaviors, health status, stress level, period of providing care, relationship to the patient, and their patients’ attributes. Participants rated their health status using a 5point Likert-type scale: 1 ¼ very poor, 2 ¼ poor, 3 ¼ passable, 4 ¼ good, and 5 ¼ very good. Stress levels of the caregivers were evaluated using a visual analog scale (VAS), a tool frequently used to measure subjective phenomena (Abekura et al., 2011; Kokubo et al., 2013). Participants rated their current stress level on the VAS, with the highest level of stress they had experienced between birth and the day of the study represented by a rating of 10. We administered the Pittsburgh Sleep Quality Index (PSQI) to evaluate perceived sleep quality in the caregivers. The PSQI was developed in 1988 for use in the screening of sleep disorders (Buysse, Reynolds, Monk, Berman, & Kupfer, 1989) and Doi, Miwa, Uchiyama, and Okawa (1998) later developed the self-administered Japanese version. The PSQI is a subjective measure that evaluates sleep quality, sleep latency, sleep duration, habitual sleep efficiency, sleep disturbances, use of sleep medication, and daytime dysfunction over 1 month. Overall,

sleep quality is determined by calculating a global PSQI score (0–21 points). A higher score on the PSQI reflects a poorer quality of sleep, with a score of 5.5 or higher indicating the presence of sleep disorders. We administered the Barthel Index to determine the level of self-sufficiency in the patients’ activities of daily living (Mahoney & Barthel, 1965). A higher total score indicates a greater level of independence in performing activities of daily living, with a score of 100 indicating the ability to be completely self-sufficient. Finally, we administered the Dementia Behavior Disturbance Scale (DBDS) to assess the patients’ behavioral disorders and psychiatric symptoms related to dementia (Baumgarten, Becker, & Gauthier, 1990). The scale consists of 28 items, each of which is rated on a 5-point Likert-type scale according to frequency of occurrence: 0 ¼ never, 1 ¼ rarely, 2 ¼ sometimes, 3 ¼ frequently, and 4 ¼ all the time. A higher total score thus indicates a greater frequency of behavioral disorders and psychiatric symptoms.

Procedures We telephoned each participant to arrange appointments for home visits on days that satisfied the following conditions: (1) the person with dementia was at home and (2) the participant was engaged in his or her normal daily activities. We sent the self-administered questionnaires, described previously, to each participant 1 week before the day of our first visit. We visited the home of each participant on 2 consecutive days. At the first visit, we had the participant read a document explaining the purpose of the study and obtained written informed consent. We then administered the questionnaires. We recorded a 12-lead ECG using an EKG PCLINK (Cardio View; Micro Medical Industries, NY) and provided the participant with an Activtracer AC301 (GMS Inc., Tokyo) and an actigraph (Micro Mini; Ambulatory Monitoring, Inc., Ardsley, NY). We attached the actigraph to the wrist of participants’ nondominant arm. We asked participants to wear the devices continuously until the next morning and to refrain from bathing but told them that they could remove the devices if they were uncomfortable or interfered with their sleep. We also asked them to complete a sleep diary immediately upon waking. The next day we visited again, removed the test equipment, and ascertained that the participants had been able to sleep as usual. We conducted this investigation from October 1 to November 30 in 2008, 2009, and 2010, and from March 1 to July 31 in 2009 and 2010. We avoided gathering data during the summer and winter to minimize the effects of length of daylight period and room temperature on sleep and autonomic activity.

Statistical Analysis We used Statistical Package for the Social Sciences (SPSS) software (version 17.0 J; SPSS, Chicago, IL) for statistical analysis. The Mann-Whitney U test, Fisher’s exact probability test, and Pearson’s w2 test were used when applicable.

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Table 1. Participant Characteristics. Characteristic Age (years), median (25th–75th percentile) Sex, female Currently employed No. family members in household Two Three or more Smokes cigarettes, yes Drinks alcoholic beverages, yes Exercises regularly, yes BMI 25 kg/m2 Perceived health status Very poor Poor Passable Good Very good Medical history Hypertension Angina pectoris Cerebrovascular disease Diabetes mellitus Dyslipidemia Perceived stress score, median (25th–75th percentile)a

Caregivers, n ¼ 20

Noncaregivers, n ¼ 20

p Value

60.0 (56.0–65.8) 16 (80.0) 6 (30.0)

64.5 (59.3–69.0) 16 (80.0) 7 (35.0)

.174 1.000 .736 .113

7 (35.0) 13 (65.0) 3 (15.0) 7 (35.0) 6 (30.0)

12 8 0 6 10

(60.0) (40.0) (0) (30.0) (50.0)

17 (85.0) 3 (15.0)

18 (90.0) 2 (10.0)

.231 .736 .197 .890

.006* 0 (0) 5 (25.0) 6 (30.0) 8 (40.0) 1 (5.0) 7 (35.0) 0 (0) 0 (0) 1 (5.0) 4 (22.2) 5.0 (3.0–6.8)

0 0 1 18 1

(0) (0) (5.0) (90.0) (5.0)

7 (35.0) 1 (5.0) 0 (0) 0 (0) 4 (22.2) 2.0 (0.3–3.0)

1.000 1.000 1.000 1.000

Impaired autonomic nervous system activity during sleep in family caregivers of ambulatory dementia patients in Japan.

The number of dementia patients requiring care is rapidly increasing in Japan. Consequently, a large percentage of family members, including spouses a...
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