Effect of neuropsychiatric symptoms of Alzheimer's disease on Chinese and American caregivers
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1 INTERNATIONAL JOURNAL OF GERIATRIC PSYCHIATRY Int J Geriatr Psychiatry 2002; 17: 29±34. DOI: /gps.510 Effect of neuropsychiatric symptoms of Alzheimer's disease on Chinese and American caregivers F. C. Pang 1 *, T. W. Chow 2, J. L. Cummings 3, V. P. Y. Leung 4, H. F. K. Chiu 4,L.C.W.Lam 4, Q. L. Chen 5,C.T.Tai 5, L. W. Chen 5, S. J. Wang 5 and J. L. Fuh 5 1 Department of Geriatrics, Tuen Mun Hospital, Hong Kong 2 Department of Neurology, University of Southern California School of Medicine, Los Angeles 3 Departments of Neurology and Psychiatry and Biobehavioral Science, UCLA School of Medicine, Los Angeles 4 Department of Psychiatry, Chinese University of Hong Kong 5 Taipei Veterans General Hospital SUMMARY Background In Chinese culture, extended family support, acceptance of age-related cognitive changes and lial tradition of caring for elders may decrease caregiver burden and distress in the context of dementia. Objective To study cross-regional and cross-cultural differences in symptom-related caregiver distress due to the behavioral problems of Chinese and American patients with Alzheimer's disease. Method Caregivers of patients with Alzheimer's disease at Taipei Veterans General Hospital, Taiwan n ˆ 89), Chinese University of Hong Kong n ˆ 31) and the UCLA Alzheimer's Disease Research Center, Los Angeles, California n ˆ 169) reported the neuropsychiatric symptoms of patients and their corresponding distress on the Neuropsychiatric Inventory. Result Presence or absence of distress due to the neuropsychiatric symptoms of the patients with Alzheimer's disease was assessed. The three centers differed signi cantly in the proportions of caregivers with distress caused by depression p < 0.05) and apathy p < 0.001). UCLA had higher proportions of caregivers with depression-related distress than Taipei. UCLA caregivers were also more stressed by apathy than caregivers in Taipei and Hong Kong. Logistic regression further supported the ndings that depression-related and apathy-related caregiver distress differed between Chinese and American caregivers p < 0.05). Conclusions The results were surprising, in that American and Chinese Taipei and Hong Kong) caregivers exhibited similar distress or lack of distress in response to delusions, hallucinations, agitation, anxiety, euphoria, disinhibition, irritability, aberrant motor behavior, sleep and appetite symptoms of Alzheimer's disease patients. Chinese caregivers were less affected by depression and apathy in patients with Alzheimer's disease than Caucasian caregivers. Copyright # 2002 John Wiley & Sons, Ltd. key words Ð apathy; Alzheimer's disease; behavior; caregivers; Chinese; dementia; depression; ethnicity; neuropsychiatric inventory; sensitivity INTRODUCTION Patients with Alzheimer's disease AD) progressively lose cognition and abilities for instrumental activities of daily living, simultaneously developing consequential behavioral and psychiatric symptoms Chen JC et al., 2000), which often cause more distress *Correspondence to: Stephen Fei-chau Pang, Department of Geriatrics, Tuen Mun Hospital, Hong Kong. Tel: 852/ Fax: 852/ feichau@netvigator.com for their caregivers than memory loss Rabins et al., 1982). Since caregivers cannot communicate their frustration to patients, caring for a patient with AD can lead to complaints of isolation, shame, and guilt Lee, 1997; Xu, 1987; Freyne et al., 1999). Caregiver distress accumulates and can result in physical illness, psychological illness, substance abuse, and other maladaptive behaviors during the adjustment process Eisdorfer and Cohen, 1981). Behaviors of AD patients that are considered disturbances by one culture may not be as problematic Received 24 April 2001 Copyright # 2002 John Wiley & Sons, Ltd. Accepted 24 April 2001
2 30 f. c. pang et al. for caregivers from another culture. Kleinman et al., 1978; Nilchaikovit et al., 1993; Connell and Gibson, 1997). Although Asian-American caregivers have shown distress levels similar to Caucasian Americans Patterson et al., 1998), traditional caregivers in Chinese countries may not have the same response to patients with AD. Chinese family members place more emphasis on harmonious interpersonal relationships and interdependence than Americans Lee, 1997; Nilchaikovit et al., 1993). Chinese children are socially mandated to care for their disabled elderly out of lial piety Patterson et al., 1998). Since Chinese view memory and behavioral problems associated with dementia as part of the normal ageing process, and dependency in old age as normative behavior Yu et al., 1993), they are more likely to accept age-related cognitive changes than Caucasians Serby et al., 1987). These characteristics may decrease their sense of burden and distress while caring for their demented family members. This study queried samples of Chinese and American caregivers from three centers in three locations: Taipei Veterans General Hospital of Taiwan, The Chinese University of Hong Kong, and UCLA in Los Angeles. Chinese people in Taiwan and Hong Kong differ signi cantly in socioeconomic status and educational level and therefore were considered as two separate sample populations Yu and Chung, 1996; Census and Statistics Department of Hong Kong, 1997; Ministry of Interior, Republic of China, 1997). We explored differences in caregiver distress as reported when patients had neuropsychiatric symptoms, hypothesizing that Chinese extended family support and greater lial obligation than Caucasian Americans would decrease caregiver distress despite the presence of dif cult neuropsychiatric symptomatology in the patients. Work by Heok and Li 1997) and Patterson et al. 1998) has indicated the opposite nding, that caregivers feel burdened by behavioral disturbances in AD patients, but the measures examined in these studies do not directly link caregiver distress to individual neuropsychiatric symptoms. Their instruments measure overall caregiver perceptions of wellbeing, which include physical health, sense of social isolation, and mastery of caregiving tasks. METHOD Data and procedures All caregivers reported on patients diagnosed with probable or possible AD according to National Institute of Neurological and Communicative Disorders and Stroke and the Alzheimer's Disease and Related Disorders Association criteria McKhann et al., 1984). At Taipei Veterans General Hospital, a trained research assistant at the Outpatient Neurobehavior Clinic interviewed the caregivers. At Prince of Wales Hospital in Shatin teaching hospital of the Chinese University of Hong Kong), psychiatrists and a trained research assistant at the Outpatient Psychogeriatric Clinic collected the data. At the UCLA Alzheimer's Disease Research Center, research nurses collected the data. Tools Clinical Dementia Rating CDR) was used to rate the overall severity of dementia. It is a global deterioration scale for assessment of primary degenerative dementia and its psychometric properties are well established Morris, 1993). The Neuropsychiatric Inventory NPI) Cummings et al., 1994; Cummings, 1997) has been translated into Mandarin and Cantonese for administration in Taiwan and Hong Kong, respectively. The inter-rater reliability of the Chinese translations was demonstrated prior to use in this study Fuh et al., 2001). The NPI consists of 12 symptoms delusions, hallucinations, agitation, depression, anxiety, euphoria, apathy, disinhibition, irritability, aberrant motor behavior, sleep, and, appetite) and has been validated for use in patients with dementia. The NPI is a structured interview for caregivers who report on the frequency and severity of abnormal behavior in their patients. They also rate their own distress in response to the behavior Kaufer et al., 1998). The NPI has been shown to be valid and reliable Cummings et al., 1994). Measures Caregiver±patient relationships were categorized into three groups: Type I referred to spouse, Type II referred to other close relatives child or sibling of patient or spouse of child) and Type III referred to friends or other relatives. Gender distribution differences, mean caregiver age, caregiver educational level year) and frequencies of relationship type were tested by Chi-square among the three centers. Caregivers in the three centers rated their distress 0±5. Using a ve-point scale dichotomous presence 1±5) or absence 0)). The proportions of caregivers who had developed symptom-related distress in the three centers were compared and tested by Chi-square
3 effect of neuropsychiatric symptoms of alzheimer's disease 31 model. The signi cant results were further examined by logistic regression with adjustments over the characteristics of patients and caregivers CDR, subscale NPI score, caregiver relationship to patients, caregiver education level, caregiver age, and caregiver gender). Chinese caregivers in Hong Kong and Taipei were also grouped together during the regression test. Odds ratios O.R.) were obtained by Exp ) of the variables with 95% con dence intervals C.I.). Sensitivity of caregiver to a given behavior was indicated by the proportion of caregivers in a city who reported distress caused by presence of the behavior. In sub-group analysis, sensitivity of caregiver groups to a given behavior was compared and tested by Chi-square model on the basis of the category of caregiver-patient relationship. Statistical signi cance was de ned as a p-value of less than 0.05, two tailed. RESULTS The demographic data of the caregivers are presented in Table 1. Caregiver mean educational levels at the three centers differed signi cantly p < 0.05). Caregivers in UCLA had the highest mean education level and caregivers in Hong Kong had the lowest mean education level. The majority of Taiwanese caregivers 61.8%) were patients' spouses Type I), and most caregivers from Hong Kong were non-spouse close relatives Type II relationship, 61.3%). In contrast, the proportion of Type III friends or other relatives) caregivers in UCLA 15.5%) was much higher than that in Taipei 2.2%) and Hong Kong 0%) Table 2. Demographic characteristics of AD patients about whom caregivers responded Characteristics of Taipei Hong Kong UCLA AD patients Mean age at 74.8, 6.9)* ) 77.4, 7.5) evaluation SD) Gender ratio 1.2:1* 6.7:1* 2.6:1* female : male) CDR ratings) Mild 0.5±1) %) %) %) Moderate 2) %) %) %) Severe 3) %) %) %) *p < 0.05, SD ˆ standard deviation. p < 0.05) Table 2). The CDR, mean age, and gender distributions of AD patients did not differ among the three centers Table 1). The frequencies of apathy and appetite problems differed among patients assessed in the three centers Table 3). UCLA had the highest proportion of AD patients who suffered from apathy and Hong Kong had the highest proportion of AD patients who suffered from appetite problem p < 0.05) Chow et al., 2001). Table 4 showed the frequency of caregivers at various severity of distress. Caregiver sensitivity to depression, appetite, and apathy problems of AD patients differed between the three centers. UCLA caregivers had a higher sensitivity to patient depression and appetite change than caregivers in Taipei p < 0.05) but did not differ from Hong Kong Table 5). Caregivers at UCLA also had higher sensitivity to patient apathy than caregivers in both Taipei and Hong Kong p < 0.001) Table 5). Logistic regression revealed that distress of caregivers Table 1. Demographic characteristics of caregivers Characteristics Taipei Hong Kong UCLA of caregivers n ˆ 89) n ˆ 31) n ˆ 169) Mean Age yrs) SD Gender female: male) 2:1 1:1 1.7:1 Mean Educational 12 11* 7 4* * Level yrs) SD Types of relationship between caregiver and AD patient* Spouse Type I) %) %) %) Close relatives 32 36%) %) %) Children/siblings/ spouses of children) Type II) Friends and other 2 2.2%) 0 0%) %) relatives Type III) *p < 0.05, n ˆ total number of AD patients in each center. Table 3. Frequency of behavioral problems in three centers Chow et al., 2001) Neuropsychiatric Taipei Hong Kong UCLA symptoms n ˆ 89) n ˆ 31) n ˆ 169) Delusion %) Hallucination %) Agitation %) Depression %) Anxiety %) Euphoria %) Apathy %)* 48* 35* 59* Disinhibition %) Irritability %) Aberrant Behavior %) Appetite %)* 28* 54* 47* Sleep %) *p < 0.05.
4 32 f. c. pang et al. Table 4. Frequency of caregivers %) reporting severity of distress in response to patients' neuropsychiatric symptoms Frequency of caregivers reporting severity of distress in the presence of NP symptoms No distress Minimal distress Mild distress Moderate distress Severe distress Very severe distress Centers TP HK U TP HK U TP HK U TP HK U TP HK U TP HK U Delusion %) Hallucination %) Agitation %) Depression %) Anxiety %) Euphoria %) Apathy %) Disinhibition %) Irritability %) Aberrant Behavior %) Sleep %) Appetite %) TP, Taipei; HK, Hong Kong; U, UCLA samples. Table 5. Caregiver distress in response to depression, appetite and apathy in AD patients Patient with Caregivers Reporting Patient with Caregivers Reporting Patient with Caregivers Reporting Distress due to Patient Depression Distress due to Patient Appetite Changes Distress due to Patient Apathy UCLA: n ˆ 95, TP: n ˆ 44, HK: n ˆ 14) UCLA: n ˆ 80; TP: n ˆ 25; HK: n ˆ 15) UCLA: n ˆ 100, TP: n ˆ 43, HK: n ˆ 11) Caregivers with Center for Signi cant 2-grp Caregivers Center for Signi cant 2-grp Caregivers with 2, p Signi cant 2-grp Distress, % comparison 2, p comparisons 2, p with Distress, % comparison 2, p comparisons 2, p Distress, % comparisons 2, p Taipei 31, 70.5% UCLA: Taipei < UCLA 12, 48% UCLA: Taipei < UCLA 28, 65% UCLA: Taipei < UCLA 14.8, , , , , , 0.005; HK < UCLA 12, Hong Kong 13, 92.9% 10, 66.7% 5, 45.5% UCLA 89, 93.7% 60, 75% 87, 87%
5 effect of neuropsychiatric symptoms of alzheimer's disease 33 Table 6. Variables Odds Ratios of developing neuropsychiatric symptom-related caregiver distress by logistic regression Odds Ratio 95% CI) Depression Appetite Apathy American/Taiwanese and Hong Kong Chinese ±177.7)* ±8.2) ±13.5)* Clinical Dementia Rating ±23.0)* ±3.0) ±2.0) NPI Subscale Score frequency x severity) ±5.0) ±1.8)* ±1.4) Relationship Type ±27.9) ±3.7) ±2.8) Caregiver Educational Year ±1.0) ±1.0) ±1.2) Caregiver Age ±1.1) ±1.1) ±1.0) Caregiver Gender Female: Male) ±5.6) ±2.7) ±2.2) * ˆ p < to appetite changes did not differ among the three centers after adjustment for the characteristics of patients and caregivers. Ethnicity of AD patient was an independent factor contributing to the caregiver distress in apathy and depression problems of AD patients p < 0.05). Caregivers from UCLA had signi cantly higher odds in reporting depression and apathy-related distress than Chinese caregivers Table 6). For AD patients with depression, higher CDR score was associated with higher rates of caregivers' distress. Higher NPI subscale scores on appetite change of AD patients also caused more caregivers' distress. Relationship to patients, age and gender of caregivers did not affect caregiver distress in relation to the behavioral problems of AD patients Table 6). Similar proportions of spousal Type I) and nonspousal caregivers Types II±III) reported distress across the behavioral symptoms of AD patients. The proportions of children or spouses of children caregivers who had distress in response to NP symptoms did not differ between Chinese Taipei and Hong Kong) and American caregivers. Caregiver±patient relationship and ethnicity of the dyad did not impact the caregiver distress reported. DISCUSSION Differences among the cultural groups were noted only in response to depression and apathy of AD patients. Taiwanese Chinese caregivers were less likely to have depression-related caregiver distress than US caregivers. Both Hong Kong and Taiwanese Chinese caregivers were less sensitive to apathy symptom of AD patients than US caregivers. This might be related to the cultural differences. Confucius classically warned his followers to be cautious in speech because too much talking results in mistakes and mistrust. Therefore, Taiwanese and Hong Kong Chinese caregivers might not regard apathy and depression of AD patients as abnormal behaviors. Also, Taiwanese and Hong Kong Chinese traditionally emphasize peace and moderation, so apathy may not be viewed as problematic by caregivers. Contrary to our expectations but in keeping with previous studies by Heok and Li 1997) and Patterson et al. 1998), Taiwanese, Hong Kong Chinese, and Caucasian American caregivers reported similar distress caused by delusions, hallucinations, agitation, anxiety, euphoria, disinhibition, aberrant motor behavior, sleep, and appetite symptoms in AD patients. Some behaviors were equally non-distressing to caregivers from all three cultural backgrounds. Although one study reports that Chinese caregivers stigmatize mental illness Lin and Fabrega, 1997), there was no evidence in the present study that the disruptive behaviors and positive psychiatric symptoms caused more distress for Taiwanese or Hong Kong Chinese caregivers than American caregivers. Research has found that spouse caregivers report higher burden than non-spouse caregivers Deimling et al., 1989; Montgomery and Kosloski, 1994; Fuh et al., 1999). However, the current study revealed that spouses had similar odds of developing caregiver distress for all behavioral problems compared with non-spouse caregivers at each center and regardless of ethnicity. Chinese caregivers were presumed to have lower distress than US caregivers if lial piety plays a role in caring elderly. In the sub-group analysis, there was no evidence that the Confucian principle of lial piety between children and parents reduced the occurrence of caregiver distress. This contrasts with a previous study by Lee and Sung 1998) that Asian caregivers are less distressed than US caregivers. We did not study the effect of duration of AD and physical health of caregivers on caregiver distress. These factors might also relate to the level of
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