Psychiatry Research 226 (2015) 242–246
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Difference in determinants of caregiver burden between amnestic mild cognitive impairment and mild Alzheimer's disease Chikako Ikeda, Seishi Terada n, Etsuko Oshima, Satoshi Hayashi, Yuko Okahisa, Manabu Takaki, Masatoshi Inagaki, Osamu Yokota, Yosuke Uchitomi Department of Neuropsychiatry, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama, Japan
art ic l e i nf o
a b s t r a c t
Article history: Received 8 April 2014 Received in revised form 24 August 2014 Accepted 27 December 2014 Available online 13 January 2015
Care for the disabled elderly can be stressful and exhausting, especially in cases of dementia. There have been a number of studies on the dementia caregiver burden, but studies focusing on differences by stages of the disease are rare. The caregiver burden of 85 caregivers of patients with amnestic mild cognitive impairment (aMCI) and 106 caregivers of patients with mild Alzheimer's disease (AD) was evaluated by the short version of the Japanese version of the Zarit Burden Interview (sZBI). The caregiver burden in mild AD was more severe than that in aMCI. In mild AD, the risk factors of caregiver burden were neurobehavioral symptoms and disturbances instrumental activities of daily living (IADL), whereas the risk factors in aMCI were neurobehavioral symptoms and memory dysfunction. The severity of dementing disease affects the caregiver burden, and somewhat different factors contribute to the burden at different stages. We should pay attention to different factors in evaluating and reducing the caregiver burden in aMCI and mild AD. & 2015 Elsevier Ireland Ltd. All rights reserved.
Keywords: Alzheimer's disease Caregiver Caregiver burden Mild cognitive impairment Zarit Burden Interview
1. Introduction Few tasks are more challenging than caring for a family member with dementia (Whitebird et al., 2013). Caregivers of patients with dementia experience a greater burden than those caring for non-demented patients (Guerra-Silla et al., 2011). As a result, family caregivers may experience significant mental health problems, as well as a deterioration of their own physical health (Hayashi et al., 2013). Thus, alleviation of the caregiver burden has become a primary public health goal (Arai and Zarit, 2011). Among dementing disorders, Alzheimer's disease (AD) is the leading cause of late-onset dementia worldwide, and among caregivers of AD patients, 68% were highly burdened and 65% exhibited depressive symptoms (Papastavrou et al., 2007). In addition, the problem of the family burden of caring for persons with AD is a common challenge in both developed and developing countries (Chan, 2010). Amnestic mild cognitive impairment (aMCI) is a risk state for AD that is characterized by a deficit in memory with preserved daily functioning (McLaughlin et al., 2014). The annualized conversion rates of aMCI to AD ranged from 11% to 16.5% for studies recruiting from clinics and from 7.4% to 8.9% for community samples (Ward et al.,
2013). Caregivers of patients with aMCI were reported to already experience a need for increased services comparable to those of individuals caring for AD patients (Ryan et al., 2010). It is plausible that in different stages of dementing diseases, the degree of the burden is different and that different factors influence the caregiver burden. However, there have been only a few studies comparing the burden of caregivers for dementia and aMCI patients. Based on previous research including our own (Gallagher et al., 2011; Fisher et al., 2011; Hayashi et al., 2013), we anticipated that the caregiver burden of caregivers for AD patients is more severe than that of caregivers for aMCI patients. Moreover, little is known about whether the risk factors of caregiver burden for patients with aMCI are similar to those for patients with AD (Ryan et al., 2012). We postulated that similar risk factors contribute to caregiver burden of patients with AD and aMCI, but that inability to perform activities of daily (ADL) life may be important in more advanced stages of the disease.
2. Methods 2.1. Participants
n Correspondence to: Department of Neuropsychiatry, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences 2-5-1 Shikata-cho, Kita-ku, Okayama 700-8558, Japan. Tel.: þ81 86 235 7242; fax: þ 81 86 235 7246. E-mail address: [email protected] (S. Terada).
http://dx.doi.org/10.1016/j.psychres.2014.12.055 0165-1781/& 2015 Elsevier Ireland Ltd. All rights reserved.
Eighty five consecutive caregivers of subjects with aMCI and 106 consecutive caregivers of subjects with mild AD were recruited from the outpatient unit of the Memory Clinic of Okayama University Hospital between September 2008 and April 2012 according to the following criteria.
C. Ikeda et al. / Psychiatry Research 226 (2015) 242–246 Inclusion criteria for caregivers were (1) being the family caregiver of an outpatient with aMCI or mild AD, (2) living with the patient or visiting him or her daily, and (3) being cognitively intact. Exclusion criteria were (1) being unable to come to hospital with the patient, (2) having a history of mental illness or substance abuse, and (3) being treated with antipsychotics, antidepressants, or anxiolytic drugs. All patients (1) underwent general physical and neurological examinations and extensive laboratory testing, including thyroid function tests, serum vitamin B12, and syphilis serology; (2) had a global Clinical Dementia Rating (CDR) of 0.5 or 1; (3) took the Mini-Mental State Examination (MMSE) (Folstein et al., 1975), revised Addenbrooke's Cognitive Examination (ACE-R) (Yoshida et al., 2012), revised Wechsler Memory Scale (WMS-R) (Sugishita, 2001), Frontal Assessment Battery (FAB) (Kugo et al., 2007), Neuropsychiatric Inventory (NPI), Barthel Index, and Functional Assessment Questionnaire (FAQ). The aMCI patients all scored Z1.5 standard deviations (S.D.) below the population mean on at least one of three neuropsychological tests (ACE-R memory score, two subscales of WMS-R), and were diagnosed as not having dementia. Previously, we reported the caregiver burden of MCI patients including amnestic and non-amnestic types (n¼ 104). In this study, we examined aMCI only (n¼85). The AD patients were all diagnosed with probable AD according to the criteria formulated by the NINCDS– ADRDA (McKhann et al., 1984). The caregiver burden of AD patients at our clinic has never been reported. In this study, AD patients with a CDR score 0.5 or 1 were defined as patients with mild AD. The exclusion criteria of the patients were (1) complications from other neurological diseases or illnesses; (2) a history of mental illness or substance abuse prior to the onset of dementia; (3) any evidence of focal brain lesions on head MRI; and (4) treatment with antipsychotics, antidepressants or anxiolytic drugs.
2.2. Ethics This study protocol was approved by the committee on human research of Okayama University Hospital on human research. After giving a complete description of the study to the subjects and their relatives, written informed consent was obtained.
2.3. Caregiver assessment The caregiver burden was measured using the short version of the Japanese version of the Zarit Burden Interview (sZBI) (Kumamoto et al., 2004). The caregivers were asked to rate their burden on a Likert scale from 0 (“never”) to 4 (“nearly always”) points. Pearson's correlation coefficient between sZBI and ZBI was 0.92 (Kumamoto et al., 2004). Consistent with previously published reports, caregivers who scored Z 9 on the sZBI were deemed to have a clinically elevated burden, and a score Z 17 of the sZBI was thought to indicate a severe burden (Kobayashi, 2008). When the patient was living alone, the person who visited the patient every day was regarded as the chief caregiver and informant. Age, sex, and relationship to the patient were investigated.
2.4. Neuropsychological tests, behavioral symptoms, and activities of daily living ACE-R was developed to provide a brief test sensitive to early stage dementia (Yoshida et al., 2012). ACE-R includes MMSE, but extends it to encompass important areas not covered by MMSE, such as frontal-executive function and visuospatial skills. For this study, we used the Japanese version of ACE-R described
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by Yoshida et al. (2012). ACE-R has five subdomains, namely attention, language, word fluency, memory, and visuospatial cognition. WMS-R is most widely used scale of adult memory in Japan (Sugishita, 2001). In this study, the general memory and delayed recall scores were used. The mean value of both scores is 100, and a higher score indicates a better memory. The FAB consists of six items, and the score on each item ranges from 0 to 3. A lower score indicates a greater degree of executive dysfunction (Kugo et al., 2007). The NPI is a valid and reliable instrument for measuring behavior in dementia (Hirono et al., 1997). It is a caregiver-based tool that assesses 10 common behaviors in dementia. The Barthel Index comprises 10 items that measure a person's daily functioning, specifically the basic activities of daily (ADL) living and mobility (Wade and Collin, 1998). The total Barthel Index score ranges from 0 to 100, and a higher score indicates a better performance. The FAQ measures instrumental ADL of older adults using the patient's family member as an informant (Pfeffer et al., 1982). The FAQ consists of 10 items, and the score on each item ranges from 0 to 3. A higher score indicates more severe impairment. The NPI, Barthel Index, and FAQ were rated by a clinical psychologist specialized in geriatric psychiatry using the caregiver interview.
2.5. Statistics Statistical analysis was performed using the SPSS 19.0J software program (SPSS Inc., Chicago, IL). In this study, we chose a sample size such that the probability level is 0.05 and statistical power level is 0.8. Fisher et al. (2011) reported that the effect size of the mean difference in emotional strain between caregivers for patients with cognitive impairment, not dementia (CIND), and dementia was almost 0.50. Therefore, to detect the difference in effect size (d¼ 0.50) of the caregiver burden between for AD and for aMCI, we needed at least 64 cases in each group. The correlations of sZBI scores to age, duration of disease, education, number of relatives living together, age of the caregiver, five subscales of ACE-R, general memory and delayed memory of WMS-R, FAB scores, NPI scores, Barthel Index scores, and FAQ scores were examined by Pearson's correlation coefficient. To identify which variables were significantly correlated with caregiver burden, we performed a multiple linear regression using sZBI scores as a dependent variable. Independent variables were gender, age, duration of disease, education, presence or absence of anti-dementia medicine, number of relatives living together, gender of caregiver, age of caregiver, relationship of caregivers to patient (spouse¼1, other¼ 0), five subscale scores of ACE-R, general memory and delayed recall scores of WMS-R, FAB scores, NPI scores, Barthel Index scores, and FAQ scores. Subsequently, forward stepwise linear regression models (entrance criterion p¼0.05, exit p¼0.10) determined if disparate predictors accounted for unique additive variance in the caregiver burden. In multiple regression analysis, two dummy variables were used instead of “Relationship of caregiver” (nominal scale). One dummy variable consisted of spouse¼1 and other¼ 0. The other consisted of child¼ 1 and other¼0. The significance for the hypothesis testing analyses was set at po0.05.
3. Results 3.1. Participants Demographic characteristics of participants are shown in Table 1. There were 85 patients with aMCI (CDR score 0.5) and 106 patients
Table 1 Demographic characteristics of patients and caregivers. Patients
aMCI
AD
t
p
n Gender, % female (n) Age in years, M 7 S.D. (range) Duration of disease (months), M7 S.D. (range) Education (years), M 7S.D. (range) Numbers of relatives living together, M 7S.D. (range) Medication, % positive (n)
85 50.6 (43) 74.7 7 8.1 29.0 7 19.5 11.4 7 2.7 1.95 7 1.60 24.7 (21)
106 68.9 (73) 76.1 77.0 34.6 7 22.3 10.8 7 2.6 1.50 7 1.40 43.4 (46)
6.610# 1.347 1.839 1.386 2.081 7.236#
0.010 0.180 0.068 0.167 0.039 0.007
Chi
p
0.164 1.377
0.870 0.502
Caregivers Gender, % female (n) Age in years, M 7 S.D. (range) Relationship Spouse, % (n) Child, % (n) Other relatives, % (n)
63.17 12.9
63.4 7 14.5
60.0 (51) 34.1 (29) 5.9 (5)
54.7 (58) 34.9 (37) 10.4 (11)
aMCI, amnestic mild cognitive impairment; AD, Alzheimer's disease. n, number; M, mean; S.D., standard deviation; Chi, chi-square; #, chi-square.
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Table 2 Neuropsychological tests, behavioral symptoms and ADL.
Table 3 Caregiver burden, Zarit Burden Interview (ZBI).
Test (full score)
aMCI
AD
t
p
ZBI, total score, M 7S.D. (range)
aMCI
AD
Zarit Personal strain Role strain MMSE (30) ACE-R (100) Attention (18) Memory (26) Word fluency (14) Language (26) Visuospatial (16) WMS-R (mean value is 100) General memory Delayed recall FAB (18) NPI (120) FAQ (30)
5.3 7 4.7 4.2 7 3.2 1.2 7 1.8 25.4 7 2.1 79.17 6.0 16.3 7 1.4 15.17 4.5 8.6 7 2.5 24.07 1.8 15.0 7 1.4
7.8 7 5.5 5.9 7 3.6 1.9 7 2.5 20.3 7 3.6 61.2 7 11.1 12.8 7 2.8 8.4 7 4.0 6.0 7 2.8 21.17 4.0 12.9 7 2.9
3.230 3.442 2.212 11.599 13.423 10.478 10.892 6.727 6.352 6.344
0.001 0.001 0.028 o0.001 o0.001 o0.001 o0.001 o0.001 o0.001 o0.001
14.1 65.9 15.3 4.7
(12) (56) (13) (4)
4.7 59.5 28.3 7.5
(5) (63) (30) (8)
14.1 54.1 28.2 3.5
(12) (46) (24) (3)
4.7 44.3 38.7 12.3
(5) (47) (41) (13)
77.6 7 11.3 71.7 7 12.9 13.0 7 2.4 3.5 7 5.1 5.9 7 4.4
62.7 7 11.5 56.6 7 7.5 10.3 7 2.8 6.4 7 7.1 13.8 7 7.4
8.924 10.141 7.274 3.219 8.758
o0.001 o0.001 o0.001 0.002 o0.001
0, % (n) 1–8, % (n) 9–16, % (n) 17–, % (n) ZBI, personal strain, M 7 S.D. (range) 0, % (n) 1–5, % (n) 6–10, % (n) 11–, % (n) ZBI, role strain, M 7 S.D. (range) 0, % (n) 1–3, % (n) 4–6, % (n) 7–, % (n)
55.3 32.9 9.4 2.4
(47) (28) (8) (2)
35.8 47.2 11.3 5.7
(38) (50) (12) (6)
aMCI, amnestic mild cognitive impairment; AD, Alzheimer's disease. ADL, activities of daily living ; MMSE, Mini Mental State Examination. ACE-R, Addenbrooke's cognitive impairment; WMS-R, revised Memory Scale. FAB, Frontal Assessment Battery; NPI, Neuropsychiatric Inventory. FAQ, Functional Assessment Questionnaire.
aMCI, amnestic mild cognitive impairment; AD, Alzheimer's disease. M, mean; S.D., standard deviation; ZBI, total score, eight items. ZBI, personal strain, five items; ZBI, role strain, three items.
Wechsler
with mild AD (CDR score 0.5 or 1). The percentages of patients who were living alone were 10.6% (n¼9) with aMCI and 14.2% (n¼15) with mild AD. Patients taking anti-dementia medicine were 24.7% (n¼21) in aMCI and 43.4% (n¼46) in mild AD. Results of neuropsychological tests are shown in Table 2. All caregiver burden scores, cognitive test scores, and scores of neuropsychiatric symptoms or activities of daily living of patients with aMCI were significantly different from those of patients with mild AD. 3.2. Caregiver burden A number of caregivers with a sZBI total score Z 9 or Z17 were 17 (20%) and 4 (4.7%), respectively, for aMCI, and 38 (35.8%) and 8 (7.5%), respectively, for mild AD (Table 3). Correlation analysis revealed a significant correlation of sZBI total scores to NPI total scores (r ¼0.588, p o0.001), ACE-R memory score (r ¼ 0.266, p ¼0.014), age of caregivers (r ¼ 0.264, p¼ 0.015), ACE-R visuospatial score (r ¼ 0.241, p ¼0.026), and FAQ scores (r ¼0.237, p ¼0.029) among patients with aMCI. Similar analysis revealed a significant correlation of sZBI total scores to NPI total scores (r ¼0.366, p o0.001), Barthel score (r ¼ 0.362, p o0.001), FAQ score (r ¼0.321, p¼ 0.001), and disease duration (r ¼0.64, p ¼0.006) among patients with mild AD. The multiple linear regression analysis showed that the sZBI scores of patients with aMCI were predicted by NPI scores and ACE-R memory scores according to the following formula: the sZBI score¼0.514 (NPI score) 0.169 (ACE-R memory score) þ16.921 (Table 4). The sZBI scores of patients with mild AD were predicted by NPI and FAQ scores: the scores of sZBI ¼0.248 (NPI score) þ 0.198 (FAQ score) þ3.450 (Table 4).
4. Discussion We showed here two significant findings. One is that the caregiver burden in mild AD is more severe than that in aMCI. The other is that major determinant of the caregiver burden was the same in both aMCI and AD, but that somewhat different factors additionally affect the caregiver burden in aMCI and AD. These results are mostly in the expected directions.
Table 4 Stepwise multiple regression analysis of ZBI scores.
aMCI
AD
Variable
B
SE
Constant NPI ACE-R memory Constant NPI FAQ
16.921 0.514 0.169 3.450 0.248 0.198
5.548 0.082 0.069 1.066 0.069 0.067
Beta
0.551 0.214 0.320 0.265
t Value
p Value
3.050 6.294 2.440 3.238 3.580 2.969
0.003 o0.001 0.017 0.002 0.001 0.004
VIF
1.008 1.008 1.031 1.031
aMCI, amnestic mild cognitive impairment; AD, Alzheimer's disease; ZBI, Zarit Burden Interview. NPI, Neuropsychiatric Inventory; FAQ, Functional Assessment Questionnaire. ACE-R, revised Addenbrooke's Cognitive Examination; VIF, Variance Inflation Factor. Adjusted R2, 0.377 in aMCI and 0.187 in AD.
Generally, psychotic symptoms paired with poor instrumental activities of daily living (IADL) functioning generate the greatest burden, while cognitive dysfunction does not significantly influence the burden in dementia including AD (Yeager et al., 2010). Our results that behavioral symptoms and IADL dysfunction significantly were related to caregiver burden in mild AD are in line with those reports. Behavioral symptoms are also reported to be factors predicting the caregiver burden of patients with MCI (Seeher et al., 2013). This is congruent with the results of this report. However, it is more difficult to determine the reason why memory disturbance is significantly related to caregiver burden in aMCI patients. It is reported that AD caregivers reported difficulty functioning, whereas MCI caregivers focused on themes of “missing the person” once they knew (Garand et al., 2012). Repeated questions may indicate an initial but severe manifestation of personality destruction to relative caregivers. Subjects with a decline in memory function often show repetitive questioning (Ornstein and Gaugler, 2012). However, the NPI scale does not include repetitive or stereotypical behavior (Hirono et al., 1997). Therefore, as stated in our previous report, it is possible that neuropsychiatric symptoms not measured by the NPI, such as repetitive questioning behavior, may contribute to the caregiver burden among caregivers of aMCI subjects (Hayashi et al., 2013). To ameliorate memory dysfunction and decrease the caregiver burden, it may be useful to prescribe cholinesterase inhibitors for patients in the MCI stage. There have been few studies focusing on the patient with mild AD and aMCI. Gallagher et al. (2011) studied 100 caregivers of
C. Ikeda et al. / Psychiatry Research 226 (2015) 242–246
patients with AD or MCI. They reported that functional decline and dependence were most predictive of caregiver burden in patients with mild impairment, while behavioral symptoms were most predictive in patients with moderate to severe disease (Gallagher et al., 2011). However, patients were divided into two groups according to MMSE scores, namely MMSE scores 420 and r20 groups. Because the group of subjects with the MMSE score 420 included both MCI and AD patients, they did not compare the difference between caregivers of MCI and AD patients. Ryan et al. (2012) studied 135 participants (40 MCI, 55 AD, 40 normal controls) and their caregivers. MCI caregivers showed similar levels of emotional, physical, and social stress as the AD caregivers (Ryan et al., 2012). The caregiver burden was related to the neuropsychiatric symptoms and executive functioning of the patients among MCI caregivers and to neuropsychiatric symptoms, visual memory, and IADL of the patients among AD caregivers (Ryan et al., 2012). These risk factors reported by Ryan et al. are roughly in line with the factors in this study. However, they used only correlation analysis and did not perform multiple regression analysis. Therefore, if a significant relationship between those risk factors was present, we cannot identify the exact contribution of each factor to caregiver burden. Fisher et al. (2011) evaluated 49 caregivers of patients with cognitive impairment, not dementia (CIND) and 120 dementia caregivers as well as patients. Depressive symptoms are more frequent in dementia caregivers than in CIND caregivers (44% versus 26.5%) (Fisher et al., 2011). In both the studies of Fisher et al. and ours, behavioral symptoms were the most important predictors of caregiver strain in both groups. However, in Fisher's study IADL disturbances affect caregiver strain in CIND patients, while in our study IADL disturbances affected the caregiver burden with mild AD patients. The study of Fisher et al. was a communitybased study, whereas our study is a clinic-based study. The mean MMSE score of CIND patients in Fisher's study is similar to that of aMCI patients in this study (25.5 in CIND patients of Fisher's study and 25.4 in aMCI patients of this study). However, the mean MMSE score of dementia in Fisher's study is lower than that of mild AD in our study (15.4 in dementia of Fisher's study and 20.3 in mild AD of this study). The differences in research settings and disease severity may cause the difference in the results of the two studies. This study has some limitations. First, our study had a crosssectional design. Therefore, it limits any conclusions regarding the causal or predictive direction. Second, subjects in this study consisted of patients at only one memory clinic at a university hospital. Those who want to receive detailed examinations, including neuroimaging, are apt to come to our clinic. Therefore, selection bias may affect the results. Third, our study did not include characteristics of caregivers such as caregivers' emotional well-being, educational level, employment, coping style, and household income. It is certainly possible that such caregiver characteristics affect the perceived burden (Zucchella et al., 2012). The severity of dementia affected the caregiver burden, even in cases with mild impairment, although somewhat different factors contribute to the burden at different stages. We should always keep the caregiver burden in mind when we diagnose patients with aMCI or AD, and pay attention to different factors for evaluating and reducing the caregiver burden in aMCI and AD. Moreover, even in the MCI stage, the caregiver burden was substantial levels. We should consider caregivers with the responsibility of caring for patients, even in the MCI stage.
Acknowledgements We thank Ms. Horiuchi, Ms. Imai, Ms. Yabe, Ms. Tsuchiyama, and Ms. Fukushima for their skillful assistance for this study. This
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work was supported by a Grant from the Japanese Ministry of Education, Culture, Sports, Science and Technology (21591517), and the Zikei Institute of Psychiatry.
References Arai, Y., Zarit, S.H., 2011. Exploring strategies to alleviate caregiver burden: effects of the National Long-Term Care insurance scheme in Japan. Psychogeriatrics 11, 183–189. http://dx.doi.org/10.1111/j.1479-8301.2011.00367.x. Chan, S.W., 2010. Family caregiving in dementia: the Asian perspective of a global problem. Dementia and Geriatric Cognitive Disorders 30, 469–478. http://dx. doi.org/10.1159/000322086. Fisher, G.G., Franks, M.M., Plassman, B.L., Brown, S.L., Potter, G.G., Llewellyn, D., Rogers, M.A., Langa, K.M., 2011. Caring for individuals with dementia and cognitive impairment, not dementia: findings from the aging, demographics, and memory study. Journal of the American Geriatric Society 59, 488–494. http://dx.doi.org/10.1111/j.1532-5415.2010.03304.x. Folstein, M.F., Folstein, S.E., McHugh, P.R., 1975. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatry Research 12, 189–198. Gallagher, D., Ni Mhaolain, A., Crosby, L., Ryan, D., Lacey, L., Coen, R.F., Walsh, C., Coakley, D., Walsh, J.B., Cunningham, C., Lawlor, B.A., 2011. Dependence and caregiver burden in Alzheimer's disease and mild cognitive impairment. American Journal of Alzheimer's Disease and Other Dementias 26, 110–114. http://dx.doi.org/10.1177/1533317510394649. Garand, L., Lingler, J.H., Deardorf, K.E., DeKosky, S.T., Schulz, R., Reynolds 3rd, C.F., Dew, M.A., 2012. Anticipatory grief in new family caregivers of persons with mild cognitive impairment and dementia. Alzheimer Disease and Associated Disorders 26, 159–165. http://dx.doi.org/10.1097/WAD.0b013e31822f9051. Guerra-Silla, M.G., Gutiérrez-Robledo, L.M., Villalpando-Berumen, J.M., PérezZepeda, M.U., Montaña-Álvarez, M., Reyes-Guerrero, J., Rosas-Carrasco, Ó., 2011. Psychometric evaluation of a Spanish language version of the Screen for Caregiver Burden (SCB) in caregivers of patients with mixed, vascular and Alzheimer's dementia. Journal of Clinical Nursing 20, 3443–3451. http://dx.doi. org/10.1111/j.1365-2702.2010.03658.x. Hayashi, S., Terada, S., Nagao, S., Ikeda, C., Shindo, A., Oshima, E., Yokota, O., Uchitomi, Y., 2013. Burden of caregivers for patients with mild cognitive impairment in Japan. International Psychogeriatrics 25, 1357–1363. http://dx. doi.org/10.1017/S1041610213000537. Hirono, N., Mori, E., Ikejiri, Y., Imamura, T., Shimomura, T., Hashimoto, M., Yamashita, H., Ikeda, M., 1997. Japanese version of the Neuropsychiatric Inventory—a scoring system for neuropsychiatric disturbance in dementia patients. No To Shinkei 49, 266–271 (in Japanese). Kobayashi, Y., 2008. Evaluation of needs for consultation of caregivers of patients with dementia. Ronen Seishin Igaku Zasshi 19, 681–686 (in Japanese). Kugo, A., Terada, S., Ata, T., Ido, Y., Kado, Y., Ishihara, T., Hikiji, M., Fujisawa, Y., Sasaki, K., Kuroda, S., 2007. Japanese version of the Frontal Assessment Battery for dementia. Psychiatry Research 153, 69–75. http://dx.doi.org/10.1016/j. psychres.2006.04.004. Kumamoto, K., Arai, Y., Ueda, T., Washio, M., 2004. Cross-validation of the short version of the Japanese version of the Zarit Caregiver Burden Interview (J-ZBI 8). Nihon Ronen Igakkai Zasshi 41, 204–210. McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., Stadlan, E.M., 1984. Clinical diagnosis of Alzheimer's disease: report of the NINCDS–ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's disease. Neurology 34, 939–944. McLaughlin, P.M., Wright, M.J., Larocca, M., Nguyen, P.T., Teng, E., Apostolova, L.G., Ringman, J.M., Zhou, Y., Cummings, J.L., Woo, E., 2014. The “Alzheimer's type” profile of semantic clustering in amnestic mild cognitive impairment. Journal of the International Neuropsychological Society 20, 1–11. http://dx.doi.org/ 10.1017/S135561771400006X. Ornstein, K., Gaugler, J.E., 2012. The problem with “problem behaviors”: a systematic review of the association between individual patient behavioral and psychological symptoms and caregiver depression and burden within the dementia patient–caregiver dyad. International Psychogeriatrics 24, 1536–1552. http://dx. doi.org/10.1017/S1041610212000737. Papastavrou, E., Kalokerinou, A., Papacostas, S.S., Tsangari, H., Sourtzi, P., 2007. Caring for a relative with dementia: family caregiver burden. Journal of Advanced Nursing 58, 446–457. http://dx.doi.org/10.1111/j.1365-2648.2007.04250.x. Pfeffer, R.I., Kurosaki, T.T., Harrah Jr., C.H., Chance, J.M., Filos, S., 1982. Measurement of the functional activities in older adults in the community. Journal of Gerontology 37, 323–329. Ryan, K.A., Weldon, A., Huby, N.M., Persad, C., Bhaumik, A.K., Heidebrink, J.L., Barbas, N., Staffend, N., Franti, L., Giordani, B., 2010. Caregiver support service needs for patients with mild cognitive impairment and Alzheimer disease. Alzheimer Disease and Associated Disorders 24, 171–176. http://dx.doi.org/ 10.1097/WAD.0b013e3181aba90d. Ryan, K.A., Weldon, A., Persad, C., Heidebrink, J.L., Barbas, N., Giordani, B., 2012. Neuropsychiatric symptoms and executive functioning in patients with mild cognitive impairment: relationship to caregiver burden. Dementia and Geriatric Cognitive Disorders 34, 206–215. http://dx.doi.org/10.1159/000339955. Seeher, K., Low, L.F., Reppermund, S., Brodaty, H., 2013. Predictors and outcomes for caregivers of people with mild cognitive impairment: a systematic literature
246
C. Ikeda et al. / Psychiatry Research 226 (2015) 242–246
review. Alzheimer's & Dementia 9, 346–355. http://dx.doi.org/10.1016/j. jalz.2012.01.012. Sugishita, M., 2001. Japanese Wechsler Memory Scale-Revised. Nihon-bunkakagakusha, Tokyo (in Japanese). Wade, D.T., Collin, C., 1998. The Barthel ADL Index: a standard measure of physical disability? International Disability Studies 10, 64–67. Ward, A., Tardiff, S., Dye, C., Arrighi, H.M., 2013. Rate of conversion from prodromal Alzheimer's disease to Alzheimer's dementia: a systematic review of the literature. Dementia and Geriatric Cognitive Disorders Extra 3, 320–332 http://dx.doi.org/10.1159/000354370. Whitebird, R.R., Kreitzer, M., Crain, A.L., Lewis, B.A., Hanson, L.R., Enstad, C.J., 2013. Mindfulness-based stress reduction for family caregivers: a randomized controlled trial. Gerontologist 53, 676–686. http://dx.doi.org/10.1093/geront/ gns126.
Yeager, C.A., Hyer, L.A., Hobbs, B., Coyne, A.C., 2010. Alzheimer's disease and vascular dementia: the complex relationship between diagnosis and caregiver burden. Issues in Mental Health Nursing 31, 376–384. http://dx.doi.org/ 10.3109/01612840903434589. Yoshida, H., Terada, S., Honda, H., Kishimoto, Y., Takeda, N., Oshima, E., Hirayama, K., Yokota, O., Uchitomi, Y., 2012. Validation of the revised Addenbrooke's Cognitive Examination (ACE-R) for detecting mild cognitive impairment and dementia in a Japanese population. International Psychogeriatrics 24, 28–37. http://dx.doi.org/10.1017/S1041610211001190. Zucchella, C., Bartolo, M., Pasotti, C., Chiapella, L., Sinforiani, E., 2012. Caregiver burden and coping in early-stage Alzheimer disease. Alzheimer Disease & Associated Disorders 26, 55–60. http://dx.doi.org/10.1097/WAD.0b013e31821aa6de.
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Difference in determinants of caregiver burden between amnestic mild cognitive impairment and mild Alzheimer's disease Chikako Ikeda, Seishi Terada n, Etsuko Oshima, Satoshi Hayashi, Yuko Okahisa, Manabu Takaki, Masatoshi Inagaki, Osamu Yokota, Yosuke Uchitomi Department of Neuropsychiatry, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama, Japan
art ic l e i nf o
a b s t r a c t
Article history: Received 8 April 2014 Received in revised form 24 August 2014 Accepted 27 December 2014 Available online 13 January 2015
Care for the disabled elderly can be stressful and exhausting, especially in cases of dementia. There have been a number of studies on the dementia caregiver burden, but studies focusing on differences by stages of the disease are rare. The caregiver burden of 85 caregivers of patients with amnestic mild cognitive impairment (aMCI) and 106 caregivers of patients with mild Alzheimer's disease (AD) was evaluated by the short version of the Japanese version of the Zarit Burden Interview (sZBI). The caregiver burden in mild AD was more severe than that in aMCI. In mild AD, the risk factors of caregiver burden were neurobehavioral symptoms and disturbances instrumental activities of daily living (IADL), whereas the risk factors in aMCI were neurobehavioral symptoms and memory dysfunction. The severity of dementing disease affects the caregiver burden, and somewhat different factors contribute to the burden at different stages. We should pay attention to different factors in evaluating and reducing the caregiver burden in aMCI and mild AD. & 2015 Elsevier Ireland Ltd. All rights reserved.
Keywords: Alzheimer's disease Caregiver Caregiver burden Mild cognitive impairment Zarit Burden Interview
1. Introduction Few tasks are more challenging than caring for a family member with dementia (Whitebird et al., 2013). Caregivers of patients with dementia experience a greater burden than those caring for non-demented patients (Guerra-Silla et al., 2011). As a result, family caregivers may experience significant mental health problems, as well as a deterioration of their own physical health (Hayashi et al., 2013). Thus, alleviation of the caregiver burden has become a primary public health goal (Arai and Zarit, 2011). Among dementing disorders, Alzheimer's disease (AD) is the leading cause of late-onset dementia worldwide, and among caregivers of AD patients, 68% were highly burdened and 65% exhibited depressive symptoms (Papastavrou et al., 2007). In addition, the problem of the family burden of caring for persons with AD is a common challenge in both developed and developing countries (Chan, 2010). Amnestic mild cognitive impairment (aMCI) is a risk state for AD that is characterized by a deficit in memory with preserved daily functioning (McLaughlin et al., 2014). The annualized conversion rates of aMCI to AD ranged from 11% to 16.5% for studies recruiting from clinics and from 7.4% to 8.9% for community samples (Ward et al.,
2013). Caregivers of patients with aMCI were reported to already experience a need for increased services comparable to those of individuals caring for AD patients (Ryan et al., 2010). It is plausible that in different stages of dementing diseases, the degree of the burden is different and that different factors influence the caregiver burden. However, there have been only a few studies comparing the burden of caregivers for dementia and aMCI patients. Based on previous research including our own (Gallagher et al., 2011; Fisher et al., 2011; Hayashi et al., 2013), we anticipated that the caregiver burden of caregivers for AD patients is more severe than that of caregivers for aMCI patients. Moreover, little is known about whether the risk factors of caregiver burden for patients with aMCI are similar to those for patients with AD (Ryan et al., 2012). We postulated that similar risk factors contribute to caregiver burden of patients with AD and aMCI, but that inability to perform activities of daily (ADL) life may be important in more advanced stages of the disease.
2. Methods 2.1. Participants
n Correspondence to: Department of Neuropsychiatry, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences 2-5-1 Shikata-cho, Kita-ku, Okayama 700-8558, Japan. Tel.: þ81 86 235 7242; fax: þ 81 86 235 7246. E-mail address: [email protected] (S. Terada).
http://dx.doi.org/10.1016/j.psychres.2014.12.055 0165-1781/& 2015 Elsevier Ireland Ltd. All rights reserved.
Eighty five consecutive caregivers of subjects with aMCI and 106 consecutive caregivers of subjects with mild AD were recruited from the outpatient unit of the Memory Clinic of Okayama University Hospital between September 2008 and April 2012 according to the following criteria.
C. Ikeda et al. / Psychiatry Research 226 (2015) 242–246 Inclusion criteria for caregivers were (1) being the family caregiver of an outpatient with aMCI or mild AD, (2) living with the patient or visiting him or her daily, and (3) being cognitively intact. Exclusion criteria were (1) being unable to come to hospital with the patient, (2) having a history of mental illness or substance abuse, and (3) being treated with antipsychotics, antidepressants, or anxiolytic drugs. All patients (1) underwent general physical and neurological examinations and extensive laboratory testing, including thyroid function tests, serum vitamin B12, and syphilis serology; (2) had a global Clinical Dementia Rating (CDR) of 0.5 or 1; (3) took the Mini-Mental State Examination (MMSE) (Folstein et al., 1975), revised Addenbrooke's Cognitive Examination (ACE-R) (Yoshida et al., 2012), revised Wechsler Memory Scale (WMS-R) (Sugishita, 2001), Frontal Assessment Battery (FAB) (Kugo et al., 2007), Neuropsychiatric Inventory (NPI), Barthel Index, and Functional Assessment Questionnaire (FAQ). The aMCI patients all scored Z1.5 standard deviations (S.D.) below the population mean on at least one of three neuropsychological tests (ACE-R memory score, two subscales of WMS-R), and were diagnosed as not having dementia. Previously, we reported the caregiver burden of MCI patients including amnestic and non-amnestic types (n¼ 104). In this study, we examined aMCI only (n¼85). The AD patients were all diagnosed with probable AD according to the criteria formulated by the NINCDS– ADRDA (McKhann et al., 1984). The caregiver burden of AD patients at our clinic has never been reported. In this study, AD patients with a CDR score 0.5 or 1 were defined as patients with mild AD. The exclusion criteria of the patients were (1) complications from other neurological diseases or illnesses; (2) a history of mental illness or substance abuse prior to the onset of dementia; (3) any evidence of focal brain lesions on head MRI; and (4) treatment with antipsychotics, antidepressants or anxiolytic drugs.
2.2. Ethics This study protocol was approved by the committee on human research of Okayama University Hospital on human research. After giving a complete description of the study to the subjects and their relatives, written informed consent was obtained.
2.3. Caregiver assessment The caregiver burden was measured using the short version of the Japanese version of the Zarit Burden Interview (sZBI) (Kumamoto et al., 2004). The caregivers were asked to rate their burden on a Likert scale from 0 (“never”) to 4 (“nearly always”) points. Pearson's correlation coefficient between sZBI and ZBI was 0.92 (Kumamoto et al., 2004). Consistent with previously published reports, caregivers who scored Z 9 on the sZBI were deemed to have a clinically elevated burden, and a score Z 17 of the sZBI was thought to indicate a severe burden (Kobayashi, 2008). When the patient was living alone, the person who visited the patient every day was regarded as the chief caregiver and informant. Age, sex, and relationship to the patient were investigated.
2.4. Neuropsychological tests, behavioral symptoms, and activities of daily living ACE-R was developed to provide a brief test sensitive to early stage dementia (Yoshida et al., 2012). ACE-R includes MMSE, but extends it to encompass important areas not covered by MMSE, such as frontal-executive function and visuospatial skills. For this study, we used the Japanese version of ACE-R described
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by Yoshida et al. (2012). ACE-R has five subdomains, namely attention, language, word fluency, memory, and visuospatial cognition. WMS-R is most widely used scale of adult memory in Japan (Sugishita, 2001). In this study, the general memory and delayed recall scores were used. The mean value of both scores is 100, and a higher score indicates a better memory. The FAB consists of six items, and the score on each item ranges from 0 to 3. A lower score indicates a greater degree of executive dysfunction (Kugo et al., 2007). The NPI is a valid and reliable instrument for measuring behavior in dementia (Hirono et al., 1997). It is a caregiver-based tool that assesses 10 common behaviors in dementia. The Barthel Index comprises 10 items that measure a person's daily functioning, specifically the basic activities of daily (ADL) living and mobility (Wade and Collin, 1998). The total Barthel Index score ranges from 0 to 100, and a higher score indicates a better performance. The FAQ measures instrumental ADL of older adults using the patient's family member as an informant (Pfeffer et al., 1982). The FAQ consists of 10 items, and the score on each item ranges from 0 to 3. A higher score indicates more severe impairment. The NPI, Barthel Index, and FAQ were rated by a clinical psychologist specialized in geriatric psychiatry using the caregiver interview.
2.5. Statistics Statistical analysis was performed using the SPSS 19.0J software program (SPSS Inc., Chicago, IL). In this study, we chose a sample size such that the probability level is 0.05 and statistical power level is 0.8. Fisher et al. (2011) reported that the effect size of the mean difference in emotional strain between caregivers for patients with cognitive impairment, not dementia (CIND), and dementia was almost 0.50. Therefore, to detect the difference in effect size (d¼ 0.50) of the caregiver burden between for AD and for aMCI, we needed at least 64 cases in each group. The correlations of sZBI scores to age, duration of disease, education, number of relatives living together, age of the caregiver, five subscales of ACE-R, general memory and delayed memory of WMS-R, FAB scores, NPI scores, Barthel Index scores, and FAQ scores were examined by Pearson's correlation coefficient. To identify which variables were significantly correlated with caregiver burden, we performed a multiple linear regression using sZBI scores as a dependent variable. Independent variables were gender, age, duration of disease, education, presence or absence of anti-dementia medicine, number of relatives living together, gender of caregiver, age of caregiver, relationship of caregivers to patient (spouse¼1, other¼ 0), five subscale scores of ACE-R, general memory and delayed recall scores of WMS-R, FAB scores, NPI scores, Barthel Index scores, and FAQ scores. Subsequently, forward stepwise linear regression models (entrance criterion p¼0.05, exit p¼0.10) determined if disparate predictors accounted for unique additive variance in the caregiver burden. In multiple regression analysis, two dummy variables were used instead of “Relationship of caregiver” (nominal scale). One dummy variable consisted of spouse¼1 and other¼ 0. The other consisted of child¼ 1 and other¼0. The significance for the hypothesis testing analyses was set at po0.05.
3. Results 3.1. Participants Demographic characteristics of participants are shown in Table 1. There were 85 patients with aMCI (CDR score 0.5) and 106 patients
Table 1 Demographic characteristics of patients and caregivers. Patients
aMCI
AD
t
p
n Gender, % female (n) Age in years, M 7 S.D. (range) Duration of disease (months), M7 S.D. (range) Education (years), M 7S.D. (range) Numbers of relatives living together, M 7S.D. (range) Medication, % positive (n)
85 50.6 (43) 74.7 7 8.1 29.0 7 19.5 11.4 7 2.7 1.95 7 1.60 24.7 (21)
106 68.9 (73) 76.1 77.0 34.6 7 22.3 10.8 7 2.6 1.50 7 1.40 43.4 (46)
6.610# 1.347 1.839 1.386 2.081 7.236#
0.010 0.180 0.068 0.167 0.039 0.007
Chi
p
0.164 1.377
0.870 0.502
Caregivers Gender, % female (n) Age in years, M 7 S.D. (range) Relationship Spouse, % (n) Child, % (n) Other relatives, % (n)
63.17 12.9
63.4 7 14.5
60.0 (51) 34.1 (29) 5.9 (5)
54.7 (58) 34.9 (37) 10.4 (11)
aMCI, amnestic mild cognitive impairment; AD, Alzheimer's disease. n, number; M, mean; S.D., standard deviation; Chi, chi-square; #, chi-square.
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C. Ikeda et al. / Psychiatry Research 226 (2015) 242–246
Table 2 Neuropsychological tests, behavioral symptoms and ADL.
Table 3 Caregiver burden, Zarit Burden Interview (ZBI).
Test (full score)
aMCI
AD
t
p
ZBI, total score, M 7S.D. (range)
aMCI
AD
Zarit Personal strain Role strain MMSE (30) ACE-R (100) Attention (18) Memory (26) Word fluency (14) Language (26) Visuospatial (16) WMS-R (mean value is 100) General memory Delayed recall FAB (18) NPI (120) FAQ (30)
5.3 7 4.7 4.2 7 3.2 1.2 7 1.8 25.4 7 2.1 79.17 6.0 16.3 7 1.4 15.17 4.5 8.6 7 2.5 24.07 1.8 15.0 7 1.4
7.8 7 5.5 5.9 7 3.6 1.9 7 2.5 20.3 7 3.6 61.2 7 11.1 12.8 7 2.8 8.4 7 4.0 6.0 7 2.8 21.17 4.0 12.9 7 2.9
3.230 3.442 2.212 11.599 13.423 10.478 10.892 6.727 6.352 6.344
0.001 0.001 0.028 o0.001 o0.001 o0.001 o0.001 o0.001 o0.001 o0.001
14.1 65.9 15.3 4.7
(12) (56) (13) (4)
4.7 59.5 28.3 7.5
(5) (63) (30) (8)
14.1 54.1 28.2 3.5
(12) (46) (24) (3)
4.7 44.3 38.7 12.3
(5) (47) (41) (13)
77.6 7 11.3 71.7 7 12.9 13.0 7 2.4 3.5 7 5.1 5.9 7 4.4
62.7 7 11.5 56.6 7 7.5 10.3 7 2.8 6.4 7 7.1 13.8 7 7.4
8.924 10.141 7.274 3.219 8.758
o0.001 o0.001 o0.001 0.002 o0.001
0, % (n) 1–8, % (n) 9–16, % (n) 17–, % (n) ZBI, personal strain, M 7 S.D. (range) 0, % (n) 1–5, % (n) 6–10, % (n) 11–, % (n) ZBI, role strain, M 7 S.D. (range) 0, % (n) 1–3, % (n) 4–6, % (n) 7–, % (n)
55.3 32.9 9.4 2.4
(47) (28) (8) (2)
35.8 47.2 11.3 5.7
(38) (50) (12) (6)
aMCI, amnestic mild cognitive impairment; AD, Alzheimer's disease. ADL, activities of daily living ; MMSE, Mini Mental State Examination. ACE-R, Addenbrooke's cognitive impairment; WMS-R, revised Memory Scale. FAB, Frontal Assessment Battery; NPI, Neuropsychiatric Inventory. FAQ, Functional Assessment Questionnaire.
aMCI, amnestic mild cognitive impairment; AD, Alzheimer's disease. M, mean; S.D., standard deviation; ZBI, total score, eight items. ZBI, personal strain, five items; ZBI, role strain, three items.
Wechsler
with mild AD (CDR score 0.5 or 1). The percentages of patients who were living alone were 10.6% (n¼9) with aMCI and 14.2% (n¼15) with mild AD. Patients taking anti-dementia medicine were 24.7% (n¼21) in aMCI and 43.4% (n¼46) in mild AD. Results of neuropsychological tests are shown in Table 2. All caregiver burden scores, cognitive test scores, and scores of neuropsychiatric symptoms or activities of daily living of patients with aMCI were significantly different from those of patients with mild AD. 3.2. Caregiver burden A number of caregivers with a sZBI total score Z 9 or Z17 were 17 (20%) and 4 (4.7%), respectively, for aMCI, and 38 (35.8%) and 8 (7.5%), respectively, for mild AD (Table 3). Correlation analysis revealed a significant correlation of sZBI total scores to NPI total scores (r ¼0.588, p o0.001), ACE-R memory score (r ¼ 0.266, p ¼0.014), age of caregivers (r ¼ 0.264, p¼ 0.015), ACE-R visuospatial score (r ¼ 0.241, p ¼0.026), and FAQ scores (r ¼0.237, p ¼0.029) among patients with aMCI. Similar analysis revealed a significant correlation of sZBI total scores to NPI total scores (r ¼0.366, p o0.001), Barthel score (r ¼ 0.362, p o0.001), FAQ score (r ¼0.321, p¼ 0.001), and disease duration (r ¼0.64, p ¼0.006) among patients with mild AD. The multiple linear regression analysis showed that the sZBI scores of patients with aMCI were predicted by NPI scores and ACE-R memory scores according to the following formula: the sZBI score¼0.514 (NPI score) 0.169 (ACE-R memory score) þ16.921 (Table 4). The sZBI scores of patients with mild AD were predicted by NPI and FAQ scores: the scores of sZBI ¼0.248 (NPI score) þ 0.198 (FAQ score) þ3.450 (Table 4).
4. Discussion We showed here two significant findings. One is that the caregiver burden in mild AD is more severe than that in aMCI. The other is that major determinant of the caregiver burden was the same in both aMCI and AD, but that somewhat different factors additionally affect the caregiver burden in aMCI and AD. These results are mostly in the expected directions.
Table 4 Stepwise multiple regression analysis of ZBI scores.
aMCI
AD
Variable
B
SE
Constant NPI ACE-R memory Constant NPI FAQ
16.921 0.514 0.169 3.450 0.248 0.198
5.548 0.082 0.069 1.066 0.069 0.067
Beta
0.551 0.214 0.320 0.265
t Value
p Value
3.050 6.294 2.440 3.238 3.580 2.969
0.003 o0.001 0.017 0.002 0.001 0.004
VIF
1.008 1.008 1.031 1.031
aMCI, amnestic mild cognitive impairment; AD, Alzheimer's disease; ZBI, Zarit Burden Interview. NPI, Neuropsychiatric Inventory; FAQ, Functional Assessment Questionnaire. ACE-R, revised Addenbrooke's Cognitive Examination; VIF, Variance Inflation Factor. Adjusted R2, 0.377 in aMCI and 0.187 in AD.
Generally, psychotic symptoms paired with poor instrumental activities of daily living (IADL) functioning generate the greatest burden, while cognitive dysfunction does not significantly influence the burden in dementia including AD (Yeager et al., 2010). Our results that behavioral symptoms and IADL dysfunction significantly were related to caregiver burden in mild AD are in line with those reports. Behavioral symptoms are also reported to be factors predicting the caregiver burden of patients with MCI (Seeher et al., 2013). This is congruent with the results of this report. However, it is more difficult to determine the reason why memory disturbance is significantly related to caregiver burden in aMCI patients. It is reported that AD caregivers reported difficulty functioning, whereas MCI caregivers focused on themes of “missing the person” once they knew (Garand et al., 2012). Repeated questions may indicate an initial but severe manifestation of personality destruction to relative caregivers. Subjects with a decline in memory function often show repetitive questioning (Ornstein and Gaugler, 2012). However, the NPI scale does not include repetitive or stereotypical behavior (Hirono et al., 1997). Therefore, as stated in our previous report, it is possible that neuropsychiatric symptoms not measured by the NPI, such as repetitive questioning behavior, may contribute to the caregiver burden among caregivers of aMCI subjects (Hayashi et al., 2013). To ameliorate memory dysfunction and decrease the caregiver burden, it may be useful to prescribe cholinesterase inhibitors for patients in the MCI stage. There have been few studies focusing on the patient with mild AD and aMCI. Gallagher et al. (2011) studied 100 caregivers of
C. Ikeda et al. / Psychiatry Research 226 (2015) 242–246
patients with AD or MCI. They reported that functional decline and dependence were most predictive of caregiver burden in patients with mild impairment, while behavioral symptoms were most predictive in patients with moderate to severe disease (Gallagher et al., 2011). However, patients were divided into two groups according to MMSE scores, namely MMSE scores 420 and r20 groups. Because the group of subjects with the MMSE score 420 included both MCI and AD patients, they did not compare the difference between caregivers of MCI and AD patients. Ryan et al. (2012) studied 135 participants (40 MCI, 55 AD, 40 normal controls) and their caregivers. MCI caregivers showed similar levels of emotional, physical, and social stress as the AD caregivers (Ryan et al., 2012). The caregiver burden was related to the neuropsychiatric symptoms and executive functioning of the patients among MCI caregivers and to neuropsychiatric symptoms, visual memory, and IADL of the patients among AD caregivers (Ryan et al., 2012). These risk factors reported by Ryan et al. are roughly in line with the factors in this study. However, they used only correlation analysis and did not perform multiple regression analysis. Therefore, if a significant relationship between those risk factors was present, we cannot identify the exact contribution of each factor to caregiver burden. Fisher et al. (2011) evaluated 49 caregivers of patients with cognitive impairment, not dementia (CIND) and 120 dementia caregivers as well as patients. Depressive symptoms are more frequent in dementia caregivers than in CIND caregivers (44% versus 26.5%) (Fisher et al., 2011). In both the studies of Fisher et al. and ours, behavioral symptoms were the most important predictors of caregiver strain in both groups. However, in Fisher's study IADL disturbances affect caregiver strain in CIND patients, while in our study IADL disturbances affected the caregiver burden with mild AD patients. The study of Fisher et al. was a communitybased study, whereas our study is a clinic-based study. The mean MMSE score of CIND patients in Fisher's study is similar to that of aMCI patients in this study (25.5 in CIND patients of Fisher's study and 25.4 in aMCI patients of this study). However, the mean MMSE score of dementia in Fisher's study is lower than that of mild AD in our study (15.4 in dementia of Fisher's study and 20.3 in mild AD of this study). The differences in research settings and disease severity may cause the difference in the results of the two studies. This study has some limitations. First, our study had a crosssectional design. Therefore, it limits any conclusions regarding the causal or predictive direction. Second, subjects in this study consisted of patients at only one memory clinic at a university hospital. Those who want to receive detailed examinations, including neuroimaging, are apt to come to our clinic. Therefore, selection bias may affect the results. Third, our study did not include characteristics of caregivers such as caregivers' emotional well-being, educational level, employment, coping style, and household income. It is certainly possible that such caregiver characteristics affect the perceived burden (Zucchella et al., 2012). The severity of dementia affected the caregiver burden, even in cases with mild impairment, although somewhat different factors contribute to the burden at different stages. We should always keep the caregiver burden in mind when we diagnose patients with aMCI or AD, and pay attention to different factors for evaluating and reducing the caregiver burden in aMCI and AD. Moreover, even in the MCI stage, the caregiver burden was substantial levels. We should consider caregivers with the responsibility of caring for patients, even in the MCI stage.
Acknowledgements We thank Ms. Horiuchi, Ms. Imai, Ms. Yabe, Ms. Tsuchiyama, and Ms. Fukushima for their skillful assistance for this study. This
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work was supported by a Grant from the Japanese Ministry of Education, Culture, Sports, Science and Technology (21591517), and the Zikei Institute of Psychiatry.
References Arai, Y., Zarit, S.H., 2011. Exploring strategies to alleviate caregiver burden: effects of the National Long-Term Care insurance scheme in Japan. Psychogeriatrics 11, 183–189. http://dx.doi.org/10.1111/j.1479-8301.2011.00367.x. Chan, S.W., 2010. Family caregiving in dementia: the Asian perspective of a global problem. Dementia and Geriatric Cognitive Disorders 30, 469–478. http://dx. doi.org/10.1159/000322086. Fisher, G.G., Franks, M.M., Plassman, B.L., Brown, S.L., Potter, G.G., Llewellyn, D., Rogers, M.A., Langa, K.M., 2011. Caring for individuals with dementia and cognitive impairment, not dementia: findings from the aging, demographics, and memory study. Journal of the American Geriatric Society 59, 488–494. http://dx.doi.org/10.1111/j.1532-5415.2010.03304.x. Folstein, M.F., Folstein, S.E., McHugh, P.R., 1975. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatry Research 12, 189–198. Gallagher, D., Ni Mhaolain, A., Crosby, L., Ryan, D., Lacey, L., Coen, R.F., Walsh, C., Coakley, D., Walsh, J.B., Cunningham, C., Lawlor, B.A., 2011. Dependence and caregiver burden in Alzheimer's disease and mild cognitive impairment. American Journal of Alzheimer's Disease and Other Dementias 26, 110–114. http://dx.doi.org/10.1177/1533317510394649. Garand, L., Lingler, J.H., Deardorf, K.E., DeKosky, S.T., Schulz, R., Reynolds 3rd, C.F., Dew, M.A., 2012. Anticipatory grief in new family caregivers of persons with mild cognitive impairment and dementia. Alzheimer Disease and Associated Disorders 26, 159–165. http://dx.doi.org/10.1097/WAD.0b013e31822f9051. Guerra-Silla, M.G., Gutiérrez-Robledo, L.M., Villalpando-Berumen, J.M., PérezZepeda, M.U., Montaña-Álvarez, M., Reyes-Guerrero, J., Rosas-Carrasco, Ó., 2011. Psychometric evaluation of a Spanish language version of the Screen for Caregiver Burden (SCB) in caregivers of patients with mixed, vascular and Alzheimer's dementia. Journal of Clinical Nursing 20, 3443–3451. http://dx.doi. org/10.1111/j.1365-2702.2010.03658.x. Hayashi, S., Terada, S., Nagao, S., Ikeda, C., Shindo, A., Oshima, E., Yokota, O., Uchitomi, Y., 2013. Burden of caregivers for patients with mild cognitive impairment in Japan. International Psychogeriatrics 25, 1357–1363. http://dx. doi.org/10.1017/S1041610213000537. Hirono, N., Mori, E., Ikejiri, Y., Imamura, T., Shimomura, T., Hashimoto, M., Yamashita, H., Ikeda, M., 1997. Japanese version of the Neuropsychiatric Inventory—a scoring system for neuropsychiatric disturbance in dementia patients. No To Shinkei 49, 266–271 (in Japanese). Kobayashi, Y., 2008. Evaluation of needs for consultation of caregivers of patients with dementia. Ronen Seishin Igaku Zasshi 19, 681–686 (in Japanese). Kugo, A., Terada, S., Ata, T., Ido, Y., Kado, Y., Ishihara, T., Hikiji, M., Fujisawa, Y., Sasaki, K., Kuroda, S., 2007. Japanese version of the Frontal Assessment Battery for dementia. Psychiatry Research 153, 69–75. http://dx.doi.org/10.1016/j. psychres.2006.04.004. Kumamoto, K., Arai, Y., Ueda, T., Washio, M., 2004. Cross-validation of the short version of the Japanese version of the Zarit Caregiver Burden Interview (J-ZBI 8). Nihon Ronen Igakkai Zasshi 41, 204–210. McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., Stadlan, E.M., 1984. Clinical diagnosis of Alzheimer's disease: report of the NINCDS–ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's disease. Neurology 34, 939–944. McLaughlin, P.M., Wright, M.J., Larocca, M., Nguyen, P.T., Teng, E., Apostolova, L.G., Ringman, J.M., Zhou, Y., Cummings, J.L., Woo, E., 2014. The “Alzheimer's type” profile of semantic clustering in amnestic mild cognitive impairment. Journal of the International Neuropsychological Society 20, 1–11. http://dx.doi.org/ 10.1017/S135561771400006X. Ornstein, K., Gaugler, J.E., 2012. The problem with “problem behaviors”: a systematic review of the association between individual patient behavioral and psychological symptoms and caregiver depression and burden within the dementia patient–caregiver dyad. International Psychogeriatrics 24, 1536–1552. http://dx. doi.org/10.1017/S1041610212000737. Papastavrou, E., Kalokerinou, A., Papacostas, S.S., Tsangari, H., Sourtzi, P., 2007. Caring for a relative with dementia: family caregiver burden. Journal of Advanced Nursing 58, 446–457. http://dx.doi.org/10.1111/j.1365-2648.2007.04250.x. Pfeffer, R.I., Kurosaki, T.T., Harrah Jr., C.H., Chance, J.M., Filos, S., 1982. Measurement of the functional activities in older adults in the community. Journal of Gerontology 37, 323–329. Ryan, K.A., Weldon, A., Huby, N.M., Persad, C., Bhaumik, A.K., Heidebrink, J.L., Barbas, N., Staffend, N., Franti, L., Giordani, B., 2010. Caregiver support service needs for patients with mild cognitive impairment and Alzheimer disease. Alzheimer Disease and Associated Disorders 24, 171–176. http://dx.doi.org/ 10.1097/WAD.0b013e3181aba90d. Ryan, K.A., Weldon, A., Persad, C., Heidebrink, J.L., Barbas, N., Giordani, B., 2012. Neuropsychiatric symptoms and executive functioning in patients with mild cognitive impairment: relationship to caregiver burden. Dementia and Geriatric Cognitive Disorders 34, 206–215. http://dx.doi.org/10.1159/000339955. Seeher, K., Low, L.F., Reppermund, S., Brodaty, H., 2013. Predictors and outcomes for caregivers of people with mild cognitive impairment: a systematic literature
246
C. Ikeda et al. / Psychiatry Research 226 (2015) 242–246
review. Alzheimer's & Dementia 9, 346–355. http://dx.doi.org/10.1016/j. jalz.2012.01.012. Sugishita, M., 2001. Japanese Wechsler Memory Scale-Revised. Nihon-bunkakagakusha, Tokyo (in Japanese). Wade, D.T., Collin, C., 1998. The Barthel ADL Index: a standard measure of physical disability? International Disability Studies 10, 64–67. Ward, A., Tardiff, S., Dye, C., Arrighi, H.M., 2013. Rate of conversion from prodromal Alzheimer's disease to Alzheimer's dementia: a systematic review of the literature. Dementia and Geriatric Cognitive Disorders Extra 3, 320–332 http://dx.doi.org/10.1159/000354370. Whitebird, R.R., Kreitzer, M., Crain, A.L., Lewis, B.A., Hanson, L.R., Enstad, C.J., 2013. Mindfulness-based stress reduction for family caregivers: a randomized controlled trial. Gerontologist 53, 676–686. http://dx.doi.org/10.1093/geront/ gns126.
Yeager, C.A., Hyer, L.A., Hobbs, B., Coyne, A.C., 2010. Alzheimer's disease and vascular dementia: the complex relationship between diagnosis and caregiver burden. Issues in Mental Health Nursing 31, 376–384. http://dx.doi.org/ 10.3109/01612840903434589. Yoshida, H., Terada, S., Honda, H., Kishimoto, Y., Takeda, N., Oshima, E., Hirayama, K., Yokota, O., Uchitomi, Y., 2012. Validation of the revised Addenbrooke's Cognitive Examination (ACE-R) for detecting mild cognitive impairment and dementia in a Japanese population. International Psychogeriatrics 24, 28–37. http://dx.doi.org/10.1017/S1041610211001190. Zucchella, C., Bartolo, M., Pasotti, C., Chiapella, L., Sinforiani, E., 2012. Caregiver burden and coping in early-stage Alzheimer disease. Alzheimer Disease & Associated Disorders 26, 55–60. http://dx.doi.org/10.1097/WAD.0b013e31821aa6de.
