The Impact of Dementia Severity on Caregiver Burden in Frontotemporal Dementia and Alzheimer Disease

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1 ORIGINAL ARTICLE The Impact of Dementia Severity on Caregiver Burden in Frontotemporal Dementia and Alzheimer Disease Eneida Mioshi, PhD,*w David Foxe, BPsych,* Felicity Leslie, BPsych,* Sharon Savage, MClinNeuro,* Sharpley Hsieh, DCN, MSc,* Laurie Miller, PhD,z John R. Hodges, FRCP,*w and Olivier Piguet, PhD*w Abstract: Caregiver burden is greater in frontotemporal dementia (FTD) than in Alzheimer disease (AD). However, little is known of the impact of the 3 main clinical variants of FTD behavioralvariant frontotemporal dementia (bvftd), semantic dementia (SemDem), and progressive nonfluent aphasia (PNFA) or the role of disease severity in caregiver burden. The Zarit Burden Inventory was used to measure caregiver burden of bvftd (n = 17), SemDem (n = 20), PNFA (n = 20), and AD (n = 19) patients. Symptom duration, caregiver age, and relationship type were matched across groups. Moreover, a number of caregiver (mood, social network) and patient variables (functional disability, behavioral changes, relationship with caregiver, and dementia stage) were addressed to investigate their impact on caregiver burden. Caregivers of bvftd patients reported the highest burden, whereas SemDem and PNFA caregivers reported burden similar to AD. A regression analysis revealed that caregiver burden in FTD, regardless of subtype, was explained by a model combining disease staging, relationship changes, and caregiver depression. Burden increased with disease severity in FTD. This study is the first to show that caregivers of SemDem, PNFA, and AD patients show similar burden, while confirming that bvftd caregivers show higher burden than AD caregivers. More importantly, this study demonstrates that burden worsens with disease progression in FTD. Key Words: caregiver burden, frontotemporal dementia, disease severity, depression, caregiver-patient relationship, disease progression (Alzheimer Dis Assoc Disord 2013;27:68 73) Received for publication May 17, 2011; accepted November 27, From the *Neuroscience Research Australia, Sydney; wschool of Medical Sciences, University of New South Wales, Kensington; and zroyal Prince Alfred Hospital, Camperdown, NSW, Australia. Supported in part by a National Health and Medical Research Council (NHMRC) of Australia research grant (#5,10,106). E.M. is a recipient of an NHMRC Postdoctoral Fellowship (#10,16,399). S.H. is a recipient of an Australian Postgraduate Award. J.R.H. is supported by an Australian Research Council Federation Fellowship Grant. O.P. is supported by an NHMRC Clinical Career Development Award Fellowship (#5,10,184). For the remaining authors no conflicts of interest were declared. Reprints: John R. Hodges, PhD, Neuroscience Research Australia, Barker St, PO Box 1165, Randwick, Sydney, NSW 2031, Australia ( Copyright r 2013 by Lippincott Williams & Wilkins Frontotemporal dementia (FTD) is an important cause of younger-onset dementia and presents with 3 main clinical variants: behavioral frontotemporal dementia (bvftd), semantic dementia (SemDem), and progressive nonfluent aphasia (PNFA). Patients with bvftd typically show progressive and debilitating changes in interpersonal skills and behavior, whereas the other 2 language variants, SemDem and PNFA, present with an insidious decline in language skills that are initially circumscribed. 1,2 Nevertheless, language difficulties alone can be very challenging, limiting social participation of patients and caregivers and ultimately also creating distress for both. It is not surprising that family members involved with FTD patients present with high rates of burden and stress. 3 5 Indeed, recent studies have shown that caregiver burden in FTD is much greater than in Alzheimer disease (AD) 4,6,7 and that patients behavioral changes can be correlated with caregiver stress in FTD and AD 3,8 10 ; however, this finding has not been universal. 11,12 Caregiver-related factors such as mood and social network are also implicated on the basis of caregiver burden. For example, the insidious depression in family caregivers is strongly associated with increased stress. 12 Moreover, the stress and burden seem to be higher for caregivers of patients residing at home, 13 but some studies of FTD caregivers have shown that stress levels were not significantly different between caregivers of nursing homes and community-dwelling patients. 4,12 The current literature shows that there is still a lack of consensus on which factors can best predict caregiver burden. Rates of disease progression vary across the 3 clinical FTD syndromes. 14 Patients with bvftd reach the severe stage in about 5 years from disease onset. By contrast, SemDem patients may take about 10 years to reach the same stage. Moreover, features from the various subtypes tend to merge as disease progresses. 15 Behavioral symptoms characteristic of bvftd tend to appear in SemDem and PNFA. Similarly, bvftd patients typically develop language difficulties later on. Numerous studies have characterized the FTD variants in terms of symptomatology, neuroimaging changes, and neuropsychological performance but the effects of each type of FTD on caregivers are unknown. These effects are important and the differences, if present, should be taken into account by professionals involved in the delivery of care. Although disease severity may play an important role in caregiver burden, no study to date has investigated this issue systematically. Although not the focus of this study, we included a group of caregivers of AD patients as a reference point to allow comparison between the disorders on the measures and for professionals less familiar with FTD. This study aimed to (1) compare caregiver burden in the FTD variants and AD; (2) identify patient and caregiver variables contributing to caregiver burden; (3) examine the effects of dementia severity on caregiver burden. METHODS Participants Data from the caregivers of bvftd (n = 17), SemDem (n = 20), PNFA (n = 20), and AD (n = 19) patients 68 Alzheimer Dis Assoc Disord Volume 27, Number 1, January March 2013

2 Alzheimer Dis Assoc Disord Volume 27, Number 1, January March 2013 attending the Frontier Research Clinic in Sydney, Australia, were collected. Caregivers age and type of relationship were matched across dementia subgroups; most caregivers were women (Table 1). All data reported here refer to the initial patient visit to the clinic. Patients were diagnosed with FTD 5,16 or AD 17 according to current consensus criteria. The majority of patients were men and PNFA patients were significantly older than bvftd patients. Other patients characteristics are described in Table 2. All caregivers and patients consented to the study and Ethics approval was obtained from the Human Research Ethics Committees of South Eastern Sydney/Illawara Area Health Service and the University of New South Wales. Instruments Caregiver: Caregiver Burden Caregiver burden was measured using the short Zarit Burden Inventory, 18 which comprises 12 questions and has been extensively used in studies of caregiver burden. Caregivers are asked to rate their feelings in terms of frequency. High scores denote increased burden, with a suggested cutoff score of indicating clinically significant burden. Caregiver: Depression and Anxiety The Depression, Anxiety and Stress Scale 21 (DASS 21) 19 was used to evaluate caregivers depression, anxiety, and stress. Existing normative data suggest cutoff scores of 10 and above as reflecting significant depression, 8 and above as being indicative of significant anxiety, and 15 and above as being indicative of significant stress. 20 Caregiver: Social Network The richness of social connections of the caregivers was assessed with the Social Network Index (SNI), 21 which generates a score of high-contact roles, such as participation in religious or voluntary activities, and the number of people in the network. On the basis of a previous FTD study, 12 the present study focused on the number of high-contact roles, given the relevance of this variable on caregiver stress. Caregiver: Quality of Bond Between Caregiver and Patient The current quality of the relationship between the caregiver and the patient was measured using the Intimate Bond Measure (IBM). 22 This measure is completed by the caregiver and generates 2 different scores: the first reflects a caring relationship from the patient toward the caregiver and the second addresses a controlling type of relationship from the patient toward the caregiver. Lower scores denote less rewarding relationships. Patient: General Cognition Patients cognitive status was measured by the Addenbrooke s Cognitive Examination Revised (ACE-R). 23 The ACE-R assesses 5 cognitive domains: attention/orientation, memory, verbal fluency, language, and visuospatial abilities. ACE-R total score is 100; higher scores reflect better ability. The ACE-R was designed to be sensitive to early stages of dementia and incorporates the MMSE. Patient: Disease Severity Disease severity was determined using the Frontotemporal Dementia Rating Scale (FRS). 14 The FRS yields 6 different disease stages, ranging from very mild to profound, on the basis of changes in activities of daily living and behavior. The range of dementia stages are very mild (5.39 to 4.12); mild (3.35 to 1.92); moderate (1.68 to 0.40); severe ( 0.59 to 2.58); very severe ( 3.09 to 4.99); and profound ( 4.98 to 6.66). The FRS score is obtained through an interview with the caregiver or the proxy informant. Patient: Behavioral Change Patients behavioral changes were evaluated with the Cambridge Behavioral Inventory Revised (CBI-R). 13 The CBI-R is a caregiver-based questionnaire that comprises 45 questions divided into 10 different domains: memory and orientation; everyday skills; self-care; abnormal behavior; mood; beliefs; eating habits; sleep; stereotypic and motor behaviors; and motivation. For the purpose of this study, the focus was on 3 domains, which are specifically related to the behavioral changes seen in FTD 24 : abnormal behavior (such as shows socially embarrassing behavior ; acts impulsively without thinking ), stereotypic and motor TABLE 1. Comparisons of Caregivers of FTD Variants (bvftd, SemDem, and PNFA) and AD on Demographic Variables, Zarit Burden Scores, Depression, Anxiety, Social Network, and Intimate Bond Measure Care and Control (Means and SD) bvftd (n = 17) SemDem (n = 20) PNFA (n = 20) AD (n = 19) Age (y) 57.3 (11.9) 55.7 (13.4) 64.6 (11.3) 61.1 (13.4) Sex, % of women Type of relationship, spouse (%) Zarit Burden (cutoff 17) 26.2 (2.2)* 16.2 (2.0) 12 (2.0) 15.7 (2.1) Depression (cutoff 10) 8.4 (8.3)w 6.6 (8.8) 4.1 (9.1) 6.3 (9) Anxiety (cutoff 8) 3.2 (6) 5.2 (5.7) 3.7 (7.3) 5.6 (8.4) Stress (cutoff 15) 7.2 (5.4) 5.9 (4.9) 4.5 (5.3) 6.9 (5) Social network high-contact roles 15.8 (6.1) 18.2 (5) 16.3 (6.1) 16.5 (5.1) Intimate bond measure care 13.9 (7.1)z 20.9 (9.4) 28.9 (8.1) 28.5 (4.2) Intimate bond measure control 9.1 (7.3) 14.5(8.9)y 8.7 (8.4) 6.8 (6.6) *bvftd > SemDem (P < 0.05), PNFA (P < 0.001), and AD (P < 0.05). wbvftd > SemDem, PNFA, and AD (P < 0.05). zbvftd < SemDem (P < 0.05), PNFA, and AD (P < 0.001). ysemdem > AD (P < 0.05). AD indicates Alzheimer disease; bvftd, behavioral variant frontotemporal dementia; PNFA, progressive nonfluent aphasia; SemDem, semantic dementia. r 2013 Lippincott Williams & Wilkins 69

3 Mioshi et al Alzheimer Dis Assoc Disord Volume 27, Number 1, January March 2013 TABLE 2. Disease Characteristics in Patients With FTD (bvftd, SemDem, and PNFA) and AD (Means and SD) bvftd (n = 17) SemDem (n = 20) PNFA (n = 20) AD (n = 19) Patient age 59 (10.6) 64.8 (7.8) 68.1 (9.8)* 67 (9) Male patients (%) Length of symptoms (y) 3.3 (2.6) 4.3 (2) 3.1 (1.7) 2.9 (2.2) General cognition ACE-R (cutoff 82/100) 68.3 (14.5) 52.7 (18)w 60.5 (18.7) 72.7 (21.1) FRS score 1.09 (1.87)z 1.27 (1.2) 2.45 (1.8) 0.96 (1.5) Severity of disease Severe Moderate Mild Moderate CBI-R abnormal behavior 35.8 (26.4)y 25.4 (25.1) 9.6 (14.9) 11.3 (16.1) CBI-R stereotypical behavior 55.4 (27.3) (39) 15.4 (26.3) 24.4 (23.9) CBI-R apathy 56.1 (25.3)z 34.2 (27) 19.1 (19.1) 23.3 (16.5) *PNFA > bvftd (P < 0.05). wsemdem < AD and bvftd (P < 0.05 for both). zbvftd > SemDem (P < 0.01), PNFA (P < 0.001), and AD (P < 0.01). ybvftd > PNFA (P < 0.01) and AD (P < 0.05). 8bvFTD > PNFA (P < 0. 01) and AD (P < 0. 05). zbvftd > PNFA (P < 0.001) and AD (P < 0.01); trend bvftd > SemDem. ACE-R indicates Addenbrooke s Cognitive Examination Revised; AD, Alzheimer disease; bvftd, behavioral variant frontotemporal dementia; CBI-R, Cambridge Behavioral Inventory Revised; FRS, Frontotemporal Dementia Rating Scale; FTD, frontotemporal dementia; PNFA, progressive nonfluent aphasia; SemDem, semantic dementia. behaviors (such as is rigid in his routine ; repeatedly uses the same catch phrase ; clock watches ), and apathy. CBI-R scores were corrected to percentages to allow for comparison among domains that have unequal number of questions. Statistical Analysis Data were analyzed using PASW Statistics 17.0 (IBM, Chicago IL). First, variables were plotted and checked for normal distribution by the Kolmogorov-Smirnov tests. Given the non-normal distribution of depression and anxiety scores for PNFA and AD subgroups, these variables were log transformed for the analyses. Scores are reported as raw scores in the text, however, for meaningful clinical interpretation. Analyses of variance were conducted to investigate the effect of group diagnosis on the burden scores of caregivers, with post hoc tests to compare differences between diagnostic groups. Multiple linear regression analysis (stepwise method) was used to identify variables underlying caregiver burden. Alpha was set at RESULTS Caregiver Variables Caregivers were matched in terms of age and type of relationship across 4 diagnostic groups (Table 1). Other demographics of interest are also displayed in Table 1. Of note, most caregivers were women and 60% were spouses. Caregiver: Caregiver Burden The analyses of variance revealed a significant group difference in caregiver burden scores (F = 8.199, df =3, P < 0.001). Post hoc tests showed that bvftd caregivers had significantly higher levels of burden than the other patient groups (P < 0.05). No other differences across groups were found. Only a small proportion (25%) of caregivers of PNFA patients was reporting burden (Fig. 1). Caregiver: Depression, Anxiety, and Stress No significant group effect was found on the anxiety and stress subscales of the DASS 21. A significant group effect was present for the depression score (F = 3.568, df = 3, P < 0.05), with bvftd caregivers reporting significantly higher depressive symptoms than all other diagnostic groups (P <0.05 for all) (Table 1). No other significant differences were found across groups. Caregiver: Social Network Quality of the social network, as measured by the SNI, did not differ significantly across diagnostic groups. All caregivers reported a similar number of high-contact roles (Table 1). Caregiver: Quality of Bond Between Caregiver and Patient Bond between patient and caregivers, as measured by the IBM, revealed significant group differences in both care (F = , df = 3, P < 0.001) and control (F = 3.346, df =3, P < 0.05) domains. For the care domain, the dyads of patient and caregivers in the bvftd group scored significantly lower (all P < 0.05) than the other dyads. No other group differences were present. On the control domain, caregiver-patients dyads with SemDem scored significantly higher than AD dyads (all P < 0.05), indicating that AD patients were the least likely to manifest a controlling relationship (Table 1). FIGURE 1. Proportion of caregivers (bvftd, SemDem, PNFA, and AD) presenting with burden and no burden according to their Zarit Burden Inventory scores. AD indicates Alzheimer disease; bvftd, behavioral variant frontotemporal dementia; PNFA, progressive nonfluent aphasia; SemDem, semantic dementia r 2013 Lippincott Williams & Wilkins

4 Alzheimer Dis Assoc Disord Volume 27, Number 1, January March 2013 Patient: General Cognition On the ACE-R, a test of general cognition, a significant group difference was present (F = 4.310; df = 3; P < 0.05). Post hoc tests revealed that SemDem patients scored significantly lower than AD and bvftd patients (both P < 0.05). No other group differences were found. Patient: Disease Severity On the FRS, which measures disease severity, a significant group difference was observed even after controlling for length of symptoms (F = ; df =3; P < 0.001). Post hoc tests (Table 2) showed that patients with bvftd were significantly more severe on the FRS than all the other patient groups (all P < 0.05). A trend toward a difference between AD and PNFA was also observed, with AD patients showing greater severity than PNFA patients (Fig. 2A). Patient: Behavioral Change Behavioral changes, as measured by a subset of the CBI-R, were present in all patient groups. These changes were particularly pronounced in bvftd and SemDem patients who were indistinguishable in terms of abnormal behavior (P = 0.552), stereotypical behavior (P = 0.803), and apathy (P = 0.052). When comparing SemDem patients with PNFA or AD patients, however, the differences were not statistically significant. SemDem patients scored significantly higher than PNFA for stereotypical behaviors. PNFA and AD patients were not distinguishable on any CBI scores. Which Variables Explain Caregiver Burden in the FTD Variants? To understand the factors underlying caregiver burden in bvftd, SemDem, and PNFA, a multiple regression analysis (stepwise method) was performed using the Zarit Burden score as the dependent variable. Eight predictor variables were selected, on the basis of previous studies. 3,12 Among the predictors, 2 were caregiver variables: (1) highcontact roles from the SNI and (2) caregiver depression, and 6 were patient variables: (3) caring relationship (IBM care), (4) controlling relationship (IBM control), (5) FTD severity (FRS), (6) CBI-R abnormal behavior, (7) CBI-R stereotypical behavior, and (8) CBI-R apathy. The best model, explaining 59% of the variance on caregiver burden scores, included disease severity, caring relationship between patient and caregiver, and caregiver depression. The FRS alone accounted for about 48% of the variance (Table 3). TABLE 3. Independent Variables Identified on the Multiple Regression Analysis; the Dependent Variable was the Zarit Burden Inventory With all FTD Caregivers Included (Stepwise Method) Zarit Burden B SE B Beta Constant Disease severity (FRS) * Caring relationship (IBM care) * Caregiver depression (DASS) * R 2 = 0.59 (P < 0.001). *P < DASS indicates Depression, Anxiety and Stress Scale; FRS, Frontotemporal Dementia Rating Scale; FTD, frontotemporal dementia; IBM, Intimate Bond Measure. To assess the effects of disease severity on caregiver burden, these 2 variables were plotted together. A significant relationship between caregiver burden and disease severity (r = 0.636, P < 0.001) was present, with higher levels of burden as disease progresses (Fig. 3). A small proportion of caregivers seemed to score high levels of burden even at milder stages of the disease, confirming that additional variables (caring relationship and caregiver depression) also play an important role in burden. DISCUSSION This study revealed significant differences in caregiver burden depending on the FTD subtype. Caregivers of patients with bvftd were markedly burdened in comparison with the caregivers of aphasic patients, who were at a similar level of burden as AD caregivers. In addition, disease severity was strongly correlated with caregiver burden, where mild patients had less burdened caregivers. Factors explaining caregiver burden in FTD were disease severity, a noncaring relationship between patient and caregiver, and depression of the caregiver. Disease severity was the main factor implicated in caregiver burden in FTD. Although not surprising, this finding has not been established formally to date. Changes in activities of daily living and in behavior, which are measured by the FRS, have been shown to be the best predictors of caregiver burden in AD. 25,26 The FRS was developed specifically to capture disease severity in FTD, therefore being more sensitive to the changes inherent in the condition that are likely to affect the family caregivers. Differences in caregiver burden rates in FTD variants are of clinical importance. BvFTD patients had the most FIGURE 2. A, Distribution of dementia severity scores for bvftd, SemDem, PNFA, and AD; lower scores denote more severity. B, Distribution of CBI scores (abnormal behavior, stereotypical behavior, and apathy) according to patient groups: bvftd, SemDem, PNFA, and AD; higher scores denote more behavioral change (means and SEM). AD indicates Alzheimer disease; bvftd, behavioral variant frontotemporal dementia; CBI, Cambridge Behavioral Inventory; PNFA, progressive nonfluent aphasia; SemDem, semantic dementia. r 2013 Lippincott Williams & Wilkins 71

5 Mioshi et al Alzheimer Dis Assoc Disord Volume 27, Number 1, January March 2013 FIGURE 3. FTD patients and caregivers plotted according to their Zarit (caregiver burden) and FRS (disease severity) scores. The dotted line on the y axis represents burden cut-off score; the dotted line on the x axis separates mild and moderate stages (right-hand side) from severe and very severe stages (left-hand side). FRS indicates frontotemporal dementia rating scale; FTD, frontotemporal dementia. burdened caregivers. Their level of disability and amount of abnormal behavior, as measured by the FRS and IBM, were the most severe among the four patient groups. In addition, the rate of caregiver depression was significantly higher among bvftd caregivers compared with the other groups, although not all caregivers reported depressive symptoms. Consistent with previous studies, behavioral changes in FTD were strongly associated with caregiver burden. 3 Interestingly, however, caregivers of SemDem patients did not report levels of burden as high as those reported by caregivers of bvftd patients, even though SemDem and bvftd patients were indistinguishable on behavioral changes. SemDem patients were, however, less severe on the FRS dementia staging scores and were reported as having a more caring relationship than bvftd patients. It seems that a combination of functional impairment and behavioral changes as measured by the FRS, rather than behavioral dysfunction alone (as measured by the CBI-R), are the main predictors of caregiver burden. This finding, although somewhat surprising, shows the importance of taking into account the FTD subtypes and their different rates of dementia progression when considering the impact of the disease on caregiver burden. The similar level of burden reported in PNFA and AD caregivers may be due to the similarity of the patients clinical presentations rather circumscribed cognitive deficits with little behavioral change, at least for a number of years. Caregivers of PNFA patients reported experiencing only a low level of burden. Two possible reasons may explain this finding: scores on the FRS indicated that the PNFA patients were relatively mildly affected. It is also possible that the language output difficulties, which are the main impairment in these patients and are observed in other patient groups, such as post-stroke patients, may be more easily accepted by the caregivers and those around the patient. Of note, it is possible that our AD caregiver sample was not reporting their highest level of burden, given the relatively short length of time in their role as a caregiver. This variable (length of time as a caregiver) should be used in future studies investigating caregiver burden in dementia. Findings from this study have implications for the planning of caregiver intervention in FTD. Targeting patient-related variables alone, such as behavioral management and/or patient disability, may not be the key to improving caregiver burden. Moreover, there is still no evidence that behavioral management strategies are effective in FTD, 27 although some have been proposed. 10,28 Although targeted behavioral interventions are important, our results indicate that interventions that aim at improving caregiver understanding of the specific changes inherent to FTD may be beneficial. For instance, changes in the relationship (from more to less caring) were an important factor in determining burden, and it is likely that many carers do not fully understand this as a result of FTD. It is, therefore, crucial that caregivers are provided with the opportunity to learn about, understand, and accept FTD symptoms and related changes, which is lacking. 29 Understanding changes inherent to the dementia process will help caregivers adjust their expectations, leading to acceptance of the diagnosis while helping them overcome the difficulties of the situation. The contribution of the grieving process to caregiver burden in FTD is also an important issue that deserves further investigation, especially given the generally younger onset of the dementia. 30 On the basis of these findings and our prior extensive experience of caregivers, 31 we have implemented a structured caregiver program, based largely on the work of Hebert et al, 32 which we hope will bring considerable practical benefit to caregivers dealing daily with these devastating and progressive disorders. Like all studies, ours has limitations. The caregiver groups were relatively small, and the burden measure used was unidimensional. Undoubtedly, a longitudinal study following caregivers from diagnosis to the end stages of the disease would provide an in-depth understanding of burden as the dementia progresses, and the impact of time on caregiver burden. In summary, this study highlights the differences in burden for caregivers depending on dementia subtype and demonstrates that disease severity in FTD plays a crucial role in the burden reported by the caregivers. These findings are relevant for the planning and delivery of support for families, reinforcing the need for tailored caregiver support that should take into account the disease stage. ACKNOWLEDGMENT The authors are very grateful for the support of all Frontier patients and caregivers. REFERENCES 1. Piguet O, Hornberger M, Mioshi E, et al. Behavioural-variant frontotemporal dementia: diagnosis, clinical staging, and management. 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6 Alzheimer Dis Assoc Disord Volume 27, Number 1, January March Kaiser S, Panegyres PK. The psychosocial impact of young onset dementia on spouses. Am J Alzheimers Dis Other Demen. 2006;21: Boutoleau-Bretonniere C, Vercelletto M, Volteau C, et al. Zarit burden inventory and activities of daily living in the behavioral variant of frontotemporal dementia. Dement Geriatr Cogn Disord. 2008;25: de Vugt ME, Riedijk SR, Aalten P, et al. Impact of behavioural problems on spousal caregivers: a comparison between Alzheimer s disease and frontotemporal dementia. Dement Geriatr Cogn Disord. 2006;22: Gallagher D, Ni Mhaolain A, Crosby L, et al. Dependence and caregiver burden in Alzheimer s disease and mild cognitive impairment. Am J Alzheimers Dis Other Demen. 2011;26: Diehl J, Mayer T, Foerstl H, et al. A support group for caregivers of patients with frontotemporal dementia. Dementia. 2003;2: Riedijk S, Duivenvoorden H, Rosso S, et al. Frontotemporal dementia: change of familial caregiver burden and partner relation in a Dutch cohort of 63 patients. Dement Geriatr Cogn Disord. 2008;26: Mioshi E, Bristow M, Cook R, et al. Factors underlying caregiver stress in frontotemporal dementia and Alzheimer s disease. Dement Geriatr Cogn Disord. 2009;27: Wear HJ, Wedderburn CJ, Mioshi E, et al. The Cambridge Behavioural Inventory Revised. Dementia and Neuropsychologia. 2008;2: Mioshi E, Hsieh S, Savage S, et al. Clinical staging and disease progression in frontotemporal dementia. Neurology. 2010;74: Kertesz A, McMonagle P, Blair M, et al. The evolution and pathology of frontotemporal dementia. Brain. 2005;128: Neary D, Snowden JS, Gustafson L, et al. Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology. 1998;51: McKhann G, Drachman D, Folstein M, et al. 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. 1984;34: Zarit SH, Anthony CR, Boutselis M. Interventions with care givers of dementia patients: comparison of two approaches. Psychol Aging. 1987;2: Lovibond PF, Lovibond SH. The structure of negative emotional states: comparison of the Depression Anxiety Stress Scales (DASS) with the Beck Depression and Anxiety Inventories. Behav Res Ther. 1995;33: Henry JD, Crawford JR. The short-form version of the Depression Anxiety Stress Scales (DASS-21): construct validity and normative data in a large non-clinical sample. Br J Clin Psychol. 2005;44: Cohen S, Doyle WJ, Skoner DP, et al. Social ties and susceptibility to the common cold. JAMA. 1997;277: Wilhelm K, Parker G. The development of a measure of intimate bonds. Psychol Med. 1988;18: Mioshi E, Dawson K, Mitchell J, et al. The Addenbrooke s Cognitive Examination Revised (ACE-R): a brief cognitive test battery for dementia screening. Int J Geriatr Psychiatry. 2006;21: Lillo P, Mioshi E, Zoing MC, et al. How common are behavioural changes in amyotrophic lateral sclerosis? Amyotroph Lateral Scler. 2011;12: Bergvall N, Brinck P, Eek D, et al. Relative importance of patient disease indicators on informal care and caregiver burden in Alzheimer s disease. Int Psychogeriatr. 2011;23: Mohamed S, Rosenheck R, Lyketsos CG, et al. Caregiver burden in Alzheimer disease: cross-sectional and longitudinal patient correlates. Am J Geriatr Psychiatry. 2010; 18: LoGiudice D, Hassett A. Uncommon dementia and the carer s perspective. Int Psychogeriatr. 2005;17(suppl 1):S223 S Merrilees J. A model for management of behavioral symptoms in frontotemporal lobar degeneration. Alzheimer Dis Assoc Disord. 2007;21:S64 S Rosness TA, Haugen PK, Engedal K. Support to family carers of patients with frontotemporal dementia. Aging Ment Health. 2008;12: Noyes BB, Hill RD, Hicken BL, et al. The role of grief in dementia caregiving. Am J Alzheimers Dis Other Demen. 2010;25: Lough S, Garfoot V. Psychological interventions in frontotemporal dementia. In: Hodges JR, ed. Frontotemporal Dementia Syndromes. Cambridge: Cambridge University Press; 2007: Hebert R, Levesque L, Vezina J, et al. Efficacy of a psychoeducative group program for caregivers of demented persons living at home: a randomized controlled trial. J Gerontol B Psychol Sci Soc Sci. 2003;58:S58 S67. r 2013 Lippincott Williams & Wilkins 73

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