CLUSTERING OF BEHAVIOURAL AND PSYCHOLOGICAL SYMPTOMS IN DEMENTIA (BPSD): A EUROPEAN ALZHEIMER S DISEASE IN CONSORTIUM (EADC) STUDY

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1 426 Original articles CLUSTERING OF BEHAVIOURAL AND PSYCHOLOGICAL SYMPTOMS IN DEMENTIA (BPSD): A EUROPEAN ALZHEIMER S DISEASE IN CONSORTIUM (EADC) STUDY M. Petrovic 1,2, C. Hurt 2, D. Collins 2, A. Burns 2, V. Camus 3, R. Liperoti 4, A. Marriott 5, F. Nobili 6, P. Robert 7, M. Tsolaki 8, B. Vellas 9, F. Verhey 10, E.J. Byrne 2 Key words: dementia, behavioural and psychological symptoms of dementia (BPSD), clusters 1 Department of Geriatrics and Gerontology, Ghent University Hospital and Heymans Institute of Pharmacology, Ghent, Belgium; 2 Division of Psychiatry, University of Manchester, Education and Research Centre, Wythenshawe Hospital, Manchester, UK; 3 Clinique Psychiatrique Universitaire, Centre Hospitalier Régional Universitaire, Tours, France; 4 Centro Medicina dell Invecchiamento, Università Cattolica del Sacro Cuore, Rome, Italy; 5 Kingshill Research Centre, Victoria Hospital, Swindon, UK; 6 Clinical Neurophysiology Service, Department of Internal Medicine, University of Genoa, Italy; 7 Centre Mémoire de Ressources et de Recherche au CHU, Université de Nice Sophia-Antipolis, France; 8 University Department of Neurology, Memory and Dementia Centre Aristotle University of Thessaloniki, Greece; 9 Centre Mémoire de Ressources et de Recherché de Toulouse, France; 10 University Hospital of Maastricht, Alzheimer Centre Limburg, Maastricht, the Netherlands Address for Correspondence: Prof. Dr. Mirko Petrovic Department of Geriatrics, University Hospital and Heymans Institute of Pharmacology De Pintelaan Gent Belgium Tel: +32 (0) Fax: +32 (0) mirko.petrovic@ugent.be ABSTRACT Objectives. This cross-sectional study investigated the relationships between behavioural and psychological symptoms of dementia (BPSD). Methods. We recruited 194 patients with dementia from the memory clinic practice of six European Alzheimer s Disease Consortium centres. BPSD were assessed using a pre-designed questionnaire comprising the Neuropsychiatric Inventory (NPI). BPSD scores were analysed by Spearman s correlation analysis and principal components factor analysis. Results were confirmed by performing Varimax rotation of the factors. Results. The NPI symptoms occurred very frequently: 96% of the patients displayed at least one symptom. Among them, apathy (59.6%) and depression (58.5%) were the most common abnormalities, followed by irritability (44.6%), anxiety (44%) and agitation (41.5%). Four NPIbased factors were identified (58% of the common variance): psychosis factor (irritability, agitation, hallucinations and anxiety), psychomotor factor (aberrant motor behaviour and delusions), mood liability factor (disinhibition, elation and depression) and instinctual factor (appetite disturbance, sleep disturbance and apathy). Conclusion: Psychosis, psychomotor factor, mood liability factor and instinctual factor form four distinct behavioural syndromes in dementia. We report the novel observation that depression

2 427 clusters together with disinhibition and elation within a mood liability factor. This finding highlights the nature of mood, and mood oscillations, from depression to disinhibition within the cluster, and has implications for treatment by taking into consideration the poles of the mood scale and any oscillation between them. INTRODUCTION Behavioural and psychological symptoms in dementia (BPSD) represent a heterogeneous group of noncognitive symptoms and behaviours that occur in subjects with dementia. BPSD have been recognised as an important component of demented syndrome, being clinically as significant as cognitive disorders (1). Although prevalence estimates for BPSD vary widely due to the heterogeneity in patient baseline characteristics and assessment methods, up to 90% of the patients with dementia experience some BPSD at any one time point (2, 3). Two population-based studies show a prevalence of about 20% for BPSD in patients with Alzheimer s disease (4, 5). In addition, three recent European studies found apathy being the most frequent symptom (6-8). BPSD are important because they cause considerable suffering and reduce the quality of life of both the patient and the caregiver, perhaps more than the cognitive difficulties themselves (9). The presence of BPSD also leads to more hospitalisations and an increased likelihood of entry into a nursing home, as they make it more difficult for the caregiver to manage the patient. This in turn increases the cost of care (10). Several studies have shown that most of BPSD do not appear in isolation but tend to occur together in clusters or syndromes. These clusters vary by time, severity, and diagnosis. A number of syndromes have been described on the basis of factor analytical studies using rating instruments designed to measure BPSD. For example, in a study of 162 patients with Alzheimer s disease, Frisoni et al. reported the presence of three factors: a mood factor, a frontal factor and a psychosis factor (3). Aalten et al. also identified three factors in a study group of 199 patients with mixed aetiologies of dementia: a mood/apathy factor, a psychosis factor and a hyperactivity factor (6). In another study of 435 patients with Alzheimer s disease, Mirakhur identified four factors: an affect factor, a physical behaviour factor, a psychosis factor and a hypomania factor (8). Table 1 summarises the factor analysis reported in these studies. Although these studies differ in design and sample size, there is a certain degree of concordance in the groups of symptoms obtained by these methods, namely depression, psychosis, psychomotor agitation and apathy. Since these findings point to the possibility that Table 1. Factor analysis reported in the studies of Frisoni et al. (3), Aalten et al. (6) and Mirakhur et al. (8), respectively Frisoni et al., 1999 Aalten et al., 2003 Mirakhur et al., 2004 Frontal Psychosis Mood Mood/apathy Psychosis Hyperactivity Affect Physical behaviour Phychosis De Ha Ag De An El Ap + + Di Ir Mo + + Sl + + Ap + + De = delusions; Ha = hallucinations; Ag = agitation; De = depression; An = anxiety; El = elation; Ap = apathy; Di = disinhibition; Ir = irritability; Mo = motor aberrant behaviour; Sl = sleep disturbances; Ap = appetite disturbances Hypomania

3 428 grouping symptoms might relate to clinical practice, diagnostic criteria for distinct syndromes of both psychosis and depression of Alzheimer s disease have been accordingly proposed in order to facilitate recognition and therapeutic targeting of these specific aspects of BPSD (11-12). In a population-based study Lyketsos et al. found that complex inter-relationships between the presence of the different symptoms in Alzheimer s disease cluster into three classes. The first class included patients with no symptoms and one symptom only, the second class showed predominantly affective symptoms, and the third class displayed a psychotic syndrome (13). All the studies described here thus far are all crosssectional in nature regarding BPSD. However, a few European studies have addressed the evolution of BPSD over time. For example, a large French study showed that on longitudinal follow-up, patients tend to develop more behavioural symptoms during the disease (7), whereas a Dutch study provided evidence that different symptoms have their own specific course, but behavioural symptoms overall are chronically present (14). Two studies from the Netherlands also reported that mood disorders appear to be early manifestations of dementia even before the emergence of cognitive symptoms and that aberrant motor behaviour is common and persistent (14-15). Finally, an Irish study illustrated that psychosis shows moderate persistence and that depressive symptoms tend to decrease in contrast to apathy (16). As to the disease severity and its effect on the caregiver, it has been shown that apathy rather than excessive behaviour has the most impact on the deterioration of the relationship between the patient and the caregiver (17). On the other hand, inappropriate strategies by the caregiver might increase the occurrence of delusions, aggressiveness, or hyperactive behaviour (18-20). It has also been shown that patients with the greatest cognitive impairment display more depression, agitation, and psychosis (21). Knowledge of symptoms and their severity in individual dementia cases are useful, but factor analysis of the variety of symptoms present in dementia attempts to group symptoms together in a meaningful way so that improved recognition of syndromes can be realized and better clinical treatments devised. Thus, given the potential to improve our understanding of BPSD, we aimed to (a) determine whether the predominantly affective and psychotic symptoms reported in the literature could be confirmed in a multi-centre study in which regional, cultural and other factors might operate, and (b) compare the symptomatic clustering found with findings of other cross-sectional studies. In addition, a further aim was to test the feasibility of international, multi-centre collection of data with electronic transfer. METHODS Patients and Settings Six different centres from the European Alzheimer s Disease Consortium (EADC) participated in the study: Nice and Toulouse (France), Thessaloniki (Greece), Lausanne (Switzerland), Manchester and Swindon (United Kingdom). Manchester was the study coordinating centre. The patients for this study were taken from memory clinic practices and all already had a working diagnosis of dementia. It should be noted that final diagnosis was not available until each centre provided a full data set for each patient. Since this study was not concerned with analysing the type of dementia with regard to BPSD clustering, the dementia aetiology of the recruited patients is not reported. Patients also had to have regular contact with a main caregiver, as their input was vital to the assessment. The registration ran from October 2002 until December Some patients had to be excluded, as the centres did not provide a full set of data. This left a total sample size of 194. Ethical approval was obtained for the study, and all patients and caregivers were required to give full informed consent in order to be able to participate. Assessment of Subjects A questionnaire was compiled which was designed to complement the standardised rating assessment as described below. This included questions on demographics, the physical health of the patient, and qualitative aspects of behaviour according to the caregiver. Each symptom required a score of up to 12 to be given, depending on its frequency and severity. Each patient was interviewed with the main caregiver, either at home or at the clinic. The interview included a section with the patient and a section with the caregiver without the patient present. The same person conducted the interviews wherever possible to eliminate bias. The person performing the assessment filled in a copy of the main study questionnaire for each patient, as well as the following standardised validated questionnaires: Mini Mental State Examination, Neuropsychiatric Inventory,

4 429 Apathy Inventory and Quality of Life in Alzheimer s Disease (22-25). Mini Mental State Examination (MMSE) This instrument is a widely used screening tool for dementia designed to test basic cognitive functioning. It looks at orientation, language, visuospatial skills, concentration, and memory. The maximum achievable score is 30 (22). Neuropsychiatric Inventory with Caregiver Distress Scale (NPI) This instrument measures neuropsychiatric disturbances in dementia, although it was originally devised for patients with Alzheimer s disease. It is considered to be equally applicable to all types of dementia, and examines 12 different symptoms. It is performed with the caregiver and thus reflects the caregiver s experience of the patient. Symptoms measured include: delusions, hallucinations (visual, auditory, gustatory, or somatic), agitation, depression, anxiety, elation, apathy, disinhibition, irritability, aberrant motor behaviour (e. g. pacing, rummaging, repetitive movements), sleep disturbances, and appetite or eating disorders (23). Data from both the Apathy Inventory and the Quality of Life in Alzheimer s disease were not considered for this paper, but for separate publications. Data Collection A Word Excel spreadsheet workbook was produced and sent to each centre taking part in the study. This was done so that each centre would enter their data in the same way and in order to eliminate potential variability in the recording of information. All numerical data taken from the paper questionnaires were entered into the standard spreadsheet workbook as described above. Qualitative data were coded according to the criteria set out by the study coordinating centre in Manchester and entered into the workbook. Each centre then sent the completed workbooks with all the study participants data via electronic transfer to Manchester. Once all the data had been received it was compiled into one large spreadsheet and then converted into Statistical Program for the Social Sciences (SPSS, version 10.1) format for analysis. Statistical Analysis Any subjects that did not have a full set of data for the NPI were not included in the analysis. All data from the NPI were coded as either 0 or 1 depending on whether the symptom was present or not. This did not take severity (score out of 12) into account. A two-sided Spearman s non-parametric correlation analysis was performed on the raw data (scores from 0-12 for each symptom). This was also carried out so as to determine which symptoms were significantly associated with other symptoms. The sample size had enough power to detect a correlation coefficient of 0.3 or above (the level at which a relationship is considered significant). Factor analysis was used to identify the underlying factors that explain the pattern of correlations within observed BPSD in this study. Principal components factor analysis was carried out on the composite scores of the NPI symptoms (12 symptoms). Factors were selected for rotation if the eigenvalue > 1 (a measure of the percentage of variance). Symptoms were included in a factor if their factor loading 0.4 (a measure of the degree of correlation). Results were confirmed by performing Varimax rotation of the factors. RESULTS The 194 patients recruited had a mean age of 75 years (SD + 8.4) and a mean MMSE score of 16 (SD + 5.1) with a range of 0 to 23. The mean MMSE score did not differ significantly between participating centres. The mean estimated duration of dementia was 3.7 years (SD + 3.2). The majority of the sample was female (62.4%). Table 2 shows the prevalence of each symptom in the sample. The symptoms that we investigated in this cross-sectional study occurred very frequently: 96% of the patients displayed at least one symptom. Among the NPI symptoms, apathy (59.6%) and depression (58.5%) were the most common abnormalities, follo- Table 2. Prevalence of behavioural and psychological symptoms of dementia in the study sample Symptom Prevalence (%) Apathy 59.6 Depression 58.5 Irritability 44.6 Anxiety 44.0 Agitation 41.5 Aberrant motor behaviour 29.5 Sleep disturbances 29.5 Delusions 25.4 Appetite disturbances 20.2 Disinhibition 19.6 Hallucinations 13.5 Elation 13.5

5 430 Table 3. Correlations between BPSD (N = 194) Ap Sl Mo Ir Di Ap El An De Ag Ha De 0.167* 0.402** 0.160* 0.200** 0.271** 0.169* Ha 0.289** 0.219** 0.215** 0.175* 0.178* 0.280** Ag 0.295** 0.513** 0.174* 0.247** De 0.224** 0.211** 0.219** An 0.157* 0.224** El 0.202** 0.332** Ap 0.171* 0.219** 0.289** 0.259** 0.175* Di 0.253** Ir 0.217** 0.156* Mo 0.179* Sl *Indicates relationships significant at the 5% level (p 0.05); **Indicates relationships significant at the 1% level (p 0.01) De = delusions; Ha = hallucinations; Ag = agitation; De = depression; An = anxiety; El = elation; Ap = apathy; Di = disinhibition; Ir = irritability; Mo = motor aberrant behaviour; Sl = sleep disturbances; Ap = appetite disturbances Table 4. Factor loadings for the four factors (1, 2, 3, 4) with eigenvalues > 1 obtained via principal component factor analysis of the 12 NPI symptom composite scores Symptom Delusions Hallucinations Agitation Depression Anxiety Elation Apathy Disinhibition Irritability Aberrant motor behaviour Sleep disturbance Appetite disturbance wed by irritability (44.6%), anxiety (44%) and agitation (41.5%). Table 3 gives the results of the Spearman s analysis, which tested the association between each symptom and every other symptom, using the scores obtained from the questionnaires. The most significant associations were found between agitation and irritability, and between delusions and aberrant motor behaviour. Agitation and psychosis (i.e. delusions and hallucinations) were significantly associated. Agitation was also significantly correlated with depression. Table 4 shows the results of the principal components factor analysis, which was carried out on the composite scores of the NPI symptoms. Four factors were identified among the NPI symptoms, which accounted for 58% of the variance. These factors were F1: irritability, agitation, hallucinations and anxiety, F2: aberrant motor behaviour and delusions, F3: disinhibition, elation and depression, and F4: appetite disorders, sleep disorders and apathy. DISCUSSION The symptoms that were investigated in this crosssectional study occurred very frequently: 96% of the patients displayed at least one symptom. This might be because the patients for this study were taken from memory clinic practice and all already had an initial diagnosis of dementia. Among the NPI symptoms, apathy and depression were the most common abnormalities, followed by irritability, anxiety, and agitation. As is evident from the results, the Spearman s correlation analysis revealed many significant associations between symptoms (Table 3). These include some that can be considered predictable, as they are related for example agitation and irritability, as well as agitation and aberrant motor behaviour. Agitation and depression were significantly associated in this study. We found that agitation was also significantly correlated with delusions and hallucinations, which further supports the finding that agitation and psychosis are linked (21), although Levy found that depression and psychosis were not associated (21). In concordance with this observation, we found no correlation between depression and delusions. On the other

6 431 hand, depression and hallucinations were significantly associated in this study. It can be concluded from the results of the Spearman s correlation analysis that BPSD not only are extremely common in patients with dementia, but also that there are many associations between them. The fact that so many symptoms were studied within a relative large data set means that some of the associations found might have occurred by chance, due to the sheer number of calculations performed. Therefore, conclusions drawn from the results of the Spearman s analysis must be, to some extent, tentative. Consequently, we performed the principal components factor analysis. We identified four factors in which the NPI symptoms cluster. The observed factors include a psychosis factor consisting of irritability, agitation, hallucinations and anxiety, a psychomotor factor comprising aberrant motor behaviour and delusions, a mood liability factor including disinhibition, elation and depression, and an instinctual factor consisting of appetite disorders, sleep disorders and apathy. In our study, the psychosis factor comprises a combination of symptoms reported by Frisoni et al. (hallucinations, irritability and agitation) (3), with those reported by Aalten et al. (hallucinations, anxiety) (6). We also noted that aberrant motor behaviour clusters together with delusions within a psychomotor factor. Aberrant motor behaviour was previously positioned either within a hyperactivity factor (6), or within a physical behaviour factor (8). Our observation also suggests various expression patterns of psychotic symptoms in dementia among the NPI symptoms, i.e. either with predominance of mood disorders or aberrant motor behaviour. We also report a novel observation that depression and the symptoms of the frontal factor reported by Frisoni et al. (3), or the hypomania factor reported by Mirakhur et al. (8), which consist of disinhibition and elation, cluster within a mood liability factor. This finding suggests that exploration of mood and its expression in terms of mood change might be an important factor to consider when formulating a treatment strategy, especially in the early stages, as Dutch studies have reported that mood disorders appear to be early manifestations of dementia (14-15). The fourth factor that we identified in this study was an instinctual factor comprising appetite disturbance, sleep disturbance and apathy. This result concurs with the findings of Mirakhur et al. (8). However, this study could not confirm an association between apathy and depression, which is not in line with the results of the study by Aalten et al. (6). Our study also reveals different patterns of psychosis expression in dementia. Given that the context of the behaviour and its impact are also important elements in assessment, it is useful to identify target symptoms in every patient expressing BPSD: is this primarily a psychotic syndrome or is the main problem mood or psychomotor agitation? The strengths of this study were the relatively large size of the whole sample and the wide reaching nature of the sample. On the other hand, there are limitations in this study, the largest of which is that the study did not deal with the aetiology of dementia. This occurred because the Excel spreadsheet sent to the participating centres did not include the requirement to report on the type of dementia. Since the analysis of BPSD in this study was never intended to be associated with the type of dementia, this did not allow us to identify clusters that could be specific for different types of dementia. Moreover, in certain types of dementia, such as frontotemporal dementia, there might be an over-representation of some behavioural clusters. The present study is also limited by its cross-sectional nature. A larger longitudinal study could determine whether the associations that we found remain stable over time. Finally, this study has shown that an international multi-centre data collection by means of electronic transfer is feasible. In general, the transfer of data was fast, and the spreadsheets sent were returned with the expected data. This also provided us with a means for a unified registration and data comparison. One minor problem, however, was the clarification of individual data issues or points, which could not be achieved instantaneously, and took some time and effort to resolve. In addition, studying patients from different European countries helped to eliminate possible cultural bias, although all centres are in developed countries. This finding might contribute to a promotion of further research on a broader basis in order to provide a more standardised detection and understanding of BPSD symptoms. REFERENCES 1. Lawlor B. Managing behavioural and psychological symptoms in dementia. Br J Psychiatry 2002; 181: Levy ML, Miller BL, Cummings JL, Fairbanks LA, Craig A. Alzheimer disease and frontotemporal dementias. Behavioral distinctions. Arch Neurol 1996; 53: Frisoni GB, Rozzini L, Gozzetti A, et al. Behavioural syndromes in

7 432 Alzheimer s disease: description and correlates. Dement Geriatr Cogn Disord 1999; 10: Lyketsos CG, Steinberg M, Tschanz JT, Norton MC, Steffens DC, Breitner JC. Mental and behavioral disturbances in dementia: findings from cache Count Study on Memory and Aging. Am Journal Psychiatry 2000; 157: Burns A, Jacoby R, Levy R. psychiatric phenomena in Alzheimer s disease. Br J Psychiatry 1990; 157: Aalten P, de Vugt ME, Lousberg R, et al. Behavioral problems in dementia: a factor analysis of the Neuropsychiatric Inventory. Dement Geriatr Cogn Disord 2003; 15: Benoit M, Staccini P, Brocker P, et al. Behavioral and psychologic symptoms in Alzheimer s disease. Rev Med Interne 2003; 24: 319s-24s. 8. Mirakhur A, Craig D, Hart DJ, McIlroy SP, Passmore AP. Behavioural and psychological syndromes in Alzheimer s disease. Int Journal Geriatr Psychiatry 2004; 19: Burns A. The burden of Alzheimer s disease. Int J Neuropsychopharmacol 2000; 3: Finkel S. Introduction to behavioural and psychological symptoms of dementia (BPSD). Int J Geriatr Psychiatry 2000; 15: S2-S Jeste DV, Finkel SI. Psychosis of Alzheimer s disease and related dementias. Diagnostic criteria for a distinct syndrome. Am J Geriatr Psychiatry 2000; 8: Olin JT, Schneider LS, Katz IR, et al. Provisional diagnostic criteria for depression of Alzheimer s disease. Am J Geriatr Psychiatry 2002; 10: Lyketsos CG, Sheppard JM, Steinberg M, et al. Neuropsychiatric disturbance in Alzheimer s disease clusters into three groups: the Cache County study. Int J Geriatr Psychiatry 2001; 16: Aalten P, de Vugt ME, Jaspers, N, Jolles J, Verhey FR. The course of neuropsychiatric symptoms in dementia. Part I: findings from the two-years longitudinal Maasbed study. Int J Geriatr Psychiatry 2005; 20: Geerlings MI, Schoevers RA, Beekman AT, et al. Depression and risk of cognitive decline and Alzheimer s disease. Results of two prospective community-based studies in The Netherlands. Br J Psychiatry 2000; 176: Eustace A, Coen R, Walsh C, et al. A longitudinal evaluation of behavioural and psychological symptoms of probable Alzheimer s disease. Int J Geriatr Psychiatry 2002; 17: de Vugt ME, Stevens F, Aalten P, et al. Behavioural disturbances in dementia patients and quality of the marital relationship. Int J Geriatr Psychiatry 2003; 18: de Vugt ME, Stevens F, Aalten P, et al. Do caregiver management strategies influence patient behaviour in dementia? Int J Geriatr Psychiatry 2004; 19: Riello R, Geroldi C, Zanetti O, Frisoni GB. Caregiver s distress is associated with delusions in Alzheimer s patients. Behav Med 2002; 28: Hamel M, Gold DP, Andres D, et al. Predictors and consequences of aggressive behavior by community-based dementia patients. Gerontologist 1990; 30, Levy ML, Cummings JL, Fairbanks LA, Bravi D, Calvani M, Carta A. Longitudinal assessment of symptoms of depression, agitation, and psychosis in 181 patients with Alzheimer s disease. Am J Psychiatry 1996; 153: Folstein MF, Folstein SE, McHugh PR. Mini-mental test : a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975; 12: Cummings JL, Mega MS, Gray K, Rosenberg-Thompson S, Gornbein, T. The Neuropsychiatric Inventory: comprehensive assessment of psychopathology in dementia. Neurology 1994; 44: Robert P, Clairet S, Benoit M, et al. The Apathy Inventory; assessment of apathy and awareness in Alzheimer s disease, Parkinson s disease and mild cognitive impairment. Int J Geriatr Psychiatry 2002; 17: Logsdon R, Gibbons L, McCurry S, Teri L. Quality of life in Alzheimer s disease: patient and caregiver reports. J Mental Health Aging 1999; 5:

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