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A Cross-Sectional Study of Neuropsychiatric Symptoms in 435 Patients With Alzheimer's Disease

Posted on: Thursday, 16 June 2005, 03:00 CDT

Objectives: The behavioral and psychological symptoms of Alzheimer's disease (AD) are associated with significant patient and caregiver distress and increased likelihood of institutionalization. We attempted to characterize in detail these symptoms and the distress they cause to caregivers. Methods: Patients with probable AD were assessed with the Mini-Mental State Exam (MMSE), Functional Assessment Staging (FAST), and the Neuropsychiatric Inventory With Caregiver Distress (NPI-D). Results: Four hundred and thirty-five patients were recruited. Neuropsychiatric symptoms of all types were highly prevalent. The most common and most persistent symptom was apathy (75%). Delusional symptoms were the least persistent. Depressive and apathetic symptoms were the earliest to appear, and hallucinations, elation/euphoria, and aberrant motor behavior were the latest symptoms to emerge. Hallucinations were significantly more common in severe dementia. Symptoms of irritability were most prevalent in early disease. Total Neuropsychiatric Symptom score was significantly correlated with MMSE and FAST score. Caregivers rated their own emotional distress levels as moderate or severe for 10 out of 12 symptom domains. The sum total of caregiver distress was strongly correlated with total NPI-D but not cognition or functional state. Distress levels did not vary when analyzed according to the patients' place of residence. Conclusions: Potentially treatable neuropsychiatric symptoms are common in AD and represent a major source of distress among caregivers. The extent of neuropsychiatric symptomatology is seen to correlate with the level of functional and cognitive disability although some symptoms are variably persistent and related to disease stage. (Am J Geriatr Psychiatry 2005; 13:460- 468)

The neuropsychiatric symptoms (NPS) of dementia may be grouped according to symptom clusters (e.g., depressive syndrome, psychotic syndrome) or disorders of function (e.g., disorders of sleep) or behavior (e.g., hitting, wandering). Broad classification into behavioral and psychological categories is also used. Apart from the considerable distress and anguish NPS produce in patients and caregivers,1-3 dementia-related behavioral change is a major independent risk factor for admission to expensive institutional care.4,5 Each 1-point increase in the Neuropsychiatrie Inventory (NPI) behavioral assessment scale costs up to $400 per year in additional healthcare expense.6 Symptoms such as aggression, mood change, apathy, and those that require continuous supervision such as wandering appear most burdensome.7,8 Reports also link behavioral characteristics such as aggression and psychosis with an inherently more unstable and rapid disease course of which accelerated cognitive decline is an integral feature.5,9,10

Clinical guidelines advising the use of cholinesterase inhibitors primarily according to Mini-Mental State Exam (MMSE) scores may inadvertently discount the importance of their use for NPS when evidence is accumulating of their usefulness.11 Prevalence studies, therefore, provide vital cues to individuals involved in the treatment of dementia to remain alert to the presence of noncognitive symptoms.

The aims of the present study were to determine the prevalence, persistence, and potential associations of NPS in Alzheimer disease (AD) and to gather information regarding caregiver distress associated with individual symptoms. This study is one of the largest conducted to date (more than 400 patients) and employed the NPI,12 a comprehensive, structured, and objective rating instrument designed and validated specifically for use in dementia. Although the study is cross-sectional, we have improved the reliability by questioning only those caregivers with an intimate knowledge of the patient's symptoms.

METHODS

Subjects

Ethical approval was obtained from the Queen's University of Belfast Research Ethics Committee, and the patient or next-of-kin provided written informed consent. We enrolled 435 patients identified from oldage psychiatry and geriatric medical clinic records who met the criteria for diagnosis of probable AD, as defined by the National Institute of Neurological and Communicative Disorders and Stroke and the Alzheimer Disease and Related Disorders Association (NINCDS-ADRDA).13 Patients with MMSE14 scores over 23/ 30 were included if all other criteria were satisfied. Dementia had to be present for at least 3 years to allow time for the emergence of aberrant behaviors. Information concerning the patient was provided by a suitable caregiver who had been in contact with the patient a minimum of 3 times per week for a minimum of 3 years. For 12 patients, the caregiver failed to meet one of these criteria, and a second caregiver (usually a second relative or nurse) who fulfilled the remaining criterion was also interviewed, and information was gathered as to the presence or absence of each symptom in question. Patients' functional status was assessed with the Functional Assessment Staging (FAST) survey,15 a tool with specific validity for advanced dementia. Behavioral and psychological symptoms were recorded with the NPI With Care-giver Distress (NPI-D),12 with reference to 1) the preceding month, and 2) symptoms appearing during the entire course of the dementia. Total Caregiver Distress was calculated as the sum of caregiver distress in each of the 12 domains.

Information regarding age, gender, family history of dementia, previous psychiatric history or head injury, educational status, residence, and use of CNS-acting drugs was also gathered during the interview with the caregiver.

Statistical Analysis

All significance tests were two-tailed; significance was defined as p <0.05. For correlations, significance was defined as Spearman's rank correlation coefficient ≥0.4 and p <0.05. The ≥0.4 criterion was included in order to avoid correlations that were too small to be of any genuine relevance. "Unsure" responses were treated as missing values. Comparisons of means were performed with the Student f-test and the Mann-Whitney z test for nonparametric samples. Chi-square analysis was used to test relationships between symptom frequency and MMSE. A univariate analysis of variance model using tests of between-subjects effects was used to analyze linear relationships involving continuous variables. A Kaplan-Meier survival analysis was performed, using symptom duration data and onset times (incorporating ongoing symptomatology as censored data). Analyses were performed using SPSS Version 11.

RESULTS

Patient Characteristics

Demographic and clinical data are shown in Table 1. Sixty-six percent of participants were women. The mean age was 78 years, and mean age at onset was estimated at 72 years. Women subjects were significantly older: mean 79 years (women) versus 76 years (men) (t= -3.237; p = 0.001). Women were significantly more cognitively impaired (mean MMSE: 12/ 30 (women), 14/30 (men) (Mann-Whitney z = - 2.269; p = 0.023) despite there being no meaningful difference in estimated duration of dementia: mean 5.6 years (women), 5.8 years (men) (Mann-Whitney z = -0.020; p = 0.979). The mean overall MMSE was 13 and median FAST score 6-b. The mean total NPI-D score was 41/ 144. We observed positive correlations between total NPI-D behavior score and FAST functional score (r = 0.5; p <0.01) and total NPI-D score and MMSE score (r = 0.4; p <0.01).

The most common initial symptom was memory impairment (affecting 65% of the patients). "Change in behavior" was the presenting complaint in 15% of patients. Psychiatric symptoms, particularly depression, delirium, or suspiciousness, were less common presenting symptoms (4%). A previous history of alcohol abuse and history of psychiatric illness were noted in 4% and 10%, respectively. Major head injury occurred in 6%. A family history of dementia (more than one first-degree relative) was recorded in 9%. Most patients (84%) had been educated to secondaryschool level, with 7% to tertiary level; only 9% had not received any education beyond primary level.

With respect to previous or current psychotropic drug use since the onset of dementia, 63% had been treated with cholinesterase inhibitors, 32% with antipsychotics, 27% with benzodiazepines, and 24% with antidepressants. Only 2% had previous or current exposure to all four classes of drug, whereas 12% and 30% recorded exposure to three and two classes of drugs, respectively; 13% of patients were not exposed to any of the four drug categories.

TABLE 1. Demographic and Clinical Data Overall and by Gender

The majority of patients (64%) lived at home, either with a caregiver (53%) or alone (11%). Figures for institutional settings were the following: residential home (5%), nursing home (24%), Elderly Mentally Infirm (EMI) unit/ward (6%).

Neuropsychiatric Symptom Prevalence Data

The frequency of positive responses to each of the 12 NPI-D domains is shown in Table 2. Only 35 of the 435 participants failed to record any positive "Yes" responses across the 12 NPI-D domains (9%). The most common symptoms within each domain are also shown.

With reference to the entire duration of the dementia until the point of sampling, apathy/indifference was the most common behavioral symptom (76%), followed by ab\errant motor behavior (65%), appetite/eating changes (64%), irritability/lability (63%), and agitation/aggression (63%). Sleep disturbance was the least common behavioral symptom (54%). Depression/dysphoria (54%), anxiety (50%), and delusions (50%) were the most common psychological symptoms. Disinhibition (30%), hallucinations (28%), and elation/ euphoria (17%) were less common psychological symptoms. Overall, the single most common "Yes" answer was in response to the question "does the subject seem less spontaneous and less active than usual?," involving 65% of all study participants. Estimated times to onset are summarized in Table 3, calculating median time-to-onset from a survival analysis. Depression/dysphoria and apathy/ indifference were the earliest, and hallucinations, elation/ euphoria, and aberrant motor behavior the latest symptoms to appear, respectively.

A survival analysis showing the persistence of each symptom domain over time is shown in Figure 1, where the proportion of patients retaining the symptom is plotted against time (in months). From the plot, it is evident that apathy was the most persistent symptom; psychotic symptoms, delusions, and hallucinations exhibited the most rapid disappearance over time.

TABLE 2. Frequency of Neuropsychiatric Symptoms (NPSs) in 435 AD Patients, as Assessed Using the NPI-D Questionnaire

TABLE 3. Estimated Median Onset Time for Each Domain, Median NPI- D Total Score, and Median Caregiver Distress Score

NPI-D composite scores of information gathered during the course of the dementia (frequency X severity) indicate that apathy, appetite/eating disturbance, sleep disturbance, and aberrant motor behavior are most problematic in terms of severity and frequency of behavior; the composite scores for psychological symptoms were generally lower (Table 3).

Mean total NPI-D score (relevant to information gathered during the course of the dementia), mean MMSE, and mean FAST score varied according to place of residence, as shown in Table 4. There was a general increase in NPS "load" following the sequence Home < Home Alone < Residential Home < Nursing Home/Ward < EMI Home/Psychiatric Ward. Functioning and cognition deteriorated between community and institutional settings (Table 4). Figure 2 is a graphic representation of variations in MMSE, FAST7 and NPI-D, according to place of residence.

FIGURE 1. Survival Analysis Showing the Disappearance of Each Symptom Domain With Time

Relationship Between Neuropsychiatric Symptoms and Cognition

The occurrence of some symptoms as recorded relevant to the month before interview varied according to the degree of dementia (Table 5). After Bonferroni correction, irritability/lability was significantly associated with an MMSE score >20 (p = 0.003); hallucinations were significantly associated with MMSE <10 (p = 0.048); all other domains showed no statistical relationship with MMSE.

Caregiver Distress

The symptoms that caused caregivers the most emotional distress (mean score 4/5: "severely distressing") were sleep disturbance, aggression/agitation, and depression/dysphoria. All other domains averaged 3/5 ("moderately" distressing), other than hallucinations and elation/euphoria (mean caregiver distress score: 2/5, "mildly distressing"). Mean caregiver distress, according to place of residence, MMSE, NPI-D score, and functional capabilities, is summarized in Table 4. Mean total care-distress was significantly related to total NPI-D score (Spearman's rank: r = 0.8; p <0.01) but not MMSE, FAST, or place of residence. A univariate analysis-of- variance model using a test of between-subjects effects showed that the relationship between NPI-D score and extent of caregiver distress was uninfluenced by current place of residence (Figure 3).

DISCUSSION

Our results indicate that NPS are very common in patients in mid- and late-phase AD, despite high recorded rates of drug use (accepting that non-pharmacological treatment strategies were not assessed). These symptoms are frequent, severe, and cause significant distress for caregivers. The extent of neuropsychiatric symptomatology correlates with the degree of cognitive failure and loss of functional capabilities, and some symptoms are related to MMSE. Importantly, 80% of symptom domains resuited in caregiver distress rated "moderately" or "severely" distressing.

TABLE 4. Differences in Mean Total NPI-D Score, Mean MMSE, Mean FAST Score, and Mean Total Caregiver Distress, by Place of Residence

FIGURE 2. Graphic Representation of Variations in MMSE, FAST, and NPI-D According to Place of Residence

TABLE 5. Chi-Square Analysis of NPI-D Domain, by MMSE Grouping: <10, 10-20, and >20, N (%)

The observation that 91% of patients have at least one positive NPI-D domain reflects the vast neuropsychiatrie load associated with AD and concurs with longitudinal studies.16-18 Our estimated prevalence rates across the 12 NPI-D domains are generally higher than previous studies using the NPI-D,19-22 although comparable in several domains to the rates observed in other cross-sectional studies when the advanced stage of the cohort is considered.23-30 Notwithstanding, several symptom categories, namely psychosis (delusions [50%]); hallucinations [28%]); aspects of affect, such as elation/euphoria (17%); irritability (63%); and abnormal motor behavior (65%) are higher than earlier reports. Some of the high endorsement rates may be due to the "devil/halo" bias effect; that is, the idea that declaration of one item may bias other item reporting. Overestimation of symptoms may be caregiver-related, particularly if they themselves are under stress, as this report demonstrates. Differences in study design create additional conflict between published data: these include the use of non-comparable assessment instruments, differences in sample size, and accepted shortcomings associated with cross-sectional rather than longitudinal methodology, particularly where symptoms are stage- specific, short-lived, or responsive to management interventions. The characteristics of patients drawn from different referring sources and places of residence will naturally influence the prevalence of NPS.

FIGURE 3- Relationship Between Degree of Caregiver Distress and Neuropsychiatric Load, by Place of Residence

We confirmed the assumption that the degree of neuropsychiatrie symptomatology correlates with the extent of cognitive failure.24,31,32 The relationship between the emergence of individual NPS and the phase of cognitive dysfunction is still under investigation. Depression may act as a risk factor for dementia or simply represent an early accompaniment to the dementing process.33,34 There was no clear relationship between degree of cognitive impairment and prevalence of depressive symptoms in this study, although depressive and apathetic symptoms were the earliest to appear. Symptoms such as psychosis, agitation, anxiety, and abnormal physical behaviors characteristically develop in the more advanced stages of the disease.24,25,34 Onset times noted in this study were comparatively late for hallucinations and aberrant motor behavior. The data on psychotic symptoms showed that hallucinations were significantly more common in those with MMSE scores below 11. Unexpectedly, irritability/lability was associated with MMSE scores over 20, and this may reflect preservation of patient awareness of his or her difficulties and represents an area for further investigation.

A graphic model showing the persistence of symptoms over time was demonstrated: psychotic symptoms were comparatively transient as judged against more persistent symptoms of apathy. This observation concurs with the longitudinal work of Haupt et al.18 Delusional and hallucinatory activity of a more "moderately persistent" nature was recorded elsewhere.23

Ten out of the twelve domains produced caregiver distress rated 3 out of 5 or above: agitation/aggression and dysphoria/depression were most troublesome, and this finding concurs with other studies.2,3 As noted by others,1 mean total care-distress was statistically related to total NPI-D score but not with MMSE nor FAST, although this is not to underestimate the difficulties caregivers face when dealing with cognitive and functional decline. Notably, caregiver distress was unrelated to the patient's place of residence. One might assume that the decision to shift the patient to a setting of higher dependency, such as a nursing home, although emotionally difficult at the time, reduces the emotional burden the caregiver experiences through reduced direct exposure.36 These results would not support this assumption.

The strengths of the present study include its size (one of the largest cross-sectional studies conducted to date), its use of a structured, objective psychiatric assessment instrument designed and validated specifically for neuropsychiatrie symptoms in dementia, and its use of caregivers with close knowledge of the patient throughout the course of dementia. However, it is limited by its retrospective nature and dependence on caregiver recall. We have tried to improve the reliability by including only those caregivers with an intimate knowledge of the patient. Although medication use was recorded, its influence on NPS was not assessed,37 nor did we assign too much significance to previous psychiatric history in terms of its influence on promoting dementia-related NPS. Some symptoms, such as depression, are perhaps more thoroughly assessed by specific depression scales.38 Yet, as experts continue to refine the definition of what constitutes depression in dementia,39,40 we recognize that tearfulness, guilt, and loss of interest (which the NPI-D efficiently captures) are perhaps more appropriate targets for treatment in this group than the more florid presentations of major depressive disorder.

We hope this work serves as a useful reminder to personnel involved in the treatment of patients \with AD and their caregivers. Clinicians, tempted to manage patients according to guidelines that erroneously emphasize cognitive failure as the primary measure of treatment need and success, must remain alert to the frequent and devastating nature of these neuropsychiatric symptoms.

Drs. Passmore and McIlroy are beneficiaries of an AD Society 3- year Project Grant. Dr. Craig is sponsored by an Ulster Garden Villages Research Grant and a British Geriatrics Society Senior Registrar Start-up Grant.

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David Craig, M.R.C.P., Ajay Mirakhur, B.Sc.

Dominic J. Hart, M.R.C.P., Stephen P. McIlroy, Ph.D.

A. Peter Passmore, M.D.

Received March 30, 2004; revised June 2, July 21, 2004; accepted July 22, 2004. From the Dept. of Geriatric Medicine, Queen's University of Belfast, Belfast, Ireland. Send correspondence and reprint requests to Dr. David Craig, Dept. of Geriatric Medicine, Queen's University of Belfast, 97 Lisburn Rd, Belfast, Ireland, e- mail: david.craig@qub.ac.uk

2005 American Association for Geriatric Psychiatry

Copyright American Psychiatric Press, Inc. Jun 2005

Source: American Journal of Geriatric Psychiatry, The

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