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Keywords:

  • aging;
  • Alzheimer's disease;
  • behavior;
  • caregiver;
  • dementia;
  • old

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. METHODS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES

Background:  Advancing age increases the risk of developing dementia. Recent studies have clarified characteristic cognitive changes in very old patients with dementia. Although non-cognitive symptoms are frequent in dementia, relatively little attention has been paid to the nature of behavioral and psychological symptoms of dementia (BPSD).

Methods:  A retrospective review of a database was performed to compare 27 very old patients with Alzheimer's disease (AD) (onset age ≥ 85) with 162 less old patients (onset age < 85). Cognitive decline, ability to carry out activities of daily living (ADL), and overall severity were rated. BPSD were evaluated using a 16-item questionnaire to the compare frequency of each symptom between old and very old groups.

Results:  Cognitive decline was equivocal in both old and very old groups. In contrast, very old patients were more impaired in ADL, and BPSD were more frequent in very old patients. Delusions, irritability, and delusional misidentification syndrome were frequent in both groups, but were more prominent in very old patients. Behavioral abnormalities such as excitement, delirium, reversed diurnal rhythm, and wandering were not prominent in old patients, but were frequent in very old patients.

Conclusions:  Very old AD patients presented more frequent BPSD than old AD patients. Troublesome behavioral abnormalities particularly prominent in the older patients might represent a heavy burden for caregivers.


INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. METHODS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES

Japan is among the countries with the most elderly in the population; the number of very old people including octogenarians, nonagenarians, and centenarians is estimated at approximately 14 000 000. This very old population subgroup has been recognized to have distinctive characteristics concerning personality,1,2 general cognitive decline,3 and problems in specific cognitive domains.4,5

Advancing age is a risk factor for dementia. More than one-fourth of individuals above 85-year develop dementia. Very old patients with dementia have been reported to show unique findings with respect to neuropathology6 and to apolipoprotein E4.7 In addition, recent studies have examined characteristics of cognitive changes from the neuropsychological perspective.8–10 Although non-cognitive symptoms are a frequent feature of dementia, relatively little attention has been paid to the nature of behavioral and psychiatric abnormalities in very old patients with dementia. Recently, such problems have been categorized as behavioral and psychological symptoms of dementia (BPSD).11,12 Hori et al. compared 11 late-onset nonagenarian patients with Alzheimer's disease (AD) to 13 younger patients with early onset.13 They concluded that the nonagenarian patients showed more frequent troublesome behavior while tending to demonstrate relatively preserved cognitive function. In the present study we compared characteristics of BPSD in very old AD patients with those in younger patients.

METHODS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. METHODS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES

Subjects were: 189 consecutive outpatients (50 men, 139 women; mean age 81.5 years ±6.2 years) who first consulted Yokufu-kai Geriatric Hospital, Tokyo, Japan between April 2000 and March 2002 and who had probable AD according to National Institute of Neurological and Communicative Disorders and Stroke – Alzheimer's Disease and Related Disorders Association (NINCDS-ADRDA) criteria.14 Subjects were divided into two groups according to age at onset of dementia: 27 very old patients (onset at ≥85 years) and 162 less old patients (onset at <85 years). Demographic data for each group including age, sex, age at onset, and duration of illness are shown in Table 1. No difference was evident for duration of illness between the two groups.

Table 1.  Demographic data
Group Age at onsetOld <85Very old ≥85P
n16227 
Men : women 41 : 121 9 : 18 0.52
Mean age (SD), years 80.0 (5.3)90.5 (2.6)<0.0001
Mean duration of  illness (SD), years  3.3 (2.0) 2.8 (1.5) 0.42

Cognitive performance, ability to carry out activities of daily living (ADL), and overall severity were rated. BPSD were evaluated using a 16-item questionnaire to compare frequency of these symptoms between old and very old groups.

Database information for each patient was reviewed retrospectively. The mini-mental state examination (MMSE)15 was used to assess general cognitive decline, and functional assessment staging (FAST)16 to quantify overall functional severity. The Nishimura-scale (NM) and the Nishimura Activities of Daily Living scale (N-ADL)17 were used as indices of ADL status. Results of MMSE, NM scale, and N-ADL were analyzed with the Spearmann rank order correlation and the Mann–Whitney U-test. Information concerning the presence of each BPSD was obtained from each caregiver using the 16-item questionnaire, which included 10 items from the Neuropsychiatric Inventory (NPI),18,19 (delusion, visual hallucinations, excitement, depression, anxiety, euphoria, indifference, disinhibition, irritability, and abnormal behavior) and six other cognitive and behavioral domains (delusional misidentification syndrome (DMS), confabulation, delirium, reversed night/day rhythm, wandering, and becoming lost). Presence of each BPSD was compared between very old and old groups using χ2-tests.

Among various BPSD, the most troublesome problems, which heavily burden caregivers, have been listed by the International Psychogeriatric Association (IPA)11 as group 1 symptoms. Such group 1 symptoms have been classified further into psychological symptoms including hallucinations, delusion, depressed mood, sleeplessness, and anxiety (group 1P) and behavioral abnormalities including physical aggression, wandering, and restlessness (group 1B). Mean numbers of group 1P and group 1B symptoms for each group were computed, and were subjected to one-way analyzes of variance (anova) with FAST stage as an independent variable.

Since the two groups examined were defined according to age at onset, an old group could have a wider range of illness duration than a very old group. To further clarify early clinical symptoms of very old patients as opposed to old patients, only patients with a duration of illness within 3 years were analyzed (n = 75; Table 2). Prevalence of each BPSD was compared between very old and old groups using χ2-tests.

Table 2.  Comparison of cognitive decline, activities of daily living level, and overall severity in two groups of Alzheimer's disease patients
GroupOldVery oldP
  1. MMSE, mini-mental state examination; N-ADL, Nishimura activities of daily living scale; NM-scale, Nishimura-scale (NM); FAST, functional assessment staging.

MMSE, mean (SD)17.4 (6.1)15.8 (6.4)0.20
N-ADL, mean (SD)50.7 (9.1)45.7 (11.1)0.01
NM scale, mean (SD)28.9 (6.6)25.8 (6.8)0.06
FAST stage
 315 0 
 47311 
 55511 
 619 50.29

RESULTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. METHODS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES

Cognitive decline, overall severity and activities of daily living

Considering all of our AD, patients’ cognitive decline as measured by MMSE, overall severity as measured by FAST, and functional and ADL status according to the NM scale and N-ADL demonstrated good correlations with one another (MMSE vs FAST, r = −0.65; MMSE vs N-ADL, r = 0.54; MMSE vs NM scale, r = 0.75; FAST vs N-ADL, r = −0.59; FAST vs NM scale, r = − 0.76; N-ADL vs NM scale, r = 0.61; all P < 0.0001).

No significant differences were obtained in the MMSE between very old and old groups. FAST stage did not differ significantly between the two groups, but none of the patients in the very old group were classified in stage 3. N-ADL showed a significant difference between the two groups, indicating lower ADL scores in the very old group. Detailed consideration of sub-scores indicated inter group differences in all physical activities such as dressing (7.7 ± 2.1 vs 6.5 ± 2.2), bathing (7.7 ± 3.0 vs 6.3 ± 3.2), eating (9.2 ± 1.2 vs 8.6 ± 1.6), and toileting (8.5 ± 2.5 vs 7.3 ± 3.5). The total score on the NM scale approached significance (P < 0.06), and sub-scores for household activities (5.7 ± 1.6 vs 5.0 ± 1.7) and memory (5.4 ± 1.4 vs 4.6 ± 1.4) showed significant differences (Table 3).

Table 3.  Frequency of individual BPSD in two groups of Alzheimer's disease patients
GroupOldVery oldP
n%n%
  1. BPSD, behavioral and psychological symptoms of dementia; DMS, delusional misidentification syndrome.

Delusions5534.01555.60.05
Indifference6137.71348.1>0.10
Irritability3421.01348.10.007
DMS3320.41348.10.003
Excitement1710.5933.30.004
Reversed rhythm15 9.3829.60.007
Wandering1811.1729.60.06
Becoming lost4024.7622.2>0.10
Abnormal behavior15 9.3518.5>0.10
Confabulation2515.4518.5>0.10
Delirium5 3.1414.80.03
Depression2716.7311.1>0.10
Anxiety11 6.8311.1>0.10
Disinhibition5 3.127.4>0.10
Visual hallucinations9 5.613.7>0.10
Euphoria4 2.500.0>0.10
Any symptom13382.12696.30.08

Characteristics of behavioral and psychological symptoms of dementia

Considered as a whole, 159 of 189 AD patients (84.1%) presented with at least one BPSD. Frequently observed BPSD with more than 20% prevalence included indifference (74/189, 39.2%), delusions (70/189, 37.0%), irritability (47/189, 24.9%), DMS (46/189, 24.3%), and becoming lost (46/189, 24.3%).

Frequency of individual BPSD was compared between very old and old groups. Very old patients presented with more BPSD than old patients. The mean number of BPSD observed was 4.0 ± 1.4 in the very old group and 2.3 ± 1.9 in the less old group (P < 0.0001). As shown in Table 4, frequencies of indifference and becoming lost were similarly high in both groups. Symptoms such as delusions, irritability, and DMS were very frequent in both groups, but were more remarkable in the very old group. In contrast, behavioral abnormalities such as excitement, delirium, reversed diurnal rhythm, and wandering were less frequent in the old group, but more prominent in the very old group.

Table 4.  Demographic data of two subgroups of Alzheimer's disease patients whose duration of illness was within 3 years
Group Age at onsetOld <85Very old ≥85P
n6411 
Men : women20 : 44 3 : 8>0.99
Mean age (SD), years78.7 (4.7)89.7 (2.8)<0.0001
Mean duration of  illness (SD), years 1.6 (0.5) 1.5 (0.8) 0.63

Very   old   patients   presented   with   more   group 1 symptoms than old patients (very old, 2.33 ± 1.3; old, 1.18 ± 1.2; P < 0.0001). Both psychological and behavioral symptoms appeared more frequently among very old than old patients (group 1P symptoms, 1.26 ± 0.9 in the very old and 0.75 ± 0.8 in the old group, P < 0.01; group 1B symptoms, 1.07 ± 1.0 in the very old and 0.43 ± 0.7 in the old group, P < 0.001). Figure 1 depicts prevalence of troublesome BPSD as a function of dementia severity. Individual anova for the old group revealed that group 1B symptoms increased with FAST stage [F2,322 = 4.80, P < 0.01] while group 1P symptoms appeared irrespective of severity of dementia (F2,322 = 0.79, P > 0.10]. In the very old group, both group 1B and 1P symptoms were unrelated to FAST stage [group 1P, F2,52 = 0.31, P > 0.10; group 1B, F2,52 = 0.63, P > 0.10).

image

Figure 1. Numbers of (a) group 1P symptoms and (b) group 1B symptoms as a function of functional assessment staging (FAST) stage. (◆) very old; (▪) old.

Download figure to PowerPoint

Characteristics of patients studied within 3 years after onset

Table 5 shows results for MMSE, NM scale, N-ADL, and FAST stage in patients within 3 years after onset. The results paralleled findings in the larger group of patients, in that very old patients presented with similar MMSE scores and FAST stages, but worse NM scale and N-ADL scores than old patients. Table 6 compares individual BPSD between very old and old patients within 3 years of onset of illness. The results indicate that clinical manifestations of AD are determined to some extent by onset age. The number of BPSD observed was 3.8 ± 1.7 in the very old group and 1.7 ± 1.8 in the less old group (P < 0.001). The results again paralleled findings in all patients, in that significant differences between age defined groups were obtained in excitement, irritability, DMS, delirium, and reversed diurnal rhythm, while presence of delusions approached significance.

Table 5.  Comparison of cognitive decline, activities of daily living level, and overall severity in two groups of Alzheimer's disease patients within 3 years after onset
GroupOldVery oldP
  1. MMSE, mini-mental state examination; N-ADL, Nishimura activities of daily living scale; NM-scale, Nishimura-scale (NM); FAST, functional assessment staging.

MMSE, mean (SD)19.7 (5.0)17.6 (7.5)0.42
N-ADL, mean (SD)54.1 (6.6)43.9 (13.1)0.003
NM scale, mean (SD)31.5 (5.6)25.7 (7.4)0.02
FAST stage
 311 0 
 432 4 
 517 5 
 6 4 20.17
Table 6.  Frequency of individual BPSD in two subgroups of Alzheimer's disease patients within 3 years after onset
GroupOldVery oldP
n% n%
  1. BPSD, behavioral and psychological symptoms of dementia; DMS, delusional misidentification syndrome.

Delusions1726.6654.50.08
DMS 4 6.3654.50.0004
Indifference1726.6545.5>0.10
Irritability1015.6545.50.04
Reversed rhythm 3 4.7436.40.007
excitement 3 4.7327.30.04
Anxiety 710.9327.3>0.10
Wandering 710.9327.3>0.10
Confabulation 710.9218.2>0.10
Becoming lost1421.9218.2>0.10
Depression1218.819.1>0.10
Abnormal behavior 3 4.719.1>0.10
Delirium 1 1.619.1>0.10
Visual hallucinations 2 3.100.0>0.10
Euphoria 3 4.700.0>0.10
Disinhibition 1 1.600.0>0.10
Any symptom5078.11090.9>0.10

DISCUSSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. METHODS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES

The present study examined characteristics of very old AD patients who developed the disease after age 85. Cognitive decline as measured by the MMSE was equivalent in the very old and old groups. Bondi et al. argued that a profile of neuropsychological deficits in very old AD lacks the disproportionate prominence of impairment in episodic memory and executive function that is typical of patients who are less old.8 Consequently, very old AD patients appear more similar cognitively to normal controls of comparable age than do less old patients. A similar observation was made by Takeda et al.20 Our results are in accordance with their findings.

In contrast, the level of ADL as shown by N-ADL and the NM scale, showed more deterioration in very old patients than in old patients. Older patients often have poor eyesight and hearing, as well as a higher prevalence of concurrent diseases and general physical decline.21 Together with dementia these unfavorable health conditions may lower ADL scores.

The most striking differences between the two groups were observed in the behavioral and psychological domain, where the very old patients had more evident problems than less old patients. Overall features of BPSD considered in the overall group were consistent with previous findings;22 abulia (indifference) and delusions were the most pervasive BPSD both in very old and old groups.18,19 Delusions were observed more frequently than hallucinations.23 Statistically significant differences between very old and old groups were obtained for delusions, excitement, irritability, DMS, delirium, and reversed diurnal rhythm. The findings are partly consistent with previous studies in that delusions and behavioral disturbance emerged as age increased.23 However, two different determinants could be postulated for the high frequency of such BPSD in older patients with AD: old age per se, and duration from onset. The effect of age could be confounded by interaction between the two factors, causing particular problems in interpreting findings in very old patients with a very long duration. In our study we therefore divided patients into groups according to onset age. In addition, no differences between groups were noted for duration of illness, essentially excluding an effect of duration. When analysis was limited to patients within 3 years after onset, results were comparable to those obtained when including all patients. The findings suggest that very old patients present with more prominent delusions and behavioral abnormalities even soon after onset of dementia. Behavioral disturbance seems to cause more caregiver distress than psychological change.24 Accordingly, caregivers for very old patients could be more distressed than those caring for less elderly patients.

The most troublesome behavioral abnormalities, designed group 1B symptoms, appeared to increase as dementia became more severe. In contrast, psychological  symptoms  (group  1P  symptoms)  were not directly related to dementia severity in very old patients. Haupt et al. reported that clinical variables such as age at entry or dementia severity do not exert substantial influence on non-cognitive symptom patterns.25 However, our results suggest that psychological symptoms and behavioral abnormalities show dissociable patterns with cognitive deterioration and dementia severity. Further investigations are warranted concerning factors affecting non-cognitive abnormalities in AD.

Despite a high prevalence of anxiety and depression reported in the oldest dementia patients in a community study,9 these were not ranked at the top of our present list, partly because of our subject sample. Incidence of depression in very old people in a community sample amounted to 133.49/1000 person years at risk, with demented subjects being at higher risk for depression.26 A similar statement could be made concerning anxiety.27 In contrast to such broad-based epidemiological studies, we investigated AD patients who consulted a geriatric psychiatry clinic. The patients typically presented with troublesome behavior that made home care difficult. In addition, as was recently reported by Isaacowitz and Smith the affect of older adults shows little influence from age.28

Since this is a retrospective study based on a semistructured interview conducted with patients and caregivers on presenting to a hospital clinic, the severity of each symptom was not rated. We currently use the NPI scale for rating and future studies will include severity of each BPSD in very old patients compared with old patients. As the number of very old patients with AD is increasing in Japan, further elucidation of their BPSD is of great importance. Assessment of BPSD is need to plan management of AD patients, and is particularly important to their caregivers.

REFERENCES

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. METHODS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES
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