Concepts and objects of awareness in Alzheimer’s disease: an updated systematic review

Lacerda, Isabel B.; Sousa, Maria Fernanda B; Santos, Raquel L.; Nogueira, Marcela M. L.; Dourado, Marcia C. N.

doi:10.1590/0047-2085000000110

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Jornal Brasileiro de Psiquiatria

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LITERATURE REVIEWS • J. bras. psiquiatr. 65 (1) • Jan-Mar 2016 • https://doi.org/10.1590/0047-2085000000110 copy

Concepts and objects of awareness in Alzheimer’s disease: an updated systematic review

Conceitos e objetos da consciência na doença de Alzheimer: uma revisão sistemática atualizada

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Objectives

To compare and discuss the objects of awareness in Alzheimer’s disease (AD): awareness of cognitive deficits, of functional activities, of social-emotional functioning and behavioral impairment.

Methods

A search in the PsycINFo, Pilots, PubMed/Medline and ISI electronic databases according to Prisma methodology was performed. We included studies about awareness in people with AD published between 2010 and 2015, with the combination of keywords: “Alzheimer AND awareness of deficits”, “Alzheimer AND anosognosia”, “Alzheimer AND insight”, “dementia AND awareness of deficits”, “dementia AND anosognosia”, “dementia AND insight”. The articles were categorized according to the specific object of awareness.

Results

Seven hundred and ten records were identified and, after application of the exclusion criteria, 191 studies were retrieved for potential use. After excluding the duplicates, 46 studies were included. Most studies assessed the cognitive domain of awareness, followed by the functional, social-emotional, and behavioral impairment domains. Memory deficits were not sufficient to explain impaired awareness in AD. Longitudinal studies did not find discrepancies between patients and caregivers’ reports, indicating that awareness is not related to cognition. Conflicting findings were observed, including the relation between awareness, mood, severity of disease, and personal characteristics.

Conclusions

The studies show lack of conceptual consensus and significant methodological differences. The inclusion of samples without differentiation of dementia etiology is associated to symptomatic differences, which affect awareness domains. Awareness in AD is a complex and multidimensional construct. Different objects elicit different levels of awareness.

Awareness; objects of awareness; anosognosia; dementia; Alzheimer

Author/year	Term used	Participants	Study Design	Domains	Awareness measurement	Results
1) Lehrner et al., 2015⁵⁴	Awareness of memory deficits	280 SCD 137 aMCI 181 naMCI 43 AD 28 PD-ch 29 PD-aMCI 58 PD-naMCI 211 HC	Cross-sectional	Cognition Functional	VSRT Delayed Recall scores from FAI scores	The strongest associations were observed between awareness and the domain memory. Further small but significant correlations were also observed for the domains attention, language and executive function
2) Mograbi et al., 2015⁵⁰	Unawareness of memory	829 AD	Cross-sectional	Cognition	Discrepancies between Self-rating and informant rating, and between people self-rating and their performance	The self-report/actual performance variable showed a relationship with cognitive impairments, such as fluency in China and visuospatial abilities in Latin America and India, and behavioral symptoms, such as mania in Latin America and hallucinations in China
3) Vogel et al., 2015¹⁴	Awareness	95 AD	Longitudinal	Cognition Behavioral	AQ-D	Despite overall cognitive decline, awareness was stable over three years in many cases and in some cases even improved awareness was found
4) Sousa et al., 2015¹	Awareness of disease	69 AD (baseline) 55 AD (follow-up)	Longitudinal	Cognition Functional	AISPDD	The first moment of evaluation showed that impairment in awareness was associated to deficits in ADL, cognitive impairments, and higher PwD quality of life ratings. At follow up, impaired awareness was associated to deficits in ADLs, and caregivers’ QoL
5) Mak et al., 2015³⁰	Anosognosia	36 AD 20 MCI 30 HC	Cross-sectional	Cognition Social-emotional	AQ-D	Anosognosia was associated with reduced global cognition and increased apathy in the AD group
6) Chen et al., 2014⁴²	Unawareness of deficits unawareness of memory deficits and unawareness of psychosis or behavioral problems	55 AD	Cross-sectional	Cognition Behavioral	GRAD	Apathy was associated with neither unawareness of memory deficits nor unawareness of psychosis and behavioral problems. Depression was correlated only with unawareness of memory deficits
7) Clare et al., 2012²⁰	Awareness of memory function and functional abilities	101 AD	Cross-sectional	Cognition Functional	MARS-MFS	Two areas of awareness – evaluative judgements of memory function and evaluative judgements of functional abilities show small to medium bivariate correlations with self-reported QoL-AD, with greater awareness related to lower QoL
8) Horning et al., 2014³⁶	Insight	107 AD	Cross-sectional	Cognition Social-emotional	NRS	Insight over and above cognitive functioning appears to play a role in an AD patient’s experience of depressed mood, anxiety, and apathy
9) Conde-Sala et al., 2014²²	Anosognosia	141 AD	Cross-sectional	Cognition Behavioral Functional	AQ-D	Patients with mild deterioration presented less anosognosia, more depression and a QoLp rating that was closer to that of caregivers. Among patients the presence of anosognosia was associated with better ratings of QoLp and with greater severity. Depression and anosognosia were inversely correlated among patients
10) Conde-Sala et al., 2014²³	Anosognosia	119 AD	Longitudinal	Cognition	CAMDEX	Anosognosia was associated with cognitive impairment, and was associated with better perceived QoL-p in moderate dementia, whereas cognitive status did not influence the ratings of these patients, moreover anosognosia and cognition act as independent variables in relation to perceived quality of life
11) Rosen et al., 2014³⁹	Metacognition	12 bvFTD 14 AD 35 HC	Cross-sectional	Cognition	20-item paired associates learning paradigm	Significant impairments in feeling of knowing accuracy in bvFTD and AD
12) Gambina et al., 2014⁴⁷	Awareness of cognitive deficits	79 AD	Cross-sectional	Cognition	AQ-D	Cognitive deficits in executive function, memory and language may mediate the association between capacity and awareness
13) Marková et al., 2014¹⁹	Awareness	101 PwD	Cross-sectional	Cognition Social-emotional Functional	MARS FAQ SEQ	Awareness of memory shows the greatest proportion of negative discrepancies (overestimation of function). Awareness of ADL also shows that a large proportion of negative discrepancies are obtained but in contrast to awareness of memory there is greater variation between individuals and more concordant responses. Awareness of socio-emotional in comparison with the other awareness phenomena shows a higher proportion of positive discrepancies observed in a substantial number of participants
14) Lindau and Bjork, 2014²⁸	Anosognosia	9 AD 12 MCI	Cross-sectional	Cognition Social-emotional	A&A	AD patients rated lower cognitive disabilities relative to the MCI patients, which is here interpreted as one sign of anosognosia in AD
15) Degirmenci et al., 2013³⁸	Cognitive insight	30 AD 15 HC	Cross-sectional	Cognition	BCIS	Self-reflectiveness and self-certainty scores were significantly lower than the controls in patients with AD
16) Zamboni et al., 2013³³	Self-awareness	17 MCI 17 AD 17 HC	Cross-sectional	Functional Cognition	Discrepancies between Self-rating and informant rating	Dysfunction of a network involving medial prefrontal and anterior temporal cortices is associated with the failure in mechanisms necessary for correct and updated self-awareness
17) Massimo et al., 2013³⁵	Self-appraisal	49 bvFTD 73 AD	Cross-sectional	Functional Cognition	Discrepancies between Self-rating and informant rating, and between people self-rating and their performance	BvFTD show significant deficits in self-appraisal across multiple cognitive domains, suggesting a fundamental impairment in self-evaluation and self-monitoring. Observed impaired self-appraisal only for episodic memory in the AD group, suggesting a domain-specific impairment for these patients
18) Amanzio et al., 2013⁴³	Awareness of deficits	117 AD 117 HC	Cross-sectional	Cognition Social-emotional Functional	AQ-D	There is a role for subcomponents of executive functions in impaired awareness of deficits such as inhibition, self-monitoring and set-shifting
19) Mårdh et al., 2013⁴⁰	Metacognition Awareness of disease	15 AD 15 HC	Cross-sectional	Cognition Functional	Self-rating and informant rating	Although patients were aware of their disease, they were not able to realize the practical consequences of their deficit
20) Verhülsdonk et al., 2013²⁴	Anosognosia	49 AD	Cross-sectional	Cognition Social-emotional	AQ-D	Patients had depressive symptoms but were unaware of them in the sense of an ‘‘affective’’ anosognosia. The phenomenon of anosognosia affects not only deficits in cognition and daily functioning, but that it can also manifest itself as non-recognition of affective symptoms
21) Conde-Sala et al., 2013²⁵	Anosognosia	164 AD	Cross-sectional	Cognition Behavioral Functional	AQ-D	More symptoms on the NPI, less depression and greater deficits in ADL, are the most relevant variables that may predict anosognosia. Greater awareness of deficits is related to a reactive depressive mood, especially in the early stages of dementia
22) Van Vliet et al., 2013¹²	Awareness	142 YO-AD 126 LO-AD	Longitudinal	Cognition Social-emotional	GRAD	Patients with YO-AD have higher levels of awareness compared with LO-AD. Intact awareness was associated with depressive symptoms, and this effect was more pronounced in YO-AD compared with LO-AD
23) Maki et al., 2012³⁴	Self-awareness	12 AP 23 AD mild 18 AD moderate 53 caregivers	Cross-sectional	Cognition Functional	AQ-D	Mild AD were generally aware of their deficits even if their assessment was insufficient. In moderate AD, insufficient awareness of deficits was related to memory, and time and spatial orientation
24) Mograbi et al., 2012⁵²	Unawareness of memory	15,022 PwD	Cross-sectional	Cognition	Discrepancies between Self-rating and informant rating, and between people self-rating and their performance	Unawareness should be seen not only as a common neurobiological feature of dementia, increasing with severity of dementia, but also as a phenomenon influenced by social and cultural factors
25) Clare et al., 2012¹³	Awareness	101 PwD	Longitudinal	Cognition Social-emotional	Discrepancies between Self-rating and informant rating	Stability in awareness for the PwD was observed despite increases in dementia-related symptoms and worsening of cognitive impairment, and in the context of no change in psychological or social well-being
26) Mograbi et al., 2012⁴⁹	Awareness of performance	23 AD 21 HC	Cross-sectional	Cognition Social-emotional	Success–failure manipulation	There is dissociation between impaired performance judgement and preserved emotional reactivity to failure in AD
27) Clare et al., 2012²⁰	Awareness	101 PwD	Cross-sectional	Cognition	Discrepancies between Self-rating and informant rating	Indices of awareness and the ratings contributing to these indices are associated with a range of PwD factors, as well as being influenced by carer well being and carer perceptions of PwD
28) Gallo et al., 2012⁴¹	Metacognition	18 AD 18 HC	Cross-sectional	Cognition	AQ-D	AD have relatively preserved metacognitive monitoring abilities on episodic memory tests, at least when the task is relatively well constrained
29) Gilleen et al., 2012¹⁵	Awareness	27 AD	Cross-sectional	Cognition Social-emotional Functional	MARS	Little relationship between awareness and personality scores, but modest associations between awareness and mood, age, and age of onset of first symptoms
30) Martyr et al., 2012⁴⁶	Awareness of functioning	50 AD 29 VaD 17 MD	Cross-sectional	Functional Cognition	Discrepancies between Self-rating and informant rating	Patients with reduced awareness of iADL ability performed better at letter fluency, indicating that awareness of functional deficits may be influenced by letter fluency
31) Spalletta et al., 2012³¹	Anosognosia	103 AD 52 a-MCI 54 md-MCI	Cross-sectional	Behavioral	AQ-D	In the mild AD group, unawareness of behavioral deficits was related to agitation and apathy, whereas global level of anosognosia, was related to aberrant motor behaviors
32) Arsenault-Lapierre et al., 2012²¹	Anosognosia	20 MCI 29 AD 20 HC	Cross-sectional	Social-emotional	AQ-D PSS	Anosognosia for dementia has an impact on psychological markers of stress, but not on physiological markers of stress in AD
33) Mendez and Shapira, 2011³⁷	Loss of insight	12 bvFTD 12 AD	Cross-sectional	Cognition Social-emotional	Self-rating performance	Compared to AD patients, those with bvFTD initially deny the presence of their disorder
34) Ohman et al.; 2011⁴⁸	Awareness of disabilities	8 MCI 18 AD 5 VaD 4 Other dementias	Cross-sectional	Functional	Client-centred assessment	Participants with the same diagnosis and similar ADL process ability measures demonstrated major differences concerning their awareness of disability
35) Amanzio et al., 2011⁴⁴	Reduced awareness of deficits	29 AD 29 HC	Cross-sectional	Cognition	AQ-D	Unaware patients are more impaired in flexible thinking and demonstrate more pronounced behavioural disinhibition and apathy with respect to aware ones
36) Galeone et al., 2011⁵¹	Unawareness for memory deficit	25 MCI 15 AD 21 HC	Cross-sectional	Cognition	Discrepancies by comparison of participants self-report with either participant performance or informant report	Unawareness for memory deficit in AD is an early symptom of their memory disorder and can be seen even in the MCI
37) Schmitter-Edgecombe and Seelye, 2011⁵⁵	Awareness of memory deficits	20 AD 20 HC	Cross-sectional	Cognition	Discrepancies between Self-rating and informant rating	Impaired awareness of memory problems but intact memory-monitoring abilities in an AD population
38) Al-Aloucy et al., 2011²⁷	anosognosia	65 AD	Cross-sectional	Cognition	Mac nair Questionnaire FBI	Anosognosia of memory deficit may be viewed as a generator of other behavioral abnormalities contributing to professional caregivers’ burden
39) Sousa et al., 2011⁴⁵	Awareness of disease	25 AD	Longitudinal	Cognition Functional	AISPDD	As the severity of dementia increases, there is also impaired awareness of disease, together with cognitive and functional deficits
40) Nelis et al., 2011¹⁷	Awareness	51 AD 29 VaD 17 MD	Cross-sectional	Cognition Social-emotional	SEQ	Unawareness of socio-emotional functioning was related to poorer cognitive functioning, suggesting a relationship between stage of dementia and degree of awareness
41) Orfei et al., 2010³²	Anosognosia	38 AD 35 a-MCI 38 md-MCI	Cross-sectional	Cognition Functional Behavioral	CIRS AQ-D	In AD, anosognosia was linked to increased age and reduced ADL. Anosognosia may be primarily affected by factors other than neuropsychological, such as neuropsychiatric symptoms
42) Vogel et al., 2010¹⁶	Awareness	321 AD	Cross-sectional	Cognition Behavioral	ARS	Alzheimer’s disease patients with very poor insight have significantly more neuropsychiatric symptoms than patients who are fully aware of their cognitive deficits
43) Stewart et al., 2010⁵³	Anosognosia of memory	23 AD 30 HC	Cross-sectional	Cognition	Measurement of Anosognosia instrument	AD patients were generally less accurate in evaluating the level of their cognitive abilities than healthy older adults
44) Leicht et al., 2010²⁹	Anosognosia	32 AD	Cross-sectional	Cognition Functional Social-emotional	CIRS, discrepancies by comparison of participants self-report with either participant performance or informant report	Discrepancies were especially pronounced for recent memory, followed by ADL, apathy and attention
45) Williamson et al., 2010¹⁸	Awareness/self-awareness	10 AD 10 FTD 10 HC	Cross-sectional	Cognition Functional	discrepancies between Self-rating and informant rating	FTD and AD patients showed impaired self-awareness of cognitive deficits relative to controls. Comparison across domains suggested greater distortions in self appraisal in FTD patients on a task on which they performed slightly better than the AD patients, and also on tasks on which they performed less well
46) Starkstein et al., 2010²⁶	Anosognosia	213 AD (baseline) 154 AD (follow-up)	Longitudinal	Social-emotional	AQ-D	Anosognosia and apathy in AD increased significantly in severity after a mean period of 18 months. Anosognosia is a significant predictor of apathy in AD

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[1] Address for correspondence: Isabel B. Lacerda. Rua Gabriel Garcia Moreno, 541, casa 1, São Conrado. 22610-360 – Rio de Janeiro, RJ, Brazil. Telephone: (55 21) 99224-2572. E-mail: isabelbvll@hotmail.com