Many recent studies report that a small proportion of older people perform in the abnormal or borderlinerange on neuropsychological tests [1,2], and that theseabnormalities occur predominantly in the domain of episodic memory [3]. While these people do not meetthe clinical criteria for any neurodegenerative disease,their performance indicates that their cognitive functionsare not normal. Three accounts of the aetiology of suchmild cognitive impairment have been put forwardrecently. The first proposes that it represents the earlystages of Alzheimer’s disease (AD), while the secondproposes that it is a product of normal ageing [4]. Thethird, and most likely, account is that mild cognitiveimpairment is a heterogeneous disorder with multiplepossible outcomes [3–5]. These proposals have beeninvestigated recently through epidemiological, genetic,cognitive and neuroradiological studies of older peopleclassified as having mild cognitive impairment. Resultsfrom these studies have been varied, which has added tothe current confusion and contradiction occurring in theageing and dementia literature. We argue that the majorcause of this confusion is the inconsistency among the
An analysis of systems of classifying mildcognitive impairment in older people
Alexander Collie, Paul Maruff
Objective:
Over the past two decades, a number of systems have been developed for theclassification of cognitive and behavioural abnormalities in older people, in order that indi-viduals at high risk of developing neurodegenerative disease, particularly Alzheimer’sdisease, may be identified well before the disease manifests clinically. This article criticallyexamines the inclusion and exclusion criteria of a number of such classification systems,to determine the effect that variations in criterion may have on clinical, behavioural andneuroimaging outcomes reported from older people with mild cognitive impairment.
Method:
Qualitative review of the literature describing systems of classifying mild cognitiveimpairment, and outcomes from clinical, behavioural, neuroimaging and genetic studies ofolder people with mild cognitive impairment.
Results:
The exclusion and inclusion criteria for these classification systems varymarkedly, as do the design of studies upon which the validity of these systems has beenassessed. Minor changes to individual exclusion/inclusion criterion may result in substan-tial changes to estimates of the prevalence and clinical outcome of mild cognitive impair-ment, while inadequate experimental design may act to confound the interpretation ofresults.
Conclusions:
As a result of these factors, accurate and consistent estimates of theoutcome of mild cognitive impairments in otherwise healthy older people are yet to beobtained. On the basis of this analysis of the literature, optimal criteria via which accurateclassifications of mild cognitive impairment can be made in future are proposed.
Keywords:
cognitive impairment, ageing, memory, diagnosis, neuropsychology.
Australian and New Zealand Journal of Pschiatry 2002; 36:133–140
Alexander Collie, Centre for Neuroscience, The University of Melbourne(Correspondence); Paul Maruff, School of Psychology, Latrobe University
Neuropsychology Laboratory, Mental Health Research Institute of Victoria, Locked Bag 11, Parkville, Victoria 3052, Australia.Email: alex@neuro.mhri.edu.au
Received 11 October 2000; revised 24 August 2001; accepted 28 August2001.
CLASSIFYING MILD COGNITIVE IMPAIRMENT134
many different systems that are currently used to clas-sify mild cognitive impairment (hereafter referred to as‘classification systems’).Identifying older people at high risk for AD is impor-tant for both the patient and their carers as it may allowtherapeutic intervention in the very earliest stages of thedisease, which in turn may delay or even prevent theonset of the disease process. In the worst case it allowsfor the planning of patient care. Such identification iscurrently hampered by the use of inadequate and incon-sistent diagnostic criteria for mild cognitive impairment.Nine such criteria have been developed, and a numberof other terms have been used to describe cognitivedysfunction in older individuals. Table1 describes theseterms and provides an acronym for each. As well asbeing an individual classification system, the term mildcognitive impairment is used increasingly to describecognitive dysfunction associated with ageing. Used inthis context, the term mild cognitive impairment impliesthat the different classification systems may be uniformand comparable, however, as discussed below this is notthe case. Because there are so many terms used for thisphenomenon (see Table2),
mild cognitive impairment
will be used in this review to describe the concept of cog-nitive impairment associated with ageing that is notclearly dementia. The acronyms listed in Table2 will beused when referring to individual classification systems.In order to determine whether mild cognitive impair-ment represents the earliest stages of AD, recent studieshave followed individuals classified as impaired accord-ing to one of the many available criteria over time(Table2).Other recent studies have sought to determinewhether impaired older individuals show increased ratesof other risk factors for AD, including the apolipoproteinE (ApoE) epsilon 4 allele, hippocampal volume reduc-tion, and self-reported memory loss (Table2). Bothtypes of investigation hypothesize that cognitivelyimpaired older individuals are at greater risk of devel-oping AD than non-impaired individuals. Despite manysuch studies being conducted recently, there is still dis-agreement about the clinical significance and outcomeof mild cognitive impairments in older people. In fact,there is still debate about the population prevalence of such impairment among older individuals [5]. Potentialreasons for these differences include inconsistent inclu-sion and exclusion criteria (Table3), and variation instudy design (e.g. sample size, baseline/follow-up inter-val), both of which may have considerable effects onstudy outcome. This review aims to compare and con-trast the inclusion and exclusion criteria of the publishedsystems for classifying mild cognitive impairment, andto determine the effects that changes to these criteriamay have on study outcome. The effect that differencesin experimental design may have on conclusions drawnfrom recent studies will also be considered. Based onthis analysis of the literature, optimal criteria for theaccurate identification of mild cognitive impairmentsare proposed.
Table1.Diagnostic and descriptive terminology for mild cognitive impairment in older people
Acronym Title Reference
AACDAgeing Associated Cognitive DeclineLevy [34]AAMIAge-Associated Memory ImpairmentCrook
et al
. [35]ACMDAge Consistent Memory DeclineCrook [24]ACMIAge Consistent Memory ImpairmentBlackford and La Rue [36]ARCDAge-Related Cognitive DeclineDSM-IV [11]ARMDAge-Related Memory DeclineBlesa
et al
. [37]BSFBenign Senescent ForgetfulnessKral [38]IMDIsolated Memory DeclineSmall
et al
. [12]IMIIsolated Memory ImpairmentBerent
et al
. [39]IMLIsolated Memory LossBowen
et al
. [40]LCDLimited Cognitive DisturbanceGurland
et al
. [41]LLFLate Life ForgetfulnessBlackford and La Rue [36]MCDMild Cognitive DisorderReisberg
et al
. [25]MCIMild Cognitive ImpairmentPetersen
et al
. [2]MDMinimal DementiaRoth
et al
. [42]MNDMild Neurocognitive DisorderDSM-IV [11]QDQuestionable DementiaMorris
et al
. [8]DSM-IV=Diagnostic and Statistical Manual of Mental Disorders–Version 4, published by the American Psychiatric Association(1994).
A. COLLIE, P. MARUFF135
Inclusion and exclusion criteria
Memory impairment
All published classification systems propose as aninclusion criterion evidence of a memory deficit (Table3).This arises from repeated findings that memory is thefirst cognitive domain affected by the AD process [2,3,6],and is also affected by the normal ageing process [7].However, the classification systems differ as to whetherthe memory impairment needs to be identified objec-tively. For example, the Age-Associated Memory Impair-ment (AAMI) and Mild Cognitive Impairment (MCI)criteria require that memory test performance be abnor-mal relative to a control group, whereas the Age-RelatedCognitive Decline (ARCD) criterion requires only a sub- jective report of problems recalling names and events. Of those classification systems that require objective evi-dence of a memory deficit, there are differences betweenthe composition of the group against which memory testperformance is compared. For example, the comparisongroup specified by the AAMI criterion is normal youngadults, whereas the MCI criterion requires an age-appropriatecontrol group. Healthy young people gener-ally have superior memory test performance than healthyolder people [7], and it is therefore likely that a greaterproportion of older individuals will be classified asimpaired when the AAMI criterion is employed. Thecomposition of groups of impaired subjects classifiedaccording to AAMI and MCI criteria are also likely to bedifferent, and their relationships to outcome measures(e.g. prevalence, progression to AD) not comparable [4].
Other cognitive impairment
Some classification systems propose that memoryimpairment be accompanied by deficits in other cog-nitive domains, although this is not required universally(Table3). For example, an individual can be classified ashaving Questionable Dementia (QD) when mild impair-ments are evident in a number of cognitive domains. Incontrast, the criteria for AAMI specifies that cognitiveprocesses other than memory remain unaffected. Deficitsin cognitive domains other than memory occur predom-inantly in more advanced stages of AD [8] or in otherneurodegenerative diseases (e.g. vascular dementia [9]),whereas the earliest stages of AD are characterized by anisolated memory impairment [3,10]. Therefore, classifi-cation systems which require impairment in multiplecognitive domains are likely to identify individuals in
Table2.Results from selected studies of older people classified as impaired according to different systems
Study System of Outcome ResultClassification measure
Smith
et al
. [5]AAMIPrevalence7–96% depending on memory test usedBarker and Jones [22]AAMIPrevalence15–58% depending upon criteriaBarker
et al
. [43]AAMIPrevalence5.8–15.8% depending on individual criteriaSoininen
et al
. [44]AAMIBrain volumeNormal hippocampal volume; hippocampal asymmetryForstl
et al
. [29]AAMIBrain volume
↓
hippocampal volumeLaakso
et al
. [45]AAMIBrain volumeNormal amygdala volumeKrasuski
et al
. [46]MCIBrain volume
↓
entorhinal, hippocampal, amygdale volumeJack
et al
. [47]MCIBrain volume
↓
hippicampal volumeTierney
et al
. [48]N/SClinical outcome24% develop AD 2years after baselineBowen
et al
. [40]IMLClinical outcome48% develop AD 31months after baselineBerent
et al
. [39]IMIClinical outcome50% develop AD 3years after baseline; 15% pseudodementiaPetersen
et al
. [2]MCIClinical outcome48% develop AD 2years after baselineForstl
et al
. [29]AAMIApoE genotype58% carry e4 allele;Blesa
et al
. [37]ARMDApoE genotype56% carry e4 allele; 37% e3/3 homozygous; 4% carry e2 alleleBartres-Faz
et al
. [49]AAMIApoE genotype18% carry e4 allele; 64% e3/3 homozygous; 18% carry e2 alleleHanninen
et al
. [50]AAMICognitive function
↓
executive function performanceFowler
et al
. [28]QDCognitive function43% display
↓
episodic memory function over 12 month periodPetersen
et al
. [2]MCICognitive function
↓
episodic memory performanceAAMI=Age-Associated Memory Impairment; MCI=Mild Cognitive Impairment; ARCD=Age-Related Cognitive Decline;IML=Isolated Memory Loss; IMI=Isolated Memory Impairment; QD=Questionable Dementia;
↓
=decreased; AD=Alzheimer’sdisease; ApoE=Apolipoprotein; N/S=system of classification system not specified. Results from studies of older people classifiedas having cognitive impairment can vary substantially according to the criteria used to classify impairment. This is true for a numberof different outcome variables, including estimated prevalence of impairment, brain volume measured with Magnetic ResonanceImaging, apolipoprotein E genotype, clinical outcome (the number of people subsequently meeting criteria for AD), andperformance on tests of cognitive function.
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Mild Cognitive Impairment in Older People
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