Neuroimaging criteria and cognitive performance in vascular mild cognitive impairment: a systematic review

Sudo, Felipe Kenji; Alves, Gilberto Sousa; Tiel, Chan; Ericeira-Valente, Letice; Moreira, Denise Madeira; Laks, Jerson; Engelhardt, Eliasz

doi:10.1590/1980-57642015DN94000394

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Dementia & Neuropsychologia

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Original Articles • Dement. neuropsychol. 9 (4) • Oct-Dec 2015 • https://doi.org/10.1590/1980-57642015DN94000394 copy

Neuroimaging criteria and cognitive performance in vascular mild cognitive impairment: a systematic review

CRITÉRIOS DE NEUROIMAGEM E DESEMPENHO COGNITIVO NO COMPROMETIMENTO COGNITIVO LEVE VASCULAR: UMA REVISÃO SISTEMÁTICA

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

The recognition of Cerebrovascular Disease (CVD) at earlier clinical stages may favor the control of vascular risk factors and prevention of dementia. However, operational criteria for symptomatic phases at non-dementia stages are often difficult, as the current criteria normally require the evidence of extensive subcortical disease.

OBJECTIVE

To identify the neuroimaging profile of Vascular Mild Cognitive Impairment (VaMCI), the impact of those aspects over cognition and the neuropsychological tests that distinguished VaMCI from other groups.

METHODS

Searches were performed in Scopus, ISI and PsycINFO, using the following key terms: "vascular mild cognitive impairment" OR "vascular cognitive impairment no dementia" OR "vascular cognitive impairment not demented" OR "subcortical mild cognitive impairment".

RESULTS

Of 249 papers, 20 studies were selected. Ten of those included only patients with severe White Matter Hyperintensities (WMH), whereas 10 others admitted subjects with moderate-to-severe WMH. Both groups showed poor performances in Executive Function (EF) tasks in comparison to normal controls and other diagnostic groups. Among EF tests, those assessing "complex" EF abilities consistently distinguished VaMCI from other groups, regardless of the severity of WMH. VaMCI subjects with severe or moderate-to-severe WMH showed cognitive deficits in comparison with other groups. "Complex" EF tests were the most useful in differentiating those patients from the other groups.

CONCLUSION

The occurrence of VaMCI may be associated with the presence of CVD at moderate levels; the detection of vascular damage at earlier stages may allow the adoption of therapeutic actions with significant effect-sizes.

Key words:
cerebrovascular disorders; vascular dementia; cerebral infarction; neurological diagnostic techniques

Author, year	N	Groups	Clinical criteria for MCI	Neuroimaging criteria for SVD	Neuropsychological tests
Frisoni et al., 2002	64	VaMCI, VaD, non-VaMCI	Dysexecutive syndrome + memory impairment + unimpaired complex ADL	Patchy WMH or diffuse symmetrical WMH + 1 lacunar infact	WCST, Category fluency, Letter fluency, Token test, Corsi test, Digit span, Prose recall
Galluzzi et al., 2005	43	VaMCI, non-VaMCI	MMSE ≥ 24, CDR=0.5	Patchy WMH or diffuse symmetrical WMH + 1 lacunar infact	WCST, Category fluency, Letter fluency, Corsi test, Digit Span, Prose recall
Nordahl et al., 2005	42	NC, VaMCI, non-VaMCI	Memory complaints, poor perfomances in Memory tasks, preserved global cognitive performances, unimpaired ADL	WMH extension above the 75th percentile (WMH above 19.375% of total white matter volume)	MMSE, Wechsler Memory Scale Revised, Memory Assessment Scales List Learning, BNT, Block design, Digit Span, Category fluency
Shim et al., 2008	57	NC, VaMCI, non-VaMCI	Objectively measured cognitive decline + unimpaired ADL	Severe WMH, periventricular WMH > 10mm, deep WMH ≥ 25 mm	MMSE, 12-word list from HVLT, Digit span, Rey-Osterrieth Complex Figure Test, BNT, Stroop, Category fluency, Letter Fluency, Go-No Go, Luria Loop test
Moretti et al., 2008	116	VaMCI, atrophic MCI, "cholinergic" MCI	Cognitive complaints + MMSE between 24 and 27, or (MMSE of 28 or higher + Clock Drawing Test of 2/6 or worse) + unimpaired ADL	Number of voxels corresponding to WMH above the upper quartile	Rey word list immediate and delayed recall, Trail Making Test A, B and B-A, Clock Drawing Test, Raven matrices, Inverted motor learning, Rey-Osterrieth Complex Figure Test, Category fluency, Letter Fluency, Token test
Fernández et al., 2011	53	NC, VaMCI, non-VaMCI	Petersen (2001), Frisoni (2002)	Extensive WMH (WMH>3 in semiovale nuclei or >5 mm in deep grey nuclei) or diffuse symmetrical WMH + 1 lacunar infact	MMSE, CERAD (Category fluency, BNT, Word list memory test, constructional praxis, TMT A and B), Digit Span, Abstraction, Letter fluency
Bella et al., 2011	20	NC, VaMCI	Not demented (DSM-IV), MMSE ≥ 24	Severe WMH, periventricular WMH > 10 mm, deep WMH ≥ 25 mm	MMSE, Stroop
Kim et al., 2012	48	VaMCI, VaD	Subjective cognitive complaints; objective cognitive decline below the 1 SD on neuropsychological tests; normal general cognitive function; normal ADL; not demented	Severe WMH, periventricular WMH > 10 mm, deep WMH ≥ 25 mm	MMSE, Digit span, Rey-Osterrieth Complex Figure Test, Seoul Verbal Learning Test, Controlled Oral Word Association Test, Stroop
Lee et al., 2014	207	VaMCI, non-VaMCI	Subjective cognitive complaints, normal ADL, cognitive performance < 16th percentile on tests, absence of dementia, focal neurological symptoms/signs	Severe WMH, periventricular WMH > 10 mm, deep WMH ≥ 25 mm	MMSE, Digit span, Rey-Osterrieth Complex Figure Test, Seoul Verbal Learning Test, Controlled Oral Word Association Test, Stroop
Sheorajpanday et al., 2014	57	VaMCI, non-VaMCI	First presentation of cognitive decline, age ≥ 55 years, intact ADL, not VaD (NINDS-AIREN), presumed vascular cause	Severe WMH, periventricular WMH > 10 mm, deep WMH ≥ 25 mm	MMSE, Wechsler Memory Scale III, Wechsler Adult Intelligence Scale III, TMT A and B, Rey-Osterrieth Complex Figure Test, Digit spam, Category fluency, Letter fluency, Raven matrices

Author, year	N	Groups	Clinical criteria for MCI	Neuroimaging criteria for SVD	Neuropsychological tests
Norlund et al., 2007	180	NC, VaMCI, non-VaMCI	Subjective and objective cognitive impairment for more than 6 months not demented.	Moderate WMH or 2 or more lacunes	Visual Object and Space Perception, Assessment of Subtle Language Deficits, Parallel Serial Mental Operations, TMT
Gainotti et al., 2008	142	NC, VaMCI, non-VaMCI	Long-term Memory performance < 2 scores from cutoff, no cognitive impairment in non-memory domains, preserved functional status	2 or more subcortical infarcts (below 2 cm of size) or 1 subcortical infact + periventricularWMH of any size	RAVLT, Rey-Osterreith Complex Figure, Digit and Spatial Span, phonological and categorical verbal fluency, Raven's Standard Progressive Matrices, Multiple Features Targets Cancellation, Vill's test for temporal rule induction, Stroop interference test
Zhou et al., 2009a	156	NC, VaMCI, non-VaMCI	Cognitive impairment + CDR=0.5 + unimpaired ADL	Wahlund scale ≥ 2 or more than 2 lacunes	MMSE, Digit Span Backwards and Forward, WHO-UCLA AVLT, Rey-Osterreith Complex Figure, Stroop, Semantic Verbal Fluency, WAIS-RC, California Card Sorting Test, CDT
Zhou et al., 2009b	160	NC, VaMCI	Cognitive impairment + CDR=0.5 + unimpaired ADL	Wahlund scale ≥ 2 or more than 2 lacunes	MMSE, Digit Span Backwards and Forward, WHO-UCLA AVLT, Rey-Osterreith Complex Figure, Stroop, Semantic Verbal Fluency, WAIS-RC, California Card Sorting Test, CDT
Norlund et al., 2011	216	VaMCI, non-VaMCI, VaMCI and non-VaMCI with and without biological markers	Cognitive complaint+ objective cognitive decline + not demented + unimpaired ADL	Moderate WMH or 2 or more lacunes	Digit Symbol, TMT, Digit Span, RAVLT, Wechsler's Logical Memory, Rey-Osterreith Complex Figure, Visual Object and Space Perception, Block Design, Token Test, Boston Naming, Semantic Verbal Fluency, Parallel Serial Mental Operations, Dual Task, Stroop, Wisconsin Card Sorting Test, Cognitive Estimation Test
Marra et al., 2011	135	VaMCI, non-VaMCI	subjective and objective cognitive deficits (worse than 1.67 SD from normal values) and normal functional status	Fazekas ≥ 2 or more than 3 lacunes; or Periventricular WMH grade 1 + 2 or more lacunes	Rey's Auditory Verbal Learning Task, Rey-Osterrieth complex figure, Stroop, Multiple Features target cancellation, Phonological and Semantic Verbal Fluency, Raven's Progressive Matrices
Villeneuve et al., 2011	72	NC, MCI with WMH and MCI without WMH	Subjective cognitive complaint + cognitive performance 1.5 SD below normative values + preserved ADL	Wahlund ≥ 2	Mémoria computerized battery, BEM-144, RL/RI word recall Task, Rey-Osterrieth complex figure, Stroop, WAIS-III, Boston Naming Test, Benton judgment of line orientation test
Yi et al., 2012	54	NC, VaMCI	Subjective cognitive complaints, objective cognitive impairments, not demented (DSM-IV), normal ou near-normal functionbal status, CDR= 0.5, MMSE≥ 24.	Moderate to severe WMH in at least 1 region with a Wahlund rating scale score ≥2 and/or multiple pericentricular and deep lacunes	MMSE, AVLT
Sudo et al., 2013	36	NC, VaMCI	Impairment of 1.5 SD below the mean on 1 or more cognitive tests in relation to normative values, preserved or mildly impaired functional activities, (FAQ <5)	Moderate or severe degree of WMH on Fazekas scale and hippocampal atrophy ≤1 on de Leon score (none or questionable atrophy)	MMSE, CAMCOG, CDT, TMT, Semantic Verbal Fluency, Boston Naming Test
Brookes et al., 2015	503	VaMCI, CVD without cognitive impairment	scoring ≤1.5 SD of the normal mean on a given test	lacunar infarcts or lacunar infarcts with leukoaraiosis (Fazekas≥2)	Brief Memory and Executive Test (BMET), MMSE, MoCA

Cognitive functions	Tests
Executive Function (EF)	Shifting	Wisconsin Card Sorting Test (WMST): perseveration, Trail-Making Test (TMT) B, Dual task, Number-Letter sequencing
	Inhibition	WCST: non-perseverative errors and categories, Go/No go, Fist/Edge/Palm sequence, Stroop test
	Working Memory/Update	Digit Span forward and backwards, Corsi test, Parallel Serial Mental Operations, CAMCOG: Working Memory Subtest, Number and Letter sequencing.
	Less specific EF tests	Category and Letter verbal fluency, Luria loop, Raven matrices, Barcelona test (Abstraction subtest), CAMCOG: Abstraction subtest, COWAT, Digit-Symbol substitution test, Cognitive estimation test, WAIS-III(picture interpretation and arrangement, Clock Drawing Test/CLOX 1 (spontaneous drawing), California Card Sorting Test
Visuospatial/visuoconstructive abilities		Block design, Rey figure: copy, TMT A, Visual Object and Space Perception, Lines cancellation test, Clock Drawing Test/CLOX 2. (copy), Multiple Features Target Cancellation
Memory		Prose recall, Babcock Story Recall test, Wechsler Memory Scale-Revised, Memory Assessment Scales, Hopkins Verbal Learning Test, Rey figure: recall and recognition, CAMCOG: Memory subtest, Five-item memory test
Language		Token test, Boston Naming test, Assessment of Subtle Language Deficits
Global Cognition		MMSE, CAMCOG, BMET

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[1] Felipe Kenji Sudo. Av. Nossa Senhora de Copacabana, 895/302 - 22060-001 Rio de Janeiro RJ - Brazil. E-mail: fksudo@gmail.com