Journal of Clinical Neuroscience xxx (2016) xxxxxx

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Journal of Clinical Neuroscience

journal homepage: www.elsevier.com/locate/jocn

Clinical Study

Impaired attention function based on the Montral Cognitive

Assessment in vascular dementia patients with frontal hypoperfusion:
The Osaki-Tajiri project
Kyoko Akanuma, Kenichi Meguro , Yuriko Kato, Yumi Takahashi, Kei Nakamura, Satoshi Yamaguchi
Division of Geriatric Behavioral Neurology, CYRIC, Tohoku University, 4-1, Seiryo-machi, Aoba-ku, IDAC, 980-8575 Sendai, Japan

a r t i c l e

i n f o

Article history:
Received 3 June 2015
Accepted 14 August 2015
Available online xxxx
Keywords:
Frontal lobe
MoCA
SPECT
Vascular dementia

a b s t r a c t
We previously reported that the Montral Cognitive Assessment (MoCA) was effective in the evaluation
of cerebrovascular diseases. We also demonstrated that the test was effective for screening for very mild
vascular dementia (VaD) in the community. Herein, we examined the effectiveness of MoCA in the assessment of patients with VaD in an outpatient clinic. Forty-four patients with VaD (National Institute of
Neurological Disorders and StrokeAssociation Internationale pour la Recherche et lEnseignement en
Neurosciences [NINDS-AIREN] criteria) and 58 patients with Alzheimers disease (AD) (National
Institute of Neurological and Communicative Disorders and StrokeAlzheimers Disease and Related
Disorders Association [NINCDS-ADRDA] criteria) were compared with 67 non-demented control subjects.
All were outpatients at the Tajiri Memory Clinic, Osaki-Tajiri, northern Japan. All underwent 1.5 Tesla MRI
and ethyl cysteinate dimer (ECD) single photon emission computed tomography (SPECT) examinations.
The SPECT images were used to classify the VaD patients into two subgroups, those with frontal hypoperfusion (F-VaD) and those without frontal hypoperfusion. The frontal hypoperfusion pattern was defined
as the P2 pattern of the Sliverman classification, with or without focal hypometabolism in other areas,
based on the agreement of three neurologists who were blinded to the results of the neuropsychological
examinations. Total scores and attention subscores on the MoCA were lower in the F-VaD group compared with other groups. Our results suggest that the MoCA attention subscale can detect VaD participants, particularly those with frontal hypoperfusion.
2015 Elsevier Ltd. All rights reserved.

1. Introduction
Vascular dementia (VaD) is a condition in which decreased
cerebral perfusion causes cognitive deterioration that interferes
with daily life. In contrast with Alzheimers disease (AD), the specific features of episodic memory impairment, apathy and decreased
level of daily activities are the main symptoms of VaD. Executive
dysfunction, based on decreased cerebral blood flow (CBF) or metabolism in the frontal lobe, is thought to be associated with these
symptoms, which may prevent the patients from taking medicine
appropriately and thus lead to worsening of their condition due
to poor control of vascular risk factors [1]. As cerebrovascular diseases (CVD) do not always involve the frontal areas, it is likely that
a remote effect via a neuronal network is responsible.
Three major subtypes of VaD have been proposed: (1) large
infarctions that cause deterioration of at least two cognitive
Corresponding author. Tel.: +81 22 717 7359; fax: +81 22 717 7339.
E-mail address: k-meg@umin.ac.jp (K. Meguro).

domains and subsequently meet the criteria for VaD (historically

referred to as multi-infarct dementia) [2]; (2) multiple lacunar
infarctions together with white matter lesions that cause executive
dysfunction (subcortical VaD) [3]; and (3) infarctions in strategic
areas such as the thalamus or caudate head that cause cognitive
dysfunction [4]. The third type, which we refer to as strategic
VaD, is thought to be a good model for analysis of the neuronal
network, since symptoms such as executive dysfunction cannot
be attributed simply to the function of small strategic areas,
but can be viewed as the expression of dysfunction of the cortical/
subcortical networks.
Diaschisis is a well-known neuroimaging finding in which basal
ganglia infarctions cause hypoperfusion in the ipsilateral cerebral
cortex or the contralateral cerebellar cortex and was originally proposed as the foundation of functional impairment in remote areas.
In early studies, Baron et al. [5,6] investigated the relationship
between cortical energy metabolism and neuropsychological
impairment linked to stroke lesions. As such, impairment was
reflected in the depression of synaptic activity in both the

http://dx.doi.org/10.1016/j.jocn.2015.08.047
0967-5868/ 2015 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Akanuma K et al. Impaired attention function based on the Montral Cognitive Assessment in vascular dementia patients
with frontal hypoperfusion: The Osaki-Tajiri project. J Clin Neurosci (2016), http://dx.doi.org/10.1016/j.jocn.2015.08.047

K. Akanuma et al. / Journal of Clinical Neuroscience xxx (2016) xxxxxx

overlying and remote areas. Functional neuroimaging using single

photon emission computed tomography (SPECT) or positron emission tomography (PET) may be appropriate to study these effects.
We previously reported that VaD with thalamic CVD manifests as
executive dysfunction and a depressive state in response to
decreased frontal CBF [7]. These observations are suggested to be
due to a remote effect that occurs via the thalamo-cortical
network.
For the assessment of executive dysfunction, which is also
specific to mild cognitive impairment (MCI) [8], the Montral Cognitive Assessment (MoCA) was developed to detect participants
with amnestic MCI in a clinic-based study [9]. With respect to
CVD, Godefroy reported [10] that among patients who had suffered
an acute stroke, those with cognitive impairment scored significantly lower on the MoCA than patients without cognitive impairment. A recent report has suggested that the MoCA is more
sensitive than the Mini-Mental State Examination (MMSE) [11] in
patients with subcortical vascular cognitive impairment [12].
In addition to our previous report that showed that very mild
subcortical VaD participants exhibited lower MoCA attention subscores than healthy elderly subjects [13], herein we examined the
effectiveness of MoCA to assess patients with VaD, especially those
with frontal hypoperfusion, in our outpatient clinic. Our hypothesis
was that VaD patients, particularly those exhibiting decreased
frontal CBF, would exhibit impaired MoCA scores.
2. Methods
2.1. Institution
The study was performed at the Osaki-Tajiri SKIP center, Japan,
which is an integrated institute for stroke, dementia, and prevention of bed-confinement in the community. The institute includes
a memory clinic for dementia that provides consultations for
approximately 300 outpatients each month. Two board-certified
neurologists, a psychiatrist, and a geriatrician work at the clinic.
Facilities for MRI (1.5 Tesla, Toshiba, Minato, Tokyo, Japan) and
99m
Tc-ethyl cysteinate dimer (99mTc- ECD) SPECT are available.
Neurobehavioral assessments are performed routinely, together
with MRI and SPECT, for the differential diagnosis of dementing
diseases in outpatients.

participate in the study. The sample size was sufficiently powered

to analyze the group effect at a significance level of p < 0.05. The
error protection was 0.05 and power was 0.8, thus the effected size
was 15 for each group.
As a negative control group, the database of healthy participants (CDR 0) from the Kurihara Project [18] was used. Briefly, a
clinical team consisting of physicians and public health nurses
determined the CDR. Initially, public health nurses visited the participants homes to evaluate their daily activities. Observations by
family members regarding the participants lives were then
described in a semi-structured questionnaire. The participants
were interviewed by public health nurses and physicians to assess
episodic memory, orientation, judgment, and so on. Finally, with
reference to the information provided by the family members,
the participants CDR levels were determined at a joint meeting
of the physicians and public health nurses.
Written informed consent was obtained from each of the participants and from the respective family members. The study was
approved by the Ethical Committees of the Osaki Citizens Hospital
and Tohoku University Graduate School of Medicine.
2.3. Cognitive assessments
We used the MoCA Japanese version (MoCA-J) [19] and MMSE
in the neuropsychological assessment of all participants. In this
study, the MoCA and MMSE were 30 point tests administered over
15 to 20 minutes. In scoring the MoCA, if the educational level was
612 years, we added 1 point to the total score. The MoCA consists
of eight subscales: visuospatial/executive function (alternating
Trail Making, cube copy, and clock-drawing task); naming (three
animal figures); memory (only repeat, no points); attention (forward and backward digit span, target detection using tapping,
and a serial subtraction task); language (sentence repetition and
verbal fluency); abstraction; delayed recall (five nouns, after
approximately 5 minutes); and orientation (time and place) [9].
The cut-off point of the MoCA-J was established at 25/26 in screening MCI in a clinic-based study [19]. Trained cognitive psychologists performed each of the cognitive assessments.
In our previous report [13], attention subscales exhibited lower
scores in very mild subcortical VaD patients compared to healthy
elderly subjects. We herein focused only the attention subscales
and the total scores.

2.2. Patients

2.4. MRI

This study involved prospective data collection from all patients

seen in the clinic. Two hundred consecutive outpatients with vascular risk factors, such as hypertension, with or without dementia
were evaluated for possible entry to this study. The entry criteria
were: (1) patients who met the National Institute of Neurological
Disorders and StrokeAssociation Internationale pour la Recherche
et lEnseignement en Neurosciences (NINDS-AIREN) criteria [14]
for VaD, or met the National Institute of Neurological and Communicative Disorders and StrokeAlzheimers Disease and Related
Disorders Association (NINCDS-ADRDA) criteria [15] for AD (positive controls); and (2) MMSE scores P9, to ensure verbal communication in the neuropsychological tests. For the dementia
diagnosis, we used the Diagnostic and Statistical Manual, Fourth
Revision with the total Clinical Dementia Rating (CDR) [16,17]
scores P0.5. The NINDS-AIREN criteria include the presence of
CVD, dementia, and a relationship between the two, supported
by a temporal relationship between CVD and the onset of dementia
within 3 months. All patients developed dementia within 3 months
of CVD diagnosis.
A total of 44 patients with VaD, 58 patients with AD, and 67
patients with vascular risk factors but no dementia agreed to

We used a 1.5 Tesla MRI (Achiva or Intera; Philips Electronics

Japan, Tokyo, Japan). The combined axial T1-weighted (repetition
time [TR]: 564, echo time [TE]: 11, flip angle [FA]: 80),
T2-weighted (TR: 4450, TE: 80, FA: 180) and fluid attenuated inversion
recovery (FLAIR) (TR: 8000, TE: 82, FA: 150, TI: 2400) images were
used to evaluate CVD. Lesions were considered to be CVD when
they exhibited low intensity on T1-weighted or FLAIR MRI and high
intensity on T2-weighted MRI at the same location. We operationally considered those changes with diameter P4 mm as CVD
(cerebral infarction). The images were evaluated visually by two
teams which consisted of two neurologists and a psychiatrist,
and a senior neurologist checked the results of both teams. If the
two teams agreed on the locations we used the data. If they did
not agree, a senior neurologist reviewed the data and made the
final decision.
2.5. SPECT
An intravenous line was established prior to the SPECT assessment. An intravenous injection of 600 MBq of 99mTc- ECD was
administered with the patient lying in a supine position with the

Please cite this article in press as: Akanuma K et al. Impaired attention function based on the Montral Cognitive Assessment in vascular dementia patients
with frontal hypoperfusion: The Osaki-Tajiri project. J Clin Neurosci (2016), http://dx.doi.org/10.1016/j.jocn.2015.08.047

K. Akanuma et al. / Journal of Clinical Neuroscience xxx (2016) xxxxxx

Frontal predominant
hypometabolism

F-VaD
sample

NF-VaD
sample

P2 pattern
of the
Sliverman
classification

Table 1
Demographics of the study population

N
Age
Men/Women
Education, years
MMSE

Healthy

AD

NF-VaD

F-VaD

67
80.6 (2.9)
26/41
9.3 (2.1)
25.3 (2.8)

58
80.5 (6.6)
19/39
9.0 (2.2)
16.4 (4.4)*

22
78.3 (8.8)
8/14
9.4 (2.2)
19.0 (4.9)*

16
81.1 (6.2)
5/11
8.8 (1.7)
15.5 (4.1)*

Data are presented as mean (SD) unless otherwise indicated.

AD = Alzheimers disease, F-VaD = frontal hypoperfusion vascular dementia,
MMSE = Mini Mental State Examination, NF-VaD = non-frontal hypoperfusion vascular dementia.
*
Significantly lower than the healthy group (analysis of variance, post hoc
comparisons, p < 0.05).

3. Results
Fig. 1. Illustrative example vascular dementia classified based on single photon
emission computed tomography images. F-VaD = frontal hypoperfusion vascular
dementia, NF-VaD = non-frontal hypoperfusion vascular dementia.

eyes closed in a dimly lit, quiet room. Ten minutes after injection of
99m
Tc-ECD, SPECT was performed using triple-head rotating
c-cameras (Multispect, Siemens, Munich, Germany) equipped with
high-resolution fanbeam collimators. For each camera, projection
data were obtained in a 128  128 format for 24 angles at 50 s
per angle. A Shepp and Logan Hanning filter was used for image
reconstruction at 0.7 cycles/cm, with attenuation correction using
Changs method.
The SPECT images were used to classify the VaD patients into
two subgroups: those with frontal hypoperfusion (F-VaD) and
those without frontal hypoperfusion (NF-VaD). The frontal hypoperfusion pattern was defined as the P2 pattern of the Sliverman
classification, with or without focal hypometabolism in other areas
[20], based on the agreement of three board-certified neurologists
who were blinded to the results of the neuropsychological examinations. If the two neurologists agreed the classification, the pattern was used. If they did not agree, a senior neurologist
classified the pattern.
According to Silvermans criteria, PET images are firstly classified into progressive (P) patterns or non-progressive (N) patterns;
the former consists of P1 (parietal/temporal with/without frontal
hypometabolism), P2 (frontal predominant hypometabolism), and
P3 (hypometabolism of both the caudate and lentiform nuclei),
while the latter includes N1 (normal metabolism), N2 (global
hypometabolism), and N3 (focal hypometabolism not meeting
the progressive PET pattern criteria). We applied the classification
rule of PET images for the SPECT images (Fig. 1).

3.1. Analysis 1
Table 1 presents the demographics of the study population. The
four groups (healthy, AD, NF-VaD, F-VaD) exhibited no significant
differences for age, sex or education level. The MMSE scores of
the AD, NF-VaD, F-VaD groups were significantly lower than those
of the healthy group, but there were no significant differences
among the three dementia groups.
3.2. Analysis 2
Table 2 presents the CVD locations for the NF-VaD and F-VaD
groups. Both groups had CVD in the thalami and caudate heads
with no significant differences between groups. There were also
no group differences for the proportion of vascular risk factors
(hypertension, dyslipidemia, diabetes mellitus) or drug treatments
(data not shown).
3.3. Analysis 3
Figure 2 presents the total MoCA scores for the four groups. The
three dementia groups (AD, NF-VaD, and F-VaD) exhibited lower
scores than the healthy group. The scores of the F-VaD group were
lower than the NF-VaD group.
The attention subscores, shown as mean (standard deviation) of
the four groups (healthy, AD, NF-VaD, and F-VaD) were 4.3 (1.4),
2.7 (1.7), 3.2 (1.7), and 1.6 (1.7), respectively. The subscore of the
F-VaD group was significantly lower than that of other groups
(p < 0.05, post hoc test).
4. Discussion

2.6. Analyses
2.6.1. Analysis 1
The one-way analysis of variance was used for the comparison
of the demographics of the four groups (healthy, AD, NF-VaD,
F-VaD), together with the MMSE scores.
2.6.2. Analysis 2
The CVD locations for the NF-VaD and F-VaD groups were
analyzed.
The thalamus and caudate head or white matter changes were
compared using chi-squared tests, since the lesions at the areas
were considered to be statistically important areas.
2.6.3. Analysis 3
Total scores and the attention subscores of MoCA for the four
groups were compared using a one-way analysis of variance with
post hoc test.

We found that the MoCA total scores and attention subscores

were lower in the F-VaD group compared with other groups.
Although there were no NF-VaD versus F-VaD differences for demographics and CVD locations, the functional changes were apparent
by SPECT images and cognitive scores.
4.1. Different diaschisis effect of the same CVD locations
About 40% (16/38) of VaD patients exhibited frontal hypoperfusion. This decreased CBF was associated with functional decline,
that is, executive dysfunction, which is consistent the original definition of diaschisis. We cannot explain why the two CVD-location
matched groups revealed this functional difference. Even the same
strategic CVD may have a different effect on diaschisis. This different neurological background has been reported to differentiate
between NF-VaD and F-VaD; however, similar CVD distributions
were noted in the thalami and caudate heads, together with similar

Please cite this article in press as: Akanuma K et al. Impaired attention function based on the Montral Cognitive Assessment in vascular dementia patients
with frontal hypoperfusion: The Osaki-Tajiri project. J Clin Neurosci (2016), http://dx.doi.org/10.1016/j.jocn.2015.08.047

K. Akanuma et al. / Journal of Clinical Neuroscience xxx (2016) xxxxxx

Table 2
CVD locations for the NF-VaD and F-VaD groups

Patients
Thalamus

N
Bilateral
Right
Left
Bilateral
Right
Left

Caudate head

Moderate + white matter changes

NF-VaD

F-VaD

22
12
3
4
1*
2
1
15

16
10
2
3
0
1
1*
10

CVD = cerebrovascular disease, F-VaD = frontal hypoperfusion vascular dementia,

NF-VaD = non-frontal hypoperfusion vascular dementia.
*
Overlapping lesions.

30
25

Total score

20
15

the NF-VaD and F-VaD groups, respectively. The F-VaD group

exhibited these symptoms more frequently but this did not reach
significance. A further prospectively designed study is needed to
investigate this finding.
4.4. Limitation of the study
We applied the original Silvermans classification of PET images
to SPECT images. The SPECT images were used to classify the VaD
patients into two subgroups, based on the agreement of three neurologists who were blinded to the findings of the neuropsychological examinations. Although the agreement was very good, a more
sophisticated method, such as statistical parametric mapping
based image subtraction, could be recommended. We attempted
to undertake image subtraction between the F-VaD and NF-VaD
groups; however, individual heterogeneity likely prevented us
from demonstrating any voxel-based difference. Furthermore,
additional executive test results, such as the Digit Symbol test,
should be assessed in future studies. However, not all the subjects
underwent such tests. Despite these limitations, we believe that
our current findings provide some information with respect to
the frontal symptoms of VaD.

10

Conflicts of Interest/Disclosures

5
0
Non-Dementia

AD

NF-VaD

F-VaD

Fig. 2. Total Montral Cognitive Assessment scores of the four groups (bars
represent standard deviation). Analysis of variance, post hoc comparisons. p < 0.05.
AD = Alzheimers disease, F-VaD = frontal hypoperfusion vascular dementia, NFVaD = non-frontal hypoperfusion vascular dementia.

degrees of white matter changes. We speculate that the frontosubcortical network is differentially affected among the two
groups; further investigation is needed to further elucidate this
point.
4.2. MoCA attention subscale
Our results suggest that the MoCA attention subscale can detect
the characteristics of VaD participants, particularly those with
frontal hypoperfusion.
Our previous findings demonstrated that the total MoCA scores
and attention subscores were lower in the very mild subcortical
VaD compared with the other MCI types. Taken together, the MoCA
attention subscale is suggested to be useful in assessing the frontosubcortical network or frontal perfusion states of CVD.
Taking frontal lobe function into consideration, the subscores of
visuospatial/executive function were also analyzed. However, no
differences were noted for the four groups (data not shown). The
visuospatial/executive subscale is made up of the Trail Making Test
B, Necker cube copying, and clock drawing test. Since visual function is stressful for older adults, these visually-loaded subscales
are thought to be inadequate for distinguishing the four groups.
4.3. Clinical implications for F-VaD
As described above, apathy or decreased levels of daily activities
are the main symptoms of VaD. Executive dysfunction based on
decreased CBF or metabolism in the frontal lobe is believed to be
associated with such symptoms, which may prevent such patients
from taking medicine appropriately and thus lead to a worsening
of their condition due to poor control of their vascular risk factors
[1]. We retrospectively analyzed the presence of such symptoms;
the number of patients with symptoms was 8/22 and 10/16 in

The authors declare that they have no financial or other

conflicts of interest in relation to this research and its publication.
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with frontal hypoperfusion: The Osaki-Tajiri project. J Clin Neurosci (2016), http://dx.doi.org/10.1016/j.jocn.2015.08.047

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Please cite this article in press as: Akanuma K et al. Impaired attention function based on the Montral Cognitive Assessment in vascular dementia patients
with frontal hypoperfusion: The Osaki-Tajiri project. J Clin Neurosci (2016), http://dx.doi.org/10.1016/j.jocn.2015.08.047