Assessment for apraxia in Mild Cognitive Impairment and Alzheimer's disease

Abstract

OBJECTIVE:
To evaluate apraxia in healthy elderly and in patients diagnosed with Alzheimer's disease (AD) and Mild cognitive impairment (MCI).

METHODS:
We evaluated 136 subjects with an average age of 75.74 years (minimum 60 years old, maximum 92 years old) and average schooling of 9 years (minimum of 7 and a maximum of 12 years), using the Mini-Mental State examination (MMSE), Cambridge Cognitive Examination (CAMCOG) and the Clock Drawing Test. For the analysis of the presence of apraxia, eight subitems from the CAMCOG were selected: the drawings of the pentagon, spiral, house, clock; and the tasks of putting a piece of paper in an envelope; the correct one hand waiving "Goodbye" movements; paper cutting using scissors; and brushing teeth.

RESULTS:
Elder controls had an average score of 11.51, compared to MCI (11.13), and AD patients, whose average apraxia test scores were the lowest (10.23). Apraxia scores proved able to differentiate the three groups studied (p=0.001). In addition, a negative correlation was observed between apraxia and MMSE scores.

CONCLUSION:
We conclude that testing for the presence of apraxia is important in the evaluation of patients with cognitive impairments and may help to differentiate elderly controls, MCI and AD.

Full text

Dement Neuropsychol 2015 March;9(1):1-7
1
Original Article
Ward M, et al. Apraxia assessment in MCI and Alzheimer’s disease
Assessment for apraxia in Mild Cognitive
Impairment and Alzheimer’s disease
Mirela Ward1, Juliana F. Cecato1, Ivan Aprahamian1, José Eduardo Martinelli1
ABSTRACT. Objective: To evaluate apraxia in healthy elderly and in patients diagnosed with Alzheimer’s disease (AD) and
Mild cognitive impairment (MCI). Methods: We evaluated 136 subjects with an average age of 75.74 years (minimum 60
years old, maximum 92 years old) and average schooling of 9 years (minimum of 7 and a maximum of 12 years), using the
Mini-Mental State examination (MMSE), Cambridge Cognitive Examination (CAMCOG) and the Clock Drawing Test. For the
analysis of the presence of apraxia, eight subitems from the CAMCOG were selected: the drawings of the pentagon, spiral,
house, clock; and the tasks of putting a piece of paper in an envelope; the correct one hand waiving “Goodbye” movements;
paper cutting using scissors; and brushing teeth. Results: Elder controls had an average score of 11.51, compared to
MCI (11.13), and AD patients, whose average apraxia test scores were the lowest (10.23). Apraxia scores proved able to
differentiate the three groups studied (p=0.001). In addition, a negative correlation was observed between apraxia and
MMSE scores. Conclusion: We conclude that testing for the presence of apraxia is important in the evaluation of patients
with cognitive impairments and may help to differentiate elderly controls, MCI and AD.
Key words: apraxia, neuropsychometric tests, elder, Alzheimer’s disease, mild cognitive impairment, diagnosis.
AVALIAÇÃO DA APRAXIA NO COMPROMETIMENTO COGNITIVO LEVE E DOENÇA DE ALZHEIMER
RESUMO. Objetivo: Avaliar apraxia em idosos saudáveis, com diagnóstico de doença de Alzheimer (DA) e Comprometimento
Cognitivo Leve (CCL). Métodos: Foram avaliados 136 indivíduos com uma idade média de 75,74 anos (mínimo de 60 anos
de idade, máximo 92 anos) e escolaridade média de 9 anos (mínimo de 7 e máximo de 12 anos), por meio do Mini-exame
do Estado Mental (MEEM), Cambridge Cognitive Examination (CAMCOG) e o teste do relógio. Para analisar a presença de
apraxia, foram selecionados oito subitens do CAMCOG: os desenhos do Pentágono, da espiral, da casa, do relógio, e também
a tarefa de colocar um pedaço de papel em um envelope e os movimentos corretos com uma mão para dar “adeus”, cortar
papel com uma tesoura e escovar os dentes. Resultados: Idosos saudáveis sem alterações cognitivas apresentaram média
de 11,51, em comparação com CCL (11,13), e DA o qual apresentou pior média no teste de apraxia (10.23). O subteste de
apraxia diferenciou os três grupos diagnósticos (p=0,001). Observou-se uma correlação negativa entre os escores de apraxia
e os do MEEM. Conclusão: Conclui-se que a investigação da presença de apraxia é importante na avaliação cognitiva de
pacientes com comprometimento cognitivo e pode ser útil em diferenciar controles idosos, indivíduos com CCL e com DA.
Palavras-chave: apraxia, testes neuropsicométricos, idoso, doença de Alzheimer, comprometimento cognitivo leve,
diagnóstico.
INTRODUCTION
According to the National Institute of
Neurological and Communicative Disor-
ders and Stroke and the Alzheimer’s Disease
and Related Disorders Association (NINCDS-
ADRDA), the diagnosis of Alzheimer’s disease
(AD) relies on decits in two or more areas
of cognition with progressive worsening of
memory and other cognitive functions. e
diagnosis of probable AD is supported by
progressive deterioration of other specic
cognitive functions such as language (apha-
sia), motor skills (apraxia) and perception
(agnosia).1 Hence, testing for these cognitive
functions, including apraxia, is a crucial part
of the dementia diagnostic assessment.2
Apraxia has a wide spectrum of disor-
ders with the common inability to perform a
skilled or learned act and several types have
been described, including a limb-kinetic type,
1Geriatrics Section, Department of Internal Medicine, Faculty of Medicine of Jundiaí, Jundiaí, State of São Paulo, Brazil.
Juliana F. Cecato. Instituto de Geriatria e Gerontologia de Jundiaí. Rua Prudente de Moraes 111– 13201-004 Jundiaí SP – Brazil. E-mail: cecatojuliana@hotmail.com.
Disclosure: The authors report no conflicts of interest.
Received July 10, 2013. Accepted in final form December 20, 2014.

Dement Neuropsychol 2015 March;9(1):1-7
2Apraxia assessment in MCI and Alzheimer’s disease Ward M, et al.
which is a form of loss of hand and nger dexterity re-
sulting from inability to connect or isolate individual
movements.3-6 Ideomotor apraxia is characterized by
the inability to correctly imitate hand gestures and
voluntarily use tools. Ideational/conceptual apraxia
is a form in which there is an inability to perform a
series of acts in the due sequence (for instance, to in-
sert a sheet of paper into an envelope) or an inability
to appropriately use a tool (for instance to use a pair of
scissors).7,8 Another type of apraxia is constructional
apraxia, in which there is diculty drawing simple g-
ures or assembling blocks to form a design. e term
visuoconstructive disability is frequently used and en-
compasses constructional apraxia. Recognizing one
type of apraxia does not exclude other concurrent types,
and multiple kinds of apraxia can be diagnosed in the
same patient.4-6
Psychomotor activity impairment and motor func-
tion diculties generated by apraxia are some of the
most distressful features of AD.3,7-9 is neurological
decit causes a loss of ability to perform precise move-
ments and gestures, hence impeding the patient to ac-
complish a learned purposeful complex act correctly.7-9
In general, apraxia advances in step with dementia and
examiners should always remember to assess the pa-
tient’s ability, for example, to write sentences, draw, fold
a sheet of paper, drink water, move the upper and lower
limbs, and other tasks of progressive diculty in order
to characterize dementia stage.7-11
However, there is no accurate instrument for mea-
suring apraxia in aging patients. In fact, most elder in-
dividuals tend to display movement and speech impair-
ments both because of dementia and due to a physiologic
deterioration of muscular and central nervous system
functions.10 In addition, apraxia features are closely
related to the patient’s educational level and activity.11
Also, the diagnosis of apraxia is dicult to character-
ize in patients with mild cognitive impairment (MCI),
dened by the American Academy of Neurology as the
presence of memory complaints and memory impair-
ment in individuals still presenting normal global cog-
nitive functioning and intact activities of daily living.1
On the other hand, apraxia assessment may help de-
ne the severity of the dementia and predict its progres-
sion.12 In addition, the presence of apraxia is important
for planning stimulatory therapies such as physiothera-
py or occupational therapy.
e aim of this study was to verify the presence of
apraxia in MCI and AD patients and its relationship to
performance on other cognitive tests and impact on ac-
tivities of daily living.
METHODS
is cross-sectional study was conducted in the De-
partment of Geriatrics and Gerontology at the Medical
School of Jundiai from January 2011 to January 2014
and included 136 consecutive individuals aged 60 years
or more with at least four years of schooling who sought
medical care and agreed to participate by signing an in-
formed consent form. Patients were classied as prob-
able and possible, or only probable, AD when they met
the NINCDS-ADRDA criteria, and as MCI according to
the criteria of Petersen.21 Patients with severe dementia
(Clinical Dementia Rating=3), history of stroke, Parkin-
son disease features, hand palsies, visual and auditory
impairments or depression were excluded. A control
group (CG) of healthy elderly was formed comprising
individuals whose performance on the neuropsycholog-
ical tests exceeded the respective cut-o points and who
did not present depressive symptoms or impairments in
daily activities.
Both the AD and MCI groups of patients as well as
the controls were submitted to a detailed in-person
clinical anamnesis; neuroimaging; laboratory; and
neuropsychiatric evaluation including the Cambridge
Cognitive Examination (CAMCOG);13 the Mini-Mental
State Examination (MMSE);14,15 the Clock Drawing Test
(CDT) ranked according to both the Mendez16 and Shul-
man17 scales; and the Geriatric Depression Scale.18 e
performance of daily activities was assessed by the Pfef-
fer Functional Activities Questionnaire (PFAQ).13,19
Eight CAMCOG test sub-items were selected for the
evaluation of apraxia. ese items were: the drawings
of the pentagon, spiral, house, clock; and the tasks of:
inserting a sheet of paper into an envelope; the correct
one hand movements designed to wave “goodbye”; cut-
ting a sheet of paper with a pair of scissors; and brushing
teeth. Scores attributed to each one of these sub-items
are described in Table 1. Low total scores, revealing bad
performance, were considered indicative of apraxia.
Statistical analyses. e data obtained were analyzed with
the SPSS (15.0) program. Normality was assessed using
the Kolmogorov-Smirnov test and was observed for all
measures in each one of the groups investigated. Age
among groups was compared using the Kruskal-Wallis
test whereas education level and gender was assessed
using the Chi-square test. Student-Newman-Keuls post-
hoc analysis was performed to dierentiate the diag-
nostic groups. Signicance level was set at 5% (p). Com-
parative analyses of the three patient groups was also
performed using Pearson’s correlation coecient (r) for
age and cognitive tests (MMSE, CAMCOG and CDT).

Dement Neuropsychol 2015 March;9(1):1-7
3Ward M, et al. Apraxia assessment in MCI and Alzheimer’s disease
RESULTS
Mean age of the participants was 75.7±7.38 years, most
elders were female (65.4 %), and the groups did not dif-
fer for age and gender distribution. Individuals in the
control group had a greater number of years of school-
ing (Table 2).
e neurological assessment using the CAMCOG,
MMSE and apraxia results, summarized in Table 3,
demonstrated that patients in the AD group had lower
scores (indicating more severe impairment) compared
to the MCI and to the healthy control groups of elders.
In fact, apraxia scores were able to distinguish the three
diagnostic groups (p<0.0001). Patients in the AD group
had scores below the cut-o point for the CAMCOG (>
80 points). Also, MCI patients’ CAMCOG scores were
higher than expected.
Age (p=0.185; Kruskal-Wallis) and gender (p=0.358;
Chi-square test) did not inuence apraxia assessment
in the three diagnostic groups. Only schooling years
inuenced the assessment signicantly (p=0.040; Chi-
square test). ere was a signicant, albeit moderate
correlation between the apraxia tests and the MMSE
(r=0.40, p<0.0001) and CAMCOG (r=0.45, p<0.0001),
CDT-Mendez (r=0.50, p<0.0001) and CDT-Shulman
(r=0.54, p<0.0001), as shown in Table 4.
e results on the Apraxia assessment, depicted in
Table 4, were associated with CAMCOG results in the
control group. is association remained signicant
Table 1. Sub-items of CAMCOG test employed for apraxia evaluation.
Apraxia Score
Drawing of the pentagon 1 point
Drawing of the spiral 1 point
Drawing the house 1 point
Drawing a clock 3 points
Putting a sheet of paper in an envelope 3 points
“Goodbye” – correct movement 1 point
Scissors – correct movement 1 point
Brushing teeth – correct movement 1 point
Total 12 points
Table 2. Demographic and schooling features of the 52 patients diagnosed with Alzheimer’s disease (AD); the 45 patients considered as
having mild cognitive impairment (MCI) and the 39 healthy control individuals (CG).
MCI AD CG p
Age years (range) 76.60±7.06 (63-92) 77.92±6.97 (64-91) 71.82±6.89 (60-89) 0.185*
Gender (%) Female 27 (60) 33 (63.5%) 29 (74.4%) **0.358
Male 18 (40) 19 (36.5%) 10 (25.6%)
Schooling 5 to 8 years 23 (51.1%) 21 (40.4%) 12 (30.8%) **0.040
> 9 years 22 (48.9%) 31 (59.6%) 27 (69.2%)
*p: Kruskal-Wallis; **p: Chi-square test.
when apraxia was controlled by schooling and age. Con-
cerning the MCI group, depicted in Table 5, apraxia was
associated with the performance on the CAMCOG and
Shulman-CDT tests where both associations remained
signicant even after controlling for the number of
years of schooling. In the AD group, depicted in Table 6,
there was a signicant association between apraxia and
both Mendez-CDT and Shulman-CDT results. ese
data suggest that the worse the clinical dementia, the
more apraxia problems appear, tending to impair even
straight-forward tasks such as drawing.
In the control group, cognitive variability was great-
er than that of apraxia, which is understandable since
Table 3. Description of MMSE, CAMCOG and apraxia assessment of the 52 patients diagnosed with Alzheimer Disease (AD); the 45 patients
considered as having a mild cognitive impairment (MCI) and the 39 healthy control individuals (CG).
Test
CG Mean±SD
(Min-Max)
MCI Mean±SD
(Min-Max)
AD Mean±SD
(Min-Max) p
MMSE 29.10±1.16
(26-30)
26.93±2.07
(21-30)
23.40±3.87
(14-29)
0.0001
CAMCOG 97.74±5.36
(82-107)
88.40±6.63
(73-100)
77.2±11.53
(52-96)
0.0001
Apraxia 11.51±0.72
(10-12)
11.13±1.08
(8-12)
10.23±1.98
(2-12)
0.001
p: Kruskal-Wallis test; Min: minimum; Max: maximum; SD: Standard deviation. MMSE: Mini-mental State Examination.

Dement Neuropsychol 2015 March;9(1):1-7
4Apraxia assessment in MCI and Alzheimer’s disease Ward M, et al.
the cognitive system is preserved. Once cognition starts
to decline, apraxia starts to become a problem; as cogni-
tive variability was reduced because of AD progression,
apraxia variability increased and new test relationships
were found, e.g. for specic praxis tests such as the CDT.
In fact, the CDT proved to be the best test to support
apraxia evaluation, even after adjusting statistical com-
parisons by schooling years.
No eect of apraxia on functional activities, as as-
sessed by the Pfeer scale, was evident.
DISCUSSION
We demonstrated that MCI and AD patients performed
worse than healthy controls on apraxia assessment
tests. is worse performance was independent of fac-
tors such as age and schooling.
It is important to point out that constructional
apraxia was more prevalent among AD patients21 in this
study. Additionally, our data corroborates ndings of
previous studies indicating that other types of apraxia
are also worse in patients with AD, especially the ideo-
motor type.23,25,27
In the case of the present study, taking into account
that both the MMSE and CAMCOG make greater use of
writing and drawing apraxia testing, both types of com-
mon apraxia (constructional and ideomotor) may be in-
volved. e failure to dierentiate between the healthy
elderly and those with AD may have been due to the fact
that apraxia is not usually found in the early stages of
the disease28. Future studies should focus on apraxia
type dierences among the three groups, since general
measures of apraxia showed signicant dierences.25-28
Table 4. Correlations between cognitive tests and apraxia with and without adjustment for schooling years in individuals from the Control group.
Age PFAQ MMSE CAMCOG Mendez Shulman
Apraxia Pearson correlation –0.145 –0.182 0.312 0.627** 0.310 0.216
Sig. (2-tailed) 0.378 0.268 0.053 0.000 0.055 0.187
N39 39 39 39 39 39
Apraxia controlled
by schooling
Correlation –0.172 –0.108 0.234 0.578 0.207 0.097
Significance (2-tailed) 0.301 0.517 0.157 0.000 0.212 0.561
Df 36 36 36 36 36 36
r: Pearson correlation coefficient; p: c2; MMSE: Mini-mental State Examination; PFAQ: Pfeffer Functional Activities Questionnaire; Mendez: CDT Mendez scoring scale; Shulman: CDT Shulman scoring scale.
Table 5. Correlations between cognitive tests and apraxia with and without adjustment for schooling years in individuals from the Mild Cognitive Impairment
(MCI) group.
Age PFAQ MMSE CAMCOG Mendez Shulman
Apraxia Pearson correlation –0.193 –0.001 0.191 0.472** 0.160 0.377*
Sig. (2-tailed) 0.204 0.997 0.208 0.001 0.293 0.011
N45 45 45 45 45 45
Apraxia controlled
by schooling
Correlation –0.321 0.010 0.165 0.466 0.083 0.307
Significance (2-tailed) 0.034 0.947 0.285 0.001 0.594 0.043
Df 42 42 42 42 42 42
r: Pearson correlation coefficient; p: c2; MMSE: Mini-mental State Examination; PFAQ: Pfeffer Functional Activities Questionnaire; Mendez: CDT Mendez scoring scale; Shulman: CDT Shulman scoring scale.
Table 6. Correlations between cognitive tests and apraxia with and without adjustment for schooling year in individuals from the Alzheimer’s disease group.
Age PFAQ MMSE CAMCOG Mendez Shulman
Apraxia Pearson Correlation 0.135 0.073 0.289* 0.214 0.539** 0.537**
Sig. (2-tailed) 0.340 0.605 0.040 0.135 0.000 0.000
N52 52 51 50 51 51
Apraxia controlled
by schooling
Correlation 0.171 0.043 0.288 0.203 0.525 0.519
Significance (2-tailed) 0.239 0.770 0.044 0.162 0.000 0.000
Df 47 47 47 47 47 47
r: Pearson correlation coefficient; p: c2; MMSE: Mini-mental State Examination; PFAQ: Pfeffer Functional Activities Questionnaire; Mendez: CDT Mendez scoring scale; Shulman: CDT Shulman scoring scale.

Dement Neuropsychol 2015 March;9(1):1-7
5Ward M, et al. Apraxia assessment in MCI and Alzheimer’s disease
Apraxia evaluation is useful in the diagnosis of de-
mentia, but is not a decisive factor since normal aging
involves a gradual decline in cognitive function.29,30 As
previously mentioned, this decline in cognitive func-
tions is dependent on educational factors, health, per-
sonality and specic capacity,29-31 explaining the rela-
tively high rate in the control group and the dierence
between patients with AD and MCI. We demonstrated
that apraxia was able to dierentiate mild cognitive im-
pairment from dementia cases. In fact, Sá et al.32 also
found that apraxia tests were able to dierentiate cases
of dementia, both in the early and late stages of the dis-
ease, probably due to the involvement of the posterior
hemisphere in early stages of AD.33
In conclusion, we demonstrated that apraxia was
present in MCI and early phases of AD. Apraxia was best
detected in MCI and AD by means of CDT scores and
new cut-o points for this aspect in these patients sug-
gests the need for further research. It is also important
to assess apraxia to aid planning of rehabilitation.
Apraxia assessment has become an important aspect
of neurodegenerative diseases and a major indicator for
psychotherapy and occupational therapy, contributing
to the quality of life of elderly primarily with cognitive
decline. In many cases, apraxia may be one of the early
symptoms of AD, as shown in this study, where patients
with MCI showed decline on apraxia tests. We conclude
that apraxia should be better assessed on cognitive tests
in older adults with dementia who may also benet
from therapies, thus reducing impact of the disease on
activities of daily living.
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