SciTz Neurology and Neurosciences
Open Access
Research:
Deepening in the Cognitive Domains of Attention and Memory During
Severe Stages of COPD
Sanchez-Cayado N1, Sampedro-Piquero P2*,Zancada-Menendez C3, Rubio S2, Lopez L3
1Hospital Universitario Central de Asturias. Rubin, s/n 33011, Spain
2Departamento de Psicología Biológica y de la Salud. Facultad de Psicología. Universidad Autónoma de Madrid. Ciudad Universitaria de Cantoblanco, Spain
3Laboratorio de Neurociencias. Departamento de Psicología. Universidad de Oviedo, plaza Feijoo s/n 33003, Spain. Instituto de
Neurociencias del Principado
de Asturias (INEUROPA)
Submitted: 29 March 2016
Accepted: 12 May 2016
Published: 17 May 2016
Copyright © 2016 Piquero PS et al.
Abstract
Introduction: Several studies have shown an association between chronic obstructive pulmonary disease (COPD) and cognitive
impairment, however, these neuropsychological deficits are still few understood. Our aim was to assess the attentional and
declarative memory cognitive domains administering a wide neuropsychological battery which included tests of different aspects
of these cognitive functions.
Methods: 20 COPD patients and 21 healthy controls were recruited voluntarily and they were assessed in different tests of
declarative memory and attention: Verbal Paired Associates I and II and Letters and Numbers (Wechsler Memory Scale
(WMS-III)); the Rey Auditory Verbal Learning Test (RAVLT); the Rey-Osterrieth Complex Figure; the Camden Memory
Test; the d2 Test; the Attentional Control Test (Luria-DNA Battery) and finally, the Symbol Digit Modalities Test (SDMT).
According to the GOLD staging scale, the COPD patients were in advanced stages of this illness (stages III and IV).
Results: COPD patients had not problems to perform the verbal memory tests, in contrast to the visual memory tests in which
this group showed important deficits possibly related to an altered visual scanning, visual tracking and perceptual speed.
Conclusion: This finding seems to be supported by the poor performance in the attentional tests. In general, COPD patients,
even in a severe illness stage, did not show important deficits in memory tests. Nevertheless, when the tests required visual
processing and speed, the deficits appeared probably due to attentional deficits. These results seem to contradict the idea that
there is a significant relationship between the severity of COPD and the cognitive dysfunction.
Keywords: COPD; Cognitive function; Attention; Memory.
Corresponding author:
Patricia Sampedro-Piquero,
Departamento de Psicología Biológica y de la Salud. Facultad de Psicología. Universidad Autónoma de Madrid. Ciudad Universitaria de Cantoblanco s/n,
28049 Madrid, Spain, Email: [email protected]
Citation: Cayado NS, Piquero PS, Menendez CE, Rubio S, Lopez L. (2016). Deepening in the Cognitive Domains of Attention and Memory During Severe Stages of COPD. SciTz Neurol
Neurosci. 2016. 1(1): 1001
memory as well as the working memory through recalling
Introduction
and recognition tasks. The immediate and delayed visual
Chronic obstructive pulmonary disease (COPD) is defined
memories were also tested. Regarding the attentional
as a disease characterized by the presence of airflow
process, we assessed the selective and sustained attention
obstruction secondary to emphysema or chronic bronchitis
and also the processing speed. Taking into account the
[1]. Its etiology is varied, including noxious particles released
previous literature, we expect to observe a diffuse cognitive
by tobacco smoke and biomass fuels as well as genetic
impairment in COPD patients with no very severe deficits,
factors, deficiency of the enzyme α-1-antitrypsin being
but explained in part by alterations in basic cognitive
present in 1% of COPD patients [1]. The prevalence of
functions, such as attention or processingspeed.
COPD enhances with age [2] and owing to the substantial
increase of the elderly population in all highly developed
Method
nations, the current public health aim focuses on the
Participants
prevention and the early diagnosis of this disease, reducing
Twenty patients (58.6±1.49 years of age) diagnosed with
and avoiding smoking habits and promoting a healthy
COPD, based on the Global Initiative for Chronic Lung
lifestyle to reduce comorbities associated, such as arterial
Disease (GOLD) criteria [16] were recruited from a
hypertension [3,4].
Respiratory rehabilitation program (Central Universitary
obvious
Hospital of Asturias, HUCA). GOLD staging uses four
manifestation of COPD along with shortness of breath,
categories of severity based on the value of FEV1 (the worse
coughing and expectoration [1], it is also associated with
a person´s airflow limitation is the lower their FEV1) (Table
many extrapulmonary features that contribute to the
1). We also registered their forced expiratory volume in one
morbidity, reduced quality of life, and, possibly, mortality
second (FEV1), oxygen saturation and the Medical Research
from this disease [5,6]. For example, anxiety and depression-
Council (MRC) breathlessness score (Table 1). 8 patients
related disorders are very common in COPD patients and
received oxygen consumption (2 of them each 12h, 4
they have an important impact not only on the quality of the
patients each 16h and 2 each 24h). All patients took an
patient´s life, but also, on the progression of the disease [7].
anticholinergic agent (Tiotropium bromide), an agonist of
On the other hand, brain function has shown to be adversely
adrenergic receptors (Salmeterol) and a corticosteroid
impaired by COPD, so Shim et al. (2001) [8] found that the
(Fluticasone) as usual medication. 4 patients were also being
cerebral metabolism is significantly altered in patients with
treated with Theophylline. As exclusion criteria, we applied
cognitive deficits, and neuroimaging techniques have
the presence of neurologic impairments (vascular disease,
revealed a reduced cerebral perfusion in frontal and parietal
dementia…), the existence of other chronic diseases as well
areas [9]affecting the cognitive functions dependent on these
as, psychiatric disorders. Control group (57.05±1.21 years of
regions. These patients usually display deficits in memory,
age) had no history of lung diseases (n=21). Both groups
speed processing and attentional/executive functions [10,
were equivalent to their age, gender and education (Table 2).
Although
airflow
obstruction
is
the
most
11]. However, we consider that one limitation of these
Table 1: COPD group classification according to GOLD staging.
previous studies is that they used very general and simple
tests [12-15].
Our aim was to assess the declarative memory and
Stage I
Mild COPD
FEV1≥ 80%
attentional functions in patients diagnosed with COPD
Stage II
Moderate COPD
(secondary to emphysema and not hypoxemic) using a wide
Stage III
Severe COPD
Stage IV
Verysevere COPD
FEV1 5079%
FEV1 3049%
FEV1 <30%
battery of neuropsychological tests which involved different
aspects of both cognitive processes. With regard to the
memory, we assessed the verbal short and long-term
Number of
participants
0
0
9
11
FEV1= 31.7±2.79 MRC= 3.45+0.26 Oxygen saturation= 91.10+0.86
Citation: Cayado NS, Piquero PS, Menendez CE, Rubio S, Lopez L. (2016). Deepening in the Cognitive Domains of Attention and Memory During Severe Stages of COPD. SciTz Neurol
Neurosci. 2016. 1(1): 1001
pair. These pairs of words have no semantic or phonetic
Procedure
relation between them. Finally, a list of 24 words is read and
the participant must recognize which were in the previous
Table 2: Demographic characteristics of the groups
list.
N
20
COPD
21
Control
GENDER
Men: 75%
Women:
25%
Men:
66.7%
Women:
33.3%
AGE
(Mean+SEM)
58.6+1.49
57.05+1.21
EDUCATION
d2 Attention Test
Primary: 40%
Secondary: 30%
Universitary:
30%
Primary: 38.1%
Secondary:
28.6%
Universitary:
33.3%
This test is made up of 14 lines with 47 characters in each
and the participant, in a limited time, must mark the letters d
and p when they are accompanied by one or two small lines
placed individually or in pairs at the top or bottom of each
letter. This test measures selective and sustained attention
and provides indexes of processing speed as well as
impulsivity in the response. The analyzed variables were: TA
The study was carried out with full respect for the
fundamental
principles
established
in
the
Helsinki
Declaration, the Convention of the Council of Europe on
human rights and biomedicine, the UNESCO Universal
Declaration on the Human Genome and Human Rights as
well as the requirements of Spanish law in the field of
biomedical research protection of personal data and
(total of answers, a measure of processing speed), TE (total
errors, omissions plus commissions). Previous scores
allowed us to calculate the following indexes: TEF (total
effectiveness in the test referred to the test execution quality),
CI (concentration index) and %Error (measures the
proportion of errors made (E) within the area of all items
processed (TA)).
bioethics. All participants were informed about the aims of
the research, questionnaires and the confidentiality of their
personal data by a declared informed consent.
Both groups performed a battery of declarative memory and
attention tests in two sessions of 35 minutes each. All testing
was conducted by experienced professionals and the
Attentional Control Test of Luria-DNA Battery
The participant must pay attention to different verbal orders
or sentences said by the experimenter and answer with
verbal and non-verbal responses. This subtest assesses
sustained attention and the ability of inhibition of distractors.
standardized administration and scoring procedures for each
test were strictly followed.
First session: The session order was the Verbal Paired
Associates I and II Test (Wechsler Memory scale-III,
(WMS-III)) [17], the d2 Attention Test [18], the Attentional
Control Test of Luria-DNA Battery [19], the Symbol Digit
Modalities Test (SDMT) [20] and the delayed retrieval of
Verbal Paired Associates Test. A brief description of each
test is summarized:
Verbal Paired Associates I and II Test (WMS-III)
SDMT
A list of different symbols is paired with numbers and the
participant must write, as fast as possible, the number paired
with the symbol. The number of correct substitutions in one
minute is measured allowing us to know the processing
speed of the participants. In this test, we also registered the
total errors (omissions plus commissions) and the error
percentage (measures the proportion of errors made within
the area of all items processed).
In the Verbal Paired Associates I, the participant is required
to remember 8 pairs of words orally presented. After this,
the first word of each pair is read and the participant must
say the second word of the pair. 4 attempts are made with
each pair of words, but in a different order. In the verbal
paired associates II, and after a delay of 30 minutes, the
participant must remember again the second word of the
Second session: The session order was the Rey Auditory
Verbal Learning Test (RAVLT) [21], the Rey-Osterrieth
Complex Figure (copy) [22], the Pictorial Recognition
Memory Test and Short Recognition Memory Test for
Faces(Camden
Memory
Test)
[23],
the
delayed
reproduction of the Rey-Osterrieth Complex Figure, the
Citation: Cayado NS, Piquero PS, Menendez CE, Rubio S, Lopez L. (2016). Deepening in the Cognitive Domains of Attention and Memory During Severe Stages of COPD. SciTz Neurol
Neurosci. 2016. 1(1): 1001
delayed retrieval of the Rey Auditory Verbal Learning Test
Statistical analyses were carried out using the SPSS
(RAVLT) and the Letters and Numbers Test (Wechsler
19.0 (SPSS Inc., IBM Corporation, Chicago, USA) and the
Memory Scale (WMS-III) [17].
results were expressed as mean +SEM. A Student´s t test
RAVLT
for independent samples was conducted and the results were
A list of words is read and the participant must remember it
considered statistically significant if p<0.05.
regardless of the order. This first list (list A) is read five times
and after each attempt, the participant is required to
remember the list. Then, another list of words (list B) is read
Results
and the participant must remember it immediately. Finally,
First session:
the participant is required to remember and recognize the
Verbal Paired Associates I and II Test (WMS-III)
list A. This test assesses the immediate and delayed verbal
The statistical analysis did not show significant differences
memory, the effect of the interference (proactive and
between groups in the number of recalled words over the 4
retroactive) between similar information, as well as the
trials (T = -0.89, p=0.38). In the delayed retrieval, the
recognition memory.
COPD group remembered fewer words than the control
Rey-Osterrieth Complex Figure
group (T = -2.96, p=0.005), but significant differences were
In the first part of the test, the participant must copy a
not found in the recognition test (T = -1.18, p=0.24).
geometric complex picture without evident meaning to
d2 Attention Test
assess the perceptive ability. After a delay of 15 minutes, the
Results showed significant differences between groups in the
participant must try to reproduce it to assess the delayed
TEF (T = -4.06, p=0.001) and CI (T = -3.64, p=0.001)
visual memory.
indexes, but not in the number of total errors (omissions
Pictorial Recognition Memory Test and Short Recognition
plus commissions) (T = 1.11, p=0.27). In contrast, we found
Memory Test for Faces (Camden Memory Test)
significant differences between groups in the percentage of
In the test of recognition of figures, 30 pictures of persons,
errors (T = 2.08, p=0.04).
places, animals and objects are shown to the participants and
Attentional Control Test of Luria-DNA Battery
then, each picture is shown again paired with two new
Significant differences were found between groups showing
pictures. The participants must decide which of the three
that the COPD group had an altered sustained attention and
pictures they saw in the first presentation. In the recognition
problems to inhibit irrelevant information (T = -2.32,
of faces, 25 photographs of persons are shownto the
p=0.03) respect to the control group.
participants and after this, they are paired with a new
SDMT
photograph. In both cases, the photographs were shown
The Student´s t test for independent samples showed that
during 3 seconds. The participants must decide which
the COPD group processed fewer number of items respect
photograph they saw in the first presentation. These subtests
to the CO group (T = -2.65, p=0.01). Respect to the number
assess the immediate visual memory recognition.
of total errors, we did not find significant differences (T =
Letters and Numbers Test (WMS-III)
significance (T = 2.19, p=0.04), being the COPD group
A series of letters and numbers is read and then, the
which showed higher percentage.
participant must remember the letters in alphabetical order
Second session:
and the numbers in sequential order. The length of the
RAVLT
series is longer in each trial. This test allows us to assess the
In the immediate retrieval and in the total of recalled items
verbal working memory.
over the trials, we did not find significant differences
Statistical analysis
between groups (T = -1.05, p=0.30; T = -1.01, p=0.32,
39
39
39
39
39
39
39
39
39
39
1.39, p=0.17), but the percentage of errors reached statistical
39
39
39
respectively). Respect to the proactive interference effect, we
Citation: Cayado NS, Piquero PS, Menendez CE, Rubio S, Lopez L. (2016). Deepening in the Cognitive Domains of Attention and Memory During Severe Stages of COPD. SciTz Neurol
Neurosci. 2016. 1(1): 1001
did not find significant differences between groups (T =
39
0.02, p=0.99), or in the retroactive interference effect (T = 39
1.93, p=0.06). In the delayed retrieval of list A, both groups
Pictorial Recognition Memory Test and Short Recognition
remembered a similar number of words (T = -1.51,
Memory Test for Faces (Camden Memory Test)
p=0.14),but significant differences were found in the
The Student´s t test for independent samples revealed
recognition test (T = -3.25, p=0.002).
significant differences between groups in the recognition of
39
39
pictures (T = -3.90, p=0.001) and faces (T =-3.83, p=0.001),
39
Rey-Osterrieth Complex Figure
39
showing the COPD group the worst performance.
In the first part of the test, Student´s t test for independent
samples did not show significant differences between groups
Letters and Numbers Test (WMS-III)
(T = -1.97, p=0.06). In the delayed reproduction of the
The Student´s t test for independent samples did not show
picture (15 minutes later) significant differences were also
significant differences between groups (T =-0.70, p=0.49).
not found (T = 1.22, p=0.76).
Table 3 shows the mean values and the comparisons
39
39
39
between groups in the different tests.
Table 3: Performance of each group in the different tests
Discussion
We conducted this study to shed light about the cognitive
CONTROL
GROUP
COPD
GROUP
performance of COPD patients in declarative memory
Total recall on Trials 1–4
17.71±0.9
16.1±1.58
(visual and verbal modalities) and attentional tests. Although
Verbal Paired Associates II (WMS-III)
Delayed recall (30 min.) Recognition
6.48±0.25
23.90±0.07
4.80±0.52*
23.70±0.16
Letters and Numbers (WMS-III)
10.52±0.36
5.95±0.47
48,33±1.73
5.14±0.35
10.90±0.49
10.24±0.50
14.81±0.08
10.05±0.58
5.35±0.47
45.35±2.42
5.15±0.49
9.40±0.61
8.95±0.70
14.15±0.1*
Verbal Paired Associates I (WMS-III)
Rey Auditory Verbal Learning Test
Immediate retrieval (Trial A1)
Total recall on Trials A1-A5
Proactive Interference (List B)
Retroactive interference (List A)
Delayed recall (30 min.)
Recognition (List A)
Rey-Osterrieth Complex Figure Copy
Delayed reproduction (15 min.)
several researches have revealed the existence of cognitive
impairment in these patients [24], however, few is known
about which cognitive functions are really impaired and the
resultsvary depending on the type of test administered and
the COPD severity.The reason of focusing on attention is
the impact of this basic cognitive function on more complex
cognitive domains, as executive functions or declarative
35.41±0.26
20.36±0.76
34.30±0.51
19.95±1.06
Camden Memory Test
Pictorial Recognition Memory Test
28.71±0.71
25.40±0.77
*
Short Recognition Memory Test for
Faces
23.81±0.24
21.40±0.60
*
d2 Test of Attention
TEF (Total effectiveness)
CI (Concentration index)
Total Errors (commissions and
missions)
% Errors (Percentage of Errors)
362.52±13.65
138.33±5.92
20.14±2.8
4.09±0.6
282±14.45*
103.40±7.6
4*
26.65±5.2
7.36±1.45*
Attentional Control Test (Luria-DNA
Battery)
Symbol Digit Modalities Test
Total Number of Items Processed
Total Errors
% Errors (Percentage of Errors)
20.86±0.30
memory, being the last analyzed in our study.
Respect to the declarative memory performance,
some studies found that this cognitive function is altered in
COPD patients [25,26], whereas other found the opposite
finding [27,28]. Our results revealed that COPD patients did
not have problems in the verbal memory tests because, even
showing differences respect to the control group (Table 4,
delayed recall of Verbal Paired Associates II and recognition
in the Rey Auditory Verbal Learning test), their performance
is within the normal range compared to the normative data
test. In the rest of variables, we did not observe significant
42±2.4
0.47±0.1
1.11±0.45
19.25±0.64
*
32.3±3.7*
0.9±0.2
3.37±0.94*
differences
between
groups
(interference
processes,
immediate retrieval or learning curve). These data seem to
indicate that the existence of differences between groups
does not supposethat the COPD group has an altered
cognitive functioning. In fact, De Carolis et al. (2011) [29]
also found significant differences between the COPD and
Citation: Cayado NS, Piquero PS, Menendez CE, Rubio S, Lopez L. (2016). Deepening in the Cognitive Domains of Attention and Memory During Severe Stages of COPD. SciTz Neurol
Neurosci. 2016. 1(1): 1001
control groups in the Mini Mental State Examination
On the other hand, the Attentional Control test
(MMSE) performance, but both were within the normal
allowed us to assess the anterior attentional system involved
range (COPD: 29.1; control: 30) and Prigatano et al. (1983)
in controlling the processing of information when the
[26] also observed that the COPD group had a worse
situation requires planification, conflict resolution or novelty
performance in the Verbal Paired Associates test (immediate
[35]. The worse performance of the COPD group seems to
and delayed retrieval), but its result was normal for its age
suggestthe existence of deficits in the prefrontal cortex-
and education.
dependent functions known as executive functions. De
Consistent with our results, other studies did not
Carolis et al. (2011) [29] also observed deficits in these
found that COPD patients had a worse performance in
superior cognitive functions (cognitive flexibility, divided
verbal memory tests. For example, Antonelli-Incalzi et al.
attention, phonological and semantic verbal fluency test,
(2003) [30] observed a normal performance in the RAVLT
non-verbal logical reasoning and problem-solving ability) and
test and Crews et al. (2003) [31] found similar results even
Antonelli-Incalzi et al. (2003) [30] also found deficits in
when the patients were in an advanced illness stage.
executive tests, such as simple analogies and sentence
Regarding the visual memory, there is also controversy
construction. According to this idea, it had been expected to
between studies [8, 9, 25, 26, 31]. Our results showed that
have found differences between groups in the Letters and
COPD patients had a good performance in the copy and
Numbers test frequently administered to assess the Working
delayed reproduction of the Rey-Osterrieth Complex Figure,
Memory (WM). However, a recent studyhas suggested that
whereas in the recognition of pictures and faces of the
WM tasks of WAIS scale are not sufficientlysensitive to
Camden Memory testshowed deficits respect to the control
analyzethe complex WM [36].
group. It is a surprising result because the recognition tests
Finally, in the SDMT, the COPD group showed a
usually are simpler than the free recall tests [32]. However,
fewer number of processed items and a higher number of
the Camden Memory test requires highly sustained attention
errors respect to the control group. The SDMT has a high
and a very efficient processing speed so, it is possible that the
sensitivity to detect brain damage and patients with this
deficits found in the COPD group could be due to its
pathology usually have a low performance in this test [37,
problems in the attentional cognitive domain. Moreover, the
38]. Moreover, a previous study has also found that COPD
Camden Memory Test is very sensitive to brain damage
patients have problems in the SDMT being their
possibly present in the COPD patients [23].In fact, De
performance positively correlated with the score in the
Carolis et al. (2011) [29] observed that COPD patients had a
Chronic Respiratory Disease Questionnaire (CRQ) [27]. On
poor visual search respect to the control group. In contrast,
the other hand, as we mentioned in d2 the test, the motor
during the copy of the Rey-Osterrieth Complex Figure, the
slowness could explain part of this worse performance result
participant must pay attention to all elements that compound
due to the characteristic of this sort of tests (non-
the figure which could facilitate the acquisition and good
computerized), but the difference between groups in the
performance during the delayed retrieval.
error percentage variable is not related to psychomotor
The main deficits of COPD group were found in
problems.
attention tests suggesting the existence of deficits in divided
Taking all into account, our results showed that
attention, visual scanning, visual tracking and perceptual and
COPD patients, in a severe illness stage,did not have
motor speed. For example, in the d2 test, COPD group
important deficits in declarative memory, above all in verbal
processed fewer number of items, had more errors and its
memory. In the case of the visual memory, the deficits found
CI was lower than the control group. Some studies have
in the Camden Memory test could be explained in part by
suggested that the poor performance of COPD patients in
an alteredvisual scanning, visual tracking and perceptual
this type of test(non-computerized) could be due to
speed. In the study of Villenueve et al. [39] the prevalence of
psychomotor problems [33, 34].
impairment in visuospatial memory and intermediate visual
Citation: Cayado NS, Piquero PS, Menendez CE, Rubio S, Lopez L. (2016). Deepening in the Cognitive Domains of Attention and Memory During Severe Stages of COPD. SciTz Neurol
Neurosci. 2016. 1(1): 1001
memory was 26.9% and 19.2%, respectively.These results
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Nevertheless, in the study of Salik et al. [14], they had found
chronic
obstructiva
crónica:
la
década
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5.
Besides, the level of education seems to be an important
Sleep-related breathing disorders and cardiovascular disease.
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7.
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