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Journal of Psychosomatic Research 105 (2018) 99–105

Contents lists available at ScienceDirect

Journal of Psychosomatic Research


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

Cognitive impairment in patients with psoriasis: A matched case-control T


study

Marco Innamoratia, , Rossella M. Quintoa, David Lesterb, Luca Iania, Dario Graceffac,
Claudio Bonifatic
a
Department of Human Sciences, European University of Rome, Rome, Italy
b
Stockton University, Galloway, NJ, USA
c
Center for the Study and Treatment of Psoriasis, San Gallicano Dermatologic Institute, IRCCS, Rome, Italy

A R T I C L E I N F O A B S T R A C T

Keywords: Background: In the past decade, a few studies have suggested that psoriasis could be associated with the presence
Psoriasis of mild cognitive deficits.
Cognitive impairment Objectives: The aim of the present matched case-control study was to investigate several cognitive domains
Anxiety (executive functions, verbal memory, attention, and language) in a sample of outpatients with psoriasis. We also
Depression
investigated whether cognitive impairment was associated with poor health-related quality of life (HRQoL) in
Quality of life
patients with psoriasis.
Methods: Fifty adult outpatients and 50 age- and sex-matched healthy controls were administered a battery of
neuropsychological tests investigating major cognitive domains, psychopathology (anxiety and depression),
alexithymia, and HRQoL.
Results: At the bivariate level, psoriasis patients (compared to healthy controls) performed worse on most of the
neuropsychological tests, and they also reported more anxiety and depressive symptoms, higher scores for
alexithymia, and worse physical and mental health. At the multivariate level, cognitive performance was in-
dependently associated with psoriasis even when controlling for psychopathology and alexithymia.
Conclusions: Patients with psoriasis show impaired cognitive performance, high levels of anxiety and depression,
and impaired quality of life. Based on the current results, clinicians should assess the presence of psychological
symptoms in their patients and evaluate whether the presence of cognitive deficits is limiting the patients' ability
to cope with the disease.

1. Introduction some researchers, building on the so-called “Brain-skin axis” hypothesis


[15], have begun to study neurocognition in patients with psoriasis
Psoriasis is a common chronic inflammatory skin disease with [16–20]. This research has suggested the possible presence of mild
psychiatric and medical comorbidity (e.g., obesity, diabetes mellitus, cognitive impairment in up to 44% of patients with psoriasis [18]. For
and depression) [1,2]. Prevalence estimates for psoriasis range from example, Colgecen and colleagues [16] found deterioration of the
1.4% to 3.3% with wide geographical and ethnic differences [3]. cognitive performance of patients with psoriasis, especially in visual-
Psoriasis causes considerable disability and affects the quality of life of spatial and executive tasks, but no correlations with disease char-
patients [4–8]. acteristics (e.g., duration, severity, and onset age). Gisondi et al. [18]
Psychological factors play an essential role in the etiology and also reported reduction in cortical thickness in parahippocampal, su-
prognosis of psoriasis, and also in the management of the illness [9]. perior temporal and frontal gyri of the left hemisphere.
Psychiatric disorders, notably anxiety and depression, are common However, to date, only a small number of studies, frequently using
comorbidities in psoriasis [10–13]. For example, in the US population, small samples, single screening instruments [16], and noncontrolled
Cohen et al. [14] found that 16.5% of patients with psoriasis met the cross-sectional designs, have supported these results [17]. Thus, the
criteria for major depression. Psychological conditions have been gen- objective of the present matched case-control study was to extend re-
erally considered as responses to the stress of living with a chronic and sults from previous studies by investigating several cognitive domains
disabling condition that also comes with social stigma. Nevertheless, (executive functions, memory, attention, and language) in a sample of


Corresponding author at: Department of Human Sciences, European University of Rome, Via degli Aldobrandeschi, 190, 00163 Rome, Italy.
E-mail address: marco.innamorati@unier.it (M. Innamorati).

https://doi.org/10.1016/j.jpsychores.2017.12.011
Received 31 October 2017; Received in revised form 6 December 2017; Accepted 22 December 2017
0022-3999/ © 2017 Elsevier Inc. All rights reserved.
M. Innamorati et al. Journal of Psychosomatic Research 105 (2018) 99–105

outpatients with psoriasis. We also investigated whether cognitive im- 2.3. Neuropsychological assessment
pairment was associated with decreased health-related quality of life
(HRQoL) in patients with psoriasis. Based on previous research, we 2.3.1. Cognitive functioning
hypothesized that: (1) patients with psoriasis are more likely to have The Mini Mental State Examination (MMSE) is a widely used and
deficits in most of the cognitive domains investigated when compared well-validated screening tool for cognitive impairment [22,23]. The
with sex- and age-matched healthy controls, even after controlling for items of the MMSE include tests of orientation, attention, learning,
the severity of anxiety, depression and alexithymia; (2) cognitive im- calculation, abstraction, information, construction, and delayed recall.
pairment is associated with decreased HRQoL; and (3) cognitive im- Sum scores range between 0 and 30, with lower scores indicating the
pairment severity is not correlated with clinical variables (i.e., severity possible presence of cognitive impairment. The diagnostic accuracy and
of the illness and onset age, even when controlling for socio- clinical utility of the MMSE in screening for dementia have been re-
demographic characteristics). ported [23,24].
The Rey Auditory Verbal-Learning Test (AVLT) [25,26] was used to
evaluate verbal memory. In the present version of the AVLT, a 15 noun-
2. Material and methods word list was read five times to the participants with a presentation rate
of one word per second, and after each trial the participant was im-
2.1. Sample mediately asked to recall as many words as possible (AVLT-I). After a
20 min delay, the participant was again asked to recall the words from
Fifty adult outpatients (22 women and 28 men) consecutively ad- the list (AVLT-D). The numbers of correct words (range of scores 0–75
mitted at the Center for the Study and Treatment of Psoriasis of the San points for the AVLT-I and 0–15 for the AVLT-D) and intrusions were
Gallicano Hospital (Rome, Italy) between November 2016 and May recorded. We used age- and education-corrected scores [27]. The AVLT
2017 participated in a matched-case control study. Inclusion criteria has demonstrated good ability to screen for mild cognitive impairment
were age between 18 and 60 years old and a diagnosis of psoriasis [28], and good predictive validity for Alzheimer's dementia type [29].
vulgaris with a Psoriasis Area Severity Index (PASI) > 3 [21]. Exclu- The Trail Making Test (TMT) [30–32] is widely used as a measure of
sion criteria were the presence of major diseases of the central nervous organized visual search, planning, attention, set shifting, cognitive
system (e.g., dementia and Parkinson disease) and a history of head flexibility, and divided attention. The test consists of two parts. In part
injuries or strokes; the presence of specific medical conditions, such as A (TMT-A), participants are asked to draw a line joining a series of high
hypertension, diabetes mellitus, and dyslipidemia, or other immune- contrast dots which are numbered from 1 to 25. In part B (TMT-B),
mediated diseases sharing the same physiological mechanism as psor- participants are asked to join a series of numbers and letters in an al-
iasis (e.g., Crohn's disease, psoriatic arthritis, and rheumatoid arthritis), ternated sequence. A participant's score was taken as the time to
and current major psychiatric disorders (e.g., schizophrenia and bipolar complete the test. The TMT is a reliable measure when testing executive
disorder) or hallucinatory and delusional phenomena; and the inability functioning [32], with good ability to screen for Alzheimer's dementia
to complete the assessment for whatever reasons, including denial of type [33].
informed consent. The Attentive Matrices Test [34] is a measure of selective and sus-
Each patient was matched for sex and age with a healthy control (22 tained attention, with good ability to screen for Alzheimer's dementia
women and 28 men). The controls were recruited from those attending type [35]. The participant is required to find target numbers (from one
adult education classes and from an advertisement posted for estab- to three) in 3 numeric matrices (10 columns of 13 numbers from 0 to 9).
lished community groups. The same inclusion/exclusion criteria used A participant's score is the number of targets correctly found and the
for the patients were used for the controls. Furthermore, we excluded numbers of false alarms and omissions. We used sex-, age-, and edu-
possible controls with current or past diagnosis of psoriasis and people cation-corrected scores [34].
with a positive history of psoriasis in their family members. The so- The Forward and Backward Digit Span test [36,37] measures the
ciodemographic and clinical characteristics of the sample are reported longest digit span recalled in both forward and backward recall. For-
in Table 1. The protocol received approval from the local Institutional ward recall assesses auditory attention and short-term retention capa-
Review Board. city; backward recall measures the ability to manipulate information in
verbal working memory. The Backward Digit Span has been reported to
have good ability to screen for Alzheimer's dementia type [38]. We used
2.2. Measures age- and education-corrected scores [39].
The Clock Drawing Test (Clock Test) [31,40] is a visuospatial task
All participants were administered a checklist assessing socio-de- capable of assessing several abilities including visuoconstructive abil-
mographic variables (sex, age, marital status, job, school attainment, ities, and executive and praxic functions. We presented a pre-drawn
and hand laterality) and a battery of neuropsychological tests. Tobacco, circle in which the participants were instructed to draw in the numbers
alcohol and drug use were assessed with one item each of the checklist. and then set the time at 2:45 pm. The scoring procedure evaluates
Participants were asked whether they were currently smoking tobacco quantity and positioning of numbers and hands (scores range 0–10)
(and how many cigarettes they were smoking daily), drinking alcohol [31]. The Clock Test can reliably screen for cognitive impairment in
beverages (and how frequently they drink during the week), and using clinical settings [41].
illegal or nonprescribed drugs (including legal highs, and how fre- The Phonemic Fluency Test (Fluency Test) [31] measures verbal
quently they used drugs during the week). Neuropsychological tests ability and executive control [31,42,43]. In the Fluency Test, the par-
were administered in a single session and in a fixed order. For the pa- ticipants are asked to orally produce words beginning with a given
tient sample, clinical information (years with the illness, comorbidities, letter. The numbers of unique correct words, repetitions, and intrusions
family history of psoriasis) were retrieved from clinical records, and the were recorded. The Fluency Test has good ability to screen for Alz-
PASI was completed by the dermatologist in charge 7–14 day before heimer's dementia type [33].
administering the tests. The PASI (score range: 0–72) assesses four body The Stroop Color Word Interference Test (Stroop Test) [44,45] is a
regions (head, trunk and upper and lower extremities) for the body reliable measure assessing selective attention, visual attention, and in-
surface area involvement of erythema, infiltration, and desquamation hibitory control, which has been reported being sensitive to lateral and
[21]. superior medial lesions of the frontal lobes [46]. We administered a
computerized version of the task, using PsychoPy, version 9. Partici-
pants were placed in front of a laptop (Lenovo® Core i5; screen 15.6″) at

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M. Innamorati et al. Journal of Psychosomatic Research 105 (2018) 99–105

Table 1
Socio-demographic and clinical characteristics of the sample.

Variables Patients n = 50 Controls n = 50 Test Significance Cohen's d

Sex Matched –
Men 28 (56.0%) 28 (56.0%)
Women 22 (44.0%) 22 (44.0%)
Age 42.02 ± 12.16 42.02 ± 12.16 Matched –
Right-handed 49 (98.0%) 50 (100.0%) 1.00 0.96a
Marital status Std. MH = 1.77 0.08
Not-married 19 (38.0%) 17 (34.0%) 1.08a
Married 26 (52.0%) 32 (64.0%) 0.79a
Divorced/widowed 5 (10.0%) 1 (2.0%) 1.17a
School attainment (number of years) Std. MH = 0.34 0.73
≤8 11 (22.0%) 10 (20.0%) 1.04a
≤ 13 22 (44.0%) 27 (54.0%) 0.82a
≥ 17 17 (34.0%) 13 (26.0%) 1.17a
Job status 0.23 0.82a
Employed 42 (84.0%) 37 (74.0%)
Unemployed 8 (16.0%) 13 (26.0%)
BMI 26.85 ± 5.11 24.93 ± 3.23 t49 = 2.49 0.02 0.37
Obesity Std. MH = 2.14 0.03
Normal weight 19 (38.0%) 24 (48.0%) 0.82a
Overweight 17 (34.0%) 23 (46.0%) 0.79a
Obese 14 (28.0%) 3 (6.0%) 1.56a
Comorbidity with other dermatological diseases 7 (14.0%) 9 (18.0%) 0.79 0.92a
Tobacco use 23 (46.0%) 14 (28.0%) 0.11 1.44a
Nuumber of daily cigarettes 4.18 ± 5.63 2.96 ± 5.63 – – –
Alcohol use 11 (22.0%) 4 (8.0%) 0.12 1.33a
Number of days in a week drinking ≥ 1 alcohol drinks 1.20 ± 2.94 0.36 ± 1.44 – – –
Drug use 0 (0.0%) 0 (0.0%) – –
Sport activities 11 (22.0%) 16 (32.0%) 0.38 0.82a
Diagnosis of psoriasis 50 (100.00%) 0 (0.0%) –
Duration of illness 16.36 ± 14.17 – –
Family history of psoriasis 28 (56.0%) – –
PASI 4.56 ± 2.25 – –

PASI = Psoriasis Area Severity Index.


Cohen's d = small effects are for a d about 0.20, medium effects are for a d about 0.50, and large effects are for a d about 0.80.
a
Conditional odds ratio.

a standard distance of about 50 cm. This version of the test included oriented thinking. Scores > 61 are indicative of severe alexithymia,
four subtests: (1) participants were presented with a list of squares and and scores between 51 and 60 indicate borderline levels of alexithymia
asked to name the color of the ink with which each square was colored [52]. Cronbach's alpha in the present sample was 0.82.
(10 presentations for each of the five colors: orange, yellow, red, blue,
green); (2) participants were asked to read a list of words that name 2.3.4. Anxiety and depressive symptoms
colors (orange, yellow, red, blue, green) presented on the screen in a The Hospital Anxiety and Depression Scales (HADS) is a reliable and
congruent ink color (word ink and word meaning coincided; 10 pre- valid measurement instrument composed of 14 items assessing anxiety
sentations for each of the five words); (3) participants were presented and depressive symptoms in clinical and nonclinical populations
with a list of words that name colors displayed on the screen in an [54–56]. The anxiety and depression subscales are comprised of seven
incongruent ink color (ink and word meaning did not coincide), and elements each, which are rated on a four-point scale (from 0 to 3). Total
were asked to name the color of the ink and ignore the word's semantic scores range from 0 to 21 for each subscale. A cutoff score above 8 is
meaning (10 presentations for each of the five colors); (4) participants used to indicate the possible presence of anxiety or depression [56].
were presented with a list of words that name colors, and asked to read Cronbach's alphas in the present sample were 0.80 and 0.65, respec-
the word, where the word's meaning and ink color were incongruent tively for depression and anxiety dimensions.
(10 presentations for each of the five colors). We calculated the mean
accuracy and response time (RT) for each subtest and presented as 2.4. Statistical analysis
difference in performance between incongruent and congruent trials
(subtest 4 – subtest 2; subtest 3 – subtest 1) [47,48]. All statistical analyses were performed using the statistical package
for the social sciences, SPSS 19.0 (IBM Corp., Armonk, NY, USA). Paired
2.3.2. Health-related quality of life t-tests, McNemar's tests, and Wilcoxon signed rank tests were used to
The 12-item Short Form Survey (SF-12) [49] is a reliable and valid test group differences. P-values were corrected for multi-testing [57].
measure assessing two dimensions of health-related quality of life, Cohen's d corrected for correlated designs and conditional odds ratio
mental and physical health [50]. Higher SF-12 scores indicate better risk were reported as measures of effect size. Conditional odds ratio risk
HRQoL. In the present sample Cronbach's alpha was 0.75. (COR; [case exposed + control unexposed] / [case unexposed + con-
trol exposed]) was reported as measure of relative risk among psoriasis
2.3.3. Alexithymia patients versus controls in NxN contingency tables.
The Toronto Alexithymia Scale (TAS-20) is a reliable and valid Considering the high number of significant variables at the bivariate
measure composed of 20 items rated on a five-point Likert-type scale analyses and a possible problem of multicollinearity among the pre-
(from 1, “strongly disagree” to 5, “strongly agree”) [51–53]. The TAS dictors, principal component analyses (PCA) were used to reduce the
measures three dimensions of alexithymia: (1) difficulty identifying number of independent variables included in the regression analyses.
feelings; (2) difficulty communicating feelings; (3) and externally- Some authors [58] suggested that the proportion of explained variance

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M. Innamorati et al. Journal of Psychosomatic Research 105 (2018) 99–105

should be at least 50%. the first PCA, we included variables measuring psychopathology and
Independent associations between psoriasis and neuropsychological alexithymia. The analysis resulted in a single component (eigen-
variables (controlling for psychopathology) were calculated by condi- value = 1.99; variance explained = 66.2%). All the variables had
tional logistic regression analysis with group (patients versus controls) factor loadings ≥0.40 (TAS-20 = 0.79, HADS-A = 0.80, HADS-
as the dependent variable. Alternative models with the inclusion of D = 0.85). Higher scores on this factor were associated with worse
cigarette smoking, alcohol use, and BMI were tested. Associations were psychopathology and greater alexithymia. The second PCA with vari-
reported as beta coefficients, odds ratios (OR) and their 95% confidence ables related to cognitive performance resulted in two components
interval (95% CI). A significant chi-squared statistic (χ2) indicates good (eigenvalues 2.70 and 1.54, variance explained 33.8% and 19.2%) that
fit of the model to the data. In the psoriasis group, partial correlations were extracted and orthogonally rotated (VARIMAX). The first com-
(rp; controlling for age) were calculated as measures of association ponent (i.e., general cognitive performance) contained most of the
between continuous variables. We performed correlational analyses variables with factor loadings ≥ 0.40 (phonemic fluency = 0.50, digit
both on scores derived from PCA and from single neuropsychological span backward and clock test = 0.53, MMSE = 0.66, TMT-B/TMT-A
tests, because although from the former we may derive a composite difference = − 0.70, attentive test = 0.71). The second component
score synthetizing the individual's cognitive performance, the in- (i.e., verbal memory) contained AVLT-I and AVLT-A, with factor load-
formation lost with these synthetic scores is high. (Not all neu- ings, respectively, of 0.92 and 0.93. For both components, a higher
ropsychological tests are included in the PCA, and for the tests included score indicates higher cognitive functioning.
not all the variance is reproduced in the factorial solution.) Because of Conditional logistic regression model had good fit to the data
the high number of tests, corrections were made for multi-testing [57]. (Table 3). General cognitive performance and verbal memory were
All statistics were considered significant if p < 0.05. independently associated with psoriasis. Patients with psoriasis were
6.7 times more likely to have lower general cognitive performance and
11.1 times more likely to have lower verbal memory than sex- and age-
3. Results
matched controls. However, the psychopathology and alexithymia
component was not associated with psoriasis. The inclusion of BMI or
3.1. Differences between groups
alcohol use in the model did not change the results (BMI: χ21
change = 0.66; p = 0.42; alcohol use: χ21 change = 0.37; p = 0.55),
The two groups did not differ in sociodemographic and clinical
and beta coefficients for both general cognitive performance and verbal
variables (Table 1). Patients with psoriasis obtained lower scores on the
memory remained significant (p < 0.05) and partially stable (beta
MMSE and performed more poorly on most of the neuropsychological
coefficients for general cognitive performance ranging between − 1.80
tests administered, except for the AVLT, TMT-A, Digit Span Forward,
and − 1.91, and beta coefficients for verbal memory ranging between
repetitions and intrusions on the Fluency Test, or the Stroop Test
− 2.54 and − 2.79). However, the inclusion of tobacco use in the model
(Table 2). Patients with psoriasis also reported more anxiety and de-
(χ21 change = 4.02; p < 0.05) changed the beta coefficients slightly
pression and alexithymia, and worse HRQoL.
(general cognitive performance: − 1.84 [se = 1.03; OR = 0.16; 95%
Due to potential problems of multicollinearity among the predictors,
CI = 0.021.20]; verbal memory: − 3.39 [se = 1.58; OR = 0.03; 95%
we reduced the number of independent variables through two PCAs. In

Table 2
Differences between groups on neuropsychological tests.

Variables Patients n = 50 Controls n = 50 Test Significance Cohen's d

MMSE 26.10 ± 2.68 28.54 ± 1.57 t49 = − 5.36 < 0.001⁎⁎ − 0.78
AVLT-I 15.53 ± 7.67 22.86 ± 5.78 t49 = − 5.44 < 0.001⁎⁎ − 0.77
AVLT-I - false recognition 2.24 ± 3.35 1.62 ± 2.15 t49 = 1.13 0.26 0.16
AVLT-D 2.26 ± 1.67 3.96 ± 1.54 t49 = − 6.51 < 0.001⁎⁎ − 0.92
AVLT-D - false recognition 0.76 ± 1.19 0.62 ± 1.09 t49 = 0.59 0.56 0.08
TMTA (seconds) 37.36 ± 14.46 36.60 ± 8.64 t49 = 0.34 0.74 0.05
TMTB (seconds) 60.82 ± 24.19 53.63 ± 14.79 t48 = 2.22 0.03⁎ 0.34
TMTB – TMTA difference (seconds) 23.51 ± 17.26 17.10 ± 11.72 t48 = 2.38 0.02⁎ 0.35
Attentive matrices 49.50 ± 8.00 52.50 ± 5.16 t49 = − 3.14 0.003⁎⁎ − 0.48
Digit span forward 5.47 ± 1.05 5.82 ± 0.71 t49 = − 2.04 0.05 − 0.30
Digit span backward 3.86 ± 0.71 4.33 ± 0.87 t49 = − 2.91 0.01⁎ − 0.41
Clock test 7.93 ± 3.13 9.22 ± 1.27 t49 = − 2.86 0.01⁎ − 0.45
Phonemic fluency test 12.06 ± 3.27 15.08 ± 2.88 t49 = − 5.01 < 0.001⁎⁎ − 0.71
Phonemic fluency – repetitions 1.10 ± 1.25 0.80 ± 1.12 t49 = 1.24 0.22 0.18
Phonemic fluency – intrusions 0.36 ± 1.04 0.44 ± 0.97 t49 = − 0.39 0.70 − 0.05
Stroop test, ink color naming - RT (seconds) 0.14 ± 0.25 0.22 ± 0.21 t48 = − 1.76 0.08 − 0.26
Stroop test, ink color naming - number of errors 2.18 ± 6.73 0.82 ± 1.15 t49 = 1.45 0.16 0.27
Stroop test, word naming - RT (seconds) 0.06 ± 0.16 0.03 ± 0.13 t48 = 1.33 0.19 0.15
Stroop test, word naming - number of errors 0.29 ± 1.00 0.06 ± 0.32 t48 = 1.47 0.15 0.24
SF-12 physical health 51.18 ± 5.87 55.66 ± 3.28 t49 = − 4.79 < 0.001⁎⁎ − 0.72
SF-12 mental health 41.22 ± 6.41 44.85 ± 7.35 t49 = − 2.55 0.01⁎ − 0.36
TAS-20 43.94 ± 11.18 36.18 ± 10.10 t49 = 3.96 < 0.001⁎⁎ 0.56
TAS-20 ≥ 61 4 (8.0%) 1 (2.0%) 0.25 1.13a
HADS-A 5.38 ± 2.73 3.92 ± 3.29 t49 = 2.43 0.02⁎ 0.35
HADS-A ≥ 8 11 (22.0%) 6 (12.0%) 0.30 1.22a
HADS-D 5.20 ± 2.86 2.76 ± 2.66 t49 = 4.46 < 0.001⁎⁎ 0.63
HADS-D ≥ 8 9 (18.0%) 2 (4.0%) 0.04⁎ 1.33a

MMSE = Mini Mental State Evaluation; TMTA = Trail Making Test A; TMTB = Trail Making Test B; TAS-20 = Toronto Alexithymia Scale-20; HADS-A = Hospital Anxiety Depression
Scale - Anxiety; HADS-D = Hospital Anxiety Depression Scale - Depression.

Significant for p < 0.05 after correction for multi-testing.
⁎⁎
Significant for p < 0.01 after correction for multi-testing.
a
Conditional odds ratio.

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M. Innamorati et al. Journal of Psychosomatic Research 105 (2018) 99–105

Table 3
Conditional logistic regression analysis.

Beta coefficients SE (Beta) Odds ratio 95% confidence intervals lower 95% confidence intervals upper Significance
(OR) level level

Component 1 – general cognitive performance −1.90 0.91 0.15 0.03 0.88 0.03
Component 2 – verbal memory −2.45 1.04 0.09 0.01 0.66 0.01
Component 3 – psychopathology and 0.78 0.51 2.17 0.80 5.94 0.13
alexithymia

Fit indices: −2LL = 18.82; χ23 global = 30.97; p < 0.001; χ23 Previous step change = 49.11; p < 0.001.
Component 1 (a higher score indicates higher cognitive functioning) = MMSE, digit span backward, phonemic fluency, attentive matrices, TMTB – TMTA difference, and clock test have
factor loadings ≥ 0.4 on this component.
Component 2 (a higher score indicates higher cognitive functioning) = ALVT-I and AVLT-D have factor loadings ≥ 0.4 on this component.
Component 3 (a higher score indicates higher psychopathology) = HADS-A, HADS-D, and TAS-20 have factor loadings ≥ 0.4 on this component.

CI = 0.0020.75]), suggesting that only verbal memory was in- involving a more diffuse neural network [59]. Although we did not
dependently associated with psoriasis. investigate brain functioning directly, previous lesion and functional
neuroimaging studies suggests a sensitivity of specific tests to the
3.2. Associations between cognitive performance and HRQoL in patients functioning of different cerebral areas [46,60].
with psoriasis The largest differences between groups were on the AVLT (d of
− 0.92 and − 0.77, respectively, for the AVLT-D and the AVLT-I).
Cognitive functioning components were not significantly associated Recently, Moradi et al. [60] investigated which brain regions activa-
with physical and mental health (general cognitive performance: tions are important for the estimation of performance on the AVLT, and
rp = 0.19 and 0.06, respectively, for physical and mental health; verbal reported that the top predictors were medial temporal lobe structures
memory: rp = 0.15 and 0.18, respectively, for physical and mental and amygdala for the estimation of AVLT-I and angular gyrus, hippo-
health), consistent with results from individual neuropsychological campus, and amygdala for the estimation of the AVLT Percent Forget-
tests (only four significant tests before correction for multi-testing and ting (an index calculated by subtracting the score of AVLT-D to the
no one after this correction. Physical health was associated with the score of the last trial used to calculate the AVLT-I). Otherwise, pho-
number of errors at the Stroop word naming [rp = − 0.21] and color nemic fluency (d = − 0.71) seems to activate both frontal areas and
naming [rp = − 0.22], and scores at the Clock Test [rp = 0.25]. Mental some non-frontal brain areas (e.g., the thalamus, parietal and temporal
health was associated only with the AVLT-D [rp = 0.22]). lobes) [46]. Finally, Stonnington et al. [61], investigated the ability of
Cognitive functioning components were also not significantly asso- T1 weighted magnetic resonance images to predict individuals' per-
ciated with years with the illness (general cognitive performance formances on neuropsychological tests, and reported that MMSE scores
rp = 0.21; p = 0.14; verbal memory rp = − 0.17; p = 0.25) and PASI (d = −0.78 in our study) correlate significantly with whole brain grey
scores (general cognitive performance rp = −0.20; p = 0.17; verbal matter changes associated with Alzheimer's disease.
memory rp = 0.03; p = 0.83), consistent with individual neu- HRQoL was not significantly associated with cognitive performance
ropsychological tests (only four significant tests before correction for (hypothesis 2). Thus, our results did not support the hypothesis that a
multi-testing and no one after this correction. PASI scores were asso- poor cognitive performance could negatively affect the quality of life of
ciated with the Attentive Matrices [rp = −0.32], and years with the patients, possibly through a reduced capacity for regulating the inner
illness was associated with the TMT-B [rp = −0.29], the AVLT-I states of people with cognitive impairment when facing potential
[rp = − 0.29], and MMSE scores [rp = −0.38]). stressors. Unfortunately, to the best of our knowledge, no previous
studies have examined this association in psoriasis. However, Stites
et al. [62] investigated how awareness of their diagnostic label could
4. Discussion
impact self-reported quality of life in older adults with varying degrees
of cognitive impairment, and found that those patients with mild cog-
Patients with psoriasis performed worse on most neuropsycholo-
nitive impairment who were aware of their diagnosis (compared to
gical tests than sex- and age-matched healthy controls (hypothesis 1),
those who were unaware) had lower satisfaction with daily life and
although, in the multivariate analysis, only episodic memory as as-
worse physical well-being.
sessed with the AVLT was independently associated with psoriasis when
Correlations among illness characteristics (i.e., the severity and
controlling the effect of psychopathology and tobacco use. Our results
chronicity of psoriasis) and performance on the neuropsychological
are consistent with the conclusions reached from the few studies that
tests were weak and non-significant (hypothesis 3). These results are
have been published [16–20], despite some inconsistencies [16–18].
consistent with the results of Marek-Jozefowicz et al.'s [17] and Col-
Marek-Jozefowicz et al. [17] reported impaired performance on the
gecen et al.'s [16] studies. Colgecen et al. [16] reported no correlations
TMT and Stroop Test which supported their conclusion of a possible
between disease characteristics and performance on neuropsycholo-
dysfunction of the prefrontal cortex in these patients while, in our
gical tests, while Marek-Jozefowicz et al. [17] found no associations
sample, the effects for these tests were nonsignificant and small. Some
between performance on neuropsychological tests and PASI scores, and
differences in the research designs might explain these inconsistencies
significant but weak associations with the duration of illness.
(e.g., cross-sectional vs. age- and sex-matched case control study design,
different versions of the Stroop Test, and differences in the mean se-
verity of the illness in the patients). However, it is evident that the 4.1. Limitations
performance on the TMT of patients from the two studies was com-
parable (TMT-A = 37.4 [SD = 14.5] seconds in our sample and 36.0 Our results should be viewed in the light of several limitations. First,
[SD not reported] in Marek-Jozefowicz et al.'s study; TMT-B = 60.8 our sample included only 50 patients with a limited range of PASI
[SD = 24.2] in our sample and 65.0 [SD not reported] in Marek-Jo- scores and future studies with larger samples and more severe forms of
zefowicz et al.'s study) while the performance of controls was not. Fi- psoriasis should be carried out. Second, we were unable to compare
nally, our results do not fully support the hypothesis of a specific dys- results from neuropsychological testing with neuroimaging investiga-
function of the prefrontal cortex, but rather a possible dysfunction tions, which could have enabled us to shed light on the underlying

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M. Innamorati et al. Journal of Psychosomatic Research 105 (2018) 99–105

brain anomalies sustaining cognitive deficits shown by patients with invisible, Exp. Dermatol. 26 (2017) 845–853.
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psoriasis: a cross-sectional study using the Montreal cognitive assessment, Am. J.
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results. Fourth, despite the fact that the groups did not differ in edu- [17] L. Marek-Jozefowicz, M. Jaracz, W. Placek, R. Czajkowski, A. Borkowska, Cognitive
cation, some of the controls possibly were attending adult education impairment in patients with severe psoriasis, Postepy Dermatol. Alergol. 34 (2017)
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classes and, therefore, they may have been better prepared for the test- [18] P. Gisondi, F. Sala, F. Alessandrini, V. Avesani, G. Zoccatelli, A. Beltramello, et al.,
taking. Fifth, the cross-sectional design of our study prevents us from Mild cognitive impairment in patients with moderate to severe chronic plaque
drawing causal inferences. Nevertheless, our study has some strengths, psoriasis, Dermatology 228 (2014) 78–85.
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