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Citation: Plichta, P.; Tyburski, E.;
Bielecki, M.; Mak, M.;
Kucharska-Mazur, J.; Podwalski, P.;
Rek-Owodzi´n, K.; Waszczuk, K.;
Sagan, L.; Michalczyk, A.; et al.
Cognitive Dysfunctions Measured
with the MCCB in Deficit and
Non-Deficit Schizophrenia. J. Clin.
Med. 2023,12, 2257. https://
doi.org/10.3390/jcm12062257
Academic Editor: Carmine Tomasetti
Received: 31 December 2022
Revised: 12 March 2023
Accepted: 13 March 2023
Published: 14 March 2023
Copyright: © 2023 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
Journal of
Clinical Medicine
Article
Cognitive Dysfunctions Measured with the MCCB in Deficit
and Non-Deficit Schizophrenia
Piotr Plichta 1, Ernest Tyburski 1, * , Maksymilian Bielecki 1, Monika Mak 1, Jolanta Kucharska-Mazur 2,
Piotr Podwalski 2, Katarzyna Rek-Owodzi ´n 1, Katarzyna Waszczuk 2, Leszek Sagan 3, Anna Michalczyk 2,
Bła˙
zej Misiak 4and Jerzy Samochowiec 2
1Department of Health Psychology, Pomeranian Medical University in Szczecin, 71-457 Szczecin, Poland
2Department of Psychiatry, Pomeranian Medical University in Szczecin, 71-457 Szczecin, Poland
3Department of Neurosurgery, Pomeranian Medical University in Szczecin, 71-252 Szczecin, Poland
4Department of Psychiatry, Wroclaw Medical University, 50-367 Wroclaw, Poland
*Correspondence: ernest.tyburski@pum.edu.pl; Tel.: +48-91-351-13-00
Abstract:
This study compared cognitive domains between deficit schizophrenia (DS) and non-
deficit schizophrenia (NDS) patients and healthy controls (HC), analyzing relationships between
psychopathological dimensions and cognitive domains. A total of 29 DS patients, 45 NDS patients,
and 39 HC subjects participated. Cognitive domains were measured using the Measurement and
Treatment Research to Improve Cognition in Schizophrenia Battery. Psychopathological symptoms
were evaluated with the Positive and Negative Syndrome Scale. Clinical groups performed poorer
than HC groups in regards to speed of processing, attention/vigilance, working memory, verbal and
visual learning and memory, reasoning and problem solving, and social cognition. DS patients scored
poorer than NDS patients in terms of all cognitive domains and the overall score, except for reasoning
and problem solving. Positive, negative, disorganization, and resistance symptoms were related to
cognitive functions only in NDS patients. Our findings suggest that the MCCB battery is sensitive to
detecting cognitive dysfunctions in both deficit and non-deficit schizophrenia.
Keywords:
schizophrenia; cognitive functions; psychopathology; deficit schizophrenia; non-deficit
schizophrenia; MCCB; PANSS
1. Introduction
Cognitive impairment is observed across all stages of schizophrenia, from the premor-
bid period, through the high-risk state, to first episode psychosis, and ultimately, to the
chronic course of the disease. The emerging deficits manifest to varying extents, depending
on the phase of the illness. They primarily involve attention, working memory, executive
functions, verbal and visual memory, social cognition, language, processing speed, and
verbal fluency [
1
–
3
]. However, schizophrenia is characterized by extreme heterogeneity
and marked clinical variance in psychopathological presentation, underlying biological
correlates, functional outcomes, and response to treatment, which hinder the possibility of
fully understanding the nature of specific or general cognitive dysfunctions. As a result,
researchers have systematically parsed the symptomatology of schizophrenia into more
homogeneous diagnostic categories, such as paranoid and non-paranoid, positive and
negative, or deficit and non-deficit subtypes [4].
First identified by Carpenter et al., deficit schizophrenia (DS) with predominant
negative symptoms is characterized by the presence of greater dysfunction and a long
duration of symptomatology [
5
]. The primary features of this subtype are, among others,
social withdrawal, poverty of speech, limited content of verbal expression, apathy, and
blunted affect. Alongside the manifested negative deficits, the basic symptoms include:
J. Clin. Med. 2023,12, 2257. https://doi.org/10.3390/jcm12062257 https://www.mdpi.com/journal/jcm
J. Clin. Med. 2023,12, 2257 2 of 16
distortion of reality, disorganization, and cognitive impairment. Compared to the non-
deficit subtype, deficit schizophrenia is associated with greater functional and structural
disorders of the brain, which can be related to more severe cognitive dysfunctions [6,7].
Most studies to date demonstrate that patients with deficit schizophrenia manifest
greater impairment in the performance of neuropsychological tasks. However, their results
do not clearly indicate whether the observed dysfunction reflects a general or specific
cognitive deficit [
8
]. Some light on this unclear matter is shed by the results of two meta-
analyses [
3
,
9
], suggesting more general cognitive impairments in deficit compared to
non-deficit schizophrenia. Notwithstanding, the authors propose that some patients with
deficit schizophrenia may in fact manifest a differential pattern of neuropsychological
impairment, which could be considerably more complicated than previously thought and
which warrants a more sophisticated and rigorous examination of the cognitive dysfunc-
tions underlying the deficit syndrome with the use of more extensive batteries of tests.
Although there is evidence of greater executive dysfunctions and reduced information
processing speed in deficit schizophrenia [
10
–
16
], research findings concerning other cogni-
tive domains are still markedly inconsistent. Some reports suggest more severe impairment
within simple attention and working memory [
11
,
17
] or verbal and visual memory in this
patient population [
18
,
19
]. Others show no differences between various patient groups in
regards to mental flexibility, attention, and verbal memory [
20
], verbal working memory
and verbal learning [21], or attention and working memory [22].
Of note, there seem to be certain gaps in previous studies that need to be addressed.
For example, visual memory but not visual learning (except [
18
]) tends to be examined
using a single trial only [
19
,
23
,
24
] in several trials, such as in the Brief Visuospatial Memory
Test-Revised [
25
]. Likewise, there is a tendency to measure working memory using the
Digit Span test [
8
,
17
,
19
,
21
,
22
,
24
,
26
], which is an easier task compared to the Letter-Number
Sequencing test, which involves greater reliance on the central executive system [
27
]. In
addition, only a few studies explored visuospatial working memory in deficit schizophre-
nia with the use of the Spatial Span or other related tasks [
3
]. What is more, to the
best of our knowledge, previous studies did not use the Neuropsychological Assessment
Battery—Mazes to measure reasoning and planning in deficit schizophrenia (except for
Fervaha et al. [27]
, but they used the more simple Mazes from Revised Wechsler Intelli-
gence Scale for Children). There are also some uncertainties regarding differences in social
cognition between various patient groups. Most previous studies used a simple task to
measure facial emotion recognition [
12
,
20
,
21
,
23
,
27
–
30
], providing limited information on
how deficit schizophrenia affects performance in the Mayer–Salovey–Caruso Emotional
Intelligence Test, which is a more complex task measuring the theory of the mind [
31
].
Thus, the answer to this emerging need to assess cognitive impairment underlying deficit
schizophrenia in a more comprehensive manner might lie in the use of a structured test
battery that could offer an extensive approach to the cognitive domains that are relevant to
this subtype.
Another important issue is the relationship between psychopathological symptoms
and cognitive impairment in different subtypes of schizophrenia. The available literature
proposes different views on these links [
32
]. Nevertheless, various meta-analyses suggest
a clear relationship between negative, positive, and disorganization symptoms and cog-
nitive functioning in schizophrenia [
33
–
35
]. Seemingly, however, the analysis of the links
between psychopathological symptoms and cognitive deficits in deficit schizophrenia has
been widely neglected (c.f. [
3
,
9
]). Even though Yu et al. [
26
] found a relationship between
negative symptoms and cognitive function in both deficit and non-deficit schizophrenia,
these links differed within different cognitive domains. What is more, negative symptoms
and cognitive functions were found to be influenced by age in the deficit variant and
by age, education, and illness duration in the non-deficit type. Chen et al. [
23
] reported
negative correlations between: (i) general psychopathology symptoms and verbal memory
in first-episode drug-naive schizophrenia with the deficit syndrome; and (ii) positive symp-
toms for verbal and visual memory in the non-deficit syndrome. In turn,
Tang et al. [30]
J. Clin. Med. 2023,12, 2257 3 of 16
demonstrated a negative relationship between positive, disorganization, and negative
symptoms and certain emotions in the context of facial emotion recognition in non-deficit
schizophrenia, but not in deficit schizophrenia.
To address the above limitations, we compared different cognitive domains (speed of
processing, attention/vigilance, working memory, verbal and visual learning memory, rea-
soning and problem solving, and social cognition) and the general score of the Measurement
and Treatment Research to Improve Cognition in Schizophrenia Battery (MCCB) [
36
,
37
]
between deficit and non-deficit schizophrenia patients, along with the healthy controls.
While the relationship between psychopathological symptoms and cognitive domains in
schizophrenia has been the subject of many studies, it remains underexplored in deficit
schizophrenia. A meta-analysis of the Positive and Negative Syndrome Scale (PANSS [
38
])
suggests that it has a five-factor structure—positive symptoms, negative symptoms, disor-
ganization, affect, and resistance—that can be extremely useful for assessing the severity of
symptoms; however, it remains underused in studies on cognitive functioning in DS. Thus,
we estimated the relationships between the five PANSS factors and cognitive domains in
both clinical groups. Based on previous findings, we hypothesized that deficit schizophre-
nia patients would manifest greater cognitive impairment and overall scores relative to
non-deficit schizophrenia and the controls. Moreover, we assumed that a complex rela-
tionship would emerge between different psychopathological dimensions and cognitive
domains, and that it would differ in both clinical groups.
2. Materials and Methods
2.1. Participants
This study included 74 patients diagnosed with schizophrenia based on the Interna-
tional Statistical Classification of Diseases and Related Health Problems (ICD-10 [
39
]) and
the Mini-International Neuropsychiatric Interview (MINI) [
40
]), and 39 healthy participants
(without mental or neurological disorders). A total of 29 patients were further diagnosed
with DS (based on the criteria proposed by Carpenter et al. [
5
]; for more details concerning
recruitment and inclusion criteria, see [
41
]), and 45 with NDS. The clinical group was
recruited in cooperation with the Department of Psychiatry of the Pomeranian Medical
University and outpatient mental health clinics in Szczecin, Poland. Healthy controls were
recruited through information spread by students and staff of the local universities. The
inclusion criteria in the clinical group were: diagnosis of schizophrenia, disease duration
of
≥
10 years, age 30–55 years, and informed consent to participate in the study. In the
control group they were: age 30–55 years and informed consent to participate in the study.
The exclusion criteria were: mental illness other than schizophrenia or other neurological
disorders, alcohol or substance use disorder, chronic somatic comorbidity that may affect
cognitive functioning (e.g., severe diseases of parenchymal organs and/or cancer), and
a history of head trauma. All participants underwent a psychological and psychiatric
examination. The former included assessment of intellectual and cognitive functioning,
while the latter comprised a detailed clinical history, measurement of neuropsychiatric
symptoms, and an overall assessment of health. All patients provided written consent to
participate in the study. The study protocol was approved by the local bioethics committee.
2.2. Neuropsychological Assessment
The Polish version of the Measurement and Treatment Research to Improve Cognition
in Schizophrenia Battery (MCCB [
36
,
37
]) was used to measure different cognitive domains.
This battery includes several subtests to assess:
-
Speed of processing—Trail Making Test (TMT: Part A), Brief Assessment of Cognition
in Schizophrenia (BACS), and the Category Fluency Test: Animal Naming (CF);
- Attention/vigilance—Continuous Performance Test—Identical Pairs (CPT-IP);
-
Working memory—Letter-Number Span (LNS) and Wechsler Memory Scale-III (
WMS III
);
- Verbal learning and memory—Hopkins Verbal Learning Test-Revised (HVLT-R);
- Visual learning and memory—Brief Visuospatial Memory Test-Revised (BVMT-R);
J. Clin. Med. 2023,12, 2257 4 of 16
- Reasoning and problem solving—Neuropsychological Assessment Battery (NAB): Mazes.
- Social cognition—Mayer–Salovey–Caruso Emotional Intelligence Test (MSCEIT).
Scores for different cognitive domains and overall scores were calculated using the
mean of the nine demographically corrected T-scores using the computer application of
MCCB [37].
Moreover, general intellectual ability as indirect premorbid IQ was assessed with the
Vocabulary and Picture Completion measures of the Wechsler Adult Intelligence Scale—
Revised, a standardized tool to measure adult general intelligence [
42
]. Both subtests
were often used to measure indirect (case-control studies) and direct (longitudinal studies)
premorbid IQ in schizophrenia (Khandaker et al. [
43
]) and previous studies have demon-
strated strong links between both subtests and full IQ [
44
,
45
] in schizophrenia patients.
Based on numerous recommendations [
46
–
50
], we selected the Vocabulary subtest as a
measure of indirect premorbid crystalized IQ and Picture Completion as a measure of
indirect premorbid fluid IQ.
2.3. Clinical Assessment
We used the Positive and Negative Syndrome Scale (PANSS) [
51
,
52
] to measure
psychopathological symptoms in DS and NDS patients, adopting the five factor structure
identified by Shafer and Dazzi [
38
], including positive and negative, disorganization, affect,
and resistance symptoms. We also used the Polish versions of the Brief Negative Symptom
Scale (BNSS) [
53
] and the Self-Evaluation of Negative Symptoms (SNS) [
54
] to measure
deficit symptoms. The BNSS is a reliable tool composed of a total of 13 items to assess
five domains of negative symptoms, i.e., anhedonia, asociality, avolition, blunted affect,
and alogia. Each item is rated on a seven-point severity scale, from 0 (symptom absent)
to 6 (severe). The SNS consists of 20 self-report items, evaluating 5 subdomains (social
withdrawal, diminished emotional range, avolition, anhedonia, and alogia) over the course
of the previous week. The Global Assessment of Functioning (GAF) [
55
] was used to assess
the severity of schizophrenia and its impact on patients’ functioning.
2.4. Statistical Analysis
Analysis of the results was performed in IBM SPSS 28 (IBM Corp., Redmont, VA, USA).
Continuous variables were described in terms of means (M) and standard deviations (SD).
The Shapiro–Wilk test and skewness and kurtosis values were used to check the normality
of the distributions. We took skewness and kurtosis values ranging from
−
2 to +2 as indicat-
ing normal distribution [
56
]. Years of education, age, premorbid crystalized IQ (WAIS-R-IV
Vocabulary), and attention/vigilance, working memory, reasoning and problem solving,
social cognition, and overall score on the MCCB were normally distributed in all groups.
In the patient groups, global functioning (GAF), chlorpromazine equivalent, and duration
of illness showed normal distributions. The following were not normally distributed:
exacerbation, results for all PANSS factors, premorbid IQ (WAIS-R-IV Picture Completion),
negative symptoms on the BNSS and SNS, and scores on three cognitive indices on the
MCCB (speed of processing, verbal learning and memory, and visual learning and mem-
ory) were non-normally distributed. Before performing further analyses, we therefore
logarithmically transformed exacerbation and negative symptoms on SNS, and Box–Cox
transformed the other variables to achieve normal distributions [
57
]. The Student’s t-test
was used to investigate differences between the two clinical groups (clinical factors and
psychopathological symptoms). An analysis of variance (ANOVA) was used to examine
differences between the three groups in different aspects of cognitive domains and overall
MCCB score. The Bonferroni post hoc test was used for comparisons between groups
(for parametric tests). To calculate the magnitudes of effect sizes of differences between
groups, Cohen’s dand
ï2
(continuous variables) and Cramér’s V(categorical variables)
were used [
58
]. Furthermore, Pearson’s rcorrelation coefficients were used to assess the
relationships between psychopathological symptoms and different cognitive domains and
overall score in the clinical groups. G*Power software was used to estimate the sensitivity
J. Clin. Med. 2023,12, 2257 5 of 16
analysis for ANOVA [
59
]. According to its results, ANOVA with 113 participants across
three groups would be sensitive to effects of
ï2
= 0.12 with 95% power (p= 0.05). This
means that our study would not be able to reliably detect effects smaller than
ï2
= 0.12. An
alpha value of 0.05 was used for all analyses.
3. Results
3.1. Demographic, Psychological and Clinical Characteristics
Table 1shows the demographic, psychological, and clinical characteristics of the
groups. While there were no significant differences in age, the groups differed significantly
in years of education (p= 0.020), sex (p= 0.011), premorbid crystalized IQ measured
by WAIS-R-IV Vocabulary (p< 0.001), and premorbid fluid IQ measured by WAIS-R-IV
Picture Completion (p< 0.001). There were more males than females in the DS group,
and post hoc analyses revealed that DS patients had fewer years of education than the
HC group (
p= 0.029
), and they showed lower fluid IQ than did the NDS and HC groups
(
p= 0.008
and p< 0.001), as well as lower crystalized IQ than NDS and HC (both: p< 0.001).
Similarly, NDS patients had lower fluid and crystalized IQ than HC (both: p< 0.001). After
Holm–Bonferroni p-value correction, DS patients showed more negative symptoms and a
larger total score on PANSS (p< 0.001 and p= 0.005), more negative symptoms on BNSS
(
p< 0.001
), and more negative symptoms on SNS (p< 0.001) than NDS patients. There were
no significant differences between clinical groups in terms of antipsychotic medications,
chlorpromazine equivalent, duration of illness, exacerbation, global functioning in GAF, or
other psychopathological symptoms on PANSS (positive symptoms, disorganization, affect,
or resistance). Additionally, the distributions of the samples regarding psychopathological
dimensions from two clinical groups are presented in Figure 1.
3.2. Differences in Cognitive Domains
As shown in Table 2(T-scores before and after transformation) and Figure 2(T-scores
before transformation), the three groups differed significantly in all cognitive domains, in
speed of processing (p< 0.001), attention/vigilance (p< 0.001), working memory (p< 0.001),
verbal learning and memory (p< 0.001), visual learning and memory (p< 0.001), reasoning
and problem solving (p< 0.001), social cognition (p< 0.001), and overall score (p< 0.001).
Post hoc analysis indicated that DS patients had lower scores on speed of processing (both:
p< 0.001), attention/vigilance (p= 0.031 and p< 0.001), working memory (both: p< 0.001),
verbal learning and memory (p= 0.019 and p< 0.001), visual learning and memory (both:
p< 0.001
), social cognition (p= 0.005 and p< 0.001), and overall score (both: p< 0.001) than
both the NDS and HC groups, as well as lower scores for reasoning and problem solving
(
p< 0.001
) than the HC group. Moreover, NDS patients exhibited lower scores than the
HC for all cognitive domains (p< 0.001) and social cognition (p= 0.002). Additionally,
distributions of the samples regarding cognitive functions from three groups are presented
in Figure S1 in Supplementary Materials.
3.3. Relationships between Psychopathological Dimensions and Cognitive Domains
As can be seen in Table 3, there were no significant correlations between psychopatho-
logical symptoms and cognitive domains in DS patients. However, in NDS patients:
positive symptoms correlated negatively with speed of processing (r=
−
0.33; p= 0.027),
reasoning and problem solving (r=
−
0.31; p= 0.040), and overall score (r=
−
0.41;
p= 0.005
);
negative symptoms correlated negatively with speed of processing (r=
−
0.30; p= 0.048);
disorganization correlated negatively with speed of processing (r=
−
0.41; p= 0.005), reason-
ing and problem solving (r=
−
0.39; p= 0.008), and overall score (r=
−
0.35; p= 0.019); and
resistance correlated negatively with speed of processing (r=
−
0.46; p= 0.001). Correlation
coefficients were not corrected.
J. Clin. Med. 2023,12, 2257 6 of 16
Table 1. Demographic, psychological, and clinical characteristics of all participants.
Deficit Schizophrenia Patients
(DS) (n= 29)
Non-Deficit Schizophrenia
Patients (NDS) (n= 45)
Healthy Controls
(HC) (n= 39) F/χ2/tï2/V/d
Age: M(SD) 38.59 (6.17) 39.16 (7.21) 37.08 (7.94) 0.90 c0.02 f
Years of education: M(SD)12.66 (3.24) i*13.53 (2.64) 14.59 (2.62) 4.06 c*0.07 f
Sex: female/male 7/22 24/21 23/16 9.01 d*0.28 g
Premorbid IQ in WAIS-R-IV:
Picture Completion: M(SD)17.86 (7.60)/20.52 (13.35) b,i, ***, j * 22.56 (6.13)/29.53 (13.24) b,k *** 29.62 (3.63)/47.46 (10.34) b43.27 c*** 0.44 f
Vocabulary: M(SD)33.97 (14.47) ) i ***, j ** 43.40 (10.18) k*** 56.18 (6.55) 38.81 c*** 0.41 f
Antipsychotic medications:
Atypical: n(%) 20 (68.97) 29 (64.44) -
2.09 d0.17 g
Atypical and typical: n(%) 8 (27.58) 12 (26.67) -
Typical: n(%) 0 (0.00) 3 (6.67) -
No medications: n(%) 1 (3.45) 1 (2.22) -
Chlorpromazine equivalent (mg):
M(SD)695.86 (311.57) 644.04 (309.71) - 0.71 e0.17 h
Duration of illness: M(SD) 16.97 (5.73) 14.00 (5.14) - 2.32 e0.55 h
Exacerbation: M(SD) 5.69 (2.44)/1.64 (0.48) a6.49 (5.01)/1.65 (0.64) a-−0.11 e−0.03 h
Global functioning in GAF: M(SD) 50.93 (14.34) 58.40 (14.21) - −2.20 e−0.52 h
Psychopathological symptoms in
PANSS:
Positive symptoms: M(SD)7.38 (2.73)/5.28 (0.06) b8.07 (4.37)/5.28 (0.06) b- 0.00 e0.00 h
Negative symptoms: M(SD)22.24 (4.66)/5.85 (0.01) b13.80 (5.19)/5.80 (0.03) b- 7.45 e*** 1.51 h
Disorganization: M(SD)12.62 (3.48)/5.36 (0.02) b11.42 (3.98)/5.34 (0.03) b- 1.93 e0.46 h
Affect: M(SD)8.24 (3.45)/5.29 (0.06) b9.29 (3.53)/5.31 (0.05) b-−1.68 e−0.40 h
Resistance: M(SD)4.34 (0.61)/5.04 (0.04) b4.89 (2.43)/5.05 (0.06) b-−1.07 e−0.23 h
Total score: M(SD)56.83 (11.17)/5.40 (0.01) b49.33 (14.68)/5.40 (0.01) b- 3.31 e*0.73 h
Negative symptoms in BNSS:
Total score: M(SD)47.07 (9.28)/2.63 (0.43) b20.07 (12.68)/1.27 (0.66) b- 9.87 e*** 2.35 h
Negative symptoms in SNS:
Total score: M(SD) 22.28 (7.38)/3.03 (0.41) a9.71 (6.89)/2.05 (0.70) a-−7.63 e*** 1.63 h
BNSS = Brief Negative Symptom Scale. GAF = Global Assessment of Functioning. PANSS = Positive and Negative Syndrome Scale. SNS = Self-Evaluation of Negative Symptoms.
WAIS-R-IV = Wechsler Adult Intelligence Scale Revised Fourth Edition. Chlorpromazine equivalents were calculated based on a proposition by [
60
].
a
Mean and standard deviation after
logarithmic transformation.
b
Mean and standard deviation after Box–Cox transformation.
c
One-way analysis of variance Ftest.
d
Chi-squared test.
e
Student’s t-test.
f
Eta squared
effect size: small (0.01–0.059), medium (0.06–0.139), large (0.14–1.00).
g
Cramer’s Veffect size: small (0.10–0.19), medium (0.20–0.59), large (0.60–1.00).
h
Cohen’s deffect size: small
(0.20–0.49), medium (0.50–0.79), large (0.80 <). All p-values for ANOVA.
i
DS patients vs. HC participants.
j
DS patients vs. NDS patients.
k
NDS patients vs. HC participants.
*p< 0.05
,
** p< 0.01, *** p< 0.001. (after Holm–Bonferroni p-value correction for Student’s t-test).
J. Clin. Med. 2023,12, 2257 7 of 16
Table 2. Comparison of MCCB cognitive domains between all participants...
Deficit Schizophrenia Patients
(DS) (n= 29)
Non-Deficit Schizophrenia
Patients
(NDS) (n= 45)
Healthy Control (HC)
(n= 39) Fï2
Speed of processing 25.93 (11.53)/3.19 (0.49) a,c ***,d *** 34.62 (12.40)/3.51 (0.36) a,e *** 53.15 (9.66)/3.97 (0.18) a43.25 *** 0.44
Attention/vigilance 23.69 (11.58) c***,d *30.22 (8.76) e*** 42.90 (11.55) 30.12 *** 0.35
Working memory 27.72 (11.40) c***,d *** 40.67 (10.95) e*** 54.51 (9.57) 53.66 *** 0.49
Verbal learning and memory 34.76 (9.24)/3.54 (0.24) a,c ***,d *40.09 (10.11)/3.68 (0.24) a,e *** 48.95 (7.50)/3.90 (0.15) a24.27 *** 0.31
Visual learning and memory 28.00 (13.78)/5.12 (4.56) b,c ***,d *** 41.71 (12.65)/9.90 (5.05) b,e *** 56.90 (8.21)/17.08 (4.29) b57.23 *** 0.51
Reasoning and problem solving 37.24 (7.85) c*** 41.49 (11.15) e*** 54.44 (9.20) 30.50 *** 0.36
Social cognition 48.24 (16.42) c***,d ** 58.00 (12.40) e** 67.87 (9.33) 20.20 *** 0.27
Overall score 20.31 (12.88) c***,d *** 34.87 (11.78) e*** 56.69 (9.13) 91.29 *** 0.62
MMCB = cognitive functioning was evaluated with Measurement and Treatment Research to Improve Cognition in Schizophrenia. F= Analysis of variance Ftest.
ï2
= Eta squared effect
size: small (0.01–0.059), medium (0.06–0.139), large (0.14–1.00).
a
Mean and standard deviation of T-scores after logarithmical transformation.
b
Mean and standard deviation of T-scores
after Box–Cox transformation. cDS patients vs. HC participants. dDS patients vs. NDS patients. eNDS patients vs. HC participants. * p< 0.05, ** p< 0.01, *** p< 0.001.
Table 3. Relationship between psychopathological symptoms measured with the PANSS and cognitive domains measured with the MCCB in the patient groups.
Deficit Schizophrenia Patients (DS) (n= 29)
Speed of
Processing Attention/Vigilance Working Memory Verbal Learning
and Memory
Visual Learning
and Memory
Reasoning and
Problem Solving Social Cognition Overall Score
r r r r r r r r
Positive
symptoms 0.08 0.02 −0.10 0.13 −0.16 −0.34 0.01 −0.11
Negative
symptoms 0.04 −0.13 0.05 0.13 −0.26 0.01 −0.02 −0.08
Disorganization −0.02 0.10 0.07 0.26 −0.04 −0.24 0.04 0.02
Affect 0.17 −0.29 0.17 0.08 −0.05 0.26 0.11 0.11
Resistance −0.31 −0.01 −0.35 −0.07 −0.25 −0.30 −0.14 −0.34
J. Clin. Med. 2023,12, 2257 8 of 16
Table 3. Cont.
Non-Deficit Schizophrenia Patients (NDS) (n= 45)
Speed of
Processing Attention/Vigilance Working Memory Verbal Learning
and Memory
Visual Learning
and Memory
Reasoning and
Problem Solving Social Cognition Overall Score
r r r r r r r r
Positive
symptoms −0.33 * −0.10 −0.25 −0.15 −0.28 −0.31 * −0.25 −0.41 **
Negative
symptoms −0.30 * −0.03 0.06 0.20 −0.04 −0.12 0.00 −0.10
Disorganization −0.41 ** −0.03 −0.22 −0.08 −0.18 −0.39 ** −0.12 −0.35 *
Affect −0.22 −0.10 −0.18 0.08 −0.11 −0.13 −0.05 −0.20
Resistance −0.46 ** −0.01 −0.01 −0.13 −0.11 −0.27 −0.13 −0.25
MMCB = cognitive functioning was evaluated with Measurement and Treatment Research to Improve Cognition in Schizophrenia. PANSS = Positive and Negative Syndrome Scale.
*p< 0.05, ** p< 0.01.
J. Clin. Med. 2023,12, 2257 9 of 16
J.Clin.Med.2023,12,xFORPEERREVIEW7of16
Figure1.Distributionsofthesamplesonpsychopathologicaldimensionsfromtwoclinicalgroups—
rawscores(PANSS:(A)=positivesymptoms;(B)=negativesymptoms;(C)=disorganization;(D)
=affect;(E)=resistance;(F)=totalscore;(G)=BNSS—totalscore,and(H)=SNS—totalscore).BNSS
=BriefNegativeSymptomScale.PANSS=PositiveandNegativeSyndromeScale.SNS=Self‐
EvaluationofNegativeSymptoms.
Figure 1.
Distributions of the samples on psychopathological dimensions from two clinical
groups—raw
scores (PANSS: (
A
) = positive symptoms; (
B
) = negative symptoms; (
C
) = disorga-
nization;
(D) = affect
; (
E
) = resistance; (
F
) = total score; (
G
) = BNSS—total score, and (
H
) = SNS—total
score). BNSS = Brief Negative Symptom Scale. PANSS = Positive and Negative Syndrome Scale.
SNS = Self-Evaluation of Negative Symptoms.
J. Clin. Med. 2023,12, 2257 10 of 16
J.Clin.Med.2023,12,xFORPEERREVIEW9of16
Figure2.Comparisonofcognitivefunctionsbetweenparticipantsfromthreegroups—untrans‐
formedT‐scores(MCCB:(A)=speedofprocessing;(B)=attention/vigilance;(C)=workingmemory;
(D)=verballearningandmemory;(E)=visuallearningandmemory;(F)=reasoningandproblem
solving;(G)=socialcognition,and(H)=overallscore).Inallboxplots,thebottomendofthebox
designatesthefirstquartile,alinewithintheboxindicatesthemedian,andthetopendofthebox
showsthethirdquartile.*indicatevalues1.5timestheinterquartilerangebelowthefirstquartile
andabovethethirdquartile.Crossesrepresentaveragevalues.Circlesdesignateindividualobser‐
vations.MCCB=MeasurementandTreatmentResearchtoImproveCognitioninSchizophrenia.
Figure 2.
Comparison of cognitive functions between participants from three groups—untransformed
T-scores (MCCB: (
A
) = speed of processing; (
B
) = attention/vigilance; (
C
) = working memory;
(D) = verbal
learning and memory; (
E
) = visual learning and memory; (
F
) = reasoning and problem
solving; (
G
) = social cognition, and (
H
) = overall score). In all box plots, the bottom end of the box
designates the first quartile, a line within the box indicates the median, and the top end of the box
shows the third quartile. * indicate values 1.5 times the interquartile range below the first quartile and
above the third quartile. Crosses represent average values. Circles designate individual observations.
MCCB = Measurement and Treatment Research to Improve Cognition in Schizophrenia.
J. Clin. Med. 2023,12, 2257 11 of 16
4. Discussion
In this study, we examined differences in cognitive performance based on the use of
the MCCB patients with deficit schizophrenia (DS) and non-deficit schizophrenia (NDS),
as well as healthy controls. Moreover, we investigated the relationship between five
psychopathological dimensions and cognitive domains.
Our results suggest greater cognitive deficits in DS patients compared to NDS patients
in all examined cognitive domains, except reasoning and problem solving. They can,
therefore, especially alongside qualitative analysis of distributions of cognitive domains
in the clinical groups and healthy controls, further support the construct validity of the
DS versus NDS distinction. In their meta-analysis, Bora et al. [
3
] showed similar results,
i.e., significant differences between patient groups in processing speed, attention, working
memory, verbal and visual memory, and social cognition. Moreover, we demonstrated
greater general cognitive dysfunctions in DS patients as reflected by overall scores on
the MCCB. Some authors suggest that DS patients manifest a general rather than specific
cognitive dysfunction [
8
]. However, the absence of inter-group differences in reasoning
and problem solving may mean that there are some cognitive domains that are less affected
in deficit schizophrenia. Admittedly, the MCCB was not designed to measure executive
functions, but reasoning and problem solving as measured by the Neuropsychological
Assessment Battery—Mazes is also a measure of planning skills, which some researchers
classify as executive functions [
61
]. It has been shown that in patients with DS, these
functions are usually impaired to a greater extent, but not all studies corroborate these
observations [
16
]. In earlier studies, tests such as the Wisconsin Card Sorting Test, the Trail
Making Test, or the Stroop Test were mainly used to assess executive functions. We found
no studies that used the NAB—Mazes, so it is difficult to compare our results against those
of other authors. However, Fervaha et al. [
27
] found significant group differences, but a
small effect size, using Mazes from WISC-R. It seems that further research is needed to
determine whether some aspects of executive functions, such as planning, are actually
more or less affected by the deficit syndrome.
Our results suggest greater impairments in deficit schizophrenia in terms of working
memory measured by two tests (Letter-Number Span and Wechsler Memory Scale-III)
included in the MCCB, which are designed to assess pattern-spatial memory and verbal
memory, with a test that burdens the central executive system to a greater extent. Similar
results have been shown in previous studies using simpler tests to assess verbal working
memory and the SS test for visuospatial working memory [
11
,
27
]. We also found greater
deficits in verbal and non-verbal learning in people with DS, in line with the results of
previous studies using the same tests (Hopkins Verbal Learning Test-Revised and Brief
Visuospatial Memory Test-Revised [
27
]). Our results therefore demonstrate that people
with DS are affected not only by memory deficits measured by single task trials, but also by
more complex learning tests involving a series of repeated learning attempts using verbal
and visual material. Previous studies showed greater deficits in social cognition in DS as
measured by simple facial emotion recognition tests. Our study further suggests that DS
patients may have deficits in theory of mind as assessed by a more complex task in which
subjects must interpret a series of stories and empathize with the thinking of others.
Moreover, we showed that both clinical groups exhibited significantly lower scores in
all cognitive domains and the overall score compared to healthy individuals, which means
that both DS and NDS patients have general cognitive impairments. Previous studies using
the MCCB in schizophrenia have repeatedly demonstrated the presence of such deficits [
62
].
Our study also concludes that the MCCB is sensitive to cognitive deficits, both in various
cognitive domains and in general cognitive functioning, in deficit schizophrenia. Due to the
fact that DS patients showed greater functional and structural abnormalities of the brain
compared to NDS patients and healthy people [
6
,
7
], it would be worthwhile in the future to
determine the relationship between the volume of various brain structures and the integrity
of the white matter of the bundles connecting cognitively important structures with the
results in individual cognitive domains assessed by the MCCB. Such research could shed
J. Clin. Med. 2023,12, 2257 12 of 16
more light on the role of changes in the brain, which in deficit schizophrenia, may be one
of the potential neurobiological correlates of cognitive dysfunction, and which, according
to both neurodevelopmental and neurodegenerative theories, most likely contribute to the
poorer functioning of patients.
We did not observe a significant relationship between psychopathological symptoms
and cognitive functions in DS patients, which may very likely be attributed to a small
sample size. However, only few previous studies analyzed the relationship between psy-
chopathological symptoms and cognitive functions in deficit schizophrenia. Their results
were also inconsistent, as some showed an association between negative symptoms and
attention [
26
] or global symptoms and verbal memory [
23
]. In turn, Tang et al. [
30
] did not
show any relationship between psychopathological symptoms and facial emotion recogni-
tion. Perhaps the inter-group relationships between deficit schizophrenia and cognitive
disorders (based on comparisons of different schizophrenia patient populations) are not
the same as intra-group relationships (based on correlation analysis). A certain explanation
for the lack of such a correlation in DS patients may be that the PANSS does not fully
measure the symptoms characteristic of the deficit syndrome, i.e., the negative symptoms
that initially occur. It seems that further studies are needed in which other scales should
be used to assess deficit symptoms in the context of their relationship with cognitive func-
tions in DS patients. On the other hand, a relationship between some psychopathological
symptoms and cognitive functions emerged in non-deficit schizophrenia, where positive,
negative, and resistance symptoms were negatively associated with speed of processing,
and positive and disorganization symptoms with reasoning and problem solving. Similar
results were provided by previous studies [
32
–
34
]. However, due to the fact that the non-
deficit schizophrenia set is a very heterogeneous group, it is difficult to clearly explain the
relationships with some cognitive domains. Several theoretical models have been proposed
in the literature [
32
], explaining, for example, the relationship between negative symptoms
and cognitive functions, but our study does not allow for the verification of such models.
Therefore, future studies are needed in which methodological solutions will allow for a
better explanation of the relationship between psychopathology and cognitive disorders
in schizophrenia.
Moreover, our results suggest psychopathological presentation between DS and NDS
patients. Indeed, differences in psychopathology emerged within the negative dimension
of the disease spectrum measured by the three administered scales (PANNS, BNSS, and
SNS). Thus, in line with other studies on psychopathological manifestation in DS [
4
,
15
,
63
],
our findings, combined with qualitative analysis of distributions of psychopathological
dimensions, support the postulated construct validity of the DS-NDS distinction. Our sam-
ple did not differ significantly in terms of age, antipsychotic medications, chlorpromazine
equivalent, duration of illness, or exacerbation. Additionally, no inter-group differences
emerged in terms of general functioning as measured by the GAF, which is inconsistent
with other reports [
63
] and may result from a small sample size. The absence of differences
in psychopathology in other dimensions is likely attributable to our study design. In
addition, since they were not in acute psychosis, the observed negative symptoms were not
due to other psychopathology, but reflected the general DS criteria.
This study has some potential limitations. The first limitation is that the group of
respondents was relatively small. The small sample of patients limits the generalizability of
the conclusions. It would be of great scientific value to increase the number of participants
in the study. The second limitation was that the proportion of females and males in each
patient group was not homogeneous (there were more male DS patients). There are some
findings suggesting that female hormones benefit the brain areas involved in cognitive
function [
64
]. This may be an alternative explanation for why NDS patients performed
better on cognitive tasks than DS patients. However, it is noted that sex is one of the risk
factors for deficit syndrome in schizophrenia. Previous studies show that more males than
females have a diagnosis of deficit schizophrenia [
3
,
4
]. The third limitation is that there were
significant differences in patient groups in fluid and crystalized intelligence. Some previous
J. Clin. Med. 2023,12, 2257 13 of 16
studies suggest that DS patients manifest poorer intellectual functioning than NDS patients,
which is probably an element characterizing this clinical population. Moreover, we used
only two subtests from the WAIS-R to measure indirect premorbid IQ. Some researchers
recommend cautious use of abbreviated forms when it is necessary to estimate the factor
index scores, and many data suggest that a statistical search for a “best” short form is largely
futile [
50
]. Thus, short forms should be selected on the basis of their efficiency in providing
the required information [
47
]. The fourth limitation concerns the inclusion criteria for the
patient groups: illness duration of
≥
10 years and age of 30–50 years. We sought to compare
DS and NDS patients as a more homogenous group. However, as this may (significantly)
restrict our ability to generalize our results to the entire schizophrenia population, our
results should be interpreted with great caution. Our study is cross-sectional and as such,
cannot control for potential cohort effects. Longitudinal studies have many advantages for
describing differences between clinical trials because this type of study design allows for
the observation of changes over time in the same participants.
5. Conclusions
Our study found cognitive impairments in patients with both deficit and non-deficit
schizophrenia. The severity of these impairments was greater in deficit schizophrenia
patients, except for reasoning and problem-solving. Our findings suggest that the MCCB
battery is sensitive for detecting cognitive dysfunctions, not only in non-deficit schizophre-
nia but also in deficit schizophrenia. Psychopathological dimensions seem to play a signifi-
cant role in the cognitive performance of non-deficit schizophrenia patients only, but their
relationship seems to be complex. However, these conclusions have limited generalizability,
as the sample size was small. Finally, our results suggest that non-deficit schizophrenia is
a heterogeneous concept, and some patients with non-deficit schizophrenia may present
persistent negative symptoms which may not necessarily be considered as primary.
Supplementary Materials:
The following supporting information can be downloaded at: https:
//www.mdpi.com/article/10.3390/jcm12062257/s1, FigureS1. Distributions of the samples on
cognitive functions from three groups – untransformed T-scores (MCCB: (A) = speed of processing;
(B) = attention/vigilance; (C) = working memory; (D) = verbal learning and memory; (E) = visual
learning and memory; (F) = reasoning and problem solving; (G) = social cognition, and (H) = overall
score). MCCB = Measurement and Treatment Research to Improve Cognition in Schizophrenia.
Author Contributions:
Conceptualization, P.P. (Piotr Plichta) and E.T.; funding acquisition, P.P. (Piotr
Plichta) and E.T.; investigation, P.P. (Piotr Plichta), E.T., M.B., K.R.-O. and P.P. (Piotr Podwalski);
methodology, P.P. (Piotr Plichta) and E.T.; project administration, P.P. (Piotr Plichta) and E.T.; supervi-
sion, B.M., J.K.-M., J.S., L.S. and M.M.; writing—original draft, P.P. (Piotr Plichta); writing—review
and editing, P.P. (Piotr Plichta), E.T., M.B., A.M., K.R.-O., K.W., P.P. (Piotr Podwalski), J.K.-M., J.S., L.S.
and M.M. All authors have read and agreed to the published version of the manuscript.
Funding:
This work was supported by the Pomeranian Medical University in Szczecin (FSN-337-441
06/2016 and FNS-246 05/2017) and the Faculty of Humanities at the University of Szczecin (504-442
3000-240-940/2015/2016). The project was also financed by the Polish Minister of Science and Higher
Education’s program named “Regional Initiative of Excellence” 2019–2022 (002/RID/2018/19) to the
amount of 12,000,000 PLN.
Institutional Review Board Statement:
The study was conducted according to the guidelines of the
Declaration of Helsinki and approved by the Ethics Committee of Pomeranian Medical University
(KB-0012/49/17 from 27 March 2017).
Informed Consent Statement:
Written informed consent was obtained from all subjects involved in
the study.
Data Availability Statement:
Data and materials for the experiments reported here are available
from the corresponding author on reasonable request.
Conflicts of Interest: The authors declare no conflict of interest.
J. Clin. Med. 2023,12, 2257 14 of 16
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