Hindawi

Behavioural Neurology
Volume 2022, Article ID 3422578, 5 pages
https://doi.org/10.1155/2022/3422578

Research Article
Verbal Reasoning Impairment in Parkinson’s Disease

Antonina Luca ,1 Giulia Donzuso ,1 Concetta D’Agate,1 Claudio Terravecchia ,1

Calogero Cicero Edoardo ,1 Giovanni Mostile ,1,2 Giorgia Sciacca ,1
Alessandra Nicoletti ,1 and Mario Zappia 1
1
Department of Medical, Surgical Sciences and Advanced Technologies “G.F. Ingrassia”, University of Catania, Catania, Italy
2
Oasi Research Institute-IRCCS, Troina, Italy

Correspondence should be addressed to Antonina Luca; antolucaster@gmail.com

Received 3 October 2022; Revised 17 November 2022; Accepted 1 December 2022; Published 10 December 2022

Academic Editor: Luigi Trojano

Copyright © 2022 Antonina Luca et al. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Background. The aim of this study was to assess verbal reasoning (VR) functioning in patients with Parkinson’s disease (PD) and
healthy controls (HCs). Methods. The non-demented PD patients and HCs matched by age and global cognition were enrolled in
this study. VR was assessed with the verbal reasoning test (VRT), total score, and subsets. Results. Eighty-seven PD patients (51
men; mean age 63:8 ± 7:9 years) and 87 HCs (46 men; mean age 63:7 ± 8:0 years) were enrolled. At univariate analysis, PD
patients presented a significantly lower score in the VRT subset classification (12:3 ± 2:1) than HCs (12:9 ± 1:7) with an odds
ratio (OR) of 0.8 (95% confidence interval [CI] 0.70–0.98; p = 0:003). The strength of association was also confirmed at
multivariate analysis (OR = 0.8, 95% CI 0.70–0.98; p = 0:003). Moreover, in PD patients, a statistically significant positive
correlation was found between VRT-classification and MoCA scores (r = 0:330; p = 0:002). Conclusions. PD patients presented
lower VR performance than HCs.

1. Introduction Parkinson’s disease (PD) is a neurodegenerative disorder

characterized by both motor (rest tremor, bradykinesia, and
Verbal reasoning (VR) is a cognitive ability considered essen- rigidity) and non-motor symptoms. Among the latter, cognitive
tial for understanding, reasoning, and problem-solving using impairment, from mild cognitive decline to overt dementia,
concepts conveyed by words, not limited to simply vocab- probably represents the most common and may conceivably
ulary comprehension or verbal fluency, leading to draw occur at any disease stage, even before the occurrence of motor
inferences from given information [1]. A “good” VR symptoms [5] or in combination with other non-motor symp-
requires the involvement of many cognitive abilities toms [6]. Although all cognitive domains (i.e., episodic mem-
including attention, working memory, abstraction, and ory, attention, and language) may potentially be impaired, the
categorization skills, crucial for cognitive performance frequent and predominant impairment of EF in PD has been
and mainly related to executive functioning (EF) [2]. In constantly reported [7, 8]. However, even if EF and VR are
particular, the ability to generalize principles from a spe- interconnected, to the best of our knowledge, to date, only few
cific and concrete one (abstraction), or to form concepts studies have investigated VR abilities in PD patients [9].
applying general rules (conceptualization and classifica- The aim of the present study was to assess VR function-
tion), represents cognitive skills interconnected with both ing in a group of non-demented PD patients and in a group
EF and VR. of healthy controls (HCs).
Actually, the impairment of these skills could lead, in
practical application, to difficulties to learn from experiences
2. Methods
in a logical, meaningful, and organized manner approaching
daily life events as they were always unexpected as a “novel Clinically established non-demented PD patients, diagnosed
experience [3, 4]. according to the Movement Disorders Society-PD criteria
2 Behavioural Neurology

[10] and a group of HCs matched by age and global cogni- Table 1: Demographic and clinical characteristics.
tion, assessed with the administration of the Montreal Cog-
nitive Assessment (MoCA), were enrolled in this study. As PD, n = 87 HCs, n = 87 p-Value
part of normal diagnostic work-up, to exclude secondary Sex (men) 51 (58.6) 46 (52.9) 0.445
Parkinsonism and to support the diagnosis of PD, all PD Age (years) 63:8 ± 7:9 63:7 ± 8:0 0.939
patients performed a brain magnetic resonance imaging Education (years) 11:8 ± 4:3 11:1 ± 3:9 0.206
(MRI) [11]. Demographic, clinical, and pharmacological
MoCA score 23:4 ± 3:1 23:6 ± 2:9 0.410
data were recorded. Levodopa equivalence daily dosage
(LEDD) was calculated [12]. Disease duration (years) 5:3 ± 3:2 — —
All participants referred to the Movement Disorders UPDRS-ME score 27:1 ± 9:5 — —
Center of the University Hospital “Policlinico-San Marco” 2:2 ± 0:6
Hoeh and Yahr stage — —
of Catania, Italy. The study was approved by the ethical
committee, and written informed consent was obtained LEDD (mg/die) 423:9 ± 320:4 — —
from all enrolled subjects. Data are expressed as mean ± standard deviation, and number and percentage.
Abbreviations: PD = Parkinson’s disease; HCs = healthy controls; UPDRS-
ME = Unified Parkinson’s Disease Rating Scale–Motor Examination;
2.1. Clinical and Neuropsychological Assessment. All enrolled MoCA = Montreal Cognitive Assessment; LEDD = levodopa equivalent dosage.
subjects underwent a standard neurological examination
performed by movement disorders specialists. For PD
confounders. The significance level was set at 0.05, and the
patients, the severity of motor status was evaluated with
95% confidence intervals (CIs) were calculated.
the Unified Parkinson’s Disease Rating Scale-Motor Exami-
nation section (UPDRS-ME) before levodopa intake. PD
patients underwent the neuropsychological evaluation two 3. Results
hours after levodopa intake. The MoCA was administered
Eighty-seven PD patients (51 men; mean age 63:8 ± 7:9
to match PD patients and HCs according to general cogni-
years) and 87 HCs (46 men; mean age 63:7 ± 8:0 years) were
tive abilities. According to the Movement Disorders Society
enrolled. Demographic and general characteristics of the two
level I diagnostic criteria, patients obtaining a pathological
groups were shown in Table 1.
MoCA score (MoCA < 26) were considered as suffering from
According to MDS level I diagnostic criteria [13], out of
mild cognitive impairment (MCI) [13].
the 87 subjects, 60 (68.9%) had MCI. A significantly higher
VR was assessed with the verbal reasoning test (VRT),
percentage of PD patients presented pathological perfor-
one of the few tests available to assess VR functioning. It is
mance at the VRT subset classification (n = 53, 60.9%) than
made up of 7 subsets, each of which has 7 items and inves-
HCs (n = 36, 41.3%; odds ratio [OR] = 2.2; 95% CI 1.20–4.04;
tigates a different aspect of reasoning, so that the total items
p = 0:010). At univariate analysis, PD patients presented a
are 49. The subsets are absurdities, intruders, relationships,
significantly lower score at the VRT subset classification
and differences; idiomatic expressions; family relations; and
(12:3 ± 2:1) than HCs (12:9 ± 1:7; OR = 0.8; 95% CI 0.70–
classification. Each subset has its own score, and the sum
0.98; p = 0:033; Table 2).
of all 7 subsets produces the total score, corrected by age
The strength of association was also confirmed at multi-
and education [2].
variate analysis adjusting for age, sex, education, and disease
duration, considered a priori confounders (OR = 0.8, 95% CI
2.2. Statistical Analysis. Data were analyzed using the 0.70–0.98; p = 0:033). No significant differences were found
STATA 16.0 software package (Stata Statistical Software: when comparing the two groups in the others VRT subset.
Release 16, StataCorp LLC, College Station, TX, USA). Moreover, only among PD patients, a statistically signif-
Quantitative variables were expressed as mean and standard icant positive correlation was found between VRT-
deviation. Qualitative variables were expressed as number classification and MoCA scores (r = 0:330; p = 0:002 ;
and percentage. The differences between means and the dif- Figure 1). At the linear regression, this correlation was con-
ferences between proportions were evaluated by the t-test firmed also adjusting for age, sex, education, and disease
and the Chi-square test, respectively. duration (coef = 0.289; 95% CI 0.02–0.55; p = 0:035).
Logistic regression, univariate analysis, was performed to
assess possible associations between PD and VRT scores 4. Discussion
(total and subset scores) analyzed as both categorical (path-
ological/normal values according to age and education In the present study, PD patients, compared to age and
adjusted cut-off) and continuous variables. Subsequently, global cognition matched HCs, presented a lower score in
multivariate analysis adjusted by sex, age, education, and the VRT total score and in almost all subsets, even if the sta-
disease duration, considered a priori confounders, was tistically significant difference was reached only for the “clas-
performed. sification” one.
Finally, Pearson’s correlation analysis was performed to Moreover, in our study, only in PD patients, the score
investigate possible correlations between VRT and MoCA obtained in the VRT-classification subset was positively cor-
scores. Linear regression was then carried out, adjusting for related with the MoCA score. Actually, the VRT-
sex, age, education, and disease duration, considered a priori classification subset explores the same cognitive ability
Behavioural Neurology 3

Table 2: Verbal reasoning in PD and HCs. Univariate analysis.

PD, n = 87 HCs, n = 87 OR 95% CI p-Value

Absurdities 10:4 ± 2:4 10:8 ± 2:6 0.9 0.84–1.07 0.399
Absurdities, pathological performance <11.73 59 (67.8) 52 (59.8) 1.4 0.76–2.63 0.270
Intruders 10:5 ± 2:7 10:2 ± 3:0 1.0 0.93–1.14 0.546
Intruders pathological performance <12.63 58 (66.7) 65 (74.7) 0.7 0.35–1.30 0.245
Relationships 9:0 ± 3:4 9:4 ± 2:9 0.9 0.87–1.05 0.370
Relationships pathological performance <12.20 73 (83.9) 66 (75.8) 1.6 0.78–3.52 0.188
Differences 12:1 ± 1:9 13:1 ± 6:5 0.9 0.77–1.05 0.212
Differences pathological performance <12.91 48 (55.2) 42 (48.2) 1.3 0.72–2.39 0.363
Idiomatic expressions 11:3 ± 2:3 11:6 ± 2:2 0.9 0.81–1.06 0.314
Idiomatic expressions pathological performance <11.83 40 (45.9) 42 (48.3) 0.9 0.50–1.65 0.761
Family relationship 8:1 ± 4:0 8:7 ± 3:1 0.9 0.87–1.03 0.207
Family relationship pathological performance <11.0 68 (78.2) 77 (88.5) 0.5 0.20–1.06 0.071
Classifications 12:3 ± 2:1 12:9 ± 1:7 0.8 0.70–0.98 0.033
Classifications pathological performance <13.20 53 (60.9) 36 (41.3) 2.2 1.20–4.04 0.010
Total score 73:5 ± 12:5 76:4 ± 11:5 0.9 0.95–1.00 0.115
Total score pathological performance <84.27 67 (77.0) 64 (73.5) 1.2 0.60–2.40 0.589
Data are expressed as mean ± standard deviation, and number and percentage. Abbreviations: PD = Parkinson’s disease; HC = healthy controls; OR = odds
ratio; CI = confidence intervals.p-value<0.005.

30

25
MoCA score

20

15
5 10 15
VRT-Classifications score

Figure 1: Pearson’s correlation between MoCA scores and VRT-classification in patients with Parkinson’s disease.

explored by the classification subset of the Frontal Assess- ries. In particular, in the VRT, the classification ability was
ment Battery, which has been recently correlated with the assessed asking the participant to determine the category to
MoCA score in an Italian sample of healthy individuals [14]. which triplets of words belong (i.e., “What are Milan, Rome
Classification subset is related to the ability of the indi- and Naples?”).
vidual to group words into categories, to individualize the To the best of our knowledge, to date, only few studies
super-ordinate concept, detecting similarities between have assessed VR in PD patients. In particular, Natsopoulos
objects belonging to the same semantic category. This ability et al. compared 27 PD patients and 27 HCs in both deduc-
needs understanding the deeper relationship between tive (i.e., syllogism) and inductive (i.e., classification) verbal
objects, rather than simply collocating it hierarchical catego- reasoning reported impaired performance in PD patients,
4 Behavioural Neurology

in particular in those patients with longer disease duration Ethical Approval

and more severe motor impairment [9].
Relatively, more recently, Young et al. [15] reported that This study was performed in line with the principles of the
PD patients (n.19) presented lower VR performance than Declaration of Helsinki and has been approved by the ethical
HCs (n = 20), also supporting the interplay between VR committee of the University Hospital “Policlinico-San
and difficulties in everyday functioning based on real-life Marco” of Catania, Italy. Protocol number: 123/2021/PO.
ecological situations (i.e., money management, food prepa-
ration, and medication use). Although our findings are in Consent
agreement with the studies performed by Natsopoulos
et al. [9] and Young et al. [15], the data are difficult to com- All the enrolled subjects signed the consent to participate.
pare due to methodological issues related to the different
tests performed to assess VR and the small sample size of Conflicts of Interest
the previous studies.
From the neuroanatomical point of view, previous MRI The author(s) declare(s) that they have no conflicts of
studies associated the impairment in classification ability to interest.
the damage of the prefrontal cortex [16], whose thickness
in PD patients has been frequently observed [17, 18]. Authors’ Contributions
Considering that VR is nothing but “understanding,”
“reasoning,” and “thinking” using concepts conveyed by AL: performed research project conception, organization,
words (but which go beyond the “simple” understanding of and execution; carried out statistical analysis design and exe-
the term), it could be deducted that its impairment could cution; and also wrote review and critique for the manu-
be associated with poor social relationships and quality of script. GD: performed research project organization and
life. VR could in fact be considered crucial for daily life execution; carried out statistical analysis design and execu-
because it allows people to better understand the relation- tion; and also wrote review and critique for the manuscript.
ship between objects, concepts, and complicated events. As CD, CT, CEC, GM, and GS: performed research project exe-
a matter of fact, deepening knowledge on this topic may be cution and wrote review and critique for the manuscript. AN
useful not only in terms of theory enhancing but also for a and MZ: performed research project conception, organiza-
better clinical and rehabilitative approach empowering tion; carried out statistical analysis design and execution;
patient’s interpersonal relationships. and also wrote review and critique for the manuscript.
We are aware that some limits should be taken into
account when interpreting our data. Due to The hospital- Acknowledgments
based design of the study did not allow us to ruled out a
selection bias related to the enrolment of more severe cases. This research did not receive specific funding. It has been
However, the majority of PD patients enrolled in our study performed as part of the employment of the authors in the
presented a short disease duration and a PD stage mild to University Hospital “Policlinico-San Marco” of Catania,
moderate. Moreover, although patients with dementia were Italy.
excluded from the study, not all the enrolled patients
obtained “normal” age and education adjusted scores at the References
MoCA. However, it should be noted that PD and HCs were
age and MoCA matched; furthermore, Santangelo et al. [19], [1] P. N. Johnson-Laird, “Levels of representation,” Science,
considering that several items of the MoCA may be “cultur- vol. 239, no. 4847, pp. 15461547, 1988.
ally biased,” suggested to apply in the Italian population a [2] B. Basagni, C. Luzzatti, E. Navarrete et al., “VRT (verbal rea-
reduced cut-off with respect to those proposed in the origi- soning test): a new test for assessment of verbal reasoning. Test
nal version [20]. Finally, although the MoCA is considered realization and Italian normative data from a multicentric
study,” Neurological Sciences, vol. 38, no. 4, pp. 643–650, 2017.
particularly sensitive in detecting executive dysfunctions,
[3] G. Davies and A. Piovesana, “Adult verbal abstract reasoning
the lack of a more “comprehensive” neuropsychological
assessment instruments and their clinimetric properties,” The
assessment did not allow us to clearly define the nature of Clinical Neuropsychologist, vol. 29, no. 7, pp. 1010–1033, 2015.
the PD-specific VR deficit.
[4] M. D. Lezak, D. B. Howieson, and D. W. Loring, Neuropsycho-
However, to the best of our knowledge, to date, our study logical Assessment, Oxford University Press, New York, NY,
is the larger study assessing VR in PD patients. Further stud- 4th edition, 2004.
ies are necessary to confirm our results and to clarify if VR [5] D. Aarsland, L. Batzu, G. M. Halliday et al., “Parkinson
impairment in PD patients could represent an early cogni- disease-associated cognitive impairment,” Nature Reviews.
tive deficit. Disease Primers, vol. 7, no. 1, p. 47, 2021.
[6] C. E. Cicero, L. Raciti, R. Monastero et al., “Cardiovascular
autonomic function and MCI in Parkinson’s disease,” Parkin-
Data Availability sonism & Related Disorders, vol. 69, pp. 55–58, 2019.
[7] G. Dirnberger and M. Jahanshahi, “Executive dysfunction in
Data supporting this research article are available from the Parkinson’s disease: a review,” Journal of Neuropsychology,
corresponding author or first author on reasonable request. vol. 7, no. 2, pp. 193–224, 2013.
Behavioural Neurology 5

[8] A. Nicoletti, A. Luca, R. Baschi et al., “Incidence of mild cogni-

tive impairment and dementia in Parkinson’s disease: the Par-
kinson’s disease cognitive impairment study,” Frontiers in
Aging Neuroscience, vol. 11, p. 21, 2019.
[9] D. Natsopoulos, Z. Katsarou, A. Alevriadou, G. Grouios,
S. Bostantzopoulou, and G. Mentenopoulos, “Deductive and
inductive reasoning in Parkinson’s disease patients and nor-
mal controls: review and experimental evidence,” Cortex,
vol. 33, no. 3, pp. 463–481, 1997.
[10] R. B. Postuma and D. Berg, “The new diagnostic criteria for
Parkinson’s disease,” in International Review of Neurobiology,
vol. 132, pp. 55–78, Elsevier, 2017.
[11] G. Mostile, A. Nicoletti, C. E. Cicero et al., “Magnetic reso-
nance Parkinsonism index in progressive supranuclear palsy
and vascular Parkinsonism,” Neurological Sciences, vol. 37,
no. 4, pp. 591–595, 2016.
[12] C. L. Tomlinson, R. Stowe, S. Patel, C. Rick, R. Gray, and C. E.
Clarke, “Systematic review of levodopa dose equivalency
reporting in Parkinson’s disease,” Movement Disorders,
vol. 25, no. 15, pp. 2649–2653, 2010.
[13] I. Litvan, J. G. Goldman, A. I. Tröster et al., “Diagnostic criteria
for mild cognitive impairment in Parkinson’s disease: move-
ment disorder society task force guidelines,” Movement Disor-
ders, vol. 27, no. 3, pp. 349–356, 2012.
[14] E. N. Aiello, A. Esposito, C. Gramegna et al., “The Frontal
Assessment Battery (FAB) and its sub-scales: validation and
updated normative data in an Italian population sample,” Neu-
rological Sciences, vol. 43, no. 2, pp. 979–984, 2022.
[15] T. L. Young, A. Granic, T. Yu Chen, C. B. Haley, and J. D.
Edwards, “Everyday reasoning abilities in persons with Par-
kinson’s disease,” Movement Disorders, vol. 25, no. 16,
pp. 2756–2761, 2010.
[16] B. Kopp, N. Rösser, S. Tabeling et al., “Performance on the
Frontal Assessment Battery is sensitive to frontal lobe damage
in stroke patients,” BMC Neurology, vol. 13, no. 1, p. 179, 2013.
[17] A. Nagano-Saito, Y. Washimi, Y. Arahata et al., “Cerebral atro-
phy and its relation to cognitive impairment in Parkinson dis-
ease,” Neurology, vol. 64, no. 2, pp. 224–229, 2005.
[18] N. Ibarretxe-Bilbao, C. Junque, M. J. Marti, and E. Tolosa,
“Brain structural MRI correlates of cognitive dysfunctions in
Parkinson’s disease,” Journal of the Neurological Sciences,
vol. 310, no. 1–2, pp. 70–74, 2011.
[19] G. Santangelo, M. Siciliano, R. Pedone et al., “Normative data
for the Montreal Cognitive Assessment in an Italian popula-
tion sample,” Neurological Sciences, vol. 36, no. 4, pp. 585–
591, 2015.
[20] Z. S. Nasreddine, N. A. Phillips, V. Bédirian et al., “The Mon-
treal Cognitive Assessment, MoCA: a brief screening tool for
mild cognitive impairment,” Journal of the American Geriat-
rics Society, vol. 53, no. 4, pp. 695–699, 2005.