Social cognition in alcohol use disorder: A meta-analysis

Running title: Social cognition in AUD

Emre Bora1,3 MD, Nabi Zorlu2 MD

1-The Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of

Melbourne and Melbourne Health, Carlton South, VIC, Australia

2-Department of Psychiatry, Katip Celebi University, Ataturk Training and Research

Hospital, Izmir-Turkey

3-6328 Sokak, no:38/2, Yali Mahallesi, Izmir, Turkey

Corresponding author: Emre Bora

ibora@unimelb.edu.au, boremre@gmail.com

Clinical trial registration details (if applicable) : Not applicable

No funding is involved
Conflict of interest and Disclosure: No conflict of interests regarding the current
menuscript. Dr Bora and Zorlu reports no other disclosures

This article has been accepted for publication and undergone full peer review but has not
been through the copyediting, typesetting, pagination and proofreading process which may
lead to differences between this version and the Version of Record. Please cite this article as
doi: 10.1002/ADD.13486

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Abstract

Background and aims

Deficits in social cognitive abilities including emotion recognition and theory of mind (ToM)
can play a significant role in interpersonal difficulties observed in alcohol use disorder
(AUD). This meta-analysis aims to estimate mean effect sizes of deficits in social cognition
in AUD and examines the effects of demographic and clinical confounding factors on the
variability of effect sizes across studies.

Methods

A literature review was conducted on research reports published from January 1990 to
January 2016. Twenty-five studies investigating ToM and facial emotion recognition
performances of 756 individuals with AUD and 681 healthy controls were selected after
applying inclusion and exclusion criteria. Weighted effect sizes (d) were calculated for ToM,
decoding and reasoning aspects of ToM, total facial emotion recognition and recognition of
each of six basic emotions.

Results

Facial emotion recognition was significantly impaired (d=0.65, 95% confidence interval
(CI)=0.42-0.89), particularly for disgust and anger. AUD was also associated with deficits in
ToM (d=0.58, 95% CI=0.36-0.81). These deficits were evident in tasks measuring both
decoding (d=0.46, 95% CI=0.19-0.73) and reasoning (d=0.72, 95% CI=0.37-1.06) aspects of
ToM. The longer duration of alcohol misuse and more depressive symptoms were associated
with more severe deficits in recognition of facial emotions.

Conclusions

Alcohol use disorder appears to be associated with significant impairment in facial emotion
recognition and theory of mind.

Key words: Social cognition; theory of mind; emotion recognition; alcohol use disorder

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Introduction
One of the characteristics of alcohol addiction is that users’ predominant focus of life
becomes obtaining and consuming alcohol at the expense of interpersonal relationships and
responsibilities. Social impairment is one of the most detrimental features of alcohol use
disorder (AUD) (1). The negative effect of chronic alcohol use on social skills is one of the
potential important contributors to poor social functioning in AUD. Diminished social skills
in AUD might be partly related to well-documented deficits in neurocognition including
executive dysfunction (2). However, deficits in social cognition might be even more relevant
for interpersonal functioning in AUD. There are a number of potential explanations for
observed social cognitive deficits in AUD. Chronic self-administration of drugs including
alcohol can lead to neuroplastic changes in cortical and striatal structures that have a role in
motivation, social cognition and affective regulation (3-4). Long-term alcohol use is also
associated with neurotoxic effects on the integrity of a number of brain regions including
medial prefrontal lobe and disrupted connectivity (5-8). Alternatively, pre-existing social
cognitive deficits might be a risk factor for AUD (9-10).

Previous studies have shown that alexithymia is significantly associated with AUD (11).
Individuals with AUD might perceive themselves as less empathetic (12). However,
relatively few studies have investigated social cognition in AUD with objective paradigms.
The most commonly used objective measure in social cognition research is recognition of
emotions in facial stimuli. Available evidence suggests that individuals with AUD
underperform healthy controls in recognition of facial emotions (13-16). However, it is not
clear if recognition of particular emotions is selectively impaired. One recent meta-analysis
found a significant deficit in total emotion recognition score but did not investigate the
deficits in the individual emotions (14).
Recently, a number of studies have investigated theory of mind (ToM) which is the ability to
attribute mental states (intentions, feelings, beliefs) to others and explain and predict others’
behaviour based on this information. ToM is a more complex aspect of social cognition and
can be particularly relevant for deficits in social functioning in AUD as it has shown to be
strongly associated with social impairment in a number of psychiatric conditions (17-18).
There has been contradicting findings regarding ToM abilities in AUD. While some authors
have found no difference between AUD and healthy controls for ToM abilities (19-20),
others suggested that AUD is associated with ToM impairment (21-22). ToM is not an
entirely homogeneous concept. Some authors have suggested a difference between tasks

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requiring decoding other’s mental state based on perceptual information such as facial
expressions (ToM-Decoding) and tasks requiring inferring other’s intentions and beliefs
(ToM-Reasoning) (23-24). Functional imaging studies have supported this notion by partial
but considerable activation differences in brain regions depending on the task used (25). It is
not yet clear if one of these aspects of ToM is relatively more impaired in AUD. A meta-
analysis of ToM findings in AUD to date can estimate the severity of these deficits and can
help to understand the heterogeneity by investigating the effects of the potential confounding
factors.
The main goal of the current meta-analysis was to estimate mean effect sizes for deficits in
facial emotion recognition and ToM abilities in AUD in comparison to healthy controls.
Another goal was to conduct analyses to estimate the effect of study-level clinical and
demographic variables on between-group differences between AUD and healthy controls.

Methods
Study selection
We followed PRISMA guidelines in conducting this meta-analysis (26). A literature search
was conducted using the databases Pubmed, PsycINFO, ProQuest and Scopus to identify the
relevant studies (January 1990 to January 2016) using the combination of keywords as
follows: Theory of mind, social cognition, alcohol. Reference lists of published reports were
also reviewed for additional studies and Google Scholar was used to retrieve unpublished
material including conference papers and theses. Inclusion criteria were studies that: (1)
Compared ToM or facial emotion recognition (accuracy in labeling based on 4 or more basic
emotions) performances of individuals with AUD and healthy controls; (2) reported sufficient
data to calculate the effect size and standard error of the between-group differences for
accuracy score of ToM and facial emotion recognition measures. We were not able to include
emotion recognition tasks that do not use facial stimuli (i.e. vocal, music) as very few studies
have used these paradigms. We included facial emotion recognition tasks in which intensity
of stimuli for each basic emotion varied across trials. However, studies that assessed facial
emotion recognition with morphed images of two different basic emotions were excluded.
MRI and electrophysiology studies that included facial emotion recognition paradigms were
not included. We excluded studies investigating social cognition in AUD samples with the
main diagnosis of opiate addiction or central nervous system diseases such as Korsakoff’s
syndrome. We contacted 2 authors for additional information but we were not able to receive
the necessary information to include these papers in the meta-analysis.

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Among 129 reports, non-relevant studies (n=68) were excluded based on information on their
abstracts and titles. The full texts of rest of the reports (n=61) were assessed for inclusion
criteria and 32 of these studies met our inclusion criteria. However, further seven of these 32
studies were excluded (see the Figure 1s as a supplementary file for the flow chart of the
study selection process and reasons for exclusion). Final selection included 25 studies
involving 756 (70.5 % males) individuals with AUD and 681 (70.0 % males) healthy controls
(Table 1)(17-20, 27-47). Fourteen of the studies excluded individuals with co-morbid drug
addiction, two studies have included some individuals with drug addiction, others were not
clear if they excluded such patients (no mention or a general statement such as current axis I
disorders excluded).
Social cognition measures
Several different ToM tasks are utilized across studies, most commonly the reading the mind
from the eyes (RMET) (48) and it is the only measure for mental state decoding aspect of
ToM (ToM-decoding) included in this meta-analysis. In RMET, individuals are instructed to
look at a series of photographs of just the eye region of the face, and picking which of four
words best describe what the person in the photo is thinking or feeling. Studies also include a
number of measures of mental state reasoning aspect of ToM (ToM-Reasoning). The most
commonly used measure for ToM-reasoning is the faux pas recognition (the task involves
recognizing faux pas in series of short stories) task (49). Other tasks include Happe's strange
stories task (assessing comprehension of mental states of characters in a story) and different
false belief tasks (50). Different sets (Mostly from Ekman) of pictures for facial stimuli are
used (51). Some studies include several different scores for facial emotion recognition but we
only included accuracy scores for labeling of six basic (anger, happiness, disgust, fear,
surprised, sad) emotions (and total emotion score).

Statistical analyses
For studies that reported more than one ToM task, a single effect size for total ToM for each
study was calculated by averaging multiple effect sizes within the study. A meta-analysis for
ToM across studies was conducted using a single averaged effect size (total ToM score)
from each study. In addition to meta-analysis for ToM measure, individual tasks analysis for
the RMET was also possible. Other than total ToM score and RMET (ToM-decoding), we
also had calculated effect sizes for mental state reasoning (ToM-reasoning). For the facial
emotion recognition, scores for total emotion, anger, disgust, fear, happiness, sadness and
surprise were calculated. The effect sizes for between-group differences for age and duration

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of education were also calculated to explore the level of matching for demographical
variables. The effect size for between-group difference for depression rating scores was also
calculated as depressive symptoms are common in AUD.

Meta-analyses were performed using packages in the R environment (OpenMetaAnalyst,

Metafor) (52-53). Effect sizes were weighted using the inverse variance method. A random
effects model (DerSimonian–Laird estimate) was used. The Q and I2 tests were used to assess
the homogeneity of the distribution of weighted effect sizes. Tau-squared (τ2), an estimate of
between-study variance, was used as a measure of heterogeneity in the random effects model.
Other than inspection of the funnel plot, Egger's test was used to assess publication bias.
Meta-regression analyses were conducted for age (effect size for between-group difference),
gender (ratio of males in AUD vs. controls), education, the duration of abuse, daily alcohol
use, the mean duration of abstinence and depressive symptoms (effect size for between-group
difference). Meta-regression analyses performed with a random-effects model were
conducted using the restricted-information maximum likelihood method with a significance
level set at p<0.05. We also conducted a subgroup analysis to investigate the effect of
abstinence on social cognitive deficits in AUD. Studies were categorized into two subgroups
including samples that were recently detoxified (AUD-R) (less than 8 weeks) and had a
longer period of abstinence (8 weeks or more) (AUD-A). Qbet test was used to statistically
compare the severity of social cognitive deficits in AUD-R and AUD-A.
--------------------Figure-1: Forest plot for meta-analysis of facial emotion recognition in
AUD----------------------------------(Approximately here)

Results
There were no significant between-group differences for age (d=0.10, CI=-0.01-0.20, Z=1.8,
p=0.06) and duration of education (d=0.14, CI=-0.03-0.31, Z=1.6, p=0.11). AUD was
associated with significantly more subclinical/mild depressive symptoms compared to
healthy controls (d=0.95, CI=0.66-1.25, Z=6.4, p<0.001).

Facial emotion recognition

Facial emotion recognition was significantly impaired in AUD (d=0.65) (Figure-1). In the
meta-analysis of individual emotions, recognition of disgust (d=0.62) and anger (d=0.47)
were relatively more impaired than other basic emotions. The effect sizes for deficits in
recognizing other emotions were modest (d=0.19-0.33) and group difference between AUD

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and controls was not significant for recognition of happiness. The distribution of effect sizes
was significantly heterogeneous for the total emotion, disgust and fear but not for other 4
basic emotions. There was no evidence of publication bias. There was no significant
difference in the severity of impairment facial emotion recognition between AUD-R and
AUD-A (d= 0.73 vs 0.52, Qbet =1.59, p=0.21).

ToM
ToM was significantly impaired in AUD (d=0.58) (Figure-2). Individuals with AUD were
impaired in both ToM-decoding (RMET) (d=0.46) and ToM-reasoning (d=0.72) tasks. The
distribution of effect sizes was significantly but modestly heterogeneous for ToM and ToM-
reasoning.There was no evidence of publication bias for ToM variables.
There was no significant difference in the severity of ToM impairment between AUD-R and
AUD-A (d= 0.57 vs 0.60, Qbet =0.03, p=0.86).
Meta-regression analyses
In meta-regression analyses, a higher ratio of males (AUD vs HC) was associated with more
severe ToM deficit (Z=2.05, p=0.04). Longer duration of abuse (Z=2.05, p=0.04), a larger
amount of daily use (Z=2.87 p=0.04) and more depressive symptoms (Z=2.07, p=0.04) were
associated with more severe deficits in recognition of facial emotions in AUD. There were no
significant relationships between other variables (age, daily consumption, education) and
social cognitive impairment in AUD.
--------------------Figure-2: Forest plot for meta-analysis of ToM in AUD--------------------------
--------(Approximately here)

Discussion
The current meta-analysis investigated facial emotion recognition and ToM in AUD in
comparison to controls. Our findings suggested that both aspects of social cognition were
impaired in AUD. Effect sizes for deficits in facial emotion recognition were larger in studies
that included individuals with AUD who had a longer duration of alcohol abuse and more
pronounced depressive symptoms.

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The deficits in facial emotion recognition and ToM were evident not only in studies that
included recently detoxified individuals but also evident in studies that included participants
who were abstinent for a longer period of time. While available evidence suggests that acute
use of high dose of alcohol has a negative effect on facial emotion recognition and ToM
(54), it is likely that deficits observed in recovering and abstinent alcoholics are related to
long-term effects or susceptibility factors of alcohol use. Abnormalities in neural networks
involved in emotional and perceptual processing seem to be associated with social cognition
deficits in AUD (55-58). The severity of overall deficit in facial emotion recognition in AUD
was comparable to the findings of Castellano et al (14). As an original contribution, the
current meta-analysis has also estimated mean weighted effect sizes of individual emotions.
The deficits in social cognition were relatively severe for ToM-Reasoning and recognition of
disgust and anger. Medial and dorsal frontal regions and its connection with subcortical areas,
inferior frontal cortex and insula are critical for reasoning about others mental state and
recognition of disgust and anger (25, 59-60). These findings are in accordance with brain
imaging findings suggesting significant structural and connectivity changes in these regions
in AUD (5-8). The severity of deficits in RMET (ToM-decoding) and fear recognition, both
of which require a significant contribution of the amygdala (59, 61), were also significant in
AUD. Difficulties in recognizing others’ mental state and emotional expressions such as
anger and disgust can significantly contribute to interpersonal challenges of individuals with
AUD, even in abstinence. The potential benefits of interventions targeting social cognitive
deficits in AUD remain to be investigated.

Another important consideration is the origin of neuroanatomical abnormalities leading to

persisting social cognitive deficits in AUD. In our meta-analysis, we found a significantly
larger effect size for the deficit in emotion recognition in studies that included individuals
with longer duration (and higher amount) of alcohol abuse. Toxic effects of alcohol on
neuronal integrity can potentially explain more severe deficits in emotion recognition in
studies with a longer mean duration of alcohol abuse. However, it is important to investigate
the potential relationship between duration of alcohol abuse and emotion recognition deficits
within individual participant level in studies with large sample sizes. It is also important to
note that preliminary evidence suggests that social cognitive deficits might be also evident at
high-risk individuals (9-10, 62). In the absence of longitudinal data, currently, it is not
possible to determine the specific contributions of alcohol-related-toxicity and susceptibility
factors on social cognitive deficits in AUD.

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Co-morbidity is another important confounder that can contribute to observed social
cognitive deficits in AUD. Generally, the studies included has excluded severe psychiatric
disorders such as psychosis and severe cognitive impairment but most of them had no give
details about important co-morbidities such as attention-deficit/hyperactivity disorder
(ADHD) and personality disorders including antisocial personality disorder (ASPD). Both of
these conditions have been associated with social cognitive deficits (63-64). The level of co-
morbidity of ADHD and ASPD with AUD can also contribute to the heterogeneity for the
findings for recognition of fearful faces in AUD as both of these conditions are associated
with relatively specific deficits in the processing of fearful stimuli (63-64). Even in the
absence of clear-cut diagnosis, personality features related to these co-morbidities such as
trait-impulsivity can play a role in the current findings as it was reported that having high
scores in Barratt impulsivity scale among individuals with AUD is associated with more
severe social cognitive deficits (33). Acute depressive symptoms are also known to be
associated with medium-sized deficits in ToM and very modest impairment in emotion
recognition (65-66). Our meta-regression analysis suggested a study-level relationship
between mild depressive symptoms and facial emotion recognition deficits in AUD. These
findings suggest that depressive symptoms can potentially contribute but cannot explain these
deficits in AUD. However, most of the available studies have not investigated the
relationship between depressive symptoms and social cognitive deficits in individual level.
Therefore, investigation of the within-individual level relationship between depressive
symptoms and social cognitive deficits in studies with large sample sizes are warranted. Co-
existing neurocognitive deficits, particularly executive dysfunction can also contribute to
poor performance in social cognitive tasks in AUD. We were not able to meta-analytically
explore the effects of executive dysfunction on social cognitive impairment in AUD due to
lack of sufficient data. There is a need for more studies relationship between social
cognitive deficits and co-morbidity in AUD. It is also important to note that co-morbidity is
also relevant for the notion of impairment in social cognition as a risk factor for AUD as most
of these conditions are susceptibility factors for developing AUD.

There are several limitations of the current meta-analysis. The most important limitation is
the cross-sectional nature of available evidence. No sufficient information regarding a
number of variables which can have an effect on observed findings (i.e subtypes of
alcoholism, cumulative alcohol use) were available in the majority of the studies included in

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the current meta-analysis. The relationship between social cognition and functional
impairment, depression and other co-morbid conditions in AUD has been rarely investigated.

As a conclusion, AUD is associated with significant deficits in facial emotion recognition and
ToM. Follow-up studies in at-risk and early years of addiction can help to distinguish relative
contributions of susceptibility factors and toxic effects of long-term alcohol use on social
cognitive abilities. Behavioral implications of social cognitive deficits and their effects on
functional impairment in AUD should be clarified further. Interventions targeting ToM and
facial emotion recognition deficits (i.e social cognitive training) can be potentially helpful to
improve the quality of life of individuals with AUD.

Acknowledgment: None
Funding: No funding is involved in preparation of the manuscript.

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Table-1 Studies included in the meta-analysis of social cognition in AUD
Study Sample Age Social Characteristics Cognitive Other Outcome
Cognition assessment Substance
abuse
Acharya& 23 39.4 Facial emotion Abs:3 weeks No mention Impaired
Dolan, AUD anger,
2012 26 HC sadness
(27)
Amenta 22 42.3 Faux pas Abs:2 weeks Premorbid IQ Excluded No difference
et al 2013 AUD
(19) 22 HC
Beaunieux 20 40.3 Faux pas Abs:2 weeks EF:TMT B, No mention ToM
et al 2011 AUD False belief Stroop, impaired
(28) 20 HC fluency,
Digit span
Bosco et al 22 40.6 Th.o.m.a.s Abs:46 weeks Excluded Impaired
2014 (29) AUD Strange stories Duration=13.5 y ToM in
22 HC Th.o.m.a.s
Carmona- 31 52.1 Facial emotion Abs:11 weeks Excluded Disgust, fear
Perrara et AUD Duration=26.5 y impaired
al 34 HC
2014 (30)
Dethier et 41 44.3 Facial emotion Abs:5.5 weeks BFRT Excluded No difference
al 2014 AUD
(31) 20 HC
Dursun 51 45.5 Facial emotion Abs: 2 weeks No mention Disgust
2007 (32) AUD (ASPD impaired
50 HC excluded)
Ersan 2014 29 46.8 RMET Abs:19 months EF:WCST, No mention ToM
(33) AUD digit impaired
30 HC Span, fluency,
Stroop, TMT
B
Frigerio 23 46.7 Facial emotion Outpatients No mention Impaired
et al 2002 AUD detoxification emotion
(34) 23 HC Not intoxicated recognition
Gizewski et 12 37.0 RMET Abs:1.5 year Premorbid IQ Many use Impaired in
al 2013 AUD Duration=11.4y other ToM
(35) 12 HC substance
Kornreich 50 43.7 Facial emotion Abs: 3 weeks No mention Anger, sad,
et al 2001 AUD (25) Disgust
(36, 41) 25 HC and >8 weeks impaired
(25)
Kornreich 25 46.3 RMET Recently Premorbid IQ Some use of No difference
et al 2011 AUD detoxified other
(37) 25 HC Abs: 3 weeks substances
inpatients
Kornreich 25 43.5 Facial emotion Abs: 3 weeks Excluded Fear impaired
et al 2012 AUD
(38) 25 HC
Matyassy 30 37.6 RMET Abs>6 months IQ Current DSM No difference
et al 2006 AUD axis I
(20) 30 HC diagnosis
excluded
Maurage 24 48.6 RMET Recently Premorbid IQ Excluded ToM
et al 2011 AUD detoxified impaired
(39) 24 HC Abs: 2 weeks
inpatients
Maurage 34 48.9 Video task Recently EF:Matrices Excluded ToM

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et al 2015 AUD -false belief detoxified impaired
(21) 34 HC Abs: 3.5 weeks
inpatients
Nandrino 50 45 RMET Recently No mention Impaired in
et al 2014 AUD V-SIR detoxified RMET
(40) 30 HC Abs>3 weeks
Quaglino et 26 44 Facial emotion Abs=2 weeks EF:Digit span, Excluded Impaired
al 2015 AUD card sorting, disgust
(42) 26 C TMT B,
matrices
Sprah et al33 45 Facial emotion Abs=8 weeks No mention No difference
2008 (43) AUD Ekman Duration=13.7
36 HC
Thoma et 20 47.4 RMET Recently IQ, Excluded ToM
al 2013 AUD Faux pas detoxified EF:TMT B, impaired
(22) 20 HC LNS
Trick et 29 40.4 Facial emotion Unclear, mixture IED No mention Impaired
al 2014 AUD of inpatients/ Premorbid IQ
(44) 31 HC outpatients
Uekermann 30 42.6 Facial emotion Abs=8 weeks IQ Excluded No differece
et al 2005 AUD Duration=6.2 y
(45) 28 HC
Uekermann 29 41.8 Humour and Abs:11 weeks IQ, Excluded ToM
et al 2006 AUD mentalisation EF:LNS, impaired
(46) 29 HC task TMT B,
Stroop
Valmas et 77AUD 51.8 Facial emotion Abs:6.6 year IQ, memory Excluded No difference
al 2014(47) 59 HC Duration:15.5
AUD=Alcohol use disorder, HC=Healthy controls, Abs=Duration of abstinence, RMET=Reading the mind from
the eyes test,
V-SIR=Versailles-Situational Intention- Reading, Th.o.m.a.s=The theory of mind asssessment scale,
EF=Executive functions,
LNS=Letter number sequencing, TMT=Trail making test, ASPD=Antisocial personality disorder

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Table-2 mean weighted effect sizes for face emotion recognition between AUD and controls
Test Sample AUD HC D 95 % CI Z P Q-test p τ2 Bias
Emotions-total 12 410 352 0.65 0.42-0.89 5.11 <0.001 0.004 0.10 0.08
Anger 10 291 276 0.47 0.30-0.63 5.51 <0.001 0.80 0 0.09
Disgust 9 266 251 0.62 0.29-0.97 3.52 0.003 <0.001 0.20 0.47
Fear 9 268 253 0.30 0.02-0.57 2.11 0.04 0.001 0.10 0.33
Sad 9 262 245 0.33 0.16-0.51 3.75 <0.001 0.89 0 0.41
Happy 9 262 245 0.19 -0.02-0.40 1.80 0.07 0.17 0.03 0.13
Surprise 4 138 146 0.27 0.03-0.51 2.24 0.02 0.85 0 0.83
ToM 12 317 298 0.58 0.36-0.81 5.0 <0.001 0.03 0.08 0.40
-RMET 7 190 171 0.46 0.19-0.73 3.35 <0.001 0.14 0.05 0.66
-ToM-Reason 7 197 177 0.72 0.37-1.06 4.09 <0.001 0.02 0.13 0.16
D=Effect size of between-group difference, Bias= p value of the Egger’s test,, HC=Healthy controls, D=Cohen
D

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Figure-1: Forest plot for meta-analysis of facial emotion recognition in AUD

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Figure-2: Forest plot for meta-analysis of ToM in AUD

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