psiquiatria-nutricional-tapajoz-2019

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Received: 30 May 2019 Revised: 8 July 2019 Accepted: 25 August 2019
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BR I E F RE PORT
DOI: 10.1002/erv.2701
Impaired theory of mind in unaffected first‐degree relatives
of patients with anorexia nervosa
Fernanda Tapajóz1,2 | Sebastian Soneira3 | Natalia Catoira4 | Alfredo Aulicino5 |
Ricardo F. Allegri1,2,6
1CONICET‐Consejo Nacional de
Investigaciones Científicas y Técnicas,
Buenos Aires, Argentina
2Service of Cognitive Neurology,
Neuropsychology and Neuropsychiatry,
Fleni, Buenos Aires, Argentina
3Section of Eating Disorders and
Nutritional Psychiatry, Psychiatry Service,
Fleni, Buenos Aires, Argentina
4Casa Hospital San Juan de Dios (Ramos
Mejía), Buenos Aires, Argentina
5Section of Eating Disorders, Hospital
General Cosme Argerich, Buenos Aires,
Argentina
6Universidad de la Costa (CUC),
Barranquilla, Colombia
Correspondence
Fernanda Tapajóz, PhD, Service of
Cognitive Neurology, Neuropsychology
and Neuropsychiatry, Fleni, Montañeses
2325, 8th floor, Ciudad Autónoma de
Buenos Aires C1428AQK, Argentina.
Email: fetapajoz@hotmail.com
Eur Eat Disorders Rev. 2019;692 27:692-699.
Abstract
Objective: Previous studies have shown theory of mind (ToM) is affected in
patients with anorexia nervosa (AN). There has also been growing interest in
the study of endophenotypes in psychiatric disorders, since they allow better
understanding of genetic mechanisms underlying different conditions, making
them potential targets for future treatment. The goal of this study was to inves-
tigate whether ToM inefficiencies observed in patients with AN, are shared by
unaffected first‐degree relatives.
Method: Performance on two ToM tasks (Reading the Mind in the Eyes and
Faux Pas Test) were compared in 17 unaffected first‐degree relatives of AN
patients and in 17 healthy individuals matched for age and level of education.
Depression, anxiety, obsessive compulsive, and eating disorder symptoms were
also assessed and correlated with ToM and clinical/demographic variables.
Results: Significant differences between groups were observed in all ToM
tasks, with relatives of AN patients showing poorer performance. ToM assess-
ment did not correlate with any clinical or demographic variable.
Conclusions: The preliminary results of this study suggest unaffected first‐
degree relatives of AN patients display similar patterns of difficulty in ToM
as reported previously for AN patients, supporting the hypothesis that
ToM inefficiencies are a familial trait in this condition.
KEYWORDS
anorexia nervosa, neuropsychology, social cognition, theory of mind, unaffected first‐degree relatives
1 | INTRODUCTION
Anorexia nervosa (AN) is a complex psychiatric disorder
that is clinically defined by low body weight, difficulties
in engaging in behaviours that restore weight, and prob-
lems in accepting that the low weight is dangerous for
health. This results in serious physical, behavioural,
and socio‐cognitive dysfunction (American Psychiatric
Association, 2013).
wileyonlinelibrary.com/journal/
The neuropsychological profile of patients with AN is
characterised by poor set shifting and weak central coher-
ence (Lang, Treasure, & Tchanturia, 2015; Lopez,
Tchanturia, Stahl, & Treasure, 2008; Roberts, Tchanturia,
Stahl, Southgate, & Treasure, 2007; Tchanturia et al.,
2012). More recently, evidence of difficulties in the
cognitive domain of social cognition, mainly in theory of
mind (ToM) has also been found (Harrison, Sullivan,
Tchanturia, & Treasure, 2009; Harrison, Sullivan,
erv © 2019 John Wiley & Sons, Ltd and Eating Disorders Association.
https://orcid.org/0000-0003-2432-8177
https://doi.org/10.1002/erv.2701
http://wileyonlinelibrary.com/journal/erv
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Highlights
• Theory of mind (ToM) inefficiencies are
observed in first degree relatives of patients
with anorexia nervosa.
• ToM can be a familial trait of anorexia
nervosa.
• In addition to previous research in which
difficulties persisted even after recovery,
results of this study suggest ToM
inefficiencies could represent a
neuropsychological endophenotype for AN.
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Tchanturia, & Treasure, 2010; Harrison, Tchanturia,
Naumann, & Treasure, 2012; Russell, Schmidt, Doherty,
Young, & Tchanturia, 2009; Tapajóz Pereira de Sampaio,
Soneira, Aulicino, & Allegri, 2013; Tchanturia et al., 2004).
The study of ToM in AN patients is relevant since a
high incidence of problems in social interaction, such as
social–emotional isolation, social phobia, fear and avoid-
ance of intense emotions, and alexithymia (Fox, 2009;
Godart et al., 2004; Schmidt, Jiwany, & Treasure, 1993;
Tiller et al., 1997) is found in this group of individuals.
Difficulties with social–emotional functioning are
believed to play an important role in the development,
maintenance (Schmidt & Treasure, 2006; Treasure &
Schmidt, 2013), and long‐term clinical outcome of
patients with eating disorders (ED; Zipfel, Löwe, Reas,
Deter, & Herzog, 2000). ToM assessment is therefore
important in ED, in order to clarify the cognitive vari-
ables underlying the clinical features observed.
Renewed interest in endophenotypes has allowed
deeper understanding of many psychiatric disorders, of
which neurocognitive functioning has become a promis-
ing focus of investigation (Flint & Munafo, 2007;
Leboyer, 2003).
The term endophenotype refers to internal traits not
clinically appreciable which can be accessed indirectly
through neuropsychological testing, for instance. For a
marker to be considered an endophenotype, it must meet
a series of conditions (Gottesman & Gould, 2003;
Miranda, Jaramillo, Valencia, & Duque, 2003) namely
be measurable, hereditary, stable (found in patients with
and without active disease), and present in unaffected
first‐degree relatives. In adults with AN, difficulties in
executive function and in central coherence were found
both in unaffected first‐degree relatives and in recovered
patients, making them potential endophenotype
candidates (Galimberti et al., 2013; Holliday, Tchanturia,
Landau, Collier, & Treasure, 2005; Lang et al., 2015;
Lopez, Tchanturia, Stahl, & Treasure, 2009; Roberts,
Tchanturia, & Treasure, 2013; Tenconi et al., 2010;
Zucker et al., 2007).
In contrast to “cold” neurocognition (set shifting and
central coherence), there are few studies on “hot” social
cognition involving ToM as a possible endophenotype in
AN. Oldershaw, Hambrook, Tchanturia, Treasure, and
Schmidt (2010) found individuals who had recovered
from AN performed similarly to controls in ToM tasks,
suggesting these abilities could improve after recovery.
Other studies, however, found that acute and recovered
AN patients performed more poorly in ToM tasks,
indicating the inefficiencies could be trait of disease and
a possible vulnerability factor in anorexia (Harrison
et al., 2012; Harrison, Tchanturia, & Treasure, 2010). In
a more recent meta‐analysis on abnormal results in
ToM observed in eating disorders (ED), Bora and Köse
(2016) found acute AN patients presented significant
difficulties in this domain. Smaller‐sized difficulties were
observed in recovered AN patients.
Aside from being present in patients after recovery, a
cognitive marker cannot be considered an endo-
phenotype unless it is also present in unaffected
first‐degree relatives (Miranda et al., 2003). Articles
reviewed for this paper revealed only one study involv-
ing twins which explored socio‐emotional processing as
a possible endophenotype (Kanakam, Krug, Raoult,
Collier, & Treasure, 2013) in which emotion recogni-
tion, attentional bias, and emotional regulation were
investigated. Although only a pilot study and statisti-
cally underpowered, the authors did detect a trend
towards more pronounced difficulties in twins with ED
and in unaffected twin siblings,indicating family co‐
segregation of difficulties. More research will be needed
on the subject to establish firm conclusions.
A fundamental issue in the search for endophenotypes
in AN is whether poor performance on ToM tests is a
familial trait. For this reason, our objective in this prelim-
inary study was to explore theory of mind in unaffected
first‐degree relatives of AN patients. Our working hypoth-
esis was that these relatives would present inefficiencies
in ToM, similar to those previously observed in AN
patients (Harrison et al., 2009; Harrison, Sullivan, et al.,
2010; Russell et al., 2009; Tapajóz Pereira de Sampaio
et al., 2013).
2 | METHOD
2.1 | Participants
Seventeen unaffected first‐degree female relatives (eight
mothers and nine sisters) of patients with a DSM‐V diag-
nosis of AN, receiving treatment at the Cormillot Clinic
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and the Argerich Hospital in Buenos Aires, together with
17 age‐ and education‐matched healthy controls (HC)
were recruited for the study. All participants were native
Spanish speakers from Buenos Aires.
Exclusion criteria included: (a) current psychiatric
disorder and/or history of neurological, psychiatric, or
systemic diseases affecting cognitive evaluation perfor-
mance; (b) use of medication/s altering cognition; (c)
alcohol and/or drug abuse, (d) diagnosis of eating disor-
der evaluated using EDI‐II; (e) pregnancy/breastfeeding;
or (f) BMI <18.5.
Healthy controls recruited through various sources
included administrative staff from institutions involved
in the study, university colleagues, and local community
members.
2.2 | Procedure and ethical considerations
A descriptive‐analytic, cross‐sectional design was used to
assess ToM in first‐degree relatives of AN patients
(F‐AN).
Participants were first interviewed to explain the
purpose of the study, clarify any possible doubts, and sign
an informed consent, previously approved by the institu-
tional ethics committee.
Individual evaluation of each participant in a quiet
environment free from external stimuli was conducted
by the first author (a psychologist, specialising in clinical
neuropsychology) and included comprehensive neuropsy-
chological as well as clinical‐psychopathologic workup.
For the purposes of this study, only results of ToM and
clinical‐psychopathologic assessments were reported.
Validated Spanish language versions of all tests were
used.
2.3 | Measures
2.3.1 | Cognitive screening
Mini‐Mental State Examination (MMSE)
A brief 30‐point questionnaire widely used to screen for
cognitive impairment (Butman et al., 2001; Folstein,
Folstein, & McHugh, 1975).
2.3.2 | Clinical‐psychopathological
evaluation
Beck depression inventory (BDI)
A 21‐question multiple‐choice self‐reported inventory
used to assess existence and severity of depression
symptoms (Beck, Steer, & Brown, 2006; Beck, Ward,
Mendelson, Mock, & Erbaugh, 1961; Brenlla &
Rodríguez, 2006).
State‐Trait Anxiety Inventory (STAI)
A 40‐item test evaluating intensity of feelings of anxiety
which distinguishes between state of anxiety and trait
anxiety (Leibovich de Figueroa, 1991; Spielberger,
Gorsuc, & Lushene, 1982).
Obsessive‐Compulsive Inventory–Revised (OCI‐R)
An 18‐item self‐reported measure of obsessive‐compulsive
disorder (OCD) symptoms in six dimensions: checking,
washing, ordering, hoarding, obsessing, and neu-
tralizing (Foa et al., 2002; Martínez‐González, Piqueras,
& Marzo, 2011).
Eating disorder inventory‐two (EDI‐II)
A 91‐item inventory evaluating symptoms and psycholog-
ical characteristics of eating behaviour disorders (Garner,
1998; Rutsztein et al., 2006). For purposes of this study,
we report only results from three “risks” subscales
(Rutsztein, Murawski, Elizathe, & Scappatura, 2010):
drive for thinness, bulimia, body dissatisfaction, and total
score.
2.3.3 | Theory of Mind Evaluation
Reading the Mind in the Eyes–affective ToM
It consists of 36 photos of the area of the eyes of people of
both sexes, whose eyes reflect complex mental states or
emotions (Baron‐Cohen, Wheelwright, Hill, Raste, &
Plumb, 2001; Serrano, 2006a). Participants are asked to
choose from between four options, which word best
describes how the person in the photograph is feeling or
thinking. For a more detailed description see Tapajóz
et al., (2013).
“Faux Pas” Test–affective and cognitive ToM
It assesses the ability of subjects to identify situations in
which someone mistakenly says something they should
not have (“faux pas”; Baron‐Cohen, O'Riordan, Stone,
Jones, & Plaisted, 1999; Serrano, 2006b). In this study, a
shortened version (10 stories) five containing faux pas
and five control stories without a faux pas were used
(for more detailed description on administration and
scoring of this task, see Tapajóz Pereira de Sampaio
et al., 2013).
2.4 | Statistical analysis
Data were analysed using the Statistical Package for
Social Sciences (SPSS), version 19 for Windows. The
TABLE 1 Participant demographics
Unaffected
AN relatives HC
Statistic p value
(n = 17) (n = 17)
Mean (SD) Mean (SD)
Age (years) 37.5 (16.0) 38.4 (11.7) U = 131.5 .658
Years of
education
14.4 (2.2) 15.7 (2.1) U = 103.0 .160
Body Mass
Index
(Kg/m2)
22.4 (3.6) 22.9 (2.5) U = 110.0 .245
Mini Mental 29.5 (0.6) 29.6 (0.4) U = 133.0 .708
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Shapiro Wilk Test was used to assess normality of distri-
bution and Levene's test for homogeneity of variance.
Parametric assumptions were not met for demographic
or clinical variables, the Faux Pas Test and the RMET
(control and accuracy for neutral emotions), therefore
the Mann–Whitney U test was used for comparison
between groups. Parametric assumptions were met for
RME (total, accuracy for male and female eyes, and
accuracy for positive and negative emotions), so a t‐test
was used. Cohen's d was used to calculate effect size,
and Spearman's rank (rs) correlation to explore the
relationship between ToM and clinical demographic
variables in the F‐AN group. p values < .05 were consid-
ered statistically significant.
BDI 9.6 (7.3) 5.7 (5.8) U = 93.5 .127
STAI‐state 23.2 (12.4) 15.6 (9.2) U = 84.0 .063
STAI‐trait 24.4 (10.4) 21.0 (9.7) U = 103.0 .370
OCI‐R total 15.0 (8.2) 15.6 (9.8) U = 126.5 .736
EDI‐II drive for
thinness
1.8 (3.7) 1.4 (2.1) U = 133.5 .929
EDI‐II bulimia 0.0 (0.0) 0.1 (0.4) U = 128.0 .790
EDI‐II body
dissatisfaction
3.3 (3.8) 4.5 (4.6) U = 120.0 .581
EDI‐II total 34.3 (12.2) 25.0 (15.4) U = 83.5 .058
AN, anorexia nervosa; BDI, Beck Depression Inventory; EDI‐II, eating disor-
der inventory‐two; HC, healthy controls; OCI‐R, obsessive‐compulsive inven-
tory–revised; STAI, State‐Trait Anxiety Inventory
3 | RESULTS
3.1 | Demographic and clinical
characteristics
Participant demographics and clinical characteristics are
shown in Table 1.
Both groups were comparable in age, years of educa-
tion, and MMSE score. No differences were observed in
other demographic, clinical, or psychopathological
variables.
3.2 | ToM performance
ToM test results are shown in Table 2.
3.2.1 | “Reading the Mind in the Eyes”
task
F‐AN group total scores were significantly lower than
those of HC for this test (p < .01), experiencing particular
difficulty recognising emotions expressed by eyes of both
males (p < .05) and females (p < .01). In addition, poorer
performance was also observed for recognition of positive
emotions (p < .05) and neutral cognitive states (p < .05).
No differences were found in the control task.
3.2.2 | “Faux Pas Test”
F‐AN group scored significantly lower than HC on the
Faux Pas Test, both for stories (p < .05) and total score
(p < .05). No differences between groups were found in
control stories or on memory questions.
3.3 | Relations between theory of mind
and clinical‐psychopathological profile
The only statistically significant correlation observed in
the F‐AN group was betweenthe total RME score and
Mini Mental (ρ = .55, p < .05).
4 | DISCUSSION
The aim of this study was to explore whether theory of
mind inefficiencies previously observed in patients with
anorexia nervosa (Harrison et al., 2009; Harrison,
Sullivan, et al., 2010; Russell et al., 2009; Tapajóz Pereira
de Sampaio et al., 2013) were also present in unaffected
first‐degree relatives.
Our results support this hypothesis, first‐degree
relatives of patients with AN presented theory of mind
difficulties (Reading the Mind in the Eyes test and Faux
Pas test) similar to those found in patients. In the RMET,
F‐AN individuals performed more poorly than healthy
controls when discriminating between masculine and
feminine gaze, as well as on identifying positive emotions
and neutral/cognitive states. F‐AN performed less well on
TABLE 2 Performance on theory of mind tests
Unaffected AN relatives HC
Statistic p value
Effect
size
(Cohen's
d)
(n = 17) (n = 17)
Mean (SD) Mean (SD)
RME total (max = 36) 22.5 (3.5) 26.5 (3.0) t = 3.4 .002 1.22
RME control (max = 36) 34.9 (1.7) 35.1 (0.6) U = 125.5 .518 na
RME male eyes only (max = 19) 12.1 (2.0) 13.7 (1.9) t = 2.3 .026 .82
RME female eyes only (max = 17) 10.4 (2.3) 12.7 (1.7) t = 3.2 .002 1.13
RME positive emotions (max = 13) 9.1 (2.2) 10.8 (1.5) t = 2.6 .013 .90
RME negative emotions (max = 15) 8.7 (2.0) 10.0 (1.7) t = 1.89 .067 na
RME neutral/cognitive states (max = 8) 4.7 (1.2) 5.7 (1.2) U = 81.0 .029 na
Faux Pas Test (history faux pas; max = 30) 23.5 (5.9) 28.1 (2.6) U = 74.0 .014 na
Faux Pas Test (history control; max = 10) 9.6 (1.0) 9.8 (0.4) U = 135.5 .760 na
Faux Pas Test (memory; max = 20) 18.9 (1.1) 19.5 (0.8) U = 95.0 .092 na
Faux Pas Test (total; max = 40) 33.2 (6.0) 38.0 (2.7) U = 72.5 .012 na
AN, anorexia nervosa; HC, healthy controls; na, not applicable; RME, Reading the Mind in the Eyes Test
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faux pas stories and with lower total scores on the FPT. A
strength of the study was to use two measures of ToM to
evaluate the different subcomponents (affective and cog-
nitive) and to analyse possible dissociations between
these (Kalbe et al., 2007; Tager‐Flusberg & Sullivan,
2000; Völlm et al., 2006). We observed that relatives of
AN patients presented inefficiencies in both affective
and cognitive subcomponents.
Difficulties observed could not be explained by differ-
ences in demographic, clinical, or cognitive variables such
as age, years of education, BMI, or symptoms of depres-
sion, anxiety, obsessive‐compulsive disorder, or ED.
Coexistence of ToM inefficiencies between AN
patients and unaffected first‐degree relatives suggests
these could be part of a family vulnerability to the
disease, although the present study was not designed to
discriminate between genetic or environmental factors
(learning style, emotional intensity, or emotion expressed
within the family unit) that might have contributed to
symptom emergence.
Kanakam et al. (2013) also evaluated ToM in first‐
degree relatives of patients with ED and found a positive
statistical trend for inefficiencies in unaffected siblings,
suggesting difficulties co‐segregate within families.
As previously mentioned, for a cognitive marker to be
considered an endophenotype, it also must be a stable
trait present in recovered patients (Miranda et al., 2003).
In most other studies evaluating ToM in patients who
recovered from anorexia (Harrison et al., 2012; Harrison,
Tchanturia, & Treasure, 2010), difficulties remained
stable although in less severe form (Bora & Köse, 2016).
Only the study by Oldershaw et al. (2010) found improve-
ment in ToM performance after recovery. However, it is
important to note that studies on recovered patients were
cross‐sectional in design, and ToM skills were not evalu-
ated during illness. To establish whether difficulties really
persist, longitudinal investigations are needed to evaluate
the same patients both during acute phases and after
recovery.
Identifying endophenotypes found in ED is of
relevance, since they could potentially contribute to the
development of new treatments by assisting in the
construction of etiological models (Treasure, 2007).
Previous studies suggest cognitive styles such as weak
central coherence and cognitive rigidity could be
endophenotype candidates for ED (Galimberti et al.,
2013; Holliday et al., 2005; Lopez et al., 2009; Tenconi
et al., 2010), both difficulties observed in recovered
patients and in unaffected first‐degree relatives.
This study suggests that in addition to cognitive styles,
ToM should also be investigated. Finding a relevant
neuropsychological feature in both patients and family
members would contribute to a better understanding of
the social inefficiencies encountered by patients as well
as to finding possible underlying genetic mechanisms
linked to AN, but at the same time, it would further
support the importance of including family members
in treatment strategies, rehabilitation sessions, and
social–emotional training programmes. Both Cognitive
Remediation and Emotional Skills Training (Davies et al.,
2012) and the Maudsley Model of Anorexia Nervosa Treat-
ment for Adults (MANTRA; Schmidt & Treasure, 2006;
Schmidt, Wade, & Treasure, 2014) have proven effective
in treating adults. Considering that not only the patient
but also their relatives find it hard to recognise complex
emotions in others, it is important in clinical
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practice to offer family members emotional‐cognitive
psychoeducation. Learning to read emotions can be related
to the level of clarity in which emotions are expressed
within the family unit, an aspect that should be worked
on jointly with patients and their families.
Aside from being a preliminary study, this paper has
several limitations such as a small sample size. However,
differences detected between groups (with a large effect
size), suggests the study does not lack power. Further
investigations in unaffected first‐degree relatives with
larger sample sizes will be required, which could also
include patients and their families, in order to better
establish correlations between them. Another limitation
was not having controlled for autistic traits during ToM
skill assessment, considering the growing body of evi-
dence indicating a link between autism and anorexia
(Leppanen, Sedgewick, Treasure, & Tchanturia, 2018).
This issue is being addressed in a forthcoming paper.
Although IQ was not measured, it is worth emphasising
that the results reported are part of a comprehensive neu-
ropsychological evaluation, which allowed us to confirm
that no participant presented intellectual disability.
MMSE results reported were also a screen for cognitive
dysfunction.
In conclusion, more research is needed on ToM in
recovered patients, especially applying longitudinal
methods. This will allow in depth exploration of the diffi-
culties encountered in the social cognition domain and
clarify whether or not ToM inefficiencies constitute a
neuropsychological endophenotype for anorexia nervosa.
ACKNOWLEDGEMENTS
Fernanda Tapajóz is grateful to his colleagues in the Fleni
Cognitive Neurology Service. The authors thank
Cormillot Institute, Argerich Hospital, and all the partic-
ipants who took part in the study. F. T. was supported by
a CONICET post‐doc fellowship.
CONFLICT OF INTEREST
The authors declare that there is no conflict of interest
regarding the publication of this article.
ORCID
Fernanda Tapajóz https://orcid.org/0000-0003-2432-8177
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How to cite this article: Tapajóz F, Soneira S,
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