Research paperAutism spectrum disorder traits are associated with empathic abilities in adults with anorexia nervosa
Introduction
Contemporary models of eating disorders (EDs) such as anorexia nervosa (AN) suggest social and emotional difficulties are key factors in the development and maintenance of the disorder (Treasure and Schmidt, 2013). During the illness, a variety of social difficulties are seen, including social anxiety (Kerr-Gaffney et al., 2018), poorer social skills (Rhind et al., 2014; Winecoff et al., 2015), and less social support (Tiller et al., 1997). Given that interpersonal problems are associated with more severe ED psychopathology (Illing et al., 2010; Tasca et al., 2011) and poorer outcomes (Franko et al., 2013; Gillberg et al., 1994; Jones et al., 2015; Zipfel et al., 2000), it is important to understand possible underlying mechanisms. One area that has received considerable attention is emotion recognition, an aspect of theory of mind (ToM). Those with AN show difficulties in recognising emotions and inferring the mental states of others, compared to healthy controls (HCs) (Bora and Kose, 2016). Individuals with AN may also have difficulties in other aspects of ToM, such as understanding social interactions and implicit social attribution, however research in this area is lacking (Leppanen et al., 2018).
The majority of emotion recognition studies in AN have used static images restricted to the face or eye-region only (Leppanen et al., 2018). Consequently, much of the information that is inherent in everyday social interactions, such as tone of voice, body language, and context is missing from such stimuli. Research has therefore investigated emotion recognition using different modalities of nonverbal communication in order to better understand the mechanisms that may underlie social difficulties in AN. For example, a few studies have examined emotion recognition from body movements or voice only. Individuals with AN were less accurate at recognising sadness but better at recognising anger conveyed through body movements compared to weight-restored AN and HCs (Lang et al., 2015; Zucker et al., 2013). However group differences became non-significant after controlling for BMI in one study (Zucker et al., 2013). AN were also less accurate than HCs at recognising emotions conveyed through voice (Kucharska-Pietura et al., 2004; Oldershaw et al., 2010). Again, group differences were not significant in one study when covariates (age, education, depression) were controlled for. Finally, a few studies have examined perception of nonverbal behaviour more holistically, using paradigms that include facial expression, posture, and vocal prosody together. For example, Gramaglia et al. (2016) used the Awareness of Social Inference Test (TASIT; McDonald et al., 2002), finding no significant differences between individuals with AN and HCs in identifying emotional states from video clips. However, the clips involved speech, therefore the task cannot be considered a pure measure of nonverbal communication only. Thus, the limited research available suggests there may be differences in perception of nonverbal communication in those with AN, however further exploration of the impact of various clinical factors, such as anxiety, depression, and BMI is required.
Relatedly, there is some evidence to suggest there are differences in empathy in AN. Empathy is considered a key component of prosocial behaviour and social cognition, as it allows us to make sense of and respond appropriately to others’ behaviour (Decety et al., 2016; Eisenberg and Miller, 1987). It comprises two major facets: cognitive and affective empathy. While cognitive empathy refers to the ability to recognise and understand the mental states of others (overlapping with the concept of ToM); affective empathy is the ability to share the feelings of others, without any direct emotional stimulation to oneself (Blair, 2005). Based on longitudinal research in a community sample, Gillberg and colleagues reported on a subgroup of participants with AN with “empathy disorders.” This group had severe problems in social understanding and communication, consistent with a diagnosis of autism spectrum disorder (ASD) (Gillberg et al., 1994). Poorer outcomes in terms of recovery and psychosocial functioning were found in this group (Anckarsäter et al., 2012; Wentz et al., 2009). More recently, several studies have used self-report measures to investigate empathy in AN. A meta-analysis of these studies reported that while overall empathy and affective empathy did not differ between AN and HC, those with AN had significantly lower cognitive empathy scores (Kerr-Gaffney et al., 2019). However, self-reported measures of empathy are limited in that they measure how empathetic individuals perceive themselves to be, rather than providing an objective measure of performance.
In those with EDs, only two studies have used a performance-based or “online” measure of empathy. Both studies found no significant differences between ED and HC groups in empathic ratings to videos or in an empathy for pain paradigm (Cardi et al., 2015; Brewer et al., 2019). However, the latter study demonstrated that high levels of alexithymia were associated with increased empathic personal distress (Brewer et al., 2019). These studies both used mixed ED samples (AN and BN), limiting the generalisability of the results for either of the two disorders, and only affective empathy was assessed. Importantly, the study by Brewer et al. (2019) demonstrates that comorbid traits such as alexithymia may explain differences in emotion processing, rather than the ED itself. Indeed, other studies in EDs have shown that alexithymia rather than ED diagnosis predicts emotion recognition abilities (Brewer et al., 2015). Thus, it is possible that the mixed results in emotion processing studies in EDs are due to samples differing in their levels of alexithymia, such that when alexithymia is particularly high in the ED group (or low in the HC group) a group difference is found.
Several other comorbid traits may influence socio-emotional cognition in AN in this way. For example, between 4 and 50% of individuals with AN show high ASD traits – scoring above clinical thresholds on diagnostic interviews for ASD (Anckarsäter et al., 2012; Vagni et al., 2016; Westwood et al., 2018, 2017). Individuals with ASD show difficulties in ToM (Happé, 1994; Kleinman et al., 2001), emotion recognition (Bal et al., 2010; Harms et al., 2010; Hubert et al., 2007), empathy (Baron-Cohen and Wheelwright, 2004; Kok et al., 2016), and social attention (Chita-Tegmark, 2016). Further, ASD traits in the general population are associated with more difficulties in these areas (Blain et al., 2017; Halliday et al., 2014; Luo et al., 2017; Zhao et al., 2018). Therefore, it is possible that high levels of ASD traits co-occur with socio-emotional processing difficulties in a proportion of those with AN. Although a few studies have found associations between high ASD traits and more severe socio-emotional difficulties, such as alexithymia (Westwood et al., 2017), social anhedonia (Adamson et al., 2018), and flattened facial affect (Lang et al., 2016), research exploring the effect of ASD traits on social cognition performance in AN is lacking. Anckarsäter et al. (2012) assessed ToM performance using the Happe cartoon task, comparing those with AN who also met criteria for ASD (AN+ASD) to those who did not (AN-ASD), as well as HCs. HCs were significantly more accurate on the mental cartoons task than AN+ASD, whereas performance in the AN-ASD group did not significantly differ from either of the other two groups, lying in the middle.
The aim of this experimental study was to examine cognitive and affective empathy and perception of nonverbal communication in AN, recovered AN (REC), and HCs. A secondary aim was to explore potential relationships between comorbid psychopathological traits and performance on social cognition tasks. As well as including measures of the aforementioned ASD traits and alexithymia, we included depression, anxiety, and social anxiety, due to their high co-occurrence with AN (Kerr-Gaffney et al., 2018; Pollice et al., 1997; Swinbourne and Touyz, 2007) and potential effects on social cognition (Attwood et al., 2017; Bourke et al., 2010; Demenescu et al., 2010; Hezel and McNally, 2014; Schreiter et al., 2013; Washburn et al., 2016).
Based on previous literature documenting difficulties in self-reported cognitive empathy (Kerr-Gaffney et al., 2019), we hypothesised that individuals with AN would show poorer cognitive empathy performance compared to HCs, but no differences in affective empathy. We expected an intermediate cognitive empathy profile in REC (scores lying between that of AN and HC). Regarding perception of nonverbal communication, we hypothesised that AN would show lower overall performance compared to HCs. We did not make any prediction on the specific modalities affected, due to a lack of research in this area.
Section snippets
Participants
Ethical approval was obtained from the National Health Service Research Ethics Committee (Camberwell St Giles, 17/LO/1960). All participants were required to be between 18 and 55 years old and fluent in English. Exclusion criteria were a history of brain trauma or learning disability. HC participants were recruited through a King's College London email circular and posters around campuses. Before taking part, HC participants were screened using the Structured Clinical Interview for DSM-5
Materials
The Wechsler Abbreviated Scale of Intelligence - Second Edition (WASI-II; Wechsler, 2011) measures verbal intelligence and perceptual reasoning, as well as full-scale IQ. The two subtest version was used (vocabulary and matrix reasoning).
The Eating Disorder Examination Questionnaire (EDE-Q; Fairburn and Beglin, 1994) measures severity of ED psychopathology. Global scores are calculated by averaging responses across items, with higher scores indicating more severe symptoms (max 6). HCs with a
Demographic information
One hundred and fifty-three participants were recruited. Out of 51 HCs, 5 were excluded based on their EDE-Q scores, and 1 REC participant was excluded due to BMI >27. Thus, 46 HCs, 51 AN and 50 REC participants were included in analyses. Demographic information is presented in Table 1. Groups were of similar age, gender, and IQ. As expected, AN had a significantly lower BMI than both REC and HC (both p<.001). Age at diagnosis was significantly older in individuals with AN compared to REC, and
Discussion
The primary aim of the current study was to compare performance across socio-emotional cognition tasks in individuals with AN, recovered AN, and HCs. To our knowledge, this is the first study to use a performance-based measure of cognitive and affective empathy in AN. Contrary to our hypothesis, there were no differences in cognitive empathy across groups. Instead, those with AN showed significantly lower affective empathy performance when stimuli were positively valanced, compared to HC.
Limitations
A limitation of the current study is the cross-sectional design. It is possible that differences in social-cognitive functioning or psychological resources contributed to the recovery of the REC group. Future research would benefit from following the same group of individuals with AN before and after recovery. Further, our study only examined a limited range of socio-emotional skills. Future studies could examine associations between comorbid psychopathology and other aspects of socio-emotional
Conclusions
Our data show that the presence of AN alone does not lead to lower empathy performance overall, with the exception of positive affective empathy. Rather, those with a previous or current diagnosis of AN plus high ASD symptoms demonstrated lower cognitive and affective empathy compared to those with low ASD symptoms. Individuals with AN and high ASD traits may require different treatment approaches or adaptations. For example, previous research has shown that patients with ASD and AN and their
Author statement
Contributors: JK, AH, and KT contributed to the study design. JK recruited and tested participants, analysed the data, and wrote the manuscript. AH and KT proofread the manuscript. KT led the research group within which the research was conducted.
Funding: JK is supported by the Economic and Social Research Council (ESRC). The research was supported by the Psychiatry Research Trust, Swiss Anorexia Nervosa Foundation (ref: 58–16), and MRC Child and Young Adult Mental Health—Underpinning the
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We would like to thank the participants who took part in the research for their time and the clinicians for their support in recruitment.
References (84)
- et al.
The twenty-item toronto alexithymia scale—I. item selection and cross-validation of the factor structure. J. psychosom
Res
(1994) - et al.
Impairment of social function in young females with recent-onset anorexia nervosa and recovered individuals
J. Adolesc. Heal.
(2017) - et al.
Subtle cues missed: impaired perception of emotion from gait in relation to schizotypy and autism spectrum traits
Schizophr. Res.
(2017) Responding to the emotions of others: dissociating forms of empathy through the study of typical and psychiatric populations
Conscious. Cogn.
(2005)- et al.
Affective empathy in schizophrenia: a meta-analysis
Schizophr. Res.
(2016) - et al.
A systematic review and meta-analysis of “Systems for social processes” in eating disorders
Neurosci. Biobehav. Rev.
(2014) Social attention in ASD: a review and meta-analysis of eye-tracking studies
Res. Dev. Disabil.
(2016)- et al.
Generalized deficit in all core components of empathy in schizophrenia
Schizophr. Res.
(2009) - et al.
Anorexia nervosa outcome: six-Year controlled longitudinal study of 51 cases including a population cohort
J. Am. Acad. Child Adolesc. Psychiatry
(1994) - et al.
Alexithymia, empathy, emotion identification and social inference in anorexia nervosa: a case-control study
Eat Behav
(2016)
Theory of mind impairments in social anxiety disorder
Behav. Ther.
Diminished facial emotion expression and associated clinical characteristics in anorexia nervosa
Psychiatry Res
Differences in the theory of mind profiles of patients with anorexia nervosa and individuals on the autism spectrum: a meta-analytic review
Neurosci. Biobehav. Rev.
Association between autistic traits and emotion adaptation to partially occluded faces
Vision Res
Intelligence and interpersonal sensitivity: a meta-analysis
Intelligence
Empathy in adults with clinical or subclinical depressive symptoms
J. Affect. Disord.
Testing a maintenance model for eating disorders in a sample seeking treatment at a tertiary care center: a structural equation modeling approach
Compr. Psychiatry
Using the ritvo autism asperger diagnostic scale-revised (RAADS-R) disentangle the heterogeneity of autistic traits in an italian eating disorder population
Res. Autism Spectr. Disord.
Theory of mind in social anxiety disorder, depression, and comorbid conditions
J. Anxiety Disord.
Long-term prognosis in anorexia nervosa: lessons from a 21-year follow-up study
Lancet
Effectiveness of emotional skills training for patients with anorexia nervosa with autistic symptoms in group and individual format
Eur. Eat. Disord. Rev.
The sociocommunicative deficit subgroup in anorexia nervosa: autism spectrum disorders and neurocognition in a community-based, longitudinal study
Psychol. Med.
State anxiety and emotional face recognition in healthy volunteers
R. Soc. open Sci.
Emotion recognition in children with autism spectrum disorders: relations to eye gaze and autonomic state
J. Autism Dev. Disord.
Introducing the minipons: a short multichannel version of the profile of nonverbal sensitivity (PONS)
J. Nonverbal Behav.
The empathy quotient: an investigation of adults with asperger syndrome or high functioning autism, and normal sex differences
J. Autism Dev. Disord.
Meta-analysis of theory of mind in anorexia nervosa and bulimia nervosa: a specific impairment of cognitive perspective taking in anorexia nervosa?
Int. J. Eat. Disord
Processing of facial emotion expression in major depression: a review
Aust. New Zeal. J. Psychiatry
Emotion recognition deficits in eating disorders are explained by co-occurring alexithymia
R. Soc. Open Sci.
Alexithymia explains increased empathic personal distress in individuals with and without eating disorders
Q. J. Exp. Psychol.
Emotional processing, recognition, empathy and evoked facial expression in eating disorders: an experimental study to map deficits in social cognition
PLoS ONE
Emotional processing of infants displays in eating disorders
PLoS ONE
Social Responsiveness Scale–Second Edition (SRS-2). Torrance
Empathy as a driver of prosocial behaviour: highly conserved neurobehavioural mechanisms across species
Philos. Trans. R. Soc. B Biol. Sci
Impaired attribution of emotion to facial expressions in anxiety and major depression
PLoS ONE
From face to face: the contribution of facial mimicry to cognitive and emotional empathy
Cogn. Emot.
Dissociation of cognitive and emotional empathy in adults with asperger syndrome using the multifaceted empathy test (MET)
J. Autism Dev. Disord.
The relation of empathy to prosocial and related behaviors
Psychol. Bull.
Assessment of eating disorders: interview or self-report questionnaire?
Int. J. Eat. Disord
Structured Clinical Interview For DSM-5 Disorders, Research Version (SCID-5-RV). Arlington
A longitudinal investigation of mortality in anorexia nervosa and bulimia nervosa
Am. J. Psychiatry
A reciprocal model of face recognition and autistic traits: evidence from an individual differences perspective
PLoS ONE
Cited by (14)
Anorexia Nervosa and Autism Spectrum Disorder: A Systematic Review
2021, Psychiatry ResearchCitation Excerpt :Among the others, Anorexia Nervosa reports the highest rates of both over-threshold and sub-threshold comorbid autistic traits. Studies with adults (using both self-report and diagnostic measures) report between 8.8% and 24.5% of participants meeting the criteria for a possible autistic condition in comorbidity (Dell'Osso et al., 2017b; Karjalainen et al., 2018; Kerr-Gaffney et al., 2020a; Kerr-Gaffney et al., 2020c; Kerr-Gaffney et al., 2020d; Kerr-Gaffney et al., 2020e; Westwood et al., 2017;). In contrast, studies with young people report slightly lower rates (between 4% and 22% of participants meeting the clinical cut-off) (Margari et al., 2019; Nazar et al., 2018; Pruccoli et al., 2021).
An updated transdiagnostic review of social cognition and eating disorder psychopathology
2021, Journal of Psychiatric ResearchCitation Excerpt :Some research suggests lower empathy in current AN compared to recovered AN (Morris et al., 2014). However, other studies have found no differences in empathy between current AN and individuals recovered from AN or who have been weight restored (Beadle et al., 2013; Kerr-Gaffney et al., 2020). Furthermore, one study found that individuals with AN had higher empathy than male controls and individuals with Asperger's Syndrome, but did not differ from female controls (Jermakow and Brzezicka, 2016).
Looking beneath the surface: Distinguishing between common features in autism and anorexia nervosa
2021, Journal of Behavioral and Cognitive TherapyCitation Excerpt :For example, individuals with AN who score above threshold on autism diagnostic measures experience heightened levels of cognitive rigidity compared to those with low autistic traits (Westwood, Mandy, & Tchanturia, 2017). Finally, the combination of these two conditions may create an additive effect, with people with AN scoring above threshold on gold-standard autism diagnostic measures exhibiting additional difficulties with emotion recognition and empathy not seen in AN only (Kerr-Gaffney, Mason et al., 2020; Kerr-Gaffney, Harrison, & Tchanturia, 2020b). Further research into similarities and differences across autistic people, autistic people with AN, and people with AN only, could give valuable insight into differentiating and diagnosing these conditions.
A multidimensional examination of affective and cognitive empathy in anorexia nervosa
2023, European Eating Disorders ReviewAlexithymia in Eating Disorders: A Narrative Review
2023, Eating Disorders: Volume 1,2