Elsevier

Journal of Affective Disorders

Volume 266, 1 April 2020, Pages 273-281
Journal of Affective Disorders

Research paper
Autism spectrum disorder traits are associated with empathic abilities in adults with anorexia nervosa

https://doi.org/10.1016/j.jad.2020.01.169Get rights and content

Highlights

  • Individuals with anorexia nervosa demonstrate lower affective empathy for positive emotions compared to controls.

  • Autistic traits predict cognitive and affective empathic abilities.

  • Perception of nonverbal communication did not differ across groups.

Abstract

Background

Social and emotional difficulties have been identified as key factors in the development and maintenance of anorexia nervosa (AN). However, few studies have investigated the influence of comorbid psychopathology on social cognition. The aim of the current study was to examine perception of nonverbal communication and empathy in AN using ecologically valid, performance-based measures, and to explore associations with comorbid psychopathology (anxiety, depression, autism spectrum disorder (ASD) traits, alexithymia, and social anxiety).

Methods

In this cross-sectional study, the Multifaceted Empathy Test (MET) and the Mini Profile of Nonverbal Sensitivity (MiniPONS) were administered to 51 adults with AN, 51 recovered AN (REC), and 51 healthy controls (HCs). Comorbid psychopathological traits were assessed using self-report questionnaires and the Autism Diagnostic Observation Schedule – 2nd edition (ADOS-2).

Results

Individuals with AN showed reduced affective empathy to positive stimuli compared to HCs, and a trend towards lower vocal prosody recognition scores relative to REC. Around a quarter of AN and REC scored above the clinical cut-off for ASD on the ADOS-2, and high ASD symptoms predicted lower cognitive and affective empathy scores.

Limitations

The study is cross-sectional, future research would benefit from examining social-cognition performance and comorbid psychopathology longitudinally.

Conclusions

The findings highlight the importance of ASD symptoms in empathy dysfunction in those with a lifetime history of AN. Future research should explore whether treatment adaptations to accommodate for differences in social-cognitive abilities may be helpful in the treatment of AN.

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.

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