Preliminary evidence for increased parasympathetic activity during social inclusion and exclusion in adolescents with functional abdominal pain
Introduction
Integration into peer groups is crucial for the individual development during adolescence. The transition period from childhood to adolescence is characterized by increasing time spent with peers and a significant decrease of time spend with parents [1], [2]. Thus, it is not surprising that the development from childhood to adolescence is also marked by growing concerns how one is perceived by peers as well as an increased sensitivity to social exclusion [3], [4]. Peer victimization during adolescence can take various forms, including direct bullying behaviors with open attacks on the victim (e.g., teasing, physical aggression) as well as more indirect manifestations such as social isolation, rejection, and exclusion from the group [5], [6], [7]. Recent meta-analyses demonstrated that peer victimization represents both an antecedent and a consequence of internalizing and externalizing mental health problems in children and adolescents [8], [9]. It has also been associated with physical health problems such as functional somatic complaints and especially symptoms of pain e.g., pediatric functional abdominal pain (FAP) [10], [11], [12], a prevalent functional gastrointestinal disorder (FGID). Despite this evidence, no study to date has directly investigated the mechanisms underlying the association between peer victimization - especially social exclusion - and functional somatic complaints in clinical pediatric samples.
Previous research has established that neural processing of both, physical and social/affective pain, are governed by partly overlapping neural substrates [13]. The association between physical and social/affective pain is probably mediated by the autonomic nervous system (ANS). For instance, pain-related FGIDs such as irritable bowel syndrome (IBS) in particular, have previously been linked to ANS imbalance and dysfunction [14], [15], [16]. The role of ANS alterations is discussed in terms of etiology and maintainance of FGIDs. It has been suggested that these disorders are related to pertubations in the brain-gut interaction and that they are influenced by reciprocal biological and psychosocial processes [17], [18]. Whereas the ANS and the hypothalamic-pituitary-adrenal (HPA) axis are thought to be crucial mediators of the bidirectional brain-gut interaction [18] in adult IBS, the research on FGIDs in children is scarce. However, there is first evidence for ANS and HPA axis disturbances in pediatric FAP and/or IBS [16], [19], [20].
Based on these observations, alterations of the ANS may represent a link between peer victimization - especially social exclusion - and FGIDs. In healthy individuals, unexpected social rejection is associated with an immediate response of the parasympathetic nervous system in terms of a transient cardiac slowing. This was demonstrated in adults [21], [22], [23], [24] and adolescents [25]. Parasympathetic activation over time periods in the range of minutes has also been reported in response to social exclusion [26]. This reaction pattern is in accordance with the notion that increased parasympathetic activation reflects processing of emotions and self-regulatory effort [27]. More precisely, parasympathetic activation in response to challenging demands may indicate increased emotional processing which could facilitate adaptive social behavior and affective responses [28], [29]. This assumption is in accordance with the neurovisceral integration model [30] which posits that parasympathetic activation can indicate the functional integrity of the neural networks implicated in emotion-cognition interactions.
However, experimental research on the ANS reaction to social exclusion has been largely carried out in healthy participant groups. Given the overlap of the neural response to social and physical pain [13], there is grounds to assume that individuals with chronic pain might also be particularly sensitive to distressing social experiences such as exclusion. This may be especially true for adolescents, since positive peer evaluation is of particular importance for this age group [31] and peer-victimization has been shown to be a considerable developmental risk [8], [9]. Despite assumptions that social stress may exacerbate somatic symptoms in clinical groups suffering from pain disorders [e.g. 32], the mechanisms mediating this relationship are not well understood. Studies on clinical samples are lacking and most importantly, no study to date has addressed these questions in clinical samples of adolescents. This knowledge is highly relevant, as chronic pain during this developmental period has been associated with impairments in academic achievement and school absenteeism [33] and with a considerable risk for an unfavorable long-term course [34].
Therefore, the present study aimed to examine the parasympathetic reaction during social exclusion in healthy adolescents and those suffering from FAP, which is one of the most prevalent pediatric pain conditions [35]. To experimentally induce social exclusion, we employed the Cyberball game, an ecologically valid, established paradigm based on a virtual ball-tossing game in which participants are included or excluded [36], [37] from peers. Given a higher vulnerability for the negative impact of social exclusion in adolescents with FAP [e.g. 10] and based on previous studies on ANS function following social rejection or exclusion [e.g. 25,26], we expected an increased parasympathetic activation during social exclusion in both groups but significantly more pronounced in adolescents with FAP as compared to controls.
Section snippets
Participants
The pediatric Rome-III criteria (36) for FAP were used as inclusion criteria for the experimental group. According to the criteria, participants were included if they experienced episodic or continuous abdominal pain at least once a week for two months or more with no evidence of an underlying organic disease. The absence of potential organic factors had to be confirmed by the managing pediatrician or gastroenterologist prior to inclusion. Twenty-one adolescents with FAP (mean age = 11.65 years, SD
Baseline characteristics
Due to technical difficulties, one participant of the FAP group was excluded. Subsequent analyses are based on 20 adolescents with FAP and 21 healthy controls. Analyzed groups did not differ with regard to age, gender, BMI, pubertal development, or rejection sensitivity (CRSQ). As expected, the FAP group scored higher on emotional and behavioral difficulties as measured by the CBCL. The FAP group was characterized by a medium pain intensity in self- and parental ratings. On average,
Discussion
The present study is the first to investigate parasympathetic activation following painful social interactions in adolescents with FAP. Analyses revealed a differential course of parasympathetic activation over time for adolescents with FAP and healthy controls. Whereas the control group showed almost no reaction, the FAP group exhibited a remarkable increase of parasympathetic activation during both consecutive phases of the Cyberball game, namely during the inclusion as well as the exclusion
Conflicts of interest and source of funding
Aiste Jusyte is funded by the LEAD Graduate School & Research Network [GSC1028], a project of the Excellence Initiative of the German federal and state governments. The authors have no conflict to declare.
Acknowledgements
The authors would like to thank Lisa Hunger, Manfred Kooistra, Laura Schuster, Lea Sum, Stephanie Vietze and Luisa Wetzel for their assistance in recruiting participants, conducting the experiment and data management/data entry, and Ryan Dutton for language editing.
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