Social behavior, cortisol, and sIgA levels in preschool children

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Abstract

Objective: This study aims to explore the possible existence of behavioral states in early stages of development, which are associated with specific cortisol production profiles and consequently with changes in the immune response [secreted immunoglobulin A (sIgA)]. Methods: The subjects were 27 boys and 21 girls of preschool age whose behavior was videotaped in free play interactions. Their behavior was then evaluated using an ethogram of the social behavior of the child. Cortisol levels were measured using a radioimmunoassay in saliva samples, and sIgA levels were measured by means of an ELISA, also in saliva samples. Results: No correlation between cortisol and sIgA levels was found. Variance analysis revealed that the only behavioral pattern, which showed significant differences with regard to cortisol levels, was isolation. Conclusions: There seems to be a connection between cortisol levels and isolation behavior; we found no relation between high cortisol levels and a lower sIgA secretion.

Introduction

Over the last few decades, there has been an important increase in data, which indicate the existence of complex links between the immune system, the central nervous system, and the endocrine system on one side and psychological phenomena such as reactions to stressful events and situations on the other [1], [2], [3], [4], [5]. It has been proven that depression, anxiety, psychological distress, social support, etc. can cause alterations in the activity of diverse parameters of the immune response. It has been hypothesized that these alterations may affect the body's capacity to combat infections, autoimmune diseases, and cancer, although no clear evidence has yet been presented [3], [6], [7], [8], [9], [10], [11], [12]. In general, research in this field (psychoneuroimmunology), which has used human subjects, has always been carried out using adults. Various authors [13], [14] have pointed out the need for research into the relation between psychological processes, neural and endocrine activity, and the immune system in children. Much of the research in this field has focused on humans in midlife and has utilized adult animal models. Less is known concerning the nature of behavioral CNS–immune interactions during early life when developmental processes within the immune system and the CNS may amplify or diminish the impact of behavioral and CNS effects [13]. Some authors have hypothesized that experiences during early stages of development could have a serious effect on the development of the immune system's response capacity, with long-term consequences for this response capacity in later stages, thereby affecting the subjects' susceptibility to disease [11], [15]. It has been found that nursery reared, as opposed to maternally reared monkeys, have lower levels of natural killer (NK) function and higher levels of mitogenic function [16].

One relevant aspect of children's early psychology is their social relationship with their peers. Children's social behavioral profile as regards their relationship with their peers is a good indication, among other things, of their degree of social adaptation and competence [17], and there is evidence that children who have difficulty relating to their peers (rejection, inhibition, etc.) tend to suffer from social adjustment problems during later stages [18], [19]. Some studies have investigated the relation between social behavior in children and cortisol levels (the principal hormone produced in response to psychosocial stress) by examining the hypothalamus–pituitary–adrenal axis (HPA) [20], [21], [22]. Some authors have suggested that the circadian pattern of cortisol production and the threshold for stress-mediated HPA activation in humans are probably developed during the early stages of development [23], [24]. In this way, at birth, the human adrenocortical system is highly labile and responsive to stimulation. Later on, it becomes increasingly difficult to elicit elevations in cortisol response to, for example, routine procedures like a physical examination followed by childhood inoculations [25], and the circadian rhythm in cortisol production becomes readily apparent [24]. This raises the possibility that early childhood experiences may affect this process, thereby influencing the HPA axis' response to subsequent environmental events. There is also a large body of evidence, which supports the assertion that the preschool years are a key period in a child's social and emotional development [26]. In particular, child–environment interactions during this period seem to be a critical factor in the development of emotional and behavioral ‘autocontrol.’ This would suggest that early individual differences in the reactivity of the HPA axis during the preschool years influence the development of the emotional and behavioral self-regulation processes. The persistent activation of the HPA axis in response to stress is associated with different conditions (immune deficiency, cognitive deterioration, and psychological maladjustment).

On the other hand, pharmacological glucocorticoids and cortisol seem to be, above all, immunosuppressives. The administration of corticosteroids results in a reduction in the number of lymphocytes [27], [28]. Glucocorticoids also, administered exogenously to various species, stunt growth and produce an increase in the catabolism of immunoglobulins and an associated decrease of these in serum, as well as antibody production decrease, cytotoxic cell generation inhibition, T helper cell number decrease, and reduction in NK cell reactivity [27]. Various studies have analyzed the relation between social behavior and immunoglobulin levels (indicative of the immune system's activity rate). Although we are not aware of any such studies involving young children, studies involving adolescents have been carried out. To be more specific, some authors have used the secreted immunoglobulin A (sIgA) as an interesting indicator. IgA is the predominant antibody detected in bodily secretions. The majority of infectious agents enter the body by means of mucosal surfaces, and the presence of IgA-type antibodies in the secretions that cover such surfaces constitutes a first line of defense against infections, especially those that affect the upper respiratory tract, the gastrointestinal tract, and the urogenital system (with regard to the first two, the majority of childhood illnesses occur during the first stages of development). It was found that the IgA response to the administration of an antigen was weaker when the subjects were in a negative mood and stronger when they were feeling more positive [29]. In the same way, it was reported that subjects exposed to humorous film significantly more often showed an increase in sIgA concentrations than subjects exposed to nonhumorous film [30]. Also, it was observed that the sIgA secretions were significantly lower in high-stress situations (academic stress) than in low-stress situations [31], [32]. In studies involving children, other authors have analyzed the relation in preschool children between events or situations, which produced psychosocial stress (starting school), adrenocortical activity (salivary cortisol levels), and immune system activity levels (measured by blood lymphocyte levels, etc.) [33]. The results suggested that starting school produces a high degree of stress capable of provoking increases in cortisol levels and demonstrated that children with greater adrenocortical reactivity have increases in B cell numbers and less effective B cell-mediated antibody production, whereas children with more behavioral difficulties show declines in all T and B cell subsets.

Studies of the relation between psychosocial factors, neuroendocrine activity, and susceptibility to disease in young children are difficult to conduct, as it is not possible to use evaluation methods, which require a developed verbal capacity. It is in this context that the evaluation of nonverbal behavior, by means of systematic observation, reveals its full analytical potential with regard to social behavior [34], [35]. This study aims to explore the possible existence of behavioral profiles in early stages of development, which are associated with specific cortisol production profiles and therefore with changes in the immune response (sIgA).

Section snippets

Subjects

The subjects were 48 preschool children (27 boys and 21 girls) from two classrooms in a private school in San Sebastian (Spain). The mean age of the sample was 4 years 8 months, with a range of 4 years 3 months–5 years 1 month. The subjects were all Caucasian, urban dwellers, and middle-to-upper class. The parents of the children were informed of the study and gave their consent for it to be carried out.

Observations in the classroom

The social interaction of the subjects with their peers was videotaped daily from February

Results

No significant correlation was found between cortisol and IgA levels. See Table 2 for an overview of the descriptive statistics relating to the physiological variables.

In order to study potential differences in behavioral patterns as a consequence of differences in the cortisol levels, subjects were divided into three groups according to percentile distribution (Low: less than or equal to 0.10; Medium: between 0.10 and 0.18; High: higher than 0.18) and according to their levels in this latter

Discussion

In this study, we have analyzed the relation between social behavior in preschool children, their cortisol levels and their immune activity (sIgA levels).

With regard to the relation found during our study between cortisol levels and social behavior, the only behavioral state for which significant differences were detected regarding cortisol levels was that of isolation: subjects from the high cortisol group and the low cortisol group demonstrated a higher degree of isolation behavior than

Acknowledgements

This research was supported by Basque Country Government Grant PI97/7. We would like to express our gratitude to the Principal's office, teaching staff, parents, and children of the ‘Santo Tomas Lizeoa’ school.

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