Introduction
Largely independent of the quality of the parent-child-relationship, children readily develop trustful relationships with companion animals, and often communicate personal matters to pets rather than to other humans (Kurdek, 2008, 2009a,b; Parish-Plass, 2008). As social companions, animals may benefit the development of children in the cognitive, emotional, and physical domains (Melson et al., 1991; Bodmer, 1998; Melson and Fine, 2006).
Attachment theory provides a particularly powerful background for the explanation of the positive socio-emotional effects of animals, although Ainsworth (1963, 1972) and Bowlby (1969/1982), the founders of attachment theory, did not integrate animals in their deliberations. In particular, attachment theory contributes toward our understanding why many humans in need of social support relate more easily and spontaneously to animals than to other humans (Brown and Katcher, 2001; Beck and Madresh, 2008; Kurdek, 2008, 2009a,b; Beetz et al., 2011). Children develop their specific attachment representation (see below) during their first year of life, mainly via interacting with their primary caregivers (Bowlby, 1969/1982). The primary function of the behavioral system (Baerends, 1976; George and Solomon, 2008; Marvin and Britner, 2008) of attachment is to establish and maintain proximity to the caregiver, ensuring caregiving and protection for the child. Thereby, this behavioral system also reduces and buffers stress, because an effective caregiver also provides a safe haven in stressful contexts and serves as a secure base for exploration of the environment (Bowlby, 1969/1982). Sensitive and reliable early caregiving generally results in secure attachment (Ainsworth et al., 1971). Secondary adaptive strategies such as insecure (avoidant or ambivalent) or disorganized attachment develop in reaction to sub-optimal caregiving. These strategies are regulated via mental representations, so-called “internal working models” (Bretherton and Munholland, 2008), which evaluate and organize the experiences made and affect how individuals respond to their primary caregivers.
In contrast to securely attached children, children with insecure-avoidant attachment have experienced their caregivers as rejecting and unsupportive and therefore, may avoid proximity rather than relating to them when stressed. As an alternative strategy, avoidant children try to distract themselves and tend to emphasize explorative behavior in stressful situations (Ainsworth and Wittig, 1969; Ainsworth et al., 1971), instead of crying or openly seeking proximity and contact. However, their cortisol levels during a separation from their caregivers are generally higher than in securely attached children (Spangler and Schieche, 1998). Attachment disorganization is characterized by a breakdown of adaptive strategies in relevant situations (Main and Solomon, 1986, 1990), which may be reflected in different ways, e.g., dissociation, disorientation, fear, or aggressive behavior, particularly in the context of social stress. Disorganized attachment may develop in response to abusive, negligent, or frightening behavior of the caregiver or in response to loss of, and separation from that person. Insecure as well as disorganized attachment, found in 60–90% of clinical samples or populations in schools for special education (van Ijzendoorn and Bakermans-Kranenburg, 1996; Julius, 2001), are considered risk factors for socio-emotional development (Strauss et al., 2002), while secure attachment is known as a potent protective factor (Werner and Smith, 1982). Also in non-clinical samples only 50% (Grossmann et al., 1981, German sample) to 60% (Ainsworth et al., 1978, US-sample) of the children show a secure attachment.
The internal working model developed with the primary caregiver is normally transferred to all further close relationships (Sroufe and Fleeson, 1988; Howes and Hamilton, 1992; Dozier et al., 2001; Sroufe et al., 2005), for example to teachers or therapists. Hence children with insecure or disorganized attachment find it more difficult than individuals with secure attachment to seek effective social support from other humans and profit from them in stressful situations (Maunder and Hunter, 2001). In general, attachment status and social support are considered major and closely related factors in modulating both the sympatho-adrenergic stress axis as well as the hypothalamo-pituitary-adrenal (HPA) axis, and in adjusting their reactivity early on (de Vries et al., 2003; Beetz et al., 2011; Julius et al., 2013). This may have far-reaching consequences for life, because sub-optimal social relations are currently recognized as a major risk factor for individual well-being and health (Coan, 2011).
This social regulation of stress and the influence of attachment representations can also be linked to other models of stress regulation such as Folkman’s and Lazarus’ transactional model of stress (Lazarus and Folkman, 1984). It can be assumed that a child (or adult) with insecure or disorganized attachment has learned that effective social support as a coping resource is not available in times of distress. Even though other resources (e.g., problem solving skills, utilitarian resources, etc.) might be available to the individual, this learned discouragement of seeking social support and thus diminished availability of social support as stress management strategy might increase the stress via an increased discrepancy between the person’s coping resources and the demands of a given situation.
It is further plausible that insecure and/or disorganized attachment could be linked to deficits in personal self-regulation, as postulated by the DEDEPRO Model (De la Fuente and Justicia, 2007). Good behavioral hetero-regulation (e.g., by the parents) in early childhood, as in a secure attachment promoted by sensitive and available caregivers, would promote the internalization of adaptive self-regulating behavior with adequate coping strategies that focus on social management. A social environment with little or inadequate social hetero-regulation (insecure attachment) in contrast, would favor the establishment of social avoidance strategies or strategies that focus on emotion management (in the sense of emotional down regulation which is typical of insecure-avoidant attachment), but are likely less effective in the regulation of physiological stress responses.
In a school context, an insecure attachment pattern impairs a student’s ability to profit from social support by his teacher or peers in stressful situations with regard to stress regulation. This again, however, negatively influences performance (e.g., in test situations) and cognitive and socio-emotional learning in general, since the prerequisites, such as executive functions (EF, e.g., cognitive flexibility, impulse control, working memory, self-motivation, problem solving, reasoning, and planning; Miyake et al., 2000) located in the prefrontal cortex are sensitive toward stress. Already slight increases in the stress-hormone cortisol are associated with a noticeable decrease in executive functioning.
According to the criteria of Ainsworth(1991; Kurdek, 2008), companion animals can be attachment figures for their owners. Animal owners, and particularly children, indeed frequently turn to their animals for social support in emotionally stressful situations (Rost and Hartmann, 1994; McNicholas and Collis, 2006). Even children with sub-optimal attachment are obviously able to meet companion animals with trust (Kurdek, 2008, 2009a,b), which is consistent with the clinical experience that children are open to relate to pets even if they would not approach human caregivers in stressful situations. Hence, attachment representations acquired with humans are seemingly not spontaneously transferred to animals. In fact, interacting with a friendly companion animal may be associated with lower cardiovascular responses and cortisol levels than interacting with people (Friedmann et al., 1983; Lynch, 1985; Allen et al., 1991, 2002; Odendaal and Meintjes, 2003). Such effects are commonly related to effective social support. Touch and physical contact, as a component of social support (Ditzen et al., 2008), is mainly observed in secure attachment relationships with humans (Hazan and Zeifman, 1999). However, it is a concomitant of interactions with friendly companion animals, especially dogs, and has been shown to significantly contribute to stress attenuation in children with insecure and disorganized attachment (Beetz et al., 2011).
Based on the hypothesis that particularly in children with insecure or disorganized attachment an animal may be a more efficient emotional social supporter than either a friendly adult or a toy dog, we predict that children with such attachment will experience a greater stress-alleviating effect from the presence of a friendly dog than of a friendly person when exposed to a social stressor. Furthermore, we expect that the quality and quantity of interactions between child and social supporter will affect stress modulation. To test these predictions, we exposed children with insecure and/or disorganized attachment to a standardized social stressor, either in the presence of a real dog, a friendly human, or a toy dog as an additional control for the potential specific effects of the presence of a real dog. To judge the effects on the HPA-axis, cortisol was determined from saliva samples. Furthermore, the behavior of children was coded from video tape.
Discussion
In our sample of male children with insecure or disorganized attachment, cortisol levels dropped significantly faster and to lower levels after a stressor when supported by a real dog in comparison with other support conditions (Figure 1). Similar to the results by Beetz et al. (2011), support condition did not affect peak salivary cortisol levels during the socially stressful situation. Self-reported, subjective stress, did not parallel salivary cortisol in the different support conditions. This is less surprising than it may seem at first, since especially persons with insecure-avoidant attachment tend to minimize or dismiss negative emotions in self-reports, also in connection with experimental stressors, while they do show expected psychophysiological stress responses (Fraley and Shaver, 1997; Mikulincer, 1998; Roisman et al., 2004; Diamond et al., 2006). Furthermore, the SAM measures each dimension only via one “item” (a row of five pictograms), which might limit its sensitivity for smaller changes in affective states. However, a within-group analysis showed a significant decrease of activation for the real dog condition only; this can be interpreted as an increase of calmness over the course of the entire procedure. Due to the preliminary character of the study and the limited sample size in the groups supported by a toy dog and a friendly student, this result might hint at possible between-group differences if sample sizes in the comparison groups were higher, in spite of the tendency to dismiss negative emotions in general in avoidantly attached individuals. However, this needs to be tested with larger samples and probably more sensitive measures.
The positive effect of the dog on post-stress relaxation fits children’s reports that in times of distress they turn to their own animals for support and generally have a trusting relationship with their companion animals (Kurdek, 2008, 2009a,b; Beetz et al., 2011). We suggest that a friendly interaction with the dog may trigger release of the hormone oxytocin, which inhibits cortisol synthesis, and thereby, also facilitates relaxation and stress regulation (de Vries et al., 2003; Beetz et al., 2011; Uvnäs-Moberg et al., 2011; Julius et al., 2013). It has indeed, been documented that friendly interactions with dogs, especially stroking them, may increase systemic oxytocin (Odendaal, 2000; Odendaal and Meintjes, 2003; Miller et al., 2009; Nagasawa et al., 2009; Handlin et al., 2011). Our assumption is supported by our finding that the stress-dampening effect of the dog was not just due to its mere presence, but actually was related to the intensity of physical contact and active stroking of the dog. Distant interaction, especially with an unfamiliar animal, is probably not as effective as physical contact in causing an increase in oxytocin levels, since pleasant touch directly triggers oxytocin release (Stock and Uvnäs-Moberg, 1998) in response to the activation of non-noxious sensory nerves stimulated by physical contact (Petersson et al., 1999; Matthiesen et al., 2001; Lund et al., 2002; Handlin et al., 2009).
Obviously most children related to the dog during the stressful procedure and were thus able to utilize it for social support, at least in the relaxation phase after the end of the stressful situation. As has been shown in previous research, interaction with animals, and even more so, with one’s own companion animal, can alleviate endocrinological and cardiovascular stress responses, very likely to a large extent mediated by oxytocin (Friedmann et al., 1983; Nagengast et al., 1997; Allen et al., 2002; Motooka et al., 2006; Cole et al., 2007; Viau et al., 2010; Beetz et al., 2011; Handlin et al., 2011; for a review see Julius et al., 2013). Since this was found in male as well as female participants, and previous research on stress responses in children found no sex-differences, it may be justified to assume similar effects in female children. However, this needs to be confirmed in further studies.