Salivary alpha amylase and cortisol responses to different stress tasks: Impact of sex

Abstract

Neuro-endocrine markers such as salivary alpha amylase (sAA) and cortisol (CORT) play an important role in establishing human responses to stressful events. Whereas sAA levels reflect sympathetic system activity, salivary cortisol appears to be a valid measure for HPA axis activity. Although many studies looked at either sAA or CORT responses in reaction to stress, work still has to be done to look at the way these systems interact, especially when both systems are activated. Additionally, sex effects in CORT responses have been investigated relatively often, but possible sex differences in sAA levels and responses, or the way both systems interact has not been the focus of sufficient studies to yield a univocal conclusion.

In this study we presented a group of healthy participants (n = 80) with two mildly stressful tasks, consisting of an aversive picture rating task and a cold pressor stress (CPS) task. The second task was compared with a control task. We expected a rise in sAA level in response to the first task and sAA as well as CORT responses on the second task and explored the interaction between the two responses.

Results indicate that sAA is indeed a sensitive marker in both psychologically and physically induced arousal paradigms, whereas a cortisol response was only observed in the CPS task. Men had higher sAA levels than women during the complete course of the study, but men and women were comparable in their responsivity to the tasks. No strong correlations between sAA and CORT responses were found.

Introduction

Neuro-endocrine markers play an important role in establishing the bodily reaction in studies on human responses to stressful events. Salivary cortisol (Cort) sampling has been used as a measure for HPA axis activity for quite some time (Kirschbaum and Hellhammer, 1994). The sympathetic adrenal medullar system (SAM) activation as part of the stress response is monitored by measurement of salivary alpha amylase (sAA) levels in several studies (Bosch et al., 1996, Granger et al., 2007, Nater et al., 2005, Rohleder et al., 2006). Studies show marked increases in sAA levels in response to stressful tasks or procedures, such as a parachute jump (Chatterton et al., 1997) or a stressful video game (Skosnik et al., 2000) as well as other types of psychological (e.g. pre-examination) stress-inductions (Bosch et al., 1996, Bosch et al., 2003). The finding that psychosocial stress stimulates sAA were underlined in studies employing the Trier Social Stress Test (TSST) (Nater et al., 2006b, Nater et al., 2005, Rohleder et al., 2004) and a study in which subjects underwent a stressful fMRI procedure, involving negative emotional picture viewing (van Stegeren et al., 2006) or video stressors (Takai et al., 2004). Finally, pharmacological manipulation of the SAM system underscored the role of sAA amylase as an indicator of sympathetic activity. Stimulation of the SAM system by administration of yohimbine (an alpha-2 adrenergic receptor antagonist) was shown to significantly increase sAA levels (Ehlert et al., 2006), whereas application of the beta-adrenergic receptor blocker propranolol was successful in reducing stress-induced sAA increases (van Stegeren et al., 2006).

Activation of the stress response in reaction to a threatening, negative or unexpected experience evokes a chain of neuro-endocrine and nervous system reactions. The SAM system with catecholamines such as noradrenaline and adrenaline, in interaction with glucocorticoïds, plays a key role in both normal homeostasis and in sympathetically mediated responses to stress. The various roles of glucocorticoïds (GCs) in stress responses have been extensively reviewed (Sapolsky et al., 2000). GC actions permit, stimulate or suppress an ongoing stress response or can be preparative for a subsequent stressor. But the exact way these systems interact in the stress response is not univocal. Although many studies looked at either NA or CORT responses in reaction to stress, reality is that both systems are part of a coherent unity that needs to work in concert. Work has to be done to look at the way these systems interact, especially when both systems are activated.

This study was designed to investigate sAA and Cortisol responses to two different stressors. The first task was a mild (psychological) stress task in which subjects watched a large set of neutral and emotional pictures from the International Affective Picture Set (IAPS) (Lang et al., 1997). The task was intended to only activate the SAM system — but not the HPA axis and evoked increased amygdala activation measured with fMRI in a previous study due to its emotional arousal (van Stegeren et al., 2005). Additionally it evoked an increase in sAA levels in healthy subjects, but no cortisol increase (van Stegeren et al., 2006). Immediately after this task the group was split: half of the participants underwent a second stress task, the other half a control condition. This stress task consisted of a cold pressor stress (CPS) procedure that has been shown in earlier studies to evoke a CORT response in a substantial proportion of the participants (Andreano and Cahill, 2006, Cahill et al., 2003). Salivary sampling at several points in time during the experiment would serve as an indication of the sAA and CORT levels, the responsivity of both systems and its possible interactions.

Based on a scarce set of studies that show that consecutive exposure to stressors showed an accumulation of stress responses (Liu et al., 2007, Sabban and Serova, 2007), we hypothesized that the response on one stress task can affect the response on consecutive experiences.

Several studies showed that men and women differ in their response to stressful events: in their personal emotional rating of emotional material (women almost always higher than men), or their memory performance of emotional information (Bradley et al., 2001, Cahill and van Stegeren, 2003, Canli et al., 2002, van Stegeren et al., 1998). Also, baseline differences between men and women were found on several cardiovascular measures such as heart rate and blood pressure (Saab et al., 1989, Suarez et al., 2004) as well as effects of sex and hormonal status on the physiological response to acute psychosocial stress (Kudielka et al., 1998, Kuhlmann and Wolf, 2005, Stark et al., 2006, Wolf et al., 2001). Several studies found a stronger salivary cortisol response in men than in women in reaction to stressors (Kirschbaum et al., 1999, Kudielka and Kirschbaum, 2005). However, sex differences do not substantially explain the variability in the CORT response to laboratory stressors in young subjects, as demonstrated in a recent large meta analysis (Dickerson and Kemeny, 2004). So, although several studies investigated sex differences in CORT response, only few studies focused on sex differences in sAA levels or responses and the studies led to ambiguous results (Kivlighan and Granger, 2006, Nater et al., 2006a, Takai et al., 2007).

The aim of the present study was twofold: the first research question is whether sAA and CORT responses are related during two consecutive stress tasks. We hypothesize that SAM system and HPA axis responses on the tasks are interconnected. More precisely, we hypothesize that subjects reacting with a sAA increase on the first task are more sensitive to a following stressful stimulus, setting up the system for a stronger response to the second task. So we hypothesized that a strong sAA response on the first task predicts a stronger sAA and CORT response on the second stress task. The second research question refers to the idea that men and women might differ in their stress response. We want to explore whether sex is affecting baseline sAA and CORT levels as well as the reactivity and the interaction of both hormonal systems.