Stress-induced changes in human salivary alpha-amylase activity—associations with adrenergic activity

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Summary

The salivary enzyme alpha-amylase has been proposed to indicate stress-reactive bodily changes. A previous study by the authors revealed marked increases in salivary alpha-amylase following psychosocial stress, indicating a stress-dependent activation of salivary alpha-amylase. Salivary alpha-amylase has been suggested to reflect catecholaminergic reactivity. Our aim was to assess/evaluate a possible relationship between salivary alpha-amylase and adrenergic parameters, i.e. catecholamines, as well as other stress markers.

Using an intra-individual repeated measures design, 30 healthy young men underwent the Trier Social Stress Test (TSST), which consists of a mental arithmetic task and free speech in front of an audience and a control condition in randomized order. Salivary alpha-amylase and salivary cortisol as well as plasma catecholamines and cardiovascular activity were repeatedly measured before, during, and after both conditions.

Significant differences were found between the stress and the rest condition in salivary alpha-amylase, salivary cortisol, plasma catecholamines, and cardiovascular parameters (heart rate, LF, HF, LF/HF). However, general alpha-amylase responses (area under the curve) were not associated with general responses in catecholamines and cortisol in the stress condition (r smaller than 0.25 for all analyses). Analysis of cardiovascular parameters indicates a positive relationship between amylase and sympathetic tone (LF/HF) during stress.

Salivary alpha-amylase is sensitive to psychosocial stress. Since it does not seem to be closely related to other biological stress markers such as catecholamines and cortisol, salivary alpha-amylase may be a useful additional parameter for the measurement of stress.

Introduction

Reliable biological indicators for stress reactions are valuable markers in both psychophysiological research and clinical practice. A number of stress markers, such as cortisol and catecholamines (norepinephrine, NE, and epinephrine, EP), have been found to reliably indicate reactivity of physiological stress systems, e.g. the hypothalamic-pituitary-adrenal (HPA) axis and the sympathetic-adrenal-medullary (SAM) system. However, stress is a multi-faceted phenomenon that requires a multidimensional measurement approach. Thus, despite the wide array of parameters used in stress research, a widening of the methodological canon is desired. Studies in animals and humans suggest that activation of the autonomic nervous system with a combination of both sympathetic and parasympathetic innervation of the salivary glands leads to high activity of the salivary enzyme alpha-amylase (Asking and Gjorstrup, 1987, Schneyer and Hall, 1991, Speirs et al., 1974). Not only exercise (Chatterton et al., 1996, Nexo et al., 1988, Steerenberg et al., 1997, Walsh et al., 1999), but also psychological stressors are able to stimulate salivary alpha-amylase. Bosch et al. (1996) were able to show anticipatory stress-dependent alterations in alpha-amylase. In another study using a laboratory task to induce acute stress, salivary alpha-amylase was measured before, during, and after an active memory task, passive watching of a gruesome video, and a control condition. Amylase output differed significantly between the three conditions, with the highest levels found during the passive video task (Bosch et al., 2003). In a recent study, employing a potent laboratory stress protocol (i.e. the Trier Social Stress Test, TSST), we found salivary alpha-amylase to be a variable that is sensitive to psychosocial stress (Nater et al., 2005), displaying pronounced increases following induction of stress compared to a rest condition. Although concomitant increases in salivary cortisol and heart rate have been observed, no statistical correlation has been found between salivary alpha-amylase and these parameters. Salivary alpha-amylase has been suggested to reflect catecholaminergic changes due to increased activation of the sympathetic-adrenal-medullary (SAM) system. The activation of salivary alpha-amylase during physical and psychological stressors, and the concomitant increases in plasma catecholamines (norepinephrine and epinephrine) due to these stressors, led to the assumption that salivary alpha-amylase can be measured as a non-invasive substitute for catecholamines. In a series of studies, subjects were exposed to physical (running, exercise, exposure to heat and cold) and psychological (examination) stressors. Significant correlations between salivary alpha-amylase and plasma norepinephrine, as well as plasma epinephrine (r=0.64, r=0.49, respectively) in the exercise conditions have been found (Chatterton et al., 1996). Using these results as support for the validity of measuring amylase instead of catecholamines, several studies were performed which measured alpha-amylase as an indicator for either epinephrine or norepinephrine (Chatterton et al., 1997, Chatterton et al., 2000, Milad et al., 1998, Morrison et al., 2003, Skosnik et al., 2000, Xiao et al., 2000).

However, the relationship between SAM parameters and salivary alpha-amylase has not been established in different stress paradigms, particularly in psychosocial stress. The aim of this study was therefore to examine the association of salivary alpha-amylase changes with plasma catecholamines. Furthermore, we examined the relationship of alpha-amylase to other stress markers, such as cortisol and cardiovascular parameters.

Section snippets

Subjects

Subjects were recruited through flyers and announcements at the University of Zurich and the Swiss Federal Institute of Technology, Zurich. All subjects were medication-free and non-smokers. Participants were required to complete a screening questionnaire that contained exclusion criteria designed to reduce confounding factors that have been shown to affect physiological dependent measures. Subjects with any acute or chronic somatic or psychiatric disorder were excluded from the study.

Sample characteristics

Thirty white male healthy subjects participated in the study (age: mean=24.8 years, SD=2.4 years, range 19–28 years; body mass index: mean=22.48, SD=1.98, range 19.4–27.1). Randomization resulted in two groups, with 15 participants undergoing the rest condition before the TSST (Group 1) and 15 participants undergoing the rest condition after they performed the TSST (Group 2). However, one subject was unable to perform the TSST because of acute illness. The randomized groups did not differ with

Discussion

This study was designed to examine stress-dependent changes in salivary alpha-amylase activity in relation to plasma catecholamines (NE and EP), as well as other variables sensitive to stress, such as salivary cortisol and cardiovascular parameters. We found a clear and distinct pattern of stress-related changes in salivary alpha-amylase, with a pronounced increase due to acute psychological stress. In line with findings from other studies applying psychological stressors, we were able to

Acknowledgements

We would like to thank Dr Beate Ditzen for help in preparation of the manuscript. We gratefully acknowledge the help of Elvira Abbruzzese, Carole Morandi, and Barbara Gläser in conducting the experiments.

This study was supported by a financial grant of the Stiftung für wissenschaftliche Forschung, University of Zurich.

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    Dr Koller passed away during preparation of this manuscript. He will be missed.

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