Psychosocial determinants of diurnal alpha-amylase among healthy Quebec workers
Introduction
Biomarkers related to psychosocial stress provide insights into the pathophysiological correlates of diverse human conditions. To date, the biomedical literature on stress-sensitive biomarkers secreted into circulation have centered on (1) the hypothalamic-pituitary-adrenal (HPA)-axis production of the stress hormone cortisol, (2) the sympathetic-adrenal-medullary (SAM)-axis release of catecholamines like adrenaline, and (3) the immune system mobilization of pro- and anti-inflammatory cytokines like interleukin-6 (Nater et al., 2013). Technological advances that led to the biochemical assessment of cortisol via saliva (Kirschbaum and Hellhammer, 1994) promoted non-invasive sampling methods that have revolutionized our understanding of the stress-disease link. By contrast, the SAM-axis and immune systems are still bound to extraction from urine and/or blood, making their incorporation into field studies less feasible. However, salivary alpha-amylase (sAA) has been found to be a proxy of SAM-axis activities (Rohleder et al., 2004) and shows promise as a stress-sensitive biomarker of health.
Alpha-amylase is a primary salivary protein involved in mucosal immune functioning by inhibition of bacteria (Scannapieco, 1994). sAA release is neurologically controlled by acinar cells that are innervated by both the sympathetic and the parasympathetic branches of the autonomic nervous system (Emmelin, 1987). This makes sAA a prime candidate to approximate SAM-axis activities that are unreliably assessed in saliva. Indeed, salivary catecholamine concentrations are several times lower than those obtained from blood, and so do not reflect the acute changes in SAM-axis activities (Kennedy et al., 2001). A growing number of studies reveal that sAA profiles are sensitive to stress exposure (Rohleder et al., 2004, Nater et al., 2005, Nater et al., 2006). Critically, sAA correlates with SAM-axis release of noradrenaline (Thoma et al., 2012), suggesting that sAA is indeed a proxy of adrenergic activities.
Diurnal variation of stress biomarkers can be assessed non-invasively via saliva. Salivary flow rate and saliva composition vary according to 24-h circadian rhythms (Dawes, 1974). Early studies showed that sAA displays low concentrations in the morning and high values in the afternoon (Ferguson et al., 1973). In the first comprehensive assessment of diurnal determinants of sAA, Nater et al. (2007) asked healthy German university students (N = 76) to sample saliva 15 times over the course of single day. Their data confirmed that sAA has a distinct diurnal profile characterized by a pronounced decrease 60-min after awakening and a steady increase of activity thereafter (Nater et al., 2007). Using diary information on momentary stress, mood, food, or physical activity, they further showed that diurnal sAA appears to be relatively independent of self-reported perceived stress and salivary cortisol, but is associated with chronic stress, positive moods, and to age differences (Nater et al., 2007). In the spirit of replication and expansion, this latter finding requires further exploration in a larger and older sample.
Psychiatric research has also endeavoured to identify whether sAA might be useful in the context of psychiatric illnesses like major depressive disorder (MDD). In a case-controlled assessment of afternoon sAA (12h00–16h00), sAA was higher among Japanese individuals with unremitted MDD (n = 28) compared to remitted MDD (n = 43) and healthy controls (n = 103) (Ishitobi et al., 2010). Likewise in another Japanese assessment of afternoon sAA (13h00–17h00), concentrations were higher among female MDD patients (n = 88) than healthy controls (n = 41) prior to an electrical stimulation task (Tanaka et al., 2012). A Polish study showed that depressed individual also show higher morning sAA (8h20–9h00) than age and sex matched controls (Cubala and Landowski, 2014). In a large Dutch cohort study (Veen et al., 2013), MDD patients showed a gradient trend for the highest evening sAA concentrations (22h00 and 23h00) among current MDD (n = 752) followed by remitted MDD patients (n = 611) and lastly healthy controls (n = 329). Recent studies have also endeavoured to link sAA to stress reactivity habituation in panic disorder patients (Petrowski et al., 2015). In sum, psychiatric conditions appear to be associated with elevated diurnal sAA; however, it is unclear whether sAA is associated with other psychiatric symptoms.
Occupational health psychology has also endeavoured to understand how work stress relates to sAA. In a German study of 215 nurses from different hospitals (Wingenfeld et al., 2010), diurnal sAA was collected at four time-points (7h00, 11h30, 17h30, and 20h00). While female nurses showed more pronounced increases in sAA over the day, psychiatric symptoms related to depression, anxiety, work stress, and burnout were not related to sAA. Among Japanese nurses (N = 25) from one hospital who provided samples 12 times over 6 days, morning and evening sAA was higher among night shifts than day shifts (Morita et al., 2014).
The effect of shift work is also important in further understanding diurnal sAA. A study of Canadian paramedics (N = 21) assessed five time-points (+30 min after awakening, 6h00, 12h00, 18h00, and bedtime) on two work days and one rest day (Wong et al., 2012). Dispatchers showed lower daily sAA production than ambulance paramedics, while rotating shift-workers exhibited a flatter sAA diurnal slope than daytime-only workers. Despite mixed directionality, these findings suggest that diurnal sAA is related to workplace stress in non-clinical populations. However, other important workplace stressors have been omitted by sAA studies. For example, stressors associated with task design (skill utilization, decision authority), demands (physical, psychological, contractual), social relations (social support, interpersonal conflicts, harassment), and gratifications (job recognition, career perspective, job insecurity) have been routinely linked to mental health symptoms (Marchand et al., 2015). Yet, whether these factors relate to sAA are, to the best of our knowledge, unknown.
Psychosocial contexts outside of the workplace are also related to sAA. For example, the stress and strain of caregiving (Savla et al., 2013), interparental aggression (Gordis et al., 2010), and acculturation (Snodgrass et al., 2012) are related to distinct diurnal patterns of sAA. This may suggest that the pervasive effects of adversity can be captured using measures of sAA. Notwithstanding, other non-work factors that are important in the stress-disease literature have often been neglected in sAA studies. These include factors like marital status, parenting, socioeconomic status, strained marital and parental relationships as well as social support outside the workplace. These stressors have also been routinely related to problems associated with psychological distress, depression, and burnout (Marchand et al., 2015).
Overall, previous sAA studies exhibit some limitations that the current study endeavours to compliment. Psychoneuroendocrine studies of sAA generally have small sample sizes, varying sampling designs, and diverse protocols that make comparisons difficult in light of the multi-directional findings reported in this growing literature. In the context of workplace stress, studies that include workers generally focus on specific employment types (e.g., nurses, teachers, managers) within specific companies that ultimately limit generalizability both nationally and internationally. Given the vast individual differences in psychosocial contexts, it is also essential that sAA be investigated while controlling for numerous factors related to health behaviors, mental health, as well as work and non-work characteristics.
In the current comprehensive study, we examined diurnal variations in sAA concentrations over the course of two work-days in a sample of 395 workers from across 34 distinct workplaces. Our research objectives were to evaluate how sub-clinical psychiatric symptoms (e.g., psychological distress, depression, burnout), work characteristics (e.g., task design, demands, social relations, gratifications), and non-work characteristics (e.g., marital, parental, economic statuses, marital and parental stress, work-family conflicts) correlate to sAA time-points throughout the diurnal course while controlling for key covariates.
Section snippets
Participants
Data came from the SALVEO study conducted in Canada to evaluate the contribution of work, family, individual characteristics, and social networks vis-à-vis workers’ mental health problems (Marchand et al., 2015). This study also aimed to understand how work, non-work, and individual stressors ‘get under the skin and skull’ to promote variations in the stress hormone cortisol and how this can explain mental symptoms in workers. For the physiological part of this study, data were collected
Results
Table 1 reports raw sAA concentrations and each psychosocial determinant used in our study sample. Compared to men, women showed lower sAA concentrations 30 min after awakening and at 14h00. Women had higher level of psychological distress, depressive symptoms, and emotional exhaustion symptoms. They also self-reported lower skill utilisation, decision authority, physical demands, working hours, and irregular work schedule. Compared to men, women used more psychotropic drugs, they smoked less,
Discussion
The aim of this study was to identify which factors related to workers’ mental health, workplace, and non-work life would show the strongest correlations to diurnal sAA. We replicate and expand the findings of Nater et al. (2007) who showed a distinct diurnal profile of sAA in young university sample. We can confirm that this sAA pattern is characterized by sharp decreases +30 min after awakening followed by rises over the course of the day with only a small decrease thereafter before bedtime.
Conclusions
To reiterate, the inability to reliably measure SAM-axis activities in saliva means that it is limited to collection via invasive blood sampling or systemic output through urine (Nater et al., 2013). We provide a replication of a seminal report in this field (Nater et al., 2007) and show that several work stress characteristics are correlated with diurnal sAA. Similar to salivary cortisol, we cannot advance without taking basal functions into consideration even if our research interests center
Contributors
Alain Marchand, Pierre Durand and Sonia Lupien designed the study and wrote the protocol. Robert-Paul Juster managed the literature. Alain Marchand undertook the statistical analysis. Alain Marchand and Robert-Paul Juster wrote the first draft of the manuscript. All authors contributed to and have approved the final manuscript.
Role of funding source
The funding sources, the Canadian Health Research Institutes and the Fonds de la recherche en santé du Québec, played no role whatsoever in this research or in the choice for submission.
Conflict of interest statement
None declared.
Acknowledgements
This study was supported by the Canadian Health Research Institutes (Grant number: 200607MHF-164381-MHF-CFCA-155960 and the Fonds de la recherche en santé du Québec (Grant number: 13928). The authors also thank Manulife for their help in workplace recruitment, and Marie-Eve Blanc and Julie Dextras-Gauthier for the field work.
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