Chronotype, social jetlag and sleep loss in relation to sex steroids

Highlights

• In men, evening chronotype was related to higher testosterone levels assessed from hair.

• In men, sleep loss was related to lower testosterone and DHEA levels.

• In women, no links between chronotype and hair testosterone, DHEA, or progesterone.

Abstract

Chronotype describes preferences for functioning at different times of the day. At the onset of puberty, a sharp shift towards eveningness starts, reaching its peak at the end of adolescence, followed by a steady shift towards morningness as the ageing process occurs. Puberty is also the time when sex differences appear, with men being more inclined to eveningness than women, which diminishes around menopause; the described pattern of changes in chronotype leads to the hypothesis that reproductive hormones may be the driving factor behind this conversion. In the present study, we aimed to verify this hypothesis by analysing participants’ testosterone, progesterone and dehydroepiandrosterone (DHEA) levels in the three months, as indicated by assays in 3-cm hair strands from the scalp. Participants (n = 239) of both sexes also completed the Munich Chronotype Questionnaire. The results showed that in men higher testosterone levels were related to eveningness and less sleep loss, whereas greater sleep loss was associated with lower levels of DHEA. In women, no associations between chronotype and levels of the analysed hormones were found. The results support the hypothesis that testosterone levels play a role in shaping eveningness. We further hypothesised that a possible cause of the higher secretion level of testosterone in men with the evening chronotype is a mechanism to offset the negative consequences of sleep loss.

Introduction

Chronotype, also called morningness-eveningness or circadian typology (Adan et al., 2012), is an individual characteristic describing preferences for functioning at different times of the day and sleep-wake timing. Although it is a dimensional variable, researchers often use categories (e.g. evening types, morning types) to facilitate communication. Evening types, in contrast to morning types, exhibit a shift towards later hours in circadian rhythms, such as sleep-wake rhythms or the secretion of hormones such as cortisol (Bailey and Heitkemper, 2001) and melatonin (Burgess and Fogg, 2008).

The evening chronotype has been related to a number of adverse health outcomes, including both mental (Jankowski and Dmitrzak-Węglarz, 2017; Taylor and Hasler, 2018) and physical health problems (Gariépy et al., 2018). These adverse outcomes are often claimed to be a side effect of the conflict between biologically driven preferences for late sleep timing and morning activities imposed by society (work, school, family care, etc.), a phenomenon called social jetlag (Wittmann et al., 2006). Aside from circadian misalignment (misalignment of sleep to the biological night; Baron and Reid, 2014), the evening chronotype can also lead to sleep loss if an individual attempts to sleep according to their biological night but needs to wake up early to fulfil morning social obligations, like the start of work or school (Jankowski, 2017; Vollmer et al., 2017).

Amongst the biological factors related to chronotypes, age demonstrates a robust effect, which is further moderated by sex (Jankowski, 2015; Roenneberg et al., 2004). In general, morningness dominates during childhood, and sex differences are not apparent (Randler et al., 2017, 2019). At the onset of puberty, a sharp shift towards eveningness begins and reaches its peak at around 18–21 years of age (Jankowski, 2015; Roenneberg et al., 2004). Afterwards, a mild shift to morningness continues with ageing. Puberty is also the time when sex differences appear, with men being more inclined to eveningness than women, which diminishes around menopause (Roenneberg et al., 2004).

The described pattern of changes in chronotype, as well as its existence in animals, has led researchers to hypothesise that reproductive hormones may be the driving factor behind chronotype (Hagenauer and Lee, 2012; Mong et al., 2011). Particular interest was paid to androgen hormones, based on the observation that gonadectomies in mice diminished evening activity in males, but not in females, and that androgen supplementation restored the sex difference in daily rhythmicity (Iwahana et al., 2008). Increasing testosterone was postulated to lead to later bedtimes in humans (Wittert, 2014). This hypothesis, linking higher testosterone with eveningness, has not been extensively tested. Randler et al. (2012b) illustrated that eveningness is related to salivary testosterone levels sampled during the morning hours (8:00–9:00). This method, however, can confound the results because different chronotypes may be tested at different time intervals from their morning testosterone peak (Brambilla et al., 2009; Lacerda et al., 1973). On the other hand, Maestripieri (2014) found no association between salivary testosterone and chronotype tested in the afternoon in men or women (13:30 – 17:00).

Moreover, social jetlag and sleep loss are salient variables that should also be considered in the context of an association between chronotypes and sex hormones. It has been suggested that social jetlag has adverse endocrine effects (Rutters et al., 2014), but no associations with sex hormones have been reported so far. On the other hand, associations between sleep loss in humans and the levels of numerous hormones have been documented (Kim et al., 2015; Van Cauter et al., 2005). Sleep loss has been related to diminished morning testosterone levels in men (Penev, 2007), and this effect was particularly prominent if sleep loss occurred in the second half of the night (Schmid et al., 2012). When both sexes were analysed, the effect of sleep loss on testosterone levels appeared in men but not in women (Cote et al., 2013). Therefore, these two sleep variables can potentially confound links between chronotype and hormone levels.

In the present study, we aimed to clarify and extend previous findings by testing long-term testosterone levels for the first time, taking advantage of testing hair (as opposed to testing saliva), according to chronotype. Furthermore, we also aimed to analyse two other sex hormones for the first time – dehydroepiandrosterone (DHEA) and progesterone in the context of chronotype. Finally, we aimed to test two salient chronotype-related sleep variables concurrently – social jetlag and sleep loss – in the context of the abovementioned hormones and to consider the associations not only in men but also in women.