Chronotype, social jetlag and sleep loss in relation to sex steroids
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.
Section snippets
Participants and procedures
In total, 239 subjects were analysed. There were 124 males aged 19–41 (24.73 ± 3.98 years) and 115 females aged 19–38 (23.14 ± 3.17 years). Using self-reporting, they were assessed as healthy and were not taking any medications or substances affecting hormone levels (including anabolic steroids and contraceptive pills) during the sampling period or in the three months prior to it. Additional exclusion criteria were pregnancy, lactation, hair inadequate for sampling (≤3 cm, dreadlocks, hair
Descriptive statistics
The descriptive statistics of the main study variables are displayed in Table 1. One can observe that there were only 47 female participants with testosterone data; in the remainder, testosterone levels were below the lower limit of sensitivity. The same was true for only 10 males. DHEA and progesterone data were available for almost all men and women (Table 1). The distribution of hormone levels was heavily right-skewed (skewness between 2.0 and 5.7) and using natural log transformation did
Discussion
The main study finding is that testosterone levels are higher in men with a later chronotype and lower levels of sleep loss, while higher levels of DHEA are associated with lower levels of sleep loss. In contrast, the analysed hormones in women appeared to be unrelated to sleep variables, but conclusively demonstrating this sex difference in the relationship between hormone levels and sleep variables would require a larger sample size.
The finding of higher testosterone levels in men with an
Conflict of interest
The authors report no conflicts of interest.
Acknowledgements
This work was supported by the National Science Center, Poland under grant 2012/07/E/HS6/0407. We are grateful to Prof. Clemens Kirschbaum for his help with the research.
References (49)
- et al.
Sleep deprivation lowers reactive aggression and testosterone in men
Biol. Psychol.
(2013) - et al.
Quantitative analysis of steroid hormones in human hair using a column-switching LC–APCI–MS/ MS assay
J. Chromatogr. B
(2013) - et al.
The neuroendocrine control of the circadian system: adolescent chronotype
Front. Neuroendocrinol.
(2012) Testosterone therapy for transgender men
Lancet Diabetes Endocrinol.
(2017)- et al.
Gonadectomy reveals sex differences in circadian rhythms and suprachiasmatic nucleus androgen receptors in mice
Horm. Behav.
(2008) Composite Scale of Morningness: psychometric properties, validity with Munich ChronoType Questionnaire and age/sex differences in Poland
Eur. Psychiatry
(2015)- et al.
Morningness-eveningness and sociosexuality: evening females are less restricted than morning ones
Pers. Individ. Dif.
(2014) Evening chronotype is associated with a more unrestricted sociosexuality in men and women
Pers. Individ. Dif.
(2018)- et al.
Eveningness is related to men’s mating success
Pers. Individ. Dif.
(2012) - et al.
Chronotype but not sleep length is related to salivary testosterone in young adult men
Psychoneuroendocrinology
(2012)
Breakpoints of time in bed, midpoint of sleep, and social jetlag from infancy to early adulthood
Sleep Med.
Beyond masculinity: testosterone, gender/sex, and human social behavior in a comparative context
Front. Neuroendocrinol.
Morningness-eveningness correlates with sleep time, quality, and hygiene in secondary school students – a multilevel analysis
Sleep Med.
Assay validation of hair androgens across the menstrual cycle
Psychoneuroendocrinology
Heavy testosterone use among bodybuilders: an uncommon cohort of illicit substance users
Mayo Clin Proc.
Natural sleep and its seasonal variations in three pre-industrial societies
Curr. Biol.
Circadian typology: a comprehensive review
Chronobiol. Int.
Circadian rhythmicity of cortisol and body temperature: morningness-eveningness effects
Chronobiol. Int.
Circadian misalignment and health
International review of psychiatry
The effect of diurnal variation on clinical measurement of serum testosterone and other sex hormone levels in men
J. Clin. Endocrinol. Metab.
Individual differences in the amount and timing of salivary melatonin secretion
PLoS One
Estradiol and progesterone modulate spontaneous sleep patterns and recovery from sleep deprivation in ovariectomized rats
Sleep
More than just sleeping in: a late timing of sleep is associated with health problems and unhealthy behaviours in adolescents
Sleep Med.
Data Analysis Using Regression and Multilevel/Hierarchical Models
Cited by (24)
Evening type negatively affects semen quality by deteriorating sperm morphology: Results from an infertility clinic
2023, European Journal of Obstetrics and Gynecology and Reproductive BiologySex differences in insomnia and risk for psychopathology in adolescence
2020, Current Opinion in PsychologyCitation Excerpt :That said, adult men have a stronger evening preference than women, a sex difference that diminishes with age [28•], suggesting circadian preference may play a limited role in the development of sex differences in insomnia. One recent study in adults suggests testosterone may be driving differences in eveningness while also offsetting the negative consequences of sleep loss that often accompany delayed sleep times [29•]. Prior research has focused on morningness/eveningness preference (i.e. an individual’s preferred time for performing daytime activities) rather than chronotype (sleep timing; [30]).