Interactions of cortisol, testosterone, and resistance

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Interactions of cortisol, testosterone, and resistance training: Influence of circadian rhythms Article in Chronobiology International · June 2010 DOI: 10.3109/07420521003778773 · Source: PubMed

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Chronobiology International, 27(4): 675–705, (2010) Copyright © Informa UK Ltd. ISSN 0742-0528 print/1525-6073 online DOI: 10.3109/07420521003778773

REVIEW ARTICLE INTERACTIONS OF CORTISOL, TESTOSTERONE, AND RESISTANCE TRAINING: INFLUENCE OF CIRCADIAN RHYTHMS

Chronobiol Int Downloaded from informahealthcare.com by 92.233.112.172 on 06/19/10 For personal use only.

Lawrence D. Hayes,1 Gordon F. Bickerstaff,2 and Julien S. Baker1 1

Department of Exercise and Sports Science Department of Biological Sciences, University of the West of Scotland, Hamilton, Scotland, UK 2

Diurnal variation of sports performance usually peaks in the late afternoon, coinciding with increased body temperature. This circadian pattern of performance may be explained by the effect of increased core temperature on peripheral mechanisms, as neural drive does not appear to exhibit nycthemeral variation. This typical diurnal regularity has been reported in a variety of physical activities spanning the energy systems, from Adenosine triphosphate-phosphocreatine (ATP-PC) to anaerobic and aerobic metabolism, and is evident across all muscle contractions (eccentric, isometric, concentric) in a large number of muscle groups. Increased nerve conduction velocity, joint suppleness, increased muscular blood flow, improvements of glycogenolysis and glycolysis, increased environmental temperature, and preferential meteorological conditions may all contribute to diurnal variation in physical performance. However, the diurnal variation in strength performance can be blunted by a repeated-morning resistance training protocol. Optimal adaptations to resistance training (muscle hypertrophy and strength increases) also seem to occur in the late afternoon, which is interesting, since cortisol and, particularly, testosterone (T) concentrations are higher in the morning. T has repeatedly been linked with resistance training adaptation, and higher concentrations appear preferential. This has been determined by suppression of endogenous production and exogenous supplementation. However, the cortisol (C)/T ratio may indicate the catabolic/anabolic environment of an organism due to their roles in protein degradation and protein synthesis, respectively. The morning elevated T level (seen as beneficial to achieve muscle hypertrophy) may be counteracted by the morning elevated C level and, therefore, protein degradation. Although T levels are higher in the morning, an increased resistance exercise–induced T response has been found in the late afternoon, suggesting greater responsiveness of the hypothalamo-pituitary-testicular axis then. Individual responsiveness has also been observed, with some participants experiencing greater hypertrophy and strength increases in response to strength protocols, whereas others respond preferentially to power, hypertrophy, or strength endurance Submitted December 14, 2009, Returned for revision January 12, 2010, Accepted February 25, 2010 Address correspondence to Lawrence Hayes, Department of Exercise and Sports Science, University of the West of Scotland, Almada Street, Hamilton, ML3 0JB, UK. E-mail: Lawrence.hayes@ uws.ac.uk

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L. D. Hayes et al. protocols dependent on which protocol elicited the greatest T response. It appears that physical performance is dependent on a number of endogenous time-dependent factors, which may be masked or confounded by exogenous circadian factors. Strength performance without time-of-day–specific training seems to elicit the typical diurnal pattern, as does resistance training adaptations. The implications for this are (a) athletes are advised to coincide training times with performance times, and (b) individuals may experience greater hypertrophy and strength gains when resistance training protocols are designed dependent on individual T response. (Author correspondence: [email protected])


Keywords Circadian rhythms; Cortisol; Resistance training; Strength; Testosterone

CIRCADIAN RHYTHMS Circadian rhythms are biological variations that repeat themselves with periodicity of ∼24 h (Reilly & Waterhouse, 2009). Most mammalian circadian rhythms originate from the endogenous pacemaker in the suprachiasmatic nucleus (SCN) (Figure 1) in the anterior hypothalamus (Sujino et al., 2007; Duguay & Cermakian, 2009). Neural and humoral outputs from the SCN communicate with other centers in the hypothalamus and endocrine system to drive a multitude of behavioral and physiological rhythms. The SCN is comprised of thousands of cells, each with an endogenous molecular oscillator (Herzog et al., 1998). Reppert and Weaver (2002) reported the core SCN oscillator is comprised of interacting positive and negative transcription/translation feedback loops. Although each cell exhibits a different circadian rhythm (Honma et al., 1998), these are synchronized to deliver a circadian rhythm with a single period. Peripheral organs and tissues also demonstrate circadian

FIGURE 1 The location of the SCN and an overview of some biochemical and physiological events associated with circadian rhythms.


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rhythmicity (Yamazaki et al., 2000; Dardente & Cermakian et al., 2007). Others have suggested that clock genes in peripheral organs show nycthemeral variance similar to the SCN (Reppert & Weaver, 2002; Duguay & Cermakian, 2009). However, the mechanism by which these oscillations in peripheral organs are conducted by the SCN has not fully been investigated. It has previously been reported that a lesion of the SCN eradicates nycthemeral rhythmicity of physiological events and behaviors (Bethea & Neil, 1980) and that transplants of a SCN have restored circadian behavior (Sujino et al., 2003, 2007). Special chronobiological techniques have been applied to differentiate between endogenous circadian rhythms from cyclic and noncyclic environmental factors that might mask or confound their expression (e.g., activity, posture, energy intake, chronotype, sleep, ambient temperature, light, and season) (Reilly & Waterhouse, 2009; Reilly 1990; Winget et al., 1985). These “unmasking” techniques have included forced desynchrony (Dijk et al., 1992), constant routine (Duffy & Dijk, 2002), ultra-short sleep-wake protocols (Kline et al., 2007), and data purification (Waterhouse et al., 1999). Although they may aid us in defining the underlying mechanisms by which circadian rhythms occur, their use in applied sports science is impractical and unnecessary, as rarely would athletes purposely desynchronize or disrupt their sleep because it would likely have a deleterious effect on performance. However, they are useful to explore mechanisms and to simulate the effect of jet-lag on performance (Reilly & Waterhouse, 2009). CORTISOL AND TESTOSTERONE Almost all biochemical and physiological parameters are circadian rhythmic (Reilly et al., 1997). The circadian pacemaker regulates the prominent 24-h variation in biological functions, including the synthesis and release of testosterone (T) and cortisol (C) (Mrosovsky, 2003). T is a steroid hormone secreted from the Leydig cells of the testes under hypothalamic and pituitary control defining the hypothalamo-pituitarytesticular (HPT) axis (Figure 2). Serum T is mainly bound to the sex hormone–binding globlin (SHBG) and albumin. The free fraction (0.5–2%) of total serum T is believed to be the biologically active fraction and, therefore, a better marker of serum T concentrations than total T. T bound to SHBG is not available for uptake by most tissues, whereas T bound to albumin is thought to have access to target tissues because albumin-bound T dissociates rapidly (Vermeulen et al., 1999). T has both anabolic and anticatabolic effects on muscle tissue (Hedge et al., 1987) as well as associated effects on sexual maturation. The direct action of T on muscle is supported by the presence of cytoplasmic receptors for it in skeletal muscle homogenates (Florini, 1987). C is a steroid hormone released by the adrenocortical glands under hypothalamic and pituitary


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FIGURE 2 The HPT axis in control of plasma testosterone (T) levels. Dotted lines represent feedback inhibition by free testosterone to modulate T production. Note that higher brain centers associated with circadian rhythms influence the hypothalamus and subsequent production of GnRH (GnRH = gonadotrophin-releasing hormone; FSH = follicle-stimulating hormone; LH = lutenizing hormone).

control defining the hypothalamo-pituitary-adrenal (HPA) axis (Figure 3). The HPA axis plays a vital role in the adaptation to endurance training and acute response to exercise. C exerts catabolic effects on muscle tissue (Florini, 1987) and has important metabolic functions, such as influencing the metabolism of lipids, proteins, and glucose. It increases the mobilization of fatty acids from fat reserves to active tissue and raises blood glucose (de Souza Vale et al., 2009). Intense physical exercise increases C (Timon et al., 2009), which may inhibit protein synthesis with consequent increase in muscle mass by its catabolic effect (de Souza Vale et al., 2009). The balance between these anabolic/catabolic hormones is often used as an indicator of overtraining (Duclos, 2008). Skeletal muscle can be regulated through changes in either protein synthesis or degradation. Ultimately, muscle mass is the net result of these protein turnover processes. Therefore, any disparity between the rate of protein synthesis and degradation will lead to a change in the size



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FIGURE 3 The HPA axis in the control of plasma cortisol (C). Dotted lines represent feedback inhibition by free C to modulate the level of C production. Note that higher brain centers associated with circadian rhythms influence the hypothalamus and subsequent production of CRH (CRH = corticotrophin-releasing hormone; ACTH = adrenocorticotrophic hormone).

of the protein tissue reserve (Millward et al., 1975). Since C primarily affects protein degradation (Kuoppasalmi & Adlercreutz, 1985), a decrease in C is expected to enhance skeletal muscle hypertrophy through reduction in protein degradation rather than increase in protein synthesis as the primary mechanism (McMurray et al., 1995).

CORTISOL AND TESTOSTERONE RHYTHMICITY Rhythms in the release of hormones constitute a common feature of almost all endocrine systems, with periodicities varying from minutes to a few hours (growth hormone [GH], lutinizing hormone [LH]), 24 h (C), week, month (hormones of the menstrual cycle), or months (e.g., seasonal variability in C; Hansen et al., 2001a; Persson et al., 2008; Reinberg et al., 1978). Both T and C exhibit circadian rhythmicity with peak concentrations in the morning, around the commencement of


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diurnal activity, and reduced concentrations in the evening and overnight (Touitou & Haus, 2000). The morning rise in C accelerates metabolism (Florini, 1987) and stimulates gluconeogenesis and proteolytic activity, resulting in increased skeletal protein turnover (Dinneen et al., 1993). The increase in T at this time may be an attempt to counteract the stimulatory effect of C on skeletal protein degradation (Kraemer, 1988). Differences between persons in circadian synchronization may be related to several factors, most notably the light-dark cycle (Aschoff, 1963), nonphotic entrainment (Klerman et al., 1998), social activity, living habits (Zhao et al., 2003; Bougard et al., 2009), and work schedule effects (Folkard, 2008; Reinberg & Ashkenazi, 2008). Hormonal response to dietary intake has been rarely documented despite evidence indicating that specific nutrients may have the potential to alter the regulation and metabolism of T and C (Volek et al., 1997). Previous studies have demonstrated that steroid hormone concentrations are subject to dietary regulation (Anderson et al., 1987; Raben et al., 1992). For example, individuals consuming a diet containing ∼20% fat, compared with a diet containing ∼40% fat, exhibit significantly lower concentrations of T (Goldin et al., 1994). Also, replacement of dietary carbohydrate with protein has been shown to decrease T concentrations (Anderson et al., 1987). These studies indicate that the energy supplied by the different macronutrients exerts significant influence on T concentrations. However, the majority of studies measuring endocrine response to food ingestion (Volek et al., 1997; Raben et al., 1992) have only documented acute responses (1–3 h) and have not concerned C. Beaven et al. (2008c) investigated the effects of caffeine supplementation on the C and T response to resistance exercise, finding a diurnal decline in T and an increase in C. Conversely, caffeine increased the exercise-induced T response to resistance exercise, and at the highest caffeine dose C continued to increase post-exercise. Although the study reported a potentially important anabolic benefit of caffeine supplementation via increase in T, it was tempered by a concomitant increase in C, raising questions about possible functional gains. Rose et al. (1972) were some of the initial investigators to document the episodic release of C and T over the day. Although C samples were only collected every 90 min, peaks in the early morning and at 12:00 and 16:00 h were clearly evident in diurnally active subjects. These observations are consistent with those of Krieger et al. (1971), who reported similar patterns only 12 months before. Concentrations of T were shown to be less erratic than those of C, with no “peaks” documented as such. Although consistent, the magnitude of the diurnal change in T levels was significantly less than C. On average, in diurnally active persons T concentration declined 42% from 06:00 h (awakening) to 23:00 h, compared with 92% for C during this span. More recently, Zhao et al. (2003)


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investigated similar parameters in Chinese men 30–60 yrs of age, reporting peak C concentrations between 04:00 and 06:00 h and a trough in the evening, between 18:00 and 24:00 h. Slightly different amplitudes were found between studies (92% in Krieger et al. [1971] versus 60% in Zhao et al. [2003] when referenced to the 24-h mean), but this may be attributed to the different statistical analysis used in the studies. Slag et al. (1981) reported similar diurnal variations in C and agreeing with Krieger et al. (1971), suggesting peaks around 12:00 and 16:00 h. However, these times coincided with meals, and a fasted group in the Slag et al. (1981) paper showed a blunted C response at these times. RHYTHMICITY OF STRENGTH PERFORMANCE The circadian rhythm of core temperature is often used as a marker of the “body clock” due to its strong endogenous component. Many measures of physical performance display circadian rhythms closely in phase with the temporal variation in body temperature, which peaks in the early evening in diurnally active individuals (Drust et al., 2005; Edwards & Waterhouse, 2008). Indeed, an increase by 1°C in core temperature could act as a warm up (Reilly et al., 1997), increasing nerve conduction velocity (Ferrario et al., 1980), joint suppleness (Fatthalah et al., 1995), and muscle strength (Reilly & Waterhouse, 2009). Increased body temperature causes vasodilation, which may increase blood supply to exercising musculature (Karvonen, 1977), thereby improving glycogenolysis and glycolysis (Febbraio et al., 1998). Therefore, increased core temperature due to circadian patterns would facilitate enhancement of the neuromuscular and metabolic systems (Souissi et al., 2004; Racinais et al., 2005; Reilly & Brooks, 1990; Jasper et al., 2009). Indirect evidence of circadian rhythms on sports performance comes from examination of the times-of-day when athletes perform best in actual sports. This type of examination clearly has high environmental validity, although it may be affected by a number of confounding variables. Previous analysis of world records seem to indicate a circadian dependency (Atkinson & Reilly, 1999), with records most commonly broken by athletes competing in the early evening, the time-of-day when body temperature is highest. However, these data need to be interpreted with caution, since many socioeconomic factors demand finals of major track and field events to be staged in the afternoon or evening for television or attendance purposes. The lack of continuity is also a problem concerning field-based investigations. Furthermore, environmental temperature may be higher in the evening, especially in the summer. Diurnal variation in meteorological conditions may affect performance in cycling or field sports where aerodynamics is of importance (Youngstedt & O’Connor, 1999). Moreover, time of morning awakening


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and whether or not meals are consumed, such as a breakfast, might also affect performance in the morning and perhaps later in the day (Bougard et al., 2009). It is sometimes possible to control for the evening-bias in event scheduling. For instance, time trials in competitive cycling are evenly distributed throughout the daylight hours; an analysis of such data by Atkinson (1994) confirmed better performance in the evening for a 16-km time trial. Tight standardization of environmental factors can be achieved in swimming, where water temperature is held constant throughout the day. Kline et al. (2007) conducted a highly internally valid investigation, eliminating a number of exogenous drivers of rhythmicity, such as the light-dark and sleep-wake cycles. Participants were subjected to an 180min ultra-short sleep-wake schedule involving 120 min awake alternating with 60 min of attempted sleep throughout a span of 50–55 h while residing in a constant light and temperature facility. Participants completed a 200-m freestyle swim trial every 9 h (every third ultra-short sleep-wake cycle). Swim performance was impaired from 02:00 to 08:00 h, with peak performance occurring at 23:00 h, in agreement with findings of others describing swim performance (Deschodt & Arsac, 2004). However, most physical performance measures have an acrophase (peak time) earlier than 23:00 h (e.g., Giacomoni et al., 2005; Jasper et al., 2009; Souissi et al., 2008). When numerous measures have been obtained throughout the 24 h, the acrophase of performance usually occurs between ∼15:30 and 20:30 h, with the amplitude of variation ranging from 2% to 11% of the daily mean (Reilly et al., 2007). However, this depends on the variable tested and the participant’s age (Myers & Badia, 1995), training status (Härmä et al., 1982), and chronotype (Drust et al., 2005; Reilly, 1990). Commonly investigated measures include muscle strength (Sedliak et al., 2008), power (Reilly & Down, 1992; Souissi et al., 2008), and flexibility (Gifford, 1987). Muscular strength (Guette et al., 2005; Martin et al., 1999; Sedliak et al., 2008) and anaerobic power, as measured by forcevelocity (Bernard et al., 1998; Souissi et al., 2004) and 30-s Wingate (Souissi et al., 2004, 2008; Reilly & Down 1992) tests, are subject to circadian rhythmicity; however, it is not clear if aerobic performance is subject to circadian influence. Some authors (Bessot et al., 2006; Hill 1996; Nicolas et al., 2008b; Brisswalter et al., 2007), but not all (Deschenes et al., 1998b; Reilly & Down, 1992), have reported evidence for circadian fluctuations in endurance tests. Diurnal variations have been shown to occur across the ATP-PC (Reilly et al., 2007; Sedliak et al., 2008), anaerobic (Souissi et al., 2002, 2004; Reilly & Down, 1992; Lericollais et al., 2009), and aerobic (Kline et al., 2007; Nicolas et al., 2008b) energy systems. With regards to strength performance and resistance exercise–induced responses, eccentric (Miles et al., 2008), isometric (Guette et al.,



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2005; Sedliak et al., 2008), and concentric (Sedliak et al., 2008) contractions have all been shown to exhibit a circadian pattern. Bessott et al. (2006) found no diurnal variation in pedal rate for maximum power production, contradicting the findings of Moussay et al. (2002). However, Moussay and colleagues (2002) only reported diurnal variation in pedal rate for all power levels