Abstract

 

Exercise has been proposed to increase serum testosterone concentrations. The analysis of existing literature demonstrates a large degree of variability in hormonal changes during exercise. In our manuscript, we summarized and reviewed the literature, and concluded that this variability can be explained by the effect of numerous factors, such as:

 

(a) the use of different types of exercise (e.g., endurance vs. resistance); 

(b) training intensity and/or duration of resting periods; 

(c) study populations (e.g., young vs. elderly; lean vs. obese; sedentary vs. athletes); and 

(d) the time point when serum testosterone was measured (e.g., during or immediately after vs. several minutes or hours after the exercise). 

 

Although exercise increases plasma testosterone concentrations, this effect depends on many factors, including the aforementioned ones. Future studies should focus on clarifying the metabolic and molecular mechanisms whereby exercise may affect serum testosterone concentrations in the short and long-terms, and furthermore, how this affects downstream mechanisms.

 

1. Introduction

 

Testosterone is the most potent naturally secreted steroid androgenic hormone. It is required for promotion of secondary male-sex characteristics, as well as muscle growth and neuromuscular adaptation . At the muscle level, testosterone is known to exert its anabolic effect via the following two mechanisms: (a) stimulating amino acid uptake and protein synthesis; and (b) inhibiting protein degradation by counteracting cortisol signalling. Age, higher body weight, poor nutritional status, stress, sleep deprivation, and alcohol consumption are known physiological factors leading to lower serum testosterone concentrations. Low plasma testosterone concentration is associated with fatigue, sexual dysfunction, depressed mood, difficulty concentrating, and hot flashes. If left untreated, patients may develop anemia, low bone mass density (i.e., osteoporosis), higher pro-atherogenic lipoprotein-associated changes, and muscle wasting. Thus, maintaining physiological levels of testosterone has significant health benefits.

 

Exercise has significant health-related benefits and it is proposed to increase plasma testosterone concentrations. However, analysis of the existing literature demonstrates a large degree of inter-individual and inter-study variability in hormonal changes during exercise. Age, body weight, and exercise type, together with exercise intensity, volume, and the involved muscle type, were studied as factors modulating these hormonal changes. This review article intends to clarify the factors that contribute to the variability in serum testosterone concentrations during exercise, and the underlying mechanisms. Part 1 will focus on the acute or immediate post-exercise changes in plasma testosterone concentrations, and Part 2 will discuss the changes in basal or resting plasma testosterone concentrations after completion of exercise protocols.

 

Part 1: Acute or Immediate Post-Exercise Testosterone Response

 

The changes in plasma testosterone concentrations during exercise may depend on multiple factors. Below we analyze the effect of the type of exercise (i.e., endurance or resistance), intensity, volume (i.e., the amount of muscle involved), obesity, and age on the acute or immediate post-exercise plasma testosterone changes.

 

(A) Endurance Exercise

 

Endurance or aerobic exercise refers to any type of cardiovascular conditioning where breathing and heart rates increase for a sustained period of time. Although different types of endurance exercises have been performed, running and ergometer cycling with different protocols were most often used. Regarding the study populations, the majority of research done using running as a study approach was conducted in elite athletes. The study subjects in ergometer cycling studies included elite athletes, moderately active people, sedentary people, and people with obesity. Some studies have been conducted in patients with type 2 diabetes or chronic heart failure; however, these will not be discussed within the scope of this blog.

 

Intensity refers to the load used for a given exercise. There appears to be a relative exercise intensity that must be reached in order to induce changes in serum testosterone concentrations. Jezova et al. [7] compared the plasma testosterone changes during ergometer cycling conducted at three different intensities: high, moderate, and low. Significant increases in the serum testosterone concentrations were seen only in the high intensity exercise group. Kraemer et al. [8] reported that, when the number of repetitions during exercise was kept constant, the intensity determined the degree of acute post-exercise increase in serum testosterone concentrations. In the study of Kraemer et al. [9], well-trained runners underwent a treadmill running exercise with stepwise increase in intensity. The first two steps were at intermittent intensity of 60% and 75% VO2max for 10 min each (i.e., step 1 and step 2, respectively). The last two steps were at high intensity: 90% and 100% VO2max for 5 and 2 min, respectively. T-Testo increased only after 5 min of exercise at 90% VO2 max (Basal vs. 90% VO2max: 18.2 ± 3.4 vs. 24.1 ± 4.6 nmol/L, p < 0.01), and remained elevated at 100% VO2, returning to baseline 1 h into recovery. 

 

These data support the notion that intensity is required to alter plasma testosterone concentrations. Galbo et al. [10] reported that, in young healthy men, a significant increase in T-Testo (~31%) was observed after 40 min of maximum intensity (reflected by the individual’s highest oxygen uptake) during exhaustive treadmill running. However, other factors may also affect this hormonal change. For example, in the above-mentioned study by Kraemer et al. [9] the increase in T-Testo was at 25 min after the start of the exercise, and thus it is possible that not only the intensity but also the duration of the exercise contributed to these results. Moreover, Maresh et al. [11] studied the same individuals under four different conditions: 70% and 85% VO2max intensities with pre-existing euhydration (i.e., EU70 and EU85) and hypohydration (i.e., H70 and H85). The results of their studies demonstrated that only EU85 resulted in increased T-Testo, suggesting that levels of both intensity as well as hydration are important in determining the outcomes of an exercise intervention. These results suggest that intensity among other factors can play a role in the immediate changes in serum testosterone concentrations with endurance exercise.

 

(B) Resistance Exercise

 

Resistance exercise, also known as strength and weight training, involves the voluntary activation of specific skeletal muscles against some form of external resistance. This external resistance is provided either by free weights, or a variety of exercise machines. Examples include heavy weightlifting, jumping, or sprinting.

 

Multiple studies have shown that resistance exercise can cause acute changes in serum testosterone concentrations. Circulating T-Testo has been shown to increase immediately after a bout of heavy resistance exercise and return to baseline or even decrease beyond that level within 30 min post-exercise. A major determinant for this increase in plasma testosterone concentrations is the muscle mass used. Involvement of a small muscle mass, even when vigorous resistance exercise is performed, does not elevate serum testosterone concentrations above resting levels. In a study of young untrained men, unilateral biceps curl exercise alone did not induce a significant change in post-exercise serum testosterone concentrations. However, the addition of bilateral knee extensions and leg press to the biceps curl protocol resulted in a significant elevation of the T-Testo. 

 

Shaner et al. [49] evaluated the hormonal changes with similar lower body multi-joint movement free (i.e., squats) or machine weight (i.e., leg press) exercises. Free weight exercises induced a greater increase in plasma testosterone concentrations than did the machine weight exercises. A potential explanation for this finding is that squatting requires balancing on two feet with substantial engagement of stabilizing and core musculature, such as the abdominals and back. Research on muscle activation has also shown that free weight exercise results in a greater muscle activation than machine exercise, likely by inducing a larger overall muscle mass involvement than similar machine-based weight exercises. These findings are supported by studies in junior Olympic-style weightlifters. 

 

Weightlifting, an example of resistance exercise involving large muscle mass, resulted in a significant elevation of T-Testo at 5 min after exercise (Basal vs. Post-exercise: 16.2 ± 6.2 vs. 21.4 ± 7.9 nmol/L). Another possible explanation for this hormonal change is the involvement of larger muscle mass, which, in addition to resistance, may be required to induce significant acute changes in plasma testosterone concentrations.

 

Not much has been reported about the effect of variable vs. constant exercise intensities on serum testosterone concentrations. However, Charro et al. [17] reported that, when the total volume of the load lifted is fixed, both the variable and constant exercise intensities produce similar acute changes in T-Testo in healthy young men. Similar effects were observed in healthy elderly men. Another study investigated the effect of a combination of exercise intensity, muscle volume (i.e., number of sets and repetition per a set), and the duration of the resting period between the sets on the acute hormonal variations. The results demonstrated that a combination of a moderate intensity, higher volume, and shorter resting periods between sets can acutely and significantly increase the post-exercise T-Testo. Interestingly, the testosterone concentrations remained elevated for 48 h after exercise cessation. Similar findings were also reported by Kreamer et al. [52] further confirming the importance of a combination of various factors to mount significant increases in the post-exercise concentrations of serum testosterone.

Lastly, Tremblay et al. [19] evaluated the effect of baseline physical activity status on hormonal changes after an exercise protocol. They studied sedentary, endurance trained, and resistance trained individuals performing endurance and resistance exercise sessions a week apart. T-Testo increased in all groups after both types of exercise sessions, but the increase was more pronounced after the resistance training. Comparing the three groups, resistance-trained individuals had a higher increase in T-Testo, especially after resistance exercise. In summary, resistance exercise appears to be a direct stimulant to testosterone production when sufficient muscle mass load is met, or when a moderate and higher exercise intensity is combined with larger muscle volume and shorter resting periods between the sets.

 

(C) Sustainability of Post-Exercise Elevated Levels of Testosterone, and Underlying Mechanisms

 

Both endurance and resistance exercise studies have demonstrated an increase in plasma testosterone concentrations upon exercising; however, these levels were not sustainable beyond several minutes. In the study by Manesh et al. [11], the increase in serum testosterone concentrations was not sustained at 20 min into the recovery. Daly et al. [20] likewise showed that, despite rapid increases in T-Testo after 30 min of endurance running, the levels significantly decreased 90 min into the recovery. Several studies have sought to investigate the potential underlying mechanisms that may explain these outcomes. Cumming et al. [6] showed that both testosterone and luteinizing hormone (LH) synchronously peaked at 20 min of progressive intensity exercise on an ergometer. However, a 45 min physiological lag between the LH pulse and testosterone production was well established, and thus LH stimulation may not be the mechanism responsible for the increase in plasma testosterone concentrations with exercise. 

 

Aerobic exercise can provide a large physiological stress to the body, resulting in a corresponding response of the neuro-endocrine system. This can be manifested by an initial rise in plasma testosterone concentrations secondary to a catecholamine surge and testicular stimulation, followed by increases in cortisol levels, a hormone that inhibits testosterone production. Others have demonstrated that an increase in serum testosterone concentrations is not secondary to increased production rate. Cadoux et al. [54] injected radiolabeled testosterone in men who underwent vigorous aerobic exercise for 50 min. The increase in plasma testosterone concentrations during the exercise was associated with a decrease in estimated hepatic plasma flow, metabolic clearance, and plasma volume. Moreover, infusion of lactate in rats, which is normally increased during exercise, was associated with a simultaneous increase in serum testosterone concentrations, particularly by increasing the testicular cAmp production. Therefore, even though aerobic exercise seems to induce the initial rise in T-Testo, this effect is not sustained due to several factors including (a) sympathetic nervous system stimulation and the subsequent inhibition of testosterone production; and (b) changes in the testosterone metabolism. 

 

In contrast, anaerobic exercise-induced stimulation of testosterone production was explained by the effect of the anaerobic glycolytic pathway on the release of gonadotropin releasing hormone (GnRH) and LH. The sustainability of exercise-induced elevation of testosterone concentrations may not vary between endurance and resistance exercise; however, the underlying mechanisms may be different.

 

(D) Obesity

 

So far, we have discussed works done in lean, young men; however, body weight and aging are inversely related to serum testosterone concentrations. In this and the following section, we will discuss how obesity and aging, respectively, affect the exercise-induced changes in testosterone concentrations. The underlying mechanisms of this relation include: (a) attenuated amplitude of LH pulses due to obesity-induced systemic inflammation; (b) increased aromatization of circulating testosterone in the adipose tissue; and (c) higher leptin production by fat cells which has been shown to disrupt testosterone production.

 

Studies investigating the effect of exercise on serum testosterone concentrations in overweight and obese individuals also show conflicting results. Rubin et al. [21] compared resistance exercise-associated serum testosterone changes in physically active lean vs. obese men. Although T-Testo was comparable between obese and lean individuals immediately after exercise, the levels were lower in the obese men (lean vs. obese: 20 vs. 8 nmol/L, p < 0.01) at 30 min into recovery. Despite the initially similar change in both groups, the baseline and integrated concentrations during recovery appeared to be inversely associated with the degree of adiposity. Sheikholeslami-Vatani et al. [22] investigated the acute effect of different resistance exercise orders on serum testosterone concentrations in untrained normal weight and obese men. Although in both groups T-Testo increased acutely post exercise, the increase was higher in the lean individuals, suggesting an obesity-associated blunting in hormonal changes with exercise. 

 

Another study by Velasco-Orjuela et al. [23] evaluated the acute effect of high-intensity, resistance, or combined exercise protocols on T-Testo in inactive overweight men. Surprisingly, none of the exercise protocols affected the T-Testo. The authors hypothesized that obesity-associated endothelial dysfunction and impaired vasodilatation in the testes may be, at least partially, responsible for the altered overall endocrine response in this population. Thus, whether exercise can still potentiate testosterone spikes in overweight and obese individuals is uncertain; and if present, they seem to be inferior to those seen in lean/normal weight men.

 

(E) Age

 

Aging is associated with declining levels of serum testosterone concentrations in men. This is secondary to the decreasing capacity of aging Leydig cells to produce testosterone in response to LH stimulation. Low plasma testosterone concentrations are associated with a number of adverse health consequences including loss of muscle mass, increased fat mass, reduced physical performance, and increased cardiovascular disease risk. The effect of exercise on serum testosterone concentrations in older men is not clearly understood. Studies in older participants refer to studies in men with an average age of 60 ± 5 years. 

 

Zmuda et al. [24] examined the acute effect of moderate physical activity with increasing intensity on T-Testo in elderly (70 ± 4 years), sedentary men. Levels acutely increased during exercise and peaked at higher intensities (basal vs. post-exercise: 11.2 vs. 16 nmol/L, p < 0.01); however, the levels returned to baseline at 60 min into recovery. Kraemer et al. [25] examined the acute effect of heavy resistance exercise on T-Testo in young (29.8 ± 5.3 years), and older (62 ± 3.2 years) men. Both groups showed significant increases in serum testosterone concentrations immediately and 5, 10, and 15 min post-exercise. However, the magnitude of increase was higher in the younger population. Another study evaluating the effect of aging on changes in serum testosterone concentrations included three groups of healthy untrained men: young (20–26 years), middle aged (33–58 years), and older (59–72 years), who performed one session of resistance training. All three groups exhibited an increase in T-Testo post exercise, with middle aged and older men showing similar relative testosterone concentration changes to younger men. Levels returned to baseline 15 min after exercise cessation in all groups. 

 

Arazi et al. [27] studied young and middle-aged men who underwent an 8-week-long progressive resistance training program. The serum testosterone concentrations were measured at four separate time points: (1) before any exercise was conducted (baseline); (2) immediately after one bout of exercise, but before the training started (i.e., pre-training immediate; I-preT); (3) immediately after completion of 8-week-long training (i.e., post-training immediate; I-postT); and (4) basal or resting post-training (PT). Compared to the baseline levels, the T-Testo concentrations were increased at I-preT in middle-aged men only. In the same group, the I-postT T-Testo were also increased and remained elevated at 30 min into the recovery. These I-postT values were also higher than the I-preT values in this group. 

 

In young men, the plasma testosterone concentrations were higher at I-preT, I-postT, and 30 min into the recovery, when compared to those of the middle-aged men. In this study, no changes were observed in the resting concentrations of serum testosterone in middle-aged men, but resting testosterone concentrations increased in young men post-training. All the analyzed studies confirmed that middle-aged and older men still mount an elevation in plasma testosterone concentrations acutely after physical activity, despite age-related hormonal declines. However, the magnitude of increase can be lower than that seen in younger men.

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Reference : Functional Morphology and Kinesiology