Over the past few decades, there has been a considerable increase in the involvement of men and women in exercise. Even athletes today undergo significantly greater levels of training compared to the sportsmen of a few decades ago[1]. An illustration of this is the extensive training regimen of the marathon runners, which can include over 200 kilometres of running every week. Although moderate exercise can have beneficial effects on health, including improved strength and cardiac output, very high intensity exercise can lead to some unwanted health problems. A physiological system that is very sensitive to external stresses like physical activity is the reproductive system and research has suggested that exercise can sometimes alter the dynamics of this endocrine system.
Experiments have been conducted to explore how male fertility may be influenced by physical training and this essay will explore how exercise may affect the reproductive function in men.
Testosterone is the steroid of primary importance in the male reproductive function and it is largely synthesised in the Leydig cells of the testes. In blood, approximately 98% of the testosterone is bound to carrier proteins like albumin and “sex hormone – binding protein” (SHBG) and the remaining 2%, called “free testosterone” (FT), is the physiologically active form. Thus, “total testosterone” (TT) includes both bound and free forms of the hormone[2].
The major reproductive role of testosterone involves facilitation of spermatogenesis. Once synthesised, the hormone diffuses to the Sertoli cells, where the levels must be maintained to ensure development of mature and viable sperm, essential for male fertility. Testosterone assists the functioning of male accessory sex glands, like prostate, seminal vesicles and epididymides. These glands play a critical role in sperm functioning and copulation[3]. Testosterone is also crucial in other aspects of male reproductive function, including libido and the ability to obtain and sustain erections.
Many studies have reported an association between testosterone and physical exercise. When reviewing such literature, the difference between resistance and endurance training should be appreciated.
Several studies have reported that resistance training can have acute effects on endocrine function. Baker et al.,[4] investigated testosterone responses immediately and 15 minutes after resistance exercise in young and older men. Although older subjects had lower testosterone than younger men, increased TT and FT levels were observed in all groups. Kraemer et al.,[5] also reported similar findings however, the results of the study should be interpreted with caution as confounding factors like sleep and smoking were not considered.
On the other hand, investigators have also recorded no elevation in testosterone levels post resistance exercise. Yarrow et al.[6] failed to detect any rises in androgen levels directly after physical exertion. Nindl et al.[7] monitored overnight blood testosterone in ten healthy men following exercise in the afternoon. As shown in figure 1, no significant increase in free or total testosterone could be observed for the first hour after exercise.
The findings disagree with the results of the aforementioned studies[4; 5] which reported a rise in testosterone immediately after exercise. Rest periods between sets of training may be a possible reason for the differing findings. However, Ahtiainen et al. [8] observed no differences in hormonal levels following exercise involving either short or long rest periods between sets. Thus, one might suggest total bout duration as a more plausible explanation since most studies reporting rises in androgen levels involved shorter training sessions of 90 minutes or less compared to the 2 hour spells of Nindl et al.[7]. Such rises in hormone levels may be due a reduction in plasma volume that occurs after exercise.
Overnight hourly blood samples collected by Nindl et al. suggested that resistance exercise could lead to suppression of testosterone as hormone levels were consistently lower in the exercise group. Figure 2 illustrates how testosterone concentrations varied all night.
It should be noted however that there is no statistically significant difference between testosterone levels of the two groups at any individual time point. Nevertheless, the results were supported by Kern et al.[9] who also reported falls in overnight TT following resistance exercise in the afternoon. On the other hand, a similar study by McMurray et al.[10] yielded conflicting results when increased testosterone levels were detected during the night after exercise. A possible explanation may be the work load that the subjects were put through during the experiments. For instance, the study of McMurray et al. involved lower total work of 18 sets compared to 50 sets in the investigation by Nindl et al. Thus, acute heavy resistance exercise may after all lead to an initial rise in testosterone followed by suppression of the hormone, an effect that may be sustained for as long as 13 hours[7].
Nindl et al. observed blunted luteinising hormone (LH) release and increased cortisol concentrations in subjects with suppressed testosterone. Therefore, inhibited hypothalamic – pituitary regulation of LH release may be responsible for the compromised hormone levels. It should be noted however that the subjects received the same amount of calories during the exercise and control conditions. This may have reduced LH secretion as decreased energy availability has been shown to lower LH levels[11]. Further evidence for a central mechanism causing testosterone suppression was provided by De Leo et al.[12], who found that injecting men with human chorionic gonadotrophin (hCG), a stimulator of testosterone secretion at Leydig cells, prevented fall in testosterone after acute resistance exercise. Elevated cortisol concentration may also have inhibited testosterone as previous research[13] has suggested such a role for the stress hormone.
Kraemer et al.[14] investigated the adaptations of the endocrine system to resistance exercise in young and old men. Figure 3 displays resting FT and TT levels at different points during the 10 weeks of exercise.
The resting TT concentrations were the same at the start and the end of training programme, thus showing that basal androgen levels are not affected by chronic resistance training. Staron et al.[15] however recorded higher basal total testosterone levels in exercising individuals after 5 weeks of intensive training compared to control subjects. Although the two groups in this study were matched for age and height, no information on potential confounding factors such as ethnicity, dietary intake and sleeping habits of the subjects was disclosed. However, the results of the study can not be ignored as the difference between the two groups only became significant after 5 weeks of exercise and remained so up to the end of the training programme. Nevertheless, other studies[16] have also failed to detect any rises in resting testosterone levels following continuous resistance exercise. FT also remained largely unchanged in both young and old subjects, except for a significant rise at 10 weeks, figure 3. This lead to the suggestion that resistance training may alter the ratio of the protein – bound and free forms of the androgen. However, the rise was only seen at 10 weeks and may have been more significant if the study was continued for longer and the effects observed over a longer period.
Acute resistance exercise does not appear to cause attenuated testosterone and reproductive function over a short period of time. Few studies following resistance trainers for longer periods have been conducted. Arce et al.[17] compared sedentary men to subjects with a history of resistance training and found that free and total testosterone levels were in fact lowered in the later. However, the investigation involved taking only one blood sample, which may have provided an imprecise estimate as androgen levels continuously fluctuate due to the daily circadian rhythm and LH pulsatility. Thus, future studies following weight lifters for a longer period of time, such as several months to years, may be conducted to help establish how resistance training may affect fertility in the long – term.
Many retrospective studies, using single blood sample measurements, have reported lower testosterone in subjects regularly involved with endurance training for as little as one year[18; 19]. The hormonal levels in these individuals have been reported to be up to 15 – 50 % lower than matched sedentary men. MacKelvie et al.[20] investigated testosterone levels in subjects with high and low training volumes. The results, summarised in figure 4, suggest a “dose – dependent” decrease in the hormonal levels following exercise.
Although taking single large values is not reliable and cannot be used to predict average hormone concentrations, such findings have been reproducible[19] and hence cannot be ignored. Other trials involving more than one measurement have also been conduced. McColl et al.[21] acquired blood samples of the subjects every 15 minutes for about 6 hours and reported similar results of lowered androgen levels.
Multiple blood sampling provides more accurate information and has been the protocol of choice in many prospective studies. Measurements obtained over weeks in subjects undertaking endurance training have not provided consistent results. Significant reductions in androgen levels have been reported in exercising subjects following months of regular training [22]. In contrast, Lucía et al.[23] did not detect significant alterations in resting testosterone levels in individuals exposed to endurance training. While the studies may be criticised for having been conducted for a short duration compared to retrospective trials, fundamental variations in protocols may in fact have been responsible for the apparent discrepancies. Examples include differences in the volume of exercise that the volunteers may have been exposed to and the training status of the subjects prior to the beginning of experiments. Furthermore, studies examining over trained athletes, who are involved in heavier than usual training, have also suggested a causative role for endurance exercise in testosterone suppression[3].
Several studies have been conducted in order to identify the mechanisms behind testosterone suppression. Such research has mainly attempted to elucidate whether the defect is “central”, in hypothalamus or pituitary, or “peripheral”, whereby the testes may be dysfunctional.
GnRH resistance at the anterior pituitary has been suggested as a possible cause of reduced androgen levels as studies involving GnRH injections have found reduced LH release in hypogonadal subjects[24]. The effect of endurance training on the amplitude and frequency of LH pulses has also been investigated. However the results so far have been mixed. Wheeler et al.[22] did not detect any changes in LH profile whereas McColl et al.[21] reported a general lowering of the LH levels. Although both studies had small sample sizes, one possible reason for the difference in results may be the higher work load in the study of McColl et al. Thus, it appears that LH levels become affected at very high training volumes.
Changes in sensitivity of the testes to alterations in LH have also been investigated. The results however, have been inconclusive. Some studies have reported lowered testicular testosterone production[25] while others have not detected any effect of exercise on androgen synthesis in the gonads[24].
Prolactin acts with LH at the testes to stimulate testosterone production. However, very high levels of the hormone can inhibit the functioning of any aspect of the hypothalamus – pituitary – gonadal axis. Basal prolactin levels are lowered in exercising men[26] and thus might contribute to reduced testosterone release.
Raised cortisol concentration has also been suggested as a possible cause of lowered testosterone levels in endurance – trained men as an inverse relationship between cortisol and testosterone has been noted. Daly et al.[27] found that a single burst of high – intensity exercise can result in a temporary increase in cortisol that may cause a fall in androgen levels.
Testosterone has several important functions in the body that can become affected if its circulating levels are reduced. Few studies have suggested that lowered androgen levels can actually compromise reproduction[28] and sperm quality by affecting the endocrinological processes dependent upon the hormone. Arce et al.[17] investigated effects of both resistance and endurance training in male subjects and found that although both groups had lower testosterone levels, semen characteristics, like sperm motility, were adversely affected only in the endurance trained group. On the other hand, Lucía et al.[23] found no significant effect of exercise on reproductive hormonal profile or semen quality in cyclists, marathon runners or tri – athletes. An explanation for the difference in findings may have been variations in the work load in the studies.
It should also be noted that the measurement of testosterone in assessing reproductive function has several criticisms. Much of the literature is complicated by the fact that researchers use different assays to measure testosterone levels and that a large number of confounders make the interpretation of testosterone difficult. Some of the confounding factors include the age, body mass, diet, smoking history, assay itself, measurements of both bound and free hormone, changes in plasma volume, alterations in clearance in different patients as well as the time of day when the sample is taken. Similarly, anabolic steroids, used widely by serious male body builders, would clearly be an independent and very significant confounder of interpretation of the data. Exercise studies in men and the suitability of comparisons within exercise groups and with controls depends on whether all of them are at the same level of fitness and whether the exercise they do is of the same quality, type or duration. Such factors further confound interpretation of data in males.
While many researchers have investigated the effect of low body weight on reproductive function in women[29], not many have comprehensively investigated a similar relationship in males. Animals under metabolic stress must invest energy in survival before reproduction, hence further studies evaluating reproductive function in low weight males are indicated.
Reduced libido has been reported in some exercise hypogonadal men, however a direct causal relationship has not been established. Other factors known to affect sex drive, such as psychological stress and fatigue, may also play be important[3].
Evidence is continuing to accumulate that exercise in men can have significant effects on major reproductive hormones and the hypothalamus – pituitary – gonadal axis. While studies investigating the impact of endurance training in men have suggested a fall in testosterone levels after continuous exercise, investigations evaluating resistance training have been inconclusive. However, lowered testosterone levels have been noted in resistance – trained men and future longitudinal studies lasting for at least 12 months should be conducted to establish the long – term effects of such training. It is unclear if the hormonal levels in exercise hypogonadal men are low enough to compromise reproduction. Nevertheless, there is evidence to suggest that excessive exercise can affect reproductive ability. Further research may be conducted to determine the importance of ethnicity and sports specificity.