Exercise Hypogonadal Males Basal Hormonal Responses

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Retrospective comparative studies examining isolated, single blood samples have found lower testosterone levels in chronically endurance-trained males. The subjects in those studies were typically distance runners who had been involved with the physical-training aspects of their sport for 1 to 15 yr. In those studies, total and free-testosterone levels in the endurance-trained men were only 60-85% of the levels of matched sedentary controls (7,35,54,56-58). Many of the early studies reporting this finding suffered from small sample sizes. However, recent work with larger numbers of subjects has substantiated the findings (59,60). These low resting testosterone levels are highly reproducible and are not just an aberration of the athletes' seasonal training regime (60).

Prospective studies have also been conducted in which blood samples have been collected for weeks or months during endurance training regimens. Findings thus far from such studies have been inconsistent. Some reports reveal significant reductions (decreases of 20-40%) in resting testosterone levels after 1 to 6 mo of intensive training (60-64), whereas other studies have found no significant change in resting testosterone after 2 to 9 mo of training (65-70). Differences in the initial training status of the subjects or the training dosage administered within these studies may explain the discrepant findings. It is also possible that some prospective studies were too brief compared to the retrospective studies in which the men with low testosterone levels had been training for many years.

Exercise-hypogonadal men also display other reproductive hormonal abnormalities in addition to low basal testosterone levels. The most frequently reported finding involves no significant elevation in resting LH to correspond with the decrease in testosterone (i.e., hypogonadotrophic-hypogonadism) (35,58,71). Additionally, resting PRL levels may be decreased (35,58). The findings of altered LH and PRL levels at rest in exercise-hypogonadal men have been interpreted by some researchers to indicate dysfunction of the hypothalamic-pituitary-testicular axis. These findings for LH and PRL have been reported in several retrospective and prospective based studies (7,35,56,58,71,72).

There are several retrospective investigations in which basal, resting blood samples were collected (i.e., serially every 20 or 30 min for 4- to 8-h periods) in exercise-hypogonadal men and in sedentary control men. Results are similar to those of the isolated-sampling studies: resting total and free-testosterone concentrations of the exercise-trained subjects were typically only 60-80% of those found in control men (56,73). As with isolated blood sampling studies, resting LH levels were not significantly elevated. Again, these findings have been cited to represent a possible dysfunction in the hypothalamic-pituitary-testicular axis.

To date, the hormonal findings described above in this section have primarily been found in endurance athletes (i.e., distance runners and triathletes). However, it is highly unlikely that these hormonal alterations are limited to this athletic-exercise group alone. The prevalence of these phenomena in endurance athletes most likely represents the tendency of researchers to focus on this group, following the initial lead of early studies conducted in the 1980s. As scientists studying exercise expand their endocrino-logical studies to include other athletic groups involved with endurance training, it is highly likely that comparable data will come forward.

Testosterone Levels

Fig. 2. Comparison of the overall percent change in hormone levels of exercise-hypogonadal men (EHM) when compared to normal, untrained men. Comparison is for a 4-h (overall mean response) period after a maximal exercise bout vs a 4-h period of rest in both groups of men. T, testosterone*; LH, lutropin*; PRL, prolactin*; C, cortisol; E2, estradiol. The * denotes significance differences between the groups (p < 0.05). The data are based on the findings in ref. 35.

Fig. 2. Comparison of the overall percent change in hormone levels of exercise-hypogonadal men (EHM) when compared to normal, untrained men. Comparison is for a 4-h (overall mean response) period after a maximal exercise bout vs a 4-h period of rest in both groups of men. T, testosterone*; LH, lutropin*; PRL, prolactin*; C, cortisol; E2, estradiol. The * denotes significance differences between the groups (p < 0.05). The data are based on the findings in ref. 35.

Exercise Responses—Testosterone, Gonadotropins, and Other Hormones

Few studies have compared how exercise-hypogonadal men and normal untrained men respond differently to exercise. Evidence suggests that in response to a single exercise bout (maximal or submaximal) the direction of the hormonal changes is similar. Testosterone and PRL are increased, whereas the gonadotropin responses are variable in both groups of men (35,72). However, in the recovery from exercise, the two groups differ. In normal men, the reproductive hormones display some degree of negative feedback "rebound" inhibition during the hours of recovery after exercise (35,53). In exercise-hypogonadal men, this rebound effect is diminished or eliminated. Currently, it is unclear whether this represents an adjustment in regulatory aspects of the controlling axis or a temporal displacement shift in the axis of the exercise-hypogo-nadal men. Obviously, the resting basal levels of the hormones in each of these groups are different; therefore, relative changes in response to exercise must be compared. Figure 2 displays recovery hormonal responses of exercise-hypogonadal men and normal men as relative change after an identical exercise bout (35).

Mechanistic Studies

Some studies have attempted to elucidate the mechanism for the proposed hypothal-amic-pituitary-testicular axis dysfunction in exercise-hypogonadal men. These studies have focused on examining whether the dysfunction is central (hypothalamic or pituitary) or peripheral (testicular) in nature.

TRAINED UNTRAINED

GROUP

Fig. 3. Mean (±SEM) integrated area under the response curve 3-h for prolactin after the injection of a dopamine antagonist (metoclopramide hydrochloride). This challenge to the pituitary was performed in groups of endurance exercise-trained male runners and age-matched sedentary controls. The significant between group difference (p < 0.05) is denoted with an asterisk. The data are based on the findings in ref. 74.

Several investigators have reported that exercise-hypogonadal men have altered PRL and LH release when either a pharmacological stimulus or an exercise bout are used to provoke the hypothalamus-pituitary (35,47,71,74). Figures 3 and 4 illustrate an augmented PRL response to metoclopramide and a reduced LH response to GnRH in exercise-hypogonadal men vs sedentary controls (74). Hyperprolactinemia is associated with decreased circulating testosterone levels (16). However, although the PRL response to an exogenous stimulus was augmented, there is no evidence that exercise-hypogonadal men are hyperprolactinemic. The converse has been demonstrated (see earlier discussion in section on Basal Hormonal Responses). The reduction in LH release could also reduce testosterone levels. Reports indicate that testicular sensitivity and response to exogenous stimuli are comparable in exercise-hypogonadal men and sedentary males (35,74,75). In contrast, Kujala et al. reported that the testicular response to a stimulus is attenuated after 4 h of exhaustive exercise (47).

Collectively, these findings suggest the development of both a central and a peripheral problem in the hypothalamic-pituitary-testicular axis; however, data in this area are limited and not yet definitive.

Cortisol

Researchers have demonstrated that acute pharmacological or pathological increases in cortisol secretion are associated with a decrease in circulating testosterone levels (33,76). Several investigators have alluded to these hormonal changes as a potential mechanism for the low testosterone levels in exercise-hypogonadal men (6,24,33,76). A single, acute exercise bout at high intensity (>60% of maximal aerobic capacity) could induce transient increases in circulating cortisol, which could bring about the

Acute Exercise Cortisol

TRAINED UNTRAINED

Fig. 3. Mean (±SEM) integrated area under the response curve 3-h for prolactin after the injection of a dopamine antagonist (metoclopramide hydrochloride). This challenge to the pituitary was performed in groups of endurance exercise-trained male runners and age-matched sedentary controls. The significant between group difference (p < 0.05) is denoted with an asterisk. The data are based on the findings in ref. 74.

2000

2000

Response Curve

TRAINED UNTRAINED

GROUP

Fig. 4. Mean (±SEM) integrated area under the response curve 3-h for luteinizing hormone (LH) after the injection of gonadotropin-releasing hormone (GnRH) (gonadorelin hydrochloride). This challenge to the pituitary was performed in groups of endurance exercise-trained male runners and age-matched sedentary controls. A significant between group difference (p < 0.05) is denoted with an asterisk. The data are based on the findings in ref. 74.

TRAINED UNTRAINED

GROUP

Fig. 4. Mean (±SEM) integrated area under the response curve 3-h for luteinizing hormone (LH) after the injection of gonadotropin-releasing hormone (GnRH) (gonadorelin hydrochloride). This challenge to the pituitary was performed in groups of endurance exercise-trained male runners and age-matched sedentary controls. A significant between group difference (p < 0.05) is denoted with an asterisk. The data are based on the findings in ref. 74.

observed reductions in testosterone via the inhibitory effects on GnRH and LH. However, current evidence suggests that hypercortisolemia is an unlikely mechanism for exercise-hypogonadism. There are relatively small, transient changes in cortisol levels in response to exercise (38,44,45,50,53,77-80). In contrast, low testosterone levels are associated with the chronic high cortisol levels of Cushing's syndrome resulting from pituitary or adrenal tumors (16,76). On the other hand, the exercise-induced changes in cortisol are well within the normal range for this hormone, regardless of whether the exercise is of moderate or high intensity. This point is illustrated in Fig. 5 (81). Nevertheless, systematic research examining the role of exercise-induced cortisol changes on testosterone production remains inadequate.

Physiological Consequences of Low Testosterone Levels

There is evidence that the low resting testosterone levels in men doing endurance training have detrimental effects on testosterone-dependent physiological processes. However, the extent of evidence is limited. Currently, only a few reports of decreased spermatogenesis or oligospermia in exercise-hypogonadal men have been published (18,82-85). One of the best controlled studies was by Arce et al. (83). Some of the key findings from that study are displayed in Table 2. Other investigators have reported that endurance-trained men may have a lowered sex drive, but a direct cause-and-effect link between a lower sex drive and circulating testosterone levels was not found in those reports (75,84,86-89). Accordingly, other factors may be affecting the libido of these athletes (e.g., overall fatigue and psychological stress) (19,86). Additionally, some evidence exists that there is no influence of endurance training on sperm characteristics and the spermatogenesis process (68). Relative to the androgenic-anabolic actions of

Testosterone Levels

Fig. 5. Mean Cortisol levels over 24-h in endurance athletes on three separate occasions; (1) control—baseline day with no exercise, (2) exercise day involving two moderate intensity exercise sessions, morning and afternoon, and (3) exercise day involving two high-intensity exercise sessions, morning and afternoon. Exercise sessions produced dose-dependent rises in serum cortisol levels lasting for 3-4 h. The data are based on the findings in ref. 81.

Fig. 5. Mean Cortisol levels over 24-h in endurance athletes on three separate occasions; (1) control—baseline day with no exercise, (2) exercise day involving two moderate intensity exercise sessions, morning and afternoon, and (3) exercise day involving two high-intensity exercise sessions, morning and afternoon. Exercise sessions produced dose-dependent rises in serum cortisol levels lasting for 3-4 h. The data are based on the findings in ref. 81.

Table 2

Semen Characteristics of Endurance-Trained Runners, Resistance-Trained Weight Lifters, and Sedentary Controls (values are means ± SEM)

Runners Weight Lifters Controls

Totals

Volume (mL)

4.2 ± 0.5

Sperm density (x106 • ml-1)

78 ± 12*

Total sperm count (x106)

332 ± 74

Normal motile count (x106)

55 ± 11

Motility

Forward progressive

40.8 ± 4.7*

Nonprogressive

5.0 ± 1.0

Nonmotile

54.2 ± 4.9*

Morphology

Normal (%)

40.2 ± 2.1*

Large (%)

2.7 ± 0.8

Small (%)

4.3 ± 0.8

Amorphous (%)

34.1 ± 2.5

Immature (%)

17.2 ± 2.4*

Round cells (x106)

8.3 ± 1.7*

In vitro sperm penetration

22 ± 5*

3.0 ± 0.5

2.5 ± 0.5

0.09

122 ± 15

176 ± 25

<.01

342 ± 36

376 ± 59

0.86

104 ± 20

107 ± 22

.09

*

58.0 ± 4.6

58.7 ± 2.4

<.01

2.8 ± 1.5

2.0 ± 1.0

.17

*

39.2 ± 3.9

39.3 ± 1.9

0.01

**

54.8 ± 2.9

47.0 ± 3.3

<.01

1.7 ± 0.9

2.3 ± 1.0

.76

2.6 ± 0.7

2.4 ± 0.5

.10

30.1 ± 2.6

37.4 ± 2.8

.19

*

10.5 ± 2.1

10.9 ± 1.2

.03

*

0.6 ± 0.4

2.5 ± 0.9

<.01

-

43 ± 7

.04

*p < 0.05 for runners vs controls. **p < 0.05 for runners vs weight lifters and controls. ***p < 0.05 for runners vs weight lifters. The data are based on the findings in ref. 83.

testosterone, there are no documented detrimental effects of the lower testosterone levels (i.e., decreased protein synthesis and muscle mass development). However, this area has not been examined thoroughly. An additional area in need of research concerns the effect of the exercise-associated decline in testosterone levels on bone demoralization in trained men. Currently, there are no conclusive findings that endurance training results in mineral content changes in men (90). Clinically, however, there is strong evidence that men with low testosterone concentrations have osteopenia (91). Additionally, several compelling case reports have described male athletes with low testosterone levels and excessively low bone mineral density (92,93).

Thus, the question arises is it necessary for endurance-trained males to supplement with testosterone-like substances to safeguard against loss of androgenic-anabolic processes. This question has not been addressed thoroughly in the literature. In one case study, Burge et al. (75) described a male runner with hypogonadotrophic hypogonadism who responded to clomiphene citrate treatment during a 5-mo period. Testosterone and gonadotropin concentrations increased into the normal range, and the subject's sexual function improved. Whether treatment was necessary is debatable. There is little evidence that disruptions in testosterone-dependent processes in exer-cise-hypogonadal men are sufficient to warrant action, but physicians must use their own medical judgement on a case-by-case basis. In extreme cases, especially in men with a low body mass index, such steps may be necessary, and a well-developed pharmacological course of therapy could be highly advantageous and efficacious.

Conversely, there may be beneficial physiologic adaptations from lowered testosterone levels. Some research indicates that lowering testosterone levels may have cardiovascular protective effects and decrease the risk of coronary heart disease (94). A study from Germany demonstrated that pharmacologically induced reduction in endogenous testosterone levels resulted in significant increases in high-density lipopro-tein (HDL) in men (95). Whether the lowering of testosterone directly contributed to the exercise-related increase in HDL remains to be determined. Nonetheless, it is important to recognize that increased physical activity promotes a healthy cardiovascular risk profile, including increased circulating HDL (96).

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    Why is basal testosterone in trained men?
    8 years ago
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