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The male reproductive system and endurance exercise

HACKNEY, ANTHONY C.

Medicine & Science in Sports & Exercise: February 1996 - Volume 28 - Issue 2 - p 180-189
Clinical Studies: Clinical Review
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During the last decade extensive research on the role of exercise upon the human reproductive system has been conducted. Primarily these investigations have focused on female subjects, but an increasing number of studies have examined male related issues. Evidence now suggests that men who participate in chronic endurance training display mild degrees of reproductive system abnormalities. The major abnormalities noted thus far are reduced resting levels of testosterone, altered pituitary release of luteinizing hormone and prolactin, and altered sperm characteristics. The purpose of this article is to briefly review the research literature on this topic and address select aspects of the impact of exercise upon the male reproductive system. The principal topics addressed in this article are acute and chronic exercise effects, consequences of hormonal changes associated with endurance training, and potential mechanisms for the reproductive system changes detected.

Applied Physiology Laboratory, Department of Physical Education, Exercise and Sport Science, University of North Carolina, Chapel Hill, NC 27599

Submitted for publication March 1995.

Accepted for publication August 1995.

This paper was presented as a Clinical Lecture at the 1994 American College of Sports Medicine national meeting in Indianapolis, Indiana. The author wishes to thank Sarah and Zachary Hackney for their help in the preparation of this manuscript.

Address for correspondence: A. C. Hackney, Ph.D., University of North Carolina, CB# 8700-Fetzer Building, Chapel Hill, NC 27599.

In the last 25 years a great deal of research on the effect of exercise upon the reproductive system has taken place. Most of this research has focused upon the female reproductive system. This seems appropriate because of the prevalence in female athletes of such conditions as oligomenorrhea and amenorrhea and the complications that arise from these problems (17). Recently, however, an increasing number of studies have begun to looked at exercise and the male reproductive system. This research has demonstrated that the effects of exercise on the male and female reproductive systems are not as vastly different as was once thought; that is, some similarities exist between the sexes in the physiological outcomes of physical training on their respective reproductive systems(27,50). For example, studies show endurance-trained men have abnormal concentrations of certain male reproductive hormones (i.e., testosterone, luteinizing hormone, prolactin). These hormonal abnormalities are similar to those displayed by endurance-trained women when intrinsic gender differences in the endocrine system are acknowledged (27,50,56).

The entire area of exercise and reproductive physiology is still rapidly evolving and many questions still remain. This last point seems especially true with respect to men, as the total volume of research examining the relationship between exercise and the male reproductive system is much less than that dealing with females. This article is an attempt to provide a brief review of the findings in the existing research that has addressed the impact of exercise upon the male reproductive system. In particular, this article will focus upon endurance exercise.

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Reproductive Physiology Overview

The male reproductive organs consist of the penis, seminal vesicle, prostrate gland, and testis. The latter (i.e., testicles) are the primary sites were the major male reproductive hormone testosterone is produced, specifically in the Leydig cells of the testis. Additionally it is at the testicle where sperm production takes place. From a fertility perspective, it is the production of sperm that is considered the key functional aspect of the entire male reproductive system. Sperm production occurs in the Sertoli cells of the testis. It is a complex process that actually can be divided in three phases; these being, spermatogenesis, spermiogenesis, and spermiation(34,36). Usually, however, in the literature the term spermatogenesis is used to refer to all of these collective processes. The overall production of sperm is under control of the endocrine system. In particular, the aspect of the endocrine system referred to as the hypothalamic-pituitary-testicular regulatory axis (HPT axis). This axis is a highly complex system involving multiple short and long negative feedback loops; it is depicted in Figure 1 and briefly explained in the following section.

Periodically the hypothalamus releases pulses of gonadotrophin-releasing hormone (GnRH) into the hypophyseal circulation, which supplies the hypothalamus and anterior pituitary. The GnRH stimulates the anterior pituitary to produce and release luteinizing hormone (LH) and follicle-stimulating hormone (FSH). The pulsatile release of GnRH results in LH and FSH also being released similarly into the systemic circulation. For normal, healthy males approximately 2 to 4 LH and FSH pulses are observed during a 6- to 8-h period. However, the amplitudes of the LH pulses are much greater than FSH. At the testicles LH and FSH interact with their target tissue (LH, Leydig cells; FSH, Sertoli cells) receptors located on the respective cell membranes. In the Leydig cells once a hormone-receptor complex is formed there is a mobilization of steroid precursors, in particular the activation of pregnenolone synthesis from cholesterol. Pregnenolone serves as the parent compound from which testosterone is derived. An additional participant in these regulatory events is the anterior pituitary hormone prolactin, which in normal concentrations acts to enhance the action of LH at the Leydig cells (5,45).

In the Sertoli cells, testosterone plays an essential role in the facilitation of the spermatogenesis process (the FSH receptor-hormone formation at the Sertoli cell results in the initiation of the spermatogenesis process). Because of the pulsatile release of LH, testosterone daily concentrations also have fluctuations over a 24-h period(55). Additionally, there is a slight circadian rhythm to the hormone release superimposed upon the pulsatility. Furthermore, there is an age-dependent pattern to the total overall concentration of circulating hormone in the male's blood. This last pattern relates to the maturation of the HPT axis; Figure 2 shows the typical changes in testosterone over a male's life time(5,6,12,59).

The circulating concentration of the various HPT axis hormones is a function of the amount of hormone entering (testicular production and secretion) and the amount leaving (metabolic clearance) the blood pool. The rates for these processes are affected by any changes in the physiological state (e.g., exercise) that alter metabolic turnover of the hormone. Due to space limitations, these issues are not discussed here; however, the reader is directed to reviews by Bunt (9) and Hackney(27) that deal with this topic at length.

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Testosterone

Testosterone is considered the primarily male sex hormone and has been the hormone “of choice,” within most of the male reproductive research conducted. For this reason much of this article will focus upon discussing the changes in testosterone in response to exercise.

Testosterone is a cholesterol-derived hormone having a sterol chemical structure (i.e., steroid classification). It is produced by either the D4 or D5 biochemical pathways within the Leydig cells (45). These pathways are schematically represented in Figure 3. Approximately 95% of the total circulating testosterone pool is of testicular origin with the remainder of adrenal origin. Most of the testosterone(≈97-98% (38,61)) circulates in the blood bound to carrier proteins. The primary carrier protein for testosterone is sex hormone binding globulin (SHBG), binding approximately 44% of the circulating hormone. Albumin and some other plasma proteins can also bind the hormone(≈54%); but, these proteins have a much lower binding affinity with testosterone than SHBG. The remaining unbound portion of the hormone is considered the “free-testosterone” and represents the biologically active form of the hormone (45).

Testosterone has several physiological roles within the male. These roles can be divided into two major categories: 1) those related to reproductive function and the development of male secondary sex characteristics (i.e., androgenic effects), and 2) those that pertain more generally to stimulation of tissue growth and development (i.e., anabolic effects).Table 1 briefly summarizes the major androgenic and anabolic effects attributed to testosterone. For more information the reader is directed to comprehensive review materials on the physiological roles of testosterone (24,38,61).

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Acute Exercise Effects: Maximal and Submaximal Exercise

Early studies. Sutton and colleagues in 1973 were some of the first to experimentally examine the impact of exercise on the circulating levels of reproductive hormones in men (53). In response to a short-term submaximal workload on a cycle ergometer, testosterone concentrations were significantly increased (after 20 min of exercise). Testosterone concentrations were then found to return to preexercise levels by 40 min into the recovery from the exercise bout. Conversely, LH was not affected significantly by the exercise. Several years later Galbo and associates (23) looked at the effect of exercise intensity on testosterone and LH responses. During a graded exercise bout(running) to exhaustion, testosterone concentrations were found to increase somewhat proportionally to the exercise intensity. Furthermore, peak testosterone responses coincided with the maximal intensity of exercise reached. The hormone concentrations then declined during the recovery period after the exercise. In this study by Galbo et al. (23), LH was relatively unchanged throughout the exercise bout; however, there was a significant decline in the concentrations during the recovery period. FSH was also assessed and the levels were found to not changed whatsoever due to the exercise session.

The effect of prolonged (>60 min) submaximal exercise on reproductive hormones was also examined in these early studies. Galbo et al.(23) found that prolonged submaximal exercise to exhaustion resulted in an initial rise in testosterone concentrations (during the exercise) followed by decline as the activity continued. This and other studies demonstrated that by the end of prolonged submaximal exercise the reduction in testosterone could typically be in the magnitude of 25% to 50% if the activity duration was 2 h or longer(16,26,46). Testosterone concentrations, however, were found to return to a normal range within 24 to 72 h into the recovery from the activity(16,23,26,46). These early studies reported conflicting responses for LH to prolonged exercise, with slight increases, decreases, or no change at all being found(20,23,27,46). Although, the LH concentrations were shown to have slight but significant reductions during the recovery period following prolonged exercise(16,22,23). These reductions appeared very transitory and levels were found to return to normal preexercise ranges relatively quickly. The findings from these early studies suggested that FSH levels in the blood were relatively unaffected by prolonged exercise(20,23,27).

Contemporary studies. Relative to testosterone, more recent research on acute bouts of maximal and submaximal exercise has not reported substantially different findings from that given in the early works(10,16,21,26,46,60). Current evidence does, however, suggest that LH concentrations are increased in response to a maximal exercise bout (either near the end of exercise or during the recovery (13,20)). Interestingly, current research continues to find that FSH does not seem to be substantially affected by graded, maximal exercise (20). The recent studies also essentially report similar findings as the early works cited above for the effects of prolonged submaximal exercise on LH and FSH(1,9,13,20,40).

Modality differences. A large amount of the available research on the male reproductive system and exercise has used distance runners as subjects. Relative to other forms of exercise, the data are limited but suggest that the testosterone, LH, and FSH responses to maximal exercise in activities such as weight lifting, rowing, swimming, and high-intensity sprinting seems comparable to what was just discussed(11,33,35,52,54). The reader is directed to other review articles that discuss modality differences at some length (1,35). Relative to submaximal exercise responses in such activities, there also do not seem to be drastic differences from what was just mentioned above. Although, a very limited amount of research has been conducted on this last issue.

Mechanism of acute changes. The primary physiological mechanism accounting for the changes in these HPT axis hormones in response to maximal and submaximal exercise is an issue of some debate. Some of the explanations proposed have been alterations in hormonal synthesis at the endocrine glands, protein binding, metabolic clearance rate, hemoconcentration (i.e., plasma volume shifts), sympathetic stimulation, GnRH pulse release, and testicular blood flow(18,19,22,23,27,37,39,53,60). The evidence so far is not entirely conclusive as to which of these factors is the exact mechanism of the respective hormonal changes to acute bouts of maximal and submaximal exercise. Most likely, however, it is a combination of several of these factors interacting to alter the hormone concentrations.

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Chronic Exercise Effects: Resting Hormone Concentrations

In recent years, the majority of exercise studies examining the male reproductive system have compared trained and untrained men to one another in a resting state. These studies have attempted to determine whether exercise training status (i.e., chronic effects) impacts upon the integrity of the HPT axis hormones (typically referred to as “resting hormonal profiling” studies). These profiling studies have employed protocols using either single, isolated blood sample or serial blood sampling to examine the HPT axis hormones. Furthermore, both retrospective and prospective approaches to research designs have been used in these studies.

Isolated sampling. The results of the retrospective, comparative studies (examining isolated, single blood samples) suggest significantly lower free and total testosterone concentrations exist in chronically (i.e., several years) endurance-trained men at rest(3,28,56). In these studies, the testosterone concentrations of the trained subjects were only 60-85% of the concentrations of age-matched, untrained men. The work by Wheeler et al.(56) has been considered the landmark study in this area as these investigators were the first to report reductions in the resting testosterone levels of endurance-trained men.

Trained males with lower testosterone also display other HPT axis hormonal abnormalities such as decreased resting concentrations of prolactin and more importantly, no significant elevations in resting LH concentrations(3,28,56). These findings of altered resting testosterone, prolactin, and LH concentrations are what led early investigators in this area to speculate that a dysfunction in the regulatory ability of the HPT axis develops in men subjected to chronic endurance training (3,32,56).

In prospective studies investigators have used exercise training to try to induce hormonal abnormalities (e.g., lowered resting testosterone concentrations) in men. In these studies, isolated blood samples have been collected over repeated days or weeks while exposing subjects to endurance training programs. Thus far, the findings of these studies have been contradictory in nature. Several studies reported significant reduction in resting testosterone occurs after 1-6 months of intensive training(11,33,57). Other studies, however, involving 2-3 months of training found no significant resting testosterone changes (seerefs. 21 and 30). The contradiction between the findings of these studies may be a factor of 1) the initial training status of the subjects, as well as 2) the magnitude of training stimulus administered and volume of training load employed. In these prospective studies the changes reported for LH, FSH, and prolactin have been as contradictory as those found for testosterone (11,21,30,57).

Serial sampling. Several retrospective profiling studies collected resting blood samples for extended periods (1-8 h, with blood sampling frequencies of 15- to 30-min intervals) and compared the responses of endurance-trained men with untrained men(2,31,32,42). These studies reported essentially identical results to the isolated sampling studies discussed above. Resting free and total testosterone concentrations were significantly lower in the trained men as compared with untrained men. In trained men the resting testosterone concentrations (total and free) were approximately 40-80% of those found in the untrained men (over the entire period of sampling). Also, as with the isolated blood sampling studies, resting LH concentrations were significantly elevated in the trained males even though reduced testosterone concentrations existed(2,32,42).

These “serial sampling” protocol studies allowed the determination of LH pulse frequency and amplitude measurements (critical factors to testicular testosterone production (12)). McColl et al. (42) have reported that LH pulse amplitude(but not frequency) was less in endurance-trained men with low resting testosterone levels. Wheeler and associates (57), however, have reported findings that are somewhat contradictory to those of McColl et al. with respect to LH. Wheeler et al. conducted a prospective study where serial blood samples (at 15-min intervals for 6 h) were collected in men before and after 6 months of endurance training (running). They found that resting LH pulsatile frequency-amplitude where unaffected by the training even though testosterone concentrations became significantly reduced (post-training values were ≈75% of pretraining levels). These LH results of Wheeler et al. are in agreement with the LH findings in the retrospective study of Hackney et al. (32). It is uncertain why there is disagreement in the LH responses among these studies. Nonetheless, most investigators have interpreted these overall hormonal findings (as with the “isolated sampling” findings) as being reflective of an alteration in the regulatory aspects of the HPT axis developing in men who perform endurance training.

Research problems and concerns. Close examination of the studies comparing the resting hormonal concentrations of endurance-trained and untrained men reveals that several potential methodological problems exist. These problems contribute to the difficulty when attempting to interpret the research findings. For example, as already noted, blood sampling for hormonal profiling can be either from an isolated blood sample or from a series of samples taken one after the other. Each of these sampling protocols has certain limitations and advantages (technical and biological) that must be taken into account before results can be evaluated and compared (see review articles, refs. 9 and 27 for a more complete discussion).

The majority of studies comparing trained men with untrained, sedentary control men have used a retrospective research approach. A problem with retrospective studies is the individuals in question have subjected themselves to the rigors of the training program for years and the investigator is supposedly observing the end result. A great deal of variance can be observed in the hormonal responses of these subjects. This is possibly due to the wide variations in interindividual response to exercise training and the different forms of exercise training employed. Furthermore, there appears to be a large discrepancy in what individual investigators define as “endurance training” and “endurance-trained states.”

In both retrospective and prospective studies it is important to look at the training loads the subjects are performing. That is, it is important to determine that when a study is being conducted that the load has been constant(i.e., no drastic changes). For example, a period of “training overload” (i.e., increased intensity and/or volume in preparation for a competition) can evoke a “stress-related” hormonal response in the HPT. This can result in a suppression of testosterone levels(43). Most, but not all, investigators seemed to have considered this point and attempted to look at endurance-trained men when they were in periods of steady-state training.

A final problem is the assumption made within many studies, that the observed effects on hormone concentrations are primarily a function of the endurance training. This assumption may not be completely valid unless such things as emotional stress, sleep loss, diet, weight loss, and hereditary factors, all of which affect hormone concentrations, are controlled(43).

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Consequences of Hormonal Changes

In men, one of the most serious consequences of an alteration in the HPT axis hormones is the potential disruption in the sperm production process. A very limited number of studies have directly addressed this problem. Ayers et al. (3) were some of the first to report spermatogenesis problems associated with exercise training. These authors found lower resting testosterone levels in distance runners without concurrent elevations in LH. In the 20 runners (30-80 miles·wk-1 training load) examined, two were found to have oligiospermic conditions and ultralow testosterone concentrations. Other similar studies have also reported this oligospermic condition in distance runners (25,49). However, all of these studies have used extremely small sample sizes, which limits the ability to generalize the findings to the population of runners as a whole. One of the most extensive clinical studies of the last few years, in this aspect of male reproductive physiology, was conducted by Arce and associates(2). These investigators found endurance runners and resistance-trained males (i.e., weight lifters) had lower resting testosterone concentrations than matched, sedentary-control men. Additionally, the semen-sperm characteristics of all subjects in the Arce et al. study were assessed. Table 2 reproduces some of the results of the semen-sperm analysis in the subjects. The results suggested the viability of the sperm in the runners and weight lifters were compromised compared to the control men. Furthermore, the number and degree of alterations detected seemed more severe in the distance runners than weight lifters.

If there is disruption of the sperm production processes obviously the issue of male infertility must arise and the question has to be asked.“Are exercising men going to have problems with fathering children?” One study that addressed this question directly was that of Baker et al. in 1984 (4). These investigators reported that high levels of sports activity together with low semen volume were associated with poor pregnancy rates. Unfortunately, the reporting of these findings was very limited and the phrase “sports activity” was not well-defined. Thus, it is difficult to place these results into a context with the studies just mentioned above concerning the development of abnormalities in the sperm production. Other reports citing male exercise-related infertility problems exist, but these are of a case study or anecdotal nature(44,47). These reports can not be discounted. Yet, these findings are extremely difficult to generalize to a larger population because of the unique medical circumstances for each report or the lack of details surrounding the development of the abnormal conditions.

The question remains, “Are exercising men at risk for developing infertility problems?” At this time the answer is a qualified“no.” The findings discussed above allude to there being a small likelihood, under certain circumstances, for exercise-related sperm production problems to develop in men. It is much too premature in the study of this area to interpret these findings as suggestive of these sperm abnormalities leading to an exercise-induced male fertility problem (i.e., inability or difficulty in conception). Much further work is needed to investigate this problem (the reader is direct to a comprehensive review by Acre and DeSouza(1) concerning this topic). Also, it is important to realize that infertility is often a very complicated issue resulting from multiple factors-problems in both or either of the adults in the relationship. Thus, endurance exercise training by a man should not be used as an“easy out” for the explanation of fertility problems or by any means as a contraceptive aid.

In women, exercise induced reproductive dysfunction and bone demineralization problems have long been connected. A similar scenario can be drawn in exercise-trained men with alterations in the HPT axis hormones. Several case studies have been reported indicating an excessive level of bone demineralization exists in trained men who are hypotestosteronemic(44,47,48). MacDougall(41) and his research group attempted to systematically study this issue. These investigators compared total and region bone density levels in groups of male runners who performed different levels of weekly training mileage to a group of matched sedentary men. Essentially no significant difference in bone density was found between any of the groups, except that some of the lower mileage runners had some degree of increased regional density in the lower leg. Furthermore, no relationship between weekly running mileage, blood testosterone concentration and bone density was found. However, it should be noted that none of the running groups in this study exhibited lower resting testosterone levels than the sedentary subjects that were used for comparison. Thus, this issue of bone demineralization is still in need of further examination and may provide a fruitful area for future research.

What is the impact of low resting testosterone on some of the other physiological processes this hormone is associated with; for example, protein synthesis or muscular growth? No significant detrimental effects on the other anabolic-androgenic processes regulated by testosterone have been reported in the literature. However, this area has not been examined thoroughly by the exercise science community and future work should pursue this area more thoroughly.

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Mechanism of Change

Physiologically, the changes within the circulating hormonal levels of the HPT axis of endurance-trained men must be due to either alterations in hormonal production rates, binding protein concentrations, or the metabolic clearance rates. Mechanistic research studies have primarily focused upon the physiological factors that can effect production as being the source of the hormonal alterations.

Hormonal and humoral factors. As noted, the gonadotroph LH is responsible for promoting the synthesis of testosterone at the testis. A study by MacConnie et al. (40) attempted to determine whether the pituitary LH release of endurance-trained and untrained (sedentary) males was different. These investigators administered three different dosages of GnRH in trained and untrained men over a 6-h period. There was a lower LH response from the trained men regardless of the dosage of GnRH administered. Interestingly, these responses are analogous to a finding reported in endurance-trained women by Boyden et al. (8). A complication in the interpretation of the MacConnie data exists because the trained subjects she used did not have significantly lower resting testosterone levels than the untrained subjects. In an additional experiment, MacConnie et al. (40) used the same groups of subjects and injected hCG (a testicular stimulant) to examine whether there were testicular testosterone production response differences between trained and untrained men. Both groups of subjects had increases in testicular testosterone production in response to hCG, but no statistically significant between group differences were observed. This suggests that there was a comparable testicular responsiveness to the hCG stimulus.

A study by Hackney and associates (31) also involved a pituitary stimulation experiment; however, the endurance-trained men examined did have significantly lower resting testosterone levels than a comparison group of sedentary (age-matched) men. Results similar to MacConnie et al.(40) were found. In response to a relative dosage of GnRH, the pituitary LH release of the trained subjects was significantly lower than that from the sedentary subjects. These findings are depicted inFigure 4. From this same experiment the testosterone changes due to the GnRH induced LH increases were also examined and like MacConnie et al. no significant difference was observed between the groups in their relative testosterone responses. These findings of MacConnie et al. and Hackney et al. have been interpreted as suggesting a hypothalamic or pituitary dysfunction-disruption in the HPT axis exists in endurance-trained men with lowered testosterone (1,31,40).

Prolactin is a hormone also associated with causing perturbations in the HPT axis. At either excessively low or high circulating levels, prolactin can result in suppression of testosterone levels in men(5,38). As noted earlier, several studies(3,28,56,57) indicate that trained men who exhibit lower testosterone levels also seem to have low resting prolactin levels. It has been speculated that the absence of prolactin at the testicle alters the effectiveness of LH to stimulate testosterone production. This theory is based upon the proposed synergistic effects of prolactin upon testicular LH receptors (5,24,56,61). However, not all investigators who have reported low resting testosterone in endurance-trained men have also reported the existence of low resting prolactin (28,32).

Some investigations have focused on the other end of the issue and looked at a potential relationship between high prolactin levels and low testosterone. Only one study has indicated elevations in resting prolactin levels occur with endurance training in men and the change corresponded with low resting testosterone (30). In this study, however, the testosterone levels did not remain chronically suppressed in response to the exercise training. Interestingly though, a study by Hackney et al.(31) showed the stimulated release of prolactin from the pituitary of endurance-trained men (i.e., with low resting testosterone) is greater than that in sedentary men. Figure 5 shows the major results of this study. These findings of Hackney et al.(31), however, were due to a drug challenge(metoclopramide hydrochloride, a dopamine antagonist) to the pituitary and not an exercise bout. A study by Boyden et al. (7) in women supports these finding of Hackney and associates. Boyden et al. used a similar drug-stimulated challenge protocol and found an enhancement in prolactin release occurs in women when they are endurance-trained.

Prolactin levels do become elevated in the blood in response to exercise(9,23), and this response seems somewhat proportional to the exercise intensity (22). However, exercise-induced prolactin increases appear rather transitory in nature and last only a few hours into the recovery from activity. Nonetheless, Smallridge et al. (51) have reported endurance runners to have a greater prolactin response to an exercise bout than sedentary men who perform the same type exercise. It is unclear, however, whether these runners in the Smallridge et al. study had lower resting testosterone levels than the comparison group of sedentary men. Along a similar line, Hackney et al.(29) have demonstrated that an endurance exercise training session results in a greatly enhanced nocturnal rise in the prolactin levels of trained men when they sleep. Yet, no direct relationship was found to exist between the changes in nighttime prolactin and testosterone responses as brought about by the daytime endurance-exercise session.

Another potential disruptive hormone to the HPT axis is cortisol. Cumming and associates (14) have demonstrated the direct infusion of cortisol into men results in concurrent declines in testosterone levels. Furthermore, a hypotestosteronemic condition is commonly found in men with Cushing's syndrome (24,61). This phenomenon is most likely due to cortisol producing a direct inhibition of the androgenesis process in the Leydig cell testosterone biosynthesis(45). Exercise does result in a significant elevation in cortisol levels (9,22) and several investigators have suggested that exercise induced increases in cortisol may be the reason for the lower resting testosterone levels in endurance-trained men(13,32,57). This hypothesis has apparently not been experimentally tested. However, in the hormonal profile studies reporting the existence of low testosterone in trained men, none have reported elevated resting cortisol levels(2,31,32,56,57,58). Thus, at this time the role of cortisol to the changes found in the HPT axis of trained men is in need of further study.

Opioid changes, in particular elevations of beta-endorphin, have also been proposed as a disrupter of the HPT axis (15,20). Yet, research so far as to the opioid response to exercise and whether it is reflective of central opioid levels (which would be the avenue effecting the HPT axis) is conflicting and confusing at best. In a review article Cumming et al. (15) commented that although this is a possible factor for the low testosterone findings in trained men, the limited available evidence suggests that it is not a strong likelihood. Again though, this point is also in need of further research.

Inadequate nutrition, in particular states of excessive negative energy balances, is also associated with dysfunctions and disruptions in HPT axis function (38,61). Wheeler and associates(58) have published a single report in which this is suggested as a possible factor for the low testosterone findings of trained men. These investigators base this hypothesis upon the outcomes of food surveys and records that were obtained from several of their groups of trained subjects who had lowered resting testosterone. This is an interesting concept, but no other investigators have provided evidence that negative energy balance states exist in exercise trained men with low resting testosterone. This is a point worth addressing, and more nutritional research relative to this issue is necessary.

Another factor that has been pursued on a limited basis is the effect of exercise catecholamine responses upon the HPT axis. The catecholamines can impact the axis at the level of testicular function as well as at higher levels in the central part of the reproductive regulatory axis-system(18,19,37,39). Several investigators(23,37) have postulated a potential role for the catecholamines in exercise testosterone changes, but for some reason this issue has not been examined in relationship to the finding of low resting testosterone in endurance-trained men.

In conclusion, the available research examining the potential mechanisms for the finding of low resting testosterone in exercise-trained men is limited and confusing. It is thought that a disruption in the HPT axis at the central and/or peripheral levels is the cause for the testosterone findings. The term“central” here referring to the hypothalamus or pituitary while“peripheral” refers to the testicular function. The current evidence suggests the type of disruption appears to be a“breakdown” in the negative feedback loop that regulates testosterone production. The majority of the research findings point in the direction of a central phenomenon being the site of the problem. It is unclear though by exactly what means exercise training is bringing about a change to the central aspects of the axis-the simple answer is we do not know. Much more work is necessary in this area of study before a more definitive conclusive can be made.

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Future Directions

It should be apparent that there is still a vast amount of research necessary in the area of how exercise impacts the male reproductive system. For example, descriptive studies that look at different types of athletic groups (using different forms of exercise training) still need to be done. Such studies may give insight into what combinations of intensity-duration-frequency as well as modality may result in reproductive abnormalities in men. However, studies along these lines are in need of expanding their sample sizes and the arrays of characterization variables(from what has been conducted in the already existing studies) to allow more definitive conclusions to be drawn in the future.

It is still unclear as to what is the exact mechanisms of how the changes in the HPT axis associated with endurance training occur. Thus, we are still in need of mechanistic based work to determine what adaptation in the endocrine system with exercise training results in the suppression of testosterone in males.

The consequences of the HPT axis changes noted are also still not clear. Furthermore, work is needed to see whether chronic exercise training has an impact on the other processes regulated by testosterone (seeTable 1) to determine whether we are unaware of some potentially negative consequences. Along these lines, young athletes are a population group in need of much further study. To date, there appears to be no studies that have looked at the effects of chronic exercise training upon their HPT axis and reproductive systems of young males.Figure 2 shows that testosterone levels alter rapidly between the ages of 10 and 18 yr. It is unclear whether this hormonal change in the HPT axis is, or can be, affected by exercise training at this critical developmental point. Thus far, reproductive abnormalities have only been found in adult males who have been involved with relatively heavy exercise training. Nonetheless, this does not preclude the likelihood of the young male athlete developing an HPT axis problem and affecting the subsequent development of their reproductive system.

These concerns and questions suggest that the area of exercise endocrinology has only begun to scratch the surface of the potential areas of needed research. The scientific community has a great deal of exciting work yet to do in this area.

Figure 1-This figure schematically depicts the hypothalamic-pituitary-testicular (HPT) axis for regulation of the male reproductive system.

Figure 1-This figure schematically depicts the hypothalamic-pituitary-testicular (HPT) axis for regulation of the male reproductive system.

Figure 2-The typical changes in testosterone over an average life time of a male are shown (Genuth, S. Endocrinology. In:

Figure 2-The typical changes in testosterone over an average life time of a male are shown (Genuth, S. Endocrinology. In:

Figure 3-This figure schematically depicts the ▵4 and ▵5 testicular androgenesis biochemical processes resulting in the production of testosterone (Newsholme, E. A. and A. R. Leech.

Figure 3-This figure schematically depicts the ▵4 and ▵5 testicular androgenesis biochemical processes resulting in the production of testosterone (Newsholme, E. A. and A. R. Leech.

Figure 4-Mean (±SEM) integrated area under the curve responses (3-h period) for luteinizing hormone following an injection of GnRH(gonadorelin hydrochloride). This challenge to the pituitary was performed in groups of male endurance-trained runners and age-matched sedentary controls. Significant between group differences (

Figure 4-Mean (±SEM) integrated area under the curve responses (3-h period) for luteinizing hormone following an injection of GnRH(gonadorelin hydrochloride). This challenge to the pituitary was performed in groups of male endurance-trained runners and age-matched sedentary controls. Significant between group differences (

Figure 5-Mean (±SEM) integrated area under the curve responses (3-h period) for prolactin following an injection of a dopamine antagonist (metoclopramide hydrochloride). This challenge to the pituitary was performed in groups of male endurance-trained runners and age-matched sedentary controls. Significant between group differences(

Figure 5-Mean (±SEM) integrated area under the curve responses (3-h period) for prolactin following an injection of a dopamine antagonist (metoclopramide hydrochloride). This challenge to the pituitary was performed in groups of male endurance-trained runners and age-matched sedentary controls. Significant between group differences(

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REFERENCES

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Keywords:

ENDOCRINE; TESTOSTERONE; PHYSICAL ACTIVITY

©1996The American College of Sports Medicine