Comparison of Serum Testosterone and ...

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Thanks are extended to Dr. Terry Kiser and Dr. Robert Kraeling of the. Department of Physiology at the Richard ... In: Landry F,. Orban W (eds) 3rd International ...
E u ~ o Journal D ~ ~ of~

Applied Physiology

Eur J Appl Physiol (1983) 50: 413-419

and Occupat~onal Physiology (L) Springer-Verlag 1983

Comparison of Serum Testosterone and Androstenedione Responses to Weight Lifting in Men and Women* Lawrence W. Weiss, Kirk J. Cureton, and Frederick N. Thompson Depts. of Physical Education and Physiology-Pharmacology, University of Georgia, Athens, Georgia 30602, USA

Summary. To determine if a sex difference exists in the androgen response to heavy-resistance exercise, serum testosterone (T) and androstenedione (A) concentrations were measured in 20 men and 20 women before and during a 2-h period following 30 min of weight lifting. Hormone concentrations from venous blood samples were determined by radioimmunoassay. Prior to weight lifting, T for men (3.51 0.24 ng . ml-') was approximately 10 times that for women (0.36 0.04 ng . ml-I), whereas A for women (1.26 0.07 0.07 ng ml-l). ng ml-') was 43% higher than for men (0.88 Immediately following weight lifting, T was increased significantly ( p < 0.01) in men (0.76 ng ml-', 21.6%), but nonsignificantly in women (0.06 ng ml-', 16.7%). Resting T levels were restored within 30 min. Serum A levels decreased significantly ( p < 0.01) below pre-exercise levels at 2 h post-exercise for both men and women. It was concluded that men have a greater absolute T response to weight lifting than women, whereas the absolute A response to weight lifting is similar in men and women.

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Key words: Androgens - Androstenedione - Sex difference - Testosterone - Weight lifting Introduction It has been suggested that increases in testosterone following heavy-resistance exercise may facilitate or enhance muscle hypertrophy (Edgerton 1973; Fahey et al. 1976; Hetrick and Wilmore 1979; Lamb 1975). If this occurs, it is possible that a sex diffe&nce in the androgen response to exercise could account for a sex difference in exercise-induced muscle hypertrophy. Although a number of * Supported by grants from Nissen/Universal Corporation and the University of Georgia Faculty Research Fund Offprint requests to: Dr. L. W. Weiss, School of H.P.E.R.N., Georgia Southern College, Statesboro, GA 30460, USA

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reports exist on the effect of exercise and training on serum androgen levels, only one previous study (Fahey et al. 1976) has compared the androgen response to weight lifting in men and women. The results of that study were inconclusive, however, due to several experimental design limitations. The present investigation was designed to compare the effects of heavy-resistance weight lifting on serum levels of androgens in men and women while minimizing these limitations. Responses of both serum testosterone and androstenedione were determined since women have a relatively high level of androstenedione and men have a relatively high level of testosterone.

Methods Twenty males and 20 females, 18-30 years of age, participated in the study. All subjects were volunteers accustomed to vigorous physical activity and familiar with weight lifting procedures, but not currently involved in a weight training program. None was taking any hormonal medication or treatment, neither oral contraceptives nor anabolic-androgenic steroids. Female subjects recorded information concerning the onset and duration of their menstrual cycles for approximately 2 months prior to the experimental phase of the investigation. Women were excluded if the duration of two consecutive cycles was less than 24 days or exceeded 38 days. Written informed consent was obtained from each subject. All subjects attended six preliminary practice sessions during which strength measurements were made and the weight lifting circuit used as the experimental treatment was practiced. Each subject then attended one additional session during which the experimental treatment was administered to a small group of subjects. All treatment sessions were held at the same time of day (1830-2130 h) in order to minimize possible diurnal variations in androgen production (Faiman and Winter 1971; Murray and Corker 1973; Naftolin et al. 1973). Women were scheduled for the treatment session during the early part of the follicular phase of the menstrual cycle, a period of minimal variability in blood androgen levels (Abraham and Chakmakjian 1973; Baird et al. 1974; Naftolin et al. 1973). For women having 28-day cycles, the experimental treatment was administered between the fourth and tenth days. For women having shorter o r longer menstrual cycles, the treatment was administered in a comparable phase of the cycle. A n equal number of males and females was tested at each session. Approximately 5 weeks were required to conduct treatment sessions for all of the subjects. The experimental treatment required each subject to perform heavy-resistance weight lifting exercises, consisting of three sets of a four-exercise circuit on a Universal Gym. The exercises completed were the latissimus pull-down, supine bench press, arm curl and leg press. The load for each exercise was set at approximately 80% of the individual's one repetition maximum (IRM), with the number of repetitions the maximum possible at each station. Approximately 2 min rest was given between each exercise. The total duration of the three-circuit routine was approximately 30 min. Because the average strength of the men was greater than that of the women, the average resistance used by the men, and therefore the total work completed, was greater than for the women. Venous blood samples were obtained from an antecubital arm vein at 30 and 15 rnin before exercise,'immediately after exercise, and at 0.5,l.O and 2.0 h following exercise. Blood samples were immediately chilled, serum harvested within 24 h and stored at -20°C until assayed. Serum concentrations,,of testosterone (A4-androstene-17/3-ol-3-one) and androstenedione (A4-androstene-3,17,diok) were measured by radioimmunoassay (Haynes et al. 1977; Mongkonpunya et al. 1975). Mean recovery of radioactively labelled testosterone from serum was 91%, and assay values were not corrected for procedural losses. Accuracy of the testosterone assay was determined by adding 10, 30, 50, 300, and 500 pg of testosterone to serum, and recovery of added testosterone averaged 92, 88, 85, 102, and 112%, respectively. Only dihydrotestosterone and androstenedione were found to cross-react (60.0 and 1.7%, respectively) with the testosterone antiserum (Kiser et al. 1978). No other steroid so tested cross-reacted with the antiserum by more than 0.1%. The

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Fig. 1. Mean (+ SEM) testosterone levels before and after weight lifting

intra-assay coefficient of variation for duplicate samples was 8.0%, while inter-assay coefficients of variation for pools of male and female serum were 4.2 and 9.8%, respectively. Mean recovery of radioactively labelled androstenedione from serum was 90%, and assay values were not corrected for procedural losses. Recovery of 50 and 100 pg of androstenedione added to serum averaged 114 and 115%, respectively. T h e only steroids to cross-react greater than 0.4% with the antiserum (CSU#866-10-8-70) were testosterone (0.7%) and dihydrotestosterone (1.2%). The intra-assay coefficient of variation for duplicate samples was 6.7%, while the inter-assay coefficient of variation for pooled female serum was 5.8%. Treatment effects were assessed statistically by using a two-factor, mixed-design analysis of variance. F ratios for the two main factors, gender and time, and for the interaction of these two factors, were calculated. Additional tests for simple main effects and the Tukey Multiple Comparison Test were used to determine which means were significantly different.

Results Prior to weight lifting, the serum testosterone concentration in men (3.51 fr 0.24 n g . ml-') was approximately 10 times that for women (0.36 k 0.04 ng - ml-'; Fig. 1). Immediately following exercise, the mean level for men was significantly higher than at rest ( p < 0.01) by 0.76 ng . ml-I (22%), while the mean level for women was 0.06 ng . ml-I (17%) higher than at rest, a nonsignifi'cgfit change @ > 0.05). Values for both men and women returned to the resting'levels by 30 min post-exercise, and decreased slightly over the next hour and a half. A significant sex by time interaction indicated there was a sex differencd in the absolute testosterone response to weight lifting. The mean androstenedione concentration in men prior to weight lifting (0.88 0.07 ng . ml-l) was 43% lower than for women (1.26 0.07 ng . ml-'; Fig. 2). Immediately following exercise, values for both sexes were increased

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Fig. 2. Mean (+ SEM) androstenedione levels before and after weight Lifting

above the resting levels by approximately 0.1 ng . ml-' (8-11%) and then progressively decreased below the resting values. No significant change in mean androstenedione levels was observed until 2 h post-exercise, when levels dropped significantly ( p < 0.01) below pre-exercise for both sexes. A nonsignificant sex by time interaction indicated the absolute androstenedione response to weight lifting was not different in men and women. Discussion

The mean resting concentration of serum testosterone was in the normal range for both men and women (Auletta et al. 1974; Baulieu and Robe1 1970; Wilkerson et al. 1980). Immediately following 30 min of weight lifting, the testosterone level was increased significantly only in men. The magnitude of the absolute response was 12.7 times greater in men, whereas the percentage change above resting levels (males, 21.6%; females, 16.7%) was more similar. These findings are in agreement with those described by Fahey et al. (1976), who reported a significant increase in serum testosterone immediately following a strenuous'~6utof weight lifting in college men, but not in college women. In that study, the absolute increase in men was 28.7 times that of the women, with the percentage increases being 19.2% and 6.8% for males and females, respectively. The authors suggested that the nonsignificant increase in testosterone by women may have been due to inexperience in weight lifting and a lack of aggressiveness in performing the exercises. The men and women also performed different weight lifting routines. In the present investigation, the men and women were

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quite similar in their experience and involvement in weight lifting, and simultaneously performed the same type of individualized exercise routine. Both men and women appeared to be highly motivated and were exorted to complete the maximum number of repetitions at each station. Thus, it is unlikely that differences between men and women in training background or in the way they performed the weight lifting routines were responsible for the sex difference in the testosterone response observed. In contrast to the present findings, Skierska et al. (1976) did not find a significant increase in serum testosterone in well-trained male weight lifters following 30 min of weight lifting. Although the duration of exercise in that study was the same as in the present, the intensity was not reported. Therefore, a difference in work intensity could be the basis for the contrasting results. In this regard, Sutton et al. (1978) found that submaximal rowing and swimming resulted in nonsignificant changes in plasma androgen levels, whereas maximal physical activity resulted in significant androgen increases. However, significant increases in serum testosterone may occur in men following submaximal cycling and running (Sutton et al. 1978; Wilkerson et al. 1980). The mean resting concentration of serum androstenedione was in the normal range for both men and women (Auletta et al. 1974; Baulieu and Robel 1970; Van Der Molen 1970). Serum androstenedione level did not increase significantly after weight lifting, but decreased significantly at 2 h post-exercise in both men and women subjects. This pattern of response differs from that reported by Kuoppasalmi et al. (1976), following interval sprint running by well-trained male runners. Androstenedione levels were significantly higher immediately following the series of sprints and did not decrease to pre-exercise levels until 6 h post-exercise. Differences in the conditioning status of the subjects and/or the mode, intensity and duration of the activity may explain the contrasting results. Sutton et al. (1978) proposed that the decrease in plasma volume accompanying vigorous exercise contributes to the increase in serum androgens, but that a reduced hepatic blood flow during exercise is primarily responsible for the increase in serum androgens. Wilkerson et al. (1980) found, however, that increases in plasma testosterone concentration following vigorous exercise were completely accounted for by a decrease in plasma volume and hemoconcentration. The similar percentage increases in serum testosterone for men and women in the present study, despite the markedly different resting levels and absolute responses, indicate that the changes were approximately proportional to resting blood levels. This suggests that either hemoconcentration and/or a reduced metabolic clearance rate may have been responsible for the serum testosterone changes. It is a poqular theory that weight lifting results in less muscle hypertrophy in women than in men because of women's lower blood androgen levels (Brown and Wilmore 1974; Mahew and Gross 1974; Wilmore 1974). Whether or not the greater absolute testosterone response by men, as found in the present investigation, contributes to a difference in the potential of men and women for work-induced skeletal muscle hypertrophy is not clear. The role of testosterone and other androgens in this type of hypertrophy in adults has not been defined.

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Although testosterone is not required for work-induced skeletal muscle hypertrophy (Goldberg 1971), it could have a function similar to that reported for growth hormone, increasing the extent of muscle hypertrophy that occurs (Goldberg and Goodman 1969; O'Malley 1969). Anabolic-androgenic steroids administered to males in combination with heavy-resistance training have accelerated strength and body size increases in some studies, while having no appreciable effect in others (American College of Sports Medicine, 1977). It is important to note that little or no muscle hypertrophy results from participation in activities such as running and swimming, although the testosterone response is similar to that obtained with weight lifting (Kuoppasalmi et al. 1976; Sutton et al. 1973; Wilkerson et al. 1980). Further, it is not known if an increase in total serum testosterone concentration, either as a result of taking anabolic-androgenic steroids and/or participating in intensive exercise, increases the circulating level of unbound testosterone, the most anabolically active state of the hormone (Baulieu and Robe1 1970; Minguell and Sierralta 1975). The anabolic significance of the higher resting and post-exercise androstenedione levels in women as compared with men is probably inconsequential, since androstenedione is approximately one-fifth as potent as testosterone in its androgenic effect (McKerns 1969). The similar androstenedione response to weight lifting in men and women coupled with higher levels in women suggest that differences in resting levels or changes in the serum concentration of this steroid resulting from weight lifting would not contribute to a sex difference in muscle hypertrophy. In summary, results of this study indicate that men have a greater absolute testosterone response to weight lifting than women, whereas the androstenedione response is similar. Additional research is needed to determine whether the greater testosterone response by men contributes to a sex difference in the extent of muscular hypertrophy experienced consequent to heavy-resistance training. Acknowledgements. Thanks are extended to Dr. Terry Kiser and Dr. Robert Kraeling of the Department of Physiology at the Richard B. Russell Agricultural Research Center in Athens, Georgia for their technical assistance in carrying out the testosterone assays.

References Abraham G , Chakmakjian Z (1973) Serum steroid levels during the menstrual cycle in a bilaterally adrenalectomized women. J Clin Endocrinol Metab 37: 518-587 American. College of Sports Medicine (1977) Position statement on the use and abuse of anaboliqandrogenic steroids in sports. Med Sci Sports 9: XI-XI11 Auletta G, Caldwell B, Hamilton G (1974) Androgens: testosterone and dihydrotestosterone. In: Jaffe B, Behrman H (eds) Methods of hormone radioimmunoassay. Academic Press, New York, pp 359-370 Baird D, Burger P, Heavon-Jones G, Scaramuzzi R (1974) The site of secretion of androstenedione in non-pregnant women. J Endocrinol 63 : 201-212 Baulieu E, Robe1 P (1970) Catabolism of testosterone and androstenedione. In: Eik-nes K (ed) The androgens of the testis. Marcel Dekker, New York, pp 50-70

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Brown C, Wilmore J (1974) The effects of maximal resistance training on the strength and body composition of women athletes. Med Sci Sports 6 : 174-177 Edgerton V (1973) Exercise and the growth and development of muscle tissue. In: Rarick G (ed) Physical activity: human growth and development. Academic Press, New York, pp 1-31 Fahey T , Rolph R, Moungmee P, Nagel J , Mortara S (1976) Serum testosterone, body composition, and strength of young adults. Med Sci Sports 8: 31-34 Faiman C, Winter J (1971) Diurnal cycles in plasma FSH, testosterone and cortisol in men. J Clin Endocrinol 33 : 186- 192 Goldberg A (1971) Biochemical events during hypertrophy of skeletal muscle. In: Alpert N (ed) Cardiac hypertrophy. Academic Press, New York, pp 301-314 Goldberg A, Goodman H (1969) Relationship between growth hormone and muscular work in determining muscle size. J Physiol 200: 655-666 Haynes N, Kiser T, Hafs H, Carruthers T, Oxender W, McCarthy M (1977) Effects of intracarotid infusion of prostaglandin E2a on plasma luteinizing hormone, testosterone and glucocorticoid concentrations in bulls. J Anim Sci 45: 1102-1107 Hetrick G, Wilmore J (1979) Androgen levels and muscle hypertrophy during an eight week weight training program for menlwomen. Med Sci Sports Exerc 11 : 102 Kiser T , Milvae R, Hafs H, Oxender W, Louis T (1978) Comparison of testosterone and androstenedione secretion in bulls given prostaglandin E2a or luteinizing hormone. J Anim Sci 46 : 436-442 Kuoppasalmi K, Naveri H, Rehunen S, Harkonen M, Adlercreuz H (1976) Effects of strenuous anaerobic running exercise on plasma growth hormone, cortisol, luteinizing hormone, testosterone, androstenedione, estrone, and estradiol. J Steroid Biochem 7 : 823-829 Lamb D (1975) Androgens and exercise. Med Sci Sports 7 : 1-5 Mahew J, Gross P (1974) Body composition changes in young women with high resistance weight training. Res Q 45 : 433-440 McKerns D (1969) Steroid hormones and metabolism. Appelton-Century Crofts, New York, pp 68-70 Minguell J, Sierralta W (1975) Molecular mechanisms of action of the male sex hormones. J Endocrinol 65: 287-315 Mongkonpunya J, Lin U, Noden P, Oxender W, Hafs H (1975) Androgens in the bovine fetus and dam. Proc Soc Exp Biol Med 148: 489-493 Murray M, Corker C (1973) Levels of testosterone and luteinizing hormone in plasma samples taken at 10-minute intervals in normal men. J Endocrinol 56: 157-158 Naftolin F, Judd J, Yen S (1973) Pulsatile patterns of gonadotropins and testosterone in man: the effects of clomiphene with and without testosterone. J Clin Endocrinol Metab 36: 285-288 07MalleyB (1969) Hormonal regulation of nucleic acid and protein synthesis. NY Acad Sci Trans 31 :478-503 Skierska E, Ustupska J, Biczoa B, Lukaszewska J (1976) Effect of physical exercise on plasma cortisol, testosterone, and growth hormone levels in weight lifters. Endokrynol Pol 27 : 159- 165 Sutton J, Coleman M, Casey J (1978) Testosterone production rate during exercise. In: Landry F, Orban W (eds) 3rd International Symposium on Biochemistry of Exercise. Symposia Specialists, Miami, pp 227-234 Sutton J, Coleman M, Casey J, Lazarus L (1973) Androgen responses during physical exercise. Br Med J 1 : 520-522 Van Der Molen H (1970) Estimation of androstenedione and testosterone. In: Eik-nes K (ed) The androgens of the testis. Marcel Dekker, New York, pp 148-149 Wilkerson J, Horvath S, Gutin B (1980) Plasma testosterone during treadmill exercises. J Appl Physiol 49..249-253 Wilmore J (1574) Alterations in strength, body composition and anthropometric measurements consequent to a 10-week weight training program. Med Sci Sports 6 : 133-138 Accepted September 27, 1982