Eur J Appl Physiol(2006) 96: 551-557 DO1 10.1007/~00421-005-0094-4
Robert R. Kraemer Daniel B. Hollander Greg V. Reeves Michelle Francois Zaid G. Ramadan Bonnie Meeker James L. Tryniecki E. P. Hebert V. Daniel Castracane
. .
Similar hormonal responses to concentric and eccentric muscle actions using relative loading Accepted: 27 October 2005 /Published online: 21 December 2005 O Springer-Verlag 2005
Abstract Conventional resistance exercise is performed using sequential concentric (CON) and eccentric (ECC) contractions, utilizing the same muscle load. Thus, relative to maximal CON and ECC resistance, the ECC contraction is loaded to a lesser degree. We have recently shown that at the same absolute load, CON contractions are associated with greater growth hormone (GH) but similar total testosterone (TT)and free testosterone (FT) responses compared with ECC contractions and attributed the larger GH response to greater relative CON loading. In the present study, we have examined the same endocrine parameters to six different upper and lower body exercises using relative loading rather than absolute loading, hypothesizing that GH responses would be similar for CON and ECC actions, but TT and FT responses would be greater after ECC contractions. Seven young men with recreational weight training experience completed an ECC and CON muscle contraction trial on two different occasions in a counterbalanced fashion. The exercises consisted of four sets of 10 repetitions of lat pull-down, leg press, bench press, leg extension, military press, and leg curl exercises at 65% of an ECC or CON 1-RM with 90 s between sets and exercises. CON and ECC actions were performed at the
R. R. Kraemer (El). D. B. Hollander . G . V. Reeves Z. G . Ramadan. J. L. Tryniecki . E. P. Hebert Department of Kinesiology and Health Studies, Southeastern Louisiana University, SLU 10845, Hammond. LA 70402, USA E-mail:
[email protected] V. D. Castracane Department of Obstetrics and Gynecology, Texas Tech University Health Sciences Center, Amarillo, TX 79106, USA
M. Francois . B. Meeker Department of Nursing, Southeastern Louisiana University, Harnmond, LA 70402, USA Present address: V . D. CaHtracane Foundation for Blood Research, Scarborough ME 04070, USA
same speed. ECC I-RMs were considered to be 120% of the CON 1-RM for the same exercise. Blood samples were collected before, immediately after, and 15 min after the exercise. GH significantly increased across both trials but was not different between the two trials. Total testosterone was not significantly altered in response to either trial; however, free testosterone concentrations increased in response to both ECC and CON trials. Data suggest that CON and ECC muscle contractions produce similar GH, T, and free testosterone responses with the same relative loading. Keywords Growth hormone . Testosterone . Free testosterone Muscle contraction Introduction
Factors affecting different metabolic and endocrine responses to resistance exercise protocols include degree of muscle loading, repetition of contractions, rest period between sets, and form of muscle contraction (Dudley et al. 1991; Durand et al 2003; Kraemer et al 1990, 1991). Eccentric muscle contractions (ECC) have been shown to be effective in increasing protein synthetic rate (Lowe et al. 1995: Wong and Booth 1990) and muscle strength (~olliandera n d ~ e s c h1990; ~ o r t o b a et ~ ~al.i 2000). Moreover, there is evidence from studies involving isokinetic contractions that maximal ECC muscle training leads to greater neural adaptations and hypertrophy than maximal concentric (CON) muscle training (Higbie et al. 1996; Hortobagyi et al. 1996). Determining hormonal and metabolic responses to CON and ECC muscle actions is important in order to develop appropriate resistance exercise protocols and equipment that optimizes muscle adaptation for both athletic populations and patients recovering from injury. Several anabolic hormones, including growth hormone (GH) and testosterone, are known to affect protein synthetic rate. A study by Kraemer et al. (2001) reported GH responses to CON isokinetic contractions
greater than ECC isokinetic contractions, but not CON/ ECC isokinetic contractions. Isokinetic contractions have been employed in most studies examining the effects of CON and ECC contractions; however, normal resistance training is typically performed with dynamic, sequential CON and ECC contractions using a constant external load for multiple exercises. At the same absolute load, CON contractions produce greater sympathetic activation (Carrasco et al. 1999), blood lactic acid levels (Carrasco et al. 1999; Overend et al. 2000), and motor unit recruitment (Enoka 1996) than ECC contractions. Thus, ECC contractions have greater loading capacity than CON contractions and during conventional resistance exercise ECC contractions are underloaded (Hortobagyi et al. 1996). Using the same absolute load, we recently demonstrated that submaximal ECC contractions produce less G H response but similar total testosterone (TT)and free testosterone (FT) responses than CON contractions and speculated the greater CON GH response was due to greater relative CON loading (Durand et al. 2003). We conducted the present study to examine the responses of the same endocrine parameters to separate muscle actions (CON and ECC) of six different upper and lower body exercises accounting for greater ECC strength using similar relative loading. We hypothesized that by using a greater relative loading protocol for ECC contractions there would be greater GH, TT, and F T responses than with our previous protocol, resulting in comparable CON and ECC G H levels, but greater TT and FT concentrations in response to ECC muscle actions.
Methods Research design
A counterbalanced design was used to compare hormonal responses to different CON and ECC muscle actions using relative loading. Subjects completed two preliminary trials on separate days to collect descriptive data. Then one-half of the subjects completed a CON trial followed by the ECC trial on a separate day. The other half of the subjects completed the ECC trial first followed by the CON trial. The average time between trials was 13 f 2.7 days. Serum levels of GH, TT, FT, and plasma levels of lactate sampled before, immediately after, and 15 min after exercise were the main outcome measures of the study (Fig. 1). Study approval was granted by the Institutional Review Board of Southeastern Louisiana University. Seven adult males were recruited from the Southeastern Louisiana University student population, gave written consent for study participation, and completed the study. The mean (f SE) physical characteristics of age, height, weight, and body fat (calculated by skinfold assessment) were 25.71 f2.17 years, 181.79 f 2.21 cm, 98.50 f 18.90 kg, and 18.35 It 2.61 %, respectively.
A medical history and lifestyle questionnaire was used to screen the subjects before participation. Criteria for inclusion were 20-36 years of age and a minimum of 2 years recreational weight training experience. Criteria for exclusion were (1) history of cardiovascular, pituitary, renal, hepatic, or metabolic disease; (2) taking medications that could alter test results (e.g., anabolic steroids, sympathoadrenal drugs); (3) smoking; (4) adherence to a reduced calorie or low-fat diet or ketogenic diet that could affect hormonal levels; (5) use of over-the-counter ergogenic aids within the past month; and (6) participation in competitive bodybuilding or weight lifting in the previous year. Preliminary trials (sessions 1 and 2) Subjects completed two preliminary trials to determine anthropometric data, familiarize subjects with the lifting equipment and protocols, determine the CON I-RM for each exercise, and establish reliability for the I-RM determinations. After height and weight were recorded, body composition was determined using a four-site (abdomen, suprailiac, triceps, and thigh) skinfold equation (Jackson and Pollock 1978). A CON 1-RM for each exercise was then determined using a modified protocol (Durand et al. 2003) from Kraemer et al. (1991). The ECC 1-RM for each exercise was calculated as 120% of the respective CON 1-RM, based upon previous data that suggest that ECC I-RM is 20-50% greater than the CON 1-RM (Bamman et al. 2001). Through pilot data we found that 65% of 20% > CON I-RM for ECC contractions and 65% of CON 1-RM for CON contractions best equalized perceptions of stress and ensured completion of protocol for the respective muscle actions. The CON and ECC I-RMs for each exercise are shown in Table I. CON and ECC trials Subjects arrived at 0745 hours and a resting blood sample was collected at 0800 hours. Using weight stack machines, subjects then completed four sets of 10 repetitions at 65% of a CON or ECC I-RM for lat pulldown (LTP), leg press (LP), bench press (BP), leg extension (LE), military press (MP), and leg curl (LC) exercises. Second and third blood samples were taken immediately after exercise and 15 min following exercise. The blood sample time points were based on several of our previous studies in which the hormonal responses to resistance exercise were observed (Durand et al. 2003; Kraemer et al. 1992, 1995). Total exercise time was approximately 45 min. Ninety seconds of rest was included between each set and exercise based on previous studies that have used similar rest period lengths and produced increases in G H and TT (Durand et al. 2003; Kraemer et al. 1992, 1995). For the CON trial, subjects lifted the weight and technicians lowered
Fig. 1 Procedures for preexperimental trials, experimental trials, and blood sampling protocol
Pre-experimental trials 2 trials of 1-RM for LTP, LP, BP, LE, MP, LC
Experimental tijals-subject
LTPLPBPLEMPLC
RO R15
arrives
4 s x 10 reps for each ex.
11
II
-15
Pre
0 fl fl 0 0
post
15post
7 days rest
1
= blood sample;
0 = 1.5 min rest between each set;
Pre, immediately before;
Post, immediately after; lSPost, 15imn after exercise; LTP, latissimus pull; LP, leg press; BP, bench press; LE, leg extension; MP, military press; LC, leg curl the weight stack with steel bar extensions or a pulley; for the ECC trial, technicians lifted the weight stack with steel bar extensions or a pulley, and subjects lowered the weight. Each repetition was performed to the taped rhythm of a timed voice so that the weight was consistently lifted or lowered in 2 s, for the CON and ECC trials, respectively.
n = 6 , due to insufficient serum for one subject. The trial factor represented CON and ECC trials and the time factor represented pre, post, and 15 min recovery times. A Scheffe test was conducted where appropriate. ANOVA analyses of GH, TT, FT, and lactate were followed by calculation of eta-squared, an indicator of effect size that provides the amount of variance explained by specific factors in the ANOVA. For example, an eta-squared of 0.17 for the time factor would mean that 17% of the variance was attributable to the Blood analyses timing of the blood sample. We also conducted a post Blood samples were analyzed for lactate, hemoglobin, hoc power analysis to determine the statistical probahematocrit, GH, T, and FT. An enzymatic colorimetric bility of detecting differences of the observed sizes as assay was used to determine lactate (Trinity Biotech, St significant given the design characteristics and number Louis, MO, USA) and hemoglobin (Pointe Scientific, of subjects in the study. Canton, MI, USA). Hematocrit was determined by the microhematocrit method. Plasma volume shifts were determined from hematocrit and hemoglobin (Dill and Results Costill 1974). GH was determined using a sensitive chemiluminescent enzymatic immunoassay (Immulite, Muscle loads, lactate, and plasma volume shifts Diagnostic Products Corp, Los Angeles, CA, USA). TT and FT were determined by radioimmunoassay Loads for the CON trial and the ECC trial are shown (Diagnostic Systems Laboratories, Webster, TX, USA). in Table 1. There was a time effect, trial effect, and GH, TT,and FT were determined in one assay. Intra- time x trial interaction for lactate. Lactate rose 578% .assay coefficients of variation were all less than 5.0%. in the CON trial and 324% in the ECC trial (Fig. 2). Eta-squared and observed power for trial, time, and interaction, respectively, were 0.2910.54, 0.08/1.0, and 0,2810.74. From pre- to post-exercise, plasma volume Statistics shifts for the respective CON and ECC trials were Hormones and lactate were analyzed using separate -5.131 (*2.35%) and -1.1 (*2.09%); from post to 2x3 (trial x time) ANOVAs with repeated measures on 15 min post, they were 2.80 (f4.02%) and 0.63 the second factor; n = 7 for all analyses except FT, ( & 1.95%). Post hoc analysis indicated that lactate was Table 1 I-RM and 65% 1-RM for lat pull, leg press, bench press, leg extension, military press, and muscle actions
leg
curl concentric and
eccentric
Exercise
Lat pull (kg)
Leg press (kg)
Bench press (kg)
Leg extension (kg)
Military press (kg)
Leg curl (kg)
CON I-RM ECC I-RM 65% CON I-RM 65% ECC I-RM
92.53 (6.78) I 11.04 (8.13)
180.19 (1 5.28) 216.23 (18.30) 117.43 (9.93)
125.65 (21.59) 150.78 (25.91)
69.48 (6.17) 83.38 (7.41) 45.16 (4.01)
64.29 (1 1.28)
34.42 (4.07) 41.30 (4.89) 22.37 (2.65) 26.85 (3.18)
60.15 (4.40) 72.17 (5.29)
140.05 (20.19)
81.67 (14.04) 98.01 (16.84)
54.19 (4.81)
77.15 (13.54) 41.79 (7.33) 50.15 (8.80)
Values are expressed as mean (f SEM)l-RM one-repetition maximum, CON concentric, ECC eccentric
E -2 F
*
sE
-
450
Q)
v,
a
0 5
7 4
300
$ -
+a
0
m
m
-I
150
2 0
0 Pre
Post Time
15Post Time
~ i 2 ~L~~~~~~ . concentrations (mean rt SE) for the concentric (CON, solid bar) and eccentric (ECC, halched bar) trials. *Significantly different from pre values. **Significantly different between CON and ECC trials
Fig. 4 Total testosterone concentrations (mean f SE) for the concentric (CON, solid bar) and eccentric (ECC, hatched bur) trials
Total and free testosterones significantly higher immediately after and 15 min after exercise (P < 0.05) compared to pre-exercise concentrations, and that the CON trial elicited greater lactate levels than the ECC trial post and 15 min post-exercise. Growth hormone There was a significant time effect but not a trial effect or a time x trial interaction for GH (GH responses shown in Fig. 3). By post-exercise, GH increased 567% in the concentric trial and 824% in the ECC trial. Eta-squared and observed power for trial, time, and interaction, respectively, were 0.02/0.07, 0.4410.96, and 0.02/0.08. Post hoc analysis indicated that GH was significantly higher immediately after and 15 min after exercise (P < 0.05) compared to pre-exercise concentrations.
*
2 9.60
.
*
E
-E
0)
b
L
f; g
Discussion
It has been reported that training using maximal isokinetic ECC contractions are associated with greater neural adaptations and greater muscle hypertrophy than
5-
9 0, 5 14
E
7.20
2 a,
0
E
TT did not reveal a time effect,' trial effect, or time x trial interaction (Fig. 4). FT showed a time effect but no trial effect or time x trial interaction. Compared to preexercise, FT was significantly higher post-exercise for both trials (Fig. 5). For TT, eta-squared and observed power for trial, time, and interaction were 0.01/0.06, 0.1310.35, and 0.11/0.29, respectively. For FT, etasquared and observed power for trial, time, and interaction were 0.001/0.05, 0,2710.60, and 0.07/0.16, respectively.
.c)
V)
0
4.80
+a
v,
F 7 a,
e! u
2.40
(3
0.00 Pre
Post Time
15Post
Fig. 3 Growth hormone concentrations (mean f SE) for the concentric (CON, solid bar) and eccentric (ECC, hatched bar) trials. *Significantly different from pre values
0
Pre
Post Time
15Post
Fig. 5 Free testosterone concentrations (mean zk SE) for the concentric (CON, solid bar) and eccentric (ECC, hatched bur) trials. *Significantly different from pre values
CON muscle actions (Hortobagyi et al. 1996). Moreover, isokinetic ECC training has been shown to increase strength to a greater degree than CON training (Higbie et al. 1996). Some of these changes may be due to effects of ECC contractions on the local IGF-I in the working muscle (Bamman et al. 2001). Although it has not been established whether acute increases in GH lead to local skeletal muscle hypertrophy, a number of investigators have hypothesized that a transient elevation of GH can produce an interaction with muscle cell receptors, aiding recovery and stimulation of hypertrophy (Kraemer et al. 1991). Previous research has suggested that GH responses to resistance exercise are affected by the type of muscle action that is employed (Durand et al. 2003; Kraemer et al. 2001). For example, Kraemer et al. (2001) have shown that isokinetic CON contractions induce greater GH responses than ECC contractions. Few studies have investigated G H and testosterone responses to different muscle actions, and no studies have investigated responses to relatively loaded CON and ECC dynamic contractions. Since different muscle actions using the same muscle loading produce different metabolic and hormonal responses (Mayer et al. 1999; Wideman et al. 2002) and since previous data suggest that these differences may be from underloading of ECC muscle actions (Durand et al. 2003), we investigated anabolic hormone responses to CON and ECC contractions using muscle loads relative to the respective CON and ECC I-RMs in dynamic resistance exercise. We demonstrated that a resistance exercise regimen of CON or ECC muscle actions performed on weight stack machines at a percentage of the respective CON or ECC 1-RM produces similar GH, total testosterone, and free testosterone responses. The findings support a portion of our hypothesis that different GH responses to CON and ECC muscle actions previously reported were due to greater loading potential of ECC muscle actions, but did not support that greater testosterone levels would be produced in response to relatively loaded ECC contractions. Relative muscle loading elicited similar TT and FT responses to CON and ECC muscle actions. This is the first study to investigate GH, TT, and FT responses to CON and ECC full range of motion contractions against a constant load, equal to a percentage of the respective CON and ECC I-RMs. GH data suggest that ECC contractions are capable of producing similar increases to that of CON muscle actions when the contractions are loaded with respect to an ECC 1-RM. Only a few studies have examined the separate effects of CON and ECC muscle actions on GH. Kraemer et al. (2001) found that GH responses to an isokinetic CON trial were significantly higher in untrained subjects than GH responses to an ECC isokinetic trial. We recently found similar separate effects using multiple exercises with full range of motion contractions using a constant (as opposed to variable) external load (Durand et al. 2003). Lactate responses were much higher in the CON than the ECC trial of the previous study that was likely due to the underloading of the ECC
contractions. The greater metabolic stress produced by the CON contractions in that study may have contributed to greater G H response since elevated H + ions (Gordon et al. 1994), lactate levels (Lowe et al. 1995; Luger et al. 1992), O2 demand, and availability (VanHelder et al. 1987) are thought to affect GH levels. In the present study, although the lactate concentrations were significantly higher in the CON than the ECC trials, the difference in lactate was not nearly as great as in the previous study (Durand et al. 2003). Specifically, lactate in the CON trial increased 729% in the previous study and 571 % in the present study, whereas lactate in the ECC trial increased 88% in the previous study and 325% in the present study. Thus, smaller differences in CON and ECC lactate responses in the present study could explain similar GH responses to CON and ECC muscle actions. Although not measured in the present study, proprioceptive feedback may have played a role in contributing to G H responses to CON and ECC trials. Repeated cycling trials with 1 h recovery in between produced similar lactate responses, but attenuated GH response in the second trial, leading the authors to conclude that proprioceptive feedback was a greater contributor to G H secretion than lactate (Stokes et al. 2002). Gosselink et al. (2000) documented GH responses through proprioceptive feedback through muscle spindles and Golgi tendon organs. Thus, proprioceptive feedback of a greater magnitude to relative loading versus absolute loading of ECC contractions may have contributed to the similar G H responses in the present study. ECC strength has been estimated to be 20-50% greater than CON strength (Bamman et al. 2001). The ECC 1-RM in the present study was estimated to be 120% of the CON 1-RM and thus it is possible that 120% of a CON 1-RM was an underestimation of the ECC 1-RM for some exercises. However, the actual determination of an ECC 1-RM is difficult and the validity of available methodology is controversial. We chose to use 65% of the 120% CON 1-RM for ECC loads after collecting pilot data with different loading regimens; this loading scheme best equalized CON and ECC perceptions of stress and ensured completion of the 4-set, 10-repetition, 6-exercise, 90 s rest period protocol. Underestimation of the ECC 1-RM would explain a greater lactate response in the CON trial. Although the number of subjects was not large in the present study, the repeated measures statistic with multiple time points and trials gave our statistical tests greater power. Additionally, the age and training background for the subjects was similar, providing a homogenous sample. Finally, observations of individual subject data indicate that endocrine responses were similar between trials and these trends suggest that more data would produce the same results. Although mechanisms for the effect of testosterone on muscle hypertrophy are not completely understood, it is known that testosterone increases protein synthetic rate
as well as satellite cell number and myonuclear number (Sinha-Hikim et al. 2003). TT has been shown to increase in response to some resistance exercise protocols. For example, increases in TT were reported in response to four sets of 10 repetitions at 88% 1-RM of BP, LPT, squats, and 80% 1-RM for overhead press, but not after two sets or six sets (at 68% 1-RM from BP, LPT, squats, and overhead press) of the same exercises (Smilios et al. 2003). It has been shown that load (resistance and repetitions), rest period length, and total work determine the magnitude of TT response to resistance exercise in men (Kraemer et a]. 1990). Additionally, higher resistancetrained athletes tend to produce greater TT response than lesser trained subjects (Ahtiainen et a]. 2004). However, few data exist comparing TT responses to CON and ECC muscle actions. Kraemer et al. (2001) found increases in TT and FT in response to separate CON and ECC isokinetic trials. We reported small but similar increases for TT in a previous study to CON and ECC trials using full ROM exercises at a constant load (Durand et al. 2003). In the present study, we did not find an increase in TT in response to CON and ECC contractions using a relative load. The lack of an increase may be due to the lower resistance training state of the subjects in this study. A small but significant increase in FT occurred in response to both resistance exercise trials, which is similar to a previous report for isokinetic contractions (Kraemer et al. 2001). Thus, assuming there was no change in sex hormone binding globulin, both forms of muscle action contributed to an increase in the availability of the biologically active form of testosterone, potentially affecting muscle growth. In conclusion, GH significantly increased in response to both CON and ECC muscle actions, but was not different between the two contraction types. Total testosterone was not significantly altered in response to either trial; however, free testosterone concentrations increased in response to ECC and CON trials, but were not different from each other. Future studies should determine fatigue characteristics of CON and ECC contractions at different workloads to capitalize on the use of eccentric movement for muscle adaptation. Acknowledgements We wish to thank all of the subjects for their participation in the study. We are especially grateful to Pam Dimarino at Texas Tech Health Sciences Center, Amarillo, for her work on the endocrine assays. The study was funded in part by a faculty development grant from Southeastern Louisiana University.
References Ahtiainen JP, Pakarinen A. Kraemer WJ, Hakkinen K (2004) Acute hormonal responses to heavy resistance exercise in streneth athletes versus nonathletes. Can J AppI . - Physiol 29:52?-543 Bamman MM, Shipp JR, Jiang J, Cower BA, Hunter GR, Goodman A, McLafferty C L Jr, Urban RJ (2001) Mechanical load increases muscle IGF-I and androgen receptor mRNA concentrations in humans. Am J Physiol Endocrinol Metab 280:E383-E390
Carrasco Dl, Delp MD, Ray CA (1999) Effect of concentric and eccentric muscle actions on muscle sympathetic nerve activity. J Appl Physiol 86:558-563 Colliander EB, Tesch PA (1990) Effects of eccentric and concentric muscle actions in resistance training. Acta Physiol Scand 140:31-39 Dill DB, Costill DL (1974) Calculation of percentage changes in volumes of blood, plasma, and red cells in dehydration. J Appl Physiol 37:247-248 Dudley GA, Tesch PA, Harris RT, Golden CL, Buchanan P (1991) Influence of eccentric actions on the metabolic cost of resistance exercise. Aviat Space Environ Med 62:678-682 Durand RJ, Castracane VD, Hollander DB, Tryniecki JL, Bamman MM, O'Neal S, Hebert EP, Kraemer RR (2003) Hormonal responses from concentric and eccentric muscle contractions. Med Sci Sports Exerc 35:3743 Enoka RM (1996) Eccentric contractions require unique activation strategies by the nervous system. J Appl Physiol 81: 2339-2346 Gordon SE, Kraemer WJ, Vos NH, Lynch JM, Knuttgen H G (1994) Effect of acid-base balance on the growth hormone response to acute high-intensity cycle exercise. J Appl Physiol 76:821-829 Gosselink KL, Grindeland RE, Roy RR, Zhong H, Bigbee AJ, Edgerton VR (2000) Afferent input from rat slow skeletal muscle inhibits bioassayable growth hormone release. J Appl Physiol 88:142-148 Higbie EJ, Cureton KJ, Warren GL, Prior BM (1996) Effects of concentric and eccentric training on muscle strength, crosssectional area, and neural activation. J Appl Physiol 81: 2173-2181 Hortobagyi T, Hill JP, Houmard JA, Fraser DD, Lambert NJ, Israel RG (1996) Adaptive responses to muscle lengthening and shortening in humans. J Appl Physiol 80:765-772 Hortobagyi T, Devita P, Money J, Barrier J (2000) Effects of standard and eccentric overload strength training in young women. Med Sci Sports Exerc 33:120&1212 Jackson AS, Pollock ML (1978) Generalized equations for predicting body density for men. Br J Nutr 40:497-504 Kraemer WJ, Marchitelli L, Gordon SE, Harman E, Dziados JE, Mello R, Frykman P, McCurry D, Fleck SJ (1990) Hormonal and growth factor responses to heavy resistance exercise protocols. J Appl Physiol 69:1442-1450 Kraemer WJ, Gordon SE, Fleck SJ, Marchitelli LJ, Mello R, Dziados JE, Friedl K, Harman E, Maresh C, Fry AC (1991) Endogenous anabolic hormonal and growth factor resvonses to heavyresistance exercise in males andwfemales.Int J ~ d o r t Med s 12:228-235 Kraemer RR, Kilgore JL, Kraemer GR, Castracane VD (1992) Growth hormone, IGF-I, and testosterone responses to resistive exercise. Med Sci Sports Exerc 2413461352 Kraemer RR, Heleniak RJ, Tryniecki JL, Kraemer GR, Okazaki NJ, Castracane VD (1995) Follicular and luteal phase hormonal resvonses to low-volume resistive exercise. Med Sci Sports EX&C 27:809-8 17 Kraemer WJ. Dudlev GA. Tesch PA. Gordon SE. Hather BM. Volek JS; ~ a t a m e s sNA (2001). The influence of musc~d action on the acute growth hormone response to resistance exercise and short-term detraining. Growth Horm IGF Res 11:75-83 Lowe DA, Warren GL, Ingalls CP, Boorstein DB, Armstrong RB (1995) Muscle function and protein metabolism after initiation of eccentric contraction-induced injury. J Appl Physiol 79: 1260-1 270 Luger A, Watschinger B, Deuster P, Svoboda T. Clodi M. Chrousos G P (1992) Plasma growth hormone and prolactin responses to graded levels of acute exercise and to a lactate infusion. Neuroendocrinology 56: 112-1 17 Mayer F, Axmann D, Horstmann T, Niess A, Striegel H, Ruf J, Dickhuth H H (1999) Metabolic and cardiocirculatory reactions after concentric and eccentric exercise of the shoulder. Int J Sports Med 20:527-53 1
Overend TJ, Versteegh TH, Thompson E, Birmingham TB, Vandervort AA (2000) Cardiovascular stress associated with concentric and eccentric isokinetic exercise in young and older adults. J Cerontol A Biol Sci Med Sci 55:B177-B182 Sinha-Hikim I, Roth SM, Lee MI, Bhasin S (2003) Testosteroneinduced muscle hypertrophy is associated with an increase in satellite cell number in healthy, young men. Am J Physiol Endocrinol Metab 285:E197-E205 Smilios I, Pilianidis T, Karamouzis M, Tokmakidis SP (2003) Hormonal responses after various resistance exercise protocols. Med Sci Sports Exerc 35:644-654 Stokes KA, Nevill ME, Hall GM, Lakomy H K (2002) Growth hormone responses to repeated maximal cycle ergometer exercise at different pedaling rates. J Appl Physiol 92:602-608
VanHelder WP, Casey K, Radomski MW (1987) Regulation of growth hormone during exercise by oxygen demand and availability. Eur J Appl Physiol Occup Physiol 56:628-632 Wideman L, Weltman JY, Hartman ML, Veldhuis JD, Weltman A (2002) Growth hormone release during acute and chronic aerobic and resistance exercise: recent findings. Sports Med 32:987-1004 Wong TS, Booth FW (1990) Protein metabolism in rat tibialis anterior muscle after stimulated chronic eccentric exercise. J Appl Physiol 69: 1718-1 724
