Both the neuromuscular and the endocrine systems have been shown to play an integrative role in acute responses and long-term adaptations to endurance and strength training. Research often shows that strength and power development are compromised when prolonged periods of strength training are combined with endurance training sessions performed on separate days (16,20,26) and on the same day (7). This phenomenon has commonly been described as the “interference effect,” which is caused by high training volume and frequency of combined endurance and strength training (19).
Several studies have shown that acute alterations and recovery of neuromuscular and endocrine function in response to a single bout of exercise are most critical in the development of long-term adaptations (7,27). Endurance and strength exercises performed on separate days elicit divergent acute neuromuscular and endocrine responses and recovery patterns that might in part explain the limitations in strength gains when both exercises are chronically combined.
Endurance performance places a relatively small demand on force production but may produce some neuromuscular fatigue (28). Resistance loadings, in contrast, typically cause drastic decreases in maximal neural activation, maximal force production, and force-time characteristics of the muscles loaded (14). Although short bouts of high-intensity endurance exercise can lead to similar acute increases in steroid hormone concentrations, as observed immediately after heavy strength loadings (35,40), prolonged intense endurance performance produces a catabolic environment, dominated by dramatic increases of cortisol (C) concentrations (8) and accompanied by decreases in testosterone (T) concentrations, after, for example, a marathon run (22,40).
Several authors have demonstrated the synergistic function of the neuromuscular and endocrine systems in acute response to exercise performance (1,31). The time course of the recovery from exercise, however, might differ between neuromuscular and endocrine variables (17). Although the recovery of neuromuscular performance after endurance or strength loadings usually takes place within 24–48 hours (15,34), serum basal T concentrations can remain decreased for much longer than 48 hours after heavy resistance loadings (17).
Acute neuromuscular and endocrine responses and recovery to endurance and strength loadings performed on separate days are recently relatively well studied, but only a few studies (e.g., 5,13) have investigated acute neuroendocrine alterations after a single session of combined endurance and strength loading. Moreover, to the best of our knowledge, no studies are available investigating short or long-term recovery. Growing evidence suggests, however, that residual fatigue caused by an initial loading may reduce the quality of a subsequent loading, reflected in specific acute responses and recovery time courses (28), leading to compromised long-term adaptations (7). Muscular force development during a strength loading conducted immediately after endurance exercise has been shown to be either decreased (9) or unaltered (13), and seems to depend on the intensity of the preceding endurance loading (10). Similarly, serum concentrations of steroid hormones (growth hormone [GH]) can be attenuated after a single combined endurance and strength loading session in physically active men (13) but have also been shown to be acutely increased (T) in strength-trained subjects performing a strength and endurance loading (5).
Considering the importance of acute neuromuscular and endocrine responses and recovery to a single session of combined endurance and strength loading for long-term adaptations, it is of crucial relevance to investigate whether the first half of a loading session (i.e., endurance or strength exercise, respectively) alters acute neuromuscular responses and recovery of the subsequent loading (i.e., strength or endurance exercise, respectively). Moreover, it is of great importance to examine whether one loading order (e.g., endurance + strength [E + S]) produces more favorable anabolic responses than the opposite order (e.g., strength + endurance [S + E]). Thus, the purpose of the present study was to investigate acute neuromuscular and endocrine responses and recovery to a single session of combined endurance and strength loading using 2 different loading orders in moderately physically active young men.
Experimental Approach to the Problem
A cross-sectional design was used to investigate the acute effects and recovery in response to a single session of combined endurance and strength loadings with different exercise orders (i.e., E + S vs. S + E). As both groups performed the identical loadings in terms of volume and intensity, specific responses and recovery patterns of neuromuscular performance and endocrine function originating from the different order were measured. Before the start of the measurements, all subjects were matched according to age, physical activity background, and physical fitness and assigned to either of 2 groups (E + S, n = 21 and S + E, n = 21). Because this research project was part of a larger study including a longitudinal training intervention, all subjects performed only 1 loading order (E + S or S + E). All subjects proceeded to the laboratory for a total of 6 times. First, the subjects were familiarized with the measurement procedures, and measurement equipment was set up according to the individual needs of each subject. During the following 2 laboratory visits, V[Combining Dot Above]O2max and maximal workload during a graded cycle ergometer test were determined. In addition, subject’s 1 repetition maximum (1RM) and maximal voluntary isometric contraction (MVCmax) during seated horizontal leg press were obtained. Thereafter, all subjects performed 1 single session of combined endurance and strength loading in the order of the corresponding group (E + S or S + E) and returned to the laboratory for recovery measurements at 24 and 48 hours after the loading session. The duration between each baseline measurement session was at least 3 days. The duration between the last baseline measurement session and the loading was a minimum of 4 days. Subjects were asked to continue their normal activities of daily living throughout the measurement period.
The subjects for the present study were recruited from the city of Jyväskylä through newspaper advertisements. After subjects expressed their interest in the research, 42 moderately physically active young men were selected through telephone interviews to participate in the study. All included subjects were free of acute and chronic illness, disease, or injury and reported not using medication that would contraindicate the performance of intense physical activity or interfere with neuromuscular function and endocrine metabolism. Furthermore, all included subjects reported to perform physical activity such as light walking, cycling, or occasionally sport games (e.g., soccer or floorball) for not more than 3 times per week but did not conduct systematic endurance or strength training. Before participation in the study, subjects were informed about the study procedures and possible risks both verbally and in written form before signing an informed consent. Before testing, subjects were required to complete a health questionnaire and obtain a resting electrocardiographic measurement, both reviewed by a cardiologist. The demographic characteristics of the subjects were as follows (mean ± SD): age 29.2 ± 4.9 years, height 178.3 ± 5.2 cm, and body mass 75.9 ± 8.6 kg. The study was conducted according to the Declaration of Helsinki, and ethical approval was granted by the University of Jyväskylä.
All baseline and loading measurements were conducted during October and November of 2011. The measurements within the combined loading included the recording of maximal isometric strength (horizontal bilateral isometric leg press) and power (countermovement jump [CMJ] on a force plate) and the determination of serum hormone and creatine kinase (CK; both from venous blood samples) and blood lactate (capillary blood) concentrations. These measurements within the loading were conducted at the following time points (Figure 1): before the start of the combined session (PRE), immediately after the first exercise (MID, after endurance or strength loading), and right after the completed combined session (POST). The follow-up measurements including the same measurements were conducted after recovery of 24 hours and 48 hours at ±1 hour from the end of the complete loading. The acute loading measurements of both groups (E + S and S + E) were conducted between 7:00 AM and 3:00 PM (mean ± SD, E + S: 9:01 AM ±1:57 hours; S + E: 8:47 AM ±2:20 hours). The corresponding follow-up measurements were conducted at the time between 9:00 AM and 4:00 PM (mean ± SD, 24 hours: E + S, 11:14 AM ±2:05 hours; S + E, 11:03 AM ±2:19 hours; 48 hours: E + S, 11:13 AM ±2:06 hours; S + E, 11:00 AM ±2:18 hours).
At PRE, 24 hours, and 48 hours, the blood sample was drawn first and then the maximal strength and power tests were conducted. At MID and POST, the blood sample was taken after the maximal strength and power tests. Blood lactate concentrations were measured by collecting capillary blood from the fingertip in both loading orders at the following time points: pre-endurance, after 10 minutes (endurance 10), after 20 minutes (endurance 20), post-endurance, pre-strength, and post-strength. To account for changes in the hydration status of subjects, body mass was determined before the start of a loading and immediately after the completion of the loading. Subjects were required to begin the combined loading in a hydrated state and were allowed to ingest 2 dl of water at MID, right after the venous blood sample was taken.
In addition to the measurements of acute loading responses and recovery, basal morning levels of serum hormone and CK were recorded by drawing venous blood samples on the day of the combined loading after 12 hours of fasting, between 7:00 and 9:00 AM. To control the experimental conditions, subjects were asked to minimize physical and mental stress on the day before and throughout the 3 days of the loading measurements. Furthermore, subjects were asked to have at least 7–8 hours of sleep and to keep their nutritional intake similar on all 3 measurement days.
Strength and Endurance Loading
The strength loading focused primarily on leg extensors and was performed on a dynamic leg press device (David 210; David Health Solutions Ltd., Helsinki, Finland). The strength loading included sets of explosive power, maximal strength, and hypertrophic loads with an overall duration of 30 minutes. The starting knee angle for all exercises was similar to the knee angle used for the determination of the 1RM during the baseline measurements (<60°).
Subjects first performed 3 sets of 10 repetitions with a load of 40% of 1RM. During these sets, subjects were instructed to fully extend their legs while producing force as rapidly and explosively as possible. Next, subjects performed a set of 3 repetitions at 75% of 1RM, followed by 3 sets of 3 repetitions with a load of 90% of 1RM (maximal strength). The resting period between all explosive and maximal sets was 3 minutes. The strength loading was concluded by performing 4 sets of 10 repetitions with a load of 75% and 80–85% of 1RM (first and last set 75%, second and third set 80–85%) with a resting period of 2 minutes between the sets, a protocol typically used during hypertrophic strength training. The initial loads were calculated from each subject’s predetermined 1RM and, in order to standardize the loading conditions, during the maximal and hypertrophic sets additional load was added to achieve at least 1 set of a true repetition maximum (i.e., 3RM and 10RM, respectively). During these maximal sets, failure was allowed, and in case the subjects were not able to perform the required amount of repetitions, assistance was provided so that both loading groups performed identical loadings.
The endurance loading was conducted on a bike ergometer (Ergomedic 839E; Monark Exercise AB, Vansbro, Sweden). Subjects performed 30 minutes of continuous cycling at 65% of their individual maximal watts (achieved during the baseline measurement). Subjects were required to keep the pedaling frequency constant at 70 rpm. In case the subjects were not able to keep up the required frequency, intensity was reduced by 15 W. If the subject was not able to return back to a frequency of 70 rpm within 1 minute, intensity was reduced by another 15 W. This procedure was repeated until the subjects were able to keep up the initial frequency.
One Repetition Maximum
Subject’s 1RM of leg extensors was determined using a seated horizontal leg press (David 210; David Health Solutions Ltd., Helsinki, Finland). Before attempting 1RM, subjects completed a warm-up consisting of 3 sets using 5 repetitions with 70% of the estimated maximal capacity, 2 repetitions at 80–85%, and 1 repetition at 90–95% with 1-minute rest between the sets. After this warm-up, no more than 5 attempts were allowed to reach 1RM. The starting knee angle for all subjects was (mean ± SD) 58.4 ± 1.9°. Subjects were instructed to grasp the handles located by the seat of the dynamometer and to keep constant contact with the seat and backrest during the complete extension to 180°. To promote maximal effort, verbal encouragement was given. The greatest weight that the subject could successfully lift (knees fully extended) at the accuracy of 1.25 kg was accepted as 1RM.
Isometric Leg Extension
Maximal isometric bilateral leg extension force (MVCmax) was measured on a horizontal dynamometer (16, Department of Biology of Physical Activity, University of Jyväskylä, Jyväskylä, Finland) in a seated position at a knee angle of 107°. Subjects were instructed to produce maximal force as rapidly as possible with the entire foot against the force plate for a duration of 3–4 seconds. Subjects were instructed to keep a constant pretension of ∼200 N before the maximal contraction. During the execution of each maximum trial, subjects were required to grasp the handles located by the seat of the dynamometer and to keep constant contact with the seat and the backrest. Verbal encouragement was given to promote maximal effort. Before the start of the loading and at both follow-up measurements (24 and 48 hours), 3 trials with a resting period of 1 minute were conducted. At MID (after E or S, respectively) and POST, only 2 subsequent trials separated by a resting period of 15 seconds were conducted. The force signal was low pass filtered (20 Hz) and analyzed (Signal software, version 4.04; Cambridge Electronic Design Ltd., Cambridge, United Kingdom). In addition to maximal force, rapid force produced in 500 milliseconds (MVC500) and maximal rate of force development at 10 milliseconds (RFD10) were calculated from the force curve.
Maximal dynamic power was determined by the CMJ height on a force plate (Department of Biology of Physical Activity, University of Jyväskylä, Jyväskylä, Finland). Subjects were asked to stand with their feet hip width apart and their hands on their hips and were instructed to perform a quick and explosive CMJ after a self-selected start. Force data were collected, low pass filtered (20Hz) and analyzed by computer software (Signal 4.04; Cambridge Electronic Design Ltd.). Jumping height was then calculated from flight time using the following equation:
Maximal workload and V[Combining Dot Above]O2max were determined using a graded protocol on the bike ergometer (Ergometrics 800; Ergoline, Bitz, Germany). The initial load for all subjects was 50 W and was increased by 25 W every 2 minutes. Heart rate was monitored continuously throughout the test (Polar S410; Polar Electro Oy, Kempele, Finland). Oxygen uptake was determined continuously breath by breath using a gas analyzer (Oxycon Pro; Jaeger, Hoechberg, Germany). Before each test, airflow calibration was performed using a manual flow calibrator, and the gas analyzer was calibrated using a certified gas mixture of 16% O2 and 4% CO2. The V[Combining Dot Above]O2max was taken as the highest 30-second V[Combining Dot Above]O2 value. To assure that V[Combining Dot Above]O2max was reached, other criteria such as heart rate, blood lactate, and respiratory exchange ratio were monitored throughout the test. Maximal workload was calculated using the following equation:
, where Wcom is the load of the last completed stage and t the time of the last incomplete stage (5).
Venous Blood Samples
Venous blood samples (10 ml) for the determination of serum hormone and CK concentrations were collected by a qualified laboratory technician, using sterile needles into serum tubes (Venosafe; Terumo Medical Co., Leuven, Hanau, Belgium). Whole blood was centrifuged at 3,500 rpm (Megafuge 1.0 R; Heraeus, Germany) for 10 minutes, after which serum was removed and stored at −80°C until analysis. Analyses of total serum T, serum C, serum GH, and serum thyroid-stimulating hormone (TSH) were performed using chemical luminescence techniques (Immulite 1000; Siemens, New York, NY, USA) and hormone-specific immunoassay kits (Siemens). The sensitivities for serum hormones were as follows: T, 0.5 nmol·L−1; C, 5.5 nmol·L−1; GH, 0.03 mIU·L−1, and TSH, 0.004 mIU·L−1. The intra-assay coefficients of variation were as follows: T, 8.5%; C, 4.6%; GH, 5.3%; and TSH, 3.9%. The interassay coefficients of variation were as follows: T, 14.2%; C, 6.1%; GH, 5.6%; and TSH, 8.9%.
Blood Lactate Concentrations
Capillary blood samples were taken from the fingertip at described time points. Blood lactate concentrations were analyzed using a Biosen lactate analyzer (S_line Lab+; EKF, Magdeburg, Germany).
Conventional statistical methods were used for the calculation of means and SDs. Before applying further statistical methods, data of both loading groups were checked for normality. Within-group differences for normally distributed variables were analyzed using repeated measures of analysis of variance with 5 levels (PRE, MID, POST, 24 hours, and 48 hours). Within-group differences for non-normally distributed variables were analyzed using the Wilcoxon signed-rank test, and p values were corrected for Bonferroni by multiplying all pairwise p values with the number of comparisons conducted for each variable. Between-loading comparisons for normally distributed variables were conducted using an independent sample t-test. If either of the 2 compared groups was not normally distributed, a nonparametric Mann-Whitney U-test was conducted. The statistical significance for all tests was set for a baseline of p ≤ 0.05, where *p < 0.05, **p < 0.01, and ***p < 0.001. Statistical analysis was conducted using IBM SPSS 19.0 (SPSS, Inc., Chicago, IL, USA).
The obtained values of the baseline measurements for strength (1RM, CMJbase, MVCmaxbase, MVC500base, and RFD10base) and endurance (V[Combining Dot Above]O2max and Workmax; Table 1) and preloading values of the same variables (Table 2) did not differ significantly between the 2 loading groups (p > 0.05). No significant differences were found in MVCmax, MVC500, RFD10, and CMJ between baseline and preloading values (p > 0.05). Fasting concentrations of serum hormones and CK (Table 3) did not differ significantly between both loading groups (p > 0.05). No significant differences in concentrations of serum hormones and CK measured in the fasting state and at preloading were found in the E + S loading group (p > 0.05). In the S + E loading group, concentrations of serum T and C were significantly lower at preloading compared with the fasting state (C: 472.3 ± 138 vs. 526.3± 108 nmol·L−1, p < 0.05; T: 12.8 ± 4.5 vs. 14.0 ± 3.8 nmol·L−1, p < 0.05).
Both loading groups showed similar reductions in body weight from PRE to POST (E + S: −1%, S + E: −1%, p > 0.05).
Strength and Power
Both the E + S and S + E loading groups induced significant acute reductions in MVCmax (Figure 2A) at MID (E + S: −14%, p < 0.001; S + E: −21%, p < 0.001) and POST (E + S: −27%, p < 0.001; S + E: −22%, p < 0.001) compared with PRE. The relative change in S + E at MID was somewhat larger than that of E + S (p = 0.056). The reduction from MID to POST was significant in E + S (−13%, p < 0.001) but not in S + E. In both loadings, MVCmax recovered significantly from POST to 24 hours (E + S: 22%, p < 0.001; S + E: +21%, p < 0.001) so that at 24 and 48 hours no significant differences compared with the preloading values were found. In both loading conditions, MVC500 (Figure 2B) was significantly reduced at POST (E + S: −26%, p < 0.001; S + E: −18%, p < 0.001) compared with PRE. In both loadings, MVC500 recovered significantly from POST to 24 hours (E + S: +17%, p < 0.001; S + E: 13%, p < 0.05), but the values remained significantly reduced compared with PRE in E + S (−9%, p < 0.01). There was a significant reduction in RFD10 at MID only in E + S (−21%, p < 0.01) and POST in both loadings (E + S: −32%, p < 0.001; S + E: −23%, p < 0.05). Also, RFD10 recovered from POST to 24 hours after both loading conditions (significant in E + S only, +30%, p < 0.01) so that both groups returned back to preloading values at 24 hours. Countermovement jump height (Figure 2C) was significantly reduced at MID only in S + E (−11%, p < 0.001). The difference between E + S and S + E at MID was, thus, significant (difference 7%, p < 0.01). Both loading conditions led to significant decreases in CMJ at POST (E + S: −15%, p < 0.001; S + E: −12%, p < 0.001) and recovered significantly from POST to 24 hours (E + S: +14%, p < 0.001; S + E: +8%, p < 0.05). No differences were found between the CMJ measures at 24 and 48 hours and preloading values in either of the loading conditions (p > 0.05).
Serum Hormone Concentrations
Total serum T concentration (Figure 3A) significantly increased in E + S at MID (+16%, p < 0.001) and remained slightly increased at POST (+7%, p > 0.05) compared with PRE. In S + E, serum T concentrations did not change at MID but were slightly increased at POST (+16% compared with MID, p < 0.01; +10% compared with PRE, p > 0.05). The difference between E + S and S + E at MID was significant (difference of 20%, p < 0.001). Serum T concentrations significantly decreased in E + S at 24 hours of recovery compared with POST (− 20%, p <0.05) and PRE (−13%, p < 0.05) and remained reduced at 48 hours (−18% compared with POST, p < 0.05; −11% compared with PRE, p = 0.068). Serum T concentrations in S + E were not significantly different from preloading values at 24 and 48 hours of recovery. Serum GH concentrations (Figure 3B) significantly increased in both loadings at MID (E + S: +242-fold, p < 0.001; S + E: +41-fold, p < 0.001) and increased further in S + E at POST (+7-fold compared with MID, p < 0.001; +272-fold compared with PRE, p < 0.001). In E + S, GH concentrations at POST were reduced compared with MID (−4-fold, p < 0.001) but remained elevated compared with PRE (+66-fold, p < 0.001). The differences between the loadings at MID and POST were significant (p < 0.001). No significant acute changes were observed for concentrations of serum TSH (Figure 3C) in either of the loadings at MID and POST. Serum TSH concentrations were significantly reduced at 24 hours compared with POST (E + S: −36%, p < 0.001; S + E: −22%, p < 0.05) and PRE (E + S: −32%, p < 0.001; S + E: −25%, p < 0.01) and remained reduced at 48 hours in E + S compared with POST (−19%, p < 0.001) and PRE (−25%, p < 0.001) and in S + E compared with PRE (−18%, p < 0.01). Concentrations of serum C (Figure 3D) did not change in E + S at MID and POST but were increased in S + E at POST compared with MID (+46%, p < 0.01). Serum C concentrations were significantly decreased at 24 hours of recovery compared with POST in S + E only (−54%, p < 0.05) and compared with PRE in both loading conditions (E + S: −21%, p < 0.01; S + E: −26%, p < 0.001) and remained reduced at 48 hours (E + S: −22%, p < 0.001; S + E: −29%, p < 0.001) compared with PRE.
Both loading conditions led to an increase in CK concentrations (Figure 4) at MID (E + S: +20%, p < 0.001; S + E: +16%, p < 0.001), which further increased at POST compared with MID (E + S: +12%, p < 0.001; S + E: +18%, p < 0.001) and PRE (E + S: +32%, p < 0.001; S + E: +34%, p < 0.01). The highest concentrations of CK were observed in both loadings at 24 hours of recovery (compared with PRE, E + S: +185%, p < 0.001; S + E: +95%, p < 0.001). The values remained significantly increased at 48 hours of recovery compared with PRE (E + S: +95%, p < 0.001; S + E: +50%, p < 0.01).
Blood Lactate Concentrations
Blood lactate concentrations measured before the start of the endurance loading were significantly higher in S + E compared with E + S (mean ± SD, 5.77 ± 2.09 vs. 1.58 ± 0.49 mmol·L−1, p < 0.001; Figure 5A). This difference was smaller after 10 minutes (7.82 ± 1.96 vs. 5.69 ± 1.98 mmol·L−1, p < 0.001) and further diminished after 20 minutes (7.60 ± 1.78 vs. 6.21 ± 2.52 mmol·L−1, p < 0.05) and was not significant at the end of the endurance loading (7.19 ± 1.99 vs. 6.28 ± 2.56 mmol·L−1, p > 0.05). Blood lactate concentrations obtained before the strength loading were significantly higher in E + S compared with S + E (4.48 ± 1.60 vs. 1.81 ± 0.61 mmol·L−1, p < 0.001), whereas no significant difference was found at post-strength loading (8.06 ± 2.62 vs. 7.45 ± 2.29 mmol·L−1, p > 0.05; Figure 5B).
This study investigated acute neuromuscular and endocrine responses and recovery to a single-session combined endurance and strength loading with 2 different exercise orders in moderately physically active men. The primary findings indicated that both loading orders led to similar significant reductions in maximal isometric force production, rapid force production produced in 500 ms, rate of force development, and power performance. Although these acute reductions in neuromuscular performance were recovered already at 24 hours, the present results showed that the time course of recovery of both neuromuscular performance and endocrine function differed. This was primarily shown by decreased concentrations of serum T and TSH still observed after 48 hours of recovery, particularly following the E + S loading order. These findings suggest that continuous cycling at moderate to high intensity performed immediately before a strength loading session consisting of various leg press protocols may considerably influence endocrine function during recovery.
Reductions in maximal and explosive neuromuscular performance have commonly been shown after both endurance (12,29,39) and strength (1,24,32) loadings. In the present study, the observed reductions of MVCmax in S + E at MID were larger than the observed reductions in E + S obtained at the same time point. Similarly, the reductions in MVC500 and CMJ height were somewhat larger at MID in S + E compared with E + S.
Typically, a strength training session with maximal loads leads to acute fatigue in the neuromuscular system, observed as dramatic decreases in maximal force production of the exercised muscles (15). Kraemer and Häkkinen (24) indicated that the magnitude of fatigue-induced decrements in neuromuscular performance is related to the overall volume, intensity, and recovery between the sets, whereas maximal loads combined with short resting intervals are likely to lead to the highest acute reductions in maximal force and power production.
Similarly to strength loading–induced reductions in force production, endurance performance may also produce neuromuscular fatigue. The magnitude of endurance exercise–induced impaired neuromuscular performance seems to be specific to the intensity of endurance exercise performed (12). Furthermore, it has been suggested that the exercise mode of the endurance loading performed has an impact on the acute alterations in neuromuscular function, although both differences (39) and similarities (30) between continuous and intermittent cycling protocols have been found. Because the largest reductions in neuromuscular performance have been obtained after prolonged repeated cycles of stretch-shortening exercises, observed in, for example, marathon running (33), the exercise mode seems to play a key role with regard to the magnitude of neuromuscular fatigue produced.
Possible reasons for reduced neuromuscular function in acute response to both strength and endurance exercises may generally be related to fatigue originating centrally, peripherally or from both. Changes in the contractile properties of the quadriceps muscle, shown by alterations of the M-wave and isometric muscular twitch (29); impaired calcium release from the sarcoplasmic reticulum (2); and ultrastructural lesions of muscle tissue (33) have been shown to affect force production during fatigue. However, because in the present study no deeper analysis of neuromuscular function was conducted (e.g., electromyographic, muscle and nerve stimulation) and the loading did not involve high-impact stretch-shortening type of exercise, as, for example, expressed by the low values of CK, the reasons for the impaired neuromuscular performance after both strength and endurance exercises remain speculative. It is also possible that blood lactate accumulation and the resulting lowered blood pH observed in the present study have inhibited the rate of cross-bridge binding, as previously shown by Sahlin (37), which then may have inhibited force production.
In the present study, the observed difference in reduction of neuromuscular performance between loading conditions at MID disappeared after both combined loadings were completed. However, the decrements in explosive and maximal force production at POST were somewhat higher in E + S compared with S + E and, in fact, significantly reduced compared with MID, whereas neuromuscular performance remained decreased after the opposite loading order. It appears that higher reductions in MVCmax, MVC500, RFD10, and CMJ were caused by the strength loading rather than the endurance cycling, but caution must be paid when applying these findings to loading protocols other than the protocol used in the present study. Cycling does not involve stretch-shortening mechanics and, thus, may not lead to comparable ultrastructural muscle tissue lesions as observed after, for example, long-distance running (33). This, in turn, might explain that in the present study, only small differences in acute changes of neuromuscular performance between both loading conditions were found.
The present study did not show differences in the level of recovery in neuromuscular performance between E + S and S + E. After both loading conditions, preloading values of MVCmax, MVC500, RFD10, and CMJ were obtained mainly already after 24 hours of recovery. Decreases in force production for up to 2–3 days have been reported by Häkkinen (14) and Ahtiainen et al. (1) after extremely strenuous bouts of bilateral dynamic leg press, with an acute decrease in maximal force down to 60% of the maximal force. After endurance exercises such as a marathon run, maximal force has been shown to recover already after 24 hours, whereas explosive force production may remain reduced for at least 2 days (33,34). Relative acute decreases of maximal and explosive force in the present study were comparably small, and thus, neuromuscular recovery was mainly completed already after 24 hours, with no noteworthy differences between both groups.
Changes in neuromuscular performance are commonly accompanied by alterations in endocrine function. Moderate to high intensity of both strength and endurance loadings elicit remarkable acute responses in both anabolic and catabolic hormonal concentrations (15,22,23,40). The most prominent findings of the present study were the significant increase of serum T concentrations at MID in E + S, and the decrease of serum T concentrations after the E + S loading and TSH and C after both loading conditions at 24 and 48 hours of recovery.
Testosterone, as an anabolic steroid, plays a major role in energy metabolism and has been identified to promote tissue repair and muscle growth. Elevated concentrations of anabolic steroids in response to an exercise training session have been typically associated with beneficial effects on maximal strength and muscle growth (23). The highest concentrations of serum T are generally observed after heavy resistance loadings with short resting intervals that are characterized by high metabolic stress (17,23). Whereas endurance loadings of shorter durations have been shown to acutely increase concentrations of anabolic hormones, high-intensity endurance exercise of prolonged duration may lead to reductions in concentrations of T (40).
Because in the present study significant increases in serum T concentrations were found at MID in E + S, elevations in T concentrations might have been induced by the endurance loading. The present endurance protocol consisted of continuous cycling of moderate to high intensity. As the subjects were moderately physically active and remarkable changes in neuromuscular fatigue were observed in E + S at MID, the present data suggest that the cycling performance required not only cardiorespiratory ability but also, to a great extent, continuous muscular effort, produced especially by the quadricep muscles, leading to increases in serum T concentrations. The strength loading, in contrast, consisted of various protocols, and particularly the neural type of resistance loadings with resting periods of 3 minutes may not be sufficient enough to induce noticeable changes in serum T concentrations (31). This may explain the observed difference between the loading groups at MID.
Serum T concentrations observed at POST did not significantly differ from the preloading values in the loading groups, which is in contrast to findings of Cadore et al. (5) who found T levels to be increased after an S + E loading in young strength-trained men. In the present study, however, serum T concentrations remained unaltered in S + E but significantly decreased in E + S at 24 and 48 hours. Interestingly, whereas neuromuscular performance in the present study was mainly recovered already after 24 hours in both loading groups, serum T responses remained reduced after the E + S loading for up to 2 days.
However, the observed decrease of TSH concentration during recovery, which was somewhat larger in E+S compared with S+E, underline the possibility of delayed alteration in endocrine function particularly after the E+S loading order. Thyroid hormones, and in particular TSH, play a major role in thermoregulation and energy metabolism but have also been shown to indirectly promote protein metabolism and tissue remodeling (38). Both endurance and strength exercises performed separately may induce acute elevations of TSH concentrations (3,6), and the magnitude of this alteration seems to be directly related to the exercise intensity (6). Because in the present study no acute alterations in concentrations of TSH were observed in either of the loading conditions, these findings may suggest that the current combined loadings were not intensive enough to acutely stimulate thyroid function. The observed decrease of TSH concentration during recovery, which was somewhat larger in E + S compared with S + E, however, underline the possibility of delayed alterations in endocrine function particularly after this loading order.
The obtained results of neuromuscular performance and changes in serum T and TSH concentrations generally provide evidence for differences in the time course of recovery between the neuromuscular performance and endocrine function. A similar phenomenon has been observed in strength athletes after an excessively strenuous strength loading session (17). The present data suggest that in moderately physically active men, continuous cycling immediately followed by a combined neural and hypertrophic strength loading session develops a state of endocrine imbalance during recovery, which is mainly reflected by decreased concentrations of serum T and TSH. Although the main cause of this observation remains speculative, it is plausible that reduced concentrations of T and TSH, especially after the E + S loading order, indicate upregulation of receptors and, thus, enhanced utilization. That would make the E + S loading order more demanding when compared with the S + E loading, leading to prolonged needs of recovery. However, in the present study, androgen receptor content was not measured, and thus, the mechanisms behind these observations remain speculative. Furthermore, whether this decrease was caused by increased needs of T for tissue remodeling and repair or, in contrast, a possibly impaired endocrine function, particularly of the pituitary gland or hypothalamus, cannot be explained by the present data. When considering the present results, one must also bear in mind that hormonal concentrations follow a circadian rhythm and considerable changes in T concentrations are generally observed particularly in the morning hours (25).
The present study did not lead to significant acute changes in concentrations of serum C compared with preloading values in either of the loading conditions. During recovery, however, the concentrations of serum C significantly decreased and remained low for at least 48 hours after both loading conditions. Previous research has shown that serum C concentrations are likely to return to baseline levels already within 2 hours after a heavy strength training session (18). After endurance exercise, however, concentrations of C have been shown to be significantly decreased after 24 hours of recovery (8). Although diurnal variations of C may potentially account for observed decreased concentrations during recovery (36), other mechanisms such as increased receptor binding or a suppressed function of the adrenal gland during recovery are possible and would underline the evidence for altered or impaired endocrine function after a combined endurance and strength loading session.
Although the loading conditions in this study led to only moderate or no increase in anabolic T and TSH and catabolic C concentrations, somewhat surprising was the magnitude of observed increases of GH concentrations in both loadings, which reached peak values considerably higher than reported in previous studies obtained immediately after endurance (35) and strength loadings only (31). Whereas some studies have shown that the magnitude of changes in GH concentrations seems to depend on intensity and volume of the exercise performed (35), other external factors such as sleep and nutrition (11) may influence acute changes in GH concentrations. Moreover, the release of GH generally occurs in a pulsatile pattern, and additional factors such as hypoxia and breath holding may have an influence on GH release and might have accounted for the observed GH concentrations in the present subjects.
Interestingly, the loading-induced significant increases in serum GH concentrations in E + S were significantly higher at MID and significantly lower at POST when compared with S + E. The present results may, thus, suggest that cycling performed first in a combined exercise session may blunt GH responses caused by strength exercises performed in the second half of the training session, a phenomenon also observed by Goto et al. (13). However, although previous studies have suggested GH release to be possibly suppressed by the accumulation of free fatty acids (13) or insulin-like growth factor-1 (21), the present data do not provide a thorough insight into the possible mechanisms behind this observation.
In conclusion, this study showed that the 2 combined endurance and strength loadings with different exercise orders led to similar acute responses in maximal and explosive force production and endocrine function in moderately physically active young men. However, although a similar recovery of neuromuscular performance in both loading groups already after 24 hours was observed, serum hormonal concentrations of T, TSH, and C remained decreased during recovery for at least 48 hours, particularly when endurance cycling was immediately followed by a strength loading session. The current loading conditions consisting of continuous cycling and various bilateral leg press protocols, thus, led to different recovery time courses between neuromuscular performance and endocrine function. It needs to be, however, considered that these results are limited to the current loading conditions of using various leg press protocols and continuous cycling, a training regimen typically used for inexperienced subjects. Thus, great care must be taken when evaluating the practical applications of these findings for other types of loading conditions and for athletic populations.
The present findings generally indicate that a complete recovery after a single-session combined endurance and strength loading may take longer than indicated by the measures of strength performance only. Because endocrine function may be altered for at least 48 hours after these strenuous exercises, the measures of neuromuscular performance may not be sufficient to detect a true recovery status. When comparing the 2 loading orders, the present results showed that after the E + S loading, the serum T concentrations were significantly reduced during the recovery for up to 48 hours, whereas the serum T concentrations after the S + E loading were not different from the concentrations measured at baseline. The present results, thus, indicate that the current E + S loading seemed to require a longer recovery when compared with the S + E loading, which may become important when performing single-session combined endurance and strength training. However, additional research is necessary to investigate the relevance of the present findings with regard to prolonged training adaptations and athletic populations.
The authors express their gratitude to the Faculty of Sport and Health Sciences at the University of Jyväskylä, Finland, for their partial financial support to this project. Furthermore, the authors acknowledge the technical staff of the Department of Biology of Physical Activity involved in the project and the subjects who volunteered to make this project possible.
1. Ahtiainen JP, Pakarinen A, Kraemer WJ, Häkkinen K. Acute hormonal and neuromuscular responses and recovery to forced vs. maximum repetitions multiple resistance exercises. Int J Sports Med 24: 410–418, 2003.
2. Allen DG, Lamb GD, Westerblad H. Impaired calcium release during fatigue. J Appl Physiol 104: 296–305, 2008.
3. Alvero-Cruz J, Ronconi M, Gil MCDA, Garcia Romero JC, Velazquez DR, Acosta AMDD. Thyroid hormones response in simulated laboratory sprint duathlon. J Hum Sport Exerc 6: 323–327, 2011.
4. Bosco C, Luhtanen P, Komi PV. Simple method for measurement of mechanical power in jumping. Eur J Appl Physiol 50: 273–282, 1983.
5. Cadore E, Izquierdo M, Goncalves dos Santos M, Martins J, Lhullier L, Pinto R, Silva RF, Kruel LFM. Hormonal responses to concurrent strength and endurance training with different exercise orders. J Strength Cond Res 26: 3281–3288, 2012.
6. Ciloglu F, Peker I, Pehlivan A, Karacabey K, Ilhan N, Saygin O, Ozmerdivenli R. Exercise intensity and its effects of thyroid hormones. Neuro Endocrinol Lett 26: 830–834, 2005.
7. Craig BW, Lucas J, Pohlman R, Stelling H. The effects of running, weightlifting and a combination of both on growth hormone release. J Appl Sport Sci Res 5: 198–203, 1991.
8. Daly W, Seegers CA, Rubin D, Dobridge JD, Hackney AC. Relationship between stress hormones and testosterone with prolonged endurance exercise. Eur J Appl Physiol 93: 375–380, 2005.
9. Denadai BS, Greco CC, Tufik S, de Mello MT. Effects of high intensity running to fatigue on isokinetic muscular strength in endurance athletes. Isokin Exerc Sci 15: 281–285, 2007.
10. De Souza EO, Tricolli V, Franchini E, Paulo AC, Regazzini M, Ugrinowitschi C. Acute effect of two aerobic exercise modes on maximum strength and strength endurance. J Strength Cond Res 21: 1286–1290, 2007.
11. Giustina A, Veldhuis JD. Pathophysiology of the neuroregulation of growth hormone secretion in experimental animals and the human. Endocr Rev 19: 717–797, 1998.
12. Gleeson N, Reilly T, Mercer T, Rakowski S, Rees D. Influence of acute endurance activity on leg neuromuscular and musculoskeletal performance. Med Sci Sports Exerc 30: 596–608, 1998.
13. Goto K, Higashiyama M, Ishii N, Takamatsu K. Prior endurance exercise attenuates growth hormone response to subsequent resistance exercise. Eur J Appl Physiol 94: 333–338, 2005.
14. Häkkinen K. Neuromuscular fatigue and recovery in male and female athletes during heavy resistance exercise. Int J Sports Med 14: 53–59, 1993.
15. Häkkinen K. Neuromuscular fatigue in males and females during strenuous heavy resistance loading. Electromyogr Clin Neurophysiol 34: 205–214, 1994.
16. Häkkinen K, Alen M, Kraemer WJ, Gorostiaga E, Izquierdo M, Rusko H, Mikkola J, Hakkinen A, Valkeinen H, Kaarakainen E, Romu S, Erola V, Ahtiainen J, Paavolainen L. Neuromuscular adaptations during concurrent strength and endurance training versus strength training. Eur J Appl Physiol 89: 42–52, 2003.
17. Häkkinen K, Pakarinen A. Acute hormonal responses to two different fatiguing heavy resistance protocols in male athletes. J Appl Physiol 74: 882–887, 1993.
18. Häkkinen K, Pakarinen A. Acute hormonal responses to heavy resistance exercise in men and women at different ages. Int J Sports Med 16: 507–513, 1995.
19. Hickson RC. Interference of strength development by simultaneously training for strength and endurance. Eur J Appl Physiol 45: 255–263, 1980.
20. Izquierdo-Gabarren M, Gonzalez De Txabarri Exposito R, Garciapallares J, Sanchezmedina L, De Villareal E, Izquierdo M. Concurrent endurance and strength training not to failure optimizes performance gains. Med Sci Sports Exerc 42: 1191–1199, 2010.
21. Jaffe C, Ocambo-Lim B, Guo W, Krueger K, Sugahara I, De-Mott-Friberg R, Bermann M, Barkan AL. Regulatory mechanisms of growth hormone secretion are sexually dimorphic. J Clin Invest 102: 153–164, 1998.
22. Karkoulias K, Habeos I, Charokopos N, Tsiamita M, Mazarakis A, Poulia A, Spiropoulos K. Hormonal responses to marathon running in non-elite athletes. Eur J Intern Med 19: 598–601, 2008.
23. Kraemer WJ, Gordon SE, Fleck SJ, Marchitelli LJ, Mello R, Dziados JE, Friedl K, Harman E, Maresh C, Fry AC. Endogenous anabolic hormonal and growth factor responses to heavy resistance exercise in males and females. Int J Sports Med 12: 228–235, 1991.
24. Kraemer WJ, Häkkinen K. Strength Training for Sport. New York: Blackwell Science Ltd., 2002.
25. Kraemer WJ, Loebel C, Volek J, Ratamess N, Newton R, Wickham R, Gotshalk L, Duncan N, Mazzetti S, Gómez A, Rubin M, Nindl BC, Häkkinen K. The effect of heavy resistance exercise on the circadian rhythm of salivary testosterone in men. Eur J Appl Physiol 84: 13–18, 2001.
26. Kraemer WJ, Patton JF, Gordon SE, Harman EA, Deschenes MR, Reynolds K, Newton RU, Triplett NT, Dziados JE. Compatibility of high-intensity strength and endurance training on hormonal and skeletal muscle adaptations. J Appl Physiol 78: 976–989, 1995.
27. Kraemer WJ, Ratamess NA. Hormonal responses and adaptations to resistance exercise and training. Sports Med 35: 339–361, 2005.
28. Leveritt M, Abernethy PJ. Acute effects of high-intensity endurance exercise on subsequent resistance activity. J Strength Cond Res 13: 47–51, 1999.
29. Lepers R, Hausswirth C, Maffiuletti N, Brisswalter J, Van Hoecke J. Evidence of neuromuscular fatigue after prolonged cycling exercise. Med Sci Sports Exerc 32: 1880–1886, 2000.
30. Lepers R, Theurel J, Hausswirth C, Bernard T. Neuromuscular fatigue following constant versus variable-intensity endurance cycling in triathletes. J Sci Med Sport 11: 381–389, 2008.
31. Linnamo V, Pakarinen A, Komi PV, Kraemer WJ, Häkkinen K. Acute hormonal responses to submaximal and maximal heavy resistance and explosive exercises in men and women. J Strength Cond Res 19: 566–571, 2005.
32. McCaulley GO, McBride JM, Cormie P, Hudson MB, Nuzzo JL, Quindry JC, Triplett NT. Acute hormonal and neuromuscular responses to hypertrophy, strength and power type resistance exercise. Eur J Appl Physiol 105: 695–704, 2009.
33. Nicol C, Komi PV, Marconnet P. Fatigue effects of marathon running on neuromuscular performance. 1. Changes in muscle force and stiffness characteristics. Scand J Med Sci Sports 1: 10–17, 1991.
34. Petersen K, Hansen C, Aagaard P, Madsen K. Muscle mechanical characteristics in fatigue and recovery from a marathon race in highly trained runners. Eur J Appl Physiol 101: 385–396, 2007.
35. Pritzlaff CJ, Wideman L, Weltman JY, Abbott RD, Gutgesell ME, Hartman ML, Veldhuis JD, Weltman A. Impact of acute exercise intensity on pulsatile growth hormone release in men. J Appl Physiol 87: 498–504, 1999.
36. Rohatagi S, Bye A, Mackie AE, Derendorf H. Mathematical modeling of cortisol circadian rhythm and cortisol suppression. Eur J Pharm Sci 4: 341–350, 1996.
37. Sahlin K. Muscle fatigue and lactic acid accumulation. Acta Physiol Scand 128: 83–91, 1986.
38. Silvestri E, Schiavo L, Lombardi A, Goglia F. Thyroid hormones as molecular determinants of thermogenesis. Acta Physiol Scand 184: 265–283, 2005.
39. Theurel J, Lepers R. Neuromuscular fatigue is greater following highly variable versus constant intensity endurance cycling. Eur J Appl Physiol 103: 461–468, 2008.
40. Tremblay MS, Chu SY, Mureika R. Methodological and statistical considerations for exercise-related hormone evaluations. Sports Med 20: 90–108, 1995.