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Journal of Clinical Endocrinology & Metabolism, doi:10.1210/jc.2004-1209
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The Journal of Clinical Endocrinology & Metabolism Vol. 90, No. 6 3268-3273
Copyright © 2005 by The Endocrine Society

Short-Term Administration of Supraphysiological Recombinant Human Growth Hormone (GH) Does Not Increase Maximum Endurance Exercise Capacity in Healthy, Active Young Men and Women with Normal GH-Insulin-Like Growth Factor I Axes

Annika Berggren, Christer Ehrnborg, Thord Rosén, Lars Ellegård, Bengt-Åke Bengtsson and Kenneth Caidahl

Departments of Clinical Physiology (A.B., K.C.), Endocrinology (C.E., T.R., B.-Å.B.), and Clinical Nutrition (L.E.), Sahlgrenska University Hospital, SE-41345 Göteborg, Sweden; and Karolinska Institute (K.C.), SE-171 76 Stockholm, Sweden

Address all correspondence and requests for reprints to: Dr. Kenneth Caidahl, Karolinska University Hospital, N2:01, SE-171 76 Stockholm, Sweden. E-mail: kencai{at}ki.se.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Context: Despite the fact that the use of GH as a doping agent in sports is widespread, little is known about its short-term effects.

Objective: The objective was to study the effects of GH on exercise capacity.

Design: A double-blind, placebo-controlled study was used, with a treatment period of 28 d.

Setting: Subjects from general community studied ambulatory at a university hospital.

Participants: Thirty healthy active young normal volunteers (15 women and 15 men) were recruited by local announcement, and all completed the study.

Intervention: All subjects were randomized to receive a low GH dose (0.033 mg/kg·d or 0.1 IU/kg·d), a high GH dose (0.067 mg/kg·d or 0.2 IU/kg·d), or placebo.

Main outcome measures: Power output and oxygen uptake on bicycle exercise were the main outcome measures.

Results: We found no effect of the low or high dosages of GH on maximum oxygen uptake during exercise (mean ± SE for placebo, 45.2 ± 1.6 to 45.2 ± 2.1 ml/kg·min; GH low dose, 42.8 ± 1.6 to 42.8 ± 1.6 ml/kg·min; GH high dose, 44.8 ± 3.4 to 44.8 ± 2.2 ml/kg·min; not significant by two-way ANOVA). Neither was there any effect on maximum achieved power output during exercise or on blood pressure, heart rate, or the electrocardiographic ST level at rest or during exercise. GH significantly increased total body weight (P = 0.028), an effect predominantly ascribed to fluid retention (increased extracellular water volume), whereas muscle mass (as indicated by intracellular water volume) did not change. However, changes in the latter correlated to changes in physical performance, possibly due to different training efforts.

Conclusion: Administration of supraphysiological recombinant human GH during a period of 4 wk does not improve power output or oxygen uptake.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
GH HAS BEEN used extensively as a doping agent, because it is believed to shorten the time required to obtain a sturdy biceps by bodybuilders or to enhance the performance of cyclists or swimmers. In GH-deficient adults, it has been demonstrated that GH increases protein synthesis and improves muscle performance, including exercise capacity (1, 2, 3, 4, 5, 6). Physical training has been shown to change circulating levels of GH and, more inconsistently, IGF-I in normal subjects in relation to improvement in oxygen uptake and muscle strength (7, 8, 9, 10). To date, no study has demonstrated a beneficial effect of exogenous GH on exercise capacity in normal active subjects. We therefore investigated the effect of high dosages of GH in this type of individual to determine the usefulness of GH as a short-term doping agent. We have evaluated the cardiovascular short-term (28-d) effects of doping doses of recombinant human GH (rhGH) in normal fit subjects as part of the GH-2000 Project, which was aimed at detecting GH abuse in sports (11).


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Subjects

Thirty healthy active subjects, who were not professional athletes, were selected. We chose 15 women (mean age, 25 yr; range, 21–30 yr) and 15 men (mean age, 27 yr; range, 18–35 yr). None of the subjects was receiving medical treatment or had a previous history of cardiopulmonary, autonomic, or neuromuscular diseases. All subjects were normotensive (blood pressure, <150/90 mm Hg), and physical examination revealed no abnormalities at the time of the study. The exclusion criteria consisted of any disease state. Females underwent a pregnancy test. All subjects were fit, meaning that they had taken part in a minimum of two training sessions a week for at least 1 yr. Informed consent was obtained, and the study was approved by the ethics committee at Goteborg University.

Exercise electrocardiogram

Computerized bicycle exercise electrocardiograms were performed using previously described technology developed at our hospital (12, 13). This includes the consecutive averaging of 10-sec intervals of the electrocardiographic signal. The ST level is measured automatically 60 msec after the end of the QRS complex. The computer program was developed locally and run on a standard personal computer. A bicycle ergometer (RE 820/830, Rodby Innovation AB, Södertälje, Sweden), with automatic load increase was used.

Oxygen uptake

An ergospirometer Vmax 29c (Sensor Medics Corp., Yorba Linda, CA) was used for gas exchange measurements. This measures tidal volume breath by breath using a flow sensor, i.e. an anemomter based on cooling a heated wire by the gas flow. The stated accuracy is ±3%. The mass flow sensor was calibrated with a calibration syringe.

Oxygen tension in inspired and mixed expired gas was analyzed using a paramagnetic oxygen sensor. Carbon dioxide tension in inspired and mixed expired gas was analyzed using an infrared absorption sensor; both had a response time less than 130 msec and an accuracy of ±0.02% (14, 15).

The gas analyzers were calibrated with two calibrated gases containing 16% O2 and 4.0% CO2, and 26.0% O2 and 0.0% CO2. Oxygen uptake (VO2) and minute ventilation were calculated breath by breath, and we used the mean value for the last 30 sec (16).

The VO2 at peak exercise (VO2 max) was determined using a bicycle with increasing load. The test was terminated at the point of subjective exhaustion. The minute ventilation, VO2, O2 pulse (oxygen pulse = VO2 per heart beat), carbon dioxide production, anaerobic threshold [by V slope method (17)], and respiratory quotient were determined.

VO2 max (peak) was regarded as being achieved if the test met two of the following criteria: 1) respiratory quotient greater than 1.0, 2) heart rate ±10 beats/min of age-predicted maximum, and 3) plateau in oxygen uptake with increasing workload. The volunteers were asked to breathe through a mouthpiece connected to a Sensor Medics Vmax 29c metabolic computer. All volunteers breathed room air.

IGF-I

Serum was stored at –80 C until analysis. Serum IGF-I was measured by RIA with a monoclonal antibody after acid-ethanol extraction, using authentic IGF-I for labeling (Nicholas Institute Diagnostics, San Juan Capistrano, CA) with intraassay coefficients of variation of 10.1%, 6.3%, and 5.7% at serum concentrations of 61.5, 340.8, and 776.9 µg/liter, respectively. The analyses were performed by Per-Arne Lundberg at Sahlgrenska University Hospital (Göteborg, Sweden).

Intracellular (ICW) and extracellular (ECW) water volumes

ICW and ECW were also determined using multifrequency bioelectrical impedance analysis spectroscopy (18). In short, reactance and resistance were determined with a 4000B Bio-Impedance Spectrum Analyzer (Xitron Technologies, San Diego, CA). The extracellular resistance and the total body water resistance were predicted and combined with body weight, height, and resistivity of ECW and ICW to calculate the total body water volume (TBW) and ECW. ICW was calculated as the ECW subtracted from the TBW (ICW = TBW – ECW).

Protocol

After a baseline evaluation, a complete history was obtained, and a physical examination was performed in all subjects. Female subjects underwent a pregnancy test. The subjects were randomized, with an even gender distribution in groups, to placebo (n = 10), 0.033 mg/kg·d or 0.1 IU/kg·d GH (n = 10), or 0.067 mg/kg·d or 0.2 IU/kg·d GH (n = 10). The treatment was administered for 28 d, and evaluations were performed before and at the end of the treatment period. Evaluations were made in terms of computerized electrocardiography recordings during bicycle exercise test starting at 70 watts with an increase in load of 20 watts each minute. Concomitant sampling and analysis of breathing gases were performed. Systolic and diastolic blood pressures were measured at rest in the supine position and sitting on the bicycle before and after the test. Systolic pressure was measured each minute throughout the test. Blood for analysis of IGF-I was collected at baseline and on d 28 of treatment.

Statistical evaluations

The data are presented as the mean ± SD for background variables and the mean ± SE for the study measures. The significance of differences between treatment groups was evaluated by ANOVA for changes from baseline to 28 d treatment values. Post hoc test (Bonferroni) was applied in the case of significant group differences. Due to low numbers, possible gender differences were not statistically tested, but are graphically illustrated in Figs. 3Go and 4Go. Pearson’s correlation coefficients were computed to evaluate relationships between changes in IGF-I, ICW, or ECW and changes in measures of exercise capacity.



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  		FIG. 3. Average maximum power output (±SE) in the same three study groups as those described in Fig. 1Go. F, Female; M, male.

 


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  		FIG. 4. Average oxygen consumption (±SE) in the same three study groups as those described in Fig. 1Go. F, Female; M, male.

 

   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
The demographic, metabolic, and cardiorespiratory findings are listed in Tables 1Go and 2Go. There were no drop-outs from the study. The 30 subjects completed 1 month of treatment. Transient fluid retention and increased sweating were reported side effects (Table 3Go). We reduced the dose for two of the subjects. There was no change in height, but the body weight was significantly altered; GH treatment caused an increase in weight (Table 1Go). This increase in weight could be explained by an increase in ECW, and neither correlated to VO2 max or power output. In contrast, individual changes in ICW correlated to VO2 max (r = 0.41; P < 0.05) and power output (r = 0.45; P = 0.02), but changes in ICW were not attributable to GH treatment. Thus, ICW did not differ significantly between treatment groups (Table 1Go), and there was no significant relation to changes in IGF-I, whereas changes in ECW were strongly related to changes in IGF-I (r = 0.66; P < 0.0001). No significant alteration was found in heart rate or blood pressure at rest, although there was a tendency toward differences in diastolic blood pressure between groups, with lower values in the high GH group compared with placebo and low GH groups (Table 1Go). In the placebo group, IGF-I did not change during treatment. IGF-I rose by 67% in the low dose group and more markedly (135%) in the high dose GH group (Table 1Go).


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  		TABLE 1. Background variables

 

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  		TABLE 2. Measures of exercise reaction

 

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  		TABLE 3. Side effects in the three treatment groups

 
We found no relationship between changes in IGF-I and changes in oxygen uptake or maximum achieved power output. Neither at rest nor during exercise was there a significant difference in the electrocardiographic ST level between treatment groups (Table 2Go). There was no significant difference between the groups in maximum heart rate response to treatment. We saw no effect of treatment on systolic blood pressure at maximum exercise, nor was there any difference between groups in O2 pulse, carbon dioxide production, anaerobic threshold, or maximum expired volume. Importantly, we found no effect by low or high dosages of GH on maximum achieved power output during exercise. Some individuals in each group displayed a slight increase in achieved power output (Fig. 1Go). There was no effect on maximum oxygen uptake (Table 2Go); the individual response of weight-adjusted VO2 is shown in Fig. 2Go. The individual gender response is illustrated in Figs. 1Go and 2Go. No systematic difference in gender response was noted, and the lack of such is also illustrated by the average values in Figs. 3Go and 4Go.



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  		FIG. 1. Maximum power output at baseline (B) and after 28 d of treatment (1 mth) in the placebo group and in the low dose GH group (0.033 mg/kg·d or 0.1 IU/kg·d) and the high dose GH group (0.067 mg/kg·d or 0.2 IU/kg·d). {circ}, Males; •, females.

 


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  		FIG. 2. VO2 max at baseline (B) and after 28 d of treatment (1 mth) in the same three study groups as those described in Fig. 1Go (for symbols, see Fig. 1Go).

 

   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
In the present study, short-term GH administration did not cause any increase in maximum power output or maximum oxygen uptake despite the administration of supraphysiological doses of GH and an increase in circulating IGF-I. Thus, high doses of GH do not appear to improve aerobic exercise capacity or oxygen uptake in active normal subjects.

There is no published evidence that GH leads to an improvement in aerobic exercise capacity in non-GH-deficient subjects (19). On the contrary, Lange et al. (20) suggested that a single relevant GH dose in combination with bicycling exaggerate plasma lactate and may be associated with a reduction in aerobic exercise capacity. A recent study of acute GH administration before exercise demonstrated no effect on total work, caloric expenditure, blood lactate, or perceived exertion, but a lower exercise oxygen consumption (21). Animals treated with GH do not appear to improve their muscle strength, and acromegalic patients may have functionally weak muscles even though they are outwardly hypertrophied (22). The use of anabolic steroids in an effort to improve athletic performance has been well documented (23). Among body builders and athletes, there is also a belief that supraphysiological doses of GH will enhance their physical appearance and performance (Committee on the Judiciary, U.S. Senate: Drug Misuse: Anabolic Steroids and Human Growth Hormone). The same document states that anecdotal reports suggest that GH may actually be preferred to anabolic steroids, because it is not easily detectable with current drug-testing protocols.

In the current study, as expected, we found increased levels of IGF-I in our treated groups, but we found no correlation between IGF-I and VO2 or maximum achieved power output. This accords with the lack of correlation between peak weight corrected VO2 and endogenous IGF-I or IGFBP-3 demonstrated by Eliakim et al. (10) in normal male subjects. Although plasma IGF-I levels not invariably reflect IGF-I bioactivity, they are in some studies related to peak VO2 (8, 9). However, these studies did not evaluate the effect of supraphysiological levels of GH and IGF-I on VO2 and the way they affect maximum power. Instead, VO2 was more of a correlate for fitness, and because GH increases during exertion, it is likely to be related to VO2 (24). A correlation between endogenous GH and VO2 in healthy young adults has been ascribed to degree of fitness (25), but age seems to be a concomitant factor for relationships to the GH-IGF-I axis (25, 26). The achieved peak VO2 has been found to be more closely related to the 24-h integrated serum GH concentration in male than in female subjects (25), whereas no gender difference was found in its age-dependent relation to a single measure of IGF-I (26). During exercise, the stimulation of GH secretion seems to be greater in women than in men (24). In contrast, we previously demonstrated in the current study population that, in terms of IGFBP-3, male subjects are more responsive than females to exogenous GH (11). Although the study lacks statistical power to test gender differences, we did not note any tendency to such with regard to maximum aerobic exercise capacity in response to supraphysiological GH treatment.

In the current study we did not evaluate all aspects of physical performance, e.g. maximum voluntary muscle strength and flexibility. However, it has been shown that in healthy subjects, even in highly trained power athletes, muscle strength does not improve after GH administration (27, 28, 29). Supraphysiological doses of rhGH may also suppress the exercise-stimulated endogenous circulating levels of GH (30) and evoke equivocal effects on the already enhanced muscle protein synthesis induced by the training itself (29, 31). In contrast, replacement therapy in GH deficiency improves reduced ventilatory function and oxygen uptake (32, 33). Furthermore, a beneficial effect of GH replacement has been noted on exercise capacity and perceived maximum power output (1, 6, 33), changes normally related to an increase in muscle mass and lean body mass (1, 2, 6). However, an increase in muscle protein synthesis may not necessarily cause an increase in muscle strength (34). Moreover, it has been demonstrated that GH-deficient adults benefit from resistance training even without replacement therapy (35, 36). Effects other than muscular, from administered GH as well as from training, may be important for work performance. In addition to its direct effects on cardiac and pulmonary muscles in GH deficiency, GH replacement is known to have profound effects on fuel metabolism (37), erythropoiesis, and total blood volume (38), but studies of such effects in healthy trained subjects are lacking. Previous findings by Deyssig et al. (27) do not suggest a muscle strength performance-enhancing effect by low dose GH administration in already trained adults. Probably due to the comparatively low dose, they achieved no total body weight gain after GH treatment, in contrast to our results. However, the weight gain after GH administration in our study was at least partly caused by an increase in ECW and not muscle mass. This could explain why we found no evidence of a positive effect on maximum aerobic exercise capacity in the present study despite the use of a high GH dosage. Small changes in ICW, independent of GH treatment, might be due to different physical exercise habits; some individuals in the various groups may have made an effort to improve their test results. An indication of this is the approximately 10-watt higher power output in each group on the second occasion.

Thus, we saw no beneficial effects of rhGH administration on aerobic exercise capacity in active healthy subjects, only water retention. This indicates that only untoward effects can be anticipated from GH abuse (39, 40). Rather, we suggest that a normal level of GH is required for maximum muscle performance to be achieved. The improvement produced by GH substitution in GH deficiency (1) and the comparatively poor exercise performance in acromegalics (22) support this theory.


   Acknowledgments
 
This study was performed in connection with the GH-2000 antidoping project, a research program performed within the competitive EU BioMed2 Research Program, initiated by the International Olympic Committee and the European Union. We are grateful to Elisabeth Aspenlid, Ann-Christin Karlsson, Ingrid Hansson, Sigrid Lindstrand, and Lena Wirén for technical assistance.


   Footnotes
 
This work was supported by the Swedish Heart-Lung Foundation, the Swedish Medical Research Council (14231), Göteborg University, the Göteborg Medical Society, and the Sahlgrenska Foundation.

First Published Online March 22, 2005

Abbreviations: ECW, Extracellular water volume; ICW, intracellular water volume; rhGH, recombinant human GH; TBW, total body water volume; VO2, oxygen uptake; VO2 max, VO2 at peak exercise.

Received June 24, 2004.

Accepted March 15, 2005.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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M. L. Healy, J. Gibney, C. Pentecost, P. Croos, D. L. Russell-Jones, P. H. Sonksen, and A. M. Umpleby
Effects of High-Dose Growth Hormone on Glucose and Glycerol Metabolism at Rest and during Exercise in Endurance-Trained Athletes
J. Clin. Endocrinol. Metab., January 1, 2006; 91(1): 320 - 327.
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