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Effect of Muscle Oxygenation during

Resistance Exercise on Anabolic Hormone
Response

Article in Medicine & Science in Sports & Exercise November 2003

DOI: 10.1249/01.MSS.0000093613.30362.DF Source: PubMed

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Effect of Muscle Oxygenation during
Resistance Exercise on Anabolic
Hormone Response
JAY R. HOFFMAN1, JOOHEE IM2, KENNETH W. RUNDELL3, JIE KANG1, SHOKO NIOKA2,
BARRY A. SPEIRING3, RYOTO KIME2, and BRITTON CHANCE2
1
The College of New Jersey, Ewing, NJ; 2Department of Biochemistry & Biophysics, University of Pennsylvania,
Philadelphia, PA; and 3Marywood University, Scranton, PA

ABSTRACT
HOFFMAN, J. R., J. IM, K. W. RUNDELL, J. KANG, S. NIOKA, B. A. SPEIRING, R. KIME, and B. CHANCE. Effect of Muscle
Oxygenation during Resistance Exercise on Anabolic Hormone Response. Med. Sci. Sports Exerc., Vol. 35, No. 11, pp. 1929 1934,
2003. Purpose: The mechanisms that underlie the affect of acute program variables on muscle growth and strength development for
strength/power athletes have been of great interest. This investigation examined the affects of two different resistance exercise protocols
on muscle oxygenation, and the anabolic hormonal response to such exercise. Methods: Eleven experienced resistance-trained male
athletes performed four sets of the squat exercise using either a low-intensity, high-volume (LI; 15 repetitions at 60% one-repetition
maximum [1-RM]) or high-intensity, low-volume (HI; 4 repetitions at 90% 1-RM) load. Venous blood samples were obtained before
(Pre), immediate (IP), 20- (20P), and 40-min (40P) postexercise. Continuous-wave near-infrared spectroscopy was used to measure
oxygen desaturation during exercise. Results: No differences in muscle deoxygenation were seen between LI and HI. However,
time-dependent postexercise reoxygenation was significantly different between the two exercise sessions (35.3 17.4 s vs 24.5
14.3 s in LI and HI, respectively). Testosterone and growth hormone (GH) concentrations were significantly elevated from Pre at IP,
20P, and 40P in both LI and HI. GH concentrations were higher (P 0.05) for LI than at HI at 20P and 40P. Conclusion: Muscle
oxygen recovery kinetics appeared to be influenced by differences in the intensity and volume of exercise, and delayed reoxygenation
appears to affect the GH response to exercise. Key Words: TESTOSTERONE, GROWTH HORMONE, WEIGHT TRAINING,
NEAR-INFRARED SPECTROSCOPY, MUSCLE ISCHEMIA

D
uring aerobic exercise, blood flow and oxygen de- majority of resistance-training programs utilize dynamic
livery to working muscle is generally increased to movements with large variations in training intensity and
meet the demands of exercise (23). However, as volume.
exercise intensity increases, intramuscular forces become The manipulation of these training variables appears to
elevated, resulting in an attenuation of exercise hyperemia have important implications on the physiological response
(4,5,9,24,26). As a consequence, increases in lactic acid and to resistance exercise. Kraemer and colleagues (13,14) have
intramuscular oxygen desaturation are observed. The rela- shown that hormonal responses to acute heavy resistance
tionship between restricted blood flow, lactic acid, and exercise are sensitive to changes in these variables (e.g., rest
oxygen desaturation within the exercising muscle has been intervals, exercise intensity, and volume) in both men and
demonstrated (9,24). Although it is generally recognized women. Specifically, significantly higher testosterone con-
that exercise resulting in high force production (i.e., resis- centrations have been observed when rest periods between
tance exercise) will result in a reduction of blood flow to sets are reduced (3 to 1 min), or when the intensity of
exercising muscle (22), studies examining this mode of exercise is decreased (5 repetition maximum [RM] to 10-
exercise are limited. Moreover, most studies investigating RM) and volume is increased (14). Similarly, circulating
blood flow in the context of resistance exercise have used a immunoreactive growth hormone concentrations increase in
static model (i.e., isometric exercise), despite the fact that a response to an acute bout of resistance exercise, and appear
to be greatest when training protocols of moderate intensity
(10-RM vs 5-RM) and short rest periods (1 min vs 3 min)
Address for correspondence: Jay R. Hoffman, Ph.D., FACSM, Department are utilized (13). The elevations in anabolic hormonal re-
of Health and Exercise Science, The College of New Jersey, P.O. Box sponse to manipulations of the acute program variables may
7718, Ewing, NJ 08628; E-mail: [email protected]. explain, in part, the variability in muscle hypertrophy observed
Submitted for publication February 2003. with different resistance training programs. For example, body-
Accepted for publication June 2003.
builders typically incorporate high-volume, moderate-intensity
0195-9131/03/3511-1929 training programs with short rest periods.
MEDICINE & SCIENCE IN SPORTS & EXERCISE Recent research has suggested that muscle ischemia
Copyright 2003 by the American College of Sports Medicine caused by vascular occlusion appears to enhance the hor-
DOI: 10.1249/01.MSS.0000093613.30362.DF monal response to exercise (30). The extent and duration of
1929
ischemia may ultimately determine the extent of tissue damage (oxy/deoxy-Hb/Mb) in the capillary bed of the vastus late-
(8) that occurs consequent to a specific stimulus, such as heavy ralis muscle at rest, during each set, and for 3 min postex-
resistance exercise. In addition, muscle damage that occurs as ercise. After each training session, cuff ischemia (CI) was
a result of heavy resistance exercise is thought to be requisite performed to obtain maximal oxy/deoxy-Hb/Mb. Linearity
for muscle hypertrophy and increases in strength (16). Thus, it of NIRS technology has been previously validated in other
would appear that resistance-training programs designed to studies (7,19), and validity for cwNIRS has been recently
invoke a greater extent and duration of muscle ischemia would established (15). The NIRS unit included a probe consisting
result in increased muscle hypertrophy. Therefore, the purpose of two LED light sources and eight photodiode detectors.
of this study is to compare the effects of a high-intensity, An 11- 7-cm optical probe with a 3-cm source-to-detector
low-volume with a low-intensity, high-volume exercise para- separation was positioned on the lateral aspect of the right
digm on muscle oxygenation during resistance exercise. In vastus lateralis at a location equidistant between the greater
addition, the relationship between muscle oxygenation and the trochanter of the femur and the muscles distal connection to
anabolic hormonal response to resistance exercise was exam- the quadriceps tendon. The location of the probe was re-
ined. The hypothesis of this study is that exercise programs that corded by noting distances from the anatomical landmarks
elicit a greater degree of muscle ischemia will result in a greater to ensure identical probe placement during all trials. Wave-
anabolic hormonal response to exercise. lengths of 730 and 850 nm were used to monitor relative
change in oxy/deoxy-Hb/Mb. Oxy-Hb/Mb of muscle tissue
was estimated by changes in the difference in signal strength
METHODS
at those wavelengths. Data acquisition sampling frequency
Subjects. Eleven experienced resistance-trained men was set at approximately 2 Hz. Relative oxy/deoxy-Hb/Mb
(20.8 1.3 yr; 96.2 14.4 kg, 182.4 7.3 cm) served as (% oxy/deoxy-Hb/Mb) for each exercise period was calcu-
subjects for this investigation. After an explanation of all lated by taking the difference between baseline at rest and
procedures, risks, and benefits each subject gave his written the greatest oxy/deoxy-Hb/Mb that occurred during exer-
informed consent to participate in this study. The Institu- cise, and dividing by the maximal oxy/deoxy-Hb/Mb ob-
tional Review Board of the College approved the research tained during CI. To obtain CI, a thigh cuff was placed
protocol. Each subject had 6.9 0.8 yr of resistance train- proximal to the probe and inflated to 260 torr for 8 min or
ing experience (range 6 8 yr), had a 1-RM squat of 184.5 until a plateau for deoxy-Hb/Mb was reached. CI was ad-
16.5 kg, and was free of any musculoskeletal and endo- ministered while subjects were seated in a semirecumbent
crine disorders. In addition, all subjects reported being free position with the instrumented leg extended horizontally
of anabolic steroid use during the previous year and were and supported. Deoxy-Hb/Mb values from the baseline,
not taking any other ergogenic supplementation during the 6 exercise, and CI were obtained by taking 10-s averages.
wk before the study. Recovery kinetics and rates after each exercise session
Testing procedure. Each subject reported to the Hu- were also determined using the cwNIRS. Half-time recovery
man Performance Laboratory on three different occasions. (T1/2) was ascertained by determining the time necessary to
During the initial visit, subjects performed a 1-RM strength achieve to 50% of maximal reoxy-Hb/Mb after exercise
test for the squat exercise. Each subject performed a cessation (4).
warm-up set using a resistance that was approximately 40 Blood measurements. During each experimental ses-
60% of his perceived maximum, then performed three to sion blood samples were obtained preexercise (PRE), im-
four subsequent attempts to determine the 1-RM with 35 mediately postexercise (IP), 20 (20P), and 40 min (40P)
min of rest between each lift. During the next two sessions, postexercise. All blood samples were obtained using a 20-
each subject performed a resistance exercise protocol con- gauge Teflon cannula placed in a superficial forearm vein.
sisting of five sets of the parallel squat exercise. The first set The cannula was maintained patent using an isotonic saline
was used as a warm-up set. For each testing session both solution placed in a three-way stopcock with a male luer
intensity and volume of exercise differed. Subjects exer- lock adapter. PRE blood samples were drawn after a 15-min
cised using either a light-intensity, high-volume (LI) (15 equilibration period before exercise. IP blood samples were
repetitions with 60% of 1-RM), or high-intensity, low-vol- taken within 30 s of exercise cessation. All blood samples
ume (HI) (4 repetitions with 90% of 1-RM) exercise proto- were drawn with a plastic syringe while the subject was in
col during each testing session. The exercise protocol was a seated position.
randomly assigned to prevent an order effect. Rest intervals After collection, blood was transferred to a Vacutainer
between sets were 3 min for both exercise sessions. Each tube containing SST Gel and Clot Activator. The blood
testing session was separated by at least 72 h and occurred was allowed to clot at room temperature and subsequently
at the same time of day to account for diurnal variation in centrifuged at 1500 g for 15 min. The resulting serum was
hormonal measurements. placed into separate 1.8-mL microcentrifuge tubes and fro-
Hemoglobin/myoglobin muscle tissue deoxy- zen at 80C for later analysis of total testosterone and
genation procedure. A 16-channel continuous wave 22-kDa growth hormone.
near infrared spectroscopy (cwNIRS; NIMS, Philadelphia, Biochemical and hormonal analyses. Serum total
PA) was used to measure changes in hemoglobin (Hb)/ testosterone and 22-kDa growth hormone concentrations were
myoglobin (Mb) muscle tissue oxygenation/deoxygenation determined using enzyme immunoassay and enzyme-linked
1930 Official Journal of the American College of Sports Medicine http://www.acsm-msse.org
immunosorbent assay, respectively (Diagnostic Systems Lab-
oratories, Webster, TX). Determinations of serum immunore-
activity values were made using a SpectraMax340 Spectropho-
tometer (Molecular Devices, Sunnyvale, CA). To eliminate
interassay variance, all samples for a particular assay were
analyzed in the same assay run. All samples were run in
duplicate with a mean intra-assay variance of 10%. The
detection limit of the testosterone and growth hormone assays
were 0.14 nmolL1 and 0.3 gL1, respectively. Lactate
concentrations were determined with an Analox GM7 enzy-
matic metabolite analyzer (Analox Instruments U.S., Lunen-
burg, MA).
Statistical analysis. Data were analyzed using a two-
way ANOVA. In the event of a significant F-ratio, post hoc
comparisons using the Bonferroni method were applied to
determine pairwise differences. In addition, paired Students
t-tests were used to analyze the area under curve (AUC),
which was calculated by using a standard trapezoidal tech-
nique. A criterion alpha level of P 0.05 was used to
determine statistical significance. A sample size of 11 sub-
jects provided 80% statistical power at an level of 0.05
(two-tailed).

RESULTS
FIGURE 1A. Comparison of serum testosterone concentrations
During LI all subjects completed the 15 required repeti- (mean SD) for various time points and resistance exercise intensities.
tions per set except one subject who completed only 12 B. Area under the curve (AUC) testosterone responses (mean SD).
repetitions during his last set of exercise. During HI, 9 of the * Significantly different from Pre; LI, 60% 1RM; HI, 90% 1RM.
11 subjects were able to complete the four repetitions re-
quired per set. One subject was only able to complete three also failed to demonstrate any significant difference be-
repetitions in his last set, and another subject was only able tween exercise sessions.
to complete 5 of the 16 total repetitions that were required. The serum growth hormone response to the two training
The duration of exercise per set was significantly (P 0.05) sessions is shown in Figure 2. Growth hormone concentra-
greater during LI (41.6 6.6 s) than in HI (21.4 3.6 s). tions were significantly (P 0.05) elevated from PRE at IP,
However, the extent of muscle deoxygenation (expressed as a 20P, and 40P in both HI and LI. However, growth hormone
percent of maximal desaturation obtained during CI) between concentrations were significantly (P 0.05) higher for LI
the two exercise sessions was not statistically significant. Dur- than HI at 20P and 40P. In addition, AUC for GH was
ing LI muscle deoxygenation reached 72.7 18.0%, whereas significantly (P 0.05) higher during LI than in HI.
HI muscle deoxygenation reached 79.9 13.4%.
After exercise, muscle reoxygenation appeared to be de-
DISCUSSION
layed during both training sessions. However, the duration
of the delay was significantly (P 0.05) different between The purpose of this study was to examine the effect of
HI and LI (24.5 14.3 s and 35.3 17.4 s, respectively). training intensity on muscle oxygenation, and to examine
Once reoxygenation began the T1/2 recovery was not dif- the relationship between muscle deoxygenation and the an-
ferent between the two training sessions (50.2 15.5 s and abolic hormonal response. The results of this study show no
51.7 16.8 s in HI and LI, respectively). apparent difference between resistance exercise protocols of
Lactate concentrations at IP were significantly (P 0.05) low-intensity, high-volume and high-intensity, low-volume
elevated above resting levels after both HI and LI testing on muscle deoxygenation. However, the duration of exer-
conditions. However, lactate concentrations for LI was cise appears to have had a greater influence on the deoxy-
significantly (P 0.05) higher at that time point than for genation and the delay in postexercise muscle reoxygen-
HI (15.3 2.3 mmolL1 and 9.7 3.3 mmolL1, ation. Although both training intensities result in similar
respectively). deoxygenation values, exercise performed at the lower in-
The serum testosterone response to the two training ses- tensity was performed for a significantly longer duration.
sions is shown in Figure 1. Testosterone concentrations Although previous research has shown that resistance train-
were significantly (P 0.05) elevated from PRE at IP, 20P, ing will reduce tissue oxygenation within contracting skel-
and 40P in both HI and LI. However, no significant differ- etal muscle (28), this was the first study to quantify the
ences were seen between exercise sessions. AUC analysis extent of muscle deoxygenation during such exercise.
MUSCLE OXYGENATION AND RESISTANCE TRAINING Medicine & Science in Sports & Exercise 1931
 lactate acid concentrations in both LI and HI. Apparently the
high intramuscular pressures, as well as the relatively short
duration of exercise resulting from heavy resistance exer-
cise, has a much greater impact on muscle deoxygenation
than lactate concentrations. It is possible that the higher
lactate concentrations seen during LI had a greater impact
on muscle reoxygenation postexercise.
A unique aspect to this study was the difference seen in
reoxygenation between LI and HI. Despite similar deoxy-
genation levels during each training session, there was a
44.1% longer delay in the start of reoxygenation after LI
compared with HI. The phenomenon of delayed reoxygen-
ation, as a function of intensity and volume during resis-
tance exercise, has not been previously seen. It is likely that
the higher lactate accumulation seen during LI facilitated a
greater O2Hb dissociation (Bohr effect). In addition, previ-
ous research has also demonstrated that O2Mb dissociation
will follow a similar pattern of O2Hb dissociation when
exercise intensity is maximal (4,19). Considering that sub-
jects were exercising at intensities that approximated their
RM for each exercise intensity, it appears that the duration
of exercise performed at a maximal effort may be more
important than the relative intensity of exercise in affecting
muscle oxygen recovery kinetics. In addition, the greater
FIGURE 2A. Comparison of serum growth hormone concentrations metabolic acidosis seen during LI may have resulted in a
(mean SD) for various time points and resistance exercise intensities.
B. Area under the curve (AUC) growth hormone responses (mean 2-adrenoreceptor-mediated constriction of arteriole mi-
SD). * Significantly different from Pre; # Significantly different be- crovessels. McGillivray-Anderson and Faber (20) have
tween LI and HI. LI, 60% 1RM; HI, 90% 1RM. demonstrated that 2-adrenoreceptors on terminal arterioles
are highly sensitive to tissue acidosis.
Interestingly, the extent of muscle deoxygenation during The athletic background of these subjects may have also
resistance exercise appears similar to values previously re- contributed to the postexercise delay in muscle reoxygen-
ported in speed skaters skating in a low position (5), alpine ation. All of the subjects in this study were anaerobic ath-
skiers during a simulated giant slalom event (26), and sprint- letes. Though speculative, it is likely that the fiber compo-
ers performing the Wingate anaerobic power test (21). De- sition of these athletes was primarily of the Type II variety.
oxygenation of skeletal tissue during exercise is a function Previous research has shown that such fibers do not dem-
of a change in blood flow and intramuscular pressure (25). onstrate the level of postexercise hyperemia seen in slow-
Intramuscular pressure is known to increase linearly with oxidative and fast-oxidative fibers common in more aerobic
increases in the force of muscle contraction, which occur as athletes (17). Therefore, it is possible that the delay in
a result of increased tension in activated muscle fibers reoxygenation after high-intensity resistance exercise may
(2,11). As intramuscular pressure increases, blood perfusion also be a function of fiber type composition and associated
to the activated skeletal muscle is reduced. This appears to vasculature density.
begin when muscle contraction exceeds 3550% of its max- Another purpose of this study was to investigate whether
imal force capability (10). In this study, resistance exercise differences in muscle oxygenation as a result of exercise
was performed at 60% and 90% of the subjects 1-RM and intensity will influence the hormonal response to such ex-
would be expected to cause elevated intramuscular pres- ercise. Previous studies have indicated that under ischemic
sures. Thus, the extent of muscle deoxygenation observed conditions the hormonal response to exercise may be en-
during each testing session was not surprising. Even though hanced (27,30). However, in these studies the ischemic
there appeared to be a tendency for greater tissue deoxy- conditions were examined via vascular occlusion. This is the
genation after HI than LI, this 7% difference in muscle first study known that has examined the affect of muscle
deoxygenation was not statistically different. deoxygenation occurring as a natural response to the exer-
Previous research has reported a moderate correlation (r cise stress on the hormonal response to resistance exercise.
0.70, P 0.05) between lactic acid concentrations and The results attained in this study confirm previous investi-
the rate of muscle deoxygenation during submaximal aero- gations that have demonstrated that growth hormone
bic exercise (18). However, despite a higher lactate concen- (27,30), but not testosterone (30), concentrations are influ-
tration seen after LI (P 0.05), there was no significant enced by tissue ischemia in actively contracting muscle.
difference between the two exercise intensities in muscle The prolonged ischemic response seen after LI, reflected
deoxygenation. In addition, no correlations (r 0.10) were by the greater delay in muscle reoxygenation, resulted in a
observed in this study between muscle deoxygenation and greater growth hormone response than that seen after HI. In
1932 Official Journal of the American College of Sports Medicine http://www.acsm-msse.org
addition, lactate concentrations were 58% higher after LI response to an acute bout of heavy resistance exercise (12).
than after HI, presumably a result of the local tissue hypoxia Although this doesnt explain the similar response of tes-
caused by elevated intramuscular pressure. Growth hormone tosterone to the two exercise protocols, it does suggest that
secretion patterns have been shown to be quite responsive to the testosterone response to acute resistance exercise is
changes in the acid-base balance of muscle (6). Increases in attenuated in highly trained men.
intramuscular acidity can stimulate sympathetic nerve ac- Testosterone concentrations after both LI and HI were
tivity through a chemoreceptive reflex that is mediated by significantly elevated from PRE. Nevertheless, it did not
intramuscular metaboreceptors (29). Thus, it appears that appear that the mechanisms responsible for elevated testos-
the duration of acute hypoxia and the accumulation of terone levels were related to muscle deoxygenation. These
metabolites during resistance training are important stimuli results support recent research by Viru and colleagues (30),
for the growth hormone response. who also reported that changes in testosterone concentra-
The importance of acute program variables such as training tions were not influenced by muscle ischemia. Though
intensity and volume on the hormonal response to exercise has previous studies have suggested that exercise-induced in-
been demonstrated (13,14). Although the response of growth creases in testosterone concentrations are related to direct
hormone in this study supports these previous investigations, Leydig cell stimulation by elevated catecholamine concen-
the response of testosterone to differences in these training trations (1) and/or through changes in hormonal clearance
variables did not. Similar to growth hormone, testosterone is rate (3), it appears that the mechanisms responsible for such
responsive to changes in acute program variables (13,14). changes are still not clear.
Generally, resistance exercise of moderate intensity (i.e., 10- In summary, although heavy resistance exercise results in
RM) appears to induce a significantly greater testosterone significant muscle deoxygenation, training intensity and
response than exercise of higher intensity (i.e., 5-RM) (13,14). volume does not seem to impact the extent of deoxygen-
However, when the hormonal response was examined using ation. The results of this study do suggest that oxygen
AUC analysis, no significant differences were seen (14). Our recovery kinetics within skeletal muscle are influenced by
results confirm these findings.
these training variables. Furthermore, stimulation of growth
Another factor that may have contributed to the similar
hormone release during resistance training does appear to be
response of testosterone in this study was the effect of the
affected by the duration of muscle ischemia and accumula-
subjects training and athletic experience. Previous studies
tion of metabolites. These same stimuli do not appear to
that have examined the effect of acute program variables on
influence changes in testosterone concentrations during
the hormonal response to resistance exercise have primarily
such exercise.
used recreationally trained subjects (13,14). The subjects of
this study were all competitive intercollegiate athletes par-
We would like to thank a dedicated group of subjects.
ticipating in a strength/power sport. Training experience has This study was supported by National Institute of Health Grant
previously been shown to result in an attenuated hormonal HL-44125-12.

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