Download Effect of testosterone administration and weight training on muscle

Effect of testosterone administration and
weight training on muscle architecture
ANTHONY J. BLAZEVICH and ANTHONY GIORGI
Department of Sport Sciences, Brunel University, Osterley Campus, Isleworth, Middlesex TW7 5DU, UNITED
KINGDOM; School of Exercise Science and Sport Management, Southern Cross University, Lismore, New South Wales,
AUSTRALIA 2480
ABSTRACT
BLAZEVICH, A. J., and A. GIORGI. Effect of testosterone administration and weight training on muscle architecture. Med. Sci. Sports
Exerc., Vol. 33, No. 10, 2001, pp. 1688 –1693. Purpose: The purpose of this study was to assess muscle architecture changes in subjects
who were administered supraphysiologic doses of testosterone enanthate (TE) and concurrently performed heavy resistance training.
Methods: Ten subjects were randomly selected from the 21 subjects who participated in a previously published study (12). Subjects
were allocated to one of two groups as per Giorgi et al. (12) and received either a saline-based placebo (nonTE) or a 3.5-mg·kg⫺1 body
weight dose of TE by deep intramuscular injection once a week for 12 wk. Subjects also performed heavy resistance training using
exercises that targeted the triceps brachii muscle. Before and after the training period, free-weight one-repetition-maximum (1-RM)
bench press strength was tested, muscle thickness and pennation of the triceps brachii lateralis were measured using ultrasound imaging,
and fascicle length was estimated from ultrasound photographs. Results: There were no significant between-group differences in
muscle thickness changes despite a trend toward increased thickness in TE subjects (TE, 23.5%, vs nonTE, 13.8%). However, 1-RM
bench press performance and muscle pennation increased significantly in TE subjects compared with nonTE subjects (P ⬍ 0.05). There
was also a trend toward longer fascicle lengths in the muscles of nonTE subjects. Conclusion: The results of the present study suggest
that the use of TE in conjunction with heavy resistance training is associated with muscle architecture changes that are commonly
associated with high-force production. Since there was little difference between the groups in muscle thickness, changes in pennation
and possibly fascicle length may have contributed to strength gains seen in TE subjects. Key Words: STEROID, PENNATION,
ULTRASOUND, TRICEPS BRACHII, FASCICLE LENGTH
T
physical performance by increasing muscle size and
strength.
Although research has examined changes in muscle size
with steroid use, no research has investigated muscle architecture changes. A muscle’s architecture has been reported
to influence its contraction properties (4,28). Generally,
muscles that are recruited during high-force, low-velocity
contractions have large pennation and/or short fibers
(4,19,20,29), whereas muscles recruited during low-force,
high-velocity movements typically have smaller pennation
and longer fibers (4,24). Indeed, Kawakami et al. (20)
reported increases in muscle pennation accompanying muscle size increases after resistance training in five subjects.
Therefore, one would expect weight trainers who often
perform high-force, low-velocity contractions to possess
muscles of larger pennation and shorter fiber lengths. Given
that those subjects who are administered supraphysiologic
doses of steroids typically gain muscle mass and strength
faster, one might also expect their architectural changes to
be more pronounced.
In 1999, Giorgi et al. (12) published data showing significantly greater gains in muscle size and strength in subjects who were administered a 3.5-mg·kg⫺1 body weight
dose of testosterone enanthate (TE) than a control group
during a 12-wk resistance training period. It is possible that
architectural changes could have contributed to the greater
strength changes in TE subjects. If this was the case, a clear
difference in architectural adaptations would be seen
he main effect of exogenous testosterone and its
derivatives on the musculoskeletal system is to increase muscle mass and strength. Numerous studies
have reported increases in body weight (3,9,10,23) and lean
body mass (7,8,23) with the use of anabolic steroids. Some
research has also shown that steroid use, when combined
with resistance training, is associated with increases in muscle fiber area (22) and muscle cross-sectional area (3). These
increases in muscle mass are primarily linked to the reduced
effects of catabolic glucocorticosteroids that are released
during stress (15) and an increased rate of protein synthesis
(14).
Increases in isometric strength (1,2,17), isokinetic
strength (10), and muscle power (2,32) have been documented after steroid administration. Low steroid doses
(⬍150 mg total testosterone), suboptimum training loads,
and disparity between training and testing modes has often
compromised studies that found no performance effects of
steroid use when accompanied by resistance training
(5,6,13,18,25) (for review, see Haupt and Rovere (15)). As
such, steroids are commonly believed to improve human
0195-9131/01/3310-1688/$3.00/0
MEDICINE & SCIENCE IN SPORTS & EXERCISE®
Copyright © 2001 by the American College of Sports Medicine
Submitted for publication May 2000.
Accepted for publication January 2001.
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between subjects who were and were not administered TE.
During the study, ultrasound photographs of the triceps
brachii muscle were taken for 10 subjects (see Methods)
from which muscle pennation and fascicle length (used as an
indicator of fiber length) could be measured. The purpose of
the present study, therefore, was to compare muscle architecture changes between subjects who were administered
supraphysiologic doses of TE and concurrently performed
heavy resistance training with those who performed resistance training but were not administered TE. Some of the
data for subjects in the present study have been previously
published (12).
METHODS
Subjects. Of the 21 subjects who volunteered for the
original study (see Giorgi et al. (12)), architectural changes
were investigated in 10 of the male subjects (mean ⫾ SD:
age, 22.4 ⫾ 3.8 yr; height, 178.7 ⫾ 6.5 cm; weight, 84.1 ⫾
8.1 kg). One subject (TE group) chosen for analysis did not
complete the 12 wk; his data were not included in the
analysis. The low subject number reflected time and funding
constraints. Written informed consent was obtained from
subjects before their participation. All subjects were currently weight training at least three times a week before
taking part in the study and had at least 1 yr of weight
training experience. Thus, none of the subjects could be
regarded as novice weight trainers. Each subject produced a
urine sample to be assayed for the presence of anabolic
steroids and other substances banned by the International
Olympic Committee (IOC). None of the subjects were taking performance-enhancing substances before the study.
The study was approved by the Human Experimentation
Ethics Committee of Southern Cross University, Australia.
Approval for a clinical trial of TE was granted by the
Therapeutic Goods Administration (Australia), and the New
South Wales Department of Health, Australia, granted approval for TE purchase.
Drug screening procedure. A screening (urinalysis)
for drugs prohibited by the IOC was performed before
participation in the study. No subjects were taking IOCbanned substances. Urine was also obtained after 6 and 12
wk to monitor testosterone levels. All subjects refrained
from the ingestion of alcohol or caffeine for 24 h before
sampling (21). Subjects also emptied their bladder 1 h
before producing a urine sample to ensure a clean and
useable sample. Urine collection took place at the same time
of day (4 – 6 p.m.) to control for effects of circadian variations (11,21). The screening was performed at the IOCaccredited Australian Sports Drug testing Laboratories
(Pymble, Sydney, Australia).
Protocol. Photographs of the subjects’ triceps brachii
lateralis muscles were taken using ultrasound imaging.
From an on-screen image and the photographs, muscle
thickness, pennation, and fascicle length were determined.
These measures have been previously performed on the
triceps muscle (19). Subsequently, subjects performed a
free-weight one-repetition-maximum (1-RM) bench press
TESTOSTERONE AND MUSCLE ARCHITECTURE
test (see Giorgi et al. (12)) to assess the strength of their
chest and arm musculature. 1-RM was typically reached by
the fourth maximal attempt. During the training period, five
subjects were randomly assigned to receive injections of TE
(TE group), whereas the remaining four subjects were injected with a placebo (nonTE group). Muscle thickness,
pennation, fascicle length, and 1-RM bench press measures
were then repeated to allow assessment of strength and
muscle architecture changes.
Muscle thickness and pennation measurement.
Muscle thickness and pennation of the triceps brachii lateralis was determined at a point midway between the tip of
the acromion process of the scapula and the olecranon
process of the ulna. This distance was measured using a set
of Holtain anthropometric calipers (Harpenden type, Holtain Ltd., Crymmych, Pembrookshire, United Kingdom).
Care was taken that precise lengths were measured and the
reliability of these measurements was determined before the
investigation taking place (see Giorgi et al. (12)). Results of
repeated measurements on the triceps muscle have been
previously published (20), and the reliability of the sonographer has also been previously reported (27). Subjects
stood with the elbow flexed to 90° and the forearm resting
on a bench. The upper arm was positioned vertically by the
subject’s side. After applying hypoallergenic, water-soluble
transmission gel to the skin, an Acuson 8 L5 (8 MHz linear;
Mountain View, CA) ultrasound transducer was placed on
the surface of the posterior arm. The muscle thickness was
determined by the Acuson Sequoia 512 system after the
muscle was manually traced on the image screen. Three
trials were recorded for the muscle thickness measurements,
with the mean score being used for subsequent analysis. The
subjects had remained relaxed and did no strenuous activity
before testing.
Photographs of the muscle were taken immediately after
measurement of muscle thickness by rotating the scanning
head to obtain a longitudinal image (19,20). Lines were
drawn along the aponeurosis and echoes from interspaces
among the fascicles on the photograph (Fig. 1) and the
angles made by these lines measured by goniometer to the
nearest 0.5°. Pennation of the muscle was taken as the
median three repeated angle measurements.
Estimation of fascicle length. Fascicle length (FL)
was estimated as the length of the hypotenuse of a triangle
with an angle equal to the pennation angle (␪) and the side
opposite to this angle equal to the muscle thickness (T),
where FL ⫽ (T/sin␪). Thus, fascicles were assumed straight
and the model did not account for fascicle curvature. Fascicle length has been commonly estimated by this method
(16,20,24). An error of approximately 3% can be expected
for relaxed muscles with short fascicles when fiber curvature is not accounted for (unpublished observations).
Training program. The training program used by the
subjects has been described previously (12). Briefly, subjects performed a weight training regimen for 12 wk. Training involved four weight training sessions per week with
two sessions consisting of exercises that targeted the triceps;
the other two sessions consisted of exercises targeting other
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FIGURE 2—Urine testosterone levels of subjects in TE and nonTE
groups. There was a significant (P < 0.01) increase in the testosterone
levels of TE subjects after TE administration.
FIGURE 1—Ultrasound photograph of triceps brachii muscle. Muscle
pennation is measured in three fibers as the angle between the aponeurosis (horizontal white line) and the fascicles (diagonal white line) as
shown on this photograph. Measures were not taken from reproduced
images such as these but directly off photographs.
body parts. All subjects were encouraged to stretch after
training, although this was not controlled in the study.
Training was periodized to prevent staleness and its intensity consistently increased to provide a stimulus for muscle
growth. Training logs were kept for each subject to ensure
adherence to the program.
Testosterone administration procedure. The testosterone administration and subject group allocation procedures have been described previously (12). Briefly, subjects received either saline-based placebo (nonTE) or a
3.5-mg·kg⫺1 body weight dose of TE (Primoteston Depot,
250 mg). The dose is equivalent to that used in studies
assessing the efficacy of TE as a male contraceptive (33) but
exceeds those purported to be used by power athletes such
as sprint runners (34). The administration of TE and the
placebo was performed weekly by deep intramuscular injections into the outer, upper quadrant of the gluteus maximus muscle using a 21-gauge (13⁄4 inch) needle. The outer,
upper quadrant was targeted to minimize the risk of impinging on nerves or blood vessels. A qualified nurse performed
all injections at the same time each week for each subject for
the 12 wk of training. Testosterone (urinary) levels were
significantly increased after TE administration in TE subjects (Fig. 2) (P ⬍ 0.01).
Data analysis. The validity of ultrasound measurement
as a means of measuring architecture of the triceps muscle
has been shown elsewhere (19), and the reliability of the
sonographer has been presented previously (27). Reliability
of muscle pennation measures was shown here by calculating the average difference between the first two of three
measurements on all subjects. The average difference was
subsequently expressed as a percent of the average of all
angles measured. Reliability of triceps brachii thickness was
estimated by calculating both the technical error of measurement (TEM%) and intraclass correlation coefficients
(ICC).
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After satisfying the assumptions of homogeneity of variance and normality of distribution of the data, a repeated
measures analysis of variance (ANOVA) was used to assess
the effect of group (TE or nonTE) on muscle thickness,
pennation, fascicle length, and bench press performance
(SPSS v10.0, SPSS, Inc., Chicago, IL). A one-way ANOVA
with Bonferroni correction was used to assess betweengroup differences in pretraining scores. Significance was set
at an alpha level of 0.05. Eta squared values were calculated
during the analysis to examine the variance explained by the
factors. Observed power was calculated when the alternative
hypothesis was set on the basis of the observed values.
Power was above 0.7 for pennation and bench press
strength, but slightly lower for fascicle length and muscle
thickness (0.40 and 0.34, respectively). Effect sizes were
calculated for muscle thickness scores to assess the effect of
group differences without consideration for sample size.
The power of fascicle length estimates was low because of
high variability of this measure (unpublished observations).
RESULTS
Reliability of pennation and thickness measures.
The average absolute difference (i.e., all differences expressed as positive) between the first two pennation angle
measurements of all fiber bundles was 0.2°. The average
pennation angle was 9.8°; therefore, an average difference
of 0.2° represents a magnitude of only 2% of the average
pennation angle. Therefore, there was little difference between repeated measurements. Estimates of triceps thickness were also reliable (triceps brachii lateralis thickness:
TEM% ⫽ 0.4%, ICC ⫽ 0.95).
Changes in strength and muscle architecture.
Pre- and posttraining data for bench press strength and
muscle architecture measures are presented in Table 1.
There was a significant time ⫻ group interaction for bench
press performance such that after the 12 wk of training, the
increase in bench press performance by TE was greater than
nonTE (F[1,7] ⫽ 17.6, P ⬍ 0.05).
The result was similar for muscle pennation, which
increased more in TE than in nonTE subjects (time ⫻
group interaction, F[1,7] ⫽ 10.24, P ⬍ 0.02). Indeed 60%
of the variance in muscle pennation can be attributed to
the time by group interaction (⌭2 ⫽ 0.59), suggesting that
http://www.acsm-msse.org
TABLE 1. Mean (SD) pre- and posttraining values for bench press strength, muscle pennation, and thickness.a
Bench Press (kg)
Pennation (°)
Thickness (mm)
Group
Before
After
Before
After
Before
After
TE
NonTE
93.3 (16.6)
109.8 (20.0)
108.1 (16.1)b
113.7 (24.9)
8.1 (2.3)
12.0 (1.8)
11.3 (3.4)b
11.5 (1.9)
24.6 (6.3)
28.0 (7.2)
31.8 (4.8)c
31.8 (6.8)c
TE, subjects were administered testosterone enanthate; NonTE, subjects were not administered testosterone enanthate.
a
TE subjects increased significantly more in bench press performance and muscle pennation than nonTE subjects (P ⬍ 0.05). There was a general increase in muscle
thickness that was not different between the groups.
b
Change was significantly greater for TE subjects.
c
Significant change over time, but no difference between groups.
TE administration was associated with increased pennation. Low pennation of the muscle compared with previously published data (19) can be attributed to the long
length at which the muscle was tested; the elbow was
flexed to 90°, with the upper arm positioned vertically by
the subject’s side.
For muscle thickness, there was an effect of time (F[1.7]
⫽ 34.0, P ⬍ 0.01), but no interaction effect (F[1,7] ⫽ 3.2,
P ⫽ 0.18). Therefore, there was an increase in triceps
muscle thickness after 12 wk of training, but the increase
was not influenced by TE administration (no group effect).
This was despite the mean increase being slightly greater for
TE subjects (effect size ⫽ 0.54; 29.5% increase in the TE
group, 13.8% increase in the nonTE group).
There was a nonsignificant time ⫻ group interaction for
fascicle length change (F[1,7] ⫽ 3.9, P ⬍ 0.1), with TE
subjects decreasing (mean score, 17.9 cm to 16.6 cm) and
nonTE subjects increasing (mean score, 13.3 cm to 16.0 cm)
in fascicle length. Low reliability of the estimation method
and low subject numbers may have prevented significant
findings.
DISCUSSION
The purpose of this study was to assess muscle architecture changes in subjects who were administered supraphysiologic doses of a steroid and concurrently performed heavy
resistance training. Subjects who were administered TE did
not significantly increase their triceps muscle thickness
more than nonTE subjects. This was despite the mean increase in thickness being greater for TE subjects (29.5% vs
13.8%) and a significant increase in urinary testosterone of
TE subjects (Fig. 2) (P ⬍ 0.01). The lack of statistical
difference between the groups may be a result of low subject
numbers reducing statistical power (power ⫽ 0.34). However, the moderate effect size (ES ⫽ 0.54) suggests that
there indeed may not have been a distinct difference between the group’s change in triceps muscle size. Furthermore, no significant differences were reported in the data
from 21 subjects by Giorgi et al. (12). In that publication,
triceps thickness increased in TE subjects from 25.5 ⫾ 5.8
mm to 33.5 ⫾ 4.0 mm, and in nonTE subjects from 25.7 ⫾
6.7 mm to 31.3 ⫾ 6.3 mm. These changes are similar to
those reported in Table 1 of the present study. As such, the
muscle thickness data of the subjects in the present study are
TESTOSTERONE AND MUSCLE ARCHITECTURE
similar to those of the whole 21 subjects presented by Giorgi
et al. (12).
Given the relationship between pennation (␪), fascicle
length (FL), and muscle thickness (T) such that T ⫽ FLsin␪,
significant increases in muscle thickness can result not only
from muscle hypertrophy but from either or both increases
in pennation and fascicle length (e.g., small changes in
fascicle length and pennation could be reflected in significant changes in thickness). TE subjects showed greater
increases in pennation, whereas nonTE subjects showed
longer fascicle lengths after training. These changes would
likely result in similar increases in muscle thickness. The
result contradicts findings of Bhasin et al. (3), who showed
a significant difference in triceps muscle size between “steroid” and “control” groups as measured by magnetic resonance imaging (MRI) after 10 wk of training. However, the
larger amount of steroid given to subjects in that study (600
mg·kg⫺1) may have contributed significantly to their increased muscle thickness.
Despite no significant difference in triceps muscle size
between TE and nonTE groups in the present study, the TE
group showed greater improvement in their 1-RM bench
press (Table 1). The greater strength increases in TE subjects were also reported in the whole 21 subjects (12). In that
publication, 1-RM bench press strength of TE subjects improved from 98 ⫾ 19 kg to 119 ⫾ 19 kg and in nonTE
subjects from 100 ⫾ 16 kg to 109 ⫾ 18 kg. Again, the
changes in bench press strength were similar to those in the
present study, although perhaps the bench press strength of
nonTE subjects used for this analysis was slightly higher
than the average of the whole 21 subjects. Nonetheless,
strength changes mirrored those of the 21 subjects as a
whole (12). It is possible then that since muscle thickness
and strength changes were similar to those presented by
Giorgi et al. (12), the architectural changes shown here
might also be indicative of those that would have occurred
in the larger groups of 21 subjects, although this cannot be
confirmed.
Subjects who were administered TE showed greater
increases in pennation compared with the nonTE controls. In fact, there was no change in triceps pennation for
nonTE subjects after 12 wk of resistance training. Larger
pennation has been seen in muscles that commonly produce high-force contractions (4,30) and could theoretically aid strength development by allowing more
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FIGURE 3—Fiber shortening in pennate muscles. Fibers of pennate
muscles not only shorten but also rotate during muscle contraction (A
to B; ␪ indicates pennation).
contractile tissue to attach to a given area of tendon
(19,20,28). Tendon excursion is also greater for a given
length of fiber shortening when the angle between the
fascicles and tendon is greater (26). This is because fibers
in pennate muscles not only shorten but rotate during
muscle shortening (Fig. 3). Effectively, both the length
and velocity of fiber shortening would be less in muscles
of greater pennation. The fibers would therefore be able
to produce greater force according to their length-tension
and force-velocity properties. As such, the increases in
pennation seen in TE subjects may theoretically have had
a positive influence on their strength development.
Fascicle length has also been linked to muscle contraction properties such that muscles with longer fibers are
recruited during high-velocity contractions (4,24). Muscles that consistently produce high-velocity contractions
may adapt to longer fiber lengths because longer fibers
possess higher shortening velocities (29,31). In humans,
muscles that provide high-force contractions often contain shorter fibers (30). For subjects in the present study,
there was a trend toward longer fascicles in the triceps
brachii lateralis of nonTE subjects (13.3 cm to 16.0 cm),
whereas there was a small decrease or no change in TE
subjects after training. In our opinion, the long fascicle
length estimates can be attributed to the low pennation
and nonparallel relationship between the line of the aponeurosis and the muscle border at which the fascicles
terminate. Our ultrasound images showed that the fascicles terminate near the muscle’s origin after traversing
approximately 10 –12 cm. Although fascicle length determined in the present study can only be considered an
estimate (given the error in fascicle length prediction and
small sample size used for the analysis), the result provides further evidence of specific adaptations such that
the muscles of TE subjects became better adapted for
high-force contractions than nonTE subjects. Consequently, subjects who use testosterone derivatives in supraphysiologic doses while performing high-intensity resistance training may attain muscle architecture better
suited to high-force development compared with those
who do not.
The mechanism by which TE affected architectural
changes is unclear. Some authors have suggested that
larger muscles possess greater pennation (19,20) because
more muscle mass could then attach to the tendon
(19,20,28). Given that previous research has shown that
increases in body mass and muscle size are greater in
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Official Journal of the American College of Sports Medicine
subjects using steroids (3,22), increases in pennation
might be expected with the greater muscle hypertrophy.
Nonetheless, there was no significant between-group difference in muscle thickness changes in the present study.
Thus, although increases in pennation might accompany
increases in muscle size, other factors must have influenced pennation changes here.
One such factor might be the retention of fluid (water/
salt) within the muscle that could occur with TE use (see
Giorgi et al. (12)). Incorporation of water into the muscle
would cause an enlargement of the muscle fibers. If the
increases in fiber size were associated with increases in
pennation, as some authors have suggested (19,20,28),
then strength changes could have resulted. This would in
turn allow greater loads to be lifted and possibly provide
a greater stimulus for muscle growth. Thus, architectural
changes may have preceded strength gains.
Alternatively, the greater pennation in TE subjects may
have been an adaptation to greater loads lifted in training.
Training logs showed that TE subjects increased their training weights faster than nonTE subjects did. Indeed, TE
subjects had increased their bench press 1-RM by 13.9 kg
after 6 wk, whereas nonTE subjects had only increased 3.8
kg. Although hypertrophy in other muscles (e.g., the pectoral muscle group) may have influenced strength changes,
adaptations in the nervous system, enhanced recovery from
training, or some other rapid adaptation may have resulted
in the greater loads being lifted. Muscle architecture may
have then changed in response to the higher training loads.
Nonetheless, it is unclear from the present data in what order
changes in muscle thickness, pennation, and strength
occurred.
It appears from our results that increases in strength
and pennation, and possibly decreases in fascicle length,
are related to TE use (or the greater training loads used by
subjects administered TE). However, there was a statistically significant difference (P ⬍ 0.05) between the
groups in bench press strength and a marked (although
nonsignificant, P ⬍ 0.07) difference in pennation before
the study. Thus, the greater changes in strength and
muscle architecture of TE subjects may have been somewhat related to their pretesting training status. Although
data from Giorgi et al. (12) showed no difference in the
groups in strength, muscle size, body height, and weight
before the study, the nonTE subjects used for the present
analysis probably represented the stronger subjects in the
group. Nonetheless, strength values reported here are not
likely to represent the upper limits of human strength, so
changes in strength should still have been possible in
both groups. It is unclear what the upper limits of architectural changes are. Interestingly, however, the stronger
nonTE group also had larger pennation and greater triceps thickness (nonsignificant), which further suggests
there is a relationship between strength and muscle
architecture.
In summary, supraphysiologic doses of TE, when combined with high-intensity weight training for 12 wk, did
not result in greater increases in triceps muscle thickhttp://www.acsm-msse.org
ness than training alone. However, muscle pennation
increased significantly compared with control subjects.
Our estimates of fascicle length also suggested that TE
administration was associated with no change, or a slight
decrease, in fascicle length, whereas subjects who did not
use TE may have had a slight increase in their fascicle
lengths. Architectural differences between the groups
may help explain their strength differences after training
because muscles that have larger pennation and shorter
fibers are commonly associated with high-force production. Therefore, in addition to increases in muscle size
shown in other studies, some of the increase in strength
associated with steroid use may be a result of architecture
changes. The results of the present study, however, do not
indicate whether architecture changes result from, or are
the cause of, greater strength increases in TE subjects.
Research investigating the mechanisms of architectural
changes, especially with large subject numbers where
type II error is reduced, is clearly warranted.
Address for correspondence: Anthony J. Blazevich, Department
of Sport Sciences, Brunel University, Osterley Campus, Borough
Road, Isleworth, Middlesex TW7 5DU, United Kingdom; E-mail:
[email protected].
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