Content uploaded by Lars Bojsen Michalsik
Author content
All content in this area was uploaded by Lars Bojsen Michalsik on Apr 09, 2018
Content may be subject to copyright.
Acute fatigue-induced changes in muscle mechanical properties and
neuromuscular activity in elite handball players following a handball
match
J. B. Thorlund, L. B. Michalsik, K. Madsen, P. Aagaard
Institute of Sports Science and Clinical Biomechanics, University of Southern Denmark, Odense, Denmark
Corresponding author: Jonas Bloch Thorlund, MSc, Institute of Sports Science and Clinical Biomechanics, University of
Southern Denmark, Campusvej 55, DK-5230 Odense, Denmark. Tel: 145 6550 3684, Fax: 145 6550 3480, E-mail:
jthorlund@health.sdu.dk
Accepted for publication 19 April 2007
The purpose of the present study was to determine the acute
fatigue development in muscle mechanical properties
and neuromuscular activity in response to handball match
play. Male elite handball players (n510) were tested
before and after a simulated handball match for maximal
isometric strength [maximal voluntary contraction (MVC)]
and rate of force development (RFD) with synchronous
electromyography (EMG) recording, while maximal
vertical jump parameters were assessed using force plate
analysis. Quadriceps and hamstrings MVC and RFD
decreased significantly post-match ( 10%, Po0.05 and
16–21%, Po0.05, respectively). During quadriceps,
MVC mean EMG amplitude [mean average voltage
(MAV)] decreased for the vastus lateralis (VL) and
rectus femoris (RF) (21–42%, P0.05), while MAV also
decreased in the antagonist biceps femoris (BF) muscle
(48–55%, Po0.01). During hamstring MVC, MAV was
reduced in BF (31%, Po0.01). Maximum EMG amplitude
during quadriceps MVC was reduced for the VL (28%,
Po0.01) and the RF (5%, Po0.05). During hamstring
MVC, maximum EMG was reduced for BF (21%,
Po0.01). Post-match maximal jump height was reduced
(5.2%, Po0.01), as was also work (6.8%, Po0.01),
velocity of center of mass (2.4–4.0%, Po0.01) and
RFD ( 30%, Po0.05). In conclusion, maximal (MVC)
and rapid muscle force characteristics (RFD, impulse)
were acutely affected concurrently with marked re-
ductions in muscle EMG following handball match
play, which may potentially lead to impaired functional
performance.
Introduction
Previous studies on fatigue have traditionally been
conducted in laboratories using a simple setup like
fatiguing dynamic knee extensions, sustained con-
tractions or all-out sprint bouts on a cycle ergometer.
However, such studies may not adequately describe
the fatigue response in more complex sports like
team handball. A handball match involves a large
number of repeated accelerations, sprints, jumps,
blocking, pushing and rapid changes in moving
directions, i.e. side cutting (Michalsik, 2004; Goros-
tiaga et al., 2006; Ronglan et al., 2006). Danish male
elite handball players often play 50 min in a 60-
min match (Michalsik, 2004) and it seems reasonable
to assume that the ability to exert maximal force
[maximal voluntary contraction (MVC)] and rapid
force exertion (rate of force development – RFD)
would decrease during a handball match especially
for the leg muscles. A recent study on fatigue in elite
female handball players focused only on perfor-
mance parameters like maximal muscle strength,
sprint time and jump height (JH) in response to a
training camp or prolonged tournament (Ronglan
et al., 2006). In this perspective, it seems important to
determine the fatigue-related effects of match play on
different aspects of mechanical muscle function
(strength, power and RFD) and neuromuscular ac-
tivity, which would be expected to have an impact on
the functional performance toward the end of the
match. The ability to exert high maximal muscle
force and large contractile RFD are both of vital
importance in modern elite handball match play,
which is emphasized by the increased use of systema-
tic resistance training by elite handball players.
Maximal force is important in actions like tackles
and in fights competing for position between defense
players and circle players, whereas RFD most likely
is of even greater functional importance for fast
movements such as sprinting, throwing and side
cutting that involve contraction times o250 ms (Aa-
gaard et al., 2002). For the knee extensors, the time
to reach maximum force is 400–600 ms (Thorstens-
son et al., 1976; Aagaard et al., 2002), which means
Scand J Med Sci Sports 2008: 18: 462–472 Copyright &2007 The Authors
Journal compilation &2007 Blackwell Munksgaard
Printed in Singapore .All rights reserved
DOI: 10.1111/j.1600-0838.2007.00710.x
462
that maximal muscle force may not be reached
during very fast movements. It is therefore of interest
to quantify the specific fatigue-induced decreases in
muscle mechanical properties including RFD be-
cause thereby valuable information could be gained
for the optimization of training in elite handball.
Resistance training is known to enhance muscle
strength and RFD due to muscular and neural
adaptations (Ha
¨kkinen et al., 1985; Aagaard et al.,
2002) and to result in improved neuromuscular
fatigue resistance (Hickson et al., 1988; Raastad
et al., 2003). The aim of this study was to determine
the acute fatigue development in muscle mechanical
properties and neuromuscular activity in response to
playing a handball match. This study is, to the best of
our knowledge, the first to examine the effect of acute
fatigue development on muscle mechanical and
neural properties in elite handball players.
Materials and methods
Subjects
The study was designed as a controlled intervention study and
included 10 male elite handball players from the top of the
premier Danish national league. All players participated in
European Cup tournaments in the season they were tested.
The subjects gave their informed consent and the conditions of
the study were approved by the local ethics committee.
Protocol – overview
Subjects were tested before (Pre) and after (Post) a simulated
handball match to establish the development of neuromuscu-
lar and muscle mechanical fatigue. Before all tests, the subjects
visited the laboratory on a separate day for familiarization to
the test procedures. Subjects were instructed not to eat the last
11
2h before testing and not to engage in any vigorous training
the day before testing. During all tests, subjects were allowed
to drink water ad libitum.
Pre and Post tests
Body height, weight and body fat percentage were measured
(Table 1), the latter by a conventional bioimpedance leg-to-leg
method, with a custom-built apparatus (Tanita-Body Compo-
sition Analyzer, TBF-3000, TANITA Corp., Tokyo, Japan)
(Heitman, 1990).
The subjects performed a 10-min general warm-up at
90 r.p.m. with a 2 kg resistance (180 W) on a Monark
ergometer cycle before the jump tests. Shortly after the
warm-up (1–2 min), subjects performed three counter move-
ment jumps (CMJ) on a force plate (Caserotti et al., 2001;
Bojsen-Møller et al., 2005; Holsgaard Larsen et al., 2007) with
a 30–45 s pause between each jump. After the jump test,
electromyography (EMG) surface electrodes were placed at
four different muscles at the preferred jump leg and the subject
was placed in an isokinetic dynamometer (more details given
below). Before the actual test, a warm-up with several sub-
maximal and a few maximal dynamic contractions was carried
out in the isokinetic dynamometer and followed by maximal
isometric tests for the quadriceps as well as the hamstrings.
Surface electrodes were then removed and the subject walked
to a handball court in a facility near the laboratories. Before
the simulated handball match, the subject was given a 5-min
period to carry out a handball-specific warm-up and was then
given instructions about the specific match protocol. After
completion of the handball match, the same test procedure
was followed as before the match, although warm-up was only
performed before the isokinetic test. See Fig. 1 for time table
and a schematic overview of the protocol. Because the Post
measurements were performed after completion of the full
match, the data obtained describe the overall fatigue response
induced by the entire match.
Test methods
Jump test – CMJ
Maximum JH was assessed as described previously described
by Caserotti et al. (2001). In brief, the subjects performed a
bilateral CMJ on a force plate (Kistler 9281 B, Winterthur,
Switzerland). The CMJ was performed from a standing
position with both hands on the hip to minimize any influence
from the arms. The subject were instructed to make a fast
downward movement to about 901knee flexion (eccentric
phase) immediately followed by a fast upward movement
(concentric phase) and while intending to jump as high as
possible. The jump was visually demonstrated to the subject
and familiarization trials were conducted on a separate day
before actual testing. At Pre test subjects carried out a short
self-chosen warm-up (after the general warm-up), followed by
three maximal CMJ with a 30–45-s rest between each jump.
No warm-up was performed before the Post test as subjects
were warmed up by the handball match activity. The trial with
the highest JH was selected for further analysis (Caserotti
et al., 2001; Bojsen-Møller et al., 2005; Holsgaard Larsen
et al., 2007).
The vertical ground reaction force signal (F
z
) was fed from
the Kistler amplifier to a 12-bit A/D converter (dt28ez Data
Translation) at a 1000Hz sampling rate and stored on a PC. The
F
z
signal was later analyzed according to the methods described
by Caserotti et al. (2001) and Davies and Rennie (1968). In brief,
the vertical velocity (v) of the center of mass was obtained by
time integration of the instantaneous acceleration:
vðtÞ¼Zt
0
aðtÞdt¼Zt
0
½FðtÞ=mgdtð1Þ
where ais the vertical acceleration, Fis the vertical force
measured by the platform, mis the body mass of the subject
and gis the acceleration due to gravity (9.81 m/s
2
). Center of
mass position (pos) was obtained by time integration of the
velocity signal and jump power was calculated continuously
throughout the movement as the instantaneous product between
Fand v(Fig. 2(c)) (Caserotti et al., 2001).
All CMJ trials were analyzed for JH and displacement (dS)
of the body center of mass (BCM) during the eccentric (dS-
ecc) and concentric (dS-con) phases, respectively. In addition,
the total duration of the takeoff phase (TDT) and the eccentric
(ecc) and concentric (con) phases (ecc 5downward move-
Table 1. Anthropometric characteristics
Anthropometric characteristics Range
Age (years) 22.8 1.5 21–28
Height (cm) 188.4 2.7 178.0–200.0
Body mass (kg) 91.7 3.0 75.4–103.3
Body fat (%)
*
10.6 1.2 8.7–13.5
Values are means SE;
n
510.
*
n
59.
Neuromuscular fatigue in elite handball
463
ment negative velocity, con 5upward positive velocity)
were calculated (T
ecc
and T
con
) (Fig. 2). Ecc was further
divided into an acceleration (T
eccACC
) and deceleration (T
ecc-
DEC) phase. TeccACC
was defined as the interval between the start
of downward movement (velocity increases negatively) and
the instant of maximal negative velocity (Caserotti et al.,
2001). T
eccDEC
was defined as the time interval between
maximal negative velocity (i.e. instant at F
z
5body mass)
and the time when velocity reached zero (i.e. the end of
downward movement). Moreover, peak force was identified
for the eccentric (F
peak-ecc
) and the concentric phase (F
peak-con
).
Mean force (F
mean-con
) was also determined for the concentric
phase. Peak power (P
peak-con
) was measured for the concentric
phase along with the velocity at peak power (V
ppeak-con
) and F
z
force at peak power (F
ppeak-con
), as well as mean power (P
mean-
con
). Furthermore, the F
z
rate of force rise (RFD) was derived
for the time intervals T
dec
to T
dec
150 ms and T
dec
to
T
dec
1100 ms (T
dec
5time of transition from deceleration to
acceleration in ecc phase, i.e. the instant where F
z
5body mass
(Fig. 2)) and lastly the total concentric work (Work-con)
and peak velocity (V
peak-con
) for the concentric phase were
determined.
Maximal isometric muscle strength, RFD and impulse
RFD and maximal isometric muscle strength were measured
in an isokinetic dynamometer (KinCom; Kinetic Communi-
cator 500 H, Chattecx Corp., Hixson, TN, USA) for the
preferred jump leg. The method used is identical to that
reported by Aagaard et al. (2002). Isometric muscle strength
was measured at a knee joint angle of 701(01, full knee
extension). Subjects were seated 101reclined and firmly
strapped at the hip and thigh. The axis of rotation of the
dynamometer lever arm was visually aligned to the axis of the
lateral femur epicondyle of the subject, and the lower leg was
attached to the lever arm of the dynamometer just above the
medial malleolus. Individual setting of the seat, backrest,
dynamometer head and lever arm length was registered so
that identical positioning could be ensured on all test occa-
sions. The dynamometer force and position signals were
sampled into a PC at a 1000 Hz sampling rate and filtered
by a fourth-order zero-lag Butterworth low-pass filter at 15
and 5 Hz cutoff frequencies, respectively. To correct for the
effect of gravity on the measured joint moments, the passive
mass of the lower leg was measured in the dynamometer at a
knee joint angle of 451(Aagaard et al., 1995). The reliability
and validity of the KinCom dynamometer have been verified
in detail previously (Farrell & Richards, 1986).
In connection to the simulated handball match, subjects
performed an isometric strength test Pre and Post. Specific
warm-up contractions were performed in the KinCom, using
several submaximal and one to three maximal dynamic con-
tractions before subjects performed five maximal isometric
contractions with 30–45-s intervals. Subjects were carefully
instructed to contract as fast and hard as possible (Aagaard
et al., 2002; Suetta et al., 2004). The trial with the
highest maximal impulse at 0–200 ms (t50 denotes onset of
contraction) was selected for further RFD analysis while the
highest MVC was obtained from the trial with the highest
peak moment. Visual feedback of the dynamometer force
output was provided to the subjects on a computer screen
after each trial (Kellis & Baltzopoulos, 1996), which allowed
trials with ‘‘counter-movements’’ to be discarded and reper-
formed.
Contractile RFD was derived from the isometric measure-
ments as the average slope of the initial time phase of the
moment–time curve (Dmoment/Dtime) at 0–30, 50, 100 and
200 ms relative to the onset of contraction (Aagaard et al.,
2002; Suetta et al., 2004). Onset of contraction for the
quadriceps and hamstrings were defined as the instant where
force increased 7.0 and 4.0 N m above the rising baseline level,
respectively, corresponding to 2% of the peak moment.
Contractile impulse was determined as the area under the
moment–time curve (moment dt) in the same time intervals.
By incorporating the accumulated time-history of contraction,
contractile impulse provides vital information on the capacity
for rapid muscle force exertion, although this parameter has
been reported only rarely (Baker et al., 1994; Aagaard et al.,
2002; Suetta et al., 2004).
The relative RFD was determined as the RFD normalized
relative to MVC. The relative RFD (%MVC/s) was calculated
from the onset of contraction to the time points of 0–30, 50,
100 and 200 ms, respectively. Furthermore, the time at peak
RFD from the onset of contraction, as well as the time to
reach 1/6, 1/2 and 2/3 MVC were determined (Aagaard et al.,
2002).
Time (min)
0 10 20 30 40 50 60 70 80 90 100 110 120 130 140 150 160
Warm-up
Start test
Pre Jump test
Placing EMG
Pre KinCom test
Intro and warm-up
Simulated handball match
Post Jump test
Placing EMG
Post KinCom test
End test
Walk to laboratory
to simulated
handball match
Fig. 1. Overview of the protocol of the Pre and Post test in connection with the simulated handball match. Warm-up 10 min,
Pre jump test 12 min, placing electromyography (EMG) 11 min, Pre KinCom test 26 min, introduction and warm-up to
simulated handball match 17 min, simulated handball match 49 min, walk to laboratory 4 min, Post jump test 7min, placing
EMG 8 min, Post KinCom test 17. Values are means; n510.
Thorlund et al.
464
The ratio of hamstrings to quadriceps strength (H/Q-ratio)
was calculated based on isometric MVC (Aagaard et al., 1998)
while H/Q-ratios based on RFD and impulse were calculated
to evaluate the explosive strength capacity of the hamstrings
relative to the quadriceps (Zebis et al., 2003).
EMG measurements
EMG signals were recorded in the knee extensors, vastus
lateralis (VL), rectus femoris (RF) and the knee flexors, biceps
femoris caput longum (BF) and semitendinosus (ST) muscles
using bipolar surface electrodes (Ambu M-00-S, Medicotest,
Ølstykke, Denmark). After careful preparation of the skin
(shaving, abrasion and cleaning with alcohol), electrodes were
placed over the muscle belly of the four different muscles with
a 20-mm interelectrode distance. Markings were carefully
made with ink around the electrodes so that identical placing
was ensured Pre and Post the simulated handball match,
because even slight changes in electrode placement could
hamper interpretation of the EMG data. EMG electrodes
were directly connected to small custom-built preamplifiers
taped to the skin. The EMG signals were led through shielded
wires to custom-built differential instrumentation amplifiers
with a frequency response of 10–10 000 Hz and a common
mode rejection ratio 4100 dB. All EMG signals were syn-
chronously sampled at a 1000 Hz sampling rate along with the
dynamometer force signal. In the later process of analysis, all
EMG signals were linearly detrended and digitally high-pass
filtered at a 5 Hz cutoff frequency, followed by full-wave
rectification and low-pass filtering at a 10 Hz cutoff frequency
(Aagaard et al., 2000). If movement artifacts remained present
in the EMG signal, the trials were re-analyzed using a 30 Hz
high-pass cutoff frequency, which effectively removed all low-
frequency signal artefacts. All filtering routines were based on
a fourth-order zero-lag Butterworth filters (Winter, 1990).
During EMG analysis, the following parameters were identi-
fied: (1) peak EMG amplitude within the entire contraction
phase ( 70 to 2500 ms); (2) integrated EMG (iEMG) at time
intervals of 0–30, 50, 100 and 200 ms relative to onset of EMG
integration (defined below); (3) average EMG [mean average
voltage (MAV) 5iEMG/integration time] also at time inter-
vals of 0–30, 50, 100 and 200 ms relative to onset of EMG
integration; (4) the rate of EMG rise (RER), determined as the
slope (DEMG/Dtime) of the filtered EMG signal Schmidtble-
icher & Buehrle, 1987; (Aagaard et al., 2002), determined at
time intervals of 0–30, 50 and 75 ms relative to onset of EMG
−2000
−200
0
2000
4000
0 1000 2000 3000 4000
0
1000
2000
3000
4000
−100
0
100
200
300
400
−40
−30
−20
−10
0
10
20
Center of Mass, Positio
n
Center of Mass, Velocity
Center of Mass, Power
Vertical Force, Fz
Time (msec)
Newton Watt cm .sec−1cm
(a)
(b)
(c)
(d)
eccentric phase concentric phase
Fig. 2. Example of a counter movement jump (data from a single subject) divided into the eccentric and concentric phases,
A, vertical position of center of mass (pos); B, velocity of center of mass (v); C, power of center of mass (P) and D, vertical
force (F).
Neuromuscular fatigue in elite handball
465
integration; and (5) EMG median power frequency (f
med
)
analysis by fast Fourier transformation (FFT) using 256
data points (256 ms) from onset of contraction. Onset of
EMG integration was initiated 70 ms before the onset of
contraction to account for the presence of electromechanical
delay (Aagaard et al., 2002; Suetta et al., 2004). For the
determination of RER, a time interval of 75 ms was used for
the longest interval, because a transient decrease in the EMG
signal was typically observed after 100 ms of neural activity
(Aagaard et al., 2002).
Simulated handball match playing
The simulated handball match consisted of a series of hand-
ball-related movements and was carried out on a handball
court in a separate university gym near the laboratories. The
handball-like movements have been characterized previously
in a work-capacity analysis in elite handball match playing
(Michalsik, 2004). For the purpose of standardization and
simplicity, the movements were divided into different rounds:
A, B and a shot round. The simulated match had seven series
of movements that was constructed to last approximately
7 min each (with a total duration of roughly 50 min) and
consisted of A, B, A, B, each series being completed by a shot
round, followed by a 30-s pause. The movements involved
were walking, jogging, running, fast running, sprinting, back-
wards running, repeated anterior–posterior movements, side-
ways movements, side-cutting and jump shot including
acceleration. The spatial distribution of the various move-
ments is listed in Table 2.
During the simulated handball match, heart rate data were
collected for each subject using a Polar Team system to
evaluate the intensity of the work performed.
Statistical analysis
Data are presented as means standard error (SE) unless
otherwise stated. In addition, range is presented for the
anthropometric data. Changes from Pre to Post the simulated
handball match were evaluated using paired t-tests (two-
tailed, 0.05 level of significance). The relationships between
parameters were evaluated using the Pearson’s product–mo-
ment method and tested for a 0.05 level of significance.
Results
The average time taken to complete the simulated
handball match was 49.4 1.4 min, and the average
heart rate during the simulated handball match was
165 3 b.p.m.
CMJ power, Fz force and RFD
The mechanical jump parameters are shown in Table
3. All displacement parameters were significantly
reduced following the simulated handball match
(JH Po0.01, dS-ecc Po0.05 and dS-con Po0.05).
In spite of the change in displacement parameters, no
significant changes were seen in the duration of the
different phases of the CMJ (i.e.; TDT, T
ecc
,T
eccACC
,
T
eccDEC
and T
con
remained unaltered – Table 3),
which means that the average movement speed had
decreased. F
peak-ecc
was reduced (Po0.05) while
F
peak-con
and F
mean-con
remained unchanged from
Pre to Post of the simulated handball match. Velocity
at peak concentric power (V
ppeak-con
) was reduced
(Po0.01) while force at peak concentric power
(F
ppeak-con
) increased (Po0.01) and as a result peak
concentric jump power (P
peak-con
) remained unal-
tered. Likewise, P
mean-con
showed no change from
Pre to Post. However, RFD (0–50 and 100 ms),
concentric work, peak concentric velocity (V
peak-
con
) and velocity at takeoff (V
takeoff
) all decreased
significantly (Po0.05) from Pre to Post.
Single-joint isometric muscle strength, RFD and impulse
(KinCom)
MVC was significantly reduced for the quadriceps
(11.3%, Po0.01) and hamstring muscles ( 9.8%,
Po0.05) Post the simulated handball match while no
changes were seen for the H/Q-ratio (Table 4). Quad-
riceps muscle RFD decreased significantly at 0–50 ms
(18.3%, Po0.05), 100 ms ( 18.2%, Po0.01) and
200 ms ( 16.1%, Po0.05). Furthermore, the peak
RFD also decreased markedly ( 21.3%, Po0.01).
Hamstring muscle RFD remained unchanged in the
very initial phase of contraction (0–50 ms) while a
significant decline in RFD was evident for the ham-
strings in the latter phase of rising muscle force at
0–100 ms ( 16.9%, Po0.05) and 200 ms ( 17.3%,
Po0.01). The RFD H/Q-ratio increased in the very
early phase of the contraction 0–30 ms (28.6%,
Po0.01) while no changes were seen at any other
time intervals (Table 4).
Quadriceps impulse was reduced at 0–100 ms
(18.0%, Po0.01) and 200 ms ( 17.0%, Po0.01)
(Table 4). Conversely, hamstring impulse increased
significantly from 0 to 30ms (17.9%, Po0.05) while
decreasing at 0–200 ms ( 14.7%, Po0.05). The H/Q
ratio for impulse showed a significant increase at
Table 2. Total distance and distance for the different movements in the
simulated handball match
Amount of
movement
Walking (m) 265.30
Jogging (m) 2781.45
Running (m) 594.30
Fast running (m) 401.25
Sprinting (m) 247.00
Backwards running (m) 265.30
Piston movements (m) 890.40
Sideways movements (m) 274.40
Acceleration in conjunction with
feints and jump shot (m)
598.50
Jump shot (number) 28
Feints (number) 56
Feints and jump shot (number) 28
Total distance, simulated handball match (m) 6,527.20
Thorlund et al.
466
0–30 ms (28.3%, Po0.01) and 50 ms (23.9%,
Po0.05) but no change at 0–100 and 200 ms (Table
4). The relative RFD increased by 23.8% at 0–30 ms
(Po0.05) and decreased by 9.7% at 0–200 ms
(P50.05) for the hamstrings (Table 4). The time at
2/3 MVC (Po0.05) for the hamstrings increased by
33.1% whereas no change occurred in any other time
parameters (Table 4).
EMG
In the initial phase of quadriceps MVC, the mean
average EMG (MAV) decreased at time intervals of
0–30 ( 30%), 50 ( 33%), 100 ( 42%) and 200 ms
(40%) for VL, 0–100 ( 40%) and 200 ms ( 21%)
for RF. Furthermore, MAV decreased at 0–100
(55%) and 200 ms ( 48%) for BF [Fig. 3(a)].
During knee flexor MVC, EMG was reduced in BF
at 0–200 ms ( 31%) [Fig. 3(b)].
Maximal EMG amplitude (peak EMG) decreased
by 28% and 5% during the quadriceps MVC for the
VL and RF, respectively. During hamstrings MVC,
peak EMG was 21% reduced for the BF (Fig. 4).
Changes in the RER during the quadriceps MVC
occurred at 0–30 ms ( 28%) for the VL and at the
time intervals of 0–30 and 50 ms for ST. During
the hamstrings MVC, reduced RER was evident for
the VL and BF at 0–75 ms ( 21% and 36%,
respectively).
Increased f
med
were evident in the quadriceps
MVC for both the VL and BF, 9.7% and 36.9%,
respectively (Table 5).
Discussion
The present study examined the acute fatigue-in-
duced impairment in muscle mechanical properties
and neuromuscular activity in elite handball players
following a simulated handball match. The main
findings were a significant decrease in maximum JH
and MVC for the quadriceps and hamstrings, which
were accompanied by marked decreases in multi-
Table 3. Jump height (JH), displacement of center of mass during eccentric (dS-ecc) and concentric (dS-con) phase
Counter movement jump
Pre Post Change (%)
Center of mass displacement parameters
JH (cm) 39.23 2.08 37.19 1.99 5.2
**
dS-ecc (cm) 33.61 2.23 30.24 2.44 10.0
*
dS-con (cm) 43.57 1.99 39.94 2.04 8.3
*
Time phases of jump
TDT (ms) 746.30 9.02 745.30 9.66 0.1
T
ecc
(ms) 483.70 8.02 495.90 8.34 2.5
T
eccACC
(ms) 310.50 6.71 308.70 6.64 0.6
T
eccDEC
(ms) 173.20 6.36 187.20 6.77 8.1
T
con
(ms) 262.60 5.09 249.40 5.55 5.0
Force parameters
F
peak-ecc
(N/kg) 23.95 1.78 22.52 1.67 6.0
*
F
peak-con
(N/kg) 24.73 1.59 25.00 1.63 1.1
F
mean-con
(N/kg) 20.36 1.16 20.68 1.27 1.6
Power parameters
P
peak-con
(N/kg) 55.61 2.28 56.28 2.36 1.2
V
ppeak-con
(m/s) 2.58 0.36 2.48 0.35 4.0
**
F
ppeak-con
(N/kg) 21.50 1.17 22.67 1.25 5.4
**
P
mean-con
(W/kg) 30.82 1.84 30.33 1.88 1.6
RFD
0–50 ms (N/s/kg) 128.12 8.12 89.05 7.31 30.5
*
0–100 ms (N/s/kg) 106.02 6.88 76.10 6.28 28.2
**
Energy, work
Work-con (J/kg) 8.07 0.79 7.52 0.74 6.8
**
Velocity parameters
V
peak-con
(m/s) 2.89 0.38 2.82 0.36 2.4
**
V
takeoff
(m/s) 2.77 0.39 2.70 0.38 2.6
**
Total duration takeoff (TDT), duration eccentric phase (
T
ecc
), duration of eccentric acceleration (
T
eccACC
) and deceleration (
T
eccDEC
) phase, duration
concentric phase (
T
con
). Peak force during eccentric (
F
peak-ecc
) and concentric (
F
peak-con
) phase, mean force (
F
mean-con
) during the concentric phase. Peak
power (
P
peak-con
), velocity at peak power (
V
ppeak-con
), force at peak power (
F
ppeak-con
) and mean power (
P
mean-con
) during concentric phase. Rate of force
development (RFD), work (Work-con) and peak velocity (
V
peak-con
) during the concentric phase. All parameters are shown before (Pre) and after (Post) the
handball match. Values are means SE;
n
510.
*
P
o0.05,
**
P
o0.01 from Pre to Post.
Neuromuscular fatigue in elite handball
467
joint RFD (CMJ) and single-joint RFD during
quadriceps and hamstrings MVC (KinCom). The
impaired mechanical jumping performance, MVC
and RFD were accompanied by marked decreases
in neuromuscular activity for both the quadriceps
and partial hamstring muscles.
Maximum JH decreased acutely by 5.2% follow-
ing the simulated handball match. Further, various
mechanical parameters in relation to the CMJ were
analyzed to assess the change in leg extension jump
power, work and force. The downward displacement
(dS-ecc) of the BCM was significantly lowered Post
while upward displacement (dS-con) was similarly
reduced. Despite the changes in BCM displacement,
the duration of the different phases of the jump was
unchanged, which means that the velocity during the
jump was reduced as also seen by the decreases in
V
peak-con
,V
ppeak-con
and V
takeoff
. These changes could
indicate a change in jumping strategy toward reduced
velocity to maintain time to produce adequate work
output (and thereby kinetic impulse) so that the
reduction in JH could be kept as small as possible.
Notably, F
peak-con
and F
mean-con
were unaltered
whereas F
ppeak-con
increased by 5%. F
peak-ecc
, on the
other hand, was reduced 6%. Changes in jump
strategy have been observed in handball players
following combined weight and jump training
(Toumi et al., 2004) and it would seem plausible
that changes in jump strategy would occur in re-
sponse to acute muscle fatigue. Therefore, the single
most important parameter responsible for the decline
in BCM velocity likely was the decline in F
z
RFD,
which was 30% reduced after the match at 0–50
and 100 ms. Previously, RFD has been used as a
measure of ‘‘explosive’’ muscle strength because it
denotes the rate of increase in contractile force in the
initial phase of contraction (Aagaard et al., 2002). In
the present study, single-joint RFD was also reduced
with fatigue (16–21%). Furthermore, single-joint
RFD (quadriceps, 0–100 ms) was positively corre-
lated [r50.64–0.65 (Pre–Post); P0.05] to dynamic
RFD obtained during the CMJ (0–100 ms), which
indicates that the fatigue-induced decline in isolated
mechanical muscle function was at least in part
responsible for the observed decline in jumping
performance. RFD is of particular functional im-
portance in fast movements like sprinting or chan-
ging direction that involves very short contraction
times o250 ms (Aagaard et al., 2002; Aagaard, 2003)
but also in a CMJ, which takes a longer time, because
more kinetic impulses can be produced in the begin-
ning of the concentric phase when contractile RFD is
high. Consequently, acute fatigue-induced reductions
in RFD may impair the force production and de-
crease the kinetic ground reaction force impulse
(RFdt) and hence reduce the speed in the explo-
sive-type movements (i.e. jumping, side cutting, etc.)
typically performed in handball. Maximum isolated
Table 4. Maximal isometric strength (MVC), rate of force development (RFD), impulse, relative RFD and time to 1/6, 1/2 and 2/3 MVC for the quadriceps
and hamstrings muscles, respectively, before (Pre) and after (Post) the simulated handball match
Quadriceps Hamstrings H/Q ratio
Pre Post Pre Post Pre Post
MVC (N m/kg) 3.90 0.63 3.46 0.63
**
1.77 0.52 1.59 0.54
*
0.43 0.27 0.45 0.29
RFD
0–30 ms (N m/s/kg) 22.63 2.83 19.24 2.84 6.92 1.53 7.83 1.76 0.28 0.28 0.38 0.22
**
0–50 ms (N m/s/kg) 26.06 2.69 21.29 2.80
*
8.74 1.68 8.56 1.94 0.30 0.29 0.35 0.25
0–100 ms (N m/s/kg) 21.46 1.64 17.55 1.97
**
9.27 1.30 7.71 1.53
*
0.42 0.26 0.42 0.31
0–200 ms (N m/s/kg) 14.19 1.55 11.90 1.47
*
6.74 0.97 5.58 1.17
**
0.47 0.29 0.46 0.30
Peak RFD (N m/s/kg) 35.13 2.86 27.64 3.07
**
15.18 1.92 12.06 2.02 0.42 0.34 0.41 0.29
Impulse
0–30 ms (N m s/kg 10
3
) 9.99 1.92 9.05 1.86 3.31 1.14 3.90 1.12
*
0.32 0.34 0.42 0.31
**
0–50 ms (N m s/kg 10
3
) 30.10 3.15 25.81 3.17 9.71 1.80 10.63 2.02 0.30 0.30 0.38 0.22
*
0–100 ms (N m s/kg 10
3
) 122.96 4.92 100.79 5.44
**
45.91 3.31 41.87 3.82 0.35 0.25 0.38 0.21
0–200 ms (N m s/kg 10
3
) 372.38 8.03 308.96 8.27
**
165.70 5.10 141.31 6.15
*
0.43 0.26 0.44 0.25
Relative RFD
0–30 ms (%MVC/s) 579.1 13.5 550.7 14.3 393.2 11.2 486.8 13.4
*
0–50 ms (%MVC/s) 667.3 12.8 608.8 13.9 491.7 11.6 528.8 14.6
0–100 ms (%MVC/s) 551.5 7.2 505.7 9.5 528.4 9.2 477.0 9.5
0–200 ms (%MVC/s) 363.0 6.5 343.8 7.0 384.3 6.6 346.9 5.9
*
Time
Time at peak RFD (ms) 46.38 3.59 45.95 3.73 66.07 5.64 69.03 5.80
Time at 1/6 MVC (ms) 27.97 2.43 31.89 3.17 39.46 2.98 39.49 3.73
Time at 1/2 MVC (ms) 79.07 4.78 104.24 6.50 97.42 5.60 109.29 7.44
Time at 2/3 MVC (ms) 160.30 6.74 198.74 10.47 128.13 4.32 170.54 7.58
*
Hamstrings/quadriceps ratios (H/Q ratio) are also calculated where relevant. Values are means SE;
n
510.
*
P
0.05,
**
P
o0.01 from Pre to Post. MVC, maximal voluntary contraction.
Thorlund et al.
468
muscle strength (MVC) was significantly reduced
Post the handball match for both the quadriceps
and the hamstring muscles. This is likely to have a
negative influence on the performance of tackles and
position infights between defense and offence players,
respectively.
Surprisingly, jumping power (P
peak-con
,P
mean-con
)
remained unchanged with fatigue even though JH
was reduced (Table 3). Power is the product of force
and velocity and it seems like the decline in velocity
at peak power was counterbalanced by an increase in
F
z
force at the instant of peak power (Table 3). On
the other hand, Work-con was also reduced in
correspondence to the reduction in maximum JH
(Table 3).
Temporal changes in contractile RFD and impulse
have, among other things, been attributed to altera-
tions in motor unit (MU) recruitment and firing
frequency, i.e. altered neural drive (Van Cutsem
et al., 1998; Aagaard et al., 2002; Aagaard, 2003).
Therefore, it seems reasonable to assume that altera-
tions in MU recruitment and a decreased firing
frequency may have played a role in the reduction
of MVC, RFD and impulse presently observed with
fatigue. The present data support this notion because
quadriceps EMG amplitude was markedly reduced
with fatigue [VL and RF, Fig. 3(a)]. Similarly, ham-
string EMG activity decreased (BF) during the knee
flexor MVC, in correspondence to the observed
decrease in flexor MVC. This finding is in accordance
with Mullany et al. (2002), who found decreased
root-mean-square (RMS) EMG amplitude during a
sustained MVC with fatigue. Studies have observed
that during isometric submaximal contractions, re-
cruitment of VL is significantly greater than VM and
RF (Alkner et al., 2000; Pincivero & Coelho, 2000)
whereas a similar degree of activation was seen at
near-maximal contractions (Pincivero & Coelho,
2000). This suggests that more pronounced fatigue
may occur in VL because many of the movements in
the simulated handball match were of submaximal
character. Because Farahmand et al. (1998) have
estimated from cross-sectional area (CSA) that VL
contributes 40% of the total quadriceps muscle
strength (VM 25% and RF, together with vastus
intermedius 35%), this would potentially result in an
even greater loss in quadriceps MVC and RFD. Our
data support this hypothesis because the peak EMG
for VL decreased by 28% during the quadriceps
MVC while it was only 5% reduced for RF. Further-
more, significant changes in MAV were observed at
all time intervals for VL while only being present in
the later time intervals for RF (0–100 and 200 ms).
The observed decrease in neuromuscular activity in
response to a simulated handball match may reflect
decreased conduction velocity (Masuda et al., 1999)
and/or motoneuron firing frequency (Bigland-
Ritchie et al., 1983) even though it has also been
suggested that discharge doublets could occur during
fatigue to avoid a decline in force and thereby
Mean EMG amplitude, MAV (uVolt)
0
100
200
300
400
500
600
700
VL RF BF ST
Mean EMG amplitude, MAV (uVolt)
0
100
200
300
400
500
VL RF
BF ST
30 ms 50 ms 100 ms 200 ms
30 ms 50 ms 100 ms 200 ms
*
**
*
**
** **
*
**
(b)
(a)
Fig. 3. Electromyography (EMG) signal amplitudes Pre
(open bars) and Post (hatched bars) a simulated handball
match. A, maximal voluntary contraction (MVC), quadri-
ceps and B, MVC, hamstrings, values are means SE. Pre
to Post differences:
*
P0.05,
**
Po0.01. The neural effer-
ent drive was calculated as the mean integrated EMG
divided by the respective integration time at the time inter-
vals of 0–30, 50, 100 and 200 ms relative to the onset of
EMG integration. MAV, mean average voltage.
Peak EMG (uV)
0
200
400
600
800
1000
1200
1400
1600
**
*
**
VL RF
BF
ST
MVC, quadriceps MVC, hamstrings
Fig. 4. Peak electromyography (EMG) signal Pre (open
bars) and Post (hatched bars) a simulated handball match.
Values are means SE. Pre to Post differences:
*
Po0.05,
**
Po0.01.
Neuromuscular fatigue in elite handball
469
increase firing frequency (Enoka & Fuglevand,
2001). Supramaximal firing rates above the firing
frequency needed to achieve maximum tetanic ten-
sion have been proposed previously to serve to
enhance RFD (Nelson, 1996; Aagaard, 2003); there-
fore, the marked decrease in neuromuscular activity
presently observed in the early contraction phase (0–
200 ms) may explain the greater impairment in RFD
(16–21% reduced) compared with the reduction in
maximal force (10–11% reduced).
f
med
was used to represent the power spectrum,
because of its lower sensitivity to noise compared
with the mean power frequency (Stulen & De Luca,
1981). In the present study, f
med
increased during
fatigue in quadriceps MVC for the VL and BF (9.7%
and 36.9%, Table 5). This is in contrast to the
decrease in f
med
typically seen with fatigue (Mullany
et al., 2002; Pincivero et al., 2006). The discrepancy
could be due to differences in the fatiguing protocol
and/or in the methodology used because the present
data were obtained during an MVC in which subjects
were asked to contract as hard and fast as possible
(Aagaard et al., 2002; Suetta et al., 2004). The
present changes in f
med
may be explained by de-
creased motor unit synchronization. The degree of
motor unit synchronization depends on the magni-
tude of common synaptic input to the spinal moto-
neurons (Semmler et al., 2002). It may be speculated
that with the present type of neuromuscular fatigue,
the magnitude of common input to the spinal moto-
neurons decreased due to a more dispersed descend-
ing motor program and/or more dispersed sources of
afferent input to the spinal motoneuron pool from
groups III and IV metabosensitive nervefibers.
Based on peak EMG, the magnitudes of antago-
nist hamstring coactivation during the quadriceps
MVC were 10–13% and 17–22% for the BF and ST,
respectively. Notably, no changes in antagonist coac-
tivation were observed in response to fatigue. During
the phase of rising muscle force, antagonist ham-
string coactivation was 1–5% and 3–7% in the BF
and ST, respectively. A fatigue-induced decline in
antagonist coactivation was seen at 0–100 ms for BF,
which, together with the decrease in mean EMG
amplitude during quadriceps MVC [0–100 and
200 ms, Fig. 3(a)] and flexor MVC [0–200 ms, Fig.
3(b)] and the reduced peak EMG amplitude during
the flexor MVC (Fig. 4), altogether indicate a selec-
tive or preferential fatigue in the lateral thigh mus-
cles. Mullany et al. (2002) suggested that a common
neural drive to the knee extensor muscles and the
antagonist BF may exist during knee extension,
which could lead to a more pronounced fatigue in
the lateral (BF) than medial (ST) hamstring muscle.
On the other hand, it seems from our data that
coactivation was greater in ST than BF. Regardless,
preferential fatigue in the lateral hamstring muscle
group could have a potential negative impact on the
neuromuscular control of rotational knee stability
and valgus control.
The origin of fatigue could also have been of a
peripheral nature, where metabolic aspects like gly-
cogen depletion, decreased intracellular pH and
potential changes in the excitation–contraction cou-
pling including Ca
21
kinetics are likely candidates
(Fitts, 2004). However, we have no measurements
that could clarify any peripheral changes in these
parameters
The simulated handball match was established
based on a work-demand analysis by Michalsik
(2004). The goal was to mimic a handball match as
precisely as possible while at the same time meeting
specific demands for standardization. Michalsik
(2004) found that players often play 50 min in a
handball match (2 halves of 30 min each the time
spend on the bench) with an average distance of
3.6 km covered, of which 10.1% was done at high
intensity. In male elite handball players, the average
intensity during a premier league match is 69% of
VO
2max
estimated from heart rate recordings (corre-
sponding to 157 beat/min, Michalsik, 2004). In
our study, the average time to complete the simulated
handball match was 49.4 min with an average heart
rate of 165 beats/min and a distance of 6.5 km
covered, of which 19.1% was performed at a high
intensity. The possibility exists, thereby, that the
Table 5. EMG median power frequency (
f
med
) in the initial contraction phase (0–256 ms) Pre and Post the simulated handball match obtained during rapid
quadriceps and hamstring MVC, respectively
Quadriceps MVC Hamstring MVC
Pre Post Change (%) Pre Post Change (%)
Muscle
Vastus lateralis (VL) (Hz) 73.7 3.6 80.8 3.9 9.7
*
86.0 4.8 83.0 4.0 3.5
Rectus femoris (RF) (Hz) 101.0 3.7 95.2 3.3 5.8 75.9 4.6 77.1 3.3 1.5
Biceps femoris (BF) (Hz) 75.7 4.5 103.6 5.0 36.9
**
107.2 4.5 110.9 4.5 3.4
Semitendinosus (ST) (Hz) 72.1 4.6 95.4 6.2 32.3 92.1 4.9 78.2 5.1 15.1
Values are means SE;
n
510.
*
P
50.05,
**
P
o0.01 from Pre to Post. MVC, maximal voluntary contraction; EMG, electromyography.
Thorlund et al.
470
physiological loading imposed by the simulated
handball match was more intense than that of an
actual handball match. However, recently, the rules
of team handball were revised to allow fast attacks
immediately following scoring, which most likely
have increased the physical intensity during match
play (Ronglan et al., 2006) compared with the work
demand analysis performed by Michalsik (2004).
In conclusion, maximum voluntary strength
(MVC) and rapid force characteristics (RFD, im-
pulse) were drastically reduced for the quadriceps
and hamstring muscles of male elite handball players
following a simulated handball match. Likewise,
eccentric F
z
force, concentric work, BCM movement
and maximum JH were reduced during complex
multi-joint testing (CMJ). These impairments in
muscle mechanical function were accompanied by
marked reductions in neuromuscular activity.
Perspectives
In the present study, fatigue-induced impairment in
mechanical muscle function and reduced neuromus-
cular activity were demonstrated acutely following a
simulated handball match. The decrease in MVC
may potentially lead to impaired functional perfor-
mance during tackling and in fights in the latter part
of the match. Likewise, the reduced RFD likely will
have a negative impact on fast movements like
accelerations, sprints and side cutting. The reduced
vertical JH potentially impairs the ability to block
shots from attacking players and conversely shoot
over the blocks during attack play. Based on these
notions, future studies should be conducted to iden-
tify the specific neuromechanical and cellular origins
of fatigue, while it would also be of great interest to
investigate the impact of different resistance training
regimes in increasing the fatigue resistance (Hickson
et al., 1988; Raastad et al., 2003) during elite hand-
ball match playing.
Key words: fatigue, MVC, RFD, neuromuscular
activity, impaired functional performance.
Acknowledgement
This study was supported by the national Danish organization
for elite sports; Team Danmark.
References
Aagaard P. Training-induced changes in
neural function. Exerc Sport Sci Rev
2003: 31(2): 61–67.
Aagaard P, Simonsen EB, Andersen JL,
Magnusson SP, Dyhre-poulsen P.
Increased rate of force development
and neural drive of human skeletal
muscle following resistance training.
J Appl Physiol 2002: 93: 1318–1326.
Aagaard P, Simonsen EB, Andersen JL,
Magnusson SP, Halkjær-Kristensen J,
Dyhre-Poulsen P. Neural inhibition
during maximal eccentric and
concentric quadriceps contraction:
effects of resistance training. J Appl
Physiol 2000: 89: 2249–2257.
Aagaard P, Simonsen EB, Magnusson
SP, Larsson B, Dyhre-Poulsen P. A
new concept for isokinetic hamstring:
quadriceps muscle strength ratio.
Am J Sports Med 1998: 26(2):
231–237.
Aagaard P, Simonsen EB, Trolle M,
Bangsbo J, Klausen K. Isokinetic
hamstring/quadriceps strength ratio:
influence from joint angular velocity,
gravity correction and contraction
mode. Acta Physiol Scand 1995: 154:
421–427.
Alkner BA, Tesch PA, Berg HE.
Quadriceps EMG/force relationship
in knee extension and leg press.
Med Sci Sports Exerc 2000: 32(2):
459–463.
Baker D, Wilson G, Carlyon B.
Generality vs. Specificity: a comparison
of dynamic and isometric measures of
strength and speed-strength. Eur J
Appl Physiol 1994: 68: 350–355.
Bigland-Ritchie B, Johansson R, Lippold
OCJ, Smith S, Woods JJ. Changes in
motoneurone firing rates during
sustained maximal voluntary con-
tractions. J Physiol 1983: 340:
335–346.
Bojsen-Møller J, Magnusson SP,
Rasmussen LR, Kjaer M, Aagaard P.
Muscle performance during maximal
isometric and dynamic contractions is
influenced by the stiffness of the
tendinous structures. J Appl Physiol
2005: 99: 986–994.
Caserotti P, Aagaard P, Simonsen EB,
Puggaard L. Contraction-specific
differences in maximal muscle power
during stretch-shortening cycle
movements in elderly males and
females. Eur J Appl Physiol 2001: 84:
206–212.
Davies CTM, Rennie R. Human power
output. Nature 1968: 217: 770–771.
Enoka RM, Fuglevand AJ. Motor unit
physiology: some unresolved issues.
Muscle Nerve 2001: 24(1): 4–17.
Farahmand F, Senavongse W, Amis AA.
Quantitative study of the quadriceps
muscles and trochlear groove geometry
related to instability of the
patellofemoral joint. J Orthop Res
1998: 16(1): 136–143.
Farrell M, Richards JG. Analysis of the
reliability and validity of the kinetic
communicator exercise device. Med Sci
Sports Exerc 1986: 18(1): 44–49.
Fitts RH. Mechanisms of muscular
fatigue. Princ Exerc Biochem 2004: 46:
279–300.
Gorostiaga EM, Granados C, Iba
´n
˜ez J,
Gonza
´lez-Badillo JJ, Izquierdo M.
Effects of an entire season on physical
fitness changes in elite male handball
players. Med Sci Sports Exerc 2006:
38(2): 357–366.
Ha
¨kkinen K, Komi PV, Ale
´n M. Effect of
explosive type strength training on
isometric force – and relaxation-time,
electromyographic and muscle
fibre characteristics of leg extensor
muscles. Acta Physiol Scand 1985: 125:
587–600.
Heitman BL. Evaluation of body fat
estimated from body mass index,
skinfolds and impedance. A
comparative study. Eur J Clin Nutrit
1990: 44(11): 831–837.
Hickson RC, Dvorak BA, Gorostiaga
EM, Kurowski TT, Foster C. Potential
for strength and endurance training to
amplify endurance performance. J
Appl Physiol 1988: 65(5): 2285–2290.
Holsgaard Larsen A, Caserotti P,
Puggard L, Aagaard P. Reproducibility
Neuromuscular fatigue in elite handball
471
and relationship of single-joint strength
vs multi-joint strength and power in
aging individuals. Scand J Med Sci
Sports 2007: 17: 43–53.
Kellis E, Baltzopoulos V. Resistive
eccentric exercise: effects of visual
feedback on maximum moments of
knee extensors and flexors. J Orthop
Sports Phys Ther 1996: 23: 120–124.
Masuda K, Masuda T, Sadoyama T,
Inaki M, Katsuta S. Changes in surface
EMG parameters during static and
dynamic fatiguing contractions. J
Electromyogr Kinesiol 1999: 9: 39–46.
Michalsik L. Analysis of working
demands of Danish handball players.
What’s going on in the gym? Learning,
teaching and research in physical
education. Denmark: Institute of
Sports Science and Clinical
Biomechanics, University of Southern
Denmark, 2004.
Mullany H, O’Malley M, Gibson ASC,
Vaughan C. Agonist–antagonist
common drive during fatiguing knee
extension efforts using surface
electromyography. J Electromyogr
Kinesiol 2002: 12: 375–384.
Nelson AG. Supramaximal activation
increases motor unit velocity of
unloaded shortening. J Appl Biomech
1996: 12: 285–291.
Pincivero DM, Coelho AJ. Activation
linearity and parallelism of the
superficial quadriceps across the
isometric intensity spectrum. Muscle
Nerve 2000: 23(3): 393–398.
Pincivero DM, Gandhi V, Timmons MK,
Coelho AJ. Quadriceps femoris
electromyogram during concentric,
isometric and eccentric phases of
fatiguing dynamic knee extensions.
J Biomech 2006: 39(2): 246–254.
Raastad T, Glomsheller T, Bjøro T,
Halle
´n J. Recovery of skeletal muscle
contractility and hormonal responses
to strength exercise after two weeks of
high-volume strength training. Scand
J Med Sci Sports 2003: 13: 159–168.
Ronglan LT, Raastad T, Børgesen A.
Neuromuscular fatigue and recovery
in elite female handball players.
Scand J Med Sci Sports 2006: 16(4):
267–273.
Semmler JG, Komatz KW, Dinenno DV,
Zhou S, Enoka RM. Motor unit
synchronisation is enhanced during
slow lengthening contractions of a
hand muscle. J Physiol 2002: 545: 681–
695.
Schmidtbleicher D, Buerhle M. Neuronal
adaption and increase of cross-
sectional area studying different
strength training methods. In:
Biomechanics X-B. ed. Johnson B.
Champaign, IL: Human Kinetics,
1987: 615–620.
Stulen FB, De Luca CJ. Frequency
parameters of the myoelectric signal as
a measure of conduction velocity.
IEEE Trans Biomed Eng 1981: 28:
515.
Suetta C, Aagaard P, Rosted A, Jakobsen
AK, Duus B, Kjaer M, Magnusson SP.
Training-induced changes in muscle
CSA, muscle strength, EMG, and
rate of force development in elderly
subjects after long-term unilateral
disuse. J Appl Physiol 2004: 97:
1954–1961.
Thorstensson A, Karlsson J, Viitasalo
HT, Luhtanen P, Komi PV. Effect of
training on EMG of human skeletal
muscle. Acta Physiol Scand 1976: 98:
232–236.
Toumi H, Best TM, Martin A, Poumarat
G. Muscle plasticity after weight and
combined (weight1jump) training.
Med Sci Sports Exerc 2004: 36(9):
1580–1588.
Van Cutsem M, Duchateau J, Hainaut K.
Changes in single motor unit behavior
contribute to the increase in
contraction speed after dynamic
training in humans. J Physiol 1998:
513: 295–305.
Winter DA. Biomechanics and motor
control of human movement, 2nd edn.
New York: Wiley-Interscience,
1990.
Zebis MK, Ellingsgaard H, Kjaer M,
Aagaard P. Definition of a new H/Q
ratio based on explosive muscle
strength in soccer players. Med Sci
Sports Exerc 2003: 35(Suppl 5): 324.
Thorlund et al.
472
