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ORIGINAL RESEARCH

The Effects of Neuromuscular Training on Knee Joint


Motor Control During Sidecutting in Female
Elite Soccer and Handball Players
Mette K. Zebis, cand.scient, PhD,* Jesper Bencke, PhD, Lars L. Andersen, cand.scient,*
Simon Dssing, MD, Tine Alkjr, PhD, S. Peter Magnusson, DMedSci,
Michael Kjr, MD, DMedSci, and Per Aagaard, PhD

Key Words: hamstrings, quadriceps, gluteus medius, prevention, ACL,


Objective: The project aimed to implement neuromuscular training test-retest, prophylactic intervention, surface EMG, CMJ, dynamic
during a full soccer and handball league season and to experimentally valgus
analyze the neuromuscular adaptation mechanisms elicited by this
training during a standardized sidecutting maneuver known to be (Clin J Sport Med 2008;18:329337)
associated with non-contact anterior cruciate ligament (ACL) injury.
Design: The players were tested before and after 1 season without
implementation of the prophylactic training and subsequently before INTRODUCTION
and after a full season with the implementation of prophylactic Female soccer and team handball athletes have a reported
training. 4- to 8-fold higher incidence of anterior cruciate ligament
(ACL) injury than their male counterparts,1,2 causing increased
Participants: A total of 12 female elite soccer players and 8 female focus on the prevention of ACL injury in female athletes. An
elite team handball players aged 26 6 3 years at the start of the study. important issue in this respect is the identification of risk
factors. Many of the factors related to the gender prevalence37
Intervention: The subjects participated in a specific neuromuscular
are linked to differences in knee joint anatomy and circulating
training program previously shown to reduce non-contact ACL
hormones and are therefore difficult to affect. In contrast,
injury.
specific neuromuscular control strategies and movement pat-
Methods: Neuromuscular activity at the knee joint, joint angles at terns in female athletes can be modified by prophylactic
the hip and knee, and ground reaction forces were recorded during training.
a sidecutting maneuver. Neuromuscular activity in the prelanding Non-contact ACL injuries typically occur during run-
phase was obtained 10 and 50 ms before foot strike on a force plate ning, cutting, and jumping tasks when the knee is slightly
and at 10 and 50 ms after foot strike on a force plate. flexed and in valgus.8 Compared to male athletes, female
athletes seem to display distinct neuromuscular strategies and
Results: Neuromuscular training markedly increased prelanding knee motion patterns in motor tasks in which there is a high
activity and landing activity electromyography (EMG) of the semi- risk of ACL injury.6,9,10 Specifically, female athletes tend
tendinosus (P , 0.05), while quadriceps EMG activity remained to land in more extended knee joint positions11,12 and with
unchanged. increased knee valgus angles during running and sidecutting.
Conclusions: Neuromuscular training increased EMG activity for During isolated knee extension, quadriceps contraction force
the medial hamstring muscles, thereby decreasing the risk of dynamic can produce substantial anterior directed shear of the tibia
valgus. This observed neuromuscular adaptation during sidecutting relative to the femur, especially at extended knee joint
could potentially reduce the risk for non-contact ACL injury. angles.1315 The shear force is counteracted not only by the
ACL but also by means of hamstring coactivation.13 Thus,
coactivation of the hamstring muscles is needed to balance
contraction of the quadriceps,16 compress the joint, and control
Submitted for publication December 4, 2007; accepted May 4, 2008. high knee extension and abduction torques.
From the *National Research Centre for the Working Environment; Institute of There is a synergistic relationship between the ACL and
Sports Medicine; Gait Laboratory, Hvidovre University Hospital; Depart- hamstring muscle group,15,1719 which in humans exhibits a
ment of Neuroscience and Pharmacology, University of Copenhagen; and
{Institute of Sports Sciences and Clinical Biomechanics, University of complex behavior.20 Although the latency of the ACL ligamento-
Southern Denmark, Copenhagen, Denmark. muscular reflex arc (.100 ms) seems too long to provide
The authors state that they have no financial interest in the products mentioned a protective mechanism per se for the ACL in acute situations,20
within this article. afferent feedback from the ACL potentially plays an important
Reprints: Mette Kreutzfeldt Zebis, cand.scientist, PhD, Institute of Sports
Medicine Copenhagen, Bispebjerg Hospital, Bispebjerg Bakke 23, Building
role in the updating and formation of preprogrammed motor
8, DK-2400 Copenhagen NV, Denmark (e-mail: mettezebis@hotmail.com). patterns for optimizing knee joint stabilization.21 These findings
Copyright 2008 by Lippincott Williams & Wilkins suggest that a change (re-programming) in movement pattern and

Clin J Sport Med  Volume 18, Number 4, July 2008 329


Zebis et al Clin J Sport Med  Volume 18, Number 4, July 2008

neuromuscular activity by means of training might reduce the parameters (see below) with a period between tests of 9 6
incidence of ACL injury among female athletes.2228 4 days.
In fact, employment of neuromuscular training was
recently shown to reduce the incidence of ACL injuries in Intervention Study
female elite handball players.24 A prophylactic neuromuscular Twenty female elite handball and soccer players
training program was developed to focus on risk-reducing (2 teams) (age, 26 6 3; height, 174 6 6; weight, 70 6 9)
movement strategies during landing, deceleration, and side- participated in the training study after a previous control
cutting maneuvers.24 Despite the success of this program, the period. One team (n = 8) participated in the best national
underlying neuromuscular adaptation mechanisms elicited by handball league, whereas the other team (n = 12) participated
this type of training remain unknown. The well-established in the best national soccer league in Denmark.
effect of neuromuscular training in reducing the incidence of Ethical approval was obtained from the local ethics com-
ACL injuries in female sports24,28,29 may thus be related to mittee, and informed consent was obtained from all players.
a remodeling of existing motor programs towards movement
and activation patterns that reduce ACL strain. ACL Intervention Injury Prevention Program
Therefore, the purpose of this study was to investigate The neuromuscular training program was originally
the effect of neuromuscular training on the specific neural developed at the Oslo Sports Trauma Research Center (www.
activation pattern of the hamstring and quadriceps muscles klokavskade.no). We modified the program to include 6 levels,
during standardized sidecutting maneuvers, a movement clos- each consisting of 3 exercises. Each of the 6 levels had to be
ely associated with non-contact ACL injury.8 followed 2 times per week for 3 weeks before progressing to
The main aim of the present study was to investigate the the next level. After completing the program (18 weeks), the
effects of prophylactic neuromuscular training on neuromus- 6 levels were performed again with increasing difficulty of
cular function at the knee joint during sidecutting in female the exercises. The main focus of the exercises was to improve
elite athletes at risk for ACL injury. awareness and neuromuscular control of the hip, knee, and
It was hypothesized that neuromuscular training would ankle muscles during standing, running, cutting, jumping, and
significantly change the pattern of neuromuscular activation landing tasks with simultaneous ball handling and included
for the lower limb muscles in a manner that potentially reduces exercises on wobble board (disc diameter, 38 cm; Norpro,
specific risk factors predisposing for ACL injury among Notoddon, Norway, 2000) and balance mat (40 3 50 cm2;
female elite team handball and soccer players. 7-cm-thick; Alusuisse Airex, Sins, Switzerland, 2000). The
program was performed twice weekly, and each exercise
session lasted 20 minutes. After careful supervision, the
MATERIALS AND METHODS involved team physiotherapists and physical trainers were
involved in the coaching of the neuromuscular training
Study Design program. The principal examiner conducted successive
A test-retest study was used to separately evaluate follow-ups every second week.
reproducibility of EMG, goniometer, and force plate measure- Data on injury, match exposure and training frequency,
ments during sidecutting in 8 individuals (see Subjects for and type of training were recorded for each week.
more details). Furthermore, the reproducibility of EMG nor-
malization procedure relative to peak amplitude during side- Outcome Measures
cutting or relative to peak amplitude during MVC was The electrode sites were shaved with a hand razor and
examined. For this purpose, the EMG activity during maximal carefully cleaned with ethanol before electrode placement on
isometric quadriceps and hamstring contraction (MVC) was the dominant leg. During the first visit, transparent paper was
obtained. placed over the leg, and recognizable anatomical landmarks
Neuromuscular activity at the knee joint was measured were identified and drawn on the paper together with the sites
during sidecutting before and after a 6-month period (control of the electrodes for each subject. This was done to ensure
season) of regular training (ie, without prophylactic training). precise and standardized placement of the electrodes at each
Furthermore, the players were tested for jump performance visit. Bipolar surface EMG electrodes (Medicotest M-00-S)
expressed by countermovement jumps (CMJ). with a 2.0-cm interelectrode distance were placed on the
After the control season, 12 months of prophylactic medial portion of the vastus lateralis (VL), vastus medialis
neuromuscular training was implemented, and the effect of (VM), and rectus femoris (RF) muscles of the quadriceps
neuromuscular training on neuromuscular activity during the femoris muscle, on the biceps femoris caput longus (BFcl) and
sidecutting maneuver was evaluated. In addition, changes in semitendinosus (ST) muscles of the hamstring muscles, and
jump performance were measured. finally on the superficial, anterior part of the gluteus medius
(GT) muscle and the muscle belly of gastrocnemius lateralis
(GL) and medialis (GM).
Subjects
The EMG electrodes were connected directly to small
Test-retest Study preamplifiers, and the signals were led through shielded wires
Eight female elite team handball players (age, 28 6 5 to custom-built differential instrumentation amplifiers with
years; height, 172 6 6 cm; weight, 71 6 9 kg) were tested on a bandwidth of 10 to 10,000 Hz and a common mode rejection
2 separate days for selected biomechanical and neuromuscular ratio .100 dB.16,30,31 It was previously documented with this

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Clin J Sport Med  Volume 18, Number 4, July 2008 Neuromuscular Training Changes Knee Joint Motor Control

experimental set-up that the amount of EMG crosstalk is (prelanding phase), and in the 10- and 50-ms time intervals
negligible (2 to 6%).16 Knee and hip joint positions were con- after foot strike (landing phase), respectively.
tinuously measured with flexible goniometers (G180; Penny & The test-retest study was mainly executed to test repro-
Giles, Christchurch, United Kingdom) that were positioned ducibility of the sidecutting maneuver. Further, the test-retest
laterally over the left knee and hip joint. Calibration of the study made it possible to examine 2 normalization procedures
goniometer signal was performed at anatomical knee and hip for highest reproducibility in the present study.
joint angles of 0 and 90 degrees using a geometric retractor.
The EMG, ground reaction forces, and goniometer position Normalization to Peak Amplitude Obtained
signals were sampled synchronously at 1000 Hz using an exter- During Sidecutting
nal A/D-converter (dt2801-A, Data Translation, Marlborough, For each sidecutting maneuver trial, the average RMS
USA) and stored on a personal computer for later analysis. EMG amplitude in the predefined time intervals was nor-
A sampling frequency of 1000 Hz for surface EMG malized to the peak amplitude measured in the same trial. This
was used in numerous previous studies30,3234 because most normalization procedure was done for each muscle examined
of the surface EMG signal is concentrated in the band between (Example: Trial 1, vastus lateralis)
20 and 200 Hz, and only negligible content occurs beyond RMS EMG amplitudei
500 Hz.35 Neuromuscular activityi ;
Peak EMG amplitudeTRIAL 1
EMG Signal Treatment where i denotes time interval.
All EMG signals were highpass filtered (5 Hz cutoff)
and smoothed by a symmetrical moving RMS filter (30 ms Normalization to Peak Amplitude Obtained
time constant).31 RMS EMG activity (mean average ampli- During MVC
tude) was obtained in predefined time intervals and sub- For each sidecutting maneuver trial, the average RMS
sequently normalized to the peak RMS EMG amplitude EMG amplitude in the predefined time intervals was nor-
recorded during the sidecutting maneuver. This procedure of malized to the highest peak amplitude obtained from 3 trials of
EMG normalization was chosen on the basis of the test-retest MVC. This was carried out for each examined muscle except
results (see below). Onset of EMG was determined by an gluteus medius, where no standardized MVC was attainable
automated signal algorithm, being the instant at which the (Example: Trial 1, vastus lateralis).
rectified EMG amplitude exceeded the mean of the preceding RMS EMG amplitudei
50 data points by more than 5% of the peak rectified EMG Neuromuscular activityi ;
amplitude. This procedure ensured that premature short- Peak EMG amplitudeMVC
lasting bursts of EMG activity were not identified as the onset where i denotes time interval.
of EMG (Figure 1). For both procedures, the neuromuscular activity in
EMG activity was obtained during maximal voluntary a given time interval for each player was then calculated as the
isometric muscle contraction (MVC) (KinCom, Kinetic Com- average of the 5 trials performed at each test session (ie, base-
municator; Chattecx Corp., Chattanooga, TN).31 The reli- line, before, and after).
ability and validity of the dynamometer have previously been
described in detail.36 Statistical Methods
Sidecutting and CMJ measurements were performed on Data are presented as means 6 standard deviation (SD).
a force plate (AMTI, Advanced Mechanical Technology, Inc.) Longitudinal changes were evaluated by the Friedman 2-way
with simultaneous EMG recordings. Goniometry (see above) analyses of variance by ranks (related samples) in which chan-
was used to record the knee and hip joint angles during side- ges were localized by multiple comparisons. Differences
cutting movements. Countermovement jump was performed between 2 tests were evaluated by Wilcoxon signed rank test
with the hands placed at the hip (akimbo), and maximal jump for paired samples. Test-retest reliability was assessed by
height was calculated from the flight time: Spearman rank correlation, intraclass correlation coefficients
(ICC), and coefficient of variation (CV).
h g 3 t2 =8 All tests were performed as 2-tailed tests at a 5% level of
where h is height of rise of body center of mass, g is significance.
acceleration of gravity, and t is the flight time. The stand-
ardized sidecutting maneuver was performed with a fixed in- RESULTS
step distance to the force plate (2 m). Instructions were given
to the subjects to perform the sidecutting as fast and forceful as Test-retest Study
possible to simulate a match situation. In each test session, 5 Test-retest data are shown in Tables 1 through 3. Mod-
sidecutting and 5 CMJ trials were performed by each subject, erate to high reproducibility was demonstrated for most of
respectively, and the average of these 5 trials was calculated for the examined parameters,37 indicating that the sidecutting
all parameters examined. maneuver test was highly reproducible.
Neuromuscular activity refers to the magnitude of nor- A higher reproducibility for most of the examined
malized RMS EMG amplitude in the given time intervals muscles were observed when normalizing to the peak EMG
examined. Neuromuscular activity during sidecutting was amplitude obtained during sidecutting maneuver rather than
obtained in the 10- and 50-ms time intervals before foot strike peak EMG amplitude obtained during MVC. Therefore,

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Zebis et al Clin J Sport Med  Volume 18, Number 4, July 2008

FIGURE 1. An example of raw EMG


activity during sidecutting in 1 subject.
The dotted lines represent the defined
onset of EMG. Full lines represent the
ground contact phase of the sidecut-
ting, named the landing phase.

normalization to peak EMG amplitude obtained during values (0 to 10 ms before landing) for mm. semitendinosus and
sidecutting was chosen. For example, when normalizing to biceps femoris were 0.861 and 0.963, respectively (Table 1).
peak EMG amplitude measured during sidecutting, the ICC In comparison, the ICC values were 0.532 and 0.609 for mm.

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Clin J Sport Med  Volume 18, Number 4, July 2008 Neuromuscular Training Changes Knee Joint Motor Control

TABLE 1. Test-retest Reliability of Normalized EMG Activity During Sidecutting (10 ms Pre-landing)
Test Mean (6SD) Retest Mean (6SD) Wilcoxon P Values ICC Spearmans Rho CV %
Normalized to peak amplitude
during MVC
Vastus lateralis (% of max) 42 6 19 45 6 14 0.889 0.675* 0.420 26.04
Vastus medialis (% of max) 54 6 11 52 6 13 0.779 0.389 0.526 18.50
Rectus femoris (% of max) 35 6 14 41 6 19 0.093 0.925* 0.857* 19.09
Gluteus medius (% of max)
Biceps femoris (% of max) 36 6 14 38 6 34 0.483 0.609* 0.790* 49.75
Semitendinosus (% of max) 51 6 21 31 6 13 0.025* 0.532* 0.476 47.12
Gastroc. lateralis (% of max) 74 6 34 68 6 28 0.401 0.791* 0.786* 25.27
Gastroc. medialis (% of max) 71 6 28 63 6 23 0.575 0.728* 0.635 24.94
Normalized to peak amplitude
during sidecutting
Vastus lateralis (% of max) 39 6 12 45 6 12 0.128 0.811* 0.713* 18.33
Vastus medialis (% of max) 46 6 11 52 6 12 0.401 -0.039 -0.048 24.23
Rectus femoris (% of max) 34 6 13 38 6 16 0.116 0.917* 0.946* 16.80
Gluteus medius (% of max) 55 6 19 50 6 19 0.441 0.803* 0.467 20.51
Biceps femoris (% of max) 43 6 14 42 6 16 0.396 0.963* 0.857* 9.06
Semitendinosus (% of max) 56 6 19 49 6 20 0.183 0.861* 0.738* 19.52
Gastroc. lateralis (% of max) 36 6 13 35 6 10 0.833 0.635 0.419 22.50
Gastroc. medialis (% of max) 32 6 9 33 6 16 0.612 0.854* 0.826* 19.71
*Denotes P , 0.05.

semitendinosus and biceps femoris, respectively, when nor- Neuromuscular Activity in the
malizing to peak amplitude obtained during MVC (Table 1). Prelanding Phase
The low reproducibility of the neuromuscular activity of Pre- to post-training neuromuscular activity in the time
vastus medialis regardless of normalization procedure is not interval 50 ms before toe down of the m. semitendinosus
unexpected and could be due to its function as a stabilizer of increased significantly from 41 6 12% to 52 6 16% (P ,
patella (Table 1). 0.01). Furthermore, in the very initial time interval before
landing (10 ms), neuromuscular activity of m. semitendinosus
Control Season increased from 32 6 15% to 44 6 19% (P , 0.01; Table 4;
Two ACL injuries were observed during the control Figure 2, left), whereas the 10-ms pre-activity level for m.
season. Neuromuscular pre-activity (Table 4) and landing acti- gluteus medius decreased from 62 6 15% to 51 6 14% (P ,
vity, onset of EMG, knee joint angle, and hip joint angle 0.05; Table 4; Figure 3).
remained unchanged in the sidecutting maneuver during the
control season. Furthermore, no change was observed in jump- Neuromuscular Activity in the Landing Phase
ing performance as measured by maximal CMJ. Neuromuscular activity measured in the 10-ms time
interval after foot strike increased for semitendinosus from
Intervention Season (Prophylactic Training) 29 6 12% to 39 6 20% (P ,0.05; Figure 2, right). However,
No ACL injuries were observed in the intervention in the 50-ms interval after foot strike, neuromuscular activity
season. remained unchanged in semitendinosus, whereas biceps

TABLE 2. Test-retest Reliability of Absolute EMG Activity During Sidecutting (Mean Average RMS Amplitude)
Preactivity (10 ms) Test Mean (6SD) Retest Mean (6SD) Wilcoxon P Value ICC Spearmans Rho CV %
Vastus lateralis (uV) 208 6 109 208 6 96 1.000 0.951* 0.810* 14.12
Vastus medialis (uV) 193 6 36 243 6 109 0.208 0.640 0.690 29.89
Rectus femoris (uV) 154 6 76 147 6 79 0.674 0.921* 0.595 18.70
Gluteus medius (uV) 199 6 176 171 6 88 0.674 0.841* 0.571 38.39
Biceps femoris (uV) 137 6 46 127 6 75 0.484 0.837* 0.690 23.79
Semitendinosus (uV) 258 6 87 176 6 76 0.017* 0.901* 0.548 30.44
Gastroc. lateralis (uV) 144 6 78 149 6 92 1.000 0.930* 0.833* 19.84
Gastroc. medialis (uV) 190 6 65 176 6 78 0.327 0.674* 0.881* 26.35
*Denotes P , 0.05.

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TABLE 3. Test-retest Reliability of Selected Parameters During Sidecutting


Variables Test Mean (6SD) Retest Mean (6SD) Wilcoxon P Value ICC Spearmans Rho CV %
Knee angle at landing (deg) 27 6 10 31 6 14 0.123 0.851* 0.857* 20.21
Hip angle at landing (deg) 47 6 19 47 6 14 0.889 0.922* 0.881* 12.90
Fz Peak (N) 1774 6 394 1836 6 365 0.484 0.851* 0.857* 10.32
Contact time (ms) 343 6 48 316 6 60 0.036* 0.934* 0.881* 7.99
CMJ (cm) 24.5 6 3.0 23.9 6 2.6 0.018* 0.988* 1.000* 2.93
Onset of ST EMG (ms) 151.2 6 27.1 134.2 6 20.7 0.067 0.806* 0.611 12.34
*Denotes P , 0.05.

femoris activity decreased from 42 6 14% to 32 6 11% (P , for magnitude and timing of the neuromuscular activity, which
0.01). Neuromuscular activity in gluteus medius decreased at indicates that the sidecutting maneuver is a consistent motor
the 10-ms and 50-ms time intervals after foot strike from 65 6 program that the player has developed during years of training.
16% to 52 6 13% and 68 6 13% to 58 6 12%, respectively The main finding in the present study was that neuro-
(P , 0.05). muscular training induced a change in the pattern of neuro-
muscular activation of the hamstring muscles during sidecutting.
Onset of EMG Activity The selective increase in semitendinosus activity in the pre-
EMG activity onset changed in semitendinosus from landing phase and the initial landing phase in parallel with the
168 6 70 ms before foot strike to 140 6 26 ms after the unchanged neuromuscular activity of the quadriceps muscles
intervention period (P , 0.05). The instant of EMG activity may represent an important adaptation in response to neuromus-
onset remained unchanged for all other muscles examined. cular training. During rapid movements like sidecutting, which
The order of onset of EMG activity for the examined muscles involve substantial eccentric quadriceps forces,38 it seems
during sidecutting was identical before and after intervention. essential to have adequate neural preactivation of the hamstring
The order was as follows: (1) gluteus medius; (2) hamstring muscles just before ground contact to protect the ACL. In
muscles; (3) gastrocnemius lateralis and medialis; and finally response to the present intervention, neuromuscular preactivity in
and closest to the time of landing (4) quadriceps (Table 5). the semitendinosus was increased during sidecutting from 41 6
Joint Angles 12% to 52 6 16% of maximal EMG. In accordance with our
findings, a previous study found that the hamstrings are not
Knee and hip joint angle at landing remained unchanged
activated maximally during rapid sidecutting, and it was spec-
(before, 30 6 11 degrees; after, 31 6 9 degrees; Figure 4).
ulated that increased coactivation of the hamstring muscles would
Jumping Performance result in a nonoptimal execution of the sidecutting maneuver.38
CMJ jump height increased from 27 6 4 cm to 29 6 4 This latter notion was not confirmed by the present results
cm (P , 0.001) after training (Figure 5). because duration of the sidecutting (ground contact time) was not
affected, despite increased neuromuscular activity in the semite-
ndinosus muscle.
DISCUSSION A study by Hewett et al39 identified dynamic valgus of
The sidecutting maneuver is a movement that the player the knee as a predisposing factor for ACL injury in female
is able to perform in match situations when the time for athletes. The balance between medial-lateral hamstring recruit-
decision-making about posture correction is extremely limited. ment seems highly important for the control of dynamic val-
The present study demonstrated high test-retest reproducibility gus. Female athletes have a disproportionately greater EMG
activity in their lateral hamstrings (biceps femoris) than male
TABLE 4. Neuromuscular Activity During Sidecutting
(10 ms Pre-landing) TABLE 5. Onset of EMG During Sidecutting
Normalized to Peak Time for
Amplitude During Pre Post Onset (ms) Before Pre Post Order of
Sidecutting Baseline (6SD) Mean (6SD) Mean (6SD) Foot Strike Mean (6SD) Mean (6SD) Onset (Pre/Post)
Vastus lateralis 44 6 15 45 6 17 48 6 12 Vastus lateralis 111 6 44 103 6 24 7/7
Vastus medialis 49 6 18 55 6 12 54 6 12 Vastus medialis 114 6 46 119 6 46 6/8
Rectus femoris 37 6 21 42 6 17 45 6 17 Rectus femoris 103 6 39 99 6 38 8/6
Gluteus medius 63 6 16 62 6 15 51 6 14* Gluteus medius 193 6 70 214 6 67 1/1
Biceps femoris 38 6 16 37 6 15 32 6 14 Biceps femoris 171 6 78 146 6 41 2/2
Semitendinosus 33 6 14 32 6 15 44 6 19* Semitendinosus 168 6 70 140 6 26* 3/3
Gastroc. lateralis 31 6 15 33 6 14 34 6 15 Gastroc. lateralis 125 6 35 132 6 39 5/4
Gastroc. medialis 34 6 14 32 6 15 32 6 15 Gastroc. medialis 129 6 25 131 6 27 4/5
*Significant difference, P , 0.05. *Significant difference, P , 0.05.

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FIGURE 2. Neuromuscular activity


recorded for the medial (ST) and lat-
eral (Bfcl) hamstring muscles before
and after neuromuscular training.
(Left) Mean average EMG amplitude
in the 10-ms time interval before foot
strike during sidecutting. (Right) 0- to
10-ms interval after landing. *Signifi-
cant difference between pre and post,
P , 0.05.

athletes when landing from a jump.6 Increased lateral ham- recommended by Kain et al, whereby the hamstring muscles
string motor unit firing potentially leads to a more open medial were activated before the quadriceps muscles and before initial
joint space and thereby potentially contributes to increased ground contact41 both before and after intervention. A main
dynamic valgus. Furthermore, Myer et al10 found that female finding in this study was that a selective change in EMG onset
athletes demonstrated a reduced medial-to-lateral (VM-to-VL) was observed for the semitendinosus muscle after training.
quadriceps EMG ratio compared to male athletes; this factor Thus, EMG onset occurred closer to the time of landing but
could also contribute to dynamic valgus in high-risk man- still before the onset of quadriceps EMG (VL, VM, RF). In
euvers. During sidecutting, medial hamstring muscle contrac- addition to the increased neuromuscular preactivity of semi-
tion therefore seems very important in compressing the medial tendinosus, the present observation may reflect a further
knee joint compartment and thereby counteracting the risk of optmization of the motor program. Interestingly, similar
dynamic valgus. Notably, the present intervention regime changes in semitendinosus EMG onset during sidecutting
resulted in an elevated ratio of preactivation EMG between was previously seen in male team handball players after
medial hamstring and quadriceps muscles during sidecutting. a period of neuromuscular training.42 In support of an opti-
Neuromuscular preplanning allows feed-forward re- mization theory, Cowling and Steele43 found that during
cruitment of the musculature that controls knee joint stability a deceleration task, the semimembranosus EMG onset occurred
during landing and pivoting maneuvers.40 The female athletes closer to the time of toe-down contact in males compared to
in the present study displayed a muscle activation pattern females, which may have enabled hamstring muscle activity to
better coincide with the high tibiofemoral shear forces generated
just after initial ground contact.43
Decreased activation of proximal stabilizing muscles
may lower the load-bearing capacity of the leg. Surprisingly,
we found a decrease in gluteus medius activity after the period
of neuromuscular training. Our finding could be explained
by the role of the anterior part of gluteus medius to act as
an internal hip rotator when the hip joint is flexed.44 Internal
femoral rotation during the sidecutting maneuver potentially
increases knee valgus moments during the landing phase,
which potentially increases strain and stress in the ACL. In a
3-dimensional study examining the kinetics of the sidecutting
maneuver, Bencke et al found that hip extensors, outward
rotators, and hip adductors are the most loaded muscle groups
around the hip joint during the crucial early part of the
sidecutting maneuver.45 This finding could indicate that high
neuromuscular activity of gluteus medius is not beneficial
during sidecutting maneuvers. In contrast to landing from a
jump, the sidecutting maneuver involves a change in direction,
FIGURE 3. Neuromuscular activity (mean average EMG which makes the forces in the frontal plane highly important.
amplitude) for gluteus medius in the 10-ms time interval before The role of gluteus medius during sidecutting maneuvers may
foot strike during sidecutting, before and after neuromuscular therefore be different from its role in movements involving
training. *Significant difference, P , 0.05. 1-leg landings in the sagittal plane.45

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Zebis et al Clin J Sport Med  Volume 18, Number 4, July 2008

although plyometric exercises were used less than in the


program by Hewett et al.48

CONCLUSIONS
An increased ratio between m. semitendinosus and m.
biceps femoris neuromuscular activity may help to prevent
excessive external rotation of the tibia and lateral joint com-
pression during instep and sidecutting maneuvers, thereby
decreasing the risk of dynamic valgus. After neuromuscular
training, semitendinosus EMG activity was selectively in-
creased during sidecutting, which likely represents an impor-
tant adaptation mechanism because it potentially decreases the
risk of dynamic valgus. Jumping performance was additionally
enhanced as a result of the neuromuscular training.

FIGURE 4. Knee joint angle at the instant of landing before and ACKNOWLEDGMENTS
after neuromuscular training. The dotted line represents a knee
This study was supported by grants from the Danish
joint angle at 30 degrees. (0 degrees = full knee extension).
Ministry of Culture Committee for Sports Research, the Team
Denmark Elite Sports Association, and FIFA.
In support of our findings, Pollard et al46 found that a
season of soccer practice combined with neuromuscular injury REFERENCES
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