Knee Surg Sports Traumatol Arthrosc (2010) 18:824830

DOI 10.1007/s00167-009-0901-2

KNEE

A meta-analysis of the effect of neuromuscular training

on the prevention of the anterior cruciate ligament injury
in female athletes
Jae Ho Yoo Bee Oh Lim Mina Ha Soo Won Lee
Soo Jin Oh Yong Seuk Lee Jin Goo Kim

Received: 19 March 2009 / Accepted: 6 August 2009 / Published online: 4 September 2009
Springer-Verlag 2009

Abstract Female athletes are more prone to anterior

cruciate ligament (ACL) injury than their male counterparts, presumably because of anatomical, hormonal, and
neuromuscular differences. Of these three, only the neuromuscular component can be modified by preventive exercise. We aimed to evaluate the effect of a neuromuscular
protocol on the prevention of ACL injury by performing
meta-analysis, and to identify essential factors by subgroup
analysis. An extensive literature review was conducted to
identify relevant studies, and eventually, only seven randomized controlled trials or prospective cohort studies were
J. H. Yoo
Department of Orthopaedic Surgery,
Soonchunhyang University Hospital,
Bucheon, South Korea

included in the analysis. The odds ratios (OR) and the

confidence interval (CI) for the overall effects of training
and of potentially contributory factors were estimated. The
OR and the 95% CI for the overall effect of the preventive
training were 0.40 and [0.27, 0.60], respectively. Subgroup
analysis revealed that an age under 18, soccer rather than
handball, pre- and in-season training rather than either preor in-season training, and the plyometrics and strengthening
components rather than balancing were significant. Metaanalysis showed that pre- and in-season neuromuscular
training with an emphasis on plyometrics and strengthening
exercises was effective at preventing ACL injury in female
athletes, especially in those under 18 years of age. Further
study is required to develop a relevant training program
protocol of appropriate intensity.

B. O. Lim
Sports Science Institute, Seoul National University,
Seoul, South Korea

Keywords Anterior cruciate ligament
Female athlete

Neuromuscular training
Prevention program

Meta-analysis

M. Ha
Department of Preventive Medicine,
Dankook University College of Medicine,
Cheonan, South Korea

Introduction

S. W. Lee
Department of Orthopaedic Surgery, Sunlin Hospital,
Pohang, South Korea
S. J. Oh
J. G. Kim (&)
Orthopedic Department, Sports Medical Center,
Seoul Paik Hospital, Inje University,
2 Ka Jur Dong, Chung Gu, Seoul 100-032, Korea
e-mail: boram107@hanmail.net
Y. S. Lee
Department of Orthopedic Surgery,
Korea University Ansan Hospital,
Seoul, South Korea

123

Anterior cruciate ligament (ACL) injuries in athletes are

common [1], and female athletes are 46 times more prone
to these injuries than their male counterparts at similar
levels of exertion, despite the fact that the majority of ACL
injuries occur in males [13]. The reported incidence of
ACL injury is as high as 1.6 per 1,000 player-hours for elite
female players in team handball during matches [4], and
the overall annual incidence of ACL injury in women is
about 38,000 cases in the United States [5]. Regardless of
recent advances in the treatment of ACL, osteoarthritis of
the knee occurs ten times more in ACL-injured knees [6].
Therefore, prevention is a key component in reducing the

Knee Surg Sports Traumatol Arthrosc (2010) 18:824830

impact of ACL injury. Furthermore, the cost of treatment,

loss of participation in a sports during in-season, the longterm rehabilitation required, and residual disability underscore the importance of prevention of ACL injuries [2, 7,
8], and this is particularly true for female athletes.
Many theories have been proposed explain the female
susceptibility to ACL injury, which include anatomical,
hormonal, and neuromuscular hypothesis [2]. However, the
anatomical and hormonal components are useful in terms
of understanding the phenomenon, they cannot be modulated. The neuromuscular background that renders the
female athletes more susceptible to ACL injuries is a more
attractive topic for research, because it can be improved by
preventive training. The majority of ACL injuries in athletes are non-contact injuries that occur during sudden
deceleration, changes in direction such as cutting or sidekicking, or landing after a jump [9, 10]. Furthermore,
biomechanical studies have shown that females land from a
jump and change direction in a more erect posture than
males with knees and hips close to full extension [9, 11
14], which jeopardizes the balance of quadriceps and
hamstrings [9, 12, 15]. In addition, women tend to land
after a jump or side-kick with greater knee valgus and
reduced internal knee varus moment [1620], which altogether place the ACL at an increased risk of injury.
Several different preventive programs have been attempted [3, 8, 2125], and each of these is based on different
design concepts and emphasizes different components of
preventive exercise including plyometrics, strengthening,
balancing, endurance, and stability. However, the overall
effectiveness of preventive exercise with respect to enhancing neuromuscular control and preventing ACL injuries in
female athletes remains to be verified [26]. Furthermore, it
has not been determined which program is most effective, and
how a program should be scheduled, and it is not known
which biomechanical component of protocol plays a consequential role. They also encompass different level of commitment, which should be taken into due consideration for the
professional athletes lie in a unique situation [26].
The purpose of this study was to evaluate the effectiveness of ACL injury prevention programs for female athletes
using meta-analysis approach, and to identify the essential
components of the prevention programs. We hypothesized
that neuromuscular training program is effective at preventing ACL injury, and that more effective training
protocols could be devised by identifying contributory
components by analyzing previously proposed protocols.

825

had considerable experience in the care of the ACL injury

participated in the study. An extensive search of the literature was performed. As of June 2007, a computerized
Medline search was conducted using multiple Boolean
operators and combinations of the following eight keywords: knee injury, ACL injury, gender difference, injury
prevention, neuromuscular training, plyometrics, strengthening training, and balance training (Table 1). The Cochrane Database for Systemic Reviews was also searched to
identify any studies that may have been published in the
orthopedic, rehabilitation, or biomechanical literature. In
addition to the web-based search, three investigators performed a manual search of Journals published in English or
Korean. The proceedings of the American Academy of
Orthopaedic Surgeons and textbooks also were scrutinized
manually. Finally, contents experts interested in ACL
injury preventive neuromuscular training programs were
contacted for additional studies that may have been missed.
Identified articles were evaluated by grading level of
evidence, as follows: (1) randomized controlled trial, (2)
prospective cohort study, (3) retrospective case control
study, (4) case series, (5) case report or expert opinion.
Only randomized controlled trials and prospective cohort
studies were included. Each member of the evaluation
committee scrutinized the identified articles and categorized each one by marking A: included in the current study,
B: considered including after committee discussion;
favorable, C: decided after committee discussion; unfavorable, D: excluded from the study, according to the
relevance of the study.
A total of 2,215 articles were identified form the keyword search and 2,184 studies were excluded after
reviewing abstracts. A review of the remaining 31 investigations by evaluation committee ruled out 24 studies, and
left 7 eligible studies by Hewett et al. [26], Heidt et al. [21],
Soderman et al. [8], Myklebust et al. [3], Mandelbaum
Table 1 Search terms used in the systemic review
Subject

Search terms

Knee injury

Knee injury, knee trauma

ACL injury

ACL tear, ACL rupture,

cruciate ligament injury

Gender difference

Sex difference, between male

and female
Injury avoidance

Injury prevention
Neuromuscular training

Neuromuscular coordination,
neuromuscular exercise

Plyometrics

Plyometric exercise,
plyometric training

Materials and methods

An evaluation committee consisting of three orthopedic
surgeons and one biomechanical investigator, all of whom

Strengthening training

Strengthening exercise

Balance training

Balance exercise,
equilibrium training

123

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Knee Surg Sports Traumatol Arthrosc (2010) 18:824830

et al. [23], Peterson et al. [24], and Pfeiffer et al. [25]

(Fig. 1).
To assess the overall effects of preventive programs by
pooling the data, we documented numbers in the trained
and untrained groups and the incidences of ACL injury in
each group. To identify the significant components of the
preventive programs, the subgroup analyses were conducted on parameters included in more than one study.
Ages was divided by 18 years for devoted college athletic
competition was implemented from that age. The types of
sports included were soccer and handball. The training
times were classified as pre-season, in-season, and both the
pre- and in-seasons. The biomechanical components of the
preventive programs were plyometrics, strengthening, and
balancing exercises (Table 2).
A meta-analysis was performed on an intention-to-treat
basis. For each study, odds ratios (OR) and 95% confidence
intervals (CI) were calculated from the frequency tables of

Fig. 1 Schematic of the literature search procedure

individual studies analyzed by MantelHaenszel common

OR estimate. The DerSimonian and Lairds methods were
used as random-effects model to obtain summary ORs and
95% CIs. Heterogeneity between studies was tested using
the chi-square test. Publication bias was assessed using the
Egger regression asymmetry test and the Begg and
Mazumdar adjusted rank correlation test [27, 28]. The
Egger test makes more assumptions and is more sensitive
to many types of bias than the Begg and Mazumdar test
[29]. Subgroup analyses were performed in the same
manner using ORs and 95% CIs. All statistical analyses
were performed using STATA (version 9.2 [Special Edition]; Stata Corp., College Station, TX, USA).

Results
Five of the seven studies supported the efficacy of the
preventive programs, while the other two studies did not.
The meta-analysis conducted by pooling the seven eligible
studies showed that the incidence of ACL injury was 34 of
3,999 in trained group, and 123 of 6,462 in untrained group
with an OR of 0.40 and a 95% CI of [0.27, 0.60] in the
fixed model, which demonstrated the effectiveness of the
preventive training (Table 3; Fig. 2). No significant heterogeneity was found among studies (Table 3), and no significant publication bias was evident (Fig. 3).
The results of the subgroup analysis are outlined in
Table 4. The OR [95% CI] of subjects under the age of 18
was 0.27 [0.14, 0.49] and training among these subjects
proved to have a more favorable effect than on adults with
0.78 [0.230, 2.64]. Training had more effect on soccer, 0.32
[0.19, 0.56] than on handball, 0.54 [0.30, 0.97]. Pre- and inseason training 0.54 [0.30, 0.97] was effective, while preseason training, 0.35 [0.10, 1.21], or in-season 0.32 [0.17,

Table 2 Type of sports, subject age, and the number of ACL injuries in trained and untrained groups
Study

Year of
publication

Age (years)

Type of sport

Training time

Biomechanical component

Hewett et al. [22]

1999

1418

Soccer, volleyball,
basketball

Pre-season

Plyometric strengthening

Heidt et al. [21]

2000

1418

Soccer

Pre-season

Plyometric strengthening

Soderman et al. [8]

2000

20.4 4.6

Soccer

In-season

Balancing

Pre-season

Plyometric balancing

20.5 5.4
Myklebust et al. [3]

2003

1635

Handball

In-season
Mandelbaum et al. [23]

2005

1418

Soccer

In-season

Plyometric strengthening agility

Peterson et al. [24]

2005

Adult

Handball

Pre-season

Plyometric balancing

In-season
Pfeiffer et al. [25]

123

2006

1418(?)

Soccer, volleyball,
basketball

In-season

Plyometric agility

Knee Surg Sports Traumatol Arthrosc (2010) 18:824830

827

Table 3 The odds ratios and confidence intervals of the seven respective studies
Study

Untrained
Uninjured

OR [95% CI]a

Trained
Injured

Uninjured

Injured

Hewett et al. [22]

453

10

364

0.25 [0.05, 1.14]

Heidt et al. [21]

250

41

0.76 [0.09, 6.25]

99

117

3.38 [0.37, 30.78]

0.60 [0.33, 1.10]

Soderman et al. [8]

Myklebust et al. [3]
Mandelbaum et al. [23]
Peterson et al. [24]
Pfeiffer et al. [25]
Total

913

29

891

17

3,751

67

1,879

0.18 [0.08, 0.41]

137

133

0.21 [0.02, 1.79]

859
6,462

3
123

574
3,999

3
34

1.50 [0.30, 7.44]

MH pooled OR (fixed)

0.40 [0.27, 0.60]

D?L pooled OR (random)

0.49 [0.24, 1.02]

Fixed model: heterogeneity v2 = 12.55 (df = 6) P = 0.051, test of OR = 1: z = 4.52 P = 0.000

Random model: heterogeneity v2 = 12.55 (df = 6) P = 0.051, estimate of between-study variance Tau-squared = 0.4435, test of OR = 1:
z = 1.90 P = 0.057
MH MantelHaenszel, D?L DerSimonian & Lairds methods, OR odds ratio, CI confidence intervals
a

ORs and 95% CIs estimated by the MantelHaenszel pooled OR estimate

Fig. 2 Meta-analysis of the effect of neuromuscular training on the

prevention of the anterior cruciate ligament injury in female athletes.
The contribution of each study to the meta-analysis (it weight) is
represented by the area of a box whose center represents the size of
the effect estimated in that study. The incidence of ACL injury was 34
among 3,999 in the trained group, and 123 among 6,462 in the

untrained group with the ORs and 95% confidence intervals of 0.40
and 0.27 to 0.60 in the MantelHaenszels fixed model and 0.49 and
0.27 to 1.02 in the DerSimonian and Lairds random model, which
manifested the effectiveness of the preventive training by this metaanalysis

0.59] was not. The plyometric 0.37 [0.24, 0.55] and

strengthening components of training protocol [0.21 [0.11,
0.43] vs. 0.69 [0.41, 1.15]] were effective whereas balancing [0.63 [0.37, 1.09] vs. 0.27 [0.14, 0.49]] was not.

subjects under 18 years of age, and for soccer rather than

handball. The pre- and in-season training was found to be
more effective than either pre-season or in-season training
alone. Plyometric and strengthening components of exercise protocols were found to be more essential than balancing. All of the above findings could be incorporated into
the neuromuscular training protocols designed to prevent
ACL injuries of female athletes.
The mechanism of ACL injury can be divided into
contact and non-contact. The non-contact mechanism
constitutes to 70% of overall incidence [10, 3032]. The
contact type of ACL injury is determined by the disposition

Discussion
The most important finding of the present study was that
neuromuscular preventive programs were found to be
effective at preventing ACL injuries in female athletes. The
favorable effect of training was more pronounced in

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Knee Surg Sports Traumatol Arthrosc (2010) 18:824830

Fig. 3 Beggs funnel plot for publication bias in meta-analysis of the

effect of neuromuscular training on the prevention of the anterior
cruciate ligament injury in female athletes. Egger test, P = 0.64;
Beggs test, P = 0.37 or odds ratio; SE standard error

of the knee and the nature of the external force at the time
of injury, which cannot be prevented by preventive exercise [31]. Neuromuscular preventive programs target noncontact ACL injuries [2, 31]. Five of the seven identified
studies in the current study compared non-contact ACL
injury [2, 3, 2325], while the other two [8, 21] studies
provided no information on non-contact or contact type of
injury. Moreover, the number of injured ACLs after a
second intervention season was not documented in
Myklebusts study [3]. The OR and 95% CI of the
remaining four studies [2, 2325] which focused only on

non-contact ACL injury were 0.36 and [0.23, 0.54], which

is even more affirmative for preventive training.
Intention to treat (ITT) and the per-protocol (PP) based
analyses should be differentiated. ITT is based on the initial treatment intent, not on the treatment eventually
administered, and is founded on the assumption that
sometimes patients do not all receive optimal treatment.
Thus, ITT more appropriately represents the real-life situation. It provides information about the potential effects of
a treatment policy rather than on the potential effects of a
specific treatment [33]. PP, unlike ITT, concerns only
patients who completed the entire treatment protocol and is
useful when the object of interest is the actual efficacy of
treatment [34]. In the Hewett et al.s meta-analysis [2], the
data were not analyzed by consistent manner in that the
Hewetts et al.s [22] and the Soderman et al.s [8] study
were analyzed by PP basis, while the others by ITT basis.
In the present study, we applied the ITT method to every
study included except the Hewetts et al. [22] study, which
could not be interpreted by ITT basis. Therefore, we conducted the current study by more decent analysis with
consistent principle.
The intensity of each study protocol deserves attention
for it must be at a certain level to have a positive effect [2].
Program intensities were very different for the Sodermans
[8] and the Hewetts [22] protocols. The balance board
training used for female soccer players in Sodermans
prospective randomized study [8] was a home-based program followed by and additional 1015 min of standard
physical training, initially conducted daily for 30 days and

Table 4 Subgroup analyses of age, type of sports, training time, and biomechanical component
Factors

Subgroups

Studies
[ref no.]

Untrained

Trained

OR
[95% CI]a

Uninjured Injured Uninjured Injured

Age

B18

[2123, 25]

Adult

[24, 25]

Type of sports Soccer

Training time

5,313

88

2,858

12

0.27 [0.14, 0.49] 0.10 (3)

0.31

0.22

236

250

0.78 [0.23, 2.64] 0.08 (1)

[8, 2123, 25] 5,412

89

2,975

16

0.32 [0.19, 0.56] 0.03 (4)

0.09

0.07

Handball

[3, 24]

34

1,024

18

0.54 [0.30, 0.97] 0.35 (1)

Pre-season

[21, 22]

In-season
[8, 23, 25]
Pre- and in-season [3, 24]
Biomechanical Plyometric (?)
component
Plyometric (-)

[3, 2125]
[8]

Strengthening (?) [2123]

1,050
703

18

405

0.35 [0.10, 1.21] 0.40 (1)

4,709
1,050

71
34

2,570
1,024

13
18

0.32 [0.17, 0.59] 0.01 (2)

0.54 [0.30, 0.97] 0.35 (1)

0.30

0.09

6,363

122

3,882

30

99

117

1.00

0.97

4,454

85

2,284

0.21 [0.11, 0.43] 0.45 (2)

0.30

0.24

38

1,715

25

0.69 [0.41, 1.15] 0.23 (3)

0.73

0.62

Balancing (?)

[3, 8, 24]

1,149

35

1,141

22

0.63 [0.37, 1.09] 0.19 (2)

1.00

0.87

Balancing (-)

[2123, 25]

5,313

88

2,858

12

0.27 [0.14, 0.49] 0.10 (3)

0.31

0.22

ORs and 95% CIs estimated by the MantelHaenszel pooled OR estimate

123

0.37 [0.24, 0.55] 0.10 (5)

Strengthening (-) [3, 8, 24, 25] 2,008

OR odds ratio, CI confidence intervals, df degree of freedom, not applicable

a

Test for
Publication bias
heterogeneity
P value (df) Beggs Eggers
P value P value

Knee Surg Sports Traumatol Arthrosc (2010) 18:824830

then at 3 times per week for the remainder of the season.

The results showed no significant differences between
training and control groups [8]. The other protocols
required more concentrated participation and higher
degrees of exercise intensity. Hewett et al. [22] incorporated a comprehensive exercise of high intensity program.
Training session times in the reviewed studies varied from
10 to 75 min. Hewett et al. (75 min) [22] and Heidt et al.
(60 min) [21] implemented comprehensive protocols,
which are probably too difficult to execute in-season period, whereas Pfeiffer et al. (20 min) [25], Peterson et al.
(10 min) [24], Mandelbaum et al. (20 min) [23], Myklebust et al. (15 min) [3], Soderman et al. (1015 min) [8]
proposed a relatively short programs, which might be
integrated into a regular exercises in-season, causing less
burden for the athletes. Great care should be taken when
pooling the data during meta-analysis due to the different
intensities of intervention. The odds ratio and the 95% CI
from the six studies excluding Sodermans study were 0.37
and [0.24, 0.55], respectively, indicating that training
programs of high intensity had a more favorable effect on
ACL injury prevention.
The prevention of non-contact ACL injury should focus
on neuromuscularbiomechanical factors for they are the
only components modifiable by training [35]. Exercise
protocols should include warming-up, plyometrics,
strengthening, balancing, agility, flexibility, postural
adaptation, and an athletic performance enhancement program [36]. In our subgroup analysis, the plyometric,
strengthening, and balancing components were found to be
the major three components of interest. Plyometric exercises increase power, muscle strength, and speed [23, 36],
whereas strengthening exercises including walking lunge,
Russian hamstrings, single toe raise increase the muscle
power to stabilize the knee joint. The effect of the balancing exercises could be enhanced by proprioceptive
exercises [3, 37]. Neuromuscular exercise programs that
combine plyometric, strengthening, and balancing have
been shown to decrease the ACL injury risk and to enhance
the athletic performance [3, 22, 37]. Hewett et al. [22]
reported that the plyometric exercises have a positive effect
on the prevention of ACL injury and that the balancing
exercises alone without other biomechanical components
do not. On the other hand, Pfeiffer et al. [25] concluded
that plyometric training does not have a favorable effect on
the preventions of ACL injury. It has also been reported
that a combination of strengthening and balancing exercises has synergistic benefit by enhancing the dynamic
stability and decreasing injury risk [3840]. Although the
optimal combination of neuromuscularbiomechanical
components remains to be verified, our study shows that
plyometric and strengthening components are probably
necessary factors of any training program.

829

The unique environment female athletes are placed in

should be taken into consideration, as should the costeffectiveness and the effect of a training program on
performance and compliance [2, 3, 23, 36]. Impractical
protocols that are time-consuming and expensive cannot
be realistically implemented. As a matter of fact, athletes
are not normally well motivated to participate in preventive programs unless they enhance athletic performance [36]. Therefore, the addition of exercise to
improve the overall athletic performance effect of a preventive training should have a positive effect on compliance [36].
Meta-analysis study has intrinsic limitations. The pooling the mixed design studies can make interpretations
difficult and sometimes leads to false results. Furthermore,
the heterogeneous nature of treatment protocols is another
concern [2], such as the aforementioned various intensities
of the exercise programs. Nevertheless, in the present
study, the positive effect of preventive exercise was always
evident. The rarity of the ACL injury incidence poses
another problem in study design in terms of the statistical
power of conclusion drawn from the findings of individual
preventive training programs.

Conclusion
This meta-analysis shows that ACL injury preventive
exercise programs are effective in female athletes, especially in those under 18 years of age, and for soccer players
rather than handball players. Plyometric and strengthening
exercises were found to be essential components of such
training protocols, whereas balancing exercises were not.

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