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Knee Surg Sports Traumatol Arthrosc (2010) 18:824–830

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 Æ Bee Oh Lim Æ Mina Ha Æ Soo Won Lee Æ
Soo Jin Oh Æ Yong Seuk Lee Æ Jin Goo Kim

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

Abstract Female athletes are more prone to anterior included in the analysis. The odds ratios (OR) and the
cruciate ligament (ACL) injury than their male counter- confidence interval (CI) for the overall effects of training
parts, presumably because of anatomical, hormonal, and and of potentially contributory factors were estimated. The
neuromuscular differences. Of these three, only the neuro- OR and the 95% CI for the overall effect of the preventive
muscular component can be modified by preventive exer- training were 0.40 and [0.27, 0.60], respectively. Subgroup
cise. We aimed to evaluate the effect of a neuromuscular analysis revealed that an age under 18, soccer rather than
protocol on the prevention of ACL injury by performing handball, pre- and in-season training rather than either pre-
meta-analysis, and to identify essential factors by subgroup or in-season training, and the plyometrics and strengthening
analysis. An extensive literature review was conducted to components rather than balancing were significant. Meta-
identify relevant studies, and eventually, only seven ran- analysis showed that pre- and in-season neuromuscular
domized controlled trials or prospective cohort studies were 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
J. H. Yoo
Department of Orthopaedic Surgery, study is required to develop a relevant training program
Soonchunhyang University Hospital, protocol of appropriate intensity.
Bucheon, South Korea
Keywords Anterior cruciate ligament  Female athlete 
B. O. Lim
Sports Science Institute, Seoul National University, Neuromuscular training  Prevention program 
Seoul, South Korea Meta-analysis

M. Ha
Department of Preventive Medicine,
Dankook University College of Medicine, Introduction
Cheonan, South Korea
Anterior cruciate ligament (ACL) injuries in athletes are
S. W. Lee
common [1], and female athletes are 4–6 times more prone
Department of Orthopaedic Surgery, Sunlin Hospital,
Pohang, South Korea to these injuries than their male counterparts at similar
levels of exertion, despite the fact that the majority of ACL
S. J. Oh  J. G. Kim (&) injuries occur in males [1–3]. The reported incidence of
Orthopedic Department, Sports Medical Center,
ACL injury is as high as 1.6 per 1,000 player-hours for elite
Seoul Paik Hospital, Inje University,
2 Ka Jur Dong, Chung Gu, Seoul 100-032, Korea female players in team handball during matches [4], and
e-mail: boram107@hanmail.net the overall annual incidence of ACL injury in women is
about 38,000 cases in the United States [5]. Regardless of
Y. S. Lee
recent advances in the treatment of ACL, osteoarthritis of
Department of Orthopedic Surgery,
Korea University Ansan Hospital, the knee occurs ten times more in ACL-injured knees [6].
Seoul, South Korea Therefore, prevention is a key component in reducing the

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Knee Surg Sports Traumatol Arthrosc (2010) 18:824–830 825

impact of ACL injury. Furthermore, the cost of treatment, had considerable experience in the care of the ACL injury
loss of participation in a sports during in-season, the long- participated in the study. An extensive search of the liter-
term rehabilitation required, and residual disability under- ature was performed. As of June 2007, a computerized
score the importance of prevention of ACL injuries [2, 7, Medline search was conducted using multiple Boolean
8], and this is particularly true for female athletes. operators and combinations of the following eight key-
Many theories have been proposed explain the female words: knee injury, ACL injury, gender difference, injury
susceptibility to ACL injury, which include anatomical, prevention, neuromuscular training, plyometrics, strength-
hormonal, and neuromuscular hypothesis [2]. However, the ening training, and balance training (Table 1). The Coch-
anatomical and hormonal components are useful in terms rane Database for Systemic Reviews was also searched to
of understanding the phenomenon, they cannot be modu- identify any studies that may have been published in the
lated. The neuromuscular background that renders the orthopedic, rehabilitation, or biomechanical literature. In
female athletes more susceptible to ACL injuries is a more addition to the web-based search, three investigators per-
attractive topic for research, because it can be improved by formed a manual search of Journals published in English or
preventive training. The majority of ACL injuries in ath- Korean. The proceedings of the American Academy of
letes are non-contact injuries that occur during sudden Orthopaedic Surgeons and textbooks also were scrutinized
deceleration, changes in direction such as cutting or side- manually. Finally, contents experts interested in ACL
kicking, or landing after a jump [9, 10]. Furthermore, injury preventive neuromuscular training programs were
biomechanical studies have shown that females land from a contacted for additional studies that may have been missed.
jump and change direction in a more erect posture than Identified articles were evaluated by grading level of
males with knees and hips close to full extension [9, 11– evidence, as follows: (1) randomized controlled trial, (2)
14], which jeopardizes the balance of quadriceps and prospective cohort study, (3) retrospective case control
hamstrings [9, 12, 15]. In addition, women tend to land study, (4) case series, (5) case report or expert opinion.
after a jump or side-kick with greater knee valgus and Only randomized controlled trials and prospective cohort
reduced internal knee varus moment [16–20], which alto- studies were included. Each member of the evaluation
gether place the ACL at an increased risk of injury. committee scrutinized the identified articles and catego-
Several different preventive programs have been attemp- rized each one by marking A: included in the current study,
ted [3, 8, 21–25], and each of these is based on different B: considered including after committee discussion;
design concepts and emphasizes different components of favorable, C: decided after committee discussion; unfa-
preventive exercise including plyometrics, strengthening, vorable, D: excluded from the study, according to the
balancing, endurance, and stability. However, the overall relevance of the study.
effectiveness of preventive exercise with respect to enhanc- A total of 2,215 articles were identified form the key-
ing neuromuscular control and preventing ACL injuries in word search and 2,184 studies were excluded after
female athletes remains to be verified [26]. Furthermore, it reviewing abstracts. A review of the remaining 31 inves-
has not been determined which program is most effective, and tigations by evaluation committee ruled out 24 studies, and
how a program should be scheduled, and it is not known left 7 eligible studies by Hewett et al. [26], Heidt et al. [21],
which biomechanical component of protocol plays a conse- Soderman et al. [8], Myklebust et al. [3], Mandelbaum
quential role. They also encompass different level of com-
mitment, which should be taken into due consideration for the
Table 1 Search terms used in the systemic review
professional athletes lie in a unique situation [26].
The purpose of this study was to evaluate the effective- Subject Search terms
ness of ACL injury prevention programs for female athletes Knee injury Knee injury, knee trauma
using meta-analysis approach, and to identify the essential ACL injury ACL tear, ACL rupture,
components of the prevention programs. We hypothesized cruciate ligament injury
that neuromuscular training program is effective at pre- Gender difference Sex difference, between male
venting ACL injury, and that more effective training and female
protocols could be devised by identifying contributory Injury prevention Injury avoidance
components by analyzing previously proposed protocols. Neuromuscular training Neuromuscular coordination,
neuromuscular exercise
Plyometrics Plyometric exercise,
plyometric training
Materials and methods
Strengthening training Strengthening exercise
Balance training Balance exercise,
An evaluation committee consisting of three orthopedic
equilibrium training
surgeons and one biomechanical investigator, all of whom

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et al. [23], Peterson et al. [24], and Pfeiffer et al. [25] individual studies analyzed by Mantel–Haenszel common
(Fig. 1). OR estimate. The DerSimonian and Laird’s methods were
To assess the overall effects of preventive programs by used as random-effects model to obtain summary ORs and
pooling the data, we documented numbers in the trained 95% CIs. Heterogeneity between studies was tested using
and untrained groups and the incidences of ACL injury in the chi-square test. Publication bias was assessed using the
each group. To identify the significant components of the Egger regression asymmetry test and the Begg and
preventive programs, the subgroup analyses were con- Mazumdar adjusted rank correlation test [27, 28]. The
ducted on parameters included in more than one study. Egger test makes more assumptions and is more sensitive
Ages was divided by 18 years for devoted college athletic to many types of bias than the Begg and Mazumdar test
competition was implemented from that age. The types of [29]. Subgroup analyses were performed in the same
sports included were soccer and handball. The training manner using ORs and 95% CIs. All statistical analyses
times were classified as pre-season, in-season, and both the were performed using STATA (version 9.2 [Special Edi-
pre- and in-seasons. The biomechanical components of the tion]; Stata Corp., College Station, TX, USA).
preventive programs were plyometrics, strengthening, and
balancing exercises (Table 2).
A meta-analysis was performed on an intention-to-treat Results
basis. For each study, odds ratios (OR) and 95% confidence
intervals (CI) were calculated from the frequency tables of 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 heter-
ogeneity was found among studies (Table 3), and no sig-
nificant 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 in-
season training 0.54 [0.30, 0.97] was effective, while pre-
Fig. 1 Schematic of the literature search procedure season 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 Age (years) Type of sport Training time Biomechanical component
publication

Hewett et al. [22] 1999 14–18 Soccer, volleyball, Pre-season Plyometric strengthening
basketball
Heidt et al. [21] 2000 14–18 Soccer Pre-season Plyometric strengthening
Soderman et al. [8] 2000 20.4 ± 4.6 Soccer In-season Balancing
20.5 ± 5.4
Myklebust et al. [3] 2003 16–35 Handball Pre-season Plyometric balancing
In-season
Mandelbaum et al. [23] 2005 14–18 Soccer In-season Plyometric strengthening agility
Peterson et al. [24] 2005 Adult Handball Pre-season Plyometric balancing
In-season
Pfeiffer et al. [25] 2006 14–18(?) Soccer, volleyball, In-season Plyometric agility
basketball

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Knee Surg Sports Traumatol Arthrosc (2010) 18:824–830 827

Table 3 The odds ratios and confidence intervals of the seven respective studies
Study Untrained Trained OR [95% CI]a
Uninjured Injured Uninjured Injured

Hewett et al. [22] 453 10 364 2 0.25 [0.05, 1.14]


Heidt et al. [21] 250 8 41 1 0.76 [0.09, 6.25]
Soderman et al. [8] 99 1 117 4 3.38 [0.37, 30.78]
Myklebust et al. [3] 913 29 891 17 0.60 [0.33, 1.10]
Mandelbaum et al. [23] 3,751 67 1,879 6 0.18 [0.08, 0.41]
Peterson et al. [24] 137 5 133 1 0.21 [0.02, 1.79]
Pfeiffer et al. [25] 859 3 574 3 1.50 [0.30, 7.44]
Total 6,462 123 3,999 34
M–H 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
M–H Mantel–Haenszel, D?L DerSimonian & Laird’s methods, OR odds ratio, CI confidence intervals
a
ORs and 95% CIs estimated by the Mantel–Haenszel pooled OR estimate

Fig. 2 Meta-analysis of the effect of neuromuscular training on the untrained group with the ORs and 95% confidence intervals of 0.40
prevention of the anterior cruciate ligament injury in female athletes. and 0.27 to 0.60 in the Mantel–Haenszel’s fixed model and 0.49 and
The contribution of each study to the meta-analysis (it weight) is 0.27 to 1.02 in the DerSimonian and Laird’s random model, which
represented by the area of a box whose center represents the size of manifested the effectiveness of the preventive training by this meta-
the effect estimated in that study. The incidence of ACL injury was 34 analysis
among 3,999 in the trained group, and 123 among 6,462 in the

0.59] was not. The plyometric 0.37 [0.24, 0.55] and subjects under 18 years of age, and for soccer rather than
strengthening components of training protocol [0.21 [0.11, handball. The pre- and in-season training was found to be
0.43] vs. 0.69 [0.41, 1.15]] were effective whereas bal- more effective than either pre-season or in-season training
ancing [0.63 [0.37, 1.09] vs. 0.27 [0.14, 0.49]] was not. alone. Plyometric and strengthening components of exer-
cise protocols were found to be more essential than bal-
ancing. All of the above findings could be incorporated into
Discussion the neuromuscular training protocols designed to prevent
ACL injuries of female athletes.
The most important finding of the present study was that The mechanism of ACL injury can be divided into
neuromuscular preventive programs were found to be contact and non-contact. The non-contact mechanism
effective at preventing ACL injuries in female athletes. The constitutes to 70% of overall incidence [10, 30–32]. The
favorable effect of training was more pronounced in contact type of ACL injury is determined by the disposition

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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 ini-
tial 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 situ-
ation. 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
Fig. 3 Begg’s funnel plot for publication bias in meta-analysis of the
effect of neuromuscular training on the prevention of the anterior
data were not analyzed by consistent manner in that the
cruciate ligament injury in female athletes. Egger test, P = 0.64; Hewett’s et al.’s [22] and the Soderman et al.’s [8] study
Begg’s test, P = 0.37 or odds ratio; SE standard error 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 Hewett’s et al. [22] study, which
of the knee and the nature of the external force at the time could not be interpreted by ITT basis. Therefore, we con-
of injury, which cannot be prevented by preventive exer- ducted the current study by more decent analysis with
cise [31]. Neuromuscular preventive programs target non- consistent principle.
contact ACL injuries [2, 31]. Five of the seven identified The intensity of each study protocol deserves attention
studies in the current study compared non-contact ACL for it must be at a certain level to have a positive effect [2].
injury [2, 3, 23–25], while the other two [8, 21] studies Program intensities were very different for the Soderman’s
provided no information on non-contact or contact type of [8] and the Hewett’s [22] protocols. The balance board
injury. Moreover, the number of injured ACLs after a training used for female soccer players in Soderman’s
second intervention season was not documented in prospective randomized study [8] was a home-based pro-
Myklebust’s study [3]. The OR and 95% CI of the gram followed by and additional 10–15 min of standard
remaining four studies [2, 23–25] which focused only on 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 Untrained Trained OR Test for Publication bias
[ref no.] [95% CI]a heterogeneity
Uninjured Injured Uninjured Injured P value (df) Begg’s Egger’s
P value P value

Age B18 [21–23, 25] 5,313 88 2,858 12 0.27 [0.14, 0.49] 0.10 (3) 0.31 0.22
Adult [24, 25] 236 6 250 5 0.78 [0.23, 2.64] 0.08 (1) – –
Type of sports Soccer [8, 21–23, 25] 5,412 89 2,975 16 0.32 [0.19, 0.56] 0.03 (4) 0.09 0.07
Handball [3, 24] 1,050 34 1,024 18 0.54 [0.30, 0.97] 0.35 (1) – –
Training time Pre-season [21, 22] 703 18 405 3 0.35 [0.10, 1.21] 0.40 (1) – –
In-season [8, 23, 25] 4,709 71 2,570 13 0.32 [0.17, 0.59] 0.01 (2) 0.30 0.09
Pre- and in-season [3, 24] 1,050 34 1,024 18 0.54 [0.30, 0.97] 0.35 (1) – –
Biomechanical Plyometric (?) [3, 21–25] 6,363 122 3,882 30 0.37 [0.24, 0.55] 0.10 (5) 1.00 0.97
component Plyometric (-) [8] 99 1 117 4 – – – –
Strengthening (?) [21–23] 4,454 85 2,284 9 0.21 [0.11, 0.43] 0.45 (2) 0.30 0.24
Strengthening (-) [3, 8, 24, 25] 2,008 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 (-) [21–23, 25] 5,313 88 2,858 12 0.27 [0.14, 0.49] 0.10 (3) 0.31 0.22
OR odds ratio, CI confidence intervals, df degree of freedom, – not applicable
a
ORs and 95% CIs estimated by the Mantel–Haenszel pooled OR estimate

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then at 3 times per week for the remainder of the season. The unique environment female athletes are placed in
The results showed no significant differences between should be taken into consideration, as should the cost-
training and control groups [8]. The other protocols effectiveness and the effect of a training program on
required more concentrated participation and higher performance and compliance [2, 3, 23, 36]. Impractical
degrees of exercise intensity. Hewett et al. [22] incorpo- protocols that are time-consuming and expensive cannot
rated a comprehensive exercise of high intensity program. be realistically implemented. As a matter of fact, athletes
Training session times in the reviewed studies varied from are not normally well motivated to participate in pre-
10 to 75 min. Hewett et al. (75 min) [22] and Heidt et al. ventive programs unless they enhance athletic perfor-
(60 min) [21] implemented comprehensive protocols, mance [36]. Therefore, the addition of exercise to
which are probably too difficult to execute in-season per- improve the overall athletic performance effect of a pre-
iod, whereas Pfeiffer et al. (20 min) [25], Peterson et al. ventive training should have a positive effect on com-
(10 min) [24], Mandelbaum et al. (20 min) [23], Mykle- pliance [36].
bust et al. (15 min) [3], Soderman et al. (10–15 min) [8] Meta-analysis study has intrinsic limitations. The pool-
proposed a relatively short programs, which might be ing the mixed design studies can make interpretations
integrated into a regular exercises in-season, causing less difficult and sometimes leads to false results. Furthermore,
burden for the athletes. Great care should be taken when the heterogeneous nature of treatment protocols is another
pooling the data during meta-analysis due to the different concern [2], such as the aforementioned various intensities
intensities of intervention. The odds ratio and the 95% CI of the exercise programs. Nevertheless, in the present
from the six studies excluding Soderman’s study were 0.37 study, the positive effect of preventive exercise was always
and [0.24, 0.55], respectively, indicating that training evident. The rarity of the ACL injury incidence poses
programs of high intensity had a more favorable effect on another problem in study design in terms of the statistical
ACL injury prevention. power of conclusion drawn from the findings of individual
The prevention of non-contact ACL injury should focus preventive training programs.
on neuromuscular–biomechanical factors for they are the
only components modifiable by training [35]. Exercise
protocols should include warming-up, plyometrics, Conclusion
strengthening, balancing, agility, flexibility, postural
adaptation, and an athletic performance enhancement pro- This meta-analysis shows that ACL injury preventive
gram [36]. In our subgroup analysis, the plyometric, exercise programs are effective in female athletes, espe-
strengthening, and balancing components were found to be cially in those under 18 years of age, and for soccer players
the major three components of interest. Plyometric exer- rather than handball players. Plyometric and strengthening
cises increase power, muscle strength, and speed [23, 36], exercises were found to be essential components of such
whereas strengthening exercises including walking lunge, training protocols, whereas balancing exercises were not.
Russian hamstrings, single toe raise increase the muscle
power to stabilize the knee joint. The effect of the bal-
ancing exercises could be enhanced by proprioceptive
exercises [3, 37]. Neuromuscular exercise programs that References
combine plyometric, strengthening, and balancing have
1. Arendt E, Dick R (1995) Knee injury patterns among men and
been shown to decrease the ACL injury risk and to enhance women in collegiate basketball and soccer. NCAA data and
the athletic performance [3, 22, 37]. Hewett et al. [22] review of literature. Am J Sports Med 23:694–701
reported that the plyometric exercises have a positive effect 2. Hewett TE, Ford KR, Myer GD (2006) Anterior cruciate ligament
on the prevention of ACL injury and that the balancing injuries in female athletes: part 2, a meta-analysis of neuromus-
cular interventions aimed at injury prevention. Am J Sports Med
exercises alone without other biomechanical components 34:490–498
do not. On the other hand, Pfeiffer et al. [25] concluded 3. Myklebust G, Engebretsen L, Braekken IH, Skjolberg A, Olsen
that plyometric training does not have a favorable effect on OE, Bahr R (2003) Prevention of anterior cruciate ligament
the preventions of ACL injury. It has also been reported injuries in female team handball players: a prospective inter-
vention study over three seasons. Clin J Sport Med 13:71–78
that a combination of strengthening and balancing exer- 4. Myklebust G, Maehlum S, Engebretsen L, Strand T, Solheim E
cises has synergistic benefit by enhancing the dynamic (1997) Registration of cruciate ligament injuries in Norwegian
stability and decreasing injury risk [38–40]. Although the top level team handball. A prospective study covering two sea-
optimal combination of neuromuscular—biomechanical sons. Scand J Med Sci Sports 7:289–292
5. Toth AP, Cordasco FA (2001) Anterior cruciate ligament injuries
components remains to be verified, our study shows that in the female athlete. J Gend Specif Med 4:25–34
plyometric and strengthening components are probably 6. Fleming BC (2003) Biomechanics of the anterior cruciate liga-
necessary factors of any training program. ment. J Orthop Sports Phys Ther 33:A13–A15

123
830 Knee Surg Sports Traumatol Arthrosc (2010) 18:824–830

7. Grindstaff TL, Hammill RR, Tuzson AE, Hertel J (2006) Neu- 24. Petersen W, Braun C, Bock W, Schmidt K, Weimann A, Dre-
romuscular control training programs and noncontact anterior scher W, Eiling E, Stange R, Fuchs T, Hedderich J, Zantop T
cruciate ligament injury rates in female athletes: a numbers- (2005) A controlled prospective case control study of a preven-
needed-to-treat analysis. J Athl Train 41:450–456 tion training program in female team handball players: the Ger-
8. Soderman K, Werner S, Pietila T, Engstrom B, Alfredson H man experience. Arch Orthop Trauma Surg 125:614–621
(2000) Balance board training: prevention of traumatic injuries of 25. Pfeiffer RP, Shea KG, Roberts D, Grandstrand S, Bond L (2006)
the lower extremities in female soccer players? A prospective Lack of effect of a knee ligament injury prevention program
randomized intervention study. Knee Surg Sports Traumatol on the incidence of noncontact anterior cruciate ligament injury.
Arthrosc 8:356–363 J Bone Joint Surg Am 88:1769–1774
9. Baratta R, Solomonow M, Zhou BH, Letson D, Chuinard R, 26. Hewett TE, Myer GD, Ford KR (2006) Anterior cruciate ligament
D’Ambrosia R (1988) Muscular coactivation. The role of the injuries in female athletes: part 1, mechanisms and risk factors.
antagonist musculature in maintaining knee stability. Am J Sports Am J Sports Med 34:299–311
Med 16:113–122 27. Begg CB, Mazumdar M (1994) Operating characteristics of a rank
10. McNair PJ, Marshall RN, Matheson JA (1990) Important features correlation test for publication bias. Biometrics 50:1088–1101
associated with acute anterior cruciate ligament injury. N Z Med 28. Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in
J 103:537–539 meta-analysis detected by a simple, graphical test. BMJ 315:629–
11. Draganich LF, Jaeger RJ, Kralj AR (1989) Coactivation of the 634
hamstrings and quadriceps during extension of the knee. J Bone 29. Macaskill P, Walter SD, Irwig L (2001) A comparison of meth-
Joint Surg Am 71:1075–1081 ods to detect publication bias in meta-analysis. Stat Med 20:641–
12. Draganich LF, Vahey JW (1990) An in vitro study of anterior 654
cruciate ligament strain induced by quadriceps and hamstrings 30. Daniel DM, Stone ML, Dobson BE, Fithian DC, Rossman DJ,
forces. J Orthop Res 8:57–63 Kaufman KR (1994) Fate of the ACL-injured patient. A pro-
13. Kirkendall DT, Garrett WE Jr (2000) The anterior cruciate liga- spective outcome study. Am J Sports Med 22:632–644
ment enigma. Injury mechanisms and prevention. Clin Orthop 31. Griffin LY, Agel J, Albohm MJ, Arendt EA, Dick RW, Garrett
Relat Res 372:64–68 WE, Garrick JG, Hewett TE, Huston L, Ireland ML, Johnson RJ,
14. Renstrom P, Arms SW, Stanwyck TS, Johnson RJ, Pope MH Kibler WB, Lephart S, Lewis JL, Lindenfeld TN, Mandelbaum
(1986) Strain within the anterior cruciate ligament during ham- BR, Marchak P, Teitz CC, Wojtys EM (2000) Noncontact ante-
string and quadriceps activity. Am J Sports Med 14:83–87 rior cruciate ligament injuries: risk factors and prevention strat-
15. Simonsen EB, Magnusson SP, Bencke J, Naesborg H, Havkrog egies. J Am Acad Orthop Surg 8:141–150
M, Ebstrup JF, Sorensen H (2000) Can the hamstring muscles 32. Noyes FR, Mooar PA, Matthews DS, Butler DL (1983) The
protect the anterior cruciate ligament during a side-cutting symptomatic anterior cruciate-deficient knee. Part I: the long-
maneuver? Scand J Med Sci Sports 10:78–84 term functional disability in athletically active individuals.
16. Ford KR, Myer GD, Hewett TE (2003) Valgus knee motion J Bone Joint Surg Am 65:154–162
during landing in high school female and male basketball players. 33. Lachin JM (2000) Statistical considerations in the intent-to-treat
Med Sci Sports Exerc 35:1745–1750 principle. Control Clin Trials 21:167–189
17. Ford P, Hodges NJ, Huys R, Williams AM (2006) The role of 34. Leandro G (2004) Meta-analysis in medical research. In: The
external action-effects in the execution of a soccer kick: a com- handbook for the understanding and practice of meta-analysis.
parison across skill level. Motor Control 10:386–404 Blackwell, Oxford, pp 98
18. Kernozek TW, Torry MR, VANH H, Cowley H, Tanner S (2005) 35. Hewett TE, Myer GD, Ford KR, Slauterbeck JR (2007) Dynamic
Gender differences in frontal and sagittal plane biomechanics neuromuscular analysis training for preventing anterior cruciate
during drop landings. Med Sci Sports Exerc 37:1003–1012 ligament injury in female athletes. Instr Course Lect 56:397–406
19. McLean SG, Huang X, Su A, Van Den Bogert AJ (2004) Sagittal 36. Myer GD, Ford KR, Hewett TE (2004) Methodological approa-
plane biomechanics cannot injure the ACL during sidestep cut- ches and rationale for training to prevent anterior cruciate liga-
ting. Clin Biomech (Bristol, Avon) 19:828–838 ment injuries in female athletes. Scand J Med Sci Sports 14:275–
20. McLean SG, Lipfert SW, van den Bogert AJ (2004) Effect of 285
gender and defensive opponent on the biomechanics of sidestep 37. Caraffa A, Cerulli G, Projetti M, Aisa G, Rizzo A (1996) Pre-
cutting. Med Sci Sports Exerc 36:1008–1016 vention of anterior cruciate ligament injuries in soccer. A pro-
21. Heidt RS Jr, Sweeterman LM, Carlonas RL, Traub JA, Tekulve spective controlled study of proprioceptive training. Knee Surg
FX (2000) Avoidance of soccer injuries with preseason condi- Sports Traumatol Arthrosc 4:19–21
tioning. Am J Sports Med 28:659–662 38. Heitkamp HC, Horstmann T, Mayer F, Weller J, Dickhuth HH
22. Hewett TE, Lindenfeld TN, Riccobene JV, Noyes FR (1999) The (2001) Gain in strength and muscular balance after balance
effect of neuromuscular training on the incidence of knee injury training. Int J Sports Med 22:285–290
in female athletes: a prospective study. Am J Sports Med 27:699– 39. Holm I, Fosdahl MA, Friis A, Risberg MA, Myklebust G, Steen
706 H (2004) Effect of neuromuscular training on proprioception,
23. Mandelbaum BR, Silvers HJ, Watanabe DS, Knarr JF, Thomas balance, muscle strength, and lower limb function in female team
SD, Griffin LY, Kirkendall DT, Garrett W Jr (2005) Effectiveness handball players. Clin J Sport Med 14:88–94
of a neuromuscular and proprioceptive training program in pre- 40. Paterno MV, Myer GD, Ford KR, Hewett TE (2004) Neuro-
venting anterior cruciate ligament injuries in female athletes: muscular training improves single-limb stability in young female
2-year follow-up. Am J Sports Med 33:1003–1010 athletes. J Orthop Sports Phys Ther 34:305–316

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