KNEE

A meta-analysis of the effect of neuromuscular trainingon the prevention of the anterior cruciate ligament injuryin female athletes

Jae Ho Yoo Æ Bee Oh Lim Æ Mina Ha Æ Soo Won Lee ÆSoo Jin Oh Æ Yong Seuk Lee Æ 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 counter-

parts, presumably because of anatomical, hormonal, and

neuromuscular differences. Of these three, only the neuro-

muscular component can be modified by preventive exer-

cise. 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 ran-

domized controlled trials or prospective cohort studies were

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 pre-

or in-season training, and the plyometrics and strengthening

components rather than balancing were significant. Meta-

analysis 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.

Keywords Anterior cruciate ligament � Female athlete �Neuromuscular training � Prevention program �Meta-analysis

Introduction

Anterior cruciate ligament (ACL) injuries in athletes are

common [1], and female athletes are 4–6 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 [1–3]. 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

J. H. Yoo

Department of Orthopaedic Surgery,

Soonchunhyang University Hospital,

Bucheon, South Korea

B. O. Lim

Sports Science Institute, Seoul National University,

Seoul, South Korea

M. Ha

Department of Preventive Medicine,

Dankook University College of Medicine,

Cheonan, South Korea

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

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

DOI 10.1007/s00167-009-0901-2

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

loss of participation in a sports during in-season, the long-

term rehabilitation required, and residual disability under-

score 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 modu-

lated. 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 ath-

letes are non-contact injuries that occur during sudden

deceleration, changes in direction such as cutting or side-

kicking, 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 [16–20], which alto-

gether place the ACL at an increased risk of injury.

Several different preventive programs have been attemp-

ted [3, 8, 21–25], 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 enhanc-

ing 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 conse-

quential role. They also encompass different level of com-

mitment, 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 effective-

ness 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 pre-

venting ACL injury, and that more effective training

protocols could be devised by identifying contributory

components by analyzing previously proposed protocols.

Materials and methods

An evaluation committee consisting of three orthopedic

surgeons and one biomechanical investigator, all of whom

had considerable experience in the care of the ACL injury

participated in the study. An extensive search of the liter-

ature was performed. As of June 2007, a computerized

Medline search was conducted using multiple Boolean

operators and combinations of the following eight key-

words: knee injury, ACL injury, gender difference, injury

prevention, neuromuscular training, plyometrics, strength-

ening training, and balance training (Table 1). The Coch-

rane 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 per-

formed 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 catego-

rized each one by marking A: included in the current study,

B: considered including after committee discussion;

favorable, C: decided after committee discussion; unfa-

vorable, D: excluded from the study, according to the

relevance of the study.

A total of 2,215 articles were identified form the key-

word search and 2,184 studies were excluded after

reviewing abstracts. A review of the remaining 31 inves-

tigations 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 prevention Injury avoidance

Neuromuscular training Neuromuscular coordination,

neuromuscular exercise

Plyometrics Plyometric exercise,

plyometric training

Strengthening training Strengthening exercise

Balance training Balance exercise,

equilibrium training

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

123

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 con-

ducted 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

individual studies analyzed by Mantel–Haenszel common

OR estimate. The DerSimonian and Laird’s 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 Edi-

tion]; 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 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-

season training, 0.35 [0.10, 1.21], or in-season 0.32 [0.17,Fig. 1 Schematic of the literature search procedure

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 14–18 Soccer, volleyball,

basketball

Pre-season Plyometric strengthening

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,

basketball

In-season Plyometric agility

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

123

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 bal-

ancing [0.63 [0.37, 1.09] vs. 0.27 [0.14, 0.49]] was not.

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

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 exer-

cise protocols were found to be more essential than bal-

ancing. 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, 30–32]. The

contact type of ACL injury is determined by the disposition

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 intervalsa ORs and 95% CIs estimated by the Mantel–Haenszel 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 Mantel–Haenszel’s fixed model and 0.49 and

0.27 to 1.02 in the DerSimonian and Laird’s random model, which

manifested the effectiveness of the preventive training by this meta-

analysis

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

123

of the knee and the nature of the external force at the time

of injury, which cannot be prevented by preventive exer-

cise [31]. Neuromuscular preventive programs target non-

contact ACL injuries [2, 31]. Five of the seven identified

studies in the current study compared non-contact ACL

injury [2, 3, 23–25], 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

Myklebust’s study [3]. The OR and 95% CI of the

remaining four studies [2, 23–25] 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 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

data were not analyzed by consistent manner in that the

Hewett’s 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 Hewett’s et al. [22] study, which

could not be interpreted by ITT basis. Therefore, we con-

ducted 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 Soderman’s

[8] and the Hewett’s [22] protocols. The balance board

training used for female soccer players in Soderman’s

prospective randomized study [8] was a home-based pro-

gram followed by and additional 10–15 min of standard

physical training, initially conducted daily for 30 days and

Fig. 3 Begg’s 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;

Begg’s test, P = 0.37 or odds ratio; SE standard error

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

Factors Subgroups Studies

[ref no.]

Untrained Trained OR

[95% CI]aTest for

heterogeneity

Publication bias

Uninjured Injured Uninjured Injured P value (df) Begg’s

P value

Egger’s

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

component

Plyometric (?) [3, 21–25] 6,363 122 3,882 30 0.37 [0.24, 0.55] 0.10 (5) 1.00 0.97

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 applicablea ORs and 95% CIs estimated by the Mantel–Haenszel pooled OR estimate

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

123

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] incorpo-

rated 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 per-

iod, whereas Pfeiffer et al. (20 min) [25], Peterson et al.

(10 min) [24], Mandelbaum et al. (20 min) [23], Mykle-

bust et al. (15 min) [3], Soderman et al. (10–15 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 Soderman’s 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 neuromuscular–biomechanical 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 pro-

gram [36]. In our subgroup analysis, the plyometric,

strengthening, and balancing components were found to be

the major three components of interest. Plyometric exer-

cises 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 bal-

ancing 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 exer-

cises has synergistic benefit by enhancing the dynamic

stability and decreasing injury risk [38–40]. Although the

optimal combination of neuromuscular—biomechanical

components remains to be verified, our study shows that

plyometric and strengthening components are probably

necessary factors of any training program.

The unique environment female athletes are placed in

should be taken into consideration, as should the cost-

effectiveness 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 pre-

ventive programs unless they enhance athletic perfor-

mance [36]. Therefore, the addition of exercise to

improve the overall athletic performance effect of a pre-

ventive training should have a positive effect on com-

pliance [36].

Meta-analysis study has intrinsic limitations. The pool-

ing 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, espe-

cially 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.

References

1. Arendt E, Dick R (1995) Knee injury patterns among men and

women in collegiate basketball and soccer. NCAA data and

review of literature. Am J Sports Med 23:694–701

2. Hewett TE, Ford KR, Myer GD (2006) Anterior cruciate ligament

injuries in female athletes: part 2, a meta-analysis of neuromus-

cular interventions aimed at injury prevention. Am J Sports Med

34:490–498

3. Myklebust G, Engebretsen L, Braekken IH, Skjolberg A, Olsen

OE, Bahr R (2003) Prevention of anterior cruciate ligament

injuries in female team handball players: a prospective inter-

vention study over three seasons. Clin J Sport Med 13:71–78

4. Myklebust G, Maehlum S, Engebretsen L, Strand T, Solheim E

(1997) Registration of cruciate ligament injuries in Norwegian

top level team handball. A prospective study covering two sea-

sons. Scand J Med Sci Sports 7:289–292

5. Toth AP, Cordasco FA (2001) Anterior cruciate ligament injuries

in the female athlete. J Gend Specif Med 4:25–34

6. Fleming BC (2003) Biomechanics of the anterior cruciate liga-

ment. J Orthop Sports Phys Ther 33:A13–A15

Knee Surg Sports Traumatol Arthrosc (2010) 18:824–830 829

123

7. Grindstaff TL, Hammill RR, Tuzson AE, Hertel J (2006) Neu-

romuscular control training programs and noncontact anterior

cruciate ligament injury rates in female athletes: a numbers-

needed-to-treat analysis. J Athl Train 41:450–456

8. Soderman K, Werner S, Pietila T, Engstrom B, Alfredson H

(2000) Balance board training: prevention of traumatic injuries of

the lower extremities in female soccer players? A prospective

randomized intervention study. Knee Surg Sports Traumatol

Arthrosc 8:356–363

9. Baratta R, Solomonow M, Zhou BH, Letson D, Chuinard R,

D’Ambrosia R (1988) Muscular coactivation. The role of the

antagonist musculature in maintaining knee stability. Am J Sports

Med 16:113–122

10. McNair PJ, Marshall RN, Matheson JA (1990) Important features

associated with acute anterior cruciate ligament injury. N Z Med

J 103:537–539

11. Draganich LF, Jaeger RJ, Kralj AR (1989) Coactivation of the

hamstrings and quadriceps during extension of the knee. J Bone

Joint Surg Am 71:1075–1081

12. Draganich LF, Vahey JW (1990) An in vitro study of anterior

cruciate ligament strain induced by quadriceps and hamstrings

forces. J Orthop Res 8:57–63

13. Kirkendall DT, Garrett WE Jr (2000) The anterior cruciate liga-

ment enigma. Injury mechanisms and prevention. Clin Orthop

Relat Res 372:64–68

14. Renstrom P, Arms SW, Stanwyck TS, Johnson RJ, Pope MH

(1986) Strain within the anterior cruciate ligament during ham-

string and quadriceps activity. Am J Sports Med 14:83–87

15. Simonsen EB, Magnusson SP, Bencke J, Naesborg H, Havkrog

M, Ebstrup JF, Sorensen H (2000) Can the hamstring muscles

protect the anterior cruciate ligament during a side-cutting

maneuver? Scand J Med Sci Sports 10:78–84

16. Ford KR, Myer GD, Hewett TE (2003) Valgus knee motion

during landing in high school female and male basketball players.

Med Sci Sports Exerc 35:1745–1750

17. Ford P, Hodges NJ, Huys R, Williams AM (2006) The role of

external action-effects in the execution of a soccer kick: a com-

parison across skill level. Motor Control 10:386–404

18. Kernozek TW, Torry MR, VANH H, Cowley H, Tanner S (2005)

Gender differences in frontal and sagittal plane biomechanics

during drop landings. Med Sci Sports Exerc 37:1003–1012

19. McLean SG, Huang X, Su A, Van Den Bogert AJ (2004) Sagittal

plane biomechanics cannot injure the ACL during sidestep cut-

ting. Clin Biomech (Bristol, Avon) 19:828–838

20. McLean SG, Lipfert SW, van den Bogert AJ (2004) Effect of

gender and defensive opponent on the biomechanics of sidestep

cutting. Med Sci Sports Exerc 36:1008–1016

21. Heidt RS Jr, Sweeterman LM, Carlonas RL, Traub JA, Tekulve

FX (2000) Avoidance of soccer injuries with preseason condi-

tioning. Am J Sports Med 28:659–662

22. Hewett TE, Lindenfeld TN, Riccobene JV, Noyes FR (1999) The

effect of neuromuscular training on the incidence of knee injury

in female athletes: a prospective study. Am J Sports Med 27:699–

706

23. Mandelbaum BR, Silvers HJ, Watanabe DS, Knarr JF, Thomas

SD, Griffin LY, Kirkendall DT, Garrett W Jr (2005) Effectiveness

of a neuromuscular and proprioceptive training program in pre-

venting anterior cruciate ligament injuries in female athletes:

2-year follow-up. Am J Sports Med 33:1003–1010

24. Petersen W, Braun C, Bock W, Schmidt K, Weimann A, Dre-

scher W, Eiling E, Stange R, Fuchs T, Hedderich J, Zantop T

(2005) A controlled prospective case control study of a preven-

tion training program in female team handball players: the Ger-

man experience. Arch Orthop Trauma Surg 125:614–621

25. Pfeiffer RP, Shea KG, Roberts D, Grandstrand S, Bond L (2006)

Lack of effect of a knee ligament injury prevention program

on the incidence of noncontact anterior cruciate ligament injury.

J Bone Joint Surg Am 88:1769–1774

26. Hewett TE, Myer GD, Ford KR (2006) Anterior cruciate ligament

injuries in female athletes: part 1, mechanisms and risk factors.

Am J Sports Med 34:299–311

27. Begg CB, Mazumdar M (1994) Operating characteristics of a rank

correlation test for publication bias. Biometrics 50:1088–1101

28. Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in

meta-analysis detected by a simple, graphical test. BMJ 315:629–

634

29. Macaskill P, Walter SD, Irwig L (2001) A comparison of meth-

ods to detect publication bias in meta-analysis. Stat Med 20:641–

654

30. Daniel DM, Stone ML, Dobson BE, Fithian DC, Rossman DJ,

Kaufman KR (1994) Fate of the ACL-injured patient. A pro-

spective outcome study. Am J Sports Med 22:632–644

31. Griffin LY, Agel J, Albohm MJ, Arendt EA, Dick RW, Garrett

WE, Garrick JG, Hewett TE, Huston L, Ireland ML, Johnson RJ,

Kibler WB, Lephart S, Lewis JL, Lindenfeld TN, Mandelbaum

BR, Marchak P, Teitz CC, Wojtys EM (2000) Noncontact ante-

rior cruciate ligament injuries: risk factors and prevention strat-

egies. J Am Acad Orthop Surg 8:141–150

32. Noyes FR, Mooar PA, Matthews DS, Butler DL (1983) The

symptomatic anterior cruciate-deficient knee. Part I: the long-

term functional disability in athletically active individuals.

J Bone Joint Surg Am 65:154–162

33. Lachin JM (2000) Statistical considerations in the intent-to-treat

principle. Control Clin Trials 21:167–189

34. Leandro G (2004) Meta-analysis in medical research. In: The

handbook for the understanding and practice of meta-analysis.

Blackwell, Oxford, pp 98

35. Hewett TE, Myer GD, Ford KR, Slauterbeck JR (2007) Dynamic

neuromuscular analysis training for preventing anterior cruciate

ligament injury in female athletes. Instr Course Lect 56:397–406

36. Myer GD, Ford KR, Hewett TE (2004) Methodological approa-

ches and rationale for training to prevent anterior cruciate liga-

ment injuries in female athletes. Scand J Med Sci Sports 14:275–

285

37. Caraffa A, Cerulli G, Projetti M, Aisa G, Rizzo A (1996) Pre-

vention of anterior cruciate ligament injuries in soccer. A pro-

spective controlled study of proprioceptive training. Knee Surg

Sports Traumatol Arthrosc 4:19–21

38. Heitkamp HC, Horstmann T, Mayer F, Weller J, Dickhuth HH

(2001) Gain in strength and muscular balance after balance

training. Int J Sports Med 22:285–290

39. Holm I, Fosdahl MA, Friis A, Risberg MA, Myklebust G, Steen

H (2004) Effect of neuromuscular training on proprioception,

balance, muscle strength, and lower limb function in female team

handball players. Clin J Sport Med 14:88–94

40. Paterno MV, Myer GD, Ford KR, Hewett TE (2004) Neuro-

muscular training improves single-limb stability in young female

athletes. J Orthop Sports Phys Ther 34:305–316

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

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