The effect of hamstring flexibility on peak hamstring muscle strain in sprinting

2017-09-21 11:54XinglinWnFengQuWillimGrrettHuiLiuBingYu
Journal of Sport and Health Science 2017年3期

Xinglin Wn,Feng Qu,Willim E.Grrett,Hui Liu,*,Bing Yu*

aBiomechanics Laboratory,Beijing Sport University,Beijing 100084,China

bDuke Sports Medicine,Department of Orthopaedic Surgery,Duke University Medical Center,Durham,NC 27710,USA

cCenter for Human Movement Science,The University of North Carolina at Chapel Hill,Chapel Hill,NC 27599,USA

The effect of hamstring flexibility on peak hamstring muscle strain in sprinting

Xianglin Wana,Feng Qua,William E.Garrettb,Hui Liua,*,Bing Yuc,*

aBiomechanics Laboratory,Beijing Sport University,Beijing 100084,China

bDuke Sports Medicine,Department of Orthopaedic Surgery,Duke University Medical Center,Durham,NC 27710,USA

cCenter for Human Movement Science,The University of North Carolina at Chapel Hill,Chapel Hill,NC 27599,USA

Background:The effect of hamstring flexibility on the peak hamstring muscle strains in sprinting,until now,remained unknown,which limited our understanding of risk factors of hamstring muscle strain injury(hamstring injury).As a continuation of our previous study,this study was aimed to examine the relationship between hamstring flexibility and peak hamstring muscle strains in sprinting.

Methods:Ten male and 10 female college students participated in this study.Hamstring flexibility,isokinetic strength data,three-dimensional(3D) kinematic data in a hamstring isokinetic test,and kinematic data in a sprinting test were collected for each participant.The optimal hamstring muscle lengths and peak hamstring muscle strains in sprinting were determined for each participant.

Results:The muscle strain of each of the 3 biarticulated hamstring muscles reached a peak during the late swing phase.Peak hamstring muscle strains were negatively correlated to hamstring flexibility(0.1179≤R2≤0.4519,p=0.001)but not to hip and knee joint positions at the time of peak hamstring muscle strains.Peak hamstring muscle strains were not different for different genders.Peak muscle strains of biceps long head (0.071±0.059)and semitendinosus(0.070±0.055)were signi ficantly greater than that of semimembranosus(0.064±0.054).

Conclusion:A potential for hamstring injury exists during the late swing phase of sprinting.Peak hamstring muscle strains in sprinting are negatively correlated to hamstring flexibility across individuals.The magnitude of peak muscle strains is different among hamstring muscles in sprinting,which may explain the different injury rate among hamstring muscles.

©2017 Production and hosting by Elsevier B.V.on behalf of Shanghai University of Sport.This is an open access article under the CC BY-NC-ND license(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Hamstring flexibility;Hamstring muscle strain injury;Injury risk factor;Muscle biomechanics;Muscle strain;Muscle strain injury

1.Introduction

Hamstring muscle strain injury(hamstring injury)is one of the most common injuries in sports involving sprinting.1–3The high injury and recurrence rates of hamstring injury result in signi ficant time and financial loses and unfortunate consequences.Although tremendous efforts have been made to prevent hamstring injury4,5and improve the rehabilitation of the injury,6the injury and recurrence rates have remained unchanged in the past 3 decades.7,8

Identifying risk factors is critical for effective prevention of hamstring injury and improvement of rehabilitation outcomesof the injury.Although hamstring flexibility is one of the potential risk factors for hamstring injury many studies were focused on,8the results of epidemiologic studies of effects of hamstring flexibility on hamstring injury or re-injury rate were contradictory.9–14A recent systematic literature review with meta-analysis failed to show evidence to support flexibility as a risk factor.15

Many theoretical studies,however,have provided evidences that support hamstring flexibility as a risk factor for hamstring injury.Several animal studies demonstrated muscle strain as the direct cause of muscle strain injury.16–21Muscle strain is de fined as the ratio of muscle length deformation to muscle resting length and can be approximated using muscle optimal length.22,23Alonso et al.24reported that the legs with less flexible hamstring muscles have greater optimal knee flexion angles at which isokinetic knee flexion moment was maximal,indicating that less flexible hamstring muscles have less hamstring optimalmuscle lengths.Our previous study found that hamstring muscle optimal lengths were positively correlated to hamstring flexibility.25These results combined together indicate that hamstring muscles with good flexibility may have lower muscle strains in a given movement such as sprinting and support flexibility as a risk factor for hamstring injury.However,the effect of hamstring flexibility on the peak hamstring muscle strains in sprinting,until this study,remained unknown.

As a continuation of our recent study that showed the relationship between hamstring muscle optimal lengths and hamstring flexibility,the purpose of this study was to examine the relationship of hamstring flexibility with actual peak hamstring muscle strains in sprinting.We hypothesized that peak hamstring muscle strains in sprinting would be negatively correlated to hamstring flexibility.We also hypothesized that peak hamstring muscle strains in sprinting would be positively correlated to hip and knee joint positions at the time of peak muscle strains,which re flects the comprehensive effects of hip flexion and knee extension on hamstring lengths.We further hypothesized that peak hamstring muscle strains in sprinting would be different for different genders.We finally hypothesized that peak hamstring muscle strains in sprinting would be different for different hamstring muscles.The results of this study should provide further theoretical evidence of the role hamstring flexibility plays in hamstring muscle strain injury and set a theoreticalbasisforfuturestudiesonthepreventionand rehabilitation of hamstring as well as other muscle strain injuries.

2.Materials and methods

2.1.Participants

Twenty sports-majored college students(10 males and 10 females)with sprint training experience who regularly participate in exercise and sport and participated in our previous study25volunteered to participate in this study.The activities these subjects are involved in include basketball,soccer, and running.The means±SD of ages,standing heights,and body masses of these participants were 24.6±3.1 years, 173.9±3.3 cm,and 65.9±6.1 kg for male participants and 23.6±0.9 years,163.8±3.8 cm,and 53.5±4.4 kg for female participants,respectively.All participants had no history of hamstring injury or other lower extremity injuries before participating in this study that prevented them from performing the tasks in this study,and each provided written consent before data collection.The study was approved by the Institutional Review Board of Beijing Sport University.

2.2.Protocol

After suf ficient warm-up,each participant underwent a passive straight leg raise(PSLR)test to determine hamstring flexibility bilaterally,a sprinting test to obtain lower extremity kinematic data of both legs in sprinting,and then an isokinetic strength test to determine hamstring muscle optimal lengths bilaterally.In the PSLR test,the participant had 3 trials for each leg as described in our previous study.25The participant laid on the floor in a supine position.The tester raised the participant’s leg with one hand and monitored the pelvis rotation with the other hand placed on the anterior superior iliac spine of the contralateral side.The participant’s leg was raised with a straight knee to a hip flexion angle at which the tester clearly felt the resistance to further hip flexion or a pelvis posterior rotation.The body position with this maximum hip flexion was recorded for each leg.

In the sprinting test,retrore flective markers were placed at the L4-L5 interface and bilaterally at the anterior superior iliac spine;the top of the crista iliac,the lateral and medial femur condyles,the lateral and medial malleolus,the tibial tuberosity; and the center of the second and third metatarsals and the posterior calcaneus.The participant completed 3 acceptable sprinting trials for each leg with maximum effort with a 2 min rest between 2 consecutive trials.An acceptable trial was a trial in which trajectories of all markers were collected in a full running gait cycle.The distance from the starting line and near edge and the center of the motion capture area was 20 m and 25 m,respectively.All participants used a standing start technique to start sprinting.

After the sprinting test,the participant had a bilateral isokinetic strength test in which the markers were remained on the body landmarks and the marker on L4-L5 was removed.The participant was seated on the IsoMed2000 strength-testing system(D&R Ferstl GmbH,Hemau,Germany)with a hip flexion of 90°.The thigh and the lower leg of the testing leg were secured on the seat and the dynamometer arm,respectively,of the strength-testing machine.The participant had 3 isokinetic knee flexion trials at an angular speed of 10°/s with maximum effort for each leg.The detailed setup of the isokinetic strength test was described in our previous study.25

2.3.Data collection

The body position with maximum hip flexion angle in the PSLR test was recorded using a high de finition digital camera (SONY HVR-V1C;Sony Corp.,Tokyo,Japan)with its optical axis perpendicular to the sagittal plane of the participant’s body.The trajectories of the re flective markers in the sprinting test were recorded using a MotionAnalysis videographic acquisition system with 8 cameras(Raptor-4;Motion Analysis Inc., Santa Rosa,CA,USA)at a sample rate of 200 frames per second.The trajectories of the re flective markers in the isokinetic strength test were recorded using a videographic acquisition system(Oqus 400;Qualisys,Gothenburg,Sweden) with 10 video cameras at a sample rate of 100 frames per second.The knee flexion torque data measured by the dynamometer in the strength-testing system were collected using a MegaWin 2.4 system(Mega Electronics Ltd.,Kuopio,Finland) at a sample rate of 100 sample per channel per second,and the videographic and dynamometer data collections were time synchronized by the Qualisys Track Manager computer program package(Version 2.9;Qualisys).

2.4.Data reduction

The maximal hip flexion angle in the PSLR test trail was reduced from the digitized digital photo of the maximal hipflexion angle taken in the PSLR test.The average of the maximal hip flexion angles from 3 PSLR trials was used as the hamstring flexibility score for each leg.The raw threedimensional(3D)trajectories of re flective markers of an isokinetic strength test trial and in a running gait cycle were filtered through a low-pass digital filter at an estimated optimal cutoff frequency of 13 Hz.26Instantaneous locations and orientations of pelvis,thigh,and shank segment reference frames were determined from 3D coordinates of re flective markers. Instantaneous locations of hamstring muscle origins and insertions in the laboratory reference frame were calculated from the local coordinates of the origins and insertions and instantaneous orientations and locations of corresponding segment reference frames.Instantaneous muscle lengths of a given hamstring muscle were determined as instantaneous distances between origin and insertion of the muscle.Detailed descriptions of the calculation of instantaneous muscle lengths can be found elsewhere.25,27,28Muscle optimal length of a hamstring muscle was identi fied as the muscle length corresponding to the calculated peak muscle force of the given hamstring muscle in the isokinetic strength test in which the participant generated the maximal peak hamstring force.Instantaneous force of each hamstring muscle was calculated from instantaneous moment generated by hamstring muscles,physiological cross-sectional areas,and moment arms of hamstring muscles.The detailed calculation of hamstring muscle force was described in detail in our previous study.25

A running gait cycle was de fined as the time period between 2 consecutive foot strikes of the same foot.The time of a foot strike was de fined as the time represented by the first frame in which the vertical coordinate of the heel or toe became a constant.The time of a toe off was de fined as the time represented by the frame immediately after the last frame in which the vertical coordinate of the toe was a constant.The stance phase was de fined as the duration from a foot strike to the subsequent toe off of the same foot,and the swing phase was de fined as the duration from a toe off to the subsequent foot strike of the same foot.Running speed was represented by the averaged horizontal velocity of the L4-L5 marker during a gait cycle.Instantaneous muscle strains(εt)of biarticulated hamstring muscles of the given leg in a gait cycle were calculated from instantaneous muscle lengths(Lt)and optimal lengths(L0)of the corresponding muscles throughout a given gait cycle as

Instantaneous knee joint angles were reduced as the Euler angles of the shank relative to the thigh with an order of rotations of(1) flexion–extension,(2)valgus–varus,and(3) internal–external rotations.Instantaneous hip joint angles were reduced as the Euler angles of thigh related to the pelvis with an order of rotation of(1) flexion–extension,(2)abduction–adduction,and(3)internal–external rotations.Detailed descriptions of joint angle calculations can be found elsewhere.29The hip–knee joint con figuration at the time of peak muscle strains was used to represent hip and knee joint position and de fined as the sum of hip flexion angle and supplementary angle of knee flexion angle at the time of peak muscle strains.

2.5.Data analysis

To test our first 3 hypotheses,linear regression analysis with a dummy variable was performed to determine the relationships of peak muscle strain with flexibility score and hip–knee configuration angle at the time of peak muscle strain for each of the biceps long head,semimembranosus,and semitendinosus.The full regression model was

where y was peak muscle strain;x1was hamstring flexibility score;x2was hip–knee con figuration angle at the time of peak muscle strain;β was the dummy variable representing gender (β=0 for males,β=1 for females);a0to a3were regression coef ficients;and e was the residual.The best regression equation was determined through a backward selection procedure.A regression coef ficient was kept in the regression equation if(1) the contribution of the corresponding term to the regression measured by partial R2was greater than 0.03 and statistically signi ficant and(2)the overall regression is statistically signi ficant.

Two-way analysis of variance(ANOVA)with mixed design were performed to test our fourth hypothesis by determining the effects of muscle and gender on the magnitudes of peak muscle strains,with muscle treated as a repeated measure while gender as independent measure.Turkey’s test was performed as post hoc analysis to locate signi ficant differences when a main effect was signi ficant.All data analyses were performed using SPSS Version16.0(SPSS,Chicago,IL,USA).Statistical signi ficance was de fined as the type I error rate≤0.05.

3.Results

Themeanrunningspeedswere7.97±0.49 m/sand 6.94±0.43 m/s for the male and female participants,respectively.Themeandurationofthestancephasewas 26.54%±2.82%and 27.08%±2.01%for the male and female participants,respectively.The muscle strain–time curves of 3 hamstring muscles reach peaks during the late swing phase (Fig.1).

The best regression equation for the peak muscle strain(y)of biceps long head as a function of flexibility score(x)was

The hip–knee con figuration angle at the time of peak muscle strain and gender were excluded from the regression with contributions to the overall regression as 0.0352(p=0.119)and 0.0242(p=0.190),respectively(Fig.2A).

The best regression equation for the peak muscle strain(y)of semimembranosus as a function of flexibility score(x)was

The hip–knee con figuration angle at the time of peak muscle strain and gender were excluded from the regression withcontributions to the overall regression as 0.0443(p=0.090) and 0.0266(p=0.181),respectively(Fig.2B).

Fig.1.Hamstring muscle strains during the running gait cycle:(A)biceps long headmusclestrain,(B)semimembranosusmusclestrain,and(C) semitendinosus muscle strain.FS=foot strike;TO=toe off.

The best regression equation for the peak muscle strain(y)of semitendinosus as a function of flexibility score(x)was

The hip–knee con figuration angle at the time of peak muscle strain and gender were excluded from the regression with contributions to the overall regression as 0.0161(p=0.335)and 0.0078(p=0.505),respectively(Fig.2C).

The ANOVA showed no signi ficant interaction effect of muscle and gender and no signi ficant main effect of gender on peak muscle strain(p=0.826 and p=0.433),but a signi ficant main effect of muscle on peak muscle strain(p=0.003) (Table 1).Post hoc analyses revealed that the peak muscle strains of biceps long head and semitendinosus were greater than that of semimembranosus(p=0.004)(Table 1).

4.Discussion

Fig.2.The relationship between flexibility score and peak strain of(A)biceps longheadmuscle,(B)semimembranosusmusclestrain,and(C) semitendinosus muscle strain(n=20,data from both legs were included in the results for each participant).

Potential for hamstring muscle strain injury exists during the late swing phase of sprinting.The results of this showed that 3 hamstring muscles had peak muscle strains during the late swing phase.These results are consistent with previous studies that demonstrated that hamstring muscle lengths peaked during the late swing phase of treadmill sprinting27and overground sprinting.28,30As previously studies showed,the direct cause of muscle strain injury is muscle strain during muscleeccentric contraction.16–21The results of this study and previous studies therefore indicate that risk for hamstring muscle injury in sprinting exists during late swing phase.However, previous studies28,30also indicated a potential for hamstring muscle strain injury during the late stance phase because hamstring lengths also peaked during the late stance phase. This difference among previous studies was explained as the difference between treadmill and over-ground running.28The results of current study,however,do not support this explanation.A careful examination of the setups for experiments in current study and the study by Yu et al.28leads to a belief that the participants in the study byYu et al.28might have been still accelerating as the distance between the starting line and the motion capture area was only 10 m.As a recent study showed the anterior tilt angle of the pelvis and the hip flexion angle are increased when accelerating with trunk in a forward lean in comparison to sprinting with a consistent speed with trunk in an upright position.31This angle difference would result in an increased hamstring muscle length deformation during the late stance phase.31

Table 1 Peak muscle strains.

The results of this study support our first hypothesis that peak hamstring muscle strains in sprinting would be negatively correlated to hamstring flexibility.The results showed that hamstring flexibility score had signi ficant contributions to the regressions of peak hamstring muscle strains in sprinting.The best regression equations showed that the greater the flexibility score,the lower the peak hamstring muscle strain.These results support flexibility as a risk factor for hamstring injury in sprinting as previous studies showed that muscle strain was the direct cause of muscle strain injury,regardless of muscle force and strain rate,and that the greater the muscle strain,the higher risk for muscle strain injury.16–21The current results suggest that in sprinting,athletes with good hamstring flexibility have lower peak hamstring muscle strains,which indicate that they may have lower risk for hamstring injury compared to athletes with poor hamstring flexibility.Nevertheless,the results of this study are inconsistent with the results of some epidemiologic studies in which hamstring flexibility did not signi ficantlycontributetothepredictionofhamstringinjury.2,9,11,32,33Possible explanations of those results include small sample size,2,9lack of consideration of the movement type of hamstring injury occurred,9,33small variation in flexibility,33large number of participants with previous hamstring injury,2,9,11,32,33great variation in age,11,32,33and intervention to hamstring flexibility.32Future studies are needed to understand the relationship between hamstring flexibility and strain injury.

The results of this study do not support our second hypothesis that peak hamstring muscle strains in sprinting would be correlated to hip and knee joint con figuration at the time of peak hamstring muscle strains.The results showed that the hip–knee angle at the time of peak muscle strains had no signi ficant contributions to regressions of peak hamstring muscle strains in sprinting.The hip–knee con figuration angle is the sum of hip flexion angle and supplementary angle of knee flexion angle,and represents the overall hip and knee joint angular position that affects hamstring length.Increasing hip flexion or increasing knee extension would increase hamstring muscle lengths and thus increase hamstring strain.The results of this study,however,suggest that differences in peak hamstring strains among participants in sprinting cannot be explained by the difference in hip and knee joint angular position among participants at the time of peak hamstring strains, which is largely due to the similarity of the movement among participants in sprinting.

The effect of hamstring flexibility on peak hamstring muscle strains could be attributed to the effect of hamstring flexibility on hamstring muscle optimal lengths found in our previous study.25As previously described,muscle strain is de fined as the ratio of muscle length deformation to muscle optimal length. Our previous study demonstrated that hamstring muscle optimal lengths were positively correlated to hamstring flexibility.Our current study demonstrated that peak hamstring muscle strains were also correlated to hamstring flexibility,but not to the hip and knee joint con figuration at the time of peak hamstring strains.These results combined together suggest that the effect of hamstring flexibility on peak hamstring muscle strains in sprinting is mainly due to the effect of muscle flexibility on hamstring muscle optimal lengths across participants.

The results of this study do not support our third hypothesis that peak hamstring muscle strains would be different for different genders with the same hamstring flexibility and hip and knee joint con figuration at the time of peak hamstring muscle strains.The results showed that gender had no signi ficant contributions to regressions of peak hamstring muscle strains in sprinting.Our previous study showed that,with the same flexibility score,the hamstring muscle optimal lengths of females were shorter in comparison to males,25which indicated that females might have greater muscle strains in running in comparison to males.The current study,however,showed that this was not true.These results indicate that there should be no difference in the risk for hamstring injury in sprinting between genders in terms of peak hamstring strains in sprinting.This indication,however,is inconsistent with most clinical studies showing that men have higher rates of hamstring injury than women in various sports involving high-speed running.34–36A possible explanation for this disagreement may be that the exercise intensity and fatigue level are different between genders in games and practices.An elevated level of fatigue may result in kinetic and kinematic adjustments in the sprinting mechanics due to decreased muscle strength,37–39which in turn affect the peak hamstring muscle strains.Future studies of genderandfatigueeffectsonpeakhamstringmuscle strains may be needed to con firm the results of this study andunderstand interaction effects of gender and fatigue on peak hamstring muscle strains in sprinting to further understand the gender difference in hamstring injury.

The results of this study support our fourth hypothesis that peak muscle strains of different hamstring muscles would be different in sprinting.The results of this study showed that the peak muscle strains of biceps long head and semitendinosus were greater than that of semimembranosus in sprinting.These results indicate that biceps long head and semitendinosus may be at higher risk for muscle strain injury compared to semimembranosus in sprinting,which is consistent with the results of epidemiologic studies.Epidemiologic studies demonstrated that biceps long head was the most frequently injured muscle among the hamstring muscles.40–42Some studies also showed that the injury rate of semitendinosus was higher than that of semimembranosus,40,41while other studies showed contrary results.43,44

The relationships of hamstring flexibility and peak hamstring muscle strains found in this study are limited as crosssectional relationships.These cross-sectional relationships only suggest that individuals with good hamstring flexibility may have lower peak hamstring muscle strains compared to those with poor flexibility,which does not necessarily mean that improving hamstring flexibility would result in a decrease in peak hamstring muscle strains in sprinting for a given individual.Future longitudinal studies are needed to con firm that the peak hamstring muscle strains of individual athletes can be reduced by improving hamstring muscle flexibility.

5.Conclusion

The potential for hamstring muscle strain injury may exist during the late swing phase of sprinting with constant speed. Peak hamstring muscle strains in sprinting are negatively correlated to hamstring flexibility across individuals.The magnitudes of peak muscle strains are different among hamstring muscles in sprinting,which may explain the different injury rate among hamstring muscles.

Acknowledgment

This research was supported by the National Natural Science Foundation of China(No.81572212)and the Fundamental Research Funds for the Central Universities of China(No. 2016BS013).

Authors’contributions

XW carried out the experiments,performed the data processing and statistical analysis,and drafted the manuscript;BY and HL conceived of the study,participated in its design and coordination,and helped to draft the manuscript;FQ and WEG helped to draft the manuscript.All authors have read and approved the final version of the manuscript,and agree with the order of presentation of the authors.

Competing interests

The authors declare that they have no competing interests.

1.Brooks JH,Fuller CW,Kemp SP,Reddin DB.Incidence,risk,and prevention of hamstring muscle injuries in professional rugby union.Am J Sports Med 2006;34:1297–306.

2.Gabbe BJ,Finch CF,Bennell KL,Wajswelner H.Risk factors for hamstring injuries in community levelAustralian football.Br J Sports Med 2005;39:106–10.

3.Woods C,Hawkins RD,Maltby S,Hulse M,Thomas A,Hodson A.The Football Association Medical Research Programme:an audit of injuries in professional football–analysis of hamstring injuries.Br J Sports Med 2004;38:36–41.

4.Ekstrand J,Hägglund M,Kristenson K,Magnusson H,Waldén M.Fewer ligament injuries but no preventive effect on muscle injuries and severe injuries:an 11-year follow-up of the UEFA Champions League injury study.Br J Sports Med 2013;47:732–7.

5.Bahr R,Thorborg K,Ekstrand J.Evidence-based hamstring injury prevention is not adopted by the majority of Champions League or Norwegian Premier League football teams:the Nordic Hamstring survey. Br J Sports Med 2015;49:1466–71.

6.Ramos GA,Arliani GG,Astur DC,de Castro Pochini A,Ejnisman B, Cohen M.Rehabilitation of hamstring muscle injuries:a literature review. Rev Bras Ortop 2016;52:11–6.

7.Opar DA,Williams MD,Shield AJ.Hamstring strain injuries:factors that lead to injury and re-injury.Sports Med 2012;42:209–26.

8.Liu H,Garrett WE,Moorman CT,Yu B.Injury rate,mechanism,and risk factors of hamstring strain injuries in sports:a review of the literature.J Sport Health Sci 2012;1:92–101.

9.Yeung SS,Suen AM,Yeung EW.A prospective cohort study of hamstring injuries in competitive sprinters:preseason muscle imbalance as a possible risk factor.Br J Sports Med 2009;43:589–94.

10.Bradley PS,Portas MD.The relationship between preseason range of motion and muscle strain injury in elite soccer players.J Strength Cond Res 2007;21:1155–9.

11.Gabbe BJ,Bennell KL,Finch CF,Wajswelner H,Orchard JW.Predictors of hamstring injury at the elite level ofAustralian football.Scand J Med Sci Sports 2006;16:7–13.

12.Henderson G,Barnes CA,Portas MD.Factors associated with increased propensity for hamstring injury in English Premier League soccer players. J Sci Med Sport 2010;13:397–402.

13.Witvrouw E,Danneels L,Asselman P,D’Have T,Cambier D.Muscle flexibility as a risk factor for developing muscle injuries in male professional soccer players.A prospective study.Am J Sports Med 2003;31:41–6.

14.Orchard J,Marsden J,Lord S,Garlick D.Preseason hamstring muscle weaknessassociatedwithhamstringmuscleinjuryin Australian footballers.Am J Sports Med 1997;25:81–5.

15.Freckleton G,Pizzari T.Risk factors for hamstring muscle strain injury in sport:a systematic review and meta-analysis.Br J Sports Med 2013;47:351–8.

16.BestTM,McElhaneyJH,GarrettWJ,MyersBS.Axialstrainmeasurements in skeletal muscle at various strain rates.J Biomech Eng 1995;117:262–5.

17.Brooks SV,Faulkner JA.Severity of contraction-induced injury is affected by velocity only during stretches of large strain.J Appl Physiol 2001;91:661–6.

18.Garrett WE,Safran MR,Seaber AV,Glisson RR,Ribbeck BM. Biomechanical comparison of stimulated and nonstimulated skeletal muscle pulled to failure.Am J Sports Med 1987;15:448–54.

19.Lieber RL,Friden J.Muscle damage is not a function of muscle force but active muscle strain.J Appl Physiol 1993;74:520–6.

20.Lieber RL,Friden J.Mechanisms of muscle injury gleaned from animal models.Am J Phys Med Rehabil 2002;81(Suppl.11):S70–9.

21.Talbot JA,Morgan DL.The effects of stretch parameters on eccentric exercise-induced damage to toad skeletal muscle.J Muscle Res Cell Motil 1998;19:237–45.

22.Kaufman KR,An KN,Litchy WJ,Chao EY.Physiological prediction of muscleforces–II.Applicationtoisokineticexercise.Neuroscience 1991;40:793–804.

23.Hatze H.Estimation of myodynamic parameter values from observations on isometrically contracting muscle groups.Eur J Appl Physiol Occup Physiol 1981;46:325–38.

24.Alonso J,McHugh MP,Mullaney MJ,Tyler TF.Effect of hamstring flexibility on isometric knee flexion angle-torque relationship.Scand J Med Sci Sports 2009;19:252–6.

25.Wan X,Qu F,Garrett WE,Liu H,Yu B.Relationships among hamstring muscle optimal length and hamstring flexibility and strength.J Sport Health Sci 2017;6:275–82.

26.Yu B,Gabriel D,Noble L,An K.Estimate of the optimum cutoff frequency for the Butterworth low-pass digital filter.J Appl Biomech 1999;15: 318–29.

27.Thelen DG,Chumanov ES,Hoerth DM,Best TM,Swanson SC,Li L,et al. Hamstring muscle kinematics during treadmill sprinting.Med Sci Sports Exerc 2005;37:108–14.

28.Yu B,Queen RM,Abbey AN,Liu Y,Moorman CT,Garrett WE. Hamstring muscle kinematics and activation during overground sprinting. J Biomech 2008;41:3121–6.

29.Kadaba MP,Ramakrishnan HK,Wootten ME.Measurement of lower extremity kinematics during level walking.J Orthop Res 1990;8:383–92.

30.Wood G.Biomechanical limitations to sprint running.Med Sci Sports Exerc 1987;25:58–71.

31.Higashihara A,Nagano Y,Takahashi K,Fukubayashi T.Effects of forward trunk lean on hamstring muscle kinematics during sprinting.J Sports Sci 2015;33:1366–75.

32.van Doormaal MC,van der Horst N,Backx FJ,Smits DW,Huisstede BM. No relationship between hamstring flexibility and hamstring injuries in male amateur soccer players:a prospective study.Am J Sports Med 2016;26:434–5.

33.Arnason A,Sigurdsson SB,Gudmundsson A,Holme I,Engebretsen L, Bahr R.Risk factors for injuries in football.Am J Sports Med 2004;32(Suppl.1):S5–16.

34.Cross KM,Gurka KK,Saliba S,Conaway M,Hertel J.Comparison of hamstring strain injury rates between male and female intercollegiate soccer athletes.Am J Sports Med 2013;41:742–8.

35.Dalton SL,Kerr ZY,Dompier TP.Epidemiology of hamstring strains in 25 NCAA Sports in the 2009–2010 to 2013–2014 academic years.Am J Sports Med 2015;43:2671–9.

36.Opar DA,Drezner J,Shield A,Williams M,Webner D,Sennett B,et al. Acute hamstring strain injury in track-and- field athletes:a 3-year observational study at the Penn Relay Carnival.Scand J Med Sci Sports 2014;24:254–9.

37.SmallK,McNaughtonL,GreigM,LovellR.Theeffectsof multidirectional soccer-speci fic fatigue on markers of hamstring injury risk.J Sci Med Sport 2010;13:120–5.

38.Small K,McNaughton L,Greig M,Lovell R.Effect of timing of eccentric hamstring strengthening exercises during soccer training:implications for muscle fatigability.J Strength Cond Res 2009;23:1077–83.

39.Small K,McNaughton LR,Greig M,Lohkamp M,Lovell R.Soccer fatigue,sprintingandhamstringinjuryrisk.IntJSportsMed 2009;30:573–8.

40.De Smet AA,Best TM.MR imaging of the distribution and location of acute hamstring injuries in athletes.AJRAm J Roentgenol 2000;174:393–9.

41.Slavotinek JP,Verrall GM,Fon GT.Hamstring injury in athletes:using MR imaging measurements to compare extent of muscle injury with amountoftimelostfromcompetition.AJRAmJRoentgenol 2002;179:1621–8.

42.Askling CM,Tengvar M,Saartok T,Thorstensson A.Acute first-time hamstring strains during high-speed running:a longitudinal study including clinical and magnetic resonance imaging findings.Am J Sports Med 2007;35:197–206.

43.Koulouris G,Connell D.Evaluation of the hamstring muscle complex following acute injury.Skeletal Radiol 2003;32:582–9.

44.Speer KP,Lohnes Jr J,Garrett WE.Radiographic imaging of muscle strain injury.Am J Sports Med 1993;21:89–95,discussion 96.

1 November 2016;revised 4 February 2017;accepted 28 February 2017

Available online 28 March 2017

Peer review under responsibility of Shanghai University of Sport.

*Corresponding authors.

E-mail addresses:liuhuibupe@163.com(H.Liu);byu@med.unc.edu (B.Yu)

http://dx.doi.org/10.1016/j.jshs.2017.03.012

2095-2546/©2017 Production and hosting by Elsevier B.V.on behalf of Shanghai University of Sport.This is an open access article under the CC BY-NC-ND license(http://creativecommons.org/licenses/by-nc-nd/4.0/).