The effectiveness of different exercises protocols to prevent the incidence of hamstring injury in athletes

Introduction Hamstring strains are the most prevalent non-contact injury associated with participation in sports. In addition to the anatomical and functional characteristics of the hamstrings, such as the biarticular organisation or the dual innervations of biceps femoris, a number of alterable and non-alterable factors have been associated with the risk of hamstring injuries in athletes. Each of these variables would impact upon hamstring injury risk within an integrated approach, by which the possibility of sustaining an injury can vary depending on the particular circumstances of each athlete. The aim of this critical review is to examine the effects of current preventative exercise protocols and to provide basic guidelines for hamstring injury prevention in athletes. Discussion Hamstring injuries occur during high-speed actions or extreme stretching; therefore, in order to prevent the incidence of these types of injuries, specific active lengthening, stretching exercises or sportsspecific drills have been integrated into regular training programmes. The response to these intervention programmes has shown mixed results. A conceptual framework is presented proposing that an effective injury prevention programme should include a combination of different specific and non-specific exercises. In addition, special consideration should be given to those eccentric exercises performed over a large muscle lengths and also emphasise the knee stabilising co-contraction actions of the hamstring. Conclusion The protective effects elicited by a well-designed preventive programme could be obtained in four weeks, with only two sessions per week involving three sets of six to eight repetitions of three openand closed-kinetic chain exercises. Future research should analyse the specific structural and functional modifications elicited by the regular application of different types of exercises and protocols aimed to reduce the risk of hamstring injury. Introduction Hamstring strain, the most prevalent non-contact injury in many team sports 1, refers to any acute physical injury, in the region of the posterior thigh, irrespective of the requirement for medical attention or time lost from sporting activities2. In team sports, such as rugby, football and cricket, the incidence of hamstring injuries has shown an upward trend over the past two decades, and currently represents between 12%–17% of total injuries, with a high rate of recurrence1,3. Several training methods involving eccentric exercises4,5, stretching6 or unstable agility exercises7 have been proposed to prevent the incidence of hamstring injuries. However, there are still some inconsistencies regarding the type of training programmes and their subsequent effects. The lack of uniform criteria for implementing injury prevention exercise programmes could be also associated with the empirical beliefs or unfounded concerns about the low compliance, time required and perceived negative effects, such as excessive hypertrophy, loss of velocity and power8,9. In this critical review, after analysing the functional actions of hamstring and their injury mechanisms, we examine the effects of different exercises used to elicit protective adaptations to potentially reduce the incidence of hamstring injuries in athletes. Additionally, we will address some practical recommendations for integrating an injury prevention programme into the athlete’s per iodised training plan. Discussion In this critical review, the authors have referenced some of their own studies. These referenced studies have been conducted in accordance with the Declaration of Helsinki (1964) and the protocols of these studies have been approved by the relevant ethics committees associated to the institution in which they were performed. All human subjects, in these referenced studies, gave informed consent to participate in the studies. Functional actions of hamstring The biarticular nature of the hamstrings allows them to act simultaneously as hip extensors and knee flexors during concentric contraction or eccentrically during concurrent hip flexion and knee extension, as observed in running and kickin g1. However, the requirements of the hamstrings in terms of force, velocity and power are limited during submaximal or low-speed movements compared to the significantly greater levels occurring in Tr ai ni ng , P er fo rm an ce & Re ha bi lit at io n * Corresponding author Email: f.j.naclerio@gre.ac.uk Centre for Sports Science and Human Performance, School of Science, University of Greenwich at Medway, Central Avenue, Chatham Maritime, Kent, ME4 4TB, United Kingdom Critical review Page 2 of 6 Co m pe ti n g in te re st s: n on e de cl ar ed . C on fl i ct o f I nt er es ts : n on e de cl ar ed . A ll au th or s co nt rib ut ed to th e co nc ep ti o n, d es ig n, a nd p re pa ra ti o n of th e m an us cr ip t, a s w el l a s re ad a nd a pp ro ve d th e fi n al m an us cr ip t. A ll au th or s ab id e by th e A ss oc ia ti o n fo r M ed ic al E th ic s (A M E) e th ic al ru le s of d is cl os ur e. Licensee OA Publishing London 2013. Creative Commons Attribution Licence (CC-BY) FOR CITATION PURPOSES: Naclerio F, Goss-Sampson M. The effectiveness of different exercises protocols to prevent the incidence of hamstring injury in athletes. OA Sports Medicine 2013 Jul 01;1(2):11. the late swing phase of the sprint or an explosive kick10. Such eccentric muscle activity may predispose the hamstrings to injury as the lengthening may exceed the mechanical limits of the muscle or lead to the accumulation of microscopic muscle damage11. In addition, when the hamstrings are considered within a functional kinetic chain, this muscle group appears to be associated with both upper body (pelvis, spine, shoulder and skull) and the lowerlimb alignment and stabilisation (Figure 1)12. These anatomical links may be the reason by which the lack of stability of the back and/or pelvis has been proposed as one of the main contributors to increased risk of hamstring injury12. Additionally, the two heads of the biceps femoris are innervated by different nerve branches of the sciatic nerve, with the tibial portion innervating the long head and the common peroneal branch innervating the short head. This dual innervation could possibly result in uncoordinated contraction and poor motor control leading to an increased rate of hamstring injury observed as fatigue progress during exercises1. Mechanism and localisation of non-contact hamstring injury Hamstring strains occur through an over acute strain episode that could be represented by a continuum from microfibre damage (as seen in association with delayed onset muscle soreness) through a partial strain or complete muscle rupture12. This injury has been strongly associated with high-eccentric muscular tension exceeding the mechanical limits of the tiss ue1. Based on the injury mechanisms and localisation, two types of hamstring injuries have been differentiated as follows: 1. Muscle fibre injuries, mainly in the biceps femoris long head and less often, in the distal semitendinosus muscle, resulting from explosive high-speed actions, such as kicking or sprinting13. 2. Tendon injuries, in particular, the proximal semimembranosus tendon occurring, when performing slow controlled stretching to an extreme position13,14. Potentially, an inter-relationship exists between eccentric force and muscle strain that dictates whether a muscle is injured. For example, the risk of strain injury would be significantly reduced when performing submaximal stretching exercises involving moderate-to-high levels of strain and low eccentric force. Similarly, the risk would be also reduced when controlling a heavy load during the eccentric phase while performing typical resistance exercises, such as bench press or sq uat1. Therefore, when athletes are regularly exposed to activities that simultaneously produce both high-strain and eccentric forces without appropriate preparation, the risk of injury is increased. Potential risks factors associated with hamstring strain in athletes Hamstring injury is a complex and multifactorial phenomena eventually sustained by the interaction of the following two types of fac tors1: 1. Alterable: fatigue, strength deficits, muscular imbalance, optimal peak torque angle, low flexibility, poor motor control or technique. 2. Non-alterable: age, ethnicity, anthropometric relationships, muscular fibre composition and previous injuries. In order to further understand the sequence of events that eventually Figure 1: Hamstring functional kinetic chain connection toward the upper torso and skull as well as to the knee, ankle and foot12. Critical review Page 3 of 6 Co m pe ti n g in te re st s: n on e de cl ar ed . C on fl i ct o f I nt er es ts : n on e de cl ar ed . A ll au th or s co nt rib ut ed to th e co nc ep ti o n, d es ig n, a nd p re pa ra ti o n of th e m an us cr ip t, a s w el l a s re ad a nd a pp ro ve d th e fi n al m an us cr ip t. A ll au th or s ab id e by th e A ss oc ia ti o n fo r M ed ic al E th ic s (A M E) e th ic al ru le s of d is cl os ur e. Licensee OA Publishing London 2013. Creative Commons Attribution Licence (CC-BY) FOR CITATION PURPOSES: Naclerio F, Goss-Sampson M. The effectiveness of different exercises protocols to prevent the incidence of hamstring injury in athletes. OA Sports Medicine 2013 Jul 01;1(2):11. lead to an injury, the causative effects of both alterable and non-alterable factors should be considered within an integrated approach. For example, the combination of age, with the lack of strength would dramatically increase the risk of injury in some athletes8. Therefore, under some circumstances, such as being an older or previously injured athlete, the effects of some modifiable risk factors as the lack of strength or poor motor control will increase the risk of injury with respect to a younger or previously uninjured athlete. A successful hamstring inj


Introduction
Hamstring strain, the most prevalent non-contact injury in many team sports 1 , refers to any acute physical injury, in the region of the posterior thigh, irrespective of the requirement for medical attention or time lost from sporting activities 2 .In team sports, such as rugby, football and cricket, the incidence of hamstring injuries has shown an upward trend over the past two decades, and currently represents between 12%-17% of total injuries, with a high rate of recurrence 1,3 .
Several training methods involving eccentric exercises 4,5 , stretching 6 or unstable agility exercises 7 have been proposed to prevent the incidence of hamstring injuries.However, there are still some inconsistencies regarding the type of training programmes and their subsequent effects.The lack of uniform criteria for implementing injury prevention exercise programmes could be also associated with the empirical beliefs or unfounded concerns about the low compliance, time required and perceived negative effects, such as excessive hypertrophy, loss of velocity and power 8,9 .In this critical review, after analysing the functional actions of hamstring and their injury mechanisms, we examine the effects of different exercises used to elicit protective adaptations to potentially reduce the incidence of hamstring injuries in athletes.Additionally, we will address some practical recommendations for integrating an injury prevention programme into the athlete's per iodised training plan.

Discussion
In this critical review, the authors have referenced some of their own studies.These referenced studies have been conducted in accordance with the Declaration of Helsinki (1964) and the protocols of these studies have been approved by the relevant ethics committees associated to the institution in which they were performed.All human subjects, in these referenced studies, gave informed consent to participate in the studies.

Functional actions of hamstring
The biarticular nature of the hamstrings allows them to act simultaneously as hip extensors and knee flexors during concentric contraction or eccentrically during concurrent hip flexion and knee extension, as observed in running and kickin g 1 .However, the requirements of the hamstrings in terms of force, velocity and power are limited during submaximal or low-speed movements compared to the significantly greater levels occurring in the late swing phase of the sprint or an explosive kick 10 .Such eccentric muscle activity may predispose the hamstrings to injury as the lengthening may exceed the mechanical limits of the muscle or lead to the accumulation of microscopic muscle damage 11 .In addition, when the hamstrings are considered within a functional kinetic chain, this muscle group appears to be associated with both upper body (pelvis, spine, shoulder and skull) and the lowerlimb alignment and stabilisation (Figure 1) 12 .These anatomical links may be the reason by which the lack of stability of the back and/or pelvis has been proposed as one of the main contributors to increased risk of hamstring injury 12 .Additionally, the two heads of the biceps femoris are innervated by different nerve branches of the sciatic nerve, with the tibial portion innervating the long head and the common peroneal branch innervating the short head.This dual innervation could possibly result in uncoordinated contraction and poor motor control leading to an increased rate of hamstring injury observed as fatigue progress during exercises 1 .

Mechanism and localisation of non-contact hamstring injury
Hamstring strains occur through an over acute strain episode that could be represented by a continuum from microfibre damage (as seen in association with delayed onset muscle soreness) through a partial strain or complete muscle rupture 12 .This injury has been strongly associated with high-eccentric muscular tension exceeding the mechanical limits of the tiss ue 1 .Based on the injury mechanisms and localisation, two types of hamstring injuries have been differentiated as follows: 1. Muscle fibre injuries, mainly in the biceps femoris long head and less often, in the distal semitendinosus muscle, resulting from explosive high-speed actions, such as kicking or sprinting 13 .2. Tendon injuries, in particular, the proximal semimembranosus tendon occurring, when performing slow controlled stretching to an extreme position 13,14 .
Potentially, an inter-relationship exists between eccentric force and muscle strain that dictates whether a muscle is injured.For example, the risk of strain injury would be significantly reduced when performing submaximal stretching exercises involving moderate-to-high levels of strain and low eccentric force.Similarly, the risk would be also reduced when controlling a heavy load during the eccentric phase while performing typical resistance exercises, such as bench press or sq uat 1 .Therefore, when athletes are regularly exposed to activities that simultaneously produce both high-strain and eccentric forces without appropriate preparation, the risk of injury is increased.

Potential risks factors associated with hamstring strain in athletes
Hamstring injury is a complex and multifactorial phenomena eventually sustained by the interaction of the following two types of fac tors 1 : 1. Alterable: fatigue, strength deficits, muscular imbalance, optimal peak torque angle, low flexibility, poor motor control or technique.2. Non-alterable: age, ethnicity, anthropometric relationships, muscular fibre composition and previous injuries.
In order to further understand the sequence of events that eventually lead to an injury, the causative effects of both alterable and non-alterable factors should be considered within an integrated approach.For example, the combination of age, with the lack of strength would dramatically increase the risk of injury in some athletes 8 .Therefore, under some circumstances, such as being an older or previously injured athlete, the effects of some modifiable risk factors as the lack of strength or poor motor control will increase the risk of injury with respect to a younger or previously uninjured athlete.
A successful hamstring injury prevention programme would attempt to reduce the negative influence of the alterable risk factors.However, as stated by Opar e t al. 1 , a risk factor cannot be considered causative unless there is a reduction in the rate of hamstring injury following an intervention focused on ameliorating them.The following sections will discuss the effects of the most proposed exercises and protocols for reducing hamstring injuries in athletes.

Stretching exercises
Whilst it has been reported that there is no relationship between static stretching and the risk of hamstring strain 13 , recent reports have suggested positive effects of stretching protocols involving several repetitions of more than 30 s (4 min in total) for reducing muscle strains 6 .In subjects with limited flexibility, it appears that the protective effects of stretching include a shift in the optimal muscle length at which the peak torque occurs towards a more open position i.e., a more extended joint angle 6 .However, caution should be taken when performing stretching exercises as a part of warm up, during and after training because a high volume of excessive hamstring stretching can be the cause of hamstring tendon strains 14 .The risk of this type of injury appears to be even greater after exercise, when a fatigued muscle-tendon complex may be at more risk of damage by extensive stretching 13 .

Active lengthening exercises
Active lengthening occurs when muscles are stretched while trying to contract.Studies suggest 11,15 that the optimum muscle length at which peak tension is recorded would be the best indicator for identifying athletes at risk of hamstring strain.Therefore, the more open the angle at which the optimal peak torque is achieved, the less the muscle will be at risk of injury 15 .
The functional and structural adaptations elicited by eccentric exercises depend on the magnitude of the resistance, movement velocity and amplitude i.e., the magnitude of muscle length achieved throughout the exercise 16 .
In both eccentric and concentric actions, as the magnitude of the resistance increases the capacity to modulate, the velocity decreases.Therefore, when using light to moderate loads (<80% 1 RM), the muscle fibres will progressively be extended during eccentric muscular action.This is the case of some active lengthening movements, such as kicking or the terminal swing of running, where biceps femoris longhead fibres would be extended close to 110% of their original length 1 .However, when using a heavy resistance (>80% 1 RM) throughout an eccentric action, muscle fibres will contract along a quasi-isometric action that is compensated by a greater elongation of the elastic components (tendons and elastic sarcomeric proteins).Thus, as the movement progresses, and the muscle-tendon unit continues to lengthen beyond its optimum length, the tension levels will decrease 17 .Therefore, if we consider that the maximal peak torque occurs always at the same fibre length 17 , the lighter the resistance, the more open the position the optimal peak torque will be produced and conversely, the heavier the resistance, the closer position the optimal peak torque will be localised.
With respect to movement amplitude, it has been demonstrated that the protective effects of eccentric exercises will be only produced over the trained range of motion, but not at longer amplitudes 18 .Thus, if eccentric exercises are performed over short ranges, smaller than those where the injury commonly occurs e.g., the last 30° of terminal swing phase, the optimal peak torque would be moved towards a closer knee angle and therefore, instead of being protective, might even be increasing the risk of hamstring strain.In order to obtain the optimum benefits, eccentric exercises should be conducted throughout the largest possible range of motion.
Different eccentric exercises using a fly wheel eccentric leg curl 19 , Nordic Curl alone 8,20 combined with other strengthening 21 or stretching exercises 21,22 have been successfully applied for reducing the incidence of hamstring injuries, enhancing hamstring eccentric strength 23 or shifting the optimal peak torque in non-previous injured a thletes [24][25][26] .However, the loading patterns and the appropriate training protocols continue to be determined.
Nordic Curls have recently been criticised because of their lack of specificity, with respect to the mechanical action where the injuries occur 16 .This exercise, require athletes, from kneeling position, to gradually lower their trunk, representing about 90% of body weight, towards the ground.For many, not well-conditioned athletes, the overload placed on the hamstrings will be excessive, especially when the trunk approaches the end of the movement.As a consequence, when the athlete is unable to control the movement, they will stop applying force and fall forward.Performing uncontrolled Nordic Curls would not elicit positive adaptations for reducing hamstring Competi ng interests: none declared.Confl ict of Interests: none declared.
All authors contributed to the concepti on, design, and preparati on of the manuscript, as well as read and approved the fi nal manuscript.
All authors abide by the Associati on for Medical Ethics (AME) ethical rules of disclosure.
Licensee strain, because the effective trained range of motion will be restricted to the closer angles (<30° of knee extension) and not transferred to the longer muscle length.In fact, it has been observed that the biceps femoris long head and semimembranosus were significantly less active than the semitendinosus and gracilis during a heavily loaded eccentric leg curl 1 .Therefore, in order to maintain an appropriate activation on the biceps femoris long head and semimembranosus, other alternative exercises, such as the eccentric single or two stiff-legged dead lifts andassisted band Nordic Curl (Figure 2) could be recommended.

Unstable-core and sport specific exercises
An effective injury prevention programme should consider the specific condition that more accurately reflects the situation where injuries occur.In addition, to the active lengthening observed during sprints or kicking, the hamstring acts as knee stabilisers counteracting and balancing the actions of the quadriceps during sportspecific activities, such as landing, deceleration or change of direction.Therefore, specific drills involving, repeated sprints, jumps, hops combined with unstable coreexercises, namely one-leg squat or lunges unstable surfaces have been proposed as effective methods for preventing hamstring injuries 24,27,28 .Verral et al. 28 reported a significant reduction of hamstring injuries in Australian football players after a four-year high-intensity intervaltraining programme combined with passive isometric hamstring stretching.In order to simulate the situation where hamstring strain occurs, athletes were instructed to forward incline the trunk when sprinting.Conversely, Daneshjoo et al. 27 observed no effect of two typically recommended specific injury prevention programmes (FIFA 11 + and Harmo Knee) to enhance hamstring strength in professional football players.More recently, Naclerio et al. 24 reported that four weeks (12 sessions) of an injury prevention programme comprising three sets of eight repetitions of the Nordic curl, forward lunges on a Bosu ® , balance trainer and eccentric single-leg dead lifts was effective in improving the maximal isometric force at both closed (80°) and open (35°) knee angles.Figure 3, depicts the torque-angle profiles determined before (for all participants n = 20) and after the training programme differentiating the training (n = 10) and control group (n = 10).Before training, all participants tended to produce the maximum torque at 45 o ; however, after the training intervention, a plateau from 35°-80° of knee flexion was observed only for the training group that exhibited a more consistent torque, which was maintained over a greater range of knee flexion angles.
The modification depicted in Figure 3 indicates a trend to increase the capacity of the hamstring to apply higher levels of force over a larger range of motion.Possibly, the effects on the knee angle-torque would be manipulated by an appropriate exercise selection.For example, the benefits of performing Nordic Curls would depend on the range of motion achieved during its execution.When performing lunges, a more quasiisometric action of the hamstring will be required and therefore, a predominant strengthening at closer knee angles would be elicited.The single-leg dead lifts involves both an active stretch and a knee stabiliser co-contraction actions of the hamstrings that in turn will be stimulating an strength enhancement of the hamstring at both the closer and the open knee angles positions 24 .

Key point for designing a hamstring injury prevention programme
• The positive effects of a low-volume injury prevention programme could be obtained over a four-week period, with only two sessions per week ivolving three sets of six to eight repetitions of three open and closed kinetic chain exercises 24,25 .
Training, Performance & Rehabilitation Licensee OA Publishing London 2013.Creative Commons Attribution Licence (CC-BY) FOR CITATION PURPOSES: Naclerio F, Goss-Sampson M. The effectiveness of different exercises protocols to prevent the incidence of hamstring injury in athletes.OA Sports Medicine 2013 Jul 01;1(2):11.

Figure 1 :
Figure 1: Hamstring functional kinetic chain connection toward the upper torso and skull as well as to the knee, ankle and foot 12 .
OA Publishing London 2013.Creative Commons Attribution Licence (CC-BY) FOR CITATION PURPOSES: Naclerio F, Goss-Sampson M. The effectiveness of different exercises protocols to prevent the incidence of hamstring injury in athletes.OA Sports Medicine 2013 Jul 01;1(2):11.

Figure 2 :
Figure 2: Three exercises proposed for prevention hamstring injuries in athletes.

Figure 3 :
Figure 3: Torque-knee angle profiles.Solid line depicts the profile obtained from all participants before the training intervention.Dashed and dotted lines, depict the profile obtained from the trained and control groups, respectively after the training intervention (non-published data).