Prevention and rehabilitation of hamstring injuries

Introduction

Hamstring injuries are a major problem in sports. There is especially a high prevalence in athletes who participate in sports that require sprinting, jumping or kicking such as football, rugby, athletics and basketball [1, 2, 3]. Hamstring injuries also have a high propensity for re-injury. One-third of the injuries will recur with the greatest risk during the initial 2 weeks following return to sport [3]. The risk for re-injury remains elevated for at least a year and the subsequent injury is often more severe than the original strain. [4, 5, 6]. In some cases a strained hamstring can cause long-term problems and have a severe impact on a player's career.

The majority of hamstring injuries occur during the late swing phase of running and eighty percent of the hamstring strains affect the long head of the biceps femoris [7, 8]. Architectural and functional differences between the hamstring muscles contribute to the tendency of the biceps femoris to be more often injured than the other muscles. In this article I will also discuss the activation patterns of the hamstring muscles during running and why the hamstrings are at a high risk of injury in sports that require sprinting.

The very high risk to recur in the early phase after returning to sport suggests that most rehabilitation plans are inadequate. To design effective rehabilitation programs several questions need to be posed and answered. What are the risk factors that increase the hamstring injury rate and how the training or rehab plan can have an impact on these risk factors? A previous hamstring strain is probably the most important risk factor for future injury. Which muscle properties are altered following a hamstring strain and why do they put the athlete at a higher risk for recurrence when he returns to play? Which exercise selection and training parameters can help prevent injury or are important in the rehabilitation in order to avoid re-injury?

Architectural characteristics, activation patterns and function

The hamstrings consist of four muscles. The semitendinosus, the semimembranosus and the long head of the biceps femoris are bi-articular and cross the hip and knee joint. The short head of the biceps femoris only spans the knee joint.

Before, the hamstring muscles were considered as one muscle group of which the muscles had similar activation patterns during knee flexion or hip extension. The anatomical characteristics of a muscle are the primary determinants of its function [9, 10]. Architectural differences between the hamstring muscles indicate that each muscle has its inherent function.

The semitendinosus and the short head of the biceps femoris are thin muscles with a lower cross-sectional area and long, parallel-arranged fibres. This makes them more suited to contract over larger distances with high speed and lower force. The long head of the biceps femoris and the semimembranosus on the other hand are bulky muscles with shorter pennate fibres, more suited for high force production [9, 10, 11, 12].

  Local stabiliser Global stabiliser Global mobiliser
Muscle Segmental stabilisation Eccentric lengthening or isometric holding to control range of motion Produce high force or power
semitendinosus  
  • Provide stability to valgus stress at the knee
  • Hip extension
  • Hip internal rotation when the hip is extended
  • Knee flexion
  • Internal knee rotation when the knee is flexed
semimembranosus  
  • Provide dynamic support to the posterior capsule
  • Resist excessive hip abduction
  • Resist external knee rotation
  • Hip extension
  • Hip internal rotation when the hip is extended
  • Knee flexion
  • Internal knee rotation when the knee is flexed
Biceps femoris (long and short head)
  • Force-closure of the sacroiliac joint through its origin at the sacrotuberous ligament (deep longitudinal system)
  • Resist internal knee rotation
  • Resist anterioposterior knee stress
  • Provide stability to varus stress at the knee
  • Hip extension
  • Knee flexion
  • External knee rotation when the knee is flexed
Function of the hamstring muscles

Risk factors

  • Strength imbalances, bilateral asymmetries and fatigue: A large prospective study of professional football players indicates that hamstring/quadriceps imbalances or bilateral assymetries can identify players at higher risk of hamstring strain and that the normalisation of these imbalances significantly reduces hamstring injury rates [13]. A strength imbalance between the hamstrings and quadriceps is the injury risk factor that has been most supported by research [13, 14, 15].
    During sprinting and kicking the hamstrings have to brake the knee extension generated by the quadriceps muscles [16]. Because the quads are stronger than the hamstrings, the hamstrings will become fatigued faster. Strength imbalances between both muscle groups will result in a faster decrease of the eccentric hamstring torque and increase the risk for hamstring strain [13].
  • Fatigue: Hamstring injuries are more likely to occur at the latter stages of a game [2, 17, 18]. Eccentric hamstring strength decreases with playing time. The fatigue effect is also speed dependent. Faster running speeds result in a greater decrease of the peak eccentric hamstring torque [18]. The decreased ability of the hamstring muscles to generate force reduces the energy absorption capacity and predisposes them to strain-type injuries [19]. The activity of the biceps femoris, the muscle in which the vast majority of hamstring strains occur, also progressively increases during each half and markedly the second half [20].

    Time of hamstring strain sustained during a football match [2]
     
  • Core instability: The force and stretch of the iliopsoas during the late stance phase and early swing phase induces an increased anterior tilt of the pelvis. This anterior pelvic tilt results in a greater hamstring stretch of the opposite limb, which is simultaneously in the late swing phase. Increased pelvic tilting when sprinting, due to core instability and compromised pelvic control, results in greater musculotendon stretch and strain of the hamstring muscles during the terminal swing phase [8].
  • Weak or inhibited gluteal muscles: Shirley Sahrmann said, "Any time you see an injured muscle, look for a weak synergist." A synergist is a muscle that performs the same joint motion. Due to delayed gluteus maximus activity, the hamstring muscles become dominant during hip extension, which can cause hamstring strains [21]
    The gluteus maximus and long head of the biceps femoris play an important role in stabilising the pelvis. Pelvic instability can alter the muscle activation timing and the load transfer through the sacro-iliacal joint [22, 23, 24].
  • Lack of proper warm-up: beneficial effects of warm-up, temperature, and stretching on the mechanical properties of muscle. These benefits potentially reduce the risks of strain injury to the muscle [25].

Function of the hamstring muscles during sprinting

The prolonged activity of the hamstrings shows the importance of these muscles for running. EMG recordings have shown that the hamstring muscles are active from mid-swing until the terminal stance phase of running [26, 27, 28, 29, 30, 31, 32]. Most of the hamstring injuries occur during the terminal swing phase [16, 33]. During this phase the knee extends while the hip is in flexion, lengthening the bi-articular hamstrings over both joints they cross. The hamstring muscles lengthen and contract eccentrically to brake the knee extension of the swing leg [16].


During the late swing phase the hamstrings contract eccentrically to brake the knee extension of the swing leg.

Just before foot-strike the hamstrings reach peak force and peak lengths [30, 34, 35, 36, 37, 38]. At high speeds the EMG activity of the hamstring muscles during the terminal swing phase have been shown to exceed the activity of a maximal voluntary contraction [32].

The peak lengths during terminal swing are approximately 10% greater than the hamstring lengths during an upright stance [30, 38]. Because of the differences in hip extension (origin on the pelvis) and knee flexion moment arms (insertion on the tibia), peak lengths are significantly larger in the long head of the biceps femoris, than the semitendinosus and semimembranosus [34]. The greater incurred musculotendon stretch by the biceps femoris may contribute to its tendency to be more often injured than the other 2 hamstring muscles [34].

Peak lengths do not increase significantly with faster sprinting speeds, while hamstring muscle force and power steadily increase with speed [8, 26, 34, 39].


Muscle activity during maximal sprinting speed [26]

Just before foot-strike the hamstrings undergo a stretch-shortening cycle to begin the concentric hip extension contraction that continuous throughout the stance phase. Before, there was hesitation to consider the hamstrings as prime movers during sprinting [40]. The reason for this hesitation is that the hamstrings beside hip extension also flex the knee, while during the stance phase of sprinting knee extension is required [41, 42, 43]. The Lombard paradox shows however that the hamstrings simultaneously perform a hip and knee extension during running [44, 45, 46, 47]. The lower leg is guided during running by foot contact with the ground and the force output of the quads. The hamstrings shorten over the hip joint during hip extension and contract eccentrically around the knee joint to pull the knee backwards into extension.

The hamstrings are active until the end of the stance phase. They are silent from the early swing phase until mid-swing [26, 40].

The way the hamstring muscles function during running explains the high propensity for injury during high-speed running.

How does a hamstring strain-type injury alter the muscles properties and why do these altered properties put the athlete at a higher risk for recurrence?

Previous hamstring injury has been associated with a shifted length-tension curve towards shorter muscle lengths and reduced eccentric hamstring strength towards full knee extension [48]. This indicates that after a hamstring strain the hamstring muscles can produce their greatest force at shorter muscle lengths compared to the pre-injury state. This also means that the end-range strength of the hamstrings is reduced. The presence of scar tissue at the site of the injury might be responsible for the shift of peak torque towards shorter muscle lengths [49]. Scar tissue is less compliant than contractile tissue and can therefore alter the mechanical properties of the muscle [50].

Because the peak force during sprinting occurs at longer muscle lengths, a shifted peak torque towards shorter lengths and reduced end-range strength place the muscle at a higher risk for re-injury [48]. This is probably a major cause of the very high recurrence rate during the first month after returning to play.


Length-tension curve

Another reason for the reduced end range eccentric hamstring strength is a decreased activation of the biceps femoris towards full knee extension [51]. A lot of athletes return to sport with inhibition and selective atrophy of the long head of the biceps [52, 53].

Scar tissue appears as early as 6 weeks after the muscle strain and persists a minimum of 5 months at the site of the injury [52]. Because the scar tissue is less compliant than muscle tissue, extensive scarring requires the muscle fibres in proximity of the scar tissue to lengthen a greater amount to reach the same overall muscle length [50]. Because the muscle region near the scar tissue is subjected to higher strain, re-injuries mostly occur near the site of prior injury. The neuromuscular inhibition is probably a protective mechanism to reduce the risk of re-injury. As a result of the inhibition the majority of athletes return to sport with atrophy, strength deficits and a shifted peak torque towards shorter muscle lengths, which places them at a higher risk for re-injury [54]. The atrophy is not limited to the injured muscle but can also affect the agonist muscles [54]. Sanfilippo et al. showed that the healing and remodelling process continues after return to sport and that the atrophy and strength deficits of the injured leg returned to normal after 6 months [54]. Other studies demonstrate however that the strength abnormalities and scar tissue remodelling and hence an elevated risk of re-injury can persist a lot longer than 6 months after the initial muscle strain [52, 53]. This emphasises the importance of functional loading and progressive rehabilitation programs.

And of course if the initial risk factors that were associated with the first injury are not addressed in the rehabilitation, they will remain to put the athlete at a higher risk of recurrence.

Rehabilitation

The high early re-injury rate following return to sport after hamstring injury indicates that the athletes return prematurely or that most rehabilitation programs are inadequate. Studies have shown that on return to sport the athlete has developed maladaptations that increase the risk of re-injury.

These maladaptations include:

  • reduced eccentric hamstring strength especially towards leg extension [48, 54, 62]
  • inhibition an atrophy of the long head of biceps femoris [51, 52, 53, 54]
  • a shift of the length-tension curve towards shorter muscle lengths [48, 54, 62]

These factors together with the initial risk factors that were associated with the original hamstring injury have to be addressed in the rehabilitation program.

The Nordic hamstring exercise and eccentric hamstring exercises:

Most of the hamstring strains occur in the terminal swing phase, when the hamstrings are contracting eccentrically at peak length [16, 33]. The ratio of eccentric hamstring strength to concentric quadriceps strength has also been shown to be a more accurate way to identify athletes with an increased risk for hamstring injury [13, 14, 15]. Strengthening the hamstring muscles eccentrically in an elongated range of motion should therefore form an important part of rehab or training [48, 55, 56, 57, 58]. Eccentric training has been shown to shift the force-length curve to longer muscle lengths [59, 60, 61, 62, 63]. Sarcomerogenesis, which is the process of adding the number of sarcomeres in series, gradually adapts the optimal muscle length to the zone in which it is operating. Not only eccentric training, but also regular strength training using exercises that are more challenging at lengthened ranges of motion can shift peak torque towards greater muscle lengths [64, 65].


Nordic hamstring exercise

The Nordic hamstring exercise is an eccentric hamstring strengthening exercise that is also more challenging towards a more extended knee position [66]. A Nordic hamstring exercise program has been shown to substantially reduce the incidence of new (60%) and recurrent (85%) hamstring injuries of football players [67]. After only 10 days of eccentric hamstring training a shift of the peak torque towards greater muscle lengths has been detected [48, 60, 61, 62, 65].

The hamstrings function at long lengths during sprinting [16, 33]. Shifting the length-tension curve and increasing the end range strength of the hamstrings counteract the maladaptations following hamstring injury and prevent fibres from reaching a length where they are susceptible to tearing [61].

Static flexibility programs have been shown unable to influence the length-tension relationship and are therefore ineffective to prevent hamstring strains [14]. Because static stretching does not require muscle contraction it is likely unable to positively affect the length-tension curve of the hamstrings in the same way as eccentric strength training.

A number of studies provide evidence that a Nordic exercise program is effective in reducing the risk of hamstring injury and recurrence, as well as improving eccentric hamstring muscle strength and sprint ability [14, 58, 67, 68, 73, 76].

For these reasons mentioned the Nordic hamstring exercise is imperative for football players, sprinters and team sport athletes.

Re-activating the long head of the biceps femoris:

Rehabilitation programs also need to focus on the re-activation of the long head of the biceps femoris muscle to counter the inhibition and atrophy associated with hamstring injury. Because research started to focus only recently on the inherent function of each of the hamstring muscles, there is limited evidence about the activation pattern of the different muscles. The anatomical characteristics of a muscle are the primary determinants of its function, so based on the architecture of the long head of the biceps femoris its function during movement can be derived [9, 10]. It is a thick muscle with a large cross-sectional area and short, pennate fibres, especially suited for high force contractions over a shorter distance [9, 11, 12]. During the stance phase of running the hamstring muscles have to contract forcefully while there is less change in muscle length because of the simultaneous hip and knee extension. This is in accordance with research that revealed the forward lunge, which involves simultaneous knee and hip extension, especially loads the long head of the biceps femoris [69]. Exercises which leg action is similar to the stance phase of running, like a resisted slide-board back lunge, a step-up or a walking lunge can counter the inhibition and atrophy associated with hamstring injury. These exercises also require horizontal force production and contribute to enhanced sprinting performance. On return to sport after hamstring injury, athletes are slower and demonstrate substantially lower horizontal force and power outputs during sprinting [70]. Hip dominant leg exercises that mimic the muscle actions during running should therefore form part of each athlete's rehabilitation plan.

  1. Slide-board back lunge
    Slide-board back lunge
  2. Walking lunge
    Walking lunge

This inability to produce a high level of horizontal force is probably related to the inhibition of the long head of the biceps femoris and stresses the importance of hamstring exercises that mimic the muscle actions during a sprint.

Enhance hamstring strength and endurance:

Strength and endurance of the hamstring muscles play an important role in the prevention of hamstring strain and recurrence. Therefore rehabilitation and training need to emphasise these bio-motor abilities.

Rehabilitation needs to focus on re-establishing adequate strength ratios between the quadriceps and hamstrings. An eccentric hamstring/concentric quadriceps strength ratio superior to 1.0, a concentric hamsting/concentric quadriceps ratio superior to 0.6 and right-left hamstring strength deficit of less than 5% have been associated with a lower risk for hamstring injury [71]. Athletes with strength imbalances have been found to be 4 to 5 times more prone to sustain a hamstring injury compared to athletes with proper strength ratios [71]. Especially the eccentric hamstring to concentric quadriceps ratio gives a good indication of the energy absorption capacity of the hamstring muscles during sprinting. Implementing hamstring strengthening, particularly in the eccentric mode will help normalise strength imbalances and reduce the risk of re-injury.

Because the hamstrings consist of a higher percentage of fast-twitch muscle fibres and co-contract with the stronger quadriceps muscles, they are prone to fatigue. To enhance the capacity of hamstrings to cope with fatigue the volume of hamstring work needs to be increased progressively during rehabilitation. Another possibility to enhance the strength endurance of the hamstring muscles is to perform some regular or eccentric strengthening exercises at the end of the running program or sport-specific training.

Core stability:

Rehab also needs to integrate exercises to promote core stability and develop neuromuscular control. Sherry et al. demonstrated a significant reduction in injury recurrence when the rehabilitation program for acute hamstring strain included core stability exercises [72]. The powerful contraction of the iliopsoas in the stance leg greatly increases the stretch that the hamstrings of the opposite side incur during the terminal swing phase [8]. Enhanced lumbo-pelvic control will better counteract the forces of the iliopsoas and hence reduce the anterior pelvic tilt and stretch of the hamstrings of the swing leg [72].

Re-activating glutes and enhancing intermuscular coordination:

The gluteus maximus is a very powerful hip extensor and also plays an important role in the stabilisation of the lumbo-pelvic region. Pelvic instability, back pain or other lower body injuries can alter the muscle activation timing [22, 23, 24]. The hamstring muscles then become dominant during hip extension as a result of gluteal inhibition or weakness [21]. Hip extension is initiated by the hamstrings and erector spinae while the activation of the gluteus maximus is delayed [22, 23, 24]. The gluteus maximus should be the primary hip extensor. Diminished gluteal function will place a higher load on the hamstrings and increases the risk of hamstring injury. Rehabilitation programs for hamstring injury should focus on restoring proper coordination patterns, consist of exercises that (re-)activate the glutes and enhance the intermuscular coordination between the glutes and hamstrings.

Ballistics:

An adequate rehab program for hamstring injury progressively integrates exercises that are more ballistic in nature [59]. Several studies show that training adaptations are velocity specific and that training adaptations are greatest near the training velocity [74, 75, 76]. The strength and eccentric exercises develop the high force - low speed end of the force-velocity curve, but they do not work the hamstrings near the contraction speeds of sprinting [74, 75, 76]. An acute hamstring strain is a high-velocity injury [8]. Exercises that develop the low force - high speed end of the spectrum will progressively prepare the hamstrings to handle high eccentric loads during the terminal swing phase [74, 75, 76]. Stair bounds, hops, alternate leg bounds will all reinforce hamstring stiffness without placing an excessive eccentric load on the hamstrings during terminal swing [77, 78]. Stiffer hamstring muscles (more compliant) can store more elastic energy during active lengthening, thereby reducing peak muscle stretch and reducing the susceptibility to injury [35]. Ballistic exercises provide a functional eccentric loading and are a good progression towards higher intensity running.

Progressive sprint loading:

An increase in running speed from 80% to 100% effort is associated with a 1.4-fold increase of peak hamstring force during the stance phase and a 1.9-fold increase of energy absorption during the terminal swing phase [8]. This means hamstring load significantly increases during the swing, but not the stance phase [8].

During rehabilitation the volume and intensity of sprinting progressively have to be augmented to prepare the athlete to return to sport. Uphill and resisted sprinting can help to make the transition from 80% to maximal speed. While the effort during uphill and resisted sprinting is maximal, the top speed is lower. The hamstring forces during the stance phase will be equal or slightly elevated compared to regular sprinting, but the amount of energy that has to be absorbed during terminal swing is significantly less. Because the hamstring muscles are especially vulnerable to strain-type injury during the late swing phase, the change of re-injury is less during resisted and uphill maximal sprinting.

References:

  1. [^] Kujala UM, Orava S, Järvinen M. Hamstring injuries. Current trends in treatment and prevention. Sports Med. 1997 Jun;23(6):397-404.
  2. [^ A B C] Woods C, Hawkins RD, Maltby S, Hulse M, Thomas A, Hodson A; Football Association Medical Research Programme. The Football Association Medical Research Programme: an audit of injuries in professional football--analysis of hamstring injuries. Br J Sports Med. 2004 Feb;38(1):36-41.
  3. [^ A B] Orchard J, Seward H. Epidemiology of injuries in the Australian Football League, seasons 1997-2000. Br J Sports Med 2002;36:39-44.
  4. [^] Hagglund M, Walden M, Ekstrand J. Previous injury as a risk factor for injury in elite football: a prospective study over two consecutive seasons. Br J Sports Med 2006;40:767-72.
  5. [^] Gabbe BJ, Bennell KL, Finch CF, et al. Predictors of hamstring injury at the elite level of Australian football. Scand J Med Sci Sports 2006;16:7-13.
  6. [^] Warren P, Gabbe BJ, Schneider-Kolsky M, et al. Clinical predictors of time to return to competition and of recurrence following hamstring strain in elite Australian footballers. Br J Sports Med 2010;44:415-19.
  7. [^] Koulouris G, Connell D. Evaluation of the hamstring muscle complex following acute injury. Skeletal Radiol. 2003;32:582-589.
  8. [^ A B C D E F G] Chumanov ES, Heiderscheit BC, Thelen DG. The effect of speed and influence of individual muscles on hamstring mechanics during the swing phase of sprinting. J Biomech 2007;40:3555-62.
  9. [^ A B C D] Lieber RL, Bodine-Fowler SC. Skeletal muscle mechanics: implications for rehabilitation. Phys Ther. 1993; 73(12): 844-856.
  10. [^ A B C] Lieber RL, Friden J. Functional and clinical significance of skeletal muscle architecture. Muscle Nerve. 2000; 23(11): 1647-1666.
  11. [^ A B] Kellis E, Galanis N, Kapetanos G, Natsis K. Architectural differences between the hamstring muscles. J Electromyogr Kinesiol. 2012 Aug;22(4):520-6.
  12. [^ A B] Makihara Y, Nishino A, Fukubayashi T, Kanamori A. Decrease of knee flexion torque in patients with ACL reconstruction: combined analysis of the architecture and function of the knee flexor muscles. Knee Surg Sports Traumatol Arthrosc. 2006; 14(4): 310-317.
  13. [^ A B C D] Croisier JL, Ganteaume S, Binet J, Genty M, Ferret JM. Strength imbalances and prevention of hamstring injury in professional soccer players: a prospective study. Am J Sports Med. 2008;36:1469-1475.
  14. [^ A B C D] Arnason A, Andersen TE, Holme I, Engebretsen L, Bahr R. Prevention of hamstring strains in elite soccer: an intervention study. Scand J Med Sci Sports. 2008;18:40-48.
  15. [^ A B] 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.
  16. [^ A B C D E] Chumanov ES, Schache AG, Heiderscheit BC, et al. Hamstrings are most susceptible to injury during the late swing phase of sprinting. Br J Sports Med 2012;46:90.
  17. [^] Ekstrand J, Hagglund M, Walden M. Injury incidence and injury patterns in professional football: the UEFA injury study. Br J Sports Med 2011;45:553-8.
  18. [^ A B] Greig M, Siegler JC. Soccer-specific fatigue and eccentric hamstrings muscle strength. J Athl Train 2009;44:180-4.
  19. [^] Garrett WE. Muscle strain injuries: clinical and basic aspects. Med Sci Sports Exerc1990;22:436-43.
  20. [^] Greig M.P, McNaughton L.R, Lovell R.J. Physiological and mechanical response to soccer-specific intermittent activity and steady-state activity. Res Sports Med. 2006;14(1):29-52.
  21. [^ A B] Shirley Sahrmann, Diagnosis and treatment of movement impairment syndromes, Mosby, 2002.
  22. [^ A B C] 22. Leinonen V, Kankaapää M, Airaksinen O and Hanninen O (2000): Back and hip extensor activities during trunk flexion/extension: effects of low back pain and rehabilitation. Archives of Physical Medical Rehabilitation 81, 32-37.
  23. [^ A B C] Nelson-Wong E, Alex B, Csepe D, Lancaster D, Callaghan JP. Altered muscle recruitment during extension from trunk flexion in low back pain developers. Clin Biomech 27(10):994-8, 2012.
  24. [^ A B C] Janda V (1985) Pain in the locomotor system - A broad approach. In Glasgow et al. (eds.) Aspects of Manipulative Therapy. Churchill Livingstone: 148-151.
  25. [^] Garrett WE., Jr Muscle strain injuries. Am J Sports Med. 1996;24:S2-8.
  26. [^ A B C D] Chumanov ES, Heiderscheit BC, Thelen DG. Hamstring musculotendon dynamics during stance and swing phases of high-speed running. Med Sci Sports Exerc2011;43:525-32.
  27. [^] Higashihara A, Ono T, Kubota J, Okuwaki T, Fukubayashi T. Functional differences in the activity of the hamstring muscles with increasing running speed. J Sports Sci. 2010;28:1085-92.
  28. [^] Jonhagen S, Ericson MO, Nemeth G, Eriksson E. Amplitude and timing of electromyographic activity during sprinting. Scand J Med Sci Sports. 1996;6:15-21.
  29. [^] Kyrolainen H, Avela J, Komi PV. Changes in muscle activity with increasing running speed J Sports Sci. 2005;23:1101-9.
  30. [^ A B C] Simonsen EB, Thomsen L, Klausen K. Activity of mono- and biarticular leg muscles during sprint running.Eur J Appl Physiol Occup Physiol. 1985;54:524-32.
  31. [^] 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.
  32. [^ A B] Kyrolainen H, Komi PV, Belli A. Changes in muscle activity patterns and kinetics with increasing running speed J Strength Cond Res. 1999;13:400-6.
  33. [^ A B C] Petersen J, Hölmich P. Evidence based prevention of hamstring injuries in sport. Br J Sports Med. 2005 Jun;39(6):319-23.
  34. [^ A B C D] Thelen DG, Chumanov ES, Hoerth DM, et al. Hamstring muscle kinematics during treadmill sprinting. Med Sci Sports Exerc 2005;37:108-14.
  35. [^ A B] Thelen DG, Chumanov ES, Best TM, Swanson SC, Heiderscheit BC. Simulation of biceps femoris musculotendon mechanics during the swing phase of sprinting. Med Sci Sports Exerc. 2005; 37(11):1911-8.
  36. [^] Wood GA. Biomechanical limitations to sprint running. In: Van Gheluwe B, Atha J, editors. Current Research in Sports Biomechanics. Basel (Switzerland): Karger; 1987. p. 58-71.
  37. [^] Yamaguchi GT, Zajac FE. A planar model of the knee joint to characterise the knee extensor mechanism. J Biomech. 1989;22:1-10.
  38. [^ A B] Schache AG, Wrigley TV, Baker R, Pandy MG. Biomechanical response to hamstring muscle strain injury. Gait Posture. 2009; 29:332-8.
  39. [^] Schache AG, Kim HJ, Morgan DL, et al. Hamstring muscle forces prior to and immediately following an acute sprinting-related muscle strain injury. Gait Posture 2010;32:136-40.
  40. [^ A B] Mero, A, Komi, P.V. Electromyographic activity in sprinting at speeds ranging from sub-maximal to supra-maximal. Medicine and Science in Sports and Exercise 1987; 19, 3, pp. 266-274.
  41. [^] Bober T, Mularczyk W. et al (1990): The mechanics of the leg swing in running. Techniques in Athletics, Cologne, 7-9 June 1990 Conference proceedings, Vol. 2, pp. 507-510.
  42. [^] McClay LS, Lake M.J, Cavanagh P.R. (1990): Muscle activity in running. Cavanagh, P.R. (Hrsg.): Biomechanics of Distance Running. Chapter 6, pp. 165-186.
  43. [^] Wood, G.A. Optimal performance criteria and limiting factors in sprint running. New Studies in Athletics 1986; 2, pp. SS-63.
  44. [^] Wiemann K and Tidow G. Relative activity of hip and knee extensors in sprinting - Implications for training. New Studies in Athletics 10(1): 29-49, 1995.
  45. [^] Molbech S. (1965): On the paradoxical effect of some two-joint muscles. Acta Morphologica Neerlando-Scandinavica 6, pp. 171-178.
  46. [^] Fischer K. (1927): Zur geführten Wirkung mehrgelenkiger Muskeln. Zeitschrift fur Anatomie and Entwicklungsgeschichte 83, pp. 7S2ff.
  47. [^] Andrews J.G. (1985): A general method for determining the functional role of a muscle. Journal of Biomechanical Engineering 107, pp. 348-353.
  48. [^ A B C D E F] Brockett CL, Morgan DL, Porske U. Predicting hamstring strain injury in elite athletes. Med Sci Sports Exerc. 2004;36(3):379-87.
  49. [^] Kaariainen M, Jarvinen T, Jarvinen M, Rantanen J, Kalimo H. Relation between myofibers and connective tissue during muscle injury repair. Scand J Med Sci Sports. 2000;10:332-337.
  50. [^ A B] Butler DL, Juncosa N, Dressler MR. Functional efficacy of tendon repair processes. Annu Rev Biomed Eng. 2004;6:303-329.
  51. [^ A B] Sole G, Milosavljevic S, Nicholson HD, et al. Selective strength loss and decreased muscle activity in hamstring injury. J Orthop Sports Phys Ther 2011;41:354-63.
  52. [^ A B C D] Silder A, Heiderscheit BC, Thelen DG, Enright T, Tuite MJ. MR observations of long-term musculotendon remodeling following a hamstring strain injury. Skeletal Radiol. 2008;37:1101-1109.
  53. [^ A B C] Croisier J, Forthomme B, Namurois M, Vanderthommen M, Crielaard J. Hamstring muscle strain recurrence and strength performance disorders. Am J Sports Med. 2002;30(2):199-203.
  54. [^ A B C D E F] Sanfilippo, J. L., A. Silder, M. A. Sherry, M. J. Tuite, and B. C. Heiderscheit. Hamstring Strength and Morphology Progression after Return to Sport from Injury. Med. Sci. Sports Exerc., Vol. 45, No. 3, pp. 448-454, 2013.
  55. [^] Arason A, Andersen TE, Holme I, et al. Prevention of hamstring strains in elite soccer: an intervention study. Scand J Med Sci 2008; 18:40-48.
  56. [^] Askling C, Karlsson J, Thorstensson A. A hamstring injury occurence in elite soccer players after preseason training with eccentric overload. Scand J Med Sci 2003; 13: 244-50.
  57. [^] Gabbe BL, Branson R, Bennel KL. A pilot randomised controlled trial of eccentric exercise to prevent hamstring injuries in community-level Australian football. J Sci Med Sport 2006; 9: 103-09.
  58. [^ A B] Petersen J, Thorborg K, Bachmann M, et al. Preventive Effect of Eccentric Training on Acute Hamstring Injuries in Men's Soccer: A cluster-Randomized Controlled Trial. Am J Sports Med 2011; 39: 2296-2303.
  59. [^ A B] Schmitt B, Tim T, McHugh M. Hamstring injury rehabilitation and prevention of reinjury using lengthened state eccentric training: a new concept. Int J Sports Phys Ther. 2012 Jun;7(3):333-41.
  60. [^ A B] Brockett CL, Morgan DL, Proske U. Human hamstring muscles adapt to eccentric exercise by changing optimum length. Med Sci Sports Exerc 2001;33:783-90.
  61. [^ A B C] Brughelli M, Cronin J, Mendiguchia J, et al. Contralateral leg deficits in kinetic and kinematic variables during running in Australian rules football players with previous hamstring injuries. J Strength Cond Res 2010;24:2539-44.
  62. [^ A B C D] Brughelli M, Nosaka K, Cronin J. Application of eccentric exercise on an Australian Rules football player with recurrent hamstring injuries. Phys Ther Sport 2009;10:75-80.
  63. [^] Kilgallon M, Donnelly AE, Shafat A. Progressive resistance training temporarily alters hamstring torque-angle relationship. Scand J Med Sci Sports 2007;17:18-24.
  64. [^] Goldspink G. Changes in muscle mass and phenotype and the expression of autocrine and systemic growth factors by muscle in response to stretch and overload. J Anat 194: 323-334, 1999.
  65. [^ A B] Seynnes OR, de Boer M, Narici MV, Early skeletal muscle hypertrophy and architectural changes in response to high-intensity resistance training. J Appl Physiol 2007; 102:368-373.
  66. [^] Iga J, Fruer CS, Deighan M, Croix MD, James DV. 'Nordic' hamstrings exercise - engagement characteristics and training responses. Int J Sports Med. 2012 Dec;33(12).
  67. [^ A B] Thorborg K. Why hamstring eccentrics are hamstring essentials. Br J Sports Med 2012;46:463-5.
  68. [^] Mjølsnes R, Arnason A, Østhagen T, Raastad T, Bahr R. A 10-week randomized trial comparing eccentric vs. concentric hamstring strength training in well-trained soccer players. Scand J Med Sci Sports. 2004 Oct;14(5):311-7.
  69. [^] Mendiguchia J, Garrues MA, Cronin JB, Contreras B, Los Arcos A, Malliaropoulos N, Maffulli N, Idoate F. Nonuniform changes in MRI measurements of the thigh muscles after two hamstring strengthening exercises. J Strength Cond Res. 2013 Mar;27(3):574-81.
  70. [^] Mendiguchia J, Samozino P, Martinez-Ruiz E, Brughelli M, Schmikli S, Morin JB, Mendez-Villanueva A. Progression of Mechanical Properties during On-field Sprint Running after Returning to Sports from a Hamstring Muscle Injury in Soccer Players. Int J Sports Med. 2014 Jan 14.
  71. [^ A B] Croisier JL, Ganteaume S, Binet J, et al. Strength imbalances and prevention of hamstring injury in professional soccer players: a prospective study. Am J Sports Med 2008;36:1469-75.
  72. [^ A B] Sherry MA, Best TM. A comparison of 2 rehabilitation programs in the treatment of acute hamstring strains. J Orthop Sports Phys Ther. 2004;34:116-125.
  73. [^] Askling C, Karlsson J, Thorstensson A. A hamstring injury occurence in elite soccer players after preseason training with eccentric overload. Scand J Med Sci 2003; 13: 244-50.
  74. [^ A B C] McBride, J.M.,T. Triplett-McBride, A.Davie, R.U. Newton, The effect of heavy- vs. light-load jump squats on the development of strength, power, and speed. J. Strength Cond. Res. 16:75-82. 2002.
  75. [^ A B C] Mero, A, P V Komi, Force-, EMG-, and elasticity-velocity relationships at submaximal, maximal and supramaximal running speeds in sprinters. Eur. J. Appl. Physiol. 55:553-561. 1986.
  76. [^ A B C] Häkkinen K, P V Komi, Effect of explosive-type strength training on electromyographic and force production characteristics of leg extensor muscles during concentric and various stretch-shortening cycle exercises. Scand. J. Sports Sci. 7:65-76. 1985a.
  77. [^] Cormie P, McGuigan MR, Newton RU. Developing maximal neuromuscular power: Part 1--biological basis of maximal power production. Sports Med. 2011 Jan 1;41(1):17-38.
  78. [^] Cormie P, McGuigan MR, Newton RU. Changes in the eccentric phase contribute to improved stretch-shorten cycle performance after training. Med Sci Sports Exerc. 2010 Sep;42(9):1731-44.